Skip to main content

Advertisement

Log in

How does women’s bone health recover after lactation? A systematic review and meta-analysis

  • Review
  • Published:
Osteoporosis International Aims and scope Submit manuscript

Abstract

Mini abstract

This is a systematic review aiming to evaluate the recovery of bone mass after lactation-related loss. Bone loss is transitory with recovery depending on the return of menstruation and weaning, and several compensatory homeostatic mechanisms are involved to minimize any significant damage to the maternal skeleton.

Abstract

Lactation has been associated with significant temporary bone loss, especially during the exclusive breastfeeding period. In the bone recovery phase, there is wide methodological heterogeneity among clinical trials, including follow-up timing, methods and sites of bone measurements, and body composition changes. The purpose of this study is to perform a systematic review and meta-analysis aiming to evaluate the recovery rate of bone mass after lactation-related loss, including the PubMed, Web of Science, and Scopus databases, with no publication date restrictions. The following MeSH terms were used: “bone diseases,” “bone resorption,” “bone density,” “osteoporosis,” “calcium,” “postpartum period,” “weaning,” “breast feeding,” and “lactation.” The inclusion criteria were as follows: prospective human studies in women of reproductive age and bone measurements with two assessments in the postpartum period at least: the first one within the first weeks of lactation and another one 12 months after delivery, 3 months following the return of menses or 3 months postweaning. This research was recorded on the Prospero database (CRD42018096586Bone). A total of 9455 studies were found and 32 papers met the inclusion criteria. The follow-up period ranged from one to 3.6 years postpartum. Lactation was associated with transient bone loss, with a strong tendency to recover in all the sites studied, depending on the return of menstruation and weaning. Small deficits in the microarchitecture of the peripheral skeleton may be present, especially in women with prolonged breastfeeding, but with no deficit regarding the hip geometry was found. Women with a successive gestation after prolonged lactation and women who had breastfed when adolescents had no significant bone loss. Bone loss related to lactation is transitory, and several compensatory homeostatic mechanisms are involved to minimize any significant damage to the maternal skeleton.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. World Health Organization. Infant and young child feeding. http://www.who.int/news-room/fact-sheets/detail/infant-and-young-child-feeding (accessed Nov 20, 2018)

  2. Fund UNCs (2018) Breastfeeding. A mother’s gift, for every child

  3. Kovacs CS (2016) Maternal mineral and bone metabolism during pregnancy, lactation, and post-weaning recovery. Physiol Rev 96:449–547

    Article  CAS  PubMed  Google Scholar 

  4. Holmberg-Marttila, Sievanen H (2000) Factors underluing changes in bone mineral during postpartum amenorrhea and lactation. Osteoporos Int 11:570–576

    Article  CAS  PubMed  Google Scholar 

  5. Wysolmerski JJ (2010) Interactions between breast, bone, and brain regulate mineral and skeletal metabolism during lactation. Ann N Y Acad Sci 1192:161–169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Grizzo FM, da Silva MJ, Pinheiro MM, Jorgetti V, Carvalho MDB, Pelloso SM (2015) Pregnancy and lactation-associated osteoporosis: bone histomorphometric analysis and response to treatment with Zoledronic acid. Calcif Tissue Int 4:421–425

    Article  CAS  Google Scholar 

  7. Sowers M, Eyre D, Hollis BW, Randolph JF, Shapiro B, Jannausch ML, Crutchfield M (1995) Biochemical markers of bone turnover in lactating and nonlactating postpartum women. J Clin Endocrinol Metab 80:2210–2216

    CAS  PubMed  Google Scholar 

  8. Sowers M, Randolph J, Shapiro B, Jannausch M (1995) A prospective study of bone density and pregnancy after and extended period of lactation with bone loss. Obstet Gynecol 85:285–289

    Article  CAS  PubMed  Google Scholar 

  9. López JM, González G, Reyes V, Campino C, Díaz S (1996) Bone turnover and density in healthy women during breastfeeding and after weaning. Osteoporos Int 6:153–159

    Article  PubMed  Google Scholar 

  10. Krebs NF, Reidinger CJ, Robertson AD, Brenner M (1997) Bone mineral density changes during lactation: maternal, dietary, and biochemical correlates. Am J Clin Nutr 65:1738–1746

    Article  CAS  PubMed  Google Scholar 

  11. Laskey MA, Prentice A (2004) Do appendicular bone measurements reflect changes in the axial skeleton? J Clin Densitom 7:296–301

    Article  PubMed  Google Scholar 

  12. Bezerra FF, Mendonça LMC, Lobato EC, O’Brien KO, Donangelo CM (2004) Bone mass is recovered from lactation to postweaning in adolescent mothers with low calciuim intakes. Am J Clin Nutr 80:1322–1326

    Article  CAS  PubMed  Google Scholar 

  13. Akesson A, Vahter M, Berglund M, Eklof T, Bremme K, Bjellerup P (2004) Bone turnover from early pregnancy to postweaning. Acta Obstet Gynecol Scand 83:1049–1055

    Article  PubMed  Google Scholar 

  14. Mansur JL, Malpeli A, Etchegoyen G, de Santiago S, Kuzminzuk M, González H (2005) Cambios por 12 meses en la densidad mineral ósea y en la composición corporal durante la lactancia en adolescentes. Revista Argentina de Endocrinologia y Metabolismo 42:148–156

    Google Scholar 

  15. Sámano R, Morales RM, Flores-Garcia A, Lira J, Isoard F, de Santiago S, Casanueva E (2011) Las adolescentes no pierden densidad mineral ósea en el posparto: estudio comparativo con adultas. Salud Publica Mex 53:1–10

    Article  Google Scholar 

  16. Glerean M, Furci A, Galich AM, Fama B, Plantalech L (2010) Bone and mineral metabolism in primiparous women and its relationship with breastfeeding: a longitudinal study. Medicina (B Aires) 70:227–232

    CAS  Google Scholar 

  17. Laskey MA, Price RI, Khoo BC, Prentice A (2011) Proximal femur structural geometry changes during and following lactation. Bone 48:755–759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Costa ML, Krupa FG, Rehder PM, Sousa MH, Costa-Paiva L, Cecatti JG (2012) Forearm bone mineral density changes during postpartum and the effects of breastfeeding, amenorrhea, body mass index and contraceptive use. Osteoporos Int 23:1691–1698

    Article  CAS  PubMed  Google Scholar 

  19. Mendez RO, Gallegos AN, Cabrera RM, Quihui L, Zozaya R, Morales GG, Valencia ME, Méndez M (2013) Bone mineral density changes in lactating adolescent mothers during the first postpartum year. Am J Hum Biol 25:222–224

    Article  PubMed  Google Scholar 

  20. Sámano R, Martínez-Rojano H, Rodriguez-Ventura A, Godínez-Martinez E, Tolentino M, López-de-Cárdenas G, Isoard F, de Santiago S (2014) Bone biomarkers and its relation with bone mineral density in adults and adolescents during the first year postpartum. Arquivos latinoamericanos de nutrición 64:24–33

    Google Scholar 

  21. 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 100:535–543

    Article  CAS  PubMed  Google Scholar 

  22. Bjørnerem Å, Ghasem-Zadeh A, Wang X et al (2017) Irreversible deterioration of cortical and trabecular microstructure associated with breastfeeding. J Bone Miner Res 32:681–687

    Article  PubMed  Google Scholar 

  23. Sowers M, Corton G, Shapiro B, Jannausch ML, Crutchfiels M, Smith ML, Randolph JF, Hohllis B (1993) Changes in bone density with lactation. JAMA 269:3130–3135

    Article  CAS  PubMed  Google Scholar 

  24. Affinito P, Tommaselli GA, di Carlo C, Guida F, Nappi C (1996) Changes in bone mineral density and calcium metabolism in breastfeeding women: a one year follow-up study. J Clin Endocrinol Metab 81:2314–2318

    CAS  PubMed  Google Scholar 

  25. Ritchie LD, Fung EB, Halloran BP, Turnlund JR, Loan MDV, Cann CE, King JC (1998) A longitudinal study of calcium homeostasis during human pregnancy and lactation and after resumption of menses. Am J Clin Nutr 67:693–701

    Article  CAS  PubMed  Google Scholar 

  26. Hopkinson JM, Butte NF, Ellis K, Smith O’B. Lactation delays postpartum bone mineral accretion and temporatily alters its regional distribution in women. J Nutr 1999; 777–783

  27. More C, Bettembuk P, Bhattoa HP, Balogh A (2001) The effects of pregnancy and lactation on bone mineral density. Osteoporos Int 12:732–737

    Article  CAS  PubMed  Google Scholar 

  28. Pearson D, Kaur M, San P, Lawson N, Baker P, Hosking D (2004) Recovery of pregnancy mediated bone loss during lactation. Bone 34:570–578

    Article  CAS  PubMed  Google Scholar 

  29. Koltkoff N, Eiken P, Kristensen B, Nielsen SP (1997) Bone mineral changes during pregnancy and lactation: a longitudinal cohort study. Clin Sci 94:405–412

    Article  Google Scholar 

  30. Laskey MA, Prentice A (1999) Bone mineral changes during and after lactation. Obstet Gynecol 94:608–615

    CAS  PubMed  Google Scholar 

  31. Karlsson C, Obrant KJ, Karlsson M (2001) Pregnancy and lactation confer reversible bone loss in humans. Osteoporos Int 12:828–834

    Article  CAS  PubMed  Google Scholar 

  32. Malpeli A, Mansur JL, de Santiago S, Villalobos R, Armanini A, Apezteguía M, González HF (2009) Changes in bone mineral density of adolescent mothers during the 12-month postpartum period. Public Health Nutr 13:1522–1527

    Article  PubMed  Google Scholar 

  33. Kulkarni B, Shatrugna V, Nagalla B, Kumar PA, Rani KU, Omkar AC (2009) Maternal weight and lean body mass may influence the lactation-related bone chances in young undernourished Indian women. Br J Nutr 101:1527–1533

    Article  CAS  PubMed  Google Scholar 

  34. Hellmeryer L, Hahn B, Fischer C, Hars O, Boekhoff J, Maier J, Hadji P (2015) Quantitative ultrasonometry during pregnancy and lactation: a longitudinal study. Osteoporos Int 26:1147–1154

    Article  Google Scholar 

  35. Ensom MH, Liu PY, Stephenson MD (2002) Effect of pregnancy on bone mineral density in healthy women. Obstet Gynecol Surv 57:99–111

    Article  PubMed  Google Scholar 

  36. Salari P, Abdollahi M (2014) The influence of pregnancy and lactation on maternal bone health: a systematic review. J Family Reprod Health 8:135–148

    PubMed  PubMed Central  Google Scholar 

  37. Shamseer L, Moher D, Clarke M et al (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. BMJ 350:g7647

    Article  PubMed  Google Scholar 

  38. Hutton B, Salanti G, Caldwell DM, Chaimani A, Schmid CH, Cameron C, Ioannidis JP, Straus S, Thorlund K, Jansen JP, Mulrow C, Catalá-López F, Gøtzsche PC, Dickersin K, Boutron I, Altman DG, Moher D (2015) The PRISMA extension statement for reporting of systematic reviews incorporating network meta-analyses of health care interventions: checklist and explanations. Ann Intern Med 162:777–784

    Article  PubMed  Google Scholar 

  39. Higgins JPT, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558

    Article  PubMed  Google Scholar 

  40. DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–188

    Article  CAS  PubMed  Google Scholar 

  41. Palmer TM, Sterne JAC (2009) Meta-analysis in Stata: an updated collection from the Stata Journal. StataCorp LP

  42. Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088–1101

    Article  CAS  PubMed  Google Scholar 

  43. Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Hozo SP, Djulbegovic B, Hozo I (2005) Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 5:13

    Article  PubMed  PubMed Central  Google Scholar 

  45. Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25:603–605

    Article  PubMed  Google Scholar 

  46. Kent GN, Price RI, Gutteridge DH et al (1990) Human lactation: forearm trabecular bone loss, increased bone turnover, and renal conservation of calcium and inorganic phosphate with recovery of bone mass following weaning. J Bone Miner Res 5:361–369

    Article  CAS  PubMed  Google Scholar 

  47. Kent GN, Price RI, Gutteridge DH, Allen JR, Rosman KJ, Smith M, Bhagat C, Wilson SG, Retallack RW (1993) Effect of pregnancy and lactation on maternal bone mass and calcium metabolism. Osteoporos Int (Suppl 1):S44–S47

  48. Møller UK, Streym SV, Mosekilde L, Rejnmark L (2012) Changes in bone mineral density and body composition during pregnancy and postpartum. A controlled cohort study. Osteoporos Int 23:1213–1223

    Article  PubMed  Google Scholar 

  49. Salles JP (2016) Bone metabolism during pregnancy. Ann Endocrinol (Paris) 77:163–168

    Article  Google Scholar 

  50. Kovacs CS (2017) The skeleton is a storehouse of mineral that is plundered during lactation and (fully?) replenished afterwards. J Bone Miner Res 32:676–680

    Article  CAS  PubMed  Google Scholar 

  51. Kovacs CS, Ralston SH (2015) Presentation and management of osteoporosis presenting in association with pregnancy or lactation. Osteoporos Int 26:2223–2241

    Article  CAS  PubMed  Google Scholar 

  52. Fudge NJ, Kovacs CS (2010) Pregnancy up-regulates intestinal calcium absorption and skeletal mineralization independently of the vitamin D receptor. Endocrinology 151:886–895

    Article  CAS  PubMed  Google Scholar 

  53. Jarniven TL (2003) Novel paradigm on the effect of estrogen on bone. J Musculoskelet Neuronal Interact 3:374–380

    Google Scholar 

  54. O'Callaghan KM, Kiely ME (2018) Ethnic disparities in the dietary requirement for vitamin D during pregnancy: considerations for nutrition policy and research. Proc Nutr Soc 77(2):164–173

    Article  CAS  PubMed  Google Scholar 

  55. Bolotin, H. H., Sievänen, H., Grashuis, J. L., Kuiper, J. W., & Järvinen, T. L. N. (2001). Inaccuracies inherent in patient‐specific dual‐energy X‐ray absorptiometry bone mineral density measurements: Comprehensive phantom‐based evaluation. Journal of bone and mineral research, 16(2), 417–426.

  56. Specker B, Binkley T (2005) High parity is associated with increased bone size and strength. Osteoporos Int 16:1969–1974

    Article  PubMed  Google Scholar 

  57. 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 23:1939–1945

    Article  CAS  PubMed  Google Scholar 

  58. Chantry CJ, Auinger P, Byrd RS (2004) Lactation among adolescent mothers and subsequent bone mineral density. Arch Pediatr Adolesc Med 158:650–656

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to F. M. F. Grizzo.

Ethics declarations

Conflicts of interest

None.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

>

ESM 1

(DOCX 13.7 kb)

ESM 2

(DOCX 31.1 kb)

ESM 3

(DOCX 16.5 kb)

ESM 4

(DOCX 166 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Grizzo, F.M.F., Alarcão, A.C.J., Dell’ Agnolo, C.M. et al. How does women’s bone health recover after lactation? A systematic review and meta-analysis. Osteoporos Int 31, 413–427 (2020). https://doi.org/10.1007/s00198-019-05236-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-019-05236-8

Keywords

Navigation