Spatial Epidemiology of Hepatitis C Virus Infection inEgypt: Analyses and Implications
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Spatial Epidemiology of Hepatitis C Virus Infection in
Egypt: Analyses and Implications
Diego F. Cuadros,1,2 Adam J. Branscum,3 F. DeWolfe Miller,4 and Laith J. Abu-Raddad1,2,5
Egypt has the highest hepatitis C virus (HCV) prevalence in the world (14.7%). The drivers
of the HCV epidemic in Egypt are not well understood, but the mass parenteral antischistosomal
therapy (PAT) campaigns in the second half of the 20th century are believed
to be the determinant of the high prevalence. We studied HCV exposure in Egypt at a
microscale through spatial mapping and epidemiological description of HCV clustering.
The source of data was the 2008 Egypt Demographic and Health Survey. We identified
clusters with high and low HCV prevalence and high and low PAT exposure using Kulldorff
spatial scan statistics. Correlations across clusters were estimated, and each cluster
age-specific HCV prevalence was described. We identified six clusters of high HCV prevalence,
three clusters of low HCV prevalence, five clusters of high PAT exposure, and four
clusters of low PAT exposure. HCV prevalence and PAT exposure were not significantly
associated across clusters (Pearson correlation coefficient [PCC] 5 0.36; 95% confidence
interval [CI] 20.12 to 0.71). Meanwhile, there was a strong association between HCV
prevalence in individuals older than 30 years of age (who could have been exposed to
PAT) and HCV prevalence in individuals 30 years of age or younger (who could not have
been exposed to PAT) (PCC 5 0.81; 95% CI 0.55-0.93). Conclusion: The findings illustrate
a spatial variation in HCV exposure in Egypt. The observed clustering was suggestive of an
array of iatrogenic risk factors, besides past PAT exposure, and ongoing transmission. The
role of PAT exposure in the HCV epidemic could have been overstated. Our findings support
the rationale for spatially prioritized interventions. (HEPATOLOGY 2014;60:1150-1159)
See Editorial on Page 1124
Hepatitis C virus (HCV), first identified in
1989,1 is an RNA virus that is primarily
transmitted through direct percutaneous
exposure to blood, such as through blood transfusions,
sharing of needles, and accidental percutaneous occupational
exposures common in healthcare workers and
dentists.2 After the discovery of this virus, a flurry of
studies around the world was conducted to document
its distribution and prevalence in human populations.3
It is now well established that HCV is a global health
challenge, with an estimated 130-170 million chronic
infections (2-3% of the global population).3,4 An
anomaly in the distribution of HCV infection, however,
was discovered in Egypt, where the prevalence
was 10-fold higher than that in other countries.5,6
The unusual high prevalence in Egypt has stimulated
research to identify the factor or factors that contributed
to such widespread HCV transmission in this
country. Based largely on indirect evidence,7-12 it was
believed that an extensive iatrogenic exposure to HCV
occurred during the mass parenteral antischistosomal
Abbreviations: CAPMAS, Egyptian Central Agency for Public Mobilization and Statistics; CI, confidence interval; CIA, chemiluminescent microplate immunoassay;
EDHS, Egypt Demographic and Health Survey; ELISA, enzyme immunoassay; GIS, Geographical information system; GPS, global positioning system; HCV,
hepatitis C virus; PAT, parenteral antischistosomal therapy; PCC, Pearson correlation coefficient; RR, relative risk; RT-PCR, real-time reverse-transcription polymerase
chain reaction.
From the 1
Infectious Disease Epidemiology Group, Weill Cornell Medical College - Qatar, Cornell University, Qatar Foundation - Education City, Doha,
Qatar; 2
Department of Healthcare Policy and Research, Weill Cornell Medical College, Cornell University, New York, NY, USA; 3
College of Public Health and
Human Sciences, Oregon State University, Corvallis, OR, USA; 4
Department of Tropical Medicine and Medical Microbiology and Pharmacology, University of
Hawaii, Honolulu, HI, USA; 5
Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
Received February 2, 2014; accepted May 29, 2014.
This study was made possible by JSREP grant number 3-014-3-007 from the Qatar National Research Fund (a member of Qatar Foundation). Additional support
was provided by the Biostatistics, Epidemiology, and Biomathematics Research Core at the Weill Cornell Medical College in Qatar. The statements made herein
are solely the responsibility of the authors.
1150
therapy (PAT) campaigns in Egypt, from as early as
1921, but most intensively during the 1960s and
1970s.11 These campaigns were phased out across
Egypt by the late 1970s and early 1980s.11
HCV prevalence levels in Egypt indicate uneven
geographic distribution, with higher HCV prevalence
found in rural areas compared to urban settings,13-15
and in Lower Egypt compared to the rest of the country.11,15
The factors contributing to the spatial heterogeneity
are not well understood, but disparity in the
intensity of past PAT campaigns has been proposed as
a cause of the geographical variation.10-12,16 A detailed
knowledge of the geographical distribution of HCV
exposure in Egypt may aid both an elucidation of the
drivers of past and present infection transmission and
identification of areas with the highest disease burden,
where interventions could be prioritized.
Aligned with the concept of “Know your epidemic,
know your response,” a successful framework and
strategy in HIV control,17 we studied HCV prevalence
in Egypt at a microscale level through spatial mapping
and epidemiological description of the clustering of
HCV exposure. With the ultimate aim of developing a
more effective strategy to control HCV infection transmission
in Egypt, and to clarify the potential drivers
of HCV transmission, we implemented a novel
approach to analyze the geographical and epidemiological
differences in areas where the probability of HCV
exposure was higher or lower, and in areas where PAT
exposure was higher or lower.
Materials and Methods
Data Sources. The main source of data in our study
was the Egypt Demographic and Health Survey (EDHS)
conducted in 2008,6 one of the largest nationally representative
studies of HCV infection ever implemented.
The survey used a stratified three-stage random cluster
sampling to enroll more than 19,500 households. The
first stage involved selecting primary sampling units such
as towns in urban areas and villages in rural areas. The
second stage included mapping and household listing,
where the global positioning system (GPS) was used to
generate the geographical information system (GIS) dataset
that stored the geographical coordinates of each of the
EDHS clusters of households. The final stage of the sampling
involved the selection of the household sample.
All women and men aged 15-59 present in the
sampled households were eligible for the survey, and
11,126 (87.1%) of these individuals agreed to and were
given an HCV biomarker test. The HCV testing protocol
included an initial round of testing to detect the
presence of antibodies against the virus. A thirdgeneration
enzyme immunoassay (ELISA), Adlatis EIAgen
HCV Ab kit, was used to test for antibodies against
HCV, and then confirmed by a chemiluminescent
microplate immunoassay (CIA) when positive.6 Quantitative
real-time reverse-transcription polymerase chain
reaction (RT-PCR) was also used at the Egyptian Ministry
of Health Central Laboratory for the detection of
HCV RNA using the RealTime m2000 system (Abbott
Laboratories, Abbott Park, IL).6 Further methodological
details related to specimen handling and laboratory
methods employed for the detection of HCV antibody
and HCV RNA can be found in El-Zanaty and Way.6
We used the dichotomous HCV antibody serological
status for each individual as the response outcome in
our statistical analyses because of our epidemiological
interest in investigating exposure to this virus, rather
than chronic infection. HCV prevalence in this article
refers strictly to the proportion of individuals who are
serologically antibody-positive for HCV. We also used
the binary answer to the question: “Ever had received
an injection to treat for schistosomiasis” as the measure
of PAT exposure. Further details related to the EDHS
methodology can be found in El-Zanaty and Way.6
Spatial Cluster Analysis. We identified spatial clusters
of high and low HCV prevalence, as well as spatial
clusters of high and low PAT exposure, using a spatial
scan statistical analysis,18 implemented in the SaTScan
software.19,20 Scan statistics are one of the most widely
used statistical methods for cluster detection in epidemiology.21,22
Briefly, scan statistical analysis uses circular
windows of varying radii that span the study region to
Address reprint requests to: Diego Cuadros, Ph.D., or Laith Abu-Raddad, Ph.D., Infectious Disease Epidemiology Group, Weill Cornell Medical College, Qatar,
Qatar Foundation, Education City, P.O. Box 24144, Doha, Qatar. E-mail: [email protected] or [email protected]; fax: 1(974)
4492-8333.
Copyright VC 2014 The Authors. HEPATOLOGY published by Wiley on behalf of the American Association for the Study of Liver Diseases. This is an open access article
under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original
work is properly cited, the use is non-commercial and no modifications or adaptations are made.
View this article online at wileyonlinelibrary.com.
DOI 10.1002/hep.27248
Potential conflict of interest: Nothing to report.
HEPATOLOGY, Vol. 60, No. 4, 2014 CUADROS ET AL. 1151
identify areas with exposure clustering. Since we aimed
to identify localized clusters, a maximum circular window
of 30 Km in radius was used for scanning clusters
of HCV exposure and PAT exposure. The circular window
was varied continuously in both location and radius
size. The radius size was varied from 0 Km up to the
fixed maximum radius (30 Km), thus creating and testing
a large number of distinct potential clusters of
diverse sizes. Each potential cluster was tested using a
likelihood ratio test to determine the statistical signifi-
cance against the null hypothesis of spatial randomness.
Clusters with P < 0.05, calculated through Monte Carlo
simulations, were identified as statistically significant,
and they were analyzed further for additional epidemiological
description.
Cluster Characterization and Correlations. After
a cluster was identified, the strength of the clustering
was estimated using the relative risk (RR) of HCV infection
within the cluster versus the area outside the cluster.
The fraction of the population living within the cluster
and HCV prevalence were also estimated for each cluster.
Correlation between HCV prevalence and PAT
exposure across the identified clusters was determined
using Pearson correlation coefficient (PCC). Agespecific
prevalence of HCV exposure for each cluster was
described. As mentioned above, PAT campaigns were
phased out across Egypt by the late 1970s and early
1980s. Therefore, we assumed that those younger than
30 years of age were virtually unexposed to PAT. This
age cutoff was then used to assess the association
between HCV prevalence in individuals older than 30
years of age (individuals who could have been exposed
to PAT) and HCV prevalence in individuals 30 years of
age or younger (individuals who could not have been
exposed to PAT). The correlation between HCV prevalence
in individuals older than 30 years and HCV prevalence
in individuals aged 30 years or younger was
calculated across the clusters using PCC. These statistical
analyses were conducted using SAS v. 9.3.23
Geographical Distribution of HCV Incidence. We
generated a mapping by governorate of the average
annual HCV incidence rate experienced by the living
Egyptian cohort, using a methodology introduced
and developed by Leske et al.,24 among others,25 and
applied recently by Miller and Abu-Raddad to study
HCV incidence in Egypt at the national level.26
Briefly, the incidence rate was estimated from the
age-stratified HCV prevalence per governorate. We
assumed that the incidence risk (P) was a cumulative
probability, ranging from 0 to 1, of HCV infection
over a certain period of time, which we took to be a
5-year age range. It follows that the cumulative probability
of incident cases for age interval x is given by
Px5 Px112Px
Dx
;
where Px is the prevalence proportion for age interval
x, Px11 is the prevalence proportion for the next older
age group (x11), and Dx is the range of ages in interval
x.
The total population size for each governorate was
obtained from the Egyptian Central Agency for Public
Mobilization and Statistics (CAPMAS), based on 2006
census data.27 To estimate the fraction of the population
in each 5-year age group for individuals aged 15-
59 in every governorate, we assumed that these proportions
were the same as the proportions estimated
for the national sample in the EDHS.
GIS analyses, including the production of cartographic
displays, were performed with ArcGIS v. 9.2.28
Results
Spatial Clustering of HCV Infection. HCV prevalence
in responders aged 15-59 years, main outcome
in our analysis, was 14.7% (95% confidence interval
[CI] 13.9-15.5%). HCV RNA positivity prevalence
was 9.8%.6 We identified six clusters of high prevalence
of HCV exposure (Fig. 1A; Table 1): Cluster 1,
located at the interface between the governorates of
Beni Suef and Minya (HCV prevalence of 33.1%);
Cluster 2, Faiyum (23.8%); Cluster 3, Dakahlia
(23.4%); Cluster 4, Kafr el-Sheikh (26.5%); Cluster 5,
Monufia (22.3%); and Cluster 6, Minya (23.1%). We
also identified three clusters of low prevalence of HCV
exposure (Fig. 1B): Cluster 7, Alexandria (7.5%);
Cluster 8, Cairo (9.4%); and Cluster 9, Luxor (5.8%).
Furthermore, 20.8% (95% CI 20.0-21.6%) of the
total population of Egypt resided within clusters of
high HCV prevalence, whereas 17.6% (95% CI 16.9-
18.4%) of the total population resided within clusters
of low HCV prevalence.
Spatial Clustering of PAT Exposure. The proportion
of the population that was ever exposed to PAT
was 9.2% (95% CI 8.6-9.7%). We identified five clusters
of high PAT exposure (Fig. 1C): Cluster 10,
located at the interface between the governorates of
Beni Suef and Minya (PAT exposure of 23.9%); Cluster
11, Sohag (19.4%); Cluster 12, Beni Suef (17.1%);
Cluster 13, Kafr el-Sheikh (22.3%); and Cluster 14,
Asyut (17.8%). In addition, we identified four clusters
of low PAT exposure (Fig. 1D): Cluster 15, Cairo
1152 CUADROS ET AL. HEPATOLOGY, October 2014
(PAT exposure 2.5%); Cluster 16, Alexandria (3.6%);
Cluster 17, Monufia (3.3%); and Cluster 18, Suez
(0%). Furthermore, 13.1% (95% CI 12.5-13.8%) of
the total population was located within clusters of
high PAT exposure, whereas 20.8% (95% CI 20.0-
21.6%) of the total population was located within
clusters of low PAT exposure.
Comparisons Between Clusters of HCV Infection
and PAT Exposure and Correlation Between HCV
Exposure and PAT Exposure. Cluster 1-Beni Suef/
Mynia, which had the largest relative risk of HCV
infection (RR 5 2.4), and implicitly the largest HCV
prevalence (33.1%), overlapped with a cluster of high
PAT exposure (Cluster 10). In contrast, PAT exposure
in the high HCV prevalence clusters of Faiyum,
Dakahlia, and Mynia was not statistically significantly
different from the national PAT exposure. Moreover,
the high PAT exposure clusters of Sohag and Asyut
had low HCV prevalence compared to the national
level (9.4% and 9.5%, respectively).
Figure 2A illustrates a comparison between HCV
prevalence and PAT exposure for each cluster identified
by scan statistics. Clusters with high or low HCV
prevalence, and clusters with high or low PAT exposure,
were scattered, with no evident overall pattern of
an association between HCV prevalence and PAT
exposure. There was a weak association, and with a
broad confidence interval consistent with the null
hypothesis of no correlation, between HCV prevalence
per cluster and the corresponding PAT exposure
(PCC 5 0.36; 95% CI 20.12 to 0.71; P 5 0.14).
There was a high HCV prevalence cluster of 22.3%,
located in the governorate of Monufia (Cluster 5), that
had also a low PAT exposure of 4.1% (Fig. 2A). Additionally,
a cluster of low PAT exposure in the Suez governorate
(Cluster 18), which contained no individuals
reporting a PAT exposure, had an HCV prevalence of
12.2%, nearly as high as the national HCV
prevalence.
Patterns of Age-Specific HCV Prevalence and Correlation
Between HCV Exposure Among the Old and
Young. The analysis of the age-specific prevalence of
HCV exposure reflected regional variations among the
clusters identified by scan statistics. The influence of
PAT on the age distribution of HCV prevalence was
evident in Cluster 1-Beni Suef/Minya, which had the
largest HCV prevalence and a high PAT exposure. The
epidemiological profile observed in this cluster showed
a curve where HCV prevalence was low and constant
for young individuals followed by a sharp rise for older
individuals, indicative of a cohort effect11 (Fig. 3B).
This cohort effect, however, was not observed in other
clusters, such as the low PAT exposure clusters (Fig.
3D), where the age-specific HCV prevalence increased
steadily with age, indicative of a steady exposure to
HCV infection. This pattern of steady increase with
age is illustrated in a high HCV prevalence cluster that
also had a low PAT exposure (Cluster 5, Monufia; Fig.
3C), and a similar pattern was observed in the other
clusters with high HCV prevalence.
Table 1. Hepatitis C Virus (HCV) and Parenteral Antischistosomal Therapy (PAT) Clustering Description
Cluster
Fraction of the Population
Within Cluster (%)
HCV Prevalence
(%)
PAT Prevalence
(%)
Relative*