Dynamics of exhaled breath temperature after smoking a cigarette and its association with lung function changes predictive of COPD risk in smokers: a cross-sectional study

  • Ivana Huljev Šipoš Department of Pulmonology, General Hospital Šibenik, Croatia
  • Slavica Labor Department of Pulmonology, University Hospital Center Osijek, Croatia; Faculty of Medicine, J.J. Strossmayer University of Osijek, Croatia, Osijek, Croatia
  • Iva Jurić Department of Cardiology, University Hospital Center Osijek, Croatia
  • Davor Plavec Dječja bolnica Srebrnjak Medicinski fakultet Sveučilišta JJ Strossmayer Osijek
  • Kristian Vlahoviček Bioinformatics Group, Division of Molecular Biology, Department of Biology, Faculty of Science, University of Zagreb, Zagreb, Croatia
  • Siniša Bogović Department of Cardiac Surgery, University Hospital Center Osijek, Croatia
  • Justinija Pavkov Vukelić Department of Medicine, County General Hospital Našice, Našice, Croatia
  • Marina Labor Department of Pulmonology, University Hospital Center Osijek, Croatia; Faculty of Medicine, J.J. Strossmayer University of Osijek, Croatia, Osijek, Croatia
Keywords: EBT, cigarette smoke toxicity, cigarette smoking, COPD risk, small airway dysfunction


Exhaled breath temperature (EBT) is a biomarker of inflammation and vascularity of the airways already shown to predict incident COPD. This cross-sectional study was aimed to assess the potential of EBT in identifying "healthy" smokers susceptible to cigarette smoke toxicity of the airways and to the risk of developing COPD by analysing the dynamics of EBT after smoking a cigarette and its associations with their demographics (age, smoking burden) and lung function. The study included 55 current smokers of both sexes, 29–62 years of age, with median smoking exposure of 15 (10–71.8) pack-years. EBT was measured at baseline and 5, 15, 30, 45, and 60 min after smoking a single cigarette. Lung function was measured with spirometry followed by a bronchodilator test. To compare changes in EBT between repeated measurements we used the analysis of variance and the area under the curve (EBTAUC) as a dependent variable. Multivariate regression analysis was used to look for associations with patient characteristics and lung function in particular. The average (±SD) baseline EBT was 33.42±1.50 °C. The highest significant increase to 33.84 (1.25) °C was recorded 5 min after the cigarette was smoked (p=0.003), and it took one hour for it to return to the baseline. EBTAUC showed significant repeatability (ICC=0.85, p<0.001) and was significantly associated with age, body mass index, number of cigarettes smoked a day, baseline EBT, and baseline FEF75 (R2=0.39, p<0.001 for the model). Our results suggest that EBT after smoking a single cigarette could be used as early risk predictor of changes associated with chronic cigarette smoke exposure.


Mathers CD, Loncar D. Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med 2006;3:e442. doi: 10.1371/journal.pmed.0030442

Singh D. Small airway disease in patients with cronic obstructive pulmonary disease. Tuberc Respir Dis (Seoul) 2017;80:317-24. doi: 10.4046/trd.2017.0080

Popov TA, Kralimarkova TZ, Labor M, Plavec D. The added value of exhaled breath temperature in respiratory medicine. J Breath Res 2017;11:034001. doi: 10.1088/1752-7163/aa7801

Labor M, Vrbica Ž, Gudelj I, Labor S, Jurić I, Plavec D. Exhaled breath temperature as a novel marker of future development of COPD: results of a follow-up study in smokers. COPD 2016;13:741-9. doi: 10.3109/15412555.2016.1164129

Vrbica Ž, Labor M, Gudelj I, Labor S, Jurić I, Plavec D; MARKO study group. Early detection of COPD patients in GOLD 0 population: an observational non-interventional cohort study - MARKO study. BMC Pulm Med 2017;17:36. doi: 10.1186/s12890-017-0378-6

Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, Crapo R, Enright P, van der Grinten CP, Gustafsson P, Jensen R, Johnson DC, MacIntyre N, McKay R, Navajas D, Pedersen OF, Pellegrino R, Viegi G, Wanger J; ATS/ERS Task Force. Standardisation of spirometry. Eur Resp J 2005;26:319-38. doi: 10.1183/09031936.05.00034805

Quanjer PH, Tammeling GJ, Cotes JE, Pedersen OF, Peslin R, Yernault JC. Lung volumes and forced ventilatory flows. Report Working Party Standardization of Lung Function Tests, European Community for Steel and Coal. Official Statement of the European Respiratory Society. Eur Respir J 1993;16(Suppl 6):5-40. doi: 10.1183/09041950.005s1693

Quanjer PH, Stanojevic S, Cole TJ, Baur X, Hall GL, Culver BH, Enright PL, Hankinson JL, Ip MS, Zheng J, Stocks J; ERS Global Lung Function Initiative. Multi-ethnic reference values for spirometry for the 3-95-yr age range: the global lung function 2012 equations. Eur Resp J 2012;40:1324-43. doi: 10.1183/09031936.00080312

Popov TA, Dunev S, Kralimarkova TZ, Kraeva S, DuBuske LM. Evaluation of a simple, potentially individual device for exhaled breath temperature measurement. Resp Med 2007;101:2044-50. doi: 10.1016/j.rmed.2007.06.005

Popov TA, Kralimarkova TZ, Dimitrov DV. Measurement of exhaled breath temperature in science and clinical practice. Breathe 2012;8:186-92. doi: 10.1183/20734735.021811

Rodgman A, Perfetti TA. The Chemical Components of Tobacco and Tobacco Smoke. Boca Raton (FL): CRC Press; 2009.

Tuder RM, Yoshida T, Fijalkowka I, Biswal S, Petrache I. Role of lung maintenance program in the heterogeneity of lung destruction in emphysema. Proc Am Thorac Soc 2006;3:673-9. doi: 10.1513/pats.200605-124SF

Tuder RM, Yoshida T. Stress responses affecting homeostasis of the alveolar capillary unit. Proc Am Thorac Soc 2011;8:485-91. doi: 10.1513/pats.201103-029MW

McCullagh A, Rosenthal M, Wanner A, Hurtado A, Padley S, Bush A. The bronchial circulation-worth a closer look: a review of the relationship between the bronchial vasculature and airway inflammation. Pediatr Pulmonol 2010;45:1-13. doi: 10.1002/ppul.21135

Baile EM, Dahlby RW, Wiggs BR, Paré PD. Role of tracheal and bronchial circulation in respiratory heat exchange. J Appl Physiol (1985) 1985;58:217-22. doi: 10.1152/jappl.1985.58.1.217

Serikov VB, Fleming NW. Pulmonary and bronchial circulations: contributions to heat and water exchange in isolated lungs. J Appl Physiol (1985) 2001;91:1977-85. doi: 10.1152/jappl.2001.91.5.1977

McFadden ER Jr, Pichurko BM, Bowman KF, Ingenito E, Burns S, Dowling N, Solway J. Thermal mapping of the airways in humans. J Appl Physiol (1985) 1985;58:564-70. doi: 10.1152/jappl.1985.58.2.564

Reid A, Heard BE. Preliminary studies of human pulmonary capillaries by India ink injection. Med Thorac 1962;19:215-9. doi: 10.1159/000192221

Cudkowicz L, Armstrong JB. The bronchial arteries in pulmonary emphysema. Thorax 1953;8:46-58. doi: 10.1136/thx.8.1.46

Hashimoto M, Tanaka H, Abe S. Quantitative analysis of bronchial wall vascularity in the medium and small airways of patients with asthma and COPD. Chest 2005;127:965-72. doi: 10.1378/chest.127.3.965

Paredi P, Ward S, Cramer D, Dip M, Barnes PJ, Kharitonov SA. Normal bronchial blood flow in COPD is unaffected by inhaled corticosteroids and correlates with exhaled nitric oxide. Chest 2007;131:1075-81. doi: 10.1378/chest.06-2154

Zanini A, Chetta A, Saetta M, Baraldo S, Castagnetti C, Nicolini G, Neri M, Oliveri D. Bronchial vascular remodelling in patients with COPD and its relationship with inhaled steroid treatment. Thorax 2009;64:1019-24. doi: 10.1136/thx.2009.114629

Carpagnano GE, Ruggieri C, Scioscia G, Storto MM, Zoppo L, Foschino-Barbaro MP. Is the exhaled breath temperature sensitive to cigarette smoking? COPD 2016;13:642-6. doi: 10.3109/15412555.2016.1143458

Paredi P, Kharitonov SA, Barnes PJ. Faster rise of EBT in asthma: a novel marker of airway inflammation? Am J Respir Crit Care Med 2002;165:181-4. doi: 10.1164/ajrccm.165.2.2103053

Xepapadaki P, Xatziioannou A, Chatzicharalambous M, Makrinioti H, Papadopoulos NG. Exhaled breath temperature increases during mild exacerbations in children with virus-induced asthma. Int Arch Allergy Immunol 2010;153:70-4. doi: 10.1159/000301581

Paredi P, Caramori G, Cramer D, Ward D, Ciaccia A, Papi A, Kharitonov SA, Barnes PJ. Slower rise of exhaled breath temperature in chronic obstructive pulmonary disease. Eur Respir J 2003;21:439-43. doi: 10.1183/09031936.03.00061902

Zebekakis PE, Nawrot T, Thijs L, Balkestein EJ, van der Heijden-Spek J, Van Bortel LM, Struijker-Boudier HA, Safar ME, Staessen JA. Obesity is associated with increased arterial stiffness from adolescence until old age. J Hypertens 2005;23:1839-46. doi: 10.1097/01.hjh.0000179511.93889.e9

Hogg JC, Paré PD, Hackett TL. The contribution of small airway obstruction to the pathogenesis of chronic obstructive pulmonary disease. Physiol Rev 2017;97:529-52. doi: 10.1152/physrev.00025.2015

Stockley JA, Cooper BG, Stockley RA, Sapey E. Small airways disease: time for a revisit? Int J Chron Obstruct Pulmon Dis 2017;12:2343-53. doi: 10.2147/COPD.S138540

Mead J. The lung’s "quiet zone". N Engl J Med 1970;282:1318-9. doi: 10.1056/NEJM197006042822311

Borrill ZL, Houghton CM, Woodcock AA, Vestbo J, Singh D. Measuring bronchodilation in COPD clinical trials. Br J Clin Pharmacol 2005;59:379-84. doi: 10.1111/j.1365-2125.2004.02261.x

Piorunek T, Kostrzewska M, Stelmach-Mardas M, Mardas M, Michalak S, Goździk-Spychalska J, Batura-Gabryel H. Small airway obstruction in chronic obstructive pulmonary disease: potential parameters for early detection. Adv Exp Med Biol 2017;980:75-82. doi: 10.1007/5584_2016_208

Galbán CJ, Han MK, Boes JL, Chughtai KA, Meyer CR, Johnson TD, Galban S, Rehemtulla A, Kazerooni EA, Martinez FJ, Ross BD. Computed tomography-based biomarker provides unique signature for diagnosis of COPD phenotypes and disease progression. Nature Med 2012;18:1711-5. doi: 10.1038/nm.2971

Boes JL, Hoff BA, Bule M, Johnson TD, Rehemtulla A, Chamberlain R, Hoffman EA, Kazerooni EA, Martinez FJ, Han MK, Ross BD, Galbán CJ. Parametric response mapping monitors temporal changes on lung CT scans in the subpopulations and intermediate outcome measures in COPD Study (SPIROMICS). Academic Radiol 2015;22:186-94. doi: 10.1016/j.acra.2014.08.015

How to Cite
Huljev ŠipošI, Labor S, Jurić I, Plavec D, Vlahoviček K, Bogović S, Pavkov VukelićJ, Labor M. Dynamics of exhaled breath temperature after smoking a cigarette and its association with lung function changes predictive of COPD risk in smokers: a cross-sectional study. Arh Hig Rada Toksikol [Internet]. 2019May31 [cited 2020Dec.2];70(2). Available from: https://arhiv.imi.hr/index.php/arhiv/article/view/1045
Original article