Implementing the new NICE guidelines for type 2 diabetes (NG28): Focusing beyond HbA1c targets and clinically phenotyping patients to the appropriate second-line agent

LAKSHMINARAYANAN VARADHAN,1 PONNUSAMY SARAVANAN,2 SARAH N ALI,3 WASIM HANIF,4 VINOD PATEL5

1 Royal Stoke University Hospital, University Hospitals of North Midlands NHS Trust, Stoke on Trent, UK
2 Division of Health Sciences, Warwick Medical School, University of Warwick, Coventry, UK; Academic Department of Diabetes, Endocrinology and Metabolism, George Eliot Hospital NHS Trust, Nuneaton, UK
3 Department of Diabetes and Endocrinology, Royal Free London NHS Foundation Trust, Pond Street, London, UK
4 University Hospitals Birmingham NHS Foundation Trust, Mindelsohn Way, Edgbaston, Birmingham, UK
5 Warwick Medical School, University of Warwick; Hon Consultant in Endocrinology and Diabetes, Acute Medicine, Medical Obstetrics, Diabetes and Endocrinology Centre, George Eliot Hospital NHS Trust, Nuneaton, UK

Address for correspondence: Dr Lakshminarayanan Varadhan Consultant Physician, Diabetes and Endocrinology, Royal Stoke University Hospital, University Hospitals of North Midlands NHS Trust, Stoke on Trent, ST4 6QG, UK
E-mail: laks.varadhan@gmail.com

https://doi.org/10.15277/bjd.2022.385

Abstract

A significant number of cardiovascular outcome trials have been published to support decision-making regarding treatment options after or alongside metformin in people with type 2 diabetes (T2DM), specifically targeting prevention of adverse cardiovascular and renal outcomes. The latest NICE guidelines recommend the use of sodium-glucose transport inhibitors (SGLT2i) in patients with cardiovascular diseases, heart failure and chronic kidney disease with diabetes and recommends the use of glucagon-like polypeptide receptor agonists (GLP-1RA) only in a selected group of patients. A comprehensive summary of the various trials, structured around patient characteristics and clinical outcomes, can help to compare the various classes of drugs and drugs within the class. Since the drug acquisition cost within a class is generally the same in the UK, the drug with the best available evidence in the class should be chosen to maximise clinical benefit for the patient. Clinical phenotyping, a process of aligning a patient to the inclusion criteria and the desired clinical outcomes of a trial, can guide the choice of the best drug within a class.

Br J Diabetes 2022;22:87-94

Key words: SGLT2i, clinical phenotyping, NICE

Introduction and methods

The management of type 2 diabetes (T2DM) should now include strategies to reduce adverse cardiovascular and renal outcomes concurrently alongside management of HbA1c. There is an overwhelming evidence base available in patients with established atherosclerotic cardiovascular disease (ASCVD), heart failure (HF) and chronic kidney disease (CKD) demonstrating reduction of significant clinical outcomes: major adverse cardiovascular events (MACE-cardiovascular deaths, non-fatal strokes or non-fatal myocardial infarction), hospitalisation for heart failure (hHF) and progression of CKD. The Association of British Clinical Diabetologists (ABCD) has published a comprehensive summary of the relevant cardiovascular outcome trials (CVOTs), dedicated CKD and HF trials in people taking glucagon-like polypeptide receptor agonists (GLP-1RA), sodium-glucose co-transporter inhibitor (SGLT2i) and dipeptidyl peptidase-4 inhibitor (DPP-4i) drugs.1 The recently published National Institute for health and Care Excellence (NICE) guidelines on type 2 diabetes (NG28) recommends: “at any stage after they have started first-line treatment, if they have or develop chronic heart failure or established ASCVD, offer an SGLT2i with proven cardiovascular benefit in addition to current treatment or replace an existing drug with the SGLT2 inhibitor”.2 An SGLT2i is therefore prioritised as an add-on to metformin in people with high CV risk and as the second-line drug option for diabetes management.3 A GLP-1RA is recommended only in a selected group of people with weight-related issues.

During a clinical consultation, once the choice of the class of drug has been decided based on the patient’s clinical assessment (add-on SGLT2i therapy or GLP-1RA) there is scope also to choose a particular drug within that class. Though the CVOTs may appear similar in terms of establishing CV safety, there are differences in the inclusion criteria and the endpoints measured. For instance, in the EMPA-REG OUTCOME trial, presence of ASCVD was an essential inclusion criterion and the trial achieved significant improvement in MACE, whereas in DECLARE-TIMI 58 only 41% had ASCVD and the reduction in MACE was not significant.4,5 Therefore, classifying the evidence base available based on the patient characteristics included and the clinical outcomes assessed can help to individualise the drug choice. The process of aligning a patient to a clinical trial, referred as clinical phenotyping, would help to maximise evidence-based practice of medicine.

We previously published a step-wise, deliberations-based, approach to the consultation process based on patient characteristics, clinical phenotyping and a clinical cost calculator (YoDa – years of drug administration; calculated as a product of NNT, duration of trial and drug acquisition cost, as a cost estimate to derive a particular benefit) to compare various SGLT2i to achieve a similar endpoint.6 The current paper provides a summary of the relevant clinical trials on SGLT2i, GLP-1RA and DPP-4i with their broad inclusion criteria and relevant clinical endpoints in a comparable format (Table 1) and a simplified summary to aid therapeutic decision-making by prescribers in clinical practice (Table 2). A summary of SGLT2i trials specifically in a patient-friendly format is also provided to facilitate patient involvement and shared-decision making (Table 3). The following approach could help in step-wise decision making process

Does the patient have ASCVD?

The main clinical intent of using an SGLT2i in treating patients with ASCVD [includes established ASCVD (myocardial infarction, stroke or peripheral vascular disease – angioplasty or amputation) or very high risk for CV events (unstable angina, angiographically proven significant vascular disease, positive stress test or high ankle-brachial pressure index)] is prevention of MACE. Among dedicated SGLT2i CVOTs on ASCVD, empagliflozin showed significant reduction in MACE; the trial involving ertugliflozin was only a non-inferiority trial. Of the GLP-1RA CVOTs, albiglutide (not available for clinical use now) showed clinical benefits and lixisenatide did not.4,7-9

A number of other CVOTs included patients with ASCVD and/or CV risk factors. Canagliflozin, liraglutide, semaglutide s/c (subcutaneous once weekly) and dulaglutide demonstrated significant reduction in MACE.10-13 Dapagliflozin and oral semaglutide did not show this benefit.5,14 However, post-hoc or exploratory analyses of CVOTs analysing the ASCVD cohort separately showed CV benefits with canagliflozin, dapagliflozin and liraglutide (Table 1).15-18 The CV benefits with SGLT2i drugs were incremental over pre-established treatments with renin-angiotensin-aldosterone system (RAAS) drugs, statins and anti-platelet therapy. The DPP-4i did not show any benefit with CV outcomes.19-22

Does the patient have HF?

Empaglifozin and dapagliflozin have shown significant reduction in hHF or CV deaths in patients with HF with reduced ejection fraction (HFrEF), with or without diabetes.23,24 A sub-study from CANVAS trial showed benefit for hHF with canagliflozin.25 Other SGLT2i CVOTs have included patients with HF but the inclusion criteria were not comparable (Table 1, 2). Empagliflozin has also subsequently shown significant benefits in patients with preserved ejection fraction heart failure (HFpEF).26 The DPP-4i or GLP-1RA CVOTs have not shown any significant benefit with respect to HF outcomes; the SAVOR-TIMI 53 trial demonstrated an increased signal for hHF with saxagliptin.21

Does the patient have CKD?

The renal composite endpoint assessed in the trials broadly includes doubling of serum creatinine, progression to renal replacement therapy or death from renal disease (with some marginal differences between trials). NICE recommends the use of an SGLT2i in patients with CKD with urine albumin creatinine ratio >30mg/mmol and consider its addition if this is between 3-30mg/mmol, to delay the progression of nephropathy.2 Dapagliflozin and canagliflozin have shown significant renal benefits, with individual benefits for decline of eGFR and progression to renal replacement therapy (RRT) in patients with significant diabetic nephropathy.27,28 CVOTs have also demonstrated benefit with the composite renal outcomes and/or more specific renal outcomes (Table 1).

941 Varadhan Table 1a

941 Varadhan Table 1b

In addition to CKD benefits, the CVOTs have also demonstrated CV benefits, with no heterogeneity noted across various GFR ranges. Further, analytical studies of CVOTs have also been published on empagliflozin, canagliflozin and liraglutide, demonstrating significant cardiovascular benefits among patients with low GFR.29-31

Addressing CV risk

High cardiovascular risk
NICE also advises consideration of an SGLT2i with a proven CV benefit at any stage of diabetes management in patients with high risk of CVD. This is defined as a QRISK2 score ≥10% (QRISK2 incorporates multiple CV risk factors under one metric [hypertension, smoking, dyslipidemia, obesity and family history of premature CVD]) or an elevated lifetime CV risk, defined as age <40 years and presence of 1 or more CV risk factors.32 Most patients who are already established on statin therapy for primary prevention can be considered to belong to this category. A number of studies included patients with multiple risk factors in various combinations in their trials (table 1: ASCVD 1(b) and 4). The trials have generally demonstrated lack of heterogeneity amongst subgroups with or without ASVD; some trials have also published post-hoc analyses specifically on CV risk cohorts.16-18,33 Clinical phenotyping, based on patient characteristics and desired clinical outcomes (Table 2,3), can help to choose among the SGLT2i.

941 Varadhan Table 2

941 Varadhan Table 3

Sub-optimal HbA1c and low QRISK2 OR age > 40 with CV risk factors
This deliberation is relevant in choosing the appropriate second-line or third-line drug in diabetes. As per NICE, the choice here would be between SGLT2i, DPP-4i, sulphonylureas and pioglitazone for second-line therapy.2 SGLT2i have significant cardiovascular and renal benefits and hence must be ideal second-line drugs, ahead of the others in the class (Table 1 and 3). Clinical phenotyping can be relevant when choosing an appropriate SGLT2i to maximize the application of evidence-based medicine in practice (Table 3).NICE has recommended the use of GLP-1RA in a selected group of patients - if triple therapy fails, one of the drugs could be substituted with GLP-1RA in patients with obesity, or where weight loss would provide desirable benefit or insulin initiation can have occupational implications. Again, clinical phenotyping could help to choose the best GLP-1RA for a particular patient, for a desired clinical outcome (Table 2). The following points could help to guide decision-making:

Both SGLT2i and GLP-1RA have supporting data for renal composite endpoints: the former are more consistent with development of new macroalbuminuria and the latter with progression of albuminuria. Amongst GLP-1RA, lixisenatide, semaglutide s/c, liraglutide and dulaglutide showed reduction in incident new macroalbuminura.9,11-13 Linagliptin, empagliflozin and canagliflozin showed evidence of reduction of albuminuria progression.4,10,20

Both SGLT2i and GLP-1RA appear to have reasonable evidence towards reduction of MACE in this cohort. Canagliflozin, liraglutide and dulaglutide demonstrated this in CVOTs, and semaglutide s/c in both CVOT and post-hoc analyses.16-18,33

SGLT2i have a better evidence base for reduction of hHF, whereas GLP-1RA and DPP-4i do not. Saxagliptin shows some signals towards worsening of HF.21

Though the papers may quote a comparable clinical benefit, the cost associated in achieving this and the clinical running costs for GLP-1RA are significantly different and need to be taken into consideration.

Previously published data have shown a comparison of benefits of using SGLT2i and GLP-1RA in clinical practice, which provide some guidance on head-to-head comparison trials.34 The NICE guidelines have provided a clear steer towards using SGLT2i ahead of GLP-1RA therapy, and this article can help to decide the best drug within the class for a given patient.34

Low-risk patient, to optimise individualized HbA1c target Most of the published trials looking at this specific cohort were conducted on an intention-to-treat basis and hence would not provide significant data on cardiovascular prevention. The choice of drugs in this cohort would generally be driven by factors such as cost, risk of weight gain, hypoglycaemia and clinician and patient preferences. CVD-REAL compared the efficacy of SGLT2i versus other oral glucose-lowering drugs in routine clinical practice and found comparable benefits in clinical endpoints irrespective of pre-existent CVD. EMPRISE published a comparative study on real-life use of empagliflozin in comparison to sitagliptin.35-37 These studies showed the consistent effect of SGLT2i outside trial settings and reflect clinical practice, with a mixed combination of patient characteristics.

941 Varadhan Key Messages

Discussion

Clinical phenotyping can help to broadly align a patient with T2DM to the trial evidence available based on his clinical characteristics, and can incorporate individualised decision-making into routine clinical practice. Our proposed approach helps to phenotype a patient as ASCVD, HF, CKD or high CV risk irrespective of their HbA1c, providing an accessible summary of the trial evidence for the drugs that can be used as second-line agents after or alongside metformin (Table 3).

There are a few factors to take into consideration with this approach.

The NICE guidelines clearly steer clinicians towards the use of SGLT2i as a preferred second add-on drug in people with high CV risk. In the UK, with the drug acquisition cost within a class being generally the same, the choice of a drug within the class can be guided by the available evidence base. However, the heterogeneity seen in the trials of a particular class of drugs may not be due to drug inefficiency but merely due to trial design and inclusion criteria.

The positive outcomes of a trial are not necessarily achievable in real-life clinical practice. Further, it cannot be assumed that clinical benefits will continue to increase or that they will be maintained beyond the duration of the trial.

Patients may fit into more than one clinical phenotype and desired clinical outcome can be multiple. Individualising trial evidence to a particular patient can be challenging and HbA1c optimisation always takes priority during clinical care.

The cost of the drug to accrue a particular benefit does not equate to the cost of acquiring the drug. The numbers needed to treat, duration of the trials and time to reach the desired outcomes are different and hence have an implication for the cost involved to accrue particular benefit. These data are again grossly different between the trials and make this cost calculation challenging.6

The clinical evidence available from clinical trials, together with the steer from the new NICE guideline, will inevitably result in an increase in the number of prescriptions of second-line agents for diabetes care, particularly SGLT2i. It is important for reasons of cost efficiency and patient outcomes that agents with the best evidence are considered for CV protection in people with diabetes.

Conclusion

Clinical phenotyping can help to map a patient based on their clinical characteristics to particular trials, which would then help to choose a class of drug, and a drug within that class. The drug choices can be made according to the clinical endpoints desired. This approach would help to align management plans to current NICE guidelines and evidence-based medicine.

Conflict of interest VP has worked with a large number of Pharmaceutical companies in the field of diabetes care. This includes: AstraZeneca, Boehringer Ingelheim, Knapp, MSD, Lilly, Novo, Sanofi, Takeda, Mylan. Has received payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events / all major companies in Diabetes Care. All profits to Charity. Has had support for attending meetings and/or travel - Occasional funded travel. Max twice a year; SA is a consultant diabetologist on the NICE guidelines committee; WA Trustee Diabetes UK, Trustee South Asian Health Foundation, Non Executive Director BMJ, Chair DMMAG Birmingham. All other authors have nothing to declare.

Funding None.

References

  1. Basu A, Patel D, Winocour P, Ryder REJ. Cardiovascular impact of new drugs (GLP-1 and gliflozins): The ABCD position statement. Br J Diabetes 2021; 21:132-48. https://doi.org/10.15277/bjd.2021.283
  2. NICE Guideline NG28: Type 2 diabetes in adults: management. 2022; Available at: https://www.nice.org.uk/guidance/ng28. Accessed 11/03/, 2022.
  3. Moran GM, Bakhai C, Song SH, Agwu JC, Guideline Committee. Type 2 diabetes: summary of updated NICE guidance. BMJ 2022;377:o775. https://doi.org/10.1136/bmj.0775
  4. Zinman B, Wanner C, Lachin JM, et al. Empagliflozin, Cardiovascular Outcomes, and Mortality in Type 2 Diabetes. N Engl J Med 2015;373(22):2117-28. https://doi.org/10.1056/NEJMoa1504720
  5. Wiviott SD, Raz I, Bonaca MP, et al. Dapagliflozin and Cardiovascular Outcomes in Type 2 Diabetes. N Engl J Med 2019;380(4):347-57. https://doi.org/10.1056/NEJMoa1812389
  6. Varadhan L, Saravanan P, Ali SN, Hanif W, Patel V. Informing and Empowering Patients and Clinicians to Make Evidence-Supported Outcome-Based Decisions in Relation to SGLT2 Inhibitor Therapies: The Use of the Novel Years of Drug administration (YoDa) Concept. Clin Drug Investig 2022;42(2):113-25. https://doi.org/10.1007/s40261-021-01105-07
  7. Hernandez AF, Green JB, Janmohamed S, et al. Albiglutide and cardiovascular outcomes in patients with type 2 diabetes and cardiovascular disease (Harmony Outcomes): a double-blind, randomised placebo-controlled trial. Lancet 2018;392(10157):1519-29. https://doi.org/10.1016/S0140-6736(18)32261-x
  8. Cannon CP, Pratley R, Dagogo-Jack S, et al. Cardiovascular Outcomes with Ertugliflozin in Type 2 Diabetes. N Engl J Med 2020;383(15):1425-35. https://doi.org/10.1056/NEJMoa2004967
  9. Pfeffer MA, Claggett B, Diaz R, et al. Lixisenatide in Patients with Type 2 Diabetes and Acute Coronary Syndrome. N Engl J Med 2015;373(23):2247- 2257. https://doi.org/10.NEJMoa1509225
  10. Neal B, Perkovic V, Mahaffey KW, et al. Canagliflozin and Cardiovascular and Renal Events in Type 2 Diabetes. N Engl J Med 2017;377(7):644-57. https://doi.org/10.1056/NEJMoa1611925
  11. Marso SP, Daniels GH, Brown-Frandsen K, et al. Liraglutide and Cardiovascular Outcomes in Type 2 Diabetes. N Engl J Med 2016;375(4):311-22. https://doi.org/10.1056/NEJMoa1603827
  12. Marso SP, Bain SC, Consoli A, et al. Semaglutide and cardiovascular outcomes in patients with type 2 diabetes. N Engl J Med 2016;375(19):1834-44. https://doi.org/10.1056/NEJMoa1607141
  13. Gerstein HC, Colhoun HM, Dagenais GR, et al. Dulaglutide and cardiovascular outcomes in type 2 diabetes (REWIND): a double-blind, randomised placebo- controlled trial. Lancet 2019;394(10193):121-30. https://doi.org/10.1016/S0140-6736(19)31149-3
  14. Husain M, Birkenfeld AL, Donsmark M, et al. Oral Semaglutide and Cardiovascular Outcomes in Patients with Type 2 Diabetes. N Engl J Med 2019; 381(9):841-51. https://doi.org/10.1056/NEJMoa1901118
  15. Furtado RHM, Bonaca MP, Raz I, et al. Dapagliflozin and Cardiovascular Outcomes in Patients With Type 2 Diabetes Mellitus and Previous Myocardial Infarction. Circulation 2019;139(22):2516-27. https://doi.org/10.1161/CIRCULATIONAHA.119.039996
  16. Mahaffey KW, Neal B, Perkovic V, et al. Canagliflozin for Primary and Secondary Prevention of Cardiovascular Events: Results From the CANVAS Program (Canagliflozin Cardiovascular Assessment Study). Circulation 2018;137(4):323-34. https://doi.org/10.1161/CIRCULATIONAHA.117032038
  17. Verma S, Poulter NR, Bhatt DL, et al. Effects of Liraglutide on Cardiovascular Outcomes in Patients With Type 2 Diabetes Mellitus With or Without History of Myocardial Infarction or Stroke. Circulation 2018;138(25):2884-94. https://doi.org/10.1161/CIRCULATIONAHA.118.034516
  18. Leiter LA, Bain SC, Hramiak I, et al. Cardiovascular risk reduction with once-weekly semaglutide in subjects with type 2 diabetes: a post hoc analysis of gender, age, and baseline CV risk profile in the SUSTAIN 6 trial. Cardiovasc Diabetol 2019;18(1):73-8. https://doi.org/10.1186/s12933-019-0871-8
  19. White WB, Cannon CP, Heller SR, et al. Alogliptin after acute coronary syndrome in patients with type 2 diabetes. N Engl J Med 2013;369(14):1327-35. https://doi.org/10.1056/NEJMoa1305889
  20. Rosenstock J, Perkovic V, Johansen OE, et al. Effect of Linagliptin vs Placebo on Major Cardiovascular Events in Adults With Type 2 Diabetes and High Cardiovascular and Renal Risk: The CARMELINA Randomized Clinical Trial. JAMA 2019;321(1):69-79. https://doi.org/10.1001/jama.2018.18269
  21. Scirica BM, Bhatt DL, Braunwald E, et al. Saxagliptin and cardiovascular outcomes in patients with type 2 diabetes mellitus. N Engl J Med 2013; 369(14):1317-26. https://doi.org/10.1056/NEJMoa1307684
  22. Green JB, Bethel MA, Armstrong PW, et al. Effect of Sitagliptin on Cardiovascular Outcomes in Type 2 Diabetes. N Engl J Med 2015;373(3):232-42. https://doi.org/10.1056/NEJMoa1501352
  23. McMurray JJV, Solomon SD, Inzucchi SE, et al. Dapagliflozin in Patients with Heart Failure and Reduced Ejection Fraction. N Engl J Med 2019; 381(21):1995-2008. https://doi.org/10.1056/NEJMoa1911303
  24. Packer M, Anker SD, Butler J, et al. Cardiovascular and Renal Outcomes with Empagliflozin in Heart Failure. N Engl J Med 2020;383(15):1413-24. https://doi.org/10.1056/NEJMoa2022190
  25. Radholm K, Figtree G, Perkovic V, et al. Canagliflozin and Heart Failure in Type 2 Diabetes Mellitus: Results From the CANVAS Program. Circulation 2018; 138(5):458-68. https://doi.org/10.1161/CIRCULATIONAHA.118.04222
  26. Anker SD, Butler J, Filippatos G, et al. Empagliflozin in Heart Failure with a Preserved Ejection Fraction. N Engl J Med 2021;385(16):1451-61. https://doi.org/10.1056/NEJM0a2107038
  27. Perkovic V, Jardine MJ, Neal B, et al. Canagliflozin and Renal Outcomes in Type 2 Diabetes and Nephropathy. N Engl J Med 2019;380(24):2295-306. https://doi.org/10.1056/NEJMoa1811744
  28. Heerspink HJL, Stefansson BV, Correa-Rotter R, et al. Dapagliflozin in Patients with Chronic Kidney Disease. N Engl J Med 2020;383(15):1436-46. https://doi.org/10.1056/NEJMoa2024816
  29. Wanner C, Inzucchi SE, Lachin JM, et al. Empagliflozin and Progression of Kidney Disease in Type 2 Diabetes. N Engl J Med 2016;375(4):323-34. https://doi.org/10.1056/NEJMoa1515920
  30. Neuen BL, Ohkuma T, Neal B, et al. Cardiovascular and Renal Outcomes With Canagliflozin According to Baseline Kidney Function. Circulation 2018; 138(15):1537-50. https://doi.org/10.1161/CIRCULATIONAHA.118.035901
  31. Mann JFE, Orsted DD, Brown-Frandsen K, et al. Liraglutide and Renal Outcomes in Type 2 Diabetes. N Engl J Med 2017;377(9):839-48. https://doi.org/10.1056/NEJMoa1616011
  32. Hippisley-Cox J, Coupland C, Vinogradova Y, et al. Performance of the QRISK cardiovascular risk prediction algorithm in an independent UK sample of patients from general practice: a validation study. Heart 2008;94(1):34-39. https://doi.org/10.1136/hrt.2007.134890
  33. Cahn A, Raz I, Leiter LA, et al. Cardiovascular, Renal and Metabolic Outcomes of Dapagliflozin versus Placebo in a primary cardiovascular Prevention Cohort: Analyses from DECLARE-TIMI 58. Emerging Therapies: Drugs and Regimens 2021;44(5):1159-67. https://doi.org/10.2337/dc20-2492
  34. Palmer SC, Tendal B, Mustafa RA, et al. Sodium-glucose cotransporter protein-2 (SGLT-2) inhibitors and glucagon-like peptide-1 (GLP-1) receptor agonists for type 2 diabetes: systematic review and network meta-analysis of randomised controlled trials. BMJ 2021;372:m4573. https://doi.org/10.1136/bmj.m4573
  35. Patorno E, Pawar A, Franklin JM, et al. Empagliflozin and the Risk of Heart Failure Hospitalization in Routine Clinical Care. Circulation 2019; 139(25):2822-30. https://doi.org/10.1161/CIRCULATIONAHA.118.039177
  36. Kosiborod M, Lam CSP, Kohsaka S, et al. Cardiovascular Events Associated With SGLT-2 Inhibitors Versus Other Glucose-Lowering Drugs: The CVD-REAL 2 Study. J Am Coll Cardiol 2018;71(23):2628-39. https://doi.org/10.1016/j/jacc.2018.03.009
  37. Kosiborod M, Cavender MA, Fu AZ, et al. Lower Risk of Heart Failure and Death in Patients Initiated on Sodium-Glucose Cotransporter-2 Inhibitors Versus Other Glucose-Lowering Drugs: The CVD-REAL Study (Comparative Effectiveness of Cardiovascular Outcomes in New Users of Sodium-Glucose Cotransporter-2 Inhibitors). Circulation 2017;136(3):249-59. https://doi.org/10.1161/CIRCULATIONAHA.117.029190