Latent infections are the most frequent form of paratuberculosis in slaughtered Friesian cattle

Abstract

Paratuberculosis is a chronic mycobacterial infection causing granulomatous enteritis in ruminants, whose pathogenesis and epidemiology poses numerous challenges, including latency and reactivation. The most recent and complete classification of paratuberculosis immunopathological types in cattle recognized five categories. In this study, 1031 slaughtered Friesian cattle were submitted to serological, microbiological and pathological examinations with the aim of maximizing the rate of case detection. In most cases, infected animals had minimal lesions and almost no other proof of infection (38.9%), while the more characteristic types with the whole constellation of microbiological and immunological evidences accounted for a lower proportion (7.7%). As these findings in cattle suggest similarities with the epidemiology of tuberculosis in humans, we propose to re-group the original immunopathological types into two broader paratuberculosis epidemio-pathogenic forms or states: latent and patent. The former term would define infections with focal lesions and might constitute an apparent resilience status representing a difficult to detect reservoir of infection whose role could become critical if later immune-compromising factors lead to re-activation. The latter would group those cases with multifocal and diffuse inflammatory lesions with higher mycobacterial load and viability suggestive of a more immediate epidemiological risk. Interestingly, the relative frequency of presentation of each profile varied with age. The proportion of latent forms remained relatively constant between 33.8% and 54.3% through adulthood from 3 years of age, while patent forms were more frequent during the first years of age and tended to decrease among the oldest individuals.

Case definition terminology for paratuberculosis (Johne’s disease)

“…Mismatches between the results of different tests for paratuberculosis are common: tissue culture results may not agree with histopathology; faecal culture may not agree with antibody ELISA. For example, MAP was cultured from the tissues of about 30% of sheep and 7% of cattle that did not have histopathological lesions [ 12 , 56 ]. More recently, in a series of trials conducted at the University of Sydney between 2006 and 2012 involving over 400 sheep that were intensively monitored and received a full necropsy, 13% of the sheep positive for MAP by tissue culture had no detectable histopathological lesions across six different regions of the gut and associated lymph nodes (unpublished data).These discrepancies can be readily understood in terms of stage of pathogenesis, site of sample selection and amount of sample examined, and biological/physical properties of the tests (for discussion see [ 28 ]).…”

“…Objective lesion scoring criteria have been published and are widely used in research applications [ 12 , 48 , 81 – 84 ]. These systems have multiple categories to describe the extent, severity and nature of the granulomatous lesions that characterize paratuberculosis.…”

“…Granulomatous lesions attributable to MAP are present. The morphological diagnosis can be refined using one of the lesion classification schemes [ 12 , 48 , 81 – 84 ] to assess the stage of disease and infer the degree of infectiousness, because multibacillary lesions are correlated with heavy faecal shedding [ 50 ]. Specific terminology is used in Australia for diagnostic purposes [ 53 ]: “a diagnosis of ‘lesions consistent with MAP infection’ is indicated if in any one section, one or more single giant cells and/or one or more accumulations of epithelioid macrophages are observed in the intestinal lamina propria and/or lymph node cortex with the presence of at least one acid fast organism (AFO) morphologically consistent with MAP” ; a finding ‘suggestive of MAP infection’ is indicated if AFO are not observed.…”

“…In one of the largest studies to date, involving detailed examination of more than 1000 cows using a battery of tests, Vazquez et al (2014) [ 12 ] confirmed that most MAP infections are subclinical, and that the microbiological and pathological features of paratuberculosis leading to disease transmission are not dissimilar to tuberculosis in humans. In both humans and livestock, infected individuals carry pathogenic mycobacteria silently into new geographic areas [ 13 – 15 ].…”

Detection of Mycobacterium avium subspecies in the gut associated lymphoid tissue of slaughtered rabbits

“…Map is the causal agent of paratuberculosis in ruminants and it has been controversially associated with human inflammatory bowel disease, more precisely with Crohn’s disease [ 15 – 17 ] and also diabetes mellitus [ 18 ]. Its prevalence in slaughtered cattle in Europe has been estimated to be up to 50 % [ 19 ]. Mas has been isolated from wood pigeons [ 20 ], roe deer [ 21 ] and horses causing tuberculous-like lesions in these animals [ 22 ].…”