Metformin improves blood glucose by increasing incretins independent of changes in gluconeogenesis in youth with type 2 diabetes
Aims/hypothesis Metformin is the only approved oral agent for youth with type 2 diabetes but its mechanism of action remains controversial. Recent data in adults suggest a primary role for the enteroinsular pathway, but there are no data in youth, in whom metformin efficacy is only ~50%. Our objecti...
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Published in | Diabetologia Vol. 63; no. 10; pp. 2194 - 2204 |
---|---|
Main Authors | , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
Berlin/Heidelberg
Springer Berlin Heidelberg
01.10.2020
Springer Nature B.V |
Subjects | |
Online Access | Get full text |
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Abstract | Aims/hypothesis
Metformin is the only approved oral agent for youth with type 2 diabetes but its mechanism of action remains controversial. Recent data in adults suggest a primary role for the enteroinsular pathway, but there are no data in youth, in whom metformin efficacy is only ~50%. Our objectives were to compare incretin concentrations and rates of glucose production and gluconeogenesis in youth with type 2 diabetes before and after short-term metformin therapy compared with peers with normal glucose tolerance (NGT).
Methods
This is a case–control observational study in youth with type 2 diabetes who were not on metformin (
n
= 18) compared with youth with NGT (
n
= 10) who were evaluated with a 2 day protocol. A 75 g OGTT was administered to measure intact glucagon-like 1 peptide (iGLP-1), gastric inhibitory polypeptide (GIP) and peptide YY (PYY). Insulinogenic index (IGI) and whole-body insulin sensitivity were calculated using glucose and insulin levels from the OGTT. Basal rates of gluconeogenesis (
2
H
2
O), glucose production ([6,6-
2
H
2
]glucose) and whole-body lipolysis ([
2
H
5
]glycerol) were measured after an overnight fast on study day 2. Youth with type 2 diabetes (
n
= 9) were subsequently evaluated with an identical 2 day protocol after 3 months on the metformin study.
Results
Compared with individuals with NGT, those with type 2 diabetes had higher fasting (7.8 ± 2.5 vs 5.1 ± 0.3 mmol/l, mean ± SD
p
= 0.002) and 2 h glucose concentrations (13.8 ± 4.5 vs 5.9 ± 0.9 mmol/l,
p
= 0.001), higher rates of absolute gluconeogenesis (10.0 ± 1.7 vs 7.2 ± 1.1 μmol [kg fat-free mass (FFM)]
−1
min
−1
,
p
< 0.001) and whole-body lipolysis (5.2 ± 0.9 vs 4.0 ± 1.4 μmol kg
FFM
−1
min
−1
,
p
< 0.01), but lower fasting iGLP-1 concentrations (0.5 ± 0.5 vs 1.3 ± 0.7 pmol/l,
p
< 0.01). Metformin decreased 2 h glucose (pre metformin 11.4 ± 2.8 vs post metformin 9.9 ± 1.9 mmol/l,
p
= 0.04) and was associated with ~20–50% increase in IGI (median [25th–75th percentile] pre 1.39 [0.89–1.47] vs post 1.43 [0.88–2.70],
p
= 0.04), fasting iGLP-1 (pre 0.3 ± 0.2 vs post 1.0 ± 0.7 pmol/l,
p
= 0.02), 2 h iGLP (pre 0.4 ± 0.2 vs post 1.2 ± 0.9 pmol/l,
p
= 0.06), fasting PYY (pre 6.3 ± 2.2 vs post 10.5 ± 4.3 pmol/l,
p
< 0.01) and 2 h PYY (pre 6.6 ± 2.9 vs post 9.0 ± 4.0 pmol/l,
p
< 0.01). There was no change in BMI, insulin sensitivity or GIP concentrations pre vs post metformin. There were no differences pre vs post metformin in rates of glucose production (15.0 ± 3.9 vs 14.9 ± 2.2 μmol kg
FFM
−1
min
−1
,
p
= 0.84), absolute gluconeogenesis (9.9 ± 1.8 vs 9.7 ± 1.7 μmol kg
FFM
−1
min
−1
,
p
= 0.76) or whole-body lipolysis (5.0 ± 0.7 vs 5.3 ± 1.3 μmol kg
FFM
−1
min
−1
,
p
= 0.20). Post metformin iGLP-1 and PYY concentrations in youth with type 2 diabetes were comparable to levels in youth with NGT.
Conclusions/interpretation
Overall, the improved postprandial blood glucose levels and increase in incretins observed in the absence of changes in insulin sensitivity and gluconeogenesis, support an enteroinsular mechanistic pathway in youth with type 2 diabetes treated with short-term metformin.
Graphical abstract |
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AbstractList | Aims/hypothesisMetformin is the only approved oral agent for youth with type 2 diabetes but its mechanism of action remains controversial. Recent data in adults suggest a primary role for the enteroinsular pathway, but there are no data in youth, in whom metformin efficacy is only ~50%. Our objectives were to compare incretin concentrations and rates of glucose production and gluconeogenesis in youth with type 2 diabetes before and after short-term metformin therapy compared with peers with normal glucose tolerance (NGT).MethodsThis is a case–control observational study in youth with type 2 diabetes who were not on metformin (n = 18) compared with youth with NGT (n = 10) who were evaluated with a 2 day protocol. A 75 g OGTT was administered to measure intact glucagon-like 1 peptide (iGLP-1), gastric inhibitory polypeptide (GIP) and peptide YY (PYY). Insulinogenic index (IGI) and whole-body insulin sensitivity were calculated using glucose and insulin levels from the OGTT. Basal rates of gluconeogenesis (2H2O), glucose production ([6,6-2H2]glucose) and whole-body lipolysis ([2H5]glycerol) were measured after an overnight fast on study day 2. Youth with type 2 diabetes (n = 9) were subsequently evaluated with an identical 2 day protocol after 3 months on the metformin study.ResultsCompared with individuals with NGT, those with type 2 diabetes had higher fasting (7.8 ± 2.5 vs 5.1 ± 0.3 mmol/l, mean ± SD p = 0.002) and 2 h glucose concentrations (13.8 ± 4.5 vs 5.9 ± 0.9 mmol/l, p = 0.001), higher rates of absolute gluconeogenesis (10.0 ± 1.7 vs 7.2 ± 1.1 μmol [kg fat-free mass (FFM)]−1 min−1, p < 0.001) and whole-body lipolysis (5.2 ± 0.9 vs 4.0 ± 1.4 μmol kgFFM−1 min−1, p < 0.01), but lower fasting iGLP-1 concentrations (0.5 ± 0.5 vs 1.3 ± 0.7 pmol/l, p < 0.01). Metformin decreased 2 h glucose (pre metformin 11.4 ± 2.8 vs post metformin 9.9 ± 1.9 mmol/l, p = 0.04) and was associated with ~20–50% increase in IGI (median [25th–75th percentile] pre 1.39 [0.89–1.47] vs post 1.43 [0.88–2.70], p = 0.04), fasting iGLP-1 (pre 0.3 ± 0.2 vs post 1.0 ± 0.7 pmol/l, p = 0.02), 2 h iGLP (pre 0.4 ± 0.2 vs post 1.2 ± 0.9 pmol/l, p = 0.06), fasting PYY (pre 6.3 ± 2.2 vs post 10.5 ± 4.3 pmol/l, p < 0.01) and 2 h PYY (pre 6.6 ± 2.9 vs post 9.0 ± 4.0 pmol/l, p < 0.01). There was no change in BMI, insulin sensitivity or GIP concentrations pre vs post metformin. There were no differences pre vs post metformin in rates of glucose production (15.0 ± 3.9 vs 14.9 ± 2.2 μmol kgFFM−1 min−1, p = 0.84), absolute gluconeogenesis (9.9 ± 1.8 vs 9.7 ± 1.7 μmol kgFFM−1 min−1, p = 0.76) or whole-body lipolysis (5.0 ± 0.7 vs 5.3 ± 1.3 μmol kgFFM−1 min−1, p = 0.20). Post metformin iGLP-1 and PYY concentrations in youth with type 2 diabetes were comparable to levels in youth with NGT.Conclusions/interpretationOverall, the improved postprandial blood glucose levels and increase in incretins observed in the absence of changes in insulin sensitivity and gluconeogenesis, support an enteroinsular mechanistic pathway in youth with type 2 diabetes treated with short-term metformin. Aims/hypothesis Metformin is the only approved oral agent for youth with type 2 diabetes but its mechanism of action remains controversial. Recent data in adults suggest a primary role for the enteroinsular pathway, but there are no data in youth, in whom metformin efficacy is only ~50%. Our objectives were to compare incretin concentrations and rates of glucose production and gluconeogenesis in youth with type 2 diabetes before and after short-term metformin therapy compared with peers with normal glucose tolerance (NGT). Methods This is a case–control observational study in youth with type 2 diabetes who were not on metformin ( n = 18) compared with youth with NGT ( n = 10) who were evaluated with a 2 day protocol. A 75 g OGTT was administered to measure intact glucagon-like 1 peptide (iGLP-1), gastric inhibitory polypeptide (GIP) and peptide YY (PYY). Insulinogenic index (IGI) and whole-body insulin sensitivity were calculated using glucose and insulin levels from the OGTT. Basal rates of gluconeogenesis ( 2 H 2 O), glucose production ([6,6- 2 H 2 ]glucose) and whole-body lipolysis ([ 2 H 5 ]glycerol) were measured after an overnight fast on study day 2. Youth with type 2 diabetes ( n = 9) were subsequently evaluated with an identical 2 day protocol after 3 months on the metformin study. Results Compared with individuals with NGT, those with type 2 diabetes had higher fasting (7.8 ± 2.5 vs 5.1 ± 0.3 mmol/l, mean ± SD p = 0.002) and 2 h glucose concentrations (13.8 ± 4.5 vs 5.9 ± 0.9 mmol/l, p = 0.001), higher rates of absolute gluconeogenesis (10.0 ± 1.7 vs 7.2 ± 1.1 μmol [kg fat-free mass (FFM)] −1 min −1 , p < 0.001) and whole-body lipolysis (5.2 ± 0.9 vs 4.0 ± 1.4 μmol kg FFM −1 min −1 , p < 0.01), but lower fasting iGLP-1 concentrations (0.5 ± 0.5 vs 1.3 ± 0.7 pmol/l, p < 0.01). Metformin decreased 2 h glucose (pre metformin 11.4 ± 2.8 vs post metformin 9.9 ± 1.9 mmol/l, p = 0.04) and was associated with ~20–50% increase in IGI (median [25th–75th percentile] pre 1.39 [0.89–1.47] vs post 1.43 [0.88–2.70], p = 0.04), fasting iGLP-1 (pre 0.3 ± 0.2 vs post 1.0 ± 0.7 pmol/l, p = 0.02), 2 h iGLP (pre 0.4 ± 0.2 vs post 1.2 ± 0.9 pmol/l, p = 0.06), fasting PYY (pre 6.3 ± 2.2 vs post 10.5 ± 4.3 pmol/l, p < 0.01) and 2 h PYY (pre 6.6 ± 2.9 vs post 9.0 ± 4.0 pmol/l, p < 0.01). There was no change in BMI, insulin sensitivity or GIP concentrations pre vs post metformin. There were no differences pre vs post metformin in rates of glucose production (15.0 ± 3.9 vs 14.9 ± 2.2 μmol kg FFM −1 min −1 , p = 0.84), absolute gluconeogenesis (9.9 ± 1.8 vs 9.7 ± 1.7 μmol kg FFM −1 min −1 , p = 0.76) or whole-body lipolysis (5.0 ± 0.7 vs 5.3 ± 1.3 μmol kg FFM −1 min −1 , p = 0.20). Post metformin iGLP-1 and PYY concentrations in youth with type 2 diabetes were comparable to levels in youth with NGT. Conclusions/interpretation Overall, the improved postprandial blood glucose levels and increase in incretins observed in the absence of changes in insulin sensitivity and gluconeogenesis, support an enteroinsular mechanistic pathway in youth with type 2 diabetes treated with short-term metformin. Graphical abstract AIMS/HYPOTHESISMetformin is the only approved oral agent for youth with type 2 diabetes but its mechanism of action remains controversial. Recent data in adults suggest a primary role for the enteroinsular pathway, but there are no data in youth, in whom metformin efficacy is only ~50%. Our objectives were to compare incretin concentrations and rates of glucose production and gluconeogenesis in youth with type 2 diabetes before and after short-term metformin therapy compared with peers with normal glucose tolerance (NGT). METHODSThis is a case-control observational study in youth with type 2 diabetes who were not on metformin (n = 18) compared with youth with NGT (n = 10) who were evaluated with a 2 day protocol. A 75 g OGTT was administered to measure intact glucagon-like 1 peptide (iGLP-1), gastric inhibitory polypeptide (GIP) and peptide YY (PYY). Insulinogenic index (IGI) and whole-body insulin sensitivity were calculated using glucose and insulin levels from the OGTT. Basal rates of gluconeogenesis (2H2O), glucose production ([6,6-2H2]glucose) and whole-body lipolysis ([2H5]glycerol) were measured after an overnight fast on study day 2. Youth with type 2 diabetes (n = 9) were subsequently evaluated with an identical 2 day protocol after 3 months on the metformin study. RESULTSCompared with individuals with NGT, those with type 2 diabetes had higher fasting (7.8 ± 2.5 vs 5.1 ± 0.3 mmol/l, mean ± SD p = 0.002) and 2 h glucose concentrations (13.8 ± 4.5 vs 5.9 ± 0.9 mmol/l, p = 0.001), higher rates of absolute gluconeogenesis (10.0 ± 1.7 vs 7.2 ± 1.1 μmol [kg fat-free mass (FFM)]-1 min-1, p < 0.001) and whole-body lipolysis (5.2 ± 0.9 vs 4.0 ± 1.4 μmol kgFFM-1 min-1, p < 0.01), but lower fasting iGLP-1 concentrations (0.5 ± 0.5 vs 1.3 ± 0.7 pmol/l, p < 0.01). Metformin decreased 2 h glucose (pre metformin 11.4 ± 2.8 vs post metformin 9.9 ± 1.9 mmol/l, p = 0.04) and was associated with ~20-50% increase in IGI (median [25th-75th percentile] pre 1.39 [0.89-1.47] vs post 1.43 [0.88-2.70], p = 0.04), fasting iGLP-1 (pre 0.3 ± 0.2 vs post 1.0 ± 0.7 pmol/l, p = 0.02), 2 h iGLP (pre 0.4 ± 0.2 vs post 1.2 ± 0.9 pmol/l, p = 0.06), fasting PYY (pre 6.3 ± 2.2 vs post 10.5 ± 4.3 pmol/l, p < 0.01) and 2 h PYY (pre 6.6 ± 2.9 vs post 9.0 ± 4.0 pmol/l, p < 0.01). There was no change in BMI, insulin sensitivity or GIP concentrations pre vs post metformin. There were no differences pre vs post metformin in rates of glucose production (15.0 ± 3.9 vs 14.9 ± 2.2 μmol kgFFM-1 min-1, p = 0.84), absolute gluconeogenesis (9.9 ± 1.8 vs 9.7 ± 1.7 μmol kgFFM-1 min-1, p = 0.76) or whole-body lipolysis (5.0 ± 0.7 vs 5.3 ± 1.3 μmol kgFFM-1 min-1, p = 0.20). Post metformin iGLP-1 and PYY concentrations in youth with type 2 diabetes were comparable to levels in youth with NGT. CONCLUSIONS/INTERPRETATIONOverall, the improved postprandial blood glucose levels and increase in incretins observed in the absence of changes in insulin sensitivity and gluconeogenesis, support an enteroinsular mechanistic pathway in youth with type 2 diabetes treated with short-term metformin. |
Author | Dai, Yuhai Walter, Peter J. Cai, Hongyi Cogen, Fran Haymond, Morey W. Chung, Stephanie T. Yang, Shanna Mabundo, Lilian S. Walter, Mary Magge, Sheela N. Meyers, Abby G. Cravalho, Celeste K. L. Chacko, Shaji Courville, Amber Sharma, Susan |
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CitedBy_id | crossref_primary_10_1016_j_metabol_2021_154956 crossref_primary_10_3389_fendo_2021_665292 crossref_primary_10_1002_edm2_206 crossref_primary_10_1016_j_mmm_2021_09_005 crossref_primary_10_1210_clinem_dgad669 crossref_primary_10_1152_ajpendo_00281_2021 crossref_primary_10_1507_endocrj_EJ22_0260 crossref_primary_10_1210_clinem_dgad508 crossref_primary_10_1111_pedi_13148 |
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Copyright | This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply 2020 This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply 2020. |
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Keywords | Type 2 diabetes Paediatric Gut hormones Gluconeogenesis |
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PublicationSubtitle | Clinical, Translational and Experimental Diabetes and Metabolism |
PublicationTitle | Diabetologia |
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Metformin is the only approved oral agent for youth with type 2 diabetes but its mechanism of action remains controversial. Recent data in... Aims/hypothesisMetformin is the only approved oral agent for youth with type 2 diabetes but its mechanism of action remains controversial. Recent data in... AIMS/HYPOTHESISMetformin is the only approved oral agent for youth with type 2 diabetes but its mechanism of action remains controversial. Recent data in... |
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SubjectTerms | Antidiabetics Blood glucose Diabetes Diabetes mellitus (non-insulin dependent) Fasting Fat-free body mass Glucagon Gluconeogenesis Glucose Glucose tolerance Glycerol Human Physiology Insulin Internal Medicine Lipolysis Medicine Medicine & Public Health Metabolic Diseases Metformin Pediatrics Peptides |
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Title | Metformin improves blood glucose by increasing incretins independent of changes in gluconeogenesis in youth with type 2 diabetes |
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