Molecular Diagnosis of Footrot and Contagious Ovine Digital Dermatitis in Small Ruminants in the Iberian Peninsula
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Ethical Concerns
2.2. Swab Samples
2.3. Pathogen Identification
2.4. Statistical Procedures
3. Results
3.1. Identification of Bacteria Species in the Samples
3.2. D. nodosus Serogroups
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Crosby-Durrani, H.E.; Clegg, S.R.; Singer, E.; Angell, J.W.; Evans, N.J.; Carter, S.D.; Blundell, R.J.; Duncan, J.S. Severe Foot Le-sions in Dairy Goats Associated with Digital Dermatitis Treponemes. J. Comp. Path. 2016, 154, 283–296. [Google Scholar] [CrossRef]
- Sullivan, L.E.; Evans, N.J.; Clegg, S.R.; Carter, S.D.; Horsfield, J.E.; Duncan, J.S.; White, D.G. Digital dermatitis treponemes associated with a severe foot disease in dairy goats. Veter. Rec. 2015, 176, 283. [Google Scholar] [CrossRef]
- Egerton, J.R.; Roberts, D.S.; Parsonson, I.M. The aetiology and pathogenesis of ovine foot-rot. I. A histological study of the bacterial invasion. J. Comp. Pathol. 1969, 79, 207–215. [Google Scholar] [CrossRef]
- Roberts, D.S.; Egerton, J.R. The aetiology and pathogenesis of ovine foot-rot. II. The pathogenic association of Fusiformis nodosus and Fusiformis necrophorus. J. Comp. Pathol. 1969, 79, 217–227. [Google Scholar] [CrossRef]
- Zanolari, P.; Dürr, S.; Jores, J.; Steiner, A.; Kuhnert, P. Ovine footrot: A review of current knowledge. Veter. J. 2021, 271, 105647. [Google Scholar] [CrossRef]
- Duncan, J.S.; Angell, J.W.; Richards, P.; Lenzi, L.; Staton, G.J.; Grove-White, D.; Clegg, S.; Oikonomou, G.; Carter, S.D.; Evans, N.J. The dysbiosis of ovine foot microbiome during the development and treatment of contagious ovine digital dermatitis. Anim. Microbiome 2021, 3, 19. [Google Scholar] [CrossRef]
- Maboni, G.; Frosth, S.; Aspán, A.; Tötemeyer, S. Ovine footrot: New insights into bacterial colonization. Vet. Rec. 2016, 179, 228. [Google Scholar] [CrossRef]
- Clifton, R.; Monaghan, E.M.; Green, M.J.; Purdy, K.J.; Green, L.E. Differences in composition of interdigital skin microbiota predict sheep and feet that develop footrot. Sci. Rep. 2022, 12, 8931. [Google Scholar] [CrossRef]
- Angell, J.; Grove-White, D.; Duncan, J. Sheep and farm level factors associated with contagious ovine digital dermatitis: A longitudinal repeated cross-sectional study of sheep on six farms. Prev. Veter. Med. 2015, 122, 107–120. [Google Scholar] [CrossRef]
- Staton, G.J.; Angell, J.W.; Grove-White, D.; Clegg, S.R.; Carter, S.D.; Evans, N.J.; Duncan, J.S. Contagious Ovine Digital Dermatitis: A Novel Bacterial Etiology and Lesion Pathogenesis. Front. Veter. Sci. 2021, 8, 722461. [Google Scholar] [CrossRef]
- Ministerio de Agricultura, Pesca y Alimentación Indicadores Económicos del Sector Ovino y Caprino de Carne. Available online: https://www.mapa.gob.es/es/ganaderia/temas/produccion-y-mercados-ganaderos/indicadoreseconomicosdelsectorovinoycaprino_carne_2023a_tcm30-511496.pdf (accessed on 20 November 2023).
- Ministerio de Agricultura, Pesca y Alimentación. Ovino de Leche, Junio de 2023. Available online: https://www.mapa.gob.es/es/ganaderia/temas/produccion-y-mercados-ganaderos/dashboardovinoleche_junio2023_tcm30-428244.pdf (accessed on 20 November 2023).
- Berga, A.M.; Sanchez, P. Incidencia económica de la Sanidad en ovino. Programas sanitarios básicos. Mundo Ganadero 1990, 8, 27–31. [Google Scholar]
- Green, L.E.; George, T.R.N. Assessment of current knowledge of footrot in sheep with particular reference to Dichelobacter nodosus and implications for elimination or control strategies for sheep in Great Britain. Vet. J. 2008, 175, 173–180. [Google Scholar] [CrossRef] [PubMed]
- Raadsma, H.; Dhungyel, O. A review of footrot in sheep: New approaches for control of virulent footrot. Livest. Sci. 2013, 156, 115–125. [Google Scholar] [CrossRef]
- Angell, J.W.; Duncan, J.S.; Carter, S.D.; Grove-White, D.H. Farmer reported prevalence and factors associated with contagious ovine digital dermatitis in Wales: A questionnaire of 511 sheep farmers. Prev. Vet. Med. 2014, 113, 132–138. [Google Scholar] [CrossRef] [PubMed]
- Egerton, J.; Roberts, D.S. Vaccination against ovine foot-rot. J. Comp. Pathol. 1971, 81, 179–185. [Google Scholar] [CrossRef] [PubMed]
- Anklam, K.; Kulow, M.; Yamazaki, W.; Döpfer, D. Development of real-time PCR and loop-mediated isothermal amplification (LAMP) assays for the differential detection of digital dermatitis associated treponemes. PLoS ONE 2017, 12, e0178349. [Google Scholar] [CrossRef]
- 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 Veter. Scand. 2022, 64, 64. [Google Scholar] [CrossRef]
- Evans, N.J.; Timofte, D.; Isherwood, D.R.; Brown, J.M.; Williams, J.M.; Sherlock, K.; Lehane, M.J.; Murray, R.D.; Birtles, R.J.; Hart, C.A.; et al. Host and environmental reservoirs of infection for bovine digital dermatitis treponemes. Veter. Microbiol. 2012, 156, 102–109. [Google Scholar] [CrossRef]
- Piriz, S.; Cuenca, R.; Valle, J.; Vadillo, S. Isolation and identification of anaerobic bacteria from ovine foot rot in Spain. Res. Vet. Sci. 1990, 49, 245–247. [Google Scholar]
- Hurtado, M.A.; Píriz, S.; Valle, J.; Jimenez, R.; Vadillo, S. Aetiology of ovine footrot in Spain. Veter. Rec. 1998, 142, 60–63. [Google Scholar] [CrossRef] [PubMed]
- Clifton, R.; Giebel, K.; Liu, N.L.B.H.; Purdy, K.J.; Green, L.E. Sites of persistence of Fusobacterium necrophorum and Dichelobacter nodosus: A paradigm shift in understanding the epidemiology of footrot in sheep. Sci. Rep. 2019, 9, 14429. [Google Scholar] [CrossRef] [PubMed]
- Bernhard, M.; Frosth, S.; König, U. First report on outbreaks of contagious ovine digital dermatitis in Sweden. Acta Vet. Scan. 2021, 63, 29. [Google Scholar] [CrossRef]
- Wilson-Welder, J.H.; Mansfield, K.; Han, S.; Bayles, D.O.; Alt, D.P.; Olsen, S.C. Lesion Material From Treponema-Associated Hoof Disease of Wild Elk Induces Disease Pathology in the Sheep Digital Dermatitis Model. Front. Veter. Sci. 2022, 8, 782149. [Google Scholar] [CrossRef]
- Rasool, A.; Farooq, S.; Kumar, S.; Kashoo, Z.A.; Dar, P.A.; Bhat, M.A.; Qureshi, S.; Hussain, I.; Shah, R.A.; Taku, A.; et al. Evidence of novel Treponema phylotypes implicated in contagious ovine digital dermatitis and association of treponemes with major lameness causing foot pathogens. Microb. Pathog. 2023, 182, 106214. [Google Scholar] [CrossRef]
- McPherson, A.S.; Whittington, R.J.; Hall, E.; Cook, E.J.; Jones, J.V.; Ang, Y.Q.; McTavish, E.L.; Dhungyel, O.P. A comparison of mul-tivalent and bivalent vaccination strategies for the control of virulent ovine footrot. Vaccine 2021, 39, 1736–1745. [Google Scholar] [CrossRef] [PubMed]
- Albuquerque, C.; Cavaco, S.; Caetano, P.; Branco, S.; Monteiro, H.; Ramos, M.; Chimenos, A.U.; Leão, C.; Botelho, A. Ovine footrot in Southern Portugal: Detection of Dichelobacter nodosus and Fusobacterium necrophorum in sheep with different lesion scores. Veter. Microbiol. 2022, 266, 109339. [Google Scholar] [CrossRef]
- Budnik, M.; Struck, A.-K.; Storms, J.; Wirth, A.; Jores, J.; Kuhnert, P.; Distl, O. Serological Diversity of Dichelobacter nodosus in German Sheep Flocks. Animals 2022, 12, 753. [Google Scholar] [CrossRef] [PubMed]
- Lacombe-Antoneli, A.; Píriz, S.; Vadillo, S. Aetiology of caprine footrot in Extremadura region, Spain. Acta Veter. Hung. 2006, 54, 313–320. [Google Scholar] [CrossRef]
- Prosser, N.S.; Monaghan, E.M.; Green, L.E.; Purdy, K.J. Serogroups of Dichelobacter nodosus, the cause of footrot in sheep, are randomly distributed across England. Sci. Rep. 2020, 10, 16823. [Google Scholar] [CrossRef]
- Wani, S.A.; Farooq, S.; Kashoo, Z.A.; Hussain, I.; Bhat, M.A.; Rather, M.A.; Aalamgeer, S. Determination of prevalence, serological diversity, and virulence of Dichelobacter nodosus in ovine footrot with identification of its predominant serogroup as a potential vaccine candidate in J&K, India. Trop Anim Health Prod. 2019, 51, 1089–1095. [Google Scholar]
- Dhungyel, O.; Whittington, R.; Egerton, J. Serogroup specific single and multiplex PCR with pre-enrichment culture and immuno-magnetic bead capture for identifying strains of D. nodosus in sheep with footrot prior to vaccination. Mol. Cell. Probes 2002, 16, 285–296. [Google Scholar] [CrossRef] [PubMed]
- McPherson, A.S.; Dhungyel, O.P.; Whittington, R.J. Detection and Serogrouping of Dichelobacter nodosus Infection by Use of Direct PCR from Lesion Swabs To Support Outbreak-Specific Vaccination for Virulent Footrot in Sheep. J. Clin. Microbiol. 2018, 56, e01730-17. [Google Scholar] [CrossRef] [PubMed]
- Dhungyel, O.; Hunter, J.; Whittington, R. Footrot vaccines and vaccination. Vaccine 2014, 32, 3139–3146. [Google Scholar] [CrossRef] [PubMed]
- Groenevelt, M.; Dekker, C.; Dhungyel, O.; Everts, R.; Hoogeveen, J.; Timmerman, A.; Zweerus, H.; Mokbel, M.; Duim, B. Serogroups of Dichelobacter nodosus detected in footrot lesions in sheep using a new multiplex real-time PCR. Adv. Anim. Biosci. 2023, 14, 186. [Google Scholar] [CrossRef]
- Dhungyel, O.; Schiller, N.; Eppleston, J.; Lehmann, D.; Nilon, P.; Ewers, A.; Whittington, R. Outbreak-specific monovalent/bivalent vaccination to control and eradicate virulent ovine footrot. Vaccine 2013, 31, 1701–1706. [Google Scholar] [CrossRef]
- Gelasakis, A.I.; Kalogianni, A.I.; Bossis, I. Aetiology, Risk Factors, Diagnosis and Control of Foot-Related Lameness in Dairy Sheep. Animals 2019, 9, 509. [Google Scholar] [CrossRef]
- Collee, J.G.; Watt, B.; Brown, R.; Johnstone, S. The recovery of anaerobic bacteria from swabs. J. Hyg. 1974, 72, 339–347. [Google Scholar] [CrossRef]
Etiologial Agent | Target Gene | Coded Protein | Reference |
---|---|---|---|
Fusobacterium necrophorum | lktA | Leukotoxin A | Commercial kit |
Dichelobacter nodosus | 16S | D16S rRNA | Commercial kit |
D. nodosus virulent strains | aprV2 | Acidic protease 2 | Commercial kit |
D. nodosus non virulent strains | aprB2 | Acidic protease 2 | Commercial kit |
D. nodosus serogroups | fimA | Fimbrial protein | Commercial kit * |
Treponema spp. | 16S | D16S rRNA | Anklam et al. 2017 [18] |
Treponema pedis | 16S-tRNA region | 16S rRNA intergenic space | Anklam et al. 2017 [18] |
Treponema phagenedenis | 16S-tRNA region | 16S rRNA intergenic space | Anklam et al. 2017 [18] |
Treponema medium | flaB2 | Flagellar filament 31.3 kDa | Anklam et al. 2017 [18] |
Pathogen Agent | Count/n | % |
---|---|---|
None | 6/105 | 5.71 |
D. nodosus | 7/105 | 6.67 |
F. necrophorum | 17/105 | 16.19 |
T. pedis | 1/105 | 0.95 |
T. medium | 1/105 | 0.95 |
T. phagedenis | 1/105 | 0.95 |
D. nodosus + F. necrophorum | 54/105 | 51.45 |
D. nodosus + F. necrophorum + T. pedis | 1/105 | 0.95 |
D. nodosus+ F necrophorum+ T. pedis + T. phagedenis | 2/105 | 1.90 |
F. necrophorum + T. pedis | 4/105 | 3.81 |
F. necrophorum + T. pedis + T. medium | 4/105 | 3.81 |
F. necrophorum+ T. pedis + T. phagedenis | 2/105 | 1.90 |
F. necrophorum+ T. pedis +T. medium + T. phagedenis | 5/105 | 4.76 |
Serotype | Count/n | % |
---|---|---|
A | (4/57) | 7.02 |
B | (9/57) | 15.8 |
C | (7/57) | 12.3 |
D | (6/57) | 10.5 |
E | (4/57) | 7.02 |
F | (3/57) | 5.26 |
H | (1/57) | 1.75 |
I | (1/57) | 1.75 |
M | (2/57) | 3.51 |
A + B + E + H | (1/57) | 1.75 |
A + C | (1/57) | 1.75 |
A + C + D | (1/57) | 1.75 |
A + D | (1/57) | 1.75 |
B + C + D | (1/57) | 1.75 |
B + D | (3/57) | 5.26 |
B + D + M | (1/57) | 1.75 |
B + E | (1/57) | 1.75 |
B + E + H | (1/57) | 1.75 |
B + H | (3/57) | 5.26 |
C + D | (2/57) | 3.51 |
D + E | (2/57) | 3.51 |
D + F | (2/57) | 3.51 |
Count/n | 57/57 |
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Benito, A.A.; Anía, S.; Ramo, M.d.l.Á.; Baselga, C.; Quílez, J.; Tejedor, M.T.; Monteagudo, L.V. Molecular Diagnosis of Footrot and Contagious Ovine Digital Dermatitis in Small Ruminants in the Iberian Peninsula. Animals 2024, 14, 481. https://doi.org/10.3390/ani14030481
Benito AA, Anía S, Ramo MdlÁ, Baselga C, Quílez J, Tejedor MT, Monteagudo LV. Molecular Diagnosis of Footrot and Contagious Ovine Digital Dermatitis in Small Ruminants in the Iberian Peninsula. Animals. 2024; 14(3):481. https://doi.org/10.3390/ani14030481
Chicago/Turabian StyleBenito, Alfredo A., Silvia Anía, María de los Ángeles Ramo, Cristina Baselga, Joaquín Quílez, María Teresa Tejedor, and Luis Vicente Monteagudo. 2024. "Molecular Diagnosis of Footrot and Contagious Ovine Digital Dermatitis in Small Ruminants in the Iberian Peninsula" Animals 14, no. 3: 481. https://doi.org/10.3390/ani14030481
APA StyleBenito, A. A., Anía, S., Ramo, M. d. l. Á., Baselga, C., Quílez, J., Tejedor, M. T., & Monteagudo, L. V. (2024). Molecular Diagnosis of Footrot and Contagious Ovine Digital Dermatitis in Small Ruminants in the Iberian Peninsula. Animals, 14(3), 481. https://doi.org/10.3390/ani14030481