STATUS OF COMMENSAL ----BORNEDISEASES RESEARCH IN INDONESIA

Lim Boo ~iat', Singgih sigit2, and Tuti R. ~adi~.

ABSTRAK

Rodents yang terdapat di rumah-rumah maupun di lapangan mempunyai peranan penting dalam penyebaran penyakit terhadap manusia dan binatang. Dalam tulisan ini disajikan peninjauan kembali literatur tentang penyakit-penyakit yang ditularkan oleh binatang, seperti : plague, scrub and murine typhus, leptospirosis, schistosomiasis, angiostrongyliasis, yang biaya terdapat di Indonesia.

INTRODUCTION mensal rodent studies for plague, on the other hand, is a national health problem, The "commensal " are those and is maintained as one of the priorities rodents that live in close proximity with in communicable diseases control pro- man and his surroundings. There is little grammes. Apart from this, there are very information on the distribution and bio- little research activities done on commen- logy of the commensal rodents inhabiting sal rodents and their parasites in relation urban areas in Indonesia. Rodent studies to public health importance in the coun- by many past workers (to quote a few try. of the important ones) were foccused in This paper reviews literatures on some rural areas, and on those rodents with of the rodent-borne diseases of zoonotic economic pest importance1 -5, while low importance based on past and present priority was given to rodents of public activities undertaken, and also suggests health importance except plague. The further research activities on its zoonotic only piece of work which mentioned implication leading to preventive mea- rodents of urban areas was dme6. Com- sures for future action.

COMMENSAL RODENTS

The commensal rodents can be divided into domestic and field rodents as shown below.

Domestic Field -

Rattus norvegicus Sewage argentiventer Rattus r. diardii Roof rat Rattus tiomanicus Wood rat Mus muscu1us House mouse Rattus exulans Palynesian rat Bandicota indica

1. WHO, P.O. Box 320 Jakarta, Indonesia. 2. Chairman of the Post-graduate Medical Entomology Programme, Faculty of Graduate Studies, Bogor Agriculture University, Bogor, Indonesia. 3. Head of & Acarology Section, National Institute of Health Research and Development, Jakarta, Indonesia.

4 Bul. Penelit. Kesehat. 14 (3) 1986 Status of commensal . . . . . Lim Boo Liat et al.

Domestic rodents: The Sewage rat, Asia and the pasific islands. It is a highly R. norvegicus (Berkenhout, 1796), origi- adaptable species and is not only found nally a native of northern Eurasia, has in the fields but also occurs indoors. spread to cities around the world by com- It is an agricultural pest in 1ndonesia5. merce. In Indonesia this species is com- The large bandicoot, Bandicota indica mon in all seaport cities. The roof rat, (Bechstein, 1800), widely distributed R. rattus diardii (Linnaeus, 1785), native throughout the oriental region, is patchily in Asia is represented by many subspe- distributed in Indonesia, and has been cies within different regions of Southeast shown to be a pest in sugar plantation Asia. This species is restricted to human (unpublished data). habitations in cities and villages throug- hout the country. The house mouse, RODENT-BORNE DISEASES M. Musculus Linnaeus, 1766, originally from Eurasia and nothern Africa, is now Rodent-borne diseases are classified an introduced species throughout the amongst the zoonotic diseases, i.e. "an rest of the world. This species is equally infection or an infections disease trans- as common as Rattus mttus and is confi- missable under natural conditions from ned to indoors only in cities, town and vertebraternimals to man". In Indonesia villages in the country. the more common rodent-borne disease encountered and received attention are Field rodents: The ricefield rat. R. plague (bacterial disease), leptospirosis argentiventer (Robinson & Kloss, 1916), (spirochaetal disease), scrub typhus and occurs throughout the major land mass murine typhus (rickettsial disease) and of the Sunda region including Malaysian angiostrongyliasis and schistosomiasis mainland. It is common in lowland rice- fields throughout Indonesia, and is a (helrninthic diseases). serious agricultural pest5. The wood rat, Bubonic plague is transmitted to humans by the bite of an infected flea, the R. tiomanicus (Miller, 1900), with distri- butional pattern similar to that of R. handling of infected rat tissues, or contact argentiventer, is an important pest in with the pus from an infected rat (Fig. 1). oilpalm estates in Indonesia5. The poly- Scrub typhus is transmitted to humans through the bites of infected larval chig- nesian rat, R. exulans (Peale, 1848), is gers in the fields (Fig. 2). Murine typhus,, widely. distributed throughout Southeast

- By infested tissue by bit. of intsct.d fI.1 -.

Flea inhsrmd with Versima postis Through r.servoir host

from patient Fig. 1. Transmission cycle of human plague

Bul. Penelit. Kesehat. 14 (3) 1986 Status of commensal . . . . . Lim Boo Liat et al.

Fig. 2. Live-cycle of Trombiculid mites and its mode of transmission.

also called shop typhus, is found where bite or any other fresh skin wound (Fig. people and occupy the same buildings. 3). Leptospirosis is usually a water-borne Transmission occurs through the faeces, disease, with infection by contact with deposited on the skin while the infected water, moist soil or vegetations cantami- flea feeds. The infectious agent (Rickett- nated with the urine of infected . sia typhi) enters through the site of the

6 Bul. penelit. Kesehat. 14 (3) 1986 Status of commensal . . . . . Lim Boo Liat et al.

Bul. Penelit. Kesehat. 14 (3) 1986 Status of commensal . . . . . Lim Boo Liat et al.

Penetration is though abraded skin of contacts is by ingesting insufficiently mucous membranes or from ingestion of cooked snails, land crabs and prawns, food contaminated with the urine of or through contaminated raw vegetables infected rats (FIg. 4). Angiostrongyliasis (Fig. 5). With the latter parasite, infection and schistosomiasis are transmitted to is from water containing larval forms human through molluscan intermediate (cercariae), and these penetrate the skin hosts. With the former parasite, human (Fig. 6).

t gets infected by

acting contaminated Eating contaminated food. food or through ----+

-- - Direct contact with spirochaete in infected urine of reservoir hosts.

urine of rat oist soil and vegetatio -g Penetration of spirochaete in abraded skin while walking in moist soil.

Penetration of spirochaete in

abraded skin while swimming or

wading inforest stream. or in ricefield. Water

Fig. 4. Life cycle of Leptospirosis and its mode of transmission to man

Bul. Penelit. Kesehat. 14 (3) 1986 CARRIERS HUMAN INFECTION

/Infective larvae which/ \

reach young adultho Digestive Tract &nd aftsr two first-stage larv more weeks sta are expelled laying eclcls wifh the faeces 1 Brain First-stage larvae infec a molluscan inte

Fig. 5. Life cicle of Angiostrongylw c antonensis and its mode of transmission to man. Status of commensal . . . . . Lim Boo Liat et al.

Bul. Penelit. Kesehat. 14 (3) 1986 Status of commensal . . . . . Lim Boo Liat et al.

PAST RESEARCH ACTIVITIES western central Java and east central Java (1892 - 1970) in the 1920's. From 1910 to 1920, a total of 240,375 plague deaths were Plague: Plague was brought into Java reported in ~ava~-l~.In 1922, plague- by infective rats, and/or fleas in cargoes like cases were reported in Makasar (Sula- of rice imported into the eastern seaport wesi) and Palembang (Sumatera) but no of Surabaya in November 1910. Additio- deaths were recorded. Prevalence of the nal importations are suspected in the disease, decreased steadily after the seaports of Semarang in 1916, Cirebon in 1930's except for some violent revivals of 1923 and Tegal 1927. Epidemics first the infection in central Java in late 1904,s were confined to east Java, then the and early 1950's. Further reduction in disease spread to southern central Java infected territory and decline in the num- within a few years (Surakarta in 1915 ber of cases continued until, by the late and Jogjakarta in 1916). Either as multi- 19507s, plague was restricted to two ple invasions westward progression of the mountainous zones (Wonogiri and Boyo- original infection, or both, plague reached lali) in the Surakarta Recidency (Fig. 7).

Flea vector : Reservoir Hosts ;

XenopsyIIa cheopis R*s exu I ans -r. diardii 0 st ivalius COcInatuS R&u s - Oa a-s Neopsylla sondiaxs O 0 00 .; 0 0:-

\ Incidence of human plague outbreaks from bagelang 1911-1970 in West, Central and East Java \ Indonesia.

G

E.ndemic plague foci in SELO and CEPOGO subdistricts only Activities ; Yearly surveillance for humac Year and rodent/ fleas --= denotes plague introduced and spread. Fig. 7. Human plague distribution in Java

Bul. Penelit. Kesehat. 14 (3) 1986 Status of commensal . . . . . Lim Boo Liat et al.

These two foci accounted for more than Weil's disease. Serum of this patient was two-thirds of all recorded human cases serologically tested and shown to be posi- of plague on the island1 3-14. The oriental tive with the sero-type indentified as rat flea, Xenopsylla cheopis, and the roof Icterus febrilis27. In subsequent years rat, R.r. diardii were incriminated as the more human sera were obtained from sus- vector and reservoir hosts of plague in pected cases in Jakarta and Surabaya of java13-14, 15-19 West and East Java, and serolo ical results From 1960 to 1968 no activities of showed the same sero-type2'. (Anony- plague surveillance were carried out in mous, 1895). Serum examination of a Java. However, plague flared up twice suspected person in Jakarta again, and it more in the Boyolali in two subdistricts was positive with sero-type which he of Selo and Cepogo in 1968 (102 cases, named it as Leptospira icterohaemoglo- 43 deaths) and again in 1970 (10 cases, binura 2 9. Following these positive cases, 2 deaths). During the 1968 outbreak, the further surveys found 196 cases in West Provincial Government in Central Java Java (Jakarta, Sukabumi, and Sindang- together with the National Communi- laya), 34 in east Java (Surabaya) and 18 cable Diseases Control (CDCIJakarta) and in Central Java Semarang)30-33. In Su- United States Naval Medical Research matera (Deli, Senembuh My, Simau, Unit-2 (NAMRU-2) carried out mass vac- Bangkinang, Bangka & Belitung) 532 cination of the populace and DDT dusting cases were found to be serologically posi- for fleas in houses of the infected areas. tive29> 34-38. In East Kalimantan (Sing- Surveillance on human cases and rodent/ kawang, Tarakan) 35 positive cases were fleas was subsequent followed up by the reported27-29, and 26 cases in Sulawesi Provincial Government. (~akassar)~~.Among these infected ca- Scrub typhus and Murine typhus: ses, 78 persons died of the disease. During Scrub typhus was first reported in north this period, a total of 842 people were sumatera2O. Later the disease was found found positive with the disease from Java, in Kalimantan and Irian ~a~a~~-~~.Most Sumatera, Kalimantan, and Sulawesi, and of these human cases were symptomatic, with a mortality rate 9.2%. There was no and some were serologically diagnoses. report of cases from other islands in the The aetiological agent, Rickettsia tsutsu- country. Four Leptospira sero-types gamushi was isolated from blood of two namely, L. inchterohaemo rrhagiae, L. patients in ~akarta~2. R. tsutsugamushi bataviae L. javanica and L. australis were was also isolated from pools of the vector identified. chigger, Leptotrombidium (L.) deliense Domestic rodents and wild bats were andL. (L.) flet~heri~~.Murine typhus, on also examined. In West and Central Java the other hand, was reported in Jakarta (Jakarta, Bogor, Semarang and Ambara- through the isolation of the agent, R. wa) 31.4% of 363 Mus musculus, 6.7% of typhi from domestic rat, R. norvegicus 30 R.r. diardii, 21.2% of 104 Rattus r. and R.r. diardii, oriental rat flea, X. cheo- brevicaudatus (=Rattus argentiuenter), pis, and also from the chigger, Ascos- 23.6% of 72 R. roquei (=R. tiomanicus) choengastia indica 2 5 -2 6. Since then there and 0% of 26 R.r. diardii Were reported33, was no work done on these two diseases 41-45. In Sumatera (Pangkalpinang) 19.8% until the 1970's. of 111 Mus musculus and 6.7% of 89 R.r. Leptospirosis : Human leptospirosis diardii positives were reported37, and in was first reported from a soldier in Jakar- Sulawesi (Makasar) 7% of 350 Mus mucu- ta who showed signs and symptoms of lus were also reported to be positive46.

Bul. Penelit. Kesehat. 14 (3)1986 Status of commensal . . . . . Lim Boo Liat et al.

Rodent leptospirosis studies showed musculus were each found with all the 7 that the infection rates were higher in sero-types, and two sero-types were from field rodents with 21.2% of 104 R. argen- RX. diardii, and 3 from R. tiomanicus tiventer and 23.6% of 72 R. tiomanicus (Table 1). Bats of the genus, Cyazopterus infected than in domestic rodents with were also examined, and some positive 14.1% of 824 M. musculus and 6.3% R.r. bats were shown to be infected only with diardii. Seven sera-types of leptospira sero-type L. cynopteri47 -4 8. were identified. R. argentiventer and M.

Tabel 1. Results of Leptospira sero-types found in man and animals spp. by past resenrch workers from 1892 to 1964.

Bul. penelk. Kesehat. 14 (3) 1986 13 Status of commensal . . . . . Lim Boo Liat et al.

Domestic cats and dogs surveyed in sy from the same patients" Based on the Jakarta (west Java) showed 9.8% of 794 finding, a stool survey was conducted in cats examined were positive with anti- the Lindu Lake area and S. japonicum bodies of L. bataviae, L. icterohaemorrha- eggs were found in 8% of 234 human giae and L. ja'vanica32~ 49-51. Of 296 samples. Further surveys revealed a pre- dogs examined from Medan (Sumatera), valence rate of 53% of 468 stool Sam- Jakarta (West Java) and Makasar (South pled55, and resurveyed of the Lindu Sulawesi), 21.6% were positive with L. Lake area found S. japonicum infections bataviae, L. javanica, L. icterohaemorrha- in 26% 347 people sarnpled58. Adult giae, L. canicola and L. pomona52-53. schistosomes in humans, dogs and wild Farm animals, i.e. swine, sheep, goats, deer found5 were considered closely water buffalo, horses, dairy and beef related to the classical form of S. japo- cattle; the sera of these animals were nicum60. The identification was only serologically tested with the various based on the morphology of the adult leptospira antigents. Positive reactions worms without doing a complete 'life- against L. pomona were found in 75% cycle study of the parasite, as the inter- (596 animals) buffalo sera, 52.7% (317) mediate host (snail) had not yet been beef cattle, 30.4% (79) swine and 14.5% found at the time. No study on the ro- (586) dairy cattle. One of 33 swine sera dents as potential reservoirs of the para- showed a reaction against L. bataviae, sites was carried out. These historical while 2 of the same sera were positive studies established the identity of the for 1. mitis and L. australis were found in 2 parasite and recognised the public health of 20 horses sera, and 1 each of the same importance of this disease, endemic to sera reacted wainst L. canicola. L. ictero- the Lindu Lake areas of Central Sulawesi. haemorrhagiae, L. pomona and L. wolfii. Angiostrongyliasis : Human cases of One of 30 goat sera was positive with eosinophilic meningoencephalitis, with L- pyrogenes5 4. suspected etiology due to Angiostrongylus Leptospira of 17 serotypes were deter- cantonensis, were reported from North mined in these studies (Table 1). Among sumateraGI-62. Subsequently, adult them, the commonest serotypes encoun- worms of A cantonensis were recovered tered in man and his commensal and in domestic and field rats (Rattus r. diar- domestic animals were L. icterohaemorr- dii and R. argentiventer) in the same area, hagiae, L. bataviae L. pomona, L. conicola. further substantiating the suspected etio- L. javanica and L. australis. The leptos- logy in the human cases63. pirosis studies carried out by past scien- tific workers showed that the disease was PRESENT RESEARCH ACTIVITIES common in man as well as in wild and (1970 - 1985) domestic animals. During this period studies on rodent- Schistosomiasis: This disease was first borne disease were re-initiated by the nati- reported in Indonesia in 1937 following onal scientists in the Health Ecology Rese- the discovery of a human case in Palu, arch Centre (HERC) of the National Insti- Central Sulawesi55. The patient was a tute of Health Research and Development 35 years old male from Tomado in the (NIHRD) and Subdirectorate of Zoonosis Lindu Lake area. In the same year, the of the Communicable Disease Control eggs of Schistosoma japonicum were (CDC) in collaboration with the United identified in tissue section taken at autop- States Naval Medical Research Unit-2

Bul. Penelit. Kesehat. 14 (3) 1986 Status of commensal . . . . . Lim Boo Liat et al.

(NAMRU-2), WHO Regional Projects on on rodents in relation to the plague trans- Schistosomiasis (SEAROIIND and on mission cycle from 1972-1974. During plague 0099), and WHO Interregional this study a detailed vertical host distri- Project of Vector Biology and Control bution in the plague endemic focus area Research Unit-2 (VBCRU-2). was mapped (Fig. 8). R.r. diardii and R. Plague: Since 1970 no further plague exulans were confirmed in the involve- outbreak has occurred in the previously ment of the infectious plague cycle, as endemic areas on Central Java. However, isolation of the pathogen (Yersinia pestis) CDC in collaboration with WHO Regional from the organs of these rodents were Project carried out an ecological study madeG4.

-KEY f Padi Rice Samiran 1500m v Upland Rice 0 Dry Field Crops A Village llt Bamboo 9 Fruit Trees Acacia Trees Common Uncommon

--R.RATTU3 3. MURINUS R. EXULANS -R TIOMANICUS K. NIVIVENTER R, ARGENTIVENTER -M.CERVICOLOR 6. INBICA --C. NOTATUS C. GLIROIDES

Fig. 8. Host distribution in the Boyolali plague focus, Central Java, Indonesia.

Bul. Penelit. Kesehat. 14 (3) 1986 Status of commensal . . . . . Lim Boo Liat et al.

Based on studies on ecological distri- rat flea, Xenopsylla cheopis as vectors of bution, patterns of movement and the the plague focus area. A third species, reaction of the plague pathogen in these Neopsylla sondiaca was the most common rats, the field rat, R. exulans was found and widespread flea, occurring both in to be resistant to the pathogen, and it houses and fields at elevations below 1000 was concluded that this species functions metres. Above 1000 metres, X. cheopis as the primary reservoir maintaining was confined mainly to houses, S. cognaa- plague. The house rat, R.r. diardii, on the tus and N. sondiaca were the common other hand, was shown to have low resis- species in the field at all elevations. Posi- tance or nearly complete susceptibility tive isolations of Y. pestis were acquired to the pathogen, thus making it a poor from S. cognatus and X. cheopis infesting reservoir during interepidemic periods. R. exulans and R.r. diardiis5. The results R.r. diardii, thus probably functions of these studies on the dynamics of the mainly as an amplifying host for the plague transmission cycle from sylvatic pathogen during outbreaks64. through peridomestic to domestic habitats Past workers incriminated a field are illustrated in Fig. 9 a--c respectively. flea, Stivalius cognatus and an oriental

-Flea transmission

ENZOOT lC . - --,Direct transmission MAINTENANCE CYCLE

cognatus sondaica / cognatus sondaica-- i I *------*

Rattus niviventer

Fig. 9.A. Potential components of the plague tramsisslon cycle in sylvatic habitats.

Bul. Penelit. Kesehat. 14 (3) 1986 Status of commensal . . . . . Lim Boo Lia.t et al.

SYLVATIC I 1 $ HABITAT

cognatus sondaica 4 / cognatus - -- .------+ Field attus exulans \

-Flea transmission - - - -Dirrct trhmission I CROPLAND - Fig. 9.B. Potential components of the plague transmission cycle in peridomestic habitats. PERIDOMESTIC I 1 1 CROPLAND

-. Flea transmission ------c Direct transmiss~on

--_----

Fig. 9.C. Potential components of the plague transmission cycle in domestic habitats. . . Bul. Penelit. Kesehal. 14 (3) 1986 Status of commensal . . . . . Lim Boo Liat et al.

In 1978 CDCIJakarta, CDCISemarang, three insecticides tested. The third field HERCIJakarta and WHO/VBCRU- 2 Ja- flea, N. sondiaca, was found highly sus- karta jointly conducted a two months ceptible to DDT67. Prior to this insec- survey of the rodents and fleas in the ticide susceptibility test of fleas in the plague focus area. In human domiciles plague focus area, a field trial of feni- 611 animals (R.r. diardii, R. exulans, R. trothion, malathion and DDT against tiomanicus, Suncus murinus) were exarni- flea from R.r. diardii in three villages ned. Of these, 93.3% was the predominant in West Java was carried out. The field house rat, R.r. diardii. In field environs areas had similar ecological biotypes to 197 rats (R. exulans, R. tiomanicus, R. that of the plague endemic focus area in niviventer) were examined, and R. exu- Central Java. The results revealed that lans, comprised 90.9% of the total catch. malathion dust at 5% was effective con- Three flea species (X. cheopis, S. cog- trolling X. cheopis up to 15 weeks, while natus, N. sondiaca) were found infesting 5% fenitrothion dust effective for 19 these domicile and field . The weeks, and DDT at 5% was not effec- flea population on animals in human do- tive68 . miciles comprised of 47.9% X. cheopis, In 1982-1983 CDCIJakarta and CDC/ 51.8% S. cognatus and 0.3% N. sondiaca, Semarang, assisted by WHO/VBCRU-2, while that in the field environs was 2.2% conducted surveillance studies again for a X. cheopis, 80.7% S. cognatus and 17.1% period of 12 months. A total of 411 pools N. sondiaca. The field flea, S. Cognatus of organs of R.r. diardii, R. exulans and S. was shown to be relatively more Common murinus from human domiciles and fields in the field than oriental rat flea, X.cheo- were isolated, and one pool of 3 R.r. diar- pis in human domiciles. dii was bipolar positive and gram negative, and this was confirmed as Y pestis. Isola- Attempts to isolate plague bacillus tions of 385 pools of fleas, X. cheopis, from 70 pools of three flea species and S. cognatus and N. sondiaca, none were 129 pools from the small mammals from positive. Negative results were also obtai- both human domiciles and field environs ned from 74 pools of bats. Serological yielded negative results. Serological stu- tests for plague antibody in 1723 sera dies of plague antibody in organs of 120 of rodents species, and 107 sera of dogs, small mammals also gave negative re- 34 cats and 229 bats also gave negative sultsG6. At the same time 197 human sera results. were tested, and only two were positive A total of 32,664 people, comprising with low titres. These two positive were of 67.3% adults and 32.7% children of old plague cases from the 1970 outbreak. both sexes from 283 subvillages in the During the same period laboratory p@ue focus area, were medically exami- susceptibility tests with 4% DDT. 0.5% ned. Of these 0.14% (47) people showed malathion, 1.O% fenithrothion and 0.2% symptoms of fever, and sera from these dieldrin* against the three flea species fever cases were taken for serological were carried out. The field flea, S. cog- tests, and only one was positive. This natus, which was highly susceptible to one has a low titre of 1:20 who was an malathion in 1972, was found to be resis- old plague case from the 1968 outbreak tant to it, but susceptible to the other (Kusharyono et a1 - unpublished). The three insecticides. The oriental rat flea, results of the survey revealed that altho- X. cheopis which was previously found ugh no new human plague case was detec- to be highly resistance to DDT, was less ted but infection in rats still l occurs. In resistant, but susceptible to the other view of the finding of positive isolates in

18 Bul. Penelit. Kesehat. 14 (3) 1986 Status of commensal . . . . . Lim Boo Liat et al. rats, control measures were carried out Leptospirosis : A recent surveillance against fleas with 10% DDT treated in study was carried out jointly by NAM- the subvillages where the positive rats RU-2 and NIHRD- They examined 186 were found. In addition, mass vaccination patients from Jakarta hospital who suf- of the populace in the plague focus area fered from fevers of unknown origins. was undertaken. Urine and blood were obtained on admis- sion from all, but second convalescent Scrub and Murine typhus: Scrub ty- specimens were obtained from only 138. phus vector studies were recently intensi- Fourteen patients died, and 34 were dis- fied. To date 69 species of chiggers have charged before second specimens could been identified, including 7-Leptotrombi- be obtained. Nine patients had evidence dium spp. Four of the Leptotrombidium of past infection with leptospirosis based spp. were confirmed as vectors of R. tsut- on microscopic serum agglutination test sugamushi, and of these L. (L.) deliense titres at dilution of less than 1:400 against and L. (L.) fletcheri were found to be serotypes: L. Hebdomadis (1 person), widely distributed. Thirty-three namma- L grippotyhposa (I), L. australis (I), lian hosts, comprising of 3 insectivores, L. batavie (I), L. icterohaemorrahagiae 3 primitive primates, 23 murids, 3 squir- (I), L. pyrogenes (2) and L. putoe (2). rels and 1 carnivore were shown to be The results showed only 2 of 186 febrile hosts of Leptotrombidium chiggers. De- hospitalized patients in Jakarta had lep- tails of this disease are dealt with in a tospirosis, one with serotype L. agrip- separate paper. Studies of murine typhus potyphosa and the second with L. hata- in human and rodents were also reinitia- ted. Seven hundred and twenty-two hu- viae 70 man sera were collected in different parts During an epidemic of jaundice, of the country and tested using the indi- thought to be caused by viral hepatitis, rect immunofluorescence technique. Anti- NAMRU-2 and NIHRD did a study at bodies of murine typhus were found in the end of 1967 and early 1968 in the 10% to 20% of the sera from Java and province of South Sumatera. Sera from Sumatera, but less than 2% in sera from 259 people were serologically tested. Of islands east of Java69. Since 1977 sero- these 18.1% were positive. Nine leptos- logical studies on rodent murine typhus pira sero-types were determined, and have been intensified by NIHRD, WHO/ among these the highest leptospira agglu- VBCRU--2 and the University of Mary- tination titres against these sera were land, U.S .A. Preliminary results revealed L. australis, L. grippotyphosa, L. ictero- that murine typhus was quite prevalent haemorrhagiae and L. hebdomadis which- in the domestic rats (R.r. diardii, R. nor- also were the most common serotypes71. vegicus) and low in the field rats. The Fifty-three domestic rats ( R. argenti high prevalence of murine typhus anti- venter and R.r. diardii) were also exami- bodies in the domestic rats supports the ned in South Sumatera. Kidney cultures theory that the infection involves indoor of two were positive, L. javanica and L. commensal rodents rather than those in batavie only. River water cultures detec- their natural outdoor environments ted Leptospira which were not identi- (Unpublished data). fied71.

Bul. ~enGlit.Kesehat. 14 (3) 1986 Bul. Penrlit. Kesehat. 14 (3) 1986 Status of commensal ...... Lim Boo Liat et al.

Comprehensive leptospirosis surveys in ted with'human disease were more com- wild mammals comprising 49 species were mon in the commensal rodents. Infection examined (Table 2). Most of the infected of sylvatic mammals was usually by Lep- animals were the domestic rat, R. norve- tospira serotypes of leeser human impor- gicus; field rat, R. argentiventer and R. tance. exulans; and 13 leptospira sero-types A geographical distribution map of were determined. These recent studies Leptospirosis infection in man and ani- indicate that Leptospirosis is quite preva- mals is presented in Fig. 10. lent in Indonesia and is an infection com- mon among the domestic and field ro- dents69. The leptospira serotypes associa-

Tabel 2. Results of attempted isolation and serology of leptospires of species in Indonesia (Modified from Table by Van Peenen et al., 1971).

Isolation Serology - - - Type of animals Number Number Number Number Numebr Number of spp. tested positive Serotypes of spp. tested Positive Serotypes

DOMESTIC RAT Rattus noruegicus 1 20 14 bataviae (7); 1 18 3 javanica, javanica (5) ; bataviae unknown (2). R.r. diardii 1 96 1 bataviae 1 94 0 I in ictero- haemorrhagiae FIELD RAT R. argentiuenter 1 18 5 australis 1 76 1 R. tiomanicus 1 1 0 1 3 0 R. exulans 1 59 4 javanica 1 49 0

FOREST RAT 7 85 3 (2) javanica, 11 136 2 (1) bataviae canicola FOREST SQUIRRELS 3 3 0 451 bataviae FOREST SHREW 1 5 0 2 7 0 HOUSE SHREW 1 5 0 I 20 1 javanica FOREST CARNIVORES 5 11 0 14 3 (3) australis, bankinang, trassovi. FOREST HERBIVORES 2 2 0 3 4 0 MONKEY 1 1 0 1 0 0 BATS 10 48 0 17 171 8 (3) copenhageni, sejroe, meda- neinsis, butem- bo, cynopteri.

+ Total 35 383 27 49 597 19

Note : Figure in parenthesis denotes number of species infected.

Bul. Penelit. Kesehat. 14 (3) 1986 2 1 Status of commensal . . . . . Lim Boo Liat et al.

Schistosomiasis : Studies of this disease domestic cattle, field and forest rats, have reactivated. The high prevalence of wild hoars, wild deer and wild cattle S. japonicum in the human was reconfir- were incriminated in the life-cycle of med'' 2-7 4, The molluscan host was found S. japonicum in the foci areas of Lindu in Lindu valley75, and subsequently des- valley, Central Sulawesi. cribed as a new subspecies of Oncome- lania, namely 0. hupensis lindoensis76 A pilot control project was carried out and the life-cycle was determined77 (Fig. in Lindu, using mass treatment with 6). The finding of this new subspecies of Ambilhar (R) at 25 mg kg body weight snail led to the discovery of the first and snail control by mollusciciding, focus of 0. hupensis in paku area. After using Byluscide (R) at dosage rates of the discovery of the snail focus, subse- 10 - 40 ppm in addition to agroenginee- quent surveys confirmed another focus of ring method and environmental sanita- schistosomiasis. Several schistosomiasis tion. The results of these control mea- studies in Lindu Valley were carried out sures, although it had taken some effect, to determine the density of 0.h. lindo- was not significant78. In later years, ensis, seasonal variation in snail, infec- mass treatment with Praziquantel at tion rate and the type and prevalence of dosage of 60 mg kg body weight was S. japonicum in wild and domestic ani- carried out in Lake Lindu. The results mals78 . showed significant reduction of preva- lence rates from an average of 15% pre- Animals surveys revealed S. japonicum treatment to 2% six months post-treat- infesting 10 or more mammal species, ment80-gl, and in Napu Valley, the pre- in addition to man, namely: R. exulans, valence was reduced to 2.5% post-reat- R hoffmani, R. chrysocomus rallus, R. ment from a range of 43 to 79 % pre- marmosurus, R. celebensis, Cervus tio- treatments2. It was apparent from these morensis, Sus scrofa, domestic cat (Felis two studies, Praziquantel is now the drug cattus), domestic dogs (Canis familaris) of choice for the treatment of S. japoni- and Viverra tangalunga79. Mammal sur- cum in the endemic area. veys have been geared to determine the The past and present studies confirmed distribution and infection rates in ro- and reconfirmed that the disease\ is ende- dents, principally R. exulans, which mic in the Lindu valey and Napu valley inhabit the cultivated lowlands of the in Central Sulawesi valley and 11).Con- disease foci in the Lindu area. Routine trol and preventive measures and research fecal examinations of wild and dornes- activities currently are undertaken by tic animal showed that domestic dogs, CDCIJakarta, CDC/Provincial and NIHRD .

Bul. Penelit. Kesc.hat. 14 (3) 1986 Status of commensal . . . . . Lim Boo Liat et al.

.

Bul. Penelit. Kesehat. 14 (3) 1986 Status of commensal . . . . . Lim Boo Liat et al.

Angiostrongyliasis : Following the dis- Three molluses have so far been incri- covery of Angiostrongylus cantonensis in minated as intermediate hosts of A. canto- commensal rodents by Kwo & Kwo nensis. They are the African giant snail (19681, another lungworm, A. malaysi- (Achatina fulica), the veronicellid slug ensis was discovered from R.r. diardii (Laevicaulis alte), and the large freshwa- in Medan, North sumaterag3. Both SPe- ter operculate (Piala scutata). These mol- cies of parasites in domestic and field luscs were confirmed as the maintaining rats at Baturaja Transmigration areas in hosts of A. cantonensisgl. With the fin- South Sumatera were found84. The latter ding of the molluscan intermediate host lungworm may have been implicated in led to the study of the life cycle of this the cases of eosinophilic meningitis62. parasite (Fig. 5). Since 1974 intensive rodent surveys for The first and only confirmed cases of these parasites in Java and Sumatera were angiostrongyliasis in Indonesia was recen- carried out, and results showed that two tly reported92. A. cantonensis was reco- species of domestic rats (R.r. diardii, R. norvegicus), four species of field rats vered intact from the interior chamber (R. exulans, R. tiomanicus, R. argentiven- of the left eye of a 23 year-old woman ter, Bandicota indica) and two species of from Semarang, Central Java. forest rats (R. bartelsii, K. lepturus) were The distribution of A. cantonensis and reservoir hosts69, 83, 85-90. A. malaysiensis in Indonesia is shown in Fig. 12.

Suspmctsd Human Cases A cantonmnsls

Sabah &rnalays8ens1s

Conf~rmnd Human Case of A cantonensls

Fig. 12. Geographic distribution of Angiostrongylus cantonensis and Angiostrongylus malaysiensis in Indonesia.

Bul. Penelit. Kesehat. 14 (3) 1986 Status of commensal . . . . . Lim Boo Liat et al.

FUTURE RESEARCH ACTIVITIES tancy or susceptibility to these insecti- sides. This can be carried out during the BACTERIAL DISEASE period when animal surveillance is being Plague: Since 1970 there has been no conducted. human plaque outbreak, however, rese- 4. Human surveillance: Passive human arch and surveillance activities after surveillance should be carried out in Selo 1970 in the plague focus areas, found and Cepogo subdistricts by the Health positive isolation of Yersinia pestis in centres there. the field rodents, R. exulans, and its 5. Rodent and flea survey other than fleas, S. cognatus in 1973. Positive iso- the plague focus areas: Spot surveys in lation of the plague bacillus was again some previous known plague endemic obtained from the house rats, R.r. diardii areas in West Java (Ciweday, Gunung in 1983. All these positive animals were Cireme) and East Java (Gunung Bromo) isolated cases which were found in restric- should be carried out once a year. ted subvillages in plague focus areas. Leptospirosis: It was apparent from In the human surveillance, 3 positive cases the past and present research surveillan- were found in 1978 and 1983 who were ce activities that the disease in man old plague cases in the 1968 and 1970 and infections in anitmals are widespread plague outbreaks, and no new cases were throughout Indonesia. The infection has detected. The presence of the plague agent been shown to be very common among being occasionally encountered in the the commensal and domestic animals in house and field rats indicates that plague Indonesia, and serotypes found in them still pkrsists in the rat reservoir hosts in are more commonly associated with the plague focus areas, thus surveillance human disease, while infection of sylvatic studies need to be continued as follows: mammals is usually by Leptospira seroty- 1. Animal surveillance: CDCIJakarta pes of lesser human importance. The and the Provincial Government in Central high prevalence of infection of man's Java will continue rodent and domestic animals and his associated wild animals, and wild animal surveillance. Animals suggests that more surveys of this disease there will be trapped, and together with in man should be carried out although its fleas will be processed for serological that the disease has not cause any drama- and isolation studies of plague bacillus. tic incidence since its discovery in 1892 in Indonesia. 2. Rat falls: The look out for dead rats can be arranged by community partici- I. ~nimalsurveillance : During rodent pation through the Public Health Services activities undertaken by either CDC/Ja- in the focus areas. The observation should karta or NIHRD/Jakarta in relation to be carried out by the Chief and his villa- other diseases, or by Port Authorities, ges, they sliould report them to the Health sample of.these rodents should be made Centres there and the latter in turn should for leptospirosis investigation. report to the Regency and Provincial 2. Human surveillance: Examination of government and subsequently notified the hospital patients with fever of unknown CDCIJakarta. origin (FUO) and those suspected with 3. Flea susceptibility test : Susceptibi- viral hepatities may serve to uncover more lity to impregnated papers of DDT, Mala- leptospirosis cases. thion and fenitrothion of rodent fleas 3. The bulk of the work carried out du- should be carried out to assess the resis- ring the past and present activities were

Bul. Penelit. Kesehat. 14 (3) 1986 Status of commensal . . . . . Lim Boo Liat et al.

concentrated in four main islands of bodies or R. mooseri in rodent hosts Indonesia, i.e. Java, Sumatera, Kaliman- to map out the distribution and preva- tan, and Sulawesi. If possible, surveillance lance of infection in these rodent hosts. work on animals and human should be This work can be carried out together extended to other islands as well to further with existing rodent activities under- map out the distribution and prevalence taken on plague, scrub typhus and rodent of this disease to ascertain its public control programmes by the NIHRD, CDC/ health importance. Jakarta, and Port Authority in the coun- try. Salmonellosis: Salmonellosis is an in- fection of man and animals with orga- nisms of the genus Salmonella. It is also HELMINTHIC DISEASES commonly known as infections food-poi Schistosomiasis : Under the working soning. There are different serotypes of group for filariasis and schistosomiasis Salmonella organisms infect a variety (Pokja Filariasis and Schistosomiasis), of domestic animals, poultry, wildlife headed by Dr. M. Sudomo of HERC, and rodents. Two of these serotypes S. NIHRD in Indonesia, follow-up research enteritidis and S. typhimurium are com- activities to be carried out jointly with mon infections to commensal rats and NIHRD/CDC/University, Jakarta are as mice. In Indonesia domestic rodents follows : (R.r. diardii, K. norvegicus and Mus 1. Research on the transmission dyna- musculus) are potential reservoir hosts of mics of schistosomiasis of man, and ani- these organisms. The organisms are mal reservoir hosts in the endemic areas. excreted in their droppings and urine 2. Laboratory studies on the mollus- and the disease is transmitted to man can host, Oncomelania hupensis lindoen- when rat contaminated food is eaten. sis to assess the life-span of the snail, Food poisoning is a common hazard in and pathogenicity in various animal hosts man throughout the world and is no (wild and laboratory-bred) exception in Indonesia. The close- asso- . ciation of these domestic rodents with 3. The modified Karto technique for man probably may warrant some caution stool examination at present is still not on this disease. very efficient to determine the infected cases, thus it is essential to investigate the most effective and practical method and also more effective serological tech- RICKE'ITSIAL DISEASES niques for diagnosis in mass survey of Scrub typhus and murine typhus: schistosomiasis. Scrub typhus or tsutsugamushi disease 4. The endemic area in Central Sula- is dealt with in its respective section. wesi is extensive (35,000 ha). A small Murine typhus studies by past and present part is cultivated, and the snail interme- activities indicate that the disease, al- diate hosts are found in the cultivated though uncommon in human, but infec- area as well as in the forest. Compare to tion to domestic rats (R. norvegicus, Mus endemic area in other countries, Lindu muscullus and R.r. diardii) were shown and Napu valleys are unique, because to be more common that what used to relative extensive area is inhabited by only think otherwise. Efforts should be made about 7000 people. In such and endemic to find out more about the epidemiology area snail control is not practicable and of this disease, and surveillance of anti- even impossible. Praziquantel is the choi-

26 Bul. Penelit. Kesehat. 14 (3) 1986 Status of commensal . . . . . Lim Boo Liat et al. ce drug shown to be very effective for an (2) if found not pathogenic to man it mass treatment in the area. Thus, control may be interesting to investigate the measures in the endemic area could be possible antagonisms between S. incogni- achieved by persistant treatment with tum and S. japonicum for a possible bio- the drug coupled with health education logical control method. and simple environmental- changes, such Angiostrongyliasis : 'l'he rat lungworm, as sanitation and hygiene, minor physical Angiostrongylus cantonensis and A. ma- changes in habits, etc. laysiensis, etiological agent of human 5. Sample of schisto- cases, with or eosinophilic meningitis are primarily para- without hepato-splenomegaly should be sites of rodents. Human infection is acci- examined physically and serologically, dental. The fact that only a single authen- before and after treatment, to see whe- tic human case caused by one of these ther the treatment can give improvement worms reported since its discovery of to the health of the patients. these parasite in 1968, indicates that this 6. Immunological study to characterize disease is not a public health importance; the humoral state of infected persons, the parasites and its geographical distri- serum 1gG and IgM should be measured bution in Indonesia are considered as in a sample of schisto-cases pre- and post parasites of medical importance only. treatment. Changes in these parameters Other helminths such as, cestodes can be correlated with the clinical picture Hymenolepis nana and H. diminuta, tre- as well as with changes in egg output. matodes Echinostoma ilocanum, E. mah- For the characterization on cell-mediated yanum, and E. lindoense, and nematodes immune response, blood for lymphocyte Trichinella spiralis are common infections transformation should be drawn from a of domestic and field rodens93 Most of sample of cases with or without hepatos- these parasites are also known to be pa- plenomegaly . thogenic to man579 94-98. Rodents do not play an important role in the direct 7. Further identification of the parasite transmision of these parasites to man. species by isoensyme genetic : studies, Like Angiostrongyliasis, they are para- kartotype and karo-systematic and elec- sites of medical importance only. Howe- tron microscopic studies of the S. japoni- ver search for these parasites in commen- cum in the endemic area are needed to sal rodents should be carried out in con- assess whether there is any strain diffe- nection with other rodent studies to find rences between the Indonesian and other out the prevalence of infections. Asian strains.

CONCLUSION Schistosomia incognitum is a parasite common among the commensal rodent Rodents play an important part in the in 1ndonesia79. This parasite has been spread of many diseases of man and do- shown to infect rodents in the schisto- mestic animals. Among rodents species, somiasis endemic area in Central Sulawesi. the "commensal rodents" which live in In one instance S. incognitum was found close proximity with human environ- in copala with S. japonicum in R. exu- ments, pose a greater threat to man of lans79. Further research on the possible the diseases they carry. All the seven of hybridisation between those two worm commensal rodent species found in Indo- species is essential to (1) whether the nesia, are also widely distributed to hybrid is pathogenic to man or animal, neighbouring Southeast Asian countries99 .

Bul. Penelit. Kesehat. 14 (3) 1986, Status of commensal . . . Lim Boo Liat et al.

Of the seven species, Rattus norvegicus, forest rodent species are also hosts of R.r. diardii and Mus musculus live inside scrub typhus. These rodents harbour houses of human habitations, and the seven scrub typhus Leptotrombidium po- other four, R. argentiventer, R. tiomani- tential vectors, and among these two, cus, R. exulans and Bandicota are field L. (L) deliense and L. (L) fletcheri, were rodents adjacent to human environs. incriminated as vectors. For murine ty- Among these field rodents, R. exulans phus, house rodents, R. novegicus and sometimes invades domain of human habi- R.r. diardii were involved as reservoir tations also. hosts only. The vector of murine typhus Diseases carried by these commensal is the oriental rat flea, Xenopsylla cheopis rodent can be broadly classified into bac- commonly infested these rodents. terial, rickettsial and helminthic diseases. Field and house rats are also common Plague and leptospirosis are the two com- reservoir hosts of some of the helmin- mon infections among the bacterial di- thic diseaseloo. Schistosomiasis, endemic seases which were very thoroughly inves- in Central Sulawesi, forest and field ro- tigated in Indonesia. The field rat, R. dents, are reservoir hosts of the parasite exulans was incriminated as the foremost Schistosoma japonicum. The field rodent, important reservoir host in the plague R. exulans is the primary reservoir host foci area, and R.r. diardii, an amplying among the different rodent hosts incri- host of human domiciles. The flea .parasit- minated. Snail, Oncomelania hupensis es of these hosts, Xenopsylla cheopis and lindoensis is the intermediate host of the Stivalius cognatus were confirmed as the parasite. In the case of S. incognitum, plague vectors64-65 . For leptospirosis, a parasite of rodents, the field rat, R exu- the house rodents involved were Mus lans is the important hosts. For Angios- musculus, R.r. diardii and R. norvegicus; trongyliasis, 8 rodent species were reser- the field rodents were R. argentiventer voir hosts of the parasites, Angiostrongy- and R. tiomanicus. In addition to invol- lus cantonensis and A. malaysiensis. ment of rodents, cats and dogs were also Among the rodent reservoir hosts, two found to be important reservoir hosts house rats, R.r. diardii and R. novegicus, of this bacterial disease. Leptospira of and 4 field rats, R. exulans, R. tiomani- 17 serotypes were isolated from these cus, R. argentiventer and Bandicota indica houses and field rodents, including cats, are important reservoir hosts of these dog, and human. parasites. The intermediate hosts are ter- Another common bacterial disease is restrial and fresh water molluscs. Other Salmonellosis where house rodents are helminths such as, cestodes Hymenolepis potential source of transmission. They nana and H. diminuta, trematodes Echi- are R. norvegicus, R.r. diardii land Mus nostoma ilocanum, E. malayanum and E. musclus, There are different serotypes of lindoense and nematode Trichinella spiralis Salmonella organisms typed, two of these are common infections of house and field S. entefitidis and S. typhimurium are rats. common infections to these house rodents. The disease where commensal rodents play a primary role in the transmission to Rickettsia1 disease, like scrub and mu- man are plague, leptospirosis, murine and rine typhus, the former disease involves scrub typhus, and angiostrongyliasis. Tho- field rodents only. They are R. argenti- se that play a tertiary role are diseases venter, R. tiomanicus, R. exulans and such as, salmonellosis, hymenolepsiasis, Bandicota indica. In addition, numerous echinostomiasis and trichinellosis.

Bul. Penelit. Kesehat. 14 (3) 1986 Status of commensal . . . . . Lim Boo Liat et al.

Commensal rodents are also involved 7. Janssen (1912) La peste in Java. Le in some viral diseases. The houses rats Caducee. August 24,220-222. R. norvegicus and R. rattus are known 8. Swellengrebel, N.H. (1913) Onderzoe- to be reservoir hosts of haemorrhagic kingen over de biologie van ratten fever with renal syndrome and rat-bite en vlooien en over andere onderwer- fever. Both these viral diseases are uncom- pen, die betrekking hebben op de mon in Indonesia. epiderniologie der pest of OstJava. Mede. burg. geneesk. Dienst Ned. Indie, 2, 90 pages. 9. ~wellengrebel,N.H. (1915) Uber die The graphics were made by Mr. E Enung Zahl der Flohe der Ratten OstJavas of the Medical Illustration Unit in NIHRD . 2. Hyg. InfektKr., 79: 492-510. We are most grateful to him. 10. Loghem, J.J. Van and Swellengrebel, N .H. (1914) Kontinuierliche und REFERENCES netastatische ~estverbreitung.2. Hyg. InfetKr., 3: 460481. 1. Otten, L. (1924) De pest op Java 11. Raadt, O.L.E. De (1916) Bijdrage tot (1911-1923). Mededeling van de de kennis der epidemiologie van de Burgelijken Geneeskundige Dienst., pest of Java. Meded. burg.geneesk 119-262. Dienst.Ned-Ind., 4: 20-28. 2. Meer oh< J.C. van der(1924) Uit 12. Stennis, P.B. Van (1923) Enkele gege- het intiene leven der. Javaansche vens over Loemopsylla cheopis en verrat (Rattus rattus brevicaudatus Pygiopsylla ahale in verband met de epidemiologie der pest. Geneesk. T Horst et de Raadt). De Topische Nu- Ned.Ind., 63: 570-596. tuur, 1: 46-52. 3. Goot, P. van der (1942) Over levens- 13. Karamoy Warouw (1959) Pandangan wijze en bestrijding van sawah rattan mengenai penjakit pes dan pembe- in het loagland van Java. Landbouw, rantasannya di Indonesia. Majalah 23: 123-394. Kedokteran Indonesia 5--9 : 7-264. 4. Rochman and D. Soekarna (1976) 14. Baltazard, M., and Bahmanyar, M. Penelitian umpan tikus dan tikus (1960) Recherches sur la peste a penempatannya di sawah. Laporan Java. Bull. Wld.HlthOrg., 23: 217- Kenzajuun Penelitian Seri Hama dun 246. Penyakit. No. 5 Lembaga Pusat Pene- litian Pertanian. 26. Gispen, R. (1950) The virus of murine 5. Dandi Soekarna, Sadji Partoatmodjo, typhus in mites (Schongastia indica, Wirjosuhardjo, and Boeadi (1980) farn. Trombiculidae). (Abstract). Problems and management of mam- Trop.Dis.Bul1, 47: 836-837. mals in Indonesia with special refe-- 27. Van Der Schroef, J.P. (1934) Ziekte rence to rat. Biotrop special Publica- van Weil in Centraal Borneo (Po- tion, 12: 35-53. roektjaoe. Gen. Tschr.Ned.Ind., 74: 6. Sody, H.J.V. (1930) Oversicht van de 500-504. ratten van Java. Zoologishe Medede- 28. Anonymous (1895) Verslag over de ling 13: 100-140. onderzoekingen verricht in het labo-

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landsch-Indische Rickettsiosis. Ge- 47. Collier, W.A., en E.H. Essevel (1938) neesk Tydech Med.Ind., 81: 238- Over een leptospira stam uit de her- 240. senen eener vleermuis. Med.D.Volks- 24. Blake, F.G., Maxcy, K.F., Sadusk, gez Ne.Ind., 27: 262-268. J.F., Kohls, G.M., and Bell, E.J. 48. Collier, W.A., en A. Mochtar (1939) (1945) Studies of tsutsugamushi En serologisch afwijkende leptospira- disease (scrub typhus, mite-borne stam uit de nier eener vleer-muis, typhus in New Guinea and adjacent GenTschr. Ned. Ind., 79: 226-231. islands). Epidemiology, clinical ob- 49. Van Lie, G.A. (1920) Weilsche xiekte servations and actiology in Dobadura (Icterus infectiosus) bij honden. Ned. area. Amer.J.Hyg., 41 :975--976. B1d.v. Diergen., 32: 327-329. 25. Gispen, R. and Warsa, R. (1951) 50. Van Lier, G.A. (1921) Weilsche Ziekte Endemic typhus in Java.11: The (Icterus infectiosus) bij honden. Ned. natural infection of rats and rat Ind.Bld.v. Diergen., 32: 327-329. ectoparasites; identity of shop ty- phus and murine typhus. (Abstract). 51. Esseveld, H. (1938) Bidragen tot het leptospira vraagstuk to Batavia naar 40. Smits, E. (1907) Ziekte van Weil op ann leiding van seroreacties met Tarakan (Borneo). Gen. Tschr.Ned. leptospirastammen bij 'Widal" sera. Ind., 72: 284-287. Ge.Tschr. Ned.Ind., 78: 2834-2839) 41. Hoesen, H.W. (1920) Verslag werk- 52. Kouwenaar, W., en J.W. Wolff (1929) zaamheden Geneesk. Laboratorium Honden als leptospira-dragers. Ne. te Weltevreden over 1919. GenTschr. Ind.Bld. v.Diergen., 41: 457459. Ned.Ind., 60: 352-357. 53. Mochtar, A., en W.A. Collier (1939) 41. Flu, P.C. (1921) Verslag werkzaam- Het leptospira-onder-zoek bij honden heden Geneesk. Eaboratoriurn te te Batavia. Ned.1nd.Bld.v. Diergen, Weltevreden over 1920. Gen. Tschr. 51 : 339-344. Ned.Ind., 61: 231-235. 54. Soeratno Partoatmodjo (1964) Penje- 43. Sardjito, M., en S. Postmus (1927) lidikan mengenai leptospirosis: Pen- Onderzoek naar het woorkomen van jakit zoonotik jang berarti bagi eko- leptospirae onder de ratten bevolking nomi dan kesehatan masjarakat di van Weltevreden. Gen. Tschr. Ned. Indonesia (Ph.D. thesis) Fakultas Ind., 67: 73--76. Kedokteran Hewan, Institut Pertani- an Bogor. 44. Mochtar, A. (1933) Over het voorko- men van de ziekte van Weil te Sema- 55. Muller, H. and Tesch, J.W. (1937) rang en omstreken. Gen.TschrJVed. Autochthone infectie met Schisto- Ind., 73: 1182-1186. soma japonicum of Cellebes. Ge- neesk. Tijdschr. Indie., 77: 2143- 45. Abdullah, N. (1961) Pemeriksaan ter- 2150. hadap leptospira pada tikus2 sawah. Rattus rattus rogui Sody. Skripsi 56. Brug and Tesch, J.W. (1937) Parasi- Universitas National, Djakarta. taire women and het Lindoe meer 46. Sardjito, M. (1929) Jaar verslag (0.a. Poloe, Celebes). Geneesk. 1928 Geneeskundig Laboratorium. Tijdschr.Nederl.Ind., 77: 2152- Gen.Tschr. Ned. Ind., 69: 861- 2156. 865. 57. Bonne, C. and Sandground, J.H.

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(1940) Bilharzia japonicum ann het flea-indices in plague endemic area Liqdoemeer. Geneesk.T.Ned.Ind., at Boyolali, Central Java, Indonesia. 80: 477481. Int. J.Zoonosis., 7: 1-14. 58. Buck, Von, A.A., And Uhrrnann, G. 67. Sustriayu, N., M. Sudomo, C. Kus- (1956) Untersuchungen uber den haryono and Lim Boo Liat (1980) gefall mit Echinostoma lindoense Susceptibility to DDT, malathion, un Schistosoma japonicum bei der fenitrothion and dieldrin of three Bevolkerung des Lindusees (Mittel flea species in the Boyolali plague Celebes). 2. Tropenmed. Parasitol. 7: endemic area, Central Java, Indone- 110-117. sia. Southeast Asian J.Trop.Med. 59. Bonne, C., Borstlap, A.J.P., Lie Kian Pub.Hlth., 2: 108-112. Molemkamp, W.J.J., and Nanning, 68. Lim Boo Liat, N. Sustriayu, I. Ladera W. (1942) Voortezet bilharzia onder- and DDT dusts against fleas on zoek in Celebes. Gennesk. T.Ned. Rattus ratus diardii in Ciloto, West -Ind., 82: 21-36. Java, Indonesia. WHO/VBC/81.802. 60. Faust, E.C. and Bonne, C. (1948) 69. Van Peenen, P.F.D., R.H. Light and Mammalian blood flukes of Celebes. J. Sulianti Saroso (1971) Field Lep- J. Parasit., 34: 124-31. tospirosis in wild mammals of Indo- 61. Smit, A.M. (1962) Eosinophilic meni- nesia - Recent surveys. Southeast Asian J. Trop.Med.Pub.Hlth., 2: ngitis at Kisaran (Indonesia) and the 493-495. problem of its etiology. Bull.Soc. Path.Exot. 55: 722-720. 71. Fresh, J.W., C.C. Tsai and Sulianti Saroso (1971) A leptospirosis study 62. Smit, A.M. (1963) Eosinophilic meni- in South Sumatera and Bank Island, ngitis. Trop.georgr.Med. 15: 225- Indonesia. Southeast Asian J. Trop. 63. Kwo, E.H. and Kwo, I.H. (1968) Med.Pub.Hlth., 2: 22-24. Occurerence of Angiostrongylus can- 72. Hadidjaja, P., Carney, W.P., Cross, tonensis in rats in North Sumatera, J.H., Jusuf, A., Sulianti Saroso, J. Indonesia. J. Parasitol., 54: 537. and Oernijati, S. (1972) Schistosomi- 64. Turner, R.W., Soeharto Padmowirjono asis japonicum and other intestinal and Supalin Martoprawiro (1975) parasites of Lake Lindu, Sulawesi Dynamics of the Plague transmission (Celebes). A premilinary report. Sou- cycle in Central Java (Ecology of thast Asian J.Trop.Med.Pub.Hlth., mammalian hosts with special refe- 3: 594-599. rence to Rattus ratus). Health Stu- 73. Hadidjaja, P. (1984). Clinical study of dies in Indonesia., 3: 41-71. Indonesian schistosomiasis at Lindu Lake area, Central Sulawesi. Southe- 65. Turner, R.W ., Supalin Martoprawiro, ast Asian J. Trop. Med. Pub. Hlth. and Soeharto Arimbi Padmowiryono 15: 507-513. (1974) Dyanics of the plague trans- 74. Clarke, M.D., Carney, W.P., Cross, mission cycle in Central Java (Ecolo- J.H., Hadidjaja, P., Oemijati, S. and gy of potential flea vectors). Health Joesoef, A. (1974) Schistosomiasis Studies in Indonesia., 2: 15-37. and other human parasitoses of 66. Kusharyono, C., Udayati, Sustriayu, Lake Lindu in Central Sulasesi (Cele- N. and. Lim Boo Liat (1980). Sur- bes), Indonesia. Ann.Trop.Med. veillance of small mamals and their Hyg., 23: 385-392.

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75. Carney, W.P., Hadidjaja, P., Davis, mo, James Campbell and Jan Putrali G.M., Clarke, M.D., Djajasasmita, (1985). The impact of schistoso- M., and Nalim S. (1972) Ocomelania miasis mass treatment on hepato- hupensis from schistosomiasis focus splenomegaly in Napu valley, Cen- in Central Sulawesi. (Celebes) J. tral Sulawesi. Souteast Asian J. Trop. Parasitol., 59: 1-34. Med. Publ. Hlth., 16 : 401-404. 76. Davis, G.M. and W.P. Carney (1973). 83. Stafford, E .E ., Sukeri, A., Sutanti, Description of Oncomelania hupensis T. (1976a) The bandicoot rat, a new lindoensis, first intermediate host host record for Angiostrongylus can- of Schistosoma japonicum in Sula- tonensis in Indonesia. Southeast wesi (Celebes). Proc. Acad. Nut. Sci. Asian J.Trop.Med.Pub.Hlth., 7: 41- 125: 1-34 44. 77. Sudomo, M., and W.P. Carney (1974) 84. Lim Boo Liat, Gandahusada, Kosim, Precontrol investigation of Schisto- E., Margono, S.S., Sustriayu, N., somiasis in Central Sulawesi. Health and Hadi, T.R. (1978) Studies of Studies in Indonesia. 2: 51-60. Angiostrongy lus cantonensis and A. 78. Dazo, B.C., Sudomo, M., Hardjawi- Malaysiensis of rodent hosts in two djaja, L., Joesoef, A., and Barodji, A. transmigration schemes in South Su- matera, Indonesia. Health Studies (1976). Control of Schistosomiasis japonicum infections in Lindu Vall- in Indonesia, 6: 15-24. ley, Central Sulawesi, Indonesia. 85. Stafford, E.E., Tanudjaja, S., Purno- Proc. 14th SEAMEO Tropmed Se- mo and Carney, W.P. (197613) Angi- minar. Schistosomiasis in Southeast ostrongylus malaysiensis in Indonesia. ' Asia and the Far East, Bangkok. Southeast Asian J.Trop.Med.Pub. Hlth., 7: 490-491. 79. Carney, W.P., Sudomo, M., Seregeg, I.G., Joesoef, A., Van Peenen, P.F. 86. Carney, W.P., Stafford, E.E., Purnomo D., Sulianti Saroso, J. and Watten, Tanudjaja, S. (1978) Angiostrongyli- R .H. ((1973b) Schistosomiasis in asis , in Indonesia: Additional geo- Indonesia: ecological and zoonotic graphic and host occurence records. aspects. Ninth Internat. Cong. Tro. Southeast Asian J.Trop.Med.Pub. Med.Malaria Athens, Greece, Oct. Hlth. 9: 516-519. 14-21 (Abstract). 87. Lim Boo Liat, Sustriayu, N. and A. 80. Putrali, T., B.C. Dazo, L. Hardjawi- Munif (1980) A study of urban djaja, M. Sudomo and A. Barodji rodents between two different social- (1980). A schistosomiasis pilot con- economic areas in Tanjung Priok, trol project in Lindu valley, Central Jakarta, Indonesia Bulletin of the Sulawesi, Indonesia. Southeast Asian Public Health Socienty, 14,: 234- J. Trop. Med. Pub Hith. 11 :450455 242. 8' Joesoef, A., Syamsuddin, N., Salman, 88. Wiroreno, W. (1975) Helminth para- K., Oman, K. And Hoz, J. (1980). sites of Rattus rattus diardii in Bo- Praziquantel trial in treating Schis- gor, West Java, Indonesia. Southeast tosoma japonicum infection in Indo- Asian J.Trop.Med.Pub.Hlth. 6: 136- nesia. Southeast Asian J. Trop. Med. 138. Publ. Hlth.. 11 : 480-485. 89. Wiroreno, W. (1978) Nematode parasi- tes of Rattus rattus diardii in Bogor, 82. Hadidjaja, P., Nurlaily Syamsuddin, Is West Java, Indonesia. Southeast Asi- Suhariah Ismid, Mohammad Sudo-

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an J.Trop.Med.Pub.Hlth. 9: 920- 95. Sandground, J.H. and Bonne, C. 525. (1940) Echinostoma Indoensis n.sp., 90. Margono, S.S. (1970) Angiostrongylus a new parasite of man in the Celebes cantonensis in Djakarta, Indonesia. with an account of its life history Southeast Asian J.Trop.Med.Pub. and epidemiology. Amer. J.Trop. Hlth., 1 : 158-159. Med., 20: 511-534. 91. Margono, S.S. and Illahude, H.D. 96. Bonne, C. (1941) Echinostomiasis aan (1974) Angiostrongylus cantonensis het Lindoemeer in Central-Celebes. in rats and intermediate hosts in Geneesk. T.Me.Ind., 81 : 1139-1167. Jakarta and its vicinity. Southeast 97. Lie Kian Joe (1951) Some trematodes Asian J.Trop.Med.Pub.Hlth.,5: 236- from man in Indonesia. Trans.Roy. 240. Soc.Trop.Med.Hyg., 44: 357. 92. Widagdo, Sunardi, Lokollo, D .M. and 98. Holz, J. (1962) Trichinellosis im Margono, S.S. (1977) Ocular angios- Raume Indonesia. Niadomsci Para- trongyliasis in Semarang, Central zytologiczne, 1: 29-30. Java. Am.J.Trop.Med.Hyg., 26: 72- 74. 99. Lim Boo Liat and Y.H. Bang (1982) Pest management in human settle- 93. Holz, J. and Liem Jan Sione (1965) ments. Protection Ecology, 4: 277-- The parasites of rat in West Java. 290. 2. Parasitenk., 25: 405-410. 100 Lim Boo Liat, I.N. Ladera and mu- . 94. Saheki, Y. (1925) An experimental nif, A. (1983) Parasite fauna of the study on the development of the commensal rats and shrews in Ja- dwarf tapeworm (Hymonolepis na- karta city, West Java, Indonesia. nu). Ann. Trop.Med.Parasito1,. 305- Hemera Zoa, 71 : (3) 213-220. 308. .

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