Skip to main content

Age at menarche in relation to prenatal rainy season exposure and altitude of residence: results from a nationally representative survey in a tropical country

  • E. C. Jansen (a1), O. F. Herrán (a2), N. L. Fleischer (a1) (a3), A. M. Mondul (a1) and E. Villamor (a1) (a4)...
  • Please note a correction has been issued for this article.

Intrauterine exposure to the rainy season in the tropics may be accompanied by high rates of infection and nutritional deficiencies. It is unknown whether this exposure is related to the extrauterine timing of development. Our aim was to evaluate the relations of prenatal exposure to the rainy season and altitude of residence with age at menarche. The study included 15,370 girls 10 to <18 years old who participated in Colombia’s 2010 National Nutrition Survey. Primary exposures included the number of days exposed to the rainy season during the 40 weeks preceding birth, and altitude of residence at the time of the survey. We estimated median menarcheal ages and hazard ratios with 95% confidence interval (CI) according to exposure categories using Kaplan–Meier cumulative probabilities and Cox proportional hazards models, respectively. All tests incorporated the complex survey design. Girls in the highest quintile of gestation days exposed to the rainy season had an earlier age at menarche compared with those in the lowest (adjusted hazard ratios (HR)=1.08; 95% CI 1.00–1.18, P-trend=0.03). Girls living at altitudes ⩾2000 m had a later age at menarche compared with those living <1000 m (adjusted HR=0.88; 95% CI 0.82–0.94, P-trend <0.001). The inverse association between gestation days during the rainy season and menarche was most apparent among girls living at altitudes ⩾2000 m (P, interaction=0.04). Gestation days exposed to the rainy season and altitude of residence were associated with the timing of sexual maturation among Colombian girls independent of socioeconomic status and ethnicity.

Corresponding author
*Address for correspondence: E. C. Jansen, Department of Nutritional Sciences, University of Michigan School of Public Health, 1415 Washington Heights, Ann Arbor, MI 48109, USA. (Email
Hide All
1. Horn, J, Opdahl, S, Engstrom, MJ, et al. Reproductive history and the risk of molecular breast cancer subtypes in a prospective study of Norwegian women. Cancer Causes Control. 2014; 25, 881889.
2. 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, 2940.
3. Cole, TJ. Secular trends in growth. Proc Nutr Soc. 2000; 59, 317324.
4. Instituto Geografico Agustin Codazzi. Imprenta Nacional de Colombia: Bogota, Cundinamarca, Colombia, 49–50.
5. Ramirez, AP, Mendoza, AR, Montoya, JM, et al. Mortality associated with peak seasons of influenza virus circulation in Bogota, Colombia, 1997-2005. Rev Panam Salud Publica. 2009; 26, 435439.
6. Ntwenya, JE, Kinabo, J, Msuya, J, Mamiro, P, Majili, ZS. Dietary patterns and household food insecurity in rural populations of Kilosa district, Tanzania. PLoS One. 2015; 10, e0126038.
7. Moore, SE, Cole, TJ, Poskitt, EM, et al. Season of birth predicts mortality in rural Gambia. Nature. 1997; 388, 434.
8. Gluckman, PD, Beedle, AS, Hanson, MA, Low, FM. Human growth: evolutionary and life history perspectives. Nestle Nutr Inst Workshop Ser. 2013; 71, 89102.
9. Klis, K, Jarzebak, K, Borowska-Struginska, B, et al. Season of birth influences the timing of first menstruation. Am J Hum Biol. 2015; 2, 226–232.
10. Matchock, RL, Susman, EJ, Brown, FM. Seasonal rhythms of menarche in the United States: correlates to menarcheal age, birth age, and birth month. Womens Health Iss. 2004; 14, 184192.
11. Gonzales, GF, Villena, A. Body mass index and age at menarche in Peruvian children living at high altitude and at sea level. Hum Biol. 1996; 68, 265275.
12. Freyre, EA, Ortiz, MV. The effect of altitude on adolescent growth and development. J Adolesc Health Care. 1988; 9, 144149.
13. Greksa, LP. Age of menarche in Bolivian girls of European and Aymara ancestry. Ann Hum Biol. 1990; 17, 4953.
14. Wiley, AS. An Ecology of High-Altitude Infancy: A Biocultural Perspective. 2004. Cambridge University Press: New York, USA.
15. Encuesta Nacional de la Situacion Nutricional en Colombia 2010. Bogotá: ICBF, Instituto Colombiano de Bienestar Familiar; 2011.
16. Poveda, G, Alvarez, DM, Rueda, OA. Hydro-climatic variability over the Andes of Colombia associated with ENSO: a review of climatic processes and their impact on one of the Earth’s most important biodiversity hotspots. Climate Dynam. 2011; 36, 22332249.
17. Pacheco, Y, Leon-Aristizabal, G. Clasificación climática de la Orinoquia Colombiana a partir de los patrones de circulación atmosférica. Meteorol Colomb. 2001; 4, 117120.
18. Villar, JCE, Ronchail, J, Guyot, JL, et al. Spatio-temporal rainfall variability in the Amazon basin countries (Brazil, Peru, Bolivia, Colombia, and Ecuador). Int J Climatol. 2009; 29, 15741594.
19. Jansen, EC, Herran, OF, Villamor, E. Trends and correlates of age at menarche in Colombia: results from a nationally representative survey. Econ Hum Biol. 2015; 19, 138144.
20. Kleinbaum, D, Klein, M. Survival Analysis: A Self-Learning Text, 3rd edn, 2012. Springer Science and Business Media: New York, NY.
21. Jongbloet, PH, Kersemaekers, WM, Zielhuis, GA, Verbeek, AL. Menstrual disorders and month of birth. Ann Hum Biol. 1994; 21, 511518.
22. Cagnacci, A, Pansini, FS, Bacchi-Modena, A, et al. Season of birth influences the timing of menopause. Hum Reprod. 2005; 20, 21902193.
23. Maisonet, M, Christensen, KY, Rubin, C, et al. Role of prenatal characteristics and early growth on pubertal attainment of British girls. Pediatrics. 2010; 126, e591e600.
24. Boldsen, JL. Season of birth and recalled age at menarche. J Biosoc Sci. 1992; 24, 167173.
25. Graham, EA, Mulkey, SS, Kitajima, K, Phillips, NG, Wright, SJ. Cloud cover limits net CO2 uptake and growth of a rainforest tree during tropical rainy seasons. Proc Natl Acad Sci U S A. 2003; 100, 572576.
26. Parisi, AV, Turnbull, DJ, Downs, NJ. Influence of high levels of cloud cover on vitamin D effective and erythemal solar UV irradiances. Photochem Photobiol Sci. 2012; 11, 18551859.
27. Reiter, RJ, Tan, DX, Korkmaz, A, Rosales-Corral, SA. Melatonin and stable circadian rhythms optimize maternal, placental and fetal physiology. Hum Reprod Update. 2014; 20, 293307.
28. Polwiang, S. The seasonal reproduction number of dengue fever: impacts of climate on transmission. PeerJ. 2015; 3, e1069.
29. Oringanje, C, Meremikwu, M, Ogar, B, Okon, A, Udoh, A. Patterns of cord, placental and post-delivery maternal malaria parasitemia. Acta Obstet Gynecol Scand. 2010; 89, 12061209.
30. Rodriguez-Martinez, CE, Rodriguez, DA, Nino, G. Respiratory syncytial virus, adenoviruses, and mixed acute lower respiratory infections in children in a developing country. J Med Virol. 2015; 87, 774781.
31. Graham, MA. “No somos iguales”: the effect of household economic standing on women’s energy intake in the Andes. Soc Sci Med. 2004; 58, 22912300.
32. Villamor, E, Marin, C, Mora-Plazas, M, Baylin, A. Vitamin D deficiency and age at menarche: a prospective study. Am J Clin Nutr. 2011; 94, 10201025.
33. Crozier, SR, Harvey, NC, Inskip, HM, et al. Maternal vitamin D status in pregnancy is associated with adiposity in the offspring: findings from the Southampton Women’s Survey. Am J Clin Nutr. 2012; 96, 5763.
34. Lee, JM, Appugliese, D, Kaciroti, N, et al. Weight status in young girls and the onset of puberty. Pediatrics. 2007; 119, e624e630.
35. Di Renzo, GC, Spano, F, Giardina, I, et al. Iron deficiency anemia in pregnancy. Womens Health (Lond). 2015; 11, 891900.
36. Uauy, R, Kain, J, Corvalan, C. How can the developmental origins of health and disease (DOHaD) hypothesis contribute to improving health in developing countries? Am J Clin Nutr. 2011; 94, 1759S1764SS.
37. Khorram, O, Keen-Rinehart, E, Chuang, TD, Ross, MG, Desai, M. Maternal undernutrition induces premature reproductive senescence in adult female rat offspring. Fertil Steril. 2015; 103, 2918 e2.
38. Correia-Branco, A, Keating, E, Martel, F. Maternal undernutrition and fetal developmental programming of obesity: the glucocorticoid connection. Reprod Sci. 2015; 22, 138145.
39. 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, 10361043.
40. Frisancho, AR. Developmental functional adaptation to high altitude: review. Am J Hum Biol. 2013; 25, 151168.
41. Hui, LL, Leung, GM, Lam, TH, Schooling, CM. Premature birth and age at onset of puberty. Epidemiology. 2012; 23, 415422.
42. Castilho, SD, Nucci, LB, Assuino, SR, Hansen, LO. The importance of memory bias in obtaining age of menarche by recall method in Brazilian adolescents. Arq Bras Endocrinol Metabol. 2014; 58, 394397.
43. Lepkowski, JM, Mosher, WD, Groves, RM, et al. Responsive design, weighting, and variance estimation in the 2006–2010 National survey of family growth. Vital Health Stat 2. 2013; 158, 152.
44. Azevedo, V, Bouillon, C. Social Mobility in Latin America: A Review of Existing Evidence. 2009. Inter-American Development Bank: Washington, DC.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Journal of Developmental Origins of Health and Disease
  • ISSN: 2040-1744
  • EISSN: 2040-1752
  • URL: /core/journals/journal-of-developmental-origins-of-health-and-disease
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed