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

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,...

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Main Authors: Robert F. Kelly, Rebecca Callaby, Nkongho F. Egbe, Diana J. L. Williams, Ngu Ngwa Victor, Vincent N. Tanya, Melissa Sander, Lucy Ndip, Richard Ngandolo, Kenton L. Morgan, Ian G. Handel, Stella Mazeri, Adrian Muwonge, Barend M. de C Bronsvoort
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-09-01
Series:Frontiers in Veterinary Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fvets.2018.00214/full
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author Robert F. Kelly
Robert F. Kelly
Rebecca Callaby
Nkongho F. Egbe
Diana J. L. Williams
Ngu Ngwa Victor
Vincent N. Tanya
Melissa Sander
Lucy Ndip
Richard Ngandolo
Kenton L. Morgan
Ian G. Handel
Ian G. Handel
Stella Mazeri
Adrian Muwonge
Barend M. de C Bronsvoort
author_facet Robert F. Kelly
Robert F. Kelly
Rebecca Callaby
Nkongho F. Egbe
Diana J. L. Williams
Ngu Ngwa Victor
Vincent N. Tanya
Melissa Sander
Lucy Ndip
Richard Ngandolo
Kenton L. Morgan
Ian G. Handel
Ian G. Handel
Stella Mazeri
Adrian Muwonge
Barend M. de C Bronsvoort
author_sort Robert F. Kelly
collection DOAJ
description 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.
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spelling doaj.art-db1224526a10413a9f66465708c9a6882022-12-22T03:32:55ZengFrontiers Media S.A.Frontiers in Veterinary Science2297-17692018-09-01510.3389/fvets.2018.00214393899Association of Fasciola gigantica Co-infection With Bovine Tuberculosis Infection and Diagnosis in a Naturally Infected Cattle Population in AfricaRobert F. Kelly0Robert F. Kelly1Rebecca Callaby2Nkongho F. Egbe3Diana J. L. Williams4Ngu Ngwa Victor5Vincent N. Tanya6Melissa Sander7Lucy Ndip8Richard Ngandolo9Kenton L. Morgan10Ian G. Handel11Ian G. Handel12Stella Mazeri13Adrian Muwonge14Barend M. de C Bronsvoort15The Roslin Institute, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Midlothian, United KingdomRoyal (Dick) School of Veterinary Studies, University of Edinburgh, Midlothian, United KingdomThe Roslin Institute, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Midlothian, United KingdomMicrobiology and Parasitology Unit, Faculty of Allied Medical Science, University of Calabar, Calabar, NigeriaVeterinary Parasitology, Institute of Infection and Global Health and School of Veterinary Science, Liverpool, United KingdomSchool of Veterinary Medicine and Sciences, University of Ngaoundere, Ngaoundere, CameroonCameroon Academy of Sciences, Yaoundé, CameroonTuberculosis Reference Laboratory Bamenda, Hospital Roundabout, Bamenda, CameroonLaboratory of Emerging Infectious Diseases, University of Buea, Buea, CameroonLaboratoire de Recherches Vétérinaires et Zootechniques de Farcha, N'Djamena, Chad0Institute of Ageing and Chronic Disease and School of Veterinary Science, University of Liverpool, Neston, United KingdomThe Roslin Institute, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Midlothian, United KingdomRoyal (Dick) School of Veterinary Studies, University of Edinburgh, Midlothian, United KingdomThe Roslin Institute, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Midlothian, United KingdomThe Roslin Institute, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Midlothian, United KingdomThe Roslin Institute, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Midlothian, United KingdomBovine 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.https://www.frontiersin.org/article/10.3389/fvets.2018.00214/fullbovine tuberculosisM. bovisco-infectionF. giganticafasciolosisCameroon
spellingShingle Robert F. Kelly
Robert F. Kelly
Rebecca Callaby
Nkongho F. Egbe
Diana J. L. Williams
Ngu Ngwa Victor
Vincent N. Tanya
Melissa Sander
Lucy Ndip
Richard Ngandolo
Kenton L. Morgan
Ian G. Handel
Ian G. Handel
Stella Mazeri
Adrian Muwonge
Barend M. de C Bronsvoort
Association of Fasciola gigantica Co-infection With Bovine Tuberculosis Infection and Diagnosis in a Naturally Infected Cattle Population in Africa
Frontiers in Veterinary Science
bovine tuberculosis
M. bovis
co-infection
F. gigantica
fasciolosis
Cameroon
title Association of Fasciola gigantica Co-infection With Bovine Tuberculosis Infection and Diagnosis in a Naturally Infected Cattle Population in Africa
title_full Association of Fasciola gigantica Co-infection With Bovine Tuberculosis Infection and Diagnosis in a Naturally Infected Cattle Population in Africa
title_fullStr Association of Fasciola gigantica Co-infection With Bovine Tuberculosis Infection and Diagnosis in a Naturally Infected Cattle Population in Africa
title_full_unstemmed Association of Fasciola gigantica Co-infection With Bovine Tuberculosis Infection and Diagnosis in a Naturally Infected Cattle Population in Africa
title_short Association of Fasciola gigantica Co-infection With Bovine Tuberculosis Infection and Diagnosis in a Naturally Infected Cattle Population in Africa
title_sort association of fasciola gigantica co infection with bovine tuberculosis infection and diagnosis in a naturally infected cattle population in africa
topic bovine tuberculosis
M. bovis
co-infection
F. gigantica
fasciolosis
Cameroon
url https://www.frontiersin.org/article/10.3389/fvets.2018.00214/full
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