Skip to main content
Top
Published in: Archives of Osteoporosis 1/2022

01-12-2022 | Osteoporosis | Review

Bone metabolism and osteoporosis during pregnancy and lactation

Authors: Abraham Yair Lujano-Negrete, Martha Cecilia Rodríguez-Ruiz, Cassandra Michele Skinner-Taylor, Lorena Perez-Barbosa, Jesus Alberto Cardenas de la Garza, Pedro Alberto García-Hernández, Luis Gerardo Espinosa-Banuelos, Luz Fernanda Gutierrez-Leal, Sofia Jezzini-Martínez, Dionicio Ángel Galarza-Delgado

Published in: Archives of Osteoporosis | Issue 1/2022

Login to get access

Abstract

Purpose

Osteoporosis in pregnancy is an uncommon disease and there is little information regarding its pathogenesis and its effects on the skeleton. This review aims to describe changes in mineral metabolism during pregnancy and lactation as well as their clinical impact.

Methods

We performed a narrative review of the literature using the PubMed and Google Scholar databases for articles published from 1955 to 2021.

Results

Mineral metabolism in the mother must adapt to the demand created by the fetus and the placenta, which together absorb calcium and other minerals from the mother to mineralize the developing fetal skeleton; analyses of iliac bone biopsies at the beginning and end of pregnancy have shown that pregnancy significantly modifies maternal bone status. The greatest demand for calcium for the maternal skeleton occurs during lactation; women who breastfeed have an even greater loss of calcium to produce milk. However, it is controversial whether breastfeeding can increase the risk of osteoporotic fractures, and the possible mechanism is considerably complicated. Osteoporosis in pregnancy is an uncommon disease characterized by the occurrence of fragility fractures, most commonly in the vertebral column, in the third trimester of pregnancy, or early postpartum. The pathogenesis of PLO remains unclear owing to its rarity; DXA provides a sensitive and specific method for diagnosing osteoporosis by measuring BMD, one of the parameters that allow a better understanding of fracture risk. One limitation is the controversy in using radiation in pregnant women and the risk to the embryo/fetus; a safe alternative can be MRI.

Conclusion

Pregnancy and lactation alter the maternal bone status; without a balance in metabolism, this may cause an increased risk of fracture due to changes in BMD. There is little information on BMD during pregnancy; more clinical studies are required to elucidate if this represents a risk factor for osteoporosis.
Literature
1.
go back to reference Sanz-Salvador L, García-Pérez M, Tarín JJ, Cano A (2015) Bone metabolic changes during pregnancy: a period of vulnerability to osteoporosis and fracture. Eur J Endocrinol 172:R53-65PubMedCrossRef Sanz-Salvador L, García-Pérez M, Tarín JJ, Cano A (2015) Bone metabolic changes during pregnancy: a period of vulnerability to osteoporosis and fracture. Eur J Endocrinol 172:R53-65PubMedCrossRef
2.
go back to reference Camacho PM, Petak SM, Binkley N et al (2020) American Association of Clinical Endocrinologists/American College of Endocrinology Clinical Practice guidelines for the diagnosis and treatment of postmenopausal osteoporosis-2020 UPDATE. Endocr Pract 26:1–46PubMedCrossRef Camacho PM, Petak SM, Binkley N et al (2020) American Association of Clinical Endocrinologists/American College of Endocrinology Clinical Practice guidelines for the diagnosis and treatment of postmenopausal osteoporosis-2020 UPDATE. Endocr Pract 26:1–46PubMedCrossRef
3.
go back to reference Leere JS, Vestergaard P (2019) Calcium metabolic disorders in pregnancy: primary hyperparathyroidism, pregnancy-induced osteoporosis, and vitamin D deficiency in pregnancy. Endocrinol Metab Clin North Am 48:643–655PubMedCrossRef Leere JS, Vestergaard P (2019) Calcium metabolic disorders in pregnancy: primary hyperparathyroidism, pregnancy-induced osteoporosis, and vitamin D deficiency in pregnancy. Endocrinol Metab Clin North Am 48:643–655PubMedCrossRef
4.
go back to reference Phillips AJ, Ostlere SJ, Smith R (2000) Pregnancy-associated osteoporosis: does the skeleton recover? Osteoporos Int 11:449–454PubMedCrossRef Phillips AJ, Ostlere SJ, Smith R (2000) Pregnancy-associated osteoporosis: does the skeleton recover? Osteoporos Int 11:449–454PubMedCrossRef
5.
go back to reference Barbour LA, Kick SD, Steiner JF, LoVerde ME, Heddleston LN, Lear JL, Barón AE, Barton PL (1994) A prospective study of heparin-induced osteoporosis in pregnancy using bone densitometry. Am J Obstet Gynecol 170:862–869PubMedCrossRef Barbour LA, Kick SD, Steiner JF, LoVerde ME, Heddleston LN, Lear JL, Barón AE, Barton PL (1994) A prospective study of heparin-induced osteoporosis in pregnancy using bone densitometry. Am J Obstet Gynecol 170:862–869PubMedCrossRef
6.
go back to reference Kovacs CS (2016) Maternal mineral and bone metabolism during pregnancy, lactation, and post-weaning recovery. Physiol Rev 96:449–547PubMedCrossRef Kovacs CS (2016) Maternal mineral and bone metabolism during pregnancy, lactation, and post-weaning recovery. Physiol Rev 96:449–547PubMedCrossRef
7.
go back to reference Shahtaheri SM, Aaron JE, Johnson DR, Purdie DW (1999) Changes in trabecular bone architecture in women during pregnancy. Br J Obstet Gynaecol 106:432–438PubMedCrossRef Shahtaheri SM, Aaron JE, Johnson DR, Purdie DW (1999) Changes in trabecular bone architecture in women during pregnancy. Br J Obstet Gynaecol 106:432–438PubMedCrossRef
8.
go back to reference Kovacs CS (2005) Calcium and bone metabolism during pregnancy and lactation. J Mammary Gland Biol Neoplasia 10:105–118PubMedCrossRef Kovacs CS (2005) Calcium and bone metabolism during pregnancy and lactation. J Mammary Gland Biol Neoplasia 10:105–118PubMedCrossRef
9.
go back to reference Abrams SA, Wen J, Stuff JE (1997) Absorption of calcium, zinc, and iron from breast milk by five- to seven-month-old infants. Pediatr Res 41:384–390PubMedCrossRef Abrams SA, Wen J, Stuff JE (1997) Absorption of calcium, zinc, and iron from breast milk by five- to seven-month-old infants. Pediatr Res 41:384–390PubMedCrossRef
10.
go back to reference Cross NA, Hillman LS, Allen SH, Krause GF, Vieira NE (1995) Calcium homeostasis and bone metabolism during pregnancy, lactation, and postweaning: a longitudinal study. Am J Clin Nutr 61:514–523PubMedCrossRef Cross NA, Hillman LS, Allen SH, Krause GF, Vieira NE (1995) Calcium homeostasis and bone metabolism during pregnancy, lactation, and postweaning: a longitudinal study. Am J Clin Nutr 61:514–523PubMedCrossRef
11.
go back to reference Kovacs CS (2001) Calcium and bone metabolism in pregnancy and lactation*. J Clin Endocrinol Metab 86:2344–2348PubMed Kovacs CS (2001) Calcium and bone metabolism in pregnancy and lactation*. J Clin Endocrinol Metab 86:2344–2348PubMed
12.
go back to reference Gustafsson MK, Romundstad PR, Stafne SN, Helvik A-S, Stunes AK, Mørkved S, Salvesen KÅ, Thorsby PM, Syversen U (2018) Alterations in the vitamin D endocrine system during pregnancy: a longitudinal study of 855 healthy Norwegian women. PLoS ONE 13:e0195041–e0195041PubMedPubMedCentralCrossRef Gustafsson MK, Romundstad PR, Stafne SN, Helvik A-S, Stunes AK, Mørkved S, Salvesen KÅ, Thorsby PM, Syversen U (2018) Alterations in the vitamin D endocrine system during pregnancy: a longitudinal study of 855 healthy Norwegian women. PLoS ONE 13:e0195041–e0195041PubMedPubMedCentralCrossRef
13.
go back to reference Pitkin RM (1985) Calcium metabolism in pregnancy and the perinatal period: a review. Am J Obstet Gynecol 151:99–109PubMedCrossRef Pitkin RM (1985) Calcium metabolism in pregnancy and the perinatal period: a review. Am J Obstet Gynecol 151:99–109PubMedCrossRef
14.
go back to reference Miyamoto T, Miyakoshi K, Sato Y, Kasuga Y, Ikenoue S, Miyamoto K, Nishiwaki Y, Tanaka M, Nakamura M, Matsumoto M (2019) Changes in bone metabolic profile associated with pregnancy or lactation. Sci Rep 9:6787–6787PubMedPubMedCentralCrossRef Miyamoto T, Miyakoshi K, Sato Y, Kasuga Y, Ikenoue S, Miyamoto K, Nishiwaki Y, Tanaka M, Nakamura M, Matsumoto M (2019) Changes in bone metabolic profile associated with pregnancy or lactation. Sci Rep 9:6787–6787PubMedPubMedCentralCrossRef
15.
go back to reference (1982) Prolactin and calcium metabolism in pregnancy and lactation. Nutr Rev 40:216–218 (1982) Prolactin and calcium metabolism in pregnancy and lactation. Nutr Rev 40:216–218
16.
go back to reference van den Elzen HJ, Wladimiroff JW, Overbeek TE, Morris CD, Grobbee DE (1995) Calcium metabolism, calcium supplementation and hypertensive disorders of pregnancy. Eur J Obstet Gynecol Reprod Biol 59:5–16PubMedCrossRef van den Elzen HJ, Wladimiroff JW, Overbeek TE, Morris CD, Grobbee DE (1995) Calcium metabolism, calcium supplementation and hypertensive disorders of pregnancy. Eur J Obstet Gynecol Reprod Biol 59:5–16PubMedCrossRef
17.
go back to reference Vidal L, Vidal M, Cabrera S, Ortega E, Santiváñez V, Polo J, Barnaby J, Vargas R, del Castillo A (2008) Metabolismo mineral óseo durante la gestación y efectos sobre la masa ósea de la madre. Anales de la Facultad de Medicina 69:198–205CrossRef Vidal L, Vidal M, Cabrera S, Ortega E, Santiváñez V, Polo J, Barnaby J, Vargas R, del Castillo A (2008) Metabolismo mineral óseo durante la gestación y efectos sobre la masa ósea de la madre. Anales de la Facultad de Medicina 69:198–205CrossRef
18.
go back to reference Xiao H, Zhou Q, Niu G, Han G, Zhang Z, Zhang Q, Bai J, Zhu X (2020) Association between breastfeeding and osteoporotic hip fracture in women: a dose-response meta-analysis. J Orthop Surg Res 15:15PubMedPubMedCentralCrossRef Xiao H, Zhou Q, Niu G, Han G, Zhang Z, Zhang Q, Bai J, Zhu X (2020) Association between breastfeeding and osteoporotic hip fracture in women: a dose-response meta-analysis. J Orthop Surg Res 15:15PubMedPubMedCentralCrossRef
19.
go back to reference Kovacs CS (2014) Osteoporosis presenting in pregnancy, puerperium, and lactation. Curr Opin Endocrinol Diabetes Obes 21:468–475PubMedCrossRef Kovacs CS (2014) Osteoporosis presenting in pregnancy, puerperium, and lactation. Curr Opin Endocrinol Diabetes Obes 21:468–475PubMedCrossRef
20.
go back to reference Ward KA, Adams JE, Mughal MZ (2005) Bone status during adolescence, pregnancy and lactation. Curr Opin Obstet Gynecol 17:435–439PubMedCrossRef Ward KA, Adams JE, Mughal MZ (2005) Bone status during adolescence, pregnancy and lactation. Curr Opin Obstet Gynecol 17:435–439PubMedCrossRef
21.
go back to reference Kolthoff N, Eiken P, Kristensen B, Nielsen SP (1998) Bone mineral changes during pregnancy and lactation: a longitudinal cohort study. Clin Sci (Lond) 94:405–412PubMedCrossRef Kolthoff N, Eiken P, Kristensen B, Nielsen SP (1998) Bone mineral changes during pregnancy and lactation: a longitudinal cohort study. Clin Sci (Lond) 94:405–412PubMedCrossRef
22.
go back to reference Roig Vilaseca D, Valero García C, Pilar Boncompte Vilanova M, Muñoz López J, Contreras García C, Romera Baurés M (2011) Sensibilidad, especificidad y valor predictivo positivo y negativo de los criterios de indicación de densitometría ósea de la agencia de evaluación de tecnologías e investigación médicas de cataluña. Reumatología Clínica 7:161–166PubMedCrossRef Roig Vilaseca D, Valero García C, Pilar Boncompte Vilanova M, Muñoz López J, Contreras García C, Romera Baurés M (2011) Sensibilidad, especificidad y valor predictivo positivo y negativo de los criterios de indicación de densitometría ósea de la agencia de evaluación de tecnologías e investigación médicas de cataluña. Reumatología Clínica 7:161–166PubMedCrossRef
23.
go back to reference Damilakis J, Perisinakis K, Vrahoriti H, Kontakis G, Varveris H, Gourtsoyiannis N (2002) Embryo/fetus radiation dose and risk from dual X-ray absorptiometry examinations. Osteoporos Int 13:716–722PubMedCrossRef Damilakis J, Perisinakis K, Vrahoriti H, Kontakis G, Varveris H, Gourtsoyiannis N (2002) Embryo/fetus radiation dose and risk from dual X-ray absorptiometry examinations. Osteoporos Int 13:716–722PubMedCrossRef
24.
go back to reference Ellegård L, Bertz F, Winkvist A, Bosaeus I, Brekke HK (2016) Body composition in overweight and obese women postpartum: bioimpedance methods validated by dual energy X-ray absorptiometry and doubly labeled water. Eur J Clin Nutr 70:1181–1188PubMedCrossRef Ellegård L, Bertz F, Winkvist A, Bosaeus I, Brekke HK (2016) Body composition in overweight and obese women postpartum: bioimpedance methods validated by dual energy X-ray absorptiometry and doubly labeled water. Eur J Clin Nutr 70:1181–1188PubMedCrossRef
25.
go back to reference Yıldız AE, Özbalcı AB, Ergen FB, Aydıngöz Ü (2021) Pregnancy- and lactation-associated vertebral compression fractures: MRI prevalence and characteristics. Osteoporos Int 32:981–989PubMedCrossRef Yıldız AE, Özbalcı AB, Ergen FB, Aydıngöz Ü (2021) Pregnancy- and lactation-associated vertebral compression fractures: MRI prevalence and characteristics. Osteoporos Int 32:981–989PubMedCrossRef
26.
go back to reference Ruiz-Irastorza G, Khamashta MA, Hughes GR (2002) Heparin and osteoporosis during pregnancy: 2002 update. Lupus 11:680–682PubMedCrossRef Ruiz-Irastorza G, Khamashta MA, Hughes GR (2002) Heparin and osteoporosis during pregnancy: 2002 update. Lupus 11:680–682PubMedCrossRef
27.
go back to reference Le Templier G, Rodger MA (2008) Heparin-induced osteoporosis and pregnancy. Curr Opin Pulm Med 14:403–407PubMedCrossRef Le Templier G, Rodger MA (2008) Heparin-induced osteoporosis and pregnancy. Curr Opin Pulm Med 14:403–407PubMedCrossRef
28.
go back to reference Dahlman TC (1993) Osteoporotic fractures and the recurrence of thromboembolism during pregnancy and the puerperium in 184 women undergoing thromboprophylaxis with heparin. Am J Obstet Gynecol 168:1265–1270PubMedCrossRef Dahlman TC (1993) Osteoporotic fractures and the recurrence of thromboembolism during pregnancy and the puerperium in 184 women undergoing thromboprophylaxis with heparin. Am J Obstet Gynecol 168:1265–1270PubMedCrossRef
30.
go back to reference Hawkins D, Evans J (2005) Minimising the risk of heparin-induced osteoporosis during pregnancy. Expert Opin Drug Saf 4:583–590PubMedCrossRef Hawkins D, Evans J (2005) Minimising the risk of heparin-induced osteoporosis during pregnancy. Expert Opin Drug Saf 4:583–590PubMedCrossRef
31.
go back to reference Schulman S, Hellgren-Wångdahl M (2002) Pregnancy, heparin and osteoporosis. Thromb Haemost 87:180–181PubMedCrossRef Schulman S, Hellgren-Wångdahl M (2002) Pregnancy, heparin and osteoporosis. Thromb Haemost 87:180–181PubMedCrossRef
32.
go back to reference Pettilä V, Leinonen P, Markkola A, Hiilesmaa V, Kaaja R (2002) Postpartum bone mineral density in women treated for thromboprophylaxis with unfractionated heparin or LMW heparin. Thromb Haemost 87:182–186PubMedCrossRef Pettilä V, Leinonen P, Markkola A, Hiilesmaa V, Kaaja R (2002) Postpartum bone mineral density in women treated for thromboprophylaxis with unfractionated heparin or LMW heparin. Thromb Haemost 87:182–186PubMedCrossRef
33.
go back to reference Carlin AJ, Farquharson RG, Quenby SM, Topping J, Fraser WD (2004) Prospective observational study of bone mineral density during pregnancy: low molecular weight heparin versus control. Hum Reprod 19:1211–1214PubMedCrossRef Carlin AJ, Farquharson RG, Quenby SM, Topping J, Fraser WD (2004) Prospective observational study of bone mineral density during pregnancy: low molecular weight heparin versus control. Hum Reprod 19:1211–1214PubMedCrossRef
34.
go back to reference Galambosi P, Hiilesmaa V, Ulander VM, Laitinen L, Tiitinen A, Kaaja R (2016) Prolonged low-molecular-weight heparin use during pregnancy and subsequent bone mineral density. Thromb Res 143:122–126PubMedCrossRef Galambosi P, Hiilesmaa V, Ulander VM, Laitinen L, Tiitinen A, Kaaja R (2016) Prolonged low-molecular-weight heparin use during pregnancy and subsequent bone mineral density. Thromb Res 143:122–126PubMedCrossRef
35.
go back to reference Douketis JD, Ginsberg JS, Burrows RF, Duku EK, Webber CE, Brill-Edwards P (1996) The effects of long-term heparin therapy during pregnancy on bone density. A prospective matched cohort study. Thromb Haemost 75:254–257PubMedCrossRef Douketis JD, Ginsberg JS, Burrows RF, Duku EK, Webber CE, Brill-Edwards P (1996) The effects of long-term heparin therapy during pregnancy on bone density. A prospective matched cohort study. Thromb Haemost 75:254–257PubMedCrossRef
36.
37.
go back to reference Jia P, Wang R, Yuan J, Chen H, Bao L, Feng F, Tang H (2020) A case of pregnancy and lactation-associated osteoporosis and a review of the literature. Arch Osteoporos 15:94PubMedCrossRef Jia P, Wang R, Yuan J, Chen H, Bao L, Feng F, Tang H (2020) A case of pregnancy and lactation-associated osteoporosis and a review of the literature. Arch Osteoporos 15:94PubMedCrossRef
39.
go back to reference Smith R, Phillips AJ (1998) Osteoporosis during pregnancy and its management. Scand J Rheumatol Suppl 107:66–67PubMedCrossRef Smith R, Phillips AJ (1998) Osteoporosis during pregnancy and its management. Scand J Rheumatol Suppl 107:66–67PubMedCrossRef
40.
go back to reference Hong N, Kim JE, Lee SJ, Kim SH, Rhee Y (2018) Changes in bone mineral density and bone turnover markers during treatment with teriparatide in pregnancy- and lactation-associated osteoporosis. Clin Endocrinol (Oxf) 88:652–658PubMedCrossRef Hong N, Kim JE, Lee SJ, Kim SH, Rhee Y (2018) Changes in bone mineral density and bone turnover markers during treatment with teriparatide in pregnancy- and lactation-associated osteoporosis. Clin Endocrinol (Oxf) 88:652–658PubMedCrossRef
41.
go back to reference Gehlen M, Lazarescu AD, Hinz C, Schwarz-Eywill M, Pfeifer M, Balasingam S, Maier A (2019) Long-term outcome of patients with pregnancy and lactation-associated osteoporosis (PLO) with a particular focus on quality of life. Clin Rheumatol 38:3575–3583PubMedCrossRef Gehlen M, Lazarescu AD, Hinz C, Schwarz-Eywill M, Pfeifer M, Balasingam S, Maier A (2019) Long-term outcome of patients with pregnancy and lactation-associated osteoporosis (PLO) with a particular focus on quality of life. Clin Rheumatol 38:3575–3583PubMedCrossRef
42.
go back to reference Jun Jie Z, Ai G, Baojun W, Liang Z (2020) Intertrochanteric fracture in pregnancy- and lactation-associated osteoporosis. J Int Med Res 48:300060519858013PubMedCrossRef Jun Jie Z, Ai G, Baojun W, Liang Z (2020) Intertrochanteric fracture in pregnancy- and lactation-associated osteoporosis. J Int Med Res 48:300060519858013PubMedCrossRef
43.
go back to reference Cohen A, Kamanda-Kosseh M, Dempster DW et al (2019) Women with pregnancy and lactation-associated osteoporosis (PLO) have low bone remodeling rates at the tissue level. J Bone Miner Res 34:1552–1561PubMedCrossRef Cohen A, Kamanda-Kosseh M, Dempster DW et al (2019) Women with pregnancy and lactation-associated osteoporosis (PLO) have low bone remodeling rates at the tissue level. J Bone Miner Res 34:1552–1561PubMedCrossRef
44.
go back to reference Hardcastle SA, Yahya F, Bhalla AK (2019) Pregnancy-associated osteoporosis: a UK case series and literature review. Osteoporos Int 30:939–948PubMedCrossRef Hardcastle SA, Yahya F, Bhalla AK (2019) Pregnancy-associated osteoporosis: a UK case series and literature review. Osteoporos Int 30:939–948PubMedCrossRef
45.
go back to reference O’Sullivan SM, Grey AB, Singh R, Reid IR (2006) Bisphosphonates in pregnancy and lactation-associated osteoporosis. Osteoporos Int 17:1008–1012PubMedCrossRef O’Sullivan SM, Grey AB, Singh R, Reid IR (2006) Bisphosphonates in pregnancy and lactation-associated osteoporosis. Osteoporos Int 17:1008–1012PubMedCrossRef
46.
go back to reference Kurabayashi T, Nagai K, Morikawa K, Kamimura N, Yanase T, Hayashi K (2021) Prevalence of osteoporosis and osteopenia assessed by densitometry in Japanese puerperal women. J Obstet Gynaecol Res 47:1388–1396PubMedCrossRef Kurabayashi T, Nagai K, Morikawa K, Kamimura N, Yanase T, Hayashi K (2021) Prevalence of osteoporosis and osteopenia assessed by densitometry in Japanese puerperal women. J Obstet Gynaecol Res 47:1388–1396PubMedCrossRef
Metadata
Title
Bone metabolism and osteoporosis during pregnancy and lactation
Authors
Abraham Yair Lujano-Negrete
Martha Cecilia Rodríguez-Ruiz
Cassandra Michele Skinner-Taylor
Lorena Perez-Barbosa
Jesus Alberto Cardenas de la Garza
Pedro Alberto García-Hernández
Luis Gerardo Espinosa-Banuelos
Luz Fernanda Gutierrez-Leal
Sofia Jezzini-Martínez
Dionicio Ángel Galarza-Delgado
Publication date
01-12-2022
Publisher
Springer London
Published in
Archives of Osteoporosis / Issue 1/2022
Print ISSN: 1862-3522
Electronic ISSN: 1862-3514
DOI
https://doi.org/10.1007/s11657-022-01077-x

Other articles of this Issue 1/2022

Archives of Osteoporosis 1/2022 Go to the issue