Contraceptive Use and Uptake of HIV-Testing among Sub-Saharan African Women

Despite improved availability of simple, relatively inexpensive, and highly effective antiretroviral treatment for HIV/AIDS, the disease remains a major public health challenge for women in sub-Saharan Africa (SSA). Given the numerous barriers in access to care for women in this region, every health issue that brings them into contact with the health system should be optimized as an opportunity to integrate HIV/AIDS prevention. Because most non-condom forms of modern contraception require a clinical appointment for use, contraception appointments could provide a confidential opportunity for access to HIV counseling, testing, and referral to care. This study sought to investigate the relationship between contraceptive methods and HIV testing among women in SSA. Data from the Demographic and Health Survey from four African countries—Congo, Mozambique, Nigeria, and Uganda—was used to examine whether modern (e.g., pills, condom) or traditional (e.g., periodic abstinence, withdrawal) forms of contraception were associated with uptake of HIV testing. Data for the current analyses were restricted to 35,748 women with complete information on the variables of interest. Chi-square tests and logistic regression models were used to assess the relationship between uptake of HIV testing and respondents' baseline characteristics and contraceptive methods. In the total sample and in Mozambique, women who used modern forms of contraception were more likely to be tested for HIV compared to those who did not use contraception. This positive association was not demonstrated in Congo, Nigeria, or Uganda. That many women who access modern contraception are not tested for HIV in high HIV burden areas highlights a missed opportunity to deliver an important intervention to promote maternal and child health. Given the increasing popularity of hormonal contraception methods in low-income countries, there is an urgent need to integrate HIV counseling, testing, and treatment into family planning programs. Women on hormonal contraceptives should be encouraged to continue to use condoms for HIV-prevention.


Introduction
In 2013, 35 million people worldwide were living with HIV, of which 2.1 million had become newly infected [1]. Roughly 70% of the world's HIV positive individuals-25 million peoplereside in sub-Saharan Africa (SSA) [1,2]. The epidemic has had widespread effects, including putting increased pressure on healthcare facilities to diagnose and treat HIV. Women in SSA are disproportionately infected with HIV via heterosexual contact during their reproductive years [2].
Finding ways to mitigate the HIV epidemic has long been a goal of researchers and world leaders alike. Abstinence and condom use are two of the three endorsed behavioral strategies recommended by HIV prevention programs, emphasizing the ABC approach to HIV reduction-i.e. abstinence, be faithful, and condom use programs. There is little doubt that condom use and abstinence provide proven prevention options in reducing HIV transmission [3,4]; however, it has become increasingly apparent that the ABC approach over simplifies the complex nature of the HIV epidemic [5][6][7].
Although SSA has one of the lowest rates of contraceptive use globally [8], the use of modern forms of contraception (e.g., pills, IUD, condom, diaphragm) in this region has changed only minimally from 2008-2014 (23.6% vs. 27.6%) [9,10]. An estimated 19.7% of married or unionized women use modern contraceptive methods compared to 5.4% who use traditional methods [8]. Currently, injectable contraception is the most prevalent form of contraception used across SSA [11,12].
Apart from condoms, no other form of contraception has been found to protect against sexually transmitted infections, including HIV. Both the World Health Organization (WHO) and the United States Agency for International Development (USAID) have acknowledged the unclear relationship between the use of hormonal contraceptives and HIV acquisition [13]. Not only are non-condom contraceptives ineffective in protecting against sexually transmitted infections in general, but hormonal contraceptives specifically have also been implicated in higher rates of HIV infection. In Asia, female sex workers were more likely to be HIV positive if they took oral contraceptives (OC) compared to female sex workers who did not take OC [13][14][15]. A meta-analysis exploring the relationship OC among African women and HIV infection found a 45% increase in seroprevalent or seroincident HIV cases among women who were using oral contraceptives (OR 1.45: 95% CI 1.15-1.83) [16]. In contrast, a different meta-analysis in SSA did not find OC to be related to risk in HIV infection [17]. Thus, the WHO and USAID advocate the use of dual contraception, which includes using both a highly effective contraception-e.g. an injectable hormonal contraception-to help prevent pregnancy and condoms to prevent the transmission of sexually transmitted infection [13,15]. However, fear of unintended pregnancy-not necessarily fear of HIV-promotes condom use [18].
Because more women in SSA are using non-condom methods of contraception, it is even more important that they understand the importance of HIV testing [2,19]. Thus, it is essential to understand the effects that contraceptive use has on the uptake of HIV testing in high HIV transmission areas of SSA. The objective achieved in this study was to examine how modern and traditional forms of contraception were associated with uptake of HIV testing. The knowledge gained from this study can aid policy makers in targeting HIV education and testing to women in SSA.  [20]. Data for the current analyses were restricted to women with complete information on the variables of interest.

Measures
Comprehensive knowledge of HIV was created using UNICEF's definition [21]. Women were classified as having comprehensive HIV knowledge if they correctly: 1) acknowledged that a healthy-looking person can have HIV; 2) identified two methods of preventing sexual transmission of HIV; and 3) rejected two common misconceptions about HIV transmission-HIV can be contracted from mosquito bites; or HIV can be contracted by sharing food with someone living with AIDS. Respondents' religion was classified into the following categories: Catholic, Muslim, Christian-other (any denomination excluding Catholicism), and Other/No religion. For these analyses, contraception was classified as either: modern contraception which describes hormonal (pills, injectables, IUDs, and implants), sterilization (both female and male), or barrier contraception (condom or diaphragm); or traditional which includes periodic abstinence, withdrawal, and other country specific forms of contraception. HIV stigma was measured as respondents answering 'No' to any of the following items: Willing to care for a relative with HIV; A female teacher infected with HIV, but is not sick, should continue teaching; I would buy vegetables from a vendor with HIV [22].

Statistical Analysis
For our analysis, only individual DHS data was used. Due to oversampling of certain populations, individual weights were used as recommended by DHS to adjust for nonresponse to questions and to make the data more representative on a national level [23]. Chi-square tests and logistic regression models were used to assess the relationship between uptake of HIV testing and respondents' baseline characteristics and contraceptive methods. Because condoms are the only form of contraception known to decrease the spread of HIV, a sensitivity analysis was conducted by reanalyzing the relationship between HIV testing and contraceptive use in both the crude and adjusted logistic regression models, excluding women who reported using condoms. Statistical significance was set at p< 0.01 for all models, and data analyses were done using the 'PROC SURVEY' command. All data cleaning and analyses were conducted using SAS 9.4 (Cary, North Carolina).
DHS surveys were conducted under the scientific and administrative oversight of the local country, including ethical review by the corresponding local ethics review board. Data collection procedures were also approved by the ORC Macro institutional review board. In addition, this secondary data-analysis was evaluated by the Mel and Enid Zuckerman College of Public Health Research Office at the University of Arizona, and was considered exempt from human subjects review.

Results
Of the 35,748 women included in the analyses, 15.7% were Congolese, 37.5% were Mozambicans, 22.6% were Nigerians, and 24.2% were Ugandans. Table 1 shows the weighted results of the participant characteristics at an aggregate level and by country. In the pooled and individual country analysis, women aged 20-29 represented  Table 2 shows the relationship between uptake of HIV testing and respondents' baseline characteristics and contraceptive methods. All Chi-square tests regarding the relationship between HIV testing and participants' sociodemographic, HIV knowledge or contraceptive use were statistically significant (p<0.01) with the exceptions of difficulty accessing a healthcare facility in Congo (p = 0.07) and Uganda (p = 0.91); religion in Uganda (p = 0.58); and contraception use in Nigeria (p = 0.47). Table 3 shows the crude and adjusted logistic regression models for the relationship between HIV testing and contraceptive use. In the total sample and in Mozambique, women who used modern forms of contraception had higher odds of being tested for HIV compared to those who did not use contraception (adjusted odds ratio [aOR] = 1.31, 95%CI: 1.16-1.48 and aOR = 2.30, CI: 1.82-2.91, respectively). In Congo, a decrease in the odds of having an HIV test was demonstrated among those who used traditional contraception compared to those who did not use any form of contraception (aOR = 0.68, CI: 0.52-0.94). No other associations between contraception use and HIV testing were demonstrated. Sensitivity analysis excluding women who use condoms did not change the results of these models (Table 4).

Discussion
Understanding the relationship between HIV testing and use of contraception in high HIV transmission areas, such as SSA, is essential to decreasing the burden of HIV, especially as the prevalence of modern contraceptive use increases. This study sought to add to the literature by describing the relationship between contraception method and HIV testing in SSA. In the total sample, women who used modern forms of contraception were more likely to be tested for HIV compared to those who did not use contraception. Individual country results varied. Women in Mozambique demonstrated an increase in the odds of being tested for HIV if they were using modern forms of contraception compared to those who did not use any form of contraception. This positive association was not demonstrated in Congo, Nigeria, or Uganda. Only women in Congo demonstrated a decrease in the odds of being tested for HIV if they used traditional forms of contraception compared to those who used no contraception. Previous studies have demonstrated that in SSA 27.6% of women used modern forms of contraception [10], which is very similar to the results of the overall sample in this study (26.4%). In Mozambique, women who used modern forms of contraception had an increase in the odds of being tested for HIV. However, extremely low rates of modern contraception use were demonstrated in Mozambique (12.1%) possibly because over 50% of women reported difficulty accessing a healthcare facility. This is particularly concerning as Mozambique is a country with one of the highest prevalence rates of HIV at 11% [24]. Therefore, although women who use modern forms of contraception had higher odds of HIV testing in Mozambique, a low proportion of the overall population fell into this group. Women in SSA-and especially those in Mozambique-may benefit from services that provide both education about, and access to, modern forms of contraception and HIV testing. Many factors decrease the uptake of HIV testing in SSA, including fear of receiving a positive HIV test result and HIV-stigma [25]. With increased access to HIV testing and counseling, the 2014 United Nations Gap Report now estimates that 48% of people know their HIV status, of which 86% of HIV positive individuals are receiving antiretroviral therapy and over three in four (76%) have achieved viral suppression [24]. However, percentages of HIV testing uptake vary greatly among SSA countries. For instance, the proportion of women tested for HIV was 50% more in Mozambique than in Congo in 2011 (33.3% total population vs. 22.5%, respectively). Uganda had the highest HIV testing rates in this study. HIV testing in Uganda also remained high as gravidity increased; in Congo, Mozambique, and Nigeria, HIV testing fluctuated as gravidity increased. Overall, uptake of HIV testing in Congo, Mozambique and Nigeria was relatively low. This data did show a substantial increase in HIV testing in each country as women who had children, compared to those who were nulliparous. Of the women who had obtained an HIV test, most received it from a government run hospital or health center: Congo (84%), Mozambique (92%), Nigeria (69%), and Uganda (68%) (results not shown). It is assumed that most of these women are partaking in HIV testing as part of antenatal care.
Because some non-condom forms of modern contraception require a clinical appointment for use, contraception appointments could provide a confidential place for access to HIV testing, education and treatment. Because of the continued fear of receiving a positive HIV test result and the associated HIV-stigma [26], providing both testing and counseling at family planning clinics may be ideal. Use of traditional forms of contraception was relatively high in Congo and Nigeria (41.8% and 22.5%, respectively). Previous studies have demonstrated that women often rely on traditional methods of birth control or abortion due to lack of knowledge about modern forms of contraception, fear of infertility, access barriers, lack of control in fertility decision making, and the association of birth control methods-especially condom use with promiscuity [27][28][29]. Finding ways to decrease the barriers associated with utilizing modern forms of contraception remain imperative to decreasing HIV.

Strengths and limitations
Most previous research on this topic has assessed the effects of HIV-testing on subsequent use of contraception, particularly condoms; however, this study compared the type of contraception used (modern and traditional) and the uptake of HIV-testing. A sensitivity analysis was also conducted to explore the relationship that non-condom forms of contraception have on HIV testing. By doing this, we can gain insight to the beliefs associated with HIV risk and contraception use. This paper is not without limitations. Although we found an association between contraceptive-use by type and HIV-testing, we cannot infer a causal relationship between contraceptive use and HIV-testing. To be precise, this present study cannot depict that using a certain form of contraceptive always results in HIV-testing. In addition, this analysis used data collected across a span of two years, from 2011 to 2013. Therefore, this study acknowledges the limited ability to conduct cross-country comparisons across different time periods.

Implications for Policy
As modern forms of contraception are introduced, healthcare providers-as well as their patients-need to be provided with fact based resources that explain what is known about the relationship between HIV acquisition and modern forms of contraception. Because the relationship between contraception utilization and subsequent HIV infection remains unclear, healthcare providers should continue to emphasize using condoms to prevent HIV acquisition. Integrating HIV education and testing into medical appointments that provide access to contraception may increase uptake of HIV testing in women who would otherwise not attend a clinic for testing. Because this study did not demonstrate a homogenous association between types of contraception and HIV testing between individual countries, there appears to be many missed opportunities for women to gain access to HIV testing. Also, providing modern forms of contraception to women in all areas of SSA could reduce vertical transmission of HIV, the number one reason for pediatric HIV infection, as contraception provides a woman the ability to plan for a future family. In Congo, women most commonly first received their current contraception from a friend or relative (42%), and in Mozambique from a health center (54%). In Nigeria and Uganda women most frequently gained access to contraceptives via the pharmacy (33%) and a private hospital or clinic (35%), respectively (results not shown). Because contraception use is often closely tied to a woman's financial resources and education-with wealthier and more educated women displaying higher rates of contraception use-providing contraception free of charge or at a low-cost is more likely to promote use among those with the greatest unmet need [30,31].

Future Directions
Very little information has been published on the relationship between a woman's method of contraception and their uptake of HIV-testing. Although condom use is the only form of contraception shown to reduce HIV transmission, inje contraception is currently the most prevalent form of contraception across SSA. Furthermore, the unclear relationship between hormonal contraceptives and HIV infection mean that women using modern contraceptionbut not condoms-may be at higher risk of HIV-transmission. Future studies that explore the relationship between modern-non-condom-forms of contraption and HIV are needed. Furthermore, studies that assess women's perceptions of HIV risk while using modern forms of contraception are needed to understand if women utilizing modern forms of contraception understand their HIV risk and need for HIV testing.

Conclusions
In this study, our pooled results demonstrated that women who used modern forms of contraception were more likely to be tested for HIV compared to those who did not use contraception. This result was true both with and without condom users in the sample. Given the increasing popularity of hormonal contraception methods, efforts should be directed at educating women about the importance of continuing to use condoms for HIV-prevention. Continued community education about HIV and the importance of knowing one's status is also needed.