Lower airway rhinovirus burden and the seasonal risk of asthma exacerbation

American Journal of Respiratory and Critical Care Medicine

Volumn 184, Issue 9, 2011, Pages 1007-1014

  Denlinger, Loren C ^a   Sorkness, Ron L ^a,b   Lee, Wai Ming ^a   Evans, Michael D ^a   Wolff, Michele J ^a   Mathur, Sameer K ^a,c   Crisafi, Gina M ^a   Gaworski, Katie L ^a   Pappas, Tressa E ^a   Vrtis, Rose F ^a   Kelly, Elizabeth A ^a   Gern, James E ^a   Jarjour, Nizar N ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c WILLIAM S MIDDLETON MEMORIAL VETERANS HOSPITAL   (United States)

Author keywords

Asthma; Exacerbation; Index; Neutrophil; Virus

Indexed keywords

VIRUS RNA;

ADULT; ARTICLE; ASTHMA; COHORT ANALYSIS; COMMON COLD; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE EXACERBATION; ENVIRONMENTAL EXPOSURE; FEMALE; FOLLOW UP; HUMAN; HUMAN RHINOVIRUS; INFLAMMATION; LOGISTIC REGRESSION ANALYSIS; LOWER RESPIRATORY TRACT INFECTION; MAJOR CLINICAL STUDY; MALE; NEUTROPHIL COUNT; NONHUMAN; PEAK EXPIRATORY FLOW; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SEASONAL VARIATION; SPUTUM ANALYSIS; SYMPTOM; UPPER RESPIRATORY TRACT INFECTION; VIRAL RESPIRATORY TRACT INFECTION; VIRUS DETECTION; VIRUS LOAD; VIRUS REPLICATION;

ACUTE DISEASE; ADOLESCENT; ADULT; ASTHMA; CASE-CONTROL STUDIES; DISEASE PROGRESSION; FEMALE; FOLLOW-UP STUDIES; FORCED EXPIRATORY VOLUME; HUMANS; INFLAMMATION; LEUKOCYTE COUNT; MALE; NASAL LAVAGE; NEUTROPHILS; PEAK EXPIRATORY FLOW RATE; PICORNAVIRIDAE INFECTIONS; PROSPECTIVE STUDIES; RECURRENCE; RESPIRATORY SYSTEM; RHINOVIRUS; SEASONS; SEVERITY OF ILLNESS INDEX; SPUTUM; VIRAL LOAD;

EID: 81055137288     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201103-0585OC     Document Type: Article

References (59)

1. Tattersfield AE, Postma DS, Barnes PJ, Svensson K, Bauer CA, O'Byrne PM, Lofdahl CG, Pauwels RA, Ullman A. Exacerbations of asthma: a descriptive study of 425 severe exacerbations. The Facet International Study Group. Am J Respir Crit Care Med 1999;160:594-599. (Pubitemid 29380678)
2. Weber EJ, Silverman RA, Callaham ML, Pollack CV, Woodruff PG, Clark S, Camargo CA Jr . A prospective multicenter study of factors associated with hospital admission among adults with acute asthma. Am J Med 2002;113:371-378. (Pubitemid 35223608)
3. O'Byrne PM, Pedersen S, Lamm CJ, Tan WC, Busse WW. Severe exacerbations and decline in lung function in asthma. Am J Respir Crit Care Med 2009;179:19-24.
4. Jackson DJ, Johnston SL. The role of viruses in acute exacerbations of asthma. J Allergy Clin Immunol 2010;125:1178-1187; quiz 1188-1179.
5. Nicholson KG, Kent J, Ireland DC. Respiratory viruses and exacerbations of asthma in adults. BMJ 1993;307:982-986. (Pubitemid 23306765)
6. Corne JM, Marshall C, Smith S, Schreiber J, Sanderson G, Holgate ST, Johnston SL. Frequency, severity, and duration of rhinovirus infections in asthmatic and non-asthmatic individuals: a longitudinal cohort study. Lancet 2002;359:831-834. (Pubitemid 34233753)
7. van Elden LJ, Sachs AP, van Loon AM, Haarman M, van de Vijver DA, Kimman TG, Zuithoff P, Schipper PJ, Verheij TJ, Nijhuis M. Enhanced severity of virus associated lower respiratory tract disease in asthma patients may not be associated with delayed viral clearance and increased viral load in the upper respiratory tract. J Clin Virol 2008;41:116-121.
8. Wark PA, Johnston SL, Moric I, Simpson JL, Hensley MJ, Gibson PG. Neutrophil degranulation and cell lysis is associated with clinical severity in virus-induced asthma. Eur Respir J 2002;19:68-75. (Pubitemid 34105570)
9. Grissell TV, Powell H, Shafren DR, Boyle MJ, Hensley MJ, Jones PD, Whitehead BF, Gibson PG. Interleukin-10 gene expression in acute virus-induced asthma. Am J Respir Crit Care Med 2005;172:433-439. (Pubitemid 41117388)
10. Johnston SL, Pattemore PK, Sanderson G, Smith S, Campbell MJ, Josephs LK, Cunningham A, Robinson BS, Myint SH, Ward ME, et al. The relationship between upper respiratory infections and hospital admissions for asthma: a time-trend analysis. Am J Respir Crit Care Med 1996;154:654-660. (Pubitemid 26327287)
11. Atmar RL, Guy E, Guntupalli KK, Zimmerman JL, Bandi VD, Baxter BD, Greenberg SB. Respiratory tract viral infections in inner-city asthmatic adults. Arch Intern Med 1998;158:2453-2459. (Pubitemid 28555504)
12. Green RM, Custovic A, Sanderson G, Hunter J, Johnston SL, Woodcock A. Synergism between allergens and viruses and risk of hospital admission with asthma: case-control study. BMJ 2002;324:763.
13. Jacoby DB. Virus-induced asthma attacks. JAMA 2002;287:755-761. (Pubitemid 34256350)
14. Guilbert TW, Denlinger LC. Role of infection in the development and exacerbation of asthma. Expert Rev Respir Med 2010;4:71-83.
15. Walter MJ, CastroM, Kunselman SJ, Chinchilli VM, Reno M, Ramkumar TP, Avila PC, Boushey HA, Ameredes BT, Bleecker ER, et al. Predicting worsening asthma control following the common cold. Eur Respir J 2008;32:1548-1554.
16. Rosenthal LA, Avila PC, Heymann PW, Martin RJ, Miller EK, Papadopoulos NG, Peebles RS Jr, Gern JE. Viral respiratory tract infections and asthma: the course ahead. J Allergy Clin Immunol 2010;125:1212-1217.
17. Calhoun WJ, Dick EC, Schwartz LB, Busse WW. A common cold virus, rhinovirus 16, potentiates airway inflammation after segmentalantigen bronchoprovocation in allergic subjects. J Clin Invest 1994;94:2200-2208. (Pubitemid 24379589)
18. Lemanske RF Jr, Dick EC, Swenson CA, Vrtis RF, Busse WW. Rhinovirus upper respiratory infection increases airway hyperreactivity and late asthmatic reactions. J Clin Invest 1989;83:1-10. (Pubitemid 19048397)
19. Grunberg K, Timmers MC, Smits HH, de Klerk EP, Dick EC, Spaan WJ, Hiemstra PS, Sterk PJ. Effect of experimental rhinovirus 16 colds on airway hyperresponsiveness to histamine and interleukin-8 in nasal lavage in asthmatic subjects in vivo. Clin Exp Allergy 1997;27:36-45. (Pubitemid 27051361)
20. Jarjour NN, Gern JE, Kelly EA, Swenson CA, Dick CR, Busse WW. The effect of an experimental rhinovirus 16 infection on bronchial lavage neutrophils. J Allergy Clin Immunol 2000;105:1169-1177. (Pubitemid 30418797)
21. Gern JE, Vrtis R, Grindle KA, Swenson C, Busse WW. Relationship of upper and lower airway cytokines to outcome of experimental rhinovirus infection. Am J Respir Crit Care Med 2000;162:2226-2231. (Pubitemid 32051692)
22. Wark PA, Johnston SL, Bucchieri F, Powell R, Puddicombe S, Laza-Stanca V, Holgate ST, Davies DE. Asthmatic bronchial epithelial cells have a deficient innate immune response to infection with rhinovirus. J ExpMed 2005;201:937-947. (Pubitemid 40524463)
23. Contoli M, Message SD, Laza-Stanca V, Edwards MR, Wark PA, Bartlett NW, Kebadze T, Mallia P, Stanciu LA, Parker HL, et al. Role of deficient type III interferon-lambda production in asthma exacerbations. Nat Med 2006;12:1023-1026. (Pubitemid 44353382)
24. Fleming HE, Little FF, Schnurr D, Avila PC, Wong H, Liu J, Yagi S, Boushey HA. Rhinovirus-16 colds in healthy and in asthmatic subjects: similar changes in upper and lower airways. Am J Respir Crit Care Med 1999;160:100-108. (Pubitemid 29326074)
25. Fraenkel DJ, Bardin PG, Sanderson G, Lampe F, Johnston SL, Holgate ST. Lower airways inflammation during rhinovirus colds in normal and in asthmatic subjects. Am J Respir Crit Care Med 1995;151:879-886.
26. DeMore JP, Weisshaar EH, Vrtis RF, Swenson CA, Evans MD, Morin A, Hazel E, Bork JA, Kakumanu S, Sorkness R, et al. Similar colds in subjects with allergic asthma and nonatopic subjects after inoculation with rhinovirus-16. J Allergy Clin Immunol 2009;124:245-252.
27. Fahy JV, Kim KW, Liu J, Boushey HA. Prominent neutrophilic inflammation in sputum from subjects with asthma exacerbation. J Allergy Clin Immunol 1995;95:843-852.
28. Pizzichini MM, Pizzichini E, Efthimiadis A, Chauhan AJ, Johnston SL, Hussack P, Mahony J, Dolovich J, Hargreave FE. Asthma and natural colds. Inflammatory indices in induced sputum: a feasibility study. Am J Respir Crit Care Med 1998;158:1178-1184. (Pubitemid 28489020)
29. Palmenberg AC, Spiro D, Kuzmickas R, Wang S, Djikeng A, Rathe JA, Fraser-Liggett CM, Liggett SB. Sequencing and analyses of all known human rhinovirus genomes reveal structure and evolution. Science 2009;324:55-59.
30. Greve JM, Davis G, Meyer AM, Forte CP, Yost SC, Marlor CW, Kamarck ME, McClelland A. The major human rhinovirus receptor is ICAM-1. Cell 1989;56:839-847. (Pubitemid 19082519)
31. Staunton DE, Merluzzi VJ, Rothlein R, Barton R, Marlin SD, Springer TA. A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell 1989;56:849-853. (Pubitemid 19082520)
32. Tomassini JE, Graham D, DeWitt CM, Lineberger DW, Rodkey JA, Colonno RJ. cDNA cloning reveals that the major group rhinovirus receptor on HeLa cells is intercellular adhesion molecule 1. Proc Natl Acad Sci USA 1989;86:4907-4911. (Pubitemid 19182207)
33. Hofer F, Gruenberger M, Kowalski H, Machat H, Huettinger M, Kuechler E, Blaas D. Members of the low density lipoprotein receptor family mediate cell entry of a minor-group common cold virus. Proc Natl Acad Sci USA 1994;91:1839-1842. (Pubitemid 24080301)
34. Lee WM, Kiesner C, Pappas T, Lee I, Grindle K, Jartti T, Jakiela B, Lemanske RF Jr, Shult PA, Gern JE. A diverse group of previously unrecognized human rhinoviruses are common causes of respiratory illnesses in infants. PLoS ONE 2007;2:e966.
35. Khetsuriani N, Lu X, Teague WG, Kazerouni N, Anderson LJ, Erdman DD. Novel human rhinoviruses and exacerbation of asthma in children. Emerg Infect Dis 2008;14:1793-1796.
36. Miller EK, Edwards KM, Weinberg GA, Iwane MK, Griffin MR, Hall CB, Zhu Y, Szilagyi PG, Morin LL, Heil LH, et al. A novel group of rhinoviruses is associated with asthma hospitalizations. J Allergy Clin Immunol 2009;123:98-104.
37. Papadopoulos NG, Bates PJ, Bardin PG, Papi A, Leir SH, Fraenkel DJ, Meyer J, Lackie PM, Sanderson G, Holgate ST, et al. Rhinoviruses infect the lower airways. J Infect Dis 2000;181:1875-1884. (Pubitemid 30416147)
38. Mosser AG, Brockman-Schneider R, Amineva S, Burchell L, Sedgwick JB, BusseWW, Gern JE. Similar frequency of rhinovirus-infectible cells in upper and lower airway epithelium. J Infect Dis 2002;185:734-743. (Pubitemid 34226201)
39. Mosser AG, Vrtis R, Burchell L, Lee WM, Dick CR, Weisshaar E, Bock D, Swenson CA, Cornwell RD, Meyer KC, et al. Quantitative and qualitative analysis of rhinovirus infection in bronchial tissues. Am J Respir Crit Care Med 2005;171:645-651. (Pubitemid 40365422)
40. Gerna G, Piralla A, Rovida F, Rognoni V,Marchi A, Locatelli F,Meloni F. Correlation of rhinovirus load in the respiratory tract and clinical symptoms in hospitalized immunocompetent and immunocompromised patients. J Med Virol 2009;81:1498-1507.
41. Sorkness RL, Lee WM, Crisafi G, Vrtis R, Gern JE, Jarjour N. Rhinovirus-associated asthma exacerbations. Am J Respir Crit Care Med 2009;181:A5157.
42. Denlinger LC, Kelly EA, Wolff M, Gaworski K, Liu LY, Guadarrama AG, Crisafi G, Lee WM, Vrtis R, Evans MD, et al. Nasal inflammatory response to viral infection in persons with and without asthma. Am J Respir Crit Care Med 2010;181:A5654.
43. Jackson GG, Dowling HF, Spiesman IG, Boand AV. Transmission of the common cold to volunteers under controlled conditions. I. The common cold as a clinical entity. AMA Arch Intern Med 1958;101:267-278.
44. Denlinger LC, Shi L, Guadarrama A, Schell K, Green D, Morrin A, Hogan K, Sorkness RL, Busse WW, Gern JE. Attenuated p2 3 7 pore function as a risk factor for virus-induced loss of asthma control. Am J Respir Crit Care Med 2009;179:265-270.
45. Sorkness RL, Gonzalez-Fernandez G, Billmeyer EE, Evans MD, Gern JE, Jarjour NN. The asthma index: a continuous variable to characterize exacerbations of asthma. J Allergy Clin Immunol 2008;122:838-840.
46. LeeWM, Grindle K, Pappas T,MarshallDJ, MoserMJ, Beaty EL, Shult PA, Prudent JR, Gern JE. High-throughput, sensitive, and accurate multiplex PCR-microsphere flow cytometry system for large-scale comprehensive detection of respiratory viruses. J Clin Microbiol 2007;45:2626-2634. (Pubitemid 47295496)
47. Olenec JP, Kim WK, Lee WM, Vang F, Pappas TE, Salazar LE, Evans MD, Bork J, Roberg K, Lemanske RF Jr., et al.Weekly monitoring of children with asthma for infections and illness during common cold seasons. J Allergy Clin Immunol 2010;125:1001-1006.
48. Bizzintino J, Lee WM, Laing IA, Vang F, Pappas T, Zhang G, Martin AC, Khoo SK, Cox DW, Geelhoed GC, et al. Association between human rhinovirus C and severity of acute asthma in children. Eur Respir J 2011;37:1037-1042.
49. Bochkov YA, Palmenberg AC, Lee WM, Rathe JA, Amineva SP, Sun X, Pasic TR, Jarjour NN, Liggett SB, Gern JE. Molecular modeling, organ culture and reverse genetics for a newly identified human rhinovirus c. Nat Med 2011;17:627-632.
50. Xiang Z,Gonzalez R,Wang Z, Xiao Y, Chen L, Li T, Vernet G, Paranhos-Baccala G, Jin Q, Wang J. Human rhinoviruses in Chinese adults with acute respiratory tract infection. J Infect 2010;61:289-298.
51. Lau SK, Yip CC, Lin AW, Lee RA, So LY, Lau YL, Chan KH, Woo PC, Yuen KY. Clinical and molecular epidemiology of human rhinovirus C in children and adults in Hong Kong reveals a possible distinct human rhinovirus C subgroup. J Infect Dis 2009;200:1096-1103.
52. Grunberg K, Sharon RF, Hiltermann TJ, Brahim JJ, Dick EC, Sterk PJ, Van Krieken JH. Experimental rhinovirus 16 infection increases intercellular adhesion molecule-1 expression in bronchial epithelium of asthmatics regardless of inhaled steroid treatment. Clin Exp Allergy 2000;30:1015-1023. (Pubitemid 30427044)
53. Suzuki T, Yamaya M, Sekizawa K, Yamada N, Nakayama K, Ishizuka S, Kamanaka M, Morimoto T, Numazaki Y, Sasaki H. Effects of dexamethasone on rhinovirus infection in cultured human tracheal epithelial cells. Am J Physiol Lung Cell Mol Physiol 2000;278:L560-L571. (Pubitemid 30152514)
54. Wark PA, Grissell T, Davies B, See H, Gibson PG. Diversity in the bronchial epithelial cell response to infection with different rhinovirus strains. Respirology 2009;14:180-186.
55. Gustafson LM, Proud D, Hendley JO, Hayden FG, Gwaltney JM Jr. Oral prednisone therapy in experimental rhinovirus infections. J AllergyClin Immunol 1996;97:1009-1014. (Pubitemid 26116996)
56. Huynh ML, Malcolm KC, Kotaru C, Tilstra JA, Westcott JY, Fadok VA, Wenzel SE. Defective apoptotic cell phagocytosis attenuates prostaglandin E2 and 15-hydroxyeicosatetraenoic acid in severe asthma alveolar macrophages. Am J Respir Crit Care Med 2005;172:972-979. (Pubitemid 41476533)
57. Fitzpatrick AM, Holguin F, Teague WG, Brown LA. Alveolar macrophage phagocytosis is impaired in children with poorly controlled asthma. J Allergy Clin Immunol 2008;121:1372-1378.
58. Marshall DJ, Reisdorf E, Harms G, Beaty E, Moser MJ, Lee WM, Gern JE, Nolte FS, Shult P, Prudent JR. Evaluation of a multiplexed pcr assay for detection of respiratory viral pathogens in a public health laboratory setting. J Clin Microbiol 2007;45:3875-3882. (Pubitemid 350274865)
59. Covar RA, Szefler SJ, Zeiger RS, Sorkness CA, Moss M, Mauger DT, Boehmer SJ, Strunk RC, Martinez FD, Taussig LM. Factors associated with asthma exacerbations during a long-term clinical trial of controller medications in children. J Allergy Clin Immunol 2008;122:741-747.