3
Understanding the Determinants of HIV Risk Behavior

Human behavior is determined by multiple factors in individuals and the environment. These factors occur at the micro-level (molecular and biological) and the macro-level (social and environmental) and often interact in mutually reciprocal relationships. The behaviors most closely linked with the epidemiology of AIDS—sexual contact and the injection of addictive drugs—are intense, intimate, and strongly driven. Approaching them requires a cross-disciplinary effort that should include refined knowledge of their neurobiological, psychological, and social bases, and the manners in which they interact.

This chapter presents an overview of findings and gaps in research on the determinants of HIV risk behavior and the application of that research to AIDS preventive interventions. This research constitutes a significant portion of the AIDS programs at NIAAA, NIDA, and NIMH.

NEUROBIOLOGICAL DETERMINANTS OF RISK BEHAVIOR

As reviewed later in this chapter, much has been learned from research on the psychosocial determinants of AIDS-related sexual and drug-using behaviors. However, research on the brain biology of sexuality and drug addiction has rarely been integrated into these studies, even though it may be critical for understanding and preventing highrisk behavior. Even to begin approaching the



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Aids and Behavior: An Integrated Approach 3 Understanding the Determinants of HIV Risk Behavior Human behavior is determined by multiple factors in individuals and the environment. These factors occur at the micro-level (molecular and biological) and the macro-level (social and environmental) and often interact in mutually reciprocal relationships. The behaviors most closely linked with the epidemiology of AIDS—sexual contact and the injection of addictive drugs—are intense, intimate, and strongly driven. Approaching them requires a cross-disciplinary effort that should include refined knowledge of their neurobiological, psychological, and social bases, and the manners in which they interact. This chapter presents an overview of findings and gaps in research on the determinants of HIV risk behavior and the application of that research to AIDS preventive interventions. This research constitutes a significant portion of the AIDS programs at NIAAA, NIDA, and NIMH. NEUROBIOLOGICAL DETERMINANTS OF RISK BEHAVIOR As reviewed later in this chapter, much has been learned from research on the psychosocial determinants of AIDS-related sexual and drug-using behaviors. However, research on the brain biology of sexuality and drug addiction has rarely been integrated into these studies, even though it may be critical for understanding and preventing highrisk behavior. Even to begin approaching the

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Aids and Behavior: An Integrated Approach putative biology of highrisk behavior, including certain sexual behaviors and drug use, requires an expanded basic knowledge base. With respect to sexuality, characterization of sexual dimorphism at the genomic, molecular, cellular, and behavioral levels is still in its early stages. Whether and how it may relate to the drive to engage in specific, highrisk sexual behavior is not known, but it should at least be explored. Similarly, although much has been learned about the biology of substance abuse, further elucidation of molecular and cellular mechanisms underlying addictive behavior may assist in the development of new therapeutic approaches to addiction, which in turn may profoundly alter the AIDS epidemic. Recent neuroscience investigations have contributed to knowledge about the biology of sexuality. However, to date most research has focused on the sexually dimorphic nature of the brain (e.g., how aspects of synaptic architecture differ in males and females) (Raisman and Field, 1971) and on potential neuroanatomical correlates of homosexuality in men (Gorski et al., 1978; LeVay, 1991). Extensive studies using experimental animals have identified specific pathways and centers in the brain and spinal cord involved in sexual responses among both males and females (Gorski, 1988; Gorski et al., 1978; Johnson, Coirini, Ball, et al., 1989; Johnson, Coirini, McEwen, et al., 1989; McEwen, Luine, and Fischette, 1988; Meisel and Pfaff, 1985; Parsons et al., 1982; Pfaff and Reiner, 1973; Pfaff and Sakuma, 1979; Pfaff and Schwartz-Giblin, 1988; Sar and Stumpf, 1975). Experimental animal studies have provided a rather detailed account of the neural and hormonal bases of a spectrum of sexual behaviors. However, it remains unknown if and how neuroanatomical and genetic factors in sexuality translate into sexual risk behavior. Indeed, the biology of sexual risk taking is a missing element in basic biomedical and neurobiological AIDS research. Some outstanding issues include: identifying the neurochemical molecular substrates, if any, associated with sexual risk taking; determining how insights from the studies of the neurobiology of sexuality would relate to highrisk sexual behavior and to sexually transmitted diseases, including AIDS; and determining how society might best integrate the study of the biology of sexuality and sexual risk taking into the broader context of sexuality, sexual behavior, and sexually transmitted diseases.

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Aids and Behavior: An Integrated Approach NEUROBIOLOGICAL BASIS OF DRUG-USING BEHAVIOR Understanding the biological basis of drug addiction is an important link to understanding drug abuse behaviors, and unlike the biology of sexuality has been the object of a great deal of research. (However, it may be less useful in understanding highrisk drug use such as sharing injection equipment.) The possible link between alcohol and highrisk sexual behaviors has also become a subject of more intense research in recent years. The addiction syndrome consists of physical dependence, psychic dependence, and tolerance (Koob and Bloom, 1988). Physical dependence is considered to be an adaptive state resulting in profound physiological disturbances upon withdrawal of drug administration. Psychic dependence has been associated with the behaviorally reinforcing properties of the drug, resulting in a sense of satisfaction and a drive requiring continued administration to produce pleasure and avoid discomfort (Koob and Bloom, 1988). Tolerance is the requirement for progressively higher drug doses for a given effect with chronic use and appears to have a major learned component (Chen, 1979; LeBlanc, Gibbins, and Kalant, 1973; Schuster, Dockens, and Woods, 1966; Siegel, 1976, 1978; Siegel and Sdao-Jarvie, 1986; Wenger et al., 1981). Recent studies on the cellular and molecular basis of dependence and tolerance suggest that the processes are separate and distinct and are mediated by different brain systems (Koob and Bloom, 1988). Traditional models of addiction suggest that one set of unspecified brain mechanisms mediate the primary, reinforcing, hedonic (pleasure-seeking) aspects of drug abuse and that, with time, a second ''adaptive" set of brain mechanisms antagonizes the first, necessitating higher doses to get the same subjective effect. The brain's adaptive response, however, also leads to a physiological reaction if the drug is withdrawn (Collier, 1980; Himmelsbach, 1943; Jaffe and Sharpless, 1968; Martin and Sloan, 1977; Solomon, 1977; Tabakoff and Hoffman, 1988). Contemporary studies are beginning to define the molecular and cellular bases of some of these well-known clinical phenomena. Identification of opioid peptides (short proteins produced by nerve cells that bind to the same receptors as heroin and other opiate drugs) and mapping of their pathways in the brain have contributed an enormous amount of new data about the biology of opiates, including heroin (Bjorklund and Lindvall, 1984; Bloom, 1983; Khachaturian et al., 1985; Merchenthaler and Maderdrut, 1985). Some of the structures associated with addiction are now

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Aids and Behavior: An Integrated Approach being defined at the molecular level. Decades of clinical research on opiate addiction have recently been augmented by the molecular cloning of opioid receptor molecules. There are three major categories of receptors (mu, kappa, and delta), each of which has at least two subtypes. Molecular genetics has begun to separate the various classes and subclasses of opioid receptors, and their structures can be used to identify and perhaps even to deliberately design drugs to further improve the treatment of opiate addiction (IOM, 1994). Cocaine addiction is less well understood than opiate addiction, but here too progress has been dramatic in recent years. It has been apparent for some time, for example, that dopamine-containing neurons are required for the primary reinforcing effects of psychostimulants such as cocaine and amphetamines (Goeders and Smith, 1983; Lyness, Friedle, and Moore, 1979; Roberts, Corcoran, and Fibiger, 1977; Roberts and Koob, 1982; Roberts et al., 1980; Routtenberg, 1972). Details of biologic mechanisms may be illustrated by focusing on cocaine, which, along with heroin, plays a pivotal role in the AIDS epidemic. Dopaminergic neurons of the ventral tegmentum and their pathways that innervate limbic and frontal cortex are essential for the acute reinforcing actions of cocaine (Goeders and Smith, 1983; Lyness, Friedle, and Moore, 1979; Pickens, Meisch, and Dougherty, 1968; Roberts, Corcoran, and Fibiger, 1977; Roberts and Koob, 1982; Roberts et al., 1980; Routtenberg, 1972; Yokel and Wise, 1975, 1976). Considerable evidence suggests that cocaine acts by inhibiting the reuptake of dopamine by nerve cells (Ritz et al., 1987). That is, dopamine is normally released by one nerve cell and binds to its nearby neighbor. The nerve cell that releases the dopamine also has a molecular pumping system that recovers a fraction of the dopamine released. Cocaine inhibits this molecular pump, thereby increasing the amount of dopamine available to bind to the second nerve cell and also keeping levels high for longer periods. Inhibition of reuptake thus prolongs and intensifies dopamine actions. Inhibition of reuptake has been documented in the limbic nucleus accumbens and produces reinforcing actions. The increased available dopamine appears to elicit reinforcement by specifically stimulating D1 and D2 dopamine receptor subtypes (Koob, Le, and Creese, 1987; Woolverton, 1986). In sum, the specific transmitter (dopamine), the molecular reuptake transporter (the molecular "pump"), and the specific receptors involved (subtyped D1 and D2) have been associated with cocaine addiction. Each of these molecules constitutes a potential target for new therapeutic agents.

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Aids and Behavior: An Integrated Approach The actual anatomical circuits in the brain that participate in the addictive process have been identified in some detail, although the story is not yet complete. Ventral tegmental dopaminergic nerve cells lead to the nucleus accumbens, which in turn projects to the ventral pallidum. Pallidal fibers innervate the pedunculopontine nucleus and dorsal medial thalamus, which are thought to mediate motor activation in experimental animals (Koob and Bloom, 1988). These pathways appear to play critical roles in cocaine-induced arousal-reinforcement. The neuroanatomic and molecular bases of the withdrawal syndrome are less clearly understood (see Koob and Bloom, 1988, for review). Chronic drug use is presumed to result in compensatory, adaptive responses that antagonize the positive, reinforcing drug actions, but details of this adaptive response are not yet clear. Drug withdrawal presumably leads to the unopposed actions of the antagonistic mechanisms resulting in adverse effects, including malaise, dysphoria, and anhedonia. Additional studies are required to define the biology of the withdrawal syndrome and associated behaviors. Neuroscience has now presented an opportunity to begin approaching the treatment of addictive drugs, including those used by injection and thus associated with HIV transmission such as heroin and injectable cocaine. Methadone has long been a successful treatment that can prevent injection of opiate drugs. Indeed, one of the principal rationales for developing new antiaddictive medications is the high mortality associated with both opiate and cocaine addiction, to which the risk of AIDS is an important contributor. In 1993, the Food and Drug Administration also approved levo-alpha-acetylmethadol (LAAM) to treat opiate addiction, and several other compounds are in clinical testing (IOM, 1994). The isolation of dopamine transporter and receptor molecules also will provide specific targets for drug development, although it is not yet clear whether or not affecting these molecular pathways will address the craving associated with cocaine addiction, and so an effective medication to combat cocaine may require substantial further advances in basic neuroscience (IOM, 1994). It may be some time before an antiaddictive medication to treat cocaine addiction, similar to methadone and LAAM in effectiveness against opiate addiction, can be found. In the long run, however, the combined efforts of neuroscientists studying the molecular, anatomic, and behavioral aspects of cocaine will very likely produce promising leads with direct treatment implications. These new molecular insights now allow entirely new approaches

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Aids and Behavior: An Integrated Approach to the biology of addiction. The scientific community faces a remarkable opportunity to combine biological and psychosocial approaches to treat addiction, reduce the factors that initially encourage abuse, and help to address a critical mode of HIV transmission. Prevention of transmission through a reduction in drug abuse is a potentially realistic goal best achieved through cross-disciplinary research. PSYCHOSOCIAL DETERMINANTS OF RISK BEHAVIOR More than a decade into the AIDS epidemic, efforts to change sex and drug using behaviors to reduce transmission of HIV have met with limited success. Sexual risk taking in the general population assessed in a limited number of studies appears to be substantial, and there is evidence that preventive behaviors have not generally been adopted. For example, a national probability study of the general heterosexual population of the United States found that condom use was low. Only 17 percent of those with multiple sex partners, 12.6 percent of those with risky sex partners, and 10.8 percent of untested transfusion recipients used condoms all the time (Catania et al., 1992). These data also suggest that the U.S. population as a whole has failed to incorporate prevention messages into sexual behavior. In fact, a consistent observation from many studies is that many of those at risk for HIV infection—whether through sex or drug use—do not recognize the danger they face (Brunswick et al., 1993; Klepinger et al., 1993; Kline and Strickler, 1993) and that, even when they do, knowledge alone is not enough to effect behavior change to reduce their risks. Understanding the resistance to as well as the motivation for behavior change is essential for designing effective AIDS prevention interventions. Basic and applied psychological and social research have contributed much to an understanding of the psychosocial and cultural determinants of HIV risk behavior. PSYCHOSOCIAL PERSPECTIVES ON RISK BEHAVIOR Theoretical models (primarily psychological) that dominate studies of HIV risk behavior fall into two major groups: those that predict risk behavior and those that predict behavior change. Models that predict risk behavior attempt to identify variables that explain, for example, why some members of a given population perform a given behavior at a given time while others do not (Fishbein et al., 1991). Models that predict behavior change focus on stages

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Aids and Behavior: An Integrated Approach through which the individual may proceed while attempting to change behavior (Fishbein et al., 1991). A third set of theoretical issues is raised by the maintenance of safe behavior once such behavior has been initiated. Early in the HIV/AIDS epidemic the Health Belief Model (Becker, 1974; Maiman and Becker, 1974; Rosenstock, 1974) and the Theory of Reasoned Action (Ajzen and Fishbein, 1977), which had been developed to explain health behaviors, were widely used to identify determinants of HIV risk behavior. The application of these models focuses on perceived susceptibility, perceived benefits, constraints to behavior, and intentions to behave in particular ways, such as using condoms, in the context of HIV risk. Social Cognitive Learning Theory (Bandura, 1977), which in its early years was used to help people overcome phobias, also has been applied to HIV risk behavior. Its central concepts are those of "modeling" and "efficacy beliefs." Modeling is the process by which people are influenced by observing others. Efficacy beliefs include outcome (or response) efficacy, which is the belief that a given behavior will result in a given outcome (e.g., a belief that wearing a condom will prevent HIV transmission), and self-efficacy, which is the individual's belief that he or she can effectively carry out a desired behavior in a particular setting (e.g., successfully negotiate the use of a condom during a sexual encounter). In recent years self-efficacy has been viewed as the key social cognitive learning variable in predicting risk behavior. By the mid-1980s most models of behavioral performance included an amalgam of variables from health belief models and social cognitive learning theory. This amalgamated theory tends to assume that individuals who formulate an intention to behave in a particular way and have the skills and self-efficacy beliefs to do so are likely to carry out the intended behavior. Many of the intervention studies reviewed below are influenced by these models and use variables from this amalgamation, especially variables assessing susceptibility, skills, and efficacy. PSYCHOLOGICAL THEORIES OF BEHAVIOR CHANGE Behavior change is a process, and as such we need models that can describe the process and identify benchmarks along its way. Stage theories of behavioral change provide researchers with tools for identifying these benchmarks so that interventions can be tailored to the place in the process that a group or community has attained with the goal of advancing them from that place. A

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Aids and Behavior: An Integrated Approach successful intervention, therefore, might not result in the elimination of a risk behavior. Instead, a successful intervention is one that advances an individual or group from one stage to another. Two stage models of change have been adapted for use with HIV risk behavior: the AIDS Risk Reduction Model and the Stages of Change Model. The AIDS Risk Reduction Model (ARRM) (Catania, Kegeles, and Coates, 1990) incorporates elements of the health belief and social cognitive learning models to describe the process through which individuals change their behavior. A goal of this model is to understand why people fail to progress over the change process. ARRM highlights three stages in the change process: Stage One is labeling highrisk behavior as problematic, which incorporates the notion of susceptibility from the health belief models. This involves knowing which sexual activities are associated with HIV transmission, believing that one is personally susceptible to contracting HIV, and believing that having AIDS is undesirable. Stage Two is making a commitment to changing highrisk behaviors, which includes weighing costs and benefits, and evaluating response efficacy, incorporating the efficacy concept from social cognitive learning theory. Stage Three is seeking and enacting solutions, that is, taking steps to actually perform the new behavior and then performing it. This enactment is influenced by social norms and problem-solving options, and it may include seeking help. The Stages of Change Model (Prochaska, in press; Prochaska and DiClemente, 1983; Prochaska, DiClemente, and Norcross, 1992), formally called the Transtheoretical Model, was developed in the context of psychotherapy and has only recently been applied to HIV risk behavior. The Centers for Disease Control and Prevention, for example, is using the model in its AIDS Community Demonstration Projects, which target hard-to-reach groups at risk for HIV infection (O'Reilly and Higgins, 1991). This model posits four stages of change: Precontemplation, in which the individual does not intend to change behavior within the next six months; Contemplation, in which the individual intends to change behavior within the next six months; Preparation, in which the individual is seriously planning behavior change within the next 30 days, has made some attempt to modify behavior, but has not yet met a specific criterion (such as always using condoms); and Action, in which the individual has modified a behavior and met a specific criterion for less than six months. Maintenance is used to describe the period in which the individual continues the behavior change beyond six months. Movement through these stages

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Aids and Behavior: An Integrated Approach does not always occur in a linear manner. Individuals often must make several attempts at behavior change before they achieve their goals. The efficacy of an intervention program to change behavior requires a good fit between the stage the individual is in and the stage that the intervention targets. The model specifies ten cognitive, affective, and behavioral strategies and techniques people use as they progress through the stages of change over time. These strategies and techniques include consciousness raising, in which the individual's level of awareness is heightened; self-reevaluation, which is the individual's reappraisal of his or her problem; social reevaluation, which focuses on the impact of a problem on others; self-liberation, which acknowledges the role of choice in behavioral change; social liberation, which involves changes in the environment that lead to more options for the individual; counter-conditioning, which changes the conditional stimuli that control responses; stimulus control, which restructures the environment to reduce the probability of a particular conditional stimulus; contingency management; dramatic relief, as through catharsis; and support relationships (Prochaska and DiClemente, 1983). An alternative to stage models is Diffusion Theory (Rogers, 1983) which describes the process by which an innovation is communicated through certain channels over time among members of a social system. Diffusion Theory informs interventions that involve entire communities rather than individuals. As such, it takes into account sociocultural influences that might inhibit or encourage particular behaviors, and it has been applied successfully in community-level interventions that will be described later (e.g., Kelly, Winett, Roffman, et al., 1993). One of the key channels for communicating new ideas is through opinion leaders. In any system, there may be innovative opinion leaders whose influence can accelerate the rate at which innovations are adopted through the social system. The interpersonal networks of opinion leaders allow them to disseminate information and to serve as social models whose behavior may be imitated by other members of the system. Interventions based on Diffusion Theory have focused on the training or persuasion of peer opinion leaders who may or may not be the same as community leaders. Diffusion Theory indirectly addresses sustainability of the intervention; a successful diffusion intervention changes the community such that the new (safer) behavior becomes normative. Additional intervention is

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Aids and Behavior: An Integrated Approach not needed once a critical portion of the targeted community has adopted the new behavior. Stage models of behavior change are helpful in that they provide diagnostic tools for determining where in the behavior change process a given group or community finds itself. For example, given the history of the AIDS epidemic in the United States, gay men as a group may recognize that unprotected sexual intercourse is a behavior that places them or their partners at risk of HIV infection. In contrast, Hispanic/Latina women as a group may not yet recognize this behavior as potentially harmful (Gomez and Marin, 1993). These two groups being at different stages of behavior change would thus require different kinds of interventions. Despite their conceptual contributions, current theoretical models are limited in their ability to predict risk behavior for two main reasons. First, with respect to sexual behavior, the models are based on the assumption that sexual encounters are regulated by self-formulated plans of action, and that individuals are acting in an intentional and volitional manner when engaging in sexual activity. However, sexual behavior is often impulsive and, at least in part, physiologically motivated. A well-formulated plan of action that is the product of a careful weighing of potential harms and benefits can be dismissed in the context of a passionate sexual encounter when competing proximal goals (i.e., sexual gratification) offset well-informed intentions (i.e., to use a condom). Second, the dominant theoretical models of behavior do not easily accommodate contextual personal and sociocultural variables such as gender and racial/ethnic culture. Gender roles and cultural values and norms influence the behavior of women and men and the nature of the relationships in which sexual activity occurs. Unsafe sexual practices often are not the result of a deficit of knowledge, motivation, or skill, but instead have meaning within a given personal and sociocultural context. With the exception of Diffusion Theory, which takes gender and culture into account, current theoretical models of HIV risk behavior do not easily accommodate contextual personal and sociocultural variables. A great deal of work remains to be done in this area. One theory that some think has potential application to understanding the context of HIV risk for women is the Self in Relation Theory of women's development. This theory suggests that the "relational self" is the core of self-structure in women and the basis for growth and development (Miller, 1986). Furthermore, this theory argues, women are basically oriented to others, and as

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Aids and Behavior: An Integrated Approach a consequence their relationships and the maintenance of these relationships are highly charged with meaning. When applied to HIV, the Self in Relation Theory would suggest that the risk involved in initiating changes in intimate relationships (i.e., changes related to risk reduction) is greater for women than for men and may undermine women's intentions and their attempts to adopt safer sex behaviors. According to this theory, within women's ascribed roles as unequals, giving to others is a central aspect of women's identity, and sex becomes something that women "give" to men. There is little room for women's realization of their own sexuality (Miller, 1986). Stepping out of the traditional role, as required by safer sex negotiation, therefore potentially places women in direct conflict with men (Miller, 1986). To date, models designed to explain or predict risk behavior tend to treat the social and environmental variables as independent variables, without considering that they may be interactive or mutually reciprocal. The models also tend to focus only on one level of analysis—the individual—without regard for other levels, such as the culture and community to which an individual belongs. SOCIAL SCIENCE PERSPECTIVES ON BEHAVIOR AND BEHAVIOR CHANGE Social science perspectives have only recently been applied broadly to AIDS research (Adam, 1992), but their potential for productively refocusing the investigation of AIDS is evidenced in some of the more recently completed ethnographies, social network analyses, and community outreach interventions and evaluations. Social science research has the capability to reveal the complex and important linkages between social structure and individual behavior and to suggest how specific social changes can inspire individual changes (Friedman, Des Jarlais, and Ward, 1994). Several social science researchers contend that an overemphasis on behavioral change at the individual level has weakened attempts to reduce the spread of HIV and is in part to blame for the limited success of behavioral interventions to date (Friedman, 1993; Kayal, 1993). Individual behavior occurs in a complex social and cultural context, and analysis that removes that behavior from its broader setting ignores essential determinants. Current theory and research, dominated by psychological models that examine rational factors and cognitive processes that shape the isolated individual's decision-making patterns, have obscured the social and relational factors involved in behavior, such as the role of

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Aids and Behavior: An Integrated Approach have shown that there is no viral leakage from the female condom (Leeper, 1990; Voeller, 1991). The female condom has several advantages over the male condom, both as a contraceptive and as an STD prevention method. First, since it is woman-controlled, women are not as dependent on the cooperation of sex partners to protect themselves from HIV and other sexually transmitted diseases. Second, the female condom is inserted before intercourse, providing additional protection against infections from pre-ejaculated fluids. Third, the female condom protects a greater proportion of the vagina, providing additional protection against STDs. Fourth, the Reality™ condom is less likely to rupture than the male condom (Bounds et al., 1988; Gollub and Stein, 1993; Leeper and Conrardy, 1989). Also, because of its loose fit, it causes less loss of sensitivity, permits penetration before complete erection of the penis, and permits continued intimacy in the resolution phase of intercourse, since it need not be removed immediately. Several small-scale studies have tested the acceptability of Reality™ among both women and men, but only two studies to date have been conducted among women at highrisk of HIV infection—commercial sex workers. In one such study, participants claimed that female condoms were more protective against HIV and STD infection and were more feasible to use than male condoms. Many used them with their regular sex partners, who also found them acceptable (Hernandez-Avila, 1992). In the other study, 90 percent of the women said they would recommend the female condom to friends (Sakondhavat, 1990). In all acceptability studies, although the samples have been small, a majority of women and men have felt that the female condom was easy to use and was an acceptable method of both contraception and HIV/STD prevention (Schilling, El-Bassel, Leeper, et al., 1991). This preliminary research suggests promising results for the female condom, including acceptability among female populations with varying sexual histories and practices. However, studies so far have been based on very small samples, and additional data are needed to further test the acceptability and efficacy of female condom use. Moreover, no studies have been conducted in the United States among women at highrisk for HIV infection, such as commercial sex workers, injection drug users, or those who exchange sex for drugs. In addition, the female condom is not readily accessible in the United States. How the new female condom will fare among highrisk populations, and in the general population, remains to be seen.

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Aids and Behavior: An Integrated Approach to the same extent as did subjects participating in interventions, it is impossible to tell whether behavior actually changed in both groups or if other factors influenced reports of behavior. Such factors might include informal communication between subjects, intensive and repeated interviews, and general societal trends (Calsyn, Saxon, Freeman, et al., 1992; Gibson, Young, and Lovelle-Drache, 1993; McCusker et al., 1992). Even though many of these individual-focused intervention studies have demonstrated sexual and drug-use behavior change, they may be limited in a few ways: (1) most rely solely on self-reported data; (2) for the most part they have not yet demonstrated long-term behavior change (beyond 6 months); (3) it is not yet known whether they work with populations outside of their target groups; (4) many interventions may not be cost-effective to implement on a larger scale, and (5) with few exceptions, they do not measure HIV transmission and do not necessarily indicate that HIV infection has been averted. COMMUNITY-FOCUSED INTERVENTIONS Sexual Behavior Intervention research at the community level has employed peerled AIDS education to reach people at highrisk for HIV infection who may not be willing to participate in small-group/programs (Kegeles et al., 1993) and to change norms in the community as a whole (Kelly, St. Lawrence, Stevenson, et al., 1992; Kelly, Winett, Roffman, et al., 1993). In one intervention study mentioned previously, gay men who served as popular opinion leaders were trained to deliver AIDS risk reduction messages to other gay men who frequented gay bars. The result of this intervention was that after three months, the number of gay men in the study who practiced unprotected sex was reduced in the range of 15 to 24 percent from baseline levels (Kelly, St. Lawrence, Stevenson, et al., 1992). When this community-based intervention was replicated in other small cities in Wisconsin, Washington, West Virginia, and New York, similar results were found at 9-month follow-up (Kelly, Winett, Roffman, et al., 1993). The goal of attracting socially isolated men into participating in safer sex educational activities was accomplished by an intervention designed by and for young gay men aged 18 to 29. This intervention reduced unprotected anal intercourse among its subjects, from 33 percent at baseline to 25 percent at 9-month follow-up in one experimental city, however, little change was observed at follow-up in control cities (Kegeles

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Aids and Behavior: An Integrated Approach et al., 1993). Although these experiments effected short-term behavioral change among gay men as a result of community-level peer education, both long-term impact and generalizability to other risk groups remain to be demonstrated. In a number of African countries, a combination of peer-led education with free condom distribution has been used to attempt to change behaviors among commercial sex workers and their clients (Lamptey, 1991; Welsh et al., 1992); however, so far, only a few programs have been evaluated for their effectiveness (Asamoah-Adu et al., 1994; Williams et al., 1992; Wilson et al., 1993). In the Nigerian state of Cross River, community-based interventions trained commercial sex workers, clients, and brothel owners and managers as peer educators, initiated community outreach by peer educators, and distributed condoms at brothels (Williams et al., 1992). A follow-up evaluation one year later found that consistent condom use had increased from 12 percent to 24 percent and, among clients, AIDS knowledge had improved and attitudes toward condom efficacy were more favorable. In Zimbabwe a similar community-level peer education and condom distribution program resulted in increased consistent condom use among sex workers (8.6 percent at baseline to 58.3 percent at 1-year follow-up) and clients (25.4 percent at baseline to 44.7 percent at follow-up) (Wilson et al., 1993). Consistent condom use by sex workers and their clients in Ghana rose from 6 percent in 1987 to 71 percent in 1988 and then fell back to 64 percent in 1991 (Asamoah-Adu et al., 1994). Condom distribution strategies have been widely used, but more careful study should be initiated to determine their efficacy in reducing HIV infections. Also, interventions should target steady partners of sex workers, since it appears that sex workers use condoms less frequently in their personal relationships than in their interactions with clients (Dorfman, Derish, and Cohen, 1992; NRC, 1990b). The impact of AIDS education on other adult heterosexual has mostly come from mass media campaigns directed at the general public. Several studies have found evidence that these campaigns have had an impact on AIDS knowledge, attitudes, and behavior (Hausser et al., 1988; Izazola, Valdespino, and Sepulveda, 1988; Lehmann et al., 1987; Mills, Campbell, and Waters, 1986; Moatti et al., 1992; Wober, 1988). For example, media campaigns in Switzerland that included mail distribution of an AIDS informational booklet and multimedia advertisements promoting condom use, nonsharing of syringes, and monogamy resulted in a demonstrated increase in AIDS knowledge, condom sales, and condom use (Hausser et al., 1988; Lehmann et al., 1987).

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Aids and Behavior: An Integrated Approach Injection Drug Use Research results from evaluations of needle exchange programs have been highly promising in showing reductions in risky drug using behavior, despite the fact that none of the evaluation studies was a randomized, controlled trial (due to the extreme difficulty of conducting such a trial in this context). In a 1993 report prepared for CDC, Lurie and Reingold (1993) reviewed sixteen such studies and found that among the 14 that evaluated the impact of needle exchange programs on the sharing of syringes, 10 demonstrated decreases in sharing and 4 showed no change. Of the 8 studies that evaluated the impact of needle exchange programs on frequency of drug injection, 3 showed a decrease, 4 showed no change, and one found that needle exchange clients were less likely to stop using drugs than a comparison group. Because these studies did not specifically address the interaction of needle exchange programs and risky sexual behavior, no firm conclusions were made in this regard (see Lurie and Reingold, 1993, for details). In the NIDA-sponsored National AIDS Demonstration Research Program (NADR), (see Box 6.1 in Chapter 6), street outreach projects that recruited out-of-treatment injection drug users into HIV prevention services contributed to a substantial reduction in the percentage of injection drug users who shared needles—from 48 percent at baseline to 24 percent at follow-up 6 months later (Stephens et al., 1993). Drug users and their sex partners also increased their consistent use of condoms by 9 percent as a result of this program (see Stephens et al., 1993, for details). Social networks of injection drug users were also targeted for peer-led street outreach in the NADR program. In one study in Chicago, 86 percent of subjects stopped sharing injection equipment and HIV seroconversion rates dropped substantially as a result of the network-approach intervention, from 5 percent at baseline to less than 1 percent at the follow-up four years later (Wicbel et al., 1993). MAINTAINING BEHAVIOR CHANGE AND PREVENTING RELAPSE Initiating change in risky behavior is only the first step in controlling the spread of HIV/AIDS. Maintaining behavior change over time is a much more significant challenge. Because many years may elapse between a person's initial infection with HIV and the onset of serious AIDS symptoms, people infected with

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Aids and Behavior: An Integrated Approach HIV must consistently restrict their sexual expression and drug use to only those acts that are safe if they are to avoid transmission of HIV to their sex and drug-using partners. Also, because HIV infection is highly concentrated within some well-defined subpopulations, each unsafe act within those groups conveys far greater risk for HIV transmission. Broad, if not universal, efforts to initiate and maintain risk reduction are necessary for avoiding continued high HIV seroconversion levels, especially among communities at higher risk. Research on sustained behavioral risk reductions has primarily focused on gay men. Although it should broaden to other groups, findings from this research may significantly contribute to all HIV prevention efforts. Using longitudinal data from the San Francisco Men's Health Study, Ekstrand and Coates (1990) discovered that after a period of engaging only in safer sex, 16 percent of participants reinitiated unprotected insertive anal intercourse and 12 percent reinitiated unprotected receptive anal intercourse. A replication study—also among gay men in San Francisco—similarly found that it was more common for men to return to unsafe sexual practices after a period of exclusively safer sex than to engage consistently in highrisk sex (Stall et al., 1990). Given the fact that HIV prevention efforts for gay men have traditionally focused almost exclusively on initiation of safer sex techniques, these findings as well as those of other longitudinal studies (Hart et al., in press; Kippax et al., 1991; O'Reilly et al., 1990) clearly indicate that ensuring consistent maintenance of safer sex over long periods of time is a challenge. The variability in rates of maintenance of safer sexual practices reported in such studies might reflect differences in sampling methods, measurement of sexual risk, observation, time periods, number of observations, the effect of loss due to follow-up bias, and prevalence of risk-taking behaviors across different populations of gay men. However, one finding that is clear from all the studies, despite these important methodological differences is that some portion of gay men reinitiate riskier sexual behaviors after a period of safer sexual behaviors, and that this behavioral pattern could be the source of continuing HIV seroconversions. The research described above relies exclusively on self-reported data, the validity of which have been discussed at length elsewhere (NRC, 1991). While self-reporting remains the best available methodology for obtaining information about AIDS risk behaviors in diverse populations, it is useful to supplement and

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Aids and Behavior: An Integrated Approach validate these data with a reliable biological outcome measure of seroconversion where possible. One study that did so (Kingsley et al., 1991) used data from the Multicenter AIDS Cohort Study (MACS), a four-city study of gay-identified men, and found that declines in HIV seroconversion observed during the first three years of the study were reversed by the fifth year, by which time 11.3 percent of the men who were initially HIV negative were estimated to have seroconverted. Based on the health education offered to study participants (including HIV testing) and based on the fact that the cohort defined by the study is aging, the researchers believed that this estimate of new seroconversions was conservative when applied to the community at large. Correlates of nonmaintenance of safer sex techniques have been empirically detected from several longitudinal research projects. These correlates include low self-efficacy, heavy drug or alcohol use, having sex under the influence of drugs or alcohol, having larger numbers of sex partners, having had sex before 1984 with someone diagnosed with AIDS, relative youth, and depression (Kelly, St. Lawrence, and Brasfield, 1991; O'Reilly et al., 1990; Stall et al., 1990). In addition to individual behavioral factors, certain social factors may influence nonmaintenance of safer sex behaviors, such as lack of community support for risk reduction, social support or pressure to take health risks, high reinforcement value for unprotected sex, and identification of unprotected anal intercourse as a favorite sexual act (Kelly, St. Lawrence, and Brasfield, 1991; O'Reilly et al., 1990; Stall et al., 1990). Identifying and understanding these correlates may have more significant impact on HIV prevention than does measuring the rates of long-term behavior maintenance. Identifying the characteristics of gay men who have seroconverted may also provide useful information about nonmaintenance of behavioral risk reduction over time. Racial/ethnic minority status, youth, lower education levels, lower socioeconomic status, and higher likelihood of cocaine or amphetamine use have been identified as correlates of HIV seroconversion in several independent studies (Kingsley et al., 1991; Waight and Miller, 1991; Willoughby et al., 1990). However, because these analyses were conducted using data sets that were not specifically designed to study nonmaintenance of safer sex techniques over time, and because many of the earlier study cohorts are aging, new cohorts of men who have sex with men should be formed in order to specifically study safer sex behavioral maintenance issues. Also, most of the

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Aids and Behavior: An Integrated Approach analyses conducted so far have not had the benefit of a theoretical model of HIV risk behavior lapse. In order to develop both basic and applied research in this area, exploratory, inductive, retrospective research designs should be employed to identify conditions under which maintenance of safer sex techniques is attenuated. That reductions in risk behavior among men who have sex with men have been maintained at all is a tribute to the successful interventions employed within these communities. However, successful HIV prevention requires long-term, community-wide maintenance of risk reduction which in turn calls for the development of new intervention models, especially those that target multiple risk behaviors. EVALUATING THE EFFECTS OF AIDS INTERVENTIONS Although identifying behavioral changes is an important outcome measure for AIDS preventive interventions, these changes do not automatically translate into reductions in HIV transmission in ways that are immediately obvious. Moreover, although modifying risky behavior is key to reducing HIV transmission, behavior change alone may not be sufficient for evaluating prevention efforts. However, with few exceptions, an attempt to estimate the number of infections averted has not been included in the design or evaluation of behavior change interventions. While it would not be possible to employ such an analysis to every prevention project, its utility as an approach should be further assessed. An ideal experimental design would be to compare direct measurement of seroconversions in populations targeted by intervention programs to those of similar populations not receiving the intervention (preferably with random assignment to treatment and control groups). There are difficulties in mounting such large-scale social experiments. For example, interventions targeting entire communities (such as needle exchange programs or making condoms available in schools) do not allow for the easy formation of treatment and control groups, while randomization is virtually impossible in such environments. Even if one could achieve such experimental setups, the incidence rate of new infections is low even in many populations at relatively highrisk for HIV. This means that unless the number of persons involved in an intervention study is extremely large, it would take many years before conventional statistical methods

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Aids and Behavior: An Integrated Approach could prove that a highly successful program is in fact highly successful. For example, consider an intervention (with 100 in the control group and 100 in the intervention group) that cuts the infection rate in half for a population of injection drug users experiencing an incidence rate of 4 infections per 100 per year. After two years the study would detect on average 7.7 new infections in the control group (incidence of .04) and 3.9 new infections in the intervention group (reduced incidence of .02). Although reducing an infection rate in half is effective, conventional statistical methods would fail to find this difference statistically significant. (Precisely this same issue currently plagues the planning and design of HIV preventive vaccine trials.) This very issue led a previous National Research Council panel to recommend using behavior change as the primary approach to evaluating AIDS preventive intervention research (NRC, 1991). However, focusing solely on behavior change outcome measures leaves unanswered the fundamental question of how many infections are really averted as a result of prevention programs. An intermediate course between solely measuring changes in behavior on the one hand, and insisting on lengthy field studies with enormous numbers of subjects on the other is the use of mathematical modeling to provide evidence for how a given prevention activity may reduce infection. The mathematical theory of epidemics is well established, and numerous researchers have applied modeling techniques to gain insights into various aspects of the AIDS epidemic (Anderson and May, 1991; Brookmeyer and Gail, 1993; Castillo-Chavez, 1989; Jager and Ruitenberg, 1992; Kaplan and Brandeau, 1994). These models mathematically integrate the key features of risky behavior (i.e., numbers of unprotected sex partners per person per unit time, number of needle-sharing occasions per person per unit time), epidemiology (i.e., the probability of HIV transmission per potentially infectious exposure, progression of HIV infection through AIDS, AIDS-induced mortality), and demography (i.e., population immigration, birth, and non-AIDS mortality rates). In addition to incorporating behavioral variables, the models allow for incorporation of prevention program operations as demonstrated by studies of needle exchange (Kaplan and O'Keefe, 1993), bleach distribution to injection drug users (Siegel, Weinstein, and Fineberg, 1991), HIV counseling and testing (Brandeau et al., 1993; Gail, Preston, and Piantadosi, 1989), and self-deferral from blood donation (Kaplan and Novick, 1990). Thus, modeling provides an attractive approach to thinking about how prevention

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Aids and Behavior: An Integrated Approach programs effect change in HIV transmission, assuming the models are structured to include all relevant parameters. For example, the evaluation of a needle exchange program in New Haven, Connecticut employs a mathematical model to estimate the impact of the program on HIV transmission among the participants of the needle exchange. The evaluation uses a syringe tracking and testing (STT) system to collect data on needles distributed and returned to the program by using anonymous code names for participants, tracking numbers for needles, and a technique that is capable of detecting HIV in the traces of blood remaining in the syringes. The data derived from the STT have revealed a significant drop in the portion of needles testing positive for HIV, and it is estimated that HIV incidence among needle exchange participants has fallen by 33 percent (Kaplan, 1994; Kaplan and O'Keefe, 1993). The ability to estimate the impact of an intervention on HIV transmission also contributes to the possibility of conducting a cost-effectiveness assessment of that intervention. In a time of shrinking federal budgets and increasing research costs, the scientific community faces greater pressure to demonstrate the social value of taxpayer-supported research. One measure of value is the cost-to-benefit ratio. In the context of HIV intervention research, dollar costs are both the costs of conducting the intervention itself and the costs of medical care for a person with AIDS. Assuming one could use the methods described above for estimating the number of HIV infections averted by the implementation of an intervention, one could then compare dollars saved in medical costs affiliated with those infections with dollars spent on conducting the intervention. One could then make an assessment about the value of investing in that particular intervention. CONCLUSION AND RECOMMENDATIONS CONCLUSION Basic science research in the neurobiological, psychological, and social sciences has uncovered a great deal of information about the range of factors underlying the behavior of individuals and groups, information that has been influential in the design of HIV preventive interventions. Theoretical models from psychology have played a particularly significant role. Yet, the mixed results of interventions informed by this basic research suggest that much remains to be learned—in particular, how the biological, psychological,

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Aids and Behavior: An Integrated Approach and social dimensions of behavior interact to encourage or prevent risky behavior and to initiate and maintain positive behavior change. Cross-disciplinary research in this regard will play an important role in improving the design and application of HIV preventive interventions. The efficacy and value of such interventions may be measured by demonstrated, sustained, positive behavior change; but with respect to AIDS prevention, it also is important to show that new infections have been averted by such change. Epidemiological and mathematical methods now exist to assess the efficacy of interventions in this regard—and their cost-to-benefit ratio—and their employment should be considered wherever appropriate. RECOMMENDATIONS FOR UNDERSTANDING THE DETERMINANTS OF HIV RISK BEHAVIOR 3.1 The committee recommends that NIAAA, NIDA, and NIMH expand basic research on the biology of sexuality as it potentially relates to highrisk sexual behaviors. This might include research on the central nervous system (CNS) sexual systems that mediate sexual behaviors, the CNS neural systems underlying sexual behavior, and the molecular genetics of sexual behaviors. 3.2 The committee recommends that NIAAA, NIDA, and NIMH expand research on the biology of substance abuse to provide additional knowledge for approaching highrisk behaviors. This might include research to define structure-activity relationships in the function of dopamine systems; the role of noradrenergic systems and molecular mechanisms in the components of addiction (including euphoria, tolerance, sensitization, and withdrawal); the role of opiate peptide receptor subtypes in components of the addiction-abuse syndrome; as well as research to identify mechanisms of cocaine addiction. 3.3 The committee recommends that, where appropriate, NIAAA, NIDA, and NIMH coordinate their efforts with other relevant federal agencies (e.g., other NIH institutes, the National Science Foundation) that are also attempting to integrate biological, behavioral, and social research to define highrisk behaviors. 3.4 The committee recommends that NIAAA, NIDA, and NIMH support AIDS research that integrates theories of gender

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Aids and Behavior: An Integrated Approach (identity, development, and dynamics) and behavior change models. 3.5 The committee recommends that NIAAA, NIDA, and NIMH expand the research effort examining social and structural factors (such as class, race/ethnicity, gender relations, and community) that increase risk for AIDS, affect progression of disease, and provide points of intervention. This might require research that takes as the unit of analysis the social context and relationship (e.g., dyads, families, communities) in which HIV occurs—as opposed to the individual at risk of or who has HIV. 3.6 The committee recommends that NIAAA, NIDA, and NIMH, in conjunction with other NIH institutes, develop new and existing woman-controlled HIV/STD prevention methods (e.g., female condoms and microbicides) and examine the social and behavioral issues related to their use. 3.7 The committee recommends that NIAAA, NIDA, and NIMH support basic and applied research on the maintenance of behavior change, for example, risky sexual behavior and alcohol and other drug-using behavior, including the prevention of relapse. (The committee notes that this has been recommended in previous NRC reports—AIDS: The Second Decade, 1990; AIDS, Sexual Behavior, and Intravenous Drug Use, 1989—but has not been attended to adequately.) 3.8 The committee recommends that NIAAA, NIDA, and NIMH expand funding for HIV intervention research initiatives, particularly those that: (1) have rigorous evaluation components; (2) investigate motivations, intentions, and barriers in addition to behavior change; (3) include outcome measures in addition to behavior change, such as HIV seroprevalence, STD rates, and pregnancy rates; and (4) target a full range of racial/ethnic, gender, and cultural groups for the purpose of assessing between-group differences. 3.9 The committee recommends that NIAAA, NIDA, and NIMH support research that estimates the number of HIV infections averted by current prevention efforts and that includes cost estimates for these efforts.