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Memorias do Instituto Oswaldo Cruz Giardia Survey in Live-trapped Small Domestic and Wild Mammals in Four Regions in the Southwest Region of the State of São Paulo, Brazil Maria Ines L Sogayar, Elizaide LA Yoshida Departamento de Parasitologia, Instituto de Biociencias, UNESP, Campus de Botucatu, 18618-000 Rubiao Junior, SP, Brasil
Code Number: OC95136
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No associated graphicsFor the first time, a survey on Giardia in live-trapped small domestic and wild mammals was performed in four regions of State of the Sao Paulo, Brazil, with special attention to the parasitism of Rattus rattus rattus by Giardia. This species was found infected in all studied sites: Botucatu (15.4%), Conchas (28.5%), Itaporanga (38.7%) and Sao Roque (100%). Two new hosts and their frequency of infection were described for Giardia in Nectomys squamipes, an aquatic rodent and in Bolomys lasiurus, a forest rodent (100% and 14.3%, respectively). Both G. muris and G. duodenalis groups were found in scrapings of intestinal mucosa of those rodents. Mixed infection was observed in some animals. It is important to emphasize the infection by G. duodenalis in the black rat as this species lives as a comensal with man and in N. squamipes as it may contaminate small streams used for domestic consumption. Therefore, further investigation will be necessary to elucidate the potencial of these rodents to act as reservoirs of Giardia for man. Key words: Giardia - rodents - Rattus rattus - Nectomys - Bolomys - Brazil Ninety five waterborne outbreaks of human giardiasis were reported from 1965 to 1985 in the United States (Craum 1990) and both human and animal contaminations from water have been implicated in most of these outbreaks. Some epidemiological surveys for wild animal populations have suggested that aquatic animals as beaver (Kirner et al. 1978, Frost et al. 1980), the water vole and muskrat (Frost et al. 1980, Navin et al. 1985, Pacha et al. 1985, 1987) can be reservoir hosts for Giardia cysts capable of infecting humans. The situation of human giardiasis infection in Brazil is endemic and the reports about Giardia in wild animals are rare. Fonseca (1916) reported the finding of G. intestinalis in monkeys (Cebus carayá); G. muris in rats (Rattus norvegicus), G. cuniculi in rabbits and hedgehog (Coendu villosus). Presence of G. irarae was shown in irara (Tayra barbara), an aquatic carnivorous animal and G. tucani in toucan (Rhamphastos ariel) by Carini (1945). Considering that investigations with wild reservoirs of Leishmania sp. have been developed in our laboratory, these animals were studied to determine the presence and type of Giardia in each animal, with special attention to the parasitism of Rattus rattus. It was the first time that this kind of work was performed in Brazil. MATERIALS AND METHODS Epidemiological data - Botucatu, Conchas, Itaporanga and Sao Roque, the four municipalities where the domestic and sylvatic mammals were captured, are situated in the southwest of the State of Sao Paulo, Brazil. The live animals were captured with livetraps (Vanzolini & Papavero 1967) using dry cheese, maize, manioc, yam, orange and birds. The capture of animals in Itaporanga and Conchas was performed in primary forests near the margin of Itarare and Peixe rivers, respectively. The other capture sites were a maize plantation, food depositories and near the houses. In Botucatu, the rodents were caught in the Campus of the University (UNESP). All the study areas were human habitats. Species of live-trapped animals - The animals were of unknown age, both sexes and belonging to several different mammalian orders and species, as follows: from Botucatu - 52 domestic rats (R. r. rattus); from Conchas: 3 armadillos (Euphractus sexcinctus); 14 opossuns (9 Didelphis marsupialis and 5 D. albiventris); 14 rodents (12 R. rattus, 1 N. squamipes, 1 Mus musculus); from Itaporanga: 101 rodents (93 R. rattus, 7 Bolomys lasiurus, 1 of de family Cricetidae); 72 opossuns (45 D. albiventris, 27 D. marsupialis); 6 lizards (Tupinambis teguixin); 2 quatis (Nasua nasua); 2 carnivorous animals (1 Procyon cancrivorus, 1 Lutreolina crassicaudata); from Sao Roque - 12 rodents (9 R. rattus, 3 N. squamipes). Parasites identification - Trophozoites and cysts of Giardia were detected by examining scrapings of the intestinal mucosa fixed in Schaudinn´s solution and stained by the HeidenhainÆs iron hematoxylin method. The faecal material was examined by Zinc flotation method. Two attempts to cultivate the parasites of G. duodenalis group from R. rattus in TYI-S-33, were made in laboratory. Measurements were taken from thirty trophozoites recovered from at least three animals of each host species, except for those recovered from a unique exemplary host. All the measurements were taken for animals from Conchas, Itaporanga and Sao Roque region; only length and width of trophozoites with median bodies were considered. RESULTS As shown in Table I, among the mammalian orders examined, only rodents were infected with Giardia. The parasitism in R. r. rattus was more expressive than in other rodents. These infected animals were found in the four studied sites. We observed that N. squamipes and B. lasiurus were found infected only in the region of Sao Roque and Itaporanga, respectively. The rodents species examined were infected by trophozoites of G. muris or G. duodenalis groups, except the B. lasiurus which had only G. muris. Some animals had mixed infection (Table II). The two attempts to cultivate the trophozoites of G. duodenalis isolated from domestic rat were unsuccessful. The trophozoites of Giardia found in the rodents were morphologically similar in appearance to G. muris or G. duodenalis groups. The measurements of trophozoites of G. muris and G. duodenalis groups were shown in Table III. A regional variation in the size of trophozoites was observed but the width of G. duodenalis from Conchas was different from those of other regions. DISCUSSION The mouse and black rat living as a commensal with man, have been recognized as vector of many human diseases. From the standpoint of epidemiological knowledgement of giardiasis, it is very interesting to know its frequency in house rodent and wild animals in Brazil where there is no reference about the presence of this intestinal parasite in those hosts. The results showed that G. muris and G. duodenalis groups were found in the intestine of R. r. rattus and N. squamipes. Some animals had mixed infection. On B. lasiurus only G. muris was detected. Regional variation was seen in the prevalence of Giardia (Table I) but frequency was high in most of the regions. Except for the rodents, all the other species of wild animals examined were negative to Giardia. As the number of the animals was small the negative results may not represent the true condition of the Giardia parasitism in those animals. Few papers give information on the presence of these intestinal protozoa in house rodents. Hamajima and Ischii (1963) detected G. muris in 11 mice (84.62%) out of 13 (Mus molossinus) from the Hakozaki region (Japan). Vives and Zeledon (1957) found trophozoites of Giardia in seven R. r. rattus, although they did not determine the species of Giardia in those hosts. Kasai (1978) reported the presence of G. muris and G. simoni in many species of rodents in Japan without discriminating the parasite and the hosts. Haiba (1956) examining the wild black rat reported its complete freedom from these flagellates. According to many authours, G. muris can parasite the black rat (Filice 1952, Kulda & Nohrynkova 1978), but there is no reference about the presence of G. duodenalis group in the black rat. Haiba (1956) could not show parasites in the intestine of wild black rat inoculated with cysts of human Giardia. In the present research, for the first time, a survey for Giardia infection in the domestic rat was performed and also determined the Giardia species occuring in that rodent. Considering the cosmopolitan way of life of R. r. rattus it is important to ask what the parasitism by G. duodenalis means. For concluding that this rodent species has a potencial to act as a possible reservoir to Giardia for man more investigations are necessary, as there is no cross transmission reference and no isolate of G. duodenalis was obtained in vitro. The present two attempts to cultivate it were unsuccessful. Cultures with trophozoites were performed but no growing could be observed. On the order hand, it was the first time that the presence of Giardia was reported in B. lasiurus, and N. squamipes. B. lasiurus, a cricetine rodent, inhabits the Brazilian low lands, cultivated or recently abandoned fields. This species is primarily nocturnal and it constructs a burrow system with several openings and one or two tunnels that lead to a spherical nest chamber about 40 cm below the surface: it is strictly terrestrial and omnivorous in captivity. N. squamipes generally occurs near a swamp, lake or stream. Its diet includes vegetation, insects, tadpoles and small fish. Nests are built on the ground under old logs or bush heaps. It is very prevalent in the State of Sao Paulo (Nowak 1991). The parasitism of N. squamipes by G. duodenalis group is very interesting because this rodent may contaminate small streams used for domestic consumption as it has been reported for beavers and muskrats in the United States. Although, the Giardia trophozoites were morphologically similar to trophozoites observed in humans, further investigations on these animals and this parasite are necessary before any conclusion about the role or the parallelism between N. squamipes and beaver or muskrat in the United States. According to Jakubowski (1990), it is prudent from the point of public health to consider that all organism of G. duodenalis group has potencial to infect man. An interesting aspect was the frequency of mixed infection. This fact has been rare and one of the first reports that showed the mixed presence of G. muris and G. lamblia in laboratory rats was performed by Haiba (1950). The present results show that the detection of intestinal trophozoites is probably a sensitive method for diagnosing Giardia mixed infection and also show that an extra attention is necessary for the examination of intestinal material, because it is easy to confuse Giardia groups when the isolate is from a host with mixed infection. The biological meaning of mixed infection needs to be elucided. TABLE I Occurence of Giardia in live-trapped animals from four regions of the state of Sao Paulo
Location Animal species No. of %
positive/total
---------------------------------------------------------
Botucatu Domestic rat (Ratms rattus rattus)
8/52 15.4
Sao Roque Domestic rat (R. r. rattus) 9/9 100.0
Aquatic rodent (Nectomys squamipes)
3/3 100.0
Conchas Armadillo (Euphractus sexcintus)
0/3 0.0
Opossum (Didelphis marsupialis)
0/9 0.0
Opossum (D. albiventris) 0/15 0.0
Domestic rat (R. r. rattus) 4/14 28.5
Forest rodent (Mus musculus) 0/1 0.0
Aquatic rodent (N. squamipes) 0/1 0.0
Itaporanga Domestic rat (R. r. rattus) 36/93 38.7
Forest rodent (Bolomys lasiurus)
1/7 14.3
Forest rodent (Cricetidae) 0/1 0.0
Opossum (D. marsupialis) 0/27 0.0
Opossum (D. albiventris) 0/45 0.0
Lizard (Tupinambis teguixin) 0/6 0.0
Quati (Nasua nasua) 0/2 0.0
Carnivorous animal (Procyon cancrivorus)
0/1 0.0
Carnivorous animal (Lulreolina crassicaudata)
0/1 0.0
TABLE II
Occurence of Giardia morphological groups in live
trapped small rodents from four regions of the State of
Sao Paulo, Brazil
Rodents Rattus rattus rattus Bolomys lasiurus
species
Location G.muris G.duod- MI^a G.muris G.duod
MI
enalis enalis
group group group group group group
-----------------------------------------------------------
Conchas^b 1 1 0
Botucatu^c 3 1 1
Itaporanga 19 9 8 1 0 0
Sao Roque 1 8 1
TABLE II contd./
Nectomys squamipes
G.muris G.duod- MI^a
enalis
group group group
----------------------------------------
Conchas^b
Botucatu^c
Itaporanga
Sao Roque 1 1 1
a: MI mixed infection; b: Giardia was not Itaporanga
identified in two animals; c: Giardia was not Sao Roque
identified in three animals
TABLE III
Dimensions of Giardia trophozoites from Ratlus
railus railus, Bolomys lasiurus and Neclomys squamipes
captured in four regions of the State of Silo Paulo,
Brazil
Giardia Mean (um) Conchas Itaporanga
group R. rattus R. rattus B. lasiurus
------------------------------------------------------------
Giardia length 9.75 12.16 12.12
muris width 6.73 8.61 8.80
Giardia length 12.98 14.23 -
duodenalis width 6.47 9.75 -
TABLE III contd./
Giardia Mean(um) Sao Roque Range
group R. rattus N. squamipes Smaller Greater
--------------------------------------------------------------
Giardia length 13.26 13.28 9.75 13.28
muris width 8.61 6.73 8.80 8.72
Giardia length 16.77 18.32 12.98 18.32
duodenalis width 9.23 9.49 6.47 9.75
ACKNOWLEDGMENTS To Regina Spiekrs from the Zoology Museum of the State of Sao Paulo who helped us to identify the species of the captured animals. To Dr Semíramis Guimaraes Ferraz Viana for the review of the manuscript and Maria Aparecida Montanha Ramos for technical assistance. REFERENCES Carini A 1945. Lista dos parasitas novos ou ainda pouco conhecidos descritos pelo Dr. Carini. Arq Biol (Sao Paulo) 29: 1-6. Craum GF 1990. Waterborne giardiasis, p. 267-293. In EA Meyer, Human parasitic diseases: Giardiasis. Elsevier, New York. Filice FP 1952. Studies on the cytology and life history of a Giardia from the laboratory rat. Univ Calif Publ Zool 57: 53-146. Fonseca OOR 1916. Estudos sobre os flagelados parasitos dos mamiferos do Brasil. Mem Inst Oswaldo Cruz 8: 5-39. Frost F, Plan B, Liechty 1980. Giardia prevalence in commercially trapped animals. J Environ Health 42: 245-249. Haiba MH 1950. Giardiasis of the rats. Trans R Soc Trop Med Hyg 44: 360-361. Haiba MH 1956. Further study on the susceptibility of murines to human giardiasis. Z Parasitenk D 17: 339-345. Hamajima F, Ishii Y 1963. Studies on the parasites of the japanase house mouse, Mus molossinus. Kyushu J Med Sci 14: 55-59. Jakubowski W 1990. The control of Giardia in water supplies, p. 335-353. In EA Meyer Human parasitic diseases: Giardiasis. Elsevier, New York. Kasai Y 1978. Studies on helminth and protozoan parasites of rats in Sapporo. Jpn J Vet Res 26: 31. Kirner JC, Littler JD, Angelo LA 1978. A waterborne outbreak of giardiasis in Camas. Washington. J Am Water Works Ass 70: 35-40. Kulda J, Nohrynkova E 1978. Giardia and giardiasis, p. 69-138. In JP Kreier Parasitic Protozoa. Academic Press, New York. Navin TR, Juranex DD, Ford M, Minedew DJ, Lippy EC, Pollard RA 1985. Case control study of waterborne giardiasis in Reno, Nevada. Am J Epidemiol 122: 269-275. Nowak RM 1991. Rodentia, p. 668-679. In RM Nowak WalkerÆs Mammals of the World. The Johns Hopkins University Press, Baltimore. Pacha RE, Clark GW, Williams EA 1985. Occurrence of Campylobacter jejuni and Giardia sp. in muskrat (Ondrata zibethica). Appl Environ Microbiol 50: 177-178. Pacha RE, Clark GW, Williams EA, Carter AM, Scheffelmaier JJ, Debusschere P 1987. Small rodents and other mammals associated with mountain meadow as reservoirs of Giardia sp. and Campylobacter spp. Appl Environ Microbiol 53: 1574-1579. Vanzolini PE, Papavero N 1967. Manual de coleta e preparaçao de animais terrestres e de água doce, Secretaria da Agricultura do Estado de Sao Paulo, Departamento de Zoologia, Sao Paulo, 223 pp. Vives N, Zeledon 1957. Observaciones parasitologicas en ratas de San Jose, Costa Rica. Rev Biol Trop 5: 173-194. Supported by FAPESP (82/2348-5 and 83/1428-7)
Received 7 November 1994 Accepted 5 June 1995 Copyright 1995 Fundacao Oswaldo Cruz (FIOCRUZ)
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