• View in gallery

    Map of northern Borneo showing the three sites within Sarawak from which subjects were recruited in the present study.

  • View in gallery

    Detailed map showing the settlements in the remote Limbang region (Long Napir, Long Balau, Rumah King, Long Sulong, and Long Rayeh) accessed in the present study.

  • View in gallery

    Detailed map showing the settlements in Mulu (Long Iman and Batu Bungan) accessed in the present study.

  • View in gallery

    Detailed map showing the settlements near Belaga village (Sungai Asap, Long Ketueh, and Long Urun) accessed in the present study.

  • View in gallery

    Prevalence by age of carriage of Helicobacter pylori antigen in stool in the total sample. The lower panel shows prevalence in subjects 0–10 years old subdivided into two-year groups. The numbers of subjects in each group are shown by the figures at the base of each bar.

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    Suerbaum S, Michetti P, 2002. Helicobacter pylori infection. N Engl J Med 347 :1175–1186.

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    Frenck RW, Clemens J, 2003. Helicobacter in the developing world. Microbes Infect 5 :705–713.

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PREVALENCE AND PREDICTORS OF HELICOBACTER PYLORI INFECTION IN CHILDREN AND ADULTS FROM THE PENAN ETHNIC MINORITY OF MALAYSIAN BORNEO

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  • 1 Faculty of Medicine and Health Sciences, Universiti Malaysia Sarawak, Kuching, Malaysia; University of Western Australia, School of Medicine and Pharmacology, Fremantle Hospital, Fremantle, Australia

To determine the prevalence of Helicobacter pylori antigen carriage in stool in the Penan ethnic minority in Malaysian Borneo, we studied 295 Penans 0.6–89.0 years of age from 1) the remote Limbang Division, 2) Mulu regional center, and 3) Belaga village. Overall, 37.7% of the subjects tested positive. Peak prevalence was reached by 10 years of age. There were no differences in age, sex, body mass index, and socioeconomic/domestic variables between antigen-positive and antigen-negative subjects. In a logistic regression analysis, subjects from Limbang were least likely to be antigen-positive (odds ratio [OR] = 0.23, 95% confidence interval [CI] = 0.12–0.44 versus other sites, P < 0.001). Availability of a flushing toilet was protective against H. pylori carriage (OR = 0.51, 95% CI = 0.27–0.95, P = 0.031). Infection with H. pylori among the Penan was less than reported in other low socioeconomic groups. The lowest prevalence in the most remote setting suggests that the infection has been a recent arrival in previously isolated communities.

INTRODUCTION

Although infection with Helicobacter pylori is a global health problem, developing countries have generally higher rates of H. pylori carriage than those found in industrialized countries, especially in children.1–4 This difference reflects socioeconomic factors including large families, crowded living conditions, and poor sanitation,5–8 but ethnicity may contribute independently.8,9 There are limited epidemiologic data from southeast Asia regarding this issue. In a study from Singapore,10 Indian Asians had a higher prevalence of antibodies to H. pylori than either Chinese or Malays with, for example, 43%, 23%, and 20% seropositivity, respectively, in the 11–20-year-old age group. Nevertheless, peninsular Malays appear to have particularly low rates of H. pylori carriage,11 with only 13.5% of symptomatic adult patients referred for upper gastrointestinal endoscopy proving to be seropositive.12 It could be argued that these southeast Asian studies have involved subjects from relatively wealthy communities, while there are other minority ethnic groups in the region that do not enjoy the same standard of living and might therefore be at greater risk of H. pylori infection.

The Penan minority were, until relatively recently, jungle nomads living in Malaysian Borneo.13–15 Most of the estimated 10,500 Penans are now semi-nomadic or live in remote settlements in the interior of Sarawak as part of Malaysian government plans to facilitate assimilation. Those who are settled are hunter-gatherers and subsistence farmers whose families inhabit crowded single-room longhouses. Illiteracy rates remain high, and understanding of personal hygiene and sanitation has been rudimentary. Property is largely shared and this extends to cooking and eating implements. Because their communities are in remote areas, health care is basic and treatment is commonly through medicinal plant extracts. Access to antibiotics has been limited. As with other poor communities in developing countries, the conditions under which the Penan live could foster the spread of H. pylori infection.

A major barrier to obtaining H. pylori prevalence data from remote communities is a lack of facilities for obtaining and processing laboratory samples including gastric biopsies and even sera. The recent development of stool antigen testing has provided a robust and convenient method of H. pylori screening that has acceptable sensitivity and specificity compared with established techniques.16–18 We have used this method to conduct the first cross-sectional study of H. pylori infection in Penan communities in Malaysian Borneo.

SUBJECTS AND METHODS

Subjects.

We studied individuals from the Penan ethnic group recruited from two districts within the state of Sarawak, namely Limbang Division in northeastern Sarawak and Bintulu Division in the hinterland of central Sarawak (Figure 1). Within the Limbang Division, we recruited subjects from either 1) communities living in the area surrounding the regional center of Mulu, or 2) from communities in the more mountainous and remote areas. In the case of Bintulu, we studied subjects living close to the village of Belaga. These sites were selected as being representative of major Penan communities living in Government-built long-house settlements. Access to the communities was only possible by jungle trails or rivers.

In the remote Limbang region (Figure 2), settlements at Long Napir (~17 families), Long Balau (~20 families), Rumah King (~7 families), Long Sulong (~5 families), and Long Rayeh (~8 families) were visited. Long Napir, the most readily accessible of these settlements, is four hours by air/ four-wheel-drive vehicle from Kuching. The remaining four settlements are an additional 1–3 hours away by four-wheel-drive vehicle/walking trail. In the case of Mulu (Figure 3), Long Iman (~32 families) and Batu Bungan (~20 families) in Mulu National Park were accessed by air/four-wheel-drive vehicle/boat/walking trail. These settlements were 2.5–3.5 hours from Kuching. For the Belaga region (Figure 4), the settlements Sungai Asap (~35 families), Long Ketueh (~32 families), and Long Urun (~6 families) were 2.5–6 hours from Kuching by air/four-wheel-drive vehicle.

Subjects were identified through village elders (who approved the study) and local medical assistants. We conducted three screening periods of up to seven days during 2001 and 2002, and Penans resident in the communities during these periods were recruited. Because of problems with literacy, verbal informed consent was obtained after explanation of study procedures and children were recruited only after parental consent was given. The study was reviewed and approved by the Universiti Malaysia Sarawak Faculty of Medicine and Health Sciences Research and Ethics Committee.

Methods.

A detailed questionnaire was administered to each subject through a Penan interpreter. The questionnaire included 1) age and sex; 2) employment status, educational level, and family income; 3) accommodation type, including number of resident family members, number of rooms, access to water and electricity, and toilet facilities; 4) history of smoking, diabetes, and other vascular risk factors; and 5) gastrointestinal symptoms (anorexia, nausea, vomiting, epigastric pain, epigastric reflux, abdominal distension, hematemesis and melena, weight loss, and previous endoscopies).

Height and weight were measured and the body mass index (BMI) was calculated. All stool samples for a H. pylori antigen assay were collected into airtight sterile containers that were put immediately in ice. The ice was replenished as necessary in settlements and major centers during transportation. The maximum times from when the stool samples were placed in ice and then transferred to freezer storage at −20°C in Kuching were 24 hours for Mulu and 36 hours for both Belaga and the remote Limbang region. Sample handling was therefore in accordance with that recommended by the assay manufacturer (Meridian Diagnostics, Inc., Cincinnati, OH).

Each stool sample was tested for the presence of H. pylori antigen using a commercially available enzyme-linked immunosorbent assay (ELISA) (Premier Platinum HpSA; Meridian Diagnostics, Inc.). A 5-mm3 aliquot of stool was added to 200 μL of diluent, mixed in a vortex, and 50 μL of the resultant suspension was pipetted into an ELISA plate well containing enzyme conjugate. After incubation and drainage, each well was washed five times with buffer and substrate was added. After further incubation, the reaction was terminated by acidification and the plates were read spectrophotometrically at a wavelength of 450 nm.

Statistical analysis was performed using the computer package SPSS for Windows version 11.5 (SPSS, Inc., Chicago, IL). Data are presented as proportions, mean ± SD, geometric mean (SD range) or, in the case of variables that did not conform to a normal or log-normal distribution, median (interquartile range). The Student’s t-test was used for comparison of two means, Fisher’s exact test for two proportions, and the chi-square test for multiple proportions. Two-group non-parametric comparisons were made by the Mann-Whitney U test. Comparison of multiple groups was done by analysis of variance and the Scheffé post-hoc test. Linear and logistic regression were used to assess independent associations between variables. A two-tailed significance level of P < 0.05 was used throughout.

RESULTS

Subject characteristics.

We recruited 295 subjects ranging in age from 7 months to 89.0 years. There were approximately equal numbers of males and females (50.2% males). The majority of subjects were from families with more than five members (52.8%) and lived in single-room communal long-houses (58.0%). Most had access to electricity (56.9%), a piped water supply (58.7%), and septic tank toilet facilities (70.5%). Of the 124 subjects more than 18 years old, 31.5% were current smokers while only 2.5% of those < 18 years old smoked. There was only one case of diabetes in the sample.

Prevalence of H. pylori antigen in stool.

Overall, 37.7% of the subjects tested positive for H. pylori antigen. The age-specific prevalence of H. pylori positivity in the total sample is shown in Figure 5. The peak prevalence was reached in the first few years of life, with a relatively stable prevalence thereafter. This pattern was seen at each of the three sites (data not shown). In univariate comparisons, there were no significant differences in age, sex, or BMI in those who were antigen positive compared with those who were antigen negative (P > 0.30 in each case). In relation to socioeconomic and domestic circumstances, there were no significant differences by H. pylori stool antigen status in educational level (no formal schooling versus some education), income bracket (< Malaysian Ringit (RM) 300/month, equivalent to < US $80/month versus ≥ RM 300/month), residence in a longhouse versus other accommodation, number of household members, or access to piped water, electricity, or septic tank toilet facilities (P > 0.06 in each case). We also examined the relationship between variables relating to gastrointestinal symptoms and history and H. pylori stool antigen status (Table 1). No significant differences were seen (P > 0.07). When we considered subjects less than 14 years old as a separate group, there was no association between antigen status and height, weight, or BMI after adjusting for age (P > 0.25 in each case).

Study site and prevalence of H. pylori antigen in stool.

Because subjects were drawn from different geographic areas, we divided them into three groups based on study site (Limbang, representing the more mountainous and remote areas of the Division, Mulu and Belaga; Table 2). Subjects from Limbang were approximately half as likely to be H. pylori antigen positive compared with the other two groups (P < 0.001, by chi-square test). The subjects from Belaga were significantly older, had a higher BMI, were more likely to be female, and were more likely to be smokers than those at the other two sites (P < 0.05, by Scheffé test). Residence in a longhouse was lowest in Belaga and highest in Mulu, and Belaga subjects were also more likely to have a family income > RM 300/month (P < 0.001, by chi-square test in each case). Access to piped water was greater in Mulu than the other two sites, but septic tank toilets with mechanical or manual flushing were most prevalent in Limbang (P < 0.001, by chi-square test in each case).

Because of the differences in key variables between the communities, we performed a logistic regression analysis with H. pylori positivity as the binary dependent variable and location (Limbang versus Belaga and Mulu), ln(age), sex, BMI, smoking status, household income, residence in a longhouse, and availability of a septic tank toilet as independent variables. There were 267 of 295 subjects with complete data who were included in the model. We excluded access to piped water because this variable was not coded in 65 subjects (approaching one-fourth of the sample). Study site was strongly predictive of H. pylori status (P < 0.001), with an odds ratio (OR) of 0.23 and a 95% confidence interval (CI) of 0.12–0.44 for H. pylori antigen in stool at Limbang relative to the other two sites. Availability of a septic tank toilet was also protective against H. pylori antigen positivity (OR = 0.51, 95% CI = 0.27–0.95, P = 0.031). The other variables were not significant in the model (P > 0.23).

DISCUSSION

The Penan ethnic minority provides a unique group in which to study the prevalence and predictors of H. pylori infection. The Penan people live in relative isolation, are usually domiciled in single-room longhouses, use communal cooking and eating utensils such as bamboo forks, may not have a reliable water supply or toilet facilities, and have limited access to antibiotic therapy that could facilitate eradication of the organism.13–15 We studied Penans living in three different situations. The prevalence of H. pylori antigen positivity was least in those living in the most remote region (the mountainous jungle of the Limbang Division of Sarawak Province), a finding that persisted after adjustment for other possible contributory variables. The 77% lower adjusted prevalence in this setting suggests that H. pylori infection has been a relatively recent arrival, and that earlier integration with other cultures such as Malays and Chinese has occurred at the other two sites. The Malaysian Government has implemented a program of resettlement of Penan communities with provision of basic housing, reliable electricity and water supplies, and sanitation. Interestingly, the Limbang people in the present study had the highest availability of septic tank toilets despite being the most geographically isolated. This proved an independent determinant of the low H. pylori prevalence, albeit relatively minor compared with study site.

The prevalence of H. pylori infection is strongly correlated with socioeconomic status but there are also wide differences between and within countries.1–4 Infection rates > 90% by five years of age have been reported in the developing world.19 Consistent with other studies,1–4 our data from children suggest that the infection is acquired in the first years of life, reaching a prevalence approaching 50% by 10 years of age. We are not aware of any prospective study that has tracked H. pylori prevalence in isolated communities with initially low infection rates, but it is possible that greater numbers of Penan will carry H. pylori in future unless living conditions improve further. Several studies have provided evidence of transmission of H. pylori within families.20,21 Due to the fact that one or both parents were away during the screening of children, we were not able to gather valid data on clustering of antigen carriage within Penan families.

We found that use of septic tank toilets with mechanical or manual flushing had an independent protective association with H. pylori prevalence compared with other methods of fecal waste disposal including pit latrines and defecation directly into the jungle and rivers. This suggests that greater attention to sanitation associated with toilet use led to reduced fecal-oral transmission. Although evidence for fecal-oral transmission of H. pylori is inconsistent,22 acute diarrhea significantly increases fecal shedding of the organism into the environment23 and diarrheal diseases are relatively common in low socioeconomic communities such as the Penan.

Despite detailed questioning relating to the common gastrointestinal manifestations of H. pylori infection, we did not show any association between antigen carriage and symptoms. This is consistent with past studies2 and the fact that the lifetime risk of peptic ulcer disease and gastric malignancy are only 15% and 0.1%, respectively, in infected individuals.24 There is no indication to treat asymptomatic carriers of the organism and, in the case of children,25 screening of those with dyspeptic symptoms using non-invasive tests is not currently recommended. Studies in the literature have not shown a consistent effect of H. pylori infection on growth and development in children,26 and we did not find an association between H. pylori antigen carriage and markers of growth in the subjects in our study who were younger than 14 years of age.

Infections that involve only humans comprise those that can persist in an individual for a prolonged period and those that are infectious only in the acute phase.27 The former exhibit high endemicity and the latter die out quickly. Helicobacter pylori is likely to fall into the first category, especially given the living conditions in Penan communities. This implies that the low prevalence of H. pylori carriage in the remote settlements of the Limbang Division is due to relatively recent introduction of the organism. Consistent with this suggestion, a study of amebic infection in the Orang Asli ethnic minority in Peninsular Malaysia showed a relatively low seroprevalence in an isolated village in the deep jungle compared with that in peri-urban settlements.28

The present study had limitations. Because of logistic problems with communication, transportation, and access, we recruited a convenience rather than a random sample. There was a disproportionate number of children, primarily because adults in Penan communities spend periods away from their settlements gathering food for their families. Even with the services of an interpreter, complete questionnaire data were not always obtainable, especially when children and adolescents were interviewed without their parents being present. Although the detection of H. pylori antigen in stool has a sensitivity and specificity of 90–95%, other tests (such as the urease test and culture of the organism from gastric biopsies) or test combinations may have improved our detection rate.16–18 Nevertheless, these cross-sectional data are the first from such a unique ethnic group and do provide insights into the epidemiology and modes of transmission of H. pylori in the Penan.

Knowledge of the health status of the Penan people is limited. The present study adds to the current knowledge base, but prospective data on H. pylori carriage are required to validate our hypothesis that the more remote Penan communities have been only relatively recently exposed to the organism. In addition, longitudinal data on H. pylori-related clinical events such as peptic ulcer disease, and perhaps also growth and development in children, would allow an assessment of the impact of H. pylori in remote ethnic communities such as the Penan, and highlight situations in which screening and treatment should be considered.

Table 1

Gastrointestinal symptoms classified by Helicobacter pylori test result*

H. pylori negative (n = 183)H. pylori positive (n = 112)
* Values are percentages of subjects in each group.
Epigastric pain
    Any history of pain54.962.2
    Pain relieved by food, milk, antacid42.853.2
    Periodicity of pain21.428.8
    Postprandial pain12.612.6
    Nocturnal pain25.735.1
    Preprandial/hunger pain47.057.7
    Pain radiating through to the back16.418.2
    Aggravated by food19.122.5
    Aggravated by chillies/spices18.615.5
    Duration of pain >30 minutes51.459.8
    Severe pain16.417.0
Anorexia1.60.9
Nausea25.725.9
Abdominal distension7.77.1
Symptoms of esophageal reflux5.56.3
Vomiting20.825.0
History of hematemesis/melena14.316.2
History of gastroscopy2.20.9
Table 2

Details of subjects classified by study site*

LimbangMuluBelaga
* Values are the geometric mean (SD range), mean ± SD, or median [interquartile range] as indicated.
P < 0.05 by analysis of variance or chi-square test.
P < 0.01 by analysis of variance or chi-square test.
§ P < 0.001 by analysis of variance or chi-square test.
Number1429657
Age (years)†13.2 (4.5–39.1)14.0 (4.7–41.5)20.2 (7.5–54.5)
Sex (% males)†53.455.233.3
Body mass index (kg/m2)‡18.1 ± 3.718.4 ± 4.520.2 ± 4.0
Current smokers (%)§10.5051.8
Domiciled in longhouse (%)§53.482.328.1
Number of family members6 [4–7]5 [4–7]6 [4–8]
No formal education (%)61.167.067.9
Monthly family income < RM300 (%)§96.299.074.5
Access to piped water (%)§53.069.456.1
Septic tank toilet (%)§91.254.256.1
Access to electricity (%)55.659.756.1
% Helicobacter pylori positive (%)§25.451.047.4
Figure 1.
Figure 1.

Map of northern Borneo showing the three sites within Sarawak from which subjects were recruited in the present study.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 71, 4; 10.4269/ajtmh.2004.71.444

Figure 2.
Figure 2.

Detailed map showing the settlements in the remote Limbang region (Long Napir, Long Balau, Rumah King, Long Sulong, and Long Rayeh) accessed in the present study.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 71, 4; 10.4269/ajtmh.2004.71.444

Figure 3.
Figure 3.

Detailed map showing the settlements in Mulu (Long Iman and Batu Bungan) accessed in the present study.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 71, 4; 10.4269/ajtmh.2004.71.444

Figure 4.
Figure 4.

Detailed map showing the settlements near Belaga village (Sungai Asap, Long Ketueh, and Long Urun) accessed in the present study.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 71, 4; 10.4269/ajtmh.2004.71.444

Figure 5.
Figure 5.

Prevalence by age of carriage of Helicobacter pylori antigen in stool in the total sample. The lower panel shows prevalence in subjects 0–10 years old subdivided into two-year groups. The numbers of subjects in each group are shown by the figures at the base of each bar.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 71, 4; 10.4269/ajtmh.2004.71.444

Authors’ addresses: Simon Siong Sing Huang, Gastroenterology, Universiti Malaysia Sarawak, 94300 Kota Samarahan, Sarawak, Malaysia, Telephone: 60-82-671-000, Fax: 60-82-672-411, E-mail: sshuang@fhs.unimas.my. Abdul Karim Russ Hassan, Internal Medicine, Universiti Malaysia Sarawak, 94300 Kota Samarahan, Sarawak, Malaysia, E-mail: hakarim@fhs.unimas.my. Keng Ee Choo, Pediatrics, Universiti Malaysia Sarawak, 94300 Kota Samarahan, Sarawak, Malaysia, E-mail: kechoo@fhs.unimas.my. Mohamad Iswandy Ibrahim, Universiti Malaysia Sarawak, 94300 Kota Samarahan, Sarawak, Malaysia. Timothy M. E. Davis, University of Western Australia, School of Medicine and Pharmacology, Fremantle Hospital, PO Box 480, Fremantle, Western Australia 6959, Australia, Telephone: 61-8-9431-3229, Fax: 61-8-9431-2977, E-mail: tdavis@cyllene.uwa.edu.au.

Acknowledgments: We are grateful to the Sarawak State Government, the Sarawak Forestry Department, the Sarawak Health Department, the Penan village headmen, the Penan medical assistants, and all study subjects for their cooperation and assistance during the study. We also thank Amy Lim Ping Ping and Liwan Lasem for help with laboratory procedures and Khatijah Yaman for data entry.

Financial support: The study was supported by Universiti Malaysia Sarawak short-term grants 238 (2000) (29) and 315 (2002) (52).

REFERENCES

  • 1

    Graham DY, 1991. Helicobacter pylori: its epidemiology and its role in duodenal ulcer disease. J Gastroenterol Hepatol 6 :105–113.

  • 2

    Vanderplas Y, 2001. The role of Helicobacter pylori in paediatrics. Current Opinion Infect Dis 14 :315–321.

  • 3

    Suerbaum S, Michetti P, 2002. Helicobacter pylori infection. N Engl J Med 347 :1175–1186.

  • 4

    Frenck RW, Clemens J, 2003. Helicobacter in the developing world. Microbes Infect 5 :705–713.

  • 5

    Malaty HM, Graham DY, 1994. Importance of childhood socioeconomic status on the current prevalence of Helicobacter pylori infection. Gut 35 :742–745.

    • Search Google Scholar
    • Export Citation
  • 6

    Teh BH, Lin JT, Pan WH, Lin SH, Wang LY, Lee TK, Chen CJ, 1994. Seroprevalence and associated risk factors of Helicobacter pylori infection in Taiwan. Anticancer Res 14 :1389–1392.

    • Search Google Scholar
    • Export Citation
  • 7

    Oliviera AMR, Queiroz DMM, Rocha GA, Mendes EN, 1994. Seroprevalence of Helicobacter pylori infection in children of low socioeconomic level in Belo Horizonte, Brazil. Am J Gastroenterol 89 :2201–2204.

    • Search Google Scholar
    • Export Citation
  • 8

    Fraser AG, Scragg R, Metcalf P, McCullough S, Yeates NJ, 1996. Prevalence of Helicobacter pylori infection in different ethnic groups in New Zealand children and adults. Aust N Z J Med 26 :646–651.

    • Search Google Scholar
    • Export Citation
  • 9

    Blecker U, Hauser B, Lanciers S, Peeters S, Suys B, Vandenplas Y, 1993. The prevalence of Helicobacter pylori-positive serology in asymptomatic children. J Pediatr Gastroenterol Nutr 16 :252–256.

    • Search Google Scholar
    • Export Citation
  • 10

    Kang JY, Yeoh KG, Ho KY, Guan R, Lim TP, Quak SH, Wee A, Teo D, Ong TW, 1997. Racial differences in Helicobacter pylori seroprevalence in Singapore: correlation with differences in peptic ulcer frequency. J Gastroenterol Hepatol 12 :655–659.

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Author Notes

Reprint requests: Timothy M. E. Davis, University of Western Australia, School of Medicine and Pharmacology, Fremantle Hospital, PO Box 480, Fremantle, Western Australia 6959, Australia.
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