The HIV epidemic remains a major global public health problem. In 2019, the number of people living with HIV (PLWH) around the world was estimated to be 38.0 million, with about 7.1 million not knowing they were living with HIV (Joint United Nations Programme on HIV/AIDS [UNAIDS], 2020). In 2019, around 1.7 million new HIV infections were reported worldwide, representing a 40% drop from the peak reached in 1998 (2.8 million) and 23% less than 2010 (2.1 million; UNAIDS, 2020). However, there is clear inequality among regions regarding HIV incidence. Among all the PLWH worldwide, 68% are from Africa, comprising 80% of affected individuals in the East and Southern Africa regions. Regarding new infections worldwide, two of three are in sub-Saharan Africa, affecting 26 million people with HIV in 2019 (UNAIDS, 2020) and making it the region with the highest burden of HIV (UNAIDS, 2019). Furthermore, HIV is the most common cause of mortality in this region (Dwyer-Lindgren et al., 2019). In 2017, sub-Saharan Africa accounted for 75% of HIV deaths worldwide, 65% of new infections, and was home to 71% of the world's PLWH.
The distribution of HIV prevalence in the 15- to 49-year-old population in this region reveals substantial differences at a local level, as well as the trend that this prevalence follows (Dwyer-Lindgren et al., 2019). Regarding the latter, a change has also been seen in the population interest group. Up until a few years ago, HIV infection in the sub-Saharan region was considered irrelevant for older adults because it was developed during youth and its complications were suffered in middle age. The current situation shows a second peak of incidence from 50 years old due to increased life expectancy resulting from the use of antiretroviral therapy and the possibility of new relationships. In this way, some authors demonstrate that an increase is expected in the incidence of HIV among the over 50s (Vollmer et al., 2017). This epidemiological change in the HIV infection implies the need for extending the segment of population that is considered of interest in this subject in the future. Moreover, the design of strategies focused on the over 50 years group will be essential. However, for the time being, the spotlight remains on the 15- to 49-year-old population.
In the analysis by gender in sub-Saharan Africa, a greater proportion of women is living with HIV. Nearly 48% of the persons diagnosed with HIV in 2019 were of the female gender; this percentage was 59% in the sub-Saharan African region (UNAIDS, 2020). Both social and biological factors contribute to the vulnerability to HIV among women, as well as the existing gender inequalities (UNAIDS, 2016a). In sub-Saharan Africa, the female population aged 15 to 24 years has twice the risk of living with HIV than the male population. Among adolescents aged 15 to 19 years old, about 83% of the new infections are in girls (UNAIDS, 2020).
The rate of new HIV infections over time offers valuable information to evaluate progress toward the reduction of the HIV transmission. Data regarding the number of people newly infected by HIV are essential to analyze epidemic trends and dynamics of viral transmission. This is an indicator related to the World Health Organization (WHO) Sustainable Development Goal 3, which includes the aim of ending the AIDS epidemic by 2030 (WHO, 2019). Additionally, the rate of new HIV infections is an indicator of the Global Strategy for Women's, Children's and Adolescents' Health (2016-2030; WHO, 2015). Applying standardized methodologies to determine the HIV incidence rate trends among women in sub-Saharan Africa may offer data to analyze the problem in greater depth. However, to date, no studies have examined this aspect using standardized methodologies. Therefore, the aim of our study was to use official data to analyze the trends in the HIV incidence rate among women in sub-Saharan African countries between the years 2000 and 2017.
Methods
Data regarding new HIV infections in sub-Saharan Africa for the 2000 to 2017 period were obtained from the United Nations Statistics Division database (2019). This period is the range of years included in the database. The mission of the United Nations Statistics Division is to "compile and disseminate global statistical information, develop standards and norms for statistical activities, and support countries' efforts to strengthen their national statistical systems" (United Nations Statistical Commission, 2020, p. 3). The database is publicly available and was updated on October 4, 2019. The HIV incidence rate is defined by the WHO as the number of new HIV infections per 1,000 uninfected population, aged 15 to 49 years old. This is the number of new cases per population at risk in a given period and is referred to as the incidence rate.
The study population comprised 45 countries of sub-Saharan Africa, regrouped into four geographical regions: West Africa (Benin, Burkina Faso, Cape Verde, Ivory Coast, Gambia, Ghana, Guinea, Guinea-Bissau, Liberia, Mali, Niger, Senegal, Sierra Leone, Togo, and Mauritania), Central Africa (Angola, Cameroon, Central African Republic, Chad, Congo, Democratic Republic of Congo, Equatorial Guinea, and Gabon), East Africa (Ethiopia, Eritrea, Djibouti, Somalia, Madagascar, Comoros, Uganda, Rwanda, Burundi, Kenya, Tanzania, Sudan, South Sudan, Mozambique, Malawi, Zambia, and Zimbabwe), and Southern Africa (Botswana, Lesotho, Namibia, Eswatini [previously Swaziland], and South Africa).
We used the joinpoint regression analysis as the statistical method to analyze significant changes in HIV incidence rate trends. This method of nonlinear regression model identifies turning points called "joinpoints" where significant changes in the linear trend occur. The zero joinpoint represents a straight line and tests for model fit with a maximum of four joinpoints. Tests of significance use a Monte Carlo permutation method (Kim et al., 2000). Joinpoint regression was applied to identify periods when there were significant changes in the HIV incidence rate, along with the corresponding annual percentage changes (APCs). We calculated the corresponding 95% confidence intervals (95% CIs) to describe the magnitude of change in each of the trends. In this model, the HIV incidence rate was the dependent variable, and the year was the independent variable. In addition, the average annual percent changes (AAPC) were calculated to describe the average APC over the 2000 to 2017 interval. In all analyses, values of p < .05 were considered statistically significant. All the analyses were carried out using joinpoint regression software (version 4.6.0.0), developed by the National Cancer Institute, USA.
Results
During the study period, the highest HIV incidence rate among women in sub-Saharan Africa was in 2000 (8.24 per 1,000), and the lowest HIV incidence rate was recorded in 2017 (3.39 per 1,000). Between 2000 and 2017, there was a global decrease trend (APC = -5.0%; 95% CI: -5.3 to -4.8), with three identifiable joinpoints. The HIV incidence rate sharply decreased between 2000 and 2003 (APC = -8.1%; 95% CI: -8.8 to -7.4). In the following two periods (2003-2010 and 2010-2014), the incidence rate also demonstrated a significant downward trend, although less pronounced (APC = -2.8%; 95% CI: -3.1 to -2.5 and APC = -4.1%; 95% CI: -5.0 to -3.2). Finally, in the last few years (2014-2017), HIV incidence rates again demonstrated a significant downward trend (APC = -8.1%; 95% CI: -9.1 to -7.2; Figure 1).
Analysis of New HIV Infections by Region
The highest HIV incidence rate in Southern Africa, East Africa, and Central Africa was in 2000 (43.68, 23.31, and 8.85, per 1,000, respectively), whereas in West Africa it was in 2003 (6.47 per 1,000). However, in all the regions, the lowest HIV incidence rate was in 2017 (East Africa: 0.02 per 1,000; West Africa: 0.05 per 1,000; Central Africa: 0.37 per 1,000; Southern Africa: 6.96 per 1,000; Figure 2).
Thus, in the period from 2000 to 2017, the four regions of sub-Saharan Africa showed a significant downward trend. The most pronounced decreases were in West Africa (AAPC = -6.6%; 95% CI: -9.3 to -3.8) and East Africa (AAPC = -5.8; 95% CI: -6.2 to -5.3; Table 1). Furthermore, two regions exhibited significant AAPC during the study period (i.e., Central Africa and East Africa), with fluctuating trends observed in both, as shown in Table 1. The other two regions did not present identifiable joinpoints between 2000 and 2017.
Analysis of New HIV Infections by Country
Among sub-Saharan African countries, the highest HIV incidence rates were observed in Eswatini (previously Swaziland; 43.68 per 1,000), Lesotho (41.60 per 1,000), and Botswana (37.24 per 1,000) in 2000. Conversely, the lowest HIV incidence rates were observed in Comoros, Somalia, Mauritania, and Madagascar, with an HIV incidence rate <0.1 per 1,000 in many years of the study period (Table 2).
The results of the regression analysis of joinpoints, the APC for each trend, and the AAPC for all the countries being studied are shown in Table 2. Over the past two decades, HIV incidence rates have decreased in all sub-Saharan African countries, except in Angola, Equatorial Guinea, and Sudan, which have remained the same, and Madagascar, where the overall trend is increasing (AAPC = 2.2; 95% CI: 0.6-3.8). The major decreases were in Mauritania (AAPC = -14.1; 95% CI: -15.5 to -12.7), Ethiopia (AAPC = -12.7; 95% CI: -14.5 to -10.9), Somalia (AAPC = -11.6; 95% CI: -12.7 to -10.6), Democratic Republic of Congo (AAPC = -11.4; 95% CI: -12.1 to -10.8), and Senegal (AAPC = -11.3; 95% CI: -12.4 to -10.1). However, the smallest decreases were in Congo (AAPC = -0.3; 95% CI: -0.5 to -0.0), Mali (AAPC = -2.8; 95% CI: -3.3 to -2.22), Guinea (AAPC = -3.1; 95% CI: -3.6 to -2.5), Burkina Faso (AAPC = -3.4; 95% CI: -4.2 to -2.7), and Central African Republic (AAPC = -3.5, 95% CI: -4 to -3).
Among the 41 countries that present a significant drop in the HIV incidence rate, seven demonstrate significant downward and upward trends over the study period. These countries are Burkina Faso, Burundi, Central African Republic, Djibouti, Eritrea, Eswatini, and Uganda. However, the number of trends differs from country to country. We can also find different downward and upward trends in Angola, Equatorial Guinea, Madagascar, and Sudan, although overall their HIV incidence rate has not dropped, as previously mentioned. In eight countries (Botswana, Cape Verde, Ivory Coast, Ethiopia, Gambia, Guinea-Bissau, Mozambique, and Sierra Leone), significant downward HIV incidence rate trends were detected, along with periods when the HIV incidence rate does not change at all significantly. Finally, in the remaining countries (a total of 27), the different trends encountered always involved a significant drop in the HIV incidence rate, as shown in Table 2.
Discussion
Our findings show a clear downward trend in the HIV incidence rate among women in sub-Saharan African countries over the past two decades. This decrease is also documented in the four geographical regions of sub-Saharan Africa and in the 45 countries being analyzed, with the exception of Angola, Equatorial Guinea, and Sudan, which do not show any change, and Madagascar, which shows an increase in incidence.
Many factors may have contributed to this general decline, including widespread antiretroviral therapy coverage (Birdthistle et al., 2019; Fettig et al., 2014; Ghosn et al., 2018; Kagaayi & Serwadda, 2016; Kharsany & Karim, 2016; Williams et al., 2015), which was promoted by WHO's "3 by 5" Initiative, aimed at increasing the number of people receiving this therapy up to 3 million by the end of 2005 (WHO, 2008). Other factors are increased adoption of safer sexual behaviors, including voluntary male medical circumcision (Birdthistle et al., 2019; Davis et al., 2021; Fettig et al., 2014), more prevention programs regarding mother-to-child transmission (Birdthistle et al., 2019; Ghosn et al., 2018), and identification of high-risk populations (Fettig et al., 2014). UNAIDS, with its 90-90-90 strategy, gave a significant impulse to the expansion of coverage for access to antiretroviral therapy in sub-Saharan Africa. By 2016, 50% of PLWH were receiving antiretroviral treatment (Ghosn et al., 2018). More than 10 million men and adolescents in sub-Saharan Africa have participated in voluntary medical male circumcision programs for HIV prevention. Randomized controlled trials have shown that voluntary medical male circumcision reduces the risk of contracting HIV by approximately 60% (UNAIDS, 2015).
However, despite this remarkable progress in reducing HIV incidence, rates remain high among women in sub-Saharan African countries. The causes that contribute to sub-Saharan women's vulnerability to HIV are complex and multifactorial and can be grouped into behavioral, biological, and structural risk factors. Behavioral factors include intergenerational partners, multiple concurrent partners, less ability to negotiate safer sex, commercial or transactional sex (Harrison et al., 2015; UNAIDS, 2016b), early sexual debut, and HIV knowledge deficits (McKinnon & Karim, 2016; UNAIDS, 2016a, 2016b). The most important known biological factors are female sensitivity to acquiring HIV due to cervical ectopy (Harrison et al., 2015; McKinnon & Karim, 2016) and an immature cervix (UNAIDS, 2016b). However, women with HIV are more likely to develop precancerous lesions if they contract the human papillomavirus because cervical cancer is the primary cause of death by cancer for sub-Saharan women. In fact, there is a high prevalence of precancerous cervical lesions among women who are living with HIV (UNAIDS, 2016a).
The most important structural factor is gender inequality, which implies the existence of social isolation, poverty, discriminatory cultural norms, orphanhood, inadequate schooling, and gender-based violence (Harrison et al., 2015; UNAIDS, 2016b). Analysis of gender inequality in HIV prevalence in sub-Saharan Africa, developed by Sia et al. (2016), suggests that it is caused by differences in the effects of risk factors between men and women; these risk factors include sociodemographic characteristics, sexual behaviors, and HIV awareness. These authors conclude that these gender inequalities have been sustained over time, explaining that, despite the downward trend in the HIV incidence rate among women in sub-Saharan countries, the figures are still very high.
An additional factor increasing the vulnerability to HIV among women is gender-based violence and sexual attacks. In some areas, the experience of physical or sexual intimate partner violence by women increases their risk of HIV infection by 1.5 times (UNAIDS, 2020). The available data show that in countries such as South Africa, Uganda, and the United Republic of Tanzania, nearly 30% women have experienced sexual and/or physical violence from an intimate partner in the last year; around 25% in Kenya, Angola, and Zambia; and more than 20% in Malawi, Rwanda, Ethiopia, Namibia, and Zimbabwe (UNAIDS, 2019). Formal education also influences the incidence of HIV, due to knowledge of the risk of HIV transmission and even due to lack of information or the existence of false beliefs (Baranczuk et al., 2019), situations that can increase sexual behavior and infection risks. In their analysis of 29 sub-Saharan African countries, Baranczuk et al. (2019) conclude that literate women usually begin their sexual relations later and also believe that they are justified to ask their husband to use a condom if he has a sexually transmitted infection (Baranczuk et al., 2019). The downward trend in the HIV incidence rate among women shown by the results of this study is consistent with the fact that the overall proportion of literacy in sub-Saharan Africa is gradually increasing and will continue to increase, particularly among the younger population (Baranczuk et al., 2019).
There are important differences among sub-Saharan Africa regions regarding epidemiological patterns associated with HIV incidence rates. In the results, the Central Africa and Southern Africa regions have shown the least decline in HIV incidence rate trends among women. In the case of Southern Africa, this could be explained by a combination of several types of behaviors that remain among populations, such as low rates of male circumcision, sexual risk behaviors like multiple concurrent partners and intergenerational sex, and migration patterns (Fettig et al., 2014). Regarding Central Africa, the 2019 report from UNAIDS underlines the vulnerable situation of young women in the West and Central African region (UNAIDS, 2019). This report reveals that in this region, almost 160 women aged 15 to 24 years become infected with HIV every day. As potential causes of this situation, it is worth mentioning a lack of comprehensive programs for prevention of HIV infections and sexual and reproductive health services exists in most countries in the region. Furthermore, many of these countries are experiencing conflict situations, insecurity, and humanitarian crises (UNAIDS, 2019).
Regarding the trends seen between 2000 and 2017, there is remarkable heterogeneity among the regions, although a pattern is emerging, with greater increases in the coastal regions in the south of sub-Saharan Africa and the greatest decreases in the belt between Botswana and Kenya and in the Central African Republic (Dwyer-Lindgren et al., 2019). The low rates of HIV in the Comoros Islands over the years of study can be explained because it was considered to be protected by several factors: island status, Muslim culture, and near-universal male circumcision (Dada et al., 2007). This situation might be similar to Madagascar. However, in this case, although Madagascar has one of the lowest rates of new HIV infections in all of sub-Saharan Africa, paradoxically a slight upward trend has been observed over the past 12 years. This could be due to the political crisis in 2009 following a government coup, which had a major impact on health sector resources (Barmania, 2015), or due to the differences in antiretroviral therapy cover (UNAIDS, 2019). In addition, Valles (2018) points to commercial sex as another important factor in this growing trend of new HIV infections because it is a common practice in the culture of Madagascar and is on the rise due to the economic crisis of recent years.
In addition, the data show that there are three countries, Angola, Equatorial Guinea, and Sudan, that do not report a significant reduction in HIV incidence rate, although they do show a downward trend from 2006 in Sudan and from 2012 in Angola and Equatorial Guinea. In the case of the latter two, the downward trend in the last few years might be the consequence of national programs implemented to prevent and treat HIV (Chrystelle et al., 2005; UNAIDS, 2014). The case of the Sudan is different, as a clear drop can be detected from the end of the civil war, when the Sudan People's Liberation Army HIV/AIDS Secretariat, which coordinates, plans, implements, and monitors HIV and AIDS programs, was set up in 2006 (Courtney et al., 2017).
To further reduce HIV infection among women in sub-Saharan Africa, public health programs must be focused on and addressed with gender inequalities in this vulnerable group. It is essential to develop interventions to empower African women against the HIV epidemic. Measures such as increasing education achievements and eliminating gender-based violence and sexual coercion are the main focus points for health policies. To this end, the male population plays a key role through greater involvement in diagnostic testing, increased awareness of safer sex, and greater adherence to antiretroviral treatment.
Some limitations of this study should be discussed. The diagnostic tests and publications on HIV trends in Africa have increased over the last few years. However, HIV is an infra-diagnosed disease, particularly in Africa, and could suffer from a higher chance of underreporting. In fact, it is estimated that in 2019, 7.1 million people did not know that they were living with HIV (UNAIDS, 2020). Accordingly, data on HIV incidence rate in Africa could not reflect actual figures because a proportion of the population with HIV could not have not been diagnosed.
Conclusions
This is the first study that examines HIV incidence rate trends among women in sub-Saharan Africa using standardized methodologies, showing a clear downward trend during the 2000 to 2017 period in most countries. Despite this decrease, the HIV incidence rates among young women are particularly high. Significant differences were detected in HIV incidence rate trends in the different regions of sub-Saharan Africa and among the 41 countries being analyzed. In 27 of them, the HIV incidence rate decreased significantly over the analyzed period. The use of the joinpoint regression statistical method to analyze significant changes in HIV incidence rate trends, the APC, and AAPC is a good approach to in-depth analysis of the incidence of HIV among women in sub-Saharan Africa.
Key Considerations
* Despite the decreasing trend of the HIV incidence rate during the 2000 to 2017 period observed in the results of this study, incidence rates among young women are particularly high in sub-Saharan Africa.
* The findings of this article highlight the vulnerability to HIV among women in sub-Saharan Africa, particularly in the region of Southern Africa and in countries such as Angola, Equatorial Guinea, Sudan, and Madagascar, where the decline of the HIV incidence rate has been limited during the 2000 to 2017 period.
* Public health policies and interventions should focus on palliating the multiple factors affecting this vulnerable group, especially in those countries where there is not a downward trend of the HIV incidence rate.
Disclosures
The authors report no real or perceived vested interests related to this article that could be construed as a conflict of interest.
Author Contributions
N. Soto-Ruiz and P. Escalada-Hernandez were responsible for supervision, validation, and writing of the original draft, as well as reviewing and editing the writing. A. Arregui-Azagra and L. San Martin-Rodriguez were responsible for conceptualization, formal analysis, and writing of the original draft, as well as reviewing and editing the writing. I. Elizalde-Beiras and A. Saralegui-Gainza were responsible for writing the original draft, as well as reviewing and editing the writing.
References