In utero infection of cattle with Mycobacterium avium subsp. paratuberculosis: A critical review and meta-analysis

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Abstract

Mycobacterium avium subsp. paratuberculosis (Mptb) causes Johne’s disease in ruminants. Disease control programmes aim to break the faecal–oral cow–calf transmission cycle through hygienic calf rearing and removal of affected cows from the herd, but these programmes do not take account of the potential for congenital infection. The aims of this study were to critically review research on in utero infection, determine the prevalence of fetal infection in cattle through meta-analysis and estimate the incidence of calves infected via the in utero route. About 9% (95% confidence limits 6–14%) of fetuses from subclinically infected cows and 39% (20–60%) from clinically affected cows were infected with Mptb (P < 0.001). These are underestimates for methodological reasons. The estimated incidence of calf infection derived via the in utero route depends on within-herd prevalence and the ratio of sub-clinical to clinical cases among infected cows. Assuming 80:20 for the latter, estimates of incidence were in the range 0.44–1.2 infected calves per 100 cows per annum in herds with within-herd prevalence of 5%, and 3.5–9.3 calves in herds with 40% prevalence. These estimates were not markedly sensitive to the value chosen for the proportion of clinical cases. In utero transmission of Mptb could retard the success of disease control programmes if the opportunities for post natal transmission via colostrum/milk and environmental contamination were able to be controlled. The consequences of fetal infection for the calves so infected are discussed in the context of diagnosis and vaccination together with recommendations for future research.

Introduction

Johne’s disease or paratuberculosis occurs globally in ruminants and in cattle it is associated with economic losses due to culling of clinical cases, reduced milk production and the costs of laboratory testing and control measures (Ott et al., 1999). However, potential impact on consumer demand for milk associated with product safety needs to be considered as the causative organism, Mycobacterium avium subsp. paratuberculosis (Mptb), may also be a cause of Crohn’s disease (Stott et al., 2005, Chamberlin and Naser, 2006). Public health authorities internationally acknowledge that a precautionary approach and further research are warranted.

Most authors agree that the faecal-oral route is the primary mechanism for transmission of Mptb and this is reflected in disease control recommendations for cattle (Clarke, 1997). These are similar in most countries and based on removal of clinical cases, identification of sub-clinical cases by objective tests, and hygienic calf rearing (Kennedy and Benedictus, 2001, Benedictus and Kalis, 2003). Compliance with calf rearing recommendations is difficult for some farmers (Wraight et al., 2000), but in any case transmission in utero could limit its effectiveness (Lawrence, 1956, McQueen and Russell, 1979). To the authors’ knowledge this topic has never been reviewed formally.

The aims of this study were to critically review published data on extra-intestinal and in utero infection, determine the prevalence of fetal infection in cattle through meta-analysis, estimate the incidence of congenital infection in calves and make recommendations for future research.

Section snippets

Material and methods

The pathogenesis of Mptb infection, evidence for extra-intestinal infection and experimental in utero infection trials were summarised following a literature review. An electronic search was conducted using search terms “in utero”, “uterus”, “fetus”, or “placenta” with the term “paratuberculosis”. In addition, a collation of early literature from 1895 (Chiodini, 1992) was searched manually.

A meta-analysis of observational studies of the prevalence of fetal infection in naturally infected cows

Results

An appraisal of natural in utero transmission of Mptb in cattle was informed by review of the pathogenesis of paratuberculosis, extra-intestinal spread of the organism and experimental infections of the bovine reproductive tract. Studies in other species were considered.

Discussion

The pathogenic mycobacteria have complex host-parasite relationships and in general have more than one mechanism of transmission between animals. While faecal–oral transmission of Mptb is likely to be the dominant means of perpetuation of Johne’s disease in livestock, it is unlikely to be the only means. It is widely acknowledged that Mptb is shed in bovine milk (Ellingson et al., 2005). Both faecal–oral and trans-mammary transmission risk is reduced through hygienic calf rearing in which cows

Conclusions

Research approaches to better understand and intervene in the process of in utero infection are likely to be difficult and expensive. The needs are to understand (1) the mechanism of access of Mptb to the uterus, particularly the relative importance of haematogenous spread, direct extension via the placental tissues, and per cervical infection with faecal-derived organisms; (2) whether the immune status of the cow influences in utero transmission to the fetus, and in particular whether

Acknowledgements

This study was supported by Dairy Australia and Drs. Andrew Padula and Robin Condron are thanked for their advice and encouragement. Drs. David Jordan and Evan Sergeant provided valuable comments on a draft of the manuscript.

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