Marks, Gary; Burris, Scott*; Peterman, Thomas A.
Fifteen years after the identification of HIV, approximately two-thirds of those in the United States who are infected with the virus are aware of their seropositive status . People who are aware of their infection can decrease the risk of developing AIDS by taking antiretroviral therapy. It is less clear, however, whether awareness has decreased the risk of transmitting the virus through unsafe sex. As more people are tested for HIV, a larger proportion of all transmission will be from people who know they are infected. Reducing this transmission is an immensely important public health concern, compounded by the long period in which many seropositive people remain asymptomatic and by new medical advances that enable infected people to live longer, healthier lives [2-5]. However, there are few programs for helping these people reduce sexual risk in the ensuing years.
HIV counseling and testing remain the primary means for delivering behavioral intervention to seropositive persons tested at publicly funded testing sites [6,7]. Although counseling and testing are valuable for establishing awareness of serostatus and for providing medical referrals, they are limited in their capacity to help infected people change their sexual risk behaviors and maintain those changes. Post-test counseling is usually delivered in a single brief session shortly after test results are conveyed. This is a time when many people who have tested positive may be unprepared psychologically or limited in their motivation or ability to assimilate prevention messages. For the most part, people who test positive for HIV must draw on their own internal resources (e.g., felt responsibility to protect others) in their attempts to change their behaviors. Seropositive people are asked to behave in ways that minimize the likelihood of transmitting the virus and to be accountable for their actions. Prevention efforts must also provide the social conditions that encourage and reinforce safe behavior.
In this review, we examine sexual risk-taking of seropositive persons and discuss the roles of personal and collective responsibility for reducing transmission of HIV. First, we describe findings of studies that have examined sexual risk behaviors of seropositive adults. Second, we consider some of the psychological factors associated with risky sex in this group and whether and how interventions aimed at increasing a sense of personal responsibility to avoid transmitting HIV may enhance prevention efforts. Although some commentators have suggested that the normalization of HIV infection has substantially reduced the social barriers to responsibility-based messages , others have more cautiously pointed to the need for more research and reflection . Third, we discuss the role of collective responsibility in HIV prevention efforts. Policymakers, researchers, and citizens alike have an obligation to help combat the HIV/AIDS epidemic. Social attitudes, norms, and practices, both within risk populations and in the broader society, influence behavior that spreads disease. Insufficient attention to the ecology of HIV prevention limits the effectiveness of individual-level interventions and hinders the development of interventions to address directly the social forces that provide too many incentives for risk and too few rewards for safety.
Prevalence of unsafe sex
Most adults are sexually active. If anything, people who have contracted HIV have been more sexually active than people who remain uninfected. Many of those with HIV infection do change their sexual practices after testing positive . Nevertheless, studies indicate that more than 70% of seropositive men and women engage in oral, vaginal, or anal sex after they become aware they have HIV [11-15] and that the probability of sexual activity increases with the length of time since they tested seropositive (unpublished data).
Some infected people do not reveal their serostatus to their sex partners. Of HIV-positive adults (mostly men), 30% had not informed any past partners, and 29% had not informed any current partners even after an average of 6h of counseling over 2 years . Another study found that 52% of sexually active HIV-positive men kept their infection status secret from one or more sex partners . The prevalence of disclosure is somewhat higher among seropositive women than men , stemming in part from the fact that women have fewer sex partners [18,19]. As the number of partners increases, the likelihood of informing any of them decreases [16,20]. Most seropositive men and women disclose their status to primary sex partners [21-26], but disclosure to other partners is less likely [19,26]. The HIV serostatus of the partner also influences disclosure: seropositive men who have sex with men (MSM) who engaged in anal intercourse informed 86% of HIV-positive partners, 46% of HIV-negative partners, and 18% of partners whose serostatus they did not know . Disclosure is associated with an increased likelihood of protected sex with uninfected partners .
Table 1 presents findings of studies that have examined the prevalence of unprotected anal or vaginal intercourse amongst HIV-positive adults. Although the varying recall periods for the self-reports make comparisons difficult, a sizable percentage of seropositive men and women engage in unprotected sexual intercourse after they learn they are infected. The studies would overestimate transmission risk if unprotected sex occurred primarily with other infected persons. HIV-positive MSM have been found to be three times more likely to have engaged in unprotected insertive anal intercourse with HIV-positive partners than with other partners . The results of other studies are similar [11,13,14,32,33,37-39]. In these partner-specific analyses, only 35-45% of the partners were seropositive; thus, many of the other partners may have been placed at risk.
Undoubtedly, most seropositive people feel a unique sense of responsibility to protect sex partners . They know that it is wrong to endanger others by exposing them to HIV without their knowledge. This is most evident when there is emotional involvement with a partner and commitment to an ongoing relationship. Indeed, disclosure of seropositive status and protected sexual activity are most likely to occur when there is commitment to partners at risk for infection, and least likely to occur with casual partners of unknown serostatus . The desire for intimacy and sexual pleasure may, at times, overcome motivation of serodiscordant couples to use condoms during sexual intercourse . Nevertheless, just as committed relationships and reduction in the number of sex partners protect against contracting HIV, they protect against transmitting the virus. Sexual partnerships of two seropositive persons also protect against infecting others.
In sexual encounters with casual partners, good intentions may not always be translated into protective behavior. Some infected persons may want to disclose and feel that it is the right thing to do but may reason that their physical appearance, preferred sex activities, or nonverbal cues (e.g., leaving medication or printed materials in plain sight) constitute disclosure. Direct disclosure is often difficult; it may stigmatize a person and precipitate other negative outcomes (e.g., refusal to have any type of sex). Some infected persons who withhold disclosure may attempt to protect partners by using a condom or by restricting the range of sexual activities. Nevertheless, keeping one‚s seropositive status secret keeps the partner from making an informed decision about risk and deters honest communication and negotiated behavior.
The responsibility to protect others can become psychologically and behaviorally challenging. Some infected people may question why they are the ones who must shoulder the responsibility for protecting others and may cognitively shift the responsibility to the partner. This cognitive shift may be initiated and reinforced by general prevention messages such as, ‚everyone who is sexually active should use a condom.‚ It may serve to rationalize high-risk acts and alleviate feelings of guilt or anxiety. Some infected persons may reason that partners who are willing to forego condoms have accepted the risk that they may be exposed to the virus and so do not need to be notified or protected.
Shifts in responsibility to protect may be influenced by the psychological states of infected persons. Anger, anxiety and tension may promote psychological overload that may trigger motivation to escape the aversive psychological state as well as the burden to protect partners [39,41]. Motivation to escape may induce a person to make external attributions of responsibility for protection (i.e., more responsibility attributed to sex partners than to self) or to use drugs before sex. These escape mechanisms may increase the likelihood of unprotected sexual intercourse . Importantly, negative affect and motivation to escape are not conducive to processing, assimilating, or acting on prevention messages. Receptiveness to those messages may be increased by interventions that help seropositive people maintain positive affective states. When people feel good about themselves and feel respected, they may be more likely to accept responsibility for their actions, more likely to orient themselves to the future, and more likely to consider the consequences of their behaviors [42-44].
The importance of responsible behavior has been a major feature of post-test counseling, and its underlying value of preventing further HIV transmission may be widely accepted by most seropositive people. But messages about personal responsibility to protect others can easily be perceived as victim blaming that only enhances the stigma of the disease and lessens the motivation to protect others. Such messages and the perceptions of social hostility they may engender can also have the broader effect of polarizing the political climate in which prevention messages are offered. We strongly believe that all infected people should receive a dual-theme message that emphasizes protecting their own health as well as that of their partners. This type of message has been featured in some brochures and literature for HIV-positive persons [45-47]. The issue of self-protection has surfaced strongly in the context of combination antiretroviral therapies. It is important that infected people gain access to these therapies and adhere strictly to prescribed treatment regimens. Adherence can lower viral load, help prevent drug resistance, and significantly improve health and prolong life [2-5]. Similarly, seropositive people who adhere to safer-sex guidelines protect themselves. Unsafe sex can lead to secondary infections (e.g., syphilis, gonorrhea, herpesvirus associated with Kaposi‚s sarcoma) that may accelerate disease progression [48-52] and heighten the infectiousness of HIV [53,54]. This type of self-protective message may be quite powerful when communicated to HIV patients by their health-care providers.
Individual-level approaches to prevention
Messages about self-protection and social responsibility to protect others are needed now more than ever, because the success of medical treatments may have unintended behavioral consequences for HIV prevention. Lowering viral load and keeping it low may reduce the likelihood that a seropositive person may infect a partner during sexual contact [55-57]. However, as treatment options enable people with HIV infection to live longer and feel healthier, those people may become more sexually active. Those who believe that low viral load renders them non-infectious may stop using condoms. Furthermore, as therapeutic successes are publicized, people‚s perceptions of HIV disease may change. What was once viewed as an acute and fatal disease may now be viewed as a chronic, manageable and survivable disease . These perceptions may increase sexual risk behaviors among infected and uninfected people. Recent studies suggest that optimism about the new HIV therapies is associated with sexual risk-taking in MSM [58-60]. Moreover, people at risk for infection may increasingly turn to HIV therapy as a perceived prophylaxis after possible sexual exposures to the virus .
Prevention messages for seropositive people and interventions for reducing sexual risk behaviors can be implemented in public clinic settings and managed care facilities. The HIV outpatient clinic is an ideal, yet underused, setting for delivering prevention messages and addressing individual behavior change. The setting provides an opportunity to reach a large number of seropositive people, to integrate behavioral intervention into routine medical care, to provide ongoing counseling and support, and to involve clinic staff (e.g., nurses, physicians, social workers) in prevention activities. Sexually transmitted disease (STD) and tuberculosis clinics afford the same opportunities. Recently published findings are encouraging. HIV-positive patients who reported that clinic staff had discussed the issue of disclosure with them were more likely than other HIV patients to have informed uninfected sex partners of their risk . These intervention opportunities hinge on seropositive people‚s access to care and on the capacity and ability of health-care workers to provide such messages.
Clinics provide an environment for developing and reinforcing attitudinal and behavioral norms for safer sex. The use of peer leaders in gay bars has promoted shifts in sexual attitudes and behaviors [62-64]. Safer sex norms can be promoted in clinics through visual cues (posters in waiting rooms and medical examining rooms), printed information, communication from providers, and a more open discussion with patients about disclosure and sexual risk. Complementary approaches can be instituted at community-based organizations (e.g., AIDS service organizations).
Finally, client-centered approaches to counseling also show much promise. Brief client-centered counseling has reduced the risk for new infections in people attending STD clinics  and may be effective in HIV clinics as well. The counseling involves working with patients to establish achievable steps they can take to reduce their risk behavior. Social workers, nurses, and physicians can easily conduct this type of intervention after proper training. At the very least, health-care providers must be able to recognize the need for, and believe in the value of, behavioral intervention and appropriate referrals.
Social aspects of individual choice
So far we have focused on some of the ways in which seropositive persons may cope with their infection. This focus posits the HIV-seropositive diagnosis as a profound event in a person‚s life. Learning one‚s seropositive status no doubt has powerful psychological and behavioral consequences. However, no matter how well we understand a person‚s cognitive and affective processes, the effectiveness of individual-level interventions is limited by the social forces impinging on a person.
The environmental factors that encourage sexual risk-taking remain largely unchanged for infected people and may foster unsafe sex after the seropositive diagnosis. This is a familiar problem in public health: interventions aimed at using diagnostic information to influence an individual‚s behavior have the advantages of salience and motivation but often call upon the individual to make changes in behavior that may be inappropriate to and unsupported in his or her social setting . Rotello, in his account of gay sexual ecology, argued just this point . He described how communities exhibit a powerful system of social rewards for practicing risky sex and having multiple partners, despite strong efforts by some within those communities to encourage risk reduction. The same may be said for heterosexuals infected with HIV. Their decisions about using condoms, about substance use, and about the responsibility of partners to each other are heavily mediated by complicated community norms . We know even less about this sexual ecology than we do about the ecology of gay men [69,70].
Gay and heterosexual communities are nested within the larger society. Their norms of sex and partnering reflect the culture as a whole and the social policies that sustain it . To point to the protective value of long-term stable relationships is to highlight the fact that American social policy has prevented such relationships among gay men. Gay sexual behavior has been shaped by social hostility toward homosexuality and by the use of law and other forms of social control to express that hostility . Gay men can still be prosecuted in some states for having sex and, in all but 10 states and the District of Columbia, a person living openly in a gay relationship has no protection from discrimination [73,74]. The stigma of homosexuality has been linked to risky behavior [75,76]. Acculturation into the gay community may reduce risky sex , but stigma and social hostility keep many MSM closeted and cut off from social support networks.
Social attitudes toward and policies concerning homosexuality have also influenced gay sexual behavior by omission. A huge array of legal rules and social practices provide incentives to most heterosexuals to form relationships that are intended to be permanent and monogamous. Through the civil status of marriage, heterosexual couples acquire tangible economic benefits ranging from favorable rules of property ownership and inheritance, to insurance benefits, to parental rights. Virtually all of these are denied to gay men and lesbians .
Heterosexual behavior is also influenced by social attitudes and policies. Heterosexuals with HIV infection tend to be poor and are disproportionately members of minority groups . In these communities, a complex set of economic and social policies may discourage marriage and endanger stable family groups [79,80]. Not the least of these are law enforcement policies that incarcerate poor black men at a staggering rate , shrinking the pool of available partners for women in communities at risk . The epidemic among heterosexuals has also been shaped powerfully by policies creating a shortage of safe injection equipment  and more broadly by a preference for interdiction and imprisonment over treatment for the nation‚s drug abuse problem [84,85]. Furthermore, the absence of a strong campaign to promote a norm of condom use [86,87] in the face of evidence that condom use protects men and women from HIV infection is yet another instance of the public health effect of society‚s difficulty addressing issues of sexuality . In broadest perspective, gender, poverty, race, and homophobia represent ‚fundamental social causes of disease‚, which should be recognized and addressed in public health work .
Taking collective responsibility for HIV prevention
The concept of collective responsibility emphasizes that all of us, infected or not, low risk or high, bear a responsibility to change our attitudes and behaviors that may promote HIV infection. Without this balance, calls for personal responsibility become almost indistinguishable from that of blaming the victim and are likely to be counterproductive to prevention efforts. Thus, it is important to distinguish between two general HIV prevention strategies: (i) individual strategies that support infected persons coping with their disease and social circumstances, and (ii) ecological or population strategies that try to modify the group norms, social practices, and laws that influence a person‚s attitudes and behaviors [66,71,90,91]. These strategies are complementary, in that changes in individuals contribute to changes in populations and vice versa. Furthermore, each approach provides useful insights to the other . They are distinct, however, in their primary focus (individual versus population) and in the sort of social science theory they rely upon.
Individual approaches to HIV prevention have become steadily better at identifying the social forces that beset people with HIV infection and helping them reduce risk behaviors in spite of those forces . Tools such as social cognitive theory  and the theory of planned behavior  can effectively model how people respond to social stimuli, and have made a tremendous contribution to HIV prevention. In these models, however, social and community factors (e.g., norms, economic conditions, laws) are seen as inputs in the cognitive processes of individuals . These theories do not undertake to explain the nature and development of social factors themselves. For that we need to look to a different body of social science work [71,90].
Ecological strategies address the social conditions in which individuals make their choices. Research and intervention at the population level complement individual strategies, both by improving the conditions with which individuals must cope and by equipping behavioral strategies with sophisticated accounts of the social forces affecting individuals. Ecological interventions seek to change structural factors inhibiting health, such as laws, public policies and institutional practices [96,97]. They also address less tangible but equally powerful cultural factors (norms, attitudes, values) through ‚the regulation of social meaning‚ [98,99], the use of law, social marketing and other tools of state power to change how people think. Thus, for example, a law protecting gay people from discrimination not only changes the structure of legal rights and protections in a community, but also expresses the idea that discrimination based on sexual orientation is ‚bad‚.
Of course, the importance of social factors in health is frequently noted [96,100]. Prevention research and programs that focus on altering community norms and practices cover a range of health threats, including smoking , diet , binge drinking , and lack of sunscreen use . We see similar approaches in HIV control , including the Community Demonstration Projects  sponsored by the US Centers for Disease Control and Prevention, efforts to change norms of sexual behavior in gay bars [62-64], and the Thai condom campaign . However, integrating interventions and research aimed at community and particularly social-level change into HIV prevention continues to be difficult and continues to happen all too rarely . The problem for prevention professionals lies not in recognizing in a general way that social conditions heavily influence health and behavior, although this claim can be politically controversial , but in finding ways to directly intervene at the population level in ways that are both effective and acceptable. Preventing HIV transmission by people who are infected is an important occasion for addressing this problem.
The conditions that impede wider use of population strategies are widely recognized. Those strategies frequently bring to the forefront deeply rooted social disputes over matters such as sexuality, drug use, race and poverty [88,109]. Attempts to change the social meaning of unhealthy behavior (i.e., making smoking seem ‚uncool‚, or condom use more ‚cool‚) are often perceived as paternalism or a government endorsement of deviance [99,110]. Furthermore, it is extremely difficult to study ‚meaning‚ as it emerges from and feeds back into the dynamics of social interaction . Given these complications, ecological strategies can easily seem to falter before the key public health question of whether they will be effective in preventing HIV given the resources available.
Although they are useful to think about, none of these objections is sufficient to overcome the factors militating towards a more widespread and effective deployment of ecological strategies to prevent HIV infection. It must be recognized that individuals and groups influence the environment all the time. Government, the private sector, and communities have created the conditions that have facilitated the spread of HIV infection. Moreover, deliberate efforts to change the ecology of HIV transmission have been part of the campaign against HIV from early in the epidemic. Closing or regulating bathhouses was intended to change the environment fostering unsafe sex and HIV transmission, and at least some of the controversy it occasioned was perceived as expressing collective disapproval of homosexuality . In some instances, state governments have used their power to try to regulate the social meaning of HIV-related behavior. For example, they have tried to encourage people to get tested for HIV by establishing privacy and anti-discrimination laws that attempt to protect people who test HIV-positive . Communities have tried to disassociate condom use from either the confession or accusation of an STD by propagating what has been called the ‚code of the condom‚ . Communities have also tried to reduce the political opposition to increasing the supply of sterile injection equipment by transforming needle exchange from paraphernalia delivery to harm reduction. Criminal transmission statutes have been enacted that supposedly ‚send a message‚ that unsafe sex is wrong. Some of the efforts, such as criminalizing sexual behavior, are bad ideas , but even the good ones have probably been pursued with less rigor than is possible. One of us (S.B.) has argued, for example, that the effort to use privacy and anti-discrimination law to reduce the social risks of HIV testing has not been sufficiently supported by research on the social concerns that deter testing and how law can be used to address those concerns . Clearly, the question is not whether to deploy interventions that aim directly at changing structural and cultural factors promoting HIV, but how to do so effectively.
In our view, the status of ecological approaches to preventing HIV infection today is analogous to the status of behavioral approaches a decade ago. There is a well-developed and diverse literature on structural causes of disease , on social epidemiology [116,117], on the social construction of disease and health [88,100], and on ways in which social norms, practices and conditions emerge to shape the individual and society [90,118]. Ecological strategies have been applied in public health generally and in HIV, but not systematically and not within a well-supported, deliberate effort to put theory to immediate public health use. Such a project would, amongst other things, study how interventions aimed at changing the social meaning of behavior have worked in other health campaigns, such as those against smoking or drunken driving, as well as major social changes such as the effort to eliminate racial discrimination. It would build stronger collaborative links on at least two axes: (i) within the research community, between people in different disciplines that focus on different levels of analysis; and (ii) between researchers and ‚consumers‚ of research (policymakers, advocates, communities) to ensure that the things consumers know and are concerned about appropriately influences research. It would examine and find ways to support health-promoting leaders and institutions in communities at risk. It would take as a major task enhancing public health‚s capacity to practically foster structural and cultural changes through law, policy and social marketing. Better methods could go a long way towards eliminating what might be referred to as the ‚social nihilism‚ that regards any effort to deliberately address community and social factors as hopelessly impractical.
Table 2 presents a number of individual and population-level measures that can plausibly be predicted to help prevent HIV transmission. We cannot prove that they will do so, nor do we mean to imply that changing the social ecology is simple or even fully within our capacity to accomplish. On the contrary, the problem posed for public health by ecological interventions is the necessity of acting without having full information. Public health as a scientific discipline requires the use of theory and research methodologies to constantly assess our premises. Public health as a source of leadership in social change requires us to bring that technical expertise and analytic rigor to bear on decisions that cannot await better data, and so ultimately depend upon intuition and political compromise .
People who have HIV infection bear both a practical and an ethical responsibility to help control the spread of HIV through their sexual behavior. Behavioral interventions are making a significant contribution to lasting behavior change among people with HIV, and may be enhanced with the integration of messages of personal responsibility. However, this personal responsibility is inseparable from the collective responsibility to create the conditions in which both seropositive and seronegative people can make healthy choices. Fulfilling this collective responsibility for individual health depends in part on material factors such as full access to high-quality health care. It depends on changes to environmental and policy conditions such as lack of access to safe injection equipment, insufficient availability of drug abuse treatment, and legal barriers to stable emotional relationships. Fulfilling society‚s responsibilities will also require changes in what all of us do: both the uninfected and the infected must model and support each other in safer behavior. Among researchers and policymakers, a major, concerted effort to develop a better understanding of social forces is necessary to develop interventions that will address HIV at the individual, social, and community levels in a way that is both effective and acceptable.
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