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AIDS
The Soc ial Ecology of HIV/AIDS Kenneth Mayera,b,c,*, HF Pizerd, Kartik K Venkateshe KEYWORDS HIV AIDS Sexual activity Travel MSM Drug use
Although studying microbiology and immunology is essential to understanding the pathogenesis of infections caused by fungi, parasites, bacteria, viruses, and other microorganisms, the reasons that epidemics occur are largely a function of human behaviors and responses to environmental changes. The study of microbial-host interactions thus is the social ecology of infectious diseases, as it attempts to understand and describe the ways in which human activities alter specific microenvironments and thereby create favorable conditions for old and new microorganisms to develop and spread. Although potential pathogens adapt to specific niches as a function of their intrinsic properties, such as the ability to withstand heat, cold or drying, and their microenvironment, it is changes in human behavior that potentiate their spread. So although Yersinia pestis caused intermittent death in remote parts of Europe before the fourteenth century, it was the development of increasingly globalized commerce throughout the Mediterranean and Black Sea that enabled rats to carry the organism onboard ships and produce the infamous Black Death, which killed 20 to 30 million Europeans or approximately one third to two thirds of the population.1 The Spanish influenza epidemic of 1918–1919 was greatly abetted by the social disruptions of World War I, where large numbers of soldiers lived in densely crowded conditions at the front and then traveled to and from the battlefield carrying infectious diseases.2 Meanwhile, malnutrition, the dislocation of millions of displaced persons, and unsanitary living conditions provided additional supports for spreading the virus. In just a few years the flu virus spread around the world in three waves, killing an estimated 50 million people. In the late 1960s, prominent medical scientists and public health officials were predicting the end of infectious diseases as a significant public health concern and were
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Brown University, 164 Summit Avenue, Providence, RI 02906, USA Miriam Hospital, Providence, RI, USA c The Fenway Institute, Fenway Community Health, Boston, MA, USA d Health Care Strategies, Inc., 213 Hamilton Street, Cambridge, MA 02139, USA e Department of Community Health, Alpert Medical School, Brown University, Box G8488, Providence, RI 02912, USA * Corresponding author. Infectious Disease Division, Miriam Hospital, 164 Summit Avenue, Providence, RI 02906. E-mail address: [email protected] (K. Mayer). b
Med Clin N Am 92 (2008) 1363–1375 doi:10.1016/j.mcna.2008.06.003 medical.theclinics.com 0025-7125/08/$ – see front matter ª 2008 Elsevier Inc. All rights reserved.
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advising policy makers to shift funding, research, and training priorities away from infectious diseases to chronic medical conditions, such as cardiovascular disease and cancer.3 Although wrong in hindsight, the optimism of the time was understandable in light of the enormous strides being made in living standards and longevity, public sanitation and public health, vaccines, antibiotics, and other new medical technologies. These experts also predicted that the advances being attained in combating infectious diseases in developed nations soon would be translated to the developing ones. As events unfolded, the optimism was short-lived. Soon there was a resurgence of old infectious diseases that had been well controlled, such as tuberculosis,4–6 and an eruption of new ones, such as AIDS, legionnaires’ disease, Lyme disease, and Ebola hemorrhagic fever. A sobering lesson was learned: microbial pathogens have the extraordinary capacity to adapt to human lifestyles, including advances in medical science and technology. THE ADVENT OF THE AIDS PANDEMIC
In only approximately 25 years during the latter decades of the twentieth century, HIV-1, the most common human immunodeficiency virus that causes AIDS, spread throughout the world to infect more than 70 million people and cause approximately 35 million deaths.7 It is now the fourth leading cause of death worldwide and accounts for approximately 25% of deaths in Africa.8 HIV-1 is part of a class of viruses known as retroviruses discovered in the first decade of the twentieth century by Payton Rous, when he observed a filterable agent capable of causing sarcoma, a type of cancer that could be transmitted between chickens. Over subsequent decades researchers were able to detect many retroviruses in a diverse array of vertebrate species. Once genes were found to be comprised of DNA and the genetic code was deciphered, investigators began to categorize the ways in which these viruses replicate through infecting cells, integrating themselves into host cell genomes and then using the host cell’s nucleus to direct the infected cell to make new viral copies. A major contribution to the understanding of their pathogenesis was to characterize the enzyme, reverse transcriptase, which allows retroviruses to infect cells through their RNA and then integrate themselves into the host genome as a DNA provirus. In the late 1970s researchers discovered that the human T- lymphotropic virus (HTLV), also a retrovirus, could lie dormant in its host for decades. Like HIV-1, in a small subset of individuals HTLV can cause hematologic malignancies and neurologic diseases, such as spastic paraparesis.7,9 These discoveries were important for understanding AIDS when in 1980 and early 1981 clinicians in New York, Los Angeles, and San Francisco observed a new syndrome of opportunistic infections and atypical neoplasms, such as Kaposi’s sarcoma, a rare hematologic malignancy, in a small group of homosexual men who had been sexually active with multiple partners and injection drug users. Soon, a smaller group of patients who had hemophilia were identified who apparently had acquired the new disease from transfusions of contaminated blood products.10 For several years there was speculation that this new disease, soon to be named the acquired immunodeficiency syndrome (AIDS), was being caused by a retrovirus, because its pattern of transmission seemed similar to that of animal retroviruses and HTLV.7,11,12 Even before the AIDS virus was isolated in 1983, the clues to unraveling what was going on were found through careful epidemiologic sleuthing and observing the sociobehavioral factors associated with HIV transmission. Because of the lack of specimen repositories in many underdeveloped parts of the world, definitive conclusions about where and when epidemics originate often has
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remained indecipherable. Recent developments in computer technology data storage and evolutionary biology, however, have enabled molecular virologists to construct schema to pinpoint patterns of microbial evolution that can be associated with temporal sequences of viral transmission in different geographic areas. The collection of multiple samples of HIV from around the world with subsequent genetic sequencing have enabled molecular epidemiologists to estimate that HIV infection developed in a remote part of sub-Saharan Africa, possibly the Democratic Republic of the Congo.13 It is clear from more recent studies that viruses that are extremely similar to HIV have been found in this region in several primate species, in particular chimpanzees whose immune systems are most homologous to humans compared with other species. Additionally, anthropologic studies conducted in several regions of central and contiguous areas of sub-Saharan Africa have demonstrated that monkey meat is a major source of protein for indigenous peoples. Researchers have documented that the preparation of monkey meat by traditional butchering methods involves substantial contact with blood and sharp objects.14 Thus, it is not difficult to imagine that a simian retrovirus made the jump from primates to humans through the process of preparing meat for local consumption. Because it can take years before retroviruses, such as HIV, produce symptoms of infection, it was likely that some significant time passed during which infected individuals were freely passing the virus on to others. Whatever the actual start date and time sequence for the leap from primate to human (recent studies suggest that there were multiple introductions into the human population), by the 1970s there existed in rural Africa a sufficiently large number of people infected with HIV to lay the foundation for a much wider and long-lasting epidemic. It also is likely that the process developed as concurrent and overlapping multiple microepidemics, each of which was fueled by local social factors. In sub-Saharan Africa of the 1960s and 1970s there were substantial population migrations of men without their spouses and families that also served to propel the transmission of HIV. These men were moving from the countryside to the city or to mineral mines and labor camps looking for work. Throughout human history concentrations of young, mobile unattached men have set the stage for transactional sex and homosexuality, both of which served at this time to spread HIV in an unsuspecting population. Over time the men brought HIV and other sexually transmitted infections (STIs), which enhance the infectiousness of HIV, back to their communities when they returned home. HIV also spread along known truck routes where men engaged in transactional sex and by soldiers involved in the many armed conflicts that engulfed the region during those years. With extremely limited public health systems, no government-sponsored prevention messages, and limited access to condoms, the migrant populations and the sex workers that served them created an ideal social ecology for the spread of HIV. TRAVEL
How could an epidemic that was slowly brewing in sub-Saharan Africa become a global pandemic in just a few decades, especially since transmission of HIV is neither airborne, waterborne, nor rapid? The answers to that question are revealed in the epidemiology of AIDS and the easy interconnectedness of people in the modern era. One factor is the ready availability of fast and relatively inexpensive international air travel that developed after World War II. Even poor and previously isolated communities now are linked to the rest of the world by jet planes capable of transporting a human pathogen around the world in less than a single day. From 1950 to 2005,
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international tourist arrivals increased 32-fold worldwide. Approximately 2 million people now cross international borders each day. In the United States, 18 airports receive more than 500,000 international arrivals annually and 14 maritime ports provide entry for an additional 150,000 passengers.15,16 People travel for work and play, and with each trip are capable of spreading microbes in a variety of ways that range from casual coughing and sneezing to sexual contact and drug use. The months or years it took to spread an infectious agent in the era of the Black Death can now occur in days or weeks. For example, on March 30, 2003, a 48-year-old businessman flew from Hong Kong, China, to Frankfurt, Germany, and then over 5 days took 7 flights to different cities in Europe.17 At the time he left Hong Kong he felt well. But, on his return to Hong Kong he was admitted to the hospital with SARS. There is no way to count the number of people that single individual came into contact with in 1 week on plane flights, in hotels and restaurants, at business meetings, and in public places generally. Each one could have been exposed to SARS.15 One of the most sensationalized early reports of HIV infection was an airline flight attendant, called patient zero, described in the book And the Band Played On.18 Despite progressive signs and symptoms of AIDS, during his travels he continued to engage in unprotected sex with other men. Over the years when the AIDS epidemic was brewing there no doubt were other travelers, many if not most of whom had no idea they were HIV positive, who engaged in unprotected sex, thus unwittingly spreading the virus. Some even traveled for the specific purpose of engaging in sexual activity, known as sex tourism, which included venues, such as Thailand and Haiti, where explosive AIDS epidemics developed early on. URBANIZATION
AIDS is primarily an urban disease in developing and developed countries. By the late 1970s and early 1980s there already was substantial seeding of HIV across major metropolitan areas of Western Europe and the United States. The social ecology of AIDS thus also is a product of the dramatic urbanization of the world’s population that occurred after World War II. In 1800, Beijing was the only city with a population of more than 1 million. Today there are more than 40 cites with a population of at least 5 million and 19 with more than 10 million. From 1950 to 2005, the world’s urban population grew from approximately 730 million to 3.2 billion, and demographers predict that by 2030 it will be approximately 5 billion.19 Today’s city often is no longer a discrete metropolitan area but a megacity that includes the original city plus other nearby urban centers and a well-connected sprawl of suburbs and semirural areas. The population of Tokyo, Yokohama, Kawasaki, and Saitama is more than 34 million; Mexico City, Nezahualcoyotl, Ecatepec, and Naucalpan contain more than 22 million. With the efficiencies of modern travel and porous borders people now move readily within, across, and between cities. The uncontrolled urbanization of the past 5 decades has been the most challenging for the developing world, where sanitation, public health, and medical infrastructures are weak or absent entirely. These settings offer the potential to create a large single human reservoir for the eruption and propagation of infectious diseases. Over the past 3 decades this included AIDS, which flourished in urban centers across the globe. In Latin American approximately one third of people who have HIV live in Brazil, where the first cases were noted in 1982; the highest concentration of cases continues to be in Rio de Janeiro and Sa˜o Paulo. In the United States, 85% of reported AIDS cases are in major metropolitan areas: approximately 200,000 in the New York metropolitan area at a rate of 29.2 per 100,000 population; 58,000 in Los Angeles at 13 per 100,000; 40,000 in San Francisco at 16.5 per 100,00; and 56,000 in Miami at 41.9 per 100,000. Although across the entire United
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States the rate of infection in nonmetropolitan areas is 5.5 per 100,000 population, it is 15.9 in metropolitan areas of 500,000 or more. In 2006, the highest rates of new United States AIDS diagnoses were in Miami (41.9 per 100,000 people), Baltimore (37.7), and Washington, DC (31.8).20
CHANGING SEXUAL MORES AND GENDER ROLES
Although male homosexuality has existed since time immemorial, it was limited by criminalization and social ostracism. And although it continues to be illegal in approximately 70 countries, societal attitudes generally have become dramatically more tolerant, especially in developed societies.21 In the United States, these changes began in the late 1960s with a public and robust expression of gay liberation. A landmark event occurred on the evening of June 27, 1969, with resistance to a police raid of the Stonewall Inn, a well-known gay bar in Greenwich Village New York. That unprovoked police action precipitated several days of rioting and within weeks the formation of the Gay Liberation Front. Unfortunately, in the era of HIV the freedom to enjoy and celebrate a gay lifestyle came with a tragic downside. In March 1983, the Centers for Disease Control and Prevention shared the results of epidemiologic investigations, which showed that homosexual men who had multiple sexual partners were at increased risk for contracting AIDS and that the period between exposure and the manifestation of symptoms could be as long as 2 years.22 These findings led to the recommendation that individuals avoid sexual contact with ‘‘persons known or suspected to have AIDS.’’ A New York Times article published in February 1983 explained that the only protection against AIDS that clinicians could offer to homosexual patients was behavior change. In particular, gay men were advised to practice monogamy and, ideally, abstain from anal intercourse.23 Many gay men balked at these recommendations, feeling that they undermined their newly won sexual freedom to participate in sexual relationships the way that heterosexuals do.18 As a result of these societal changes, there was a proliferation of bathhouses, bars, and other venues where men could have anonymous homosexual sex with multiple partners. By the 1970s there were clearly observed increases in STIs and hepatitis B among men who have sex with men (MSM); and by the 1980s there was the epidemic of HIV.24–26 Without effective antiretroviral therapy the 1980s produced a mounting death toll in the gay community. The psychologic trauma was enormous. The emotional devastation also catalyzed a tremendous outpouring of positive energy in the gay community that included prevention outreach, volunteerism, support for people living with AIDS, organizing for inclusion in public health planning, and advocating for greater government funding for medical services, scientific research, and public health programs. There were tangible results from these efforts, as individual behavior change produced a demonstrable reduction in the number of new STIs and HIV infections among MSM.27 The development and widespread availability of effective highly active antiretroviral therapy by 1996, however, made it seem like AIDS could be managed. This, in turn encouraged some individuals to return to sexual risk taking and with that there was an up-tick in HIV transmission, in particular in young MSM.28 Meanwhile, the Internet became a new way for people to find sexual partners and arrange for explicit sexual activities. Studies have shown that sexual activity arranged on-line, especially among gay men, is associated with increased unsafe sex, casual partnering, recreational drug use, and sex with HIV-positive persons, including HIV-infected men having unsafe sex with HIV-uninfected men. These encounters also are associated with transactional sex and STIs, including rectal
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gonorrhea. Adding all these factors together, the Internet has the potential for accelerating the spread of HIV.29 Meanwhile, in North America and Europe there also was a sexual revolution for heterosexuals, in large part the result of advances in contraception for women that for the first time in history allowed them to engage in sexual intercourse without fear of unwanted pregnancy. This medical breakthrough was occurring at the same time there were profound social changes for women, which offered them an unprecedented degree of independence and opportunity. More freely and equally than ever before, women were able to participate in higher education and the workforce and to live on their own without fear of social stigma. As part of the 1960s sexual revolution it became acceptable and common for unmarried women and men to pursue sex for its own pleasure, for women to seek and insist on their own sexual gratification, and for men to become better lovers to accommodate them. Yet, despite the fact that young women and men in developed nations commonly engage in premarital sex, there has been relatively little HIV transmission in the group that enjoys higher education and socioeconomic status. Here it seems that feminism played a protective role by giving women the self-esteem and wherewithal to insist on safer sex. For example, between 1991 and 2003, condom use during last intercourse increased from 46% to 63% among adolescents whereas the use of oral contraception declined.30 After 1990, the prevalence of genital chlamydia declined among women entering job training and by the late 1990s so had the number of new HIV infections among adolescents.27,31 In the short run, at least, the impact of changing women’s roles may not be as protective in recently traditional societies as it has been in the West. Women across much of Asia are enjoying unprecedented opportunities in education, the workplace, and their ability to socialize outside the home and family. In Thailand, for instance, young women attend universities, communicate by cell phone and the Internet, and in general enjoy a degree of personal freedom unheard of in their mothers’ generation. With these societal changes has come an increase in STIs among young women and the possibility of an upsurge in HIV. Meanwhile, the subordination of women in traditional societies continues to be a potent factor in the social ecology of AIDS. In general it still is taboo in these cultures to openly discuss sex even in marriage. In India, for example, being married and monogamous is the number one risk factor for a woman who becomes HIV infected, as husbands frequent brothels and bring infection home.32,33 Using condoms is not acceptable in marriage. A dutiful wife is expected to bear many children and to ignore her husband’s infidelity. She has little personal or economic autonomy and few social supports to help her negotiate sexual matters. DRUG USE
Injecting recreational drugs had been present in developed societies for more than a century by the time the AIDS epidemic surfaced. Today, approximately 10% of HIV transmission worldwide can be attributed to injection drug use (IDU) through the sharing of unsterile injection equipment. It is an important factor for HIV transmission virtually everywhere there is an epidemic and a principal driver in China, Southeast Asia, and Eastern Europe.34 It is likely that HIV was introduced into cohorts of drug users via sexual contact and then amplified greatly by continuing IDU. Poverty, social and income inequality, crime, and social norms play important roles. The HIV epidemic in New York City probably began in the mid-1970s. It was illegal to purchase and possess drugs and drug use paraphernalia, which contributed to the reuse and sharing of syringes and equipment. Shooting galleries sprang up in poor
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neighborhoods, where injection drug users got high together and sometimes engaged in sex, including transactional sex. Although complex psychologic and social factors play into drug addiction, the illegal status of recreational drugs increases their black market prices, which in turn creates a continuing need to obtain ready cash to support addiction and, thus, the frequent overlap between transactional sex and injecting drug use. The need to maintain the high of the drug experience goes along with a desire to be with other drug users and with sharing paraphernalia. Harm reduction and syringe exchange programs were rarely available until the 1990s, by which time the HIV epidemic was already well established in the IDU community. Since then, programs to facilitate drug users’ access to sterile injecting equipment and decriminalizing the possession of sterile syringes have been associated with decreases in HIV.35,36 Although drug users face many barriers to quitting, more needs to be done to provide access to these programs. Noninjection substance use is a factor in HIV transmission among MSM, adolescents, the poor and homeless, and youth. Recreational drugs associated with increased risk for HIV transmission include alcohol, which is consumed in most countries by a large portion of the youth and adult populations, amphetamines, cocaine, nitrites (‘‘poppers’’), marijuana, and methylenedioxymethamphetamine (ecstasy). Often, these drugs are used in combination as polydrug abuse. All are shown to increase the risk for engaging in high-risk sex, including unprotected vaginal and anal intercourse and sex with anonymous or multiple partners. SPECIAL AT-RISK POPULATIONS
Although the number of new HIV infections in the United States has remained fairly constant in recent years at approximately 40,000 annually, the impact continues to be disproportionate in certain populations and the epidemiology of each risk group points to the relevant social ecology.37 From 1985 to 2004, the proportion of new AIDS cases among women increased from 18% to 27%, but as it is for STIs generally, the risk is higher for African American women than other racial and ethnic groups, including approximately 21 times more for African American women than white women. Overall, in 2004, approximately half of all new cases of AIDS were among African Americans who make up approximately 13% of the United States population.38–40 Many prevention programs are being tried to combat these disparities, including turning to African American churches to spread information and understanding about the spread of HIV and The Balm in Gilead, which sponsors The Black Church Week of Prayer for the Healing of AIDS.41 Of the approximately 1 million people living with HIV in the United States, approximately 60% are MSM. Young MSM have higher rates of HIV infection than older men, and young African American MSM have higher rates than young white MSM. Studies show that younger gay men engage in more risk taking, including drug use; have higher rates of STIs, which facilitate HIV transmission; and are less likely to avail themselves of HIV testing than the general population. Throughout the world, AIDS is primarily a disease among the young. Twenty-five percent of HIV infections worldwide are in youth between the ages of 15 and 24, and in 2005–2006 almost 50% of all new HIV infections worldwide were in this group.8 This demographic group thus accounts for 5000 to 6000 new infections daily and approximately 2.3 million new cases each year. In high-income countries, young people account for approximately one third of new cases, most among young MSM. In Asia most new infections in the younger population are the result of IDU. The risk for youth is greatest in sub-Saharan Africa, which accounts for approximately two
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thirds of all AIDS in young people worldwide and where HIV prevalence reaches 40% in some communities.8,42 In these settings merely being an adolescent and entering into a sexual relationship with one person, which many in the West consider normal adolescent development, puts a young person at risk. Age of sexual debut, particularly for young women, and partnering with older men also are risk factors.43 These patterns reflect disparities in power and opportunity between men and younger women. High rates of other STIs, the relative immaturity of the genital tract in young women, and a lack of routine male circumcision also have an impact on risk. In South Africa, approximately three quarters of HIV-positive individuals between the ages of 15 and 24 are women and more than 20% of pregnant women attending prenatal clinics have HIV. More than 400,000 infants are HIV infected worldwide each year, approximately 90% in Africa, and approximately half of new infections are transmitted through breastfeeding.8 This is a tragedy that can be prevented with good prenatal care, antiretroviral therapy, HIV testing, and prevention of mother-to-child transmission of HIV services, which can reduce mother-to-child transmission of HIV to less than 2%.44–46 Sex workers are another group of people particularly affected by the worldwide social ecology of AIDS. As early as 1985, the HIV infection rate among sex workers was as high as 62% in Nairobi, Kenya, and by the late 1980s it was 89% in Abidjan, Coˆte d’Ivoire.47,48 Sex workers face many risks: large number of sexual contacts and low level of condom use, high prevalence of other STIs, and lack of access to medical services. Sex work can be direct, which means it is open and formal, or indirect, when it is hidden or informal. In many developing countries, it is a social norm for men to purchase sex and 20% to 40% of men report having done so.49–51 The overwhelming majority of women engaged in sex work are poor and poorly educated. Frequently, they have been victims of childhood violence and sexual abuse and continue sex work in an environment of exploitation, threat, and violence. Many are drug users or have sexual contact with injection drug users. The fact that sex work is illegal and socially ostracized means these women face obstacles to accessing medical services. For example, although prostitution is lawful in the former Soviet Union, it is not legal to live in Moscow without a special permit. Women from other parts of the country who come to Moscow and engage in sex work thus are there illegally and report restrictions in their access to health services. They are subject to exploitation and abuse generally, including rape, and sexual exploitation by pimps, clients, and even the police.52 Although efforts are being made to help sex workers worldwide, most programs have been implemented on a small scale and most sex workers as yet have not had access to them. To date there have been some notable programmatic successes, such as high levels of condom use in Benin, Thailand, and Cambodia, which probably have been effective in reducing the HIV rate among sex workers and by doing so probably helped to slow the AIDS epidemic in the general population.51,53 Incarceration and institutionalization also are important factors in the transmission of HIV throughout the world. In 2006 there were more than 2 million people in United States prisons, and an estimated one fourth of people living with AIDS in the United States had spent some time incarcerated. In this population the percentage of women (2.3%) who are HIV infected is higher than for men (1.7) and higher for African American (2%) and Hispanic/Latino (1.8%) populations than for whites (1%). China and the Russian Federation also have high incarceration rates, and it is assumed they have or will have HIV/AIDS epidemics in their institutions. To date, these governments have not provided what are believed reliable data on HIV infection rates in their institutions. China did not publicly acknowledge the existence of HIV/AIDS until 2001, but it is believed that approximately half of
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China’s HIV-positive population contracted the virus through IDU. This likely puts the incarcerated population at risk for an HIV epidemic, because intravenous drug use often is associated with incarceration. The risk factors associated with HIV transmission among institutionalized persons include addiction and IDU before and during incarceration, mental illness, hepatitis C and other infectious diseases, forced and consensual sex especially among MSM, and tattooing. In 1993 the WHO recommended condom distribution in prisons, but this has yet to become a widespread practice.54 It is not clear how effective condom distribution would be because coercive sex is common and many inmates would not want to be known publicly in the facility as participating in sex with other men. In 1982 it was discovered that several hemophiliacs had developed AIDS, and even though this was before the HIV had been isolated, it was presumed that the cause of their infection was receipt of contaminated blood products. This finding further confirmed the already widespread conclusion that the new immune deficiency disorder behaved in its transmission like hepatitis B and C viruses, cytomegalovirus, and other agents that are spread by high-risk sexual activity and IDU. There were national scandals in the United States, France, Japan, and Canada and a more recent scandal in China among blood donors in which unscrupulous profit-making companies reused unsterile blood-collecting equipment. In developed nations, the blood banking community responded quickly, based first and foremost on a system of voluntary donation and careful screening of donors. Although there now are effective laboratory tests to detect HIV contamination of donor units, blood bankers know that even with advances in laboratory testing, the front-line prevention against blood contamination is a voluntary system of blood donation coupled with careful questioning about relevant donor behaviors, including health status, history of receiving a transfusion or medical treatment in certain places, drug use, sexual activity, travel, and residency. There is not now and probably never will be a laboratory test for every potential blood pathogen. The result of these efforts is a success story in AIDS prevention in developed nations where HIV infection via blood transfusion is extremely rare; in the United States, for HIV-1, it is as low as 1 in 676,000 units transfused. Unfortunately, this is not the case in sub-Saharan Africa and parts of Asia, as a consequence of inadequate resources and out dated technology in the health sector.10,55
LOOKING AHEAD
Although the global AIDS epidemic probably peaked in 2000–2001, there are an estimated 4 million new cases annually and the downstream impacts of what has already occurred will be felt for generations to come.37,39 In Africa it has reversed decades of progress previously made in reducing mortality and increasing life expectancy. Although a highly protective vaccine or effective oral or topical chemoprophylaxis would greatly slow the spread of HIV to new individuals in endemic areas and new regions, recent clinical trials suggest that a successful anti-HIV vaccine will take many more years to develop. Even if chemoprophylaxis studies prove effective in decreasing HIV transmission, the daily use of medications that comes with significant costs and side effects is likely to be a holding action at best. One unavoidable conclusion from the social ecology of HIV transmission is that it is difficult to impede the spread of an infectious agent that is transmitted through pleasurable human activities—in this case sexual activity and recreational drugs. Despite billions of dollars spent on prevention programs, HIV continues to thrive in its various human niches and short of a vaccine there is no magic bullet that can combat human nature.
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So, more needs to be done with the tools currently available. The foundation for this work is epidemiology that uncovers the hot spots of an epidemic and, thereby, directs where to focus attention. There must be constant attention to prevention even among low-risk populations, however, or facing the peril of seeing a low incidence pathogen get out of hand. This is what occurred in Africa during the early days of AIDS, when governments were slow to respond and the virus was free to spread to unsuspecting people. Prevention efforts require a wide array of programs that involve mass public health education, provider-patient communication, HIV testing, linkage to care, enlisting the assistance of community leaders, and government and nongovernmental allocation of resources to keep successful existing programs well funded and to encourage new and creative ones. For each risk group there needs to be targeted interventions that deal with the behaviors and underlying causes for HIV transmission. For instance, one clear example is combating substance abuse, which is known to encourage high-risk sexual activity. Interventions would include education, treatment, and harm reduction. There also is, of course, the bigger picture that includes poverty, segregation of neighborhoods, and the culture of drug use. Another example is in the education and empowerment of women, especially in traditional societies, to provide them with the self-esteem and social backing to insist on safe sex. Even if an effective microbicide is developed in short order, it would be necessary to provide women in these settings the social tools to use it. Interventions are needed with sex workers that include changing government policies that make them vulnerable to abuse and exploitation and disease. Interventions with MSM are needed that involve the entire community, particularly in societies where gay men still are much in the closet. The lessons learned from the activism begun in the 1980s in the United States can be applied elsewhere. And, there needs to be continued focus on prevention research, including program evaluation, to understand what works and how to implement successful pilot programs on a larger scale. Even among populations studied as extensively as MSM substance users, few people are accessing substance use treatment services. In the National HIV Behavioral Surveillance System, for instance, only 16% of MSM substance users reported ever accessing treatment services.56 It is important to understand why people at risk do not access services to overcome the barriers standing in their way. This basic theme can be applied throughout. Determined government action to combat AIDS is critical. Brazil is a success story in this regard. With the end of military rule, Brazil’s democracy activists turned to public health. New constitutional language declared universal health to be a basic human right and with that efforts were made to greatly expand health services to underserved groups and regions, including the goal of providing universal access to antiretroviral drugs and ramping up HIV prevention programs. HIV prevention messages now are widely disseminated in Brazil’s public spaces, often by well-known entertainers, athletes, and models. Prevention programs, including harm reduction, reach out to high-risk groups, such as MSM, sex workers, injection drug users, and incarcerated persons. Public education helps destigmatize AIDS and encourages individuals to voluntarily partake of HIV testing and counseling. It is estimated that approximately one third of Brazilians infected with HIV know their status as opposed to only approximately 10% of those infected elsewhere in the developing world. Although the AIDS epidemic exploded in much of the developing world during the 1990s, because of effective public effort it remained stabilized and contained in Brazil.57,58 Until there is a biologic tool to prevent HIV transmission, no single type of prevention program is going to work for each at-risk population in the diverse geographic and cultural settings where HIV has found its human niche.
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REFERENCES
1. Cliff A, Haggett P. Time, travel and infection. Br Med Bull 2004;69:87–99. 2. Barry J. The great influenza. The epic story of the deadliest plague in history. New York: Viking; 2004. 3. Garrett L. Betrayal of trust: the collapse of global public health. New York: Hyperion; 2000. 4. Dye C, Scheele S, Dolin P, et al. Consensus statement. Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. WHO Global Surveillance and Monitoring Project. J Am Med Assoc 1999;282(7):677–86. 5. Corbett E, Watt CJ, Walker N, et al. The growing burden of tuberculosis: global trends and interactions with the HIV epidemic. Arch Intern Med 2003;163(9):1009–21. 6. Dye C, Watt CJ, Bleed DM, et al. Evolution of tuberculosis control and prospects for reducing tuberculosis incidence, prevalence, and deaths globally. J Am Med Assoc 2005;293(22):2767–75. 7. Kanki P, Essex ME. Virology. In: Mayer K, Pizer HF, editors. The AIDS pandemic: impact on science and society. New York: Academic Press; 2004. p. 13–35. 8. Unaids. UNAIDS/WHO AIDS epidemic update. Available at: http://www.unaids. org/epidemic-update/. Accessed May 9, 2008. 9. Murphy E. The clinical epidemiology of human T-lymphotropic virus type II (HTLV-II). J Acquir Immune Defic Syndr 1996;13(Suppl 1):S215–219. 10. Page P, Pizer HF. Protecting blood safety. In: Mayer KH, Pizer HP, editors. The social ecology of infectious diseases. London: Elsevier; 2008. p. 187–214. 11. Gallo R, Salahuddin SZ, Popovic M, et al. Frequent detection and isolation of cytopathic retroviruses (HTLV-III) from patients with AIDS and at risk for AIDS. Science 1984;224(4648):500–3. 12. Essex M, McLane MF, Kanki PJ, et al. Retroviruses associated with leukemia and ablative syndromes in animals and in human beings. Cancer Res 1985;45: 4534s–8s. 13. Hahn B, Shaw GM, DeCock KM, et al. AIDS as a zoonosis, scientific and public health implications. Science 2000;287:607–14. 14. Wolfe N, Daszak P, Kilpatrick AM, et al. Bushmeat hunting and deforestation in prediction of zoonoses emergence. Emerg Infect Dis 2005;11(12):1822–7. 15. Wilson M, Chen LH. Travel. In: Mayer KH, Pizer HP, editors. The Social ecology of infectious diseases. London: Elsevier; 2008. p. 17–49. 16. Sivitz LB, Stratton K, Benjamin GC, editors. Quarantine stations at ports of entry: protecting the public’s health. The National Academies Press; 2006. 17. Breugelmans J, Zucs P, Porten K, et al. SARS transmission and commercial aircraft. Emerg Infect Dis 2004;10(8):1502–3. 18. Shilts R. And the band played on. New York: St. Martin’s Press; 1987. 19. United Nations Department of Economic and Social Affairs. World Urbanization Prospects: the 2007 revision. Available at: http://www.un.org/esa/population/ publications/wup2007/2007WUP_ExecSum_web.pdf. Accessed June 22, 2008. 20. Avert. United States AIDS cases in major cities. Available at: http://www.avert. org/usastatc.htm. Accessed May 25, 2008. 21. Timberlake S. Men having sex with men and human rights: the UNAIDS perspective. Presented at the ILGA World Conference, Pre-Conference: MSM and Gay Men’s Health Geneva, Switzerland; March 27–April 3, 2006. 22. Centers for Disease Control and Prevention. Current trends prevention of acquired immune defi ciency syndrome (AIDS): report of inter-agency recommendations. MMWR Morb Mortal Wkly Rep 1983;32:101–3.
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23. Henig R. AIDS: a new disease’s deadly odyssey. The New York Times. February 6, 1983. 24. Fichtner R, Aral SO, Blount JH, et al. Syphilis in the United States: 1967–1979. Sex Transm Dis 1983;10(2):77–80. 25. Ostrow D, Altman NL. Sexually transmitted diseases and homosexuality. Sex Transm Dis 1983;10:208–15. 26. Rotello G. Sexual ecology: AIDS and the destiny of gay men. New York: Penguin Books; 1997. 27. Celentano D, Sifakis F, Go V, et al. Changing sexual mores and disease transmission. HP. In: Mayer KH, Pizer HP, editors. The social ecology of infectious diseases. London: Elsevier; 2008. p. 50–76. 28. Ekstrand M, Coates TJ. Maintenance of safer sexual behaviors and predictors of risky sex: the San Francisco Men’s Health Study. Am J Public Health 1990;80: 973–7. 29. Bull S, McFarlane M. Soliciting sex on the Internet: what are the risks for sexually transmitted diseases and HIV? Sex Transm Infect 2000;27:545–50. 30. Biddlecom A. Trends in sexual behaviours and infections among young people in the United States. Sex Transm Infect 2004;80(Suppl 2):74–9. 31. Mertz K, Ransom RL, St Louis ME, et al. Prevalence of genital chlamydial infection in young women entering a national job training program, 1990–1997. Am J Public Health 2001;91:1287–90. 32. Newmann S, Sarin P, Kumarasamy N, et al. Marriage, monogamy and HIV: a profile of HIV-infected women in south India. Int J STD AIDS 2000;11:250–3. 33. Gangakhedkar R, Bentley ME, Divekar AD, et al. Spread of HIV infection in married monogamous women in India. J Am Med Assoc 1997;278(23):2090–2. 34. Hammett T, Wu Z, Duc TT, et al. ‘Social evils’ and harm reduction: the evolving policy environment for human immunodeficiency virus prevention among injection drug users in China and Vietnam. Addiction 2008;103(1):137–45. 35. Watters J, Estilo MJ, Clark GL, et al. Syringe and needle exchange as HIV/AIDS prevention for injection drug users. J Am Med Assoc 1994;271(2):115–20. 36. Ouellet L, Huo D, Bailey SL. HIV risk practices among needle exchange users and nonusers in Chicago. J Acquir Immune Defic Syndr 2004;37(1):1187–96. 37. Centers for Disease Control and Prevention. Epidemiology of HIV/AIDS—United States, 1981–2005. MMWR Morb Mortal Wkly Rep 2006;55:589–92. 38. U.S. Census Bureau. Infoplease. Available at: http://www.infoplease.com/spot/ bhmcensus1.html. Accessed May 30, 2008. 39. Centers for Disease Control and Prevention. Racial/ethnic disparities in diagnoses of HIV/AIDS—33 states, 2001–2004. MMWR Morb Mortal Wkly Rep 2006; 55:121–5. 40. Centers for Disease Control and Prevention. HIV/AIDS among African Americans. Atlanta (GA): US Department of Health and Human Services; 2006. 41. Avery B, Bashir S. The road to advocacy—searching for the rainbow. Am J Public Health 2003;93:1207–10. 42. Pettifor A, van der Straten A, Dunbar MS, et al. Early age of first sex: a risk factor for HIV infection among women in Zimbabwe. AIDS 2004;18:1435–42. 43. Abdool Karim Q. Heterosexual transmission of HIV - the importance of a gendered perspective in HIV prevention. In: Abdool Karim S, Abdool Karim Q, editors. HIV/ AIDS in South Africa. Cape Town (South Africa): Cambridge University Press; 2005. p. 243–61. 44. Newell M, Thorne C. Antiretroviral therapy and mother-to-child transmission of HIV-1. Expert Rev Anti infect Ther 2004;2(5):717–32.
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45. McIntyre J, Lallemaent M. The prevention of mother-to-child transmission of HIV: are we translating scientific success into programmatic failure? Current Opinion in HIV & AIDS 2008;3(2):139–45. 46. Fowler M, Lampe MA, Jamieson DJ, et al. Reducing the risk of mother-to-child human immunodeficiency virus transmission: past successes, current progress and challenges, and future directions. Am J Obstet Gynecol 2007;197:S3–9. 47. Hunt C. Migrant labor and sexually transmitted disease: AIDS in Africa. J Health Soc Behav 1989;30(4):353–73. 48. Simonsen J, Plummer FA, Ngugi EN, et al. HIV infection among lower socioeconomic strata prostitutes in Nairobi. AIDS 1990;4(2):139–44. 49. Wilson D, Dubley I, Msimanga S, et al. Psychosocial predictors of reported HIVpreventive behaviour change among adults in Bulawayo, Zimbabwe. Cent Afr J Med 1991;37(7):196–202. 50. Aklilu M, Messele T, Tsegaye A, et al. Factors associated with HIV-1 infection among sex workers of Addis Ababa, Ethiopia. AIDS 2001;15(1):87–96. 51. Morison L, Weiss HA, Buve A, et al. Commercial sex and the spread of HIV in four cities in sub-Saharan Africa. AIDS 2001;15(Suppl 4):S61–9. 52. Stachowiak J, Peryshkina A. Women’s health and women’s rights: selling sex in Moscow. In: Beyrer C, Pizer HF, editors. Public Health and Human Rights: evidence-based approaches. Baltimore (MD): Johns Hopkins University Press; 2007. p. 88–104. 53. Rojanapithayakorn W, Hanenberg R. The 100% condom program in Thailand. AIDS 1996;10(1):1–7. 54. World Health Organization. Interventions to address HIV in prison: prevention of sexual transmission. Available at: http://www.who.int/hiv/idu/oms_ea_sexual_ transmission_df.pdf. Accessed May 30, 2008. 55. Heyns A, Benjamin RT, Swanevelder JPR. Blood supply and demand. Lancet 2005;365(9478):2151. 56. Sanchez J, Finlayson T, Drake A, et al. Human Immunodeficiency Virus (HIV) risk, prevention, and testing behaviors—United States, National HIV Behavioral Surveillance System: men who have sex with men, November 2003–April 2005. MMWR Morb Mortal Wkly Rep 2006;55(SS06):1–16. 57. Okie S. Fighting HIV–lessons from Brazil. N Engl J Med 2006;354(19):1977–81. 58. Gauri V, Beyrer C, Vaillancourt D. Human Rights principles to public health practice. In: Beyrer C, Pizer HF, editors. Public health and human rights: evidence-based approaches. Baltimore, (MD): Johns Hopkins University Press; 2007. p. 289–329.
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Although studying microbiology and immunology is essential to understanding the pathogenesis of infections caused by fungi, parasites, bacteria, viruses, and other microorganisms, the reasons that epidemics occur are largely a function of human behaviors and responses to environmental changes. The study of microbial-host interactions thus is the social ecology of infectious diseases, as it attempts to understand and describe the ways in which human activities alter specific microenvironments and thereby create favorable conditions for old and new microorganisms to develop and spread. Although potential pathogens adapt to specific niches as a function of their intrinsic properties, such as the ability to withstand heat, cold or drying, and their microenvironment, it is changes in human behavior that potentiate their spread. So although Yersinia pestis caused intermittent death in remote parts of Europe before the fourteenth century, it was the development of increasingly globalized commerce throughout the Mediterranean and Black Sea that enabled rats to carry the organism onboard ships and produce the infamous Black Death, which killed 20 to 30 million Europeans or approximately one third to two thirds of the population.1 The Spanish influenza epidemic of 1918–1919 was greatly abetted by the social disruptions of World War I, where large numbers of soldiers lived in densely crowded conditions at the front and then traveled to and from the battlefield carrying infectious diseases.2 Meanwhile, malnutrition, the dislocation of millions of displaced persons, and unsanitary living conditions provided additional supports for spreading the virus. In just a few years the flu virus spread around the world in three waves, killing an estimated 50 million people. In the late 1960s, prominent medical scientists and public health officials were predicting the end of infectious diseases as a significant public health concern and were
a
Brown University, 164 Summit Avenue, Providence, RI 02906, USA Miriam Hospital, Providence, RI, USA c The Fenway Institute, Fenway Community Health, Boston, MA, USA d Health Care Strategies, Inc., 213 Hamilton Street, Cambridge, MA 02139, USA e Department of Community Health, Alpert Medical School, Brown University, Box G8488, Providence, RI 02912, USA * Corresponding author. Infectious Disease Division, Miriam Hospital, 164 Summit Avenue, Providence, RI 02906. E-mail address: [email protected] (K. Mayer). b
Med Clin N Am 92 (2008) 1363–1375 doi:10.1016/j.mcna.2008.06.003 medical.theclinics.com 0025-7125/08/$ – see front matter ª 2008 Elsevier Inc. All rights reserved.
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advising policy makers to shift funding, research, and training priorities away from infectious diseases to chronic medical conditions, such as cardiovascular disease and cancer.3 Although wrong in hindsight, the optimism of the time was understandable in light of the enormous strides being made in living standards and longevity, public sanitation and public health, vaccines, antibiotics, and other new medical technologies. These experts also predicted that the advances being attained in combating infectious diseases in developed nations soon would be translated to the developing ones. As events unfolded, the optimism was short-lived. Soon there was a resurgence of old infectious diseases that had been well controlled, such as tuberculosis,4–6 and an eruption of new ones, such as AIDS, legionnaires’ disease, Lyme disease, and Ebola hemorrhagic fever. A sobering lesson was learned: microbial pathogens have the extraordinary capacity to adapt to human lifestyles, including advances in medical science and technology. THE ADVENT OF THE AIDS PANDEMIC
In only approximately 25 years during the latter decades of the twentieth century, HIV-1, the most common human immunodeficiency virus that causes AIDS, spread throughout the world to infect more than 70 million people and cause approximately 35 million deaths.7 It is now the fourth leading cause of death worldwide and accounts for approximately 25% of deaths in Africa.8 HIV-1 is part of a class of viruses known as retroviruses discovered in the first decade of the twentieth century by Payton Rous, when he observed a filterable agent capable of causing sarcoma, a type of cancer that could be transmitted between chickens. Over subsequent decades researchers were able to detect many retroviruses in a diverse array of vertebrate species. Once genes were found to be comprised of DNA and the genetic code was deciphered, investigators began to categorize the ways in which these viruses replicate through infecting cells, integrating themselves into host cell genomes and then using the host cell’s nucleus to direct the infected cell to make new viral copies. A major contribution to the understanding of their pathogenesis was to characterize the enzyme, reverse transcriptase, which allows retroviruses to infect cells through their RNA and then integrate themselves into the host genome as a DNA provirus. In the late 1970s researchers discovered that the human T- lymphotropic virus (HTLV), also a retrovirus, could lie dormant in its host for decades. Like HIV-1, in a small subset of individuals HTLV can cause hematologic malignancies and neurologic diseases, such as spastic paraparesis.7,9 These discoveries were important for understanding AIDS when in 1980 and early 1981 clinicians in New York, Los Angeles, and San Francisco observed a new syndrome of opportunistic infections and atypical neoplasms, such as Kaposi’s sarcoma, a rare hematologic malignancy, in a small group of homosexual men who had been sexually active with multiple partners and injection drug users. Soon, a smaller group of patients who had hemophilia were identified who apparently had acquired the new disease from transfusions of contaminated blood products.10 For several years there was speculation that this new disease, soon to be named the acquired immunodeficiency syndrome (AIDS), was being caused by a retrovirus, because its pattern of transmission seemed similar to that of animal retroviruses and HTLV.7,11,12 Even before the AIDS virus was isolated in 1983, the clues to unraveling what was going on were found through careful epidemiologic sleuthing and observing the sociobehavioral factors associated with HIV transmission. Because of the lack of specimen repositories in many underdeveloped parts of the world, definitive conclusions about where and when epidemics originate often has
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remained indecipherable. Recent developments in computer technology data storage and evolutionary biology, however, have enabled molecular virologists to construct schema to pinpoint patterns of microbial evolution that can be associated with temporal sequences of viral transmission in different geographic areas. The collection of multiple samples of HIV from around the world with subsequent genetic sequencing have enabled molecular epidemiologists to estimate that HIV infection developed in a remote part of sub-Saharan Africa, possibly the Democratic Republic of the Congo.13 It is clear from more recent studies that viruses that are extremely similar to HIV have been found in this region in several primate species, in particular chimpanzees whose immune systems are most homologous to humans compared with other species. Additionally, anthropologic studies conducted in several regions of central and contiguous areas of sub-Saharan Africa have demonstrated that monkey meat is a major source of protein for indigenous peoples. Researchers have documented that the preparation of monkey meat by traditional butchering methods involves substantial contact with blood and sharp objects.14 Thus, it is not difficult to imagine that a simian retrovirus made the jump from primates to humans through the process of preparing meat for local consumption. Because it can take years before retroviruses, such as HIV, produce symptoms of infection, it was likely that some significant time passed during which infected individuals were freely passing the virus on to others. Whatever the actual start date and time sequence for the leap from primate to human (recent studies suggest that there were multiple introductions into the human population), by the 1970s there existed in rural Africa a sufficiently large number of people infected with HIV to lay the foundation for a much wider and long-lasting epidemic. It also is likely that the process developed as concurrent and overlapping multiple microepidemics, each of which was fueled by local social factors. In sub-Saharan Africa of the 1960s and 1970s there were substantial population migrations of men without their spouses and families that also served to propel the transmission of HIV. These men were moving from the countryside to the city or to mineral mines and labor camps looking for work. Throughout human history concentrations of young, mobile unattached men have set the stage for transactional sex and homosexuality, both of which served at this time to spread HIV in an unsuspecting population. Over time the men brought HIV and other sexually transmitted infections (STIs), which enhance the infectiousness of HIV, back to their communities when they returned home. HIV also spread along known truck routes where men engaged in transactional sex and by soldiers involved in the many armed conflicts that engulfed the region during those years. With extremely limited public health systems, no government-sponsored prevention messages, and limited access to condoms, the migrant populations and the sex workers that served them created an ideal social ecology for the spread of HIV. TRAVEL
How could an epidemic that was slowly brewing in sub-Saharan Africa become a global pandemic in just a few decades, especially since transmission of HIV is neither airborne, waterborne, nor rapid? The answers to that question are revealed in the epidemiology of AIDS and the easy interconnectedness of people in the modern era. One factor is the ready availability of fast and relatively inexpensive international air travel that developed after World War II. Even poor and previously isolated communities now are linked to the rest of the world by jet planes capable of transporting a human pathogen around the world in less than a single day. From 1950 to 2005,
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international tourist arrivals increased 32-fold worldwide. Approximately 2 million people now cross international borders each day. In the United States, 18 airports receive more than 500,000 international arrivals annually and 14 maritime ports provide entry for an additional 150,000 passengers.15,16 People travel for work and play, and with each trip are capable of spreading microbes in a variety of ways that range from casual coughing and sneezing to sexual contact and drug use. The months or years it took to spread an infectious agent in the era of the Black Death can now occur in days or weeks. For example, on March 30, 2003, a 48-year-old businessman flew from Hong Kong, China, to Frankfurt, Germany, and then over 5 days took 7 flights to different cities in Europe.17 At the time he left Hong Kong he felt well. But, on his return to Hong Kong he was admitted to the hospital with SARS. There is no way to count the number of people that single individual came into contact with in 1 week on plane flights, in hotels and restaurants, at business meetings, and in public places generally. Each one could have been exposed to SARS.15 One of the most sensationalized early reports of HIV infection was an airline flight attendant, called patient zero, described in the book And the Band Played On.18 Despite progressive signs and symptoms of AIDS, during his travels he continued to engage in unprotected sex with other men. Over the years when the AIDS epidemic was brewing there no doubt were other travelers, many if not most of whom had no idea they were HIV positive, who engaged in unprotected sex, thus unwittingly spreading the virus. Some even traveled for the specific purpose of engaging in sexual activity, known as sex tourism, which included venues, such as Thailand and Haiti, where explosive AIDS epidemics developed early on. URBANIZATION
AIDS is primarily an urban disease in developing and developed countries. By the late 1970s and early 1980s there already was substantial seeding of HIV across major metropolitan areas of Western Europe and the United States. The social ecology of AIDS thus also is a product of the dramatic urbanization of the world’s population that occurred after World War II. In 1800, Beijing was the only city with a population of more than 1 million. Today there are more than 40 cites with a population of at least 5 million and 19 with more than 10 million. From 1950 to 2005, the world’s urban population grew from approximately 730 million to 3.2 billion, and demographers predict that by 2030 it will be approximately 5 billion.19 Today’s city often is no longer a discrete metropolitan area but a megacity that includes the original city plus other nearby urban centers and a well-connected sprawl of suburbs and semirural areas. The population of Tokyo, Yokohama, Kawasaki, and Saitama is more than 34 million; Mexico City, Nezahualcoyotl, Ecatepec, and Naucalpan contain more than 22 million. With the efficiencies of modern travel and porous borders people now move readily within, across, and between cities. The uncontrolled urbanization of the past 5 decades has been the most challenging for the developing world, where sanitation, public health, and medical infrastructures are weak or absent entirely. These settings offer the potential to create a large single human reservoir for the eruption and propagation of infectious diseases. Over the past 3 decades this included AIDS, which flourished in urban centers across the globe. In Latin American approximately one third of people who have HIV live in Brazil, where the first cases were noted in 1982; the highest concentration of cases continues to be in Rio de Janeiro and Sa˜o Paulo. In the United States, 85% of reported AIDS cases are in major metropolitan areas: approximately 200,000 in the New York metropolitan area at a rate of 29.2 per 100,000 population; 58,000 in Los Angeles at 13 per 100,000; 40,000 in San Francisco at 16.5 per 100,00; and 56,000 in Miami at 41.9 per 100,000. Although across the entire United
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States the rate of infection in nonmetropolitan areas is 5.5 per 100,000 population, it is 15.9 in metropolitan areas of 500,000 or more. In 2006, the highest rates of new United States AIDS diagnoses were in Miami (41.9 per 100,000 people), Baltimore (37.7), and Washington, DC (31.8).20
CHANGING SEXUAL MORES AND GENDER ROLES
Although male homosexuality has existed since time immemorial, it was limited by criminalization and social ostracism. And although it continues to be illegal in approximately 70 countries, societal attitudes generally have become dramatically more tolerant, especially in developed societies.21 In the United States, these changes began in the late 1960s with a public and robust expression of gay liberation. A landmark event occurred on the evening of June 27, 1969, with resistance to a police raid of the Stonewall Inn, a well-known gay bar in Greenwich Village New York. That unprovoked police action precipitated several days of rioting and within weeks the formation of the Gay Liberation Front. Unfortunately, in the era of HIV the freedom to enjoy and celebrate a gay lifestyle came with a tragic downside. In March 1983, the Centers for Disease Control and Prevention shared the results of epidemiologic investigations, which showed that homosexual men who had multiple sexual partners were at increased risk for contracting AIDS and that the period between exposure and the manifestation of symptoms could be as long as 2 years.22 These findings led to the recommendation that individuals avoid sexual contact with ‘‘persons known or suspected to have AIDS.’’ A New York Times article published in February 1983 explained that the only protection against AIDS that clinicians could offer to homosexual patients was behavior change. In particular, gay men were advised to practice monogamy and, ideally, abstain from anal intercourse.23 Many gay men balked at these recommendations, feeling that they undermined their newly won sexual freedom to participate in sexual relationships the way that heterosexuals do.18 As a result of these societal changes, there was a proliferation of bathhouses, bars, and other venues where men could have anonymous homosexual sex with multiple partners. By the 1970s there were clearly observed increases in STIs and hepatitis B among men who have sex with men (MSM); and by the 1980s there was the epidemic of HIV.24–26 Without effective antiretroviral therapy the 1980s produced a mounting death toll in the gay community. The psychologic trauma was enormous. The emotional devastation also catalyzed a tremendous outpouring of positive energy in the gay community that included prevention outreach, volunteerism, support for people living with AIDS, organizing for inclusion in public health planning, and advocating for greater government funding for medical services, scientific research, and public health programs. There were tangible results from these efforts, as individual behavior change produced a demonstrable reduction in the number of new STIs and HIV infections among MSM.27 The development and widespread availability of effective highly active antiretroviral therapy by 1996, however, made it seem like AIDS could be managed. This, in turn encouraged some individuals to return to sexual risk taking and with that there was an up-tick in HIV transmission, in particular in young MSM.28 Meanwhile, the Internet became a new way for people to find sexual partners and arrange for explicit sexual activities. Studies have shown that sexual activity arranged on-line, especially among gay men, is associated with increased unsafe sex, casual partnering, recreational drug use, and sex with HIV-positive persons, including HIV-infected men having unsafe sex with HIV-uninfected men. These encounters also are associated with transactional sex and STIs, including rectal
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gonorrhea. Adding all these factors together, the Internet has the potential for accelerating the spread of HIV.29 Meanwhile, in North America and Europe there also was a sexual revolution for heterosexuals, in large part the result of advances in contraception for women that for the first time in history allowed them to engage in sexual intercourse without fear of unwanted pregnancy. This medical breakthrough was occurring at the same time there were profound social changes for women, which offered them an unprecedented degree of independence and opportunity. More freely and equally than ever before, women were able to participate in higher education and the workforce and to live on their own without fear of social stigma. As part of the 1960s sexual revolution it became acceptable and common for unmarried women and men to pursue sex for its own pleasure, for women to seek and insist on their own sexual gratification, and for men to become better lovers to accommodate them. Yet, despite the fact that young women and men in developed nations commonly engage in premarital sex, there has been relatively little HIV transmission in the group that enjoys higher education and socioeconomic status. Here it seems that feminism played a protective role by giving women the self-esteem and wherewithal to insist on safer sex. For example, between 1991 and 2003, condom use during last intercourse increased from 46% to 63% among adolescents whereas the use of oral contraception declined.30 After 1990, the prevalence of genital chlamydia declined among women entering job training and by the late 1990s so had the number of new HIV infections among adolescents.27,31 In the short run, at least, the impact of changing women’s roles may not be as protective in recently traditional societies as it has been in the West. Women across much of Asia are enjoying unprecedented opportunities in education, the workplace, and their ability to socialize outside the home and family. In Thailand, for instance, young women attend universities, communicate by cell phone and the Internet, and in general enjoy a degree of personal freedom unheard of in their mothers’ generation. With these societal changes has come an increase in STIs among young women and the possibility of an upsurge in HIV. Meanwhile, the subordination of women in traditional societies continues to be a potent factor in the social ecology of AIDS. In general it still is taboo in these cultures to openly discuss sex even in marriage. In India, for example, being married and monogamous is the number one risk factor for a woman who becomes HIV infected, as husbands frequent brothels and bring infection home.32,33 Using condoms is not acceptable in marriage. A dutiful wife is expected to bear many children and to ignore her husband’s infidelity. She has little personal or economic autonomy and few social supports to help her negotiate sexual matters. DRUG USE
Injecting recreational drugs had been present in developed societies for more than a century by the time the AIDS epidemic surfaced. Today, approximately 10% of HIV transmission worldwide can be attributed to injection drug use (IDU) through the sharing of unsterile injection equipment. It is an important factor for HIV transmission virtually everywhere there is an epidemic and a principal driver in China, Southeast Asia, and Eastern Europe.34 It is likely that HIV was introduced into cohorts of drug users via sexual contact and then amplified greatly by continuing IDU. Poverty, social and income inequality, crime, and social norms play important roles. The HIV epidemic in New York City probably began in the mid-1970s. It was illegal to purchase and possess drugs and drug use paraphernalia, which contributed to the reuse and sharing of syringes and equipment. Shooting galleries sprang up in poor
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neighborhoods, where injection drug users got high together and sometimes engaged in sex, including transactional sex. Although complex psychologic and social factors play into drug addiction, the illegal status of recreational drugs increases their black market prices, which in turn creates a continuing need to obtain ready cash to support addiction and, thus, the frequent overlap between transactional sex and injecting drug use. The need to maintain the high of the drug experience goes along with a desire to be with other drug users and with sharing paraphernalia. Harm reduction and syringe exchange programs were rarely available until the 1990s, by which time the HIV epidemic was already well established in the IDU community. Since then, programs to facilitate drug users’ access to sterile injecting equipment and decriminalizing the possession of sterile syringes have been associated with decreases in HIV.35,36 Although drug users face many barriers to quitting, more needs to be done to provide access to these programs. Noninjection substance use is a factor in HIV transmission among MSM, adolescents, the poor and homeless, and youth. Recreational drugs associated with increased risk for HIV transmission include alcohol, which is consumed in most countries by a large portion of the youth and adult populations, amphetamines, cocaine, nitrites (‘‘poppers’’), marijuana, and methylenedioxymethamphetamine (ecstasy). Often, these drugs are used in combination as polydrug abuse. All are shown to increase the risk for engaging in high-risk sex, including unprotected vaginal and anal intercourse and sex with anonymous or multiple partners. SPECIAL AT-RISK POPULATIONS
Although the number of new HIV infections in the United States has remained fairly constant in recent years at approximately 40,000 annually, the impact continues to be disproportionate in certain populations and the epidemiology of each risk group points to the relevant social ecology.37 From 1985 to 2004, the proportion of new AIDS cases among women increased from 18% to 27%, but as it is for STIs generally, the risk is higher for African American women than other racial and ethnic groups, including approximately 21 times more for African American women than white women. Overall, in 2004, approximately half of all new cases of AIDS were among African Americans who make up approximately 13% of the United States population.38–40 Many prevention programs are being tried to combat these disparities, including turning to African American churches to spread information and understanding about the spread of HIV and The Balm in Gilead, which sponsors The Black Church Week of Prayer for the Healing of AIDS.41 Of the approximately 1 million people living with HIV in the United States, approximately 60% are MSM. Young MSM have higher rates of HIV infection than older men, and young African American MSM have higher rates than young white MSM. Studies show that younger gay men engage in more risk taking, including drug use; have higher rates of STIs, which facilitate HIV transmission; and are less likely to avail themselves of HIV testing than the general population. Throughout the world, AIDS is primarily a disease among the young. Twenty-five percent of HIV infections worldwide are in youth between the ages of 15 and 24, and in 2005–2006 almost 50% of all new HIV infections worldwide were in this group.8 This demographic group thus accounts for 5000 to 6000 new infections daily and approximately 2.3 million new cases each year. In high-income countries, young people account for approximately one third of new cases, most among young MSM. In Asia most new infections in the younger population are the result of IDU. The risk for youth is greatest in sub-Saharan Africa, which accounts for approximately two
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thirds of all AIDS in young people worldwide and where HIV prevalence reaches 40% in some communities.8,42 In these settings merely being an adolescent and entering into a sexual relationship with one person, which many in the West consider normal adolescent development, puts a young person at risk. Age of sexual debut, particularly for young women, and partnering with older men also are risk factors.43 These patterns reflect disparities in power and opportunity between men and younger women. High rates of other STIs, the relative immaturity of the genital tract in young women, and a lack of routine male circumcision also have an impact on risk. In South Africa, approximately three quarters of HIV-positive individuals between the ages of 15 and 24 are women and more than 20% of pregnant women attending prenatal clinics have HIV. More than 400,000 infants are HIV infected worldwide each year, approximately 90% in Africa, and approximately half of new infections are transmitted through breastfeeding.8 This is a tragedy that can be prevented with good prenatal care, antiretroviral therapy, HIV testing, and prevention of mother-to-child transmission of HIV services, which can reduce mother-to-child transmission of HIV to less than 2%.44–46 Sex workers are another group of people particularly affected by the worldwide social ecology of AIDS. As early as 1985, the HIV infection rate among sex workers was as high as 62% in Nairobi, Kenya, and by the late 1980s it was 89% in Abidjan, Coˆte d’Ivoire.47,48 Sex workers face many risks: large number of sexual contacts and low level of condom use, high prevalence of other STIs, and lack of access to medical services. Sex work can be direct, which means it is open and formal, or indirect, when it is hidden or informal. In many developing countries, it is a social norm for men to purchase sex and 20% to 40% of men report having done so.49–51 The overwhelming majority of women engaged in sex work are poor and poorly educated. Frequently, they have been victims of childhood violence and sexual abuse and continue sex work in an environment of exploitation, threat, and violence. Many are drug users or have sexual contact with injection drug users. The fact that sex work is illegal and socially ostracized means these women face obstacles to accessing medical services. For example, although prostitution is lawful in the former Soviet Union, it is not legal to live in Moscow without a special permit. Women from other parts of the country who come to Moscow and engage in sex work thus are there illegally and report restrictions in their access to health services. They are subject to exploitation and abuse generally, including rape, and sexual exploitation by pimps, clients, and even the police.52 Although efforts are being made to help sex workers worldwide, most programs have been implemented on a small scale and most sex workers as yet have not had access to them. To date there have been some notable programmatic successes, such as high levels of condom use in Benin, Thailand, and Cambodia, which probably have been effective in reducing the HIV rate among sex workers and by doing so probably helped to slow the AIDS epidemic in the general population.51,53 Incarceration and institutionalization also are important factors in the transmission of HIV throughout the world. In 2006 there were more than 2 million people in United States prisons, and an estimated one fourth of people living with AIDS in the United States had spent some time incarcerated. In this population the percentage of women (2.3%) who are HIV infected is higher than for men (1.7) and higher for African American (2%) and Hispanic/Latino (1.8%) populations than for whites (1%). China and the Russian Federation also have high incarceration rates, and it is assumed they have or will have HIV/AIDS epidemics in their institutions. To date, these governments have not provided what are believed reliable data on HIV infection rates in their institutions. China did not publicly acknowledge the existence of HIV/AIDS until 2001, but it is believed that approximately half of
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China’s HIV-positive population contracted the virus through IDU. This likely puts the incarcerated population at risk for an HIV epidemic, because intravenous drug use often is associated with incarceration. The risk factors associated with HIV transmission among institutionalized persons include addiction and IDU before and during incarceration, mental illness, hepatitis C and other infectious diseases, forced and consensual sex especially among MSM, and tattooing. In 1993 the WHO recommended condom distribution in prisons, but this has yet to become a widespread practice.54 It is not clear how effective condom distribution would be because coercive sex is common and many inmates would not want to be known publicly in the facility as participating in sex with other men. In 1982 it was discovered that several hemophiliacs had developed AIDS, and even though this was before the HIV had been isolated, it was presumed that the cause of their infection was receipt of contaminated blood products. This finding further confirmed the already widespread conclusion that the new immune deficiency disorder behaved in its transmission like hepatitis B and C viruses, cytomegalovirus, and other agents that are spread by high-risk sexual activity and IDU. There were national scandals in the United States, France, Japan, and Canada and a more recent scandal in China among blood donors in which unscrupulous profit-making companies reused unsterile blood-collecting equipment. In developed nations, the blood banking community responded quickly, based first and foremost on a system of voluntary donation and careful screening of donors. Although there now are effective laboratory tests to detect HIV contamination of donor units, blood bankers know that even with advances in laboratory testing, the front-line prevention against blood contamination is a voluntary system of blood donation coupled with careful questioning about relevant donor behaviors, including health status, history of receiving a transfusion or medical treatment in certain places, drug use, sexual activity, travel, and residency. There is not now and probably never will be a laboratory test for every potential blood pathogen. The result of these efforts is a success story in AIDS prevention in developed nations where HIV infection via blood transfusion is extremely rare; in the United States, for HIV-1, it is as low as 1 in 676,000 units transfused. Unfortunately, this is not the case in sub-Saharan Africa and parts of Asia, as a consequence of inadequate resources and out dated technology in the health sector.10,55
LOOKING AHEAD
Although the global AIDS epidemic probably peaked in 2000–2001, there are an estimated 4 million new cases annually and the downstream impacts of what has already occurred will be felt for generations to come.37,39 In Africa it has reversed decades of progress previously made in reducing mortality and increasing life expectancy. Although a highly protective vaccine or effective oral or topical chemoprophylaxis would greatly slow the spread of HIV to new individuals in endemic areas and new regions, recent clinical trials suggest that a successful anti-HIV vaccine will take many more years to develop. Even if chemoprophylaxis studies prove effective in decreasing HIV transmission, the daily use of medications that comes with significant costs and side effects is likely to be a holding action at best. One unavoidable conclusion from the social ecology of HIV transmission is that it is difficult to impede the spread of an infectious agent that is transmitted through pleasurable human activities—in this case sexual activity and recreational drugs. Despite billions of dollars spent on prevention programs, HIV continues to thrive in its various human niches and short of a vaccine there is no magic bullet that can combat human nature.
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So, more needs to be done with the tools currently available. The foundation for this work is epidemiology that uncovers the hot spots of an epidemic and, thereby, directs where to focus attention. There must be constant attention to prevention even among low-risk populations, however, or facing the peril of seeing a low incidence pathogen get out of hand. This is what occurred in Africa during the early days of AIDS, when governments were slow to respond and the virus was free to spread to unsuspecting people. Prevention efforts require a wide array of programs that involve mass public health education, provider-patient communication, HIV testing, linkage to care, enlisting the assistance of community leaders, and government and nongovernmental allocation of resources to keep successful existing programs well funded and to encourage new and creative ones. For each risk group there needs to be targeted interventions that deal with the behaviors and underlying causes for HIV transmission. For instance, one clear example is combating substance abuse, which is known to encourage high-risk sexual activity. Interventions would include education, treatment, and harm reduction. There also is, of course, the bigger picture that includes poverty, segregation of neighborhoods, and the culture of drug use. Another example is in the education and empowerment of women, especially in traditional societies, to provide them with the self-esteem and social backing to insist on safe sex. Even if an effective microbicide is developed in short order, it would be necessary to provide women in these settings the social tools to use it. Interventions are needed with sex workers that include changing government policies that make them vulnerable to abuse and exploitation and disease. Interventions with MSM are needed that involve the entire community, particularly in societies where gay men still are much in the closet. The lessons learned from the activism begun in the 1980s in the United States can be applied elsewhere. And, there needs to be continued focus on prevention research, including program evaluation, to understand what works and how to implement successful pilot programs on a larger scale. Even among populations studied as extensively as MSM substance users, few people are accessing substance use treatment services. In the National HIV Behavioral Surveillance System, for instance, only 16% of MSM substance users reported ever accessing treatment services.56 It is important to understand why people at risk do not access services to overcome the barriers standing in their way. This basic theme can be applied throughout. Determined government action to combat AIDS is critical. Brazil is a success story in this regard. With the end of military rule, Brazil’s democracy activists turned to public health. New constitutional language declared universal health to be a basic human right and with that efforts were made to greatly expand health services to underserved groups and regions, including the goal of providing universal access to antiretroviral drugs and ramping up HIV prevention programs. HIV prevention messages now are widely disseminated in Brazil’s public spaces, often by well-known entertainers, athletes, and models. Prevention programs, including harm reduction, reach out to high-risk groups, such as MSM, sex workers, injection drug users, and incarcerated persons. Public education helps destigmatize AIDS and encourages individuals to voluntarily partake of HIV testing and counseling. It is estimated that approximately one third of Brazilians infected with HIV know their status as opposed to only approximately 10% of those infected elsewhere in the developing world. Although the AIDS epidemic exploded in much of the developing world during the 1990s, because of effective public effort it remained stabilized and contained in Brazil.57,58 Until there is a biologic tool to prevent HIV transmission, no single type of prevention program is going to work for each at-risk population in the diverse geographic and cultural settings where HIV has found its human niche.
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