Year : 2010 | Volume
: 2 | Issue : 1 | Page : 15--27
Looking at complicating non-biological issues in women with HIV
Chaturaka Rodrigo1, Senaka Rajapakse2,
1 University Medical Unit, National Hospital of Sri Lanka, Sri Lanka
2 Department of Clinical Medicine, Faculty of Medicine, University of Colombo, Sri Lanka
University Medical Unit, National Hospital of Sri Lanka
Introduction: The increasing number of women acquiring Human Immunodeficiency Virus (HIV) has resulted in a «SQ»feminization«SQ» of the epidemic. In this article we are reviewing whether females are disadvantaged in the epidemic, due to factors independent of the biological differences in sexes. Materials and Methods: We searched MEDLINE and EMBASE for articles with key words «SQ»Women«SQ», «SQ»Gender,«SQ» and «SQ»HIV«SQ» in any field. The search was restricted to articles published in English within the last 10 years (1999-2009). Data were coded independently by two reviewers from 94 selected sources. The coded data were categorized under five commonly encountered concepts; violence, poverty, gender norms, prevention-/treatment-related issues, and Highly Active Anti-Retroviral Treatment (HAART). Results: The link between inter-partner violence (IPV) and HIV risk for women is observed by many authors. In assessing the link between poverty and HIV, indicators such as food insufficiency and income inequality may be better indicators compared to wealth itself. Although women are disadvantaged with male-dominated gender norms, evidence suggests that the traditional norms are changing in many societies. A positive association between living in urban communities, education, and better HIV knowledge has been observed in females, although it is not always synonymous with reduced risk behavior. Conclusions: Women are still disadvantaged in many HIV-related issues such as poverty, violence, and gender norms. At least in Africa, there is evidence of a positive change in spheres of education and gender norms. However, the situation in Asia is largely unexplored.
|How to cite this article:|
Rodrigo C, Rajapakse S. Looking at complicating non-biological issues in women with HIV.J Global Infect Dis 2010;2:15-27
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Rodrigo C, Rajapakse S. Looking at complicating non-biological issues in women with HIV. J Global Infect Dis [serial online] 2010 [cited 2021 Jan 23 ];2:15-27
Available from: https://www.jgid.org/text.asp?2010/2/1/15/59246
The latest estimates of the HIV (Human Immunodeficiency Virus) epidemic suggest that 33 million people live with it worldwide. Fifty percent of them are women.  However, in 1985, only 35% of the infected were women.  The main mode of transmission has shifted from male homosexual contact to heterosexual contact over the last 20 years. More women getting infected via heterosexual intercourse has resulted in 'feminization of HIV/AIDS'.  The percentage of infected women varies in different regions, but the numbers are increasing (Sub-Saharan Africa = 60%, Caribbean = 45-50%, Asia and Latin America = 30-40%, Eastern Europe and Central Asia = 30%).  This changing face of the epidemic calls for a careful review of gender-related differences of HIV.
An analysis of sexual behavior in 59 countries has shown that in many developing countries the age of sexual initiation has risen for women. Still, due to the late age in marriage, the prevalence of premarital sex has increased.  This and other trends in sexual behavior are dependent on local factors such as poverty, culture, gender norms, media influence, and so on. Transmission of HIV and other sexually transmitted diseases (STDs) are also influenced by these issues, which may affect men and women differently. Identifying these factors and their gendered effects will have major implications in prevention strategies.
During the synthesis of our review, it seemed logical to broadly categorize the gender-related variables as biological and nonbiological. The clinical manifestations, differences in pathogenesis, pregnancy-related issues, response to HAART, and side effects are some biological issues. As the scope of the topic is vast, we restricted our review to examine only the nonbiological factors, with gender implications, and how they relate to women at risk and women living with HIV/AIDS.
Materials and Methods
We searched the electronic databases; MEDLINE and EMBASE with the keywords 'Women' 'Gender,' and 'HIV' in any f ield, using the software Endnote X1.01, to the filter articles. The search was limited to articles published in English over the last 10 years (1999-2009). Bibliographies of cited literature were also searched. Relevant publications and epidemiological data were also downloaded from websites of international agencies such as the World Bank, United Nations Joint Program on HIV/AIDS (UNAIDS), and World Health Organization (WHO). All abstracts were read independently by the two authors, and relevant articles were identified for review of the full articles.
Sources were screened for relevance to the topic, originality, a well-described methodology, rigor of statistical analysis, and an adequate sample size, where relevant. Sources were excluded where sample size was inadequate (except in qualitative studies), methodology was not well-described, statistical analysis was unclear, and where the full article was unavailable. Ninety four sources from a selected 115 (81.7%) were reviewed. Coding was done by two reviewers independently blinded to each other. Codes were grouped into concepts commonly encountered (e.g., gender norms, violence, poverty, treatment- and prevention-related issues) during the search, under the broader category of nonbiological factors. Data sources included reviews published in core clinical journals, cohort studies, qualitative studies, interventional studies, case-control studies, cross-sectional analysis, and epidemiological data. The inter-reviewer agreement for data included in the final synthesis was 100%. A summary of cited literature is shown in [Table 1],[Table 2],[Table 3].
Violence against women can occur in different settings including civil wars, communal disputes, and domestic violence. , The gender based violence (GBV) defined in this article includes all forms of physical, sexual, and emotional abuse against women. A cross-sectional survey in eight African countries revealed that 18% of the women had experienced GBV within one year.  Another multicenter study in ten countries (n-24,097) reported the lifetime risk of inter-partner violence (IPV) to be in the range of 15-71%, indicating a wide range of variation in communities. 
It is established that HIV is more likely to be transmitted in an act of forced penetration rather than during voluntary sex, due to factors such as inability to negotiate on safer sex and breach of epithelial barriers (with trauma) making it easier for the virus to enter the blood stream.  Forced sex increases the woman's chances of contracting a sexually transmitted disease (STD) four-fold. 
Violence makes women vulnerable to HIV
A population-based survey in Tanzania concluded that women had a significantly higher risk of HIV [Odds ratio(OR)-2.0] if they had experienced coerced sex before 18 years of age.  Fonck et al.  reports a two-fold higher risk of lifetime intimate partner violence for HIV positive women. A cross-sectional survey by Dunkle et al.  in South Africa has shown that intimate partner violence (OR-1.48) and high level of male control in a relationship (OR-1.52) was associated with HIV infection.
However, Jewkes et al.  has shown that while IPV is strongly associated with many HIV risk factors, it was not directly or significantly correlated with HIV positivity when corrected for other risk behaviors. A similar conclusion of an indirect relationship between IPV and HIV is suggested by Pettifor et al. and Langen et al. , This difference can be partly explained by the sample selection (general population vs. at-risk population). Many risk factors having a direct association with HIV, such as, age gap between the partners, frequency of intercourse, and number of sexual partners in the past year can be linked to IPV as well. In fact, Jewkes et al.  have demonstrated an association between such HIV risk factors and IPV, although a direct association has not been seen between IPV and HIV positivity.
An interventional prospective study in South Africa, by Pronyk et al.,  showed that economic empowerment and skill development of women reduced IPV by 55% in the intervention group. The microfinance initiative was linked with an HIV awareness program. However, neither the risk behaviors nor the HIV prevalence showed a significant difference at the end of follow up (after three years) between groups.
Studies outside Africa report a strong association between violence and HIV risk. In a cross-sectional survey of adolescents in USA, Viosin et al.  have reported that those exposed to family or community violence are three to four times more likely than their peers to engage in HIV risk behaviors. However, this association was more common in boys than in girls. In a survey of Hispanic women in Boston, USA, Raj et al.  have reported increased HIV risk for abused women than non-abused women. In India, a systematic multistage survey delineated a close relationship between IPV and risk behavior [men with extramarital affairs and STD symptoms were more likely to abuse their wives (OR-6.22 and 2.43, respectively)]. 
In addition to IPV, women are victimized by other means, especially in times of war and civil unrest. Rape of women is well-documented in many civil wars in Africa (Rwanda, Sierra Leone, and Liberia). In some situations women were deliberately raped by HIV positive individuals to inflict psychological trauma and a 'painful' death.  In Nepal, at the beginning of the Maoist insurgency (1999), the HIV prevalence in Kathmandu stood at 2.7%. Three years later it had shot up to 17%.  Vulnerability of refugee women for transactional sex was identified as a risk factor for HIV in a survey of the Lugufu refugee camp (Tanzania) by Rowley et al.  A significant proportion of refugees reported forced sex (P  Subsequent analysis of the sero-status of such sex-trafficked Nepali women have shown disproportionately higher rates of HIV infection compared to native Indian sex workers. , While many studies and interventions have targeted female sex workers (FSWs), few have observed the STD profile and HIV risk of male clients of FSWs. They are an important source of spreading the infection via heterosexual intercourse. Recent studies in Mexico, China, and India have all shown high risk behaviors and fairly high rates of HIV and other STDs in this group. ,,
HIV positivity makes women vulnerable to violence
Violence following disclosure of the sero-status is not a universal phenomenon. It depends on the locality studied. Studies in United States have failed to demonstrate a higher rate of domestic violence against HIV-positive women when compared to sero-negative women. ,, In a study by Gielen et al.  , only 4% of the sample reported physical abuse immediately following disclosure. Still 45% reported some form of abuse since the time of disclosure.
A study in Tanzania showed that HIV-positive women had a higher risk of physical and sexual violence than HIV-negative women.  Violence was more likely to occur when the sero-status of the partner was unknown. In a prospective study in Kenya, 10% of the women experienced violence or disruption of the relationship following disclosure. 
In a statistical analysis of UNAIDS data from 77 countries, Talbott et al.  have identified that income inequality within a country has a positive correlation with HIV prevalence. Several studies reporting a link between violence and HIV also report a correlation between poverty and HIV. ,, Limited financial power limits autonomy in sex for women. Langen et al.  reports that women who are economically dependent on their partners are less likely to insist on condoms during sex. There are several other studies conducted in Sub Saharan Africa that correlates low socioeconomic status with a high HIV risk. ,,
Food insufficiency is a marker of poverty that places women at a significant disadvantage to acquire HIV. In a population-based, cross-sectional study in Swaziland and Botswana, Weiser et al.  report that food insufficiency is associated with many risk behaviors for HIV (inconsistent condom use with a non-primary partner [Adjusted odds ratio (AOR) -1.73], intergenerational sexual relationships (AOR-1.46), sex exchange (AOR-1.84), and lack of control in a sexual relationship (AOR-1.68)). Interestingly, men reported fewer instances of food insufficiency and a lesser correlation between that and risk behaviors. Dunkle et al.  and Oyefara  have independently confirmed some of these associations with food insufficiency.
Several studies outside Africa, have demonstrated a positive correlation between HIV risk and poverty, for women. A study in China on FSWs has shown that some entered the trade voluntarily.  However, the driving force for selling sex was poverty. If social poverty was avoided it is assumed that these women would not sell sex and will not be at risk of acquiring HIV. Many 'low end' FSWs in India (streetwalkers) are unable to negotiate with the client to minimize risk behaviors. Unfortunately they account for a larger proportion of all FSWs.  Interestingly in Australia, a wealthier country, no difference in lifetime self-reported STDs have been observed in streetwalkers, private and brothel based sex workers. 
Migration for economic reasons is another risk factor for HIV in both sexes.  Women have become a sizable proportion of the migrant population, which may have a significance in the feminization of the epidemic. , Migrant male workers' risk of acquiring an STD has been linked to the time spent in the host country.  In the South Asian context, these men are an important source of infection for women (both spousal and non-spousal partners). ,
The studies by Oyefara  , Dunkle et al.  and Weiser et al.  need special mention as they have not restricted the measures of poverty to family income. There may be differences in the way income is distributed in a family, which may be disadvantageous to the women. This phenomenon may create a state of 'relative poverty' for women and female children (depending on the gender norms of the society) although the family income is reasonable. Pronyck et al.  in their interventional study failed to show a reduction in HIV incidence or risk behaviors in the intervention group, despite the upliftment of economic standing, which may be a result of the above phenomena. The study in Botswana and Swaziland showed little correlation between low socioeconomic status and HIV risk, while there was a significant risk correlation for food insufficiency.  In fact food insufficiency may be a better marker of poverty as it represents a final common pathway of poverty than income. It is important to identify similar markers of poverty in different societies that might better correlate with HIV risk than wealth.
Gender norms and culture
Gender norms can be defined as appropriate behaviors, beliefs, attitudes and conduct per gender as directed by society. It is a learnt behavior. In assigning gender roles, the phenotypical differences of genders are redefined as feminine and masculine with different capabilities in societal functioning (e.g., division of labor, power sharing, economic responsibility, dominance and submission).  Such gender norms are different in various societies and subject to change with time.  Yet, in many countries, especially in the developing world where HIV is spreading fast, females serve a subservient role to men as dictated by gender norms and culture. , These traditional norms place women at an increased risk as they have less freedom in choosing their partners, initiating and pacing sexual activity and negotiating on safer sex. , In addition, some traditions, customs and beliefs are also harmful to women (wife inheritance, having sex with a virgin as a cure for HIV). ,
In our review, we have identified several studies linking gender roles to risk behavior. In a cross sectional analysis of females in detention in Georgia, USA, Voisin et al.  concludes that gender norms favoring male dominance as well as high-risk peer norms were significantly associated with STD risk (P et al.  in South Africa gives an insight on changing gender roles and their impact on HIV. Their results were different to what was expected. Among men, hyper-romanticism and favoring of male dominance were associated with more consistent condom use (especially with the primary partner). More open sexual ideology was associated with less consistent condom use. Interestingly, more open sexual norms and hyper-romanticism in women was significantly associated with more partners. Similar unexpected findings were reported by Kaufman et al.  They showed that endorsement of traditional male dominant gender norms were associated with less HIV risk behavior for men. However, a negative attitude toward women showed (as expected) a positive correlation with risk behavior.
Qualitative studies may be a better tool to assess the complex interactions between gender norms and HIV, although the generalizability of findings remains doubtful. The interference of prevalent gender norms with HIV-prevention strategies is delineated by Go et al.  in a qualitative study in slum communities of Chennai, India. Risk behaviors such as multiple partners for men were 'acceptable' by the prevalent norms. Using condoms with regular partners was rare even when women were aware of its protection (as it would imply questioning a man's fidelity). Refusal of sex with husband was not an option even when the wife perceived a risk of infection. Similar findings were reported by Hebling et al.  Despite being educated on HIV transmission risks, women were unable to take precautionary measures due to prevalent gender norms and male dominance. In a study on African American adolescents in USA, Kerrigan et al.  explain how the female gender ideologies of care taking and emotional strength (standing by the man) can make them value relationship intimacy more than protection against HIV/STDs.
Despite their obvious negative impact on AIDS control, the traditional norms may have served a protective role against HIV too. In many developing nations, premarital sex is discouraged by tradition and is highly stigmatized. The 'virginity' of a female is still expected till marriage in many Asian and African societies. ,, Though it is a marker of discrimination against women, the fear of such discrimination may have discouraged premarital sex among adolescents helping to keep the epidemic at bay. It is interesting to note how the changing gender norms have made an impact on premarital sex, virginity norms, and HIV prevalence.
Gender differences in adherence to prevention and treatment measures
It is a commonly held view that women have less access to HIV/STD prevention programs, especially in developing nations. In three high prevalence African countries (Burkina Faso, Ghana, Zambia), a better knowledge of HIV in females was associated with living in a community with more opportunities (better education, higher age in marriage and initiation of sex).  A positive association between HIV knowledge and education has been reported in several other studies in Africa. ,,,, A community-based study in rural Malawi has shown that while both sexes had a good knowledge of transmission of HIV/AIDS, men were more knowledgeable than women. Age, education, occupations other than farming, and childhood residency in a city were associated with better knowledge. 
The few studies conducted outside Africa (within our search limitations) showed conflicting results. A cross-sectional analysis among university students in Afghanistan showed that only 28.3% of students had a good knowledge of AIDS and the scores were better in females.  A similar study in China has shown that the overall knowledge scores were significantly high in males compared to females (P  Yet, the level of education had a minimal impact in certain situations. A survey among secondary school girls in New Delhi, India has shown gross inadequacy of HIV- and STD-related knowledge (30% thought HIV can be cured, 21% thought oral contraceptive pills (OCP) would protect against HIV). 
The importance of educational interventions for women has been underscored in several studies. ,,,, Diclemente et al.  in a randomized controlled trial demonstrated that adolescent girls who underwent a comprehensive educational package on HIV/AIDS had significantly less risk behaviors in a 12-month follow-up period. Gavin et al.  in their study on adolescent females in Zimbabwe have shown that those who had sex education in schools had a decreased risk of HIV (OR-0.43). Chhabra et al.  and Hecej et al.  have reported better risk reduction practices in adolescent females compared to males following an educational program in India and Croatia, respectively. Interestingly a similar program targeting a different high-risk group in China (clients of FSWs) has shown promising results, with a significant increase in those using prevention services (OR-2.2). 
HIV testing, risk perception, and disclosure of sero-status are also reported to show a gender difference. Age, literacy, good doctor-patient relationship were associated with disclosure for men while having children, and being religious were associations for disclosure in women.  A cross-sectional survey among African American adolescents in the US has shown that females were significantly more likely to undergo voluntary HIV testing (OR-2.4 to 2.7) than males. 
However, several studies involving sexually active females have shown that a good knowledge of HIV is not synonymous with avoiding risk behavior. ,, In other words the knowledge is not put to practice. There are two main reasons for this paradox, impaired risk perception , and social barriers, that limits sexual autonomy for women. Some authors suggest a gender difference in risk perception as well. 
The paradoxical impact of education on HIV in the early 1990s in Africa is worth mentioning. HIV was associated with a better education in the early days of the epidemic in Africa. Some authors explain this phenomenon by the hypothesis that better educated had better jobs, more money, and more access to paid sex and IV drug use.  Education without an effective sex education component may have a minimal role in countering the epidemic. Asia today, may be in the state Africa was two decades ago.
Highly active antiretroviral therapy
In this section we discuss the results of studies that have looked into a gendered difference in HAART-related issues (availability, accessibility, and adherence), excluding those related to the biological differences of sexes (side effects and clinical and viral response).
An analytical study of 23 sero-converter cohorts from Europe, Australia, and Canada have shown that women fared better after HAART was introduced. Comparing the pre-HAART (before 1997) period and the HAART era, authors have reported a lesser risk of AIDS and death in women compared to men (OR-0.76 and 0.68, respectively).  Moore et al. and Chen et al. have both reported a better outcome for females in two cohorts on HAART. ,
It is speculated that women in resource-limited settings may have restricted access to treatment due to socioeconomic constraints and gender norms.  However, the evidence is contrary to this. Chandra et al.  , Muula et al.,  and Braitstein et al.  have all shown that women are not at a disadvantage in access to HAART, in resource-limited settings. The epidemiology update of UNAIDS for 2008 confirm these findings. In 45 developing countries (with the exception of Chile and Belize) the coverage was better for females with HIV. Still, it is important to note that the overall coverage of HAART in these settings was low. In many countries, coverage of the HIV-positive population with HAART was less than 40% for both men and women. Only 35% of pregnant women had access to the therapy in 2008. 
Adherence to therapy is another dimension of interest. Several authors have reported women to be less adherent to HAART. ,,,, Several possible associations with this observation are depression, , alcohol dependence, , other substance misuse, , and increased side effects in women. 
In summary, as expected, violence, gender norms, and poverty placed women at a disadvantage with regard to HIV/AIDS (increased risk of contracting HIV and increasing the burden of those living with the disease). However, regarding access to HAART, females fared better than males in many parts of the world.
In interpretation of the available evidence, the following issues need attention:
The vulnerability of sex-trafficked women, prostitutes, and victims of rape to HIV is obvious. However, the rise in the rate of infections at times of war and displacement is simply not a case of women being raped by the 'enemy'. It may be the result of a complex interaction of several risk factors like, transactional sex, poverty, lack of opportunities, breakdown of civil order, and less rigid sexual norms.
Many studies only demonstrate that HIV positive women were significantly subjected to violence compared to the HIV-negative population. It is not clear whether the violence increased or began after sero-status disclosure. More studies are needed to identify which comes first; violence or HIV, or is it a vicious cycle.
Poverty and its relation to HIV is simply not an issue that can be reduced to the availability of money. Low income countries obviously may have many risk factors for HIV spread such as illiteracy, unemployment, and lack of opportunities for women. Yet, countries with a better income also have their own risk factors (fast life style, overcrowding in cities, and prostitution). Even in the affluent countries there may be microenvironments that are disadvantaged and not any different from the developing world with regard to HIV risk. When the data are generalized to the whole country, these significances go unnoticed. This argument is further supported by the findings of Talbott et al.  who showed that while the gross domestic product (GDP) of a country shows little or no relation to HIV/AIDS prevalence, the income inequality shows a positive correlation.
Regarding gender norms, there is the obvious need to discuss the conflicting or rather unexpected findings of some studies, , which do not collaborate with the view of high HIV transmission risk and traditional gender norms. This may be partly explained by the theory that traditional gender roles are changing in contemporary societies. Evidence for such change has been documented in the educated younger generations of South Africa. , Such contrasts may also be influenced by the improved awareness of the transmission of HIV. The more consistent use of condoms by dominant males may be an expression of responsibility or a measure for their own protection as they are likely to have multiple partners. More open sexual ideology being associated with less condom use may be an indicator of trust and selection of an educated and similar partner. Still the association of hyper-romanticism and open sexual ideology with more partners, in females, is difficult to explain. However some weaknesses in the study methodology may have influenced the outcome. The samples were not representative of the general population (Harrison et al.  used a sample with a disproportionate number of females in the ratio of 2:1, while Kaufman et al.  used a sample of high-risk males only). The sample sizes were limited to generalize the findings to a larger community.
On educational interventions and their gender implications, many studies have demonstrated a positive link between living in urban communities, education, and better HIV knowledge for women. ,,,, Faced with the epidemic, many Sub Saharan countries have initiated educational campaigns for the public, with funding from global agencies. The positive impact of such interventions are clearly visible, specially with regard to females. , However, the picture in the Asian context is less promising. Although many countries in Asia are still considered to be low prevalence, this can be a false state of complacency. Despite the fact that cultural barriers may prevent effective sex education at schools; the risk behaviors are high even among those having access to education. , Male dominance and gender norms limit a woman's ability to protect herself from infection despite being educated about HIV/AIDS. Therefore, we propose that a successful education program must concentrate on both sexes equally and be sensitive to prevalent gender norms in the society.
The evidence does not support the commonly held belief that women are at a disadvantage with access to HAART in resource-limited settings. This may be explained by the fact that women have two motives to enter a treatment plan to treat themselves and to prevent mother-to-child transmission.
There were several limitations in our review; it was limited to articles published in English only, and it is possible that important studies published in other languages were missed. Most of the data was from African and Asian countries; data from Latin American and Eastern European countries was minimal. Data on response to HAART was predominantly available from cohorts in developed countries. Such gaps in the available data affect the validity and generalizability of our conclusions.
We have recognized the following as areas with 'gaps in knowledge'. These issues should be explored with further research.
Incidence and form of violence against HIV-positive women by intimate partner and others, following disclosure of sero-status in developing countries is not well explored.Specific markers of poverty that may reflect the relationship between HIV and women better than wealth itself, needs to be investigated. Such markers may be different in each community (as food insufficiency was an indicator in some African countries).Changing gender norms and their impact on women and HIV has been inadequately explored in Asia. The protective role (if any) of traditional gender norms and virginity norms needs to be identified.Specific issues in different societies that cause discordance between knowledge and practice has to be analyzed as this has a direct impact in policy design on prevention.Why do women have better access to HAART (as shown by statistics) despite the commonly held belief to the contrary? It is important to keep track of sex ratios on HAART as more people gain access to it, to avoid discrimination of women.Identification of culturally appropriate educational tools to impart sex education for adolescents is a need of the hour.
The gendered implications of many aspects of HIV are apparent. The traditionally held view that women are at a disadvantage is true with regard to several issues such as violence, poverty, and gender norms. In treatment-related issues, women (at least in Africa) have made significant gains with better awareness. The access to HAART was better for females in many resource-limited settings, although the overall coverage was unsatisfactory.
Much of the work done in the last decade has focused on the Sub Saharan Africa, which is the hub of infection with large numbers of patients. However, the social and cultural dynamics of Asia and Africa are quite different. Although many Asian countries (India, China) are considered to be low prevalence ones for HIV, the disease burden may actually be considerable in Asia for two reasons; the large population (even a smaller percentage equates to a large number of infections) and under-reporting. Given the potential reservoir of infection, the focus of research in the coming decade should be Asia.
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