Botswana seems an unlikely place for an AIDS epidemic. Vast and underpopulated, it is largely free of the teeming slums, war zones, and inner-city drug cultures that epidemiologists say are typical niches for the human immunodeficiency virus. Botswana is an African paradise. Shortly after gaining its independence from Britain in 1966, large diamond reserves were discovered, and the economy has since grown faster — and for longer — than that of virtually any other nation in the world. Education is free, corruption is rare, crime rates are low, and the nation has never been at war. Citizens are loyal: A visitor quickly learns that even mild criticism of anything related to Botswana is considered impolite. Yet this country, with all these advantages, has the highest HIV-infection rate in the world.
The virus has spread extremely rapidly in Botswana. Two decades ago, virtually no one there was HIV-positive. By 1992 an estimated 20 percent of sexually active adults were infected. By 1995 that proportion had reached one-third, and today it is roughly 40 percent. In Francistown, Botswana’s second largest city, nearly half of all pregnant women in the main hospital test positive for HIV. The picture in the rest of sub-Saharan Africa is nearly as dire. AIDS has killed Zulu nurses in South Africa, Masai teachers in Tanzania, Kikuyu housewives in Kenya, Pygmy elders in Uganda. HIV infection rates range from around 6 percent in Uganda to 39 percent in Swaziland.
Such numbers are astronomical compared with most of the world. In the United States, less than 1 percent of the population is infected; in Russia and India the figure hovers around 1 percent. Even in Thailand, with its thriving sex and drug trades, the proportion of infected barely exceeds 2 percent.
The high rates come despite efforts in many communities to stem the HIV epidemic through educational programs, condom distribution, and treatment for such sexually transmitted diseases as gonorrhea and syphilis, which create genital sores and ulcers that make it easier for the virus to spread. In most cases these programs have had little effect. The growing disaster has forced AIDS experts to reconsider old theories about how HIV spreads in Africa.
Outside of sub-Saharan Africa, many HIV-positive people are injecting drug users, prostitutes, and highly promiscuous homosexual men who may have hundreds of different sexual partners every year. But most Africans with HIV claim never to use drugs, engage in prostitution, or have large numbers of sexual partners. To explain the high infection rates, scientists have advanced theories ranging from nutritional deficiencies to more virulent HIV strains to different sexual customs. In the 1980s Australian demographer John Caldwell insisted that the virus was spreading rapidly in Africa simply because people there tended to have more sexual partners than people elsewhere. He pointed to the cultural desire for many children, the tradition of polygamy, and other aspects of African society that contributed to a greater tolerance of promiscuous behavior than in the West. Caldwell’s views sparked controversy and for years received little attention. Recently, though, some experts, including epidemiologist James Chin of the University of California at Berkeley, have revisited the theory. Chin believes it’s the only possible explanation: “People tell me not to say it, but I strongly believe it.”
Some studies do show that Africans have more — but not vastly more — sexual partners, on average, than people in Western countries. For example, a study of sexual behavior in Zimbabwe, where roughly 33 percent of adults are HIV-positive, found that in a single year, most people have between one and three sexual partners. Of course, prostitutes in Zimbabwe may have more than 100 partners a year, just as prostitutes elsewhere in the world do, but most HIV-positive Zimbabweans are not prostitutes.
In the early 1990s, Martina Morris, then a member of the sociology and public-health departments at Columbia University (and now a professor of sociology and statistics at the University of Washington in Seattle), tried to solve the mystery of HIV in Africa mathematically. She had helped devise a computer program to predict the spread of HIV in a given population based on such factors as the number of sexual partners people had and the duration of those relationships. At the time, Uganda had one of the highest HIV-infection rates in the world, so she flew there in 1993 to gather data on sexual behavior.
“Just after I arrived in Uganda, I had to give a lecture to Ugandan doctors at the medical school in Kampala, telling them what I planned to do,” she recalls. “At the time there was talk in Uganda about helicopter scientists — whites from the United States and Europe who just parachuted in, took data, and didn’t work with local African experts. I was the only American woman in the room, and it was a tough audience. The HIV rate was estimated to be 18 percent at the time, and here I was trying to explain how mathematical models were going to help. They listened, and then at the end, one man raised his hand and asked, ‘Could your model handle more than one partner at a time?’ I said, ‘No.’ The man walked out. The others sat down with me and said I had to include concurrent partnerships in my model. Otherwise it would be irrelevant.”
The idea that long-term simultaneous partnerships might increase the spread of HIV was first proposed by British epidemiologists Robert May and Charlotte Watts in 1992. But Morris had not seen their article when she set out for Uganda in 1993, and her mathematical tools were not up to the complicated task of modeling multiple long-term partnerships anyway.
An added difficulty was that Morris would be asking Ugandans to answer intimate questions about their sexual behavior. So she replaced the impersonal language of standard questionnaires with a structured conversation. She asked the respondent whom he or she last had sex with, how the couple met, how long they had been together, whether they were still together, and so on. Then she asked about the respondent’s previous sexual partner. “Respondents love it, because it’s really like gossip,” Morris explains. “In a way, people are telling the story of their lives.”
Morris then conducted similar surveys in Thailand and the United States — with fascinating results. She found that the average Ugandan and the average American claimed roughly the same number of sexual partners in their lives. About 25 percent of people (of both sexes) in both countries said they had more than 10 partners in their lives. But similar rates of promiscuity did not result in similar rates of infection. The HIV rate in Uganda peaked at 18 percent in the early to mid-1990s but never exceeded 1 percent in the United States. And in Thailand, where many more men — 65 percent — reported 10 or more partners, the HIV rate barely rose above 2 percent.
A key difference between Uganda and Thailand, Morris found, is that men in Uganda often maintained two or more long-term sexual relationships at once. In Thailand, most men had only one long-term sexual relationship — with their wives. Half the Thai men in Morris’s survey said that they had sex with prostitutes but rarely the same one twice. On average they saw five prostitutes each year. Although many Thai prostitutes are HIV-positive, the men’s risk of infection was relatively low because Thai men generally had sex with each one only once.
The likelihood of contracting the virus during a single sexual act is believed to be quite low, between 1 in 100 and 1 in 1,000. So if an HIV-positive man has sex once with hundreds of different uninfected people, chances are he will infect only one of them. Generating an HIV epidemic such as Uganda’s probably requires that people be exposed to the virus repeatedly. As Morris discovered, Ugandan men and women had sex many times over many years with each of their partners. If one of those partners was HIV-positive, the relationship would prove very risky over time.
In the United States, Morris found a different pattern. Heterosexual Americans, like Ugandans, tend to have several long-term relationships, but they usually have them sequentially, not at the same time. If an American contracts HIV, she probably won’t pass it on right away, and if she eventually does, her new partner probably won’t pass it on right away either.
In 1993 Morris teamed up with mathematician Mirjam Kretzschmar of the National Institute of Public Health in Holland to develop a new computer program that could model simultaneous partnerships. So far she has run the program with data from Uganda, Thailand, and the United States, and the simulations reproduce the same prevalence of HIV observed in those countries in the early 1990s, when the data were collected.
Morris contends that Africans in ordinary heterosexual relationships are linked, not only to each other but also to the partners of their partners’ partners — and to the partners of those partners — via a web of sexual relationships extending across huge regions. If one member contracts HIV, then everyone else may too. Anti-AIDS campaigns warn against contact with prostitutes, but Morris says simultaneous long-term relationships are far more dangerous.
“The work she’s been doing is very exciting,” says Geoff Garnett, a professor of epidemiology at Imperial College London. He says the biology of the virus is probably similar everywhere, and differences in infection rates are most likely attributable to differences in sexual behavior. “I don’t think concurrency explains everything, but it is very interesting.”
Morris’s computer models do not consider that HIV-positive people are more likely to pass the virus on to others in the first few weeks or months following infection. The infectiousness of HIV varies with the concentration of the virus in the blood — the more virus there is, the more likely it will get into genital fluids and be passed on during sex. During the first few weeks and months after infection, a person’s blood teems with the virus. But then the immune system produces antibodies that attack HIV. Virus levels fall and may remain low for years, rising again when the person’s immune system eventually fails and AIDS symptoms appear. Some estimates suggest that a person who has been recently infected with HIV may be as much as 100 times more likely to transmit the virus to a partner than someone who has been infected for a long time. African-style simultaneous long-term relationships may therefore be even riskier than Morris’s models assume. If one member of a Ugandan sexual network becomes HIV-positive, the virus will spread very quickly to all other members of the network in a very short time.
One morning not long ago, I accompanied an HIV-prevention worker in Botswana named Willington Mongwa as he made his rounds in Old Naledi, a relatively poor neighborhood in the capital, Gaborone. We passed a bar in which about 15 people, most of them men, sat on tree stumps drinking beer made from distilled sorghum. I asked Willington if we could ask the drinkers some questions. We approached a group of three young men, and they offered us some of their beer and gratefully accepted the condoms we offered them. “How long will it take you to go through those?” I asked one man. “Let’s see, there are about 10 here, so it should take about 15 days.” I asked him how many girlfriends he had, and he told me he had three, one real girlfriend and two secret girlfriends. He had been seeing all three for at least two years. He used condoms with the secret girlfriends but not with the real one. How many secret boyfriends do those secret girlfriends have? I asked. He said he didn’t know, but you can never trust women, and that’s why he used condoms. And the real girlfriend? “As I said, you never know with women, but if she has other partners, I hope she uses condoms with them.”
Several other men I met had similar sexual arrangements. Most women I spoke to denied that they had partners other than their husbands or fiancés, but the men frankly assumed that women conducted their affairs much as they themselves did.
Botswana is a culture of migrants, where both men and women often spend time away from their homes and may have long-term relationships with different people in different places. The traditional form of wealth is cattle, which are kept on remote cattle posts. For centuries boys tended the cattle, and men visited the herds from time to time, leaving their wives behind. During colonial times, Botswana’s economy was tied to South Africa’s, and many men went to work in the mines and cities around Johannesburg. Since the 1980s, Botswana’s own urban centers have grown enormously, and the shuttling of both sexes between town and village has increased.
Even though Botswana is a relatively wealthy country by African standards, some 38 percent of the population is classified as poor. The government provides rations to the destitute, but many people told me they had experienced deprivation and unemployment. Women in Botswana generally work at low-wage jobs such as housecleaning, child care, or farming. As a result, girls and women are drawn into relationships with relatively wealthy men who help them and their families. These men may have several long-term female sexual partners at the same time — one or two in their home villages and one or two in town. Meanwhile, a woman may draw on more than one man to help pay her family’s bills.
Girls are particularly vulnerable. Roughly equal numbers of men and women in Botswana are HIV-positive, but the HIV rate is much higher among teenage girls than among teenage boys, although boys and girls become sexually active at roughly the same age. A study in 2001 found that 20 percent of girls in one region of Botswana had been asked by their teachers to have sex; half said they accepted, fearing lower grades if they said no.
Unlike many African countries, where government AIDS programs have been desultory, the Botswanan government is at war against the virus. Anti-AIDS banners are everywhere, and news about the epidemic appears daily in newspapers and on the radio and TV. Free condoms are available in remote clinics, bars, and shops. Botswana’s was the first African government to offer free treatment with antiretroviral drugs. The government has also funded a Danish-run program that employs field-workers to bring the message of HIV prevention to every household.
Despite these efforts, the HIV epidemic in Botswana shows few signs of abating. Harvard anthropologist Edward Green, who also serves on the Bush administration’s Presidential Advisory Council for HIV and AIDS and is the author of Rethinking AIDS Prevention, believes he knows why. Like many government AIDS programs in Africa, Botswana’s has been heavily influenced by Western donors, who have spent billions of dollars promoting condoms but have placed little emphasis on advising people to have fewer sexual partners. Studies show that even when used consistently, condoms fail to prevent infection 10 percent of the time, due to breakage and human error. In any case, most people do not use condoms every time they have sex but only with prostitutes and casual partners. Many people use them early in a long-term relationship but then dispense with them later on as a gesture of trust. But these long-term relationships are the very ones that Morris believes are the most risky.
The solution, says Green, is for people to limit themselves to one sexual partner. In Uganda, where the slogan of the government HIV prevention program in the 1980s and 1990s was “zero grazing,” HIV rates have fallen from 18 percent in 1993 to around 6 percent today. A report from the United States Agency for International Development says the number of men with casual sexual partners fell from 35 percent in 1989 to 15 percent.
Other governments, including Botswana’s, have begun campaigns like Uganda’s, with mixed results. Why haven’t these campaigns been more successful? In many places where HIV rates have fallen, widespread behavioral change has been accompanied by extraordinary activism. In the early 1990s, there was a vibrant movement devoted to the fight against AIDS. Hundreds of community-based organizations and activist groups had sprung up, most run by women. Uganda has Africa’s oldest, most vigorous women’s movement, dating back to the 1940s. In the 1980s, activist women made AIDS part of their struggle, which added enormous momentum to the government’s zero-grazing campaign. In many respects, the fight against AIDS in Uganda resembles the fight against AIDS in the United States in the 1980s, when gay men came to see the struggle against HIV as part of the struggle for gay rights. As the movement gained strength, the HIV rate among these men rapidly declined, just as in Uganda.
Botswana’s women’s movement is only 20 years old. The government is listening to women as never before, but much remains to be done to improve the everyday lives of women at risk for HIV. Traditions of protest are weak in Botswana. Fighting AIDS may depend on an anger that the women of this long-contented nation are only beginning to acquire.
Male Circumcision and HIV
For years researchers have puzzled over why most West African countries have lower HIV-infection rates than southern and East African countries. They thought it might have something to do with the Muslim religion, widely practiced in West Africa, which imposes restrictions on women’s sexual freedom. However, another likely factor is male circumcision, which is ritually practiced by Muslims and many others.
Several studies suggest that male circumcision protects both men and their sexual partners from HIV infection. This is not true of female circumcision, or female genital mutilation, which is extremely dangerous. In African countries where male circumcision is common, such as Senegal, Mali, Ghana, Benin, and the entire region of North Africa, HIV rates tend to be much lower than in countries such as Botswana, Malawi, and Swaziland. In countries with high rates of HIV, provinces and districts that have high rates of circumcision, such as Inhambane in Mozambique or Dar es Salaam in Tanzania, tend to have lower HIV rates.
Two African tribes with very high HIV-infection rates are the Zulu of South Africa and the Tswana of Botswana. Before colonial times, men in both tribes underwent circumcision rituals during adolescence. But when King Shaka united the Zulu tribe in the 1820s, he abolished the ritual, and when Christian missionaries settled in with the Tswana in the late 19th century, they declared circumcision a barbaric practice.
Circumcision removes mucosal tissue and cell types in the foreskin that contain special “receptors” for HIV. Some estimates suggest that circumcision may cut a man’s risk of contracting HIV by 70 percent. If true, this would mean that male circumcision may prove more effective than any of the HIV vaccines undergoing clinical trials. It would also be much cheaper, carry few side effects, and require no booster shots. Randomized, controlled trials of circumcision for HIV prevention are under way in South Africa, Kenya, and Uganda, and the results should be known within three years. — H.E.