European Journal of Epidemiology 15: 439±445, 1999. Ó 1999 Kluwer Academic Publishers. Printed in the Netherlands.
Seroprevalence of HIV, HCV and syphilis in Brazilian prisoners: Preponderance of parenteral transmission E. Massad, M. Rozman, R.S. Azevedo, A.S.B. Silveira, K. Takey, Y.I. Yamamoto, L. Strazza, M.M.C. Ferreira, H.B. Carvalho & M.N. Burattini NUPAIDS, The University of SaÄo Paulo, SaÄo Paulo, Brazil Accepted in revised form 18 January 1999
Abstract. Between November 1993 and April 1994, our physicians' team interviewed and took blood samples of 631 prisoners randomly drawn from the largest prison of South America, which counted about 4700 inmates at that time. The interview consisted of questions related to risk behaviour for HIV infection, and the subjects were asked to provide blood for serological tests for HIV, hepatitis C and syphilis. Our main purpose was to investigate the relationship between HCV and injecting drug use as related to HIV seropositivity. Participation in the
study was voluntary and con®dentiality was guaranteed. Overall prevalences found were as follows: HIV: 16% (95% con®dence interval (CI): 13±19%); HCV: 34% (95% CI: 30±38%), and syphilis: 18% (95% CI: 15±21%). Acknowledged use of ever injecting drug was 22% and no other parenteral risk was reported. Our results, as compared with other studies in the same prison, suggest that HIV prevalence has been stable in recent years, and that the major risk factor for HIV infection in this population is parenteral exposure by injecting drug use.
Key words: AIDS, Hepatitis C, Injecting drug abusers, Prisoners, Seroprevalence Introduction AIDS was ®rst reported among prisoners in 1983 by Wormser et al. [1], who described seven cases of AIDS diagnosed between September 1981 and June 1982 in a New York prison. None of those prisoners were homosexual, but all had been intravenous drug users (IDUs) prior to incarceration. In the past decade, several health organizations like the CDC [2], the Council of Europe [3] and the WHO [4] have highlighted key aspects of HIV infection in prisons: the high proportion of IDUs among AIDS cases, the high prevalence of HIV infection among IDUs and the high and increasing proportion of IDUs in prison populations. Since then, many studies have investigated drug injectors and HIV infection in prison [5]. HIV infection and AIDS are major public health concerns for prison authorities [6]. The problem has been fueled by the rapidly increasing numbers of prisoners in many countries [7] and the increasing proportion of inmates who are injecting drug users. As mentioned by Bird and Gore [8] prisons are `selectively enriched' with injecting drug users. Several studies have provided evidence that signi®cant rates of high risk behaviour (injecting drug use, sharing of needles and syringes, and sexual activity) occur in correctional settings [9±16]. In a recent Scottish study [17] it was demonstrated that 27% of the inmates reported injecting drug usage at any time in life. Of these, 59% confessed the use inside the
prison, of which a quarter had ®rst injected inside the prison. In addition, some other works have reported high levels of HIV seroprevalence in prison institutions [6, 18±20]. The Brazilian penal system comprises 511 penitentiaries with 59,954 places, which host around 86,500 prisoners of whom approximately 50% are in the State of SaÄo Paulo. They are predominantly male (96.3%), of which 40% are aged between 31 and 50 years, with an average age of 31 years old. Also, they are in the majority single, poor and illiterate. With respect to their delicts, burglary/robbery account for 40%, with homicide (16%) and drug related delicts (13%) being the next most frequent ones. In addition, about 30% of them report ever having used illicit drugs in life [21]. In a recent review relating the occurrence of HIV infection among Brazilian prisoners [21], we identi®ed 19 seroprevalences studies, of which 13 were carried out in the State of SaÄo Paulo. HIV seroprevalences found ranged between 0% and 37%, according to the geographical region of the prison (low or high HIV endemicity) and to the frequency of reported drug usage among prisoners. A study carried out in 1987 with 923 prisoners from the Carandiru Complex, of the SaÄo Paulo State penal system, found an HIV seroprevalence of 12.5% [22]. Another survey carried out in 1692 recent admitted prisoners to the same SaÄo Paulo State Penitentiary demonstrated a seroprevalence of 14.9% in 1990 and 17.3% in 1991 [23]. Also, a study carried
440 out in SaÄo Paulo among arrested disadvantage youths, aged between 12 and 18 years old, showed a high prevalence of HIV (3.5%), of sexual risk behavior (86%) and of injecting drug usage (12%) [24]. Moreover, a number of studies have shown a high prevalence of HIV among Brazilian IDUs [25±27]. As of September 1997, 26% of the 110,845 reported AIDS cases in Brazil were directly attributable to injection drug use [28]. HIV prevalence among IDUs ranges from 25% in Rio de Janeiro [29], to 60% in Santos [27] and 70% in ItajõÂ [30] Also, a strong correlation has been shown between IDU and HIV infection in prisoners [31]. Serosurveys of HIV infection among inmates entering prison serve to estimate the extent and scope of infection, to identify the reservoir from which intraprison transmission might occur, to provide an empirical foundation for the development and re®nement of policy and prevention programmes, and to supplement information from other sources on the extent and scope of HIV infection in the community from which the inmates originate and to which they return [5]. Every year, more than 8 million prisoners are released from the North-American penal system, a fact that illustrates the potential danger of HIV, tuberculosis and other infections acquired or aggravated inside the prisons [32]. On the other hand, there is evidence of an increased incidence of sexually transmitted diseases (STDs) among prisoners, which act as coadjuvant facilitating HIV transmission by the sexual route [33]. In addition, approximately 1 in 10 male inmates have sex while in prison [10], and only a small fraction of prisons systems make condoms available, leaving the prisoners to their own care [34]. The aim of this paper is to describe the epidemiological background as related to HIV seroprevalence, in order to provide information for a better understanding of the main route of HIV transmission among inmates of the Carandiru Complex of the SaÄo Paulo penal system. Methods The target population SaÄo Paulo has the largest penal institution of Latin America and third in the world, the so-called Carandiru complex, localized downtown of SaÄo Paulo City, which lodges about 10,000 prisoners. This ®gure comprises about 20% of the total penal system of the State of SaÄo Paulo, in which one death per day attributed to AIDS has been reported in the last few years (Schechtman, 1993, personal communication; no ocial data on AIDS/HIV incidence in the system is available). At the time of this study prevalence of HIV infection among prisoners of the State of SaÄo Paulo ranged from 14.9% to 17.3% [23]. This study was carried out in one of the prisons of the Carandiru
complex, the so-called `Casa de DetencËaÄo' (Detention House, DH) which comprised, at the survey time, 4677 male inmates. This prison is supposed to be a transitory step for those individuals who are awaiting ®nal sentence. However, they stay in fact for several years, with an average residence of 2.78 years. This implies a very heterogenous population with very distinct patterns of crimes committed. Thus, 9% of the population have their sentences associated directly with drug smuggling and 39% with any other indirect relationship with drugs use. The sampling method Sample size, n, was determined based on an expected seroprevalence to HIV, P, of 15% [23], with speci®ed relative precision, e, of 20% and con®dence level, a, of 95% according to [35]: n
z21ÿa=2
1 ÿ P e2 P
which, after correction for a ®nite population and assuming 20% refusal, resulted in 600 individuals. These individuals were selected by randomly drawing their prison ®les in steps calculated by a computer program. In addition, were included all individuals recently admitted to the institution during the ®rst two weeks period of the study (n=68). They were included in order to provide evidence from the epidemiological background of this population (the extent and scope of HIV infection in the community from which the inmates originate) and, perhaps more important, to allow comparisons with previous studies carried out in recently admitted prisoners of the same prison, as mentioned in [22, 23]. Participation in the study was voluntary and con®dentiality was guaranteed. Thirty-seven individuals refused to participate in the study, resulting in the ®nal sample of 631 inmates (which corresponds to 95% of the proposed sample). The ®eld work Between the months of November 1993 and April 1994, 631 inmates were interviewed, clinically examined and bled for serological examination. The interview consisted of answering a standardised questionnaire, adapted from the one used in the WHO Multi-City Study of HIV infection among IDU [36]. It was tested in this speci®c population through a pilot study and included speci®c questions related to past imprisonment history, risky behaviors related to HIV infection, besides clinical aspects related to HIV/AIDS infection. The interviews were exclusively conducted by the physicians of our team, and the results of the serological tests performed were delivered directly to the prisoners. Ocial administrative sta did not have access to the answers of individual questionnaire nor to the results of the serological tests, but the latter were promptly noti®ed
441 to the medical sta responsible for the care of the prisoners. In addition, by the time of the noti®cation of serological tests to the prisoners they were oered professional counselling by the psychologists and psychiatrists of our team. Laboratory tests Serological examination for HIV and hepatitis C were performed by standard ELISA techniques with commercial kits from EmbrabioÒ and Abbot Diagnostics DivisionÒ (second generation kit), respectively. Syphilis was screened by standard TPHA technique with commercial kit by Bio-MeÂrieuxÒ. Those with positive ELISA reaction to HIV were con®rmed by Western Blot technique, using commercial kit by Diagnostic PasteurÒ, and those with a positive ELISA reaction to HCV were con®rmed by immunoblot, using commercial kit by EmbrabioÒ. Determination of CD4+ T-lymphocytes absolute counting was performed in the HIV-positive individuals by microsphere assay as described by [37]. HIV-positive individuals were classi®ed according to the 1993 Revised Classi®cation System for HIV Infection and Expanded AIDS Surveillance Case De®nition for Adolescents and Adults, due to CDC AIDS workgroup [38]. Statistical analysis The association between risky behavior and HIV infection was evaluated by multivariate analysis using logistic regression. HIV seropositivity was considered the dependent variable, and the independent risk associated variables included: (i) injecting drug use ± at least once in life versus never; (ii) male homo/bisexual relationship ± yes versus no; (iii) sexual risky behavior, de®ned as either having had unprotected intercourse with an eventual partner in the last 6 months or having had sex with an HIV positive partner; (iv) history of blood transfusion ± yes or no; and ®nally, (v) HCV and syphilis (TPHA) seropositivity, which were included in the analysis as possible surrogates for parenteral and sexual exposition to HIV, respectively. The initial assessment was carried out by applying univariate and strati®ed analysis using the softwares EPI INFO [39] and EGRET [40]. Results The age of the prisoners included in the sample ranged between 18 and 80 years old with an average of 30.8 and a median of 29 years. Thirty-®ve percent had been incarcerated for at least two years before admission to DH, but the average time of imprisonment before admission to DH was 0.96 years. The average time of imprisonment in DH was 2.8 years (median 2 years), ranging from 1 to 14 years. Overall seroprevalence for HIV found was 16.0% (95% CI: 13.1±18.9) with 2.5% of undetermined
Western-Blot reaction. The latter were considered negative to HIV for the purposes of this analysis. Antibodies against hepatitis C were found in 34.1% (95% CI: 30.4±37.8) of the population, and against syphilis in 18.1% (95% CI: 15.0±21.2). In twelve (5.6%) individuals, ELISA seropositivity to HCV were not con®rmed by immunoblot and they were considered negative to HCV for the purposes of the present analysis. Ninety-eight individuals were positive to HIV, but we could determine the CD4 counts of only 62 of them, due to insucient volume of the blood sample. Of these, 2 had CD4 counts lesser than 200/mm3, 7 had CD4 counts between 200±500/mm3 and the remaining 53 had CD4 counts above 500/ mm3. In addition, 13 out of the 98 HIV-positive individuals (13.3%; 95% CI: 8.5±18.1%) ful®lled the CDC-1993 criteria for AIDS. No parenteral exposure other than injecting drug use and blood transfusion was reported. Table 1 shows the results of the univariate and multivariate analysis for the risk factors related to HIV infection in this work. All risk factors with signi®cant association with HIV at the univariate analysis were included in the multivariate analysis, in addition to the positivity to syphilis. The later was included because we assumed that it could be a marker for sexually transmitted HIV. In addition we performed a multivariate risk analysis without including HCV and syphilis serology. In this case, intravenous drug usage was the variable most signi®cantly associated with HIV infection (odds ratio (OR): 8.27; 95% CI: 5.07±13.49). This OR is almost the same that was found in the univariate analysis, contrasting with the OR found for this variable in the multivariate analysis including HCV serology (see Table 1). This fact demonstrates that HCV seropositivity is more strongly associated with HIV than IDU, and that those variable are correlated. On the other hand, the OR for the variables describing sexual risk did not change signi®cantly when excluding syphilis serology from the analysis. In order to analyze the possible eects of colinearity between reported use of injecting drugs and hepatitis C, as well as between reported homo/bisexuality or sexual risky behavior and syphilis, we de®ned two new variables describing parenteral exposure (which includes those with a positive response either to injecting drug ± acknowledged ± or hepatitis C ± seropositivity) and sexual exposure (the same as above, now applying for homo/bisexuality or sexual risky behavior or TPHA reactivity). Table 2 shows the results of the multivariate analysis considering the interactions between these two new variables. As can be noted from Table 2, we found a negative interaction between variables associated with sexual and parenteral exposure to HIV. This holds true either when we consider seropositivity to syphilis and HCV as surrogates of the route of exposition or when
442 Table 1. Results of the uni- and multivariate analysis of the risk factors associated with HIV infection among male inmates (n=631) HIV+ n (%)
HIV) n (%)
Total n (%)
Injecting drug use No Yes
39 (6.6) 59 (9.9)
420 (70.6) 77 (12.9)
459 (77.1) 136 (22.9)
8.2 (5.0±13.3)
3.4 (1.8±6.2)
Homo/bisexual behavior No Yes
78 (13.2) 20 (3.4)
450 (76.3) 42 (7.1)
528 (89.5) 62 (10.5)
2.7 (1.5±4.8)
2.4 (1.1±5.4)
Sexual risk behavior No Yes
46 (7.9) 50 (8.6)
285 (49.2) 198 (34.2)
331 (57.2) 248 (42.8)
1.6 (1.01±2.5)
1.6 (0.9±2.9)
History of blood transfusion No Yes
86 (14.8) 9 (1.5)
448 (77.0) 39 (6.7)
534 (91.8) 48 (8.2)
1.3 (0.6±2.9)
a
HCV serology No Yes
16 (2.7) 75 (12.5)
375 (62.3) 136 (22.6)
391 (65.0) 211 (35.0)
15.4 (8.5±27.9)
TPHA reactivity No Yes
71 (12.4) 19 (3.3)
395 (68.9) 88 (15.4)
466 (81.3) 107 (18.7)
1.3 (0.8±2.4)
Risk factor
a
OR (95% CI) univariate analysis
OR (95% CI) multivariate analysis
10.5 (5.1±21.7)
1.6 (0.8±3.1)
Not included in the multivariate analysis.
Table 2. Results of the multivariate analysis of the risk behaviors associated with HIV infection, considering the possible interactions between sexual and parenteral exposure to HIV Risk factor Sexual exposure No Yes Parenteral exposure No Yes
Univariate analysis OR
Multivariate analysisa OR (95% CI)
1.0 1.7
1.5 (0.9±2.6)
7.7 (2.2±26.4)
1.0 16.7
16.2 (8.4±31.1)
39.6 (13.9±113.3)
Interaction No Yes a
Multivariate analysis OR (95% CI)
1.0 0.13 (0.03±0.5)
Considering the interactions between the variables.
we consider the variables parenteral and sexual exposure to HIV, as described above. These results are shown in Table 3. Discussion Our results, when compared with previous studies [22, 23], suggest a stationary situation of overall HIV prevalence in the past few years for this prison. Furthermore, reported drug use inside this prison has remained approximately constant, around an overall prevalence of 5% (as compared with 15% among HIV-positives), over the last decade [41]. Both the above described prevalences re¯ect the virtual ab-
sence of prevention programs directed to this particular population. In addition, in spite of the fact that the prisoners had been regularly tested for HIV in the last decade, only a negligible (less than 5%) fraction of them knew about their HIV serostatus at the time of this study. We demonstrated a strong correlation between HIV and HCV seroprevalences in the studied population, even in the absence of acknowledged use of injecting drug. This fact, allied to the lack of signi®cant correlation between HIV and syphilis seroprevalences, in addition to the low correlation (though statistically signi®cant) found between HIV and homo/bisexual habits suggest that the parenteral route is the most likely way of HIV transmission in
443 Table 3. Odds ratios of the possible interactions between sexual and parenteral exposure to HIV in the studied population Sexual variables
HCV)
HCV+
TPHA) TPHA+ Homo/bisexuality) Homo/bisexuality+
1.0 4.7 1.0 9.7 Parenteral exposure) 1.0 7.7
14.5 9.6 15.8 19.1 Parenteral exposure+ 36.9 38.7
Sexual exposure) Sexual exposure+
this population. In fact, HCV analysis was performed based on the assumption that it can be used as a surrogate indicator for parenteral transmission. This assumption, although not indisputable, has some support in the literature [42±45]. Moreover, as can be noted from Table 1, the variation in the OR for HCV seroprevalence when comparing the results of the uni and multivariate analysis showed a reduction of 32% whilst the reduction in the OR of acknowledged injecting drug was of 60%. This ®nding indicates that HCV seroprevalence is more strongly associated with HIV infection than the acknowledged use of injecting drugs. Therefore, HCV seropositivity can be considered a better indicator of parenteral exposure to HIV than the reported use of injecting drug use, at least in this population. In addition, as shown in Tables 2 and 3, the multivariate analysis using the new composite variables has shown that HCV prevalence and acknowledgement of drug injection information complement each other in the measurement of parenteral exposure to HIV infection. The fact that HCV prevalence is a more reliable indicator of parenteral exposure to HIV is not surprising since IDU is a criminal oence in Brazil, and therefore the acknowledgement of its use in an epidemiological survey conducted inside a prison should not be expected, even when the interviews were conducted by a non-sta physician, which is the case in this study. The analysis of the interactions between parenteral versus sexual exposure to HIV and between HCV and syphilis seropositivity, after correction for age, pointed to a negative interaction between those variables. This could be assigned to a lower sexual activity among IDUs as already reported [46]. The in¯uence of drug abuse on sexuality is usually felt to be negative (decline in libidinal energy, impotence), and often brings about a decrease in sexual contacts. This is equally true for both opiates and stimulants (cocaine, amphetamine). Promiscuous behavior is rare as such, however a large proportion of drug users is at some stage exposed to prostitution [46]. The latter is particularly true for female IDUs, which
is not the case in our sample. However, as our questionnaire did not address this speci®c question, further studies should be pursued in order to clarify this point. It should be mentioned that the prevalence of HIV infection found inside this prison is about 75 times higher than in the general community at large. In addition, about 50% of this population have regular sexual intercourse with female partners living outside the prison (a legal right of Brazilian prisoners), of whom only 2.7% report regular use of condoms. The prevalence of HIV among these sexual mates is about 10% (unpublished data), which is an indication of their role as potential vectors of social transmission of HIV to the community at large. The above mentioned discussion, allied to the relatively low average time of imprisonment (2.78 years), which results in about 10,000 prisoners liberated every year by the SaÄo Paulo penal system, indicates the potential risk that this community represent to the population at large as a possible vector for HIV. So, there is an urgent need for the implementation of educational campaigns on HIV prevention directed to the inmate population and to their sexual partners, besides free distribution of condoms, at least during the visiting period, together with other control strategies. Finally, a few words should be added about the limitations of this study. First we should comment that we are well aware of the potential bias caused by the inclusion of all recently admitted prisoners, during the ®eld phase, into the randomly drawn sample from the prison population. However, as mentioned in the methods we included those prisoners in order to evaluate potential changes in HIV prevalence in recent years among this social strata outside the prison. Second we should comment on the limitations of the instrument applied to collect information about habits and risk behaviors to HIV infection. We are well aware of the high sensitivity of responses to the wording of questions, particularly in the area of drug use/sexual behavior investigations. However, our instrument was previously adjusted to speci®c language obstacles that could compromise comprehension, in a pilot phase. Nevertheless, this would not avoid potential bias due to the expected reluctance to acknowledge illegal and/or not socially approved practices. To minimise bias, the interviews were conducted in a private and closed room, with the prisoners alone with our interviewer, in order to establish a relationship as con®dential as possible given the circumstances. Notwithstanding the above mentioned limitations, we believe that our results are in good agreement and reinforce the current beliefs on the main route of HIV transmission among prisoners. In this sense, the use of HCV serology as a proxy to HIV parenteral transmission seems to be an appropriate alternative, to be considered in future studies.
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[email protected]
