Recent condom use by arrested injection drug users in King County, Washington, USA

International Journal of Drug Policy 17 (2006) 222–229

Research paper

Recent condom use by arrested injection drug users in King County, Washington, USA Richard D. Burt a,∗ , Hanne Thiede a,1 , Elizabeth T. Barash a,2 , Keith Sabin b,3 a

Public Health Seattle-King County, 106 Prefontaine Place South, Seattle, WA 98104, USA b Global AIDS Project, Centers for Disease Control and Prevention, Atlanta, GA, USA

Received 20 December 2005; received in revised form 20 March 2006; accepted 25 March 2006

Abstract Background: Sexual transmission is a significant HIV infection route among injection drug users (IDU) in the United States and condom use is a primary means of HIV prevention. To help guide and evaluate public health measures to reduce HIV infection, we examined HIV prevalence among IDU and evaluated condom use levels, time trends and associations with sociodemographic, sexual and drug-related variables. Methods: Interviews and HIV screening were conducted among 1765 arrested IDU recruited from two jails (in Seattle and Kent) in King County, Washington, from 1998 through 2002. Results: HIV prevalence was 2.5%. Prevalence was higher for participants reporting a history of sex work and for men reporting male-tomale, which together accounted for 26 of the 44 HIV-positive participants. In the previous 6 months, among sexually active participants, 13% reported using condoms always, 22% sometimes and 65% never. There was a significant rise in condom use over time, with 14% reporting any condom use in 1998 and 44% in 2002. In both males and females, condom use rose as a function of the number of sexual partners; in females the rise was especially steep. Condom use was more likely to be reported by men reporting a recent male sex partner and less likely to be reported by amphetamine injectors. Condom use was less frequently reported by older participants than younger among those recruited at the Kent Jail but not the Seattle jail. Conclusions: The trend towards increasing likelihood of condom use over time and the tendency of Seattle-area IDU at highest risk to be more likely to report condom use suggest measurable, if modest, progress in reducing risk of sexual transmission of HIV among Seattle IDU. © 2006 Published by Elsevier B.V. Keywords: HIV; Injection drug users; Condoms

Introduction A substantial proportion of HIV infections in the United States (U.S.) occurs among injection drug users (IDU). The Centers for Disease Control and Prevention (CDC; 2005) estimates that 2004, in the 33 states with HIV reporting, 15% of persons with a diagnosis of HIV/AIDS were IDU and another 3% were male IDU who also reported sex with another man. ∗

Corresponding author. Tel.: +1 206 296 4580; fax: +1 206 205 4041. E-mail addresses: [email protected] (R.D. Burt), [email protected] (H. Thiede), [email protected] (E.T. Barash), [email protected] (K. Sabin). 1 Fax: +1 206 205 4041. 2 Fax: +1 206 205 5281. 3 Fax: +1 404 639 8105. 0955-3959/$ – see front matter © 2006 Published by Elsevier B.V. doi:10.1016/j.drugpo.2006.03.007

At least an additional 3% of HIV diagnoses were in persons reporting heterosexual contact with an IDU (Centers for Disease Control and Prevention, 2005), so that over 20% of HIV transmission in the U.S. is associated with injection drug use. Transmission of HIV by sexual contact is an important component of the contemporary injection drug-associated HIV epidemic in the U.S. In a cohort of San Francisco IDU, new HIV infection was more strongly associated with sexual transmission than with sharing of injection equipment (Kral et al., 2001). In a long-term follow-up of Baltimore IDU (Strathdee et al., 2001), among female IDU, recent diagnosis of a sexually transmitted disease (STD) was associated with more than twice the risk for new HIV infection, while injection-related variables showed no independent associa-

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tions. For males in this cohort, male-to-male sexual contact was independently associated with HIV incidence. There is strong evidence that condom use can substantially reduce the sexual transmission of HIV (National Institute of Allergy and Infectious Diseases, 2000). Three meta-analyses have found that condom use reduced HIV transmission by 80–95% (Centers for Disease Control and Prevention, 2001; Davis & Weller, 1999; Pinkerton & Abramson, 1997; Weller & Davis, 2005). Promoting condom use has been recognized as an important component of strategies to reduce transmission of HIV in the United States (Centers for Disease Control and Prevention, 2001). Increased use of condoms in transactions with sex workers has been reported to have been instrumental in reducing HIV prevalence among military recruits in Thailand (Nelson et al., 1996). Levels of condom use have been found to increase over time intervals in which HIV levels have fallen among pregnant women attending antenatal clinics in Uganda (Asiimwe-Okiror et al., 1997) and Zimbabwe (Gregson et al., 2006), although it is difficult to differentiate the specific contribution of condom use in these data from other changes in sexual risk behaviour. As sexual transmission accounts for a substantial proportion of HIV incidence in U.S. IDU, knowledge of the patterns of and trends in condom use in IDU can help guide public health policies to reduce the burden of HIV. From 1998 through 2002, the Kiwi study, as part of a collection of model surveillance systems for HIV among IDU, conducted an HIV behavioural and serologic survey of arrested IDU in King County, Washington, USA, which includes the city of Seattle and surrounding communities. We report here the pattern of HIV prevalence in this population and examine condom use among study participants it terms of overall levels, time trends and the associations of condom use with sociodemographic, sexual and drug-related characteristics.

Methods Study recruitment and data collection Participant recruitment and data collection methods are described in detail elsewhere (Thiede, Romero, Bordelon, Hagan, & Murrill, 2001). We recruited participants from the two jails in which the overwhelming majority of persons arrested in King County are incarcerated, one in downtown Seattle, serving primarily persons arrested within the city of Seattle, and the Kent Regional Justice Center, serving those arrested in suburban and rural communities in King County south of Seattle. Participants were recruited in two ways. First, recently arrested inmates were screened at jail intake during a series of randomly selected time slots. Second, inmates visiting the jail health clinics for HIV counselling and testing were screened. Inmates who met the eligibility requirements—having injected drugs within the past 12 months, being 18 years of age or older, and being able to communicate in English—were invited to participate. Recruit-

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ment started in the downtown Seattle jail in September of 1998 and at the Kent facility in November of 2000 and continued at both sites through December 2002. Following a blood draw, participants completed an interviewer–administered survey. Testing for HIV used an enzyme immunoassay (Abbott Laboratories, Abbott Park, IL, USA and Vironostika HIV 1 Micro ELISA system, BioMureiux, Durham, NC, USA). Positive test results were confirmed using Western blot (Novopath HIV-1 Immunopath, Biorad, Hercules, CA, USA). All participants provided informed consent and were offered both pre- and post-test counselling. Study procedures were reviewed and approved by the institutional review boards of the state of Washington State and the Centers for Disease Control and Prevention. Data analysis HIV prevalence and patterns of overall condom use are described for the total study population of 1765 participants. Time trends in condom use were evaluated for the 1417 participants reporting any vaginal or anal sex during the previous 6 months. To ensure consistency with other CDC sites participating in HIV serologic and risk behaviour studies in correctional facilities, the study questionnaire was revised on September 1, 2001. To circumvent problems posed by the differing formulations of the questions in the two questionnaire versions, we limited the analysis of associations of condom use with sociodemographic, sexual and drug-related characteristics to the 717 participants surveyed by this revised questionnaire. All major findings in this group were similar to those obtained from an analysis of the full Kiwi study population. Univariate associations were evaluated by χ2 statistics and time trends by a linear χ2 test for trend. Participants reporting having ever been paid for sex with money or drugs were classified as having a history of sex work. Male-to-male sex was defined in terms of reporting a male sex partner in the older questionnaire and with reference to anal sex with another male in the newer. The time frame for recent male-to-male sex was 1 year in the older questionnaire and 6 months in the newer. Logistic regression analysis was used to control for confounding. Any condom use during anal or vaginal sex in the past 6 months was defined as the outcome variable. We identified a set of potentially confounding variables whereby each variable was significantly associated with condom use in logistic regression models containing all the other variables and no other variable entered the model with a p-value less than 0.05. All pair-wise interactions among this collection of variables were investigated. Because the interaction between gender and number of sex partners was significant (pinteraction < 0.001), we constructed separate variables for numbers of sex partners in men and women. As we were concerned about differences in the participant populations from the two jails, interactions between jail site and the vari-

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ables significantly associated with condom use were also investigated. As an interaction between age and jail site was significant (pinteraction < 0.001), results for age are presented separately for participants recruited in Seattle and Kent. The final models included terms for age among recruits from Seattle and Kent, number of sex partners in men and women, calendar year of interview and participants’ primary injection drug. The reported p-values derive from likelihood ratio tests for entering a variable into a model controlled for all these variables. Adjusted odds ratios (ORs) and 95% confidence intervals (CIs) are reported only for variables found to have a significant association (p ≤ 0.05) with condom use in the logistic regression analysis.

Results Participant characteristics After eliminating duplicate interviews, a total of 1765 records were available for analysis. Of persons approached at jail intake for a screening interview 7.7% refused screening (Thiede, Romero, Bordelon, Hagan & Murrill, 2001). Of those screened and determined to be eligible, 60% eventually completed a study interview. Among participants completing an interview, 52% had been recruited at jail intake and 48% at the jail health clinics. The final study population was very similar to the eligible IDU screened at jail intake in terms of age (mean age in each group = 35 years; p = 0.56), racial

distribution (64% versus 67% white, respectively; p = 0.41) and sex (77% male in both groups; p = 0.96). HIV prevalence Of the 1748 participants with definitive test results, 44 (2.5%) were HIV seropositive (Table 1). Of the 39 HIVpositive participants from whom data were available on knowledge of their HIV status, 24 (62%) reported having tested previously positive. Compared with White participants, HIV prevalence was lower for Blacks and higher for Hispanics, although these differences were not statistically significant. Males reporting recent male-to-male sex or a history of sex work were significantly more likely to be HIV positive than others. Among men reporting a history of sex work, 61% reported never having had sex with another man. In this group, HIV prevalence was 2.7%, somewhat higher than that for men reporting neither sex with men nor sex work (1.5%) and well below that of men reporting ever engaging in male-to-male sex (9.8%). A history of either male-to-male sex or of sex work was reported by 26 of the 44 HIV-positive participants. Overall condom use Of the 1765 total participants, 1417 (80%) reported having had vaginal or anal sex during the previous 6 months, 308 (18%) reported no anal or vaginal sex within this time period, and 40 (2%) did not supply valid condom use data. Among

Table 1 HIV prevalence in arrested Seattle-area IDU, 1998–2002

Overall Lacking valid results

Number of HIV positive

Number of participants

44

1748 17

Total

Percentage of HIV seropositive

p value

2.5

1765

Race White Black Hispanic Native American Other

31 3 6 1 3

1125 265 128 100 126

2.8 1.1 4.7 1.0 2.4

0.22

Sex Male Female

37 7

1341 407

2.8 1.7

0.24

Male-to-male sex (men) Never male-to-male sex Ever male-to-male sex, not recent Recent male-to-male sex

19 1 16

1155 84 88

1.6 1.2 18.2

<0.001

History of sex work Males Never Ever

22 12

1138 191

1.9 6.3

<0.001

1 6

189 215

0.5 2.8

0.08

Females Never Ever

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47%) (Table 2b), followed by amphetamines (33%). Many participants reported injecting multiple drugs. Younger participants were more likely to report condom use than older participants among recruits from both the Seattle and Kent jails, although the difference was significant only among the latter (Table 2a). While similar proportions of the youngest participants reported condom use at both sites, in Kent the oldest participants were substantially less likely to report condom use. Although Hispanics, and to a lesser extent Blacks, reported more condom use than did White participants, in multivariate analysis race was not significantly associated with condom use, largely as a result of controlling for number of sex partners and, to a lesser degree, age. Though women were more likely to report using condoms than men, no evidence of an independent association with gender remained after controlling for number of sex partners. Education, site of incarceration (Seattle or Kent) and venue of recruitment (jail intake or clinic) were not associated with condom use. Associations of condom use with sexual and drug-related characteristics Fig. 1. Any condom use (and 95% confidence intervals) during anal or vaginal sex during the previous 6 months among 1417 sexually active arrested Seattle-area IDU, 1998–2002.

the 1417 sexually active participants, 185 (13%) reported always using condoms during the previous 6 months, 310 (22%) sometimes and 922 (65%) never. Time trends Among the 1417 sexually active participants, there was a sustained increase over time in the proportion reporting any use of condoms (Fig. 1), from 14% in 1998 to 44% in 2002 (ptrend < 0.001). The slope of the trend was continuous through 2001, when the data collection instrument changed. The increase in reported condom use over time was observed in both men and women, in participants who did and did not report a history of sex work, in men who did and did not report recent sex with another man, in participants recruited in the Seattle and in the Kent jails and in those recruited at jail intake and from the jail clinics (ptrend ≤ 0.006 for all groups). Associations of condom use with sociodemographic characteristics Associations with any use of condoms in anal or vaginal sex in the preceding 6 months were evaluated among the 717 sexually active participants who completed the new questionnaire in 2001 and 2002. Of these participants, 67% were white, 77% were male, the median age was 35 years and approximately 33% had some education beyond secondary school (Table 2a). Thirty eight percent were enrolled from the Kent jail and 52% were recruited at jail intake. Heroin was the most commonly reported primary injection drug (by

For both men and women, the likelihood of condom use rose sharply as a function of the number of sex partners (Table 2b). The increase in condom use as a function of partner number was significantly steeper for women than for men (pinteraction < 0.001). Of the 91 men (14% of male participants) who reported having ever had anal sex with another man, 39 (7% of male participants) reported doing so in the previous 6 months. These men were more than twice as likely as other men to report condom use. Almost half (19/39 = 49%) of men reporting recent male-to-male anal sex also reported female sex partners in the previous 6 months. The likelihood of condom use in male-to-male anal sex among men reporting such sex (24/39 = 62%) was somewhat higher than the likelihood their of condom use during sex with women (10/19 = 53%) and substantially higher than for other men in heterosexual vaginal or anal sex (37%). More than half of the women and just under one-quarter of the men reported a history of sex work. Women reporting a history of sex work were more likely to report condom use than other women. However, in logistic regression models, in particular after control for the number of sexual partners, we found no evidence of an independent association between a history of sex work and condom use in either men or women. Participants reporting amphetamines as their most frequently injected drug were less likely to report condom use than were heroin users. Only 10% of the male amphetamine injectors reported recent male-to-male sex. Crack use was not associated with condom use. Neither was reporting a needle exchange as the primary source of new needles. Condom use was associated with not having injected with a needle used by someone else during the previous 6 months.

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Table 2a Associations of any condom use in anal or vaginal sex in the previous 6 months by arrested, sexually active Seattle-area IDU, 2001–2002: sociodemographic variables Population distribution

Univariate analyses

N

Percentage of any condom use

%

Logistic regression modelsa p-value

Odds ratio

95% confidence interval

p-value

Overall

717

Age Seattle jail ≤20 21–30 31–40 >40

19 116 171 141

4 26 38 32

58 44 44 38

0.14

Kent jail ≤20 21–30 31–40 >40

12 90 122 46

4 33 45 17

58 61 34 17

<0.001

Race White Black Hispanic Native American Other

478 91 70 43 33

67 13 10 6 5

40 47 59 40 42

0.04

0.27

Sex Male Female

550 167

77 23

39 55

<0.001

0.55

Education High school grad.

180 304 233

25 42 33

47 41 40

0.30

0.81

Site of incarceration Seattle Kent

447 270

62 38

43 42

0.30

0.46

Recruitment venue Jail intake Jail clinic

370 347

52 48

41 44

0.46

0.26

a

42

1.00 0.49 0.44 0.44

0.16–1.49 0.15–1.33 0.14–1.36

0.22

1.00 1.19 0.27 0.09

0.31–4.62 0.07–1.02 0.02–0.40

<0.001

Logistic regression models are controlled for year, age, number of sex partners in males and females and primary injection drug.

Participants who reported having tested positive for HIV previous to study recruitment were more likely than others to report condom use (50% versus 35%) but there were only 18 such participants who were sexually active and the finding was not statistically significant (p = 0.20).

sponsored source, although information on HIV testing location was not available.

Exposure of participants to sources of public health advice

Our finding that more than half the HIV-positive participants reported either a history of sex work or of recent male-to-male sex demonstrates that sexual risk factors are associated with HIV prevalence in arrested Seattle-area IDU. This result is consistent with reports of a significant association of sexual risk factors with HIV incidence among IDU in San Francisco (Kral et al., 2001), Baltimore (Strathdee et al., 2001), as well as earlier data from Seattle (Harris, Thiede, McGough, & Gordon, 1993). This reinforces the importance of sexual transmission in contemporary HIV infection among IDU in the U.S. and demonstrates the impor-

We were interested in evaluating the potential exposure of participants to public health prevention efforts. Fiftyseven percent of participants reported having used a needle exchange. Forty-six percent reported having been advised to be vaccinated for hepatitis A or B, or had been tested for hepatitis C by a local health department, an STD clinic or jail. Eighty-eight percent reported having been previously tested for HIV, which is likely to have been through a public health

Discussion

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Table 2b Associations of any condom use in anal or vaginal sex in the previous 6 months by arrested, sexually active Seattle-area IDU, 2001–2002: sexual and drug-related variables

Overall

Population distribution

Univariate analyses

N

Percentage of any condom use

%

717

Number of sex partners, 6 months Males 1 241 2 101 3–4 95 5+ 112

Logistic regression modelsa p-value

Odds ratio

95% confidence interval

1.00 3.13 4.77 9.21

1.82–5.40 2.73–8.34 5.32–15.9

1.00 2.19 11.31 171.3

0.78–6.16 4.05–31.6 21.4–1372

p-value

42

44 18 17 20

19 43 58 67

<0.001

<0.001

Females 1 2 3–4 5+

69 24 31 43

41 14 19 26

23 42 74 98

<0.001

Male sex work Never Ever

419 131

76 24

37 44

0.29

0.31

Female sex work Never Ever

66 101

40 61

42 62

0.01

0.55

Male-to-male anal sex, 6 months No 510 Yes 39

93 7

37 59

0.01

Primary injection drug Heroin Speedballs Cocaine Amphetamines

47 8 11 33

41 48 58 38

0.01

64 36

38 49

0.004

0.88

Needle exchange primary source of needles No 344 51 Yes 330 49

46 40

0.14

0.89

Injection with a used needle, 6 months Any 452 67 None 221 33

40 48

0.05

337 56 81 237

Crack primary non-injection drug No 456 Yes 261

a

<0.001

1.00 2.24

1.05–4.78

1.00 1.59 1.82 0.52

0.79–3.18 1.00–3.29 0.32–0.84

1.00 1.78

0.04

<0.001

0.003 1.22–2.61

Logistic regression models are controlled for year, age, number of sex partners in males and females and primary injection drug.

tance of promoting condom use for HIV prevention among IDU. The decidedly modest levels of condom use we observed are consistent with the low levels that have been reported in other IDU populations in the United States and other countries (Metzger et al., 1993; Rhodes, Donoghoe, Hunter, Soteri, & Stimson, 1994; Tyndall et al., 2002; Watkins, Metzger, Woody, & McLellan, 1993). There clearly remains a continuing need for efforts to increase condom use among IDU. Nonetheless, we noted a sustained and statistically significant increase in the proportion of IDU reporting any use of condoms over the 5-year study period. In contrast, rather constant levels of condom use have been found in the general U.S. population between 1996 and 2000 (Anderson, 2003).

While condom use by IDU in some other U.S. locations has been observed to increase over time (Longshore, Annon, & Anglin, 1998; Watters, 1994), such changes are by no means universal among U.S. IDU (Battjes, Pickens, & Brown, 1995; Semaan et al., 1998). Comparisons of the likelihood of condom use among different subgroups of our study population revealed informative differences. We found a striking association between likelihood of condom use and number of sex partners. In our data men reporting recent male-to-male anal sex were more likely to report condom use, even after control for partner number. Because multiple sex partners and male-to-male anal sex are prime risk factors for HIV transmission, these data suggest that study participants had evaluated their risk

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for HIV infection and practiced preventive measures accordingly. Our findings that younger participants, at least those recruited at the Kent jail, were more likely to report use of condoms are consistent with data from national surveys in the U.S. (Centers for Disease Control and Prevention, 1998; Piccinino & Mosher, 1998; Sonenstein, Ku, Lindberg, Turner, & Pleck, 1998; Sonenstein, Pleck, & Ku, 1989). Condom use among younger IDU is of particular importance because young age has been consistently associated with increased risk for HIV seroconversion among IDU in the United States and other countries (Fennema, Van Ameijden, Van Den, & Coutinho, 1997; Nicolosi, Leite, Musicco, Molinari, & Lazzarin, 1992; Solomon et al., 1993; Strathdee et al., 2001). Participants reporting amphetamines as their primary injection drug were less likely than others to report condom use. Data from California, have also found that amphetamine users report less condom use than users of other drugs (Molitor et al., 1999). As 90% of amphetamine injectors in our study reported no male-to-male sex, this finding is not driven by the distinctive patterns of amphetamine use and risky sexual behaviour that have been reported among men reporting male-to-male sex (Colfax et al., 2005; Harris et al., 1993; Molitor et al., 1999). Amphetamine injectors thus represent a population with a potentially increased risk of sexual HIV transmission, which should be targeted by public health prevention programs. No association with condom use was found for a number of other variables: race, educational level, site (and thus community) of incarceration, recruitment from the jail clinic or from intake, needle-exchange use or crack consumption. This suggests that the patterns we observed were not narrowly confined to specific subgroups but rather were broadly applicable throughout the study population. A number of limitations should be considered. Although our study population of 1765 represents 12% of the roughly 15,000 IDU estimated to reside in the Seattle area (Friedman et al., 2004), it is difficult to evaluate the degree to which our results can be generalized to the Seattle-area IDU population due to potential recruitment biases created by the inherently clandestine nature of illegal drug use, local arrest patterns, and the unstable and marginal social circumstances of many IDU. Incarceration, nonetheless, is likely to be a common experience for IDU. An earlier Seattle IDU study found high rates of incarceration; 90% had been in jail and 29% had been in jail during the previous month (O’Driscoll et al., 2001). Data inaccuracies associated with the inherent potential for bias in self-report should also be taken into account. It has been asserted that IDU are more likely to change drug use behaviours than sexual behaviour and, while this may well be true, there also exist data that sexual risk behaviour among IDU is not entirely intractable to modification. Significant reductions in unsafe sex with primary and casual partners between 1991 and 1997 have been reported from serial cross-sectional studies of IDU in New York (Des Jarlais et al., 2000). IDU in Amsterdam reported a substan-

tial decline in sexual risk behaviour (Van Ameijden, van den Hoek, & Coutinho, 1996), mediated through changes in partner selection and number of sexual encounters, as well as increased condom use. Sexual risk behaviours in a cohort of Chicago IDU declined over a 4-year time span (Wiebel et al., 1996). The proportion of participants reporting five or more partners declined over a 5-year period in a cohort of San Francisco IDU (Moss et al., 1994). Trends toward increased condom use over time among some populations of IDU have been noted (Longshore et al., 1998; Watters, 1994). While we cannot establish a specific correlation between any public health program and the patterns of condom use in our study population, there is evidence that a substantial proportion of participants had contact with a public health program in which condom use could have been or, in the future could be, promoted. Our data demonstrate a measurable level of risk reduction in the sexual behaviour of IDU, as shown by the increase in likelihood of condom use over time and by the findings that IDU at highest risk of sexual transmission of HIV, those with multiple sex partners, men reporting male-to-male sex and the young, were more likely to report condom use. These data suggest that the promotion of condom use among IDU is feasible and that doing so may play a material role in HIV prevention in this population. Acknowledgements This study was funded by a cooperative agreement with the Centers for Disease Control and Prevention (U62/CCU006260). We thank Jim Harms and the other staff at the King County Department of Adult and Juvenile Detention and the Jail Health Services Program, Linda Oakley, Michael Romero and the other Kiwi Study Staff, the Public Health Laboratory, and the Kiwi Study participants for their contributions to this study. We also thank P. Lynne Stockton, VMS, MS for editorial assistance and Bob Wood, MD; Gary Goldbaum, MD, MPH; and Kathleen Gallagher, DSc, MPH, for critically reading the manuscript. References Anderson, J. E. (2003). Condom use and HIV risk among US adults. American Journal of Public Health, 93, 912–914. Asiimwe-Okiror, G., Opio, A. A., Musinguzi, J., Madraa, E., Tembo, G., & Carael, M. (1997). Change in sexual behaviour and decline in HIV infection among young pregnant women in urban Uganda. AIDS, 11, 1757–1763. Battjes, R. J., Pickens, R. W., & Brown, L. S., Jr. (1995). HIV infection and AIDS risk behaviors among injecting drug users entering methadone treatment: An update. Journal of Acquired Immune Deficiency Syndromes and Human Retrovirology, 10, 90–96. Centers for Disease Control and Prevention. (1998). Trends in sexual risk behaviors among high school students—United States, 1991–1997. Morbidity and Mortality Weekly Report, 47, 749–752. Centers for Disease Control and Prevention. (2001). HIV prevention strategic plan through 2005. Atlanta, GA: Centers for Disease Control and Prevention.

R.D. Burt et al. / International Journal of Drug Policy 17 (2006) 222–229 Centers for Disease Control and Prevention. (2005). HIV/AIDS surveillance report, 2004 (Vol. 16, Rep. No. 15). Atlanta, GA: U.S. Department of Health and Human Services. Colfax, G., Coates, T. J., Husnik, M. J., Huang, Y., Buchbinder, S., Koblin, B., et al. (2005). Longitudinal patterns of methamphetamine, popper (amyl nitrite), and cocaine use and high-risk sexual behavior among a cohort of San Francisco men who have sex with men. Journal of Urban Health, 82, i62–i70. Davis, K. R., & Weller, S. C. (1999). The effectiveness of condoms in reducing heterosexual transmission of HIV. Family Planning Perspectives, 31, 272–279. Des Jarlais, D. C., Perlis, T., Friedman, S. R., Chapman, T., Kwok, J., Rockwell, R., et al. (2000). Behavioral risk reduction in a declining HIV epidemic: Injection drug users in New York City, 1990–1997. American Journal of Public Health, 90, 1112–1116. Fennema, J. S., Van Ameijden, E. J., Van Den, H. A., & Coutinho, R. A. (1997). Young and recent-onset injecting drug users are at higher risk for HIV. Addiction, 92, 1457–1465. Friedman, S. R., Tempalski, B., Cooper, H., Perlis, T., Keem, M., Friedman, R., et al. (2004). Estimating numbers of injecting drug users in metropolitan areas for structural analyses of community vulnerability and for assessing relative degrees of service provision for injecting drug users. Journal of Urban Health, 81, 377–400. Gregson, S., Garnett, G. P., Nyamukapa, C. A., Hallett, T. B., Lewis, J. J., Mason, P. R., et al. (2006). HIV decline associated with behavior change in eastern Zimbabwe. Science, 311, 664–666. Harris, N. V., Thiede, H., McGough, J. P., & Gordon, D. (1993). Risk factors for HIV infection among injection drug users: Results of blinded surveys in drug treatment centers, King County, Washington, 1988–1991. Journal of Acquired Immune Deficiency Syndromes, 6, 1275–1282. Kral, A. H., Bluthenthal, R. N., Lorvick, J., Gee, L., Bacchetti, P., & Edlin, B. R. (2001). Sexual transmission of HIV-1 among injection drug users in San Francisco, USA: Risk-factor analysis. Lancet, 357, 1397–1401. Longshore, D., Annon, J., & Anglin, M. D. (1998). Long-term trends in self-reported HIV risk behavior: Injection drug users in Los Angeles, 1987 through 1995. Journal of Acquired Immune Deficiency Syndromes and Human Retrovirology, 18, 64–72. Metzger, D. S., Woody, G. E., McLellan, A. T., O’Brien, C. P., Druley, P., Navaline, H., et al. (1993). Human immunodeficiency virus seroconversion among intravenous drug users in- and out-of-treatment: An 18-month prospective follow-up. Journal of Acquired Immune Deficiency Syndromes, 6, 1049–1056. Molitor, F., Ruiz, J. D., Flynn, N., Mikanda, J. N., Sun, R. K., & Anderson, R. (1999). Methamphetamine use and sexual and injection risk behaviors among out-of-treatment injection drug users. American Journal of Drug Alcohol Abuse, 25, 475–493. Moss, A. R., Vranizan, K., Gorter, R., Bacchetti, P., Watters, J., & Osmond, D. (1994). HIV seroconversion in intravenous drug users in San Francisco, 1985–1990. AIDS, 8, 223–231. National Institute of Allergy and Infectious Diseases. (2000). Workshot summary: Scientific evidence on condom effectiveness for sexually transmitted disease (STD) prevention. Herndon, VA: National Institutes of Health, Department of Health and Human Services. Nelson, K. E., Celentano, D. D., Eiumtrakol, S., Hoover, D. R., Beyrer, C., Suprasert, S., et al. (1996). Changes in sexual behavior and a decline in HIV infection among young men in Thailand. New England Journal of Medicine, 335, 297–303. Nicolosi, A., Leite, M. L., Musicco, M., Molinari, S., & Lazzarin, A. (1992). Parenteral and sexual transmission of human immunodeficiency virus in intravenous drug users: A study of seroconversion. The

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Northern Italian Seronegative Drug Addicts (NISDA) Study. American Journal of Epidemiology, 135, 225–233. O’Driscoll, P. T., McGough, J., Hagan, H., Thiede, H., Critchlow, C., & Alexander, E. R. (2001). Predictors of accidental fatal drug overdose among a cohort of injection drug users. American Journal of Public Health, 91, 984–987. Piccinino, L. J., & Mosher, W. D. (1998). Trends in contraceptive use in the United States: 1982–1995. Family Planning Perspectives, 30, 4–10, 46. Pinkerton, S. D., & Abramson, P. R. (1997). Effectiveness of condoms in preventing HIV transmission. Social Science & Medicine, 44, 1303–1312. Rhodes, T., Donoghoe, M., Hunter, G., Soteri, A., & Stimson, G. V. (1994). Sexual behaviour of drug injectors in London: Implications for HIV transmission and HIV prevention. Addiction, 89, 1085– 1096. Semaan, S., Kotranski, L., Collier, K., Lauby, J., Halbert, J., & Feighan, K. (1998). Temporal trends in HIV risk behaviors of out-of-treatment injection drug users and injection drug users who smoke crack. Journal of Acquired Immune Deficiency Syndromes and Human Retrovirology, 19, 274–281. Solomon, L., Astemborski, J., Warren, D., Munoz, A., Cohn, S., Vlahov, D., et al. (1993). Differences in risk factors for human immunodeficiency virus type 1 seroconversion among male and female intravenous drug users. American Journal of Epidemiology, 137, 892–898. Sonenstein, F. L., Ku, L., Lindberg, L. D., Turner, C. F., & Pleck, J. H. (1998). Changes in sexual behavior and condom use among teenaged males: 1988 to 1995. American Journal of Public Health, 88, 956–959. Sonenstein, F. L., Pleck, J. H., & Ku, L. C. (1989). Sexual activity, condom use and AIDS awareness among adolescent males. Family Planning Perspectives, 21, 152–158. Strathdee, S. A., Galai, N., Safaiean, M., Celentano, D. D., Vlahov, D., Johnson, L., et al. (2001). Sex differences in risk factors for HIV seroconversion among injection drug users: A 10-year perspective. Archives of Internal Medicine, 161, 1281–1288. Thiede, H., Romero, M., Bordelon, K., Hagan, H., & Murrill, C. S. (2001). Using a jail-based survey to monitor HIV and risk behaviors among Seattle area injection drug users. Journal of Urban Health, 78, 264–278. Tyndall, M. W., Patrick, D., Spittal, P., Li, K., O’Shaughnessy, M. V., & Schechter, M. T. (2002). Risky sexual behaviours among injection drugs users with high HIV prevalence: Implications for STD control. Sexually Transmitted Infections, 78(Suppl. 1), i170–i175. Van Ameijden, E. J., van den Hoek, J. A., & Coutinho, R. A. (1996). Large declines in sexual risk behavior with noncommercial partners among heterosexual injection drug users in Amsterdam, 1989–1995. American Journal of Epidemiology, 144, 772–781. Watkins, K. E., Metzger, D., Woody, G., & McLellan, A. T. (1993). Determinants of condom use among intravenous drug users. AIDS, 7, 719–723. Watters, J. K. (1994). Trends in risk behavior and HIV seroprevalence in heterosexual injection drug users in San Francisco, 1986–1992. Journal of Acquired Immune Deficiency Syndromes, 7, 1276–1281. Weller, S. C., & Davis, K. R. (2005). Condom effectiveness in reducing heterosexual HIV transmission (Review). The Cochrane Library, (2) (Chichester, UK: John Wiley & Sons). Wiebel, W. W., Jimenez, A., Johnson, W., Ouellet, L., Jovanovic, B., Lampinen, T., et al. (1996). Risk behavior and HIV seroincidence among out-of-treatment injection drug users: A 4-year prospective study. Journal of Acquired Immune Deficiency Syndromes and Human Retrovirology, 12, 282–289.