Temporal dynamics of the early immune response following Mycobacterium bovis infection of cattle.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
31 Jan 2024
31 Jan 2024
Historique:
received:
01
12
2023
accepted:
17
01
2024
medline:
1
2
2024
pubmed:
1
2
2024
entrez:
31
1
2024
Statut:
epublish
Résumé
Bovine tuberculosis is an infectious disease of global significance that remains endemic in many countries. Mycobacterium bovis infection in cattle is characterized by a cell-mediated immune response (CMI) that precedes humoral responses, however the timing and trajectories of CMI and antibody responses determined by newer generation assays remain undefined. Here we used defined-antigen interferon-gamma release assays (IGRA) and an eleven-antigen multiplex ELISA (Enferplex TB test) alongside traditional tuberculin-based IGRA and IDEXX M. bovis antibody tests to assess immune trajectories following experimental M. bovis infection of cattle. The results show CMI responses developed as early as two-weeks post-infection, with all infected cattle testing positive three weeks post-infection. Interestingly, 6 of 8 infected animals were serologically positive with the Enferplex TB assay as early as 4 weeks post-infection. As expected, application of the tuberculin skin test enhanced subsequent serological reactivity. Infrequent M. bovis faecal shedding was observed but was uncorrelated with observed immune trajectories. Together, the results show that early antibody responses to M. bovis infection are detectable in some individuals and highlight an urgent need to identify biomarkers that better predict infection outcomes, particularly for application in low-and-middle income countries where test-and-slaughter based control methods are largely unfeasible.
Identifiants
pubmed: 38297023
doi: 10.1038/s41598-024-52314-x
pii: 10.1038/s41598-024-52314-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2600Subventions
Organisme : Department for Environment, Food and Rural Affairs, UK Government
ID : SE3318
Organisme : Bill and Melinda Gates Foundation
ID : OPP1176950
Informations de copyright
© 2024. Crown.
Références
Mellado, M. et al. Milk yield and reproductive performance of Holstein cows testing positive for bovine tuberculosis. Trop. Anim. Health Prod. 47, 1061–1066. https://doi.org/10.1007/s11250-015-0828-1 (2015).
doi: 10.1007/s11250-015-0828-1
pubmed: 25894823
Olea-Popelka, F. et al. Zoonotic tuberculosis in human beings caused by Mycobacterium bovis-a call for action. Lancet Infect. Dis. 17, e21–e25. https://doi.org/10.1016/s1473-3099(16)30139-6 (2017).
doi: 10.1016/s1473-3099(16)30139-6
pubmed: 27697390
Smith, R. L., Tauer, L. W., Sanderson, M. W. & Gröhn, Y. T. Minimum cost to control bovine tuberculosis in cow-calf herds. Prev. Vet. Med. 115, 18–28. https://doi.org/10.1016/j.prevetmed.2014.03.014 (2014).
doi: 10.1016/j.prevetmed.2014.03.014
pubmed: 24703601
pmcid: 4076834
Tschopp, R. et al. Effect of bovine tuberculosis on selected productivity parameters and trading in dairy cattle kept under intensive husbandry in Central Ethiopia. Front. Vet. Sci. 8, 698768. https://doi.org/10.3389/fvets.2021.698768 (2021).
doi: 10.3389/fvets.2021.698768
pubmed: 34368283
pmcid: 8334357
Malone, K. M. & Gordon, S. V. Mycobacterium tuberculosis complex members adapted to wild and domestic animals. Adv. Exp. Med. Biol. 1019, 135–154. https://doi.org/10.1007/978-3-319-64371-7_7 (2017).
doi: 10.1007/978-3-319-64371-7_7
pubmed: 29116633
Rodriguez-Campos, S., Smith, N. H., Boniotti, M. B. & Aranaz, A. Overview and phylogeny of Mycobacterium tuberculosis complex organisms: Implications for diagnostics and legislation of bovine tuberculosis. Res. Vet. Sci. 97(Suppl), S5-s19. https://doi.org/10.1016/j.rvsc.2014.02.009 (2014).
doi: 10.1016/j.rvsc.2014.02.009
pubmed: 24630673
de la Rua-Domenech, R. et al. Ante mortem diagnosis of tuberculosis in cattle: A review of the tuberculin tests, gamma-interferon assay and other ancillary diagnostic techniques. Res. Vet. Sci. 81, 190–210. https://doi.org/10.1016/j.rvsc.2005.11.005 (2006).
doi: 10.1016/j.rvsc.2005.11.005
pubmed: 16513150
Pollock, J. M. & Neill, S. D. Mycobacterium bovis infection and tuberculosis in cattle. Vet. J. 163, 115–127 (2002).
doi: 10.1053/tvjl.2001.0655
pubmed: 12093187
Waters, W. R. et al. Early antibody responses to experimental Mycobacterium bovis infection of cattle. Clin. Vaccine Immunol. 13, 648–654. https://doi.org/10.1128/CVI.00061-06 (2006).
doi: 10.1128/CVI.00061-06
pubmed: 16760322
pmcid: 1489550
Lyashchenko, K. P., Vordermeier, H. M. & Waters, W. R. Memory B cells and tuberculosis. Vet. Immunol. Immunopathol. 221, 110016. https://doi.org/10.1016/j.vetimm.2020.110016 (2020).
doi: 10.1016/j.vetimm.2020.110016
pubmed: 32050091
Lepper, A. W., Pearson, C. W. & Corner, L. A. Anergy to tuberculin in beef cattle. Aust. Vet. J. 53, 214–216. https://doi.org/10.1111/j.1751-0813.1977.tb00188.x (1977).
doi: 10.1111/j.1751-0813.1977.tb00188.x
pubmed: 901321
Palmer, M. V. et al. Biomarkers of cell-mediated immunity to bovine tuberculosis. Vet. Immunol. Immunopathol. 220, 109988. https://doi.org/10.1016/j.vetimm.2019.109988 (2020).
doi: 10.1016/j.vetimm.2019.109988
pubmed: 31846797
Vordermeier, H. M. et al. Correlation of ESAT-6-specific gamma interferon production with pathology in cattle following Mycobacterium bovis BCG vaccination against experimental bovine tuberculosis. Infect. Immun. 70, 3026–3032 (2002).
doi: 10.1128/IAI.70.6.3026-3032.2002
pubmed: 12010994
pmcid: 128013
Pollock, J. M. et al. Immune responses in bovine tuberculosis. Tuberculosis 81, 103–107. https://doi.org/10.1054/tube.2000.0258 (2001).
doi: 10.1054/tube.2000.0258
pubmed: 11463230
Thom, M. et al. The effect of repeated tuberculin skin testing of cattle on immune responses and disease following experimental infection with Mycobacterium bovis. Vet. Immunol. Immunopathol. 102, 399–412. https://doi.org/10.1016/j.vetimm.2004.08.005 (2004).
doi: 10.1016/j.vetimm.2004.08.005
pubmed: 15541793
Whelan, C. et al. Performance of the Enferplex TB assay with cattle in Great Britain and assessment of its suitability as a test to distinguish infected and vaccinated animals. Clin. Vaccine Immunol. 17, 813–817. https://doi.org/10.1128/cvi.00489-09 (2010).
doi: 10.1128/cvi.00489-09
pubmed: 20219883
pmcid: 2863378
McCorry, T. et al. Shedding of Mycobacterium bovis in the nasal mucus of cattle infected experimentally with tuberculosis by the intranasal and intratracheal routes. Vet. Rec. 157, 613–618. https://doi.org/10.1136/vr.157.20.613 (2005).
doi: 10.1136/vr.157.20.613
pubmed: 16284329
Bulterys, M. A. et al. Point-of-care urine LAM tests for tuberculosis diagnosis: A status update. J. Clin. Med. https://doi.org/10.3390/jcm9010111 (2019).
doi: 10.3390/jcm9010111
pubmed: 31906163
pmcid: 7020089
Liu, C. et al. Quantification of circulating Mycobacterium tuberculosis antigen peptides allows rapid diagnosis of active disease and treatment monitoring. Proc. Natl. Acad. Sci. USA 114, 3969–3974. https://doi.org/10.1073/pnas.1621360114 (2017).
doi: 10.1073/pnas.1621360114
pubmed: 28348223
pmcid: 5393254
Minion, J. et al. Diagnosing tuberculosis with urine lipoarabinomannan: Systematic review and meta-analysis. Eur. Respir. J. 38, 1398–1405. https://doi.org/10.1183/09031936.00025711 (2011).
doi: 10.1183/09031936.00025711
pubmed: 21700601
Schofield, D. A., Sharp, N. J. & Westwater, C. Phage-based platforms for the clinical detection of human bacterial pathogens. Bacteriophage 2, 105–283. https://doi.org/10.4161/bact.19274 (2012).
doi: 10.4161/bact.19274
pubmed: 23050221
pmcid: 3442824
Swift, B. M. C. et al. The development and use of Actiphage(®) to detect viable mycobacteria from bovine tuberculosis and Johne’s disease-infected animals. Microb. Biotechnol. 13, 738–746. https://doi.org/10.1111/1751-7915.13518 (2020).
doi: 10.1111/1751-7915.13518
pubmed: 31793754
Health, W. O. f. A. Bovine Tuberculosis. Terrestrial Manual. https://www.woah.org/app/uploads/2021/03/3-04-06-bovine-tb.pdf (2018).
Srinivasan, S. et al. A defined antigen skin test for the diagnosis of bovine tuberculosis. Sci. Adv. 5, eaax4899. https://doi.org/10.1126/sciadv.aax4899 (2019).
doi: 10.1126/sciadv.aax4899
pubmed: 31328169
pmcid: 6636981
Waters, W. R. et al. Development and evaluation of an enzyme-linked immunosorbent assay for use in the detection of bovine tuberculosis in cattle. Clin. Vacc. Immunol. 18, 1882–1888. https://doi.org/10.1128/CVI.05343-11 (2011).
doi: 10.1128/CVI.05343-11
McGoldrick, A., Bensaude, E., Ibata, G., Sharp, G. & Paton, D. J. Closed one-tube reverse transcription nested polymerase chain reaction for the detection of pestiviral RNA with fluorescent probes. J. Virol. Methods 79, 85–95. https://doi.org/10.1016/s0166-0934(99)00010-5 (1999).
doi: 10.1016/s0166-0934(99)00010-5
pubmed: 10328538
Wolff, C., Hörnschemeyer, D., Wolff, D. & Kleesiek, K. Single-tube nested PCR with room-temperature-stable reagents. PCR Methods Appl. 4, 376–379. https://doi.org/10.1101/gr.4.6.376 (1995).
doi: 10.1101/gr.4.6.376
pubmed: 7580934