Identifying digital dermatitis infection reservoirs in beef cattle and sheep

Abstract

Digital dermatitis (DD) is a superficial infectious dermatitis of the digital skin of cattle and sheep that can be very painful, causing severe lameness in affected animals. Bovine digital dermatitis (BDD) in dairy cattle has now been reported in most countries they are farmed, and DD in sheep, known as contagious ovine digital dermatitis (CODD) is rapidly emerging as a severe infectious foot disease since first reports from the UK in 1997. Spirochaetes, of the genus Treponema have frequently been found in large numbers in BDD lesions and are now considered the primary causative bacteria of BDD. Three treponeme phylogroups are consistently isolated from dairy cattle BDD in the UK and the USA, which are known as Treponema medium- like, Treponema phagedenis- like spirochaetes and Treponema pedis. Over the past 40 years research has focused on dairy cattle BDD and overlooked whether the disease exists in beef cattle herds in the UK, and whether the same aetiological agents are causal. There is also limited information on the causative bacteriological agents of CODD. Furthermore, no definitive transmission routes or infection reservoirs of DD in either cattle or sheep had thus far been delineated, with only a single study finding a potential reservoir site of DD treponemes in the dairy cattle gastrointestinal (GI) tract. Using molecular bacteriological studies it was found that CODD and beef cattle BDD, as in dairy cattle BDD, show a high association with the three DD treponeme phylogroups. All CODD and beef BDD lesions investigated had at least one of the three DD treponeme phylogroups present in the lesions and these treponemes were also isolated from a high proportion of lesions. No DD treponemes were detected in healthy sheep or beef cattle foot tissue. Upon 16S rRNA gene sequence analysis all isolates showed a high similarity, if not 100% identity, to representatives of each treponeme phylogroup isolated from dairy cattle BDD lesions, indicating a shared aetiology between DD in all three animals. Additionally, the same treponeme bacteria were detected and isolated from a new undefined foot disease in dairy goats in the UK indicating that cross-species transmission of DD may have occurred causing DD infection in a previously unaffected domestic livestock species. To understand potential transmission routes and infection reservoirs of DD, the host GI tract and hoof trimming equipment were investigated. Of the sheep gingival (n= 40) and rectal tissues (n= 40), 1/40 gingival tissues were positive for DD- associated treponemes (T. pedis), and 3/40 rectal tissues (one containing T. medium- like and two tissues containing T. pedis). No DD- associated treponeme DNA was amplified from beef cattle rectal tissues (n= 40), however 4/40 beef gingival tissues were positive for DD- associated treponemes (all containing T. phagedenis- like). A T. phagedenis- like DD treponeme was isolated from the rectal tissue of a CODD symptomatic sheep. Beef cattle (n= 41) and sheep (n= 79) faeces failed to amplify DD- associated Treponema DNA. Twenty two treponemes were isolated from sheep faeces; however, upon phylogenetic analysis these clustered with considered non-pathogenic treponemes, which interestingly exhibited farm specific diversity in their 16S rRNA gene. Trimming equipment was tested after being used to trim cattle and sheep hooves, and subsequently after disinfection of equipment. Of the blades used to trim DD symptomatic animals (n= 26, cattle and sheep combined), 25/26 were found to be positive for at least one of the DD Treponema phylotypes. This figure was reduced to 10/26 (38%) after disinfection of the blades. Following culture of a swab, an isolate belonging to the T. phagedenis- like spirochaetes was isolated from a knife sample after trimming a DD positive cow. Beef cattle sera from DD positive and negative farms were investigated to understand whether beef cattle’s perceived lower prevalence of BDD in the UK is due to a lack of exposure to treponemes, or a protective immune response. Beef cattle from DD positive farms appeared to produce a strong immunological response to treponemes, compared with DD negative farm animal sera. Therefore the perceived lower prevalence of DD in beef cattle does not appear to be due to a protective response in these animals, but more likely due to a lack of exposure to DD treponemes. In conclusion, these studies have produced vital information describing DD in beef cattle and sheep and their respective aetiological agents allowing for more appropriate treatments in the future. Additionally, given the two potential transmission routes delineated from the data, effective actions can be taken to prevent the spread of DD within current hosts and to limit emergence into yet unknown additional host species