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.
Similar content being viewed by others
References
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)
Fund UNCs (2018) Breastfeeding. A mother’s gift, for every child
Kovacs CS (2016) Maternal mineral and bone metabolism during pregnancy, lactation, and post-weaning recovery. Physiol Rev 96:449–547
Holmberg-Marttila, Sievanen H (2000) Factors underluing changes in bone mineral during postpartum amenorrhea and lactation. Osteoporos Int 11:570–576
Wysolmerski JJ (2010) Interactions between breast, bone, and brain regulate mineral and skeletal metabolism during lactation. Ann N Y Acad Sci 1192:161–169
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
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
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
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
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
Laskey MA, Prentice A (2004) Do appendicular bone measurements reflect changes in the axial skeleton? J Clin Densitom 7:296–301
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
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
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
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
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
Laskey MA, Price RI, Khoo BC, Prentice A (2011) Proximal femur structural geometry changes during and following lactation. Bone 48:755–759
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
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
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
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
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
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
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
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
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
More C, Bettembuk P, Bhattoa HP, Balogh A (2001) The effects of pregnancy and lactation on bone mineral density. Osteoporos Int 12:732–737
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
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
Laskey MA, Prentice A (1999) Bone mineral changes during and after lactation. Obstet Gynecol 94:608–615
Karlsson C, Obrant KJ, Karlsson M (2001) Pregnancy and lactation confer reversible bone loss in humans. Osteoporos Int 12:828–834
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
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
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
Ensom MH, Liu PY, Stephenson MD (2002) Effect of pregnancy on bone mineral density in healthy women. Obstet Gynecol Surv 57:99–111
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
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
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
Higgins JPT, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558
DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–188
Palmer TM, Sterne JAC (2009) Meta-analysis in Stata: an updated collection from the Stata Journal. StataCorp LP
Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088–1101
Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634
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
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
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
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
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
Salles JP (2016) Bone metabolism during pregnancy. Ann Endocrinol (Paris) 77:163–168
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
Kovacs CS, Ralston SH (2015) Presentation and management of osteoporosis presenting in association with pregnancy or lactation. Osteoporos Int 26:2223–2241
Fudge NJ, Kovacs CS (2010) Pregnancy up-regulates intestinal calcium absorption and skeletal mineralization independently of the vitamin D receptor. Endocrinology 151:886–895
Jarniven TL (2003) Novel paradigm on the effect of estrogen on bone. J Musculoskelet Neuronal Interact 3:374–380
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
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.
Specker B, Binkley T (2005) High parity is associated with increased bone size and strength. Osteoporos Int 16:1969–1974
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
Chantry CJ, Auinger P, Byrd RS (2004) Lactation among adolescent mothers and subsequent bone mineral density. Arch Pediatr Adolesc Med 158:650–656
Author information
Authors and Affiliations
Corresponding author
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.
Rights and permissions
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00198-019-05236-8