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Lower Levels of Antiretroviral Therapy Enrollment Among Men with HIV Compared with Women — 12 Countries, 2002–2013

Andrew F. Auld, MBChB1; Ray W. Shiraishi, PhD1; Francisco Mbofana, MD2; Aleny Couto, MD2; Ernest Benny Fetogang, PhD3; Shenaaz El-Halabi, MPH3; Refeletswe Lebelonyane, MD3; Pilatwe Tlhagiso Pilatwe, MSc3; Ndapewa Hamunime, MD4; Velephi Okello, MD5; Tsitsi Mutasa-Apollo, MBChB6; Owen Mugurungi, MD6; Joseph Murungu, MD6; Janet Dzangare, MSc6; Gideon Kwesigabo, MD7; Fred Wabwire-Mangen, MD8; Modest Mulenga, MD9; Sebastian Hachizovu, MBChB9; Virginie Ettiegne-Traore, MD10; Fayama Mohamed, MSAE11; Adebobola Bashorun, MD12; Do Thi Nhan, MD13; Nguyen Huu Hai, MD13; Tran Huu Quang, MSc14; Joelle Deas Van Onacker, MD15; Kesner Francois, MD15; Ermane G. Robin, MD15; Gracia Desforges, MD15; Mansour Farahani, MD16; Harrison Kamiru, DrPH17; Harriet Nuwagaba-Biribonwoha, MBChB17; Peter Ehrenkranz, MD18; Julie A. Denison, PhD19; Olivier Koole, MD20; Sharon Tsui, MPH19; Kwasi Torpey, PhD21; Ya Diul Mukadi, MD22; Eric van Praag, MD23; Joris Menten, MSc20; Timothy D. Mastro, MD24; Carol Dukes Hamilton, MD24; Oseni Omomo Abiri, MPH25; Mark Griswold, MSc26; Edna Pierre, MD26; Carla Xavier, MSc27; Charity Alfredo, MD27; Kebba Jobarteh, MD27; Mpho Letebele, MD28; Simon Agolory, MD29; Andrew L. Baughman, PhD29; Gram Mutandi, MBChB29; Peter Preko, MD25; Caroline Ryan, MD30; Trong Ao, ScD30; Elizabeth Gonese, MPH31; Amy Herman-Roloff, PhD31; Kunomboa A. Ekra, MD32; Joseph S. Kouakou, MD32; Solomon Odafe, MD33; Dennis Onotu, MD33; Ibrahim Dalhatu, MD33; Henry H. Debem33; Duc B. Nguyen, MD34; Le Ngoc Yen, MD34; Abu S. Abdul-Quader, PhD34; Valerie Pelletier, MD35; Seymour G. Williams, MD36; Stephanie Behel, MPH1; George Bicego, PhD1; Mahesh Swaminathan, MD1; E. Kainne Dokubo, MD1; Georgette Adjorlolo-Johnson, MD37; Richard Marlink, MD16; David Lowrance, MD38; Thomas Spira, MD1; Robert Colebunders, MD20; David Bangsberg, MD39; Aaron Zee, MPH1; Jonathan Kaplan, MD1; Tedd V. Ellerbrock, MD1

Equitable access to antiretroviral therapy (ART) for men and women with human immunodeficiency virus (HIV) infection is a principle endorsed by most countries and funding bodies, including the U.S. President's Emergency Plan for AIDS (acquired immunodeficiency syndrome) Relief (PEPFAR) (1). To evaluate gender equity in ART access among adults (defined for this report as persons aged ≥15 years), 765,087 adult ART patient medical records from 12 countries in five geographic regions* were analyzed to estimate the ratio of women to men among new ART enrollees for each calendar year during 2002–2013. This annual ratio was compared with estimates from the Joint United Nations Programme on HIV/AIDS (UNAIDS) of the ratio of HIV-infected adult women to men in the general population. In all 10 African countries and Haiti, the most recent estimates of the ratio of adult women to men among new ART enrollees significantly exceeded the UNAIDS estimates for the female-to-male ratio among HIV-infected adults by 23%–83%. In six African countries and Haiti, the ratio of women to men among new adult ART enrollees increased more sharply over time than the estimated UNAIDS female-to-male ratio among adults with HIV in the general population. Increased ART coverage among men is needed to decrease their morbidity and mortality and to reduce HIV incidence among their sexual partners. Reaching more men with HIV testing and linkage-to-care services and adoption of test-and-treat ART eligibility guidelines (i.e., regular testing of adults, and offering treatment to all infected persons with ART, regardless of CD4 cell test results) could reduce gender inequity in ART coverage.

Three approaches to sampling and analysis were employed in the 12 studied countries (Table). In Botswana, Haiti, Mozambique, and Namibia, where large, centralized, electronic ART patient monitoring systems are employed, all available data from 2002–2013 were analyzed. In each of these countries, 67%–100% of all ART patients and 58%–100% of all ART facilities were captured in the electronic system. In Côte d'Ivoire, Nigeria, Swaziland, Vietnam, and Zimbabwe, nationally representative samples of ART facilities were selected, with probability of selection proportional to size. In Tanzania, Uganda, and Zambia, health facilities were purposively selected by investigators to represent the range of ART facilities in each country and ensure that the study remained feasible. Among the eight sample-based surveys, a sample frame of study-eligible ART patients was created at each selected facility, and simple random sampling was used to select the sample of records. Eligibility criteria included initiation of ART ≥6 months before data abstraction, during 2002–2013, and at age ≥15 years. Data were abstracted from ART records onto standardized abstraction forms by trained study personnel.

For each of the 12 countries, the ratio of women to men who were newly enrolled in ART during 2002–2013 was compared with the current ratio of women to men among cumulative ART patients who were alive on ART by the end of each calendar year and with UNAIDS estimates of the ratio of women to men among adults living with HIV for each calendar year. To assess a country's ART program accessibility to women with HIV compared with men with HIV, the percent difference between the most recently available female-to-male new ART enrollee ratio and the UNAIDS estimate of the ratio of women to men among persons with HIV in the general population for the same calendar year was calculated. Data were analyzed using statistical software, and study design was controlled for during analyses.

Across the 12 countries, 765,087 adult ART patient records were analyzed. (Graphs of data for all countries are available online at http://stacks.cdc.gov/view/cdc/35684.) In all countries except Vietnam, the most recent estimates of the female-to-male ratio among new ART enrollees, and the ratio of women to men currently enrolled in ART exceeded the UNAIDS female-to-male ratios among persons with HIV. In addition, in seven countries (Botswana, Côte d'Ivoire, Haiti, Nigeria, Mozambique, Swaziland, and Zambia), point estimates of the ratio of female-to-male new ART enrollees increased more sharply over time than did the UNAIDS female-to-male ratios among persons with HIV. The trends in female-to-male ratios of current ART enrollees closely paralleled the new ART enrollee ratio trends.

In east Africa, the most recent female-to-male new ART enrollee ratios were 2.10 in both Tanzania and Uganda for 2009; in contrast, the 2009 UNAIDS female-to-male ratios among adults with HIV were 1.38 and 1.31, respectively. Compared with males, adult females with HIV were approximately 53% and 60% more likely to access ART in Tanzania and Uganda, respectively (Figure).

In southern Africa, the most recent female-to-male new ART enrollee ratios were 1.95 in Botswana (2013); 2.73 in Mozambique (2013); 1.61 in Namibia (2012); 1.91 (95% confidence interval [CI] = 1.70–2.13) in Swaziland (2010); 1.57 in Zambia (2009); and 1.76 (95% CI = 1.53–1.99) in Zimbabwe (2009); whereas the corresponding calendar year UNAIDS female-to-male ratios among adults with HIV for these countries were 1.30, 1.49, 1.13, 1.43, 1.05, and 1.43, respectively. Compared with males living with HIV in southern Africa, females living with HIV were 23%–83% more likely to access ART (Figure).

In west Africa, the most recent female-to-male new ART enrollee ratios were 2.21 (95% CI = 1.77–2.64) in Côte d'Ivoire (2007) and 2.34 (95% CI = 1.86–2.83) in Nigeria (2011); the corresponding calendar year UNAIDS female-to-male ratios among adults with HIV were 1.28 and 1.34, respectively. Compared with men, adult women with HIV were about 73% and 75% more likely to access ART in Côte d'Ivoire and Nigeria, respectively.

In Haiti in 2013, the female-to-male new ART enrollee ratio was 1.89, and the UNAIDS female-to-male ratio among persons with HIV was 1.43. Compared with men, adult women with HIV were 32% more likely to access ART in 2013. Finally, in Vietnam in 2009, the female-to-male new ART enrollee ratio was 0.34 (95% CI = 0.27–0.41), which was similar to the UNAIDS female-to-male ratio among persons with HIV (0.39).

Discussion

This analysis of 765,087 adult ART patient records from 12 countries is the most up-to-date and comprehensive assessment of disproportionate ART enrollment among adult women with HIV compared with men, in resource-limited settings (2). In 10 African countries and Haiti (countries with generalized HIV epidemics) women with HIV were more likely to access ART than men with HIV. In addition, in six African countries and Haiti, gender-related disparities in ART coverage appear to be increasing over time. The adult ART program sex distribution was largely reflective of the UNAIDS female-to-male ratio among persons with HIV in only one country, Vietnam.

Higher ART coverage among adult women with HIV in the African countries and Haiti could occur for a number of potential reasons. First, HIV testing and counseling is a part of routine antenatal care, which provides an early entry point to ART for women with HIV. Second, ART eligibility criteria are currently more inclusive for adult women with HIV than men because, to prevent mother-to-child transmission (PMTCT) for pregnant women with HIV, all 12 countries except Nigeria§ have adopted guidelines recommending universal, lifelong ART, regardless of the results of the CD4 cell count test (referred to as PMTCT Option B+). Third, differences between men and women in health-seeking behavior might also play a role, with men considered more likely to delay access to health care for reasons that include stigma, male norms that discourage admitting ill health, and employment responsibilities, which might involve within-country and cross-border migration (3).

In many of the countries studied, gender inequity in ART coverage appears to be increasing. At the patient level, the recent initiation of PMTCT B+ might explain recent disproportionate accelerations in ART coverage among women in some countries (e.g., Mozambique initiated PMTCT B+ in 2013). However, at governance- and funder-levels, lack of initiatives to address gender inequities in ART coverage might result from tacitly holding men responsible for failing to access ART services, rather than assigning responsibility for improving male ART coverage to global health programs (4). Recent data show that men's health is often considered a lower priority than women's health in global health programs (5). However, this prioritization is not based on disease burden as estimated using disability-adjusted life years: HIV and the other nine top contributors to global disability-adjusted life years are more burdensome in men than in women (5).

Of the 12 countries studied, only Vietnam had female-to-male new ART enrollee ratios similar to UNAIDS female-to-male ratios among persons with HIV. A possible explanation is that Vietnam has a concentrated epidemic, affecting predominantly male persons who inject drugs, and therefore, from the beginning, the ART program in Vietnam has been focused on addressing the disease within this population (6). In Vietnam, men with HIV commonly access ART through routine HIV testing and counseling at needle and syringe exchange programs and methadone maintenance therapy clinics (6). In contrast, women with HIV primarily access HIV testing and linkage to ART via outreach activities to female sex workers, and through routine HIV testing at antenatal care clinics; this coverage was low in 2005, but is increasing (6,7). Continued monitoring of Vietnam's ART program gender ratios is warranted, as women account for increasing proportions of new HIV infections (6).

The findings in this report are subject to at least four limitations. First, UNAIDS estimates of female-to-male ratios among all persons with HIV are derived from epidemic models with inherent uncertainty, limiting the ability to make statistical comparisons between UNAIDS-derived and cohort-derived ratios. Second, cohort data varied in size and generalizability. Third, this study analyzed average female-to-male ratios for adults; future analyses to examine effect modification across adult age groups are needed. Finally, this analysis did not evaluate gender ratios among persons being tested for HIV or linking to care, which would help explain observed ratios among ART enrollees.

Increasing ART coverage among men with HIV would reduce morbidity and mortality in this group and contribute to reducing HIV incidence among their sex partners (8), including adolescent girls and young women, a priority population for PEPFAR. Strategic program changes needed to reach more HIV-infected men with ART include identification of routine HIV testing systems, similar to HIV testing and counseling for women in antenatal care settings, and adoption of test-and-treat guidelines, which was recommended by the World Health Organization for the first time this year (9). Although more data on how to increase HIV testing and linkage to ART among HIV-infected men in resource-limited settings are needed, available evidence suggests a strategic combination of facility- and community-based approaches is required (10). From a program management perspective, ensuring that men are not overlooked in gender-related strategic documents prepared by funders (5), special initiatives to reach men with HIV, performance-based financing that provides incentives to reach both men and women, and tailored program evaluation strategies, including gender disaggregation of HIV treatment cohort data (5), are needed.


1Division of Global HIV/AIDS, Center for Global Health, CDC; 2National Institute of Health, Mozambique; 3Ministry of Health, Botswana; 4Ministry of Health and Social Services, Namibia; 5Ministry of Health, Swaziland; 6Ministry of Health, Zimbabwe; 7Muhimbili University of Health and Allied Sciences, Tanzania; 8Infectious Diseases Institute, Makerere University College of Health Sciences, Uganda; 9Tropical Diseases Research Center, Zambia; 10Ministry of Health, Côte d'Ivoire; 11Directorate General of Budget and Finance, Côte d'Ivoire; 12Ministry of Health, Nigeria; 13Vietnam Authority of HIV/AIDS Control, Vietnam; 14Hanoi School of Public Health, Vietnam; 15Programme National Lutte Sida/MSPP, Haiti; 16Harvard T.H. Chan School of Public Health, Boston, Massachusetts; 17ICAP, New York, New York; 18Gates Foundation, Seattle, Washington; 19Social and Behavioral Health Sciences, FHI 360, Washington, DC; 20Institute of Tropical Medicine, Department of Clinical Sciences, Belgium; 21FHI 360, Zambia; 22FHI 360, Haiti; 23FHI 360, Tanzania; 24Global Health, Population and Nutrition, FHI 360, Durham, North Carolina; 25University of Texas, School of Biomedical Informatics, Houston, Texas; 26National Alliance of State & Territorial AIDS Directors, Washington, DC; 27Division of Global HIV/AIDS, Center for Global Health, CDC, Mozambique; 28Division of Global HIV/AIDS, Center for Global Health, CDC, Botswana; 29Division of Global HIV/AIDS, Center for Global Health, CDC, Namibia; 30Division of Global HIV/AIDS, Center for Global Health, CDC, Swaziland; 31Division of Global HIV/AIDS, Center for Global Health, CDC, Zimbabwe; 32Division of Global HIV/AIDS, Center for Global Health, CDC, Côte d'Ivoire; 33Division of Global HIV/AIDS, Center for Global Health, CDC, Nigeria; 34Division of Global HIV/AIDS, Center for Global Health, CDC, Vietnam; 35Division of Global HIV/AIDS, Center for Global Health, CDC, Haiti; 36Division of Global Health Protection, Center for Global Health, CDC, South Africa; 37Elizabeth Glaser Pediatric AIDS Foundation, Los Angeles, California; 38Division of Global Health Protection, Center for Global Health, CDC, Haiti; 39Massachusetts General Hospital, Boston, Massachusetts.

Corresponding author: Andrew Auld, aauld@cdc.gov, 404-639-8997.

References

  1. Office of the President of the United States. President's Emergency Plan for AIDS Relief. Updated gender strategy: December 2013. Washington, DC: Office of the President of the United States; 2015. Available at http://www.pepfar.gov/documents/organization/219117.pdf.
  2. Muula AS, Ngulube TJ, Siziya S, et al. Gender distribution of adult patients on highly active antiretroviral therapy (HAART) in Southern Africa: a systematic review. BMC Public Health 2007;7:63.
  3. Cornell M, Schomaker M, Garone DB, et al.; International Epidemiologic Databases to Evaluate AIDS Southern Africa Collaboration. Gender differences in survival among adult patients starting antiretroviral therapy in South Africa: a multicentre cohort study. PLoS Med 2012;9:e1001304.
  4. Cornell M, Myer L. Moving beyond gender stereotypes. Lancet 2013;382:506.
  5. Hawkes S, Buse K. Gender and global health: evidence, policy, and inconvenient truths. Lancet 2013;381:1783–7.
  6. Kato M, Long NH, Duong BD, et al. Enhancing the benefits of antiretroviral therapy in Vietnam: towards ending AIDS. Curr HIV/AIDS Rep 2014;11:487–95.
  7. Dinh TH, Detels R, Nguyen MA. Factors associated with declining HIV testing and failure to return for results among pregnant women in Vietnam. AIDS 2005;19:1234–6.
  8. Cohen MS, Chen YQ, McCauley M, et al. Prevention of HIV-1 infection with early antiretroviral therapy. N Engl J Med 2011;365:493–505.
  9. Lundgren JD, Babiker AG, Gordin F, et al. Initiation of antiretroviral therapy in early asymptomatic HIV Infection. N Engl J Med 2015;373:795–807.
  10. Hensen B, Taoka S, Lewis JJ, Weiss HA, Hargreaves J. Systematic review of strategies to increase men's HIV-testing in sub-Saharan Africa. AIDS 2014;28:2133–45.

* East Africa: Tanzania, Uganda; Southern Africa: Botswana, Mozambique, Namibia, Swaziland, Zambia, Zimbabwe; West Africa: Côte d'Ivoire, Nigeria; Caribbean: Haiti; Southeast Asia: Vietnam.

Additional information available at http://aidsinfo.unaids.org/.

§ Additional information available at http://www.hivpolicywatch.org/.

Additional information available at http://www.pepfar.gov/partnerships/ppp/dreams/index.htm.


Summary

What is already known on this topic?

Equitable access to antiretroviral therapy (ART) for human immunodeficiency virus (HIV)-infected men and women is a principle endorsed by most countries and funding bodies, including the U.S. President's Emergency Plan for AIDS Relief (PEPFAR).

What is added by this report?

To evaluate gender equity in ART access, 765,087 adult ART patient medical records from 12 countries were analyzed to estimate the female-to-male new ART enrollee ratio for each calendar year during 2002–2013. This annual ratio was compared with corresponding Joint United Nations Programme on HIV/AIDS (UNAIDS) estimates of adult female-to-male ratios among all persons with HIV. In all 10 African countries and Haiti, the most recent estimate of the ratio of women to men newly enrolled in ART significantly exceeded the UNAIDS estimate of the ratio of women to men among persons with HIV by 23%–83%.

What are the implications for public health practice?

Reaching more men with HIV testing and linkage-to-care services and adoption of test-and-treat ART-eligibility guidelines could reduce gender inequity in ART coverage. Government- and donor-level policy and management shifts, including endorsement of male-health–focused strategies, performance-based financing that provides incentives to reach both men and women, and gender disaggregation of HIV treatment cohort data are also needed. Prioritizing increased ART coverage among men with HIV could decrease male morbidity and mortality and reduce HIV incidence among sexual partners.


TABLE. Study designs for antiretroviral therapy (ART) cohort evaluations — 12 countries, 20022013

Region

Country

Stage 1: selection of study sites

Stage 2: selection of study patients

Assessment year

No. clinics

No. study-eligible clinics*

No. adult clinic enrollees

Estimated no. study-eligible adult ART enrollees at study-eligible clinics

Site sampling technique

No. clinics selected

Age at ART initiation (yrs)

ART enrollment years

Patient sampling technique at selected study clinics

Planned sample size*

No. eligible medical records

analyzed

Dates of data collection

East Africa

Tanzania

2007

210

85

41,920

37,728

Purposive

6

≥18

2004–2009

SRS

1,500

1,457

04–07/2010

Uganda

2007

286

114

45,946

41,351

Purposive

6

≥18

2004–2009

SRS

1,500

1,466§

04–07/2010

Southern Africa

Botswana

2014

302

176

247,856

217,082

Census

176

≥15

2002–2013

Census

217,082

217,082

10/2013

Mozambique

2014

288

170

456 055

306,335

Census

170

≥15

2004–2013

Census

306,335

306,335

04/2014

Namibia

2013

213

213

140,224

138,054

Census

213

≥15

2003–2012

Census

138,054

138,053

12/2013

Swaziland

2009

31

31

50,767

50,767

PPS

16

≥15

2004–2010

SRS

2,500

2,510

11/2011–02/2012

Zambia

2007

322

129

65,383

58,845

Purposive

6

≥18

2004–2009

SRS

1,500

1,214**

04–07/2010

Zimbabwe

2008

104

70

103,806

93,811

PPS

40

≥15

2007–2009

SRS

4,000

3,896††

01–06/2010

West Africa

Côte d'Ivoire

2007

124

78

36,943

36,110

PPS

34

≥15

2004–2007

SRS

4,000

3,682

11/2009–03/2010

Nigeria§§

2009

178

139

168,335

167,438

PPS

35

≥15

2004–2011

SRS

3,500

3,496

12/2012–08/2013

Caribbean

Haiti

2013

149

149

52,120

78,317

Census

149

≥15

2002–2013

Census

78,317

78,317

04/2014

Southeast Asia

Vietnam

2009

173

120

28,090

25,000

PPS

30

≥15

2005–2009

SRS

7,587

7,579¶¶

01–06/2010

Total

2,380

1,474

1,385,325

1,250,838

881

765,875

765,087

Abbreviations: PPS = probability-proportional-to-size; SRS = simple random sampling.

* To keep sample-based studies feasible, in Côte d'Ivoire, Nigeria, Vietnam, and Zimbabwe, only facilities with ≥50 adults on ART were eligible for sampling, whereas in Tanzania, Uganda, and Zambia only facilities that had enrolled ≥300 adults on ART were eligible.

In Tanzania, record of one patient was excluded from 1,458 sampled because of missing age data at ART initiation.

§ In Uganda, records of six patients were excluded from 1,472 sampled because of missing age data at ART initiation.

In Namibia, among those adults enrolled on ART during 2003–2012, one patient with missing gender information was excluded from analysis.

** In Zambia, 243 of 1,457 records sampled were excluded because of noncompliance with simple random sampling procedures at one site.

†† In Zimbabwe, 23 selected patients with either missing gender (n = 12) or missing outcome (n = 11) were excluded from analysis.

§§ In Nigeria, implicit stratification was used in the sampling approach.

¶¶ In Vietnam, among observations from 7,587 records sampled, four were excluded because of lack of gender information and four because of lack of outcome date.


FIGURE. Percent difference between female-to-male new antiretroviral therapy enrollee ratios and corresponding UNAIDS ratios of females to males among all persons with HIV, by country* — 12 countries, 2002–2013

The figure above is a bar chart showing the percent difference between female-to-male new antiretroviral therapy enrollee ratios and corresponding UNAIDS ratios of females to males among all persons with HIV, by country, in 12 countries during 2002-2013.

Abbreviations: AIDS = acquired immunodeficiency syndrome; HIV = human immunodeficiency virus; UNAIDS = Joint United Nations Programme on HIV/AIDS.

* East Africa: Tanzania, Uganda; Southern Africa: Botswana, Mozambique, Namibia, Swaziland, Zambia, Zimbabwe; West Africa: Côte d'Ivoire, Nigeria; Caribbean: Haiti; Southeast Asia: Vietnam.

Alternate Text: The figure above is a bar chart showing the percent difference between female-to-male new antiretroviral therapy enrollee ratios and corresponding UNAIDS ratios of females to males among all persons with HIV, by country, in 12 countries during 2002-2013.



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