166
Views
3
CrossRef citations to date
0
Altmetric
Article

The inflammatory biomarker YKL-40 is elevated in the serum, but not the sputum, of E-cigarette users

ORCID Icon, , &
Pages 55-66 | Received 27 Mar 2020, Accepted 03 Nov 2020, Published online: 17 Nov 2020

References

  • Dai H, Leventhal AM. Prevalence of e-cigarette use among adults in the United States, 2014–2018. JAMA. 2019;322(18):1824.
  • Mirbolouk M, Charkhchi P, Kianoush S, et al. Prevalence and distribution of e-cigarette use among U.S. adults: behavioral risk factor surveillance system, 2016. Ann Intern Med. 2018;169(7):429–438. doi:10.7326/M17-3440.
  • Hajek P, Phillips-Waller A, Przulj D, et al. A randomized trial of e-cigarettes versus nicotine-replacement therapy. N Engl J Med. 2019;380(7):629–637.
  • Walker N, Parag V, Verbiest M, Laking G, Laugesen M, Bullen C. Nicotine patches used in combination with e-cigarettes (with and without nicotine) for smoking cessation: a pragmatic, randomised trial. Lancet Respir Med. 2020;8(1):54–64.
  • McNeill AB, Calder R, Hitchman SC, Hajek P, McRobbie H. E-Cigarettes: An Evidence Update. London: Public Health England; 2015.
  • Layden JE, Ghinai I, Pray I, et al. Pulmonary illness related to e-cigarette use in illinois and wisconsin — preliminary report. N Engl J Med. 2020;382(10):903–916.
  • Perez MF, Atuegwu NC, Mead EL, Oncken C, Mortensen EM. Adult e-cigarettes use associated with a self-reported diagnosis of COPD. Int J Environ Res Public Health. 2019;16(20):3938.
  • Perez MF, Atuegwu NC, Oncken CM, Mead EL, Mortensen EM. Association of electronic cigarette use and asthma in never smokers. Ann Am Thorac Soc. 2019;16(11):1453–1456.
  • Cho JH, Paik SY. Association between electronic cigarette use and asthma among high school students in South Korea. PLoS One. 2016;11(3):e0151022. doi:10.1371/journal.pone.0151022.
  • Choi K, Bernat DE. Cigarette use among Florida youth with and without asthma. Am J Prev Med. 2016;51(4):446–453.
  • Schweitzer RJ, Wills TA, Tam E, Pagano I, Choi K. E-cigarette use and asthma in a multiethnic sample of adolescents. Prev Med. 2017; 105:226–231. doi:10.1016/j.ypmed.2017.09.023.
  • Wills TA, Pagano I, Williams R, Tam E. E-cigarette use and respiratory disorder in an adult sample. Drug Alcohol Depend. 2019; 194:363–370.
  • McConnell R, Barrington-Trimis JL, Wang K, et al. Electronic-cigarette use and respiratory symptoms in adolescents. Am J Respir Crit Care Med. 2017;195(8):1043–1049.
  • Crotty Alexander LE, Drummond CA, Hepokoski M, et al. Chronic inhalation of e-cigarette vapor containing nicotine disrupts airway barrier function and induces systemic inflammation and multiorgan fibrosis in mice. Am J Physiol Regul Integr Comp Physiol. 2018;314(6):R834–R847.
  • Garcia-Arcos I, Geraghty P, Baumlin N, et al. Chronic electronic cigarette exposure in mice induces features of COPD in a nicotine-dependent manner. Thorax. 2016;71(12):1119–1129. doi:10.1136/thoraxjnl-2015-208039.
  • Larcombe AN, Janka MA, Mullins BJ, Berry LJ, Bredin A, Franklin PJ. The effects of electronic cigarette aerosol exposure on inflammation and lung function in mice. Am J Physiol Lung Cell Mol Physiol. 2017;313(1):L67–L79. doi:10.1152/ajplung.00203.2016.
  • Lim HB, Kim SH. Inhallation of e-cigarette cartridge solution aggravates allergen-induced airway inflammation and hyper-responsiveness in mice. Toxicol Res. 2014;30(1):13–18. doi:10.5487/TR.2014.30.1.013.
  • Matsuura H, Hartl D, Kang MJ, et al. Role of breast regression protein-39 in the pathogenesis of cigarette smoke-induced inflammation and emphysema. Am J Respir Cell Mol Biol. 2011;44(6):777–786. doi:10.1165/rcmb.2010-0081OC.
  • Chupp GL, Lee CG, Jarjour N, et al. A chitinase-like protein in the lung and circulation of patients with severe asthma. N Engl J Med. 2007;357(20):2016–2027.
  • Sakazaki Y, Hoshino T, Takei S, et al. Overexpression of chitinase 3-like 1/YKL-40 in lung-specific IL-18-transgenic mice, smokers and COPD. PLoS One. 2011;6(9):e24177. doi:10.1371/journal.pone.0024177.
  • Majewski S, Tworek D, Szewczyk K, et al. Overexpression of chitotriosidase and YKL-40 in peripheral blood and sputum of healthy smokers and patients with chronic obstructive pulmonary disease. COPD. 2019;14:1611–1631.
  • Holmgaard DB, Mygind LH, Titlestad IL, et al. Plasma YKL-40 and all-cause mortality in patients with chronic obstructive pulmonary disease. BMC Pulm Med. 2013;13(1):77.
  • Korthagen NM, van Moorsel CHM, Barlo NP, et al. Serum and BALF YKL-40 levels are predictors of survival in idiopathic pulmonary fibrosis. Respir Med. 2011;105(1):106–113.
  • Guerra S, Halonen M, Sherrill DL, et al. The relation of circulating YKL-40 to levels and decline of lung function in adult life. Respir Med. 2013;107(12):1923–1930.
  • James AJ, Reinius LE, Verhoek M, et al. Increased YKL-40 and chitotriosidase in asthma and chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2016;193(2):131–142. doi:10.1164/rccm.201504-0760OC.
  • Johansen JS. Studies on serum YKL-40 as a biomarker in diseases with inflammation, tissue remodelling, fibroses and cancer. Dan Med Bull. 2006;53(2):172–209.
  • Johansen JS, Hoyer PE, Larsen LA, Price PA, Mollgard K. YKL-40 protein expression in the early developing human musculoskeletal system. J Histochem Cytochem. 2007;55(12):1213–1228. doi:10.1369/jhc.7A7245.2007.
  • Reidel B, Radicioni G, Clapp P, et al. Cigarette use causes a unique innate immune response in the lung involving increased neutrophilic activation and altered mucin secretion. Am J Respir Crit Care Med. 2018;197(4):492–501.
  • Shen Y, Wolkowicz MJ, Kotova T, Fan L, Timko MP. Transcriptome sequencing reveals e-cigarette vapor and mainstream-smoke from tobacco cigarettes activate different gene expression profiles in human bronchial epithelial cells. Sci Rep. 2016; 6:23984. doi:10.1038/srep23984.
  • Martin EM, Clapp PW, Rebuli ME, et al. E-cigarette use results in suppression of immune and inflammatory-response genes in nasal epithelial cells similar to cigarette smoke. Am J Physiol Lung Cell Mol Physiol. 2016;311(1):L135–144. doi:10.1152/ajplung.00170.2016.
  • Song MA, Reisinger SA, Freudenheim JL, et al. Effects of electronic cigarette constituents on the human lung: a pilot clinical trial. Cancer Prev Res (Phila). 2020;13(2):145–152.
  • Khan NA, Yogeswaran S, Wang Q, Muthumalage T, Sundar IK, Rahman I. Waterpipe smoke and e-cigarette vapor differentially affect circadian molecular clock gene expression in mouse lungs. PLoS One. 2019;14(2):e0211645. doi:10.1371/journal.pone.0211645.
  • Singh KP, Lawyer G, Muthumalage T, et al. Systemic biomarkers in electronic cigarette users: implications for noninvasive assessment of vaping-associated pulmonary injuries. ERJ Open Res. 2019;5(4):00182–2019–02019.
  • Cropsey KL, Trent LR, Clark CB, Stevens EN, Lahti AC, Hendricks PS. How low should you go? Determining the optimal cutoff for exhaled carbon monoxide to confirm smoking abstinence when using cotinine as reference. Nicotine Tob Res. 2014;16(10):1348–1355. doi:10.1093/ntr/ntu085.
  • Foulds J, Veldheer S, Berg A. Electronic cigarettes (e-cigs): views of aficionados and clinical/public health perspectives. Int J Clin Pract. 2011;65(10):1037–1042. doi:10.1111/j.1742-1241.2011.02751.x.
  • Pizzichini E, Pizzichini MM, Kidney JC, et al. Induced sputum, bronchoalveolar lavage and blood from mild asthmatics: inflammatory cells, lymphocyte subsets and soluble markers compared. Eur Respir J. 1998;11(4):828–834.
  • Yan X, Chu JH, Gomez J, et al. Noninvasive analysis of the sputum transcriptome discriminates clinical phenotypes of asthma. Am J Respir Crit Care Med. 2015;191(10):1116–1125. doi:10.1164/rccm.201408-1440OC.
  • Strober W. Trypan blue exclusion test of cell viability. Curr Protoc Immunol. 2015; 111:A3 B 1-3.
  • An Atlas of Induced Sputum: An Aid for Research and Diagnosis. New York: Parthenon Publishing Group; 2004.
  • R Core Team. R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing; 2013.
  • Bojesen SE, Johansen JS, Nordestgaard BG. Plasma YKL-40 levels in healthy subjects from the general population. Clin Chim Acta. 2011;412(9–10):709–712. doi:10.1016/j.cca.2011.01.022.
  • Flouris AD, Poulianiti KP, Chorti MS, et al. Acute effects of electronic and tobacco cigarette smoking on complete blood count. Food Chem Toxicol. 2012;50(10):3600–3603.
  • Higuchi T, Omata F, Tsuchihashi K, Higashioka K, Koyamada R, Okada S. Current cigarette smoking is a reversible cause of elevated white blood cell count: cross-sectional and longitudinal studies. Prev Med Rep. 2016; 4:417–422. doi:10.1016/j.pmedr.2016.08.009.
  • van Eeden SF, Hogg JC. The response of human bone marrow to chronic cigarette smoking. Eur Respir J. 2000;15(5):915–921.
  • Blidberg K, Palmberg L, Dahlen B, Lantz AS, Larsson K. Increased neutrophil migration in smokers with or without chronic obstructive pulmonary disease. Respirology. 2012;17(5):854–860.
  • Mortaz E, Adcock IM, Ito K, Kraneveld AD, Nijkamp FP, Folkerts G. Cigarette smoke induces CXCL8 production by human neutrophils via activation of TLR9 receptor. Eur Respir J. 2010;36(5):1143–1154. doi:10.1183/09031936.00062209.
  • Khan NA, Lawyer G, McDonough S, et al. Systemic biomarkers of inflammation, oxidative stress and tissue injury and repair among waterpipe, cigarette and dual tobacco smokers. Tob Control. 2020;29(Suppl 2):s102–s109. doi:10.1136/tobaccocontrol-2019-054958.
  • Oltmanns U, Chung KF, Walters M, John M, Mitchell JA. Cigarette smoke induces IL-8, but inhibits eotaxin and RANTES release from airway smooth muscle. Respir Res. 2005; 6:74 doi:10.1186/1465-9921-6-74.
  • Nadigel J, Audusseau S, Baglole CJ, Eidelman DH, Hamid Q. IL-8 production in response to cigarette smoke is decreased in epithelial cells from COPD patients. Pulm Pharmacol Ther. 2013;26(5):596–602. doi:10.1016/j.pupt.2013.03.002.
  • Mio T, Romberger DJ, Thompson AB, Robbins RA, Heires A, Rennard SI. Cigarette smoke induces interleukin-8 release from human bronchial epithelial cells. Am J Respir Crit Care Med. 1997;155(5):1770–1776. doi:10.1164/ajrccm.155.5.9154890.
  • Choi W-J, Lee J-W, Cho AR, Lee Y-J. Dose-dependent toxic effect of cotinine-verified tobacco smoking on systemic inflammation in apparently healthy men and women: a nationwide population-based study. Int J Environ Res Public Health. 2019;16(3):503.
  • Wang H, Liao H, Ochani M, et al. Cholinergic agonists inhibit HMGB1 release and improve survival in experimental sepsis. Nat Med. 2004;10(11):1216–1221. doi:10.1038/nm1124.
  • Bagaitkar J, Zeller I, Renaud DE, Scott DA. Cotinine inhibits the pro-inflammatory response initiated by multiple cell surface Toll-like receptors in monocytic THP cells. Tob Induc Dis. 2012;10(1):18–18. doi:10.1186/1617-9625-10-18.
  • Rubin RL, Hermanson TM, Bedrick EJ, et al. Effect of cigarette smoke on autoimmunity in murine and human systemic lupus erythematosus. Toxicol Sci. 2005;87(1):86–96., Jr.
  • Lerner CA, Sundar IK, Yao H, et al. Vapors produced by electronic cigarettes and e-juices with flavorings induce toxicity, oxidative stress, and inflammatory response in lung epithelial cells and in mouse lung. PLoS One. 2015;10(2):e0116732 doi:10.1371/journal.pone.0116732.
  • Wang Q, Sundar IK, Li D, et al. E-cigarette-induced pulmonary inflammation and dysregulated repair are mediated by nAChR α7 receptor: role of nAChR α7 in SARS-CoV-2 Covid-19 ACE2 receptor regulation . Respir Res. 2020;21(1):154. doi:10.1186/s12931-020-01396-y.
  • Lee CG, Cruz CSD, Herzog E, Rosenberg SM, Ahangari F, Elias JA. YKL-40, a Chitinase-like Protein at the Intersection of Inflammation and Remodeling. Am J Respir Crit Care Med. 2012;185(7):692–694. doi:10.1164/rccm.201202-0203ED.
  • Tong X, Liu S, Ma Y, Wang D, Fan H. The serum YKL-40 is a useful biomarker for asthma. European Respiratory Journal. 2017; 50:PA3566.
  • Tong X, Wang D, Liu S, et al. The YKL-40 protein is a potential biomarker for COPD: a meta-analysis and systematic review. COPD. 2018;13:409–418.
  • Johansen JS, Milman N, Hansen M, Garbarsch C, Price PA, Graudal N. Increased serum YKL-40 in patients with pulmonary sarcoidosis–a potential marker of disease activity? Respir Med. 2005;99(4):396–402.
  • Fantino E, Gangell CL, Hartl D, Sly PD. Airway, but not serum or urinary, levels of YKL-40 reflect inflammation in early cystic fibrosis lung disease. BMC Pulm Med. 2014;14(1):28.
  • Rathcke CN, Raymond I, Kistorp C, Hildebrandt P, Faber J, Vestergaard H. Low grade inflammation as measured by levels of YKL-40: Association with an increased overall and cardiovascular mortality rate in an elderly population. Int J Cardiol. 2010;143(1):35–42.
  • Johansen JS, Bojesen SE, Tybjaerg-Hansen A, Mylin AK, Price PA, Nordestgaard BG. Plasma YKL-40 and total and disease-specific mortality in the general population. Clin Chem . 2010;56(10):1580–1591.
  • Llorens F, Thüne K, Tahir W, et al. YKL-40 in the brain and cerebrospinal fluid of neurodegenerative dementias. Mol Neurodegener. 2017;12(1):83.
  • Volck B, Johansen JS, Stoltenberg M, et al. Studies on YKL-40 in knee joints of patients with rheumatoid arthritis and osteoarthritis. Involvement of YKL-40 in the joint pathology. Osteoarthritis Cartilage. 2001;9(3):203–214. doi:10.1053/joca.2000.0377.
  • Gao J, Iwamoto H, Koskela J, et al. Characterization of sputum biomarkers for asthma-COPD overlap syndrome. COPD. 2016;11:2457–2465.
  • Hector A, Kormann MS, Mack I, et al. The chitinase-like protein YKL-40 modulates cystic fibrosis lung disease. PLoS One. 2011;6(9):e24399 doi:10.1371/journal.pone.0024399.
  • Lee JH, Park KH, Park JW, Hong CS. YKL-40 in induced sputum after allergen bronchial provocation in atopic asthma. J Investig Allergol Clin Immunol. 2012; 22:501–507.
  • Otsuka K, Matsumoto H, Niimi A, et al. Sputum YKL-40 levels and pathophysiology of asthma and chronic obstructive pulmonary disease. Respiration. 2012;83(6):507–519.
  • Kalininskiy A, Bach CT, Nacca NE, et al. Croft DP. E-cigarette, or vaping, product use associated lung injury (EVALI): case series and diagnostic approach. Lancet Respir Med. 2019;7(12):1017–1026.
  • Blagev DP, Harris D, Dunn AC, Guidry DW, Grissom CK, Lanspa MJ. Clinical presentation, treatment, and short-term outcomes of lung injury associated with e-cigarettes or vaping: a prospective observational cohort study. Lancet. 2019;394(10214):2073–2083.
  • Flacco ME, Ferrante M, Fiore M, et al. Cohort study of electronic cigarette use: safety and effectiveness after 4 years of follow-up. Eur Rev Med Pharmacol Sci. 2019;23(1):402–412. doi:10.26355/eurrev_201901_16789.
  • Shields PG, Berman M, Brasky TM, et al. A review of pulmonary toxicity of electronic cigarettes in the context of smoking: a focus on inflammation. Cancer Epidemiol Biomarkers Prev. 2017;26(8):1175–1191. doi:10.1158/1055-9965.EPI-17-0358.
  • McRobbie H, Phillips A, Goniewicz ML, et al. Effects of switching to electronic cigarettes with and without concurrent smoking on exposure to nicotine, carbon monoxide, and acrolein. Cancer Prev Res (Phila)). 2015;8(9):873–878. doi:10.1158/1940-6207.CAPR-15-0058.
  • Shahab L, Goniewicz ML, Blount BC, et al. Nicotine, carcinogen, and toxin exposure in long-term e-cigarette and nicotine replacement therapy users: a cross-sectional study. Ann Intern Med. 2017;166(6):390–400. doi:10.7326/M16-1107.
  • Jorenby DE, Smith SS, Fiore MC, Baker TB. Nicotine levels, withdrawal symptoms, and smoking reduction success in real world use: a comparison of cigarette smokers and dual users of both cigarettes and E-cigarettes. Drug Alcohol Depend. 2017; 170:93–101. doi:10.1016/j.drugalcdep.2016.10.041.
  • Eaton DL, Kwan LY, Stratton K, editors. Public Health Consequences of E-Cigarettes. Washington (DC): National Academic Press; 2018.
  • Zhu S-H, Sun JY, Bonnevie E, et al. Four hundred and sixty brands of e-cigarettes and counting: implications for product regulation. Tob Control. 2014;23(suppl 3):iii3–iii9.
  • Goniewicz ML, Smith DM. Are some e-cigarette users "blowing smoke"?: Assessing the accuracy of self-reported smoking abstinence in exclusive e-cigarette users. Nicotine Tob Res. 2019;21(5):699–700. doi:10.1093/ntr/nty085.
  • Rubinstein ML, Delucchi K, Benowitz NL, Ramo DE. Adolescent exposure to toxic volatile organic chemicals from e-cigarettes. Pediatrics. 2018;141(4):e20173557.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.