https://orcid.org/0009-0003-1199-1479
Figures
Abstract
Background
Healthcare workers (HCWs) are at higher risk of contracting hepatitis B virus (HBV) and hepatitis C virus (HCV) infections. Currently, there is no estimate of pooled data on the prevalence of HBV and HCV infections among HCWs in the country. Thus, this review aimed to determine the pooled prevalence of hepatitis B and C infections among HCWs in Ethiopia.
Materials and methods
A comprehensive literature search was conducted using electronic databases, including PubMed, Cochrane Library, Science Direct, Hinari, and African Journals Online to identify pertinent articles from the inception to April 2024. The protocol has been registered in the International Prospective Register of Systematic Reviews (PROSPERO; CRD42024527940) and conducted per the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. Data were extracted independently by two authors and analyzed using STATA version 11 software. A random-effect model and Egger’s test were computed to estimate the pooled prevalence and assess publication bias, respectively.
Results
A total of 18 studies involving4,948 healthcare workers were included in this review to estimate the pooled prevalence of HBV and HCV infections among HCWs in Ethiopia. The overall prevalence of HBV was 5.93% (95% CI; 3.22–8.63). The sub-group analysis showed that the prevalence of HBV among medical waste handlers and health professionals was8.6% (95% CI; 3.01–14.13) and 4.98% (95% CI; 1.85–8.11), respectively. The combined prevalence of HCV was 1.12% (95% CI; -4.19–6.43). In the sub-group analysis, the prevalence of HCV among medical waste handlers and health professionals was1.44% (95% CI; -5.28–8.18) and 0.59% (95% CI; -8.09–9.27), respectively.
Conclusion
In this review, we found a higher (5.93%) and moderate (1.12%) prevalence of HBV and HCV infections, respectively among Ethiopian HCWs. Therefore, to reduce the infectious burden of HBV and HCV among HCWs; there is a need to strict adherence to infection prevention and control measures. In addition, adequate HBV vaccination coverage for HCWs is mandatory to reduce the burden of HBV infection in the country.
Citation: Girmay G, Bewket G, Amare A, Angelo AA, Wondmagegn YM, Setegn A, et al. (2024) Seroprevalence of viral hepatitis B and C infections among healthcare workers in Ethiopia: A systematic review and meta-analysis. PLoS ONE 19(11): e0312959. https://doi.org/10.1371/journal.pone.0312959
Editor: Livia Melo Villar, FIOCRUZ, BRAZIL
Received: April 20, 2024; Accepted: October 15, 2024; Published: November 7, 2024
Copyright: © 2024 Girmay et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the article and its supporting information files.
Funding: The author(s) received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Abbreviations: Anti-HCV, Antibody to Hepatitis C Virus; CIA, Chemiluminescent immunoassay; ELISA, Enzyme-linked immunosorbent assay; HBsAg, Hepatitis B surface antigen; HBV, Hepatitis B Virus; HCV, Hepatitis C Virus; HCWs, Healthcare workers; PRISMA, Preferred Reporting Items for Systematic Reviews and Meta-Analyses; WHO, World Health Organization
Introduction
Hepatitis B virus (HBV) and hepatitis C virus (HCV) are the two most prevalent types of viral hepatitis and are common causes of cirrhosis, hepatocellular carcinoma, and chronic hepatitis infection in developing countries [1, 2].Viral hepatitis caused by hepatitis B and C viruses is the sixth-leading cause of morbidity and mortality worldwide. In 2016, around 292 million individuals were estimated to have had a chronic HBV infection, and 71.1 million to have had a chronic HCV infection [3, 4]. About 70 million individuals in Africa suffer from chronic viral hepatitis; 60 million of these cases are caused by HBV and 10 million by HCV infections. Ethiopia is also considered to have a medium to high prevalence of viral hepatitis [5, 6].
Healthcare workers (HCWs) are more likely to be exposed to HBV and HCV infections. Those HCWs, particularly Health professionals and medical waste handlers have a four-fold increased risk of contracting HBV and HCV infections compared to the general public who do not work in healthcare settings [7, 8]. Healthcare workers are commonly at risk of acquiring HBV and HCV infections by percutaneous exposure to contaminated sharp instruments or mucosal-cutaneous exposure to possibly infectious blood or blood products [7, 9]. Based on the World Health Organization (WHO) report, from a total of 36 million HCWs across the world; about 3 million of them could encounter sharp and needle stick injuries annually. Thus, around two and one million HCWs have been exposed to the risk of HBV and HCV infections, respectively [9, 10]. In addition, nearly half of African HCWs are occupationally exposed to blood products and body fluids, thus appears to be an increased incidence of hepatitis B and C viruses among HCWs in the continent [11, 12].
Assessing the relative contributions of HBV and HCV to the prevalence of liver disease is essential for setting public health strategies and strengthening preventative measures [13, 14]. Despite, the WHO’s recommendations for the hepatitis B vaccine, the vaccination coverage among HCWs in the country is insufficient as evidenced by a meta-analysis report only 20% of Ethiopian HCWs had received a full-dose HBV vaccine [15, 16]. Several studies have been conducted in Ethiopia on the prevalence of HBV and HCV infections with varying results [17–21] and the pooled prevalence is still uncertain. For instance, the prevalence of HBV was 2.5% in southwest Ethiopia [17], 6.3% in Addis Ababa [22], and 9.6% in eastern Ethiopia [23]. Besides, the prevalence of HCV was 0.42% in southwest Ethiopia [17] and 1.59% in Addis Ababa [18]. Currently, no estimate of pooled data shows the prevalence of HBV and HCV among HCWs in the country. Thus, this review aimed to determine the pooled prevalence of hepatitis B and C infections among HCWs in Ethiopia.
Methods
Study design and protocol registration
This systematic review and meta-analysis were performed per the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [24] (S1 Table). The protocol has been registered in the International Prospective Register of Systematic Reviews (PROSPERO), with a reference number; CRD42024527940.
Search strategy
A comprehensive systematic literature search was carried out using electronic databases, including PubMed, Cochrane Library, Science Direct, Hinari, and African Journals Online, to find all relevant articles reporting the prevalence of HBV and HCV viruses among HCWs in Ethiopia from the inception to April 2024. Additional searches were also conducted to find relevant studies using Google Scholar, Google, manual searching, and cross-references of identified primary studies and/or review articles. We applied the search terms separately and in combination with Boolean operators such as "OR" and "AND". The following search strategy has been developed for PubMed and then customized for other electronic databases: (((((((((((Seroprevalence) OR (Prevalence)) AND ("hepatitis B virus")) OR ("HBV")) OR ("hepatitis C virus")) OR ("HCV"))) OR (("hepatitis viruses"))) AND (healthcare workers)) OR (health professional)) OR (healthcare provider)) OR (medical waste handler) AND (Ethiopia [MeSH]).
Eligibility criteria
Inclusion criteria.
We included studies based on the condition/context/population (CoCoP) approach. Healthcare workers (P) are defined in this review as physicians, clinical nurses, medical laboratory professionals, midwives, medical assistants, and medical waste handlers/collectors who have direct contact with patient body fluids, including blood, sperm, and stool samples, as well as exposure to sharp objects and needle stick injuries. Studies conducted in Ethiopia (Co) that are cross-sectional, case-control, and cohort in nature reported the seroprevalence of HBV and/or HCV infection (Co), with no restriction in the year of publication. Studies using the hepatitis B surface antigen (HBsAg) and anti-HCV antibody for HBV and HCV diagnosis respectively were included in this review.
Study selection and quality assessment
All potentially suitable papers were examined following duplicates or ineligible papers were removed. Full-text articles were reviewed per the eligibility criteria to identify studies for inclusion or exclusion in the current study. Relevant information was extracted from all eligible studies by two independent review authors (GG and MA) and discrepancies between the authors were addressed through discussion with the third review author (AA). The Joana Briggs Institute (JBI) critical appraisal checklist for simple prevalence studies was used to evaluate the quality of the included studies [25]. The JBI checklist is composed of 9 questions. (Q1) Was the sample frame appropriate to address the target population? (Q2) Were study participants sampled appropriately? (Q3) Was the sample size adequate? (Q4) Were the study subjects and the setting described in detail? (Q5) Was the data analysis conducted with sufficient coverage of the identified sample? (Q6)Were valid methods used for the identification of the condition? (Q7) Was the condition measured in a standard, reliable way for all participants? (Q8) Was there an appropriate statistical analysis? (Q9) Was the response rate adequate, and if not, was the low response rate managed appropriately? A score of 1 was given for answering "Yes" to each question, while 0 was given for answering "Not reported" or "Not appropriate." Subsequently, the individual response scores were tallied to arrive at a final score that ranged from 0 to 9.Based on the assigned points, the authors decided to categorize the included articles’ quality as high (7 to 9), moderate (4 to 6), or low (0 to 3) (S2 Table).
Data extraction
Two review authors (GG and MA) independently evaluated the methodological quality of the included studies and extracted all the relevant information; discrepancies were addressed through discussion with a third review author (AA). A standardized data collection form was used to collect information on the publication year, study period, study setting/region, study population, sample size, study design, sampling procedure/method, diagnostic methods used to detect HBsAg or anti-HCV, and HBV vaccination status.
Statistical methods and analysis
The extraction and entry of all the relevant data were performed using Microsoft Excel and exported to Stata version 11 software for analysis. The pooled prevalence of HBV and/or HCV with 95% confidence intervals was depicted using a forest plot. An index of heterogeneity (I2 statistic) was used to assess the degree of heterogeneity among the studies. The level of heterogeneity was interpreted as Low, moderate, and high when the values of the I2 statistic became 25%, 50%, and 75%, respectively [26]. A random-effects model was used in all pooled analyses due to the variations in the prevalence of included studies. The pooled prevalence of HBV and/or HCV among different study populations, regions, and other parameters was assessed using the sub-group analysis. The presence of publication bias was demonstrated using a funnel plot and Egger’s test statistics. A p-value < 0.05 in Egger’s test was considered as evidence of significant publication bias.
Results
Literature search results
A total of 1,491 studies published between December 1989 and July 2023 that were retrieved from initial electronic searches using international databases, Google Scholar, Google search, and manual searching. Seven hundred sixty-eight records were removed due to duplicates, from the screened 723 studies; 689 studies were excluded following title and abstract screening. In addition, 16 studies were excluded following full-text screening. Thus, a total of 18 eligible studies were included in this systematic review and meta-analysis (Fig 1).
Characteristics of the included studies
A total of 18eligible studies [17–23, 27–37] on 4,948 healthcare workers were included in this systematic review and meta-analyses. Of those, 3,723 and 1,225 were health professionals and medical waste handlers, respectively. Fortunately, all the studies used a cross-sectional study design. Of the 18 included studies, 10 studies used a convenient sampling, followed by 5 studies used simple random sampling, and the other 2 and 1 studies used multi-stage sampling and systematic random sampling, respectively. The majorities (12 studies) were conducted between the years 2013 to 2021 whereas; the other 5 studies were conducted between the years 2001 to 2012. On the other hand, only one study was conducted before the year 2000. Of the 18 studies included, 6 studies were conducted in Addis Ababa city administration, 5 in the Amhara region, 4 in the Oromia region, 2 in the Harari region, and 1 in the Sidama region (Table 1).The minimum and maximum number of study participants included were 70 in Amhara region [28] and 612 in Oromia region [35], respectively. Of the 4, 948included healthcare workers, 2, 938 of them were females. The mean age of study participants ranged from 25 to 37.6 years. Of the 18 studies, 7 studies reported the prevalence of both HBV and HCV, whereas 11 studies reported HBV alone. Ten and 7 studies determined the seropositivity of HBsAg and/or anti-HCV using the enzyme-linked immunosorbent assay (ELISA) and rapid test kits, respectively. Whereas, only a single study determined HBsAg seropositivity using a chemiluminescent immunoassay (CIA) (Table 1).
Prevalence of HBV and HCV infections among healthcare workers in Ethiopia
This systematic review and meta-analysis included 18 eligible studies to estimate the pooled prevalence of HBV and HCV infection among HCWs. The minimum and maximum prevalence was 0.64% (Addis Ababa) [27] and 20.40% (Harari) [34], respectively for HBV and 0.42% (Oromia) [17] and 4.30% (Amhara) [28], respectively for HCV.A total of 18 studies reported the prevalence of HBV among HCWs, thus the pooled prevalence of HBV using a random effect model was 5.93% (95% CI; 3.22–8.63) with no evidence of heterogeneity (I2 = 0.0%; p = 0.847) (Fig 2). Whereas, the pooled prevalence of HCV from 7 studies using a random effect model was 1.12% (95% CI; -4.19–6.43), no evidence of heterogeneity (I2 = 0.0%; p = 1.000) (Fig 3).
Sub-group analysis
The prevalence of HBV and HCV among different types of sampling methods, types of the study population/group, study year, study setting/regions, and the types of diagnostic methods to detect HBsAg and/or anti-HCV were addressed using sub-group analysis by random effect model.The sub-group analysis by study population identified that the pooled prevalence of HBV among medical waste handlers and health professionals was8.6% (95% CI; 3.01–14.13) (I2 = 5.3%; p =
0.386) and 4.98% (95% CI; 1.85–8.11) (I2 = 0.0%; p = 0.968), respectively (Table 2).
This meta-analysis also found1.44% (95% CI; -5.28–8.18) (I2 = 0.0%; p = 0.999) and 0.59% (95% CI; -8.09–9.27) (I2 = 0.0%; p = 0.970) combined prevalence of HCV among medical waste handlers and health professionals, respectively (Table 3). Analysis of sub-group by study region identified that the highest prevalence of HBV was found among studies conducted in Harari region; 14.60% (95% CI; 4.19–25.00) with moderate heterogeneity (I2 = 54.7; p = 0.137) and the lowest HBV prevalence was found in a study conducted in Sidama region; 1.32% (95% CI; -14.48–17.11). Similarly, the highest prevalence of HCV was observed among studies conducted in the Amhara region; 1.62% (95% CI; -7.70–10.94) (I2 = 0.0%; p = 0.969) whereas, the lowest prevalence of HCV was found in a study done in Oromia region; 0.42% (95% CI; -12.21–13.04) (Tables 2 and 3).
The highest combined prevalence of HBV per year of study was found among studies conducted between the years 2001 and 2012; 6.39% (95% CI; -0.09.19–12.87) (I2 = 0.0%; p = 0.943) and the lowest prevalence of HBV was observed in a study done before the year 2000; 5.71 (95% CI; -3.39–14.80). For HCV, the combined prevalence was 1.24% (95% CI; -4.99–7.46) (I2 = 0.0%; p = 0.999) and 0.82% (95% CI; -9.37–11.01) (I2 = 0.0%; p = 0.983) among studies conducted between the years 2001 to 2012 and 2013 to 2021, respectively (Tables 2 and 3).
This meta-analysis also performed sub-group analysis by the diagnostic methods used and identified that the pooled prevalence of HBV was found 8.37% (3.63–13.10) (I2 = 13.5%; p = 0.327), 4.70% (95% CI; 1.03–8.38) (I2 = 0.0%; p = 0.996), and 0.64% (95% CI; -10.40–11.68) among studies detected HBsAg using a rapid test kit, ELISA, and CIA, respectively (Table 2). Besides, the combined prevalence of HCV among studies that detected anti-HCV using ELISA and rapid test kit was 1.20% (95% CI; -4.69–7.09) (I2 = 0.0%; p = 0.999) and 0.79% (95% CI; -11.50–13.09) (I2 = 0.0%; p = 0.979), respectively (Table 3).
Prevalence of HBV vaccination status among healthcare workers in Ethiopia
In this systematic review and meta-analysis study we estimated the pooled prevalence of HBV vaccination status among HCWs. Even though, all 18 studies included in this review had not reported complete data on the number of fully vaccinated HCWs; data from 9 studies showed that the prevalence of HBV full-dose vaccination status among HCWs was 14.62% (95% CI; -15.63–44.87) (I2 = 98.9%; p = < 0.001). The minimum and maximum prevalence of HBV vaccination status was 1.6% (Addis Ababa) (95% CI; -9.39–12.59) [27] and 83.33% (Harari) (95% CI; 79.48–87.18) [23], respectively (S1 Fig).
Publication bias
The presence of publication bias was assessed statistically for the included studies using Egger’s statistics test at a significant level of less than 0.05. The findings of the Egger test revealed that there was no publication bias in both HBV (p = 0.846) and HCV (p = 0.12) (Tables 4 and 5).
These results were depicted using a funnel plot which showed a symmetrical display of the prevalence reported by all the included studies in this systematic review and meta-analysis (Figs 4 and 5).
Discussion
In this systematic review and meta-analysis, we estimated the pooled prevalence of HBV and HCV infection among HCWs in Ethiopia. A total of 4,948 HCWs from 18 studies was used to determine the combined prevalence of HBV and/or HCV. Thus, the pooled prevalence of HBV and HCV was 5.93% (95% CI; 3.22–8.63) and 1.12% (95% CI; -4.19–6.43), respectively. The combined prevalence of HBV in this meta-analysis was almost similar to the previous meta-analysis conducted in Ethiopia [38] which reported 6% HBV pooled prevalence. The current prevalence of HBV was consistent with the WHO HBV infection endemicity classification with 5–7% of HBsAg prevalence [39] and comparable with the previous meta-analysis report from Ethiopia;7.4% [6]. Moreover, the prevalence of HBV in this study was also in line with previous meta-analysis studies conducted among HCWs from Africa; 6.81% [40], and Asia and Africa; 5% [41].
On the other hand, the pooled prevalence of HBV in this study was higher than previous global meta-analysis reports among HCWs and waste collectors [42–44], where the combined prevalence of HBV ranged from 0.04% to 2.3%. In addition, the prevalence of HBV in this study was higher compared with previous reports among HCWs from eastern Mediterranean and Middle Eastern countries [45] and Iranian healthcare workers [46] with an HBV pooled prevalence of 0.4% and 2.77%, respectively. These discrepancies in the variation of HBV prevalence might be due to the difference in the disease distribution among the developed and middle-income countries in the world [2, 47]. This variation might be also attributed to inadequate access to HBV screening and patient management, lack of HBV vaccination utility, and limited adherence to WHO safety recommendations among HCWs and medical waste collectors in developing countries [16, 48, 49]. Besides, the combined prevalence of HBV in this study was lower than previous reports from Sudan [50], Nigeria [51], and Vietnam [52], where the prevalence of HBV among the general population was 12.07%, 9.5%, and 10.5%, respectively. The current prevalence of HBV was also lower compared with a previous meta-analysis from Brazil among waste collectors [53]. The variation in the combined prevalence observed among different regions of the world might be due to the difference in study population (general population and/or waste collectors versus HCWs and/or medical waste handlers) and the difference in HBV diseases distribution.
Whereas, the current combined prevalence of HCV was comparable with previous Ethiopian meta-analysis studies [6, 54] which reported that the pooled prevalence of HCV in the country was 2% and 3.1%, respectively. The prevalence of HCV in this study was in line with previous meta-analysis reports from Vietnam [52] and Sudan [50], where the HCV prevalence reports were 0.26% and 2.74%, respectively. Moreover, our finding on the prevalence of HCV was comparable with previous Global reports among waste handlers; 0.08% [43] and African meta-analysis study among HCWs; 5.58% [40]. This variation in the prevalence of HCV across different regions might be due to the different rates of exposure to HCV among HCWs and/or medical waste handlers versus the general population. The possible reason for the discrepancies might be that HCWs and/or medical waste handlers are highly vulnerable to occupational-associated blood and body fluid exposure as compared to the general populations, where the major route of HCV transmission is through contact with blood and body fluids [55, 56].
The sub-group analysis on the prevalence of HBV among HCWs by the study population was observed in Ethiopia. Our finding showed that the combined prevalence of HBV was higher among medical waste handlers (8.6%) than health professionals (4.98%). Besides, the prevalence of HCV was almost comparable between health professionals (0.59%) and medical waste handlers (1.44%). Our finding was per the fact that medical waste handlers had a higher rate of exposure to sharp materials, blood products, and body fluids [57, 58]. This variation in the prevalence of HBV among medical waste handlers versus health professionals might be due to the difference in the HBV vaccination coverage, limited knowledge and awareness of medical waste handlers on the transmission of HBV and waste management, low adherence of medical waste handlers to the WHO safety recommendations [20, 59, 60]. The prevalence of HBV among HCWs in this study was observed indifferent regions of Ethiopia which showed that a higher combined prevalence of HBV was observed in the Harari region (14.60%)than Amhara region (4.86%), Addis Ababa city administration (4.70%), Oromia region (4.20%), and Sidama region (1.32%). Besides, the prevalence of HCV in this study was almost comparable across regions of Ethiopia, where the HCV prevalence was 1.62% in the Amhara region, 1.16% in Addis Ababa city administration, 0.66% in the Sidama region, and 0.42% in Oromia region. Accordingly, our findings showed that a higher prevalence of HBV was observed in the Harari region. This finding was supported by previous Ethiopian studies conducted in eastern Ethiopia which reported a higher burden of HBV among different population groups [61–63],where the HBV prevalence was 11.5%, 11.7%, and 7.85%, respectively. The prevalence of HBV among HCWs showed that there was a slight decrement across different categories of study years as it was 6.39% and 5.84% in studies conducted between the years 2001–12 and 2013–21, respectively. This slight decrement in the combined prevalence of HBV across study years might be due to a slightly increasing awareness of HBV transmission, diagnosis, and implementation of preventive medicines across years which was supported by the recent study done by Chonka et al. showed that the majority of study participants had a good knowledge to HBV infection [64]. The combined prevalence of HBV among HCWs by rapid test kit and ELISA was 8.37% and 4.70%, respectively. Accordingly, the result suggested that a higher prevalence of HBV was observed by rapid test kits than by ELISA tests. Even though, rapid test kits are widely employed in developing countries to screen HBV and HCV infections [65]. The higher prevalence of HBV by rapid test kits in this meta-analysis was supported by a previous cohort study conducted in France by Julie et al. which showed that rapid tests could produce a false negative result and a limited positive predictive value [66].
In this systematic review and meta-analysis study we estimated the pooled prevalence of HBV full-dose vaccination status among HCWs. Data from 9 studies showed that the prevalence of HBV full-dose vaccination status was 14.62%. Accordingly, results suggested that the prevalence of fully vaccinated HCWs was still low. Our finding was supported by previous meta-analysis studies [16, 67] which showed that the prevalence of full-dose HBV vaccine coverage among HCWs was 20.04% and 24.7%, respectively. This variation in the prevalence of HBV vaccine coverage might be attributed to the lack of cost-effective strategies that maximize the benefit of HBV vaccination to HCWs and limited access and utilization of HBV vaccine [68].
As strength, this study strictly adhered to the PRISMA guidelines and applied a comprehensive literature search, quality assessment, and data extraction from relevant articles by two independent authors, and discrepancies were resolved by the third author. In addition, we included all studies conducted in Ethiopia from December 1989 to April 2024which helps to generalize the pooled prevalence of HBV and HCV infection in the country. However, as a limitation, this study included some studies containing small sample sizes, which might affect the combined prevalence of HBV and HCV infection among HCWs in the country.
Conclusion and recommendations
In this review, we found a higher and moderate prevalence of HBV and HCV infections, respectively among Ethiopian HCWs, particularly among Health professionals and medical waste handlers. Thus, strict adherence to infection control measures, effective implementation of prevention and control policies for HBV and HCV infections. In addition, adequate HBV vaccination coverage for HCWs is needed to reduce the burden of HBV infection in the country.
Supporting information
S1 Table. Showing the Preferred Reporting Items for systematic review and meta-analysis (PRISMA) 2020 checklist.
https://doi.org/10.1371/journal.pone.0312959.s001
(DOCX)
S2 Table. Quality assessment of individual studies included for meta-analysis on the prevalence of HBV and HCV among healthcare workers in Ethiopia.
https://doi.org/10.1371/journal.pone.0312959.s002
(DOCX)
S1 Fig. The forest plot showing the pooled prevalence of HBV vaccination status among healthcare workers in Ethiopia.
https://doi.org/10.1371/journal.pone.0312959.s003
(TIF)
Acknowledgments
The authors of this review would like to express their gratitude to all the authors of primary studies.
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