Transmission parameters of Mycobacterium avium subspecies paratuberculosis infections in a dairy herd going through a control program

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Abstract

A Johne's disease control program, including stringent management practices and a test-and-cull program (whole-herd fecal-samples taken twice a year), was implemented on a medium-sized Pennsylvania dairy farm that was suffering losses from clinical Johne's disease. The data that emerged from the control program, combined with birthdates, culling dates, lactation information and pedigrees, yielded an extensive longitudinal dataset. The dataset was processed through SAS 9.1 for statistical analysis; herd-level disease dynamics and dam-to-daughter transmission parameters were calculated. After the implementation of the program in 1984, prevalence dropped dramatically from 60% to less than 20% in 1989. After an apparent prevalence peak (25%) in 1991 due to improved test sensitivity, prevalence maintained a plateau of 10% from 1996 to 2000. After the implementation of the program, 9.5% of the offspring from test-negative dams and 26.8% of the offspring from known-infected dams became infected with Mycobacterium avium subspecies paratuberculosis (Map) (χ2 = 14.7; p = 0.0001). Calves born shortly following the calving of an infected dam and calves growing up with a future high shedder were more likely to be infected compared to calves without this risk profile. It was concluded that, after the implementation of the control program, the most important causes of infections of susceptible calves were their own dams or infected animals which had calved recently.

Introduction

Johne's disease or paratuberculosis is an incurable chronic wasting disease of ruminants that causes major economic losses to dairy farms all over the world (Ott et al., 1999). Johne's disease is caused by Mycobacterium avium subspecies paratuberculosis (Map) and is characterized by a very long incubation period (up to several years). There is a dose–response relationship between the exposure to Map and the severity and time to onset of clinical Johne's disease (Sweeney et al., 1992). Animals up to one year old are thought to be most susceptible to Map infection (Sweeney, 1996, Whitlock and Buergelt, 1996). Clinical signs include diarrhea, a decline in milk production and loss of body weight despite good appetite. Understanding of the transmission dynamics of Map is key to control programs that aim to eliminate Johne's disease on farm level. Previous studies modeling Johne's disease assumed that Map-infection on a dairy farm is only spread from infectious adults (≥2 years) to calves (Collins and Morgan, 1991, Groenendaal and Galligan, 2003). In the period preceding the onset of clinical symptoms, infected animals may intermittently spread (large) quantities of Map in their feces, milk and colostrum and thus infect susceptible calves (Nielsen et al., 2002, Aly and Thurmond, 2005). This subclinical shedding is generally thought to be the main factor in maintaining Map-infections in farms. However, in herds where all shedders are detected through routine screening and subsequently removed from the herd, Map is not eradicated, suggesting that additional transmission mechanisms play a role in maintaining Map in the population (Kalis et al., 2004). In this study we estimated parameters for the transmission of Map, based on the results from a longitudinal Johne's disease study on a Pennsylvania dairy farm. Several Map transmission patterns were evaluated, such as dam-to-daughter transmission, Map transmission to calves from unrelated adults and potential calf-to-calf transmission.

Section snippets

Herd description and outline of the study

This study analyzed fecal culture data from a medium-sized Pennsylvania dairy farm. The animals on the farm were mostly registered Guernseys. Between 1983 and 2003, the size of the lactating population increased from 40 to 90 cows. In the early 1980s, the farm suffered severe losses from Johne's disease, with several clinical cases per year. A Johne's disease control program was set up by veterinarians from the University of Pennsylvania at New Bolton Center (NBC). In January 1984, this Johne's

Descriptive statistics

During the first whole-herd fecal sampling in July 1983, there were 38 cows in the lactating population. Between the first sampling and the last sampling in May 2003, 436 more cows entered the lactating population for a total of 474 cows in the lactating population during the course of the control program. Of these 474 cows, 470 were assessed via fecal culture. The average number of samples taken per cow in the lactating population was 6.2 (S.D. = 3.97; Min = 0; Max = 25). The number of cows sampled

Discussion

The data in this paper come from a unique set of animals within one well-managed dairy herd over a period of approximately 20 years. Such well-documented, longitudinally followed populations are required to study infection dynamics in infections with a very slow progression. Although the number of observations may be small in some of the sub-analyses, the high quality and uniqueness of the data still provide for credibility of the observed relationships. We believe that the high quality of the

Acknowledgements

Support for this work was provided in part by the USDA Agricultural Research Service (Agreement No. 5823 23 12653156) for the Regional Dairy Quality Management Alliance. Support was also provided by the Johne's Disease Integrated Program (USDA contract 45105). Financial support was provided by the state of Pennsylvania.

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    However, in other herds all animals were fecal shedders at least once during the year. Although 1 yr is a limited time frame compared with other longitudinal studies that encompassed several years or even decades (such as Benedictus et al., 2008), it was our objective to focus on a realistic time period to aid in the farmers' decision-making and the control of disease. Despite the high value of longitudinal field data highlighted by previous studies (Mitchell et al., 2015b; Schukken et al., 2015), longitudinal field studies of MAP in dairy cattle continue to be scarce.

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