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Acute and long-term effects of infection by the respiratory syncytial virus in children with congenital cardiac malformations

Published online by Cambridge University Press:  03 May 2005

Timothy F. Feltes
Affiliation:
Section of Pediatric Cardiology, Ohio State University and The Heart Center at Children's Hospital, Columbus, Ohio, United States of America
Jessie R. Groothuis
Affiliation:
Hollis-Eden Pharmaceuticals, Inc., San Diego, California, United States of America

Abstract

All newborn infants have limited pulmonary reserve compared with older children. This puts them at increased risk of respiratory complications, such as those associated with infection by the respiratory syncytial virus. Young children with congenital cardiac disease are particularly likely to suffer severe disease related to infection by the virus. In these children, the extreme vulnerability of the lung to pulmonary oedema is compounded by the additional burden caused by the respiratory syncytial virus.

In addition to the well-documented acute pulmonary effects of infection with the respiratory syncytial virus, there may also be consequent long-term respiratory morbidity. Clinical studies have shown that infection by the virus in infancy is associated with a higher risk of developing subsequent bronchial obstructive disease. Much debate surrounds the mechanisms underlying this association. It is thought that a combined immunological and neurogenic response mechanism is likely. Prevention of severe respiratory disease in infants and young children with congenital heart disease due to infection by the virus may, therefore, offer both immediate and long-term benefits. Indeed, an increasing body of evidence supports this hypothesis, indicating a clinical rationale for prophylaxis against the virus in infancy, in order to reduce the chance of developing reactive airways disease and asthma in later life.

Type
Original Article
Copyright
© 2005 Cambridge University Press

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References

Navas L, Wang E, de Carvalho V, Robinson J. Improved outcome of respiratory syncytial virus infection in a high-risk hospitalized population of Canadian children. Pediatric Investigators Collaborative Network on Infections in Canada. J Pediatr 1992; 121: 348354.Google Scholar
Boyce TG, Mellen BG, Mitchel EF Jr, Wright PF, Griffin MR. Rates of hospitalization for respiratory syncytial virus infection among children in Medicaid. J Pediatr 2000; 137: 865870.Google Scholar
Simoes EA. Immunoprophylaxis of respiratory syncytial virus: global experience. Respir Res 2002; 3 (Suppl 1): S26S33.Google Scholar
Khongphatthanayothin A, Wong PC, Samara Y, et al. Impact of respiratory syncytial virus infection on surgery for congenital heart disease: postoperative course and outcome. Crit Care Med 1999; 27: 19741981.Google Scholar
Inselman LS, Mellins RB. Growth and development of the lung. J Pediatr 1981; 98: 115.Google Scholar
Langston C. Normal and abnormal structural development of the human lung. Prog Clin Biol Res 1983; 140: 7591.Google Scholar
Langston C, Kida K, Reed M, Thurlbeck WM. Human lung growth in late gestation and in the neonate. Am Rev Respir Dis 1984; 129: 607613.Google Scholar
Hansen T, Corbet A. Pulmonary physiology of the newborn. In: Taeusch HW, Ballard RA (eds). Avery's Diseases of the Newborn. Elsevier Saunders, Philadelphia, 2005, pp 634647.
Johnson RJ, Haworth SG. Pulmonary vascular and alveolar development in tetralogy of Fallot: a recommendation for early correction. Thorax 1982; 37: 893901.Google Scholar
Guyton AC, Lindsey AW. Effect of elevated left atrial pressure and decreased plasma protein concentration on the development of pulmonary edema. Circ Res 1959; 7: 649657.Google Scholar
Feltes TF, Hansen TN. Effects of an aorticopulmonary shunt on lung fluid balance in the young lamb. Pediatr Res 1989; 26: 9497.Google Scholar
West JB, Mathieu-Costello O. Structure, strength, failure and remodeling of the pulmonary blood-gas barrier. Annu Rev Physiol 1999; 61: 543572.Google Scholar
Miserocchi G, Negrini D, Passi A, De Luca G. Development of lung edema: interstitial fluid dynamics and molecular structure. News Physiol Sci 2001; 16: 6671.Google Scholar
Drake RE, Doursout MF. Pulmonary edema and elevated left atrial pressure: four hours and beyond. News Physiol Sci 2002; 17: 223226.Google Scholar
West JB. Invited review: pulmonary capillary stress failure. J Appl Physiol 2000; 89: 24832489.Google Scholar
Fu Z, Heldt GP, West JB. Increased fragility of pulmonary capillaries in newborn rabbit. Am J Physiol Lung Cell Mol Physiol 2003; 284: L703L709.Google Scholar
Kingsbury MP, Huang W, Donnelly JL, et al. Structural remodelling of lungs in chronic heart failure. Basic Res Cardiol 2003; 98: 295303.Google Scholar
Patterson CE, Lum H. Update on pulmonary edema: the role and regulation of endothelial barrier function. Endothelium 2001; 8: 75105.Google Scholar
Gorenflo M, Gross P, Bodey A, et al. Plasma endothelin-1 in patients with left-to-right shunt. Am Heart J 1995; 130: 537542.Google Scholar
Schneeberger EE, McCarthy KM. Cytochemical localization of Na+-K+-ATPase in rat type II pneumocytes. J Appl Physiol 1986; 60: 15841589.Google Scholar
Matthay MA, Folkesson HG, Clerici C. Lung epithelial fluid transport and the resolution of pulmonary edema. Physiol Rev 2002; 82: 569600.Google Scholar
Guazzi M, Agostoni P, Guazzi MD. Modulation of alveolar-capillary sodium handling as a mechanism of protection of gas transfer by enalapril, and not by losartan in chronic heart failure. J Am Coll Cardiol 2001; 37: 398406.Google Scholar
Drake R, Giesler M, Laine G, Gabel J, Hansen T. Effect of outflow pressure on lung lymph flow in unanesthetized sheep. J Appl Physiol 1985; 58: 7076.Google Scholar
Johnson SA, Vander Straten MC, Parellada JA, Schnakenberg W, Gest AL. Thoracic duct function in fetal, newborn, and adult sheep. Lymphology 1996; 29: 5056.Google Scholar
Feltes TF, Hansen TN. Pulmonary edema. In: Garson A Jr, Bricker T, Fisher DJ, Neish SR (eds). The Science and Practice of Pediatric Cardiology. Williams & Wilkins, Baltimore, 1998, pp 313327.
von der Weid PY, Zhao J, Van Helden DF. Nitric oxide decreases pacemaker activity in lymphatic vessels of guinea pig mesentery. Am J Physiol Heart Circ Physiol 2001; 280: H2707H2716.Google Scholar
Griese M. Respiratory syncytial virus and pulmonary surfactant. Viral Immunol 2002; 15: 357363.Google Scholar
Carpenter TC, Reeves JT, Durmowicz AG. Viral respiratory infection increases susceptibility of young rats to hypoxia-induced pulmonary edema. J App Physiol 1998; 84: 10481054.Google Scholar
Carpenter TC, Stenmark KR. Predisposition of infants with chronic lung disease to respiratory syncytial virus-induced respiratory failure: a vascular hypothesis. Pediatr Infect Dis J 2004; 23 (Suppl): S33S40.Google Scholar
Lee CG, Yoon HJ, Zhu Z, et al. Respiratory syncytial virus stimulation of vascular endothelial cell growth factor/vascular permeability factor. Am J Respir Cell Mol Biol 2000; 23: 662669.Google Scholar
Garofalo RP, Patti J, Hintz KA, Hill V, Ogra PL, Welliver RC. Macrophage inflammatory protein-1alpha (not T helper type 2 cytokines) is associated with severe forms of respiratory syncytial virus bronchiolitis. J Infect Dis 2001; 184: 393399.Google Scholar
Legg JP, Hussain IR, Warner JA, Johnston SL, Warner JO. Type 1 and type 2 cytokine imbalance in acute respiratory syncytial virus bronchiolitis. Am J Respir Crit Care Med 2003; 168: 633639.Google Scholar
McNamara PS, Flanagan BF, Selby AM, Hart CA, Smyth RL. Pro- and anti-inflammatory responses in respiratory syncytial virus bronchiolitis. Eur Respir J 2004; 23: 106112.Google Scholar
Sheeran P, Jafri H, Carubelli C, et al. Elevated cytokine concentrations in the nasopharyngeal and tracheal secretions of children with respiratory syncytial virus disease. Pediatr Infect Dis J 1999; 18: 115122.Google Scholar
Carpenter TC, Stenmark KR. Endothelin receptor blockade decreases lung water in young rats exposed to viral infection and hypoxia. Am J Physiol Lung Cell Mol Physiol 2000; 279: L547L554.Google Scholar
Kunzelmann K, Beesley AH, King NJ, Karupiah G, Young JA, Cook DI. Influenza virus inhibits amiloride-sensitive Na+ channels in respiratory epithelia. Proc Natl Acad Sci USA 2000; 97: 1028210287.Google Scholar
Towne JE, Harrod KS, Krane CM, Menon AG. Decreased expression of aquaporin (AQP)1 and AQP5 in mouse lung after acute viral infection. Am J Respir Cell Mol Biol 2000; 22: 3444.Google Scholar
Suzuki S, Noda M, Sugita M, Ono S, Koike K, Fujimura S. Impairment of transalveolar fluid transport and lung Na+-K+-ATPase function by hypoxia in rats. J Appl Physiol 1999; 87: 962968.Google Scholar
Carpenter TC, Schomberg S, Nichols C, Stenmark KR, Weil JV. Hypoxia reversibly inhibits epithelial sodium transport but does not inhibit lung ENaC or Na-K-ATPase expression. Am J Physiol Lung Cell Mol Physiol 2003; 284: L77L83.Google Scholar
Sigurs N. Epidemiologic and clinical evidence of a respiratory syncytial virus-reactive airway disease link. Am J Respir Crit Care Med 2001; 163: S2S6.Google Scholar
Piedimonte G. The association between respiratory syncytial virus infection and reactive airway disease. Respir Med 2002; 96 (Suppl B): S25S29.Google Scholar
Openshaw PJ, Dean GS, Culley FJ. Links between respiratory syncytial virus bronchiolitis and childhood asthma: clinical and research approaches. Pediatr Infect Dis J 2003; 22 (Suppl): S58S64; discussion S64S65.Google Scholar
Sigurs N, Bjarnason R, Sigurbergsson F, Kjellman B. Asthma and immunoglobulin E antibodies after respiratory syncytial virus bronchiolitis: a prospective cohort study with matched controls. Pediatrics 1995; 95: 500505.Google Scholar
Sigurs N, Bjarnason R, Sigurbergsson F, Kjellman B. Respiratory syncytial virus bronchiolitis in infancy is an important risk factor for asthma and allergy at age 7. Am J Respir Crit Care Med 2000; 161: 15011507.Google Scholar
Wang SZ, Forsyth KD. Asthma and respiratory syncytial virus infection in infancy: is there a link? Clin Exp Allergy 1998; 28: 927935.Google Scholar
Openshaw PJ. Potential mechanisms causing delayed effects of respiratory syncytial virus infection. Am J Respir Crit Care Med 2001; 163: S10S13.Google Scholar
Martinez FD. Respiratory syncytial virus bronchiolitis and the pathogenesis of childhood asthma. Pediatr Infect Dis J 2003; 22 (Suppl): S76S82.Google Scholar
Piedimonte G. Contribution of neuroimmune mechanisms to airway inflammation and remodeling during and after respiratory syncytial virus infection. Pediatr Infect Dis J 2003; 22 (Suppl): S66S74; discussion S74S75.Google Scholar
Welliver RC. Immunology of respiratory syncytial virus infection: eosinophils, cytokines, chemokines and asthma. Pediatr Infect Dis J 2000; 19: 780783; discussion 784785; 811813.Google Scholar
Culley FJ, Pollott J, Openshaw PJ. Age at first viral infection determines the pattern of T cell-mediated disease during reinfection in adulthood. J Exp Med 2002; 196: 13811386.Google Scholar
Ogra PL. Respiratory syncytial virus: the virus, the disease and the immune response. Paediatr Respir Rev 2004; 5 (Suppl A): S119S126.Google Scholar
Colten HR, Krause JE. Pulmonary inflammation – a balancing act. N Engl J Med 1997; 336: 10941097.Google Scholar
King KA, Hu C, Rodriguez MM, Romaguera R, Jiang X, Piedimonte G. Exaggerated neurogenic inflammation and substance P receptor upregulation in RSV-infected weanling rats. Am J Respir Cell Mol Biol 2001; 24: 101107.Google Scholar
Masoli M, Fabian D, Holt S, Beasley R. Global Initiative for Asthma (GINA) Program (2004). The global burden of asthma: executive summary of the GINA Dissemination Committee report. Allergy 2004; 59: 469478.Google Scholar
Piedimonte G, King KA, Holmgren NL, Bertrand PJ, Rodriguez MM, Hirsch RL. A humanized monoclonal antibody against respiratory syncytial virus (palivizumab) inhibits RSV-induced neurogenic-mediated inflammation in rat airways. Pediatr Res 2000; 47: 351356.Google Scholar
Simoes EA, Carbonell-Estrany X, Kimpen JJ, et al. Palivizumab use decreases risk of recurrent wheezing in preterm children (Abstract #4772), European Respiratory Society Congress, Glasgow, UK, September 48, 2004.