Latent infections are the most frequent form of paratuberculosis in slaughtered Friesian cattle

  1. Vázquez, Patricia
  2. Garrido Urkullu, Joseba M.
  3. Molina, Elena
  4. Geijo Vázquez, María V.
  5. Gómez, Nieves
  6. Pérez Pérez, Valentín
  7. Sevilla Agirregomoskorta, Iker
  8. Alonso Hearn, Marta
  9. Cortés Alonso, Mª Adoración
  10. Juste Jordán, Ramón Antonio
Journal:
Spanish journal of agricultural research

ISSN: 1695-971X 2171-9292

Year of publication: 2014

Volume: 12

Issue: 4

Pages: 1049-1060

Type: Article

DOI: 10.5424/SJAR/2014124-5978 DIALNET GOOGLE SCHOLAR lock_openDialnet editor

More publications in: Spanish journal of agricultural research

Sustainable development goals

Abstract

Paratuberculosis is a chronic mycobacterial infection causing granulomatous enteritis in ruminants, whose pathogenesis and epidemiology poses numerous challenges, including latency and reactivation. The most recent and complete classification of paratuberculosis immunopathological types in cattle recognized five categories. In this study, 1031 slaughtered Friesian cattle were submitted to serological, microbiological and pathological examinations with the aim of maximizing the rate of case detection. In most cases, infected animals had minimal lesions and almost no other proof of infection (38.9%), while the more characteristic types with the whole constellation of microbiological and immunological evidences accounted for a lower proportion (7.7%). As these findings in cattle suggest similarities with the epidemiology of tuberculosis in humans, we propose to re-group the original immunopathological types into two broader paratuberculosis epidemio-pathogenic forms or states: latent and patent. The former term would define infections with focal lesions and might constitute an apparent resilience status representing a difficult to detect reservoir of infection whose role could become critical if later immune-compromising factors lead to re-activation. The latter would group those cases with multifocal and diffuse inflammatory lesions with higher mycobacterial load and viability suggestive of a more immediate epidemiological risk. Interestingly, the relative frequency of presentation of each profile varied with age. The proportion of latent forms remained relatively constant between 33.8% and 54.3% through adulthood from 3 years of age, while patent forms were more frequent during the first years of age and tended to decrease among the oldest individuals.

Bibliographic References

  • Alonso-Hearn M, Molina E, Geijo M, Vazquez P, Sevilla IA, Garrido JM, Juste RA, 2012. Immunization of adult dairy cattle with a new heat-killed vaccine is associated with longer productive life prior to cows being sent to slaughter with suspected paratuberculosis. J Dairy Sci 95: 618-629. http://dx.doi.org/10.3168/jds.2009-2860
  • Balseiro AM, 2004. Paratuberculosis bovina: valoración de las reacciones cruzadas con la prueba de la tuberculina, evaluación de técnicas diagnósticas y prevalencia en Asturias. Doctoral thesis. Univ. León, León, Spain.
  • Balseiro A, Prieto JM, Espí A, Perez V, García Marín JF, 2003. Presence of focal and multifocal paratuberculosis lesions in mesenteric lymph nodes and the ileocaecal valve of cattle positive to the tuberculin skin test. Vet J 166: 210-212. http://dx.doi.org/10.1016/S1090-0233(02)00312-X
  • Barry CE 3rd, Boshoff HI, Dartois V, Dick T, Ehrt S, Flynn J, Schnappinger D, Wilkinson RJ, Young D, 2009. The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nat Rev Microbiol 7: 845-855.
  • Bastida F, Juste RA, 2011. Paratuberculosis control: a review with a focus on vaccination. J Immune Based Ther Vaccines 9: 8. http://dx.doi.org/10.1186/1476-8518-9-8
  • Brooks-Pollock E, Conlan AJ, Mitchell AP, Blackwell R, McKinley TJ, Wood JL, 2013. Age-dependent patterns of bovine tuberculosis in cattle. Vet Res 44: 97. http://dx.doi.org/10.1186/1297-9716-44-97
  • Cassidy JP, 2006. The pathogenesis and pathology of bovine tuberculosis with insights from studies of tuberculosis in humans and laboratory animal models. Vet Microbiol 112: 151-161. http://dx.doi.org/10.1016/j.vetmic.2005.11.031
  • Chiodini RJ, Van Kruiningen HJ, Merkal RS, 1984. Ruminant paratuberculosis (Johne's disease): the current status and future prospects. Cornell Vet 74: 218-262.
  • Chiodini RJ, Chamberlin WM, Sarosiek J, McCallum RW, 2012. Crohn's disease and the mycobacterioses: a quarter century later. Causation or simple association? Crit Rev Microbiol 38: 52-93. http://dx.doi.org/10.3109/1040841X.2011.638273
  • Collins MT, 2011. Food safety concerns regarding paratuberculosis. Vet Clin North Am Food Anim Pract 27: 631-636. http://dx.doi.org/10.1016/j.cvfa.2011.07.009
  • Corbett EL, Watt CJ, Walker N, Maher D, Williams BG, Raviglione MC, Dye C, 2003. The growing burden of tuberculosis: global trends and interactions with the HIV epidemic. Arch Intern Med 163: 1009-1021. http://dx.doi.org/10.1001/archinte.163.9.1009
  • Flynn JL, Chan J, 2001. Tuberculosis: latency and reactivation. Infect Immun 69: 4195-4201. http://dx.doi.org/10.1128/IAI.69.7.4195-4201.2001
  • González J, Geijo MV, García-Pariente C, Verna A, Corpa JM, Reyes LE, Ferreras MC, Juste RA, García Marín JF, Pérez V, 2005. Histopathological classification of lesions associated with natural paratuberculosis infection in cattle. J Comp Pathol 133: 184-196. http://dx.doi.org/10.1016/j.jcpa.2005.04.007
  • Groenendaal H, Nielen M, Jalvingh AW, Horst SH, Galligan DT, Hesselink JW, 2002. A simulation of Johne's disease control. Prev Vet Med 54: 225-245. http://dx.doi.org/10.1016/S0167-5877(02)00027-2
  • Jones GJ, Pirson C, Gideon HP, Wilkinson KA, Sherman DR, Wilkinson RJ, Hewinson RG, Vordermeier HM, 2011. Immune responses to the enduring hypoxic response antigen Rv0188 are preferentially detected in Mycobacterium bovis infected cattle with low pathology. PLoS One 6: e21371. http://dx.doi.org/10.1371/journal.pone.0021371
  • Jungersen G, Mikkelsen H, Grell SN, 2012. Use of the johnin PPD interferon-gamma assay in control of bovine paratuberculosis. Vet Immunol Immunopathol 148: 48-54. http://dx.doi.org/10.1016/j.vetimm.2011.05.010
  • Juste RA, Marco JC, Sáez de Ocáriz C, Adúriz JJ, 1991. Comparison of different media for the isolation of small ruminant strains of Mycobacterium paratuberculosis. Vet Microbiol 28: 385-390. http://dx.doi.org/10.1016/0378-1135(91)90073-O
  • Juste RA, Alonso-Hearn M, Molina E, Geijo M, Vazquez P, Sevilla IA, Garrido JM, 2009. Significant reduction in bacterial shedding and improvement in milk production in dairy farms after the use of a new inactivated paratuberculosis vaccine in a field trial. BMC Res Notes 2: 233. http://dx.doi.org/10.1186/1756-0500-2-233
  • Larsen AB, Merkal RS, Cutlip RC. 1975. Age of cattle as related to resistance to infection with Mycobacterium paratuberculosis. Am J Vet Res 36: 255-257.
  • Lombard JE, 2011. Epidemiology and economics of paratuberculosis. Vet Clin North Am Food Anim Pract 27: 525-535. http://dx.doi.org/10.1016/j.cvfa.2011.07.012
  • Magombedze G, Ngonghala CN, Lanzas C, 2013. Evaluation of the "Iceberg Phenomenon" in Johne's disease through mathematical modelling. PLoS One 8: e76636. http://dx.doi.org/10.1371/journal.pone.0076636
  • Mon ML, Viale M, Baschetti G, Alvarado Pinedo F, Gioffre A, Travería G, Willemsen P, Bakker D, Romano MI. 2012. Search for Mycobacterium avium subspecies paratuberculosis antigens for the diagnosis of paratuberculosis. Vet Med Int: 860362.
  • Moss MT, Sanderson JD, Tizard ML, Hermon-Taylor J, el-Zaatari FA, Markesich DC, Graham DY, 1992. Polymerase chain reaction detection of Mycobacterium paratuberculosis and Mycobacterium avium subsp silvaticum in long term cultures from Crohn's disease and control tissues. Gut 33: 1209-1213. http://dx.doi.org/10.1136/gut.33.9.1209
  • Nielsen SS, Ersbøll AK, 2006. Age at occurrence of Mycobacterium avium subspecies paratuberculosis in naturally infected dairy cows. J Dairy Sci 89: 4557-4566. http://dx.doi.org/10.3168/jds.S0022-0302(06)72505-X
  • Nielsen SS, Toft N, 2008. Ante mortem diagnosis of paratuberculosis: a review of accuracies of ELISA, interferon-gamma assay and faecal culture techniques. Vet Microbiol 129: 217-235. http://dx.doi.org/10.1016/j.vetmic.2007.12.011
  • Nielsen SS, Toft N, 2009. A review of prevalences of paratuberculosis in farmed animals in Europe. Prev Vet Med 88: 1-14. http://dx.doi.org/10.1016/j.prevetmed.2008.07.003
  • Nielsen SS, Toft N, Okura H, 2013. Dynamics of specific anti-Mycobacterium avium subsp. paratuberculosis antibody response through age. PLoS One 8: e63009. http://dx.doi.org/10.1371/journal.pone.0063009
  • Parikka M, Hammarén MM, Harjula SK, Halfpenny NJ, Oksanen KE, Lahtinen MJ, Pajula ET, Iivanainen A, Pesu M, Rämet M, 2012. Mycobacterium marinum causes a latent infection that can be reactivated by gamma irradiation in adult zebrafish. PLoS Pathog 8: e1002944. http://dx.doi.org/10.1371/journal.ppat.1002944
  • Pathak S, Awuh JA, Leversen NA, Flo TH, Asjø B, 2012. Counting mycobacteria in infected human cells and mouse tissue: a comparison between qPCR and CFU. PLoS One 7: e34931. http://dx.doi.org/10.1371/journal.pone.0034931
  • Perez V, Moreno O, Mu-oz M, Garcia-Pariente C, Benavides J, Delgado L, Gonzalez J, Luis M, Fuertes M, Garcia-Marin JF, Ferreras MC, 2009. Diagnosis of paratuberculosis in slaughtered calves in the Northwest of Castilla y León (Spain) by pathological methods. Proc 10th Int Coll on Paratuberculosis, Minneapolis (USA), Aug 9-14. p: 184.
  • Seiler P, Ulrichs T, Bandermann S, Pradl L, Jörg S, Krenn V, Morawietz L, Kaufmann SH, Aichele P, 2003. Cell-wall alterations as an attribute of Mycobacterium tuberculosis in latent infection. J Infect Dis 188: 1326-1331. http://dx.doi.org/10.1086/378563
  • Stamp JT, Watt JA, 1954. Johne's disease in sheep. J Comp Pathol 64: 26-40. http://dx.doi.org/10.1016/S0368-1742(54)80005-1
  • Sweeney RW, Whitlock RH, Hamir AN, Rosenberger AE, Herr SA, 1992. Isolation of Mycobacterium paratuberculosis after oral inoculation in uninfected cattle. Am J Vet Res 53: 1312-1314.
  • Sweeney RW, Uzonna J, Whitlock RH, Habecker PL, Chilton P, Scott P, 2006. Tissue predilection sites and effect of dose on Mycobacterium avium subs. paratuberculosis organism recovery in a short-term bovine experimental oral infection model. Res Vet Sci 80: 253-259. http://dx.doi.org/10.1016/j.rvsc.2005.07.007
  • Van Rhijn I, Godfroid J, Michel A, Rutten V, 2008. Bovine tuberculosis as a model for human tuberculosis: advantages over small animal models. Microbes Infect 10: 711-715. http://dx.doi.org/10.1016/j.micinf.2008.04.005
  • Vázquez P, Garrido JM, Juste RA, 2012. Effects on paratuberculosis on Friesian cattle carcass weight and age at culling. Span J Agric Res 10: 662-670. http://dx.doi.org/10.5424/sjar/2012103-2728
  • Vazquez P, Garrido JM, Juste RA, 2013. Specific antibody and interferon-gamma responses associated with immunopathological forms of bovine paratuberculosis in slaughtered Friesian cattle. PLoS One 8: e64568. http://dx.doi.org/10.1371/journal.pone.0064568
  • Whitlock RH, Wells SJ, Sweeney RW, Van Tiem J, 2000. ELISA and fecal culture for paratuberculosis (Johne's disease): sensitivity and specificity of each method. Vet Microbiol 77: 387-398. http://dx.doi.org/10.1016/S0378-1135(00)00324-2
  • Whittington R, 2010. Cultivation of Mycobacterium avium subsp. paratuberculosis. In: Paratuberculosis: organism, disease, control (Behr MA & Collins DM, eds.). CAB Int, Wallingford (UK), pp: 244-266. http://dx.doi.org/10.1079/9781845936136.0244
  • Windsor PA, Whittington RJ, 2010. Evidence for age susceptibility of cattle to Johne's disease. Vet J 184: 37-44. http://dx.doi.org/10.1016/j.tvjl.2009.01.007