Viral bronchiolitis in young rats causes small airway lesions that correlate with reduced lung function.

Viral illness with wheezing during infancy is associated with the inception of childhood asthma. Small airway dysfunction is a component of childhood asthma, but little is known about how viral illness at an early age may affect the structure and function of small airways. We used a well-characterized rat model of postbronchiolitis chronic airway dysfunction to address how postinfectious small airway lesions affect airway physiological function and if the structure/function correlates persist into maturity. Brown Norway rats were sham- or virus inoculated at 3 to 4 weeks of age and allowed to recover from the acute illness. At 3 to 14 months of age, physiology (respiratory system resistance, Newtonian resistance, tissue damping, and static lung volumes) was assessed in anesthetized, intubated rats. Serial lung sections revealed lesions in the terminal bronchioles that reduced luminal area and interrupted further branching, affecting 26% (range, 13-39%) of the small airways at 3 months of age and 22% (range, 6-40%) at 12 to 14 months of age. At 3 months of age (n = 29 virus; n = 7 sham), small airway lesions correlated with tissue damping (rs = 0.69) but not with Newtonian resistance (rs = 0.23), and Newtonian resistance was not elevated compared with control rats, indicating that distal airways were primarily responsible for the airflow obstruction. Older rats (n = 7 virus; n = 6 sham) had persistent small airway dysfunction and significantly increased Newtonian resistance in the postbronchiolitis group. We conclude that viral airway injury at an early age may induce small airway lesions that are associated quantitatively with small airway physiological dysfunction early on and that these defects persist into maturity.

[1]  T. Mahr,et al.  Rhinovirus Wheezing Illness and Genetic Risk of Childhood-Onset Asthma , 2013, Pediatrics.

[2]  S. Fain,et al.  Pulmonary 3He magnetic resonance imaging of childhood asthma. , 2013, The Journal of allergy and clinical immunology.

[3]  A. Wexler,et al.  Postnatal growth of tracheobronchial airways of Sprague–Dawley rats , 2011, Journal of anatomy.

[4]  A. Fitzpatrick,et al.  Sex dependence of airflow limitation and air trapping in children with severe asthma. , 2011, The Journal of allergy and clinical immunology.

[5]  Jeffrey J. Fredberg,et al.  Oscillation Mechanics of the Respiratory System , 2011 .

[6]  R. Stein,et al.  Respiratory syncytial virus and asthma: still no final answer , 2010, Thorax.

[7]  William W Busse,et al.  Role of viral respiratory infections in asthma and asthma exacerbations , 2010, The Lancet.

[8]  P. Sly,et al.  Do early-life viral infections cause asthma? , 2010, The Journal of allergy and clinical immunology.

[9]  T. Mahr Wheezing Rhinovirus Illnesses in Early Life Predict Asthma Development in High-Risk Children , 2009, Pediatrics.

[10]  Tebeb Gebretsadik,et al.  The severity-dependent relationship of infant bronchiolitis on the risk and morbidity of early childhood asthma. , 2009, The Journal of allergy and clinical immunology.

[11]  W. Busse,et al.  Lung function in adults with stable but severe asthma: air trapping and incomplete reversal of obstruction with bronchodilation. , 2008, Journal of applied physiology.

[12]  S. Guerra,et al.  Low IFN-γ production in the first year of life as a predictor of wheeze during childhood , 2007 .

[13]  R. Sorkness,et al.  Altered allergen-induced eosinophil trafficking and physiological dysfunction in airways with preexisting virus-induced injury. , 2007, American journal of physiology. Lung cellular and molecular physiology.

[14]  S. Erzurum,et al.  Features of severe asthma in school-age children: Atopy and increased exhaled nitric oxide. , 2006, The Journal of allergy and clinical immunology.

[15]  D. Hyde,et al.  Cyclic exposure to ozone alters distal airway development in infant rhesus monkeys. , 2006, American journal of physiology. Lung cellular and molecular physiology.

[16]  R. Sorkness,et al.  Attenuated innate mechanisms of interferon-gamma production in rats susceptible to postviral airway dysfunction. , 2004, American journal of respiratory cell and molecular biology.

[17]  R. Sorkness,et al.  Contribution of airway closure to chronic postbronchiolitis airway dysfunction in rats. , 2004, Journal of applied physiology.

[18]  S. Giguère,et al.  IL-12 reduces the severity of Sendai virus-induced bronchiolar inflammation and remodeling. , 2003, Cytokine.

[19]  R. Sorkness,et al.  Origin of Respiratory Virus-Induced Chronic Airway Dysfunction Exploring Genetic, Developmental, and Environmental Factors in a Rat Model of the Asthmatic Phenotype , 2003 .

[20]  N. Papadopoulos,et al.  Respiratory infections in allergy and asthma , 2003 .

[21]  R. Sorkness,et al.  Persistence of viral RNA in 2 rat strains differing in susceptibility to postbronchiolitis airway dysfunction. , 2002, The Journal of allergy and clinical immunology.

[22]  R. Sorkness,et al.  Chronic Postbronchiolitis Airway Instability Induced with Anti-IFN-γ Antibody in F344 Rats , 2002, Pediatric Research.

[23]  R. Sorkness,et al.  Chronic postbronchiolitis airway instability induced with anti-IFN-gamma antibody in F344 rats. , 2002, Pediatric research.

[24]  R. Sorkness,et al.  Prevention of Chronic Postbronchiolitis Airway Sequelae with IFN- γ Treatment in Rats , 1999 .

[25]  R. Sorkness,et al.  Chronic, episodic, reversible airway obstruction after viral bronchiolitis in rats. , 1997, American journal of respiratory and critical care medicine.

[26]  W. Busse,et al.  Parainfluenza virus-induced persistence of airway inflammation, fibrosis, and dysfunction associated with TGF-beta 1 expression in brown Norway rats. , 1996, American journal of respiratory and critical care medicine.

[27]  R. Sorkness,et al.  Virus-induced airway obstruction and parasympathetic hyperresponsiveness in adult rats. , 1994, American journal of respiratory and critical care medicine.

[28]  S. Sorden,et al.  Brown Norway rats are high responders to bronchiolitis, pneumonia, and bronchiolar mastocytosis induced by parainfluenza virus. , 1991, Experimental lung research.

[29]  S. Young,et al.  Postnatal growth of pulmonary acini and alveoli in normal and oxygen-exposed rats studied by serial section reconstructions. , 1989, The American journal of anatomy.

[30]  Castleman Wl Alterations in pulmonary ultrastructure and morphometric parameters induced by parainfluenza (Sendai) virus in rats during postnatal growth. , 1984 .

[31]  W. Castleman Alterations in pulmonary ultrastructure and morphometric parameters induced by parainfluenza (Sendai) virus in rats during postnatal growth. , 1984, The American journal of pathology.

[32]  W. Castleman Respiratory tract lesions in weanling outbred rats infected with Sendai virus. , 1983, American journal of veterinary research.

[33]  E. Weibel,et al.  The postnatal growth of the rat lung. I. Morphometry , 1974, The Anatomical record.

[34]  M. Jacobsen,et al.  Postnatal growth and function of the pre-acinar airways , 1972, Thorax.

[35]  K. H. Mclean The pathology of acute bronchiolitis; a study of its evolution. II. The repair phase. , 1957, Australasian annals of medicine.

[36]  K. H. Mclean The pathology of acute bronchiolitis; a study of its evolution. I. The exudative phase. , 1956, Australasian annals of medicine.