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

Alireza Najimi; Mohammad Gholami-Fesharaki; Mohsen Rowzati

doi:10.5812/hepatmon.102004

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

authors:

Alireza Najimi ¹ , Mohammad Gholami-Fesharaki ^{1
, *} , Mohsen Rowzati ²

1 Department of Biostatistics, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran

2 Occupational Health Center, Isfahan Mobarakeh Steel Company, Isfahan, Iran

Hepatitis Monthly: Vol.20, issue 5; e102004

published online: May 18, 2020

article type: Systematic Review

received: February 24, 2020

accepted: March 15, 2020

DOI: https://doi.org/10.5812/hepatmon.102004

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.

Keywords

Hepatitis C Iran Prevalence Epidemiology Multilevel Analysis Prisoner Systematic Review

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 ( $p_{i}$ ) is assumed to be homogeneous (homogeneity assumption) with normal distribution and a mean of θ and variance of $V_{i}$ 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 $L o g i t (p_{i j k}) = ω + u_{j (i)} + v_{i}$ , in which $u_{j (i)}$ and $v_{i}$ 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.

Figure 1.

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

Province	First Author	Ref.	Year of Publication	Year of Study	Mean Age	Number of HCV Cases	Study Sample Size
Alborz	Moradi	(10)	2018	2015	39.49	145	1282
Alborz	Sharafi	(15)	2019	2017 - 2018	36.5	106	1788
Azerbaijan, East	Asgari	(16)	2008	2003	NA	74	472
	Asgari	(16)	2008	2002	NA	104	517
	Asgari	(16)	2008	2001	NA	118	579
	Asgari	(16)	2008	2000	NA	115	480
	Moradi	(10)	2018	2015	39.49	11	297
	Naghili	(17)	2012	2007	31.3	55	192
Bushehr	Asgari	(16)	2008	2002	NA	166	403
Bushehr	Asgari	(16)	2008	2001	NA	147	355
Chaharmahal and Bakhtiari	Tajbakhsh	(18)	2008	NA	25.8	76	600
Chaharmahal and Bakhtiari	Moradi	(11)	2019	2016	36.29	14	201
Fars	Alasvand	(19)	2015	2012	37	41	300
Fars	Moradi	(10)	2018	2015	39.49	58	771
Qazvin	Moradi	(11)	2019	2016	36.29	60	518
Guilan	Mohtasham Amiri	(20)	2007	2003	34.7	209	460
Guilan	Moradi	(11)	2019	2016	36.29	105	1010
Golestan	Khodabakhshi	(21)	2007	2002 - 2003	NA	28	121
Hamadan	Alizadeh	(22)	2005	2002	37.9	128	427
Hamadan	Moradi	(10)	2018	2015	39.49	74	538
Hormozgan	Davoodian	(23)	2009	2002	35.4	163	249
Hormozgan	Moradi	(11)	2019	2016	36.29	50	540
Isfahan	Alasvand	(19)	2015	2012	37	101	300
	Asgari	(16)	2008	2004	NA	51	98
	Asgari	(16)	2008	2003	NA	144	250
	Ataei	(24)	2011	NA	32	644	1485
	Kassaian	(25)	2012	2009	32.6	392	943
	Nokhodian	(26)	2012	2008 - 2009	16.59	7	160
	Nokhodian	(27)	2012	2009	34.54	12	163
Isfahan, Lorestan, and Chaharmahal and Bakhtiari	Javadi	(28)	2006	2003		513	1431
Kerman	Alasvand	(19)	2015	2012	37	10	312
Kerman	Moradi	(10)	2018	2015	39.49	34	455
Kermanshah	Alasvand	(19)	2015	2012	37	53	400
	Asgari	(16)	2008	2001	NA	353	1052
	Asgari	(16)	2008	2004	NA	349	896
	Khademi	(29)	2019	2017	35.52	230	1034
	Moradi	(11)	2019	2016	36.29	76	576
Khorasan, North	Moradi	(11)	2019	2016	36.29	14	280
Khorasan, Razavi	Alasvand	(19)	2015	2012	37	43	400
	Asgari	(16)	2008	2005	NA	19	45
	Asgari	(16)	2008	2004	NA	5	66
	Asgari	(16)	2008	2002	NA	71	106
	Asgari	(16)	2008	2003	NA	76	112
	Ghorbani	(30)	2008	2004 - 2006	NA	30	139
	Khajedaluee	(31)	2016	2008	34.42	272	1114
	Moradi	(10)	2018	2015	39.49	90	1033
	Rowhani-Rahbar	(32)	2004	2001	32.8	60	101
Khorasan, South	Azarkar	(33)	2010	2008	34.7	29	358
	Azarkar	(34)	2007	NA	34.1	31	400
	Ghafari	(35)	2019	2016	37.4	24	300
	Ziaee	(36)	2014	2009 - 2010	34.7	68	881
Khuzestan	Moradi	(11)	2019	2016	36.29	108	956
Kohgiluyeh and Boyer-Ahmad	Moradi	(11)	2019	2016	36.29	5	171
Kohgiluyeh and Boyer-Ahmad	Sarkari	(37)	2012	2009 - 2010	NA	72	616
Kurdistan	Asgari	(16)	2008	2003	NA	105	400
Lorestan	Moradi	(10)	2018	2015	39.49	43	378
Markazi	Sofian	(38)	2012	2009	30.7	91	153
Mazandaran	Moradi	(10)	2018	2015	39.49	26	398
Mazandaran	Zakizadeh	(39)	2006	2001	39.4	96	312
Sistan and Baluchestan	Moradi	(10)	2018	2015	39.49	41	356
Sistan and Baluchestan	Salehi	(40)	2001	NA	NA	40	441
Tehran	Alasvand	(19)	2015	2012	37	25	408
	Mir-Nasseri	(41)	2011	2001 - 2002	35.85	311	386
	Mir-Nasseri	(42)	2005	2001	36.58	271	346
	Mir-Nasseri	(43)	2008	2001	36	301	386
	Moradi	(11)	2019	2016	36.29	84	1940
	Zali	(44)	2001	1995	34.2	182	402
Yazd	Moradi	(11)	2019	2016	36.29	15	296
Zanjan	Asgari	(16)	2008	2001	NA	195	360
	Asgari	(16)	2008	2004	NA	276	468
	Asgari	(16)	2008	2002	NA	288	480
	Asgari	(16)	2008	2003	NA	324	523
	Khani	(45)	2003	2001	33.7	165	346

Table 2.

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

Province	Number of Studies	Prevalence (95 CI)
Alborz	2	8.58 (3.32 - 13.85)
Azerbaijan, East	6	18.56 (10.75 - 26.38)
Bushehr	2	41.29 (37.78 - 44.79)
Chaharmahal and Bakhtiari	3	18.10 (5.99 - 30.20)
Fars	2	10.34 (4.34 - 16.35)
Guilan	2	21.29 (19.22 - 23.47)
Golestan	1	23.14 (15.62 - 30.65)
Hamadan	2	21.78 (5.88 - 37.67)
Hormozgan	2	14.32 (11.95 - 16.96)
Isfahan	8	34.30 (21.06 - 47.54)
Kerman	2	5.27 (1.09 - 9.45)
Kermanshah	5	24.23 (14.42 - 34.05)
Khorasan, North	1	5.00 (2.44 - 7.55)
Khorasan, Razavi	9	33.66 (22.73 - 44.60)
Khorasan, South	4	7.83 (6.64 - 9.03)
Khuzestan	1	11.30 (9.30 - 13.30)
Kohgiluyeh and Boyer-Ahmad	2	9.78 (7.79 - 12.07)
Kurdistan	1	26.25 (21.94 - 30.56)
Lorestan	2	26.84 (24.16 - 29.66)
Markazi	1	59.47 (51.70 - 67.25)
Mazandaran	2	17.18 (14.47 - 20.16)
Qazvin	1	11.58 (8.82 - 14.33)
Sistan and Baluchestan	2	10.09 (7.72 - 12.45)
Tehran	6	48.72 (19.37 - 78.08)
Yazd	1	5.06 (2.57 - 7.56)
Zanjan	5	56.73 (51.96 - 61.50)
Multilevel Pooled Effect		24.88 (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.

Figure 2.

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

Footnotes

Authors' Contribution: M. GH.F.: data analysis and study supervision; A. N.: data collection and manuscript writing; M. R.: data collection
Conflict of Interests: The authors declare that they have no conflict of interest.
Ethical Approval: IR.MODARES.REC.1397.254.
Funding/Support: Tarbiat Modares University funded the study.

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