Association Between Parity and Bone Mineral Density in the National Health and Nutrition Examination Survey.

Cristina M Gildee, Patricia Ann Kramer
Author Information
  1. Cristina M Gildee: Department of Anthropology, University of Washington, Seattle, Washington, USA. ORCID
  2. Patricia Ann Kramer: Department of Anthropology, University of Washington, Seattle, Washington, USA.

Abstract

OBJECTIVE: Bone remodeling relies on a dynamic process of concurrent deposition and resorption of bone material, which regulates bone mineral density (BMD), a critical component of overall bone health. Chronic dysregulation of the remodeling process during an individual's life can result in low BMD, osteoporosis, reduced mineral reserves and/or increased fracture risk. Prior studies have investigated the link between parity and BMD, positing that one cost of reproduction is increased bone resorption above deposition, resulting in net BMD loss. Further, bone remodeling is sensitive to repetitive mechanical loading, suggesting that differences in bone loading could modify associations between parity and BMD. We seek to understand how reproductive investment (using parity as a proxy) challenges bone remodeling.
METHODS: We examined associations between parity and regional BMD using anthropometric, dual-energy x-ray absorptiometry, and questionnaire data from the National Health and Nutrition Examination Survey (2007-2018 cohorts; n���=���5144).
RESULTS: In unadjusted linear regressions, higher parity was associated with lower BMD in all regions except the thoracic spine, arms, and total BMD (p���<���0.004). In regressions adjusting for BMI and age, parity was positively associated with BMD in the pelvis, arms, and total BMD (p���<���0.004). The maximally controlled models, which adjust for race/ethnicity, sedentary time, poverty income ratio, and lifetime estrogen exposure, among other health and lifestyle variables, yielded similar results.
DISCUSSION: Our results suggest that more rigorous statistical modeling and selection of reproductive cost variables may help explicate the biological mechanisms underlying conflicting parity-BMD associations and their impact on bone health and aging.

Keywords

References

  1. Amiri, M., I. Nabipour, B. Larijani, et al. 2008. ���The Relationship of Absolute Poverty and Bone Mineral Density in Postmenopausal Iranian Women.��� International Journal of Public Health 53, no. 6: 290���296. https://doi.org/10.1007/S00038���008���8033���X.
  2. Baird, D. T., S. Cnattingius, J. Collins, et al. 2006. ���Nutrition and Reproduction in Women.��� Human Reproduction Update 12, no. 3: 193���207. https://doi.org/10.1093/HUMUPD/DMK003.
  3. Bj��rnerem, ��., L. A. Ahmed, L. J��rgensen, J. St��rmer, and R. M. Joakimsen. 2011. ���Breastfeeding Protects Against Hip Fracture in Postmenopausal Women: The Troms�� Study.��� Journal of Bone and Mineral Research 26, no. 12: 2843���2850. https://doi.org/10.1002/JBMR.496.
  4. Borer, K. T. 2005. ���Physical Activity in the Prevention and Amelioration of Osteoporosis in Women Interaction of Mechanical, Hormonal and Dietary Factors.��� Sports Medicine 35, no. 9: 779���830.
  5. Center for Health Statistics. 2018. ���NHANES Body Composition Procedures Manual.���
  6. Christen, P., K. Ito, R. Ellouz, et al. 2014. ���Bone Remodelling in Humans is Load���Driven but not Lazy.��� Nature Communications 5, no. 1: 1���5. https://doi.org/10.1038/ncomms5855.
  7. Crane, J. L., K. E. Ackerman, A. R. Verardo, and L. K. Bachrach. 2020. ���Hormonal Contraception and Bone Health in Adolescents.��� Frontiers in Endocrinology 1: 603. https://doi.org/10.3389/fendo.2020.00603.
  8. Dufour, D. L., and M. L. Sauther. 2002. ���Comparative and Evolutionary Dimensions of the Energetics of Human Pregnancy and Lactation.��� American Journal of Human Biology 14, no. 5: 584���602. https://doi.org/10.1002/ajhb.10071.
  9. Ellison, P. T. 2003. ���Energetics and Reproductive Effort.��� American Journal of Human Biology 15, no. 3: 342���351. https://doi.org/10.1002/AJHB.10152.
  10. Eriksen, E. F. 2010. ���Cellular Mechanisms of Bone Remodeling.��� Reviews in Endocrine and Metabolic Disorders 11, no. 4: 219���227. https://doi.org/10.1007/S11154���010���9153���1.
  11. Felson, D. T., Y. Zhang, M. T. Hannan, W. B. Kannel, and D. P. Kiel. 1995. ���Alcohol Intake and Bone Mineral Density in Elderly Men and Women: The Framingham Study.��� American Journal of Epidemiology 142, no. 5: 485���492. https://doi.org/10.1093/OXFORDJOURNALS.AJE.A117664.
  12. Frost, H. M. 2003. ���Bone's Mechanostat: A 2003 Update.��� Anatomical Record���Part A Discoveries in Molecular, Cellular, and Evolutionary Biology 275, no. 2: 1081���1101. https://doi.org/10.1002/AR.A.10119.
  13. Genant, H. K., K. Engelke, T. Fuerst, et al. 1996. ���Noninvasive Assessment of Bone Mineral and Structure: State of the Art.��� Journal of Bone and Mineral Research 11, no. 6: 707���730. https://doi.org/10.1002/jbmr.5650110602.
  14. Ginaldi, L., M. C. Benedetto, and M. Martinis. 2005. ���Osteoporosis, Inflammation and Ageing.��� Immunity & Ageing 2, no. 1: 14. https://doi.org/10.1186/1742���4933���2���14.
  15. Gittleman, J. L., and S. D. Thompson. 1988. ���Energy Allocation in Mammalian Reproduction.��� American Zoologist 28: 863���875. https://academic.oup.com/icb/article/28/3/863/99186.
  16. Greene, D. A., and G. A. Naughton. 2006. ���Adaptive Skeletal Responses to Mechanical Loading During Adolescence.��� Sports Medicine 36, no. 9: 723���732. https://doi.org/10.2165/00007256���200636090���00001.
  17. Grobman, W. A., C. B. Parker, M. Willinger, et al. 2018. ���Racial Disparities in Adverse Pregnancy Outcomes and Psychosocial Stress.��� Obstetrics and Gynecology 131, no. 2: 328���335. https://doi.org/10.1097/AOG.0000000000002441.
  18. Gunter, K. B., H. C. Almstedt, and K. F. Janz. 2012. ���Physical Activity in Childhood May be the Key to Optimizing Lifespan Skeletal Health.��� Exercise and Sport Sciences Reviews 40, no. 1: 13���21. https://doi.org/10.1097/JES.0B013E318236E5EE.
  19. Gur, A., K. Nas, R. Cevik, A. J. Sarac, S. Ataoglu, and M. Karakoc. 2003. ���Influence of Number of Pregnancies on Bone Mineral Density in Postmenopausal Women of Different Age Groups.��� Journal of Bone and Mineral Metabolism 21: 234���241.
  20. Hillier, T. A., J. H. Rizzo, K. L. Pedula, et al. 2003. ���Nulliparity and Fracture Risk in Older Women: The Study of Osteoporotic Fractures.��� Journal of Bone and Mineral Research 18, no. 5: 893���899. https://doi.org/10.1359/JBMR.2003.18.5.893.
  21. Holbrook, T. L., and E. Barrett���Connor. 1993. ���A Prospective Study of Alcohol Consumption and Bone Mineral Density.��� British Medical Journal 306, no. 6891: 1506���1509. https://doi.org/10.1136/BMJ.306.6891.1506.
  22. Hwang, I. R., Y. K. Choi, W. K. Lee, et al. 2016. ���Association Between Prolonged Breastfeeding and Bone Mineral Density and Osteoporosis in Postmenopausal Women: KNHANES 2010���2011.��� Osteoporosis International 27, no. 1: 257���265. https://doi.org/10.1007/S00198���015���3292���X.
  23. InterLACE Study Team. 2019. ���Variations in Reproductive Events Across Life: A Pooled Analysis of Data From 505 147 Women Across 10 Countries.��� Human Reproduction (Oxford, England) 34, no. 5: 881���893. https://doi.org/10.1093/HUMREP/DEZ015.
  24. Jasienska, G., R. G. Bribiescas, A. S. Furberg, S. Helle, and A. N����ez���de la Mora. 2017. ���Human Reproduction and Health: An Evolutionary Perspective.��� Lancet 390, no. 10093: 510���520. https://doi.org/10.1016/S0140���6736(17)30573���1.
  25. Kanis, J. A., L. J. Melton, C. Christiansen, C. C. Johnston, and N. Khaltaev. 1994. ���The Diagnosis of Osteoporosis.��� Journal of Bone and Mineral Research 9, no. 8: 1137���1141. https://doi.org/10.1002/JBMR.5650090802.
  26. Kirkwood, T. B. L., and M. R. Rose. 1991. ���Evolution of Senescence: Late Survival Sacrificed for Reproduction.��� Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 332, no. 1262: 15���24. https://doi.org/10.1098/RSTB.1991.0028.
  27. Lee, E. N. 2019. ���Effects of Parity and Breastfeeding Duration on Bone Density in Postmenopausal Women.��� Asian Nursing Research 13, no. 2: 161���167. https://doi.org/10.1016/j.anr.2019.04.002.
  28. Lovett, J. L., M. A. Chima, J. K. Wexler, et al. 2017. ���Oral Contraceptives Cause Evolutionarily Novel Increases in Hormone Exposure: A Risk Factor for Breast Cancer.��� Evolution, Medicine, and Public Health 2017, no. 1: 97���108. https://doi.org/10.1093/EMPH/EOX009.
  29. Madimenos, F. C. 2015. ���An Evolutionary and Life���History Perspective on Osteoporosis.��� Annual Review of Anthropology 44, no. 1: 189���206. https://doi.org/10.1146/Annurev���Anthro���102214���013954.
  30. Madimenos, F. C., J. J. Snodgrass, M. A. Liebert, T. J. Cepon, and L. S. Sugiyama. 2012. ���Reproductive Effects on Skeletal Health in Shuar Women of Amazonian Ecuador: A Life History Perspective.��� American Journal of Human Biology 24, no. 6: 841���852. https://doi.org/10.1002/AJHB.22329.
  31. Melton, L. J. 1997. ���The Prevalence of Osteoporosis.��� Journal of Bone and Mineral Research 12, no. 11: 1769���1771. https://doi.org/10.1359/JBMR.1997.12.11.1769.
  32. Mundy, G. R. 2007. ���Osteoporosis and Inflammation.��� Nutrition Reviews 65, no. 12: 147���151. https://doi.org/10.1111/j.1753���4887.2007.tb00353.x.
  33. Murphy, S., K. T. Khaw, H. May, and J. E. Compston. 1994. ���Parity and Bone Mineral Density in Middle���Aged Women.��� Osteoporosis International: A Journal Established as Result of Cooperation Between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 4, no. 3: 162���166. https://doi.org/10.1007/BF01623063.
  34. Navarro, M. C., M. Sosa, P. Saavedra, et al. 2009. ���Poverty is a Risk Factor for Osteoporotic Fractures.��� Osteoporosis International 20, no. 3: 393���398. https://doi.org/10.1007/S00198���008���0697���9.
  35. Pate, R. R., H. M. MacDonald, and V. P. S. Tan. 2012. ���Physical Activity and Children's Bone Health: A Little Goes a Long Way.��� Exercise and Sport Sciences Reviews 40, no. 1: 2���3. https://doi.org/10.1097/JES.0B013E31823CD77A.
  36. Prentice, A. 2003. ���Micronutrients and the Bone Mineral Content of the Mother, Fetus and Newborn.��� Journal of Nutrition 133, no. 5: 1693S���1699S. https://doi.org/10.1093/JN/133.5.1693S.
  37. Prentice, A. M., and A. Prentice. 1988. ���Energy Costs of Lactation.��� Annual Review of Nutrition 8: 63���79. https://doi.org/10.1146/annurev.nu.08.070188.000431.
  38. Psaki, S. R., E. K. Chuang, A. J. Melnikas, D. B. Wilson, and B. S. Mensch. 2019. ���Causal Effects of Education on Sexual and Reproductive Health in Low and Middle���Income Countries: A Systematic Review and Meta���Analysis.��� SSM ��� Population Health 8: 100386. https://doi.org/10.1016/J.SSMPH.2019.100386.
  39. Rasgon, N. L., C. Magnusson, A. L. V. Johansson, N. L. Pedersen, S. Elman, and M. Gatz. 2005. ���Endogenous and Exogenous Hormone Exposure and Risk of Cognitive Impairment in Swedish Twins: A Preliminary Study.��� Psychoneuroendocrinology 30, no. 6: 558���567. https://doi.org/10.1016/J.PSYNEUEN.2005.01.004.
  40. Reginster, J. Y., and N. Burlet. 2006. ���Osteoporosis: A Still Increasing Prevalence.��� Bone 38, no. 2 Suppl 1: 4���9. https://doi.org/10.1016/J.BONE.2005.11.024.
  41. Ruff, C., B. Holt, and E. Trinkaus. 2006. ���Who's Afraid of the Big Bad Wolff?: ���Wolff's Law��� and Bone Functional Adaptation.��� American Journal of Physical Anthropology 129, no. 4: 484���498. https://doi.org/10.1002/AJPA.20371.
  42. Shams���White, M. M., M. Chung, M. Du, et al. 2017. ���Dietary Protein and Bone Health: A Systematic Review and Meta���Analysis From the National Osteoporosis Foundation.��� American Journal of Clinical Nutrition 105, no. 6: 1528���1543. https://doi.org/10.3945/AJCN.116.145110.
  43. Sharma, N., T. Natung, R. Barooah, and S. S. Ahanthem. 2016. ���Effect of Multiparity and Prolonged Lactation on Bone Mineral Density.��� Journal of Menopausal Medicine 22, no. 3: 161���166. https://doi.org/10.6118/JMM.2016.22.3.161.
  44. Song, S. Y., Y. Kim, H. Park, Y. J. Kim, W. Kang, and E. Y. Kim. 2017. ���Effect of Parity on Bone Mineral Density: A Systematic Review and Meta���Analysis.��� Bone 101: 70���76. https://doi.org/10.1016/J.BONE.2017.04.013.
  45. Specker, B., and T. Binkley. 2005. ���High Parity Is Associated With Increased Bone Size and Strength.��� Osteoporosis International: A Journal Established as Result of Cooperation Between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 16, no. 12: 1969���1974. https://doi.org/10.1007/S00198���005���1978���1.
  46. Stieglitz, J., B. A. Beheim, B. C. Trumble, F. C. Madimenos, H. Kaplan, and M. Gurven. 2015. ���Low Mineral Density of a Weight���Bearing Bone Among Adult Women in a High Fertility Population.��� American Journal of Physical Anthropology 156, no. 4: 637���648. https://doi.org/10.1002/AJPA.22681.
  47. Sugiyama, T., A. Yamaguchi, and S. Kawai. 2002. ���Effects of Skeletal Loading on Bone Mass and Compensation Mechanism in Bone: A New Insight Into the Mechanostat Theory.��� Journal of Bone and Mineral Metabolism 20, no. 4: 196���200. https://doi.org/10.1007/S007740200028.
  48. Vargas Zapata, C. L., C. M. Donangelo, L. R. Woodhouse, S. A. Abrams, E. Martin Spencer, and J. C. King. 2004. ���Calcium Homeostasis During Pregnancy and Lactation in Brazilian Women With Low Calcium Intakes: A Longitudinal Study 1���4.��� American Journal of Clinical Nutrition 80: 417���439.
  49. Wallace, I. J., S. Worthington, D. T. Felson, et al. 2017. ���Knee Osteoarthritis has Doubled in Prevalence Since the Mid���20th Century.��� Proceedings of the National Academy of Sciences of the United States of America 114, no. 35: 9332���9336. https://doi.org/10.1073/PNAS.1703856114.
  50. Yang, Y., S. Wang, and H. Cong. 2022. ���Association Between Parity and Bone Mineral Density in Postmenopausal Women.��� BMC Women's Health 22, no. 1: 87. https://doi.org/10.1186/S12905���022���01662���9.
  51. Zhu, K., and R. L. Prince. 2012. ���Calcium and Bone.��� Clinical Biochemistry 45, no. 12: 936���942. https://doi.org/10.1016/J.CLINBIOCHEM.2012.05.006.

Grants

  1. T32AG066574/NIH HHS
  2. P2C HD042828/NICHD NIH HHS

MeSH Term

Humans
Bone Density
Female
Nutrition Surveys
Parity
Adult
Middle Aged
United States
Young Adult
Aged
Absorptiometry, Photon
Bone Remodeling

Word Cloud

Created with Highcharts 10.0.0BMDboneparityremodelinghealthassociationsBoneprocessdepositionresorptionmineralincreasedcostreproductionloadingreproductiveusingNationalHealthNutritionExaminationSurveyregressionsassociatedarmstotalp���<���0004variablesresultsOBJECTIVE:reliesdynamicconcurrentmaterialregulatesdensitycriticalcomponentoverallChronicdysregulationindividual'slifecanresultlowosteoporosisreducedreservesand/orfractureriskPriorstudiesinvestigatedlinkpositingoneresultingnetlosssensitiverepetitivemechanicalsuggestingdifferencesmodifyseekunderstandinvestmentproxychallengesMETHODS:examinedregionalanthropometricdual-energyx-rayabsorptiometryquestionnairedata2007-2018cohortsn���=���5144RESULTS:unadjustedlinearhigherlowerregionsexceptthoracicspineadjustingBMIagepositivelypelvismaximallycontrolledmodelsadjustrace/ethnicitysedentarytimepovertyincomeratiolifetimeestrogenexposureamonglifestyleyieldedsimilarDISCUSSION:suggestrigorousstatisticalmodelingselectionmayhelpexplicatebiologicalmechanismsunderlyingconflictingparity-BMDimpactagingAssociationParityMineralDensityNHANES

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