Journal of Medicine and Medical Sciences Vol. 1(3) pp. 065-070 April 2010
Available online http://www.interesjournals.org/JMMS
Copyright ©2010 International Research Journals
Full Length Research paper
Seroprevalence and risk factors of hepatitis A virus
among school children from different socioeconomic
status in Abidjan, Cote D’Ivoire.
Zinzendorf Nanga Yessé1, Kouassi- Agbessi Bra Thérèse 1, Oga Agbaya Serge2, Ahoussou
Everali1, Loukou Yao Guillaume1.
1
Département De Bactériologie-Virologie, UFR De Pharmacie, Université De Cocody, BP V34, Abidjan, Côte d’Ivoire
Département De Santé Publique Et d’Hydrologie, UFR De Pharmacie, Université De Cocody, BP V34, Abidjan, Côte
d’Ivoire
2
Accepted 05 April, 2010
Hepatitis A virus (HAV) has a worldwide but the developing countries are characterized by a high
endemic pattern of HAV. With improving conditions, the populations of these countries which have had
no contact with HAV increase and more susceptible to infection. The prevalence and risk factors of HAV
were assessed in children from Abidjan. From December 2002 to may 2003, HAV antibodies were
detected in serum samples in 306 children of 5-18 years, from Abidjan. In addition, demographic and
socioeconomic data were collected. The overall prevalence of antibodies to HAV was 81.3% and was
significantly correlated with the age of participants. It was 39.6% among those <6 years and 83.7%
among those >15 years. Among predictive factors studied, the type of housing, environment, sewage
disposal, parent’s education, number of siblings and economic status were highly associated with the
seroprevalence of HAV. The children with high socioeconomic status presented the lower rates. The
results of this study suggest that Abidjan is a high endemic area; however the children coming from
high socio-economic environment remain vulnerable to the HAV. Anti HAV vaccination could be
recommended with children of high socioeconomic status.
Key-words: hepatitis A, seroprevalence, risk factors, children, Abidjan
INTRODUCTION
Hepatitis A is an acute, usually self-limiting infection of
the liver caused by hepatitis A virus (HAV). Transmission
occurs primarily through the faecal-oral route and is
closely associated with poor sanitary conditions. The
most common modes of transmission include close
personal contact with an infected person and ingestion of
contaminated food and water (Synder and Pickering,
1996). The virus has a worldwide distribution and causes
about 1.5 million cases of clinical hepatitis each year. In
young children, HAV infection is usually asymptomatic
whereas symptomatic disease occurs more commonly
among adults. Antibodies against HAV developed in
response to infection and seroprevalence can be used as
a marker of viral transmission in a community (WHO
2000). The epidemiology of HAV is highly correlated with
*Corresponding author email:nangatchocht@yahoo.fr;
Tel:222(07743132/22476433)
age and level of hygiene (Margolis 1992; Steven 2001).
Three epidemiologic patterns of endemic (low,
intermediate, and high), are seen worldwide (Margolis
1992; Steven 2001). Industrialized countries are characterized by a low endemic pattern and seroprevalence
ranged from 13% to 50% in adults (Hendley 1972;
Jacobsen and Koopman 2004). In regions of intermediate
endemic, seroprevalence among adults varies from 60%
to 97%. Young children are not usually infected and
infection occurs at a later age in adolescents and young
adults (Hendley 1972; Jacobsen and Koopman 2004). In
developing countries, more than 90% of the population
has acquired natural immunity before 10 years of age
(Jacobsen and Koopman, 2004). With improving conditions, these countries enter a transition phase in which
the average age of infection and the proportions of the
populations which have had no contact with HAV increase. Therefore those populations are more susceptible to infection. These susceptible populations’ cons-
066 J. Med. Med. Sci.
serum was separated by centrifugation at 2000 rpm for 20mn. Serum sample was stored at -20°C until tested for antibodies to HAV
(IgM and IgM+IgG) by a qualitative enzyme-linked immunosorbent
assay (Enzygnost anti-HAV, Dade Berhing, Marburg, Germany)
according to manufacturer’s instructions. (Desbois 2005)
titute a greater burden of disease and a significant public
health problem (Chatproedprai et al., 2007; Jacobsen
and Koopman, 2004).
In Cote d’Ivoire, a country which is considered as an
area of high endemicity for HAV infection marked
economic, hygiene and sanitary improvements have
taken place in recent years, especially in urban areas
(Gouvernal 1983; Paulais 1991). We hypothesize that
improvements in living conditions may lead to changes in
the epidemiology of HAV infection, with a decrease in
antibody prevalence among children,consequently a
significant proportion of the adolescent and adult populations will run a risk of infection. The aim of this study
was to determine the age-specific seroprevalence of HAV
in a young population. In addition, factors associated with
anti-HAV prevalence are assessed.
The statistical analysis was performed by using the EpiInfo version
6 programs, the chi-squared test and Fisher's exact test for proportion comparison. Differences were regarded as significant when
p < 0.05.
MATERIALS AND METHODS
RESULTS
Study design and subjects
This is a cross-sectional study carried out in three medical centers
of Abidjan (School Medical Centers: Attecoubé, Externat Saint-Paul
of Plateau, and Sainte Anne-Marie International Clinic of Cocody),
from December 2002 to May 2003. The School children who were
asked to participle in this study, had minor medical problems
(headache, pallor, falls, cuts, school accidents, problems in visual
acuity, etc.). After written informed consents obtained from parents,
children aged 3-18 years, who consecutively attend in the medical
centers for ambulatory care during the period of the study, were recruited. Children who attended twice and more during the study period were included only once. The sample size was calculated
according to the formula No= 2 P (1 – P)/ I2, precision I = 5%, ecart
type = 1.96, sensitivity = 5%, prevalence P = 80%), No=246. The
study was reviewed and approved by the National Ethical Committee.
Collected data
Adolescents were interviewed personally while the parents of the
young children were interviewed by a member of the research team
for data collection. Data collected included demographic ones on
children (age, gender) and socioeconomic characteristics (type of
housing, area of residence, number of siblings, access to potable
water) and their parents (monthly income, educational level), their
previous history of symptomatic hepatitis A (history of jaundice) and
hepatitis A vaccine. Participants were allocated in four groups, <6
years, 6-10 years, 11-14 years and >15 years. Housing was classified as modern high standing (villa), modern and middle standing
(council flat) and old (traditional house). Three types of area (under,
fairly and very equipped) were identified according to the level of
public equipment, asphalted road, regular collecting of refuse,
gutter stone, etc. Based on educational level, parents were allocated into group 1 (university level), group 2 (illiterate) and group 3
(others consisted in primary and secondary level). The economic
status (ES) were performed by the Ministry of the Planification according to the monthly income of the parents, high ES (>1600 $US),
middle ES (400-1600 $US), low ES (<400 $US).
Determination of anti-hepatitis A antibodies
Blood samples were collected from children for HAV serology. The
Level of alanine amino-transferase
The level of liver enzyme alanine amino-transferase (ALT) in serum
was evaluated to assess liver function by a kinetic method (Gesan
Diagnostic Kit, Trapani, Italy) (Rizzo 2009)
Statistical analysis
During the study period, 337 children were enrolled.
There were 28 refusals to participate (for blood sample
collection) and 3 children who had already been vaccinated against hepatitis A was excluded, giving 306 children selected. The mean age (standard deviation) was
10.09 ± 4.78 years and sex ratio 1.41. The mean age
(standard deviation) of the 249 HAV positive and 57 HAV
negative was 10.62 ± 4.32 and 7.98 ± 2.63 respectively
(p<0.001). The overall prevalence of antibodies to HAV
was 81.4 (CI95% = 76.5 – 85.5) % and was significantly
correlated with the age (p<0.0001). It was 39.6% in
children < 6 years old and increased to 83.7% among
those >15 years. Males had a higher prevalence of antibodies to HAV (83.2%) than females (78.7%) although
this did not reach statistical significant differences
(p>0.05). The relation between seroprevalence and
children’s education have showed no statistically significant difference (p>0.05). Their age, gender and education distribution is shown in Table 1. The results of
table 2 shown that besides age, other variables were
significantly associated with HAV seroprevalence which
included the type of housing (p<0.001), environment
(p<0.001), potable water (p<0.005) sewage disposal
(p<0.001), number of siblings (p<0.001), father’s education (p<0.005), mother’s education (p<0.02) socioeconomic status (p<0.001). Children living in traditional
house (85.2%) and coming from under equipped area
(96.4%) are more exposed to HAV than children from
villa (64.4%) and very equipped areas (40.5%) (p<0.001).
The risk of anti-HAV decreased with higher ES, 97.9%
and 37.9% (low SES vs high SES), father’s education
98.5%and 55.7% (illiterate vs university), mother’s education 85.5% and 50.6% (illiterate vs university). The risk
of anti-HAV increased with higher number of siblings,
51.4% (0-3) and 92.3% (10 and more). The relation
between HAV seroprevalence and sociodemographic
Yessé et al. 067
Table 1. Seroprevalence of anti-hepatitis A (HAV) antibodies among the children according socio-demographic variables
variables
Age (years)
<6
6-10
11-15
>15
Gender
female
male
Education
kindergarten
primary
secondary
Tested (N=306)
Anti-HAV positive (N=249)
N0 (%)
63
124
82
37
25 (39.6)
116(93.5)
77(93.9)
31(83.7)
<0.0001*
127
179
100(78.7)
149(83.2)
0.31
29
153
124
22(75.8)
139(82.3)
101(81.4)
0.71
p
*Significant value
parameter is showed in table 2. From logistic analysis,
potable and sewage disposable were the most important
factors of prediction of HAV seropositivity among the participants. The risk of infection with HAV was 3.2 times
higher among children using potable water outside house
than those used potable water inside house. Using nonhygienic sewage disposal increased the risk of HAV infection 2.6 fold compared to using a private toilet with
flush (Table3). Among the 249 HAV-seropositive children,
37 had symptomatic disease (jaundice, fever, HAV IgM
positive), 8 (<6years), 24 (6-10 years), 5 (>15
years).Among the children with symptomatic disease, 10
presented acute hepatitis with elevated serum ALT
(range 68-120 IU/L). Table 4 shows no statistical significant difference in the seroprevalence of HAV antibodies
between children with history of jaundice or contact with a
jaundiced patient and those without (p>0.05). Table 5
shows the comparison between the children of low and
middle SES and those from high SES. Seroprevalence of
HAV antibodies was significantly higher among children
of low and middle SES (85.9%) than among children of
high SES (37.9%) (p<0.001).The proportion of children
with history with symptomatic HAV infection contracted at
10 years of age or older was significantly higher among
children of high SES than among those of very low and
middle SES (p<0.001).
DISCUSSION
This study which is related to the seroprevalence of HAV
is the first one conducted in Ivory Coast. The sample size
has been restricted by financial pressures for the determination of anti-hepatitis A antibodies.The overall prevalence of HAV antibodies was 81.4%. The rate obtained
was similar to those observed in studies conducted in
African countries as Sierra Leone (Hodges et al., 1998)
and Madagascar (Morvan et al., 1994; Raharimanga et
al., 2008). Previous studies have shown that HAV infection in regions with a high endemicity pattern occur
mainly in children under five years old (Khalil et al.,1998)
In addition, studies conducted in developing countries
have described a variation in the endemic pattern of HAV
infection, which has demonstrated a reduction of this
infection in children and an increase among adolescents
and adults (Kaya et al., 2007; Tosun et al., 2004; Tufenkeji 1999). The present study corroborates this endemicity pattern variation, demonstrating a gradual increase
in HAV infection from children. However many recent
reports indicate a global change in seroepidemiological
patterns of hepatitis A infection. In Delhi (India), seroprevalence in people younger than 35 years old was
similar to that of the more developed European countries
(Das et al., 2000). In Thailand, the prevalence of antiHAV was 1.95% in Bangkok and 12.7% in other provinces in people younger than 25 years (Ratanasuwan et
al., 2004).
A history of hepatitis A or of a contact with a case of
hepatitis has been shown to be associated with anti-HAV
seropositivity (Khalil et al., 1998). In the present study, no
statistically significant association was found. While more
than 80% of cases of hepatitis A occurring in children
under 5 years of age are asymptomatic, infected children
without jaundice case still shed the virus and serve as a
source of infection for others (Gendrel 2004). In the
study, children who had history of symptomatic HAV
infection (more contracted infection before 10 years of
age but more than 18% contracted the infection at age
10 years). Tosun et al. (2004) reported a shift of seropositivity from children to adolescents in Turkey, especially in families with average or high SES. In the present study, the majority of low SES children with a history
of symptomatic infection were under 10 years of age
while for children of high SES the majority who gave
068 J. Med. Med. Sci.
Table 2. Seroprevalence of anti-hepatitis A (HAV) antibodies among the children according socio-economic variables.
Tested (N=306)
Anti-HAV positive (N=249) N0 (%)
p
traditional
163
139(85.2)
<0.001*
council flat
98
81(82.6)
villa
45
29(64.4)
under equipped
141
136(96.4)
fairly equipped
128
98(76.5)
very equipped
37
15(40.5)
variables
Type of housing
Environment
<0.001*
Potable water
outside house
20
18(90)
inside house
286
231(80.7)
non hygienic
205
179(90.6)
private toilet with flush
101
70(64.2)
0-3
107
55(51.4)
4-6
139
137(98.5)
7-9
47
45(95.7)
10
13
12(92.3)
university
113
63(55.7)
illiterate
67
66(98.5)
others
126
120(95.2)
university
75
38(50.6)
illiterate
166
142 (85.5)
others
97
69(71.1)
low
194
190(97.9)
middle
83
29
48(57.8)
11(37.9)
<0.005*
Sewage disposal
<0.001*
Number of siblings
<0.001*
Father’s education
<0.005*
Mother’s education
<0.02*
SES
high
<0.001*
Under, fairly and very equipped environment were identified according to the level of public equipment (asphalted road, regular
collecting of refuse, gutter stone, etc…) .The economic status (ES) were performed by the Ministry of the Planification according to the
monthly income of the parents, high (>1600 $US), middle (400-1600 $US) and low (<400 $US). *Significant value. Others (father’s and
mother’s education): primary and secondary
history of symptomatic infection was aged 10 years.
Children who got symptomatic infection above age of 10
years reported severe form of symptoms compared to
younger children. Previous authors reported that the
severity of HAV illness increases with age (Arguedas and
Fallon, 2004; Chatproedprai et al., 2007; Jacobsen et al.,
2004).
Hawkes et al (1981) reported a significantly higher HAV
seroprevalence rate in boys. In the present study, there is
not a difference related sex with HAV seroprevalence.
The results obtained were in agreements with previous
Yessé
et al. 069
Table 3. Multiple logistic analysis identifying risk factors significant predictive of hepatitis A virus seropositivity.
variables
Potable water
inside house
outside house
Sewage disposal
private toilet with flush
non hygienic disposal
% 95 confidence interval
lower border
upper border
Odds ratio
3.2
1.1
2.5
10.4
1.2
4.8
p
<0.01*
<0.05*
*significant value
Table 4. Seroprevalence of anti-hepatitis A virus antibodies in relation to history of hepatitis and liver activity.
variables
History of jaundice
Yes
No
Tested (N=306) N0 (%)
Anti-HAV positive (N=249) N0 (%)
p
49 (16.0)
257 (84.0)
37 (14.8)
212 (85.2)
0.25
97 (31.7)
209 (68.3)
74 (76.2)
175 (83.7)
0.11
294 (96.1)
12 (3.9)
239 (96.0)
10 (4.0)
0.84
contact with jaundiced persons
Yes
No
Serum ALT
40
>40
ALAT: alanine transaminase
Table 5. Seroprevalence and history of symptomatic hepatitis A virus infection according to socioeconomic status
variables
HAV seroprevalence
Positive
Negative
History symptomatic HAV
infection, age contracted
<10 years
10 years
Low and Middle Socioeconomic
status (N=277) N0 (%)
High Socioeconomic
status (N=29) N0 (%)
p
238 (85.9)
39 (14.1)
11 (37.9)
18 (62.1)
<0.0
01*
33 (89.1)
4 (10.9)
2 (22.2)
7 (77.8)
<0.0
01*
*Significant value
investigators (Das et al., 2000; Vancelik et al., 2006).
Several previous studies showed a clear inverse correlation between exposure to HAV and socioeconomic
level. It is well known that HAV infection is strongly correlated with poverty and inadequate sanitation. Increasing
household income, education, water quality and quantity,
sanitation, and hygiene lead to decreased HAV prevalence (Salama et al 2007; Zago-Gomes et al., 2005).
The factors such as the area of residence, economic
status (ES), number of siblings, type of housing which reflect the socioeconomic status and hygiene conditions of
a population, were significantly associated with HAV seroprevalence rates. In previous epidemiologic studies conducted on HAV seroprevalence, the same risk factors
were found (Erdogan et al., 2004; Kaya et al., 2007;
Zago-Gomes et al., 2005). The results obtained showed
that the education level of parents was significantly correlated with HAV seroprevalence, reaching 31.8% in children with parents who had a university education versus
65.3% in those with less education. This finding was reported by previous studies (Khalil et al., 1998).
Hepatitis A virus (HAV) is a health problem in countries
where seroepidemiology shows changes from hyperendemicity to intermediate endemicity. Then, there are
different patterns with area of low prevalence; some studies indicate a decline of anti-HAV prevalence among
urban children and the possibility of an outbreak of HAV
infection among this population. The infection is predicted
to shift to adulthood with more severe clinical
manifestation in the future. Then it is important to
determine the pattern of hepatitis A virus infection in each
community in order to optimize vaccination strategies:
070 J. Med. Med. Sci.
high risk population for vaccination should be identified
(Andre et al., 2002; Jacobsen et al., 2004). In Côte
d’Ivoire, this study showed that there are different patterns among children. Children of high SES were more
likely to be vulnerable to infection in adolescence than
those of low SES.
In conclusion, the results of this study suggest that the
seroprevalence of HAV among children of Abidjan remains relatively high. However a minority of the population, made up of children who live in high socioeconomic environment, remains vulnerable to the HAV,
according to the rate of immunization. In addition to continuous improvement of hygiene and socio-economic
con-ditions, the mass vaccination as recommended by
the WHO (Andre et al., 2002), should be implemented in
the vulnerable child population.
ACKNOWLEDGEMENTS
We are grateful for Institut Pasteur d’Abidjan-Cocody for
their advice and technical supports. We acknowledge the
children and parents who participated in this research.
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