The association between various smoking behaviors, cotinine biomarkers and skin autofluorescence, a marker for advanced glycation end product accumulation

Robert P van Waateringe, Marjonneke J Mook-Kanamori, Sandra N Slagter, Melanie M van der Klauw, Jana V van Vliet-Ostaptchouk, Reindert Graaff, Helen L Lutgers, Karsten Suhre, Mohammed M El-Din Selim, Dennis O Mook-Kanamori, Bruce H R Wolffenbuttel, Robert P van Waateringe, Marjonneke J Mook-Kanamori, Sandra N Slagter, Melanie M van der Klauw, Jana V van Vliet-Ostaptchouk, Reindert Graaff, Helen L Lutgers, Karsten Suhre, Mohammed M El-Din Selim, Dennis O Mook-Kanamori, Bruce H R Wolffenbuttel

Abstract

Background: Skin autofluorescence, a biomarker for advanced glycation end products (AGEs) accumulation, has been shown to predict diabetes-related cardiovascular complications and is associated with several environmental and lifestyle factors. In the present study, we examined the association between various smoking behaviors and skin autofluorescence, as well as the association between several cotinine biomarkers and skin autofluorescence, using both epidemiological and metabolomics data.

Methods: In a cross-sectional study, we evaluated participants from the LifeLines Cohort Study and the Qatar Metabolomics Study on Diabetes (QMDiab). In the LifeLines Cohort Study smoking behavior and secondhand smoking were assessed in 8,905 individuals including 309 individuals (3.5%) with type 2 diabetes. In QMDiab, cotinine biomarkers were measured in saliva, plasma and urine in 364 individuals of whom 188 (51%) had type 2 diabetes. Skin autofluorescence was measured non-invasively in all participants using the AGE Reader.

Results: Skin autofluorescence levels increased with a higher number of hours being exposed to secondhand smoking. Skin autofluorescence levels of former smokers approached levels of never smokers after around 15 years of smoking cessation. Urinary cotinine N-oxide, a biomarker of nicotine exposure, was found to be positively associated with skin autofluorescence in the QMDiab study (p = 0.03).

Conclusions: In the present study, we have demonstrated that secondhand smoking is associated with higher skin autofluorescence levels whereas smoking cessation has a beneficial effect on skin autofluorescence. Finally, urinary cotinine N-oxide might be used as an alternative way for questionnaires to examine the effect of (environmental) tobacco smoking on skin autofluorescence.

Conflict of interest statement

Competing Interests: RG is founder and shareholder of DiagnOptics BV, Groningen, the Netherlands, manufacturing autofluorescence readers (http://www.diagnoptics.com) which has been used in the present study. This does not alter our adherence to PLOS ONE policies on sharing data and materials.

Figures

Fig 1. Skin autofluorescence stratified for smoking…
Fig 1. Skin autofluorescence stratified for smoking class (LifeLines Cohort Study).
Bars represent mean SAF Z scores (adjusted for age, creatinine clearance and diabetes), whiskers reflect standard error of the mean. Never smoker (n = 3670), Former smoker (n = 3321), Light smoker (0–10 gram tobacco per day, n = 878), Moderate smoker (10–20 gram tobacco per day, n = 537), heavy smoker (>20 gram tobacco per day, n = 475). SAF, skin autofluorescence; AU, arbitrary units; NS, not significant.
Fig 2. Effect of smoking cessation on…
Fig 2. Effect of smoking cessation on skin autofluorescence in former smokers participating in the LifeLines study.
Dots show mean SAF Z-scores (adjusted for age, BMI, creatinine clearance and diabetes status). Whiskers reflect standard error of the mean. SAF, skin autofluorescence
Fig 3. Effect of secondhand smoking on…
Fig 3. Effect of secondhand smoking on skin autofluorescence in never- and former smokers participating in the LifeLines study.
Bars represent mean SAF Z scores (adjusted for age, creatinine clearance and diabetes status) in never smokers and former smokers who stopped smoking for more than 15 years, whiskers reflect standard error of the mean. 0 hours (n = 4213), 1–5 hours (n = 676), 6–10 hours (n = 78), >11 hours (n = 15). SAF, skin autofluorescence; Arbitrary Units, AU; NS, not significant.

References

    1. Baynes JW, Thorpe SR. Glycoxidation and lipoxidation in atherogenesis. Free Radic Biol Med. 2000; 28(12):1708–1716 .
    1. Monnier VM. Nonenzymatic glycosylation, the Maillard reaction and the aging process. J Gerontol. 1990; 45(4):B105–11:.
    1. Dunn JA, McCance DR, Thorpe SR, Lyons TJ, Baynes JW. Age-dependent accumulation of N epsilon-(carboxymethyl)lysine and N epsilon-(carboxymethyl)hydroxylysine in human skin collagen. Biochemistry. 1991; 30(5):1205–1210:.
    1. Dyer DG, Dunn JA, Thorpe SR, Bailie KE, Lyons TJ, McCance DR, et al. Accumulation of Maillard reaction products in skin collagen in diabetes and aging. J Clin Invest. 1993; 91(6):2463–2469 doi: .
    1. Brownlee M. Lilly Lecture 1993. Glycation and diabetic complications. Diabetes. 1994; 43(6):836–841:.
    1. Meerwaldt R, Zeebregts CJ, Navis G, Hillebrands JL, Lefrandt JD, Smit AJ. Accumulation of advanced glycation end products and chronic complications in ESRD treated by dialysis. Am J Kidney Dis. 2009; 53(1):138–150 doi: .
    1. Meerwaldt R, Graaff R, Oomen PH, Links TP, Jager JJ, Alderson NL, et al. Simple non-invasive assessment of advanced glycation endproduct accumulation. Diabetologia. 2004; 47(7):1324–1330 doi: .
    1. Meerwaldt R, Lutgers HL, Links TP, Graaff R, Baynes JW, Gans RO, et al. Skin autofluorescence is a strong predictor of cardiac mortality in diabetes. Diabetes Care. 2007; 30(1):107–112 doi: .
    1. Lutgers HL, Graaff R, Links TP, Ubink-Veltmaat LJ, Bilo HJ, Gans RO, et al. Skin autofluorescence as a noninvasive marker of vascular damage in patients with type 2 diabetes. Diabetes Care. 2006; 29(12):2654–2659 doi: .
    1. Meerwaldt R, Hartog JW, Graaff R, Huisman RJ, Links TP, den Hollander NC, et al. Skin autofluorescence, a measure of cumulative metabolic stress and advanced glycation end products, predicts mortality in hemodialysis patients. J Am Soc Nephrol. 2005; 16(12):3687–3693 doi: .
    1. de Vos LC, Boersema J, Mulder DJ, Smit AJ, Zeebregts CJ, Lefrandt JD. Skin autofluorescence as a measure of advanced glycation end products deposition predicts 5-year amputation in patients with peripheral artery disease. Arterioscler Thromb Vasc Biol. 2015; 35(6):1532–1537 doi: .
    1. Hoonhorst SJ, Lo Tam Loi AT, Hartman JE, Telenga ED, van den Berge M, Koenderman L, et al. Advanced glycation end products in the skin are enhanced in COPD. Metabolism. 2014; 63(9):1149–1156 doi: .
    1. Koetsier M, Lutgers HL, de Jonge C, Links TP, Smit AJ, Graaff R. Reference values of skin autofluorescence. Diabetes Technol Ther. 2010; 12(5):399–403 doi: .
    1. van Waateringe RP, Slagter SN, van der Klauw MM, van Vliet-Ostaptchouk JV, Graaff R, Paterson AD, et al. Lifestyle and clinical determinants of skin autofluorescence in a population-based cohort study. Eur J Clin Invest. 2016; 46(5):481–490 doi: .
    1. Cerami C, Founds H, Nicholl I, Mitsuhashi T, Giordano D, Vanpatten S, et al. Tobacco smoke is a source of toxic reactive glycation products. Proc Natl Acad Sci U S A. 1997; 94(25):13915–13920:.
    1. Connor Gorber S, Schofield-Hurwitz S, Hardt J, Levasseur G, Tremblay M. The accuracy of self-reported smoking: a systematic review of the relationship between self-reported and cotinine-assessed smoking status. Nicotine Tob Res. 2009; 11(1):12–24 doi: .
    1. Benowitz NL. Biomarkers of environmental tobacco smoke exposure. Environ Health Perspect. 1999; 107 Suppl 2:349–355:.
    1. Benowitz NL. Cotinine as a biomarker of environmental tobacco smoke exposure. Epidemiol Rev. 1996; 18(2):188–204:.
    1. Seccareccia F, Zuccaro P, Pacifici R, Meli P, Pannozzo F, Freeman KM, et al. Serum cotinine as a marker of environmental tobacco smoke exposure in epidemiological studies: the experience of the MATISS project. Eur J Epidemiol. 2003; 18(6):487–492:.
    1. Stolk RP, Rosmalen JG, Postma DS, de Boer RA, Navis G, Slaets JP, et al. Universal risk factors for multifactorial diseases: LifeLines: a three-generation population-based study. Eur J Epidemiol. 2008; 23(1):67–74 doi: .
    1. Eny KM, Lutgers HL, Maynard J, Klein BE, Lee KE, Atzmon G, et al. GWAS identifies an NAT2 acetylator status tag single nucleotide polymorphism to be a major locus for skin fluorescence. Diabetologia. 2014; 57(8):1623–1634 doi: .
    1. Mook-Kanamori DO, Selim MM, Takiddin AH, Al-Homsi H, Al-Mahmoud KA, Al-Obaidli A, et al. 1,5-Anhydroglucitol in saliva is a noninvasive marker of short-term glycemic control. J Clin Endocrinol Metab. 2014; 99(3):E479–83 doi: .
    1. Mook-Kanamori MJ, Selim MM, Takiddin AH, Al-Homsi H, Al-Mahmoud KA, Al-Obaidli A, et al. Ethnic and gender differences in advanced glycation end products measured by skin auto-fluorescence. Dermatoendocrinol. 2013; 5(2):325–330 doi: .
    1. Cockcroft DW, Gault MH. Prediction of creatinine clearance from serum creatinine. Nephron. 1976; 16(1):31–41:.
    1. Evans AM, DeHaven CD, Barrett T, Mitchell M, Milgram E. Integrated, nontargeted ultrahigh performance liquid chromatography/electrospray ionization tandem mass spectrometry platform for the identification and relative quantification of the small-molecule complement of biological systems. Anal Chem. 2009; 81(16):6656–6667 doi: .
    1. Ohkuma T, Iwase M, Fujii H, Kaizu S, Ide H, Jodai T, et al. Dose- and time-dependent association of smoking and its cessation with glycemic control and insulin resistance in male patients with type 2 diabetes mellitus: the Fukuoka Diabetes Registry. PLoS One. 2015; 10(3):e0122023 doi: .
    1. Nicholl ID, Stitt AW, Moore JE, Ritchie AJ, Archer DB, Bucala R. Increased levels of advanced glycation endproducts in the lenses and blood vessels of cigarette smokers. Mol Med. 1998; 4(9):594–601:.
    1. Yanbaeva DG, Dentener MA, Creutzberg EC, Wesseling G, Wouters EF. Systemic effects of smoking. Chest. 2007; 131(5):1557–1566 doi: .
    1. Unoki H, Bujo H, Yamagishi S, Takeuchi M, Imaizumi T, Saito Y. Advanced glycation end products attenuate cellular insulin sensitivity by increasing the generation of intracellular reactive oxygen species in adipocytes. Diabetes Res Clin Pract. 2007; 76(2):236–244 doi: .
    1. Cai W, Ramdas M, Zhu L, Chen X, Striker GE, Vlassara H. Oral advanced glycation endproducts (AGEs) promote insulin resistance and diabetes by depleting the antioxidant defenses AGE receptor-1 and sirtuin 1. Proc Natl Acad Sci U S A. 2012; 109(39):15888–15893 doi: .
    1. Goldin A, Beckman JA, Schmidt AM, Creager MA. Advanced glycation end products: sparking the development of diabetic vascular injury. Circulation. 2006; 114(6):597–605 doi: .
    1. Schmidt AM, Hasu M, Popov D, Zhang JH, Chen J, Yan SD, et al. Receptor for advanced glycation end products (AGEs) has a central role in vessel wall interactions and gene activation in response to circulating AGE proteins. Proc Natl Acad Sci U S A. 1994; 91(19):8807–8811:.
    1. Basta G, Lazzerini G, Massaro M, Simoncini T, Tanganelli P, Fu C, et al. Advanced glycation end products activate endothelium through signal-transduction receptor RAGE: a mechanism for amplification of inflammatory responses. Circulation. 2002; 105(7):816–822:.
    1. den Dekker MA, Zwiers M, van den Heuvel ER, de Vos LC, Smit AJ, Zeebregts CJ, et al. Skin autofluorescence, a non-invasive marker for AGE accumulation, is associated with the degree of atherosclerosis. PLoS One. 2013; 8(12):e83084 doi: .
    1. Mulder DJ, van Haelst PL, Gross S, de Leeuw K, Bijzet J, Graaff R, et al. Skin autofluorescence is elevated in patients with stable coronary artery disease and is associated with serum levels of neopterin and the soluble receptor for advanced glycation end products. Atherosclerosis. 2008; 197(1):217–223 doi: .
    1. de Vos LC, Noordzij MJ, Mulder DJ, Smit AJ, Lutgers HL, Dullaart RP, et al. Skin autofluorescence as a measure of advanced glycation end products deposition is elevated in peripheral artery disease. Arterioscler Thromb Vasc Biol. 2013; 33(1):131–138 doi: .
    1. Avila-Tang E, Al-Delaimy WK, Ashley DL, Benowitz N, Bernert JT, Kim S, et al. Assessing secondhand smoke using biological markers. Tob Control. 2013; 22(3):164–171 doi: .
    1. Pirkle JL, Flegal KM, Bernert JT, Brody DJ, Etzel RA, Maurer KR. Exposure of the US population to environmental tobacco smoke: the Third National Health and Nutrition Examination Survey, 1988 to 1991. JAMA. 1996; 275(16):1233–1240:.
    1. Benowitz NL, Bernert JT, Caraballo RS, Holiday DB, Wang J. Optimal serum cotinine levels for distinguishing cigarette smokers and nonsmokers within different racial/ethnic groups in the United States between 1999 and 2004. Am J Epidemiol. 2009; 169(2):236–248 doi: .
    1. Wagenknecht LE, Cutter GR, Haley NJ, Sidney S, Manolio TA, Hughes GH, et al. Racial differences in serum cotinine levels among smokers in the Coronary Artery Risk Development in (Young) Adults study. Am J Public Health. 1990; 80(9):1053–1056:.
    1. Taylor AE, Johnson DC, Kazemi H. Environmental tobacco smoke and cardiovascular disease. A position paper from the Council on Cardiopulmonary and Critical Care, American Heart Association. Circulation. 1992; 86(2):699–702:.
    1. Flouris AD, Vardavas CI, Metsios GS, Tsatsakis AM, Koutedakis Y. Biological evidence for the acute health effects of secondhand smoke exposure. Am J Physiol Lung Cell Mol Physiol. 2010; 298(1):L3–L12 doi: .
    1. Schick S, Glantz S. Philip Morris toxicological experiments with fresh sidestream smoke: more toxic than mainstream smoke. Tob Control. 2005; 14(6):396–404 doi: .
    1. Wang Y, Ji J, Liu YJ, Deng X, He QQ. Passive smoking and risk of type 2 diabetes: a meta-analysis of prospective cohort studies. PLoS One. 2013; 8(7):e69915 doi: .
    1. Barnoya J, Glantz SA. Cardiovascular effects of secondhand smoke: nearly as large as smoking. Circulation. 2005; 111(20):2684–2698 doi: .
    1. Iversen B, Jacobsen BK, Lochen ML. Active and passive smoking and the risk of myocardial infarction in 24,968 men and women during 11 year of follow-up: the Tromso Study. Eur J Epidemiol. 2013; 28(8):659–667 doi: .
    1. Howard DJ, Ota RB, Briggs LA, Hampton M, Pritsos CA. Oxidative stress induced by environmental tobacco smoke in the workplace is mitigated by antioxidant supplementation. Cancer Epidemiol Biomarkers Prev. 1998; 7(11):981–988:.
    1. Facchini FS, Hollenbeck CB, Jeppesen J, Chen YD, Reaven GM. Insulin resistance and cigarette smoking. Lancet. 1992; 339(8802):1128–1130:.
    1. Chowdhury P, Rayford PL, Chang LW. Pathophysiological effects of nicotine on the pancreas. Proc Soc Exp Biol Med. 1998; 218(3):168–173:.
    1. Wannamethee SG, Shaper AG, Perry IJ, British Regional Heart Study. Smoking as a modifiable risk factor for type 2 diabetes in middle-aged men. Diabetes Care. 2001; 24(9):1590–1595:.
    1. Jha P, Ramasundarahettige C, Landsman V, Rostron B, Thun M, Anderson RN, et al. 21st-century hazards of smoking and benefits of cessation in the United States. N Engl J Med. 2013; 368(4):341–350 doi: .
    1. Filozof C, Fernandez Pinilla MC, Fernandez-Cruz A. Smoking cessation and weight gain. Obes Rev. 2004; 5(2):95–103 doi: .
    1. Gepner AD, Piper ME, Johnson HM, Fiore MC, Baker TB, Stein JH. Effects of smoking and smoking cessation on lipids and lipoproteins: outcomes from a randomized clinical trial. Am Heart J. 2011; 161(1):145–151 doi: .
    1. Eliasson B, Attvall S, Taskinen MR, Smith U. Smoking cessation improves insulin sensitivity in healthy middle-aged men. Eur J Clin Invest. 1997; 27(5):450–456:.
    1. Johnson HM, Gossett LK, Piper ME, Aeschlimann SE, Korcarz CE, Baker TB, et al. Effects of smoking and smoking cessation on endothelial function: 1-year outcomes from a randomized clinical trial. J Am Coll Cardiol. 2010; 55(18):1988–1995 doi: .

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