© 2003 American Public Health Association
Beryl A. Koblin is with the New York Blood Center, New York, NY. Margaret A. Chesney and Thomas J. Coates are with the School of Medicine, University of California, San Francisco. Marla J. Husnik and Yijian Huang are with the Statistical Center for HIV/AIDS Research and Prevention, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, Wash. Sam Bozeman is with Abt Associates Inc, Cambridge, Mass. Connie L. Celum is with the Department of Medicine, University of Washington, Seattle. Susan Buchbinder is with the San Francisco Department of Public Health. Kenneth Mayer is with the Fenway Community Health Center, Boston, Mass. David McKirnan is with the Howard Brown Health Center, Chicago, Ill. Franklyn N. Judson is with Denver Public Health and the University of Colorado Health Sciences Center, Denver. Correspondence: Requests for reprints should be sent to Beryl A. Koblin, PhD, New York Blood Center, 310 E 67th St, New York, NY 10021 (e-mail: beryl_koblin{at}nybc.org).
Objectives. We describe the prevalence of risk behaviors at baseline among men who have sex with men (MSM) who were enrolled in a randomized behavioral intervention trial conducted in 6 US cities. Methods. Data analyses involved MSM who were negative for HIV antibodies and who reported having engaged in anal sex with 1 or more partners in the previous year. Results. Among 4295 men, 48.0% and 54.9%, respectively, reported unprotected receptive and insertive anal sex in the previous 6 months. Unprotected sex was significantly more likely with 1 primary partner or multiple partners than with 1 nonprimary partner. Drug and alcohol use were significantly associated with unprotected anal sex. Conclusions. Our findings support the continued need for effective intervention strategies for MSM that address relationship status, serostatus of partners, and drug and alcohol use.
After a decline in rates of HIV infection in the United States among men who have sex with men (MSM) in the late 1980s and early 1990s,1,2 reports indicate a resurgence in the spread of HIV and other sexually transmitted diseases (STDs) in this population. For example, in San Francisco, cases of rectal gonorrhea increased from 1994 to 1997,3 and during a period of reintroduction of syphilis in Seattle between 1997 and 2001, more than two thirds of those affected were MSM4; a similar outbreak of syphilis occurred in southern California in 2000.5 Other cities have reported increases in STD rates among MSM.6 Furthermore, evidence is accumulating that HIV prevalence rates among MSM are high in some cities79 and are increasing from levels observed in the late 1980s and early 1990s.1013 Research on interventions designed to prevent HIV acquisition and transmission actively continues in the areas of preventive vaccines, microbicides, STD control, and antiretroviral therapy. Because in many cases effective forms of these interventions are not yet available, there continues to be a critical need for interventions focused on initiating and maintaining behavior change. Research has been conducted to create and guide the development of behavioral interventions and to assess the efficacy of interventions in changing HIV risk behaviors among MSM.14,15 Although extensive changes in risk behaviors have been documented among MSM, large randomized clinical trials in which the study outcome is HIV infection, the most direct measure of an interventions effect, have not been conducted. To date, we are aware of only 1 trial of an HIV prevention intervention among MSM that involved a biological endpoint.16 However, that study did not include HIV infection as a study endpoint. The EXPLORE study is the first randomized trial conducted among MSM in the United States that was designed to test the efficacy of a behavioral intervention in preventing acquisition of HIV by using HIV infection as the endpoint. In this article, we describe risk prevalence rates at baseline among the studys large multisite cohort of MSM in an attempt to identify risk behaviors that may be continuing the HIV epidemic. Furthermore, we present data on relationships of specific HIV risk behaviors to the following known risk factors: type and number of sexual partners and alcohol and drug use. These data, in conjunction with the companion article by Chesney et al.17 describing the intervention in detail, illustrate the variations in the risk profiles of the study population and support the need for a multifaceted, individually tailored intervention.
Study Population From January 1999 to February 2001, men who were negative for HIV antibodies were recruited in 6 US cities: Boston, Chicago, Denver, New York, San Francisco, and Seattle. Men were eligible if they were aged 16 years or older and reported having engaged in anal sex with 1 or more men during the past year. Men were excluded if they reported that they had been involved in a mutually monogamous relationship for 2 or more years with a male partner known to be negative for HIV antibodies. Recruitment strategies varied by city but included advertising; street outreach and outreach at clubs, bars, bathhouses, sex clubs, health clubs, and video arcades; referrals from other cohort studies, current study participants, and community agencies and clinics; and use of Internet sites targeting MSM, community forums, mailings, and a recruitment video.
Data Collection Approximately 2 weeks after being screened, participants received their HIV and gonorrhea test results and underwent posttest counseling. Men who were negative for HIV antibodies were asked to enroll in the trial and were randomized to the intervention or control condition. Every 6 months, participants return for a behavioral assessment, HIV pretest counseling, and specimen collection and will do so until study completion (July 2003), each time obtaining test results and posttest counseling within 2 weeks. Participants with positive test results are referred for medical and social services.
Laboratory Testing
Data Management The statistical center provided each site with a laptop computer containing the ACASI program used to collect baseline risk assessment data. At least once per week, site staff transferred the data, and these files were processed to create SAS (SAS Institute Inc: Cary, NC) data sets. SAS data files were merged with supporting demographic and other baseline data used in the present analyses.
Study Monitoring
Statistical Analysis We included data collected at the screening and enrollment visits in our analyses. Global associations are presented for the analyses of alcohol and drug use and sexual risk, because occasions in which substance use and sexual risk were reported in the 6 months before baseline may not have been concurrent. For each classification of partner HIV serostatus, study participants were categorized as (1) having only 1 partner of that serostatus who was their primary partner, (2) having only 1 partner of that serostatus who was not a primary partner, or (3) having multiple partners of that serostatus, regardless of whether 1 of these partners was a primary partner.
We constructed z-score statistics in a pairwise fashion (Figure 1
Screening and Enrollment Screening visits took place between January 1999 and February 2001. Among the 4862 individuals screened, 4716 (97.0%) were found to be negative for HIV antibodies and eligible for study participation; 4295 (91.1%) enrolled. Men were recruited through a variety of methods: outreach to clubs, bars, and other public venues (22.7%); advertising (15.3%); mailings (13.6%); referrals from friends (13.3%); street outreach (10.7%); and referrals from clinics and physicians (10.4%). The remaining 14% of the participants were recruited through referrals from other research studies and community-based organizations and via community forums, the Internet, and a recruitment video.
The demographic characteristics of the population are presented in Table 1
Men enrolled in the study for a variety of reasons. A large percentage (57.5%) enrolled for what we classified as altruistic reasons: helping to stop the AIDS epidemic, believing that the study was important, giving to their community, or doing something to honor a person they knew who had HIV or AIDS or who had died of AIDS. Another 21.8% enrolled because they thought that they might feel more motivated to avoid risk-taking behaviors. Twelve percent enrolled to use the free services offered by the study (8.4% for free HIV testing and 3.6% for free counseling), and 3.2% enrolled to obtain current information about HIV research. Only 1.4% enrolled because a partner, friend, or family member wanted them to participate, and only 0.9% enrolled to receive monetary compensation for participating. Specimens to be used in determining biological endpoints were collected at the screening visit. Blood specimens for HIV antibody testing were collected from all enrolled participants. Almost all of the men (96.9%) donated a urine specimen for the leukocyte esterase test, and 70.8% had a rectal swab taken for rectal gonorrhea testing.
Baseline Risk Behaviors and STDs
With regard to specific sexual risk behaviors, 45.2% of the men reported engaging in unprotected receptive oral sex with ejaculation, 48.0% reported engaging in unprotected receptive anal sex, and 54.9% reported engaging in unprotected insertive anal sex. Among combinations of these 3 behaviors, 78.1% of the men reported unprotected receptive oral sex with ejaculation or unprotected anal sex (Table 2
The percentages of men who reported sexual risk behaviors varied according to the serostatus of their partners; the largest percentages of men reported each of these behaviors with HIV-negative partners, followed by partners of unknown status (Table 3
For alcohol and drug use, 26.2% of the men reported drinking alcohol at least 3 days per week, and 10.6% were heavy drinkers (i.e., they consumed at least 4 drinks per day or consumed an amount equal to 6 drinks per occasion). We found that marijuana was the noninjection drug most likely to be used (46.3% of men), followed by poppers (amyl nitrates) (36.6%); hallucinogens, including ecstasy (24.0%); cocaine (19.3%); and amphetamines (12.9%). Ten percent of the men reported recent injection drug use. Drug use and alcohol use also were examined by geographic region: East Coast (New York and Boston), Midwest/West (Chicago and Denver), and West Coast (San Francisco and Seattle). The largest between-region difference involved amphetamine use. The percentage of men reporting amphetamine use was higher in the West Coast region (20.0%) than in the East Coast (9.2%) or Midwest/West (9.1%) region. The percentage of men reporting heavy alcohol use was significantly higher in the Midwest/West region (14.3%) than in the East Coast (8.6%) or West Coast (9.2%) region. Between-region differences also were observed for marijuana use (West Coast: 52.4%; East Coast: 44.9%; Midwest/West: 41.3%), cocaine use (East Coast: 22.2%; Midwest/West: 19.2%; West Coast: 16.5%), and use of hallucinogens (West Coast: 27.2%; East Coast: 25.0%; Midwest/West: 19.4%), although these differences were smaller (comparison Ps < .0001). No geographic differences were found in the use of poppers. Almost 13% of the men reported having had a specific STD in the 6 months before they enrolled in the study. The STD most frequently reported was chlamydia (4.2%), followed by gonorrhea (3.3%), genital or rectal warts (3.1%), and anogenital herpes (2.6%). Nonspecific STD symptoms were reported by 10.6% of the men. The symptoms most frequently reported were burning during urination and discharge from the penis (7.1%). Urine screening (via leukocyte esterase test) for nonspecific inflammation revealed 75 (1.8%) positive specimens; of 71 specimens sent for diagnostic testing for gonorrhea (via ligase chain reaction), however, only 3 were positive. Only 0.7% of the men had positive rectal gonorrhea cultures.
Situational Factors
Men who reported having used marijuana, poppers, hallucinogens, cocaine, or amphetamines in the 6 months before study enrollment were significantly more likely than men who did not use such drugs to report unprotected anal sex during that same period, regardless of the HIV serostatus of their partners (Table 4
Baseline data from the EXPLORE behavioral intervention trial illustrate a number of features that are critical for the conduct of this trial and that can provide information for the conduct of other intervention trials among MSM. Furthermore, these baseline data underscore that the HIV epidemic among MSM residing in the United States continues to be a major public health issue. One relevant study feature was the recruitment of a large cohort of high-risk MSM. This recruitment effort was the result of a coordinated effort among and within study sites and a variety of recruitment methods.18 Almost half of the EXPLORE respondents were recruited via direct street outreach and outreach at venues frequented by MSM, in conjunction with advertising efforts. The remainder of the cohort was recruited by means of a variety of strategies that were necessary to facilitate the recruitment of younger men and minority men, important subpopulations of MSM at particular risk. One of the challenges in developing an effective intervention is to ensure that it is relevant to population subgroups and their circumstances. Previous studies have shown that MSM base their choice of whether to engage in unprotected anal sex on several partner or relationship characteristics, including known or perceived partner serostatus, relationship status (e.g., regular vs casual), and number of partners.1922 Most researchers have found that elevated risks are associated with primary partners. In contrast, the EXPLORE baseline data indicate that men with multiple partners of unknown and positive status were engaging in just as much unprotected anal sex as were men with only 1 primary partner. This finding is of particular concern, as such situations carry risks of disease acquisition from partners who are HIV positive, a group that includes recently infected men who may report that they are HIV negative but who in fact may be highly infectious. EXPLORE also showed that men with multiple partners positive for HIV antibodies were more likely to report unprotected insertive anal sex than unprotected receptive anal sex. From a risk reduction perspective, these men may be taking a calculated risk, in that unprotected insertive anal sex carries a significant but lower risk of HIV acquisition relative to unprotected receptive anal sex.23 Almost 25% of men with multiple partners positive for HIV antibodies reported unprotected receptive anal sex, a percentage only slightly lower than that observed among men with 1 primary positive partner. Clearly, this is a situation involving high risk of HIV transmission. Finally, there is the possibility that "negotiated safety" discussions are occurring among these men and their antibody-negative partners,20,22 although this aspect of relationships was not assessed in the EXPLORE study. About half of the men with 1 primary HIV-negative partner reported unprotected sex. These data support the need to understand the relationship status and known or perceived serostatus of potential partners before counseling MSM about sexual risk. Interventions targeted at MSM also need to directly address use of alcohol and drugs. Of particular concern is the high proportion of EXPLORE men who reported drug use and engaging in unprotected receptive anal sex with partners of positive and unknown status, the sexual behavior with the highest risk. Although the present analysis demonstrates only the correlation between sexual risk and substance use, this combination has been observed in numerous studies conducted among MSM2426 and continues to be an important factor in defining sexual risks in this population. Furthermore, given that 10% of the study population reported recently injecting drugs, interventions must inquire about injection drug use and provide guidance for prevention strategies. Finally, and of significant concern, this contemporary cohort of MSM is at high risk of HIV infection. The largest US observational cohort investigation of MSM preceding the EXPLORE study was the first HIVNET Vaccine Preparedness Study (VPS-1), which was conducted from 1995 to 1997 at the same study sites as EXPLORE. The VPS-1 cohort exhibited an HIV incidence rate of 1.55 per 100 person-years, a high incidence.27 The level of baseline risk behaviors in the EXPLORE cohort was higher than that of the VPS-1 cohort (unpublished HIVNET data), owing in part to differences in mode of questionnaire administration (ACASI vs interview) but also as a consequence in part of EXPLOREs efforts to increase the proportions of younger men and minority men in the cohort. The EXPLORE baseline data, in conjunction with information on the ongoing resurgence of STDs, increased HIV incidence rates, and changes in risk behaviors among MSM in many US cities, emphasize the continued need for effective behavioral strategies designed to prevent HIV infection among MSM.
Support for this study was provided by the National Institute of Allergy and Infectious Diseases through the HIV Prevention Trials Network (grant numbers U01 AI46749 to Family Health International, with a subcontract to Abt Associates Inc; grant U01 AI48016 to Columbia University; grant U01 AI47981 to the University of Washington; grant U01 AI48040 to the Fenway Community Health Center; and grant U01 AI47995 to the University of California San Francisco). We gratefully acknowledge the contributions of the study participants. The members of the EXPLORE Study Team are as follows: Fenway Community Health Center: Felipe Agredano, Rodrigo Barahona, Keith Bell, Christine Borges, Manual Burnias, Mark Cayabayab, Dan Church, Allison Cohn, Yvonne Colon, Janet Dargon, Nancy DeSousa, Judy Erdman, Josh Gagne, Eliza Goodhue, Juan Jimenez, William Johnson, Wilfred Labiosa, Ana Lara, Darren LeBlanc, Vin Longo, Marc Manseau, Marshall Miller, Matthew Mimiaga, Elie Mohns, Arnel Montenegro, David Pantalone, Oscar Patino, Tracey Rogers, Edual Ruiz, Liz Salomon, Julio Silva, Laura van der Leeden, Rodney VanDerwarker, and Curt Weber. Howard Brown Community Health Center: Althea Batticks, Jason Bird, Liz Bradshaw, Robert Brown, Tom Buckingham, Toni Buckingham, Kelly Carson, Irene Chubinsky, Scott Clark, Scott Cook, Jeff Eichholz, Erica Gaffold, Sanford Gaylord, Mark Hartfield, David Henry, Brent Hope, Dale Gluth, Shane Gosselink, Jenny Hopwood, Laura Hosto, Jennifer Howard, D. J. Jacques, Heather Jandura, Susan Killelea, Andy Knight, Simone Koehlinger, Melissa Kohnke, Felicity LaBoy, Han Lee, Kandis Martin, Nicole Martin, Michele McGrady, Cheron McNeal, Denise Miles, Gino Moore, Michael Munn, Jose Narvaez, Aisha Nawab, Arlette Oblaza, Kevin OKeefe, Liz Perez, Elisse Pertiller, Kelly Picketts, Borris Powell, Chris Powers, Bart Ramey, Ingrid Rodriguez, Laurez Rutledge, Porfirio Sanchez, Michael Saven, Chris Schmidt, Mark Schulze, Jim Skinner, David Snyder, Al Sorrese, Justin St. Andre, Gerry Taranzo, Ted Taylor, Sonia Torres, Kristin Vanfossan, Gregory Victorianne, and Erik Wetz. Denver Public Health: Misty Aas, Ramon Armendariz, Chloe Bailey, Brian Bost, Julie Caine, David Cline, Stuart Cooper, Kent Curtis, Beth Deyo, John Douglas, Michael Furhman, Rene Gonzalez, Jeff Hiller, Paul Huber, Sharon Huber, Ken Miller, Philip Osteen, Laurie Peter, Doug Robinson, Dave Ward, Tim Wright, and Andrew Yale. New York Blood Center: Anne Aldrich, Louise Austin, Lynne Bartell, Jane Bensel, Roberta Bernet, Damian Bird, Adam Bonilla, Carolyn Booher, Michael Camacho, Bradley Clark, Kent Curtis, Nikki Englert, Tonya Flores, George Gates, Corinne Geller, Octavio Gonzalez, Denise Goodman, Krista Goodman, Joshua Hinson, Sean Lawrence, Thomas Lee, Jay Loeffel, Angelo Luna, Larry Metzger, Carolle Morris, Patrick OQuinn, Eric Ortiz, Ofiji Parris, Alfredo Perez, Terrence Precord, Alberto Rodriguez, Jason Santiago, Craig Siulinski, Leah Strock, Paul Teixeira, Eric Torres, Francesca Valenti, Curt Weber, Avery White, and Jess Zimmerman. University of Washington: Scott Britt, Fransing Daisy, Aline Dang, Tennessee Dickenson, Niles Eaton, Terry Elliott, Raymond Evans, Paul Farley, Mark Fleming, George Froehle, Jerome Galea, Hal Garcia-Smith, Patrick Gonzalez, Bruce Gooding, Krista Goodman, Justin Haines, Keifa Herzog, Rick Hieb, Eric Hildebrandt, Damon Jameson, E. J. Janson, Thom Kelty, Bill Krutch, Erin Lennon, Matt Leidholm, Alfredo Lopez, Paul Louey, Matt Meko, Jenny Melmed, Dany-Paul Mucha, Shelley Ozscuro, Joe Picciano, Jim Price, Monica Rayne, Alex Rodriguez, Barbara Steele, Nancy Stoaks, Jason Stucky, Matthew Swank, Stephen Tabet, Jeff Thompson, Dennis I. Torres, John Torres, Patrick Tschumper, Paul B. Verano, Ken Wheeler, and Robert Yoon. San Francisco Department of Public Health: Jonas Abella, Mike Ahern, Ari Bacharat, Alba Barreto, Christopher Boyden-DeShazer, Jesse Brooks, Meredith Broome, Tony Buckman, David Colbert, Emily Cole, Grant Colfax, Joao De Sales, Alfonso Diaz, Michael Edgar, Beth Faraguna, Paige Fratesi, Vincent Fuqua, Reggie Gage, Anjali Garg, Dale Gluth, Ted Guggenheim, Gavin Hall, Thomas Knoble, Rachel Langdon, Irene Lee, Jennifer Lessard, Nicole Lightburn, Tim Matheson, Corvette Moore, Mario Moreno, Paul OMalley, Jennifer Owen, Jesus Perez, Robin Rifkin, Chris Rubino, Mateo Rutherford, Jennifer Sarche, Georgia Schreiber, Rob Schwarz, Craig Siulinski, John Stryker, Jason Tomasian, Jim Touchstone, Seth Watkins, Sarah Wheeler, Belinda Van, and Allison Zerbe. Center for AIDS Prevention Studies: Patrick Barresi, Kevin Filocamo, Cliff Leonardi, Scott Stumbo, and Matthew Troy. Abt Associates Inc: Dana Benet, Sam Clark, Anne Coletti, Michelle Culp, Kirsten Firla, Michael Iatesta, Maria Madison, Sean McKee, and George Seage. Statistical Center for HIV/AIDS Research and Prevention: Neil Albright, Geetha Beauchamp, Rana Bonnice, Lynette Browne, Claire Chapdu, Maya Covarrubias, Martina Deseyve, Lynda Emel, Alice Fisher, Eileen Hess, Sarah Holte, MaryAnn Klotz, Wolfe Maykut, Peter McDonnell, Barbara Metch, Geoff Minerbo, Lisa Ondrejcek, Jennifer Schille, Steve Self, and Al Williams. Human Participant Protection This study was approved by the institutional review boards of all institutions involved. Written informed consent was obtained from all participants.
Note. The content of this article does not necessarily reflect the views or policies of the National Institute of Allergy and Infectious Diseases or the HIV Prevention Trials Network, nor does mention of trade names, commercial products, or organizations imply endorsement by the US government. B. A. Koblin, M. A. Chesney, and T. J. Coates conceived the study and oversaw all aspects of its implementation. M. J. Husnik and Y. Huang performed the data analyses. S. Bozeman was responsible for protocol implementation. B. A. Koblin, C. L. Celum, S. Buchbinder, K. Mayer, D. McKirnan, and F. N. Judson supervised all aspects of study implementation at the individual research sites. All of the authors helped to conceptualize ideas, interpret findings, and review drafts of the article. Accepted for publication January 27, 2002.
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