ECOLOGY AND INFECTION RATES OF NATURAL VECTORS OF FILARIASIS IN TANAI-IINTAN, SOUTH KALIMANTAN (BORNEO), Soeroto ~tmosoedjono',~urnomo', Sutanti ~atiwa~anto', Harijani A. ~arwoto~,and Michael J. ~an~s'

Data ekologi nyamuk vektor &n tingkat infeksi filana secam ahmi &n secam buatan telah diperokh a2ui perkebunan karet di Kalimantan Selatan, Indonesia. Berbagai macam cam penangkapan &lam kondki ekologi yang berbeda telah dipakai dalam pengumpulan 51 jenis nyamuk (N = 95.735). Pembedahan nyamuk, infeksi buatan dan identijikasi larva jiIanMamengikuti prosedur dan kunci yang sudah baku. Infeksi filaria Brugia, Breinlia dan Cardiofilaria secara alami ditemukan pada nyamuk crassipes Dan' penelitian ini dapat dijelaskan hasil infeksi budan, kepadatan populasi nyamuk secara musiman dan perbandingan cam penangkapan nyamuk.

INTRODUCTION forest at approximately 25 meters elevation (Fig. 2). ~h~majorit~of the human population In September 1978, a collaborative study on the estate (245 persons), comprised of was begun in Tanah Intan, South Kalimantan approximately 60% resettled Javanese and 40% (Borneo), Indonesia by the Indonesian Ministry indigenous Banjarnese, derived their livelihood of Health and the U.S. Naval Medical Research from tapping rubber. Before initial mass Unit No. 2, Detachment, Jakarta, in order to treatment with diethylcarbamazine citrate define the role of feral and domestic (~ilarzan~),the infection rate for Bnrgia malayi as reservoir hosts for human filarial pathogens. in this human population was approximately (Fig. 1) The results of this study revealed that 29.0%. Wchereria bancmfti was not detected the domestic cat (Felis catus) and the Silvered in the blood sampled. At eight months post- leaf monkey (Presbytis cristata) were hosts for treatment the infection prevalence decreased both Brugia malayi and Brugia pahangi.(1'2'3'4) to 2.4% (20 ul fingerprick blood, 250 Additionally, it was also found that li cristata individuals) and decreased further at 14 months harbored three other species of filariid post-treatment to 1.6% (N = 191). At 24 nematodes, namely, Wuchereria kalimantani, a months post-treatment the infection rate had Cardio rlaria s p . and Dirofilan'a magnilar- increased to 4.9% (N = 314), presumably vatumL2) (Table 1). because of a resurgance in transmission. The study area consisted of a rubber This report includes information on the estate (1,680 hectares) (3" 20' S, 115" 02' E,) adult ecology and infection rates of vector surrounded by small rice fields and secondary mosquitoes in the defined study areas.

1 U.S. Naval Medical Research Unit No. 2, Box 3, Unit 8132 APO AP 96520-8132 2 The National Institute of Health Research and Development, Ministry of Health, Jakarta, Indonesia

BuL Penelit Kesehat 21 (2) 1993 Figure 1. Location of study site (Tanah Intan) in South Kalimantan, Indonesia.

Tabel 1. Infection rate of hosts for filariid nematodes in South Kalimantan (Borneo), Indonesia.

Number (%) positk for Host and Location Number Brugia Brugia Wuchereria Cardionlaria Dirofifaria Examined malayi pahangi kallmantanl magnilarvatum

Prosbytis cntstala Tanah Intan 106 22 (20.8) 5 (4.7) 36 (33.9) 1 (0.9) 1 (0.9) Felis catus L. Barabai 144 2 (1.4) 23 (16.0) - - - Pengiuran 18 - 3 (16.7) - - Sungai Siepai 23 - 11 (47.9) - - Tanah Intan 102 2 (1.9) 8 (7.8) - - -

TOTAL 287 26 (9.1) 50 (17.4) 36 (12.5) 1 (0.4) 1 (0.4)

from Palmieri et. at (24)

Bul. Penelif. Kesehaf. 21 (2) 1993 MATERlALS AND METHODS Ecology The general ecological settings in the area Collection of study have been descriied el~ewhere.(''~) Mosquitoes were captured in-various Mosquitoes were trapped at 7 routine ecological settings using battery-operated CDC surveillance collecting sites within the study light traps and modified Tliidad-type traps area. Four areas used wooden platforms built baited with either monkey, cat, or C02 (dry ice).@) Baited Trinidad-type traps were in trees at 15 and 25 meters above ground level suspended from large trees using a rope and with pulley systems between trees for pulley system at either 1-3 meters, 9-12 meters suspending and retriving traps (Fig. 2). These or 15-21 meters for 12-hour periods. collecting sites included the following Collection of human and monkey biting environmental interfaces: ricefieldlforest, mosquitoes were made during the day swamplforest; riverinelforest; rubber forest; (06.00-18.9 and night (18.00-06.04 from either dense secondary forest; riverinelvillage; rubber temporary huts built of bamboo and banana village; and open-village. leaves at ground level or from wooden platforms built in the canopy at 15-25 meters above ground Specimen Preparation level (Fig. 2). Biting and landing mosquitoes Collected mosquitoes were transferred to were collected from human volunteers or caged paper holding cups for identification and silvered leaf monkeys (Presbytis cristata) using dissection within the following day. Mosquitoes mouth aspirators. Within the central village were anesthetized with chloroform and electricity was supplied to the estate director's identified to species based upon morphological home, from 19.~to allowing the viewing characters. Because of the close similarity in of a television, made available to the villagers. morphology, Mansonia bonneae and Mansonia During this period, landing and biting dives were pooled as one group. Mosquitoes mosquitoes were collected using mouth were dissected for filarial infections,(6) and aspirators from the TV. viewing audience. semi-permanent mount preparations of a Daily rainfall data was collected on site representative sample of early stage and and tabulated to monthly totals. No attempt infective larvae were made.(7) Initially, grouped was made to measure temperature or humidity species were dissected in pools of 15-50 in saline changes at the macro or micro-environmental solution (0.85%) and microscopically examined levels. Based on local meterological data, for all developing forms of filaria. Subsequent monthly temperature extremes are slight and capture of species previously found positive for are principally a reflection of amounts and filariid larvae, were individually dissected and frequency of seasonal precipitation. examined for infection rates.

Bul. Penelit Kesehal 21 (2) 1993 3 DANAU .BUNDAS

S

A PLATFORM A . ~i~u&2. Study Site depicting villages and platform locations in Tanah Intan.

Experimental Infections compared with those larvae recovered form A sakple of the infective larvae recovered natural infections with the exception of from individually dissected mosquitoes were Wucherena kalimantani where the natural either injected intraperitoneally or sub- vector was not yet known. cutaneously into domestic cats (Felis catus) and mongolian jirds (Meriones unquiculatus) for Filariid Larvae Identification observations on experimental develop- ment.(6'8'9) Experimentally developed fiariid larvae were examined in accordance with the Laboratory-bred adult female mosquitoes, technique described.('') Identification of 2-3 days after emergence, were fed on hosts various larval stages to genus or species were with known filarial infections. Female based upon established taxonomic mosquitoes were allowed to sugar-feed 2 days before blood feeding and thereafter as desired. Microfilaria Fully fed mosquitoes were grouped and dissected every 24-48 hours to recover first, Microfilariae (mff) were recovered from second and third-stage developing filaria larvae blood and/or intraperitoneal fluid of (Table 5). Larval forms were morphologically experimentally infected jirds. Blood and

4 Bul. Penelit. Kesehat. 21 (2) 1993 Ecology and infection rate9 ...... Soeroto A. eta1

intraperitoneal fluid was either smeared on glass fields. In areas where the canopy provided slides, air dried, dehemoglobinized, air dried, partial covering, Cq. crassipes could be collected fixed with absolute methanol and stained in using sweep nets in the heavy bush undergrowth. Giemsa (pH 7.2) or placed in 2% buffered This species was seldom collected in formalin (modified Knott technique) and unprotected open village areas. stained with methylene Identi- fication was made using available taxonomic Elevation. The majority of Cq. crassipes keys. were collected from the mid-to-upper-level collection sites of the canopy (9-21 meters) RESULTS except in cases where monkey bait was used (Table 3). Nearly 70% of the Cq. crassipes Collections attracted to monkeys were at the 1-3meter level. Of the 95,735 mosquitoes collected and Bait Preference. During January to examined from September 1978 through November 1979, human and cat baited traps November 1979, 9 genera (Coquillettidia, were placed together in a variety of locations 47.1%; Mansonia, 24.8%; Culex 24.5%; at various elevation. Of the Cq. crassipes Anopheles, 2.4%; Aedes, 0.8%; Umnotaenia, collected, 58.6% preferred cat bait while 41.4% Aedeomyia, Annigeres, and Ficalbia, 0.4%) and were attracted to the human bait. In collections 51 different species were identified (Table 2). made between November 1978 and June 1979, Only Mansonia uniformis, Ma. bonneae, Ma. a comparison between human and monkey bait dives, and Coquillettidia cmssipes were found revealed that 65.6% of the Cq. crassipes were harboring developing fdariid larvae. Only these attracted to monkeys while only 34.4% four species will be described herein. preferred humans. Of the 27,883 Cq. Coquillettidia crassipes Van der Wulp 1881 cmssipes examined, 193 (0.7%) were positive Coquillettidia crassipes was the most for 873 infective stage larva of Cardiojilaria sp. (4.6 larvaelinfectivemosquito). No other filariid commonly trapped mosquito, representing species were recovered from Cq. crassipes. 29.1% of the overall collections, irrespective of Rainfall and Seasonal Fluctuation. From bait used or season trapped. October 1978 through November 1979 the Habitat. Cq. crassips was most often percent population of Cq. cmssipes trapped, collected throughout the day and night in relative to all species collected varied by 10.9 forested areas where the canopy provided either to 40%. In general, the overall percentage partial or full coverage. This included rubber trapped dropped following periods of highest forest, secondary forest, village forest fringe, rainfall and increased during periods of lowest and forested and village areas bordering rice precipitation. (Table 4)

BvI. Penelit. Kesehat. 21 (2) 1993 5 Emlog+ and infeetioa rsta -..-.. Soemlo A et.01

Tabel 2. Mosquitoes from Tanah Intan, South Kalimantan.

AEDES 1. Ae. albopictus Cc gelidus 2. Ae. lineatopennis Cx. quinquefasciatus 3. Ae. novoniveus Cc (pipiens) spp. 4. Ae (par) spp. Cc fuscocephala 5. Ae. vms Cx. sinensis 6. Ae Cfin) spp Cc vishnui 7. Ae (par) spp Cc pseudovishnui Cc ochracea Cx. nigropuctatus Cr. (sitiens) spp Cx. mimulus AEDEOMYIA Clw. hutchinsoni 1. Ae. catastica Cr. whitmorei

COQUILLETITIDIA MANSONIA 1. Cq. ochracea 1. Ma. annulata 2. Cq. crassipes 2. Ma. annulifera 3. Cq. nigrosignata 3. Ma. uniformis 4. Cq. hdgkini 4. Ma. indiana 5. Cq. aureosquamata 5. Ma. bonneae 6. Ma. dives URANOTAENIA SP. ARMIGERES 1. Ar. kuchingensis 2. Armigeres sp. FICALBIA SP.

ANOPHELES 1. An. aconitus 8. An. kochi 2. An. barbirostris 9. An. tessellatus 3. An. nigem-mus 10. An. pujutensis 4. An. peditaeniatus 11 An. separatus 5. An. maculatus 12. An. campestris 6. An. vagus 13. An. minimus 7. An. umbrosus 14. An. letifer

Bul. Penelit Kesehat 21 (2) 1993 @coIowand infection raca .-...... Socroto A aal

Tabel 3. Comparison of percentages of Coquillettidia crassipes, Mansonia bonneaeldives and Ma. unifomis collected at various elevations using various bait attractants.

cq. crpssiprs Elevation (metes) €02 Cat Human Monkey 1-3 23.7 37.3 324 68.2 19-12 41.9 - - - 15 - 21 34.4 62.7 67.6 31.8

Ma. bomeac/d~vts

1-3 11.7 32.5 46.2 37.0 9- 12 46.4 - - - 15 - 21 41.9 67.5 53.8 63.0

Ma udfonnis

1-3 38.5 66.8 66.1 63.8 9 - 12 27.7 - - - 15 - 21 33.8 33.2 33.9 36.2

Mansonia bonneae Edwards 1930 Elevation. This species group showed no Mansonia dives (Schiner) 1868 strong preference, although the majority Adult Ma bonneae and Ma dives are trapped while using animal bait (53.8%- 68.5%) morphologically very similar and were grouped were found in the upper levels of the canopy together for practical and statistical purposes. (12-21 meters). Between 32.5% to 46.2% of They were the least common of the filaria vector Ma bonneaeldives were collected at ground mosquitoes trapped but the fourth most level (1-3 meters) while using animal bait common species collected, representing 9.2% (Table 3). of the overall collections. Ma. bonneaeldives were collected throughout the year at all Bait Prefer- During January to elevations. November 1979 collections from human and cat bait, placed together in a variety of ecological Habitat. Both species were collected both settings at various elevations, showed that 70.9% day and night most often in forested areas heavily or partially covered by canopy. In of Ma. bonneaeldives were attracted to human forest/village areas, Ma. bonneaeldives were bait while only 29.1% were attracted to cat bait. trapped near human and animal dwellings. At During November 1978 and June 1979, when night they would be found feeding in open human and monkey bait preferences were village areas unprotected by the canopy as well compared, it was found that 91.5% of Ma. as inside dwellings. These species were seldom bonneaeldives were attracted to humans while found in open rice fields or swamps. only 8.5% were attracted to monkey bait.

Bul. Penelil Kesehul 21 (2) 1993 7 Table 4. Comparison of Coquillettidia crassipes, Mansonia bonneaddives and Ma. uniformis with overall collections due to influence of seasonal variation and rainfall fluctuation (September 1978 - November 1979). Eedojg and infeetion rata ...... Soeroto A &a1

Infection Rates. A total of 8,785 Ma. bait (Table 3). This affinity for animal and bonneaeldives were examined of which 3 were human bait was independent of the elevation found positive for 5 larvae (L3) of Bmgia sp. of capture. during January 1979. No other filariid species Infection Of the nearly 16,500 Ma. were recovered from this species group. uniformis examined, 7 were found positive for Rainfall.From 13L3 larvae of Bnrgia sp. In addition 1specimen December to February (rainy season) was found infected with a single L3 of the genus populations of Ma. bonneaeldives were at Breinlia . their maximum. The overall percentage of In populations trapped (14.4%- 22.5%) increased general, the overall percentage of population following periods of increased rain and during of Ma. uniformis trapped dropped following peak rains (410-630 mmlmonth). Conversely, periods of highest rainfall and increased when populations decreased to 4.5% in March and rainfall was below 300 mmtmonth (Tible 4). 0.1% in October during the dry season (35- During October and November of 1979, 325 mmtmonth) (Table 4). following periods when rainfall fell below 100 mmtmonth, no Ma. uniformis were collected.

Mansonia unifonnis Theobald 1901 Exnerimentalm fections MMosauitoes Mansonia uniformis was most often Table (5) summarizes results from trapped during the wet seasons, and accounted laboratory reared mosquitoes allowed to feed for 17.2% of the overall collections. It was the on infected hosts of Brugia malayi, Brugia third most commonly trapped mosquito and the pahangi and Wuchereria kalimantani. All most commonly trapped vector of Brugian mosquitoes were fed once on infected blood filariasis. This species showed the highest and maintained under controlled laboratory preference for human and/or animal bait. conditions. Mosquitoes were dissected 10-12 Habitat. This species was most often days post-infection. collected from early evening through Mansonia uniformis was shown to mid-morning in villages with open canopy and support B. pahangi and B. malayi, whereas, with heavy bush and banana groves. During the Aedes aegypti was completely refractory to both. evening, Ma. uniformis was commonly found Four species of Anopheles were tested, and in the open village areas where it accounted with the exception of An. vagus, all were found for over fifty percent of all mosquito species susceptible to a limited degree to Brugia andlor collected. W kalimantani. The role these anophelines play in the transmission of these parasites to natural Bevatim. 63.8% to 66.8% of all Ma. and human hosts is unknown. uniformis were collected at 1-3 meters in elevation, regardless of the animal bait used All results reported herein should be considered preliminary in scope because in most (Table 3). This species was also present at 15-21 cases the number of mosquitoes tested was meter elevations. (33.2%-36.2% ). small. Conclusive observations can onlv be Bait Preferen=. Ma. uniforjnis was reported after repeated experimentation and equally attracted to human, cat and monkey further field work.

Bul. Penelit Kesehat. 21 (2) 1993 9 Eoolojg and bfrclion nto I---.. Saaolo A ad

Tabel 5. Results of mosquitoes experimentally exposed to hosts with known filariid infections.

DISCUSSION . .. Errors. .in Fll- Previous Vector Studies. Over the past Vector. All to commonly these 100 years, many detailed studies and authors have encountered situations where L2 and/or infective L3 filariid larvae have been comprehensive reviews concerning the vectors ascribed to a human infecting fiariid species of human and animal filariasis in and without previous specific morphological Indonesia have been reported.('4915916917)The characterization. Bird, amphibian, reptile and majority of the reports concerning vectors of mammal infecting filariids are much more Brugian and Bancroftian fiariasis originated widespread than commonly realized (29,30,31,32) from Peninsular ~ala~sia('~j~~)and East and can be confused with developing larvae ~ala~sia(~~,~l).Several reports have combined of either Brugia or Wircherena. For example, reviews of past vector studies with original Table 6 (NAMRU-2, unpublished data) vector data from Southeast ~sia('~), summarizes the variety of filarial worms and ~ala~sia(~~'~~'~~)and ~ndonesia.(~~~~~~~) A vectors from various locations in South comprehensive bibliography of medical Kalimantan found between 1977 and 1979. In parasitology in Indonesia provides a large this study, 193 Cq. crassips were found positive number of early reports of human and animal for 873 filariid larvae, all identified as fiariasis from the Dutch East Indies and the Cardiofilana sp. on direct examination or Malay archipelago.(28) confirmed by experimental feeding. This

10 Bul. Penelit. Kesehat. 21 (2) 1993 mosquito vector was not observed to harbor tim~ri.(~'~~~)This and other unpublished other species of fdariae. Piessens et aL(33)listed surveys have so far failed to detect B. timori Coquillettidia sp (presumably Cq. crassipes as as a natural parasite in Kalimantan. Wxthout an important vector of Brugia malayi from the detailed morphologic descriptions and same areas as the present study. Partono et experimental studies of sympatric third-stage al.(34) also lists Ma. cmssipes ( = Cq. cmssipes) developing larvae common to animals and man as a vector of B. mdayi in two areas of West in a given area, attempts at specific Kalimantan. Unfortunately, in neither case do identification will yield, at best, suspect results. the authors report how species identification The N-1 Vectprs. Because of the was determined. However, this is not to say recent changes and refinements in mosquito that this species can not play a role in Brugia , accuracy of earlier vector transmission. Based on laboratory and field identifications are questionable, especially observations Chiang et al.(35*36)concluded that in an endemic area with high densities of Cq. when original specimens are no longer available crassipes, it could act as a secondary vector of for examination.(29) Brugian fdariasis in Peninsular Malaysia. Most authors agree that the principal In this study we found no significant natural vectors ofBrugiapahangi and B. malayi morphological difference between third-stage within the Southeast Asian area are either larvae of B. malayi and B. pahangi and would Mansonia unifomis, Ma. bonneae, or Ma. dives find it little more than speculation to place a although Ma. indiana, Ma. annulata, Anopheles species determination on these larvae. During barbirosb-is An. nigenimus and An. campestris this investigation, careful indentification of have also been implicated in 1ndonesia.(17) Brugia microfdaria and developing larvae were From this investigation it can be concluded made regarding the possible presence of Brugia that: 1) man, cat, and silvered leaf monkey are

Tabel 6. Mosquito host-range for filariid larvae (natural infection) in South Kalimantan, 1977 - 1979.

Genus/Speeies Breinlia Bntgia Cardio- Dim- Pele- Setaria Unknown spp filaria filaria citus

Ma annulata + + + Ma annutifera + Ma bonneaddives + + Ma indiana + + Ma uniformis + + + + Cq. crassipes + + + + An. nigerrimus + + An. peditaeniatus 4-

BuL Penelit Kesehat 21 (2) 1993 11 the primary definitive hosts for Bmgia WUCHERERL4 KALIWTANk Ae&s tog04 infections. The silvered leaf monkey also serves Anopheles subpictus and Culew quinque- as host for Wuchereria kalimantani and farcicrtus (Ll, L2). Dirofilaria magnilarvatum, and possibly As illustrated in table (6) much work Cardiofilmio sp., 2) Coquillettidia cmssipes was remains to be done in order to unravel the the most commonly caught mosquito from the complex zoonotic and epidemiologic area studied, being found in areas partially to relationships between parasite, vector and fully covered by canopy, at all elevations, and humans. Much of the work so far described was attracted to cat, monkey, and human bait. is preliminary and thus requires more intensive The population density of Cq. crassipes investigations and follow up. As new and increased during periods of low rainfall and existing filarial parasites of animals and humans captures harbored only Cardiofilana sp. 3) are studied, efforts must continue in elucidating Mansonia bonneae and Ma. dives were the their life cycle, vectors and possible epide- least commonly trapped vector species but was miological implications. found at all elevations, in areas both heavily and partially covered by canopy and in ACKNOWLEDGEMENT forest-village localities unprotected by the This study was supported by the canopy. The population density of Ma. Indonesian National Institutes of Health bonneaeldives increased during periods of high Research and Development and the Naval rainfall. Both species, as a group, were Medical Research and Development preferentially attracted to humans and Command, Navy Department, for Work Units harbored species of Brugia. 4) Mansonia ZF51.524-009-0085 and 3M161102BS13. uniformis was the third most commonly AD410. trapped mosquito and the most commonly The opinions and assertions contained trapped vector of Brugia. It was most often herein are those of the authors and are not collected in village areas during the night at to be construed as official or reflecting the views of the Indonesian Ministry of Health, the 1-3 meter elevations. Ma. uniformis was equally Navy Department or the U.S. Department of attracted to animal and human bait all Defense. elevations. The population density of Ma. Reprint requests to Publications Office, unifomis increased during periods of low U.S. Naval Medical Research Unit No.2, rainfall but decreased when rainfall fell below Kompleks LITBANGKES R.I. J1. Percetakan 100 mmtmonth. Ma. uniformis harbored Negara No. 29 Jakarta 10560. species of Brugia and Breinlia. 5) Preliminary In conducting research using animals, the observations on experimental intermediate investigators adhered to the "Guide for hosts for the following filariae included: Laboratory Animal Facilities and Care" of the BR UGIA sp.: Aedes togoi,Anopheles nigern'mus, Institute of Laboratory Animal Resources, An. barbirostris, Armigeres subalbatus; National Research Council (revision, 1978).

Bul. Penelit KesehaL 21 (2) 1993 and infedion rata -...-. Soeroro A daI

REFERENCES Nelson, G.S. (1%0). The identification of filarial .larvae in their vectors. Ind. J. Mal. 14:585-592. 1. Palmieri, J.R, Purnomo, Lee, V.H., Dennis, D.T., Marwoto, H.A. (1980). Parasites in the silvered leaf WHO (1987). Control of lymphatic filariasis. A monkey, Prcsbytls cristatus Eschscholtz 1821, with manual for health personnel. World Health a note on a Wuchereria-like nematode. J. Parasitol, Organization, Geneva, 89 p. 66:170-171. Sivanandam, S and Mak, J.W. (1975). Some 2. Palmieri, J.R, Purnomo, Lee, V.H., Dennis, D.T., problems associatedwith the processing and staining Marwoto, H.A. (1980). Filariid parasites of South of blood film for filaria diagnosis. Journal of Medical Kalimantan (Borneo) Indonesia. Wuchereria Health and Laboratory Technology of Malaysia. kallmanlani Sp. N. (Nematoda: Filaroidea) from 2:4-6 . the Silvered Leaf Monkey Prcsbyiis cristatus Eschscholtz 1821. J. Parasitol, 66:645-651. Hawking, F. (1973). The distribution of human filariasis throughout the world. I1 Asia. WHO 3. Masbar, S., Palmieri, J.R, Marwoto, H.S., Purnomo mimeograph WHO/FIU 73.114. and Darwis, F. (1981). Blood parasites of wild and domestic animals from South Kalimantan (Borneo), Sasa, M. (1976). Human filariasis. A global survey Indonesia. South East Asian J. Tmp. Med. Pub. of epidemiology and control. Univ. Tokyo Press, Hlth. 12(1):4246. 819 p. 4. Palmieri, J.R, Masbar, S., Purnomo, Marwoto, H.A., Lie, KJ. (1970). The distribution of filariasis in Tirtokusumo,S. and Darwis, E (1985). The domestic Indonesia. A summary of published information. cat as a host for Brugian filariasis in South Southeast Asian J. Trop. Med. Pub.Hlth. 1:366-376. Kalimantan (Borneo), Indonesia. Journal of Helminthology, 59:277-281. Lim, B.L., Kurniawan, L., Sudomo, M., and Arbain, J. (1985). Status of Brugian filariasis research in 5. Sommerman, K.M., and Simmet, R.P. (1967). Versatile mosquito trap. Mosq. News 27412417. Indonesia and future studies. Bul. Penelit. Kesehatan. 13(2):31-55. 6. Ramachandran, C.P. (1970). A guide to methods and techniques in filariasis investigations. Bull. Inst. Laing, A.B.C., Edeson, J.F.B., and Wharton, RH. Med. Res. Fed. Malaya, 15:39 p. (1960). Studies on filariasis in Malaya: The vertebrate hosts of Brugia malayi and B. pahangi. 7. Wharton, R.H. (1959). A simple method for Ann. Trop. Med. Parasitol. 54:92-99. mounting and preserving filarial larvae. Bull. Wld. Hlth. Org. 20:729-730. Laing, A.B.G., Edeson, J.F.B., Wharton RH. (1961) Studies on filariasis in Ma1aya:further experiments 8. Ramachandran, C.P., Sivanandam, S. (1970). on the transmission of Brugia malayi and Experimental studies on the transmission of Wuchereria bancrotti to the domestic cat. Wuchereria bancrofli. Ann. Trop. Med. Parasitol, Southeast Asian J. Trop. Med. Pub. Hlth. 1:150-152. 55:86-92.

9. Palmieri, J.R., Connor, D.H., Purnomo, Dennis, Barclay, R (1969). Filariasis in Sabah, East Malaysia. D.T., Marwoto, H.A. (1982). Experimental Ann. Trop. Med. Parasit. 63473488. Infection of Wuchereria bancrofli in the silvered leaf monkey Presbyli crbtatus Eschschlotz 1821. Hii, J.L.K., Kan S., Chin, ICE and Chan M.RC. J. Helmintol. 56243-245. (1984). Anopheles (Cellia) balabacensis Baisas is 10. Lowrie, R.C. Jr., and Eberhard, M.L. (1980). A new a vector of Wuchereria bancrofti in Sabah, technique for immobilizing filaria larvae using Malaysia. Trans. Roy. Soc. Trop. Med. Hyg. dimethyl sulfoxide (DMSO) J. Parasit. 66169-170. 78:281-282.

Bul. Penelit. Kesehat 21 (2) 1993 Eedogi and infeetion rater ..-.-....Soemto A eLal

Wharton, RH. (1960). Studies on filariasis in Dissanaike, A.S. (1979). Zoonotic aspects of filarial Malaya, field and laboratory investigations of the infectious in man. Bull. Wld. Hlth. Org. 599-357 vectors of a rural strain of Wucbereria bancrofli. Ann. Trop. Med. Parasit. 54:78-91. Nelson, G.S. (1%5) Filarial infections as zoonoses. J.Helminth. 39229-249. Wharton, RH. (1962). The biology of Mansonin mosquitoes in relation to the transmission of Piessens,W.F, McGreevy, P.B., Piessens, P.W., filariasis in Malaya, Bulletin No. 11, Institute for McGreevy, M., Koiman, I. V., Saroso J.S. and Dennis Medical Research, Malaysia, 114p. D.T. (1980). Immune Responses in Human Infections with Brugia malayi. J. Clin. Invest. Wilson, T. (1961). Filariasis in ~ala; - a general 653172-179. review. Trans. Royal Soc. Trop. Med. Hyg. 35:107-134. Partono, E, Djakaria, Oemijati, S., Joesoef, A., Clarke, M.D., Cole, W.C., Lien J.C. and Cross, J.H. Brug, S.L. (1928). Fiariasis in Nederlandsch-Indie (197). Filariasis in West Kalimantan. Southeast 1. Geneesk. Tijdschr. Nederl.-Indie, 68:681-704 Asian J. Trop. Med. Pub. Hlth., 8549563.

Lie, KJ. and Rees, D.M. (1958). Filariasis in Chiang, G.L., Samarawickrema, W.A., Mak, J.W., Indonesia: distribution, incidence and vectors. Proc. Cheong, W.H., Sulaiman I. and Yap H.H. (1986). Int. Congr. Trop. Med. Malaria, Lisbon, 11:360. Field and laboratory observations on CoquiUettidia crassips in relation to transmission of Bmgia Lim, B.L. (1985). Distribution of Brugia malayi in malayi in Peninsular Malaysia. Ann. Trop. Med. relation to landscape ecology, resewoir hosts and & Parasit. 80:117-121. mosquito vectors in Indonesia. Trop. Biomed. 2:34-39. Chiang, G.L., Samarawickrema, W.A., Eng, KL., Cheong, W.H., Sulaiman, I., and Yap, H.H. (1986). Lim, H.K. (1974). .Bibliography of medical Field studies on the surveillance of Coquiilettldia parasitology in Indonesia (1855-1968). U.S. Naval crassipes (Van der Wulp) and the isolation of a Medical Research Unit, Taipei, NAMRU-2-SP-36: strain of CardioNaria in Peninsular Malaysia. Ann. 111-125. Trop. Med. & Parasit. 80:235-2c14.

Edeson, J.F.B. and Wilson, T. (1964). The Purnomo, Partono F, Dennis, D.T. and epidemiology of filariasis due to Wuchereria Atmosoedjono, S. (1976) Development of the Timor bancrolti and Brugia malayl. Annual Rev. filaria in Aedes togoi : Preliminary observations. J. Entomology, 9245-268. Parasitol; 62:881-885.

Nelson, G.S., Hiesch RB. and Furlong M. (1962). Purnomo, Dennis, D.T., and Partono F. (19n) The Studies in filariasis in East . 11. Filarial microfilaria of Brugia timori (Partono et al, 1977 infections in man, animals and mosquitoes on the = Timor microfilaria, David and Edeson, 1964): Kenya coast. Trans. R. Soc. Trop. Med. Hyg. Morphologic description with comparison to Bmgia 56:202-217. malayi in Indonesia J. Parasitol; 63:1001-1006.

Bnl. Penelil Kesehal 21 (2) 1993