Effect of Culling Management Practices on the Seroprevalence of Johne’s Disease in Holstein Dairy Cattle in Central Italy
Abstract
:1. Introduction
2. Materials and Methods
2.1. Dairy Farms and Study Area
2.2. Study Design and Sample Size
2.3. Sample Collection
2.4. Data Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Whittington, R.; Donat, K.; Weber, M.F.; Kelton, D.; Nielsen, S.S.; Eisenberg, S.; Arrigoni, N.; Juste, R.; Sáez, J.L.; Dhand, N.; et al. Control of paratuberculosis: Who, why and how. A review of 48 countries. BMC Vet. Res. 2019, 15, 198. [Google Scholar] [CrossRef] [Green Version]
- Mac-Johnston, A.; Buncic, S.; Bènard, G.; Cenci-Goga, B.; Cubero, G. Opinion of the Scientific Panel on Biological Hazards on a request from the Commission related on Revision of Meat Inspection Procedures for Lambs and Goats. EFSA J. 2004, 54, 1–49. [Google Scholar]
- Anonymous. Council Regulation 1099/2009 of 24 September 2009 on the Protection of Animals at the Time of Killing; FAO: Rome, Italy, 2009. [Google Scholar]
- Anonymous. The Risk of Transmission of Mycobacterium avium subsp. paratuberculosis via Bovine Semen. EFSA J. 2004, 110, 1–59. [Google Scholar]
- Garvey, M. Mycobacterium Avium Paratuberculosis: A Disease Burden on the Dairy Industry. Animals 2020, 10, 1773. [Google Scholar] [CrossRef] [PubMed]
- Nielsen, S.S.; Toft, N. A review of prevalences of paratuberculosis in farmed animals in Europe. Prev. Vet. Med. 2009, 88, 1–14. [Google Scholar] [CrossRef]
- Windsor, P.A.; Whittington, R.J. Evidence for age susceptibility of cattle to Johne’s disease. Vet. J. 2010, 184, 37–44. [Google Scholar] [CrossRef] [PubMed]
- MacDonald-Phillips, K.A.; Keefe, G.P.; VanLeeuwen, J.; Shaw, D.H.; McClure, J.; McKenna, S.L.B. Dairy producer satisfaction and knowledge transfer with the veterinary-administered risk assessment and management plan in a voluntary Johne’s disease control program. J. Dairy Sci. 2022, 105, 2499–2508. [Google Scholar] [CrossRef] [PubMed]
- Kudahl, A.B.; Sorensen, J.T.; Nielsen, S.S.; Ostergaard, S. Simulated economic effects of improving the sensitivity of a diagnostic test in paratuberculosis control. Prev. Vet. Med. 2007, 78, 118–129. [Google Scholar] [CrossRef]
- Lu, Z.; Mitchell, R.M.; Smith, R.L.; Van Kessel, J.S.; Chapagain, P.P.; Schukken, Y.H.; Grohn, Y.T. The importance of culling in Johne’s disease control. J. Theor. Biol. 2008, 254, 135–146. [Google Scholar] [CrossRef]
- Stott, A.W.; Jones, G.M.; Humphry, R.W.; Gunn, G.J. Financial incentive to control paratuberculosis (Johne’s disease) on dairy farms in the United Kingdom. Vet. Rec. 2005, 156, 825–831. [Google Scholar] [CrossRef] [PubMed]
- Dorshorst, N.C.; Collins, M.T.; Lombard, J.E. Decision analysis model for paratuberculosis control in commercial dairy herds. Prev. Vet. Med. 2006, 75, 92–122. [Google Scholar] [CrossRef] [PubMed]
- Ridge, S.E.; Baker, I.M.; Hannah, M. Effect of compliance with recommended calf-rearing practices on control of bovine Johne’s disease. Aust. Vet. J. 2005, 83, 85–90. [Google Scholar] [CrossRef] [PubMed]
- Mõtus, K.; Rilanto, T.; Viidu, D.-A.; Orro, T.; Viltrop, A. Seroprevalence of selected endemic infectious diseases in large-scale Estonian dairy herds and their associations with cow longevity and culling rates. Prev. Vet. Med. 2021, 192, 105389. [Google Scholar] [CrossRef] [PubMed]
- Tiwari, A.; VanLeeuwen, J.A.; McKenna, S.L.B.; Keefe, G.P.; Barkema, H.W. Johne’s disease in Canada Part I: Clinical symptoms, pathophysiology, diagnosis, and prevalence in dairy herds. Can. Vet. J. 2006, 47, 874–882. [Google Scholar]
- Mariano, V.; McCrindle, C.M.E.; Cenci-Goga, B.; Picard, J.A. Case-Control Study To Determine whether River Water Can Spread Tetracycline Resistance to Unexposed Impala (Aepyceros melampus) in Kruger National Park (South Africa). Appl. Environ. Microbiol. 2009, 75, 113–118. [Google Scholar] [CrossRef] [Green Version]
- Cenci-Goga, B.T.; Vescera, F.; Paolotto, P.; McCrindle, C.M.E.; Roberti, U. Seroprevalence of Mycobacterium avium subspecies paratuberculosis in cows in Umbria, Italy. Vet. Rec. 2010, 167, 577–578. [Google Scholar] [CrossRef]
- Akinwande, M.; Dikko, H.; Samson, A. Variance Inflation Factor: As a Condition for the Inclusion of Suppressor Variable(s) in Regression Analysis. Open J. Stat. 2015, 5, 754–767. [Google Scholar] [CrossRef] [Green Version]
- Tiwari, A.; VanLeeuwen, J.A.; Dohoo, I.R.; Stryhn, H.; Keefe, G.P.; Haddad, J.P. Effects of seropositivity for bovine leukemia virus, bovine viral diarrhoea virus, Mycobacterium avium subspecies paratuberculosis, and Neospora caninum on culling in dairy cattle in four Canadian provinces. Vet. Microbiol. 2005, 109, 147–158. [Google Scholar] [CrossRef]
- Collins, M.T.; Gardner, I.A.; Garry, F.B.; Roussel, A.J.; Wells, S.J. Consensus recommendations on diagnostic testing for the detection of paratuberculosis in cattle in the United States. J. Am. Vet. Med. Assoc. 2006, 229, 1912–1919. [Google Scholar] [CrossRef] [Green Version]
- McAloon, C.G.; Roche, S.; Ritter, C.; Barkema, H.W.; Whyte, P.; More, S.J.; O’Grady, L.; Green, M.J.; Doherty, M.L. A review of paratuberculosis in dairy herds—Part 1: Epidemiology. Vet. J. 2019, 246, 59–65. [Google Scholar] [CrossRef]
- Whitlock, R.H.; Wells, S.J.; Sweeney, R.W.; van Tiem, J. ELISA and fecal culture for paratuberculosis (Johne’s disease) sensitivity and specificity of each method. Vet. Microbiol. 2000, 77, 387–398. [Google Scholar] [CrossRef]
- Chaubey, K.K.; Gupta, R.D.; Gupta, S.; Singh, S.V.; Bhatia, A.K.; Jayaraman, S.; Kumar, N.; Goel, A.; Rathore, A.S.; Sahzad; et al. Trends and advances in the diagnosis and control of paratuberculosis in domestic livestock. Vet. Quart. 2016, 36, 203–227. [Google Scholar] [CrossRef]
- McAloon, C.G.; Whyte, P.; More, S.J.; Green, M.J.; O’Grady, L.; Garcia, A.; Doherty, M.L. The effect of paratuberculosis on milk yield—A systematic review and meta-analysis. J. Dairy Sci. 2016, 99, 1449–1460. [Google Scholar] [CrossRef] [Green Version]
- Garcia, A.B.; Shalloo, L. Invited review: The economic impact and control of paratuberculosis in cattle. J. Dairy Sci. 2015, 98, 5019–5039. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Crociati, M.; Sylla, L.; van Straten, M.; Stradaioli, G.; Monaci, M. Estimating the net return of a remote calving alarm system in a dairy farm. J. Dairy Sci. 2020, 103, 9646–9655. [Google Scholar] [CrossRef]
- Dallago, G.M.; Wade, K.M.; Cue, R.I.; McClure, J.T.; Lacroix, R.; Pellerin, D.; Vasseur, E. Keeping Dairy Cows for Longer: A Critical Literature Review on Dairy Cow Longevity in High Milk-Producing Countries. Animals 2021, 11, 808. [Google Scholar] [CrossRef]
- Muskens, J.; Elbers, A.R.; van Weering, H.J.; Noordhuizen, J.P. Herd management practices associated with paratuberculosis seroprevalence in Dutch dairy herds. J. Vet. Med. B Infect. Dis. Vet. Public Health 2003, 50, 372–377. [Google Scholar] [CrossRef]
- Nielsen, S.S.; Toft, N. Assessment of management-related risk factors for paratuberculosis in Danish dairy herds using Bayesian mixture models. Prev. Vet. Med. 2007, 81, 306–317. [Google Scholar] [CrossRef] [PubMed]
- European Commission Directorate-General Health & Consumer Protection, Directorate B—Scientific Health Opinions, Unit B3—Management of Scientific Committees II. Possible Links between Crohn’s Disease and Paratuberculosis; Report of the Scientific Committee on Animal Health and Animal Welfare—Adopted 21 March 2000; European Commission Directorate-General Health & Consumer Protection, Directorate B—Scientific Health Opinions, Unit B3—Management of Scientific Committees II: Brussels, Belgium, 2000. [Google Scholar]
- Khol, J.L.; Damoser, J.; Dünser, M.; Baumgartner, W. Paratuberculosis, a notifiable disease in Austria-Current status, compulsory measures and first experiences. Prev. Vet. Med. 2007, 82, 302–307. [Google Scholar] [CrossRef]
- Pozzato, N.; Capello, K.; Comin, A.; Toft, N.; Nielsen, S.S.; Vicenzoni, G.; Arrigoni, N. Prevalence of paratuberculosis infection in dairy cattle in Northern Italy. Prev. Vet. Med. 2011, 102, 83–86. [Google Scholar] [CrossRef] [PubMed]
- Gonda, M.G.; Chang, Y.M.; Shook, G.E.; Collins, M.T.; Kirkpatrick, B.W. Effect of Mycobacterium paratuberculosis infection on production, reproduction, and health traits in US Holsteins. Prev. Vet. Med. 2007, 80, 103–119. [Google Scholar] [CrossRef]
- Wells, S.J.; Hartmann, W.L.; Anderson, P.L. Evaluation of progress made by dairy and beef herds enrolled in the Minnesota Johne’s Disease Control Program. J. Am. Vet. Med. Assoc. 2008, 233, 1920–1926. [Google Scholar] [CrossRef] [PubMed]
- Gamberale, F.; Pietrella, G.; Sala, M.; Scaramella, P.; Puccica, S.; Antognetti, V.; Arrigoni, N.; Ricchi, M.; Cersini, A. Management of Mycobacterium avium subsp. paratuberculosis in dairy farms: Selection and evaluation of different DNA extraction methods from bovine and buffaloes milk and colostrum for the establishment of a safe colostrum farm bank. Microbiol. Open 2019, 8, e875. [Google Scholar] [CrossRef] [Green Version]
- Cenci-Goga, B.T.; Stazzoni, G.; Paolotto, P. Prevalence of Johne’s-disease infection in cattle in Umbria, Italy. Meso 2008, 10, 145–149. [Google Scholar]
- Crociati, M.; Sylla, L.; Stradaioli, G.; Monaci, M.; Zecconi, A. Assessment of Sensitivity and Profitability of an Intravaginal Sensor for Remote Calving Prediction in Dairy Cattle. Sensors 2021, 21, 8348. [Google Scholar] [CrossRef] [PubMed]
- Rossi, E.; Ferri, N.; Crociati, M.; Monaci, M.; Stradaioli, G.; Sylla, L. Remote monitoring system as a tool for calving management in Mediterranean Buffalo heifers (Bubalus bubalis). Reprod. Domest. Anim. 2020, 55, 1803–1807. [Google Scholar] [CrossRef] [PubMed]
Farm | n. of Adult Cows | n. of Cows Tested | % of Cows Tested | +ve | −ve | AP | TP | 95% CI | |
---|---|---|---|---|---|---|---|---|---|
1 | 24 | 23 | 95.83 | 1 | 22 | 4.3 | 6.8 | 0.0 | 17.1 |
2 | 19 | 19 | 100.00 | 1 | 18 | 5.3 | 8.7 | 0.0 | 21.4 |
3 | 38 | 35 | 92.11 | 2 | 33 | 5.7 | 9.6 | 0.0 | 19.4 |
4 | 24 | 23 | 95.83 | 1 | 22 | 4.3 | 6.8 | 0.0 | 17.1 |
5 | 29 | 27 | 93.10 | 2 | 25 | 7.4 | 13.1 | 0.0 | 25.8 |
6 | 18 | 18 | 100.00 | 1 | 17 | 5.6 | 9.3 | 0.0 | 22.7 |
7 | 30 | 28 | 93.33 | 1 | 27 | 3.6 | 5.2 | 0.0 | 13.5 |
8 | 18 | 18 | 100.00 | 1 | 17 | 5.6 | 9.3 | 0.0 | 22.7 |
9 | 28 | 27 | 96.43 | 1 | 26 | 3.7 | 5.5 | 0.0 | 14.1 |
10 | 27 | 26 | 96.30 | 3 | 23 | 11.5 | 21.5 | 0.0 | 37.3 |
11 | 158 | 112 | 70.89 | 5 | 107 | 4.5 | 7.1 | 2.3 | 11.8 |
12 | 135 | 100 | 74.07 | 1 | 99 | 1.0 | 0.0 | 0.0 | 0.0 |
13 | 30 | 28 | 93.33 | 1 | 27 | 3.6 | 5.2 | 0.0 | 13.5 |
14 | 70 | 60 | 85.71 | 1 | 59 | 1.7 | 1.4 | 0.0 | 4.3 |
15 | 42 | 38 | 90.48 | 1 | 37 | 2.6 | 3.3 | 0.0 | 9.0 |
16 | 150 | 108 | 72.00 | 5 | 103 | 4.6 | 7.4 | 2.5 | 12.3 |
17 | 108 | 85 | 78.70 | 5 | 80 | 5.9 | 10.0 | 3.6 | 16.3 |
18 | 66 | 57 | 86.36 | 1 | 56 | 1.8 | 1.5 | 0.0 | 4.7 |
19 | 425 | 202 | 47.53 | 13 | 189 | 6.4 | 11.1 | 6.8 | 15.4 |
20 | 400 | 196 | 49.00 | 12 | 184 | 6.1 | 10.5 | 6.2 | 14.7 |
Total | 1839 | 1230 | 66.88 | 59 | 1171 | 4.8 | 7.7 | 6.3 | 9.2 |
Audit Check List | Management Practices in the 20 Selected Farms |
---|---|
Area where calves are born | Dedicated maternity area |
Time elapsed from birth to calf removal from its dam | <6 h |
Adequate separation of area for unweaned calves from adult cattle and effluent from adult cattle | yes |
Age when replacement heifers graze paddocks of adult cattle | 20–22 months old (at 6–7 months of pregnancy, A.I. at 14–15 months) |
Milk or milk replacer fed to calves | Colostrum for 3–5 days then milk replacer |
frequency of feeding | bid |
Method for feeding | Bucket with colostrum/milk from negative mothers or pathogen-free milk replacer |
Bedding into the maternity area | Straw |
Shelter | Shade—roof and sides |
Source of water for unweaned calves | Town water, bore water, spring water |
Water provided to calves from birth | Yes |
Supplements | Yes |
Type of supplements for unweaned | Pellets after 4–5 days and some hay |
Age when calves receive the supplement | 1–6 days |
Source of hay | Both home (80%) and purchased (20%) |
Age at weaning | <10 weeks |
Source of water for weaned calves | Town water, bore water, spring water |
Type of supplements for weaned calves | Pellets |
Average productive life | Group A: <1100 days, Group B: >1500 days |
Replacement heifers introduced | Yes (<5%), none during the study |
Source of replacement | Private sales |
Individual Variables | OR (95% CI) | p-Value |
---|---|---|
After implementation | 1.105 (0.612–1.997) | 0.7408 |
Farm | Average Productive Life | n. of Adult Cows | n. of Cows Tested | % of Cows Tested | +ve | −ve | AP | TP | 95% CI | |
---|---|---|---|---|---|---|---|---|---|---|
1 | Group B | 21 | 20 | 95.24 | 1 | 19 | 5.0 | 8.2 | 0.0 | 20.2 |
2 | Group B | 22 | 10 | 45.45 | 0 | 10 | 0.0 | 0.0 | 0.0 | 0.0 |
3 | Group B | 42 | 18 | 42.86 | 1 | 17 | 5.6 | 9.3 | 0.0 | 22.7 |
4 | Group B | 25 | 14 | 56.00 | 0 | 14 | 0.0 | 0.0 | 0.0 | 0.0 |
5 | Group B | 27 | 12 | 44.44 | 1 | 11 | 8.3 | 15.0 | 0.0 | 35.2 |
6 | Group B | 20 | 8 | 40.00 | 0 | 8 | 0.0 | 0.0 | 0.0 | 0.0 |
7 | Group B | 27 | 11 | 40.74 | 0 | 11 | 0.0 | 0.0 | 0.0 | 0.0 |
8 | Group B | 20 | 4 | 20.00 | 0 | 4 | 0.0 | 0.0 | 0.0 | 0.0 |
9 | Group B | 25 | 3 | 12.00 | 0 | 3 | 0.0 | 0.0 | 0.0 | 0.0 |
10 | Group B | 29 | 11 | 37.93 | 1 | 10 | 9.1 | 16.5 | 0.0 | 38.5 |
11 | Group B | 166 | 73 | 43.98 | 3 | 70 | 4.1 | 6.3 | 0.8 | 11.9 |
12 | Group A | 126 | 61 | 48.41 | 1 | 60 | 1.6 | 1.3 | 0.0 | 4.2 |
13 | Group B | 33 | 12 | 36.36 | 0 | 12 | 0.0 | 0.0 | 0.0 | 0.0 |
14 | Group B | 75 | 35 | 46.67 | 0 | 35 | 0.0 | 0.0 | 0.0 | 0.0 |
15 | Group B | 49 | 22 | 44.90 | 0 | 22 | 0.0 | 0.0 | 0.0 | 0.0 |
16 | Group B | 152 | 73 | 48.03 | 4 | 69 | 5.5 | 9.1 | 2.5 | 15.8 |
17 | Group B | 110 | 69 | 62.73 | 3 | 66 | 4.3 | 6.8 | 0.9 | 12.8 |
18 | Group B | 66 | 27 | 40.91 | 0 | 27 | 0.0 | 0.0 | 0.0 | 0.0 |
19 | Group A | 410 | 45 | 10.98 | 3 | 42 | 6.7 | 11.6 | 2.2 | 20.9 |
20 | Group A | 387 | 260 | 67.18 | 17 | 243 | 6.5 | 11.3 | 7.5 | 15.2 |
Total group A | 923 | 366 | 39.65 | 21 | 345 | 5.7 | 9.7 | 6.6 | 12.7 | |
Total group B | 909 | 422 | 46.42 | 14 | 408 | 3.3 | 4.7 | 2.7 | 6.8 | |
Total | 1832 | 788 | 43.01 | 35 | 753 | 4.4 | 7.0 | 5.2 | 8.8 |
Individual Variables | OR (95% CI) | p-Value |
---|---|---|
Normal culling type | 0.564 (0.282–1.125) | 0.1041 |
Farm size | 1.003 (1.001–1.005) | 0.0169 |
Individual Variables | OR (95% CI) | p-Value | VIF |
---|---|---|---|
Normal culling type | 2.446 (0.412–14.525) | 0.3249 | 3.57 |
Farm size | 1.006 (0.999–1.012) | 0.0734 | 3.57 |
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Crociati, M.; Grispoldi, L.; Chalias, A.; Monaci, M.; Cenci-Goga, B.; Sylla, L. Effect of Culling Management Practices on the Seroprevalence of Johne’s Disease in Holstein Dairy Cattle in Central Italy. Vet. Sci. 2022, 9, 162. https://doi.org/10.3390/vetsci9040162
Crociati M, Grispoldi L, Chalias A, Monaci M, Cenci-Goga B, Sylla L. Effect of Culling Management Practices on the Seroprevalence of Johne’s Disease in Holstein Dairy Cattle in Central Italy. Veterinary Sciences. 2022; 9(4):162. https://doi.org/10.3390/vetsci9040162
Chicago/Turabian StyleCrociati, Martina, Luca Grispoldi, Athanasios Chalias, Maurizio Monaci, Beniamino Cenci-Goga, and Lakamy Sylla. 2022. "Effect of Culling Management Practices on the Seroprevalence of Johne’s Disease in Holstein Dairy Cattle in Central Italy" Veterinary Sciences 9, no. 4: 162. https://doi.org/10.3390/vetsci9040162