Cardioprotective effects of SGLT2 inhibitors are possibly associated with normalization of the circadian rhythm of blood pressure

Hypertension Research

Volumn 40, Issue 6, 2017, Pages 535-540

  Rahman, Asadur ^a   Hitomi, Hirofumi ^a   Nishiyama, Akira ^a  

^a KAGAWA UNIVERSITY   (Japan)

Author keywords

Cardioprotective effects; circadian rhythm of blood pressure; SGLT2 inhibitor; type 2 diabetes

Indexed keywords

SODIUM GLUCOSE COTRANSPORTER 2; ANTIDIABETIC AGENT; SLC5A2 PROTEIN, HUMAN;

ARTERIAL STIFFNESS; BLOOD PRESSURE; BODY WEIGHT; CARDIOVASCULAR DISEASE; CIRCADIAN RHYTHM; DIASTOLIC BLOOD PRESSURE; GLUCOSE BLOOD LEVEL; HEART PROTECTION; HYPOTENSION; INSULIN SENSITIVITY; MORBIDITY; MORTALITY; NATRIURESIS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PLEIOTROPY; REVIEW; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; HUMAN;

ANIMALS; BLOOD PRESSURE; CARDIOVASCULAR DISEASES; CIRCADIAN RHYTHM; HUMANS; HYPOGLYCEMIC AGENTS; SODIUM-GLUCOSE TRANSPORTER 2;

EID: 85016614784     PISSN: 09169636     EISSN: 13484214     Source Type: Journal    
DOI: 10.1038/hr.2016.193     Document Type: Review

References (83)

1. Fox CS, Pencina MJ, Wilson PW, Paynter NP, Vasan RS, D'Agostino RB Sr. Lifetime risk of cardiovascular disease among individuals with and without diabetes stratified by obesity status in the Framingham heart study. Diabetes Care 2008; 31: 1582-1584.
2. Kabakov E, Norymberg C, Osher E, Koffler M, Tordjman K, Greenman Y, Stern N. Prevalence of hypertension in type 2 diabetes mellitus: impact of the tightening definition of high blood pressure and association with confounding risk factors. J Cardiometab Syndr 2006; 1: 95-101.
3. Zinman B, Wanner C, Lachin JM, Fitchett D, Bluhmki E, Hantel S, Mattheus M, Devins T, Johansen OE, Woerle HJ, Broedl UC, Inzucchi SEInvestigators E-RO. Empagliflozin, cardiovascular outcomes, and mortality in type 2 diabetes. N Engl J Med 2015; 373: 2117-2128.
4. Mogi M, Horiuchi M. To overcome two diseases with one pill. Hypertens Res 2016; 39: 399-400.
5. Laakso M, Kuusisto J. Insulin resistance and hyperglycaemia in cardiovascular disease development. Nat Rev Endocrinol 2014; 10: 293-302.
6. Filippatos TD, Tsimihodimos V, Elisaf MS. Mechanisms of blood pressure reduction with sodium-glucose co-transporter 2 (SGLT2) inhibitors. Expert Opin Pharmacother 2016; 17: 1581-1583.
7. White WB. Ambulatory blood pressure monitoring: dippers compared with non-dippers. Blood Press Monit 2000; 5 (Suppl 1): S17-S23.
8. Ohkubo T, Hozawa A, Yamaguchi J, Kikuya M, Ohmori K, Michimata M, Matsubara M, Hashimoto J, Hoshi H, Araki T, Tsuji I, Satoh H, Hisamichi S, Imai Y. Prognostic significance of the nocturnal decline in blood pressure in individuals with and without high 24-h blood pressure: the Ohasama study. J Hypertens 2002; 20: 2183-2189.
9. Ohkubo T, Imai Y, Tsuji I, Nagai K, Watanabe N, Minami N, Kato J, Kikuchi N, Nishiyama A, Aihara A, Sekino M, Satoh H, Hisamichi S. Relation between nocturnal decline in blood pressure and mortality. The Ohasama Study. Am J Hypertens 1997; 10: 1201-1207.
10. Tikkanen I, Narko K, Zeller C, Green A, Salsali A, Broedl UC, Woerle HJ. Investigators E-RB. Empagliflozin reduces blood pressure in patients with type 2 diabetes and hypertension. Diabetes Care 2015; 38: 420-428.
11. Mori H, Okada Y, Kawaguchi M, Tanaka Y. A case of type 2 diabetes with a change from a non-dipper to a dipper blood pressure pattern by dapagliflozin. J UOEH 2016; 38: 149-153.
12. Hassler C, Burnier M. Circadian variations in blood pressure: implications for chronotherapeutics. Am J Cardiovasc Drugs 2005; 5: 7-15.
13. Hermida RC, Ayala DE, Portaluppi F. Circadian variation of blood pressure: the basis for the chronotherapy of hypertension. Adv Drug Deliv Rev 2007; 59: 904-922.
14. Della Mea P, Lupia M, Bandolin V, Guzzon S, Sonino N, Vettor R, Fallo F. Adiponectin, insulin resistance, and left ventricular structure in dipper and nondipper essential hypertensive patients. Am J Hypertens 2005; 18: 30-35.
15. Cuspidi C, Meani S, Salerno M, Valerio C, Fusi V, Severgnini B, Lonati L, Magrini F, Zanchetti A. Cardiovascular target organ damage in essential hypertensives with or without reproducible nocturnal fall in blood pressure. J Hypertens 2004; 22: 273-280.
16. Fogari R, Zoppi A, Malamani GD, Lazzari P, Destro M, Corradi L. Ambulatory blood pressure monitoring in normotensive and hypertensive type 2 diabetes. Prevalence of impaired diurnal blood pressure patterns. Am J Hypertens 1993; 6: 1-7.
17. Pierdomenico SD, Pierdomenico AM, Coccina F, Lapenna D, Porreca E. Circadian blood pressure changes and cardiovascular risk in elderly-treated hypertensive patients. Hypertens Res 2016; 39: 805-811.
18. Fagard RH, Thijs L, Staessen JA, Clement DL, De Buyzere ML, De Bacquer DA. Night-day blood pressure ratio and dipping pattern as predictors of death and cardiovascular events in hypertension. J Hum Hypertens 2009; 23: 645-653.
19. Sturrock ND, George E, Pound N, Stevenson J, Peck GM, Sowter H. Non-dipping circadian blood pressure and renal impairment are associated with increased mortality in diabetes mellitus. Diabet Med 2000; 17: 360-364.
20. Ayala DE, Moya A, Crespo JJ, Castineira C, Dominguez-Sardina M, Gomara S, Sineiro E, Mojon A, Fontao MJ, Hermida RCHygia Project I. Circadian pattern of ambulatory blood pressure in hypertensive patients with and without type 2 diabetes. Chronobiol Int 2013; 30: 99-115.
21. 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: 229-234.
22. Group AC, 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: 2560-2572.
23. Duckworth W, Abraira C, Moritz T, Reda D, Emanuele N, Reaven PD, Zieve FJ, Marks J, Davis SN, Hayward R, Warren SR, Goldman S, McCarren M, Vitek ME, Henderson WG, Huang GD, Investigators V. Glucose control and vascular complications in veterans with type 2 diabetes. N Engl J Med 2009; 360: 129-139.
24. Salsali A, Kim G, Woerle HJ, Broedl UC, Hantel S. Cardiovascular safety of empagli-flozin in patients with type 2 diabetes: a meta-analysis of data from randomized placebo-controlled trials. Diabetes Obes Metab 2016; 18: 1034-1040.
25. Sonesson C, Johansson PA, Johnsson E, Gause-Nilsson I. Cardiovascular effects of dapagliflozin in patients with type 2 diabetes and different risk categories: a meta-analysis. Cardiovasc Diabetol 2016; 15: 37.
26. Neal B, Perkovic V, de Zeeuw D, Mahaffey KW, Fulcher G, Stein P, Desai M, Shaw W, Jiang J, Vercruysse F, Meininger G, Matthews D. Rationale, design, and baseline characteristics of the Canagliflozin Cardiovascular Assessment Study (CANVAS)-a randomized placebo-controlled trial. Am Heart J 2013; 166: 217-223e211.
27. Clinicaltrials.gov. Multicenter trial to evaluate the effect of dapagliflozin on the incidence of cardiovascular events (DECLARE-TIMI58). Accessed on 08 January 2016 https://clinicaltrials.gov/ct2/show/NCT01730534.
28. Singh JS, Fathi A, Vickneson K, Mordi I, Mohan M, Houston JG, Pearson ER, Struthers AD, Lang CC. Research into the effect Of SGLT2 inhibition on left ventricular remodelling in patients with heart failure and diabetes mellitus (REFORM) trial rationale and design. Cardiovasc Diabetol 2016; 15: 97.
29. Clinicaltrials.gov. Cardiovascular outcomes following ertugliflozin treatment in type 2 diabetes mellitus participants with vascular disease, the VERTIS CV Study (MK-8835-004). Accessed on 09 September 2016 https://clinicaltrials.gov/ct2/show/NCT01986881.
30. Lin B, Koibuchi N, Hasegawa Y, Sueta D, Toyama K, Uekawa K, Ma M, Nakagawa T, Kusaka H, Kim-Mitsuyama S. Glycemic control with empagliflozin, a novel selective SGLT2 inhibitor, ameliorates cardiovascular injury and cognitive dysfunction in obese and type 2 diabetic mice. Cardiovasc Diabetol 2014; 13: 148.
31. Zaccardi F, Webb DR, Htike ZZ, Youssef D, Khunti K, Davies MJ. Efficacy and safety of sodium-glucose co-transporter-2 inhibitors in type 2 diabetes mellitus: systematic review and network meta-analysis. Diabetes Obes Metab 2016; 18: 783-794.
32. Ng CM, Yiu SF, Choi KL, Choi CH, Ng YW, Tiu SC. Prevalence and significance of white-coat hypertension and masked hypertension in type 2 diabetics. Hong Kong Med J 2008; 14: 437-443.
33. Eguchi K, Pickering TG, Hoshide S, Ishikawa J, Ishikawa S, Schwartz JE, Shimada K, Kario K. Ambulatory blood pressure is a better marker than clinic blood pressure in predicting cardiovascular events in patients with/without type 2 diabetes. Am J Hypertens 2008; 21: 443-450.
34. Tamura K, Wakui H, Azushima K, Uneda K, Umemura S. Circadian blood pressure rhythm as a possible key target of SGLT2 inhibitors used for the treatment of Type 2 diabetes. Hypertens Res 2016; 39: 396-398.
35. Lambers Heerspink HJ, de Zeeuw D, Wie L, Leslie B, List J. Dapagliflozin a glucose-regulating drug with diuretic properties in subjects with type 2 diabetes. Diabetes Obes Metab 2013; 15: 853-862.
36. Amin NB, Wang X, Mitchell JR, Lee DS, Nucci G, Rusnak JM. Blood pressure-lowering effect of the sodium glucose co-transporter-2 inhibitor ertugliflozin, assessed via ambulatory blood pressure monitoring in patients with type 2 diabetes and hypertension. Diabetes Obes Metab 2015; 17: 805-808.
37. Chilton R, Tikkanen I, Crowe S, Johansen OE, Broedl UC, Woerle HJ, Hach T. 4b.03: empagliflozin reduces systolic blood pressure in dipper and non-dipper patients with type 2 diabetes and hypertension. J Hypertens 2015; 33 (Suppl 1): e53.
38. Weber MA, Mansfield TA, Cain VA, Iqbal N, Parikh S, Ptaszynska A. Blood pressure and glycaemic effects of dapagliflozin vs. placebo in patients with type 2 diabetes on combination antihypertensive therapy: a randomised, double-blind, placebo-controlled, phase 3 study. Lancet Diabetes Endocrinol 2016; 4: 211-220.
39. Takeshige Y, Fujisawa Y, Rahman A, Kittikulsuth W, Nakano D, Mori H, Masaki T, Ohmori K, Kohno M, Ogata H, Nishiyama A. A sodium-glucose co-transporter 2 inhibitor empagliflozin prevents abnormality of circadian rhythm of blood pressure in salt-treated obese rats. Hypertens Res 2016; 39: 415-422.
40. Guidelines (JSH 2014). Chapter 7. Hypertension complicated by other diseases. Hypertens Res 2014; 37: 315-324.
41. Kotsis V, Stabouli S, Papakatsika S, Rizos Z, Parati G. Mechanisms of obesity-induced hypertension. Hypertens Res 2010; 33: 386-393.
42. Shimizu I, Yoshida Y, Minamino T. A role for circadian clock in metabolic disease. Hypertens Res 2016; 39: 483-491.
43. Ukkola O, Vasunta RL, Kesaniemi YA. Non-dipping pattern in ambulatory blood pressure monitoring is associated with metabolic abnormalities in a random sample of middle-aged subjects. Hypertens Res 2009; 32: 1022-1027.
44. Rahman A, Kittikulsuth W, Fujisawa Y, Sufiun A, Rafiq K, Hitomi H, Nakano D, Sohara E, Uchida S, Nishiyama A. Effects of diuretics on sodium-dependent glucose cotransporter 2 inhibitor-induced changes in blood pressure in obese rats suffering from the metabolic syndrome. J Hypertens 2016; 34: 893-906.
45. Senador D, Shewale S, Irigoyen MC, Elased KM, Morris M. Effects of restricted fructose access on body weight and blood pressure circadian rhythms. Exp Diabetes Res 2012; 2012: 459087.
46. Maury E, Ramsey KM, Bass J. Circadian rhythms and metabolic syndrome: from experimental genetics to human disease. Circ Res 2010; 106: 447-462.
47. Masaki T, Anan F, Yoshimatsu H. Visceral fat accumulation is associated with circadian blood pressure in Japanese patients with impaired glucose tolerance. Diabetes Care 2011; 34: e32.
48. Blonde L, Stenlof K, Fung A, Xie J, Canovatchel W, Meininger G. Effects of canagliflozin on body weight and body composition in patients with type 2 diabetes over 104 weeks. Postgrad Med 2016; 128: 371-380.
49. Seino Y, Sasaki T, Fukatsu A, Ubukata M, Sakai S, Samukawa Y. Efficacy and safety of luseogliflozin as monotherapy in Japanese patients with type 2 diabetes mellitus: a randomized, double-blind, placebo-controlled, phase 3 study. Curr Med Res Opin 2014; 30: 1245-1255.
50. Yokono M, Takasu T, Hayashizaki Y, Mitsuoka K, Kihara R, Muramatsu Y, Miyoshi S, Tahara A, Kurosaki E, Li Q, Tomiyama H, Sasamata M, Shibasaki M, Uchiyama Y. SGLT2 selective inhibitor ipragliflozin reduces body fat mass by increasing fatty acid oxidation in high-fat diet-induced obese rats. Eur J Pharmacol 2014; 727: 66-74.
51. Bolinder J, Ljunggren O, Kullberg J, Johansson L, Wilding J, Langkilde AM, Sugg J, Parikh S. Effects of dapagliflozin on body weight, total fat mass, and regional adipose tissue distribution in patients with type 2 diabetes mellitus with inadequate glycemic control on metformin. J Clin Endocrinol Metab 2012; 97: 1020-1031.
52. Oliva RV, Bakris GL. Blood pressure effects of sodium-glucose co-transport 2 (SGLT2) inhibitors. J Am Soc Hypertens 2014; 8: 330-339.
53. Li L, Soonthornpun S, Chongsuvivatwong V. Association between circadian rhythm of blood pressure and glucose tolerance status in normotensive, non-diabetic subjects. Diabetes Res Clin Pract 2008; 82: 359-363.
54. van Bruggen EF, Kremer J. Electron microscopy of bovine and human cervical mucus. Int J Fertil 1970; 15: 50-57.
55. Anan F, Takahashi N, Ooie T, Yufu K, Saikawa T, Yoshimatsu H. Role of insulin resistance in nondipper essential hypertensive patients. Hypertens Res 2003; 26: 669-676.
56. Ferrannini E, Muscelli E, Frascerra S, Baldi S, Mari A, Heise T, Broedl UC, Woerle HJ. Metabolic response to sodium-glucose cotransporter 2 inhibition in type 2 diabetic patients. J Clin Invest 2014; 124: 499-508.
57. Merovci A, Solis-Herrera C, Daniele G, Eldor R, Fiorentino TV, Tripathy D, Xiong J, Perez Z, Norton L, Abdul-Ghani MA, DeFronzo RA. Dapagliflozin improves muscle insulin sensitivity but enhances endogenous glucose production. J Clin Invest 2014; 124: 509-514.
58. Brands MW, Manhiani MM. Sodium-retaining effect of insulin in diabetes. Am J Physiol Regul Integr Comp Physiol 2012; 303: R1101-R1109.
59. El-Atat FA, Stas SN, McFarlane SI, Sowers JR. The relationship between hyperinsuli-nemia, hypertension and progressive renal disease. J Am Soc Nephrol 2004; 15: 2816-2827.
60. de la Sierra A, Redon J, Banegas JR, Segura J, Parati G, Gorostidi M, de la Cruz JJ, Sobrino J, Llisterri JL, Alonso J, Vinyoles E, Pallares V, Sarria A, Aranda P, Ruilope LM. Spanish Society of Hypertension Ambulatory Blood Pressure Monitoring Registry Investigators. Prevalence and factors associated with circadian blood pressure patterns in hypertensive patients. Hypertension 2009; 53: 466-472.
61. Uzu T, Ishikawa K, Fujii T, Nakamura S, Inenaga T, Kimura G. Sodium restriction shifts circadian rhythm of blood pressure from nondipper to dipper in essential hypertension. Circulation 1997; 96: 1859-1862.
62. Uzu T, Kimura G. Diuretics shift circadian rhythm of blood pressure from nondipper to dipper in essential hypertension. Circulation 1999; 100: 1635-1638.
63. Iijima H, Kifuji T, Maruyama N, Inagaki N. Pharmacokinetics, pharmacodynamics, and safety of canagliflozin in japanese patients with type 2 diabetes mellitus. Adv Ther 2015; 32: 768-782.
64. Kopp C, Linz P, Dahlmann A, Hammon M, Jantsch J, Muller DN, Schmieder RE, Cavallaro A, Eckardt KU, Uder M, Luft FC, Titze J. 23Na magnetic resonance imaging-determined tissue sodium in healthy subjects and hypertensive patients. Hypertension 2013; 61: 635-640.
65. Frohlich ED, Susic D. Sodium and its multiorgan targets. Circulation 2011; 124: 1882-1885.
66. 23Na magnetic resonance imaging of the lower leg of acute heart failure patients during diuretic treatment. PLoS ONE 2015; 10: e0141336.
67. Schmieder R, Ott C, Linz P, Jumar A, Friedrich S, Titze J, Hammon M, Uder M, Kistner I. Os 12-03 Sglt-2-inhibition with dapagliflozin reduces tissue sodium content. J Hypertens 2016; 34 (Suppl 1) ISH 2016 Abstract Book e76.
68. Lekakis JP, Zakopoulos NA, Protogerou AD, Papaioannou TG, Kotsis VT, Pitiriga V, Tsitsirikos MD, Stamatelopoulos KS, Papamichael CM, Mavrikakis ME. Arterial stiffness assessed by pulse wave analysis in essential hypertension: relation to 24-h blood pressure profile. Int J Cardiol 2005; 102: 391-395.
69. Salvetti M, Muiesan ML, Rizzoni D, Bettoni G, Monteduro C, Corbellini C, Viola S, Agabiti-Rosei E. Night time blood pressure and cardiovascular structure in a middle-aged general population in northern Italy: the Vobarno Study. J Hum Hypertens 2001; 15: 879-885.
70. Phillips RA, Butkevich A, Sheinart KF, Tuhrim S. Dipping is superior to cusums analysis in assessment of the risk of stroke in a case-control study. Am J Hypertens 2001; 14: 649-652.
71. Kikuya M, Ohkubo T, Asayama K, Metoki H, Obara T, Saito S, Hashimoto J, Totsune K, Hoshi H, Satoh H, Imai Y. Ambulatory blood pressure and 10-year risk of cardiovascular and noncardiovascular mortality: the Ohasama study. Hypertension 2005; 45: 240-245.
72. Cherney DZ, Perkins BA, Soleymanlou N, Har R, Fagan N, Johansen OE, Woerle HJ, von Eynatten M, Broedl UC. The effect of empagliflozin on arterial stiffness and heart rate variability in subjects with uncomplicated type 1 diabetes mellitus. Cardiovasc Diabetol 2014; 13: 28.
73. Chilton R, Tikkanen I, Cannon CP, Crowe S, Woerle HJ, Broedl UC, Johansen OE. Effects of empagliflozin on blood pressure and markers of arterial stiffness and vascular resistance in patients with type 2 diabetes. Diabetes Obes Metab 2015; 17: 1180-1193.
74. Equiluz-Bruck S, Schnack C, Kopp HP, Schernthaner G. Nondipping of nocturnal blood pressure is related to urinary albumin excretion rate in patients with type 2 diabetes mellitus. Am J Hypertens 1996; 9: 1139-1143.
75. Wanner C, Inzucchi SE, Lachin JM, Fitchett D, von Eynatten M, Mattheus M, Johansen OE, Woerle HJ, Broedl UC, Zinman BInvestigators E-RO. Empagliflozin and progression of kidney disease in type 2 diabetes. N Engl J Med 2016; 375: 323-334.
76. Cherney D, Lund SS, Perkins BA, Groop PH, Cooper ME, Kaspers S, Pfarr E, Woerle HJ, von Eynatten M. The effect of sodium glucose cotransporter 2 inhibition with empagliflozin on microalbuminuria and macroalbuminuria in patients with type 2 diabetes. Diabetologia 2016; 59: 1860-1870.
77. 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: 590-597.
78. Hagbarth KE, Vallbo AB. Afferent response to mechanical stimulation of muscle receptors in man. Acta Soc Med Ups 1967; 72: 102-104.
79. Bailey CJ, Gross JL, Pieters A, Bastien A, List JF. Effect of dapagliflozin in patients with type 2 diabetes who have inadequate glycaemic control with metformin: a randomised, double-blind, placebo-controlled trial. Lancet 2010; 375: 2223-2233.
80. Causevic A, Semiz S, Macic Dzankovic A, Cico B, Dujic T, Malenica M, Bego T. Relevance of uric Acid in progression of type 2 diabetes mellitus. Bosn J Basic Med Sci 2010; 10: 54-59.
81. Culleton BF, Larson MG, Kannel WB, Levy D. Serum uric acid and risk for cardiovascular disease and death: the Framingham Heart Study. Ann Intern Med 1999; 131: 7-13.
82. Turak O, Ozcan F, Tok D, Isleyen A, Sokmen E, Tasoglu I, Aydogdu S, Sen N, McFann K, Johnson RJ, Kanbay M. Serum uric acid, inflammation, and nondipping circadian pattern in essential hypertension. J Clin Hypertens (Greenwich) 2013; 15: 7-13.
83. Ferrannini E, Ramos SJ, Salsali A, Tang W, List JF. Dapagliflozin monotherapy in type 2 diabetic patients with inadequate glycemic control by diet and exercise: a randomized, double-blind, placebo-controlled, phase 3 trial. Diabetes Care 2010; 33: 2217-2224.