Pulmonary complications in diabetes mellitus

Chronic Respiratory Disease

Volumn 5, Issue 2, 2008, Pages 101-108

  Kaparianos, A ^a   Argyropoulou, E ^a   Sampsonas, F ^a   Karkoulias, K ^a   Tsiamita, M ^a   Spiropoulos, K ^a  

^a UNIVERSITY OF PATRAS   (Greece)

Author keywords

Alveolar gas exchange; Autonomic neuropathy; Diabetes mellitus; Lung dysfunction; Pulmonary function tests

Indexed keywords

ACETYLCHOLINE; CARBON MONOXIDE; DIPEPTIDYL CARBOXYPEPTIDASE; ENDOMORPHIN 1; ENDOMORPHIN 2; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOSE; GLYCOSYLATED HEMOGLOBIN; HYDROGEN PEROXIDE; INDUCIBLE NITRIC OXIDE SYNTHASE; NEUROKININ A; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OPIATE RECEPTOR; PEROXYNITRITE; PEROXYNITROUS ACID; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SUBSTANCE P;

AUTONOMIC NEUROPATHY; BRONCHUS TONE; DIABETIC ANGIOPATHY; DISEASE ASSOCIATION; ENZYME ACTIVITY; EXERCISE; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; LUNG BLOOD VESSEL; LUNG CAPILLARY; LUNG CLEARANCE; LUNG COMPLICATION; LUNG DIFFUSION CAPACITY; LUNG DISEASE; LUNG FUNCTION TEST; LUNG GAS EXCHANGE; LUNG MECHANICS; LUNG SCINTISCANNING; NEUROTRANSMISSION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SPIROMETRY; ANIMAL; BREATHING; DIABETES MELLITUS; FORCED EXPIRATORY VOLUME; LUNG; LUNG ALVEOLUS; PATHOPHYSIOLOGY; PHYSIOLOGY; VITAL CAPACITY;

ANIMALS; DIABETES COMPLICATIONS; FORCED EXPIRATORY VOLUME; HUMANS; LUNG; LUNG DISEASES; OXIDATIVE STRESS; PULMONARY ALVEOLI; PULMONARY GAS EXCHANGE; RESPIRATION; SPIROMETRY; VITAL CAPACITY;

EID: 53449101839     PISSN: 14799723     EISSN: 14799731     Source Type: Journal    
DOI: 10.1177/1479972307086313     Document Type: Review

References (92)

1. 1 Engelgau MM Geiss LS. The burden of diabetes mellitus. In: Leahy, JL, Clark, NG, Cefalu, WT. Medical management of diabetes mellitus. New York: Marcel Dekker ; 2000.
2. The Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 1993 ; 329: 977 - 986.
3. UK Prospective Diabetes Study (UKPDS) Group. Intensive blood-glucose control with sulfonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). Lancet 1998 ; 352: 837 - 853.
4. Bell D Collier A Mathews DM Cooksey EJ Mettardy GJR Clarke BF. Are reduced lung volumes in IDDM due to defect in connective tissue? Diabetes 1988 ; 37: 829 - 831.
5. Cooper BG Taylor R Alberti KGMM Gibson GJ. Lung function in patients with diabetes mellitus. Respir Med 1990 ; 84: 235 - 239.
6. Guazzi M Brambilla R Pontone G Agostoni P Guazzi MD. Effects of non-insulin dependent diabetes mellitus on pulmonary function and exercise tolerance in chronic congestive heart failure. Am J Cardiol 2002 ; 89: 191 - 197.
7. Vracko R Thorning D Huang TW. Basal lamina of alveolar epithelial and capillaries. Quantitative changes with aging and with diabetes mellitus. Am Rev Respir Dis 1979 ; 120: 973 - 983.
8. Kodolova IM Lysenko LV Saltykov BB. Changes in the lungs in diabetes mellitus. Arkh Patol 1982 ; 44: 35 - 40.
9. Brownlee M Vlassara H Cerami A. Non-enzymatic glycosylation and the pathogenesis of diabetic complications. Ann Intern Med 1984 ; 101: 527 - 537.
10. Ofulue AF Kida K Thurbleck WM. Experimental diabetes and the lung: I. Changes in growth, morphometry, and biochemistry. Am Rev Respir Dis 1988 ; 137: 162 - 166.
11. Schernthaner G Haber P Kummer F Ludwig H. Lung elasticity in juvenile-onset diabetes mellitus. Am Rev Respir Dis 1977 ; 116: 544 - 546.
12. Maccioni FJ Colebatch HJ. Lung volume and distensibility in insulin dependent diabetes mellitus. Am Rev Respir Dis 1991 ; 143: 1253 - 1256.
13. Strojek K Ziora D Sroczynski JW Oklek K. Pulmonary complications of type 1 (insulin-dependent) diabetic patients. Diabetologia 1992 ; 35: 1173 - 1176.
14. Katoh J Hara Y Kurusu M Miyaji J Narutaki K. Cardiorespiratory function as assessed by exercise testing in patients with non-insulin dependent diabetes mellitus. J Int Med Res 1996 ; 24: 209 - 213.
15. Sandler M Bunn AE Stewart RI. Cross-section study of pulmonary function in patients with insulin-dependent diabetes mellitus. Am Rev Respir Dis 1987 ; 135: 1223 - 1229.
16. Barrett-Connor E Frette C. NIDDM, impaired glucose tolerance, and pulmonary function in older adults: the Rancho Bernardo Study. Diabetes Care 1996 ; 19: 1441 - 1444.
17. Schnack C Festa A Schwarzmaier-D'Assie A Haber P Schernthaner G. Pulmonary dysfunction in type 1 diabetes in relation to metabolic long-term control and to incipient diabetic nephropathy. Nephron 1996 ; 74: 395 - 400.
18. Innocenti F Fabbri A Anichini R Tuci S Pettina G Vannucci F. Indications of reduced pulmonary function in type 1 (insulin-dependent) diabetes mellitus. Diabetes Res Clin Pract 1994 ; 25: 161 - 168.
19. Meo SA Al-Drees AM Arif M Al-Rubean K. Lung function in type 2 Saudi diabetic patients. Saudi Med J 2006 ; 27: 338 - 343.
20. Boulbou MS Gourgoulianis KI Klisiaris VK Tsikrikas TS Stathakis NE Molyvdas PA. Diabetes mellitus and lung function. Med Princ Pract 2003 ; 12: 87 - 91.
21. Primhak RA Whincup G Tsanakas JN Milner RD. Reduced vital capacity in insulin-dependent diabetes. Diabetes 1987 ; 36: 324 - 326.
22. Cazzato S Bernardi F Salardi S Tassinari D Corsini I Ragni L. Lung function in children with diabetes mellitus. Pediatr Pulmonol 2004 ; 37: 17 - 23.
23. Lange P Groth S Kastrup J Mortensen J Appleyard M Nyboe J. Diabetes mellitus, plasma glucose and lung function in a cross-sectional population study. Eur Respir J 1989 ; 2: 14 - 19.
24. Lange P Groth S Mortensen J Appleyard M Nyboe J Schnohr P. Diabetes mellitus and ventilatory capacity: a five year follow up study. Eur Respir J 1990 ; 3: 288 - 292.
25. Lange P Parner J Schnohr P Jensen G. Copenhagen City Heart Study: longitudinal analysis of ventilatory capacity in diabetic and nondiabetic adults. Eur Respir J 2002 ; 20: 1406 - 1412.
26. Enright P Kronmal R Higgins M Schenker M Haponik E. Spirometry reference values for women and men 65 to 85 years of age. Am Rev Respir Dis 1993 ; 147: 125 - 133.
27. Walter RE Beiser A Givelber RJ O'Connor GT Gottlieb DJ. Association between glycemic state and lung function: the Framingham Heart Study. Am J Respir Crit Care Med 2003 ; 167: 911 - 916.
28. Lawlor DA Ebrahim S Davey Smith G. Association of measures of lung function with insulin resistance and type 2 diabetes: findings from the British Women's Heart and Health Study. Diabetologia 2004 ; 47: 195 - 203.
29. Davis T Knuiman M Kendall P Vu H Davis WA. Reduced pulmonary function and its associations in type 2 diabetes: the Fremantle Diabetes Study. Diabetes Res Clin Pract 2000 ; 50: 153 - 159.
30. Litonjua AA Lazarus R Sparrow W DeMolles D Weiss S. Lung function in type 2 diabetes: the Normative Aging Study. Respir Med 2005 ; 99: 1583 - 1590.
31. Engstrom G Hedblad B Nilsson P Wollmer P Berglund G Janzon L. Risk of developing diabetes is inversely related to lung function: a population-based cohort study. Diabet Med 2002 ; 19: 167 - 170.
32. Engstrom G Hedblad B Nilsson P Wollmer P Berglund G Janzon L. Lung function, insulin resistance and the incidence of cardiovascular disease. A longitudinal cohort study. J Intern Med 2003 ; 253: 574 - 581.
33. Benbassat CA Stern E Mordechai K Lebzelter J Blum I Fink G. Pulmonary function in patients with diabetes mellitus. Am J Med Sci 2001 ; 322: 127 - 132.
34. Wanke TH Formanek D Auginer M Zwick H Irsigler K. Pulmonary gas exchange and oxygen uptake during exercise in patients with type 1 diabetes mellitus. Diabet Med 1992 ; 9: 252 - 257.
35. Niranjan V McBrayer DG Ramirez LC Raskin P Hsia CC. Glycemic control and cardiopulmonary function in patients with insulin-dependent diabetes mellitus. Am J Med 1997 ; 103: 504 - 513.
36. Cefalu W Skyler J Kourides I Landschulz W Balagtas C Cheng S. Inhaled Insulin Study Group. Inhaled human insulin treatment in patients with type 2 diabetes mellitus. Ann Intern Med 2001 ; 134: 203 - 207.
37. Skyler J Weinstock R Raskin P Yale JF Barrett E, Gerich. Use of inhaled insulin in a basal/bolus insulin regimen in type 1 diabetic subjects: a 6-month, randomized, comparative trial. Diabetes Care 2005 ; 28: 1630 - 1605.
38. Morgan W Reger R. Rise and fall of the FEV1. Chest 2000 ; 118: 1639 - 1644.
39. Cavan DA Parkes A O'Donnell MJ Freeman W Cayton RM. Lung function and diabetes. Respir Med 1991 ; 85: 257 - 258.
40. Ofulue F Thurlbeck WM. Experimental diabetes and the lung. II. In vivo connective tissue metabolism. Am Rev Respir Dis 1988 ; 138: 284 - 289.
41. Lazarus R Sparrow D Weiss ST. Handgrip strength and insulin levels: cross-sectional and prospective associations in the Normative Aging study. Metabolism 1997: 46: 1266 - 1269.
42. 42 Guyton AC Hall TE. Physical principles of gas exchange, diffusion of oxygen and carbon dioxide through the respiratory membrane. In: AC Guyton JE Hall, (eds), Textbook of medical physiology. 2000 10th ed. Philadelphia: WB Saunders ; p. 452 - 462.
43. Incalzi R Fuso A Giordano A Pitocco D Maiolo C Calcagni ML. Neuroadrenergic denervation of the lung in type 1 diabetes mellitus complicated by autonomic neuropathy. Chest 2002 ; 121: 443 - 451.
44. Chang CT Liu FY Lin CC Wang TY Lee CC Kao A. Usefulness of technetium-99m hexanethylpropylene amine oxime lung scan to detect subclinical lung injury in patients with noninsulin-dependent diabetes mellitus. J Diabetes Complicat 2004 ; 18: 229 - 232.
45. Minette PH Buysschaert M Rahier J Veriter C Frans A. Pulmonary gas exchange in life-long nonsmoking patients with diabetes mellitus. Respiration 1999 ; 66: 20 - 24.
46. Guvener N Tutuncu BN Akcay S Eyuboglu F Gokcel A. Alveolar gas exchange in patients with type 2 diabetes mellitus. Endocr J 2003 ; 50: 663 - 667.
47. Guazzi M Oreglia I Guazzi MD. Insulin improves alveolar-capillary membrane gas conductance in type 2 diabetes. Diabetes Care 2002 ; 25: 1802 - 1806.
48. Weir DC Jennings PE Hendy MS Barnet AH Burge PS. Short reports transfer factor carbon monoxide in patients with and without microangiopathy. Thorax 1988 ; 43: 725 - 726.
49. Celik P Ozmen B Yorgancioglu A Ozmen D Cok G. Pulmonary function parameters in patients with diabetes mellitus. Turk J Endocr Metab 1999 ; 1: 5 - 10.
50. Britton J. Is the carbon monoxide transfer factor diminished in the presence of diabetic retinopathy in patients with insulin-dependent diabetes mellitus? Eur Respir J 1988 ; 1: 403 - 406.
51. Ozsahin K Tugrul A Mert S Yuksel M Tugrul G. Evaluation of pulmonary alveolo-capillary permeability in type 2 diabetes mellitus using technetium 99mTc-DTPA aerosol scintigraphy and carbon monoxide diffusion capacity. J Diabetes Complicat 2006 ; 20: 205 - 209.
52. Caner B Ugur O Bayraktar M Ulutuncel N Mentes T Telatar F. Impaired lung epithelial permeability in diabetics detected by technetium-99m-DTPA aerosol scintigraphy. J Nucl Med 1994 ; 35: 204 - 206.
53. Mousa K Onadeko BO Mohamed M. Technetium 99mTc-DTPA clearance in the evaluation of pulmonary involvement in patients with diabetes mellitus. Respir Med 2000 ; 94: 1053 - 1056.
54. Farina J Furio V Fernandez-Acenero MJ Muzas MA. Nodular fibrosis of the lung in diabetes mellitus. Virchows Arch. 1995 ; 427: 61 - 63.
55. Weynand B Jonckheere A Frans A Rahier J. Diabetes mellitus induces a thickening of the pulmonary basal lamina. Respiration 1999 ; 66: 14 - 19.
56. Watanabe K Senju S Toyoshima H Yoshida M. Thickness of the basement membrane of bronchial epithelial cells in lung diseases as determined by transbronchial biopsy. Respir Med 1997 ; 91: 406 - 410.
57. Plopper CG Morishige WK. Alterations in granular (type II) pneumocyte ultrastructure by streptozotocin-induced diabetes in the rat. Lab Invest 1978 ; 38: 143 - 148.
58. Popov D Simionescu M. Alterations of lung structure in experimental diabetes, and diabetes associated with hyperlipidaemia in hamsters. Eur Respir J 1997 ; 10: 1850 - 1858.
59. Heaton RW Guy RJ Gray BJ Watkins PJ Costello JF. Diminished bronchial reactivity to cold air in diabetic patients with autonomic neuropathy. BMJ 1984 ; 289: 149 - 151.
60. Santos e Fonseca CM Manco JC Gallo L Barreira AA Foss MC. Cholinergic bronchomotor tone and airway caliber in insulin-dependent diabetes mellitus. Chest 1992 ; 101: 1038 - 10343.
61. Nishimura M Miyamoto K Suzuki A Yamamoto H Tsuji M Kishi F. Ventilatory and heart responses to hypoxia and hypercapnia in patients with diabetes mellitus. Thorax 1989 ; 44: 251 - 257.
62. Weisbrod CJ Eastwood PR O'Driscoll GO Green DJ. Abnormal ventilatory responses to hypoxia in type 2 diabetes. Diabet Med 2005 ; 22: 563 - 568.
63. Tantucci C Scionti L Bottini P Dottorini ML Puxeddu E Casucci G. Influence of autonomic neuropathy of different severities on the hypercapnic drive to breathing in diabetic patients. Chest 1997 ; 112: 145 - 153.
64. Tantucci C Bottini P Fiorani C Dottorini ML Santeusanio F Provinciali L. Cerebrovascular reactivity and hypercapnic respiratory drive in diabetic autonomic neuropathy. J Appl Physiol 2001 ; 90: 889 - 896.
65. Tantucci C Bottini P Dottorini ML Puxeddu E Casucci G Scionti L. Ventilatory response to exercise in diabetic patients with autonomic neuropathy. J Appl Physiol 1996 ; 81: 1978 - 1986.
66. Scano G Filippelli M Romagnoli I Mancini M Misuri G Duranti R. Hypoxic and hypercapnic breathlessness in patients with diabetes mellitus. Chest 2000 ; 117: 960 - 967.
67. Barnes PJ. Neural control of human airways in health and disease. Am Rev Respir Dis 1986 ; 134: 1289 - 1314.
68. Yu Y Wang X Cui Y Fan Y Liu J Wang R. Abnormal modulation of cholinergic neurotransmission by endomorphin 1 and endomorphin 2 in isolated bronchus of type 1 diabetic rats. Peptides 2006 ; 27: 2770 - 2777.
69. Neidle A Manigault I Wajda IJ. Distribution of opiate-like substances in rat tissues. Neurochem Res 1979 ; 4: 399 - 410.
70. Stein C. The control of pain in peripheral tissues by opioids. New Engl J Med 1995 ; 332: 1685 - 1690.
71. Kuo HP Rohde JA Barnes PJ Rogers DF. Differential inhibitory effects of opioids on cigarette smoke, capsaicin and electrically-induced goblet cell secretion in guinea-pig. Br J Pharmacol 1992 ; 105: 361 - 366.
72. Misawa M Sato J Furukawa Y Chiba Y Hosokawa T. Abnormal modulation of cholinergic neurotransmission by opioid in hyperresponsive bronchus in rats. Gen Pharmacol 1996 ; 27: 441 - 444.
73. Antonelli Incalzi R Fuso L Giordano A Pitocco D Maicio C Calcagni ML. Neuroadrenergic denervation of the lung in type I diabetes mellitus complicated by autonomic neuropathy. Chest 2002 ; 121: 443 - 451.
74. Antonelli Incalzi R Fuso L Pitocco D Basso S Trove A Longobardi A. Decline of neuroadrenergic bronchial innervation and respiratory function in type 1 diabetes mellitus: a longitudinal study. Diabetes Metab Res Rev 2007 ; 23: 311 - 316.
75. Duchen LW Anjorin A Watkins PJ Mackay JD. Pathology of autonomic neuropathy in diabetes mellitus. Ann Intern Med 1980 ; 92: 301 - 303.
76. Koziel H Koziel MJ. Pulmonary complications of diabetes mellitus. Pneumonia. Infect Dis Clin North Am 1995 ; 9: 65 - 96.
77. Marvisi M Marani G Brianti M. Della, Porta, R. Pulmonary complications in diabetes mellitus. Recenti Prog Med 1996 ; 87: 623 - 627.
78. Ardigo D Valtuena S Zavaroni I Baroni MC Delsignore R. Pulmonary complications of diabetes mellitus: the role of glycemic control. Curr Drug Targets Inflamm Allergy 2004 ; 3: 455 - 458.
79. Wolff SP Dean RT. Glucose autoxidation and protein modification; potential role of autoxidative glycosylation in diabetes. Biochem J 1987 ; 245: 243 - 250.
80. Yan SD Schmidt AM Anderson GM Zhang J Brett J Zou YS. Enhanced cellular oxidant stress by the interaction of advanced glycation end products with their receptors/binding proteins. J Biol Chem 1994 ; 269: 9889 - 9897.
81. Abuja PM Albertini R. Methods for monitoring oxidative stress, lipid peroxidation and oxidation resistance of lipoproteins. Clin Chim Acta 2001 ; 306: 1 - 17.
82. Hensley K Williamson KS Floyd RA. Measurement of 3-nitrotyrosine and 5-nitro-gamma-tocopherol by high-performance liquid chromatography with electrochemical detection. Free Radic Biol Med 2000 ; 28: 520 - 528.
83. Radi R Beckman JS Bush KM Freeman BA. Peroxynitrite-induced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxide. Arch Biochem Biophys 1991 ; 288: 481 - 487.
84. Strain JJ. Disturbances of micronutrient and antioxidant status in diabetes. Proc Nutr Soc 1991 ; 50: 591 - 604.
85. Mc Lennan SV Hefferen S Wright L Rae C Fisher E Yue DK. Changes in hepatic glutathione metabolism in diabetes. Diabetes 1991 ; 40: 344 - 348.
86. Gumieniczek A Hopkala H Wojtowicz Z Wysocka M. Changes in antioxidant status of lung tissue in experimental diabetes in rabbits. Clin Biochem 2002 ; 35: 147 - 149.
87. Young IS Torney JJ Trimble ER. The effect of ascorbate supplementation on oxidative stress in the streptozotocin diabetic rat. Free Radic Biol Med 1992 ; 13: 41 - 46.
88. 88 Oztay F Kandil A Gurel E Ustunova S Kapucu A Balci H. The relationship between nitric oxide and leptin in the lung of rat with streptozotocin-induced diabetes. Cell Biochem Funct 2007 [Epub ahead of print].
89. Sridulyakul P Chakraphan D Bhattarakosol P Patumraj S. Endothelial nitric oxide synthase expression in systemic and pulmonary circulation of streptozotocin induced diabetic rats: comparison using image analysis. Clin Hemorheol Microcirc 2003 ; 29: 423 - 428.
90. Mehta S. The effects of nitric oxide in acute lung injury. Vascul Pharmacol 2005 ; 43: 390 - 403.
91. Speyer CL Neff TA Warner RL Guo RF Sarma JV Riedemann NC. Regulatory effects of iNOS on acute lung inflammatory responses in mice. Am J Pathol 2003 ; 163: 2319 - 2328.
92. McCloud LL Parkerson JB Zou L Rao RN Catravas JD. Reduced pulmonary endothelium-bound angiotensin converting enzyme activity in diabetic rabbits. Vascular Pharmcol 2005 ; 41: 159 - 165.