Human Fascioliasis in Bolivia: a General Analysis and Acriticalreview of Existing Data

Home , Cutusuma, El Alto, Huarina, Ingavi Province, Omasuyos Province, Palca Municipality

HUMAN FASCIOLIASIS IN BOLIVIA: A GENERAL ANALYSIS AND ACRITICALREVIEW OF EXISTING DATA

2 S. MAS-COMA', R. ANGLES\ W. STRAUSS , J.G. ESTEBAN', J.A.OVIEDO' & P. BUCHONI.3

I Departamento de Parasitologia, Facultad de Farmacia, Universidad de Valencia, Av. Vicente Andres Estelles sin, 46100 Burjassot - Valencia, Spain 2Division de Parasitologia y Micologia, lnstituto Nacional de Laboratorios de Salud «Nestor Morales villazon» (INLASA), Secretaria Nacional de Salud, Ministerio de Desarrollo Humano, Pasaje Rafael Subieta No. 1889 (lado del Estado Mayor General), Miraflores, La Paz, Bolivia 3Laboratorio de Sanidad Animal de Kallutaca, Programa de Fomento Lechero, Corporacion Regional de Desarrollo de La Pa; (CORDEPAZ),

Av. Juan Pablo 11, Crra. de El Alto kill 5, El Alto, Bolivia

Received 15 November 1994; accepted 3 March 1995

REFERENCE:MAS-COMA(S.), ANGLES(R.), STRAUSS(W.), ESTEBAN(J.G.), OVIEDO(J.A.) & BUCHON(P.), 1995.- Human fascioliasis in Bolivia: a general analysis and a critical review of existing data. Research and Reviews in Parasitology, 55 (2): 73-93.

SUMMARY:The large extent of human fascioliasis by the liver fluke species Fasciola hepatica has only been recognized in recent years. However, most of the literature dealing with human fascioliasis refers to more or less isolated cases, so that only a few real endemic regions of human fascioliasis have been investigated up to the present. Bolivia does not even appear in recent reviews, because previous case reports were not published or published in local journals or diffusion booklets. Thus, published information is very scarce, despite the facts that the human endemic of fascioliasis in the Bolivian orthern Altiplano is well known to specialists and the zone has proved to have the highest human prevalences recorded. This paper aims to establish the real situation of knowledge on this human fascioliasis endemic by reviewing the existing literature on fascioliasis in the orthern Altiplano of Bolivia, composed mainly of unpublished documents and locally published reports. Most of these reports and studies were made by non-specialists and, consequently, the data furnished have not been appropriately reviewed and must therefore be considered in their true value, in many cases only at informative or suggestive level. This does not mean, however, that this large set of data is not very valuable. This review shows that there is useful information available on several important aspects, mainly coprological and immunological surveys on humans, sheep and cattle. Coprological and serological survey results include prevalences up to 72% and 100% in humans, up to 100% and 89% in sheep, and up to 100% and 60% in cattle of given localities, respectively. In humans, the existence of other parasitic diseases makes it difficult to establish clinical and pathological patterns, morbidity and mortality caused by fascioliasis. Bolivian official organisations recognize the important impact of both the human health problem and the veterinary economic and production losses due to fascioliasis in the Altiplano. Accordingly, national control programmes have already been established. But unfortunately the knowledge concerning essential aspects is largely insufficient. Concerning the liver fluke, there is no research work carried out on parasite species determination nor on its life cycle and transmission, a fact which is very important, taking into account that F. hepatica appears to be a parasite typical of very low altitude regions and sea level zones in other parts of the world. The Bolivian human endemic zone is located between Lake Titicaca and the valley of the city of La Paz, at an altitude of 3800-4100 m, although field research is needed to establish the real geographical extent of the human and livestock health problems. The few studies undertaken on the in- tennediate snail hosts suggest the presence of two different Iymnaeid species in the endemic area, Lymnaea viatrix and L. cubensis var., both with the capacity of transmitting the parasite. At any rate, both malacological and parasitological data need specialist confirmation, taking into conside- ration that these two species are typical American sea level region inhabitants. Studies on potential wild animal reservoirs, such as hares and mainly murid and herbivorous caviomorph rodents, possibly playing a role in parasite transmission, are needed. There is much information on human nutritional status, habits, ethnic customs and religious aspects of the Ayrnara inhabitants, which may be related to the disease. Careful studies on milieu characteristcs, environmental and climatic conditions related to fascioliasis are lacking.

KEY WORDS:Human fascioliasis, review, Northern Altiplano, Bolivia.

CONTE TS

Introduction. 74 The parasite .. 75 Species determination 75 Life cycle and transmission .. 75 The endemic zone. 76 The geographic distribution of Fasciola hepatica. 76 The milieu and environmental risk factors 77 Plants involved in transmission. 78 The human host. 78 Coprological and immunological surveys. . . 78 Clinical and pathological observations. 81 ational control programmes. 81 Association with other parasite species 82 Human contamination sources. 82 utritional status. 83 74 S. MAS-COMA et al.

Human habits, ethnic customs and religious aspects . 83 Treatment 84 The molluscan intermediate host. 85 Species determination. 85 Geography, ecology and population dynamics. 85 Snail control measures.. 86 The domestic animal reservoirs . 86 CoprologicaJand immunological surveys .. 86 Sheep . 86 Cattle. 86 Alpacas 89 Economic and production losses due to fascioliasis. 89 National control programmes . 89 Treatment.. 89 The potential free living animal reservoirs. 90 Acknowledgements. 90 References.... 90

INTRODUCTION fascioliasis in the Northern Altiplano of Bolivia is exten- sive. This literature is, however, composed mainly of un- The recent review by CHEN & Morr (1990) has de- published papers of different types (reports to ministries; monstrated that human fascioliasis is more important internal reports of organisms; university theses; a few than was formerly believed, that human infection by papers presented to meetings; etc.). Moreover, most of Fasciola hepatica (Linnaeus, 1758)(Trematoda:Fascio- these reports and studies were made by non-specialists lidae) takes place in all continents and that in given and, consequently, the data furnished have not been ap- countries the number of cases is high. Thus, this disease propriately reviewed and must therefore be considered in has been largely underestimated, above all when taking many cases only at informative or suggestive level. This into account the number of cases in which infection is does not mean, however, that this large set of data is not not diagnosed, whether due to an asymptomatic or little- very valuable. That is why a complete review was under- symptomatic disease course or to an incorrect diagnosis taken to establish the real situation of knowledge before of the causes in symptomatic cases. Today, knowledge the beginning and during the first phases of the above- clearly suggests that if carefully researched, the extent mentioned research project. and prevalences all over the world would be markedly The aim of this paper is to present the results of this re- larger than what is shown in the review table made by view. Because of the unpublished nature of most of the CHE & Morr (1990). reports considered, most references cited at the end of However, most of the literature dealing with human this article will be unavailable for the reader. But the au- fascioliasis refers to more or less isolated cases (CHEN & thors of the present review consider that justice must be Morr, 1990), so that only a few real endemic regions of done to so many persons from different origins and pro- human fascioliasis have been investigated up to the pre- fessions who in one way or another have contributed to sent: Portugal (SAMPAIO SILVA in CHEN & Morr, the knowledge of fascioliasis in the endemic region of 1990), Iran (BAHAR et al., 1990; MASSOUD, 1990; POUR- the Bolivian Northern Altiplano, a zone which has pro- TAGHVA et al., 1990), Peru (STORK et al., 1973; KNo- ved to present the highest human prevalences by F. he- BLOCH, 1985; K OBLOCH et al., 1985; NAQUIRA, pers. patica infection, as already emphasized by HILL YER et comm.) and Bolivia. al. (1992). Bolivia does not even appear in CHEN & Mo'rr's Owing to the Bolivian administrative tradition of ma- world review (1990), because previous case reports were king numerous internal reports in official and public or- not published or published in local journals or diffusion ganisations and institutions, we cannot be sure that this booklets. Only one paper has appeared after 1990 in an review covers all studies carried out on human and ani- international journal (HILLYER et al., 1992). Thus pu- mal fascioliasis in the Bolivian Northern Altiplano.We blished information is very scarce, despite the fact that assume that there are most probably a very few other un- the human endemic of fascioliasis in Bolivia is well published papers which we were unable to find or obtain known to specialists, at least in the recent years. (e.g. ARAUJO, 1965; PA YNO, 1977; BOTELLO, MACH 1- In 1992, when starting a large multidisciplinary inter- CADO & PUCH, 1981). It must also be taken into account national project on human fascioliasis in the Bolivian that the results obtained in human and animal fasciolia- Northern Altiplano, a careful search for previously sis studies performed in recent years by the Bolivian co- known data on the question was initiated. During these authors of the present paper are actually being analysed last years it has been found that the existing literature on for future publications and consequently the contents of Human fascioliasis in Bolivia 7S the related unpublished internal reports made at the time tiplanic endemic zone in question has a mean altitude of of these surveys are not included in this review. At any about 4000 m and F. hepatica is a parasite which is typi- rate, we consider that the large information compiled in cally present in low altitude zones. At any rate, several the present review is sufficient as to correctly estimate fascioliasis endemic zones, both by F. hepatica and Fas- the present situation of knowledge on this very impor- ciola gigantica Cobbold, 1855, are known in altitude re- tant medical and veterinary health problem in Bolivia, gions, in Europe (MANGA-GONZALEZ, GONZALEZ- and hence merit the appropriate published diffusion. Per- LANZA & OTERO-MERINO, 1991; PAREAU et al., 1994), mission to use and refer to the contents of the unpubli- Africa (BERGEON & LAURENT, 1970; SCOTT & GOLL, shed internal reports was previously obtained in all cases. 1977; VAN SOMEREN, 1946; LOKER et al., 1993) and In the very few cases in which permission was denied for Asia (KE DALL, 1954; KE DALL & PARFITT, 1959; Mo different reasons, neither is the content reviewed nor is REL & MAHATO, 1987), as well as in Central (PEREZ-RE- the paper included in the references. YES, JIME EZ- AVA & VARELA-RAMIREZ, 1985) and South America (MORALES & PINO, 1981, 1983). These reports concern, however, transmission zones of only an THE PARASITE intermediate altitude of no more than 2000-2500 m. Inte- restingly anyway, potential Iymnaeid intermediate snail host species are able to reach higher altitudes than the di- Species determination genean parasite within the same region, as is the case of The existence of F. hepatica in the Bolivian Northern the European Lymnaea truncatula (MUlier, 1774) (Gas- Altiplano has long been known. Indian inhabitants in tropoda: Lyrnnaeidae), which has been found even up to this region usually know the presence of this liver fluke, 2600 m (EUZEBY, 1971), whereas F. hepatica is never which they call «talpalako» in the Aymara language. found in such altitudes in Europe. Most probably, this However, the first published reports on this digenean pa- phenomenon is related to a lack of compatibility be- rasite in the Bolivian Altiplano did not appear until the tween the parasite and the altitude population snails, as seventies. Research activities carried out by UENO and suggested by the results of a first assay carried out in the eoworkers on the presence of F. hepatica in domestic Department of Parasitology of the University of Valen- animal hosts and also in molluscan intermediate hosts cia, Spain. (ARANDIA, 1972; UENO & MORALES, 1973; MORALES In the neighbouring country of Peru there are several LAVADENZ, 1973; UENO et al., 1975) seem to be the pa- endemic zones also located in high altitude regions, such pers which gave rise to the long list of investigations car- as the Cajamarca valley, Mantaro valley, etc. (STORK et ried out mainly by local but also by a few foreign resear- al., 1973; KNOBLOCH, 1985; KNOB LOCH et al., 1985; chers on the veterinary problem of fascioliasis in the NAQUIRA, pers. comm.). However, no appropriate cha- Altiplanic region in question. racterization studies of the F. hepatica strains involved As for human fascioliasis, the first known reports con- have been undertaken up to the present, as in the Boli- cern only cases diagnosed in the city of La Paz. The pa- vian Northern Altiplano. per by HARTMA N & PATl-O (1962), which concerns In the Altiplano, it is unquestionable that F. hepatica only a two-case clinical report in La Paz, is the first pu- has perfectly adapted to such an altitude, but we do not blished paper that could be found. However, the first know what bioecological strategies it has used to adapt mention of human fascioliasis in Bolivia was made by nor what the epidemiological and pathological conse- PINILLA & PAZ in the journal «El Hospital} in 1939, and quences of this adaptation are. Moreover, we have here afterwards PINILLA published a long paper on 20 human not only a peculiar altitude-adapted strain, but also diffe- cases detected in La Paz in the journal «Semana Me- rent involved definitive and intermediate host species dica» of Buenos Aires. Studies on human fascioliasis did detected so far, all this together with the possibility of not start until the paper by VERAZAI (1982) which was other free-living mammal species also having a role of followed by the more important research activities of reservoir in the Altiplano. The altitude adaptation and A GLES and eo workers (ANGLES, 1986 a, b; Mo TERO the different possible transmission circulations open a BUSTILLOS, 1987; MOll A PADILLA, 1987; CE TELLAS wide spectrum of very interesting genetic divergences. GUEVARA, 1987). Afterwards, the larger diffusion rea- The need for research on the genotypic and phenotypic ched by the booklet written by CACERES VEGA (1989) characterization of this altitude adapted strain of F. he- constituted the basis on which foreign specialists be- patica by appropriate techniques is evident. came interested. It is worth mentioning, however, that in reality no ap- Life cycle and transmission propriate study on the parasite itself has been carried out, whether by means of a detailed morphoanatomic parasi- No research work on the life cycle of the parasite in tological study or through more sophisticated techniques the Bolivian Altiplano has been done. There are, howe- (isoenzymes, molecular probes, etc.). In fact, in no paper ver, a few dispersed data which furnish interesting infor- can a mention of parasite determination be found. This mation, mainly concerning prevalence distribution aspect takes on great interest when we recall that the AI- throughout a year's period. 76 S. MAS-COMA et al.

VENO et al. (1975) carried out attempts to infect Alti- fascioliasis in Bolivia is mainly known from the Alti- planic Iymnaeid snails in the laboratory, but unfortuna- pIano. Nevertheless, there are not so many Altiplanic lo- tely (due to the cold temperature of the laboratory condi- calities in which studies on human and/or animal facio- tions) no successful experimental infection with eggs up liasis have been carried out. to cercariae shedding was obtained after 4 months post- In the Bolivian Altiplano, F. hepatica has only been infection, although immature rediae could be seen after detected in the Department of La Paz (surface: 133985 10 weeks. The same authors mentioned that during the km'; 2406185 inhabitants in 1990) covering different lo- period December 1971 to May 1972, a total of 44 (6,4%) calities of four provinces in the Northern Altiplano and among 664 Lymnaea viatrix from Achocalla, Belen, Ba- the neighbouring large valley of the city of La Paz: tallas and Chirapaca were naturally infected with F. he- A) Los Andes Prov.: patica, with great differences depending on the area, and -Batallas: the digenean parasite has been detected in hu- that 36 (12,3%) of 292 Lymnaea cubensis var. were in- man beings (VELA PACHECO, 1988), in cattle (LOZANO fected. According to these authors, in the Altiplano, cer- Mo ROY, 1974) and in Iymnaeid snails (UE 0 et aI., carial shedding is suspected to take place over a period 1975); from April to July. -Calasaya: in humans (McAuLEY, 1991; BJORLA D et At definitive host level, VENO et al. (1975) noted that aI., 1992); outbreaks of acute fascioliasis in domestic animals were -Chijipata Alto: in humans (VELA PACHECO, 1988); recorded from the end of April to the beginning of Au- -Chirapaca: in sheep (MORALES LAVADENZ, 1973; Lo gust, especially from May to July, or in the dry season of ZANO MONROY, 1974; UENO et aI., 1975), in cattle June and July. ORTUBE GOITIA(1986) gave information (ARANDlA, 1972; MORALES LAVADENZ, 1973; r.o. on the yearly chronology of cattle infection by F. hepa- ZA 0 Mo ROY, 1974; UENO et aI., 1975) and in Iym- tica in the Kallutaca area. This author detected the follo- naeid snails (MORALES LAVADENZ, 1973; UE 0 et al., wing prevalences by coprological analyses: 9,3% in Oc- 1975); tober; 15,6% in January; 42% in April; 26,5% in May; -Chojasivi: in sheep (STU DELL & MOLLINEDO, 1978; 51 % in June; 36% in July; 46,8% in August; and 31 % in MARTlNEZ et al., 1991). September. -Collantaka: in cattle (LOZANO MONROY, 1974); -Corapata: in humans (BRYAN et aI., 1989; ANGLES, 1990; HrLLYER et al., 1992), in sheep (VILLCA, CRUZ THE ENDEMIC ZONE & ALCON, 1989; HILLYER, SOLERDE GALANES, Bu CHON & BJORLAND, 1993) and in cattle (VILLCA, CRUZ & ALCON, 1989; HILLYER, SOLERDE GALANES, Bu- The geographic distribution of Fasciola hepatica CHO & BJORLAND, 1993); The presence of F. hepatica is known in several parts -Cullucachi: in humans (VERAZAI , 1982; CACERES of the country of Bolivia (Cochabamba, Sucre, Santa VEGA, 1989); Cruz, etc. -e.g. see CUEV AS, 1980" all very far from the -Cutusuma: in humans (ANGLES, 1986 a, b; MONTERO area of the orthern Altiplano and neighbouring valley BUSTILLOS, 1987; MOLL A PADILLA, 1987; CENTE- of the city of La Paz here reviewed. In several of these LLAS GUEVARA, 1987); places, prevalences in domestic animals appear to be -Kallutaca: in humans (ORTUBE GOIT/A, 1986), in sheep very high, as the 100% detected in sheep (20 animals in- (LOZANO MONROY, 1974; VILLCA, CRUZ & ALCON, fected among 20 studied) from Callimbaya (prov. Sud 1989) and in cattle (ORTUBE GOITIA, 1986; VILLCA, Yungas) by LOZANO MONROY (1974). The finding of CRUZ & ALCON, 1989); unidentified operculate ova (45X35 urn) resembling -Santa Ana: in humans (McAuLEY, 1991; BJORLAND et fluke eggs in children from Amarete, a village situated at al., 1992); 3700 m altitude and 200 km north of La Paz, by BASSET, -Takachira: in cattle (LOZA 0 Mo ROY, 1974); GAUMERAIS & BASSET-POUG ET (1986), does not seem -Tambillo: in cattle (LOZA 0 Mo ROY, 1974). to concern fascioliasis, but is probably a cestodiasis by a B) Omasuyos Prov.: pseudophyllidean. -Belen: in sheep (MORALES LA VADENZ, 1973; LOZANO Except the region of the Northern Altiplano, in all ot- MONROY, 1974; VE 0 et aI., 1975), in cattle (ARAN- her zones or localities fascioliasis is known as a veteri- DIA, 1972; MORALES LAVADENZ, 1973; LOZANO MON- nary problem.At any rate, sporadic human cases have ROY, 1974; UENO et aI., 1975), in alpacas (MORALES been found in these regions, e.g. VELA PACHECO (1988) LA VADENZ, 1973; LOZANO MONROY, 1974; VENO et mentioned fascioliasis in a child interned in the Hospital al., 1975) and in Iymnaeid snails (MORALES LAVA- del Nifio de La Paz, coming from the locality of Vinto, DENZ, 1973; UENO et al., 1975); prov. Quillacollo (Cochabamba). -Chua: in humans (VELA PACHECO, 1988); In the Altiplano, moreover, fascioliasis appears to -Huarina-Cota Cota Alta: in sheep (LOZA 0 MONROY, constitute a very important human health problem. This 1974); is why many local authors and a few foreign specialists -Pajchani: in sheep (LOZA 0 MO ROY,1974); have specially studied this region. As a consequence, -Tauca: in humans (ANGLES, 1986 a; Mo TERO BUSTI- Human fascioliasis in Bolivia 77

LLOS, 1987; MOLINA PADILLA, 1987; CE TELLASGUE- The milieu and environmental risk factors VARA, 1987). C) lngavi Prov.: Only a few authors (VILLCA, CRUZ & ALCO , 1989; - Viacha: in sheep (MORALES LA VADE Z, 1973; UE 0 et CACERES VEGA, 1989) have analysed the Altiplanic mi- aI., 1975) and in cattle (MORALES LAVADEZ, 1973; lieu from the point of view of fascioliasis-related envi- UE 0 et aI., 1975); ronmental risk factors. VILLCA, CRUZ & ALCON(1989), D) Murillo Prov.: when studying fascioliasis in Corapata (a community -Achocalla: in humans (LOZA 0 Mo ROY, 1974), in with a human population of 1200 inhabitants living in sheep (UE 0 et aI., 1975), in cattle (MORALES LA VA- 299 habited houses), mentioned the presence of large DE Z, 1973; SALAZARESCOBAR, (979) and in Iymna- plains with permanent humidity favouring snail multipli- eid snails (MORALES LAVADE z, 1973; UE 0 et aI., cation. Such natural conditions are the consequence of 1975); the abundance of water from the thaw of the snows of -El Alto: in cattle (SALAZARESCOBAR, 1979); the mountains, originating canals and permanent pools -La Paz: in humans in several hospitals (PINILLA & PAZ, of water. 1939; PINILLA, 1939; HARTMANN & PATINO, 1962; The study of CACERES VEGA (1989) on the commu- FLORES SERNA & ESTEVEZ MARTINI, 1988) and in cat- nity of Cullucachi (mean temperature of 9,4° C; mean tle in the suburbean area (SALAZAR ESCOBAR, 1979) as rainfall of 5,736 mm) was more complete. According to well as in the slaughterhouse of La Paz (FLORESSERNA this author, the lacustrian region, including the zones of & ESTEVEZ MARTINI, 1988); Cullucachi, Pefias and Pucarani, comprises about 10% of -Palca: in cattle (SALAZAR ESCOBAR, 1979); the national population, that is, approximately 500000 -RIo Abajo: in cattle (SALAZAR ESCOBAR, 1979). inhabitants distributed in not more than 5000 km', which means it is the most densely inhabited zone of the The results obtained in surveys on human subjects country, with about 40 inhabitants per km", This author from the communities of Cutusuma, Chijipata Bajo, Chi- described the soils of the zone in detail, as being heavy jipata Alto, Paitiri, Karapata, Esquiri, Cachilaya, Oque- and scarcely acid, with imperfect drainage owing to the titi, and Wilajahuira made by ESPA - A VASQUEZ (1989) superficiality of the phreatic levels, including pasture are not included in this list, because in said paper the grasslands with permanent irrigation called «bofedales», geographic origin of the positive samples is unfortuna- with natural vegetation comprising short and juicy grass. tely not specified. These lands, with scarce drainage, present a 50-90 cm According to the above-noted list, the distribution of layer of humus, are rich in organic substances and ac- F. hepatica in the Northern Altiplano seems to cover quire a typical black colour, although they can be dark parts of the four political provinces. According to the brown in low draining conditions. The influence of Lake I E(1992), the surface and human population of these Titicaca makes this zone favourable for agricultural provinces of Bolivia (surface of the country: 1098581 work. Livestock, fundamentally cattle, pig and sheep, km'; total human population in Bolivia: 6344396 inhabi- develops mainly on the esplanade and «bofedales» under tants) are as follows: Los Andes: 1658 km2 and 61627 rustic breeding systems. The author emphasized the mar- inhabitants; Omasuyos: 2065 km2 and 73415 inhabitants; ked decrease of sheep populations because of the lack of Ingavi: 5410 km2 and 77896 inhabitants;Murillo: 4705 animal health and the contamination of grasslands. Simi- km2 and around 1200000 inhabitants, including the two larly, he described the under-nourished appearance of most important cities, La Paz and El Alto with 710940 cattle and pigs, despite the abundance of forage, because and 392774 inhabitants, respectively. Geographically, of parasite infections and the lack of permanent grass- the parasite distribution concerns mainly the corridor lands. In spite of this economic deterioration, most of the between the northern Oriental Andine mountain chain, rural families dedicate their daily work and base their in the North, and the small hill chain besides Pucarani economy on the breeding and fattening of cattle and and Cutusuma, in the South, and from the locality of El pigs. According to estimations by community authori- Alto, at an altitude of 4100 m in the East, to Lake Titi- ties, animal populations are less numerous than in the caca, at 3820 m altitude in the West. There is a northern rest of the Altiplano. Thus, in Cullucachi the approxima- extension around Lake Titicaca, which extends to Chua tely 250 families have an average of 1,28 cattle, 1,4 pigs, in the West and to Belen in the North. In the South the 4,28 birds, 0,6 rabbits, 0,12 mules and 0,08 sheep. Gene- most extreme locality appears to be Viacha. Concerning ral life conditions in Cullucachi have decreased in qua- the Eastern boundary, according to the results of surveys lity in recent years because of progressive reduction of in cattle, the endemic zone of the Altiplano extends into land productivity owing to a reduction of the agrarian the large valley of the city of La Paz, even up to RIO soils as well as to a degradation and contamination of Abajo, and marginal subvalleys of the La Paz valley soils due to excessive overpasturing and the lack of crop such as Achocalla. After the findings of the parasite in rotation. human subjects in La Paz hospitals, it is clear that the ru- Although not mentioned in any written document or ral problem of fascioliasis in the Altiplano shows an ex- report consulted, human inhabitants of the endemic zone tension in the urban and suburbean areas of La Paz. most frequently relate the disease with Lake Titicaca. 78 S. MAS-COMA et al.

Local people tell about an increase of «talpalako», affec- 1970 to 1985 in three hospitals of La Paz (Hospital ting both humans and animals, taking place after the Obrero 0.1 de la CNSSLa Paz, Hospital de Clfnicas La inundation of large bordering zones of the Lake in the Paz, and Instituto Gastroenterol6gico Boliviano Japones year 1986 (see VACHER,BRASIERDE THUY & LlBER- La Paz). From these 95 cases, 80% of them were diagno- MAN, 1991). And although it appears to be true that the sed by clinical methods and 20% were surgical findings. parasite is more prevalent in the zone just around Lake Unfortunately, the authors noted no information on the Titicaca, the suggested liver fluke/Lake Titicaca rela- geographic origin of the patients nor on how and where tionship still remains to be appropriately analysed. they were infected. At any rate, FLORESSERNA& ESTE- VEZMARTINI(1988) and VELA PACHECO(1988) clearly demonstrated that the rural human health problem cau- Plants involved in transmission sed by F. hepatica in the Northern Altiplano has a geo- Only the paper of UENO et at. (1975) deals with the graphic urban extension in the city of La Paz. presence of metacercariae in plant species. These authors The first study on human fascioliasis carried out in the studied semi-aquatic plants collected from a swamp in Altiplano was made by VERAZAI (1982).This author the Achocalla province. According to the fluke number studied two Altiplano communities:Villa de la Cruz and obtained in guinea pigs experimentally infected with Cullucachi. Among students 4 to 20 years of age, 151 100 g of plant, they classified the plants as 7 kinds: Corn- stool specimens were examined. Of these, 90 (72%) positae: 56,3; Eleocharis sp.: 50,9; Senicio sp.: 12,0; Va- were positive. All of the positive specimens came from llisneria sp.: 10,3; Scirpus sp.: 3,3; Ranunculaceae: 2,6; students in Cullucachi. Of the 90 positive specimens, Liliaceae: O. 13,6% were from children aged 4-7 years, 36,0% from ages 8-11 years, 20,0% from ages 12-15 years, and 2,4% from subjects aged 16-20 years. THE HUMAN HOST The following survey on human fascioliasis in the Alti- pIano was carried out by ORTUBEGOITIA(1986) in Ka- Ilutaca. This author studied ninety 1-18 year-old children Coprological and immunological surveys coprologically by direct smear with lugol. The total pre- The paper by HARTMANN& PATlNO (1962) reports valence by F. hepatica was 47,7% (of which 61,12% two clinical cases diagnosed in the Hospital General in were males and 38,88% females), distributed according La Paz, one interesting extrahepatic case of subcutane- to age groups in the following manner: I in 5-year-old ous epigastric parasite location in a woman and another children (yoc), 8 in 6-yoc, 8 in 7-yoc, IS in 8-yoc, 12 in case of a 46-year-old man with parasite biliary location. 9-yoc, 9 in IO-yoc, 8 in l l-yoc, 13 in 12-yoc, 4 in 13-yoc, These authors opportunely noted that the first published 3 in 14-yoc, 4 in 15-yoc, I in 16-yoc, 2 in 17-yoc, and 2 papers on human fascioliasis in Bolivia were in fact in 18-yoc. Quantitatively, this author found 59 children those of PINILLA& PAZ (1939) and PI IHA(1939), who presenting 1-10 eggs in faeces (65,56%) and 31 with 10- made a report on 20 human cases also detected in La 20 eggs in faeces (34,17%)(the author did not follow a Paz. given methodological pattern; egg counting in faeces LOZANOMo ROY (1974) made a large coprological from each subject was done by summing eggs counted in survey of sheep and cattle coming mainly from different one or several microscope slides in each of which an un- localities of the Altiplano, and a few from another part of determined small amount of faeces had been put). Bolivia (prov. Sud Yungas), by means of the N.I.A.H. A more complete study was undertaken in 1986 and technique (sedimentation technique after the National 1987 by ANGLES,STRAUSSand coworkers in the locali- Institute of Animal Health of USA). Studying a total of ties of Cutusuma and Tauca. Human surveys were ca- 22 human stool samples from the village of Achocalla, rried out by coprological techniques (MONTEROBUSTI- in the valley of the city of La Paz, this author detected a LLOS, 1987), intraderrnoreaction test (MOll A PADILLA, moderate infection (10-30 eggs/5 g of faeces) in two of 1987), and indirect immunofluorescence test (CE TE- them (0,9% positive). LLASGUEVARA, 1987) applied to the same human sub- Other papers dealing with human fascioliasis cases jects (mainly schoolchildren). MARTT EZ et at. (1991) diagnosed in La Paz were those of VELA PACHECO noted that another human survey (a coprological study (1988) and FLORESSERNA& ESTEVEZMARTINI(1988). having yielded 25% positive in schoolchildren) was ea- VELAPACHECO(1988), carried out a clinical study of 7 rried out in the locality of Cutusurna in 1983 by the IN- cases in 3-13 year-old children hospitalized in the Hos- LASA Institute, but most probably they were confusing pital del Nifio of La Paz during 1986 and 1987, most of it with the 25% positive coprological survey carried out them coming from the Bolivian Altiplano: 2 from Chiji- by INLASA in the locality of Corapata mentioned by pata Alto, I from the region of Chua, and 2 from the VILLCA,CRUZ & ALCO (1989). zone of Batallas (of the two other cases, one was of un- Mo TERO BUSTILLOS(1987) used nine different eo- determined geographic origin and the other from Vinto, prological techniques: direct smear, Kato-Katz, gravity prov. Quillacollo, Cochabarnba). FLORES SER A & Es sedimentation, concentration by centrifugation with wa- TEVEZMARTINI(1988) reviewed 95 cases reported from ter, N.I.A.H. sedimentation technique, forrnol-ether con- Human fascioliasis in Bolivia 79

centration, the Charles and Barthelemy technique modi- tion tests. Unfortunately, this author does not report the fied by Greenway, the Bailenger technique, and the Ro- positive cases according to localities, nor to age groups. man technique. In Cutusuma a total of 115 subjects (72 Only a mention of a greater concentration of high levels males and 43 females) among 183 studied proved to be of antibodies in children younger than 15 is given. positive (52%) and in Tauca a total of 8 (4 males and 4 VILLCA, CRUZ & ALCO (1989) summarized the re- females) among 38 studied presented eggs in stools sults obtained in the studies carried out in the locality of (3,6%). No differences related to sex were found, with Corapata in 1988. These authors refer to a coprological 34,4% in males and 21,2% in females. The following study made by the INLASA Institute of 88 subjects of an prevalences according to age were found in Cutusuma age of 5-45 years, of which 25% were positive, as well and Tauca respectively: l-lO-year-old subjects (yos): as to an immunological survey by counterirnrnunoelec- 26,2% and 0%; 11-20-yos: 17,2% and 2,3%; 21-30-yos: trophoresis carried out in Puerto Rico which gave a 4% and 0%; 31-40-yos: 2,7% and 0,4%; 41-50-yos: 50,6% positive rate among 77 subjects studied, and fi- 1,8% and 0,2%; 5 I-60-yos: 0,4% and 0%; > 60-yos: 1% nally to an indirect immunofluorescence survey made by and 0%. INLASA which gave a 57,5% positive rate among 80 MOll A PADILLA(1987) applied an intradermoreac- subjects studied. On the whole, 55,4% of the subjects tion test with an antigen obtained from F. hepatica show positive for all the tests. adults from cattle. The test was considered positive if an The paper by CACERES VEGA (1989) is undoubtedly induration zone diameter of 5 mm or more appeared 48 h the most complete among those written by Bolivian after inoculation. In Cutusuma a total of 91 subjects (43 authors. This author reports a 13,5% positive rate obtai- males and 48 females) were considered positive among ned in a coprological survey of 275 schoolchildren by 113 studied (55 males and 58 females) (80,53% = 38% + means of the direct smear and formol-ether concentra- 42%). In Tauca a total of 13 subjects (10 males and 3 fe- tion techniques, as well as a 71,9% rate (= 57% positive males) were considered positive among 72 studied (42 + 14,9% doubtful) obtained with the complement fixa- males and 30 females) (18,05% = 13,8% + 4,2%). Ac- tion immunological test among 114 children of9-16 years cording to age the results were as follows: Cutusuma: in the same school of the community of Cullucachi.CA- 4/0 positive/negative in 1-4-year-old subjects (yos); 46/9 CERESVEGA (1989) did, moreover, a review on several in 5-9-yos; 30/9 in 10-14-yos; 11/4 in >15-yos; Tauca: aspects related to fascioliasis, such as the milieu, way of 0/0 in 1-4-yos; 2/9 in 5-9-yos; 9/32 in 10-14-yos; 2/18 in life of the human inhabitants, risk factors, water and plant > 15-yos.The diameter of the induration zone in the po- consumption, agropecuary customs, human defaecation sitive subjects was: Cutusuma: 7 subjects with 5-13 mm; habits, religious ethnic characteristics, clinics and patho- 9 with 13-21 mm; 14 with 21-29 mm; 21 with 29-37 logy, other concomitant parasites, nutritional status, and mm; 14 with 37-45 mm; 9 with 45-53 mm; 6 with 53-61 even control measure proposals (see below). mm; 3 with 61-69 mm; 7 with 69-77 mm; I with 77-85 From 1988 until 1993, a series studies were carried out mm; Tauca: 7 with 5-8 mm; 3 with 8-11 mm; I with I 1- thanks to the cooperation of specialists from the USA 14 mm; I with 14-17 mm; I with 80-83 mm. A 90,56% and Bolivian centres. These studies included coprologi- sensibility by comparison to coprology was estimated. cal and immunological surveys in the communities of CE TELLASGUEVARA(1987) applied the indirect im- Corapata, Calasaya and Santa Ana and furnished results munofluorescence test with an antigen obtained from pa- which were the object of several papers (BRYA et al., rasite adults from cattle and sheep. Very high positive 1989; McAuLEY, 1991; HILLYER et al., 1992; BJOR- results were obtained: in Cutusuma a total of 83 sera ap- LANDet al., 1992). peared to be reactive among 90 studied (92,2%) and in BRYAN et al. (1989) performed a study of community Tauca all sera proved to be reactive among a total of members aged 5-45 years in the village of Corapata: only 8 sera studied (100%). Compared with the results 26% gave positive results in stool samples, and 39% and obtained in coprological tests, the author finds a 94,3% 45% were positive in ELISA and IFA, respectively. Af- sensibility and a 100% specificity for his indirect immu- ter combining faecal and serologic results, the overall nofluorescence test. prevalence of human fascioliasis in Corapata was 40%. ESPANAVASQUEZ(1989) applied an ELISA test using Attempts were made to define risk factors for humans a soluble proteic antigen. This author studied a total of acquiring infection. Potential risk factors analysed were: 121 human sera from subjects aged 5 to more than 55 age, gender, diet, water source, animal contact, animal years (mainly 5-14 year-old children), from different lo- husbandry, fuel use/storage, zone of residence, and pre- calities: Cutusuma (97 sera), Chijipata Bajo (5), Chiji- valence of infection in household cattle herd. The con- pato Alto (6), Paitiri (7), Karapata (I), Esquiri (I), Ca- clusion was that fascioliasis is highly endemic in hu- chilaya (I), Oquetiti (I), and Wilajahuira (2). A total of mans in this community. Also, women over 23 years of 114 sera were positive among the 121 examined age appear to be at increased risk for fascioliasis.The (94,21 %), without significant differences according to possibility of geographic clustering was also noted. sex. Very high specificity (100%) and sensibility (96,66- McA ULEY(1991) and BJORLANDet al. (1992) refer to 97, 18%) were obtained by comparison with coprologi- an outbreak of acute fascioliasis in the community of cal, indirect immunofluorescence and intraderrnoreac- Calasaya, of approximately 500 persons, near Lake Titi- 80 S. MAs-CoMA et al. cacao Based on a random sample of the community (71 H[LL YER et al. (1992) applied two serologic techni- subjects of ages 1-81), 21 % shed eggs in faeces, 23% of ques, the Falcon assay screening test-enzyme-linked im- the persons developed acute fascioliasis during the late munosorbent assay (FAST-ELISA) and the enzyme-lin- rainy season (April-May) in 1991, and 49% had serolo- ked immunoelectrotransfer blot (EITB), to 100 serum gic evidence by ELISA of latent or chronic infection. samples, as well as the formol ether concentration tech- Interestingly, women appeared more likely than males nique and Kato-Katz technique to 73 stool samples from to have fascioliasis (38% vs. 20%). There was no evi- the same individuals (age range: 5-45; male/female ratio dence of geographic clustering. In a parallel study in the 1: I) from the community of Corapata. Fascioliasis pre- nearby village of Santa Ana, 66% of 32 persons eviden- valence results were: 20 positive among 73 stool sam- ced F. hepatica antibodies as measured by FAST- ples (27%); 531100 in FAST-ELISA (53%); 421100 in ELlSA (but unfortunately it was not a randomly-selec- FAST-ELlS A +EITB (42%). According to this study, ted population). immunological techniques demonstrate that coprological

Locality Age rank Total No. No. or % Method Observations Authors (years) studied positive

La Paz 20 ? PINILLA & PAZ (1939); PINILLA (1939) La Paz H. Gral. 2 clin. + surg. HARTMA N & PATI-O(1962) La Paz H. Obr. I 65 80% clin. + 20% surg. 1970-1985 FLoREs SER A & ESTEVEZ MARTII (1988) La Paz H.Clin. 9 80% clin. + 20% surg. 1970-1985 FLoREs SERNA & ESTEVEZ MARTINI (1988) La Paz I.G.B.J. 21 80% c1in. + 20% surg. 1980-1985 FLORES SER A & ESTEVEZ MARTII ( 1988) Achocalla 22 0,9% coprology NIAH s. t. LOZANO Mo ROY (1974) Cullucachi 4-20 151 72% coprology VERAZAIN(1982) Cullucachi schoolchildren 275 [3,5% coprology dir. smear + for.-eth. c. CACERES VEGA (1989) Cullucachi 9-16 114 71,9% serology compl. fixation test CACERES VEGA (1989) Kallutaca 1-18 90 47,7% coprology dir. smear with lugol ORTUBE GOITIA(1986) Cutusuma 1->60 183 52,0% coprology 9 different techniques Mo TERO BUSTILLOS(1987) Cutusuma 1->15 113 80,53% immunology IDR MOLlNA PADILLA(1987) Cutusuma 5->30 90 92,22% serology IFI CENTELLASGUEVARA(1987) Tauca 1->60 38 3,6% coprology 9 different techniques MONTERo BUSTILLOS(1987) Tauca 5->15 72 18,05% immunology IDR MOll A PADILLA(1987) Tauca 5->30 8 100% serology IFI CE TELLASGUEVARA (1987) Chijipata Alto (3-13) 2 diagnosed in La Paz 1986-1987 VELA PACHECO(1988) Chua (3-13) I diagnosed in La Paz 1986-1987 VELA PACHECO(1988) Batallas (3-13) 2 diagnosed in La Paz 1986-1987 VELA PACHECO(1988) Corapata 17 clinics VILLCA, CRUZ & ALCO ( 1989) Corapata 5-45 88 25% coprology in [ LASA VILLCA, CRUZ & ALCON (1989) Corapata 5-45 77 50,6% serology CIE; in Puerto Rico VILLCA, CRUZ & ALCON(1989) Corapata 5-45 80 57,5% serology IFI; in INLASA VILLCA, CRUZ & ALCON (1989) Corapata 5-45 26% coprology BRYANetal.(1989) Corapata 5-45 39% serology ELlSA BRYANetal.(1989) Corapata 5-45 45% serology IFA BRYANetal.(1989) Corapata 5-45 100 53% serology FAST-EllSA HILLYER et al.(1992) Corapata 5-45 100 42% serology FAST-ELlSA + EITB HILLYER et al. (1992) Corapata 5-45 73 27% coprology for.-eth. c. + Kato-Katz HILLYER et al. (1992) Calasaya 1-81 71 21% coprology BJORLANDet al. (1993) Calasaya 1-81 71 23% clinics April-May 1991 BJORLANDet al. (1993) Calasaya 1-81 71 49% serology ELlSA BJORLANDet at. (1993) Santa Ana 32 66% serology FAST-ELlSA BJORLANDet al. (1993) Alliplano* 5-55 121 94,21% serology ELlSA ESPANA VASQUEZ( 1989)

Table 1.- Prevalences recorded in human surveys according to localities of the Bolivian Northern Altiplano. l-i.Gral.e+lospital General de La Paz; H.Obr.1 =Hospital Obrero No.1 de la CNSS La Paz; H.Clin.=Hospital de Clfnicas La Paz; I.G.B.J.=lnstituto Gastroenterol6gico Boliviano Japones La Paz; *=results obtained in surveys made by ESPANA VASQUEZ (1989) are not included because the author did not specify prevalences according to localities; (3-13)=concrete age not specified for each patient; clin.eclinical diagnostics; surg.=surgical finding; NIAH s. t.esedirnentation technique after the ational Institute of Animal Health; dir. smear = direct smear; for.--eth. c =formol- ether concentration; 1D.=intradermoreaction; lFl eindirect immunofluorescence; CIE=counterimmunoelectrophoresis; IFA=immunofluorescent assay; FAST-ELlSA=Falcon assay screening test-enzyme-linked immunosorbent assay; El'TBeenzyrne-Iinked immunoelectrotransfer blot. Human fascioliasis in Bolivia 81

studies underestimate real prevalences. HILLYER et at. dren presented 3 or more crises of recurrent abdominal (1992) concluded, like MARTINEZet al. (1991), that in pain of varying intensity, 98% presented chronic diar- the Bolivian Altiplano around Lake Titicaca the levels of rhoea, 40% of the children positive at high dilutions in human infection by F. hepatica are the highest reported the complement fixation test presented jaundice which in the world so far. suggested massive infection inducing liver lesions and Results obtained in coprological and immunological obstruction, 15% of the children positive + doubtful in surveys on human fascioliasis carried out in the Bolivian the complement fixation test presented hepatomegalia, Altiplano and neighbouring valley and subvalleys of La and 30% presented skin alterations. Paz are summarized in Table 1. Because it was impossible to know the child mortality rate through death certificates, CACERESVEGA (1989) requested community authorities and school directors to Clinical and pathological observations furnish information on the number of children who had HARTMANN& PATINO(1962) reported two cases diag- died in the previous year. The information obtained was: nosed in a hospital of La Paz, one of which was an inte- 15 deaths among 20 newborns due to unidentified cau- resting extrahepatic case of subcutaneous epigastric pa- ses, and 8 deaths among children less than 5 years old rasite location. because of gastrointestinal problems. The author conclu- MONTEROBUSTILLOS(1987), in his studies in Cutu- ded that the zone of Cullucachi was impoverished, with suma and Tauca, detected a slight eosinophilia of 5-9% inhabitants in extreme indigence and with morbidity and and a moderate eosinophilia of 10-13% in 29,8% and mortality rates related to a deterioration of life condi- 16,4% of the subjects studied, respectively, among tions. These are the consequence of the limits marked by which 20,2% and 13,5% presented F. hepatica eggs in meager landed properties for agronomic practices intro- faeces. duced for rural families by the governmental Agrarian In the studies in Cutusuma and Tauca, no clear rela- Reformation. Owing to the high zoonosis endemicity, tionship with eosinophilia was observed by MOLlNAPA- meager landed properties lead to a low productivity and DlLLA(1987): among 60 subjects presenting a positive further to an infrasubsistence consumption level, which intradermoreaction test, 23 showed a normal eosinophi- is, moreover, related to a process of health-disease of lia (these subjects were considered to be in the parasite very peculiar characteristics derived from the local pro- adult stage phase) and 37 showed slight or moderate eo- duction and consumption manners. sinophilia (considered to be in the parasite adult stage According to MARTINEZet al. (1991), asymptomatic phase or in a reinfection phase). and oligosymptomatic clinical forms are dominant in the In Corapata, VILLCA, CRUZ & ALCON (1989) told of hyperendemic zone of the Altiplano. This contradiction the detection of tens of severe cases, several deaths and with clinical observations reported by other authors is hundreds with moderate disease. They report, moreover, probably due to confusion induced by other factors, such on 12 fatal cases and about 20 critical cases showing as malnutrition and infection by other parasites. signs and symptoms typical of the acute phase. They also mentioned patients presenting enlarged abdomen National control programmes and thorax, painful hepatomegalia, marked mucocutane- ous pallidity, and small scars in the epigastric region Fascioliasis in Bolivia represents not only a large re- and/or right hypochondrium because of exteriorization gional problem for the Aymara Indians of the Northern of migratory flukes. In all they diagnosed up to 17 sub- Altiplano, but a disease of real negative socio-economic jects by clinical observations. effects, owing to the high prevalences in human beings In Cullucachi, CACERES VEGA (1989) emphasized, and in domestic animals close to the city of La Paz and from the haematological point of view, that none of the up to the touristic zone of Lake Titicaca. This is offi- children studied presented hemoglobin levels under the cially recognized by the Bolivian government, as dedu- minimum limit, a fact unexpected owing to the high ced by the resolutions of the Health and related Minis- number of parasites and low nutritional status of the tries, which include fascioliasis in the list of the most children. He explained this fact because of both the exis- important zoonoses needing the development of national ting parasites not being haematophagous and the evident campaigns. compensation related to high altitude conditions. This In Bolivia, fascioliasis was listed as the first of the author observed, moreover, that 55,3% of the children three most important zoonoses (1.- Fascioliasis; 2.- Te- presented higher than normal eosinophilia, 25% of the niasis/Cisticercosis; 3.- Hidatidosis). The importance children even more than 500 eosinophils/ul. Of the im- of these zoonoses lead the Bolivian Ministry to create munologically positive children, 75% showed increased the «Cornite Tecnico de Vigilancia y Control de Zoo- eosinophilia and 63% of the doubtful cases presented an nosis» in 1989, to coordinate policies, strategies, pro- average of 700 eosinophils/ul. A 50% association be- grammes, and activities of public and private organisa- tween positive + doubtful cases and eosinophilia higher tions, in the fight against these parasitic diseases. This than 250 eosinophils/ul was detected (35% with positive Committee comprises the following institutions: a) Mi- cases). From the clinical point of view, 98% of the chi 1- nisterio de Previsi6n Social y Salud Publica: Direcci6n 82 S. MAS-COMA et at.

Nacional de Epidemiologia, Jefatura Nacional de Zoo- des and 6,070/0 by T. trichiura in 494 Bolivian subjects nosis, Direcci6n del Instituto Nacional de Laboratorios living at an altitude of 3300 m. de Salud (INLASA), Divisi6n de Parasitologia de IN- CACERESVEGA (1989), in a coprological survey (di- LASA, Direcci6n Nacional de Saneamiento Ambiental, rect smear, formol ether concentration) of 275 school- and Jefatura Nacional de Control de Alimentos y Bebi- children in Cullucachi, found the following prevalences: das; b) Ministerio de Asuntos Campesinos y Agropecua- 17,30/0 by Giardia intestinalis; 10,20/0 by Hymenolepis rios: Direcci6n General de Ganaderia, Direcci6n Nacio- nana; 5,50/0 by Taenia spp. (solium/saginata); 7,80/0 by nal de Salud Animal, and Direcci6n Nacional de Trichuris trichiura; 1,570/0by Strongyloides stercoralis; Recursos Naturales y Medio Ambiente. The Divisi6n de 42,50/0 by Ascaris lumbricoides; and 1,570/0 by Entero- Parasitologia of the INLASA Institute was considered as bius vermicularis. a National Reference Centre for the diagnosis of these Concerning fascioliasis, the most important conclu- diseases (Ministerial Resolution of 4th August 1989, Mi- sion is that there are several human parasitic diseases nisterio de Previsi6n Social y Salud Publica & Ministe- which are present in the same fascioliasis endemic areas. rio de Asuntos Campesinos y Agropecuarios, La Paz - This makes it difficult to separate symptomatology, pa- JUSTlNIA 0 & ARCE LEMA, 1989). thology, morbidity and mortality induced by fascioliasis from that caused by the other parasites or by different as- sociations of parasite species. Also to be taken into ac- Association with other parasite species count is the possibility of cross-reactions in serological ORTUBEGOITIA(1986) found, in a survey of 90 chil- tests, above all with other helminth species such as ces- dren in Kallutaca: 26 (28,90/0) infected by Entamoeba. todes (H. nana, Taenia spp., cysticercosis by Taenia so- coli; I (l,10/0)with E. histolytica; 2 (2,20/0) with Blas- hum) or nematodes (mainly A. lumbricoides). Studies on tocystis hominis; 4 (44,40/0) with Ascaris lumbricoides; 2 both aspects, parasitic diseases present and immunologi- (2,20/0)with Enterobius vermicularis; 2 (2,20/0) with Tri- cal diagnostic tests, are needed. churis trichiura; 7 (7,70/0) with Hymenolepis nana; 2 (2,20/0)with Taenia spp. (noted as Taenia ovis); I (1,1 0/0) Human contamination sources with Strongyloides stercoralis. HILLYER et at. (1992) found eggs of the following Several of the authors working on human fascioliasis species in 73 stool samples from Corapata: 260/0Trichu- have tried to obtain information on the possible ways of ris trichiura, 90/0Ascaris lumbricoides, and 60/0Taenia acquiring the infection in the Bolivian Altiplano. spp. VELA PACHECO(1988) already presupposed the oral VILLCA,CRUZ & ALCON(1989) noted the results ob- infection route when noting that humans, as well as do- tained in the study of 88 stool samples from 5-45 year- mestic animals of the Altiplano eat the so-called «cocha- old subjects in Corapata, studied in the INLASA Insti- yuyo» (= «layta» in Aymara language), the «chullu» tute: Entamoeba histolytica (28,40/0), E. coli (80,60/0), (= the sweet root of the typical totora plant) and the «osk- Endolimax nana (50,00/0), Chilomastix mesnili (9,1 0/0), hosco» (= the root of the smaller plants called totorilla). Iodamoeba buetschlii (27,20/0), Giardia intestinalis BRYAN et at. (1989) performed a complete study of (9,10/0), Taenia spp. (6,80/0), Hymenolepis nana (4,50/0), community members aged 5-45 years in the village of Trichuris trichiura (23,80/0), Strongyloides stercoralis Corapata and reached the conclusion that children who (2,20/0), undetermined ancylostomids (2,20/0), and Asca- eat «kjosco» (a popular aquatic plant) appear to be at in- ris lumbricoides (7,90/0). Only 4,50/0 of the subjects sho- creased risk for fascioliasis. Similarly, of the multiple wed no parasite, and in 15,90/0 of them only 1 parasite risk factors for infection that were evaluated in Calasaya species was detected. Poliparasitisms detected were: by BJORLAND et at. (1992), only consumption of 21,60/0 of the subjects with 2 parasite species, 22,70/0 «kjosco» while tending animals was associated with de- with 3, 26,10/0with 4, 6,80/0with 5, and 2,30/0with 6. velopment of acute fascioliasis. There is an anonymous report on the prevalences by MARTINEZet at. (1991) mentioned that in the zone Ascaris lumbricoides and Trichuris trichiura in the Alti- around Lake Titicaca an ecological niche is present planic communities of Compi, at Lake Titicaca (3809 m which appears to be favourable for both the parasite and altitude), and San Miguel, near Oruro (4114 m altitude) the vegetables involved in the transmission to human (ANON, 1965). Prevalences of 17,60/0 and 14,90/0 in beings: water-cress (Nasturtium officinale), totora Compi and of 14,30/0 and 14,30/0 in San Miguel, by A. (Schoenoplectus tatora), cochayuyo (Ulva purpurea), lumbricoides and T. trichiura respectively, were found. totorilla, etc., known by the rural inhabitants as «oko- In this report, no conclusions were reached when trying roro», «chullu» (a bulbose root) and «sakha» (the stem), to relate the results with the nutritional status of the sub- «llayta» and «oskhosco», respectively. jects analysed by height, weight, hemoglobin and hema- The reports suggest that human infection is related to tocrit, for reasons linked to subject race and the high alti- traditional consumption of uncooked aquatic plants: to- tude of the milieu.Another study on human ascariasis tora = «chullu»: Schoenoplectus californicus ssp. tatora and trichuriasis at altitude was that of ELFO-CALvo et at. (Cyperaceae); matara: Juncus andicola (Juncaceae); to- (1976), who found prevalences of 8,1 % by A. lumbricoi- torilla = «kosko-oskosko»: Juncus ebracteatus (Junca- Human fascioliasis in Bolivia 83 ceae); watercress = berros = «okororo»: Mimulus gla- long bones. This delayed height appears after a prolon- bratus and Nasturtium officinale (Scrophulariaceae); ged duration of this deficit, and is increased by health brow algae = cochaguyo = «llayta»: Nostoc sp. (Cianofi- factors such as high risk endemic parasitoses involving tas); and many others still to be determined. Unfortuna- pathologies which diminish the growth and development tely, there is no systematic and descriptive paper dealing capacities of children. In Cullucachi, 57,3% of the chil- with fresh-water aquatic plants in the Bolivian orthern dren lacking height were infected by parasites, and Altiplano, so an appropriate determination of plant spe- 35,2% also presented a weight deficit. Differences in re- cies involved in transmission is very difficult at present. lation to normal values appeared to be very small in the Moreover, a confusion in the Aymara terms can also be first school years, but rose to levels markedly under the observed (spelling of Aymara words in the present re- minimum values after the age of 6, both for height and view article maintains the exact orthography used in the weight. It is worth mentioning that CACERES VEGA papers reviewed; note the different spellings used by dif- (1989) detected a 90% association of fascioliasis preva- ferent authors for the same Aymara word). Only the pa- lence with malnutrition patterns in schoolchildren. On per by FRANKEN (1991) eo veri ng the flora of aquatic the whole, the author concluded that socio-economic plants in the neighbouring valley of La Paz offers valua- conditions had markedly deteriorated in recent years ble information on the botanic aspect. It is evident that causing an increase of acutely under-nourished children appropriate studies on fascioliasis-transmitting aquatic in the rural area, to such an extent that only 2,3% of the plants are needed. children showed development and growth within normal Whereas the above-mentioned authors only refer to values. possibly transmitting plants, CACERES VEGA (1989) is the only author to note the feasibility of drinking water Human habits, ethnic customs and religious aspects as an infection route. In his studies, carried out in the community of Cullucachi, this author noted the impor- The relationships of fascioliasis with several of these tant role of water in the genesis of the local epidemiolo- aspects have been analysed by a few authors. The Nort- gic pattern, by participating in the transmission of disea- hern Bolivian Altiplano endemic zone is mainly inhabi- ses. All children surveyed consumed previously ted by Aymara natives. The poverty and bad health con- untreated water from a well and a canal shared with ani- ditions of the inhabitants of the fascioliasis endemic mals. Both well and canal are in places where humans zone explain some characteristics, such as the rudimen- and animals eliminated biological residua, thus causing tary home, the consumption of aquatic plants and of non- their contamination. Food, mainly local vegetables, is potable water, outdoor defaecation habits, and inappro- washed with contaminated water, increasing the risk of priate livestock breeding systems. acquiring an illness and dying from a parasitic, bacterial CACERES VEGA (1989) reported that though all the in- or viral disease. According to this author, fascioliasis habitants of Cullucachi had their own house, these hou- may be acquired by drinking contaminated water instead ses presented very bad living conditions: roofs made of of eating water-cress and other aquatic plants, since the straw or calamine, walls of adobe or sun dried bricks, inhabitants do not usually eat these plants. and only one room in 75% of the houses, with an ave- The possibility of infection by drinking contaminated rage of 5 family members living in absolute promis- water implies that the Altiplanic strain of F. hepatica is cuousness, with small animals such as chicken, dogs, able to produce free (= not attached to plants or any other cats and rabbits. Although electric power was available object present in water), floating metacercarial cysts. in Cullucachi, the majority of houses were not connec- Although this capacity is already known in several Euro- ted. Most inhabitants own only a few small pieces of pean strains of this parasite, it has yet to be demonstrated land or even ruts, which has given rise to a dangerous in the Altiplanic strain of F. hepatica. man-animal accumulation, causing unhealthy risk conditions which generate disease and death. VILLCA, CRUZ & ALCO (1989) emphasized that die- Nutritional status tary habits and customs of the Altiplanic inhabitants ap- While carrying out his studies on human fascioliasis in pear to be related to F. hepatica infection in humans. Ac- the community of Cullucachi, CACERES VEGA (1989) cording to these authors, almost everybody above all, undertook an interesting analysis of the nutritional status children living in endemic zones has tried the sweet totora of the schoolchildren surveyed (275 children, 5-15 years root and the so-called «ghosco-ghosco». The so-called old). According to the results of this author, only 40% of «ghocha-yuyos», water-cress and other aquatic plants, are the children anthropometrically analysed (weight and eaten but not as much. These authors also noted the abso- height) were found to be in the normal range and 37,5% lute lack of potable water and the inappropriate stool ma- showed acute malnutrition, appearing to be under the nagement, which gives rise to a general consumption of minimum allowable level. The highest nutritional pro- water shared by humans and animals from a single water blem seemed to be chronic malnutrition, shown by a de- source contaminated with faecal stools. lay in growth, as the consequence of a protein and CACERES VEGA (1989) and MARTI EZ et al. (1991) energy deficit affecting the longitudinal growth of the also emphasized the importance of outdoor defaecation 84 S. MAS-COMA et at. habits of the inhabitants of the endemic zones, a habit but it represents a rnythic, symbolic horizon from which which appears to be the rule in rural areas of Bolivia. a series of conducts and interpretations of this process CACERESVEGA (1989) added that 95% of the children arise. Concerning fascioliasis, there is no conscious rela- he surveyed defaecate outdoors and only 5% use latri- tionship between cause and effect. Parasitoses and other nes. Many of these latrines are located near canals and internal diseases without specific location are usually wells. The latrines are, moreover, unclean, thus constitu- considered as a punishment or a retaliation of the «de- ting infection foci. miurgos», that is, a «Pachamarnan jasuti pachawa» Obviously, all the above-mentioned authors were thin- (=punishment by the Pacharnama). A fatalistic guilt fee- king of the importance of F. hepatica eggs shed in stools ling appears when faced with the possibility of death, its by humans and the consequent rniracidial infection of existence not being questioned because of its divine and lyrnnaeids inhabiting water collections present in the zo- immutable character. The repairing rite of agents like the nes used by humans for defaecation. However, it must «coli iris» or the «yatiris» is intended to purify and re- be noted here that the transmission capacity of human- verse such fatality. In a given manner, this could explain shed eggs has never been demonstrated in F. hepatica up that diarrhoea processes or macroscopic parasite elimi- to the present. Appropriate research on this aspect is nee- nation are considered as completely normal in the exis- ded to know if human beings also play a role in the ting routine of the rural inhabitant. The relationship bet- transmission of the liver fluke in the Bolivian Altiplano. ween bad hygiene and lack of food or man-animal The relationship of inappropriate agronomic practices cohabitation with human disease is unknown. According with fascioliasis was analysed by CACERES VEGA to CACERESVEGA (1989), it can be concluded that there (1989). In Bolivia, the appearance of the poor and indi- is a total lack of knowledge on the biological phenome- gent small land holder is one of the most important non and the causes of fascioliasis and other parasitic di- transformations in recent years. This regimen of meager seases. landed properties affects 100% of the Bolivian population involved in agricultural practice and covers less Treatment than 70% of their food needs.These rural people pro- gressively lose their agronomic work vocation, mainly Different antifascioliasic drugs have been used in the because of a decrease in their land. Their poverty beco- Bolivian Altiplano for human treatment. mes more pronounced owing to the man-animal stacking HARTMANN& PATI- 0 (1962) treated one case of sub- as a direct consequence of this space restriction, which cutaneous parasite location with emetine (0,04 g during in turn appears to be related with the diseases transmit- 2 weeks) and another normal case of liver location surgi- ted from animals to man, as in the case of fascioliasis. cally. VELAPACHECO(1988) applied dehydroernetine (I Finally, the absence of pasturing zones and the difficulty rug/kg/day during 10 days) to 5 cases and praziquantel in crop rotation lead to the contamination of pastures and (30 mg/kg/day in 2 doses during 8-10 days) to 2 cases in forage, causing important alterations in the ecological 3-13 year-old children; six of these cases improved their environment, including true endernics of zoonoses, health condition but one child of 10 died. above all fascioliasis. As part of a large study carried out by the I LASA According to CACERESVEGA (1989), ORTUBEGOITIA Institute in Cutusurna from November 4-9, 1986, inclu- (1986) and MARTINEZet al. (1991), in the endemic zone ding 223 intradermic reactions, 198 hernoglobin deter- a family has approximately 1-2 cattle, sheep, pigs, and 4- rninations, 198 blood smears, 100 serum samples, 200 5 birds, although meat, milk and wool production is low. stool samples and 200 clinical histories, treatment was According to official data, the estimated animal popula- applied from December 16-19, 1986, to subjects having tion includes 6 sheep and 3,4 cattle per family, which shown a positive result in coprology or intraderrnoreac- means:A) sheep: Ingavi 93474, Los Andes 73950, Orna- tion.A total of 31 subjects were treated with praziquan- suyos 88098; B) cattle: Ingavi 52969, Los Andes 41905, tel at a dose rate of 20 mg/kg weight each 24 h during 2 Omasuyos 49922 (I E, 1992). Livestock is nourished days and 49 other subjects with triclabendazole at a dose with cultivated forages (oats, barley, alfalfa), aquatic rate of 12 mg/kg weight in a single dose (ANGLES, 1986 plants from Lake Titicaca and from the «bofedales» (to- b; STRAUSSet al., 1986). Results obtained briefly descri- tora, algae) and pasture in native lands. The pasture sys- bed by MONTEROBUSTILLOS(1987). Mebendazole, pra- tem differs according to zones: in Omasuyos province ziquantel and triclabendazole were applied in Cutusurna, and part of Los Andes province, pasturing is controlled as well as in Tauca (MOTEROBUSTILLOS,1987). After (the animal is fastened in the pasturing place), whereas 24 h postreatrnent with mebendazole no changes were in Ingavi province and part of Los Andes province pas- detected in the number of eggs shed, but after 24 h pos- turing is free or mixed (pasturing groups are composed treatment with praziquantel and triclabendazole an incre- of cattle, sheep and other species). ase of the egg number was observed. CACERESVEGA(1989) is the only author who empha- VILLCA, CRUZ & ALCON (1989) mentioned that peo- sizes the ignorance of Ayrnaras concerning biological ple medicate themselves with products for veterinary use risk. Among Ayrnaras, the so-called «usu» constitutes (Valvasen®, Fasinex's'), pure alcohol and others (pro- not only a conception of illness or health, of life or death, ducts not specified) in Corapata and that such self-rnedi- Human fascioliasis in Bolivia 85

cation is generally carried out in all communities where classified as L. viatrix were characterized by the follo- F. hepatica is present. According to these authors, self- wing characteristics: general shape: elongate; shell treatment had not apparently been effective, since only a length 10,0-11,0 mm; shell width: 5,0-6,5 mm; aperture temporary improvement was obtained. VILLCA,CRUZ & length: 5,2-5,4 mm; aperture width: 3,2-3,5 mm; number ALCON (1989) treated 17 clinically diagnosed subjects, of whorls: always 6; spire large; tumidity of whorls mar- 11 with dehydroernetine, 3 with emetine, and 3 others kedly well developed; peristome: smooth.The speci- with bithionol. Moreover, 34 subjects diagnosed copro- mens these authors determined as L. cubensis var. were logically and/or immunologically were treated with bi- characterized as follows: general shape: elongate or thionol at doses of 40 mg/kg weight/day on alternate ovate; shell length 8,0-9,5 mm; shell width: 5,0-5,5 mm; days. The percentage of abandonment of the treatment aperture length: 4,7-5,0 mm; aperture width: 3,3-3,8 was 14,3% for dehydroemetine and 0% for bithionol. mm; number of whorls: 5-6, the majority with 5; spire Adverse effects were detected in the treatment with both middle-sized; tumidity of whorls well developed; peris- products, but were slightly larger in dehydroemetine tome: smooth. (14,3%) than in bithionol (8,8%). Clinical improvement There is only one more morpho-systematic paper on was observed in 78,6% of the subjects treated with dehy- Iymnaeids of the Bolivian Altiplano. In a review paper, droemetine and in 100% of those treated with bithionol. LOBATOPARAENSE(1982) summarized the geographical Death took place in only 1 case (a severely ill 7-year-old distribution of L. viatrix in South America, including a girl died on the third day of treatment) among the sub- record of this lymnaeid species in the locality of Guaqui, jects treated with dehydroemetine (7, I %) and in none at the southern coast of Lake Titicaca. It is worth men- among those treated with bithionol (0%). tioning that this author did not discuss nor mention the A treatment study was undertaken by ANGLES(1990) previous findings of L. viatrix and L. cub ens is var. in the in Corapata. On one side, subjects previously treated Bolivian Altiplano by UENO et al. (1975). Interestingly, with Amebin® or Fasinex® were serologically analysed the Brazilian malacologist LOBATO PARAENSE(1982) with an ELISA test. Several patients showed high anti- added that L. cubensis cannot be anatomically differen- body levels, which was interpreted as the consequence tiated from L. viatrix. of subjects having continued eating infected plants, of an incomplete treatment or of varying effects of the drug Geography, ecology and population dynamics for different individuals. On the other side, 53 subjects were treated with bithionol. Studies showed that bithio- The presence of lymnaeid snails in the Bolivian Nor- nol was well tolerated at the conditions of altitude, nutri- thern Altiplano was first mentioned by MORALESLAVA- tion and dose used (25-50 mg/kg/day during 14 days), DENZ(1973). As a result of the research studies carried although in certain patients a kidney injury appeared out together with UENO and coworkers, this author des- (abnormal creatinine values without having received any cribed the finding of L. viatrix in Chirapaca (25% infec- previous treatment). Only 2 among 65 patients showed ted with rediaea and cercariae of F. hepatica) and Acho- F. hepatica eggs in stools. Additional selective treat- call a (5,8-24% infected according to the season), of L ments for Giardia intestinalis and Entamoeba histolytica cubensis in Chirapaca (0% infected), Belen (15,2% in- are finally recommended (ANGLES, 1990). fected) and Achocalla (4% infected), and of Lymnaea Self-treatment with triclabendazole for veterinary use spp. in Chirapaca (0% infected) and Belen (0% infec- (Pasinex'P), apparently with a good tolerance, by inhabited). However, infected snails were distinguished by tants in the fascioliasis endemic region of the Bolivian rupture and organ separation for larval stage search, Northern Altiplano has also been noted by MARTINEZet which means that no experimental infection of labora- al. (1991). tory mammals for species verification was undertaken and opens the possibility of confusion with other digenean species presenting morphologically similar larval THE MOLLUSCAN INTERMEDIATE HOST stages, such as bird notocotylids and echinostomes. According to UENO et al. (1975), L. viatrix is distribu- Despite the importance of the molluscan intermediate ted mainly in canals and shallow swamps in valleys of host in the life cycle of F. hepatica, as well as in the Achocalla province, whereas L. cubensis var. generally transmission and epidemiology of fascioliasis, only a inhabits low, humid areas, although the distribution of few authors have undertaken research activities on the both overlaps in the higher, cooler and drier plateaux of snails transmitting fascioliasis in the Bolivian Altiplano. Belen, Batallas and Chirapaca. Finally, MARTINEZet al. (1991) noted the presence of both species, L. viatrix and L. cubensis, in the so-called Species determination «bofedales», swampy zones distributed throughout the Two species of lymnaeid snails were collected by endemic region, but without any geographic detail. UENO et al. (1975) as present in fluke-infected areas of Thus, no appropriate study has been carried out so far the Northern Bolivian Altiplano: Lymnaea viatrix and on the Bolivian Altiplano snail strains, their vector capa- Lymnaea cubensis var. The Altiplanic Iymnaeids they city, biology, population dynamics, ecology and trans- 86 S. MAS-COMA et al. mission. The adaptation of these Lymnaea species to sur- Sheep: MORALESLAVADENZ(1973) carried out a copro- vive in the Bolivian Altiplano, at an altitude of 3800- logical survey in 6-month to 1-year-old sheep in the zo- 4100 m, where yearly seasonal differences are not mar- nes of Chirapaca, Belen and Viacha. Prevalences detec- ked and where diurnal/nocturnal thermic differences are ted with the N.I.AH. sedimentation technique were: very pronounced (night temperatures being extreme), Chirapaca 78,2% infected from 56 animals studied; Be- poses a series of very interesting questions concerning len: 66,6% of 90 animals (Corriedale and Targee races); all these aspects. Viacha: 68,6% of 265 animals (Corriedale and Targee races). Fascioliasis intensity in sheep was studied in 5 g stool samples with the so-called Dermis technique (see Snail control measures DENNIS, STO E & SWANSON,1954); averages of 1203, Several authors have referred to wild anatid birds as 13,2 and 4,5 eggs were found in animals with high natural biological control agents of Iymnaeid snails (n=25), moderate (n=4) and low (n=9) infection, respecti- transmitting fascioliasis in the Altiplano, taking into ac- vely. High intensity of infection was also found in all the count the duck populations linked to Lake Titicaca and necropsies of 10 livers from sheep of Viacha and Belen. its surrounding zones. VILLCA, CRUZ & ALCON (1989) By means of the N.I.A.H. sedimentation technique ap- mentioned ecological changes giving rise to the decrease plied to 5 g stool samples, LozANO MONROY(1974) de- of duck populations in recent years as a cause of the in- tected the following prevalences in sheep, according to crease of fascioliasis. CACERESVEGA (1989) proposed localities: A) Omasuyos Prov.: Belen 62,5% (5 infected the use of snail-predator wild ducks for the biological of 8 studied); Pajchani 100% (5 of 5); Huarina - Cota control of Iymnaeids. FRANKEN& PINTO(1989), in a Cota Alta 100% (13 of 13); Chirapaca 100% (7 of 7); B) project proposal on the ecology and biological control of Ingavi Prov.: Guaqui 0% (0 of 6); San Antonio 0% (0 of F. hepatica in the bordering zones of Lake Titicaca, 6): Patorani 0% (0 of 5); Achuta 0% (0 of 5); Tihuanaco emphasized the need for a study on wild anatid predators 0% (0 of 5); C) Los Andes Prov.: Kallutaca 88,9% (8 of of aquatic snails, for a study on other invertebrates anta- 9); Takachira 0% (0 of 5); Pillapi 0% (0 of 3); San Juan gonistic of lymnaeids, and the need to make the carto- Rosario 0% (0 of 5); Tambillo 0% (0 of 9). graphy of the «bofedales» (presumed to be the transmis- Also using the sedimentation technique, UENO et al. sion foci) in the endemic region. (1975) obtained the following prevalences in sheep: A) The ineffectiveness of the use of molluscicides like Achocalla (animals not treated): 78,4% infected of 125 copper sulfate, sodium pentachlorofenate and N-tritil- animals studied; B) Belen (animals treated with fascioli- morfolene for control measures has been noted by CACE- cides once or twice a year): 66,7% of 90; C) Chirapaca RESVEGA(1989) and MARTINEZet al. (1991). (not treated): 78,3% of 46; D) Viacha (treated with fasciolicides once or twice a year): 88,3% of 179. STUNDELL& MOLLlNEOO(1978) and MARTI EZet al. THE DOMESTIC ANIMAL RESERVOIRS (1991) reported an outbreak of fascioliasis in sheep in Chojasivi related to a decrease of local wild duck popu- According to official data, in the whole Bolivian Alti- lation which prey on aquatic snails, thus acting as biolo- pIano there are the following number of livestock popu- gical control agents of the intermediate hosts. lations: 5346953 sheep, 483859 cattle, 352984 pigs, VILLCA,CRUZ & ALCON(1989) obtained a 14,54% F. 1429140 llamas, and 149680 alpacas (MACA, 1988). In hepatica prevalence in 220 sheep analysed in their eo- the fascioliasis endemic region of the Bolivian Northern prological study in Corapata. Altiplano, the main domestic animals are sheep, cattle, Immunological studies in Altiplanic sheep have only pigs, camelids and rabbits (CACERESVEGA, 1989; MAR- been performed by HILLYER et al. (1993). Seropreva- TINEZet al., 1991). Curiously, no mention is made of lence studies of fascioliasis by FAST-ELlSA in sheep horses and donkeys, numerous in the endemic region, (29 herds totaling 184 sheep) in 1988 in the same area of domestic guinea pigs, relatively frequent in houses of gi- Corapata in which seroprevalence studies in humans had ven zones, and goats, very rare in the region but also pre- been done before, showed 89% positive in sheep. In pa- sent, despite their well-known role as potential definitive rallel faecal studies, eggs were only found in 22 of the hosts of F. hepatica (see review by BORAY, 1982). 184 sheep (12%), while 163 were positive by serology (sensitivity 100%). Coprological and immunological surveys Cattle:The first paper dealing with fascioliasis in cattle Several surveys have been carried out on fascioliasis from the Bolivian orthern Altiplano was that of ARA - of livestock species in the Northern Altiplano endemic OIA(1972).This author obtained, by coprological tech- region. Most of the studies were coprological surveys, niques, 36,4% positive (28 infected of 77 bovines stu- but a few serological research studies have been underta- died) and 63,4% positive (19 of 30) in Belen and ken in recent years. Only sheep, cattle and alpacas were Chirapaca, respectively. involved in the surveys. Summarized results for sheep MORALESLAVAOENZ(1973) carried out a coprological and cattle are shown in Fig. 2 and 3. survey in I to 2-year-old cattle in the zones of Achocalla, Human fascioliasis in Bolivia 87

Locality Total o. % Method Observations Authors studied positive

Chirapaca 56 78,2 NIAH s. t. < I year-old MORALESLAVADENZ (1973) Chirapaca 7 100 IAH s. L LOZANO Mo ROY(1974) Chirapaca 46 78,3 lAH s. t. not treated UE 0 et al. (1975) Belen 90 66,6 lAH s. L < I year-old MORALESLAVADENZ (1973) Belen 8 62,5 IAH s. t. LOZA 0 Mo ROY(1974) Belen 90 66,7 lAH s. t. treated UENOet al. (1975) Viacha 265 68,6 IAH s. t. < I year-old MORALESLAVADEZ (1973) Viacha 179 88,3 IAH s. t. treated UE 0 et al. (1975) Pajchani 5 100 lAH s. t. LOZANO MONROY(1974) Huarina - Cota Cota Alta 13 100 IAH s. L LOZA 0 MONROY(1974) Guaqui 6 0 IAH s. t. LOZA 0 MONROY(1974) San Antonio 6 0 NIAH s. t. LOZANO MONROY (1974) Patorani 5 0 NIAH s. t. LOZANO MONROY(1974) Achuta 5 0 NIAH s. t. LOZANO MONROY (1974) Tihuanaco 5 0 NIAH s. t. LOZANO MONROY (1974) Kallutaca 9 88,9 NIAH s. t. LOZANO MONROY (1974) Takachira 5 0 NIAH s. t. LOZANO MONROY(1974) Pillapi 3 0 NIAH s. t. LOZANO MONROY(1974) San Juan Rosario 5 0 NIAH s. t. LOZANO MONROY(1974) Tambillo 9 0 NIAH s. t. LOZANO MONROY(1974) Achocalla 125 78,4 NIAH s. t. not treated UENO et at. (1975) Corapata 220 14,54 coprology VILLCA, CRUZ & ALCON (1989) Corapata 184 89 FAST-ELlSA HILLYER et al. (1993) Corapata 184 12 coprology HILLYER et al (1993

Table 2.- Prevalences recorded in sheep surveys according to localities of the Bolivian Northern Altiplano. NIAH s. r.esedirnentaticn technique after the ational Institute of Animal Health; coprologyecoprological technique not specified; treated / not treated=animals treated/not treated previously during the same year of the survey; < I year old=animals aged less than I year.

Chirapaca, Belen and Viacha. Prevalences detected with 63,3% of 30; C) Viacha (animals treated with fasciolici- the N.I.AH. sedimentation technique were: Achocalla: des once or twice a year): 100% of 10. As can be seen, 78,4% infected from 125 animals studied (the majority these are part of the results obtained by MORALESLAVA- belonging to Holstein and mixed Holstein-Creole races); DENZ(1973) (see above). Chirapaca: 63,3% of 30 animals (all Creole race); Belen: SALAZAR ESCOBAR (1979) carried out coprological 36,3% of 77 animals (the majority Swiss brown and seve- surveys with the N.I.A.H. sedimentation technique of ral Creole); Viacha: 100% of 10 animals.Fascioliasis in- bovines older than 1 year from the urban and suburban tensity in cattle was studied in 5 g stool samples with areas of the Department of La Paz. Studied areas were Dermis technique; averages of 74,8, lA and 3,5 eggs were La Paz city (urban area and marginal suburbs including found in animals with high (n = 14), moderate (n = 5) and bound animals), El Alto (Northern Altiplano plain; pas- low (n = 13) infection, respectively. ture grounds for animals during the breeding season and A year later, LOZANO MONROY (1974) undertook a surrounding places), Achocalla (small valley), Palca coprological study with the N.l.A.H. sedimentation tech- (small hills and small streams) and Rio Abajo (strait va- nique on 5 g stool samples from cattle, obtaining the fo- lley furrowed by the Choqueyapu river which crosses llowing prevalences: A) Omasuyos Prov.: Belen 85% the city of La Paz). The total cattle population of all this (17 infected of 20 animals studied); Pajchani 0% (0 of zone was estimated to be 7488 animals, of which 700 5); Batallas 100% (22 of 22); Chirapaca 84,6% (11 of were surveyed. The coprological study of 5 g stool sam- 13); B) Ingavi Prov.: Guaqui 0% (0 of 6); San Antonio ples showed a total prevalence of 40,57% infected with 0% (0 of 1):Patorani 0% (0 of 3); Achuta 0% (0 of I); F. hepatica during the July-October period of 1977. De- Tihuanaco 0% (0 of 5); C) Los Andes Prov.: Kallutaca tailed results were: 35,92% infected of 206 bovines stu- 0% (0 of 8); Takachira 40% (4 of 10); Pillapi 0% (0 of died in the city of La Paz; 34,90% of 106 studied in El 8); San Juan Rosario 0% (0 of 23); Tambillo 12% (2 of Alto; 36,87% of 160 studied in Achocalla; 59,77% of 18); Sullkataka 0% (0 of 7); Collantaka 66,7% (4 of 6). 174 studied in Palca; 18,51 % of 54 studied in Rio Abajo. UE 0 et al. (1975) also studied stool samples from The animals presenting higher prevalences were the cattle by the sedimentation method. The prevalence re- group of 4-5-year-old bovines (43,95%) and the less in- sults they obtained were: A) Belen (bovines treated with fected were the 1-3-year old ones (36,73%). No signifi- fasciolicides once or twice a year): 36,4% infected of 77 cant differences were observed between males and fema- bovines studied; B) Chirapaca (animals not treated): les, nor between races (Holstein, cross-breed, Creole). 88 S. MAS-COMA et al.

Locality Total o. % Method Observations Authors studied positive

Belen 77 36,4 coprology ARANDIA(1972) Belen 77 36,3 NIAH s. t. 1-2 year-old MORALESLAVADENZ(1973) Belen 20 85 NIAH s. t. LOZANOMONROY(1974) Belen 77 36,4 NIAH s. t. treated UENO et at. (1975) Chirapaca 30 63,4 coprology ARANDIA(1972) Chirapaca 30 63,3 NIAH s. t. 1-2 year-old MORALESLAVADENZ(1973) Chirapaca 13 84,6 NIAH s. t. LOZANOMONROY(1974) Chirapaca 30 63,3 NIAH s. t. not treated UE 0 et at. (1975) Achocalla 125 78,4 IAH s. t. 1-2 year-old MORALESLAVADENZ(1973) Achocalla 160 36,87 NIAH s. t. > I year-old SALAZARESCOBAR(1979) Viacha 10 100 NIAH s. t. 1-2 year-old MORALESLAVADEZ(1973) Viacha 10 100 NLAHs. t. treated UE 0 et al. (1975) Pajchani 5 0 NLAH s. t. LOZANOMo ROY(1974) Batallas 22 100 NIAH s. t. LOZANOMONROY(1974) Guaqui 6 0 NIAH s. t. LOZANOMONROY(1974) San Antonio I 0 NIAH s. t. LOZANOMONROY(1974) Patorani 3 0 NIAH s. t. LOZANOMONROY(1974) Achuta I 0 NIAH s. t. LOZANOMONROY(1974) Tihuanaco 5 0 NIAHs. t. LOZANOMONROY(1974) Kallutaca 8 0 NIAH s. t. LOZANOMo ROY(1974) Kallutaca 90 54,45 NIAH s. t. ORTUBEGOITIA(1986) Kallutaca area 296 74,68 NIAH s. t. ORTUBEGOITIA(1986) Takachira 10 40 IAH s. t. LOZA 0 MONROY(1974) Pillapi 8 0 IAH s. t. LOZA 0 MONROY(1974) San Juan Rosario 23 0 NIAH s. t. LOZANOMONROY(1974) Tambillo 18 12 NIAH s. t. LOZANOMONROY(1974) Sullkataka 7 0 NIAH s. t. LOZANOMONROY(1974) Collantaka 6 66,7 NIAH s. t. LOZANOMONROY(1974) La Paz city 206 35,92 NIAH s. t. > I year-old SALAZARESCOBAR(1979) El Alto 106 34,90 NIAH s. t. > I year-old SALAZARESCOBAR(1979) Palca 174 59,77 NIAH s. t. > 1 year-old SALAZARESCOBAR(1979) Rio Abajo 54 18,51 NIAH s. t. > I year-old SALAZARESCOBAR(1979) La Paz slaughterhouse 944 65,7 necropsy from Altiplano/l975 FLORES& ESTEVEZ(1988) La Paz slaughterhouse 1481 63,2 necropsy from Altiplano/l976 FLORES& ESTEVEZ(1988) La Paz slaughterhouse 1881 68,7 necropsy from Altiplano/l977 FLORES& ESTEVEZ(1988) La Paz slaughterhouse 1729 67,7 necropsy from Altiplano/l978 FLORES& ESTEVEZ(1988) La Paz slaughterhouse 1833 69,1 necropsy from Altiplano/l979 FLORES& ESTEVEZ(1988) Corapata 327 28,13 coprology VILLCA,CRUZ & ALCO (1989) Corapata 60 ELlSA + IFA BRYANet at. (1989) Corapata 299 58 FAST-ELlSA in 1988 HILLYERet at. (1993) Corapata 147 57 FAST-ELlSA in 1989 HILLYERet at. (1993) Corapata 147 26 coprology in 1989 HILLYERet at. (1993)

Table 3.- Prevalences recorded in cattle surveys according to localities of the Bolivian Northern Altiplano. NIAH s. t.=sedimentation technique after the National Institute of Animal Health; IFA=immunofluorescent assay; FAST-ELlSA=Falcon assay screening test- enzyme-linked immunosorbent assay; year-oldeage of animals studied; treated/not treatedeanirnals treated/not treated previously during the same year of the survey; from Altiplano=animals analysed from the Altiplano.

ORTUBE GOITIA (1986), using the same N.I.A.H. se- mild, 55 with moderate and 15J with severe infection. dimentation technique in Kallutaca, studied not only FLORES SERNA & ESTEVEZ MARTINI (1988) carried prevalences but also intensities (1-10 eggs found: mild out a survey on cattle from the Altiplano and sacrificed infection; 10-20 eggs: moderate infection; 30 or more in the municipal slaughterhouse of La Paz, located in the eggs: severe infection). On the Kallutaca farm the re- Achachicala zone. F. hepatica was found in: 65,7% of sults were: 49 infected among 90 animals studied 944 bovines in the year 1975; 63,2% of 1481 in 1976; (54,45%), including 2 with mild, 7 with moderate and 68,7% of 1881 in 1977; 67,7% of 1729 in 1978; and 40 with severe infection. In the influence area of the 69, I% of 1833 in 1979. The summarized result was farm, a total of 221 animals were found infected among 67,17% of 7868 in the five-year period 1975-1979. Ac- 296 bovines surveyed (74,68%), including 15 with cording to these results, the authors concluded that pre- Human fascioliasis in Bolivia 89 valences are high and maintained through time. It is According to UENO et at. (1975) and MART! EZet al. worth mentioning that no bovine from the Bolivian re- (1991), the mortality rate by F. hepatica in sheep is esti- gion of Alto Beni presented fascioliasis. mated to be not less than 15-25% annually. According to VILLCA,CRUZ & ALCON(1989) obtained a 28,13% F. UENO et al. (1975), a heavy loss in animal production is hepatica prevalence in 327 cattle analysed in their eo- inflicted. prological study in Corapata. A study on the influence of F. hepatica infection on Immunological studies have been performed by BRYAN milk production by cattle in the Kallutaca farm was et at. (1989) and HILLYERet at. (1993). A bovine serosur- made by ORTUBE GOITIA(1986). This author showed vey carried out by BRYANet at. (1989) in the village of that in January fascioliasis decreases to a 10% preva- Corapata yielded 60% positive with ELISA and IFA (im- lence and milk production increases up to 6500 I, whe- munofluorescent assay). reas in August the opposite takes place, with highest le- HILLYER et at. (1993) developed seroprevalence stu- vels on infection leading to a decrease of milk dies of fascioliasis by FAST-ELISA in cattle (41 herds production to 4400 I, which represents a milk decrease totaling 299 cattle in 1988; 34 herds totaling 147 animals of68,75%. sampled in 1989) in the same area of Corapata in which VILLCA, CRUZ & ALCON (1989) mentioned that ani- seroprevalence studies in humans had been done before. mals were affected to a very high level owing to the inju- Results obtained were 58% positive in 1988 and 57% ries caused, including even an almost total extermination positive in 1989. According to faecal studies, eggs were of sheep. According to the authors, ten years ago rural found in 38 of 147 cattle (26%), while 84 were serologi- families could have up to 200 and 250 sheep, whereas cally positive (sensitivity 82%). today only a few families with no more than 15-20 individuals can be seen. The low production of meat and Alpacas: Concerning South American camelids inhabi- milk caused by severe infection levels ranging between ting the fascioliasis endemic zone of the Northern Alti- 20 and 100% in numerous communities makes livestock piano, only a few surveys have been made on alpacas exploitation very difficult. This becomes extremely im- and none on llamas. portant in the Altiplano, because sheep and cattle are the MORALESLAVADENZ(1973) studied alpacas from Be- main sources of income in subsistence agriculture. len. The N.I.A.H. sedimentation technique showed 59% of 22 alpacas shedding F. hepatica eggs in stools. Fas- National control programmes cioliasis intensity in alpacas was studied in 5 g stool samples with the Dermis technique; averages of 75,4, 16 Official data of the year 1985 refer to 500000 cattle li- and 2,5 eggs were found in animals with high (n=7), mo- ving in the Bolivian Altiplano, which represents 10,64% derate (n=2) and low (n=2) infection, respectively. UENO of bovines in all of Bolivia. Among them, 297490 et at. (1975) referred to the same results (59,1% infected (6,04%) inhabit the La Paz Department. According to of 22 alpacas studied in Belen) already reported by Mo. the same official paper, a total of 2513000 sheep are li- RALESLAVADE Z (1973). ving in this Department of La Paz. Owing to the impor- A similar study on alpacas from Belen was carried tance of these data, a programme to fight against fascio- out one year later by LozANO MONROY (1974), but liasis for the period of 1989-1993, including objectives, only by means of the N.I.A.H. sedimentation technique instruments and recommendations, was established applied to 5 g stool samples. A total of 25 alpacas (ANON, 1989). This programme clearly recognized the among 29 studied showed eggs in their stools (86,2%), importance of animal fascioliasis in the Northern Alti- including the following intensities: 22 alpacas presen- piano, as acknowledged by the governmental authorities ted fewer than 10 eggs, 2 alpacas showed between 10 of Bolivia. and 30 eggs, and only I alpaca presented more than 30 eggs. Treatment Only a few papers have been found on veterinary Economic and production losses due to fascioliasis treatments, although much of the livestock is treated Although no study has been carried out on clinical and against fascioliasis in the Northern Altiplano. Today this pathological observations in livestock from the Bolivian treatment is mainly with triclabendazole (Fasinex's'), Northern Altiplano, there are however a very few studies systematically in farm animals and only whenever possi- dealing with economic and production losses. ble in animals belonging to families, depending on drug The latest estimate by the Bolivian Ministry in 1986 availability and acquisition capacity of the owners. reports an annual loss of 5 million US $ in the livestock According to UENO & MORALES(1973), sheep on a of the Altiplano owing to zoonoses, mainly fascioliasis; farm where animals were dying from acute fascioliasis this fact increases in importance when we take into ac- were given diamphenetide at 85-116 mg/kg body-weight count that, among the Aymara Indians, livestock tradi- or niclofolan at 3,2-4,3 mg/kg. Diamphenetide was tions are passed on through the family (CARTER& MA- found to be highly effective; almost 100% of immature MANI, 1982; ALBO, 1988). F. hepatica were killed, but a few adult flukes were still 90 S. MAS-COMAet at. alive at post-mortem examination 10 days after treat- Paz (see MERCADO TUDOR & MlRALES GOYTIA, 1991) ment. No adult flukes were recovered from the animals is evident. which received niclofolan, but the drug appeared to have It is worth mentioning that both murids and cavio- no effect against immature flukes under 8 mm long. Du- morphs are, respectively, omnivorous and herbivorous ring the period of the experiment by UENO & MORALES rodents already well-known as viable definitive hosts of (1973), 5 untreated sheep died of acute fascioliasis; no F. hepatica in laboratory conditions (MAS-COMA et al., treated sheep died. 0 signs of toxicity were observed. 1988). Studies are evidently needed to ascertain whether Based on published data for other parts of the world, hares and/or given rodent species may play a role in the ORTUBE GOITlA (1986) discusses the most probable ch- transmission of F. hepatica and up to which level, in or- ronology of the annual life cycle of F. hepatica in the der to consider their possible epidemiological impor- Northern Altiplano, according to seasons and their tem- tance as free-living reservoirs of the liver fluke in the peratures. This author suggests that to achieve the most Northern Bolivian Altiplano. effective results in the Altiplano, treatment must be applied at the end of autumn, the end of winter and in mid- summer. He also mentioned studies in which 6 months ACKOWLEDGEME TS were needed to destroy 80% of metacercariae, but the Study supported by a Project (Contract o. TS3-CT94-0294) of author did not note whether such data are results from the STD Programme of the Commission of the European Commu- his studies on the Altiplano or from studies by other aut- nities (DG XII:Science, Research and Development), Brussels, hors in other regions of the world. EU, and by the Programme of Scientific Cooperation with Latin VILLCA, CRUZ & ALCON (1989), after a prevalence America of the Institute de Cooperacion Iberoamericana of the study in cattle and sheep in Corapata, recommended a Agencia Espafiola de Coopcracion Internacional (T.C.T.-A.E.C.I.). treatment campaign with Fasinex'v, supported by diffu- The authors want to acknowledge the facilities and collaboration received from the following organisations, institutions and centres, sion obtained through Radio San Gabriel and Radio as well as their respective representatives or directors: Instituto Mendez Agricultura. Nacional de Laboratorios de Salud (INLASA) of La Paz; Direc- cion Nacional de Relaciones Internacionales as well as the Direc- cion Nacional de Epidemiologfa of the Ministerio de Prevision So- THE POTENTIAL FREE LIVING cial y Salud Publica (today become the Secretarfa Nacional de A IMALRESERVOIRS Salud of the new Ministerio de Desarrollo Humano) in La Paz; Co- mite Regional de Zoonosis and Centro Piloto La Paz of the Unidad Sanitaria La Paz; Academia Boliviana de Medicina in la Paz; Ser- The literature on fascioliasis shows that several wild vicio de Laboratorios de Diagnostico e Investigacion en Salud animals must be considered as potential reservoirs parti- (SELADIS) of the Facultad de Farmacia y Bioquirnica of the Uni- cipating in the transmission of the parasite and hence in versidad Mayor de San Andres (UMSA) in La Paz; Direccion Na- the local epidemiology of the disease (see BAILENGER et cional de Produccion Pecuaria and the Instituto Nacional de Biolo- al., 1965; BORAY, 1982; MAS-COMA et al., 1987, 1988; gfa Animal of Chasquiparnpa-Calacoto both of the Ministerio de Asuntos Campesinos y Agropecuarios (M.A.C.A.) in La Paz; ALCAINO et al., 1990; APT et al., 1993). In the Northern Granja de Mejoramiento Ganadero de Kallutaca related to the Pro- Bolivian Altiplano only rodents and hares may be taken grama de Fomento Lechero of the Corporacion Regional de Desa- into account in this sense. rrollo de La Paz (CORDEPAZ); Instituto de Ecologfa of the Facul- According to our knowledge, research on rodents and tad de Ciencias Puras y aturales of the Universidad Mayor de hares inhabiting the fascioliasis endemic zone in the San Andres in Calacoto-La Paz; Museo Nacional de Historia Natu- Northern Bolivian Altiplano has never been undertaken. ral in Cota Cota-La Paz;Centro de Datos para la Conservacion (de After the information obtained, hares seem to be introdu- America Latina y el Caribe) in Cota Cota-La Paz; Laboratorio de Biologfa "San Calixto" in La Paz; Office of the Pan American He- ced from the Peruvian neighbouring zone. alth Organization in La Paz; and Danish GO Danchurchaid-Boli- Concerning rodents, nobody knows which rodent spe- via in La Paz. cies inhabit the fascioliasis endemic zone. A first evaluation made together with specialists of the University of California, Davis (California, USA)(Or. S.L. Gardner) and the Museo Nacional de Historia Natural of La Paz REFERENCES (Director Or. F.J. Cerda Dura, Lic. J. Sarmiento, Lic. T. ALBO(X.), compiler, 1988.- Raices de America: el Mundo Ay- Tarifa) provided the following list of rodent species to mara. U ESCO, Sociedad Quinto Centenario, Alianza Edito- be expected as most probably present in the Bolivian rial, S.A., Madrid, 607 pp. Northern Altiplano: Mus musculus (Muridae), Oryzomys ALCAI 0 (H.), VEGA(F.), KLEIN(P.), GORMA (T.) & APT (W.), spp., Oligoryzomys spp., Akodon spp., Calomys lepidus, 1990.- Fascioliasis en caballos, cerdos y conejos silvestres de la Calomys spp., Phyllotis spp., Neotomys spp and Andi- provincia de Talca, VII Region Chile. Parasitologia al Dia, 14: nomys spp.(Cricetidae), Ctenomys leucodon and Cte- 9-13. ANGLES(R.), 1986 a.- Informe del estudio de distomatosis hepa- nomys spp.(Octodontidae), Lagidium viscacia (Chinchi- tica en las localidades de Tauca (provincia Omasuyos) y Cutu- lidae) and Galea musteloides, Cavia aperea and Cavia suma (provincia Los Andes). Informe de INLASA a la Direc- porcellus (Caviidae). The similarity of this list with the cion Nacional de Salud y a la OPS/OMS, La Paz, Unpublished rodent species known in the neighbouring valley of La document, 13 pp. Human fascioliasis in Bolivia 91

ANGLES(R.), 1986 b.- Tratamiento realizado a los pobladores de CACERES VEGA(E.), 1989.- Fasciola hepatica - «Enfermedad )' Cutusuma. Informe presentado a la Direccion Sanitaria el Mi- Pobreza Campesina», Accion un Maestro Mas, Imprenta Meto- nisterio de Prevision Social y Salud Publica, La Paz, Unpubli- dista, La Paz, 20 I pp. shed document, 4 pp. CARTER (W.E.) & MAMA I (M.P.), 1982.- «Irpa Chico»: lndivi- ANGLES(R.), 1990.- Informe final del tratamiento de distomatosis duo y Comunidad en la Cultura Aymara. Librerfa - Editorial Ju- humana en Corapata Junio-Julio 1990. Documento presentado ventud, La Paz, 460 pp. por Plan Internacional Altiplano Bolivia a la Division Nacional CENTELLASGUEVARA (M.R.), 1987.- Ynmunojluorescencia indi- de Zoonosis del Ministerio de Prevision Social y Salud Publica, recta en el diagnostico de la Distomatosis hepdtica humana. Te- La Paz, Unpublished document, 20 pp. sis de Grado, Facultad de Farmacia y Bioqufmica, Universidad ANON, 1965.- Prevalence of selected parasitic infections and nutri- Mayor de San Andres (UMSA), La Paz, 76 pp. tional status. in: Estudios Epidemiologicos del Cuerpo de Paz; CHEN(M.G.) & MOTT (K.E.), 1990.- Progress in assessment of La Paz, Chapter 3: 101-183. morbidity due to Fasciola hepatica infection: a review of recent AON, 1989.- Perfil de program a para la vigilancia y control de la literature. Tropical Diseases Bulletin, 87 (4): RI-R38. fascioliasis en Bolivia 1989-1993. in: Primer Seminario Nacio- CUEVAS(F.), 1980.- Prevalencia de la Fascioliasis ell bovinos sa- nal de Vigilancia y Control de la Fascioliasis, TeniasislCisticer- crificados ell el Maradero Municipal 1965-1977 Santa Crur - cosis e Hidatidosis (8-9 Junio 1989). Conclusiones y recomen- Bolivia, 1980. Tesis de Grado, Facultad de Ciencias de la Salud, daciones de propuestas prograrnaticas. Ministerio de Prevision Carrera de Medicina Veterinaria y Zootecnia, Universidad Boli- Social y Salud Publica, Ministerio de Asuntos Campesinos y viana «Gabriel Rene Moreno», Santa Cruz, 60 pp. Agropecuarios, Program a de Coordinacion en Supervivencia In- DENNls (W.R.), STONE (W.M.) & SWANSON (L.E.), 1954.- A fantil, La Paz, I: 1-17. new laboratory and field diagnostic test for fluke ova in feces. ARANDIA(R.), 1972.- Informe ecologico de la parasitosis ovina en Journal of the American Veterinary Medicine Association, el Altiplano. Instituto Nacional de Biologfa Animal (l.N.B.A.), 124: 47-50. La Paz (cited in ORTUBEGOITIA, 1986). ELFo-CALvo (D.), CAMACHO(M.),CHUNGARA(E.) & CASTILLO ARAUJO(H.), 1965.- Los parasites del ganado y su control en Bo- (S.), 1976.- Parasitosis en la altura. In: IV Congreso Latinoame- livia. Ministerio de Agricultura, Servicio de Extension Agrfcola. ricano de Parasitologia (San Jose, Costa Rica, Dec. 1976), Re- El Extensionista, Boletin lnformativo, 5 (Enero) (cited in OR- sumenes de Trabajos Libres: 71. TUBEGOITIA, 1986). ESPANAVASQUEZ(CF.), 1989.- Diagnostico de Distomatosis he- APT (W.), AGUILERA(X.), VEGA (F.), ALCAI 0 (H.), ZULANTAY pdtica humana utilizando antigeno soluble de Fasciola hepa- (l.), APT (P.), Go ZALEZ(V.), RETAMAL(C.), RODRIGUEZ(J.) & tica. Tesis de Grado, Facultad de Farmacia y Bioquimica, Un i- SA DOVAL(J .), 1993. Prevalencia de Fascioliasis en humanos, versidad Mayor de San Andres, La Paz, 109 + 3 pp. caballos, cerdos y conejos silvestres en tres provincias de Chile. EUZEBY(J .), 1971.- Ecologie et biologie de Lymnea truncatula en Boletin de la Oficina Sanitaria Panamericana., I 15 (5): 405-414. Europe. Cahiers de Medecine veterinaire, 40: 283-289. BAHAR(K.), SOLYMANLOU(F.), POURTAGHVA(M.), RAHIMI(F.B.) FLoREs SERNA(A.F.) & ESTEVEZMARTINI(R.), 1988.- Fasciolasis & NIKBIN(B.), 1990.- A modified antigen currently used in en la ciudad de La Paz. Cuadernos del Hospital de Clinicas, La diagnosis and follow up of recent epidemy of distomatosis in Paz; 34 (2): 14-18. Iran. Bulletin de la Societe Francaise de Parasitologie, 8 FRANKEN(M.), 199\.- Plantas acuaticas, In: Historia Natural de (Suppl. 2): 985. un Valle en Los Andes:La Pa; (E. Forno & M. Baudoin edit.), BAILENGER (J.), TRIBOULEY (Y.), Au YOT (B.) & DURET (J.), Institute de Ecologfa, Universidad Mayor de San Andres 1965.- Importance des Leporides comme reservoirs sauvages (UMSA), La Paz: 511-520. dans l'epidemiologie des distomatoses a Fasciola hepatica et FRA KE(M.) & PINTO(J.), 1989.- Estudio de la ecologfa de Fas- Dicrocoelium dendriticum. Annales de Parasitologie Humaine ciola hepatica. Documento de Propuesta de Proyecto, Instituto et Comparee, 40: 51-54. de Ecologfa, Universidad Mayor de San Andres (UMSA), La BASSET (D.), GAUMERAIS(H.) & BASSET-POUGNET(A.), 1986.- Paz, Unpublished manuscript, 20 pp. Parasitoses intestinales infantiles dans une collectivite indienne HARTMANN(L.F.) & PATINO(F.), 1962.- Distomatosis extrahepa- de I' Altiplano bolivien. Bulletin de la Societe de Pathologie tica. Prensa Medica, La Paz; 14, 104-106. Exotique, 79 (2): 237-246. HILLYER(G.V.), SOLERDE GALANES(M.), RODRIGUEZ-PEREZ(L), BERGEON(P.) & LAURENT(M.), 1970.- Differences entre la mor- BJORLAND(J.), SILVADE LAGRAVA(M.), RAMIREZGUZMAN(S.) phologie testiculaire de Fasciola hepatica et Fasciola gigantica. & BRYAN (R.T.), 1992.- Use of the Falcon Assay Screening Revue d'Elevage et de Medecine Vererinaire des Pays Tropi- Test -Enzyme-Linked Immunosorbent Assay (FAST-ELlSA) caux, 23: 223-227. and the Enzyme-Linked Immunoelectrotransfer Blot (EITB) to BJORLAND(J.), McAULEY (J.B.), STRAUSS(W.), RICHER(G.), A - determine the prevalence of human Fascioliasis in the Bolivian TEZA A (A.), HILLYER(G. V.), JURA EK(D. D.) & BRYA(R.T.), Altiplano. American Journal of Tropical Medicine and Hygiene, 1992.-An outbreak of acute fasciolasis in humans in the Boli- 46: 603-609. vian Altiplano. In: XII Congreso Panamericano de Ciencias Ve- HILLYER (G. V.), SOLERDE GALA ES (M.), BUCHO(P.) & BJOR- terinarias (Santiago de Chile, Chile, Oct. 1992), Abstracts of LAND(J .), 1993.- Herd evaluation by enzyme-linked immuno- papers. sorbent assay for the determination of Fasciola hepatica infec- BORAY(J.C.), 1982.- Fascioliasis. In: Handbook Series in Zoono- tion in sheep and cattle from the Altiplano of Bolivia. In: XI ses. Section C. Parasitic Zoonoses. Volume III (G.V. Hillyer & Congreso Latino-Americano de Parasitologia (Lima, Peru, CE. Hopla edit.), CRC Press, Boca Raton-Florida: 71-88. Nov. 1993), Abstracts of papers. BOTELLO(Ch.), MACHICADO(E.) & PUCH (R.), 1981.- Distomato- INE, 1992.- Bolivia en cifras 1992. Instituto Nacional de Estadls- sis hepatica,Estacion Experimental de Belen, Instituto Boli- tica, La Paz. viano de Tecnologia Agropecuaria, Serie Ganadera No. 6, La JUSTINIANO(J.G.) & ARCE LEMA(J.), 1989.- Resolucion Biminis- Paz, Bolivia (cited in ORTUBE GOITlA, 1986). terial o. 0597 de 4 de Agosto de 1989 por la que se declara de BRYAN(R.T.),EsPI DOLA(C), LAGRAvA(M.),AGREDA(W.), EVE- interes la Vigilancia y Control de la Fascioliasis, Teniasis-Cisti- RAERT(D.) & HILLYER(G.), 1989.- Fascioliasis among Aymara cercosis e Hidatidosis en las areas epizoendemicas del territorio Indians, Bolivia. In: Epidemic Intelligence Service 38th Annual nacional y se crea el «Cornite tecnico de Vigilancia y Control de Conference (Atlanta, 3-7 April 1989), Abstract of papers. las Zoonosis». Ministerio de Prevision Social y Salud Publica y 92 S. MAS-COMA et al.

Ministerio de Asuntos Campesinos y Agropecuarios, La Paz, de eleccion para el diagnostico de la Distomatosis hepatica hu- Bolivia, 2 pp. mana. Tesis de Grado, Facultad de Farmacia y Bioquimica, Uni- KENDALL(S.B.), 1954.- Fascioliasis in Pakistan. Annals of Tropi- versidad Mayor de San Andres (UMSA), La Paz, 131 pp. cal Medicine and Parasitology, 48: 307-313. MORALES(G.) & PINO (L.A.), 1981.- Lymnaea cubensis Pfeiffer, KENDALL(S.B.) & PARFITT(J.W.), 1959.- Studies on susceptibi- 1839, hospedador interrnediario de F. hepatica en la zona alta lity of some species of Lymnaea to infection with Fasciola gi- de los Andes trujillanos, Venezuela. Boletin de la Direccion de gantica and F. hepatica. Annals of Tropical Medicine and Para- Malariologia y Sanidad Ambiental, 21 (I): 39. sitology, 53: 220-227. MORALES(G.) & PI 0 (L.A.), 1983.- Infection de Lymnaea cubensis KNOBLOCH(J.), 1985.- Human fascioliasis in Cajarnarca/Peni. 11. par Fasciola hepatica dans une region d'altirude, au Venezuela. Humoral antibody response and antigenaemia. Tropical Medi- Annates de Parasitologie Humaine et Comparee, 58: 27-30. cine and Parasitology, 36:91-93. MORALES LAVADENZ (GUSTAVO), 1973.- Algunos aspectos de KNOBLOCH(J.), DELGADO(A.E.), ALVAREZ(G.A.), REYMANN(U.) Fascioliasis en areas altiplanicas proximas a la ciudad de La & BIALEK(R.), 1985.- Human fascioliasis in Cajamarca/Peni. 1. Par. Tesis de Grado, Facultad de Ciencias de la Salud,Carrera Diagnostic methods and treatment with praziquantel. Tropical Veterinaria, Universidad Boliviana «Gabriel Rene Moreno», Medicine and Parasitology, 36:88-90. Santa Cruz, 31 pp. LOBAToPARAE SE (W.), 1982.- Lymnaea viatrix and Lymnaea co- MOREL (A.M.) & MAHATO(S. .), 1987.- Epidemiology of fascio- lumella in the Neotropical region: a distributional outline. Me- liasis in the Koshi hills of epal. Tropical Animal Health and morias do Instituto Oswaldo Cruz; 77 (2): 181-188. Production, 19: 33-38. LOKER (E.S.), HOFKIN(B.Y.), MKOJl (G.M.), MUNGAI (B.), ORTUBE GOITIA(M.C.), 1986.- Estudio epizodemico sobre Fas- KIHARA(J.) & KOECH (D.K.), 1993.- Distributions of freshwa- ciola hepatica y otras parasitosis.Su incidencia sobre el sistema ter snails in southern Kenya with implications for the biological de produccion de leche en el area de influencia de la Granja de control of schistosomiasis and other snail-mediated parasites. Mejoramiento Bovino de Kallutaca. Tesis de Grado, Facultad de Journal of Medical and Applied Malacology, 5: 1-20. Ciencias de la Salud (Carrera de Fannacia y Bioquimica), Uni- LOZA 0 Mo ROY(B.), 1974.- Fasciola hepatica: encuesta para- versidad Mayor de San Andres (UMSA), La Paz, 57 pp. sitologica en el departamento de La Paz, Tesis de Grado, Facul- PAREAU(M.), Ra DELAUD(D.), DREYFUSS(G.), BOUTEILLE(B.) & tad de Ciencias de la Salud (Carrera Bioquimica), Universidad DARDE (M.L.), 1994.- Fasciola hepatica Linne: observations Boliviana Mayor de San Andres, La Paz, 47 pp. epiderniologiques sur les cas de distomatose humaine dans le MACA, 1988.- Estadisticas agropecuarias de 1988. Ministerio de Limousin (France) par rapport it I'altitude des cressonieres natu- asuntos Campesinos y Agropecuarios (MACA), La Paz. relIes. Bulletin de la Societe Francaise de Parasitologie, 12: MANGA-GONZALEZ(Y.), GONzALEz-LANzA (C.) & OTERO-MERINO 167-174. (C.B.), 1991.- atural infection of Lymnaea truncatula by the PAY 0 (J.M.), 1977.- Identificacion de parasitos de importancia liver fluke Fasciola hepatica in the Porma Basin, Le6n, NW veterinaria en los animales del Departamento de La Paz: (Cited Spain. Journal of Helminthology, 65: 15-27. in ORTUBEGOITIA, 1986). MARTI EZ (E.), MOLLI EDO (S.), TORREZ (M.) & MIRA DA (R.), PEREZ-REYES(R.), JIME EZ- AVA(J.J.) & VARELA-RAMIREZ(A.), 1991.- Distomatosis hepatica en el Altiplano boliviano. Trabajo 1985.- Fascioliasis en el Estado de Chihuahua, Mexico. I Sus- financiado por ellnstituto Privado Pasteur Bolivia.Unpublished ceptibilidad de Fossaria modicella (Say, 1825), huesped inter- manuscript, La Paz, 11 pp. mediario local. Revista Latino-Americana de Microbiologia, 27: MAS-COMA(S.), FONS (R.), FELlU(C.), BARGUES(M.D.), VALERO 367-372. (M.A.) & GALAN-PUCHADES(M.T.), 1987.- Consequences des PINILLA(C.), 1939.- (20 casos de Fascioliasis humana en La Paz). phenornenes lies it I'Insularite dans les maladies parsitaires. La Semana Medica, Buenos Aires (cited in HARTMAN & PATI-O, Grande douve du foie (Fasciola hepatica) et les Murides en 1962). Corse. Bulletin de la Societe Neuchdteloise des Sciences Natu- PINILLA(C.) & PAZ(D.), 1939.- (Fascioliasis humana en La Paz). relies, 110: 57-62. El Hospital (cited in HARTMA & PATI-O, 1962). MAS-COMA (S.), Fo S (R.), FELIU (C.), BARGUES(M.D.), VALERO POURTAGHVA(M.), SHAFI (A.), SABERI(A.), BAHAR(K.) & SOLY· (M.A.) & GALAN-PUCHADES(M.T.), 1988.- Small mammals as MANLOU(F.), 1990.- Fasciolase en Iran. Bulletin de la Societe natural definitive hosts of the liver fluke, Fasciola hepatica Lin- Francaise de Parasitologie, 8 (Suppl. I): 404. naeus, 1758 (Trematoda: Fasciolidae): a review and two new re- SALAZARESCOBAR(S.), 1979.- Prevaiencia de la Fascioliasis he- cords of epidemiologic interest on the island of Corsica. Rivista pdtica bovina en el area urbana y suburbana de la ciudad de La di Parassitologia, 5 (49), I: 73-78. Paz, Tesis de Grado, Facultad de Ciencias de la Salud, Carrera MASSOUD(J.), 1990.- Fascioliasis outbreak of man and drug test de Medicina Veterinaria y Zootecnia, Universidad Boliviana (Triclabendazole) in Caspian littoral, northern part of [ran, «Gabriel Rene Moreno», Santa Cruz, 33 pp. 1989. Bulletin de la Societe Francaise de Parasitologie, 8 SCOTT(J.M.) & GOLL (P.H.), 1977.- The epidemiology and ant- (Suppl. I): 438. helminthic control of ovine fascioliasis in the Ethiopian Central McAuLEY (lB.), 1991.- Fascioliasis in Calasaya, Bolivia.CDC Highlands. British veterinary Journal, 133: 273-280. consultant preliminary report to the Bolivian Ministry of Health, STORK (M.G.), VENABLES(G.S.), JENNINGS(S.M.F.) & BEESLEY Unidad Sanitaria La Paz, Danchurchaid, and the United States (J.R.), 1973.- An investigation of endemic fascioliasis in Peru- Agency for International Development. Unpublished manus- vian village children. Journal of Tropical Medicine and Hy- cript, 16 pp. giene, 76: 231-235. MERCADOTUDOR(1.0.) & MIRALLESGOYTIA(J .), 1991.- Mamffe- STRAUSS (W.), CETELLAS (M.R.), Mo TERO (I.), TORREZ (M.), ros. In: Historia Natural de un Valle en Los Andes: La Pa; (E. MARTINEZ(E.) & ANGLES (R.), 1986.- lnforme del tratamiento Forno & M. Baudoin edit.), lnstituto de Ecologia, Universidad para eliminar distomas hepaticos realizado a los pobladores de Mayor de San Andres (UMSA), La Paz: 293-343. Cutusuma.Informe de INLASA a UNICEF, La Paz, Unpublis- MOLlNA PADILLA(0.1.), 1987.- La. valide; de la intradermoreac- hed document, 3 pp. cion como tecnica de diagnostico de Distomatosis hepdtica hu- STUNDELL (M.) & MOLLlNEDO(S.), 1979.- El T'alpalako en las mana. Tesis de Grado, Facultad de Farmacia y Bioquimica, Un i- orillas del Lago Titicaca, Chojasivi. lnforme de la Misi6n Berlin versidad Mayor de San Andres (UMSA), La Paz, 76 pp. - Schonow, Departamento de Parasitologfa, Facultad de Medi- MONTEROBUSTILLOS(I.E.), 1987.- Tecnica coproparasitologica cina, Universidad de Berlin, Unpublished document. Human fascioliasis in Bolivia 93

UENO (H.) & MORALES(G.), 1973.- Fasciolicidal activity of fluke in East Africa. Journal of Animal Ecology, 15: 170-197. diamphenetide and niclofolan against Fasciola hepatica in VELA PACHECO (E.), 1988.- Fascioliasis hepato-biliar en la infan- sheep in the Altiplano Region of Bolivia. National Institute of cia. Revista de la Sociedad Boliviana de Pediatria, La Paz; 27 Animal Health Quarterly, 13, 75-79. (2): 397-404. UE 0 (H.), ARA DIA(R.), MORALES (G.) & MEDINA(G.), 1975.- VERAZAIN(L.), 1982.- Estudio de investigaci6n sobre incidencia Fascioliasis of livestock and snail host for Fasciola in the Alti- de Fasciola hepatica en grupos escolares de dos comunidades piano region of Bolivia. National Institute of Animal Health (Villa de la Cruz y Cullucachi), Provincia Los Andes del Depar- Quarterly, 15: 61-67. tarnento de La Paz. Informe de CORDEPAZ,Unpublished ma- VACHER (1.1.), BRASIERDE THUY (E.) & LIBERMA (M.), 1991.- nuscript. Influencia del lago en la agricultura local. In: El Lago Titicaca. VILLCA (M.E.), CRUZ (D.) & ALCO(C.), 1989.- Experiencias en Sfntesis del conocimiento limnologico actual (C. Dejoux & A. el control de la Fascioliasis hepatica 1988-1989. Informe de la litis edit.), ORSTOM-HISBOL, La Paz: 517-530. organizaci6n Foster Parents Plan del Plan Altiplano La Paz a la VA SOMEREN(V.D.), 1946.- The habitats and tolerance ranges of Jefatura acional de Zoonosis del Ministerio de Previsi6n So- Lymnaea (Radix) caillaudi, the intermediate snail host of the liver cial y Salud Publica, La Paz, Unpublished manuscript, 15 pp.