Liver fluke (Fasciola hepatica) co‐infection with bovine tuberculosis (bTB) in cattle: A retrospective animal‐level assessment of bTB risk in dairy and beef cattle

Abstract

Bovine tuberculosis (bTB), caused by Mycobacterium bovis, remains a persistent problem for cattle industries in endemic countries. The frequency, quality, and performance of tests, and the presence of wildlife reservoirs, have been identified as impediments to eradication. Recently, exposure to helminth infection (Fasciola hepatica) has been associated negatively with the disclosure of bTB. Here, for the first time, we assess impact of concurrent infections of Fasciola hepatica and the disclosure of bTB at the animal‐level using large surveillance datasets. We utilized a dataset of 138,566 animal records from an abattoir from Northern Ireland (2011–2013). The presence of F. hepatica infection was assessed from macroscopic tissue inspection at abattoir. Multivariable models were developed to assess co‐infection associations with bTB status based on: Single Intradermal Comparative Tuberculin Test (SICTT), lesion, bacteriological confirmation, including either all animals, or only skin‐test negative animals (lesions at routine slaughter; LRS; confirmed nonreactors at routine slaughter; cNRs) or positive (reactors) animals alone, respectively. The relationship between skin tuberculin reaction sizes and fluke status was also explored for a subset of animals with field recordings (n = 24,680). Controlling for known risk factors (e.g., climatic, herd, and individual level characteristics), we did not find significant associations between the SICTT (standard or severe interpretation), lesion, nor confirmation status of animals and their liver fluke status. The only exception was a negative association between liver fluke positivity, and LRS or cNRs, respectively; though effect‐sizes were small (e.g., LRS Odds‐Ratio: 0.87; 95% CI: 0.76–1.00). There was limited evidence of a relationship between tuberculin reaction sizes during SICTT testing and liver fluke infection status. These data do not support the contention that the detection of bTB using skin‐tests or reactor postmortem follow‐up may be compromised by co‐infection at a population level, but the relationship with lesion formation (pathogenesis) may indicate an impact for postmortem surveillance.

Liver fluke (Fasciola hepatica) co‐infection with bovine tuberculosis in cattle: A prospective herd‐level assessment of herd bTB risk in dairy enterprises

“…These results concur with the overall findings of recent animal‐level analyses of concurrent infection from Northern Ireland (Byrne et al, ; Byrne, Graham, Brown, et al, ; Byrne et al, ), but do not appear to be consistent with other recent herd‐level epidemiological models from Great Britain (Claridge et al, ). Furthermore, our results do not appear to be consistent with animal experiments, whereby co‐infection has reduced the immunological reaction during bTB testing, such that it could impact on the diagnosis of the pathogen (Claridge et al, ; Flynn et al, ).…”

“…A second limitation is that bulk milk testing gives an overall level of infection across the (milking) herd, but this may mask substantial inter‐individual risk variation. However, we have undertaken additional analyses at the animal level to try to verify the conclusions of this work (Byrne et al, ; Byrne, Graham, Brown, et al, ; Byrne et al, ). Taking both pieces of work (retrospective animal‐ and prospective herd‐level analyses) together would tend to support the hypothesis of limited observed association between bTB and F. hepatica infection in Northern Ireland.…”

“…by being associated with smaller size or counts of lesions, Byrne, Graham, Brown, et al, or reduced bacterial load Garza‐Cuartero et al, ), it is possible that, if anything, liver fluke infection could reduce the bTB‐VL confirmation rates of truly infected cattle. Other research from Northern Ireland on the impact of liver fluke status on SICCT tuberculin reaction sizes uncovered a negative association at univariable level, but this association was confounded by age‐class (Byrne et al, ). Furthermore, the size effect was very small (<1 mm), indicating low clinical or practical impact, concurring with the conclusions of Howell ().…”

“…However, for animals in the same cohort with bTB‐VLs, there was an association between maximum lesion size classes (categorized broadly as small, medium or large lesions) and liver fluke status (Byrne, Graham, Brown, et al, ), with fluke positive animals disclosing smaller lesions than animals without evidence of fluke infection. Using a larger surveillance dataset (~130,000 animals), Byrne et al () did not report an association with a number of metrics of bTB—SICCT results, presence of lesions, laboratory confirmation—and fluke status. However, there was a negative association found between the disclosure of lesions at routine slaughter (essentially, these are animals with bTB‐VL lesions found at abattoir that have not been disclosed during ante‐mortem testing) and fluke status.…”

“…To estimate seasonal variation in liver fluke risk, bulk milk sampling from a statutory scheme was related to whole herd bTB test results. It was anticipated that this study would clarify the population‐level association between F. hepatica and bTB in NI, and complement retrospective animal‐level analyses from the same population (Byrne et al, ). Specifically, we wanted to test the hypothesis that there was a negative association between liver fluke infection risk and bTB breakdown risk at the herd level (sensu Claridge et al, ).…”