Knowledge, practices, and epidemiology of bovine fasciolosis in smallholder farming areas of South Africa

Abstract

Bovine fasciolosis (infection with Fasciola species) causes morbidity and mortality in cattle and has zoonotic implications and deleterious economic effects, especially on smallholder cattle farmers. The smallholder farmers’ level of knowledge and practices about bovine fasciolosis are not known in communal farming areas of Northwest province. Additionally, the prevalence of bovine fasciolosis, haematochemical changes caused by fasciolosis in cattle, and the species identity and genetic diversity of Fasciola species infection in cattle are not known in the communal farming areas of Northwest province, South Africa. The broad objective of this study was to establish the molecular epidemiology of bovine fasciolosis in the communal farming areas of Northwest province, South Africa. The knowledge, attitudes, and practices concerning bovine fasciolosis among smallholder cattle farmers (n = 153) were determined in three villages of the Moretele Local Municipality in Bojanala District, North West Province of South Africa using a structured questionnaire. As a follow-up, a cross-sectional study was conducted to determine the occurrence of bovine fasciolosis in cattle (n = 277) using the sedimentation technique, real-time polymerase chain reaction (qPCR), and faecal antigen enzyme-linked immunosorbent assay (Ag ELISA) in five villages of the Moretele Local Municipality in Bojanala District, North West Province. Furthermore, the effect of Fasciola species infection on haematological and biochemical parameters was determined in communally grazed cattle using Auto (ADVIA® 120 Hematology system). Lastly, Fasciola species were characterised in infected communally grazed cattle by sequence analysis of the nuclear ribosomal internal transcribed spacer 2 (ITS-2 gene) and the mitochondrial cytochrome oxidase 1 (CO1) regions. No evaluated factors were significantly associated with a positive fasciolosis epidemiological knowledge score. Education level (P = 0.046), cattle breeds being reared (P = 0.022), and management system (P < 0.001) of the smallholder farmers were associated with a positive practice score concerning bovine fasciolosis prevention. Only 73 (26.40 %) cattle were positive using the qPCR assay while 36 (13.00 %) were positive using the sedimentation technique, though with low feacal egg counts. All cattle samples were negative for bovine fasciolosis using faecal Ag ELISA. Location, breed, sex, age, and faecal consistency score did not affect cattle’s qPCR positivity to bovine fasciolosis (p>0.05). The egg per gram load of Fasciola correlated significantly (P < 0.05) with the RBC, Hb, and PCV in Fasciola-infected cattle. There was a decrease in glutamate dehydrogenase and an increase in gamma-glutamyl transferase in the infected compared to non-infected cattle. A total of 30 (41.1%) of the 73 PCR positive cattle were infected with F. hepatica, 25 (34.2%) with F. gigantica, and 18 (24.7%) with both species. Fasciola hepatica ITS-2 sequences are grouped into two different clusters, one cluster with reference sequences from China, Libya, and Peru and the other cluster with a sequence from Spain. The F. gigantica ITS-2 sequences grouped in one cluster together with sequences from sheep from Libya and cattle from Chad. The F. gigantica CO1 sequences grouped with F. gigantica sequences from Zimbabwe, while F. hepatica CO1 sequences grouped with F. hepatica sequences from sheep and cattle from Japan, Tunisia, Austria, and Ecuador. It was concluded that farmers in the study area generally possessed poor epidemiological knowledge and their educational status and system of management influenced their adoption of satisfactory practices of prevention and control of bovine fasciolosis. The prevalence of fasciolosis was relatively high, especially using the qPCR method. Patent Fasciola infection was associated with a relative decrease in the values of most of the haematochemical indices but did not significantly alter the erythrogram, leucogram, and serum chemistry of communal cattle. There was co-infection of both F. hepatica and F. gigantica in cattle in the study areas which may be indicative of future Fasciola species hybridization.