1. Background
Infection with hepatitis C virus (HCV) is increasingly recognized as a major global health problem (1). It has been estimated that 2% to 3% of the global population (170 million people) are now infected with HCV (2). By the 1970’s or earlier, HCV was established in some populations of people who inject drugs (PWID) (3), with estimates of nearly 13.2 million PWID worldwide (4), about 50% of whom seem to have been exposed to HCV infection (5).
Iran has a long established history of illicit drug use. However, a rapid change in the pattern of drug use, with an increase in injecting drug use (mostly heroin), has been observed (6). Evidence suggests that Iran has the highest rate of opioid use globally (6, 7), and according to the national survey of drug use in Iran, at least 1.12 million people are dependent on illicit drugs, about 5% of whom are current users (6).
Today, injecting drug use is a major and perhaps the most important risk factor for the increasing transmission of HCV infection in the Iranian population (8). The prevalence of HCV infection in PWID ranges from 20% to 90% in different studies (5, 9-17). High-risk injection behaviors are the leading cause of HCV infection among PWID (18). The primary risk factor for HCV infection in PWID is using a needle or syringe, which has been already used by another user (sharing syringes) (13, 15, 19-23). Sharing other injection equipments (eg, cookers, swabs, tourniquets, and mixing water) is also common among PWID (24-28).
Other identified risk factors for HCV in PWID include history of imprisonment (13, 15, 16), drug injection more than the daily frequency (29, 30), history of tattooing (15), and duration of injecting drug use (13). However, there is no recent information on HCV prevalence in PWID in Kermanshah, Iran. The purpose of this study was to measure the prevalence of HCV infection and determine the risk factors for HCV among PWID in Kermanshah.
2. Methods
2.1. Design and Participants
In this cross sectional study, conducted between January and April 2017, samples were recruited from 2 drop-in centers, affiliated to Kermanshah University of Medical Sciences, as well as related community outreach sites. Using snowball sampling, males (above 18 years), who self-reported at least 1 drug injection in the month before the interview, resided in Kermanshah, and provided a written consent form, were recruited in the study. The participants were stratified, based on whether or not they had attended harm-reduction programs regularly (at least 4 visits in the past month) and received harm-reduction kits.
2.2. Questionnaire
Trained interviewers collected data by completing a biobehavioral questionnaire during face-to-face interviews. The questionnaire consisted of 3 sections including demographic information, drug use history, and risky behavior information over the past month before the interview. Prior to administration, the questionnaire content was discussed among 10 experts in fields of epidemiology, behavioral sciences, and harm reduction. Kappa coefficient and intraclass correlation coefficient (ICC) were measured to evaluate the reliability of the questionnaire. ICC ranged from 0.86 to 1, and Kappa coefficient was 0.9-1 for all the variables.
2.3. Ethical Considerations
For confidentiality, no identifying information was collected from the participants. Through the consent procedure, the participants were informed about the objectives, risks, and advantages of participating in the study. They were allowed to withdraw from the study at any time.
2.4. Statistical Analysis
Continuous variables are expressed as mean ± standard deviation, and categorical variables are presented as number and percentage. Logistic regression analysis was used to determine the association between HCV status and the associated factors, reported as odds ratio (OR) and 95% confidence interval (CI). Variables with P–value below 0.2 were entered into the multiple regression analysis. All data analyses were performed using SPSS version 21 (IBM Corp, Armonk, NY).
2.5. Serological Assay
HCV infection test was performed on venous blood samples, collected from subjects after completing the questionnaire. Serum samples were tested for anti-HCV antibodies, using a rapid chromatographic immunoassay for qualitative detection of HCV antibodies in the serum, known as HCV rapid test device (ABON BioPharm Hangzhou Co., Ltd.; sensitivity, > 99.53%; specificity, 99.78%). Positive samples according to the HCV rapid test were considered anti-HCV positive. All the participants with positive HCV antibodies were referred to a behavioral consultation center, affiliated to Kermanshah University of Medical Sciences for HCV RNA testing via reverse transcription-polymerase chain reaction (RT-PCR) as a confirmatory test. Follow-up was not part of the present study, and we did not collect the subjects’ PCR results.
3. Results
3.1. Baseline Demographics
A total of 606 male PWID were recruited in the study. The mean age of the participants was 36.7 ± 8.5 years (range, 18 - 65 years), and the mean (SD) years of education was 8.04 (3.8) years. In total, 270 (44.6%) subjects had attended needle and syringe programs (NSPs) at least once a week during the past 4 weeks (regular attendance group). About half of the participants (53.3%) were unemployed, and 36.1% were homeless (Table 1).
Table 1.Demographic Characteristics of the Participants Based on HCV Antibody Status
| Characteristics | Number (%) | HCV Negative (n, 274) No (45%) | HCV Positive (n, 332) No (55%) | P Value |
|---|---|---|---|---|
| Age, group (years) | ||||
| < 30 | 119 (19.6) | 89 (32.5) | 30 (9.0) | 0.000 |
| 30 - 39 | 281 (46.4) | 107 (39.1) | 174 (52.4)a | |
| 40 - 49 | 156 (25.7) | 51 (18.6) | 105 (31.6)a | |
| ≥ 50 | 50 (8.3) | 27 (9.9) | 23 (6.9)a | |
| Education | ||||
| Illiterate | 49 (8.1) | 26 (9.5) | 23 (6.9) | 0.004 |
| Elementary school | 125 (20.6) | 39 (14.2) | 86 (25.9)a | |
| Middle school (up to grade 9) | 90 (14.9) | 37 (13.5) | 53 (16.0) | |
| High school (up to grade 12) | 314 (51.8) | 158 (57.7) | 156 (47.0) | |
| University | 28 (4.6) | 14 (5.1) | 14 (4.2) | |
| Marital status | ||||
| Single | 382 (63.0) | 162 (59.1) | 220 (66.3) | 0.000 |
| Married | 98 (16.2) | 70 (25.5) | 28 (8.4)a | |
| Divorced | 105 (17.3) | 32 (11.7) | 73 (22.0)a | |
| Separated | 21 (3.5) | 10 (3.6) | 11 (3.3) | |
| Occupation | ||||
| Employed | 283 (46.7) | 142 (51.8) | 141 (42.5) | 0.022 |
| Unemployed | 323 (53.3) | 132 (48.2) | 191 (57.5) | |
| Homelessness | ||||
| Yes | 219 (36.1) | 63 (23.0) | 156 (47.0) | 0.000 |
| No | 387 (63.9) | 211 (77.0) | 176 (53.0) | |
| Regular attendance of harm-reduction programs | ||||
| Yes | 336 (55.4) | 149 (54.4) | 187 (56.3) | 0.681 |
| No | 270 (44.6) | 125 (45.6) | 145 (43.7) |
aThere is a statistical significance with the first group (P< 0.05).
The mean (SD) duration of drug use and injecting drug use was 17.1 (8.1) and 7.3 (6.4) years, respectively. Among the participants, 77.6% had a history of imprisonment, 62% had a history of tattooing, and 55.3% had a history of sharing injecting equipments in the month before the interview. The minority of the participants (1.8%) reported sharing needles and syringes within the past month (Table 2).
Table 2.HCV Risk Factors in the Participants Based on HCV Antibody Status
| Characteristics | Number (%) | HCV Negative (n, 274) No (45%) | HCV Positive (n, 332) No (55%) | P Value |
|---|---|---|---|---|
| Imprisonment | ||||
| No | 470 (77.6) | 171 (62.4) | 299 (90.1) | 0.000 |
| Yes | 136 (22.4) | 103 (37.6) | 33 (9.9) | |
| Number of injections per day | ||||
| < 2 | 221 (36.5) | 160 (58.4) | 61 (18.4) | 0.000 |
| ≥ 2 | 385 (63.5) | 114 (41.6) | 271 (81.6) | |
| History of tattooing | ||||
| No | 230 (38.0) | 147 (53.6) | 83 (25.0) | 0.000 |
| Yes | 376 (62.0) | 127 (46.4) | 249 (75.0) | |
| Sharing equipments within the past month | ||||
| No | 266 (43.9) | 172 (62.8) | 94 (28.3) | 0.000 |
| Yes | 340 (56.1) | 102 (37.2) | 238 (71.7) | |
| Needle/syringe sharing within the past month | ||||
| No | 595 (98.2) | 272 (99.3) | 323 (97.3) | 0.123 |
| Yes | 11 (1.8) | 2 (0.7) | 9 (2.7) | |
| Age at first drug use (years) | ||||
| < 25 | 509 (84.0) | 214 (78.1) | 295 (88.9) | 0.000 |
| ≥ 25 | 97 (16.0) | 60 (21.9) | 37 (11.1) | |
| Age at first drug injection (years) | ||||
| < 25 | 158 (26.1) | 61 (22.3) | 97 (29.2) | 0.063 |
| ≥ 25 | 448 (73.9) | 213 (77.7) | 235 (70.8) |
3.2. Anti-HCV Prevalence
HCV antibody testing of 606 samples showed that 54.8% (n, 332; CI, 50.8% - 58.7%) were positive for exposure to HCV infection. Among 332 people who were positive for HCV antibodies, 251 (75%) self-reported their HCV status. Only 12 (4.8%) participants self-reported positive HCV, 11 (4.4%) self-reported negative HCV, and the remaining 228 (90.8%) reported not knowing their current HCV antibody status. Among 453 participants who self-reported their HCV status, 93.4% reported not knowing their current HCV antibody status. Only 12 (2.6%) samples in our study reported positive HCV, and 18 (4%) samples reported being currently HCV negative.
3.3. Risk Factor Analysis
In the bivariate analysis, several variables were identified as factors correlated with the presence of HCV antibodies. These variables included 2 or more injections per day, a longer duration of drug injection, history of tattooing, history of shared equipments, needle and syringe sharing within the past month, history of imprisonment, age at first drug use, and age of first drug injection (P < 0.2) (Table 3).
Table 3.Multiple Logistic Regression Analysis of Factors Associated with HCV Status in PWID in Kermanshah, Iran
| Characteristics | Unadjusted OR (95% CI) | P Value for Unadjusted OR | AOR (95% CI) | P Value for AOR |
|---|---|---|---|---|
| Occupation | ||||
| Employed | 1 | 1 | ||
| Unemployed | 1.45 (1.05 - 2.01) | 0.022 | 0.89 (0.57 - 1.37) | 0.600 |
| Regular attendance in NSPs | ||||
| Yes | 1 | |||
| No | 0.92 (0.67 - 1.27) | 0.632 | ||
| Homelessness | ||||
| No | 1 | 1 | ||
| Yes | 2.96 (2.08 - 4.23) | 0.000 | 1.48 (0.93 - 2.34) | 0.095 |
| Number of injections per day | ||||
| < 2 | 1 | 1 | ||
| ≥ 2 | 6.23 (4.31 - 9.00) | 0.000 | 4.27 (2.80 - 6.53) | 0.000 |
| History of tattooing | ||||
| No | 1 | 1 | ||
| Yes | 3.47 (2.46 - 4.89) | 0.000 | 2.54 (1.69 - 3.81) | 0.000 |
| Sharing equipments within the past month | ||||
| No | 1 | 1 | ||
| Yes | 4.27 (3.03 - 6.01) | 0.000 | 3.77 (2.49 - 5.71) | 0.000 |
| History of imprisonment | ||||
| No | 1 | 1 | ||
| Yes | 5.45 (3.53 - 8.43) | 0.000 | 2.36 (1.42 - 3.92) | 0.001 |
| Needle/syringe sharing within the past month | ||||
| No | 1 | 1 | ||
| Yes | 3.78 (0.81 - 17.68) | 0.090 | 1.16 (.23 - 5.87) | 0.853 |
| Age of first drug use (years) | ||||
| < 25 | 1 | 1 | ||
| ≥ 25 | 0.44 (0.28 - 0.69) | 0.000 | 1.15 (0.64 - 2.06) | 0.639 |
| Age of first drug injection (years) | ||||
| < 25 | 1 | 1 | ||
| ≥ 25 | 0.69 (0.47 - 1.005) | 0.053 | 0.72 (0.45 - 1.14) | 0.166 |
Abbreviations: OR: odds ratio; AOR: adjusted odds ratio (all variables with P value < 0.2 entered the model).
Multiple logistic regression analysis revealed factors associated with anti-HCV infection (Table 3). Adjusted OR for people reporting no shared equipments within the past month was 3.77 times higher than the OR of people who reported no shared equipments (P = 0.000 < 0.001). The adjusted OR of positive anti-HCV among those injecting twice or more per day was 4.33 (P = 0.000 < 0.001), compared to people who reported injections only once a day (or less). Moreover, both history of tattooing and history of imprisonment were significant in the final model.
4. Discussion
In the present study, we investigated factors correlated with the serological prevalence of anti-HCV among male PWID in Kermanshah, Iran. In line with previous research, we found a significant association between HCV antibody positivity and duration of drug injection, history of tattooing, history of sharing equipments within the past month, history of imprisonment, and frequency of injection per day (13, 15).
4.1. Prevalence of HCV Antibodies
A recent national estimate of HCV prevalence among PWID was 51.46% (95% CI, 34.30 - 68.62) (31). In the present study, we found an HCV antibody prevalence of 54.8% (95% CI, 50.8 to 58.7) in the PWID samples. An earlier study examining HCV among PWID in Isfahan, Iran reported that the prevalence of HCV antibodies was 47.1% (15). Previous research has established that the prevalence of HCV infection in PWID typically ranges between 20% and 90%. However, the rates vary depending on the geographical location, duration of exposure to injecting drug use, number of injections per day, and sharing needles, syringes, or injecting equipments (5).
The high prevalence of HCV antibodies in PWID establishes this population as one of the most important target groups for HCV prevention, treatment, and harm-reduction programs because of their important role in HCV transmission. The world health organization (WHO) has recently introduced global elimination targets for HCV by 2030 (32). Therefore, promotion of HCV treatment, together with sustained harm-reduction interventions, is crucial to achieving these goals in Iran.
4.2. Variables Correlated with HCV
The present findings indicated that HCV exposure is associated with history of imprisonment, history of tattooing, sharing equipments within the past month, and higher frequency of injections per day. A key finding of this study was the association between recent equipment sharing and risk of HCV transmission. This finding is supported by research performed in Tehran, Iran, where sharing injecting equipments was identified as a risk factor for HCV infection (13).
Previous research has also identified history of imprisonment as one of the major risk factors for HCV infection in Iran and around the world (15, 16, 33, 34). Many PWID with a history of imprisonment have poor health. Therefore, prison screening for infectious diseases, such as HCV, and provision of health education and prevention programs are essential in this population. There is also evidence that treatment for HCV in prison settings is achievable and cost-effective (35, 36).
Multiple studies have shown a significant association between history of tattooing and HCV infection. The present study was consistent with previous research from North America, Australia, and Italy, where the odds of being HCV positive increased by 3.4, 2.7, and 1.91, respectively in cases reporting a history of tattooing inside prison (37-39). Moreover, our findings could provide further evidence on the significant association between injecting frequency and HCV infection (29, 30). This reinforces the need to provide PWID with targeted education about HCV transmission and to increase access to sterile injecting equipments (not only sterile needles and syringes) in harm-reduction programs.
There are some limitations in the present study. Although this is a cross sectional study, it included more than 1 recruitment strategy to identify and enroll eligible participants. While the study sample is limited to male PWID from Kermanshah, it is not a random PWID sample. Therefore, the results cannot be generalized to all male drug injectors in Kermanshah or more broadly in Iran. The cross sectional design of the study also prevented the precise analysis of sequential association between risky behaviors and anti-HCV status. Moreover, all behavioral data are self-reported in this study, and therefore, there may be some recall biases; however, limiting a large part of the data to the past month could decrease the bias. Overall, self-report of behaviors has been previously shown to be of adequate reliability and validity in Iranian opiate users (14, 40).
4.3. Conclusion
To reduce the high prevalence of HCV infection among male PWID, it is necessary to provide optimal harm-reduction programs, especially NSPs. If we are to ensure that male PWID can avert new HCV infections and reinfections, increasing harm-reduction coverage and HCV treatment is a priority. Further studies using larger sample sizes and female injectors are required to fully understand the HCV prevalence and risk factors in other parts of Kermanshah.
