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Tropical Biomedicine 29(4): 544–550 (2012)

Prevalence of intestinal and blood parasites among wild in Kuala Lumpur,

Siti Shafiyyah, C.O., Jamaiah, I.*, Rohela, M., Lau, Y.L. and Siti Aminah, F. Department of Parasitology, Faculty of Medicine, University of Malaya, 50603 Kuala Lumpur, Malaysia *Corresponding author email: [email protected] Received 2 May 2012; received in revised form 14 August 2012; accepted 25 August 2012

Abstract. A survey was undertaken to investigate the prevalence of intestinal and blood parasites among wild rats in urban area of Kuala Lumpur, Malaysia. A total of 137 stool and blood samples were collected from wild rats from Sentul and Chow Kit areas. Five of rats were captured and supplied by Kuala Lumpur City Hall. The most common was Rattus rattus diardii (Malayan Black ), 67%, followed by Rattus norvegicus (Norway rat), 10%, Rattus argentiventer (rice-field rat), 10%, Rattus tiomanicus (Malaysian field rat), 9% and Rattus exulans (), 4%. Rattus rattus diardii is commonly known to live in human environment and they are normally identified as pests to human community. More male rats were captured (61%) compared to female (39%). Out of 137 samples, 81.8% samples were positive with intestinal parasites, with 86.2% from Sentul area and 78.5% from Chow Kit area. Six different parasites were detected. The most common intestinal helminth parasite detected was Nippostrongylus brasiliensis (80.3%), followed by Hymenolepis nana (23.4%), Capillaria hepatica (13.9%) and Hymenolepis diminuta (2.9%). Intestinal protozoan detected was Entamoeba histolytica/E. dispar (8.8%). (1.5%) was the only blood parasite detected.

INTRODUCTION studied the prevalence of helminths in in Egypt. The overall prevalence Rats are highly successful in adapting to of helminths was 52.8%. The commonest many environments throughout the world. cestode detected was H. diminuta and There are more than 1700 species of rodents the commonest nematode detected was identified in the world. Rodents form the Capillaria hepatica. largest group of in Malaysia. They In Malaysia, the first recorded act as reservoir host for many zoonotic prevalence of parasite in wild rats was pathogens including parasites that pose a reported by Adams in 1933 (Adams, 1933). health risk to humans (Paramasvaran et al., Singh & Chee-Hock (1971) examined 999 2009). feral rats and 450 were positive for nematode Many studies have been done on the parasites. Then in 1977, Liat et al. (1977) prevalence of parasites among wild rats reported the prevalence of C. hepatica throughout the world. Tung et al. (2009) infection in wild rodents collected from the examined 95 rodents and shrews from States of Kelantan, Selangor and Johore in different localities of Taichung, . The peninsular Malaysia. Capillaria hepatica overall prevalence of parasites was 93.7%. appears to be widespread throughout Easterbrook et al. (2008) examined 162 rats Malaysia with a wide range of hosts among in Baltimore, Maryland, USA. Endoparasites species. Leong et al. in 1979 examined detected were mainly Nippostrongylus 151 house rats, Rattus rattus diardii from braziliensis (71.6%) and Hymenolepis five different localities, Jinjang, Dato diminuta (34.4%). Elshazly et al. (2008) Keramat, Kuala Lumpur, Sungai Besi and

544 Selayang Baru, for parasites. Nineteen group, higher prevalence were among species of parasites were recovered. H. juveniles 95.7% (22 out of 23) compared to diminuta and N. brasiliensis were the adults, 78.9% (90 out of 114). Stool samples predominant species (Leong et al., 1979). were collected from rectum using a scoop Paramasvaran et al. in 2009 studied 97 and placed immediately into the screw- rodents collected from five wet markets capped stool container. Blood was collected (Chow Kit, Dato Keramat, Setapak, Jinjang from the heart using a needle and syringe and and Kepong) in Kuala Lumpur. A total of 17 placed into EDTA bottle. A drop of blood was different species of parasites were identified used to make a thin blood smear. The samples from three species of rats. Up to date, none of were transported back to Department of the above studies reported blood parasite, Parasitology, Faculty of Medicine, University Entamoeba histolytica/E. dispar in the rats. of Malaya. Stool samples were preserved in The main objective of this study was to 5% potassium dichromate to avoid fungal conduct a complete study on the prevalence growth and stored in cold room at 4ºC before of intestinal and blood parasites in wild rats being processed. in Kuala Lumpur. The results should facilitate evaluation of the endemic level of these Sample examination parasites in rats and to evaluate the infection Keys and illustrations used to identify the risk to human. rodent species were those of Harrison (1962) and Medway (1969). All stool samples were examined microscopically by both saline and MATERIALS AND METHODS iodine wet mounts. Saline wet mounts was made by mixing approximately 2 mg of stool Sample collection with a drop of saline on a glass microscope A total of 137 rats were captured mostly from slide. Similarly, iodine wet mount was wet markets in Sentul (58) and Chow Kit (79), prepared by adding approximately 2 mg of Kuala Lumpur, Malaysia by Kuala Lumpur stool to a drop of Lugol’s iodine on a glass City Hall workers (Dewan Bandaraya Kuala microscope slide and placing a cover slip on Lumpur, DBKL) between June 2011 until end the stool suspension. These wet mounts were of July 2011. Steel wire traps (28cm x 18cm) microscopically examined initially by using were used and baited with tapioca and dried a low-power (10×) objective and then using fish. These rats were collected the night a high-power (40×) objective of a compound before and were examined immediately light microscope. Thin blood smear was made the following morning. Morphometric and stained with Giemsa and examined measurements were taken, together with microscopically. The study protocol was records of length and fur colour, to assist in approved by the Ethics Committee of species identification. The dissection was House (Pusat Haiwan Makmal), University performed at the Pusat Kurungan Haiwan, of Malaya, Malaysia (Ethic Ref. No.: PAR/20/ Jalan Air Jernih, Taman Air Panas, Kuala 09/2011/JI (R). Lumpur. Trapped rats were killed humanely by placing them into a cloth bag containing cotton wool soaked with chloroform. The rats RESULTS were disposed off by DBKL. The percentage of male rats captured were higher (61%) than A total of 137 wild rats’ stool and blood female (39%). Out of 137 samples, 112 (81.8%) samples were collected from Sentul and samples were positive with intestinal Chow Kit areas in Kuala Lumpur, Federal parasites with 86.2% (50 out of 58) from Sentul Territory of Malaysia. Five rat species were area and 78.5% (62 out of 79) from Chow Kit captured by Kuala Lumpur City Hall. The most area. The prevalence of intestinal parasites common was R. rattus diardii (the common were more frequent in male rats than female house rat/Malayan ) (67.2%). The rats, 83% (70 out of 84) and 79% (42 out of 53) house rat is one of the principal domestic respectively. According to the general age pests in urban Malaysia, commonly seen

545 nesting in fields and bushes near human female, 83% and 79% respectively. According habitations (Harrison, 1962). They are to the general age group, juvenile was more reservoirs for a number of parasites (Leong prevalent with 95.7% compared to adult, et al., 1979; Sinniah, 1979) and pose a threat 78.9%. Out of 137 samples, 81.8% were as a potential disseminator of plague, positive with intestinal parasites. The scrub and murine typhus, tularaemia and highest prevalence was N. brasiliensis, bartonellosis. This was followed by R. 80.3%, followed by Hymenolepis nana, 23.4%, norvegicus (Norway rats) (10.2%). Norway C. hepatica, 13.9% and the least was H. rat is found wherever food and shelter diminuta, 2.9%. The only intestinal protozoan are abundant. They are aggressive and detected was E. histolytica/E. dispar, 8.8%. extremely adaptable to a wide range of Trypanosoma lewisi (1.5%) was the only conditions. They are found in towns, cities, blood parasite detected (Table 1). and rural areas. They may be found in barns, fields, ditches, corn cribs, and dumps. They often burrow in the ground beneath DISCUSSION protective cover (Linzey, 1995). Next was R. argentiventer (rice-field rat) (10%), primarily Nippostrongylus brasiliensis (rat’s resides in cultivated areas such as rice fields hookworm) was the most common intestinal and grasslands. It is largely dependent on parasite detected in this study among wild human rice fields and plantations for survival. rats in urban area of Kuala Lumpur, Malaysia. Rice field rats take shelter in burrows in soil, This nematode was also reported by many under rocks, and in logs (Kennedy, 1999). previous studies among wild rats in Belgrade Rattus tiomanicus (Malaysian field rat) (Kataranovski et al., 2011), Taiwan (Tung (8.8%) is a highly arboreal species that et al., 2009), Baltimore, Maryland, USA inhabits secondary forest and is a serious pest (Easterbrook et al., 2008) and Kuala Lumpur of oil palm plantations in peninsular wet market, Malaysia (Paramasvaran et al., Malaysia, feeding on the ripening fruit (Wood 2009). It was also found in the wood rat R. & Chung, 1990). The least species captured tiomanicus in West Malaysia (Krishnasamy was R. exulans (Polynesian rat) (4.4%). et al., 1980), and Chiangmai, These rats can live in a wide range of habitats (Namue & Wongsawad, 1997). It was also including grassland, scrub and forest, reported among house rats, R. rattus diardii however they do require adequate food from Sungai Besi area, Kuala Lumpur in 1979 supplies and shelter (Taylor, 1975). (Leong et al., 1979). The percentage of male rat captured Hymenolepis nana (the dwarf tape- was higher (61%) than female (39%). The worm) was the most common cestode infections were more frequent in male than detected in this study. Other researchers also

Table 1. Prevalence of intestinal and blood parasites among wild rats in Kuala Lumpur

Number of positive sample Prevalence Parasites (n) (%)

Intestinal Helminthes Nippostrongylus brasiliensis 110 80.3 Hymenolepis nana 32 23.4 Capillaria hepatica 19 13.9 Hymenolepis diminuta 4 2.9 Intestinal Protozoa Entamoeba histolytica/E. dispar 12 8.8 Blood Protozoa Trypanosoma lewisi 2 1.5

546 reported this parasite in their studies among acquires the infection in the same manner as wild rats, in Sudan (Fagir & El-Rayah, 2009), H. nana that is via ingestion of infected Taiwan (Tung et al., 2009), and Malaysia intermediate host. Its infection may cause (Paramasvaran et al., 2009) and among the diarrhoea or occasionally cachexia in man wood rat in Malaysia (Krishnasamy et al., (Sun, 1988). 1980). Hymenolepis nana is the smallest Entamoeba histolytica/E. dispar was tapeworm that infects human. Most patients detected for the first time in the stool of the infected are children due to swallowing of rats in Malaysia. Entamoeba histolytica was rat’s flea which contains the infective reported among wild rats caught in London. cysticercoid stage. Mild infections are The naturally infected rats were restricted to usually asymptomatic. Severe infection a localized focus, in which cases of human may cause headache, dizziness, pruritis, amoebiasis were discovered, thus providing diarrhoea, restlessness or even convulsion circumstantial evidence of the human origin in man (Sun, 1988). of the infection, and throwing light on the Capillaria hepatica, the second possible role of rats as reservoir hosts (Neal, commonest nematode reported in this study 1951). In severe amoebiasis, trophozoites was also reported among rats in Belgrade invade the intestinal mucosa, enter the (Kataranovski et al., 2011), Taiwan, (Tung et circulation and spread hematogenously al., 2009), and Malaysia (Paramasvaran et causing development of extra-intestinal al., 2009). It causes a disease known as abscesses. Mostly it will end up in the liver hepatic capillariasis, a zoonosis, mainly a causing amoebic liver abscesses. Brain and disease of rats and is rarely seen in man. lung may be infected, but cases are rare. Cases have been reported in , USA, Entamoeba dispar is not pathogenic. Turkey, South Africa, Mexico and Brazil. Trypanosoma lewisi is transmitted by Clinical features are acute or subacute fleas to rat and is the only blood parasite hepatitis with eosinophilia. The cause of detected in this study. Trypanosoma lewisi death is extensive liver damage or secondary normally infects rodents and utilize fleas as bacterial infection. The major pathologic vectors. Rats are infected principally by oral change is granulomatous inflammation in the route, through ingestion of flea faeces or fleas. liver (Sun, 1988). The disease is contracted Trypanosoma lewisi has been reported in by ingesting embryonated eggs in food and numerous studies among wild rodents all drink. In the animal host, the larvae hatch in over the world. Among black rats in Niger, the caecum, then penetrate the mucosa and West Africa (Dobigny et al., 2011), Rattus find their way to the liver. Within 3 weeks, and species in Thailand the parasites mature and start to lay eggs in (Jittapalapong et al., 2008), free living rats the liver. The eggs remain in the liver until in Poland (Karbowiak & Wita, 2001), R. the host dies, whereupon they are released norvegicus in Brazil (Linardi & Botelho, into the soil and become embryonated within 2002), rats collected from different localities 2-6 weeks. When the liver of an infected in northern Iraq (Molan & Hussein, 1988), and animal is eaten, the unembryonated eggs are house rats in Ibadan (Akinboade et al., 1981). discharged in the stool. This phenomenon is Although this trypanosome subgenus is known as spurious infection and 19 cases considered non-pathogenic to rodents, on rare were detected in this study. occasions it was reported to cause disease Hymenolepis diminuta has also been in humans. Trypanosoma lewisi is an animal reported among rats in Belgrade species and is usually non pathogenic in (Kataranovski et al., 2011), Sudan (Fagir humans but can acquire the desired virulence & El-Rayah, 2009), Baltimore, USA and emerge as human pathogen causing (Easterbrook et al., 2008), in the city of serious disease, in the right combination of Doha, Qatar (Abu-Madi et al., 2005), Nigeria environmental, host and organism related (Mafiana et al., 1997), Kuala Lumpur, factors. Under the fast changing environ- Malaysia (Leong et al., 1979) and peninsula mental scenario there is an urgent need to be Malaysia (Krishnasamy et al., 1980). Man prepared for these emerging zoonoses (Kaur

547 et al., 2007). Trypanosoma lewisi infection was supported by University of Malaya, High has been reported in infants including a Impact Research Fund (Grant No. E-000050- 45-day-old Thai infant displaying fever, 20001). anaemia, cough and anorexia (Sarataphan et al., 2007). It was also reported in a two months old infant in urban Mumbai, India REFERENCES (Kaur et al., 2007) and in a 4-month-old Malaysian infant with a 3-week history of Abu-Madi, M.A., Behnke, J.M., Mikhail, M., lassitude, loss of appetite, feverish and Lewis, J.W. & Al-Kaabi, M.L. (2005). anaemic with a heavy trypanosome infection Parasite populations in the upon admission (Johnson, 1933). Weinman Rattus norvegicus from Doha, Qatar disagree that this was Trypanosoma lewisi between years: the effect of host age, sex and he thought that Johnson’s patient may and density. Journal Helminthology have been infected with the trypanosomes 79(2): 105-111. of primates (Weinman, 1970). Recently, Adams, A.R.D. (1933). Report on a collection trypanosomes of T. lewisi were observed in of nematodes from the Federated Malay the peripheral blood smear of a 37-day-old States. Annals of Tropical Medicine and Indian infant admitted off feeds, with fever Parasitology 27: 1. and convulsions (Verma et al., 2011). Akinboade, O.A., Dipeolu, O.O., Ogunji, F.O. Rats being closely associated with man & Adegoke, G.O. (1981). The parasites harbours many different kinds of intestinal obtained and bacteria isolated from and blood parasites and serve as great house rats (Rattus rattus Linnaeus, 1758) potential for zoonotic infections to man. This caught in human habitations in Ibadan, study as well as previous studies clearly Nigeria. International Journal of shows that control of domestic rats is of prime Zoonoses 8(1): 26-32. importance in the prevention and control of Dobigny, G., Poirier, P., Hima, K., Cabaret, O., zoonotic infections in man. Gauthier, P., Tatard, C., Jean-Marc, C. & This study clearly showed that intestinal Bretagne, S. (2011). Molecular survey of parasites are highly prevalent in rats in the rodent-borne Trypanosoma in Niger with urban city of Kuala Lumpur, Malaysia. The special emphasis on T. lewisi imported ever increasing in the amount of garbage by invasive black rats. Acta Tropica collected and the rise in the number of slums 117(3): 183-188. in big cities contribute to the high prevalence Easterbrook, J.D., Kaplan, J.B., Glass, G.E., of rats. The close proximity of man with rats Watson, J. & Klein, S.L. (2008). A survey in housing areas may contribute significantly of rodent-borne pathogens carried by to the spread of many zoonotic diseases. wild-caught Norway rats: a potential threat to laboratory rodent colonies. Acknowledgements. The authors would like Laboratory 42(1): 92-98. to express their gratitude to the Director and Elshazly, A.M., Awad, S.I., Azab, M.S., staff of the Pest Control Division of Kuala Elsheikha, H.M., Abdel-Gawad, A.G., Lumpur City Hall (Dewan Bandaraya Kuala Khalil, H.H. & Morsy, T.A. (2008). Lumpur, DBKL) (i.e. Mr. Chandra Kantipal, Mr. Helminthes of synanthropic rodents Omar, Mr. Helmi, Mr. Khairul) for the use of (Rodentia: ) from Dakahlia their facilities in Setapak and for their and Menoufia, Egypt. Journal of the assistance in trapping rats in area of Sentul Egyptian Society of Parasitology 38(3): and Chow Kit, Kuala Lumpur. The study 727-740. protocol (Ethic Ref. No. : PAR/20/09/2011/JI Fagir, D.M. & El-Rayahel, A. (2009). Parasites (R) was approved by Ethics Committee of of the Nile rat in rural and urban regions Animal House (Pusat Haiwan Makmal), of Sudan. Integrative Zoology 4(2): 179- University of Malaya, Malaysia. The study 187.

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