APPENDIX B

Figure B1a. The distribution of A. lumbricoides in Southeast Asia, as indicated by province-level estimates based on available survey data. White indicates those provinces where no relevant data were located.

% infected 0 0.1 - 9.9 10 - 49.9 50 - 79.9 80 - 100 No data

32

Figure B1b. The distribution of T. trichiura in Southeast Asia, as indicated by province-level estimates based on available survey data. White indicates those provinces where no relevant data were located.

% infected 0 0.1 - 9.9 10 - 49.9 50 - 79.9 80 - 100 No data

33

Figure B1c. The distribution of hookworm in Southeast Asia, as indicated by province-level estimates based on available survey data. White indicates those provinces where no relevant data were located.

% infected 0 0.1 - 9.9 10 - 49.9 50 - 79.9 80 - 100 No data

34

Figure B2. The distribution of schistosomiasis in Southeast Asia, as indicated by province-level estimates based on available survey data. White indicates those provinces where no relevant data were located.

% infected 0 0.1 - 19.9 20 - 49.9 50 - 79.9 80 - 100

300

300

600 Kilometers

35

Figure B3. The distribution of filariasis in Southeast Asia, as indicated by province-level estimates based on available survey data. White indicates those provinces where no relevant data were located.

% infected 0 0.1 - 1.9 2 - 4.9 5 - 10

300

300

600 Kilometers

36

Figure B4a. Predicted prevalence of A. lumbricoides in communities for Southeast Asia, as derived from regression models of the relation between prevalence in Vietnam and environmental variables derived from remotely sensed satellite sensor data.

37

Figure B4b. Predicted prevalence of T. trichiura in communities for Southeast Asia, as derived from regression models of the relation between prevalence in Vietnam and environmental variables derived from remotely sensed satellite sensor data.

38

This page is left intentionally blank

39

Human helminth infections in Indonesia, East Timor and the Philippines

Report to UNICEF East Asia and Pacific Region Office 19 Phra Atit Road, Bangkok 10200, Thailand

2002

Dr Simon Brooker Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine Keppel Street, London WC1E 7HT. Email: simon.brooker@lshtm.ac.uk

40

1: INTRODUCTION Although Southeast Asia is known to have a high prevalence of soil-transmitted helminth infection (Urbani & Palmer, 2001), the distribution and prevalence of infection has not been fully described before. Yet, renewed interest in helminth control has lead to an increased impetus to attain comprehensive data, allowing available control interventions to be most rationally and costeffectively deployed. In concert with these changes in international health priorities, there have been tremendous developments in methods to map and analyze epidemiological information. Geographical information systems (GIS) are increasingly being used to collate and map available epidemiological data and have been used in several studies mapping disease distributions. The development of such GIS maps can contribute towards the design and implementation of disease control programmes. In particular, they can allow the identification and priorization of target areas, and also offer an effective means of monitoring the impact of control programmes. For helminth infections, applications of GIS have until recently been undertaken only in Africa (Brooker et al., 2000). Through recent support of UNICEF EAPRO, this GIS approach was extended to include the mapping of helminth infections in Southeast Asia (Anon., 2002). Initially, the work included Cambodia, Lao PDR, Myanmar, Thailand and Vietnam (the Mekong countries). The present work extends this work and develops a GIS database of helminth infection in Indonesia (including East and West Timor) and the Philippines using from available survey data in the region, in order to describe the distribution of infection and the implications for helminth control in the sub-region.

41

2: MATERIALS AND METHODS Geographical information systems (GIS) were used to capture existing infection data from the published literature and develop province-level descriptive maps of helminth infections. An extensive computer literature review and reference tracing was undertaken to identify studies which reported data on the prevalence of helminth infection in Indonesia (including East and West Timor) and the Philippines. Prevalence estimates were only accepted for analysis if they were based on a single community or a group of localized communities. Data were excluded if they came from hospital surveys, as these tend to be biased samples, if they did not provide the sample size and/or the number positive (necessary to undertake the weighted analysis), or if there were inconsistencies in the calculations presented. The province-level prevalence estimates were extracted from published surveys where available, and incorporated into a standardized database format (Brooker et al., 2000; Anon., 2002). The location data of each survey was identified and allocated to a specific province as identified in the UNEP GIS database (http://grid2.cr.usgs.gov/datasets/datalist.php3) (Figure 1). Mean prevalences were calculated for the provinces in which more than one survey had been conducted by taking the weighted mean of the individual survey prevalences, with weights given according to sample size. Geographical data are displayed using ArcView (Version 3.2, ERSI, CA, 1998).

The Phillippines

Cagayan Valley Ilocos Central Luzon Bicol Eastern Western Visayas Visayas Southern Central Tagalog Visayas Northern Western Mindanao MindanaoCentral Mindanao Southern Mindanao

Aceh Sumatera Utara Riau Sumatera Barat Jambi Sumatera Bengkulu Selatan Lampung Kalimantan Barat Kalimantan Tengah Kalimantan Selatan Sulawesi Tengah Sulawesi Selatan Sulawesi Tenggara Kalimantan Timur

Sulawesi Utara

Maluku

Irian Jaya

Indonesia

Jawa Jawa Barat Tengah Jawa Timur

Bali

Nusa Tenggara Barat

East Timor

West Timor

East Timor

Figure 1. Provinces in Indonesia, the Philippines, and East Timor.

42

3: RESULTS 3.1. Schistosomiasis Schistosomiasis in the sub-region is due to Schistosoma japonicum and occurs in restricted foci. In Indonesia schistosomiasis is limited to two isolated foci, namely the Napu and Lindi valleys in Central Sulawesi. A comprehensive control programme has successfully reduced the prevalence of infection to <2% (Izhar et al., 2002). In the Philippines, schistosomiasis is more widely distributed but the endemic areas are well known (Figure 2). In particular, schistosomiasis occurs in Mindanao and Visayas in the south of the country and isolated foci in Southern Tagalog (Leonardo et al., 2002). In these areas some 1.76 million people are estimated to be directly exposed to infection. However, control programmes have successfully reduced the prevalence of infection in recent years and the national prevalence is estimated to be 4.7%. Schistosomiasis is currently targeted for elimination as a public health problem in endemic areas in the next four years.

Figure 2. Distribution of schistosomiasis in the Philippines. Taken from Leonardo et al., 2002.

3.2. Intestinal nematode species Intestinal nematode species are more widely distributed across the sub-region. The literature search identified 36 references for Indonesia, describing 50 surveys, but only six references for Philippines describing six surveys (Table 1). Unsurprisingly, no suitable data were identified for East Timor.
Table 1. The prevalence of intestinal nematode species in the Philippines as derived from available survey data
Locality Age group No. examined A. lumbricoides T. trichiura Hookworm Reference

Siniloan (Southern Tagalog) All ages Palawan (Southern Tagalog) Adults Cebu Island (Central Viasyas) Adults Cebu Island (Central Viasyas) All ages Talim Island (Central Luzon) Adults Bukidnon (Northern Mindanao) Adults

142 353 1014 7891 2083 831

40.3 39.7 50.1 60.4 91.9 33.8

71.4 26.9 53.5 34.3 93.5 12.2

32.6 23.0 12.5 7.5 41.4

Yamamoto et al 2000 Oberst & Alquiza 1987 Cross et al 1977 Bulatao-Jayme et al. (1978) Jueco et al 1973 Carney et al 1981

43

Because few surveys were identified for the Philippines no further analysis is made in this report. However, despite differences in the timings of surveys and survey methods, the report provides detailed information on the distribution of soil-transmitted helminths in Indonesia.

3.2.1. Geographical distribution of intestinal nematode species The maps of soil-transmitted helminth distribution in Indonesia over the past three decades are presented in Figure 3. These maps show marked variation in the prevalence of infection for each of the intestinal nematode species. The data indicate that there may be distinct regions of high prevalence within the region including Irian Jaya and Sumatera Utara. Low prevalence areas are found in Jawa Timor. However, the province-level analysis adopted here belies the variation in prevalence found within provinces.

(a)

(b)

(c)
% infected 0 0.1 - 19.9 20 - 49.9 50 - 79.9 80 - 100

1000

1000

2000 Kilometers

Figure 3. The distribution of (a) A. lumbricoides, (b) T. trichiura and (c) hookworm in Indonesia, as indicated by province-level estimates based on available survey data. White indicates those provinces where no relevant data were located.

44

Climatic factors such as temperature, humidity and rainfall may be important influencing factor in the distribution of infection. In Indonesia, the range of maximum temperature (as estimated from satellitederived land surface temperature) is 16 oC in the highlands of Irian Jaya to 43 oC in the lowlands of Jawa Timor. In the Philippines, temperature ranges from 25 oC in parts of Mindanao to 45 oC in the north of the country (Figure 4). Previous work in Africa and Southeast Asia (Brooker et al. 2002a, b) suggests that A. lumbricoides and T. trichiura occurs at low prevalence where maximum LST exceeds 40 oC. Thus the low prevalence observed in Jawa Timor, Indonesia could be explained by the relatively high temperatures compared to hose observed in the rest of the country. Similarly, although data is lacking, low prevalences could be predicted in West Timor and parts of Luzon in the Philippines. Based on observed temperatures, it is predicted that East Timor would have moderate levels of infection warranting the need for control. In the highlands of Irian Jaya and Samatera, by contrast, low prevalences are predicted because of the relatively low temperatures, although this is not immediately clear from the province-level analysis (Figure 3).

Figure 4. Maximum land surface temperature (LST) as derived from 8km NOAA-AVHRR satellite data.

Where temperatures are suitable for the transmission of nematode species, other factors such peoples educational level, personal and environmental hygiene, and agricultural practices will also influence the level of transmission. It is unclear however which of these factors are responsible for determining levels of infection and it probably reflects the interaction of several different factors. This requires further investigation. Although accurate estimates of number at risk of infection are not currently available it is probable that intestinal nematode infections are a public health problem throughout the sub-region. Using population estimates from national census agencies in Indonesia (http://www.bps.go.id) and the Philippines (http://www.census.gov.ph), it is estimated that there are 51.8 million school-age children in Indonesia and 19.5 million school-age children in the Philippines. With the exception of highland areas, much of the sub-region experiences suitable temperatures for the helminth transmission and therefore school-based control programmes should be considered throughout the sub-region.

45

To better estimate the need for the treatment, future surveys can help identify priority areas for control and estimate the numbers requiring treatment. For the control of helminth infections, current WHO recommendations are based on the concept of sample surveys within defined ecological zones. The use of ecological zone maps derived from satellite sensor data are shown to be of value in defining sampling clusters in conducting rapid and valid epidemiological surveys of different helminth species (Brooker et al., 2002c). Such an approach could usefully be adopted in areas where survey data are lacking. 3.2.2. Age patterns in infection prevalence Analysis of infection prevalence by age group in Indonesia indicates that all age groups are risk of infection, although hookworm and T. trichiura prevalence tends to increases with increasing age, whereas A. lumbricoides prevalence decreases with increasing age (Table 2). This analysis demonstrates that control is warranted across all age groups.
Table 2. Prevalence of infection by age group in Indonesia from surveys conducted since 1970.

Age group A. lumbricoides T. trichiura Hookworm No. of surveys Pre-school 63.7 50.0 38.1 27 School-aged 53.0 56.3 40.7 38 Adults 50.8 56.0 65.9 32

3.2.3. Impact of control programmes in Indonesia During the 1970s numerous surveys were conducted in several areas of Indonesia showing a high prevalence of soil-transmitted helminthes across the country. In the period 1975-1980, limited governmental and non-governemental control programmes were initiated. During the 1990s, the Department of Health implemented a targeted mass treatment programme in areas where prevalence exceeds 30% (Margono, 2001). Since very few localities have been surveyed more than once, it is difficult to determine the precise impact of the control programme. However, a crude comparison of infection prevalence by province between the 1970s and the 1990s indicate a general reduction in the prevalence of infection, especially in Jawa Tengah and Jawa Barat (Figure 5). The reduction in prevalence is likely to be a reflection of the impact of control programmes, but also a reflection in improvements in sanitation and general living standards. Nonetheless, the present situation in Indonesia underlies the continued need for treatment programmes throughout the country.

100 90 80
Percent infected
A. lumbricoides T. trichiura Hookworm

70 60 50 40 30 20 10
1970s 1990s 1970s 1990s 1970s 1990s 1970s 1990s 1970s 1990s 1970s 1990s

Bali

Irain Jaya

Jawa Barat

Jawa Tengah

Sulawesi Selatan

Sulawesi

Figure 5. Prevalence of infection by province in Indonesia during the 1970s and 1990s

46

4: SUMMARY AND RECOMMENDATIONS The following recommendations are a digest of the analysis undertaken throughout the body of this report and follow loosely the order in which they were discussed. The GIS mapping of helminths demonstrates geographical variation of helminth infection in Indonesia (including East and West Timor) and the Philippines, which should be used to guide helminth control programmes. Schistosomiasis has a restricted distribution and is the subject of concerted control efforts in both Indonesia and the Philippines. With on-going control in the region, schistosomiasis is likely to be eliminated as a public health problem in the near future. With the exception of highland areas, intestinal nematode species are prevalent throughout the region and across all age groups, and thereby warrants treatment programmes. Although national control efforts have been effective in reducing prevalence levels, continued control efforts are recommended in all areas exception highland areas. The present province-level analysis ignores small-scale variation in prevalence. The use of temperature maps, as derived from satellite sensor data, can help predict levels of prevalence and thereby further help guide control programmes more precisely. Further work is needed to map the small-scale variation in intestinal helminth species in the region and in relation to satellitederived climatic factors. Many areas in the region are without suitable prevalence data and further searches should be conducted in-country, including sources in Ministries of Health or research institutes. Appropriate institutions should be contacted to investigate the availability of further prevalence data. To help guide national control measures, future prevalence surveys should be planned in East Timor.

47

5: REFERENCES Anon. (2002). Human helminth infections in South East Asia. Commissioned for UNICEF East Asia and Pacific Region Office, Bangkok. Brooker, S., Rowlands, M., Haller, L., Savioli, L. & Bundy, D.A.P. (2000). Towards an atlas of human helminth infection in sub-Saharan Africa: the use of geographical information systems (GIS). Parasitology Today 16 (7), 303-307. Brooker, S., Hay, S.I., Tchuem Tchuent, L.A. & Ratard, R. (2002a). Using NOAA-AVHRR data to model helminth distributions for planning disease control in Cameroon, West Africa. Photogrammetric Engineering and Remote Sensing 68, 175-179.
Brooker. S., Pratap, S., Waikagul, J., Suvanee, S., Kojima, S., Takeuchi, T., Luong, T.V & Looareesuwan, S. (2002b). Soil-transmitted helminth infections and parasite control in Southeast Asia. Southeast Asian Journal of Tropical Medicine and Public Health (in press). Brooker, S., Beasley, N.M.R., Ndinaromtan. M., Madjiouroum, E.M., Baboguel, M., Djenguinabe, E., Hay, S.I. & Bundy, D.A.P. (2002c). Use of remote sensing and a geographical information system in a national helminth control programme in Chad. Bulletin of the World Health Organization 80, 783-789. Izhar, A., Sinaga, R.M., Sudomo, M. & Wardiyo, N.D. (2002). Recent situation of schistosomiasis in Indonesia.

Acta Tropica 82, 283-288. Leonardo, LR, Acosta, LP, Olveda RM & Aligui, GDL. (2002). Difficulties and strategies in the control of schistosomiasis in the Philippines Acta Tropica 82 295-299. Margono, S.S. (2001). Review on the control of soil-transmitted helminthiases in Indonesia: the role of parasitologists. In Collected Papers on the Control of Soil-transmitted Helminthiases. Ed. Hayashi, S. pp. 169-172.

48

Appendix 1. Summary descriptives of the database on the prevalence of helminth infection in Indonesia (including East and West Timor) and the Philippines.
Table A1. Summary descriptives of the database on the prevalence of helminth infection in Indonesia. Complete database available from author (simon.brooker@lshtm.ac.uk) Country Locality No. of stools Species Source examined examined1 Indonesia Bali 2331 Hk Bakta et al. (1993) Indonesia Oksibil Valley, Irian Jaya 200 As, Tr, Hk Bangs et al. (1996) Indonesia Poso Valley, Central Sulawesi 671 As, Tr, Hk Carney et al. (1974) Indonesia Napu, Central Sulawesi 347 As, Tr, Hk Carney et al. (1977a) Carney et al. (1977a) Indonesia Besoa, Central Sulawesi 656 As2, Tr, Hk Indonesia Central Sulawesi 789 As, Tr, Hk Carney et al. (1977b) Indonesia South Sulawesi 369 As, Tr, Hk Carney et al. (1977b) Indonesia Central Java 743 As, Tr, Hk Clarke et al. (1973a) Indonesia Kresek, West Java 603 As, Tr, Hk Clarke et al. (1973b) Indonesia Lindu Valley, Central Sulawesi 1417 As, Tr, Hk Clarke et al. (1974) Indonesia Luwu, South Sulawesi 659 As, Tr, Hk Cross et al. (1972) Indonesia South Kalinantan, Borneo 2169 As, Tr, Hk Cross et al. (1975) Indonesia Northern Sumatra 2057 As, Tr, Hk Cross et al. (1976a) Indonesia West Kalimantan, Borneo 2101 As, Tr, Hk Cross et al. (1976b) Indonesia North Sulawesi 828 As, Tr, Hk Cross et al. (1977a) Indonesia Irian Jaya 114 As, Tr, Hk Cross et al. (1977b) Indonesia Sumatra 227 As, Tr, Hk Higgins et al. (1984) Indonesia Java 831 As, Tr, Hk Higgins et al. (1984) Higgins et al. (1984) Indonesia Flores 329 As, Tr2, Hk Indonesia Asahan Regency, North Sumatra 977 As, Tr, Hk Imai et al. (1985) Indonesia Alor, East Nusa Tenggara Islands 311 As, Tr, Hk Joesoef & Dennis (1980) Indonesia South Sulawesi 765 As, Tr, Hk Joseph et al. (1978) Indonesia South Sumatera 731 As, Tr, Hk Margono (2001) Indonesia West Sumatera 738 As, Tr, Hk Margono (2001) Indonesia West Java 1252 As, Tr, Hk Margono (2001) Indonesia Jakarta 91 As, Tr, Hk Margono (2001) Indonesia Jakarta 602 As, Tr, Hk Margono (2001) Indonesia Yogyakarta 1153 As, Tr, Hk Margono (2001) Indonesia Central Java 595 As, Tr, Hk Margono (2001) Indonesia East Java 1061 As, Tr, Hk Margono (2001) Indonesia South Sulawesi 1156 As, Tr, Hk Margono (2001) Indonesia North Sulawesi 1199 As, Tr, Hk Margono (2001) Indonesia Bali 1150 As, Tr, Hk Margono (2001) Indonesia South Sumatra 280 As, Tr, Hk Margono et al. (2001a) Indonesia South Sumatra 365 As, Tr, Hk Margono et al. (2001b) Indonesia Karakuak, West Flores 104 As, Tr, Hk Purnomo et al. (1980) Indonesia North Sulawesi 156 As, Tr, Hk Stafford et al. (1976) Stafford et al. (1980a) Indonesia Torro Valley, Central Sulawesi 287 As2, Tr2, Hk Indonesia Bali 270 As, Tr, Hk Stafford et al. (1980b) Indonesia Palolo Valley 401 As, Tr, Hk Van Peenan et al. (1977) Indonesia Halmahera Island 389 As, Tr, Hk Mangali et al. (1994) Indonesia Likupang, North Sulawesi 419 As, Tr, Hk Hasegawa et al. (1992) Indonesia Campalagian, South Sulawesi 398 As, Tr, Hk Mangali et al. (1993) Indonesia Ujung Pandang, South Sulawesi 507 As, Tr, Hk Mangali et al. (1993) Indonesia Tanjung Priok, Jakarta 302 As, Tr Karyadi et al. (1996)

49

Indonesia Indonesia Indonesia Indonesia Indonesia Philippines Philippines Philippines Philippines Philippines Philippines

Sukaraja, West Java Bali Barru, South Sulawesi Purworejo, Central Java Bali Siniloan Buridnon Province, Mindanao Cebu Island Cebu Island Talim Island, Rizal Palawan, Southern Tagalog

348 2394 654 442 454 142 831 1014 7891 2083 353

As, Tr, Hk As, Tr, Hk As, Tr, Hk As, Tr, Hk Hk As, Tr As, Tr, Hk As, Tr, Hk As, Tr, Hk As, Tr, Hk As, Tr, Hk

Pegelow et al. (1997) Widjana & Sutisna (2000) Toma et al. (1999) Nurdiati et al. (2001) Bakta & Budhianto (1994) Yamamoto et al. 2000 Carney et al. 1981 Cross et al. 1977 Bulatao-Jayne et al. 1978 Jueco et al. 1977 Oberst & Alquiza 1987

As = Ascaris lumbricoides; Tr = Trichuris trichiura; Hk = hookworm

References included in the GIS database 2. Bakta, I.M., Widjana, I.D.P. & Sutisna, P. (1993). Some epidemiological aspects of hookworm infection among the rural population of Bali, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health. 24, 87-93. Bakta, I.M. & Budhinto, F.X. (1994). Hookworm anaemia in the adult population of Jagapati village, Bali, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health. 25, 459-463. Bangs, M.J., Purnomo, Andersen, E.M, & Anthony, R.L. (1996). Intestinal parasites of humans in a highland community of Irian Jaya, Indonesia. Annals of Tropical Medicine and Parasitology 90, 1, 4953. Carney, W.P., Putrali, J. & Caler, J.M. (1974). Intestinal parasites and malaria in the Poso Valley, Central Sulawesi, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health. 5, 368373. Carney WP, Masri S, Stafford EE & Putrali J. (1977a). Intestinal and blood parasites in the North Lore District, Central Sulawesi, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health 8, 165-172. Carney WP, Van, P.F.D., See, R., Hagelstein, E. & Lima, B. (1977b). Parasites of man in remote areas of Central and South Sulawesi, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health 8, 165-172. Clarke MD, Cross JH, Carney WP, Bechner WM, Oemijati S, Partono P et al. (1973a). A parasitological survey in the Jogjakarta area of Central Java, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health 4, 195-201. Clarke, M.D., Cross, J.H., Gunning, J-J., Reynolds, D., Oemijati, S., Partono, F., Hudojo & Hadi. (1973b). Human malarias and intestinal parasites in Kresek, West Java, Indonesia, with a cursory serological survey for toxoplasmosis and amoebiasis. Southeast Asian Journal of Tropical Medicine and Public Health. 4, 32-36. Clarke MD, Carney WP, Cross JH, Hadidjaja P, Oemijati S & Joesoef A. (1974). Schistosomiasis and other human parasitoses of Lake Lindu in Central Sulawesi (Celebes), Indonesia. American Journal of Tropical Medicine and Hygiene 23, 385-392.

3.

4.

5.

6.

7.

8.

9.

10.

50

11.

Cross, J.H., Clarke, M.D., Irving, G.G., Duncan, C.F., Partono, F., Hudojo, Oemijati, S. Noor, N. & Borahina. (1972). Intestinal parasites and malaria in Margolembo, Luwu Regency, South Sulawesi, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health. 3, 587-593. Cross, J.H., Clarje, M.D., Durfee, P.T., Irving, G.S., Taylor, J., Partono, F., Joesoef, A., Hudojo & Oemijati, S. (1975). Parasitology survey and seroepidemiology of amoebiasis in South Kalimantan (Borneo), Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health. 6, 52-60. Cross JH, Clarke MD, Cole WC, Lien JC, Partono F, Joesoef A et al. (1976a). Parasitology survey in Northern Sumatra, Indonesia. Journal of Tropical Medicine 79, 123-131. Cross, J.H., Clarke, M.D., Cole, W.C., Lien, J.C., Partono, F., Djakaria, Joesoef, A. & Oemijati, S. (1976b). Parasitic infections in humans in West Kalimantan (Borneo), Indonesia. Tropical and Geographical Medicine. 28, 121-30. Cross JH, Wheeling CH, Stafford EE, Irving GS, Petersen HV, Gindo S et al. (1977a). Biomedical survey on the Minahasa Peninsula of North Sulawesi, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health 8, 390-399. Cross, J.H., Irving, G.S., Anderson, K.E., Gunawan, S. & Saroso, J.S. (1977b). Biomedical survey in Irian Jaya (West Irian), Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health. 8, 532-536. Hadju, V., Abadi, K., Stephenson, L.S., Noor, N.N., Mohammed, H.O. & Bowman, D.D. (1995). Inestinal helminthiasis, nutritional status, and their relationship; a cross-sectional study in urabn slum school children in Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health. 26, 719-729. Hasegawa, H., Miyagi, I., Toma, T., Kamimura, K., Nainggolan, I.J.J., Tumewu-Wagei, M., MandagiWaworuntu, H.G., Kapojos, F.X., Runtuwene, J., Paath-Runtupalit, C. & Syafruddin. Intestinal parasitic infections in Likupang, North Sulawesi, Indonesia. (1992). Southeast Asian Journal of Tropical Medicine and Public Health. 23, 219-227. Higgins DA, Jenkins DJ, Purnomo LK, Harun S & Juwono SS. (1984). Human intestinal parasitism in three areas of Indonesia: a survey. Annals of Tropical Medicine and Parasitology 78, 637-648. Imai, J.I., Sakamoto, O., Munthe, E. & Sinulingga, S. (1985). Survey for soil-transmitted helminths in Asahan Regency, North Sumatra, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health. 16, 441-446. Joesoef, A. & Dennis, D.T. (1980). Intestinal and blood parasites of man on Alor Island Southeast Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health, 11, 43-47. Joseph SW, Carney WP, Van Peenen PFD, Russell D & Saroso JS. (1978). Human parasitoses of the Malili Area, South Sulawesi (Celebes) Province, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health 9, 264-271. Karyadi, E., Gross, R., Sastroamidjojo, S., Dillon, D., Richards, A.L. & Sutanto (1996). Anthelminthic treatment raises plasma iron levels but does not decrease the acute-phase response in Jakarta school children. Southeast Asian Journal of Tropical Medicine and Public Health 27, 742-753. Mangali, A., Sasabone, P., Syafruddin, Abadi, K., Hasegawa, H., Toma, T., Kamimura, K. & Miyagi, I. (1993). Intestinal parasitic infections in Campalagian District, South Sulawesi, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health 24, 313-320. Mangali, A., Sasabone, P., Syafruddin, Abadi, K., Hasegawa, H., Toma, T., Kamimura, K., Hasan, M., Miyagi, I. & Mogi, M. (1994). Prevalence of intestinal helminthic infections in Kao District, North Halmahera, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health 25, 737-743.

12.

13.

14.

15.

16.

17.

18.

19.

20.

21.

22.

23.

24.

25.

51

26.

Margono, S.S. (2001). Review on the control of soil-transmitted helminthiases in Indonesia: the role of parasitologists. In Collected Papers on the Control of Soil-transmitted Helminthiases. Ed. Hayashi, S. pp. 169-172. Margono, S.S., Abidin, S.A.N, Ismid, I.S., Anwar, C., Zit, Z. & Dj, R. (2001a). Prevalence and intensity of soil-transmitted helminthic infections in two sub-villages of South Sumatra, Indonesia: association with economic level, behaviour and environmental sanitation. In Collected Papers on the Control of Soil-transmitted Helminthiases. Ed. Hayashi, S. pp. 169-172. Margono, S.S., Zit, Z., Ismid, I.S., Anwar, C. & Abidin, S.A.N., (2001b). Infection and re-infection rate of hookworm and other soil-transmitted helminthic infections in school children in South Sumatra, Indonesia. In Collected Papers on the Control of Soil-transmitted Helminthiases. Ed. Hayashi, S. pp. 118-124. Nurdiati, D.S., Suyoko, Hakimi, M. & Winkvist, A. (2001). Impact of intestinal helminth infection on anemia and iron status during pregnancy: a community based study in Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health 32, 14-22. Pegelow, K., Groos, R., Pietrzik, K., Lukito, W., Richards, A.L. & Fryauff, D.J. (1997). Parasitological and nutritional situation of school children in the Sukaraja District, West Java, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health 28, 173-190. Purnomo, Partino, F. & Soewarta, A. (1980). Human intestinal parasites in Karakuak, West Flores, Indonesia and the effect of treatment with mebendazole and pyrantel pamoate. Southeast Asian Journal of Tropical Medicine and Public Health 11, 324-327. Stafford EE, Masri S & Sorensen K. (1976). Parasitological survey in Gorontalo, North Sulawesi, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health 7, 405-410. Stafford EE, Dennis DT, Masri S & Sudomo M. (1980a). Intestinal and blood parasites in the Torro Valley, Central Sulawesi, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health 11, 468-472. Stafford E.E., Sudomo, M., Masri, S. & Brown, R.J. (1980b). Human parasitoses in Bali, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health 11, 319-323. Toma, T., Miyagi, I., Kamimura, K., Tokuyama, Y., Hasegawa, H., Selomo, M., Dahlan, D., Majid, I., Hasanuddin, I., Ngatimin, R., Mogi, M. & Kuwabara, N. (1999). Southeast Asian Journal of Tropical Medicine and Public Health 30, 68-77. Van Peenen, D., Carney, P., See, R., Gundelfinger, B.F. & Cross, J.H. (1977). Disease survey of Palolo Valley, Central Sulawesi, Indonesia. II. Intestinal parasites, malaria and filariasis. Military Medicine June, 454-457. Widjana, D.P. & Sutisna, P. (2000). Prevalence of soil-transmitted helminth infections in the rural population of Bali, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health 31, 454-459.

27.

28.

29.

30.

31.

32.

33.

34.

35.

36.

37.

PHILIPPINES

38. 39.

Bulatao-Jayme, J., Villavieja, G.M., Alcalde, P.V. Varerio, T.E. (1978). Food consumption, intestinal parasitism and anemia on the Visayas. Journal of the Philippine Medical Association 54, 224-244. Carney, W.P., de Veyra, V., Cala, E.M. & Cross, J.H. (1981). Intestinal parasites of man in Bukidnon, Philippines, with emphasis on schistosomiasis. Southeast Asian Journal of Tropical Medicine and Public Health 12, 24-29. Cross, J.H., Wheeling, C., Banzon, T., Basaca-Sevilla, V. & Sevilla, J. (1977). Amoebiasis and intestinal parasitic infections in a population on Cebu Island, the Philippines. Annals of Tropical Medicine and Parasitology 71, 437-440.

40.

52

41.

Jueco, N.L., Palaypay, M.A. & Aceremo, L. (1973). Prevalence and intensity of intestinal parasitism on Talim Island, Binangonan, Rizal, Philippines. Southeast Asian Journal of Tropical Medicine and Public Health 4, 582-587. Oberst, R.B. & Alquiza, L.M. (1987). Survey of intestinal parasites on Palawan, Philippines. (1987). Southeast Asian Journal of Tropical Medicine and Public Health 18, 197-201. Yamamoto, R., Nagai, N., Kawabata, M., Leon, W.U., Ninomiya, R. & Kozumi, N. (2000). Effect of intestinal helminthiasis on nutritional status of schoolchildren. Southeast Asian Journal of Tropical Medicine and Public Health 31, 755-761.

42.

43.

53