Mastitis risk effect on the economic consequences of paratuberculosis control in dairy cattle: A stochastic modeling study

Autoři: Leslie J. Verteramo Chiu aff001;  Loren W. Tauer aff002;  Yrjo T. Gröhn aff001;  Rebecca L. Smith aff003
Působiště autorů: Department of Population Medicine and Diagnostic Sciences, Cornell University College of Veterinary Medicine, Ithaca, New York, United States of America aff001;  Charles H. Dyson School of Applied Economics and Management, Cornell SC Johnson Business College, Cornell University, Ithaca, New York, United States of America aff002;  Department of Pathobiology, University of Illinois, College of Veterinary Medicine, Urbana, Illinois, United States of America aff003
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: 10.1371/journal.pone.0217888


The benefits and efficacy of control programs for herds infected with Mycobacterium avium subsp. paratuberculosis (MAP) have been investigated under various contexts. However, most previous research investigated paratuberculosis control programs in isolation, without modeling the potential association with other dairy diseases. This paper evaluated the benefits of MAP control programs when the herd is also affected by mastitis, a common disease causing the largest losses in dairy production. The effect of typically suggested MAP controls were estimated under the assumption that MAP infection increased the rate of clinical mastitis. We evaluated one hundred twenty three control strategies comprising various combinations of testing, culling, and hygiene, and found that the association of paratuberculosis with mastitis alters the ranking of specific MAP control programs, but only slightly alters the cost-benefit difference of particular MAP control components, as measured by the distribution of net present value of a representative U.S. dairy operation. In particular, although testing and culling for MAP resulted in a reduction in MAP incidence, that control led to lower net present value (NPV) per cow. When testing was used, ELISA was more economically beneficial than alternative testing regimes, especially if mastitis was explicitly modeled as more likely in MAP-infected animals, but ELISA testing was only significantly associated with higher NPV if mastitis was not included in the model at all. Additional hygiene was associated with a lower NPV per cow, although it lowered MAP prevalence. Overall, the addition of an increased risk of mastitis in MAP-infected animals did not change model recommendations as much as failing to consider.

Klíčová slova:

Death rates – Enzyme-linked immunoassays – Hygiene – Mastitis – Milk – Paratuberculosis – Bovine mastitis – Molting


1. Marcé C, Ezanno P, Weber MF, Seegers H, Pfeiffer DU, Fourichon C. Modeling within-herd transmission of Mycobacterium avium subspecies paratuberculosis in dairy cattle: a review. J Dairy Sci. 2010;93: 4455–70. doi: 10.3168/jds.2010-3139 20854979

2. Kudahl AB, Nielsen SS, Sørensen JT. Relationship between antibodies against Mycobacterium avium subsp. paratuberculosi s in milk and shape of lactation curves. Prev Vet Med. 2004;62: 119–134. doi: 10.1016/j.prevetmed.2003.11.008 15156998

3. Aly SS, Anderson RJ, Adaska JM, Jiang J, Gardner IA. Association between Mycobacterium avium subspecies paratuberculosis infection and milk production in two California dairies. J Dairy Sci. 2010;93: 1030–40. doi: 10.3168/jds.2009-2611 20172223

4. Nielsen SS, Krogh MA, Enevoldsen C. Time to the occurrence of a decline in milk production in cows with various paratuberculosis antibody profiles. J Dairy Sci. 2009;92: 149–55. doi: 10.3168/jds.2008-1488 19109273

5. Lombard JE, Garry FB, McCluskey BJ, Wagner BA. Risk of removal and effects on milk production associated with paratuberculosis status in dairy cows. J Am Vet Med Assoc. 2005;227: 1975–1981. doi: 10.2460/javma.2005.227.1975 16379637

6. Raizman EA, Fetrow JP, Wells SJ, Godden SM, Oakes MJ, Vazquez G. The association between Mycobacterium avium subsp. paratuberculosis fecal shedding or clinical Johne’s disease and lactation performance on two Minnesota, USA dairy farms. Prev Vet Med. 2007;78: 179–195. doi: 10.1016/j.prevetmed.2006.10.006 17118473

7. Gonda MG, Chang YM, Shook GE, Collins MT, Kirkpatrick BW. Effect of Mycobacterium paratuberculosis infection on production, reproduction, and health traits in US Holsteins. Prev Vet Med. 2007;80: 103–119. doi: 10.1016/j.prevetmed.2007.01.011 17350703

8. Sorge US, Lissemore KD, Godkin A, Hendrick SH, Wells SJ, Kelton DF. Associations between paratuberculosis milk ELISA result, milk production, and breed in Canadian dairy cows. J Dairy Sci. 2011;94: 754–761. doi: 10.3168/jds.2010-3404 21257043

9. Smith RL, Gröhn YT, Pradhan AK, Whitlock RH, Van Kessel JS, Smith JM, et al. The effects of progressing and nonprogressing Mycobacterium avium ssp. paratuberculosis infection on milk production in dairy cows. J Dairy Sci. 2016;99: 1383–1390. doi: 10.3168/jds.2015-9822 26686721

10. Vanleeuwen JA, Haddad JP, Dohoo IR, Keefe GP, Tiwari A, Tremblay R. Associations between reproductive performance and seropositivity for bovine leukemia virus, bovine viral-diarrhea virus, Mycobacterium avium subspecies paratuberculosis, and Neospora caninum in Canadian dairy cows. Prev Vet Med. 2010;94: 54–64. doi: 10.1016/j.prevetmed.2009.11.012 20015556

11. Smith RL, Strawderman RL, Schukken YH, Wells SJ, Pradhan AK, Espejo LA, et al. The effect of Johne’s disease status on reproduction and culling in dairy cattle. J Dairy Sci. 2010;93: 3513–3524. doi: 10.3168/jds.2009-2742 20655419

12. Marcé C, Beaudeau F, Bareille N, Seegers H, Fourichon C. Higher non-return rate associated with Mycobacterium avium subspecies paratuberculosis infection at early stage in Holstein dairy cows. Theriogenology. 2009;71: 807–16. doi: 10.1016/j.theriogenology.2008.10.017 19117602

13. Tiwari A, VanLeeuwen JA, Dohoo IR, Stryhn H, Keefe GP, Haddad JP. 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. doi: 10.1016/j.vetmic.2005.05.011 15970402

14. Barkema HW, Orsel K, Nielsen SS, Koets AP, Rutten VPMG, Bannantine JP, et al. Knowledge gaps that hamper prevention and control of Mycobacterium avium subspecies paratuberculosis infection. Transbound Emerg Dis. 2017;65: 125–148. doi: 10.1111/tbed.12723 28941207

15. Moravkova M, Babak V, Kralova a, Pavlik I, Slana I. Culture and quantitative IS900 Real-time PCR-based analysis of the persistence of Mycobacterium avium subsp. paratuberculosis in a controlled dairy cow farm environment. Appl Environ Microbiol. 2012;78: 6608. doi: 10.1128/AEM.01264-12 22773642

16. Ferrouillet C, Wells SJ, Hartmann WL, Godden SM, Carrier J. Decrease of Johne’s disease prevalence and incidence in six Minnesota, USA, dairy cattle herds on a long-term management program. PrevVetMed. 2009;88: 128–137.

17. Garcia AB, Shalloo L. Invited review : The economic impact and control of paratuberculosis in cattle. J Dairy Sci. 2015;98: 1–21.

18. Pillars RB, Grooms DL, Wolf CA, Kaneene JB. Economic evaluation of Johne’s disease control programs implemented in Michigan dairy farms. Prev Vet Med. 2009;90: 223–232. doi: 10.1016/j.prevetmed.2009.04.009 19464741

19. Radia D, Bond K, Limon G, van Winden S, Guitian J. Relationship between periparturient management, prevalence of MAP and preventable economic losses in UK dairy herds. Vet Rec. 2013;173: 343–+. doi: 10.1136/vr.101408 23897995

20. Groenendaal H, Wolf CA. Farm-level economic analysis of the US national Johne’s Disease Demonstration Herd Project. J Am Vet Med Assoc. 2008;233: 1852–1858. doi: 10.2460/javma.233.12.1852 19072597

21. Wolf R, Clement F, Barkema HW, Orsel K. Economic evaluation of participation in a voluntary Johne’s disease prevention and control program from a farmer’s perspective-The Alberta Johne’s Disease Initiative. J Dairy Sci. 2014;97: 2822–34. doi: 10.3168/jds.2013-7454 24582447

22. Robins J, Bogen S, Francis A, Westhoek A, Kanarek A, Lenhart S, et al. Agent-based model for Johne’s disease dynamics in a dairy herd. Vet Res. 2015;46: 68. doi: 10.1186/s13567-015-0195-y 26091904

23. Kudahl AB, Sørensen JT, Nielsen SS, Østergaard S. Simulated economic effects of improving the sensitivity of a diagnostic test in paratuberculosis control. Prev Vet Med. 2007;78: 118–29. doi: 10.1016/j.prevetmed.2006.10.004 17101188

24. Kudahl AB, Nielsen SS, Østergaard S. Economy, efficacy, and feasibility of a risk-based control program against paratuberculosis. J Dairy Sci. 2008;91: 4599–609. doi: 10.3168/jds.2008-1257 19038935

25. Groenendaal H, Galligan DT. Economic consequences of control programs for paratuberculosis in midsize dairy farms in the United States. J Am Vet Med Assoc. 2003;223: 1757–1763. doi: 10.2460/javma.2003.223.1757 14690205

26. Aly SS, Anderson RJ, Whitlock RH, Fyock TL, McAdams SC, Byrem TM, et al. Cost-effectiveness of diagnostic strategies to identify Mycobacterium avium subspecies paratuberculosis super-shedder cows in a large dairy herd using antibody enzyme-linked immunosorbent assays, quantitative real-time polymerase chain reaction, and bacte. J Vet Diagnostic Investig. 2012;24: 821–32. doi: 10.1177/1040638712452107 22807510

27. Cho J, Tauer LW, Schukken YH, Smith RL, Lu Z, Gröhn YT. Cost Effective Control Strategies for Johne’s Disease in Dairy Herds. Can J Agric Econ. 2013;61: 583–608. doi: 10.1111/j.1744-7976.2012.01270.x

28. Massaro T, Lenhart S, Spence M, Drakes C, Yang G, Agusto F, et al. Modeling For Cost Analysis Of Johne’s Disease Control Based On EVELISA Testing. J Biol Syst. 2013;21: 1340010. doi: 10.1142/S021833901340010X

29. Dorshorst NC, Collins MT, Lombard JE. Decision analysis model for paratuberculosis control in commercial dairy herds. Prev Vet Med. 2006;75: 92–122. Available: 16564101

30. Konboon M, Bani-yaghoub M, Id POP, Rhee N, Id SA. A nested compartmental model to assess the efficacy of paratuberculosis control measures on U. S. dairy farms. 2018; 1–25.

31. Smith RL, Al-Mamun MA, Gröhn YT. Economic consequences of paratuberculosis control in dairy cattle: A stochastic modeling study. Prev Vet Med. 2017;138: 17–27. doi: 10.1016/j.prevetmed.2017.01.007 28237232

32. Diéguez FJ, Arnaiz I, Sanjuan ML, Vilar MJ, Yus E. Management practices associated with Mycobacterium avium subspecies paratuberculosis infection and the effects of the infection on dairy herds. Vet Rec. 2008;162: 614–617. doi: 10.1136/vr.162.19.614 18480020

33. Arrazuria R, Arnaiz I, Fouz R, Calvo C, Eiras C, Diaguez F. Association between Mycobacterium avium subsp. paratuberculosis infection and culling in dairy cattle herds Asociación entre la infección por Mycobacterium avium subsp. paratuberculosis y las causas de eliminación en rebaños de ganado lechero. Arch Med Vet. 2008;44: 39–44. doi: 10.4067/S0301-732X2014000100006

34. Rossi G, Gröhn YT, Schukken YHYHYH, Smith RL. The effect of Mycobacterium avium subspecies paratuberculosis infection on clinical mastitis occurrence in dairy cows. J Dairy Sci. 2017;100: 7446–7454. doi: 10.3168/jds.2017-12721 28711261

35. Smith RL, Schukken YH, Gröhn YT. A new compartmental model of Mycobacterium avium subsp paratuberculosis infection dynamics in cattle. Prev Vet Med. 2015;122: 298–305. doi: 10.1016/j.prevetmed.2015.10.008 26520176

36. Pradhan AK, Van Kessel JAS, Karns JS, Wolfgang DR, Hovingh E, Nelen KA, et al. Dynamics of endemic infectious diseases of animal and human importance on three dairy herds in the northeastern United States. J Dairy Sci. 2009;92: 1811–1825. doi: 10.3168/jds.2008-1486 19307664

37. Bar D, Tauer LW, Bennett GJ, González RN, Hertl JA, Schukken YH, et al. The cost of generic clinical mastitis in dairy cows as estimated by using dynamic programming. J Dairy Sci. 2008;91: 2205–14. doi: 10.3168/jds.2007-0573 18487643

38. Levy H. Stochastic Dominance and Expected Utility : Survey and Analysis. 1Management Sci. 1992;38: 555–593.

39. Harris TR, Mapp HP. A Stochastic Dominance Comparison of Water-Conserving Irrigation Strategies. Am J Agric Econ. 1986;68: 298. doi: 10.2307/1241431

40. Carnell R. lhs: Latin Hypercube Samples [Internet]. 2017.

41. Mitchell RM, Whitlock RH, Gröhn YT, Schukken YH. Back to the real world: Connecting models with data. Prev Vet Med. 2015;118: 215–225. doi: 10.1016/j.prevetmed.2014.12.009 25583453

42. Smith RL, Al-Mamun MA, Gröhn YT. Economic consequences of paratuberculosis control in dairy cattle: A stochastic modeling study. Prev Vet Med. 2017;138: 17–27. doi: 10.1016/j.prevetmed.2017.01.007 28237232

43. Collins MT, Eggleston V, Manning EJB. Successful control of Johne’s disease in nine dairy herds: results of a six-year field trial. J Dairy Sci. 2010;93: 1638–43. doi: 10.3168/jds.2009-2664 20338441

44. Benedictus A, Mitchell RM, Linde-Widmann M, Sweeney RW, Fyock TL, Schukken YH, et al. Transmission parameters of Mycobacterium avium subspecies paratuberculosis infections in a dairy herd going through a control program. Prev Vet Med. 2008;83: 215–227. doi: 10.1016/j.prevetmed.2007.07.008 17868937

45. Nielsen SS, Toft N. Effect of management practices on paratuberculosis prevalence in Danish dairy herds. J Dairy Sci. 2011;94: 1849–1857. doi: 10.3168/jds.2010-3817 21426974

46. Clark DL, Koziczkowski JJ, Radcliff RP, Carlson RA, Ellingson JLE. Detection of Mycobacterium avium subspecies paratuberculosis: comparing fecal culture versus serum enzyme-linked immunosorbent assay and direct fecal polymerase chain reaction. J Dairy Sci. 2008;91: 2620–7. doi: 10.3168/jds.2007-0902 18565921

47. Sweeney RW, Whitlock RH, McAdams SC, Fyock TL. Longitudinal Study of ELISA Seroreactivity to Mycobacterium Avium subsp. Paratuberculosis in Infected Cattle and Culture-Negative Herd Mates. J Vet Diagnostic Investig. 2006;18: 2–6. doi: 10.1177/104063870601800102 16566252

48. van Schaik G, Stehman SM, Jacobson RH, Schukken YH, Shin SJ, Lein DH. Cow-level evaluation of a kinetics ELISA with multiple cutoff values to detect fecal shedding of Mycobacterium avium subspecies paratuberculosis in New York State dairy cows. Prev Vet Med. 2005;72: 221–236. doi: 10.1016/j.prevetmed.2005.01.019 16169619

49. Collins MT, Gardner IA, Garry F, Roussel AJ, Wells SJ. 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. Available: 17173528

50. Whitlock RH, Wells SJ, Sweeney RW, Van Tiem J. ELISA and fecal culture for paratuberculosis (Johne’s disease): sensitivity and specificity of each method. Vet Microbiol. 2000;77: 387–398. Available: 11118724

51. Taddei S, Robbi C, Cesena C, Rossi I, Schiano E, Arrigoni N, et al. Detection of Mycobacterium Avium Subsp. Paratuberculosis in Bovine Fecal Samples: Comparison of Three Polymerase Chain Reaction—Based Diagnostic Tests with a Conventional Culture Method. J Vet Diagnostic Investig. 2004;16: 503–508. doi: 10.1177/104063870401600603 15586564

52. Leite FL, Stokes KD, Robbe-Austerman S, Stabel JR. Comparison of fecal DNA extraction kits for the detection of Mycobacterium avium subsp. paratuberculosis by polymerase chain reaction. J Vet Diagnostic Investig. 2013;25: 27–34. doi: 10.1177/1040638712466395 23166181

53. Meens E, Rambaud T, Arnaud D. Evaluation of diagnostic tests to classify cattle, in control plans, according to their levels of excretion of Mycobacterium avium Paratuberculosis. 12th International Colloquium on Paratuberculosis. Parma, Italy; 2014. p. P-03.13.

54. Vitale N, Possidente R, D’Errico V, Dondo A, Bergagna S, Barbero R, et al. Estimating diagnostic accuracy of paratuberculosis (PTB) diagnostic test with latent class models. 12th International Colloquium on Paratuberculosis. Parma, Italy; 2014. p. P-02.10.

55. Sweeney RW, Gardner IA, Hines MEI, Anderson R, Byrem TM, Collins MT, et al. Comparison of 3 fecal culture, 2 fecal PCR, 2 serum ELISA, and milk ELISA for diagnosis of paratuberculosis in US dairy cattle. 12th International Colloquium on Paratuberculosis. Parma, Italy; 2014. p. P-02.47.

56. Adaska JM, Anderson RJ. Seroprevalence of Johne’s-disease infection in dairy cattle in California, USA. Prev Vet Med. 2003;60: 255–261. 12900163

57. Cornell University Animal Health Diagnostic Center. Test and Fee Schedule [Internet]. 2015.

58. Collins MT, Manning EJB. Testing Services. In: Johne’s Information Center [Internet]. 2015.

59. Besser T. New Strategies for Johne’s Disease Testing. In: Washington Animal Disease Diagnostic Lab [Internet]. 2015 [cited 10 Dec 2015].’s-testing

60. Tests and Fees. In: Iowa State Veterinary Diagnostic Laboratory [Internet]. 2015 [cited 10 Dec 2015].

61. Indiana Animal Disease Diagnostic Laboratory. Fee Schedule [Internet]. 2015 [cited 10 Dec 2015].

62. USDA:ERS. National Milk Cost of Production. In: Milk Cost of Production Estimates [Internet]. 2010 [cited 9 Sep 2015].

63. Karszes J. Dairy Replacement Programs : Costs & Analysis 3 rd Quarter 2012. 2014;

64. USDA:NASS. Quick Stats. In: Quick Stats. 2015.

65. USDA. Agricultural Prices Summary 2003–2007. In: Agricultural Prices [Internet]. 2008.

66. Bar D, Gröhn YT, Bennett GJ, González RN, Hertl JA, Schulte HF, et al. Effect of repeated episodes of generic clinical mastitis on milk yield in dairy cows. J Dairy Sci. 2007;90: 4643–53. doi: 10.3168/jds.2007-0145 17881685

67. Groenendaal H, Nielen M, Jalvingh AW, Horst SH, Galligan DT, Hesselink JW. A simulation of Johne’s disease control. Prev Vet Med. 2002;54: 225–245. Available: 12114011

68. Breen JE, Green MJ, Bradley AJ. Quarter and cow risk factors associated with the occurrence of clinical mastitis in dairy cows in the United Kingdom. J Dairy Sci. 2009;92: 2551–61. doi: 10.3168/jds.2008-1369 19447987

69. Verteramo Chiu LJ, Tauer LW, Al-Mamun MA, Kaniyamattam K, Smith RL, Gröhn YT. An agent-based model evaluation of economic control strategies for paratuberculosis in a dairy herd. J Dairy Sci. 2018; doi: 10.3168/jds.2017-13175 29705432

Článek vyšel v časopise


2019 Číslo 9

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…

Kurzy Doporučená témata