HIV-1 Incidence Among Active Duty United States Army Personnel, September 21, 2004

Transcription

1 HIV-1 Incidence Among Active Duty United States Army Personnel, September 21, 2004 Protocol Approval By The George Washington University Medical Center Institutional Review Board IRB # U020403EX SUBMITTED BY Zahid Rathore, BS In Partial Fulfillment of the Requirements For the Masters of Public Health Degree from The George Washington University School of Public Health and Health Services Department of Epidemiology and Biostatistics

2 Table of Contents Table of Contents... 2 Acknowledgments... 3 Abstract... 4 Introduction... 4 Methods... 5 Results... 6 Discussion References

3 Acknowledgments I am indebted to Warren B. Sateren, MPH for all his help and support on this project. His advice has been invaluable. Special thanks is also extended to Dr. Nelson Hsing and Dr. Dante Verme for their guidance and support during my time at The George Washington University, School of Public Health & Health Services. Lastly, I would like to thank my family and friends for their endless support. 3

4 HIV-1 Incidence Among Active Duty United States Army Personnel, Zahid Rathore, BS Preceptors: Warren B. Sateren, MPH, Phillip O. Renzullo, PhD, Mark J. Milazzo Abstract Objective: As the HIV-1 epidemic grows in unique sub-populations, surveillance provides valuable information for tracking the HIV-1 epidemic. Long-term follow-up of cohorts offers the opportunity to determine the rate and risk of new HIV-1 infections. The active duty component of the U.S. Army is a good cohort with which to monitor HIV-1 infection trends in the U.S. because it is a dynamic cohort into which young, sexually active people are continuously added and removed. Methods: Data was extracted from the U.S. Army Medical Surveillance Activity (AMSA) database and trends in HIV-1 infection were assessed using SAS software. Incidence rates among the population and sub-groups were calculated as the number of HIV-1 infections per 1,000 person years of follow-up. Unadjusted and adjusted relative risk estimates were calculated using Poisson regression. Results: 1,410 incident HIV-1 infections were detected among 1,732,419 soldiers who were on active duty at any time between 1985 and 2003, contributing 9,582,252 PY of follow-up. Overall HIV-1 incidence rates declined from a high of 0.46 per 1,000 PY in 1985/86 to 0.07 per 1,000 PY in the first six months of Incidence rates were highest among year olds (0.17 per 1,000 PY), blacks (0.34 per 1,000 PY), males (0.16 per 1,000 PY), unmarried soldiers ( per 1,000 PY), personnel who have served less than three years (0.19 per 1,000 PY), and enlisted personnel (0.18 per 1,000 PY). Occupational analysis revealed that incidence rates were highest among enlisted healthcare (0.26 per 1,000 PY) and non-occupational personnel (0.28 per 1,000 PY). Among officers, health care personnel had the highest incidence rate (0.09 per 1,000 PY). Both unadjusted and adjusted relative risks were highest among black personnel (RR = 4.63) compared to white personnel. Conclusion: While overall incidence rates have declined over the 18-year followup window, incidence rates have risen in the past several years among certain sub-populations, specifically, young, black, single, enlisted soldiers. Continued surveillance is vital in order to identify the high-risk populations, especially given the recent increase in HIV-1 incidence worldwide. Introduction The objective of this project was to reevaluate HIV-1 infection trends among active duty United States army personnel, tested between 1985 and Previous studies (Renzullo, et al, 2001) have documented HIV-1 infection trends among the same population from 1985 to As the HIV-1 epidemic grows within the United States, several studies have documented that the HIV epidemic is propagating from unique socioeconomic and racial populations (Ruiz, 2000). The thoroughness of military health records lends to a unique opportunity to collect data on, in this case, a young, racially/ethnically and geographically diverse, sexually active population whose characteristics parallel those in the general population who could be at risk for acquiring the HIV virus. Surveillance continues to provide valuable information for tracking the HIV-1 epidemic. Information gathered from this activity can be used not only to describe the dynamics of the maturing epidemic, but can also be used to develop and disseminate effective, targeted prevention programs for those at highest risk. Additionally, periodic and timely 4

5 determination of the rate of new infections is vital for evaluating the success of HIV-1 prevention programs. Long-term follow-up of cohorts offers the opportunity to determine the rate and risk of new HIV-1 infections. Risk-based cohorts (including men who have sex with men (MSM) and injection drug users (IDU)) have provided excellent information on the risk of HIV-1 infection (Kaslow et al, 1987; Goedert et al, 1987; Winkelstein, et al, 1987; Hessol et al, 1989; Vlahov et al, 1991; Samuel et al, 1993). In addition to these cohorts, population-based cohorts consisting of individuals who may not be at high risk from HIV-1 infection can also provide information on the risk of HIV-1 infection in the general population. Since a number of the cohorts assembled in the 1980 s and 1990 s have aged considerably, they may no longer be representative of those currently at greatest risk of infection. The active duty component of the U.S. Army is a good cohort with which to monitor HIV-1 infection trends in the United States because it is a dynamic cohort into which young people are continuously added and removed. Active duty personnel undergo periodic and regular HIV-1 testing for both routine (biennial birth month testing, during physical exams every 2 to 5 years and prior to deployment) and adjunct (performed in association with medical evaluations) indications. Methods The cohort in this study consists of U.S Army personnel who were on active duty at anytime between November 1985 (the beginning of the Department of Defense HIV-1 testing program) and June 30, Data was extracted from the Army Medical Surveillance Activity (AMSA) database containing demographic, occupational information, along with HIV status. Blood serum samples from individuals were tested with a commercial ELISA. Samples that tested positive were retested in duplicate, and samples that were found to be repeatedly reactive were tested by Western blot analysis. A positive test was defined as a reactive ELISA followed by a diagnostic Western blot (at least two of the following bands: p 24, gp 41 and gp120 and/or gp160) with the same result from a second serum specimen. A negative 5

6 test was defined as a non-reactive Western blot. Indeterminate Western blot results were further verified using other non-diagnostic tests including PCR. Endpoints were either a first documented positive HIV-1 antibody test or a last negative antibody test prior to June 30, The seroconversion date was defined as the midpoint between the dates of the last HIV-1 negative test and the first HIV-1 positive test. Personyears (PY) accrued from the first negative HIV-1 test date to the seroconversion date (for seroconverters) or up to the most recent negative test date (for non-serconverters). HIV-1 incidence rates were calculated as the number of HIV-1 seroconversions per 1,000 PY of follow-up. Data was analyzed using the SAS statistical software package (SAS V 8.0, Cary, NC). Trends in HIV-1 infection were assessed with demographic variables that included: year, age, race/ethnicity, gender, marital status, length of service, rank/grade, and occupational group. Age was grouped into those less than 20, 20 to 24, 25 to 29 and those 30 and older. Marital status was grouped into married or unmarried (which includes separated / divorced). Length of service was categorized at less than 3 years or 3 or more years of service. Race/ethnicity was self-reported and individuals were coded as white, black, Hispanic or other. Other includes the small number of Asian / Pacific Islanders and American Indians in the U.S. Army cohort (4% of HIV-1 seroconverters). Records with incomplete data were removed from analysis, including records with inaccurate date of birth values. HIV-1 incidence rates (and their 95% confidence intervals) among the population and sub-groups were calculated as the number of HIV-1 infections per 1,000 PY of follow-up. Unadjusted and adjusted relative risk estimates (and 95% confidence intervals) for the association between demographic variables and HIV-1 infection were calculated using Poisson regression. Mapping was conducting using ArcView software (ArcView v. 3.2, ESRI, Redlands, CA). These maps display the pattern of home-of-record to HIV-1 positive Army active duty personnel. Results Since the DoD began the HIV-1 testing program in October 1985, 1,410 incidence HIV-1 infections have been detected among 1,732,419 soldiers who were on active duty at any time 6

7 between 1985 and 2003, contributing 9,582,252 PY of follow-up. Figure 1 displays the overall incidence rates per 1,000 PY from 1985/86 to 2003 as well gender specific rates. Overall HIV-1 incidence rates declined dramatically from a high of 0.46 per 1,000 PY in 1985/86 to 0.07 per 1,000 PY in the first six months of Similar results can be seen for the incidence rates for both men (0.48 per 1,000 PY in 1985/86 and 0.08 per 1,000 PY in 2003) and women (0.28 per 1,000 PY in 1985/86 and 0.03 per 1,000 PY in 2003). Figure 1. Annual HIV-1 incidence rates per 1,000 PY by gender among US Army active duty personnel, Incidence Rate per 1000 PY Overall Women Men Year Table 1 presents the HIV-1 incidence rates associated with 6 demographic variables (age, race, gender, marital status, length of service and rank/grade). Incidence rates were highest among year olds (0.17 per 1,000 PY), blacks (0.34 per 1,000 PY), males (0.16 per 1,000 PY), unmarried soldiers ( per 1,000 PY), personnel who have served less than three years (0.19 per 1,000 PY), and enlisted personnel (0.18 per 1,000 PY). Table 2 presents the HIV-1 incidence rates associated with military occupational groups for both enlisted and officer personnel. Among enlisted personnel, health care staff have the highest incidence rate (0.26 per 1,000 PY). Similarly, among officers, heath care staff have the highest incidence rate (0.09 per 1,000 PY). 7

8 Unadjusted relative risks (RR) rates (see table 1) were highest among personnel under the age of 25 (1.00) as compared to other age groups with the RR declining to 0.66 for those over 30. Blacks were 4.63 times more likely to acquire HIV-1 infection than white personnel, while Hispanics were at 1.51 times greater risk. Males had a 2.28 greater risk when compared to females, and unmarried personnel had a 1.97 greater risk than married personnel. Lastly, enlisted health care personnel were at 2.69 times greater risk than other enlisted occupations. Similar results were found among officers with health care officers having a RR of 1.37 for HIV-1 infection. When examining the adjusted RR (see table 1), which was adjusted for year, gender, race/ethnicity, age, marital status, rank/grade, and length of service, similar population subgroups were at risk when compared to the unadjusted relative risks. Blacks were 4.63 times more likely to acquire HIV-1 infection than whites, while Hispanics were at 1.62 times greater risk. Males had a 3.18 greater risk when compared to females, and unmarried personnel had a 1.82 greater risk than married personnel. Much like the results from the unadjusted analysis, enlisted health care personnel had a 2.98 greater risk of HIV-1 infection, while health care officers were 7.44 times more likely to acquire HIV-1 infection. HIV-1 incidence and unadjusted relative risks of HIV-1 infection showed a decline with increasing age. This however changed in the adjusted model where increasing age was associated with increased HIV-1 risk. Those aged between 25 and 29 and those older than 30 were approximately 50% more likely to acquire HIV-1 infection in the adjusted model, which was statistically significant. 8

9 Table 1. HIV-1 incidence and relative risks among US Army active duty personnel, 1985/ Relative Risk Demographic Variable Total Number of n (%) HIV-1+ Incidence rate (95%CI) Unadjusted (95%CI) Adjusted (95% CI)* Person Years (PY) Age < , (7%) 0.17 (0.13-) ,884, (36%) 0.18 ( ) ( ) ,256, (26%) 0.16 ( ) 0.91 ( ) 1.58 ( ) 30 3,856, (31%) 0.12 (-0.13) 0.66 ( ) 1.49 ( ) Race White 5,836, (30%) 0.07 ( ) Black 2,529, (61%) 0.34 ( ) 4.63 ( ) 4.63 ( ) Hispanic 671, (5%) 0.11 ( ) 1.51 ( ) 1.62 ( ) Other 484, (4%) 0.11 ( ) 1.50 ( ) 1.55 ( ) Gender Male 8,309, (87%) 0.16 ( ) 2.28 ( ) 3.18 ( ) Female 1,261, (13%) 0.07 ( ) Marital Status Married 5,334, (56%) ( ) Unmarried 4,246, (44%) ( ) 1.97 ( ) 1.82 ( ) Length of Service < 3 years 2,613, (27%) 0.19 ( ) years 6,969, (73%) 0.13 ( ) 0.70 ( ) 0.75 ( ) Rank/Grade Officer 2,241, (23%) 0.04 ( ) 0.23 ( ) 0.34 ( ) Enlisted 7,312, (76%) 0.18 ( ) * Adjustment was performed based on year, gender, race/ethnicity, age, marital status, rank/grade and length of service.

10 Table 2. HIV-1 incidence and relative risks among US Army active duty enlisted and officer personnel, 1985/ Relative Risk Demographic Variable Total Number of n (%) HIV-1+ Incidence rate (95%CI) Unadjusted (95%CI) Adjusted (95% CI)* Person Years (PY) Enlisted Occupations Infantry 1,860, (20%) 0.14 ( ) 1.46 ( ) 1.49 ( ) Electronic 397, (5%) 0.18 ( ) 1.82 ( ) 1.86 ( ) Communication 736, (10%) 0.19 ( ) 1.92 ( ) 2.03 ( ) Health Care 557, (11%) 0.26 ( ) 2.69 ( ) 2.98 ( ) Other Technical 226, (3%) 0.19 ( ) 1.90 ( ) 2.03 ( ) Administration 1,363, (26%) 0.25 ( ) 2.60 ( ) 2.58 ( ) Electric / Mechanical 1,031, (8%) ( ) Crafts workers 163, (2%) 0.13 ( ) 1.31 ( ) 1.34 ( ) Supply Handlers 898, (12%) 0.18 ( ) 1.85 ( ) 1.80 ( ) Non-Occupational 75, (2%) 0.28 ( ) 2.84 ( ) 3.37 ( ) Officer Occupations Not Identified 707,071 2 (2%) (-0.01) - - General 10,707 0 (0%) (-) - - Tactical 559, (28%) 0.05 ( ) 0.70 ( ) 3.14 ( ) Intelligence 104,029 4 (4%) 0.04 (-0.08) 0.58 ( ) 2.77 ( ) Engineering 195, (14%) 0.07 (0.03-) Scientists 83,845 2 (2%) 0.02 ( ) 0.36 ( ) 1.60 ( ) Health Care 273, (27%) 0.09 ( ) 1.37 ( ) 7.44 ( ) Administrators 115,543 8 (9%) 0.07 ( ) 1.04 ( ) 4.91 ( ) Supply Officers 163, (14%) 0.08 ( ) 1.19 ( ) 4.70 ( ) * Adjustment was performed based on year, gender, race/ethnicity, age, marital status, rank/grade and length of service. 10

11 Figure 2 (a-f). Overall incidence rates per 1,000 PY by gender, race/ethnicity, age, marital status, rank/grade and length of service, 1985/ Male Female White Black Hispanic Other < >30 Married Unmarried Officer Enlisted < 3 years >= 3 years 11

12 Figure 3 (a-b). Occupational incidence rates per 1,000 PY by enlisted personnel and officers, 1985/ Infantry Electronic Communication Health Care Other Technical Administration Electric / Mechanical Crafts workers Supply Handlers Non- Occupational Not Identified Officer General Tactical Intelligence Engineering Scientists Health Care Administrators Supply Officers Non- Occupational Figures 2 (a-f) and 3 (a-b) graphically display incidence rates by gender, race, age, marital status, rank, length of service and occupation (for enlisted personnel and officers). Incidence rates were highest among males, blacks, year olds, unmarried personnel, enlisted soldiers, those who have served less than 3 years, non-occupational enlisted personnel, and health care officers. 12

13 Figures 4 (a-d) and 5 (a-c) graphically display incidence rates by several variables (including: race, age, marital status, rank, length of service, and gender stratified by race) by year. These graphs display an overall reduction in HIV-1 infection over time, however, there are several findings of note. Specifically, rates among blacks, black males, black females, and unmarried personnel are, in some cases, substantially higher and depart from the declining trend. Figure 6 graphically displays incidence rates among males by race, age and marital status. Incidence rates were highest for year old unmarried black males among all unmarried black males, year old married black males among all married black males, and 30 year old and over unmarried Hispanic males among all Hispanic males. Incidence rates were the highest for 30 year old and over unmarried white males among all white males. Figure 7 graphically displays incidence rates among males by year and rank. Declines in HIV-1 infection over the 18 years of follow-up are considerable. However, rates among blacks, both enlisted personnel and officers, are consistently and dramatically higher. Figure 8 graphically displays incidence rates among males by year, marital status and race. Much like the results seen in figure 7, incidence rates have declined dramatically, however rates among married and unmarried blacks are statistically significantly elevated when compared to whites and individuals from all other races. Figure 9 displays the prevalence of HIV-1 infection among personnel based on the individual home of record zip code which is grouped by county. Home of record zip code is defined as the individuals home county of residence prior to military service. While HIV-1infection is existent virtually everywhere throughout the U.S., clustering of higher prevalence exists in the south, southeast, and northeast. 13

14 Figure 4 (a-d). Incidence rates per 1,000 PY by race, age, marital status and rank by year Age < 25 Age 25 to 29 Age White Black Hispanic Other Enlisted Officer / Warrant Not Married Married

15 Figure 5 (a-c). Incidence rates per 1,000 PY by length of service, and gender stratified by race by year < 3 Years of Service 3+ Years of Service White Male Black Male Hispanic Male Other Male White Female Black Female Hispanic Female

16 Figure 6. Incidence rates (with 95% confidence intervals) per 1,000 PY among male active duty U.S. Army Personnel 1985/ by race, age and marital status. Figure 7. Incidence rates per 1,000 PY among male active duty U.S. Army Personnel 1985/ by year and rank. 16

17 Figure 8. Incidence rates per 1,000 PY among male active duty U.S. Army Personnel 1985/ by year, marital status and race. Figure 9. Prevalence of HIV-1 infection among US Army active duty personnel, by county. 17

18 Discussion Given the sensitivity surrounding sexual preferences and behavior among individuals in the military, unique challenges are encountered in military HIV epidemiological research. Resultantly, the military has not been a well-studied population for behavioral risk factors. The few studies that have been conducted have documented specific sexual behaviors and practices and their associated HIV-1 risks. Specifically, Renzullo, et al (1990) documented elevated risk of HIV infection associated with same-sex behavior, sexual activity resulting in contact with blood, sexual contact with prostitutes, and sexual contact with injecting drug users (IDU). Levin et al (1995) documented significant risk among military personnel who had had six or more lifetime sex partners, engaged in sex with partners on the first day of meeting, and had sex with three or more casual partners. Bray et al (1999), as part of a series of annual surveys of health related behaviors among military personnel, observed and documented prevalence and risk of sexually transmitted infections (STI) among military personnel. The lifetime prevalence of STI was 19.9% among Army personnel. In contrast to the gender disparity observed for HIV-1 infections in U.S. Army personnel, females reported a higher lifetime prevalence rate (29.5%) compared to males (18.3%). Among sexually active unmarried personnel, 44.3% reported they used a condom during their last sexual encounter. There are several possible explanations regarding the elevated (compared to civilian populations) STI prevalence rate among Army personnel including: young age, single marital status, living away from home for the first time, and being part of an environment where there is increased risktaking behavior. Bray et al also investigated the relationship between injecting drug use (IDU) and risk of HIV-1 transmission. Because the U.S. military has stringent drug testing policies (both routine and random screening) and strict zero-tolerance drug use policies, illicit drug use is typically low among military personnel when compared to civilians. Bray et al reported only 4.9% of all U.S. Army personnel had used any illicit drugs (other than marijuana) in 18

19 the previous 12 months. Risk factors for increased drug use included: younger age, lower educational level, being unmarried, lower rank/grade, and being male. Risk factors among military personnel derived from this analysis are consistent with risk factors in the general population. Similarities in demographic risk factors are evident among the military population including race (African-American), age (young), gender (males) and marital status (single). Reports from the CDC and WHO have documented that young, single, African-American, males are at highest risk for HIV infection (CDC, 2004). The results from this analysis corroborate the findings from the CDC and WHO. Additional analyses documented occupational risk associated with HIV-1 infection for the first time within a military population. Figure 2e clearly displays the difference in incidence rates among enlisted personnel and officers in general in which enlisted individuals have over four times greater incidence than officers (0.18/1,000 PY vs. 0.04/1,000 PY respectively). Figures 3a and 3b graphically displays incidence rates among 20 various occupational groups by rank. Among enlisted personnel health care workers had one of the highest incidence rates (0.26/1,000 PY), second only to those soldiers working in non-classifiable occupations (0.28/1,000PY). While incidence is significantly lower among officers, health care personnel again have the highest incidence rate (0.09/1,000 PY), followed by supply officers (0.08/1,000 PY). Black personnel have consistently higher HIV-1 incidence rates than all other races across the 18 years of follow-up. Figures 4a, 5b, 6, 7 and 8 clearly show this trend graphically. The difference between incidence rates for blacks when compared to other races (figure 4a) is dramatic despite reductions in overall HIV-1 incidence rates over the 18-year follow-up window. The difference in incidence rates among black personnel is even more pronounced in figure 5b, which displaces incidence rates of males by race. When comparing males by year, rank/grade and race (figure 6), it should be noted that incidence rates have declined; however between the time periods and both black enlisted personnel and black officers have dramatic increases in HIV-1 incidence. Similar trends are seen when comparing males by year, marital status and race 19

20 (figure 8). A substantial rise in incidence is seen among single black males between the and time periods. This should be of particular concern as this mirrors trends in the general population. Additional follow-up should include thorough monitoring of this sub-population. The disparity among HIV-1 incidence rates between married and not married personnel has increased over the 18-year follow-up window, which is seen in figure 4c. Similar trends are seen when comparing incidence rates among males by race, age and marital status in figure 6. As age increases among married black males, HIV-1 incidence decreases, while it remains higher and unaffected across all age groups among unmarried black males. As age increases among unmarried Hispanic males, there is a dramatic increase in HIV-1 incidence. There is a slight reduction in incidence among the complimentary married cohort of Hispanic males. Lastly, an increase in age among unmarried white males lends to an increase in HIV-1 incidence. There is no clear pattern among married white males or among males whose race is designated as other. Statistically significant relative risks for HIV-1 infection were also observed for certain occupational groups when adjusted for all other variables (year, gender, age, race/ethnicity, marital status, length of service), suggesting that there might be some unknown factor at work. Conversely, it has been well documented that the acquisition of HIV-1 via needle stick injuries is relatively low (for example Do, 2003) therefore this occupational risk is not a significant contributor to the risk among health care workers. No information was available concerning sexual risk behaviors or educational background. There have been some anecdotal reports suggesting MSM (men who have sex with men) might be over-represented in some occupations (health care) compared to others (infantry). Research is needed to identify current personal risk behaviors associated with HIV infection among military personnel. Since only partial data is available for 2003 (January June) it is important to continue surveillance activities among this population, especially given the rise in HIV incidence worldwide. As the HIV epidemic expands and evolves, it will be important to identify 20

21 and track the high-risk sub-populations. By identifying high-risk populations, prevention programs can be designed to effectively target those at highest risk for HIV-1 infection. 21

22 References Bray R., Sanchez R., Ornstein M., et al. (1999) Department of Defense survey of health related behaviors among military personnel. Research Triangle Institute Report RTI/7034/006-FR. Research Triangle Park, NC: DoD. Centers for Disease Control and Prevention. (2004). Cases of HIV infection and AIDS in the United States, by race/ethnicity, HIV/AIDS Surveillance Supplemental Report: 10(1). Also available at: http: // Do, AM. (2003). Occupationally acquired human immunodeficiency virus (HIV) infection: National case surveillance data during 20 years of the HIV epidemic in the United States. Infect Control Hosp Epidemiol. 24: Goedert J., Kesller C., Aledort L., et al. (1987). A prospective study of human immunodeficiency virus type I and the development of AIDS in subjects with hemophilia. New England Journal of Medicine. 321: Hessol N., Lifson A., O Malley P., et al. (1989). Prevalence, incidence, and progression of human immunodeficiency virus infection in homosexual and bisexual men in hepatitis B vaccine trials, American Journal of Epidemiology. 130: Kaslow R., Ostrow D., Detels R., et al. (1987). The multicenter AIDS cohort study: rationale, organization, and selected characteristics of the participants. American Journal of Epidemiology. 126: Levin L., Peterman T., Renzullo P, et al. (1995). HIV-1 seroconversion and risk behaviors among young men in the U.S. Army. American Journal of Public Health. 85: Renzullo, P., Sateren, W., Garner, R., Milazzo, M., Birx, D., McNeil, J. (2001). HIV-1 seroconversion in United States Army active duty personnel, AIDS. 15: Renzullo, P., McNeil J., Levin L., Bunin J., Brundage J. (1990). Risk factors for prevalent human immunodeficiency virus (HIV) infection in active duty Army men who initially report no identified risk: A case control study. Journal of AIDS. 3: Ruiz S., Gable A., Kaplan E., Stoto M., Fineberg H., Trussell J. (2000). No time to lose: getting more from HIV prevention. Committee on HIV Prevention Strategies in the United States, Division of Health Promotion and Disease Prevention, Institute of Medicine, National Academy of Sciences. 22

23 Samuel M., Hessol N., Shiboski S., Engel R., Speed T., Winkelstein, W. (1993). Factors associated with human immunodeficiency virus seroconversion in homosexual men in three San Francisco cohort studies Journal of Acquired Immune Deficiency Syndrome. 6: Vlahov D., Antony J., Munoz A., et al. (1991). The ALIVE study, a longitudinal study of HIV-1 infection in intravenous drug users: description of methods and characteristics of participants. NIDA Research Monographs. 109: Winkelstein W., Lyman D., Padian N., et al. (1987). Sexual practices and risk of infection by the human immunodeficiency virus: The San Francisco men s health study. JAMA. 257: