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Up to 17 000 persons in the USA became infected with hepatitis C virus (HCV) in 2007, and many cases have unknown transmission routes. To date research on transmission of HCV via shared implements used to snort or smoke non-injection drugs has been inconclusive.
We tested stored sera for HCV antibodies (anti-HCV) in a large population-based study of homeless and marginally housed persons in San Francisco. We examined the association between sharing implements used for snorting and smoking drugs and anti-HCV while controlling for sociodemographic variables in those who denied everinjecting drugs (n = 430). We also examined the association of anti-HCV status with history of incarceration, tattoo and piercing history, sexual history and alcohol consumption.
Seventeen percent of our sample was anti-HCV positive. We found no statistically significant associations with sharing implements used to smoke or snort drugs with anti-HCV status in our various multivariate models. There was a statistically significant negative association between ever snorting cocaine and anti-HCV status (adjusted odds ratio: 0.39; 95% confidence interval: 0.21–0.73). There were no other statistically significant associations with any other measured covariates in multivariate analyses.
Our findings suggest that sharing implements to snort or smoke drugs is not a significant risk factor for anti-HCV-positive status.
Hepatitis C virus (HCV) is a significant cause of morbidity and mortality in the USA. Chronic HCV infection is the most frequent cause of chronic liver disease, and recent research has shown significant potential increase in disease-associated mortality.1,2 The prevalence of HCV in the USA has remained close to 2% over the last decade.3,4 Recent surveillance data from the Centers of Disease Control and Prevention (CDC) estimated ~17 000 new HCV infections in the USA in 2007, with 35% of the reported cases having unknown risk factors for infection.5
Research into non-injection drug use as a potential source of HCV infection has been inconclusive. Several studies have demonstrated that non-injection drug users have a higher anti-HCV prevalence than the general population, with estimates ranging from 5 to 29%.6–8 Two studies have found an association between intranasal use of cocaine and anti-HCV,9,10 and researchers have isolated HCV RNA in nasal secretions and implements used for drug inhalation.11 Blood-contaminated non-injection implements such as straws could transmit infection via damaged nasal mucosa.12 Similarly, other research demonstrated low viral titers of HCV in saliva,13 lending plausibility to shared oral drug utensils such as crack pipes as a route of transmission. While some studies have shown an association with sharing non-injection implements or non-injection drug use and HCV infection,1,9,13 others have not shown a significant association.7,14,15
Research examining other potential permucosal routes of transmission also has yielded inconsistent results. While permucosal contact via sexual intercourse is a biologically plausible route of infection, sexual transmission of hepatitis C is inefficient when compared with other viral infections such as HIV and hepatitis B.16 Although having multiple sexual partners, being infected with HIV, engaging in mucosally traumatic sexual behaviors and having sexually transmitted infections have been associated with higher HCV prevalence,16–19 overall infection via sexual contact appears to be rare even among persons with high-risk behaviors20 but may be increasing in HIV-positive men who have sex with men;21,22 Bottieau, Apers et al. 2010).
Research examining other percutaneous risk factors such as tattooing and piercing, which could expose individuals to HCV-contaminated needles, has not produced definitive conclusions regarding an association with HCV infection. One study suggested that association with tattooing could be explained if tattooing served as a surrogate marker for a history of injection drug use.23 The association could also depend on whether the tattooing is done in licensed or unlicensed settings, the presence of specific dyes, the quality of the tattoo or deficiencies in proper instrument sterilization.24–27 Similarly, piercing could hypothetically expose people to HCV, yet studies have shown no such link.1,28,29
Homeless persons who denied ever injecting drugs have many of the characteristics that have been associated with increased anti-HCV prevalence: high rates of non-injection drug use, close association with intravenous drug use (IDU) and increased sexual risk behavior.30,31 The homeless are therefore a key population in which to study HCV transmission. We reviewed data for participants who denied every injecting drugs in a large population-based study of homeless and marginally housed persons in San Francisco to estimate anti-HCV prevalence and examined the association of anti-HCV status with sharing non-injection drug implements, specifically used crack pipes and used straws, rolled dollar bills or similar utensils for the snorting of powdered illicit drugs.
We used sample information from data collected through the Research and Access to Care for the Homeless study of homeless and marginally housed adults in San Francisco between 1999 and 2000. This study selected participants by systematic sampling within three different types of settings: 5 homeless shelters, 6 locations providing free lunches and 28 hotels for low-income individuals.32 The hotels were chosen for the sample with probability proportional to the number of beds in the hotels while all the large homeless shelters and free lunch programs were included (serving over 100 people per day). Study participants gave their birth date and their parents' first names as unique identifiers used to receive HIV test results; we collected no other identifying information. The Institutional Review Board of the University of California, San Francisco approved all procedures and the University of California, Berkeley approved the analysis of de-identified data.
Subjects completed a detailed questionnaire including information about sociodemographics (e.g. age, ethnicity and education level), any history of homelessness/marginal housing, history of jail or prison time, alcohol/drug use, sexual behavior, and tattooing and piercing history. We separated jail and prison time as distinct categories of incarceration in order to assess whether subject characteristics could differ across the two settings, especially since the difference in the typical lengths of stays33 could affect HCV exposure. We defined participants as having ever injected drugs if they reported ever injecting specific drugs (heroin, methamphetamine, cocaine or other drugs) or if they answered yes to a general question about any lifetime injection of illicit drugs or drugs that were not prescribed for the participant.
We categorized sex as male or female and divided men into those who reported having sex with men (MSM) as described below and others.34 Participants described their sexual behavior with the following categories: ‘straight behavior only’, ‘mostly straight behavior’, ‘bisexual behavior’, ‘mostly gay behavior’ and ‘gay behavior only’. We classified men who reported any sexual behavior category other than ‘straight behavior only’ as MSM. Participants were asked their number of lifetime sexual partners in four categories: ‘<5’, ‘6–25’, ‘25–100’ and ‘>100’.
Participants also reported total duration spent homeless/marginally housed in months and years, and we categorized this variable as ‘<1 year/marginally housed’, ‘1–5 years’ and ‘>5 years’. We defined homelessness as having spent any period of time outdoors, in an emergency shelter or in a place not designated as a living residence35 and included the term ‘marginally housed’ to refer to people who resided in low-income single-room occupancy hotels or presented at free food lines despite being housed.36 We assigned subjects who stated that they had never been homeless to the ‘<1 year’ category.
Any instance of drug use and routes of administration were elicited for crack cocaine, powder cocaine, heroin and methamphetamines. We asked if participants had ever shared crack pipes and straws or other items for smoking or snorting drugs, and asked if they ever had oral burns or blisters from smoking crack. We defined heavy drinking as more than five drinks or four drinks per day on typical drinking days for men and women, respectively.
Serum samples collected following the completion of the questionnaire were stored at −70°C. HCV antibody testing was performed at the CDC Hepatitis Reference Laboratory in 2005, using Ortho HCV Version 3.0 ELISA (Ortho-Clinical Diagnostics, Raritan, NJ), and for samples in which the signal-to-cutoff ratio was between 1.0 and 3.8 and recombinant immunoblot assay (Chiron RIBA HCV 3.0 SIA, Chiron Corp., Emeryville, CA) was conducted for confirmation. At the time of data collection, we also performed HIV pre-test counseling and HIV antibody testing using ELISA with western blot confirmation (Unilab, Tarzana, CA) immediately following the study interview. HIV results were available 1 week after the blood draw.
We calculated univariate percentages to describe the overall distribution of the variables of interest stratified by HCV antibody status. We also calculated odds ratios and 95% confidence intervals (CIs) to examine the association of the explanatory variables with anti-HCV status. We subsequently created a multivariate logistic regression model to examine the independent associations of snorting or smoking drugs with being anti-HCV positive, while controlling for sociodemographics (age, education, sex and ethnicity), duration of homelessness, history of jail or prison time, HIV status, sexual history, tattooing history, piercing history and alcohol consumption (Model 1). Our in-depth analysis of drug equipment sharing behavior focused only on crack and powder cocaine users. Therefore, we divided those who ever smoked or snorted drugs into those who smoked crack cocaine vs. other drugs and those who snorted powder cocaine vs. other drugs. Next, we constructed another model using only the observations of respondents who reported ever snorting cocaine (n = 252) to examine the effect of sharing snorting implements, while controlling for all other variables listed above (Model 2). We also constructed a model to examine the independent effect of sharing crack pipes and having burns or blisters due to smoking crack while controlling for all other variables among respondents who ever reported smoking crack (n = 307) (Model 3). Lastly, we constructed a model to further examine associations with tattooing among those who had ever been tattooed (n = 86) as we noted an increased risk associated with tattooing and HCV in bivariate analysis. We examined the independent effect of the number of tattoos, whether the tattooing was conducted in prison, jail or other non-commercial settings (Model 4) controlling for sociodemographics, duration of homelessness, history of jail or prison time, HIV status, sexual history, piercing history and heavy alcohol consumption.
A total number of 1542 people participated in the study, and 1225 agreed to have their blood samples stored for future analysis. After excluding subjects with indeterminate anti-HCV results, there were 1220 participants left in the sample. Of these, 430 participants reported no history of injecting drugs; 790 participants consistently reported a history of injecting drugs. These participants were 73% male with a mean age of 44 (SD = 8.8; Table 1). African-Americans made up the majority of the sample (56%) with 28% white and 16% of other or mixed race. Three-quarters (74%) of the participants had at least a high school education. The majority (70%) reported a history of jail time, while 20% had ever been in prison. There was a high level of chronic homelessness; 44% had spent 1–5 years homeless and 15% had been homeless for >5 years. Seventeen percent were anti-HCV positive and 8% were anti-HIV positive. This was in marked contrast to the group who reported a history of injection drug use: the majority (83%) was anti-HCV positive.
We examined the drugs used and the route of administration (Table 1). More than half of the participants (54%) reported ever using both powder and crack cocaine, 9% ever used powder cocaine exclusively and 22% ever used crack cocaine exclusively. Approximately 2% of our study participants reported no illegal drug use. Sixty-five percent of the participants reported ever snorting any drugs with the majority snorting cocaine exclusively. In contrast, 78% reported ever smoking any drugs with most reporting smoking crack cocaine only (Table 1). Seventy percent of cocaine users had ever shared a straw, dollar bill, key or spoon that was used by someone else to snort the drug; 75% of crack smokers had used a crack pipe that someone else had used and 36% had ever had blisters or burns on their mouth or lips from smoking crack.
One-quarter (22%) of participants reported that they had ever been tattooed, and of those who had a tattoo, 28% received their tattoos exclusively in commercial settings, 28% had been tattooed in jail or prison and 43% overall received at least one of their tattoos in a non-professional setting that was not jail or prison. In regards to piercing history, 48% reported a history of piercing and most (65%) had one to two piercings. Twenty-one percent of the sample were men who reported a history of sex with men, 26% of the sample reported 26–100 lifetime sexual partners and 22% reported that they had >100 sexual partners.
There were significant associations (P-value <0.05; odds ratios with 95% CIs are in Table 1) between anti-HCV status and the level of education completed (less than high school vs. greater than or equal to high school education; 26.4 vs. 13.8%), history of tattoos (yes vs. no; 26.0 vs. 14.5%) and ever been in jail (yes vs. no; 19.7 vs. 10.8%). Regarding drug use, there was a negative association between anti-HCV and ever snorting cocaine (ever snorted cocaine vs. never snorting drugs; 11.8 vs. 24.5%). In contrast, there was a positive association between anti-HCV status and exclusive use of crack cocaine but not powder cocaine (ever used crack cocaine vs. ever used other drugs other than powder or crack cocaine; 31.6 vs. 15.0%). There were no significant associations between anti-HCV status and having shared specific implements for smoking crack or snorting cocaine.
Table 2 details the results of Model 1 examining the associations of snorting or smoking drugs and HCV antibody while controlling for sociodemographics and factors such as tattooing, incarceration and sexual history for the entire sample. The negative association in the model between snorting cocaine and HCV antibody among people with no history of injection drug use (adjusted odds ratio (AOR): 0.39; 95% CI: 0.21–0.73) was statistically significant. However, there was borderline significance (0.05 < P < 0.10) for having less than a high school education (AOR: 1.80; 95% CI: 0.98–3.31), ever being in jail (AOR: 1.91; 95% CI: 0.93–3.67) or ever being tattooed (AOR: 1.86; 95% CI: 0.94–3.67). There was no significant association of sharing snorting equipment with persons with HCV antibody (AOR: 1.02; 95% CI: 0.39–2.69) among those who had ever snorted cocaine in Model 2. In this model, ever smoking crack cocaine was negatively associated with HCV antibody positivity (AOR: 0.28; 95% CI: 0.09–0.88). There was neither a significant association of crack pipe sharing (AOR: 1.27; 95% CI: 0.55–2.92) nor of having burns or blisters from smoking crack (AOR: 0.74; 95% CI: 0.35–1.56) with HCV antibody among those who had ever smoked crack cocaine in Model 3. There was a significant negative association between ever snorting cocaine and HCV antibody positivity (AOR: 0.26; 95% CI: 0.12–0.53) in Model 3. Model 4, which examined only tattooed study participants, showed no association between receiving tattoos in non-professional (AOR: 1.15; 95% CI: 0.17–8.02) or jail/prison settings (AOR: 0.21; 95% CI: 0.02–2.34) and HCV antibody status.
Neither our bivariate nor multivariate analyses found a positive association between sharing non-injection drug equipment and the odds of being anti-HCV positive. Instead, we found an unexpected inverse association between anti-HCV status and snorting heroin, cocaine or methamphetamine, which was statistically significant in our bivariate analysis and in some instances in our multivariate analyses. There was also a negative association between smoking crack cocaine and anti-HCV status in the multivariate model that looked only at powdered cocaine users; a similar association was seen between snorting powdered cocaine and HCV antibody positivity in the model focusing on crack cocaine smokers. We do not believe that snorting or smoking drugs reduces the risk of becoming infected with HCV. A possible explanation is reporting bias, specifically that some participants who had injected drugs and who are at increased risk of HCV infection may have been uncomfortable reporting any drug use (injection or non-injection). Under-reporting of injection drug use is plausible given the high overall prevalence (17%) of anti-HCV in this sample of persons who reported no injection drug use.
We found consistent with other studies 4,6,7,13 that homeless and marginally housed non-injection users have a higher prevalence of HCV than the general population (17% in our study vs. 1.6% in a sample of the US population participating in the National Health and Nutrition Examination Survey [NHANES] 1999–2002).4 In addition, our study demonstrated substantial prevalence of powdered and smoked drug consumption among this non-injection population.
The relationship between anti-HCV positivity and exclusive crack use in bivariate analysis is likely due to the interaction among the separate drug snorting and drug smoking variables. The fact that crack users who do not use cocaine had a higher risk of being seropositive for HCV antibody could indicate that their exclusive crack use is proxy for some unmeasured variable in our analysis that could increase HCV risk. Exclusive crack cocaine users are more likely to be African-American and to have less than a high school education (data not shown). As our analysis focused on biologically plausible methods of HCV transmission and found no association between anti-HCV positivity and sharing crack pipes or having burns or sores due to smoking crack, it is likely that this association is due to residual confounding.
We found that ever being tattooed was associated with increased odds of being anti-HCV positive in our bivariate but not our multivariate analysis. Only 28% of those who had tattoos received them exclusively in commercial settings and homeless or marginally housed people may be more likely to receive tattoos in unsanitary conditions that increase blood exposure to HCV. Tattooing in this population could also serve as a marker for HCV risk behavior such as undisclosed injection drug use.
There was an association between education level and being anti-HCV positive in the bivariate analysis but not the multivariate model. This is consistent with other research that demonstrated an increasing prevalence in HCV infection with decreased educational status.3,14,4 Other studies have shown no statistically significant differences between the level of education and HCV status.13,27 The association between educational attainment and HCV infection status suggests that there are unmeasured factors associated with lower educational status that are associated with increased risk of HCV infection among non-injection drug users.
There was also a trend for older participants in our sample to have a higher prevalence of anti-HCV positivity, although this was not statistically significant in the bivariate or multivariate analysis. Previous research has demonstrated that most Americans who are anti-HCV positive were born between the 1940s and 1960s while there is decreased prevalence in adolescents and younger adults.4 Our study results are consistent with these findings.
Finally, we did not find a significant association between being anti-HCV positive and having an increasing number of sexual partners. However, there was a trend towards increased risk for being anti-HCV positive in the bivariate analysis that was not replicated in the multivariate analysis. This suggests that there may be factors within the measurement of sexual partners that could be associated with an increased rate of HCV infection, and a recent study indicated a possible correlation between increasing numbers of sexual partners and the possibility of being an injection drug user.37
Although this study did not show a significant association between sharing non-injection implements and anti-HCV status, the prevalence of anti-HCV was high in this sample of homeless and marginally housed persons and warrants further examination. While public health strategies for reducing HCV transmission have focused mostly on injection drug users, these data may indicate a benefit in targeting marginally housed people for routine HCV testing and subsequent treatment to further decrease HCV morbidity and transmission.
As noted above, behavioral information was based on self-report, and under-reporting of injection drug use in conjunction with the denial of snorting or smoking drugs could have led to the protective odds ratios noted for these behaviors. Other studies have reported attempts at verification such as examining participants for track marks.13 Although this study had no barriers to participation based on injection status, as noted above, participants may have misrepresented both their injecting drug use and snorting or smoking drugs because of the illicit nature or because of stigma associated with these activities. In addition, recall bias for behaviors reported over a lifetime may also have biased the results to the null. Because this was a cross-sectional study, we have limited evidence to evaluate causality.
This work was supported by the National Institutes of Mental Health Grant 54907 and D.R.B. received additional support from the National Institutes of Mental Health Grant K-24 87227; the National Institutes of Mental Health had no involvement in study design, collection, analysis and interpretation of the data, nor in the decision to submit the paper for publication.
We thank the National Institutes of Mental Health for funding provided by the National Institutes of Mental Health Grant 54907 and additional support received by David R. Bangsberg from the National Institutes of Mental Health Grant K-24 87227.