Iranian Journal of Veterinary Surgery

Iranian Journal of Veterinary Surgery

Molecular Isolation of Treponema spp from Ovine Footrot Lesions, Finding Evidence for Contagious Ovine Digital Dermatitis

Document Type : Original Article

Authors
1 Resident of Veterinary Surgery, Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran.
2 Department of Pathobiology, Faculty of Veterinary Medicine, Shahrekord University, Shahrekord, Iran.
3 Department of Clinical Sciences, Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran.
Abstract
Contagious ovine digital dermatitis (CODD), a severe lameness-causing bacterial foot disease, significantly impacts the sheep industry's economy and welfare. Treponema species responsible for bovine digital dermatitis (BDD), including Treponema medium, Treponema phagedenis, and Treponema pedis, have been identified in CODD lesions. In this study, Treponema spp. was detected in 42 skin samples from 110 sheep that had footrot lesions (38%). The lesions were more presented on hindlimbs (55.5%). The Kurdish sheep breed exhibited the highest Treponema positivity rate with 47.8% (n = 20), while pure Afshari sheep and Afshari-Kurdish hybrids showed an equal prevalence of 26.2%. The prevalence of lesion scores 4 and 5 in the Treponema-positive group (33.3% and 40.5% respectively) was significantly higher compared to the Treponema-negative group (23.5% and 11.8% respectively) further underscores the potential role of Treponema infection in the progression of severity of the infection. The southern region of the Khorasan Razavi province exhibited a significantly higher prevalence of Treponema-positive cases (88.1%, n = 37) compared to the northern regions (7.1%, n = 3) and Mashhad (4.8%, n = 2). This is the first report of investigation of the possible presence of CODD in Iranian sheep flocks, which should be potentially considered to prevent negative impacts on sheep production, welfare, and antibiotic use (improper antibiotic usage) in the farms.
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  1. Duncan JS, Angell JW, Carter SD, Evans NJ, Sullivan LE, Grove-White DH. Contagious ovine digital dermatitis: an emerging disease. The Veterinary Journal. 2014; 201: 265-268. doi: 10.1016/j.tvjl.2014.06.007
  2. Harwood D, Cattell J. Virulent foot rot in sheep. Veterinary Record. 1997; 141(3): 83.
  3. Angell JW, Duncan JS, Carter SD, Grove-White DH.  Farmer reported prevalence and factors associated with contagious ovine digital dermatitis in Wales: a questionnaire of 511 sheep farmers. Preventive Veterinary Medicine. 2014; 113: 132-138. doi: 10.1016/j.prevetmed.2013.09.014
  4. Dickins A, Clark CCA, Kaler J, Ferguson E, O’Kane H, Green LE.  Factors associated with the presence and prevalence of contagious ovine digital dermatitis: a 2013 study of 1136 random English sheep flocks. Preventive Veterinary Medicine. 2016; 130: 86-93. doi: 10.1016/j.prevetmed.2016.06.009
  5. Tegtmeyer PC, Staton GJ, Evans NJ, Rohde J, Punsmann TM, Ganter M. First cases of contagious ovine digital dermatitis in Germany. Acta Veterinaria Scandinavica. 2020; 62: 46.  doi: 10.1186/s13028-020-00544-0
  6. Bernhard M, Frosth S, König U. First report on outbreaks of contagious ovine digital dermatitis in Sweden. Acta Veterinaria Scandinavica. 2021; 63: 29. doi: 10.1186/s13028-021-00595-x
  7. Alsaaod M, Schmid RM, Zwahlen N, Soto Martin S, Wildi N, Seuberlich T, Steiner A. First case description of contagious ovine digital dermatitis in Switzerland. Schweizer Archiv für Tierheilkunde. 2022; 164: 851-859. doi: 10.17236/sat00378
  8. Angell JW, Blundell R, Grove-White DH, Duncan JS.  Clinical and radiographic features of contagious ovine digital dermatitis and a novel lesion grading system. Veterinary Record. 2015; 176: 544-544. doi: 10.1136/vr.102978
  9. Wassink GJ, Moore LJ, Grogono-Thomas R, Green LE. Exploratory findings on the prevalence of contagious ovine digital dermatitis in sheep in England and Wales during 1999 to 2000. The Veterinary record. 2003; 152: 504-506. doi: 10.1136/vr.152.16.504
  10. Duncan JS, Grove-White D, Moks E, Carroll D, Oultram JW, Phythian CJ, Williams HW.  Impact of footrot vaccination and antibiotic therapy on footrot and contagious ovine digital dermatitis. Veterinary Record. 2012; 170: 462-462. doi: 10.1136/vr.100363
  11. Phythian CJ, Cripps PC, Grove-White D,  Jones PH, Michalopoulou E, Duncan JS. Observing lame sheep: evaluating test agreement between group-level and individual animal methods of assessment. Animal Welfare. 2013; 22: 417-422. doi: 10.7120/09627286.22.4.417
  12. Collighan RJ, Naylor RD, Martin PK, Cooley BA, Buller N, Woodward MJ. A spirochete isolated from a case of severe virulent ovine foot disease is closely related to a treponeme isolated from human periodontitis and bovine digital dermatitis. Veterinary Microbiology. 2000; 74: 249-257. doi: 10.1016/S0378-1135(00)00190-5
  13. Naylor R, Martin P, Jones J, Burnell MC.  Isolation of spirochaetes from an incident of severe virulent ovine footrot. The Veterinary Record. 1998; 143: 690.
  14. Sayers G, Marques PX, Evans NJ, O'grady L, Doherty ML, Carter SD, Nally JE. Identification of spirochetes associated with contagious ovine digital dermatitis. Journal of Clinical Microbiology. 2009; 47(4): 1199-1201. doi: 10.1128/jcm.01934-08
  15. Angell JW, Crosby-Durrani HE, Duncan JS, Carter SD, Blundell R.  Histopathological characterization of the lesions of contagious ovine digital dermatitis and immunolabelling of treponema-like organisms. Journal of Comparative Pathology. 2015; 153: 212-226. doi: 10.1016/j.jcpa.2015.10.178
  16. Sullivan LE, Clegg SR, Angell JW, Newbrook K, Blowey RW, Carter SD, Bell J, Duncan JS, Grove-White DH, Murray RD, Evans NJ.  High-level association of bovine digital dermatitis Treponema spp. with contagious ovine digital dermatitis lesions and presence of Fusobacterium necrophorum and Dichelobacter nodosus. Journal of Clinical Microbiology. 2015; 53: 1628-1638. doi: 10.1128/jcm.00180-15
  17. Sullivan LE, Evans NJ, Blowey RW, Grove-White DH, Clegg SR, Duncan JS, Carter SD.  A molecular epidemiology of treponemes in beef cattle digital dermatitis lesions and comparative analyses with sheep contagious ovine digital dermatitis and dairy cattle digital dermatitis lesions. Veterinary Microbiology. 2015; 178: 77-87. doi: 10.1016/j.vetmic.2015.04.011
  18. Evans NJ, Blowey RW, Timofte D, Isherwood DR, Brown JM, Murray R, Paton RJ, Carter SD.  Association between bovine digital dermatitis treponemes and a range of ‘non-healing’ bovine hoof disorders. Veterinary Record. 2011; 168: 214-214. doi: 10.1136/vr.c5487
  19. Staton GJ, Angell JW, Grove-White D, Clegg SR, Carter SD, Evans NJ, Duncan JS. Contagious ovine digital dermatitis: a novel bacterial etiology and lesion pathogenesis Contagious ovine digital dermatitis: A novel bacterial etiology and lesion pathogenesis. Frontiers in Veterinary Science. 2021; 8. doi: 10.3389/fvets.2021.722461
  20. Frosth S, König U, Nyman AK, Pringle M, Aspán A. Characterisation of Dichelobacter nodosus and detection of Fusobacterium necrophorum and Treponema spp. in sheep with different clinical manifestations of footrot. Veterinary Microbiology. 2015; 179: 82-90. doi: 10.1016/j.vetmic.2015.02.034
  21. Winter AC. Lameness in sheep. Small Ruminant Research. 2008; 76: 149-153. doi: 10.1016/j.smallrumres.2007.12.008
  22. Witcomb LA, Green LE, Kaler J, Ul-Hassan A, Calvo-Bado LA, Medley GF, Grogono-Thomas R, Wellington EM.  A longitudinal study of the role of Dichelobacter nodosus and Fusobacterium necrophorum load in initiation and severity of footrot in sheep. Preventive Veterinary Medicine. 2014; 115: 48-55. doi: 10.1016/j.prevetmed.2014.03.004
  23. Zhou H, Bennett G, Hickford JGH. Variation in Fusobacterium necrophorum strains present on the hooves of footrot infected sheep, goats and cattle. Veterinary Microbiology. 2009; 135: 363-367. doi: 10.1016/j.vetmic.2008.09.084
  24. Clifton R, Green L. Pathogenesis of ovine footrot disease: a complex picture. Veterinary Record. 2016; 176: 225-227. doi: 10.1016/j.vetmic.2008.09.084
  25. Norris SJ, Paster BJ, Smibert RM. Genus IV. Treponema Schaudinn 1905. In: Krieg NR, Staley JT, Brown DR, Hedlund BP, Paster BJ, Ward NL, Ludwig W, Whitman WB. Eds, Bergey’s Manual of Systematic Bacteriology, 2nd Edn, Vol 4, Springer, New York, USA. 2010:  501–531.
  26. Moore LJ, Woodward MJ, Grogono-Thomas R. The occurrence of treponemes in contagious ovine digital dermatitis and the characterisation of associated Dichelobacter nodosus. Veterinary Microbiology. 2005; 111: 199-209. doi: 10.1016/j.vetmic.2005.10.016
  27. Moore LJ, Wassink GJ, Green LE, Grogono-Thomas R.  The detection and characterisation of Dichelobacter nodosus from cases of ovine footrot in England and Wales. Veterinary Microbiology. 2005; 108: 57-67. doi: 10.1016/j.vetmic.2005.01.029
  28. Evans Nicholas J, Brown Jennifer M, Demirkan I, ingh P, Getty B, Timofte D, Vink WD, Murray RD, Blowey RW, Birtles RJ, Hart CA. Association of unique, isolated treponemes with bovine digital dermatitis lesions. Journal of Clinical Microbiology. 2009; 47: 689-696. doi: 10.1128/jcm.01914-08
  29. Evans NJ, Timofte D, Isherwood DR, Brown JM, Williams JM, Sherlock K, Lehane MJ, Murray RD, Birtles RJ, Hart CA, Carter SD.  Host and environmental reservoirs of infection for bovine digital dermatitis treponemes. Veterinary Microbiology. 2012; 156: 102-109. doi: 10.1016/j.vetmic.2011.09.029
  30. Stewart DJ, Claxton PD. Ovine footrot: clinical diagnosis and bacteriology. In: Corner LA, Bagust TJ. Eds. Australian Standard Diagnostic Techniques for Animal Diseases, Commonwealth Scientific and Industrial Research Organisation, East Melbourne, Australia, 1993; 21-24.
  31. Clegg SR, Mansfield KG, Newbrook K, Sullivan LE, Blowey RW, Carter SD, Evans NJ.  Isolation of digital dermatitis treponemes from hoof lesions in wild North American elk (Cervus elaphus) in Washington State, USA. Journal of Clinical Microbiology. 2014; 53: 88-94. doi: 10.1128/jcm.02276-14
  32. Crosby-Durrani HE, Clegg SR, Singer E, Angell JW, Evans NJ, Carter SD, Blundell RJ, Duncan JS.  Severe foot lesions in dairy goats associated with digital dermatitis treponemes. Journal of Comparative Pathology. 2016; 154: 283-296. doi: 10.1016/j.jcpa.2016.04.001
  33. Evans NJ, Brown JM, Demirkan I, Murray RD, Vink WD, Blowey RW, Hart CA, Carter SD.  Three unique groups of spirochetes isolated from digital dermatitis lesions in UK cattle. Veterinary Microbiology. 2008; 130: 141-150. doi: 10.1016/j.vetmic.2007.12.019
  34. Duncan JS, Angell JW, Richards P, Lenzi L, Staton GJ, Grove-White D, Clegg S, Oikonomou G, Carter SD, Evans NJ.  The dysbiosis of ovine foot microbiome during the development and treatment of contagious ovine digital dermatitis. Animal microbiome. 2021; 3: 1-21. doi: 10.1186/s42523-021-00078-4
  35. Duncan JS, Grove-White D, Oultram JWH,  Phythian CJ, Van Dijk J, Carter SD, Cripps PJ, Williams HJ.  Effects of parenteral amoxicillin on recovery rates and new infection rates for contagious ovine digital dermatitis in sheep. Veterinary Record. 2011; 169: 606-606. doi: 10.1136/vr.d4394
  36. Angell JW, Grove-White DH, Duncan JS. Sheep and farm level factors associated with contagious ovine digital dermatitis: A longitudinal repeated cross-sectional study of sheep on six farms. Preventive Veterinary Medicine. 2015; 122: 107-120. doi: 10.1016/j.prevetmed.2015.09.016
  37. Rosander A, Mourath S, König U, Nyman A, Frosth S.  Field study on the prevalence of ovine footrot, contagious ovine digital dermatitis, and their associated bacterial species in Swedish sheep flocks. Pathogens. 2023. doi: 10.3390/pathogens12101224
  38. Rosander A, Albinsson R, König U, Nyman A, Frosth S. Prevalence of bacterial species associated with ovine footrot and contagious ovine digital dermatitis in Swedish slaughter lambs. Acta Veterinaria Scandinavica. 2022; 64: 6.  doi: 10.1186/s13028-022-00625-2
  39. König U, Nyman A-KJ, de Verdier K. Prevalence of footrot in Swedish slaughter lambs. Acta Veterinaria Scandinavica. 2011; 53: 27. 
Volume 19, Issue 2 - Serial Number 41
October 2024
Pages 118-124

  • Receive Date 27 November 2023
  • Revise Date 30 December 2023
  • Accept Date 08 January 2024
  • First Publish Date 08 January 2024