Seroepidemiological study of Helicobacter pylori infection in South African children

TRANSACTIONS

OFTHE

ROYAL

SOCIETY

Seroepidemiological children

OFTROPICAL

MEDICINE

AND

study of Helicobacterpylori

HYGIENE

(1997) 91,393-395

infection

M. A. Satharl, E. Gouw&, A. E. Simjee’ and A. M. Mayat ‘Gastrointestinal 2Centre for Epidemiological Research, Medical Research Council, Durban, South Afica

393

in South African

Unit, Department of Medicine and

Abstract The seroepidemiology of Helicobacterpylori infection was studied in 68 1 randomly selected Black children from newborn to 13 years of age (333 boys, mean age 8.05 years, and 348 girls, mean age 7.76 years) in KwaZuluJNatal, South Africa. H. pylori infection was identified serologically using an enzyme-linked immunosorbent assay to detect the presence of immunoglobulin G against H. pylori. Demographic information collected included age, gender, family income, overcrowding, educational level, and possession of domestic pets. The seroprevalence of H. pylori infection was compared to a known faecal-orally transmitted infection, hepatitis A virus (HAV); 66% of the children were seropositive forH. pylori. There was an age-specific increase in H. pylori infection, with more than 80% of children being infected by the age of 10 years. There was no significant difference (-0.338) in the seropositivity of H. pylori infection between boys (68%) and girls (64%), nor was there any significant difference in H. pyloriinfection related to pets, level of parents’ education, crowding, and income, by either univariate or multivariate analysis. However, there was a significant association (P
Address for correspondence: Mr M. A. Sathar, Gastrointestinal Unit, l?O. Box 17039, Congella, 4013, South Africa; phone +27 31 360 3522, fax +27 31 253 832.

factors. We also compared the seroprevalence of H. pylori infection with a known faecal-orally transmitted infection, HAV. Patients and Methods Study site The study was done in Umlazi, a dormitory township of metronolitan Durban in the nrovince of KwaZulu! Natal, S&h Africa. Umlazi has-a ‘third world’ demographic profile and consists predominantly of one Black population group. Running water is available in many of the established homes but not in the squatter communities. There is a lack of adequate disposal of faeces. Study population Sera were obtained from 681 children from newborn to 13 years of age, including 333 boys (mean age: 8.05 years) and 348 girls (mean age: 7.76 years), divided into aliquots and stored at -80°C during a previous study of the prevalence and transmission patterns of hepatitis B virus in South African children (IiBDOOL &UXIM et al., 1988, 1991). The method of sampling has been described elsewhere L4BDOOL KARIM et al., 1988. 199 1). Briefly, schoolchildren aged 6-l 3 years f;om 1d schools in Umlazi were selected randomly in proportion to total school attendance; children aged l-6 years were selected by sequential random sampling from every 17th household in 6 different sections of Umlazi; and infants from newborn up to one year old were randomly selected from 7 Umlazi clinics in proportion to clinic attendance. A questionnaire obtained detailed information, including sociodemoaravhic data, which was considered to be important-in-the epidemiology of H. pyZori from each individual. The data included narents’ educational level and occupation, pets at horn;, attendance at day care centres, age, gender, and overcrowding (total number of people in the household, number of rooms, and number of people per room). Serology Immunoglobulin G (IaG) antibodies to HAV were measured by means of a-commercially available radioimmunoassav (Abbott Laboratories. Chicaeo. Illinois. USA). H. pylon’ IgG antibodies were measured by a commercially available enzyme-liked immunosorbent assay (ELISA) (PyloriStatTM, Whittaker Bioproducts, Wakersille, Maryland, USA), by linear regression analysis using 3 standards and 2 controls. The sensitivity and specificity of the assay have been described elsewhere (SATHAR et al., 1991).

M. A. SATHAR ETAL.

394

Statistical analysis x2 or t tests were used to assess univariate associations between H. pylon’ and possible risk factors. In addition, multiple logistic regression was performed to determine which factors contributed independently to the presence of H. pylon’. The relationship between H. pylon’ and HAV infection was adjusted for age, and age-adjusted odds ratios (ORs) and 95% confidence intervals (95% CIs) were calculated.

HAV infection were independently associated with age-i.e., the seropositivity rate of both increased with an increase in age. Hence age appeared to be a significant confounding factor. However, adjusting for age using logistic regression caused this apparent association to disappear. The risk of HAV seropositive children being H. pylon’ seropositive was not significantly greater than that of HAV seronegative children in each age group (ORz1.018, 95% CI 0.66-1.58).

Results Four hundred and forty-eight of 681 children tested (66%) were seropositive for H. pylon’. There was an agespecific increase in the prevalence of H. pylon’ infection, with seropositivity rates of 50% (908) in newborn-5 months old infants, 29% (8/28) in 6-l 1 months old infants, and 85% (55/64) in those aged 9-10 years. The association between age and H. pylori was highly significant (P
Discussion Our results showed that H. pylori infection was very common and the initial infection was acquired in early childhood. The 50% seropositivity rate in infants under 6 months of age found in this study was similar to that reported by HOLCOMRE et al. (1992). This high seroprevalence at birth indicates high prevalence in the mothers and the subsequent drop in seropositivity could be attributed to the natural regression of maternally acquired H. pyZori IgG antibodies. From the age of 6 months the ambulatory child comes into intimate contact with its environment and other children, as well as with adults in whom the prevalence of infection is known to be high (SATHAR et al., 1994a), and their seropositivity rate increased after the age of 12 months. Several studies have confirmed that the prevalence of H. pyloriis influenced by conditions at childhood (h&NDALL et al., 1992; ~~I-ICHELL et al., 1992; PATEL et al., 1994). In developed countries, prevalence of H. pyZori was higher if there was more than one person per room in the family home during childhood, if a bed was shared, or if there was no hot water in the house (MENDALL et al., 1992). In Peru, higher socioeconomic status and indoor plumbing were not protective if children drank water from a municipal supply; water obtained from a private well with indoor plumbing decreased their chances for acquiring H. pylori infection (KLEIN et al., 199 1). Although we were unable to show any significant association between H. pylori and the sociodemoindicators measured, family income, graphic educational level, socioeconomic status, and housing density have been shown to be associated with the prevalence of H. pylon’ (see LOUW et aL, 1993). KwaZuWNatal, one of 9 provinces of South Africa, is home to 20% of South Africa’s population with 7.9 million inhabitants, 81% of whom are Black (ANONYMOUS, 199 1). Black persons in KwaZulu/Natal earn the lowest average annual income per caput in South Africa ( 18 1 296 rand, equivalent to less than E350). Of the total population of South Africa, KwaZulu/Natal has the highest illiteracy rate (27.8%) and the highest number of people per household (7.14) (.&ONyMOUS, 199 1). The prevalence of HAV infection reflects the degree of socioeconomic development of a community (SATHAR et al., 1994b). The high prevalence of HAV infection in children in our study population confirms the inadequate sanitation and water supply, poor hygiene and overcrowded living conditions prevalent in this community. The significant association between HAV and H. pylon’ is indirect evidence that transmission of H. pylon’ may be by the faecal-oral route. It could be speculated that HAV antibodies in mothers are present at a lower level than H. pylori antibodies, which are kept high by chronic H. pylotiinfection. As a result, whilst the child’s HAV antibodies are undetectable by 6-l 1 months, H. pylon’ antibodies take longer to decline to undetectable levels. Infants aged 6-l 1 months become infected with H. pylon earlier than with HAV, even though the subsequent increase in the rate of acquisition is less steep. If this is true, it may suggest different modes of transmission for HAV and H. pylori. Improvements in hygiene, living conditions and public amenities have resulted in H. pylon’ infection becoming less prevalent (EUROGAST STUDY GROUP, 1993); a definite cohort effect has been demonstrated, implying that the infection is becoming less frequent in those

Table 1. Possible with

Helicobacter

risk factors and their pylori infection

association

No. of subjects

Percentage seropositive

329

52.0 63.0 45.7 59.8 68.0 64.0

Risk factor Possession of pets Attendance

at creche

Gender

Yes No Yes No Male Female

Table 2. Overcrowding level as possible risk fylori infection

34;; 36;; 348

and parents’ educational factors for Helicobacter H. pylori infection Seropositive Seronegative

Factor Crowding (no. of persons per room)a Parents’ educational level (years)a

2.3f 1.4

2*3f 1.25

6,45+ 2.48

6.62+ 2.7

aMeansfstandard errors.

100. 80. z 0 B z 2

so. 40. 20.

.._~._._ O-6 6-11 Months

1

2

3

4

5

.

.

.

.

.

.

.

-

6

7

8

0

10

11

12

13

Age (years)

Figure. Seroprevalence of H. pylori (broken line) and hepatitis A virus (continuous line) in Black South African children.

SEROEPIDEMIOLOGY

OF HELICOBACTER

395

PYLORI

populations whose socioeconomic conditions have immoved. In the maioritv of Black South Africans. in bhom H. pylori and’ eV infections are prevalent,‘the condition is asymptomatic and the community has more pressing social and health care problems. Improving living conditions in early childhood would limit the chances of faecal-oral transmission and decrease the prevalence of infection with H. pylon’. Acknowledgements Financial support for the study was obtained from the University of Natal Medical School Research Fund and the South African Medical Research Council. We acknowledge the assistance of Dr S. S. Abdool-Karim of the Centre for Epidemiological Research, South African Medical Research Council. We thank the Medical Sunerintendent of Kine Edward VIII Hospital, Durban, for his permission to publish: References Anonymous (1991). Population cen~r4s 1991. Pretoria, South Africa: Central Statistical Services, report no. 03/01/00. Abdool Karim, S. S., Coovadia, H. M., Windsor, I. M., Thejpal, R., van den Ende, J. & Fouche, A. (1988). The prevalence and transmission of hepatitis B virus infection in urban, rural and institutionalized Black children of Natal/ KwaZulu, South Africa. International Journal of Epidemiology, 17,168-173. Abdool Karim, S. S., Thejpal, R. & Coovadia, H. M. (1991). Household clustering and intrahousehold transmission patterns of hepatitis B virus infection in South Africa. ZnternationalJourna1 of Epidemiology, 20,495-503. Bamford, K. B., Bickley, J., Collins, J. S. A., Johnston, B. T, Potts, S., Boston,V., Owen, R. J. & Sloan, J. M. (1993). Hehcobacterpylori: comparison of DNA fingerprints provides evidence for intrafamilial infection. Gut, 34,1348-1350. Eurogast Study Group (1993). Epidemiology of, and risk factors for, Helicobacter pylori infection among 3194 asymptomatic subjects in 17 populations. Gut, 34, 1672-1676. Ferguson, D. A., Li, C., Patel, N. R., Mayberry, W. R., Chi, D. S. &Thomas, E. (1993). Isolation of Helicobacterpylorifrom saliva. Journal of Clinical MicrobioZogy, 31, 2802-2804. Holcombe, C., Lucas, S. B., Umar, H. & Abba, A. (1990). Helicobacter (=Campylobacter) pylori in Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene, 84, 294-296. Holcombe, C., Omotara, B. A., Eldridge, J. & Jones, D. M. ( 1992). Helicobacter pylori, the most common bacterial infection in Africa: a random serological study. American 3ournal of Gastroenterology, 87,28-30. Holcombe, C.,Tsimiri, S., Eldridge, J. & Jones, D. M. (1993). Prevalence of antibody to Helicobacter pylori in children in northern Nigeria. Transactions of the Royal Society of Tropical Medicine and Hygiene, 87, 19-2 1. Kelly, S. M., Pitcher, M. C. L., Farmery, S. M. & Gibson, G. RI (1994). Isolation of Helicobacter pyjori from faeces of patients with dyspepsia in the United Kingdom. Gastroenterology, 107,167 1-1674.

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1996; revised 17 February 18 February 1997

1997; ac-