Prevalence of Hepatitis C Virus in Iranian Prisoners: An Updated Systematic Review and Multilevel Meta-Analysis Study

authors:

avatar Alireza Najimi ORCID 1 , avatar Mohammad Gholami-Fesharaki ORCID 1 , * , avatar Mohsen Rowzati 2

Department of Biostatistics, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran
Occupational Health Center, Isfahan Mobarakeh Steel Company, Isfahan, Iran

How To Cite Najimi A, Gholami-Fesharaki M, Rowzati M. Prevalence of Hepatitis C Virus in Iranian Prisoners: An Updated Systematic Review and Multilevel Meta-Analysis Study. Hepat Mon. 2020;20(5):e102004. https://doi.org/10.5812/hepatmon.102004.

Abstract

Context:

Hepatitis C is one of the most dangerous viral infections causing chronic liver disease.

Objectives:

The current study aimed to estimate the pooled prevalence of hepatitis C in Iranian prisoners.

Evidence Acquisition:

Articles were identified through searching international databases, including PubMed, Scopus, Elsevier, Google Scholar, and Web of Science and Iranian databases, including Scientific Information Database (SID), Health.barakatkns, IranDoc, Civilica, and MagIran. We systematically reviewed all studies reporting the prevalence of HCV in Iranian prisoners. All studies conducted ELISA tests for the evaluation of HCV antibodies. In this study, a multilevel meta-analysis method was used to estimate the pooled prevalence.

Results:

The electronic search identified 147 records, 33 of which were relevant papers used for the pooled meta-analysis of HCV prevalence. Overall, the prevalence of HCV using a multilevel meta-analysis approach was 24.88% (95% CI = 19.12 - 31.69). The highest pooled HCV rate was related to Markazi province (59.47% [95% CI = 51.70 - 67.25]), while the lowest pooled HCV rate belonged to North Khorasan province (5.00% [95% CI = 2.44 - 7.55]). A decreasing HCV prevalence trend was observed between 1995 and 2018.

Conclusions:

The results of the study showed that the prevalence of HCV is significantly high among prisoners in Iran. An enhanced training program is needed for prisoners and prison staff to improve the prisoners’ health status.

1. Context

Hepatitis C Virus (HCV) is a major public health problem. It is associated with morbidity and mortality and imposes a substantial burden on the worldwide healthcare system (1, 2). About 399,000 people die each year due to hepatitis C, mostly from cirrhosis and hepatocellular carcinoma. A previous study estimated 71 million people (1% of the world’s population) living with HCV infection in 2015 (3).

Based on the available data, most countries in the Middle East and North Africa (MENA) have a low-to-moderate anti-HCV prevalence (4). A prison is a high-risk place for prisoners who are engaged in risky behaviors such as injecting drugs, tattooing, unwanted sexual intercourse, and sharing syringes. The HCV prevalence is generally higher among prisoners than in the general population, mainly due to risky behaviors of prisoners (5-7). Prisoners are susceptible to various infectious diseases and may spread them after they return to society (8). Information about the HCV prevalence in prisoners can lead to appropriate decisions in public health policy and management.

The previous meta-analysis of HCV prevalence among Iranian prisoners was done by Behzadifar et al. (9) in 2018. Two other studies did not use two rounds of a national study (bio-behavioral and observational studies of HBV and HCV in Iran prisons) conducted in 2015 and 2016 (10, 11) and not reported the prevalence of HCV by province.

2. Objectives

This systematic review and meta-analysis study was done to estimate the pooled HCV prevalence using a new statistical approach (multilevel meta-analysis) in prisoners.

3. Evidence Acquisition

3.1. Search Strategy

All studies used ELISA tests for assessing HCV antibodies. The literature on the HCV-Ab prevalence in Iran was acquired through searching international databases, including PubMed, Scopus, Elsevier, Google Scholar, and Web of Science and Iranian databases, including Scientific Information Database (SID), IranDoc, Health.barakatkns, MagIran, and Civilica. Our last search was conducted on February 8, 2020. To search and include related studies as many as possible, we used the terms “Hepatitis C”, “HCV”, “Prevalence”, “Epidemiology”, “Prison”, “Prisoner”, “Inmates”, “Jails”, and “Iran” (or the names of its provinces) as keywords in titles and/or abstracts in the MeSH word search database.

3.2. Selection of Studies and Data Extraction

Published studies were regarded as qualified for the analysis if they met the following criteria: (1) cross-sectional studies with the full text of the paper available in the Persian or English languages, (2) studies with a sample size of more than 30, and (3) studies reporting the prevalence of HCV antibodies by the ELISA test in Iran provinces. Conversely, the following studies were excluded: (1) non-English or non-Persian full-text reports, (2) studies not providing enough data to estimate the prevalence rate, (3) studies designed as letters to the editor, expert opinions, editorials, commentaries, case-reports, case-series, and reviews, and (4) Studies reporting overlapping data.

3.3. Data Extraction

All articles categorized as potentially relevant were reviewed separately by both of the authors (Mohsen Rowzati and Alireza Najimi-Varzaneh). They evaluated the relevance of each report and summarized the following data using Excel datasheets: First author’s name, year of publication, year of study, number of HCV patients, study sample size, name of the province, and mean age of responders. The analysis was conducted according to the preferred reporting items for systematic reviews and meta-analyses (PRISMA) (12). In this study, “The Newcastle Ottawa Scale (NOS)” was used to assess the quality of the included studies. For better data extraction, we used blinding and task separation (13).

3.4. Statistical Analysis

In the current meta-analysis study, two approaches were applied for data analysis. First, we used the “metafor” package in R, version 3.6, software. In this technique, the heterogeneity among the studies was assessed using the Q test (P < 0.10) and I-squared statistics (I2 > 40%). According to the results of the heterogeneity test, we used fixed or random-effect models to determine the prevalence of HCV. According to the central limit theorem, to estimate the pooled effect (θ) in the fixed-effects model, the prevalence of hepatitis C in each study (pi) is assumed to be homogeneous (homogeneity assumption) with normal distribution and a mean of θ and variance of Vi while in the random-effects model, the homogeneity assumption is violated. The other main assumption for the conventional meta-analysis approach (fixed or random-effects) is the independence of studies (14). This assumption cannot be achieved in prevalence studies because studies that are from the same location are dependent on each other (14).To solve such problems, we proposed a multi-level meta-analysis method with the “lme4” package considering Logitpijk=ω+uj(i)+vi, in which uj(i) and vi are random effects for study homogeneity and location dependency, respectively. After estimating ω, the pooled effect (θ) was calculated with θ=exp(ω)/(1+exp(ω)).

4. Results

4.1. Search Results and Study Selection

The study selection process is depicted in Figure 1. A total of 147 studies were potentially associated with the prevalence of HCV in Iran provinces. After reviewing the abstracts and titles, 98 studies were eliminated based on the stated inclusion and exclusion criteria. After the full-text screening and quality assessment, a total of 33 records were deemed as eligible studies published until 2019.

Screening of Articles Based on PRISMA Statement
Screening of Articles Based on PRISMA Statement

4.2. Prevalence of Hepatitis C Virus in Iranian Prisoners

Table 1 presents the study characteristics, including the reference, province, first author’s name, year of publication, year of study, mean age, number of HCV patients, and study sample size. Table 2 represents the pooled prevalence of hepatitis C according to the prevalence in each province of Iran, as well as the pooled prevalence obtained by the multilevel meta-analysis. As can be seen, the pooled prevalence of HCV in prisoners was 24.88% with a 95% Confidence Interval (CI) of 19.12% - 31.69%. The results also showed a decreasing trend in the HCV prevalence between 1995 and 2018.

Table 1.

Characteristics of the Included Studies of HCV Epidemiology in Iran

ProvinceFirst AuthorRef.Year of PublicationYear of StudyMean AgeNumber of HCV CasesStudy Sample Size
AlborzMoradi(10)2018201539.491451282
Sharafi(15)20192017 - 201836.51061788
Azerbaijan, EastAsgari(16)20082003NA74472
Asgari(16)20082002NA104517
Asgari(16)20082001NA118579
Asgari(16)20082000NA115480
Moradi(10)2018201539.4911297
Naghili(17)2012200731.355192
BushehrAsgari(16)20082002NA166403
Asgari(16)20082001NA147355
Chaharmahal and BakhtiariTajbakhsh(18)2008NA25.876600
Moradi(11)2019201636.2914201
FarsAlasvand(19)201520123741300
Moradi(10)2018201539.4958771
QazvinMoradi(11)2019201636.2960518
GuilanMohtasham Amiri(20)2007200334.7209460
Moradi(11)2019201636.291051010
GolestanKhodabakhshi(21)20072002 - 2003NA28121
HamadanAlizadeh(22)2005200237.9128427
Moradi(10)2018201539.4974538
HormozganDavoodian(23)2009200235.4163249
Moradi(11)2019201636.2950540
IsfahanAlasvand(19)2015201237101300
Asgari(16)20082004NA5198
Asgari(16)20082003NA144250
Ataei(24)2011NA326441485
Kassaian(25)2012200932.6392943
Nokhodian(26)20122008 - 200916.597160
Nokhodian(27)2012200934.5412163
Isfahan, Lorestan, and Chaharmahal and BakhtiariJavadi(28)200620035131431
KermanAlasvand(19)201520123710312
Moradi(10)2018201539.4934455
KermanshahAlasvand(19)201520123753400
Asgari(16)20082001NA3531052
Asgari(16)20082004NA349896
Khademi(29)2019201735.522301034
Moradi(11)2019201636.2976576
Khorasan, NorthMoradi(11)2019201636.2914280
Khorasan, RazaviAlasvand(19)201520123743400
Asgari(16)20082005NA1945
Asgari(16)20082004NA566
Asgari(16)20082002NA71106
Asgari(16)20082003NA76112
Ghorbani(30)20082004 - 2006NA30139
Khajedaluee(31)2016200834.422721114
Moradi(10)2018201539.49901033
Rowhani-Rahbar(32)2004200132.860101
Khorasan, SouthAzarkar(33)2010200834.729358
Azarkar(34)2007NA34.131400
Ghafari(35)2019201637.424300
Ziaee(36)20142009 - 201034.768881
KhuzestanMoradi(11)2019201636.29108956
Kohgiluyeh and Boyer-AhmadMoradi(11)2019201636.295171
Sarkari(37)20122009 - 2010NA72616
KurdistanAsgari(16)20082003NA105400
LorestanMoradi(10)2018201539.4943378
MarkaziSofian(38)2012200930.791153
MazandaranMoradi(10)2018201539.4926398
Zakizadeh(39)2006200139.496312
Sistan and BaluchestanMoradi(10)2018201539.4941356
Salehi(40)2001NANA40441
TehranAlasvand(19)201520123725408
Mir-Nasseri(41)20112001 - 200235.85311386
Mir-Nasseri(42)2005200136.58271346
Mir-Nasseri(43)2008200136301386
Moradi(11)2019201636.29841940
Zali(44)2001199534.2182402
YazdMoradi(11)2019201636.2915296
ZanjanAsgari(16)20082001NA195360
Asgari(16)20082004NA276468
Asgari(16)20082002NA288480
Asgari(16)20082003NA324523
Khani(45)2003200133.7165346
Table 2.

Pooled Prevalence of Hepatitis C Virus in Iranian Prisoners According to Province Using the Random-Effects Model

ProvinceNumber of StudiesPrevalence (95 CI)
Alborz28.58 (3.32 - 13.85)
Azerbaijan, East618.56 (10.75 - 26.38)
Bushehr241.29 (37.78 - 44.79)
Chaharmahal and Bakhtiari318.10 (5.99 - 30.20)
Fars210.34 (4.34 - 16.35)
Guilan221.29 (19.22 - 23.47)
Golestan123.14 (15.62 - 30.65)
Hamadan221.78 (5.88 - 37.67)
Hormozgan214.32 (11.95 - 16.96)
Isfahan834.30 (21.06 - 47.54)
Kerman25.27 (1.09 - 9.45)
Kermanshah524.23 (14.42 - 34.05)
Khorasan, North15.00 (2.44 - 7.55)
Khorasan, Razavi933.66 (22.73 - 44.60)
Khorasan, South47.83 (6.64 - 9.03)
Khuzestan111.30 (9.30 - 13.30)
Kohgiluyeh and Boyer-Ahmad29.78 (7.79 - 12.07)
Kurdistan126.25 (21.94 - 30.56)
Lorestan226.84 (24.16 - 29.66)
Markazi159.47 (51.70 - 67.25)
Mazandaran217.18 (14.47 - 20.16)
Qazvin111.58 (8.82 - 14.33)
Sistan and Baluchestan210.09 (7.72 - 12.45)
Tehran648.72 (19.37 - 78.08)
Yazd15.06 (2.57 - 7.56)
Zanjan556.73 (51.96 - 61.50)
Multilevel Pooled Effect24.88 (19.12 - 31.69)

5. Discussion

The findings of this study showed that the estimated prevalence of HCV among Iranian prisoners was 24.88% (number of studies = 33). This rate is lower than the rate reported in Behzadifar et al. study (9) (number of studies = 17, reported HCV prevalence = 28%). Such a difference can be attributed to the number of studies used in the meta-analysis and the use of a powerful statistical approach. In the multilevel meta-analysis, the heterogeneity of each province can be corrected from the overall pooled effect, and the estimation of the pooled effect is reported with higher accuracy (14). Previously published meta-analysis studies have reported the HCV prevalence in different subsets of the Iranian population. This rate is higher than the prevalence in the general population (reported HCV prevalence = 0.6%) (46) and lower than the rate among people who inject drugs (reported HCV prevalence = 52.2%) (1). In comparison with the international studies, this rate is higher than the prevalence reported among prisoners in Egypt (23.6%), Pakistan (15.6%), Libya (23.7%) (47), Italy (22.4%) (48) Brazil (2.4%) (49), France (4.8%) (50), the United States (18%) (51), and Hungary (4.9%) (52) and lower than the rate in California (34.3%) (8), Indonesia (34.1%) (53), Lebanon (28.1%) (47), and Irish prisoners (37%) (54).

Differences in the prevalence of HCV in different studies are due to differences in the type of prisons and prisoners. Most prisoners are at risk of hepatitis due to high-risk behaviors such as injecting drugs, addiction, sexual misconduct, and violence (19). On the other hand, prisoners are not isolated from society; many prisoners are kept for a short period, and many of them return to the community and contact with the general public. This makes hepatitis C prisoners a risk group for HCV transmission to the community. Therefore, paying attention to the prevalence of hepatitis C among prisoners can guarantee community health (19).

Our results also showed a decreasing trend in the HCV prevalence between 1995 and 2018 (Figure 2). Such a reduction can be the result of implementing educational programs and effective therapeutic strategies targeting hepatitis C by the Ministry of Health.

The trend of HCV prevalence among prisoners in Iran
The trend of HCV prevalence among prisoners in Iran

Some limitations exist in the present study, the first of which is not mentioning the type of prisoners in the published articles, and the second is the lack of data and studies from some provinces.

Two strong points of this study are the use of two rounds of a national study conducted in 2015 and 2016 (10, 11) and the use of a new statistical approach (multilevel meta-analysis) for calculating the pooled effect.

6. Conclusions

According to this study, hepatitis C has a high prevalence among prisoners in Iran. Consequently, we recommend the regular screening of prisoners, separating the affected prisoners from the rest, taking remedial measures including easy access to disposable syringes and needles, health education (personal and community), and treatment of addicted prisoners.

Acknowledgements

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