Association of Fasciola gigantica Co-infection With Bovine Tuberculosis Infection and Diagnosis in a Naturally Infected Cattle Population in Africa.

Robert F Kelly,Lucy Ndip,Richard Ngandolo,Kenton L Morgan,Barend M De C Bronsvoort,Adrian Muwonge,Diana J L Williams,Nkongho F Egbe,Ngu Ngwa Victor,Stella Mazeri,Rebecca Callaby,Vincent N Tanya,Melissa Sander,Ian G Handel

doi:10.3389/fvets.2018.00214

Abstract

Bovine tuberculosis (bTB), caused by Mycobacterium bovis, remains a major livestock and public health problem in both high and low-income countries. With the current absence of an effective vaccine, control in cattle populations is reliant on regular testing and removal of positive animals. However, surveillance and control are hampered by imperfect diagnostic tests that have poorly described properties in naturally infected populations. Recent research in cattle co-infected with the temperate liver fluke, Fasciola hepatica, has raised concerns about the performance of the intradermal skin test in high fluke incidence areas. Further, recent studies of parasitic co-infections have demonstrated their impact on Th1 and Th2 responses, concurrent disease pathology and susceptibility to mycobacterial infections. Here we report for the first time the association of co-infection with the tropical liver fluke, Fasciola gigantica, with the presence of bTB-like lesions and the IFN-γ response in naturally infected African cattle. After adjusting for age and sex we observed a complex interaction between fluke status and breed. Fulani cattle had a higher risk of having bTB-like lesions than the mixed breed group. The risk of bTB-like lesions increased in the mixed breed group if they had concurrent evidence of fluke pathology but was less clear in the coinfected Fulani breed. Further, we observed a slight decline in the IFN-γ levels in fluke infected animals. Finally we explored factors associated with IFN-γ false negative results compared to the presence of bTB-like lesions. Fulani cattle had a higher risk of having a false negative result compared to the mixed breed group. Further, the mixed breed cattle had an increased risk of being false negative if also co-infected with fluke. Interesting, as with the risk of bTB-like lesions, this association was less clear in the Fulani cattle with weak evidence of a slight decrease in risk of having a false negative test result when fluke pathology positive. This interesting interaction where different breeds appear to have different responses to co-infections is intriguing but further work is needed to confirm and understand more clearly the possible confounding effects of different other co-infections not measured here, breed, management or exposure risks.

Highlights

In natural populations, individuals are usually infected with multiple pathogens, known as “co-infections,” rather than single infections [1]
Interactions between bovine tuberculosis and the temperate liver fluke F. hepatica have been shown in the United Kingdom [3, 19]
But less is known about the interactions of bovine tuberculosis and the tropical fluke F. gigantica

Summary

Introduction

Individuals are usually infected with multiple pathogens, known as “co-infections,” rather than single infections [1]. In the presence of multiple co-infections, the immune response observed to an individual pathogen, across a population, is variable. This has been shown to depend on the combination of infections and their differing interactions with the host immune system and other infections [2]. Co-infections with Fasiola hepatica have been implicated as a potential reason for poor bTB diagnostic test performance and disagreement between tests [3]. Co-infections with F. hepatica have been shown to down-regulate the Th1 responses (with a resultant dampening of the IFN-γ response), with subsequent predominance of Th2 responses, in order for the parasite to survive and reproduce [4,5,6,7,8]

Methods

Results

Conclusion