Secondary hyperparathyroidism: Benign bystander or culpable contributor to adverse health outcomes?

Southern Medical Journal

Volumn 105, Issue 1, 2012, Pages 36-42

  Peiris, Alan N ^a,b   Youssef, Dima ^a,b   Grant, William B ^a,b  

^a East Tennessee State University   (United States)

^b Sunlight   (United States)

Author keywords

25(OH) vitamin D; cardiovascular disease; mortality; parathyroid hormone; renal disease; secondary hyperparathyroidism

Indexed keywords

25 HYDROXYVITAMIN D; PARATHYROID HORMONE;

BLOOD VESSEL CALCIFICATION; CALCIFICATION; CARDIOVASCULAR DISEASE; CORONARY RISK; DISEASE ASSOCIATION; DISEASE EXACERBATION; HEART FAILURE; HORMONE ACTION; HUMAN; KIDNEY FAILURE; MORTALITY; NORADRENALIN RELEASE; OUTCOME ASSESSMENT; PARATHYROID HORMONE BLOOD LEVEL; PATHOGENESIS; PROGNOSIS; RACE DIFFERENCE; REVIEW; SECONDARY HYPERPARATHYROIDISM; VALVULAR CALCIFICATION; VITAMIN BLOOD LEVEL; VITAMIN D DEFICIENCY;

EID: 84855161864     PISSN: 00384348     EISSN: 15418243     Source Type: Journal    
DOI: 10.1097/SMJ.0b013e31823c4155     Document Type: Review

References (94)

1. Shimoyama M, Ogino K, Furuse Y, et al. Signaling pathway and chron-otropic action of parathyroid hormone in isolated perfused rat heart. J Cardiovasc Pharmacol 2001;38:491-499. (Pubitemid 32868220)
2. Crass MF 3rd, Moore PL, Strickland ML, et al. Cardiovascular responses to parathyroid hormone. Am J Physiol 1985;249(2 Pt 1):E187-E194. (Pubitemid 15008828)
3. Sambrook PN, Chen JS, March LM, et al. Serum parathyroid hormone is associated with increased mortality independent of 25-hydroxy vitamin d status, bone mass, and renal function in the frail and very old: a cohort study. JClin Endocrinol Metab 2004;89:5477-5481. (Pubitemid 39518428)
4. Nilsson IL, Wadsten C, Brandt L, et al. Mortality in sporadic primary hyperparathyroidism: nationwide cohort study of multiple parathyroid gland disease. Surgery 2004;136:981-987. (Pubitemid 39452296)
5. Tanaka M, Tokunaga K, Maruyama T, et al. Parathyroidectomy markedly reduces oxidative stress in a patient with primary hyperparathyroidism. TherApherDial 2011;15(1 suppl):38-41.
6. Vestergaard H, Østergaard Kristensen L. Normocalcemia and persistent elevated serum concentrations of 1-84 parathyroid hormone after operation for sporadic parathyroid adenoma: evidence of increased morbidity from cardiovascular disease. World J Surg 2002;26:657-660. (Pubitemid 36920338)
7. Bjorkman M, Sorva A, Tilvis R. Parathyroid hormone as a mortality predictor in frail aged inpatients. Gerontology 2009;55:601-606.
8. Carlstedt F, Lind L, Wide L, et al. Serum levels of parathyroid hormone are related to the mortality and severity of illness in patients in the emergency department. Eur J Clin Invest 1997;27:977-981. (Pubitemid 28012617)
9. Fisher A, Goh S, Srikusalanukul W, et al. Elevated serum PTH is independently associated with poor outcomes in older patients with hip fracture and vitamin D inadequacy. Calcif Tissue Int 2009;85:301-309.
10. Cawthon PM, Parimi N, Barrett-Connor E, et al. Serum 25-hydroxyvitamin D, parathyroid hormone, and mortality in older men. J Clin Endocrinol Metab 2010;95:4625-4634.
11. Bozic B, Loncar G, Prodanovic N, et al. Parathyroid hormone response to vitamin D insufficiency in elderly males with chronic heart failure. PhysiolRes 2011;60:S155-S163.
12. Chen JS, Sambrook PN, March L, et al. Hypovitaminosis D and parathyroid hormone response in the elderly: effects on bone turnover and mortality. Clin Endocrinol (Oxf) 2008;68:290-298.
13. Covic A, Kothawala P, Bernal M, et al. Systematic review of the evidence underlying the association between mineral metabolism disturbances and risk of all-cause mortality, cardiovascular mortality and cardiovascular events in chronic kidney disease. Nephrol Dial Transplant 2009;24:1506-1523.
14. Ganesh SK, Stack AG, Levin NW, et al. Association of elevated serum PO(4), Ca x PO(4) product, and parathyroid hormone with cardiac mortality risk in chronic hemodialysis patients. J Am Soc Nephrol 2001;12: 2131-2138. (Pubitemid 32880350)
15. Linhartová K, Veselka J, Sterbáková G, et al. Parathyroid hormone and vitamin D levels are independently associated with calcific aortic stenosis. Circ J2008;72:245-250.
16. Schmitz F, Ewering S, Zerres K, et al. Parathyroid hormone gene variant and calcific aortic stenosis. J Heart Valve Dis 2009;18:262-267.
17. Neves KR, Graciolli FG, dos Reis LM, et al. Vascular calcification: contribution of parathyroid hormone in renal failure. Kidney Int 2007;71: 1262-1270. (Pubitemid 46884255)
18. Akmal M, Barndt RR, Ansari AN, et al. Excess PTH in CRF induces pulmonary calcification, pulmonary hypertension and right ventricular hypertrophy. Kidney Int 1995;47:158-163.
19. Amin M, Fawzy A, Hamid MA, et al. Pulmonary hypertension in patients with chronic renal failure: role of parathyroid hormone and pulmonary artery calcifications. Chest 2003;124:2093-2097. (Pubitemid 38010574)
20. Coen G, Ballanti P, Mantella D, et al. Bone turnover, osteopenia and vascular calcifications in hemodialysis patients. A histomorphometric and multislice CT study. Am J Nephrol 2009;29:145-152.
21. Goldsmith DJ, Covic A, Sambrook PA, et al. Vascular calcification in long-term haemodialysis patients in a single unit: a retrospective analysis. Nephron 1997;77:37-43. (Pubitemid 27395339)
22. Zouboulis CC, Blume-Peytavi U, Lennert T, et al. Fulminant metastatic calcinosis with cutaneous necrosis in a child with end-stage renal disease and tertiary hyperparathyroidism. Br J Dermatol 1996;135:617-622. (Pubitemid 26340279)
23. 3. Nephrol Dial Transplant 2003;18:1770-1776. (Pubitemid 37098547)
24. Cozzolino M, Ronco C. The impact of paricalcitol on left ventricular hypertrophy. Contrib Nephrol 2011;171:161-165.
25. Wei M, Esbaei K, Bargman JM, et al. Inverse correlation between serum magnesium and parathyroid hormone in peritoneal dialysis patients: a contributing factor to adynamic bone disease? Int Urol Nephrol 2006;38: 317-322. (Pubitemid 44138160)
26. Cheng SL, Shao JS, Halstead LR, et al. Activation of vascular smooth muscle parathyroid hormone receptor inhibits Wnt/beta-catenin signaling and aortic fibrosis in diabetic arteriosclerosis. Circ Res 2010;107:271-282.
27. Hörl WH. The clinical consequences of secondary hyperparathyroidism: focus on clinical outcomes. Nephrol Dial Transplant 2004;19(5 suppl): V2-V8. (Pubitemid 39214193)
28. Potthoff SA, Janus A, Hoch H, et al. PTH-receptors regulate norepi-nephrine release in human heart and kidney. Regul Pept 2011;171:35-42.
29. Bhuriya R, Li S, Chen SC, et al. Plasma parathyroid hormone level and prevalent cardiovascular disease in CKD stages 3 and 4: an analysis from the Kidney Early Evaluation Program (KEEP). Am J Kidney Dis 2009; 53(4 suppl 4):S3-S10.
30. Lishmanov A, Dorairajan S, Pak Y, et al. Elevated serum parathyroid hormone is a cardiovascular risk factor in moderate chronic kidney disease. Int Urol Nephrol 2011;Feb 15 Epub ahead of print.
31. Zitt E, Kirsch AH, Haueis M, et al. The PTH (1-84)/non-PTH (1-84) ratio is a risk factor for cardiovascular events in hemodialysis patients. Clin Nephrol 2011;75:309-318.
32. Avram MM, Mittman N, Myint MM, et al. Importance of low serum intact parathyroid hormone as a predictor of mortality in hemodialysis and peritoneal dialysis patients: 14 years of prospective observation. Am J Kidney Dis 2001;38:1351-1357. (Pubitemid 34193126)
33. Dimkovic NB, Bargman J, Vas S, et al. Normal or low initial PTH levels are not a predictor of morbidity/mortality in patients undergoing chronic peritoneal dialysis. Perit Dial Int 2002;22:204-210. (Pubitemid 34546332)
34. Drechsler C, Krane V, Grootendorst DC, et al. The association between parathyroid hormone and mortality in dialysis patients is modified by wasting. Nephrol Dial Transplant 2009;24:3151-3157.
35. Drechsler C, Grootendorst DC, Boeschoten EW, et al. Changes in parathyroid hormone, body mass index and the association with mortality in dialysis patients. Nephrol Dial Transplant 2011;26:1340-1346.
36. New N, Mohandas J, John GT, et al. Calcific uremic arteriolopathy in peritoneal dialysis populations. Int J Nephrol 2011;2011:982854.
37. Agapitou V, Dimopoulos S, Mpouchla A, et al. Serum intact parathyroid hormone levels independently predict exercise capacity in stable heart failure patients. Int J Cardiol 2011;146:462-464.
38. Schierbeck LL, Jensen TS, Bang U, et al. Parathyroid hormone and vitamin DVmarkers for cardiovascular and all cause mortality in heart failure. Eur J Heart Fail 2011;13:626-632.
39. Sugimoto T, Tanigawa T, Onishi K, et al. Serum intact parathyroid hormone levels predict hospitalisation for heart failure. Heart 2009;95: 395-398.
40. Hagström E, Ingelsson E, Sundström J, et al. Plasma parathyroid hormone and risk of congestive heart failure in the community. Eur J Heart Fail 2010;12:1186-1192.
41. Nasri H, Baradaran A. Close association between parathyroid hormone and left ventricular function and structure in end-stage renal failure patients under maintenance hemodialysis. Bratisl Lek Listy 2004;105: 368-373.
42. Rostand SG, Drüeke TB. Parathyroid hormone, vitamin D, and cardiovascular disease in chronic renal failure. Kidney Int 1999;56:383-392. (Pubitemid 29353135)
43. Schlüter KD, Piper HM. Cardiovascular actions of parathyroid hormone and parathyroid hormone-related peptide. Cardiovasc Res 1998; 37:34-41. (Pubitemid 28122613)
44. Ballen KK, Shpall EJ, Avigan D, et al. Phase I trial of parathyroid hormone to facilitate stem cell mobilization. Biol Blood Marrow Transplant 2007;13:838-843. (Pubitemid 46902439)
45. Huber BC, Fischer R, Brunner S, et al. Comparison of parathyroid hormone and G-CSF treatment after myocardial infarction on perfu-sion and stem cell homing. Am J Physiol Heart Circ Physiol 2010;298: H1466-H1471.
46. Pagliarulo C, Salvatore P, Napoli C. Targeting vascular niche by parathyroid hormone. Curr Med Chem 2008;15:2984-2990.
47. Huber BC, Brunner S, Segeth A, et al. Parathyroid hormone is a DPP-IV inhibitor and increases SDF-1Ydriven homing of CXCR4(+) stem cells into the ischaemic heart. Cardiovasc Res 2011;90:529-537.
48. Loncar G, Bozic B, Cvorovic V, et al. Relationship between RANKL and neuroendocrine activation in elderly males with heart failure. Endocrine 2010;37:148-156.
49. Kamycheva E, Sundsfjord J, Jorde R. Serum parathyroid hormone levels predict coronary heart disease: the TromsL Study. Eur J Cardiovasc Prev Rehabil 2004;11:69-74. (Pubitemid 38388927)
50. Schillaci G, Pucci G, Pirro M, et al. Large-artery stiffness: a reversible marker of cardiovascular risk in primary hyperparathyroidism. Atherosclerosis 2011;218:96-101.
51. Marini C, Giusti M, Armonino R, et al. Reduced coronary flow reserve in patients with primary hyperparathyroidism: a study by G-SPECT myocardial perfusion imaging. Eur J Nucl Med Mol Imaging 2010;37: 2256-2263.
52. Grandi NC, Breitling LP, Hahmann H, et al. Serum parathyroid hormone and risk of adverse outcomes in patients with stable coronary heart disease. Heart 2011;97:1215-1221.
53. Fisher AA, Southcott EK, Srikusalanukul W, et al. Relationships between myocardial injury, all-cause mortality, vitamin D, PTH, and biochemical bone turnover markers in older patients with hip fractures. Ann Clin Lab Sci 2007;37:222-232. (Pubitemid 47311338)
54. Anderson JL, Vanwoerkom RC, Horne BD, et al. Parathyroid hormone, vitamin D, renal dysfunction, and cardiovascular disease: dependent or independent risk factors? Am Heart J 2011;162:331.e2-339.e2.
55. Pilz S, Tomaschitz A, Drechsler C, et al. Parathyroid hormone level is associated with mortality and cardiovascular events in patients undergoing coronary angiography. Eur Heart J 2010;31:1591-1598.
56. Cunningham J, Danese M, Olson K, et al. Effects of the calcimimetic cinacalcet HCl on cardiovascular disease, fracture, and health-related quality of life in secondary hyperparathyroidism. Kidney Int 2005;68: 1793-1800. (Pubitemid 43169924)
57. Hjelmesaeth J, HofsL D, Aasheim ET, et al. Parathyroid hormone, but not vitamin D, is associated with the metabolic syndrome in morbidly obese women and men: a cross-sectional study. Cardiovasc Diabetol 2009;8:7.
58. RLislien J, Van Calster B, Hjelmesth J. Parathyroid hormone is a plausible mediator for the metabolic syndrome in the morbidly obese: a cross-sectional study. Cardiovasc Diabetol 2011;10:17.
59. Snijder MB, Lips P, Seidell JC, et al. Vitamin D status and parathyroid hormone levels in relation to blood pressure: a population-based study in older men and women. J Intern Med 2007;261:558-565. (Pubitemid 46835978)
60. Szulc P, Claustrat B, Delmas PD. Serum concentrations of 17beta-E2 and 25-hydroxycholecalciferol (25OHD) in relation to all-cause mortality in older menVthe MINOS study. Clin Endocrinol (Oxf) 2009;71:594-602.
61. Williams DM, Fraser A, Lawlor DA. Associations of vitamin D, parathyroid hormone and calcium with cardiovascular risk factors in US adolescents. Heart 2011;97:315-320.
62. Arad Y, Spadaro LA, Roth M, et al. Serum concentration of calcium, 1,25 vitamin D and parathyroid hormone are not correlated with coronary calcifications. An electron beam computed tomography study. Coron Artery Dis 1998;9:513-518. (Pubitemid 28517595)
63. Taylor EN, Rimm EB, Stampfer MJ, et al. Plasma fibroblast growth factor 23, parathyroid hormone, phosphorus, and risk of coronary heart disease. Am Heart J 2011;161:956-962.
64. Jiang B, Morimoto S, Yang J, et al. Expression of parathyroid hormone/parathyroid hormone-related protein receptor in vascular endothelial cells. J Cardiovasc Pharmacol 1998;31:S142-S144.
65. Perkovic V, Hunt D, Griffin SV, et al. Accelerated progression of calcific aortic stenosis in dialysis patients. Nephron Clin Pract 2003;94:c40-c45.
66. Fritsch S, Lindner V, Welsch S, et al. Intravenous delivery of PTH/PTHrP type 1 receptor cDNA to rats decreases heart rate, blood pressure, renal tone, renin angiotensin system, and stress-induced cardiovascular responses. J Am Soc Nephrol 2004;15:2588-2600. (Pubitemid 41103365)
67. Barlet JP, Coxam V, Davicco MJ. Relation between the parathyroid glands and arterial pressure: is there a parathyroid hypertensive factor? Presse Med 1995;24:1703-1706.
68. Fardella C, Rodriguez-Portales JA. Intracellular calcium and blood pressure: comparison between primary hyperparathyroidism and essential hypertension. J Endocrinol Invest 1995;18:827-832. (Pubitemid 26064018)
69. Barletta G, De Feo ML, Del Bene R, et al. Cardiovascular effects of parathyroid hormone: a study in healthy subjects and normotensive patients with mild primary hyperparathyroidism. J Clin Endocrinol Metab 2000;85:1815-1821. (Pubitemid 32269282)
70. Nyby MD, Hino T, Berger ME, et al. Desensitization of vascular tissue to parathyroid hormone and parathyroid hormoneYrelated protein. Endocrinology 1995;136:2497-2504.
71. Iseki K. Parathyroid hormone and the vascular response to norepineph-rine. Am J Hypertens 1990;3:238SY240S.
72. Smajilovic S, Schaal-Jensen R, Jabbari R, et al. Effect of intermittent versus continuous parathyroid hormone in the cardiovascular system of rats. Open Cardiovasc Med J 2010;4:110-116.
73. Perkovic V, Hewitson TD, Kelynack KJ, et al. Parathyroid hormone has a prosclerotic effect on vascular smooth muscle cells. Kidney Blood Press Res 2003;26:27-33. (Pubitemid 36438798)
74. 3-1alpha-hydroxylase is expressed in human vascular smooth muscle cells and is upregulated by parathyroid hormone and estrogenic compounds. Circulation 2005;111:1666-1671. (Pubitemid 40525167)
75. Rashid G, Bernheim J, Green J, et al. Parathyroid hormone stimulates the endothelial expression of vascular endothelial growth factor. Eur J Clin Invest 2008;38:798-803.
76. Coen G, Mantella D, Sardella D, et al. Asymmetric dimethylarginine, vascular calcifications and parathyroid hormone serum levels in hemo-dialysis patients. J Nephrol 2009;22:616-622.
77. Goodman WG. Medical management of secondary hyperparathyroidism in chronic renal failure. Nephrol Dial Transplant 2003;18:iii2Yiii8.
78. Akmal M, Kasim SE, Soliman AR, et al. Excess parathyroid hormone adversely affects lipid metabolism in chronic renal failure. Kidney Int 1990;37:854-858. (Pubitemid 20089216)
79. Akmal M, Massry SG, Goldstein DA, et al. Role of parathyroid hormone in the glucose intolerance of chronic renal failure. J Clin Invest 1985;75:1037-1044. (Pubitemid 15115274)
80. Alvarez JA, Ashraf AP, Hunter GR, et al. Serum 25-hydroxyvitamin D and parathyroid hormone are independent determinants of whole-body insulin sensitivity in women and may contribute to lower insulin sensitivity in African Americans. Am J Clin Nutr 2010;92:1344-1349.
81. Fraser A, Williams D, Lawlor DA. Associations of serum 25-hydroxyvitamin D, parathyroid hormone and calcium with cardiovascular risk factors: analysis of 3 NHANES cycles (2001-2006). PLoS One 2010; 5:e13882.
82. Boudville NC, Hodsman AB. Renal function and 25-hydroxyvitamin D concentrations predict parathyroid hormone levels in renal transplant patients. Nephrol Dial Transplant 2006;21:2621-2624. (Pubitemid 44644541)
83. Melamed ML, Eustace JA, Plantinga LC, et al. Third-generation parathyroid hormone assays and all-cause mortality in incident dialysis patients: the CHOICE study. Nephrol Dial Transplant 2008;23:1650-1658. (Pubitemid 351767752)
84. D'Amour P. Circulating PTH molecular forms: what we know and what we don't. Kidney Int Suppl 2006;102:S29-S33.
85. Sebastian EM, Suva LJ, Friedman PA. Differential effects of intermittent PTH(1-34) and PTH(7-34) on bone microarchitecture and aortic calcification in experimental renal failure. Bone 2008;43:1022-1030.
86. Shao JS, Cheng SL, Charlton-Kachigian N, et al. Teriparatide (human parathyroid hormone (1-34)) inhibits osteogenic vascular calcification in diabetic low density lipoprotein receptor-deficient mice. J Biol Chem 2003;278:50195-50202. (Pubitemid 37548859)
87. Vieth R, Ladak Y, Walfish PG. Age-related changes in the 25-hydroxyvitamin D versus parathyroid hormone relationship suggest a different reason why older adults require more vitamin D. J Clin Endo-crinol Metab 2003;88:185-191. (Pubitemid 36115163)
88. Stein MS, Wark JD, Scherer SC, et al. Falls relate to vitamin D and parathyroid hormone in an Australian nursing home and hostel. J Am Geriatr Soc 1999;47:1195-1201. (Pubitemid 29473291)
89. Adami S, Viapiana O, Gatti D, et al. Relationship between serum parathyroid hormone, vitamin D sufficiency, age, and calcium intake. Bone 2008;42:267-270.
90. Soilu-Hänninen M, Laaksonen M, Laitinen I, et al. A longitudinal study of serum 25-hydroxyvitamin D and intact parathyroid hormone levels indicate the importance of vitamin D and calcium homeostasis regulation in multiple sclerosis. J Neurol Neurosurg Psychiatry 2008;79: 152-157. (Pubitemid 351236545)
91. Aloia JF, Chen DG, Chen H. The 25(OH)D/PTH threshold in black women. J Clin Endocrinol Metab 2010;95:5069-5073.
92. Grant WB, Peiris AN. Possible role of serum 25-hydroxyvitamin D in BlackYWhite health disparities in the United States. J Am Med Dir Assoc 2010;11:617-628.
93. Robien K, Cutler GJ, Lazovich D. Vitamin D intake and breast cancer risk in postmenopausal women: the Iowa Women's Health Study. Cancer Causes Control 2007;18:775-782. (Pubitemid 46988245)
94. Lim U, Freedman DM, Hollis BW, et al. A prospective investigation of serum 25-hydroxyvitamin D and risk of lymphoid cancers. Int J Cancer 2009;124:979-986.