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Sexually Transmitted Diseases:
doi: 10.1097/01.olq.0000233666.67788.fc
Editorial

Men Who Have Sex With Men and Women: Pieces of the U.S. HIV Epidemic Puzzle

Adimora, Adaora A. MD, MPH*†; Fullilove, Robert E. EdD†

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From the *Department of Medicine, School of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina; and the †Community Research Group, Columbia University School of Public Health, New York, NY

The authors greatly appreciate Dr. Victor J. Schoenbach’s insightful comments and review of the manuscript.

Correspondence: Adaora A. Adimora, MD, MPH, Division of Infectious Diseases, 130 Mason Farm Road, CB #7030, Bioinformatics Building, UNC School of Medicine, Chapel Hill, NC 27599-7030. E-mail: adimora@med.unc.edu

ALTHOUGH MANY STUDIES HAVE EXAMINED the behavior of men who have sex with men (MSM), public health research has devoted considerably less attention to the characteristics of men who have sex with both men and women (MSM/W) and the role that their sexual networks play in the HIV epidemic.

In this issue of Sexually Transmitted Diseases, Hightow et al confirm and extend the HIV epidemiology literature through their report of a study that examined both individual-level behaviors and sexual network characteristics among newly reported HIV-infected MSM/W (16%), MSM (57%), or only with women (MSW; 27%).1 Most of the men were black (69%), and 13% were college students. There were significant differences between MSM/W and both MSM and MSW, and the study identified several individual-level behaviors and network characteristics that increased MSM/W’s risk of HIV acquisition and transmission.

Estimates of the prevalence of male bisexual behavior in the general population are controversial mainly because of differences in sampling methods and in the manner in which bisexuality is defined. Nonetheless, estimates suggest that approximately 4% to 6% of men in the United States have been bisexually active during adulthood and 0.7% have been active during the past year.2,3 Between 62% and 79% of gay men have had sex with women; 15% to 26% of these men had been married to women.4

Few population-based studies report the prevalence of male same-sex activity among black men in the general U.S. population. The National Health and Social Life Survey, using a probability sample of men in the United States, found that the same proportion of black and white men (5%) had had sex with a men during adulthood.3 Among MSM, however, blacks are more likely than those of other races and ethnicities to be bisexually active,5–9 a finding consistent with the Hightow et al data.1

The extent of HIV transmission from MSM/W to women is also unclear. At least 14% of all men with AIDS in the United States between 1981 and 1990 were bisexual. Between 1981 and 1990, 11% of women with AIDS in the United States reported sex with a bisexual man as their only risk factor for HIV infection, and the proportions of AIDS cases resulting from sex with a bisexual man were 3 to 5 times higher among black and Hispanic women than among white women.7 In recent years, the proportion of female AIDS cases resulting from sex with a bisexual man appears to have fallen: 2% of women with AIDS reported sex with a bisexual man in 2004 (3% white, 2% black, and 2% Hispanic). However, risk factors for transmission are not reported for many women, especially blacks and Hispanics,10 so these data may underestimate the proportion of women with AIDS who had sex with a bisexual man. Ekstrand et al found marked reductions in risk behaviors among a cohort of bisexual men in San Francisco and concluded that they were “unlikely to be a common vector for spreading HIV infection to women.”11 Similarly, mathematical modeling analysis estimated that HIV transmission from MSM/W to women constituted a “relatively minor” portion of new HIV infections in the United States each year.12

No population-based data document HIV seroprevalence among MSM/W, and such data are unlikely to be forthcoming given the difficulties of studying this hidden population. The Centers for Disease Control and Prevention used venue-based sampling to estimate HIV prevalence among MSM in 5 cities that participated in the National HIV Behavioral Surveillance system.13 At least 320 of the 1,767 men identified themselves as bisexual. HIV prevalence was high (25%) overall and varied considerably by race/ethnicity: 46% among blacks, 21% whites, and 17% Hispanics. Moreover, almost half of the HIV-infected men had unrecognized infection, with blacks and Hispanics being more likely to be unaware of their HIV infection than whites (67%, 48%, and 18%, respectively). Many of these infections appeared to have been recently acquired.

There are few quantitative data on sexual behavior of MSM/W, and national probability samples and longitudinal surveys are especially lacking.14 Available estimates vary but overall suggest a relatively high prevalence of sexual risk behavior. Hightow et al found that MSM/W had more sex partners than MSM and were more likely to have syphilis.1 Indeed, there is some evidence that MSM/W belong to the core group of sexually transmitted infection (STI) transmitters, those with frequent partner change who help sustain STIs within the population. Moreover, in some studies, approximately one third of MSM/W reported unprotected anal sex with male partners.15,16 Others report higher levels of sexual risk behavior (noncondom use) with female than with male partners11,17 and describe greater participation in other behaviors that increase risk of HIV infection such as injection drug use1,14 and increased alcohol consumption among MSM/W compared with MSM.17

The extent of sexual interaction among MSM/W, other subpopulations, and the general population is equally difficult to define yet is of key importance in determining the contribution of MSM/W to population HIV transmission. Hightow et al1 and others4,18,19 have found that a substantial proportion of males who trade sex are MSM/W. Many of these men have wives or girlfriends, some of whom are also commercial sex workers. Moreover, many male sex workers perceive their clients as either bisexual or heterosexual, supporting the concept of bridging among MSM/W, other high-risk subpopulations, and the general population.20 Similarly, in Hightow et al’s study, MSM/W were also linked to the general population through their sexual contacts with college students.1

Because sexual networks are critical in the spread of STIs, specific examination of these networks illuminates key aspects of HIV transmission beyond the information typically gleaned from individual-level studies. MSM/W, by definition, act as a sexual network bridge between MSM and women with whom they have sex. Although in theory, bridging could be confined to isolated networks such as a “3-node component” composed of a bisexual man with concurrent long-term sexual relationships with a woman and another man, each of whom in turn has sex only with the MSM/W, the HIV-infected MSM/W in Hightow et al’s study population1 were apparently highly connected. Addition of MSM/W to the network of MSM and MSW HIV-positive students resulted in a much larger sexual network of people across more colleges, a finding that suggests that MSM/W played an important role in HIV transmission in this setting.

Debate in the popular press21,22 concerning bisexuality and the AIDS epidemic has mainly focused on HIV transmission from MSM/W to individual women, but the population of MSM/W appears relatively small, and the number of women they directly infect is probably small as well. Nevertheless, if, as demonstrated by Hightow et al in this study setting, MSM/W have a central role in connecting multiple sexual networks that would otherwise remain separate, MSM/W could have a substantial impact on population transmission.

Explanations for the markedly increased HIV rates among blacks have remained elusive but have focused on the high prevalence of STIs and on sexual network characteristics.23,24 The role of MSM/W is therefore especially relevant to the epidemiology of HIV infection among blacks because of the high HIV prevalence among black MSM and the apparently large proportion of them who have sex with women.5 Moreover, high rates of syphilis and other STIs facilitate HIV transmission through those networks.

In summary, despite the potential importance of MSM/W to population HIV transmission, there is relatively little information concerning the number of MSM/W and their sexual behavior. Hightow et al’s study adds to the literature by documenting HIV-positive MSM/W’s central role in sexually linking people across risk groups and geographic locations.1 The Hightow et al study supplies several missing pieces of the puzzle of the HIV epidemic among blacks. The data reveal an explosive combination of individuals who have sex within an extremely high-prevalence population of individuals, many of whom are unaware of their infection and may in fact have recently acquired it. Bisexual men act as bridges between this MSM subpopulation and the general population of black heterosexuals. It is indeed important to determine, as Hightow et al assert, whether the HIV epidemic among blacks travels within 2 loosely connected epidemics, one among MSM and one among heterosexuals or through “a single, highly interconnected epidemic among MSM, MSM/W, and heterosexuals.”1

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References

1. Hightow LB, Leone PA, MacDonald PDM, et al. Men who have sex with men and women: A unique risk group for HIV transmission on North Carolina college campuses. Sex Transm Dis 2006; 33:585–593.

2. Smith TW. Adult sexual behavior in 1989: number of partners, frequency of intercourse and risk of AIDS. Fam Plann Perspect 1991; 23:102–107.

3. Laumann EO, Gagnon JH, Michael RT, et al. The Social Organization of Sexuality. Chicago: The University of Chicago Press, 1994.

4. Doll LS, Beeker C. Male bisexual behavior and HIV risk in the United States: Synthesis of research with implications for behavioral interventions. AIDS Educ Prev 1996; 8:205–225.

5. Millett G, Malebranche D, Mason B, et al. Focusing ‘down low’: Bisexual black men, HIV risk and heterosexual transmission. J Natl Med Assoc 2005; 97:52S–59S.

6. Binson D, Michaels S, Stall R, et al. Prevalence and social distribution of men who have sex with men: United States and its urban centers. Journal of Sex Research 1995; 32:245–254.

7. Chu SY, Peterman TA, Doll LS, et al. AIDS in bisexual men in the United States: Epidemiology and transmission to women. Am J Public Health 1992; 82:220–224.

8. Doll LS, Petersen L, White C, et al. Homosexually and nonhomosexually identified men who have sex with men: A behavioral comparison. Journal of Sex Research 1992; 29:1–14.

9. Montgomery JP, Mokotoff ED, Gentry AC, et al. The extent of bisexual behaviour in HIV-infected men and implications for transmission to their female sex partners. AIDS Care 2003; 15:829–837.

10. HIV/AIDS Surveillance Report, 2004, vol 16. Atlanta: US Department of Health and Human Services, Centers for Disease Control and Prevention. Available at: www.cdc.gov/hiv/stats/hasrlink.htm. Accessed April 11, 2006.

11. Ekstrand ML, Coates TJ, Guydish JR, et al. Are bisexually identified men in San Francisco a common vector for spreading HIV infection to women? Am J Public Health 1994; 84:915–919.

12. Kahn JG, Gurvey J, Pollack LM, et al. How many HIV infections cross the bisexual bridge? An estimate from the United States. AIDS 1997; 11:1031–1037.

13. Centers for Disease Control and Prevention. HIV prevalence, unrecognized infection, and HIV testing among men who have sex with men—Five US cities, June 2004–April 2005. MMWR Morb Mortal Wkly Rep 2005; 54:597–601.

14. Doll LS, Ostrow DG. Homosexual and bisexual behavior. In: Holmes KK, Mardh PA, PFS, et al., eds. Sexually Transmitted Disease. New York: McGraw-Hill, 1999:151–162.

15. Heckman TG, Kelly JA, Sikkema KJ, et al. Differences in HIV risk characteristics between bisexual and exclusively gay men. AIDS Educ Prev 1995; 7:504–512.

16. McKirnan DJ, Stokes JP, Doll L, et al. Bisexually active men: Social characteristics and sexual behavior. Journal of Sex Research 1995; 32:65–76.

17. Wold C, Seage GR 3rd, Lenderking WR, et al. Unsafe sex in men who have sex with both men and women. J Acquir Immun Defic Syndr Hum Retrovirol 1998; 17:361–367.

18. Elifson KW, Boles J, Sweat M. Risk factors associated with HIV infection among male prostitutes. Am J Public Health 1993; 83:79–83.

19. Diaz T, Chu SY, Frederick M, et al. Sociodemographics and HIV risk behaviors of bisexual men with AIDS: Results from a multistate interview project. AIDS 1993; 7:1227–1232.

20. Morse EV, Simon PM, Osofsky HJ, et al. The male street prostitute: A vector for transmission of HIV infection into the heterosexual world. Soc Sci Med 1991; 32:535–539.

21. Denizet-Lewis B. Double lives on the down low. The New York Times Magazine, August 3, 2003.

22. Vargas JA. HIV-positive, without a clue; black men’s hidden sex lives imperiling female partners. The Washington Post, August 4, 2003, B:B. 01.

23. Adimora AA, Schoenbach VJ. Social context, sexual networks, and racial disparities in rates of sexually transmitted infections. J Infect Dis 2005; 191:S115–122.

24. Adimora AA, Schoenbach VJ, Martinson FE, et al. Heterosexually transmitted HIV infection among African Americans in North Carolina. J Acquir Immun Defic Syndr 2006; 41:616–623

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