Our study found evidence of F. hepatica infection on 4 out of 5 farms in the major milk producing province in Cuba. Moreover, this infection was not only highly prevalent, but also significantly associated with decreases in milk yield.
In previous abattoir-based studies in Cuba, F. hepatica parasites were observed to be present between 20 and 50% of the animals. However, the latter studies were conducted at the individual cow level [14, 15] and in a different geographical region of Cuba. Moreover, it is known that meat inspection at the slaughterhouse has a lower sensitivity than serology-based methods [16].
The evidence of widespread F. hepatica infection in Cuban dairy herds, together with the known deleterious effects of F. hepatica on animal welfare and productivity suggest than these infections should be considered of major importance in Cuban dairy farms. However, on high-input, intensive, Holstein-pedigree farms, milk production per cow per year was more than 6 times that of the Cuban mixed breed cattle studied here. Cuban cattle are not genetically capable of achieving such high levels of milk production, they eat a less nutritious diet and, in subtropical climates, they often face higher parasite burdens. Because Cuban cattle are likely under lower metabolic stress than their European counterparts in intensive production systems, it could be proposed that parasite-ascribed decreases in milk production in Cuba should be lower than, for example, in Europe. However, in the UK, in high yielding herds, F. hepatica – associated decreases were estimated at 15% [4], compared to estimated decreases of 18% to 32% in the present study. The Cuban estimate is substantially higher than the 3% reduction described in Belgium in herds with high ODR [11] and the 6% in Spanish herds with high infection levels [13]. Partly, these differences may be ascribed to the fact that we did not control for some confounding factors, such as lactation stage, age composition or somatic cell count data in our analysis. This was not possible, as these data are not routinely collected in Cuban dairy farms. Therefore, further elucidation of the true and recoverable production impact would require an intervention trial using anthelmintic treatment under field conditions [17].
The impact of parasite infections on food security may be more keenly felt in countries where demand is already outstripping supply. At the same time, options for control are likely to be more limited in subtropical systems. For example, with very few water sources available, options for pasture rotation are limited. In Cuba, anthelmintic treatments for F. hepatica are not used routinely either because of a lack of availability in the Cuban market and/or a lack of diagnostic routine. This study made a start with the identification of risk factors, which should aid in the development of control recommendations for the Cuban dairy sector. Different farming systems had different ODR levels. UEB farms, which are normally the larger farms, with more extensive access to suitable habitats for lymnaeid snails, had higher ODRs. Similarly, farms with a higher number of hectares available had higher ODRs. In Denmark, larger dairy herds were also more prone to F. hepatica infection [18]. In Turkey and Tanzania, large-scale and traditional (stationary herds without effective disease control) dairy farms presented higher prevalence of Fasciola sp. than small-scale farms [19, 20]. This may be related to intensively grazed pastures and to an increased likelihood of cattle encountering fluke-contaminated snail habitats on larger farms.
Access to suitable habitats for lymnaeid snails, usually man-made ponds of stagnant water used to water cattle, indeed appears to be an important factor contributing to higher levels of infection. In this study, farms with less grass as a proportion of the total diet, available during the dry season, had significantly higher antibody titers. On these farms, cattle will normally be congregated around these habitats for lymnaeid snails and receive supplementation with other food sources, such as sugar cane byproducts. They will therefore have increased contact time with metacercaria-contaminated snail-infested areas. Access to, and type of, water sources could be the key overriding factor in fluke transmission in Cuba. This may be an important area to focus on in terms of limiting losses to the parasite.
Grazing alongside horses was not a significant risk factor whereas, in agreement with other studies [21], co-grazing with small ruminants clearly increased the risk of higher ODR levels.
There were significant differences in ODR levels between municipalities. The reason for this could include local environmental differences as well as differences in local farm management practices [22]. In the UK, McCann, Baylis and Williams [23] detected rainfall as the main responsible factor of variation (23%) in F. hepatica BTM antibody levels, whilst farm management explained about 21% of variation. Bennema et al. [24] found that in regions with relatively homogenous climatic and environmental conditions, management factors are the primary factors determining F. hepatica infection risk. Further research is recommended to determine the importance of water source as well as of infection and the local environmental (soil type, local pasture, infection with other parasite, bacterial interactions, landscape features) and climatic conditions affecting the infection risk. Moreover, it is necessary to evaluate the impact of host factors such as age and genetic make-up. Ultimately, this could result in local risk maps and evidence-based and practical management recommendations such as sanitation of pastures and water sources and targeted anthelmintic treatment during periods of highest infection pressure [24, 25].