Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-21T05:23:26.049Z Has data issue: false hasContentIssue false

Biomarkers as diagnostic tools for mycobacterial infections in cattle

Published online by Cambridge University Press:  28 December 2020

Hyun-Eui Park
Affiliation:
Department of Infectious Disease, College of Veterinary Medicine, Seoul National University, Seoul, 08826, Republic of Korea
Han Sang Yoo*
Affiliation:
Department of Infectious Disease, College of Veterinary Medicine, Seoul National University, Seoul, 08826, Republic of Korea Bio-MAX/N-Bio Institute, Seoul National University, Seoul, 08826, Republic of Korea
*
Author for correspondence: Han Sang Yoo, Department of Infectious Disease, College of Veterinary Medicine, Seoul National University, Seoul, 08826, Republic of Korea. E-mail: [email protected]

Abstract

Mycobacterial infections are widely distributed in animals and cause considerable economic losses, especially in livestock animals. Bovine paratuberculosis and bovine tuberculosis, which are representative mycobacterial infections in cattle, are difficult to diagnose using current-generation diagnostics due to their relatively long incubation periods. Thus, alternative diagnostic tools are needed for the detection of mycobacterial infections in cattle. A biomarker is an indicator present in biological fluids that reflects the biological state of an individual during the progression of a specific disease. Therefore, biomarkers are considered a potential diagnostic tool for various diseases. Recently, the number of studies investigating biomarkers as tools for diagnosing mycobacterial infections has increased. In human medicine, many diagnostic biomarkers have been developed and applied in clinical practice. In veterinary medicine, however, many such developments are still in the early stages. In this review, we summarize the current progress in biomarker research related to the development of diagnostic biomarkers for mycobacterial infections in cattle.

Type
Review Article
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adnane, M, Chapwanya, A, Kaidi, R, Meade, KG and O'Farrelly, C (2017) Profiling inflammatory biomarkers in cervico-vaginal mucus (CVM) postpartum: potential early indicators of bovine clinical endometritis? Theriogenology 103, 117122.CrossRefGoogle ScholarPubMed
Adnane, M, Kelly, P, Chapwanya, A, Meade, KG and O'Farrelly, C (2018) Improved detection of biomarkers in cervico-vaginal mucus (CVM) from postpartum cattle. BMC Veterinary Research 14, 297.CrossRefGoogle ScholarPubMed
Alonso-Hearn, M, Canive, M, Blanco-Vazquez, C, Torremocha, R, Balseiro, A, Amado, J, Varela-Martinez, E, Ramos, R, Jugo, BM and Casais, R (2019) RNA-Seq analysis of ileocecal valve and peripheral blood from Holstein cattle infected with Mycobacterium avium subsp. paratuberculosis revealed dysregulation of the CXCL8/IL8 signaling pathway. Scientific Reports 9, 14845.CrossRefGoogle ScholarPubMed
Anderson, ST, Kaforou, M, Brent, AJ, Wright, VJ, Banwell, CM, Chagaluka, G, Crampin, AC, Dockrell, HM, French, N, Hamilton, MS, Hibberd, ML, Kern, F, Langford, PR, Ling, L, Mlotha, R, Ottenhoff, THM, Pienaar, S, Pillay, V, Scott, JAG, Twahir, H, Wilkinson, RJ, Coin, LJ, Heyderman, RS, Levin, M and Eley, B (2014) Diagnosis of childhood tuberculosis and host RNA expression in Africa. New England Journal of Medicine 370, 17121723.CrossRefGoogle ScholarPubMed
Aranday-Cortes, E, Hogarth, PJ, Kaveh, DA, Whelan, AO, Villarreal-Ramos, B, Lalvani, A and Vordermeier, HM (2012) Transcriptional profiling of disease-induced host responses in bovine tuberculosis and the identification of potential diagnostic biomarkers. PLoS One 7, e30626.CrossRefGoogle ScholarPubMed
Arango-Sabogal, JC, Labrecque, O, Paré, J, Fairbrother, JH, Roy, JP, Wellemans, V and Fecteau, G (2016) Evaluation of a PCR assay on overgrown environmental samples cultured for Mycobacterium avium subsp. paratuberculosis. Journal of Veterinary Diagnostic Investigation 28, 638645.CrossRefGoogle ScholarPubMed
Bernitz, N, Clarke, C, Roos, EO, Goosen, WJ, Cooper, D, van Helden, PD, Parsons, SDC and Miller, MA (2018) Detection of Mycobacterium bovis infection in African buffaloes (Syncerus caffer) using QuantiFERON®-TB Gold (QFT) tubes and the Qiagen cattle type® IFN-gamma ELISA. Veterinary Immunology and Immunopathology 196, 4852.CrossRefGoogle Scholar
Blanco, FC, Bigi, F and Soria, MA (2014) Identification of potential biomarkers of disease progression in bovine tuberculosis. Veterinary Immunology and Immunopathology 160, 177183.CrossRefGoogle ScholarPubMed
Bögli-Stuber, K, Kohler, C, Seitert, G, Glanemann, B, Antognoli, MC, Salman, MD, Wittenbrink, MM, Wittwer, M, Wassenaar, T, Jemmi, T and Bissig-Choisat, B (2005) Detection of Mycobacterium avium subspecies paratuberculosis in Swiss dairy cattle by real-time PCR and culture: a comparison of the two assays. Journal of Applied Microbiology 99, 587597.CrossRefGoogle ScholarPubMed
Britton, LE, Cassidy, JP, O'Donovan, J, Gordon, SV and Markey, B (2016) Potential application of emerging diagnostic techniques to the diagnosis of bovine Johne's disease (paratuberculosis). Veterinary Journal 209, 3239.CrossRefGoogle Scholar
Caminiti, A, Pelone, F, LaTorre, G, De Giusti, M, Saulle, R, Mannocci, A, Sala, M, Della Marta, U and Scaramozzino, P (2016) Control and eradication of tuberculosis in cattle: a systematic review of economic evidence. Veterinary Record 179, 7075.CrossRefGoogle ScholarPubMed
Cha, SB, Yoo, A, Park, HT, Sung, KY, Shin, MK and Yoo, HS (2013) Analysis of transcriptional profiles to discover biomarker candidates in Mycobacterium avium subsp. paratuberculosis-infected macrophages, RAW 264.7. Journal of Microbiology and Biotechnology 23, 11671175.CrossRefGoogle ScholarPubMed
Cho, YS, Jung, SC and Oh, S (2015) Diagnosis of bovine tuberculosis using a metal oxide-based electronic nose. Letters in Applied Microbiology 60, 513516.CrossRefGoogle ScholarPubMed
Coad, M, Doyle, M, Steinbach, S, Gormley, E, Vordermeier, M and Jones, G (2019) Simultaneous measurement of antigen-induced CXCL10 and IFN-γ enhances test sensitivity for bovine TB detection in cattle. Veterinary Microbiology 230, 16.CrossRefGoogle Scholar
Collins, MT (2011) Diagnosis of paratuberculosis. Veterinary Clinics of North America: Food Animal Practice 27, 581591.Google ScholarPubMed
Cook, KL, Flis, SA and Ballard, CS (2013) Sensitivity of Mycobacterium avium subsp. paratuberculosis, Escherichia coli and Salmonella enterica serotype Typhimurium to low pH, high organic acids and ensiling. Journal of Applied Microbiology 115, 334345.CrossRefGoogle Scholar
Correia-Neves, M, Fröberg, G, Korshun, L, Viegas, S, Vaz, P, Ramanlal, N, Bruchfeld, J, Hamasur, B, Brennan, P and Källenius, G (2019) Biomarkers for tuberculosis: the case for lipoarabinomannan. ERJ Open Research 5, 001152018.CrossRefGoogle ScholarPubMed
Cousins, DV, Whittington, R, Marsh, I, Masters, A, Evans, RJ and Kluver, P (1999) Mycobacteria distenct from Mycobacterium avium subsp. paratuberculosis isolated from the faeces of ruminants possess IS900-like sequences detectable IS900 polymerase chain reaction: implications for diagnosis. Molecular and Cellular Probes 13, 431442.CrossRefGoogle ScholarPubMed
David, J, Barkema, HW, Guan le, L and De Buck, J (2014a) Gene-expression profiling of calves 6 and 9 months after inoculation with Mycobacterium avium subspecies paratuberculosis. Veterinary Research 45, 96.CrossRefGoogle Scholar
David, J, Barkema, HW, Mortier, R, Ghosh, S, Guan le, L and De Buck, J (2014b) Gene expression profiling and putative biomarkers of calves 3 months after infection with Mycobacterium avium subspecies paratuberculosis. Veterinary Immunology and Immunopathology 160, 107117.CrossRefGoogle Scholar
De Buck, J, Shaykhutdinov, R, Barkema, HW and Vogel, HJ (2014) Metabolomic profiling in cattle experimentally infected with Mycobacterium avium subsp. paratuberculosis. PLoS One 9, e111872.CrossRefGoogle ScholarPubMed
de Kruijf, M, Govender, R, Yearsley, D, Coffey, A and O'Mahony, J (2017) A comparative study evaluating the efficacy of IS_MAP04 with IS900 and IS_MAP02 as a new diagnostic target for the detection of Mycobacterium avium subspecies paratuberculosis from bovine faeces. Veterinary Microbiology 204, 104109.CrossRefGoogle ScholarPubMed
de la Rua-Domenech, R, Goodchild, AT, Vordermeier, HM, Hewinson, RG, Christiansen, KH and Clifton-Hadley, RS (2006) Ante mortem diagnosis of tuberculosis in cattle: a review of the tuberculin tests, gamma-interferon assay and other ancillary diagnostic techniques. Research in Veterinary Science 81, 190210.CrossRefGoogle ScholarPubMed
de Lisle, GW, Green, RS and Buddle, BM (2017) Factors affecting the gamma interferon test in the detection of bovine tuberculosis in cattle. Journal of Veterinary Diagnostic Investigation 29, 198202.CrossRefGoogle ScholarPubMed
de Silva, K, Begg, DJ, Plain, KM, Purdie, AC, Kawaji, S, Dhand, NK and Whittington, RJ (2013) Can early host responses to mycobacterial infection predict eventual disease outcomes? Preventive Veterinary Medicine 112, 203212.CrossRefGoogle ScholarPubMed
de Silva, K, Plain, K, Purdie, A, Begg, D and Whittington, R (2018) Defining resilience to mycobacterial disease: characteristics of survivors of ovine paratuberculosis. Journal of Veterinary Diagnostic Investigation 29, 198202.Google Scholar
Drain, PK, Bajema, KL, Dowdy, D, Dheda, K, Naidoo, K, Schumacher, SG, Ma, S, Meermeier, E, Lewinsohn, DM and Sherman, DR (2018) Incipient and subclinical tuberculosis: a clinical review of early stages and progression of infection. Clinical Microbiology Reviews 31, e00021–18.CrossRefGoogle ScholarPubMed
Eda, S, Bannantine, JP, Waters, WR, Mori, Y, Whitlock, RH, Scott, MC and Speer, CA (2006) A highly sensitive and subspecies-specific surface antigen enzyme-linked immunosorbent assay for diagnosis of Johne's disease. Clinical and Vaccine Immunology 13, 837844.CrossRefGoogle ScholarPubMed
Ellis, CK, Rice, S, Maurer, D, Stahl, R, Waters, WR, Palmer, MV, Nol, P, Rhyan, JC, VerCauteren, KC and Koziel, JA (2017) Use of fecal volatile organic compound analysis to discriminate between non-vaccinated and BCG-vaccinated cattle prior to and after Mycobacterium bovis challenge. PLoS One 12, e0179914.CrossRefGoogle ScholarPubMed
Elnaggar, MM, Abdellrazeq, GS, Elsisy, A, Mahmoud, AH, Shyboub, A, Sester, M, Khaliel, SA, Singh, M, Torky, HA and Davis, WC (2017) Evaluation of antigen specific interleukin-1β as a biomarker to detect cattle infected with Mycobacterium bovis. Tuberculosis (Edinb) 105, 5359.CrossRefGoogle ScholarPubMed
Englund, S, Bölske, G and Johansson, KE (2002) An IS900-like sequence found in a Mycobacterium sp. other than Mycobacterium avium subsp. paratuberculosis. FEMS Microbiology Letters 209, 267271.CrossRefGoogle Scholar
Ereqat, S, Nasereddin, A, Levine, H, Azmi, K, Al-Jawabreh, A, Greenblatt, CL, Abdeen, Z and Bar-Gal, GK (2013) First-time detection of Mycobacterium bovis in livestock tissues and milk in the West Bank, Palestinian Territories. PLoS Neglected Tropical Diseases 7, e2417.CrossRefGoogle ScholarPubMed
Facciuolo, A, Kelton, DF and Mutharia, LM (2013) Novel secreted antigens of Mycobacterium paratuberculosis as serodiagnostic biomarkers for Johne's disease in cattle. Clinical and Vaccine Immunology 20, 17831791.CrossRefGoogle ScholarPubMed
Farrell, D, Shaughnessy, RG, Britton, L, MacHugh, DE, Markey, B and Gordon, SV (2015) The identification of circulating MiRNA in bovine serum and their potential as novel biomarkers of early Mycobacterium avium subsp paratuberculosis infection. PLoS One 10, e0134310.CrossRefGoogle ScholarPubMed
Fecteau, ME, Hovingh, E, Whitlock, RH and Sweeney, RW (2013) Persistence of Mycobacterium avium subsp. paratuberculosis in soil, crops, and ensiled feed following manure spreading on infected dairy farms. Canadian Veterinary Journal 54, 10831085.Google ScholarPubMed
Fitzgerald, JE, Bui, ETH, Simon, NM and Fenniri, H (2017) Artificial nose technology: status and prospects in diagnostics. Trends in Biotechnology 35, 3342.CrossRefGoogle ScholarPubMed
Foley, C, Chapwanya, A, Callanan, JJ, Whiston, R, Miranda-CasoLuengo, R, Lu, J, Meijer, WG, Lynn, DJ, O' Farrelly, C and Meade, KG (2015) Integrated analysis of the local and systemic changes preceding the development of post-partum cytological endometritis. BMC Genomics 16, 811.CrossRefGoogle ScholarPubMed
Fontana, S, Pacciarini, M, Boifava, M, Pellesi, R, Casto, B, Gastaldelli, M, Koehler, H, Pozzato, N, Casalinuovo, F and Boniotti, MB (2018) Development and evaluation of two multi-antigen serological assays for the diagnosis of bovine tuberculosis in cattle. Journal of Microbiological Methods 153, 118126.CrossRefGoogle Scholar
Franco, MM, Paes, AC, Ribeiro, MG, de Figueiredo Pantoja, JC, Santos, AC, Miyata, M, Leite, CQ, Motta, RG and Listoni, FJ (2013) Occurrence of mycobacteria in bovine milk samples from both individual and collective bulk tanks at farms and informal markets in the southeast region of Sao Paulo, Brazil. BMC Veterinary Research 9, 85.CrossRefGoogle ScholarPubMed
Gao, X, Guo, X, Li, M, Jia, H, Lin, W, Fang, L, Jiang, Y, Zhu, H, Zhang, Z, Ding, J and Xin, T (2019) Interleukin 8 and pentaxin (c-reactive protein) as potential new biomarkers of bovine tuberculosis. Journal of Clinical Microbiology 57, pii: e00274-19.CrossRefGoogle ScholarPubMed
Gilardoni, LR, Fernández, B, Morsella, C, Mendez, L, Jar, AM, Paolicchi, FA and Mundo, SL (2016) Mycobacterium paratuberculosis detection in cow's milk in Argentina by immunomagnetic separation-PCR. Brazilian Journal of Microbiology 47, 506512.CrossRefGoogle ScholarPubMed
Golby, P, Villarreal-Ramos, B, Dean, G, Jones, GJ and Vordermeier, M (2014) MicroRNA expression profiling of PPD-B stimulated PBMC from M. bovis-challenged unvaccinated and BCG vaccinated cattle. Vaccine 32, 58395844.CrossRefGoogle Scholar
Goosen, WJ, Cooper, D, Miller, MA, van Helden, PD and Parsons, SD (2015) IP-10 is a sensitive biomarker of antigen recognition in whole-blood stimulation assays used for the diagnosis of Mycobacterium bovis infection in African buffaloes (Syncerus caffer). Clinical and Vaccine Immunology 22, 974978.CrossRefGoogle Scholar
Hadi, SA, Waters, WR, Palmer, M, Lyashchenko, KP and Sreevatsan, S (2018) Development of a multidimensional proteomic approach to detect circulating immune complexes in cattle experimentally infected with Mycobacterium bovis. Frontiers in Veterinary Science 5, 141.CrossRefGoogle ScholarPubMed
Holcomb, ZE, Tsalik, EL, Woods, CW and McClain, MT (2017) Host-based peripheral blood gene expression analysis for diagnosis of infectious diseases. Journal of Clinical Microbiology 55, 360368.CrossRefGoogle ScholarPubMed
Hutchinson, P, Barkham, TM, Tang, W, Kemeny, DM, Chee, CB and Wang, YT (2015) Measurement of phenotype and absolute number of circulating heparin-binding hemagglutinin, ESAT-6 and CFP-10, and purified protein derivative antigen-specific CD4T cells can discriminate active from latent tuberculosis infection. Clinical and Vaccine Immunology 22, 200212.CrossRefGoogle Scholar
Hurley, WL and Theil, PK (2011) Perspectives on immunoglobulins in colostrum and milk. Nutrients 3, 442474.CrossRefGoogle ScholarPubMed
Iannaccone, M, Cosenza, G, Pauciullo, A, Garofalo, F, Proroga, YT, Capuano, F and Capparelli, R (2018) Milk microRNA-146a as a potential biomarker in bovine tuberculosis. Journal of Dairy Research 85, 178180.CrossRefGoogle ScholarPubMed
Jenkins, AO, Gormley, E, Gcebe, N, Fosgate, GT, Conan, A, Aagaard, C, Michel, AL and Rutten, VPMG (2018) Cross reactive immune responses in cattle arising from exposure to Mycobacterium bovis and non-tuberculous mycobacteria. Preventive Veterinary Medicine 152, 1622.CrossRefGoogle ScholarPubMed
Jones, GJ, Whelan, A, Clifford, D, Coad, M and Vordermeier, HM (2012) Improved skin test for differential diagnosis of bovine tuberculosis by the addition of Rv3020c-derived peptides. Clinical and Vaccine Immunology 19, 620622.CrossRefGoogle ScholarPubMed
Jorgensen, JB (1977) Survival of Mycobacterium paratuberculosis in slurry. Nordisk Veterinaermedicin 29, 267270.Google ScholarPubMed
Kabeer, BS, Raja, A, Raman, B, Thangaraj, S, Leportier, M, Ippolito, G, Girardi, E, Lagrange, PH and Goletti, D (2011) IP-10 response to RD1 antigens might be a useful biomarker for monitoring tuberculosis therapy. BMC Infectious Diseases 11, 135.CrossRefGoogle ScholarPubMed
Kasbohm, E, Fischer, S, Küntzel, A, Oertel, P, Bergmann, A, Trefz, P, Miekisch, W, Schubert, JK, Reinhold, P, Ziller, M, Fröhlich, A, Liebscher, V and Köhler, H (2017) Strategies for the identification of disease-related patterns of volatile organic compounds: prediction of paratuberculosis in an animal model using random forests. Journal of Breath Research 11, 047105.CrossRefGoogle Scholar
Klepp, LI, Eirin, ME, Garbaccio, S, Soria, M, Bigi, F and Blanco, FC (2019) Identification of bovine tuberculosis biomarkers to detect tuberculin skin test and IFNγ release assay false negative cattle. Research in Veterinary Science 122, 714.CrossRefGoogle ScholarPubMed
Küntzel, A, Fischer, S, Bergmann, A, Oertel, P, Steffens, M, Trefz, P, Miekisch, W, Schubert, JK, Reinhold, P and Köhler, H (2016) Effects of biological and methodological factors on volatile organic compound patterns during cultural growth of Mycobacterium avium ssp. paratuberculosis. Journal of Breath Research 10, 037103.CrossRefGoogle ScholarPubMed
Küntzel, A, Oertel, P, Fischer, S, Bergmann, A, Trefz, P, Schubert, J, Miekisch, W, Reinhold, P and Köhler, H (2018) Comparative analysis of volatile organic compounds for the classification and identification of mycobacterial species. PLoS One 13, e0194348.CrossRefGoogle ScholarPubMed
Lamont, EA, Ribeiro-Lima, J, Waters, WR, Thacker, T and Sreevatsan, S (2014a) Mannosylated lipoarabinomannan in serum as a biomarker candidate for subclinical bovine tuberculosis. BMC Research Notes 7, 559.CrossRefGoogle Scholar
Lamont, EA, Janagama, HK, Ribeiro-Lima, J, Vulchanova, L, Seth, M, Yang, M, Kurmi, K, Waters, WR, Thacker, T and Sreevatsan, S (2014b) Circulating Mycobacterium bovis peptides and host response proteins as biomarkers for unambiguous detection of subclinical infection. Journal of Clinical Microbiology 52, 536543.CrossRefGoogle Scholar
Larsen, AB, Merkal, RS and Vardaman, TH (1956) Survival time of Mycobacterium paratuberculosis. American Journal of Veterinary Research 17, 549551.Google ScholarPubMed
Lawn, SD (2012) Point-of-care detection of lipoarabinomannan (LAM) in urine for diagnosis of HIV-associated tuberculosis: a state of the art review. BMC Infectious Diseases 12, 103.CrossRefGoogle ScholarPubMed
Leung, KS, Siu, GK, Tam, KK, Ho, PL, Wong, SS, Leung, EK, Yu, SH, Ma, OC and Yam, WC (2018) Diagnostic evaluation of an in-house developed single-tube, duplex, nested IS6110 real-time PCR assay for rapid pulmonary tuberculosis diagnosis. Tuberculosis (Edinb) 112, 120125.CrossRefGoogle ScholarPubMed
Lewis, JM, Savage, RS, Beeching, NJ, Beadsworth, MBJ, Feasey, N and Covington, JA (2017) Identifying volatile metabolite signatures for the diagnosis of bacterial respiratory tract infection using electronic nose technology: a pilot study. PLoS One 12, e0188879.CrossRefGoogle Scholar
Li, L, Wagner, B, Freer, H, Schilling, M, Bannantine, JP, Campo, JJ, Katani, R, Grohn, YT, Radzio-Basu, J and Kapur, V (2017) Early detection of Mycobacterium avium subsp. paratuberculosis infection in cattle with multiplex-bead based immunoassays. PLoS One 12, e0189783.CrossRefGoogle ScholarPubMed
Li, L, Bannantine, JP, Campo, JJ, Randall, A, Grohn, YT, Schilling, MA, Katani, R, Radzio-Basu, J, Easterling, L and Kapur, V (2019) Identification of sero-diagnostic antigens for the early diagnosis of Johne's disease using MAP protein microarrays. Scientific Reports 9, 17573.CrossRefGoogle ScholarPubMed
Lyashchenko, KP, Grandison, A, Keskinen, K, Sikar-Gang, A, Lambotte, P, Esfandiari, J, Ireton, GC, Vallur, A, Reed, SG, Jones, G, Vordermeier, HM, Stabel, JR, Thacker, TC, Palmer, MV and Waters, WR (2017) Identification of novel antigens recognized by serum antibodies in bovine tuberculosis. Clinical and Vaccine Immunology 24, pii: e00259-17.CrossRefGoogle ScholarPubMed
MacHugh, DE, Gormley, E, Park, SD, Browne, JA, Taraktsoglou, M, O'Farrelly, C and Meade, KG (2009) Gene expression profiling of the host response to Mycobacterium bovis infection in cattle. Transboundary and Emerging Diseases 56, 204214.CrossRefGoogle ScholarPubMed
Malone, KM and Gordon, SV (2017) Mycobacterium tuberculosis complex members adapted to wild and domestic animals. Advances in Experimental Medicine and Biology 1019, 135154.CrossRefGoogle ScholarPubMed
Malvisi, M, Palazzo, F, Morandi, N, Lazzari, B, Williams, JL, Pagnacco, G and Minozzi, G (2016) Responses of bovine innate immunity to Mycobacterium avium subsp. paratuberculosis infection revealed by changes in gene expression and levels of microRNA. PLoS One 11, e0164461.CrossRefGoogle ScholarPubMed
Marassi, CD, Medeiros, L, McNair, J and Lilenbaum, W (2011) Use of recombinant proteins MPB70 or MPB83 as capture antigens in ELISAs to confirm bovine tuberculosis infections in Brazil. Acta Tropica 118, 101104.CrossRefGoogle ScholarPubMed
Mathevon, Y, Foucras, G, Falguières, R and Corbiere, F (2017) Estimation of the sensitivity and specificity of two serum ELISAs and one fecal qPCR for diagnosis of paratuberculosis in sub-clinically infected young-adult French sheep using latent class Bayesian modeling. BMC Veterinary Research 13, 230.CrossRefGoogle ScholarPubMed
Maurer, DL, Ellis, CK, Thacker, TC, Rice, S, Koziel, JA, Nol, P and VerCauteren, KC (2019) Screening of microbial volatile organic compounds for detection of disease in cattle: development of lab-scale method. Scientific Reports 9, 12103.CrossRefGoogle ScholarPubMed
Mayeux, R (2004) Biomarkers: potential uses and limitations. NeuroRx 1, 182188.CrossRefGoogle ScholarPubMed
McGill, I, Saunders, R, Eastwood, B, Menache, A, Dalzell, F, Hill, S, Irving, B, Knight, A and Jones, M (2018) Mycobacterium bovis tuberculosis in hunting hounds. Veterinary Record 183, 387388.CrossRefGoogle ScholarPubMed
Mehta, PK, Raj, A, Singh, NP and Khuller, GK (2014) Detection of potential microbial antigens by immuno-PCR (PCR-amplified immunoassay). Journal of Medical Microbiology 63, 627641.CrossRefGoogle Scholar
Michel, AL, Müller, B and van Helden, PD (2010) Mycobacterium bovis at the animal-human interface: a problem, or not? Veterinary Microbiology 140, 371381.CrossRefGoogle ScholarPubMed
Michelet, L, de Cruz, K, Karoui, C, Tambosco, J, Moyen, JL, Hénault, S and Boschiroli, ML (2018) Second line molecular diagnosis for bovine tuberculosis to improve diagnostic schemes. PLoS One 13, e0207614.CrossRefGoogle ScholarPubMed
Monasta, L, Pierobon, C, Princivalle, A, Martelossi, S, Marcuzzi, A, Pasini, F and Perbellini, L (2017) Inflammatory bowel disease and patterns of volatile organic compounds in the exhaled breath of children: a case-control study using ion molecule reaction-mass spectrometry. PLoS One 12, e0184118.CrossRefGoogle ScholarPubMed
Nagata, R, Kawaji, S and Mori, Y (2013) Use of enoyl coenzyme A hydratase of Mycobacterium avium subsp. paratuberculosis for the serological diagnosis of Johne's disease. Veterinary Immunology and Immunopathology 155, 253258.CrossRefGoogle ScholarPubMed
Nielsen, SS and Toft, N (2008) Ante mortem diagnosis of paratuberculosis: a review of accuracies of ELISA, interferon-gamma assay and faecal culture techniques. Veterinary Microbiology 129, 217235.CrossRefGoogle ScholarPubMed
Palmer, MV, Thacker, TC, Rabideau, MM, Jones, GJ, Kanipe, C, Vordermeier, HM and Ray Waters, W (2020) Biomarkers of cell-mediated immunity to bovine tuberculosis. Veterinary Immunology and Immunopathology 220, 109988.CrossRefGoogle ScholarPubMed
Park, HE, Shin, MK, Park, HT, Jung, M, Cho, YI and Yoo, HS (2016) Gene expression profiles of putative biomarker candidates in Mycobacterium avium subsp. paratuberculosis-infected cattle. Pathogens and Disease 74, ftw022.CrossRefGoogle ScholarPubMed
Park, HE, Park, HT, Jung, YH and Yoo, HS (2017a) Establishment a real-time reverse transcription PCR based on host biomarkers for the detection of the subclinical cases of Mycobacterium avium subsp. paratuberculosis. PLoS One 12, e0178336.CrossRefGoogle Scholar
Park, HT, Park, HE, Cho, YI, Kim, EH, Jung, M, Shin, SW, Lee, SH, Kim, DY and Yoo, HS (2017b) Potential biomarkers as an indicator of vertical transmission of Johne's disease in a Korean native cattle farm. Journal of Veterinary Science 18, 343349.CrossRefGoogle Scholar
Park, HE, Park, HT, Jung, YH and Yoo, HS (2018) Gene expression profiles of immune-regulatory genes in whole blood of cattle with a subclinical infection of Mycobacterium avium subsp. paratuberculosis. PLoS One 13, e0196502.CrossRefGoogle ScholarPubMed
Parsons, SD, McGill, K, Doyle, MB, Goosen, WJ, van Helden, PD and Gormley, E (2016) Antigen-specific IP-10 release is a sensitive biomarker of Mycobacterium bovis infection in cattle. PLoS One 11, e0155440.CrossRefGoogle ScholarPubMed
Ramos, DF, Silva, PE and Dellagostin, OA (2015) Diagnosis of bovine tuberculosis: review of main techniques. Brazilian Journal of Biology 75, 830837.CrossRefGoogle ScholarPubMed
Samba-Louaka, A, Robino, E, Cochard, T, Branger, M, Delafont, V, Aucher, W, Wambeke, W, Bannantine, JP, Biet, F and Héchard, Y (2018) Environmental Mycobacterium avium subsp. paratuberculosis hosted by free-living amoebae. Frontiers in Cellular and Infection Microbiology 8, 28.CrossRefGoogle ScholarPubMed
Sánchez-Soto, E, Ponce-Ramos, R, Hernández-Gutiérrez, R, Gutiérrez-Ortega, A, Álvarez, AH, Martínez-Velázquez, M, Absalón, AE, Ortiz-Lazareno, P, Limón-Flores, A, Estrada-Chávez, C and Herrera-Rodríguez, SE (2017) Colostrum proinflammatory cytokines as biomarkers of bovine immune response to bovine tuberculosis (bTB). Microbial Pathogenesis 103, 5764.CrossRefGoogle Scholar
Schiller, I, Oesch, B, Vordermeier, HM, Palmer, MV, Harris, BN, Orloski, KA, Buddle, BM, Thacker, TC, Lyashchenko, KP and Waters, WR (2010) Bovine tuberculosis: a review of current and emerging diagnostic techniques in view of their relevance for disease control and eradication. Transboundary and Emerging Diseases 57, 205220.Google ScholarPubMed
Schmidt, C, Plate, A, Angele, B, Pfister, HW, Wick, M, Koedel, U and Rupprecht, TA (2011) A prospective study on the role of CXCL13 in Lyme neuroborreliosis. Neurology 76, 10511058.CrossRefGoogle ScholarPubMed
Seth, M, Lamont, EA, Janagama, HK, Widdel, A, Vulchanova, L, Stabel, JR, Waters, WR, Palmer, MV and Sreevatsan, S (2009) Biomarker discovery in subclinical mycobacterial infections of cattle. PLoS One 4, e5478.CrossRefGoogle ScholarPubMed
Shin, SJ, Cho, D and Collins, MT (2008) Diagnosis of bovine paratuberculosis by a novel enzyme-linked immunosorbent assay based on early secreted antigens of Mycobacterium avium subsp. paratuberculosis. Clinical and Vaccine Immunology 15, 12771281.CrossRefGoogle ScholarPubMed
Shin, MK, Park, H, Shin, SW, Jung, M, Lee, SH, Kim, DY and Yoo, HS (2015a) Host transcriptional profiles and immunopathologic response following Mycobacterium avium subsp. paratuberculosis infection in mice. PLoS One 10, e0138770.CrossRefGoogle Scholar
Shin, MK, Park, HT, Shin, SW, Jung, M, Im, YB, Park, HE, Cho, YI and Yoo, HS (2015b) Whole-blood gene-expression profiles of cows infected with Mycobacterium avium subsp. paratuberculosis reveal changes in immune response and lipid metabolism. Journal of Microbiology and Biotechnology 25, 255267.CrossRefGoogle Scholar
Shirmohammadi, K, Sohrabi, S, Jafarzadeh Samani, Z, Effatpanah, H, Yadegarazari, R and Saidijam, M (2018) Evaluation of altered expression of miR-9 and miR-106a as an early diagnostic approach in gastric cancer. Journal of Gastrointestinal Oncology 9, 4651.CrossRefGoogle ScholarPubMed
Smith, RL, Schukken, YH, Pradhan, AK, Smith, JM, Whitlock, RH, Van Kessel, JS, Wolfgang, DR and Grohn, YT (2011) Environmental contamination with Mycobacterium avium subsp. paratuberculosis in endemically infected dairy herds. Preventive Veterinary Medicine 102, 19.CrossRefGoogle ScholarPubMed
Sockett, DC, Conrad, TA, Thomas, CB and Collins, MT (1992) Evaluation of four serological tests for bovine paratuberculosis. Journal of Clinical Microbiology 30, 11341139.CrossRefGoogle ScholarPubMed
Souza, II, Melo, ES, Ramos, CA, Farias, TA, Osório, AL, Jorge, KS, Vidal, CE, Silva, AS, Silva, MR, Pellegrin, AO and Araújo, FR (2012) Screening of recombinant proteins as antigens in indirect ELISA for diagnosis of bovine tuberculosis. Springerplus 1, 77.CrossRefGoogle ScholarPubMed
Souza, IIF, Rodrigues, RA, Gonçalves Jorge, KS, Silva, MR, Lilenbaum, W, Vidal, CES, Etges, RN, Kostovic, M and Araújo, FR (2019) ELISA Using a recombinant chimera of ESAT-6/MPB70/MPB83 for Mycobacterium bovis diagnosis in naturally infected cattle. Journal of Veterinary Medical Science 81, 914.CrossRefGoogle ScholarPubMed
Srinivasan, S, Jones, G, Veerasami, M, Steinbach, S, Holder, T, Zewude, A, Fromsa, A, Ameni, G, Easterling, L, Bakker, D, Juleff, N, Gifford, G, Hewinson, RG, Vordermeier, HM and Kapur, V (2019) A defined antigen skin test for the diagnosis of bovine tuberculosis. Science Advances 5, eaax4899.CrossRefGoogle Scholar
Stabel, JR (1998) Johne's disease: a hidden threat. Journal of Dairy Science 81, 283288.
Stabel, JR and Robbe-Austerman, S (2011) Early immune markers associated with Mycobacterium avium subsp. paratuberculosis infection in a neonatal calf model. Clinical and Vaccine Immunology 18, 393405.CrossRefGoogle Scholar
Steinbach, S, Vordermeier, HM and Jones, GJ (2019) Potential of the dual IFN-γ/IL-2 fluorescence-immunospot assay to distinguish different stages in bovine tuberculosis. Veterinary Immunology and Immunopathology 217, 109930.CrossRefGoogle ScholarPubMed
Strimbu, K and Tavel, JA (2010) What are biomarkers? Current Opinion in HIV & AIDS 5, 463466.CrossRefGoogle ScholarPubMed
Sweeney, RW (2011) Pathogenesis of paratuberculosis. Veterinary Clinics of North America: Food Animal Practice 27, 537546.Google ScholarPubMed
Tong, H, Wang, Y, Li, Y, Liu, S, Chi, C, Liu, D, Guo, L, Li, E and Wang, C (2017) Volatile organic metabolites identify patients with gastric carcinoma, gastric ulcer, or gastritis and control patients. Cancer Cell International 17, 108.CrossRefGoogle ScholarPubMed
Traxler, S, Bischoff, AC, Saß, R, Trefz, P, Gierschner, P, Brock, B, Schwaiger, T, Karte, C, Blohm, U, Schröder, C, Miekisch, W and Schubert, JK (2018) VOC Breath profile in spontaneously breathing awake swine during influenza A infection. Scientific Reports 8, 14857.CrossRefGoogle ScholarPubMed
Trefz, P, Koehler, H, Klepik, K, Moebius, P, Reinhold, P, Schubert, JK and Miekisch, W (2013) Volatile emissions from Mycobacterium avium subsp. paratuberculosis mirror bacterial growth and enable distinction of different strains. PLoS One 8, e76868.CrossRefGoogle ScholarPubMed
Tucci, P, González-Sapienza, G and Marin, M (2014) Pathogen-derived biomarkers for active tuberculosis diagnosis. Frontiers in Microbiology 5, 549.CrossRefGoogle ScholarPubMed
van den Esker, MH and Koets, AP (2019) Application of transcriptomics to enhance early diagnostics of mycobacterial infections, with an emphasis on Mycobacterium avium ssp. paratuberculosis. Veterinary Sciences 6, 59.CrossRefGoogle ScholarPubMed
van Kooten, HC, Mackintosh, CG and Koets, AP (2006) Intra-uterine transmission of paratuberculosis (Johne's disease) in farmed red deer. New Zealand Veterinary Journal 54, 1620.CrossRefGoogle Scholar
Walzl, G, McNerney, R, du Plessis, N, Bates, M, McHugh, TD, Chegou, NN and Zumla, A (2018) Tuberculosis: advances and challenges in development of new diagnostics and biomarkers. Lancet Infectious Diseases 18, e199e210.CrossRefGoogle ScholarPubMed
Waters, WR, Maggioli, MF, Palmer, MV, Thacker, TC, McGill, JL, Vordermeier, HM, Berney-Meyer, L, Jacobs, WR Jr and Larsen, MH (2015) Interleukin-17A as a biomarker for bovine tuberculosis. Clinical and Vaccine Immunology 23, 168180.CrossRefGoogle ScholarPubMed
Whitlock, RH and Buergelt, C (1996) Preclinical and clinical manifestations of paratuberculosis (including pathology). Veterinary Clinics of North America: Food Animal Practice 12, 345356.Google Scholar
Whittington, RJ, Marshall, DJ, Nicholls, PJ, Marsh, IB and Reddacliff, LA (2004) Survival and dormancy of Mycobacterium avium subsp. paratuberculosis in the environment. Applied and Environmental Microbiology 70, 29893004.CrossRefGoogle ScholarPubMed
World Health Organization (2015) The use of Lateral Flow Urine Lipoarabinomannan Assay (LF-LAM) for the Diagnosis and Screening of Active tuberculosis in People Living with HIV. Policy Update. Geneva, Switzerland: WHO.Google Scholar
Wright, K, Plain, K, Purdie, A, Saunders, BM and de Silva, K (2019) Biomarkers for detecting resilience against mycobacterial disease in animals. Infection and Immunity 88, e0040119.CrossRefGoogle ScholarPubMed
Xin, T, Gao, X, Yang, H, Li, P, Liang, Q, Hou, S, Sui, X, Guo, X, Yuan, W, Zhu, H, Ding, J and Jia, H (2018) Limitations of using IL-17A and IFN-γ-induced protein 10 to detect bovine tuberculosis. Frontiers in Veterinary Science 5, 28.CrossRefGoogle ScholarPubMed
You, Q, Verschoor, CP, Pant, SD, Macri, J, Kirby, GM and Karrow, NA (2012) Proteomic analysis of plasma from Holstein cows testing positive for Mycobacterium avium subsp. paratuberculosis (MAP). Veterinary Immunology and Immunopathology 148, 243251.CrossRefGoogle Scholar