Equines as reservoirs of human fascioliasis: transmission capacity, epidemiology and pathogenicity inFasciola hepatica-infected mules

Abstract

Fascioliasis is a zoonotic disease caused by liver flukes transmitted by freshwater lymnaeid snails. Donkey and horse reservoir roles have been highlighted in human endemic areas. Liver fluke infection in mules has received very limited research. Their role in disease transmission, epidemiological importance and Fasciola hepatica pathogenicity are studied for the first time. Prevalence was 39.5% in 81 mules from Aconcagua, and 24.4% in 127 from Uspallata, in high-altitude areas of Mendoza province, Argentina. A mean amount of 101,242 eggs/mule/day is estimated. Lymnaeids from Uspallata proved to belong to ribosomal DNA internal transcribed spacer (ITS) markers ITS-1 and ITS-2 combined haplotype 3C of Galba truncatula. These lymnaeids were experimentally susceptible to infection by egg miracidia from mules. Infectivity, number of cercariae/snail and shedding period fit the enhanced F. hepatica/G. truncatula transmission pattern at very high altitude. This indicates that the mule is able to maintain the F. hepatica cycle independently. Individual burdens of 20 and 97 flukes were found. Mule infection susceptibility is intermediate between donkey and horse, although closer to the latter. Anatomo-pathology and histopathology indicate that massive infection may cause mule death. Haematological value decreases of red blood cells, haemoglobin, leucocytes and lymphocytes indicate anaemia and strong immunosuppression. Strongly increased biochemical marker values indicate liver function alterations. The mule probably played a role in the past exchanges with Chile and Bolivia through Mendoza province. Evidence suggests that mules could contribute to the spread of both F. hepatica and G. truncatula to human fascioliasis-endemic areas in these countries.

Fascioliasis in Llama, Lama glama, in Andean Endemic Areas: Experimental Transmission Capacity by the High Altitude Snail Vector Galba truncatula and Epidemiological Analysis of Its Reservoir Role

“…The bile ducts of South American camelids show more similarity with the equine bile system than with the bile system of domestic ruminants [ 105 ]. Despite this, the histopathological picture of fascioliasis in llamas suggests a low resistance to liver fluke infection and has been reported to be more similar to that in sheep [ 99 , 100 , 106 ] than to that in equines [ 107 ]. Indeed, F. hepatica infection is a common cause of production loss and mortality in domesticated New World camelids [ 44 , 55 , 57 , 58 , 108 ].…”

“…However, it should be considered that llamas may play a disease-spreading role if used as pack animals in rural areas ( Figure 7 D,E and Figure 8 ), as already highlighted in the case of donkeys [ 25 ] and mules [ 107 ], the latter two with a capacity to transport pronouncedly higher weights of goods [ 111 ]. Such a fascioliasis-spreading capacity poses a problem for the implementation of a One Health initiative, because pack animals may give rise to movements of the parasite and the vector from one part to another of the zone selected for control intervention, or the introduction of the parasite and/or the vector from outside into that zone.…”

Donkey Fascioliasis Within a One Health Control Action: Transmission Capacity, Field Epidemiology, and Reservoir Role in a Human Hyperendemic Area

“…If presenting a high immunological refractory response, liver flukes will survive less time inside that host and the contribution to transmission will consequently be restricted in quantity and time, as is the case of several cattle races. Fascioliasis is known to be different in equines and ruminants from the pathogenicity point of view, with the horse as the most resistant, the donkey as the most susceptible, and the mule showing intermediate profile although closer to those of the horse (90). Indeed, F. hepatica infection has been reported to be fatal for donkeys (86), and the pathology caused by a F. gigantica infection in donkeys has already been analyzed post-mortem in Egypt (91).…”

“…In mules, it was observed that a massive infection by 97 adult flukes was highly pathogenic and finally fatal, and that the maximum daily output was 794,500 eggs/mule/day (90).…”

“…Thus, although the main introduction purpose was the in-situ production of mules, donkeys easily adapted to the hypoxic conditions of the high altitude environments of the Andean valleys and altiplanos, where they were increasingly used by the high altitude communities because of the lower adaptation capacity of horses (95). The biochemical and hematological parameters in mules at high altitude have recently been assessed (90), and in donkeys the respective reference intervals have also been established (96), including the Creole donkey in South America (97). However, the analysis of these parameters in high altitude for Andean donkeys is still pending.…”