Login Register Cart 0
Generic placeholder image

Current Respiratory Medicine Reviews

Editor-in-Chief

ISSN (Print): 1573-398X
ISSN (Online): 1875-6387

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Association of Serum Malondialdehyde and C-reactive Protein Levels with Exacerbations of Chronic Obstructive Pulmonary Disease

Author(s): Amir Behnam Kharazmi, Atefeh Abedini*, Arda Kiani, Shahriar Barouti and Shooka Mohammadi

Volume 18, Issue 1, 2022

Published on: 31 January, 2022

Page: [34 - 43] Pages: 10

DOI: 10.2174/1573398X18666220104143532

Price: $65

Abstract

Background: Chronic obstructive pulmonary disease (COPD) is related to oxidant/antioxidant imbalance and systemic inflammation.

Objective: This study was conducted to evaluate associations of serum levels of C-reactive protein (CRP) and malondialdehyde (MDA) with the severity and exacerbations of COPD.

Methods: A matched case-control study was performed among 200 COPD patients (100 cases and 100 controls) who were referred to Masih Daneshvari Hospital in Tehran, Iran. Cases were exacerbators with equal to or greater than two ambulatory exacerbations or one hospitalization; controls were non-exacerbators who had one/no ambulatory exacerbation during the preceding 12 months. Blood samples were collected for CRP, MDA, and erythrocyte sedimentation rate (ESR) analysis. In addition, spirometry, the COPD assessment test (CAT) score, the modified Medical Research Council (mMRC) dyspnea scale, and the BODEx index were applied.

Results: The mean (SD) age of the patients was 65.31 (8.46) years. Those with exacerbations had significantly lower FEV1 and higher CRP, MDA, ESR, BMI, BODEx index, CAT, and mMRC scores compared to non-exacerbators. There were significant differences in CRP, MDA, ESR, FVC, FEV1, FEV1/FVC, BMI, BODEx index, mMRC, and CAT scores between the GOLD group. Moreover, multivariate analysis showed that higher levels of CRP (OR=0.61, p=0.023), MDA (OR=0.28, p=0.001), ESR (OR=0.86, p=0.029), CAT score (OR=0.84, p=0.012), BODEx index (OR=0.89, p <0.001), BMI (OR=0.42, p <0.001), and lower FEV1% (OR=0.77, p <0.001) were independent risk factors for frequent exacerbations.

Conclusion: In conclusion, elevated serum MDA and CRP levels in combination may serve as prognostic indicators of the severity and exacerbation of COPD.

Keywords: Exacerbations, MDA, CRP, CAT score, BODEx, mMRC, COPD.

« Previous Next »
Graphical Abstract

[1]
Paliogiannis P, Fois AG, Sotgia S, et al. The neutrophil-to-lymphocyte ratio as a marker of chronic obstructive pulmonary disease and its exacerbations: A systematic review and meta-analysis. Eur J Clin Invest 2018; 48(8): e12984.
[http://dx.doi.org/10.1111/eci.12984] [PMID: 29924383]
[2]
Aydemir Y, Aydemir Ö, Şengül A, et al. Comparison of oxidant/antioxidant balance in COPD and non-COPD smokers. Heart Lung 2019; 48(6): 566-9.
[http://dx.doi.org/10.1016/j.hrtlng.2019.07.005] [PMID: 31371032]
[3]
Pandey S, Garg R, Kant S, Gaur P, Vitamin D. C-reactive protein, and oxidative stress markers in chronic obstructive pulmonary disease. Tzu-Chi Med J 2019; 33(1): 80-6.
[http://dx.doi.org/10.4103/tcmj.tcmj_198_19] [PMID: 33505883]
[4]
Cho WK, Lee CG, Kim LK. COPD as a disease of immunosenescence. Yonsei Med J 2019; 60(5): 407-13.
[http://dx.doi.org/10.3349/ymj.2019.60.5.407] [PMID: 31016901]
[5]
Barnes PJ. Inflammatory mechanisms in patients with chronic obstructive pulmonary disease. J Allergy Clin Immunol 2016; 138(1): 16-27.
[http://dx.doi.org/10.1016/j.jaci.2016.05.011] [PMID: 27373322]
[6]
López Caro JC, Santibáñez M, García Rivero JL, et al. Sputum microbiome dynamics in chronic obstructive pulmonary disease patients during an exacerbation event and post-stabilization. Respiration 2019; 98(5): 447-54.
[http://dx.doi.org/10.1159/000501988] [PMID: 31437842]
[7]
Prasad B. Chronic obstructive pulmonary disease (COPD). Int J Pharm Res Technol 2020; 10(1): 67-71.
[8]
Herse F, Kiljander T, Lehtimäki L. Annual costs of chronic obstructive pulmonary disease in Finland during 1996-2006 and a prediction model for 2007-2030. NPJ Prim Care Respir Med 2015; 25(1): 15015.
[http://dx.doi.org/10.1038/npjpcrm.2015.15] [PMID: 25811648]
[9]
Portegies ML, Lahousse L, Joos GF, et al. Chronic obstructive pulmonary disease and the risk of stroke. The Rotterdam Study. Am J Respir Crit Care Med 2016; 193(3): 251-8.
[http://dx.doi.org/10.1164/rccm.201505-0962OC] [PMID: 26414484]
[10]
Hashemi SY, Momenabadi V, Faramarzi A, Kiani A. Trends in burden of chronic obstructive pulmonary disease in Iran, 1995-2015: findings from the global burden of disease study. Arch Public Health 2020; 78: 45.
[http://dx.doi.org/10.1186/s13690-020-00426-x] [PMID: 32509302]
[11]
Bai JW, Chen XX, Liu S, Yu L, Xu JF. Smoking cessation affects the natural history of COPD. Int J Chron Obstruct Pulmon Dis 2017; 12: 3323-8.
[http://dx.doi.org/10.2147/COPD.S150243] [PMID: 29180862]
[12]
Pandey S, Garg R, Kant S, Verma AK, Ahmad I, Ahmad MK. Serum CRP levels in healthy controls and stable COPD and its correlation with different stages of COPD in north Indian population. Int J Res Dev Pharm Life Sci 2018; 7(1): 2918-23.
[http://dx.doi.org/10.21276/IJRDPL.2278-0238.2018.7(1).2918-2923]
[13]
Vogelmeier CF, Criner GJ, Martinez FJ, et al. Global strategy for the diagnosis, management, and prevention of chronic obstructive lung disease 2017 report. GOLD executive summary. Am J Respir Crit Care Med 2017; 195(5): 557-82.
[http://dx.doi.org/10.1164/rccm.201701-0218PP] [PMID: 28128970]
[14]
Shin B, Kim S-H, Yong SJ, et al. Early readmission and mortality in acute exacerbation of chronic obstructive pulmonary disease with community-acquired pneumonia. Chron Respir Dis 2019; 16: 1479972318809480.
[http://dx.doi.org/10.1177/1479972318809480] [PMID: 30428701]
[15]
Miravitlles M, Anzueto A. A new two-step algorithm for the treatment of COPD. Eur Respir J 2017; 49(2): 1602200.
[http://dx.doi.org/10.1183/13993003.02200-2016] [PMID: 28179443]
[16]
Ritchie AI, Wedzicha JA. Definition, causes, pathogenesis, and consequences of chronic obstructive pulmonary disease exacerbations. Clin Chest Med 2020; 41(3): 421-38.
[http://dx.doi.org/10.1016/j.ccm.2020.06.007] [PMID: 32800196]
[17]
Anzueto A, Miravitlles M. Chronic obstructive pulmonary disease exacerbations: a need for action. Am J Med 2018; 131(9S): 15-22.
[http://dx.doi.org/10.1016/j.amjmed.2018.05.003] [PMID: 29777660]
[18]
Halpin DM, Miravitlles M, Metzdorf N, Celli B. Impact and prevention of severe exacerbations of COPD: a review of the evidence. Int J Chron Obstruct Pulmon Dis 2017; 12: 2891-908.
[http://dx.doi.org/10.2147/COPD.S139470] [PMID: 29062228]
[19]
Zinellu E, Zinellu A, Fois AG, et al. Oxidative stress biomarkers in chronic obstructive pulmonary disease exacerbations: a systematic review. Antioxidants 2021; 10(5): 710.
[http://dx.doi.org/10.3390/antiox10050710] [PMID: 33946941]
[20]
Mendy A, Forno E, Niyonsenga T, Gasana J. Blood biomarkers as predictors of long-term mortality in COPD. Clin Respir J 2018; 12(5): 1891-9.
[http://dx.doi.org/10.1111/crj.12752] [PMID: 29227024]
[21]
Horita N, Kaneko T. Assessment of Inflammation in COPD: Are There any Biomarkers that Can be Used to Assess Pulmonary and Systemic Inflammation? InChronic Obstructive Pulmonary Disease. Singapore: Springer Press 2017; pp. 135-58.
[22]
Nuñez A, Marras V, Harlander M, et al. Association between routine blood biomarkers and clinical phenotypes and exacerbations in chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis 2020; 15: 681-90.
[http://dx.doi.org/10.2147/COPD.S240720] [PMID: 32280207]
[23]
Ayala A, Muñoz MF, Argüelles S. Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid Med Cell Longev 2014; 2014: 360438.
[http://dx.doi.org/10.1155/2014/360438] [PMID: 24999379]
[24]
Cui X, Gong J, Han H, et al. Relationship between free and total malondialdehyde, a well-established marker of oxidative stress, in various types of human biospecimens. J Thorac Dis 2018; 10(5): 3088-97.
[http://dx.doi.org/10.21037/jtd.2018.05.92] [PMID: 29997978]
[25]
Zinellu E, Zinellu A, Fois AG, et al. Reliability and usefulness of different biomarkers of oxidative stress in chronic obstructive pulmonary disease. Oxid Med Cell Longev 2020; 2020: 4982324.
[http://dx.doi.org/10.1155/2020/4982324] [PMID: 32509143]
[26]
Bajpai J, Prakash V, Kant S, et al. Study of oxidative stress biomarkers in chronic obstructive pulmonary disease and their correlation with disease severity in north Indian population cohort. Lung India 2017; 34(4): 324-9.
[http://dx.doi.org/10.4103/lungindia.lungindia_205_16] [PMID: 28671162]
[27]
Tian W, Jiang W, Yao J, et al. Predictors of mortality in hospitalized COVID-19 patients: A systematic review and meta-analysis. J Med Virol 2020; 92(10): 1875-83.
[http://dx.doi.org/10.1002/jmv.26050] [PMID: 32441789]
[28]
Saad AB, Migaou A, Mhamed SC, Fahem N, Rouatbi N, Joobeur S. Relationship between CRP levels and the severity of COPD acute exacerbations among group D COPD patients. Eur Respiratory Soc 2020; 56: 2443.
[29]
Khan A, Khan S, Khan MM, Alam R, Srivastava V. Comparative study of malondialdehyde and superoxide dismutase in diagnosed COPD patients. Indian J Basic Appl Med Res 2019; 8(2): 189-96.
[30]
Xiong W, Xu M, Zhao Y, Wu X, Pudasaini B, Liu JM. Can we predict the prognosis of COPD with a routine blood test? Int J Chron Obstruct Pulmon Dis 2017; 12: 615-25.
[http://dx.doi.org/10.2147/COPD.S124041] [PMID: 28243079]
[31]
Bestall JC, Paul EA, Garrod R, Garnham R, Jones PW, Wedzicha JA. Usefulness of the Medical Research Council (MRC) dyspnoea scale as a measure of disability in patients with chronic obstructive pulmonary disease. Thorax 1999; 54(7): 581-6.
[http://dx.doi.org/10.1136/thx.54.7.581] [PMID: 10377201]
[32]
Jones PW, Harding G, Berry P, Wiklund I, Chen WH, Kline Leidy N. Development and first validation of the COPD Assessment Test. Eur Respir J 2009; 34(3): 648-54.
[http://dx.doi.org/10.1183/09031936.00102509] [PMID: 19720809]
[33]
Soler-Cataluña JJ, Martínez-García MÁ, Sánchez LS, Tordera MP, Sánchez PR. Severe exacerbations and BODE index: two independent risk factors for death in male COPD patients. Respir Med 2009; 103(5): 692-9.
[http://dx.doi.org/10.1016/j.rmed.2008.12.005] [PMID: 19131231]
[34]
Singh D, Agusti A, Anzueto A, et al. Global strategy for the diagnosis, management, and prevention of chronic obstructive lung disease: the GOLD science committee report 2019. Eur Respir J 2019; 53(5): 1900164.
[http://dx.doi.org/10.1183/13993003.00164-2019] [PMID: 30846476]
[35]
Lim JU, Lee JH, Kim JS, et al. Comparison of world health organization and asia-pacific body mass index classifications in COPD patients. Int J Chron Obstruct Pulmon Dis 2017; 12: 2465-75.
[http://dx.doi.org/10.2147/COPD.S141295] [PMID: 28860741]
[36]
Wedzicha JA, Miravitlles M, Hurst JR, et al. Management of COPD exacerbations: A European respiratory society/American thoracic society guideline. Eur Respir J 2017; 49(3): 1600791.
[http://dx.doi.org/10.1183/13993003.00791-2016] [PMID: 28298398]
[37]
Ghaffaripour H, Mirkarimi M, Hassanzad M, Boloursaz M, Mohammadi S. Evaluation of inflammatory biomarkers in Iranian patients with cystic fibrosis. Curr Respir Med Rev 2020; 16(3): 184-92.
[http://dx.doi.org/10.2174/1573398X16999201026223411]
[38]
Tan DBA, Armitage J, Teo T-H, Ong NE, Shin H, Moodley YP. Elevated levels of circulating exosome in COPD patients are associated with systemic inflammation. Respir Med 2017; 132: 261-4.
[http://dx.doi.org/10.1016/j.rmed.2017.04.014] [PMID: 28476471]
[39]
Groenewegen KH, Postma DS, Hop WC, Wielders PL, Schlösser NJ, Wouters EF. COSMIC Study Group. Increased systemic inflammation is a risk factor for COPD exacerbations. Chest 2008; 133(2): 350-7.
[http://dx.doi.org/10.1378/chest.07-1342] [PMID: 18198263]
[40]
Wang ZL. Evolving role of systemic inflammation in comorbidities of chronic obstructive pulmonary disease. Chin Med J (Engl) 2010; 123(23): 3467-78.
[PMID: 22166533]
[41]
Hoogendoorn M, Hoogenveen RT, Rutten-van Mölken MP, Vestbo J, Feenstra TL. Case fatality of COPD exacerbations: a meta-analysis and statistical modelling approach. Eur Respir J 2011; 37(3): 508-15.
[http://dx.doi.org/10.1183/09031936.00043710] [PMID: 20595157]
[42]
Anzueto A. Impact of exacerbations on COPD. Eur Respir Rev 2010; 19(116): 113-8.
[http://dx.doi.org/10.1183/09059180.00002610] [PMID: 20956179]
[43]
Wedzicha JA, Rabe KF, Martinez FJ, et al. Efficacy of roflumilast in the COPD frequent exacerbator phenotype. Chest 2013; 143(5): 1302-11.
[http://dx.doi.org/10.1378/chest.12-1489] [PMID: 23117188]
[44]
Sadatsafavi M, McCormack J, Petkau J, Lynd LD, Lee TY, Sin DD. Should the number of acute exacerbations in the previous year be used to guide treatments in COPD? Eur Respir J 2021; 57(2): 2002122.
[http://dx.doi.org/10.1183/13993003.02122-2020] [PMID: 32855228]
[45]
Guerra B, Gaveikaite V, Bianchi C, Puhan MA. Prediction models for exacerbations in patients with COPD. Eur Respir Rev 2017; 26(143): 160061.
[http://dx.doi.org/10.1183/16000617.0061-2016] [PMID: 28096287]
[46]
Zhang Y, Bunjhoo H, Xiong W, Xu Y, Yang D. Association between C-reactive protein concentration and chronic obstructive pulmonary disease: a systematic review and meta-analysis. J Int Med Res 2012; 40(5): 1629-35.
[http://dx.doi.org/10.1177/030006051204000501] [PMID: 23206444]
[47]
Heidari B. The importance of C-reactive protein and other inflammatory markers in patients with chronic obstructive pulmonary disease. Caspian J Intern Med 2012; 3(2): 428-35.
[PMID: 24358439]
[48]
Jing Z, Chun C, Ning S, Hong Z, Bei H, Wan-Zhen Y. Systemic inflammatory marker CRP was better predictor of readmission for AECOPD than sputum inflammatory markers. Arch Bronconeumol 2016; 52(3): 138-44.
[http://dx.doi.org/10.1016/j.arbr.2015.05.029] [PMID: 26002550]
[49]
Leuzzi G, Galeone C, Taverna F, Suatoni P, Morelli D, Pastorino U. C-reactive protein level predicts mortality in COPD: a systematic review and meta-analysis. Eur Respir Rev 2017; 26(143): 160070.
[http://dx.doi.org/10.1183/16000617.0070-2016] [PMID: 28143876]
[50]
Garcia-Rio F, Miravitlles M, Soriano JB, et al. EPI-SCAN Steering Committee. Systemic inflammation in chronic obstructive pulmonary disease: a population-based study. Respir Res 2010; 11(1): 63.
[http://dx.doi.org/10.1186/1465-9921-11-63] [PMID: 20500811]
[51]
Hurst JR, Donaldson GC, Perera WR, et al. Use of plasma biomarkers at exacerbation of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2006; 174(8): 867-74.
[http://dx.doi.org/10.1164/rccm.200604-506OC] [PMID: 16799074]
[52]
Perera WR, Hurst JR, Wilkinson TM, et al. Inflammatory changes, recovery and recurrence at COPD exacerbation. Eur Respir J 2007; 29(3): 527-34.
[http://dx.doi.org/10.1183/09031936.00092506] [PMID: 17107990]
[53]
Tofan F, Rahimi-Rad MH, Rasmi Y, Rahimirad S. High sensitive C-reactive protein for prediction of adverse outcome in acute exacerbation of chronic obstructive pulmonary disease. Pneumologia 2012; 61(3): 160-2.
[PMID: 23175870]
[54]
Kluchová Z, Petrášová D, Joppa P, Dorková Z, Tkáčová R. The association between oxidative stress and obstructive lung impairment in patients with COPD. Physiol Res 2007; 56(1): 51-6.
[http://dx.doi.org/10.33549/physiolres.930884] [PMID: 16497100]
[55]
Voskresenska N, Voicehovska J, Vojcehovska A, Orlikovs G, Skesters A. Malondialdehyde level in chronic obstructive pulmonary disease exacerbations. Eur Respir Soc 2015; 46: OA2920.
[http://dx.doi.org/10.1183/13993003.congress-2015.OA2920]
[56]
Zeng M, Li Y, Jiang Y, Lu G, Huang X, Guan K. Local and systemic oxidative stress and glucocorticoid receptor levels in chronic obstructive pulmonary disease patients. Can Respir J 2013; 20(1): 35-41.
[http://dx.doi.org/10.1155/2013/985382] [PMID: 23457673]
[57]
Lee S-D, Huang M-S, Kang J, et al. Investigators of the Predictive Ability of CAT in Acute Exacerbations of COPD (PACE) Study. The COPD assessment test (CAT) assists prediction of COPD exacerbations in high-risk patients. Respir Med 2014; 108(4): 600-8.
[http://dx.doi.org/10.1016/j.rmed.2013.12.014] [PMID: 24456695]
[58]
Mackay AJ, Donaldson GC, Patel AR, Jones PW, Hurst JR, Wedzicha JA. Usefulness of the chronic obstructive pulmonary disease assessment test to evaluate severity of COPD exacerbations. Am J Respir Crit Care Med 2012; 185(11): 1218-24.
[http://dx.doi.org/10.1164/rccm.201110-1843OC] [PMID: 22281834]
[59]
Miravitlles M, García-Sidro P, Fernández-Nistal A, Buendía MJ, Espinosa de los Monteros MJ, Molina J. Course of COPD assessment test (CAT) and clinical COPD questionnaire (CCQ) scores during recovery from exacerbations of chronic obstructive pulmonary disease. Health Qual Life Outcomes 2013; 11(1): 147.
[http://dx.doi.org/10.1186/1477-7525-11-147] [PMID: 23987232]
[60]
Feliz-Rodriguez D, Zudaire S, Carpio C, et al. Evolution of the COPD Assessment Test score during chronic obstructive pulmonary disease exacerbations: determinants and prognostic value. Can Respir J 2013; 20(5): e92-7.
[http://dx.doi.org/10.1155/2013/398120] [PMID: 24093119]
[61]
Zhou A, Zhou Z, Peng Y, Zhao Y, Duan J, Chen P. The role of CAT in evaluating the response to treatment of patients with AECOPD. Int J Chron Obstruct Pulmon Dis 2018; 13: 2849-58.
[http://dx.doi.org/10.2147/COPD.S175085] [PMID: 30237709]
[62]
Marin JM, Carrizo SJ, Casanova C, et al. Prediction of risk of COPD exacerbations by the BODE index. Respir Med 2009; 103(3): 373-8.
[http://dx.doi.org/10.1016/j.rmed.2008.10.004] [PMID: 19013781]
[63]
Ong K-C, Earnest A, Lu S-J. A multidimensional grading system (BODE index) as predictor of hospitalization for COPD. Chest 2005; 128(6): 3810-6.
[http://dx.doi.org/10.1378/chest.128.6.3810] [PMID: 16354849]
[64]
Cote CG, Dordelly LJ, Celli BR. Impact of COPD exacerbations on patient-centered outcomes. Chest 2007; 131(3): 696-704.
[http://dx.doi.org/10.1378/chest.06-1610] [PMID: 17356082]
[65]
Lambert AA, Putcha N, Drummond MB, et al. COPDGene Investigators. Obesity is associated with increased morbidity in moderate to severe COPD. Chest 2017; 151(1): 68-77.
[http://dx.doi.org/10.1016/j.chest.2016.08.1432] [PMID: 27568229]
[66]
Cecere LM, Littman AJ, Slatore CG, et al. Obesity and COPD: associated symptoms, health-related quality of life, and medication use. COPD 2011; 8(4): 275-84.
[http://dx.doi.org/10.3109/15412555.2011.586660] [PMID: 21809909]
[67]
Wei Y-F, Tsai Y-H, Wang C-C, Kuo P-H. Impact of overweight and obesity on acute exacerbations of COPD - subgroup analysis of the Taiwan Obstructive Lung Disease cohort. Int J Chron Obstruct Pulmon Dis 2017; 12: 2723-9.
[http://dx.doi.org/10.2147/COPD.S138571] [PMID: 28979114]
[68]
Carroll JF, Chiapa AL, Rodriquez M, et al. Visceral fat, waist circumference, and BMI: impact of race/ethnicity. Obesity (Silver Spring) 2008; 16(3): 600-7.
[http://dx.doi.org/10.1038/oby.2007.92] [PMID: 18239557]
[69]
Ischaki E, Papatheodorou G, Gaki E, Papa I, Koulouris N, Loukides S. Body mass and fat-free mass indices in COPD: relation with variables expressing disease severity. Chest 2007; 132(1): 164-9.
[http://dx.doi.org/10.1378/chest.06-2789] [PMID: 17505043]
[70]
Skyba P, Kluchova Z, Joppa P, Petrasova D, Tkacova R. Nutritional status in relation to respiratory impairment and systemic inflammation in patients with acute exacerbations of COPD. Med Sci Monit 2009; 15(10): CR528-33.
[PMID: 19789512]
[71]
Pinto-Plata VM, Müllerova H, Toso JF, et al. C-reactive protein in patients with COPD, control smokers and non-smokers. Thorax 2006; 61(1): 23-8.
[http://dx.doi.org/10.1136/thx.2005.042200] [PMID: 16143583]
[72]
Karadag F, Kirdar S, Karul AB, Ceylan E. The value of C-reactive protein as a marker of systemic inflammation in stable chronic obstructive pulmonary disease. Eur J Intern Med 2008; 19(2): 104-8.
[http://dx.doi.org/10.1016/j.ejim.2007.04.026] [PMID: 18249305]
[73]
Broekhuizen R, Wouters EF, Creutzberg EC, Schols AM. Raised CRP levels mark metabolic and functional impairment in advanced COPD. Thorax 2006; 61(1): 17-22.
[http://dx.doi.org/10.1136/thx.2005.041996] [PMID: 16055618]
[74]
Breyer M-K, Spruit MA, Celis AP, Rutten EP, Janssen PP, Wouters EF. CIRO Network. Highly elevated C-reactive protein levels in obese patients with COPD: a fat chance? Clin Nutr 2009; 28(6): 642-7.
[http://dx.doi.org/10.1016/j.clnu.2009.05.005] [PMID: 19540024]
[75]
Tommola M, Ilmarinen P, Tuomisto LE, et al. Differences between asthma-COPD overlap syndrome and adult-onset asthma. Eur Respir J 2017; 49(5): 1602383.
[http://dx.doi.org/10.1183/13993003.02383-2016] [PMID: 28461298]
[76]
Gonçalves I, Guimarães MJ, van Zeller M, Menezes F, Moita J, Simão P. GI DPOC-Grupo de Interesse na Doença Pulmonar Obstrutiva Crónica. Clinical and molecular markers in COPD. Pulmonology 2018; 24(4): 250-9.
[http://dx.doi.org/10.1016/j.pulmoe.2018.02.005] [PMID: 29898875]

Rights & Permissions Print Cite
Article Metrics
15
1
© 2024 Bentham Science Publishers | Privacy Policy