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Title: Environmental contamination with Mycobacterium avium subsp. paratuberculosis in endemically infected dairy herds

Author
item SMITH, R. - Cornell University
item SCHUKKEN, Y. - Cornell University
item PRADHAN, A. - Cornell University
item SMITH, J. - University Of Vermont
item WHITLOCK, R. - University Of Pennsylvania
item Van Kessel, Jo Ann
item WOLFGANG, D. - Pennsylvania State University
item GROHN, V. - Cornell University

Submitted to: Preventive Veterinary Medicine
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/22/2011
Publication Date: 10/1/2012
Citation: Smith, R., Schukken, Y., Pradhan, A., Smith, J., Whitlock, R., Van Kessel, J.S., Wolfgang, D., Grohn, V. 2012. Environmental contamination with Mycobacterium avium subsp. paratuberculosis in endemically infected dairy herds. Preventive Veterinary Medicine. 102:1-9.

Interpretive Summary: A large number of US dairy herds are positive for Johne’s disease and the dairy industry incurs large economic losses as a result of this insidious disease. Johne’s disease in cattle is caused by a chronic intestinal infection with Mycobacterium avium subsp. paratuberculosis (MAP), due to ingestion of the organism. After a long latent or dormant period, animals infected with MAP begin to shed the organism in their feces, thereby contaminating the farm environment. This environmental contamination with MAP is thought to be one of the primary sources of infection for dairy cattle. The exact link between fecal shedding of MAP by individual cows and environmental contamination levels at the herd level was explored with a cross-sectional analysis of longitudinally collected (over 6 years) samples on three dairy farms. In endemically infected herds, a high proportion of dairy cattle shedding MAP was found to increase both the odds of the herd environment being contaminated with MAP and the amount or concentration of MAP in the environment. A high average amount of MAP in the feces of animals was also predictive for both these MAP indicators. The relationship between MAP prevalence and environmental sample results also held at the pen level. Increased amounts of MAP in the pen environment were predictive of the presence of animals shedding high amounts of MAP. Environments without direct contact with adult cattle or their feces were unlikely to be contaminated with MAP. Environmental sampling of 6 manure collection points was found to have a relatively poor diagnostic sensitivity for the presence of MAP in a herd. Our data on three precisely documented herds would imply that environmental samples tend to underestimate the true herd prevalence of MAP. These results can be used to help the dairy industry develop dairy farm sampling strategies that are efficient at identifying MAP-positive and MAP-negative herds.

Technical Abstract: Environmental contamination with Mycobacterium avium subsp. paratuberculosis (MAP) is thought to be the primary source of infection for dairy cattle. The exact link between fecal shedding of MAP by individual cows and environmental contamination levels at the herd level was explored with a cross-sectional analysis of longitudinally collected samples on three dairy farms. Samples from multiple environmental sites in 3 commercial dairy herds in the Northeast US were cultured quarterly for MAP, providing 898 samples (113 (12.6%) were culture-positive), and all animals in the herds were tested biannually by fecal culture (FC), for 6 years. Of the environmental sites sampled, manure storage areas and shared alleyways were most likely to be culture-positive. Environmental sample results were compared to FC results from the concurrent or previous sampling date, where appropriate, at both the herd and the pen level. At the herd level a 1 log unit increase in average fecal shedding increased the odds of a positive environmental sample by 3.5 and increased the average amount of MAP in the sample by 2.1 cfu/g. At pen level, the odds were increased by a factor of 3 and the average amount of MAP was increased by 1.1 cfu/g. There was no significant relationship between environmental sample status and the distance between shedding animals and the sample’s location, and neighboring pens did not affect the results of the pen-level analysis. The amount of MAP in pen-level samples is positively correlated with the number of animals in the pen shedding >30 cfu/g of MAP. Of the 45 testing dates (42 FC positive) for which 6 environmental samples met the criteria for the U.S. Voluntary Bovine Johne’s Disease Control Program, 16 were positive, resulting in a herd sensitivity of 0.38 (95% CI: 0.23 to 0.52). None of the 3 FC negative testing dates produced positive environmental samples. Although environmental sampling can be used as a tool in understanding the level of MAP infection in a herd or pen, it is not a sensitive diagnostic method for herd positivity and should be used with caution.