Endotoxin and (1→3)-β-D-glucan contamination in electronic cigarette products sold in the United States

Environmental Health Perspectives

Volumn 127, Issue 4, 2019, Pages

  Lee, Mi Sun ^a   Allen, Joseph G ^a   Christiani, David C ^a,b  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 1,3 GLUCAN; ENDOTOXIN; MENTHOL; NICOTINE; BACTERIAL TOXIN; BETA GLUCAN; MYCOTOXIN;

ARTICLE; ASTHMA; CONTROLLED STUDY; CORRELATION COEFFICIENT; HUMAN; INFLAMMATION; LEUKOCYTE COUNT; LIMIT OF DETECTION; LUNG FUNCTION; MICROBIAL CONTAMINATION; NOSE OBSTRUCTION; PRIORITY JOURNAL; RISK FACTOR; TOBACCO; TURBIDIMETRY; UNITED STATES; VAPING; ELECTRONIC CIGARETTE;

BACTERIAL TOXINS; BETA-GLUCANS; ELECTRONIC NICOTINE DELIVERY SYSTEMS; ENDOTOXINS; MYCOTOXINS; UNITED STATES;

EID: 85065287743     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/EHP3469     Document Type: Article

References (57)

1. Adhikari A, Gupta J, Wilkins JR 3rd, Olds RL, Indugula R, Cho KJ. 2011. Airborne microorganisms, endotoxin, and (1→3)-beta-d-glucan exposure in greenhouses and assessment of respiratory symptoms among workers. Ann Occup Hyg 55:272–285, PMID: 21177263, https://doi.org/10.1093/annhyg/meq082.
2. Allen JG, Flanigan SS, LeBlanc M, Vallarino J, MacNaughton P, Stewart JH. 2016. Flavoring chemicals in e-cigarettes: diacetyl, 2,3-pentanedione, and acetoin in a sample of 51 products, including fruit-, candy-, and cocktail-flavored e-cigarettes. Environ Health Perspect 124(6):733–739, PMID: 26642857, https://doi.org/10.1289/ehp.1510185.
3. Basinas I, Sigsgaard T, Kromhout H, Heederik D, Wouters IM, Schlünssen V. 2015. A comprehensive review of levels and determinants of personal exposure to dust and endotoxin in livestock farming. J Expo Sci Environ Epidemiol 25(2):123–137, PMID: 24280684, https://doi.org/10.1038/jes.2013.83.
4. Bekki K, Uchiyama S, Ohta K, Inaba Y, Nakagome H, Kunugita N. 2014. Carbonyl compounds generated from electronic cigarettes. Int J Environ Res Public Health 11(11):11192–11200, PMID: 25353061, https://doi.org/10.3390/ijerph111111192.
5. Bos MP, Tommassen J. 2004. Biogenesis of the Gram-negative bacterial outer membrane. Curr Opin Microbiol 7(6):610–616, PMID: 15556033, https://doi.org/10.1016/j.mib.2004.10.011.
6. Brass DM, Hollingsworth JW, Cinque M, Li Z, Potts E, Toloza E, et al. 2008. Chronic LPS inhalation causes emphysema-like changes in mouse lung that are associated with apoptosis. Am J Respir Cell Mol Biol 39(5):584–590, PMID: 18539952, https://doi.org/10.1165/rcmb.2007-0448OC.
7. Brass DM, Savov JD, Gavett SH, Haykal-Coates N, Schwartz DA. 2003. Subchronic endotoxin inhalation causes persistent airway disease. Am J Physiol Lung Cell Mol Physiol 285(3):L755–L761, PMID: 12794002, https://doi.org/10.1152/ajplung. 00001.2003.
8. Carnes MU, Hoppin JA, Metwali N, Wyss AB, Hankinson JL, O'Connell EL, et al. 2017. House dust endotoxin levels are associated with adult asthma in a U.S. farming population. Ann Am Thorac Soc 14(3):324–331, PMID: 27977294, https://doi.org/10.1513/AnnalsATS.201611-861OC.
9. Castellan RM, Olenchock SA, Kinsley KB, Hankinson JL. 1987. Inhaled endotoxin and decreased spirometric values. An exposure-response relation for cotton dust. N Engl J Med 317(10):605–610, PMID: 3614274, https://doi.org/10.1056/NEJM198709033171005.
10. Cheng T. 2014. Chemical evaluation of electronic cigarettes. Tob Control 23 (Suppl 2):ii11–ii17, https://doi.org/10.1136/tobaccocontrol-2013-051482.
11. Chun LF, Moazed F, Calfee CS, Matthay MA, Gotts JE. 2017. Pulmonary toxicity of e-cigarettes. Am J Physiol Lung Cell Mol Physiol 313(2):L193–L206, PMID: 28522559, https://doi.org/10.1152/ajplung.00071.2017.
12. Cullen KA, Ambrose BK, Gentzke AS, Apelberg BJ, Jamal A, King BA. 2018. Notes from the field: use of electronic cigarettes and any tobacco product among middle and high school students-United States, 2011-2018. MMWR Morb Mortal Wkly Rep 67(45):1276–1277, PMID: 30439875, https://doi.org/10.15585/mmwr.mm6745a5.
13. Donham KJ. 2010. Community and occupational health concerns in pork production: a review. J Anim Sci 88(13 Suppl):E102–E111, PMID: 20154166, https://doi.org/10. 2527/jas.2009-2554.
14. Douwes J. 2005. (1→3)-Beta-D-glucans and respiratory health: a review of the scientific evidence. Indoor Air 15(3):160–169, PMID: 15865616, https://doi.org/10. 1111/j.1600-0668.2005.00333.x.
15. Douwes J, Van Strien R, Doekes G, Smit J, Kerkhof M, Gerritsen J, et al. 2006. Does early indoor microbial exposure reduce the risk of asthma? The Prevention and Incidence of Asthma and Mite Allergy birth cohort study. J Allergy Clin Immunol 117(5):1067–1073, PMID: 16675334, https://doi.org/10.1016/j.jaci.2006.02.002.
16. Family Smoking Prevention and Tobacco Control Act. 2009. Pub. L No. 111–31 (111th Congress, 22 June 2009). https://www.fda.gov/TobaccoProducts/Labeling/RulesRegulationsGuidance/ucm246129.htm [accessed 30 October 2016].
17. Farsalinos KE, Kistler KA, Gillman G, Voudris V. 2015. Evaluation of electronic cigarette liquids and aerosol for the presence of selected inhalation toxins. Nicotine Tob Res 17(2):168–174, PMID: 25180080, https://doi.org/10.1093/ntr/ntu176.
18. Farsalinos KE, Spyrou A, Tsimopoulou K, Stefopoulos C, Romagna G, Voudris V. 2014. Nicotine absorption from electronic cigarette use: comparison between first and new-generation devices. Sci Rep 4:4133, PMID: 24569565, https://doi.org/10.1038/srep04133.
19. Fernández E, Ballbé M, Sureda X, Fu M, Saltó E, Martinez-Sánchez JM. 2015. Particulate matter from electronic cigarettes and conventional cigarettes: a systematic review and observational study. Curr Environ Health Rep 2(4):423– 429, PMID: 26452675, https://doi.org/10.1007/s40572-015-0072-x.
20. Fessler MB, Carnes MU, Salo PM, Wilkerson J, Cohn RD, King D, et al. 2017. House dust endotoxin and peripheral leukocyte counts: results from two large epidemiologic studies. Environ Health Perspect 125(5):057010, PMID: 28599265, https://doi.org/10.1289/EHP661.
21. Geiss O, Bianchi I, Barahona F, Barrero-Moreno J. 2015. Characterisation of mainstream and passive vapours emitted by selected electronic cigarettes. Int J Hyg Environ Health 218(1):169–180, PMID: 25455424, https://doi.org/10.1016/j. ijheh.2014.10.001.
22. Giovenco DP, Hammond D, Corey CG, Ambrose BK, Delnevo CD. 2015. E-cigarette market trends in traditional U.S. retail channels, 2012-2013. Nicotine Tob Res 17(10):1279–1283, PMID: 25542918, https://doi.org/10.1093/ntr/ntu282.
23. Goniewicz ML, Hajek P, McRobbie H. 2014a. Nicotine content of electronic cigarettes, its release in vapour and its consistency across batches: regulatory implications. Addiction 109(3):500–507, PMID: 24345184, https://doi.org/10.1111/add.12410.
24. Goniewicz ML, Knysak J, Gawron M, Kosmider L, Sobczak A, Kurek J, et al. 2014b. Levels of selected carcinogens and toxicants in vapour from electronic cigarettes. Tob Control 23(2):133–139, PMID: 23467656, https://doi.org/10.1136/tobaccocontrol-2012-050859.
25. Hasday JD, Bascom R, Costa JJ, Fitzgerald T, Dubin W. 1999. Bacterial endotoxin is an active component of cigarette smoke. Chest 115(3):829–835, PMID: 10084499, https://doi.org/10.1378/chest.115.3.829.
26. Herzog B, Gerberi J, Scott A. 2014. Equity Research: Tobacco-Nielsen C-Store Data-E-Cig $ Sales Decline Moderates. Charlotte, NC: Wells Fargo Securities. http://www.c-storecanada.com/attachments/article/153/Nielsen%20C-Stores% 20-%20Tobacco.pdf [accessed 30 August 2015].
27. Holst G, Høst A, Doekes G, Meyer HW, Madsen AM, Sigsgaard T. 2015. Determinants of house dust, endotoxin, and beta-(1,3)-d-glucan in homes of Danish children. Indoor Air 25(3):245–259, PMID: 25039673, https://doi.org/10. 1111/ina.12143.
28. Ingebrethsen BJ, Cole SK, Alderman SL. 2012. Electronic cigarette aerosol particle size distribution measurements. Inhal Toxicol 24(14):976–984, PMID: 23216158, https://doi.org/10.3109/08958378.2012.744781.
29. Iossifova Y, Reponen T, Sucharew H, Succop P, Vesper S. 2008. Use of (1-3)-β-D-glucan concentrations in dust as a surrogate method for estimating specific fungal exposures. Indoor Air 18(3):225–232, https://doi.org/10.1111/j.1600-0668. 2008.00526.x.
30. Jensen RP, Luo W, Pankow JF, Strongin RM, Peyton DH. 2015. Hidden formaldehyde in e-cigarette aerosols. N Engl J Med 372(4):392–394, PMID: 25607446, https://doi.org/10.1056/NEJMc1413069.
31. Klager S, Vallarino J, MacNaughton P, Christiani DC, Lu Q, Allen JG. 2017. Flavoring chemicals and aldehydes in e-cigarette emissions. Environ Sci Technol 51(18):10806–10813, PMID: 28817267, https://doi.org/10.1021/acs.est. 7b02205.
32. Lai PS, Fresco JM, Pinilla MA, Macias AA, Brown RD, Englert JA, et al. 2012. Chronic endotoxin exposure produces airflow obstruction and lung dendritic cell expansion. Am J Respir Cell Mol Biol 47(2):209–217, PMID: 22517795, https://doi.org/10.1165/rcmb.2011-0447OC.
33. Lai PS, Hang JQ, Valeri L, Zhang FY, Zheng BY, Mehta AJ, et al. 2015. Endotoxin and gender modify lung function recovery after occupational organic dust exposure: a 30-year study. Occup Environ Med 72(8):546–552, PMID: 25666844, https://doi.org/10.1136/oemed-2014-102579.
34. Lane SR, Sewell RD. 2006. Correlative measurement of four biological contaminants on cotton lint, and their implications for occupational health. Int J Occup Environ Health 12(2):120–125, PMID: 16722191, https://doi.org/10.1179/oeh.2006. 12.2.120.
35. Larsson L, Szponar B, Pehrson C. 2004. Tobacco smoking increases dramatically air concentrations of endotoxin. Indoor Air 14(6):421–424, PMID: 15500635, https://doi.org/10.1111/j.1600-0668.2004.00290.x.
36. Lee MK, Carnes MU, Butz N, Azcarate-Peril MA, Richards M, Umbach DM, et al. 2018. Exposure related to house dust microbiota in a U.S. farming population. Environ Health Perspect 126(6):067001, PMID: 29863827, https://doi.org/10.1289/EHP3145.
37. Lee MS, LeBouf RF, Son YS, Koutrakis P, Christiani DC. 2017. Nicotine, aerosol particles, carbonyls and volatile organic compounds in tobacco-and menthol-flavored e-cigarettes. Environ Health 16(1):42, PMID: 28449666, https://doi.org/10.1186/s12940-017-0249-x.
38. Maheswaran D, Zeng Y, Chan-Yeung M, Scott J, Osornio-Vargas A, Becker AB, et al. 2014. Exposure to Beta-(1,3)-D-glucan in house dust at age 7-10 is associated with airway hyperresponsiveness and atopic asthma by age 11-14. PLoS One 9(6):e98878, PMID: 24905346, https://doi.org/10.1371/journal.pone.0098878.
39. Marynak KL, Gammon DG, Rogers T, Coats EM, Singh T, King BA. 2017. Sales of nicotine-containing electronic cigarette products: United States, 2015. Am J Public Health 107(5):702–705, PMID: 28323467, https://doi.org/10.2105/AJPH. 2017.303660.
40. Melstrom P, Koszowski B, Thanner MH, Hoh E, King B, Bunnell R, et al. 2017. Measuring PM2.5, ultrafine particles, air nicotine and wipe samples following the use of electronic cigarettes. Nicotine Tob Res 19(9):1055–1061, PMID: 28340080, https://doi.org/10.1093/ntr/ntx058.
41. Orr MS. 2014. Electronic cigarettes in the USA: a summary of available toxicology data and suggestions for the future. Tob Control 23(Suppl 2):ii18–ii22, PMID: 24732158, https://doi.org/10.1136/tobaccocontrol-2013-051474.
42. Pankow JF, Kim K, McWhirter KJ, Luo W, Escobedo JO, Strongin RM, et al. 2017. Benzene formation in electronic cigarettes. PLoS One 12(3):e0173055, PMID: 28273096, https://doi.org/10.1371/journal.pone.0173055.
43. Park DU, Ryu SH, Kim SB, Yoon CS. 2011. An assessment of dust, endotoxin, and microorganism exposure during waste collection and sorting. J Air Waste Manag Assoc 61(4):461–468, PMID: 21516941.
44. Park HR, O'Sullivan M, Vallarino J, Shumyatcher M, Himes BE, Park JA, et al. 2019. Transcriptomic response of primary human airway epithelial cells to flavoring chemicals in electronic cigarettes. Sci Rep 9:1400, PMID: 30710127 https://doi.org/10.1038/s41598-018-37913-9.
45. Pauly JL, Paszkiewicz G. 2011. Cigarette smoke, bacteria, mold, microbial toxins, and chronic lung inflammation. J Oncol 2011:819129, PMID: 21772847, https://doi.org/10.1155/2011/819129.
46. Schober W, Szendrei K, Matzen W, Osiander-Fuchs H, Heitmann D, Schettgen T, et al. 2014. Use of electronic cigarettes (e-cigarettes) impairs indoor air quality and increases FeNO levels of e-cigarette consumers. Int J Hyg Environ Health 217(6):628–637, PMID: 24373737, https://doi.org/10.1016/j.ijheh.2013.11.003.
47. Schram-Bijkerk D, Doekes G, Douwes J, Boeve M, Riedler J, et al. 2005. Bacterial and fungal agents in house dust and wheeze in children: the PARSIFAL study. Clin Exp Allergy 35(10):1272–1278, PMID: 16238785, https://doi.org/10.1111/j.1365-2222.2005.02339.x.
48. Szponar B, Pehrson C, Larsson L. 2012. Bacterial and fungal markers in tobacco smoke. Sci Total Environ 438:447–451, PMID: 23026151, https://doi.org/10.1016/j. scitotenv.2012.08.067.
49. Thorn J, Rylander R. 1998. Airways inflammation and glucan in a rowhouse area. Am J Respir Crit Care Med 157(6 Pt 1):1798–1803, PMID: 9620908, https://doi.org/10.1164/ajrccm.157.6.9706081.
50. Thorne PS, Mendy A, Metwali N, Salo P, Co C, Jaramillo R, et al. 2015. Endotoxin exposure: predictors and prevalence of associated asthma outcomes in the United States. Am J Respir Crit Care Med 192(11):1287–1297, PMID: 26258643, https://doi.org/10.1164/rccm.201502-0251OC.
51. Uchiyama S, Ohta K, Inaba Y, Kunugita N. 2013. Determination of carbonyl compounds generated from the e-cigarette using coupled silica cartridges impregnated with hydroquinone and 2,4-dinitrophenylhydrazine, followed by high-performance liquid chromatography. Anal Sci 29(12):1219–1222, PMID: 24334991.
52. USP (United States Pharmacopeia). 2016. Bacterial Endotoxins. 39, NF 34 Chapter OpenSPILessThanSPI85OpenSPIGreaterThanSPI Bacterial Endotoxins Test.
53. Wang TW, Gentzke A, Sharapova S, Cullen KA, Ambrose BK, Jamal A. 2018. Tobacco product use among middle and high school students-United States, 2011-2017. MMWR Morb Mortal Wkly Rep 67(22):629–633, PMID: 29879097, https://doi.org/10.15585/mmwr.mm6722a3.
54. Watkins SL, Glantz SA, Chaffee BW. 2018. Association of noncigarette tobacco product use with future cigarette smoking among youth in the population assessment of tobacco and health (PATH) study, 2013-2015. JAMA Pediatr 172(2):181–187, PMID: 29297010, https://doi.org/10.1001/jamapediatrics.2017.4173.
55. Wells Fargo Securities. 2014. Equity Research: Tobacco—Nielsen C-Store Data— ecig$Sales Decline Moderates. Wells Fargo Securities.
56. Williams M, Villarreal A, Bozhilov K, Lin S, Talbot P. 2013. Metal and silicate particles including nanoparticles are present in electronic cigarette cartomizer fluid and aerosol. PLoS One 8(3):e57987, PMID: 23526962, https://doi.org/10. 1371/journal.pone.0057987.
57. Yoda Y, Tamura K, Shima M. 2017. Airborne endotoxin concentrations in indoor and outdoor particulate matter and their predictors in an urban city. Indoor Air 27(5):955–964, PMID: 28161889, https://doi.org/10.1111/ina.12370.