Helminth communities from two urban rat populations in Kuala Lumpur, Malaysia

Particle and Fibre Toxicology

John W Lewis³  Jerzy M Behnke¹  Siti N Mohd Zain² 

[1] School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK;School of Biological Sciences, University of Malaya, 50603 Kuala Lumpur, Malaysia;School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 0EX, UK

关键词: Heterakis spumosum;    Nippostrongylus brasiliensis;    Mastophorus muris;    Hymenolepis nana;    Hymenolepis diminuta;    helminth species diversity;    nematodes;    helminths;    Rattus rattus;    Rattus norvegicus;   

Others  :  1233068
DOI  :  10.1186/1756-3305-5-47

 received in 2011-12-13, accepted in 2012-03-07,  发布年份 2012

【 摘 要 】

Background

The prevalence of parasitic infections among commensal animals such as black and brown rats in many tropical countries is high and in comparison with studies on rodents in temperate climates, little is known about the community structure of their parasites. Rodent borne parasites pose threats to human health since people living in close proximity to rodent populations can be exposed to infection.

Methods

The helminth community structures of two urban rat populations in Kuala Lumpur, Malaysia were investigated. The rats were from two contrasting sites in the city caught over a period of 21 months in 2000-2002.

Results

Eleven species of helminth parasites comprising seven nematodes (Heterakis spumosum, Mastophorus muris, Nippostrongylus brasiliensis, Syphacia muris,Pterygodermatites tani/whartoni, Gongylonema neoplasticum, Angiostrongylus malaysiensis), three cestodes (Hymenolepis (Rodentolepis) nana, H. diminuta and Taenia taeniaeformis) and one acanthocephalan (Moniliformis moniliformis) were recovered from 346 Rattus rattus and 104 R. norvegicus from two urban sites, Bangsar and Chow Kit, during 2000-2002. Rattus rattus harboured over 60% of all helminths compared with R. norvegicus, although both host species played a dominant role in the different sites with, for example R. norvegicus at Bangsar and R. rattus at Chow Kit accounting for most of the nematodes. Overall 80% of rats carried at least one species of helminth, with the highest prevalences being shown by H. diminuta (35%), H. spumosum (29.8%) and H. nana (28.4%). Nevertheless, there were marked differences in prevalence rates between sites and hosts. The influence of extrinsic (year, season and site) and intrinsic (species, sex and age) factors affecting infracommunity structure (abundance and prevalence of infection) and measures of component community structure were analyzed.

Conclusions

Since at least two species of rat borne helminths in Kuala Lumpur have the potential to infect humans, and these showed high prevalences in the rats, the assessment and regular monitoring of infections carried by wild rodents have important roles to play in public health.

【 授权许可】

   
2012 Mohd Zain et al; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Davis S, Calvet E, Leirs H: Fluctuating rodent populations and risk to humans from rodent-borne zoonoses. Vect Borne Zoonot Dis 2005, 5:305-314.
• [2]Meerburg BG, Singleton GR, Kijlstra A: Rodent-borne diseases and their risks for pubic health. Crit Rev Microbiol 2009, 35:221-270.
• [3]Elsheikha HM, Clayton SJ, Yon LK: Parasitic zoonoses at the rodent-captive primate-human health interface. J Egypt Soc Parasitol 2009, 39:447-460.
• [4]Antoniou M, Psaroulaki A, Toumazos P, Mazeris A, Ioannou I, Papaprodromou M, Georgiou K, Hristofi N, Patsias A, Loucaides F, Moschandreas J, Tsatsaris A, Tselentis Y: Rats as indicators of the presence and dispersal of pathogens in Cyprus: ectoparasites, parasitic helminths, enteric bacteria, and encephalomyocarditis virus. Vect Borne Zoonot Dis 2010, 10:867-873.
• [5]Jansen A, Schnieder T: Weil's disease in a rat owner. Lancet Infect Dis 2011, 11:152.
• [6]Kisielewska K: Ecological organization of intestinal helminth grouping in Clethrionomys glareolus (Schreb.) (Rodentia). V. Some questions concerning helminth groupings in the host individuals. Acta Parasitol Pol 1970, 17:197-208.
• [7]Lewis JW: Helminth parasites of British rodents and insectivores. Mam Rev 1987, 17:81-93.
• [8]Webster JP, MacDonald DW: Parasites of wild brown rats (Rattus norvegicus) on UK farms. Parasitology 1995, 111:247-255.
• [9]Abu-Madi MA, Behnke JM, Lewis JW, Gilbert FS: Descriptive epidemiology of Heligmosomoides polygrus in Apodemus sylvaticus from three contrasting habitats in south-east England. J Helminthol 1998, 72:93-100.
• [10]Abu-Madi MA, Behnke JM, Lewis JW, Gilbert FS: Seasonal and site specific variation in the component community structure of intestinal helminths in Apodemus sylvaticus from three contrasting habitats in south-east England. J Helminthol 2000, 72:7-15.
• [11]Behnke JM, Lewis JW, Mohd Zain SN, Gilbert FS: Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host-age, sex and year on prevalence and abundance of infections. J Helminthol 1999, 73:31-44.
• [12]Behnke JM, Bajer A, Harris PD, Newington L, Pidgeon E, Rowlands G, Sheriff C, Kuliś-Malkowska K, Siński E, Gilbert FS, Barnard CJ: Temporal and between-site variation in helminth communities of bank voles (Myodes glareolus) from N.E. Poland. 2. The infracommunity level. Parasitology 2008, 135:999-1018.
• [13]Vandegrift KJ, Hudson PJ: Could parasites destabilize mouse populations?The potential role of Pterygodermatites peromysci in the population dynamics of freeliving mice, Peromyscus leucopus. Int J Parasitol 2009, 39:1253-1262.
• [14]Pederson AB, Grieves TJ: The interaction of parasites and resources cause crashes in a wild mouse population. J Anim Ecol 2008, 77:370-377.
• [15]Dunn FL, Lim BL, Yap LF: Endoparasite patterns in mammals of the Malayan Rain Forest. Ecology 1968, 49:1179-1184.
• [16]Mulkit S, Cheong CK: On a collection of nematode parasites from Malayan Rats. S E Asian J Trop Med Pub Health 1971, 2:516-521.
• [17]Ow-Yang CK: Studies on the nematode parasite of Malaysian rodents. I. The Rhabdiasidea, Trichuridea and Oxyuridae. J Helminthol 1971, 45:93-109.
• [18]Lim BL, Lim TW, Cheah W, Yap LF: Angiostrongylus malaysiensis from Tuaran, Sabah, with reference to the distribution of the parasite in Malaysia. S E Asian J Trop Med Pub Health 1976, 7:384-389.
• [19]Yap LF, DeWitt GF, Krishnasamy M, Sivanandam S, Yen PFK: Protozoan and helminth parasites of small wild mammals in a new Felda Settlement Jenderak Utara, central Pahang, Peninsular Malaysia. S E Asian J Trop Med Pub Health 1977, 8:345-353.
• [20]Leong TS, Lim BL, Krishnasamy M: Parasite fauna of the house rat Rattus rattus diardii in Kuala Lumpur and nearby villages. S E Asian J Trop Med Pub Health 1979, 10:112-136.
• [21]Sinniah B: Parasites of some rodents in Malaysia. S E Asian J Trop Med Pub Health 1979, 10:115-121.
• [22]Krishnasamy M, Singh KI, Ambu S, Ramachandran P: Seasonal prevalence of the helminth fauna of the wood rat, Rattus tiomanicus (Miller) in West Malaysia. Folia Parasitol 1980, 27:231-235.
• [23]Inder Singh K, Krishnasamy M, Ho TM: Collection of small vertebrates and their endoparasites from Ulu Endau, Johore, Malaysia. Malay Nat J 1987, 41:349-356.
• [24]Ambu S, Krishnasamy M, Ramachandran P, Ramos R: Helminth infections of rodents in Orang Asli settlements in Selangor, Malaysia-possible health risks. Trop Biomed 1996, 13:123-127.
• [25]Paramasvaran S, Krishnasamy M, Lee HL, John J, Lokman H, Naseem BM, Rehana AS, Santhana RJ: Helminth infections in small mammals from Ulu Gombak Forest Reserve and the risk to human health. Trop Biomed 2005, 22:191-194.
• [26]Syed-Arnez ASK, Mohd Zain SN: A study of wild rats and their endoparasite fauna from Endau Rompin National Park, Johor. Malay J Sci 2006, 25:19-39.
• [27]Mohd Zain SN: Endoparasites of rodents in two islands of the Straits of Malacca. Malay J Sci 2008, 27:123-127.
• [28]Paramasvaran S, Sani RA, Hassan L, Hanjeet K, Krishnasamy M, John J, Santhana R, Sumarni MG, Lim KH: Endo-parasite fauna of rodents caught in five wet markets in Kuala Lumpur and its potential zoonotic implications. Trop Biomed 2009, 26:67-72.
• [29]MacDonald D, Barrett P: Collins Field Guide Mammals of Britain & Europe. London, UK, Harper Collins; 2005.
• [30]Brooks JE, Rowe FP: Vector control series: rodents, training and information guide. World Health Organization, WHO/VBC/87.949; 1987:107.
• [31]Rohlf FJ, Sokal RR: Statistical Tables. San Franscisco, USA, W.H. Freeman W.H. and Company; 1995.
• [32]Poulin R: The disparity between observed and uniform distributions: a new look at parasite aggregation. Int J Parasitol 1993, 23:937-944.
• [33]Elliott JM: Some Methods for the Statistical Analysis of Samples of Benthic Invertebrates. Cumbria, UK, Freshwater Biological Association; 1977.
• [34]Venables WN, Ripley BD: Modern Applied Statistics with S-Plus. New York, USA, Springer; 1997.
• [35]Keymer AE, Dobson AP: The ecology of helminths in populations of small mammals. Mam Rev 1987, 17:105-116.
• [36]Montgomery SSJ, Montgomery WI: Spatial and temporal variation in the infracommunity structure of helminths of Apodemus sylvaticus (Rodentia: Muridae). Parasitology 1989, 98:145-150.
• [37]Montgomery SSJ, Montgomery WH: Structure, community and species interactions in helminth communities of wood mice Apodemus sylvaticus. Int J Parasitol 1990, 20:225-242.
• [38]Gregory RD, Keymer AE, Clarke JR: Genetics, sex and exposure: the ecology of Heligmosomoides polygyrus (Nematoda) in the wood mouse. J Anim Ecol 1990, 59:363-378.
• [39]Haukisalmi V, Henttonen H: Coexistence in helminths of the bank vole Clethrionomys glareolus. I. Patterns of co-occurrence. J Anim Ecol 1993, 62:221-229.
• [40]Haukisalmi V, Hentonnen H: Analysing interspecific associations in parasites: alternative methods and effects of sampling heterogeneity. Oecologica 1998, 116:565-574.
• [41]Behnke JM, Gilbert FS, Abu-Madi MA, Lewis JW: Do the helminth parasites of wood mice interact? J Anim Ecol 2005, 74:982-993.
• [42]Abu-Madi MA, Lewis JW, Mikhail M, El-Nagger ME, Behnke JM: Monospecific helminth and arthropod infections in an urban population of brown rats from Doha, Qatar. J Helminthol 2001, 75:313-320.
• [43]Myers BJ, Kuntz RE, Wells WH: Helminth parasites of reptiles, birds and mammals in Egypt VII. Check list of nematodes collected from 1948-1955. Can J Zool 1962, 40:531-538.
• [44]Zakaria M, Zaghloul TM: Parasitic infection of Rattus norvegicus in Kuwait. Proc First Symp Rec Advs Rodent Control, Kuwait 1982, 136-143.
• [45]Seong JK, Huh S, Lee JS, Oh YS: Helminths in Rattus norvegicus in Chunchon, Korea. Kor J Parasitol 1995, 33:235-237.
• [46]Mafiana CF, Osho MB, Sam-Wo-Bo S: Gastrointestinal helminth parasites of the black rat (Rattus rattus) in Abeokuta, southwest Nigeria. J Helminthol 1997, 71:217-220.
• [47]Zima J, Kral B: Karyotypes of European Mammals,2. Acta Sci Nat Acad Sci Bohem 1984, 18:62.
• [48]Corbet GB, Harris S: The Handbook of British Mammals. Oxford, UK, Blackwell; 1991:588.
• [49]Poulin R: Macroecological patterns of species richness in parasite assemblages. Basic Appl Ecol 2004, 5:423-434.
• [50]Walther BA, Morand S: Comparative performance of species richness estimation methods. Parasitology 1998, 116:395-405.
• [51]Feliu C, Renaud F, Catzeflis F, Hugot J-P, Durand P, Morand S: A comparative analysis of parasite species richness of Iberian rodents. Parasitology 1997, 115:453-466.
• [52]Wertheim G: Helminth parasites of the rat Rattus norvegicus from Haifa and Tel-Aviv. Bull Res Council Isreal 1963, 10E:125-129.
• [53]Verster A: A taxonomic revision of the genus Taenia Linnaeus, 1758 S. Str. Onderstepoort J Vet Res 1969, 36:3-58.
• [54]Gillespie SH: The epidemiology of Toxocara canis . Parasitology Today 1988, 4:180-182.
• [55]Hildebrand J, Zalesny G, Okulewicz A, Baskkiewicz K: Preliminary studies on the zoonotic importance of rodents as a reservoir of toxocariasis from recreation grounds in Wroclaw,Poland. Helminthologia 2009, 46:80-84.
• [56]Moravec F: Proposal of a new systematic arrangement of nematodes of the family Capillariidae. Folia Parasitol 1982, 29:119-132.
• [57]Owen IL: Parasitic zoonoses in Papua New Guinea. J Helminthol 2005, 79:1-14.
• [58]Chomel BB: Zoonoses of house pets other than dogs, cat and birds. Ped Infs Dis J 1992, 11:479-487.
• [59]Tena D, Simon MP, Gimeno C, Pomata MTP, Illescas S, Amondarain I, Gonzales A, Dominguez J, Bisquert J: Human infection with Hymenolepis diminuta: case report from Spain. J Clin Microbiol 1998, 36:2375-2376.
• [60]MacNish MG, Morgan UM, Behnke JM, Thompson RCA: Failure to infect laboratory rodent hosts with human isolates of Rodentolepis (= Hymenolepis) nana. J Helminthol 2002, 76:37-43.
• [61]MacNish MG, Morgan-Ryan UM, Monis PT, Behnke JM, Thompson RCA: A molecular phylogeny of nuclear and mitochondrial sequences in Hymenolepis nana (Cestoda) supports the existence of a cryptic species. Parasitology 2002, 125:567-575.
• [62]Welch JS: Parasitology field studies. Twenty seventh Annual Report of the Queensland Inst Medl Res, Brisbane 1972, 22-23.
• [63]Reynoldson JA, Behnke JM, Pallant LJ, MacNish MG, Gilbert F, Thompson RAC: Failure of pyrantel in treatment of human hookworm infections (Ancylostoma duodenale) in the Kimbereley region of north west Australia. Acta Tropica 1997, 68:301-312.
• [64]Brandt LJ: Commentary. Gastrointest Endoscopy 2009, 70:785.
• [65]Ragunathan L, Kalivaradhan SK, Ramadass S, Nagaraj M, Ramesh K: Helminthic infections in school children in Puducherry, South India. J Microbiol Immunol Infect 2010, 43:228-32.
• [66]Sinniah B: Prevalence, treatment and reinfection of intestinal helminths among schoolchildren in Kuala Lumpur, Malaysia. Pub Health 2005, 98:38-42.
• [67]Sagin DD, Mohamed M, Ismail G, Jok JJ, Lim LH, Pui JNF: Intestinal parasitic infection among five interior commuities at Ipper Rejang River, Sarawak, Malaysia. SE Asian J Trop Med Pub Health 2002, 33:18-22.
• [68]Sinniah B, Sinniah D, Singh M, Poon GK: Prevalence of parasitic infections in Malaysian oil palm estate workers. SE Asian J Trop Med Pub Health 1978, 9:272-276.
• [69]Quentin JC: Morphogenese larvarie du spiruride Mastophorus muris (Gmelin, 1790). Ann Parasitol (Paris) 1970, 45:839-855.
• [70]Beaucournu JC, Chabaud AG: Infestation spontanée de Puces par le spiruride Mastophorus muris (Gmelin). Ann Parasitole (Paris) 1963, 38:931-934.
• [71]Charleston WAG, Innes JG: Seasonal trends in the prevalence and intensity of spiruroid nematode infections of Rattus r. rattus. New Zealand J Zool 1980, 7:141-145.
• [72]Decker KH, Duszynski DW, Patrick MJ: Biotic and abiotic effects on endoparasites infecting Dipodomys and perognathus species. J Parasitol 2001, 87:300-307.
• [73]Behnke JM: Evasion of immunity by nematode parasites causing chronic infections. Adv Parasitol 1987, 26:1-70.
• [74]Maizels RM, Balic A, Gomez-Escobar N, Nair M, Taylor MD, Allen JE: Helminth parasites - masters of regulation. Immunol Rev 2004, 201:89-116.
• [75]Andreassen J, Bennet-Jenkin EM, Bryant C: Immunology and biochemistry of Hymenolepis diminuta. Adv in Parasitol 1999, 42:223-275.
• [76]Hamada GS, Wertheim G: Mastophorus muris (Nematoda: spirurina): cuticular ultrastructure of the adult and third stage larva. J. Parasitol 1978, 64:448-558.
• [77]Isaak DD, Jacobson RH, Reed ND: The course of Hymenolepis nana infections in thymus-deficient mice. Int Arch Allergy Appld Immunol 1977, 55:504-513.
• [78]Rothwell TLW: Immune expulsion of parasitic nematodes from the alimentary tract. Int J Parasitol 1989, 19:139-168.
• [79]Else KJ, Finkelman FD: Intestinal nematode parasites, cytokines and effector mechanisms. Int J Parasitol 1998, 28:1145-1158.
• [80]Gregory RD: On the interpretation of host-parasite ecology: Heligmosomoides polygyrus (Nematoda) in wild wood mouse (Apodemus sylvaticus) populations. J Zool 1992, 226:109-121.
• [81]Ferrari N, Cattadori IM, Nespereira J, Rizzoli A, Hudson PJ: The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis. Ecol Let 2004, 7:88-94.
• [82]Luong LT, Grear DA, Hudson PJ: Male hosts are responsible for the transmission of a trophically transmitted parasite, Pterygodermatites peromysci, to the intermediate host in the absence of sex-biased infection. Int J Parasitol 2009, 39:1263-1268.
• [83]Poulin R: Sexual inequalities in helminth infections: a cost of being a male? Am Nat 1996, 147:287-295.
• [84]Nasher AK: Helminths of Saudi Arabia. Helminth parasites of the spiny mouse Acomys dimidiatus (Cretzschmar) from southwest Saudi Arabia. Fauna Saudi Arabia 1984, 6:127-129.