Evaluation of clinical, histological and immunological changes and qPCR detection of Mycoplasma hyopneumoniae in tissues during the early stages of mycoplasmal pneumonia in pigs after experimental challenge with two field isolates

Veterinary Microbiology

Volumn 161, Issue 1-2, 2012, Pages 186-195

  Woolley, Lauren K ^a,b   Fell, Shayne ^a   Gonsalves, Jocelyn R ^a   Walker, Mark J ^c   Djordjevic, Steven P ^d   Jenkins, Cheryl ^a   Eamens, Graeme J ^a  

^a NSW DEPARTMENT OF PRIMARY INDUSTRIES   (Australia)

^b UNIVERSITY OF WOLLONGONG   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

Author keywords

Clinical; Cytokines; Histopathology; Mycoplasma hyopneumoniae; Mycoplasmal pneumonia; Quantitative polymerase chain reaction

Indexed keywords

BACTERIAL DNA; INTERLEUKIN 1BETA; INTERLEUKIN 6;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; BACTERIUM DETECTION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; COUGHING; CYTOKINE RESPONSE; DNA CONTENT; DNA DETERMINATION; EVALUATION; EXPERIMENTAL INFECTION; HISTOPATHOLOGY; KIDNEY; LIVER; MYCOPLASMA HYOPNEUMONIAE; MYCOPLASMA PNEUMONIA; NONHUMAN; PNEUMONIA; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; SLAUGHTERHOUSE; SPLEEN; SWINE; TRACHEOBRONCHIAL TOILET;

ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CYTOKINES; INTERLEUKIN-6; LUNG; MYCOPLASMA HYOPNEUMONIAE; PNEUMONIA OF SWINE, MYCOPLASMAL; POLYMERASE CHAIN REACTION; SWINE; TIME FACTORS;

MYCOPLASMA HYOPNEUMONIAE; SUIDAE;

EID: 84869868854     PISSN: 03781135     EISSN: 18732542     Source Type: Journal    
DOI: 10.1016/j.vetmic.2012.07.025     Document Type: Article

References (54)

1. Artiushin S., Minion F.C. Arbitrarily primed PCR analysis of Mycoplasma hyopneumoniae field isolates demonstrates genetic heterogeneity. Int. J. Syst. Bacteriol. 1996, 46:324-328.
2. Asai T., Okada M., Ono M., Irisawa T., Mori Y., Yokomizo Y., Sato S. Increased levels of tumor necrosis factor and interleukin 1 in bronchoalveolar lavage fluids from pigs infected with Mycoplasma hyopneumoniae. Vet. Immunol. Immunopathol. 1993, 38:253-260.
3. Asai T., Okada M., Ono M., Mori Y., Yokomizo Y., Sato S. Detection of interleukin-6 and prostaglandin E2 in bronchoalveolar lavage fluids of pigs experimentally infected with Mycoplasma hyopneumoniae. Vet. Immunol. Immunopathol. 1994, 44:97-102.
4. Bogema D.R., Scott N.E., Padula M.P., Tacchi J.L., Raymond B.B.A., Jenkins C., Cordwell S.J., Minion F.C., Walker M.J., Djordjevic S.P. Sequence TTKF down arrow QE defines the site of proteolytic cleavage in Mhp683 Protein, a novel glycosaminoglycan and cilium adhesin of Mycoplasma hyopneumoniae. J. Biol. Chem. 2011, 286:41217-41229.
5. Burnett T.A., Dinkla K., Rohde M., Chhatwal G.S., Uphoff C., Srivastava M., Cordwell S.J., Geary S., Liao X., Minion F.C., Walker M.J., Djordjevic S.P. P159 is a proteolytically processed, surface adhesin of Mycoplasma hyopneumoniae: defined domains of P159 bind heparin and promote adherence to eukaryote cells. Mol. Microbiol. 2006, 60:669-686.
6. Choi C., Kwon D., Jung K., Ha Y., Lee Y.H., Kim O., Park H.K., Kim S.H., Hwang K.K., Chae C. Expression of inflammatory cytokines in pigs experimentally infected with Mycoplasma hyopneumoniae. J. Comp. Pathol. 2006, 134:40-46.
7. DeBey M.C., Ross R.F. Ciliostasis and loss of cilia induced by Mycoplasma hyopneumoniae in porcine tracheal organ cultures. Infect. Immun. 1994, 62. 5312-5318; 5333 ref.
8. Deutscher A.T., Jenkins C., Minion F.C., Seymour L.M., Padula M.P., Dixon N.E., Walker M.J., Djordjevic S.P. Repeat regions R1 and R2 in the P97 paralogue Mhp271 of Mycoplasma hyopneumoniae bind heparin, fibronectin and porcine cilia. Mol. Microbiol. 2010, 78:444-458.
9. Dinarello C.A. Role of interleukin-1 in infectious disease. Immunol. Rev. 1992, 127:119-146.
10. Djordjevic S.P., Cordwell S.J., Djordjevic M.A., Wilton J., Minion F.C. Proteolytic processing of the Mycoplasma hyopneumoniae cilium adhesin. Infect. Immun. 2004, 72:2791-2802.
11. Etheridge J.R., Cottew G.S., Lloyd L.C. Isolation of Mycoplasma hyopneumoniae from lesions in experimentally infected pigs. Aust. Vet. J. 1979, 55:356-359.
12. Freundt E.A., Erno H. Identification of mycoplasmas. Methods in Microbiology 1979, vol. 13:407. Academic Press, London.
13. Frey J., Haldimann A., Nicolet J. Chromosomal heterogeneity of various Mycoplasma hyopneumoniae field strains. Int. J. Syst. Bacteriol. 1992, 42. 275-280; 232 ref.
14. Goodwin R.F.W., Hodgson R.G., Whittlestone P., Woodhams R.L. Some experiments relating to artificial immunity in enzootic pneumonia of pigs. J. Hyg. Cambr. 1969, 67:465-476.
15. Hsu T., Minion F.C. Identification of the cilium binding epitope of the Mycoplasma hyopneumoniae P97 adhesin. Infect. Immun. 1998, 66:4762-4766.
16. Hsu T., Artiushin S., Minion F.C. Cloning and functional analysis of the P97 swine cilium adhesin gene of Mycoplasma hyopneumoniae. J. Bacteriol. 1997, 179:1317-1323. 1336 ref.
17. Irigoyen L.F., Alstine W., Turek v., Clark J., van Alstine L.K.W. Ultrastructural observation of the airways of recovered and susceptible pigs after inoculation with Mycoplasma hyopneumoniae. Pesq. Vet. Bras. 1998, 18:1-7.
18. Jenkins C., Wilton J.L., Minion F.C., Falconer L., Walker M.J., Djordjevic S.P. Two domains within the Mycoplasma hyopneumoniae cilium adhesin bind heparin. Infect. Immun. 2006, 74:481-487.
19. Kwon D., Choi C., Chae C. Chronologic localization of Mycoplasma hyopneumoniae in experimentally infected pigs. Vet. Pathol. 2002, 39:584-587.
20. Le Carrou J., Laurentie M., Kobisch M., Gautier-Bouchardon A.V. Persistence of Mycoplasma hyopneumoniae in experimentally infected pigs after marbofloxacin treatment and detection of mutations in the parC gene. Antimicrob. Agents Chemother. 2006, 50:1959-1966.
21. Livingston C.W., Stair E.L., Underdahl N.R., Mebus C.A. Pathogenesis of mycoplasmal pneumonia in swine. Am. J. Vet. Res. 1972, 33:2249-2258.
22. Lorenzo H., Quesada ó., Assunçao P., Castro A., Rodríguez F. Cytokine expression in porcine lungs experimentally infected with Mycoplasma hyopneumoniae. Vet. Immunol. Immunopathol. 2006, 109:199-207.
23. Maes D., Verdonck M., Deluyker H., Kruif A., De Kruif d.A. Enzootic pneumonia in pigs. Vet. Q. 1996, 18:104-109.
24. Maes D., Segales J., Meyns T., Sibila M., Pieters M., Haesebrouck F. Control of Mycoplasma hyopneumoniae infections in pigs. Vet. Microbiol. 2008, 126:297-309.
25. Marois C., Le Carrou J., Kobisch M., Gautier-Bouchardon A.V. Isolation of Mycoplasma hyopneumoniae from different sampling sites in experimentally infected and contact SPF piglets. Vet. Microbiol. 2007, 120:96-104.
26. Messier S., Ross R.F., Paul P.S. Humoral and cellular immune responses of pigs inoculated with Mycoplasma hyopneumoniae. Am. J. Vet. Res. 1990, 51:52-58.
27. Meyns T., Maes D., Dewulf J., Vicca J., Haesebrouck F., de Kruif A. Quantification of the spread of Mycoplasma hyopneumoniae in nursery pigs using transmission experiments. Prev. Vet. Med. 2004, 66:265-275.
28. Meyns T., Maes D., Calus D., Ribbens S., Dewulf J., Chiers K., de Kruif A., Cox E., Decostere A., Haesebrouck F. Interactions of highly and low virulent Mycoplasma hyopneumoniae isolates with the respiratory tract of pigs. Vet. Microbiol. 2007, 120:87-95.
29. Minion F.C., Adams C., Hsu T., Hsu T.D. R1 region of P97 mediates adherence of Mycoplasma hyopneumoniae to swine cilia. Infect. Immun. 2000, 68:3056-3060.
30. Minion F.C., Lefkowitz E.J., Madsen M.L., Cleary B.J., Swartzell S.M., Mahairas G.G. The genome sequence of Mycoplasma hyopneumoniae strain 232, the agent of swine mycoplasmosis. J. Bacteriol. 2004, 186:7123-7133.
31. Mouton W.G., Pfitzner J., Bessell J.R., Maddern G.J. Bronchial anatomy and single-lung ventilation in the pig. Can. J. Anaesth. 1999, 46:701-703.
32. Pinto P.M., Klein C.S., Zaha A., Ferreira H.B. Comparative proteomic analysis of pathogenic and non-pathogenic strains from the swine pathogen Mycoplasma hyopneumoniae. Proteome Sci. 2009, 7.
33. Ro L.H., Ross R.F. Comparison of Mycoplasma hyopneumoniae strains by serologic methods. Am. J. Vet. Res. 1983, 44:2087-2094. 2034 ref.
34. Rodriguez F., Ramirez G.A., Sarradell J., Andrada M., Lorenzo H. Immunohistochemical labelling of cytokines in lung lesions of pigs naturally infected with Mycoplasma hyopneumoniae. J. Comp. Pathol. 2004, 130:306-312.
35. Sarradell J., Andrada M., Ramirez A.S., Fernandez A., Gomez-Villamandos J.C., Jover A., Lorenzo H., Herraez P., Rodriguez F. A morphologic and immunohistochemical study of the bronchus-associated lymphoid tissue of pigs naturally infected with Mycoplasma hyopneumoniae. Vet. Pathol. 2003, 40:395-404.
36. Scarman A.L., Chin J.C., Eamens G.J., Delaney S.F., Djordjevic S.P. Identification of novel species-specific antigens of Mycoplasma hyopneumoniae by preparative SDS-PAGE ELISA profiling. Microbiology (Reading) 1997, 143:663-673.
37. Seymour L.M., Falconer L., Deutscher A.T., Minion F.C., Padula M.P., Dixon N.E., Djordjevic S.P., Walker M.J. Mhp107 is a member of the multifunctional adhesin family of Mycoplasma hyopneumoniae. J. Biol. Chem. 2011, 286:10097-10104.
38. Sorensen V., Ahrens P., Barfod K., Feenstra A.A., Feld N.C., Friis N.F., Bille Hansen V., Jensen N.E., Pedersen M.W. Mycoplasma hyopneumoniae infection in pigs: duration of the disease and evaluation of four diagnostic assays. Vet. Microbiol. 1997, 54:23-34.
39. Stakenborg T., Vicca J., Butaye P., Maes D., Peeters J., de Kruif A., Haesebrouck F. The diversity of Mycoplasma hyopneumoniae within and between herds using pulsed-field gel electrophoresis. Vet. Microbiol. 2005, 109:29-36.
40. Stakenborg T., Vicca J., Maes D., Peeters J., de Kruif A., Haesebrouck F., Butaye P. Comparison of molecular techniques for the typing of Mycoplasma hyopneumoniae isolates. J. Microbiol. Methods 2006, 66:263-275.
41. Strait E.L., Madsen M.L., Minion F.C., Christopher-Hennings J., Dammen M., Jones K.R., Thacker E.L. Real-time PCR assays to address genetic diversity among strains of Mycoplasma hyopneumoniae. J. Clin. Microbiol. 2008, 46:2491-2498.
42. Taylor J.D. Ch 14: the lungs. Pathology of the Pig: A Diagnostic Guide 1996, 233-234. The Pig Research and Development Corporation, Barton, A.C.T, Australia. L.D. Sims, J.R.W. Glastonbury (Eds.).
43. Thacker E.L. Chapter 42: mycoplasmal diseases. Diseases of Swine 2006, 701-717. Blackwell Publishing, Oxford, UK. B.E. Straw, J.J. Zimmerman, S. D'Allaire, D. Taylor (Eds.).
44. Vasconcelos A.T., Ferreira H.B., Bizarro C.V., Bonatto S.L., Carvalho M.O., Pinto P.M., Almeida D.F., Almeida L.G., Almeida R., Alves-Filho L., Assunção E.N., Azevedo V.A., Bogo M.R., Brigido M.M., Brocchi M., Burity H.A., Camargo A.A., Camargo S.S., Carepo M.S., Carraro D.M., de Mattos Cascardo J.C., Castro L.A., Cavalcanti G., Chemale G., Collevatti R.G., Cunha C.W., Dallagiovanna B., Dambrós B.P., Dellagostin O.A., Falcão C., Fantinatti-Garboggini F., Felipe M.S., Fiorentin L., Franco G.R., Freitas N.S., Frías D., Grangeiro T.B., Grisard E.C., Guimarães C.T., Hungria M., Jardim S.N., Krieger M.A., Laurino J.P., Lima L.F., Lopes M.I., Loreto E.L., Madeira H.M., Manfio G.P., Maranhão A.Q., Martinkovics C.T., Medeiros S.R., Moreira M.A., Neiva M., Ramalho-Neto C.E., Nicolás M.F., Oliveira S.C., Paixão R.F., Pedrosa F.O., Pena S.D., Pereira M., Pereira-Ferrari L., Piffer I., Pinto L.S., Potrich D.P., Salim A.C., Santos F.R., Schmitt R., Schneider M.P., Schrank A., Schrank I.S., Schuck A.F., Seuanez H.N., Silva D.W., Silva R., Silva S.C., Soares C.M., Souza K.R., Souza R.C., Staats C.C., Steffens M.B., Teixeira S.M., Urmenyi T.P., Vainstein M.H., Zuccherato L.W., Simpson A.J., Zaha A. Swine and poultry pathogens: the complete genome sequences of two strains of Mycoplasma hyopneumoniae and a strain of Mycoplasma synoviae. J. Bacteriol. 2005, 187:5568-5577.
45. Vicca J., Stakenborg T., Maes D., Butaye P., Peeters J., de Kruif A., Haesebrouck F. Evaluation of virulence of Mycoplasma hyopneumoniae field isolates. Vet. Microbiol. 2003, 97:177-190.
46. Villarreal I., Maes D., Meyns T., Gebruers F., Calus D., Pasmans F., Haesebrouck F. Infection with a low virulent Mycoplasma hyopneumoniae isolate does not protect piglets against subsequent infection with a highly virulent M. hyopneumoniae isolate. Vaccine 2009, 27:1875-1879.
47. Villarreal I., Maes D., Vranckx K., Calus D., Pasmans F., Haesebrouck F. Effect of vaccination of pigs against experimental infection with high and low virulence Mycoplasma hyopneumoniae strains. Vaccine 2011, 29:1731-1735.
48. Vranckx K., Maes D., Marchioro S.B., Villarreal I., Chiers K., Pasmans F., Haesebrouck F. Vaccination reduces macrophage infiltration in bronchus-associated lymphoid tissue in pigs infected with a highly virulent Mycoplasma hyopneumoniae strain - art. no 24. BMC Vet. Res. 2012, 8:12.
49. Whittlestone P. Porcine mycoplasmas. The Mycoplasmas II. Human and Animal Mycoplasmas 1979, 133-176. Academic Press, New York. J.G. Tully, R.F. Whitcomb (Eds.).
50. Wilton J.L., Scarman A.L., Walker M.J., Djordjevic S.P. Reiterated repeat region variability in the ciliary adhesin gene of Mycoplasma hyopneumoniae. Microbiology (Reading) 1998, 144:1931-1943.
51. Wilton J., Jenkins C., Cordwell S.J., Falconer L., Minion F.C., Oneal D.C., Djordjevic M.A., Connolly A., Barchia I., Walker M.J., Djordjevic S.P. Mhp493 (P216) is a proteolytically processed, cilium and heparin binding protein of Mycoplasma hyopneumoniae. Mol. Microbiol. 2009, 71:566-582.
52. Zhang Q., Young T.F., Ross R.F., Zhang Q.J. Identification and characterization of a Mycoplasma hyopneumoniae adhesin. Infect. Immun. 1995, 63:1013-1019. 1040 ref.
53. Zielinski G.C., Ross R.F. Effect of growth in cell cultures and strain on virulence of Mycoplasma hyopneumoniae for swine. Am. J. Vet. Res. 1990, 51:344-348.
54. Zoja C., Wang J.M., Bettoni S., Sironi M., Renzi D., Chiaffarino F., Abboud H.E., Vandamme J., Mantovani A., Remuzzi G., Rambaldi A. Interleukin-1 beta and tumor necrosis factor-alpha induce gene expression and production of leukocyte chemotactic factors, colony-stimulating factors, and interleukin-6 in human mesangial cells. Am. J. Pathol. 1991, 138:991-1003.