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Clinical characteristics of pregnancy and lactation associated osteoporosis: An online survey study

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Abstract

Summary

Pregnancy and lactation associated osteoporosis is a rare and often severe osteoporosis presentation. Little information is available about etiology, clinical characteristics, risk factors and predictors of severity. Using an anonymized questionnaire, we defined clinical characteristics and potential risk factors for disease severity in PLO including primiparity, heparin exposure and celiac disease.

Purpose

Pregnancy and lactation associated osteoporosis (PLO) is a rare form of early-onset osteoporosis in which young women present with fractures, usually multiple vertebral fractures, during late pregnancy or lactation. Little information is available about etiology, clinical characteristics, risk factors and predictors of disease severity.

Methods

PLO patients were recruited to complete an anonymized online questionnaire. Disease severity was defined as total number of fractures during or after the first pregnancy associated with a fracture(s). Analyses related disease severity to potential predictors including diseases/conditions or medication exposures.

Results

177 completed surveys were received between 5/29/2018 and 1/12/2022. Average age at initial PLO fracture event was 32 ± 5 years. The majority were primiparous with singleton pregnancy and 79% fractured during lactation. Subjects reported 4.7 ± 2.7 total PLO fractures, with 48% reporting ≥ 5 fractures. Vertebral fractures, reported by 164/177 responders (93%), were the most common fracture type.

Conditions and medications most commonly reported included vitamin D deficiency, amenorrhea unrelated to pregnancy, nephrolithiasis, celiac disease (CD), oral steroid use, heparin products during pregnancy and progestin only contraceptive after pregnancy. CD and heparins exposure during pregnancy were significantly related to disease severity.

Conclusion

This is the largest study characterizing clinical features of PLO to date. The large number of participants and broad range of clinical and fracture characteristics queried has yielded novel information on the characteristics of PLO and potential risk factors for its severity, including primiparity, exposure to heparin and CD. These findings provide important preliminary data that can help target future mechanistic investigations.

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Data Availability

The data used to support the findings of the study are included within the article.

References

  1. Dunne F, Walters B, Marshall T, Heath DA (1993) Pregnancy associated osteoporosis. Clin Endocrinol (Oxf) 39:487–490

    Article  CAS  PubMed  Google Scholar 

  2. Hardcastle SA (2022) Pregnancy and Lactation Associated Osteoporosis. Calcif Tissue Int 110:531–545

    Article  CAS  PubMed  Google Scholar 

  3. Hardcastle SA, Yahya F, Bhalla AK (2019) Pregnancy-associated osteoporosis: a UK case series and literature review. Osteoporos Int 30:939–948

    Article  CAS  PubMed  Google Scholar 

  4. Kyvernitakis I, Reuter TC, Hellmeyer L, Hars O, Hadji P (2018) Subsequent fracture risk of women with pregnancy and lactation-associated osteoporosis after a median of 6 years of follow-up. Osteoporos Int 29:135–142

    Article  CAS  PubMed  Google Scholar 

  5. Laroche M, Talibart M, Cormier C, Roux C, Guggenbuhl P, Degboe Y (2017) Pregnancy-related fractures: a retrospective study of a French cohort of 52 patients and review of the literature. Osteoporos Int 28:3135–3142

    Article  CAS  PubMed  Google Scholar 

  6. Phillips AJ, Ostlere SJ, Smith R (2000) Pregnancy-associated osteoporosis: does the skeleton recover? Osteoporos Int 11:449–454

    Article  CAS  PubMed  Google Scholar 

  7. Hadji P, Boekhoff J, Hahn M, Hellmeyer L, Hars O, Kyvernitakis I (2017) Pregnancy-associated osteoporosis: a case-control study. Osteoporos Int 28:1393–1399

    Article  CAS  PubMed  Google Scholar 

  8. 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 

  9. Kovacs CS (2014) Osteoporosis presenting in pregnancy, puerperium, and lactation. Curr Opin Endocrinol Diabetes Obes 21:468–475

    Article  PubMed  Google Scholar 

  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 269:3130–3135

    Article  CAS  PubMed  Google Scholar 

  11. Hadji P, Boekhoff J, Hahn M, Hellmeyer L, Hars O, Kyvernitakis I (2017) Pregnancy-associated transient osteoporosis of the hip: results of a case-control study. Arch Osteoporos 12:11

    Article  PubMed  Google Scholar 

  12. Curtiss PH Jr, Kincaid WE (1959) Transitory demineralization of the hip in pregnancy. A report of three cases. J Bone Joint Surg Am 41-A:1327–1333

    Article  PubMed  Google Scholar 

  13. 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 

  14. Muir JM, Andrew M, Hirsh J, Weitz JI, Young E, Deschamps P, Shaughnessy SG (1996) Histomorphometric analysis of the effects of standard heparin on trabecular bone in vivo. Blood 88:1314–1320

    Article  CAS  PubMed  Google Scholar 

  15. Shaughnessy SG, Young E, Deschamps P, Hirsh J (1995) The effects of low molecular weight and standard heparin on calcium loss from fetal rat calvaria. Blood 86:1368–1373

    Article  CAS  PubMed  Google Scholar 

  16. Irie A, Takami M, Kubo H, Sekino-Suzuki N, Kasahara K, Sanai Y (2007) Heparin enhances osteoclastic bone resorption by inhibiting osteoprotegerin activity. Bone 41:165–174

    Article  CAS  PubMed  Google Scholar 

  17. Dahlman TC, Sjoberg HE, Ringertz H (1994) Bone mineral density during long-term prophylaxis with heparin in pregnancy. Am J Obstet Gynecol 170:1315–1320

    Article  CAS  PubMed  Google Scholar 

  18. Barbour LA, Kick SD, Steiner JF, LoVerde ME, Heddleston LN, Lear JL, Baron AE, Barton PL (1994) A prospective study of heparin-induced osteoporosis in pregnancy using bone densitometry. Am J Obstet Gynecol 170:862–869

    Article  CAS  PubMed  Google Scholar 

  19. 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 168:1265–1270

    Article  CAS  PubMed  Google Scholar 

  20. Backos M, Rai R, Thomas E, Murphy M, Dore C, Regan L (1999) Bone density changes in pregnant women treated with heparin: a prospective, longitudinal study. Hum Reprod 14:2876–2880

    Article  CAS  PubMed  Google Scholar 

  21. 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 19:1211–1214

    Article  CAS  PubMed  Google Scholar 

  22. Galambosi PJ, Kaaja RJ, Stefanovic V, Ulander VM (2012) Safety of low-molecular-weight heparin during pregnancy: a retrospective controlled cohort study. Eur J Obstet Gynecol Reprod Biol 163:154–159

    Article  CAS  PubMed  Google Scholar 

  23. 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 34:1552–1561

    Article  CAS  PubMed  Google Scholar 

  24. Fasano A, Catassi C (2012) Clinical practice. Celiac disease N Engl J Med 367:2419–2426

    Article  CAS  PubMed  Google Scholar 

  25. Bianchi ML, Bardella MT (2008) Bone in celiac disease. Osteoporos Int 19:1705–1716

    Article  PubMed  Google Scholar 

  26. Leffler DA, Green PH, Fasano A (2015) Extraintestinal manifestations of coeliac disease. Nat Rev Gastroenterol Hepatol 12:561–571

    Article  CAS  PubMed  Google Scholar 

  27. Heikkila K, Pearce J, Maki M, Kaukinen K (2015) Celiac disease and bone fractures: a systematic review and meta-analysis. J Clin Endocrinol Metab 100:25–34

    Article  CAS  PubMed  Google Scholar 

  28. Di Stefano M, Mengoli C, Bergonzi M, Corazza GR (2013) Bone mass and mineral metabolism alterations in adult celiac disease: pathophysiology and clinical approach. Nutrients 5:4786–4799

    Article  PubMed  PubMed Central  Google Scholar 

  29. Pazianas M, Butcher GP, Subhani JM, Finch PJ, Ang L, Collins C, Heaney RP, Zaidi M, Maxwell JD (2005) Calcium absorption and bone mineral density in celiacs after long term treatment with gluten-free diet and adequate calcium intake. Osteoporos Int 16:56–63

    Article  CAS  PubMed  Google Scholar 

  30. Fornari MC, Pedreira S, Niveloni S et al (1998) Pre- and post-treatment serum levels of cytokines IL-1beta, IL-6, and IL-1 receptor antagonist in celiac disease. Are they related to the associated osteopenia? Am J Gastroenterol 93:413–418

    Article  CAS  PubMed  Google Scholar 

  31. Bodnar LM, Simhan HN, Powers RW, Frank MP, Cooperstein E, Roberts JM (2007) High prevalence of vitamin D insufficiency in black and white pregnant women residing in the northern United States and their neonates. J Nutr 137:447–452

    Article  CAS  PubMed  Google Scholar 

  32. Jeyakumar A, Shinde V, Ravindran R (2021) Pooled estimate of vitamin D deficiency among pregnant women in India: a systematic review and meta-analysis. J Health Popul Nutr 40:28

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

These studies were supported by FDA RO1 FD006007 (AC), the Simon-Strauss Foundation and the Thomas L. Kempner, Jr. and Katheryn C. Patterson Foundation.

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Authors and Affiliations

  1. Division of Endocrinology, Department of Medicine, College of Physicians & Surgeons, Columbia University Irving Medical Center, 180 Fort Washington Avenue, #904 , New York, NY, 10032, USA

    Ananya V. Kondapalli, Mafo Kamanda-Kosseh, John M. Williams, Mariana Bucovsky, Ivelisse Colon, Elizabeth Shane & Adi Cohen

  2. Department of Biostatistics and Epidemiology, Rutgers School of Public Health, Piscataway, NJ, USA

    Stephanie Shiau

Authors
  1. Ananya V. Kondapalli
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  2. Mafo Kamanda-Kosseh
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Correspondence to Adi Cohen.

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The authors have nothing to disclose.

Conflict of Interest

The authors (Ananya V. Kondapalli, Mafo Kamanda-Kosseh, John M. Williams, Stephanie Shiau, Mariana Bucovsky, Ivelisse Colon, Elizabeth Shane, Adi Cohen) declare that they have no conflict of interest.

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Kondapalli, A.V., Kamanda-Kosseh, M., Williams, J.M. et al. Clinical characteristics of pregnancy and lactation associated osteoporosis: An online survey study. Osteoporos Int 34, 1477–1489 (2023). https://doi.org/10.1007/s00198-023-06793-9

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  • DOI: https://doi.org/10.1007/s00198-023-06793-9

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