Fecal culture and two fecal-PCR methods for the diagnosis of Mycobacterium avium subsp. paratuberculosis in a seropositive herd

Authors

  • Nathalia M. Correa Valencia University of Antioquia
  • Nicolás F. Ramírez University of Antioquia
  • Michael Bülte Justus Liebig University Giessen
  • Jorge A. Fernández Silva University of Antioquia

DOI:

https://doi.org/10.17533/udea.rccp.v30n2a02

Keywords:

culture medium, ELISA, Johne's disease, MAP, molecular diagnosis

Abstract

Background: paratuberculosis is a slow-developing infectious disease, characterized by chronic granulomatous enterocolitis. This disease has a variable incubation period from 6 months to over 15 years, and is caused by Mycobacterium avium subsp. paratuberculosis (MAP). Its detection by direct and indirect diagnostic techniques has been of special interest. Objective: to report the diagnosis and detection of MAP using several diagnostic tests in a herd of the Northern region of Antioquia, Colombia. Methods: serum samples from the study herd were analyzed, using a commercial ELISA (enzyme-linked immunosorbent assay) kit. Fecal samples were cultured by duplicate using Herrold´s egg yolk medium (HEYM), and analyzed by an endpoint IS900-specific nested PCR protocol, and a commercial F57-real-time PCR kit. Results: eight out of 27 serum samples in the study herd resulted ELISA-positive. None of fecal samples resulted positive to HEYM culture by duplicate and none were found to be positive by F57-real-time PCR. Seven of the 27 fecal samples were found to be positive by end-point IS900-specific nested PCR. Agreement was found between ELISA and end-point IS900-specific nested PCR in one of the animals. Conclusion: the present study gives information about the agreement between direct and indirect MAP-detection techniques, using different matrixes from animals under the same husbandry conditions.

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Author Biographies

Nathalia M. Correa Valencia, University of Antioquia

VM., MSc., DSc (c), Research Line in Epidemiology and Veterinary Public Health, Centauro Research Group, School of Veterinary Medicine, Faculty of Agrarian Sciences, University of Antioquia, Medellín, Colombia.

 

Nicolás F. Ramírez, University of Antioquia

VM., MSc., Dr. An. Sci., Research Line in Epidemiology and Veterinary Public Health, Centauro Research Group, School of Veterinary Medicine, Faculty of Agrarian Sciences, University of Antioquia, Medellín, Colombia.

Michael Bülte, Justus Liebig University Giessen

Prof., Dr. Vet. Med., Institute for Veterinary Food Science, Department of Veterinary Medicine, Justus Liebig University Giessen, Giessen, Germany.

Jorge A. Fernández Silva, University of Antioquia

VM., MSP., Dr. Vet. Med., Research Line in Epidemiology and Veterinary Public Health, Centauro Research Group, School of Veterinary Medicine, Faculty of Agrarian Sciences, University of Antioquia, Medellín, Colombia.

References

Alinovi CA, Ward MP, Lin TL, Moore GE, Wu CC. Real-time PCR, compared to liquid and solid culture media and ELISA, for the detection of Mycobacterium avium subsp. paratuberculosis. Vet Microbiol 2009; 14:177-179.

Al-Soud W, Radstrom AP. Capacity of nine thermostable DNA polymerases to mediate DNA amplification in the presence of PCR-inhibiting samples. Appl Environ Microbiol 1998; 64:3748-3753.

Álvarez J, de Juan L Bezos J, Romero B, Sáez JL, Marqués S, Domíngues C, Minguez O, Fernández-Mardomingo B, Mateos A, Domínguez L, Aranaz, A. Effect of paratuberculosis on the diagnosis of bovine tuberculosis in a cattle herd with a mixed infection using interferon-gamma detection assay. Vet Microbiol 2009; 135:389-393.

Aly SS, Mangold BL, Whitlock RH, Sweeney RW, Anderson RJ, Jiang J, Schukken YH, Hovingh E, Wolfgang D, Van Kessel JAS, Karns JS, Lombard JE, Smith JM, Gardner IA. Correlation between Herrold egg yolk medium culture and real-timequantitative polymerase chain reaction results for Mycobacterium avium subspecies paratuberculosisin pooled fecal and environmental samples. J Vet Diagn Invest 2010; 22(5):677-683.

Aly SS, Anderson RJ, Whitlock RH, Fyock TL, McAdams SC, Byrem TM, Jiang J, Adaska JM, Gardnerl IA. Cost-effectiveness of diagnostic strategies to identify Mycobacterium avium subspecies paratuberculosis super-shedder cows in a large dairy herd using antibody enzyme-linked immunosorbent assays, quantitative real-time polymerase chain reaction, and bacterial culture. J Vet Diagnostic Invest 2012; 24:821-832.

Anonymous. Uniform program standards for the voluntary bovineJohne's disease control program. In: United States Department of Agriculture-USDA, Animal and Plant Health Inspection Service-APHIS; 2010. 40 p.

Atreya R, Bülte M, Gerlach GF, Goethe R, Hornef MW, Köhler H, Meensd J, Möbiusf P, Roebg E, Weissh S. Facts, mythsand hypotheses on the zoonotic nature of Mycobacterium avium subspecies paratuberculosis. Int J Med Microbiol 2014; 304(7):858-867.

Ayele WY, Machá ková M, Pavlík I. The transmission and impact of paratuberculosis infection in domestic and wild ruminants. Vet Med Czech 2001; 46:205-224.

Bölske G, Herthnek D. Diagnosis of paratuberculosis by PCR. In: Behr MA, Collins DM, editors. Paratuberculosis: Organism, disease, control. First edition. Cambridge, MA: Editorial Cabi International; 2010. p. 267-278.

Bulander K. Vergleichende Untersuchungen zum Nachweisvon Mycobacterium avium ssp. paratuberculosis in Milchrinderbeständen. Dissertation, Fachbereich Veterinärmedizin, Justus-Liebig-Universität Giessen, Germany 2009. 214p.

Bull TJ, Sidi-Boumedine K, McMinn EJ, Stevenson K, Pickup R, Hermon-Taylor J. Mycobacterial interspersed repetitiveunits (MIRU) differentiate Mycobacterium avium subspecies paratuberculosis from other species of the Mycobacterium avium complex. Mol Cel Probes 2003; 17:157-164.

Bülte M, Schonenbrucher H, Abdulmawjood A. From farm to fork —Mycobacteriumavium ssp. paratuberculosis (MAP) as zoonotic agent? Berl Munch Tierarztl Wochenschr 2005; 118:377-385.

Cernicchiaro N, Wells SJ, Janagama H, Sreevatsan S. Influence of type of culture medium on characterization of Mycobacterium avium subsp. paratuberculosis subtypes. J Clin Microbiol 2008; 46(1):145-149.

Chacon O, Bermudez LE, Barletta RG. Johne’s disease, inflammatory bowel disease, and Mycobacterium paratuberculosis. Annu Rev Microbiol 2004; 58:329-363.

Clark Jr DL, Koziczkowski JJ, Radcliff RP, Carlson RA, Ellingson JLE. Detection of Mycobacterium avium subspecies paratuberculosis: comparing fecal culture versus serum enzyme-linked immunosorbent assay and direct fecal polymerase chain reaction. J Dair Sci 2008; 91:2620-2627.

Clarke CJ. The pathology and pathogenesis of paratuberculosis in ruminants and other species. J Comp Path 1997; 116:217-261.

Coetsier C, Vannuffel P, Blondeel N, Denef JF, Cocito C, Gala JL. Duplex PCR for differential identification of Mycobacterium bovis, M. avium, and M. avium subsp. paratuberculosis in formalin-fixed paraffin-embedded tissues from cattle. J Clin Microbiol 2000; 38:3048-3054.

Collins MT. Diagnosis of paratuberculosis. Vet Clin North Am Food Anim Pract 1996; 12:357-371.

Collins DM, Gabric DM, de Lisle GW. Identification of a repetitive DNA sequence specific to Mycobacterium paratuberculosis. FEMS Microbiol Lett 1989; 60:175-178.

Collins DM, Gabric DM, de Lisle GW. Identification of two groups of Mycobacterium paratuberculosis strains by restriction endonuclease analysis and DNA hybridization. J Clin Microbiol 1990; 28:1591-1596.

Collins MT, Gardner IA, Garry FB, Roussel AJ, Wells SJ. Consensus recommendations on diagnostic testing for the detection of paratuberculosis in cattle in the United States. J Am Vet Med Assoc 2006; 229:1912-1919.

Collins MT, Sockett DC, Goodger WJ, Conrad TA, Thomas CB, Carr DJ. Herd prevalence and geographic distribution of, and risk factors for, bovine paratuberculosis in Wisconsin. J Am Vet Med Assoc 1994; 204(4): 636-641.

Correa Valencia NM, Ramírez NF, Olivera M, Fernández Silva JA. Milk yield and lactation stage are associated with positive results to ELISA for Mycobacterium avium subsp. paratuberculosis in dairy cows from Northern Antioquia, Colombia: a preliminary study. Trop Anim Health Prod 2016; 48:1191-1200.

Cousins DV, Whittington R, Marsh I, Masters A, Evans RJ, Kluver P. Mycobacteria distinct from Mycobacterium avium subsp. paratuberculosis isolated from the faeces of ruminants possess IS900 -like sequences detectable IS900 polymerase chain reaction: implications for diagnosis. Mol Cell Probes 1999;13:431-442.

Crossley BM, Zagmutt-Vergara FJ, Fyock TL, Whitlock RH, Gardner IA. Fecal shedding of Mycobacterium avium subsp. paratuberculosis by dairy cows. Vet Microbiol 2005; 107: 257-263.

Dieguez FJ, Arnaiz I, Sanjuan ML, Vilar MJ, Yus E. Management practices associated with Mycobacterium avium subspecies paratuberculosis infection and the effects of the infection on dairy herds. Vet Rec 2008; 162:614-617.

Dreier S, Khol JL, Stein B, Fuchs K, Gutler S, Baumgartner W. Serological, bacteriological and molecular biological survey of paratuberculosis (Johne’s disease) in Austrian cattle. J Vet Med B Infect Dis Vet Public Health 2006; 53:477-481.

Eamens GJ, Whittington RJ, Marsh IB, Turner ML, Saunders V, Kemsley PD, Rayward D. Comparative sensitivity of various fecal culture methods and ELISA in dairy cattle herds with endemic Johne's disease. Vet Microbiol 2000; 85:243-251.

Ellingson JL, Stabel JR, Bishai WR, Frothingham R, Miller JM. Evaluation of the accuracy and reproducibility of a potential PCR panel assay for rapid detection and differentiation of Mycobacterium avium subsp. paratuberculosis. Mol Cell Probes 2000; 14:153-161.

Englund S, Bölske G, Ballagi-Pordány A, Johansson KE. Detection of Mycobacterium avium subsp. paratuberculosis in tissue samples by single, fluorescent and nested PCR based on the IS900 gene. Vet Microbiol 2001; 81:257-271.

Englund S, Bolske G, Johansson KE. An IS900-like sequencefound in a Mycobacterium sp. other than Mycobacterium avium subsp. paratuberculosis. FEMS Microbiol Lett 2002; 209:267-271.

Fecteau ME, Whitlock RH. Paratuberculosis in cattle. In: Behr MA, Collins DM, editors. Paratuberculosis: Organism, disease, control. First edition. Cambridge, MA: Editorial Cabi International; 2010. p. 144-153.

Fernández Silva JA, Abdulmawjood A, Akineden O, Bülte M. Serological and molecular detection of Mycobacterium avium subsp. paratuberculosisin cattle of dairy herds in Colombia. Trop Anim Health Prod 2011a; 43:1501-1507.

Fernández Silva JA, Abdulmawjood A, Bülte M. Diagnosisand molecular characterization of Mycobacterium aviumsubsp. paratuberculosis from dairy cows in Colombia. Vet Med Int 2011b; 1-29.

Fernández Silva JA, Ramírez Vásquez NF. Factors associated with the paratuberculosis serum enzyme-linked immunosorbent assay (ELISA) status of dairy cows from two municipalities of the Northern Antioquia, Colombia. Rev Colomb Cienc Pecu 2015; 28(Sup):91.

Füllgrabe RAR. Untersuchungen zum kulturellen und Molekularbiologischen nachweis von Mycobacterium avium ssp. paratuberculosis (MAP) aus humanen darmbioptaten. Inaugural-Dissertation, Fachbereich Veterinärmedizin, Justus-Liebig-Universität Giessen, 2009. 308p. http://geb.uni-giessen.de/geb/volltexte/2009/6826/pdf/FuellgrabeRegina-2008-12-18.pdf

García Ab, Shalloo L. Invited review: the economic impactand control of paratuberculosis in cattle. J Dairy Sci 2015;98(8):501939.

Gill CO, Saucier L, Meadus WJ. Mycobacterium avium subsp. paratuberculosisin dairy products, meat, and drinking water. J Food Prot 2011; 74:480-499.

Glanemann B, Hoelzle LE, Bogli-Stuber K, Jemmi T, Wittenbrink MM. Detection of Mycobacterium avium subspecies paratuberculosisin Swiss dairy cattle by culture and serology. Schweiz Arch Tierheilkd 2004; 146:409-415.

Godfroid J, Delcorps C, Irenge LM, Walravens K, Marche S, Gala JL. Definitive differentiation between single and mixed mycobacterial infections in red deer (Cervus elaphus) by a combination of duplex amplification of p34 and F57 sequences and Hpy188I enzymatic restriction of duplex amplicons. Clin Microbiol 2005; 43:4640-4648.

Goodger WJ, Collins MT, Nordlund KV, Eisele C, PelletierJ, Thomas CB, Sockett DC. Epidemiologic study of on-farm management practices associated with prevalence of Mycobacterium paratuberculosis infections in dairy cattle. J Am Vet Med Assoc 1996; 208:1877-1881.

Grant IR, Ball HJ, Rowe MT. Isolation of Mycobacterium paratuberculosis from milk by immunomagnetic separation. Appl Environ Microbiol 1998; 64(9):3153-3158.

Green EP, Tizard MLV, Moss MT, Thompson J, Winterbourne DJ, McFadden JJ, Hermon Taylor J. Sequence and characteristics of IS900, an insertion element identified in a human Crohn’s disease isolate of Mycobacterium paratuberculosis. Nucleic Acids Res 1989; 17:9063-9073.

Hanifian S. Survival of Mycobacterium avium subsp. paratuberculosis in ultra-filtered white cheese. Lett Appl Microbiol 2014; 16.

Harris NB, Barletta RG. Mycobacterium aviumsubspeciesparatuberculosis in veterinary medicine. Clin Microbiol Rev 2001; 14:489-512.

Herthnek D. Molecular diagnostic methods for Mycobacterium avium subsp. paratuberculosis: more than a gut feeling. Inaugural-Dissertation Dr. med. vet. Faculty of Veterinary Medicine and Animal Science, Department of Biomedical Sciences and Veterinary Public Health, Uppsala, 2009, 67p.

Herthnek D, Bölske G. New PCR systems to confirm real-time PCR detection of Mycobacterium avium subsp. paratuberculosis. BMC Microbiol 2006 4; 6:87.

Ikonomopoulos J, Gazouli M, Pavlik I, Bartos M, Zacharatos P, Xylouri E, Papalambros E, Gorgoulis V. Comparative evaluation of PCR assays for the robust molecular detectionof Mycobacterium avium subsp. paratuberculosis. J Microbiol Methods 2004; 56:315-321.

Inglis GD, Kalischuck LD. Use of PCR for direct detection of Campylobacter species in bovine feces. Appl Environ Microbiol 2003; 69; 3435-3447.

Jakobsen MB, Alban L, Nielsen SS. A cross-sectional study of paratuberculosis in 1155 Danish dairy cows. Prev Vet Med 2000; 46:15-27.

Kalis CH, Barkema HW, Hesselink JW, van Maanen C, Collins MT. Evaluation of two absorbed enzyme-linked immunosorbent assays and a complement fixation test as replacements for fecal culture in the detection of cows shedding Mycobacterium avium subspecies paratuberculosis. J Vet Diagn Invest 2002; 14:219-224.

Kawaji S, Taylor DL, Mori Y, Whittington RJ. Detection of Mycobacterium avium subsp. paratuberculosis in ovine feces by direct quantitative PCR has similar or greater sensitivity compared to radiometric culture. Vet Microbiol 2007; 125(1-2):36-48.

Keller SM, Stephan R, Kuenzler R, Meylan M, Wittenbrink MM. Comparison of fecal culture and F57 real-time polymerase chain reaction for the detection of Mycobacterium avium subspecies paratuberculosis in Swiss cattle herds with a history of paratuberculosis. Acta Vet Scand 2014; 56:68.

Khare S, Adams LG, Osterstock J, Roussel A, David L. Effects of shipping and storage conditions of fecal samples on viability of Mycobacterium paratuberculosis. J Clin Microbiol 2008;46(4):1561-1562.

Kim SG, Shin SJ, Jacobson RH, Miller LJ, Harpending PR, Stehman SM, Rossiter CA, Lein DA. Development and application of quantitative polymerase chain reaction assay basedon the ABI 7700 system (TaqMan) for detection and quantificationof Mycobacterium avium subsp. paratuberculosis. J Vet Diagn Invest 2002; 14(2):126-131.

Kralik P, Nocker A, Pavlik I. Mycobacterium avium subsp. paratuberculosis viability determination using F57 quantitative PCR in combination with propidium monoazide treatment. Int J Food Microbiol 2010; 141 Suppl 1:S80-6.

Künzler R, Torgerson P, Keller S, Wittenbrink M, Stephan R, Knubben-Schweizer G, Berchtold B, Meylan M. Observed management practices in relation to the risk of infection with paratuberculosis and to the spread of Mycobacterium avium ssp. paratuberculosis in Swiss dairy and beef herds. BMC Vet Res 2014; 10:132.

Lavers CJ, Dohoo IR, McKenna SL, Keefe GP. Sensitivity and specificity of repeated test results from a commercial milk enzyme-linked immunosorbent assay for detection of Mycobacterium avium subspecies paratuberculosis in dairy cattle. J Am Vet Med Association 2015; 246(2):236-244.

Leite FL, Stokes KD, Robbe-Austerman S, Stabel JR. Comparisonof fecal DNA extraction kits for the detection of Mycobacterium avium subsp. paratuberculosis by polymerase chain reaction. J Vet Diagn Invest 2013; 25(1):27-34.

Liverani E, Scaioli E, Cardamone C, Dal Monte P, Belluzzi A. Mycobacterium avium subspecies paratuberculosis in the etiology of Crohn’s disease, cause or epiphenomenon? World J Gastroenterol 2014; 20(36):13060-130670.

Manning EJ, Collins MT. Mycobacterium avium subsp. paratuberculosis: pathogen, pathogenesis and diagnosis. Rev Sci Tech 2001; 20:133-150.

McAloon Cg, Whyte P, More Sj, Green Mj, O’grady L, Garcia A, Doherty Ml. The effect of paratuberculosis on milk yield —A systematic review and meta-analysis. J Dairy Sci 2016;99(2):1449-1160.

McKenna SL, Barkema HW, Keefe GP, Sockett DC. Agreement between three ELISAs for Mycobacterium avium subsp. paratuberculosis in dairy cattle. Vet Microbiol 2006; 114:285-291.

Merkal RS. Diagnostic methods for detection of paratuberculosis (Johne’s disease). 74th Annual Meeting of the US Animal Health Association, 1970, Abstract 74, p. 620-3, USA.

Möbius P, Hotzel H, Rassbach A, Kohler H. Comparison of 13 single-round and nested PCR assays targeting IS900, ISMav2, F57 and locus 255 for detection of Mycobacterium avium subsp. paratuberculosis. Vet Microbiol 2008a; 126:324-333.

Möbius P, Luyven G, Hotzel H, Köhler H. High genetic diversity among Mycobacterium avium subsp. paratuberculosis strains from German cattle herds shown by combination of IS900 restriction fragment length polymorphism analysis and mycobacterial interspersed repetitive unit-variable-numbertandem-repeat typing. J Clin Microbiol 2008b; 46(3):972-981.

Mon ML, Viale M, Baschetti G, Alvarado Pinedo F, Gioffre A, Travería G, Willemsen P, Bakker D, Romano MI. Search for Mycobacterium avium subspecies paratuberculosis antigens for the diagnosis of paratuberculosis. Vet-Med International 2012, 860362.

Motiwala AS, Amonsin A, Strother M, Manning EJ, Kapur V, Sreevatsan S. Molecular epidemiology of Mycobacterium avium subsp. paratuberculosis isolates recovered from wild animal species. J Clin Microbiol 2004; 42:1703-1712.

Motiwala AS, Strother M, Theus NE, Stich RW, Byrum B, Shulaw WP, Kapur V, Sreevatsan S. Rapid detection and typing of strains of Mycobacterium avium subsp. paratuberculosis from broth cultures. J Clin Microbiol 2005; 43:2111-2117.

Muskens J, Mars MH, Elbers AR, van Maanen K, Bakker D. The results of using faecal culture as confirmation test of paratuberculosis-seropositive dairy cattle. J Vet Med B Infect Dis Vet Public Health 2003; 50:231-234.

National Advisory Committee on Microbiological Criteria for Foods. Assessment of food as a source of exposure to Mycobacterium avium subspecies paratuberculosis (MAP). J Food Prot 2010; 73:1357-1397.

Nielsen SS. Transitions in diagnostic tests used for detection of Mycobacterium avium subsp. paratuberculosis infections in cattle. Vet Microbiol 2008; 132(3-4):274-282.

Nielsen SS. Immune-based diagnosis of paratuberculosis. In: Behr, M.A., Collins, D.M. (Eds.), Paratuberculosis: Organism, Disease, Control. CAB International, Oxfordshire, 2010. pp. 284-293.

Nielsen SS, Toft N. Ante-mortemdiagnosis of paratuberculosis: a review of accuracies of ELISA, interferon-gama assay, and fecal culture techniques. Vet Microbiol 2008; 129:217-235.

Nielsen SS, Toft N. A review of prevalences of paratuberculosis in farmed animals in Europe. Prev Vet Med 2009; 88:1-14.

Radomski N, Kreitmann L, McIntosh F, Behr MA. The critical role of DNA extraction for detection of mycobacteria in tissues. PLoS One 2013; 8:e78749.

Rajeev S, Zhang Y, Sreevatsan S, Motiwala AS, Byrum B. Evaluation of multiple genomic targets for identification and confirmation of Mycobacterium avium subsp. paratuberculosis isolates using real-time PCR. Vet Microbiol 2005; 105:215-221.

Reddacliff LA, Vadali A, Whittington RJ. The effect of decontamination protocols on the numbers of sheep strain Mycobacterium avium subsp. paratuberculosis isolated from tissues and faeces. Vet Microbiol 2003; 24:271-282.

Odumeru J, Gao A, Chen S, Raymond M, Mutharia L. Use of the bead beater for preparation of Mycobacterium paratuberculosis template DNA in milk. Can J Vet Res 2001; 65(4):201-205.

Salem M, Heydel C, El-Sayed A, Ahmed SA, Zschöck M, Baljer G. Mycobacterium avium subspecies paratuberculosis: an insidious problem for the ruminant industry. Trop Anim Health Prod 2013; 45:351-366.

Schönenbrücher H, Abdulmawjood A, Failing K, Bülte M. New triplex real-time PCR assay for detection of Mycobacterium avium subsp. paratuberculosis in bovine feces. Appl. Environ Microbiol 2008; 74:2751-2758.

Sidoti F, Banche G, Astegiano S, Allizond V, Cuffini AM, Bergallo M. Validation and standardization of IS900 and F57 real-time quantitative PCR assays for the specific detection and quantification of Mycobacterium aviumsubsp. paratuberculosis. Can J Microbiol 2011; 57(5):347-354.

Slana I, Liapi M, Moravkova M, Kralova A, Pavlik I. Mycobacterium avium subsp. paratuberculosis in cow bulk tank milk in Cyprus detected by culture and quantitative IS900 and F57 real-time PCR. Prev Vet Med 2009; 89(3-4):223-226.

Sorge US, Lissemore K, Godkin A, Jansen J, Hendrick S, Wells S, Kelton DF. Risk factors for herds to test positive for Mycobacterium avium ssp. paratuberculosis-antibodies with a commercial milk enzyme-linked immunosorbent assay (ELISA) in Ontario and western Canada. Can Vet J 2012; 53:963-970.

Stabel JR., Bosworth TL, Kirkbride TA, Forde RL, Whitlock RH. A simple, rapid, and effective method for the extraction of Mycobacterium paratuberculosis DNA from fecal samples for polymerase chain reaction. J Vet Diagn Investig 2004; 16:22-30.

Stabel JR, Bannantine JP. Development of a nested PCR method targeting a unique multicopy element, ISMap02, for detection of Mycobacterium avium subsp. paratuberculosis in fecal samples. J Clin Microbiol 2005; 43:4744-4750.

Stevenson K. Comparative differences between strains of Mycobacterium avium subsp. paratuberculosis. In: Behr MA, Collins DM, editors. Paratuberculosis: Organism, disease, control. First edition. Cambridge, MA: Editorial Cabi International; 2010a.p. 126-132.

Stevenson K. Diagnosis of Johne ́s disease: current limitations and prospects. Cattle Practice 2010b; 18:104-109.

Stevenson K. Genetic diversity of Mycobacterium avium subspecies paratuberculosis and the influence of strain type on infection and pathogenesis: a review. Vet Res 2015; 46:64.

Stevenson K, Sharp JM. The contribution of molecular biology to Mycobacterium avium subspecies paratuberculosis research. Vet J 1997; 153(3):269-286.

Stich RW, Byrum B, Love B, Theus N, Barber L, Shulaw WP. Evaluation of an automated system for non-radiometric detection of Mycobacterium avium paratuberculosis in bovine feces. J Microbiol Methods 2004; 56(2):267-275.

Strommenger B, Stevenson K, Gerlach GF. Isolation and diagnostic potential of ISMav2, a novel insertion sequence-like element from Mycobacterium avium subspecies paratuberculosis. FEMS Microbiol Lett 2001; 196:31-37.

Sweeney RW. Transmission of paratuberculosis. Vet Clinic North Am Food Anim Pract 1996; 12(2):305-312.

Sweeney RW, Whitlock RH, McAdams S, Fyock T. Longitudinalstudy of ELISA seroreactivity to Mycobacterium avium subsp. paratuberculosis in infected cattle and culture negative herd mates. J Vet Diagn Invest 2006; 18:2-6.

Sweeney RW, Collins MT, Koets AP, McGuirk SM, Roussel AJ. Paratuberculosis (Johne’s disease) in cattle and other susceptible species. J Vet Intern Med 2012; 26(6):1239-1250.

Taddei R, Barbieri I, Pacciarini ML, Fallacara F, Belletti GL, Arrigoni N. Mycobacterium porcinum strains isolated from bovine bulk milk: implications for Mycobacterium avium subsp. paratuberculosis detection by PCR and culture. Vet Microbiol 2008; 130(3-4):338-347.

Tasara T, Hoelzle LE, Stephan R. Development and evaluation of a Mycobacterium avium subspecies paratuberculosis (MAP) specific multiplex PCR assay. Int J Food Microbiol 2005;104:279-287.

Tiwari A, VanLeeuwen JA, McKenna LB, Keefe GP, Barkema HW. Johne’s disease in Canada. Part I. Clinical symptoms, pathophysiology, diagnosis, and prevalence in dairy herds. J Vet Can 2006; 47:874-882.

Tiwari A, VanLeeuwen JA, Dohoo IR, Keefe GP, Haddad JP, Scott HM, Whiting T. Risk factors associated with Mycobacterium avium subspecies paratuberculosis seropositivity in Canadian dairy cows and herds. Prev Vet Med 2009; 88:32-41.

Thorton CG, Passen S. Inhibition of PCR amplification by phytic acid, and treatment of bovine fecal specimens with phytase to reduce inhibition. J Microbiol Methods 2004; 100:97-204.

USDA, APHIS, VS, and CEAH. National Animal Health Monitoring System (NAHMS) dairy 2007: Johne’s disease on U.S. dairy operations. United States Department of Agriculture, Animal and Plant Health Inspection Service, Veterinary Services National Animal Health Monitoring System, Washington, DC. 2008. [Access date: February 1st, 2016]. URL: https://www.aphis.usda.gov/animal_health/nahms/dairy/downloads/dairy07/Dairy07_is_Johnes.pdf

Vansnick E, De Rijk P, Vercammen F, Geysen D, Rigouts L, Portaels F. Newly develop primers for the detection of Mycobacterium avium subsp. paratuberculosis. Vet Microbiol 2004; 100:197-204.

van Schaik G, Stehman SM, Schukken YH, Rossiter CR, Shin SJ. Pooled fecal culture sampling for Mycobacterium avium subsp. paratuberculosis at different herd sizes and prevalence. J Vet Diagn Investig 2003; 15:233-241.

van Schaik G, Pradenas F M, Mella N A, Kruze V J. Diagnostic validity and costs of pooled fecal samples and individual blood or fecal samples to determine the cow- and herd-status for Mycobacterium avium subsp. paratuberculosis. Prev Vet Med 2007; 82(1-2):159-165.

Vansnicka E, de Rijkb P, Vercammenc F, Geysena D, Rigoutsb L, Portaelsb F. Newly developed primers for the detection of Mycobacterium avium subspecies paratuberculosis. Vet Microbiol2004; 100(3-4):197-204.

Vilar AL, Santos CS, Pimenta CL, Freitas TD, Brasil AW, Clementino IJ, Alves CJ, Bezerra CS, Riet Correa F, Oliveira TS, Azevedo SS. Herd-level prevalence and associated risk factors for Mycobacterium avium subsp. paratuberculosis in cattle in the State of Paraíba, Northeastern Brazil. Prev Vet Med 2015; 121(1-2):49-55.

Waddell LA, Rajić A, Stärk KD, McEwen SA. The zoonotic potential of Mycobacterium avium ssp. paratuberculosis: a systematic review and meta-analyses of the evidence. Epidemiol Infect 2015; 143(15):3135-3157.

Waddell LA, Rajić A, Stärk KD, McEwen SA. The potential public health impact of Mycobacterium avium ssp. paratuberculosis: Global opinion survey of topic specialists. Zoon Pub Health2016; 63(3):212-222.

Wells SJ, Wagner BA. Herd-level risk factors for infection with Mycobacterium paratuberculosis in US dairies and association between familiarity of the herd manager with the disease or prior diagnosis of the disease in that herd and use of preventive measures. J Am Vet Med Assoc 2000; 216:1450-1457.

Whitlock RH, Buergelt C. Preclinical and clinical manifestation of paratuberculosis (including pathology). Vet Clin North Am Food Anim Pract 1996; 12:345-356.

Whitlock RH, Wells SJ, Sweeney RW, Van Tiem J. Vet Microbiol 2000; 77(3-4):387-398.

Whittington RJ. Factors affecting isolation and identification of Mycobacterium avium subsp. paratuberculosis from fecal and tissue samples in a liquid culture system. J Clin Microbiol 2009; 47(3):614-622.

Whittington RJ. Cultivation of Mycobacterium avium subsp. paratuberculosis. In: Behr MA, Collins DM, editors. Paratuberculosis: Organism, disease, control. First edition. Cambridge, MA: Editorial Cabi International; 2010. p. 244-260.

Whittington RJ, Marsh IB, Saunders V, Grant IR, Juste R, Sevilla IA, Manning EJ, Whitlock RH. Culture phenotypes of genomically and geographically diverse Mycobacterium avium subsp. paratuberculosis isolates from different hosts. J Clin Microbiol 2011; 49:1822-1830.

Zecconi A, Mosca A, Piccinini R, Robbi C. A comparison of seven different protocols to extract Mycobacterium avium subspecies paratuberculosis DNA from bovine feces. In: Juste RA, Geijo MV, Garrido JM (Eds) Proceedings of the seventh international colloquium on paratuberculosis. International Association for Paratuberculosis, Madison, WI, pp. 270-273.

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2017-04-26

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Correa Valencia, N. M., Ramírez, N. F., Bülte M., & Fernández Silva, J. A. (2017). Fecal culture and two fecal-PCR methods for the diagnosis of Mycobacterium avium subsp. paratuberculosis in a seropositive herd. Revista Colombiana De Ciencias Pecuarias, 30(2), 101–115. https://doi.org/10.17533/udea.rccp.v30n2a02

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Original research articles