research proposal on reproductive health

Click through the PLOS taxonomy to find articles in your field.

For more information about PLOS Subject Areas, click here .

Loading metrics

Open Access

Peer-reviewed

Research Article

Evaluating the effectiveness of sexual and reproductive health services during humanitarian crises: A systematic review

Roles Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Writing – original draft, Writing – review & editing

* E-mail: [email protected]

Affiliations Health in Humanitarian Crises Centre, London School of Hygiene & Tropical Medicine, London, United Kingdom, Centre for Maternal, Adolescent, Reproductive and Child Health (MARCH), London School of Hygiene & Tropical Medicine, London, United Kingdom

Roles Formal analysis, Writing – original draft, Writing – review & editing

Affiliation Health in Humanitarian Crises Centre, London School of Hygiene & Tropical Medicine, London, United Kingdom

Roles Conceptualization, Formal analysis, Writing – review & editing

Affiliation Centre for Maternal, Adolescent, Reproductive and Child Health (MARCH), London School of Hygiene & Tropical Medicine, London, United Kingdom

Roles Conceptualization, Funding acquisition, Methodology, Writing – review & editing

Affiliation Department of Reproductive Health and Research, World Health Organization, Geneva, Switzerland

Roles Conceptualization, Funding acquisition, Writing – review & editing

• Neha S. Singh, 
• James Smith, 
• Sarindi Aryasinghe, 
• Rajat Khosla, 
• Lale Say, 
• Karl Blanchet

• Published: July 6, 2018
• https://doi.org/10.1371/journal.pone.0199300
• Reader Comments

An estimated 32 million women and girls of reproductive age living in emergency situations, all of whom require sexual and reproductive health (SRH) information and services. This systematic review assessed the effect of SRH interventions, including the Minimum Initial Service Package (MISP) on a range of health outcomes from the onset of emergencies.

Methods and findings

We searched EMBASE, Global Health, MEDLINE and PsychINFO databases from January 1, 1980 to April 10, 2017. This review was registered with the PROSPERO database with identifier number CRD42017082102. We found 29 studies meet the inclusion criteria. We found high quality evidence to support the effectiveness of specific SRH interventions, such as home visits and peer-led educational and counselling, training of lower-level health care providers, community health workers (CHWs) to promote SRH services, a three-tiered network of health workers providing reproductive and maternal health services, integration of HIV and SRH services, and men’s discussion groups for reducing intimate partner violence. We found moderate quality evidence to support transport-based referral systems, community-based SRH education, CHW delivery of injectable contraceptives, wider literacy programmes, and birth preparedness interventions. No studies reported interventions related to fistulae, and only one study focused on abortion services.

Conclusions

Despite increased attention to SRH in humanitarian crises, the sector has made little progress in advancing the evidence base for the effectiveness of SRH interventions, including the MISP, in crisis settings. A greater quantity and quality of more timely research is needed to ascertain the effectiveness of delivering SRH interventions in a variety of humanitarian crises.

Citation: Singh NS, Smith J, Aryasinghe S, Khosla R, Say L, Blanchet K (2018) Evaluating the effectiveness of sexual and reproductive health services during humanitarian crises: A systematic review. PLoS ONE 13(7): e0199300. https://doi.org/10.1371/journal.pone.0199300

Editor: Ines Keygnaert, Ghent University, BELGIUM

Received: January 3, 2018; Accepted: June 5, 2018; Published: July 6, 2018

Copyright: © 2018 Singh et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are available in Table 2 included within the paper. Additionally, all included papers in the systematic review are available on the websites of the journals in which they were published.

Funding: This work was funded with support from the Department of Reproductive Health & Research, World Health Organization (to Karl Blanchet). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

The World Health Organisation defines health emergencies as sudden-onset events from naturally occurring or man-made hazards, or gradually deteriorating situations through which the risk to public health steadily increases over time.[ 1 ] It is estimated that 1 billion, or about 14% of the world’s population, live in areas affected by conflict.[ 2 ] According to the United Nations High Commissioner for Refugees, the number of forcibly displaced people has nearly doubled in the past two decades (from 33.9 million in 1997 to 65.6 million in 2016), with numbers remaining at a record high.[ 3 ] Given the changing nature of conflict and protracted crises, the average time spent in displacement has now reached 20 years.[ 3 ] The United Nations Population Fund estimates that of the more than 100 million people in need of humanitarian assistance in 2015, 32 million were women and girls aged 15–49 years.[ 4 ]

Women and girls are disproportionately affected in both sudden and protracted emergencies,[ 5 ] and face multiple sexual and reproductive health (SRH) challenges in conflict and post-conflict settings.[ 6 ] Inadequate or interrupted access to SRH services can also increase the number of people affected, generating a high risk of: mortality or morbidity due to pregnancy-related causes; unintended or unwanted pregnancies due to lack of information or access to contraceptive services; complications related to unsafe abortions; sexual and gender-based violence (SGBV); and an increased incidence of sexually transmitted infections (STIs), including HIV.[ 7 , 8 ] These challenges limit women’s empowerment and their participation in the recovery process, resulting in violations of their human rights, and a reduction in the resources available to alleviate suffering and to be directed towards the process of recovery. Furthermore, there is an economic case for investing in SRH services in humanitarian crises settings, which face financial and other constraints, as it is estimated that for each additional $1 US dollar spent on contraceptive services above the current level of funding in crisis settings, the cost of maternal and newborn health-related care would be reduced by $2.22.[ 4 ]

Over the past two decades, there has been increased attention to SRH in populations in humanitarian settings. In 1994, the importance of refugees’ rights to SRH were articulated and globally agreed in Chapter X of the proceedings of the International Conference on Population and Development in Cairo.[ 9 ] In 1995, the growing awareness of, and commitment to, addressing emergency SRH needs culminated in the formation of the Inter-Agency Working Group (IAWG) on Reproductive Health in Crises, tasked with promoting access to quality SRH care among women and other vulnerable populations impacted by humanitarian crises.[ 10 ] In 1999, the IAWG developed a field manual to provide guidance to field staff on reproductive health interventions in emergencies, and included a chapter on the Minimum Initial Service Package (MISP), to be implemented within 48 hours of the onset of every humanitarian crisis. The MISP aims to facilitate the coordination of SRH services, prevent and manage the consequences of sexual violence, reduce HIV transmission, minimise maternal and neonatal morbidity and mortality, and plan for comprehensive SRH services in the post-crisis phase.

Despite increasing attention to SRH in humanitarian settings, recent evaluations of the MISP have been mixed.[ 11 , 12 ] A systematic review in 2015 [ 13 ] found no peer-reviewed papers that evaluated MISP implementation comprehensively since the first global evaluation in 2004, which identified a low awareness among health actors, and no systematic implementation of the MISP.[ 14 ] The literature is even sparser for studies assessing the effectiveness of SRH interventions including the MISP in humanitarian crises.[ 13 , 15 , 16 ] The only systematic review conducted to date to assess the effectiveness of SRH interventions in humanitarian settings reported a low quantity and quality of evidence, but notably did not comprehensively search for studies focusing on abortion, or aim to disaggregate data by vulnerable sub-populations, e.g. adolescents.[ 15 ]

To build upon progress made and to address evidence gaps, we aimed to consolidate the existing evidence base for the effectiveness of SRH interventions including the MISP from the onset of emergencies by conducting a broader systematic review. Our systematic review aimed to assess the effect of SRH interventions including the MISP and its components reported in the peer-reviewed literature between 1980 and 2017 on a range of health outcomes from the onset of emergencies. As part of this objective, we also aimed to assess issues related to targeting of SRH interventions including the MISP, e.g. whether they are delivered to vulnerable populations such as those with disabilities, sex workers, adolescent girls, and lesbian, gay, transsexual, queer and intersex (LGBTQI) populations.

This systematic literature review adhered to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement ( S1 Appendix ).[ 17 ] The review was registered with the PROSPERO database with identifier number CRD42017082102. The inclusion and exclusion criteria are detailed in Table 1 .

• PPT PowerPoint slide
• PNG larger image
• TIFF original image

https://doi.org/10.1371/journal.pone.0199300.t001

Search strategy and selection criteria

Search terms for SRH were based on the definition of SRH from the International Conference on Population and Development in 1994 [ 9 ] and from the World Health Organisation’s SRH strategies and guidance in 2010 [ 18 ] and 2017 [ 19 ]. SRH refers to a state of physical, emotional, mental and social well-being in relation to sexuality and reproductive health; it is not merely the absence of disease, dysfunction or infirmity. [ 4 , 18 ] International guidelines on SRH in conflict-affected settings include activities related to family planning, abortion, HIV/AIDS and STIs including PMTCT, maternal and newborn health, and SGBV.[ 20 ]

We defined a humanitarian crisis as a serious disruption of the functioning of a community or a society causing widespread human, material, economic or environmental losses that exceed the ability of the affected community or society to cope using its own resources, necessitating a request to the national or international level for external assistance. The crisis situation may either be man-made (e.g. armed conflict) or a natural phenomenon (e.g. drought). Only studies from low-income or middle-income countries were included in this study, as the majority of humanitarian crises occur in these countries, and the resources and strategies available to address them are very different in high-income countries.

A detailed protocol with specific search terms are provided in S2 Appendix , and were generated by the authors and then supplemented by searching for other search strategies used in previous systematic reviews on similar topics.[ 21 , 22 ] We also consulted a trained information science and Cochrane review specialist at the London School of Hygiene and Tropical Medicine to review our literature searching syntax and strategy.

We included studies from peer-reviewed journals across the following four databases: EMBASE, Global Health, MEDLINE and PsychINFO. We complemented searches by screening the reference lists of papers for potentially relevant studies, as well as reference lists of relevant systematic reviews. We also consulted experts on SRH service delivery and research to identify additional research not identified during our systematic search (see Acknowledgments section for list of experts). Selection criteria for literature are detailed in Table 1 .

Data analysis

We downloaded all returned citations from the searched databases into an Endnote library and applied a standard data-screening process ( Fig 1 ). We based the primary and secondary outcomes of interest for inclusion from the IAWG field manual, 14 as it is an established and widely used manual for SRH in crisis-affected settings, and was selected based on discussion with the SRH expert committee. Inclusion and exclusion criteria applied during screening are outlined in Table 1 . Data from the final selected studies were then extracted into a Microsoft Excel database, with data extraction fields including study author and year, setting, crisis type, crisis stage, study design and methods, research setting, health outcomes and intervention descriptions. First round data screening and extraction were independently conducted by NSS, JS and SA. Second round detailed data extraction was conducted independently and in duplicate by NSS and JS.

https://doi.org/10.1371/journal.pone.0199300.g001

We used a narrative synthesis approach due to the heterogeneity of study outcomes, interventions and methods. Findings were synthesised by main SRH outcomes including those included in an earlier systematic review by Warren et al. on SRH interventions in humanitarian settings [ 15 ] i.e. family planning; abortion; prevention, treatment, and care for STIs including HIV/AIDS; maternal, newborn and child health, including obstetric care; SGBV; and studies with cross-cutting SRH themes. These themes were developed iteratively after thematic analysis of the studies’ stated aims and primary reported health outcome of interest.

The quality of reporting in the included studies were assessed using the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) and Consolidated Standards of Reporting Trials (CONSORT) checklists,[ 23 , 24 ] which are commonly used for reporting the quality of observational studies and randomised controlled trials. Both checklists include measures regarding the reporting of participant selection, sample sizes, variables, data sources, bias, descriptive and outcome data, interpretation, and generalisability, among others. In order to further explore the quality of reporting, we awarded papers one point for reporting each of the items on the relevant checklist. When totalled, these points formed the numerator of a proportional score, with the denominator the total number of possible relevant checklist items which varied slightly by study type, i.e. 22 total points for the STROBE checklist, and 25 total points for the CONSORT checklist. NSS, JS and SA conducted quality assessment, who each independently evaluated the quality of all included studies and discussed each discrepancy until consensus was reached. For this systematic review, the study team determined a priori that papers with a score of <33% were considered low reporting quality, moderate quality if 34–66%, and high quality if >67%. These quality thresholds have been used in a previous systematic review on SRH in humanitarian crises settings.[ 22 ]

A total of 14,510 citations were returned from peer-reviewed databases, with one additional study provided by expert recommendation ( Fig 1 ). Following full screening, the review of reference lists, and a review of two existing systematic reviews on similar topics, [ 13 , 15 ] a total of 29 studies met the inclusion criteria ( Table 2 ).

https://doi.org/10.1371/journal.pone.0199300.t002

Of the 29 included studies, 23 (79.3%) were published during the last decade between January 2007 and March 2017. In relation to the geographical distribution of the studies, 17 studies (58.6%) were conducted in Africa, a further nine studies (31.0%) in Asia, one study was conducted in Haiti (3.4%) while the remaining two studies (6.9%) both comprised sites in multiple countries. In relation to the typology of humanitarian crisis, 24 studies (82.8%) were conducted in areas affected by armed conflict, and the two multi-site studies (6.9%) were conducted in areas affected by both armed conflict and natural disasters. The remaining three studies (10.3%) were conducted in areas affected by a natural disaster: the first study focused on the 2005 earthquake in northern Pakistan; the second study focused on the 2013 Typhoon Haiyan in the Philippines; and the third study was conducted in the aftermath of the 2010 earthquake in Haiti.

Of the included studies, over a third (34.5%, n = 10) examined the effectiveness of interventions relating to pregnancy and maternal and newborn health (MNH). Six studies (20.7%) assessed family planning interventions, while a further five studies (17.2%) assessed interventions addressing either HIV or STIs. Three studies (10.3%) examined interventions related to SGBV, while only one study (3.4%) focused on the prevention of mother-to-child transmission of HIV (PMTCT). The remaining four studies (13.8%) assessed a number of cross-cutting SRH domains, of which three studies (10.3%) focused on both family planning and MNH interventions, and one study (3.4%) addressed family planning and abortion care. Notably, no studies addressed interventions aimed at responding to, or the prevention of, vaginal injuries and fistulae.

Study quality

All 29 studies were assessed for quality of reporting using the STROBE checklist. The majority of the observational studies (72.4%, n = 21) were found to be of high quality,[ 25 – 44 ] and the remaining eight studies (27.6%) were of moderate quality.[ 45 – 51 ]

There were common areas in which the included studies in this review provided low quality reporting. All moderate quality quantitative studies stated changes in health outcomes, but statistical associations between the intervention and the outcome were inconsistently reported, i.e. most studies did not report differences between SRH interventions and outcomes. Second, it was also not clear whether relevant confounders and biases were considered during the design of the study and analysis of the data.

Family planning

We identified six studies related to family planning. Along with other SRH outcomes, all six studies assessed contraceptive use in their respective contexts. One paper assessed a refugee-led reproductive health group operating across 48 Guinean refugee camps that recruited refugee nurses and midwives to local health facilities, trained lay women to provide health education and contraception, and to facilitate referrals. Individuals who reported the reproductive health group facilitators as their primary source of information were more likely to be current users of contraception (aOR = 1.3, 95% CI 0.7, 4.2, non-significant).[ 25 ] A home-based counselling and awareness programme for internally displaced women in Sudan led to an increase in the use of modern family planning methods (aOR 2.8, 95% CI 2.0, 4.1).[ 27 ] A programme of mobile outreach and public health strengthening in Uganda led to an increase in the number of women who reported ever using a family planning method (aOR 2.23, 95% CI 1.7, 2.92, P<0.001), and a reduction in the unmet need for family planning from 52.1% to 35.7% (aOR 0.47, 95% CI 0.37, 0.6, P<0.001).[ 26 ] A study in Pakistan providing subsidised healthcare to refugees reported use of contraceptives in the subsidised group (54%) was more than double the use reported in the non-subsidised group (25%), (P<0.001), and reported that the non-subsidised group was more likely to use the oral contraceptive pill (40.7%), whereas the subsidised group was more likely to have tubal ligation (36.7%) (p<0.001).[ 52 ] A multi-country study involving sites in Chad, the Democratic Republic of the Congo, Djibouti, Mali, and Pakistan assessed the impact of a CARE programme that included staff training, supervision in health facilities, the supply of contraceptives, community mobilisation, and awareness raising. An absolute number of 52,616 new users of modern methods of contraception were reported, of which an average of 61% of users across all sites opted for long-acting reversible contraception.[ 46 ] A study in rural Afghanistan assessed the impact of health education and the delivery of injectable contraceptives by community health workers. Over an eight-month period between 2005 and 2006, contraceptive use increased by 24–27% across three sites.[ 45 ]

Pregnancy & maternal and newborn health

We included ten studies reporting on pregnancy or maternal and newborn health-related outcomes. A cross-sectional study amongst internally-displaced women in Darfur, Sudan assessed the impact of a maternal health education programme delivered in the form of home visits. Receiving maternal health education at home was associated with a 43% reduction in the odds of giving birth at home as compared to in a healthcare facility (aOR 0.57, 95% CI: 0.35, 0.93).[ 34 ] Another study amongst internally-displaced women in Darfur found that following the implementation of an interpersonal and mass education campaign, women were more likely to deliver at a healthcare facility (OR 5.4, 95% CI: 4.0, 7.4, P<0.001).[ 35 ] Two studies assessed the effect of referral systems on access to hospital-based care. Following the implementation of an ambulance-based referral system and improved hospital telecommunications in Yirol, South Sudan, the authors reported that 99.1% of the estimated number of women with absolute obstetric indications were treated at the hospital.[ 51 ] A second study examined the impact of a hospital-based vehicle, motorbikes at satellite primary healthcare centres, along with community education activities and facility improvements, on service utilisation and case fatality rates in Bo, Sierra Leone during the period 1992–1993. Service utilisation more than doubled in the period following initiation of the transport system. The case fatality rate declined from 20% to 10% in the post-intervention period. However, there was no significant difference in outcomes between those who were referred using a hospital vehicle and those who used other means to reach the hospital.[ 48 ]

In the Philippines, following Typhoon Haiyan, training of trainers and quality assurance workshops were held, with subsequent improvements in 24-hour access to skilled birth attendants from 84% to 96% at three months (p<0.05).[ 36 ] An evaluation of a programme in West Darfur, Sudan implemented by Medair, including primary healthcare service provision, health promotion activities, and the training of midwives, reported an increase in skilled birth attendance from 35.7% to 52.7% (p = 0.025).[ 37 ] The implementation of a community-based safe motherhood programme in Kabul Province, Afghanistan, delivered by a cadre of newly trained community midwives, reported an increase in the proportion of women receiving antenatal care from 37.3% in 2004 to 91.2% in 2006 (p<0.01), and an increase in the proportion of women delivering at a healthcare facility from 31.3% to 55.2% (p<0.01).[ 33 ]

An evaluation of an International Rescue Committee (IRC) programme, which aimed to reduce maternal mortality among Afghan refugees in Pakistan by establishing emergency obstetric care centres, training community members on safe motherhood, and linking primary care with pregnancy-related education, reported a reduction in the maternal mortality ratio from 291 to 102 per 100000 live births between the first and fifth years of the programme. A reduction in the neonatal mortality rate from 25 to 20.7 per 1000 live births was also reported during the same period, while the proportion of births registered in an emergency obstetric care facility increased from 4.8% in 1996 to 67.2% in 2007.[ 49 ] A study conducted by Save the Children evaluated a birth preparedness package programme implemented in eastern Nepal between 2003 and 2004. The programme involved an educational component delivered by community healthcare workers, and preparation in advance of delivery to optimise maternal and newborn health outcomes. Along with improvements in essential newborn practices, the proportion of women reporting one or more antenatal care visit increased from 60% to 84% (p<0.001), and use of postnatal care within six weeks of delivery increased from 45% to 72% (p<0.001). Changes in the use of a skilled birth attendant were not statistically significant.[ 32 ]

Another study conducted in the Maela refugee camp on the Thai-Myanmar border assessed the effect of a special care baby unit on neonatal and cause-specific mortality rates. Between 2008 and 2011, the neonatal mortality rate declined from 21.8 to 10.7 deaths per 1000 live births (p = 0.03), while cause-specific mortality also fell in relation to the four main causes of neonatal death: prematurity, early onset neonatal sepsis, congenital abnormalities, and jaundice.[ 50 ]

HIV and STIs

A study conducted by Médecins Sans Frontières (MSF) in the conflict-affected region of Bukavu, eastern Democratic Republic of the Congo, reported a median weight gain of 2.5kg and a CD4 gain of 163 cells/ml at 6-months for patients initiated on generic, fixed dose anti-retroviral treatment.[ 47 ] A second study on 24 MSF programmes in 12 countries reported a median 12-month survival of 0.89 (95% CI: 0.88, 0.91) and a median 6-month CD4 gain of 129 cells/mm 3 following the integration of HIV care and treatment programmes with other medical activities.[ 30 ]

A third non-randomised cohort study amongst internally displaced women in Haiti reported an increase in condom use (AOR 4.05, 95% CI: 1.86, 8.83, p<0.001) following implementation of a peer health worker-led intervention involving a video-based session on HIV and STIs, followed by a six-week psycho-educational programme.[ 31 ] A pre-post study of an HIV/AIDS and STI prevention project, including outreach and education activities, in Sierra Leone identified an increase from 38% condom use at last sexual encounter to 68% amongst commercial sex workers, and from 39% to 68% amongst those who identified as members of the military forces.[ 28 ] Following the roll-out of HIV prevention education activities in an urban setting in Sierra Leone amongst adolescents aged 15 to 24 years, contraceptive use increased from 16% to 46% amongst female adolescents, and from 16% to 37% amongst male adolescents (p < .01) [ 29 ].

One study examined the effectiveness of a comprehensive PMTCT programme in conflict-affected northern Uganda. Over the course of a ten-year period, the proportion of HIV-positive women delivering in a health facility increased from 56% to 81% (p = 0.033).[ 44 ]

Sexual and gender-based violence

Three studies, all of which were randomised controlled trials, reported SGBV outcomes. A trial in the Ivory Coast compared the impact of participation in a gender dialogue group and an economic empowerment programme, versus participation only in the economic empowerment programme. Women participating in both the gender dialogue group and the economic empowerment programme were less likely to report economic abuse (OR 0.39, 95% CI 0.25, 0.6, p<0.0001), and were less likely to be accepting of the justification given for violent acts (β = -0.97, 95% CI -1.67, -0.28, p = 0.006).[ 38 ] A second randomised-controlled trial conducted in the Ivory Coast examined the effect of a sixteen-week intimate partner violence prevention programme. Men who received the intervention reported a decreased intention to use physical intimate partner violence (aRR 0.83, 95% CI 0.66, 1.06). Men in the intervention arm reported a greater ability to control their hostility and manage conflict (aRR 1.3, 95% CI 1.06, 1.58). A non-statistically significant difference was identified in reported levels of physical and/or sexual intimate partner violence (aRR 0.52, 95% CI 0.18, 1.51).[ 39 ]

A third randomised controlled trial conducted in the Democratic Republic of the Congo compared the impact of either cognitive processing therapy (comprising one individual session and 11 group sessions), or individual support for female survivors of sexual violence with high levels of post-traumatic stress and combined depression and anxiety symptoms. Both the individual support and group therapy arms reported a statistically significant improvement in all checklist scores (HSCL-25 score, PSTD checklist, and the functional-impairment score) at the end of the intervention, which was sustained at six months post-intervention (p<0.001).[ 40 ]

Interventions targeting outcomes across multiple SRH domains

Four studies reported on outcomes that spanned both family planning and pregnancy and maternal and neonatal health outcomes. A three-tiered community-based intervention in Myanmar employed traditional birth attendants to provide antenatal services and assist with deliveries, while health workers provided antenatal care and family planning supplies, and maternal health workers oversaw the aforementioned activities and attended both normal and complicated deliveries. Use of a modern method of contraception increased from 23.9% to 45.0% (prevalence rate ratio (PRR) 1.88, 95% CI 1.63, 2.17). Unmet family planning needs dropped from 61.7% to 40.5% (PRR 0.65, 95% CI 0.60, 0.72), while birth attendance by someone trained in emergency obstetric care increased from 5.1% to 48.7% (PRR 9.55, 95% CI 7.21, 12.64).[ 42 ] A cross-sectional study reviewed the possible impact of a reproductive health literacy programme amongst refugee women in Guinea. Half of the survey respondents (50%) reported current use of modern contraceptives, while 24% reported using a condom the last time they had sex, of which both findings were interpreted by study authors as an increase since implementation of the reproductive health literacy programme. The study found that 92% of women who reported becoming pregnant since the implementation of the reproductive health literacy programme reported attending at least three antenatal visits.[ 41 ]

In another study evaluating the effectiveness of an emergency obstetric care (EmOC) intervention, a trained physician was posted to a district general hospital in Makeni, Sierra Leone. Additional training was conducted, an unused operating theatre was operationalised, and a generator and blood bank were installed. The proportion of women accessing the hospital increased from 31 in 1990 to 98 in 1995, with a reduction in the case fatality rate from 32% to 5%. Notably, 444 induced abortion-related procedures were performed, compared with only 22 in 1990.[ 53 ]

Following the 2005 earthquake in Pakistan, a four-year project was initiated by USAID with the aim of improving the management capacity of district health authorities, improving access to primary healthcare services, increasing community participation in service management, and improving household-level knowledge and health-seeking behaviour. The study found non-statistically significant increases in the use of modern contraceptives (18% to 22%), at least one antenatal care visit (70.3% to 73.6%), and presence of a skilled birth attendant (36% to 38%). The study also found a statistically significant increase from 25% to 33.3% (p<0.01) in women receiving postnatal care.[ 43 ]

This review identified 29 studies assessing the effectiveness of SRH interventions in humanitarian crises published between 1980 and 2017. We found high quality evidence for specific interventions appearing to have improved SRH outcomes, including home visits and peer-led educational and counselling, training of lower-level health care providers, the use of CHWs to promote SRH services, a three-tiered network of health workers providing SRH services, the integration of HIV and SRH services, and men’s discussion groups to address intimate partner violence. We found moderate quality evidence to support transport-based referral systems, community-based SRH education, CHW delivery of injectable contraceptives, wider literacy programmes, and birth preparedness interventions. We identified no studies focusing on adolescents, LGBTQ populations or people with disabilities. Additionally, no studies measured the effectiveness of interventions addressing the comprehensive clinical management of rape, or the response to, or prevention of, vaginal injuries and fistulae.

The quality of studies included in the review was variable. Three quarter of the studies (72.4%, n = 21) used either experimental designs, i.e. randomised controlled trials, or quasi-experimental study designs, which provided some statistical measure of difference between intervention and outcome. However, where appropriate, there was often insufficient adjustment for potential confounders Evidence of attribution was particularly weak, with the vast majority of studies using cross-sectional and pre-post study designs with no control.

Although the majority of studies (72.4%, n = 21) were graded as high quality, the application of the STROBE checklist revealed a number of commonly recurring methodological weaknesses. Blinding was rarely used, including in the randomised controlled trials, which risks reporting bias of health outcomes. There was a lack of controlled studies, limited appreciation of clear exposures and confounders, absence of reporting on sampling methods, and an inadequate handling of bias. However, it is recognised that for a number of SRH interventions and in certain humanitarian contexts, blinding or use of control groups is not possible or appropriate. There was also limited use of stratification, for example by gender or age, and so potentially differing health outcomes in more vulnerable groups is missing.

We recognise that there are many logistical and ethical challenges related to SRH research in humanitarian crises. However, the more developed evidence base for other health outcomes in similar crises settings, e.g. mental health and communicable diseases,[ 16 ] signals that conducting more rigorous research in humanitarian contexts is possible. Given the lack of longitudinal data or studies with an adequate control comparison group, innovative ways of collecting data, e.g. using information and communication technologies (ICT) widely used by many conflict-affected populations such as WhatsApp, should be tested. These data collection methods may prove beneficial for researchers, healthcare providers, and organisations seeking to collect health outcome data at the individual-level, and from populations on the move who have traditionally been challenging to follow up. There is also a need for innovation in establishing stronger referral and follow-up systems in crisis settings to ensure health outcomes used to assess effectiveness are as close to its true effectiveness as possible. Researchers should also consider use of alternative study designs where standard RCTs are not operationally or ethically possible. Adjusted approaches such as stepped wedge trial designs could be used more widely in order to establish a counterfactual through the use of a control group, while remaining operationally and ethically acceptable. Additionally, no studies reported measuring outcomes beyond the study period, signalling the need to have data on longer-term effects of SRH interventions on target populations affected by humanitarian crises. Despite a well-established SRH evidence base in stable settings, further robust research is needed to determine effective and cost-effective interventions to improve SRH outcomes in populations in crisis settings.

This systematic review had a number of limitations. Caution must be exercised in generalising our study’s findings, as the specific contexts, and enabling and restrictive factors to intervention delivery and effectiveness, varied widely between studies. Although we based search terms and developed inclusion criteria to best address our research aim, our search may have missed identifying additional papers from relevant SRH domains. We also did not conduct a search for grey literature. Our strict study design criteria also excluded qualitative studies, which form a key component of the literature in this field. However, we only included quantitative studies demonstrating quantitative change over time with the aim of extracting a certain type of evidence to inform our findings on the effectiveness of SRH interventions in crisis settings. Additionally, only papers written in English and French were included. We applied a narrative synthesis approach to the findings, as we were unable to conduct a meta-analysis due to the heterogeneous nature of intervention types, indicators and methods used in the included studies. We used the STROBE checklist to assess the quality of reporting in studies, but a more specialised quality assessment tool such as the Newcastle Ottawa Scale or Cochrane Collaboration's tool for assessing risk of bias would have provided a more robust review of quality.[ 54 ]

This systematic review found high quality evidence to support improved SRH outcomes through home visits and peer-led educational and counselling, training of lower-level health care providers, CHWs to promote SRH services, a three-tiered network of health workers providing SRH services, the integration of HIV and SRH services, and men’s discussion groups for the reduction of intimate partner violence. However, the types of study design including many studies with no control group, the limited use of statistical data, and the variable quality of studies, signal that caution must be exercised in the interpretation of these results. There is a need for a higher quantity and quality of more timely research on the effectiveness of SRH interventions in humanitarian crises, in particular focusing on outcomes amongst adolescents, and studies that focus on safe abortion care, post-abortion care, vaginal injury and fistulae, the prevention of SGBV, and the comprehensive clinical management of rape.

Supporting information

S1 appendix. prisma checklist..

https://doi.org/10.1371/journal.pone.0199300.s001

S2 Appendix. Systematic review protocol.

https://doi.org/10.1371/journal.pone.0199300.s002

Acknowledgments

We thank Maria Rodriguez, Loulou Kobeissi, Adam Poulter, Robyn Drysdale, Rajrattan Rokhande and Sara Nam for reviewing the study protocol. The authors alone are responsible for the views expressed in this manuscript and they do not represent the views, decisions or policies of the institutions with which they are affiliated.

• 1. World Health Organization. Emergency Response Framework 2014 [5 December 2017]. Available from: http://apps.who.int/iris/bitstream/10665/89529/1/9789241504973_eng.pdf?ua=1 .
• 2. State of world population New York: United Nations Population Fund; 2015 [14 November]. Available from: http://www.unfpa.org/sites/default/files/sowp/downloads/State_of_World_Population_2015_EN.pdf .
• View Article
• PubMed/NCBI
• Google Scholar
• 4. Adding It Up: The Costs and Benefits of Investing in Sexual and Reproductive Health: Guttmacher Institute; 2017 [14 November]. Available from: https://www.guttmacher.org/fact-sheet/adding-it-up-contraception-mnh-2017 .
• 6. United Nations. Report of the Secretary-General on women and peace and security New York: United Nations; 2014 [21 November 2018]. Available from: http://www.un.org/ga/search/view_doc.asp?symbol=S/2014/693 .
• 9. Report of the International Conference on Population and Development. International Conference on Population and Development; New York: United Nations 1994.
• 14. United Nations High Commissioner for Refugees. Reproductive Health Services for Refugees and Internally Displaced Persons: Report of an Inter-agency Global Evaluation. 2004.
• 18. World Health O. Measuring sexual health: Conceptual and practical considerations and related indicators. 2010.
• 19. World Health O. Sexual health and its linkages to reproductive health: an operational approach. Sexual health and its linkages to reproductive health: an operational approach2017.

• Feature Article
• Developmental Biology

Meta-Research: The need for more research into reproductive health and disease

• Natalie D Mercuri

• Department of Physiology, University of Toronto, Canada ;
• Open access
• Copyright information
• Comment Open annotations (there are currently 0 annotations on this page).
• 2,380 views
• 157 downloads
• 5 citations

Share this article

Cite this article.

• Brian J Cox
• Copy to clipboard
• Download BibTeX
• Download .RIS
• Figures and data

Introduction

Conclusions, data availability, decision letter, author response, article and author information.

Reproductive diseases have a significant impact on human health, especially on women’s health: endometriosis affects 10% of all reproductive-aged women but is often undiagnosed for many years, and preeclampsia claims over 70,000 maternal and 500,000 neonatal lives every year. Infertility rates are also rising. However, relatively few new treatments or diagnostics for reproductive diseases have emerged in recent decades. Here, based on analyses of PubMed, we report that the number of research articles published on non-reproductive organs is 4.5 times higher than the number published on reproductive organs. Moreover, for the two most-researched reproductive organs (breast and prostate), the focus is on non-reproductive diseases such as cancer. Further, analyses of grant databases maintained by the Canadian Institutes of Health Research and the National Institutes of Health in the United States show that the number of grants for research on non-reproductive organs is 6–7 times higher than the number for reproductive organs. Our results suggest that there are too few researchers working in the field of reproductive health and disease, and that funders, educators and the research community must take action to combat this longstanding disregard for reproductive science.

It is difficult to overstate the impact of reproductive disease. Adverse pregnancy outcomes – which include preterm delivery, low birth weight, hypertensive disorders, and gestational diabetes –impact the acute and chronic health of the population ( Barker, 1997 ; Williams, 2011 ; Lewis et al., 2012 ). About 20% of all pregnancies require medical intervention ( Murray and Lopez, 1998 ), and in lower resource settings, pregnancy and delivery complications are a leading cause of maternal and neonatal death ( WHO, 2019 ).

In 1992, the Institute of Medicine in the United States published a report called Strengthening Research in Academic OB-GYN Departments that outlined areas of research with obstetrics and gynecology where improvements were needed, such as low-birth-weight infants, fertility complications, and pregnancy-induced hypertension ( Institute of Medicine, 1992 ). Three decades later, despite the essential nature and impact of the reproductive system, these issues are still major challenges in reproductive health.

Gender inequality and bias have been issues since the onset of biological and medical research. For example, including women as subjects in clinical research was not standard practice until after 1986 ( Liu and Mager, 2016 ). There has been progress in developing policies to increase the representation of women (as both subjects and researchers) and in providing education on gender inequality for all researchers, but women are still underrepresented in scientific and medical research ( Huang et al., 2020 ).

There are a variety of stigmas and taboos surrounding any topic relating to reproductive function. Menstruation is one function that has faced stigmatization that persists today ( Litman, 2018 ; Pickering, 2019 ), with women often feeling too embarrassed to talk about this natural process or even complete an essential task, such as purchasing menstrual products at a local store. Political power highly affects reproductive health care and rights over other biological processes. In many countries, ongoing political and legal battles directly affect access to safe reproductive health care, including contraception, safe abortion, and gender identity rights ( Pugh, 2019 ). There are parallels between the low level of research into reproductive diseases and the response to the AIDS epidemic in the 1980s. The long delay in recognizing AIDS as a significant health issue, and then implementing research policies, perpetuated false ideas surrounding the lifestyles of those affected by the disease and created a barrier to expanding sexual education and seeking healthcare, likely costing many lives ( Francis, 2012 ). Despite great advances in AIDS research and treatment, including social awareness, public health stigma still lingers in society ( Turan et al., 2017 ). Similar increases in advocacy and public awareness are needed to overcome these barriers affecting reproductive health.

Reproductive pathologies are often challenging to diagnose and properly treat, which increases the risk of comorbidity development. Moreover, a long-standing lack of research into reproductive health and disease means that the acute and chronic healthcare burden caused by reproductive pathologies is likely to continue increasing. This lack of research likely results from historic and ongoing systemic biases against female-focused research, and from political and legal challenges to female reproductive health ( Coen-Sanchez et al., 2022 ). In this exploratory analysis we seek to understand the “research gap” between reproductive health and disease and other areas of medical research, and to suggest ways of closing this gap.

Comparing numbers of publications

To benchmark research on reproductive health and disease, we used the PubMed database to compare the number of articles published on seven reproductive organs and seven non-reproductive organs between 1966 and 2021 ( Table 1 ). While the reproductive organs are not essential to postnatal life, we posit that the placenta and the uterus are as essential to fetal survival in utero as the lungs and the heart are to postnatal survival after birth. Our analysis revealed that the average number of articles on non-reproductive organs was 4.5 times higher than the number on reproductive organs (and ranged between about 2 and 20 in pairwise comparisons). The reproductive organs with the most publications were the breast and prostate.

Total number of matching articles from PubMed for seven non-reproductive keywords and seven reproductive keywords for the period 1966–2021.

The research landscape can change over time and efforts to reduce gender bias in research might have had an impact on the volume of reproductive research, so we plotted the number of publications on the 14 organs as a function year between 1966 and 2021 ( Figure 1A ). Breast and prostate were the only reproductive organs to increase in publication at a rate similar to the kidney; the second least studied non-reproductive organ in our list. The intestine was the only non-reproductive organ to show similar publication rates to the other five reproductive organs. To investigate further, we compared disease-driven research versus research not related to disease.

Number of articles published every year on seven reproductive organs and seven non-reproductive organs.

( A ) The number of articles published on most of the non-reproductive organs (including the brain, heart, lung and liver) has increased more rapidly than the number of articles published on the reproductive organs. ( B ) Removing articles that contain the keyword cancer has relatively little effect on the number of articles for non-reproductive organs (with the exception of the lung), but has a significant impact on the number of articles for the two reproductive organs with the most articles: the breast and prostate. Data extracted from PubMed using organ-specific keyword searches for the period 1966–2021.

Figure 1—source data 1

Articles per year for reproductive and non-reproductive organs, with and without the keyword cancer.

Comparing research related to disease and research not related to disease

In the 1970s, the National Institutes of Health (NIH) initiated a war on cancer, and the breast and prostate are both associated with sex-specific cancers. We reassessed publication data with the added search parameter "NOT cancer" to eliminate cancer-based research ( Figure 1B ). We observed a reduction of approximately 20% for most non-reproductive organs; however, the reduction for publication on the breast and prostate was about 80%, suggesting that most research on these organs is driven by an interest in cancer research rather than reproductive health and disease ( Figure 1B ).

Then, for each organ, we plotted the number of publications related to disease on the vertical axis, and the number not related to disease on the horizontal axis, which revealed a high degree of variation among the organs ( Figure 2 ). For three non-reproductive organs (brain, heart, and liver) the number of publications not related to disease was almost three times as high as the number related to disease, and for two non-reproductive organs (kidney and lung) the numbers were similar. For the breast and prostate, on the other hand, the number of publications related to disease was three times as high as the number not related to disease. For the five remaining reproductive organs, and also for the intestine and pancreas, the number of publications not related to disease was about twice as high as the number related to disease (although the total number of publications for these seven organs was about an order of magnitude lower than the number for the other seven organs).

Comparing research related to disease and research not related to disease for reproductive and non-reproductive organs.

For each organ (colored circles) the vertical axis shows the number of publications for the period 1966–2021 related to disease, and the horizontal axis shows the number not related to disease: the area of the circle is proportional to the total number of publications. The straight blue line corresponds to equal numbers of disease-related and non-disease-related publications, so organs to the right of this line (notably non-reproductive organs such as the brain, heart and liver) tend to be the subject of more basic or non-disease-related research, whereas organs to the left of this line (notably reproductive organs such as the breast and prostate) tend to be the subject of disease-related research. The lung is the only non-reproductive organ in our sample to the left of the blue line.

Figure 2—source data 1

Total number of articles on research related to disease and research not related to disease for reproductive and non-reproductive organs.

Research funding

Next we used databases belonging to the Canadian Institutes of Health Research (CIHR) and the NIH to investigate funding trends for the different organs. The 14 keywords (brain, heart, liver, lung, kidney, intestine, pancreas, breast, prostate, ovary, uterus, penis, testes, and placenta) were entered into each database, and we extracted funding data for the period between 2013 and 2018. These organs were chosen as keywords to investigate the funding related to a basic understanding of the biology of these organs. Although grants that relate to pregnancy or fertility may not be captured, these topics are much broader and would introduce subtopics outside of the reproductive scope, similar to using keywords such as metabolism or behaviour. Table 2 gives the number of projects for each keyword and the corresponding average funding amount per grant for the CIHR, and the same for the NIH. Our analysis found that the mean grant amounts for the CIHR and NIH are similar between different keyword research topics (CIHR: $ 370 000 ± $ 50 000; NIH: $ 481 500 ± $ 50 000). The similar funding amounts between different organs are encouraging and may result from standard funding guidelines for biomedical research. However, our analysis found that the average number of funded projects is much higher for non-reproductive organs compared to reproductive organs for both the CIHR (800 vs 115) and the NIH (31 000 vs 5 300).

Total number of projects funded and average grant (in Canadian or US dollars) for the Canadian Institutes of Health Research (columns 2 and 3) and the US National Institutes of Health (columns 4 and 5) for the years 2013–2018 for seven non-reproductive keywords and seven reproductive keywords (column 1).

Table 2—source data 1.

Source data for Table 2 .

Our analysis suggests a bias against research into reproductive health and disease, and it is important that efforts are made to eliminate this bias so that research into reproductive medicine does not fall further behind. The higher levels of research observed for some reproductive organs (notably the breast and prostate) were driven by cancer-focused research, but this has not led to an increase in the level of non-disease-related research on these organs ( Figure 1B ). Factors such as Breast Cancer Awareness Month ( Jacobsen and Jacobsen, 2011 ) and screening programmes for prostate cancer ( Dickinson et al., 2016 ) likely led to the increase in publications about these two reproductive organs.

While our analysis is suggestive that many reproductive organs achieve a good balance of non-disease versus disease-related research, the paucity of research is highly problematic to the field. An important consideration is that a lack of non-disease-related research on reproductive organs may hinder progress in diagnosing and treating a wide range of pathologies (including preeclampsia, polycystic ovary syndrome, and endometriosis).

In a competitive funding system, publications are correlated to successful grants and dollar values awarded. Across research areas, we found that the mean grant dollar amounts per project are similar. However, the numbers of funded research projects on non-reproductive organs were higher than the numbers for reproductive organs by a factor of 6–7 (which is slightly larger than the discrepancy seen in publication rates). An important consideration is that the part of the NIH that supports reproductive research in the US, the National Institute of Child Health and Development, is one of the lowest-funded institutes at the NIH and does not have the word reproduction in its title. In Canada, the Human Development, Child and Youth Health Institute of CIHR is a funder of most pregnancy and reproductive biology grants, typically awarded through the Clinical Investigation – A panel, and it may be that the use of a clinical panel to fund this area of research inhibits non-diseased focused research. This panel is well-funded relative to other panels; however, some research areas (e.g., cardiovascular and neurological research) have more than one panel.

A growing political and societal emphasis is placed on disease-related research, such as cancer. This may arise from a view of basic research as ineffective or inefficient compared to applied research ( Lee, 2019 ). Perhaps this is best seen in our analysis by the high percentage of research publications on the prostate and breast that are due to cancer research, whereas most research on the other reproductive organs we studied was not disease-related. While the placenta and uterus are widely viewed as causal organs for reproductive complications that claim large numbers of maternal and neonatal lives, and treatments cost tens of billions of US dollars every year, there is relatively little disease-related research into these organs. The investigation of cancer biology within a reproductive organ can rely on knowledge of cancer in other organ systems. However, the low levels of research into reproductive organs relative to other organs means that there is much less foundational knowledge to rely on when seeking to develop treatments for diseases of these organs. Moreover, there are fewer researchers who are experienced on working with these organs.

There are several limitations to our approach. One important limitation is that the number of unfunded grant applications is not accessible, so we could not determine if the lower numbers of grants for research on reproductive health and disease were due to proportionally lower total application numbers, or to a bias against reproductive research. Funding bodies should conduct internal analyses to determine appropriate action. The use of keywords to distinguish between non-disease and disease-related research is a limitation, and the relatively low numbers of publications on reproductive organs can also present challenges when making comparisons. However, the differences we observe between research into reproductive and non-reproductive organs (as measured by numbers of publications and levels of funding) are large and are unlikely to result from missing search terms.

How can we address the research gap and enable the field of reproductive health and disease to catch up with other areas of research? Based on our analysis, we need to increase the number of researchers working on reproductive organs and related pathologies. Recent efforts by the NIH, such as the Human Placenta Project ( Guttmacher et al., 2014 ), indicate a recognition of the need to increase research capacity in reproductive sciences, and may lead to further increases in both interest and research capacity in the longer term.

New researchers may avoid the reproductive field due to social and political factors and the research gap (ie, the low levels of grant funding and publications), and this in turn may discourage students and trainees, which will make it even more difficult to increase the size of the research base. While continued advocacy, education, and political lobbying may help to overcome many of the social and political factors, closing the research gap will require other approaches.

To increase researchers and research output, we may learn lessons from the examples of breast and prostate cancer. In both cases, research increased dramatically from a historically low level. While public campaigns played a prominent role in these increases, the existence of a large pool of researchers and trainees already working on other types of cancers was probably more important (as it was these researchers, rather than those doing non-disease-related research on these organs, who did most of the work on breast and prostate cancer). However, this is unlikely to work for preeclampsia and other reproductive pathologies as there are no large pools of existing researchers available to switch the focus of their work.

Therefore, to increase research capacity, we should promote collaborations between researchers working on reproductive health and disease and those working in other areas of physiology and medicine, especially other areas with much higher research capacities. There are plenty of examples that show the benefit of such an integrated approach. For instance, female sex hormones protect against many aging diseases, such as cardiovascular and neurological diseases, leading to the prescription of hormone replacement therapies after menopause in some women ( Paciuc, 2020 ).

Links to immunology, cardiology and other systems can be used to increase research capacity. During pregnancy, there are dramatic changes in maternal physiology, including metabolism, the immune system, and cardio-pulmonary systems, and consequently, these are the same systems affected by reproductive pathologies. Preeclampsia predisposes the mother to a long-term cardiovascular risk of developing peripheral artery disease, coronary artery disease, and congestive heart failure ( Rana et al., 2019 ). Additionally, complications of the liver and kidney are associated with preeclampsia. Polycystic ovary syndrome and endometriosis are related to metabolism problems and the risk of cancer development. Children born from pregnancies affected by preeclampsia or fetal growth restriction are at a 2.5 times higher risk of developing hypertension and require anti-hypertensive medications as adults ( Ferreira et al., 2009 ; Fox et al., 2019 ).

The pathological interaction of reproductive with non-reproductive systems and organs should attract investigators from nephrology, hepatology and cardiovascular research, where the total number of researchers is 10–20 times as high as the number in reproductive health and disease. If just 1% of the researchers in the cardiovascular field were to refocus on pregnancy-related cardiovascular adaptation and pathologies, this would increase reproductive research by 10%.

Our neglect of the placenta and reproductive biology impedes other biomedical research areas. In cancer research, the methylation patterns of tumours look most like those found in the placenta, but why placenta methylation patterns are so unlike all other organs is not known ( Smith et al., 2017 ; Rousseaux et al., 2013 ). In regenerative medicine, the immune-modulating genes used by the placenta ( Szekeres-Bartho, 2002 ) are repurposed to generate universally transplantable stem cells and tissues ( Han et al., 2019 ). A poor understanding of reproductive biology is dangerous, considering emerging diseases that affect pregnancy and fetal development, such as the recent Zika virus outbreak ( Schuler-Faccini et al., 2016 ; Calvet et al., 2016 ). There are likely many other broad benefits to better understanding reproductive biology. The time to act is now, as waiting longer will not improve the situation.

Publication rates

Published research manuscripts were searched in NCBI’s PubMed database ( https://pubmed.ncbi.nlm.nih.gov/ ) between and including the years 1966 and 2021. Keywords for each search pertained to a specific organ or disease and were limited to the title/abstract of the manuscripts. The organs used for these analyses were the brain, heart, liver, lung, kidney, intestine, pancreas, breast, prostate, ovary, uterus, penis, testes, and placenta. We restricted the organ publication timelines to the years 1966–2021 and extracted the annual article count. The organ publication timeline was reconducted with the addition of the search parameter "NOT cancer".

Funding rates

Grant funding data was obtained from the CIHR funding database ( https://webapps.cihr-irsc.gc.ca/funding/Search?p_language=E&p_version=CIHR ) and the NIH reporter tool ( https://reporter.nih.gov ) by searching keywords in the title and abstracts/summary. Keywords used for these searches were brain, heart, liver, lung, kidney, intestine, pancreas, breast, prostate, ovary, uterus, penis, testes, and placenta. The years were restricted to 2013–2018. The total number of projects pertaining to each search term during this period was extracted, and the total amount of funding for those projects was averaged.

All graphs were produced using R (version 4.0.2) in R Studio (version 1.3.1073). R packages used were ggplot2, tidyverse, formattable, gridExtra, RColorBrewer, ggrepel.

All data were obtained from public databases (PubMed/NCBI, NIH and CIHR). Source data files for Figure 1, Figure 2 and Table 2 are available (see figure and table captions for details).

• Google Scholar
• de Filippis I
• de Sequeira PC
• de Mendonça MCL
• de Oliveira L
• Tschoeke DA
• Thompson FL
• Dos Santos FB
• Nogueira RMR
• de Filippis AMB
• Coen-Sanchez K
• El-Mowafi IM
• Idriss-Wheeler D
• Dickinson J
• Connor Gorber S
• Stehouwer CDA
• Lewandowski AJ
• Guttmacher AE
• Ferreira LMR
• Strominger JL
• Meissner TB
• Barabási AL
• Institute of Medicine
• Jacobsen GD
• Jacobsen KH
• Pickering K
• Karumanchi SA
• Rousseaux S
• Debernardi A
• Nagy-Mignotte H
• Moro-Sibilot D
• Brichon P-Y
• Lantuejoul S
• de Reyniès A
• Brambilla C
• Brambilla E
• Schuler-Faccini L
• Feitosa IML
• Horovitz DDG
• Cavalcanti DP
• Doriqui MJR
• Wanderley HYC
• El-Husny AS
• Sanseverino MTV
• Brazilian Medical Genetics Society–Zika Embryopathy Task Force
• Cacchiarelli D
• Szekeres-Bartho J
• Browning WR
• Mugavero MJ
• Peter Rodgers Senior and Reviewing Editor; eLife, United Kingdom
• Marleen van Gelder Reviewer
• James Roberts Reviewer

In the interests of transparency, eLife publishes the most substantive revision requests and the accompanying author responses.

Decision letter after peer review:

Thank you for submitting the paper "A Poor Research Landscape Hinders the Progression of Knowledge and Treatment of Reproductive Diseases" for consideration by eLife . Your article has been reviewed by 3 peer reviewers, and the evaluation has been overseen by a Reviewing Editor and a Senior Editor. The following individuals involved in review of your submission have agreed to reveal their identity: Marleen van Gelder (Reviewer #1); James Roberts (Reviewer #3).

This article will need considerable revision to be suitable for publication as a Feature Article. In particular, you will need to address the concerns raised by the referees (see below), and also address a number of editorial points.

Reviewer #1

In this manuscript, Mercuri and Cox aimed to quantify the advancement of research in reproductive sciences relative to other medical disciplines. They compared two indicators of the research landscape: published research manuscripts and funded projects. The results showed lower publication rates for research on reproductive organs compared to selected non-reproductive organs, in particular concerning basic research. In addition, a relatively small number of grants was funded for projects on diseases with a reproductive focus. Based on these data, the authors concluded that the gap in knowledge and treatment of diseases of the reproductive organs is at least partially caused by a poor research landscape.

Although the conclusions of this paper are somewhat supported by the data, some aspects of the methods and reporting need to be clarified.

[Note: The following point is covered by the queries in the Word version I have sent you]

1) The manuscript, and in particular the Introduction and Discussion sections, could benefit from restructuring, in which adhering to a relevant reporting guideline may be helpful. For example, the authors provide relatively extensive background information on a number of important reproductive health disorders, but the level of detail does not contribute to setting the aim for the study. Moreover, the last paragraph of the introduction section (lines 92-100) already seems to include the conclusion of this paper.

[Note: Please address points b, d and f below. The other points are covered by the queries in the Word version I have sent you]

2) Concerns regarding the methods:

a) Citations in PubMed are known to be selective before 1966; consider using a fixed start date/year for the search.

b) The results strongly depend on the organs and diseases selected to be included in the 'reference group'. Provide a rationale for the selection of organs, which in the current analysis only seem to include major organs that are known to be well-studied, and not organs such as skin, eyes, intestine, pancreas, spleen or urinary bladder. The selection is vital for drawing robust conclusions from the data.

c) The approach to distinguish between basic and applied research is not validated.

d) The prevalence of diseases reported in Figure 4 is highly country-specific, in particular for tuberculosis. Therefore, this comparison may not be suitable for an international audience.

e) The most important limitation of the grant funding data was already mentioned: "the number and keywords of failed grant applications were not accessible" (lines 271-272). Therefore, it is hard to draw conclusions on failure of grant applications on reproductive health.

f) The rationale for the keywords used in the funding databases is missing and likely to yield selective results. Many reproductive health related projects may be missed, as keywords such as pregnancy and subfertility were not included. And also in this search, the selection of keywords for the reference group seems biased.

[Note: Please consider adding a table as suggested below; however, this is optional rather than essential.]

3) To emphasize the lack of knowledge in relation to disease burden, a table summarizing the prevalence, number of publications, and grants could summarize the results.

[Note: This point is covered by the queries in the Word version I have sent you]

4) A number of topics and statements in the Discussion section seem to be unrelated to the aim of this study. Examples include the female representation in STEM disciplines and the correlation between research publications and changes in policy (this was not specifically analyzed and would require additional analyses).

Reviewer #2

[Note: Please address the following point]

While the authors have attempted to be broad in their assessment of reproduction research, they seem to neglect two very broad areas of women's health for which there is little research: menstruation and menopause. Both are only mentioned in the discussion, and referenced with respect to promotion of the study of human physiology. Given the focus on lack of basic understanding of reproductive organs, it may be worth mentioning these, particularly in comparison to the depth of research on erectile dysfunction; this may also help to emphasize the fact that the lack of research in reproduction primarily affects women (though there are of course consequences for men's health, including the period in the womb).

Figure 1: the color code is not clear; Not sure how this could be better represented, but maybe listing the organs from high to low for both parts a and b in the legend? Or magnifying one part of each graph? In particular, the 80% loss of publications in breast/prostate when applying the search term "NOT cancer" does not come through; so perhaps a graph focusing on just these two organs showing the original search and the "NOT cancer" search results would be best?

Tables 2 and 3: It is not clear how this search was done; was the project title or abstract of grants searched for these key terms?

Discussion (including lines 259-260): I'm not sure that the conclusion drawn here is consistent with the data? The authors somewhat confusingly alternate between lack of research in reproduction as a whole vs. lack of basic research in this area.

[Note: Addressing the following point is optional, not essential.]

Another point of discussion that merits mention here is how the lack of interest/emphasis on reproduction research by funding agencies in turn affects the perception of "impact" of such research: i.e. both in terms of how low impact factors of reproduction journals are compared to journals in other fields, but also how the high-impact journals (Cell/Science/Nature) view/receive submissions from researchers in this area. Reviewer #3

The authors propose that research in reproductive areas lags behind that of other areas of biology. They support this with information from publications and funding sources.

This is a presentation of importance to investigators in all fields, funders and the general public. For reproductive investigators it provides objective data to support the lagging of reproductive research and to investigators in other areas of biology and the general public should be an eye opening demonstration of the huge gap between research in reproduction and other areas of biology. One would hope it would also provide a motivation to funders to modify the situation.

The authors remind us of the importance of reproduction on the survival of the species and provide extensive data on specific examples of the impact of reproductive diseases. They then use review of publications keyed to reproductive organs and non-reproductive organs both currently and over time. They point out that research on non-reproductive organs is 5 to 20 times more frequent than that on reproductive organs. [Note: Please address the point made in the following sentence] They should make it clearer that this is referring to specific organs and not a comparison sum of research on all organs of reproduction and not reproduction. They show that over time this discrepancy has increased with the exception of prostate, and breast research but even with those it is evident this is research related specifically to cancer and not normal organ function.

They make a slightly less compelling comparison on the portion of research devoted to basic understanding or clinical research which for nonreproductive organs is considerably more for basic science than in reproductive organs. [Note: Please address the point made in the following sentence] However, this is likely compromised by the relative minute number of either type of studies in reproduction.

They then make comparisons between the impact of specific reproductive topics and publications. They state that although preeclampsia and breast cancer have a similar prevalence the number of breast cancer publications are much higher. [Note: Please address the point made in the following sentence] To me the comparison of a disorder with high mortality (breast cancer) and far lower mortality (preeclampsia) does not provide a compelling argument and also is a little off target for comparing reproductive and nonreproductive research.

[Note: Please address the point made in the following paragraph]

They make a similar comparison of PCOS a reproductive disorder with other non-reproductive disorders of similar or lower prevalence, autism, tuberculosis, Crohn's Disease and Lupus with a much lower publication rate for PCOS. Again, this seems a bit of comparing apples and oranges.

They investigate the relative funding of research on these topics in the US and Canada and find that the size of individual grants for reproductive and non-reproductive research in both countries is similar but that the number of funded grants for specific non-reproductive organs is, that like that of publications, is about 2 to 20 times higher for nonreproductive organs.

The authors present their conclusions of the reason for the discrepancy. They point out gender bias which has been a target for improvement for several years and has been reduced but research is still not on an equal basis for men and women. However, the bias goes beyond gender since male reproductive research publications and funding also lags. They conclude that there is a general bias against reproductive research. [Note: Please consider mentioning the following point in your article] Interestingly they do not cite a major support for this conclusion, that the major NIH institute supporting reproductive research, the National Institute of Child Health and Development (NICHD)is one lowest funded institutes and does not have reproduction in its title.

They provide two general suggestions to increase reproductive research. The first is to increase funding and the second to involve other forms of research in studies supporting the role of reproductive disorders and physiology in non-reproductive studies. [Note: Please address the point made in the rest of this paragraph] They point out the relationship of preeclampsia to later life cardiovascular disease as an example of this. Unfortunately, they state this relationship as causal which has not been established. Nonetheless studying preeclampsia will likely provide information useful to cardiovascular health.

It is possible that linking publications and funding amounts to conclusions about bias against reproductive research is not precise. However, the magnitude of the differences strongly supports the authors' premise.

This interesting presentation makes and important point about the fact that reproductive research lags beyond other biological research. They do this through the use of publication and grant funding reviews. The differences are large in a direction that support the point they are making. There are some suggestions that I believe would improve the presentation.

[Note: Please address the following three points]

1. There should be a bit more discussion of the limitations of their approach.

2. In the comparisons of disorders of reproduction and non-reproduction they should indicate the limitations of comparing very different disorders.

3. Preeclampsia as a cause of later life CVD has not been established. They are related.

Reviewer #1 In this manuscript, Mercuri and Cox aimed to quantify the advancement of research in reproductive sciences relative to other medical disciplines. They compared two indicators of the research landscape: published research manuscripts and funded projects. The results showed lower publication rates for research on reproductive organs compared to selected non-reproductive organs, in particular concerning basic research. In addition, a relatively small number of grants was funded for projects on diseases with a reproductive focus. Based on these data, the authors concluded that the gap in knowledge and treatment of diseases of the reproductive organs is at least partially caused by a poor research landscape. Although the conclusions of this paper are somewhat supported by the data, some aspects of the methods and reporting need to be clarified. [Note: The following point is covered by the queries in the Word version I have sent you] 1) The manuscript, and in particular the Introduction and Discussion sections, could benefit from restructuring, in which adhering to a relevant reporting guideline may be helpful. For example, the authors provide relatively extensive background information on a number of important reproductive health disorders, but the level of detail does not contribute to setting the aim for the study. Moreover, the last paragraph of the introduction section (lines 92-100) already seems to include the conclusion of this paper.

This query has been responded to the in Word file

[Note: Please address points b, d and f below. The other points are covered by the queries in the Word version I have sent you] 2) Concerns regarding the methods: a) Citations in PubMed are known to be selective before 1966; consider using a fixed start date/year for the search.

This query has been responded to the in Word file. We have now used a fixed date of 1966 as the early timepoint and as indicated in the Word file.

Organs such as brain, heart and lungs are essential for life. The placenta is similarly essential. Other organs such as kidney and liver are also essential but not as immediate. We now include the intestine as a reference point.

Our preliminary analysis found that Skin has over 800,000 publication mentions, but it is not clear if this is the skin organ or a skin on something more work to eliminate background skin hits would be needed. Epidermis has 60,000 hits that are likely more specific, but we did find may abstracts and titles on the skin organ that do not use epidermis. Eyes are nearly 700,000 publications, intestine also over 700,000, pancreas has over 200,000 spleen is also over 200,000 urinary bladder has 130,000, which is similar to the placenta at just over 100,000

This preliminary search seems to still support our conclusion that placenta and reproductive organs are under-researched and only add a list of other organs that are better studied.

Comparisons of diseases has been removed from the manuscript.

We have removed disease focused terms form the search to ensure we capture organ focus research. The inclusion of pregnancy or subfertility would be misleading as it would include disciplines such as sociology and psychology. This is akin to searching for diabetes or metabolism to understand the research landscape on the pancreas.

We felt the separate tables made the information more digestible.

This query has been responded to the in Word file. We have extensively edited and redrafted the Discussion section.

Reviewer #2 [Note: Please address the following point] While the authors have attempted to be broad in their assessment of reproduction research, they seem to neglect two very broad areas of women's health for which there is little research: menstruation and menopause. Both are only mentioned in the discussion, and referenced with respect to promotion of the study of human physiology. Given the focus on lack of basic understanding of reproductive organs, it may be worth mentioning these, particularly in comparison to the depth of research on erectile dysfunction; this may also help to emphasize the fact that the lack of research in reproduction primarily affects women (though there are of course consequences for men's health, including the period in the womb). Figure 1: the color code is not clear; Not sure how this could be better represented, but maybe listing the organs from high to low for both parts a and b in the legend? Or magnifying one part of each graph? In particular, the 80% loss of publications in breast/prostate when applying the search term "NOT cancer" does not come through; so perhaps a graph focusing on just these two organs showing the original search and the "NOT cancer" search results would be best?

These corrections have been made to the in Word file.

We agree and have focused the discussion on the general low level of publications and low level of researchers in the field.

Another point of discussion that merits mention here is how the lack of interest/emphasis on reproduction research by funding agencies in turn affects the perception of "impact" of such research: i.e. both in terms of how low impact factors of reproduction journals are compared to journals in other fields, but also how the high-impact journals (Cell/Science/Nature) view/receive submissions from researchers in this area.

This is an issue many discipline struggle with. A low number of researchers in a field tends to create low levels of impact as measured through citations. Attempts to normalize impact factors and citation rates to the size of the field may help. While we agree with the reviewers comments we cannot address within our study.

Reviewer #3 The authors propose that research in reproductive areas lags behind that of other areas of biology. They support this with information from publications and funding sources. This is a presentation of importance to investigators in all fields, funders and the general public. For reproductive investigators it provides objective data to support the lagging of reproductive research and to investigators in other areas of biology and the general public should be an eye opening demonstration of the huge gap between research in reproduction and other areas of biology. One would hope it would also provide a motivation to funders to modify the situation. The authors remind us of the importance of reproduction on the survival of the species and provide extensive data on specific examples of the impact of reproductive diseases. They then use review of publications keyed to reproductive organs and non-reproductive organs both currently and over time. They point out that research on non-reproductive organs is 5 to 20 times more frequent than that on reproductive organs. [Note: Please address the point made in the following sentence] They should make it clearer that this is referring to specific organs and not a comparison sum of research on all organs of reproduction and not reproduction. They show that over time this discrepancy has increased with the exception of prostate, and breast research but even with those it is evident this is research related specifically to cancer and not normal organ function.

Thank you for this comment. These clarifications have been made to the in Word file.

We agree that the lower level make estimating the ratio of basic to applied very challenging. But there seems to be a tendency to bias to basic research. We made some changes to the results and discussion to acknowledge this challenge.

We agree and have remove the section discussing a comparison of disease prevalence and mortalities. We realize there was no benefit to comparison disease prevalence and severity.

They investigate the relative funding of research on these topics in the US and Canada and find that the size of individual grants for reproductive and non-reproductive research in both countries is similar but that the number of funded grants for specific non-reproductive organs is, that like that of publications, is about 2 to 20 times higher for nonreproductive organs. The authors present their conclusions of the reason for the discrepancy. They point out gender bias which has been a target for improvement for several years and has been reduced but research is still not on an equal basis for men and women. However, the bias goes beyond gender since male reproductive research publications and funding also lags. They conclude that there is a general bias against reproductive research. [Note: Please consider mentioning the following point in your article] Interestingly they do not cite a major support for this conclusion, that the major NIH institute supporting reproductive research, the National Institute of Child Health and Development (NICHD)is one lowest funded institutes and does not have reproduction in its title.

Thank you for this comment, we have added it!

Thank you for the comment, we modified our statement to an observed increased risk of cardiovascular disease, as the risk may be causal or associated as the reviewer stated.

It is possible that linking publications and funding amounts to conclusions about bias against reproductive research is not precise. However, the magnitude of the differences strongly supports the authors' premise. This interesting presentation makes and important point about the fact that reproductive research lags beyond other biological research. They do this through the use of publication and grant funding reviews. The differences are large in a direction that support the point they are making. There are some suggestions that I believe would improve the presentation. 1. There should be a bit more discussion of the limitations of their approach.

We have added more caveats about our approach and interpretation

The comparisons of diseases has been removed.

This is addressed as per the above comment.

Author details

Natalie D Mercuri is in the Department of Physiology, University of Toronto, Toronto, Canada

Contribution

Competing interests.

Brian J Cox is in the Department of Physiology and the Department of Obstetrics and Gynaecology, University of Toronto, Toronto, Canada

For correspondence

University of toronto, canada research chairs.

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Acknowledgements

We thank the University of Toronto and the Department of Physiology for providing the opportunity and supporting the completion of this review. We also thank the librarians who offered expert advice on keyword searches of databases.

Publication history

• Received: October 28, 2021
• Preprint posted: November 19, 2021 (view preprint)
• Accepted: December 12, 2022
• Accepted Manuscript published: December 13, 2022 (version 1)
• Accepted Manuscript updated: December 13, 2022 (version 2)
• Version of Record published: December 21, 2022 (version 3)

© 2022, Mercuri and Cox

This article is distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use and redistribution provided that the original author and source are credited.

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

Downloads (link to download the article as pdf).

• Article PDF

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools), categories and tags.

• reproductive biology
• reproductive health
• meta-research

Research organism

• Of interest

Dynamic modes of Notch transcription hubs conferring memory and stochastic activation revealed by live imaging the co-activator Mastermind

Further reading.

• Chromosomes and Gene Expression

Developmental programming involves the accurate conversion of signalling levels and dynamics to transcriptional outputs. The transcriptional relay in the Notch pathway relies on nuclear complexes containing the co-activator Mastermind (Mam). By tracking these complexes in real time, we reveal that they promote the formation of a dynamic transcription hub in Notch ON nuclei which concentrates key factors including the Mediator CDK module. The composition of the hub is labile and persists after Notch withdrawal conferring a memory that enables rapid reformation. Surprisingly, only a third of Notch ON hubs progress to a state with nascent transcription, which correlates with polymerase II and core Mediator recruitment. This probability is increased by a second signal. The discovery that target-gene transcription is probabilistic has far-reaching implications because it implies that stochastic differences in Notch pathway output can arise downstream of receptor activation.

Coupling and uncoupling of midline morphogenesis and cell flow in amniote gastrulation

Large-scale cell flow characterizes gastrulation in animal development. In amniote gastrulation, particularly in avian gastrula, a bilateral vortex-like counter-rotating cell flow, called ‘polonaise movements’, appears along the midline. Here, through experimental manipulations, we addressed relationships between the polonaise movements and morphogenesis of the primitive streak, the earliest midline structure in amniotes. Suppression of the Wnt/planar cell polarity (PCP) signaling pathway maintains the polonaise movements along a deformed primitive streak. Mitotic arrest leads to diminished extension and development of the primitive streak and maintains the early phase of the polonaise movements. Ectopically induced Vg1, an axis-inducing morphogen, generates the polonaise movements, aligned to the induced midline, but disturbs the stereotypical cell flow pattern at the authentic midline. Despite the altered cell flow, induction and extension of the primitive streak are preserved along both authentic and induced midlines. Finally, we show that ectopic axis-inducing morphogen, Vg1, is capable of initiating the polonaise movements without concomitant PS extension under mitotic arrest conditions. These results are consistent with a model wherein primitive streak morphogenesis is required for the maintenance of the polonaise movements, but the polonaise movements are not necessarily responsible for primitive streak morphogenesis. Our data describe a previously undefined relationship between the large-scale cell flow and midline morphogenesis in gastrulation.

• Physics of Living Systems

Morphogenesis: The enigma of cell intercalation

Geometric criteria can be used to assess whether cell intercalation is active or passive during the convergent extension of tissue.

Be the first to read new articles from eLife

• Open access
• Published: 01 December 2021

Refocusing on sexually transmitted infections (STIs) to improve reproductive health: a call to further action

• Akaninyene Otu 1 , 2 ,
• Georges Danhoundo 3 ,
• Igor Toskin 3 ,
• Veloshnee Govender 3 &
• Sanni Yaya 4 , 5  

Reproductive Health volume  18 , Article number:  242 ( 2021 ) Cite this article

5109 Accesses

6 Citations

5 Altmetric

Metrics details

The current state of sexually transmitted infections (STIs)

STIs are infections that result from the transmission of a pathogenic organism by sexual contact [ 1 ]. Globally, STIs constitute a major burden and a significant public health challenge, driven by health systems challenges related to inadequately resourced, poor quality services on the one hand and social stigma and discrimination surrounding STIs on the other, which together discourage many people from seeking and receiving services (i.e. counselling, testing, and treatment) [ 2 ]. The World Health Organization (WHO) estimated that in 2016 the global annual incidence of four of the eight most prevalent STIs (i.e. chlamydia, gonorrhoea, trichomoniasis and syphilis) among people 15–49 years of age was 376.4 million infections [ 3 ]. These four infections are curable, unlike viral infections such as HIV, hepatitis B, herpes simplex virus (HSV) and human papillomavirus (HPV), requiring long term management and treatment.

Intersection between sexual health, reproductive health and STIs

Sexual health, which encompasses STIs, is understood as a state of physical, emotional, mental and social wellbeing in relation to sexuality. It encompasses not only certain aspects of reproductive health—such as being able to control one’s fertility and being free from sexual dysfunction and sequelae related to sexual violence or female genital mutilation—but also, the possibility of having pleasurable and safe sexual experiences, free of coercion, discrimination and violence [ 4 ].

Sexual health and reproductive health are inextricably interlinked. For example, efforts to prevent and control chlamydia have important implications for future fertility, as chlamydia is a major cause of infertility. Likewise, access to and use of contraception can impact sexual pleasure and enjoyment [ 5 ].

Despite significant strides made globally in improving reproductive health, 180 women are estimated to die daily from complications of pregnancy and childbirth arising mostly from preventable or treatable causes, such as infections [ 6 ]. STIs account for a significant proportion of infections that impact negatively on reproductive health. Major disruptions to health services arising from the COVID-19 pandemic has further aggravated the tenuous situation, particularly for vulnerable groups globally and deepening inequities in access and health outcomes [ 7 ]. These vulnerable groups include the youth, young women and migrants. Given the unequivocal recognition that reproductive health (and sexual heath) are a cornerstone of sustainable development, global agencies including the World Health Organization (WHO) and the United Nations Population Fund (UNFPA) have remained resolute in their call for the reprioritisation of reproductive health [ 7 , 8 ]. This has culminated in the launch of the Ending Preventable Maternal Mortality (EPMM) initiative by the WHO and UNFPA with established targets to be achieved by 2025 [ 6 ].

The reproductive health consequences of STIs include pelvic inflammatory disease with permanent damage to the fallopian tubes, uterus, and surrounding tissues, which can lead to infertility, mother-to-child transmission, adverse pregnancy outcomes and chronic pelvic pain. For example, STIs are estimated to cause infertility in at least 24,000 women each year in the US [ 9 ]; over 900,000 pregnant women were confirmed to have syphilis in 2012 and this resulted in approximately 350,000 adverse birth outcomes including stillbirth. In 2016, there were an estimated 473 congenital syphilis cases per 100,000 live births [ 10 ].

STIs can reduce fertility of the infected individuals via several mechanisms: by directly damaging organs and reproductive cells, by indirectly inducing tissue damage, scarring and obstruction [ 11 , 12 ]. In 2020, the estimated incident cases of STIs globally were as follows: 128 million chlamydia cases; 82 million gonorrhoea cases; 7.1 million trichomoniasis cases and 7.1 million syphilis cases [ 13 ]. Alarming increases both in gonorrhoea and syphilis is being recorded among men who have sex with men (MSM) and bisexual men [ 14 ] coupled with the increasing global incidence of drug-resistant gonorrhoea even in affluent countries such as the US [ 15 ].

HPV remains the most common viral infection of the reproductive tract with two HPV types (16 and 18) giving rise to 70% of cervical cancers and pre-cancerous cervical lesions [ 16 ]. In 2020 alone, there were a total of 604,000 new cases of cervical cancer with 341,000 deaths from cervical cancer and 1.5 million people were newly infected with hepatitis B virus [ 17 ]. HPV and hepatitis B are STIs which are preventable by vaccination. The presence of an STI magnifies the risk of acquiring or transmitting HIV by as much as two to three times [ 18 ]. HIV continues to have devastating health effects globally, having killed 36.3 million people so far with an estimated 37.7 people living with HIV at the end of 2020, over two thirds (25.4 million) of whom are in Africa [ 19 ].

Giant strides made

In 2016, the WHO proposed five strategic directions for 2016–2021 with priority actions for countries to prevent and control STIs [ 18 ]. The strategic directions were in line with the 2030 Agenda for Sustainable Development for ending STIs as a major public health issue and included: information for focused action (understanding the STI epidemic and response); interventions for impact (addressing the first dimension of universal health coverage); delivering for equity (addressing the second dimension of universal health coverage); financing for sustainability and innovation for acceleration. The focus of these strategies was primarily on three key STIs namely gonorrhoea (in view of the risk of coinfection with other STI’s and rising risk of drug-resistant gonorrhoea), syphilis (with the aim of eliminating congenital syphilis), and HPV (with a focus on vaccination to eliminate cervical cancer) [ 18 ].

Significant progress has been made with the establishment of screening and monitoring mechanisms for STIs in many countries. By 2019–2020, 97 of 110 countries (87%) surveyed by the WHO had STI surveillance in place with 64% of countries having conducted surveillance of gonococcal antimicrobial susceptibility in 2019–2020 [ 18 ]. In the same time period, 19 (25%) of 75 countries surveyed reported > 80% HPV vaccine coverage [ 13 ]. With respect to HIV and hepatitis B diagnosis, an estimated 84% of people living with HIV were aware of their HIV status in 2020 [ 20 ] while 30.4 million people living with hepatitis B knew their hepatitis B status at the end of 2019.

Advances have also been recorded with improved access to treatment of STIs. The majority of countries (103 of 111; 93%) surveyed had policies for antenatal screening and treatment of syphilis in place in 2019–2020. Moreover, 59% of countries included the HPV vaccine in the national immunization schedule [ 18 ]. In 2020, 73% of people living with HIV accessed treatment and 6.6 million people with hepatitis B received treatment in 2019 [ 18 ].

Yet many gaps remain

Despite many countries having established screening and treatment programmes for STIs, the incidence of most STIs such as chlamydia, gonorrhoea and trichomoniasis is plateauing [ 21 ]. The underlying reasons, while context-specific, are largely combination of both health systems and service delivery challenges as well as wider social and gender norms that contribute to stigma and discrimination in both communities and healthcare settings.

On the health systems side, across many settings, insufficient integration of STI services with existing and routine services (e.g. family planning, maternal health, HIV) at primary care challenges both effective service and continued reliance on vertical programmes contributes to duplication of services and challenges access and overall sustainability [ 21 ]. In addition, lack of trained health workers, laboratory capacity, adequate supplies of appropriate medicines and capacity to screen for asymptomatic infections contribute to poor quality services.

For STIs such as hepatitis B, treatment is lifelong and requires regular laboratory monitoring of hepatitis B viral load, which adds to the overall cost of controlling such an STI. However, there is evidence that testing and treatment for STIs remain cost-effective interventions [ 22 ]. Despite this, there is a seeming reluctance on the part of many governments to fund and execute STI control strategies. These issues have been given lower priority in the face of competing demands for scarce resources [ 23 ].

On the demand side, social and gender inequalities, stigma and discrimination disproportionately affect vulnerable and key populations, both in terms of risk of infection and access to STI services. These populations include adolescent girls and young women, sex workers, MSM, people who inject drugs, prisoners and transgender people [ 21 ]. In low- and middle-income countries, which account for 75–80% of STIs, poor access to effective and affordable STI services and high prevalence of drug resistant pathogens is disproportionately experienced by young people who are sexually active; migrant and displaced due to wars and natural catastrophes; people involved in transactional sex [ 22 ].

What is left to be done?

Globally, reproductive health cannot be improved without urgently accelerating progress and delivering on commitments to existing STI control strategies. Primary prevention of STIs should be upscaled to modify sexual behaviour by encouraging practices such as delayed onset of sexual debut, sexual abstinence and mutually faithful sexual relationships among communities as well as promotion of partners reduction and condom use. Long-term outcomes of primary prevention strategy should include a paradigm shift from a disease-centered approach to sexual health and reproductive health promotion with a positive attitude towards sexuality, based on the core concept of well-being, and tailored behavioural interventions linked to the evidence-based biomedical approaches in one package to prevent new cases of STIs [ 24 ].

Promotion of appropriate treatment seeking behaviour for STIs should be promoted at grassroots level. Provision of treatment of people with STIs in order to prevent further transmission among communities remains a key strategy to eliminate STIs as a public health threat. To achieve this, STI prevention and care services will need to be cascaded to the primary health care level. Intensified screening and case finding of STI should be widely adopted along with linkage to treatment and engagement in care. Vaccination activities for hepatitis B and HPV will need to be expanded by carefully addressing policy bottlenecks, cost, vaccine supply and rollout issues. Capacity building (improvement of health provider competencies) should be implemented for a wide range of actors in healthcare to support this process.

To facilitate the provision of quality and equitable STI care services at grassroots level, the WHO launched updated guidelines for the management of symptomatic STIs in June 2021 [ 21 ]. These guidelines which provide updated, evidence-informed clinical and practical recommendations for managing persons with STIs should be adopted and implemented at scale.

Targeted STI control interventions for vulnerable and key populations such as adolescent girls, MSM and people who inject drugs should be prioritised. With the current push towards elimination of some of these STIs, price reduction strategies for STI testing, vaccines and drugs are critical. More research is essential to discover safe, effective and cheaper vaccines, drugs and point of care tests for STIs and address the emerging antibiotic resistance. Greater allocation of funds for STI control activities is required from government and relevant stakeholders. Private–public partnership in the provision of STI testing and treatment should be facilitated to promote resource sharing, collaboration and economies of scale.

STIs pose behavioural, social, economic, structural, and political challenges—these multifaceted issues should be addressed by interventions at multiple points along the STI-care continuum via a combination of prevention strategies, backed by strong political and financial commitment. Only by priority setting and multisectoral public health approaches will the STI epidemic be addressed and reproductive health and rights guaranteed.

FAWCO. The impact of sexually transmitted infections (STIs) on women’s health. https://www.fawco.org/global-issues/health/health-articles/4051-the-impact-of-sexually-transmitted-infections-stis-on-women-s-health .

Starrs AM, Ezeh AC, Barker G, Basu A, Bertrand JT, Blum R, et al. Accelerate progress—sexual and reproductive health and rights for all: report of the Guttmacher-Lancet Commission. The Lancet. 2018;391(10140):2642–92.

Article   Google Scholar  

Rowley J, Vander Hoorn S, Korenromp E, Low N, Unemo M, Abu-Raddad LJ, et al. Chlamydia, gonorrhoea, trichomoniasis and syphilis: global prevalence and incidence estimates, 2016. Bull World Health Organ. 2019. https://doi.org/10.2471/BLT.18.228486 .

Article   PubMed   PubMed Central   Google Scholar  

World Health Organization. Sexual health, human rights and the law. Geneva: World Health Organization; 2015. https://apps.who.int/iris/bitstream/handle/10665/175556/9789241564984_eng.pdf .

World Health Organization. WHO guidelines for the treatment of Chlamydia trachomatis . Geneva: World Health Organization; 2016. http://apps.who.int/iris/bitstream/handle/10665/246165/9789241549714-eng.pdf?sequence=1 .

World Health Organization. New global targets to prevent maternal deaths. https://www.who.int/news/item/05-10-2021-new-global-targets-to-prevent-maternal-deaths .

World Health Organization. 6 Priorities for women and health. https://www.who.int/news-room/spotlight/6-priorities-for-women-and-health .

United Nations Population Fund. UNFPA inputs to 2021 HLPF theme and related 9 SDGs under review. https://sustainabledevelopment.un.org/index.php?page=view&type=30022&nr=2806&menu=3170 .

Hamblin J, 2013. 24,000 U.S. Women become infertile every year from undiagnosed STIs, https://www.theatlantic.com/health/archive/2013/04/24-000-us-women-become-infertile-every-year-from-undiagnosed-stis/274666/ .

Global hepatitis report 2017. Geneva: World Health Organization; 2017. https://www.who.int/hepatitis/publications/global-hepatitisreport2017/en/ .

Gimenes F, et al. Male infertility: a public health issue caused by sexually transmitted pathogens. Nat Rev Urol. 2014;11:672–87. https://doi.org/10.1038/nrurol.2014.285 .

Article   PubMed   Google Scholar  

Hart RJ. Physiological aspects of female fertility: role of the environment, modern lifestyle, and genetics. Physiol Rev. 2016;96:873–909. https://doi.org/10.1152/physrev.00023.2015 .

Article   CAS   PubMed   Google Scholar  

WHO/UNICEF estimates. Geneva: World Health Organization; 2021. https://immunizationdata.who.int/ .

Centers for Disease Control and Prevention. Reported STDs in the United States, 2017. High burden of STDs threatens millions of Americans. https://www.cdc.gov/nchhstp/newsroom/docs/factsheets/std-trends-508.pdf .

Eisinger RW, Erbelding E, Fauci AS. Refocusing research on sexually transmitted infections. J Infect Dis. 2020;222:1432–4.

World Health Organization. Human papillomavirus (HPV) and cervical cancer. https://www.who.int/news-room/fact-sheets/detail/human-papillomavirus-(hpv)-and-cervical-cancer .

Web Annex 1. Key data at a glance. In: Global progress report on HIV, viral hepatitis and sexually transmitted infections, 2021. Accountability for the global health sector strategies 2016–2021: actions for impact. Geneva: World Health Organization; 2021. Licence: CC BY-NC-SA 3.0 IGO.

World Health Organization. Global health sector strategy on sexually transmitted infections 2016–2021. Geneva: World Health Organization; 2016.

Google Scholar  

World Health Organization. HIV/AIDS. https://www.who.int/news-room/fact-sheets/detail/hiv-aids .

UNAIDS 2021. Global HIV statistics. https://www.unaids.org/sites/default/files/media_asset/UNAIDS_FactSheet_en.pdf .

Guidelines for the management of symptomatic sexually transmitted infections. Geneva: World Health Organization; 2021. Licence: CC BY-NC-SA 3.0 IGO.

Mayaud P, Mabey D. Approaches to the control of sexually transmitted infections in developing countries: old problems and modern challenges. Sex Transm Infect. 2004;80:174–82.

Article   CAS   PubMed   PubMed Central   Google Scholar  

Tordrup D, Hutin Y, Stenberg K, Lauer JA, Hutton DW, Toy M, et al. Cost-effectiveness of testing and treatment for hepatitis B virus and hepatitis C virus infections: an analysis by scenarios, regions, and income. Value Health. 2020;23(12):1552–60.

Toskin I, Bakunina N, Gerbase AC, et al. A combination approach of behavioural and biomedical interventions for prevention of sexually transmitted infections. Bull World Health Organ. 2020;98:431–4. https://doi.org/10.2471/BLT.19.238170 .

Download references

Some of the authors are present staff members of the World Health Organization. The authors alone are responsible for the views expressed in this article and they do not necessarily represent the views, decisions or policies of the institutions with which they are affiliated.

This work was pa​rtially funded by the UNDP-UNFPA-UNICEF-WHO-World Bank Special Programme of Research, Development and Research Training in Human Reproduction (HRP), a cosponsored programme executed by the World Health Organization (WHO).

Author information

Authors and affiliations.

Department of Infection and Travel Medicine, Leeds Teaching Hospitals NHS Trust, Leeds, UK

Akaninyene Otu

Department of Internal Medicine, College of Medical Sciences, University of Calabar, Calabar, Cross River State, Nigeria

Department of Sexual and Reproductive Health and Research, World Health Organization, Geneva, Switzerland

Georges Danhoundo, Igor Toskin & Veloshnee Govender

School of International Development and Global Studies, University of Ottawa, 120 University Private, Ottawa, ON, K1N 6N5, Canada

The George Institute for Global Health, Imperial College London, London, UK

You can also search for this author in PubMed   Google Scholar

Contributions

AO and SY came up with the idea for the article and drafted the first version. GD, IT and VG provided guidance and critically reviewed the manuscript. SY had final responsibility to submit. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Sanni Yaya .

Ethics declarations

Ethics approval and consent to participate.

Not applicable.

Consent for publication

Competing interests.

Sanni Yaya is Editor-in-chief of Reproductive Health.

Additional information

Publisher's note.

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ . The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/ ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Cite this article.

Otu, A., Danhoundo, G., Toskin, I. et al. Refocusing on sexually transmitted infections (STIs) to improve reproductive health: a call to further action. Reprod Health 18 , 242 (2021). https://doi.org/10.1186/s12978-021-01296-4

Download citation

Published : 01 December 2021

DOI : https://doi.org/10.1186/s12978-021-01296-4

Share this article

Anyone you share the following link with will be able to read this content:

Sorry, a shareable link is not currently available for this article.

Provided by the Springer Nature SharedIt content-sharing initiative

Reproductive Health

ISSN: 1742-4755

• General enquiries: [email protected]

What women want from women's reproductive health research: a qualitative study

Affiliations.

• 1 Carefertility, Nottingham, UK.
• 2 School of Medicine & Dentistry, University of Aberdeen, Aberdeen, UK.
• 3 Assisted Reproduction Unit, Aberdeen Maternity Hospital University of Aberdeen, Aberdeen, UK.
• PMID: 25182181
• PMCID: PMC5810697
• DOI: 10.1111/hex.12233

Background: Researchers are being urged to involve patients in the design and conduct of studies in health care with limited insight at present into their needs, abilities or interests. This is particularly true in the field of reproductive health care where many conditions such as pregnancy, menopause and fertility problems involve women who are otherwise healthy.

Objective: To ascertain the feasibility of involving patients and members of the public in research on women's reproductive health care (WRH).

Setting: University and tertiary care hospital in north-east Scotland; 37 women aged 18-57.

Method: Four focus groups and one individual interview were audio-recorded and verbatim transcripts analysed thematically by two researchers using a grounded theory approach.

Results and discussion: Most participants were interested in WRH, but some participated to promote a health issue of special concern to them. Priorities for research reflected women's personal concerns: endometriosis, polycystic ovary syndrome, menopause, fertility risks of delaying parenthood and early post-natal discharge from hospital. Women were initially enthusiastic about getting involved in research on WRH at the design or delivery stage, but after discussion in focus groups, some questioned their ability to do so or the time available to commit to research. None of the respondents expected payment for any involvement, believing that the experience would be rewarding enough in itself.

Conclusions: Involving patients and public in research would include different perspectives and priorities; however, recruiting for this purpose would be challenging.

Keywords: focus group; public involvement; women's health research.

© 2014 John Wiley & Sons Ltd.

Publication types

• Research Support, Non-U.S. Gov't
• Biomedical Research*
• Focus Groups
• Health Services Needs and Demand
• Middle Aged
• Qualitative Research
• Reproductive Health*
• Women's Health
• Young Adult

• Open access
• Published: 27 February 2022

Access to preventive sexual and reproductive health care for women from refugee-like backgrounds: a systematic review

• Natasha Davidson 1 ,
• Karin Hammarberg 1 ,
• Lorena Romero 2 &
• Jane Fisher 1  

BMC Public Health volume  22 , Article number:  403 ( 2022 ) Cite this article

11k Accesses

26 Citations

11 Altmetric

Metrics details

Globally, the number of forcibly displaced women is growing. Refugee and displaced women have poorer health outcomes compared to migrant and host country populations. Conflict, persecution, violence or natural disasters and under-resourced health systems in their country of origin contribute to displacement experiences of refugee and displaced women. Poor health outcomes are further exacerbated by the migration journey and challenging resettlement in host countries. Preventive sexual and reproductive health (SRH) needs of refugee and displaced women are poorly understood. The aim was to synthesise the evidence about access to preventive SRH care of refugee and displaced women.

A systematic review of qualitative, quantitative and mixed methods studies of women aged 18 to 64 years and health care providers' (HCPs’) perspectives on barriers to and enablers of SRH care was undertaken. The search strategy was registered with PROSPERO in advance of the search (ID CRD42020173039). The MEDLINE, PsycINFO, Embase, CINAHL, and Global health databases were searched for peer-reviewed publications published any date up to 30th April 2020. Three authors performed full text screening independently. Publications were reviewed and assessed for quality. Study findings were thematically extracted and reported in a narrative synthesis. Reporting of the review followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses recommendations.

The search yielded 4083 results, of which 28 papers reporting 28 studies met inclusion criteria. Most related to contraception and cervical or breast cancer screening. Three main themes and ten subthemes relating to SRH care access were identified: interpersonal and patient encounter factors (including knowledge, awareness, perceived need for and use of preventive SRH care; language and communication barriers), health system factors (including HCPs discrimination and lack of quality health resources; financial barriers and unmet need; HCP characteristics; health system navigation) and sociocultural factors and the refugee experience (including family influence; religious and cultural factors).

Conclusions

Implications for clinical practice and policy include giving women the option of seeing women HCPs, increasing the scope of practice for HCPs, ensuring adequate time is available during consultations to listen and develop refugee and displaced women’s trust and confidence, strengthening education for refugee and displaced women unfamiliar with preventive care and refining HCPs’ and interpreters’ cultural competency. More research is needed on HCPs’ views regarding care for refugee and displaced women.

Peer Review reports

Globally, the number of people who are forcibly displaced both within countries and across borders as a result of conflict, persecution, violence or natural disasters has grown by over 50% in the last 10 years. In 2009, 43.3 million people were forcibly displaced, increasing to 79.5 million at the end of 2019 [ 1 ]. Of those, 45.7 million comprise internally displaced people, 26 million refugees and 4.2 million asylum-seekers [ 1 ]. Forcibly displaced people include those who have meet the United Nations criteria for being a refugee [ 2 ], those seeking asylum who are not yet granted refugee status and internally displaced people who have fled their region of origin within their country but have not crossed an international border. In general, refugee and displaced people with past and current migration experiences are considered vulnerable members of the community. The experiences and potential vulnerabilities of women and girls differ significantly from those of men and boys. Women are often afforded lower social status than men which places them in a position of dependency to men. Lack of educational opportunities make it more difficult for women to access decision-making positions and safe employment opportunities. At least half the forcibly displaced people are women and girls [ 3 ] with many living for protracted periods in refugee camps in poor conditions [ 4 ]. We acknowledge the importance of person-first language but in the interests of brevity, throughout this paper we refer to women from refugee-like backgrounds as “refugee and displaced women”. This term signifies the context of women’s refugee-like backgrounds and experiences. By definition refugee and displaced women have fled their country or region of origin. The refugee experience places these women in situations which create vulnerability.

Pre-migration experiences caused by violence, torture, rape or witnessing the torture or killing of family or friends are associated with poor psychological and physical health outcomes [ 5 ]. Postmigration stress also contributes to poor general health, particularly in refugee and displaced women [ 6 ]. Most refugee and displaced women have not voluntarily chosen to leave their country of origin, often depart at short notice, have lengthy journeys within their own country or crossing international borders. They may be separated from family members in transit or at the time of resettlement, have reduced social support systems, be survivors of torture and have lost most of their material possessions, wealth and status [ 7 ]. Further, access to ongoing, familiar health services is lost [ 8 ]. In their systematic review of young women in Africa, Ivanovna and colleagues [ 9 ] concluded that access to and availability of sexual and reproductive health (SRH) care is often limited in low-income country humanitarian settings. As a result, refugee and displaced women are at risk of adverse health outcomes such as unintended pregnancy due to a lack of access to contraception [ 10 , 11 ], lack of access to abortion services [ 12 ], sexually transmitted infections [ 13 ] and sexual and gender-based violence [ 14 ].

Universal publicly available access to SRH care has been recognized by the World Health Organisation as a priority in global health [ 15 ]. It is also of key importance in Sustainable Development Goal 3 which seeks to ensure good health and wellbeing for all and Sustainable Development Goal 5 which seeks to achieve gender equity [ 16 ]. In World Bank classified [ 17 ] low-income countries however, women’s health services, particularly preventive SRH care including contraception, cervical and breast cancer screening and human papilloma virus (HPV) vaccination is often not available or not of a quality that meets the World Health Organisation framework for human rights standards [ 18 ]. A fact further supported at the International Conference on Human Rights in 2013 [ 19 ]. Poor quality relates to lack of universal access to SRH care and scarce human and financial resources [ 20 ] in addition to lack of patient centred care [ 21 ] and respectful, effective and efficient communication [ 22 ]. The concept of an Essential Package of Health Services was initiated by World Health Organisation in 2014 to progress universal access to SRH. Its aim was to provide priority health services for vulnerable populations in fragile settings, where needs often exceed available resources [ 15 ]. The Essential Package of Health Services across most low- and middle-income countries excludes many SRH services [ 23 ]. An analysis based on low- and middle-income countries’ health services [ 20 ] showed almost all countries included maternal health care and some had SRH care for family planning and sexually transmitted infection/human immunodeficiency virus prevention and management. However, the majority did not mention infertility, or screening for cervical and breast cancers. By contrast, most women in high-income countries have free or low cost universal SRH access in primary health care including screening for reproductive cancers [ 24 ]. The poor quality of SRH care but also a lack of available services, leads to low utilisation of these services [ 25 ] further contributing to barriers refugee and displaced women may experience in accessing care [ 26 ]. In 2004, a global evaluation of reproductive health services for refugees and internally displaced people concluded that most people affected by conflict lack adequate SRH care. Refugee and displaced women have been overlooked in humanitarian and in transit low-income country settings and consequently have unmet SRH needs and poor SRH outcomes [ 27 ].

Following resettlement refugee and displaced women’s use of primary health care is limited. A systematic review by Hadgkiss and Renzaho [ 28 ] examining asylum seekers residing in the community in high-income countries found they had higher tertiary level health service use but lower preventive health service use than the host population. Annual hospitalisation rates among asylum seekers in the Netherlands varied from 12 to 20% compared with 7% in the general population. With regard to use of preventive health services, 25% of asylum seekers had undergone a cervical pap screening test compared with 62% in the host population [ 28 ]. Similarly, Sarría-Santamera and her colleagues compared use of health services between populations and found over-use of emergency services and under-use of preventive care services among immigrants and refugees compared to host populations [ 29 ].

To date research on refugee and migrant women’s access to SRH care has mainly focused on pregnancy, childbirth and post-partum health care [ 30 , 31 , 32 , 33 , 34 , 35 ]. Others have focused on people with refugee-like backgrounds experiences in general practice [ 36 , 37 ]. Few systematic reviews on the topic of SRH disaggregate findings pertaining to refugees, internally displaced people and asylum seekers from those of other immigrants [ 35 , 38 ]. Refugee and displaced women have particular needs when engaging with the SRH care [ 39 ].

Primary HCPs are key to ensuring SRH care needs are meet, yet understanding of HCPs’ perspectives on refugee and displaced women’s access to care is limited. One systematic review of qualitative studies explored challenges and facilitators for HCPs providing general primary healthcare for refugees and asylum seekers in high-income countries [ 40 ]. This review identified multiple barriers experienced by HCPs in providing care for refugees and asylum seekers. Factors related to HCPs competency and responsiveness can contribute to the underutilisation of SRH care by refugee and displaced women [ 41 ]. Brandenberger and colleagues [ 38 ] go one step further and identify the need for comprehensive training of HCPs to understand the specific requirements of migrants and refugees.

There is a gap in the literature that explicitly addresses access to preventive SRH care outside pregnancy and maternal health among refugee, internally displaced and asylum seeker populations. It is not known what the experiences of access to preventive SRH care and provision of care are for refugee and displaced women nor the views of HCPs delivering care to this group. The aim of this review was to synthesize the evidence on barriers to and enablers of access to preventive SRH care from the perspectives of refugee and displaced women and their health care providers.

The systematic review was registered with PROSPERO database in advance of the search (ID CRD42020173039). Reporting of the review followed the Preferred Reporting Items for Systematic Reviews and Meta-Analysis recommendations [ 42 ].

Selection criteria

Inclusion and exclusion criteria.

The inclusion criteria were studies that have been peer-reviewed, used qualitative, quantitative or mixed methods and have investigated barriers to or enablers of access to SRH care from the perspective of refugee and displaced women defined as refugees, asylum seekers and internally displaced people; or HCPs’ views about providing SRH care to refugee and displaced women in primary health care settings. Exclusion criteria were investigations of maternity or obstetric care (Additional File 1 ).

Search strategy

The search strategy was devised by ND with the assistance of a specialist information analyst, LR. The MEDLINE, EMBASE, PsycINFO, CINAHL and GLOBAL HEALTH databases were searched for peer reviewed papers published any date up to 30th April 2020. The search strategy was based on the Sample, Phenomenon of Interest, Design, Evaluation, Research type (SPIDER) tool [ 43 ] to optimise identification of relevant articles. The detailed search strategy is documented in Additional file 2 .

Search limits included: English language and women aged 18 to 64 years. No date or country of setting limits were applied. The included articles’ reference lists were hand-searched for additional relevant articles. Articles identified in the search were exported to EndNote X9. After removal of duplicates the remaining articles were exported to Covidence Systematic Review Management Platform [ 44 ].

Titles and abstracts were screened for relevance by ND and articles that did not meet inclusion criteria were removed. Full text of the remaining articles were reviewed independently in Covidence [ 44 ] by ND, KH and JF. Any disagreements were resolved through discussion to come to a final decision.

Data extraction

Study characteristics were extracted by ND using a pre-set proforma in Microsoft Excel. Data were extracted on the following key characteristics: author, title, year published, country of study, study aim, theoretical framework, study design, sampling technique, participant characteristics (including age group, country of origin, migration category and time since arrival), sample size, data collection method, data analysis, outcome measures, SRH topic covered, and key findings.

Quality assessment

Study quality was assessed using the Kmet Standard Quality Assessment Criteria for Evaluating Primary Research framework for appraisal tool [ 45 ]. The Kmet tool provides a systematic reproducible and quantitative means of appraising qualitative and quantitative studies. Mixed-methods studies were appraised using both the qualitative and quantitative quality assessment criteria. In addition, for all studies, evidence of human research ethics committee approval was scored 0 for ‘no ethics approval’ and 1 for ‘has ethics approval’ approved by a formally constituted ethics committee.

Data synthesis

Narrative synthesis is a systematic approach to searching for and quality appraising evidence. In systematic reviews it is used to explore relationships within and between study findings. Narrative synthesis is an area of emerging research in the field of systematic reviews, however there are broad guidelines which have been followed to guide this review process [ 46 ]. This method was reported because characteristics of the study designs and outcomes were too diverse to yield a meaningful summary of findings using a meta-analysis.

The main findings and conclusions were grouped and coded inductively into descriptive themes that emerged from the data within the two categories of “barriers to” and “enablers of” access to SRH care, as defined by the review aim. Findings were only coded if they related to barriers to or enablers of SRH care. Data were further grouped into the SRH topic. Findings were coded to iteratively develop and refine descriptive themes, with each study able to contribute new themes. Following the organisation of these descriptive themes, categorisation and generation of higher-level analytical themes were devised. Quantitative data were described separately and used to complement or refute the qualitative evidence.

Systematic database searches yielded 4083 articles. 28 studies were included in the review (Fig.  1 ).

Flow diagram showing the process of study selection (adapted from [ 42 ])

Study characteristics

Study characteristics and main findings are shown in Tables  1 and 2 .

Study locations

Of the 28 studies, 13 were conducted in the USA [ 48 , 53 , 55 , 56 , 57 , 59 , 60 , 61 , 63 , 69 , 72 , 73 , 74 ], two each in Australia [ 62 , 64 ], Jordan [ 52 , 68 ], Lebanon [ 49 , 50 ] and Canada [ 70 , 71 ], one each in Congo [ 66 ], Israel [ 54 ], Netherlands [ 67 ], Pakistan [ 65 ], South Korea [ 65 ], Thailand [ 47 ] and one was a multi country study which included Bangladesh, Jordan, Djibouti, Kenya, Malaysia and Uganda [ 51 ].

Data collection methods

Studies were qualitative ( n  = 16), cross sectional surveys ( n  = 8) and mixed methods; a combination of either focus group discussions (FGDs) or semi structured interviews and surveys ( n  = 4). Of those using qualitative methods, nine involved FGDs [ 49 , 50 , 53 , 55 , 56 , 57 , 59 , 60 , 61 ], four semi structured interviews [ 49 , 52 , 58 , 63 ], three in-depth/key informant interviews [ 47 , 56 , 64 ], three both FGDs and in-depth interviews [ 48 , 51 , 54 ] and one used a novel storytelling method [ 62 ]. Of the 12 studies using quantitative methods, nine used face-to-face interview based surveys in respondents’ homes [ 47 , 51 , 65 , 66 , 68 , 70 , 73 ] or in a medical clinic [ 72 ] and one used an online survey [ 57 ]. The remaining studies used population-based data sources (electronic medical and national immigration record databases) [ 67 , 71 ] and review of medical charts [ 69 ].

Study samples

Twenty-six studies focused on refugees [ 47 , 48 , 49 , 50 , 51 , 52 , 53 , 55 , 56 , 57 , 58 , 59 , 60 , 61 , 62 , 63 , 64 , 65 , 67 , 68 , 69 , 70 , 71 , 72 , 73 , 74 ], one on asylum seekers [ 54 ] and one on internally displaced persons [ 66 ]. Five studies included perspectives of HCPs (not further specified) [ 48 , 51 , 74 ] and one each of physicians [ 54 ] and nurses [ 50 ]. Ethnic groups included Somali /Somali Bantu in seven studies [ 48 , 53 , 55 , 56 , 60 , 72 , 73 ], Syrian [ 49 , 50 , 52 ] and Bhutanese [ 57 , 59 , 64 ] in three studies each, and one each in Afghani [ 65 ], Albanian [ 70 ], Burmese [ 59 ], Cambodian [ 47 ], Congolese [ 66 ], Eritrean [ 54 ], Iraqi [ 61 ], North Korean [ 58 ], Palestinian [ 68 ], West African [ 62 ] or a combination of these ethnic groups [ 51 , 63 , 67 , 69 , 71 ]. Participants’ ethnicity was not described in one study [ 74 ]. Qualitative data were available from 994 participants (samples ranged between 5 and ~ 65) and quantitative data were available from 469, 984 participants (samples ranged between 42 and 455,684).

Recruitment methods

Recruitment methods were described in all but one qualitative study [ 51 ]. They included convenience sampling with [ 48 , 52 , 53 , 54 , 55 , 61 , 62 , 63 ] or without snowball sampling [ 49 , 60 ] through community or health centres, migrant resource centres or places of worship. Purposive sampling was used in studies of refugee and displaced women and HCPs in various primary health care settings [ 50 , 51 , 56 , 58 , 62 ]. Several studies engaged community gatekeepers such as community activists, group leaders or women community partners in recruitment of participants [ 47 , 50 , 54 , 55 , 59 ]. Of eight quantitative studies, four recruited convenience samples [ 66 , 72 , 73 , 74 ], two obtained data from random samples of households [ 65 ] and families [ 70 ] and two employed medical record searching [ 67 , 69 ].

The quality of the 28 studies varied considerably with KMET scores ranging between 0.60 and 1.0 for qualitative and 0.50 to 1.0 for quantitative studies. Twenty-two studies reported obtaining ethics approval and six did not. Quality assessment is summarized in Additional files 3 and 4 .

Type of SRH topic examined

All but two studies included at least one of the three main SRH topics: contraception [ 47 , 48 , 49 , 50 , 51 , 52 , 53 , 54 , 55 , 56 , 65 , 66 , 67 , 68 ], cervical cancer screening [ 57 , 58 , 60 , 62 , 71 , 74 ] or breast screening [ 63 , 64 ] with the remaining three examining a combination of these [ 61 , 69 , 70 ]. One examined access to primary care for women who had experienced female genital cutting of different types [ 73 ] and one women’s preference for providers of general physical examinations which include breast and pelvic examinations [ 72 ].

Thematic extraction of findings

Table  3 summarises the three main themes and 10 subthemes identified in this review.

Interpersonal and patient encounter factors - patient interactions with health care systems and HCPs

Knowledge, awareness and use of preventive srh care.

Contraception Almost all studies on contraception reported some lack of knowledge, awareness and barriers to uptake among women [ 47 , 48 , 49 , 51 , 52 , 53 , 54 , 56 , 66 , 68 ]. Negative beliefs or misperceptions about side effects of contraceptive methods were evident in three high quality qualitative studies of Somali and Syrian women residing in the US and Lebanon [ 49 , 53 , 56 ]. Inaccurate beliefs about contraception included; consequent inability to conceive after discontinuing contraception and decreased sex drive [ 53 ], and fear that modern contraceptives cause infertility [ 56 ], menstrual irregularities and mood disorders [ 49 ]. Six studies conducted in Jordan, Democratic Republic of Congo, Thailand and other low-income countries assessed whether women had ever used contraceptives [ 47 , 51 , 66 , 68 ], their awareness of methods of contraception [ 51 ], and information received about contraception [ 66 ]. A high quality qualitative study of Syrian women in Jordan found they had high awareness of modern contraceptive methods but limited access to contraceptive counselling and services [ 52 ]. High awareness and low use of contraception was more evident in low compared with high-income countries due mainly to overburdened health services, cultural pressures regarding fertility, poorly trained service providers, health service disrupted by conflict, distance to service delivery points, cost of transport, religious opposition, language barriers with providers, and provider biases [ 51 , 52 , 66 ]. In refugee camp settings contraceptive knowledge was moderate in Afghan refugee women in Pakistan, Rohingya refugee women in Bangladesh [ 51 , 65 ] to high in internally displaced people in the Democratic Republic of the Congo [ 65 , 66 ] while actual usage was low in Cambodian refugees in the Khao Phlu Camp in Thailand [ 47 , 66 , 70 ]. Where the value and knowledge of contraception was moderate to high women reported approval of their friends and spouses. Women having discussions with their husbands about the number of children they should have supported contraceptive use [ 65 ]. One study reported that women themselves made the decision to use contraception [ 66 ]. Conversely, barriers for contraceptive use included the husband making decisions about the wife’s access to birth control, fear of side effects, lack of information, having a current illness, expense, being too old, being unable to obtain them and husband’s refusal to permit contraceptive use [ 47 ].

Cervical and breast cancer screening Knowledge, awareness and/or uptake of cancer screening was reported in nine studies conducted in high-income countries in the US [ 59 , 60 , 61 , 69 ], Australia [ 62 , 64 ], Canada [ 70 ] and South Korea [ 58 ]. Women’s understanding of causes of disease and disease prevention was reported to be limited in most studies [ 57 , 58 , 59 , 60 , 61 , 62 , 64 , 69 ]. While some participants resettling in the US and Australia had heard of cervical cancer in four studies of Somali and Iraqi women [ 56 , 60 , 61 , 62 ], studies of other ethnic groups had variable and at times inaccurate knowledge of cancer aetiology [ 59 , 60 , 61 , 62 ], cancer prevention [ 57 , 58 , 61 , 62 ] and the purpose of screening [ 64 , 69 ]. One study in the US reported Iraqi women would undergo screening only if provided with explanations of the exam and its necessity [ 61 ] which corroborates the importance women placed on doctors’ screening recommendations [ 49 , 64 ]. A study of HCPs’ views in the US reported that women from various ethnicities were unfamiliar with tests to identify disease at its early stages [ 74 ].

Less knowledge and awareness of HPV and HPV vaccination compared with cervical screening was evident in two US studies of Somali and Bhutanese women [ 57 , 60 ] with varying understanding of whether the virus causes cancer [ 60 ] (HPV vaccination has been offered in the US since 2006). Cross sectional surveys measuring rates of breast and cervical screening among refugee and displaced women found lower screening rates when compared with the host country populations of the US and Canada [ 57 , 69 , 70 ]. Barriers to screening identified in Somali and Bhutanese refugee women and refugee women from other ethnic groups were limited or no knowledge regarding cervical cancer and its prevention [ 57 , 60 ].

Perceived need for preventive SRH care

Unfamiliarity with preventive care and low perceived need for it was apparent in seven studies of Somali, Iraqi, Bhutanese and North Korean women conducted in the US [ 56 , 57 , 59 , 61 ], Australia [ 62 ], Canada [ 70 ] and South Korea [ 58 ]. The belief that only symptomatic women need to undergo screening was common in eight studies [ 56 , 57 , 58 , 59 , 62 , 63 , 64 , 69 ], with absence of symptoms being one reason for not having cervical [ 58 ] or breast screening [ 64 ]. This resulted in women not seeking preventive care [ 62 , 64 ] or delaying seeking care until a problem became unbearable [ 61 ]. One high quality study of Bosnian, Iraqi and Somali women found doctors in some countries of origin focused only on acute, not preventive care [ 63 ]. A study of US HCPs' views found that refugee women often sought care only when symptomatic [ 74 ].

Language and communication

Access to care related to communication was reported in four studies on contraception [ 48 , 51 , 54 , 56 ], three on cervical and breast cancer screening [ 57 , 59 , 64 ] and one on female genital cutting [ 73 ]. Limited English language proficiency [ 57 , 59 , 64 , 73 ] and poor literacy impacted on access to care [ 64 , 73 ] and were challenging for HCPs and Somali and Eritrean women alike [ 48 , 54 , 74 ]. In two studies the real communication barrier was reported to be that telephone or in person interpreters did not understand the concepts being discussed [ 48 , 59 ]. Other studies reported few, if any, translation services available in any healthcare facilities [ 54 , 59 ], HCPs being unaware of language requirements [ 48 ] and women feeling rushed and unable to see or hear telephone interpreters [ 59 ]. Communicating with interpreters and providers during reproductive health consultations was reported to lead to embarrassment, shyness or stigma for some women [ 47 , 48 , 59 , 61 , 63 , 64 ].

Health care system factors – health system factors and their impact on outcomes

Health care provider discrimination and lack of quality health resources.

HCP discrimination described as poor communication and perceived lack of care [ 54 ], judgemental approaches and disrespectful behaviour in the provision of contraception impacted on refugee women in low income country settings in access to care [ 50 ]. A lack of affordable and acceptable methods of contraception offered to women in Jordan and other refugee camp settings, [ 51 , 52 ] was also identified as a barrier to contraceptive use in studies of Syrian and Eritrean women in low-income country settings [ 50 , 51 , 52 , 54 ]. HCPs in Lebanon reported their own discrimination in the form of negative attitudes towards Syrian women; one study suggesting women were irresponsible, unreliable and ignorant when seeking care [ 50 ]. Other studies in low-income countries indicated poor or second-class treatment occurred due to poor communication, inadequate length of time required address women’s needs, providers own attitudes and fears towards asylum seekers in Israel [ 54 ] and gaps in their own skills and knowledge in providing care [ 51 ].

Studies of HCPs’ views conducted in low-income countries of Lebanon, Israel and others found limited acceptable contraceptive methods impacted on accessing care [ 50 , 51 , 54 ]. An associated lack of quality resources and perceptions of low-quality care such as provision of incorrect information, incorrect prescriptions, poor hygiene in SRH care were cited in high- and low-income settings [ 51 , 54 , 55 ]. Women’s negative clinical encounters with HCPs in low-income country settings coupled with fear of maltreatment when seeking contraception, unwillingness to have contraception prescribed and time constraints were reported experiences of discrimination [ 47 , 50 , 54 ]. Discrimination appears to have continued following resettlement. One Dutch study reported fewer discussions about contraception between General Practitioners and refugee and displaced women compared with other migrants or host country populations [ 67 ]. Another US study reported poor recognition of women’s experience of physical pain by their HCP [ 61 ]. Fear and mistrust in seeking care as a result of trauma, sexual violence and bad experiences of screening and diagnosis were also evident among refugee women of various ethnicities in studies conducted in the US and Australia [ 59 , 62 , 63 ].

Financial barriers and unmet need

Cost was cited as the main barrier to preventive care by many women [ 49 , 50 , 54 , 59 ] and HCPs [ 54 ] particularly in low-income settings where access to free healthcare was not universal. Low awareness of the availability of free contraceptive services was cited in two studies in Lebanon and Cambodia [ 47 , 49 ]. Afghani and Palestinian refugee women in informal settlements and refugee camps in neighbouring countries were between two and 13 times more likely to use contraceptives if costs were subsidised [ 65 , 68 ]. A South Korean study of women refugees from North Korea found cost deterred women from cervical screening [ 58 ]. In one high quality study, lack of health insurance had a strong association with women’s access to maternal and reproductive health care across the continuum of primary care services including family planning and was the most common reason for postponing a visit to primary care [ 73 ].

Health care provider characteristics

In several studies women from different ethnic groups expressed concern about receiving care from male HCPs [ 58 , 59 , 62 , 72 ] with some choosing to forgo care rather than discuss reproductive health topics or undertake cervical screening [ 48 , 71 ]. Odunukan and others found Somali women preferred a woman provider for physical examinations [ 72 ]. HCPs showed insight into their own limitations with regard to caring for refugee and displaced women. Despite women being receptive to screening information in early resettlement, HCPs reported that lack of knowledge, concerns about the timing of information delivery and their own discomfort were barriers to discussing screening [ 74 ].

Health system navigation

The complexity of healthcare systems impacted on access in seven studies, though the nature of the difficulties varied according to low- or high-income country setting [ 47 , 51 , 54 , 57 , 59 , 63 , 69 ]. In low-income settings distance to service point, lack of transport and the fragmented nature of service provision [ 51 , 54 ] were identified as barriers to contraceptive care even when clinic opening times/ locations and contraceptives were available [ 54 ]. Navigating and understanding the health system and making appointments were barriers reported in high-income host countries [ 59 , 63 , 69 ].

Sociocultural factors and the refugee experience - the influence on outcomes of refugee and resettlement experiences

Family influence.

Ten studies in both high- and low-income country settings suggested family influence affected women’s utilisation of contraception, breast and cervical screening [ 47 , 48 , 49 , 50 , 51 , 52 , 53 , 55 , 58 , 60 ]. Husband’s resistance to birth control and having the final decision about contraceptive use [ 49 , 51 , 53 ] impacted on access. Acceptance by women about the dominant role of the male partner in the decision-making [ 50 , 52 ], family’s interference [ 49 ] as well as deferral to HCPs decision making [ 48 ] also impacted on contraceptive use across high and low-income countries. HCPs in Thailand reported that Cambodian women were considered candidates for contraception only after approval from their husbands [ 47 ] despite women wanting to stop or delay childbearing [ 47 ]. Conversely, a Jordanian study of displaced Palestinian women serviced by the United Nations Relief and Works Agency found they had greater access to health-related resources such as contraception than the host population [ 68 ].

Religious factors

Religious opposition to contraception was apparent in high and low-middle income country settings [ 48 , 51 , 53 , 56 , 66 ]. It was taboo for a woman to state she did not want more children [ 53 ], nor to use modern birth control as it was forbidden by religion [ 48 ]. Religious teachings actively discouraged modern contraceptive use in five of the six population groups included in one multi-country study [ 51 ]. The importance of marriage and fidelity for Cambodian women in Thailand created a barrier to using contraception [ 47 ]. However, in other ethnic groups such as internally displaced Congolese women, religious opposition to contraception was low [ 66 ]. Amongst Somali women resettling in the US, contraception was more acceptable when framed as temporary assistance for birth spacing as this agreed with the tenets their religion [ 55 ]. SRH services differ in each resettlement country. This may provide insight on why the barriers to contraception varied across ethnicity and host country. HCPs in the US reported that despite there being strong opposition to contraception in Somali culture and religion, they asked for and used contraception upon resettlement [ 48 ].

Cultural attitudes

Traditional cultural attitudes towards fertility influenced modern contraceptive use following displacement [ 51 , 52 , 56 , 73 ]. In one qualitative study of Syrian women in Jordan, pressure to marry and begin childbearing early was the main barrier for some (young and unmarried) women but not others [ 52 ]. In Somali culture, one US study reported that contraception is not discussed with young unmarried women and girls as pre-marital sex is stigmatized and disapproved of [ 56 ]; a finding supported by another study among unmarried Iraqi, Burmese, Rohingya, and Somali women in refugee resettlement camps in several low-income countries [ 51 ].

Engagement with HCPs was also reported to influence access to contraception. In a group of Somali bantu women in the US considerable cultural deference given to authority figures and an accompanying lack of self-advocacy in interactions with HCPs influenced access [ 48 ]. Tanabe and colleagues [ 51 ] reported that emergency contraception was offered to survivors of sexual assault by HCPs working in a gender-based violence program in refugee resettlement camps in low-income countries. However, they reportedly disapproved of making emergency contraception available for non-sexual assault cases, citing it could promote promiscuity [ 51 ]. For Somali women resettled in the US, being circumcised was found to impede entry into the health system and access to primary HCPs [ 73 ].

Positive relationships with and positive attitudes towards doctors and other HCPs were reported to improve access to care by Burmese and Bhutanese arrivals in the US [ 59 , 63 ]. A key theme for women from these ethnic groups was the preference for women providers due to the cultural considerations of modesty and privacy and the association with honour and virtue. Other studies in the US and Jordan found the presence of trusted woman providers and interpreters improved the cultural acceptability of services and increased uptake of contraception and cervical screening [ 52 , 59 , 71 , 74 ]. Intervention strategies to promote cervical screening and HPV vaccination were identified in three studies. They were language and culture specific web, telephone and community-based programs [ 60 ], free biennial screenings [ 58 ] and screening self-collection which is a particularly effective intervention for refugee and displaced women for reasons outlined above [ 62 ]. Congolese women resettled in the US and Syrian women resettled in Lebanon reported more equal relationships and increased empowerment regarding women’s changing roles in decision making about contraceptive use following resettlement [ 50 , 55 ]. Desire for educational achievement and the absence of extended family were identified as factors facilitating contraceptive use in one US study of Somali women [ 56 ]. Support from husbands in health decisions, encouragement from partners and other family members were reported to impact positively on women’s decision to have cervical screening in the US and Canada [ 58 , 60 ]. Interpreters conveying educational messages about cervical screening and HPV vaccination were reported to increase take-up of screening [ 57 , 60 ]. Furthermore, interpreters in the US with some medical knowledge who were members of the Somali refugee community and acted as ‘refugee mentors’ improved access to care [ 73 ].

To our knowledge this is the first systematic review of the evidence that explicitly addresses access to preventive SRH care for refugee, asylum seeker and internally displaced women. Most research has focused on identifying barriers, much less on enablers of access to care. There was consistent evidence about three factors impacting on access: patient experiences of clinical encounters, the host countries’ healthcare systems and the sociocultural context of a refugees’ journey.

There are few investigations of HCPs’ perspectives and their experiences of providing SRH care for refugee and displaced women. This limits the opportunity to ascertain consistencies and inconsistencies between refugee and displaced women and HCPs’ views. Most investigations were of refugees with only one each of internally displaced people and asylum seekers limiting the opportunity to compare the differences between these groups.

Strengths and limitations of the systematic review

A comprehensive search of five databases was conducted using a published protocol. It was supplemented by citation searches, so all relevant studies were likely to have been identified. Study selection bias was minimised by having pre-set inclusion criteria and having three authors undertake full text screening independently, with differences in opinion resolved in discussions among all authors. Two authors independently assessed the quality of the included studies using a well-established quality assessment tool [ 45 ].

The varied study designs, and their use of qualitative, quantitative and mixed methods precluded meta-analysis of findings. However, the inclusion of methodologically diverse studies and the narrative synthesis enabled a comprehensive understanding of SRH care access for refugee and displaced women. The foundation of the qualitative evidence was complementary to quantitative results, presenting a complete picture of women’s experiences. For instance, quantitative studies estimated prevalence of contraceptive knowledge, contraceptive information provision, and prevalence of use of contraception amongst refugee and displaced women. Whereas, qualitative studies elucidated the reasons why women’s uptake of contraception was low in some settings. Qualitative studies also described women’s views on their decision to use contraception and perceptions of service availability, accessibility, and quality.

Similarly, quantitative studies established rates of breast and cervical screening as well as cancer knowledge and awareness among refugee and displaced women. Whereas qualitative studies provided details on the overlapping complexities and context of why women were aware of breast and cervical screening but had not accessed the services, despite its availability in high income countries.

A strength of the narrative synthesis is that it enabled overlaying of themes across studies. It also allowed the comparison of findings and relationships between studies. When interconnected points of similarity are identified and shaped in a narrative synthesis, findings are likely generalisable and can be used to inform policy and practice [ 75 ].

The exclusion of non-English language articles may have meant that relevant publications in other languages were not included. We therefore acknowledge that the included articles may not reflect all cultural perspectives. Furthermore, it is possible that the searches did not identify studies where refugees, asylum seekers or internally displaced people were referred to as ‘migrants’ or ‘immigrants’. The selected studies focused mainly on women with refugee status already determined in the destination country. There may be additional barriers for internally displaced people and asylum seekers that are not described fully in this review due to the limited number of studies of women in these groups. The limited number of internally displaced people and asylum seeker studies also makes it difficult to draw subgroup comparisons.

Strengths and limitations of the included studies

Overall, the quality of the studies was high with none judged as poor quality. Study designs and methodologies were appropriate for the studies’ aims and closely aligned with their outcome measures. A strength of both qualitative and quantitative studies was that most data came from primary sources - the women themselves, through a variety of methods. The definition of ‘refugee’ was consistent across studies which suggests the results reflect the experiences of refugee and displaced women.

Of the qualitative studies, few reported on the quality assessment criteria of “reflexivity”. Reflexivity is the acknowledgement of cultural differences and asymmetry in the researcher - participant relationship and how these may affect the study method used, participant recruitment, and study findings and conclusions [ 76 ].

Methodological quality

Many studies used convenience sampling strategies. This may have resulted in an overrepresentation of women already seeking care, or a bias toward those with greater ability to navigate the health system. The studies would more accurately represent the factors impacting on access to care had recruitment gone beyond and included community members yet to engage with health and community services. Qualitative studies used either focus groups or interviews; methods considered the most appropriate for eliciting views on sensitive topics in vulnerable populations [ 77 , 78 ]. Studies used face to face bilingual researchers or interpreters, a recognised method for overcoming challenges of participants low literacy and/or low health literacy [ 79 ].

Quantitative studies were strengthened by using validated survey instruments translated into participants’ language. However, some instruments had not been cross-culturally validated and back translated. Most surveys were administered individually and verbally, modes of delivery considered the least burdensome for those with low literacy [ 80 ].

Overview of findings

There are many barriers to SRH care in both high and low- and middle-income country settings, including women’s low perceived need for preventive care, cultural attitudes and beliefs about family planning, cervical and breast cancer screening and HPV vaccination, stigma and shame surrounding women’s access to and use of SRH care services, discriminatory practices, lack of women HCPs, culturally competent care, and language barriers. However, our review indicates that many barriers are exacerbated by the refugee context and that additional barriers to SRH exist in LMIC settings. Deficiencies in infrastructure and transport, costs of transport to access services, and fragmentation of the health care system, especially in refugee camp settings and in poorly resourced resettlement countries, limit women’s access to SRH care and support. Male partners’ influences in decision-making about women’s SRH can limit access to contraceptive counselling and services. Health provider biases in providing contraception, poor awareness of SRH services, a lack of privacy and confidentiality, and respectful and woman-friendly SRH services were other barriers in many low- and middle-income resettlement settings.

Conversely, enablers to SRH care were mainly reported in high income countries. Resettlement in high income settings found women’s agency and self-determination are highly valued and are reflected in principles of service provision including for women who are refugees when accessing SRH. This was probably reflected in women reporting greater ownership of their SRH care, [ 48 ], increased equality in their personal relationships, [ 55 ] and more positive relationships with their HCPs [ 59 , 63 ].

Patient experiences of clinical encounters

The breadth of the studies reviewed was reflected in the seventeen different cultural and ethnic backgrounds identified conducted across sixteen high- and low-income countries. Despite this diversity, similar patterns of access to SRH care were reported. One consistent finding was that unfamiliarity with preventive SRH care and low health literacy impacted on accessing care. Key components of health literacy were identified throughout the review; difficulties navigating the health system, lack of knowledge of disease aetiology, poor health care practices, limited sense of self-advocacy and the challenges of taking ownership of one’s health. These factors were exacerbated by women’s lack of autonomy and this quantitative study found both physical and emotional domestic violence had a significant impact on refugee women receiving contraception [ 68 ].

Communication barriers were consistently highlighted. Irrespective of women’s ethnic background or host country language barriers coupled with poor cultural competence in service provision impacted on access. Communication barriers are known to create difficulties negotiating health systems [ 81 ] and decrease the quality of healthcare once refugee and displaced women are engaged in the system [ 82 , 83 ]. The lack of and poor quality of interpreters as well as interpreters’ lack of health/SRH knowledge were also highlighted [ 48 ]. When discussing SRH, engaging qualified medical interpreters is preferred by refugee and displaced women [ 84 ] and has been shown to enhance the delivery of SRH care to women with limited English proficiency [ 85 ].

Host countries’ health care system

Women consistently reported experiencing discrimination and disrespectful care though this was more evident in low-income countries informal resettlements arrangements [ 50 , 51 , 54 , 61 ]. Cultural competence is the ability to participate ethically and effectively in personal and professional intercultural settings. It requires being aware of one’s own cultural values and respectful of others values, beliefs, traditions and customs [ 86 ]. Culturally competent practice impacts on health care experiences but is challenging for many HCPs [ 7 , 87 ]. Poor cultural awareness results in incorrect assumptions about refugee health needs which in turn results in decreased quality of health care and low health service utilisation [ 88 ], which was highlighted in both high- and low-income countries in this review.

Gender discordance is the discrepancy between the gender of the patient and the HCP [ 89 ]. Patient - provider gender discordance was a consistent barrier across SRH topics, ethnic groups and host country settings. Being seen by a woman provider was a key influencing factor in accessing SRH care [ 50 , 58 , 64 ]. The review highlighted that women were more likely to seek SRH care and be more comfortable expressing their needs with women HCPs and interpreters.

Sociocultural context of a refugees’ journey

Many sociocultural barriers also exist for women from migrant backgrounds who are not refugees [ 90 ]. However, refugee and displaced women may experience violence, trauma in their countries of origin and prolonged and dangerous in transit journeys prior to arrival in a resettlement country. Consequently, there are additional and more acute sociocultural barriers to accessing SRH for this group upon arrival. These barriers include family, cultural and religious influences as well as knowledge, awareness and use of SRH care [ 9 , 90 ].

Specific barriers to care for vulnerable subgroups of refugee and displaced women were identified. Younger unmarried women [ 50 ] and women who had experienced female genital cutting [ 73 ] faced additional layers of disadvantage in accessing SRH care. In this review the patterns of access of those sub-groups were difficult to establish given the limited number of related studies.

There was uniformity of findings relating to positive influences on access to SRH care across ethnic groups and healthcare contexts. Interpersonal factors included establishing trust, confidence and communication between refugee and displaced women and HCPs, HCPs training in cultural competency, provision of quality medical interpreters and patient-provider gender concordance. This suggests building meaningful relational connections, acknowledging refugees’ journey, establishing rapport, taking the time needed to communicate and access to women providers are important in the provision of care to refugee and displaced women.

Implications for clinical practice and future research

Clinical practice.

Key solutions to addressing access to care lie in strengthening SRH education for refugee and displaced women, including offering culturally sensitive information about the importance of preventive SRH care and how the health system functions in the host country. Such initiatives are known to lead to increased utilisation of services [ 91 ] and better SRH outcomes [ 74 , 92 ].

Interventions to improve health literacy might include offering preventive SRH education in appropriate languages, targeting reading levels and design of printed material and using the Teach-Back method in face to face education [ 93 ], supporting health system navigation, and promoting self-efficacy and self-advocacy skills.

Ongoing HCPs professional development and education encompassing culturally competency and awareness of SRH needs leads to better health care provision of ethnically diverse groups [ 94 ]. Cultural competence training has been developed to improve access to care [ 95 ], and has resulted in better quality care [ 96 , 97 ] and reduced discrimination in settings with diverse ethnic groups [ 98 ]. Ensuring adequate refugee-specific health services and well-trained culturally sensitive HCPs, such as specialist General Practitioners, refugee health nurses, and bicultural healthcare workers may improve SRH care for refugee and displaced women. Health policy aimed at providing bilingual community support workers and medical interpreters as advocates with knowledge and sensitivity to address SRH topics would benefit women during resettlement. Providing an understanding of the complex SRH care needs of refugee and displaced women in undergraduate and professional development programs would further facilitate access. Ensuring specific health literacy education modules for primary HCPs as a component of their continuing professional development should be a priority. Such initiatives should be a priority in high-income resettlement countries where standards and guidelines can be set and adapted appropriately to low-income country settings with less resources.

Addressing gender discordance by employing more women General Practitioners, increasing the scope of practice for refugee health nurses, and giving women the option of choosing the gender of practitioners may facilitate care. This, together with providing adequate human resourcing allowing longer consultation times to accommodate cultural needs, to listen and develop women’s trust and confidence and confirm screening and contraception information is understood could enhance access to care.

Future research

HCPs knowledge and behaviour toward refugee and displaced women significantly impact women’s access to SRH. More research is needed to understand HCPs educational and cultural competency needs. Furthermore, identifying HCPs understanding of health literacy principles to support them in developing strategies towards facilitating women’s health literacy is needed. Identifying additional positive influences on access to care for refugee and displaced women, particularly in the early resettlement period when women feel more empowered to make their own decisions regarding SRH care, should be a priority. Further research in the area of access to preventive SRH care for women who have experienced female genital cutting is also warranted.

The findings of this review show that to improve access to culturally sensitive and patient-centred care SRH care in primary healthcare settings, interpersonal factors including knowledge, awareness perceived need for and use of preventive SRH care; language and communication barriers, health system factors including HCP discrimination, lack of quality health resources; financial barriers and unmet need; HCP characteristics; health system navigation and sociocultural factors including family influence; religious and cultural factors need to be addressed. The findings can inform practice, public health policy, and health professional education to ensure refugee and displaced women have access to quality preventive SRH care in primary care settings, particularly in low-incomes countries where most refugees seek resettlement.

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Abbreviations

Country of origin

Family Planning

Focus Group Discussion

Host country

Health Care Provider

Human Papilloma Virus

Oral contraceptive pill

Sexual and Reproductive Health

United States of America

United Nations High Commissioner for Refugees. Figures at a Glance, Geneva. 2020 https://www.unhcr.org/en-au/figures-at-a-glance.html . Accessed 20 Oct 2020.

United Nations High Commissioner for Refugees. What is a refugee? Geneva. 2020 https://www.unhcr.org/en-au/what-is-a-refugee.html . Accessed 11 Nov 2021.

United Nations High Commissioner for Refugees. Global trends forced displacement. Geneva: UNHCR; 2019. https://www.unhcr.org/60b638e37/unhcr-global-trends-2020.html Accessed 11 Nov 2021.

United Nations High Commissioner for Refugees. Protracted Refugee situations: the search for practical solutions. Geneva: UNHCR; 2006 https://www.unhcr.org/4444afcb0.pdf Accessed 1 June 2020

Crosby SS. Primary care management of non-English-speaking refugees who have experienced trauma: a clinical review. JAMA. 2013;310(5):519–28.

Article   CAS   PubMed   Google Scholar  

Dowling A, Enticott J, Kunin M, Russell G. The association of migration experiences on the self-rated health status among adult humanitarian refugees to Australia: an analysis of a longitudinal cohort study. Int J Equity Health. 2019;18(1):130.

Article   PubMed   PubMed Central   Google Scholar  

McKeary M, Newbold B. Barriers to care: the challenges for Canadian refugees and their health care providers. J Refug Stud. 2010;23(4):523–45.

Article   Google Scholar  

Chiarenza A, Dauvrin M, Chiesa V, Baatout S, Verrept H. Supporting access to healthcare for refugees and migrants in European countries under particular migratory pressure. BMC Health Serv Res. 2019;19(1):513.

Ivanova O, Rai M, Kemigisha E. A systematic review of sexual and reproductive health knowledge, experiences and access to services among refugee, migrant and displaced girls and young women in Africa. Int J Environ Res Public Health. 2018;15(8):1–12.

Seyife A, Fisseha G, Yebyo H, Gidey G, Gerensea H. Utilization of modern contraceptives and predictors among women in Shimelba refugee camp, northern Ethiopia. PLoS One. 2019;14(3):e0212262.

Bakesiima R, Cleeve A, Larsson E, Tumwine JK, Ndeezi G, Danielsson KG, et al. Modern contraceptive use among female refugee adolescents in northern Uganda: prevalence and associated factors. Reprod Health. 2020;17(1):67.

Jennings L, George AS, Jacobs T, Blanchet K, Singh NS. A forgotten group during humanitarian crises: a systematic review of sexual and reproductive health interventions for young people including adolescents in humanitarian settings. Confl Heal. 2019;13:57.

Spiegel PB, Bennedsen AR, Claass J, Bruns L, Patterson N, Yiweza D, et al. Prevalence of HIV infection in conflict-affected and displaced people in seven sub-Saharan African countries: a systematic review. Lancet. 2007;369(9580):2187–95.

Article   PubMed   Google Scholar  

Parish A. Gender-Based Violence against Women: Both Cause for Migration and Risk along the Journey: Migration Policy Institute; 2017 https://www.migrationpolicy.org/article/gender-based-violence-against-women-both-cause-migration-and-risk-along-journey . Accessed 2 Oct 2020.

World Health Organisation. Universal health coverage for sexual and reproductive health. Geneva. 2020 https://www.who.int/reproductivehealth/publications/financing-uhc-for-sexual-reproductive-health-evidence-brief/en/ . Accessed 5 Nov 2020.

United Nations. Transforming our World: The 2030 Agenda for Sustainable Development. 2015. https://sustainabledevelopment.un.org/post2015/transformingourworld/publication . Accessed 30 July 2020.

The World Bank. World Bank Country and Lending Groups Country Classification 2020 https://datahelpdesk.worldbank.org/knowledgebase/articles/906519-world-bank-country-and-lending-groups . Accessed 24 Nov 2020.

Cottingham J, Kismodi E, Hilber AM, Lincetto O, Stahlhofer M, Gruskin S. Using human rights for sexual and reproductive health: improving legal and regulatory frameworks. Bull World Health Organ. 2010;88(7):551–5.

Germain A. Editor meeting human rights norms for the quality of sexual and reproductive health information and services: Discussion paper. International Conference on Human Rights; 2013. Noordwijk, The Netherlands: United Nations Population Fund; 2013.

Sundari Ravindran TK, Govender V. Sexual and reproductive health services in universal health coverage: a review of recent evidence from low- and middle-income countries. Sex. Reprod Health Matters. 2020:28(2):1–22.

Filler T, Jameel B, Gagliardi AR. Barriers and facilitators of patient centered care for immigrant and refugee women: a scoping review. BMC Public Health. 2020;20(1):1013.

Vermeir P, Vandijck D, Degroote S, Peleman R, Verhaeghe R, Mortier E, et al. Communication in healthcare: a narrative review of the literature and practical recommendations. Int J Clin Pract. 2015;69(11):1257–67.

Article   CAS   PubMed   PubMed Central   Google Scholar  

Williams K, Warren C, Askew I. Planning and implementing an essential package of sexual and reproductive health services. Geneva: United Nations Populations Fund. 2010. https://www.unfpa.org/sites/default/files/resource-pdf/Essential_Package_Integration.pdf . Accessed 2 Oct 2020.

World Health Organisation. Primary health care on the road to universal health coverage - monitoring report. Geneva; 2019. https://www.who.int/publications/i/item/9789240029040 . Accessed 24 Nov 2020.

Casey SE. Evaluations of reproductive health programs in humanitarian settings: a systematic review. Confl Heal. 2015;9(1):S1.

Google Scholar  

Amiri M, El-Mowafi IM, Chahien T, Yousef H, Kobeissi LH. An overview of the sexual and reproductive health status and service delivery among Syrian refugees in Jordan, nine years since the crisis: a systematic literature review. Reprod Health. 2020;17(1):166.

Foster AM, Evans DP, Garcia M, Knaster S, Krause S, McGinn T, et al. The 2018 inter-agency field manual on reproductive health in humanitarian settings: revising the global standards. Reprod Health Matters. 2017;25(51):18–24.

Hadgkiss EJ, Renzaho AM. The physical health status, service utilisation and barriers to accessing care for asylum seekers residing in the community: a systematic review of the literature. Aust Health Rev. 2014;38(2):142–59.

Sarria-Santamera A, Hijas-Gomez AI, Carmona R, Gimeno-Feliu LA. A systematic review of the use of health services by immigrants and native populations. Public Health Rev. 2016;37:28.

Riggs E, Davis E, Gibbs L, Block K, Szwarc J, Casey S, et al. Accessing maternal and child health services in Melbourne, Australia: reflections from refugee families and service providers. BMC Health Serv Res. 2012;12:117.

Yelland J, Riggs E, Szwarc J, Casey S, Duell-Piening P, Chesters D, et al. Compromised communication: a qualitative study exploring afghan families and health professionals' experience of interpreting support in Australian maternity care. BMJ Qual Saf. 2016;25(4):e1.

Owens C, Dandy J, Hancock P. Perceptions of pregnancy experiences when using a community-based antenatal service: a qualitative study of refugee and migrant women in Perth, Western Australia. Women Birth. 2016;29(2):128–37.

O'Mahony J, Donnelly T. Immigrant and refugee women's post-partum depression help-seeking experiences and access to care: a review and analysis of the literature. J Psychiatr Ment Health Nurs. 2010;17(10):917–28.

Khanlou N, Haque N, Skinner A, Mantini A, Kurtz LC. Scoping review on maternal health among immigrant and refugee women in Canada: prenatal, intrapartum, and postnatal care. J Pregnancy. 2017;2017:8783294.

Heslehurst N, Brown H, Pemu A, Coleman H, Rankin J. Perinatal health outcomes and care among asylum seekers and refugees: a systematic review of systematic reviews. BMC Med. 2018;16(1):89.

Cheng IH, Drillich A, Schattner P. Refugee experiences of general practice in countries of resettlement: a literature review. Br J Gen Pract. 2015;65(632):E171–E6.

Bhatia R, Wallace P. Experiences of refugees and asylum seekers in general practice: a qualitative study. BMC Fam Pract. 2007;8:48.

Brandenberger J, Tylleskar T, Sontag K, Peterhans B, Ritz N. A systematic literature review of reported challenges in health care delivery to migrants and refugees in high-income countries - the 3C model. BMC Public Health. 2019;19:755.

Mengesha ZB, Perz J, Dune T, Ussher J. Refugee and migrant women's engagement with sexual and reproductive health care in Australia: a socio-ecological analysis of health care professional perspectives. PLoS One. 2017;12(7):e0181421.

Robertshaw L, Dhesi S, Jones LL. Challenges and facilitators for health professionals providing primary healthcare for refugees and asylum seekers in high-income countries: a systematic review and thematic synthesis of qualitative research. BMJ Open. 2017;7(8):e015981.

Mengesha ZB, Perz J, Dune T, Ussher J. Preparedness of health care professionals for delivering sexual and reproductive health care to refugee and migrant women: a mixed methods study. Int J Environ Res Public Health. 2018;15:174.

Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol. 2009;62(10):1006–12.

Cooke A, Smith D, Booth A. Beyond PICO: the SPIDER tool for qualitative evidence synthesis. Qual Health Res. 2012;22(10):1435–43.

Covidence. Better systematic review management (2020) https://www.covidence.org/ . Accessed 20 Oct 2020.

Kmet LM, Lee RC, Cook LS. Standard quality assessment criteria for evaluating primary research papers from a variety of fields. Edmonton, Canada: Alberta Heritage Foundation for Medical Research; 2004.

Popay JRH, Sowden A, Petticrew M, Arai L, Rodger M, Britten N, et al. Guidance on the conduct of narrative synthesis in systematic reviews. A Product from the ESRC Methods Programme. Lancaster: Lancaster University; 2006.

Morrison V. Contraceptive need among Cambodian refugees in Khao Phlu camp. Int Fam Plan Perspect. 2000;26(4):188–92.

Gurnah K, Khoshnood K, Bradley E, Yuan C. Lost in translation: reproductive health care experiences of Somali bantu women in Hartford, Connecticut. J Midwifery Women's Health. 2011;56(4):340–6.

Cherri Z, Gil Cuesta J, Rodriguez-Llanes JM, Guha-Sapir D. Early marriage and barriers to contraception among Syrian refugee women in Lebanon: a qualitative study. Int J Environ Res Public Health. 2017;14(8):25.

Kabakian-Khasholian T, Mourtada R, Bashour H, El Kak F, Zurayk H. Perspectives of displaced Syrian women and service providers on fertility behaviour and available services in west Bekaa, Lebanon. Reprod Health Matters. 2017;25(Supplement 1):S75–86.

Tanabe M, Myers A, Bhandari P, Cornier N, Doraiswamy S, Krause S. Family planning in refugee settings: findings and actions from a multi-country study. Conflict and Health. 2017;11:9.

West L, Isotta-Day H, Ba-Break M, Morgan R. Factors in use of family planning services by Syrian women in a refugee camp in Jordan. J Fam Plann Reprod Health Care. 2017;43(2):96–102.

Agbemenu K, Volpe EM, Dyer E. Reproductive health decision-making among US-dwelling Somali bantu refugee women: a qualitative study. J Clin Nurs. 2018;27(17–18):3355–62.

Gebreyesus T, Gottlieb N, Sultan Z, Ghebrezghiabher HM, Tol W, Winch PJ, et al. Barriers to contraceptive careseeking: the experience of Eritrean asylum-seeking women in Israel. Ethn Health. 2020;25(2):255–72.

Royer PA, Olson LM, Jackson B, Weber LS, Gawron L, Sanders JN, et al. "In Africa, there was no family planning. Every year you just give birth": family planning knowledge, attitudes, and practices among Somali and Congolese refugee women after resettlement to the United States. Qual Health Res. 2020;30(3):391–408.

Zhang Y, McCoy EE, Scego R, Phillips W, Godfrey E. A qualitative exploration of Somali refugee Women's experiences with family planning in the U.S. J Immigr Minor Health. 2020;22(1):66–73.

Haworth RJ, Margalit R, Ross C, Nepal T, Soliman AS. Knowledge, attitudes, and practices for cervical cancer screening among the Bhutanese refugee community in Omaha, Nebraska. J Community Health. 2014;39(5):872–8.

Kim K, Kim S, Chung Y. A qualitative study exploring factors associated with pap test use among north Korean refugees. Health Care Women Int. 2017;38(10):1115–29.

Lor B, Ornelas IJ, Magarati M, Do HH, Zhang Y, Jackson JC, et al. We should know ourselves: Burmese and Bhutanese refugee Women's perspectives on cervical Cancer screening. J Health Care Poor Underserved. 2018;29(3):881–97.

Allen EM, Lee HY, Pratt R, Vang H, Desai JR, Dube A, et al. Facilitators and barriers of cervical Cancer screening and human papilloma virus vaccination among Somali refugee women in the United States: a qualitative analysis. J Transcult Nurs. 2019;30(1):55–63.

Ross Perfetti A, Abboud S, Behme M, Barg FK. Understanding wellness and barriers to care among Iraqi refugee women in the United States. Health Soc Care Commun. 2019;27(6):1430–7.

Babatunde-Sowole OO, Power T, Davidson PM, DiGiacomo M, Jackson D. Health screening and preventative health care in refugee women: a qualitative analysis. Contemp Nurse. 2020:1–30.

Saadi A, Bond BE, Percac-Lima S. Bosnian, Iraqi, and Somali refugee women speak: a comparative qualitative study of refugee health beliefs on preventive health and breast Cancer screening. Womens Health Issues. 2015;25(5):501–8.

Parajuli J, Horey D, Avgoulas M-I. Access to breast cancer screening -- perception, and perceived barriers among older Bhutanese refugee women resettled in Australia: a qualitative study. Aust J Cancer Nurs. 2019;20(1):14–8.

Raheel H, Karim MS, Saleem S, Bharwani S. Knowledge, Attitudes and practices of contraception among afghan refugee women in Pakistan: a cross-sectional study. PLoS One. 2012;7(11).

Kisindja RM, Kimona C, Etoy M, Dorme F, Benfield N. Family planning knowledge and use among women in camps for internally displaced people in the Democratic Republic of the Congo. Int J Gynaecol Obstet. 2017;138(3):256–60.

Raben LAD, Muijsenbergh METCvd. Inequity in contraceptive care between refugees and other migrant women?: a retrospective study in Dutch general practice. Fam Pract. 2018;35(4):468–74.

Pierce H. Reproductive health care utilization among refugees in Jordan: Provisional support and domestic violence. Women Health. 2019;15:1–10.

Barnes DM, Harrison CL. Refugee women's reproductive health in early resettlement. J Obstet Gynecol Neonatal Nurs. 2004;33(6):723–8.

Redwood-Campbell L, Thind H, Howard M, Koteles J, Fowler N, Kaczorowski J. Understanding the health of refugee women in host countries: lessons from the Kosovar re-settlement in Canada. Prehospital Disaster Med. 2008;23(4):322–7.

Lofters AK, Moineddin R, Hwang SW, Glazier RH. Predictors of low cervical cancer screening among immigrant women in Ontario, Canada. BMC Womens Health. 2011;11(1):20.

Odunukan OW, Abdulai RM, Hagi Salaad MF, Lahr BD, Flynn PM, Wieland ML. Provider and interpreter preferences among Somali women in a primary care setting. J Prim Care Community Health. 2015;6(2):105–10.

Banke-Thomas A, Agbemenu K, Johnson-Agbakwu C. Factors associated with access to maternal and reproductive health care among Somali refugee women resettled in Ohio, United States: a cross-sectional survey. J Immigr Minor Health. 2019;21(5):946–53.

Zhang Y, Ornelas IJ, Do HH, Magarati M, Jackson JC, Taylor VM. Provider perspectives on promoting cervical Cancer screening among refugee women. J Community Health. 2017;42(3):583–90.

Finfgeld-Connett D. Generalizability and transferability of meta-synthesis research findings. Oxford, UK. 2010. 246–254.

Finlay L, Gough B. ProQuest. Reflexivity : a practical guide for researchers in health and social sciences. 1st ed. Malden: Blackwell Science; 2003.

Pranee L. Focus group methodology and sensitive topics and vulnerable groups. London: SAGE Publications Ltd; 2011. p. 107.

Merry L, Clausen C, Gagnon AJ, Carnevale F, Jeannotte J, Saucier JF, et al. Improving qualitative interviews with newly arrived migrant women. Qual Health Res. 2011;21(7):976–86.

Wangdahl J, Westerling R, Lytsy P, Martensson L. Perspectives on health examination for asylum seekers in relation to health literacy - focus group discussions with Arabic and Somali speaking participants. BMC Health Serv Res. 2019;19(1):676.

Bowling A. Mode of questionnaire administration can have serious effects on data quality. J Public Health (Oxf). 2005;27(3):281–91.

Floyd A, Sakellariou D. Healthcare access for refugee women with limited literacy: layers of disadvantage. Int J Equity Health. 2017;16(1).

Bischoff A, Bovier PA, Isah R, Francoise G, Ariel E, Louis L. Language barriers between nurses and asylum seekers: their impact on symptom reporting and referral. Soc Sci Med. 2003;57(3):503–12.

Schyve PM. Language differences as a barrier to quality and safety in health care: the joint commission perspective. J Gen Intern Med. 2007;22(Suppl 2):360–1.

Degni F, Suominen S, Essen B, El Ansari W, Vehvilainen-Julkunen K. Communication and cultural issues in providing reproductive health care to immigrant women: health care providers' experiences in meeting the needs of [corrected] Somali women living in Finland. J Immigr Minor Health. 2012;14(2):330–43.

Mengesha ZB, Perz J, Dune T, Ussher J. Talking about sexual and reproductive health through interpreters: the experiences of health care professionals consulting refugee and migrant women. Sexual Reprod Healthcare. 2018;16:199–205.

The University of Sydney. What is cultural competence? Sydney: National Centre for Cultural Competence; 2021 https://www.sydney.edu.au/nccc/about-us/what-is-cultural-competence.html . Accessed 29 July 2021.

Saha S, Beach MC, Cooper LA. Patient centeredness, cultural competence and healthcare quality. J Natl Med Assoc. 2008;100(11):1275–85.

PubMed   Google Scholar  

Rade DA, Crawford G, Lobo R, Gray C, Brown G. Sexual health help-seeking behavior among migrants from sub-Saharan Africa and South East Asia living in high income countries: a systematic review. Int J Environ Res Public Health. 2018;15(7):22.

Bertakis KD, Azari R. Patient-centered care: the influence of patient and resident physician gender and gender concordance in primary care. J Women's Health (Larchmt). 2012;21(3):326–33.

Metusela C, Ussher J, Perz J, Hawkey A, Morrow M, Narchal R, et al. "In my culture, we Don't know anything about that": sexual and reproductive health of migrant and refugee women. Int J Behav Med. 2017;24(6):836–45.

Carroll J, Epstein R, Fiscella K, Gipson T, Volpe E, Jean-Pierre P, et al. Caring for Somali women: implications for clinician-patient communication. Patient Educ Couns. 2007;66(3):337–45.

Anaman JA, Correa-Velez I, King J. A survey of cervical screening among refugee and non-refugee African immigrant women in Brisbane, Australia Health Promotion. J Aust. 2016;28(3):217–24.

Murray L, Elmer S, Elkhair J. Perceived barriers to managing medications and solutions to barriers suggested by Bhutanese former refugees and service providers. J Transcult Nurs. 2018;29(6):570–7.

Truong M, Paradies Y, Priest N. Interventions to improve cultural competency in healthcare: a systematic review of reviews. BMC Health Serv Res. 2014;14:99.

Betancourt JR, Green AR, Carrillo JE, Ananeh-Firempong O. Defining cultural competence: a practical framework for addressing racial/ethnic disparities in health and health care. Public Health Rep. 2003;118(4):293–302.

Zeh P, Sandhu HK, Cannaby AM, Sturt JA. The impact of culturally competent diabetes care interventions for improving diabetes-related outcomes in ethnic minority groups: a systematic review. Diabet Med. 2012;29(10):1237–52.

Handtke O, Schilgen B, Mösko M. Culturally competent healthcare – a scoping review of strategies implemented in healthcare organizations and a model of culturally competent healthcare provision. PLoS One. 2019;14(7):e0219971.

Shepherd SM, Willis-Esqueda C, Newton D, Sivasubramaniam D, Paradies Y. The challenge of cultural competence in the workplace: perspectives of healthcare providers. BMC Health Serv Res. 2019;19(1):135.

Download references

Acknowledgements

JF is supported by the Finkel Professorial Fellowship which receives funding from the Finkel Family Foundation. ND holds an Australian Government Research Training Scholarship.

There was no funding source for this particular study.

Author information

Authors and affiliations.

Global and Women’s Health, School of Public Health and Preventive Medicine, Monash University Faculty of Medicine Nursing and Health Sciences, Melbourne, VIC, Australia

Natasha Davidson, Karin Hammarberg & Jane Fisher

The Ian Potter Library, The Alfred Hospital, Melbourne, Victoria, Australia

Lorena Romero

You can also search for this author in PubMed   Google Scholar

Contributions

The search strategy was devised by ND with the assistance of LR. ND contributed to the PROSPERO submission. Titles and abstracts were searched by ND. Screening of full text articles was undertaken by ND, JF and KH independently. Quality assessment was conducted by ND, JF and KH. The data extraction, analysis and narrative synthesis involved ND, with JF and KH bringing a wider perspective to the analysis. All authors contributed to the development of the manuscript and approved the final version.

Authors’ information

All listed authors have approved the manuscript before submission, including the names and order of authors.

Corresponding author

Correspondence to Natasha Davidson .

Ethics declarations

Ethics approval and consent to participate.

Not applicable.

Consent for publication

Competing interests.

We declare no competing interests.

Additional information

Publisher’s note.

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Additional file 1..

Selection criteria.

Additional file 2.

Database search strategy.

Additional file 3.

Quality assessment of quantitative studies and quantitative component of mixed methods.

Additional file 4.

Quality assessment of qualitative studies and quality component of mixed methods.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ . The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/ ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Cite this article.

Davidson, N., Hammarberg, K., Romero, L. et al. Access to preventive sexual and reproductive health care for women from refugee-like backgrounds: a systematic review. BMC Public Health 22 , 403 (2022). https://doi.org/10.1186/s12889-022-12576-4

Download citation

Received : 07 April 2021

Accepted : 06 January 2022

Published : 27 February 2022

DOI : https://doi.org/10.1186/s12889-022-12576-4

Share this article

Anyone you share the following link with will be able to read this content:

Sorry, a shareable link is not currently available for this article.

Provided by the Springer Nature SharedIt content-sharing initiative

• Sexual and reproductive health
• Health care providers

BMC Public Health

ISSN: 1471-2458

• Submission enquiries: [email protected]
• General enquiries: [email protected]