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Infection and pubertal timing: a systematic review

Published online by Cambridge University Press:  13 July 2016

J. A. McDonald ,
S. M. Eng ,
O. O. Dina ,
C. M. Schooling  and
M. B. Terry
J. A. McDonald*
Affiliation:
Mailman School of Public Health, Columbia University, New York, NY, USA
S. M. Eng
Affiliation:
Mailman School of Public Health, Columbia University, New York, NY, USA
O. O. Dina
Affiliation:
Mailman School of Public Health, Columbia University, New York, NY, USA
C. M. Schooling
Affiliation:
School of Public Health, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong SAR, People’s Republic of China China and School of Public Health, The City University of New York and Hunter College, New York, NY, USA
M. B. Terry
Affiliation:
Mailman School of Public Health, Columbia University, New York, NY, USA Herbert Irving Comprehensive Cancer Center, New York, NY, USA
*
*Address for correspondence: J. A. McDonald, Department of Epidemiology, Mailman School of Public Health, Columbia University, 722 West 168th St, New York, NY 10032, USA. (Email [email protected])
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Abstract

The decline in age of pubertal timing has serious public health implications ranging from psychosocial adjustment problems to a possible increase in reproductive cancers. One biologically plausible explanation for the decline is a decrease in exposures to infections. To systematically review studies that assess the role of infection in pubertal timing, Medline, Web of Science and EMBASE were systematically searched and retrieved studies were reviewed for eligibility. Eligible studies examined the association between infections, including microbial exposures, and physical pubertal characteristics (breast, genitalia and pubic hair development) or age at menarche. We excluded studies that were published in a language other than English, focused on precocious puberty, were case studies, and/or included youth with autoimmune diseases. We report on study design, population characteristics, measurement of infection and puberty and the main effects of infection on pubertal development. Based on our search terms we identified 1372 unique articles, of which only 15 human and five animal studies met our eligibility criteria. Not all studies examined all outcomes. Infection was associated with later breast development (4/4 human studies), with less consistent evidence for genitalia and pubic hair development. Seven studies assessed age at menarche with inconsistent findings (three supporting later, four no association). We conclude that a small but consistent literature supports that infection is associated with later breast development; the evidence for other pubertal events and age at menarche is less clear. Where fewer childhood infections coincide with the rise in incidence of hormone-related cancers.

Keywords

breast developmentinfectionmenarchepubertyreview
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 7 , Issue 6: Themed Issue: Developmental Origins of Adult Mental Health and Illness , December 2016 , pp. 636 - 651
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2016 

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References

1. Euling, SY, Herman-Giddens, ME, Lee, PA, et al. Examination of US puberty-timing data from 1940 to 1994 for secular trends: panel findings. Pediatrics. 2008; 121(Suppl. 3), S172–S191.CrossRefGoogle ScholarPubMed
2. Marshall, W, Tanner, J. Variations in pattern of pubertal changes in girls. Arch Dis Child. 1969; 235, 291–303.CrossRefGoogle Scholar
3. Kaplowitz, P. Pubertal development in girls: secular trends. Curr Opin Obstet Gynecol. 2006; 18, 487–491.CrossRefGoogle ScholarPubMed
4. Biro, FM, Greenspan, LC, Galvez, MP. Puberty in girls of the 21st century. J Pediatr Adolesc Gynecol. 2012; 25, 289–294.CrossRefGoogle Scholar
5. Herman-Giddens, ME. Recent data on pubertal milestones in United States children: the secular trend toward earlier development. Int J Androl. 2006; 29, 241–246, discussion 286–290.CrossRefGoogle ScholarPubMed
6. Tinggaard, J, Mieritz, MG, Sorensen, K, et al. The physiology and timing of male puberty. Curr Opin Endocrinol Diabetes Obes. 2012; 19, 197–203.CrossRefGoogle ScholarPubMed
7. Ellis, BJ. Timing of pubertal maturation in girls: an integrated life history approach. Psychol Bull. 2004; 130, 920–958.CrossRefGoogle ScholarPubMed
8. Golub, MS, Collman, GW, Foster, PM, et al. Public health implications of altered puberty timing. Pediatr. 2008; 121(Suppl. 3), S218–S230.Google ScholarPubMed
9. Walvoord, EC. The timing of puberty: is it changing? Does it matter? J Adolesc Health. 2010; 47, 433–439.CrossRefGoogle ScholarPubMed
10. Charalampopoulos, D, McLoughlin, A, Elks, CE, Ong, KK. Age at menarche and risks of all-cause and cardiovascular death: a systematic review and meta-analysis. Am J Epidemiol. 2014; 180, 29–40.CrossRefGoogle Scholar
11. Prentice, P, Viner, RM. Pubertal timing and adult obesity and cardiometabolic risk in women and men: a systematic review and meta-analysis. Int J Obes (Lond). 2013; 37, 1036–1043.CrossRefGoogle Scholar
12. Sorensen, K, Mouritsen, A, Aksglaede, L, et al. Recent secular trends in pubertal timing: implications for evaluation and diagnosis of precocious puberty. Horm Res Paediatr. 2012; 77, 137–145.CrossRefGoogle ScholarPubMed
13. 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
14. Sun, SS, Schubert, CM, Chumlea, WC, et al. National estimates of the timing of sexual maturation and racial differences among US children. Pediatrics. 2002; 110, 911–919.CrossRefGoogle ScholarPubMed
15. Herman-Giddens, ME, Slora, EJ, Wasserman, RC, et al. Secondary sexual characteristics and menses in young girls seen in office practice: a study from the Pediatric Research in Office Settings network. Pediatrics. 1997; 99, 505–512.CrossRefGoogle Scholar
16. Lee, PA. Normal ages of pubertal events among American males and females. J Adolesc Health Care. 1980; 1, 26–29.CrossRefGoogle ScholarPubMed
17. Wu, T, Mendola, P, Buck, GM. Ethnic differences in the presence of secondary sex characteristics and menarche among US girls: the third National Health and Nutrition Examination Survey, 1988–1994. Pediatrics. 2002; 110, 752–757.CrossRefGoogle ScholarPubMed
18. Freedman, DS, Khan, LK, Serdula, MK, et al. Relation of age at menarche to race, time period, and anthropometric dimensions: the bogalusa heart study. Pediatrics. 2002; 110, e43.CrossRefGoogle ScholarPubMed
19. Biro, FM, Galvez, MP, Greenspan, LC, et al. Pubertal assessment method and baseline characteristics in a mixed longitudinal study of girls. Pediatrics. 2010; 126, e583–e590.CrossRefGoogle Scholar
20. Biro, FM, Greenspan, LC, Galvez, MP, et al. Onset of breast development in a longitudinal cohort. Pediatrics. 2013; 132, 1019–1027.CrossRefGoogle ScholarPubMed
21. Aksglaede, L, Sorensen, K, Petersen, JH, Skakkebaek, NE, Juul, A. Recent decline in age at breast development: the copenhagen puberty study. Pediatrics. 2009; 123, e932–e939.CrossRefGoogle ScholarPubMed
22. Papadimitriou, A, Pantsiotou, S, Douros, K, et al. Timing of pubertal onset in girls: evidence for non-gaussian distribution. J Clin Endocr Metab. 2008; 93, 4422–4425.CrossRefGoogle ScholarPubMed
23. Semiz, S, Kurt, F, Kurt, DT, Zencir, M, Sevinc, O. Pubertal development of turkish children. J Pediatr Endocr Met. 2008; 21, 951–961.Google ScholarPubMed
24. Ahmed, ML, Ong, KK, Dunger, DB. Childhood obesity and the timing of puberty. Trends Endocrin Metab. 2009; 20, 237–242.CrossRefGoogle ScholarPubMed
25. Marshall, WA, Tanner, JM. Variations in the pattern of pubertal changes in boys. Arch Dis Child. 1970; 45, 13–23.CrossRefGoogle ScholarPubMed
26. Herman-Giddens, ME, Steffes, J, Harris, D, et al. Secondary sexual characteristics in boys: data from the Pediatric Research in Office Settings network. Pediatrics. 2012; 130, e1058–e1068.CrossRefGoogle ScholarPubMed
27. Juul, A, Teilmann, G, Scheike, T, et al. Pubertal development in Danish children: comparison of recent European and US data. Int J Androl. 2006; 29, 247–255, discussion 286–290.CrossRefGoogle ScholarPubMed
28. Mul, D, Fredriks, AM, van Buuren, S, et al. Pubertal development in the Netherlands 1965–1997. Pediatr Res. 2001; 50, 479–486.CrossRefGoogle ScholarPubMed
29. Sorensen, K, Aksglaede, L, Petersen, JH, Juul, A. Recent changes in pubertal timing in healthy Danish boys: associations with body mass index. J Clin Endocrinol Metab. 2010; 95, 263–270.CrossRefGoogle ScholarPubMed
30. Goldstein, JR. A secular trend toward earlier male sexual maturity: evidence from shifting ages of male young adult mortality. PLoS One. 2011; 6, e14826.CrossRefGoogle ScholarPubMed
31. Kryst, L, Kowal, M, Woronkowicz, A, Sobiecki, J, Cichocka, BA. Secular changes in height, body weight, body mass index and pubertal development in male children and adolescents in Krakow, Poland. J Biosoc Sci. 2012; 44, 495–507.CrossRefGoogle ScholarPubMed
32. Monteilh, C, Kieszak, S, Flanders, WD, et al. Timing of maturation and predictors of Tanner stage transitions in boys enrolled in a contemporary British cohort. Paediatr Perinat Epidemiol. 2011; 25, 75–87.CrossRefGoogle Scholar
33. Herman-Giddens, ME, Kaplowitz, PB, Wasserman, R. Navigating the recent articles on girls’ puberty in pediatrics: what do we know and where do we go from here? Pediatrics. 2004; 113, 911–917.CrossRefGoogle Scholar
34. Beunen, GP, Rogol, AD, Malina, RM. Indicators of biological maturation and secular changes in biological maturation. Food and Nutr Bull. 2006; 27(Suppl. 4 Growth Standard), S244–S256.CrossRefGoogle ScholarPubMed
35. Krieger, N, Kiang, MV, Kosheleva, A, et al. Age at menarche: 50-year socioeconomic trends among US-born black and white women. Am J Public Health. 2015; 105, 388–397.CrossRefGoogle ScholarPubMed
36. Tanner, JM, Eveleth, PB. Puberty, Biologic and Psychosocial Components. 1975. Stenfert Kroese: Leiden, the Netherlands.Google Scholar
37. Gould HN, Gould MR. Age of first menstruation in mothers and daughters. J Am Med Assoc. 1932; 98, 1349–1352.Google Scholar
38. Damon A, Damon ST, Reed RB, Valadian I. Age at menarche of mothers and daughters, with a note on accuracy of recall. Hum Biol. 1969; 41, 161–175.Google Scholar
39. Anderson, SE, Dallal, GE, Must, A. Relative weight and race influence average age at menarche: results from two nationally representative surveys of US girls studied 25 years apart. Pediatrics. 2003; 111(Pt 1), 844–850.CrossRefGoogle ScholarPubMed
40. Anderson SE, Must A. Interpreting the Continued Decline in the average age at menarche: results from two nationally representative surveys of U.S. girls studied 10 years apart. J Pediatr. 2005; 147, 753–760.Google Scholar
41. Fryar CD, Carroll MD, Ogden CL. Prevalence of overweight and obesity among children and adolescents: United States, 1963–1965 through 2011–2012. National Center for Health Statistics. 19 September 2014. Available from http://www.cdc.gov/nchs/data/hestat/obesity_child_11_12/obesity_child_11_12.htm.Google Scholar
42. Lakshman, R, Elks, CE, Ong, KK. Childhood Obesity. Circulation. 2012; 126, 1770–1779.CrossRefGoogle ScholarPubMed
43. Kaplowitz, PB. Link between body fat and the timing of puberty. Pediatrics. 2008; 121(Suppl. 3), S208–S217.CrossRefGoogle ScholarPubMed
44. Biro, FM, McMahon, RP, Striegel-Moore, R, et al. Impact of timing of pubertal maturation on growth in black and white female adolescents: the national heart, lung, and blood institute growth and health study. J Pediatr. 2001; 138, 636–643.CrossRefGoogle ScholarPubMed
45. Himes, JH, Obarzanek, E, Baranowski, T, et al. Early sexual maturation, body composition, and obesity in African-American girls. Obes Res. 2004; 12(Suppl), 64S–72S.CrossRefGoogle ScholarPubMed
46. Wang, Y. Is obesity associated with early sexual maturation? A comparison of the association in American boys versus girls. Pediatrics. 2002; 110, 903–910.CrossRefGoogle ScholarPubMed
47. Frisch, RE, Revelle, R. Height and weight at menarche and a hypothesis of critical body weights and adolescent events. Science. 1970; 169, 397–399.CrossRefGoogle Scholar
48. Hwang, JY, Shin, C, Frongillo, EA, Shin, KR, Jo, I. Secular trend in age at menarche for South Korean women born between 1920 and 1986: the Ansan Study. Ann Hum Biol. 2003; 30, 434–442.CrossRefGoogle ScholarPubMed
49. Ma, HM, Du, ML, Luo, XP, et al. Onset of breast and pubic hair development and menses in urban chinese girls. Pediatrics. 2009; 124, e269–e277.CrossRefGoogle ScholarPubMed
50. Huen, KF, Leung, SS, Lau, JT, et al. Secular trend in the sexual maturation of southern Chinese girls. Acta Paediatr. 1997; 86, 1121–1124.CrossRefGoogle ScholarPubMed
51. Nunez-de la Mora, A, Chatterton, RT, Choudhury, OA, Napolitano, DA, Bentley, GR. Childhood conditions influence adult progesterone levels. PLoS Med. 2007; 4, e167.CrossRefGoogle ScholarPubMed
52. Cho, GJ, Park, HT, Shin, JH, et al. Age at menarche in a Korean population: secular trends and influencing factors. Eur J Pediatr. 2010; 169, 89–94.CrossRefGoogle Scholar
53. Woolf, SH, Aron, L. ed. U.S. Health in International Perspective: Shorter Lives, Poorer Health, 2013. The National Academies Press: Washington, DC.Google Scholar
54. Rohan, TE, Jain, MG, Howe, GR, Miller, AB. Dietary folate consumption and breast cancer risk. J Natl Cancer Inst. 2000; 92, 266–269.CrossRefGoogle ScholarPubMed
55. Towne, B, Czerwinski, SA, Demerath, EW, et al. Heritability of age at menarche in girls from the Fels Longitudinal Study. Am J Phys Anthropol. 2005; 128, 210–219.CrossRefGoogle ScholarPubMed
56. Cousminer, DL, Berry, DJ, Timpson, NJ, et al. Genome-wide association and longitudinal analyses reveal genetic loci linking pubertal height growth, pubertal timing and childhood adiposity. Hum Mol Genet. 2013; 22, 2735–2747.CrossRefGoogle ScholarPubMed
57. He, C, Kraft, P, Chen, C, et al. Genome-wide association studies identify novel loci associated with age at menarche and age at natural menopause. Nat Genet. 2009; 41, 724–728.CrossRefGoogle Scholar
58. Perry, JRB, Stolk, L, Franceschini, N, et al. Meta-analysis of genome-wide association data identifies two loci influencing age at menarche. Nat Genet. 2009; 41, 648–650.CrossRefGoogle ScholarPubMed
59. Elks, CE, Perry, JRB, Sulem, P, et al. Thirty new loci for age at menarche identified by a meta-analysis of genome-wide association studies. Nat Genet. 2010; 42, 1077–1085.CrossRefGoogle ScholarPubMed
60. Dvornyk, V, Waqar-ul-Haq, . Genetics of age at menarche: a systematic review. Hum Reprod Update. 2012; 18, 198–210.CrossRefGoogle ScholarPubMed
61. Spencer, KL, Malinowski, J, Carty, CL, et al. Genetic variation and reproductive timing: African American women from the population architecture using genomics and epidemiology (page) study. PLoS One. 2013; 8, e55258.CrossRefGoogle ScholarPubMed
62. Diamanti-Kandarakis, E, Gore, AC. Endocrine Disruptors and Puberty. 2012. Humana Press: New York, NY.CrossRefGoogle Scholar
63. Roy, JR, Chakraborty, S, Chakraborty, TR. Estrogen-like endocrine disrupting chemicals affecting puberty in humans – a review. Med Sci Monit. 2009; 15, RA137–RA145.Google ScholarPubMed
64. Özen, S, Darcan, Ş. Effects of environmental endocrine disruptors on pubertal development. J Clin Res Pediatr Endocrinol. 2011; 3, 1–6.CrossRefGoogle ScholarPubMed
65. Yermachenko, A, Dvornyk, V. Nongenetic determinants of age at menarche: a systematic review. BioMed Res Int. 2014; 2014, 371583.CrossRefGoogle ScholarPubMed
66. Ulijaszek, SJ. The international growth standard for children and adolescents project: environmental influences on preadolescent and adolescent growth in weight and height. Food Nutr Bull. 2006; 27(Suppl. 4 Growth Standard), S279–S294.CrossRefGoogle ScholarPubMed
67. Ibanez, L, Ferrer, A, Marcos, MV, Hierro, FR, de Zegher, F. Early puberty: rapid progression and reduced final height in girls with low birth weight. Pediatrics. 2000; 106, E72.CrossRefGoogle ScholarPubMed
68. Voordouw, JJ, van Weissenbruch, MM, Delemarre-van de Waal, HA. Intrauterine growth retardation and puberty in girls. Twin Res. 2001; 4, 299–306.CrossRefGoogle ScholarPubMed
69. Adair, LS. Size at birth predicts age at menarche. Pediatrics. 2001; 107, E59.CrossRefGoogle ScholarPubMed
70. Ong, KK, Potau, N, Petry, CJ, et al. Opposing influences of prenatal and postnatal weight gain on adrenarche in normal boys and girls. J Clin Endocrinol Metab. 2004; 89, 2647–2651.CrossRefGoogle ScholarPubMed
71. Hochberg, Ze, Belsky, J. Evo-devo of human adolescence: beyond disease models of early puberty. BMC Med. 2013; 11, 113.CrossRefGoogle ScholarPubMed
72. Crimmins, EM, Finch, CE. Infection, inflammation, height, and longevity. Proc Nat Acad Sci USA. 2006; 103, 498–503.CrossRefGoogle ScholarPubMed
73. Melosi, MV. The Sanitary City: Urban Infrastructure in America from Colonial Times to the Present. 2000. Johns Hopkins University Press: Baltimore.Google Scholar
74. Rolff, J. Bateman’s principle and immunity. Proc Biol Sci . 2002; 269, 867–872.CrossRefGoogle ScholarPubMed
75. Jasienska, G. Reproduction and lifespan: trade-offs, overall energy budgets, intergenerational costs, and costs neglected by research. Am J Hum Biol. 2009; 21, 524–532.CrossRefGoogle ScholarPubMed
76. Bilbo, SD, Klein, SL. Special issue: the neuroendocrine-immune axis in health and disease. Horm Behav. 2012; 62, 187–190.CrossRefGoogle ScholarPubMed
77. Klein, SL. Immune cells have sex and so should journal articles. Endocrinology. 2012; 153, 2544–2550.CrossRefGoogle ScholarPubMed
78. Klein, SL. The effects of hormones on sex differences in infection: from genes to behavior. Neurosci Biobehav Rev. 2000; 24, 627–638.CrossRefGoogle Scholar
79. Need, EF, Atashgaran, V, Ingman, WV, Dasari, P. Hormonal regulation of the immune microenvironment in the mammary gland. Jf Mammary Gland Biol Neoplasia. 2014; 19, 229–239.CrossRefGoogle ScholarPubMed
80. Kwok, MK, Leung, GM, Lam, TH, Schooling, CM. Early life infections and onset of puberty: evidence from Hong Kong’s children of 1997 birth cohort. Am J Epidemiol. 15 2011; 173, 1440–1452.CrossRefGoogle ScholarPubMed
81. Grumbach, MM. The neuroendocrinology of human puberty revisited. Horm Res. 2002; 57, 2–14.Google ScholarPubMed
82. Waldhauser, F, Weissenbacher, G, Frisch, H, Pollak, A. Pulsatile secretion of gonadotropins in early infancy. Eur J Pediatr. 1981; 137, 71–74.CrossRefGoogle ScholarPubMed
83. Winter, JS, Hughes, IA, Reyes, FI, Faiman, C. Pituitary-gonadal relations in infancy: 2. Patterns of serum gonadal steroid concentrations in man from birth to two years of age. J Clin Endocrinol Metab. 1976; 42, 679–686.CrossRefGoogle Scholar
84. Chellakooty, M, Schmidt, IM, Haavisto, AM, et al. Inhibin A, inhibin B, follicle-stimulating hormone, luteinizing hormone, estradiol, and sex hormone-binding globulin levels in 473 healthy infant girls. J Clin Endocrinol Metab. 2003; 88, 3515–3520.CrossRefGoogle ScholarPubMed
85. Melmed, S, Polonsky, KS, Larsen, RP, Kronenberg, HM. Williams Textbook of Endocrinology, 12th edn, 2011. Saunders/Elsevier: Philadelphia, PA.Google Scholar
86. Kaplowitz, P. Update on precocious puberty: girls are showing signs of puberty earlier, but most do not require treatment. Adv Pediatr. 2011; 58, 243–258.CrossRefGoogle Scholar
87. Gluckman, PD, Hanson, MA. Changing times: the evolution of puberty. Mol Cell Endocrinol. 2006; 254–255, 26–31.CrossRefGoogle ScholarPubMed
88. de Martino, M, Tovo, P-A, Galli, L, et al. Puberty in perinatal HIV-1 infection: a multicentre longitudinal study of 212 children. AIDS. 2001; 15, 1527–1534.CrossRefGoogle ScholarPubMed
89. Buchacz, K, Rogol, AD, Lindsey, JC, et al. Delayed onset of pubertal development in children and adolescents with perinatally acquired HIV infection. J Acquir Immune Defic Syndr. 2003; 33, 56–65.CrossRefGoogle ScholarPubMed
90. Ferrand, RA, Bandason, T, Musvaire, P, et al. Causes of acute hospitalization in adolescence: burden and spectrum of HIV-related morbidity in a country with an early-onset and severe HIV epidemic: a prospective survey. PLoS Med. 2010; 7, e1000178.CrossRefGoogle Scholar
91. Williams, PL, Abzug, MJ, Jacobson, DL, et al. Pubertal onset in children with perinatal HIV infection in the era of combination antiretroviral treatment. AIDS. 2013; 27, 1959–1970.CrossRefGoogle ScholarPubMed
92. Wu, JF, Tsai, WY, Tung, YC, et al. Effect of menarche onset on the clinical course in females with chronic hepatitis B virus infection. J Pediatr. 2014; 165, 534–538.CrossRefGoogle ScholarPubMed
93. Cole, TJ, Salem, SI, Hafez, AS, Galal, OM, Massoud, A. Plasma albumin, parasitic infection and pubertal development in Egyptian boys. Trans R Soc Trop Med Hyg. 1982; 76, 17–20.CrossRefGoogle ScholarPubMed
94. Ibrahim, II, Barakat, RM, Bassiouny, HK, et al. Effect of urinary bilharzial infection on male pubertal development and endocrine functions. Arch Androl. 1983; 11, 59–64.CrossRefGoogle ScholarPubMed
95. Aroke, AH, Asonganyi, T, Mbonda, E. Influence of a past history of Gambian sleeping sickness on physical growth, sexual maturity and academic performance of children in Fontem, Cameroon. Ann Trop Med Parasitol. 1998; 92, 829–835.CrossRefGoogle ScholarPubMed
96. Bernhard, P, Makunde, RW, Magnussen, P, Lemnge, MM. Genital manifestations and reproductive health in female residents of a Wuchereria bancrofti – endemic area in Tanzania. Trans R Soc Trop Med Hyg. 2000; 94, 409–412.CrossRefGoogle ScholarPubMed
97. Braga, C, Dourado, I, Ximenes, R, Miranda, J, Alexander, N. Bancroftian filariasis in an endemic area of Brazil: differences between genders during puberty. Rev Soc Bras Med Trop. 2005; 38, 224–228.CrossRefGoogle Scholar
98. Fox, LM, Wilson, SF, Addiss, DG, et al. Clinical correlates of filarial infection in Haitian children: an association with interdigital lesions. Am J Trop Med Hyg. 2005; 73, 759–765.CrossRefGoogle ScholarPubMed
99. Rosenstock, SJ, Jorgensen, T, Andersen, LP, Bonnevie, O. Association of Helicobacter pylori infection with lifestyle, chronic disease, body-indices, and age at menarche in Danish adults. Scand J Public Health. 2000; 28, 32–40.Google ScholarPubMed
100. Khan, AD, Schroeder, DG, Martorell, R, Haas, JD, Rivera, J. Early childhood determinants of age at menarche in rural guatemala. Am J Hum Biol. 1996; 8, 717–723.3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
101. Blell, M, Pollard, TM, Pearce, MS. Predictors of age at menarche in the newcastle thousand families study. J Biosoc Sci. 2008; 40, 563–575.CrossRefGoogle ScholarPubMed
102. Marshall, W, Tanner, J. Growth and physiological development during adolescence. Annu Rev Med. 1968; 19, 283–300.CrossRefGoogle ScholarPubMed
103. Marshall, WA, Tanner, JM. Variations in pattern of pubertal changes in girls. Arch Dis Child. 1969; 44, 291–303.CrossRefGoogle ScholarPubMed
104. Lacau-Mengido, IM, Mejia, ME, Diaz-Torga, GS, et al. Endocrine studies in ivermectin-treated heifers from birth to puberty. J Anim Sci. 2000; 78, 817–824.CrossRefGoogle ScholarPubMed
105. Ramaley, JA, Phares, CK. Delay of puberty onset in males due to suppression of growth hormone. Neuroendocrinology. 1983; 36, 321–329.CrossRefGoogle ScholarPubMed
106. Ramaley, JA, Phares, CK. Delay of puberty onset in females due to suppression of growth hormone. Endocrinol. 1980; 106, 1989–1993.CrossRefGoogle ScholarPubMed
107. Osaer, S, Goossens, B, Jeffcoate, I, Holmes, P. Effects of Trypanosoma congolense and nutritional supplements in Djallonke ewes on live weight during pregnancy, post partum weight, haematology parameters and lamb performance. Res Vet Sci. 1998; 65, 65–69.CrossRefGoogle ScholarPubMed
108. Mukasa-Mugerwa, E, Kasali, OB, Said, AN. Effect of nutrition and endoparasitic treatment on growth, onset of puberty and reproductive activity in Menz ewe lambs. Theriogenology. 1991; 36, 319–328.CrossRefGoogle ScholarPubMed
109. Fabre-Nys, C, Gelez, H. Sexual behavior in ewes and other domestic ruminants. Horm Behav. 2007; 52, 18–25.CrossRefGoogle ScholarPubMed
110. Chumlea, WC, Schubert, CM, Roche, AF, et al. Age at menarche and racial comparisons in US girls. Pediatrics. 2003; 111, 110–113.CrossRefGoogle ScholarPubMed
111. Reynolds, EL, Wines, JV. Individual differences in physical changes associated with adolescence in girls. Am J Dis Child. 1948; 75, 329–350.Google ScholarPubMed
112. Nicolson, AB, Hanley, C. Indices of physiological maturity: derivation and interrelationships. Child Dev. 1953; 24, 3–38.Google ScholarPubMed
113. Kovats, S, Carreras, E, Agrawal, H. Sex steroid receptors in immune cells. In Sex Hormones and Immunity to Infection (eds. Klein LS, Roberts C), 2010; pp. 53–91. Springer: Berlin Heidelberg.CrossRefGoogle Scholar
114. Klein, SL, Nelson, RJ. Influence of social factors on immune function and reproduction. Rev Reprod. 1999; 4, 168–178.CrossRefGoogle ScholarPubMed
115. Verthelyi, D. Sex hormones as immunomodulators in health and disease. Int Immunopharmacol. 2001; 1, 983–993.CrossRefGoogle ScholarPubMed
116. Tanriverdi, F, Silveira, LF, MacColl, GS, Bouloux, PM. The hypothalamic–pituitary–gonadal axis: immune function and autoimmunity. J Endocrinol. 2003; 176, 293–304.CrossRefGoogle ScholarPubMed
117. Mavoungou, D, Lansoud-Soukate, J, Dupont, A. Steroid and gonadotropin hormone levels in young African women with filarial infection. J Steroid Biochem. 1989; 34, 577–580.CrossRefGoogle ScholarPubMed
118. Muehlenbein, MP, Alger, J, Cogswell, F, James, M, Krogstad, D. The reproductive endocrine response to Plasmodium vivax infection in Hondurans. Am J Trop Med Hyg. 2005; 73, 178–187.CrossRefGoogle ScholarPubMed
119. Larralde, C, Morales, J, Terrazas, I, Govezensky, T, Romano, MC. Sex hormone changes induced by the parasite lead to feminization of the male host in murine Taenia crassiceps cysticercosis. J Steroid Biochem Mol Biol. 1995; 52, 575–580.CrossRefGoogle ScholarPubMed
120. Boonekamp, JJ, Ros, AH, Verhulst, S. Immune activation suppresses plasma testosterone level: a meta-analysis. Biol Lett. 2008; 4, 741–744.CrossRefGoogle ScholarPubMed
121. Nilsson, C, Jennische, E, Ho, HP, et al. Postnatal endotoxin exposure results in increased insulin sensitivity and altered activity of neuroendocrine axes in adult female rats. Eur J Endocrinol. 2002; 146, 251–260.CrossRefGoogle ScholarPubMed
122. Schooling, CM, Dowd, JB, Jones, HE. Helicobacter pylori is associated with lower androgen activity among men in NHANES III. Gut. 2013; 62, 1384–1385.CrossRefGoogle ScholarPubMed
123. Reincke, M, Arlt, W, Heppner, C, et al. Neuroendocrine dysfunction in African trypanosomiasis. The role of cytokines. Ann NY Acad Sci. 1998; 840, 809–821.CrossRefGoogle ScholarPubMed
124. Biro, FM, Pinney, SM, Huang, B, et al. Hormone changes in peripubertal girls. J Clin Endocrinol Metab. 2014; 99, 3829–3835.CrossRefGoogle ScholarPubMed
125. Biro, FM, Huang, B, Daniels, SR, Lucky, AW. Pubarche as well as thelarche may be a marker for the onset of puberty. J Pediatr Adolesc Gynecol. 2008; 21, 323–328.CrossRefGoogle ScholarPubMed
126. Rothman, KJ. Epidemiology: An Introduction. 2002. Oxford University Press: New York, NY.Google Scholar
127. Hjalgrim, H, Smedby, KE, Rostgaard, K, et al. Infectious mononucleosis, childhood social environment, and risk of Hodgkin lymphoma. Cancer Res. 2007; 67, 2382–2388.CrossRefGoogle ScholarPubMed
128. Chang, ET, Zheng, T, Weir, EG, et al. Childhood social environment and Hodgkin’s lymphoma: new findings from a population-based case-control study. Cancer Epidemiol Biomarkers Prev. 2004; 13, 1361–1370.CrossRefGoogle ScholarPubMed
129. Casadevall, A, Pirofski, LA. Host-pathogen interactions: basic concepts of microbial commensalism, colonization, infection, and disease. Infect Immun. 2000; 68, 6511–6518.CrossRefGoogle ScholarPubMed
130. Harn, DA, McDonald, J, Atochina, O, Da’dara, AA. Modulation of host immune responses by helminth glycans. Immunol Rev. 2009; 230, 247–257.CrossRefGoogle ScholarPubMed
131. McDonald, JA. Elucidating the activation properties of the Th2 PAMP, lacto-N-fucopentaose III (Order No. 3365351). Available from ProQuest Dissertations & Theses Global. (304889882). Retrieved 6 May 2016 from http://ezproxy.cul.columbia.edu/login?url=http://search.proquest.com/docview/304889882?accountid=10226.Google Scholar
132. Bhakhri, B, Prasad, M, Choudhary, I, Biswas, K. Delayed puberty: experience of a tertiary care centre in India. Ann Trop Paediatr. 2010; 30, 205–212.CrossRefGoogle ScholarPubMed
133. Büyükgebiz, A, Dündar, B, Böber, E, Büyükgebiz, B. Helicobacter pylori infection in children with constitutional delay of growth and puberty. J Pediatr Endocrinol Metab. 2001; 14, 549–551.CrossRefGoogle ScholarPubMed
134. Mills, J, Stolley, P, Davies, J, Moshang, TJ. Premature thelarche. Natural history and etiologic investigation. Am J Dis Child. 1981; 138, 743–745.CrossRefGoogle Scholar
135. Ahmed, M, Ong, K, Dunger, D. Childhood obesity and the timing of puberty. Trends Endocrinol Metab. 2009; 20, 237–242.CrossRefGoogle ScholarPubMed
136. McAllister, EJ, Dhurandhar, NV, Keith, SW, et al. Ten putative contributors to the obesity epidemic. Crit Rev Food Sci Nutr. 2009; 49, 868–913.CrossRefGoogle Scholar
137. Gabbert, C, Donohue, M, Arnold, J, Schwimmer, JB. Adenovirus 36 and obesity in children and adolescents. Pediatrics. 2010; 126, 721–726.CrossRefGoogle ScholarPubMed
138. Schooling, CM, Jones, HE, Leung, GM. Lifecourse infectious origins of sexual inequalities in central adiposity. Int J Epidemiol. 2011; 40, 1556–1564.CrossRefGoogle ScholarPubMed
139. Ellis, BJ, Shirtcliff, EA, Boyce, WT, Deardorff, J, Essex, MJ. Quality of early family relationships and the timing and tempo of puberty: effects depend on biological sensitivity to context. Dev Psychopathol. 2011; 23, 85–99.CrossRefGoogle ScholarPubMed
140. Schooling, CM, Jiang, CQ, Lam, TH, et al. Leg length and age of puberty among men and women from a developing population: the Guangzhou Biobank cohort study. Am J Hum Biol. 2010; 22, 683–687.CrossRefGoogle ScholarPubMed
141. Hwang, AE, Mack, TM, Hamilton, AS, et al. Childhood infections and adult height in monozygotic twin pairs. Am J Epidemiol. 2013; 178, 551–558.CrossRefGoogle ScholarPubMed
142. Stagi, S, Galli, L, Cecchi, C, et al. Final height in patients perinatally infected with the human immunodeficiency virus. Horm Res Paediatr. 2010; 74, 165–171.CrossRefGoogle ScholarPubMed
143. Kessler, M, Kaul, A, Santos-Malave, C, et al. Growth patterns in pubertal HIV-infected adolescents and their correlation with cytokines, IGF-1, IGFBP-1, and IGFBP-3. J Pediatr Endocrinol Metab. 2013; 26, 639–644.CrossRefGoogle ScholarPubMed
144. Patel, P, Mendall, MA, Khulusi, S, Northfield, TC, Strachan, DP. Helicobacter pylori infection in childhood: risk factors and effect on growth. BMJ. 1994; 309, 1119–1123.CrossRefGoogle ScholarPubMed
145. Karlberg, J. A biologically-oriented mathematical model (ICP) for human growth. Acta Paediatr Scand Suppl. 1989; 350, 70–94.CrossRefGoogle ScholarPubMed
146. Houghton, LC, Cooper, GD, Bentley, GR, et al. A migrant study of pubertal timing and tempo in British-Bangladeshi girls at varying risk for breast cancer. Breast Cancer Res. 2014; 16, 469.CrossRefGoogle ScholarPubMed
147. Evans, T, Sany, O, Pearmain, P, et al. Differential trends in the rising incidence of endometrial cancer by type: data from a UK population-based registry from 1994 to 2006. Br J Cancer. 2011; 104, 1505–1510.CrossRefGoogle ScholarPubMed
148. Johnson, RH, Chien, FL, Bleyer, A. Incidence of breast cancer with distant involvement among women in the United States, 1976 to 2009. JAMA. 2013; 309, 800–805.CrossRefGoogle ScholarPubMed
149. Huyghe, E, Matsuda, T, Thonneau, P. Increasing incidence of testicular cancer worldwide: a review. J Urol. 2003; 170, 5–11.CrossRefGoogle ScholarPubMed
150. Bodicoat, DH, Schoemaker, MJ, Jones, ME, et al. Timing of pubertal stages and breast cancer risk: the Breakthrough Generations Study. Breast Cancer Res. 2014; 16, R18.CrossRefGoogle ScholarPubMed
151. Centers for Disease Control and Prevention (CDC). National Center for Health Statistics (NCHS). National Health and Nutrition Examination Survey Data. Hyattsville, MD: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, 1976–1980. http://www.cdc.gov/nchs/nhanes/nhanesii.htm.Google Scholar