- Research article
- Open Access
- Open Peer Review
The epidemiology of hepatitis C virus in Egypt: a systematic review and data synthesis
BMC Infectious Diseases volume 13, Article number: 288 (2013)
Egypt has the highest prevalence of hepatitis C virus (HCV) in the world, estimated nationally at 14.7%. Our study’s objective was to delineate the evidence on the epidemiology of HCV infection among the different population groups in Egypt, and to draw analytical inferences about the nature of HCV transmission in this country.
We conducted a systematic review of all data on HCV prevalence and incidence in Egypt following PRISMA guidelines. The main sources of data included PubMed and Embase databases. We also used a multivariate regression model to infer the temporal trend of HCV prevalence among the general population and high risk population in Egypt.
We identified 150 relevant records, four of which were incidence studies. HCV incidence ranged from 0.8 to 6.8 per 1,000 person-years. Overall, HCV prevalence among pregnant women ranged between 5-15%, among blood donors between 5-25%, and among other general population groups between 0-40%. HCV prevalence among multi-transfused patients ranged between 10-55%, among dialysis patients between 50-90%, and among other high risk populations between 10% and 85%. HCV prevalence varied widely among other clinical populations and populations at intermediate risk. Risk factors appear to be parenteral anti-schistosomal therapy, injections, transfusions, and surgical procedures, among others. Results of our time trend analysis suggest that there is no evidence of a statistically significant decline in HCV prevalence over time in both the general population (p-value: 0.215) and high risk population (p-value: 0.426).
Egypt is confronted with an HCV disease burden of historical proportions that distinguishes this nation from others. A massive HCV epidemic at the national level must have occurred with substantial transmission still ongoing today. HCV prevention in Egypt must become a national priority. Policymakers, and public health and medical care stakeholders need to introduce and implement further prevention measures targeting the routes of HCV transmission.
The Egyptian Demographic Health Survey (EDHS), a cross sectional survey including hepatitis C virus (HCV) biomarkers, was conducted in 2008 on a large nationally representative sample . It estimated HCV prevalence among the 15–59 years age group to be 14.7% . Accordingly, Egypt has the highest HCV prevalence in the world [2–4]. This unparalleled level of exposure to this infection appears to reflect a national level epidemic. It has been postulated that the epidemic has been caused by extensive iatrogenic transmission during the era of parenteral-antischistosomal-therapy (PAT) mass-treatment campaigns [5, 6]. Today, HCV infection and its complications are among the leading public health challenges in Egypt .
Multiple community- and facility-based studies were conducted among different population groups in Egypt over the last two decades to assess the distribution of infection in the population. These studies have immensely improved our understanding of HCV epidemiology in Egypt. Nevertheless, two lingering and critical questions regarding HCV transmission in Egypt are yet to be addressed satisfactorily:
Does the high HCV prevalence reflect mainly historical exposures during the PAT campaigns before 1985, with limited current infection incidence?
If not, to what extent is HCV transmission still ongoing, and what are the drivers, risk factors, and modes of this transmission?
The objective of our study is to attempt, at least in part, to address these two questions through a comprehensive systematic review and integrated analysis of multiple sources of data about HCV prevalence and incidence in Egypt. Our study examined side-by-side information collected by different methods, by different investigators, and in different populations, allowing us to corroborate hypotheses across datasets, thereby reducing the impact of potential biases that can exist in a single study, dataset, or line of evidence. Our approach also facilitated an identification of the key research, policy, and programming priorities that require further investigation and consideration.
Data sources and search strategy
We conducted a systematic review of the prevalence and incidence of HCV in the different population groups in Egypt following the PRISMA guidelines . The PRISMA checklist can be found in Table S1, see Additional file 1. The main data sources for this investigation were: PubMed (Medline) and Embase databases. The above data sources were searched with no time or language restrictions. PubMed and Embase were searched using both MeSH/Emtree terms, respectively, and text terms. MeSH/Emtree terms were exploded to cover all subheadings. Details of the search criteria for each of these databases can be found below:
PubMed: ((“Hepatitis C”[Mesh] OR “Hepatitis C Antibodies”[Mesh] OR “Hepatitis C Antigens”[Mesh] OR “Hepacivirus”[Mesh] OR “Hepatitis C, chronic/epidemiology”[Mesh] OR “Hepatitis C, chronic/etiology”[Mesh] OR “Hepatitis C, chronic/transmission”[Mesh] OR “Hepatitis C, chronic/virology”[Mesh] OR “Hepatitis C”[Text] OR “HCV”[Text]) AND (“Egypt”[Mesh] or Egypt[Text])).
Embase: (egypt.mp. or exp Egypt/) and (exp hepatitis C/ or exp Hepatitis C virus/ or hepatitis C.mp. or HCV.mp. or hepacivirus.mp.).
Our study did not need an ethics committee approval or written informed consent because it relies entirely on published data.
The results of the searches were imported to a reference manager, Endnote, where duplicate publications were identified and excluded. The remaining unique and potentially relevant records were then imported into Microsoft Excel where screening for relevance and eligibility took place. The titles and abstracts of all records retrieved were screened for relevance independently by two of the authors (YM and SR). Screening for relevance was conducted in two stages: 1) Stage 1 involved screening all titles and abstracts to exclude all non-relevant articles; 2) Stage 2 involved retrieving and screening the full-text of all articles deemed relevant after the initial abstract screening, to further exclude any remaining non-eligible articles. Inconsistencies between reviewers were discussed and sorted out by consensus.
A publication was considered eligible for inclusion in the review if it had data on at least one of the following outcomes of interest: 1) prevalence of HCV as detected by HCV antibodies; and 2) incidence of HCV as detected by HCV antibodies. Only studies reporting primary data were included. Reviews of literature were excluded, but all data reported were checked and compared to the results of our search. Any additional study identified in the excluded review and not retrieved by our search was identified and added to our review. Case reports and case series were excluded. All other study designs were eligible for inclusion. Distinction was made between the number of “reports” (actual publications i.e. papers, conference abstracts etc.) and the number of “studies” (actual study and research project). Multiple reports of the same study were identified as duplicates and counted as one study.
Eligible studies were then categorized into two types: prevalence studies and incidence studies. Any article reporting both the prevalence and incidence of HCV was counted as two studies, one for incidence and one for prevalence. Results were then pooled into one list containing all eligible and unique studies.
Data extraction and population classification
The following data were then extracted from each eligible study included in the review: author, year of data collection, year of publication, city, study site, study design, sampling technique, population (blood donors, barbers, health care workers, injecting drug users (IDUs) etc.), socio-demographic characteristics of the population (sex, age, rural vs. urban etc.), sample size, and prevalence and/or incidence of HCV. Although our search criteria did not specifically target publications reporting HCV RNA prevalence or risk factors in Egypt, we extracted this information from eligible publications when available. Risk factors were extracted only if they were statistically significant in a multivariate regression analysis within a study that was found relevant according to our search criteria.
Data on the above mentioned indicators were extracted from included records and entered into a computerized database on Microsoft Excel. Extracted data were then classified and analyzed on the basis of the study population’s risk of acquiring HCV. The four defined major population risk groups are:
Populations at direct or high risk: this group includes IDUs, multi-transfused patients such as hemophiliacs and thalassemics, dialysis patients, and viral hepatitis patients, among others.
Populations at indirect or intermediate risk: this group includes familial contacts of HCV patients i.e. their children, spouses, and other household contacts; select practitioners of professions at risk of HCV such as dentists, healthcare workers and barbers; populations with potential IDU exposures including: prisoners and HIV patients; and populations with health facility/injecting exposures such as diabetic patients and hospitalized populations.
General population groups (populations which are not at an elevated risk of HCV exposure): pregnant women, blood donors, children, rural populations, army recruits or fire brigade personnel, outpatient clinic attendees, populations defined in case–control studies as healthy populations (controls), among other groups categorized together as “other general population” groups.
Special clinical population groups such as Hodgkin’s lymphoma (HL) patients, lichen planus (LP), and liver disease patients, among others. This category includes patients with specific diseases that require clinical care, and thus can be exposed to HCV in medical care facilities, though at variable levels of risk that is difficult to categorize among any of the above mentioned population groups.
Within any specific category of the above population groups, considerable heterogeneity and different subgroup trends may exist.
In order to create prevalence figures, HCV prevalence measures within each of the population groups above were stratified into two strata: pre-2001 and post-2001, based on the year in which the study was conducted. The year 2001 was chosen as the cut-off year, as this was the year in which the Egyptian Ministry of Health initiated broad infection control programs in the country .
Time trend analysis
We conducted a time trend analysis investigating the change in HCV prevalence among the general population and high risk population in Egypt with respect to time. We started by conducting univariate linear regression analyses examining the change in HCV prevalence over time in each of the general population subgroups separately. A similar analysis was conducted in each of the high risk population subgroups. To avoid systematic biases in any one subgroup and to increase the statistical power of the time trend analysis, we also used a multivariate linear regression model estimating the temporal trend in HCV prevalence, while adjusting for the different subgroups in each population grouping. Two such models were performed: one for the general population and the other for the high-risk population. Mean HCV prevalence was modeled using a model that includes as predictors: time (in years) and the different general population subgroups (or high risk population subgroups).
The general population regression model stipulates that:
Similarly, the high risk population regression model stipulates that:
In both models, βi are the parameters of the statistical model and Time and sub-population names are the indicator variables.
Data used for these analyses were extracted from the eligible studies included in this review. In the presence of both an overall HCV prevalence measure as well as stratified prevalence measures, we included only the overall prevalence measure. Including both overall and stratified prevalence measures from the same study would have given more weight to those studies, relative to others, thereby biasing our results. The year of data collection was estimated for studies missing this variable. This was done by conducting a correlation analysis between the year of data collection and the year of publication for studies having data on both, followed by a paired t-test to estimate the mean difference between them. We then applied this difference to the year of publication to estimate the year of data collection when missing. Midpoints were calculated and used for studies conducted over a number of years. The statistical analysis was conducted using STATA version 11 (STATA corporation, College Station, Texas).
The study selection process is described in Figure 1, as adapted from the PRISMA 2009 flow diagram . The number of records retrieved through both PubMed and Embase was 1,146 as of August 1, 2012, out of which 445 were excluded as duplicates. After assessing all documents according to their titles and abstracts, the full-text of 183 records were retrieved for screening in addition to 11 papers identified through references of reviews. Of those, 150 records were found eligible for inclusion in the present article. Only one relevant record was identified outside the PubMed and Embase search; the EDHS . No single report has reported both a relevant incidence measure and a relevant prevalence measure.
Five incidence measures were identified through our search, reported in four incidence reports (Table 1). All studies were conducted in rural areas of Egypt among village residents, pregnant women, and children [10–13]. Overall high HCV incidence rates were observed in these studies ranging from 0.8 to 6.8 per 1,000 person-years.
Prevalence of HCV in the general population
Sixty-nine studies reported HCV prevalence in the general population. Details are shown in Table 2. HCV prevalence among the general population of Egypt is documented to be very high. The 2008 EDHS measured HCV prevalence to be 14.7% among a nationally representative sample of 11,126 Egyptians aged 15–59 years old . The diverse HCV studies conducted among different general population subgroups, regardless of design or methodology, consistently report a very high HCV prevalence, as high as 41% in some studies . Overall, the prevalence appears to increase dramatically with age with the highest rates observed among populations aged greater than 40 years.
A number of studies were conducted among blood donors. A higher prevalence is observed among paid blood donors and family replacement blood donors compared to voluntary donors [10–12]. Male blood donors had a higher prevalence than their female counterparts . Blood donors from rural areas had a higher prevalence than those from urban areas .
Multiple studies were conducted among village residents in high HCV prevalence areas (Table 2). The overall prevalence in rural areas averaged about 20%, higher than the national average. A study conducted in Kalama, a village in the Nile Delta, reported HCV prevalence of 40% among village residents . Similar to blood donor studies, village residents were shown to have a higher prevalence among males compared to females [62, 81], and a marked growth in prevalence with age [56, 58, 59]. A study conducted in 1997, among 3,993 residents of a village in the Nile Delta region, observed prevalence rates in children, ages 0–19, ranging between 7 and 9.9%. This rate increased to 27.6% in those 20–39 years and more than doubled to 56.7% among village residents greater than 40 years of age .
High HCV prevalence was also observed among pregnant women and children in Egypt. Recent studies conducted among pregnant women reported a prevalence of about 8% in Assuit  and Benha , and as high as 15.8% in rural villages of the Nile Delta . Studies conducted among rural school children reported an average prevalence of about 7% [53, 66, 68, 69], while the average prevalence in children attending outpatient clinics was found to be approximately 4% [18, 19, 21, 22]. High prevalence was also observed among select subgroups such as tourism workers , army recruits [53, 79] and fire brigade personnel .
Figure 2A depicts the range of prevalence within each subgroup in studies conducted pre- and post-2001. Among blood donors, studies appear to cluster at lower HCV prevalence levels post- 2001 infection control programs, compared to pre-2001. However, no distinct pattern can be observed within each of the other subgroups.
Prevalence of HCV among populations at direct or high risk of exposure
We classified populations at direct or high risk of HCV exposure into six subcategories: viral hepatitis patients, multi-transfused patients, thalassemia patients, schistosmiasis patients, patients on hemodialysis and IDUs. Table 3 lists all the studies in each sub-category and the reported prevalence measures.
Among patients diagnosed with acute viral hepatitis, HCV prevalence ranged from as low as 4.3%  to as high as 78.7% . Once more, we observed a higher prevalence among studies conducted in rural populations versus urban populations. A recent study conducted in 2010 reported an HCV prevalence of 8.7% among children with viral hepatitis .
The majority of studies in multi-transfused and thalassemia patients were conducted among children. High HCV prevalence rates were observed with averages of about 42% among multi-transfused children and about 58% among children with thalassemia. Multiple studies were also conducted among hemodialysis patients (mostly adults). Very high HCV prevalence was found in both adult populations and children on hemodialysis.
There were six studies that investigated HCV prevalence among schistosomiasis patients. Of these, only two explicitly mentioned previous PAT exposure. However, from the studies context, and given the high HCV prevalence across all of these studies, exposure to previous PAT campaigns seems to be implicitly assumed. Accordingly, we chose to classify these six studies in one subgroup: schistosomiasis patients, and not separate them into two categories based on previous PAT exposure.
Overall, the average HCV prevalence among schistosomiasis patients was about 38%. A recent study by Sabah et al. reported a prevalence of 84.0% among schistosomiasis patients treated with PAT 20 to 30 years ago, and a prevalence of 7.7% among schistosomiasis patients treated orally up to 8 years ago .
Figure 2B depicts the range of prevalence within each subgroup in studies conducted pre and post-2001. No distinct pattern can be discerned in the distribution of HCV prevalence pre- and post-2001 within each of the different subgroups.
Prevalence of HCV among populations at indirect or intermediate risk of exposure
Populations at indirect or intermediate risk of exposure to HCV were classified into the following subcategories: diabetic patients, hospital outpatient attendees, hospitalized populations, household contacts of index cases (HCV positive cases), sexually transmitted infection (STI) patients, periodontal disease patients, prisoners, and populations working in select professions. Details are shown in Table S2, see Additional file 1.
Considerable HCV prevalence was reported among diabetic children in Egypt compared to other countries. A recent study conducted in 2010, among 692 diabetic children with an average age of 10.4 years, reported a prevalence of 2.5% . Previous studies conducted among diabetic children reported much higher levels of 29.4%  and 44.1% . In contrast, HCV prevalence among adult diabetic patients was 20.0%  and 60.3% . Substantial HCV prevalence was also observed among patients attending hospitals, ranging between 0%  and 72.8% . We identified one study conducted among periodontal disease patients reporting a prevalence of 13.0% . Multiple studies were conducted investigating HCV prevalence among the children, spouses, and family contacts of HCV positive cases. Studies conducted among children of index cases usually focused on children of infected mothers to examine the vertical transmission of HCV. HCV RNA prevalence among infants born to HCV positive mothers ranged between 3.8%  and 25.0% . HCV prevalence among spouses of index patients was as high as 35.5% . In a study of family contacts of index patients, the prevalence was 5.7% .
Six studies were conducted among populations in select HCV-relevant professions (Table S2 of Additional file 1). HCV prevalence among health care workers averaged about 17%, whereas among barbers it was 12.3% . We were able to identify only one study among prisoners which reported a prevalence of 31.4% .
The range of HCV prevalence within each subgroup in studies conducted pre- and post-2001 can be observed in Figure 3A. No distinct pattern can be discerned in the distribution of HCV prevalence pre- and post-2001 within each of the different subgroups.
Prevalence of HCV among special clinical populations
A large fraction of studies were conducted among different clinical populations (Table S3 of Additional file 1). Overall, HCV prevalence was very high across all special clinical population groups. The average HCV prevalence among non-Hodgkin’s lymphoma (NHL) patients was roughly 41%, while among orthopedic patients it was about 39%. HCV prevalence among hepatocellular carcinoma (HCC) cases ranged between 61.0% and 90.3%, with a higher prevalence observed among rural versus urban populations . Three studies were conducted among pediatric cancer patients [81, 118, 119]. HCV prevalence among children with leukemia was 19.0% . HCV prevalence among patients with pediatric malignancies who had just ended chemotherapy was 39.6% . More recently, Sharaf-Eldeen et al. reported HCV prevalence of 43.0% among children with malignant cancers .
No distinct pattern can be discerned in the distribution of HCV prevalence pre- and post-2001 within each of the different special clinical population subgroups (Figure 3B).
Measures of RNA prevalence are included in Tables 2–3, and S2-S3 of Additional file 1. RNA prevalence was high across studies in the different population groups. Higher RNA prevalence was observed among studies conducted among high risk groups and special clinical populations compared to the general population and indirect or intermediate risk groups. Overall, the average RNA prevalence among those HCV-antibody positive was approximately 60%.
Risk factors of HCV
Increasing age, a history of PAT, and residing in rural areas were by far the most common risk factors or associations with HCV infection across studies [26, 62]. Other common risk factors were related to healthcare settings such as history of blood transfusions, invasive procedures, injections, perinatal care, and dental work [15, 61, 62, 69, 71, 82, 87]. Saleh et al. reported a greater risk for incident infection among women whose babies were delivered by a physician rather than by a nurse or a traditional birth attendant, in a health facility rather than at their home, and in women having complicated vaginal deliveries . Among children, incident infection was associated with hospitalization and low birth weight . Community and informal health provider related exposures such as circumcision, cautery, and injections were also associated with HCV infection [62, 82, 120]. A number of studies have also suggested intrafamilial transmission though the exact exposures responsible are not clear [14, 121].
Time trend analysis
General population model
Twenty six of the 87 general population studies had the year of data collection missing. The results of our paired t-test identified a mean difference of 3.1 years (95% CI: 2.6 to 3.6) between the year of publication and the year of data collection, for studies with both values present. We applied this time lag to estimate the year of data collection for studies missing this value.
In the univariate linear regression analyses for each subgroup separately, blood donors were the only subgroup showing a statistically significant change in HCV prevalence over time (p-value of 0.001). Table S4, see Additional file 1, reports the results of the univariate analyses.
In the multivariate linear regression analysis for the combined general population subgroups, there was no evidence of a statistically significant decline in HCV prevalence over time (p-value of 0.215). HCV prevalence in the general population changed at a rate of −0.24% per year (95% CI: -0.63 to 0.14). Figure 4 displays the trend in HCV prevalence with time in each of the eight general population subgroups.
Direct or high risk population model
Twenty five of the 46 direct or high risk population studies had the year of data collection missing. The results of the paired t-test identified a mean difference of 3.3 years (95% CI: 4.0 to 2.6) between the year of publication and the year of data collection. We applied this time lag to estimate the year of data collection for studies missing this value.
As was the case for the general population univariate and multivariate analyses, there was no evidence of a statistically significant decline in HCV prevalence over time for each high risk population subgroup (results not shown) and in the high risk population as a whole (p-value of 0.426). HCV prevalence in the high risk population declined at a rate of −0.38% per year (95% CI: -1.35 to 0.58). Figure S5, of Additional file 1, displays the trend in HCV prevalence with time in each of the five high risk subgroups. IDUs were excluded from this figure as there was only one observation.
We have systematically reviewed HCV infection prevalence and incidence across the different population groups in Egypt. The results of our study indicate that Egypt is enduring a large HCV disease burden, and is likely to be the most affected nation worldwide by this infection. HCV prevalence and incidence across the diverse population groups were found to be much higher than those in other countries around the globe [3, 122, 123]. This makes HCV and its complications one of the leading public health problems that Egypt has to confront today.
The results of this synthesis indicate that Egypt has endured a large HCV epidemic at the national level, and that there is substantial endemic HCV transmission in this country. HCV prevalence is at high levels across essentially all population groups, demonstrating the expansive nature of this epidemic, and that it is not isolated to specific population groups or geographic areas.
Despite being a major driver of HCV incidence and prevalence in many countries , the relative contribution of IDUs to HCV incidence and prevalence in Egypt is much smaller than that in other countries. This is because of the specific context of HCV in Egypt, where HCV transmission is associated with medical exposures in the context of a general population HCV epidemic. Still, there is a contribution from injecting drug use to HCV transmission that is, in terms of absolute scale, comparable to other countries. The prevalence of injecting drug use in Egypt is estimated to be 0.21% , and according to the only study we found, HCV prevalence among IDUs is 63% . Considering that HCV prevalence in the population is 14.7% , injecting drug use may explain at most only about 1% of the national HCV prevalence in Egypt.
It is widely believed that the PAT campaigns to control schistosomiasis are the major drivers of the HCV epidemic in Egypt . During the early twentieth century, schistosomiasis was highly prevalent in Egypt, especially in rural areas . From the 1950s to the early 1980s, the Egyptian Ministry of Health led large-scale campaigns to control the disease . Millions of people were treated with intravenous injections of tartar emetic, before an oral drug replaced this standard of care across the country in the 1980s . Reuse of glass syringes and lax sterilization practices during PAT campaigns appear to have caused widespread infection with HCV, which by the 1990s, had replaced schistosomiasis as the primary cause of liver disease in Egypt [6, 126].
Our study supports a major role for the PAT campaigns in driving HCV incidence. Different studies have shown a dramatic increase in HCV prevalence with age; a cohort effect that may be explained, at least in part, by the early association between PAT and HCV transmission [26, 60–62, 82, 127]. Our results also highlight gender and geographical differences in HCV prevalence [36, 64, 71, 75, 128, 129], with higher prevalence observed in males and rural dwellers compared to females and individuals living in urban areas. These differences may also be in part attributed to the PAT campaigns, as rural areas and males were more affected by the schistosomiasis disease burden and hence were main targets of these campaigns .
However, the totality of the evidence synthesized here suggests that the PAT campaigns are one driver among others of HCV transmission in Egypt, and that substantial HCV transmission is still ongoing. High HCV prevalence is found among hospitalized and the special clinical populations; populations that have experienced various facility-based medical procedures. Elevated HCV prevalence is also found among individuals exposed to even minor medical care procedures, within and beyond established health care facilities. Community studies have found strong correlations between HCV infection and different medical exposures such as injections, blood transfusions, surgical procedures, perinatal care, and dental treatment [15, 61, 62, 69, 71, 82, 87].
HCV prevalence among children, in particular, highlights the ongoing transmission of HCV in Egypt. Not only were these children born well after the end of the PAT campaigns, but also a large fraction of them were born after the implementation of the more stringent infection control measures in the country. Nevertheless, considerable prevalence levels are found among children in multiple studies. These studies suggest that children have been exposed to HCV vertically through mother-to-child transmission [24, 25, 27–29] (high RNA prevalence was documented among infants of HCV positive mothers, ranging between 3.8% and 11.1% [24, 25, 27–29, 130, 131]), or horizontally possibly through household exposures [14, 114, 115, 121, 131]. Medical exposures to HCV at a very young age have been also indicated [19, 22, 110, 132]. High HCV levels were reported among thalassemic children [19, 96, 133], children on hemodialysis [22, 132] and diabetic children [19, 22, 110].
HCV prevalence among the mothers of infected children, who tend to be young themselves, has been also associated with medical exposures and/or household exposures [24, 25, 27, 28]. Injecting drug use is unlikely to contribute much to HCV prevalence among these mothers, given the context of the HCV epidemic in Egypt. Moreover, injecting drug use among women in the Middle East and North Africa region is believed to be marginal with only about 10% or less of IDUs being females in this region [134–136].
Results of our time trend analysis suggest that, contrary to expectations, there appears to be a small decline, though statistically not significant, in HCV prevalence over time in the general population and high risk population in Egypt. In the univariate subgroup-specific analyses, only blood donors have shown a statistically significant decline in HCV prevalence. However, this decline is difficult to interpret since recruitment of blood donors changed over time, particularly by excluding HCV positive individuals. While it can take a long time for the prevalence of HCV to decline after the PAT exposures, this fact may not be sufficient to explain the lack of tangible decline. Egypt’s population has almost doubled in the past two to three decades since the epidemic was first discovered, and well after the end of the PAT campaigns. The large influx of uninfected birth cohorts does not appear to have reduced HCV prevalence, possibly suggesting that HCV incidence has not declined as expected following the end of the PAT campaigns and adoption of more stringent infection control measures.
Another potential explanation for the lack of substantial decline in incidence is the very high baseline HCV prevalence in the country. For a given mode of transmission, such as reuse of unclean needles or syringes, the transmission risk is dependent on the probability that the needle/syringe was used previously on an HCV infected person, which is HCV RNA prevalence. Even if the prevalence of the modes of transmissions in Egypt today is similar to other neighboring countries, the high background prevalence can drive much more incidence. In neighboring Libya for example, with an HCV RNA prevalence of less than 1% [134, 137], a reuse of an unclean needle is more than ten-fold less likely to lead to an HCV transmission than in Egypt where HCV RNA prevalence is 9.8% .
Our study identified the lack of an empirical nationally-representative incidence study. It is a priority to document current HCV incidence rate in the population, which continues to be the most critical open question in HCV epidemiology in Egypt today, and is subject to much debate [127, 138]. A recent mathematical modeling study, based on the EDHS data, estimated that the average HCV incidence rate over the lifetime of the living Egyptian population cohort to be 6.9 per 1,000 person-year . This estimate however does not capture the temporal trend in HCV incidence rate and may not be representative of the current level of HCV transmission. A recent study suggested that current HCV incidence rate is about 2.0 per 1000 person-year .
While the evidence for an epidemic at the national level is overwhelming, some of the potential drivers of this epidemic, such as the PAT campaigns and contaminated blood, are no longer present. Therefore, it seems plausible that HCV incidence rate has declined drastically in the last two decades since the discovery of the epidemic in 1991–1992 [30, 139], as Breban et al. have recently suggested through their incidence estimate . Nevertheless, our study could not identify a signature for a major reduction in incidence, and the totality of evidence points towards substantial ongoing HCV transmission, though the precise scale of which is not yet known.
In terms of limitations, there was an element of subjectivity in classifying different studies into different population subgroups. For example, studies conducted in rural children were classified under children even though they fall into two subgroups: rural populations and children. Furthermore, there was variability in the diagnostic assays used across the studies. Earlier studies typically reported the use of 1st and 2nd generation ELISA tests, which lack the sensitivity and specificity of the 3rd generation ELISA tests. Such variability in assays may impact the representativeness of the reported prevalence measures. There was also considerable variability in methodology and quality among the studies assessed. Most of the studies identified were cross-sectional or case–control in study design. Sample size varied widely across studies. The sampling was most often convenience sampling, though several studies have used probability-based samples [1, 61, 69], most notably the EDHS conducted in 2008 . For a fraction of the studies the year of data collection was not available but was estimated using the year of publication, this may affect the time trend analysis. Given that only statistically significant risk factors were extracted, this may have introduced a positive-association selection bias in our reporting of risk factors.
Our study highlights that Egypt is confronted with an HCV disease burden of historical proportions. An HCV epidemic at the national level must have occurred with substantial transmission still ongoing today. As opposed to other countries where HCV dynamics is focused in specific high risk groups, such as IDUs, HCV transmission in Egypt has reached diverse population groups including those not conventionally identified to be at risk of infection. HCV transmission appears to be focused in formal and informal health care settings, though transmission may be occurring in the community and at the household level, but through poorly-identified exposures.
HCV prevention in Egypt must be a national priority. Policymakers and public health and medical care stakeholders need to introduce and implement further prevention measures targeting the iatrogenic transmission routes, such as very stringent infection control practices. Scientific research needs to be expanded to measure current HCV incidence rate and to identify precisely the modes of HCV transmission in medical care, community, and household settings. Such studies will pave the way for effective prevention interventions that can be developed, experimentally tested, and implemented. It is also essential to develop cost-effective strategies for treatment and case management of the large pool of 5–7 million chronically infected persons with HCV in Egypt.
Hepatitis C virus
Egyptian demographic health survey
Parenteral antischistosomiasis therapy
Injecting drugs use
Sexually transmitted infection
Kidney transplant patient
Chronic liver disease
- Rheumatic HD:
Rheumatic heart disease
Chronic renal failure
Systemic lupus erythematosus
El-Zanaty F, Way A: Egypt Demographic and Health Survey 2008. Egyptian: Ministry of Health. 2009, Cairo: El-Zanaty and Associates, and Macro International
Lavanchy D: Evolving epidemiology of hepatitis C virus. Clin Microbiol Infect. 2011, 17 (2): 107-115. 10.1111/j.1469-0691.2010.03432.x.
Alter MJ: Epidemiology of hepatitis C virus infection. World J Gastroenterol. 2007, 13 (17): 2436-2441.
Shepard CW, Finelli L, Alter MJ: Global epidemiology of hepatitis C virus infection. Lancet Infect Dis. 2005, 5 (9): 558-567. 10.1016/S1473-3099(05)70216-4.
Frank C, Mohamed MK, Strickland GT, Lavanchy D, Arthur RR, Magder LS, El Khoby T, Abdel-Wahab Y, Aly Ohn ES, Anwar W, et al: The role of parenteral antischistosomal therapy in the spread of hepatitis C virus in Egypt. Lancet. 2000, 355 (9207): 887-891. 10.1016/S0140-6736(99)06527-7.
Strickland GT: Liver disease in Egypt: hepatitis C superseded schistosomiasis as a result of iatrogenic and biological factors. Hepatology. 2006, 43 (5): 915-922. 10.1002/hep.21173.
Miller FD, Abu-Raddad LJ: Evidence of intense ongoing endemic transmission of hepatitis C virus in Egypt. Proc Natl Acad Sci USA. 2010, 107 (33): 14757-14762. 10.1073/pnas.1008877107.
Moher D, Liberati A, Tetzlaff J, Altman DG, The PG: Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Med. 2009, 6 (7): e1000097-10.1371/journal.pmed.1000097.
Talaat M, Kandeel A, Rasslan O, Hajjeh R, Hallaj Z, El-Sayed N, Mahoney FJ: Evolution of infection control in Egypt: Achievements and challenges. Am J Infect Control. 2006, 34 (4): 193-200. 10.1016/j.ajic.2005.05.028.
Halim AB, Mansour O, Salman T, el-Ahmady O: Incidence of hepatitis C virus in Egyptians. J Hepatol. 1994, 21 (4): 687-
Elkareh S: HCv screening of donors in Governmental Blood Transfusion Centers at Menoufia Governorate (from Jan. 2008 to Oct. 2008). Vox Sang. 2009, 96: 89-90.
Eita N: Prevalence of HCV and HBV infections among blood donors in Dakahilia, Egypt. Vox Sang. 2009, 96: 106-107.
Rushdy O, Moftah F, Zakareya S: Trasmitted transfused viral infections among blood donors during years 2006 and 2007 in suez canal area, Egypt. Vox Sang. 2009, 96: 86-87.
Mohamed MK, Abdel-Hamid M, Mikhail NN, Abdel-Aziz F, Medhat A, Magder LS, Fix AD, Strickland GT: Intrafamilial transmission of hepatitis C in Egypt. Hepatology. 2005, 42 (3): 683-687. 10.1002/hep.20811.
Saleh DA, Shebl F, Abdel-Hamid M, Narooz S, Mikhail N, El-Batanony M, El-Kafrawy S, El-Daly M, Sharaf S, Hashem M, et al: Incidence and risk factors for hepatitis C infection in a cohort of women in rural Egypt. Trans R Soc Trop Med Hyg. 2008, 102 (9): 921-928. 10.1016/j.trstmh.2008.04.011.
Mostafa A, Taylor SM, El-Daly M, El Hoseiny M, Bakr I, Arafa N, Thiers V, Rimlinger F, Abdel-Hamid M, Fontanet A, et al: Is the hepatitis C virus epidemic over in Egypt? Incidence and risk factors of new hepatitis C virus infections. Liver Int. 2010, 30 (4): 560-566. 10.1111/j.1478-3231.2009.02204.x.
Saleh DA, Shebl FM, El-Kamary SS, Magder LS, Allam A, Abdel-Hamid M, Mikhail N, Hashem M, Sharaf S, Stoszek SK, et al: Incidence and risk factors for community-acquired hepatitis C infection from birth to 5 years of age in rural Egyptian children. Trans R Soc Trop Med Hyg. 2010, 104 (5): 357-363. 10.1016/j.trstmh.2010.01.009.
Khalifa AS, Mitchell BS, Watts DM, El-Samahy MH, El-Sayed MH, Hassan NF, Jennings GB, Hibbs RG, Corwin AL: Prevalence of hepatitis C viral antibody in transfused and nontransfused Egyptian children. Am J Trop Med Hyg. 1993, 49 (3): 316-321.
Soliman AT, Amer AE, Demian RS, el-Nanawy AA, el Azzouni OF: Prevalence of hepatitis-C antibody seropositivity in healthy Egyptian children and four high risk groups. J Trop Pediatr. 1995, 41 (6): 341-343. 10.1093/tropej/41.6.341.
Miras A, Morris K, Soper C: Hepatitis C virus prevalence in children in a highly endemic region of Egypt. Pediatr Infect Dis J. 2002, 21 (10): 987-
El-Raziky MS, El-Hawary M, Esmat G, Abouzied AM, El-Koofy N, Mohsen N, Mansour S, Shaheen A, Abdel Hamid M, El-Karaksy H: Prevalence and risk factors of asymptomatic hepatitis C virus infection in Egyptian children. World J Gastroenterol. 2007, 13 (12): 1828-1832.
Kandil ME, Rasheed MA, Saad NE: Hepatitis C and B viruses among some high risk groups of Egyptian children. J Med Sci. 2007, 7 (8): 1259-1267.
Hassan NF, Kotkat A: Prevalence of antibodies to hepatitis C virus in pregnant women in Egypt. J Infect Dis. 1993, 168 (1): 248-249. 10.1093/infdis/168.1.248.
Agha S, Sherif LS, Allam MA, Fawzy M: Transplacental transmission of hepatitis C virus in HIV-negative mothers. Res Virol. 1998, 149 (4): 229-234. 10.1016/S0923-2516(98)80004-6.
Kassem AS, El-Nawawy AA, Massoud MN, Abou El-Nazar SY, Sobhi EM: Prevalence of hepatitis C virus (HCV) infection and its vertical transmission in Egyptian pregnant women and their newborns. J Trop Pediatr. 2000, 46 (4): 231-233. 10.1093/tropej/46.4.231.
Stoszek SK, Abdel-Hamid M, Narooz S, El Daly M, Saleh DA, Mikhail N, Kassem E, Hawash Y, El Kafrawy S, Said A, et al: Prevalence of and risk factors for hepatitis C in rural pregnant Egyptian women. Trans R Soc Trop Med Hyg. 2006, 100 (2): 102-107. 10.1016/j.trstmh.2005.05.021.
Zahran KM, Badary MS, Agban MN, Abdel Aziz NH: Pattern of hepatitis virus infection among pregnant women and their newborns at the Women’s Health Center of Assiut University, Upper Egypt. Int J Gynaecol Obstet. 2010, 111 (2): 171-174. 10.1016/j.ijgo.2010.06.013.
AbdulQawi K, Youssef A, Metwally MA, Ragih I, AbdulHamid M, Shaheen A: Prospective study of prevalence and risk factors for hepatitis C in pregnant Egyptian women and its transmission to their infants. Croat Med J. 2010, 51 (3): 219-228. 10.3325/cmj.2010.51.219.
Abo Elmagd EK, Abdel-Wahab KS, Alrasheedy ZE, Khalifa AS: An Egyptian study of mother to child transmission of hepatitis C virus. Int J Virology. 2011, 7 (3): 100-108. 10.3923/ijv.2011.100.108.
Kamel MA, Ghaffar YA, Wasef MA, Wright M, Clark LC, Miller FD: High HCV prevalence in Egyptian blood donors. Lancet. 1992, 340 (8816): 427-
Selim O, Rafik M, el-Zayadi A: Prevalence of hepatitis C virus among non-A, non-B-related chronic liver disease in Egypt. J Hepatol. 1992, 14 (2–3): 416-417.
Darwish NM, Abbas MO, Abdelfattah FM, Darwish MA: Hepatitis C virus infection in blood donors in Egypt. J Egypt Public Health Assoc. 1992, 67 (3–4): 223-236.
Darwish MA, Raouf TA, Rushdy P, Constantine NT, Rao MR, Edelman R: Risk factors associated with a high seroprevalence of hepatitis C virus infection in Egyptian blood donors. Am J Trop Med Hyg. 1993, 49 (4): 440-447.
Quinti I, Renganathan E, El Ghazzawi E, Divizia M, Sawaf G, Awad S, Pana A, Rocchi G: Seroprevalence of HIV and HCV infections in Alexandria, Egypt. Zentralblatt fur Bakteriologie: international journal of medical microbiology. 1995, 283 (2): 239-244. 10.1016/S0934-8840(11)80205-7.
Bassily S, Hyams KC, Fouad RA, Samaan MD, Hibbs RG: A high risk of hepatitis C infection among Egyptian blood donors: the role of parenteral drug abuse. Am J Trop Med Hyg. 1995, 52 (6): 503-505.
Khattab MA, Eslam M, Sharwae MA, Hamdy L: Seroprevalence of hepatitis C and B among blood donors in Egypt: Minya Governorate, 2000–2008. Am J Infect Control. 2010, 38 (8): 640-641. 10.1016/j.ajic.2009.12.016.
Attia MAM, Zekri ARN, Goudsmit J, Boom R, Khaled HM, Mansour MT, De Wolf F, Alam El-Din HM, Sol CJA: Diverse patterns of recognition of hepatitis C virus core and nonstructural antigens by antibodies present in Egyptian cancer patients and blood donors. J Clin Microbiol. 1996, 34 (11): 2665-2669.
Arthur RR, Hassan NF, Abdallah MY, El-Sharkawy MS, Saad MD, Hackbart BG, Imam IZ: Hepatitis C antibody prevalence in blood donors in different governorates in Egypt. Trans R Soc Trop Med Hyg. 1997, 91 (3): 271-274. 10.1016/S0035-9203(97)90070-5.
Selim O, Ibrahim EH, Hamdy H, Dabbous H, Ahdy A, Moneim SA, el-Zayadi AR: Does schistosomiasis play a role in the high sero prevalence of HCV antibody among Egyptians?. Trop Gastroenterol. 1997, 18 (3): 98-100.
Gad A, Tanaka E, Orii K, Rokuhara A, Nooman Z, Serwah AH, Shoair M, Yoshizawa K, Kiyosawa K: Relationship between hepatitis C virus infection and schistosomal liver disease: not simply an additive effect. J Gastroenterol. 2001, 36 (11): 753-758. 10.1007/s005350170017.
Tanaka Y, Agha S, Saudy N, Kurbanov F, Orito E, Kato T, Abo-Zeid M, Khalaf M, Miyakawa Y, Mizokami M: Exponential spread of hepatitis C virus genotype 4a in Egypt. J Mol Evol. 2004, 58 (2): 191-195. 10.1007/s00239-003-2541-3.
Hashish MH, El-Barrawy MA, Mahmoud OA, Abdel Rahman NW: TT virus among blood donors in Alexandria. J Egypt Public Health Assoc. 2005, 80 (5–6): 651-664.
El-Gilany AH, El-Fedawy S: Bloodborne infections among student voluntary blood donors in Mansoura University, Egypt. East Mediterr Health J. 2006, 12 (6): 742-748.
Agha S, El-Mashad N, El-Malky M, El-Shony H, El-Sherif MZ, El-Hasan MA, Tanaka Y, Mizokami M: Prevalence of low positive anti-HCV antibodies in blood donors: Schistosoma mansoni co-infection and possible role of autoantibodies. Microbiol Immunol. 2006, 50 (6): 447-452.
El Damaty SI, Hassan SK, Mohamed MK, El Hosini M, Rekacewicz C, Fontanet A: Surveillance system for HCV infection: testing a model based on blood banks. J Egypt Public Health Assoc. 2007, 82 (5–6): 451-471.
El-Zayadi AR, Ibrahim EH, Badran HM, Saeid A, Moneib NA, Shemis MA, Abdel-Sattar RM, Ahmady AM, El-Nakeeb A: Anti-HBc screening in Egyptian blood donors reduces the risk of hepatitis B virus transmission. Transfus Med. 2008, 18 (1): 55-61. 10.1111/j.1365-3148.2007.00806.x.
Ismail AM, Ziada HN, Sheashaa HA, Shehab El-Din AB: Decline of viral hepatitis prevalence among asymptomatic Egyptian blood donors: a glimmer of hope. Eur J Intern Med. 2009, 20 (5): 490-493. 10.1016/j.ejim.2009.03.005.
Ashour D, Moftah F, Gobran H, Ekram D: Decreasing the risk of transfusion transmitted infections (TTIS) in the Egyptian Blood Transfusion Services. Vox Sang. 2009, 96: 103-104.
Radwan D, Moftah F, Goubran H, Mosa M, Ibrahem G: Over all representation of NAT results and correlation of NAT negativity with seropositive blood donors. Vox Sang. 2010, 99: 87-
Wasfi OA, Sadek NA: Prevalence of hepatitis B surface antigen and hepatitis C virus antibodies among blood donors in Alexandria, Egypt. East Mediterr Health J. 2011, 17 (3): 238-242.
Awadalla HI, Ragab MH, Nassar NA, Osman MAH: Risk factors of hepatitis C infection among Egyptian blood donors. Cent Eur J Public Health. 2011, 19 (4): 217-221.
Farawela H, Khorshied M, Shaheen I, Gouda H, Nasef A, Abulata N, Mahmoud HA, Zawam HM, Mousa SM: The association between hepatitis C virus infection, genetic polymorphisms of oxidative stress genes and B-cell non-Hodgkin’s lymphoma risk in Egypt. Infect Genet Evol. 2012, 12 (6): 1189-1194. 10.1016/j.meegid.2012.04.007.
Abdel-Wahab MF, Zakaria S, Kamel M, Abdel-Khaliq MK, Mabrouk MA, Salama H, Esmat G, Thomas DL, Strickland GT: High seroprevalence of hepatitis C infection among risk groups in Egypt. Am J Trop Med Hyg. 1994, 51 (5): 563-567.
Kamel MA, Miller FD, el Masry AG, Zakaria S, Khattab M, Essmat G, Ghaffar YA: The epidemiology of Schistosoma mansoni, hepatitis B and hepatitis C infection in Egypt. Ann Trop Med Parasitol. 1994, 88 (5): 501-509.
Darwish NM, Abbas MO, Hady SI, Mohammed TA: Study of the high prevalence of HCV in Egypt. J Egypt Public Health Assoc. 1995, 70 (3–4): 397-414.
Darwish MA, Faris R, Clemens JD, Rao MR, Edelman R: High seroprevalence of hepatitis A, B, C, and E viruses in residents in an Egyptian village in the Nile delta: A pilot study. Am J Trop Med Hyg. 1996, 54 (6): 554-558.
Abaza SM, Mehanna S, Winch PJ, el-Sayed HF: The prevalence of hepatitis B and C infections among immigrants to a newly reclaimed area endemic for Schistosoma mansoni in Sinai, Egypt. Acta Trop. 1997, 68 (2): 229-237. 10.1016/S0001-706X(97)00097-1.
Nafeh MA, Medhat A, Shehata M, Mikhail NNH, Swifee Y, Abdel-Hamid M, Watts S, Fix AD, Strickland GT, Anwar W, et al: Hepatitis C in a community in upper Egypt: I. Cross-sectional survey. Am J Trop Med Hyg. 2000, 63 (5–6): 236-241.
Abdel-Aziz F, Habib M, Mohamed MK, Abdel-Hamid M, Gamil F, Madkour S, Mikhail NN, Thomas D, Fix AD, Strickland GT, et al: Hepatitis C virus (HCV) infection in a community in the Nile Delta: Population description and HCV prevalence. Hepatology. 2000, 32 (1): 111-115. 10.1053/jhep.2000.8438.
Darwish MA, Faris R, Darwish N, Shouman A, Gadallah M, El-Sharkawy MS, Edelman R, Grumbach K, Rao MR, Clemens JD: Hepatitis C and cirrhotic liver disease in the Nile delta of Egypt: A community-based study. Am J Trop Med Hyg. 2001, 64 (3–4): 147-153.
Ragab H, Mangoud AM, Eissa MH, Afefy AF, Ibrahem IA, Mahrous S, el-Sadawy M, et al: Hepatitis C virus infection at Sharkia Governorate, Egypt: seroprevalence and associated risk factors. J Egypt Soc Parasitol. 2004, 34 (1): 367-384.
Arafa N, El Hoseiny M, Rekacewicz C, Bakr I, El-Kafrawy S, El Daly M, Aoun S, Marzouk D, Mohamed MK, Fontanet A: Changing pattern of hepatitis C virus spread in rural areas of Egypt. J Hepatol. 2005, 43 (3): 418-424. 10.1016/j.jhep.2005.03.021.
Mohamed MK, Bakr I, El-Hoseiny M, Arafa N, Hassan A, Ismail S, Anwar M, Attala M, Rekacewicz C, Zalata K, et al: HCV-related morbidity in a rural community of Egypt. J Med Virol. 2006, 78 (9): 1185-1189. 10.1002/jmv.20679.
Eassa S, Eissa M, Sharaf SM, Ibrahim MH, Hassanein OM: Prevalence of hepatitis C virus infection and evaluation of a health education program in el-ghar village in zagazig, egypt. J Egypt Public Health Assoc. 2007, 82 (5–6): 379-404.
Aguilar CE, Soliman AS, McConnell DS, Zekri AR, Banerjee M, Omar A, Sharawy M, Omar S, Raouf A, Sowers MR: Androgen profiles among Egyptian adults considering liver status. J Gastroenterol Hepatol. 2008, 23 (7 Pt 2): e137-e145.
El-Sherbini A, Hassan W, Abdel-Hamid M, Naeim A: Natural history of hepatitis C virus among apparently normal schoolchildren: Follow-up after 7 years. J Trop Pediatr. 2003, 49 (6): 384-385. 10.1093/tropej/49.6.384.
Mohamed MK, Magder LS, Abdel-Hamid M, El-Daly M, Mikhail NN, Abdel-Aziz F, Medhat A, Thiers V, Strickland GT: Transmission of hepatitis C virus between parents and children. Am J Trop Med Hyg. 2006, 75 (1): 16-20.
El Sherbini A, Mohsen SA, Hasan W, Mostafa S, El Gohary K, Moneib A, Abaza AH: The peak impact of an Egyptain outbreak of hepatitis C virus: Has it passed or has not yet occurred?. Liver Int. 2007, 27 (6): 876-877. 10.1111/j.1478-3231.2007.01501.x.
Barakat SH, El-Bashir N: Hepatitis C virus infection among healthy Egyptian children: Prevalence and risk factors. J Viral Hepat. 2011, 18 (11): 779-784. 10.1111/j.1365-2893.2010.01381.x.
El-Sayed NM, Gomatos PJ, Rodier GR, Wierzba TF, Darwish A, Khashaba S, Arthur RR: Seroprevalence survey of Egyptian tourism workers for hepatitis B virus, hepatitis C virus, human immunodeficiency virus, and Treponema pallidum infections: Association of hepatitis C virus infections with specific regions of Egypt. Am J Trop Med Hyg. 1996, 55 (2): 179-184.
Mohamed MK, Hussein MH, Massoud AA, Rakhaa MM, Shoeir S, Aoun AA, Aboul Naser M: Study of the risk factors for viral hepatitis C infection among Egyptians applying for work abroad. J Egypt Public Health Assoc. 1996, 71 (1–2): 113-147.
Gohar SA, Khalil RY, Elaish NM, Khedr EM, Ahmed MS: Prevalence of antibodies to hepatitis C virus in hemodialysis patients and renal transplant recipients. J Egypt Public Health Assoc. 1995, 70 (5–6): 465-484.
Halim AB, Garry RF, Dash S, Gerber MA: Effect of schistosomiasis and hepatitis on liver disease. Am J Trop Med Hyg. 1999, 60 (6): 915-920.
Hassan MM, Zaghloul AS, El-Serag HB, Soliman O, Patt YZ, Chappell CL, Beasley RP, Hwang LY: The role of hepatitis C in hepatocellular carcinoma: a case control study among Egyptian patients. J Clin Gastroenterol. 2001, 33 (2): 123-126. 10.1097/00004836-200108000-00006.
Strickland GT, Elhefni H, Salman T, Waked I, Abdel-Hamid M, Mikhail NN, Esmat G, Fix A: Role of hepatitis C infection in chronic liver disease in Egypt. Am J Trop Med Hyg. 2002, 67 (4): 436-442.
El-Sayed GM, Mohamed WS, Nouh MA, Moneer MM, El-Mahallawy HA: Viral genomes and antigen detection of hepatitis B and C viruses in involved lymph nodes of Egyptian non-Hodgkin’s lymphoma patients. Egypt J Immunol. 2006, 13 (1): 105-114.
El Bassuoni MA, Obada MA, Korah T, El Sayed S: Assessment of Treg cells CD4 + CD25+ in chronic cirrhotic liver disease and hepatocellular carcinoma Egyptian patients. Hepatitis Monthly. 2008, 8 (3): 173-177.
Salama KM, Selim Oel S: Hepatitis G virus infection in multitransfused Egyptian children. Pediatr Hematol Oncol. 2009, 26 (4): 232-239. 10.1080/08880010902897591.
Farghaly AG, Barakat RM: Prevalence, impact and risk factors of hepatitis C infection. J Egypt Public Health Assoc. 1993, 68 (1–2): 63-79.
Mohamed MK: Epidemiology of HCV in Egypt 2004. The Afro-Arab Liver Journal. 2004, 3 (2): 41-52.
Sharaf-Eldeen S, Salama K, Eldemerdash S, Hassan HMS, Semesem M: Hepatitis B and C Viruses in Egyptian children with malignancy. J Med Sci. 2007, 7 (6): 1003-1008.
Habib M, Mohamed MK, Abdel-Aziz F, Magder LS, Abdel-Hamid M, Gamil F, Madkour S, Mikhail NN, Anwar W, Strickland GT, et al: Hepatitis C virus infection in a community in the Nile Delta: Risk factors for seropositivity. Hepatology. 2001, 33 (1): 248-253. 10.1053/jhep.2001.20797.
El-Gohary A, Hassan A, Uchida T, Shikata T, Nooman Z: Prevalence of hepatitis E virus among acute sporadic hepatitis patients in Suez. Int Hepatol Commun. 1994, 2 (4): 218-222. 10.1016/0928-4346(94)90074-4.
El Gaafary MM, Rekacewicz C, Abdel-Rahman AG, Allam MF, El Hosseiny M, Hamid MA, Colombani F, Sultan Y, El-Aidy S, Fontanet A, et al: Surveillance of acute hepatitis C in Cairo, Egypt. J Med Virol. 2005, 76 (4): 520-525. 10.1002/jmv.20392.
Meky FA, Stoszek SK, Abdel-Hamid M, Selim S, Abdel-Wahab A, Mikhail N, El-Kafrawy S, El-Daly M, Abdel-Aziz F, Sharaf S, et al: Active surveillance for acute viral hepatitis in rural villages in the Nile Delta. Clin Infect Dis. 2006, 42 (5): 628-633. 10.1086/500133.
Zakaria S, Fouad R, Shaker O, Zaki S, Hashem A, El-Kamary SS, Esmat G: Changing patterns of acute viral hepatitis at a major urban referral center in Egypt. Clin Infect Dis. 2007, 44 (4): e30-e36. 10.1086/511074.
Kalil KA, Farghally HS, Hassanein KM, Abd-Elsayed AA, Hassanein FE: Hepatitis C virus infection among paediatric patients attending University of Assiut Hospital, Egypt. Eastern Mediterranean health journal = La revue de sante de la Mediterranee orientale = al-Majallah al-sihhiyah li-sharq al-mutawassit. 2010, 16 (4): 356-361.
Talaat M, El-Sayed N, Kandeel A, Azab MA, Afifi S, Youssef FG, Ismael T, Hajjeh R, Mahoney FJ: Sentinel surveillance for patients with acute hepatitis in Egypt, 2001–04. East Mediterr Health J. 2010, 16 (2): 134-140.
Eldin SS, Seddik I, Daef EA, Shata MT, Raafat M, Abdel Baky L, Nafeh MA: Risk factors and immune response to hepatitis E viral infection among acute hepatitis patients in Assiut, Egypt. Egypt J Immunol. 2010, 17 (1): 73-86.
Badawy AA, Khalil HH: The aetiology of acute viral hepatitis among some Egyptian youth. J Egypt Soc Parasitol. 2012, 42 (1): 203-206.
Said ZN, El-Sayed MH, El-Bishbishi IA, El-Fouhil DF, Abdel-Rheem SE, El-Abedin MZ, Salama II: High prevalence of occult hepatitis B in hepatitis C-infected Egyptian children with haematological disorders and malignancies. Liver Int. 2009, 29 (4): 518-524. 10.1111/j.1478-3231.2009.01975.x.
Tonbary YA, Elashry R, Zaki Mel S: Descriptive epidemiology of hemophilia and other coagulation disorders in mansoura, egypt: retrospective analysis. Mediterranean journal of hematology and infectious diseases. 2010, 2 (3): e2010025-
El-Faramawy AAM, El-Rashidy OF, Tawfik PH, Hussein GH: Transfusion transmitted hepatitis: Where do we stand now? A one center study in upper Egypt. Hepatitis Monthly. 2012, 12 (4): 286-291.
Abdelwahab MS, El-Raziky MS, Kaddah NA, Abou-Elew HH: Prevalence of hepatitis C virus infection and human immunodeficiency virus in a cohort of Egyptian hemophiliac children. Ann Saudi Med. 2012, 32 (2): 200-202.
Khalifa AS, Salem M, Mounir E, El-Tawil MM, El-Sawy M, Abd Al-Aziz MM: Abnormal glucose tolerance in Egyptian beta-thalassemic patients: possible association with genotyping. Pediatr Diabetes. 2004, 5 (3): 126-132. 10.1111/j.1399-543X.2004.00051.x.
Abdalla NM, Galal A, Fatouh AA, Eid K, Salama EEE, Gomma HE: Transfusion transmitted virus (TTV) infection in polytransfused Egyptian thalassemic children. J Med Sci. 2006, 6 (5): 833-837.
Omar N, Salama K, Adolf S, El-Saeed GS, Abdel Ghaffar N, Ezzat N: Major risk of blood transfusion in hemolytic anemia patients. Blood Coagul Fibrinolysis. 2011, 22 (4): 280-284. 10.1097/MBC.0b013e3283451255.
Mansour AK, Aly RM, Abdelrazek SY, Elghannam DM, Abdelaziz SM, Shahine DA, Elmenshawy NM, Darwish AM: Prevalence of HBV and HCV infection among multi-transfused Egyptian thalassemic patients. Hematol Oncol Stem Cell Ther. 2012, 5 (1): 54-59.
Bassily S, Hyams KC, El-Masry NA, Hassan NF, Watts DM: Hepatitis C virus infection and hepatosplenic schistosomiasis . Scand J Infect Dis. 1992, 24 (5): 687-688. 10.3109/00365549209054660.
Zekri ARN, Sedkey L, El-Din HMA, Abdel-Aziz AO, Viazov S: The pattern of transmission transfusion virus infection in Egyptian patients . Int J Infect Dis. 2002, 6 (4): 329-331. 10.1016/S1201-9712(02)90173-6.
El-Sabah AA, El-Metwally MT, Abozinadah NY: Hepatitis C and B virus in schistosomiasis patients on oral or parenteral treatment. J Egypt Soc Parasitol. 2011, 41 (2): 307-314.
Hassan NF: Prevalence of hepatitis C antibodies in patient groups in Egypt. Trans R Soc Trop Med Hyg. 1993, 87 (6): 638-10.1016/0035-9203(93)90270-Z.
Hassan AA, Khalil R: Hepatitis C in dialysis patients in egypt: relationship to dialysis duration, blood transfusion, and liver disease. Saudi J Kidney Dis Transpl. 2000, 11 (1): 72-73.
Shatat HZ, Kotkat AM, Farghaly AG: Immune response to hepatitis B vaccine in haemodialysis patients. J Egypt Public Health Assoc. 2000, 75 (3–4): 257-275.
Gad A, Tanaka E, Orii K, Rokuhara A, Nooman Z, El-Hamid Serwah A, El-Sherif A, El-Essawy M, Yoshizawa K, Kiyosawa K: Clinical significance of TT virus infection in maintenance hemodialysis patients of an endemic area for hepatitis C infection. Hepatology Research. 2002, 22 (1): 13-19. 10.1016/S1386-6346(01)00112-7.
El Yazeed SA NAEL-G, Younes K, El-Ghobary A: Antiphospholipid antibodies in Egyptian patients with chronic renal failure. J Med Sci. 2006, 6 (3): 468-473.
Attia EA, Hassan SI, Youssef NM: Cutaneous disorders in uremic patients on hemodialysis: an Egyptian case-controlled study. Int J Dermatol. 2010, 49 (9): 1024-1030. 10.1111/j.1365-4632.2010.04466.x.
Ibrahim S: Quality of care assessment and adherence to the international guidelines considering dialysis, water treatment, and protection against transmission of infections in university hospital-based dialysis units in Cairo, Egypt. Hemodial Int. 2010, 14 (1): 61-67. 10.1111/j.1542-4758.2009.00398.x.
Drew L, Hamdy L, El-Sherbini E, Sadek Sel D, Saleh E, el-Ghazzawi E: Intravenous drug addicts: a high risk group for infection with human immunodeficiency virus, hepatitis viruses, cytomegalo virus and bacterial infections in Alexandria Egypt. J Egypt Public Health Assoc. 1995, 70 (1–2): 127-150.
El-Karaksy H, Anwar GH, El-Raziky MS, El-Hawary M, Hashem M, El-Sayed R, El-Shabrawi M, Mohsen N, Fouad H, Esmat G: Anti-HCV prevalence among diabetic and non-diabetic Egyptian children. Curr Diabetes Rev. 2010, 6 (6): 388-392. 10.2174/157339910793499137.
Elmagd MM, Bakr MA, Metwally AH, Wahab AM: Clinicoepidemiologic study of posttransplant diabetes after living-donor renal transplant. Exp Clin Transplant. 2008, 6 (1): 42-47.
El-Medany OM: El-Din Abdel Wahab KS, Abu Shady EA, Gad El-Hak N: Chronic liver disease and hepatitis C virus in Egyptian patients. Hepatogastroenterology. 1999, 46 (27): 1895-1903.
Farghaly AG, Mansour GA, Mahdy NH, Yousri A: Hepatitis B and C virus infections among patients with gingivitis and adult periodontitis: seroprevalence and public health importance. J Egypt Public Health Assoc. 1998, 73 (5–6): 707-735.
Morad WS: Transmission of hepatitis C between spouses an epidemiological study at National Liver Institute hospital. Int J Infect Dis. 2011, 15: S81-
El-Zayadi A, Khalifa AA, El-Misiery A, Naser AM, Dabbous H, Aboul-Ezz AA: Evaluation of risk factors for intrafamilial transmission of HCV infection in Egypt. J Egypt Public Health Assoc. 1997, 72 (1–2): 33-51.
Shalaby S, Kabbash IA, El Saleet G, Mansour N, Omar A, El Nawawy A: Hepatitis B and C viral infection: prevalence, knowledge, attitude and practice among barbers and clients in Gharbia governorate, Egypt. East Mediterr Health J. 2010, 16 (1): 10-17.
Ezzat S, Abdel-Hamid M, Abdel-Latif Eissa S, Mokhtar N, Labib AN, El-Ghorory L, Mikhail NN, Abdel-Hamid A, Hifnawy T, Strickland GT, et al: Associations of pesticides, HCV, HBV, and hepatocellular carcinoma in Egypt. Int J Hyg Environ Health. 2005, 208 (5): 329-339. 10.1016/j.ijheh.2005.04.003.
Meir H, Balawi I, Nayel H, El Karaksy H, El Haddad A: Hepatic dysfunction in children with acute lymphoblastic leukemia in remission: Relation to hepatitis infection. Med Pediatr Oncol. 2001, 36 (4): 469-473. 10.1002/mpo.1111.
Mostafa EE A, Mansour T, Amin M, Sidhom I, Khairy A, El Zomor H: Seroprevalence of Hepatitis B and C in Pediatric Malignancies. J Egypt Natl Canc Inst. 2003, 15 (1): 33-42.
Medhat A, Shehata M, Magder LS, Mikhail N, Abdel-Baki L, Nafeh M, Abdel-Hamid M, Strickland GT, Fix AD: Hepatitis c in a community in Upper Egypt: risk factors for infection. Am J Trop Med Hyg. 2002, 66 (5): 633-638.
Plancoulaine S, Mohamed MK, Arafa N, Bakr I, Rekacewicz C, Tregouet DA, Obach D, El Daly M, Thiers V, Feray C, et al: Dissection of familial correlations in hepatitis C virus (HCV) seroprevalence suggests intrafamilial viral transmission and genetic predisposition to infection. Gut. 2008, 57 (9): 1268-1274. 10.1136/gut.2007.140681.
Wasley A, Alter MJ: Epidemiology of hepatitis C: Geographic differences and temporal trends. Semin Liver Dis. 2000, 20 (1): 1-16. 10.1055/s-2000-9506.
Sievert W, Altraif I, Razavi HA, Abdo A, Ahmed EA, Alomair A, Amarapurkar D, Chen CH, Dou X, El Khayat H, et al: A systematic review of hepatitis C virus epidemiology in Asia, Australia and Egypt. Liver Int. 2011, 31 (SUPPL. 2): 61-80.
Aceijas C, Rhodes T: Global estimates of prevalence of HCV infection among injecting drug users. Int J Drug Policy. 2007, 18 (5): 352-358. 10.1016/j.drugpo.2007.04.004.
Aceijas C, Friedman SR, Cooper HLF: Estimates of injecting drug users at the national and local level in developing and transitional countries, and gender and age distribution (vol 82, pg 10, 2006). Sex Transm Infect. 2006, 82 (4): 344-344.
Yahia M: Global health: A uniquely Egyptian epidemic. Nature. 2011, 474 (7350 SUPPL.): S12-S13.
Breban R, Doss W, Esmat G, Elsayed M, Hellard M, Ayscue P, Albert M, Fontanet A, Mohamed M: Towards realistic estimates of HCV incidence in Egypt. J Viral Hepat. 2012, doi:10.1111/j.1365-2893.2012.01650.x.
Waked IA, Saleh SM, Moustafa MS, Raouf AA, Thomas DL, Strickland GT: High prevalence of hepatitis C in Egyptian patients with chronic liver disease. Gut. 1995, 37 (1): 105-107. 10.1136/gut.37.1.105.
Demian AD: Prevalence of anaesthetic co-morbid factors among urological patients in a tertiary referral centre in Egypt. Egyptian J Anaesth. 2004, 20 (3): 325-330.
Madwar MA, El-Gindy I, Fahmy HM, Shoeb NM, Massoud BA: Hepatitis C virus transmission in family members of Egyptian patients with HCV related chronic liver disease. J Egypt Public Health Assoc. 1999, 74 (3–4): 313-332.
Shebl FM, El-Kamary SS, Saleh DA, Abdel-Hamid M, Mikhail N, Allam A, El-Arabi H, Elhenawy I, El-Kafrawy S, El-Daly M, et al: Prospective cohort study of mother-to-infant infection and clearance of hepatitis C in rural Egyptian villages. J Med Virol. 2009, 81 (6): 1024-1031. 10.1002/jmv.21480.
Hammad AM, Zaghloul MH: Hepatitis G virus infection in Egyptian children with chronic renal failure (single centre study). Ann Clin Microbiol Antimicrob. 2009, 8: 36-10.1186/1476-0711-8-36.
El Gohary A, Hassan A, Nooman Z, Lavanchy D, Mayerat C, El Ayat A, Fawaz N, Gobran F, Ahmed M, Kawano F, et al: High prevalence of hepatitis C virus among urban and rural population groups in Egypt. Acta Trop. 1995, 59 (2): 155-161. 10.1016/0001-706X(95)00075-P.
Abu-Raddad L, Akala FA, Semini I, Riedner G, Wilson D, Tawil O: Characterizing the HIV/AIDS epidemic in the Middle East and North Africa: Time for Strategic Action. Middle East and North Africa HIV/AIDS Epidemiology Synthesis Project. World Bank/UNAIDS/WHO Publication. 2010, Washington DC: The World Bank Press
Abu-Raddad LJ, Hilmi N, Mumtaz G, Benkirane M, Akala FA, Riedner G, Tawil O, Wilson D: Epidemiology of HIV infection in the Middle East and North Africa. AIDS. 2010, 24 (Suppl 2): S5-23. 10.1097/01.aids.0000386729.56683.33.
Mumtaz GWH, Thomas S, Riome S, Setayesh H, Riedner G, Semini I, Tawil O, Akala FA, Wilson D, Abu-Raddad L: HIV epidemics are emerging among people who inject drugs in the Middle-East and North Africa: Systematic review and data synthesis. Under review. 2012
Fadlalla FMY, Mumtaz G, Abu-Raddad L: The epidemiology of hepatitis C virus in the Arab Maghreb countries: A systematic review and meta-analysis. Under preparation. 2012
Miller FDA-RL: Quantifying current hepatitis C virus incidence in Egypt. Under review. 2012
Saeed AA, Fairclough D, Bacchus R, Ring C, Garson J, al-Admawi AM, al-Rasheed A: Hepatitis C virus infection in Egyptian volunteer blood donors in Riyadh. Lancet. 1991, 338 (8764): 459-460.
The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2334/13/288/prepub
We are grateful for the Qatar National Research Fund for supporting this work (NPRP 04-924-3-251), and the support provided by the Biostatistics, Epidemiology, and Biomathematics Research Core at the Weill Cornell Medical College in Qatar. The authors are also grateful for the valuable suggestions and comments by the reviewers of this article.
The Qatar National Research Fund (NPRP 04-924-3-251) and the Biostatistics, Epidemiology, and Biomathematics Research Core at the Weill Cornell Medical College- Qatar.
The authors declare that they have no competing interests.
YM and SR conducted the literature review and data retrieval. YM conducted extraction, analysis and wrote the first draft of the paper. GM participated in study design. FDM contributed to the study design and analyses. LJA conceived and led the design of the study, analyses, and drafting of the article. All authors contributed to discussion of the results and writing of the manuscript. All authors read and approved the final manuscript.
Electronic supplementary material
Additional file 1: Table S1: PRISMA Checklist. Table S2. Prevalence of hepatitis C virus among populations at indirect or intermediate risk of exposure in Egypt. Table S3. Prevalence of hepatitis C virus among special clinical populations in Egypt. Table S4. Hepatitis C virus time trend analysis for each general population subgroup. Figure S5. Hepatitis C virus time trend analysis among populations at direct or high risk of exposure. (DOCX 289 KB)
About this article
Cite this article
Mohamoud, Y.A., Mumtaz, G.R., Riome, S. et al. The epidemiology of hepatitis C virus in Egypt: a systematic review and data synthesis. BMC Infect Dis 13, 288 (2013) doi:10.1186/1471-2334-13-288
- Hepatitis C Virus
- Systematic Review