Prevalence of Fasciola giganticainfection in slaughtered animals in south-eastern Lake Chad area in relation to husbandry practices and seasonal water levels

Fasciolosis is a parasitic disease of herbivorous mammals caused by trematodes of the genus Fasciola. In livestock, it causes severe reductions in milk and meat yield as well as losses due to decreased fertility [1, 2]. The host animals become infected with Fasciola metacercariae when they ingest contaminated vegetation close to or within water bodies. Swamp areas and seasonally flooded areas at the borders of Lake Chad provide an optimal habitat for the parasites and the intermediate hosts, which are freshwater snails of the family Lymnaeidae.

In sub-Saharan Africa, infections with Fasciola gigantica have often been described [2–5]. In the Lake Chad area, two previous studies from Niger and Cameroon [6, 7] have described the disease, but there is no publication from the Chadian side of the lake. Fasciola gigantica has been reported in Chadian cattle and small ruminants in a Central African study of wild ruminants [8] and in a treatment study on Chadian cattle [9]. Fasciola hepatica infection has not been reported in Chad.

Fasciolosis is perceived as a significant animal health problem by the mobile pastoralist population in the south-eastern Lake Chad area, particularly since other diseases like bovine pleuropneumonia, against which vaccination is compulsory, are better controlled. Most pastoralist camp leaders expressed concerns about their animals grazing on contaminated pastures in close proximity to water bodies of Lake Chad during a participatory research needs assessment [10]. Some pastoralists are aware that it is possible to treat animals for liver flukes with anti-parasitic drugs, but access to quality drugs is difficult in the remote zones [11].

The majority of the income for mobile pastoralists in this area is generated by selling milk and animals at local markets [12], so the adverse economic impact of fasciolosis is of primary importance. The mobile pastoralists observe the parasites when they slaughter animals and are aware that this is a cause of reduced milk production and body weight. This study was initiated to investigate the mobile pastoralists’ priority concern of fasciolosis in their livestock.

Fasciola gigantica specimens (n = 11) measured between 2 and 5 cm, with a mean size of 3.2 cm.

Among all positive animals (n = 200), 53% (n = 106) were classified as lightly infected (1-10 parasites), 18% (n =36) as moderately infected (11-100 parasites) and 29% (n = 58) as heavily infected (> 100 parasites). In cattle, 19% of infections (n = 17) were light, 20% (n = 18) moderate and 61% (n = 54) heavy; in goats, 80% (n = 65) were light, 17% (n = 14) moderate and 2% (n = 2) heavy; and in sheep, 80% (n = 24) light, 13% (n = 4) moderate and 7% (n = 2) heavy. There was a significant difference between the degree of infection in cattle and small ruminants. Sheep and goats had very similar prevalence and burdens.

The prevalence in cattle in Sidje, the slaughter slab closest to Lake Chad, was significantly higher than in Gredaya (p = 0.003). Seasonal trends indicate a lower prevalence between the months of August to October, comprising the rainy season, compared to the rest of the year in all species.

Geospatial distribution

The prevalence rates were plotted according to the coordinates of the villages of origin to show the geospatial distribution of animals and the proportion of positive animals. The size of the circle corresponds to the number of animals originating in each village (Figure 2 shows the data for goats, data for cattle are shown in Additional file 1: Figure S1, data for sheep are shown in Additional file 2: Figure S2). There is a notable relationship between proximity to the lake and infection with F. gigantica in all three species.

This is the first publication on Fasciola infection in cattle, sheep and goats in the Lake Chad area of Chad. The results support a relationship between the infection of livestock with F. gigantica and the ethnic group of the livestock holder. The ethnic group likely serves as a proxy for the type of animal husbandry practiced [10]. The Kouri cattle, which were kept on islands in the lake, were 100% positive for F. gigantica. Although the sample size was very small (n = 6), nonetheless there was clearly a high prevalence in these animals. The livestock kept by Peul, who utilise pastures close to the lake and its seasonal extensions, also showed a high prevalence (55% overall, 95% for cattle). In contrast was the low prevalence found in the Gorane and Kanembou livestock. The Gorane pastoralists do not move close to the lake, but stay in drier areas to the east. The Kanembou culture and husbandry practices are, in general, similar to the Gorane, although in the study zone, the majority of Kanembou were sedentary rather than mobile. The prevalence found in Arab livestock ranged in between that found in the other ethnic groups (Kouri/Peul and Gorane/Kanembou). This finding is supported considering that Arab cattle breeders in the zone were semi-nomadic, only moving their animals towards the lake at the end of the dry season, when the pastures around their villages were depleted.

There was a notable relationship between proximity to the lake and infection with F. gigantica in all three species. The geospatial distribution and the analysis of grazing patterns strongly suggest that Lake Chad is the source of infection. This would also explain the observed seasonal trend, which is likely due to migration away from the lake during the rainy season when grass is more widely available, potentially reducing exposure to the contaminated areas close to the lake. Further research is currently continuing to establish the seasonal dynamics of F. gigantica. The results of this study support a strong recommendation, for Kouri and Peul livestock, for treatment against F. gigantica infection with an initial prophylactic dose when entering the lake region and a second dose at the beginning of the rainy season, or when leaving the area. This type of programme could reduce pasture contamination and the effects on livestock productivity, particularly for Arab livestock that is not continuously grazed near the lake. In contrast, no preventive treatment is necessary for Gorane and Kanembou livestock that are grazed in areas not near the lake. Because they are not in proximity to open water, these animals have a negligible risk of infection. Our recommendation is in line with that of the local veterinarian in the Gredaya administrative district, who recommended treatment every three months as long as animals were kept near the lake.

It was noted that prevalence and degree of infection differ between species. This is likely due to feeding patterns as well as specific husbandry practices. Small ruminants avoid wet areas, instead preferring to graze and browse on dry ground. However, grazing dry pastures is not completely protective, as Fasciola metacercariae can remain viable for some time on vegetation and in some of the intermediate host snails of the genus Lymnaea in previously flooded areas [13, 14]. Pastoralists in the study area reported that they kept their small ruminants away from the more humid areas near the water as long as possible to decrease the risk of infection, as also noted by Tager-Kagan in the 1970s [6].

In this study, sheep and goats had comparable infection intensities. The similar burden in sheep and goats could indicate similar susceptibility to infection and/or result from use of comparable feeding areas. Although sheep commonly graze ground cover, while goats typically browse shrubs and trees, the Lake Chad region is now densely populated with herds and subject to increased agricultural cultivation, so there are relatively few shrubs, particularly at the end of the dry season.

The higher prevalence noted in cattle at the slaughter slab in Sidje is likely because many Peul pastoralists pass by this village when leaving the lake or stay nearby during the rainy season.

In this study, meat inspection was performed according to the routine local inspection procedure, which consisted of one long transverse cut in the liver along the bile ducts. The method of examination was a limitation to this study in that it provided only a semi-quantitative measurement of the parasite burden. While it would have been ideal to examine the entire organ by cutting it into small pieces to visualise all biliary ducts, the cost to purchase every liver precluded such a method. Using the standard meat inspection approach, it is possible that some animals with few parasites might have been misclassified as not infected. Also, particularly in cattle due to the large liver size, multiple incisions might have shown a higher number of parasites. Therefore, the prevalence and degree of F. gigantica infection intensity might have been underestimated using the standard, locally available, semi-quantitative evaluation method employed in this study, but the exposure patterns revealed are nonetheless significant and valid, despite a potentially decreased sensitivity of this method.

Although fasciolosis is increasingly being recognised as a human public health issue [15, 16], there is very little literature on F. gigantica from Chad or the Lake Chad region, with the most recent dating from the late 1970s [6–8]. At that time, the recommended control measure was routine deworming treatment of livestock once or preferably twice per year, before and after the rainy season [6, 9]. Based on the results of the present study, this recommendation should still be implemented for herds grazing near Lake Chad. Further cost-benefit analysis is warranted, as findings would provide evidence for information campaigns and policy development. It is also recommended to assess pastoralist’s access to and the quality of available treatments for fasciolosis in remote areas.

This research quantifies the prevalence of F. gigantica in slaughtered livestock in south-eastern Lake Chad area and provides a semi-quantitative assessment of the burden of infection.

The results showed that animals which had grazed in close proximity to the lake and its seasonal extensions had a high risk of infection. Cattle of Peul and Kouri ethnic groups were most affected. These groups keep their animals at the shore of Lake Chad or on islands within the lake.

The study confirms the pastoralists’ perceptions of disease priorities with fasciolosis as an important health problem.

Treatment against fasciolosis is recommended for animals grazing near or at the lake, and further economic analysis of such treatment is warranted.

The data set supporting the results of this article is available in Additional file 3.