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Published in final edited form as: J Infect Public Health. 2022 Nov 12;15(12):1436–1445. doi: 10.1016/j.jiph.2022.11.008

Epidemiology of occult hepatitis B and C in Africa: A systematic review and meta-analysis

Juliette Laure Ndzie Ondigui a,b, Sebastien Kenmoe c,*, Cyprien Kengne-Ndé d, Jean Thierry Ebogo-Belobo e, Guy Roussel Takuissu f, Raoul Kenfack-Momo g, Donatien Serge Mbaga a, Serges Tchatchouang h, Josiane Kenfack-Zanguim g, Robertine Lontuo Fogang i, Elisabeth Zeuko'o Menkem j, Ginette Irma Kame-Ngasse e, Jeannette Nina Magoudjou-Pekam g, Arnol Bowo-Ngandji a, Nadège Mafopa Goumkwa b, Seraphine Nkie Esemu c, Lucy Ndip c, Sara Honorine Riwom Essama a, Judith Torimiro b
PMCID: PMC7613883  EMSID: EMS157310  PMID: 36395668

Abstract

Background

Occult hepatitis B (OBI) and C (OCI) infections lead to hepatic crises including cases of liver cirrhosis and even hepatocellular carcinoma (HCC). OBI and OCI also pose a significant problem of their transmissibility. This study aimed to assess the overall prevalence of OBI and OCI in the African continent, a region highly endemic for classical hepatitis B and C viruses.

Methods

For this systematic review and meta-analysis, we searched: PubMed, Web of Science, African Journal Online and African Index Medicus for published studies on the prevalence of OBI and OCI in Africa. Study selection and data extraction were performed by at least two independent investigators. Heterogeneity (I2) was assessed using the χ2 test on the Cochran Q statistic and H parameters. Sources of heterogeneity were explored by subgroup analyses. This study was registered in PROSPERO, with reference number CRD42021252772.

Results

We obtained 157 prevalence data for this meta-analysis, from 134 studies for OBI prevalence; 23 studies on OCI prevalence, and a single study on the OBI case fatality rate. The overall estimate for the prevalence of OBI was 14.8% [95% CI = 12.2-17.7] among 18579 participants. The prevalence of seronegative OBI and seropositive OBI was 7.4% [95% CI = 3.8-11.8] and 20.0% [95% CI = 15.3-25.1] respectively. The overall estimate for the prevalence of OCI was 10.7% [95% CI = 6.6-15.4] among 2865 participants. The pooled prevalence of seronegative OCI was estimated at 10.7% [95%CI = 4.8-18.3] and that of seropositive OCI at 14.4% [95%CI = 5.2-22.1]. In Sub-group analysis, patients with malignancies, chronic hepatitis C, and hemodialysis had a higher OCI prevalence. While those with malignancies, liver disorders, and HIV positive registered highest OBI prevalence.

Conclusion

This review shows a high prevalence of OBI and OCI in Africa, with variable prevalence between countries and population groups.

Keywords: Occult hepatitis B, Occult hepatitis C, Prevalence, Africa

Introduction

In the early 1980 s, a new form of clinical hepatitis B virus (HBV) infection was described, corresponding to the presence of HBV DNA in the liver and/or serum of patients in whom the HBs antigen (Ag) is undetectable by the usual serology tests. This was called occult hepatitis B (OBI) [1–3]. Based on the antibody profile of HBV, OBI can be distinguished into seropositive-OBI (anti-HBc and/or anti-HBs positive) and seronegative-OBI (anti-HBc and anti-HBs negative)[4]. A similar entity was studied in 2005, by Castillo et al., on the ability of hepatitis C virus (HCV) to replicate in peripheral blood mono-nuclear cells (PBMCs) of patients in the absence of viral RNA in serum and detectable anti-HCV antibodies, thus describing an occult HCV infection[5,6]. Two types of OCI are recognized: seronegative OCI (anti HCV antibody-negative and serum HCV RNA-negative) and seropositive OCI (anti HCV antibody-positive and serum HCV RNA-negative)[7]. These occult forms of hepatitis B and C can lead to hepatic crises including cases of chronic liver infection and liver cirrhosis [8]. It is known that OBI plays a role in the development of hepatocellular carcinoma [9]. These entities highlight multiple concerns, including the potential for transmission of this form of infection through blood transfusion, hemodialysis, or from mother to child [10]. The OBI and OCI have been described in a variety of individuals, including hemodialysis patients, patients with sustained virologic response, immunocompromised individuals, patients with abnormal liver function, and apparently healthy subjects. Multiple meta-analyses on the prevalence of OBI and OCI have shown great variability in estimates according to population categories, regions, type of tests used, and the level of endemicity of the disease [9,11–17]. Two global meta-analyses with partial analyses for Africa reported the prevalence of OBI at 3.7% [15], seronegative OCI at 9.6% and seropositive OCI at 13.3% [17]. The highest prevalence of OBI was in countries with high endemicity of classical hepatitis B, including Africa, with prevalence of up to 35.6% in the general population in Uganda [15]. Similar to classical hepatitis C infection, which has the highest prevalence in Egypt, this meta-analysis showed that OCI had the highest prevalence in North Africa, represented only by Egypt [17]. Other meta-analyses have estimated the prevalence of OBI in Africa among people living with HIV at 11.2% [16] and in Sudan at 15.5% [12]. In a regional meta-analysis in the Middle East and Eastern Mediterranean countries the prevalence of OCI was estimated at 10.0% with the highest prevalence recorded in Egypt [14]. Estimates of a high OBI prevalence of 34% was reported in Western Europe and Northern America [18] and a lower OBI prevalence of 4% was observed in Asia [19]. Thus, there are no systematic syntheses for OBI and OCI for Africa which is a highly endemic region for classical HBV and HCV infections. In this meta-analysis, we compiled all available evidence for OBI and OCI in Africa with differences across populations and regions. The results of this review may help consider OBI and OCI in the WHO goal of eliminating viral hepatitis by 2030. It will also help to sound the alarm on the need to strengthen the diagnostic capacities of OBI and OCI in Africa which has limited access to molecular testing.

Materials and methods

Registration

This systematic review was conducted in full compliance with the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta - Analyses) guidelines (S1 Table) [20]. The protocol of this systematic review was developed and registered on PROSPERO (International prospective register of systematic reviews) on June 03, 2021 under the digital identifier: https://www.crd.york.ac.uk/pros-pero/display_record.php? ID = CRD42021252772.

Search strategy

In May 2021, an electronic literature search was performed and the following databases were used: PubMed, Web of Science, African Journal Online and African Index Medicus. A second update search was performed in July 2022 to search for additional articles. We used a combination of the keywords covering OBI, OCI, the names of African countries and regions as well as the boolean operators OR and AND as illustrated in detail in S2 Table. This search strategy was also adapted to identify relevant articles from other databases. To complement the bibliographic database search and identify potential additional data sources, we reviewed the reference list of all relevant articles. All search results were managed using Endnote X9 credential management software, and all duplicates were removed using this same software.

Inclusion and exclusion criteria

We considered published studies, without any restrictions in time, population category or detection assay. We classified populations for OBI as: 1) HBsAg negative 2) HBsAg negative and Anti-HBc positive, and 3) HBsAg negative and Anti-HBc negative [21,22], and for OCI as 1) seronegative OCI (anti HCV antibody-negative and serum HCV RNA-negative), 2) seropositive OCI (anti HCV antibody-positive and serum HCV RNA-negative), and 3) seropositive and/or seronegative OCI [7]. Only reports written in English and/or French were included. Exclusion criteria included all of the following: case reports, reviews and articles for which: studies were conducted outside Africa, sample size ≤ 10 participants, no baseline data for the longitudinal study, no data on OBI and/or OCI prevalence or case fatality rate, and no data on number of negative HBsAg tested.

Study selection and data extraction process

Duplicates identified in the full list of studies were removed. The titles and abstracts of articles retrieved from the electronic literature search were independently reviewed by four researchers, and the full texts of potentially eligible articles were obtained and further assessed for final inclusion. Articles were selected based on the availability of data needed to calculate the prevalence of OBI and/or OCI in the study. Data from the included studies were extracted using a Google Form by 18 of the study authors and verified by SK. Data extracted were first author name, year of publication, design of study, WHO region, UNSD region, country, country’s income level, sampling method, time of data collection, period of study, age of study participants, recruiting framework, population categories, OBI and/or OCI diagnostic method, and prevalence of OBI and/or OCI in Africa. We considered as the high-risk groups of OBI: HIV-positive patients, patients with chronic liver disease, patients on hemodialysis, patients with hematological disorders, patients with malignancies, organ recipients, healthcare workers, patients who inject drugs and men who have sex with men [12,19,23]. We grouped apparently healthy individuals, blood donors, the general population, and pregnant women as the low-risk group for OBI.

Disagreements observed during study selection and data extraction were resolved by discussion and consensus.

Quality assessment

The tool developed by Hoy et al. for cross-sectional studies was used to assess the methodological quality of the included studies (S3 Table) [24]. Discussion and consensus were used to resolve disagreements.

Statistical analysis

Study-specific estimates were pooled using DerSimonian and Laird’s random-effects model meta-analysis [25]. This model provided the overall prevalence, the 95% confidence interval and the prediction interval which informs about the values of future studies. Heterogeneity was assessed by the Cochrane statistical test, and the p value of the Q test (< 0.05) was used to indicate significant heterogeneity and quantified by I2 values, assuming I2 values of 25%, 50% and 75% represent respectively low, moderate and high heterogeneity[26,27]. Publication bias was assessed using Egger’s test and funnel plot [28]. Subgroup analyses were performed based on study design, sampling approach, setting, timing of sample collection, countries, WHO region, UNSD region, country income level, age range, population categories, and OBI and/or OCI diagnostic assays. We considered p values < 0.05, to be statistically significant. R software version 4.1.0 was used to perform the analyses[29,30].

Results

Selection of studies

As of 07/18/2022, 496 studies were analysed with no additional studies added from the manual search. After removing the duplicates (152), 344 articles were screened. The full text evaluation led to the elimination of 78 studies for several reasons, including lack of data on OBI and/or OCI prevalence or case fatality rate, or small sample size (S4 Table). In all, a total of 109 articles reporting the prevalence and/or case fatality rate of OBI and/or OCI in Africa were included in this synthesis (Fig. 1) [3,31–138].

Fig. 1. PRISMA flow diagram demonstrating the literature search and screening process.

Fig. 1

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Study characteristics

Overall, we obtained 157 prevalence data for this meta-analysis, including 133 studies for OBI prevalence; 23 studies for OCI prevalence, and a single study for OBI case fatality rate (S5, S6, and S7 Tables). The OBI case fatality rate study reported a total of 6 deaths among 72 OBI and HIV infected patients in Botswana [108]. The studies were published between 2006 and 2022 in general and respectively from 2006 to 2022 and 2010-2022 for OBI and OCI. Participants were registered from 1997 to 2021. The majority of studies were cross-sectional (84.7%) with non-probability sampling (88.5%). The study setting was mainly in the hospital (93.6%). The studies were carried out in 21 African countries, mainly in Egypt (44.6%) and South Africa (13.4%). The largest number of studies were from lower-middle-income countries (68.2%). Most of the studies recruited adults (61.8%). Of the included studies, 39 (24.8%) were carried out in HIV infected patients, 27 (16.6%) in patients with chronic hepatitis C infection, 19 (12.1%) in blood donors, and 19 (12.1%) in hemodialysis patients. The diagnosis of OCI was either performed using conventional RT-PCR (5.7%) or real-time RT-PCR (8.3%). OBI diagnosis was made using conventional PCR (46.5%) or real-time PCR (39.5%). The type of sample used was blood for OBI (100%) and peripheral blood mononuclear cells (PBMCs) for OCI (100%). Most of the prevalence data were at moderate risk of bias (59.2%).

The prevalence of occult C infection

In total, the twenty-three studies reporting OCI prevalence data in Africa were conducted only in Egypt. The pooled OCI prevalence was estimated to be 10.7% [95% CI = 6.6-15.4] on a sample of 2865 participants with substantial heterogeneity (I2 = 90.7% [95% CI = 87.4-93.2], p < 0.001) (Table 1, Figs. 2 and 3). Two studies presented the prevalence of seropositive and/or seronegative OCI without distinction with an estimated at 5.8% [95% CI = 0.8-13.9] in a total of 100 participants. There was a total of 14 studies reporting seronegative OCI prevalence. The pooled seronegative OCI prevalence was estimated to be 10.7% [95% CI = 4.8-18.3] in a sample of 908 participants. There was a total of 7 studies reporting seropositive OCI prevalence. The overall seropositive OCI prevalence was estimated to be 14.4% [95% CI = 5.2-22.1], with a total of 1857 participants.

Table 1. Summary of meta-analysis results for the prevalence of occult hepatitis B and C in in Africa.

Prevalence. % (95%CI) 95% Prediction interval N Studies N Participants H (95%CI) §I2 (95%CI) P heterogeneity
OBI prevalence in Africa
Overall 14.9 [12.2–17.7] [0–54.1] 133 18579 5.1 [4.9–5.4] 96.2 [95.8-96.5] < 0.001
Cross-sectional 15.7 [12.7–18.9] [0-56.1] 116 15443 5.1 [4.8–5.3] 96.1 [95.7-96.5] < 0.001
Low risk of bias 15.7 [11.6–20.1] [0–53.5]   51   7535 4.9 [4.6–5.3] 95.9 [95.2-96.5] < 0.001
OCI prevalence in Africa
Overall 10.7 [6.7–15.5] [0–38.7]   23   2865 3.3 [2.8–3.8] 90.7 [87.4-93.2] < 0.001
Cross-sectional 8.9 [5.1–13.5] [0–32.1]   17   2451 2.9 [2.4–3.5] 88.2 [82.7-92] < 0.001
Low risk of bias 12.2 [6–20.2] [0–49]   12   2141 4 [3.3-4.9] 93.8 [90.9-95.8] < 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

Fig. 2. Prevalence of occult hepatitis B and C virus infection in Africa.

Fig. 2

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Fig. 3. Prevalence of seronegative and seropositive occult hepatitis C virus infection in Africa.

Fig. 3

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The prevalence of occult B infection

A total of 133 studies reporting prevalence data on OBI were conducted in 5 UNSD regions of Africa: Central Africa, Eastern Africa, West Africa, Northern Africa, and Southern Africa (Fig. 2). The OBI prevalence was estimated at 14.8% [95% CI = 12.2-17.7] in a sample of 18579 participants with significant heterogeneity (I2 = 96.2% [95% CI = 95.8-96.5], p < 0.0001) (Table 1, Figs. 2, 4, and S1 Fig). The pooled prevalence of seropositive OBI was estimated at 20.0% [95% CI = 15.3-25.1] among 6873 participants. Prevalence data on seronegative OBI were obtained from 32 studies and the prevalence was estimated at 7.4% [95% CI = 3.8-11,8] with 2896 participants. A total of 44 studies reported on seropositive and/or seronegative OBI with an estimated prevalence of 14.3% [95% CI = 10.1-19.2] in 8810 participants. Few studies provided data on the variation of seropositive or seronegative OBI with anti-HBs (only 9 studies). The distribution of OBI prevalence according to anti-HBs was as follows: 17.32% [4.37; 35.69] for anti-HBc negative/ anti-HBs negative, 30.95% [17.10; 46.62] for anti-HBc positive/ anti-HBs negative, 27.41% [ 8.89; 50.70] anti-HBc positive/ anti-HBs positive, and 0% for anti-HBc negative/ anti-HBs positive (S3 Fig).

Fig. 4. Prevalence of seronegative and seropositive occult hepatitis B virus infection in Africa.

Fig. 4

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Subgroup analyses

Occult hepatitis C infection

The OCI prevalence was statistically different (p = 0.005) according to the population categories with an estimated prevalence of 34.9% in patients with malignancies, 12.3% in those with chronic hepatitis C, 7.2% in hemodialysis patients, and 1.1% in apparently healthy individuals (S8 Table). OCI prevalence did not vary significantly by study design (p = 0.380), sampling approach (p = 0.460), type of OCI (seropositive or seronegative) (p = 0.819), and diagnostic method (p = 0.067).

Occult hepatitis B infection

Variation of OBI prevalence was statistically significant by country (p < 0.001), categories of population (p < 0.001), and type of OBI (seropositive or seronegative) (p < 0.001) (S8 Table). The highest OBI prevalence rates were in Morocco (42.8%), Gabon (22.6%), and South Africa (20.2%). Patients with malignancies, patients with liver disorders, and HIV positive patients were the three population categories with the highest OBI prevalence, 41.9%, 33.1%, and 17.0% respectively. The seropositive OBI prevalence (20.1%) was significantly higher than that of seronegative OBI (8.0%). The OBI prevalence did not vary significantly by study design (p = 0.360), sampling approach (p = 0.117), setting (hospital or community-based) (p = 0.360), timing of data collection (p = 0.875), WHO region (p = 0.544), UNSD region (p = 0.384), country income level (p = 0.395), age range (p = 0.799), and diagnostic method (p = 0.659).

Publication bias

Egger’s tests were significant for the OCI prevalence (P < 0.001) and OBI prevalence in Africa (P = 0.014), suggesting the presence of a publication bias. Funnel plots confirmed the results of publication bias obtained by Egger’s test (S2 and S4 Figs).

Discussion

We performed a meta-analysis to provide an estimate of the prevalence and case fatality rate of OBI and OCI in Africa. A total of 109 studies were reviewed and a total of 18579 and 2865 participants were assessed for OBI and OCI respectively. There was only one study that reported deaths (6/72) in HIV-positive subjects with OBI in Botswana. The prevalence of OBI ranged from 0% to 100% and the prevalence of OCI ranged from 0% to 60%. An estimated prevalence of OCI (10.7%) and OBI (14.8%) was obtained in relevant articles published between 2010 and 2022 in Africa. Overall, we found a higher prevalence of OCI in patients with malignancies, in patients with chronic hepatitis C, and in hemodialysis patients. Patients with malignancies, patients with liver disorders, and HIV positive patients were the population groups with the highest OBI prevalence.

Our results show that apart from Egypt, studies on OCI in Africa are very rare. Although Egypt has the highest prevalence of HCV in the world [139], many other African countries also have significant HCV prevalence, including Cameroon, Burundi and Morocco [140]. From this observation, it is therefore necessary to conduct additional studies on OCI in other African countries outside of Egypt. Studies have shown risks of reactivating the presence of OCI in subjects with a sustained virological response to HCV [17]. With the arrival of new direct-acting HCV treatments [141], OCI studies on those patients with a sustained virologic response are needed. Our systematic review found that the combined prevalence of OCI was 10.7% (14.4% for OCI seropositive and 10.7% for OCI seronegative). Related studies have reported similar prevalence of OCI at 10% in Middle Eastern and Eastern Mediterranean countries [14]. In a global review, the prevalence of seropositive OCI was estimated at 13.3% and seronegative OCI at 9.6%. [17]. These related reviews suggest that the prevalence of OCI is high in subjects with chronic liver disease, subjects who inject drugs, HIV positive subjects and patients on hemodialysis. [14,17]. We also found similar results in the present work, with a higher prevalence in patients with malignancies, patients with hepatological disorders, HIV positive patients and patients on hemodialysis. So far, no studies were found on OCI in people at high risk of HCV, such as people who inject drugs or men who have sex with men, so these studies are needed in Africa.

The prevalence of OBI is known to be very variable according to population categories. The high-risk groups reported by the authors included HIV-positive patients, patients with chronic liver disease, patients on hemodialysis, patients with hematological disorders, patients with malignancies, organ recipients, healthcare workers, patients who inject drugs and men who have sex with men [12,19,23]. The geographical context is also an important source of variability in the prevalence of OBI. The main factors of this variability include the endemicity of circulation of classic hepatitis B (low, intermediate or high level), the socio-demographic index and the rate of vaccination coverage for infection due to the hepatitis B virus [15,23]. Diagnostic factors such as the type of samples (blood, peripheral blood mononuclear cells or liver tissue) and the sensitivity and specificity of diagnostic techniques for the targets (DNA, HBsAg, anti-HBc, anti-HBs) are also associated with a significant influence of the prevalence of OBI [18,23]. Because of all these variability factors, objective comparisons between estimates from studies with different methodological approaches are difficult. Similar prevalence to the one found in our review were reported in a national review in Sudan (15.5%) and in a second review conducted in Africa among HIV-positive patients (11.2%) [12,16]. The prevalence of HBV in HIV-positive patients in Africa is known to be high due to the high endemicity of these two diseases and their common route of transmission [142]. Therefore, the high prevalence of OBI also found in HIV-positive subjects in this study suggests the need for HBV DNA testing in these high-risk patients in Africa. Africa is a highly endemic area for classic HBV. So, hoping for the elimination of HBV as recommended by the WHO, strengthening vaccination policies against HBV is necessary and more particularly in patients with malignancies and HIV-positive patients [143]. Compared to the prevalence of OBI in this work, Xie et al., estimated a lower pooled prevalence of 4% from 70 studies conducted in Asia [19]. Surprisingly, the highest prevalences have been estimated for areas of the world with the lowest endemicity, notably 36% and 25% for Western Europe and North America, respectively [18].

Our study is mainly limited by the representativeness of the included studies. All OCI prevalence studies were conducted in Egypt and OBI prevalence data were usually collected in certain regions, which might not represent national prevalence and due to unavailability of data from OCI. Only 15/55 African countries were represented in this review. Therefore, the data may not be sufficient to represent the whole continent for the OBI and the OCI. In addition, substantial residual statistical heterogeneity in prevalence measures was identified in the overall and subgroup meta-analyses for OBI and OCI. Despite these limitations, the main strength of our review is that we identified a very large number of studies, which covered multiple categories of symptomatic, apparently healthy populations at high risk of HCV and HBV infection. We also took into account in our estimates the variability of prevalence according to anti-HCV serological status as well as that of anti-HBc.

Conclusion

This review presents a summary of the prevalence of OBI and OIC in Africa. It shows that despite the great variability of prevalence according to population category and geographic region, in general, the prevalence of OBI and OCI in Africa are high and patients with malignancies, hemodialysis patients and HIV patients are groups at high risk for these infections. This highlights the need to include more appropriate OCI and OBI screening programs to target those at high risk of infection. In addition, the lack of data in several African countries shows the need for researchers to investigate this field, particularly in countries with high endemicity for HBV/HCV.

Supplementary Material

Supplementary data associated with this article can be found in the online version at 10.1016/j.jiph.2022.11.008.

Supplementary Material

Acknowledgement

Not applicable.

Funding

This project is part of the EDCTP2 programme supported by the European Union under grant agreement TMA2019PF-2705.

Abbreviations

Ag

antigen

HBV

hepatitis B virus

HCC

hepatocellular carcinoma

HCV

hepatitis C virus

OBI

occulthepatitis B

OCI

occulthepatitis C

PBMC

peripheral blood mononuclear cells

Footnotes

CRediT authorship contribution statement

Kenmoe S, Ndzie Ondigui JL, and Torimiro J were responsible for conception and design of the study as well as project administration; Ndzie Ondigui JL, Kenmoe S, Kengne-Ndé C, Ebogo-Belobo JT, Takuissu GR, Kenfack-Momo R, Mbaga DS, Tchatchouang S, Kenfack-Zanguim J, Lontuo Fogang R, Zeuko’o Menkem E, Kame-Ngasse GI, Magoudjou-Pekam JN, Bowo-Ngandji A, Mafopa Goumkwa N, Nkie Esemu S, Ndip L, Riwom Essama SH, Torimiro J were responsible for the data curation and interpretation of results; Kengne-Nde C and Kenmoe S were responsible for statistical analysis; Kenmoe S and Ndzie Ondigui JL wrote the original draft; All authors critically reviewed the first draft and approved the final version of the paper for submission, and have read and approve the final manuscript.

Consent for publication

Not applicable.

Competing interests

None.

References

  • [1].Thiers V, Nakajima E, Kremsdorf D, Mack D, Schellekens H, Driss F, et al. Transmission of Hepatitis B from Hepatitis-B-seronegative subjects. Lancet. 1988;332(8623):1273–6. doi: 10.1016/s0140-6736(88)92891-7. [DOI] [PubMed] [Google Scholar]
  • [2].Vallet-Pichard A, Pol S. L’hépatite B occulte. Virologie. 2008;12(2):87–94. doi: 10.1684/12-2.2011.87-94-article-1. [DOI] [PubMed] [Google Scholar]
  • [3].Esmail MA, Mahdi WK, Khairy RM, Abdalla NH. Genotyping of occult hepatitis B virus infection in Egyptian hemodialysis patients without hepatitis C virus infection. J Infect Public Health. 2016;9(4):452–7. doi: 10.1016/j.jiph.2015.11.018. [DOI] [PubMed] [Google Scholar]
  • [4].Raimondo G, Pollicino T, Cacciola I, Squadrito G. Occult hepatitis B virus in-fection. J Hepatol. 2007;46(1):160–70. doi: 10.1016/j.jhep.2006.10.007. [DOI] [PubMed] [Google Scholar]
  • [5].Castillo I, Rodríguez-Iñigo E, Bartolomé J, de Lucas S, Ortíz-Movilla N, López-Alcorocho JM, et al. Hepatitis C virus replicates in peripheral blood mono-nuclear cells of patients with occult hepatitis C virus infection. Gut. 2005;54(5):682–5. doi: 10.1136/gut.2004.057281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [6].Chevaliez S. Hepatitis C virus replicates in peripheral blood mononuclear cells of patients with occult hepatitis C virus infection 9. JOHN LIBBEY EUROTEXT; 2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [7].Austria A, Wu GY. Occult Hepatitis C Virus Infection: A Review. J Clin Transl Hepatol. 2018;6(2):155–60. doi: 10.14218/JCTH.2017.00053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [8].Rezaee-Zavareh MS, Hadi R, Karimi-Sari H, Hossein Khosravi M, Ajudani R, Dolatimehr F, et al. Occult HCV infection: the current state of knowledge. Iran Red Crescent Med J. 2015;17(11):e34181. doi: 10.5812/ircmj.34181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [9].Huang X, Hollinger FB. Occult hepatitis B virus infection and hepatocellular carcinoma: a systematic review. J Viral Hepat. 2014;21(3):153–62. doi: 10.1111/jvh.12222. [DOI] [PubMed] [Google Scholar]
  • [10].Carreño V, Bartolomé J, Castillo I, Quiroga JA. New perspectives in occult hepatitis C virus infection. World J Gastroenterol. 2012;18(23):2887–94. doi: 10.3748/wjg.v18.i23.2887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [11].Dolatimehr F, Khosravi MH, Rezaee-Zavareh MS, Alavian SM. Prevalence of occult HCV infection in hemodialysis and kidney-transplanted patients: a sys-tematic review. Future Virol. 2017;12(5):315–22. [Google Scholar]
  • [12].Eltom K, Albeely A, El Hussein A, Elkhidir IM, Enan K. Occult hepatitis B virus infection in Sudan: a systematic review and meta-analysis. JGH Open. 2020;4(5):800–7. doi: 10.1002/jgh3.12411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [13].Fu S, et al. Prevalence of occult hepatitis C virus infection in patients with chronic liver disease: a systematic review and meta-analysis. Hepatol Int. 2020;14:S130. [Google Scholar]
  • [14].Hedayati-Moghaddam MR, Soltanian H, Ahmadi-Ghezeldasht S. Occult hepa-titis C virus infection in the Middle East and Eastern Mediterranean countries: a systematic review and meta-analysis. World J Hepatol. 2021;13(2):242–60. doi: 10.4254/wjh.v13.i2.242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [15].Ji DZ, Pang XY, Shen DT, Liu SN, Goyal H, Xu HG. Global prevalence of occult hepatitis B: A systematic review and meta-analysis. J Viral Hepat. 2022;29(5):317–29. doi: 10.1111/jvh.13660. [DOI] [PubMed] [Google Scholar]
  • [16].Kajogoo VD, Swai SS, Gurung S. Prevalence of occult hepatitis B among HIV-positive individuals in Africa: A systematic review and meta-analysis 10. SAGE Open Med. 2022:20503121211072748. doi: 10.1177/20503121211072748. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [17].Mbaga DS, Kenmoe S, Bikoï JN, Takuissu GR, Amougou-Atsama M, Okobalemba EA, et al. Global prevalence of occult hepatitis C virus: a systematic review and meta-analysis. World J Method. 2022;12(3):179–90. doi: 10.5662/wjm.v12.i3.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [18].Pisaturo M, Onorato L, Russo A, Chiodini P, Coppola N. An estimation of the prevalence of occult HBV infection in Western Europe and in Northern America: A meta-analysis. J Viral Hepat. 2020;27(4):415–27. doi: 10.1111/jvh.13248. [DOI] [PubMed] [Google Scholar]
  • [19].Xie WY, Sun C, He H, Deng C, Sheng Y. Estimates of the prevalence of occult HBV infection in Asia: a systematic review and meta-analysis. Infect Dis (Lond) 2022;54(12):881–96. doi: 10.1080/23744235.2022.2115126. [DOI] [PubMed] [Google Scholar]
  • [20].Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA G. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLOS Med. 2009;6(7):e1000097. doi: 10.1371/journal.pmed.1000097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [21].Manzini P, Abate ML, Valpreda C, Milanesi P, Curti F, Rizzetto M, et al. Evidence of acute primary occult hepatitis B virus infection in an Italian repeat blood donor. Transfusion. 2009;49(4):757–64. doi: 10.1111/j.1537-2995.2008.02041.x. [DOI] [PubMed] [Google Scholar]
  • [22].Raimondo G, Locarnini S, Pollicino T, Levrero M, Zoulim F, Lok AS, et al. Update of the statements on biology and clinical impact of occult hepatitis B virus infection. J Hepatol. 2019;71(2):397–408. doi: 10.1016/j.jhep.2019.03.034. [DOI] [PubMed] [Google Scholar]
  • [23].Choi D, Lee G, Kim KH, Bae H. Particulate matter exacerbates the death of dopaminergic neurons in Parkinson’s Disease through an inflammatory response. Int J Mol Sci. 2022;23(12) doi: 10.3390/ijms23126487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [24].Hoy D, Brooks P, Woolf A, Blyth F, March L, Bain C, et al. Assessing risk of bias in prevalence studies: modification of an existing tool and evidence of interrater agreement. J Clin Epidemiol. 2012;65(9):934–9. doi: 10.1016/j.jclinepi.2011.11.014. [DOI] [PubMed] [Google Scholar]
  • [25].DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–88. doi: 10.1016/0197-2456(86)90046-2. [DOI] [PubMed] [Google Scholar]
  • [26].Cochran WG. The combination of estimates from different experiments. Biometrics. 1954;10:101–29. [Google Scholar]
  • [27].Veroniki AA, Jackson D, Viechtbauer W, Bender R, Bowden J, Knapp G, et al. Methods to estimate the between-study variance and its uncertainty in meta-analysis. Res Synth Methods. 2016;7(1):55–79. doi: 10.1002/jrsm.1164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [28].Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. Bmj. 1997;315(7109):629–34. doi: 10.1136/bmj.315.7109.629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [29].Schwarzer G. meta: An R Package for Meta-Analysis. 2007;7:40–45. [Google Scholar]
  • [30].Borenstein MH, Higgins Larry V, Julian PT, Rothstein Hannah R. Introduction to Meta-Analysis. John Wiley and Sons; 2009. p. 421. [Google Scholar]
  • [31].Emad Allam M, et al. Hepatitis C virus in peripheral mononuclear cells in patients on regular hemodialysis. 2017:547–552. [Google Scholar]
  • [32].Mamdouh ME, Tamer M, Nayel Abd Elhamed Z. Occult Hepatitis B virus infection among Egyptian hepatitis C virus seropositive and seronegative hemodialysis patients in Sohag government. Upper Egypt. 2015:113–118. [Google Scholar]
  • [33].Gachara G, Magoro T, Mavhandu L, Lum E, Kimbi HK, Ndip RN, et al. Characterization of occult hepatitis B virus infection among HIV positive patients in Cameroon. AIDS Res Ther. 2017;14(1):11. doi: 10.1186/s12981-017-0136-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [34].Mahmoud OAEK, Ghazal AAER, Metwally DES, Shamseya MM, Hamdallah HM. Detection of occult hepatitis B virus among chronic hepatitis C patients. Alex J Med. 2016;52(2):115–23. [Google Scholar]
  • [35].N’Dri-Yoman T, Anglaret X, Messou E, Attia A, Polneau S, Toni T, et al. Occult HBV infection in untreated HIV-infected adults in Cote d’Ivoire. Antivir Ther. 2010;15(7):1029–34. doi: 10.3851/IMP1641. [DOI] [PubMed] [Google Scholar]
  • [36].Ali NK, Mohamed RR, Saleh BE, Alkady MM, Farag ES. Occult hepatitis C virus infection among haemodialysis patients. Arab J Gastroenterol. 2018;19(3):101–5. doi: 10.1016/j.ajg.2018.09.001. [DOI] [PubMed] [Google Scholar]
  • [37].Akintule OA, Olusola BA, Odaibo GN, Olaleye DO. Occult HBV infection in Nigeria. Arch Basic Appl Med. 2018;6(1):87–93. [PMC free article] [PubMed] [Google Scholar]
  • [38].Hannachi N, Bahri O, Ben Fredj N, Boukadida J, Triki H. Risk of vertical transmission of hepatitis B virus in Tunisia. Arch Inst Pasteur Tunis. 2010;87(1-2):17–24. [PubMed] [Google Scholar]
  • [39].Dhifallah I, Khedhiri M, Chouikha A, Kharroubi G, Hammami W, Sadraoui A, et al. Hepatitis viruses take advantage of traditional practices to increase the burden of hepatocellular carcinoma in Tunisia. Arch Virol. 2020;165(1):33–42. doi: 10.1007/s00705-019-04440-5. [DOI] [PubMed] [Google Scholar]
  • [40].Fopa D, Candotti D, Tagny CT, Doux C, Mbanya D, Murphy EL, et al. Occult hepatitis B infection among blood donors from Yaoundé, Cameroon. Blood Transfus. 2019;17(6):403–8. doi: 10.2450/2019.0182-19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [41].Gouas DA, Villar S, Ortiz-Cuaran S, Legros P, Ferro G, Kirk GD, et al. TP53 R249S mutation, genetic variations in HBX and risk of hepatocellular carcinoma in The Gambia. Carcinogenesis. 2012;33(6):1219–24. doi: 10.1093/carcin/bgs135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [42].Khattab MA, Zakaria Y, Sadek E, Abd El Fatah AS, Fouad M, Khattab M, et al. Detection of hepatitis C virus (HCV) RNA in the peripheral blood mononuclear cells of HCV-infected patients following sustained virologic response. Clin Exp Med. 2022 doi: 10.1007/s10238-022-00791-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [43].Elgohry I, Elbanna A, Hashad D. Occult hepatitis B virus infection in a cohort of Egyptian chronic hemodialysis patients. Clin Lab. 2012;58(9-10):1057–61. [PubMed] [Google Scholar]
  • [44].Salpini R, Fokam J, Ceccarelli L, Santoro MM, Nanfack A, Sosso SM, et al. High burden of HBV-infection and atypical HBV strains among HIV-infected Cameroonians. Curr HIV Res. 2016;14(2):165–71. doi: 10.2174/1570162x13666150930114742. [DOI] [PubMed] [Google Scholar]
  • [45].Elkashef KA, Emam WA, Mesbah NM, Abo-Elmatty DM, Abdel-Hamed AR. Prevalence of occult Hepatitis C virus infection in egyptian patients with lymphoma: a new vision. Diagn (Basel) 2022;12(4) doi: 10.3390/diagnostics12041015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [46].Elmaghloub R, Elbahrawy A, El Didamony G, Hashim A, Morsy MH, Hantour O, et al. Occult hepatitis B infection in Egyptian health care workers. East Mediterr Health J. 2017;23(5):329–34. doi: 10.26719/2017.23.5.329. [DOI] [PubMed] [Google Scholar]
  • [47].Kishk R, Atta HA, Ragheb M, Kamel M, Metwally L, Nemr N. Genotype characterization of occult hepatitis B virus strains among Egyptian chronic hepatitis C patients. East Mediterr Health J. 2014;20(2):130–8. [PubMed] [Google Scholar]
  • [48].Daef EA, Makhlouf NA, Ahmed EH, Mohamed AI, Abd El Aziz MH, El-Mokhtar MA. Serological and molecular diagnosis of occult hepatitis B virus infection in Hepatitis C chronic liver diseases. Egypt J Immunol. 2017;24(1):37–48. [PubMed] [Google Scholar]
  • [49].Mahmoud AI, Elsherbiny NM, Afifi NA, Ahmed BM, Yasin AS. Occult Hepatitis B infection among blood donors in Al Azhar university hospital, Upper Egypt: the current status after 25 years of vaccine introduction. Egypt J Immunol. 2018;25(1):45–56. [PubMed] [Google Scholar]
  • [50].Mohamed EA, Elballat MAE, El-Awdy MMK. Hepatitis C virus in peripheral mononuclear cells in patients on regular hemodialysis. Egypt J Hosp Med. 2017;67(2):547–52. [Google Scholar]
  • [51].Taha SE, El-Hady SA, Ahmed TM, Ahmed IZ. Detection of occult HBV infection by nested PCR assay among chronic hepatitis C patients with and without hepatocellular carcinoma. Egypt J Med Hum Genet. 2013;14(4):353–60. [Google Scholar]
  • [52].El-Shishtawy S, Sherif N, Abdallh E, Kamel L, Shemis M, Saleem AA, et al. Occult Hepatitis C virus infection in hemodialysis patients; single center study. Electron Physician. 2015;7(8):1619–25. doi: 10.19082/1619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [53].Abdelmoemen G, Khodeir SA, Abou-Saif S, Kobtan A, Abd-Elsalam S. Prevalence of occult hepatitis C virus among hemodialysis patients in Tanta university hospitals: a single-center study. Environ Sci Pollut Res Int. 2018;25(6):5459–64. doi: 10.1007/s11356-017-0897-y. [DOI] [PubMed] [Google Scholar]
  • [54].Thabit AG, Hassan MA, Agban MN, Makhlouf NA, Khalil NK, Hassan HM, et al. Prevalence of occult HBV infection among chronic hepatitis C patients in upper Egypt. Environ Sci Pollut Res Int. 2017;24(1):131–42. [PubMed] [Google Scholar]
  • [55].El-Maksoud MA, Habeeb MR, Ghazy HF, Nomir MM, Elalfy H, Abed S, et al. Clinicopathological study of occult hepatitis B virus infection in hepatitis C virus-associated hepatocellular carcinoma. Eur J Gastroenterol Hepatol. 2019;31(6):716–22. doi: 10.1097/MEG.0000000000001388. [DOI] [PubMed] [Google Scholar]
  • [56].Serwah MA, Omar SA, Khedr MS, Abdel-Hamid A. Occurrence and clinical characteristics of occult hepatitis C virus infection in hemodialysis units at Ismailia, Egypt. Eur J Gastroenterol Hepatol. 2021;33:1009–14. doi: 10.1097/MEG.0000000000002075. [DOI] [PubMed] [Google Scholar]
  • [57].Selim HS, Abou-Donia HA, Taha HA, El Azab GI, Bakry AF. Role of occult hepatitis B virus in chronic hepatitis C patients with flare of liver enzymes. Eur J Intern Med. 2011;22(2):187–90. doi: 10.1016/j.ejim.2010.12.001. [DOI] [PubMed] [Google Scholar]
  • [58].Mbangiwa T, Kasvosve I, Anderson M, Thami PK, Choga WT, Needleman A, et al. Chronic and occult Hepatitis B virus infection in pregnant women in Botswana. Genes (Basel) 2018;9(5) doi: 10.3390/genes9050259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [59].Abu El Makarem MA, Abdel Hamid M, Abdel Aleem A, Ali A, Shatat M, Sayed D, et al. Prevalence of occult hepatitis B virus infection in hemodialysis patients from egypt with or without hepatitis C virus infection. Hepat Mon. 2012;12(4):253–8. doi: 10.5812/hepatmon.665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [60].Youssef SS, Nasr AS, El Zanaty T, El Rawi RS, Mattar MM. Prevalence of occult hepatitis C virus in egyptian patients with chronic lymphoproliferative disorders. Hepat Res Treat. 2012;2012:429784. doi: 10.1155/2012/429784. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [61].Elrashidy H, El-Didamony G, Elbahrawy A, Hashim A, Alashker A, Morsy MH, et al. Absence of occult hepatitis B virus infection in sera of diabetic children and adolescents following hepatitis B vaccination. Hum Vaccin Immunother. 2014;10(8):2336–41. doi: 10.4161/hv.29521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [62].Zaghloul H, El-Sherbiny W. Detection of occult hepatitis C and hepatitis B virus infections from peripheral blood mononuclear cells. Immunol Invest. 2010;39(3):284–91. doi: 10.3109/08820131003605820. [DOI] [PubMed] [Google Scholar]
  • [63].Beykaso G, Mulu A, Giday M, Berhe N, Selamu M, Hailu D, et al. Occult Hepatitis B Virus Infection and Its Risks of Cryptic Transmission in Southern Ethiopia. Infect Drug Resist. 2022;15:619–30. doi: 10.2147/IDR.S344668. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [64].Mekky MA, Sayed HI, Abdelmalek MO, Saleh MA, Osman OA, Osman HA, et al. Prevalence and predictors of occult hepatitis C virus infection among Egyptian patients who achieved sustained virologic response to sofosbuvir/daclatasvir therapy: a multi-center study. Infect Drug Resist. 2019;12:273–9. doi: 10.2147/IDR.S181638. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [65].Foaud H, Maklad S, Mahmoud F, El-Karaksy H. Occult hepatitis B virus infection in children born to HBsAg-positive mothers after neonatal passive-active immunoprophylaxis. Infection. 2015;43(3):307–14. doi: 10.1007/s15010-015-0733-6. [DOI] [PubMed] [Google Scholar]
  • [66].Yousif MM, Elsadek Fakhr A, Morad EA, Kelani H, Hamed EF, Elsadek HM, et al. Prevalence of occult hepatitis C virus infection in patients who achieved sustained virologic response to direct-acting antiviral agents. Infez Med. 2018;26(3):237–43. [PubMed] [Google Scholar]
  • [67].Abdelaziz H, et al. Molecular and serological characterization of occult hepatitis B among blood donors in Maputo, Mozambique. Int J Immunopathol Pharm. 2020;115:e200006. doi: 10.1590/0074-02760200006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [68].Firnhaber C, Viana R, Reyneke A, Schultze D, Malope B, Maskew M, et al. Occult hepatitis B virus infection in patients with isolated core antibody and HIV co-infection in an urban clinic in Johannesburg, South Africa. Int J Infect Dis. 2009;13(4):488–92. doi: 10.1016/j.ijid.2008.08.018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [69].Mudawi H, Hussein W, Mukhtar M, Yousif M, Nemeri O, Glebe D, et al. Overt and occult hepatitis B virus infection in adult Sudanese HIV patients. Int J Infect Dis. 2014;29:65–70. doi: 10.1016/j.ijid.2014.07.004. [DOI] [PubMed] [Google Scholar]
  • [70].Youssef A, Yano Y, El-Sayed Zaki M, Utsumi T, Hayashi Y. Characteristics of hepatitis viruses among Egyptian children with acute hepatitis. Int J Oncol. 2013;42(4):1459–65. doi: 10.3892/ijo.2013.1822. [DOI] [PubMed] [Google Scholar]
  • [71].Lotfi AA, Mohamed AE, Shalaby NA, Eissa DS, El-Dabaa E, Sallam AM, et al. Occult hepatitis C virus infection in patients with malignant lymphoproliferative disorders. Int J Immunopathol Pharmacol. 2020;34:2058738420961202. doi: 10.1177/2058738420961202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [72].Firnhaber C, Chen CY, Evans D, Maskew M, Schulz D, Reyneke A, et al. Prevalence of hepatitis B virus (HBV) co-infection in HBV serologically-negative South African HIV patients and retrospective evaluation of the clinical course of mono-and co-infection. Int J Infect Dis. 2012;16(4):E268–72. doi: 10.1016/j.ijid.2011.12.007. [DOI] [PubMed] [Google Scholar]
  • [73].Bajjou T, Elannaz H, Tagajdid M, Elghafouli H, Laraqui A, Abi R, et al. Occult hepatitis B virus infection in Moroccan HIV infected patients. Int J Res Med Sci. 2015 March;3(3):617. 2015 2017. [Google Scholar]
  • [74].Youssef A, Yano Y, Utsumi T, abd El-alah EM, abd El-Hameed A, Serwah A, et al. Molecular epidemiological study of hepatitis viruses in Ismailia, Egypt. Intervirology. 2009;52(3):123–31. doi: 10.1159/000219385. [DOI] [PubMed] [Google Scholar]
  • [75].Hamers RL, Zaaijer HL, Wallis CL, Siwale M, Ive P, Botes ME, et al. HIV-HBV coinfection in Southern Africa and the effect of lamivudine- versus tenofovir-containing cART on HBV outcomes. J Acquir Immune Defic Syndr. 2013;64(2):174–82. doi: 10.1097/QAI.0b013e3182a60f7d. [DOI] [PubMed] [Google Scholar]
  • [76].Mahgoub S, Candotti D, El Ekiaby M, Allain JP. Hepatitis B virus (HBV) infection and recombination between HBV genotypes D and E in asymptomatic blood donors from Khartoum, Sudan. J Clin Microbiol. 2011;49(1):298–306. doi: 10.1128/JCM.00867-10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [77].Abd Alla MDA, Elibiary SA, Wu GY, El-Awady MK. Occult HCV Infection (OCI) diagnosis in cirrhotic and non-cirrhotic naïve patients by intra-PBMC nested viral RNA PCR. J Clin Transl Hepatol. 2017;5(4):319–26. doi: 10.14218/JCTH.2017.00034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [78].Amponsah-Dacosta E, Lebelo RL, Rakgole JN, Selabe SG, Gededzha MP, Mayaphi SH, et al. Hepatitis B virus infection in post-vaccination South Africa: occult HBV infection and circulating surface gene variants. J Clin Virol. 2015;63:12–7. doi: 10.1016/j.jcv.2014.11.032. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [79].Mphahlele MJ, Lukhwareni A, Burnett RJ, Moropeng LM, Ngobeni JM. High risk of occult hepatitis B virus infection in HIV-positive patients from South Africa. J Clin Virol. 2006;35(1):14–20. doi: 10.1016/j.jcv.2005.04.003. [DOI] [PubMed] [Google Scholar]
  • [80].Abd El Kader Mahmoud O, Abd El Rahim Ghazal A, El Sayed Metwally D, Elnour AM, Yousif GE. Detection of occult hepatitis B virus infection among blood donors in Sudan. J Egypt Public Health Assoc. 2013;88(1):14–8. doi: 10.1097/01.EPX.0000427065.73965.c8. [DOI] [PubMed] [Google Scholar]
  • [81].El-Ghitany EM, Farghaly AG, Hashish MH. Occult hepatitis B virus infection among hepatitis C virus seropositive and seronegative blood donors in Alexandria, Egypt. J Egypt Public Health Assoc. 2013;88(1):8–13. doi: 10.1097/01.EPX.0000422774.29308.b3. [DOI] [PubMed] [Google Scholar]
  • [82].El-Sherif A, Abou-Shady M, Abou-Zeid H, Elwassief A, Elbahrawy A, Ueda Y, et al. Antibody to hepatitis B core antigen as a screening test for occult hepatitis B virus infection in Egyptian chronic hepatitis C patients. J Gastroenterol. 2009;44(4):359–64. doi: 10.1007/s00535-009-0020-3. [DOI] [PubMed] [Google Scholar]
  • [83].Kew MC, Welschinger R, Viana R. Occult hepatitis B virus infection in Southern African blacks with hepatocellular carcinoma. J Gastroenterol Hepatol. 2008;23(9):1426–30. doi: 10.1111/j.1440-1746.2008.05481.x. [DOI] [PubMed] [Google Scholar]
  • [84].Shaker O, Ahmed A, Abdel Satar I, El Ahl H, Shousha W, Doss W. Occult hepatitis B in Egyptian thalassemic children. J Infect Dev Ctries. 2012;6(4):340–6. doi: 10.3855/jidc.1706. [DOI] [PubMed] [Google Scholar]
  • [85].Ndow G, et al. Prevalence and clinical significance of occult hepatitis B infection in The Gambia, West Africa. J Infect Dis. 2021 doi: 10.1093/infdis/jiab327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [86].Helaly GF, El Ghazzawi EF, Shawky SM, Farag FM. Occult hepatitis B virus infection among chronic hemodialysis patients in Alexandria, Egypt. J Infect Public Health. 2015;8(6):562–9. doi: 10.1016/j.jiph.2015.04.019. [DOI] [PubMed] [Google Scholar]
  • [87].Omar HH, Taha SA, Hassan WH, Omar HH. Impact of schistosomiasis on increase incidence of occult hepatitis B in chronic hepatitis C patients in Egypt. J Infect Public Health. 2017;10(6):761–5. doi: 10.1016/j.jiph.2016.11.010. [DOI] [PubMed] [Google Scholar]
  • [88].Hoffmann CJ, Mashabela F, Cohn S, Hoffmann JD, Lala S, Martinson NA, et al. Maternal hepatitis B and infant infection among pregnant women living with HIV in South Africa. J Int AIDS Soc. 2014;17(1):18871. doi: 10.7448/IAS.17.1.18871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [89].Abdelrahim SS, Khairy R, Esmail MA, Ragab M, Abdel-Hamid M, Abdelwahab SF. Occult hepatitis C virus infection among Egyptian hemodialysis patients. J Med Virol. 2016;88(8):1388–93. doi: 10.1002/jmv.24467. [DOI] [PubMed] [Google Scholar]
  • [90].Apica BS, Seremba E, Rule J, Yuan HJ, Lee WM. High prevalence of occult hepatitis B infection in an African urban population. J Med Virol. 2016;88(4):674–80. doi: 10.1002/jmv.24372. [DOI] [PubMed] [Google Scholar]
  • [91].Barth RE, Huijgen Q, Tempelman HA, Mudrikova T, Wensing AM, Hoepelman AI. Presence of occult HBV, but near absence of active HBV and HCV infections in people infected with HIV in rural South Africa. J Med Virol. 2011;83(6):929–34. doi: 10.1002/jmv.22026. [DOI] [PubMed] [Google Scholar]
  • [92].Compston LI, Li C, Sarkodie F, Owusu-Ofori S, Opare-Sem O, Allain JP. Prevalence of persistent and latent viruses in untreated patients infected with HIV-1 from Ghana, West Africa. J Med Virol. 2009;81(11):1860–8. doi: 10.1002/jmv.21614. [DOI] [PubMed] [Google Scholar]
  • [93].El Shazly Y, Hemida K, Rafik M, Al Swaff R, Ali-Eldin ZA, GadAllah S. Detection of occult hepatitis C virus among healthy spouses of patients with HCV infection. J Med Virol. 2015;87(3):424–7. doi: 10.1002/jmv.24074. [DOI] [PubMed] [Google Scholar]
  • [94].Lukhwareni A, Burnett RJ, Selabe SG, Mzileni MO, Mphahlele MJ. Increased detection of HBV DNA in HBsAg-positive and HBsAg-negative South African HIV/AIDS patients enrolling for highly active antiretroviral therapy at a Tertiary Hospital. J Med Virol. 2009;81(3):406–12. doi: 10.1002/jmv.21418. [DOI] [PubMed] [Google Scholar]
  • [95].Meschi S, Schepisi MS, Nicastri E, Bevilacqua N, Castilletti C, Sciarrone MR, et al. The prevalence of antibodies to human herpesvirus 8 and hepatitis B virus in patients in two hospitals in Tanzania. J Med Virol. 2010;82(9):1569–75. doi: 10.1002/jmv.21852. [DOI] [PubMed] [Google Scholar]
  • [96].Musyoki AM, Msibi TL, Motswaledi MH, Selabe SG, Monokoane TS, Mphahlele MJ. Active co-infection with HBV and/or HCV in South African HIV positive patients due for cancer therapy. J Med Virol. 2015;87(2):213–21. doi: 10.1002/jmv.24055. [DOI] [PubMed] [Google Scholar]
  • [97].Powell EA, Gededzha MP, Rentz M, Rakgole NJ, Selabe SG, Seleise TA, et al. Mutations associated with occult hepatitis B in HIV-positive South Africans. J Med Virol. 2015;87(3):388–400. doi: 10.1002/jmv.24057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [98].El-Sayed MH, Said Z, Abo-Elmagd EK, Ebeid F, Salama II. High risk of HBV infection among vaccinated polytransfused children with malignancy. J Pedia Hematol Oncol. 2021;43(1):e45–50. doi: 10.1097/MPH.0000000000001887. [DOI] [PubMed] [Google Scholar]
  • [99].Opaleye OO, Oluremi AS, Atiba AB, Adewumi MO, Mabayoje OV, Donbraye E, et al. Occult Hepatitis B virus infection among HIV positive patients in Nigeria. J Trop Med. 2014;2014:796121. doi: 10.1155/2014/796121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [100].Raouf HE, Yassin AS, Megahed SA, Ashour MS, Mansour TM. Seroprevalence of occult hepatitis B among Egyptian paediatric hepatitis C cancer patients. J Viral Hepat. 2015;22(2):103–11. doi: 10.1111/jvh.12260. [DOI] [PubMed] [Google Scholar]
  • [101].Chasela CS, Kourtis AP, Wall P, Drobeniuc J, King CC, Thai H, et al. Hepatitis B virus infection among HIV-infected pregnant women in Malawi and transmission to infants. J Hepatol. 2014;60(3):508–14. doi: 10.1016/j.jhep.2013.10.029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [102].Kitab B, Ezzikouri S, Alaoui R, Nadir S, Badre W, Trepo C, et al. Occult HBV infection in Morocco: from chronic hepatitis to hepatocellular carcinoma. Liver Int. 2014;34(6):e144–50. doi: 10.1111/liv.12482. [DOI] [PubMed] [Google Scholar]
  • [103].Said ZN, El-Sayed MH, El-Bishbishi IA, El-Fouhil DF, Abdel-Rheem SE, El-Abedin MZ, et al. High prevalence of occult hepatitis B in hepatitis C-infected Egyptian children with haematological disorders and malignancies. Liver Int. 2009;29(4):518–24. doi: 10.1111/j.1478-3231.2009.01975.x. [DOI] [PubMed] [Google Scholar]
  • [104].Mhalla S, Hammoud R, Frih A, Kadri Y, El Argoubi A, Elmay M, et al. Prevalence and risk factors of hepatitis B and C among hemodialysis patients in Tunisia. Med Mal Infect. 2018;48(3):175–9. doi: 10.1016/j.medmal.2017.11.006. [DOI] [PubMed] [Google Scholar]
  • [105].Diarra B, Yonli AT, Sorgho PA, Compaore TR, Ouattara AK, Zongo WA, et al. Occult Hepatitis B Virus Infection and Associated Genotypes among HBsAg-negative Subjects in Burkina Faso. Mediterr J Hematol Infect Dis. 2018;10(1):e2018007. doi: 10.4084/MJHID.2018.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [106].Akinbami A, Badiru M, Uche E, Onyekwere C, Ismail K, Olowoselu O, et al. The Prevalence of Occult Hepatitis B Infection among Blood Donors in Lagos, Nigeria. Niger Med J. 2019;60(1):22–6. doi: 10.4103/nmj.NMJ_29_19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [107].Otegbayo JA, et al. Profile of Hepatitis B and Hepatitis C Markers in Asymptomatic Chronic HBV Infection in an Endemic Population. Niger J Gastroenterol Hepatol. 2009;1(2) [Google Scholar]
  • [108].Ryan K, Anderson M, Gyurova I, Ambroggio L, Moyo S, Sebunya T, et al. High Rates of Occult Hepatitis B Virus Infection in HIV-positive individuals initiating antiretroviral therapy in Botswana. Open Forum Infect Dis. 2017;4(4):ofx195. doi: 10.1093/ofid/ofx195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [109].Kengne M, Medja Y, Tedom, Nwobegahay JM. Residual risk for transfusion-transmitted hepatitis B virus infection due to occult hepatitis B virus infection in donors living in Yaoundé, Cameroon. Pan Afr Med J. 2021;39:175. doi: 10.11604/pamj.2021.39.175.22365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [110].Peliganga LB, Mello VM, de Sousa P, Horta M, Soares ÁD, Nunes J, et al. Transfusion transmissible infections in blood donors in the Province of Bié, Angola, during a 15-Year follow-up, imply the need for pathogen reduction technologies. Pathogens. 2021;10(12) doi: 10.3390/pathogens10121633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [111].Aluora PO. Seroprevalence and genotypic characterization of HBV among low risk voluntary blood donors in Nairobi, Kenya. PLoS One. 2020;17(1):176. doi: 10.1186/s12985-020-01447-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [112].Bell TG, Makondo E, Martinson NA, Kramvis A. Hepatitis B virus infection in human immunodeficiency virus infected southern African adults: occult or overt-that is the question. PLoS One. 2012;7(10):e45750. doi: 10.1371/journal.pone.0045750. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [113].Bivigou-Mboumba B, Amougou-Atsama M, Zoa-Assoumou S, M’boyis Kamdem H, Nzengui-Nzengui GF, Ndojyi-Mbiguino A, et al. Hepatitis B infection among HIV infected individuals in Gabon: occult hepatitis B enhances HBV DNA prevalence. PLoS One. 2018;13(1):e0190592. doi: 10.1371/journal.pone.0190592. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [114].Bivigou-Mboumba B, François-Souquière S, Deleplancque L, Sica J, Mouinga-Ondémé A, Amougou-Atsama M, et al. Broad Range of Hepatitis B Virus (HBV) patterns, dual circulation of quasi-subgenotype A3 and HBV/E and heterogeneous HBV mutations in HIV-positive patients in Gabon. PLoS One. 2016;11(1):e0143869. doi: 10.1371/journal.pone.0143869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [115].Carimo AA, Gudo ES, Maueia C, Mabunda N, Chambal L, Vubil A, et al. First report of occult hepatitis B infection among ART naïve HIV seropositive in-dividuals in Maputo, Mozambique. PLoS One. 2018;13(1):e0190775. doi: 10.1371/journal.pone.0190775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [116].Jepkemei KB, Ochwoto M, Swidinsky K, Day J, Gebrebrhan H, McKinnon LR, et al. Characterization of occult hepatitis B in high-risk populations in Kenya. PLoS One. 2020;15(5):e0233727. doi: 10.1371/journal.pone.0233727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [117].Oluyinka OO, Tong HV, Bui Tien S, Fagbami AH, Adekanle O, Ojurongbe O, et al. Occult Hepatitis B Virus Infection in Nigerian Blood Donors and Hepatitis B Virus Transmission Risks. PLoS One. 2015;10(7):e0131912. doi: 10.1371/journal.pone.0131912. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [118].Patel NH, Meier-Stephenson V, Genetu M, Damtie D, Abate E, Alemu S, et al. Prevalence and genetic variability of occult hepatitis B virus in a human im-munodeficiency virus positive patient cohort in Gondar, Ethiopia. PLoS One. 2020;15(11):e0242577. doi: 10.1371/journal.pone.0242577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [119].Salyani A, Shah J, Adam R, Otieno G, Mbugua E, Shah R. Occult hepatitis B virus infection in a Kenyan cohort of HIV infected anti-retroviral therapy naive adults. PloS One. 2021;16(1):e0244947. doi: 10.1371/journal.pone.0244947. 0244947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [120].Mandour M, Nemr N, Shehata A, Kishk R, Badran D, Hawass N. Occult HBV infection status among chronic hepatitis C and hemodialysis patients in Northeastern Egypt: regional and national overview. Rev Soc Bras Med Trop. 2015;48(3):258–64. doi: 10.1590/0037-8682-0037-2015. [DOI] [PubMed] [Google Scholar]
  • [121].Ayuk J, Mphahlele J, Bessong P. Hepatitis B virus in HIV-infected patients in northeastern South Africa: prevalence, exposure, protection and response to HAART. S Afr Med J. 2013;103(5):330–3. doi: 10.7196/samj.6304. [DOI] [PubMed] [Google Scholar]
  • [122].Mayaphi SH, Roussow TM, Masemola DP, Olorunju SA, Mphahlele MJ, Martin DJ. HBV/HIV co-infection: the dynamics of HBV in South African patients with AIDS. S Afr Med J. 2012;102(3 Pt 1):157–62. doi: 10.7196/samj.4944. [DOI] [PubMed] [Google Scholar]
  • [123].Alduraywish A, Ragheb M, Taher I, Louis N, Aldossari K, Kishk R. Prevalence, risk factors and impact of occult HCV infection on liver morbidity among haemo-dialysis patients: hospital-based cross-sectional study. Scand J Gastroenterol. 2020;55(8):963–9. doi: 10.1080/00365521.2020.1790649. [DOI] [PubMed] [Google Scholar]
  • [124].Ayana DA, Mulu A, Mihret A, Seyoum B, Aseffa A, Howe R. Occult Hepatitis B virus infection among HIV negative and positive isolated anti-HBc individuals in eastern Ethiopia. Sci Rep. 2020;10(1):22182. doi: 10.1038/s41598-020-79392-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [125].de Mendoza C, Bautista JM, Pérez-Benavente S, Kwawu R, Fobil J, Soriano V, et al. Screening for retroviruses and hepatitis viruses using dried blood spots reveals a high prevalence of occult hepatitis B in Ghana. Ther Adv Infect Dis. 2019;6:2049936119851464. doi: 10.1177/2049936119851464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [126].El-Zayadi AR, Ibrahim EH, Badran HM, Saeid A, Moneib NA, Shemis MA, et al. Anti-HBc screening in Egyptian blood donors reduces the risk of hepatitis B virus transmission. Transfus Med. 2008;18(1):55–61. doi: 10.1111/j.1365-3148.2007.00806.x. [DOI] [PubMed] [Google Scholar]
  • [127].Busch M, et al. Seronegative and occult hepatitis C virus infections in patients with hematological disorders. Transfusion. 2017;162(1):63–9. doi: 10.1007/s00705-016-3049-7. [DOI] [PubMed] [Google Scholar]
  • [128].Sondlane TH, Mawela L, Razwiedani LL, Selabe SG, Lebelo RL, Rakgole JN, et al. High prevalence of active and occult hepatitis B virus infections in healthcare workers from two provinces of South Africa. Vaccine. 2016;34(33):3835–9. doi: 10.1016/j.vaccine.2016.05.040. [DOI] [PubMed] [Google Scholar]
  • [129].Belyhun Y, Liebert UG, Maier M. Molecular epidemiology of hepatitis B virus among HIV co-infected and mono-infected cohorts in Northwest Ethiopia. Virol J. 2022;19(1):53. doi: 10.1186/s12985-022-01774-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [130].Emara MH, El-Gammal NE, Mohamed LA, Bahgat MM. Occult hepatitis B infection in egyptian chronic hepatitis C patients: prevalence, impact on pegylated interferon/ribavirin therapy. Virol J. 2010;7:324. doi: 10.1186/1743-422X-7-324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [131].Hassan ZK, Hafez MM, Mansor TM, Zekri AR. Occult HBV infection among Egyptian hepatocellular carcinoma patients. Virol J. 2011;8:90. doi: 10.1186/1743-422X-8-90. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [132].Kishk R, Nemr N, Elkady A, Mandour M, Aboelmagd M, Ramsis N, et al. Hepatitis B surface gene variants isolated from blood donors with overt and occult HBV infection in north eastern Egypt. Virol J. 2015;12:153. doi: 10.1186/s12985-015-0389-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [133].Olotu AA, Oyelese AO, Salawu L, Audu RA, Okwuraiwe AP, Aboderin AO. Occult Hepatitis B virus infection in previously screened, blood donors in Ile-Ife, Nigeria: implications for blood transfusion and stem cell transplantation. Virol J. 2016;13:76. doi: 10.1186/s12985-016-0533-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [134].Burnett RJ, et al. Molecular detection of occult Hepatitis B virus in plasma and urine of renal transplant patients in Khartoum state Sudan. Viruses. 2020;97:126–30. doi: 10.1016/j.ijid.2020.05.101. [DOI] [PubMed] [Google Scholar]
  • [135].van Drimmelen H, et al. Surveillance and impact of occult hepatitis B virus, SEN virus, and torque teno virus in Egyptian hemodialysis patients with chronic hepatitis C virus infection. Vox Sang. 2020;92:13–8. doi: 10.1016/j.ijid.2019.12.011. [DOI] [PubMed] [Google Scholar]
  • [136].Attia KA, Eholié S, Messou E, Danel C, Polneau S, Chenal H, et al. Prevalence and virological profiles of hepatitis B infection in human immunodeficiency virus patients. World J Hepatol. 2012;4(7):218–23. doi: 10.4254/wjh.v4.i7.218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [137].Elkady A, Iijima S, Aboulfotuh S, Mostafa Ali E, Sayed D, Abdel-Aziz NM, et al. Characteristics of escape mutations from occult hepatitis B virus infected patients with hematological malignancies in South Egypt. World J Hepatol. 2017;9(9):477–86. doi: 10.4254/wjh.v9.i9.477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [138].Said ZN, Sayed MH, Salama II, Aboel-Magd EK, Mahmoud MH, Setouhy ME, et al. Occult hepatitis B virus infection among Egyptian blood donors. World J Hepatol. 2013;5(2):64–73. doi: 10.4254/wjh.v5.i2.64. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [139].Kouyoumjian SP, Chemaitelly H, Abu-Raddad LJ. Characterizing hepatitis C virus epidemiology in Egypt: systematic reviews, meta-analyses, and metaregressions. Sci Rep. 2018;8(1):1661. doi: 10.1038/s41598-017-17936-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [140].Karoney MJ, Siika AM. Hepatitis C virus (HCV) infection in Africa: a review. Pan Afr Med J. 2013;14:44. doi: 10.11604/pamj.2013.14.44.2199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [141].D’Ambrosio R, Degasperi E, Colombo M, Aghemo A. Direct-acting antivirals: the endgame for hepatitis C? Curr Opin Virol. 2017;24:31–7. doi: 10.1016/j.coviro.2017.03.017. [DOI] [PubMed] [Google Scholar]
  • [142].Kenfack-Momo R, Kenmoe S, Takuissu GR, Ebogo-Belobo JT, Kengne-Ndé C, Mbaga DS, et al. Epidemiology of hepatitis B virus and/or hepatitis C virus infections among people living with human immunodeficiency virus in Africa: a systematic review and meta-analysis. PLoS One. 2022;17(5):e0269250. doi: 10.1371/journal.pone.0269250. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [143].Zampino R, Boemio A, Sagnelli C, Alessio L, Adinolfi LE, Sagnelli E, et al. Hepatitis B virus burden in developing countries. World J Gastroenterol. 2015;21(42):11941–53. doi: 10.3748/wjg.v21.i42.11941. [DOI] [PMC free article] [PubMed] [Google Scholar]

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