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*

* 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

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*

* 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*

* 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 21^st 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.

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