Nitric oxide levels in patients with diabetes mellitus: A systematic review and meta-analysis

Nitric Oxide - Biology and Chemistry

Volumn 61, Issue , 2016, Pages 1-9

  Assmann, Taís S ^a,b   Brondani, Letícia A ^a   Bouças, Ana P ^a   Rheinheimer, Jakeline ^a,b   de Souza, Bianca M ^a,b   Canani, Luís H ^a,b   Bauer, Andrea C ^a   Crispim, Daisy ^a,b  

^a HOSPITAL DE CLÍNICAS DE PORTO ALEGRE   (Brazil)

^b FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

Meta analysis; Nitric oxide levels and diabetes mellitus

Indexed keywords

NITRIC OXIDE;

ARTICLE; ASIAN; BLOOD LEVEL; DIABETIC PATIENT; EUROPEAN; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; NON INSULIN DEPENDENT DIABETES MELLITUS; PRIORITY JOURNAL; SYSTEMATIC REVIEW; ADOLESCENT; ADULT; BLOOD; CHILD; DIABETES MELLITUS; META ANALYSIS; YOUNG ADULT;

ADOLESCENT; ADULT; CHILD; DIABETES MELLITUS; HUMANS; NITRIC OXIDE; YOUNG ADULT;

EID: 84989339887     PISSN: 10898603     EISSN: 10898611     Source Type: Journal    
DOI: 10.1016/j.niox.2016.09.009     Document Type: Article

References (81)

1. [1] American Diabetes Association, Classification and diagnosis of diabetes. Diabetes Care, 38(S8-S16), 2015.
2. [2] American Diabetes Assocation, Diagnosis and classification of diabetes mellitus. Diabetes Care 35:Suppl 1 (2012), S64–S71.
3. [3] International Diabetes Federation. Epidemiology [Available from: www.idf.org].
4. [4] Pfeilschifter, J., Does nitric oxide, an inflammatory mediator of glomerular mesangial cells, have a role in diabetic nephropathy?. Kidney Int. 51 (1995), S50–S60.
5. [5] Avogaro, A., Albiero, M., Menegazzo, L., de Kreutzenberg, S., Fadini, G.P., Endothelial dysfunction in diabetes: the role of reparatory mechanisms. Diabetes Care 34:Suppl 2 (2011), S285–S290.
6. [6] Schmidt, H.H., Walter, U., NO at work. Cell 78:6 (1994), 919–925.
7. [7] Dellamea, B.S., Leitao, C.B., Friedman, R., Canani, L.H., Nitric oxide system and diabetic nephropathy. Diabetol. Metab. Syndr., 6(1), 2014, 17.
8. [8] Napoli, C., Ignarro, L.J., Nitric oxide and pathogenic mechanisms involved in the development of vascular diseases. Arch. Pharmacol. Res. 32:8 (2009), 1103–1108.
9. [9] Bredt, D.S., Snyder, S.H., Nitric oxide: a physiologic messenger molecule. Ann. Rev. Biochem. 63 (1994), 175–195.
10. [10] Caimi, G., Hopps, E., Montana, M., Noto, D., Canino, B., Lo Presti, R., et al. Evaluation of nitric oxide metabolites in a group of subjects with metabolic syndrome. Diabetes Metab. Syndr. 6:3 (2012), 132–135.
11. [11] Zou, M.H., Cohen, R., Ullrich, V., Peroxynitrite and vascular endothelial dysfunction in diabetes mellitus. Endothelium 11:2 (2004), 89–97.
12. [12] Pacher, P., Beckman, J.S., Liaudet, L., Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 87:1 (2007), 315–424.
13. [13] Brownlee, M., The pathobiology of diabetic complications: a unifying mechanism. Diabetes 54:6 (2005), 1615–1625.
14. [14] Pitocco, D., Zaccardi, F., Di Stasio, E., Romitelli, F., Santini, S.A., Zuppi, C., et al. Oxidative stress, nitric oxide, and diabetes. Rev. Diabet. Stud. 7:1 (2010), 15–25.
15. [15] Beckman, J.S., Crow, J.P., Pathological implications of nitric oxide, superoxide and peroxynitrite formation. Biochem. Soc. Trans. 21:2 (1993), 330–334.
16. [16] Honing, M.L., Morrison, P.J., Banga, J.D., Stroes, E.S., Rabelink, T.J., Nitric oxide availability in diabetes mellitus. Diabetes Metab. Rev. 14:3 (1998), 241–249.
17. [17] Förstermann, U., Nitric oxide and oxidative stress in vascular disease. Pflugers Arch. 459:6 (2010), 923–939.
18. [18] Adela, R., Nethi, S.K., Bagul, P.K., Barui, A.K., Mattapally, S., Kuncha, M., et al. Hyperglycaemia enhances nitric oxide production in diabetes: a study from South Indian patients. PLoS One, 10(4), 2015, e0125270.
19. [19] Aydin, A., Orhan, H., Sayal, A., Ozata, M., Sahin, G., Işimer, A., Oxidative stress and nitric oxide related parameters in type II diabetes mellitus: effects of glycemic control. Clin. Biochem. 34:1 (2001), 65–70.
20. [20] Hoeldtke, R.D., Bryner, K.D., McNeill, D.R., Warehime, S.S., Van Dyke, K., Hobbs, G., Oxidative stress and insulin requirements in patients with recent-onset type 1 diabetes. J. Clin. Endocrinol. Metab. 88:4 (2003), 1624–1628.
21. [21] Mylona-Karayanni, C., Gourgiotis, D., Bossios, A., Kamper, E.F., Oxidative stress and adhesion molecules in children with type 1 diabetes mellitus: a possible link. Pediatr. Diabetes 7:1 (2006), 51–59.
22. [22] Pitocco, D., Zaccardi, F., Di Stasio, E., Romitelli, F., Martini, F., Scaglione, G.L., et al. Role of asymmetric-dimethyl-L-arginine (ADMA) and nitrite/nitrate (NOx) in the pathogenesis of oxidative stress in female subjects with uncomplicated type 1 diabetes mellitus. Diabetes Res. Clin. Pract. 86:3 (2009), 173–176.
23. [23] Daimon, M., Sugiyama, K., Saitoh, T., Yamaguchi, H., Hirata, A., Ohnuma, H., et al. Increase in serum ceruloplasmin levels is correlated with a decrease of serum nitric oxide levels in type 2 diabetes. Diabetes Care 23:4 (2000), 559–560.
24. [24] Krause, M., Rodrigues-Krause, J., O'Hagan, C., De Vito, G., Boreham, C., Susta, D., et al. Differential nitric oxide levels in the blood and skeletal muscle of type 2 diabetic subjects may be consequence of adiposity: a preliminary study. Metab. Clin. Exp. 61:11 (2012), 1528–1537.
25. [25] Shiekh, G.A., Ayub, T., Khan, S.N., Dar, R., Andrabi, K.I., Reduced nitrate level in individuals with hypertension and diabetes. J. Cardiovasc Dis. Res. 2:3 (2011), 172–176.
26. [26] Bender, S.B., Herrick, E.K., Lott, N.D., Klabunde, R.E., Diet-induced obesity and diabetes reduce coronary responses to nitric oxide due to reduced bioavailability in isolated mouse hearts. Diabetes Obes. Metab. 9:5 (2007), 688–696.
27. [27] Kim, F., Pham, M., Maloney, E., Rizzo, N.O., Morton, G.J., Wisse, B.E., et al. Vascular inflammation, insulin resistance, and reduced nitric oxide production precede the onset of peripheral insulin resistance. Arterioscler. Thromb. Vasc. Biol. 28:11 (2008), 1982–1988.
28. [28] Tatsch, E., Bochi, G.V., Piva, S.J., De Carvalho, J.A., Kober, H., Torbitz, V.D., et al. Association between DNA strand breakage and oxidative, inflammatory and endothelial biomarkers in type 2 diabetes. Mutat. Res. 732:1–2 (2012), 16–20.
29. [29] Moher, D., Liberati, A., Tetzlaff, J., Altman, D.G., Group, P., Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J. Clin. Epidemiol. 62:10 (2009), 1006–1012.
30. [30] Stroup, D.F., Berlin, J.A., Morton, S.C., Olkin, I., Williamson, G.D., Rennie, D., et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of Observational Studies in Epidemiology (MOOSE) group. JAMA 283:15 (2000), 2008–2012.
31. [31] de Souza, B.M., Brondani, L.A., Boucas, A.P., Sortica, D.A., Kramer, C.K., Canani, L.H., et al. Associations between UCP1 -3826A/G, UCP2 -866G/A, Ala55Val and Ins/Del, and UCP3 -55C/T polymorphisms and susceptibility to type 2 diabetes mellitus: case-control study and meta-analysis. PLoS One, 8(1), 2013, e54259.
32. [32] Brondani, L.A., Assmann, T.S., de Souza, B.M., Boucas, A.P., Canani, L.H., Crispim, D., Meta-analysis reveals the association of common variants in the uncoupling protein (UCP) 1-3 genes with body mass index variability. PLoS One, 9(5), 2014, e96411.
33. [33] Sortica, D.A., Buffon, M.P., Souza, B.M., Nicoletto, B.B., Santer, A., Assmann, T.S., et al. Association between the ENPP1 K121Q polymorphism and risk of diabetic kidney disease: a systematic review and meta-analysis. PLoS One, 10(3), 2015, e0118416.
34. [34] Stang, A., Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur. J. Epidemiol. 25:9 (2010), 603–605.
35. [35] Higgins, J.P., Thompson, S.G., Quantifying heterogeneity in a meta-analysis. Stat. Med. 21:11 (2002), 1539–1558.
36. [36] Higgins, J.P., Thompson, S.G., Deeks, J.J., Altman, D.G., Measuring inconsistency in meta-analyses. BMJ 327:7414 (2003), 557–560.
37. [37] Egger, M., Davey Smith, G., Schneider, M., Minder, C., Bias in meta-analysis detected by a simple, graphical test. BMJ 315:7109 (1997), 629–634.
38. [38] Milsom, A.B., Jones, C.J., Goodfellow, J., Frenneaux, M.P., Peters, J.R., James, P.E., Abnormal metabolic fate of nitric oxide in Type I diabetes mellitus. Diabetologia 45:11 (2002), 1515–1522.
39. [39] Savino, A., Pelliccia, P., Schiavone, C., Primavera, A., Tumini, S., Mohn, A., et al. Serum and urinary nitrites and nitrates and Doppler sonography in children with diabetes. Diabetes Care 29:12 (2006), 2676–2681.
40. [40] Ferlito, S., Gallina, M., Nitrite plasma levels in type 1 and 2 diabetics with and without complications. Panminerva Med. 40:4 (1998), 304–308.
41. [41] Chiarelli, F., Cipollone, F., Romano, F., Tumini, S., Costantini, F., di Ricco, L., et al. Increased circulating nitric oxide in young patients with type 1 diabetes and persistent microalbuminuria: relation to glomerular hyperfiltration. Diabetes 49:7 (2000), 1258–1263.
42. [42] Hoeldtke, R.D., Bryner, K.D., McNeill, D.R., Hobbs, G.R., Riggs, J.E., Warehime, S.S., et al. Nitrosative stress, uric Acid, and peripheral nerve function in early type 1 diabetes. Diabetes 51:9 (2002), 2817–2825.
43. [43] Catalano, M., Carzaniga, G., Perilli, E., Jun, T., Scandale, G., Andreoni, S., et al. Basal nitric oxide production is not reduced in patients with noninsulin-dependent diabetes mellitus. Vasc. Med. 2:4 (1997), 302–305.
44. [44] Maejima, K., Nakano, S., Himeno, M., Tsuda, S., Makiishi, H., Ito, T., et al. Increased basal levels of plasma nitric oxide in Type 2 diabetic subjects. Relationship to microvascular complications. J. Diabetes Complicat. 15:3 (2001), 135–143.
45. [45] Doganay, S., Evereklioglu, C., Er, H., Türköz, Y., Sevinç, A., Mehmet, N., et al. Comparison of serum NO, TNF-alpha, IL-1beta, sIL-2R, IL-6 and IL-8 levels with grades of retinopathy in patients with diabetes mellitus. Eye (Lond) 16:2 (2002), 163–170.
46. [46] Izumi, N., Nagaoka, T., Mori, F., Sato, E., Takahashi, A., Yoshida, A., Relation between plasma nitric oxide levels and diabetic retinopathy. Jpn. J. Ophthalmol. 50:5 (2006), 465–468.
47. [47] Guerra, A.F.R., Ayala, G.V., Nuevo, J.J.L., López, L.R., Brizuela, L.M.R., Correlación entre la concentración de nitritos y albuminuria en pacientescon diabetes tipo 2 normotensos e hipertensos. Med. Int. Mex. 24 (2008), 329–333.
48. [48] Nunes, S.F., Figueiredo, I.V., Soares, P.J., Costa, N.E., Lopes, M.C., Caramona, M.M., Semicarbazide-sensitive amine oxidase activity and total nitrite and nitrate concentrations in serum: novel biochemical markers for type 2 diabetes?. Acta Diabetol. 46:2 (2009), 135–140.
49. [49] Ghosh, A., Sherpa, M.L., Bhutia, Y., Pal, R., Dahal, S., Serum nitric oxide status in patients with type 2 diabetes mellitus in Sikkim. Int. J. Appl. Basic Med. Res. 1:1 (2011), 31–35.
50. [50] Chien, W.Y., Yang, K.D., Eng, H.L., Hu, Y.H., Lee, P.Y., Wang, S.T., et al. Increased plasma concentration of nitric oxide in type 2 diabetes but not in nondiabetic individuals with insulin resistance. Diabetes Metab. 31:1 (2005), 63–68.
51. [51] Ouvina, S.M., La Greca, R.D., Zanaro, N.L., Palmer, L., Sassetti, B., Endothelial dysfunction, nitric oxide and platelet activation in hypertensive and diabetic type II patients. Thromb. Res. 102:2 (2001), 107–114.
52. [52] Vanizor, B., Orem, A., Karahan, S.C., Kiran, E., Erem, C., Aliyazicioglu, R., et al. Decreased nitric oxide end-products and its relationship with high density lipoprotein and oxidative stress in people with type 2 diabetes without complications. Diabetes Res. Clin. Pract. 54:1 (2001), 33–39.
53. [53] Abou-Seif, M.A., Youssef, A.A., Evaluation of some biochemical changes in diabetic patients. Clin. Chim. Acta 346:2 (2004), 161–170.
54. [54] Pereira, F.O., Frode, T.S., Medeiros, Y.S., Evaluation of tumour necrosis factor alpha, interleukin-2 soluble receptor, nitric oxide metabolites, and lipids as inflammatory markers in type 2 diabetes mellitus. Mediat. Inflamm., 2006(1), 2006, 39062.
55. [55] Apakkan Aksun, S., Ozmen, B., Ozmen, D., Parildar, Z., Senol, B., Habif, S., et al. Serum and urinary nitric oxide in Type 2 diabetes with or without microalbuminuria: relation to glomerular hyperfiltration. J. Diabetes Complicat. 17:6 (2003), 343–348.
56. [56] Zahedi Asl, S., Ghasemi, A., Azizi, F., Serum nitric oxide metabolites in subjects with metabolic syndrome. Clin. Biochem. 41:16–17 (2008), 1342–1347.
57. [57] Ghasemi, A., Zahediasl, S., Azizi, F., Reference values for serum nitric oxide metabolites in an adult population. Clin. Biochem. 43:1–2 (2010), 89–94.
58. [58] Lau, J., Ioannidis, J.P., Terrin, N., Schmid, C.H., Olkin, I., The case of the misleading funnel plot. BMJ 333:7568 (2006), 597–600.
59. [59] Yang, P., Cao, Y., Li, H., Hyperglycemia induces inducible nitric oxide synthase gene expression and consequent nitrosative stress via c-Jun N-terminal kinase activation. Am. J. Obstet. Gynecol., 203(2), 2010, 185 e5-11.
60. [60] Zhang, X., Fu, Y., Xu, X., Li, M., Du, L., Han, Y., et al. PERK pathway are involved in NO-induced apoptosis in endothelial cells cocultured with RPE under high glucose conditions. Nitric oxide 40 (2014), 10–16.
61. [61] Cai, S., Khoo, J., Channon, K.M., Augmented BH4 by gene transfer restores nitric oxide synthase function in hyperglycemic human endothelial cells. Cardiovasc Res. 65:4 (2005), 823–831.
62. [62] Shahid, S.M., Mahboob, T., Correlation between glycosylated hemoglobin (HbA1c) and serum nitrite oxide (NO). Aust. J. Basic Appl. Sci. 3 (2009), 1323–1327.
63. [63] Ishii, N., Patel, K.P., Lane, P.H., Taylor, T., Bian, K., Murad, F., et al. Nitric oxide synthesis and oxidative stress in the renal cortex of rats with diabetes mellitus. J. Am. Soc. Nephrol. 12:8 (2001), 1630–1639.
64. [64] Cosentino, F., Hishikawa, K., Katusic, Z.S., Luscher, T.F., High glucose increases nitric oxide synthase expression and superoxide anion generation in human aortic endothelial cells. Circulation 96:1 (1997), 25–28.
65. [65] Duplain, H., Burcelin, R., Sartori, C., Cook, S., Egli, M., Lepori, M., et al. Insulin resistance, hyperlipidemia, and hypertension in mice lacking endothelial nitric oxide synthase. Circulation 104:3 (2001), 342–345.
66. [66] Shankar, R.R., Wu, Y., Shen, H.Q., Zhu, J.S., Baron, A.D., Mice with gene disruption of both endothelial and neuronal nitric oxide synthase exhibit insulin resistance. Diabetes 49:5 (2000), 684–687.
67. [67] Kapur, S., Bedard, S., Marcotte, B., Cote, C.H., Marette, A., Expression of nitric oxide synthase in skeletal muscle: a novel role for nitric oxide as a modulator of insulin action. Diabetes 46:11 (1997), 1691–1700.
68. [68] Perreault, M., Marette, A., Targeted disruption of inducible nitric oxide synthase protects against obesity-linked insulin resistance in muscle. Nat. Med. 7:10 (2001), 1138–1143.
69. [69] Tsuchiya, K., Sakai, H., Suzuki, N., Iwashima, F., Yoshimoto, T., Shichiri, M., et al. Chronic blockade of nitric oxide synthesis reduces adiposity and improves insulin resistance in high fat-induced obese mice. Endocrinol 148:10 (2007), 4548–4556.
70. [70] Noronha, B.T., Li, J.M., Wheatcroft, S.B., Shah, A.M., Kearney, M.T., Inducible nitric oxide synthase has divergent effects on vascular and metabolic function in obesity. Diabetes 54:4 (2005), 1082–1089.
71. [71] Cha, H.N., Kim, Y.W., Kim, J.Y., Kim, Y.D., Song, I.H., Min, K.N., et al. Lack of inducible nitric oxide synthase does not prevent aging-associated insulin resistance. Exp. Geront 45:9 (2010), 711–718.
72. [72] Kurohane Kaneko, Y., Ishikawa, T., Dual role of nitric oxide in pancreatic beta-cells. J. Pharmacol. Sci. 123:4 (2013), 295–300.
73. [73] Smukler, S.R., Tang, L., Wheeler, M.B., Salapatek, A.M., Exogenous nitric oxide and endogenous glucose-stimulated beta-cell nitric oxide augment insulin release. Diabetes 51:12 (2002), 3450–3460.
74. [74] Eizirik, D.L., Flodstrom, M., Karlsen, A.E., Welsh, N., The harmony of the spheres: inducible nitric oxide synthase and related genes in pancreatic beta cells. Diabetologia 39:8 (1996), 875–890.
75. [75] Wu, G., Nitric oxide synthesis and the effect of aminoguanidine and NG-monomethyl-L-arginine on the onset of diabetes in the spontaneously diabetic BB rat. Diabetes 44:3 (1995), 360–364.
76. [76] Cnop, M., Welsh, N., Jonas, J.C., Jorns, A., Lenzen, S., Eizirik, D.L., Mechanisms of pancreatic beta-cell death in type 1 and type 2 diabetes: many differences, few similarities. Diabetes 54:Suppl 2 (2005), S97–S107.
77. [77] Flodstrom, M., Tyrberg, B., Eizirik, D.L., Sandler, S., Reduced sensitivity of inducible nitric oxide synthase-deficient mice to multiple low-dose streptozotocin-induced diabetes. Diabetes 48:4 (1999), 706–713.
78. [78] Takamura, T., Kato, I., Kimura, N., Nakazawa, T., Yonekura, H., Takasawa, S., et al. Transgenic mice overexpressing type 2 nitric-oxide synthase in pancreatic beta cells develop insulin-dependent diabetes without insulitis. J. Biol. Chem. 273:5 (1998), 2493–2496.
79. [79] Mata-Greenwood, E., Chen, D.B., Racial differences in nitric oxide-dependent vasorelaxation. Reprod. Sci. 15:1 (2008), 9–25.
80. [80] Cantu-Medellin, N., Kelley, E.E., Xanthine oxidoreductase-catalyzed reduction of nitrite to nitric oxide: insights regarding where, when and how. Nitric oxide 34 (2013), 19–26.
81. [81] Battelli, M.G., Polito, L., Bolognesi, A., Xanthine oxidoreductase in atherosclerosis pathogenesis: not only oxidative stress. Atherosclerosis 237:2 (2014), 562–567.