Cover Journal of the American Veterinary Medical Association
Journal of the American Veterinary Medical Association
ISSN:
0003-1488
Publication Date:
15 Jul 2017

  • 1. Schmitt SM, Fitzgerald SD, Cooley TM, et al. Bovine tuberculosis in free-ranging white-tailed deer in Michigan. J Wildl Dis 1997; 33: 749–758.

    • Search Google Scholar
    • Export Citation

  • 2. Okafor CC, Grooms DL, Bruning-Fann CS, et al. Descriptive epidemiology of bovine tuberculosis in Michigan (1975–2010): lessons learned. Vet Med Int 2011; 2011: 874924.

    • Search Google Scholar
    • Export Citation

  • 3. Kaneene JB, VanderKlok M, Bruning-Fann CS, et al. Prevalence of Mycobacterium bovis infection in cervids on privately owned ranches. J Am Vet Med Assoc 2002; 220: 656–659.

    • Search Google Scholar
    • Export Citation

  • 4. USDA APHIS. Bovine tuberculosis eradication uniform methods and rules, effective January 1, 2005. Available at: www.aphis.usda.gov/animal_health/animal_diseases/tuberculosis/downloads/tb-umr.pdf. Accessed Mar 31, 2017.

  • 5. USDA Food Safety and Inspection Service. Guideline Number 4. Inspection of tuberculin reactors. Available at: www.fsis.usda.gov/wps/wcm/connect/9b50790b-3875-4a76-a565-8fc7f374043e/TB_Guideline_4_88.pdf?MOD=AJPERES. Accessed Mar 31, 2017.

  • 6. Miller JM, Jenny AL, Payeur JB. Polymerase chain reaction detection of Mycobacterium tuberculosis complex and Mycobacterium avium organisms in formalin-fixed tissues from culture-negative ruminants. Vet Microbiol 2002; 87: 15–23.

    • Search Google Scholar
    • Export Citation

  • 7. Robbe-Austerman S, Bravo DM, Harris B. Comparison of the MGIT 960, BACTEC 460 TB and solid media for isolation of Mycobacterium bovis in United States veterinary specimens. BMC Vet Res 2013; 9: 74.

    • Search Google Scholar
    • Export Citation

  • 8. Bradner L, Robbe-Austerman S, Beitz DC, et al. Chemical decontamination with N-acetyl-l-cysteine–sodium hydroxide improves recovery of viable Mycobacterium avium subsp paratuberculosis organisms from cultured milk. J Clin Microbiol 2013; 51: 2139–2146.

    • Search Google Scholar
    • Export Citation

  • 9. Higgins J, Camp P, Farrell D, et al. Identification of Mycobacterium spp of veterinary importance using rpoB gene sequencing. BMC Vet Res 2011; 7: 77.

    • Search Google Scholar
    • Export Citation

  • 10. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25: 1754–1760.

  • 11. Li H, Handsaker B, Wysoker A, et al. The sequence alignment/map format and SAMtools. Bioinformatics 2009; 25: 2078–2079.

  • 12. DePristo MA, Banks E, Poplin R, et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 2011; 43: 491–498.

    • Search Google Scholar
    • Export Citation

  • 13. Van der Auwera GA, Carneiro MO, Hartl C, et al. From FastQ data to high confidence variant calls: the Genome Analysis Toolkit best practices pipeline. Curr Protoc Bioinformatics 2013; 11: 11.10.1–11.10.33.

    • Search Google Scholar
    • Export Citation

  • 14. McKenna A, Hanna M, Banks E, et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010; 20: 1297–1303.

    • Search Google Scholar
    • Export Citation

  • 15. International Union of Pure and Applied Chemistry and International Union of Biochemistry and Molecular Biology Joint Commission on Biochemical Nomenclature and Nomenclature Commission of IUBMB. In: Liebecq C, ed. Biochemical nomenaclature: and related documents: a compendium. 2nd ed. London: Portland Press Ltd, 1992; 122–126.

    • Search Google Scholar
    • Export Citation

  • 16. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30: 1312–1313.

    • Search Google Scholar
    • Export Citation

  • 17. Robinson JT, Thorvaldsdóttir H, Winckler W, et al. Integrative genomics viewer. Nat Biotechnol 2011; 29: 24–26.

  • 18. Fitzgerald SD, Hollinger C, Mullaney TP, et al. Herd outbreak of bovine tuberculosis illustrates that route of infection correlates with anatomic distribution of lesions in cattle and cats. J Vet Diagn Invest 2016; 28: 129–132.

    • Search Google Scholar
    • Export Citation

  • 19. Memorandum of Understanding Between Michigan Department of Agriculture and Rural Development and the Michigan Department of Natural Resources and the United States Department of Agriculture. Available at: www.michigan.gov/documents/emergingdiseases/MOU_TB_MDARD_MDNR_USDA_signed_051916_526238_7.pdf. Accessed Mar 31, 2017.

  • 20. USDA APHIS. Guidelines for surveillance of bovine tuberculosis in wildlife. June 2011. Available at: www.aphis.usda.gov/animal_health/animal_diseases/tuberculosis/downloads/wildlife_tb_surv_manual.pdf. Accessed Mar 31, 2017.

  • 21. Michigan Department of Natural Resources. Michigan deer management plan. Appendix D: a review of deer management in Michigan. Available at: www.michigan.gov/dnr/0,4570,7-153-10363_41153—,00.html. Accessed Mar 3, 2016.

  • 22. O'Brien DJ, Fitzgerald SD, Lyon TJ, et al. Tuberculous lesions in free-ranging white-tailed deer in Michigan. J Wildl Dis 2001; 37: 608–613.

    • Search Google Scholar
    • Export Citation

  • 23. O'Brien DJ, Schmitt SM, Fierke JS, et al. Epidemiology of Mycobacterium bovis in free-ranging white-tailed deer, Michigan, USA, 1995–2000. Prev Vet Med 2002; 54: 47–63.

    • Search Google Scholar
    • Export Citation

  • 24. Bruning-Fann CS, Schmitt SM, Fitzgerald SD, et al. Mycobacterium bovis in coyotes from Michigan. J Wildl Dis 1998; 34: 632–636.

  • 25. Bruning-Fann CS, Schmitt SM, Fitzgerald SD, et al. Bovine tuberculosis in free-ranging carnivores from Michigan. J Wildl Dis 2001; 37: 58–64.

    • Search Google Scholar
    • Export Citation

  • 26. Walter WD, Fischer JW, Anderson CW. Surveillance and movements of Virginia opossum (Didelphis virginiana) in the bovine tuberculosis region of Michigan. Epidemiol Infect 2013; 141: 1498–1508.

    • Search Google Scholar
    • Export Citation

  • 27. O'Brien DJ, Schmitt SM, Fitzgerald SD, et al. Management of bovine tuberculosis in Michigan wildlife: current status and near term prospects. Vet Microbiol 2011; 151: 179–187.

    • Search Google Scholar
    • Export Citation

  • 28. Brooks-Pollock E, Conlan AJ, Mitchell AP, et al. Age-dependent patterns of bovine tuberculosis in cattle. Vet Res 2013; 44: 97.

  • 29. Francisco TI, Orloski KA, Roberts NJ. Investigation of a Mycobacterium bovis outbreak in cattle at a Colorado dairy in 2010. J Am Vet Med Assoc 2014; 244: 805–812.

    • Search Google Scholar
    • Export Citation

  • 30. Roetzer A, Diel R, Kohl TA, et al. Whole genome sequencing versus traditional genotyping for investigation of a Mycobacterium tuberculosis outbreak: a longitudinal molecular epidemiological study. PLoS Med 2013; 10:e1001387.

    • Search Google Scholar
    • Export Citation

  • 31. de la Rua-Domenech R, Goodchild AT, Vordermeier HM, et al. Ante mortem diagnosis of tuberculosis in cattle: a review of the tuberculin tests, γ-interferon assay and other ancillary diagnostic techniques. Res Vet Sci 2006; 81: 190–210.

    • Search Google Scholar
    • Export Citation

  • 32. Cagiola M, Feliziani F, Severi G, et al. Analysis of possible factors affecting the specificity of the gamma interferon test in tuberculosis-free cattle herds. Clin Diagn Lab Immunol 2004; 11: 952–956.

    • Search Google Scholar
    • Export Citation

  • 33. Holsinger VH, Rajkowski KT, Stabel JR. Milk pasteurisation and safety: a brief history and update. Rev Sci Tech 1997; 16: 441–451.

  • 34. Hurley WL, Theil PK. Perspectives on immunoglobulins in colostrum and milk. Nutrients 2011; 3: 442–474.

  • 35. Claeys WL, Cardoen S, Daube G, et al. Raw or heated cow milk consumption: review of risks and benefits. Food Control 2013; 31: 251–262.

    • Search Google Scholar
    • Export Citation

  • 36. Langer AJ, Ayers T, Grass J, et al. Nonpasteurized dairy products, disease outbreaks, and state laws—United States, 1993–2006. Emerg Infect Dis 2012; 18: 385–391.

    • Search Google Scholar
    • Export Citation

  • 37. Zarden CF, Marassi CD, Figueiredo EE, et al. Mycobacterium bovis detection from milk of negative skin test cows. Vet Rec 2013; 172: 130.

    • Search Google Scholar
    • Export Citation

Advertisement

Use of whole-genome sequencing and evaluation of the apparent sensitivity and specificity of antemortem tuberculosis tests in the investigation of an unusual outbreak of Mycobacterium bovis infection in a Michigan dairy herd

Colleen S. Bruning-Fann DVM, MS1, Suelee Robbe-Austerman DVM, PhD2, John B. Kaneene DVM, MPH, PhD3, Bruce V. Thomsen DVM, PhD4, John D. Tilden Jr DVM, MPH5, Jean S. Ray DVM, PhD6, Richard W. Smith DVM7, Scott D. Fitzgerald DVM, PhD8, Steven R. Bolin DVM, PhD9, Daniel J. O'Brien DVM, PhD10, Thomas P. Mullaney MVB, PhD11, Tod P. Stuber BS12, James J. Averill DVM, PhD13, and David Marks MS14
View More View Less
  • 1 Veterinary Services, APHIS, USDA, 3001 Coolidge Rd #325, East Lansing, MI 48823.
  • | 2 National Veterinary Services Laboratories, APHIS, USDA, 1920 Dayton Ave, Ames, IA, 50010.
  • | 3 Center for Comparative Epidemiology, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824.
  • | 4 National Veterinary Services Laboratories, APHIS, USDA, 1920 Dayton Ave, Ames, IA, 50010.
  • | 5 Food and Dairy Divisions, Michigan Department of Agriculture and Rural Development, 525 W Allegan St, Lansing, MI 48933.
  • | 6 Veterinary Services, APHIS, USDA, 3001 Coolidge Rd #325, East Lansing, MI 48823.
  • | 7 Animal Industry Divisions, Michigan Department of Agriculture and Rural Development, 525 W Allegan St, Lansing, MI 48933.
  • | 8 Diagnostic Center for Population and Animal Health, College of Veterinary Medicine, Michigan State University, Lansing, MI 48910.
  • | 9 Diagnostic Center for Population and Animal Health, College of Veterinary Medicine, Michigan State University, Lansing, MI 48910.
  • | 10 Wildlife Disease Laboratory, Michigan Department of Natural Resources, 4125 Beaumont Rd, Lansing, MI 48910.
  • | 11 Diagnostic Center for Population and Animal Health, College of Veterinary Medicine, Michigan State University, Lansing, MI 48910.
  • | 12 National Veterinary Services Laboratories, APHIS, USDA, 1920 Dayton Ave, Ames, IA, 50010.
  • | 13 Animal Industry Divisions, Michigan Department of Agriculture and Rural Development, 525 W Allegan St, Lansing, MI 48933.
  • | 14 Wildlife Services, APHIS, USDA, 2651 Coolidge Rd #101, East Lansing, 48823.
DOI:
https://doi.org/10.2460/javma.251.2.206
Volume/Issue:
Volume 251: Issue 2
Online Publication Date:
15 Jul 2017
Restricted access
Reprints and Permissions Purchase Article

Abstract

OBJECTIVE To describe use of whole-genome sequencing (WGS) and evaluate the apparent sensitivity and specificity of antemortem tuberculosis tests during investigation of an unusual outbreak of Mycobacterium bovis infection in a Michigan dairy herd.

DESIGN Bovine tuberculosis (bTB) outbreak investigation.

ANIMALS Cattle, cats, dog, and wildlife.

PROCEDURES All cattle in the index dairy herd were screened for bTB with the caudal fold test (CFT), and cattle ≥ 6 months old were also screened with a γ-interferon (γIFN) assay. The index herd was depopulated along with all barn cats and a dog that were fed unpasteurized milk from the herd. Select isolates from M bovis–infected animals from the index herd and other bTB-affected herds underwent WGS. Wildlife around all affected premises was examined for bTB.

RESULTS No evidence of bTB was found in any wildlife examined. Within the index herd, 53 of 451 (11.8%) cattle and 12 of 21 (57%) cats were confirmed to be infected with M bovis. Prevalence of M bovis–infected cattle was greatest among 4- to 7-month-old calves (16/49 [33%]) followed by adult cows (36/203 [18%]). The apparent sensitivity and specificity were 86.8% and 92.7% for the CFT and 80.4% and 96.5% for the γIFN assay when results for those tests were interpreted separately and 96.1% and 91.7% when results were interpreted in parallel. Results of WGS revealed that M bovis–infected barn cats and cattle from the index herd and 6 beef operations were infected with the same strain of M bovis. Of the 6 bTB-affected beef operations identified during the investigation, 3 were linked to the index herd only by WGS results; there was no record of movement of livestock or waste milk from the index herd to those operations.

CONCLUSIONS AND CLINICAL RELEVANCE Whole-genome sequencing enhanced the epidemiological investigation and should be used in all disease investigations. Performing the CFT and γIFN assay in parallel improved the antemortem ability to detect M bovis–infected animals. Contact with M bovis–infected cattle and contaminated milk were major risk factors for transmission of bTB within and between herds of this outbreak.

Abstract

OBJECTIVE To describe use of whole-genome sequencing (WGS) and evaluate the apparent sensitivity and specificity of antemortem tuberculosis tests during investigation of an unusual outbreak of Mycobacterium bovis infection in a Michigan dairy herd.

DESIGN Bovine tuberculosis (bTB) outbreak investigation.

ANIMALS Cattle, cats, dog, and wildlife.

PROCEDURES All cattle in the index dairy herd were screened for bTB with the caudal fold test (CFT), and cattle ≥ 6 months old were also screened with a γ-interferon (γIFN) assay. The index herd was depopulated along with all barn cats and a dog that were fed unpasteurized milk from the herd. Select isolates from M bovis–infected animals from the index herd and other bTB-affected herds underwent WGS. Wildlife around all affected premises was examined for bTB.

RESULTS No evidence of bTB was found in any wildlife examined. Within the index herd, 53 of 451 (11.8%) cattle and 12 of 21 (57%) cats were confirmed to be infected with M bovis. Prevalence of M bovis–infected cattle was greatest among 4- to 7-month-old calves (16/49 [33%]) followed by adult cows (36/203 [18%]). The apparent sensitivity and specificity were 86.8% and 92.7% for the CFT and 80.4% and 96.5% for the γIFN assay when results for those tests were interpreted separately and 96.1% and 91.7% when results were interpreted in parallel. Results of WGS revealed that M bovis–infected barn cats and cattle from the index herd and 6 beef operations were infected with the same strain of M bovis. Of the 6 bTB-affected beef operations identified during the investigation, 3 were linked to the index herd only by WGS results; there was no record of movement of livestock or waste milk from the index herd to those operations.

CONCLUSIONS AND CLINICAL RELEVANCE Whole-genome sequencing enhanced the epidemiological investigation and should be used in all disease investigations. Performing the CFT and γIFN assay in parallel improved the antemortem ability to detect M bovis–infected animals. Contact with M bovis–infected cattle and contaminated milk were major risk factors for transmission of bTB within and between herds of this outbreak.

Supplementary Materials

    • Supplementary Table S1 (PDF 611 kb)
    • Supplementary Table S2 (PDF 616 kb)

Contributor Notes

Mr. Marks' present address is Wildlife Services, APHIS, USDA, 11213 Aurora Ave, Urbandale, IA 50322.

Address correspondence to Dr. Kaneene (kaneenej@cvm.msu.edu).