Using Gay Men s Sexual Networks to Reduce Sexually Transmitted Disease (STD)/Human Immunodeficiency Virus (HIV) Transmission
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1 Sexually Transmitted Diseases, October supplement 2005, Vol. 32, No. 10, p.s48 S52 DOI: /01.olq Copyright 2005, American Sexually Transmitted Diseases Association All rights reserved. Using Gay Men s Sexual Networks to Reduce Sexually Transmitted Disease (STD)/Human Immunodeficiency Virus (HIV) Transmission DAN WOHLFEILER, MPH,* AND JOHN J. POTTERAT, BA Abstract: An individual s risk of acquiring or transmitting a sexually transmitted disease or HIV is affected both by individual risk factors and by one s location within a sexual network. Therefore, prevention efforts must consider intervening with both individuals and with network conformations. Helping gay and bisexual men make more informed choices about their partners and fragmenting networks to reduce the likelihood of risky encounters between high-risk core group members and those at lower risk are two strategies for reducing transmission in this population. Network-level interventions are particularly well suited for places such as commercial sex venues and Internet sites where gay and bisexual men meet new sexual partners. FOR MORE THAN 2 decades, public health and community workers have struggled to find ways to reduce the human immunodeficiency virus (HIV) and sexually transmitted disease (STD) burden among gay and bisexual men (men who have sex with men (MSM)). Their script has been risk-behavior modification, and their audience has been individual gay men. Although risk-behavior modifications have effected reductions in HIV transmission among MSM, they are difficult to maintain. 1 Might there be other ways to help reduce STD/HIV transmission? Theoretical and empirical evidence suggests that a network intervention approach aimed at altering the architecture of networks in ways that fragment transmission pathways may be effective. 2 4 Although contact-tracing efforts can also serve to fragment networks, success may depend on locating a large proportion of exposed partners. However, as articles in this issue attest, in populations of MSM, many partners are anonymous or not locatable. Other network interventions have used social networks, many of which overlap with sexual networks, to diffuse risk-reduction messages, syringes, and condoms and to support norms favoring risk reduction. 5 7 Many have also identified key social venues as places to conduct these activities and to promote testing Fewer have attempted to intervene in the networks themselves or in the social venues in such a way as to help fragment the networks and The authors thank the participants in the California Department of Health Services meeting regarding the implications of sexual networks, as well as Houston Gilbert, Holly Howard, and Mary McFarlane for helpful suggestions. Correspondence: Dan Wohlfeiler, MPH, STD Control Branch, California Dept. of Health Services, 300 Frank H. Ogawa Plaza, Suite 520, Oakland, CA dwohlfei@dhs.ca.gov. Received for publication October 26, 2004, and accepted March 3, From the *California Department of Health Services, Sexually Transmitted Diseases (STD) Control Branch, Oakland, California; and Independent Consultant, Colorado Springs, Colorado reduce the odds of mixing occurring between high- and low-risk individuals. In this paper, we first provide an overview of sexual networks and their importance in STD/HIV transmission dynamics. Next, we explore the potential implications of MSM commercial sex venues and the Internet for sexual transmission and suggest approaches for interventions and research. Many of the particulars we present emerged from a discussion, sponsored by the California Department of Health Services in September 2003, of the implications of the network perspective for STD/HIV interventions. Our focus is on bathhouses, sex clubs, and the Internet. Although we do not discuss other venues (e.g., bars, circuit, or private sex parties), many of these ideas are applicable to them. Overview of Sexual Networks Networks matter because of structure. The 2 networks shown in Fig. 1 demonstrate that what matters is not simply risk behavior but the architecture of networks and how such conformation can modulate risk of STD acquisition and transmission. Each network below consists of 8 persons (circles) connected by 9 relationships (lines). Two persons each have 3 partners, and the other 6 each have 2 partners. Yet, transmission will be less efficient in network A, and prevention will be more difficult in network B. In A, in just 2 steps from the index person, half the network can be infected and half spared; in B, 2 steps can result in everyone being infected except for the person on the extreme right. In A, sparing half the population from exposure requires cutting 1 bridge, while in B, it requires cutting 3 bridges. In a word, for epidemics, network structure may be destiny. 2 Sexual networks consist of persons who are sexually connected directly or indirectly to one another. Networks that are important for sustaining STD/HIV transmission in communities share several key features: a sufficient number of persons, moderate to high density of connections, centrality of infected persons, and patterns of partner selection (e.g., mixing between high- and low-risk persons). For example, men of different ethnicities 11,12 or ages may report similar levels of risk at the individual level yet will experience widely differing infection rates. Young men s greatest risk of infection has been associated with having unprotected anal sex with older men, 13 who are more likely to be infected. Blacks S48
2 Vol. 32 No. 10 supplement USING SEXUAL NETWORKS TO REDUCE STD/HIV TRANSMISSION S49 Fig. 1. The architecture of sexual networks as epidemiologic destiny. (From: Klovdahl AS, Potterat J, Woodhouse D, et al. HIV infection in a social network: a progress report. Bull Méthodol Sociol 1992; 36:24 33.) experience higher rates of STD/HIV than do whites, a fact that has been linked to sexual mixing (network) patterns. High-risk blacks are more likely to choose partners from high-, moderate-, and low-risk profiles, while whites are more likely to be concordant (high-risk with high-risk, low-risk with low-risk). 11 Sexual mixing patterns are also important on the partner mixing continuum, for such configuration will affect how quickly STD can propagate. Persons may be mutually monogamous or may accumulate partners one at a time (serial monogamy) or move back and forth among different partners (concurrency). Exclusively monogamous persons are not, by definition, part of a sexual network. Persons who practice concurrency are at much higher risk of disease acquisition and transmission than are those who practice serial monogamy, even if overall they have the same number of partners during the same time period. 14,15 Figure 2 illuminates this point. If individual A has 5 partners (B, C, D, E, and F) in sequence and is exposed to STDs or HIV by his third partner (D), he is in a position to infect his subsequent 2 partners (E and F) only (Fig. Fig. 2. a, Serial monogamy. After A is exposed to infected partner D, 3 are potentially infected. (Figure prepared by Department of Health Services.) b, Concurrency. After A is exposed to infected partner D, 5 are potentially infected. Concurrency facilitates more transmission than serial monogamy. (Figure prepared by Department of Health Services.) 2a). Because concurrency implies having multiple sexual partners and going back and forth among them, this pattern considerably increases the probability for transmission to all partners in the network. Figure 2b indicates that if A gets infected by D, and A continues to have unprotected sex with all partners, going back and forth among them, all 5 partners are poised for infection, including partners B and C, with whom A first had sex before he met the third partner. Of particular relevance to gay men s sexual networks is the importance of numbers, not simply patterns of connectivity. While many men report relatively few partners, an appreciable minority of MSM report high numbers of partners (STOP AIDS Project, San Francisco). These numbers are reportedly increasing in cities such as Seattle 16 and San Francisco. 17 Of concern are data from Great Britain indicating that gay men who report the highest number of partners are also those most likely to engage in unprotected sex. 18 Researchers often refer to such high-risk persons as members of core groups. 19 They are reported to contribute a disproportionate share of HIV/STDs and can fuel sustained transmission even when they make up only a minority of the population. 19 Rather than being a part of a static entity, men may enter and exit the core group at different times in their lives. In addition, high-risk behavior appears to be correlated with synchronous epidemics ( syndemics 20 ) of substance use (particularly methamphetamines), histories of childhood sexual abuse, clinical depression, and reports of partner violence. The more complex the syndemic mix, the higher the level of sexual risk. 20 Current Interventions in Gay Male Sexual Venues STD/HIV interventions in the commercial sex venues of MSM have been erratic and essentially passive. These venues, including bathhouses and sex clubs, as well as the Internet, are important precisely because they facilitate sexual mixing between high-risk and low-risk individuals. Therefore, they should be accorded greater disease intervention attention. Venues such as bars have been shown to tie together networks that might otherwise appear to be geographically isolated from one another. 8,21 Public health workers have permitted these venues to operate on their own terms and have only episodically used them as places to educate and test at-risk persons. 9,22 Of note, also in this issue, is Cieselski s report that the number of blood tests obtained from patrons of commercial sex venues was remarkably low, as was their yield of infectious syphilis cases. 9a This datum stands in marked contrast to the high proportion of MSM patients with infectious syphilis who report meeting partners in such commercial venues. The low percentage of positive results suggests that persons likeliest to harbor the infection may be the least likely to seek testing. Such observations make it improbable that offering testing within these establishments will have sufficient impact on the STD and HIV burdens in MSM. The Internet and the Potential for Fragmenting Transmission Networks Fragmentation of transmission networks may succeed where passive testing and other individual interventions have had less than the intended impact. Two fragmentation strategies have been suggested. The first would be to help men make informed choices about their partners and thus become better shoppers. 23 In brief, the more information men have about their partners sexual history, risk-taking preferences, and HIV/STD status, presumably the better equipped they will be to make informed choices regarding partners, sexual practices, and use of personal protection. 23 Second, fragmentation of high-risk networks may consist of discour-
3 S50 WOHLFEILER AND POTTERAT Sexually Transmitted Diseases October supplement 2005 aging contact between core-group, high-risk members both infected and uninfected and low-risk men. This may not require finding a specific bridge but rather aiming at reducing the overall number of bridges. Thus, for example, even if low-risk men have unprotected sex with other low-risk men, they probably face a much-diminished risk of STD/HIV acquisition and transmission. The Internet and Network-Informed Interventions Men who seek partners on the Internet have been found to report having more partners than do men who do not seek partners on the Internet. 24 The Internet makes it easier for men to find new partners, even in urban areas where diverse and multiple venues already exist. Moreover, in cities where few businesses or other venues exist for men to meet each other, the Internet provides a new set of opportunities. The Internet also has the potential to alter the patterns of how high-risk and low-risk men meet. Particularly important is the advent of numerous Internet sites specifically promoting barebacking (unprotected anal sex). Such sites may not attract lowrisk men and therefore can serve to fragment high-risk networks by separating core MSM from lower-risk MSM. In addition, other Internet venues (e.g., chat rooms and websites) attract specific types of MSM, based on age or ethnic preferences, HIV status, outness, or marital status. To the extent that such websites and chat rooms attract men with low STD/HIV prevalence and with discriminating norms favoring sexual risk reduction, they may afford protection from infection through isolation from men experiencing high prevalence rates. On the other hand, to the extent that these men have high prevalence rates and weak norms for protection, recruitment of partners through such sites may increase the core s influence. As McFarlane et al. 9 report in this issue, public health workers throughout the United States are exploring interventions that target men who seek sex via the Internet. Such interventions include online advertising; outreach; partner notification; and interactive, targeted interventions. As outlined below, the Internet has the potential to provide the information needed to become better shoppers, to fragment sexual networks by pulling low-risk men away from high-risk men, and to facilitate partner notification and services. Using Member Profiles and Computerized Algorithms to Help Men Become Better Shoppers Many Internet venues ask users to describe themselves and their preferences in partners. For example, one popular site asks men to state their risk-taking preferences, providing the option of selecting either looking for safe sex only or needs further discussion ( Profile completion permits persons to state these preferences once, reducing the awkwardness of having to repeat them with each prospective partner, a process that many men find difficult. 25 Large Internet venues that are not specifically designed for meeting sexual partners, such as America Online, should be encouraged to follow Yahoo s example, and provide Adult Profiles, which can then ask explicit questions regarding risk-taking preferences and other information. Although Internet providers have expressed concerns about liability for asking patrons to reveal their illicit drug use behavior, asking patrons to disclose that they do not use drugs may help lower-risk men find a low-risk partner efficiently while not necessarily implying that those who have not explicitly denied drug use are indeed using. Manhunt.net, an internet site used by gay men around the US, added no pnp ( no party and play ) to its profile screen at the end of 2004 for this purpose. A Dutch site, created a computerized algorithm that allowed patrons to enter information describing themselves and their preferences and provided them with tailored feedback. (This tailored algorithm was temporarily removed in January 2005.) Thus, for example, the site s algorithm offered advice to an out gay man seeking sex with a new partner, regarding how long he and his primary partner should continue to use condoms. It also offered, by comparison, a closeted young man advice about how to use the Internet safely in his search for partners. One of the algorithm s important characteristics was that it was placed at the site s entrance, requiring participants to complete its queries before navigating to areas of the site where they could seek partners. This helped assure that all participants received a minimum of information while also helping to establish a norm of making informed choices in contrast to many efforts that, unless assertive, reach only those who specifically request information. Future algorithms could provide local STD/HIV incidence data, as well as referrals to clinical and psychosocial interventions. Fragmenting Sexual Networks Online A San Francisco, CA, AIDS educator recently created a website designed to attract men who only seek safe sex: org. This venue specifically forbids the promotion of unprotected sex. Between its creation in October 2003 and the end of June 2005, more than 2500 men have signed up for membership (Frank Strona, personal communication, Sept. 7, 2005). Another new website, also serves to promote seroconcordant relationships. Both of these websites are examples of fragmenting sexual networks: the first website by separating low-risk from high-risk MSM, regardless of HIV status, the second by separating infected from uninfected persons. Facilitating Partner Notification Online In this issue, Klausner and colleagues 26 describe multiple online interventions that can exploit the Internet s characteristics for public health advantage. In addition, gay men should be encouraged to continue attempts to locate information about their sexual partners. The Internet, in particular, usually requires that a minimum of identifying information (e.g., a username) be exchanged between partners. By maintaining personal logs of these names, rather than deleting the names, gay men would be in a better position to have partners informed of STD/HIV exposure. Bathhouses and Network-Informed Interventions Bathhouses and sex clubs are venues where men who seek multiple partners seek out other men who seek multiple partners. From a network perspective, these venues provide an environment that facilitates concurrency and rapid partner change among both high-risk and low-risk men. Currently, there is little consensus on what constitutes a well-run educational program within a bathhouse. Nor are there data as to what percentage of bathhouse patrons take part in STD/HIV testing programs. Other than a dearth of identifying information about bathhouse partners to facilitate partner notification, challenges include encouraging disclosure of HIV status in a setting that does not favor open communication. For example, data collected from a Los Angeles convenience sample show that 85% of men do not discuss HIV status in bathhouses. 27 Moreover, studies show that many bathhouse and sex club patrons are likelier to use illicit drugs than are those who do not use such facilities. 28
4 Vol. 32 No. 10 supplement USING SEXUAL NETWORKS TO REDUCE STD/HIV TRANSMISSION S51 Entrance Strategies: Making the Marketplace Safer Versus Making Men Better Shoppers Bathhouses and sex clubs typically allow outreach initiatives and STD/HIV testing by outside agencies and, sometimes, in collaboration with their own staff. In addition, sex club managers typically post messages in several locations, encouraging frequent testing and discouraging high-risk behavior. In San Francisco, CA, for example, staff members inform patrons of club rules at entry. Local policies require reviewing club rules with patrons verbally, which may also involve written and verbal consent. Anecdotal evidence suggests that verbally reviewing club rules with patrons at entry helps establish a norm favoring condom use and lays the groundwork for further enforcing the behavior in clubs where monitoring is possible. 29 These clubs do not have private rooms, which thus facilitates enforcement. A recent small-scale experiment in Seattle indicates that encouraging disclosure of HIV status in bathhouses and sex clubs may be acceptable. A group of HIV-positive individuals obtained consent from a local venue to hand all patrons 3 stickers, one indicating HIV-positive, one HIV-negative, and one??, one of which to post on their room doors. Each person received the 3 stickers and did not have to disclose their status to the outreach worker. Many patrons accepted these stickers, and some reported avoiding sex with partners of discordant status or engaging in safer sex based on the posted sticker. Of those surveyed, the majority wanted this event to be repeated. 30 Fragmenting Sexual Networks Through Sex Club and Bathhouse Policies In several cities, attempts have been made to prohibit unprotected anal sex in bathhouses and sex clubs. Some venues have implemented policies prohibiting unprotected anal sex and offer no private rooms, which facilitates enforcement; some have implemented similar policies but also provide private rooms, which renders enforcement difficult. Unfortunately, there have been no studies to test association between venue design and policy and persistence or reduction of high-risk sexual behavior. Conclusion MSM have created efficient ways of finding sexual partners. For disease control purposes, finding efficient (and acceptable) ways of reducing opportunities for STD/HIV transmission in MSM sexual venues needs to be accorded greater priority than has heretofore been the case. Historically, commercial sex venues have provided a rich marketplace where sex can be explicitly offered, sought, and arranged, with minimal social or moral constraints a context that has been insufficiently addressed by public health interventions. The advent of the Internet has greatly expanded opportunities for finding sexual partners fast and efficiently, requiring renewed intervention efforts. The sexual network perspective provides researchers, interventionists, and epidemiologists the opportunity to test various solutions. Although few interventions have been evaluated for efficacy in reducing STD or HIV transmission 4 (and none of these are reported in this paper), neither have many of the interventions currently being advocated for, or implemented in, these settings. 9,26 The need for ongoing data collection, especially from sites that cater specifically to high-risk men, is evident. Similarly, we do not yet understand how different club designs and policies in one metropolitan area may serve to disperse or concentrate the core. For example, in the San Francisco Bay Area, there are five sex clubs within the city limits, each with strict policies prohibiting unprotected sex and offering no private rooms. However, clubs offering private rooms and no prohibitions against unprotected sex are easily reachable in adjacent cities. Data are needed to determine whether core group members tend to select sex clubs with few rules, as well as to more efficiently target prevention resources. Intervening in MSM sexual networks and in the context in which men are meeting new sexual partners has the potential to reduce transmission even in the absence of interventions that can reduce individual risk behavior particularly among those at highest risk. These interventions will require a leadership commitment from public health workers and sensitivity to the tenets and values of the various MSM communities. Gay men and MSM have shown themselves to be highly capable of absorbing and understanding complex treatment information. There is every reason to believe that these same men can help educate their peers about sexual networks and to design and evaluate programs for their efficacy in reducing STD/HIV transmission. References 1. Stall RD, Hays RB, Waldo CR, Ekstrand M, McFarland W. The gay 90s: a review of research in the 1990s on sexual behavior and HIV risk among men who have sex with men. Aids 2000; 14(suppl 3): S Klovdahl A, Potterat J, Woodhouse D, Muth J, Muth S. HIV infection in an urban social network: a progress report. Bull Method Soc 1992; 1992: Potterat JJ, Rothenberg RB, Muth SQ. Network structural dynamics and infectious disease propagation. Int J STD AIDS 1999; 10: Rothenberg RB, Sterk C, Toomey KE, et al. Using social network and ethnographic tools to evaluate syphilis transmission. Sex Transm Dis 1998; 25: Neaigus A. The network approach and interventions to prevent HIV among injection drug users. Public Health Rep 1998; 113(suppl 1): Kelly JA, St Lawrence JS, Diaz YE, et al. HIV risk behavior reduction following intervention with key opinion leaders of population: an experimental analysis. Am J Public Health 1991; 81: Amirkhanian YA, Kelly JA, Kabakchieva E, McAuliffe TL, Vassileva S. Evaluation of a social network HIV prevention intervention program for young men who have sex with men in Russia and Bulgaria. AIDS Educ Prev 2003; 15: De P, Singh AE, Wong T, Yacoub W, Jolly AM. Sexual network analysis of a gonorrhoea outbreak. Sex Transm Infect 2004; 80: McFarlane M, Kachur R, Klausner J, Roland E, Cohen M. Internetbased health promotion and disease control in the 8 cities: successes, barriers and future plans. Sex Transm Dis 2005; 32(10)supplement: S60 S64.. 9a. Ciesielski C, Kahn R, Taylor M, Gallagher K, Prescott L, Arrowsmith S. Control of syphilis outbreaks in men who have sex with men: the role of screening in nonmedical settings. Sex Transm Dis 2005; 32(10)supplement:S37 S Woods WJ, Binson D, Pollack LM, Wohlfeiler D, Stall RD, Catania JA. Public policy regulating private and public space in gay bathhouses. J Acquir Immun Defic Syndr 2003; 32: Laumann EO, Youm Y. Racial/ethnic group differences in the prevalence of sexually transmitted diseases in the United States: a network explanation. Sex Transm Dis 1999; 26: Choi KH, Operario D, Gregorich SE, Han L. Age and race mixing patterns of sexual partnerships among Asian men who have sex with men: implications for HIV transmission and prevention. AIDS Educ Prev 2003; 15: Blower S, Service S. Calculating the odds of HIV infection due to sexual partner selection. AIDS Behav 1997; 1: Watts CH, May RM. The influence of concurrent partnerships on the dynamics of HIV/AIDS. Math Biosci 1992; 108: Morris M, Kretzschmar M. Concurrent partnerships and the spread of HIV. Aids 1997; 11:
5 S52 WOHLFEILER AND POTTERAT Sexually Transmitted Diseases October supplement Wood B. The manifesto and other STD & HIV prevention interventions for men who have sex with men, Seattle & King County, Washington. Presented at the Strategies to Address Sexually Transmitted Diseases and HIV Transmission among MSM conference. Atlanta, GA: July 1, Kent CK, Chaw JK, Chen YQ, Wohlfeiler D, JD K. Doubling of mean number of reported sex partners among men who have sex with men seeking STD services: San Francisco, [abstract 0320]. In: 15th Annual meeting of the International Society of Sexually Transmitted Disease Research. Ottawa, Ontario, Canada, Davies P, Reid D, Weatherburn P. Putting it About: Health Promotion for Gay Men with Higher Numbers of Sexual Partners: CHAPS R&D Briefing Papers. London: Sigma Research; Thomas JC, Tucker MJ. The development and use of the concept of a sexually transmitted disease core. J Infect Dis 1996; 174(suppl 2): S Stall R, Mills TC, Williamson J, et al. Association of co-occurring psychosocial health problems and increased vulnerability to HIV/ AIDS among urban men who have sex with men. Am J Public Health 2003; 93: Potterat JJ, Rothenberg RB, Woodhouse DE, Muth JB, Pratts CI, Fogle JS 2nd. Gonorrhea as a social disease. Sex Transm Dis 1985; 12: Taylor M, Montoya J, Cantrell R, et al. Interventions in the commercial sex industry during the rise in syphilis rates among men who have sex with men (MSM). Sex Transm Dis 2005; 32(10)supplement:S53 S Laumann E. Bathhouses and gay men/msm: a network perspective. Presented at the Implications of Sexual Networks for HIV/STD Prevention for Gay Men conference, Oakland, CA, Sept , McFarlane M, Bull SS, Rietmeijer CA. The Internet as a newly emerging risk environment for sexually transmitted diseases. JAMA 2000; 284: Peebles B. Comments made at the Strategies to Address Sexually Transmitted Diseases and HIV Transmission Among MSM conference, Atlanta, GA, July 1, Klausner J, Kent CK, Wolf W, et al. The public health response to epidemic syphilis, San Francisco, Sex Transm Dis 2005; 32(10)supplement: S11 S Bingham T, Secura G, King C. HIV prevalence, HIV incidence and risk behaviors among men seeking HIV testing and prevention services inside Los Angeles Bathhouses. Abstract 196. Centers for Disease Control and Prevention National HIV Prevention conference, Atlanta, GA, Parsons JT, Halkitis PN. Sexual and drug-using practices of HIVpositive men who frequent public and commercial sex environments. AIDS Care 2002; 14: Bense B. Problem or solution? California s experience with bathhouses. Abstract L3. National STD Prevention conference. San Diego, Spielberg F. Bathhouses and sex clubs: How risky are their patrons? How can that drive our programs and policies? Abstract B04. National STD Prevention conference. Philadelphia, PA, 2004.
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