Effects of reducing blood pressure on renal outcomes in patients with type 2 diabetes: Focus on SGLT2 inhibitors and EMPA-REG OUTCOME.

[en] Empagliflozin, a sodium-glucose cotransporter type 2 (SGLT2) inhibitor, has enabled remarkable reductions in cardiovascular and all-cause mortality as well as in renal outcomes in patients with type 2 diabetes (T2D) and a history of cardiovascular disease in the EMPA-REG OUTCOME. These results have been attributed to haemodynamic rather than metabolic effects, in part due to the osmotic/diuretic action of empagliflozin and the reduction in arterial blood pressure (BP). The present narrative review includes the results of meta-analyses of trials evaluating the effects on renal outcomes of lowering BP in patients with T2D, with a special focus on the influence of baseline and achieved systolic BP, and compares the renal outcome results of the EMPA-REG OUTCOME with those of other major trials with inhibitors of the renin-angiotensin system in patients with T2D and the preliminary findings with other SGLT2 inhibitors, and also evaluates post hoc analyses from the EMPA-REG OUTCOME of special interest as regards the BP-lowering hypothesis and renal function. While systemic BP reduction associated to empagliflozin therapy may have contributed to the renal benefits reported in EMPA-REG OUTCOME, other local mechanisms related to kidney homoeostasis most probably also played a role in the overall protection observed in the trial.

Disciplines :

Endocrinology, metabolism & nutrition
Pharmacy, pharmacology & toxicology
Cardiovascular & respiratory systems

Author, co-author :

Scheen, André ; Université de Liège > Département des sciences cliniques > Département des sciences cliniques

DELANAYE, Pierre ; Centre Hospitalier Universitaire de Liège - CHU > Department of Medicine > Division of Nephrology, Dialysis, Transplantation and Hypertension

Language :

English

Title :

Effects of reducing blood pressure on renal outcomes in patients with type 2 diabetes: Focus on SGLT2 inhibitors and EMPA-REG OUTCOME.

Publication date :

2017

Journal title :

Diabetes and Metabolism

ISSN :

1262-3636

eISSN :

1878-1780

Publisher :

Elsevier Masson, Paris, France

Issue :

epub ahead of print

Peer reviewed :

Peer Reviewed verified by ORBi

Commentary :

Available on ORBi :

since 24 March 2017

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Bibliography

[1] Ferrannini, E., Cushman, W.C., Diabetes and hypertension: the bad companions. Lancet 380 (2012), 601–610.
[2] Van Buren, P.N., Toto, R., Hypertension in diabetic nephropathy: epidemiology, mechanisms, and management. Adv Chronic Kidney Dis 18 (2011), 28–41.
[3] Gregg, E.W., Li, Y., Wang, J., Burrows, N.R., Ali, M.K., Rolka, D., et al. Changes in diabetes-related complications in the United States, 1990–2010. N Engl J Med 370 (2014), 1514–1523.
[4] Stratton, I.M., Cull, C.A., Adler, A.I., Matthews, D.R., Neil, H.A., Holman, R.R., Additive effects of glycaemia and blood pressure exposure on risk of complications in type 2 diabetes: a prospective observational study (UKPDS 75). Diabetologia 49 (2006), 1761–1769.
[5] Tight blood pressure control and risk of macrovascular and microvascular complications in type 2 diabetes: UKPDS 38. UK Prospective Diabetes Study Group. BMJ 317 (1998), 703–713.
[6] UK Prospective Diabetes Study (UKPDS) 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 352 (1998), 837–853.
[7] Zoungas, S., de Galan, B.E., Ninomiya, T., Grobbee, D., Hamet, P., Heller, S., et al. Combined effects of routine blood pressure lowering and intensive glucose control on macrovascular and microvascular outcomes in patients with type 2 diabetes: new results from the ADVANCE trial. Diabetes Care 32 (2009), 2068–2074.
[8] Ismail-Beigi, F., Craven, T.E., O'Connor, P.J., Karl, D., Calles-Escandon, J., Hramiak, I., et al. Combined intensive blood pressure and glycemic control does not produce an additive benefit on microvascular outcomes in type 2 diabetic patients. Kidney Int 81 (2012), 586–594.
[9] Sundstrom, J., Arima, H., Jackson, R., Turnbull, F., Rahimi, K., Chalmers, J., et al. Effects of blood pressure reduction in mild hypertension: a systematic review and meta-analysis. Ann Intern Med 162 (2015), 184–191.
[10] Xie, X., Atkins, E., Lv, J., Bennett, A., Neal, B., Ninomiya, T., et al. Effects of intensive blood pressure lowering on cardiovascular and renal outcomes: updated systematic review and meta-analysis. Lancet 387 (2016), 435–443.
[11] Kintscher, U., Benefit of blood pressure control in diabetic patients. Curr Hypertens Rep, 17, 2015, 50.
[12] Joven, M.H., Anderson, R.J., Update on blood pressure control and renal outcomes in diabetes mellitus. Curr Diabetes Rep, 15, 2015, 44.
[13] Arguedas, J.A., Leiva, V., Wright, J.M., Blood pressure targets for hypertension in people with diabetes mellitus. Cochrane Database Syst Rev, 10, 2013, CD008277.
[14] Esler, M., SPRINT, or false start, toward a lower universal treated blood pressure target in hypertension. Hypertension 67 (2016), 266–267.
[15] Cryer, M.J., Horani, T., DiPette, D.J., Diabetes and hypertension: a comparative review of current guidelines. J Clin Hypertens (Greenwich) 18 (2016), 95–100.
[16] Hansson, L., Zanchetti, A., Carruthers, S.G., Dahlof, B., Elmfeldt, D., Julius, S., et al. 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 351 (1998), 1755–1762.
[17] Estacio, R.O., Jeffers, B.W., Gifford, N., Schrier, R.W., Effect of blood pressure control on diabetic microvascular complications in patients with hypertension and type 2 diabetes. Diabetes Care 23:Suppl 2 (2000), B54–B64.
[18] Jerums, G., Panagiotopoulos, S., Ekinci, E., MacIsaac, R.J., Cardiovascular outcomes with antihypertensive therapy in type 2 diabetes: an analysis of intervention trials. J Hum Hypertens 29 (2015), 473–477.
[19] Lv, J., Ehteshami, P., Sarnak, M.J., Tighiouart, H., Jun, M., Ninomiya, T., et al. Effects of intensive blood pressure lowering on the progression of chronic kidney disease: a systematic review and meta-analysis. CMAJ 185 (2013), 949–957.
[20] Mancia, G., Fagard, R., Narkiewicz, K., Redon, J., Zanchetti, A., Bohm, M., et al. 2013 ESH/ESC guidelines for the management of arterial hypertension: the Task Force for the Management of Arterial Hypertension of the European Society of Hypertension (ESH) and of the European Society of Cardiology (ESC). Eur Heart J 34 (2013), 2159–2219.
[21] Kidney Disease: Improving Global Outcomes (KDIGO) Blood Pressure Work Group, KDIGO Clinical Practice Guideline for the Management of Blood Pressure in Chronic Kidney Disease. Kidney Int 2 (2012), 337–414.
[22] Bangalore, S., Fakheri, R., Toklu, B., Messerli, F.H., Diabetes mellitus as a compelling indication for use of renin angiotensin system blockers: systematic review and meta-analysis of randomized trials. BMJ, 352, 2016, i438.
[23] Flack, J.M., Nolasco, C., Levy, P., The case for low blood pressure targets. Am J Hypertens 30 (2017), 3–7.
[24] Majewski, C., Bakris, G.L., Has RAAS blockade reached its limits in the treatment of diabetic nephropathy?. Curr Diabetes Rep, 16, 2016, 24.
[25] Lozano-Maneiro, L., Puente-Garcia, A., Renin–angiotensin–aldosterone system blockade in diabetic nephropathy. Present evidences. J Clin Med 4 (2015), 1908–1937.
[26] Gorriz, J.L., Nieto, J., Navarro-Gonzalez, J.F., Molina, P., Martinez-Castelao, A., Pallardo, L.M., Nephroprotection by hypoglycemic agents: do we have supporting data?. J Clin Med 4 (2015), 1866–1889.
[27] Marso, S.P., Daniels, G.H., Brown-Frandsen, K., Kristensen, P., Mann, J.F., Nauck, M.A., et al. Liraglutide and cardiovascular outcomes in type 2 diabetes. N Engl J Med 375 (2016), 311–322.
[28] Marso, S.P., Bain, S.C., Consoli, A., Eliaschewitz, F.G., Jodar, E., Leiter, L.A., et al. Semaglutide and cardiovascular outcomes in patients with type 2 diabetes. N Engl J Med 375 (2016), 1834–1844.
[29] Scheen, A.J., Pharmacodynamics, efficacy and safety of sodium–glucose co-transporter type 2 (SGLT2) inhibitors for the treatment of type 2 diabetes mellitus. Drugs 75 (2015), 33–59.
[30] Scheen, A.J., Paquot, N., Metabolic effects of SGLT2 inhibitors beyond increased glucosuria: a review of clinical evidence. Diabetes Metab 40 (2014), S4–S11.
[31] Inzucchi, S.E., Zinman, B., Wanner, C., Ferrari, R., Fitchett, D., Hantel, S., et al. SGLT-2 inhibitors and cardiovascular risk: proposed pathways and review of ongoing outcome trials. Diab Vasc Dis Res 12 (2015), 90–100.
[32] Ghosh, R.K., Bandyopadhyay, D., Hajra, A., Biswas, M., Gupta, A., Cardiovascular outcomes of sodium–glucose cotransporter 2 inhibitors: a comprehensive review of clinical and preclinical studies. Int J Cardiol 212 (2016), 29–36.
[33] Oliva, R.V., Bakris, G.L., Blood pressure effects of sodium–glucose co-transport 2 (SGLT2) inhibitors. J Am Soc Hypertens 8 (2014), 330–339.
[34] Maliha, G., Townsend, R.R., SGLT2 inhibitors: their potential reduction in blood pressure. J Am Soc Hypertens 9 (2015), 48–53.
[35] Imprialos, K.P., Sarafidis, P.A., Karagiannis, A.I., Sodium–glucose cotransporter-2 inhibitors and blood pressure decrease: a valuable effect of a novel antidiabetic class?. J Hypertens 33 (2015), 2185–2197.
[36] Baker, W.L., Smyth, L.R., Riche, D.M., Bourret, E.M., Chamberlin, K.W., White, W.B., Effects of sodium–glucose co-transporter 2 inhibitors on blood pressure: a systematic review and meta-analysis. J Am Soc Hypertens, 8, 2014 262–75.e9.
[37] Scheen, A.J., Effects of reducing blood pressure on cardiovascular outcomes and mortality in patients with type 2 diabetes: focus on SGLT2 inhibitors and EMPA-REG OUTCOME. Diabetes Res Clin Pract 121 (2016), 204–214.
[38] Lovshin, J.A., Gilbert, R.E., Are SGLT2 inhibitors reasonable antihypertensive drugs and renoprotective?. Curr Hypertens Rep, 17, 2015, 551.
[39] Scheen, A.J., SGLT2 inhibitors: benefit/risk balance. Curr Diabetes Rep, 16, 2016, 92.
[40] Zinman, B., Wanner, C., Lachin, J.M., Fitchett, D., Bluhmki, E., Hantel, S., et al. Empagliflozin, cardiovascular outcomes, and mortality in type 2 diabetes. N Engl J Med 373 (2015), 2117–2128.
[41] Wanner, C., Inzucchi, S.E., Lachin, J.M., Fitchett, D., von Eynatten, M., Mattheus, M., et al. Empagliflozin and progression of kidney disease in type 2 diabetes. N Engl J Med 375 (2016), 323–334.
[42] Scheen, A.J., Reduction in cardiovascular and all-cause mortality in the EMPA-REG OUTCOME trial: a critical analysis. Diabetes Metab 42 (2016), 71–76.
[43] Sattar, N., McLaren, J., Kristensen, S.L., Preiss, D., McMurray, J.J., SGLT2 inhibition and cardiovascular events: why did EMPA-REG Outcomes surprise and what were the likely mechanisms?. Diabetologia 59 (2016), 1333–1339.
[44] Rajasekeran, H., Lytvyn, Y., Cherney, D.Z., Sodium–glucose cotransporter 2 inhibition and cardiovascular risk reduction in patients with type 2 diabetes: the emerging role of natriuresis. Kidney Int 89 (2016), 524–526.
[45] Kimura, G., Importance of inhibiting sodium–glucose cotransporter and its compelling indication in type 2 diabetes: pathophysiological hypothesis. J Am Soc Hypertens 10 (2016), 271–278.
[46] Takeuchi, T., Dohi, K., Omori, T., Moriwaki, K., Sato, Y., Nakamori, S., et al. Diuretic effects of sodium–glucose cotransporter 2 inhibitor in patients with type 2 diabetes mellitus and heart failure. Int J Cardiol 201 (2015), 1–3.
[47] McMurray, J., EMPA-REG – the “diuretic hypothesis”. J Diabetes Complications 30 (2016), 3–4.
[48] Scheen, A.J., Reappraisal of the diuretic effect of empagliflozin in EMPA-REG OUTCOME: comparison with classic diuretics. Diabetes Metab 42 (2016), 224–233.
[49] John, M., Empagliflozin: not just a glorified diuretic. Indian J Endocrinol Metab 20 (2016), 154–156.
[50] Thomas, M.C., Jandeleit-Dahm, K., Bonnet, F., Beyond Glycosuria: Exploring the intrarenal effects of SGLT-2 inhibition in diabetes. Diabetes Metab 40 (2014), S17–S22.
[51] De Nicola, L., Gabbai, F.B., Liberti, M.E., Sagliocca, A., Conte, G., Minutolo, R., Sodium/glucose cotransporter 2 inhibitors and prevention of diabetic nephropathy: targeting the renal tubule in diabetes. Am J Kidney Dis 64 (2014), 16–24.
[52] Kalra, S., Singh, V., Nagrale, D., Sodium–glucose cotransporter-2 inhibition and the glomerulus: a review. Adv Ther 33 (2016), 1502–1518.
[53] DeFronzo, R.A., Hompesch, M., Kasichayanula, S., Liu, X., Hong, Y., Pfister, M., et al. Characterization of renal glucose reabsorption in response to dapagliflozin in healthy subjects and subjects with type 2 diabetes. Diabetes Care 36 (2013), 3169–3176.
[54] Lambers Heerspink, H.J., 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 15 (2013), 853–862.
[55] Cherney, D.Z., Perkins, B.A., Soleymanlou, N., Maione, M., Lai, V., Lee, A., et al. Renal hemodynamic effect of sodium–glucose cotransporter 2 inhibition in patients with type 1 diabetes mellitus. Circulation 129 (2014), 587–597.
[56] Heerspink, H.J., Perkins, B.A., Fitchett, D.H., Husain, M., Cherney, D.Z., Sodium glucose cotransporter 2 inhibitors in the treatment of diabetes: cardiovascular and kidney effects. Potential mechanisms and clinical applications. Circulation 134 (2016), 752–772.
[57] Gilbert, R.E., SGLT-2 inhibition in patients with kidney disease. Diabetes Metab 40 (2014), S23–S27.
[58] Fioretto, P., Zambon, A., Rossato, M., Busetto, L., Vettor, R., SGLT2 inhibitors and the diabetic kidney. Diabetes Care 39:Suppl 2 (2016), S165–S171.
[59] Emdin, C.A., Rahimi, K., Neal, B., Callender, T., Perkovic, V., Patel, A., Blood pressure lowering in type 2 diabetes: a systematic review and meta-analysis. JAMA 313 (2015), 603–615.
[60] Ettehad, D., Emdin, C.A., Kiran, A., Anderson, S.G., Callender, T., Emberson, J., et al. Blood pressure lowering for prevention of cardiovascular disease and death: a systematic review and meta-analysis. Lancet 387 (2016), 957–967.
[61] Brunstrom, M., Carlberg, B., Effect of antihypertensive treatment at different blood pressure levels in patients with diabetes mellitus: systematic review and meta-analyses. BMJ, 352, 2016, i717.
[62] Bangalore, S., Kumar, S., Lobach, I., Messerli, F.H., Blood pressure targets in subjects with type 2 diabetes mellitus/impaired fasting glucose: observations from traditional and Bayesian random-effects meta-analyses of randomized trials. Circulation 123 (2011), 2799–2810.
[63] Bakris, G.L., Weir, M.R., Shanifar, S., Zhang, Z., Douglas, J., van Dijk, D.J., et al. Effects of blood pressure level on progression of diabetic nephropathy: results from the RENAAL study. Arch Intern Med 163 (2003), 1555–1565.
[64] Mancia, G., Schumacher, H., Redon, J., Verdecchia, P., Schmieder, R., Jennings, G., et al. Blood pressure targets recommended by guidelines and incidence of cardiovascular and renal events in the Ongoing Telmisartan Alone and in Combination With Ramipril Global Endpoint Trial (ONTARGET). Circulation 124 (2011), 1727–1736.
[65] Anderson, R.J., Bahn, G.D., Emanuele, N.V., Marks, J.B., Duckworth, W.C., Group, V.S., Blood pressure and pulse pressure effects on renal outcomes in the Veterans Affairs Diabetes Trial (VADT). Diabetes Care 37 (2014), 2782–2788.
[66] Leehey, D.J., Zhang, J.H., Emanuele, N.V., Whaley-Connell, A., Palevsky, P.M., Reilly, R.F., et al. BP and renal outcomes in diabetic kidney disease: the veterans affairs nephropathy in diabetes trial. Clin J Am Soc Nephrol 10 (2015), 2159–2169.
[67] Weber, M.A., Bloch, M., Bakris, G.L., Weir, M.R., Zappe, D.H., Dahlof, B., et al. Cardiovascular outcomes according to systolic blood pressure in patients with and without diabetes: an ACCOMPLISH substudy. J Clin Hypertens (Greenwich) 18 (2016), 299–307.
[68] Imai, E., Chan, J.C., Ito, S., Yamasaki, T., Kobayashi, F., Haneda, M., et al. Effects of olmesartan on renal and cardiovascular outcomes in type 2 diabetes with overt nephropathy: a multicentre, randomised, placebo-controlled study. Diabetologia 54 (2011), 2978–2986.
[69] Imai, E., Ito, S., Haneda, M., Harada, A., Kobayashi, F., Yamasaki, T., et al. Effects of blood pressure on renal and cardiovascular outcomes in Asian patients with type 2 diabetes and overt nephropathy: a post hoc analysis (ORIENT-blood pressure). Nephrol Dial Transplant 31 (2016), 447–454.
[70] Pohl, M.A., Blumenthal, S., Cordonnier, D.J., De Alvaro, F., Deferrari, G., Eisner, G., et al. Independent and additive impact of blood pressure control and angiotensin II receptor blockade on renal outcomes in the irbesartan diabetic nephropathy trial: clinical implications and limitations. J Am Soc Nephrol 16 (2005), 3027–3037.
[71] de Galan, B.E., Perkovic, V., Ninomiya, T., Pillai, A., Patel, A., Cass, A., et al. Lowering blood pressure reduces renal events in type 2 diabetes. J Am Soc Nephrol 20 (2009), 883–892.
[72] Gosmanov, A.R., Lu, J.L., Sumida, K., Potukuchi, P.K., Rhee, C.M., Kalantar-Zadeh, K., et al. Synergistic association of combined glycemic and blood pressure level with risk of complications in US veterans with diabetes. J Hypertens 34 (2016), 907–913.
[73] De Cosmo, S., Viazzi, F., Piscitelli, P., Giorda, C., Ceriello, A., Genovese, S., et al. Blood pressure status and the incidence of diabetic kidney disease in patients with hypertension and type 2 diabetes. J Hypertens 34 (2016), 2090–2098.
[74] Uzu, T., Kida, Y., Yamauchi, A., Kume, S., Isshiki, K., Araki, S., et al. The effects of blood pressure control levels on the renoprotection of type 2 diabetic patients without overt proteinuria. J Am Soc Hypertens 6 (2012), 124–131.
[75] Leehey, D.J., Kramer, H.J., Daoud, T.M., Chatha, M.P., Isreb, M.A., Progression of kidney disease in type 2 diabetes – beyond blood pressure control: an observational study. BMC Nephrol, 6, 2005, 8.
[76] Eriksen, B.O., Stefansson, V.T., Jenssen, T.G., Mathisen, U.D., Schei, J., Solbu, M.D., et al. Elevated blood pressure is not associated with accelerated glomerular filtration rate decline in the general non-diabetic middle-aged population. Kidney Int 90 (2016), 404–410.
[77] ACCORD Study Group, Cushman, W.C., Evans, G.W., Byington, R.P., Goff, D.C. Jr., Grimm, R.H. Jr., et al. Effects of intensive blood-pressure control in type 2 diabetes mellitus. N Engl J Med 362 (2010), 1575–1585.
[78] SPRINT Research Group, Wright, J.T. Jr., Williamson, J.D., Whelton, P.K., Snyder, J.K., Sink, K.M., et al. A randomized trial of intensive versus standard blood-pressure control. N Engl J Med 373 (2015), 2103–2116.
[79] O'Hare, A.M., Hotchkiss, J.R., Kurella Tamura, M., Larson, E.B., Hemmelgarn, B.R., Batten, A., et al. Interpreting treatment effects from clinical trials in the context of real-world risk information: end-stage renal disease prevention in older adults. JAMA Intern Med 174 (2014), 391–397.
[80] Bilous, R., Microvascular disease: what does the UKPDS tell us about diabetic nephropathy?. Diabet Med 25:Suppl 2 (2008), 25–29.
[81] Investigators HOPES, Effects of ramipril on cardiovascular and microvascular outcomes in people with diabetes mellitus: results of the HOPE study and MICRO-HOPE substudy. Lancet 355 (2000), 253–259.
[82] Brenner, B.M., Cooper, M.E., de Zeeuw, D., Keane, W.F., Mitch, W.E., Parving, H.H., et al. Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy. N Engl J Med 345 (2001), 861–869.
[83] Lewis, E.J., Hunsicker, L.G., Clarke, W.R., Berl, T., Pohl, M.A., Lewis, J.B., et al. Renoprotective effect of the angiotensin-receptor antagonist irbesartan in patients with nephropathy due to type 2 diabetes. N Engl J Med 345 (2001), 851–860.
[84] Marre, M., Lievre, M., Chatellier, G., Mann, J.F., Passa, P., Menard, J., et al. Effects of low dose ramipril on cardiovascular and renal outcomes in patients with type 2 diabetes and raised excretion of urinary albumin: randomised, double blind, placebo controlled trial (the DIABHYCAR study). BMJ, 328, 2004, 495.
[85] Mann, J.F., Schmieder, R.E., Dyal, L., McQueen, M.J., Schumacher, H., Pogue, J., et al. Effect of telmisartan on renal outcomes: a randomized trial. Ann Intern Med 151:1–10 (2009), W1–W2.
[86] Haller, H., Ito, S., Izzo, J.L. Jr., Januszewicz, A., Katayama, S., Menne, J., et al. Olmesartan for the delay or prevention of microalbuminuria in type 2 diabetes. N Engl J Med 364 (2011), 907–917.
[87] Patel, A., MacMahon, S., Chalmers, J., Neal, B., Woodward, M., Billot, L., et al. Effects of a fixed combination of perindopril and indapamide on macrovascular and microvascular outcomes in patients with type 2 diabetes mellitus (the ADVANCE trial): a randomised controlled trial. Lancet 370 (2007), 829–840.
[88] Zoungas, S., Chalmers, J., Neal, B., Billot, L., Li, Q., Hirakawa, Y., et al. Follow-up of blood-pressure lowering and glucose control in type 2 diabetes. N Engl J Med 371 (2014), 1392–1406.
[89] Heerspink, H.J., Ninomiya, T., Perkovic, V., Woodward, M., Zoungas, S., Cass, A., et al. Effects of a fixed combination of perindopril and indapamide in patients with type 2 diabetes and chronic kidney disease. Eur Heart J 31 (2010), 2888–2896.
[90] Strippoli, G.F., Craig, M., Deeks, J.J., Schena, F.P., Craig, J.C., Effects of angiotensin converting enzyme inhibitors and angiotensin II receptor antagonists on mortality and renal outcomes in diabetic nephropathy: systematic review. BMJ, 329, 2004, 828.
[91] Mann, J.F., Schmieder, R.E., McQueen, M., Dyal, L., Schumacher, H., Pogue, J., et al. Renal outcomes with telmisartan, ramipril, or both, in people at high vascular risk (the ONTARGET study): a multicentre, randomised, double-blind, controlled trial. Lancet 372 (2008), 547–553.
[92] Parving, H.H., Brenner, B.M., McMurray, J.J., de Zeeuw, D., Haffner, S.M., Solomon, S.D., et al. Cardiorenal end points in a trial of aliskiren for type 2 diabetes. N Engl J Med 367 (2012), 2204–2213.
[93] Mavrakanas, T.A., Gariani, K., Martin, P.Y., Mineralocorticoid receptor blockade in addition to angiotensin converting enzyme inhibitor or angiotensin II receptor blocker treatment: an emerging paradigm in diabetic nephropathy: a systematic review. Eur J Intern Med 25 (2014), 173–176.
[94] Hou, J., Xiong, W., Cao, L., Wen, X., Li, A., Spironolactone add-on for preventing or slowing the progression of diabetic nephropathy: a meta-analysis. Clin Ther, 37, 2015 2086–103.e10.
[95] Currie, G., Taylor, A.H., Fujita, T., Ohtsu, H., Lindhardt, M., Rossing, P., et al. Effect of mineralocorticoid receptor antagonists on proteinuria and progression of chronic kidney disease: a systematic review and meta-analysis. BMC Nephrol, 17, 2016, 127.
[96] Komers, R., Plotkin, H., Dual inhibition of renin–angiotensin–aldosterone system and endothelin-1 in treatment of chronic kidney disease. Am J Physiol Regul Integr Comp Physiol 310 (2016), R877–R884.
[97] Vasilakou, D., Karagiannis, T., Athanasiadou, E., Mainou, M., Liakos, A., Bekiari, E., et al. Sodium–glucose cotransporter 2 inhibitors for type 2 diabetes: a systematic review and meta-analysis. Ann Intern Med 159 (2013), 262–274.
[98] Yale, J.F., Bakris, G., Cariou, B., Yue, D., David-Neto, E., Xi, L., et al. Efficacy and safety of canagliflozin in subjects with type 2 diabetes and chronic kidney disease. Diabetes Obes Metab 15 (2013), 463–473.
[99] Heerspink, H.J., Johnsson, E., Gause-Nilsson, I., Cain, V.A., Sjostrom, C.D., Dapagliflozin reduces albuminuria in patients with diabetes and hypertension receiving renin–angiotensin blockers. Diabetes Obes Metab 18 (2016), 590–597.
[100] Kohan, D.E., Fioretto, P., Johnsson, K., Parikh, S., Ptaszynska, A., Ying, L., The effect of dapagliflozin on renal function in patients with type 2 diabetes. J Nephrol 29 (2016), 391–400.
[101] Fioretto, P., Stefansson, B.V., Johnsson, E., Cain, V.A., Sjostrom, C.D., Dapagliflozin reduces albuminuria over 2 years in patients with type 2 diabetes mellitus and renal impairment. Diabetologia 59 (2016), 2036–2039.
[102] Barnett, A.H., Mithal, A., Manassie, J., Jones, R., Rattunde, H., Woerle, H.J., et al. Efficacy and safety of empagliflozin added to existing antidiabetes treatment in patients with type 2 diabetes and chronic kidney disease: a randomised, double-blind, placebo-controlled trial. Lancet Diabetes Endocrinol 2 (2014), 369–384.
[103] Heerspink, H.J., Desai, M., Jardine, M., Balis, D., Meininger, G., Perkovic, V., Canagliflozin slows progression of renal function decline independently of glycemic effects. J Am Soc Nephrol 28 (2017), 368–375.
[104] Cherney, D., Lund, S.S., Perkins, B.A., Groop, P.H., Cooper, M.E., Kaspers, S., et al. The effect of sodium glucose cotransporter 2 inhibition with empagliflozin on microalbuminuria and macroalbuminuria in patients with type 2 diabetes. Diabetologia 9 (2016), 1860–1870.
[105] Muskiet, M.H., van Raalte, D.H., van Bommel, E., Smits, M.M., Tonneijck, L., Understanding EMPA-REG OUTCOME. Lancet Diabetes Endocrinol 3 (2015), 928–929.

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