Abstract
Hypercalcemia affects approximately 1% of the worldwide population. This electrolyte abnormality is frequent both in out and inpatients (varies from 0,17 to 5% in hospitalized, however incidence increases even up to 7,5% in emergency departments in some populations). Primary hyperparathyroidism (PHPT) and hypercalcemia of malignancy (HCM), account for more than 90 percent of all causes of hypercalcemia. Other causes of hypercalcemia, such as vitamin D intoxication, granulomatous disorders, milk-alkali syndrome, medications, familial hypocalciuric hypercalcemia and immobilization amount to less than 10% of all causes of hypercalcemia. However, once primary hyperparathyroidism or cancer has been excluded, other causes of hypercalcemia, often life-threatening and requiring appropriate causal management, should be considered. Considering rare etiologies is important, nevertheless, when primary hyperparathyroidism or malignancy do not account for the hypercalcemia. The review describes patophysiology, symptoms and diagnostic approach to the most relevant causes of hypercalcemia.
References
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3. Turesson I, Bjorkholm M, Blimark CH et al. Rapidly changing myeloma epidemiology in the general population: Increased incidence, older patients, and longer survival. European Journal of Haematology. 2018 Jun 25; 101(2): 237–244. DOI: 10.1111/ejh.13083
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6. Walker MD, Shane E. Hypercalcemia. JAMA. 2022 Oct 25; 328(16): 1624. DOI: 10.1001/jama.2022.18331
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10. Marcocci C, Cetani F. Hypercalcemia. Endocrinology and Metabolism Clinics of North America 2021 Dec 1; 50(4): 15–16. DOI: https://doi.org/10.1016/j.ecl.2021.07.011
11. El‐Hajj Fuleihan G, Chakhtoura M, Cipriani C, Eastell R, Karonova T, Liu J, et al. Classical and Nonclassical Manifestations of Primary Hyperparathyroidism. Journal of Bone and Mineral Research. 2022 Oct 17; 37(11): 2330–2350. DOI: 10.1002/jbmr.4679
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13. Bilezikian JP, Khan AA, Silverberg SJ et al. Evaluation and Management of Primary Hyperparathyroidism: Summary Statement and Guidelines from the Fifth International Workshop. Journal of Bone and Mineral Research. 2022 Oct 17; 37(11): 2293–2314.
DOI: 10.1002/jbmr.4677
14. Silverberg SJ. Primary hyperparathyroidism: Diagnosis, differential diagnosis, and evaluation. UpToDate. Apr 2023. https://www.uptodate.com/contents/primary-hyperparathyroidism-diagnosis-differential-diagnosis-and-evaluation (accessed May 5, 2023).
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16. Britto JM, Fenton AJ, Holloway WR, Nicholson GC. Osteoblasts mediate thyroid hormone stimulation of osteoclastic bone resorption. Endocrinology. 1994 Jan; 134(1): 169–176. DOI: 10.1210/endo.134.1.8275930
17. Kimura S, Nishimura Y, Yamaguchi K et al. A case of pheochromocytoma producing parathyroid hormone-related protein and presenting with hypercalcemia. The Journal of Clinical Endocrinology and Metabolism. 1990 Jun 1; 70(6): 1559–1563. DOI: 10.1210/jcem-70-6-1559
18. Diamond T, Thornley S. Addisonian crisis and hypercalcaemia. Australian and New Zealand Journal of Medicine. 1994 Jun; 24(3): 316. DOI: 10.1111/j.1445-5994.1994.tb02181.x
19. Vasikaran SD, Tallis GA, Braund WJ. Secondary hypoadrenalism presenting with hypercalcaemia. Clinical Endocrinology. 1994 Aug 1; 41(2): 261–264. DOI: 10.1111/j.1365-2265.1994.tb02540.x
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21. Mirrakhimov A. Hypercalcemia of malignancy: An update on pathogenesis and management. North American Journal of Medical Sciences. 2015; 7(11): 483. DOI: 10.4103/1947-2714.170600
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24. Martin TJ, Johnson RW. Multiple actions of parathyroid hormone‐related protein in breast cancer bone metastasis. British Journal of Pharmacology. 2019 Jul 2; 178(9): 1923–1935. DOI: https://doi.org/10.1111/bph.14709
25. Pearse RN, Sordillo EM, Yaccoby S et al. Multiple myeloma disrupts the TRANCE/ osteoprotegerin cytokine axis to trigger bone destruction and promote tumor progression. Proceedings of the National Academy of Sciences. 2001 Sep 18; 98(20): 11581–11586. DOI: 10.1073/pnas.201394498
26. Tian E, Zhan F, Walker RC, et al. The Role of the Wnt-Signaling Antagonist DKK1 in the Development of Osteolytic Lesions in Multiple Myeloma. The New England Journal of Medicine. 2003 Dec 25; 349(26): 2483–2494. DOI: 10.1056/NEJMoa030847
27. Maalouf N. Hypercalcemia in granulomatous diseases. UpToDate. April 2023. Available from: https://www.uptodate.com/contents/hypercalcemia-in-granulomatous-diseases (accessed on May 5, 2023)
28. Sandler LM, Winearls CG, Fraher LJ et al. Studies of the hypercalcaemia of sarcoidosis: effect of steroids and exogenous vitamin D3 on the circulating concentrations of 1,25-dihydroxy vitamin D3. The Quarterly Journal of Medicine. 1984; 53(210): 165–180
29. Adams JS. Effective Reduction in the Serum 1,25-Dihydroxyvitamin D and Calcium Concentration in Sarcoidosis-Associated Hypercalcemia with Short-Course Chloroquine Therapy. Annals of Internal Medicine. 1989 Sep 1; 111(5) :437. DOI: 10.7326/0003-4819-111-5-437
30. Adams JS, Sgarma OP, Diz MM et al. Ketoconazole Decreases the Serum 1,25-Dihydroxyvitamin D and Calcium Concentration in Sarcoidosis-Associated Hypercalcemia. The Journal of Clinical Endocrinology & Metabolism. 1990 Apr; 70(4): 1090–1095. DOI: 10.1210/jcem-70-4-1090
31. Holick MF, Binkley NC, Bischoff-Ferrari HA et al. Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. The Journal of clinical endocrinology and metabolism. 2011; 96(7): 1911–1930 DOI: 10.1210/jc.2011-0385
32. Płudowski P, Kos-Kudła B, Walczak M et al. Guidelines for Preventing and Treating Vitamin D Deficiency: A 2023 Update in Poland. Nutrients. 2023 Jan 1; 15(3): 695
33. Pettifor JM. Serum Levels of Free 1,25-Dihydroxyvitamin D in Vitamin D Toxicity. Annals of Internal Medicine. 1995 Apr 1; 122(7): 511. DOI: 10.7326/0003-4819-122-7-199504010-00006
34. Lowe H, Cusano NE, Binkley N et al. Vitamin D Toxicity due to a Commonly Available “Over the Counter” Remedy from the Dominican Republic. The Journal of Clinical Endocrinology & Metabolism. 2011 Feb 1; 96(2): 291–295. https://doi.org/10.1210/jc.2010-1999
35. Selby PL, Davies M, Marks JS et al. Vitamin D intoxication causes hypercalcaemia by increased bone resorption which responds to pamidronate. Clinical Endocrinology. 1995 Nov; 43(5): 531–536. DOI: 10.1111/j.1365-2265.1995.tb02916.x
36. Burman KD, Monchik JM, Earll JM et al. Ionized and total serum calcium and parathyroid hormone in hyperthyroidism. Annals of Internal Medicine. 1976 Jun 1; 84(6):668–671. DOI: 10.7326/0003-4819-84-6-668
37. Beall DP, Scofield HR. Milk-Alkali Syndrome Associated with Calcium Carbonate Consumption: Report of 7 Patients with Parathyroid Hormone Levels and an Estimate of Prevalence Among Patients Hospitalized with Hypercalcemia. Medicine. 1995 Mar; 74(2): 89–96. DOI: 10.1097/00005792-199503000-00004
38. Stubbs Jr. The milk-alkali syndrome. UpToDate. April 2023. Available from:
https://www.uptodate.com/contents/the-milk-alkali-syndrome (accessed on May 5, 2023)
39. Shane E. Etiology of hypercalcemia. UpToDate. April 2023. Available from: https://www.uptodate.com/contents/etiology-of-hypercalcemia (accessed on May 5, 2023)
40. Nordenström J, Strigård K, Perbeck L et al. Hyperparathyroidism associated with treatment of manic-depressive disorders by lithium. The European Journal of Surgery = Acta Chirurgica. 1992 Apr 1; 158(4): 207–211.
41. Tsai WC, Wang WJ, Chen WL et al. Surviving a Crisis of Immobilization Hypercalcemia. Journal of the American Geriatrics Society. 2012 Sep; 60(9): 1778–1780. DOI: 10.1111/j.1532-5415.2012.04129.x
42. Yeh MW, Ituarte PHG, Zhou HC et al. Incidence and Prevalence of Primary Hyperparathyroidism in a Racially Mixed Population. The Journal of Clinical Endocrinology and Metabolism. 2013 Mar 1; 98(3): 1122–1129. DOI: 10.1210/jc.2012-4022
43. Mariathasan S, Andrews KA, Thompson E, Challis BG, Wilcox S, Pierce H, et al. Genetic testing for hereditary hyperparathyroidism and familial hypocalciuric hypercalcaemia in a large UK cohort. Clinical Endocrinology. 2020 Jun 12;93(4):409–418. DOI: 10.1111/cen.14254
44. Strodel WE, Thompson NW, Eckhauser FE et al. Malignancy and concomitant primary hyperparathyroidism. Journal of Surgical Oncology. 1988 Jan 1; 37(1): 10–12. DOI: 10.1002/jso.2930370104
45. Misiorowski, W., Czajka-Oraniec, I., Kochman, M. et al. Osteitis fibrosa cystica—a forgotten radiological feature of primary hyperparathyroidism. 2017 Endocrine 58, 380–385. https://doi.org/10.1007/s12020-017-1414-2
2. American Cancer Society. How Common is Breast Cancer? 2021 Apr 6. Available from: https://www.cancer.org/cancer/breast-cancer/about/how-common-is-breast-cancer.html (accessed May 5, 2023)
3. Turesson I, Bjorkholm M, Blimark CH et al. Rapidly changing myeloma epidemiology in the general population: Increased incidence, older patients, and longer survival. European Journal of Haematology. 2018 Jun 25; 101(2): 237–244. DOI: 10.1111/ejh.13083
4. Goltzman D. Approach to Hypercalcemia. Endotext; 2023 Apr 16. Available from: https://www.endotext.org/chapter/approach-to-hypercalcemia/ (accessed May 5, 2023)
5. Lee CT, Yang CC, Lam KK et al. Hypercalcemia in the emergency department. The American Journal of the Medical Sciences. 2006 Mar 1; 331(3): 119–123. DOI: https://doi.org/10.1097/00000441-200603000-00002
6. Walker MD, Shane E. Hypercalcemia. JAMA. 2022 Oct 25; 328(16): 1624. DOI: 10.1001/jama.2022.18331
7. Tonon CR, Silva TAAL, Pereira FWL et al. A Review of Current Clinical Concepts in the Pathophysiology, Etiology, Diagnosis, and Management of Hypercalcemia. Medical Science Monitor: International Medical Journal of Experimental and Clinical Research. 2022 Feb 26;28:e935821. Available from: https://medscimonit.com/abstract/full/idArt/935821 (accessed May 5, 2023)
8. Stubbs Jr. Relation between total and ionized serum calcium concentrations. UpToDate. Apr 2023. Available from: https://www.uptodate.com/contents/relation-between-total-and-ionized-serum-calcium-concentrations (accessed May 5, 2023)
9. Arnold A. Primary hyperparathyroidism: Pathogenesis and etiology. UpToDate. Apr 2023. Available from: https://www.uptodate.com/contents/primary-hyperparathyroidism-pathogenesis-and-etiology (accessed May 5, 2023)
10. Marcocci C, Cetani F. Hypercalcemia. Endocrinology and Metabolism Clinics of North America 2021 Dec 1; 50(4): 15–16. DOI: https://doi.org/10.1016/j.ecl.2021.07.011
11. El‐Hajj Fuleihan G, Chakhtoura M, Cipriani C, Eastell R, Karonova T, Liu J, et al. Classical and Nonclassical Manifestations of Primary Hyperparathyroidism. Journal of Bone and Mineral Research. 2022 Oct 17; 37(11): 2330–2350. DOI: 10.1002/jbmr.4679
12. Marx SJ, Goltzman D. Evolution of Our Understanding of the Hyperparathyroid Syndromes: A Historical Perspective. Journal of bone and mineral research: the official journal of the American Society for Bone and Mineral Research. 2019 Jan 1; 34(1): 22–37. DOI: 10.1002/jbmr.3650
13. Bilezikian JP, Khan AA, Silverberg SJ et al. Evaluation and Management of Primary Hyperparathyroidism: Summary Statement and Guidelines from the Fifth International Workshop. Journal of Bone and Mineral Research. 2022 Oct 17; 37(11): 2293–2314.
DOI: 10.1002/jbmr.4677
14. Silverberg SJ. Primary hyperparathyroidism: Diagnosis, differential diagnosis, and evaluation. UpToDate. Apr 2023. https://www.uptodate.com/contents/primary-hyperparathyroidism-diagnosis-differential-diagnosis-and-evaluation (accessed May 5, 2023).
15. Burman KD, Monchik JM, Earll JM et al. Ionized and total serum calcium and parathyroid hormone in hyperthyroidism. Annals of Internal Medicine. 1976 Jun 1; 84(6): 668–671. DOI: 10.7326/0003-4819-84-6-668
16. Britto JM, Fenton AJ, Holloway WR, Nicholson GC. Osteoblasts mediate thyroid hormone stimulation of osteoclastic bone resorption. Endocrinology. 1994 Jan; 134(1): 169–176. DOI: 10.1210/endo.134.1.8275930
17. Kimura S, Nishimura Y, Yamaguchi K et al. A case of pheochromocytoma producing parathyroid hormone-related protein and presenting with hypercalcemia. The Journal of Clinical Endocrinology and Metabolism. 1990 Jun 1; 70(6): 1559–1563. DOI: 10.1210/jcem-70-6-1559
18. Diamond T, Thornley S. Addisonian crisis and hypercalcaemia. Australian and New Zealand Journal of Medicine. 1994 Jun; 24(3): 316. DOI: 10.1111/j.1445-5994.1994.tb02181.x
19. Vasikaran SD, Tallis GA, Braund WJ. Secondary hypoadrenalism presenting with hypercalcaemia. Clinical Endocrinology. 1994 Aug 1; 41(2): 261–264. DOI: 10.1111/j.1365-2265.1994.tb02540.x
20. Shane E. Diagnostic approach to hypercalcemia. UpToDate. April 2023. Available from: https://www.uptodate.com/contents/diagnostic-approach-to-hypercalcemia (accessed May 5, 2023)
21. Mirrakhimov A. Hypercalcemia of malignancy: An update on pathogenesis and management. North American Journal of Medical Sciences. 2015; 7(11): 483. DOI: 10.4103/1947-2714.170600
22. Horowitz MJ. Hypercalcemia of malignancy: Mechanisms. UpToDate. April 2023. Available from: https://www.uptodate.com/contents/hypercalcemia-of-malignancy-mechanisms (accessed on May 5, 2023)
23. Fuleihan GEH, Clines GA, Hu MI et al. Treatment of Hypercalcemia of Malignancy in Adults: An Endocrine Society Clinical Practice Guideline. The Journal of Clinical Endocrinology & Metabolism. 2022; Dec 21; 108(3): 507–528. DOI: 10.1210/clinem/dgac621
24. Martin TJ, Johnson RW. Multiple actions of parathyroid hormone‐related protein in breast cancer bone metastasis. British Journal of Pharmacology. 2019 Jul 2; 178(9): 1923–1935. DOI: https://doi.org/10.1111/bph.14709
25. Pearse RN, Sordillo EM, Yaccoby S et al. Multiple myeloma disrupts the TRANCE/ osteoprotegerin cytokine axis to trigger bone destruction and promote tumor progression. Proceedings of the National Academy of Sciences. 2001 Sep 18; 98(20): 11581–11586. DOI: 10.1073/pnas.201394498
26. Tian E, Zhan F, Walker RC, et al. The Role of the Wnt-Signaling Antagonist DKK1 in the Development of Osteolytic Lesions in Multiple Myeloma. The New England Journal of Medicine. 2003 Dec 25; 349(26): 2483–2494. DOI: 10.1056/NEJMoa030847
27. Maalouf N. Hypercalcemia in granulomatous diseases. UpToDate. April 2023. Available from: https://www.uptodate.com/contents/hypercalcemia-in-granulomatous-diseases (accessed on May 5, 2023)
28. Sandler LM, Winearls CG, Fraher LJ et al. Studies of the hypercalcaemia of sarcoidosis: effect of steroids and exogenous vitamin D3 on the circulating concentrations of 1,25-dihydroxy vitamin D3. The Quarterly Journal of Medicine. 1984; 53(210): 165–180
29. Adams JS. Effective Reduction in the Serum 1,25-Dihydroxyvitamin D and Calcium Concentration in Sarcoidosis-Associated Hypercalcemia with Short-Course Chloroquine Therapy. Annals of Internal Medicine. 1989 Sep 1; 111(5) :437. DOI: 10.7326/0003-4819-111-5-437
30. Adams JS, Sgarma OP, Diz MM et al. Ketoconazole Decreases the Serum 1,25-Dihydroxyvitamin D and Calcium Concentration in Sarcoidosis-Associated Hypercalcemia. The Journal of Clinical Endocrinology & Metabolism. 1990 Apr; 70(4): 1090–1095. DOI: 10.1210/jcem-70-4-1090
31. Holick MF, Binkley NC, Bischoff-Ferrari HA et al. Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. The Journal of clinical endocrinology and metabolism. 2011; 96(7): 1911–1930 DOI: 10.1210/jc.2011-0385
32. Płudowski P, Kos-Kudła B, Walczak M et al. Guidelines for Preventing and Treating Vitamin D Deficiency: A 2023 Update in Poland. Nutrients. 2023 Jan 1; 15(3): 695
33. Pettifor JM. Serum Levels of Free 1,25-Dihydroxyvitamin D in Vitamin D Toxicity. Annals of Internal Medicine. 1995 Apr 1; 122(7): 511. DOI: 10.7326/0003-4819-122-7-199504010-00006
34. Lowe H, Cusano NE, Binkley N et al. Vitamin D Toxicity due to a Commonly Available “Over the Counter” Remedy from the Dominican Republic. The Journal of Clinical Endocrinology & Metabolism. 2011 Feb 1; 96(2): 291–295. https://doi.org/10.1210/jc.2010-1999
35. Selby PL, Davies M, Marks JS et al. Vitamin D intoxication causes hypercalcaemia by increased bone resorption which responds to pamidronate. Clinical Endocrinology. 1995 Nov; 43(5): 531–536. DOI: 10.1111/j.1365-2265.1995.tb02916.x
36. Burman KD, Monchik JM, Earll JM et al. Ionized and total serum calcium and parathyroid hormone in hyperthyroidism. Annals of Internal Medicine. 1976 Jun 1; 84(6):668–671. DOI: 10.7326/0003-4819-84-6-668
37. Beall DP, Scofield HR. Milk-Alkali Syndrome Associated with Calcium Carbonate Consumption: Report of 7 Patients with Parathyroid Hormone Levels and an Estimate of Prevalence Among Patients Hospitalized with Hypercalcemia. Medicine. 1995 Mar; 74(2): 89–96. DOI: 10.1097/00005792-199503000-00004
38. Stubbs Jr. The milk-alkali syndrome. UpToDate. April 2023. Available from:
https://www.uptodate.com/contents/the-milk-alkali-syndrome (accessed on May 5, 2023)
39. Shane E. Etiology of hypercalcemia. UpToDate. April 2023. Available from: https://www.uptodate.com/contents/etiology-of-hypercalcemia (accessed on May 5, 2023)
40. Nordenström J, Strigård K, Perbeck L et al. Hyperparathyroidism associated with treatment of manic-depressive disorders by lithium. The European Journal of Surgery = Acta Chirurgica. 1992 Apr 1; 158(4): 207–211.
41. Tsai WC, Wang WJ, Chen WL et al. Surviving a Crisis of Immobilization Hypercalcemia. Journal of the American Geriatrics Society. 2012 Sep; 60(9): 1778–1780. DOI: 10.1111/j.1532-5415.2012.04129.x
42. Yeh MW, Ituarte PHG, Zhou HC et al. Incidence and Prevalence of Primary Hyperparathyroidism in a Racially Mixed Population. The Journal of Clinical Endocrinology and Metabolism. 2013 Mar 1; 98(3): 1122–1129. DOI: 10.1210/jc.2012-4022
43. Mariathasan S, Andrews KA, Thompson E, Challis BG, Wilcox S, Pierce H, et al. Genetic testing for hereditary hyperparathyroidism and familial hypocalciuric hypercalcaemia in a large UK cohort. Clinical Endocrinology. 2020 Jun 12;93(4):409–418. DOI: 10.1111/cen.14254
44. Strodel WE, Thompson NW, Eckhauser FE et al. Malignancy and concomitant primary hyperparathyroidism. Journal of Surgical Oncology. 1988 Jan 1; 37(1): 10–12. DOI: 10.1002/jso.2930370104
45. Misiorowski, W., Czajka-Oraniec, I., Kochman, M. et al. Osteitis fibrosa cystica—a forgotten radiological feature of primary hyperparathyroidism. 2017 Endocrine 58, 380–385. https://doi.org/10.1007/s12020-017-1414-2
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