Pre-infection of pigs with Mycoplasma hyopneumoniae induces oxidative stress that influences outcomes of a subsequent infection with a swine influenza virus of H1N1 subtype

Veterinary Microbiology

Volumn 162, Issue 2-4, 2013, Pages 643-651

  Deblanc, C ^a   Robert, F ^b   Pinard, T ^b   Gorin, S ^a   Queguiner S ^a   Gautier Bouchardon, A V ^a   Ferre S ^a   Garraud, J M ^b   Cariolet, R ^a   Brack, M ^c   Simon, G ^a  

^a FRENCH AGENCY FOR FOOD   (France)

^b Research and Development Service   (France)

^c Oxidative Stress College   (France)

Author keywords

Co infection; Mycoplasma hyopneumoniae; Oxidative stress; Pigs; Swine influenza virus

Indexed keywords

GLYCOPROTEIN E1; GLYCOPROTEIN E2;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATE; BLOOD SAMPLING; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; EUROPE; FEEDING; HYPERTHERMIA; INFLAMMATION; INFLUENZA A (H1N1); INFLUENZA VIRUS A H1N1; INOCULATION; MYCOPLASMA HYOPNEUMONIAE; MYCOPLASMAL PNEUMONIA OF SWINE; NONHUMAN; NOSE SMEAR; OXIDATIVE STRESS; SWINE; SYMPTOM; VIRUS SHEDDING; VIRUS STRAIN; WEIGHT GAIN;

ANIMALS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA, HUMAN; LUNG; MYCOPLASMA HYOPNEUMONIAE; ORTHOMYXOVIRIDAE INFECTIONS; OXIDATIVE STRESS; SUS SCROFA; SWINE; SWINE DISEASES; VIRUS SHEDDING;

ANIMALIA; AVES; MYCOPLASMA HYOPNEUMONIAE; ORTHOMYXOVIRIDAE; SUIDAE; SWINE INFLUENZA VIRUS;

EID: 84872489711     PISSN: 03781135     EISSN: 18732542     Source Type: Journal    
DOI: 10.1016/j.vetmic.2012.11.028     Document Type: Article

References (35)

1. Akcil E., Yavuz G., Kocak M. Effects of inflammation and antiinflammatory treatment on serum trace elements concentrations. Biol. Trace Elem. Res. 2003, 93:95-104.
2. Alava M.A., Gonzalezramon N., Heegaard P., Guzylack S., Toussaint M.J.M., Lipperheide C., Madec F., Gruys E., Eckersall P.D., Lampreave F., Pineiro A. Pig-MAP, porcine acute phase proteins and standardisation of assays in Europe. Comp. Haematol. Int. 1997, 7:208-213.
3. Avron A., Gallily R. Mycoplasma stimulates the production of oxidative radicals by murine peritoneal macrophages. J. Leukoc. Biol. 1995, 57:264-268.
4. Babior B.M. Oxidants from phagocytes: agents of defense and destruction. Blood 1984, 64:959-966.
5. Barbe F., Atanasova K., Van Reeth K. Cytokines and acute phase proteins associated with acute swine influenza infection in pigs. Vet. J. 2011, 187:48-53.
6. Buffinton G.D., Christen S., Peterhans E., Stocker R. Oxidative stress in lungs of mice infected with influenza A virus. Free Radic. Res. Commun. 1992, 16:99-110.
7. Cai J., Chen Y., Seth S., Furukawa S., Compans R.W., Jones D.P. Inhibition of influenza infection by glutathione. Free Radic. Biol. Med. 2003, 34:928-936.
8. Cornelli U., Terranova R., Luca S., Cornelli M., Alberti A. Bioavailability and antioxidant activity of some food supplements in men and women using the D-Roms test as a marker of oxidative stress. J. Nutr. 2001, 131:3208-3211.
9. de la Villehuchet A.M., Brack M., Dreyfus G., Oussar Y., Bonnefont-Rousselot D., Chapman M.J., Kontush A. A machine-learning approach to the prediction of oxidative stress in chronic inflammatory disease. Redox Rep. 2009, 14:23-33.
10. Deblanc C., Gorin S., Quéguiner S., Gautier-Bouchardon A.V., Ferré S., Amenna N., Cariolet R., Simon G. Pre-infection of pigs with Mycoplasma hyopneumoniae modifies outcomes of infection with European swine influenza virus of H1N1, but not H1N2, subtype. Vet. Microbiol. 2012, 157:96-105.
11. Fablet C., Marois-Crehan C., Simon G., Grasland B., Jestin A., Kobisch M., Madec F., Rose N. Infectious agents associated with respiratory diseases in 125 farrow-to-finish pig herds: a cross-sectional study. Vet. Microbiol. 2012, 157:152-163.
12. Ghezzi P. Role of glutathione in immunity and inflammation in the lung. Int. J. Gen. Med. 2011, 4:105-113.
13. Ghezzi P., Ungheri D. Synergistic combination of N-acetylcysteine and ribavirin to protect from lethal influenza viral infection in a mouse model. Int. J. Immunopathol. Pharmacol. 2004, 17:99-102.
14. Hennet T., Peterhans E., Stocker R. Alterations in antioxidant defences in lung and liver of mice infected with influenza A virus. J. Gen. Virol. 1992, 73(Pt 1):39-46.
15. Hermeyer K., Jacobsen B., Spergser J., Rosengarten R., Hewicker-Trautwein M. Detection of Mycoplasma bovis by in-situ hybridization and expression of inducible nitric oxide synthase, nitrotyrosine and manganese superoxide dismutase in the lungs of experimentally-infected calves. J. Comp. Pathol. 2011, 145:240-250.
16. Huang Y., Zaas A.K., Rao A., Dobigeon N., Woolf P.J., Veldman T., Oien N.C., McClain M.T., Varkey J.B., Nicholson B., Carin L., Kingsmore S., Woods C.W., Ginsburg G.S., Hero A.O. Temporal dynamics of host molecular responses differentiate symptomatic and asymptomatic influenza A infection. PLoS Genet. 2011, 7:e1002234.
17. Kumar P., Sharma S., Khanna M., Raj H.G. Effect of quercetin on lipid peroxidation and changes in lung morphology in experimental influenza virus infection. Int. J. Exp. Pathol. 2003, 84:127-134.
18. Kuntz-Simon G., Kaiser C., Madec F. Swine influenza. Infectious and Parasitic Diseases of Livestock 2010, 273-285. Lavoisier, Paris. P.C. Lefevre, J. Blancou, D.W. Taylor (Eds.).
19. Kuntz-Simon G., Madec F. Genetic and antigenic evolution of swine influenza viruses in Europe and evaluation of their zoonotic potential. Zoonoses Public Health 2009, 56:310-325.
20. Lykkesfeldt J., Svendsen O. Oxidants and antioxidants in disease: oxidative stress in farm animals. Vet. J. 2007, 173:502-511.
21. Madec F., Kobisch M. Bilan lésionnel des poumons de porcs charcutiers à l'abattoir. Journées de la Recherche Porcine en France 1982, 1982:405-412.
22. Marco-Ramell A., Pato R., Pena R., Saco Y., Manteca X., Ruiz De La Torre J.L., Bassols A. Identification of serum stress biomarkers in pigs housed at different stocking densities. Vet. J. 2011, 190:e66-e71.
23. Marois C., Dory D., Fablet C., Madec F., Kobisch M. Development of a quantitative Real-Time TaqMan PCR assay for determination of the minimal dose of Mycoplasma hyopneumoniae strain 116 required to induce pneumonia in SPF pigs. J. Appl. Microbiol. 2010, 108:1523-1533.
24. 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.
25. Mayne S.T. Antioxidant nutrients and chronic disease: use of biomarkers of exposure and oxidative stress status in epidemiologic research. J. Nutr. 2003, 133:933S-940S.
26. Miller J.K., Brzezinska-Slebodzinska E., Madsen F.C. Oxidative stress, antioxidants, and animal function. J. Dairy Sci. 1993, 76:2812-2823.
27. OIE, 2008. Manual of Diagnostic Tests & Vaccines for Terrestrial Animals.
28. Peterhans E. Oxidants and antioxidants in viral diseases: disease mechanisms and metabolic regulation. J. Nutr. 1997, 127:962S-965S.
29. Pomorska-Mol M., Markowska-Daniel I., Pejsak Z. Acute phase protein response during subclinical infection of pigs with H1N1 swine influenza virus. Vet. Microbiol. 2012, 159:499-503.
30. Robert F., Bebin K., Garreau J., Gueriot J., Foret R., Brack M., Garrel C. Evaluation et correction du stress oxydatif du porcelet en post sevrage. Journées de la Recherche Porcine 2009, 173-178.
31. 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. Online 2003, 40:395-404.
32. Schafer E.R., Oneal M.J., Madsen M.L., Minion F.C. Global transcriptional analysis of Mycoplasma hyopneumoniae following exposure to hydrogen peroxide. Microbiology 2007, 153:3785-3790.
33. Schwarz K.B. Oxidative stress during viral infection: a review. Free Radic. Biol. Med. 1996, 21:641-649.
34. Sies H. Oxidative stress: from basic research to clinical application. Am. J. Med. 1991, 91:31S-38S.
35. Spackman E., Senne D.A., Myers T.J., Bulaga L.L., Garber L.P., Perdue M.L., Lohman K., Daum L.T., Suarez D.L. Development of a real-time reverse transcriptase PCR assay for type A influenza virus and the avian H5 and H7 hemagglutinin subtypes. J. Clin. Microbiol. 2002, 40:3256-3260.