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Published in: Respiratory Research 1/2014

Open Access 01-12-2014 | Research

Clinical and computed tomographic predictors of chronic bronchitis in COPD: a cross sectional analysis of the COPDGene study

Authors: Victor Kim, Adam Davey, Alejandro P Comellas, Meilan K Han, George Washko, Carlos H Martinez, David Lynch, Jin Hwa Lee, Edwin K Silverman, James D Crapo, Barry J Make, Gerard J Criner, The COPDGene® Investigators

Published in: Respiratory Research | Issue 1/2014

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Abstract

Background

Chronic bronchitis (CB) has been related to poor outcomes in Chronic Obstructive Pulmonary Disease (COPD). From a clinical standpoint, we have shown that subjects with CB in a group with moderate to severe airflow obstruction were younger, more likely to be current smokers, male, Caucasian, had worse health related quality of life, more dyspnea, and increased exacerbation history compared to those without CB. We sought to further refine our clinical characterization of chronic bronchitics in a larger cohort and analyze the CT correlates of CB in COPD subjects. We hypothesized that COPD patients with CB would have thicker airways and a greater history of smoking, acute bronchitis, allergic rhinitis, and occupational exposures compared to those without CB.

Methods

We divided 2703 GOLD 1–4 subjects in the Genetic Epidemiology of COPD (COPDGene®) Study into two groups based on symptoms: chronic bronchitis (CB+, n = 663, 24.5%) and no chronic bronchitis (CB-, n = 2040, 75.5%). Subjects underwent extensive clinical characterization, and quantitative CT analysis to calculate mean wall area percent (WA%) of 6 segmental airways was performed using VIDA PW2 (http://​www.​vidadiagnostics.​com). Square roots of the wall areas of bronchi with internal perimeters 10 mm and 15 mm (Pi10 and Pi15, respectively), % emphysema, %gas trapping, were calculated using 3D Slicer (http://​www.​slicer.​org).

Results

There were no differences in % emphysema (11.4 ± 12.0 vs. 12.0 ± 12.6%, p = 0.347) or % gas trapping (35.3 ± 21.2 vs. 36.3 ± 20.6%, p = 0.272) between groups. Mean segmental WA% (63.0 ± 3.2 vs. 62.0 ± 3.1%, p < 0.0001), Pi10 (3.72 ± 0.15 vs. 3.69 ± 0.14 mm, p < 0.0001), and Pi15 (5.24 ± 0.22 vs. 5.17 ± 0.20, p < 0.0001) were greater in the CB + group. Greater percentages of gastroesophageal reflux, allergic rhinitis, histories of asthma and acute bronchitis, exposures to dusts and occupational exposures, and current smokers were seen in the CB + group. In multivariate binomial logistic regression, male gender, Caucasian race, a lower FEV1%, allergic rhinitis, history of acute bronchitis, current smoking, and increased airway wall thickness increased odds for having CB.

Conclusions

Histories of asthma, allergic rhinitis, acute bronchitis, current smoking, a lower FEV1%, Caucasian race, male gender, and increased airway wall thickness are associated with CB. These data provide clinical and radiologic correlations to the clinical phenotype of CB.
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Literature
1.
go back to reference Kim V, Criner GJ: Chronic bronchitis and chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2013, 187: 228-237. 10.1164/rccm.201210-1843CI.PubMedCrossRef Kim V, Criner GJ: Chronic bronchitis and chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2013, 187: 228-237. 10.1164/rccm.201210-1843CI.PubMedCrossRef
2.
go back to reference Kim V, Han MK, Vance GB, Make BJ, Newell JD, Hokanson JE, Hersh CP, Stinson D, Silverman EK, Criner GJ: The chronic bronchitic phenotype of COPD: an analysis of the COPDGene study. Chest. 2011, 140: 626-633. 10.1378/chest.10-2948.PubMedPubMedCentralCrossRef Kim V, Han MK, Vance GB, Make BJ, Newell JD, Hokanson JE, Hersh CP, Stinson D, Silverman EK, Criner GJ: The chronic bronchitic phenotype of COPD: an analysis of the COPDGene study. Chest. 2011, 140: 626-633. 10.1378/chest.10-2948.PubMedPubMedCentralCrossRef
3.
go back to reference Burgel PR, Nesme-Meyer P, Chanez P, Caillaud D, Carre P, Perez T, Roche N, Initiatives Bronchopneumopathie Chronique Obstructive Scientific Committee: Cough and sputum production are associated with frequent exacerbations and hospitalizations in COPD subjects. Chest. 2009, 135: 975-982. 10.1378/chest.08-2062.PubMedCrossRef Burgel PR, Nesme-Meyer P, Chanez P, Caillaud D, Carre P, Perez T, Roche N, Initiatives Bronchopneumopathie Chronique Obstructive Scientific Committee: Cough and sputum production are associated with frequent exacerbations and hospitalizations in COPD subjects. Chest. 2009, 135: 975-982. 10.1378/chest.08-2062.PubMedCrossRef
4.
go back to reference Innes AL, Woodruff PG, Ferrando RE, Donnelly S, Dolganov GM, Lazarus SC, Fahy JV: Epithelial mucin stores are increased in the large airways of smokers with airflow obstruction. Chest. 2006, 130: 1102-1108. 10.1378/chest.130.4.1102.PubMedCrossRef Innes AL, Woodruff PG, Ferrando RE, Donnelly S, Dolganov GM, Lazarus SC, Fahy JV: Epithelial mucin stores are increased in the large airways of smokers with airflow obstruction. Chest. 2006, 130: 1102-1108. 10.1378/chest.130.4.1102.PubMedCrossRef
5.
go back to reference Saetta M, Turato G, Baraldo S, Zanin A, Braccioni F, Mapp CE, Maestrelli P, Cavallesco G, Papi A, Fabbri LM: Goblet cell hyperplasia and epithelial inflammation in peripheral airways of smokers with both symptoms of chronic bronchitis and chronic airflow limitation. Am J Respir Crit Care Med. 2000, 161: 1016-1021. 10.1164/ajrccm.161.3.9907080.PubMedCrossRef Saetta M, Turato G, Baraldo S, Zanin A, Braccioni F, Mapp CE, Maestrelli P, Cavallesco G, Papi A, Fabbri LM: Goblet cell hyperplasia and epithelial inflammation in peripheral airways of smokers with both symptoms of chronic bronchitis and chronic airflow limitation. Am J Respir Crit Care Med. 2000, 161: 1016-1021. 10.1164/ajrccm.161.3.9907080.PubMedCrossRef
6.
go back to reference Hogg JC, Chu FS, Tan WC, Sin DD, Patel SA, Pare PD, Martinez FJ, Rogers RM, Make BJ, Criner GJ, Cherniack RM, Sharafkhaneh A, Luketich JD, Coxson HO, Elliott WM, Sciurba FC: Survival after lung volume reduction in chronic obstructive pulmonary disease: insights from small airway pathology. Am J Respir Crit Care Med. 2007, 176: 454-459. 10.1164/rccm.200612-1772OC.PubMedPubMedCentralCrossRef Hogg JC, Chu FS, Tan WC, Sin DD, Patel SA, Pare PD, Martinez FJ, Rogers RM, Make BJ, Criner GJ, Cherniack RM, Sharafkhaneh A, Luketich JD, Coxson HO, Elliott WM, Sciurba FC: Survival after lung volume reduction in chronic obstructive pulmonary disease: insights from small airway pathology. Am J Respir Crit Care Med. 2007, 176: 454-459. 10.1164/rccm.200612-1772OC.PubMedPubMedCentralCrossRef
7.
go back to reference Kim V, Criner GJ, Abdallah HY, Gaughan JP, Furukawa S, Solomides CC: Small airway morphometry and improvement in pulmonary function after lung volume reduction surgery. Am J Respir Crit Care Med. 2005, 171: 40-47. 10.1164/rccm.200405-659OC.PubMedCrossRef Kim V, Criner GJ, Abdallah HY, Gaughan JP, Furukawa S, Solomides CC: Small airway morphometry and improvement in pulmonary function after lung volume reduction surgery. Am J Respir Crit Care Med. 2005, 171: 40-47. 10.1164/rccm.200405-659OC.PubMedCrossRef
8.
go back to reference Hogg JC, Chu F, Utokaparch S, Woods R, Elliott WM, Buzatu L, Cherniack RM, Rogers RM, Sciurba FC, Coxson HO, Pare PD: The nature of small-airway obstruction in chronic obstructive pulmonary disease. N Engl J Med. 2004, 350: 2645-2653. 10.1056/NEJMoa032158.PubMedCrossRef Hogg JC, Chu F, Utokaparch S, Woods R, Elliott WM, Buzatu L, Cherniack RM, Rogers RM, Sciurba FC, Coxson HO, Pare PD: The nature of small-airway obstruction in chronic obstructive pulmonary disease. N Engl J Med. 2004, 350: 2645-2653. 10.1056/NEJMoa032158.PubMedCrossRef
9.
go back to reference Pelkonen M, Notkola IL, Nissinen A, Tukiainen H, Koskela H: Thirty-year cumulative incidence of chronic bronchitis and COPD in relation to 30-year pulmonary function and 40-year mortality: a follow-up in middle-aged rural men. Chest. 2006, 130: 1129-1137. 10.1378/chest.130.4.1129.PubMedCrossRef Pelkonen M, Notkola IL, Nissinen A, Tukiainen H, Koskela H: Thirty-year cumulative incidence of chronic bronchitis and COPD in relation to 30-year pulmonary function and 40-year mortality: a follow-up in middle-aged rural men. Chest. 2006, 130: 1129-1137. 10.1378/chest.130.4.1129.PubMedCrossRef
10.
go back to reference Reid LM: Pathology of chronic bronchitis. Lancet. 1954, 266: 274-278.PubMed Reid LM: Pathology of chronic bronchitis. Lancet. 1954, 266: 274-278.PubMed
11.
go back to reference Sciurba F, Martinez FJ, Rogers RM, Make B, Criner GJ, Cherniak RM, Patel SA, Chu F, Coxson HO, Sharafkhaneh A, Elliott WM, Luketich JD, Sin DD, Hogg JC: The effect of small airway pathology on survival following lung volume reduction surgery (LVRS): [abstract]. Proc Am Thorac Soc. 2006, 3: A712-CrossRef Sciurba F, Martinez FJ, Rogers RM, Make B, Criner GJ, Cherniak RM, Patel SA, Chu F, Coxson HO, Sharafkhaneh A, Elliott WM, Luketich JD, Sin DD, Hogg JC: The effect of small airway pathology on survival following lung volume reduction surgery (LVRS): [abstract]. Proc Am Thorac Soc. 2006, 3: A712-CrossRef
12.
go back to reference Regan EA, Hokanson JE, Murphy JR, Make B, Lynch DA, Beaty TH, Curran-Everett D, Silverman EK, Crapo JD: Genetic epidemiology of COPD (COPDGene) study design. COPD. 2010, 7: 32-43. 10.3109/15412550903499522.PubMedPubMedCentralCrossRef Regan EA, Hokanson JE, Murphy JR, Make B, Lynch DA, Beaty TH, Curran-Everett D, Silverman EK, Crapo JD: Genetic epidemiology of COPD (COPDGene) study design. COPD. 2010, 7: 32-43. 10.3109/15412550903499522.PubMedPubMedCentralCrossRef
13.
go back to reference ATS Committee on Proficiency Standards for Clinical Pulmonary Function Laboratories: ATS statement: guidelines for the six-minute walk test. Am J Respir Crit Care Med. 2002, 166: 111-117.CrossRef ATS Committee on Proficiency Standards for Clinical Pulmonary Function Laboratories: ATS statement: guidelines for the six-minute walk test. Am J Respir Crit Care Med. 2002, 166: 111-117.CrossRef
14.
go back to reference Nakano Y, Muro S, Sakai H, Niimi A, Kalloger SE, Mishima M, Pare PD: Computed tomographic measurements of airway dimensions and emphysema in smokers: correlation with lung function. Am J Respir Crit Care Med. 2000, 162: 1102-1108. 10.1164/ajrccm.162.3.9907120.PubMedCrossRef Nakano Y, Muro S, Sakai H, Niimi A, Kalloger SE, Mishima M, Pare PD: Computed tomographic measurements of airway dimensions and emphysema in smokers: correlation with lung function. Am J Respir Crit Care Med. 2000, 162: 1102-1108. 10.1164/ajrccm.162.3.9907120.PubMedCrossRef
15.
go back to reference Patel BD, Coxson HO, Pillai SG, Agusti AG, Calverley PM, Donner CF, Make BJ, Muller NL, Rennard SI, Vestbo J, Wouters EF, Hiorns MP, Nakano Y, Camp PG, Nasute Fauerbach PV, Screaton NJ, Campbell EJ, Anderson WH, Pare PD, Levy RD, Lake SL, Silverman EK, Lomas DA: Airway wall thickening and emphysema show independent familial aggregation in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2008, 178: 500-505. 10.1164/rccm.200801-059OC.PubMedCrossRef Patel BD, Coxson HO, Pillai SG, Agusti AG, Calverley PM, Donner CF, Make BJ, Muller NL, Rennard SI, Vestbo J, Wouters EF, Hiorns MP, Nakano Y, Camp PG, Nasute Fauerbach PV, Screaton NJ, Campbell EJ, Anderson WH, Pare PD, Levy RD, Lake SL, Silverman EK, Lomas DA: Airway wall thickening and emphysema show independent familial aggregation in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2008, 178: 500-505. 10.1164/rccm.200801-059OC.PubMedCrossRef
17.
go back to reference Seemungal TA, Donaldson GC, Bhowmik A, Jeffries DJ, Wedzicha JA: Time course and recovery of exacerbations in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2000, 161: 1608-1613. 10.1164/ajrccm.161.5.9908022.PubMedCrossRef Seemungal TA, Donaldson GC, Bhowmik A, Jeffries DJ, Wedzicha JA: Time course and recovery of exacerbations in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2000, 161: 1608-1613. 10.1164/ajrccm.161.5.9908022.PubMedCrossRef
18.
go back to reference Nakano Y, Muller NL, King GG, Niimi A, Kalloger SE, Mishima M, Pare PD: Quantitative assessment of airway remodeling using high-resolution CT. Chest. 2002, 122: 271S-275S.PubMedCrossRef Nakano Y, Muller NL, King GG, Niimi A, Kalloger SE, Mishima M, Pare PD: Quantitative assessment of airway remodeling using high-resolution CT. Chest. 2002, 122: 271S-275S.PubMedCrossRef
19.
go back to reference Vestbo J, Prescott E, Lange P: Association of chronic mucus hypersecretion with FEV1 decline and chronic obstructive pulmonary disease morbidity. Copenhagen City Heart Study Group. Am J Respir Crit Care Med. 1996, 153: 1530-1535. 10.1164/ajrccm.153.5.8630597.PubMedCrossRef Vestbo J, Prescott E, Lange P: Association of chronic mucus hypersecretion with FEV1 decline and chronic obstructive pulmonary disease morbidity. Copenhagen City Heart Study Group. Am J Respir Crit Care Med. 1996, 153: 1530-1535. 10.1164/ajrccm.153.5.8630597.PubMedCrossRef
20.
go back to reference Sherman CB, Xu X, Speizer FE, Ferris BG, Weiss ST, Dockery DW: Longitudinal lung function decline in subjects with respiratory symptoms. Am Rev Respir Dis. 1992, 146: 855-859. 10.1164/ajrccm/146.4.855.PubMedCrossRef Sherman CB, Xu X, Speizer FE, Ferris BG, Weiss ST, Dockery DW: Longitudinal lung function decline in subjects with respiratory symptoms. Am Rev Respir Dis. 1992, 146: 855-859. 10.1164/ajrccm/146.4.855.PubMedCrossRef
21.
go back to reference Achenbach T, Weinheimer O, Biedermann A, Schmitt S, Freudenstein D, Goutham E, Kunz RP, Buhl R, Dueber C, Heussel CP: MDCT assessment of airway wall thickness in COPD patients using a new method: correlations with pulmonary function tests. Eur Radiol. 2008, 18: 2731-2738. 10.1007/s00330-008-1089-4.PubMedCrossRef Achenbach T, Weinheimer O, Biedermann A, Schmitt S, Freudenstein D, Goutham E, Kunz RP, Buhl R, Dueber C, Heussel CP: MDCT assessment of airway wall thickness in COPD patients using a new method: correlations with pulmonary function tests. Eur Radiol. 2008, 18: 2731-2738. 10.1007/s00330-008-1089-4.PubMedCrossRef
22.
go back to reference Orlandi I, Moroni C, Camiciottoli G, Bartolucci M, Pistolesi M, Villari N, Mascalchi M: Chronic obstructive pulmonary disease: thin-section CT measurement of airway wall thickness and lung attenuation. Radiology. 2005, 234: 604-610. 10.1148/radiol.2342040013.PubMedCrossRef Orlandi I, Moroni C, Camiciottoli G, Bartolucci M, Pistolesi M, Villari N, Mascalchi M: Chronic obstructive pulmonary disease: thin-section CT measurement of airway wall thickness and lung attenuation. Radiology. 2005, 234: 604-610. 10.1148/radiol.2342040013.PubMedCrossRef
23.
go back to reference Gelb AF, Zamel N, Hogg JC, Muller NL, Schein MJ: Pseudophysiologic emphysema resulting from severe small-airways disease. Am J Respir Crit Care Med. 1998, 158: 815-819. 10.1164/ajrccm.158.3.9801045.PubMedCrossRef Gelb AF, Zamel N, Hogg JC, Muller NL, Schein MJ: Pseudophysiologic emphysema resulting from severe small-airways disease. Am J Respir Crit Care Med. 1998, 158: 815-819. 10.1164/ajrccm.158.3.9801045.PubMedCrossRef
24.
go back to reference Forey BA, Thornton AJ, Lee PN: Systematic review with meta-analysis of the epidemiological evidence relating smoking to COPD, chronic bronchitis and emphysema. BMC Pulm Med. 2011, 11: 36-10.1186/1471-2466-11-36. 2466-11-36PubMedPubMedCentralCrossRef Forey BA, Thornton AJ, Lee PN: Systematic review with meta-analysis of the epidemiological evidence relating smoking to COPD, chronic bronchitis and emphysema. BMC Pulm Med. 2011, 11: 36-10.1186/1471-2466-11-36. 2466-11-36PubMedPubMedCentralCrossRef
25.
go back to reference Trupin L, Earnest G, San Pedro M, Balmes JR, Eisner MD, Yelin E, Katz PP, Blanc PD: The occupational burden of chronic obstructive pulmonary disease. Eur Respir J. 2003, 22: 462-469. 10.1183/09031936.03.00094203.PubMedCrossRef Trupin L, Earnest G, San Pedro M, Balmes JR, Eisner MD, Yelin E, Katz PP, Blanc PD: The occupational burden of chronic obstructive pulmonary disease. Eur Respir J. 2003, 22: 462-469. 10.1183/09031936.03.00094203.PubMedCrossRef
26.
go back to reference Matheson MC, Benke G, Raven J, Sim MR, Kromhout H, Vermeulen R, Johns DP, Walters EH, Abramson MJ: Biological dust exposure in the workplace is a risk factor for chronic obstructive pulmonary disease. Thorax. 2005, 60: 645-651. 10.1136/thx.2004.035170.PubMedPubMedCentralCrossRef Matheson MC, Benke G, Raven J, Sim MR, Kromhout H, Vermeulen R, Johns DP, Walters EH, Abramson MJ: Biological dust exposure in the workplace is a risk factor for chronic obstructive pulmonary disease. Thorax. 2005, 60: 645-651. 10.1136/thx.2004.035170.PubMedPubMedCentralCrossRef
27.
go back to reference Ehrlich RI, White N, Norman R, Laubscher R, Steyn K, Lombard C, Bradshaw D: Predictors of chronic bronchitis in South African adults. Int J Tuberc Lung Dis. 2004, 8: 369-376.PubMed Ehrlich RI, White N, Norman R, Laubscher R, Steyn K, Lombard C, Bradshaw D: Predictors of chronic bronchitis in South African adults. Int J Tuberc Lung Dis. 2004, 8: 369-376.PubMed
28.
go back to reference Martinez CH, Kim V, Chen Y, Kazerooni EA, Murray S, Criner GJ, Curtis JL, Regan EA, Wan E, Hersh CP, Silverman EK, Crapo JD, Martinez FJ, Han MK, The Copdgene Investigators: The clinical impact of non-obstructive chronic bronchitis in current and former smokers. Respir Med. 2013, in press Martinez CH, Kim V, Chen Y, Kazerooni EA, Murray S, Criner GJ, Curtis JL, Regan EA, Wan E, Hersh CP, Silverman EK, Crapo JD, Martinez FJ, Han MK, The Copdgene Investigators: The clinical impact of non-obstructive chronic bronchitis in current and former smokers. Respir Med. 2013, in press
29.
go back to reference Barish CF, Wu WC, Castell DO: Respiratory complications of gastroesophageal reflux. Arch Intern Med. 1985, 145: 1882-1888. 10.1001/archinte.1985.00360100152025.PubMedCrossRef Barish CF, Wu WC, Castell DO: Respiratory complications of gastroesophageal reflux. Arch Intern Med. 1985, 145: 1882-1888. 10.1001/archinte.1985.00360100152025.PubMedCrossRef
30.
go back to reference Hurst JR, Vestbo J, Anzueto A, Locantore N, Mullerova H, Tal-Singer R, Miller B, Lomas DA, Agusti A, Macnee W, Calverley P, Rennard S, Wouters EF, Wedzicha JA, Evaluation Of Copd Longitudinally To Identify Predictive Surrogate Endpoints (Eclipse) Investigators: Susceptibility to exacerbation in chronic obstructive pulmonary disease. N Engl J Med. 2010, 363: 1128-1138. 10.1056/NEJMoa0909883.PubMedCrossRef Hurst JR, Vestbo J, Anzueto A, Locantore N, Mullerova H, Tal-Singer R, Miller B, Lomas DA, Agusti A, Macnee W, Calverley P, Rennard S, Wouters EF, Wedzicha JA, Evaluation Of Copd Longitudinally To Identify Predictive Surrogate Endpoints (Eclipse) Investigators: Susceptibility to exacerbation in chronic obstructive pulmonary disease. N Engl J Med. 2010, 363: 1128-1138. 10.1056/NEJMoa0909883.PubMedCrossRef
31.
go back to reference Ramos F, Krahnke JS, Harnden SM, Connett J, Albert RK, Criner GJ: Acute exacerbation of chronic obstructive pulmonary disease in patients with and without history of gastroesophageal reflux disease: [abstract]. Am J Respir Crit Care Med. 2013, 187: A5704- Ramos F, Krahnke JS, Harnden SM, Connett J, Albert RK, Criner GJ: Acute exacerbation of chronic obstructive pulmonary disease in patients with and without history of gastroesophageal reflux disease: [abstract]. Am J Respir Crit Care Med. 2013, 187: A5704-
32.
go back to reference Desai P, Kim V: Management of chronic bronchitis in chronic obstructive pulmonary disease. US Resp Rev. 2011, 7: 102-106. Desai P, Kim V: Management of chronic bronchitis in chronic obstructive pulmonary disease. US Resp Rev. 2011, 7: 102-106.
33.
go back to reference de Oca MM, Halbert RJ, Lopez MV, Perez-Padilla R, Talamo C, Moreno D, Muino A, Jardim JR, Valdivia G, Pertuze J, Meneze AM: The chronic bronchitis phenotype in subjects with and without COPD: the PLATINO study. Eur Respir J. 2012, 40: 28-36. 10.1183/09031936.00141611.PubMedCrossRef de Oca MM, Halbert RJ, Lopez MV, Perez-Padilla R, Talamo C, Moreno D, Muino A, Jardim JR, Valdivia G, Pertuze J, Meneze AM: The chronic bronchitis phenotype in subjects with and without COPD: the PLATINO study. Eur Respir J. 2012, 40: 28-36. 10.1183/09031936.00141611.PubMedCrossRef
34.
go back to reference Speizer FE, Fay ME, Dockery DW, Ferris BG: Chronic obstructive pulmonary disease mortality in six U.S. cities. Am Rev Respir Dis. 1989, 140: S49-55. 10.1164/ajrccm/140.3_Pt_2.S49.PubMedCrossRef Speizer FE, Fay ME, Dockery DW, Ferris BG: Chronic obstructive pulmonary disease mortality in six U.S. cities. Am Rev Respir Dis. 1989, 140: S49-55. 10.1164/ajrccm/140.3_Pt_2.S49.PubMedCrossRef
35.
go back to reference Kim V, Sternberg AL, Washko GR, Make BJ, Han MK, Martinez FJ, Criner GJ: Severe chronic bronchitis in advanced emphysema increases mortality and hospitalizations. J COPD. 2013, 10: 667-678. 10.3109/15412555.2013.827166.CrossRef Kim V, Sternberg AL, Washko GR, Make BJ, Han MK, Martinez FJ, Criner GJ: Severe chronic bronchitis in advanced emphysema increases mortality and hospitalizations. J COPD. 2013, 10: 667-678. 10.3109/15412555.2013.827166.CrossRef
Metadata
Title
Clinical and computed tomographic predictors of chronic bronchitis in COPD: a cross sectional analysis of the COPDGene study
Authors
Victor Kim
Adam Davey
Alejandro P Comellas
Meilan K Han
George Washko
Carlos H Martinez
David Lynch
Jin Hwa Lee
Edwin K Silverman
James D Crapo
Barry J Make
Gerard J Criner
The COPDGene® Investigators
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Respiratory Research / Issue 1/2014
Electronic ISSN: 1465-993X
DOI
https://doi.org/10.1186/1465-9921-15-52

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