Advertisement

Associations Between Breastfeeding History and Early Postmenopausal Bone Loss

  • Chantal M. J. de Bakker
  • Lauren A. Burt
  • Leigh Gabel
  • David A. Hanley
  • Steven K. BoydEmail author
Original Research
  • 35 Downloads

Abstract

This study aimed to evaluate associations of parity and breastfeeding history with postmenopausal bone loss. Early postmenopausal women from the Canadian Multicentre Osteoporosis Study were divided into three groups based on their reproductive histories: nulliparous (NP, n = 10), parous with < 6 months breastfeeding (P-NBF, n = 14), and parous with > 6 months breastfeeding (P-BF, n = 21). Women underwent dual X-ray absorptiometry and high-resolution peripheral quantitative computed tomography imaging at baseline and after 6 years to evaluate bone mineral density (BMD), bone microstructure, and finite element-estimated failure load. Average age at baseline was 57 years. Baseline density, microstructure, and failure load were not different among groups. In all women, total and cortical BMD decreased significantly at the tibia and radius. P-BF women only experienced a significant decline in tibial trabecular BMD, with a greater magnitude of change for P-BF than NP women (p = 0.002). Overall, results suggest that early postmenopausal bone health did not differ based on parity or breastfeeding history. Over the 6-year follow-up period, postmenopausal bone loss was evident in all women, with subtle differences in the rate of postmenopausal change among women with varying breastfeeding histories. Parous women who had breastfed for at least 6 months showed an elevated rate of trabecular BMD loss at the tibia. Meanwhile, correlation analyses suggest that longer durations of breastfeeding may be associated with reduced cortical bone loss at the radius. The lack of differences among groups in FE-derived failure load suggests that parity and breastfeeding history is unlikely to significantly affect postmenopausal risk of fracture.

Keywords

Bone microarchitecture High-resolution peripheral quantitative computed tomography Menopause Breastfeeding Parity 

Notes

Acknowledgements

Thank you to all of the participants who volunteered their time to take part in this study. The authors also would like to thank Anne Cooke, Taryn Harris, Duncan Raymond, Jane Allan, and Bernice Love for participant recruitment, questionnaire administration, and scan acquisition. This study was funded by the Canadian Institutes of Health Research (CIHR) MOP-106611. CMJdB and LG were supported by an Alberta Innovates Postgraduate Fellowship and T. Chen Fong Postdoctoral Fellowship (Department of Radiology, Cumming School of Medicine, University of Calgary).

Authors Contributions

Study design: CMJdB, LAB, DAH, SKB. Data acquisition & analysis: CMJdB, LAB, LG, SKB. Drafting of manuscript: CMJdB, LAB, LG. All authors contributed to revising the manuscript and approved the final version of the submitted manuscript. CMJdB and SKB take responsibility for the integrity of the data analysis, and all authors agree to be accountable for the work.

Compliance with Ethical Standards

Conflicts of interest

Chantal MJ de Bakker, Lauren A Burt, Leigh Gabel, and Steven K Boyd have nothing to disclose. David A Hanley reports grants and personal fees from Amgen and Eli Lilly outside of the submitted work.

Human and Animal Rights

All procedures in this study were approved by the University of Calgary Conjoint Health Research Ethics Board and are in accordance with international ethical standards.

Informed Consent

Informed consent was obtained from all participants prior to study initiation.

Supplementary material

223_2019_638_MOESM1_ESM.docx (18 kb)
Supplementary file1 (DOCX 17 kb)
223_2019_638_MOESM2_ESM.docx (4.9 mb)
Supplementary file2 (DOCX 4996 kb)
223_2019_638_MOESM3_ESM.docx (9.1 mb)
Supplementary file3 (DOCX 9290 kb)

References

  1. 1.
    Kanis JA (2002) Diagnosis of osteoporosis and assessment of fracture risk. Lancet 359:1929–1936PubMedCrossRefGoogle Scholar
  2. 2.
    Clarke BL, Khosla S (2010) Female reproductive system and bone. Arch Biochem Biophys 503:118–128PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Fox KM, Magaziner J, Sherwin R, Scott JC, Plato CC, Nevitt M, Cummings S (1993) Reproductive correlates of bone mass in elderly women. Study of Osteoporotic Fractures Research Group. J Bone Miner Res 8:901–908PubMedCrossRefGoogle Scholar
  4. 4.
    Goshtasebi A, Berger C, Barr SI, Kovacs CS, Towheed T, Davison KS, Prior JC (2018) Adult premenopausal bone health related to reproductive characteristics-population-based data from the Canadian Multicentre Osteoporosis Study (CaMos). Int J Environ Res Public Health 15:E1023PubMedCrossRefGoogle Scholar
  5. 5.
    Wysolmerski JJ (2002) The evolutionary origins of maternal calcium and bone metabolism during lactation. J Mammary Gland Biol Neoplasia 7:267–276PubMedCrossRefGoogle Scholar
  6. 6.
    Kovacs CS (2016) Maternal mineral and bone metabolism during pregnancy, lactation, and post-weaning recovery. Physiol Rev 96:449–547PubMedCrossRefGoogle Scholar
  7. 7.
    VanHouten JN, Wysolmerski JJ (2003) Low estrogen and high parathyroid hormone-related peptide levels contribute to accelerated bone resorption and bone loss in lactating mice. Endocrinology 144:5521–5529PubMedCrossRefGoogle Scholar
  8. 8.
    Kalkwarf HJ, Specker BL, Bianchi DC, Ranz J, Ho M (1997) The effect of calcium supplementation on bone density during lactation and after weaning. N Engl J Med 337:523–528PubMedCrossRefGoogle Scholar
  9. 9.
    Karlsson C, Obrant KJ, Karlsson M (2001) Pregnancy and lactation confer reversible bone loss in humans. Osteoporos Int 12:828–834PubMedCrossRefGoogle Scholar
  10. 10.
    Sowers M, Corton G, Shapiro B, Jannausch ML, Crutchfield M, Smith ML, Randolph JF, Hollis B (1993) Changes in bone density with lactation. JAMA 269:3130–3135PubMedCrossRefGoogle Scholar
  11. 11.
    Ensom MH, Liu PY, Stephenson MD (2002) Effect of pregnancy on bone mineral density in healthy women. Obstet Gynecol Surv 57:99–111PubMedCrossRefGoogle Scholar
  12. 12.
    Moller UK, Vieth Streym S, Mosekilde L, Rejnmark L (2012) Changes in bone mineral density and body composition during pregnancy and postpartum. A controlled cohort study. Osteoporos Int 23:1213–1223PubMedCrossRefGoogle Scholar
  13. 13.
    Cooke-Hubley S, Kirby BJ, Valcour JE, Mugford G, Adachi JD, Kovacs CS (2017) Spine bone mineral density increases after 6 months of exclusive lactation, even in women who keep breastfeeding. Arch Osteoporos 12:73PubMedCrossRefGoogle Scholar
  14. 14.
    Cheung AM, Adachi JD, Hanley DA et al (2013) High-resolution peripheral quantitative computed tomography for the assessment of bone strength and structure: a review by the Canadian Bone Strength Working Group. Curr Osteoporos Rep 11:136–146PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Samelson EJ, Broe KE, Xu H et al (2019) Cortical and trabecular bone microarchitecture as an independent predictor of incident fracture risk in older women and men in the Bone Microarchitecture International Consortium (BoMIC): a prospective study. Lancet Diabetes Endocrinol 7:34–43PubMedCrossRefGoogle Scholar
  16. 16.
    Bjørnerem A, Ghasem-Zadeh A, Wang X, Bui M, Walker SP, Zebaze R, Seeman E (2017) Irreversible deterioration of cortical and trabecular microstructure associated with breastfeeding. J Bone Miner Res 32:681–687PubMedCrossRefGoogle Scholar
  17. 17.
    Brembeck P, Lorentzon M, Ohlsson C, Winkvist A, Augustin H (2015) Changes in cortical volumetric bone mineral density and thickness, and trabecular thickness in lactating women postpartum. J Clin Endocrinol Metab 100:535–543PubMedCrossRefGoogle Scholar
  18. 18.
    Burt LA, Hanley DA, Boyd SK (2017) Cross-sectional versus longitudinal change in a prospective HR-pQCT study. J Bone Miner Res 32:1505–1513PubMedCrossRefGoogle Scholar
  19. 19.
    Macdonald HM, Nishiyama KK, Kang J, Hanley DA, Boyd SK (2011) Age-related patterns of trabecular and cortical bone loss differ between sexes and skeletal sites: a population-based HR-pQCT study. J Bone Miner Res 26:50–62CrossRefPubMedGoogle Scholar
  20. 20.
    World Health Organization (2014) Comprehensive implementation plan on maternal, infant, and young child nutrition. World Health Organization, GenevaGoogle Scholar
  21. 21.
    Prior JC (1998) Perimenopause: the complex endocrinology of the menopausal transition. Endocr Rev 19:397–428PubMedCrossRefGoogle Scholar
  22. 22.
    Shepherd JA, Schousboe JT, Broy SB, Engelke K, Leslie WD (2015) Executive summary of the 2015 ISCD position development conference on advanced measures from DXA and QCT: fracture prediction beyond BMD. J Clin Densitom 18:274–286PubMedCrossRefGoogle Scholar
  23. 23.
    Looker AC, Wahner HW, Dunn WL, Calvo MS, Harris TB, Heyse SP, Johnston CC Jr, Lindsay R (1998) Updated data on proximal femur bone mineral levels of US adults. Osteoporos Int 8:468–489PubMedCrossRefGoogle Scholar
  24. 24.
    Burt LA, Manske SL, Hanley DA, Boyd SK (2018) Lower bone density, impaired microarchitecture, and strength predict future fragility fracture in postmenopausal women: 5-year follow-up of the calgary CaMos cohort. J Bone Miner Res 33:589–597PubMedCrossRefGoogle Scholar
  25. 25.
    Buie HR, Campbell GM, Klinck RJ, MacNeil JA, Boyd SK (2007) Automatic segmentation of cortical and trabecular compartments based on a dual threshold technique for in vivo micro-CT bone analysis. Bone 41:505–515CrossRefPubMedGoogle Scholar
  26. 26.
    Burghardt AJ, Buie HR, Laib A, Majumdar S, Boyd SK (2010) Reproducibility of direct quantitative measures of cortical bone microarchitecture of the distal radius and tibia by HR-pQCT. Bone 47:519–528PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Boutroy S, Bouxsein ML, Munoz F, Delmas PD (2005) In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab 90:6508–6515PubMedCrossRefGoogle Scholar
  28. 28.
    MacNeil JA, Boyd SK (2008) Improved reproducibility of high-resolution peripheral quantitative computed tomography for measurement of bone quality. Med Eng Phys 30:792–799PubMedCrossRefGoogle Scholar
  29. 29.
    Macneil JA, Boyd SK (2008) Bone strength at the distal radius can be estimated from high-resolution peripheral quantitative computed tomography and the finite element method. Bone 42:1203–1213PubMedCrossRefGoogle Scholar
  30. 30.
    Pistoia W, van Rietbergen B, Lochmuller EM, Lill CA, Eckstein F, Ruegsegger P (2002) Estimation of distal radius failure load with micro-finite element analysis models based on three-dimensional peripheral quantitative computed tomography images. Bone 30:842–848PubMedCrossRefGoogle Scholar
  31. 31.
    de Bakker CM, Li Y, Zhao H, Leavitt L, Tseng WJ, Lin T, Tong W, Qin L, Liu XS (2018) Structural adaptations in the rat tibia bone induced by pregnancy and lactation confer protective effects against future estrogen deficiency. J Bone Miner Res 33(12):2165–2176PubMedCrossRefPubMedCentralGoogle Scholar
  32. 32.
    Alderman BW, Weiss NS, Daling JR, Ure CL, Ballard JH (1986) Reproductive history and postmenopausal risk of hip and forearm fracture. Am J Epidemiol 124:262–267PubMedCrossRefGoogle Scholar
  33. 33.
    Cure-Cure C, Cure-Ramirez P, Teran E, Lopez-Jaramillo P (2002) Bone-mass peak in multiparity and reduced risk of bone-fractures in menopause. Int J Gynaecol Obstet 76:285–291PubMedCrossRefGoogle Scholar
  34. 34.
    Mori T, Ishii S, Greendale GA, Cauley JA, Ruppert K, Crandall CJ, Karlamangla AS (2015) Parity, lactation, bone strength, and 16-year fracture risk in adult women: findings from the Study of Women's Health Across the Nation (SWAN). Bone 73:160–166PubMedCrossRefGoogle Scholar
  35. 35.
    Cooke-Hubley S, Gao Z, Mugford G et al (2019) Parity and lactation are not associated with incident fragility fractures or radiographic vertebral fractures over 16 years of follow-up: Canadian Multicentre Osteoporosis Study (CaMos). Arch Osteoporos 14:49PubMedCrossRefGoogle Scholar
  36. 36.
    de Bakker CM, Altman-Singles AR, Li Y, Tseng WJ, Li C, Liu XS (2017) Adaptations in the microarchitecture and load distribution of maternal cortical and trabecular bone in response to multiple reproductive cycles in rats. J Bone Miner Res 32:1014–1026PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Wiklund PK, Xu L, Wang Q et al (2012) Lactation is associated with greater maternal bone size and bone strength later in life. Osteoporos Int 23:1939–1945PubMedCrossRefGoogle Scholar
  38. 38.
    Specker B, Binkley T (2005) High parity is associated with increased bone size and strength. Osteoporos Int 16:1969–1974PubMedCrossRefGoogle Scholar
  39. 39.
    Recker R, Lappe J, Davies K, Heaney R (2000) Characterization of perimenopausal bone loss: a prospective study. J Bone Miner Res 15:1965–1973PubMedCrossRefGoogle Scholar
  40. 40.
    Greendale GA, Sowers M, Han W, Huang MH, Finkelstein JS, Crandall CJ, Lee JS, Karlamangla AS (2012) Bone mineral density loss in relation to the final menstrual period in a multiethnic cohort: results from the Study of Women's Health Across the Nation (SWAN). J Bone Miner Res 27:111–118PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Burt LA, Bhatla JL, Hanley DA, Boyd SK (2017) Cortical porosity exhibits accelerated rate of change in peri- compared with post-menopausal women. Osteoporos Int 28:1423–1431PubMedCrossRefGoogle Scholar
  42. 42.
    Seifert-Klauss V, Fillenberg S, Schneider H, Luppa P, Mueller D, Kiechle M (2012) Bone loss in premenopausal, perimenopausal and postmenopausal women: results of a prospective observational study over 9 years. Climacteric 15:433–440PubMedCrossRefGoogle Scholar
  43. 43.
    Bjørnerem A, Bui QM, Ghasem-Zadeh A, Hopper JL, Zebaze R, Seeman E (2013) Fracture risk and height: an association partly accounted for by cortical porosity of relatively thinner cortices. J Bone Miner Res 28:2017–2026PubMedCrossRefGoogle Scholar
  44. 44.
    Natland ST, Andersen LF, Nilsen TI, Forsmo S, Jacobsen GW (2012) Maternal recall of breastfeeding duration twenty years after delivery. BMC Med Res Methodol 12:179PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Radiology, Cumming School of Medicine, McCaig Institute for Bone and Joint HealthUniversity of CalgaryCalgaryCanada

Personalised recommendations