https://orcid.org/0000-0001-6597-5755
Figures
Abstract
Background
Due to its invasive procedure patients on hemodialysis (HD) are at high risk of infections. Infections acquired in dialysis units can prolong hospitalization date and/or prolong illness in patients, and increase treatment cost. There are no adequate data on the prevalence of Hepatitis B virus (HBV) and Hepatitis C virus (HCV) infections in HD patients. Therefore, this study aimed to estimate the pooled prevalence and associated factors of HBV and HCV infections among HD patients in Africa.
Method
The databases PubMed, Medline, EMBASE, Cochrane library, web of science, African Journals Online, Science Direct, and Google Scholar were searched to identify relevant studies. The review was performed based on Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. Data were extracted independently by two authors and analyzed using STATA 11. A random-effect model was fitted to estimate the pooled prevalence with their 95% confidence interval. To detect publication bias funnel plots analysis and Egger weighted regression tests were done.
Results
The overall pooled prevalence of HBV and HCV infection among HD patients in Africa was 9.88% (95% CI: 7.20–12.56) I2 = 97.9% and 23.04% (95% CI: 18.51–2757) I2 = 99.6%, respectively. In addition, the pooled prevalence of HBV and HCV co-infection was 7.18% (95% CI: 3.15–11.20) I2 = 99.6%. Duration of dialysis was found to be the contributing factor for the occurrence of HBV and HCV among HD patients (OR = 1.44; 95% CI: 1.04, 2.01).
Conclusion
This study showed that there is high prevalence of HBV and HCV infections in HD patients in Africa. Therefore, strict adherence to precautions of infection control measures, isolation of seropositive patients, improvement in infrastructures, adequate screening of HBV and HCV for the donated blood, and decentralized HD services is needed to minimize the risk of HBV and HCV infections in HD facilities.
Citation: Adane T, Getawa S (2021) The prevalence and associated factors of hepatitis B and C virus in hemodialysis patients in Africa: A systematic review and meta-analysis. PLoS ONE 16(6): e0251570. https://doi.org/10.1371/journal.pone.0251570
Editor: Isabelle Chemin, Centre de Recherche en Cancerologie de Lyon, FRANCE
Received: January 12, 2021; Accepted: April 28, 2021; Published: June 22, 2021
Copyright: © 2021 Adane, Getawa. 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: The datasets used and/or analyzed during the current study are available at https://doi.org/10.5061/dryad.xksn02vg9.
Funding: The author(s) received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Abbreviations: ELISA, Enzyme-Linked Immunosorbent Assay; ESRD, End‑Stage Renal Disease; HBV, Hepatitis B virus; HCV, Hepatitis C Virus; HD, Hemodialysis; MEIA, microparticle enzyme immunoassay JBI: Johana bridges institute; RPHA, reverse passive hemagglutination WHO: World Health Organization
Introduction
Hepatitis is inflammation of the liver due to viral infection and leads to significant morbidity and mortality [1]. The HBV and HCV infection are highly infectious and transmitted from person to person by blood transfusions, sexual, and vertical routes [2]. They are the most common viral infections among individuals with renal disease [3]. Patents having renal disease do not clear the viral infections efficiently, hence the disease is associated with reduced immunity [4]. Patients with end‑stage renal disease (ESRD) are at increased risk of acquiring HBV and HCV infections than the general population due to their deficient immune response, exposure to blood transfusions, and HD equipment [5]. These patients are often anemic, require prolonged vascular access, and have a high possibility of exposure to infected patients and contaminated equipment, and cross-contamination from the dialysis circuits [6]. Nosocomial and iatrogenic transmission, duration of ESRD, duration of dialysis, and mode of dialysis are other risk factors in HD patients [7,8]. HD patients are potentially susceptible to infection with these blood-borne viral agents (HBV and HCV) compared to the general population making them a persistent public health concern as they are a cause of increased morbidity and mortality [9,10].
Africa has the second largest number of chronic HBV carriers after Asia and is considered as a region of high endemicity [11]. HCV is highly prevalent in patients undergoing maintenance HD where it adversely affects patient survival [12,13]. The global prevalence of HCV infection ranges from 0.6% in Canada, 1.5% in Japan, to 6% in Africa [14]. The prevalence of HBV and HCV during HD varies across countries. Strict infection control measures implemented in developed countries has minimized the transmission rate. However, the prevalence remains high in developing countries [15]. This might be due to low strict adherence to standard precautions and routine HD precautions, the absence of vaccinations, and the lack of financial resources [16].
There were a lot of studies that reported the prevalence of HBV and HCV among HD patients in different countries of Africa. However, there was no study that showed the pooled prevalence and associated factors of HBV and HCV among HD patients in the continent. Therefore, this systematic review and meta-analysis aimed to estimate the pooled prevalence and associated factors of HBV and HCV in HD patients in Africa. The study also determines the pooled prevalence of HBV and HCV virus in those patients in the different geographical areas (Northern, Central, Western, Eastern, and Southern) of Africa. The result of this study may provide insight to public health policymakers to plan appropriate public health interventions in the continent and also national level.
Methods and materials
Study design and protocol registration
This systematic review and meta-analysis were performed per the PRISMA guideline [17] (S1 Table). The protocol has been registered in the International Prospective Register of Systematic Reviews (PROSPERO), with the assigned number of CRD42021224905.
Search strategy
PubMed, Medline, EMBASE, Cochrane library, web of science, African Journals Online, Science Direct, and Google Scholar were the databases searched by two authors (TA and SG) to identify all articles reporting the prevalence of HBV and HCV infection in HD patients in Africa. Besides, a manual search was also conducted for relevant articles. We used the search terms separately and in combination using Boolean operators like “OR” or “AND”. An example of a search strategy used was as follows: ((((((((((prevalence) AND (seroprevalence)) OR (hepatitis)) OR (hepatitis viruses)) OR (hepatitis B virus)) OR (hepatitis C virus)) OR (HBV)) OR (HCV)) AND (hemodialysis patients)) OR (HD patients)) AND using African search filter developed by Pienaar et al to identify prevalence studies [18].
Eligibility criteria
Inclusion criteria.
Cross-sectional and cohort studies which reported the prevalence of HBV and/or HCV infection, published in peer-reviewed journals in English language only, conducted in the continent of Africa, used the HBsAg test to diagnose HBV infection and anti-HCV antibody test for HCV infection, and published from 1998 to 30 November 2020 were included in this review.
Study selection and quality assessment
After removing ineligible or duplicated papers, all potential eligible papers were reviewed. Full-text papers were retrieved for review and extraction of relevant information. The authors agreed to settle their disagreement through discussion. The Joana Brigg’s Institute (JBI) critical appraisal checklist for simple prevalence was used to assess the quality of included studies [19]. This tool comprised of 9 questions. (1) Was the sample frame appropriate to address the target population? (2) Were study participants sampled appropriately? (3) Was the sample size adequate? (4) Were the study subjects and the setting described in detail? (5) Was the data analysis conducted with sufficient coverage of the identified sample? (6) Were valid methods used for the identification of the condition? (7) Was the condition measured in a standard, reliable way for all participants? (8) Was there an appropriate statistical analysis? (9) Was the response rate adequate? For each question, a score of 0 was assigned for ‘not reported or not appropriate’ and 1 for ‘yes’. Then, the scores were summarized to get a total score ranging from 0 to 9. Based on the assigned points, articles were categorized as having a high (7–9), medium (5–7), or low (0–4) quality. Those articles with high and medium quality were included in the final analysis (S2 Table).
Data extraction
Two authors (SG and TA) extracted the necessary information from all the included studies including the name of the author, publication year, study year, the mean age of study participants, type of study, the sample size, sampling techniques, number of the infected cases, duration of dialysis, and methods used to detect HBsAg or anti-HCV antibody.
Statistical analysis
Eligible data were extracted and entered into Microsoft Excel and then exported to Stata version 11.0 software for analysis. The pooled prevalence of HBV and HCV along with the 95% confidence intervals was visually displayed using a forest plot. The heterogeneity of the included studies was evaluated using an index of heterogeneity (I2 statistic). Low, moderate, and high levels of heterogeneity were considered when the values of I2 becomes 25%, 50%, and 75%, respectively [20]. In all the pooled analyses, a random-effects model was used when heterogeneity was present due to variations of effects from individual studies. The potential sources of heterogeneity were identified using sub-group, meta-regression, and sensitivity analysis. Publication bias was investigated statistically using Egger’s test. A p-value < 0.05 in Egger’s test was considered as evidence of statistically significant publication bias.
Results
Of 1,820 studies identified in the initial search, 423 were removed due to duplicates. Moreover, 1,349 studies were excluded in the title and abstract screening, and in the full‑text screening, 23 cases were excluded. Finally, all the 39 studies were included in the final meta-analysis (Fig 1).
Characteristics of included studies
A total of 39 published articles on 23,538 HD patients were included in this review. Regarding the study design, 24 and 5 studies had used a cross-sectional and retrospective design, respectively. However, the other 10 studies did not report their research design. Of the total studies, 5 studies had used a convenient sampling while the other 34 studies did not report their sampling techniques. Of the 39 studies included, five studies were conducted in Nigeria, 3 in Cameroon, 5 in Sudan, 5 in Libya, 8 in Egypt, 1 in Senegal, 1 in Angola, 1 in Togo, 4 in Tunisia, 1 in Ethiopia, 1 in South Africa, 3 in Morocco, and 1 in Kenya. The minimum and maximum numbers of study participants were 46 in Sudan [21] and 4290 in Tunisia [22], respectively. The mean age of study participants ranged from 39.9 to 53.4 years. Of the 39 studies, 19 studies reported the prevalence of both HBV and HCV, 16 studies reported HCV alone, and 4 studies reported HBV alone. Sixteen studies reported the average duration of dialysis of the patients. Twenty-six and 5 studies reported the HBV and/or HCV prevalence using ELISA (enzyme-linked immunosorbent assay) and rapid kit tests, respectively. However, 5 studies did not explain the type of test they used for the determination of hepatitis infection. Reverse passive hemagglutination (RPHA), CILA (chemiluminescence immunoassay), and microparticle enzyme immunoassay (MEIA) tests were used by 3 separate studies (Table 1).
Prevalence of HBV and HCV
Thirty-nine published studies were included in this systematic review and meta-analysis to estimate the pooled prevalence of HBV and HCV infection among HD patients. The minimum prevalence was 0.8% (Libya) [25] and 2.3% (Nigeria) [23] for HBV and HCV, respectively. On the other hand, the maximum prevalence of HBV and HCV was 60.7% (Egypt) [59] and 60.9% (Egypt) [43], respectively. A total of 23 studies reported the prevalence of HBV in HD patients. Accordingly, the pooled prevalence of HBV was 9.88% (95% CI: 7.20–12.56) I2 = 97.9% (Table 2).
On the other hand, a meta-analysis of 35 studies for HCV showed that the pooled prevalence of HCV in HD patients was and 23.04% (95% CI: 18.51–2757) I2 = 99.6% (Table 3). Moreover, the pooled prevalence of HBV and HCV coinfection was 7.18% (95% CI: 3.15–11.20) I2 = 99.6%.
Subgroup analysis of detection method, region, and year of study
The prevalence of HBV among different types of detection methods, regions of the studies performed, and years of the study were analyzed by subgroup analysis. The combined prevalence of HBV by ELISA, rapid kit, other methods, and NA (methods not clear) was 7.59 (95%CI: 5.38–9.80), 7.50% (95% CI: 2.26–12.73), 6.48% (95% CI: 3.15–9.82), and 20.21% (95% CI: -6.51–49.92), respectively. The combined prevalence of HBV in Western, Central, Northern, and East African countries was 6.57% (95% CI: 3.48–9.58), 7.88% (95% CI: 5.13–10.63), 12.27% (95% CI: 8.19–16.35), and 4.09% (95% CI: -2.50–10.68), respectively. The pooled prevalence of HBV per year of study was as follows: 1994–2008; 11.22% (95% CI: 6.34–16.09), 2009–2015; 5.10% (95% CI: 2.54–7.66), 2016–2020; 11.70% (95% CI: 6.79–16.61), and NA (study year not clear); 4.0% (955 CI: 3.20–4.80) (Table 2).
Across regions, the combined prevalence of HCV among HD patients was as follows: Northern Africa 29.69% (95% CI: 21.47–37.91), Central Africa, 14.63% (95% CI: 3.18–26.07), Western Africa, 4.37% (95% CI: 1.75–7.00), South Africa, 21.00% (95% CI: 13.13–28.87), and East Africa, 3.21% (95% CI: 1.37–5.04). Furthermore, the pooled prevalence of HCV in HD patients was 12.66% (95% CI: -4.32–19.80), 9.09% (95%CI: 3.76–14.43), 11.17% (95% CI: 5.89–16.45), and 8.97% (95% CI: 2.41–15.53) in 1996–2008, 2009–2015, 2016–2020, and NA (year of study not clear, respectively. The combined prevalence of HCV in HD patients was 22.55% (95% CI: 17.76–27.34), 4.46% (95% CI: 1.89–7.23), 15.84% (95% CI: 6.45–38.13), 39.52% (95% CI: -29.13–49.92) according to ELISA, rapid kit, other methods, and NA (methods not clear) (Table 3).
Publication bias.
The included studies were assessed for potential publication bias statistically by Egger’s test. The result of Egger’s test indicated publication bias, in both HBV (P-values = 0.013) and HCV (P-values = <0.001). This was depicted graphically by a funnel plot which showed a non-symmetrical display of prevalence reported by all the included studies (Figs 2 and 3).
Association between duration of dialysis and HBV and HCV
Analysis of 5 studies to assess the association between duration of dialysis and HBV and HCV showed that duration of dialysis (OR = 1.44; 95% CI: 1.04, 2.01) was found to be the contributing factor for the occurrence of HBV and HCV among HD patients (Fig 4).
Sensitivity analysis
Due to the high heterogeneity of results in both HCV and HBV, a sensitivity analysis was done by omitting each study step by step to assess the effect of each study on the pooled prevalence. The result showed that omitted studies don’t have a significant effect on the pooled prevalence of HCV and HBV among hemodialysis patients as indicated in Figs 5 and 6, respectively.
Meta-regression.
In this study, meta-regression were performed on continuous covariates such as study year, the mean age of the participants, sample size, and duration of dialysis. Accordingly, the result of the meta-regression showed that the pooled prevalence of HCV among HD patients was not associated with the study year, the mean age of the participants, and duration of dialysis (Table 4).
Discussion
This systematic review and meta-analysis was conducted to determine the pooled prevalence of HBV and HCV in HD patients of Africa. Thirty-nine studies based on 23, 538 HD patients were included in this study. The result suggested that the pooled prevalence of HBV and HCV infection among HD patients were 9.88% (95% CI: 7.20–12.56) I2 = 97.9% and 23.04% (95% CI: 18.51–2757) I2 = 99.6%, respectively. The coinfection of HBV-HCV among HD patients was 7.18% (95% CI: 3.15–11.20) I2 = 99.6%. The prevalence of HBV in this study is almost similar to a systematic review conducted in Vietnam by Duong et al [60] which reported that the national pooled prevalence of HBV in the country is 9.7%.
The prevalence of HCV antibody reported in this study (23.04%) is lower than a previous meta-analysis reports in Vietnam (32.6%) [60], Pakistan (32.33%), China (41.1%) [61], and Asia (31%) [62]. On the other hand, the prevalence of HCV infection on HD patients in this study (Africa) is higher than in Europe and the USA (5%-10% or less). This variation in the prevalence rates of HCV across different regions might be because of the disparity of medical conditions in developed and developing countries [63]. Besides, this might be due to a lack of education and awareness of HCV transmission, a lack of qualified and competent medical personnel, a lack of proper health infrastructure, inadequate implementation of practices recommended by the WHO, and inadequate screening of HCV for donated blood [64]. In this systematic review and meta-analysis, the coinfection rate of HBV-HIV was (7.18%). This might support the ideology that declares coinfection rates directly correlate with the burden of individual strain infections.
The subgroup analysis showed that HCV infection prevalence among the HD patients was observed across all regions of Africa. Our results show that the prevalence of HCV among HD patients is higher in Northern Africa (29.69%) than in South Africa (21.00%), in central Africa (14.63%), western Africa (4.37%), and East Africa (3.21%). The prevalence of HBV among HD patients has also been observed across different regions of Africa. Accordingly, the result showed that it was higher in Northern Africa (12.27%), central Africa (7.88%), Western Africa (6.57%), and East Africa (4.09%). This finding was per the fact that North African countries seem to have a higher prevalence than the sub-Saharan and East African countries [31,33,42]. This variability may be due to differences in ethnicity, health provision system, and characteristics of the study population. The prevalence of HCV among HD patients shows a gradual decrement across different categories of study years as it is 12.66% and 11.17% in 1996–2008 and 2016–2020, respectively. A study conducted in Senegal by Seck et al showed that the decline in the prevalence of HCV among HD patients could be due to the development and implementation of preventive strategies, more adherence of the medical staff to the aseptic measures, and a better transfusion policy [44]. Improved infection control, vaccination, and isolation of Hepatitis infected patients during HD are other factors contributing to the low prevalence observed [23].
The prevalence of HBV by ELISA and rapid kits was 7.59 (95%CI: 5.38–9.80) and 7.50% (95% CI: 2.26–12.73), respectively. Similarly, the combined prevalence of HCV in HD patients was 22.55% (95% CI: 17.76–27.34) and 4.46% (95% CI: 1.89–7.23) according to ELISA and rapid kit, respectively. The result of this study highlights that the prevalence of HBV and HCV in HD patients was higher in ELISA as compared to rapid kits. This might be hypothesized that rapid screening test kits are associated with more false negatives compared to the ELISA technique as confirmed by a study conducted in Nigeria [65]. Moreover, a study conducted by Chameera et al says that rapid kits showed less sensitivity and Negative predictive value [66]. However, with several limitations, rapid tests are frequently the only viable option for infectious screening in resource-limited settings [67].
With respect to the associated factors associated with HBV and HCV infection, being on long-term HD was 1.14 more likely to be infected with hepatitis than their counterparts. It is estimated that as the frequency of dialysis increases, the higher the prevalence of hepatitis. There may be other causes of transmission, such as the re-use of the dialyzers and pipelines, frequent cardiopulmonary bypass and repeated needle puncture during the treatment, sharing of dialysis machines, and incomplete disinfection. Control of contagion and minimizing the frequency of blood transfusion are the key to reduce the incidence of hepatitis in HD patients. Moreover, adherence to universal hygiene standards, disinfection of dialysis machines and instruments, avoidance of unnecessary and unsafe injections of blood products, and treatment with antiviral medicines are important to prevent hepatitis [47,61].
Strengths and limitations: the strength of the study is its comprehensive literature search by two independent authors to extract all available published articles. Besides, we included articles published across all corners of Africa (Northern, Central, Western, Eastern, and Southern) that helps to generalize the finding of the study to the continent. The study also comprised on large sample size with a total population of 23,538. The study includes articles published only in English languages that finally compromise the result of the study. There is also significantly high heterogeneity in the included studies.
Conclusion
This study showed that there is high prevalence of HBV and HCV infections in HD patients in Africa. Therefore, strict adherence to precautions of infection control measures, isolation of seropositive patients, improvement in infrastructures, adequate screening of HBV and HCV for the donated blood, and decentralized HD services is needed to minimize the risk of HBV and HCV infections in HD facilities.
Supporting information
S1 Table. Presents Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) checklist.
https://doi.org/10.1371/journal.pone.0251570.s001
(DOCX)
S2 Table. Quality assessment of the studies included in systematic review and meta-analysis of HBV and HCV among HD patients in Africa.
https://doi.org/10.1371/journal.pone.0251570.s002
(DOCX)
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