Global women's health is more than maternal health: a review of gynecology care needs in low-resource settings.

Volume 70, Number 3 OBSTETRICAL AND GYNECOLOGICAL SURVEY Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.

CME REVIEW ARTICLE

CHIEF EDITOR’S NOTE: This article is part of a series of continuing education activities in this Journal through which a total of 36 AMA PRA Category 1 Credits™ can be earned in 2015. Instructions for how CME credits can be earned appear on the last page of the Table of Contents.

Global Women’s Health Is More Than Maternal Health: A Review of Gynecology Care Needs in Low-Resource Settings Nuriya Robinson, MD,* Cynthia Stoffel, MPH, RN,† and Sadia Haider, MD, MPH* *Assistant Professor, and †Research Manager, Department of Obstetrics and Gynecology at the University of Illinois at Chicago, Chicago, IL Women’s health care efforts in low-resource settings are often focused primarily on prenatal and obstetric care. However, women all over the world experience significant morbidity and mortality related to cervical cancer, sexually transmitted infections, and urogynecologic conditions as well as gynecologic care provision including insufficient and ineffective family planning services. Health care providers with an interest in clinical care in low-resource settings should be aware of the scope of the burden of gynecologic issues and strategies in place to combat the problems. This review article discusses the important concerns both in the developing world as well as highlights similar disparities that exist in the United States by women’s age, race and ethnicity, and socioeconomic status. Ultimately, this review article aims to inform and update health care providers on critical gynecologic issues in low-resource settings. Target Audience: Obstetricians and gynecologists, family physicians Learning Objectives: After participating in this activity, the learner will be better able to inform and update clinicians on critical gynecologic topics in global health, identify and discuss significant causes of morbidity and mortality in low-resource settings globally, and delineate parallels between global women’s health challenges and gynecologic care disparities in the United States.

The focus of women’s health in low-resource settings, specifically low- and middle-income countries, has often been limited to that of prenatal and obstetric care. This is further supported by the focus of Millennium Development Goal number 5, which is composed of 2 targets to improve maternal health: (1) reducing by 3 quarters between 1990 and 2014 the maternal mortality ratio and (2) achieving by 2015 universal access to reproductive health.1 Although the target 5.2 includes indicators for contraceptive prevalence rate, adolescent birth rate, and unmet needs for family planning, important issues in women’s health exist that are not limited to reproductive health concerns. While maternal health is inarguably important as many factors contribute to the burden of maternal mortality All authors and staff in a position to control the content of this CME activity and their spouses/life partners (if any) have disclosed that they have no financial relationships with, or financial interests in, any commercial organizations pertaining to this educational activity. Correspondence requests to: Sadia Haider, MD, MPH, 820 S Wood St, M/C 808, Chicago, IL 60612. E-mail: [email protected].

in low-resource settings (Table 1), gynecologic conditions are a significant threat to morbidity and mortality in women across the globe as well. Of all cervical cancer–related deaths worldwide, 85% occur in the developing world.4,5 Likewise, preventable deaths due to unsafe abortion claim an estimated 50,000 lives each year.6 There is urgent need to focus on gynecologic conditions in low-resource settings in order to address existing gaps in care, which negatively impact women’s health. Multiple factors limit the prioritization of gynecologic women’s health in the developing world. These include competing health agendas, poorly structured health systems, poverty, cultural factors, limited resources, and a dearth of providers.7–9 As a result of the various barriers to gynecologic care provision, cervical cancer, pregnancy risks resulting from insufficient and ineffective family planning services, sexually transmitted infections (STIs), and urogynecologic conditions including obstetric fistulas remain endemic in many resourcepoor areas around the world.

www.obgynsurvey.com | 211

Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.

9

212

Obstetrical and Gynecological Survey

TABLE 1 Causes of Maternal Mortality by Region by Year Hemorrhage, Hypertensive Direct/Indirect % Disease, % Infection, % Abortion, % Causes, % Embolism, % Africa Systematic review,* data collected 1990–20022 WHO systematic analysis,† 2003–20093 Asia Systematic review,* data collected 1990–20022 WHO systematic analysis,† 2003–20093 Latin America/Caribbean Systematic review,* data collected 1990–20022 WHO systematic analysis,† 2003–20093

33.9 24.7

9.1 15.9

15.9 10.2

3.9 9.4

21.6 37.6

2.0 2.1

30.8 30.6

9.1 10.9

11.6 11.6

5.7 5.8

14.1 36.7

0.4 4.4

20.8 23.1

25.7 22.1

7.7 8.3

12.0 9.9

7.7 33.3

0.6 3.2

Total rows do not compute to 100% because of differences in data reported across the 2 articles. Anemia and obstructed labor are not included. *Unclassified deaths and deaths due to ectopic pregnancy are not included. HIV included in the infection category. †HIV included in direct/indirect causes.

Similarly, in the United States, significant health disparities exist between women based on age, socioeconomic status, and race and ethnicity.10 Gynecologic concerns in the United States echo those of our lowresource counterparts to the extent that marginalized populations have worse health outcomes in comparison to other groups of women.11 While efforts are underway to address reproductive health disparities in the United States, acknowledging such concerns abroad is relevant and worthwhile. This article seeks to discuss the leading causes of gynecologic-related morbidity and mortality for women in resource-limited areas. In addition, parallels between gynecologic health challenges in global and domestic settings will be drawn, and current initiatives to address gaps in gynecologic health care will be highlighted. CERVICAL CANCER According to the World Health Organization (WHO), cervical cancer is the second most common female cancer worldwide with approximately 500,000 new diagnoses each year.12 In the developing world, cervical cancer is the leading cause of female mortality, accounting for 85% of the estimated 250,000 yearly disease-related deaths.4 High-risk areas such as Eastern Africa, Melanesia, and Southern and Middle Africa bear cervical cancer rates 81-fold greater than do regions across the world deemed low risk, such as Australia, New Zealand, and Western Asia.4 Differences in disease burden and survival on a global scale relate to cervical cancer screening ability, diagnostic capability, and follow-up. SCREENING Cervical cancer is considered a preventable gynecologic cancer because of the development of screening modalities, including the Papanicolaou test (Pap smear)

and the human papillomavirus (HPV) DNA test, which has become more widely used in recent years to document the presence of oncogenic viral strains responsible for cervical cancer.13 In the developed world, both tests are routinely performed and considered the criterion standard for diagnosing premalignant and malignant lesions.14 However, in resource-limited settings, access to preventive services is often limited by myriad of factors resulting in gross underscreening of at-risk women.15,16 Barriers to screening include patient-related factors such as financial constraints, lack of awareness of need for screening, and cultural factors limiting interest in screening. In addition, there are provider-related and structural barriers such as personnel shortages, inadequately trained staff, and lack of supporting infrastructure preventing the ability to provide widespread screening.17,18 Subsequently, only 19% of women eligible for cervical cancer screening in developing countries receive a Pap smear.16 In 2002, the WHO outlined essential elements necessary for an effective cytology screening program in middle-income countries. Of note, there are no existing screening programs in low-income countries. Training program elements included training of relevant health care professionals, coming to a consensus on the appropriate age group to be screened and the frequency of screening, adequately collecting and preparing Pap smears, efficiently transporting smears to laboratories, having access to high-quality centralized laboratory services, establishing procedures to report screening results to women, and providing appropriate follow-up in instances of positive and negative results after determining what constitutes an abnormality.14 And while standardizing components of screening programs is necessary, meeting these requirements is unlikely in the majority of low-resource settings where supplies of Pap smear tests are insufficient, health care providers


Global Women’s Health • CME Review Article

are unavailable to perform or interpret results, and laboratory facilities for identifying abnormalities are nonexistent. Thus, consideration of the context, the setting, and current infrastructure is important when considering the feasibility of screening programs. VACCINATION To help offset the shortage of organized screening programs, HPV vaccination has been introduced as an opportunity for primary prevention in girls aged 9 to 13 years.19 Targeting the HPV strains primarily responsible for 70% of cervical cancers, vaccination has the potential to decrease disease incidence and to lessen the impact of cervical cancer on the developing world. The potential of this preventive strategy, however, is opposed by 2 major concerns—the utility of the vaccine in the event exposure to oncogenic strains has occurred prior to vaccination and the reality of its cost, which is considered the largest barrier to widespread implementation.19 Negotiating pricing and programmatic costs is an outstanding issue, which must be addressed if lowresource countries plan to proceed with effective vaccination coverage among the target population. VISUAL INSPECTION WITH ACETIC ACID In settings where neither conventional screening mechanisms nor primary prevention is feasible, a low-cost alternative to cytology screening through visual inspection with acetic acid (VIA) has been supported by the Alliance for Cervical Cancer Prevention.20 Visual inspection with acetic acid involves performing a speculum examination with direct application of acetic acid to the cervix and subsequent observation with the naked eye for the development of acetowhite lesions using a light source.14,17 Benefits of the method include its low cost, efficiency in diagnosing abnormalities, simplicity, and relative ease of use with minimal equipment

213

(Table 2).21–23 Midlevel providers may be trained to perform the examination, thus eliminating the need for increasing physician presence in what may be a limited workforce. The examination is dependent on the observer’s eyesight and skill level, although proficiency can be obtained through sufficient training and supervision.24 In 2007, Sankaranarayanan and colleagues23 randomized women in 114 study clusters to either VIA with trained nurses or a control group. Those with positive screening tests then underwent colposcopy, biopsies, and cryotherapy as indicated. The authors observed both a 25% reduction in cervical cancer incidence and a 35% reduction in cervical cancer mortality in the intervention group, suggesting adequate VIA training can reduce the burden of disease due to cervical cancer in resource-limited settings.23 Visual inspection with acetic acid has not only been shown to be a safe, effective, and feasible cervical cancer screening method in low-resource settings, it has also been considered acceptable to women.17,25 Whereas limitations to VIA do exist, namely, lower specificity potentially leading to overtreatment and its inability to assess the endocervix, a major advantage of VIA is the ability to diagnose and treat in a single visit. In resource-poor settings where transportation logistics and cost affect health care utilization, eliminating the need for subsequent follow-up is of paramount importance. The process of VIA coupled with cryotherapy performed in the outpatient setting for treatment of positive lesions has been coined “screen and treat” approach.20,26,27 The 2013 WHO publication, Guidelines for Screening and Treatment of Precancerous Lesions for Cervical Cancer Prevention, supports immediate treatment of lesions suspected as high-grade disease during screening.28 The goal of the “screen and treat” method is to decrease progression of precancerous lesions to cervical cancer by providing rapid screening and

TABLE 2 Advantages and Limitations of VIA14 Advantages

Limitations

• Test characteristic of VIA consistent across studies with different designs • Comparable sensitivity of VIA in detecting high-grade disease as good as cytology • More rapid training of VIA screeners than cytotechnologists or medical technologists • Real-time screening test results available immediately • Comparable reproducibility of VIA to that of other tests • Simpler and cheaper than other screening tests (eg, cytology and HPV DNA testing) • Able to perform in extremely low-resource settings • Potential to minimize loss to follow-up

• Low specificity compared with cytology (high rates of false positivity) • High test-positive rate (10%–35%) • Overinvestigation and overtreatment of screen-positive women in test and treat conditions • No standardized methods of quality control • Training methods and competency evaluation not yet standardized • Essentially leads to detection of ectocervical disease • Uncertain how VIA works in an integrated service delivery model • Performance decay, potential need for retraining


214


treatment in a single visit. In settings where an HPV DNA test is feasible, this should be done first followed by treatment as needed. However, in areas where an HPV test is not practical, WHO recommends screening with VIA followed by treatment.28 To evaluate the impact of immediate treatment for positive screening tests, Denny et al15 performed a randomized clinical trial of 6555 nonpregnant women in a large South African township. The women underwent screening with HPV DNA and VIA and were subsequently randomized to either cryotherapy for positive HPV DNA, cryotherapy for screen-positive VIA, or delayed evaluation. Colposcopy with biopsy of acetowhite lesions at 6 months found a statistically significant decrease in cervical intraepithelial neoplasia grade 2 or worse lesions in both the HPV DNA (P < 0.001) and VIA groups (P = 0.02) when compared with the control group. Although no longer statistically significant, this trend continued at 12 months as well.15 Substantial progress to reduce the impact of cervical cancer in low-resource settings has been slow. Hopefully, moving forward more widespread implementation of low-cost interventions such as VIA for screening and cryotherapy for treatment purposes will help decrease the incidence, morbidity, and mortality associated with cervical cancer in resource-poor areas worldwide, while efforts continue to fund and implement HPV vaccination broadly.

contraceptive use exist may assist with more customized approaches for family planning services throughout the developing world where the greatest need remains. Efforts aimed at reducing the gap between contraceptive prevalence and need are often met with challenges unique to low-resource settings. Literature on barriers to increasing contraception uptake cites social, medical, cultural, and demographic barriers as largely responsible for unmet need.7 In addition, a small proportion of women still report lack of knowledge of modern contraceptive methods and misinformation as a reason for nonuse; however, substantial progress has been made in this particular area in recent years.7,34 BARRIERS Social Barriers 34

Darroch et al examined tabulated Demographic Health Survey (DHS) responses from 29 Sub-Saharan African countries, 4 countries in South Central Asia, and 3 countries in South East Asia and reported nearly 25% of women with unmet need in these 3 regions cite fear of adverse effects as the primary deterrent for nonuse. An additional social factor affecting contraceptive use involves stigma associated with desiring contraception for sexually active young women and unmarried women.37 Medical Barriers

FAMILY PLANNING The provision of reliable contraception is one of the most effective prevention strategies to decrease deaths of women and children in the developing world.29–31 Yet, the global unmet need for modern contraception (including oral contraceptives, implants, injectables, intrauterine devices, male condoms, female condoms, male vasectomy, female tubal ligation, lactational amenorrhea method, and emergency contraception32) remains alarmingly high at 26%.33,34 In 2012, in the developing world specifically, an estimated 222 million women desired pregnancy spacing or no future fertility but were not using modern contraceptive methods. The highest proportion of these women (73%) lived in 1 of the 69 poorest countries in the world.33 When unmet need is examined by region, povertyrelated inequities are apparent. In Sub-Saharan Africa, unmet need is most significant at 60% followed by western Asia (50%) and south Asia (34%).35 Although contraceptive prevalence overall has steadily increased over the last 30 years worldwide, prevalence throughout developing regions is not equal.36 Recognizing that regional and subregional differences in patterns of

Provider bias and misinterpretation of eligibility criteria for method use have been shown to affect access to and adoption of methods.38,39 A survey analyzing medical barriers in Tanzania revealed 10% to 13% of providers refrain from offering at least 1 method of contraception because of personal preferences.40 Age and parity restrictions are not uncommonly arbitrarily imposed on clients seeking family planning options, and in some instances, at the provider’s discretion, marriage status may play a role in dictating a client’s candidacy for particular contraceptive options, namely, long-acting reversible contraceptive (LARC) methods.38,39 Also affecting method choice is the availability of resources— providers and commodities. The shortage of health care providers in the developing world has been partially addressed through task shifting or delegating tasks to less specialized members of health care teams. In the area of reproductive health for instance, community health workers have been trained to appropriately dispense condoms and contraceptive pills, both of which are vital to increasing access to some form of contraception for women who may not otherwise have options.8 However, skilled providers are necessary for initiation of



LARC methods—administration of injectables and insertion of the intrauterine device and contraceptive implant. Without the availability of adequate numbers of providers or commodities, women’s contraceptive choices are limited, and limited choice impacts uptake.41 Lastly, a systematic review of qualitative research addressing barriers to contraceptive uptake for 11- to 24-year-old women highlighted fear of receiving a poor reception by clinic staff as a reason for not accessing contraception.42 Cultural Barriers In many societies, the ability of women to plan their families is limited by their societal status. Gender inequality and the low decision-making power of women restrict their contraceptive options and impact their ability to have control over their reproductive health. Sexual intentions, opposition to contraceptive use by a partner, and differences in fertility preferences between partners all affect use or nonuse of contraception.7,9,37 Religious and cultural beliefs around the role of contraception have been shown to influence women’s decisions around contraceptive uptake.34 Demographic Barriers The primary demographic barriers to contraceptive use involve age, wealth, locale, and educational attainment. Clear correlations have been demonstrated between modern contraceptive use and older age, wealth, urban locations, and higher educational attainment. Of these barriers, economic status is the greatest predictor of contraceptive use and more specifically LARC use.34,43 According to a review of DHS data from 13 Sub-Saharan African countries between the years of 1997 and 2006, women in the highest quintile of wealth are much more likely to use long-term contraceptive methods.43 A similar trend was observed in a review of DHS from 55 developing countries where disparity in use was greater in richer countries, and in poor countries, poorer women were also less likely to use contraception.7 Beyond wealth, contraceptive use is directly correlated to clinic access. The distance from a woman’s house to the clinic and travel time to access the clinic are both negatively correlated with contraceptive use.7 UNSAFE ABORTION Effective contraception helps avert unintended pregnancy. However, in settings where universal access to contraception is limited, unplanned pregnancies represent a substantial proportion of the approximately 210 million

215

pregnancies, which occur per year worldwide.44 In fact, in 2012, it was estimated that 42% of the 190 million pregnancies that occurred in the developing world were unplanned, contributing to a global unintended pregnancy rate of 53 per 1000 reproductive-aged women.34,45 When unplanned pregnancies do occur, women in the developing world in particular face challenges with obtaining abortion services, namely, preabortion counseling, safe abortion, and postabortion care with contraceptive counseling to prevent repeat unintended pregnancy and/or abortion.44 According to WHO, an unsafe abortion is “a procedure for terminating an unintended pregnancy carried out either by persons lacking the necessary skills or in an environment that does not conform to minimal medical standards, or both.”37,44,46 Complications resulting from unsafe abortion such as infection, bleeding, and damage to organs contribute to the inequity in maternal deaths seen throughout the developing world.47 An estimated 50,000 women die each year of unsafe abortion, a preventable cause of maternal mortality, which disproportionately affects the world’s poorest women.44 The magnitude of the global burden of abortion-related morbidity and mortality is staggering, especially when considering abortion-related complications account for the largest proportion of gynecologic hospital admissions in resource-limited areas each year.48 A 2006 review by Singh48 compared national estimates of hospital admissions for abortion-related indications in 13 developing countries. Northern Africa was shown to have the highest hospitalization rates for abortioninduced complications (12 per 1000 women), followed by Eastern Africa (10 per 1000), Western Asia (8 per 1000), and South and Central America (8 per 1000, respectively). It should be noted that while these hospitalization rates represent the best available data from Africa, Asia, and Latin America, true estimates of complications resulting from induction abortion are unavailable because many women who undergo unsafe abortion procedures do not seek medical attention.48 Restrictive abortion laws, stigma associated with abortion, and poor access to abortion providers and services, even in countries where abortion is legal, account for the nearly 22 million unsafe abortions that occur worldwide each year. Ninety-seven percent of unsafe abortions take place in low-resource settings throughout Sub-Saharan Africa, Latin America, and Asia, highlighting global disparities in access to comprehensive family planning services.6,37,44,48,49 Jewkes et al50 conducted an exploratory study in the Gauteng Province of South Africa to examine reasons why South African women were not utilizing available abortion services 3 years following legalization of abortion in the


216


country. Lack of information regarding the passage of legislation legalizing abortion, poor access to facilities providing abortion services, unacceptable wait times at abortion clinics, and concern for poor treatment by clinic staff contributed to the continued use of traditional healers, home remedies, and over-the-counter pharmaceutical methods to induce abortion outside the established facilities designated for abortion care.50 Sedgh et al51 echo the sentiment that legalization of abortion does not necessarily correlate with safer abortion as legalized public abortion services may be more costly, the eligibility criteria and regulations more burdensome, and the risks of loss of confidentiality greater than obtaining an abortion in the private sector. In the face of the multiple barriers women face to receiving family planning services, global programmatic efforts have been enacted to overcome the challenged described above. After the 2012 London Summit on Family Planning, the FP2020 global partnership was created to work toward ensuring that all women, regardless of where they live, have access to contraceptives. Some of the specific approaches and existing resources to realize the goal of FP2020 include evidence-based guidelines on all major methods of family planning,52 integration of family planning services into all aspects of women’s health care,53 training of community health workers to promote reproductive health and family planning and administration of injectable contraceptives with targeted monitoring and evaluation,8 and increasing efforts to promote uptake of LARC methods, specifically in the postpartum period.54 The fundamental decisions around when, how, and under what circumstances to plan a family are personal, yet factors beyond a woman’s control are often major determinants of her reproductive choices regardless of her intentions. While elimination of unplanned pregnancy is unrealistic at this juncture, provision of comprehensive family planning services that meet the needs of reproductive aged women is a reasonable goal for developing countries to pursue. To more effectively meet the reproductive health needs of women in the developing world, greater emphasis on understanding childbearing intentions of women, integrating family planning services in general health care,55 and improving efforts to educate women on the benefits of effective contraception and the consequences of unintended pregnancy46 is needed. Universal access to family planning has been a global priority since the 1994 Cairo International Conference on Population and Development.55 Although there is still much work to be done to reach this goal, being mindful of the potential impact that improved access to family planning services can have in low-resource

settings is important. Beyond the individual health benefits women receive, family planning also empowers women by allowing them reproductive choice and positively impacts the socioeconomic and environmental landscape of families, communities, and nations.55,56 Thus, the consequences/repercussions of limited contraceptive and abortion care are substantial and cannot be underestimated. SEXUALLY TRANSMITTED INFECTIONS The global burden of morbidity and mortality related to STIs lies in the developing world and poses a tremendous challenge for resource-poor countries economically, socially, and medically. In 2008, an estimated 499 million new cases of curable STIs (gonorrhea, chlamydia, syphilis, and trichomoniasis) occurred, with the majority of these occurring in resource-limited countries.57 Gonorrhea and chlamydia were responsible for 106 million cases each, whereas syphilis and trichomoniasis 11 million and 276 million, respectively.58 Similarly, incurable STIs—HPV and herpes simplex virus type 2 (HSV-2)—account for disease in an estimated 800 million people worldwide, whereas 35 million people were estimated to be living with human immunodeficiency virus (HIV) at the end of 2012.59,60 Hepatitis B, another incurable STI, which can lead to liver failure and liver cancer, is thought to chronically infect 5% to 10% of the adult population worldwide.61 These statistics illustrate the significant impact STIs have on global health. More specifically, the sexual and reproductive health and gynecologic consequences of STI acquisition—neonatal and fetal death, infertility, and cervical cancer—are most apparent in Sub-Saharan Africa, where the world’s STI burden is concentrated.59,62,63 Global attention on STI prevention and treatment dates back to the 1994 International Conference on Population and Development, where as a response to the rising incidence of STIs and a particular focus on women, a “Programme of Action” advised incorporating STI prevention and treatment services in reproductive and sexual health programs.64 Twenty years later, the goals of improving STI prevention and treatment services are unchanged. Gottlieb et al58 describe the overarching objectives of STI programs, which are to prevent new infection by focusing on behavioral modifications and to treat infections in order to prevent ongoing transmission. Meeting these goals, however, has proved challenging. Substantial progress in the prevention of STIs in lowresource settings has been hindered by a lack of focus on STIs as a result of prioritization of other global health concerns, scarcity of resources for primary prevention



efforts, and slow adherence to “safer sex” messages including abstinence, delay of sexual debut, monogamy, and condom use.58,62,64 The enormous attention and resources funneled toward the HIV epidemic have also threatened programmatic success in mitigating the adverse effects of other STIs.64 In addition, sexual forays may not always reflect sexual intentions in settings where negotiating power for members of vulnerable populations, including adolescents and women, is low and gender-based violence is high. Sex may therefore be either unplanned or forced, and in both scenarios, preventive measures for STI transmission are not often taken into consideration, leading to higher risk of infection.62,63 Attempts to treat and reduce the prevalence of STIs have been negatively affected by lack of access to treatment, antibiotic resistance to gonorrhea treatment regimens, underreporting of infections, and alternative care-seeking behavior with traditional healers and those outside the formal health care system.58 To help navigate STI control efforts moving forward, some have suggested using a model similar to the more successful HIV prevention and treatment programs. In contrast to rising rates of curable STIs, HIV infections have consistently declined over the last 2 decades partly due to a multipronged intervention termed “combination prevention,” which couples “behavioral, biomedical, and structural interventions” in a synergistic manner.64 Ensuring timely and effective treatment of other STIs directly affects HIV incidence and prevalence as HIV transmission has been shown to be facilitated by other STIs, most notably HSV-2 and syphilis, which each confer a 3-fold risk increase of HIVacquisition.59,62 Increased risk of HIV acquisition in the presence of gonorrhea or chlamydia has also been demonstrated.58 Thus, appropriately treating curable STIs has the potential to significantly decrease the incidence and prevalence of HIV. The syndromic approach to treatment is the mainstay of medical management of STIs in the developing world where reliable testing and laboratory infrastructure to accurately screen for and diagnose disease are scarce or nonexistent.64 The disadvantage with WHO’s recommendation for syndromic management, however, depends completely on symptomatic persons seeking treatment,58 which can be risky for 2 reasons: (1) persons presenting with nonspecific symptoms may be treated and labeled as having an STI leading both to overdiagnosis and overtreatment and the accompanying burden of the long-term sociocultural effects associated with an STI history, and (2) infected persons are not always symptomatic. In fact, the majority of STI-infected persons are asymptomatic.58 Unrecognized disease then

217

increases risk for ongoing transmission of disease within the population.58 In women at high risk for acquiring STIs, including sex workers, women in HIV discordant relationships, and injection drug users, stigma reduction and universal access to comprehensive family planning services have been touted as the most effective means to provide and encourage uptake of STI prevention and treatment methods.64 Three multipronged action points were developed by the WHO to combat the problematic effects of the STI burden on the developing world.59 These include the following: • scale-up of effective STI prevention services, including integration of STI services, including risk reduction and symptom recognition in primary care, reproductive health, and HIV care settings; • promotion of strategies to enhance STI prevention impact, including integration of STI services in routine health care settings, efforts to reduce the stigma associated with STIs, and improved data collection and surveillance systems for STIs; and • support for new technology development for STI prevention, including rapid testing for STIs, the development of vaccinations for STIs beyond what is available, and cost-effective single-dose treatment regimens. Primary prevention in the form of vaccinations is available only for hepatitis B and HPV. The hepatitis B vaccine has been available since 1982 and recommended by the WHO since 1992. The vaccination is 95% effective in infection prevention, and in the 90% of countries that have adopted vaccination, 90% coverage has been attained.58,59,61 Vaccinations for other STIs are not yet on the horizon. In addition to the WHO action points, interventions to lessen the impact of STIs such as integration of syphilis testing into antenatal care and microbicide use for HSV-2 and HIV prevention have been suggested as possible next steps.63 Prevention and treatment of STIs are of paramount importance, given the far-reaching implications of STI prevalence on the reproductive health and well-being of women. The multifactorial nature contributing to high global STI prevalence requires a multilayer intervention to combat disease in low-resource settings. A combination of approaches including primary prevention interventions, improved and reliable diagnosis, low-cost treatment modalities, and social efforts to decrease stigma associated with STIs and to address gender inequality is necessary if strides in the morbidity and mortality associated with STIs are to be made.63


218


UROGYNECOLOGIC DISEASE The consequences of urogynecologic disease in lowresource settings range from medical to social and economic and are costly both to affected individuals and to the societies in which they live. The deleterious impact of obstetric fistula or an abnormal communication between the vagina and either bladder or rectum, pelvic organ prolapse, and female genital mutilation (FGM) is underreported, overlooked, and understudied, largely as a result of the characteristically low socioeconomic status of the affected population.65,66 Yet the health effects of urogynecologic disease have serious implications on disease burden in the developing world. Fistula Obstetric fistula results from ischemia of pelvic floor tissue in instances of obstructed labor without timely intervention. Labor abnormalities coupled with poor access to obstetric care and lack of emergency obstetric services lead to increased risk of fistula formation and poor obstetric outcomes in poor, young, illiterate, primiparous women living and laboring in rural areas.65,66 Although less common than obstetric fistula, traumatic gynecologic fistulas occurring after domestic violence also affect the health of women in low-resource settings and result in similar physical health repercussions.67 The associated leakage of urine or feces, depending on the location of the abnormal communication, can be debilitating physically, whereas the odor associated with leakage has been shown to affect the emotional and social well-being of affected women, often leading to social isolation, depression, dissolution of marriages, and inability to work.66,68 The prevalence of fistula at a population level is estimated at 0.29 per 1000 women; however, regional disparities are present.69 Fistulas are most common in Sub-Saharan Africa (1.57 per 1000 women) and Asia (1.20 per 1000 women), regions where the status of women is low and prioritization of women’s health remains a work in progress.65,69,70 More common in adolescents with small and underdeveloped pelvises, one of the strategies to decrease the incidence of fistulas is through advocacy to increase minimum age for marriage in societies where women marry young, delaying age at first pregnancy and increasing access to maternity and family planning services.65,70,71 For affected women, fistula repair is an option at designated fistula centers throughout the developing world, although barriers to accessing repair services include lack of knowledge regarding surgical options, cost of the procedure, scarcity of providers trained in repair, and lack of capable facilities where a repair can be performed.66,71 Based on the 2006 WHO

guidelines for fistula management and program development, fistula centers, or centers well versed in caring for affected women, are expected to have an 85% success rate of closure with 90% or more resolved incontinence. Of nearly equal importance to surgery in the health and well-being of fistula patients is the societal reintegration, which relies on intensive counseling and physical and social rehabilitation.71 Pelvic Organ Prolapse According to a 2011 Cochrane Review examining management options for pelvic organ prolapse, an estimated 50% of parous women experience prolapse to some degree irrespective of delivery route.72,73 Prolapse results from an increase in intra-abdominal pressure whether as a result of pregnancy and childbearing, constipation, chronic cough, or physically laborious work such as farming or heavy lifting in resource-poor settings especially.73 Reported symptoms include physical discomfort due to pelvic heaviness or presence of a bulge, bowel and bladder changes, and sexual dysfunction. A study examining Nigerian women with pelvic floor disorders observed an increased risk of depression in affected women as well.68 Treatment is guided by degree of prolapse and symptoms and may include conservative therapies such as pelvic floor training or lifestyle modifications, mechanical therapy using pessaries, and surgical treatment to reduce prolapse and repair the pelvic floor.71,73 To gain a better understanding of the risks of prolapse in low-resource settings more specifically, where larger family sizes and hard labor are more common than in developed countries, Eleje et al73 performed a retrospective chart review of gynecologic clinic patients at a teaching hospital in Nigeria over a 5-year period. Determinants of prolapse were actually found to be quite similar to those reported in mainstream literature. Menopausal status, increasing parity, history of increased intra-abdominal pressure, low educational attainment, and aging were found to commonly affect the patient population in Nigeria.73 Although factors leading to prolapse are well known and demonstrated in the literature, a paucity of data exists discussing preventive measures to reduce the incidence of prolapse. Female Genital Mutilation According to the WHO, FGM encompasses practices, which involve “partial or total removal of the external female genitalia or other injury to the female genital organs for nonmedical reasons.”74 The procedure is performed as part of cultural and religious ceremonies or rites-of-passage procedures, and in parts of



Asia, the Middle East, and Africa, where FGM is most common, it has become part of the social norm.74 One hundred million to 140 million girls and women worldwide are estimated to have undergone FGM.74 True estimates of FGM prevalence are difficult to ascertain because of the sensitive nature of the procedure and reliance on self-reporting behaviors.75 However, geographic and ethnic differences in the prevalence of FGM and in the extent of genitalia mutilated are known to exist.74 Alteration of female genitalia has been associated with enhanced sexual desirability for men and decreased risks of infidelity and sexual immorality for affected women.74 Although FGM has been purported to improve the health and hygiene of women, these claims have not been substantiated. In fact, the WHO stated that no health benefits are conferred on female recipients of mutilation techniques75,76 and in fact can cause long-term consequences such as recurrent urinary tract infections, cysts, infertility, increased risk for complications related to childbirth, and need for surgical intervention later in life.77 A systematic review examining key factors contributing to continuation of FGM was conducted by Berg and Underland.75 The authors cite “cultural tradition, sexual morals, marriageability, religion, health benefits, and male sexual enjoyment” as incentives to continue the practice.75 Alternatively, deterrents to mutilation include health consequences, realization that FGM is not a religious mandate, illegal nature of act, and rejection of the practice by Western countries where exiled members of countries with high FGM rates are now living.75 To date, efforts to reduce the prevalence of FGM have focused on educational and legislative interventions.75 As a result of an emphasis on legal procedures to end FGM, 23 countries in Africa had imposed restrictive legislation on FGM as of 2012.78 Continuation of FGM, however, is still likely unless gender relations are adequately addressed. Gender inequality is one of the driving forces perpetuating FGM; thus, preventive measures aimed at FGM decline must consider power differences among men and women and aim to prioritize women’s rights.74 CONCLUSIONS Prevention is the common thread among gynecologic health conditions in the developing world. Cervical cancer is largely preventable through screening and treatment for precancerous lesions. Complications related to unintended pregnancy and unsafe abortion are preventable through access to effective contraception and safe abortion services. Sexually transmitted infection

219

acquisition and its associated morbidity are preventable through timely treatment. Urogynecologic complications resulting from prolonged unattended labor are preventable through access to skilled delivery. Similarly, in the United States, gynecologic disease is largely preventable. Yet, rates of cervical cancer, unintended pregnancy, and STIs in particular are disproportionately higher in a subset of women—those who are young, racial and ethnic minorities, and poor and who live in geographically remote areas. Cervical cancer rates in the United States have decreased dramatically as a result of widespread availability of screening modalities.13 However, racial, ethnic, and socioeconomic disparities in screening, incidence and mortality rates persist. Black women have the highest mortality due to cervical cancer, whereas Hispanic women have the highest incidence of disease.79 The majority of new cancers occur among women who have never been screened or who have not been screened at the recommended intervals.11 Recent data published by the Centers for Disease Control and Prevention show 11.4% of American women within the recommended screening age of 21 to 65 years have not been screened within the last 5 years.11 According to the 2012 Behavioral Risk Factor Surveillance System findings, regional predilections, health insurance status, and lack of a routine health care provider were shown to most heavily influence nonadherence to screening recommendations for the reported 8 million unscreened women. Disparities in reproductive health outcomes, such as disparities seen in cervical cancer, continue to exist in the United States as well. It has been well documented that racial minorities have higher rates of unintended pregnancy and STIs than their white counterparts.80,81 In addition to race, other social determinants such as low socioeconomic and educational statuses are known factors that impact reproductive health. Finer and Zolna80 combined data from several national reproductive health surveys and demonstrated an inverse correlation between unintended pregnancy rate and years of educational attainment. The same was seen with income and unintended pregnancy rate—higher-income women had the lowest rates of unintended pregnancy, whereas the opposite is true of poorer women. Outcomes for STIs mimic the trend in pregnancy intentions. Ineffective use of contraceptive barrier methods not only contributes to unintended pregnancy, but also leads to an increase in STIs in high-risk populations such as racial minorities and poor women.81 When comparing young black women, aged 15 to 19 years, with whites in the same age bracket, significantly higher STI rates have been observed. Black teens are


220


16 times more likely than whites to be infected with gonorrhea, 6 times more likely to be infected with chlamydia, and 30 times more likely to be infected with syphilis.82 American Indians/Alaska Natives and Hispanics also have higher STI rates in comparison to whites.82 Blacks also bear the burden of HIV in the United States, with new infections among black women estimated at 20 times the rate of new infections in whites and 5 times the rate of Hispanic women.83 Women at risk for poor gynecologic health outcomes in the United States share risk factors with high-risk women in the developing world. Common themes of poverty, youth, low educational status, and poor access to care have impacted the incidence and prevalence of gynecologic disease both at home and abroad. In both settings, increased attention to preventive measures such as education, vaccinations, and improved access to reproductive health care has the highest potential of reducing reproductive health disparities among women both in the United States and throughout the developing world. REFERENCES 1. United Nations. 2010. Millennium Development Goals indicators. Available at: http://mdgs.un.org/unsd/mdg/Default.aspx. Accessed December 13, 2014. 2. Kahn KS, Wojdyla D, Say L, et al. WHO analysis of causes of maternal death: a systematic review. Lancet. 2006;367:1066–1074. 3. Say L, Chou D, Gemmill A, et al. Global causes of maternal death: a WHO systematic analysis. Lancet. 2014;2:3323–3333. 4. Ferlay J, Soerjomataram I, Ervik M, et al. GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC Cancer Base No. 11 [Internet]. Lyon, France: International Agency for Research on Cancer; 2013. Available at: http://globocan.iarc.fr. Accessed August 9, 2014. 5. Dehlendorf C, Rodriguez MI, Levy K, et al. Disparities in family planning. Am J Obstet Gynecol. 2011;202:214–220. 6. Grimes DA, Benson J, Singh S, et al. Unsafe abortion: the preventable pandemic. Lancet. 2006;368:1908–1919. 7. Campbell M, Sahin-Hodoglugil NN, Potts M. Barriers to fertility regulation: a review of the literature. Stud Fam Plann. 2006; 37:87–98. 8. World Health Organization. Optimizing Health Worker Roles To Improve Access to Key Maternal and Newborn Health Interventions Through Task Shifting. Geneva, Switzerland: World Health Organization; 2012. Available at: http://www.who.int/reproductivehealth/ publications/maternal_perinatal_health/978924504843/en/. Accessed September 8, 2014. 9. McCleary-Sills J, McGonagle A, Malhotra A. Women's Demand for Reproductive Control: Understanding and Addressing Gender Barriers, Washington, DC: International Center for Research on Women; 2012. 10. Centers for Disease Control and Prevention. CDC health disparities and inequalities report—United States, 2011. MMWR. 2011;60 (suppl):1–109. 11. Benard VB, Thomas CC, King J, et al. Vital signs: cervical cancer incidence, mortality, and screening—United States, 2007-2012. MMWR. 2014;4:1004–1009. 12. World Health Organization. Comprehensive Cervical Cancer Prevention and Control: A Healthier Future for Girls and Women. Geneva, Switzerland: World Health Organization; 2013.

13. Saslow D, Solomon D, Lawson HW, et al. American Cancer Society, American Society for Colposcopy and Cervical Pathology, and American Society for Clinical Pathology Screening Guidelines for the prevention and early detection of cervical cancer. J Low Genit Tract Dis. 2012;16:175–204. 14. World Health Organization. Cervical Cancer Screening in Developing Countries: Report of a WHO Consultation. Geneva, Switzerland: World Health Organization; 2002. 15. Denny L, Kuhn L, de Souza M, et al. Screen-and-treat approaches for cervical cancer prevention in low-resource settings: a randomized controlled trial. JAMA. 2005;294:2173–2181. 16. Gakidou E, Nordhagen S, Obermeyer Z. Coverage of cervical cancer screening in 57 countries: low average levels and large inequalities. PLoS Med. 2008;5:e132. 17. Camacho Carr K, Sellors JW. Cervical cancer screening in low resource settings using visual inspection with acetic acid. J Midwifery Womens Health. 2004;49:329–337. 18. Ndikom CM, Ofi BA. Awareness, perception and factors affecting utilization of cervical cancer screening services among women in Ibadan, Nigeria: a qualitative study. Reprod Health. 2012;9:11. 19. Agosti JM, Goldie SJ. Introducing HPV vaccine in developing countries—key challenges and issues. N Engl J Med. 2007;356: 1908–1910. 20. Blumenthal PD, Lauterbach M, Sellors JW, et al. Training for cervical cancer prevention programs in low-resource settings: focus on visual inspection with acetic acid and cryotherapy. Int J Gynecol Obstet. 2005;89(suppl 2):S30–S37. 21. Hegde D, Shetty H, Shetty PK, et al. Diagnostic value of acetic acid comparing with conventional Pap smear in the detection of colposcopic biopsy–proved CIN. J Cancer Res Ther. 2011; 7:454–458. 22. Perkins RB, Langrish SM, Stern FJ, et al. Comparison of visual inspection and Papanicolaou (Pap) smears for cervical cancer screening in Honduras: should PAP smears be abandoned? Trop Med Int Health. 2007;12:1018–1025. 23. Sankaranarayanan R, Esmy PO, Rajkumar R, et al. Effect of visual screening on cervical cancer incidence and mortality in Tamil Nadu, India: a cluster-randomised trial. Lancet. 2007;370:398–406. 24. Aggarwal P, Batra S, Gandhi G, et al. Comparison of Papanicolaou test with visual detection tests in screening for cervical cancer and developing the optimal strategy for low resource settings. Int J Gynecol Cancer. 2010;20:862–868. 25. Gaffikin L, Lauterbach M, Emerson M. Safety, Acceptability, and Feasibility of a Single Visit Approach to Cervical Cancer Prevention: Results From a Demonstration Project in Rural Thailand. Baltimore, MD: JHPIEGO Corporation; 2003. 26. World Health Organization. Prevention of Cervical Cancer Through Screening Using Visual Inspection With Acetic Acid (VIA) and Treatment With Cryotherapy: A Demonstration Project in Six African Countries (Malawi, Madagascar, Nigeria, Uganda, the United Republic of Tanzania, and Zambia). Geneva, Switzerland: World Health Organization; 2012. 27. Jacob M, Broekuhizen FF, Castro W, et al. Experience using cryotherapy for treatment of cervical precancerous lesions in low-resource settings. Int J Gynaecol Obstet. 2005;89(suppl 2): S13–S20. 28. World Health Organization. Guidelines for Screening and Treatment of Precancerous Lesions for Cervical Cancer Prevention. Geneva, Switzerland: World Health Organization; 2013. 29. Cleland J, Conde-Agudelo A, Peterson H, et al. Contraception and health. Lancet. 2012;380:149–156. 30. Stover J, Ross J. How increased contraceptive use has reduced maternal mortality. Matern Child Health J. 2010;14:687–695. 31. Ahmed S, Li Q, Liu L, et al. Maternal deaths averted by contraceptive use: an analysis of 172 countries. Lancet. 2012;380:111–125. 32. World Health Organization. Family Planning Fact Sheet No. 351. [WHO Web site]. May 2013. Available at: http://www.who.int/ mediacentre/factsheets/fs351/en/. Accessed November 7, 2014. 33. Darroch JE. Trends in contraceptive use. Contraception. 2013; 87:259–263.


Global Women’s Health • CME Review Article 34. Darroch JE, Sedgh G, Ball H. Contraceptive Technologies: Responding to Women’s Needs. New York: Guttmacher Institute; 2011. 35. Darroch JE, Singh S. Trends in contraceptive need and use in developing countries in 2003, 2008, and 2012: an analysis of national surveys. Lancet. 2013;381:1756–1762. 36. Singh S, Darroch JE. Adding It Up: Costs and Benefits of Contraceptive Services—Estimates for 2012. New York: Guttmacher Institute and United Nations Population Fund (UNFPA); 2012. Available at: http://www. guttmacher.org/pubs/AIU-2012estimates.pdf. Accessed September 24, 2014. 37. Faúndes A. Unsafe abortion—the current global scenario. Best Pract Res Clin Obstet Gynaecol. 2010;24:467–477. 38. Greene E, Stanback J. Old barriers need not apply: opening doors for new contraceptives in the developing world. Contraception. 2012;85:11–14. 39. Bertrand JT, Hardee K, Magnani RJ, et al. Access, quality of care and medical barriers in family planning programs. Int Fam Plan Perspect. 1995;21:64–69. 40. Speizer IS, Hotchkissk DR, Magnani RJ, et al. Do service providers in Tanzania unnecessarily restrict clients’ access to contraceptive methods? Int Fam Plan Perspect. 2000;26:13–20. 41. Ross J, Hardee K, Mumford E, et al. Contraceptive method choice in developing countries. Int Fam Plan Perspect. 2002;28:32–40. 42. Williamson LM, Parkes A, Wight D, et al. Limits to modern contraceptive use among young women in developing countries: a systematic review of qualitative research. Reprod Health. 2009;6:3. 43. Creanga AA, Gillespie D, Karklins S, et al. Low use of contraception among poor women in Africa: an equity issue. Bull World Health Organ. 2011;89:258–266. 44. World Health Organization. Unsafe Abortion: Global and Regional Estimates of the Incidence of Unsafe Abortion and Associated Mortality in 2008. Geneva, Switzerland: World Health Organization; 2011. 45. Sedgh G, Singh S, Hussain R. Intended and unintended pregnancies worldwide in 2012 and recent trends. Stud Fam Plann. 2014;45:301–314. 46. Sedgh G, Hussain R, Bankole A, et al. Women With an Unmet Need for Contraception in Developing Countries and Their Reasons for Not Using a Method. Occasional Report. New York: Guttmacher Institute; 2007 No. 37. 47. Ahman E, Shah IH. New estimates and trends regarding unsafe abortion mortality. Int J Gynaecol Obstet. 2011;115:121–126. 48. Singh S. Hospital admissions resulting from unsafe abortion: estimates from 13 developing countries. Lancet. 2006;368: 1887–1892. 49. Shah IH, Ahman E. Unsafe abortion in 2008: global and regional levels and trends. Reprod Health Matters. 2010;18:90–101. 50. Jewkes RK, Gumede T, Westaway MS, et al. Why are women still aborting outside designated facilities in metropolitan South Africa? BJOG. 2005;112:1236–1242. 51. Sedgh G, Singh S, Henshaw SK, et al. Legal abortion worldwide in 2008: levels and recent trends. Perspect Sex Reprod Health. 2011;43:188–198. 52. World Health Organization. Family Planning: A Global Handbook for Providers. Geneva, Switzerland: World Health Organization; 2011. 53. Jhpiego Corporation. Family Planning and Reproductive Health [Jhpiego Web site]. Available at: http://www.jhpiego.org/content/ family-planning-and-reproductive-health. Accessed October 28, 2014. 54. Population Services International. Postpartum IUD Insertion [PSI Web site]. 2014. Available at: http://www.psi.org/program/postpartum-iud-insertion/. Accessed November 7, 2014. 55. Mbizvo MT, Phillips SJ. Family planning: Choices and challenges for developing countries. Best Pract Res Clin Obstet Gynaecol. 2014;28:931–943. 56. Fabic MS, Choi Y, Bongaarts J, et al. Meeting demand for family planning within a generation: The post-2015 agenda. Lancet. 2014.

57. 58.

59.

60.

61.

62. 63. 64.

65. 66. 67. 68. 69. 70. 71. 72. 73. 74. 75.

76.

77.

221

Available at: http://dx.doi.org/10.1016/S0140-6736(14)61055-2. Accessed September 24, 2014. World Health Organization. Global Incidence and Prevalence of Selected Curable Sexually Transmitted Infections—2008. Geneva, Switzerland: World Health Organization; 2012. Gottlieb SL, Low N, Newman LM, et al. Toward global prevention of sexually transmitted infections (STIs): the need for STI vaccines. Vaccine. 2014;32:1527–1535. World Health Organization. Sexually Transmitted Infections (STIs): The Importance of a Renewed Commitment to STI Prevention and Control in Achieving Global Sexual and Reproductive Health. Geneva, Switzerland: World Health Organization; 2014. UNAIDS. AIDS by the Numbers. Geneva, Switzerland: UNAIDS; 2013. Available at: http://www.unaids.org/sites/default/files/ media_asset/JC2571_AIDS_by_the_numbers_en_1.pdf. Accessed October 16, 2014. World Health Organization. Hepatitis B. Geneva, Switzerland: World Health Organization; 2014. Available at: http://www. who.int/mediacentre/factsheets/fs204/en/. Accessed August 27, 2014. Mayaud P, Maybe D. Approaches to the control of sexually transmitted infections in developing countries: old problems and modern challenges. Sex Transm Infect. 2004;80:174–182. Gottlieb SL, Newman LM, Amin A, et al. Sexually transmitted infections and women’s sexual and reproductive health. Int J Gynaecol Obstet. 2013;123:183–184. Ortayli N, Ringheim K, Collins L, et al. Sexually transmitted infections: Progress and challenges since the 1994 international conference on population and development (ICPD). Contraception. 2014;90(6 Suppl):S22–S31. Capes T, Ascher-Walsh C, Abdoulaye I, et al. Obstetric fistula in low and middle income countries. Mt Sinai J Med. 2011; 78:352–361. Kayondo M, Wasswa S, Kabakyenga J, et al. Predictors and outcome of surgical repair of obstetric fistula at a regional referral hospital, Mbarara, Western Uganda. BMC Urol. 2011;11:1–9. Onsrud M, Sjoveian S, Lubiriri R, et al. Sexual violence-related fistulas in the Democratic Republic of Congo. Int J Gynaecol Obstet. 2008;103:265–269. Zeleke BM, Avele TA, Woldetsadik MA, et al. Depression among women with obstetric fistula, and pelvic organ prolapse in northwest Ethiopia. BMC Psychiatry. 2013;13:236. Adler AJ, Ronsmans C, Calvert C, et al. Estimating the prevalence of obstetric fistula: a systematic review and meta-analysis. BMC Pregnancy Childbirth. 2013;13:246. Melah GS, Massa AA, Yahaya UR, et al. Risk factors for obstetric fistulae in North-Eastern Nigeria. J Obstet Gynecol. 2007; 27:819–823. World Health Organization (WHO). Obstetric Fistula: Guiding Principles for Clinical Management and Programme Development. Geneva, Switzerland: World Health Organization; 2006. Hagen S, Stark D. Conservative prevention and management of pelvic organ prolapse in women. Cochrane Database Syst Rev. 2011;12:1–69. Eleje GU, Udeghunam OI, Ofojebe CJ, et al. Determinants and management outcomes of pelvic organ prolapse in a low resource setting. Ann Med Health Sci Res. 2012;495:796–801. World Health Organization. Eliminating Female Genital Mutilation: An Interagency Statement. Geneva, Switzerland: World Health Organization; 2008. Berg RC, Underland V. Gynecological consequences of female genital mutilation/cutting: a systematic review and meta-analysis. Obstet Gynecol Int. 2013;2013:496564. World Health Organization. A Multi-country Study on Gender, Sexuality and Vaginal Practices: Implications for Sexual Health. Geneva, Switzerland: World Health Organization; 2012. World Health Organization. Female Genital Mutilation. Geneva, Switzerland: World Health Organization; 2014. Available at: http:// www.who.int/mediacentre/factsheets/fs241/en/. Accessed August 27, 2014.


222


78. Yoder PS, Wang S, Johansen E. Estimates of female genital mutilation/cutting in 27 African countries and Yemen. Stud Fam Plann. 2013;44:189–204. 79. Centers for Disease Control and Prevention. Cervical cancer rates by race and ethnicity [CDC Web site]. August 27, 2014. Available at: http://www.cdc.gov/cancer/cervical/statistics/race. htm. Accessed November 5, 2014. 80. Finer LB, Zolna MR. Unintended pregnancy in the United States: incidence and disparities, 2006. Contraception. 2011;84:478–485.

81. Sonfield A. New study points to high STI rates among teens, major disparities among population groups. Guttmacher Policy Review. 2008;11:20 82. Centers for Disease Control and Prevention. Sexually Transmitted Disease Surveillance 2011. Atlanta, GA: US Department of Health and Human Services; 2012. 83. Centers for Disease Control and Prevention. Estimated HIV incidence among adults and adolescents in the United States, 2007–2010. HIV Surveill Suppl Rep. 2012;17:1–26.


PCT perspective: primary care is more than health.

Redefining global health priorities: Improving cancer care in developing settings.

The Pan-University Network for Global Health: framework for collaboration and review of global health needs.

Ensuring the security of health care in conflict settings: an urgent global health concern.

Perceptions of postnatal depression and health care needs in a South African sample: the "mental" in maternal health care.

Test result management in global health settings.

Global maternal health: from women's survival to respectful care.

Mental health: More than neurobiology.

Maternal - Child Health Needs Assessment in Haiti.

Towards a more nuanced global mental health.

DeSalvo: health IT is 'more than just EHRs'.

Our health is global health.

Global health response to crises needs reform.

Patient Education. The Nutrition Needs of Patients With Chronic Kidney Disease in Health Care Community Settings.

When is a global health program global?

Bone health in children with special health care needs.

Hazardous waste compliance in health care settings.

Open learning in health care settings.

More than just the T-shirt: reflections from first-time participants in global health service.

Global health care of the critically ill in low-resource settings.

One Health: more than just collaboration.

Towards an agenda for implementation science in global health: there is nothing more practical than good (social science) theories.

The global health financing revolution: why maternal health is missing the boat.

Lessons from the Field Count more than Ever: The New Era of Global Health.