1887

Abstract

The severity of respiratory syncytial virus (RSV) infections appears to differ with age in both humans and bovines. A primary RSV infection in naïve infants and in young calves runs a more severe course when they are 1–6 months old than in their first month of life. The relative lack of clinical signs in the first month of age may be due to high levels of maternally derived neutralizing antibodies or low exposure to infectious virus. This study examined whether age-dependent differences in the pathogenesis of bovine RSV (bRSV) between neonatal and young calves may be due to differences in age-dependent immunocompetence. To study the effect of age and immune parameters on bRSV disease in neonatal and young calves, neonatal (1-day-old) calves without maternally derived antibodies were infected experimentally with bRSV and the severity of disease and immune responses were evaluated in comparison with disease in similar 6-week-old infected calves. Neonatal calves had more extensive virus replication and lung consolidation, but lower pro-inflammatory [in particular tumour necrosis factor alpha (TNF-)] responses, specific humoral immune responses, lung neutrophilic infiltration and clinical signs of disease than 6-week-old calves. The lack of correlation between virus replication and clinical signs suggests an important role of pro-inflammatory cytokines, in particular TNF-, in the disease. The capacity to produce pro-inflammatory TNF- appeared to increase with age, and may explain the age-dependent differences in RSV pathogenesis.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.020842-0
2010-10-01
2019-11-17
Loading full text...

Full text loading...

/deliver/fulltext/jgv/91/10/2497.html?itemId=/content/journal/jgv/10.1099/vir.0.020842-0&mimeType=html&fmt=ahah

References

  1. Angen, O., Thomsen, J., Larsen, L. E., Larsen, J., Kokotovic, B., Heegaard, P. M. & Enemark, J. M. ( 2009; ). Respiratory disease in calves: microbiological investigations on trans-tracheally aspirated bronchoalveolar fluid and acute phase protein response. Vet Microbiol 137, 165–171.[CrossRef]
    [Google Scholar]
  2. Antonis, A. F., Schrijver, R. S., Daus, F., Steverink, P. J., Stockhofe, N., Hensen, E. J., Langedijk, J. P. & van der Most, R. G. ( 2003; ). Vaccine-induced immunopathology during bovine respiratory syncytial virus infection: exploring the parameters of pathogenesis. J Virol 77, 12067–12073.[CrossRef]
    [Google Scholar]
  3. Babiuk, L. A., Lawman, M. J. & Ohmann, H. B. ( 1988; ). Viral–bacterial synergistic interaction in respiratory disease. Adv Virus Res 35, 219–249.
    [Google Scholar]
  4. Baker, J. C., Ames, T. R. & Markham, R. J. ( 1986; ). Seroepizootiologic study of bovine respiratory syncytial virus in a dairy herd. Am J Vet Res 47, 240–245.
    [Google Scholar]
  5. Becnel, D., You, D., Erskin, J., Dimina, D. M. & Cormier, S. A. ( 2005; ). A role for airway remodeling during respiratory syncytial virus infection. Respir Res 6, 122.[CrossRef]
    [Google Scholar]
  6. Bryson, D. G., McFerran, J. B., Ball, H. J. & Neill, S. D. ( 1978; ). Observations on outbreaks of respiratory disease in housed calves – (2) pathological and microbiological findings. Vet Rec 103, 503–509.[CrossRef]
    [Google Scholar]
  7. Chase, C. C., Hurley, D. J. & Reber, A. J. ( 2008; ). Neonatal immune development in the calf and its impact on vaccine response. Vet Clin North Am Food Anim Pract 24, 87–104.[CrossRef]
    [Google Scholar]
  8. Coghe, J., Uystepruyst, C. H., Bureau, F., Detilleux, J., Art, T. & Lekeux, P. ( 2000; ). Validation and prognostic value of plasma lactate measurement in bovine respiratory disease. Vet J 160, 139–146.[CrossRef]
    [Google Scholar]
  9. Coomber, B. L., Nyarko, K. A., Noyes, T. M. & Gentry, P. A. ( 2001; ). Neutrophil–platelet interactions and their relevance to bovine respiratory disease. Vet J 161, 41–62.[CrossRef]
    [Google Scholar]
  10. Decleva, E., Dri, P., Menegazzi, R., Busetto, S. & Cramer, R. ( 2002; ). Evidence that TNF-induced respiratory burst of adherent PMN is mediated by integrin α L β 2. J Leukoc Biol 72, 718–726.
    [Google Scholar]
  11. Delespesse, G., Yang, L. P., Ohshima, Y., Demeure, C., Shu, U., Byun, D. G. & Sarfati, M. ( 1998; ). Maturation of human neonatal CD4+ and CD8+ T lymphocytes into Th1/Th2 effectors. Vaccine 16, 1415–1419.[CrossRef]
    [Google Scholar]
  12. Fogarty, U., Quinn, P. J. & Hannan, J. ( 1983; ). Bronchopulmonary lavage in the calf: a new technique. Ir Vet J 37, 35–38.
    [Google Scholar]
  13. Haslett, C. ( 1999; ). Granulocyte apoptosis and its role in the resolution and control of lung inflammation. Am J Respir Crit Care Med 160, S5–S11.[CrossRef]
    [Google Scholar]
  14. Heegaard, P. M., Godson, D. L., Toussaint, M. J., Tjørnehøj, K., Larsen, L. E., Viuff, B. & Ronsholt, L. ( 2000; ). The acute phase response of haptoglobin and serum amyloid A (SAA) in cattle undergoing experimental infection with bovine respiratory syncytial virus. Vet Immunol Immunopathol 77, 151–159.[CrossRef]
    [Google Scholar]
  15. Janssen, R., Bont, L., Siezen, C. L., Hodemaekers, H. M., Ermers, M. J., Doornbos, G., van 't Slot, R., Wijmenga, C., Goeman, J. J. & other authors ( 2007; ). Genetic susceptibility to respiratory syncytial virus bronchiolitis is predominantly associated with innate immune genes. J Infect Dis 196, 826–834.[CrossRef]
    [Google Scholar]
  16. Kampen, A. H., Olsen, I., Tollersrud, T., Storset, A. K. & Lund, A. ( 2006; ). Lymphocyte subpopulations and neutrophil function in calves during the first 6 months of life. Vet Immunol Immunopathol 113, 53–63.[CrossRef]
    [Google Scholar]
  17. Kimman, T. G., Zimmer, G. M., Westenbrink, F., Mars, J. & van Leeuwen, E. ( 1988; ). Epidemiological study of bovine respiratory syncytial virus infections in calves: influence of maternal antibodies on the outcome of disease. Vet Rec 123, 104–109.[CrossRef]
    [Google Scholar]
  18. Langedijk, J. P., Middel, W. G., Schaaper, W. M., Meloen, R. H., Kramps, J. A., Brandenburg, A. H. & van Oirschot, J. T. ( 1996; ). Type-specific serologic diagnosis of respiratory syncytial virus infection, based on a synthetic peptide of the attachment protein G. J Immunol Methods 193, 157–166.[CrossRef]
    [Google Scholar]
  19. Lukens, M. V., van de Pol, A. C., Coenjaerts, F. E., Jansen, N. J., Kamp, V. M., Kimpen, J. L., Rossen, J. W., Ulfman, L. H., Tacke, C. E. & other authors ( 2010; ). A systemic neutrophil response precedes robust CD8+ T-cell activation during natural respiratory syncytial virus infection in infants. J Virol 84, 2374–2383.[CrossRef]
    [Google Scholar]
  20. Mallard, B. A., Dekkers, J. C., Ireland, M. J., Leslie, K. E., Sharif, S., Vankampen, C. L., Wagter, L. & Wilkie, B. N. ( 1998; ). Alteration in immune responsiveness during the peripartum period and its ramification on dairy cow and calf health. J Dairy Sci 81, 585–595.[CrossRef]
    [Google Scholar]
  21. McNamara, P. S., Flanagan, B. F., Selby, A. M., Hart, C. A. & Smyth, R. L. ( 2004; ). Pro- and anti-inflammatory responses in respiratory syncytial virus bronchiolitis. Eur Respir J 23, 106–112.[CrossRef]
    [Google Scholar]
  22. Menge, C., Neufeld, B., Hirt, W., Schmeer, N., Bauerfeind, R., Baljer, G. & Wieler, L. H. ( 1998; ). Compensation of preliminary blood phagocyte immaturity in the newborn calf. Vet Immunol Immunopathol 62, 309–321.[CrossRef]
    [Google Scholar]
  23. Morrison, P. T., Thomas, L. H., Sharland, M. & Friedland, J. S. ( 2007; ). RSV-infected airway epithelial cells cause biphasic up-regulation of CCR1 expression on human monocytes. J Leukoc Biol 81, 1487–1495.[CrossRef]
    [Google Scholar]
  24. Neuzil, K. M., Tang, Y. W. & Graham, B. S. ( 1996; ). Protective role of TNF-α in respiratory syncytial virus infection in vitro and in vivo. Am J Med Sci 311, 201–204.[CrossRef]
    [Google Scholar]
  25. Rontved, C. M., Tjørnehøj, K., Viuff, B., Larsen, L. E., Godson, D. L., Ronsholt, L. & Alexandersen, S. ( 2000; ). Increased pulmonary secretion of tumor necrosis factor-α in calves experimentally infected with bovine respiratory syncytial virus. Vet Immunol Immunopathol 76, 199–214.[CrossRef]
    [Google Scholar]
  26. Rutigliano, J. A. & Graham, B. S. ( 2004; ). Prolonged production of TNF-α exacerbates illness during respiratory syncytial virus infection. J Immunol 173, 3408–3417.[CrossRef]
    [Google Scholar]
  27. Siegrist, C. A. ( 2001; ). Neonatal and early life vaccinology. Vaccine 19, 3331–3346.[CrossRef]
    [Google Scholar]
  28. Slocombe, R. F., Malark, J., Ingersoll, R., Derksen, F. J. & Robinson, N. E. ( 1985; ). Importance of neutrophils in the pathogenesis of acute pneumonic pasteurellosis in calves. Am J Vet Res 46, 2253–2258.
    [Google Scholar]
  29. Snowder, G. D., Van Vleck, L. D., Cundiff, L. V. & Bennett, G. L. ( 2006; ). Bovine respiratory disease in feedlot cattle: environmental, genetic, and economic factors. J Anim Sci 84, 1999–2008.[CrossRef]
    [Google Scholar]
  30. Soethout, E. C., Antonis, A. F., Ulfman, L. H., Hoek, A., van der Most, R. G., Muller, K. E. & Rutten, V. P. ( 2004; ). Bovine respiratory syncytial virus infection influences the impact of α 4- and β 2-integrin-mediated adhesion of peripheral blood neutrophils. Clin Exp Immunol 138, 388–395.[CrossRef]
    [Google Scholar]
  31. Tjørnehøj, K., Uttenthal, A., Viuff, B., Larsen, L. E., Rontved, C. & Ronsholt, L. ( 2003; ). An experimental infection model for reproduction of calf pneumonia with bovine respiratory syncytial virus (BRSV) based on one combined exposure of calves. Res Vet Sci 74, 55–65.[CrossRef]
    [Google Scholar]
  32. Tregoning, J. S., Yamaguchi, Y., Harker, J., Wang, B. & Openshaw, P. J. ( 2008; ). The role of T cells in the enhancement of respiratory syncytial virus infection severity during adult reinfection of neonatally sensitized mice. J Virol 82, 4115–4124.[CrossRef]
    [Google Scholar]
  33. Van der Poel, W. H., Brand, A., Kramps, J. A. & Van Oirschot, J. T. ( 1994; ). Respiratory syncytial virus infections in human beings and in cattle. J Infect 29, 215–228.[CrossRef]
    [Google Scholar]
  34. van der Poel, W. H., Schrijver, R. S., Middel, W. G., Kramps, J. A., Brand, A. & Van Oirschot, J. T. ( 1996; ). Experimental reproduction of respiratory disease in calves with non-cell-culture-passaged bovine respiratory syncytial virus. Vet Q 18, 81–86.[CrossRef]
    [Google Scholar]
  35. Varga, J., Szenci, O., Dufrasne, I., Borzsonyi, L. & Lekeux, P. ( 1998; ). Respiratory mechanical function in newborn calves immediately postpartum. Vet J 156, 73–75.[CrossRef]
    [Google Scholar]
  36. Verhoeff, J., Van der Ban, M. & van Nieuwstadt, A. P. ( 1984; ). Bovine respiratory syncytial virus infections in young dairy cattle: clinical and haematological findings. Vet Rec 114, 9–12.[CrossRef]
    [Google Scholar]
  37. Viuff, B., Tjørnehøj, K., Larsen, L. E., Rontved, C. M., Uttenthal, A., Ronsholt, L. & Alexandersen, S. ( 2002; ). Replication and clearance of respiratory syncytial virus: apoptosis is an important pathway of virus clearance after experimental infection with bovine respiratory syncytial virus. Am J Pathol 161, 2195–2207.[CrossRef]
    [Google Scholar]
  38. You, D., Becnel, D., Wang, K., Ripple, M., Daly, M. & Cormier, S. A. ( 2006; ). Exposure of neonates to respiratory syncytial virus is critical in determining subsequent airway response in adults. Respir Res 7, 107.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.020842-0
Loading
/content/journal/jgv/10.1099/vir.0.020842-0
Loading

Data & Media loading...

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error