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Childhood body mass index at 5.5 years mediates the effect of prenatal maternal stress on daughters’ age at menarche: Project Ice Storm

Published online by Cambridge University Press:  28 December 2016

A. Duchesne ,
A. Liu ,
S. L. Jones ,
D. P. Laplante Open the ORCID record for D. P. Laplante [Opens in a new window]  and
S. King
A. Duchesne
Affiliation:
Department of Psychology, University of Toronto, Toronto, ON, Canada
A. Liu
Affiliation:
Douglas Mental Health University Institute, McGill University, Montreal, QC, Canada
S. L. Jones
Affiliation:
Douglas Mental Health University Institute, McGill University, Montreal, QC, Canada Department of Psychiatry, McGill University, Montreal, QC, Canada
D. P. Laplante
Affiliation:
Douglas Mental Health University Institute, McGill University, Montreal, QC, Canada
S. King*
Affiliation:
Douglas Mental Health University Institute, McGill University, Montreal, QC, Canada Department of Psychiatry, McGill University, Montreal, QC, Canada
*
*Address for correspondence: S. King, Douglas Mental Health University Institute, 6875 LaSalle Blvd, Verdun, QC, Canada, H4H 1R3. (Email Suzanne.king@mcgill.ca)
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Abstract

Early pubertal timing is known to put women at greater risk for adverse physiological and psychological health outcomes. Of the factors that influence girls’ pubertal timing, stress experienced during childhood has been found to advance age at menarche (AAM). However, it is not known if stress experienced by mothers during or in the months before conception can be similarly associated with earlier pubertal timing. Prenatal maternal stress (PNMS) is associated with metabolic changes, such as increased childhood adiposity and risk of obesity, that have been associated with earlier menarchal age. Using a prospective longitudinal design, the present study tested whether PNMS induced by a natural disaster is either directly associated with earlier AAM, or whether there is an indirect association mediated through increased girls’ body mass index (BMI) during childhood. A total of 31 girls, whose mothers were exposed to the Quebec’s January 1998 ice storm during pregnancy were followed from 6 months to 5 1/2 to 5.5 years of age. Mother’s stress was measured within 6 months of the storm. BMI was measured at 5.5 years, and AAM was assessed through teen’s self-report at 13.5 and 15.5 years of age. Results revealed that greater BMI at 5.5 years mediated the effect of PNMS on decreasing AAM [B=−0.059, 95% confidence intervals (−0.18, −0.0035)]. The present study is the first to demonstrate that maternal experience of stressful conditions during pregnancy reduces AAM in the offspring through its effects on childhood BMI. Future research should consider the impact of AAM on other measures of reproductive ability.

Keywords

age at menarchebody mass indexprenatal maternal stressProject Ice Stormpuberty

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Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 8 , Issue 2 , April 2017 , pp. 168 - 177
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© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2016 

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References

1. Choi, J-H, Yoo, H-W. Control of puberty: genetics, endocrinology, and environment. Curr Opin Endocrinol Diabetes Obes. 2013; 20, 62–68.CrossRefGoogle ScholarPubMed
2. Canoy, D, Beral, V, Balkwill, A, et al. Age at menarche and risks of coronary heart and other vascular diseases in a large UK cohort. Circulation. 2015; 131, 237–244.Google Scholar
3. He, C, Zhang, C, Hunter, DJ, et al. Age at menarche and risk of type 2 diabetes: results from 2 large prospective cohort studies. Am J Epidemiol. 2010; 171, 334–344.Google Scholar
4. Janghorbani, M, Mansourian, M, Hosseini, E. Systematic review and meta-analysis of age at menarche and risk of type 2 diabetes. Acta Diabetol. 2014; 51, 519–528.Google Scholar
5. Berkey, CS, Frazier, AL, Gardner, JD, Colditz, GA. Adolescence and breast carcinoma risk. Cancer. 1999; 85, 2400–2409.Google Scholar
6. Hsieh, CC, Trichopoulos, D, Katsouyanni, K, Yuasa, S. Age at menarche, age at menopause, height and obesity as risk factors for breast cancer: associations and interactions in an international case-control study. Int J Cancer. 1990; 46, 796–800.CrossRefGoogle Scholar
7. Karageorgi, S, Hankinson, SE, Kraft, P, De Vivo, I. Reproductive factors and postmenopausal hormone use in relation to endometrial cancer risk in the Nurses’ Health Study cohort 1976–2004. Int J Cancer. 2010; 126, 208–216.Google Scholar
8. Rosner, B, Colditz, GA, Willett, WC. Reproductive risk factors in a prospective study of breast cancer: the Nurses’ Health Study. Am J Epidemiol. 1994; 139, 819–835.CrossRefGoogle Scholar
9. Black, SR, Klein, DN. Early menarcheal age and risk for later depressive symptomatology: the role of childhood depressive symptoms. J Youth Adolesc. 2012; 41, 1142–1150.Google Scholar
10. Colich, NL, Foland-Ross, LC, Eggleston, C, Singh, MK, Gotlib, IH. Neural aspects of inhibition following emotional primes in depressed adolescents. J Clin Child Adolesc Psychol. 2016; 45, 21–30.CrossRefGoogle ScholarPubMed
11. Culpin, I, Heron, J, Araya, R, Joinson, C. Early childhood father absence and depressive symptoms in adolescent girls from a UK cohort: the mediating role of early menarche. J Abnorm Child Psychol. 2015; 43, 921–931.Google Scholar
12. Toffol, E, Koponen, P, Luoto, R, Partonen, T. Pubertal timing, menstrual irregularity, and mental health: results of a population-based study. Arch Womens Ment Health. 2013; 17, 127–135.Google Scholar
13. Trépanier, L, Juster, R-P, Marin, M-F, et al. Early menarche predicts increased depressive symptoms and cortisol levels in Quebec girls ages 11 to 13. Dev Psychopathol. 2013; 25(Pt 1), 1017–1027.Google Scholar
14. Baams, L, Dubas, JS, Overbeek, G, van Aken, MAG. Transitions in body and behavior: a meta-analytic study on the relationship between pubertal development and adolescent sexual behavior. J Adolesc Health. 2015; 56, 586–598.Google Scholar
15. Vaughan, EB, Van Hulle, CA, Beasley, WH, Rodgers, JL, D’Onofrio, BM. Clarifying the associations between age at menarche and adolescent emotional and behavioral problems. J Youth Adolesc. 2015; 44, 922–939.Google Scholar
16. Herrenkohl, LR. Prenatal stress reduces fertility and fecundity in female offspring. Science. 1979; 206, 1097–1099.Google Scholar
17. Frye, CA, Orecki, ZA. Prenatal stress alters reproductive responses of rats in behavioral estrus and paced mating of hormone-primed rats. Horm Behav . 2002; 42, 472–483.CrossRefGoogle ScholarPubMed
18. Anderson, DK, Rhees, RW, Fleming, DE. Effects of prenatal stress on differentiation of the sexually dimorphic nucleus of the preoptic area (SDN-POA) of the rat brain. Brain Res. 1985; 332, 113–118.Google Scholar
19. Moyer, JA, Herrenkohl, LR, Jacobowitz, DM. Stress during pregnancy: effect on catecholamines in discrete brain regions of offspring as adults. Brain Res. 1978; 144, 173–178.CrossRefGoogle ScholarPubMed
20. Tahirović, HF. Menarchal age and the stress of war: an example from Bosnia. Eur J Pediatr. 1998; 157, 978–980.Google Scholar
21. Mendle, J, Leve, LD, Van Ryzin, M, Natsuaki, MN, Ge, X. Associations between early life stress, child maltreatment, and pubertal development among girls in foster care. J Res Adolesc. 2011; 21, 871–880.Google Scholar
22. Boynton-Jarrett, R, Wright, RJ, Putnam, FW, et al. Childhood abuse and age at menarche. J Adolesc Health. 2013; 52, 241–247.Google Scholar
23. Belsky, J, Steinberg, L, Houts, RM, Halpern-Felsher, BL. The development of reproductive strategy in females: early maternal harshness --> earlier menarche --> increased sexual risk taking. Dev Psychol. 2010; 46, 120–128.Google Scholar
24. Moffitt, TE, Caspi, A, Belsky, J, Silva, PA. Childhood experience and the onset of menarche: a test of a sociobiological model. Child Dev. 1992; 63, 47–58.Google Scholar
25. Wierson, M, Long, PJ. Forehand RL. Toward a new understanding of early menarche: the role of environmental stress in pubertal timing. Adolescence. 1993; 28, 913–924.Google Scholar
26. Ellis, BJ, Garber, J. Psychosocial antecedents of variation in girls’ pubertal timing: maternal depression, stepfather presence, and marital and family stress. Child Dev. 2000; 71, 485–501.Google Scholar
27. Dancause, KN, Laplante, DP, Fraser, S, et al. Prenatal exposure to a natural disaster increases risk for obesity in 5 ${\raise0.7ex\hbox{$1$} \!\mathord{\left/ {\vphantom {1 2}}\right.\kern-\nulldelimiterspace}\!\lower0.7ex\hbox{$2$}}$ year old children. Pediatr Res. 2012; 71, 126–131.CrossRefGoogle Scholar
28. Dancause, KN, Laplante, DP, Hart, KJ, et al. Prenatal stress due to a natural disaster predicts adiposity in childhood: the Iowa Flood Study. J Obes. 2015; 2015, 570541.CrossRefGoogle ScholarPubMed
29. Hohwu, L, Zhu, JL, Graversen, L, et al. Prenatal parental separation and body weight, including development of overweight and obesity later in childhood. PLoS One. 2015; 10, e0119138.Google Scholar
30. Bhat, SK, Beilin, LJ, Robinson, M, Burrows, S, Mori, TA. Contrasting effects of prenatal life stress on blood pressure and body mass index in young adults. J Hypertens. 2015; 33, 711–719, ; discussion 719.Google Scholar
31. Stout, SA, Espel, EV, Sandman, CA, Glynn, LM, Davis, EP. Fetal programming of children’s obesity risk. Psychoneuroendocrinology. 2015; 53, 29–39.Google Scholar
32. Dancause, KN, Veru, F, Andersen, RE, Laplante, DP, King, S. Prenatal stress due to a natural disaster predicts insulin secretion in adolescence. Early Hum Dev. 2013; 89, 773–776.CrossRefGoogle ScholarPubMed
33. Ong, KK, Emmett, P, Northstone, K, et al. Infancy weight gain predicts childhood body fat and age at menarche in girls. J Clin Endocrinol Metab. 2009; 94, 1527–1532.Google Scholar
34. Dunger, DB, Ahmed, ML, Ong, KK. Early and late weight gain and the timing of puberty. Mol Cell Endocrinol. 2006; 254–255, 140–145.Google Scholar
35. Marcovecchio, ML, Chiarelli, F. Obesity and growth during childhood and puberty. World Rev Nutr Diet. 2013; 106, 135–141.Google Scholar
36. Pinkney, J, Streeter, A, Hosking, J, et al. Adiposity, chronic inflammation, and the prepubertal decline of sex hormone binding globulin in children: evidence for associations with the timing of puberty (Earlybird 58). J Clin Endocrinol Metab. 2014; 99, 3224–3232.Google Scholar
37. Salgin, B, Norris, SA, Prentice, P, et al. Even transient rapid infancy weight gain is associated with higher BMI in young adults and earlier menarche. Int J Obes. 2015; 39, 939–944.Google Scholar
38. King, S, Dancause, K, Turcotte-Tremblay, A-M, Veru, F, Laplante, DP. Using natural disasters to study the effects of prenatal maternal stress on child health and development. Birth Defects Res C Embryo Today. 2012; 96, 273–288.CrossRefGoogle Scholar
39. Cheng, ER, Park, H-J, Wisk, LE, et al. Examining the link between women’s exposure to stressful life events prior to conception and infant and toddler health: the role of birth weight. J Epidemiol Community Health. 2016; 70, 245–252.Google Scholar
40. Heijmans, BT, Tobi, EW, Stein, AD, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci USA. 2008; 105, 17046–17049.Google Scholar
41. Nuckolls, KB, Kaplan, BH, Cassel, J. Psychosocial assets, life crisis and the prognosis of pregnancy. Am J Epidemiol. 1972; 95, 431–441.Google Scholar
42. Ryzhavskii, BY, Sokolova, TV, Fel’dsherov, YI, et al. Effect of emotional stress in pregnant rats on brain development of their progeny. Bull Exp Biol Med. 2001; 132, 737–740.Google Scholar
43. Shachar-Dadon, A, Schulkin, J, Leshem, M. Adversity before conception will affect adult progeny in rats. Dev Psychol. 2009; 45, 9–16.Google Scholar
44. Witt, WP, Litzelman, K, Cheng, ER, Wakeel, F, Barker, ES. Measuring stress before and during pregnancy: a review of population-based studies of obstetric outcomes. Matern Child Health J. 2014; 18, 52–63.Google Scholar
45. Zaidan, H, Gaisler-Salomon, I. Prereproductive stress in adolescent female rats affects behavior and corticosterone levels in second-generation offspring. Psychoneuroendocrinology. 2015; 58, 120–129.Google Scholar
46. Laplante, DP, Zelazo, PR, Brunet, A, King, S. Functional play at 2 years of age: effects of prenatal maternal stress. Infancy. 2007; 12, 69–93.Google Scholar
47. Koo, MM, Rohan, TE. Accuracy of short-term recall of age at menarche. Ann Hum Biol. 1997; 24, 61–64.CrossRefGoogle ScholarPubMed
48. Petersen, AC, Crockett, L, Richards, M, Boxer, A. A self-report measure of pubertal status: reliability, validity, and initial norms. J Youth Adolesc. 1988; 17, 117–133.Google Scholar
49. Bromet, E, Dew, MA. Review of psychiatric epidemiologic research on disasters. Epidemiol Rev. 1995; 17, 113–119.Google Scholar
50. McFarlane, AC. Relationship between psychiatric impairment and a natural disaster: the role of distress. Psychol Med. 1988; 18, 129–139.Google Scholar
51. Brunet, A, St-Hilaire, A, Jehel, L, King, S. Validation of a French version of the Impact of Event Scale – Revised. Can J Psychiatry. 2003; 48, 55–60.Google Scholar
52. Weiss, DS, Marmar, CR. The Impact of Event Scale – Revised. In Assessing Psychological Trauma and PTSD: A Practitioner’s Handbook (eds. Wilson JP, Keane TM), 1997; pp. 399–411. Guilford: New York.Google Scholar
53. Kuczmarski, RJ, Ogden, CL, Grummer-Strawn, LM, et al. CDC growth charts: United States. Adv Data. 2000; (314), 1–27.Google Scholar
54. Fay, RA, Dey, PL, Saadie, CM, Buhl, JA, Gebski, VJ. Ponderal index: a better definition of the ‘at risk’ group with intrauterine growth problems than birth-weight for gestational age in term infants. Aust N Z J Obstet Gynaecol. 1991; 31, 17–19.Google Scholar
55. Khoury, MJ, Berg, CJ, Calle, EE. The ponderal index in term newborn siblings. Am J Epidemiol. 1990; 132, 576–583.Google Scholar
56. Hollingshead, AB. Four-Factor Index of Social Status. 1973. Yale University Press: New Haven, CT.Google Scholar
57. Jacobsen, B, Kinney, DK. Perinatal complications in adopted and non-adopted samples of schizophrenics and controls. Acta Psychiatr Scand. 1980; 62(Suppl. 285), 337–346.Google Scholar
58. McNeil, TF, Sjöström, K. The McNeil–Sjöström OC Scale: A Comprehensive Scale for Measuring Obstetric Complications.Department of Psychiatry, Lund University, New York; 1994.Google Scholar
59. Sarason, IG, Johnson, JH, Siegel, JM. Assessing the impact of life changes: development of the Life Experience Survey. J Consult Clin Psychol. 1978; 46, 932–946.Google Scholar
60. Yermachenko, A, Dvornyk, V. Nongenetic determinants of age at menarche: a systematic review. Biomed Res Int. 2014; 2014, 371583.Google Scholar
61. Hayes, AF. Introduction to Mediation, Moderation, and Conditional Process Analysis. 2013. The Guilford Press: New York.Google Scholar
62. 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, 551–561.Google Scholar
63. Dubois, L, Girard, M. Early determinants of overweight at 4.5 years in a population-based longitudinal study. Int J Obes. 2006; 30, 610–617.Google Scholar
64. 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, 957–962.Google Scholar
65. Ernst, A, Kristensen, SL, Toft, G, et al. Maternal smoking during pregnancy and reproductive health of daughters: a follow-up study spanning two decades. Hum Reprod. 2012; 27, 3593–3600.Google Scholar
66. Windham, GC. Age at menarche in relation to maternal use of tobacco, alcohol, coffee, and tea during pregnancy. Am J Epidemiol. 2004; 159, 862–871.Google Scholar
67. 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, 515–523.Google Scholar
68. Cao-Lei, L, Elgbeili, G, Massart, R, et al. Pregnant women’s cognitive appraisal from a natural disaster affects DNA methylation in their children 13 years later: Project Ice Storm. Transl Psychiatry. 2015; 5, e515.CrossRefGoogle ScholarPubMed
69. Hohwu, L, Li, J, Olsen, J, Sorensen, TI, Obel, C. Severe maternal stress exposure due to bereavement before, during and after pregnancy and risk of overweight and obesity in young adult men: a Danish National Cohort Study. PLoS ONE. 2014; 9, e97490.Google Scholar
70. Li, J, Olsen, J, Vestergaard, M, et al. Prenatal stress exposure related to maternal bereavement and risk of childhood overweight. PLoS ONE.. 2010; 5, e11896.Google Scholar
71. Martos-Moreno, GA, Chowen, JA, Argente, J. Metabolic signals in human puberty: effects of over and undernutrition. Mol Cell Endocrinol. 2010; 324, 70–81.Google Scholar
72. Della Torre, S, Benedusi, V, Fontana, R, Maggi, A. Energy metabolism and fertility: a balance preserved for female health. Nat Rev Endocrinol . 2014; 10, 13–23.CrossRefGoogle ScholarPubMed
73. Boyne, MS, Thame, M, Osmond, C, et al. Growth, body composition, and the onset of puberty: longitudinal observations in Afro-Caribbean children. J Clin Endocrinol Metab. 2010; 95, 3194–3200.Google Scholar
74. Davison, KK, Marshall, SJ, Birch, LL. Cross-sectional and longitudinal associations between TV viewing and girls’ body mass index, overweight status, and percentage of body fat. J Pediatr. 2006; 149, 32–37.Google Scholar
75. Davison, KK, Susman, EJ, Birch, LL. Percent body fat at age 5 predicts earlier pubertal development among girls at age 9. Pediatrics. 2003; 111, 815–821.Google Scholar
76. Farahmand, M, Ramezani Tehrani, F, Azizi, F. Whether age of menarche is influenced by body mass index and lipoproteins profile? A retrospective study. Iran J Reprod Med. 2012; 10, 337–342.Google Scholar
77. Kaplowitz, PB, Slora, EJ, Wasserman, RC, Pedlow, SE, Herman-Giddens, ME. Earlier onset of puberty in girls: relation to increased body mass index and race. Pediatrics. 2001; 108, 347–353.Google Scholar
78. Lee, JM, Appugliese, D, Kaciroti, N, et al. Weight status in young girls and the onset of puberty. Pediatrics. 2007; 119, e624–e630.Google Scholar
79. Zhai, L, Liu, J, Zhao, J, et al. Association of obesity with onset of puberty and sex hormones in Chinese girls: a 4-year longitudinal study. PLoS ONE. 2015; 10, e0134656.Google Scholar
80. Parent, A-S, Franssen, D, Fudvoye, J, Gérard, A, Bourguignon, J-P. Developmental variations in environmental influences including endocrine disruptors on pubertal timing and neuroendocrine control: revision of human observations and mechanistic insight from rodents. Front Neuroendocrinol. 2015; 38, 12–36.Google Scholar
81. Parent, A-S, Teilmann, G, Juul, A, et al. The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr Rev. 2003; 24, 668–693.CrossRefGoogle ScholarPubMed
82. De Bond, J-AP, Smith, JT. Kisspeptin and energy balance in reproduction. Reproduction. 2014; 147, R53–R63.CrossRefGoogle ScholarPubMed
83. Pérez-Pérez, A, Sánchez-Jiménez, F, Maymó, J, et al. Role of leptin in female reproduction. Clin Chem Lab Med. 2015; 53, 15–28.Google Scholar
84. de Ridder, CM, de Boer, RW, Seidell, JC, et al. Body fat distribution in pubertal girls quantified by magnetic resonance imaging. Int J Obes Relat Metab Disord. 1992; 16, 443–449.Google Scholar
85. King, S, Laplante, DP. Using natural disasters to study prenatal maternal stress in humans. In Perinatal Programming of Neurodevelopment (ed. Antonelli MC), 2015; pp. 285–313. Springer: New York.Google Scholar
86. Cao-Lei, L, Dancause, KN, Elgbeili, G, et al. DNA methylation mediates the impact of exposure to prenatal maternal stress on BMI and central adiposity in children at age 13(1/2) years: Project Ice Storm. Epigenetics. 2015; 10, 749–761.Google Scholar
87. Barrett, ES, Swan, SH. Stress and androgen activity during fetal development. Endocrinology. 2015; 156, 3435–3441.Google Scholar
88. Schopper, H, Klaus, T, Palme, R, Ruf, T, Huber, S. Sex-specific impact of prenatal stress on growth and reproductive parameters of guinea pigs. J Comp Physiol B. 2012; 182, 1117–1127.Google Scholar
89. Smith, JW, Waddell, BJ. Increased fetal glucocorticoid exposure delays puberty onset in postnatal life. Endocrinology. 2000; 141, 2422–2428.Google Scholar
90. Leonhardt, M, Lesage, J, Croix, D, et al. Effects of perinatal maternal food restriction on pituitary-gonadal axis and plasma leptin level in rat pup at birth and weaning and on timing of puberty. Biol Reprod. 2003; 68, 390–400.Google Scholar
91. O’Donnell, KJ, Bugge Jensen, A, Freeman, L, et al. Maternal prenatal anxiety and downregulation of placental 11β-HSD2. Psychoneuroendocrinology. 2012; 37, 818–826.Google Scholar
92. Hohwü, L, Li, J, Olsen, J, Sørensen, TIA, Obel, C. Severe maternal stress exposure due to bereavement before, during and after pregnancy and risk of overweight and obesity in young adult men: a Danish National Cohort Study. PLoS ONE. 2014; 9, e97490.Google Scholar
93. Zaidan, H, Leshem, M, Gaisler-Salomon, I. Prereproductive stress to female rats alters corticotropin releasing factor type 1 expression in ova and behavior and brain corticotropin releasing factor type 1 expression in offspring. Biol Psychiatry. 2013; 74, 680–687.Google Scholar
94. Rinaudo, P, Wang, E. Fetal programming and metabolic syndrome. Annu Rev Physiol. 2012; 74, 107–130.Google Scholar
95. Ramrakha, S, Caspi, A, Dickson, N, Moffitt, TE, Paul, C. Psychiatric disorders and risky sexual behaviour in young adulthood: cross sectional study in birth cohort. BMJ. 2000; 321, 263–266.CrossRefGoogle ScholarPubMed
96. Vicary, JR, Klingaman, LR, Harkness, WL. Risk factors associated with date rape and sexual assault of adolescent girls. J Adolesc, 1995; 18, 289–306.Google Scholar
97. Mendle, J, Ferrero, J. Detrimental psychological outcomes associated with pubertal timing in adolescent boys. Dev Rev. 2012; 32, 49–66.Google Scholar
98. Skoog, T, Bayram Özdemir, S. Explaining why early-maturing girls are more exposed to sexual harassment in early adolescence. J Early Adolesc. 2016; 36, 490–509.Google Scholar
99. Liestøl, K. Menarcheal age and spontaneous abortion: a causal connection? Am J Epidemiol. 1980; 111, 753–758.Google Scholar
100. Wyshak, G. Age at menarche and unsuccessful pregnancy outcome. Ann Hum Biol. 1983; 10, 69–73.Google Scholar