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Published by Oxford University Press on behalf of the International Epidemiological Association
ß The Author 2009; all rights reserved. Advance Access publication 6 May 2009
International Journal of Epidemiology 2009;38:757–765
doi:10.1093/ije/dyp194
Community transmission of hepatitis B virus in
Egypt: results from a case–control study in
Greater Cairo
Adela Paez Jimenez,1 Noha Sharaf El-Din,2 Mostafa El-Hoseiny,2 Mai El-Daly,3,4
Mohamed Abdel-Hamid,3,5 Saeed El Aidi,6 Yehia Sultan,7 Nasr El-Sayed,8 Mostafa Kamal Mohamed2
and Arnaud Fontanet1*
Accepted
7 October 2008
Background To identify current risk factors for hepatitis B virus (HBV) transmission in Greater Cairo.
Methods
A 1:1 matched case–control study was conducted in two ‘fever’
hospitals in Cairo. Acute hepatitis B cases were patients with
acute hepatitis, positive HBs antigen, and high anti-HBc IgM
titres. Control subjects were acute hepatitis A patients (positive
anti-HAV IgM) or relatives of patients diagnosed with acute hepatitis C, identified at the same hospitals, with no past HBV infection
(negative anti-HBc) and matched to cases on the same age and
sex. Conditional logistic regression was used to identify factors
associated with acute hepatitis B.
Results
Between April 2002 and June 2006, 233 cases and 233 controls were
recruited to the study. In multivariate analysis, factors associated
with an increased HBV risk in males were illiteracy [odds ratio
(OR) ¼ 6.1, 95% confidence interval (CI) ¼ 2.8–13.1], shaving at
barbers (OR ¼ 2.1, 95% CI ¼ 1.1–3.9) and injecting drug use (IDU)
(OR ¼ 3.4, 95% CI ¼ 1.0–11.4). In females, factors associated with
an increased HBV risk were illiteracy (OR ¼ 2.2, 95% CI ¼ 1.0–5.0),
recent (<1 year) marriage (OR ¼ 42.0, 95% CI ¼ 3.8–463.9 compared
with single women) and giving birth (OR ¼ 3.7, 95% CI ¼ 1.0–13.9).
Conclusion In this study, HBV transmission took place primarily in the community, whether as a result of recent marriage (presumably first
sexual intercourse), shaving at barbershops or IDU, and was more
common among illiterates. Health promotion campaigns should
be carried out to increase awareness about community transmission
of HBV. In addition to routine immunization for infants and other
populations, premarital screening might be useful to identify at-risk
spouses in order to propose targeted immunization.
Keywords
Acute hepatitis, risk factors, hepatitis B infection, epidemiology, Egypt
5
1
2
3
4
Emerging Disease Epidemiology Unit, Institut Pasteur, Paris,
France.
Department of Community, Environmental and Occupational
Medicine, Faculty of Medicine, Ain Shams University, Cairo,
Egypt.
Viral Hepatitis Research Laboratory, National Hepatology &
Tropical Medicine Research Institute, Cairo, Egypt.
National Liver Institute, Menoufia University, Shibin El Kom,
Egypt.
Department of Microbiology, Faculty of Medicine, Minia
University, Minia, Egypt.
6
Hepatitis Section, Imbaba Fever Hospital, Cairo, Egypt.
7
Hepatitis Section, Abassaia Fever Hospital, Cairo, Egypt.
8
Department of Preventive Affairs, Ministry of Health and
Population, Cairo, Egypt.
* Corresponding author. Unité d’Epidémiologie des Maladies
Emergentes, Institut Pasteur, 25–28, rue du Docteur Roux,
Bâtiment Laveran 3ème étage, 75724 Paris cedex 15, France.
E-mail: [email protected]
757
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INTERNATIONAL JOURNAL OF EPIDEMIOLOGY
Introduction
Hepatitis B vaccination is the most effective measure
to prevent hepatitis B virus (HBV) infection and its
consequences, including cirrhosis of the liver, liver
cancer, liver failure and death.1 Persons infected as
infants or young children are less likely to develop
acute hepatitis but more likely to develop chronic
infection, and are the main reservoir for continued
HBV transmission.2,3
Mass immunization lowers transmission rates and
hence, pushes back the average age of infection.4
This phenomenon has been well documented in
Italy.5 In the USA, following implementation of
universal vaccination of infants beginning at birth in
the early 1990s, as well as routine vaccination of
previously unvaccinated children and adolescents
plus vaccination of adults at risk in 1995, incidence
of acute hepatitis B declined by 75%, with the greatest
decrease (96%) occurring among children and adolescents. At present, adults account for 95% of new
infections in the USA. In these low-endemicity countries [0.1–2% HBs antigen (HBsAg) prevalence], ongoing HBV transmission occurs primarily among
unvaccinated adults through sexual transmission
and injecting drug use (IDU).6
A similar decrease in HBV incidence is expected
among children in intermediate-endemicity countries
(3–5% HBsAg prevalence), such as Saudi Arabia7 or
Egypt,8 where 90% immunization coverage has been
achieved.9 In Egypt, HBV vaccination was included in
1992 in the Expanded Program of Immunization
(EPI) with injections at 2, 4 and 6 months of age
using recombinant vaccine.10 To identify current risk
factors for HBV transmission among older adolescents
and adults in Greater Cairo, we have conducted
a case–control study, the results of which are presented in this article.
Methods
A matched case–control study was conducted enrolling incident acute symptomatic hepatitis B patients
identified through a surveillance system for acute
hepatitis in two public ‘fever’ hospitals in Cairo
(description of the surveillance system published
elsewhere11).
Patients with recent (<3 weeks) symptoms suggestive of hepatitis (fever and/or jaundice) were invited
to participate in the study. After providing informed
consent (from parents if <18 years of age), they
answered orally administered standardized questionnaires covering socio-demographic characteristics,
present and past health conditions, and exposure to
potential risk factors for viral hepatitis during the
6 months preceding the onset of symptoms.
Exposures were categorized as iatrogenic and community related. Iatrogenic exposures included history of
invasive medical procedures (e.g. surgery, intravenous
catheter, endoscope, blood transfusion, drip infusions,
injections), obstetrical procedures (women only) and
dental treatment. Community exposures included history of circumcision, shaving at barbershops, sharing
razors or nail trimmers with family members, getting
manicures or pedicures at beauty salons, and tattooing and ear-piercing. Questions on high-risk behaviour such as multiple sexual partners or drug use
(e.g., pills, sniffing or injecting) were only asked to
men, due to their sensitive nature.
Serum samples were collected and tested according
to the manufacturer’s instructions for the following
hepatitis markers: anti-HAV IgM (HAVABÕ , M EIA,
Abbott Laboratories, Diagnostics Division, IL, USA),
anti-HBc IgM (CORZYMEÕ , M rDNA, Abbott
Laboratories, Diagnostics Division, IL, USA), HBs antigen (AUSZYME MONOCLONALÕ , third generation
EIA, Abbott Laboratories, Diagnostics Division, IL,
USA), anti-HCV antibody (INNOTESTÕ HCV Ab IV,
Innogenetics, Ghent, Belgium). For patients whose
anti-HAV and anti-HBc IgM were negative, HCV
RNA was detected by direct nested reverse transcriptase polymerase chain reaction (in-house array using
50 -untranslated region primers).12 Standard liver
functions were also tested, including alanine aminotransferase (ALT), aspartate aminotransferase (AST),
bilirubin and alkaline phosphatase.
An acute hepatitis B case was defined as a patient
with acute hepatitis symptoms lasting for <3 weeks,
ALT three times or higher the upper limit of normal
(ULN), no haemolysis and no obstructive cause
of jaundice, positive HBs antigen and anti-HBc IgM
readings at least twice the optical density cut-off
chosen to be positive according to the manufacturer’s
instructions (to rule out moderate elevations of antiHBc IgM in chronic hepatitis B).13
Controls were recruited among hepatitis A patients
(anti-HAV IgM positive) or among the relatives of the
hepatitis C patients identified in the same fever hospitals (note: a case–control study on factors associated
with acute hepatitis C is on going; this is the original
purpose for controls among relatives of acute hepatitis
C cases). All were anti-HBc antibody negative
(i.e. had not been infected by HBV in the past).
Controls were matched 1:1 to cases on the same age
and sex. No case was <11 years old, whereas only
seven hepatitis A controls were 440 years old.
Therefore, for matching purposes, only 10–40-yearsold subjects were included in the final analysis.
Statistical analysis
Categorical and continuous variables were compared
across groups using Chi-square and Mann–Whitney
U-test, respectively. All putative exposures were
tested for association with acute hepatitis B in univariate analysis and those with P < 0.20 were then
entered into a conditional logistic regression model
to examine their independent effect. Since sex was
found to be an effect modifier on socio-demographic
COMMUNITY TRANSMISSION OF HBV IN EGYPT
characteristics (marriage status and illiteracy, defined
as the lack of ability to read and write), since many
potential risk factors were sex specific (e.g. pregnancy,
ear-piercing, barber shaving), and since questions
regarding high-risk behaviours were only asked
to men (alcohol consumption, drug use and sexual
promiscuity), we present data separately for men
and women.
The final models were obtained through stepwise
deletion of variables until all variables left in the
model had P < 0.05. Two-tailed P-values were reported.
We also tested whether the results would differ
according of the series of controls used. Therefore,
for each pair of observations (i.e. a case and its
matched control), we allocated the value 1 if the control was a hepatitis A patient, or 0 if the control was a
relative of hepatitis C patient. We then tested in each
of the two final models (males and females) whether
there was any effect modification by this newly
created variable for each of the exposures associated
with acute hepatitis B. All statistical analyses
were performed using STATA 9.0 software (Stata
Corporation, College Station, TX, USA).
The study was conducted with the approval of the
Institutional Review Board at the Egyptian Ministry
of Population and Health (MOPH), and with
759
clearance from the ethics committee of the National
Hepatology and Tropical Medicine Research Institute
in Cairo, Egypt.
Results
Between April 2002 and June 2006, 233 cases and as
many controls matched on the same age and sex
were identified in the two study hospitals. Among
the 233 controls, 124 (53%) were relatives of patients
diagnosed with acute hepatitis C and 109 were acute
hepatitis A patients.
Clinical description of cases
Among the 233 HBV cases retained for the analysis,
64% (149) were men with a median interquartile
range (IQR) age of 22 (19–26) years and 36% (84)
were women with a median (IQR) age of 23 (20–
27) years (Table 1). All 233 cases were symptomatic
and 76.4% had an insidious onset. Median ALT was
765 IU/l (close to 20 times the ULN, 40 IU/l), and no
difference was observed between men and women.
There was no age effect on the duration of illness,
but an effect of sex, with a longer mean (SD) duration of symptoms at the time of examination for
Table 1 Recruitment and clinical among male and female acute hepatitis B cases, Greater Cairo, 2002–06
All patients
(N ¼ 233)
Males
(N ¼ 149)
Females
(N ¼ 84)
P-value
2002
47 (20.2%)
33 (22.2%)
14 (16.7%)
0.633
2003
65 (27.9%)
41 (27.5%)
24 (28.6%)
2004
64 (27.5%)
37 (24.8%)
27 (32.1%)
2005
53 (22.8%)
36 (24.2%)
17 (20.2%)
2006
4 (1.7%)
2 (1.3%)
2 (2.4%)
9.4 ( 4.6)
9.9 ( 4.8)
8.5 ( 4.3)
0.03
Time trend in case identification
Symptoms
Mean (þSD) duration (days)a
Fever
112 (48.1%)
65 (43.6%)
47 (55.9%)
0.07
Jaundice
231 (99.1%)
148 (99.3%)
83 (98.8%)
0.68
Light clay stools
192 (82.4%)
123 (82.5%)
69 (82.1%)
0.9
Dark urine
228 (97.8%)
146 (97.9%)
82 (97.6%)
0.7
Abdominal pain
176 (75.5%)
103 (69.1%)
73 (86.9%)
0.002
Vomiting
135 (57.9%)
84 (56.4%)
49 (58.3%)
0.58
765 (570–1301)
765 (570–1176)
785 (550–1554)
0.75
575 (365–902)
550 (368–854)
600 (365–1007)
0.24
8.8 (6.4–12.6)
8.7 (6.0–12.2)
9.4 (7.3–12.9)
0.13
156 (107–236)
163 (115–241)
146 (100–216)
0.20
Liver functions: median (IQR)
Alanine aminotransferase (IU/l)b
Aspartate aminotransferase (IU/l)
Total bilirubin (mg/dl)a
Alkaline phosphatase (IU/l)
Data missing:
a
Three males.
b
Two males.
c
Six males and three females.
c
b
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INTERNATIONAL JOURNAL OF EPIDEMIOLOGY
males compared with females [9.9 (4.8) vs 8.5 (4.3)
days, respectively, P ¼ 0.03].
Socio-demographic characteristics associated
with acute hepatitis B
The proportion of illiterates was higher among HBV
cases (35.0%) compared with controls (12.8%)
(P < 0.001) (Table 2). This increase in HVB risk due
to illiteracy was true for both sexes but the risk was
of a higher magnitude for men [odds ratio (OR) ¼ 6.6,
95% confidence interval (CI) ¼ 3.1–14.0] compared
with women (OR ¼ 2.5, 95% CI ¼ 1.3–5.1) (P-value
for the interaction term ¼ 0.07). The same effect modification by sex was found with marriage, with a
higher magnitude of the associated risk for women
(OR ¼ 8.0, 95% CI ¼ 3.1–20.7) compared with men
(OR ¼ 1.2, 95% CI ¼ 0.6–2.5) (P-value for the interaction term ¼ 0.007). After splitting marriage into categories by duration of marriage, the increased risk of
acute hepatitis B was particularly elevated for women
married for <1 year (OR ¼ 49.4, 95% CI ¼ 4.3–562.0),
compared with singles.
Iatrogenic exposures
Iatrogenic exposures in the past 6 months were quite
common in the control series, as shown by the percentage who received injections (15.4 and 38.1% for
males and females, respectively), dental treatment
(10.7 and 17.9%, respectively) or stitches (4.0 and
7.1%, respectively) (Table 3). In general, females
experienced more frequent invasive medical procedures than males. However, none of the procedures
was associated with an increase in HBV risk except
for giving birth (OR ¼ 3.3, 95% CI ¼ 1.1–9.8).
Episiotomy, forceps and Caesarean section were not
individually associated with an increase in HBV risk,
but numbers were low for each procedure (data not
shown). Dental and gum treatments have been
previously described as risk factors for HBV transmission.14,15 In our data, none of the dental procedures
(gingival treatment, tooth filling, tooth extraction and
dental anaesthesia) was associated with an increase
in HBV risk.
Community exposures
Acupuncture and tattooing were not common practices among study participants. There was no difference among cases and controls regarding ear-piercing
or getting manicures or pedicures in beauty salons
(Table 4). Noteworthy is the finding that shaving at
barbershops was at increased risk of HBV transmission (OR ¼ 2.4, 95% CI ¼ 1.3–4.4) since this is a very
common practice among Egyptian men (64.4% of
controls).
Only men were asked about high-risk behaviour,
such as drinking alcohol, sexual promiscuity or drug
use. The frequency of alcohol consumption (17% of
controls) and drug use (13% of controls) was higher
than expected. Alcohol use (OR ¼ 2.7, 95% CI ¼ 1.5–
4.8) and IDU (OR ¼ 4.2, 95% CI ¼ 1.4–13.9) were associated with acute hepatitis B.
Multivariate analysis
In multivariate analysis, we found the same risk factors related to HBV transmission as in the univariate
analysis (Table 5). Among men, illiteracy, shaving at
barbershops and IDU all remain associated with a
substantial increase in risk. Among women, illiteracy
was again associated with increased risk, as well as
recent marriage and giving birth. For each of these
Table 2 Distribution of socio-demographic risk factors among male and female acute hepatitis B cases and controls,
Greater Cairo, 2002–06
Males (N ¼ 298)
Cases (%)
Controls (%)
(N ¼ 149)
(N ¼ 149)
ORa
(95% CI)
Females (N ¼ 168)
Cases (%)
Controls (%)
(N ¼ 84)
(N ¼ 84)
ORa
(95% CI)
Education
Illiterate
Some education
46 (30.9)
10 (6.7)
6.6 (3.1–14.0)
36 (42.9)
20 (23.8)
2.5 (1.3–5.1)
103 (69.1)
139 (93.3)
1
48 (57.1)
64 (76.2)
1
113 (75.8)
116 (77.9)
1
14 (16.7)
38 (45.2)
1
36 (24.2)
33 (22.2)
1.2 (0.6–2.5)
70 (83.3)
46 (54.8)
8.0 (3.1–20.7)
Marital status
Single
Married
Marriage duration (years)
113 (75.8)
116 (77.9)
1
14 (16.7)
38 (45.2)
1
<1
4 (2.7)
1 (0.7)
5.0 (0.5–51.6)
8 (9.5)
1 (1.2)
49.4 (4.3–562.0)
1–5
Single
a
18 (12.4)
19 (12.8)
0.9 (0.4–2.1)
25 (29.7)
16 (19.0)
7.7 (2.5–23.5)
6–10
6 (4.2)
11 (7.4)
0.6 (0.1–2.2)
16 (19.0)
13 (15.5)
12.9 (2.9–55.9)
410
4 (2.7)
2 (1.3)
1.9 (0.3–13.9)
12 (14.3)
12 (14.3)
10.3 (1.4–75.5)
Estimated using conditional logistic regression.
Statistically significant ORs are shown in bold.
COMMUNITY TRANSMISSION OF HBV IN EGYPT
761
Table 3 Health care-related risk factors among male and female acute hepatitis B cases and controls, Greater Cairo,
2002–06
Males (N ¼ 298)
Cases (%)
Controls (%)
(N ¼ 149)
(N ¼ 149)
Invasive medical procedures
Hospitalization
Females (N ¼ 168)
Cases (%)
Controls (%)
(N ¼ 84)
(N ¼ 84)
ORa
(95% CI)
ORa
(95% CI)
9 (6.0)
8 (5.4)
1.1 (0.4–3.1)
15 (17.9)
11 (13.1)
1.4 (0.6–3.2)
0
1 (0.7)
–
1 (1.2)
0
–
Intensive care unit
Surgery
6 (4.0)
0
–
3 (3.6)
4 (4.8)
0.7 (0.2–3.4)
Stitches
12 (8.0)
6 (4.0)
2.1 (0.8–5.7)
8 (9.5)
6 (7.1)
1.3 (0.5–3.9)
Injections
19 (12.8)
23 (15.4)
0.8 (0.4–1.5)
30 (35.7)
32 (38.1)
0.9 (0.5–1.7)
IV infusion
6 (4.0)
5 (3.4)
1.2 (0.4–4.0)
14 (16.7)
13 (15.5)
1.1 (0.5–2.5)
Catheter
3 (2.0)
1 (0.7)
3.2 (0.3–32.1)
3 (3.6)
1 (1.2)
3.0 (0.3–28.8)
Abscess
6 (4.0)
0
–
1 (1.2)
3 (3.6)
0.3 (0.03–3.2)
Endoscopy
Transfusion
0
0
–
0
1 (1.2)
–
1 (0.7)
0
–
4 (4.8)
1 (1.2)
4.7 (0.5–46.2)
Obstetrical history (females only)
Pregnancy
NA
NA
22 (26.2)
9 (10.7)
1.7 (0.7–4.5)
Delivery
NA
NA
14 (16.7)
5 (6.0)
3.3 (1.1–9.8)
18 (12.1)
16 (10.7)
1.2 (0.5–2.4)
13 (15.5)
15 (17.9)
0.8 (0.4–1.9)
14 (9.4)
10 (6.7)
0.8 (0.1–7.0)
11 (13.1)
12 (14.3)
3.6 (0.3–38.7)
Dental treatment
Any
Gingival treatment
Tooth filling
Tooth extraction
Anesthesia
a
Estimated using conditional logistic regression.
Statistically significant ORs are shown in bold.
NA ¼ not applicable.
Table 4 Community exposures among male and female acute hepatitis B cases and controls, Greater Cairo, 2002–06
Males (N ¼ 298)
Cases (%)
Controls (%)
(N ¼ 149)
(N ¼ 149)
ORa
(95% CI)
Females (N ¼ 168)
Cases (%)
Controls (%)
(N ¼ 84)
(N ¼ 84)
ORa
(95% CI)
Community exposures
Circumcision
0
0
–
0
0
116 (77.8)
96 (64.4)
2.4 (1.3–4.4)
NA
NA
17 (11.4)
20 (13.4)
0.8 (0.4–1.6)
NA
NA
4 (2.7)
1 (0.7)
4.1 (0.5–37)
9 (10.7)
3 (3.6)
85 (57.0)
102 (68.5)
0.8 (0.4–1.3)
58 (69.1)
55 (65.5)
1.6 (0.8–3.6)
NA
NA
4 (4.8)
2 (2.4)
2.1 (0.4–11.8)
3 (2.0)
1 (0.7)
3.1 (0.3–29.6)
0
0
–
49 (32.9)
25 (16.8)
2.7 (1.5–4.8)
9 (6.0)
11 (7.4)
1.0 (0.4–2.8)
Drug use
39 (26.2)
20 (13.4)
2.4 (1.3–4.4)
IDU
15 (10.1)
4 (2.7)
4.2 (1.4–13.9)
Shaving at barber
Sharing razor blades
Manicure
Sharing nail cutter
Ear-piercing
Tattooing
High-risk habits (males only)
Drinking alcohol
Sexual promiscuity
a
Estimated using conditional logistic regression.
Statistically significant ORs are shown in bold.
NA ¼ not applicable.
–
3.6 (0.9–14.5)
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INTERNATIONAL JOURNAL OF EPIDEMIOLOGY
Table 5 Multivariate analysis showing factors independently associated with acute hepatitis B by sex, Greater Cairo,
2002–06
Males (N ¼ 292)
adjusted OR (95% CI)a
6.1 (2.8–13.1)
Illiteracy
Barber shaving
Intravenous drug use
Females (N ¼ 155)
adjusted OR (95% CI)b
2.2 (1.0–5.0)
2.1 (1.1–3.9)
NA
3.4 (1.0–11.4)
NA
Marriage duration (years)
Single
1
<1
42.0 (3.8–463.9)
1–5
Not in the final model
4.5 (1.4–4.8)
6–10
7.1 (1.6–32.5)
410
3.5 (0.4–308)
Giving birth in the past 6 months
a
Estimated using conditional
the variables included in the
Estimated using conditional
the variables included in the
NA ¼ not applicable.
b
NA
3.7 (1.0–13.9)
logistic regression. Only 292 participants out of 298 were included due to missing data for any of
regression.
logistic regression. Only 155 participants out of 168 were included due to missing data for any of
regression.
models (males and females), the magnitude of risk
associated with each exposure was no different
according to the series of controls used (hepatitis A
patients or relatives of hepatitis C patients) (test for
interaction not significant).
Discussion
This is the first study of risk factors for HBV transmission among older adolescents and adults in
an intermediate-endemicity country that has recently
implemented a national immunization plan for
infants. The main finding of this study is that of continuing HBV transmission as a result of community,
rather than iatrogenic, exposure (except for obstetrical
procedures in women).
This study has several strengths: (i) it recruited incident cases, who as such had a well-defined 6-month
exposure period preceding the onset of symptoms
(the length of HBV’s incubation period), allowing
for the use of detailed questionnaires; (ii) the use of
incident cases also allowed for the identification of
current sources of exposure to HBV in Greater Cairo,
making our findings particularly relevant for on-going
prevention programs; and (iii) analyses had 80%
power to detect associations characterized by OR as
being as low as 1.8 for exposures present among 50%
of controls or 2.2 for exposures present among 10%
of controls (although the power decreased with subsequent sex stratification, the initial analysis for
iatrogenic exposures was performed with combined
male and female datasets without identifying any
risk factors associated with acute hepatitis B).
The study has, however, some limitations: by focusing on symptomatic cases, it selects for an age distribution which does not reflect that of all acute
infections, since symptomatic forms of acute infections are associated with older age. Indeed, while
the absence of children in our sample may be related
to vaccine efficacy, it may also reflect the rarity of
symptomatic forms among children. Still, it is unlikely that recruiting only symptomatic forms of infection would select for specific exposures or routes of
transmission unless these are related to age. Another
limitation concerns the avoidance of certain sensitive
questions about behaviours (mainly alcohol use, drug
use and sexual promiscuity) with women. As a result,
we were not able to identify these factors as risk factors for HBV transmission in women. Had we identified these factors, some associations documented in
this paper such as with educational level might have
been weakened. However, we believe that these behaviours are rare in the female population for cultural
reasons and thus would have limited confounding
ability in this context.
Interestingly, community transmission, rather than
iatrogenic transmission, was responsible for most
cases documented in this study. Among males,
shaving at barbershops was associated with a 2 fold
increase in risk of infection, a rather worrisome
figure considering that a majority of males (64% of
controls in this study) continue to get shaves at barbershops. This is a well-known risk factor not only for
HBV16 but also for HCV,17,18 calling for targeted education programmes. Barbers are usually unaware of
the concept of blood-borne transmission, and razors
and scissors are used repeatedly for different
COMMUNITY TRANSMISSION OF HBV IN EGYPT
customers without intervening sterilization.19,20 An
additional risk that needs to be further explored is
the ‘hijama’, or wet cupping, where blood is drawn
by vacuum from a small skin incision for therapeutic
purposes. Since the location is first shaved to ensure a
tight seal with the cup, it is frequently performed by
barbers. It is worth noting that in many countries,
laws have been passed to enforce sterilization of
equipment in barbershops.
Among males, another important contribution to
HBV transmission was intravenous drug use. The substantial proportion of controls (13%) who acknowledged drug use, with almost 3% admitting
intravenous drug use, was a surprise to us. The low
socio-economic status of study participants consulting
at ‘Fever hospitals’ may explain this high proportion.
As recommended by the Centers for Diseases Control
and Prevention (Atlanta, USA),6 HBV immunization
should be offered to drug users. In addition, given the
magnitude of the HCV pandemic in Egypt and the
growing concern regarding HIV transmission, needle
exchange programmes, accompanied by awareness
activities, should be urgently considered.
In females, marriage emerged as a risk factor for
acute HBV infection. The increase in risk was independent of pregnancy and delivery in multivariate
analysis and much higher for women being married
<1 year (i.e. recently married women). In a country
where premarital sex is rare, and notwithstanding
household transmission through the multiple exposures shared by married couples (e.g. sharing of personal hygiene items), this suggests a significant rate
of HBV transmission through first sexual contact with
infected spouses. Sexual transmission within married
couples has already been speculated as a possible
explanation for the high prevalence of HBV infection
in a closed population of Saudi Arabia.21 It may be
wise to consider premarital screening for HBV infection22 in order to propose immunization to nonimmune spouses marrying a chronically infected individual. Furthermore, considering the high fertility rate
among recently married women, and the risk of transmission to newborns, HBsAg screening of pregnant
women should be considered where feasible. If the
mother is found to be chronically infected, newborns
may benefit from HBV immunization at birth, as well
as administration of hepatitis B immunoglobulin.23
While HBV is transmissible through contact with
infected blood, no iatrogenic factor other than past
birth delivery was found associated with HBV transmission in this study. We were not able to identify
which of the procedures related to delivery might
have explained this association. This will unfortunately limit the type of recommendations that can
be made, excepting the standard precautions against
blood-borne infections in medical settings. Whether
the low relative contribution of iatrogenic transmission to new HBV infections reflects an improvement
763
in infection control in hospital facilities in Egypt24
needs to be confirmed through other studies.
Of note, we are currently gathering data for a similar
analysis comparing acute hepatitis C cases and controls from the same hospitals, and will assess whether
iatrogenic factors emerge as risk factors for another
blood-borne infection for which community transmission is probably much more limited.
More difficult to interpret is this study’s finding that
illiteracy is a risk factor for HBV infection, especially
since controls came from the same socio-economic
background. Low educational attainment has previously been associated with higher prevalence of hepatitis B in both developed and developing countries.25–27
But illiteracy is not in itself a specific mechanism for
HBV transmission and could stand in for other risk
factors, such as community exposures or high-risk
habits, which may not have been adequately identified
in our questionnaire. This is particularly true for women
for whom questions about risk habits were avoided.
It may also reflect the fact that prevention messages
do not reach the most vulnerable groups.
In conclusion, this study has confirmed the ongoing transmission of HBV in Greater Cairo during
a transition period following the introduction of childhood immunization. While efforts related to bloodborne infection control in medical settings should be
continued, this study suggests that the majority of
HBV transmission occurs within the community.
Based on the results of this study, health promotion
campaigns and prevention programs should be targeted to specific groups, such as intravenous drugs
users and barbershops clients and owners.
Premarital screening for HBV infection should be proposed. Finally, control of HBV transmission should be
viewed in the larger context of blood-borne infection
control, in a country where HCV infection rates are
among the world’s highest.
Funding
Agence Nationale de Recherche sur le SIDA et les
hépatites virales – France (ANRS 1203 & 12122).
Acknowledgements
The authors are indebted to the ‘Fever Hospital’
Abassaia and Imbaba and to the Department of
Community Medicine of Aim Shams University for
the scientific and logistical support in the recruitment
and diagnosis of the study participants, as well as
to the participants themselves for their assistance
in providing this information. The National
Hepatology and Tropical Medicine Research Institute
carried out the laboratory analysis for this project.
Conflict of interest: None declared.
764
INTERNATIONAL JOURNAL OF EPIDEMIOLOGY
KEY MESSAGES
A case–control study was performed in Greater Cairo (Egypt) to identify current risk factors for HBV
transmission.
In this setting, HBV transmission took place primarily in the community, whether as a result of
recent marriage (presumably first sexual intercourse), shaving at barbershops or IDU, and was more
common among illiterates.
Health promotion campaigns and prevention programmes should be targeted to specific groups, such
as IDUs and barbershop tenants and clients. In addition to routine immunization for infants and
other populations, premarital screening might be useful to identify at-risk spouses in order to propose
targeted immunization.
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