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| ABSTRACT |
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| INTRODUCTION |
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In industrialized countries, which are characterized by a low endemicity pattern, prevalence is low during childhood, but the non-immune adult population (seroprevalence ranges from 13% to 50% in adults)2,46 is exposed to epidemics and severe forms of hepatitis A, mostly limited to risk groups. In regions of intermediate endemicity where hygiene conditions are variable, seroprevalence in adults varies from 60% to 97%. Young children are usually not infected and infection occurs at a later age in adolescents and young adults, which explains the higher incidence of symptomatic hepatitis.2,57
In developing countries, low economic status, high crowding, and inadequate water treatment contribute to a high endemicity pattern; more than 90% of the population has acquired natural immunity before 10 years of age and often shows asymptomatic forms. In those countries, overt forms of hepatitis A are relatively rare with exceptional severe forms.1,6
The epidemiologic pattern of hepatitis A infection is currently changing in many developing countries where socioeconomic conditions are improving. As a result, these countries no longer demonstrate the epidemiologic characteristics of countries with a high endemicity of hepatitis A and other infectious diseases transmitted via the orofecal route. Studies conducted in such emerging countries have reported epidemiologic changes over the last decades, indicating that hepatitis A affects the population at a later age,3,79 drawing these countries closer to those with intermediate endemicity with an increased risk of symptomatic, potentially more severe disease forms that occur in older individuals.
In Tunisia, epidemiologic data on HAV are fragmentary and limited to studies on acute symptomatic hepatitis A infection. In the 1970s and 1980s, such studies showed a high endemicity of hepatitis A at a maximum age of 510 years, with a higher frequency pattern in fall.10 Serologic diagnosis has recently been used more widely in this country, and an incidence rate of 11.9/100,000 inhabitants was reported in 1998, although this figure is most likely an underestimate.11 No age-specific seroprevalence data are currently available in Tunisia. The aim of this study was to determine the age-specific seroprevalence of HAV in a young population according to socioeconomic status, and to detect a likely change in the epidemiology of infection.
| SUBJECTS AND METHODS |
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The targeted population included children and those 523 years old in elementary and secondary schools of the private and public sectors in the governorate of Sousse during the school year of 20012002. This study population constituted a representative sample of school children.
Two-stage cluster sampling was used for random selection of institutions and classes that was proportional to the number of school children in each institution. In the first stage, we sampled schools; in the second stage, we sampled classes from these schools. Sample size calculation was based on a 50% HAV seroprevalence estimation with a 2% precision rate and a 95% confidence level. The formula for sample size determination yielded a total of 2,400 school children. As regards urbanization level, Distribution of schools in various regions was taken into account during sampling. School children were allocated to three groups according to their school location: 1) urban area: children from schools in the city of Sousse, 2) suburban area: children from schools in municipal areas, and 3) rural area: children from school in non-municipal areas.
Collected data. Data collected included general information on school children (age, sex, educational level, and socioeconomic characteristics that included the number of siblings, type of residence, source of water supply, and waste water sewage) and their parents (origin, educational level, occupation, social insurance coverage). Participants were allocated to three age groups: 59 years, 1015 years, and > 15 years. Housing was classified as modern in the case of a villa and old in the case of an apartment or traditional house. Based on educational level, parents were allocated into either group 1 (university level) or group 2 (other).
Data collection method. Epidemiologic data were collected from questionnaires and health files from school medical records. After informed consent was obtained from parents, blood samples were collected from school children for HAV serology. This study was conducted as part of collaboration between the Infectious Diseases, Epidemiology and Virology departments of the University Hospital Farhat Hached and the School Health Department. Four school physicians were involved with completion of questionnaires, and blood samples were obtained by four nurses, all with previous experience with a pediatric population. Serum samples were tested for IgG antibodies to HAV by a qualitative enzyme-linked immunosorbent assay (ETI-AB-HAVK-3; Diasorin, Stillwater, MN). Results were read on a multimode plate reader and results were compared with the optical densities of positive and negative controls.
Statistical analysis. Data were analyzed, using SPSS version 9.0 software (SPSS, Inc., Chicago, IL). A descriptive analysis was followed by bivariate analysis using a chi-square test for comparison of the various sub-groups with a 5% statistical significance level. A multivariate analysis with logistic regression was used to determine predictors variables associated with seroprevalence among the significant factors found by bivariate analysis. Odds ratios and 95% confidence intervals were calculated presented for these variables.
| RESULTS |
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The overall prevalence of antibodies to HAV was 60% and was significantly correlated with the age and origin of participants. It was 44.2% in children < 10 years old and increased to 83% among those > 15 years old (Table 1
). Antibodies to HAV were found in 89.9% of school children from rural areas, 69.1% from suburban areas, and 39.7% from the city of Sousse; their age distribution is shown in Table 2
. In some schools in central Sousse, the seroprevalence of HAV ranged from 5.5% to 11% in children < 12 years old and from 30% to 50% in those > 15 years old. In rural areas, seroprevalence was 100% in those 10 years old in some schools. Besides age and origin, other variables significantly associated with HAV seroprevalence included source of drinking water, waste water sewage, number of people living in the same housing, type of housing, and education level of parents (Table 1
). Multivariate analysis confirmed the specific effects of the residence of school children and source of drinking water. These two factors were independent of age, type of housing, and number of persons per household (Table 3
).
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| DISCUSSION |
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90% at 10 years of age.2 This increase in HAV seroprevalence with age has also been found in India,9 southern Taiwan,8 and in Mexican adolescents who emigrated to the United States who showed an increase in HAV seroprevalence from 34% in five-year-old children to 81% in those > 14 years of age.13 Improvement of hygiene and socioeconomic conditions has undoubtedly contributed to this epidemiologic shift. However, seroprevalence rates are still more elevated than those reported in European countries, where HAV seroprevalence rates do not exceed 25% in adolescents (Table 4
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Significant sex differences, such as the slightly higher seroprevalence in females observed in our study, have not been reported by other investigators.9,13,17,18 However, Hawkes and others reported a significantly higher HAV seroprevalence rate in boys 46 years of age.19
We have shown that the education level of parents was significantly correlated with HAV seroprevalence, reaching 42.4% in school children with parents with a university education versus 65.9% in those with less education. This finding was previously reported by Stroffolini and others.15
In conclusion, the results of this study suggest that HAV epidemiology has changed in Tunisia from a high to an intermediate endemicity pattern. Preventive activities should be adapted to this epidemiologic shift, which has left an increasing proportion of non-immune adults unprotected with a high risk of severe hepatitis A20 with serious public health consequences. In addition to continued improvement of hygiene and socioeconomic conditions, mass vaccination as recommended by the World Health Organization21 in areas of intermediate endemicity should be implemented in Tunisia.
Received August 11, 2004. Accepted for publication January 22, 2005.
Acknowledgments: We thank Dr. Veronique Delpire for her editorial contribution to this manuscript. The American Committee on Clinical Tropical Medicine and Travelers Health (ACCTMTH) assisted with publication expenses.
* Address correspondence to Dr. Amel Letaief, Department of Internal Medicine and Infectious Diseases Unit, University Hospital Farhat Hached, Sousse 4000, Tunisia. E-mail: amel.lataief{at}famso.rnu.tn ![]()
Authors addresses: Amel Letaief, Nawfal Kaabia, and Letaief Jemni, Department of Internal Medicine and Infectious Diseases Unit, University Hospital Farhat Hached, Sousse 4000, Tunisia, Telephone/Fax: 216-73-211-183, E-mail: amel.letaief{at}famso.rnu.tn. Rafika Gaha, School Health Department, Sousse 4000, Tunisia, Telephone: 216-73-221-411, Fax: 216-73-226-702. Amel Bousaadia and Fatma Lazrag, School Health and Regional Health Department, Sousse 4000, Tunisia, Telephone: 216-73-221-411, Fax: 216-73-226-702. Halim Trabelsi, Microbiology Unit, University Hospital Farhat Hached, Sousse 4000, Tunisia, Telephone: 216-73-221-411, Fax: 216-73-226-702. Hassen Ghannem, Department of Epidemiology, University Hospital Farhat Hached, Sousse 4000, Tunisia, Telephone: 216-73-221-411, Fax: 216-73-226-702.
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