A New Nexus for HIV/AIDS Research

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Science  28 Jul 2006:
Vol. 313, Issue 5786, pp. 488-490
DOI: 10.1126/science.313.5786.488

Talented investigators and explosive spread in men who have sex with men have made this country a hot spot for clinical studies

LIMA, IQUITOS, AND NAUTA, PERU—On a Friday night this June at a gay disco in Iquitos, a jungle city that's the jump-off point for touring the Amazon rainforest, drag queens danced to the thump of “Voulez-vous coucher avec moi?” in a Miss Adonis contest. The event, staged by the Asociación Civil Selva Amazónica, was part entertainment, part HIV prevention, and part recruitment for an AIDS vaccine trial.

Recruiting station.

“Lashmi” leads a teach-in about drag queens that doubles as an attempt to find volunteers for an AIDS vaccine trial.

Welcome to Peru, a somewhat incongruous hotbed of HIV/AIDS research. “Everyone's going to Peru, and it's not because they have a huge epidemic,” says Robert Grant, a virologist at the University of California, San Francisco (UCSF), who runs one of many collaborative projects now under way. “It's because of the research climate.”

Intensive efforts are now under way to understand the country's perplexing epidemiology—the epidemic is concentrated among men who have sex with men (MSM) and has not “bridged” much to other groups—and to evaluate new treatment and prevention strategies. The scope and scale of the research enterprise is especially remarkable given the government's foot-dragging when it comes to offering anti-HIV drugs to people who need them (see sidebar).

Only 0.6% of Peruvian adults were infected with HIV by the end of 2005, according to the Joint United Nations Programme on HIV/AIDS (UNAIDS). But studies suggest that the prevalence in Peruvian MSM—a group that includes many bisexuals who consider themselves heterosexual—is 10% in Iquitos and the surrounding area and more than twice as high in Lima. It's on this group that researchers have focused their attention. “It's a very concentrated epidemic, and we have a very good relationship with the community,” explains epidemiologist Jorge Sánchez, who runs Asociación Civil Impacta Salud y Educación (Impacta), a nongovernmental organization based in Lima.

Similarly, Carlos Cáceres, an epidemiologist at the Universidad Peruana Cayetano Heredia in Lima, has a team of AIDS researchers working closely with high-risk communities to evaluate behavioral interventions, viral spread, and strategies to reduce stigma and discrimination. “There's a lot to be studied here,” says Cáceres.

Both Sánchez's and Cáceres's groups have strong ties to U.S. academics, participate in international multisite studies, and receive substantial funding from the U.S. National Institutes of Health (NIH). A challenge, says Cáceres, is ensuring that such collaborations serve both Peru's own interests and those of the funder.

Why Peru?

Many factors have contributed to Peru becoming a nexus of collaborative HIV/AIDS research, but explanations usually return to Sánchez and Cáceres. “There are great people here,” says Rubén Mayorga, the Lima-based UNAIDS country coordinator. “And there's an acknowledgment that HIV is a big problem among gay men or men who have sex with men.”

Sánchez and Cáceres—who, to the frustration of many, have a strained relationship—command wide respect from colleagues around the world. Sánchez was the first of some 40 Peruvian researchers who were funded by NIH's Fogarty International Center to train at the University of Washington (UW), Seattle, with King Holmes, a renowned expert on sexually transmitted diseases. Sánchez then headed Peru's national AIDS program within the Ministry of Health. When he left, he took many members of his team and started Impacta. His group now collaborates with both UW and Grant's lab at UCSF. Cáceres has a doctorate in public health from UC Berkeley and works closely with Thomas Coates's AIDS research team at UC Los Angeles.

Mayorga says Sánchez and Cáceres have a deep understanding of the communities that they are studying because they are both part of them. “I know exactly what it means to have a partner who weighs 40 kilos and you need to take him to shower because he cannot shower himself,” says Sánchez, who had a partner die of AIDS in 1990. “I cannot take my personal life out of my thinking.” Cáceres, too, says his personal links to the community shape the way he does epidemiology. “It's public health and prevention mixed with sexual rights and human rights and empowering the community,” he says.

Epidemiologist Javier Lama, a co-investigator with the NIH-sponsored HIV Vaccine Trials Network, says Peru is particularly poised to do prevention studies because of the high incidence, or rate of new infections, in MSM. Such high incidence rates, ranging from 3.5% in Iquitos to 6.2% in Lima, enable researchers to discern whether a prevention intervention works with relatively smaller, shorter trials than would be needed in locales with, say, 1% incidence.

Grant is now working with Lama, Sánchez, and other Impacta researchers to launch one of the most ambitious—and contentious—prevention studies in the world: an evaluation of whether antiretroviral drugs used to treat infection can lower transmission rates if uninfected people take them each day. Four studies of so-called pre-exposure prophylaxis (PrEP) have been blocked or aborted in Africa and Asia because of community protests about trial designs as well as problems with data quality. But Grant is confident that the placebo-controlled trial—which is slated to start in November and will test a combination of the anti-HIV drugs tenofovir and FTC in 1400 Peruvian and Ecuadorian MSM—will fly. “The advantage of working here is they have a mobilized population,” says Grant. He says Peru also has a proven track record of quickly enrolling volunteers.

In addition to the PrEP study and trials of experimental AIDS vaccines, Impacta is also playing a leading role in two multicountry studies that are evaluating whether the drug acyclovir can help people infected with herpes simplex virus 2 avoid acquiring or transmitting HIV. Impacta is part of an NIH network that tests new HIV treatments, too.

Cáceres and his co-workers spend about half their effort on a multicountry behavioral study funded by the U.S. National Institute of Mental Health that's testing “diffusion of innovation” theory. The researchers identify popular opinion leaders in various poor neighborhoods, educate them about HIV prevention, and then assess whether that intervention helps lower HIV incidence in the community. This team also has a study under way to gauge whether art can reduce stigma and discrimination against HIV-infected people. On World AIDS Day last year, they distributed T-shirts made by artists to all the staff and patients at three Lima hospitals. The T-shirts had messages on them that, roughly translated, said all of us are living with HIV.

Why mainly MSM?

Although all Peruvians may be living with the HIV epidemic, the virus has not made many inroads outside the MSM population. Female sex workers, for example, have a prevalence of less than 2% in Lima, and a 2002 study of nearly 4500 sex workers from 24 smaller cities found a prevalence of only 0.62%. The prevalence in women in general is a mere 0.2%

These findings might suggest that few MSM have sex with women, but that's not the case. “A big part of the MSM community is married,” says UNAIDS's Mayorga. Indeed, a survey, now in press, of more than 4000 MSM between 1996 and 2002 in Peru found that in one year, 47% of the men reported having had sex with a woman.

Leading lights.

Carlos Cáceres (left) and Jorge Sánchez run two separate HIV/AIDS research programs in collaboration with U.S. research teams.

Cáceres suggests that the heterosexual epidemic has not taken off in part because monogamy is the norm in the Peruvian women who become infected by bisexual partners. Says Cáceres, “The epidemic stops in them and doesn't spread.” He notes, too, that Peru has no injecting drug use, which in other countries is another way that the epidemic commonly bridges into heterosexual women. Sánchez says “of course it surprises me” that more women are not infected, but his work suggests that bisexual men, because of their sexual practices (typically “insertive” rather than “receptive” in anal sex), have a lower HIV prevalence than that of men who exclusively have male partners.

Net gains

A team from Selva Amazónica recently drove a few hours to the town of Nauta to attend a volleyball game. In Peru, volleyball has long had the reputation of being a sport for gay men—macho men play soccer—and the Selva Amazónica team wanted to see whether they might recruit volunteers for one of Impacta's prevention trials.

Although gay men once feared playing volleyball in public, onlookers filled the town square in Nauta to watch two teams spike the net in the sweltering Amazonian sun. “The environment for gay people in Peru has markedly changed in the last 5 years, and it's really because of the way the AIDS epidemic has been addressed,” said Grant, who had come along for the ride. So far, in Nauta, however, AIDS has not had much impact: The head of the town's gay organization says he does not know anyone here who has died from the disease or is even infected.

Net gain.

Volleyball games like this one in Nauta are popular hangouts for gay men, making them key sites for HIV/AIDS researchers who do prevention work and stage clinical trials.

Then again, Nauta has all the ingredients needed for HIV to take off. The only place to buy condoms this day is the town's hospital, which gives them away for family planning but charges everyone else. No one offers HIV tests. And judging by the turnout at the volleyball game, there's a substantial MSM population.

All of which explains why Selva Amazónica came here—and why Peru is so enthusiastic about research. Anyone who joins the group's studies receives free condoms, HIV tests, counseling, checkups, and education. And that means that the abundance of HIV/AIDS research here may have a huge payoff, regardless of whether the trials ultimately yield positive results.

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