Intestinal parasitism in Malayan aborigines (Orang Asli)*

Bull. Org. mond. Sant) 1972, 46, 99-113 Bull. Wid Hlthi Org. Intestinal parasitism in Malayan aborigines (Orang Asli) * F. L. DUNN 1 Surveys were conducted in the southern Malay peninsula to assess intestinal parasitism in the aboriginal ethnic minority groups. Faecal specimens from 1 273 persons were examined by the thiomersal-iodine-formol direct-smear technique. Prevalences are reported and, for helminth infections, data on worm burdens. The state of sanitation in each of 9 cultural-ecological groups was assessed by means of a simplified system of scoring for variables. Particular attention was paid to relationships between cultural and ecological factors, sanitation, and observedpatterns of intestinal parasitism. The author also discusses the fact that the number of parasitic species diminishes in habitats simplified by man, whereas an increase occurs in the prevalence and intensity of the more adaptable species that persist in ecosystems of low complexity. The aborigines of Malaya are minority peoples who live in the closest possible association with the tropical forests of the lowlands and hills of the southern Malay peninsula. Their traditional modes of life reflect their adaptation to tropical forest ecosystems. Today many of these citizens of Malaya (West Malaysia) live outside the forest itself, but most of their villages are located close to the forest edge. Even though only about half of the aboriginal population (totalling some 46 000 in 1965, according to the official census of the Department of Aboriginal Affairs) remains within primary-forest areas, these are essentially forest people. The forests that support them are not homogene- ous. Many types of forest exist in the peninsula, reflecting differences in rainfall, topography, under- lying rocks and soils, and altitude. Thus the contrasts in village habitats in various parts of Malaya are considerable, and now, after more than 100 years of intensive development accompanied by much forest clearance, they are even greater than in the past. Aboriginal villages are found not only in most types of primary forest below the altitude of 900 m but * From the Department of International Health and the G. W. Hooper Foundation, University of California, San Francisco, Calif., USA, and the Institute for Medical Re- search, Kuala Lumpur, Malaysia. This study was supported in part by Research Grant TW 00144 from the International Centers for Medical Research and Training (ICMRT) Pro- gram, National Institutes of Health, Bethesda, Md., USA. 1 Professor, Department of International Health, Uni- versity of California, San Francisco, Calif., USA. also in areas of secondary forest or scrub vegetation, usually near a surviving stand of primary forest, and also often near a rubber estate, a tin-mining pool, or even a large town. Together with this diversity in habitats there are many cultural differences between tribes, partly owing to the influence ofmore advanced communities, especially during the last three decades. This diversity prompted the epidemiological study reported here. Surveys were conducted in 1962-64 to gather data on the prevalence and density of intestinal parasites with particular regard to ecological and cultural associations. A further reason for the inves- tigation was that the Department of Aboriginal Af- fairs needed basic data on intestinal parasitism in aboriginal populations in order to proceed with clinical and preventive medical programmes on a rational basis (Bolton, 1968). In conjunction with this study the thiomersal-iodine-formol direct-smear (TIF-DS) technique of examining faecal specimens for the presence of intestinal parasites was evaluated as an epidemiological method. The results of this evaluation have already been reported in a methodo- logical paper (Dunn, 1968a) that complements the present contribution. THE MALAYAN ABORIGINES In their study of the Malayan aborigines, Skeat & Blagden (1906) established three major ethnolinguis- tic divisions, which are still valid: Negrito (= Se- 2785 -99- F. L. DUNN mang), Senoi (= Sakai), and Melayu Asli or abori- ginal Malay (= Jakun or Proto-Malay). The lan- guages and dialects of the two divisions first men- tioned are considered to belong to the Austro-asiatic stock. Approximate centres of distribution of most of the larger aboriginal groups in Malaya are shown in Fig. 1. Small populations of Negritos still survive as no- madic hunters, fishers, and " gatherers " or as semi- settled, part-time cultivators in southernmost Thai- land and the northern interior of Malaya. About half a dozen territorial and ethnic subdivisions have been defined. Despite intermarriage with their Senoi neighbours, and the considerable cultural influence of the Senoi, the Negritos constitute a single, fairly homogeneous, ethnic group. The official figure for Fig. 1. Approximate centres of distribution of the larger aboriginal groups in the southern Malay peninsula. 100 INTESTINAL PARASITISM IN MALAYAN ABORIGINES 101 the Negrito population in Malaya in 1965 was 1 447. Perhaps as many as 500 more live in the forests of southern Thailand. Living entirely within West Malaysia, generally south and west of the Negrito areas, are the Senoi- speaking groups. The principal Senoi ethnolinguistic groups are: the Temiar, who officially numbered about 9 300 persons in 1965 and live mainly in the hills of the north; the Semai (about 12750), broadly distributed throughout the hills and lowlands south of the Temiar area; the Jahut (about 1 900), the Che Wong (about 300), and the Semelai (about 1 400), in Pahang; and the Mah Meri (about 1 200), living along and near the southern and central Selangor coast. The third main division of Malayan aborigines overlaps territorially, genetically, linguistically, and culturally with that of the Senoi. The two main ethnic groups are the Jakun, who numbered about 7 300 persons in 1965 and are distributed primarily in Pahang and Johore, and the Temuan (about 7 200) of Selangor, westernmost Pahang, Negri Sem- bilan, and Malacca. The Temuan, the Jakun, and a few other small but seemingly distinct ethnic groups (totalling about 1 600 persons in 1965) constitute the principal peninsular representatives of a larger body of forest people of the region comprising southern Malaya, eastern Sumatra, and the islands of the Malacca Straits. These people are animists and prac- tise shifting cultivation. They all speak (or at one time spoke) languages belonging to the Malayo- Polynesian stock and closely related to the Malay language spoken today in southern and western Malaya. Some groups have lost their ethnic and linguistic identity since the beginning of this century. MATERIALS AND METHODS During the investigation, consisting of two hospital surveys and a series of field surveys, 1 273 persons, representing about 3% of the aboriginal population of Malaya, were examined for the presence of intes- tinal protozoa and helminths. These persons com- prised the following: (a) 200 patients admitted con- secutively to the Gombak Orang Asli Hospital, near Kuala Lumpur, for all causes (first hospital survey); (b) 237 consecutive, but selected, admissions to the same hospital (second hospital survey), only persons with signs or symptoms suggestive of intestinal para- sitism being included (the patients in these two series represented all the principal ethnolinguistic groups in Malaya except Negritos); and (c) 836 villagers (86 Negritos, 542 Senoi, and 208 Melayu Asli) from whom specimens were collected on the spot (field surveys). Table 1 shows the ethnic identities of the 200 unselected patients and of the 836 villagers examined in the field surveys, as well as their means of subsistence and their habitats. Faecal specimens from all 1 273 persons were collected and preserved in thiomersal-iodine-formol (TIF) following standard methods (Sapero & Law- less, 1953). The specimens were later examined by the TIF direct-smear technique (TIF-DS) (Dunn, 1968a). In order to determine the prevalence and the intensity of helminth infection, at least 2 TIF direct smears from 24-mg specimens were examined for each subject. The egg-counts were recorded, using the following score for worm burden: 1-2 eggs per smear (+), 3-19 eggs (+ +), 20-79 eggs (+ + +), 80 or more eggs (++++). Survey counts 1 and efficiencies 2 were calculated according to procedures already outlined (Dunn, 1968a). For Ascaris the survey count was 4 020 eggs per g, corresponding to an efficiency of 90-95 % in detecting all possible Ascaris infections; for Trichuris, 1 430 eggs per g, or an efficiency of 80-85%; and for hookworm, 1 010 eggs per g, or an efficiency of about 75%. The true prevalence of hookworm was substantially underestimated in virtually all the sur- veys even though the prevalence rates in the groups investigated are uniformly high. Very slight infec- tions (1 egg per smear) were missed from time to time (as they also would have been with one of the dilution egg-counting methods). The extent of under- estimation was about the same in all the surveys because prevalence rates, worm burdens, and survey counts were nearly comparable. In practice this underestimation is insignificant in an epidemiologi- cal study such as this, where relative frequencies are being compared. Since efficiency can be estimated with the aid of the survey count, a good approxima- tion of the actual number of very slight infections missed can easily be calculated for any given survey. Efficiency in detecting intestinal protozoal infections cannot be measured in the same fashion, but com- plete scanning of two 22 x 22 mm smears at different magnifications is an effective way to recognize most such infections. 1 The survey count is the mean helminth egg-count per g of faeces per person infected in a surveyed population. 2 Efficiency, expressed as a percentage, denotes the effectiveness of faecal smear examinations in detecting all infections by a helminth species in a survey population. F. L. DUNN Table 1. Ethnic group, means of subsistence, and habitat of Malayan aborigines examined for intestinal parasitism No. examined Field First Ethnic group Means of subsistence Habitat surveys a hospital(total: 836) survey(total: 200) Negrito Semai & Jahut Semai & Jahut (Senoi) Semai (Senoi) Temiar (Senoi) semi-nomadic hunting, gathering, fishing (HGF) shifting cultivation (also HGF) mixed (casual labour, rubber tapping, shifting cultivation, HGF) primary lowland forest (below 600 m) primary hill forest(600-900 m) primary lowland forest (below 600 m) lowland secondary & primary forest village outside forest near town, & Malay village lowland swamp forest Semelai (Senoi) (chiefly secondary) & shifting cultivation swampy lakeside (also HGF) Jakun (Melayu primary lowland swamp Asli) forest Temuan (Melayu Asli) mixed (casual labour, rubber tapping, shifting cultivation, HGF) lowland secondary & primary forest a Each figure represents the total number of persons examined in any one field survey. GENERAL FINDINGS Consolidated results Table 2 summarizes the main findings of this investigation. Not including the pseudoparasite He- terodera, 22 species of helminth and protozoon were recorded as parasitic or probably parasitic in Ma- layan aborigines. Five of these stand out as particu- larly important in terms of potential pathogenicity and prevalence: Entamoeba histolytica, Giardia lam- blia, Ascaris lumbricoides, Trichuris trichiura, and hookworm. In Malaya, hookworm infection in man 74 12 191 45 83 85 119 19 67 75 54 12 45 20 50 21 11 53 102 103INTESTINAL PARASITISM IN MALAYAN ABORIGINES Table 2. Intestinal parasitism in Malayan aborigines: consolidated survey findings First hospital Second hospital survey survey Field surveys All surveys Intestinal parasites (200 unselected (237 selected (836 villagers) (1 273 persons) patients) patients) No. | % No. % No. % No. _ % Intestinal protozoa Entamoeba histolytica E. hartmanni E. coli Endolimax nana lodamoeba butschlii Dientamoeba fragilis Giardia lamblia Chilomastix mesnili ' Small flagellates - Trichomonas hominis Balantidium cofl Isospora sp. Major helminths Hookworm + a Ascaris lumbricoides ++ Trichuris trichiura ++ Persons negative for all intestinal parasites 16 11 53 18 6 24 4 3 144 80 51 13 8.0 5.5 26.5 9.0 3.0 0.5 12.0 2.0 0.5 1.5 0.5 0.5 72.0 (55.6) b (35.4) (9.0) 75 37.5 23 (30.7) 24 (32.0) 20 (26.7) 8 (10.7) 110 55.0 52 (47.3) 39 (35.5) 16 (14.6) 3 (2.7) 8 -4. 8 4.0 32 3 66 17 3 23 4 6 120 54 54 11 103 16 36 40 11 155 49 50 41 15 30 13.5 1.3 27.9 7.2 1.3 9.7 1.7 2.5 0.4 50.6 (45.0) (45.0) (9.2) (0.8) 43.5 (15.5) (35.0) (38.8) (10.7) 65.4 (31.6) (32.3) (26.5) (9.7) 17 30 239 44 26 2 91 19 24 3 0 610 345 246 19 0 320 61 144 87 28 463 251 172 36 4 2.0 3.6 28.6 5.3 3.1 0.2 10.9 2.3 2.9 0.1 0.4 73.0 (56.6) (40.3) (3.1) (-) 38.3 (19.1) (45.0) (27.2) (8.8) 55.4 (54.2) (37.2) (7.8) (0.9) 1 2.7 73 8.7 65 44 358 79 35 3 138 27 31 5 4 1 874 479 351 43 1 498 100 204 147 47 728 352 261 93 22 111 5.1 3.5 28.1 6.2 2.8 0.2 10.8 2.1 2.4 0.4 0.3 0.1 68.7 (54.8) (40.2) (4.9) (0.1) 39.1 (20.1) (41.0) (29.5) (9.4) 57.2 (48.4) (35.9) (12.8) (3.0) 8.7 a Worm burden scores based on TI F- DS egg-counts: + = very slight infection;++ + + = heavy infection. b Figures in parentheses show percentages of infected persons at each level of worm burden. F. L. DUNN is caused predominantly by Necator americanus. No attempt was made in these studies to determine the proportions of Necator and Ancylostoma infections. Two other nonpathogenic parasites-Endolimax nana and especially Entamoeba coli-were moderately pre- valent. In addition to the parasites listed in Table 2, eggs or larvae of the following helminths were recorded in the surveys at very low rates of preva- lence: Enterobius vermicularis, Strongyloides sterco- ralis, Trichostrongylus sp., an unknown larval nema- tode, two unknown trematode spp., Taenia sp., Hymenolepis nana, and Heterodera sp. The study provides reasonably good estimates of prevalence for most species but not, of course, for Enterobius vermicularis or Strongyloides stercoralis. Pinworm surveys were not attempted. The culture of Strongyloides was not feasible under field conditions; although it would have been possible in the hospital surveys, it was omitted for lack of time. Among the rare species, Balantidium coli is of particular interest. This parasite had not been reported in man on the Malay peninsula before 1963, when a preliminary note on its occurrence was published (Dunn & Bol- ton, 1963), although it was on record that the para- site had been found in Chinese in Singapore (Deso- witz et al., 1961). In 2 of the 4 cases Balantidium infection was associated-not necessarily causally- with dysentery. Three of these cases were recorded in Semelai from a village in central Pahang, which at the time was the only aboriginal locality where pig- rearing was practised. Thus Balantidium in Malayan aborigines may be regarded as an introduced infec- tion. Possibly the infections in Semelai were acquired from their pigs, but the evidence for this suggestion is only circumstantial. Parasitic species recorded for the first time in Malayan aborigines were: Entamoeba hartmanni, E. coli, Endolimax nana, Iodamoeba butschlii, Dient- amoeba fragilis, Giardia lamblia, Chilomastix mesnili, Trichomonas hominis, Balantidium coli, Isospora sp., Trichostrongylus sp., unknown dicrocoelid trema- tode species No. 1, unknown trematode species No. 2, and Hymenolepis nana. The length of this list shows that very little attention has been devoted so far to parasitic infection, particularly protozoan, in Ma- layan tribal people. The eggs of two unknown trema- todes posed a diagnostic problem, although the eggs of one at least can be recognized as those of a dicrocoelid. Only one parasitic species previously recorded in Malayan aborigines (Sandosham, 1954) -Dipylidium caninum-was not found in this inves- tigation. Discussion of consolidated results It is noteworthy that the second hospital survey -covering a series of selected patients with symp- toms suspected to be caused by intestinal parasites revealed discrepancies in prevalence apparently re- lated to this selection procedure. In comparison with the first hospital survey, in which unselected patients were examined, Trichuris was more frequent (by X2 test, P <0.05) and Entamoeba hartmanni (P <0.02) and hookworm (P 40.001) were less so. E. histolytica and Ascaris appeared to be more frequent in the second hospital series, but the differences are not statistically significant. The rate for E. histolytica in the field surveys was significantly lower (P <0.001) than that in the second hospital survey; the rates for E. hartmanni were not significantly different. The selection of patients in the second hospital survey apparently favoured the detection of parasites caus- ing diarrhoea, dysentery, and abdominal pain. These differences in prevalence and intensity between sur- veys provide indirect evidence of the clinical patency and importance of the more intense Ascaris and Trichuris infections. The significantly higher propor- tion of patients not infected with any species of intestinal parasite in the second hospital survey than in the first (P <0.01) reflects the examination of many parasite-free infants with diarrhoea. Table 2 provides worm burden data of value in assessing the public health importance of the princi- pal soil-transmitted helminths in Malayan aboriginal populations. The following scores and observations are relevant in evaluating these findings: + (1-2 eggs per 3-mg smear) = less than about 1 000 eggs per g of faeces: + + (3-19 eggs) = about 1 000 to about 6 700 eggs per g; + ++ (20-79 eggs) = about 6 700 to about 26 700 eggs per g; + + + + (80 or more eggs) = more than about 26 700 eggs per g. For Ascaris, the score of 20 000 eggs per g has been estimated to correspond to a " moderate" worm burden; for Trichuris, 20000 eggs per g probably represents a " heavy " infection; for Necator, 6 600 and 10 200 eggs per g correspond to the detectable anaemia thresholds in males and females, respective- ly, according to one report (WHO Expert Committee on Helminthiases, 1964). In each survey category about 10% of persons harbouring Ascaris shed more than 26 700 eggs per g (score: + ± ++); infections of this intensity are 104 INTESTINAL PARASITISM IN MALAYAN ABORIGINES 105 judged to be more than moderate. Indeed, many + + + Ascaris infections could be described as mo- derate or heavier. A considerable number of these aborigines clearly support heavy Ascaris burdens, and the infection constitutes an important public health problem. Terms such as " moderate" and " heavy " are, of course, clinically irrelevant in asca- riasis since even a single worm poses a threat to the host. The data in Table 2 suggest that Trichuris is not a general health problem since only 3 % of all infec- tions can be considered as heavy. However, as shown below, Trichuris varies highly in prevalence and intensity. In certain aboriginal communities it ap- pears to be a significant cause of disease. Many cases of diarrhoea and dysentery in the second hospital series were also clearly associated with heavy (+ + + +) Trichuris infections, which constituted 9.7% of all Trichuris infections in that survey. Table 2 shows that, despite the high prevalence of hookworm, only about 5% of all infections recorded were sufficiently heavy to cause anaemia, if the threshold is taken to be a worm burden correspond- ing to 6 000-10 000 eggs per g. Although common, hookworm infection alone does not seem to be responsible for much disease. However, a few cases of severe anaemia in the second hospital series were associated with heavy hookworm burdens, and this highly prevalent infection is undoubtedly an import- ant additive factor in anaemia and other states of ill health. Severe anaemia is rare in Malayan aborigines (only 10 of 237 patients were included in the second hospital series because of anaemia and suspected heavy hookworm infection), but marginal anaemia is common and is seemingly the product of a group of contributory factors (including hookworm and per- haps Trichuris) that vary in relative importance from one cultural-ecological setting to another (Polunin, 1953). Parasitism in males and in females The prevalence rates, for male and female hosts, of infection by the most common intestinal parasites have been summarized in Table 9.1 In this table, data on the 200 unselected patients of the first hospital survey are combined with data on 737 of the 836 vil- lagers examined in the field surveys (information on age and sex could not be obtained for some remote forest dwellers). I Owing to lack of space, it has not been possible to include this table in the present article. However, copies are available, on request, from the Library, World Health Organization, 1211 Geneva 27, Switzerland. These consolidated findings show few differences in prevalence according to sex. Entamoeba coli is significantly more prevalent in females (P <0.01); Ascaris and Trichuris, while differing little in preva- lence between the sexes, tend to infect females some- what more severely, but the difference is not statistic- ally significant. Parasitism according to age Tables 101 and 111 present age-specific rates for seven age groups. All ages were recorded by Dr J. M. Bolton, Chief Medical Officer of the Department of Aboriginal Affairs, or by one of several trained aboriginal medical assistants. Ages recorded for per- sons born since the late 1940s are reasonably accu- rate; for those more than 20 years old, the estimated age may differ from the real age by 5-10 years. Thus only 10-year age groups are justified for persons aged more than 20 years. Similar proportions of persons in all age groups were entirely free from intestinal parasitism at the time of examination. Neither the Entamoeba histoly- tica rates nor those for E. hartmanni differ signifi- cantly (by x2 test) between the seven age groups. Endolimax nana showed a pronounced upward trend in prevalence with increasing age. Unfortunately, little is known about the duration of E. nana infec- tions in man. If such infections are long-lasting, E. nana can be regarded as a crude indicator of the degree and length of exposure to conditions of poor environmental hygiene. E. coli rates remain stable during the early and middle years of life, but rise somewhat in old age for no apparent reason. The Giardia lamblia curve differs strikingly: most children acquire infection at an early age; rates rise to a peak between the ages of 5 and 9 years and then fall sharply with increasing age (apparently rising again in old age). The data gathered in this study show that the prevalence rates of the major soil-transmitted hel- minths in the villagers and unselected hospital pa- tients examined resemble those reported elsewhere (WHO Expert Committee on Helminthiases, 1964). Hookworm is generally acquired later than Ascaris and Trichuris, but prevalence rates rise higher and remain at a plateau (higher than 70%) throughout life. In these aboriginal populations, as in others studied elsewhere, the highest prevalence rates occur between the ages of 10 and 30 years. The Ascaris age-specific curve is entirely different: infection is acquired early, and prevalence rates fall consistently with increasing age. The Trichuris curve is also F. L. DUNN distinctive: whipworm infection is acquired early, rates decline substantially after the age of 20, and particularly between the ages of 20 and 29 years, and rise again with old age. Hookworm intensity as measured by egg output varies remarkably little from one age group to an- other. Egg output is not markedly lower in the 0-10- year span-a finding that is in accord with experi- mental findings in animals but not with certain other epidemiological studies of hookworm in man (WHO Expert Committee on Helminthiases, 1964). On the other hand, Ascaris and Trichuris worm burdens-as might have been expected-are substantially heavier in the early years of life. Parasitism in infants The data for infants aged 0-1 year were examined separately to determine the ages at which para- sites are acquired. The combined surveys related to 33 infants of the following ages: 21 days (1), 2 months (2), 4 months (1), 5 months (2), 6 months (2), 7 months (1), 8 months (1), 9 months (1), 11 months (1), and " about 1 year " (21). Of these infants, 15 were free from all parasites; 10 (30%) harboured Trichuris; 12 (36 %), Ascaris; and only 4 (12%), hookworm. Other parasites in- cluded Giardia (in 3 infants); "small flagellates" -probably Embadomonas-(in 1); Entamoeba coli (in 1); and eggs of Trichostrongylus sp. (in 1). The age of the youngest infant harbouring each species was: 6 months for hookworm and Giardia, 5 months for Ascaris, and " about 1 year " for Trichuris, E. coli, small flagellates, and Trichostrongylus. THE FIRST HOSPITAL SURVEY: AN ENVIRONMENTAL COMPARISON The initial survey of 200 patients admitted conse- cutively to hospital for all cause provided an early opportunity to compare parasitism in Malayan ab- origines-those who have left their traditional forest environment, on the one hand, and those who are still forest dwellers and subsistence cultivators on the other. Dr Bolton independently classified each of these 200 patients as " inside " (meaning forest- dwelling, traditional agriculturists) or " outside" (meaning those living outside the forest or close to a town who are more or less involved in the cash economy and more or less divorced from the tradi- tional shifting cultivation). Table 3 presents data in terms of these simple categories. It reveals differences in pattern that appear Table 3. The first hospital survey: an environmental comparison of patients living - inside "and ' outside" the forest a - Inside - Outside - Data (64 patients) (136 patients) No. % No. % Males 43 88 Females 21 48 Negative for all parasites 4 4 With symptoms suggesting intestinal parasitism 2 3.1 31 22.8 E. histolytica 2 3.1 14 10.3 E. hartmanni 1 1.6 10 7.4 E. coli 17 26.6 35 25.7 E. nana 4 6.3 14 10.3 G. lamblia 6 9.4 18 13.2 Hookworm 52 81.3 92 67.7 Ascaris 6 9.4 69 50.7 Trichuris 13 20.3 97 71.3 a See text for an explanation of inside ' and ' outside - in this context. to be associated with environmental and cultural differences between the two groups-given equal proportions of males and females, similar ages (not included in the table), and a relatively homogeneous genetic background. Only 33 of these 200 patients presented symptoms suggestive of intestinal para- sitism, yet 31 of these 33 were " outsiders ". This is consistent with significantly higher prevalence rates for Ascaris (P<0.001), Trichuris (P<0.001), and Entamoeba histolytica (P <0.05) in the "outside" group. Hookworm is significantly more prevalent " inside " (P <0.05). Entamoeba coli is about equally prevalent in both groups, and the rates for E. hart- manni, Endolimax nana, and Giardia lamblia do not differ significantly. Egg-count scoring for soil-trans- mitted helminths was also revealing: hookworm burdens were roughly similar in the two groups but Ascaris and Trichuris burdens were far heavier in the " outsiders ". This preliminary comparison provided the stimulus for a further investigation (described in the next section) into the distribution of parasites among these aborigines. 106 INTESTINAL PARASIISM IN MALAYAN ABORIGINES CULTURAL-ECOLOGICAL GROUPS, SANITATION, AND INTESTINAL PARASITISM The ethnic groups listed in Table 1 are rearranged and more fully characterized in Table 4. The tabu- lated data are self-explanatory except for the cate- gory " Sanitary status (and score) ". The descriptive scale used for sanitary status is: good, fairly good, fair, fairly poor, and poor. No good or better sanitary conditions were observed in the aboriginal villages visited during the field surveys. Latrines, or other receptacles for faeces, such as buckets, were not used in any of the surveyed communities. Semiquantitative scores for sanitary status are also given. The sanitary assessments in Table 4 were reached after the following factors had been considered: (1) Excreta and rubbish disposal practices do not appear to differ strikingly from one ethnic group or community to another. In all groups, defecation by very young children (toddlers) is relatively "promis- cuous "-that is, the child may defected close to or under the house, or at least within the village confines. However, even young children are discouraged from defecating in village streams whose water may be used for drinking and bathing. Yet this prohibition does not prevent the contamination of village water sources with faecal material because children often cleanse themselves after defecation, deliberately or inadvertently, while playing in village streams. Older children and adults are more secretive about defeca- tion and usually leave the village area for that purpose. As far as these aboriginal communities are con- cerned, contamination by defecation may be visual- ized as a series of concentric zones (this generaliza- tion is based on observations in Temuan, Semai, Temiar, and Semelai communities). At the centre, contamination is largely caused by toddlers, who Table 4. Living conditions in nine cultural-ecological groups of Malayan aborigines Ethnic No. Sntr group examined Habitat Mobility Means of subsistence Housing status (andscore) a Negrito 86 primary lowland forest semi-nomadic hunting, gathering, temporary shelters on the fairly good (below 600 m) fishing (HGF) ground (slightly elevated (30) sleeping platforms) Temiar 236 primary hill forest (600- occasional shifting cultivation and substantial houses on fairly good 900 m) residence shifts HGF piles (some longhouses) (30) Semai 65 ,, ,, ,, single- or double-room fairly good and Jahut houses on piles (28) 83 primary lowland forest ,, ,, ,, fair (below 600 m) (27) 50 lowland secondary and semi-permanent mixed (casual labour, single- or double-room fairly poor primary forest settlements rubber tapping, shifting houses of poorer quality (20) Semai cultivation, HGF) on piles 85 squatter village outside permanent ,, usually double-room poor forest near town, and settlement houses of poorer quality (12) Malay village on piles (some plank floors) Jakun 78 primary lowland swamp occasional shifting cultivation and usually single-room fair forest residence shifts HGF houses on piles (26) Semelai 159 lowland swamp forest semi-permanent shifting cultivation, usually double-room fairly poor(chiefly secondary) and settlements pig-rearing, HGF houses on piles (19) swampy lakeside Temuan 194 lowland secondary and semi-permanent mixed (casual labour, usually double-room fairly poor primary forest settlements rubber tapping, shifting houses of poorer quality (17) cultivation, HGF) on piles a See page 109 for an explanation of the method of establishing scores for sanitary status. 107 F. L. DUNN usually defecate near or under their homes; older persons rarely do so. The scrub, and village orchards and back gardens constitute a second zone favoured for defecation by older children, especially males. Adults only infrequently use these areas close to the village centre. Still farther out, the zone of gardens and fields is favoured for defecation by females, especially adults and adolescents. Adolescent and adult males may also resort to cultivated areas for defecation, but more often they do so at the forest fringe or in the outermost zone, the forest itself. Thus environmental contamination with human fae- ces occurs in zones according to age and sex. Conta- mination is most pronounced at the centre, around and under houses, where toddlers are concentrated in a relatively small area. It is lowest in the wider peripheral zones-the cultivated areas and especially the forest. Those who use these areas disperse their faeces, thus inadvertently minimizing the chances that any helminth eggs that may be passed will reach new human hosts. Rubbish disposal is casual in all Malayan abori- ginal populations. Household refuse falls or is thrown to the ground under or around the house. Although house sweeping is a common practice, sweeping the earth under and around the house is less frequent. Plank-floored houses present special problems be- cause refuse that would fall through the gaps in a floor made of split bamboo or other stems may accumulate within the house. (2) Although sanitary behaviour appears to be similar in all communities, certain environmental and cultural variables interact with customary be- haviour to produce different sanitary conditions. These variables include: Population density and crowding. Communities with large populations crowded into small areas will suffer more intense environmental contamination by defecation in a given span of time than will commu- nities with small and widely dispersed populations. One Semai village outside the forest and near a town provides a striking example of this effect. In this village, refuse and children's faeces were abundantly scattered about. The casual visitor could readily see that the environment of this densely populated vil- lage would be heavily contaminated; this contrasted with the impression of relative cleanliness in many highland Temiar villages. Land availability around the village. The sanitary status of a village is less likely to be poor if it is surrounded by forest and ample land for cultivation, as in the Temiar communities. Under such condi- tions defecation is well dispersed and soil contamina- tion is minimized. At the other extreme, the Semai village near a town is virtually a squatter community wedged in between a highway, a Malay village, and barren tin-mining wasteland (with little screening vegetation). Here defecation cannot be naturally dis- persed and contamination of the village area is inevitably intense. Community mobility. In the semi-nomadic Negrito way of life, with frequent abandonment of dwellings and new dwelling construction in " clean " locations, the contaminated environment-soil, refuse accumu- lations, water supply-is often left behind. At the other extreme, those aborigines who live in perma- nent settlements never escape the contamination of their surroundings-a contamination that can only become worse until it reaches a climax level and stabilizes. Agricultural subsistence v. hunting, gathering, and fishing. The degree of contact with the soil is another determinant of sanitary conditions in a community. Negrito populations that subsist without agriculture have much less contact with potentially contami- nated soil in the areas around their villages. Agricul- turists (other than those who produce only tree crops) are regularly exposed to any pathogens that the soil may harbour. Ground-level v. pile-elevated housing. Most Negritos live on or close to the ground in shelters that may be occupied for only a few weeks. Their daily contact with the soil in the vicinity of their homes must be substantially greater than that of any other aboriginal group in Malaya. The pile dwelling offers many advantages in the tropics, not the least of which is elevation of the living surface above the contaminated surroundings of the house. Domestic animals that may ingest refuse andfaecal matter within the village area. Pigs, dogs, and other domestic animals, when present in large numbers, can play a significant role as scavengers in reducing environmental contamination within a village. Environmental factors affecting the viability of hel- minth eggs and larvae in the soil. The Temiar (and some Semai and Jahut), living at cooler, higher elevations than other groups, may suffer less from soil-transmitted helminthiases because the type of soil and the low temperatures in those regions may adversely affect the viability of helminth eggs. In some warmer lowland areas, on the other hand, soil 108 INTESTINAL PARASITISM IN MALAYAN ABORIGINES Table 5. Scoring form for the semiquantitative assessment of sanitary conditions in Malayan aboriginal communities Variables affecting Score (from 1 to 5) for each variable Intravillage population high 2 intermediate 4 lowdensity 1 3 5 Village population high 2 intermediate 4 low size 1 3 5 Land availability around village little or none limited intermediate abundantLand aailab ity oun l ag 1 2 3 4 5 Community mobility none low intermediate high1 2 3 4 _ Agriculture versus hunting, fully agricultural 25 % HGF 50 % HGF 75 % HGF 100% HGF gathering, & fishing (HGF) 1 2 3 4 5 Ground-level housing versus ground low posts low piles medium piles high piles pile dwellings 1 2 3 4 Domestic animals that may absent few intermediate many scavenge refuse (pigs, 1 2 3 4 5dogs, etc.) Environmental factors affecting viability of helminth eggs all favourable *t dt all un- and larvae (altitude, humi- for parasites 2 nerme ae 4 favourable dity, temperature, soil type, 1 5 etc.) conditions are optimum for the transmission of hook- worm, whipworm, and Ascaris. The variables described above were used in making a semiquantitative assessment of the sanitary condi- tions in aboriginal communities by means of the scoring form in Table 5. This permits a score (from 1 to 5) to be assigned to a particular community for each of 8 variables affecting the sanitary status. The total of these 8 variable scores (which must lie between 8 and 40) is the " sanitary score" for that community. With the information provided by this score a descriptive sanitary status can be assigned to each community on the following basis: poor (scores from 8 to 13), fairly poor (14-20), fair (21-27), fairly good (28-34), good (35-40). The sanitary status shown in Table 4 can then be related to the prevalence rates for 8 intestinal parasites (Table 6) and to estimates of the intensity of helminth infection (worm burden) (Table 7). Tables 6 and 7 show the distribution of intestinal parasites in terms of prevalence and intensity. In the Temiar, for example, Ascaris is almost absent, Tri- churis is relatively rare (and the few infections are light), whereas hookworm is highly prevalent, with worm burdens comparable to those in most of the other ethnic groups studied. The main intestinal protozoa are of low to very low prevalence. In the Negrito group, also of the northern Malayan forest, the pattern differs somewhat: hookworm infection is almost universal and worm burdens are heavier than in any other Malayan aboriginal population. Trichu- ris (P<0.001), Ascaris (P<0.001), Entamoeba coli (P <0.02), and Giardia lamblia (P <0.02) are signifi- cantly more prevalent than among the Temiar. The differences in intestinal parasitism between the Negrito and Temiar groups cannot be ascribed merely to differences in sanitary status (Table 4 shows this to be similar in the two groups) or in behaviour related to the disposal of faeces and rubbish. How- ever, certain variables affecting sanitary status differ substantially between the two groups: housing, mo- bility of the community, means of subsistence, and habitats. Thus the observed differences in the distri- bution of parasites are almost certainly associated 109 F. L. DUNN c N CI 0)N4 N CD0 OD ,CI 0 0c CD II. C') 0) CDCD CD 0 _OC| o. |c 0. | | o ico _ _ 0 N CD CD CD r CD t .2 ~0CD C0 CDI 0 LCD 0) 0) -CC)- C.4 e.C6r( 0 00(Y N3 X N N Ulcc co o s 0| co ai)so -o aw Na1 )co| cDs =j P| 4 v 6i4 =4 e cn ;~ o a) PIr CD C- Co Lo co D C- ___ 0 *0 C') o co oo o It 0)o C' C- 0 0 )Nzo o CD OD .~~~~_-NOU 1 '1 0 e N NO (DoDo 0)CD0 'o_: co I co 0 - O IL CD6 C4 C6 C CD .N CD CD C C--Dr co 000o 00 0 CD r. -. 000000C 0 P~-z CD 0N1C') C' C') CY) c')N1 Cb 04 CO 0 ~ C') r 0 co Lo r C) r 00 CD 0 0C - D LO. N42c ~ c 01) z CD C') 0) UC) N0 *0 2 co cD L) C') 0 CD 00 a) Wt cDE N0m 0 0 L 00 C-. CD 0) C'co0 %-, 0 0 v 6 z 0 aD 0 0o z .E 0 C,) ~ ~ ~ ~ m~0C -6 n E -|' E E (D (D I ._ ' C C ._ ZE-_ x0 0C xo 6 c z D -00 >-0. 110 cn a) C ._m 0 .0 co C co co 2 0 0. 0 'a 0 C.)0) a) C.) co 0 a) C 0 CO a) Q C- a) n C a) co a) 0. a) CO co Co a) .0 co INTESTINAL PARASITISM IN MALAYAN ABORIGINES Table 7. Intensity of helminth infection (worm burden) in nine cultural-ecological groups of Malayan aborigines Proportion infected (%) No. Hookworm Ascaris TrichurisGroup examined Egg-count score Egg-count score Egg-count score + ++ +++ + I + +T+++ + I ++ +++ I++++ Negrito 86 31.3 63.7 5.0 40.0 60.0 85.5 14.5 Temiar 236 54.1 42.6 3.3 100.0 80.0 12.7 7.3 Semai & Jahut 65 55.9 41.2 2.9 54.8 7.7 23.1 15.4 79.0 21.0 83 72.2 27.8 27.3 45.4 27.3 100.0 Semai 50 48.5 42.5 9.0 24.1 34.5 27.6 13.8 40.0 40.0 16.7 3.3 85 75.5 20.4 4.1 12.5 47.9 27.1 12.5 53.5 42.3 4.2 Jakun 78 46.0 46.0 8.0 9.8 58.8 27.5 3.9 52.1 45.8 2.1 Semelai 159 64.9 31.5 3.6 15.9 46.0 31.0 7.1 67.8 31.3 0.9 Temuan 194 58.8 36.0 5.2 25.2 35.7 26.9 12.2 21.4 54.3 20.9 3.4 Total No. examined & 1 036 56.4 39.4 4.2 21.3 42.5 27.1 9.1 53.0 36.8 9.1 1.1 average scores _ _ [ 1 __ __ 1 1 __ __ 1 __ __ 1 _ _ with differences in one or more (or all) of these four variables. However, the data at hand do not show which is the most important in accounting for a particular difference in parasitism between the Ne- grito and Temiar groups. These cultural-ecological comparisons narrow the range of possible causal associations, but a detailed epidemiological investiga- tion would be necessary to explain these differences as well as others shown in the tables. Another example of contrasts in the distribu- tion pattern of intestinal parasites is that between the Temiar and the 85 Semai examined in a village outside the forest, near a town. Their scores for sanitary status differ greatly: fairly good (30) for the Temiar and poor (12) for the Semai. Most of the sanitary variables that have been discussed differ profoundly between these two groups, reflecting strik- ingly different sanitary conditions. In this compari- son of conditions " inside " and " outside " the forest we have a refined version of the crude comparison between " inside " and " outside " patients described earlier (see page 106) and summarized in Table 3. The prevalence rates for all intestinal protozoa are substantially higher in the Semai squatter village, and the rate for Giardia lamblia is one of the highest on record for this agent. Entamoeba histolytica (P<0.05) and E. hartmanni (P<0.001) are much more prevalent in the squatter community. Ascaris (P<0.001) and Trichuris (P<0.001) rates also are higher, and worm burdens heavier, in the squatter population. However, hookworm is significantly more prevalent (P <0.001) in the Temiar, who also suffer from a heavier worm burden than the squatter Semai. These contrasts reflect the effects, on intestinal parasitism in a human population, of a rather recent change in the way of life. The Semai of this squatter settlement left their traditional forest life after the 1940s. Thus the differences in the prevalence and intensity of infection between them and the Temiar are measures of the disease burden that was imposed upon the Semai population as it experienced ecologi- cal displacement and the influence of cultures that are more advanced technologically. ill F. L. DUNN ECOLOGICAL COMPLEXITY, DIVERSITY, AND NUMBER OF SPECIES OF INTESTINAL PARASITES As has been noted elsewhere (Dunn, 1968b), the principles of ecological diversity and complexity ap- ply to both parasitic and nonparasitic organisms. The number of species of parasite in man is closely related to the complexity of the ecosystem of which he is an element. Thus, one would expect that Negri- tos subsisting on hunting, fishing, and gathering in the complex ecosystem of the Malayan rain forest -and who therefore do not significantly modify their habitat-would be subject to a greater variety of parasites than those aborigines who have drastic- ally simplified their surroundings in preparing land for settlement and cultivation. In support of this hypothesis, Table 8 presents data on the numbers of parasitic protozoan and helminth species found in the aborigines examined during the course of the field surveys. The Negritos harboured more species of intestinal parasite than any other ethnic group studied. Of the groups listed in Table 8, only the Negritos subsist in the forest without modifying it. When the tropical forest ecosystem is simplified by man, some species of intestinal organism are elimi- nated as potential parasites of human beings. They are insufficiently adaptable to such simplified habi- tats-i.e., their natural cycles of transmission are disrupted by simplification. Thus parasites that re- quire intermediate hosts in addition to the human host are the most susceptible to elimination as man clears and cuts back the forest. In this study, several such parasites-Hymenolepis nana and two unidenti- fied species of trematode-were detected only in Table 8. Numbers of species of intestinal protozoa and helminths found in various ethnic groups of Malayan aborigines No. No. of No. of TotalEthnic group examined protozoan helminth No. of species species species Negrito 86 9 9 18 Temiar 191 7 5 12 Semai & Jahut 45 5 6 11 83 8 4 12 Semai 85 8 4 12 Jakun 67 6 5 11 Semelai 138 loa 4 14 a 75 8 6 14 Temuan 54 7 3 10 12 3 3 6 a Includes an introduced parasite, Balantidium coli, not found in other Malayan aborigines. people of the primary forests. Yet some of the more adaptable parasites, such as Ascaris, Trichuris, Giar- dia, and Entamoeba histolytica, could be likened to weeds. Although they infect forest people, they are much more successful, in terms of prevalence and intensity, in simplified habitats. They are most suc- cessful of all in the ultimate simplification of the Semai squatter village. ACKNOWLEDGEMENTS These studies would not have been possible without the support and collaboration of Dr J. M. Bolton, Medical Officer, Department of Aboriginal Affairs, Federation of Malaysia. The encouragement and suggestions of Dr Paul C. Beaver, Tulane University, New Orleans, La., USA, are gratefully acknowledged; and I am indebted to Mr Harry C. S. Lee for his assistance in the laboratory. I also wish to thank all those, too numerous to mention by name-villagers and members of the medical field staff of the Department of Aboriginal Affairs-who con- tributed so much to the successful completion of the surveys. RESUME PARASITISME INTESTINAL CHEZ DES ABORIGtNES MALAIS (ORANG ASLI) On a men6 en 1962/64 des enquetes sur le parasitisme intestinal parmi les Orang Asli, groupe ethnique mino- ritaire du sud de la peninsule malaise. Cette etude etait -motiv&e par l'absence quasi complete de donn6es sur la prevalence des infestations par les helminthes et les protozoaires chez ces aborigenes par ailleurs remarquables par la diversite de leurs conditions culturelles et ecolo- giques. 112 INTESTINAL PARASITTSM IN MALAYAN ABORIGINES 113 Un examen direct des feces conservees dans une solution de thiomersal-iode-formol a ete effectu6 chez 1273 personnes, dont 437 sujets hospitalises et 836 villageois. Vingt-deux especes d'helminthes et de protozoaires, parasites ou probablement parasites, ont ete identifiees, cinq d'entre elles (Entamoeba histolytica, Giardia lamblia, Ascaris lumbricoides, Trichuris trichiura, ankylostome) pr6sentant une importance particuliere en raison de leur pathogenicite potentielle et de leur frequence. On a constate une plus forte prevalence des infestations et une charge parasitaire plus elevee chez les indigenes ayant abandonn6 leur milieu traditionnel. Cependant I'ankylostomiase et le parasitisme A Entamoeba coli etaient egalement frequents dans tous les groupes etudies. Cer- taines populations offrant une gamme de caract6ristiques culturelles et ecologiques ont fait l'objet d'une enquete plus approfondie, dont les r6sultats, analyses et present6s sous forme de tableaux, font ressortir des variations considerables du parasitisme intestinal. Un fait remar- quable est 1'existence d'un plus grand nombre d'especes parasitaires chez les Negritos, groupe vivant en foret et s'adonnant a la chasse, A la peche et A la cueillette des fruits, que dans d'autres populations vivant dans un milieu qu'elles ont entrepris de modifier et ou certaines esp6ces de parasites ne peuvent subsister. REFERENCES Bolton, J. M. (1968) Brit. med. J., 2, 818-823 Desowitz, R. S., Zaman, V. & Ng, W. K. (1961) Singapore med. J., 2, 91-93 Dunn, F. L. (1968a) Bull. Wid Hlth Org., 39, 439-449 Dunn, F. L. (1968b) Epidemiological factors: health and disease in hunter-gatherers. In: Lee, R. B. & DeVore, I., ed., Man the hunter, Chicago, Aldine Publishing Company, pp. 221-228 Dunn, F. L. & Bolton, J. M. (1963) Singapore med. J., 4, 175-176 Polunin, I. (1953) Med. J. Malaya, 8, 55-174 Sandosham, A. A. (1954) In: Audy, J. R., ed., Malaysian Parasites I-XV, Kuala Lumpur, Institute for Medical Research, Studies: No. 26, pp. 210-211 Sapero, J. J. & Lawless, D. K. (1953) Amer. J. trop. Med. Hyg., 2, 613-619 Skeat, W. W. & Blagden, C. 0. (1906) Pagan races of the Malay peninsula, London & New York, Macmillan, 2 vols WHO Expert Committee on Helminthiases (1964) Wld Hlth Org. techn. Rep. Ser., No. 277, p. 14