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Prevalence and high risk behaviours associated with HCV testing among people who inject drugs: a systematic review and Meta-analysis

Abstract

Background

Hepatitis C diagnosis could be a gateway to behavioral change and subsequent decline in transmission among people who inject drugs (PWIDs). We assessed the association between the social determinants of PWID, their risk behaviors and hepatitis C testing.

Methods

We searched for studies in English published before May 1, 2020, on PubMed, Scopus, Cochrane, and Web of Science to identify primary studies on the factors associated with hepatitis C virus (HCV) testing among PWID. After reviewing for study duplicates, the full-text of selected articles were assessed for eligibility using Population, Intervention, Comparator, Outcomes (PICO) criteria. i) population: individuals who report injecting drugs; ii) intervention: HCV testing in the past year; iii) comparator: PWIDs who did not have an HCV test; iv) outcome: HCV testing among PWIDs and v) study type: cross-sectional, cohort, and case-control studies. Two independent reviewers (author BA and AB) chose the references in a two-phased monitoring process. The authors gathered data from selected papers, including the surname of the first author, publication date, participant demographic data (age, sex, and level of education) and other characteristics like previous HCV testing, past treatment attempts, duration of injecting drug use and condomless sex. We used fixed and random-effects meta-analysis models to estimate the pooled prevalence, pooled odds ratio (OR), and 95% confidence intervals. The data were analyzed using Stata 12.0 software.

Results

After a detailed assessment of over 12,000 articles, a total of 16 studies containing 38,952 participants met the eligibility criteria. Our findings showed a pooled prevalence rate of 61.01% (95% CI, 34.65–84.32%) for recent HCV testing among PWIDs. Being female (OR = 1.69, 95%CI = 1.13, 2.26), aged > 30 years, (OR = 2.61, 95%CI = 1.66–3.56) having past treatment attempt (OR = 2.24, 95%CI = 1.80–2.68), and reporting a previous test (OR = 2.03, 95%CI = 1.23–2.82). were significantly associated with having a recent HCV test.,,. Finding of present study was that unprotected sex had a negative association with HCV testing. Those PWIDs who had unprotected sex were 0.56 times less likely to have completed HCV testing during last year (OR = 0.56, 95%CI = 0.33–0.78).

Conclusion

Prevention programs that address age > 30 years, being female, past treatment attempt, previous testing of safe sexual practices, are strongly recommended to prioritize HCV risk reduction strategies.

Background

Hepatitis C virus (HCV) infection is a major public health problem, causing a preventable liver-related morbidity and mortality globally [1,2,3]. The World Health Organization (WHO) has defined targets for HCV treatment and diagnosis, representing a step towards the goal of elimination by 2030 [4]. Nevertheless, rates of HCV testing, treatment, and linkage to care are still low in many places around the world [5]. A number of social factors impact on treatment access including unstable housing, social stigma, health care providers’ attitudes, criminalization of drug use, and gender [6,7,8,9]. Historically, HCV infection has been described as a silent epidemic, with estimations suggesting that half of those infected are not currently aware of their HCV status [10]. People who inject drugs (PWIDs) carry a higher HCV burden than other people, with HCV prevalence in this group being estimated at over 50% [11, 12]. The criminalization of drug use and the political response means custodial settings have high rates of HCV prevalence [13,14,15].

The sharing of previously used injecting equipment means that PWID are the population most at risk for HCV infection in nearly all middle and high-income countries. Undiagnosed and untreated HCV infection can cause cirrhosis, hepatic decompensation, liver cancer, and death [16]. HCV diagnosis itself could be a helpful strategy [17] in behavioral change [18] and producing a decline of HCV transmission [19, 20].

As part of the elimination strategy, WHO suggests regular testing of PWIDs (at least yearly) [21]. However, such regular HCV testing by active drug users relies on many factors, for example, heightened levels of risk awareness among PWID, availability of testing sites and drug- treatment workers who integrate testing as a normal part of their work [22]. Low rates of HCV treatment uptake among PWIDs have been attributed to barriers at the provider, patient and systems levels. Not least of which have previously been treatment complexity together with limited capacity, the side effects from interferon-based treatment, social stigma and discrimination which may influence the willingness of physicians to provide treatment for PWIDs [23,24,25].

In addition to financial barriers, other barriers that might prevent PWIDs from accessing HCV treatment and testing include the high levels of discrimination and stigma that may exist inside of conventional healthcare settings, which may influence on patient-provider relationships and the willingness on the part of physicians to treat PWIDs [22, 25].

Despite evidence that the availability of direct acting antivirals has made HCV testing and treatment more accessible [26] PWIDs continue miss out. Making HCV (anti-HCV) and verifying chronic HCV infection by RNA testing are the essential first steps along the treatment cascade [27]. The aim of this investigation was to clarify the contributing factors for engaging PWIDs in HCV testing.

Methods

The present study was conducted based on the instructions in Protocols of Systematic Reviews and Meta-Analyses (PRISMA) [28, 29].

Search strategy and study selection

The process of our study selection is presented in Fig. 1.

Fig. 1
figure 1

PRISMA flow diagram

We selected 8348 papers from across 4 databases, and included additional manual searches of the reference lists for papers published before May 1, 2020. To identify and select studies two independent researchers (A.B. and B.A.) reviewed the electronic databases of PubMed, Scopus, Web of Science, and Cochrane independently (Table 1).

Table 1 search strategy

We included English language papers in the study, and also, we considered limitations such as time and geographic items. We reviewed papers twice based on the abstract and on the relevancy to the subject.

Inclusion criteria based on PICOS:

  • Population: Individuals who report injecting drugs

  • Intervention: HCV testing in the past year

  • The Comparison Group: PWIDs who did not conduct HCV testing

  • Outcomes: HCV testing among PWIDs.

  • Study design: We included cross-sectional, cohort, and case-control studies.

We excluded qualitative studies, secondary studies, systematic reviews and, meta-analysis studies, and also, we excluded non-English language papers from our study.

Data extraction and study quality assessment

Two independent researchers (AB and BA) reviewed and assessed the papers applying a standardized data collection form. Any contradictions between the two researchers were eliminated by discussing with two other members of the research team (EA and YF). We used Microsoft Excel software for data extraction and management. Two independent reviewers (author BA and AB) chose the references in a two-phased monitoring process. First, we eliminated duplicated titles/abstracts (89% agreement) according to the criteria one through three mentioned below. Second, titles/abstracts that met these initial criteria were selected for full-text review based on the inclusion criteria (96% agreement).

The authors gathered data from selected papers, including the surname of the first author, publication date, participant demographic data (age, sex, and level of education) and other characteristics like previous HCV testing, past treatment attempts, duration of injecting drug use and unprotected sex. The Newcastle-Ottawa Scale (NOS) [30] proposed by the Cochrane Collaboration [31] was used to evaluate the quality of the reviewed papers (Table 2).

Table 2 main characteristic of included studies

To evaluate the quality of papers included in the meta-analysis, we applied a modified version of NOS. This was used to evaluate statistical quality, sample representativeness, sample size, and comparability between people were the domains used for the NOS when evaluating the quality of individual studies. We applied agreement beyond chance (unweighted kappa) for evaluating agreement between the two authors (BA and AB) during the quality assessment. The levels of poor, slight, fair, moderate, substantial, and almost perfect levels of agreement were showed by the values 0, 01–0.02, 0.021–0.04, 0.041–0.06, 0.061–0.08, and 0.081–1.00, respectively [48].

Data synthesis and statistical analysis

The present meta-analysis was conducted by generating pooled odds ratios (OR) and the 95% confidence intervals on recognizing factors associated with HCV testing among PWID. We computed the OR applying a 2*2 table, and we considered OR < 1 as a positive association between HCV testing and the target variable. An OR >1 (as the statistical threshold for assessing the relationship between outcome variables and expositive variables) suggests a protective relationship between variables and vice versa. To evaluate the lack of correlation between studies, we applied Q test with a P value < 0.05 and I2 statistics with a cutoff of ≥50%. We assessed 95% confidence intervals for I2 where we considered negative values as zero. We applied the random-effects model to calculate pooled estimation, considering the different sampling methods of the studies. To identify any publication bias, we used Begg’s and Egger’s publication bias approach both in graphical and statistical manners [49, 50]. P-values of less than 0.05 were considered significant. We demonstrated the association between social and demographical determinants by an OR and 95% CI, and showed the results in forest plots. For data analysis, we conducted the meta and metabias commands in STATA version 13.0 (STATA Corporation, College Station, TX.

Results

Study characteristics

After careful evaluations of the extracted citations, 16 studies were included [32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47]. Selected studies were from four WHO regions (five from Region of the Americas [n = 15,795 participants], five from the European Region [n = 6870 participants], three from South-East Asia [n = 13,661 participants] and three from the Western Pacific region [n = 2626 participants]. The USA had the highest number of reports (4 studies, 15,132 participants). Considering country income level, 12 studies (n = 23,678) were conducted within high-income countries, 1 study (n = 427) within upper-middle-income countries and three studies were (n = 14,847) from a lower middle-income country.

Results of the meta-analysis

In Table 2, the key characteristics of the included studies for factors associated with HCV testing uptake among PWIDs are presented. The impact can be inferred through plots 2–9.

Figure 2 indicates the association between being age > 30 years and HCV testing among PWIDs. Our findings show PWIDs aged > 30 years were 2.61 times more likely to report having had an HCV test during last year (OR = 2.61, 95%CI = 1.66–3.56).

Fig. 2
figure 2

the association between age > 30 years with HCV testing uptake among PWID

As illustrated in Figs. 3, and 4, there were no significant associations found with HCV testing among PWIDs and their duration of injecting (OR = 1.92, 95%CI = 0.50–3.33), and high school education (OR = 1.55, 95%CI = 0.32–2.78).

Fig. 3
figure 3

the association between duration of injecting drug use with HCV testing uptake among PWID

Fig. 4
figure 4

the association between had high school education with HCV testing uptake among PWID

Figure 5 shows the positive impact of being female and HCV testing among PWIDs, and the overall heterogeneity was about 0%. The pooled effect size has a respective positive impact and the lower boundary is about 1.13, and the higher is 2.26. The OR indicated a positive and effective role that being female has on HCV testing among PWIDs. Participants who were female were 1.69 times more likely to test for HCV in the last 12 months (OR = 1.69, 95%CI = 1.13, 2.26).

Fig. 5
figure 5

the association between being female with HCV testing uptake among PWID

Additionally, Fig. 6 indicates a significant correlation between past treatment attempts and HCV testing among PWID. PWIDs in this situation were 2.24 times more likely to have had an HCV test in the previous 12 months than PWIDs who did not report any past treatment attempts (OR = 2.24, 95%CI = 1.80–2.68).

Fig. 6
figure 6

The association between past treatment attempt with HCV testing uptake among PWID

Another finding from our data was previous testing had a positive association with HCV testing. Those PWIDs who had a previous test were 2.03 times more likely to have completed a recent HCV test (last 12 months) (OR = 2.03, 95%CI = 1.23–2.82) (Fig. 7).

Fig. 7
figure 7

The association between previous HCV testing with HCV testing uptake among PWID

Finding of present study was that unprotected sex had a negative association with HCV testing. Those PWIDs who had unprotected sex were 0.56 times less likely to have completed HCV testing during last year (OR = 0.56, 95%CI = 0.33–0.78) (Fig. 8).

Fig. 8
figure 8

The association between had unprotected sex with HCV testing uptake among PWID

Figure 9 shows a significant pooled prevalence of 61.01% (95% CI, %34.65-%84.32) for the prevalence of HCV testing among PWIDs.

Fig. 9
figure 9

The prevalence of HCV testing uptake among PWID

To identify the probable publication bias, the Egger’s test and the graph were performed. Considering the symmetry assumption, there was no significant publication bias in the reviewed studies selected for inclusion. As regards the funnel plot, the distribution of the articles was not oriented and for most of them, it was identical confirming no publication biases observed in our study. The publication bias test indicates considerable bias based on Eggers test (coefficient = 3.66, P value < 0.001) (Fig. 10).

Fig. 10
figure 10

The Eggers plot for detect publication bias among studies

Discussion

This meta-analysis study aimed to explore factors associated with recent HCV testing among PWIDs. The prevalence of recent HCV testing uptake was high. Past 12 months testing for HCV was associated with being aged > 30 years, being female, having a past treatment attempt and reporting previous HCV testing. HCV testing was reported by 61.01% of the study participants which could indicate enhanced access to harm reduction interventions. Many drug treatment services require initial HCV screening for PWIDs and such services are in the perfect position to conduct long-term follow-up and monitoring of HCV testing in this population.

Moreover, a strong predictor for a recent HCV test was being over the age of30 years. Given the correlation between a longer duration of drug injecting and the increased odds of high-risk injecting. This may reflect an association between increased HCV test-taking and longer injecting history. However, studies also show that HCV infection can also occur in the early stages of people’s injecting careers [51]. While the risks are high in this group evidence suggests they ae also more likely to be conscious of the advantages in HCV testing [52, 53]. In addition, while recent HCV testing and female gender were independently correlated the risks are more challenging to manage. Sex work and injection-assistance [54] have been shown to increase vulnerability to HCV infection [38].

Addressing injecting couple’s relationships in terms of developing and conducting HCV testing and considering gender-specific needs are necessary if increased HCV testing is to be achieved [55]. Our study suggests that accessing drug treatment by PWIDs is a determining factor in recent HCV test-taking. In line with this result, other studies have highlighted the advantages of drug treatment in facilitating access to healthcare services for PWIDs [56, 57] especially HIV and HCV treatment programs [58]. However, when excluding treatment from the variable definition, drug treatment and recent HCV testing were not associated and this may be a result of inadequate staff training on the risks and transmission methods of HCV.

There is evidence that providing education programs for drug treatment staff aimed at improving the HCV awareness i is beneficial in promoting HCV services among PWID [59]. HIV service integration highlights the need for developing strategies due to increased demands [9, 60]. Such plans could help to improve the HCV-related knowledge of the general population, which in turn results in eliminating targets. Network-based recruitment and the use of PWID peer facilitators might enhance the detection rates of HCV cases [61,62,63]. Accordingly, network referral strategies could be combined to increase HCV testing and treatment at the community level.

Furthermore, there was an independent association between confirmatory PCR testing and undergoing HCV testing within the past 12 months. Enhanced awareness of the need for confirmatory testing in healthcare providers and PWIDs is essential if WHO elimination goals are to be achieved. Approximately 33% of PWIDs with histories of active HCV infection had received HCV professional surveys (e.g., liver biopsy or FibroScan1) before being introduced to interferon-free regimens. However, there is a significant gap between healthcare engagement and the receipt of HCV treatment in the era of interferon-based therapy. It is reported that 1–2% of PWIDs received treatment per year. Additionally, a cumulative therapy of 10% at the end of 2011 are extensively in line with these data [39]. Consistent with prior research [33, 39] we found that having unprotected sex was negatively associated with having been tested for HCV. There is a data discrepancy on HIV-related counseling programs and undertaking the relevant test in terms of high-risk sexual behaviors. A tremendous body of literature suggested a major decline in claiming multiple partnerships and unprotected sexual relationships. On the other hand, some investigators [64,65,66], documented either adverse or poor effects of test-taking on behavioral modifications [67, 68]. Sex-related high-risk behaviors, such as the lack of using sexual protection tools and fisting, which in turn, could be mucosal traumatic and result in bleeding. These factors have also been suggested to be related to contracting HCV risk [69,70,71]. It is still debatable whether bleeding plays an essential role in the transmission of HCV. Some investigations have detected HCV in seminal and rectal fluids in males who were infected with HIV and supported that such fluids could interfere with the transmission of HCV [72, 73].

Limitations and strengths of the study

The study limitations include first, relying on HCV self-reports (study samples might have failed to completely percept the HCV diagnosis approach, i.e., comprising 2 test forms, the reported data may be biased by overestimating). Although not commonly implemented such limitations could be eliminated by achieving confirmation of prior HCV testing. Second, most of the included studies were cross-sectional meaning causal and temporal relationships between risk behavior and HCV testing are not possible. However, this meta-analyses may enhance the statistical inference of analyses and incresase the reliability of the evidence. Third, few studies investigated the association between risk behavior and HCV testing, emphasizing this gap in the literature. Also, since we did not interfere with the setting of independent and dependent variables, we had to report only the data that were published in the articles. A.

The strengths of our study include the number of high-quality studies reviewed, the large representative sample and the multivariate analysis which regulaed for potential confounders. These factors provided greater statistical power and strengthened the results of the reviewed studies and enhanced the chance of recognizing a true effect of exposure [74]. Longitudinally design research aiming at chronic HCV infection detection as well as HCV treatment enrollment, are warranted in PWIDs.

Conclusion

The findings of the present study illustrate the important factors that may be effective to increase HCV testing rates among PWID, which may improve prevention and reduce transmission. This study concludes that better understand the social determinants of injecting risk provides an area for exploring effective interventions to improve HCV testing practices and individual risk reduction. As such the integration of HCV testing and treatment within exisiting low threshold harm reduction programs could be a possible solution to address the HCV burden among PWID and ultimately helping to reach the WHO goal of global elimination.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

CI:

Confidence intervals

HCV:

Hepatitis C virus

NSPs:

Needle and syringe programmes

NOS:

Newcastle-Ottawa Scale

OR:

Odds ratio

PICO:

Population, Intervention, Comparator, Outcomes

PRISMA:

Protocols of Systematic Reviews and Meta-Analyses

PWIDs:

People who inject drugs

WHO:

World Health Organization

References

  1. Crowley D, Van Hout M, Murphy C, Kelly E, Lambert J, Cullen W. Hepatitis C virus screening and treatment in Irish prisons from a governor and prison officer perspective-a qualitative exploration. Health Justice. 2018;6(1):1–10.

    Google Scholar 

  2. Degenhardt L, Charlson F, Stanaway J, Larney S, Alexander LT, Hickman M, Cowie B, Hall WD, Strang J, Whiteford H. Estimating the burden of disease attributable to injecting drug use as a risk factor for HIV, hepatitis C, and hepatitis B: findings from the global burden of disease study 2013. Lancet Infect Dis. 2016;16(12):1385–98.

    PubMed  Google Scholar 

  3. Lavanchy D. The global burden of hepatitis C. Liver Int. 2009;29(s1):74–81.

    PubMed  Google Scholar 

  4. Organization WH. Combating hepatitis B and C to reach elimination by 2030: advocacy brief: World Health Organization; 2016.

  5. Bajis S, Dore GJ, Hajarizadeh B, Cunningham EB, Maher L, Grebely J. Interventions to enhance testing, linkage to care and treatment uptake for hepatitis C virus infection among people who inject drugs: a systematic review. Int J Drug Policy. 2017;47:34–46.

    PubMed  Google Scholar 

  6. Harris M, Rhodes T. Hepatitis C treatment access and uptake for people who inject drugs: a review mapping the role of social factors. Harm Reduct J. 2013;10(1):7.

    PubMed  PubMed Central  Google Scholar 

  7. Bayat AH, Mohammadi R, Moradi-Joo M, Bayani A, Ahounbar E, Higgs P, Hemmat M, Haghgoo A, Armoon B. HIV and drug related stigma and risk-taking behaviors among people who inject drugs: a systematic review and meta-analysis. J Addict Dis. 2020;38(1):71–83.

    PubMed  Google Scholar 

  8. Rezaei F, Noroozi A, Armoon B, Farhoudian A, Massah O, Sharifi H, Ahounbar E, Khodadost M, Mohammadi F, Barkhordar N, et al. Social determinants and hepatitis C among people who inject drugs in Kermanshah, Iran: socioeconomic status, homelessness, and sufficient syringe coverage. J Subst Abus. 2017;22(5):474–8.

    Google Scholar 

  9. Armoon B, Noroozi M, Jorjoran Shushtari Z, Sharhani A, Ahounbar E, Karimi S, Ahmadi S, Farhoudian A, Rahmani A, Abbasi M, et al. Factors associated with HIV risk perception among people who inject drugs: findings from a cross-sectional behavioral survey in Kermanshah, Iran. J Subst Use. 2018;23(1):63–6.

    Google Scholar 

  10. Martin NK, Vickerman P, Dore GJ, Hickman M. The hepatitis C virus epidemics in key populations (including people who inject drugs, prisoners and MSM): the use of direct-acting antivirals as treatment for prevention. Curr Opin HIV AIDS. 2015;10(5):374–80.

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Degenhardt L, Peacock A, Colledge S, Leung J, Grebely J, Vickerman P, Stone J, Cunningham EB, Trickey A, Dumchev K, et al. Global prevalence of injecting drug use and sociodemographic characteristics and prevalence of HIV, HBV, and HCV in people who inject drugs: a multistage systematic review. Lancet Glob Health. 2017;5(12):e1192–207.

    PubMed  PubMed Central  Google Scholar 

  12. Nelson PK, Mathers BM, Cowie B, Hagan H, Des Jarlais D, Horyniak D, Degenhardt L. Global epidemiology of hepatitis B and hepatitis C in people who inject drugs: results of systematic reviews. Lancet (London, England). 2011;378(9791):571–83.

    Google Scholar 

  13. Larney S, Kopinski H, Beckwith CG, Zaller ND, Jarlais DD, Hagan H, Rich JD, van den Bergh BJ, Degenhardt L. Incidence and prevalence of hepatitis C in prisons and other closed settings: results of a systematic review and meta-analysis. Hepatology (Baltimore, Md). 2013;58(4):1215–24.

    Google Scholar 

  14. Vescio MF, Longo B, Babudieri S, Starnini G, Carbonara S, Rezza G, Monarca R. Correlates of hepatitis C virus seropositivity in prison inmates: a meta-analysis. J Epidemiol Community Health. 2008;62(4):305.

    CAS  PubMed  Google Scholar 

  15. Dolan K, Wirtz AL, Moazen B, Ndeffo-Mbah M, Galvani A, Kinner SA, Courtney R, McKee M, Amon JJ, Maher L, et al. Global burden of HIV, viral hepatitis, and tuberculosis in prisoners and detainees. Lancet (London, England). 2016;388(10049):1089–102.

    Google Scholar 

  16. John-Baptiste A, Krahn M, Heathcote J, Laporte A, Tomlinson G. The natural history of hepatitis C infection acquired through injection drug use: meta-analysis and meta-regression. J Hepatol. 2010;53(2):245–51.

    PubMed  Google Scholar 

  17. ECDC E: Prevention and control of infectious diseases among people who inject drugs. Guidance in brief 2011.

    Google Scholar 

  18. Bruneau J, Zang G, Abrahamowicz M, Jutras-Aswad D, Daniel M, Roy É. Sustained drug use changes after hepatitis C screening and counseling among recently infected persons who inject drugs: a longitudinal study. Clin Infect Dis. 2014;58(6):755–61.

    PubMed  Google Scholar 

  19. Martin NK, Vickerman P, Foster GR, Hutchinson SJ, Goldberg DJ, Hickman M. Can antiviral therapy for hepatitis C reduce the prevalence of HCV among injecting drug user populations? A modeling analysis of its prevention utility. J Hepatol. 2011;54(6):1137–44.

    CAS  PubMed  Google Scholar 

  20. Grebely J, Matthews GV, Lloyd AR, Dore GJ. Elimination of hepatitis C virus infection among people who inject drugs through treatment as prevention: feasibility and future requirements. Clin Infect Dis. 2013;57(7):1014–20.

    PubMed  Google Scholar 

  21. Organization WH: WHO guidelines on hepatitis B and C testing: World Health Organization; 2017.

    Google Scholar 

  22. Edlin BR, Kresina TF, Raymond DB, Carden MR, Gourevitch MN, Rich JD, Cheever LW, Cargill VA. Overcoming barriers to prevention, care, and treatment of hepatitis C in illicit drug users. Clin Infect Dis. 2005;40(Suppl 5):S276–85.

    PubMed  PubMed Central  Google Scholar 

  23. McGowan CE, Fried MW. Barriers to hepatitis C treatment. Liver Int. 2012;32(s1):151–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Volk ML. Antiviral therapy for hepatitis C: why are so few patients being treated? J Antimicrob Chemother. 2010;65(7):1327–9.

    CAS  PubMed  Google Scholar 

  25. Chan KY, Stoové MA, Sringernyuang L, Reidpath DD. Stigmatization of AIDS patients: disentangling Thai nursing students' attitudes towards HIV/AIDS, drug use, and commercial sex. AIDS Behav. 2008;12(1):146–57.

    PubMed  Google Scholar 

  26. Milne R, Price M, Wallace B, Drost A, Haigh-Gidora I, Nezil FA, Fraser C. From principles to practice: description of a novel equity-based HCV primary care treatment model for PWID. Int J Drug Policy. 2015;26(10):1020–7.

    PubMed  Google Scholar 

  27. Meyer JP, Moghimi Y, Marcus R, Lim JK, Litwin AH, Altice FL. Evidence-based interventions to enhance assessment, treatment, and adherence in the chronic hepatitis C care continuum. Int J Drug Policy. 2015;26(10):922–35.

    PubMed  PubMed Central  Google Scholar 

  28. Bayani A, Ghiasvand H, Rezaei O, Fattah Moghaddam L, Noroozi A, Ahounbar E, Higgs P, Armoon B. Factors associated with HIV testing among people who inject drugs: a meta-analysis. J Addict Dis. 2020:1–14.

  29. Rezaei O, Ghiasvand H, Higgs P, Noroozi A, Noroozi M, Rezaei F, Armoon B, Bayani A. Factors associated with injecting-related risk behaviors among people who inject drugs: a systematic review and meta-analysis study. J Addict Dis. 2020:1–18.

  30. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25(9):603–5.

    Google Scholar 

  31. Higgins JP, Green S. Cochrane handbook for systematic reviews of interventions, vol. 4: Wiley; 2011.

  32. Barocas JA, Brennan MB, Hull SJ, Stokes S, Fangman JJ, Westergaard RP: Barriers and facilitators of hepatitis C screening among people who inject drugs: a multi-city, mixed-methods study. Harm Reduct J 2014, 11(1):1.

  33. Sogarwal R, Madge V, Bishi P, Woleng A, Garg R. Predisposing, enabling, and need factors associated with utilization of HCV testing services among PWID in two settings in India. Hepatology Med Pol. 2016;1(1):1.

    Google Scholar 

  34. Anagnostou O, Fotiou A, Kanavou E, Antaraki A, Terzidou M, Richardson C, Kafetzopoulos E, DRIDMDGo OKANA, Alexakou K, Androulakis G. Factors associated with HCV test uptake in heroin users entering substitution treatment in Greece. HIV Med. 2018;19:34–9.

    CAS  PubMed  Google Scholar 

  35. Bajis S, Maher L, Treloar C, Hajarizadeh B, Lamoury FM, Mowat Y, Schulz M, Marshall AD, Cunningham EB, Cock V. Acceptability and preferences of point-of-care finger-stick whole-blood and venepuncture hepatitis C virus testing among people who inject drugs in Australia. Int J Drug Policy. 2018;61:23–30.

    PubMed  Google Scholar 

  36. Butler K, Day C, Sutherland R, van Buskirk J, Breen C, Burns L, Larney S. Hepatitis C testing in general practice settings: a cross-sectional study of people who inject drugs in Australia. Int J Drug Policy. 2017;47:102–6.

    PubMed  Google Scholar 

  37. Ti L, Kaplan K, Hayashi K, Suwannawong P, Wood E, Kerr T. Low rates of hepatitis C testing among people who inject drugs in Thailand: implications for peer-based interventions. J Public Health. 2013;35(4):578–84.

    CAS  Google Scholar 

  38. Iakunchykova O, Meteliuk A, Zelenev A, Mazhnaya A, Tracy M, Altice FL. Hepatitis C virus status awareness and test results confirmation among people who inject drugs in Ukraine. Int J Drug Policy. 2018;57:11–7.

    PubMed  PubMed Central  Google Scholar 

  39. Iversen J, Grebely J, Catlett B, Cunningham P, Dore GJ, Maher L. Estimating the cascade of hepatitis C testing, care and treatment among people who inject drugs in Australia. Int J Drug Policy. 2017;47:77–85.

    PubMed  Google Scholar 

  40. Enkelmann J, Gassowski M, Nielsen S, Wenz B, Roß S, Marcus U, Bremer V, Zimmermann R. High prevalence of hepatitis C virus infection and low level of awareness among people who recently started injecting drugs in a cross-sectional study in Germany, 2011–2014: missed opportunities for hepatitis C testing. Harm Reduct J. 2020;17(1):1–10.

    Google Scholar 

  41. Solomon SS, Quinn TC, Solomon S, McFall AM, Srikrishnan AK, Verma V, Kumar MS, Laeyendecker O, Celentano DD, Iqbal SH. Integrating HCV testing with HIV programs improves hepatitis C outcomes in people who inject drugs: a cluster-randomized trial. J Hepatol. 2020;72(1):67–74.

    CAS  PubMed  Google Scholar 

  42. Hayes B, Briceno A, Asher A, Yu M, Evans JL, Hahn JA, Page K. Preference, acceptability and implications of the rapid hepatitis C screening test among high-risk young people who inject drugs. BMC Public Health. 2014;14(1):645.

    PubMed  PubMed Central  Google Scholar 

  43. Fernàndez-López L, Folch C, Majó X, Gasulla L, Casabona J. Implementation of rapid HIV and HCV testing within harm reduction programmes for people who inject drugs: a pilot study. AIDS Care. 2016;28(6):712–6.

    PubMed  Google Scholar 

  44. Anderson ES, Pfeil SK, Deering LJ, Todorovic T, Lippert S, White DA. High-impact hepatitis C virus testing for injection drug users in an urban ED. Am J Emerg Med. 2016;34(6):1108–11.

    PubMed  Google Scholar 

  45. Boucher LM, Bayoumi AM, Mark AE, Cooper C, Martin A, Marshall Z, Boyd R, Oickle P, Diliso N, Pineau D. Hepatitis C testing, status and treatment among marginalized people who use drugs in an inner city setting: an observational cohort study. Substance use & misuse. 2019;54(1):18–30.

    Google Scholar 

  46. Strauss SM, Munoz-Plaza C, Tiburcio NJ, Astone-Twerell J, Des Jarlais DC, Gwadz M, Hagan H, Osborne A, Rosenblum A. Barriers and facilitators to undergoing hepatitis C virus (HCV) testing through drug treatment programs. J Drug Issues. 2008;38(4):1161–85.

    Google Scholar 

  47. Hope V, McVeigh J, Smith J, Glass R, Njoroge J, Tanner C, Parry J, Ncube F, Desai M. Low levels of hepatitis C diagnosis and testing uptake among people who inject image and performance enhancing drugs in England and Wales, 2012-15. Drug Alcohol Depend. 2017;179:83–6.

    CAS  PubMed  Google Scholar 

  48. Landis JR, Koch GG. The measurement of observer agreement for categorical data. biometrics. 1977:159–74.

  49. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50(4):1088–101.

    CAS  Google Scholar 

  50. Egger M, Smith GD, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. Bmj. 1997;315(7109):629–34.

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Garfein RS, Vlahov D, Galai N, Doherty MC, Nelson KE. Viral infections in short-term injection drug users: the prevalence of the hepatitis C, hepatitis B, human immunodeficiency, and human T-lymphotropic viruses. Am J Public Health. 1996;86(5):655–61.

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Xia Y-H, Chen W, Tucker JD, Wang C, Ling L. HIV and hepatitis C virus test uptake at methadone clinics in southern China: opportunities for expanding detection of bloodborne infections. BMC Public Health. 2013;13(1):899.

    PubMed  PubMed Central  Google Scholar 

  53. Pugatch D, Anderson BJ, O’Connell JV, Elson LC, Stein MD. HIV and HCV testing for young drug users in Rhode Island. J Adolesc Health. 2006;38(3):302–4.

    PubMed  Google Scholar 

  54. O'Connell JM, Kerr T, Li K, Tyndall MW, Hogg RS, Montaner JS, Wood E. Requiring help injecting independently predicts incident HIV infection among injection drug users. JAIDS. 2005;40(1):83–8.

    PubMed  Google Scholar 

  55. Morris MD, Evans J, Montgomery M, Yu M, Briceno A, Page K, Hahn JA. Intimate injection partnerships are at elevated risk of high-risk injecting: a multi-level longitudinal study of HCV-serodiscordant injection partnerships in San Francisco, CA. PLoS One. 2014;9(10):e109282.

    PubMed  PubMed Central  Google Scholar 

  56. Loughlin AM, Schwartz R, Strathdee SA. Prevalence and correlates of HCV infection among methadone maintenance attendees: implications for HCV treatment. Int J Drug Policy. 2004;15(2):93–101.

    Google Scholar 

  57. Walley AY, White MC, Kushel MB, Song YS, Tulsky JP. Knowledge of and interest in hepatitis C treatment at a methadone clinic. J Subst Abus Treat. 2005;28(2):181–7.

    Google Scholar 

  58. Wood E, Hogg RS, Kerr T, Palepu A, Zhang R, Montaner JS. Impact of accessing methadone on the time to initiating HIV treatment among antiretroviral-naive HIV-infected injection drug users. Aids. 2005;19(8):837–9.

    CAS  PubMed  Google Scholar 

  59. Birkhead GS, Klein SJ, Candelas AR, O’Connell DA, Rothman JR, Feldman IS, Tsui DS, Cotroneo RA, Flanigan CA. Integrating multiple programme and policy approaches to hepatitis C prevention and care for injection drug users: a comprehensive approach. Int J Drug Policy. 2007;18(5):417–25.

    PubMed  Google Scholar 

  60. Solomon SS, Solomon S, McFall AM, Srikrishnan AK, Anand S, Verma V, Vasudevan CK, Balakrishnan P, Ogburn EL, Moulton LH. Integrated HIV testing, prevention, and treatment intervention for key populations in India: a cluster-randomised trial. Lancet HIV. 2019;6(5):e283–96.

    PubMed  PubMed Central  Google Scholar 

  61. Solomon SS, McFall AM, Lucas GM, Srikrishnan AK, Kumar MS, Anand S, Quinn TC, Celentano DD, Mehta SH. Respondent-driven sampling for identification of HIV-and HCV-infected people who inject drugs and men who have sex with men in India: a cross-sectional, community-based analysis. PLoS Med. 2017;14:11.

    Google Scholar 

  62. Hellard M, Rolls DA, Sacks-Davis R, Robins G, Pattison P, Higgs P, Aitken C, McBryde E. The impact of injecting networks on hepatitis C transmission and treatment in people who inject drugs. Hepatology (Baltimore, Md). 2014;60(6):1861–70.

    Google Scholar 

  63. Hellard M, McBryde E, Sacks Davis R, Rolls DA, Higgs P, Aitken C, Thompson A, Doyle J, Pattison P, Robins G. Hepatitis C transmission and treatment as prevention - the role of the injecting network. Int J Drug Pol. 2015;26(10):958–62.

    Google Scholar 

  64. van de Laar T, Pybus O, Bruisten S, Brown D, Nelson M, Bhagani S, Vogel M, Baumgarten A, Chaix M-L, Fisher M. Evidence of a large, international network of HCV transmission in HIV-positive men who have sex with men. Gastroenterology. 2009;136(5):1609–17.

    PubMed  PubMed Central  Google Scholar 

  65. Lockart I, Matthews GV, Danta M. Sexually transmitted hepatitis C infection: the evolving epidemic in HIV-positive and HIV-negative MSM. Curr Opin Infect Dis. 2019;32(1):31–7.

    PubMed  Google Scholar 

  66. Yaphe S, Bozinoff N, Kyle R, Shivkumar S, Pai NP, Klein M. Incidence of acute hepatitis C virus infection among men who have sex with men with and without HIV infection: a systematic review. Sex Transm Infect. 2012;88(7):558–64.

    PubMed  Google Scholar 

  67. Meffre C, Le Strat Y, Delarocque-Astagneau E, Dubois F, Antona D, Lemasson JM, Warszawski J, Steinmetz J, Coste D, Meyer JF. Prevalence of hepatitis B and hepatitis C virus infections in France in 2004: social factors are important predictors after adjusting for known risk factors. J Med Virol. 2010;82(4):546–55.

    PubMed  Google Scholar 

  68. Pioche C, Pelat C, Larsen C, Desenclos J, Jauffret-Roustide M, Lot F, Pillonel J, Brouard C. Estimation de la prévalence de l'hépatite C en population générale, France métropolitaine, 2011. Bull Epidemiol Hebd. 2016;13:224–9.

    Google Scholar 

  69. Ireland G, Higgins S, Goorney B, Ward C, Ahmad S, Stewart C, Simmons R, Lattimore S, Lee V. Evaluation of hepatitis C testing in men who have sex with men, and associated risk behaviours, in Manchester, UK. Sex Transm Infect. 2017;93(6):404–9.

    CAS  PubMed  Google Scholar 

  70. Larsen C, Chaix M-L, Le Strat Y, Velter A, Gervais A, Aupérin I, Alric L, Duval X, Miailhes P, Pioche C. Gaining greater insight into HCV emergence in HIV-infected men who have sex with men: the HEPAIG Study. PLoS One. 2011;6:12.

    Google Scholar 

  71. Turner J, Rider A, Imrie J, Copas A, Edwards S, Dodds J, Stephenson J. Behavioural predictors of subsequent hepatitis C diagnosis in a UK clinic sample of HIV positive men who have sex with men. Sex Transm Infect. 2006;82(4):298–300.

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Foster AL, Gaisa MM, Hijdra RM, Turner SS, Morey TJ, Jacobson KB, Fierer DS. Shedding of hepatitis C virus into the rectum of HIV-infected men who have sex with men. Clin Infect Dis. 2016:ciw740.

  73. Turner SS, Gianella S, Yip MJ, van Seggelen WO, Gillies RD, Foster AL, Barbati ZR, Smith DM, Fierer DS. Shedding of hepatitis C virus in semen of human immunodeficiency virus-infected men. In: Open forum infectious diseases: 2016: Oxford University Press; 2016.

  74. Yazdanian M, Armoon B, Noroozi A, Mohammadi R, Bayat A-H, Ahounbar E, Higgs P, Nasab HS, Bayani A, Hemmat M. Dental caries and periodontal disease among people who use drugs: a systematic review and meta-analysis. BMC Oral Health. 2020;20(1):44.

    PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This study was sponsored by Social Determinants of Health Research Center, Saveh University of Medical Sciences, Saveh, Iran.

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This research did not receive any specific grant from funding agencies in the public, commercial, or non-for-profit sectors.

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AB. and BA. Conceived the study EA and B.A. collected all data. AB, AHB and EA analyzed and interpreted the data. YF and B.A. drafted the manuscript. All authors commented on the drafts of the manuscript and approved the final copy of the paper for submission.

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Correspondence to Bahram Armoon.

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Karimi, S.E., Bayani, A., Higgs, P. et al. Prevalence and high risk behaviours associated with HCV testing among people who inject drugs: a systematic review and Meta-analysis. Subst Abuse Treat Prev Policy 15, 64 (2020). https://doi.org/10.1186/s13011-020-00306-1

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