A concomitant review of the effects of diabetes mellitus and hypothyroidism in wound healing

World Journal of Gastroenterology

Volumn 12, Issue 17, 2006, Pages 2721-2729

  Ekmektzoglou, Konstantinos A ^a,c   Zografos, Georgios C ^b  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^b HIPPOKRATION HOSPITAL   (Greece)

^c NONE   (Greece)

Author keywords

Anastomosis; Diabetes mellitus; Hypothyroidism; Wound healing

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADVANCED GLYCATION END PRODUCT; EPIDERMAL GROWTH FACTOR; GLUCOCORTICOID; GLUCOSE; GLUCOSE TRANSPORTER 1; HEMOGLOBIN A1C; HYDROXYPROLINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN; INSULIN RECEPTOR; INSULINASE; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; LEVOTHYROXINE; MATRIX METALLOPROTEINASE; PLATELET DERIVED GROWTH FACTOR; PROTEIN KINASE C; RECOMBINANT BASIC FIBROBLAST GROWTH FACTOR; RECOMBINANT PLATELET DERIVED GROWTH FACTOR BB; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RETINOL; SOMATOMEDIN BINDING PROTEIN; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; THYROID HORMONE; TUMOR NECROSIS FACTOR ALPHA; ZINC;

BIOCHEMISTRY; DIABETES MELLITUS; DIABETIC NEUROPATHY; DIABETIC RETINOPATHY; DRUG POTENTIATION; GASTROINTESTINAL DISEASE; GLUCOSE BLOOD LEVEL; HISTOPATHOLOGY; HUMAN; HYPERGLYCEMIA; HYPOTHYROIDISM; INTESTINE ANASTOMOSIS; LIPID METABOLISM; METABOLIC DISORDER; MICROANGIOPATHY; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN METABOLISM; REVIEW; TISSUE REGENERATION; WOUND DEHISCENCE; WOUND HEALING IMPAIRMENT;

EID: 33744488826     PISSN: 10079327     EISSN: None     Source Type: Journal    
DOI: 10.3748/wjg.v12.i17.2721     Document Type: Review

References (101)

1. Norris SO, Provo B, Stotts NA. Physiology of wound healing and risk factors that impede the healing process. AACN Clin Issues Crit Care Nurs 1990; 1: 545-552
2. Stadelmann WK, Digenis AG, Tobin GR. Impediments to wound healing. Am J Surg 1998; 176: 39S-47S
3. Rosenberg CS. Wound healing in the patient with diabetes mellitus. Nurs Clin North Am 1990; 25: 247-261
4. Flynn MD, Tooke JE. Aetiology of diabetic foot ulceration: a role for the microcirculation? Diabet Med 1992; 9: 320-329
5. Pober JS, Cotran RS. The role of endothelial cells in inflammation. Transplantation 1990; 50: 537-544
6. Silhi N. Diabetes and wound healing. J Wound Care 1998; 7: 47-51
7. Christopherson K. The impact of diabetes on wound healing: implications of microcirculatory changes. Br J Community Nurs 2003; 8: S6-13
8. Collins N. Diabetes, nutrition, and wound healing. Adv Skin Wound Care 2003; 16: 291-294
9. Terranova A. The effects of diabetes mellitus on wound healing. Plast Surg Nurs 1991; 11: 20-25
10. Marhoffer W, Stein M, Maeser E, Federlin K. Impairment of polymorphonuclear leukocyte function and metabolic control of diabetes. Diabetes Care 1992; 15: 256-260
11. Kwoun MO, Ling PR, Lydon E, Imrich A, Qu Z, Palombo J, Bistrian BR. Immunologic effects of acute hyperglycemia in nondiabetic rats. JPEN J Parenter Enteral Nutr 1997; 21: 91-95
12. McMurtry AL, Cho K, Young LJ, Nelson CF, Greenhalgh DG. Expression of HSP70 in healing wounds of diabetic and nondiabetic mice. J Surg Res 1999; 86: 36-41
13. Mohan IK, Das UN. Effect of L-arginine-nitric oxide system on chemical-induced diabetes mellitus. Free Radic Biol Med 1998; 25: 757-765
14. Haluzik M, Nedvidkova J, Skrha J. Treatment with the NO-synthase inhibitor, methylene blue, moderates the decrease in serum leptin concentration in streptozotocin-induced diabetes. Endocr Res 1999; 25: 163-171
15. Moulin V, Lawny F, Barritault D, Caruelle JP. Platelet releasate treatment improves skin healing in diabetic rats through endogenous growth factor secretion. Cell Mol Biol (Noisy-le-grand) 1998; 44: 961-971
16. Beer HD, Longaker MT, Werner S. Reduced expression of PDGF and PDGF receptors during impaired wound healing. J Invest Dermatol 1997; 109: 132-138
17. Bitar MS. Insulin-like growth factor-1 reverses diabetes-induced wound healing impairment in rats. Horm Metab Res 1997; 29: 383-386
18. Hehenberger K, Heilborn JD, Brismar K, Hansson A. Inhibited proliferation of fibroblasts derived from chronic diabetic wounds and normal dermal fibroblasts treated with high glucose is associated with increased formation of l-lactate. Wound Repair Regen 1998; 6: 135-141
19. Darby IA, Bisucci T, Hewitson TD, MacLellan DG. Apoptosis is increased in a model of diabetes-impaired wound healing in genetically diabetic mice. Int J Biochem Cell Biol 1997; 29: 191-200
20. Fukui M, Nakamura T, Ebihara I, Shirato I, Tomino Y, Koide H. ECM gene expression and its modulation by insulin in diabetic rats. Diabetes 1992; 41: 1520-1527
21. King L. Impaired wound healing in patients with diabetes. Nurs Stand 2001; 15: 39-45
22. Morain WD, Colen LB. Wound healing in diabetes mellitus. Clin Plast Surg 1990; 17: 493-501
23. Meyer JS. Diabetes and wound healing. Crit Care Nurs Clin North Am 1996; 8: 195-201
24. Edelson GW. Systemic and nutritional considerations in diabetic wound healing. Clin Podiatr Med Surg 1998; 15: 41-48
25. Lioupis C. Effects of diabetes mellitus on wound healing: an update. J Wound Care 2005; 14: 84-86
26. Komesu MC, Tanga MB, Buttros KR, Nakao C. Effects of acute diabetes on rat cutaneous wound healing. Pathophysiology 2004; 11: 63-67
27. Greenhalgh DG. Wound healing and diabetes mellitus. Clin Plast Surg 2003; 30: 37-45
28. Kamal K, Powell RJ, Sumpio BE. The pathobiology of diabetes mellitus: implications for surgeons. J Am Coll Surg 1996; 183: 271-289
29. Fahey TJ 3rd, Sadaty A, Jones WG 2nd, Barber A, Smoller B, Shires GT. Diabetes impairs the late inflammatory response to wound healing. J Surg Res 1991; 50: 308-313
30. Goodson WH 3rd, Hunt TK. Wound healing and the diabetic patient. Surg Gynecol Obstet 1979; 149: 600-608
31. Goodson WH 3rd, Hunt TK. Wound healing in experimental diabetes mellitus: importance of early insulin therapy. Surg Forum 1978; 29: 95-98
32. Goodson WH 3rd, Hung TK. Studies of wound healing in experimental diabetes mellitus. J Surg Res 1977; 22: 221-227
33. Hennessey PJ, Ford EG, Black CT, Andrassy RJ. Wound collagenase activity correlates directly with collagen glycosylation in diabetic rats. J Pediatr Surg 1990; 25: 75-78
34. McMurry JF Jr. Wound healing with diabetes mellitus. Better glucose control for better wound healing in diabetes. Surg Clin North Am 1984; 64: 769-778
35. Sannomiya P, Pereira MA, Garcia-Leme J. Inhibition of leukocyte chemotaxis by serum factor in diabetes mellitus: selective depression of cell responses mediated by complement-derived chemoattractants. Agents Actions 1990; 30: 369-376
36. Robson MC, Heggers JP. Effect of hyperglycemia on survival of bacteria. Surg Forum 1969; 20: 56-57
37. Seifter E, Rettura G, Padawer J, Stratford F, Kambosos D, Levenson SM. Impaired wound healing in streptozotocin diabetes. Prevention by supplemental vitamin A. Ann Surg 1981; 194: 42-50
38. Engel ED, Erlick NE, Davis RH. Diabetes mellitus: impaired wound healing from zinc deficiency. J Am Podiatry Assoc 1981; 71: 536-544
39. Yue DK, McLennan S, Marsh M, Mai YW, Spaliviero J, Delbridge L, Reeve T, Turtle JR. Effects of experimental diabetes, uremia, and malnutrition on wound healing. Diabetes 1987; 36: 295-299
40. Duckworth WC, Fawcett J, Reddy S, Page JC. Insulin-degrading activity in wound fluid. J Clin Endocrinol Metab 2004; 89: 847-851
41. Doxey DL, Ng MC, Dill RE, Iacopino AM. Platelet-derived growth factor levels in wounds of diabetic rats. Life Sci 1995; 57: 1111-1123
42. Greenhalgh DG, Sprugel KH, Murray MJ, Ross R. PDGF and FGF stimulate wound healing in the genetically diabetic mouse. Am J Pathol 1990; 136: 1235-1246
43. Hennessey PJ, Black CT, Andrassy RJ. Epidermal growth factor and insulin act synergistically during diabetic healing. Arch Surg 1990; 125: 926-929
44. Bitar MS, Labbad ZN. Transforming growth factor-beta and insulin-like growth factor-I in relation to diabetes-induced impairment of wound healing. J Surg Res 1996; 61: 113-119
45. Spravchikov N, Sizyakov G, Gartsbein M, Accili D, Tennenbaum T, Wertheimer E. Glucose effects on skin keratinocytes: implications for diabetes skin complications. Diabetes 2001; 50: 1627-1635
46. Pavlidis TE, Galatianos IN, Papaziogas BT, Lazaridis CN, Atmatzidis KS, Makris JG, Papaziogas TB. Complete dehiscence of the abdominal wound and incriminating factors. Eur J Surg 2001; 167: 351-354; discussion 355
47. Prakash A, Kapur M, Maini BS. Wound healing in experimental diabetes: histological, histochemical and biochemical studies. Indian J Med Res 1973; 61: 1200-1206
48. Prakash A, Pandit PN, Sharman LK. Studies in wound healing in experimental diabetes. Int Surg 1974; 59: 25-28
49. Thornton FJ, Barbul A. Healing in the gastrointestinal tract. Surg Clin North Am 1997; 77: 549-573
50. Wagner OJ, Egger B. Influential factors in anastomosis healing. Swiss Surg 2003; 9: 105-113
51. Gottrup F, Andreassen TT. Healing of incisional wounds in stomach and duodenum: the influence of experimental diabetes. J Surg Res 1981; 31: 61-68
52. Takeuchi K, Takehara K, Tajima K, Kato S, Hirata T. Impaired healing of gastric lesions in streptozotocin-induced diabetic rats: effect of basic fibroblast growth factor. J Pharmacol Exp Ther 1997; 281: 200-207
53. Verhofstad MH, Hendriks T. Diabetes impairs the development of early strength, but not the accumulation of collagen, during intestinal anastomotic healing in the rat. Br J Surg 1994; 81: 1040-1045
54. Verhofstad MH, Bisseling TM, Haans EM, Hendriks T. Collagen synthesis in rat skin and ileum fibroblasts is affected differently by diabetes-related factors. Int J Exp Pathol 1998; 79: 321-328
55. Verhofstad MH, Hendriks T. Complete prevention of impaired anastomotic healing in diabetic rats requires preoperative blood glucose control. Br J Surg 1996; 83: 1717-1721
56. van der Hem LG, Verhofstad MH, Bocken CF, van der Vliet JA, Hendriks T. Pancreatic islet transplantation prevents impaired healing of intestinal anastomoses in diabetes. Transplant Proc 1994; 26: 660-661
57. Verhofstad MH, Lomme RM, de Man BM, Hendriks T. Intestinal anastomoses from diabetic rats contain supranormal levels of gelatinase activity. Dis Colon Rectum 2002; 45: 554-561
58. Martens MF, Hendriks T. Postoperative changes in collagen synthesis in intestinal anastomoses of the rat: differences between small and large bowel. Gut 1991; 32: 1482-1487
59. Verhofstad MH, Lange WP, van der Laak JA, Verhofstad AA, Hendriks T. Microscopic analysis of anastomotic healing in the intestine of normal and diabetic rats. Dis Colon Rectum 2001; 44: 423-431
60. Onodera H, Ikeuchi D, Nagayama S, Imamura M. Weakness of anastomotic site in diabetic rats is caused by changes in the integrity of newly formed collagen. Dig Surg 2004; 21: 146-151
61. Brasken P. Healing of experimental colon anastomosis. Eur J Surg Suppl 1991;: 1-51
62. Witte MB, Barbul A. Repair of full-thickness bowel injury. Crit Care Med 2003; 31: S538-S546
63. Makela JT, Kiviniemi H, Laitinen S. Risk factors for anastomotic leakage after left-sided colorectal resection with rectal anastomosis. Dis Colon Rectum 2003; 46: 653-660
64. Siperstein MD. Special medical problems in surgical patients. In: Way LW, eds. Current surgical diagnosis and treatment. California: Lange Medical Publications, 1994: 42
65. Murkin JM. Anesthesia and hypothyroidism: a review of thyroxine physiology, pharmacology, and anesthetic implications. Anesth Analg 1982; 61: 371-383
66. Crowley WF Jr, Ridgway EC, Bough EW, Francis GS, Daniels GH, Kourides IA, Myers GS, Maloof F. Noninvasive evaluation of cardiac function in hypothyroidism. Response to gradual thyroxine replacement. N Engl J Med 1977; 296: 1-6
67. Zwillich CW, Pierson DJ, Hofeldt FD, Lufkin EG, Weil JV. Ventilatory control in myxedema and hypothyroidism. N Engl J Med 1975; 292: 662-665
68. Derubertis FR Jr, Michelis MF, Bloom ME, Mintz DH, Field JB, Davis BB. Impaired water excretion in myxedema. Am J Med 1971; 51: 41-53
69. Swanson JW, Kelly JJ Jr, McConahey WM. Neurologic aspects of thyroid dysfunction. Mayo Clin Proc 1981; 56: 504-512
70. Shenfield GM. Influence of thyroid dysfunction on drug pharmacokinetics. Clin Pharmacokinet 1981; 6: 275-297
71. Catz B, Russell S. Myxedema, shock and coma. Seven survival cases. Arch Intern Med 1961; 108: 407-417
72. Ladenson PW, Levin AA, Ridgway EC, Daniels GH. Complications of surgery in hypothyroid patients. Am J Med 1984; 77: 261-266
73. Prockop DJ, Sjoerdsma A. Significance of urinary hydroxyproline in man. J Clin Invest 1961; 40: 843-849
74. Benoit FL, Theil GB, Watten RH. Hydroxyproline excretion in endocrine disease. Metabolism 1963; 12: 1072-1082
75. Kivirikko KI, Koivusalo M, Laitinen O, Lamberg BA. Hydroxyproline in the serum and urine of patients with hyperthyroidism. J Clin Endocrinol Metab 1964; 24: 222-223
76. Kowalewski K, Yong S. Hydroxyproline in healing dermal wounds of normal and hypothyroid rats. Acta Endocrinol (Copenh) 1967; 54: 1-7
77. Lennox J, Johnston ID. The effect of thyroid status on nitrogen balance and the rate of wound healing after injury in rats. Br J Surg 1973; 60: 309
78. Mehregan AH, Zamick P. The effect of triiodothyronine in healing of deep dermal burns and marginal scars of skin grafts. A histologic study. J Cutan Pathol 1974; 1: 113-116
79. Herndon DN, Wilmore DW, Mason AD Jr, Curreri PW. Increased rates of wound healing in burned guinea pigs treated with L-thyroxine. Surg Forum 1979; 30: 95-97
80. Kivirikko KI, Laitinen O, Aer J, Halme J. Metabolism of collagen in experimental hyperthyroidism and hypothyroidism in the rat. Endocrinology 1967; 80: 1051-1061
81. McNeill AD, Thomson JA. Long-term follow-up of surgically treated thyrotoxic patients. Br Med J 1968; 3: 643-646
82. Pirk FW, ElAttar TM, Roth GD. Effect of analogues of steroid and thyroxine hormones on wound healing in hamsters. J Periodontal Res 1974; 9: 290-297
83. Alexander MV, Zajtchuk JT, Henderson RL. Hypothyroidism and wound healing: occurrence after head and neck radiation and surgery. Arch Otolaryngol 1982; 108: 289-291
84. Cannon CR. Hypothyroidism in head and neck cancer patients: experimental and clinical observations. Laryngoscope 1994; 104: 1-21
85. Erdogan M, Ilhan YS, Akkus MA, Caboglu SA, Ozercan I, Ilhan N, Yaman M. Effects of L-thyroxine and zinc therapy on wound healing in hypothyroid rats. Acta Chir Belg 1999; 99: 72-77
86. Saner G, Savasan S, Saka N. Zinc metabolism in hypothyroidism. Lancet 1992; 340: 432-433
87. Panchenko MV, Stetler-Stevenson WG, Trubetskoy OV, Gacheru SN, Kagan HM. Metalloproteinase activity secreted by fibrogenic cells in the processing of prolysyl oxidase. Potential role of procollagen C-proteinase. J Biol Chem 1996; 271: 7113-7119
88. Franzen LE, Ghassemifar MR. Connective tissue repair in zinc deficiency. An ultrastructural morphometric study in perforated mesentery in rats. Eur J Surg 1992; 158: 333-337
89. Natori J, Shimizu K, Nagahama M, Tanaka S. The influence of hypothyroidism on wound healing. An experimental study. Nippon Ika Daigaku Zasshi 1999; 66: 176-180
90. Safer JD, Crawford TM, Fraser LM, Hoa M, Ray S, Chen TC, Persons K, Holick MF. Thyroid hormone action on skin: diverging effects of topical versus intraperitoneal administration. Thyroid 2003; 13: 159-165
91. Safer JD, Fraser LM, Ray S, Holick MF. Topical triiodothyronine stimulates epidermal proliferation, dermal thickening, and hair growth in mice and rats. Thyroid 2001; 11: 717-724
92. Faergemann J, Sarnhult T, Hedner E, Carlsson B, Lavin T, Zhao XH, Sun XY. Dose-response effects of tri-iodothyroacetic acid (Triac) and other thyroid hormone analogues on glucocorticoid-induced skin atrophy in the haired mouse. Acta Derm Venereol 2002; 82: 179-183
93. Paladini RD, Takahashi K, Bravo NS, Coulombe PA. Onset of re-epithelialization after skin injury correlates with a reorganization of keratin filaments in wound edge keratinocytes: defining a potential role for keratin 16. J Cell Biol 1996; 132: 381-397
94. Freedberg IM, Tomic-Canic M, Komine M, Blumenberg M. Keratins and the keratinocyte activation cycle. J Invest Dermatol 2001; 116: 633-640
95. Wojcik SM, Bundman DS, Roop DR. Delayed wound healing in keratin 6a knockout mice. Mol Cell Biol 2000; 20: 5248-5255
96. Paramio JM, Casanova ML, Segrelles C, Mittnacht S, Lane EB, Jorcano JL. Modulation of cell proliferation by cytokeratins K10 and K16. Mol Cell Biol 1999; 19: 3086-3094
97. Wawersik MJ, Mazzalupo S, Nguyen D, Coulombe PA. Increased levels of keratin 16 alter epithelialization potential of mouse skin keratinocytes in vivo and ex vivo. Mol Biol Cell 2001; 12: 3439-3450
98. Safer JD, Crawford TM, Holick MF. A role for thyroid hormone in wound healing through keratin gene expression. Endocrinology 2004; 145: 2357-2361
99. Radoja N, Diaz DV, Minars TJ, Freedberg IM, Blumenberg M, Tomic-Canic M. Specific organization of the negative response elements for retinoic acid and thyroid hormone receptors in keratin gene family. J Invest Dermatol 1997; 109: 566-572
100. Zografos GC, Martis K, Morris DL. Laser Doppler flowmetry in evaluation of cutaneous wound blood flow using various suturing techniques. Ann Surg 1992; 215: 266-268
101. Zografos GC, Simeonidis KM, Parasi AS, Messaris EG, Menenakos EE, Dontas IA, Marti KC, Androulakis GA. Adhesion formation: intraperitoneal catheters in surgical practice. J Invest Surg 2002; 15: 37-43