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Brief Reports

Indian Pediatrics 2002; 39:936-941 

Prevalence of Hepatitis A in Children and Adolescents in Adana, Turkey


Hacer Yapicioglu, Emre Alhan+, Dincer Yildizdas, Akgun Yaman* and
Nafiz Bozdemir+

From the Departments of Pediatrics, *Microbiology and +Family Medicine of Cukurova University, Faculty of Medicine, Adana, Turkey.

Correspondence to: Dr. Hacer Yapicioglu, Departments of Pediatrics, Cukurova University, Faculty of Medicine, 01330 Adana, Turkey.

Manuscript received: December 4, 2001; Initial review completed: January 21, 2002;

Revision accepted: April 10, 2002.

 

The present study was aimed at determining the seroprevalence of anti-HAV in children and adolescents in the city of Adana, Turkey. The overall prevalence of anti-HAV was 44.4% (316/711). The prevalence increased with advancing age i.e. 28.8% (2.1-6 yr), 49.8% (6.1-12 yr), and 68% (12.1-16.5 yr) (P < 0.0001). Seroprevalence was significantly lower in children less than 6 years and belonging to higher socioeconomic status.

Key words: Hepatitis A, Seroprevalence, Socioeconomic status.

Viral hepatitis is a major health problem in Turkey as in most developing countries. The prevalence of antibodies to hepatitis A virus in general population shows striking geographic differences. Its occurrence and age dependence is determined to a large extent by environmental and socioeconomic conditions. With economic development and consequent improvements in the levels of sanitation and quality of water supply, there is a shift in the peak age of infection from childhood to adulthood(1). In this study, we aimed to determine the anti-HAV seroprevalence and the factors affecting it in children and adolescents of different age groups and socioeconomic status (SES) in Adana, a city in southern Turkey.

Subjects and Methods

Adana is an industrialized city in southern Turkey with a population about one million and five hundred thousands. The study was carried out in children and adolescents of three SES groups as low, middle and high.

Sampling procedures: There are 93 districts in the city of Adana. These were categorized as high, middle or low SES districts according to the infrastructural and the estimated socioeconomic levels of their inhabitants. One district was selected from each of three groups based on the stratified cluster sampling method and three streets were selected randomly from each selected district based on the random numbers table.

Socioeconomic level of the families was determined by taking into account their household items and several sources on socioeconomic structure of Turkey(2). A questionnaire was filled by parents which included the parents’ jobs, monthly income, parents’ education level, source of drinking water, kind of sewage system, home ownership, if rented how much the rent was, having a car, and the presence of household items (refrigerator, television, washing machine, video, computer, air conditioner). Total score of all these parameters was 24. Mean score was 13.6 ± 3.9 (maximum score was 24, minimum score was 5). The subjects having score between 5-9 were accepted to be as low SES, between 9.1-14 as middle SES and between 14.1-24 as high SES group. In each SES group, subjects were regrouped as preschool (2.1-6 years old), elementary school (6.1-12 years old) and high school (12.1-16.5 years old) level.

Sample size: As the population of children and adolescents was not exactly known, sample size representing children and adolescents in Adana was calculated by the formula (n =(t1-a) (pxq) / S2) using an a of 0.05 and a b of 80%, P of 50%, q of 50%, S of 0.05 and t1-a of 95%(3). According to the formula, it was estimated that blood samples had to be taken from at least 600 subjects.

Blood samples were obtained between October 1st and November 30th 1998. On the first street of the three selected districts, houses were visited randomly and 5 mL of blood was obtained from each child and/or adolescent in the household upon permission of the parents. If the number was not sufficient on the first street, blood was obtained from the subjects on the second and third streets. Serum samples were stored at –20ºC and subsequently tested for anti-HAV. For analysis of the total anti-HAV, AxSYM apparatus (Abbott Laboratories, Illinois, USA) and the MEIA (Microparticle Enzyme Immunoassay) method were used.

Statistical analysis: Data was analyzed using the SPSS-X 6.0 for Windows. Chi-square and and student’s t tests were performed for comparison of independent samples.

Results

The study was carried out in 711 children and adolescents (355 male, 356 female) aged 2.1 to 16.5 years (mean age 8.3 years). There were 104, 329 and 278 subjects in low, middle and high SES groups respectively. The overall prevalence for anti-HAV antibodies was 44.4% (316/711). There was no significant difference with respect to sex (P > 0.05). None of the subjects was vaccinated for HAV. The age specific prevalence of anti-HAVis depicted in Fig. 1. Anti-HAV was detected in 10.6% of children aged 2.1 to 4 years and then rose gradually in the older age groups i.e., 28.8% (2.1-6 yr), 49.8% (6.1-12 yr), and 68% (12.1-16.5 yr) (P < 0.0001).

History of jaundice was obtained in only 9.4% (67/711) of the subjects. While anti-HAV seropositivity was 74.6% (50/67) among these individuals, it was 41.3% (266/644) among those without history of jaundice (P < 0.001). Thus, 84.2% (266/316) of the subjects seropositive for anti-HAV seem to have had asymptomatic HAV infection. Anti-HAV positivity among subjects whose family members had a history of jaundice was found to be higher than in those from families without a history of jaundice (60.4% vs 42%, P < 0.001). Parents’ educational level was inversely associated with the prevalence of anti-HAV in the sense that as the educational level of the parents increased the prevalence decreased (P < 0.0001). The average monthly income of the families was 555 US dollars. Anti-HAV seroprevalence was found to be lower in families with higher monthly income (P < 0.0001) (Table 1).

Table I__ Anti-HAV Seroprevalence Among Children and Adolescents in Relation to Parents’ Education and Monthly Income.

 
Total
Anti-HAV positive
 
n
(%)
n
(%)
Parents education*
<5 years
54
(7.6)
45
(83.0)
Elementary school
276
(38.8)
153
(55.4)
Junior high school
78
(10.9)
31
(39.7)
High school
206
(28.6)
64
(31.1)
University
97
(13.6)
23
(23.7)
Total
711
(100)
316
(44.4)
Monthly income (US $)*
73-215
149
(20.9)
96
(64.4)
216-435
234
(32.9)
108
(46.2)
436-870
181
(25.5)
72
(39.4)
>870
147
(20.7)
40
(27.2)
Total
711
(100)
316
(44.4)
* P < 0.0001 (chi-square test)

There was no difference in anti-HAV seroprevalence in the 2.1-6 year age group with regard to the SES variable (P > 0.05). In the 6.1-12 year age group, the seroprevalence in the high SES group was found to be significantly lower than that of the low SES group (39.6% vs 60%), (P < 0.05). In the 12.1-16.5 year age group, no statistical difference was found between low and middle SES groups (P > 0.05). However, the differences between the low and high SES groups and between the middle and high SES groups were significant (86.9% vs 53.4% and 78.1% vs 53.4%, respectively), (P < 0.005, P < 0.001)) (Fig. 2).

Discussion

Hepatitis A is primarily an infection of childhood and it is mostly asymptomatic in this age group. It follows a severe clinical course in adolescents and adults. Since it is enterically transmitted, it is more commonly seen in lower socioeconomic communities where sanitation and hygienic conditions are poor(1).

In a study carried out on children and adolescents in Italy, a country with low endemicity, the prevalence of anti-HAV among the 3-5, 6-7, 11-12, 14-16 and the 17-19 age groups was determined as 2.3%, 3.9%, 10%, 9.7% and 16.3%, respectively(4). From Delhi, India, Dutta et al. reported the prevalence of anti-HAV as 80% by 5 years of age(5). Seroprevalence of HAV in Turkish adults is reported to be between 75.6% and 100% among adolescents and adults. The anti-HAV seroprevalence was 91.7% in blood donors in Adana(6).

Our results are similar to those observed in the western parts of Turkey, however seropositivity in the eastern provinces is 1.5-2 times greater than our results(7). The difference observed may be due to the different socioeconomic levels between the regions,eastern provinces being poorer.

In this study, when the level of education and income of the parents increased, we observed a significant decrease in anti-HAV seropositivity of the subjects. Similar to our results, Stroffolini et al.(4) in Italy, and Barros et al.(8) in Portugal found a significantly lower anti-HAV seroprevalence in children and adolescents whose parents had a higher level of education. We believe that the children whose parents have a higher education level are more likely to maintain a better hygiene and also the parents being in higher employment stand the chance of raising the welfare level of the family.

 

The 91.8% anti-HAV seroprevalence found in a study conducted on adults in Adana(6) is similar to 86.9% and 78.1% anti-HAVseroprevalence among 12.1-16.5 years old age groups in the low and middle SES. However, the seroprevalence of anti-HAV in the 6.1-12 and 12.1-16.5 years old age children and adolescents among high SES were found to be lower (39.6% and 53.4 %, respectively). In our opinion, the difference is due to the fact that these children from a high socioeconomic level are in schools with better hygienic conditions and their schoolmates also come from high socioeconomic backgrounds. From this result, it is seen that two of every three children in the 6.1-12 years old and one of every two children in the 12.1-16.5 years old with high SES are susceptible to HAV infection. As HAV infection affects these ages severely and as these children live in endemic area, an infection acquired especially during school age and afterwards will lead to irregular attendance at school, and also infection during advanced ages is likely to increase the risk of hospitalization and consequently loss of working hours.

The seroprevalence was found to be much higher in families where the household was crowded. These results highlight the importance of household contact in the spread of HAV(4,8,9). On the other hand, while there was no statistical correlation between anti-HAV positivity and the number of 0-6 years old siblings in the household, as the number of 6.1-12 years old siblings in household increased, so did anti-HAV seropositivity in children. In other studies conducted in this country, anti-HAV positivity among especially elementary school age children was found to be significantly higher compared to the preschool age children(6). A probable reason for this trend could be crowded school atmosphere where interpersonal contact is greater and hence an increase in the risk of infection. Probably, the children who undergo asymptomatic infections carry the infection home and infect other siblings.

To conclude, it was observed that anti-HAV prevalence among children and adolescents from Adana, Turkey increased with age, with higher rates observed among subjects with lower socioeconomic status. It seems that the children and adolescents in low SES develop natural infection or clinical infection itself. In contrast, more subjects from high SES group are susceptible to HAV infection. For this reason, we consider that in our country immunization of the children from high SES may be useful before they start school, i.e. by the age of 6 years.

Acknowledgment

The authors wish to thank Intern Dr. Hakan Evren for his help in data collection.

Contributors: HY designed the study, collected the samples, interpreted the results and drafted the manuscript. EA designed, coordinated and supervised the study, helped in drafting the final paper and he will act as guarantor for the paper. DY helped in collecting the samples and interpreting the results. AY carried out the serologic tests. NB helped in statistical analysis.

Funding: Cukurova University Research Foundation (grant no TF-98 UF).

Competing interests: none stated.

Key Messages

• Hepatitis A infection is high in Turkey and seroprevalence increases with age and higher rates are observed among subjects at lower socioeconomic status.

• Children from high socioeconomic status are susceptible to HAV infection. Immunization of the children from high socioeconomic status may be useful before they start school.

 

 

 References


1. Battegay M, Gust ID, Feinstone SM. Hepatitis A Virus. In: Principles and Practice of Infectious Diseases, 4th edn. Eds. Mandell GL, Bennett JE, Dolin RN. New York, Churchill Livingstone, 1995; pp 1636-1656.

2. Atalay B, Kantas M, Beyazit S. Research of family structure in Turkey. Devlet Planlama Teskilatl (OPT). Sosyal Planlama Genel Mudurlugu, , Yayin No: DTP: 2313-SGPM: 421, Ankara, 1992.

3. Ingelfinger JA, Mosteller F, Thibodean L, Ware JH. Biostatistics in Clinical Medicine, 2nd edn. NY, London, Toronto, Macmillan, 1987.

4. Stroffolini T, Chiaramonte M, Franco E, Rapicetta M, De Mattia D, Mura L, et al. Baseline seroepidemiology of hepatitis A virus infection among children and teenagers in Italy. Infection 1991; 19: 97-100.

5. Dutta AK, Aggarwal A, Kapoor AK, Ray GN, Batra S. Seroepidemiology of hepatitis A in Delhi. Indian J Pediatr 2000; 67: 77-79.

6. Dundar IH, Yaman A, Cetiner S, Kilic NB, Apan TZ. The prevalence of hepatitis markers in specimens from blood donors and randomly selected patients. J Assoc Turk Microbiol; 1994: 24:236-239.

7. Akbulut A, Kilic FS, Felek S. The prevalance of Hepatitis A in the Elazig region. Turk J Med Sci 1996; 26: 375-378.

8. Barros H, Oliveir F, Miranda H. A survey on hepatitis A in Portuguese children and adolescents. J Viral Hepat 1999; 6: 249-253.

9. Minuk GY, Ding LX, Hannon C, Sekla L. The risks of transmission of acute hepatitis A and B virus infection in an urban centre. J Hepatol 1994; 21:118-121.

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