Age at which dairy cattle become Mycobacterium avium subsp. paratuberculosis faecal culture positive

https://doi.org/10.1016/j.prevetmed.2010.07.004Get rights and content

Abstract

Age at which cattle become faecal culture positive for Mycobacterium avium subsp. paratuberculosis (Map) can be used as a proxy parameter for age at onset of faecal shedding, which is an important parameter in the control of Map in cattle herds. To investigate the age at becoming faecal culture positive, survival analysis methods were applied. The analyses were carried out on asynchronous interval censored data of faecal culture results of samples collected from 18,979 female Holstein-Frisian cattle in 353 Dutch herds between 1996 and 2002. The data were analysed with a Weibull proportional hazards model.

The results indicate that the distribution of age at onset of faecal shedding in Holstein-Frisian dairy cattle in infected herds is associated with the within-herd prevalence. In higher classes of apparent prevalence, cattle started to shed Map at younger age on average. In herds with an apparent prevalence <0.05, 0.05–0.1, 0.1–0.2 and ≥0.2, the proportion (95% CI) of cattle with onset of faecal shedding before 2 years of age was estimated at 1% (0.5%; 2%), 4% (3%; 5%), 8% (5%; 10%) and 20% (11%; 32%), respectively.

This study indicates that a considerable proportion of young stock is shedding Map, especially in high prevalence herds. Therefore, infectious young stock should be a major concern in the control of paratuberculosis.

Introduction

Paratuberculosis (or Johne's disease) in cattle is an infectious disease caused by Mycobacterium avium subsp. paratuberculosis (Map). The disease is widespread world-wide and causes significant economic losses. Control programmes for paratuberculosis are based on improvement of farm management (e.g., separation of young stock from adult cattle) and on early culling of infected cattle to reduce transmission of Map within a herd.

In the development of control programmes, it has frequently been assumed that young stock do not become infectious. Provided that adult cattle are highly resistant to infection, this assumption means that effective separation of young stock from adult cattle largely prevents postnatal infection. However, this assumption is in contrast with observed faecal shedding of Map in experimentally infected young stock (Rankin, 1959, Rankin, 1961, McDonald et al., 1999, Waters et al., 2003), young stock exposed to experimentally infected cattle (Rankin, 1961, van Roermund et al., 2007) and naturally infected young stock (Kalis et al., 1999, McDonald et al., 1999, Waters et al., 2003, Antognoli et al., 2007). Moreover, calf–calf transmission has experimentally been demonstrated (van Roermund et al., 2007).

The age at onset of faecal shedding depends on the progression of the infection within an infected individual. Progression of the infection depends on the age at infection and the infectious dose (Begg and Whittington, 2008, Mitchell et al., 2009), and these parameters are related to the within-herd prevalence. Also, genetic variation exists in dairy cattle for susceptibility to (progression of) infection with Map and faecal shedding of Map (Koets et al., 2000, Mortensen et al., 2004, Gonda et al., 2006, Hinger et al., 2008, Pinedo et al., 2009, Koets et al., 2010). This genetic variation may result in differences in susceptibility between breeds (Kirckpatrick, 2010). Therefore, the age at onset of faecal shedding might depend on within-herd prevalence and breed. However, the aforementioned studies demonstrating faecal shedding of Map in young stock (Rankin, 1959, Rankin, 1961, Kalis et al., 1999, McDonald et al., 1999, Waters et al., 2003, Antognoli et al., 2007, van Roermund et al., 2007) included only small numbers of cattle and herds, and quantitative data on the age at onset of faecal shedding were lacking. Therefore, the aim of the present study was to quantify the distribution of age at onset of faecal shedding in Holstein-Frisian dairy cattle in infected herds. The age at onset of faecal shedding was approximated by the age at which cattle become faecal culture positive.

Section snippets

Data

A database was set up containing test results of all bovine faecal samples submitted between 1st January 1996 and 31st December 2002 to the GD Animal Health Service's laboratory for individual faecal culture (IFC), or pooled faecal culture (PFC) for Map. To check for completeness, the annual numbers of results retrieved for each of the test methods were compared with numbers presented in financial reports of the laboratory. For all year and test combinations, results were retrieved for >95% of

Herds and cattle

Observations were obtained for 18,979 female pure Holstein-Frisian cattle (including all age groups) from 353 herds, for which at least one IFC result was available, a unique animal identification could be matched, and information on date of birth was available. From these 18,979 cattle, a total number of 30,438 individual faecal samples were cultured (Fig. 1). Of these 30,438 samples, 4343 samples were collected before 2 years of age, from 3182 cattle in 149 herds. The distribution of the

Discussion

In this study, the age distribution at onset of faecal shedding in dairy cattle in infected herds was approximated by the distribution of age at onset of detectable faecal shedding of Map. The results indicate that this age distribution is strongly associated with the within-herd prevalence. In herds in higher prevalence classes, cattle start to shed Map at younger age on average (Fig. 3). A considerable proportion of cattle start shedding Map before 2 years of age, especially in high

Acknowledgements

This study was financially supported by the Dutch Ministry of Agriculture, Nature and Food Quality, and the Dutch Dairy Production Board. The authors would like to thank G. de Jong, A.P.W. de Roos and R. van Hoorne (NRS) for providing the pedigree records, A. Luppen and H.B.M. Assink for providing access to the laboratory results, and H. Brouwer-Middelesch for advice on SAS. Comments of H. Groenendaal, T.J.G.M. Lam, H.J.W. van Roermund, H.J. van Weering and the reviewers and editors on the

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