Prevalence of flukes (Fasciola hepatica and paramphistomids) in cattle in south-eastern Mexico

In addition to the nutritional, reproductive and management aspects that limit the productivity of cattle (Vite et al., 2015), parasite damage represents an economic problem in livestock as they affect animal health and can even cause death of susceptible animals (Delafosse, 2022; Sargison et al., 2016). The adverse effects of Fasciola hepatica on milk production have been estimated at an approximate reduction of 1.37 – 1.78 kg of milk per cow per day, with losses between US$5,974.1 – 8,660.0 (Villa-Mancera & Reynoso-Palomar, 2019). In addition, in meat cattle production, the losses have been estimated at US$1.41 billion in Mexico, due to low weight gain and condemnation of livestock by-products (Rodríguez-Vivas et al., 2017). The negative effects derived from liver fluke infection affect daily weight gain, live weight and carcass weight with reductions of 9 %, 6 % and 0.6 %, respectively, although no changes have been observed in the total weight or milk production (Hayward et al., 2021).

The importance of endoparasites has been highlighted for a long time (Sardar et al., 2006) and it has been reported that gastrointestinal nematodes (GIN) have a high prevalence, especially in calves (Stromberg et al., 2015), while in adult cattle the trematodes are highly prevalent as indicated in Colombia (Pinilla et al., 2020). Of the flukes of veterinary importance, Fasciola hepatica is a cosmopolitan species with a wide presence on all continents (Jones et al., 2022; Nyirenda et al., 2019). The disease fasciolosis is caused by F. hepatica or Fasciola gigantica and together have an extensive geographic range, with a major impact on livestock (Elelu & Eisler, 2018; Naranjo-Lucena et al., 2018). In Mexico, the presence of F. hepatica in cattle has been reported for both the northeast (Munguía-Xóchihua et al., 2007) and southeast (Ojeda-Robertos et al., 2014), with highly variable prevalence reaching up to 50 % in some cases. Fasciolosis is considered an important disease because it constitutes a zoonosis and its presence has been indicated in around 70 countries with reported cases in both animals and humans (Torgerson, 2013). However, human fasciolosis has rarely been diagnosed in Mexico but a clinical report on this disease in the acute phase was reported in Puebla (Cruz y López et al., 2016).

In the trematode class, there is another group belonging to the Paramphistomidae family, which is composed of several genera that cause the disease called paramphistomidosis. These parasites affect the gastrointestinal tract, causing haemorrhagic inflammation of the intestines after excystation and subsequent migration of the juvenile fluke to the target organ. In acute cases the thickness of mucosa and submucosa of intestines occur (Atcheson et al., 2020). The presence of both species has been observed in Mexico, mainly in the tropics, where climatic conditions favour the development of gastrointestinal parasites, so the prevalence of F. hepatica and the existence of Paramphistomum cervi has been reported in Tabasco since 1989 (Rangel-Ruiz et al., 2003, 1999) and to date there are studies in the southern region of Mexico (González-Garduño et al., 2019; Ojeda-Robertos et al., 2020, 2014). However, the importance and high prevalence of rumen fluke have been indicated recently, a situation similar to that of many other countries that have evaluated the prevalence of this group of trematodes (Huson et al., 2018; Ojeda-Robertos et al., 2014; Ploeger et al., 2017).

Due to the importance of flukes in cattle health, the objective of this study was to study the risk factors and prevalence of the flukes F. hepatica and paramphistomids in cattle in south-eastern Mexico.

All applicable international, national and institutional guidelines for the care and use of animals were followed. The procedures were in accordance with the Official Mexican Standard NOM-033-SAG/ZOO-2014 on methods to kill domestic and wild animals, and NOM-051-Z00-1995 on humane treatment in the movement of animals.

The rumen fluke species identified by morphology corresponded to Cotylophoron cotylophorum and to Paramphistomum cervi (Fig. 2). In the case of P. cervi, the size was 7.75 ± 0.96 long and 2.75 ± 0.65 wide. Surface without papillae. Genital pore of gracile type with an absent genital sphincter and sphincter papilla. Acetabulum subterminal, from paramphistomum type. While in the case of C. cotylophorum the size was 6.02 ± 1.24 long and 3.40 ± 0.54 width; surface with papillae. Acetabulum subterminal, of the cotylophoron type and the terminal genitalium of cotylophoron type according to Eduardo (1985).

Fig. 2.

Rumen fluke counts

The highest counts of adult rumen flukes corresponded to 434 specimens located in cattle in Chiapas state and only 108 in Tabasco state. The average values were 41 ± 51 specimens in the positive cattle and the values broken down by sex, age and state of origin are indicated in Figure 3.

Fig 3.

In the present study, the prevalence of trematodes in Tabasco, Chiapas and Campeche states in Mexico reached 36 – 41 %, while for F. hepatica it was only 18.6 % and for rumen flukes 33.4 %. These values are at the same level as those indicated in previous studies in this area in which a prevalence of 29 % is reported for liver fluke and 27.6 % for paramphistomids, the latter with a range of 27 to 50 % (González-Garduño et al., 2020; Ico-Gómez et al., 2021). The studies with liver fluke in other countries of the American continent such as Colombia indicated 20.5 % of coprological prevalence and 41.5 % of seroprevalence (Pinilla et al., 2020) and in Peru a prevalence of 59 % was reported (Julon et al., 2020). In addition, in Argentina, a prevalence range of 40 – 80 % has been documented (Kleiman et al., 2007), while in Brazil, the rumen fluke prevalence of 26 % was indicated in a study from 1982 (Mattos & Ueno, 1996) and a similar prevalence was indicated in Venezuela (Gauta et al., 2011).

Paramphistomids also have a wide dispersion and in the last two decades reports have increased in various countries (Sanabria & Romero, 2008) even in Europe, where it is considered an emerging disease (Huson et al., 2017). Generally, high importance has been attributed to liver fluke due to its ability to infect different species of mammals, including humans, and there are generally more studies than those of rumen fluke, although the coexistence of both flukes is the result population dynamics of hosts influenced by environmental factors (Dreyfuss et al., 2014; Naranjo-Lucena et al., 2018).

Of the two rumen fluke species found in the region, P. cervi has been cited in previous studies in the same region, while C. cotylophorum has been described morphologically and recently in Camagüey, Cuba, was identified molecularly (León Companioni et al., 2020). In Mexico, is important that subsequent studies perform molecular analysis because is necessary to discriminate between the different species that have been reported in the region (González-Garduño et al., 2020).

The average counts of rumen flukes obtained in Mexico were lower (41 adult specimens) than those indicated in Iran (100 – 200 adult flukes) in slaughterhouse studies (Khedri et al., 2015). Additionally, in Spain, highest values were recorded (165 – 300 adult specimens) (González-Warleta et al., 2013). In the case of faecal egg counts, in France was observed that 19 % of bovines excreted more than 200 epg of rumen fluke (Delafosse, 2022), values higher than the average count obtained in the present study. In Spain, the mean values in excretion are close to 20 epg (González-Warleta et al., 2013). However, for F. hepatica in cattle from Argentina (Moriena et al., 2004), a small number of trematode eggs with values very similar to those indicated in the present study was reported. The prevalence of both flukes (liver and rumen flukes) depended on the type of diagnostic test performed and with sedimentation technique the highest prevalence was observed. Although it was not possible to perform diagnostic tests in blood, seroprevalence is more sensitive and therefore, of a higher value than the detection of eggs in faeces (40 % vs 20 %), as indicated by a study on F. hepatica in cattle in Colombia (Pinilla et al., 2020). The results of the faecal egg count in the region showed that 18.6 % of the adult animals were infected. However, it could be a higher percentage since some were not detected with this technique, which can have 59 to 68 % sensitivity (Carneiro et al., 2018). In slaughterhouse studies show a higher prevalence for F. hepatica due to the presence of eggs in the bile content (39.4 %) and lower prevalence due to the presence of adult parasites in the bile ducts (32.4 %) and the egg count (15.5 %) in faeces (Giraldo Forero et al., 2016). However, studies in slaughterhouses show a great variability in results with values as low as 12 % and up to 30 % with the condemnation of livers due to the presence of F. hepatica (Hernández-Guzmán et al., 2021). The low prevalence of F. hepatica (1 %) in the slaughterhouses of the present study can be associated with the fact that they were the result of samplings carried out at fixed times and not of the systematic registration of all animals that entered the slaughterhouses. In addition, many of the animals destined for slaughter have come from feedlots where they were previously dewormed and therefore, less likely to carry adult parasites. In the case of rumen fluke, the diagnosis in faeces (42 %) was higher than prevalence of adult parasites in the rumen of sacrificed animals (26.7 %), as previously indicated.

Of the risk factors, the land physiography (landform including topography, water and soil) is very important in the presence of parasitic diseases, both for fasciolosis and for paramphistomosis. In the farms located in flat areas prone to flooding with soils with a high proportion of clay, the probabilities of occurrence of F. hepatica were 16 times higher than in hilly areas. In the case of rumen flukes, there was a five times greater probability of infection in flood-prone areas than in the hills. Environmental conditions have been considered as one of the main factors affecting the distribution of F. hepatica (Hernández-Guzmán et al., 2021), among which the type of soil, precipitation and altitude stand out (Jiménez-Rocha et al., 2017), as confirmed by a study in Bangladesh (Khan et al., 2017). These factors affect the distribution of both liver and rumen flukes and their intermediate host, snails of species as Galba truncatula (Jones et al., 2022) Lymnaea glabra (Dreyfuss et al., 2014; Naranjo-Lucena et al., 2018) and in Mexico the presence of Fossaria humilis and F. bulimoides (Cruz-Mendoza et al., 2004) is related with the presence of F. hepatica. However, for rumen fluke it is necessary to determine the intermediate host species related to the highest occurrence. In addition to environmental conditions, another author attributes the high prevalence of trematodes to a lack of prevention and control strategies in the bovine population (Pinedo et al., 2010).

In the place of origin, differences were observed in the prevalence of both trematodes, which is the result of multiple factors that affect the presence of the parasite, as suggested by studies that address the diagnosis of these trematodes (Hernández-Guzmán et al., 2021; Jiménez-Rocha et al., 2017; Jones et al., 2022; Naranjo-Lucena et al., 2018).

Females presented higher prevalence than males because this last receive different health and nutritional management that females, especially when they are destined for slaughter. In relation to age, the results of this study indicate a higher prevalence in adult animals, which is consistent with the study carried out by Moriena et al. (2004) in Argentina, whose results indicate that the prevalence rate increased in direct proportion to the animals’ age. Additionally, in Colombia, bovines older than two years of age had a five times greater risk of presenting these parasites than younger animals (Pinilla et al., 2020). The low prevalence found in young cattle has been associated in principle with the long prepatent period of F. hepatica (12 weeks), so the presence of eggs in faeces could be higher in adult animals, due to the probability of infection increases in grazing (Livia-Córdova et al., 2021). In addition, in the case of rumen fluke, the effectiveness of anthelmintics is much lower than in the case of F. hepatica (Ico-Gómez et al., 2021). It may be one of the reasons why the prevalence results are higher for this group of parasites. In addition, other studies should be conducted to determine the influence of the host on the prevalence of paramphistomidosis.