Global epidemiology of hepatitis C virus in dialysis patients: A systematic review and meta-analysis

Raoul Kenfack-Momo; Marceline Djuidje Ngounoue; Sebastien Kenmoe; Guy Roussel Takuissu; Jean Thierry Ebogo-Belobo; Cyprien Kengne-Ndé; Donatien Serge Mbaga; Elisabeth Zeuko’o Menkem; Robertine Lontuo Fogang; Serges Tchatchouang; Juliette Laure Ndzie Ondigui; Ginette Irma Kame-Ngasse; Josiane Kenfack-Zanguim; Jeannette Nina Magoudjou-Pekam; Arnol Bowo-Ngandji; Maimouna Mahamat; Seraphine Nkie Esemu; Lucy Ndip; Richard Njouom

doi:10.1371/journal.pone.0284169

. 2024 Feb 8;19(2):e0284169. doi: 10.1371/journal.pone.0284169

Global epidemiology of hepatitis C virus in dialysis patients: A systematic review and meta-analysis

Raoul Kenfack-Momo ¹, Marceline Djuidje Ngounoue ¹, Sebastien Kenmoe ^2,^*, Guy Roussel Takuissu ³, Jean Thierry Ebogo-Belobo ⁴, Cyprien Kengne-Ndé ⁵, Donatien Serge Mbaga ⁶, Elisabeth Zeuko’o Menkem ⁷, Robertine Lontuo Fogang ⁸, Serges Tchatchouang ⁹, Juliette Laure Ndzie Ondigui ⁶, Ginette Irma Kame-Ngasse ⁴, Josiane Kenfack-Zanguim ¹, Jeannette Nina Magoudjou-Pekam ¹, Arnol Bowo-Ngandji ⁶, Maimouna Mahamat ^10,¹¹, Seraphine Nkie Esemu ², Lucy Ndip ², Richard Njouom ¹²

Editor: Chen-Hua Liu¹³

¹Department of Biochemistry, The University of Yaounde I, Yaounde, Cameroon

²Department of Microbiology and Parasitology, University of Buea, Buea, Cameroon

³Centre for Food, Food Security and Nutrition Research, Institute of Medical Research and Medicinal Plants Studies, Yaounde, Cameroon

⁴Medical Research Centre, Institute of Medical Research and Medicinal Plants Studies, Yaounde, Cameroon

⁵Epidemiological Surveillance, Evaluation and Research Unit, National AIDS Control Committee, Douala, Cameroon

⁶Department of Microbiology, The University of Yaounde I, Yaounde, Cameroon

⁷Department of Biomedical Sciences, University of Buea, Buea, Cameroon

⁸Department of Animal Biology, University of Dschang, Dschang, Cameroon

⁹Scientific Direction, Centre Pasteur du Cameroun, Yaoundé, Cameroon

¹⁰Faculty of Medicine and Biomedical Sciences, University of Yaoundé 1, Yaoundé, Cameroon

¹¹Hemodialysis Unit, Yaoundé General Hospital, Yaoundé, Cameroon

¹²Virology Department, Centre Pasteur of Cameroon, Yaoundé, Cameroon

¹³National Taiwan University Hospital, TAIWAN

Competing Interests: The authors have declared that no competing interests exist.

^✉

* E-mail: ken_sebas@yahoo.fr

Roles

Raoul Kenfack-Momo: Conceptualization, Data curation, Methodology, Project administration, Validation, Writing – original draft, Writing – review & editing

Marceline Djuidje Ngounoue: Conceptualization, Methodology, Project administration, Validation, Writing – review & editing

Sebastien Kenmoe: Conceptualization, Data curation, Formal analysis, Funding acquisition, Methodology, Project administration, Validation, Writing – original draft, Writing – review & editing

Guy Roussel Takuissu: Data curation, Methodology, Validation, Writing – review & editing

Jean Thierry Ebogo-Belobo: Data curation, Methodology, Validation, Writing – review & editing

Cyprien Kengne-Ndé: Data curation, Formal analysis, Methodology, Validation, Writing – review & editing

Donatien Serge Mbaga: Data curation, Methodology, Validation, Writing – review & editing

Elisabeth Zeuko’o Menkem: Data curation, Methodology, Validation, Writing – review & editing

Robertine Lontuo Fogang: Data curation, Methodology, Validation, Writing – review & editing

Serges Tchatchouang: Data curation, Methodology, Validation, Writing – review & editing

Juliette Laure Ndzie Ondigui: Data curation, Methodology, Validation, Writing – review & editing

Ginette Irma Kame-Ngasse: Data curation, Methodology, Validation, Writing – review & editing

Josiane Kenfack-Zanguim: Data curation, Methodology, Validation, Writing – review & editing

Jeannette Nina Magoudjou-Pekam: Data curation, Methodology, Validation, Writing – review & editing

Arnol Bowo-Ngandji: Data curation, Methodology, Validation, Writing – review & editing

Maimouna Mahamat: Methodology, Validation, Writing – review & editing

Seraphine Nkie Esemu: Methodology, Validation, Writing – review & editing

Lucy Ndip: Methodology, Validation, Writing – review & editing

Richard Njouom: Conceptualization, Methodology, Project administration, Supervision, Validation, Writing – review & editing

Chen-Hua Liu: Editor

PMCID: PMC10852299 PMID: 38330063

Abstract

Dialysis is a replacement therapy for patients with End-Stage Renal Disease (ESRD). Patients on dialysis are at high risk of acquiring hepatitis C virus (HCV), which has become a leading cause of morbidity and mortality in this population. There is a wide range of prevalence of HCV in dialysis populations around the world. It is still unknown how prevalent HCV infection is among worldwide dialysis patients (including those undergoing hemodialysis and peritoneal dialysis). A review was conducted to estimate the global epidemiology of hepatitis C in dialysis patients. We searched PubMed, Excerpta Medica Database (Embase), Global Index Medicus and Web of Science until October 2022. A manual search of references from relevant articles was also conducted. Heterogeneity was evaluated by the χ² test on Cochrane’s Q statistic, and the sources of heterogeneity were investigated using subgroup analysis. In order to assess publication bias, funnel plots and Egger tests were conducted, and pooled HCV prevalence estimates were generated using a DerSimonian and Laird meta-analysis model. The study is registered with PROSPERO under CRD42022237789. We included 634 papers involving 392160 participants. The overall HCV case fatality rate was 38.7% (95% CI = 28.9–49). The global prevalence of HCV infection in dialysis population group were 24.3% [95% CI = 22.6–25.9]. As indicated by UNSD region, country, dialysis type, and HCV diagnostic targeted; Eastern Europe had the highest prevalence of 48.6% [95% CI = 35.2–62], Indonesia had 63.6% [95% CI = 42.9–82], hemodialysis patients had 25.5% [95% CI = 23.8–27.3], and anti-HCV were detected in 24.5% [95% CI = 22.8–26.2]. Dialysis patients, particularly those on hemodialysis, have a high prevalence and case fatality rate of HCV infection. Hemodialysis units need to implement strict infection control measures.

Introduction

Hepatitis C virus (HCV) is a small enveloped RNA virus, 55–65 nm in diameter, that targets the liver, causing mild inflammation (acute hepatitis) or severe and persistent inflammation (chronic hepatitis) [1]. HCV is the major cause of mortality from cirrhosis and/or hepatocellular carcinoma (HCC), and therefore a public health problem [2]. It is estimated that there are 58 million chronic HCV infected people worldwide, and 1.5 million new infections occur each year. As a blood-borne virus, HCV is primarily transmitted by blood. Depending on the geographical region, the transmission routes vary. Among these pathways, transfusions, intravenous drug use (IDU) and dialysis are most widely documented [2, 3]. As a result, dialysis would already be a route of HCV transmission, and needs to be emphasized more and more. Numerous studies have shown that dialysis patients are at high risk of acquiring HCV infections [4–6]. In a systematic review, hemodialysis (HD) significantly increases the likelihood of contracting HCV [7]. In another systematic review, high incidence rates of HCV infection were found in patients on HD [8]. Another study found that HD patients with HCV experience significantly worse quality of life (pruritus, depression, and anorexia) than HD patients without HCV [9]. Dialysis patients are increasingly at risk of HCV liver disease, which has become a major concern for health policy makers and care providers [10, 11]. In fact, individuals with End-Stage Renal Disease (ESRD) suffer from impaired immune systems, resulting in viral infections like HCV not clearing as effectively [12]. Increasing access to diagnosis and treatment is essential for reducing HCV-related mortality and morbidity in dialysis patients, according to WHO. The lack of epidemiological data that can map the pooled prevalence of HCV in worldwide dialysis centres and target those most in need of treatment will prevent this from being possible. HCV prevalence in different dialysis centres has been the subject of several systematic reviews. A number of these studies have been conducted in nations such as Afghanistan, India, Vietnam, China, Iran, Brazil, and Pakistan [7, 13–20].

Another has been conducted in the Middle East and North Africa, Latin America and Caribbean, Asia, and Africa regions [21–25]. A couple of narrative reviews (one on the worldwide magnitude of HCV in HD populations from 1999–2007; the other on HCV transmission in the dialysis setting and prevention strategies) are published [26, 27]. At the global level, two systematic reviews were published on HCV in HD patients. In the first one, the incidence rate (IR) was estimated between 1990–2012; while the most recent one examined the prevalence, associated risk factors, and mortality of hepatitis C infection in hemodialysis patients [8, 28]. Currently, no summary of evidence is available that reports the worldwide pooled prevalence of HCV in dialysis patients (including hemodialysis and peritoneal dialysis). Thus, the present systematic review and meta-analysis was conducted to determine the global prevalence of hepatitis C virus in dialysis patients.

Materials and methods

Data sources and search strategy

A guideline for reporting systematic reviews (S1 Checklist) guided the design of this review (S1 Table) [29]. The search strategy (S2 Table) was applied to four databases: Medline, Excerpta Medica Database (Embase), Global Index Medicus, and Web of Science. The screening of all documents related to HCV infection among dialysis patients worldwide was restricted to English and French. Initially, we conducted our search in December 2021; however, we updated it in October 2022. In November 2022, we conducted manual searches of references from relevant articles and previous systematic reviews to identify any additional relevant references that may have been missed by online searches. A copy of the protocol was registered in PROSPERO under number CRD42022237789.

Study selection

After applying our search strategy, articles were exported to Endnotes version X9 software, where duplicates were removed. RKM and SK independently selected articles based on their titles and/or abstracts on the Rayyan review platform. Fourteen reviewers obtained the full texts and screened potential eligible articles. Discussions and consensus were used to resolve disagreements between reviewers.

Eligibility criteria

The included studies met the following criteria: 1) where cross-sectional, case control and cohort studies; 2) describe the diagnostic method used; 3) performed worldwide, and limited to human studies; 4) reporting HCV prevalence in hemodialysis and peritoneal units without regard to age, gender, sampling approach, ethnicity or clinical presentation, publication year, HCV detection method, or sample type; 5) reporting number of deaths in hemodialysis and peritoneal HCV positives patients. A study with fewer than 10 dialysis patients, case reports, and past reviews that did not provide data on HCV prevalence among dialysis patients were excluded. In addition, duplicates and studies without abstracts or full texts were excluded.

Data extraction

A standardized Google form was used to extract the data independently. Among the extracted data were: the first name of the authors, the year of publication, the study design, the geographical location (UNSD region, WHO region, country income level), the sampling method, the study period, the inclusion criteria, the sample size, the type of dialysis (hemodialysis, peritoneal dialysis), the diagnostic technique used to detect HCV, the diagnostic target (HCV-Ab, HCV-Ag, HCV-RNA), the number of subjects infected by HCV, the number of HCV positive with known outcomes, the number of death in HCV positives patients, and participant characteristics (mean age, SD).

Quality assessment

Using the method developed by Hoy et al. [30], we assessed the quality of the studies included. In this scale, two domains were assessed: internal (target population representation, sampling representation, random selection method, and data source) and external (appropriate inclusion criteria, size adequacy, reliability, validity, mode of sample collection, length of study period, reporting numerator(s) and denominator(s) for HCV prevalence) validity for a total score of 10 points. Study scores of 7–10, 3–6, and 0–3 points were classified as low, moderate, and high risk of bias, respectively (S3 Table).

Data synthesis and analysis

A DerSimonian and Laird random-effects meta-analysis model with inverse variance method was used to pool study-specific estimates [31]. Cochrane’s Q statistic is quantified by I2 values, with I2 values of 25%, 50%, and 75% representing low, moderate, and high heterogeneity, respectively [32]. A funnel plot and Egger test were used to assess publication bias [33]. Subgroup analyses were performed to estimate prevalence variations by HCV diagnostic technique and target, type of dialysis, WHO region, UNSD region, country income level, country, study design, and sampling method. R software version 4.0.3 was used to conduct the analyses [34, 35], and a p value of 0.05 indicated a significant difference.

Results

Results of literature search

In the initial search, we identified 8441 articles, and 3044 duplicates were excluded (Fig 1). We obtained 177 articles from other sources. Based on the titles and abstracts, 4379 articles were excluded. The full-text screening of the remaining 1195 articles resulted in the exclusion of 561 studies for multiple reasons (S4 Table). In the end, 634 articles met our inclusion criteria and were included in the qualitative and quantitative synthesis (S1 Text).

Characteristics of included studies

The characteristics of included studies are shown in S5 and S6 Tables. The majority of the 634 articles included in this review were cross-sectional studies (89.8%). Articles were published between 1990–2022, and participants were recruited between 1968–2022. Study participants ranged in mean age from 7.7 to 72.7 years, and most were recruited from hemodialysis centers (91.8%) and urban areas (57.9%). The male proportion ranged from 12 to 95.4%, the duration of dialysis was between 0.2 and 25.7 years, and the number of dialysis sessions per month was between 3 and 16. According to the WHO Region, most studies were conducted in Europe (34.4%), followed by Eastern Mediterranean (25.1%), Western Pacific (14.4%), America (12.6%), South-East Asia (9.8%) and Africa (2.7%). Most of the studies were conducted in high-income countries (48.7%), upper-middle-income countries (30.6%), lower-middle-income countries (17.5%), and low-income countries (2.4%). Most studies were conducted in Italy (11%), India (7.3%), Iran (7.1%), Japan (6.3%), Brazil (5.8%), and Saudi Arabia (5.4%). The most common HCV diagnostic method was indirect ELISA (66.6%), and most studies indicated a moderate risk of bias (65.9%) (S7 Table).

Case fatality rate estimate of hepatitis C virus infections in dialysis peoples

According to Fig 2, an overall HCV fatality rate of 38.7% (95% CI; 28.9–49) was obtained from 490 HCV-positive dialysis participants recruited from eight studies conducted in eight countries (Morocco, Saudi Arabia, India, Italy, Japan, America, Iran, and China). A high level of heterogeneity was observed between studies that estimated HCV fatality rates (I2 = 77.5% [55.6%; 88.7%], p <0.001). Egger’s regression test result (Table 1) and funnel plot (S1 Fig) showed no publication bias (P = 0.221). Studies with a low bias risk and cross-sectional designs produced similar results in sensitivity analyses.

Table 1. Summary of meta-analysis results for epidemiology of hepatitis C virus in dialysis patients.

	Prevalence. % (95%CI)	95% Prediction interval	N Studies	N Participants	^¶H (95%CI)	^§I² (95%CI)	P heterogeneity
HCV case fatality rate in HD
Overall	38.7 [28.9–49]	[10.6–71.4]	8	490	2.1 [1.5–3]	77.5 [55.6–88.7]	<0.001
Cross-sectional	32.3 [18.4–47.9]	[0–86]	5	294	2.5 [1.7–3.8]	84.1 [64.2–92.9]	<0.001
Low risk of bias	46 [39.8–52.3]	[30.7–61.7]	6	452	1.3 [1–2]	37.7 [0–75.2]	0.155
HCV prevalence in HD
Overall	24.3 [22.6–25.9]	[0–70.8]	667	392160	11.6 [11.5–11.8]	99.3 [99.2–99.3]	<0.001
Cross-sectional	24.2 [22.4–26]	[0–72.7]	597	317425	11.5 [11.3–11.6]	99.2 [99.2–99.3]	<0.001
Low risk of bias	23.9 [21–26.8]	[0–72.6]	229	246733	15.9 [15.7–16.2]	99.6 [99.6–99.6]	<0.001

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CI: confidence interval; N: Number; 95% CI: 95% Confidence Interval; NA: not applicable. ¶H is a measure of the extent of heterogeneity, a value of H = 1 indicates homogeneity of effects and a value of H >1indicates a potential heterogeneity of effects. §: I2 describes the proportion of total variation in study estimates that is due to heterogeneity, a value > 50% indicates presence of heterogeneity.

Global prevalence estimates of hepatitis C virus in dialysis patients

Based on a pooled analysis of 392160 dialysis patients, the prevalence of HCV infection was estimated at 24.3% [95% CI = 22.6–25.9], with considerable heterogeneity (I2 = 99.3% [99.2–99.3], p < 0.001) (Fig 3, Table 1, S2 Fig). The Egger’s test and funnel plot indicated statistically significant publication bias (P = 0.001) (S3 Fig). Anti-HCV prevalence was 24.5% [95% CI = 22.8–26.2]; HCV core antigen (HCV-core Ag) was 16.7% [95% CI = 3.4–37]; anti-HCV/HCV-core Ag was 22.5% [95% CI = 14.6–31.6]; and viral RNA was 23% [95% CI = 17.9–28.7].

Subgroup analyses

A subgroup analysis was conducted to estimate prevalence variations based on HCV diagnostic technique and target, type of dialysis, WHO region, UNSD region, income level, country, study design, and sampling approach (S8 Table). Indonesia (63.6%, 95% CI = 42.9–82), Romania (55.3%, 95% CI = 30.8–78.5), Egypt (55.2%, 95% CI = 47.1–63.2), Kosovo (48.2%, 95% CI = 41–55.5), and Poland (46.7%, 95% CI = 37.9–55.5) had the highest prevalence rates (p<0.001) (Fig 4). Based on WHO region, prevalence was significantly higher in Eastern Mediterranean (27.9%; 95% CI: 24.3–31.6), South-East Asia (25.3%; 95% CI: 16.2–35.6) and Europe (24.6%; 95% CI: 21.9–27.4) (p<0.001). Among UNSD Regions, Eastern Europe (48.6%; 95% CI = 35.2–62), Southeastern Asia (35.5%; 95% CI = 16.5–57.2), Western Asia (34.9%; 95% CI = 29.3–40.6), and Northern Africa (32.9%; 95% CI = 25.7–40.5) had the highest prevalence. Other significant differences were observed based on the type of dialysis (higher prevalence in hemodialysis, p = 0.001) and HCV diagnostic method (higher prevalence when using indirect ELISA, p = 0.003).

Fig 4 — The base map was taken from (https://www.naturalearthdata.com/) and modified with Qgis software.

Discussion

This systematic review and meta-analysis aimed to determine the global epidemiology of hepatitis C virus in dialysis patients. In total, 634 studies were included, published between 1990 and 2022, and conducted on 392160 dialysis patients. A case fatality rate of 38.7% was obtained from eight studies. The global prevalence of HCV infection in dialysis patients was 24.3%. In the Eastern Mediterranean, South-East Asia, and Europe WHO regions, as well as in Eastern Europe, Southeastern Asia, Western Asia, and Northern Africa UNSD regions, the prevalence was significantly higher.

The high HCV fatality rate estimated at 38.7% in this study is not surprising given that many studies have investigated the relationship between anti-HCV antibody and/or HCV-RNA positive status and survival in patients on long-term dialysis have found that mortality is very high in this patient group [36–39]. This excess death is not well understood, and there is active research underway to determine the reasons. The natural course of HCV in dialysis patients has not yet been investigated, even though it differs from other HCV positive patient groups [40]. In HCV-positive dialysis patients, worse quality of life (anemic complications and high hospitalizations) may explain increased mortality [9, 37]. It has also been suggested that HCV infection can adversely affect hemodialysis survival through direct effects such as liver disease (cirrhosis and hepatocellular carcinoma) [36, 41]. However, these direct effects remain unclear due to the lower survival rate of dialysis patients with HCV-positive cirrhosis and hepatocellular carcinoma (HCC) [42]. HCV infection may also negatively impact survival through indirect effects such as cardiovascular disorders, immune deficiencies, and sepsis [43, 44]. The number of articles that allowed us to determine HCV case fatality rate in this study was relatively small (08 articles) and the number of patients who were considered for this purpose was relatively small (N = 490 patients). Our recommendation is to focus on this goal in prospective studies.

The pooled HCV infection rate in world dialysis patients (24.3%) is very close to the 21% found by Greeviroj et al. in their recent meta-analysis [28]. Furthermore, it is fourteen times higher than the prevalence of hepatitis C in the general population, estimated at 1.8% in a recent systematic review [45]. Also, it is much higher than the global prevalence of HCV infection (0.87% in blood donors, 3.4% in men who have sex with men, 17.7% in prisoners, and 2·4% in people living with HIV) [26, 39, 46–50].

Among the settings was HCV is most commonly transmitted, dialysis centres were the most common. Several risk factors were suggested to explain this high prevalence of HCV in dialysis centres: immune response failure, high blood transfusions, inadequate screening of HCV for donated blood, no use of erythropoietin, contamination in the operational process of the dialysis environ, time on dialysis, high prevalence of HCV in dialysis unit, cross-contamination, contaminated hands of staff, understaffing, lack of medically qualified and competent personnel, repeated needle puncture, incomplete disinfection machine [14, 51–70]. Researchers have demonstrated that implementing preventive measures to control infection and a better transfusion policy on dialysis units could lead to declines in HCV prevalence among HD patients [71]. According to some studies, treating HCV-infected patients with dedicated machines could reduce HCV transmission in dialysis units [66, 72–77]. For other studies, isolation of HCV infected subjects in HD units is not required if universal infection control precautions are applied strictly [78–80]. Phylogenetic studies have suggested some mechanisms of HCV spread among hemodialysis patients. There is a high probability of nosocomial dissemination of HCV in dialysis units through cross-contamination (patient-to-patient transmission) [81–88]. Napoli et al. suggested diagnosing the infection during the acute phase to reduce the burden of HCV in hemodialysis patients [89]. Most studies (N = 561) included in this summary used anti-HCV antibodies as HCV diagnostics, which cannot distinguish between resolved and current infections. In addition, because of the long serological window, detecting HCV infection by targeting anti-HCV antibodies could be delayed, and viraemia could occur without HCV antibodies being detected [90–94]. Nucleic Acid Amplification Technology (NAT) is recommended by Kidney Disease Improving Global Outcomes (KDIGO) to diagnose HCV in dialysis patients [10]. NAT technology targeting at viral-RNA has several challenges (requires complex instrumentation), especially in resource-limited settings [95].

For several authors, the HCV-core Ag is more sensitive and specific than NAT techniques and may be an alternative to them [96–100]. But very few studies that determine HCV core antigen prevalence in dialysis population have been carried out (only 04 in this report). The next studies should target HCV-core Ag to determine the precise prevalence of HCV and to better monitor the spread of HCV in dialysis units. We found that prevalence of anti-HCV antibodies, anti-HCV/HCV-core Ag and viral RNA are very close (24.5%, 22.5% and 23% respectively). Anti-HCV/HCV-core Ag is enzyme immunoassay enables to detect the presence of anti-HCV antibodies and/or Core viral antigen in sample. However, only 02 studies have allowed us to determine the prevalence of HCV in dialysis patients, using a 4th generation enzyme immunoassay (Monolisa HCV Ag-Ab), which may been overestimate. Several reports have shown that, most patients with anti-HCV antibodies in HD units have viral genomes [101–105]. Thus, Elzouki al believes that anti-HCV antibodies positive HD patients can be considered potentially infective [106]. Moreover, George et al. failed to confirm the presence of HCV viraemia in anti-HCV antibodies negatives HD patients, and the authors concluded that routine HCV RNA detection in anti-HCV-negative HD patients appears rather unnecessary [104]. However, in other reports, a poor correlation between anti-HCV antibodies and the presence of HCV-RNA was found [12, 106]. In this systematic review we did not performed analysis to determine the correlation between the two markers. Next summary should focus on it.

There are some limitations in the current study. First, our HCV pooled prevalence showed significant heterogeneity and publication bias in the current study. The case fatality rate estimates also showed heterogeneity. Secondly, in some regions and countries, the HCV prevalence in dialysis patients was determine from a single article, and this cannot be representative of the exact burden in these regions or countries.

Third, we only selected articles in English and French. We provided the first global pooled prevalence of HCV infection in dialysis patients (including hemodialysis and peritoneal dialysis) and estimate the case fatality rate of this virus in this population.

There is a high prevalence of HCV infection as well as a high case fatality rate in this study. With an increase in the number of dialysis patients requiring admission, strategies aimed at preventing and eradicating HCV in dialysis units are urgently needed.

Supporting information

S1 Checklist. Preferred reporting items for systematic reviews and meta-analyses checklist.

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S1 Table. Preferred reporting items for systematic reviews and meta-analyses checklist.

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S2 Table. Search strategy in databases.

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S3 Table. Items for risk of bias assessment.

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S4 Table. Main reasons of exclusion of eligible studies.

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S5 Table. Characteristics of included studies.

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S6 Table. Individual characteristics of included studies.

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S7 Table. Risk of bias assessment.

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S8 Table. Subgroup analyses of prevalence of hepatitis C virus in dialysis patients.

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S1 Text. List of included studies.

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S1 Fig. Funnel chart for publications of the hepatitis C virus case fatality rate in dialysis patients.

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S2 Fig. Global prevalence estimate of hepatitis C virus infection in dialysis patients.

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S3 Fig. Funnel chart for publications of the hepatitis C virus prevalence in dialysis patients.

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Data Availability

All relevant data are within the manuscript and its Supporting Information files.

Funding Statement

This project is part of the EDCTP2 programme supported by the European Union under grant agreement TMA2019PF-2705. Grant Recipient: Dr Sebastien Kenmoe. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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PONE-D-23-01990Global Epidemiology of Hepatitis C Virus in Dialysis patients: a systematic review and meta-analysis.PLOS ONE

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Reviewer #1: Yes

Reviewer #2: No

Reviewer #3: Partly

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Reviewer #1: Yes

Reviewer #2: No

Reviewer #3: I Don't Know

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Reviewer #3: No

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Reviewer #1: Thanks for this comprehensive review of the global epidemiology of hepatitis C virus in dialysis patients. There is no major issue to modify.

[minor problem]

1. The abbreviation could be shown in the first place (hepatocellular carcinoma [HCC], line 12, page 17)

Reviewer #2: The authors reported a systemic review and meta-analysis on global epidemiology of hepatitis C virus in dialysis patients. They included 634 papers and concluded that hemodialysis cases have a high prevalence and case fatality rate. They also showed the significant regional variation, and the included papers had a moderate risk of bias, and high index of heterogeneity. The authors targeted an important issue and the results had potentially valuable information for the regional public health issue. However, several issues need to be addressed before further consideration.

Major issue:

2. Numerical errors and inconsistence need a thorough review of the whole article to verify data and made correction. For example, third line of the Discussion part: “392.160” , line 111 “eight studies conducted in seven countries”, in the result table: “8” study, in the discussion ”The number of articles that allowed us to determine HCV case fatality rate in this study was relatively small (07 articles).

3. About 75% of anti-HCV dialysis patient were viremia, and the HCV core antigen method is a relative new methodology. The presented data showed similar prevalence of Anti-HCV, HCV core antigen and HCV RNA without further analysis and discussion may lead to misunderstanding for the readers.

Reviewer #3: The authors did a meta-analysis on the global epidemiology of hepatitis C virus (HCV) infection in dialysis patients, they found that the global prevalence of HCV infection in the dialysis population was 24.3%, the overall case fatality rate was 38.7%, while Eastern Europe and Indonesia had the highest prevalence rates among regions and countries respectively. They concluded that dialysis particularly hemodialysis patients have a high prevalence and case fatality rate of HCV infection, so strategies aimed at preventing and eradicating HCV and strict infection control measures are urgently needed in hemodialysis units. This manuscript was less innovative in study design nor comprehensive in terms of the global point of view, and the conclusions were less informative and robust, (i) a single article report from one country or region is not able to represent its prevalence rate for that country or region, and (ii) it lack reports from Taiwan which make it ‘no data’ on the global map, figure 4. (Lee JJ et al. J Formos Med Assoc 2022 ‘Trends of treated hepatitis B, hepatitis C, and tuberculosis infection in long-term hemodialysis patients in Taiwan: A nationwide survey in 2010-2018.’, Wei YJ, et al. J Viral Hepat 2021 ‘Evolutionary seroepidemiology of viral hepatitis and the gap in hepatitis C care cascades among uremic patients receiving hemodialysis in Taiwan – the Formosa-Like Group.’ etc.), and (iii) there are significant heterogeneity and publication bias in its inclusion studies.

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PLoS One. 2024 Feb 8;19(2):e0284169. doi: 10.1371/journal.pone.0284169.r002

Author response to Decision Letter 0

16 Mar 2023

Review Comments to the Author

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Authors: The legend of the figure now indicates this: “The base map was taken from (https://www.naturalearthdata.com/) and modified with Qgis software.”

Reviewer #1: Thanks for this comprehensive review of the global epidemiology of hepatitis C virus in dialysis patients. There is no major issue to modify.

Authors: We thank the reviewer for this appreciation.

1. The abbreviation could be shown in the first place (hepatocellular carcinoma [HCC], line 12, page 17)

Authors: Thank you for your valuable feedback. We agree with your suggestion and have now included the abbreviation for "hepatocellular carcinoma" (HCC) in the first instance of its use on line 5.

Authors: We thank the reviewer for this summary and appreciation.

1. The high case fatality rate is in line with the well-known high mortality and poor outcome of the HCV dialysis patient. However, little information was provided in the method part. For example, only 8 papers of the 634 papers were included in this part of analysis. More information and discussion about the paper selection criteria, research type, data extraction, data of hospital mortality or long-term mortality need to be addressed. Authors: Thank you for this valuable feedback on our manuscript. We have provided more information regarding case fatality rate on selection criteria, research type in the methods section. We would like to clarify that we conducted a systematic review and meta-analysis to identify and synthesize the best available evidence on the mortality of HCV dialysis patients. We followed the PRISMA guidelines and used a comprehensive search strategy to identify relevant studies. We included only studies that met our inclusion criteria, which were based on the research question and study design. We acknowledge that we included a small number of studies in our analysis, but we believe that they were the most relevant and high-quality studies available.

“The included studies met the following criteria: 1) where cross-sectional, case control and cohort studies; 2) Reporting HCV prevalence in hemodialysis and peritoneal units; 3) reporting number of deaths in HCV positives dialysis patients.”

“The extracted data included: the number of HCV positive with known outcomes, the number of deaths in HCV positives”

2. Numerical errors and inconsistence need a thorough review of the whole article to verify data and made correction. For example, third line of the Discussion part: “392.160”, line 111 “eight studies conducted in seven countries”, in the result table: “8” study, in the discussion ”The number of articles that allowed us to determine HCV case fatality rate in this study was relatively small (07 articles).

Authors: Thank you for your thorough review and for bringing to our attention the numerical errors and inconsistencies in our article. We apologize for any confusion these errors may have caused and appreciate the opportunity to correct them. We have carefully reviewed the manuscript and have made the necessary corrections to address the issues you raised.

Authors: Thank you for your valuable feedback. We acknowledge that the HCV core antigen method is a relatively new methodology, and further analysis and discussion are necessary to address the similarities in the prevalence of Anti-HCV, HCV core antigen, and HCV RNA. In response to your comment, we have revised our manuscript to include a more detailed analysis of the data, including a discussion of the limitations and potential biases associated with the HCV core antigen method. We have also added a section to clarify the similarities and differences between the different testing methods and how they may impact the interpretation of our findings.

Authors: Thank you for the valuable feedback on our manuscript. We appreciate your comments and have carefully considered them. In response to your comments, we have updated our discussion section to highlight the limitations of our study design and the need for more comprehensive global data on HCV prevalence in dialysis patients. Regarding the heterogeneity and publication bias in the included studies, we conducted a subgroup analysis and found that the overall results remained robust. However, we have added a section to our limitations discussing these issues and the potential impact on our conclusions. We have also included the articles you mentioned in the references section. Finally, 13 articles were attributed to Taiwan that had been incorrectly attributed to another country previously. Thank you.

About Lee JJ et al, this article was excluded after reviewer the full-text (article 278 in Appendix 4). Indeed, we included articles with a detailed description of the diagnostic method used. The article by Lee et al., used ICD codes for diagnosis.

“In some regions and countries, the HCV prevalence in dialysis patients was determine from a single article, and this cannot be representative of the exact burden in these regions or countries” ; “our HCV pooled prevalence showed significant heterogeneity and publication bias in the current study”.

PLoS One. doi: 10.1371/journal.pone.0284169.r003

Decision Letter 1

Chen-Hua Liu

27 Mar 2023

Global Epidemiology of Hepatitis C Virus in Dialysis patients: a systematic review and meta-analysis.

PONE-D-23-01990R1

Dear Dr. Kenmoe,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

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Chen-Hua Liu

Academic Editor

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #1: Yes

Reviewer #2: Yes

**********

6. Review Comments to the Author

Reviewer #1: Thanks for the comprehensive review of the global epidemiology of the hepatitis C virus in dialysis patients. The authors have replied to most major issues addressed by reviewers, and I have no more problems to address.

Reviewer #2: (No Response)

**********

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Reviewer #1: No

Reviewer #2: No

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PLoS One. doi: 10.1371/journal.pone.0284169.r004

Acceptance letter

Chen-Hua Liu

28 Mar 2023

PONE-D-23-01990R1

Global Epidemiology of Hepatitis C Virus in Dialysis patients: a systematic review and meta-analysis.

Dear Dr. Kenmoe:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

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Thank you for submitting your work to PLOS ONE and supporting open access.

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on behalf of

Dr. Chen-Hua Liu

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

S1 Checklist. Preferred reporting items for systematic reviews and meta-analyses checklist.

(PDF)

Click here for additional data file.^{(54.3KB, pdf)}

S1 Table. Preferred reporting items for systematic reviews and meta-analyses checklist.

(PDF)

Click here for additional data file.^{(139.9KB, pdf)}

S2 Table. Search strategy in databases.

(PDF)

Click here for additional data file.^{(84KB, pdf)}

S3 Table. Items for risk of bias assessment.

(PDF)

Click here for additional data file.^{(195.7KB, pdf)}

S4 Table. Main reasons of exclusion of eligible studies.

(PDF)

Click here for additional data file.^{(345.2KB, pdf)}

S5 Table. Characteristics of included studies.

(PDF)

Click here for additional data file.^{(139.8KB, pdf)}

S6 Table. Individual characteristics of included studies.

(PDF)

Click here for additional data file.^{(948.4KB, pdf)}

S7 Table. Risk of bias assessment.

(PDF)

Click here for additional data file.^{(683.3KB, pdf)}

S8 Table. Subgroup analyses of prevalence of hepatitis C virus in dialysis patients.

(PDF)

Click here for additional data file.^{(3.1MB, pdf)}

S1 Text. List of included studies.

(PDF)

Click here for additional data file.^{(322.3KB, pdf)}

S1 Fig. Funnel chart for publications of the hepatitis C virus case fatality rate in dialysis patients.

(PDF)

Click here for additional data file.^{(110.1KB, pdf)}

S2 Fig. Global prevalence estimate of hepatitis C virus infection in dialysis patients.

(PDF)

Click here for additional data file.^{(170.8KB, pdf)}

S3 Fig. Funnel chart for publications of the hepatitis C virus prevalence in dialysis patients.

(PDF)

Click here for additional data file.^{(204.9KB, pdf)}

Data Availability Statement

All relevant data are within the manuscript and its Supporting Information files.

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PERMALINK

Global epidemiology of hepatitis C virus in dialysis patients: A systematic review and meta-analysis

Raoul Kenfack-Momo

Marceline Djuidje Ngounoue

Sebastien Kenmoe

Guy Roussel Takuissu

Jean Thierry Ebogo-Belobo

Cyprien Kengne-Ndé

Donatien Serge Mbaga

Elisabeth Zeuko’o Menkem

Robertine Lontuo Fogang

Serges Tchatchouang

Juliette Laure Ndzie Ondigui

Ginette Irma Kame-Ngasse

Josiane Kenfack-Zanguim

Jeannette Nina Magoudjou-Pekam

Arnol Bowo-Ngandji

Maimouna Mahamat

Seraphine Nkie Esemu

Lucy Ndip

Richard Njouom

Roles

Abstract

Introduction

Materials and methods

Data sources and search strategy

Study selection

Eligibility criteria

Data extraction

Quality assessment

Data synthesis and analysis

Results

Results of literature search

Fig 1. Flow diagram for retrieving and processing article selection.

Characteristics of included studies

Case fatality rate estimate of hepatitis C virus infections in dialysis peoples

Fig 2. Case fatality race of hepatitis C virus infections in dialysis population.

Table 1. Summary of meta-analysis results for epidemiology of hepatitis C virus in dialysis patients.

Global prevalence estimates of hepatitis C virus in dialysis patients

Fig 3. Prevalence estimates of hepatitis C virus infection in dialysis patients.

Subgroup analyses

Fig 4. Global prevalence of hepatitis C virus infection in dialysis patients.

Discussion

Supporting information

Data Availability

Funding Statement

References

Decision Letter 0

Chen-Hua Liu

Roles

Author response to Decision Letter 0

Decision Letter 1

Chen-Hua Liu

Roles

Acceptance letter

Chen-Hua Liu

Roles

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

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