Eur. J. Epidemiol. 0392-2990
EUROPEAN JOURNAL
September 1992, p. 723-729
Vol. 8, No. 5
OF EPIDEMIOLOGY
CONDOM USE AND SEXUAL HABITS OF HETEROSEXUAL INTRAVENOUS DRUG USERS IN NORTHERN ITALY D. SERRA1NO .1, S. FRANCESCHI*, E. VACCHER**, S. DIODATO***, D. ERRANTE**, I. CROSATO**, S. GUARNERI* and U. TIRELLI** *Epidemiology Unit and **AIDS Unit - Aviano Cancer Centre - 33081 Aviano (PN) - Italy. ***Public Drug Assistance Centre - USL 11 "Pordenonese"- Ospedale Civile 33170 Pordenone - Italy.
Key words: HIV - Intravenous drug use - Condom use - Heterosexual behaviour In order to assess modes of human immunodeficiency virus (H/V) transmission from heterosexual intravenous drug users (IVDUs) to their partners, condom use and sexual habits with both steady and occasional partners were investigated. A total of 349 heterosexual 1VDUs (247 men and 102 women) who ignored, at the time of interview, their H1V serostatus were interviewed. Respondents were asked for information on condom use and sexual habits for the three year period prior to the interview. Nearly 40% of IVDUs reported sexual intercourse with both steady partners and occasional partners. Fifty-four percent of their steady partners and 48% of their occasional partners were individuals who did not belong to groups at risk for HIV infection. Anal intercourse with steady partners was reported by 29% of 1VDUs and 24% of IVDUs with occasional partners. Condom use during vaginal intercourse was seldom reported: 83% of IVDUs never used a condom with steady partners and 75% did not use one with occasional partners. 1VDUs who were 1) unmarried, 2) enrolled in the study after 1986, 3) partners of not at-risk individuals, 4) partners of a foreigner and, 5) aware of their partners H1V seropositivity showed significantly higher, albeit still low, frequencies of condom use with steady partners. Conversely, all these factors seemed to have little impact on condom use with occasional partners. Condom use and sexual habits were similarly reported by H1V-positive and H/V-negative IVDUs. The present study shows that high-risk sexual behaviours among IVDUs are very widespread and it stresses the need for intensive counselling to promote condom use among IVDUs.
INTRODUCTION
The proportion of AIDS patients who acquired human immunodeficiency virus (HIV or HIV-1) infection by means of heterosexual transmission is rapidly increasing in Italy. The number of M D S cases among persons whose only risk factor for HIV infection was one or more sexual contacts with HIVinfected persons rose from 71 in 1987 (4.2% of all AIDS cases) to 514 in 1990 (6.4% of the cases) (8). Intravenous drug users (IVDUs) are the population 1 Corresponding author.
723
group at highest risk for HIV infection and AIDS, nearly 70% of the Italian AIDS cases occurred among them (8), and they also constitute the most important reservoir for HIV heterosexual transmission to the general population. Indeed, among heterosexuals with AIDS whose partner's risk group was known, 84% of women and 58% of men were partners of HIVinfected 1VDUs (8). Notwithstanding the importance of H1V sexual spread from IVDUs to their heterosexual, non-drugusing partners, there is little epidemiologic information on the prevalence of high-risk sexual behaviours of IVDUs and their partners (18, 20). Some studies have
Serraino D. et aL
Eur. J. Epidemiol.
suggested that condoms are seldom used by IVDUs (10, 11), while others have focused on the importance of prostitution among IVDUs as a source of HIV heterosexual spread (4, 17). In order to assess potential modes of HIV transmission from IVDUs to their sexual partners, we have investigated condom use and sexual habits of heterosexual IVDUs, exploring their behaviour with steady and/or occasional partners.
TABLE 1. - Distribution of 349 IVDUs, according to gender and other characteristics. Northeast Italy, 19841988. SEX Characteristics
Men (n = 247)
Women (n = 102)
No. (%)
No. (%)
100 (41) 67 (27) 80 (32)
48 (47) 30 (29) 24 (24)
Age (years):
< = 23 24-26 > = 27
MATERIALS AND METHODS
The present study is part of a larger crosssectional study on prevalence and determinants of HIV infection in IVDUs that began in 1984 in the Friuli-Venezia Giulia region, northeast Italy. Methods and results concerning the association between druguse habits and the risk of HIV infection have been previously described (16). Briefly, all IVDUs presenting for heroin abuse treatment to eight public drug assistance centres and who agreed to be tested for HIV antibodies were enrolled in the study. Before knowing the result of the blood test, each subject was asked for informed consent and then interviewed by the physician in charge of the drug assistance centre. Efforts were undertaken to train the physicians in order to standardize data collection procedures. Information was elicited, using a standard questionnaire, on socio-demographic factors, history of drug use and sexual behaviour for the three year period prior to the interview. The relative frequency of condom use during vaginal, oral and anal intercourse was estimated by means of a four-point scale: 1) never (0%); 2) sometimes (1-500/0); 3) often (51-990/0) and 4) always (1000/0). A partner was defined as steady if the sexual relationship had lasted for at least six months. Occasional partners were all other sexual partners. All HIV antibody tests were performed in a single laboratory. A subject was considered HIV-positive if a repeatedly positive ELISA test was confn-med by Western blot. Chi-square was used to assess statistical significance of differences between proportions, while, for ordered categorical variables with three or more levels, the Chi-square test for linear trend was computed (12). Odds ratios (ORs) and their 950/0 confidence intervals (CIs) were computed to estimate the association between condom use and several characteristics of IVDUs. Unconditional, multiple logistic regression (MLR) equations were fitted (2), allowing for age, sex and marital status. Betweeen March 1984 and December 1988, a total of 434 male and 147 female IVDUs were enrolled in the study. In the three years prior to the interview, 405 men (93%) and 134 women (920/0) reported heterosexual activity. The study group for this investigation consists of the 349 persons (247 men and 102 women) for whom information on condom use and sexual habits was available. They represent 61%
X~ for trend
2.45; p = 0.12
Marital statusa:
Single Married
x~
201 (82) 45 (18)
67 (67) 33 (33)
7.99; p < 0.01
HIV antibody: Negative Positive
137 (55) 110 (45)
69 (68) 33 (32)
4.43; p = 0.04 Type o f sexual partner:
Steady partners only Occasional partners only Both steady and occasional partners
98 (40) 50 (20)
58 (57) 7 (7)
99 (40)
37 (36)
12.95; p < 0.01 Condom use with steadJ" b partners:
724
Never Sometimes/often Always
X~ for trend
156 (80) 29 (15)
85 (90) 8 (8)
10 (5)
2 (2)
3.99; p = 0.05
Condom use with a' c occasional partners:
Never Sometimes/often Always X~ for trend
104 (76) 17 (12) 16 (12)
27 (73) 6 (16) 4 (11)
O.O3; p = 0.86
a: The sum does not add up to the total because of missing values; b: 57 IVDUs who reported occasional partners only were excluded; c: 156 IVDUs who reported steady partners only were excluded.
Vol. 8, 1992
Sexual habits of intravenous drug users
of the male and 76% of the female 1VDUs who reported heterosexual activity during the three-year period prior to interview and were attending five of the eight drug treatment centres in the study.
Condom use during vaginal intercourse was seldom reported. Twenty percent of male and 10% of female IVDUs (p < 0.05) stated ever using a condom with steady partners and 24% of men and 27% of women reported condom use with occasional partners (Table 1). Moreover, there were few IVDUs who reported having always used condoms, 4% with steady partner and 12% with occasional partners (Table 1). Oral intercourse was reported by approximately 75% of IVDUs, and there were no significant differences between frequency of oral sex with steady partners and occasional partners or between men and women (Fig. 1). The frequency of anal intercourse was similarly reported by male IVDUs with steady (280/0) or occasional (270/0) partners, whereas women seemed more likely to have anal intercourse with their steady partner than with occasional partners (30% and 14%, respectively, p = 0.06) (Fig. 1). There was no significant difference in the frequency of condom use and other sexual habits
RESULTS
Female 1VDUs in the present study were slightly younger (median age was 24 years for women and 25 for men), more likely to be married (p < 0.01) and less often infected with HIV (32% vs 45% seropositive, p = 0.04) than male 1VDUs (Table 1). In the three years prior to the interview, women appear to have had a higher mean number of sexual partners than men (19.7 and 13.3, respectively, p = 0.06). Eighty percent of male IVDU and 93% of female IVDU reported having had a steady partner, but nearly 40% of IVDUs of both sexes had had sexual intercourse with both steady and occasional partners (Table 1). percent
percent
1
100 C:t:~H v n~r+n~r
80
60
40
20
Oral s e x
Anal sex
Condom use
percent
100
Anal sex
Orltl eex
lefcent
loo 7
/
Occasional p~r)ner
•
80
ao"
60
80
40
40-
0cga_.~ion~dpartner
20"
0
-
Oral =ex
l
Men
~
L/
0
Amd eex Women
m
Figure 1. - Frequency of oral and anal intercourse, with steady and occasional partners, according to gender of interviewee.
~ft4g e e x
Oral sex
Condom u s e
HIV-pos ~
HIV-neg
Figure 2. - Frequency of condom use, oral and anal intercourse, with steady and occasional partners, according to HIV serostatus.
725
Serraino D. et al.
Eur. J. Epidemiol.
TABLE 2. - Condom use during vaginal intercourse, according to type of partner and other characteristics. Northeast Italy, 1984-1988. Steady partners (n = 290) a Condom use (No.) % MLR-OR c (95% CI)
(No.)
(84) (84) (122)
14 18 18
(56) (45) (73)
(72) (215)
6 21
(117) (56) (117)
13 13 23
1 1.0 (0.42.0 (1.03.83; p = 0.05
(129) (98) (56)
18 17 14
1 0.9 (0.40.6 (0.20.78; p = 0.38
Use of cocained: No Yes
(123) (157)
18 15
Prostitution.~ No Yes
(269) (19)
HIV-antibody : Negative Positive
Characteristics
Age (years): > = 27 24-26 < = 23 X~ for trend Marital statusd : Married Single
1 1.2 (0.51.1 (0.50.39; p = 0.53
2.8) 2.5)
20 29 26
1 1.8 (0.7- 4.7) 1.5 (0.6- 3.6) 0.69; p = 0.41
(27) (144)
19 25
1 1.5 (0.5- 4.4)
2.6) 4.1)
(56) (35) (83)
23 17 28
1 0.7 (0.2- 2.2) 1.3 (0.6- 3.0) 0.61; p = 0.43
1.8) 1.7)
(73) (60) (38)
22 23 26
1 1.2 (0.5- 2.8) 1.8 (0.6- 5.4) 1.03; p = 0.31
1 0.8 (0.4-
1.5)
(59) (114)
20 25
1 1.2 (0.6- 2.7)
17 16
1 1.1 (0.3-
4.2)
(158) (16)
22 50
1 4.3 (1.2-14.8)
(175) (115)
17 17
1 0.9 (0.5-
1.7)
(88) (86)
20 28
1 1.4 (0.7- 2.9)
Partner from a high-risk group: Yes No
(140) (150)
10 23
1 2.3 (1.1-
4.8)
(84) (90)
24 24
1 1.0 (0.5- 2.1)
Partners' nationaOty : Italian Foreigner
(284) (6)
15 83
1 22.1 (2.5-198.7)
(160) (14)
24 21
1 0.8 (0.2- 3.1)
Awareness of partners" HIV seropositivity: No Yes
(259) (31)
15 32
(169) (5)
24 40
1 2.2 (0.3-14.6)
Year of interview: = 1987 ~ f o r trend Duration of heroin d addiction (years): =8 for trend
1 4.0 (1.4- 11.9)
Occasional partners (n = 174)b Condom use % MLR-OR° (95% CI)
1 2.8 (1.2-
6.8)
2 IVDUs who reported information on condom use with occasional partners but not with steady partners were excluded; b: 19 IVDUs who reported information on condom use with steady partners but not with occasional partners were excluded; c: Multiple logistic regression odds ratio (MLR-OR), and 95°/0confidence interval (CI), adjusted for sex, age and marital status; d: The sum does not add up to the total because of missing values. a:
726
Vol. 8, 1992
Sexual habits of intravenous drug users
condom with their occasional partners (OR = 4.3, 95% CI: 1.2-14.8), as compared with IVDUs who did not report prostitution. Conversely, the frequency of condom use with steady partners was comparable in IVDU prostitutes and in the rest of IVDUs. Having a partner not otherwise at risk for HIV infection (OR = 2.3), or a foreign partner (OR = 22.1), or being aware of the partner's HIV seropositivity (OR = 2.8) were all factors significantly associated with an increased, albeit still low, frequency of condom use with the steady partner. These characteristics did not seem to affect, however, condom use with occasional partners, although very few IVDUs (2 men and 3 women) were aware of the seropositive status of their occasional partners (Table 2).
percent 1O0 Steady partner 80
60
40
20
"
-
~
......
(----~Z-7 IVDU
HIV-po=ltlve
7
Foreigner
DISCUSSION
~rc~t • 100" Occasional partner 80604020-
J
.
l
IVDU
HIV-poeltlve
Foce4oner
Partner's characteristics I
Men
~
Women
Figure 3. - Characteristics of steady and occasional partners, according to gender of interviewee.
between HIV-positive and HIV-negative 1VDUs (Fig. 2). None of the IVDUs in the present investigation reported sexual intercourse with at-risk individuals apart from 1VDUs, and more IVDU women than men were the steady partner of an IVDU (69% vs 39%; p < 0.01). Female IVDUs were also more frequently aware of the seropositivity of their steady partner (p < 0.01) or occasional partners (p = 0.05) than male IVDU (Fig. 3). The associations between several factors and condom use with steady partners and with occasional partners are shown in table 2. Unmarried IVDUs showed a four-fold higher frequency of condom use with their steady partner than married IVDUs (OR = 4.0, 95% CI: 1.4-11.9). A significant trend of increase in the frequency of condom use with the steady partner by year of enrollement in the study emerged (p = 0.05), whereas no change across the study period was seen regarding the use of condoms with occasional partners (Table 2). IVDUs who reported episodes of prostitution (10 men and 16 women) were more likely to use a
Transmission of HIV among IVDUs occurs primarily through needle and syringe sharing and, to a lesser extent, by sexual intercourse (5-7, 14). Sexual intercourse plays, however, a very important role in HIV spread from IVDUs to the general population. Data concerning the sexual behaviour of IVDUs are, therefore, important in order to assess modes of HIV spread and to design effective AIDS education and prevention programmes. The present investigation focused on condom use and sexual habits of 1VDUs, and the study supports previous research indicating that IVDUs constitute an important source of H1V heterosexual spread (9, 10, 19). Among the findings of the study, the high proportion of partners who were not otherwise at risk for HIV infection and the very low frequency of condom use are of particular concern. As seen in IVDUs in Amsterdam (19), nearly 40% of IVDU men and women in the present study reported sexual intercourse with both steady and occasional partners, and approximately half of their partners did not belong to groups at risk for HIV infection. From these data, male IVDUs appear to play a more important role than female IVDUs in the heterosexual transmission of HW, since 65% of their steady partners were non-drug-using women and condoms were used infrequently. This finding is in agreement with the epidemiology of AIDS among heterosexuals in Italy, where non-drug-using women who were partners of male IVDUs represented the largest group with AIDS (8). The low prevalence of condom use among heterosexual IVDUs, consistently documented by other studies (3, 9-11, 15, 19), is confirmed in the present investigation. Some differences which emerged in the frequency of condom use with steady and occasional partners are worth noting. Among IVDUs in New York City, those who lived together with their steady partner showed a lower, although not significantly different, frequency of condom use (11). Similarly, in the present study, a significantly higher frequency of condom use with steady partners emerged among unmarried IVDUs. A
727
Serraino D. et al.
Eur. J. Epidemiol.
decrease in needle-sharing among IVDUs has been shown, but an increase in condom use and the adoption of safer sex practices over time has never been reported in IVDUs (1, 7, 13). While an almost two-fold increase of IVDUs who reported condom use with their steady partners after 1986 may be encouraging, it is worth noting that no consistent increase in condom use with occasional partners was seen during the study period. Previous research has documented a positive association between one's knowledge of partner's HIV seropositivity and condom use (11, 18). In the present study, the frequency of condom use was somewhat higher among IVDUs who knew the HIV seropositive status of their partner. However, two thirds of IVDUs did not use condoms despite such knowledge and very few IVDUs were aware of a partner's HIV seropositivity, particularly with regards to occasional partners. Prostitution and anal intercourse have been shown to be important modes of HIV heterosexual transmission (6, 10, 16, 17). In the present study a higher frequency of condom use with occasional partners, but not with steady partners, emerged among IVDUs who reported prostitution. This finding is in agreement with the higher frequency of condom use reported among IVDU prostitutes with their clients in Amsterdam, where over 80% reported use of condoms, as compared with their non-paying partners (19). Twenty-nine percent of IVDUs in the present study reported having ever had anal intercourse with their steady partner and 24% with their occasional partners. The prevalence of such sexual behaviour was, overall, similar to that found among IVDUs in the USA (10). Some limitations of the present study, which are common to much research on HIV infection among IVDUs, are worth noting. The lack of random selection of the population sample hampers the generalizability of the findings, since serf-referring IVDUs may not be representative of the IVDU population in the area under study. In addition, information on condom use and sexual habits was obtained only from a sub-set of self-referred IVDUs. Furthermore, misreporting on some of the factors investigated is likely to have occurred and information on other relevant aspects of sexual habits, such as number of sexual encounters and duration of sexual relationship, was not available. The study, however, is one of the largest ever conducted in this area (10, 11, 19), and it offers the opportunity to compare the frequency of condom use and sexual habits of heterosexual 1VDUs with their steady and occasional partners. Regarding the comparison of HIV-positive and HIV-negative IVDUs, it is important to bear in mind that condom use and sexual habits herein investigated concerned a period when the subjects were not yet aware of their HIV serostatus. ARhough efforts were made to exclude from the study all IVDUs who knew their HIV serostatus before the interview, it is possible
that some subjects did not report previous HIV antibody tests. Obviously, IVDUs may have changed their highrisk sexual habits after knowledge of their blood test result. Further follow-up information is essential for evaluating the impact of knowing one's HIV seropositivity on his/her sexual behaviour. In conclusion, the present study confirms that high-risk sexual behaviours among IVDUs are very widespread and that IVDUs are very reluctant to protect themselves and their partners from HIV infection through sexual intercourse. This held true even when the study participants, who did not know before the interview whether they were HIV-positive, had a steady partner known to be seropositive. Further research on sexual habits oflVDUs and their partners is needed in order to overcome barriers to condom use and to identify optimal sexual risk reduction strategies. Acknowledgements: We would like to thank the staff of the drug assistance centres and of the AIDS Unit - Aviano Cancer Centre - for their valuable collaboration and Dr. D. Gerdol for controlling all the questionnaires. Thisworkwas supportedbya grantfromthe ItalianMinistry of Health - Istituto Superiore di Sanit~t, IV Progetto AIDS 1991, Contract No. 6202-027 and No. 6205-006 - Rome, Italy. REFERENCES 1.
Becker M.H. and Joseph J.G. (1988): AIDS and behavioral change to reduce risk: a review - Am. J. Public Health 78 (4): 394-410.
2.
Breslow N.E. and Day N.E. (1980): Statistical methods in cancer research. Lyon, IARC Scientific Publication No. 32, pp 192-246.
3.
Brown L.S. and Primm B.J. (1988): Sexual contacts of intravenous drag users: implications for the next spread of the AIDS epidemic - J. Natl. Med. Assoc. 80: 651-656.
4.
Casabona J. Sanche E. Salinas Lacasa C. and Verani P. (1990): Seroprevalence and risk factors for HIV transmission among female prostitutes: a community survey - Eur. J. Epidemiol. : 248-252.
5.
Chasson .E. Moss A. . Onishi . Osmond D. and Carlson J . . (1987): H u m a n immunodeficiency virus infection in heterosexual intravenous drug users in San Francisco - Am. J. Public Health, 77: 169-172.
6.
Coutinho .A. (1990): Epidemiology and prevention of AIDS among intravenous drug users - Journal of Acquired I m m u n e Deficiency Syndromes 3: 413-416.
7.
Des Jarlais D.C. and riedman S. . (1987): Editorial Review: H I V infection among intravenous drug users: epidemiology and risk reduction - AIDS 1: 67-76.
728
Vol. 8, 1992
.
Sexual habits of intravenous drug users
Istituto Superiore di San#it (1991): Aggiornamento dei
14. Nicolosi A., Musicco M., Saracco A., Molinari S., Ziliani N. and Lazzarin A. (1990): Incidence and risk factors of H I V infection: a prospective study of seronegative drug users from Milan and Northern Italy, 1987-1989 - Epidemiology 1: 453-459.
casi di AIDS conclamato notificati in Italia al 31 dicembre 1990. Roma. . Lewis D.K. and Watters J.K. (1991): Sexual risk behaviour among heterosexual intravenous drug users: ethnic and gender variation - AIDS 5: 77-83.
15. Ralph N. and Spigner C. (1986): Contraceptive practices among female heroin addicts - Am. J. Public Health 76:' 1016-1017.
10. Lewis D.K., Watters J.K. and Case P. (1990): The prevalence of high-risk sexual behaviour in male intravenous drug users with steady female partners Am. J. Public Health 80: 465-466.
16. Serraino D., Franceschi S., Vaccher E., et al. (1991): Risk factors for human immunodeficiency virus infection in 581 intravenous drug users, northeast Italy, 1984-1988 International Journal of Epidemiology 20: 264-270.
11. Magura S., Shapiro J.L., Siddigi Q. and Lipton D.S. (1990): Variables influencing condom use among intravenous drug users - Am. J. Public Health 80: 8284.
17. Tirelli U., Vaccher E., Sorio R., et al. (1986): HTLV-III antibodies in drug addicted prostitutes used by US soldiers in Italy (Letter) - J A M A 256: 711-712.
12. Mantel N. (1963): Chi-square test with one degree of freedom extension of the Mantel-Haenszel procedure - J. Am. Stat. Ass. 58: 690-700. 13. Nicotosi A., Molinari S., Musicco M., Saracco A., Ziliani N. and Lazzarin A. (1991): Positive modification on injecting behaviour among intravenous heroin users from Milan and Northern Italy 1987-1989 - British Journal of Addiction 86: 91102.
18. Turner C.E (1989): Research on sexual behaviours that transmit HIV: progress and problems - AIDS 3 (suppl 1): $63-$69. 19. Van Den Hock J.A.R., Van Haastrecht H.J.A. and Coutinho R.A. (1990): Heterosexual behaviour of intravenous drug users in Amsterdam: implications for the AIDS epidemic - AIDS 4: 449-453. 20. Wellings K., Field J., Wadsworth J., Johnson A.M., Anderson R.M. and Bradshaw S.A. (1990): Sexual lifestyles under scrutiny - Nature 348: 276-278.
729
EUROPEAN JOURNAL
September 1992, p. 723-729
Vol. 8, No. 5
OF EPIDEMIOLOGY
CONDOM USE AND SEXUAL HABITS OF HETEROSEXUAL INTRAVENOUS DRUG USERS IN NORTHERN ITALY D. SERRA1NO .1, S. FRANCESCHI*, E. VACCHER**, S. DIODATO***, D. ERRANTE**, I. CROSATO**, S. GUARNERI* and U. TIRELLI** *Epidemiology Unit and **AIDS Unit - Aviano Cancer Centre - 33081 Aviano (PN) - Italy. ***Public Drug Assistance Centre - USL 11 "Pordenonese"- Ospedale Civile 33170 Pordenone - Italy.
Key words: HIV - Intravenous drug use - Condom use - Heterosexual behaviour In order to assess modes of human immunodeficiency virus (H/V) transmission from heterosexual intravenous drug users (IVDUs) to their partners, condom use and sexual habits with both steady and occasional partners were investigated. A total of 349 heterosexual 1VDUs (247 men and 102 women) who ignored, at the time of interview, their H1V serostatus were interviewed. Respondents were asked for information on condom use and sexual habits for the three year period prior to the interview. Nearly 40% of IVDUs reported sexual intercourse with both steady partners and occasional partners. Fifty-four percent of their steady partners and 48% of their occasional partners were individuals who did not belong to groups at risk for HIV infection. Anal intercourse with steady partners was reported by 29% of 1VDUs and 24% of IVDUs with occasional partners. Condom use during vaginal intercourse was seldom reported: 83% of IVDUs never used a condom with steady partners and 75% did not use one with occasional partners. 1VDUs who were 1) unmarried, 2) enrolled in the study after 1986, 3) partners of not at-risk individuals, 4) partners of a foreigner and, 5) aware of their partners H1V seropositivity showed significantly higher, albeit still low, frequencies of condom use with steady partners. Conversely, all these factors seemed to have little impact on condom use with occasional partners. Condom use and sexual habits were similarly reported by H1V-positive and H/V-negative IVDUs. The present study shows that high-risk sexual behaviours among IVDUs are very widespread and it stresses the need for intensive counselling to promote condom use among IVDUs.
INTRODUCTION
The proportion of AIDS patients who acquired human immunodeficiency virus (HIV or HIV-1) infection by means of heterosexual transmission is rapidly increasing in Italy. The number of M D S cases among persons whose only risk factor for HIV infection was one or more sexual contacts with HIVinfected persons rose from 71 in 1987 (4.2% of all AIDS cases) to 514 in 1990 (6.4% of the cases) (8). Intravenous drug users (IVDUs) are the population 1 Corresponding author.
723
group at highest risk for HIV infection and AIDS, nearly 70% of the Italian AIDS cases occurred among them (8), and they also constitute the most important reservoir for HIV heterosexual transmission to the general population. Indeed, among heterosexuals with AIDS whose partner's risk group was known, 84% of women and 58% of men were partners of HIVinfected 1VDUs (8). Notwithstanding the importance of H1V sexual spread from IVDUs to their heterosexual, non-drugusing partners, there is little epidemiologic information on the prevalence of high-risk sexual behaviours of IVDUs and their partners (18, 20). Some studies have
Serraino D. et aL
Eur. J. Epidemiol.
suggested that condoms are seldom used by IVDUs (10, 11), while others have focused on the importance of prostitution among IVDUs as a source of HIV heterosexual spread (4, 17). In order to assess potential modes of HIV transmission from IVDUs to their sexual partners, we have investigated condom use and sexual habits of heterosexual IVDUs, exploring their behaviour with steady and/or occasional partners.
TABLE 1. - Distribution of 349 IVDUs, according to gender and other characteristics. Northeast Italy, 19841988. SEX Characteristics
Men (n = 247)
Women (n = 102)
No. (%)
No. (%)
100 (41) 67 (27) 80 (32)
48 (47) 30 (29) 24 (24)
Age (years):
< = 23 24-26 > = 27
MATERIALS AND METHODS
The present study is part of a larger crosssectional study on prevalence and determinants of HIV infection in IVDUs that began in 1984 in the Friuli-Venezia Giulia region, northeast Italy. Methods and results concerning the association between druguse habits and the risk of HIV infection have been previously described (16). Briefly, all IVDUs presenting for heroin abuse treatment to eight public drug assistance centres and who agreed to be tested for HIV antibodies were enrolled in the study. Before knowing the result of the blood test, each subject was asked for informed consent and then interviewed by the physician in charge of the drug assistance centre. Efforts were undertaken to train the physicians in order to standardize data collection procedures. Information was elicited, using a standard questionnaire, on socio-demographic factors, history of drug use and sexual behaviour for the three year period prior to the interview. The relative frequency of condom use during vaginal, oral and anal intercourse was estimated by means of a four-point scale: 1) never (0%); 2) sometimes (1-500/0); 3) often (51-990/0) and 4) always (1000/0). A partner was defined as steady if the sexual relationship had lasted for at least six months. Occasional partners were all other sexual partners. All HIV antibody tests were performed in a single laboratory. A subject was considered HIV-positive if a repeatedly positive ELISA test was confn-med by Western blot. Chi-square was used to assess statistical significance of differences between proportions, while, for ordered categorical variables with three or more levels, the Chi-square test for linear trend was computed (12). Odds ratios (ORs) and their 950/0 confidence intervals (CIs) were computed to estimate the association between condom use and several characteristics of IVDUs. Unconditional, multiple logistic regression (MLR) equations were fitted (2), allowing for age, sex and marital status. Betweeen March 1984 and December 1988, a total of 434 male and 147 female IVDUs were enrolled in the study. In the three years prior to the interview, 405 men (93%) and 134 women (920/0) reported heterosexual activity. The study group for this investigation consists of the 349 persons (247 men and 102 women) for whom information on condom use and sexual habits was available. They represent 61%
X~ for trend
2.45; p = 0.12
Marital statusa:
Single Married
x~
201 (82) 45 (18)
67 (67) 33 (33)
7.99; p < 0.01
HIV antibody: Negative Positive
137 (55) 110 (45)
69 (68) 33 (32)
4.43; p = 0.04 Type o f sexual partner:
Steady partners only Occasional partners only Both steady and occasional partners
98 (40) 50 (20)
58 (57) 7 (7)
99 (40)
37 (36)
12.95; p < 0.01 Condom use with steadJ" b partners:
724
Never Sometimes/often Always
X~ for trend
156 (80) 29 (15)
85 (90) 8 (8)
10 (5)
2 (2)
3.99; p = 0.05
Condom use with a' c occasional partners:
Never Sometimes/often Always X~ for trend
104 (76) 17 (12) 16 (12)
27 (73) 6 (16) 4 (11)
O.O3; p = 0.86
a: The sum does not add up to the total because of missing values; b: 57 IVDUs who reported occasional partners only were excluded; c: 156 IVDUs who reported steady partners only were excluded.
Vol. 8, 1992
Sexual habits of intravenous drug users
of the male and 76% of the female 1VDUs who reported heterosexual activity during the three-year period prior to interview and were attending five of the eight drug treatment centres in the study.
Condom use during vaginal intercourse was seldom reported. Twenty percent of male and 10% of female IVDUs (p < 0.05) stated ever using a condom with steady partners and 24% of men and 27% of women reported condom use with occasional partners (Table 1). Moreover, there were few IVDUs who reported having always used condoms, 4% with steady partner and 12% with occasional partners (Table 1). Oral intercourse was reported by approximately 75% of IVDUs, and there were no significant differences between frequency of oral sex with steady partners and occasional partners or between men and women (Fig. 1). The frequency of anal intercourse was similarly reported by male IVDUs with steady (280/0) or occasional (270/0) partners, whereas women seemed more likely to have anal intercourse with their steady partner than with occasional partners (30% and 14%, respectively, p = 0.06) (Fig. 1). There was no significant difference in the frequency of condom use and other sexual habits
RESULTS
Female 1VDUs in the present study were slightly younger (median age was 24 years for women and 25 for men), more likely to be married (p < 0.01) and less often infected with HIV (32% vs 45% seropositive, p = 0.04) than male 1VDUs (Table 1). In the three years prior to the interview, women appear to have had a higher mean number of sexual partners than men (19.7 and 13.3, respectively, p = 0.06). Eighty percent of male IVDU and 93% of female IVDU reported having had a steady partner, but nearly 40% of IVDUs of both sexes had had sexual intercourse with both steady and occasional partners (Table 1). percent
percent
1
100 C:t:~H v n~r+n~r
80
60
40
20
Oral s e x
Anal sex
Condom use
percent
100
Anal sex
Orltl eex
lefcent
loo 7
/
Occasional p~r)ner
•
80
ao"
60
80
40
40-
0cga_.~ion~dpartner
20"
0
-
Oral =ex
l
Men
~
L/
0
Amd eex Women
m
Figure 1. - Frequency of oral and anal intercourse, with steady and occasional partners, according to gender of interviewee.
~ft4g e e x
Oral sex
Condom u s e
HIV-pos ~
HIV-neg
Figure 2. - Frequency of condom use, oral and anal intercourse, with steady and occasional partners, according to HIV serostatus.
725
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Eur. J. Epidemiol.
TABLE 2. - Condom use during vaginal intercourse, according to type of partner and other characteristics. Northeast Italy, 1984-1988. Steady partners (n = 290) a Condom use (No.) % MLR-OR c (95% CI)
(No.)
(84) (84) (122)
14 18 18
(56) (45) (73)
(72) (215)
6 21
(117) (56) (117)
13 13 23
1 1.0 (0.42.0 (1.03.83; p = 0.05
(129) (98) (56)
18 17 14
1 0.9 (0.40.6 (0.20.78; p = 0.38
Use of cocained: No Yes
(123) (157)
18 15
Prostitution.~ No Yes
(269) (19)
HIV-antibody : Negative Positive
Characteristics
Age (years): > = 27 24-26 < = 23 X~ for trend Marital statusd : Married Single
1 1.2 (0.51.1 (0.50.39; p = 0.53
2.8) 2.5)
20 29 26
1 1.8 (0.7- 4.7) 1.5 (0.6- 3.6) 0.69; p = 0.41
(27) (144)
19 25
1 1.5 (0.5- 4.4)
2.6) 4.1)
(56) (35) (83)
23 17 28
1 0.7 (0.2- 2.2) 1.3 (0.6- 3.0) 0.61; p = 0.43
1.8) 1.7)
(73) (60) (38)
22 23 26
1 1.2 (0.5- 2.8) 1.8 (0.6- 5.4) 1.03; p = 0.31
1 0.8 (0.4-
1.5)
(59) (114)
20 25
1 1.2 (0.6- 2.7)
17 16
1 1.1 (0.3-
4.2)
(158) (16)
22 50
1 4.3 (1.2-14.8)
(175) (115)
17 17
1 0.9 (0.5-
1.7)
(88) (86)
20 28
1 1.4 (0.7- 2.9)
Partner from a high-risk group: Yes No
(140) (150)
10 23
1 2.3 (1.1-
4.8)
(84) (90)
24 24
1 1.0 (0.5- 2.1)
Partners' nationaOty : Italian Foreigner
(284) (6)
15 83
1 22.1 (2.5-198.7)
(160) (14)
24 21
1 0.8 (0.2- 3.1)
Awareness of partners" HIV seropositivity: No Yes
(259) (31)
15 32
(169) (5)
24 40
1 2.2 (0.3-14.6)
Year of interview: = 1987 ~ f o r trend Duration of heroin d addiction (years): =8 for trend
1 4.0 (1.4- 11.9)
Occasional partners (n = 174)b Condom use % MLR-OR° (95% CI)
1 2.8 (1.2-
6.8)
2 IVDUs who reported information on condom use with occasional partners but not with steady partners were excluded; b: 19 IVDUs who reported information on condom use with steady partners but not with occasional partners were excluded; c: Multiple logistic regression odds ratio (MLR-OR), and 95°/0confidence interval (CI), adjusted for sex, age and marital status; d: The sum does not add up to the total because of missing values. a:
726
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Sexual habits of intravenous drug users
condom with their occasional partners (OR = 4.3, 95% CI: 1.2-14.8), as compared with IVDUs who did not report prostitution. Conversely, the frequency of condom use with steady partners was comparable in IVDU prostitutes and in the rest of IVDUs. Having a partner not otherwise at risk for HIV infection (OR = 2.3), or a foreign partner (OR = 22.1), or being aware of the partner's HIV seropositivity (OR = 2.8) were all factors significantly associated with an increased, albeit still low, frequency of condom use with the steady partner. These characteristics did not seem to affect, however, condom use with occasional partners, although very few IVDUs (2 men and 3 women) were aware of the seropositive status of their occasional partners (Table 2).
percent 1O0 Steady partner 80
60
40
20
"
-
~
......
(----~Z-7 IVDU
HIV-po=ltlve
7
Foreigner
DISCUSSION
~rc~t • 100" Occasional partner 80604020-
J
.
l
IVDU
HIV-poeltlve
Foce4oner
Partner's characteristics I
Men
~
Women
Figure 3. - Characteristics of steady and occasional partners, according to gender of interviewee.
between HIV-positive and HIV-negative 1VDUs (Fig. 2). None of the IVDUs in the present investigation reported sexual intercourse with at-risk individuals apart from 1VDUs, and more IVDU women than men were the steady partner of an IVDU (69% vs 39%; p < 0.01). Female IVDUs were also more frequently aware of the seropositivity of their steady partner (p < 0.01) or occasional partners (p = 0.05) than male IVDU (Fig. 3). The associations between several factors and condom use with steady partners and with occasional partners are shown in table 2. Unmarried IVDUs showed a four-fold higher frequency of condom use with their steady partner than married IVDUs (OR = 4.0, 95% CI: 1.4-11.9). A significant trend of increase in the frequency of condom use with the steady partner by year of enrollement in the study emerged (p = 0.05), whereas no change across the study period was seen regarding the use of condoms with occasional partners (Table 2). IVDUs who reported episodes of prostitution (10 men and 16 women) were more likely to use a
Transmission of HIV among IVDUs occurs primarily through needle and syringe sharing and, to a lesser extent, by sexual intercourse (5-7, 14). Sexual intercourse plays, however, a very important role in HIV spread from IVDUs to the general population. Data concerning the sexual behaviour of IVDUs are, therefore, important in order to assess modes of HIV spread and to design effective AIDS education and prevention programmes. The present investigation focused on condom use and sexual habits of 1VDUs, and the study supports previous research indicating that IVDUs constitute an important source of H1V heterosexual spread (9, 10, 19). Among the findings of the study, the high proportion of partners who were not otherwise at risk for HIV infection and the very low frequency of condom use are of particular concern. As seen in IVDUs in Amsterdam (19), nearly 40% of IVDU men and women in the present study reported sexual intercourse with both steady and occasional partners, and approximately half of their partners did not belong to groups at risk for HIV infection. From these data, male IVDUs appear to play a more important role than female IVDUs in the heterosexual transmission of HW, since 65% of their steady partners were non-drug-using women and condoms were used infrequently. This finding is in agreement with the epidemiology of AIDS among heterosexuals in Italy, where non-drug-using women who were partners of male IVDUs represented the largest group with AIDS (8). The low prevalence of condom use among heterosexual IVDUs, consistently documented by other studies (3, 9-11, 15, 19), is confirmed in the present investigation. Some differences which emerged in the frequency of condom use with steady and occasional partners are worth noting. Among IVDUs in New York City, those who lived together with their steady partner showed a lower, although not significantly different, frequency of condom use (11). Similarly, in the present study, a significantly higher frequency of condom use with steady partners emerged among unmarried IVDUs. A
727
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Eur. J. Epidemiol.
decrease in needle-sharing among IVDUs has been shown, but an increase in condom use and the adoption of safer sex practices over time has never been reported in IVDUs (1, 7, 13). While an almost two-fold increase of IVDUs who reported condom use with their steady partners after 1986 may be encouraging, it is worth noting that no consistent increase in condom use with occasional partners was seen during the study period. Previous research has documented a positive association between one's knowledge of partner's HIV seropositivity and condom use (11, 18). In the present study, the frequency of condom use was somewhat higher among IVDUs who knew the HIV seropositive status of their partner. However, two thirds of IVDUs did not use condoms despite such knowledge and very few IVDUs were aware of a partner's HIV seropositivity, particularly with regards to occasional partners. Prostitution and anal intercourse have been shown to be important modes of HIV heterosexual transmission (6, 10, 16, 17). In the present study a higher frequency of condom use with occasional partners, but not with steady partners, emerged among IVDUs who reported prostitution. This finding is in agreement with the higher frequency of condom use reported among IVDU prostitutes with their clients in Amsterdam, where over 80% reported use of condoms, as compared with their non-paying partners (19). Twenty-nine percent of IVDUs in the present study reported having ever had anal intercourse with their steady partner and 24% with their occasional partners. The prevalence of such sexual behaviour was, overall, similar to that found among IVDUs in the USA (10). Some limitations of the present study, which are common to much research on HIV infection among IVDUs, are worth noting. The lack of random selection of the population sample hampers the generalizability of the findings, since serf-referring IVDUs may not be representative of the IVDU population in the area under study. In addition, information on condom use and sexual habits was obtained only from a sub-set of self-referred IVDUs. Furthermore, misreporting on some of the factors investigated is likely to have occurred and information on other relevant aspects of sexual habits, such as number of sexual encounters and duration of sexual relationship, was not available. The study, however, is one of the largest ever conducted in this area (10, 11, 19), and it offers the opportunity to compare the frequency of condom use and sexual habits of heterosexual 1VDUs with their steady and occasional partners. Regarding the comparison of HIV-positive and HIV-negative IVDUs, it is important to bear in mind that condom use and sexual habits herein investigated concerned a period when the subjects were not yet aware of their HIV serostatus. ARhough efforts were made to exclude from the study all IVDUs who knew their HIV serostatus before the interview, it is possible
that some subjects did not report previous HIV antibody tests. Obviously, IVDUs may have changed their highrisk sexual habits after knowledge of their blood test result. Further follow-up information is essential for evaluating the impact of knowing one's HIV seropositivity on his/her sexual behaviour. In conclusion, the present study confirms that high-risk sexual behaviours among IVDUs are very widespread and that IVDUs are very reluctant to protect themselves and their partners from HIV infection through sexual intercourse. This held true even when the study participants, who did not know before the interview whether they were HIV-positive, had a steady partner known to be seropositive. Further research on sexual habits oflVDUs and their partners is needed in order to overcome barriers to condom use and to identify optimal sexual risk reduction strategies. Acknowledgements: We would like to thank the staff of the drug assistance centres and of the AIDS Unit - Aviano Cancer Centre - for their valuable collaboration and Dr. D. Gerdol for controlling all the questionnaires. Thisworkwas supportedbya grantfromthe ItalianMinistry of Health - Istituto Superiore di Sanit~t, IV Progetto AIDS 1991, Contract No. 6202-027 and No. 6205-006 - Rome, Italy. REFERENCES 1.
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Sexual habits of intravenous drug users
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