Top

22-01-2018 | Hypertension | Review | Article

Hypertension with diabetes mellitus complications

Journal: Hypertension Research

Authors: Daisuke Yamazaki, Hirofumi Hitomi, Akira Nishiyama

Publisher: Nature Publishing Group UK

Abstract

Chronic diabetic complications are classified as microvascular or macrovascular and contribute to mortality and loss of quality of life. Hyperglycemia plays a critical role in the pathogenesis of microvascular complications, such as diabetic retinopathy, incipient nephropathy, and neuropathy, while atherosclerosis contributes to the pathogenesis of macrovascular complications. Diabetes mellitus and hypertension are frequently present together. Among many microvascular diabetic complications, hypertension plays a predominant role in the progression of diabetic nephropathy by glomerular hyperfiltration. Hypertension also induces atherosclerosis in diabetes. Thus, hypertension is a high-risk factor for both microvascular and macrovascular chronic diabetic complications. In this review, we summarize the current knowledge on the pathophysiological mechanisms of microvascular and macrovascular chronic diabetic complications with particular emphasis on the contribution of hypertension. We also briefly discuss various options available for the treatment of each diabetic complication.

Koopmanschap M, Code- Advisory Board. Coping with type II diabetes: the patient’s perspective. Diabetologia. 2002;45:S18–22.CrossRefPubMed

Morrish NJ, Wang SL, Stevens LK, Fuller JH, Keen H. Mortality and causes of death in the WHO multinational study of vascular disease in diabetes. Diabetologia. 2001;44:S14–21.CrossRefPubMed

Zoungas S, Woodward M, Li Q, Cooper ME, Hamet P, Harrap S, Heller S, Marre M, Patel A, Poulter N, Williams B, Chalmers J, Advance Collaborative group. Impact of age, age at diagnosis and duration of diabetes on the risk of macrovascular and microvascular complications and death in type 2 diabetes. Diabetologia. 2014;57:2465–74.CrossRefPubMed

Diabetes Control and Complications Trial Research Group, Nathan DM, Genuth S, Lachin J, Cleary P, Crofford O, Davis M, Rand L, Siebert C. 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;329:977–86.CrossRef

UK Prospective Diabetes Study Group. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). Lancet. 1998;352:837–53.

Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes. 2005;54:1615–25.CrossRefPubMed

UK Prospective Diabetes Study Group. Tight blood pressure control and risk of macrovascular and microvascular complications in type 2 diabetes: UKPDS 38. BMJ. 1998;317:703–13.

American Diabetes Association. Role of cardiovascular risk factors in prevention and treatment of macrovascular disease in diabetes. Diabetes Care. 1989;12:573–9.

Reaven GM, Lithell H, Landsberg L. Hypertension and associated metabolic abnormalities -the role of insulin resistance and the sympathoadrenal system. N Engl J Med. 1996;334:374–81.CrossRefPubMed

10.

Horita S, Seki G, Yamada H, Suzuki M, Koike K, Fujita T. Insulin resistance, obesity, hypertension, and renal sodium transport. Int J Hypertens. 2011;2011:391762.CrossRefPubMedPubMedCentral

11.

Klein R, Klein BE, Moss SE, Davis MD, DeMets DL. Is blood pressure a predictor of the incidence or progression of diabetic retinopathy? Arch Intern Med. 1989;149:2427–32.CrossRefPubMed

12.

Gupta N, Mansoor S, Sharma A, Sapkal A, Sheth J, Falatoonzadeh P, Kuppermann B, Kenney M. Diabetic retinopathy and VEGF. Open Ophthalmol J. 2013;7:4–10.CrossRefPubMedPubMedCentral

13.

Pe’er J, Folberg R, Itin A, Gnessin H, Hemo I, Keshet E. Upregulated expression of vascular endothelial growth factor in proliferative diabetic retinopathy. Br J Ophthalmol. 1996;80:241–5.CrossRefPubMedPubMedCentral

14.

Pierce EA, Avery RL, Foley ED, Aiello LP, Smith LE. Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization. Proc Natl Acad Sci USA. 1995;92:905–9.CrossRefPubMedPubMedCentral

15.

Brown DM, Nguyen QD, Marcus DM, Boyer DS, Patel S, Feiner L, Schlottmann PG, Rundle AC, Zhang J, Rubio RG, Adamis AP, Ehrlich JS, Hopkins JJ, Ride, RIDE and RISE Research Group. Long-term outcomes of ranibizumab therapy for diabetic macular edema: the 36-month results from two phase III trials: RISE and RIDE. Ophthalmology. 2013;120:2013–22.CrossRefPubMed

16.

Srivastava BK, Rema M. Does hypertension play a role in diabetic retinopathy? J Assoc Physicians India. 2005;53:803–8.PubMed

17.

Kohner EM, Patel V, Rassam SM. Role of blood flow and impaired autoregulation in the pathogenesis of diabetic retinopathy. Diabetes. 1995;44:603–7.CrossRefPubMed

18.

de la Rubia G, Oliver FJ, Inoguchi T, King GL. Induction of resistance to endothelin-1’s biochemical actions by elevated glucose levels in retinal pericytes. Diabetes. 1992;41:1533–9.CrossRefPubMed

19.

Suzuma I, Hata Y, Clermont A, Pokras F, Rook SL, Suzuma K, Feener EP, Aiello LP. Cyclic stretch and hypertension induce retinal expression of vascular endothelial growth factor and vascular endothelial growth factor receptor-2: potential mechanisms for exacerbation of diabetic retinopathy by hypertension. Diabetes. 2001;50:444–54.CrossRefPubMed

20.

Aiello LP, Cahill MT, Wong JS. Systemic considerations in the management of diabetic retinopathy. Am J Ophthalmol. 2001;132:760–76.CrossRefPubMed

21.

Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group, Lachin JM, Genuth S, Cleary P, Davis MD, Nathan DM. Retinopathy and nephropathy in patients with type 1 diabetes four years after a trial of intensive therapy. N Engl J Med. 2000;342:381–9.CrossRef

22.

Ohkubo Y, Kishikawa H, Araki E, Miyata T, Isami S, Motoyoshi S, Kojima Y, Furuyoshi N, Shichiri M. Intensive insulin therapy prevents the progression of diabetic microvascular complications in Japanese patients with non-insulin-dependent diabetes mellitus: a randomized prospective 6-year study. Diabetes Res Clin Pract. 1995;28:103–17.CrossRefPubMed

23.

The Diabetes Control and Complications Trial Research Group. Early worsening of diabetic retinopathy in the Diabetes Control and Complications Trial. Arch Ophthalmol. 1998;116:874–86.

24.

Estacio RO, Jeffers BW, Gifford N, Schrier RW. Effect of blood pressure control on diabetic microvascular complications in patients with hypertension and type 2 diabetes. Diabetes Care. 2000;23:B54–64.PubMed

25.

Do DV, Wang X, Vedula SS, Marrone M, Sleilati G, Hawkins BS, Frank RN. Blood pressure control for diabetic retinopathy. Cochrane Database Syst Rev. 2015;1:CD006127.PubMedPubMedCentral

26.

Chaturvedi N, Sjolie AK, Stephenson JM, Abrahamian H, Keipes M, Castellarin A, Rogulja-Pepeonik Z, Fuller JH. Effect of lisinopril on progression of retinopathy in normotensive people with type 1 diabetes. The EUCLID Study Group. EURODIAB controlled trial of lisinopril in insulin-dependent diabetes mellitus. Lancet. 1998;351:28–31.CrossRefPubMed

27.

Matthews DR, Stratton IM, Aldington SJ, Holman RR, Kohner EM, UKPDS group. Risks of progression of retinopathy and vision loss related to tight blood pressure control in type 2 diabetes mellitus: UKPDS 69. Arch Ophthalmol. 2004;122:1631–40.CrossRefPubMed

28.

Chaturvedi N, Porta M, Klein R, Orchard T, Fuller J, Parving HH, Bilous R, Sjolie AK, Direct Programme Study Group. Effect of candesartan on prevention (DIRECT-Prevent 1) and progression (DIRECT-Protect 1) of retinopathy in type 1 diabetes: randomised, placebo-controlled trials. Lancet. 2008;372:1394–402.CrossRefPubMed

29.

Sjolie AK, Klein R, Porta M, Orchard T, Fuller J, Parving HH, Bilous R, Chaturvedi N, Direct Programme Study Group. Effect of candesartan on progression and regression of retinopathy in type 2 diabetes (DIRECT-Protect 2): a randomised placebo-controlled trial. Lancet. 2008;372:1385–93.CrossRefPubMed

30.

Keech AC, Mitchell P, Summanen PA, O’Day J, Davis TM, Moffitt MS, Taskinen MR, Simes RJ, Tse D, Williamson E, Merrifield A, Laatikainen LT, d’Emden MC, Crimet DC, O’Connell RL, Colman PG, Field study investigators. Effect of fenofibrate on the need for laser treatment for diabetic retinopathy (FIELD study): a randomised controlled trial. Lancet. 2007;370:1687–97.CrossRefPubMed

31.

Gross JL, de Azevedo MJ, Silveiro SP, Canani LH, Caramori ML, Zelmanovitz T. Diabetic nephropathy: diagnosis, prevention, and treatment. Diabetes Care. 2005;28:164–76.CrossRefPubMed

32.

Stehouwer CD, Smulders YM. Microalbuminuria and risk for cardiovascular disease: Analysis of potential mechanisms. J Am Soc Nephrol. 2006;17:2106–11.CrossRefPubMed

33.

Dahlquist G, Stattin EL, Rudberg S. Urinary albumin excretion rate and glomerular filtration rate in the prediction of diabetic nephropathy; a long-term follow-up study of childhood onset type-1 diabetic patients. Nephrol Dial Transplant. 2001;16:1382–86.CrossRefPubMed

34.

Ravid M, Brosh D, Ravid-Safran D, Levy Z, Rachmani R. Main risk factors for nephropathy in type 2 diabetes mellitus are plasma cholesterol levels, mean blood pressure, and hyperglycemia. Arch Intern Med. 1998;158:998–1004.CrossRefPubMed

35.

Ohkuma T, Nakamura U, Iwase M, Ide H, Fujii H, Jodai T, Kaizu S, Kikuchi Y, Idewaki Y, Sumi A, Hirakawa Y, Kitazono T. Effects of smoking and its cessation on creatinine- and cystatin C-based estimated glomerular filtration rates and albuminuria in male patients with type 2 diabetes mellitus: the Fukuoka Diabetes Registry. Hypertens Res. 2016;39:744–51.CrossRefPubMed

36.

Helal I, Fick-Brosnahan GM, Reed-Gitomer B, Schrier RW. Glomerular hyperfiltration: definitions, mechanisms and clinical implications. Nat Rev Nephrol. 2012;8:293–300.CrossRefPubMed

37.

Thomson SC, Vallon V, Blantz RC. Kidney function in early diabetes: the tubular hypothesis of glomerular filtration. Am J Physiol Ren Physiol. 2004;286:F8–15.CrossRef

38.

Hostetter TH, Rennke HG, Brenner BM. The case for intrarenal hypertension in the initiation and progression of diabetic and other glomerulopathies. Am J Med. 1982;72:375–80.CrossRefPubMed

39.

Yasuda T, Kondo S, Homma T, Harris RC. Regulation of extracellular matrix by mechanical stress in rat glomerular mesangial cells. J Clin Invest. 1996;98:1991–2000.CrossRefPubMedPubMedCentral

40.

Arima S, Ito S. The mechanisms underlying altered vascular resistance of glomerular afferent and efferent arterioles in diabetic nephropathy. Nephrol Dial Transplant. 2003;18:1966–9.CrossRefPubMed

41.

Mbanya JC, Thomas TH, Taylor R, Alberti KG, Wilkinson R. Increased proximal tubular sodium reabsorption in hypertensive patients with type 2 diabetes. Diabet Med. 1989;6:614–20.CrossRefPubMed

42.

Vallon V, Richter K, Blantz RC, Thomson S, Osswald H. Glomerular hyperfiltration in experimental diabetes mellitus: potential role of tubular reabsorption. J Am Soc Nephrol. 1999;10:2569–76.PubMed

43.

Thomson SC, Rieg T, Miracle C, Mansoury H, Whaley J, Vallon V, Singh P. Acute and chronic effects of SGLT2 blockade on glomerular and tubular function in the early diabetic rat. Am J Physiol Regul Integr Comp Physiol. 2012;302:R75–83.CrossRefPubMed

44.

Van Buren PN, Toto R. Hypertension in diabetic nephropathy: epidemiology, mechanisms, and management. Adv Chronic Kidney Dis. 2011;18:28–41.CrossRefPubMedPubMedCentral

45.

Nielsen FS, Hansen HP, Jacobsen P, Rossing P, Smidt UM, Christensen NJ, Pevet P, Vivien-Roels B, Parving HH. Increased sympathetic activity during sleep and nocturnal hypertension in Type 2 diabetic patients with diabetic nephropathy. Diabet Med. 1999;16:555–62.CrossRefPubMed

46.

Prabhakar S, Starnes J, Shi S, Lonis B, Tran R. Diabetic nephropathy is associated with oxidative stress and decreased renal nitric oxide production. J Am Soc Nephrol. 2007;18:2945–52.CrossRefPubMed

47.

Advance Collaborative Group, Patel A, MacMahon S, Chalmers J, Neal B, Billot L, Woodward M, Marre M, Cooper M, Glasziou P, Grobbee D, Hamet P, Harrap S, Heller S, Liu L, Mancia G, Mogensen CE, Pan C, Poulter N, Rodgers A, Williams B, Bompoint S, de Galan BE, Joshi R, Travert F. Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes. N Engl J Med. 2008;358:2560–72.CrossRef

48.

Writing Team for the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group. Sustained effect of intensive treatment of type 1 diabetes mellitus on development and progression of diabetic nephropathy: the Epidemiology of Diabetes Interventions and Complications (EDIC) study. JAMA. 2003;290:2159–67.CrossRef

49.

Fioretto P, Steffes MW, Sutherland DE, Goetz FC, Mauer M. Reversal of lesions of diabetic nephropathy after pancreas transplantation. N Engl J Med. 1998;339:69–75.CrossRefPubMed

50.

Heart Outcomes Prevention Evaluation (HOPE) Study Investigators. Effects of ramipril on cardiovascular and microvascular outcomes in people with diabetes mellitus: results of the HOPE study and MICRO-HOPE substudy. Lancet. 2000;355:253–9.

51.

Viberti G, Wheeldon NM, MicroAlbuminuria Reduction With VALsartan (MARVAL) Study Investigators. . Microalbuminuria reduction with valsartan in patients with type 2 diabetes mellitus: a blood pressure-independent effect. Circulation. 2002;106:672–8.CrossRefPubMed

52.

Makino H, Haneda M, Babazono T, Moriya T, Ito S, Iwamoto Y, Kawamori R, Takeuchi M, Katayama S, Innovation Study Group. Prevention of transition from incipient to overt nephropathy with telmisartan in patients with type 2 diabetes. Diabetes Care. 2007;30:1577–8.CrossRefPubMed

53.

Bakris GL, Williams M, Dworkin L, Elliott WJ, Epstein M, Toto R, Tuttle K, Douglas J, Hsueh W, Sowers J. Preserving renal function in adults with hypertension and diabetes: a consensus approach. National Kidney Foundation Hypertension and Diabetes Executive Committees Working Group. Am J Kidney Dis. 2000;36:646–61.CrossRefPubMed

54.

Shimamoto K, Ando K, Fujita T, Hasebe N, Higaki J, Horiuchi M, Imai Y, Imaizumi T, Ishimitsu T, Ito M, Ito S, Itoh H, Iwao H, Kai H, Kario K, Kashihara N, Kawano Y, Kim-Mitsuyama S, Kimura G, Kohara K, Komuro I, Kumagai H, Matsuura H, Miura K, Morishita R, Naruse M, Node K, Ohya Y, Rakugi H, Saito I, Saitoh S, Shimada K, Shimosawa T, Suzuki H, Tamura K, Tanahashi N, Tsuchihashi T, Uchiyama M, Ueda S, Umemura S, Japanese Society of Hypertension Committee for Guidelines for the Management of H. . The Japanese Society of Hypertension Guidelines for the Management of Hypertension (JSH 2014). Hypertens Res. 2014;37:253–390.CrossRefPubMed

55.

Accord Study Group, Cushman WC, Evans GW, Byington RP, Goff DC Jr., Grimm RH Jr., Cutler JA, Simons-Morton DG, Basile JN, Corson MA, Probstfield JL, Katz L, Peterson KA, Friedewald WT, Buse JB, Bigger JT, Gerstein HC, Ismail-Beigi F. Effects of intensive blood-pressure control in type 2 diabetes mellitus. N Engl J Med. 2010;362:1575–85.CrossRef

56.

Brenner BM, Cooper ME, de Zeeuw D, Keane WF, Mitch WE, Parving HH, Remuzzi G, Snapinn SM, Zhang Z, Shahinfar S, Renaal Study Investigators. . Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy. N Engl J Med. 2001;345:861–9.CrossRefPubMed

57.

Lewis EJ, Hunsicker LG, Clarke WR, Berl T, Pohl MA, Lewis JB, Ritz E, Atkins RC, Rohde R, Raz I, Collaborative Study Group. Renoprotective effect of the angiotensin-receptor antagonist irbesartan in patients with nephropathy due to type 2 diabetes. N Engl J Med. 2001;345:851–60.CrossRefPubMed

58.

Imai E, Ito S, Haneda M, Chan JC, Makino H, Orient Investigators. Olmesartan reducing incidence of endstage renal disease in diabetic nephropathy trial (ORIENT): rationale and study design. Hypertens Res. 2006;29:703–9.CrossRefPubMed

59.

Imai E, Chan JC, Ito S, Yamasaki T, Kobayashi F, Haneda M, Makino H, Orient study investigators. Effects of olmesartan on renal and cardiovascular outcomes in type 2 diabetes with overt nephropathy: a multicentre, randomised, placebo-controlled study. Diabetologia. 2011;54:2978–86.CrossRefPubMedPubMedCentral

60.

Strippoli GF, Bonifati C, Craig M, Navaneethan SD, Craig JC. Angiotensin converting enzyme inhibitors and angiotensin II receptor antagonists for preventing the progression of diabetic kidney disease. Cochrane Database Syst Rev. 2006, Issue 4. Art. No.: CD006257.

61.

Parving HH, Brenner BM, McMurray JJ, de Zeeuw D, Haffner SM, Solomon SD, Chaturvedi N, Persson F, Desai AS, Nicolaides M, Richard A, Xiang Z, Brunel P, Pfeffer MA, Altitude Investigators. Cardiorenal end points in a trial of aliskiren for type 2 diabetes. N Engl J Med. 2012;367:2204–13.CrossRefPubMed

62.

Zinman B, Wanner C, Lachin JM, Fitchett D, Bluhmki E, Hantel S, Mattheus M, Devins T, Johansen OE, Woerle HJ, Broedl UC, Inzucchi SE, EMPA-REG OUTCOME Investigators. Empagliflozin, cardiovascular outcomes, and mortality in type 2 diabetes. N Engl J Med. 2015;373:2117–28.CrossRefPubMed

63.

Wanner C, Inzucchi SE, Lachin JM, Fitchett D, von Eynatten M, Mattheus M, Johansen OE, Woerle HJ, Broedl UC, Zinman B, EMPA-REG OUTCOME Investigators. Empagliflozin and progression of kidney disease in type 2 diabetes. N Engl J Med. 2016;375:323–34.CrossRefPubMed

64.

Heerspink HJ, Johnsson E, Gause-Nilsson I, Cain VA, Sjostrom CD. Dapagliflozin reduces albuminuria in patients with diabetes and hypertension receiving renin-angiotensin blockers. Diabetes Obes Metab. 2016;18:590–7.CrossRefPubMedPubMedCentral

65.

Dyck PJ, Kratz KM, Karnes JL, Litchy WJ, Klein R, Pach JM, Wilson DM, O’Brien PC, Melton LJ 3rd, Service FJ. The prevalence by staged severity of various types of diabetic neuropathy, retinopathy, and nephropathy in a population-based cohort: the Rochester Diabetic Neuropathy Study. Neurology. 1993;43:817–24.CrossRefPubMed

66.

Dyck PJ, Davies JL, Wilson DM, Service FJ, Melton LJ 3rd, O’Brien PC. Risk factors for severity of diabetic polyneuropathy: intensive longitudinal assessment of the Rochester Diabetic Neuropathy Study cohort. Diabetes Care. 1999;22:1479–86.CrossRefPubMed

67.

Forrest KY, Maser RE, Pambianco G, Becker DJ, Orchard TJ. Hypertension as a risk factor for diabetic neuropathy: a prospective study. Diabetes. 1997;46:665–70.CrossRefPubMed

68.

Yagihashi S, Mizukami H, Sugimoto K. Mechanism of diabetic neuropathy: where are we now and where to go? J Diabetes Investig. 2011;2:18–32.CrossRefPubMed

69.

Dyck PJ. Hypoxic neuropathy: does hypoxia play a role in diabetic neuropathy? The 1988 Robert Wartenberg lecture. Neurology. 1989;39:111–8.CrossRefPubMed

70.

Cameron NE, Eaton SE, Cotter MA, Tesfaye S. Vascular factors and metabolic interactions in the pathogenesis of diabetic neuropathy. Diabetologia. 2001;44:1973–88.CrossRefPubMed

71.

Bravenboer B, Kappelle AC, Hamers FP, van Buren T, Erkelens DW, Gispen WH. Potential use of glutathione for the prevention and treatment of diabetic neuropathy in the streptozotocin-induced diabetic rat. Diabetologia. 1992;35:813–7.CrossRefPubMed

72.

Makin A, Lip GY, Silverman S, Beevers DG. Peripheral vascular disease and hypertension: a forgotten association? J Hum Hypertens. 2001;15:447–54.CrossRefPubMed

73.

Callaghan BC, Little AA, Feldman EL, Hughes RA. Enhanced glucose control for preventing and treating diabetic neuropathy. Cochrane Database Syst Rev. 2012, Issue 6. Art. No.: CD007543.

74.

Cameron NE, Cotter MA, Robertson S. Angiotensin converting enzyme inhibition prevents development of muscle and nerve dysfunction and stimulates angiogenesis in streptozotocin-diabetic rats. Diabetologia. 1992;35:12–8.CrossRefPubMed

75.

Malik RA, Williamson S, Abbott C, Carrington AL, Iqbal J, Schady W, Boulton AJ. Effect of angiotensin-converting-enzyme (ACE) inhibitor trandolapril on human diabetic neuropathy: randomised double-blind controlled trial. Lancet. 1998;352:1978–81.CrossRefPubMed

76.

Tesfaye S. Advances in the management of diabetic peripheral neuropathy. Curr Opin Support Palliat Care. 2009;3:136–43.CrossRefPubMed

77.

Huffman C, Stacey BR, Tuchman M, Burbridge C, Li C, Parsons B, Pauer L, Scavone JM, Behar R, Yurkewicz L. Efficacy and safety of pregabalin in the treatment of patients with painful diabetic peripheral neuropathy and pain on walking. Clin J Pain. 2015;31:946–58.CrossRefPubMed

78.

Yasuda H, Hotta N, Nakao K, Kasuga M, Kashiwagi A, Kawamori R. Superiority of duloxetine to placebo in improving diabetic neuropathic pain: results of a randomized controlled trial in Japan. J Diabetes Investig. 2011;2:132–9.CrossRefPubMed

79.

Hotta N, Akanuma Y, Kawamori R, Matsuoka K, Oka Y, Shichiri M, Toyota T, Nakashima M, Yoshimura I, Sakamoto N, Shigeta Y. Long-term clinical effects of epalrestat, an aldose reductase inhibitor, on diabetic peripheral neuropathy: the 3-year, multicenter, comparative aldose reductase inhibitor-diabetes complications trial. Diabetes Care. 2006;29:1538–44.CrossRefPubMed

80.

Ziegler D, Hanefeld M, Ruhnau KJ, Hasche H, Lobisch M, Schutte K, Kerum G, Malessa R. Treatment of symptomatic diabetic polyneuropathy with the antioxidant alpha-lipoic acid: a 7-month multicenter randomized controlled trial (ALADIN III Study). ALADIN III Study Group. Alpha-Lipoic Acid in Diabetic Neuropathy. Diabetes Care. 1999;22:1296–301.CrossRefPubMed

81.

Ziegler D, Low PA, Litchy WJ, Boulton AJ, Vinik AI, Freeman R, Samigullin R, Tritschler H, Munzel U, Maus J, Schutte K, Dyck PJ. Efficacy and safety of antioxidant treatment with alpha-lipoic acid over 4 years in diabetic polyneuropathy: the NATHAN 1 trial. Diabetes Care. 2011;34:2054–60.CrossRefPubMedPubMedCentral

82.

Vinik AI, Maser RE, Mitchell BD, Freeman R. Diabetic autonomic neuropathy. Diabetes Care. 2003;26:1553–79.CrossRefPubMed

83.

Shibao C, Lipsitz LA, Biaggioni I, American Society of Hypertension Writing Group. Evaluation and treatment of orthostatic hypotension. J Am Soc Hypertens. 2013;7:317–24.CrossRefPubMedPubMedCentral

84.

Spallone V, Maiello MR, Morganti R, Mandica S, Frajese G. Usefulness of ambulatory blood pressure monitoring in predicting the presence of autonomic neuropathy in type I diabetic patients. J Hum Hypertens. 2007;21:381–6.CrossRefPubMed

85.

Kannel WB, McGee DL. Diabetes and cardiovascular risk factors: the Framingham study. Circulation. 1979;59:8–13.CrossRefPubMed

86.

Haffner SM, Lehto S, Ronnemaa T, Pyorala K, Laakso M. Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N Engl J Med. 1998;339:229–34.CrossRefPubMed

87.

The DECODE-study group on behalf of the European Diabetes Epidemiology Group. Is fasting glucose sufficient to define diabetes? Epidemiological data from 20 European studies. Diabetologia. 1999;42:647–54.

88.

Fuller JH, Stevens LK, Wang SL. Risk factors for cardiovascular mortality and morbidity: the WHO mutinational study of vascular disease in diabetes. Diabetologia. 2001;44:S54–64.CrossRefPubMed

89.

UK Prospective Diabetes Study Group. Effect of intensive blood-glucose control with metformin on complications in overweight patients with type 2 diabetes (UKPDS 34). Lancet. 1998;352:854–65.

90.

Dormandy JA, Charbonnel B, Eckland DJ, Erdmann E, Massi-Benedetti M, Moules IK, Skene AM, Tan MH, Lefebvre PJ, Murray GD, Standl E, Wilcox RG, Wilhelmsen L, Betteridge J, Birkeland K, Golay A, Heine RJ, Koranyi L, Laakso M, Mokan M, Norkus A, Pirags V, Podar T, Scheen A, Scherbaum W, Schernthaner G, Schmitz O, Skrha J, Smith U, Taton J, PROactive Investigators. Secondary prevention of macrovascular events in patients with type 2 diabetes in the PROactive Study (PROspective pioglitAzone Clinical Trial In macroVascular Events): a randomised controlled trial. Lancet. 2005;366:1279–89.CrossRefPubMed

91.

Scirica BM, Bhatt DL, Braunwald E, Steg PG, Davidson J, Hirshberg B, Ohman P, Frederich R, Wiviott SD, Hoffman EB, Cavender MA, Udell JA, Desai NR, Mosenzon O, McGuire DK, Ray KK, Leiter LA, Raz I, SAVOR-TIMI 53 Steering Committee and Investigators. Saxagliptin and cardiovascular outcomes in patients with type 2 diabetes mellitus. N Engl J Med. 2013;369:1317–26.CrossRefPubMed

92.

Green JB, Bethel MA, Armstrong PW, Buse JB, Engel SS, Garg J, Josse R, Kaufman KD, Koglin J, Korn S, Lachin JM, McGuire DK, Pencina MJ, Standl E, Stein PP, Suryawanshi S, Van de Werf F, Peterson ED, Holman RR, TECOS Study Group. Effect of sitagliptin on cardiovascular outcomes in type 2 diabetes. N Engl J Med. 2015;373:232–42.CrossRefPubMed

93.

Marso SP, Daniels GH, Brown-Frandsen K, Kristensen P, Mann JF, Nauck MA, Nissen SE, Pocock S, Poulter NR, Ravn LS, Steinberg WM, Stockner M, Zinman B, Bergenstal RM, Buse JB, LEADER Steering Committee, LEADER Trial Investigators. Liraglutide and cardiovascular outcomes in type 2 diabetes. N Engl J Med. 2016;375:311–22.CrossRefPubMedPubMedCentral

94.

Rahman A, Hitomi H, Nishiyama A. Cardioprotective effects of SGLT2 inhibitors are possibly associated with normalization of the circadian rhythm of blood pressure. Hypertens Res. 2017;40:535–40.CrossRefPubMed

95.

Yoshikawa T, Kishi T, Shinohara K, Takesue K, Shibata R, Sonoda N, Inoguchi T, Sunagawa K, Tsutsui H, Hirooka Y. Arterial pressure lability is improved by sodium-glucose cotransporter 2 inhibitor in streptozotocin-induced diabetic rats. Hypertens Res. 2017;40:646–51.CrossRefPubMed

96.

Hansson L, Zanchetti A, Carruthers SG, Dahlof B, Elmfeldt D, Julius S, Menard J, Rahn KH, Wedel H, Westerling S. Effects of intensive blood-pressure lowering and low-dose aspirin in patients with hypertension: principal results of the Hypertension Optimal Treatment (HOT) randomised trial. HOT study group. Lancet. 1998;351:1755–62.CrossRefPubMed

97.

Kushiro T, Kario K, Saito I, Teramukai S, Sato Y, Okuda Y, Shimada K. Increased cardiovascular risk of treated white coat and masked hypertension in patients with diabetes and chronic kidney disease: the HONEST study. Hypertens Res. 2017;40:87–95.CrossRefPubMed

98.

Cholesterol Treatment Trialists’ (CTT) Collaborators, Kearney PM, Blackwell L, Collins R, Keech A, Simes J, Peto R, Armitage J, Baigent C. Efficacy of cholesterol-lowering therapy in 18,686 people with diabetes in 14 randomised trials of statins: a meta-analysis. Lancet. 2008;371:117–25.CrossRef

99.

Itoh H, Kurihara I, Miyashita K, Tanaka M. Clinical significance of ‘cardiometabolic memory’: a systematic review of randomized controlled trials. Hypertens Res. 2017;40:526–34.CrossRefPubMed

100.

Keech A, Simes RJ, Barter P, Best J, Scott R, Taskinen MR, Forder P, Pillai A, Davis T, Glasziou P, Drury P, Kesaniemi YA, Sullivan D, Hunt D, Colman P, d’Emden M, Whiting M, Ehnholm C, Laakso M, FIELD study investigators. . Effects of long-term fenofibrate therapy on cardiovascular events in 9795 people with type 2 diabetes mellitus (the FIELD study): randomised controlled trial. Lancet. 2005;366:1849–61.CrossRefPubMed

101.

Oikawa S, Yokoyama M, Origasa H, Matsuzaki M, Matsuzawa Y, Saito Y, Ishikawa Y, Sasaki J, Hishida H, Itakura H, Kita T, Kitabatake A, Nakaya N, Sakata T, Shimada K, Shirato K, JELIS Investigators. Suppressive effect of EPA on the incidence of coronary events in hypercholesterolemia with impaired glucose metabolism: Sub-analysis of the Japan EPA Lipid Intervention Study (JELIS). Atherosclerosis. 2009;206:535–9.CrossRefPubMed

102.

ORIGIN Trial Investigators, Bosch J, Gerstein HC, Dagenais GR, Diaz R, Dyal L, Jung H, Maggiono AP, Probstfield J, Ramachandran A, Riddle MC, Ryden LE, Yusuf S. N-3 fatty acids and cardiovascular outcomes in patients with dysglycemia. N Engl J Med. 2012;367:309–18.CrossRef

103.

Cannon CP, Blazing MA, Giugliano RP, McCagg A, White JA, Theroux P, Darius H, Lewis BS, Ophuis TO, Jukema JW, De Ferrari GM, Ruzyllo W, De Lucca P, Im K, Bohula EA, Reist C, Wiviott SD, Tershakovec AM, Musliner TA, Braunwald E, Califf RM, IMPROVE-IT Investigators. Ezetimibe added to statin therapy after acute coronary syndromes. N Engl J Med. 2015;372:2387–97.CrossRefPubMed

104.

Ference BA, Robinson JG, Brook RD, Catapano AL, Chapman MJ, Neff DR, Voros S, Giugliano RP, Davey Smith G, Fazio S, Sabatine MS. Variation in PCSK9 and HMGCR and risk of cardiovascular disease and diabetes. N Engl J Med. 2016;375:2144–53.CrossRefPubMed

105.

Gaede P, Vedel P, Larsen N, Jensen GV, Parving HH, Pedersen O. Multifactorial intervention and cardiovascular disease in patients with type 2 diabetes. N Engl J Med. 2003;348:383–93.CrossRefPubMed

Be confident that your patient care is up to date

Medicine Matters is being incorporated into Springer Medicine, our new medical education platform.

Alongside the news coverage and expert commentary you have come to expect from Medicine Matters diabetes, Springer Medicine's complimentary membership also provides access to articles from renowned journals and a broad range of Continuing Medical Education programs. Create your free account »

Medicine Matters Diabetes

Abstract

Be confident that your patient care is up to date