Secondary Reservoir Role of Domestic Animals Other Than Sheep and Cattle in Fascioliasistransmission Inthenorthern Bolivian Altiplano
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Research and Reviews in Parasitology, 57 (I): 39-46 (1997) Published by A.P.E. © 1997 Asociaci6n de Parasitologos Espaiioles (A.P.E.) Printed in Barcelona. Spain SECONDARY RESERVOIR ROLE OF DOMESTIC ANIMALS OTHER THAN SHEEP AND CATTLE IN FASCIOLIASISTRANSMISSION INTHENORTHERN BOLIVIAN ALTIPLANO 1 1 I 3 S. MAS-COMA',A. RODRIGUEZ , M.D. BARGUES , M.A. VALERO , J.R. COELLd & R. A GLES IDeportamento de Parasitologia, Facultad de Farmacia, Universidad de Yatencia, AI'. Yicente Andres Estelles Sill, 46100 Burjassot - Yalencia, Spain 2LaboralOrio de Biologia, Colegio "Sail Calixto», Casilla 283, La Pa; Bolivia 3Ullidad de Parasitologia, lnstltuto Nacional de l.aboratorios de Salud «Nestor Morales Yillaton» (INLASA). Pasaje Rafae/Subieta No. 1889, Miraj7ores, La Pat; Bolivia Received 29 March 1997; accepted 25 May 1997 REFERENCE:MAS-COMA(S.), RODRIGUE(ZA.), BARGUES(M.D.), VALERO(M.A.), COELLO(J.R.) & ANGLES(R.), 1997.- Secondary reservoir role of domestic animals other than sheep and cattle in fascioliasis transmission in the Northern Bolivian Altiplano. Research and Reviews in Parasitology, 57 (I): 39-46. ABSTRACTR: esearch studies were undertaken to analyse the possible reservoir role played by pigs, donkeys, horses, llamas and alpacas present in the Fasciola hepatica human endemic region of the Northern Bolivian Altiplano. Coprological analyses showed liver fluke eggs in the stools of 27, I% of 59 pigs, and 15,4% of 65 donkeys.Egg output (eggs per g of faeces: epg) was 4-65 epg (mean: 21,6 epg) in pigs and 3-10 I epg (mean: 38,8 epg) in donkeys. No positive samples were found in horses, goats and llamas. A comparison with a coprological control study performed in sheep (61,5% of 26 sheep infected, with a range of 3-145 epg and a mean of 44,7 epg) and with literature data on alpacas and cattle from the same endemic region is carried out. According to the populations of pigs, donkeys. horses, goats, llamas and alpacas present in the endemic region, it may be concluded that only pigs and donkeys represent potential reservoir hosts of the parasite in the orthern Bolivian Altiplano. The need to take pigs and donkeys into account within preventive and control measures is pointed out. KEYWORDS:Fasciola hepatica. transmission, pigs, donkeys. horses, goats. llamas, alpacas, prevalences, egg output. human fascioliasis, orthern Bolivian Altiplano. I TRODUCTION cies concomitantly parasitizing F. hepatica-infected hu- man subjects (ESTEBAN et al., I997a, c, d). Besides its well-known veterinary importance (MA- Multidisciplinary studies were undertaken to unders- LEK, 1980; BORAY, 1982), fascioliasis by Fasciola hepa- tand how this digenean parasite is able to reach such tica (Linnaeus, 1758) (Trematoda: Fasciolidae) has also high transmission rates in the orthern Bolivian Alti- proved to be a great worldwide health problem (CHE & piano, a region of a very high altitude of 3800-4100 m. MOTT, 1990; MAS-COMA et al., 1997; MAS-COMA, BAR- Up to the present, the Altiplanic liver fluke has shown no GUES & ESTEBAN, 1997). Recent papers estimate human significant difference when compared to European F. infection up to 2,4 million (RIM et al., 1994) or even 17 hepatica, both at genotypic (MARQUEZ & MAS-COMA, million people (HOPKINS, 1992). Studies carried out in 1993) and phenotypic levels (VALERO et al., 1997). Con- recent years have demonstrated that the most important cerning the intermediate snail host, despite initial reports human fascioliasis endemic regions are located in South of two different Iymnaeid transmitting species (Lymnaea America (MAS-COMA et al., 1995; WHO, 1995; HILL- viatrix d'Orbigny, 1835 and Lymnaea cubensis Pfeiffer, YER & APT, 1997; MAS-COMA, BARGUES & ESTEBAN, 1839 variety) in the Bolivian Altiplano (UENO et al., 1997). 1975), it has been recently demonstrated that only one Among the human fascioliasis endemic regions, the transmitting species is there. Shell morphology Northern Bolivian Altiplano has shown to be the area in (OVIEDO, BARGUES & MAS-COMA, 1995a; ROUMEGOUX which the highest human prevalences and intensities are et al., 1997), visceral mass anatomy (OVIEDO, BARGUES known. Different studies have reported human prevalen- & MAS-COMA, 1995a; ROUMEGOUX et al., 1997), mole- ces of up to 70% in coprological surveys (MAS-COMA et cular (BARGUES & MAS-COMA, 1997; BARGUES et al., al.,1995;ESTEBA et al., 1997a,b;A GLESetal., 1997) 1997) and isoenzyme (JABBOUR-ZAHAB et al., 1997) and even higher in immunological surveys (HILL YER et studies have proved that this species is the European al., 1992; MAS-COMA et al., 1995; BJORLAND et al., Lymnaea truncatula (MUlier, 1774), most probably in- 1995; STRAUSS et al., 1997). lntensities in Bolivian chil- troduced by Spanish colonizers long ago. dren, measured as egg output in stools, ranged from 24 Veterinary surveys performed by both coprological and to 5064 eggs per gram (epg), with arithmetic and geome- serological tests have shown that sheep and cattle present tric means of 474-100 I and 201-309 epg, respectively high F. hepatica infection prevalences and intensities in (ESTEBAN et al., 1997b). Moreover, the human fasciolia- the Altiplanic endemic zone (UENO & MORALES, 1973; sis problem in the Altiplano is increased by the presence UE 0 et al., 1975; MAS-COMA et al., 1995; BUCHON & of many other pathogenic protozoan and helminth spe- MAS-COMA, 1995; HILLYER et al., 1996; BUCHON et al., 40 S. MAS-COMA et al. 1997). At any rate, these prevalences and intensities To consider a mammal species able to play a signifi- found in Altiplanic sheep and cattle are similar to those cant role in the transmission of the liver fluke in a given known in other non-human endemic regions, that is, not zone, different aspects must converge: A) the parasite as high as to constitute a very large environmental conta- must be able to develop, mature and produce eggs that mination with liver fluke eggs. It must be taken into ac- are expelled with faeces; B) prevalences must be suffi- count that Iymnaeid snail populations in the Altiplano do cient and not sporadic in time; C) egg output must be not appear to be numerous and dense (OVIEDO, BARGUES sufficiently high; D) populations of the mammal species & MAS-COMA, I995b) enough to explain by themselves in question must be sufficiently numerous and dense; E) the very high human infection rates. parasite eggs shed with stools must prove to be viable, With the aim to investigate other factors that can im- that is, able to embryonate, hatch, the miracidium capa- prove liver fluke transmission in the orthern Bolivian ble to infect a susceptible Iymnaeid snail, intramolluscan Altiplano, research studies were undertaken to analyse larval stages be able to develop, cercariae to be produ- the possible reservoir role which could be played by ot- ced, shed in sufficient number and metamorphose into her domestic animal species present in the endemic encysted metacercariae, and the latter be able to success- zone. In the Altiplano, Aymara inhabitants markedly de- fully infect a susceptible definitive host species. pend upon livestock, owing to the agricultural difficul- The present paper deals with aspects A, B, C and 0 ties proper to the high altitude. That is why numerous ot- concerning large mammal species. Studies being pre- her domestic mammal species are present in the region sently carried out on aspect E in large mammals, as well (MAS-COMA et al., 1995): large mammals such as pigs, as on all aspects concerning small mammals, will be the donkeys, horses, goats, llamas and alpacas; small mam- objectives of further papers. mals such as lagomorphs (rabbits, hares) and even ro- dents (guinea pigs). All these species have already de- MATERIAL ANDMETHODS monstrated their capacity to be successfully infected by F. hepatica (BORAY, 1982; MAS-COMA et al., 1987, Animal samples: Animals surveyed were in localities where the 1988). presence of Iymnaeid snails assuring F. hepatica transmission was Fig. 1.- Map of the fascioliasis human endemic region in the Northern Bolivian Altiplano showing localities in which domestic animal stool samples were obtained. I = Queroni; 2 = Huacullani; 3 = Chojasihui; 4 = Lacaya Baja; 5 = Chiripujo; 6 = Korila; 7 = Caleria; 8 = Chi- jipata Alto; 9 = Batallas; 10= Chirapaca; II = Palcoco; 12 = Ancocagua: 13 = Tambillo. Secondary reservoirs of fascioliasis in the Bolivian Altiplano 41 previously verified (Fig. I). Localities in areas where human pre- Although familial herds comprising only one animal can valences and intensities have proved to be high were preferentially be observed (most usually sheep or cattle, sometimes surveyed, such as the Chirapaca-Batallas-Chijipata Alto-Cutusuma pigs, rarely donkeys), they almost always include more area in the so-called «corridor of Batallas» (MAs-CoMA et al .. than one species (two, sometimes three, rarely four diffe- 1995;ESTEBAN et al., 1997b; ANGLES et al., 1997; STRAUSS et al., 1997), and the Chiripujo-Chojasihui-Lacaya Baja-Huacullani- rent species together), among sheep, cattle, pigs and Queroni area in the so-called «corridor of Huacullani» (ESTEBAN et donkeys (Fig. 2 B, D, H). In the endemic zone a family al., 1997a). Stool samples from llamas could only be obtained at a has approximately 1-2 cattle, sheep, pigs, and 4-5 birds. weekly trade fair of llamas in the locality of Paicoco. Estimates of After official data, the estimated animal population in- the populations of all domestic animal species were made during cludes 6 sheep and 3,4 cattle per family. In the locality numerous visits to all zones of the Northern Bolivian Altiplano en- of Ancocagua, for instance, familial herds include 0-50 demic region carried out in the 1992-1997 period. sheep (mean 14,6), 0-17 cattle (mean 8, I), and 0-4 don- Stool collection and preparation:Stool samples were obtained keys (mean 0,9). In Chijipata Alto, herds sometimes from pigs, donkeys.