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Age at Menarche and Gallstone Disease in Middle-Aged Women

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Abstract

The goal of this study was to explore the association between age at menarche and gallstone disease (GSD) in Korean women and to determine whether any of the observed associations were mediated by adult adiposity. A cross-sectional study was performed on 83 275 Korean women, aged 30 years or older, who underwent a health checkup examination between March 2011 and April 2013. Information regarding age at menarche was collected using standardized, self-administered questionnaires. Gallstone disease was defined as either having gallstones or having had a cholecystectomy based on ultrasound. Logistic regression models were used to evaluate the association between age at menarche and GSD. Of the 83 275 women evaluated in this study, 3341 had GSD. Age at menarche was negatively associated with the prevalence of GSD. In a multivariable-adjusted model adjusting for potential confounders including reproductive factors and body weight at age 20, the odds ratios (95% confidence intervals) for GSD comparing menarche at <12, 12, 14, 15, and 16 to 18 years to menarche at 13 years were 1.46 (1.23-1.75), 1.19 (1.04-1.35), 0.97 (0.87-1.09), 0.92 (0.82-1.03), and 0.89 (0.78-1.02), respectively (P for trend <.001). Adjusting for adult body mass index or percentage fat mass (%) partially reduced these associations; however, they remained statistically significant. Early menarche was associated with increasing prevalence of GSD in a large sample of middle-aged women. The findings of this study extend the range of adverse health outcomes associated with early menarche and suggest that obesity prevention strategies could be useful for reducing the risk of GSD in women who experience early menarche.

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References

  1. Elks, CE, Ong, KK Whole genome associated studies for age at menarche. Brief Funct Genomics. 2011;10(2):91–97.

    CAS  PubMed  Google Scholar 

  2. Must, A, Phillips, SM, Naumova, EN, et al. Recall of early menstrual history and menarcheal body size: after 30 years, how well do women remember? Am J Epidemiol. 2002;155(7): 672–679.

    CAS  PubMed  Google Scholar 

  3. Charalampopoulos, D, McLoughlin, A, Elks, CE, Ong, KK Age at menarche and risks of all-cause and cardiovascular death: a sys-tematic review and meta-analysis. Am J Epidemiol. 2014;180(1): 29–40.

    PubMed  PubMed Central  Google Scholar 

  4. Walvoord, EC The timing of puberty: is it changing? Does it matter? J Adolesc Health. 2010;47(5):433–439.

    PubMed  Google Scholar 

  5. Kivimaki, M, Lawlor, DA, Smith, GD, et al. Association of age at menarche with cardiovascular risk factors, vascular structure, and function in adulthood: the Cardiovascular Risk in Young Finns study. Am J Clin Nutr. 2008;87(6):1876–1882.

    CAS  PubMed  Google Scholar 

  6. Remsberg, KE, Demerath, EW, Schubert, CM, Chumlea, WC, Sun, SS, Siervogel, RM Early menarche and the development of cardiovascular disease risk factors in adolescent girls: the Fels Longitudinal Study. J Clin Endocrinol Metab. 2005;90(5): 2718–2724.

    CAS  PubMed  Google Scholar 

  7. Elks, CE, Ong, KK, Scott, RA, et al; InterAct Consortium. Age at menarche and type 2 diabetes risk: the EPIC-InterAct study. Dia-betes Care. 2013;36(11):3526–3534.

    Google Scholar 

  8. Heys, M, Schooling, CM, Jiang, C, et al. Age of menarche and the metabolic syndrome in China. Epidemiology. 2007;18(6): 740–746.

    PubMed  Google Scholar 

  9. Pierce, MB, Leon, DA Age at menarche and adult BMI in the Aberdeen children of the 1950s cohort study. Am J Clin Nutr. 2005;82(4):733–739.

    CAS  PubMed  Google Scholar 

  10. Okamoto, K, Horisawa, R, Kawamura, T, et al. Menstrual and reproductive factors for subarachnoid hemorrhage risk in women: a case-control study in Nagoya, Japan. Stroke. 2001;32(12): 2841–2844.

    CAS  PubMed  Google Scholar 

  11. Ryu, S, Chang, Y, Choi, Y, et al. Age at menarche and nonalcoholic fatty liver disease. J Hepatol. 2015;62(5):1164–1170.

    PubMed  Google Scholar 

  12. Stinton, LM, Shaffer, EA Epidemiology of gallbladder disease: cholelithiasis and cancer. Gut Liver. 2012;6(2):172–187.

    PubMed  PubMed Central  Google Scholar 

  13. Sun, H, Tang, H, Jiang, S, et al. Gender and metabolic differences of gallstone diseases. World J Gastroenterol. 2009;15(15):1886–1891.

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Cirillo, DJ, Wallace, RB, Rodabough, RJ, et al. Effect of estrogen therapy on gallbladder disease. JAMA. 2005;293(3): 330–339.

    CAS  PubMed  Google Scholar 

  15. Shaffer, EA Epidemiology and risk factors for gallstone disease: has the paradigm changed in the 21st century? Curr Gastroenterol Rep. 2005;7(2):132–140.

    PubMed  Google Scholar 

  16. Portincasa, P, Moschetta, A, Palasciano, G Cholesterol gallstone disease. Lancet. 2006;368(9531):230–239.

    CAS  PubMed  Google Scholar 

  17. Demerath, EW, Towne, B, Chumlea, WC, et al. Recent decline in age at menarche: the Fels Longitudinal Study. Am J Hum Biol. 2004;16(4):453–457.

    PubMed  Google Scholar 

  18. 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(1):89–94.

    PubMed  Google Scholar 

  19. Everhart, JE, Ruhl, CE Burden of digestive diseases in the United States part I: overall and upper gastrointestinal diseases. Gastro-enterology. 2009;136(2):376–386.

    Google Scholar 

  20. Chen, YC, Chiou, C, Lin, MN, Lin, CL The prevalence and risk factors for gallstone disease in Taiwanese vegetarians. PLoS One. 2014;9(12):e115145.

    PubMed  PubMed Central  Google Scholar 

  21. Basso, L, McCollum, PT, Darling, MR, Tocchi, A, Tanner, WA A study of cholelithiasis during pregnancy and its relationship with age, parity, menarche, breast-feeding, dysmenorrhea, oral contra-ception and a maternal history of cholelithiasis. Surg Gynecol Obstet. 1992;175(1):41–46.

    CAS  PubMed  Google Scholar 

  22. Liu, B, Beral, V, Balkwill A; Million Women Study Collaborators. Childbearing, breastfeeding, other reproductive factors and the subsequent risk of hospitalization for gallbladder disease. Int J Epidemiol. 2009;38(1):312–318.

    PubMed  Google Scholar 

  23. Chang, Y, Kim, BK, Yun, KE, et al. Metabolically-healthy obesity and coronary artery calcification. J Am Coll Cardiol. 2014; 63(24):2679–2686.

    PubMed  Google Scholar 

  24. Gaudineau, A, Ehlinger, V, Vayssiere, C, Jouret, B, Arnaud, C, Godeau, E Factors associated with early menarche: results from the French Health Behaviour in School-aged Children (HBSC) study. BMC Public Health. 2010;10:175.

    PubMed  PubMed Central  Google Scholar 

  25. Craig, CL, Marshall, AL, Sjostrom, M, et al. International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc. 2003;35(8):1381–1395.

    PubMed  Google Scholar 

  26. Oh, JY, Yang, YJ, Kim, BS, Kang, JH Validity and reliability of Korean version of International Physical Activity Questionnaire (IPAQ) short form. Korean J Fam Med. 2007; 28(7):532–541.

    Google Scholar 

  27. Wen, CP, David Cheng, TY, Tsai, SP, et al. Are Asians at greater mortality risks for being overweight than Caucasians? Redefining obesity for Asians. Public Health Nutr. 2009;12(4): 497–506.

    PubMed  Google Scholar 

  28. Malavolti, M, Mussi, C, Poli, M, et al. Cross-calibration of eight-polar bioelectrical impedance analysis versus dual-energy X-ray absorptiometry for the assessment of total and appendicular body composition in healthy subjects aged 21-82 years. Ann Hum Biol. 2003;30(4):380–391.

    CAS  PubMed  Google Scholar 

  29. Everhart, JE, Khare, M, Hill, M, Maurer, KR Prevalence and ethnic differences in gallbladder disease in the United States. Gastro-enterology. 1999;117(3):632–639.

    CAS  Google Scholar 

  30. Harlow, SD, Gass, M, Hall, JE, et al. Executive summary of the Stages of Reproductive Aging Workshop P 10: addressing the unfinished agenda of staging reproductive aging. J Clin Endocri-nol Metab. 2012;97(4):1159–1168.

    CAS  Google Scholar 

  31. 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(8):1036–1043.

    CAS  Google Scholar 

  32. Feng, Y, Hong, X, Wilker, E, et al. Effects of age at menarche, reproductive years, and menopause on metabolic risk factors for cardiovascular diseases. Atherosclerosis. 2008;196(2): 590–597.

    CAS  PubMed  Google Scholar 

  33. Stender, S, Nordestgaard, BG, Tybjaerg-Hansen, A Elevated body mass index as a causal risk factor for symptomatic gallstone dis-ease: a Mendelian randomization study. Hepatology. 2013;58(6): 2133–2141.

    CAS  PubMed  Google Scholar 

  34. Nervi, F, Miquel, JF, Alvarez, M, et al. Gallbladder disease is associated with insulin resistance in a high risk Hispanic popula-tion. J Hepatol. 2006;45(2):299–305.

    CAS  PubMed  Google Scholar 

  35. Chang, Y, Sung, E, Ryu, S, Park, YW, Jang, YM, Park, M Insulin resistance is associated with gallstones even in non-obese, non-diabetic Korean men. J Korean Med Sci. 2008;23(4): 644–650.

    PubMed  PubMed Central  Google Scholar 

  36. Poretsky, L, Cataldo, NA, Rosenwaks, Z, Giudice, LC The insulin-related ovarian regulatory system in health and disease. Endocr Rev. 1999;20(4):535–582.

    CAS  PubMed  Google Scholar 

  37. Thijs, C, Knipschild, P Oral contraceptives and the risk of gall-bladder disease: a meta-analysis. Am J Public Health. 1993;83(8): 1113–1120.

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Hulley, S, Grady, D, Bush, T, et al. Randomized trial of estrogen plus progestin for secondary prevention of coronary heart disease in postmenopausal women. Heart and Estrogen/progestin Replacement Study (HERS) Research Group. JAMA. 1998; 280(7):605–613.

    CAS  PubMed  Google Scholar 

  39. Wang, HH, Liu, M, Clegg, DJ, Portincasa, P, Wang, DQ New insights into the molecular mechanisms underlying effects of estrogen on cholesterol gallstone formation. Biochim Biophys Acta. 2009;1791(11):1037–1047.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Brand, JS, Chan, MF, Dowsett, M, et al. Cigarette smoking and endogenous sex hormones in postmenopausal women. J Clin Endocrinol Metab. 2011;96(10):3184–3192.

    CAS  PubMed  Google Scholar 

  41. Law, MR, Hackshaw, AK A meta-analysis of cigarette smoking, bone mineral density and risk of hip fracture: recognition of a major effect. BMJ. 1997;315(7112):841–846.

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Al-Zoughool, M, Dossus, L, Kaaks, R, et al. Risk of endometrial cancer in relationship to cigarette smoking: results from the EPIC study. Int J Cancer. 2007;121(12):2741–2747.

    CAS  PubMed  Google Scholar 

  43. Luo, J, Margolis, KL, Wactawski-Wende, J, et al. Association of active and passive smoking with risk of breast cancer among postmenopausal women: a prospective cohort study. BMJ. 2011;342:d1016.

    PubMed  PubMed Central  Google Scholar 

  44. Casey, VA, Dwyer, JT, Coleman, KA, Krall, EA, Gardner, J, Vala-dian, I Accuracy of recall by middle-aged participants in a longitudinal study of their body size and indices of maturation earlier in life. Ann Hum Biol. 1991;18(2):155–166.

    CAS  PubMed  Google Scholar 

  45. Rhoads, GG, Kagan, A The relation of coronary disease, stroke, and mortality to weight in youth and in middle age. Lancet. 1983; 1(8323):492–495.

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Occupational and Environmental Medicine, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Samsung Main Building B2, 250, Taepyung-ro 2ga, Jung-gu, Seoul, 04514, South Korea

    Seungho Ryu MD, PhD, Yoosoo Chang MD, PhD & Byung Seong Suh MD, PhD

  2. Center for Cohort Studies, Total Healthcare Center, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, South Korea

    Seungho Ryu MD, PhD, Yoosoo Chang MD, PhD, Yuni Choi BS, Min-Jung Kwon MD, PhD, Kyung Eun Yun MD, PhD, Hyun-Suk Jung MD, Bo-Kyoung Kim MD, Yoo Jin Kim MPH, Juhee Cho PhD & Eun Chul Chung MD, PhD

  3. Department of Clinical Research Design and Evaluation, SAIHST, Sungkyunkwan University, Seoul, South Korea

    Seungho Ryu MD, PhD, Yoosoo Chang MD, PhD & Juhee Cho PhD

  4. Department of Laboratory Medicine, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, South Korea

    Min-Jung Kwon MD, PhD

  5. Department of Obstetrics and Gynecology, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, South Korea

    Kye-Hyun Kim MD, PhD

  6. Department of Radiology, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, South Korea

    Eun Chul Chung MD, PhD

  7. Department of Family Medicine, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, South Korea

    Hocheol Shin MD, PhD

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  1. Seungho Ryu MD, PhD
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  2. Yoosoo Chang MD, PhD
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  3. Yuni Choi BS
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  4. Min-Jung Kwon MD, PhD
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  9. Kye-Hyun Kim MD, PhD
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  13. Byung Seong Suh MD, PhD
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Corresponding authors

Correspondence to Seungho Ryu MD, PhD or Yoosoo Chang MD, PhD.

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Ryu, S., Chang, Y., Choi, Y. et al. Age at Menarche and Gallstone Disease in Middle-Aged Women. Reprod. Sci. 23, 1304–1313 (2016). https://doi.org/10.1177/1933719116638187

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