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Secondhand smoke exposure is associated with proteinuria in children with chronic kidney disease

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Abstract

Background

In adults with chronic kidney disease (CKD), cigarette smoking is associated with an increased risk for CKD progression and transplant failure. In children, secondhand smoke (SHS) exposure has been associated with elevated blood pressure. There are no studies on the prevalence and effect of SHS exposure in CKD.

Methods

Subjects were enrolled in the Chronic Kidney Disease in Children (CKiD) Study, an observational cohort of 366 children aged 1 to 16 years with CKD. Secondhand smoke exposure was obtained via questionnaire. SHS exposure was also determined based on urine cotinine (Ucot) measurements (1 ng/mL ≤ Ucot < 75 ng/mL). The cross-sectional association of SHS exposure with proteinuria was assessed.

Results

Using Ucot, 22 % of subjects were exposed to SHS. SHS exposure was significantly associated with lower maternal education and African American race, and a greater prevalence of nephrotic range proteinuria and left ventricular hypertrophy. In a multivariate model (including sex, age, race, maternal education, income level, private insurance status, abnormal birth history and CKD diagnosis), the prevalence odds of nephrotic range proteinuria was 2.64, (95 % confidence interval 1.08, 6.42) higher in children exposed to SHS compared to those unexposed.

Conclusions

In our cohort of children with CKD, SHS exposure was common (22 %) and independently associated with nephrotic range proteinuria. Exposure to SHS may be an important factor to consider in CKD progression.

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References

  1. Marshall L, Schooley M, Ryan H, Cox P, Easton A, Healton C, Jackson K, Davis KC, Homsi G, Centers for Disease Control and Prevention (2006) Youth tobacco surveillance-united states, 2001–2002. MMWR Surveill Summ 55:1–56

    PubMed  Google Scholar 

  2. Mitsnefes MM (2008) Cardiovascular complications of pediatric chronic kidney disease. Pediatr Nephrol 23:27–39

    Article  PubMed  Google Scholar 

  3. Orth SR, Hallan SI (2008) Smoking: a risk factor for progression of chronic kidney disease and for cardiovascular morbidity and mortality in renal patients—absence of evidence or evidence of absence? Clin J Am Soc Nephrol 3:226–236

    Article  PubMed  Google Scholar 

  4. Zitt N, Kollerits B, Neyer U, Mark W, Heininger D, Mayer G, Kronenberg F, Lhotta K (2007) Cigarette smoking and chronic allograft nephropathy. Nephrol Dial Transplant 22:3034–3039

    Article  CAS  PubMed  Google Scholar 

  5. Yamamoto R, Nagasawa Y, Shoji T, Iwatani H, Hamano T, Kawada N, Inoue K, Uehata T, Kaneko T, Okada N, Moriyama T, Horio M, Yamauchi A, Tsubakihara Y, Imai E, Rakugi H, Isaka Y (2010) Cigarette smoking and progression of IgA nephropathy. Am J Kidney Dis 56:313–324

    Article  CAS  PubMed  Google Scholar 

  6. Jones-Burton C, Seliger SL, Scherer RW, Mishra SI, Vessal G, Brown J, Weir MR, Fink JC (2007) Cigarette smoking and incident chronic kidney disease: a systematic review. Am J Nephrol 27:342–351

    Article  PubMed  Google Scholar 

  7. Hogan SL, Vupputuri S, Guo X, Cai J, Colindres RE, Heiss G, Coresh J (2007) Association of cigarette smoking with albuminuria in the united states: the third national health and nutrition examination survey. Ren Fail 29:133–142

    Article  CAS  PubMed  Google Scholar 

  8. Pijanowska M, Zajaczkowska M (2004) Passive smoking and patterns of 24-hour ambulatory blood pressure in healthy children. Pol Merkur Lekarski 16:320–322

    PubMed  Google Scholar 

  9. Kallio K, Jokinen E, Raitakari OT, Hamalainen M, Siltala M, Volanen I, Kaitosaari T, Viikari J, Ronnemaa T, Simell O (2007) Tobacco smoke exposure is associated with attenuated endothelial function in 11-year-old healthy children. Circulation 115:3205–3212

    Article  CAS  PubMed  Google Scholar 

  10. Neufeld EJ, Mietus-Snyder M, Beiser AS, Baker AL, Newburger JW (1997) Passive cigarette smoking and reduced HDL cholesterol levels in children with high-risk lipid profiles. Circulation 96:1403–1407

    Article  CAS  PubMed  Google Scholar 

  11. Moskowitz WB, Schwartz PF, Schieken RM (1999) Childhood passive smoking, race, and coronary artery disease risk: the MCV twin study. Medical college of Virginia. Arch Pediatr Adolesc Med 153:446–453

    Article  CAS  PubMed  Google Scholar 

  12. Omoloja A, Chand D, Greenbaum L, Wilson A, Bastian V, Ferris M, Bernert J, Stolfi A, Patel H (2010) Cigarette smoking and second-hand smoking exposure in adolescents with chronic kidney disease: a study from the Midwest pediatric nephrology consortium. Nephrol Dial Transplant 26:908–913

    Article  PubMed  Google Scholar 

  13. Caraballo RS, Giovino GA, Pechacek TF (2004) Self-reported cigarette smoking vs. serum cotinine among U.S. adolescents. Nicotine Tob Res 6:19–25

    Article  CAS  PubMed  Google Scholar 

  14. Jones-Burton C, Vessal G, Brown J, Dowling TC, Fink JC (2007) Urinary cotinine as an objective measure of cigarette smoking in chronic kidney disease. Nephrol Dial Transplant 22:1950–1954

    Article  CAS  PubMed  Google Scholar 

  15. Molander L, Hansson A, Lunell E, Alainentalo L, Hoffmann M, Larsson R (2000) Pharmacokinetics of nicotine in kidney failure. Clin Pharmacol Ther 68:250–260

    Article  CAS  PubMed  Google Scholar 

  16. Domino EF (1995) Nontobacco sources of cotinine in the urine of nonsmokers. Clin Pharmacol Ther 57:479

    Article  CAS  PubMed  Google Scholar 

  17. Benowitz NL, Dains KM, Dempsey D, Herrera B, Yu L, Jacob P 3rd (2009) Urine nicotine metabolite concentrations in relation to plasma cotinine during low-level nicotine exposure. Nicotine Tob Res 11:954–960

    Article  CAS  PubMed  Google Scholar 

  18. Furth SL, Cole SR, Moxey-Mims M, Kaskel F, Mak R, Schwartz G, Wong C, Muñoz A, Warady BA (2006) Design and methods of the chronic kidney disease in children (CKiD) prospective cohort study. Clin J Am Soc Nephrol 1:1006–1015

    Google Scholar 

  19. Flynn JT, Mitsnefes M, Pierce C, Cole SR, Parekh RS, Furth SL, Warady BA, Chronic Kidney Disease in Children Study Group (2008) Blood pressure in children with chronic kidney disease: a report from the chronic kidney disease in children study. Hypertension 52:631–637

    Article  CAS  PubMed  Google Scholar 

  20. Bernert JT Jr, Turner WE, Pirkle JL, Sosnoff CS, Akins JR, Waldrep MK, Ann Q, Covey TR, Whitfield WE, Gunter EW, Miller BB, Patterson DG Jr, Needham LL, Hannon WH, Sampson EJ (1997) Development and validation of sensitive method for determination of serum cotinine in smokers and nonsmokers by liquid chromatography/atmospheric pressure ionization tandem mass spectrometry. Clin Chem 43:2281–2291

    CAS  PubMed  Google Scholar 

  21. U.S. Department of Health and Human Services (2006) The Health Consequences of Involuntary Exposure to Tobacco Smoke: A Report of the Surgeon General. U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health

  22. Kallio K, Jokinen E, Hamalainen M, Saarinen M, Volanen I, Kaitosaari T, Viikari J, Ronnemaa T, Simell O, Raitakari OT (2009) Decreased aortic elasticity in healthy 11-year-old children exposed to tobacco smoke. Pediatrics 123:e267–e273

    Article  PubMed  Google Scholar 

  23. Yolton K, Dietrich K, Auinger P, Lanphear BP, Hornung R (2005) Exposure to environmental tobacco smoke and cognitive abilities among U.S. children and adolescents. Environ Health Perspect 113:98–103

    Article  CAS  PubMed  Google Scholar 

  24. Pirkle JL, Flegal KM, Bernert JT, Brody DJ, Etzel RA, Maurer KR (1996) Exposure of the US population to environmental tobacco smoke: the third national health and nutrition examination survey, 1988 to 1991. JAMA 275:1233–1240

    Article  CAS  PubMed  Google Scholar 

  25. National High Blood Pressure Education Program Working Group on High Blood Pressure in Children and Adolescents (2004) The fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. Pediatrics 114:555–576

    Article  Google Scholar 

  26. Soergel M, Kirschstein M, Busch C, Danne T, Gellermann J, Holl R, Krull F, Reichert H, Reusz GS, Rascher W (1997) Oscillometric twenty-four-hour ambulatory blood pressure values in healthy children and adolescents: a multicenter trial including 1141 subjects. J Pediatr 130:178–184

    Article  CAS  PubMed  Google Scholar 

  27. Urbina E, Alpert B, Flynn J, Hayman L, Harshfield GA, Jacobson M, Mahoney L, McCrindle B, Mietus-Snyder M, Steinberger J, Daniels S, American Heart Association Atherosclerosis, Hypertension, and Obesity in Youth Committee (2008) Ambulatory blood pressure monitoring in children and adolescents: recommendations for standard assessment: a scientific statement from the American heart association atherosclerosis, hypertension, and obesity in youth committee of the council on cardiovascular disease in the young and the council for high blood pressure research. Hypertension 52:433–451

    Article  CAS  PubMed  Google Scholar 

  28. Khoury PR, Mitsnefes M, Daniels SR, Kimball TR (2009) Age-specific reference intervals for indexed left ventricular mass in children. J Am Soc Echocardiogr 22:709–714

    Article  PubMed  Google Scholar 

  29. Rubenstein D, Jesty J, Bluestein D (2004) Differences between mainstream and sidestream cigarette smoke extracts and nicotine in the activation of platelets under static and flow conditions. Circulation 109:78–83

    Article  CAS  PubMed  Google Scholar 

  30. Hoegg UR (1972) Cigarette smoke in closed spaces. Environ Health Perspect 2:117–128

    Article  CAS  PubMed  Google Scholar 

  31. Obert DM, Hua P, Pilkerton ME, Feng W, Jaimes EA (2011) Environmental tobacco smoke furthers progression of diabetic nephropathy. Am J Med Sci 341:126–130

    Article  PubMed  Google Scholar 

  32. Boor P, Casper S, Celec P, Hurbankova M, Beno M, Heidland A, Amann K, Sebekova K (2009) Renal, vascular and cardiac fibrosis in rats exposed to passive smoking and industrial dust fibre amosite. J Cell Mol Med 13:4484–4491

    Article  CAS  PubMed  Google Scholar 

  33. Jaimes EA, Tian RX, Raij L (2007) Nicotine: the link between cigarette smoking and the progression of renal injury? Am J Physiol Heart Circ Physiol 292:H76–H82

    Article  CAS  PubMed  Google Scholar 

  34. Taylor AE, Johnson DC, Kazemi H (1992) Environmental tobacco smoke and cardiovascular disease. A position paper from the council on cardiopulmonary and critical care, American Heart Association. Circulation 86:699–702

    Article  CAS  PubMed  Google Scholar 

  35. Mannino DM, Homa DM, Matte T, Hernandez-Avila M (2005) Active and passive smoking and blood lead levels in U.S. adults: data from the third national health and nutrition examination survey. Nicotine Tob Res 7:557–564

    Article  CAS  PubMed  Google Scholar 

  36. Yu CC, Lin JL, Lin-Tan DT (2004) Environmental exposure to lead and progression of chronic renal diseases: a four-year prospective longitudinal study. J Am Soc Nephrol 15:1016–1022

    Article  CAS  PubMed  Google Scholar 

  37. Vaziri ND, Ding Y, Ni Z, Gonick HC (1997) Altered nitric oxide metabolism and increased oxygen free radical activity in lead-induced hypertension: effect of lazaroid therapy. Kidney Int 52:1042–1046

    Article  CAS  PubMed  Google Scholar 

  38. Schwerdt G, Gordjani N, Benesic A, Freudinger R, Wollny B, Kirchhoff A, Gekle M (2006) Chloroacetaldehyde- and acrolein-induced death of human proximal tubule cells. Pediatr Nephrol 21:60–67

    Article  PubMed  Google Scholar 

  39. Jaimes EA, DeMaster EG, Tian RX, Raij L (2004) Stable compounds of cigarette smoke induce endothelial superoxide anion production via NADPH oxidase activation. Arterioscler Thromb Vasc Biol 24:1031–1036

    Article  CAS  PubMed  Google Scholar 

  40. Barnoya J, Glantz SA (2005) Cardiovascular effects of secondhand smoke: nearly as large as smoking. Circulation 111:2684–2698

    Article  PubMed  Google Scholar 

  41. Wakefield M, Banham D, Martin J, Ruffin R, McCaul K, Badcock N (2000) Restrictions on smoking at home and urinary cotinine levels among children with asthma. Am J Prev Med 19:188–192

    Article  CAS  PubMed  Google Scholar 

  42. Oddoze C, Dubus JC, Badier M, Thirion X, Pauli AM, Pastor J, Bruguerolle B (1999) Urinary cotinine and exposure to parental smoking in a population of children with asthma. Clin Chem 45:505–509

    CAS  PubMed  Google Scholar 

  43. Benowitz NL, Kuyt F, Jacob P 3rd, Jones RT, Osman AL (1983) Cotinine disposition and effects. Clin Pharmacol Ther 34:604–611

    Article  CAS  PubMed  Google Scholar 

  44. Chen X, Stanton B, Hopper J, Khankari N (2011) Sources, locations, and predictors of environmental tobacco smoke exposure among young children from inner-city families. J Pediatr Health Care 25:365–372

    Article  PubMed  Google Scholar 

  45. Avila-Tang E, Al-Delaimy WK, Ashley DL, Benowitz N, Bernert JT, Kim S, Samet JM, Hecht SS (2012) Assessing secondhand smoke using biological markers. Tob Control 1:1–2. doi:10.1136/tobaccocontrol-2011-050298

    Google Scholar 

  46. Matsumoto A, Matsumoto A, Ichiba M, Payton NM, Oishi H, Hara M (2012) Simultaneous measurement of urinary total nicotine and cotinine as biomarkers of active and passive smoking among Japanese individuals. Environ Health Prev Med 1:1–2. doi:10.1007/s12199-012-0307-5

    Google Scholar 

  47. Jain R, Balhara YP, Jhanjee S, Sethi H (2012) Concordance between urinary cotinine levels and self-reported tobacco use among drug-dependent persons: a pilot study. Subst Abus 33:99–102

    Article  PubMed  Google Scholar 

  48. Kramer U, Lemmen CH, Behrendt H, Link E, Schafer T, Gostomzyk J, Scherer G, Ring J (2004) The effect of environmental tobacco smoke on eczema and allergic sensitization in children. Br J Dermatol 150:111–118

    Article  CAS  PubMed  Google Scholar 

  49. Dolcini MM, Adler NE, Lee P, Bauman KE (2003) An assessment of the validity of adolescent self-reported smoking using three biological indicators. Nicotine Tob Res 5:473–483

    PubMed  Google Scholar 

  50. Tyc VL, Hovell MF, Winickoff J (2008) Reducing secondhand smoke exposure among children and adolescents: emerging issues for intervening with medically at-risk youth. J Pediatr Psychol 33:145–155

    Article  PubMed  Google Scholar 

  51. Zbikowski SM, Klesges RC, Robinson LA, Alfano CM (2002) Risk factors for smoking among adolescents with asthma. J Adolesc Health 30:279–287

    Article  PubMed  Google Scholar 

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Acknowledgments

We would like to acknowledge the assistance of Adrienne Stolfi in the conceptualization of the project. CKiD is funded by the NIDDK, with additional funding from NINDS, NICHD and NHLBI (U01-DK-66143, U01-DK-66174, and U01-DK-66116). The Clinical Pharmacology Laboratory at the University of California San Francisco receives support from the NIH (S10 RR026437 and P30 DA012393). Funding for urine cotinine and creatinine evaluation was provided by the Research Foundation of Dayton Children’s Medical Center, Dayton, Ohio, USA.

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Correspondence to Abiodun Omoloja.

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The study was presented in part as a platform presentation at the American Society of Pediatric Nephrology Annual Meeting 2011 held at Denver, Colorado.

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Omoloja, A., Jerry-Fluker, J., Ng, D.K. et al. Secondhand smoke exposure is associated with proteinuria in children with chronic kidney disease. Pediatr Nephrol 28, 1243–1251 (2013). https://doi.org/10.1007/s00467-013-2456-1

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  • DOI: https://doi.org/10.1007/s00467-013-2456-1

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