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Published in: Environmental Health and Preventive Medicine 1/2018

Open Access 01-12-2018 | Review article

Association of prenatal and childhood environment smoking exposure with puberty timing: a systematic review and meta-analysis

Authors: Yiwen Chen, Qin Liu, Wenyan Li, Xu Deng, Bo Yang, Xin Huang

Published in: Environmental Health and Preventive Medicine | Issue 1/2018

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Abstract

Objectives

Mothers who smoke during pregnancy or while their children are small were common in some populations. Epidemiological studies have tried to detect the effect of prenatal tobacco smoke (PTS), and childhood environmental tobacco smoke (ETS) on puberty timing have not shown a consensus results. We aimed to examine current evidence and estimate the associations between PTS or/and ETS and puberty timing.

Methods

Seven databases were searched from inception to May 2017. All the cohort studies examining the associations between PTS and/or ETS and puberty timing were identified. Two reviewers independently screened all studies, evaluated the quality of eligible studies, and extracted the data. The quality assessment of the eligible cohort studies was based on the Newcastle-Ottawa Scale. Risk ratio (RR), standard mean difference (SMD), and 95% confidence intervals (CIs) were calculated and pooled by CMA (Version 2.0, Biostat, Inc., USA).

Results

Compared with controls, girls with PTS and ETS exposure have an earlier age at menarche (SMD − 0.087, 95% CI 0.174 to − 0.000), and similar results were found in both PTS subgroup (SMD − 0.097, 95% CI − 0.192 to − 0.002) and prospective cohort subgroup (SMD − 0.171, 95% CI − 0.253 to − 0.090). And number of boys with early voice break in PTS group was significantly increasing than non-exposed boys (RR 1.34, 95% CI 1.29 to 1.40).

Conclusions

PTS exposure possibly decrease age of menarche of girls, and studies on boys were urgent needed. Appropriate and comprehensive outcome measures using unified criteria to classify puberty should be reported in future studies.
Appendix
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Literature
1.
go back to reference Prentice S, Fulford AJ, Jarjou LM, Goldberg GR, Prentice A. Evidence for a downward secular trend in age of menarche in a rural Gambian population. Ann Hum Biol. 2010;37(5):717–21.CrossRefPubMedPubMedCentral Prentice S, Fulford AJ, Jarjou LM, Goldberg GR, Prentice A. Evidence for a downward secular trend in age of menarche in a rural Gambian population. Ann Hum Biol. 2010;37(5):717–21.CrossRefPubMedPubMedCentral
2.
go back to reference Euling SY, Herman-Giddens ME, Lee PA, Selevan SG, Juul A, Sørensen T, et al. Examination of US puberty-timing data from 1940 to 1994 for secular trends: panel findings. Pediatrics. 2008;121(3):172–91.CrossRef Euling SY, Herman-Giddens ME, Lee PA, Selevan SG, Juul A, Sørensen T, et al. Examination of US puberty-timing data from 1940 to 1994 for secular trends: panel findings. Pediatrics. 2008;121(3):172–91.CrossRef
3.
go back to reference Lee PA, Guo SS, Kulin HE. Age of puberty: data from the United States of America. APMIS. 2001;109(103):81–8.CrossRefPubMed Lee PA, Guo SS, Kulin HE. Age of puberty: data from the United States of America. APMIS. 2001;109(103):81–8.CrossRefPubMed
4.
go back to reference Aksglaede L, Sørensen K, Petersen JH, Skakkebaek NE, Juul A. Recent decline in age at breast development: the Copenhagen Puberty Study. Pediatrics. 2009;123(5):932–9.CrossRef Aksglaede L, Sørensen K, Petersen JH, Skakkebaek NE, Juul A. Recent decline in age at breast development: the Copenhagen Puberty Study. Pediatrics. 2009;123(5):932–9.CrossRef
5.
go back to reference Tanner JM. Growth at adolescence: with a general consideration of the effects of hereditary and environmental factors upon growth and maturation from birth to maturity, vol. 2. Oxford: Blackwell Scientific Publications; 1962. p. 326. Tanner JM. Growth at adolescence: with a general consideration of the effects of hereditary and environmental factors upon growth and maturation from birth to maturity, vol. 2. Oxford: Blackwell Scientific Publications; 1962. p. 326.
6.
go back to reference Karpati AM, Rubin CH, Kieszak SM, Marcus M, Troiano RP. Stature and pubertal stage assessment in American boys: the 1988–1994 third National Health and Nutrition Examination Survey. J Adolesc Health. 2002;30(3):205–12.CrossRefPubMed Karpati AM, Rubin CH, Kieszak SM, Marcus M, Troiano RP. Stature and pubertal stage assessment in American boys: the 1988–1994 third National Health and Nutrition Examination Survey. J Adolesc Health. 2002;30(3):205–12.CrossRefPubMed
7.
go back to reference Reiter EO, Lee PA. Have the onset and tempo of puberty changed? Arch Pediatri Adolesc Med. 2011;155(9):988–9.CrossRef Reiter EO, Lee PA. Have the onset and tempo of puberty changed? Arch Pediatri Adolesc Med. 2011;155(9):988–9.CrossRef
8.
go back to reference Neves AG, Kasawara KT, Godoymiranda AC, Oshika FH, Chaim EA, Surita FG. Early menarche and teenager pregnancy as risk factors for morbid obesity among reproductive-age women: a case-control study. Clinics. 2017;72(9):547–53.CrossRefPubMedPubMedCentral Neves AG, Kasawara KT, Godoymiranda AC, Oshika FH, Chaim EA, Surita FG. Early menarche and teenager pregnancy as risk factors for morbid obesity among reproductive-age women: a case-control study. Clinics. 2017;72(9):547–53.CrossRefPubMedPubMedCentral
9.
go back to reference Bubach S, Loret CDM, Hardy R, Dreyfus J, Santos AC, Horta BL. Early menarche and blood pressure in adulthood: systematic review and meta-analysis. J Public Health. 2017;(Suppl(1)):1-9. Bubach S, Loret CDM, Hardy R, Dreyfus J, Santos AC, Horta BL. Early menarche and blood pressure in adulthood: systematic review and meta-analysis. J Public Health. 2017;(Suppl(1)):1-9.
10.
go back to reference Collaborative Group on Hormonal Factors in Breast Cancer. Menarche, menopause, and breast cancer risk: individual participant meta-analysis, including 118964 women with breast cancer from 117 epidemiological studies. Lancet Oncol. 2012;13(11):1141–51.CrossRefPubMedCentral Collaborative Group on Hormonal Factors in Breast Cancer. Menarche, menopause, and breast cancer risk: individual participant meta-analysis, including 118964 women with breast cancer from 117 epidemiological studies. Lancet Oncol. 2012;13(11):1141–51.CrossRefPubMedCentral
11.
go back to reference Carwile JL, Willett WC, Spiegelman D, Hertzmark E, Rich-Edwards J, Frazier AL, Michels KB. Sugar-sweetened beverage consumption and age at menarche in a prospective study of US girls. Hum Reprod. 2015;30(3):675–83.CrossRefPubMedPubMedCentral Carwile JL, Willett WC, Spiegelman D, Hertzmark E, Rich-Edwards J, Frazier AL, Michels KB. Sugar-sweetened beverage consumption and age at menarche in a prospective study of US girls. Hum Reprod. 2015;30(3):675–83.CrossRefPubMedPubMedCentral
12.
go back to reference Mishra GD, Pandeya N, Dobson AJ, Chung HF, Anderson D, Diana K, Sandin S, Giles GG, Bruinsma F, Hayashi K, Lee JS, Mizunuma H, Cade JE, Burley V, Greenwood DC, Goodman A, Simonsen MK, Adami HO, Demakakos P, Weiderpass E. Early menarche, nulliparity and the risk for premature and early natural menopause. Hum Reprod. 2017;32(3):679–86.PubMedPubMedCentral Mishra GD, Pandeya N, Dobson AJ, Chung HF, Anderson D, Diana K, Sandin S, Giles GG, Bruinsma F, Hayashi K, Lee JS, Mizunuma H, Cade JE, Burley V, Greenwood DC, Goodman A, Simonsen MK, Adami HO, Demakakos P, Weiderpass E. Early menarche, nulliparity and the risk for premature and early natural menopause. Hum Reprod. 2017;32(3):679–86.PubMedPubMedCentral
13.
go back to reference Mendle J, Ferrero J. Detrimental psychological outcomes associated with pubertal timing in adolescent boys. Dev Rev. 2012;32(1):49–66.CrossRef Mendle J, Ferrero J. Detrimental psychological outcomes associated with pubertal timing in adolescent boys. Dev Rev. 2012;32(1):49–66.CrossRef
14.
go back to reference Towne B, Czerwinski SA, Demerath EW, Blangero J, Roche AF, Siervogel RM. Heritability of age at menarche in girls from the Fels longitudinal study. Am J Phys Anthropol. 2005;128(1):210–9.CrossRefPubMed Towne B, Czerwinski SA, Demerath EW, Blangero J, Roche AF, Siervogel RM. Heritability of age at menarche in girls from the Fels longitudinal study. Am J Phys Anthropol. 2005;128(1):210–9.CrossRefPubMed
15.
go back to reference Zacharias L, Wurtman RJ. Age at menarche: genetic and environmental influences. N Engl J Med. 1969;280(16):868–75.CrossRefPubMed Zacharias L, Wurtman RJ. Age at menarche: genetic and environmental influences. N Engl J Med. 1969;280(16):868–75.CrossRefPubMed
16.
go back to reference Yermachenko A, Dvornyk V. Nongenetic determinants of age at menarche: a systematic review. Biomed Res Int. 2014;2014(1):371583.PubMedPubMedCentral Yermachenko A, Dvornyk V. Nongenetic determinants of age at menarche: a systematic review. Biomed Res Int. 2014;2014(1):371583.PubMedPubMedCentral
17.
go back to reference Buluş AD, Aşci A, Erkekoglu P, Balci A, Andiran N, Koçer-Gümüşel B. The evaluation of possible role of endocrine disruptors in central and peripheral precocious puberty. Toxicol Mech Methods. 2016;26(7):493–500.CrossRefPubMed Buluş AD, Aşci A, Erkekoglu P, Balci A, Andiran N, Koçer-Gümüşel B. The evaluation of possible role of endocrine disruptors in central and peripheral precocious puberty. Toxicol Mech Methods. 2016;26(7):493–500.CrossRefPubMed
18.
go back to reference Gould GS, Bar-Zeev Y, Bovill M, Atkins L, Gruppetta M, Clarke MJ, et al. Designing an implementation intervention with the Behaviour Change Wheel for health provider smoking cessation care for Australian indigenous pregnant women. Implement Sci. 2017;12(1):114.CrossRefPubMedPubMedCentral Gould GS, Bar-Zeev Y, Bovill M, Atkins L, Gruppetta M, Clarke MJ, et al. Designing an implementation intervention with the Behaviour Change Wheel for health provider smoking cessation care for Australian indigenous pregnant women. Implement Sci. 2017;12(1):114.CrossRefPubMedPubMedCentral
19.
go back to reference Oberg M, Jaakkola MS, Woodward A, Peruga A, Prüss-Ustün A. Worldwide burden of disease from exposure to second-hand smoke: a retrospective analysis of data from 192 countries. Lancet. 2011;377(9760):139–46.CrossRefPubMed Oberg M, Jaakkola MS, Woodward A, Peruga A, Prüss-Ustün A. Worldwide burden of disease from exposure to second-hand smoke: a retrospective analysis of data from 192 countries. Lancet. 2011;377(9760):139–46.CrossRefPubMed
20.
go back to reference Fukuda M, Fukuda K, Shimizu T, Nobunaga M, Byskov AG, Andersen CY. Maternal smoking during pregnancy and age at menarche of premenopausal and postmenopausal daughters. Hum Reprod. 2013;28(2):551–2.CrossRefPubMed Fukuda M, Fukuda K, Shimizu T, Nobunaga M, Byskov AG, Andersen CY. Maternal smoking during pregnancy and age at menarche of premenopausal and postmenopausal daughters. Hum Reprod. 2013;28(2):551–2.CrossRefPubMed
21.
go back to reference Zhang Z, Hartman TJ. Birth weight is associated with age at menarche in US girls. Clin Pediatr. 2014;53(1):82–5.CrossRef Zhang Z, Hartman TJ. Birth weight is associated with age at menarche in US girls. Clin Pediatr. 2014;53(1):82–5.CrossRef
22.
go back to reference Kolasa E, Hulanicka B, Waliszko A. Does exposure to cigarette smoke influence girls’ maturation? Przegl Epidemiol. 1998;52(3):339–50.PubMed Kolasa E, Hulanicka B, Waliszko A. Does exposure to cigarette smoke influence girls’ maturation? Przegl Epidemiol. 1998;52(3):339–50.PubMed
23.
go back to reference Shrestha A, Nohr EA, Bech BH, Ramlau-Hansen CH, Olsen J. Smoking and alcohol use during pregnancy and age of menarche in daughters. Hum Reprod. 2011;26(1):259–65.CrossRefPubMed Shrestha A, Nohr EA, Bech BH, Ramlau-Hansen CH, Olsen J. Smoking and alcohol use during pregnancy and age of menarche in daughters. Hum Reprod. 2011;26(1):259–65.CrossRefPubMed
24.
go back to reference Håkonsen LB, Ernst A, Ramlau-Hansen CH. Maternal cigarette smoking during pregnancy and reproductive health in children: a review of epidemiological studies. Asian J Androl. 2014;16(1):39–49.CrossRefPubMed Håkonsen LB, Ernst A, Ramlau-Hansen CH. Maternal cigarette smoking during pregnancy and reproductive health in children: a review of epidemiological studies. Asian J Androl. 2014;16(1):39–49.CrossRefPubMed
25.
go back to reference Yermachenko A, Dvornyk V. A meta-analysis provides evidence that prenatal smoking exposure decreases age at menarche. Reprod Toxicol. 2015;58:222–8.CrossRefPubMed Yermachenko A, Dvornyk V. A meta-analysis provides evidence that prenatal smoking exposure decreases age at menarche. Reprod Toxicol. 2015;58:222–8.CrossRefPubMed
26.
go back to reference Wells G, Shea BO, O’Connell D, Peterson J, Welch V, Losos M. The Newcastle-Ottawa scale (NOS) for assessing the quality of nonrandomized studies in Meta-analysis. Appl Eng Agric. 2014;18(6):727–34. Wells G, Shea BO, O’Connell D, Peterson J, Welch V, Losos M. The Newcastle-Ottawa scale (NOS) for assessing the quality of nonrandomized studies in Meta-analysis. Appl Eng Agric. 2014;18(6):727–34.
27.
go back to reference Ownby RL, Crocco E, Acevedo A, John V, Loewenstein D. Depression and risk for Alzheimer disease: systematic review, meta-analysis, and meta regression analysis. Arch Gen Psychiatry. 2006;63(5):530–8.CrossRefPubMedPubMedCentral Ownby RL, Crocco E, Acevedo A, John V, Loewenstein D. Depression and risk for Alzheimer disease: systematic review, meta-analysis, and meta regression analysis. Arch Gen Psychiatry. 2006;63(5):530–8.CrossRefPubMedPubMedCentral
28.
go back to reference Sutton AJ, Duval SJ, Tweedie RL, Abrams KR, Jones DR. Empirical assessment of effect of publication bias on meta-analyses. BMJ. 2000;320(7249):1574–7.CrossRefPubMedPubMedCentral Sutton AJ, Duval SJ, Tweedie RL, Abrams KR, Jones DR. Empirical assessment of effect of publication bias on meta-analyses. BMJ. 2000;320(7249):1574–7.CrossRefPubMedPubMedCentral
29.
go back to reference Håkonsen LB, Olsen J, Støvring H, Ernst A, Thulstrup AM, Zhu JL. Maternal cigarette smoking during pregnancy and pubertal development in sons. A follow-up study of a birth cohort. Andrology. 2013;1(2):348–55.CrossRefPubMed Håkonsen LB, Olsen J, Støvring H, Ernst A, Thulstrup AM, Zhu JL. Maternal cigarette smoking during pregnancy and pubertal development in sons. A follow-up study of a birth cohort. Andrology. 2013;1(2):348–55.CrossRefPubMed
30.
go back to reference Ernst A, Kristensen SL, Toft G, Thulstrup AM, Håkonsen LB, Olsen SF. Maternal smoking during pregnancy and reproductive health of daughters: a follow-up study spanning two decades. Hum Reprod. 2012;27(12):3593–600.CrossRefPubMed Ernst A, Kristensen SL, Toft G, Thulstrup AM, Håkonsen LB, Olsen SF. Maternal smoking during pregnancy and reproductive health of daughters: a follow-up study spanning two decades. Hum Reprod. 2012;27(12):3593–600.CrossRefPubMed
31.
go back to reference Windham GC, Zhang L, Longnecker MP, Klebanoff M. Maternal smoking, demographic and lifestyle factors in relation to daughter’s age at menarche. Paediatr Perinat Epidemiol. 2008;22(6):551–61.CrossRefPubMedPubMedCentral Windham GC, Zhang L, Longnecker MP, Klebanoff M. Maternal smoking, demographic and lifestyle factors in relation to daughter’s age at menarche. Paediatr Perinat Epidemiol. 2008;22(6):551–61.CrossRefPubMedPubMedCentral
32.
go back to reference Ferris JS, Flom JD, Tehranifar P, Mayne ST, Terry MB. Prenatal and childhood environmental tobacco smoke exposure and age at menarche. Paediatr Perinat Epidemiol. 2010;24(6):515–23.CrossRefPubMedPubMedCentral Ferris JS, Flom JD, Tehranifar P, Mayne ST, Terry MB. Prenatal and childhood environmental tobacco smoke exposure and age at menarche. Paediatr Perinat Epidemiol. 2010;24(6):515–23.CrossRefPubMedPubMedCentral
33.
34.
go back to reference Behie AM, O'Donnell MH. Prenatal smoking and age at menarche: influence of the prenatal environment on the timing of puberty. Hum Reprod. 2015;30(4):957–62.CrossRefPubMed Behie AM, O'Donnell MH. Prenatal smoking and age at menarche: influence of the prenatal environment on the timing of puberty. Hum Reprod. 2015;30(4):957–62.CrossRefPubMed
35.
go back to reference Windham GC, Bottomley C, Birner C, Fenster L. Age at menarche in relation to maternal use of tobacco, alcohol, coffee, and tea during pregnancy. Am J Epidemiol. 2004;159(9):862–71.CrossRefPubMed Windham GC, Bottomley C, Birner C, Fenster L. Age at menarche in relation to maternal use of tobacco, alcohol, coffee, and tea during pregnancy. Am J Epidemiol. 2004;159(9):862–71.CrossRefPubMed
36.
go back to reference Ramezani Tehrani F, Mirmiran P, Gholami R, Gholami R, Moslehi N, Azizi F, et al. Factors influencing menarcheal age: results from the cohort of Tehran lipid and glucose study. Int J Endocrinol Metab. 2014;12(3):16130.CrossRef Ramezani Tehrani F, Mirmiran P, Gholami R, Gholami R, Moslehi N, Azizi F, et al. Factors influencing menarcheal age: results from the cohort of Tehran lipid and glucose study. Int J Endocrinol Metab. 2014;12(3):16130.CrossRef
37.
go back to reference Rubin C, Maisonet M, Kieszak S, Monteilh C, Holmes A, Flanders D, et al. Timing of maturation and predictors of menarche in girls enrolled in a contemporary British cohort. Paediatr Perinat Epidemiol. 2009;23(5):492–504.CrossRefPubMed Rubin C, Maisonet M, Kieszak S, Monteilh C, Holmes A, Flanders D, et al. Timing of maturation and predictors of menarche in girls enrolled in a contemporary British cohort. Paediatr Perinat Epidemiol. 2009;23(5):492–504.CrossRefPubMed
38.
go back to reference Maisonet M, Christensen KY, Rubin C, Holmes A, Flanders WD, Heron J, et al. Role of prenatal characteristics and early growth on pubertal attainment of British girls. Pediatrics. 2010;126(3):591–600.CrossRef Maisonet M, Christensen KY, Rubin C, Holmes A, Flanders WD, Heron J, et al. Role of prenatal characteristics and early growth on pubertal attainment of British girls. Pediatrics. 2010;126(3):591–600.CrossRef
39.
go back to reference Fried PA, James DS, Watkinson B. Growth and pubertal milestones during adolescence in offspring prenatally exposed to cigarettes and marihuana. Neurotoxicol Teratol. 2001;23(5):431–6.CrossRefPubMed Fried PA, James DS, Watkinson B. Growth and pubertal milestones during adolescence in offspring prenatally exposed to cigarettes and marihuana. Neurotoxicol Teratol. 2001;23(5):431–6.CrossRefPubMed
40.
41.
go back to reference Flom JD, Cohn BA, Tehranifar P, Houghton LC, Wei Y, Protacio A, et al. Earlier age at menarche in girls with rapid early life growth: cohort and within sibling analyses. Ann Epidemiol. 2017;27(7):187–93.CrossRefPubMed Flom JD, Cohn BA, Tehranifar P, Houghton LC, Wei Y, Protacio A, et al. Earlier age at menarche in girls with rapid early life growth: cohort and within sibling analyses. Ann Epidemiol. 2017;27(7):187–93.CrossRefPubMed
42.
go back to reference Dossus L, Kvaskoff M, Bijon A, Fervers B, Boutron-Ruault MC, Mesrine S, et al. Determinants of age at menarche and time to menstrual cycle regularity in the French E3N cohort. Ann Epidemiol. 2012;22(10):723–30.CrossRefPubMed Dossus L, Kvaskoff M, Bijon A, Fervers B, Boutron-Ruault MC, Mesrine S, et al. Determinants of age at menarche and time to menstrual cycle regularity in the French E3N cohort. Ann Epidemiol. 2012;22(10):723–30.CrossRefPubMed
43.
go back to reference Hart R, Sloboda DM, Doherty DA, Norman RJ, Atkinson HC, Newnham JP, et al. Prenatal determinants of uterine volume and ovarian reserve in adolescence. J Clin Endocrinol Metab. 2009;94(12):4931–7.CrossRefPubMed Hart R, Sloboda DM, Doherty DA, Norman RJ, Atkinson HC, Newnham JP, et al. Prenatal determinants of uterine volume and ovarian reserve in adolescence. J Clin Endocrinol Metab. 2009;94(12):4931–7.CrossRefPubMed
44.
go back to reference Morris DH, Jones ME, Schoemaker MJ, Ashworth A, Swerdlow AJ. Determinants of age at menarche in the UK: analyses from the breakthrough generations study. Br J Cancer. 2010;103(11):1760–4.CrossRefPubMedPubMedCentral Morris DH, Jones ME, Schoemaker MJ, Ashworth A, Swerdlow AJ. Determinants of age at menarche in the UK: analyses from the breakthrough generations study. Br J Cancer. 2010;103(11):1760–4.CrossRefPubMedPubMedCentral
45.
46.
go back to reference Ravnborg TL, Jensen TK, Andersson AM, Toppari J, Skakkebaek NE, Jørgensen N. Prenatal and adult exposures to smoking are associated with adverse effects on reproductive hormones, semen quality, final height and body mass index. Hum Reprod. 2011;26(5):1000–11.CrossRefPubMed Ravnborg TL, Jensen TK, Andersson AM, Toppari J, Skakkebaek NE, Jørgensen N. Prenatal and adult exposures to smoking are associated with adverse effects on reproductive hormones, semen quality, final height and body mass index. Hum Reprod. 2011;26(5):1000–11.CrossRefPubMed
47.
go back to reference Carter RC, Jacobson JL, Dodge NC, Granger DA, Jacobson SW. Effects of prenatal alcohol exposure on testosterone and pubertal development. Alcohol Clin Exp Res. 2014;38(6):1671–9.CrossRefPubMedPubMedCentral Carter RC, Jacobson JL, Dodge NC, Granger DA, Jacobson SW. Effects of prenatal alcohol exposure on testosterone and pubertal development. Alcohol Clin Exp Res. 2014;38(6):1671–9.CrossRefPubMedPubMedCentral
48.
go back to reference Liu T, Gatsonis CA, Baylin A, Buka SL. Prenatal exposure to cigarette smoke and benign breast disease. Epidemiology. 2010;21(5):736–43.CrossRefPubMed Liu T, Gatsonis CA, Baylin A, Buka SL. Prenatal exposure to cigarette smoke and benign breast disease. Epidemiology. 2010;21(5):736–43.CrossRefPubMed
49.
go back to reference Sharpe RM. Environmental/lifestyle effects on spermatogenesis. Philos Trans R Soc Lond Ser B Biol Sci. 2010;365(1546):1697–712.CrossRef Sharpe RM. Environmental/lifestyle effects on spermatogenesis. Philos Trans R Soc Lond Ser B Biol Sci. 2010;365(1546):1697–712.CrossRef
50.
go back to reference Jensen TK, Jørgensen N, Punab M, Haugen TB, Suominen J, Zilaitiene B, t al. Association of in utero exposure smoking with reduced semen quality and testis size in adulthood: a crosssectional study of 1,770 young men from the general population in five European countries. Am J Epidemiol. 2004;159(1):49–58.CrossRefPubMed Jensen TK, Jørgensen N, Punab M, Haugen TB, Suominen J, Zilaitiene B, t al. Association of in utero exposure smoking with reduced semen quality and testis size in adulthood: a crosssectional study of 1,770 young men from the general population in five European countries. Am J Epidemiol. 2004;159(1):49–58.CrossRefPubMed
Metadata
Title
Association of prenatal and childhood environment smoking exposure with puberty timing: a systematic review and meta-analysis
Authors
Yiwen Chen
Qin Liu
Wenyan Li
Xu Deng
Bo Yang
Xin Huang
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Environmental Health and Preventive Medicine / Issue 1/2018
Print ISSN: 1342-078X
Electronic ISSN: 1347-4715
DOI
https://doi.org/10.1186/s12199-018-0722-3

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