Objective Previous studies regarding the association between parental smoking and the risk of childhood brain tumors (CBT) have reported inconsistent results. We performed a meta-analysis to summarize evidence on this association and to quantify the potential dose-response relationship. Methods A systematic literature search was conducted in the Medline and Embase databases. The summary relative risks (RRs) with 95% confidence intervals (CIs) were calculated. Dose–response meta-analysis was also performed for studies that reported categorical risk estimates for a series of smoking exposure levels. Results A total of 17 studies fulfilled the inclusion criteria. In the meta-analyses, the summary RRs (95% CIs) of CBT for maternal smoking during pregnancy, paternal smoking during pregnancy, maternal smoking before pregnancy, and paternal smoking before pregnancy were 0.96 (0.86–1.07), 1.09 (0.97–1.22), 0.93 (0.85–1.00), and 1.09 (1.00–1.20), respectively. Dose-response meta-analysis also showed no significant association between parental smoking and the risk of CBT. Conclusions Findings from our meta-analysis indicate that parental smoking may not be associated with a risk of CBT.
References
[1]
Mueller S, Chang S (2009) Pediatric brain tumors: current treatment strategies and future therapeutic approaches. Neurotherapeutics 6: 570–586. doi: 10.1016/j.nurt.2009.04.006
[2]
Gajjar A, Packer RJ, Foreman NK, Cohen K, Haas-Kogan D, et al. (2013) Children's Oncology Group's 2013 blueprint for research: central nervous system tumors. Pediatr Blood Cancer 60: 1022–1026. doi: 10.1002/pbc.24427
[3]
Kyritsis AP, Bondy ML, Rao JS, Sioka C (2010) Inherited predisposition to glioma. Neuro Oncol 12: 104–113. doi: 10.1093/neuonc/nop011
[4]
Giovino GA, Mirza SA, Samet JM, Gupta PC, Jarvis MJ, et al. (2012) Tobacco use in 3 billion individuals from 16 countries: an analysis of nationally representative cross-sectional household surveys. Lancet 380: 668–679. doi: 10.1016/s0140-6736(12)61085-x
[5]
Klip H, Burger CW, de Kraker J, van Leeuwen FE (2001) Risk of cancer in the offspring of women who underwent ovarian stimulation for IVF. Hum Reprod 16: 2451–2458.
[6]
Anderson LM, Hecht SS, Dixon DE, Dove LF, Kovatch RM, et al. (1989) Evaluation of the transplacental tumorigenicity of the tobacco-specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-bu？tanonein mice. Cancer Res 49: 3770–3775.
[7]
Balansky R, Ganchev G, Iltcheva M, Nikolov M, Steele VE, et al. (2012) Differential carcinogenicity of cigarette smoke in mice exposed either transplacentally, early in life or in adulthood. Int J Cancer 130: 1001–1010. doi: 10.1002/ijc.26103
[8]
Izzotti A, Balansky RM, Cartiglia C, Camoirano A, Longobardi M, et al. (2003) Genomic and transcriptional alterations in mouse fetus liver after transplacental exposure to cigarette smoke. FASEB J 17: 1127–1129. doi: 10.1096/fj.02-0967fje
[9]
Lackmann GM, Salzberger U, Tollner U, Chen M, Carmella SG, et al. (1999) Metabolites of a tobacco-specific carcinogen in urine from newborns. J Natl Cancer Inst 91: 459–465. doi: 10.1093/jnci/91.5.459
[10]
Florek E, Piekoszewski W, Basior A, Merritt AT, Mazela J, et al. (2011) Effect of maternal tobacco smoking or exposure to second-hand smoke on the levels of 4-(methylnitrosamino)-1-(3-pyridyl)-1-bu？tanol(NNAL) in urine of mother and the first urine of newborn. J Physiol Pharmacol 62: 377–383.
[11]
Milunsky A, Carmella SG, Ye M, Hecht SS (2000) A tobacco-specific carcinogen in the fetus. Prenat Diagn 20: 307–310. doi: 10.1002/(sici)1097-0223(200004)20:4<307::aid-pd797>3.0.co;2-m
[12]
Brooks DR, Mucci LA, Hatch EE, Cnattingius S (2004) Maternal smoking during pregnancy and risk of brain tumors in the offspring. A prospective study of 1.4 million Swedish births. Cancer Causes Control 15: 997–1005. doi: 10.1007/s10552-004-1123-z
[13]
Filippini G, Farinotti M, Ferrarini M (2000) Active and passive smoking during pregnancy and risk of central nervous system tumours in children. Paediatr Perinat Epidemiol 14: 78–84. doi: 10.1046/j.1365-3016.2000.00230.x
[14]
Pang D, McNally R, Birch JM (2003) Parental smoking and childhood cancer: results from the United Kingdom Childhood Cancer Study. Br J Cancer 88: 373–381.
[15]
Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, et al. (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283: 2008–2012. doi: 10.1001/jama.283.15.2008
[16]
Greenland S (1987) Quantitative methods in the review of epidemiologic literature. Epidemiol Rev 9: 1–30.
[17]
DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7: 177–188. doi: 10.1016/0197-2456(86)90046-2
[18]
Greenland S, Longnecker MP (1992) Methods for trend estimation from summarized dose-response data, with applications to meta-analysis. Am J Epidemiol 135: 1301–1309.
[19]
Orsini N, Li R, Wolk A, Khudyakov P, Spiegelman D (2012) Meta-analysis for linear and nonlinear dose-response relations: examples, an evaluation of approximations, and software. Am J Epidemiol 175: 66–73. doi: 10.1093/aje/kwr265
[20]
Harrell FE Jr, Lee KL, Pollock BG (1988) Regression models in clinical studies: determining relationships between predictors and response. J Natl Cancer Inst 80: 1198–1202. doi: 10.1093/jnci/80.15.1198
[21]
Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21: 1539–1558. doi: 10.1002/sim.1186
[22]
Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50: 1088–1101. doi: 10.2307/2533446
[23]
Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315: 629–634. doi: 10.1136/bmj.315.7109.629
[24]
Milne E, Greenop KR, Scott RJ, Ashton LJ, Cohn RJ, et al. (2013) Parental smoking and risk of childhood brain tumors. Int J Cancer 133: 253–259. doi: 10.1002/ijc.28004
[25]
Barrington-Trimis JL, Searles Nielsen S, Preston-Martin S, Gauderman WJ, Holly EA, et al. (2013) Parental smoking and risk of childhood brain tumors by functional polymorphisms in polycyclic aromatic hydrocarbon metabolism genes. PLoS One 8: e79110. doi: 10.1371/journal.pone.0079110
[26]
Stavrou EP, Baker DF, Bishop JF (2009) Maternal smoking during pregnancy and childhood cancer in New South Wales: a record linkage investigation. Cancer Causes Control 20: 1551–1558. doi: 10.1007/s10552-009-9400-5
[27]
Plichart M, Menegaux F, Lacour B, Hartmann O, Frappaz D, et al. (2008) Parental smoking, maternal alcohol, coffee and tea consumption during pregnancy and childhood malignant central nervous system tumours: the ESCALE study (SFCE). Eur J Cancer Prev 17: 376–383. doi: 10.1097/cej.0b013e3282f75e6f
[28]
Filippini G, Maisonneuve P, McCredie M, Peris-Bonet R, Modan B, et al. (2002) Relation of childhood brain tumors to exposure of parents and children to tobacco smoke: the SEARCH international case-control study. Surveillance of Environmental Aspects Related to Cancer in Humans. Int J Cancer 100: 206–213. doi: 10.1002/ijc.10465
[29]
Schuz J, Kaletsch U, Kaatsch P, Meinert R, Michaelis J (2001) Risk factors for pediatric tumors of the central nervous system: results from a German population-based case-control study. Med Pediatr Oncol 36: 274–282. doi: 10.1002/1096-911x(20010201)36:2<274::aid-mpo1065>3.3.co;2-4
[30]
Hu J, Mao Y, Ugnat AM (2000) Parental cigarette smoking, hard liquor consumption and the risk of childhood brain tumors—a case-control study in northeast China. Acta Oncol 39: 979–984. doi: 10.1080/02841860050215972
[31]
Ji BT, Shu XO, Linet MS, Zheng W, Wacholder S, et al. (1997) Paternal cigarette smoking and the risk of childhood cancer among offspring of nonsmoking mothers. J Natl Cancer Inst 89: 238–244. doi: 10.1093/jnci/89.3.238
[32]
Bunin GR, Buckley JD, Boesel CP, Rorke LB, Meadows AT (1994) Risk factors for astrocytic glioma and primitive neuroectodermal tumor of the brain in young children: a report from the Children's Cancer Group. Cancer Epidemiol Biomarkers Prev 3: 197–204.
[33]
Gold EB, Leviton A, Lopez R, Gilles FH, Hedley-Whyte ET, et al. (1993) Parental smoking and risk of childhood brain tumors. Am J Epidemiol 137: 620–628.
[34]
John EM, Savitz DA, Sandler DP (1991) Prenatal exposure to parents' smoking and childhood cancer. Am J Epidemiol 133: 123–132.
[35]
Kuijten RR, Bunin GR, Nass CC, Meadows AT (1990) Gestational and familial risk factors for childhood astrocytoma: results of a case-control study. Cancer Res 50: 2608–2612.
[36]
Howe GR, Burch JD, Chiarelli AM, Risch HA, Choi BC (1989) An exploratory case-control study of brain tumors in children. Cancer Res 49: 4349–4352.
[37]
Stjernfeldt M, Ludvigsson J, Berglund K, Lindsten J (1986) Maternal smoking during pregnancy and the risk of childhood cancer. Lancet 2: 687–688. doi: 10.1016/s0140-6736(86)91664-8
[38]
Pollack IF, Jakacki RI (2011) Childhood brain tumors: epidemiology, current management and future directions. Nat Rev Neurol 7: 495–506. doi: 10.1038/nrneurol.2011.110
[39]
Vinchon M, Leblond P, Caron S, Delestret I, Baroncini M, et al. (2011) Radiation-induced tumors in children irradiated for brain tumor: a longitudinal study. Childs Nerv Syst 27: 445–453. doi: 10.1007/s00381-011-1390-4
[40]
Baldwin RT, Preston-Martin S (2004) Epidemiology of brain tumors in childhood—a review. Toxicol Appl Pharmacol 199: 118–131. doi: 10.1016/j.taap.2003.12.029
[41]
Bunin GR, Robison LL, Biegel JA, Pollack IF, Rorke-Adams LB (2006) Parental heat exposure and risk of childhood brain tumor: a Children's Oncology Group study. Am J Epidemiol 164: 222–231. doi: 10.1093/aje/kwj174
[42]
Hargreave M, Jensen A, Toender A, Andersen KK, Kjaer SK (2013) Fertility treatment and childhood cancer risk: a systematic meta-analysis. Fertil Steril 100: 150–161. doi: 10.1016/j.fertnstert.2013.03.017
[43]
Huncharek M, Kupelnick B, Klassen H (2002) Maternal smoking during pregnancy and the risk of childhood brain tumors: a meta-analysis of 6566 subjects from twelve epidemiological studies. J Neurooncol 57: 51–57.
[44]
Flenady V, Koopmans L, Middleton P, Froen JF, Smith GC, et al. (2011) Major risk factors for stillbirth in high-income countries: a systematic review and meta-analysis. Lancet 377: 1331–1340. doi: 10.1016/s0140-6736(10)62233-7
[45]
Oken E, Levitan EB, Gillman MW (2008) Maternal smoking during pregnancy and child overweight: systematic review and meta-analysis. Int J Obes (Lond) 32: 201–210. doi: 10.1038/sj.ijo.0803760
[46]
Antonopoulos CN, Sergentanis TN, Papadopoulou C, Andrie E, Dessypris N, et al. (2011) Maternal smoking during pregnancy and childhood lymphoma: a meta-analysis. Int J Cancer 129: 2694–2703. doi: 10.1002/ijc.25929
[47]
Klimentopoulou A, Antonopoulos CN, Papadopoulou C, Kanavidis P, Tourvas AD, et al. (2012) Maternal smoking during pregnancy and risk for childhood leukemia: a nationwide case-control study in Greece and meta-analysis. Pediatr Blood Cancer 58: 344–351. doi: 10.1002/pbc.23347
[48]
Tuomisto J, Holl K, Rantakokko P, Koskela P, Hallmans G, et al. (2009) Maternal smoking during pregnancy and testicular cancer in the sons: a nested case-control study and a meta-analysis. Eur J Cancer 45: 1640–1648. doi: 10.1016/j.ejca.2009.01.017
[49]
Linschooten JO, Verhofstad N, Gutzkow K, Olsen AK, Yauk C, et al. (2013) Paternal lifestyle as a potential source of germline mutations transmitted to offspring. FASEB J 27: 2873–2879. doi: 10.1096/fj.13-227694
[50]
Laubenthal J, Zlobinskaya O, Poterlowicz K, Baumgartner A, Gdula MR, et al. (2012) Cigarette smoke-induced transgenerational alterations in genome stability in cord blood of human F1 offspring. FASEB J 26: 3946–3956. doi: 10.1096/fj.11-201194
[51]
Rice JM (2004) Causation of nervous system tumors in children: insights from traditional and genetically engineered animal models. Toxicol Appl Pharmacol 199: 175–191. doi: 10.1016/j.taap.2003.12.031
[52]
Tredaniel J, Boffetta P, Little J, Saracci R, Hirsch A (1994) Exposure to passive smoking during pregnancy and childhood, and cancer risk: the epidemiological evidence. Paediatr Perinat Epidemiol 8: 233–255. doi: 10.1111/j.1365-3016.1994.tb00455.x
[53]
Florescu A, Ferrence R, Einarson T, Selby P, Soldin O, et al. (2009) Methods for quantification of exposure to cigarette smoking and environmental tobacco smoke: focus on developmental toxicology. Ther Drug Monit 31: 14–30. doi: 10.1097/ftd.0b013e3181957a3b
[54]
Searles Nielsen S, Dills RL, Glass M, Mueller BA (2014) Accuracy of prenatal smoking data from Washington State birth certificates in a population-based sample with cotinine measurements. Ann Epidemiol 24: 236–239. doi: 10.1016/j.annepidem.2013.12.008
[55]
Murphy SE, Wickham KM, Lindgren BR, Spector LG, Joseph A (2013) Cotinine and trans 3'-hydroxycotinine in dried blood spots as biomarkers of tobacco exposure and nicotine metabolism. J Expo Sci Environ Epidemiol 23: 513–518. doi: 10.1038/jes.2013.7
[56]
Yang J, Pearl M, Jacob P III, DeLorenze GN, Benowitz NL, et al. (2013) Levels of cotinine in dried blood specimens from newborns as a biomarker of maternal smoking close to the time of delivery. Am J Epidemiol 178: 1648–1654. doi: 10.1093/aje/kwt182
[57]
Larsson SC, Orsini N, Wolk A (2010) Vitamin B6 and risk of colorectal cancer: a meta-analysis of prospective studies. JAMA 303: 1077–1083. doi: 10.1001/jama.2010.263
