chapter7 Chapter 7

Not listening, and not explaining the epidemic, 1989-2009 Informed opinion and active co-operation on the part of the public are of the utmost importance in the improvement of the health of the people. – Constitution of the World Health Organization, 1946[i] One-way communication from health experts to the public has characterized and damaged the response to HIV in countries with generalized epidemics. Researchers have not worked with HIV-positive adults to trace the source of their infections, and health experts have not believed HIV-positive adults who deny heterosexual risks. From racial stereotype to hypothesis Through the early 1990s, most AIDS experts supposed that the spread of HIV among the general population in Africa, but not in the US or Europe, was largely due to Africans having more sexual partners than Americans or Europeans. In 1989, one journal article described Africans as susceptible to AIDS because they are less cautious, more impulsive, less inhibited sexually, and less intelligent.[iii] This unusually crude presentation resonated with widely held views of African sexual behavior. Stillwagon attributes misunderstanding of Africa’s AIDS epidemic to ‘Centuries-old stereotypes that emphasize exotic and exceptional sexuality’ in Africa. [ii] As early as 1989-90, surveys of sexual behavior coordinated by the Global Programme on AIDS in 12 African countries challenged stereotypes of African sexual behavior. Findings from these surveys were ‘totally incompatible with the view…that the HIV pandemic in Africa was fueled by extreme promiscuity…The results from the African surveys do not portray a region with uniquely high levels of partner change.’[iv] Furthermore, these surveys showed big differences in sexual behavior from one African country to another – differences that did not correspond to differences in HIV prevalence. In 1991, Packard and Epstein criticized the ‘premature closure of African AIDS research.’[v] …[A]ssumptions about the importance of sexual promiscuity in the transmission of HIV in Africa were initially based on limited, and in some cases methodologically questionable data. These assumptions, nonetheless, served to shape both the questions which AIDS researchers asked and the way in which they interpreted data. This narrowing of research in turn discouraged serious consideration of the role of alternative avenues of transmission… We are in fact much further from understanding the epidemiology of AIDS in Africa than some medical researchers, development officers, and social scientists would have us believe… Table 7.1: Proportions of men and women aged 15-49 years reporting 0-1 sexual partners in the past year, and proportions of HIV infections in such men and women, in 24 countries with generalized HIV epidemics* Country, year of survey Adult HIV prevalence (%) Women reporting 0-1 sex partners last year Men reporting 0-1 sex partners last year % of all women % of HIV- positive women % of all men % of HIV-positive men Africa Mali, 2006 1.2 100 100 97 96 Rwanda, 2005 3.0 100 99 97 97 Ethiopia, 2005 1.4 100 98 98 88 Zimbabwe, 2005-06 18.1 99 98 91 90 Malawi, 2004 11.8 99 98 90 85 Ghana, 2003 2.2 99 97 90 89 Niger, 2006 0.7 99 100 88 70 Burkina Faso, 2003 1.8 99 97 85 91 Zambia, 2007 14.3 99 97 84 75 Benin, 2006 1.4 99 99 79 72 Swaziland, 2006-07 25.9 98 97 86 75 Kenya, 2003 6.7 98 95 89 78 DRC, 2007 1.3 97 97 83 81 Uganda, 2004-05 6.4 97 95 79 66 Tanzania, 2007-08 5.7 97 96 82 72 Guinea. 2005 1.5 97 96 75 56 Cote d’Ivoire, 2005 4.7 96 93 75 75 Cameroon, 2004 5.5 95 91 70 48 Liberia, 2007 1.6 94 90 82 90 Lesotho, 2004 23.5 92 89 77 70 Asia and the Caribbean India, 2005-06 0.28 100 99 99 97 Cambodia, 2005 0.6 100 100 94 79 Haiti, 2005-06 2.2 99 94 77 76 Dom Republic, 2007 0.8 97 97 76 69 * All countries for which data are available from national surveys. Note: Percentages of women and of HIV-positive women with 0-1 sex partners in the past year are calculated from published data from national surveys by subtracting the numbers of women and of HIV-positive women with two or more sex partners from totals for women. Percentages for men are calculated in the same way. Sources: See the Statistical Annex. In national surveys in 20 African countries, Haiti, and the Dominican Republic during 2003-08, over 90 percent of women reported 0-1 sexual partners in the past year, and these women accounted for 89 percent to 100 percent of HIV infections in women (Table 7.1). Across the same 22 countries, men who reported 0-1 sexual partners in the past year accounted for 48 percent to 97 percent of HIV infections in men. Similarly, surveys in Cambodia and India found little or no concentration of HIV infections in the small minority of adults reporting two or more sexual partners in the past year. In 2006, a prominent review of information on sexual behavior around the world reported a ‘comparatively high prevalence of multiple partnerships in developed countries, compared with parts of the world with far higher rates of sexually transmitted infections and HIV, such as African countries…’[vi] Nevertheless, some experts have continued to argue that distinctive patterns of heterosexual behavior have been responsible for Africa’s ferocious AIDS epidemics. In recent years, the most common formulation of this argument has been that Africans have more concurrent partners (more than one ongoing relationship). For example, a book published in 2007, relying on data selected from surveys in several countries during 1989-90, generalized that ‘From 20% to 40% of sexually active adults (both males and females) in many SSA [sub-Saharan African] populations’ have ‘unprotected sex with multiple and concurrent sex partners.’[vii] Clearly, diverse views of African sexual behavior have survived findings from years of research, and continue to influence experts’ explanations of Africa’s HIV epidemics. Unethical research: exposing and disrespecting participants From the late 1980s and continuing into the 21st century, prominent research projects intended to study HIV transmission risks and HIV-related disease tested and followed HIV-positive and HIV-negative Africans without telling them the results of their HIV tests. Researchers watched adults who did not know they were HIV-positive infect unsuspecting spouses, watched them sicken and die, watched HIV-positive women birth and infect children, and watched the children die. Testing and not telling not only exposed research participants to unnecessary risk, but also showed disrespect for their ability to help researchers to identify risks. Researchers who did not tell Africans they were infected were not able to work with them to trace the source of their infections. Thus, testing and not telling not only kept Africans in the dark about their HIV infections, but also kept researchers in the dark about the factors that made Africa’s HIV epidemics the worst in the world. In such projects, researchers have characteristically offered participants a free additional HIV test with counseling at a nearby clinic. Many participants did not go for additional tests. From this, the researchers’ defense for following people who did not know they were HIV-positive has been that they did not want to know. But there is another way to approach the issue. If someone does not want to receive the results of their HIV test, the researcher can refuse to enroll them in the study. In 1988, the US Office for Protection from Research Risks established a policy that ‘Individuals may not be given the option “not to know” the result, either at the time of consenting to be tested or thereafter.’[viii] One project that followed that policy in Kigali, Rwanda, from 1988 had no problem enrolling pregnant women in research: ‘…all but a handful of women wanted to know their test results and many requested that HIV testing and counseling be provided to their spouses as well.’[ix] However, the US policy allowed exceptions. From 1989, researchers funded by the US government began a large study in Rakai, Uganda, testing and enrolling men and women without insisting they learn their HIV status. The study followed and retested thousands of adults, and continued at least into 2006. During 1994-98, the Rakai project followed hundreds of discordant couples. In a large sub-sample of these couples, just over half the HIV-positive partners ‘had requested and received HIV counseling, …25% stated that they had informed their partners,’ and ‘Condom use was low…’[x] With many partners in discordant couples not knowing that they or their spouses were infected, the project observed 50 incident infections in men and 40 in women with HIV-positive partners.[xi] Similarly, a project in Mwanza, Tanzania, during 1991-94 observed six incident infections in men and women with HIV-positive partners. The study team noted:[xii] In most prospective studies, intensive counseling of discordant couples has resulted in the adoption of safer sexual practices, and this has limited their capacity to examine risk factors and transmission rates. In the Mwanza study…cohort members were only informed of their HIV status if they accessed a parallel voluntary counseling and testing service. Only a small number of participants pursued this service. During 1997-2000, the Zimbabwe Vitamin A for Mothers and Babies (ZVITAMBO) study tested and followed over 4,400 HIV-positive women and their newborn children, observing HIV infections and deaths in the children.[xiii] As the study was designed,[xiv] Mothers could learn their [HIV test] results at any time during the study..., but they were not required to do so. This feature makes ZVITAMBO unique. All other studies of infant feeding and HIV have been conducted among mothers who knew their HIV status. Table 7.2: Funders for selected studies that followed HIV-positive Africans who did not know they were infected Where and when Who was followed? Who paid for the research? Uganda, Rakai, from 1989 to at least 2006 [xv] Adults, including couples, and some infants National Institute of Allergy and Infectious Diseases, US; National Institute of Child Health and Development, US; Rockefeller Foundation; Fogarty Foundation; GlaxoWellcome Foundation; John Snow Inc.; Pfizer Inc. Tanzania, Mwanza, 1991-94 [xvi] Adults, including couples Commission of the European Communities; Center for International Migration and Development, Germany; Department for International Development, UK; Medical Research Council, UK Zimbabwe, Harare, 1997-2000 [xvii] Mothers and infants Canadian International Development Agency; USAID; Bill and Melinda Gates Foundation; Rockefeller Foundation; BASF (Ludwigshafen, Germany) Sources: See references by row. Less than 20 percent of women chose to learn their HIV status. Ninety-two percent of HIV-positive mothers were still breastfeeding at one year.[xviii] With prolonged breastfeeding, the project observed 64 incident infections in children between the ages of 12 and 24 months. If the project had told women they were HIV-positive and might infect their children, could the women have managed replacement feeding, or at least weaned children after 6 months? These were urban women, in one of the wealthier countries in Africa. More than 80 percent of the women and more than 90 percent of their husbands had received at least 8 years of education. Rich country governments and other prominent organizations funded these projects (Table 7.2), and institutional review boards approved them. Even so, these and other similar projects in Africa compare unfavorably to the widely criticized Tuskegee Study of Untreated Syphilis in the Negro Male. From 1932 to 1972, the Tuskegee Study followed African-American men with syphilis, watching them sicken and die without treating their syphilis. The men had tertiary syphilis, so they could not transmit to others, but they suffered heart disease, dementia, and other health damage. Participants in HIV research in Africa who did not know they were HIV-positive not only sickened and died but also passed HIV to spouses and children. Despite the Nuremberg Code,[xix] the World Medical Association Declaration of Helsinki,[xx] and other documents that provide ethical guidelines for medical research, it is a continuing challenge to recognize and to stop unethical research, particularly in Africa. Disbelieving people who deny sexual exposures Another manifestation of researchers and other AIDS experts devaluing and disrespecting people living with HIV, and what they have to teach others about the epidemic, is the common practice among AIDS experts of disbelieving HIV-positive people who deny sexual exposures to HIV. From the 1980s, substantial numbers of HIV-positive men and women in countries with generalized epidemics have reported never having penetrative sex. In a national survey of women aged 15-19 years in Zimbabwe during 2001-02, 41 percent of 192 women who were HIV-positive reported having no sex partners ever.[xxi] South Africa’s 2005 national survey found 4.3 percent HIV prevalence and (using special blood tests to differentiate new from old infections) a rate of incidence of 1.5 percent per year among adults who reported no sexual partners ever.[xxii] In national surveys in 24 countries with generalized epidemics during 2003-08, HIV prevalence ranged from 0 percent to 5.2 percent in women who claimed to be virgins, and from 0 percent to 3.7 percent in men who claimed to be virgins (Table 7.3). In addition, many studies in Africa have found HIV prevalence or incidence in adults who are not virgins, but who report no possible sexual exposure to HIV. For example, a study in Zimbabwe during 1999-2003 followed more than 1,000 initially HIV-negative women. After three years, another round of HIV tests found 48 women with new infections. Twelve of these 48 women reported no sexual partners after their last HIV-negative test. Surprisingly, women reporting no sexual partners acquired HIV faster than women who reported one or more sex partners (1.6 percent vs. 1.2 percent per year).[xxiii] South Africa’s 2005 national survey found the same rate of HIV incidence – 2.4 percent per year – in non-virgin adults who reported no sex partners in the past 12 months as in adults who reported one or more sex partners in that period.[xxiv] Many researchers and other AIDS experts have routinely interpreted HIV infections in Africans who deny sexual exposures as evidence that they have misreported their sexual behavior.[xxv] There is no doubt that people often lie and sometimes forget, and it is good science to question evidence. However, it is not good science to reject unwelcome evidence for 20 years without doing what is necessary to collect ‘solid’ evidence that one trusts to test an hypothesis. Table 7.3: HIV prevalence in virgin men and women aged 15-49 years in countries with generalized epidemics* Countries HIV prevalence (%) All women Virgin women All men Virgin men Africa Benin, 2006 1.5 0.3 1.2 0.2 Burkina Faso, 2003 1.8 0.5 1.9 0.8 Cameroon, 2004 6.8 0.7 4.1 1.0 Cote d’Ivoire, 2005 6.4 0.0 2.9 0.4 DRC, 2007 1.6 1.2 0.9 0.6 Ethiopia, 2005 1.9 0.1 0.9 0.2 Ghana, 2003 2.7 0.0 1.5 0.2 Guinea, 2005 1.9 0.1 0.9 0.6 Kenya, 2003 8.7 1.6 4.6 0.9 Lesotho, 2004 26.4 5.0 19.3 3.7 Liberia, 2007 1.8 0.3 1.2 0.2 Malawi, 2004 13.3 2.5 10.2 1.8 Mali, 2006 1.4 0.0 0.7 0.9 Niger, 2006 0.7 0.2 0.7 0.2 Rwanda, 2005 3.6 0.8 2.3 0.2 Swaziland, 2006-07 31.1 5.2 19.7 2.1 Tanzania, 2007-08 6.6 0.7 4.6 1.1 Uganda, 2004-05 7.5 0.8 5.0 0.2 Zambia, 2007 16.1 3.7 12.3 3.5 Zimbabwe, 2005-06 21.1 3.9 14.5 2.7 Asia and the Caribbean Dominican Republic, 2007 0.8 0.0 0.8 0.3 Cambodia, 2005-06 0.6 0.1 0.6 0.0 Haiti, 2005-06 2.3 0.0 2.0 0.2 India, 2005-06 0.22 0.03 0.36 0.13 * All countries for which data are available from national surveys. Sources: See the Statistical Annex. Examples of incomplete research with unreliable conclusions As described in previous sections, researchers have often not told research participants that they are infected, and so have not been able to work with them to trace the source of their infections. Researchers have also routinely disbelieved participants who deny sexual exposures, and they have seldom asked about blood exposures. Here are several examples of research designed and implemented in ways that deny and ignore information on risks for HIV infection. Example of faulty research among African women A study in Rakai, Uganda, during 1994-99, observed much higher HIV incidence in unmarried pregnant women (9.9 percent per year) than in married pregnant women (1.6 percent per year) or in non-pregnant unmarried or married women (1.6 percent and 1.0 percent per year, respectively). [xxvi] Even though high incidence was strikingly concentrated in unmarried pregnant women, the study team proposed that hormonal changes during pregnancy increased women’s susceptibility to acquire HIV from sexual partners. This hypothesis did not agree with reported evidence. Notably, among the subset of women whose partners were known to be HIV-positive, pregnant women acquired HIV infection less than twice as fast as non-pregnant women. Furthermore, all pregnant women, married and unmarried, who acquired HIV infection reported no sexual partner other than the fetus’ father in the past year. The study did not consider that unmarried pregnant women were more likely to seek abortions than married pregnant women, and to contract HIV during abortions. (Similarly, women who knew their husbands were HIV-positive might also seek abortions.) Ignoring risks from abortions, the study team did not report available information on pregnancy loss,[xxvii] which they could have used to test this hypothesis. This alternate hypothesis has obvious implications for HIV prevention. Moreover, the study did not tell women their HIV status, and so did not benefit from their views about how they might have been infected, and did not work with them to trace the source of their infections. Example of faulty research among African men During 2002-06, three studies – in South Africa,[xxviii] Uganda,[xxix] and Kenya[xxx] – solicited men wanting to be circumcised, then on a random basis circumcised some men first, but told others to wait. Following and retesting the men, the studies observed that circumcised men acquired HIV infection only 24-45 percent as fast as uncircumcised men. All three study teams concluded that lower HIV incidence in circumcised men was due to less sexual acquisition of HIV. That may be so. But to reach that conclusion, the study teams rejected what the men reported about their sexual behavior and ignored information about non-sexual risks. Consider a basic question: What percentage of the incident infections in men in these three studies were acquired from sexual partners? In the South African trial, 23 (of 69) infections occurred in men who reported no unprotected sex during the relevant observation interval (the time from their last negative test to their first positive test). Similarly, in Uganda, 16 (of 67) infections occurred in men who reported no sex partners (6 infections) or 100 percent condom use (10 infections). The trial in Kenya did not report how sexual exposures related to HIV incidence – except for seven men infected in the first three months (sensitive tests did not find HIV in the men’s blood at the beginning of the trial). Five of the seven men, including three of four who had been circumcised, reported no sexual exposures from the beginning of the trial until their first HIV-positive test. If men with no sexual exposures acquired HIV from non-sexual risks, this no doubt occurred for some of the men with sexual exposures as well. Thus, if one accepts the men’s reported sexual behavior, standard epidemiological analyses (see notes to Table 8.1) suggest that a majority of their infections came from non-sexual risks. If the studies had been done correctly, and had traced sexual partners, that would settle the matter. However, that was not done. Although two of the three studies (in Kenya and Uganda) told men their HIV status, neither of these studies worked with men with incident infections to see if their sexual partners were the source of their infections. Considering how few partners were involved in the Ugandan study – men reported more than one sexual partner during less than a third of the observation intervals, and 47 percent of the men were married – tracing and testing most of the men’s partners would appear to have been feasible. The South African study team was the only one that estimated HIV transmission per sexual exposure to HIV. Because the study team did not trace and test the men’s partners, the estimate was based on a model which assumed that some percentage of their sexual partners were HIV-positive. This approach produced some surprising (and unreliable) results: for example, that condom use decreased HIV transmission per event by 10 percent only, while circumcision decreased it by 75 percent.[xxxi] What about non-sexual risks? In the South African trial, men who reported an injection, blood transfusion, and/or hospitalization were 1.7 times more likely to become HIV-positive than men who did not report these risks. This was the only one of the three trials to report blood exposures during follow-up. Two studies reported that 30-43 percent of HIV infections occurred during intervals when men reported genital ulcers or other genital symptoms or problems, but neither study reported the associated skin-piercing tests and treatments. In the Kenyan trial, circumcision might have infected four men whose infections were recognized one month later, but the study did not mention that possibility. These studies, with their ignored evidence (on sexual exposures) and missing evidence (on blood exposures and on HIV status of sexual partners), launched programs to circumcise millions of African men. These programs may alleviate HIV epidemics, although information on HIV prevalence in circumcised and uncircumcised men from national surveys in 13 African countries (see Table 7.4) suggests otherwise. If one believes what the men reported about their sexual behavior, a lot of their infections came from blood exposures. If so, programs to circumcise millions of men should be carried out with extreme caution, and (other) important initiatives to cut HIV incidence are to warn men about blood exposures, and to improve infection control in hospitals and clinics. Failing to identify sexual factors responsible for generalized HIV epidemics If heterosexual coitus accounts for most HIV infections in generalized epidemics, what factor or factors allow HIV to transmit so much more extensively through heterosexual sex in generalized vs. concentrated epidemics? From studies of discordant couples in the US, Europe, and Africa, widely quoted estimates of transmission per coital act range from 0.05 percent to 0.11 percent, or once every 900 to 2,000 events.[xxxii] Similarly, most studies of HIV transmission between discordant couples – even when couples are not aware that one partner is HIV-positive – report that not more than 10 percent of the HIV-negative spouses contract HIV from their husbands or wives during a year.[xxxiii] With observed low rates of transmission between spouses, how could sexual transmission create generalized epidemics, especially the terrible epidemics found in Southern Africa and in many cities in East and Central Africa? The first idea, that Africans were outrageously promiscuous, fell to evidence in the early 1990s. Over the ensuing fifteen years, a host of other hypotheses supposed that one or more sex-related factors accelerate sexual transmission enough to create generalized epidemics. Although many behaviors or physical conditions are personal risks to acquire or to transmit HIV through sex, studies have been unable to show that these factors explain differences in HIV prevalence between Africa and Europe, or across African countries. For example, having a genital ulcer is a personal risk – people are more likely to acquire HIV infection from sexual partners if either has a genital ulcer than if neither does. However, studies across Africa have found that communities in which more people have genital ulcers, gonorrhea, herpes simplex virus type 2 (genital herpes), or other sexually transmitted diseases do not consistently have greater HIV prevalence or incidence than communities in which fewer people have these conditions.[xxxiv] Similarly, some experts aver that higher HIV prevalence in Africa is due to Africans having more concurrent (overlapping) sexual partners than people in other continents.[xxxv] Having two ongoing sexual partnerships may be a personal risk to acquire and to transmit HIV. However, African communities in which more people have concurrent partners do not consistently have higher HIV prevalence than other African communities.[xxxvi] Table 7.4: Percentage of men circumcised, and HIV prevalence in circumcised and uncircumcised men in 13 countries with generalized epidemics* Countries, year of survey % of men circumcised HIV prevalence (%) in Ratio of HIV prevalence in circumcised vs. uncircumcised men Circumcised men Uncircumcised men Swaziland, 2006-07 10 26 29 0.90 Rwanda, 2005 10 3.8 2.7 1.4 Zimbabwe, 2005-06 11 20 19 1.1 Zambia, 2007 13 13 15 0.87 Uganda, 2004-05 26 4.7 7.4 0.64 Lesotho, 2004 59 26 24 1.0 Tanzania, 2007-08 69 4.6 9.0 0.51 Kenya, 2003 88 3.7 22 0.17 Ethiopia, 2005 88 1.1 1.2 0.92 Burkina Faso, 2003 90 2.1 4.2 0.50 Cameroon, 2004 93 5.1 1.5 3.5 Ghana, 2003 95 2.0 1.8 1.1 Cote d’Ivoire, 2005 97 3.4 5.3 0.64 * Because many African men are circumcised in their late teens, the table reports circumcision and HIV prevalence by circumcision status for men aged 20 years and above. These percentages are calculated from published data by subtracting data for men aged 15-19 years from data for all men. Depending on the country, data are for men aged 20 to 49, 54, or 59 years. The table includes all countries for which relevant data are available from published national surveys. Sources: See the Statistical Annex. From the late 1980s and continuing, some people have argued that lack of male circumcision – which may be a personal risk for men to acquire HIV infection – explains high HIV prevalence in some African communities.[xxxvii] A lot of evidence is inconsistent with this hypothesis (see Table 7.4). For example, Rwanda, with only 10 percent of men circumcised, has only 3 percent HIV prevalence in adults, and saw little epidemic growth from 1986 to 2005. Over the same period, adult HIV prevalence in Lesotho, with 59 percent of men circumcised, increased from 0 percent to 24 percent. Although most men in India, China, and Western Europe are uncircumcised, their HIV prevalence – even including MSMs and IDUs – is less than 0.5 percent. Finally, in 5 of 13 African countries with data from national surveys, HIV prevalence was higher in circumcised than in uncircumcised men (see Table 7.4). Considering the often 100-fold difference between HIV prevalence in non-IDU and non-MSM adults in generalized compared to concentrated epidemics, if sexual factors account for those differences, they should not be so hard to find. Money for research has not been a problem, nor has access to Africans willing to participate in research. From the mid-1980s to 2009, researchers looking for the risks that cause Africa’s HIV epidemics have followed tens of thousands of HIV-negative Africans for periods ranging from less than a year to more than 15 years, and have observed thousands of incident infections. Even so, researchers have been unable to identify sexual behaviors or conditions which distinguish African countries with the worst HIV epidemics from other African countries or from European countries with concentrated epidemics. Poor research methods -- notably, not working with research participants to trace the source of their infections -- have undermined efforts to explain generalized epidemics. Failing to explain high HIV prevalence in women In countries and communities with the worst generalized epidemics, HIV prevalence increases from low levels in women aged 15 years to reach a maximum in women in their late 20s to late 30s (Figure 7.1). In young women, high rates of HIV incidence boost HIV prevalence. However, high rates of incidence are also required to maintain high HIV prevalence in women aged over 25 years. Figure 7.1: HIV prevalence in women by age in Southern Africa Sources: See the Statistical Annex. Consider what happens to women in Lesotho, where a national survey found HIV prevalence over 40 percent for women aged 25 to 39 years. Without treatment, approximately 4 percent of Lesothan women aged 25 to 39 years die of AIDS each year (calculating 10 percent annual mortality among the 40 percent who are HIV-positive). To maintain 40 percent prevalence, another 4 percent of women (or 7 percent of the 60 percent who are HIV-negative) must be newly infected each year. In other words, approximately 7 percent of susceptible (HIV-negative) women aged 25 to 39 years acquire HIV infections each year – a rate that may well be higher than for younger women. In short, women in the worst generalized epidemics acquire HIV infections at high rates from their late teens at least through their 30s. Moreover, appreciable levels of HIV prevalence – and incidence – continue in older women.[xxxviii] A recent study in Gondar, Ethiopia, found 4.7 percent HIV prevalence among women aged 50 to more than 70 years, including two HIV-positive women aged 70 years who had been widowed for 11 years.[xxxix] HIV prevalence in older women in this study exceeded the 1.9 percent prevalence for women aged 15 to 49 years in Ethiopia’s 2005 national survey. Because there are a lot of HIV-positive men in generalized epidemics, many women acquire HIV from sexual partners. But sex is not necessarily the whole story. Limited sexual risks in young women Women’s sexual risks vary over their lifetime. Before they are married, women are at risk from casual partners, some of whom may become spouses or cohabiting partners. In the worst generalized epidemics, young women who report few sexual partners are nevertheless at high risk for infection. For example, in Carletonville, South Africa, in 1999, sexually active women aged 16-18 years reported an average of 1.7 sexual partners in their life (almost all casual), and few sexual contacts per partnership – yet 21 percent were HIV-positive.[xl] Similarly, in Kisumu, Kenya, in 1997-98, 20 percent of unmarried women less than 20 years old who reported only one lifetime sexual partner were HIV-positive.[xli] Various hypotheses have been proposed to explain how the limited sexual activity reported by young women in many African communities could account for their observed high rates of HIV prevalence. One is that women have sex with older men, who are more likely to be HIV-positive than younger men. Another is that younger vs. older women have much greater biological susceptibility to sexual acquisition of HIV. None of these hypotheses has been rigorously tested by tracing casual partners that are alleged to infect young women. Also, the challenge to understand generalized epidemics is to explain high incidence in women at least through their 30s, not only in young women. Limited sexual risks in older women Between the ages of 25 and 49 years, most women in Africa and in other countries with generalized epidemics are married, and most married women report no non-spousal partners. Nevertheless, in 14 of 24 countries with generalized epidemics and with available data from national surveys, more than half of HIV-positive married women aged 15 to 49 years had HIV-negative husbands (Table 7.5). Because HIV transmission can go both ways, some women with HIV-positive husbands no doubt infected their husbands, rather than the other way around. Furthermore, even when both partners are HIV-positive, wives and husbands may have acquired their infections from different outside sources. Studies in Uganda and Zambia that sequenced HIV from couples in which both partners were HIV-positive found dissimilar HIV and therefore unlinked infections in 9 percent and 13 percent of couples, respectively. And a study in Malawi found that as many as 33 percent of concordant HIV-positive couples had dissimilar HIV and possibly unlinked infections.[xlii] Table 7.5: HIV infection in couples in countries with generalized epidemics* Country HIV in couples (% of couples) % of married HIV-positive women with HIV-negative partners Both HIV-positive Wife only HIV-positive Husband only HIV-positive Africa Benin, 2006 0.2 0.9 0.9 82 Burkina Faso, 2003 0.3 0.7 0.7 70 Cameroon, 2004 2.4 2.7 2.4 53 Cote d’Ivoire, 2005 1.4 3.7 2.3 73 DRC, 2007 0.2 1.1 0.6 85 Ethiopia, 2005 0.3 1.0 0.8 77 Ghana, 2003 1.0 1.5 1.6 60 Guinea, 2005 0.4 0.7 1.0 64 Kenya, 2003 3.7 4.6 2.8 55 Lesotho, 2004 20.2 4.5 8.9 18 Liberia, 2007 0.3 1.2 0.7 80 Malawi, 2004 7.0 4.0 5.7 36 Mali, 2006 0.4 0.8 0.3 67 Niger, 2006 0.2 0.4 0.6 67 Rwanda, 2005 1.7 0.8 1.4 32 Swaziland, 2006-07 28.8 8.7 7.7 23 Tanzania, 2007-08 2.5 2.8 3.5 53 Uganda, 2004-05 3.4 1.8 2.8 35 Zambia, 2007 8.0 4.6 6.6 37 Zimbabwe, 2005-06 14.7 5.2 8.1 26 Asia and the Caribbean Dominican Rep, 2007 0.4 0.4 0.4 50 Cambodia, 2005-06 0.5 0.1 0.4 17 Haiti, 2005 1.5 1.2 2.0 44 India, 2005-06 0.11 0.07 0.32 39 * All countries for which data are available from national surveys. Sources: See the Statistical Annex. A recent World Bank paper interprets the high proportion of HIV-positive wives with HIV-negative husbands in national surveys in Africa as evidence that ‘extramarital sexual activity among cohabiting women…is a substantial source of vulnerability to HIV,’ and that ‘self-reported sexual behaviors are not very reliable.’[xliii] Some women no doubt misreport the number of their sexual partners. But to simply assume and assert that HIV-positive women with HIV-negative partners acquired their infections from extramarital liaisons and then lied about it is not only bad science, but also dangerous for women. What the World Bank has done in publishing such unsupported allegations is equivalent to the town gossip and troublemaker telling husbands – without evidence – that their wives are fooling around. Both the popular and the scholarly AIDS literature are full of anecdotes of philandering HIV-positive husbands, poverty-driven sex work, and sugar-daddies. But these anecdotes do not describe the reality for most HIV-positive women in generalized epidemics. The ‘average’ HIV-positive woman has had few pre-marital partners and few or no extra-marital partners, has had a sufficiently high social status that she was not driven to trade sex for favors, and has – often – an HIV-negative husband. What’s missing? From hypothesis to stigma In 1987, Jonathan Mann distinguished three epidemics related to HIV. The first was the spread of HIV infection. The second was the spread of AIDS disease in persons infected with HIV. The third epidemic was the ‘denial, blame, stigmatization, prejudice and discrimination which the fear of AIDS brings out in individuals and societies.’[xliv] In Africa and later in other countries with generalized epidemics, HIV prevention messages that attributed almost all HIV infections in adults to sex – messages which grew out of the hypothesis that African promiscuity caused generalized epidemics – spread this third epidemic. Such messages ‘educated’ the public to see HIV infection as a sign – stigma – of sexual promiscuity. In effect, these HIV prevention messages translated racial stereotypes of sexual behavior into stigma against HIV-positive men and women. Stigma and limited testing obstruct public knowledge of the epidemic Until well into the 1990s, the AIDS epidemic was invisible to most Africans. In the late 1980s, less than 1 percent of adults were HIV-positive in most communities. Thus, even in communities where HIV prevalence soared over 10 percent in the 1990s, annual deaths from AIDS often did not reach 1 in 100 adults until the early 21st century. Besides, many AIDS-related deaths could be attributed to other causes. During the 1990s, testing to tell people if they were or were not HIV-positive was not a priority in international AIDS programs. When an article in Lancet proposed home-based testing to make it easier for people in developing countries to learn their HIV status,[xlv] WHO’s experts objected, arguing that there was no evidence telling people their HIV status would reduce transmission, and that no care was available, so ‘the only promise offered here is the potential rejection of the HIV-positive person.’[xlvi] During the 1990s, getting an HIV test was onerous and/or expensive for most Africans. In a review of HIV testing services in 21 African countries in 2001, only seven countries reported more than 20 government testing sites, and only five reported any testing in the private sector.[xlvii] As of 2000, Piot, the executive director of UNAIDS, estimated that only 5 percent of HIV-positive people in developing countries were aware of their infection, and judged that ‘In Africa there is basically only one country where access to testing and counselling is reasonable, and that is Uganda.’[xlviii] For people in generalized epidemics, the best information they had during the 1990s that HIV was spreading through their communities were reports from sentinel surveys that tested pregnant women in antenatal clinics. But because these surveys disconnected blood samples from names before testing for HIV, no one knew who was infected. Thus, even as governments reported HIV prevalence soaring among women at antenatal clinics, people looked at their own and their spouses’ sexual behavior, and supposed that others – sex workers, clients, bad people – were the ones who were infected. For example, in a 2000-01 study among Zambian women who did not know their HIV status, more than half the women who were HIV-positive considered themselves to be at no or low risk for HIV infection.[xlix] The belief that sexual exposures accounted for most HIV infections and the stigma that linked HIV to sexual misbehavior were mutually reinforcing. People who had no sexual risks were unlikely to seek HIV tests. Most people who found themselves to be HIV-positive – with or without sexual risks – tried to hide their infections. However, people with recognized sexual risks, such as sex workers and widows of men who had died from AIDS, were less able to do so. Public awareness of AIDS in people with recognized sexual risks supported the view that all HIV came from sex. Even for counselors and doctors who saw and interviewed HIV-positive people, the belief that HIV infection in adults was a sign of sexual behavior often limited what they could see. For example, doctors and counselors interviewed during a study in India in 2005 explained, ‘Men are like that, they go out and then come home and infect their wives; how can we believe when they tell us that they have not had sex outside marriage?’ and ‘He is a truck driver, what can you expect?’[l] Misinformation drives stigma Discrimination against HIV-positive people is due in part to mistaken fears that the disease may spread through casual contact – such as sharing eating utensils – and in part to aversion to serious illness from any cause. But an important contributor to discrimination is the belief that almost all HIV infections in adults in countries with generalized epidemics come from sex. Of course, people must be warned about sexual risks – the problem was the lack of attention to other risks, including especially risks in ‘virtuous’ behaviors such as seeking healthcare or dental care. Because so few people knew they were infected, and because stigma discouraged even those few from talking about their condition, the public knew very little about what was happening from personal experience. Even after tens of millions had been infected, and millions had died, the public’s ideas about the presence of AIDS in their communities, and of how HIV was spreading, depended almost entirely on what public health authorities told them. In this situation, if health authorities did not, either deliberately or inadvertently, provide full and accurate information, what people believed about HIV could wander far from reality. Many organizations have tried to fight stigma by encouraging people not to be so critical of those who are promiscuous, which is both controversial and difficult. Another more effective and accurate way to defuse stigma is to repeatedly and persistently draw attention to children and adults with HIV from unsafe healthcare, and to warn people about such risks. In this way, people will come to see that an HIV infection is not a reliable sign of sexual exposure to HIV. Some AIDS experts have obstructed such messages, arguing that public discussion of iatrogenic transmission will ‘detract from prevention efforts aimed at reducing the sexual transmission of HIV’[li] and lead to ‘behavioral disinhibition.’[lii] These arguments reflect negative perceptions of peoples’ intelligence and sexual behavior – that they cannot keep two risks in mind at the same time, and that they will use any excuse to be sexually promiscuous without condoms. For health experts, these arguments are also a self-serving excuse not to acknowledge nosocomial infections, and thereby to violate medical ethics by not warning people about risks in health care (see Chapter 9). Extending a metaphor AIDS experts in Africa have been like traffic safety experts who persistently analyze accidents with the limiting assumption that all traffic on a two-way street comes exclusively from one direction. After decades, such traffic safety experts are still arguing and hypothesizing about why some intersections are many times more dangerous than others, and are still refusing to take a good look at how much traffic might be coming from the other direction. Single-minded attention to sex in HIV research contributes to single-minded attention to sex in HIV prevention messages. These messages – supported by billions of dollars in foreign aid – promote the stigmatizing assumption that an adult’s HIV infection is a reliable sign of sexual exposure. [i] ‘Constitution of the World Health Organization.’ Bull WHO 2002; 80: 984. [ii] Stillwagon E. AIDS and the Ecology of Poverty. Oxford: Oxford University Press, 2006. p. 135. [iii] Rushton JP, Bogaert AF. ’Population differences in susceptibility to AIDS: An evolutionary analysis’, Soc Sci Med, 1989, 28: 1211-20. [iv] Cleland J, Ferry B, Carael M. ‘Summary and conclusions’, in Cleland J, Ferry B (eds). Sexual behavior and AIDS in the developing world. Geneva: WHO, 1995, pp. 208-28. p. 211. [v] Packard RM, Epstein P. ‘Epidemiologists, social scientists, and the structure of medical research on AIDS in Africa’, Soc Sci Med, 1991, 33: 771-83. p. 781. [vi] Wellings K, Collumbien M, Slaymaker E, et al. ‘Sexual behavior in context: A global perspective’, Lancet, 2006, 368: 1706-28. p. 1723. [vii] Chin J. The AIDS Pandemic: The collision of epidemiology with political correctness. Abingdon, UK: Radcliffe, 2007. pp 146-7. [viii] Public Health Service (PHS). ‘Policy on informing those tested about HIV serostatus.’ Washington, DC: PHS, 1988. Available at: http://www.hhs.gov/ohrp/humansubjects/guidance/hsdc88jun.htm (accessed 9 September 2007). [ix] Allen SA, Karita E, N’gandu N, et al. ‘The evolution of voluntary testing and counseling as an HIV prevention strategy’, in Gibney L, DiClemente RJ, Vermund SH, (eds). Preventing HIV in Developing Countries: Biomedical and behavioral approaches. New York: Kluwer Academic, 1999. pp. 87-108. p. 103. [x] Gray RH, Wawer MJ, Brookmeyer R, et al. ‘Probability of HIV-1 transmission per coital act in monogamous, heterosexual, HIV-1 discordant couples in Rakai, Uganda’, Lancet, 2001, 357: 1149-53. p. 1152. [xi] Quinn TC, Wawer MJ, Sewankambo N, et al. ‘Viral load and heterosexual transmission of human immunodeficiency virus type 1’, N Engl J Med, 2000, 342: 921-9. [xii] Hugonnet S, Mosha F, Todd J, et al. ‘Incidence of HIV infection in stable sexual partnerships: A retrospective cohort study of 1802 couples in Mwanza Region, Tanzania’, J Acquir Immune Defic Syndr, 2002, 30: 73-80. p. 77. [xiii] Humphrey JH, Iliff PJ, Marinda ET, et al. ‘Effects of a single large dose of vitamin A, given during the postpartum period to HIV-positive women and their infants, on child HIV infection, HIV-free survival, and mortality’, J Infect Dis, 2006, 193: 860-71; Marinda E, Humphrey JH, Iliff PJ, et al. ‘Child mortality according to maternal and infant HIV status in Zimbabwe’, Ped Infect Dis J, 2007, 26: 519-26. [xiv] Piwoz EG, Iliff PJ, Tavengwa N, et al. ‘An education and counseling program for preventing breast-feeding-associated HIV transmission in Zimbabwe: design and impact on maternal knowledge and behavior’, J Nutr, 2005, 135: 950-5. p. 951. [xv] Gray RH et al. ‘Probability of HIV-1 transmission per coital act’; Gray RH, Wabwire-Mangen F, Kigozi G, et al. ‘Randomized trial of presumptive sexually transmitted disease therapy during pregnancy in Rakai, Uganda’, Am J Obstet Gynecol, 2001, 185: 1209-17. [xvi] Hugonnet S et al. ‘Incidence of HIV infection in stable sexual partnerships’. [xvii] Humphrey JH et al. ‘Effects of a single large dose of vitamin A’. [xviii] Humphrey JH et al. ‘Effects of a single large dose of vitamin A’. [xix] ‘Nuremberg Code.’ Available from: http://www.hhs.gov/ohrp/irb/irb_appendices.htm#j5 (accessed 9 September 2007). [xx] ‘World Medical Association Declaration of Helsinki.’ Available from: www.wma.net/e/policy/b3.htm (accessed 9 September 2007). [xxi] Gavin L, Galavotti C, Dube H, et al. ‘Factors associated with HIV infection in adolescent females in Zimbabwe’, J Adolesc Health, 2006, 39: 596.e11-18. [xxii] Rehle T, Shisana O, Pillay V, et al. ‘National HIV incidence measures – New insights into the South African epidemic’, S Afr Med J, 2007, 97: 194-9. [xxiii] Lopman BA, Garnett GP, Mason PR, et al. ‘Individual level injection history: A lack of association with HIV incidence in rural Zimbabwe’, PLoS Med, 2005, 2(2): e37. [xxiv] Rehle T et al. ‘National HIV incidence measures’. [xxv] Allen S, Tice J, Van de Perre P, et al. ‘Effect of serotesting with counselling on condom use and seroconversion among HIV discordant couples in Africa’, BMJ, 1992, 304: 1605-9; Lopman BA et al. ‘Individual level injection history’. [xxvi] Gray RH, Li X, Kigozi G, et al. ‘Increased risk of incident HIV during pregnancy in Rakai, Uganda: a prospective study’, Lancet, 2005, 366: 1182-8. [xxvii] Gray RH et al. ‘Randomized trial of presumptive sexually transmitted disease therapy’. [xxviii] Auvert B, Taljaard D, Lagarde E, et al. ‘Randomized, controlled intervention trial of male circumcision for reduction of HIV infection risk: The ANRS 1265 trial’, PLoS Med, 2005, 2: e298. [xxix] Gray RH, Kigozi G, Serwadda D, et al. ‘Male circumcision for HIV prevention in men in Rakai, Uganda: a randomized trial’, Lancet, 2007, 369: 657-66. [xxx] Bailey RC, Moses S, Parkere CB, et al. ‘Male circumcision for HIV prevention in young men in Kisumu, Kenya: a randomised controlled trial’, Lancet, 2007, 369: 643-56. [xxxi] Mahiane S-G, Legeai C, Taljaard D, et al. ‘Transmission probabilities of HIV and herpes simplex virus type 2, effect of male circumcision and interaction: a longitudinal study in a township of South Africa’, AIDS 2009; 23: 377-383. [xxxii] CDC. ‘Antiretroviral postexposure prophylaxis after sexual, injection drug-use, or other nonoccupational exposure to HIV in the United States: Recommendations from the US Department of Health and Human Services’, MMWR, 2005, 54 (No. RR-2): 1-20; Gray RH et al. ‘Probability of HIV-1 transmission per coital act’. [xxxiii] Gisselquist D, Potterat JJ. ‘Heterosexual transmission of HIV in Africa: An empiric estimate’, Int J STD AIDS, 2003, 14: 162-73. [xxxiv] Wawer MJ, Sewankambo NK, Serwadda D, et al. ‘Control of sexually transmitted diseases for AIDS prevention in Uganda: A randomized community trial’, Lancet, 1999, 353: 525-535; Kamali A, Quigley M, Nakiyingi J, et al. ‘Syndromic management of sexually-transmitted infections and behaviour change interventions on transmission of HIV-1 in rural Uganda: a community randomized trial’, Lancet, 2003, 361: 645-52; Gisselquist D, Potterat JJ, Brody S. ‘Running on empty: Sexual co-factors are insufficient to fuel Africa’s turbo-charged HIV epidemic’, Int J STD AIDS, 2004, 15: 442-52. [xxxv] Epstein H. The Invisible Cure. New York: Farrar, Straus and Giroux, 2007; Chin J. The AIDS Pandemic. [xxxvi] Lagarde L, Auvert B, Carael M, et al. ‘Concurrent sexual partnerships and HIV prevalence in five urban communities of sub-Saharan Africa’, AIDS, 2001, 15: 877-84. Mishra V, Bignami-Van Assche S. Concurrent Sexual Partnerships and HIV Infection: evidence from national population-based surveys. DHS Working Papers No. 62. Calverton, Maryland: Macro International Inc.: 2009. [xxxvii] Bongaarts J, Reining P, Way P, et al. ‘The relationship between male circumcision and HIV infection in African populations’, AIDS, 1989, 3: 373-7; Moses S, Bradley JE, Nagelkerke NJD, et al. ‘Geographical patterns of male circumcision practices in Africa: Association with HIV seroprevalence’, Int J Epidemiol, 1990, 19: 693-7. [xxxviii] Schmid GP, Williams BG, Garcia-Calleja JM, et al. ‘The unexplored story of HIV and ageing’. Bull WHO, 2009, 87: 162-3. [xxxix] Kassu A, Mekonnen A, Bekele A, et al. ‘HIV and syphilis infection among elderly people in northwest Ethiopia’, Jpn J Infect Dis, 2004, 57: 264-7. [xl] Auvert B, Ballard R, Campbell C, et al. ‘HIV infection among youth in a South African mining town is associated with herpes simplex virus-2 seropositivity and sexual behaviour’, AIDS, 2001, 15: 885-98. [xli] Glynn JR, Carael M, Auvert B, et al. ‘Why do young women have a much higher prevalence of HIV than young men? A study in Kisumu, Kenya and Ndola, Zambia, AIDS, 2001, 15 (suppl 4): S51-60. [xlii] Wawer MJ, Gray RH, Sewankambo NK, et al. ‘Rates of HV-1 transmission per coital act, by stage of infection, in Rakai, Uganda’. J Infect Dis, 2005, 191: 1403-9; Fideli US, Allen SA, Musonda R, et al. ‘Virologic and immunologic determinants of heterosexual transmission of human immunodeficiency virus type 1 in Africa’, AIDS Res Hum Retroviruses, 2001, 17: 901-10; McCormack GP, Glynn JR, Crampin AC, et al. ‘Early evolution of the human immunodeficiency virus type 1 subtype C epidemic in rural Malawi’, J Virol, 2002, 76: 12890-9. [xliii] de Walque D. ‘Discordant couples: HIV infection among couples in Burkina Faso, Cameroon, Ghana, Kenya, and Tanzania’, World Bank Policy Research Working Paper 3956. Washington DC: World Bank, 2006. pp. 1, 18. [xliv] Panos Institute. The 3rd Epidemic: Repercussions of the Fear of AIDS. London: Panos Publications, 1990. p. i. [xlv] Frerichs RR. ‘Personal screening for HIV in developing countries’, Lancet, 1994, 343: 960-2. [xlvi] Mertens TE, Smith GD, Van Praag E. ‘Home testing for HIV [letter]’, Lancet, 1994, 343: 1293. [xlvii] WHO. The Health Sector Response to HIV/AIDS: Coverage of selected services in 2001. Geneva: WHO, 2002. [xlviii] Great Britain, House of Commons (Session 2000-2001), International Development Committee. Third Report, HIV/AIDS: The impact on social and economic development, vol. 2 (HC 354-II). London: House of Commons, 2001. Evidence of Peter Piot on 18 July 2000. [xlix] Stringer EM, Sinkala M, Kumwenda R, et al. ‘Personal risk perception, HIV knowledge and risk avoidance behavior, and their relationships to actual HIV serostatus in an urban African obstetric population’, J Acquir Immune Defic Syndr, 2004, 35: 60-6. [l] Correa M, Gisselquist D. HIV from Blood Exposures in India – An exploratory study. Colombo: Norwegian Church Aid, 2005. p. 51. [li] Garnett GP, Fraser C. ‘Let it be sexual – Selection, aggregation and distortion used to construct a case against sexual transmission [letter]’, Int J STD AIDS, 2003, 14: 782-4. p. 782. [lii] Gray R, Thoma M, Kiwanuka N, et al. ‘HIV transmission through health care in sub-Saharan Africa, authors’ replies [letter]’, Lancet, 2004, 364: 1666.