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Metabolic response to sodium-glucose cotransporter 2 inhibition in type 2 diabetic patients
Open accessAbstract
BACKGROUND: Sodium-glucose cotransporter 2 (SGLT2) inhibitors lower glycemia by enhancing urinary glucose excretion. The physiologic response to pharmacologically induced acute or chronic glycosuria has not been investigated in human diabetes. METHODS: We evaluated 66 patients with type 2 diabetes (62 ± 7 years, BMI = 31.6 ± 4.6 kg/m(2), HbA1c = 55 ± 8 mmol/mol, mean ± SD) at baseline, after a single dose, and following 4-week treatment with empagliflozin (25 mg). At each time point, patients received a mixed meal coupled with dual-tracer glucose administration and indirect calorimetry. RESULTS: Both single-dose and chronic empagliflozin treatment caused glycosuria during fasting (median, 7.8 [interquartile range {IQR}, 4.4] g/3 hours and 9.2 [IQR, 5.2] g/3 hours) and after meal ingestion (median, 29.0 [IQR, 12.5] g/5 hours and 28.2 [IQR, 15.4] g/5 hours). After 3 hours of fasting, endogenous glucose production (EGP) was increased 25%, while glycemia was 0.9 ± 0.7 mmol/l lower (P < 0.0001 vs. baseline). After meal ingestion, glucose and insulin AUC decreased, whereas the glucagon response increased (all P < 0.001). While oral glucose appearance was unchanged, EGP was increased (median, 40 [IQR, 14] g and 37 [IQR, 11] g vs. 34 [IQR, 11] g, both P < 0.01). Tissue glucose disposal was reduced (median, 75 [IQR, 16] g and 70 [IQR, 21] g vs. 93 [IQR, 18] g, P < 0.0001), due to a decrease in both glucose oxidation and nonoxidative glucose disposal, with a concomitant rise in lipid oxidation after chronic administration (all P < 0.01). β Cell glucose sensitivity increased (median, 55 [IQR, 35] pmol • min(-1) • m(-2) • mM(-1) and 55 [IQR, 39] pmol • min(-1) • m(-2) • mM(-1) vs. 44 [IQR, 32] pmol • min(-1) • m(-2) • mM(-1), P < 0.0001), and insulin sensitivity was improved. Resting energy expenditure rates and those after meal ingestion were unchanged. CONCLUSIONS: In patients with type 2 diabetes, empagliflozin-induced glycosuria improved β cell function and insulin sensitivity, despite the fall in insulin secretion and tissue glucose disposal and the rise in EGP after one dose, thereby lowering fasting and postprandial glycemia. Chronic dosing shifted substrate utilization from carbohydrate to lipid. Trial registration. ClinicalTrials.Gov NCT01248364 (EudraCT no. 2010-018708-99). Funding. This study was funded by Boehringer Ingelheim.
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“Previous RCTs reported that selective SGLT2 inhibitors, a new class of anti-diabetes drugs, have been shown to reduce body weight (1–3 kg reduction) in diabetic patients with and without obesity [99–102].”
From Long-Term Efficacy and Safety of Anti-Obesity Treatment: Where Do We Stand? (2021) · cites this paper as [99]
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“…порівняно з іншими гіпоглікемічними препаратами полягає в тому, що вони індукують втрату ваги у пацієнтів із ЦД2 та одночасно сприятливо впливають на ліпідний обмін [47-48]. іSGLT2, ймовірно, викликають втрату ваги, зменшуючи загальне споживання енергії організмом і сприяючи осмотичному діурезу.”
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“…to a peak concentration of 370 nM within 2 h. 23 Our previous electrophysiological measurements indicate a rapid onset of dapagliflozin’s effects, 18 and it was not deemed necessary to test a range of doses because it does not exhibit the complex dose-dependent effects on glucagon secretion…”
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“The pooled HbA1c reduction of approximately − 0.49% is consistent with an additive glycemic effect when SGLT2 inhibition is combined with pioglitazone-based insulin sensitization (31, 34 – 37).”
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“reduced vascular inflammation,[135] possible indirect antiarrhythmic effects of empagliflozin,[134] and possible beneficial cardiac effects of increased glucagon levels.[41,134,136,137]”
BackgroundSGLT2 Inhibitors and Ketoacidosis: Pathophysiology and Management
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Renal Effects of Empagliflozin in Patients with Type 2 Diabetes Mellitus
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New approaches to reduce recurrent PCI: to angioplasty and beyond!
Sabouret, P. F., Manzo‐Silberman, S., Alasnag, M. A., Fysekidis, M., Gulati, M., Galati, G., Spadafora, L., Banach, M., Biondi‐Zoccai, G., & Bhatt, D. L. (2023) · European Heart Journal Open · doi:10.1093/ehjopen/oead049 · Cited by 1
“Chronic administration is associated with weight loss, and better metabolic profile with increased lipolysis, increased glucagon secretion, improved lipid oxidation, and lower circulating insulin levels.(47,48) For SGLT2i, protection from MI is also well documented; in all four major RCTs there were high percentages o…”
Watanabe, K., Yamaguchi, S., Kosakai, Y., Ioji, T., & Ishihara, H. (2023) · Clinical Drug Investigation · doi:10.1007/s40261-023-01317-z · Cited by 1
“Increased plasma glucagon levels were first reported in patients receiving treatment with SGLT2is [27, 28] but the effect has not been attributed to a direct action of SGLT2is.”
BackgroundGlucose handling by the brain and its implication in metabolic syndrome
Mukhopadhyay, R., Chowdhury, A. S., & Palui, R. (2024) · Elsevier eBooks · doi:10.1016/b978-0-323-85732-1.00083-9 · Cited by 1
Insulin therapy: a century of continuing progress
Bolli, G. B., Fanelli, C. G., Lucidi, P., & Porcellati, F. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-91707-0.00006-1 · Cited by 1
Ketonuria in an adult with Prader-Willi syndrome and diabetes mellitus: A case report
Xu, X., Wang, D., Pan, H., Li, J., Li, B., & He, Z. (2024) · Medicine · doi:10.1097/md.0000000000037096 · Cited by 1
“[10,11] Besides, the SGLT-2 inhibitor itself stimulates glucagon secretion, [12,13] further enhancing lipolysis and ketogenesis.”
BackgroundCarrero, R. S. D. V., Blanco, A., Daimiel, L., Blanco, M. J., Segovia, R. C., de la Garza, R. G., & Martínez‐Urbistondo, D. (2024) · Biomedicines · doi:10.3390/biomedicines12030692 · Cited by 1
Deshmukh, N., Kalshetti, M. S., Patil, M., Autade, P., & Sangle, G. V. (2024) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/1440-1681.13854 · Cited by 1
Habas, E. M., Habas, A. M., Elzouki, I., Alfitori, G. B., Arrayes, E., Rayani, A., Farfar, K., Habas, E., & Elzouki, A.-N. Y. (2024) · Journal of Diabetes and Endocrine Practice · doi:10.1055/s-0044-1782673 · Cited by 1
“11,24,47 This effect of SGLT2 inhibitors is due to the heightened insulin sensitivity and improved beta-cell activity, 48,49 leading to better safe HbA1c control.”
Dehydration-induced AVP stimulates glucagon release and ketogenesis
Hill, T. G., Briant, L. J. B., Kim, A., Wu, Y., Rorsman, P., Asterholm, I. W., & Benrick, A. (2025) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00505.2024 · Cited by 4
Bhosle, D. S., Chandekar, B., & Shelke, S. (2025) · Journal of the Association of Physicians of India · doi:10.59556/japi.73.0925 · Cited by 1
“25 According to a study conducted by Matthaei et al., subjects who received 52 weeks of dapagliflozin treatment were found to have greater reductions in HbA1c and FPG levels, as compared to those who received the placebo.”
Hagiwara, A., Yamaguchi, S., Miyashita, K., Kinouchi, K., Hayashi, K., & Itoh, H. (2025) · Hypertension Research · doi:10.1038/s41440-025-02287-9 · Cited by 1
“Initial weight loss is generally attributed to osmotic diuresis and calorie loss from glucose excretion; however, long-term reductions in body fat mass indicate the involvement of additional mechanisms [39 – 43].”
Les acidocétoses diabétiques atypiques
Schlienger, J.-L., & Halimi, S. (2016) · Médecine des Maladies Métaboliques · doi:10.1016/s1957-2557(16)30118-3 · Cited by 1
Amelioration of arterial pressure lability: an unmissable target for diabetes management
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Guías para el tratamiento de la diabetes mellitus tipo 2. Sociedad Argentina de Diabetes
Faingold, M. C., Commendatore, V., González, C. D., Bragagnolo, J. C., Sinay, I. R., Lapertosa, S., Vázquez, F., Musso, C., Alvariñas, J., Dios, A. D., et al. (2016) · Revista de la Sociedad Argentina de Diabetes · doi:10.47196/diab.v50i2.2 · Cited by 1
Nomoto, H., & Miyoshi, H. (2017) · British Journal of Research · doi:10.21767/2394-3718.100021 · Cited by 1
“Moreover, hepatic gluconeogenesis, lipolysis, and increased glucagon prevent hypoglycemia and can inhibit glucose variability [26,27].”
BackgroundMurata, M., Adachi, H., Nakade, T., & Oshima, S. (2018) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2018.09.001 · Cited by 1
Reprint of: Blood Sugar Regulation for Cardiovascular Health Promotion and Disease Prevention
Schwarz, P. E. H., Timpel, P., Harst, L., Greaves, C. J., Ali, M. K., Lambert, J. D., Weber, M. B., Almedawar, M. M., & Morawietz, H. (2018) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2018.10.026 · Cited by 1
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Factors that predict glycaemic response to sodium‐glucose linked transporter (SGLT) inhibitors
Harding, A. L., Bediaga, N. G., Galligan, A., Colman, P. G., Fourlanos, S., & Wentworth, J. M. (2020) · Internal Medicine Journal · doi:10.1111/imj.14805 · Cited by 1
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Isotopic Tracers for the Measurement of Metabolic Flux Rates
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Metabolic effects of empagliflozine
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A translational viewpoint explaining its potential salutary effects
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Glucagon in Islet and Metabolic Regulation
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Radellini, S., Vigneri, E., Guarnotta, V., Pantò, F., & Giordano, C. S. D. S. (2021) · Diabetes Therapy · doi:10.1007/s13300-021-01119-6 · Cited by 1
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Prié, D. (2015) · Médecine des Maladies Métaboliques · doi:10.1016/s1957-2557(15)30051-1
Les inhibiteurs de SGLT2 : pour quels patients ? Quelle place dans la stratégie thérapeutique ?
Guerci, B. (2015) · Médecine des Maladies Métaboliques · doi:10.1016/s1957-2557(15)30057-2
Orale Antidiabetika ermöglichen eine individualisierte Therapie
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“is not detrimental to the operation of SGLT2 is SLCA2 secondary mutation of the gene, leading to daily urinary excretion up to 100 grams of glucose [3] [4] [9]-[16].”
BackgroundStinkens, K., & Mathieu, C. (2016) · touchREVIEWS in Endocrinology · doi:10.17925/ee.2016.12.01.33
“EUROPEAN ENDOCRINOLOGY to inhibit lipolysis and prevent ketogenesis.(11) Recently, a direct effect of SGLT2i on the alpha-cells of the islets of Langerhans has also been described.”
Background
Metadata
- Authors
- Ferrannini, E., Muscelli, E., Frascerra, S., Baldi, S., Mari, A., Heise, T., Broedl, U. C., & Woerle, H.-J.
- Affiliations
- University of Pisa (IT)
- National Research Council (IT)
- Profil Institute for Metabolic Research (DE)
- Boehringer Ingelheim (Germany) (DE)
- Corresponding author
- Ferrannini, Ele
- Venue
- Journal of Clinical Investigation
- Published
- 2014-01-27
- Volume
- 124
- Issue
- 2
- Pages
- 499-508
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC3904627
- OpenAlex
- W2157405334
- Cited by
- 1,134
- References
- 45
- Citations by year
- 2026: 55 · 2025: 68 · 2024: 80 · 2023: 81 · 2022: 92 · 2021: 117 · 2020: 106 · 2019: 103 · 2018: 97 · 2017: 90 · 2016: 121 · 2015: 83 · 2014: 39
- FWCI
- 89.27
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- CINECA IRIS Institutial research information system (University of Pisa) (submittedVersion)
- Funders
- American Diabetes Association
- Bristol-Myers Squibb
- Eli Lilly and Company
- AstraZeneca
- Sanofi
- Novo Nordisk
- Astellas Pharma
- Daiichi Sankyo Europe
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Treatment and Management
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Management and Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Keywords
- SGLT2 inhibitors, empagliflozin, type 2 diabetes, glycosuria, endogenous glucose production, glucose oxidation, nonoxidative glucose disposal, lipid oxidation, beta-cell glucose sensitivity, glucagon response, insulin response, glucose metabolism, indirect calorimetry, mixed meal tolerance, urinary glucose excretion, glucose homeostasis
- MeSH terms
- Sodium-Glucose Transporter 2 Inhibitors, Aged, Benzhydryl Compounds, Blood Glucose, Calorimetry, Diabetes Mellitus, Type 2, Female, Glucose, Glucosides, Glycosuria, Glycated Hemoglobin, Humans, Insulin, Male, Metformin, Middle Aged, Oxygen, Body Mass Index, Postprandial Period, Area Under Curve, Insulin-Secreting Cells, Sodium-Glucose Transporter 2
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