Fascioliasis in Cattle in the Human High Endemic Region of the Bolivian Northern Altiplano

FASCIOLIASIS IN CATTLE IN THE HUMAN HIGH ENDEMIC REGION OF THE BOLIVIAN NORTHERN ALTIPLANO

1 2 2 2 2 1 P. BUCHON • , H. CUENCA , A.QUlTON , A.M. CAMACH0 & S. MAS-COMA

I Departamento de Parasitologia, Facultad de Farmacia, Universidad de Valencia, Av. Vicenl Andres Estelles sin, 46100 Burjassot - Valencia, Spain 2Laboratorio 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 km 5, El A 110, Bolivia

Received 29 October 1996; accepted 17 May 1997

REFERENCE:BUCHON(P.), CUE CA(H.), QUITO (A.), CAMACHO(A.M.) & MAS-COMA(S.), 1997.- Fascioliasis in cattle in the human high endemic region of the Bolivian orthern Altiplano. Research and Reviews in Parasitology, 57 (2): 71-83. ABSTRACT:Coprological surveys were carried out to study Fasciola hepatica infection in 5491 cattle from II zones and 107communities on the Bolivian Altiplano, where the highest prevalences and intensities in human subjects have been found. The research work had the aim of contribu- ting to the knowledge about the geographical distribution of the liver fluke and the epidemiological reservoir host role of bovines in the transmission of the disease in this endemic area. According to the results obtained, the parasite is present throughout almost all the Northern Bolivian Alti- pIano, but it does not extend toward the Central Bolivian Altiplano, in the South.The total prevalence found in cattle of the Northern Bolivian Altiplano was 16,5%. The prevalences were irregularly distributed, varying considerably according to zones (7,8-34,0%) and communities (0,0- 66,6%). Bovines of less than I year appear to be only rarely infected (8, I%), whereas the prevalence increases markedly in animals aged 1-2years (35,I%) and is apparently maintained at a similar level in cattle aged more than 2 years (29,2%). Prevalences do not show marked monthly changes and community prevalence ranges are very wide within each month. It may be assumed that the contamination of the environment by eggs expelled by cattle is assured throughout the year. Egg output numbers do not vary considerably within a given community (usually between I and 30 eggs/4 g faeces) and in no case did the count reach 100. A few communities showed relatively high numbers in the upper range (up to 96 eggs/4 g faeces). It is concluded that in the orthern Bolivian Altiplano, cattle participate in the contamination of the environment with liver fluke eggs at a level similar to sheep. According to the prevalence and egg output results obtained, cattle may be considered, like sheep, a main reservoir host of fascioliasis in this Altiplanic endemic zone. At any rate, infection rates in Altiplanic bovines do not appear to be high enough to explain the high infection rates detected in human subjects of the Northern Bolivian Altiplano. KEYWORDS:Liver fluke, Fasciola hepatica, fascioliasis, cattle, coprological surveys, geographical distribution, prevalences, intensities, Northern Bolivian Altiplano.

INTRODUCTION probably by Spanish colonizers (OVIEDO, BARGUES & MAS-COMA, J995a; BARGUES & MAS-COMA, 1997; BAR- The veterinary importance of fascioliasis caused by GUES et al., 1997; JABBOUR-ZAHAB et al., 1997). the cosmopolitan liver fluke species Fasciola hepatica In this fascioliasis endemic zone of the orthern Boli- (Linnaeus, 1758) (Trematoda: Fasciolidae) in livestock vian Altiplano, several studies have been undertaken to has long been well known (MALEK, 1980; BORAY, understand how the liver fluke is able to reach such 1982). Recently, it has been verified that it represents, transmission rates to human beings. Among these rese- moreover, a great human health problem (MAS-COMA & arch activities, investigations have been performed to as- BARGUES, 1997; MAS-COMA et al., 1998), with up to al- certain what role domestic and wild potential animal de- most seven thousand human cases diagnosed in the five finitive host species may play in the epidemiology of the continents (CHE & MOTT, 1990; ESTEBAN, BARGUES disease. Concerning domestic animals, several studies & MAS-COMA, 1998) and several world regions presen- on sheep, cattle and alpacas were carried out some time ting human endemic areas (MAS-COMA, BARGUES & Es- ago (UE 0 & MORALES, 1973; UENO et al., 1975; many TEBA, 1998). other reports, either unpublished or published in local In Bolivia, the region of the Northern Altiplano has pro- journals or diffusion booklets - see review by MAS- ved to be the zone in which the highest prevalences and COMA et al., 1995) to which a few recent ones must be intensities in human subjects have been found up to the added (BUCHON & MAS-COMA, 1995; HILLYER et al., present (HILLYER et al., 1992; MAS-COMA et al., 1995; 1996). A more recent paper by MAS-COMA et al. (1997) BJORLAND et al., 1995; ESTEBAN et al., 1997a, b; ANGLES has evaluated the epidemiological role played by domes- et al., 1997; STRAUSS et al., 1997). This endemic zone, tic animal species other than sheep and cattle, conclu- between Lake Titicaca and the valley of the city of La ding that only pigs and donkeys must be taken into ac- Paz, presents the peculiar characteristic of being at the count. Finally, FuE TES et al. (1997) analyzed the very high altitude of 3800-4200 m. Moreover, the inter- potential role of wild animal species present in the Alti- mediate molluscan host has recently proved to be the ba- planic endemic zone and concluded that small mammals sommatophoran species Lymnaea truncatula (Muller, (Lagomorpha and Rodentia) do not play a role in the 1774) (Lymnaeidae) imported long ago to Bolivia most transmission of the disease. 72 P. BUCHON et al.

From the results of the above-mentioned studies, we lence, incidence and egg number in faeces throughout the different know now that sheep and cattle are the main reservoir months of the year. Another problem which could not be avoided is that, in given communities, sometimes a treatment of all animals had animal host species and that pigs and donkeys may be taken place more or less time (one or several months) before stool considered important secondary reservoir species in the samples were collected; there are communities in which treatments Northern Bolivian Altiplano. Concerning pigs and don- are regular and programmed, in others they are sometimes done irre- keys, both qualitative (prevalences) and quantitative (in- gularly (when animals appear to be affected or when the owner has tensities by counting liver fluke egg number in faeces) money to treat the herd), and in others not at all. studies have been carried out (MAS-COMA et al., 1997). Concerning sheep and cattle, however, research studies Stool sample preparation and study: In the Animal Health Labo- ratory of Kallutaca, from each stool sample a quantity of 4 g was up to the present refer only to prevalence surveys made sedimerued twice, first with 50 ml of detergent solution (I mill 000 by different coprological or serological methods in a few crrr') after filtration and second with 50 ml water, and stained with given Altiplanic localities (UENO et al., 1975; MAS- methyl green according to DENNIS, STONE & SWA SON (1954), be- COMA et al., 1995; BUCHON & MAS-COMA, 1995; HILL- fore examination under light microscope for F. hepatica eggs. YER et al., 1996). Qualitative analyses giving rise to prevalence results were made in In the Northern Bolivian Itiplano, there is a lack of all communities surveyed (Table I), but investigations on the relationship of prevalences with age groups (Table 2) and quantitative analyses both on fluke burden aspects and on geographi- studies on egg output (Table 4) could only be performed in given cal distribution of the parasite among sheep and cattle communities. populations. The present research work aims to contri- bute to these two aspects concerning cattle. For geographical distribution analyses, cattle are more appropriate than sheep because bovines are more resistant to reinfec- RESULTS tion and the parasites only survive up to 1 year in them, whereas sheep are relatively susceptible to reinfection Geographical distribution and the liver fluke life-span can be as long as 11 years in them (DAWES & HUGHES, 1964; DELEON & QUII\JONES, The geographical distribution of communities where 1981; SMITHERS, 1982; HAROUN & HILL YER, 1986). cattle herds are infected by F. hepatica is shown in Fig. Hence, cattle are more useful as information tools to as- I. All zones studied are inhabited by cattle infected by certain the geographical distribution of transmission the liver fluke, excepting the Patacarnaya zone, in the foci, as in the Bolivian Altiplano cattle transport from South. According to these results, the parasite is present one to another place is not common. throughout almost all the Northern Bolivian Altiplano, but it does not extend toward the Central Bolivian Alti- pIano. The presence of the digenean parasite in cattle in MATERIAL AND METHODS the so-called «Tiwanaku corridor» seems to be rare and to follow a patchy distribution, according to the results Animal samples: From 1991 to 1994, 5491 cattle (Holstein, obtained in communities of the Tiwanaku zone and Gua- Brown Swiss, native and crossbreeds) faecal samples from animals qui zone. aged 5 months to 12 years were collected from II zones of the Bo- livian AItiplano in the Departament of La Paz. These II zones were divided into 107 communities (Fig. I, Table I):A) orthern Prevalences Altiplano: a) Omasuyos province: zone of Belen-Achacachi (14 communities); b) Los Andes province: zones of Pucarani (11 com- F. hepatica infection prevalences according to communities), Huayrocondo (3), Kallutaca (6), Laja (3) and Tambillo munities and zones are shown in Table I. The total pre- (6); c) Murillo province: zone of Saythu (6 communities); d) In- valence in the Northern Bolivian Altiplano is gavi province: zones of Tiwanaku (10 communities), Guaqui (9) 16,5%, and Viacha (18): B) Central Altiplano: a) Aroma province: zone of that is, 908 bovines detected shedding eggs among the Patacamaya (21 communities). Each one of these communities re- 5491 surveyed. Table 1 shows that the prevalences are ceived technical assistance from the Dairy Development Pro- irregularly distributed: there are zones with relatively gramme of the Regional Corporation of Development of La Paz high total prevalences, such as Kallutaca (34,0%) and (CORDEPAZ). In accordance with the study's purpose of ascertai- Tarnbillo (31,9%), and others presenting low prevalen- ning the role of cattle in parasite transmission and, consequently, ces, such as Pucarani (7,8%), Tiwanaku (8, I %) and the need to know the number of liver fluke eggs expelled with faeces and which contaminate the environment, only coprological Guaqui (8,0%). Within a given zone, community preva- surveys are here considered. lences vary considerably:Belen-Achacachi: 0,0-56,8%; Pucarani: 2,5-66,6%; Huayrocondo: 8,5-45,4%; Kallu- Stool sample collection: Faecal samples were directly collected taca: 0,0-50,0%; Laja: 8,0-26,3%; Tambillo: 4,0-45,2%; from the rectum of animals and transported to the Animal Health Saythu: 1,7-50,0%; Tiwanaku: 0,0-24,6% (only I com- Laboratory of Kallutaca within the following 5 hours. The number munity infected); Guaqui: 0,0-63,6%; Viacha: 0,0- of samples collected from each community was a minimum of 10% of the cattle population. Although several communities could be sur- 64,9%. veyed more than once, unfortunately stool sample collection could Results obtained in the studies on the relationship of not be made following the different annual seasons in a community prevalences with age groups are shown in Table 2. Bovi- and. thus, no data are available to analyse the variations of preva- nes aged less than I year appear to be only rarely infec- Fascioliasis in cattle in the Bolivian Altiplano 73

RI 1

66. Viacha El' .70 67. 69. 71 680 • 72· 73 • 76 740 o~ 75 77

078 z., 790 800 ~~.. C,

~;:~" C~ :'·L'/';?<~-',; ./

r-: '.

o 87 88

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Patacamaya 91

92093 98 0 940 o 0 990 97 960 95 1000 o 0102 0105 CENTRAL 101 0 ALTIPLANO 1030 104

Fig. 1.- Map of the Bolivian Altiplano showing zones and communities in which cattle were coprologically surveyed for Fasciola hepatica infection. For the names of the communities see respective numbers in Table I.• = communities with fascioliasis; 0 = communities in which fascioliasis was not detected. 74 P. BUCHO et at.

ZONE o. in map No. animals o. Prevalence ZONE No. in map No. animals No. Prevalence Community (see Fig. I) studied positive % Community (see Fig. I) studied positive %

BELEN-ACHACACHI ZONE: GUAQUI ZONE: Warisata I 4 2 50,0 Humamarca 44 45 7 15,5 Chijipina 2 156 44 28,2 San Antonio 45 13 3 23,1 Chijipina Grande 3 16 8 50,0 Jahuirapampa 46 11 7 63,6 Quenaquitara 4 27 5 18,5 Guaqui 47 14 0,0 Tacamara 5 176 100 56,8 Belen Pitutas 48 182 14° 7,6 Irarna Belen 6 17 0,0 Belen Patacarnaya 49 95 0,0 Chahuirapampa 7 252 1°5 5,9 Patarani 50 40 ° 0,0 Chahuirapampa Chico 8 12 2 16,6 Copagira 51 35 4° 11,4 L1onkoputunku 9 12 6 50,0 Andamarca 52 24 2 8,3 Jahuiralaca 10 24 4 16,6 TOTAL 459 37 8,0 Tipampa 11 59 28 47,4 Avichaca 12 316 43 13,6 TIWA AKUZO E: Asuntia 13 59 12 20,3 Yanarico 53 118 29 24,6 Pugunhuyo 14 36 9 25,0 Chambitaraco 54 12 0,0 TOTAL 1166 278 23,8 Chambi Chico 55 11 ° 0,0 Tiwanaku 56 8 ° 0,0 HUA YROCONDO ZONE: Guaraya 57 29 ° 0,0 Calasaya 15 33 15 45,4 Achaca 58 70 ° 0,0 Warisuyo 16 22 9 40,9 Caluyo 59 20 ° 0,0 Huayrocondo farm 17 248 21 8,5 Pircuta 60 25 ° 0,0 TOTAL 303 45 14,8 Chufiuchufiuni 61 56 ° 0,0 Callamarca 62 17 ° 0,0 PUCARANI ZONE: TOTAL 356 29° 8,1 Oquetiti 18 3 I 33,3 Sehuenca 19 144 9 6,2 VIACHA ZONE: Hospital 20 9 3 33,3 Pallina Laja 63 113 27 23,9 Iquiaca 21 10 I 10,0 Chonchocoro 64 22 9 40,9 Cota-Cota 22 15 3 20,0 Huanocollo 65 38 20 52,6 Sebaruyo 23 6 2 33,3 Pallina Chico 66 17 I 5,9 Pampacollo 24 3 2 66,6 Hilata San Jose 67 8 I 12,5 Ancocagua 25 195 22 11,3 Hilata Arriba 68 16 0,0 Kerarani 26 118 3 2,5 Choquenaira farm 69 74 48° 64,9 Cohani 27 19 I 5,2 Lirnani 70 45 7 15,5 Chojfiacollo 28 124 4 12,1 Chacorna 71 67 I 1,5 TOTAL 646 51 7,8 Achica Abajo 72 37 I 2,7 Calisaya 73 24 I 4,2 KALLUT ACA ZONE: Villa Arriendo 74 12 0,0 Kella-Kella 29 153 56 36,6 Pan de Azucar 75 33 ° 0,0 Capacasi 30 21 8 38,1 Muramaya 76 25 ° 0,0 Pomamaya 31 24 0,0 Achica Arriba 77 11 ° 0,0 Kallutaca 32 42 ° 0,0 lrpa Chico 78 I1 ° 0,0 Kallutaca farm 33 252 126° 50,0 Hichuraya Alto 79 14 ° 0,0 Ticuyo 34 77 4 5,2 Hichuraya 80 31 ° 0,0 TOTAL 569 194 34,0 TOTAL 598 116° 19,3

LAJA ZO E: PATACAMAYA ZO E: Orkojipifia 35 36 7 19,4 Challapata 87 19 0,0 Sulkataka 36 19 5 26,3 Ayo-Ayo 88 4 ° 0,0 Laja 37 25 2 8,0 Mantecani 89 8 ° 0,0 TOTAL 80 14 17,5 San Martin Iquiaca 90 15 ° 0,0 Patacamaya 91 IS ° 0,0 TAMBILLO ZONE: San Juan Culta 92 7 ° 0,0 Puchuni 38 3 I 33,3 Arajllanga 93 25 ° 0,0 Tambillo 39 50 2 4,0 Maso Cruz 94 95 ° 0,0 Masaya 40 16 2 12,5 Zora-Zora 95 31 ° 0,0 Caleria 41 43 3 7,0 Titiriri 96 77 ° 0,0 Chojasihui 42 29 9 31,0 Taypillanga 97 17 ° 0,0 Huacullani 43 210 95 45,2 Cochinitos 98 9 ° 0,0 TOTAL 351 112 31,9 Romero Pampa 99 16 ° 0,0 San Juan Sirca 100 19 ° 0,0 SA YTHU ZONE: Carachuyo 101 158 ° 0,0 Tuni 81 18 9 50,0 Thola Sirca 102 22 ° 0,0 Fascioliasis in cattle in the Bolivian Altiplano 75

ZONE No. in map No. animals No. Prevalence ZONE No. in map No. animals No. Prevalence Community (see Fig. I) studied positive % Community (see Fig. 1) studied positive %

SA YTHUZONE (cont.): PATACAMAYAZONE(cont.): Saythu 82 10 I 10,0 San Jose 103 45 0 0,0 Kajchiri 83 116 19 16,4 liiacamaya 104 94 0 0,0 Asunta Quilhuiri 84 4 1 25,0 Chijmuni 105 22 0 0,0 Kella-Kella 85 8 I 12,5 Piquiriani 106 9 0 0,0 Palomar 86 58 I 1,7 Sora-Sora 107 42 0 0,0 TOTAL 214 32 14,9 TOTAL 749 0 0,0

Table 1.- Prevalences obtained in coprological surveys on cattle from different zones and communities of the orthern Bolivian Altiplano. For the geographical location of zones and communities see respective numbers in Fig.I ted (8,1 %), whereas the prevalence increases markedly ver, as we move toward the south into the Central Boli- in animals aged 1-2 years (35, I%) and is apparently vian Altiplano (Patacamaya zone). The environmental maintained at a similar level in cattle aged more than 2 inhospitality of the Central Bolivian Altiplano may ex- years (29,2%). plain the absence of F. hepatica-infected bovines in this Prevalence results according to months are noted in southern zone. The influence of Lake Titicaca in the Table 3. When comparing the monthly results (indepen- Northern Altiplano (FUENTESet al., 1998) is lost, giving dently of years) it can be observed that prevalences do rise to very hard climatic conditions in the Central Alti- not show marked monthly changes and that community pIano, mainly temperature and humidity decreases prevalence ranges are very wide within each month (to- (RUTHSATZ, 1983; LORINI & LIBERMAN, 1983) which tal prevalence; prevalence range; number of communi- become inappropriate for the survival of both interme- ties surveyed in each month): January: 41,8%; 0,0- diate Iymnaeid snail host and liver fluke larval stages. 57,9%; 4; February: 24,8%; 1,7-52,6%; 7; March: Concerning the existence of fascioliasis-infected cattle 18,6%; 7,2-44,6%; 9; April: 15,0%; 0,0-50,0%; 10; in communities of the Guaqui zone, taking into account May: 39,9%; 1,4-83,8%; 4; June: 20,9%; 0,0-63,6%; 14; that only one community (Yanarico) presents infected July: 14,6%; 0,0-66,6%; 22; August: 26,3%; 1,9-87,5%; animals in the Tiwanaku zone, in the northern part of the 13; September: 21,8%; 6,5-80,0%; 12; October: 22,1%; same «Tiwanaku corridor», the question that arises is 0,0-60,0%; 15; November: 17,8%; 0,0-58,4%; 17; De- whether in the Guaqui zone, in the southern part of this cember: 30,4%; 22,7-50,0%; 2. The somewhat higher corridor, there are F. hepatica transmission foci or not. prevalences in January, May and December are not sig- The information obtained from herd owners suggest that nificant owing to the too small number of surveys ca- several bovines of Guaqui communities are already in- rried out in these months. fected when imported from neighbouring Peru, where they acquire fascioliasis in the plains located on the wes- tern side of Lake Titicaca, on the Peruvian Altiplano. Intensities Egg output counts are noted in Table 4. Egg output Prevalences means ranged only 2,7-12,6 eggs/4 g faeces among the different zones. Egg output numbers do not vary consi- In general, F. hepatica infection prevalence ranges derably within a given community (usually between I found in our surveys (Table 1) agree with prevalences and 30 eggs/4 g faeces) and in no case did the count re- detected by coprological methods in cattle from several ach 100. A few communities showed relatively high Altiplanic localities in previous studies, although preva- numbers in the upper range:Kallutaca farm: up to 88; \ences sometimes found by other authors in selected lo- Huanocollo: up to 93; Avichaca: up to 96; Tipampa: up calities or areas (Chirapaca, Achocalla, Batallas, Kallu- to 81; Taramaya: up to 70. Concerning egg output means taca area, Viacha) appear to be higher than those within a community, only a very few surpassed the num- detected in our studies:Belen (85,0% infected of 20 ani- ber of 10: Huanocollo: 13,0; Avichaca: 29,0; Jahuira- mals surveyed), Chirapaca (84,6% of 13), Achocalla laca: 16,6; Tipampa: 23,5; Warisata: 10,5. (78,4% of 125), Pajchani (0% of 5), Batallas (100% of 22), Guaqui (0% of 6), San Antonio (0% of I), Patarani (0% of 3), Achuta (0% of 1), Tiwanaku (0% of 5), Kallu- DISCUSSION taca farm (54,4% of 90), Kallutaca area (74,7% of 296), Takachira (40,0% of 10), Pillapi (0% of 8), San Juan Ro- sario (0% of23), Tambillo (12,0% of 18), Sulkataka (0% Geographical distribution of 7), Collantaka (66,6% of 6), La Paz city (35,9% of The geographical distribution of liver fluke-infected 206), El Alto (34,9% of 106), Palca (59,8% of 174), Rio cattle covers all the zones studied in the Northern Boli- Abajo (18,5% of 54), and Corapata (28,1 % of 327) (see vian Altiplano (Fig. I). The parasite disappears, howe- review by MAS-COMA et al., 1995); Corapata (26,0% of 76 P.BUCHO et al.

Age Total

< I year 1-2 years > 2 years

ZONES No. No.(%) No. No. (%) No. No. (%) No. No. (%) Communities examined positive examined positive examined positive examined positive

BELE -ACHACACHI ZONE Chahuirapampa 3 0(0,0) 29 5 (17,2) 32 5 (15,6) Avichaca 2 0(0,0) 12 5 (41,6) 14 5 (35,7) Llonkoputunku I 0(0,0) 11 6 (54,5) 12 6 (50,0) Warisata 4 2 (50,0) 4 2 (50,0)

HUAYROCO DO ZONE Warisuyo 4 3 (75.0) 4 3 (75,0) Calasaya I (100) 14 11 (78.5) 15 12 (80,0)

PUCARANIZONE Ancocagua 0(0,0) 25 I (4,0) 26 I (3,8) Chojfiacollo 23 2 (8,6) 23 2 (8,6) Cota-Cota 7 0(0,0) 18 3 (16,6) 25 3 (1,2) Pampacollo 3 2 (66,6) 3 2 (66,6) Oquetiti 3 I (33,3) 3 I (33,3) Iquiaca I 0(0,0) 9 1(11,1) 10 I (10,0) Hospital 3 0(0.0) 6 3 (50,0) 9 3 (33,3) Sebaruyo 6 2 (33,3) 6 2 (33,3)

KALLUTACA ZONE Capacasi 2 I (50,0) 3 2 (66,6) 13 3 (23,0) 18 6 (33,3) Kella-Kella 2 0(0,0) 6 4 (66,6) 34 15 (44,1) 42 19 (45,2) Ticuyo 15 0(0,0) 12 I (8,3) 34 3 (8,8) 61 4 (6,5)

LAJA ZO E Orkojipiria 5 0(0,0) 9 2 (22,2) 14 2 (14,2) Sulkataca 2 0(0,0) 5 I (20,0) 12 4 (33,3) 19 5 (26,3) Laja I 0(0,0) 6 2 (33,3) 10 0(0,0) 17 2 (11,7)

TAMBILLO ZONE Puchuni 3 I (33,3) 3 I (33,3) Masaya 2 0(0,0) 4 2 (50,0) 6 2 (33,3) Caleria 13 2 (15,3) 13 2 (15,3) Huacullani 17 9 (52,9) 17 9 (52,9)

GUAQUIZONE Andamarca 14 2 (14,2) 14 2 (14,2) Copagira 13 3 (23,0) 13 3 (23,0) Belen Pitutas 82 8 (9,7) 82 8 (9,7) Humamarca 2 0(0,0) 2 I (50,0) 31 6 (19,3) 35 7 (20,0) Jahuirapampa I I (100) 10 6 (60,0) 11 7 (63,6) San Antonio 13 3 (23,0) 13 3 (23,0)

TlWANAKU ZO E Chufiuchufiuni 1(100) I (100)

VIACHA ZONE Chonchocoro I 0(0,0) 8 3 (37,5) 9 3 (33,3) Pallina Laja 7 1(14,2) 4 I (25,0) 20 11 (55,0) 31 13 (41,9) Choquenaira farm 5 I (20,0) 25 17 (68,0) 44 30 (68,1) 74 48 (64,8)

SAYTHU ZONE Tuni 12 8 (66,6) 12 8 (66,6) Saythu 10 I (10,0) 10 I (10,0) Kella-Kella 8 I (12,5) 8 I (12,5) Asunta Quilhuiri 4 I (25,0) 4 I (25,0)

TOTAL 37 3 (8, I) 91 32 (35,1) 585 171 (29,2) 713 206 (28,8)

Table 2.- Prevalences obtained in coprological surveys on cattle from different zones and communities of the orthern Bolivian Altiplano, according to age groups. Fascioliasis in cattle in the Bolivian Altiplano 77

Months Year Community Zone No. o. % Prevalence examined positive positive range

JANUARY 1992 Kajchiri Saythu 5 0 0,0 1993 Tacamara Belen-Achacachi 164 95 57,9 Chijipina Belen-Achacachi 109 29 26,6 Yanarico Tiwanaku 52 14 26,9 TOTAL 330 138 41,8 0.0-57,9

FEBRUARY 1992 Chahuirapampa Belen-Achacachi 28 I 3,5 Palomar Saythu 58 I 1,7 Chonchocoro Viacha 13 6 46,1 Huanocollo Viacha 38 20 52,6 Limani Viacha 25 7 28,0 1993 Jahuiralaca Belen-Achacachi 6 I 16,6 Kallutaca farm Kallutaca 25 12 48,0 TOTAL 193 48 24,8 1,7-52,6

MARCH 1991 Huayrocondo farm Huayrocondo 72 6 8,0 Kallutaca farm Kallutaca 112 35 31,2 1992 Kella-Kella Kallutaca 13 3 23,0 Kajchiri Saythu 29 4 13,7 Tuni Saythu 6 I 16,6 1993 Avichaca Belen-Achacachi 162 17 lOA Tipampa Belen-Achacachi 47 21 44,6 1994 Belen Pitutas Guaqui 69 5 7,2 Humamarca Guaqui 24 5 20.8 TOTAL 534 97 18,6 7,2-44,6

APRIL 1991 Pungunhuyo Belen-Achacachi 36 9 25,0 Ticuyo Kallutaca 16 0 0,0 Tambillo Tambillo 12 I 8,3 Huacullani Tambillo 4 2 50,0 1992 Jahuiralaca Belen-Achacachi 18 3 16,6 Huayrocondo farm Huayrocondo 87 9 10,3 Warisuyo Huayrocondo 18 6 33,3 Calasaya Huayrocondo 18 3 16,6 Kajchiri Saythu 55 11 20,0 Achica Abajo Viacha 28 0 0,0 TOTAL 292 44 15,0 0,0-50,0

MAY 1992 Ancocagua Pucarani 60 4 6,6 Kallutaca farm Kallutaca 62 52 83.8 Chacoma Viacha 67 I 1,4 1994 Choquenaira farm Viacha 74 48 64,8 TOTAL 263 105 39,9 1,4-83,8

JUNE 1992 Cohani Pucarani 19 I 5,2 Kerarani Pucarani 35 0 0,0 Tambillo Tambillo 20 I 5.0 Caleria Tambillo 30 I 3,3 Chojasihui Tambillo 14 5 35.7 Huacullani Tambillo 100 45 45,0 Calisaya Viacha 15 0 0,0 Pallina Chico Viacha 17 I 5,8 Hilata San Jose Viacha 8 I 12,5 1993 Andamarca Guaqui 14 2 14,2 1994 Copagira Guaqui 13 3 23,0 Belen Pitutas Guaqui 39 3 7,6 Jahuiraparnpa Guaqui 11 7 63,6 San Antonio Guaqui 13 3 23,0 TOTAL 348 73 20,9 0,0-63,6 78 P. BUCHO et at.

Months Year Community Zone No. o. % Prevalence examined positive positive range

JULY 1991 Kella-Kella Kallutaca 6 I 16,6 1992 Huayrocondo farm Huayrocondo 89 6 6,7 Kallutaca farm Kallutaca 27 14 51,8 Masaya Tambillo 10 0,0 Chojasihui Tambillo 15 4° 26,6 Huacullani Tambillo 40 8 20,0 Belen Pitutas Guaqui 11 I 9,0 1993 Sehuenca Pucarani 92 8 8,6 Ancocagua Pucarani 41 5 12,1 Kerarani Pucarani 83 3 3,6 Chajfiocollo Pucarani 66 9 13,6 Laja Laja 8 0,0 1994 Chahuirapampa Belen-Achacachi 20 °3 15,0 Chahuirapampa ChicoBelen-Achacachi 12 2 16,6 Avichaca Belen-Achacachi 14 4 28,5 Llonkoputunku Belen-Achacachi 12 6 50,0 Warisata Belen-Achacachi 4 2 50,0 Pampacollo Pucarani 3 2 66,6 Oquetiti Pucarani 3 I 33,3 Iquiaca Pucarani 10 I 10,0 Hospital Pucarani 9 3 33,3 Sebaruyo Pucarani 6 2 33,3 TOTAL 581 85 14,6 0,0-66,6

AUGUST 1991 Sehuenca Pucarani 52 I 1,9 1992 Chahuirapampa Belen-Achacachi 21 I 4,7 Chijipina Grande Belen-Achacachi 11 5 45,4 Tipampa Belen-Achacachi 8 7 87,5 Tacamara Belen-Achacachi 8 5 62,5 Chenaquitara Belen-Achacachi 27 5 18,5 Orkojipifia Laja 5 3 60,0 1994 Pampacollo Pucarani 3 2 66,6 Oquetiti Pucarani 3 I 33,3 Iquiaca Pucarani 10 I 10,0 Hospital Pucarani 9 3 33,3 Sebaruyo Pucarani 6 2 33,3 Warisuyo Huayrocondo 4 3 75,0 TOTAL 167 44 26,3 1,9-87,5

SEPTEMBER 1992 Chajfiocollo Pucarani 35 4 11,4 Orkojipifia Laja 1I 2 18,1 Pallina Laja Viacha 55 7 12,7 1993 Avichaca Belen-Achacachi 26 3 11,5 Asuntia Belen-Achacachi 59 12 20,3 1994 Calasaya Huayrocondo 15 12 80,0 Kella-Kella Kallutaca 42 19 45,2 Ticuyo Kallutaca 61 4 6,5 Tuni Saythu 12 8 66,6 Saythu Saythu 10 I 10,0 Kella-Kella Saythu 8 I 12,5 Asunta Quilhuiri Saythu 4 I 25,0 TOTAL 338 74 21,8 6,5-80,0

OCTOBER 1991 Chahuirapampa Belen-Achacachi 19 I 5,2 Avichaca Belen-Achacachi 114 19 16,6 Kajchiri Saythu 27 4 14,8 1992 Chijipina Grande Belen-Achacachi 5 3 60,0 Tipampa Belen-Achacachi 4 0,0 Tacamara Belen-Achacachi 4 ° 0,0 Kella-Kella Kallutaca 49 1°6 32,6 1993 Chijipina Belen-Achacachi 39 14 35,8 Ancocagua Pucarani 68 12 17,6 Fascioliasis in cattle in the Bolivian Altiplano 79

Months Year Community Zone No. No. % Prevalence examined positive positive range

1994 Capacasi KaJlutaca 21 8 38,0 Orkojipiiia Laja 20 2 10,0 Sulkataca Laja 19 5 26,3 Laja Laja 17 2 11,7 TambiJlo TambiJlo 14 0,0 PaJlina Laja Viacha 31 1°4 45,1 TOTAL 451 100 22,1 0,0-60,0

NOVEMBER 1992 Chahuirapampa Belen-Achacachi 159 8 5,0 Kella-Kella KaJlutaca 43 17 39,5 Huacullani Tambillo 53 31 58,4 Belen Pitutas Guaqui 53 5 9,4 PaJlina Laja Viacha 17 4 23,5 1993 Ancocagua Pucarani 26 I 3,8 Chojiiacollo Pucarani 23 2 8,6 Cota-Cota Pucarani 15 3 20,0 Achica Abajo Viacha 9 I 11, I Calisaya Viacha 9 I 11, I 1994 Puchuni TambiJlo 3 I 33,3 Masaya TambiJlo 6 2 33,3 Caleria Tambillo 13 2 15,3 Andamarca Guaqui 10 0,0 Copagira Guaqui 7 ° 0,0 Humamarca Guaqui 11 °2 18,1 Chonchocoro Viacha 9 3 33,3 TOTAL 466 83 17,8 0,0-58,4

DECEMBER 1993 Kallutaca farm Kallutaca 26 13 50,0 Yanarico Tiwanaku 66 15 22,7 TOTAL 92 28 30,4 22,7-50,0

Table 3.- Prevalences of Fasciola hepatica infection in cattle from communities of the Northern Bolivian Altiplano, according to the months of the year in which the survey was carried out. Communities in which the parasite has never been detected are not included; in the few cases in which a community was surveyed two times in the same month in 2 different years, only the month survey in which more animals were examined is considered.

147)(HILLYER et al., 1996); Belen (63,4% of 77), Chira- are probably slightly higher than those detected by paca (63,3% of 30), and Viacha (LOO% of 10)(UENO et FAST-ELlSA, since some infected cattle are seronega- al., 1975). tive (HILL YER et al., 1996). This agrees with true infec- HILLYER et al. (1996) already mentioned that coprolo- tion rates obtained by necropsy in cattle coming from gical techniques underestimate real prevalences in Boli- different parts of the Northern Bolivian Altiplano and vian Altiplanic cattle by around a 30%. In a comparison sacrificed in the municipal slaughterhouse of La Paz of the efficacy of immunological and coprological tech- (FLORES SERNA & ESTEVEZ MARTINI, 1988): F. hepa- niques in detecting fascioliasis infection in bovines from tica was found in 65,7% of 944 bovines in 1975; 63,2% the Bolivian Altiplanic locality of Corapata, they sho- of 1481 in 1976; 68,7% of 1881 in 1977; 67,7% of 1729 wed that 57% of 147 cattle were positive by FAST- in 1978; and 69,1 % of 1833 in 1979. The summarized ELlSA, whereas only 26% of the same animals appear result was 67,17% of 7868 in the five-year period 1975- positive by coprology. 1979. According to these results, FLORESSERNA & Es- Adult cattle are considerably resistant to reinfection TEVEZ MARTINI (1988) concluded that in the Northern (HAROU & HILLYER, 1986) or may self-cure, as shown Bolivian Altiplano cattle prevalences are high and main- by significant drops in faecal egg counts after 20 weeks tained through time. of primary infection and by becoming egg-negative after Concerning the relationship between prevalence and 1 year of infection (DE LEO & QUINO ES, 1981). When host age (Table, 2), the above-mentioned resistance to cattle self-cure, the antibody levels decrease concur- reinfection and/or self-cure capacities of cattle may ex- rently, with a clear decline by 28 weeks of infection plain why the F. hepatica infection prevalence does not (HILLYER, SANCHEZ & DE LEON, 1985). Hence, cattle increase with age after the I-2-year-old group. seroprevalence rates may be low as a reflection of this According to the distribution of the prevalence rates self-cure and/or lack of reinfection and consequent low (total prevalences and prevalence ranges) by months antibody levels, although true infection levels in cattle (Table 3), it may be assumed that the contamination of 80 P.BUCHO et al.

Community No. animals Eggs/4 g faeces Community No. animals Eggs/4 g faeces studied range mean studied range mean

BELE -ACHACACHI ZO E: Chahuiraparnpa 252 1-5 2,0 Tacamara 176 1-70 8,6 Pugunhuyo 36 1-7 3,0 Quenaq IIitara 27 1-3 2,0 Chahuiraparnpa Chico 12 1-4 1,5 Chijipina 156 1-20 5,8 Avichaca 316 1-96 29,0 Asuntia 59 1-10 5,0 Jahuiralaca 24 2-55 16.6 Llonkoputunku 12 2-18 7,6 Chijipina Grande 16 1-7 3,0 Warisata 4 3-18 10.5 Tiparnpa 59 1-81 23,5 TOTAL 1149 1-96 12,6

HUA YROCONDO ZONE: Huayrocondo farm 248 2-23 5,6 Calasaya 33 1-49 7,2 Warisuyo 22 1-7 3,2 TOTAL 303 1-49 5,6

PUCARA I ZONE: Sehuenca 144 1-20 4,5 Pampacollo 3 I 1,0 Ancocagua 195 1-23 4,2 Oquetiti 3 I 1,0 Cohani 19 1-18 9,5 Iquiaca 10 I 1,0 Kerarani 118 I 1,0 Hospital 9 I 1,0 Chojfiacollo 124 1-30 7,8 Seba.ruyo 6 I 1,0 Cota-Cota 15 1-30 10.0 TOTAL 646 1-30 4.5

KALL TACA ZONE: Kallutaca farm 252 1-88 6,2 Ticuyo 77 1-23 9,5 Capacasi 21 1-7 3,8 Kella-Kella 153 1-30 3,9 TOTAL 503 1-88 5,9

LAJAZO E: Orkojipifia 36 2-31 7,5 Laja 25 1-13 7,0 Sulkataka 19 1-12 5,8 TOTAL 80 1-31 6,9

TAMBILLO ZONE: Puchuni 3 2 2,0 Chojasihui 29 1-9 6,2 Tambillo 50 1-2 1,5 Huacullani 210 1-20 7,2 Masaya 16 1 1,0 Caleria 43 I 1,0 TOTAL 351 1-20 5,2

GUAQUl ZONE: Andamarca 24 2-7 4,3 Jahuiraparnpa 11 1-9 4,3 Copagira 35 1-2 1,3 San Antonio 13 2-4 2,3 Belen Pitutas 182 1-16 3,2 Humamarca 45 I 1,0 TOTAL 310 1-16 2,7 rrw ANAKU ZONE: Yanarico 118 1-24 4,3 TOTAL 118 1-24 4,3

VIACHAZONE: Chonchocoro 22 1-12 5,0 Pallina Chico 17 6 6,0 Huanocollo 38 1-93 13,0 Hilata San Jose 8 I 1,0 Limani 45 1-2 1,0 Pallina Laja 113 1-11 7,0 Achica Abajo 37 5 5,0 Choquenaira farm 74 1-16 2,6 Chacoma 67 2 2,0 Calisaya 24 6 6,0 TOTAL 445 1-93 4,5

SAYTHU ZO E: Kajchiri 116 1-20 3,7 Asunta Quilhuiri 4 1,0 Tuni 18 1-17 10,0 Palomar 58 1,0 Saythu 10 1 1,0 Kella-Kella 8 3 3,0 TOTAL 214 1-20 3,2

Table 4.- lntensities measured as Fasciola hepatica egg output (number of eggs/4 g of faeces) obtained in coprological surveys on cattle from different zones and communities of the orthern Bolivian Altiplano. Only communities presenting fascioliasis-infected animals in which quantitative analyses could be performed are noted. Fascioliasis in cattle in the Bolivian Altiplano 81 the environment by eggs expelled by cattle is assured In cattle of the Northern Bolivian Altiplano, the num- throughout the year. No significant monthly prevalence ber of eggs per 4 g of faeces does not seem to be very changes throughout the year could be detected in our high, although it must not be forgotten that cattle defe- surveys, although nothing can be deduced from this be- cate a pronouncedly greater amount of stools per day cause the communities surveyed and their number per (l5-35 kg faeces/day) than other definitive animal host month were not equivalent. In this sense, UENO et al. species of the liver fluke such as sheep (1-3 kg (1975) noted that outbreaks of acute fascioliasis in do- faeces/day) (MORROS SARDA, 1967; GORTLER et al., mestic animals of the Northern Bolivian Altiplano were 1979). This means that liver fluke eggs become diluted recorded from the end of April to the beginning of Au- in such an amount of faeces, egg numbers appearing low gust, especially from May to July, or in the dry season of although in reality the number of eggs expelled by a bo- June and July. ORTUBE GOITIA (1986 in MAS-COMA et vine host per day is very high (e.g. in the community of al., 1995) gave information on the yearly chronology of A vichaca where the highest egg output was detected: 96 cattle infection by F. hepatica in the Kallutaca area, de- eggs/4 faeces = 24 eggs/g faeces, which means 360000- tecting the following prevalences by coprological analy- 840000 eggs/bovine/day). This implies that, in the Nort- ses: 9,3% in October; 15,6% in January; 42% in April; hern Bolivian Altiplano, cattle participate in the conta- 26,5% in May; 5 I % in June; 36% in July; 46,8% in Au- mination of the environment with liver fluke eggs at a gust; and 31 % in September. level similar to sheep (see MAS-COMA et al., 1997). In low altitude endemic zones, F. hepatica transmission typically shows a seasonality marked mainly by rainfall and temperature variations (see FUENTES et aI., 1998). In CO eLUSION the high altitude Northern Bolivian Altiplano, however, temperature and rainfall variations may influence liver According to the prevalence and egg output results ob- fluke transmission to a lesser extent because: tained, cattle may be considered, like sheep, a main re- -L. truncatula snails of the Northern Bolivian Altiplano servoir host of fascioliasis in this Altiplanic endemic show to be more aquatic than amphibious European zone. At any rate, compared with other animal fasciolia- snails of the same species; moreover, they inhabit per- sis endemic zones in low altitude regions of other coun- manent water collections, as opposed to their European tries and continents in which humans become infected conspecific snails which are usually found in tempo- only sporadically and isolately (see MAS-COMA, BAR- rary water bodies (OVIEDO, BARGUES & MAS-COMA, GUES & STEBAN, 1998), infection rates in Altiplanic bo- 1995b); hence, Altiplanic Iymnaeids are not so depen- vines do not appear to be high enough to explain the dent on rainfall, although the increase in size of water high infection rates detected in human subjects of the collections during the rainy season in the months of Northern Bolivian Altiplano. November to April (FuE TES et al., 1998) may give rise to an increase of Iymnaeid populations; -in the Northern Bolivian Altiplano mean daily tempera- ACKNOWLEDGEMENTS tures vary only very slightly throughout the year, whe- Sample collection and stool diagnostic techniques were funded reas they vary very pronouncedly throughout a day; at by Corporacion Regional de Desarrollo de La Paz (CORDEPAZ), any rate, minimum daily temperatures decrease mainly El Alto, Bolivia, and Danish NGO Danchurchaid-Bolivia, La Paz. during the months of May, June, July and August to le- Bolivia. vels which can be damaging for the survival of the liver The present analysis was made thanks to a Project (Contract No. fluke larval stages (FUENTES et al., 1998). TS3-CT94-0294) of the STD Programme of the Commission of the European Communities (DG XII: Science, Research and Deve- lopment). Brussels. EU, to the Programme of Scientific Coopera- Intensities tion with Latin America of the Instituto de Cooperacion Iberoame- ricana of the Agencia Espariola de Cooperacion Internacional Daily egg output per adult liver fluke is generally in- (I.C.I.-A.E.C.I.), Madrid, and to Project No.UE96-0001 of the Di- versely proportional to the intensity of the fluke burden. reccion General de lnvestigacion Cientffica y Tecnica (DGICYT), In moderate infections the daily egg output is usually Spanish Ministry of Education and Science.Madrid. P. Buchon thanks the STD Programme of the Commission of constant, whereas in heavy infections the egg output va- the European Communities (DG XII: Science, Research and Deve- ries considerably (CHE & MOTT, 1990). The egg output lopment), Brussels, EU, and the MUTlSScholarship Programme of the adult liver flukes in livestock species is relatively of the Institute de Cooperacion Iberoamericana of the Agencia Es- high. In sheep the daily egg output per fluke is depen- pafiola de Cooperacion Internacional (lCI-AECl), Madrid for fe- dent on the number of the flukes in the liver and varies llowships. This research was performed in partial fulfillment of a from 4000 to 50000 and the average numbers range from doctoral degree by P. Buchon at the Department of Parasitology of 8800 to 25 I 00 during 13 to 19 weeks after infection (BO- the University of Valencia, Spain. Miss J. Miralles, Mr. A. Franco, Mr. A. Tufiiio and other colla- RAY, 1969). These levels are much higher than those ob- borating members of Sanidad Animal -PROFOLE (La Paz, Boli- served in a highly infected sheep or bovine, whose ave- via) contributed in technical aspects. lng. A. Gallo, general respon- rage daily production is estimated to be 3000-3500 eggs sible of Programa de Fomento Lechero (El Alto, Bolivia) provided per fluke (CHE & MOTT, 1990). the necessary infrastructure and institutional support. 82 P. BUCHO et al.

The authors want to acknowledge the facilities and collaboration en la ciudad de La Paz. Cuadernos del Hospital de Clinicas, La received from the following institutions and centers, as well as Paz; 34 (2): 14-18. their respective representatives or directors: Direcci6n Nacional de FUENTES (M.V.), COELLO (J.R.), BARGUES (M. D.), VALERO Relaciones Internacionales as well as the Direcci6n Nacional de (M.A.), ESTEBA(J.G.), FONS (R.) & MAS-COMA (S.), 1997.- Epidemiologfa of the Ministerio de Previsi6n Social y Salud PU- Small mammals (Lagomorpha and Rodentia) and fascioliasis blica in La Paz; Cornite Regional de Zoonosis and Centro Piloto transmission in the Northern Bolivian Altiplano endemic zone. 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