The diuretic effects of SGLT2 inhibitors: A comprehensive review of their specificities and their role in renal protection.

DELANAYE, Pierre; Scheen, André

doi:10.1016/j.diabet.2021.101285

Article (Scientific journals)

The diuretic effects of SGLT2 inhibitors: A comprehensive review of their specificities and their role in renal protection.

DELANAYE, Pierre; Scheen, André

2021 • In Diabetes & metabolism, 47 (6), p. 101285

Peer reviewed

Permalink
https://hdl.handle.net/2268/264370

DOI
10.1016/j.diabet.2021.101285

PubMed
34597788

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

2021 D&M diuretic effect of sglt2.pdf

Publisher postprint (841.44 kB)

Request a copy

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Diabetic kidney disease; Natriuresis; Osmotic diuresis; Renal outcome; SGLT2 inhibitors

Abstract :

[en] Sodium-glucose cotransporter type 2 inhibitors (SGLT2is) are new oral glucose-lowering agents that provide cardiovascular and renal protection in both patients with and without type 2 diabetes. Because of their unique mechanism of action, increased glucosuria is associated with osmotic diuresis and some natriuresis, yet the latter seems mostly transient. The potential role of the diuretic effect in overall cardiovascular and renal protection by SGLT2is remains a matter of debate. Precise evaluation of the diuretic effect is not so easy and most studies relied upon indirect estimations that led to divergent results, presumably also explained by different study designs and population characteristics. Everybody agrees upon the fact that SGLT2is are different from other classical diuretics (thiazides and loop diuretics) as they present some favourable properties, i.e. reduced sympathetic activity, preserved potassium balance, lower risk of acute renal injury, decrease of serum uric acid level. The potential role of the diuretic effect of SGLT2is on renal outcomes is still unclear, yet their ability to reduce albuminuria and dampen the risk of heart failure may contribute to improve renal prognosis besides other complex underlying mechanisms. In this comprehensive review we first critically analyse the results obtained with indirect methods that assess a diuretic effect of SGLT2is, second we describe the specificities of the diuretic activity of SGLT2is compared with other classical diuretics, and third we discuss the potential mechanisms by which the diuretic effect of SGLT2is could contribute to the improvement of renal outcomes consistently reported with this innovative amazing pharmacological class.

Disciplines :

Urology & nephrology
Pharmacy, pharmacology & toxicology

Author, co-author :

DELANAYE, Pierre ; Centre Hospitalier Universitaire de Liège - CHU > Département de médecine interne > Service de néphrologie

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

Language :

English

Title :

The diuretic effects of SGLT2 inhibitors: A comprehensive review of their specificities and their role in renal protection.

Publication date :

2021

Journal title :

Diabetes & metabolism

ISSN :

1262-3636

eISSN :

1878-1780

Volume :

Issue :

Pages :

101285

Peer reviewed :

Peer reviewed

Commentary :

Available on ORBi :

since 19 October 2021

Statistics

Number of views

76 (2 by ULiège)

Number of downloads

3 (3 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Scheen, A.J., Sodium-glucose co-transporter type 2 inhibitors for the treatment of type 2 diabetes mellitus. Nature Rev Endocrinol 16 (2020), 556–577.
DeFronzo, R.A., Reeves, W.B., Awad, A.S., Pathophysiology of diabetic kidney disease: impact of SGLT2 inhibitors. Nature Rev Nephrol 17 (2021), 319–334.
American Diabetes A. 9. Pharmacologic approaches to glycemic treatment: standards of medical care in diabetes-2021. Diabetes Care 44 (2021), S111–S124.
Butler, J., Usman, M.S., Khan, M.S., Greene, S.J., Friede, T., Vaduganathan, M., et al. Efficacy and safety of SGLT2 inhibitors in heart failure: systematic review and meta-analysis. ESC Heart Failure 7 (2020), 3298–3309.
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.
Zelniker, T.A., Wiviott, S.D., Raz, I., Im, K., Goodrich, E.L., Bonaca, M.P., et al. SGLT2 inhibitors for primary and secondary prevention of cardiovascular and renal outcomes in type 2 diabetes: a systematic review and meta-analysis of cardiovascular outcome trials. Lancet 393 (2019), 31–39.
McMurray, J.J.V., Solomon, S.D., Inzucchi, S.E., Kober, L., Kosiborod, M.N., Martinez, F.A., et al. Dapagliflozin in patients with heart failure and reduced ejection fraction. N Engl J Med 381 (2019), 1995–2008.
Packer, M., Anker, S.D., Butler, J., Filippatos, G., Pocock, S.J., Carson, P., et al. Cardiovascular and renal outcomes with empagliflozin in heart failure. N Engl J Med 383 (2020), 1413–1424.
Anker, S.D., Butler, J., Filippatos, G., Ferreira, J.P., Bocchi, E., Bohm, M., et al. Empagliflozin in heart failure with a preserved ejection fraction. N Engl J Med, 2021, 10.1056/NEJMoa2107038 Aug 27.
Neuen, B.L., Young, T., Heerspink, H.J.L., Neal, B., Perkovic, V., Billot, L., et al. SGLT2 inhibitors for the prevention of kidney failure in patients with type 2 diabetes: a systematic review and meta-analysis. Lancet Diabetes Endocrinol 7 (2019), 845–854.
Delanaye, P., Wissing, K.M., Scheen, A.J., SGLT2 inhibitors: renal outcomes according to baseline albuminuria. Clin Kidney J, 2021, 10.1093/ckj/sfab096 June 11.
Heerspink, H.J.L., Stefansson, B.V., Correa-Rotter, R., Chertow, G.M., Greene, T., Hou, F.F., et al. Dapagliflozin in patients with chronic kidney disease. N Engl J Med 383 (2020), 1436–1446.
McMurray, J., EMPA-REG - the "diuretic hypothesis". J Diabetes Complications 30 (2016), 3–4.
Kimura, G., Diuretic action of sodium-glucose cotransporter 2 inhibitors and its importance in the management of heart failure. Circ J 80 (2016), 2277–2281.
Grodin, J.L., Tang, W.H.W., Sodium-glucose cotransporter-2 Inhibitors and loop diuretics for heart failure: priming the natriuretic and metabolic reserve of the kidney. Circulation 142 (2020), 1055–1058.
Sen, T., Heerspink, H.J.L., A kidney perspective on the mechanism of action of sodium glucose co-transporter 2 inhibitors. Cell Metab 33 (2021), 732–739.
Tuttle, K.R., Brosius, F.C., 3rd, Cavender MA, Fioretto, P., Fowler, K.J., Heerspink, H.J.L., et al. SGLT2 inhibition for CKD and cardiovascular disease in type 2 diabetes: report of a scientific workshop sponsored by the National Kidney Foundation. Am J Kidney Dis 77 (2021), 94–109.
Scheen, A.J., Reappraisal of the diuretic effect of empagliflozin in EMPA-REG OUTCOME: comparison with classic diuretics. Diabetes Metab 42 (2016), 224–233.
Ansary, T.M., Nakano, D., Nishiyama, A., Diuretic effects of sodium glucose cotransporter 2 inhibitors and their influence on the renin-angiotensin system. Int J Mol Sci, 20, 2019 pii: E629.
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.
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.
Kawasoe, S., Maruguchi, Y., Kajiya, S., Uenomachi, H., Miyata, M., Kawasoe, M., et al. Mechanism of the blood pressure-lowering effect of sodium-glucose cotransporter 2 inhibitors in obese patients with type 2 diabetes. BMC Pharmacol Toxicol, 18, 2017, 23.
Amin, N.B., Wang, X., Mitchell, J.R., Lee, D.S., Nucci, G., Rusnak, J.M., 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 17 (2015), 805–808.
Ohara, K., Masuda, T., Murakami, T., Imai, T., Yoshizawa, H., Nakagawa, S., et al. Effects of the sodium-glucose cotransporter 2 inhibitor dapagliflozin on fluid distribution: a comparison study with furosemide and tolvaptan. Nephrology 24 (2019), 904–911.
Damman, K., Beusekamp, J.C., Boorsma, E.M., Swart, H.P., Smilde, T.D.J., Elvan, A., et al. Randomized, double-blind, placebo-controlled, multicentre pilot study on the effects of empagliflozin on clinical outcomes in patients with acute decompensated heart failure (EMPA-RESPONSE-AHF). Eur J Heart Fail 22 (2020), 713–722.
Devineni, D., Vaccaro, N., Polidori, D., Rusch, S., Wajs, E., Effects of hydrochlorothiazide on the pharmacokinetics, pharmacodynamics, and tolerability of canagliflozin, a sodium glucose co-transporter 2 inhibitor, in healthy participants. Clin Ther 36 (2014), 698–710.
Wilding, J.P., Norwood, P., T'Joen, C., Bastien, A., List, J.F., Fiedorek, F.T, A study of dapagliflozin in patients with type 2 diabetes receiving high doses of insulin plus insulin sensitizers: applicability of a novel insulin-independent treatment. Diabetes Care 32 (2009), 1656–1662.
Boorsma, E.M., Beusekamp, J.C., Ter Maaten, J.M., Figarska, S.M., Danser, A.H.J., van Veldhuisen, D.J., et al. Effects of empagliflozin on renal sodium and glucose handling in patients with acute heart failure. Eur J Heart Fail 23 (2021), 68–78.
Scholtes, R.A., Muskiet, M.H.A., van Baar, M.J.B., Hesp, A.C., Greasley, P.J., Karlsson, C., et al. Natriuretic effect of two weeks of dapagliflozin treatment in patients with type 2 diabetes and preserved kidney function during standardized sodium intake: results of the DAPASALT trial. Diabetes Care 44 (2021), 440–447.
Sasaki, T., Seino, Y., Fukatsu, A., Ubukata, M., Sakai, S., Samukawa, Y., Pharmacokinetics, pharmacodynamics, and safety of luseogliflozin in Japanese patients with type 2 diabetes mellitus: a randomized, single-blind, placebo-controlled trial. Adv Ther 32 (2015), 319–340.
Sha, S., Polidori, D., Heise, T., Natarajan, J., Farrell, K., Wang, S.S., et al. Effect of the sodium glucose co-transporter 2 inhibitor canagliflozin on plasma volume in patients with type 2 diabetes mellitus. Diabetes Obes Metab 16 (2014), 1087–1095.
Iijima, H., Kifuji, T., Maruyama, N., Inagaki, N., Pharmacokinetics, pharmacodynamics, and safety of canagliflozin in Japanese patients with type 2 diabetes mellitus. Adv Ther 32 (2015), 768–782.
Tanaka, H., Takano, K., Iijima, H., Kubo, H., Maruyama, N., Hashimoto, T., et al. Factors affecting canagliflozin-induced transient urine volume increase in patients with type 2 diabetes mellitus. Adv Ther 34 (2017), 436–451.
Yasui, A., Lee, G., Hirase, T., Kaneko, T., Kaspers, S., von Eynatten, M., et al. Empagliflozin induces transient diuresis without changing long-term overall fluid balance in Japanese patients with type 2 diabetes. Diabetes Ther 9 (2018), 863–871.
Griffin, M., Rao, V.S., Ivey-Miranda, J., Fleming, J., Mahoney, D., Maulion, C., et al. Empagliflozin in heart failure: diuretic and cardiorenal effects. Circulation 142 (2020), 1028–1039.
Eickhoff, M.K., Dekkers, C.C.J., Kramers, B.J., Laverman, G.D., Frimodt-Moller, M., Jorgensen, N.R., et al. Effects of dapagliflozin on volume status when added to renin-angiotensin system inhibitors. J Clin Med, 8, 2019, 779.
van Bommel, E.J.M., Muskiet, M.H.A., van Baar, M.J.B., Tonneijck, L., Smits, M.M., Emanuel, A.L., et al. The renal hemodynamic effects of the SGLT2 inhibitor dapagliflozin are caused by post-glomerular vasodilatation rather than pre-glomerular vasoconstriction in metformin-treated patients with type 2 diabetes in the randomized, double-blind RED trial. Kidney Int 97 (2020), 202–212.
Komoroski, B., Vachharajani, N., Feng, Y., Li, L., Kornhauser, D., Pfister, M., Dapagliflozin, a novel, selective SGLT2 inhibitor, improved glycemic control over 2 weeks in patients with type 2 diabetes mellitus. Clin Pharmacol Ther 85 (2009), 513–519.
Ellison, D.H., Clinical pharmacology in diuretic use. Clin J Am Soc Nephrol 14 (2019), 1248–1257.
Mordi, N.A., Mordi, I.R., Singh, J.S., McCrimmon, R.J., Struthers, A.D., Lang, C.C., Renal and cardiovascular effects of SGLT2 inhibition in combination with loop diuretics in patients with type 2 diabetes and chronic heart failure: the RECEDE-CHF trial. Circulation 142 (2020), 1713–1724.
Fukuoka, S., Dohi, K., Takeuchi, T., Moriwaki, K., Ishiyama, M., Omori, T., et al. Mechanisms and prediction of short-term natriuretic effect of sodium-glucose cotransporter 2 inhibitor in heart failure patients coexisting type 2 diabetes mellitus. Heart Vessels 35 (2020), 1218–1226.
Fathi, A., Vickneson, K., Singh, J.S., SGLT2-inhibitors; more than just glycosuria and diuresis. Heart Fail Rev 26 (2021), 623–642.
Bjornstad, P., Greasley, P.J., Wheeler, D.C., Chertow, G.M., Langkilde, A.M., Heerspink, H.J.L., et al. The potential roles of osmotic and nonosmotic sodium handling in mediating the effects of sodium-glucose cotransporter 2 inhibitors on heart failure. J Card Fail, 2021 Jul 18;S1071-9164(21)00291-8.
Heerspink, H.J.L., 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.
Dekkers, C.C.J., Sjostrom, C.D., Greasley, P.J., Cain, V., Boulton, D.W., Heerspink, H.J.L., Effects of the SGLT2 inhibitor dapagliflozin on estimated plasma volume in patients with type 2 diabetes. Diabetes Obes Metab 21 (2019), 2667–2673.
Jensen, J., Omar, M., Kistorp, C., Tuxen, C., Gustafsson, I., Kober, L., et al. Effects of empagliflozin on estimated extracellular volume, estimated plasma volume, and measured glomerular filtration rate in patients with heart failure (Empire HF Renal): a prespecified substudy of a double-blind, randomised, placebo-controlled trial. Lancet Diabetes Endocrinol 9 (2021), 106–116.
Nassif, M.E., Windsor, S.L., Tang, F., Husain, M., Inzucchi, S.E., McGuire, D.K., et al. Dapagliflozin effects on lung fluid volumes in patients with heart failure and reduced ejection fraction: results from the DEFINE-HF trial. Diabetes Obes Metab 23 (2021), 1426–1430.
Hallow, K.M., Helmlinger, G., Greasley, P.J., McMurray, J.J.V., Boulton, D.W., Why do SGLT2 inhibitors reduce heart failure hospitalization? A differential volume regulation hypothesis. Diabetes Obes Metab 20 (2018), 479–487.
Mullens, W., Martens, P., Empagliflozin and renal sodium handling: an intriguing smart osmotic diuretic. Eur J Heart Fail 23 (2021), 79–82.
Schork, A., Saynisch, J., Vosseler, A., Jaghutriz, B.A., Heyne, N., Peter, A., et al. Effect of SGLT2 inhibitors on body composition, fluid status and renin-angiotensin-aldosterone system in type 2 diabetes: a prospective study using bioimpedance spectroscopy. Cardiovasc Diabetol, 18, 2019, 46.
Ohara, K., Masuda, T., Morinari, M., Okada, M., Miki, A., Nakagawa, S., et al. The extracellular volume status predicts body fluid response to SGLT2 inhibitor dapagliflozin in diabetic kidney disease. Diabetol Metab Syndr, 12, 2020, 37.
Docherty, K.F., Jhund, P.S., Inzucchi, S.E., Kober, L., Kosiborod, M.N., Martinez, F.A., et al. Effects of dapagliflozin in DAPA-HF according to background heart failure therapy. Eur Heart J 41 (2020), 2379–2392.
Jhund, P.S., Solomon, S.D., Docherty, K.F., Heerspink, H.J.L., Anand, I.S., Bohm, M., et al. Efficacy of dapagliflozin on renal function and outcomes in patients with heart failure with reduced ejection fraction: results of DAPA-HF. Circulation 143 (2021), 298–309.
Nomiyama, T., Shimono, D., Horikawa, T., Fujimura, Y., Ohsako, T., Terawaki, Y., et al. Efficacy and safety of sodium-glucose cotransporter 2 inhibitor ipragliflozin on glycemic control and cardiovascular parameters in Japanese patients with type 2 diabetes mellitus; Fukuoka Study of Ipragliflozin (FUSION). Endocr J 65 (2018), 859–867.
List, J.F., Woo, V., Morales, E., Tang, W., Fiedorek, F.T., Sodium-glucose cotransport inhibition with dapagliflozin in type 2 diabetes. Diabetes Care 32 (2009), 650–657.
Mazer, C.D., Hare, G.M.T., Connelly, P.W., Gilbert, R.E., Shehata, N., Quan, A., et al. Effect of empagliflozin on erythropoietin levels, iron stores and red blood cell morphology in patients with type 2 diabetes and coronary artery disease. Circulation 141 (2020), 704–707.
Ghanim, H., Abuaysheh, S., Hejna, J., Green, K., Batra, M., Makdissi, A., et al. Dapagliflozin suppresses hepcidin and increases erythropoiesis. J Clin Endocrinol Metab, 2020, 105.
Sano, M., Takei, M., Shiraishi, Y., Suzuki, Y., Increased hematocrit during sodium-glucose cotransporter 2 inhibitor therapy indicates recovery of tubulointerstitial function in diabetic kidneys. J Clin Med Res 8 (2016), 844–847.
Lee, P.C., Ganguly, S., Goh, S.Y., Weight loss associated with sodium-glucose cotransporter-2 inhibition: a review of evidence and underlying mechanisms. Obes Rev 19 (2018), 1630–1641.
Bolinder, J., Ljunggren, O., Kullberg, J., Johansson, L., Wilding, J., Langkilde, A.M., et al. 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 97 (2012), 1020–1031.
Scheen, A.J., Type 2 diabetes and thiazide diuretics. Curr. Diab. Rep., 18, 2018, 6.
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.
Sternlicht, H., Bakris, G.L., Blood pressure lowering and sodium-glucose co-transporter 2 inhibitors (SGLT2is): more than osmotic diuresis. Curr Hypertens Rep, 21, 2019, 12.
Wile, D., Diuretics: a review. Ann Clin Biochem 49 (2012), 419–431.
Verma, A., Patel, A.B., Waikar, S.S., SGLT2 inhibitor: not a traditional diuretic for heart failure. Cell Metab 32 (2020), 13–14.
Scheen, A.J., Effect of SGLT2 inhibitors on the sympathetic nervous system and blood pressure. Curr Cardiol Rep, 21, 2019, 70.
Herat, L.Y., Magno, A.L., Rudnicka, C., Hricova, J., Carnagarin, R., Ward, N.C., et al. SGLT2 inhibitor-induced sympathoinhibition: a novel mechanism for cardiorenal protection. JACC Basic Transl Sci 5 (2020), 169–179.
Shimizu, W., Kubota, Y., Hoshika, Y., Mozawa, K., Tara, S., Tokita, Y., et al. Effects of empagliflozin versus placebo on cardiac sympathetic activity in acute myocardial infarction patients with type 2 diabetes mellitus: the EMBODY trial. Cardiovasc Diabetol, 19, 2020, 148.
Lymperopoulos, A., Borges, J.I., Cora, N., Sizova, A., Sympatholytic mechanisms for the beneficial cardiovascular effects of SGLT2 inhibitors: a research hypothesis for dapagliflozin's effects in the adrenal gland. Int J Mol Sci, 22, 2021, 7684.
Lin, Z., Wong, L.Y.F., Cheung, B.M.Y., Diuretic-induced hypokalaemia: an updated review. Postgrad Med J, 2021 Mar 9;postgradmedj-2020-139701.
Greenberg, A., Diuretic complications. Am J Med Sci 319 (2000), 10–24.
Weir, M.R., Slee, A., Sun, T., Balis, D., Oh, R., de Zeeuw, D., et al. Effects of canagliflozin on serum potassium in the CANagliflozin cardioVascular Assessment Study (CANVAS) Program. Clin Kidney J 14 (2021), 1396–1402.
Yavin, Y., Mansfield, T.A., Ptaszynska, A., Johnsson, K., Parikh, S., Johnsson, E., Effect of the SGLT2 inhibitor dapagliflozin on potassium levels in patients with type 2 diabetes mellitus: a pooled analysis. Diabetes Ther 7 (2016), 125–137.
Hwang, Y.J., Lyu, B., Chang, A.R., Inker, L.A., Grams, M.E., Shin, J.I., Sodium-glucose cotransporter-2 inhibitors and the risk of abnormal serum potassium level. Clin J Am Soc Nephrol 16 (2021), 1094–1096.
Neuen, B.L., Oshima, M., Perkovic, V., Agarwal, R., Arnott, C., Bakris, G., et al. Effects of canagliflozin on serum potassium in people with diabetes and chronic kidney disease: the CREDENCE trial. Eur Heart J, 2021, ehab497 Aug 23.
Toto, R.D., Goldenberg, R., Chertow, G.M., Cain, V., Stefansson, B.V., Sjostrom, C.D., et al. Correction of hypomagnesemia by dapagliflozin in patients with type 2 diabetes: a post hoc analysis of 10 randomized, placebo-controlled trials. J Diabetes Complications, 33, 2019, 107402.
Oost, L.J., van der Heijden, A., Vermeulen, E.A., Bos, C., Elders, P.J.M., Slieker, R.C., et al. Serum magnesium is inversely associated with heart failure, atrial fibrillation, and microvascular complications in type 2 diabetes. Diabetes Care 44 (2021), 1757–1765.
Bell, D.S.H., Goncalves, E., Diabetogenic effects of cardioprotective drugs. Diabetes Obes Metab 23 (2021), 877–885.
Papaetis, G.S., Empagliflozin therapy and insulin resistance-associated disorders: effects and promises beyond a diabetic state. Arch Med Sci Atheroscler Dis 6 (2021), e57–e78.
Kielstein, J.T., Pontremoli, R., Burnier, M., Management of hyperuricemia in patients with chronic kidney disease: a focus on renal protection. Curr Hypertens Rep, 22, 2020, 102.
Zhao, Y., Xu, L., Tian, D., Xia, P., Zheng, H., Wang, L., et al. Effects of sodium-glucose co-transporter 2 (SGLT2) inhibitors on serum uric acid level: a meta-analysis of randomized controlled trials. Diabetes Obes Metab 20 (2018), 458–462.
Ahmadieh, H., Azar, S., Effects of sodium glucose cotransporter-2 inhibitors on serum uric acid in type 2 diabetes mellitus. Diabetes Technol Ther 19 (2017), 507–512.
Johnsson, K., Johnsson, E., Mansfield, T.A., Yavin, Y., Ptaszynska, A., Parikh, S.J., Osmotic diuresis with SGLT2 inhibition: analysis of events related to volume reduction in dapagliflozin clinical trials. Postgrad Med 128 (2016), 346–355.
Scott, J., Jones, T., Redaniel, M.T., May, M.T., Ben-Shlomo, Y., Caskey, F., Estimating the risk of acute kidney injury associated with use of diuretics and renin angiotensin aldosterone system inhibitors: a population based cohort study using the clinical practice research datalink. BMC Nephrol, 20, 2019, 481.
Menne, J., Dumann, E., Haller, H., Schmidt, B.M.W., Acute kidney injury and adverse renal events in patients receiving SGLT2-inhibitors: a systematic review and meta-analysis. PLoS Med, 16, 2019, e1002983.
Heerspink, H.J.L., Oshima, M., Zhang, H., Li, J., Agarwal, R., Capuano, G., et al. Canagliflozin and kidney-related adverse events in type 2 diabetes and CKD: findings from the randomized CREDENCE trial. Am J Kidney Dis, 2021 May 23;S0272-6386(21)00626-0.
Mayer, G.J., Wanner, C., Weir, M.R., Inzucchi, S.E., Koitka-Weber, A., Hantel, S., et al. Analysis from the EMPA-REG OUTCOME((R)) trial indicates empagliflozin may assist in preventing the progression of chronic kidney disease in patients with type 2 diabetes irrespective of medications that alter intrarenal hemodynamics. Kidney Int 96 (2019), 489–504.
Sridhar, V.S., Tuttle, K.R., Cherney, D.Z.I., We can finally stop worrying about SGLT2 inhibitors and acute kidney injury. Am J Kidney Dis 76 (2020), 454–456.
Zannad, F., Rossignol, P., Cardiorenal syndrome revisited. Circulation 138 (2018), 929–944.
Bouquegneau, A., Krzesinski, J.M., Delanaye, P., Cavalier, E., Biomarkers and physiopathology in the cardiorenal syndrome. Clin Chim Acta 443 (2015), 100–107.
Delanaye, P., Scheen, A.J., Preventing and treating kidney disease in patients with type 2 diabetes. Expert Opin Pharmacother 20 (2019), 277–294.
Heerspink, H.J.L., Greene, T., Tighiouart, H., Gansevoort, R.T., Coresh, J., Simon, A.L., et al. Change in albuminuria as a surrogate endpoint for progression of kidney disease: a meta-analysis of treatment effects in randomised clinical trials. Lancet Diabetes Endocrinol 7 (2019), 128–139.
Buter, H., Hemmelder, M.H., Navis, G., de Jong, P.E., de Zeeuw, D., The blunting of the antiproteinuric efficacy of ACE inhibition by high sodium intake can be restored by hydrochlorothiazide. Nephrol Dial Transplant 13 (1998), 1682–1685.
Esnault, V.L., Ekhlas, A., Delcroix, C., Moutel, M.G., Nguyen, J.M., Diuretic and enhanced sodium restriction results in improved antiproteinuric response to RAS blocking agents. J Am Soc Nephrol 16 (2005), 474–481.
Trujillo, H., Caravaca-Fontan, F., Caro, J., Morales, E., Praga, M., The forgotten antiproteinuric properties of diuretics. Am J Nephrol 52 (2021), 435–449.
Bakris, G.L., Agarwal, R., Anker, S.D., Pitt, B., Ruilope, L.M., Rossing, P., et al. Effect of finerenone on chronic kidney disease outcomes in type 2 diabetes. N Engl J Med 383 (2020), 2219–2229.
Pitt, B., Filippatos, G., Agarwal, R., Anker, S.D., Bakris, G.L., Rossing, P., et al. Cardiovascular events with finerenone in kidney disease and type 2 diabetes. N Engl J Med, 2021, 10.1056/NEJMoa2110956 Aug 28.
Piperidou, A., Sarafidis, P., Boutou, A., Thomopoulos, C., Loutradis, C., Alexandrou, M.E., et al. The effect of SGLT-2 inhibitors on albuminuria and proteinuria in diabetes mellitus: a systematic review and meta-analysis of randomized controlled trials. J Hypertens 37 (2019), 1334–1343.
Bae, J.H., Park, E.G., Kim, S., Kim, S.G., Hahn, S., Kim, N.H., Effects of sodium-glucose cotransporter 2 inhibitors on renal outcomes in patients with type 2 diabetes: a systematic review and meta-analysis of randomized controlled trials. Sci Rep, 9, 2019, 13009.
Sternlicht, H.K., Bakris, G.L., Reductions in albuminuria with SGLT2 inhibitors: a marker for improved renal outcomes in patients without diabetes?. Lancet Diabetes Endocrinol 8 (2020), 553–555.
Oshima, M., Neuen, B.L., Li, J., Perkovic, V., Charytan, D.M., de Zeeuw, D., et al. Early change in albuminuria with canagliflozin predicts kidney and cardiovascular outcomes: a post hoc analysis from the CREDENCE trial. J Am Soc Nephrol 31 (2020), 2925–2936.
Waijer, S.W., Xie, D., Inzucchi, S.E., Zinman, B., Koitka-Weber, A., Mattheus, M., et al. Short-term changes in albuminuria and risk of cardiovascular and renal outcomes in type 2 diabetes mellitus: a post hoc analysis of the EMPA-REG OUTCOME trial. J Am Heart Assoc, 9, 2020, e016976.
Felker, G.M., Ellison, D.H., Mullens, W., Cox, Z.L., Testani, J.M., Diuretic therapy for patients with heart failure: JACC state-of-the-art review. J Am Coll Cardiol 75 (2020), 1178–1195.
Thakar, C.V., Christianson, A., Himmelfarb, J., Leonard, A.C., Acute kidney injury episodes and chronic kidney disease risk in diabetes mellitus. Clin J Am Soc Nephrol 6 (2011), 2567–2572.
Clark, A.L., Kalra, P.R., Petrie, M.C., Mark, P.B., Tomlinson, L.A., Tomson, C.R., Change in renal function associated with drug treatment in heart failure: national guidance. Heart 105 (2019), 904–910.
Kuriyama, S., A potential mechanism of cardio-renal protection with sodium-glucose cotransporter 2 inhibitors: amelioration of renal congestion. Kidney Blood Press Res 44 (2019), 449–456.
Pellicori, P., Fitchett, D., Kosiborod, M.N., Ofstad, A.P., Seman, L., Zinman, B., et al. Use of diuretics and outcomes in patients with type 2 diabetes: findings from the EMPA-REG OUTCOME trial. Eur J Heart Fail 23 (2021), 1085–1093.
Packer, M., Butler, J., Zannad, F., Pocock, S.J., Filippatos, G., Ferreira, J.P., et al. Empagliflozin and major renal outcomes in heart failure. N Engl J Med, 2021, 10.1056/NEJMc2112411 Aug 27.
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.
Cooper, M.E., Inzucchi, S.E., Zinman, B., Hantel, S., von Eynatten, M., Wanner, C., et al. Glucose control and the effect of empagliflozin on kidney outcomes in type 2 diabetes: an analysis from the EMPA-REG OUTCOME trial. Am J Kidney Dis 74 (2019), 713–715.
Scheen, A.J., Delanaye, P., Effects of reducing blood pressure on renal outcomes in patients with type 2 diabetes: focus on SGLT2 inhibitors and EMPA-REG OUTCOME. Diabetes Metab 43 (2017), 99–109.