Eosinophils as diagnostic tools in chronic lung disease

Expert Review of Respiratory Medicine

Volumn 7, Issue 1, 2013, Pages 33-42

  Eltboli, Osama ^a   Brightling, Christopher E ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

asthma; biomarkers; chronic cough; chronic obstructive pulmonary disease; eosinophils; idiopathic pulmonary fibrosis

Indexed keywords

CD34 ANTIGEN; CHEMOKINE RECEPTOR CCR3; COLONY STIMULATING FACTOR 1; CORTICOSTEROID; EOSINOPHIL CATIONIC PROTEIN; EOSINOPHIL PEROXIDASE; EOSINOPHIL PROTEIN X; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 13; INTERLEUKIN 3; INTERLEUKIN 4; INTERLEUKIN 5; LUMICAN; MAJOR BASIC PROTEIN; MEPOLIZUMAB; MOMETASONE FUROATE; PREDNISOLONE; RESLIZUMAB; TENASCIN;

AIRWAY OBSTRUCTION; AIRWAY REMODELING; ASTHMA; CAUSE OF DEATH; CHEST TIGHTNESS; CHRONIC COUGH; CHRONIC LUNG DISEASE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CORTICOSTEROID THERAPY; CYTOKINE RELEASE; CYTOKINE RESPONSE; CYTOTOXICITY; DISEASE ASSOCIATION; DISEASE EXACERBATION; DYSPNEA; EOSINOPHIL; EOSINOPHIL COUNT; EOSINOPHILIA; FIBROSING ALVEOLITIS; FORCED EXPIRATORY VOLUME; HOSPITAL ADMISSION; HUMAN; INTERSTITIAL LUNG DISEASE; LEUKOCYTE COUNT; LUNG LAVAGE; NASAL LAVAGE; NOSE POLYP; OCCUPATIONAL ASTHMA; PHASE 3 CLINICAL TRIAL (TOPIC); PROTEIN EXPRESSION; PROTEIN MOTIF; RANDOMIZED CONTROLLED TRIAL (TOPIC); RESPIRATORY TRACT INFLAMMATION; REVIEW; SEVERE PERSISTENT ASTHMA; SPUTUM; STEM CELL; TH2 CELL; THORAX RADIOGRAPHY; WHEEZING;

EID: 84873136114     PISSN: 17476348     EISSN: 17476356     Source Type: Journal    
DOI: 10.1586/ers.12.81     Document Type: Review

References (97)

1. Pavord ID, Pizzichini MM, Pizzichini E, Hargreave FE. The use of induced sputum to investigate airway inflammation. Thorax 52(6), 498-501 (1997). (Pubitemid 27298498)
2. Brightling CE. Clinical applications of induced sputum. Chest 129(5), 1344-1348 (2006).
3. Wardlaw AJ, Brightling C, Green R, Woltmann G, Pavord I. Eosinophils in asthma and other allergic diseases. Br. Med. Bull. 56(4), 985-1003 (2000). (Pubitemid 32417164)
4. Denburg JA. Bone marrow in atopy and asthma: hematopoietic mechanisms in allergic inflammation. Immunol. Today 20(3), 111-113 (1999). (Pubitemid 29130338)
5. Uhm TG, Kim BS, Chung IY. Eosinophil development, regulation of eosinophilspecific genes, and role of eosinophils in the pathogenesis of asthma. Allergy. Asthma Immunol. Res. 4(2), 68-79 (2012).
6. Wardlaw AJ. Molecular basis for selective eosinophil trafficking in asthma: a multistep paradigm. J. Allergy Clin. Immunol. 104(5), 917-926 (1999).
7. Saha S, Brightling CE. Eosinophilic airway inflammation in COPD. Int. J. Chron. Obstruct. Pulmon. Dis. 1(1), 39-47 (2006).
8. Symon FA, Lawrence MB, Williamson ML, Walsh GM, Watson SR, Wardlaw AJ. Functional and structural characterization of the eosinophil P-selectin ligand. J. Immunol. 157(4), 1711-1719 (1996). (Pubitemid 126449115)
9. Woltmann G, McNulty CA, Dewson G, Symon FA, Wardlaw AJ. Interleukin-13 induces PSGL-1/P-selectin-dependent adhesion of eosinophils, but not neutrophils, to human umbilical vein endothelial cells under flow. Blood 95(10), 3146-3152 (2000). (Pubitemid 30321166)
10. Swaminathan GJ, Myszka DG, Katsamba PS, Ohnuki LE, Gleich GJ, Acharya KR. Eosinophil-granule major basic protein, a C-type lectin, binds heparin. Biochemistry 44(43), 14152-14158 (2005). (Pubitemid 41533040)
11. Navarro S, Aleu J, Jiménez M, Boix E, Cuchillo CM, Nogués MV. The cytotoxicity of eosinophil cationic protein/ ribonuclease 3 on eukaryotic cell lines takes place through its aggregation on the cell membrane. Cell. Mol. Life Sci. 65(2), 324-337 (2008).
12. Gibson PG, Woolley KL, Carty K, Murree-Allen K, Saltos N. Induced sputum eosinophil cationic protein (ECP) measurement in asthma and chronic obstructive airway disease (COAD). Clin. Exp. Allergy 28(9), 1081-1088 (1998). (Pubitemid 28432630)
13. Pizzichini MM, Pizzichini E, Clelland L et al. Sputum in severe exacerbations of asthma: kinetics of inflammatory indices after prednisone treatment. Am. J. Respir. Crit. Care Med. 155(5), 1501-1508 (1997). (Pubitemid 27216650)
14. Fujimoto K, Yasuo M, Urushibata K, Hanaoka M, Koizumi T, Kubo K. Airway inflammation during stable and acutely exacerbated chronic obstructive pulmonary disease. Eur. Respir. J. 25(4), 640-646 (2005). (Pubitemid 40528756)
15. Rohde G, Gevaert P, Holtappels G et al. Soluble interleukin-5 receptor α is increased in acute exacerbation of chronic obstructive pulmonary disease. Int. Arch. Allergy Immunol. 135(1), 54-61 (2004). (Pubitemid 39279432)
16. Fiorini G, Crespi S, Rinaldi M, Oberti E, Vigorelli R, Palmieri G. Serum ECP and MPO are increased during exacerbations of chronic bronchitis with airway obstruction. Biomed. Pharmacother. 54(5), 274-278 (2000). (Pubitemid 30432097)
17. van Dalen CJ, Winterbourn CC, Kettle AJ. Mechanism of nitrite oxidation by eosinophil peroxidase: implications for oxidant production and nitration by eosinophils. Biochem. J. 394(Pt 3), 707-713 (2006).
18. Ayars GH, Altman LC, Gleich GJ, Loegering DA, Baker CB. Eosinophil-and eosinophil granule-mediated pneumocyte injury. J. Allergy Clin. Immunol. 76(4), 595-604 (1985). (Pubitemid 15245025)
19. Trautmann A, Schmid-Grendelmeier P, Krüger K et al. T cells and eosinophils cooperate in the induction of bronchial epithelial cell apoptosis in asthma. J. Allergy Clin. Immunol. 109(2), 329-337 (2002). (Pubitemid 34158302)
20. Chang KC, Lo CW, Fan TC et al. TNF-α mediates eosinophil cationic proteininduced apoptosis in BEAS-2B cells. BMC Cell Biol. 11, 6 (2010).
21. Saetta M, Di Stefano A, Maestrelli P et al. Airway eosinophilia in chronic bronchitis during exacerbations. Am. J. Respir. Crit. Care Med. 150(6 Pt 1), 1646-1652 (1994). (Pubitemid 24361741)
22. Jatakanon A, Lim S, Barnes PJ. Changes in sputum eosinophils predict loss of asthma control. Am. J. Respir. Crit. Care Med. 161(1), 64-72 (2000). (Pubitemid 30055904)
23. Fujimoto K, Kubo K, Matsuzawa Y, Sekiguchi M. Eosinophil cationic protein levels in induced sputum correlate with the severity of bronchial asthma. Chest 112(5), 1241-1247 (1997). (Pubitemid 27497854)
24. Virchow JC Jr, Hölscher U, Virchow C Snr. Sputum ECP levels correlate with parameters of airflow obstruction. Am. Rev. Respir. Dis. 146(3), 604-606 (1992).
25. Pizzichini E, Pizzichini MM, Efthimiadis A et al. Indices of airway inflammation in induced sputum: reproducibility and validity of cell and fluid-phase measurements. Am. J. Respir. Crit. Care Med. 154(2 Pt 1), 308-317 (1996). (Pubitemid 26269096)
26. Gürsel G, Türktas H, Gökçora N, Tekin IO. Comparison of sputum and serum eosinophil cationic protein (ECP) levels in nonatopic asthma and chronic obstructive pulmonary disease. J. Asthma 34(4), 313-319 (1997). (Pubitemid 27365642)
27. Balzano G, Stefanelli F, Iorio C et al. Eosinophilic inflammation in stable chronic obstructive pulmonary disease. Relationship with neutrophils and airway function. Am. J. Respir. Crit. Care Med. 160(5 Pt 1), 1486-1492 (1999).
28. Amici MD, Moratti R, Quaglini S, Alesina R, Peona V. Increased serum inflammatory markers as predictors of airway obstruction. J. Asthma 43(8), 593-596 (2006). (Pubitemid 44581253)
29. Bathoorn E, Kerstjens H, Postma D, Timens W, MacNee W. Airways inflammation and treatment during acute exacerbations of COPD. Int. J. Chron. Obstruct. Pulmon. Dis. 3(2), 217-229 (2008). (Pubitemid 352037882)
30. Fahy JV, Corry DB, Boushey HA. Airway inflammation and remodeling in asthma. Curr. Opin. Pulm. Med. 6(1), 15-20 (2000).
31. Holgate ST, Arshad HS, Roberts GC, Howarth PH, Thurner P, Davies DE. A new look at the pathogenesis of asthma. Clin. Sci. 118(7), 439-450 (2010).
32. Messina MS, O'Riordan TG, Smaldone GC. Changes in mucociliary clearance during acute exacerbations of asthma. Am. Rev. Respir. Dis. 143(5 Pt 1), 993-997 (1991).
33. Innes AL, Carrington SD, Thornton DJ et al. Ex vivo sputum analysis reveals impairment of protease-dependent mucus degradation by plasma proteins in acute asthma. Am. J. Respir. Crit. Care Med. 180(3), 203-210 (2009).
34. Belda J, Leigh R, Parameswaran K, O'Byrne PM, Sears MR, Hargreave FE. Induced sputum cell counts in healthy adults. Am. J. Respir. Crit. Care Med. 161(2 Pt 1), 475-478 (2000). (Pubitemid 30129455)
35. Green RH, Brightling CE, Woltmann G, Parker D, Wardlaw AJ, Pavord ID. Analysis of induced sputum in adults with asthma: identification of subgroup with isolated sputum neutrophilia and poor response to inhaled corticosteroids. Thorax 57(10), 875-879 (2002). (Pubitemid 35178612)
36. Hunter CJ, Brightling CE, Woltmann G, Wardlaw AJ, Pavord ID. A comparison of the validity of different diagnostic tests in adults with asthma. Chest 121(4), 1051-1057 (2002). (Pubitemid 34280422)
37. Simpson JL, McElduff P, Gibson PG. Assessment and reproducibility of non-eosinophilic asthma using induced sputum. Respiration 79(2), 147-151 (2010).
38. Pizzichini E, Pizzichini MM, Gibson P et al. Sputum eosinophilia predicts benefit from prednisone in smokers with chronic obstructive bronchitis. Am. J. Respir. Crit. Care Med. 158(5 Pt 1), 1511-1517 (1998).
39. Bacci E, Cianchetti S, Bartoli M et al. Low sputum eosinophils predict the lack of response to beclomethasone in symptomatic asthmatic patients. Chest 129(3), 565-572 (2006).
40. Brightling CE, Monteiro W, Ward R et al. Sputum eosinophilia and short-term response to prednisolone in chronic obstructive pulmonary disease: a rand-omized controlled trial. Lancet 356(9240), 1480-1485 (2000).
41. Brightling CE, McKenna S, Hargadon B et al. Sputum eosinophilia and the short term response to inhaled mometasone in chronic obstructive pulmonary disease. Thorax 60(3), 193-198 (2005). (Pubitemid 40380276)
42. Pavord ID, Brightling CE, Woltmann G, Wardlaw AJ. Non-eosinophilic corticosteroid unresponsive asthma. Lancet 353(9171), 2213-2214 (1999). (Pubitemid 29295261)
43. Gibson PG, Simpson JL, Saltos N. Heterogeneity of airway inflammation in persistent asthma: evidence of neutrophilic inflammation and increased sputum interleukin-8. Chest 119(5), 1329-1336 (2001). (Pubitemid 32686012)
44. Green RH, Brightling CE, McKenna S et al. Asthma exacerbations and sputum eosinophil counts: a randomised controlled trial. Lancet 360(9347), 1715-1721 (2002). (Pubitemid 35447900)
45. Turner MO, Hussack P, Sears MR, Dolovich J, Hargreave FE. Exacerbations of asthma without sputum eosinophilia. Thorax 50(10), 1057-1061 (1995).
46. McGrath KW, Icitovic N, Boushey HA et al.; Asthma Clinical Research Network of the National Heart, Lung, and Blood Institute. A large subgroup of mild-tomoderate asthma is persistently noneosinophilic. Am. J. Respir. Crit. Care Med. 185(6), 612-619 (2012).
47. Berry M, Morgan A, Shaw DE et al. Pathological features and inhaled corticosteroid response of eosinophilic and non-eosinophilic asthma. Thorax 62(12), 1043-1049 (2007). (Pubitemid 350206195)
48. Douwes J, Gibson P, Pekkanen J, Pearce N. Non-eosinophilic asthma: importance and possible mechanisms. Thorax 57(7), 643-648 (2002). (Pubitemid 34761769)
49. Jiang YW, Sun YC, Zhou QT, Gai XY, Cao WL, Yao WZ. [The relationship between sputum eosinophils and responses to treatment of inhaled glucocorticoids in patients with persistent asthma]. Zhonghua Jie He He Hu Xi Za Zhi 30(6), 447-451 (2007).
50. Little SA, Chalmers GW, MacLeod KJ, McSharry C, Thomson NC. Non-invasive markers of airway inflammation as predictors of oral steroid responsiveness in asthma. Thorax 55(3), 232-234 (2000). (Pubitemid 30245974)
51. Meijer RJ, Postma DS, Kauffman HF, Arends LR, Koëter GH, Kerstjens HA. Accuracy of eosinophils and eosinophil cationic protein to predict steroid improvement in asthma. Clin. Exp. Allergy 32(7), 1096-1103 (2002). (Pubitemid 34779609)
52. Anees W, Huggins V, Pavord ID, Robertson AS, Burge PS. Occupational asthma due to low molecular weight agents: eosinophilic and non-eosinophilic variants. Thorax 57(3), 231-236 (2002). (Pubitemid 34214409)
53. Lemière C, D'Alpaos V, Chaboillez S et al. Investigation of occupational asthma: sputum cell counts or exhaled nitric oxide? Chest 137(3), 617-622 (2010).
54. Leuppi JD, Salome CM, Jenkins CR et al. Predictive markers of asthma exacerbation during stepwise dose reduction of inhaled corticosteroids. Am. J. Respir. Crit. Care Med. 163(2), 406-412 (2001).
55. Chlumský J, Striz I, Terl M, Vondracek J. Strategy aimed at reduction of sputum eosinophils decreases exacerbation rate in patients with asthma. J. Int. Med. Res. 34(2), 129-139 (2006).
56. Jayaram L, Pizzichini MM, Cook RJ et al. Determining asthma treatment by monitoring sputum cell counts: effect on exacerbations. Eur. Respir. J. 27(3), 483-494 (2006). (Pubitemid 43372521)
57. Petsky HL, Cates CJ, Lasserson TJ et al. A systematic review and meta-analysis: tailoring asthma treatment on eosinophilic markers (exhaled nitric oxide or sputum eosinophils). Thorax 67(3), 199-208 (2012).
58. Haldar P, Pavord ID, Shaw DE et al. Cluster analysis and clinical asthma phenotypes. Am. J. Respir. Crit. Care Med. 178(3), 218-224 (2008).
59. Turner S, Paton J, Higgins B, Douglas G; British Guidelines on the Management of Asthma. British guidelines on the management of asthma: what's new for 2011? Thorax 66(12), 1104-1105 (2011).
60. Lougheed MD, Lemiere C, Ducharme FM et al.; Canadian Thoracic Society Asthma Clinical Assembly. Canadian Thoracic Society 2012 guideline update: diagnosis and management of asthma in preschoolers, children and adults. Can. Respir. J. 19(2), 127-164 (2012).
61. Kulkarni NS, Hollins F, Sutcliffe A et al. Eosinophil protein in airway macrophages: a novel biomarker of eosinophilic inflammation in patients with asthma. J. Allergy Clin. Immunol. 126(1), 61-69.e3 (2010).
62. Leckie MJ, ten Brinke A, Khan J et al. Effects of an interleukin-5 blocking monoclonal antibody on eosinophils, airway hyper-responsiveness, and the late asthmatic response. Lancet 356(9248), 2144-2148 (2000).
63. Flood-Page PT, Menzies-Gow AN, Kay AB, Robinson DS. Eosinophil's role remains uncertain as anti-interleukin-5 only partially depletes numbers in asthmatic airway. Am. J. Respir. Crit. Care Med. 167(2), 199-204 (2003). (Pubitemid 36076080)
64. Kips JC, O'Connor BJ, Langley SJ et al. Effect of SCH55700, a humanized anti-human interleukin-5 antibody, in severe persistent asthma: a pilot study. Am. J. Respir. Crit. Care Med. 167(12), 1655-1659 (2003). (Pubitemid 36760679)
65. Flood-Page P, Swenson C, Faiferman I et al.; International Mepolizumab Study Group. A study to evaluate safety and efficacy of mepolizumab in patients with moderate persistent asthma. Am. J. Respir. Crit. Care Med. 176(11), 1062-1071 (2007). (Pubitemid 350223751)
66. Haldar P, Brightling CE, Hargadon B et al. Mepolizumab and exacerbations of refractory eosinophilic asthma. N. Engl. J. Med. 360(10), 973-984 (2009).
67. Pavord ID, Korn S, Howarth P et al. Mepolizumab for severe eosinophilic asthma (DREAM): a multicentre, double-blind, placebo-controlled trial. Lancet 380(9842), 651-659 (2012).
68. Nair P, Pizzichini MM, Kjarsgaard M et al. Mepolizumab for prednisone-dependent asthma with sputum eosinophilia. N. Engl. J. Med. 360(10), 985-993 (2009).
69. Flood-Page P, Menzies-Gow A, Phipps S et al. Anti-IL-5 treatment reduces deposition of ECM proteins in the bronchial subepithelial basement membrane of mild atopic asthmatics. J. Clin. Invest. 112(7), 1029-1036 (2003). (Pubitemid 38056318)
70. Castro M, Mathur S, Hargreave F et al.; Res-5-0010 Study Group. Reslizumab for poorly controlled, eosinophilic asthma: a randomized, placebo-controlled study. Am. J. Respir. Crit. Care Med. 184(10), 1125-1132 (2011).
71. Stanescu D, Sanna A, Veriter C et al. Airways obstruction, chronic expectora-tion, and rapid decline of FEV1 in smokers are associated with increased levels of sputum neutrophils. Thorax 51(3), 267-271 (1996). (Pubitemid 26086470)
72. Rutgers SR, Timens W, Kaufmann HF, van der Mark TW, Koëter GH, Postma DS. Comparison of induced sputum with bronchial wash, bronchoalveolar lavage and bronchial biopsies in COPD. Eur. Respir. J. 15(1), 109-115 (2000). (Pubitemid 30068945)
73. Pesci A, Majori M, Cuomo A et al. Neutrophils infiltrating bronchial epithelium in chronic obstructive pulmonary disease. Respir. Med. 92(6), 863-870 (1998). (Pubitemid 28360616)
74. Pesci A, Balbi B, Majori M et al. Inflammatory cells and mediators in bronchial lavage of patients with chronic obstructive pulmonary disease. Eur. Respir. J. 12(2), 380-386 (1998). (Pubitemid 28389533)
75. Wen Y, Reid DW, Zhang D, Ward C, Wood-Baker R, Walters EH. Assessment of airway inflammation using sputum, BAL, and endobronchial biopsies in current and ex-smokers with established COPD. Int. J. Chron. Obstruct. Pulmon. Dis. 5, 327-334 (2010).
76. Yamamoto C, Yoneda T, Yoshikawa M et al. Airway inflammation in COPD assessed by sputum levels of interleukin-8. Chest 112(2), 505-510 (1997). (Pubitemid 27349446)
77. Dippolito R, Foresi A, Chetta A et al. Eosinophils in induced sputum from asymptomatic smokers with normal lung function. Respir. Med. 95(12), 969-974 (2001). (Pubitemid 34013545)
78. Hospers JJ, Schouten JP, Weiss ST, Postma DS, Rijcken B. Eosinophilia is associated with increased all-cause mortality after a follow-up of 30 years in a general population sample. Epidemiology 11(3), 261-268 (2000). (Pubitemid 30228192)
79. Hospers JJ, Schouten JP, Weiss ST, Rijcken B, Postma DS. Asthma attacks with eosinophilia predict mortality from chronic obstructive pulmonary disease in a general population sample. Am. J. Respir. Crit. Care Med. 160(6), 1869-1874 (1999). (Pubitemid 30004689)
80. Siva R, Green RH, Brightling CE et al. Eosinophilic airway inflammation and exacerbations of COPD: a randomised controlled trial. Eur. Respir. J. 29(5), 906-913 (2007). (Pubitemid 46711894)
81. Bafadhel M, McKenna S, Terry S et al. Acute exacerbations of chronic obstructive pulmonary disease: identification of biologic clusters and their biomarkers. Am. J. Respir. Crit. Care Med. 184(6), 662-671 (2011).
82. Papi A, Bellettato CM, Braccioni F et al. Infections and airway inflammation in chronic obstructive pulmonary disease severe exacerbations. Am. J. Respir. Crit. Care Med. 173(10), 1114-1121 (2006). (Pubitemid 43726892)
83. Bafadhel M, McKenna S, Terry S et al. Blood eosinophils to direct corticosteroid treatment of exacerbations of chronic obstructive pulmonary disease: a randomized placebo-controlled trial. Am. J. Respir. Crit. Care Med. 186(1), 48-55 (2012).
84. Irwin RS, Baumann MH, Bolser DC et al. Diagnosis and management of cough executive summary: ACCP evidence-based clinical practice guidelines. Chest 129(Suppl. 1), S1-S23 (2006).
85. Noseda A. [Management of chronic cough]. Rev. Med. Brux. 31(4), 250-254 (2010).
86. Brightling CE, Ward R, Goh KL, Wardlaw AJ, Pavord ID. Eosinophilic bronchitis is an important cause of chronic cough. Am. J. Respir. Crit. Care Med. 160(2), 406-410 (1999). (Pubitemid 29380649)
87. Brightling CE. Chronic cough due to nonasthmatic eosinophilic bronchitis: ACCP evidence-based clinical practice guidelines. Chest 129(Suppl. 1), S116-S121 (2006).
88. Pratter MR, Brightling CE, Boulet LP, Irwin RS. An empiric integrative approach to the management of cough: ACCP evidence-based clinical practice guidelines. Chest 129(Suppl. 1), S222-S231 (2006).
89. Berry MA, Hargadon B, McKenna S et al. Observational study of the natural history of eosinophilic bronchitis. Clin. Exp. Allergy 35(5), 598-601 (2005). (Pubitemid 40769283)
90. Brightling CE, Woltmann G, Wardlaw AJ, Pavord ID. Development of irreversible airflow obstruction in a patient with eosinophilic bronchitis without asthma. Eur. Respir. J. 14(5), 1228-1230 (1999).
91. Pizzichini MM, Pizzichini E, Parameswaran K et al. Nonasthmatic chronic cough: no effect of treatment with an inhaled corticosteroid in patients without sputum eosinophilia. Can. Respir. J. 6(4), 323-330 (1999). (Pubitemid 29427951)
92. Birring SS, Parker D, McKenna S et al. Sputum eosinophilia in idiopathic pulmonary fibrosis. Inflamm. Res. 54(2), 51-56 (2005). (Pubitemid 40585346)
93. Fujimoto K, Kubo K, Yamaguchi S, Honda T, Matsuzawa Y. Eosinophil activation in patients with pulmonary fibrosis. Chest 108(1), 48-54 (1995).
94. Antoniou KM, Alexandrakis M, Tzanakis N et al. Induced sputum versus bronchoalveolar lavage fluid in the evaluation of patients with idiopathic pulmonary fibrosis. Respiration. 72(1), 32-38 (2005). (Pubitemid 40470275)
95. Hiwatari N, Shimura S, Sasaki T et al. Prognosis of idiopathic pulmonary fibrosis in patients with mucous hypersecretion. Am. Rev. Respir. Dis. 143(1), 182-185 (1991).
96. Corren J, Lemanske RF, Hanania NA et al. Lebrikizumab treatment in adults with asthma. N. Engl. J. Med. 365(12), 1088-1098 (2011).
97. Jia G, Erickson RW, Choy DF et al.; Bronchoscopic Exploratory Research Study of Biomarkers in Corticosteroid-refractory Asthma (BOBCAT) Study Group. Periostin is a systemic biomarker of eosinophilic airway inflammation in asthmatic patients. J. Allergy Clin. Immunol. 130(3), 647-654.e10 (2012).