Role of distal diabetic polyneuropathy in the development of media calcification in patients with diabetesmellitus
Abstract
Arterial media calcification is a common finding in diabetes mellitus (DM) and is associated with distal symmetric neuropathy. Arterialcalcification also emerges as a complication of chronic kidney disease and is considered to be a risk factor for cardiovascular andgeneral morbidity. "Calcification" is actually not an accurate term, because morphologic alterations also include bone tissue formationor "ossification". Both processes are complex and exist in tight connection with bone homeostasis. Connection between distal symmetricneuropathy and arterial calcification suggests that neuropathy may be an independent risk factor for cardiovascular morbidity.
About the Authors
Natalya Alexandrovna Molitvoslovova
Endocrinology Research Centre, Moscow
Gagik Radikovich Galstyan
Endocrinology Research Centre, Moscow
References
1. Mönckeberg JG. Uber die reine Mediaverkalkung der Exrtremitätenarterien und ihr Verhalten zur Arteriosklerose. Virchows Arch. (Pathol. Anat.). 1903; (171):141-167.
2. Everhart JE, Pettit DJ, Knowler WC, Rose FA, Bennett PH. Medial artery calcification and its association with mortality and complications of diabetes. Diabetologia. 1988 Jan;31(1):16-23.
3. Lehto S, Niskanen L, Suhonen M, Rönnemaa T, Laakso M. Medial artery calcification: a neglected harbinger of cardiovascular complications in non-insulin dependent diabetes mellitus. Arterioscler Thromb Vasc Biol. 1996 Aug;16(8):978-983.
4. Proudfoot D, Shanahan CM. Biology of calcification in vascular cells: intima versus media. Herz. 2001 Jun;26(4):245-251.
5. Virchow R. Cellular pathology as based upon physiological and pathological histology. New York: Dover; 1863.
6. Vattikuti R, Towler DA. Osteogenic regulation of vascular calcification: an early perspective. Am J Physiol Endocrinol Metab. 2004 May;286(5):E686-696.
7. Neven E, Dauwe S, De Broe ME, D'Hause PC, Persy V. Endochondral bone formation is involved in media calcification in rats and in men. Kidney Int. 2007 Sep;72(5):574-581. Epub 2007 May 30.
8. Collin-Osdoby P. Regulation of vascular calcification by osteoclast regulatory factors RANKL and osteoprotegerin. Circ Res. 2004 Nov 26;95(11):1046-1057.
9. Abedin M, Tintut Y, Demer LL. Vascular calcification: mechanisms and clinical ramifications. Arterioscler Thromb Vasc Biol. 2004 Jul;24(7):1161-1170. Epub 2004 May 20.
10. Giachelli CM, Speer MY, Li X, Rajachar RM, Yang H. Regulation of vascular calcification: roles of phosphate and osteopontin. Circ Res. 2005 Apr 15;96(7):717-722.
11. Hofbauer LC, Brueck CC, Sanahan CM, Schoppet M, Dobnig H. Vascular calcification and osteoporosis-from clinical observation towards molecular understanding. Osteoporos Int. 2007 Mar;18(3):251-259. Epub 2006 Dec 7.
12. Moe SM, Chen NX. Pathophysiology of vascular calcification in chronic kidney disease. Circ Res. 2004 Sep 17;95(6):560-567.
13. Abedin M, Tintut Y, Demer LL. Mesenchymal stem cells and the artery wall. Circ Res. 2004 Oct 1;95(7):671-676.
14. Boström K, Watson KE, Horn S, Wortham C, Hennan IM, Demer LL. Bone morphogenetic protein expression in human atherosclerotic lesions. J Clin Invest. 1993 Apr;91(4):1800-1809.
15. Shao JS, Cai J, Towler DJ. Molecular mechanisms of vascular calcification: lessons learned from the aorta. Arterioscler Thromb Vasc Biol. 2006 Jul;26(7):1423-1430. Epub 2006 Apr 6.
16. Tyson KL, Reynolds JL, McNair R, Zhang Q, Weissberg PL, Shanahan CM. Osteochondrocytic transcription factors and their target genes exhibit distinct patterns of expression in human arterial calcification. Arterioscler Thromb Vasc Biol. 2003 Mar 1;23(3):489-494. Epub 2003 Jan 30.
17. Pavelock KA, Girard BM, Schutz KC, Braas KM, May V. Bone morphogenetic protein down-regulation of neuronal pituitary adenylate cyclase-activating polypeptide and reciprocal effects on vasoactive intestinal peptide expression. J Neurochem. 2007 Feb;100(3):603-616. Epub 2006 Dec 1.
18. Anderson HC. Molecular biology of matrix vesicles. cClin Orthop Relat Res. 1995 May;(314):266-268.
19. Clarke MC, Littlewood TD, Figg N, Maguire JJ, Davenport AP, Goddard M. Chronic apoptosis of vascular smooth muscle cells accelerates atherosclerosis and promotes calcification and medial degeneration. Circ Res. 2008 Jun 20;102(12):1529- 1538. Epub 2008 May 22.
20. Sims TJ, Rasmussen LM, Oxlund H, Bailey AJ. The role of glycation cross-links in diabetic vascular stiffening. Diabetologia. 1996 Aug;39(8):946-951.
21. Greenwald SE. Ageing of the conduit arteries. J Pathol. 2007 Jan;211(2):157-172.
22. Simionescu A, Simionescu DT, Vyavahare NR. Osteogenic responses in fibroblasts activated by elastin degradation products and transforming growth factor-1. Am J Pathol. 2007 Jul;171(1):116-123.
23. Li X, Hsueh-Ying Y, Giachelli CM. Role of the sodiumdependent cotransporter, Pit-1, in vascular smooth muscle cell calcification. Circ Res. 2006 Apr 14;98(7):905-912. Epub 2006 Mar 9.
24. Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes. 2005 Jun;54(6):1615-1625.
25. Olesen P, Ledet T, Rasmussen LM. Arterial osteoprotegerin: increased amounts in diabetes and modifiable synthesis from vascular smooth muscle cells by insulin and TNF-alpha. Diabetologia. 2005 Mar;48(3):561-568. Epub 2005 Feb 8.
26. Wang CC, Sorribas V, Sharma G, Levi M, Draznin B. Insulin attenuates vascular smooth muscle calcification but increases vascular smooth muscle cell phosphate transport. Atherosclerosis. 2007 Nov;195(1):e65-75. Epub 2007 Apr 6.
27. Hofbauer LC, Schoppet M. Osteoprotegerin: a link between osteoporosis and arterial calcification? Lancet. 2001 Jul 28;358(9278):257-259.
28. Rogers A, Eastell R. Circulating osteoprotegerin and receptor activator for nuclear factor kappaB ligand: clinical utility in metabolic bone disease assessment. J Clin Endocrinol Metab. 2005 Nov;90(11):6323-6331. Epub 2005 Aug 16.
29. Bucay N, Sarosi I, Dunstan CR, Morony S, Tarpley J, Capparelli C, Scully S, Tan HL, Xu W, Lacey DL, Boyle WJ, Simonet WS. Osteoprotegerindeficient mice develop early onset osteoporosis and arterial calcification. Genes Dev. 1998 May 1;12(9):1260-1268.
30. Panizo S, Cardus A, Encinas M, Parisi E, Valcheva P, López- Ongil S, Coll B, Fernandez E, Valdivielso JM. RANKL increases vascular smooth muscle cell calcification through a RANK-BMP4- dependent pathway. Circ Res. 2009 May 8;104(9):1041-1048. Epub 2009 Mar 26a
31. Browner WS, Lui L-Y, Cummings SR. Associations of serum osteoprotegerin levels with diabetes, stroke, bone density, fractures and mortality in elderly women. J Clin Endocrinol Metab. 2001 Feb;86(2):631-637.
32. Schoppett M, Sattler AM, Schaefer JR, Herzum M, Maisch B, Hofbauer LC. Increased osteoprotegerin serum levels in men with coronary artery disease. J Clin Endocrinol Metab. 2003 Mar;88(3):1024-1028.
33. Avignon A, Sultan A, Piot C, Elaerts S, Cristol JP, Dupuy AM. Osteoprotegerin is associated with silent coronary artery disease in high-risk but asymptomatic type 2 diabetic patients. Diabetes Care. 2005 Sep;28(9):2176-2180.
34. Rasmussen LM, Tarnow L, Hansen TK, Parving HH, Flyvbjerg A. Plasma osteoprotegerin levels are associated with glycaemic status, systolic blood pressure, kidney function and cardiovascular morbidity in type 1 diabetic patients. Eur J Endocrinol. 2006 Jan;154(1):75-81.
35. Anand DV, Lahiri A, Lim E, Hopkins D, Corder R. The relationship between plasma osteoprotegerin levels and coronary artery calcification in uncomplicated type 2 diabetic subjects. J Am Coll Cardiol. 2006 May 2;47(9):1850-1857. Epub 2006 Apr 19.
36. Kim SM, Lee J, Ryu OH, Lee KW, Kim HY, Seo JA, Kim SG, Kim NH, Baik SH, Choi DS, Choi KM. Serum osteoprotegerin levels are associated with inflammation and pulse wave velocity. Clin Endocrinol (Oxf). 2005 Nov;63(5):594-598.
37. Secchiero P, Corallini F, Pandolfi A, Consoli A, Candido R, Fabris B, Celeghini C, Capitani S, Zauli G. An increased osteoprotegerin serum release characterizes the early onset of diabetes mellitus and may contribute to endothelial cell dysfunction Am J Pathol. 2006 Dec;169(6):2236-2244.
38. Knudsen ST, Foss CH, Poulsen PL, Andersen NH, Mogensen CE, Rasmussen LM. Increased plasma concentrations of osteoprotegerin in type 2 diabetic patients with microvascular complications. Eur J Endocrinol. 2003 Jul;149(1):39-42.
39. Edmonds ME, Morrison N, Laws JW, Watkins PJ. Medial arterial calcification and diabetic neuropathy. Br Med J (Clin Res Ed). 1982 Mar 27;284(6320):928-930.
40. Young MJ, Adams JE, Anderson GF, Boulton AJ, Cavanagh PR. Medial artery calcification in the feet of diabetic patients and matched non-diabetic controls. Diabetologia. 1993 Jul;36(7):615-621.
41. Mayfield JA, Caps MT, Boyko EJ, Ahroni JH, Smith DG. Relationship of medial arterial calcinosis to autonomic neuropathy and adverse outcomes in a diabetic veteran population. J Diabetes Complications. 2002 Mar-Apr;16(2):165-171.
42. Psyrogiannis A, Kyriazopoulou V, Vagenakis AG. Medial arterial calcification is frequently found in patients with microalbuminuria. Angiology. 1999 Dec;50(12):971-975.
43. Sinha S, Munichoodappa CS, Kozak GP. Neuroarthropathy (Charcot joints) in diabetes mellitus (clinical study of 101 cases). Medicine (Baltimore). 1972 May;51(3):191-210.
44. Jeffcoate WJ, Game F, Cavanagh PR. The role of proinflammatory cytokines in the cause of neuropathic osteoarthropathy (acute Charcot foot) in diabetes. Lancet. 2005 Dec 10;366(9502):2058-2061. Epub 2005 Aug 10.
45. Laroche M, Delmotte A. Increased arterial calcification in Paget's disease of bone. Calcif Tissue Int. 2005 Sep;77(3):129-133. Epub 2005 Sep 8.
46. Goebel FD, Füessel HS. Mönckeberg's sclerosis after sympathetic denervation in diabetic and non-diabetic subjects. Diabetologia. 1983 May;24(5):347-350.
47. Forst T, Pfützner A, Kann P, Lobmann R, Schäfer H, Beyer J. Association between diabetic-autonomic-C-fibre-neuropathy and medial wall calcification in the outcome of trophic foot lesions. Exp Clin Endocrinol Diabetes. 1995;103(2):94-98.
48. Maguire AM, Craig ME, Craighead A, Chan AK, Cusumano JM, Hing SJ, Silink M, Howard NJ, Donaghue KC. Autonomic nerve testing predicts the development of complications. Diabetes Care. 2007 Jan;30(1):77-82.
49. Naot D, Cornish J. The role of peptides and receptors of the calcitonin family in the regulation of bone metabolism. Bone. 2008 Nov;43(5):813-818. Epub 2008 Jul 18.
50. Zochodne DW, Verge VM, Cheng C, Sun H, Johnston J. Does diabetes target ganglion neurones? Progressive sensory neurone involvement in long-term experimental diabetes. Brain. 2001 Nov;124(Pt 11):2319-2334.
51. Jiang Y, Nyengaard JG, Zhang JS, Jakobsen J. Selective loss of calcitonin gene-related peptide-expressing primary sensory neurons of the a-cell phenotype in early and experimental diabetes. Diabetes. 2004 Oct;53(10):2669-2675.
52. La Fontaine J, Harkless LB, Sylvia VL, Carnes D, Heim-Hall J, Jude E. Levels of endothelial nitric oxide synthase and calcitonin gene-related peptide in the Charcot foot: a pilot study. J Foot Ankle Surg. 2008 Sep-Oct;47(5):424-429. Epub 2008 Jul 14.
53. McDougall JJ, Yeung G, Leonard CA, Bray RC. A role for calcitonin gene-related peptide in rabbit knee joint ligament healing. Can J Physiol Pharmacol. 2000 Jul;78(7):535-540.
54. Lerner UH. Deletions of genes encoding calcitonin/alpha- CGRP, amylin and calcitonin receptor have given new and unexpected insights into the function of calcitonin receptors and calcitonin receptor-like receptors in bone. J Musculoskelet Neuronal Interact. 2006 Jan-Mar;6(1):87-95.
55. Cornish J, Callon KE, Bava U, Kamona SA, Cooper GJ, Reid IR. Effects of calcitonin, amylin, and calcitonin gene-related peptide on osteoclast development. Bone. 2001 Aug;29(2):162-168.
56. Yamaguchi M, Kojima T, Kanekawa M, Alhara N, Nogimura A, Kasai K. Neuropeptides stimulate production of interleukin-6, and tumor necrosis factor-alpha in human dental pulp cells. Inflamm Res. 2004 May;53(5):199-204. Epub 2004 Apr 21.
57. Martin CD, Jimenez-Andrade JM, Ghilardi JR, Mantyh PW. Organization of a unique net-like meshwork of CGRP+ sensory fibers in the mouse periosteum: implications for the generation and maintenance of bone fracture pain. Neurosci Lett. 2007 Nov 12;427(3):148-152. Epub 2007 Sep 1.
58. Elefteriou F, Ahn JD, Takeda S, Starbuck M, Yang X, Liu X, Kondo H, Richards WG, Bannon TW, Noda M, Clement K, Vaisse C, Karsenty G. Leptin regulation of bone resorption by the sympathetic nervous system. Nature. 2005 Mar 24;434(7032):514-520. Epub 2005 Feb 20.
59. Ishizuka K, Hirukawa K, Nakamura H, Togari A. Inhibitory effect of CGRP on osteoclast formation by mouse bone marrow cells treated with isoproterenol. Neurosci Lett. 2005 Apr 29;379(1):47-51. Epub 2005 Jan 18.
60. Armano S, Atai M, Goto S, Togari A. Inhibitory effect of NPY on isoprenaline-induced osteoclastogenesis in mouse bone marrow cells. Biochim Biophys Acta. 2007 Jun;1770(6):966-73. Epub 2007 Mar 1.
61. Do Y, McKallip RJ, Nagarkatti M, Nagarkatti PS. Activation through cannabinoid receptors 1 and 2 on dendritic cells triggers NF-kappa-B-dependent apoptosis: novel role for endogenous and exogenous cannabinoids in immunoregulation. J Immunol. 2004 Aug 15;173(4):2373-2382.
62. Soedamah-Muthu SS, Chaturvedi N, Witte DR, Stevens LK, Porta M, Fuller JP. Relationship between risk factors and mortality in type 1 diabetic patients in Europe. Diabetes Care. 2008 Jul;31(7):1360-1366. Epub 2008 Mar 28.
63. Forsblom CM, Sane T, Groop PH, Tötterman KJ, Kallio M, Saloranta C, Laasonen L, Summanen P, Lepäntalo M, Laatikainen L, Matikainen E, Teppo AM, Koskimies S, Groop L. Risk factors for mortality in Type II (non-insulin dependent) diabetes: evidence of a role for neuropathy and a protective effect of HLA-DR4. Diabetologia. 1998 Nov;41(11):1253-1262.
64. Coppini DV, Bowtell PA, Weng C, Young PJ, Sönksen PH. Showing neuropathy is related to increased mortality in diabetic patients-a survival analysis using an accelerated failure time model. J Clin Epidemiol. 2000 May;53(5):519-523.
65. Rossing P, Hougaard P, Borch-Johnsen K, Parving HH. Predictors of mortality in insulin-dependent diabetes: 10 year observational follow-up study. BMJ. 1996 Sep 28;313(7060):779-784.
66. Stephenson JM, Kenny S, Stevens LK, Fuller JH, Lee E. Proteinuria and mortality in diabetes: the WHO multinational study of vascular disease in diabetes. Diabet Med. 1995 Feb;12(2):149-155
67. Olson JC, Erbey JR, Williams KV, Becker DJ, Edmundowicz D, Kelsey SF, Tyrrell KS, Orchard TJ. Subclinical atherosclerosis and estimated glucose disposal rate as predictors of mortality in type 1 diabetes. Ann Epidemiol. 2002 Jul;12(5):331-337.
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Molitvoslovova N.A., Galstyan G.R. Role of distal diabetic polyneuropathy in the development of media calcification in patients with diabetesmellitus. Diabetes mellitus. 2012;15(2):64-69. (In Russ.)
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