Hostname: page-component-8448b6f56d-tj2md Total loading time: 0 Render date: 2024-04-17T16:21:04.279Z Has data issue: false hasContentIssue false
  • English
  • Français

Epidemiology of hepatitis C virus among hemodialysis patients in the Middle East and North Africa: systematic syntheses, meta-analyses, and meta-regressions

Published online by Cambridge University Press:  09 October 2017

M. HARFOUCHE ,
H. CHEMAITELLY ,
S. MAHMUD ,
K. CHAABNA ,
S. P. KOUYOUMJIAN ,
Z. AL KANAANI  and
L. J. ABU-RADDAD
M. HARFOUCHE
Affiliation:
Infectious Disease Epidemiology Group, Weill Cornell Medicine-Qatar, Cornell University, Qatar Foundation – Education City, Doha, Qatar
H. CHEMAITELLY
Affiliation:
Infectious Disease Epidemiology Group, Weill Cornell Medicine-Qatar, Cornell University, Qatar Foundation – Education City, Doha, Qatar
S. MAHMUD
Affiliation:
Infectious Disease Epidemiology Group, Weill Cornell Medicine-Qatar, Cornell University, Qatar Foundation – Education City, Doha, Qatar
K. CHAABNA
Affiliation:
Infectious Disease Epidemiology Group, Weill Cornell Medicine-Qatar, Cornell University, Qatar Foundation – Education City, Doha, Qatar Department of Healthcare Policy & Research, Weill Cornell Medicine, Cornell University, New York, USA
S. P. KOUYOUMJIAN
Affiliation:
Infectious Disease Epidemiology Group, Weill Cornell Medicine-Qatar, Cornell University, Qatar Foundation – Education City, Doha, Qatar
Z. AL KANAANI
Affiliation:
Infectious Disease Epidemiology Group, Weill Cornell Medicine-Qatar, Cornell University, Qatar Foundation – Education City, Doha, Qatar
L. J. ABU-RADDAD*
Affiliation:
Infectious Disease Epidemiology Group, Weill Cornell Medicine-Qatar, Cornell University, Qatar Foundation – Education City, Doha, Qatar Department of Healthcare Policy & Research, Weill Cornell Medicine, Cornell University, New York, USA
*
*Author for correspondence: Professor L. J. Abu-Raddad, Infectious Disease Epidemiology Group, Weill Cornell Medicine-Qatar, Qatar Foundation – Education City, P.O. Box 24144, Doha, Qatar. (Email: lja2002@qatar-med.cornell.edu)
Rights & Permissions [Opens in a new window]

Summary

We aimed to investigate hepatitis C virus (HCV) epidemiology among hemodialysis (HD) patients in the Middle East and North Africa (MENA). Our data source was an HCV biological measures database populated through systematic literature searches. Descriptive epidemiologic syntheses, effects meta-analyses and meta-regressions, and genotype analyses were conducted. We analyzed 289 studies, including 106 463 HD patients. HCV incidence ranged between 0 and 100% as seroconversion risk, and between 0 and 14·7 per 1000 person-years as incidence rate. The regional pooled mean estimate was 29·2% (95% CI: 25·6–32·8%) for HCV antibody positive prevalence and 63·0% (95% CI: 55·4–70·3%) for the viremic rate. Region within MENA, country income group, and year of data collection were associated with HCV prevalence; year of data collection adjusted odds ratio was 0·92 (95% CI: 0·90–0·95). Genotype diversity varied across countries with four genotypes documented regionally: genotype 1 (39·3%), genotype 2 (5·7%), genotype 3 (29·6%), and genotype 4 (25·4%). Our findings showed that one-third of HD patients are HCV antibody positive and one-fifth are chronic carriers and can transmit the infection. However, HCV prevalence is declining. In context of growing HD patient population and increasing HCV treatment availability, it is critical to improve standards of infection control in dialysis and expand treatment coverage.

Keywords

Epidemiologyhemodialysishepatitis CMiddle East and North Africaprevalence
Type
Original Papers
Information
Epidemiology & Infection , Volume 145 , Issue 15 , November 2017 , pp. 3243 - 3263
Check for updates
Creative Commons
Creative Common License - CCCreative Common License - BYCreative Common License - NCCreative Common License - ND
This is an Open Access article, distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives licence (http://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is unaltered and is properly cited. The written permission of Cambridge University Press must be obtained for commercial re-use or in order to create a derivative work.
Copyright
Copyright © Cambridge University Press 2017

INTRODUCTION

Viral hepatitis is the 7th leading cause of mortality worldwide with hepatitis C virus (HCV) accounting for about half of this mortality [Reference Stanaway1]. Though HCV infection is a public health concern globally, the Middle East and North Africa (MENA) is the most affected region by this infection [Reference Stanaway1–3]. For 2015, MENA was estimated to have the highest incidence rate of all regions at 62·5 per 100 000 person-year, second largest incidence at 409 000 new infections per year, highest HCV antibody prevalence at 2·3%, and largest number of chronically infected people at 15 million [2].

Recent breakthroughs in HCV treatment, notably the introduction of highly effective direct-acting antivirals (DAA), have ushered a new era for controlling HCV and reducing its disease burden [Reference Flamm4]. Global targets have been set to eliminate HCV and reduce its mortality by 2030 [5, 6].

HCV is a blood borne pathogen transmitted parenterally such as through sharing of injections and use of contaminated medical equipment [Reference Prati7]. Patients undergoing hemodialysis (HD) are at a higher risk of HCV exposure due to sharing of dialysis machines [Reference Sy and Jamal8]. It has been estimated that HD increases the odds of acquiring HCV by five folds [Reference Sun9]. Characterizing HCV infection levels in HD patients and controlling its transmission through this mode of exposure are integral to improving the quality and healthcare utilization of HD. More specifically, this would lead to the prevention of unnecessary health complications such as liver disease and hepatic malignancies, and to a reduction in associated healthcare costs [Reference Bikbov10–Reference Fabrizi, Poordad and Martin12].

Against this background, we aimed to characterize HCV epidemiology among HD patients in the MENA region by: (1) systematically describing the evidence on HCV antibody incidence and prevalence in this population; (2) estimating the mean country-specific HCV prevalence in HD patients; (3) estimating HCV viremic rate in HD patients, that is the prevalence of HCV chronic infection (HCV RNA positivity) among antibody positive patients; (4) assessing associations with HCV prevalence in this population; and (5) assessing the frequency, distribution, and diversity of HCV genotypes in HD patients. This study was conducted under the umbrella of the MENA HCV Epidemiology Synthesis Project, an on-going effort to characterize HCV epidemiology and inform key public health research, policy, and programming priorities in MENA [Reference Mohamoud13–Reference Chaabna, Chemaitelly, Mumtaz and Abu-Raddad19].

METHODOLOGY

Data source

Our source of data was the MENA HCV Epidemiology Synthesis Project database. This database consists of several sub-databases that include an HCV antibody incidence database comprising 47 incidence studies among 29 600 participants, an HCV antibody prevalence database comprising 2543 antibody prevalence studies among 52 598 736 participants, an HCV RNA prevalence (among antibody positive persons) database comprising 178 RNA prevalence studies among 19 593 HCV antibody-positive participants, and an HCV genotype frequency database comprising 338 HCV genotype studies among 82 257 participants.

The MENA HCV Epidemiology Synthesis Project database was compiled through systematic searches of the literature [Reference Mohamoud13, Reference Fadlalla15–Reference Chemaitelly, Chaabna and Abu-Raddad17, Reference Chemaitelly20–Reference Al-Kanaani and Abu-Raddad22] informed by the Cochrane Collaboration handbook [Reference Higgins and Green23] and reporting the findings using the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) guidelines [Reference Moher24]. The searched literature included international databases (PubMed and Embase), regional databases, national databases, and the MENA HIV/AIDS Epidemiology Synthesis Project database [Reference Abu-Raddad25, Reference Abu-Raddad26], in addition to gray literature comprised of public health reports and routine data reporting, which are available from the authors upon request. The systematic reviews used broad search criteria with no language or year restrictions, to capture all publications pertinent to HCV since the discovery of the virus in 1989 [Reference Choo27, Reference Kuo28]. The systematic searches screened for duplicate studies and excluded them to avoid double counting of any single study.

The definition of the MENA region in these searches and in the present article included the 24 countries of Afghanistan, Algeria, Bahrain, Djibouti, Egypt, Iran, Iraq, Jordan, Kuwait, Lebanon, Libya, Mauritania, Morocco, Oman, Pakistan, Palestine, Qatar, Saudi Arabia, Somalia, Sudan, Syria, Tunisia, the United Arab Emirates (UAE), and Yemen.

For the purpose of the present study, we also searched the literature (non-systematically) for studies of the population proportion of HD patients in MENA countries – that is the proportion of HD patients among the whole population in a given country. For estimating the number of people undergoing dialysis, the total population size in each country was obtained from the United Nations World Population Prospects database [29]. The MENA region estimate was calculated as a weighted (by population size) mean of available country measures.

Quantitative analyses

Meta-analyses

We conducted meta-analyses to estimate the country-specific mean HCV antibody prevalence. We further stratified HCV prevalence measures by year of publication and conducted meta-analyses for three different but consecutive temporal durations to descriptively examine changes in prevalence with time. Studies consisting of a minimum of 20 participants were included. We also conducted meta-analyses to estimate the country-specific mean viremic rate. Studies consisting of a minimum of 10 antibody-positive participants were included. In the event that the study reported HCV prevalence by different strata, such as age and sex, among others, the total sample size was replaced with stratified measures whenever the sample size requirement was fulfilled for each stratum.

Meta-analyses were conducted whenever we had three or more measures to be pooled using a DerSimonian–Laird random-effects model with inverse variance weighting [Reference Borenstein30]. The variance was stabilized using the Freeman–Tukey type arcsine square-root transformation [Reference Freeman and Tukey31]. Cochran's Q test was implemented to assess evidence for heterogeneity in effect size; a P-value < 0·1 was considered significant [Reference Borenstein32, Reference Higgin33]. The I 2 was calculated to assess the proportion of between-study variation in effect size (HCV prevalence or HCV viremic rate) that is due to actual differences in effect size between studies [Reference Borenstein32]. The prediction interval was calculated to assess the distribution of true effects around the estimated mean [Reference Borenstein32, Reference Higgins, Thompson and Spiegelhalter34].

Meta-regressions

We conducted meta-regressions on HCV prevalence studies to assess associations with HCV prevalence. Four types of potential predictors were specified a priori and included in the analyses: region within MENA, country income group, year of data collection, and sample size. Factors with a P-value < 0·1 in univariable analyses were eligible for inclusion in the final multivariable model. Factors with a P-value < 0·05 in the multivariable model were considered as significant predictors.

The region variable consisted of seven strata based on geographic proximity: Fertile Crescent (Iraq, Jordan, Lebanon, Palestine, and Syria); Gulf (Kuwait, Oman, Saudi Arabia, UAE, and Qatar); Horn of Africa (Yemen and Sudan); Maghreb (Algeria, Libya, Morocco, and Tunisia); Egypt; Iran; and Pakistan. This classification covers all MENA countries with available HCV data in HD patients.

The income group variable stratified countries according to their income group per World Bank classification [35]. Low middle-income countries included Egypt, Morocco, Pakistan, Sudan, Syria, Tunisia, and Yemen. Upper middle-income countries included Algeria, Iran, Iraq, Jordan, Lebanon, Libya, and Palestine. High-income countries included Kuwait, Oman, Saudi Arabia, Qatar, and UAE.

For the year-of-data-collection variable, we imputed the missing observations using the median of the observed values calculated by subtracting the year of data collection from the year of publication for each study. A sensitivity analysis was conducted with missing values for the non-imputed observations. The results were similar with no impact on statistical significance (Supplementary Table S1 on the Cambridge Journals Online website).

Genotype diversity

We analyzed the regional and country-specific frequency, distribution, and diversity of HCV genotypes among HD patients. The regional analysis was conducted based on actual frequency from available studies, and also as a weighted estimate by each country's population size. The frequency for each genotype was calculated with individuals testing positive for multiple genotypes contributing separately to the sum of cases for each genotype, as per earlier methodology [Reference Messina36]. Genotype diversity was assessed using Shannon Diversity Index [Reference Shannon37].

Statistical analyses were conducted using R studio version 3.3.2 [38] and StataSE version 13 [39].

RESULTS

HD in MENA

The population proportion of patients undergoing HD varied across countries (Table 1). The lowest reported was 250·2 per million population in Bahrain, and the highest reported was 665·4 per million population in Lebanon. Based on available population proportions, we estimated the country-specific number of patients undergoing HD (Table 1). The lowest was 327 patients in Bahrain, and the highest was 25 225 in Iran. The MENA region population proportion was 383·6 per million population yielding an estimate of 239 759 HD patients.

Table 1. Population proportion of hemodialysis (HD) in the Middle East and North Africa (MENA) [40]

a The population proportion of HD for the MENA region was estimated as a weighted mean of available country measures.

Scope of evidence

Out of the MENA HCV Epidemiology Synthesis Project database, we identified 21 HCV incidence measures among a total of 8857 HD patients (Supplementary Table S2), 205 HCV antibody prevalence measures among a total of 92 341 HD patients (Table 2), 31 HCV RNA prevalence measures among a total of 3172 HCV antibody-positive HD patients (Supplementary Fig. S1), and 31 HCV genotype frequency measures among a total of 2093 HCV RNA-positive HD patients (Table 6; Supplementary Fig. S2).

Table 2. Studies reporting hepatitis C virus (HCV) antibody prevalence among hemodialysis patients across the Middle East and North Africa

HD, Hemodialysis; Prev., Prevalence.

Out of the 24 included countries, data were available from 19 countries. The number of data points varied by country. Iran, Saudi Arabia, Tunisia, and Egypt contributed the largest number of data points. Several countries contributed as little as one data point.

HCV antibody incidence among HD patients

Egypt (n = 6), Lebanon (n = 6), and Morocco (n = 4) are the countries with the largest number of studies reporting HCV incidence among HD patients (Supplementary Table S2). Most studies had a follow-up duration ranging from 6 to 36 months, and reported incidence either as a risk of seroconversion or as an incidence rate. Seroconversion risk varied widely and was in the range of 0–100%. Incidence rate also varied substantially and was in the range of 0–14·7 per 1000 person-years. Incidence varied extensively even within the same country. For example, in Lebanon, HCV incidence rate varied from 0 to 14·7 per 1000 person-years across different geographical sites [Reference Rached120].

HCV antibody prevalence among HD patients

Iran (n = 41), Saudi Arabia (n = 39), and Egypt (n = 26) are the countries with the largest number of studies reporting HCV prevalence among HD patients (Table 2). HCV antibody prevalence varied widely within and across countries and was in the range of 0–100% with a median of 26·5%. For example, in Egypt, HCV prevalence varied from 10·0% to 100% across different geographical sites at different times.

Table 3 shows the pooled mean estimate of HCV prevalence by country, by temporal duration, and for the region. The country-specific mean estimate ranged from 7·3% (95% CI: 3·7–11·7%) in Lebanon to 65·5% (95% CI: 56·5–74·1%) in Egypt. HCV prevalence was 51·6% (95% CI: 46·1–57·1%) in years of publication 1989–1998, and decreased to 27·8% (95% CI: 23·1–32·8%) in 1999–2008, and 18·8% (14·5–23·5%) in 2009–2016.

Table 3. Pooled mean estimate for hepatitis C virus (HCV) antibody prevalence among hemodialysis patients across countries of the Middle East and North Africa

CI, Confidence interval; UAE, United Arab Emirates.

a Q: The Cochran's Q statistic is a measure assessing the existence of heterogeneity in effect size.

b I 2: A measure that assesses the magnitude of between-study variation that is due to differences in effect size across studies rather than chance.

c Prediction interval: A measure that estimates the 95% interval in which the true effect size in a new study will lie.

The mean estimate for the region was 29·2% (95% CI: 25·6–32·8%). Egypt, Syria, Saudi Arabia, Yemen, Morocco, and Qatar had a mean estimate exceeding 40%. There was strong evidence for heterogeneity in effect size (that is HCV prevalence) in all countries (P ⩽ 0·01). The vast majority of the variation was due to variation in effect size rather than chance (I 2 > 50%). The prediction intervals confirmed substantial variation in effect size in each country. Forest plots for the country-specific meta-analyses can be found in Supplementary Fig. S3.

HCV viremic rate among HD patients

Tunisia (n = 13) is the country with the largest number of studies reporting HCV viremic rate among HD patients (Table 4). For the rest of the countries, there were either few or no measures. HCV viremic rate varied across studies and was in the range of 19·1–93·3% with a median of 65·4%. The pooled mean estimate for HCV viremic rate across MENA was 63·0% (95% CI: 55·4–70·3%). There was evidence for heterogeneity in effect size estimates (here HCV viremic rate) across the region with a P < 0·0001. The I 2 for the pooled estimate was indicative of the variation being due to true differences in effect size rather than chance (I 2 = 94·0%). The prediction interval confirmed substantial variation in effect size. Forest plot for the regional meta-analysis can be found in Supplementary Fig. S1.

Table 4. Pooled mean estimate for hepatitis C virus (HCV) viremic rate among hemodialysis patients across countries of the Middle East and North Africa. HCV viremic rate is the prevalence of HCV chronic infection (HCV RNA positivity) among antibody-positive persons

HCV, Hepatitis C virus; RNA, Ribonucleic acid.

a Q: The Cochran's Q statistic is a measure assessing the existence of heterogeneity in effect size.

b I 2: A measure that assesses the magnitude of between-study variation that is due to differences in effect size across studies rather than chance.

c Prediction interval: A measure that estimates the 95% interval in which the true effect size in a new study will lie.

Associations with HCV antibody prevalence among HD patients

Table 5 shows the results of the univariable and multivariable meta-regressions. Region, income group, and year of data collection were associated with HCV antibody prevalence in the univariable analysis (P-value < 0·1 for all three variables). Sample size was not associated with HCV prevalence (P-value > 0·7).

Table 5. Univariable and multivariable meta-regression models for hepatitis C virus (HCV) antibody prevalence among hemodialysis patients across the Middle East and North Africa

OR, Odds ratio; AOR, Adjusted odds ratio; LMIC, Low middle-income country; UMCI, Upper middle-income country; HIC, High-income country.

a The adjusted R-square for the full model was 54·48%.

b Fertile Crescent includes: Iraq, Jordan, Lebanon, Palestine, and Syria.

c Gulf includes: Kuwait, Oman, Qatar, Saudi Arabia, and Unite Arab Emirates.

d Horn of Africa includes: Yemen and Sudan.

e Maghreb includes: Algeria, Libya, Morocco, and Tunisia.

f Income group was removed from the multivariable analysis because of collinearity.

In the final multivariable analysis, region and year of data collection were included, but income group was not due to collinearity. The model explained 54·48% of the variation. Relative to the Fertile Crescent, the odds (for higher HCV prevalence) was much larger in Egypt; adjusted odds ratio (AOR) of 7·43 (95% CI: 4·44–12·44). It was also higher in Pakistan (AOR = 2·47; 95% CI: 1·07–5·69) and the Gulf region (AOR = 1·77; 95% CI: 1·08–2·90), but lower in Iran (AOR = 0·38; 95% CI: 0·24–0·58). Importantly, the AOR for the year of data collection was 0·92 (95% CI: 0·90–0·95) indicating declining HCV prevalence in HD patients year by year.

Risk factors for HCV infection among HD patients

Few studies assessed risk factors for HCV infection among HD patients. Duration and frequency of dialysis and exposure to blood transfusions were the most commonly reported risk factors [Reference Abdel-Wahab45, Reference Gohar51, Reference Goher52, Reference Saddik and El62, Reference Ramzi109, Reference Othman and Monem182].

HCV genotype and subtype distribution among HD patients

Table 6 shows the frequency, distribution, and Shannon Diversity Index of HCV genotypes among HD patients. Supplementary Fig. S2 also shows the distribution of HCV genotypes and subtypes.

Table 6. Frequency, distribution, and Shannon Diversity Index of hepatitis C virus (HCV) genotypes among hemodialysis patients across the Middle East and North Africa

No data were found for HCV genotypes 5, 6, and 7.

a The maximum value for Shannon Diversity Index is 1·95 assuming full genotype diversity of seven HCV genotypes [Reference Chemaitelly, Chaabna and Abu-Raddad17, Reference Shannon37].

b Each individual testing positive for multiple genotypes contributed separately to the sum of cases for each genotype.

The vast majority (92·3%) of viremic HD patients were infected by a single strain (Supplementary Fig. S2). At the regional level, four HCV genotypes were documented in HD patients: genotype 1 (68·8%), genotype 2 (9·6%), genotype 3 (7·9%), and genotype 4 (13·5%). Weighted by country population size, the regional genotype distribution was: genotype 1 (39·3%), genotype 2 (5·7%), genotype 3 (29·6%), and genotype 4 (25·4%). No cases of genotypes 5, 6, and 7 were reported.

Genotype 1 was commonly found in Morocco (100%), Tunisia (77·3%), Jordan (73·3%), Syria (60·7%), Iran (55·7%), Bahrain (55·5%), Iraq (51·5%), and Saudi Arabia (46·8%). It was also common in Lebanon (28·1%), Pakistan (22·2%), and Egypt (16·1%).

Genotype 4 was commonly found in Egypt (83·9%), Saudi Arabia (50·0%), Iraq (45·4%), and Lebanon (40·6%). It was also present in the rest of the countries apart from Morocco. Pakistan was the only country where genotype 3 was the most common genotype (62·2%). Genotype 3 was also common in Iran (39·4%), but otherwise rare in the rest of the countries. Genotype 2 was common in Bahrain (33·3%) and Lebanon (25·0%), and somewhat common in Pakistan (13·3%) and Tunisia (11·8%), but otherwise rare.

For genotype 1, subtype 1a and 1b were commonly observed in MENA (Supplementary Fig. S2). Subtypes 2a, 2b, 2c, 3a, 3b, and 4a were also detected in this region. Combinations of the above genotypes and subtypes were observed among multiply infected individuals.

Genotype diversity varied across countries. It was highest in Lebanon with a relative Shannon Diversity Index of 63·7% (score: 1·24 out of a maximum of 1·95) and lowest in Morocco 0·0% (score: 0·0 out of a maximum of 1·95). For the region as a whole, the relative Shannon Diversity Index was 49·1% (score: 0·95 out of a maximum of 1·95) for the unweighted analysis, and 63·9% (score: 1·24 out of a maximum of 1·95) for the weighted analysis by country population size.

DISCUSSION

Through a comprehensive investigation of HCV epidemiology among HD patients in MENA, we found that there is ongoing and considerably high HCV incidence in this population across the region. However, the incidence rate varied between countries and across different settings within the same country (Supplementary Table S2). We also found high HCV prevalence in HD patients, with the prevalence varying substantially across the region and within each country. About one-third (29·2%) of HD patients have already been infected with HCV (Table 3), with two-thirds of them (63·0%) being chronic carriers (Table 4) that can potentially transmit the infection to other patients through dialysis. We also found substantial diversity of HCV genotypes in HD patients, with genotype 1 being the most common at the regional level (Table 6). Importantly, we found that HCV prevalence in HD patients is on a declining trend (Tables 3 and 5).

These findings suggest that the standard of infection control in dialysis differs across countries and across dialysis units within each country. They also indicate that extensive improvement is needed to control HCV transmission among HD patients. Fortunately, improvements appear to be already taking place as validated by the declining trend in prevalence. These findings highlight further the importance of addressing HCV infection and disease burden in HD patients, especially considering the recent availability and increasing affordability of DAAs for HCV treatment [Reference Flamm4], and that the number of patients undergoing dialysis is rising rapidly with the aging of the population and growing prevalence of chronic diseases that lead to renal disease [40, 195–Reference Anand, Bitton and Gaziano197].

Our pooled mean estimate for HCV prevalence indicated that HCV prevalence among HD patients in MENA is higher than that in other regions such as Europe (7·2%) [Reference Zampieron198], the USA (7·9%) [Reference Patel199, Reference Finelli200], and the Asia-Pacific region (range across countries of 1–18%) [Reference Johnson201]. This finding may not only suggest inferior standards of dialysis in MENA, but may also reflect the higher background HCV prevalence in the whole population in this region [2, 3]. Indeed, HCV prevalence among HD patients in MENA countries reflected in part HCV prevalence in the population at large in each country. For example, HCV prevalence among HD patients in Egypt and Pakistan was much higher than that in other MENA countries (Table 5), reflecting the higher prevalence in the wider population in these two countries [Reference Mohamoud13, Reference Al-Kanaani and Abu-Raddad22].

The high HCV incidence and prevalence in HD patients appear to reflect improper application of infection control measures, such as by healthcare personnel to maintain hands hygiene [Reference Patel199, 202], to change gloves routinely [Reference Patel199, 202], and to clean the dialysis unit and equipment properly between patients [Reference Sy and Jamal8, Reference Zampieron203]. With the continuing conflict emergencies in several countries and the large refugee and migrant populations, overloading dialysis units and depletion of medical resources is a growing concern [204, Reference Daw and Dau205]. These emergencies appear to have led to reuse and sharing of supplies and equipment intended for single usage such as infusion vials and machine filters [Reference Daw and Dau205, Reference Fabrizi and Messa206]. The lingering emergencies may undermine the recent improvements and reverse the trend of declining HCV prevalence in HD patients.

We found substantial diversity in the circulating HCV genotypes in HD patients across countries. However, this diversity appeared to reflect the distribution of circulating genotypes in each country [Reference Mahmud207]. For example, the dominant genotypes among HD patients in Egypt and Pakistan were genotypes 4 and 3, respectively (Table 6), similar to the dominant genotypes in the wider population in these two countries [Reference Mahmud207]. These findings may indicate overlapping transmission networks where HCV is circulating from one population to another through different modes of exposure including dialysis.

A review of HCV among HD patients in the Middle East has been recently published [Reference Ashkani-Esfahani, Alavian and Salehi-Marzijarani208]. Its findings agreed overall with our findings despite differences between the two studies in the focus, scope, and analysis plans. Our study covered more countries in MENA over a longer duration, examined analytically trends and associations, and reported a broader set of outcome measures and analyses (such as for the genotype distribution). In total, 205 studies were included in our analyses compared to 56 studies in Ashkani-Esfahani et al. study [Reference Ashkani-Esfahani, Alavian and Salehi-Marzijarani208]. Both studies concluded that there is high HCV prevalence in HD patients that needs to be addressed through targeted interventions.

Our study had several limitations. The availability of data varied from one county to another and we did not identify any data for five MENA countries (Afghanistan, Bahrain, Djibouti, Mauritania, and Somalia). Sample size varied also across studies and the sampled HD populations may have been sampled from specific geographic areas within a given country, and may not be representative of the wider HD population in the country. Despite these limitations, we were able to identify a large volume of data for MENA countries that allowed us to conduct different types of analyses, generate multiple inferences, and produce a comprehensive mapping of HCV epidemiology among HD patients in this region.

CONCLUSIONS

Our findings revealed ongoing HCV incidence and high HCV prevalence among HD patients in MENA, but incidence and prevalence appear to be declining year by year. About one-fifth of HD patients are chronic carriers of HCV infection, in need of HCV treatment, and potentially can transmit the infection to other HD patients. In context of rapidly growing HD patient population, these findings highlight the need to improve standards of infection control in dialysis in MENA.

Moreover, in context of recent availability and increasing affordability of DAAs for HCV treatment, these findings highlight the urgency to address HCV infection and disease burden in HD patients. Governments that are reluctant to take on national level HCV elimination projects, could initially focus on HD patients as a candidate population for micro-elimination as a way to advance the agenda for HCV DAA treatment. With HCV circulation among HD patients being a major mode of HCV transmission, tackling this infection and disease burden is critical to HCV global elimination and mortality reduction targets by 2030.

SUPPLEMENTARY MATERIAL

The supplementary material for this article can be found at https://doi.org/10.1017/S0950268817002242.

ACKNOWLEDGEMENTS

This publication was made possible by NPRP grant number 9-040-3-008 from the Qatar National Research Fund (a member of Qatar Foundation). The findings achieved herein are solely the responsibility of the authors. The authors are also grateful for infrastructure support provided by the Biostatistics, Epidemiology, and Biomathematics Research Core at Weill Cornell Medicine-Qatar.

DECLARATION OF INTEREST

The authors have no competing interest to declare.

References

REFERENCES

1. Stanaway, JD, et al. The global burden of viral hepatitis from 1990 to 2013: findings from the Global Burden of Disease Study 2013. The Lancet 2016; 388: 1081–1088.Google Scholar
2. World Health Organization. Global Viral Hepatitis Report. Geneva: World Health Organization, 2017 (http://www.who.int/hepatitis/publications/global-hepatitis-report2017/en/). Accessed May 2017. Licence: CC BY-NC-SA 3.0 IGO.Google Scholar
3. World Health Organization. The Epidemiology of Hepatitis C Virus in the World Health Organization Eastern Mediterranean Region: Implications for Strategic Action. Eastern Mediterranean Hepatitis C Virus Epidemiology Synthesis Project, 2017 (in press).Google Scholar
4. Flamm, SL. Advances in the treatment of hepatitis C virus infection from EASL 2015. Gastroenterology & Hepatology 2015; 11: Supplement 3.Google Scholar
5. World Health Organization. Global Health Sector Strategy on Viral Hepatitis 2016–2021. Towards Ending Viral Hepatitis. World Health Organization, 2016 (http://www.who.int/hepatitis/strategy2016-2021/ghss-hep/en/). Accessed May 2017.Google Scholar
6. World Health Organization. Combating Hepatitis B and C to Reach Elimination by 2030: Advocacy Brief. World Health Organization, 2016 (http://www.who.int/hepatitis/publications/hep-elimination-by-2030-brief/en/). Accessed May 2017.Google Scholar
7. Prati, D. Transmission of hepatitis C virus by blood transfusions and other medical procedures: a global review. Journal of Hepatology 2006; 45: 607–616.Google ScholarPubMed
8. Sy, T, Jamal, MM. Epidemiology of hepatitis C virus (HCV) infection. International Journal of Medical Sciences 2006; 3: 41–46.CrossRefGoogle ScholarPubMed
9. Sun, J, et al. Hepatitis C infection and related factors in hemodialysis patients in China: systematic review and meta-analysis. Renal Failure 2009; 31: 610–620.CrossRefGoogle Scholar
10. Bikbov, B. Hepatitis C virus and kidney disease: evidence, hope, and hurdles. Nephron 2017; 136: 51–53.Google Scholar
11. Fabrizi, F, et al. Meta-analysis: effect of hepatitis C virus infection on mortality in dialysis. Alimentary Pharmacology & Therapeutics 2004; 20: 1271–1277.Google Scholar
12. Fabrizi, F, Poordad, FF, Martin, P. Hepatitis C infection and the patient with end-stage renal disease. Hepatology 2002; 36: 3–10.CrossRefGoogle ScholarPubMed
13. Mohamoud, YA, et al. The epidemiology of hepatitis C virus in Egypt: a systematic review and data synthesis. BMC Infectious Diseases 2013; 13: 288.CrossRefGoogle ScholarPubMed
14. Chaabna, K, et al. Protocol for a systematic review and meta-analysis of hepatitis C virus (HCV) prevalence and incidence in the horn of Africa sub-region of the Middle East and North Africa. Systematic Reviews 2014; 3: 146.Google Scholar
15. Fadlalla, FA, et al. The epidemiology of hepatitis C virus in the Maghreb region: systematic review and meta-analyses. PLoS ONE 2015; 10: e0121873.Google Scholar
16. Mohamoud, YA, Riome, S, Abu-Raddad, LJ. Epidemiology of hepatitis C virus in the Arabian Gulf countries: systematic review and meta-analysis of prevalence. International Journal of Infectious Diseases 2016; 46: 116–125.Google ScholarPubMed
17. Chemaitelly, H, Chaabna, K, Abu-Raddad, LJ. The epidemiology of hepatitis C virus in the Fertile Crescent: systematic review and meta-analysis. PLoS ONE 2015; 10: e0135281.Google Scholar
18. Mahmud, S, Akbarzadeh, V, Abu-Raddad, LJ. The epidemiology of hepatitis C virus in Iran: Systematic review and meta-analyses. (under preparation). 2017.Google Scholar
19. Chaabna, KMY, Chemaitelly, H, Mumtaz, GR, Abu-Raddad, LJ. Protocol for a systematic review and meta-analysis of hepatitis C virus (HCV) prevalence and incidence in The Horn of Africa sub-region of the Middle East and North Africa. PROSPERO 2014: CRD42014010318, 2014 (http://www.crd.york.ac.uk/PROSPERO/display_record.asp?ID=CRD42014010318).Google Scholar
20. Chemaitelly, H, et al. The epidemiology of hepatitis C virus in Afghanistan: systematic review and meta-analysis. International Journal of Infectious Diseases 2015; 40: 54–63.Google Scholar
21. Chaabna, K, Kouyoumjian, SP, Abu-Raddad, LJ. Hepatitis C virus epidemiology in Djibouti, Somalia, Sudan, and Yemen: systematic review and meta-analysis. PLoS ONE 2016; 11: e0149966.Google Scholar
22. Al-Kanaani, ZMS, Abu-Raddad, L. The epidemiology of hepatitis C virus in Pakistan: systematic review and meta-analyses (under preparation). 2016.Google Scholar
23. Higgins, JP, Green, S. Cochrane handbook for systematic reviews of interventions: John Wiley & Sons, 2011.Google Scholar
24. Moher, D, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Medicine 2009; 6: e1000097.Google Scholar
25. Abu-Raddad, LJ, et al. Characterizing the HIV/AIDS Epidemic in the Middle East and North Africa: Time for Strategic Action. World Bank Publications, 2010 (https://openknowledge.worldbank.org/handle/10986/2457), License: CC BY 3·0 IGO. Accessed May 2017.Google Scholar
26. Abu-Raddad, LJ, et al. Epidemiology of HIV infection in the Middle East and North Africa. AidS 2010; 24: S5–S23.Google Scholar
27. Choo, Q-L, et al. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepititis genome. Science 1989; 244: 359.Google Scholar
28. Kuo, G, et al. An assay for circulating antibodies to a major etiologic virus of human non-A, non-B hepatitis. Science 1989; 244: 362–364.Google Scholar
29. DESA U. World population prospects: the 2015 revision, key findings and advance tables. Working Paper No 2015.Google Scholar
30. Borenstein, M, et al. A basic introduction to fixed-effect and random-effects models for meta-analysis. Research synthesis methods 2010; 1: 97–111.Google Scholar
31. Freeman, MF, Tukey, JW. Transformations related to the angular and the square root. The Annals of Mathematical Statistics 1950; Dec 1: 607–611.Google Scholar
32. Borenstein, M, et al. Front Matter, in Introduction to Meta-Analysis. Chichester, UK: John Wiley & Sons, Ltd, 2009.Google Scholar
33. Higgin, J, et al. Measuring inconsistency in meta-analysis. British Medical Journal 2003; 327: 557–560.Google Scholar
34. Higgins, J, Thompson, SG, Spiegelhalter, DJ. A re-evaluation of random-effects meta-analysis. Journal of the Royal Statistical Society: Series A (Statistics in Society) 2009; 172: 137–159.Google Scholar
35. The World Bank. World Bank country and lending groups. 2017 (https://datahelpdesk.worldbank.org/knowledgebase/articles/906519-world-bank-country-and-lending-groups). Accessed May 2017.Google Scholar
36. Messina, JP, et al. Global distribution and prevalence of hepatitis C virus genotypes. Hepatology 2015; 61: 77–87.Google ScholarPubMed
37. Shannon, CE. The mathematical theory of communication. 1963. In. Europe PMC, 1996.Google Scholar
38. Anon. RStudio Team. RStudio: Integrated Development. Boston, MA: R. RStudio, Inc., 2015 (http://www.rstudio.com/).Google Scholar
39. Anon. StataCorp. 2015. Stata Statistical Software: Release 14. College Station, TX: StataCorp LP.Google Scholar
40. United States Renal Data System. 2016 USRDS Annual Data Report: Epidemiology of Kidney Disease in the United States. Bethesda, MD: National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases, 2016 (https://www.usrds.org/2016/view/Default.aspx). Accessed May 2017.Google Scholar
41. National Office of Statistics (Algeria). National Office of Statistics: Algeria Population and Housing Census 2008. In, 2008.Google Scholar
42. Afredj, N. Hepatite B, C et grossesse, Conference presentation at: Palais de la culture Moufdi Zakaria, Algerie. 7em Journee de La Clinique Medicale, 2009.Google Scholar
43. Zitouni, S, et al. Prevalence et incidence des hepatites virales VHB et VHC et prevalence de la infection HCV/HCB dans trois centres D'hemodialyse a Constantine-Algerie. La 4ème journée Nationale d'Hygiène Hospitalière et de Lutte Contre les Infections associées aux soins Palais de la Culture – Algerie, 2011, p. 209.Google Scholar
44. Abdel Hady, SI, El-Din, MS, El-Din, ME. A high hepatitis E virus (HEV) seroprevalence among unpaid blood donors and haemodialysis patients in Egypt. The Journal of the Egyptian Public Health Association 1998; 73: 165–179.Google Scholar
45. Abdel-Wahab, MF, et al. High seroprevalence of hepatitis C infection among risk groups in Egypt. The American Journal of Tropical Medicine and Hygiene 1994; 51: 563–567.Google Scholar
46. Attia, EA, Hassan, SI, Youssef, NM. Cutaneous disorders in uremic patients on hemodialysis: an Egyptian case-controlled study. International Journal of Dermatology 2010; 49: 1024–1030.Google Scholar
47. El Gohary, A, et al. High prevalence of hepatitis C virus among urban and rural population groups in Egypt. Acta Tropica 1995; 59: 155–161.Google Scholar
48. El Sayed Zaki, M, Magdy Abd El Razek, H, Magdy Abd El Razek, M. Hepatitis E viral seroprevalence among multiple transfused Egyptian children. Journal of Viral Hepatitis 2013; 20: 40–41.Google Scholar
49. El-Emshaty, WM, et al. Diagnostic performance of an immunoassay for simultaneous detection of Hcv core antigen and antibodies among haemodialysis patients. Brazilian Journal of Microbiology: [Publication of the Brazilian Society for Microbiology] 2011; 42: 303–309.Google Scholar
50. Elgohry, I, Elbanna, A, Hashad, D. Occult hepatitis B virus infection in a cohort of Egyptian chronic hemodialysis patients. Clinical Laboratory 2011; 58: 1057–1061.Google Scholar
51. Gohar, SA, et al. Prevalence of antibodies to hepatitis C virus in hemodialysis patients and renal transplant recipients. The Journal of the Egyptian Public Health Association 1994; 70: 465–484.Google Scholar
52. Goher, SA, et al. Dialyzer reuse and hepatitis C virus in hemodialysis population in Egypt. Scientific Medical Journal 1998; 10: 43–54.Google Scholar
53. Hammad, AM, Zaghloul, MHED. Hepatitis G virus infection in Egyptian children with chronic renal failure (single centre study). Annals of Clinical Microbiology and Antimicrobials 2009; 8: 1.Google Scholar
54. Hassan, NF, Kotkat, A. Prevalence of antibodies to hepatitis C virus in pregnant women in Egypt. The Journal of Infectious Diseases 1993; 168: 248–249.Google Scholar
55. Helaly, GF, et al. Occult hepatitis B virus infection among chronic hemodialysis patients in Alexandria, Egypt. Journal of Infection and Public Health 2015; 8: 562–569.Google Scholar
56. Mouchiran, FH, et al. Hepatitis C Virus Infection among hemodialysis patients. Egyptian Journal of Medical Microbiology 1995; 4: 289–229.Google Scholar
57. Ibrahim, S. Quality of care assessment and adherence to the international guidelines considering dialysis, water treatment, and protection against transmission of infections in university hospital-based dialysis units in Cairo, Egypt. Hemodialysis International International Symposium on Home Hemodialysis 2010; 14: 61–67.Google Scholar
58. Ismail, ZA, et al. Prevalence of hepatitis C virus antibodies in hemodialysis patients. The Medical Journal of Cairo University 1994; 62: 283–291.Google Scholar
59. Kamal, NN, et al. Health-related quality of life among hemodialysis patients at El-Minia University Hospital, Egypt. Journal of Public Health (Germany) 2013; 21: 193–200.Google Scholar
60. Kandil, ME, Rasheed, MA, Saad, NE. Hepatitis C and B viruses among some high risk groups of Egyptian children. Journal of Medical Sciences 2007; 7: 1259–1267.Google Scholar
61. Khodir, SA, et al. Prevalence of HCV infections among hemodialysis patients in Al Gharbiyah Governorate, Egypt. Arab Journal of Nephrology and Transplantation 2012; 5: 145–147.Google Scholar
62. Saddik, Y, El, Azoni M. Hepatitis C virus [HCV] antibodies in patients with chronic renal failure and treated with regular hemodialysis and those treated with renal transplantation. Scientific Medical Journal 1997; 9: 79–99.Google Scholar
63. Shatat, HZ, Kotkat, AM, Farghaly, AG. Immune response to hepatitis B vaccine in haemodialysis patients. The Journal of the Egyptian Public Health Association 2000; 75: 257–275.Google Scholar
64. Zahran, AM. Prevalence of seroconversion of hepatitis C virus among hemodialysis patients in Menoufia Governorate, Egypt. Arab Journal of Nephrology and Transplantation 2014; 7: 133–135.Google Scholar
65. Aghakhani, A, et al. Significance of hepatitis B core antibody as the only marker of hepatitis B virus infection in high risk patients. Iranian Journal of Pathology 2009; 4: 80–84.Google Scholar
66. Alavian, SM, et al. Anti-hepatitis E antibody in hemodialysis patients in Isfahan, Iran: prevalence and risk factors. Hepatitis Monthly 2015; 15: e23633.Google ScholarPubMed
67. Ali, J, Besharat, S, Khodabakshi, B. Hepatitis C in hemodialysis centers of Golestan province, northeast of Iran (2005). Hepatitis Monthly 2008; 8: 61–65.Google Scholar
68. Amiri, ZM, Shakib, AJ, Toorchi, M. Seroprevalence of hepatitis C and risk factors in haemodialysis patients in Guilan, Islamic Republic of Iran. Eastern Mediterranean Health Journal 2005; 11: 372–376.Google Scholar
69. Azarkar, Z, et al. Survey of HBV and HCV markers in haemodialysis and thalassemia, South Khorasan, Birjand 2007. Scientific Journal of Iranian Blood Transfusion Organization 2009; 6: 233–237.Google Scholar
70. Bozorghi, S, et al. Assessment of prevalence and risk factors of hepatitis C virus infection in haemodialysis patients in Ghazvin. Scientific Journal of Iran Blood Transfusion Organization 2006; 2: 331–337.Google Scholar
71. Broumand, B, et al. Prevalence of hepatitis C infection and its risk factors in hemodialysis patients in Tehran: preliminary report from “the effect of dialysis unit isolation on the incidence of hepatitis C in dialysis patients” project. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 2002; 13: 467–472.Google Scholar
72. Dadgaran, S. Prevalence and risk factors of hepatitis C virus among hemodialysis patients. Journal of Guilan University of Medical Sciences 2005; 14: 76–86.Google Scholar
73. Dadmanesh, M, et al. Evaluation of prevalence and risk factors of hepatitis G virus infection among hemodialysis patients referred to Iranian army hospitals in Tehran during 2012–2013. Hepatitis Monthly 2015; 15: e18322.Google Scholar
74. Eslamifar, A, et al. Hepatitis G virus exposure in dialysis patients. International Urology and Nephrology 2007; 39: 1257–1263.Google Scholar
75. Ghadir, M, et al. Effect of hepatitis C and B infections on anemia in hemodialysis patients. Journal of Medical Council of Islamic Republic of Iran 2009; 27: Pe9–Pe15, En155.Google Scholar
76. Haghazali, S, et al. Occult HBV infection in hemodialysis patients in Qazvin. Razi Journal of Medical Sciences 2011; 18: 8–15.Google Scholar
77. Hamissi, J, Hamissi, H. Occurrence of hepatitis B and C infection among hemodialyzed patients with chronic renal failure in Qazvin, Iran: a preliminary study. International Journal of Collaborative Research on Internal Medicine & Public Health 2011; 3: 89–96.Google Scholar
78. Jahromi, SA, Nejat, E, Hosseini, M. Prevalence of anti-HCV antibody in haemodialysis patients referring to haemodialysis unit of Jahrom. Journal of Medical Sciences (Jahrom medical journal) 2007; 5: 38–43.Google Scholar
79. Joukar, F, et al. Hepatitis C and hepatitis B seroprevalence and associated risk factors in hemodialysis patients in Guilan province, north of Iran: HCV and HBV seroprevalence in hemodialysis patients. Hepatitis Monthly 2011; 11: 178–181.Google Scholar
80. Kalantari, H, et al. Prevalence and risk factors of hepatitis B and C viruses among hemodialysis patients in Isfahan, Iran. Advanced Biomedical Research 2014; 3: 73.Google Scholar
81. Kassaian, N, et al. Hepatitis C in patients with multi blood transfusion in Isfahan, Iran. Hepatology International 2011; 5(1): 226.Google Scholar
82. Mahdavi, MM, et al. Hepatitis B infection in hemodialysis patients in Tehran province, Iran. Hepatitis Monthly 2009; 9: 206–210.Google Scholar
83. Mak, VM, et al. A study on the prevalence of anti-hepatitis C virus among the hemodialysis patients referred to Sirra hospital of Ahwaz. Jundishapur Scientific Medical Journal 2001; 29: 1–5.Google Scholar
84. Makhlough, A, Jamshidi, M, Mahdavi, MR. Hepatitis C prevalence studied by polymerase chain reaction and serological methods in haemodialysis patients in Mazandaran, Iran. Singapore Medical Journal 2008; 49: 921–923.Google Scholar
85. Mansour-Ghanael, F, et al. Prevalence of hepatitis B and C infection in hemodialysis patients of Rasht (Center of Guilan Province, Northern part of Iran). Hepatitis Monthly 2009; 9: 45–49.Google Scholar
86. Mousavi, SSB, Motemednia, F, Mousavi, MB. Epidemiology of hepatitis e virus infection in patients on chronic hemodialysis. Jundishapur Journal of Microbiology 2014; 7: e6993.Google Scholar
87. Rostami, Z, et al. Health related quality of life in Iranian hemodialysis patients with viral hepatitis: changing epidemiology. Hepatitis Monthly 2013; 13: e9611.Google Scholar
88. Sabur, BBP, Mehrabi, Y. Evaluation of prevalence rate and distribution of the predisposing factors of hepatitis C in hemodialysis patients in Kermanshah province (1999–2000). Behbood Journal 2003; 27: 60–66.Google Scholar
89. Salehi, M, et al. Hepatitis G virus exposure in dialysis patients and blood donors in Isfahan-Iran. International Journal of Preventive Medicine 2014; 5: S219.Google Scholar
90. Samarbaf-Zadeh, AR, et al. Prevalence of hepatitis G virus among hemodialysis and kidney transplant patients in Khuzestan Province, Iran. Jundishapur Journal of Microbiology 2015; 8: e20834.Google Scholar
91. Samimi-Rad, K, Hosseini, M. Hepatitis C virus infection and hcv genotypes of hemodialysis patients. Iranian Journal of Public Health 2008; 37: 146–152.Google Scholar
92. Seyrafian, S, et al. Comparison and prevalence of hepatitis B and C infection and hepatitis B vaccination in hemodialysis patients and staffs in 13 hemodialysis centers in Isfahan (Iran). Nephrology Dialysis Transplantation 2006; 21: 484–484.Google Scholar
93. Somi, MH, et al. Hepatitis C virus infection in dialysis centers of Tabriz, Iran: a multicenter study. Archives of Clinical Infectious Diseases 2007; 2: 23–26.Google Scholar
94. Somi, MH, et al. Risk factors of HCV seroconversion in hemodialysis patients in Tabriz, Iran. Hepatitis Monthly 2014; 14: e17417.Google Scholar
95. Taremi, M, et al. Hepatitis E virus infection in hemodialysis patients: a seroepidemiological survey in Iran. BMC Infectious Diseases 2005; 5: 36.Google Scholar
96. Taziki, O, Espahbodi, F. Prevalence of hepatitis C virus infection in hemodialysis patients. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 2008; 19: 475–478.Google Scholar
97. Toosi, MN, et al. Risk factors and seroprevalence of hepatitis B and C infections among hemodialysis patients in Tehran. Iranian Journal of Pathology 2007; 2: 181–186.Google Scholar
98. Zahedi, MJ, et al. Seroprevalence of hepatitis viruses B, C, D and HIV infection among hemodialysis patients in Kerman province, South-East Iran. Hepatitis Monthly 2012; 12: 339–343.Google Scholar
99. Ziaee, M, Azizee, R, Namaei, MH. Prevalence of HCV infection in hemodialysis patients of South Khorasan in comparison With HBV, HDV, HTLV I/II, And HIV infection. Bangladesh Journal of Medical Science 2014; 13: 36.Google Scholar
100. Abdul-Aziz, M, et al. Prevalence of hepatitis B & C among people attending Kirkuk public health laboratory. Al-Taqani 2001; 23: 6–15.Google Scholar
101. Abdullah, AM, Hardan, A, Latif, II. Genotyping of hepatitis C virus isolates from Iraqi hemodialysis patients by reverse transcription-PCR and one step nested RT-PCR. Diyala Journal of Medicine 2012; 3: 9–18.Google Scholar
102. Abdullah, BA, Khaled, MD, Maarouf, MN. Detection of hepatitis C virus (HCV) by ELISA, RIBA and reverse transcriptase- polymerase chain reaction (RT-PCR) technique among kidney dialysis patients in Nineveh governorate/Iraq. Science Journal of Thi-Qar 2012; 3: 55–67.Google Scholar
103. Al-Dulaimi, SBK, et al. Toxoplasma gondii, HCV, and HBV seroprevalence in haemodialysis patients with chronic renal failure in Al-Kindy Hospital Baghdad, Iraqi. Al-Mustansiriyah Journal of Science 2012; 23: 33–38.Google Scholar
104. Al-Mashhadani, JI. Hepatitis C virus infection among haemodialysis patients in Al-Anbar governorate. Iraqi Journal of Community Medicine 2007; 20: 20–23.Google Scholar
105. Hassan, AS. Prevalence of anti-hepatitis C virus antibodies among blood donors and risky groups in Diyala. Journal of the Faculty of Medicine of Baghdad 2008; 50: 467–470.Google Scholar
106. Khattab, OS. Prevalence and risk factors for hepatitis C virus infection in hemodialysis patients in an Iraqi renal transplant center. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 2008; 19: 110–115.Google Scholar
107. Khattab, OS. How to decrease the prevalence of hepatitis C in Iraqi hemodialysis patients. The Iraqi Postgraduate Medical Journal 2010; 9: 31–35.Google Scholar
108. Mnuti, JK, Al-Abbudi, FA. Hepatitis C virus infection assessment among chronic hemodialysis patients in Al-Kadhmiya teaching hospital. Iraqi Postgraduate Medical Journal 2011; 10: 460–464.Google Scholar
109. Ramzi, ZS, et al. Prevalence and risk factors for hepatitis C virus infection in hemodialysis patients in Sulaimani. Zanco Journal of Medical Sciences 2010; 14: 44–50.Google Scholar
110. Shihab, SS, et al. Viral hepatitis infections in Basrah haemodialysis unit: serological diagnosis and viral loading. European Journal of Experimental Biology 2014; 4: 106–112.Google Scholar
111. Al-Jamal, M, et al. Hepatitis C virus (HCV) infection in hemodialysis patients in the south of Jordan. Saudi Journal of Kidney Diseases and Transplantation 2009; 20: 488.Google Scholar
112. Batchoun, RG, Al-Najdawi, MA, Al-Taamary, S. Anti-ENA antibody profile in hepatitis C patients undergoing hemodialysis. Saudi Journal of Kidney Diseases and Transplantation 2011; 22: 682–688.Google Scholar
113. Batieha, A, et al. Epidemiology and cost of haemodialysis in Jordan. Eastern Mediterranean Health Journal 2007; 13: 654–663.Google Scholar
114. Bdour, S. Hepatitis C virus infection in Jordanian haemodialysis units: serological diagnosis and genotyping. Journal of Medical Microbiology 2002; 51: 700–704.Google Scholar
115. Ghunaimat, M, et al. Point prevalence of hepatitis C antibodies among hemodialysis patients at king Hussein medical center. Journal of the Royal Medical Services 2007; 14: 63–67.Google Scholar
116. Said, RA, et al. Hepatitis C virus infection in hemodialysis patients in Jordan. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 1995; 6: 140–143.Google Scholar
117. Altawalah, H. Prevalence of Blood Borne Viruses in the Dialysis Unit, Mubarak Al-Kabeer Hospital, Kuwait. Idsa: IDWeek 2014, 2014.Google Scholar
118. El-Reshaid, K, et al. Hepatitis C virus infection in patients on maintenance dialysis in Kuwait: epidemiological profile and efficacy of prophylaxis. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 1995; 6: 144–150.Google Scholar
119. Abdelnour, GE, et al. Detection of anti-hepatitis C-virus antibodies and hepatitis C-virus RNA in Lebanese hemodialysis patients. European Journal of Epidemiology 1997; 13: 863–867.Google Scholar
120. Rached, AA, et al. Incidence and prevalence of hepatitis B and hepatitis C viruses in hemodialysis patients in Lebanon. World Journal of Nephrology 2016; 5: 101.Google Scholar
121. Mourani, C, et al. Multicenter study of children with terminal renal failure in Lebanon. Le Journal Medical Libanais the Lebanese Medical Journal 1999; 47: 309–312.Google Scholar
122. Naman, RE, et al. Hepatitis C virus in hemodialysis patients and blood donors in Lebanon. Le Journal Medical Libanais the Lebanese Medical Journal 1996; 44: 4–9.Google ScholarPubMed
123. Alashek, WA, McIntyre, CW, Taal, MW. Epidemiology and aetiology of dialysis-treated end-stage kidney disease in Libya. BMC Nephrology 2012; 13: 1.Google Scholar
124. Alashek, WA, McIntyre, CW, Taal, MW. Hepatitis B and C infection in haemodialysis patients in Libya: prevalence, incidence and risk factors. BMC Infectious Diseases 2012; 12: 265.Google Scholar
125. Daw, MA, et al. Prevalence of hepatitis C virus antibodies among different populations of relative and attributable risk. Saudi Medical Journal 2002; 23: 1356–1360.Google Scholar
126. Elzouki, AN, et al. Prevalence of anti-hepatitis C virus antibodies and hepatitis C virus viraemia in chronic haemodialysis patients in Libya. Nephrology, Dialysis, Transplantation: Official Publication of the European Dialysis and Transplant Association – European Renal Association 1995; 10: 475–476.CrossRefGoogle ScholarPubMed
127. El-Zouki, AY, Bendard, AB, Sharif, MS. HCV in hemodialysis patients in Benghazi, Libya. Annals of Saudi Medicine 1993; 13: 203.Google Scholar
128. Benani, A, et al. HCV genotypes in Morocco. Journal of Medical Virology 1997; 52: 396–398.3.0.CO;2-X>CrossRefGoogle ScholarPubMed
129. Benjelloun, S, et al. Anti-HCV seroprevalence and risk factors of hepatitis C virus infection in Moroccan population groups. Research in Virology 1996; 147: 247–255.Google Scholar
130. Boulaajaj, K, et al. Prevalence of hepatitis C, hepatitis B and HIV infection among haemodialysis patients in Ibn-Rochd University Hospital, Casablanca. Nephrologie and Therapeutique 2005; 1: 274–284.Google Scholar
131. Foullous, A, et al. Epidemiological and virological study of hepatitis c virus infection in hemodialysis (case of six centers) in Morocco. Journal of Biology, Agriculture and Healthcare 2015; 5: 99–105.Google Scholar
132. Lioussfi, Z, et al. Viral hepatitis C and B among dialysis patients at the Rabat University Hospital: prevalence and risk factors. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 2014; 25: 672–679.Google Scholar
133. Sekkat, S, et al. Prevalence of anti-HCV antibodies and seroconversion incidence in five haemodialysis units in Morocco. Nephrologie and Therapeutique 2008; 4: 105–110.Google Scholar
134. Al-Dhahry, SHS, et al. Antibodies to hepatitis C virus in Omani patients with renal disease. Transplantation Proceedings 1992; 24: 1938–1939.Google Scholar
135. Ali, I, et al. Prevalence of HCV among the high risk groups in Khyber Pakhtunkhwa. Virology Journal 2011; 8: 296.Google Scholar
136. Christi, SM, Khan, AM, Bashir, F. Serological monitoring of HCV marker in hemodialysis patients from tertiary care hospitals of Karachi. Medical Forum Monthly 2015; 26: 6–11.Google Scholar
137. Gul, A, Iqbal, F. Prevalence of hepatitis C in patients on maintenance haemodialysis. Journal of the College of Physicians and Surgeons – Pakistan 2003; 13: 15–18.Google Scholar
138. Khan, S, et al. Rising burden of hepatitis C virus in hemodialysis patients. Virology Journal 2011; 8: 438.Google Scholar
139. Khokhar, N, et al. Risk factors for hepatitis C virus infection in patients on long-term hemodialysis. Journal of the College of Physicians and Surgeons Pakistan 2005; 15: 326–328.Google Scholar
140. Mahmud, HM, et al. Hemodialysis patients profile at Dow university of health sciences, Karachi. Pakistan. Pakistan Journal of Medical Sciences 2014; 30: 1327.Google Scholar
141. Mumtaz, A, et al. Erectile dysfunction in haemodialysis patients. Journal of Ayub Medical College Abbottabad 2009; 21: 4–7.Google Scholar
142. Al Zabadi, H, Rahal, H, Fuqaha, R. Hepatitis B and C prevalence among hemodialysis patients in the West Bank hospitals, Palestine. BMC Infectious Diseases 2016; 16: 41.Google Scholar
143. Dumaidi, K, Al-Jawabreh, A. Prevalence of occult HBV among hemodialysis patients in two districts in the northern part of the West Bank, Palestine. Journal of Medical Virology 2014; 86: 1694–1699.Google Scholar
144. El-kader, YE-OA, Elmanama, AA, Ayesh, BM. Prevalence and risk factors of hepatitis B and C viruses among haemodialysis patients in Gaza strip, Palestine. Virology Journal 2010; 7: 210.Google Scholar
145. Abboud, O, Rashid, A, Al-Kaabi, S. Hepatitis C virus infection in hemodialysis patients in Qatar. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 1995; 6: 151–153.Google ScholarPubMed
146. Al-Ghamdi, SM, Al-Harbi, AS. Hepatitis C virus sero-status in hemodialysis patients returning from holiday: another risk factor for HCV transmission. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 2001; 12: 14–20.Google Scholar
147. Al-Jiffri, AM, et al. Hepatitis C virus infection among patients on hemodialysis in Jeddah: a single center experience. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 2003; 14: 84–89.Google Scholar
148. Al-Mugeiren, M, et al. Seropositivity to hepatitis C virus (HCV) in Saudi children with chronic renal failure maintained on haemodialysis. Annals of Tropical Paediatrics 1992; 12: 217–219.Google Scholar
149. Al-Muhanna, FA. Hepatitis C virus infection among hemodialysis patients in the eastern region of Saudi Arabia. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 1995; 6: 125–127.Google Scholar
150. Al Nasser, MN, et al. Seropositivity to hepatitis C virus in Saudi haemodialysis patients. Vox Sanguinis 1992; 62: 94–97.Google Scholar
151. Al Saran, K, et al. Factors affecting response to hepatitis B vaccine among hemodialysis patients in a large Saudi Hemodialysis Center. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 2014; 25: 185–191.Google Scholar
152. Al Shohaib, SS, et al. The prevalence of hepatitis C virus antibodies among hemodialysis patients in Jeddah area, Saudi Arabia. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 1995; 6: 128–131.Google Scholar
153. Alsaran, KA, et al. Effect of hepatitis C virus on hemoglobin and hematocrit levels in Saudi hemodialysis patients. Renal Failure 2009; 31: 349–354.Google Scholar
154. Ayoola, E, et al. Prevalence and significance of antibodies to hepatitis C virus among Saudi haemodialysis patients. Journal of Medical Virology 1991; 35: 155–159.Google Scholar
155. Bahakim, H, et al. Hepatitis C virus antibodies in high-risk Saudi groups. Vox Sanguinis 1991; 60: 162–164.Google Scholar
156. Bernieh, B, et al. Prevalence of hepatitis C virus antibodies in hemodialysis patients in madinah Al munawarah. Saudi Journal of Kidney Diseases Transplantation 1995; 6: 132–135.Google ScholarPubMed
157. Fakunle, YM, et al. Prevalence of antibodies to hepatitis C virus in hemodialysis patients in Riyadh. Annals of Saudi Medicine 1991; 11: 504–506.Google Scholar
158. Huraib, S, et al. High prevalence of and risk factors for hepatitis C in haemodialysis patients in Saudi Arabia: a need for new dialysis strategies. Nephrology, Dialysis, transplantation: Official Publication of the European Dialysis and Transplant Association – European Renal Association 1995; 10: 470–474.Google Scholar
159. Hussein, MM, et al. Observations in a Saudi-Arabian dialysis population over a 13-year period. Nephrology Dialysis Transplantation 1994; 9: 1072–1076.Google Scholar
160. Hussein, MM, et al. The impact of polymerase chain reaction assays for the detection of hepatitis C virus infection in a hemodialysis unit. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 2007; 18: 107–113.Google Scholar
161. Karkar, A, et al. Prevention of viral transmission in HD units: the value of isolation. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 2006; 17: 183–188.Google Scholar
162. Kashem, A, Karim, MR. Prevalence of hepatitis B and C among hemodialysis patients in Najran of Saudi Arabia. Bangladesh Renal Journal 2002; 21: 34–38.Google Scholar
163. Kashem, A, et al. Hepatitis C virus among hemodialysis patients in Najran: prevalence is more among multi-center visitors. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 2003; 14: 206–211.Google Scholar
164. Kumar, R. Hepatitis C virus infection among hemodialysis patients in the Najran region of Saudi Arabia. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 1997; 8: 134–137.Google Scholar
165. Mitwalli, A, et al. Hepatitis C in chronic renal failure patients. American Journal of Nephrology 1992; 12: 288–291.Google Scholar
166. Mitwalli, AH, et al. Hepatitis G virus (HGV) infection in Saudi dialysis patients and healthy controls. Saudi Journal of Gastroenterology : Official Journal of the Saudi Gastroenterology Association 2000; 6: 79–83.Google Scholar
167. Saran, KA, et al. Evaluation of quality of care in a large Saudi hemodialysis center (Prince Salman Center for Kidney Diseases, Riyadh, KSA). Renal Failure 2011; 33: 555–561.Google Scholar
168. Saxena, AK, et al. Prevalence of hepatitis C antibodies among hemodialysis patients in Al-hasa region of Saudi Arabia. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 2001; 12: 562–565.Google Scholar
169. Saxena, AK, Panhotra, BR. The susceptibility of patients with type-2 diabetes to hepatitis C virus infection during long-term haemodialysis. Swiss Medical Weekly 2003; 133: 611–618.Google Scholar
170. Saxena, AK, et al. Impact of dedicated space, dialysis equipment, and nursing staff on the transmission of hepatitis C virus in a hemodialysis unit of the Middle East. American Journal of Infection Control 2003; 31: 26–33.Google Scholar
171. Saxena, AK, Panhotra, BR. The impact of nurse understaffing on the transmission of hepatitis C virus in a hospital-based hemodialysis unit. Medical Principles and Practice 2004; 13: 129–135.Google Scholar
172. Shaheen, FA, et al. Prevalence of hepatitis C antibodies among hemodialysis patients in the Western province of Saudi Arabia. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 1995; 6: 136–139.Google Scholar
173. Shobokshi, OA, et al. Hepatitis C virus seroprevalence rate among Saudis. Saudi Medical Journal 2003; 24: S81–S86.Google Scholar
174. Souqiyyeh, MZ, et al. The annual incidence of seroconversion of antibodies to the hepatitis C virus in the hemodialysis population in Saudi Arabia. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 1995; 6: 167–173.Google Scholar
175. Souqiyyeh, MZ, et al. Dialysis centers in the kingdom of Saudi Arabia. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 2001; 12: 293–304.Google Scholar
176. Soyannwo, MA, et al. Hepatitis C antibodies in haemodialysis and pattern of end-stage renal failure in Gassim, Saudi Arabia. African Journal of Medicine and Medical Sciences 1996; 25: 13–22.Google Scholar
177. Tashkandy, MA, et al. An audit of end-stage renal disease in a tertiary care hospital. Archives of Hellenic Medicine 2012; 29: 207–211.Google Scholar
178. El-Amin, HH, et al. Hepatitis C virus infection in hemodialysis patients in Sudan: two centers’ report. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 2007; 18: 101–106.Google Scholar
179. Gasim, GI, et al. Epidemiology of hepatitis B and hepatitis C virus infections among hemodialysis patients in Khartoum, Sudan. Journal of Medical Virology 2012; 84: 52–55.Google Scholar
180. Suliman, SM, et al. Prevalence of hepatitis C virus infection in hemodialysis patients in Sudan. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 1995; 6: 154–156.Google Scholar
181. Abdulkarim, AS, et al. Hepatitis C virus genotypes and hepatitis G virus in hemodialysis patients from Syria: identification of two novel hepatitis C virus subtypes. The American Journal of Tropical Medicine and Hygiene 1998; 59: 571–576.Google Scholar
182. Othman, B, Monem, F. Prevalence of antibodies to hepatitis C virus among hemodialysis patients in Damascus, Syria. Infection 2001; 29: 262–265.Google Scholar
183. Moukeh, G, et al. Epidemiology of hemodialysis patients in Aleppo city. Saudi Journal of Kidney Diseases and Transplantation 2009; 20: 140.Google Scholar
184. Ayed, K, et al. Hepatitis C virus infection in hemodialysis patients from Tunisia: national survey by serologic and molecular methods. Transplantation Proceedings 2003; 35: 2573–2575.Google Scholar
185. Ben Othman, S, et al. High prevalence and incidence of hepatitis C virus infections among dialysis patients in the East-Centre of Tunisia. Pathologie Biologie 2004; 52: 323–327.Google Scholar
186. Hmaied, F, et al. Hepatitis C virus infection among dialysis patients in Tunisia: incidence and molecular evidence for nosocomial transmission. Journal of Medical Virology 2006; 78: 185–191.Google Scholar
187. Hachicha, J, et al. Viral hepatitis C in chronic hemodialyzed patients in southern Tunisia. Prevalence and risk factors. Annales de medecine interne 1995; 146: 295–298.Google Scholar
188. Hmida, S, et al. HCV antibodies in hemodialyzed patients in Tunisia. Pathologie Biologie 1995; 43: 581–583.Google Scholar
189. Jemni, S, et al. Seropositivity to hepatitis C virus in Tunisian haemodialysis patients. Nouvelle revue francaise d'hematologie 1994; 36: 349–351.Google Scholar
190. Sassi, F, et al. Hepatitis C virus antibodies in dialysis patients in Tunisia: a single center study. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 2000; 11: 218–222.Google ScholarPubMed
191. El Shahat, YI, et al. Hepatitis C virus infection among dialysis patients in United Arab Emirates. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 1995; 6: 157–162.Google Scholar
192. Aman, K, et al. Prevalence and associated factors of hepatitis C virus infection among renal disease patients on maintenance hemodialysis in three health centers in Aden, Yemen: a cross sectional study. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 2015; 26: 380–385.Google Scholar
193. Haidar, NA. Prevalence of hepatitis B and hepatitis C in blood donors and high risk groups in Hajjah, Yemen Republic. Saudi Medical Journal 2002; 23: 1090–1094.Google Scholar
194. Selm, SB. Prevalence of hepatitis C virus infection among hemodialysis patients in a single center in Yemen. Saudi Journal of Kidney Diseases and Transplantation: an Official Publication of the Saudi Center for Organ Transplantation, Saudi Arabia 2010; 21: 1165–1168.Google Scholar
195. Word Health Organization. Global Status Report on Noncommunicable Diseases 2014. World Health Organization, 2014 (http://www.who.int/nmh/publications/ncd-status-report-2014/en/). Accessed May 2017.Google Scholar
196. Grassmann, A, et al. ESRD patients in 2004: global overview of patient numbers, treatment modalities and associated trends. Nephrology Dialysis Transplantation 2005; 20: 2587–2593.Google Scholar
197. Anand, S, Bitton, A, Gaziano, T. The gap between estimated incidence of end-stage renal disease and use of therapy. PLoS ONE 2013; 8: e72860.Google Scholar
198. Zampieron, A, et al. European study on epidemiology and management of hepatitis C virus (HCV) infection in the haemodialysis population part 3: prevalence and incidence. European Dialysis and Transplant Nurses Association/European Renal Care Association Journal 2006; 32: 42–44.Google Scholar
199. Patel, PR, et al. Epidemiology, surveillance, and prevention of hepatitis C virus infections in hemodialysis patients. American Journal of Kidney Diseases 2010; 56: 371–378.Google Scholar
200. Finelli, L, et al. National surveillance of dialysis-associated diseases in the United States, 2002. Seminars in dialysis 2005; 18: 52–61.Google Scholar
201. Johnson, DW, et al. Frequencies of hepatitis B and C infections among haemodialysis and peritoneal dialysis patients in Asia-pacific countries: analysis of registry data. Nephrology Dialysis Transplantation 2009; 24: 1598–1603.Google Scholar
202. Center for disease control and prevention. Recommendations for preventing transmission of infections among chronic hemodialysis patients; 2001. (MMWR recommendations and reports).Google Scholar
203. Zampieron, A, et al. European study on epidemiology and the management of HCV in the haemodialysis population. Part 1: Centre policy. European Dialysis and Transplant Nurses Association/European Renal Care Association Journal 2004; 30: 84–90.Google Scholar
204. MoPH. Syrian Refugees Crisis: Impact on Lebanese Public Hospitals. Lebanon: APIS Health Consulting Group Report: Ministry of public Health, 2016.Google Scholar
205. Daw, MA, Dau, AA. Hepatitis C virus in Arab world: a state of concern. The Scientific World Journal 2012; 2012: 719494.Google Scholar
206. Fabrizi, F, Messa, P. Transmission of hepatitis C virus in dialysis units: a systematic review of reports on outbreaks. The International Journal of Artificial Organs 2015; 38: 471–480.Google Scholar
207. Mahmud, S, et al. Hepatitis C virus genotypes in the Middle East and North Africa: Distribution, diversity, and patterns. Journal of Medical Virology 2017.Google Scholar
208. Ashkani-Esfahani, S, Alavian, SM, Salehi-Marzijarani, M. Prevalence of hepatitis C virus infection among hemodialysis patients in the Middle-East: a systematic review and meta-analysis. World Journal of Gastroenterology 2017; 23: 151–166.Google Scholar
Figure 0

Table 1. Population proportion of hemodialysis (HD) in the Middle East and North Africa (MENA) [40]

Figure 1

Table 2. Studies reporting hepatitis C virus (HCV) antibody prevalence among hemodialysis patients across the Middle East and North Africa

Figure 2

Table 3. Pooled mean estimate for hepatitis C virus (HCV) antibody prevalence among hemodialysis patients across countries of the Middle East and North Africa

Figure 3

Table 4. Pooled mean estimate for hepatitis C virus (HCV) viremic rate among hemodialysis patients across countries of the Middle East and North Africa. HCV viremic rate is the prevalence of HCV chronic infection (HCV RNA positivity) among antibody-positive persons

Figure 4

Table 5. Univariable and multivariable meta-regression models for hepatitis C virus (HCV) antibody prevalence among hemodialysis patients across the Middle East and North Africa

Figure 5

Table 6. Frequency, distribution, and Shannon Diversity Index of hepatitis C virus (HCV) genotypes among hemodialysis patients across the Middle East and North Africa

Supplementary material: File

Harfouche et al supplementary material 1

Harfouche et al supplementary material

Download Harfouche et al supplementary material 1(File)
File 8.3 MB