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A novel fast-slow model of diabetes progression: Insights into mechanisms of response to the interventions in the Diabetes Prevention Program


Autoři: Andrea De Gaetano aff001;  Thomas Andrew Hardy aff002
Působiště autorů: CNR-IASI BioMatLab (Italian National Research Council - Institute of Analysis, Systems and Computer Science - Biomathematics Laboratory), Rome, Italy aff001;  Lilly Research Laboratories, Eli Lilly and Company, Lilly Corporate Center, Indianapolis, Indiana, United States of America aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222833

Souhrn

Several models for the long-term development of T2DM already exist, focusing on the dynamics of the interaction between glycemia, insulinemia and β-cell mass. Current models consider representative (fasting or daily average) glycemia and insulinemia as characterizing the compensation state of the subject at some instant in slow time. This implies that only these representative levels can be followed through time and that the role of fast glycemic oscillations is neglected. An improved model (DPM15) for the long-term progression of T2DM is proposed, introducing separate peripheral and hepatic (liver and kidney) insulin actions. The DPM15 model no longer uses near-equilibrium approximation to separate fast and slow time scales, but rather describes, at each step in slow time, a complete day in the life of the virtual subject in fast time. The model can thus represent both fasting and postprandial glycemic levels and describe the effect of interventions acting on insulin-enhanced tissue glucose disposal or on insulin-inhibited hepatic glucose output, as well as on insulin secretion and β-cell replicating ability. The model can simulate long-term variations of commonly used clinical indices (HOMA-B, HOMA-IR, insulinogenic index) as well as of Oral Glucose Tolerance or Euglycemic Hyperinsulinemic Clamp test results. The model has been calibrated against observational data from the Diabetes Prevention Program study: it shows good adaptation to observations as a function of very plausible values of the parameters describing the effect of such interventions as Placebo, Intensive LifeStyle and Metformin administration.

Klíčová slova:

Glomerular filtration rate – Glucose – Insulin – Insulin secretion – Toxicity – Glucagon – Nephrons


Zdroje

1. Makroglou A, Li J, Kuang YY (2006) Mathematical models and software tools for the glucose-insulin regulatory system and diabetes: An overview. Applied Numerical Mathematics 56: 559–573. doi: 10.1016/j.apnum.2005.04.023

2. Ajmera I, Swat M, Laibe C, Le Novère N, Chelliah V (2013) The impact of mathematical modeling on the understanding of diabetes and related complications. CPT Pharmacometrics and Systems Pharmacology 2: e54. doi: 10.1038/psp.2013.30 23842097

3. Palumbo P, Ditlevsen S, Bertuzzi A, De Gaetano A (2013) Mathematical modeling of the glucose–insulin system: A review. Math Biosci 244: 69–81. doi: 10.1016/j.mbs.2013.05.006 23733079

4. Palumbo P, Pizzichelli G, Panunzi S, Pepe P, De Gaetano A (2014) Model-based control of plasma glycemia: Tests on populations of virtual patients. Math Biosci 257: 2–10. doi: 10.1016/j.mbs.2014.09.003 25223234

5. De Gaetano A, Gaz C, Palumbo P, Panunzi S (2015) A unifying organ model of pancreatic insulin secretion. PLoS One 10: e0142344. doi: 10.1371/journal.pone.0142344 26555895

6. Borri A, Panunzi S, De Gaetano A (2016) A glycemia-structured population model. J Math Biol 73(1): 39–62. doi: 10.1007/s00285-015-0935-7 26440781

7. Topp BG, Promislow K, deVries G, Miura RM, Finegood DT (2000) A model of beta-cell mass, insulin, and glucose kinetics: pathways to diabetes. J Theor Biol 206: 605–619. doi: 10.1006/jtbi.2000.2150 11013117

8. Bagust A, Evans M, Beale S, Home PD, Perry AS, Stewart M (2006) A model of long-term metabolic progression of type 2 diabetes mellitus for evaluating treatment strategies. PharmacoEconomics 24S1: 5–19. doi: 10.2165/00019053-200624001-00002

9. de Winter W, DeJongh J, Post T, Ploeger B, Urquhart R, Moules I, et al. (2006) A mechanism-based disease progression model for comparison of long-term effects of pioglitazone, metformin and gliclazide on disease processes underlying type 2 diabetes mellitus. J Pharmacokinet Pharmacodyn 33: 313–343. doi: 10.1007/s10928-006-9008-2 16552630

10. De Gaetano A, Hardy T, Beck B, Abu-Raddad E, Palumbo P, Bue-Valleskey J, et al. (2008) Mathematical models of diabetes progression. Am J Physiol 295: E1462–E1479.

11. Ribbing J, Hamrén B, Svensson MK, Karlsson MO (2010) A model for glucose, insulin, and beta-cell dynamics in subjects with insulin resistance and patients with type 2 diabetes. J Clin Pharmacol 50: 861–872. doi: 10.1177/0091270009349711 20484615

12. Boutayeb W, Lamlili MEN, Boutayeb A, Derouich M (2014) Mathematical modelling and simulation of β-cell mass, insulin and glucose dynamics: Effect of genetic predisposition to diabetes. J Biomedical Science and Engineering 7: 330–342. doi: 10.4236/jbise.2014.76035

13. Palmér R, Nyman E, Penney M, Marley A, Walker G, Cedersund G, et al. (2014) Effects of il-1β–blocking therapies in type 2 diabetes mellitus: A quantitative systems pharmacology modeling approach to explore underlying mechanisms. CPT Pharmacometrics Syst Pharmacol 3: e118. doi: 10.1038/psp.2014.16 24918743

14. Ha J, Satin LS, Sherman AS (2016) A mathematical model of the pathogenesis, prevention, and reversal of type 2 diabetes. Endocrinology 157(2): 624–635. doi: 10.1210/en.2015-1564 26709417

15. Larsen CM, Faulenbach M, Vaag A, Vølund A, Ehses JA, Seifert B, et al. (2007) Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N Engl J Med 356: 1517–1526. doi: 10.1056/NEJMoa065213 17429083

16. Larsen CM, Faulenbach M, Vaag A, Ehses JA, Donath MY, Mandrup-Poulsen T (2009) Sustained effects of interleukin-1 receptor antagonist treatment in type 2 diabetes. Diabetes Care 32: 1663–1668. doi: 10.2337/dc09-0533 19542207

17. Sloan-Lancaster J, Abu-Raddad E, Polzer J, Miller JW, Scherer JC, De Gaetano A, et al. (2013) Double-blind, randomized study evaluating the glycemic and anti-inflammatory effects of subcutaneous ly2189102, a neutralizing il-1beta antibody, in patients with type 2 diabetes. Diabetes Care 36(8): 2239–46. doi: 10.2337/dc12-1835 23514733

18. Hardy TA, Abu-Raddad E, Porksen N, De Gaetano A (2012) Evaluation of a mathematical model of diabetes progression against observations in the diabetes prevention program. Am J Physiol 303: E200–E212.

19. Kitabchi AE, Temprosa M, Knowler WC, Kahn SE, Fowler SE, Haffner SM, et al. (2005) Role of insulin secretion and sensitivity in the evolution of type 2 diabetes in the diabetes prevention program: effects of lifestyle intervention and metformin. Diabetes 54: 2404–2414. doi: 10.2337/diabetes.54.8.2404 16046308

20. Knowler WC, Barrett-Connor E, Fowler SE, Hamman RF, Lachin JM, Walker EA, et al. (2002) Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N Engl J Med 346: 393–403. doi: 10.1056/NEJMoa012512 11832527

21. Knowler WC, Hamman RF, Edelstein SL, Barrett-Connor E, Ehrmann DA, Walker EA, et al. (2005) Prevention of type 2 diabetes with troglitazone in the diabetes prevention program. Diabetes 54: 1150–1156. doi: 10.2337/diabetes.54.4.1150 15793255

22. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC (2003) Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52: 102–110.

23. Sakuraba H, Mizukami H, Yagihashi N, Wada R, Hanyu C, Yagihashi S (2002) Reduced beta-cell mass and expression of oxidative stress-related dna damage in the islet of japanese type ii diabetic patients. Diabetologia 45(1): 85–96. doi: 10.1007/s125-002-8248-z 11845227

24. Yoon KH, Ko SH, Cho JH, Lee JM, Ahn YB, Song KH, et al. (2003) Selective beta-cell loss and alpha-cell expansion in patients with type 2 diabetes mellitus in korea. J Clin Endocrinol Metab 88(5): 2300–2308. doi: 10.1210/jc.2002-020735 12727989

25. Rahier J, Wallon J, Loozen S, Lefevre A, Gepts W, Haot J (1983) The pancreatic polypeptide cells in the human pancreas: the effects of age and diabetes. J Clin Endocrinol Metab 56(3): 441–444. doi: 10.1210/jcem-56-3-441 6337179

26. Street CN, Lakey JR, Shapiro AM, Imes S, Rajotte RV, Ryan EA, et al. (2004) Islet graft assessment in the edmonton protocol: implications for predicting long-term clinical outcome. Diabetes 53(12): 3107–3114. doi: 10.2337/diabetes.53.12.3107 15561940

27. Brissova M, Fowler MJ, Nicholson WE, Chu A, Hirshberg B, Harlan DM, et al. (2005) Assessment of human pancreatic islet architecture and composition by laser scanning confocal microscopy. J Histochem Cytochem 53(9): 1087–1097. doi: 10.1369/jhc.5C6684.2005 15923354

28. Hanley SC, Austin E, Assouline-Thomas B, Kapeluto J, Blaichman J, Moosavi M, et al. (2010) β-cell mass dynamics and islet cell plasticity in human type 2 diabetes. Endocrinology 151(4): 1462–1472. doi: 10.1210/en.2009-1277 20176718

29. Van Assche FA, Aerts L, De Prins F (1978) A morphological study of the endocrine pancreas in human pregnancy. Br J Obstet Gynaecol 85(11): 818–820. doi: 10.1111/j.1471-0528.1978.tb15835.x 363135

30. Hugl SR, White MF, Rhodes CJ (1998) Insulin-like growth factor i (igf-i)-stimulated pancreatic beta-cell growth is glucose-dependent. synergistic activation of insulin receptor substrate-mediated signal transduction pathways by glucose and igf-i in ins-1 cells. J Biol Chem 273: 17771–17779.

31. Pechhold K, Koczwara K, Zhu X, Harrison VS, Walker G, Lee J, et al. (2009) Blood glucose levels regulate pancreatic beta-cell proliferation during experimentally-induced and spontaneous autoimmune diabetes in mice. PLoS One 4. doi: 10.1371/journal.pone.0004827

32. Porat S, Weinberg-Corem N, Tornovsky-Babaey S, Schyr-Ben-Haroush R, Hija A, Stolovich-Rain M, et al. (2011) Control of pancreatic beta cell regeneration by glucose metabolism. Cell Metab 13: 440–449. doi: 10.1016/j.cmet.2011.02.012 21459328

33. Yki-Jarvinen H (1992) Glucose toxicity. Endocr Rev 13: 415–431. doi: 10.1210/edrv-13-3-415 1425483

34. Yki-Jarvinen H (1998) Toxicity of hyperglycaemia in type 2 diabetes. Diabetes Metab Rev 14 Suppl 1: S45–S50.

35. Donath MY, Halban PA (2004) Decreased beta-cell mass in diabetes: significance, mechanisms and therapeutic implications. Diabetologia 47(3): 581–589. doi: 10.1007/s00125-004-1336-4 14767595

36. Ritzel RA, Butler AE, Rizza RA, Veldhuis JD, Butler PC (2006) Relationship between beta-cell mass and fasting blood glucose concentration in humans. Diabetes Care 29(3): 717–718. doi: 10.2337/diacare.29.03.06.dc05-1538 16505537

37. Maedler K, Spinas GA, Lehmann R, Sergeev P, Weber M, Fontana A, et al. (2001) Glucose induces β-cell apoptosis via upregulation of the Fas receptor in human islets. Diabetes 50: 1683–1690. doi: 10.2337/diabetes.50.8.1683 11473025

38. Maedler K, Schumann DM, Schulthess F, Oberholzer J, Bosco D, Berney T, et al. (2006) Aging correlates with decreased β-cell proliferative capacity and enhanced sensitivity to apoptosis. Diabetes 55: 2455–2462.

39. Reers C, Erbel S, Esposito I, Schmied B, Büchler MW, Nawroth PP, et al. (2009) Impaired islet turnover in human donor pancreata with aging. Eur J Endocrinol 160: 185–191. doi: 10.1530/EJE-08-0596 19004984

40. Tyrberg B, Eizirik DL, Hellerstrom C, Pipeleers DG, Andersson A (1996) Human pancreatic beta-cell deoxyribonucleic acid-synthesis in islet grafts decreases with increasing organ donor age but increases in response to glucose stimulation in vitro. Endocrinology 137: 5694–5699.

41. Iozzo P, Beck-Nielsen H, Laakso M, Smith U, Yki-Jarvinen H, Ferrannini E (1999) Independent influence of age on basal insulin secretion in nondiabetic humans. J Clin Endocrinol Metab 84: 863–868. doi: 10.1210/jcem.84.3.5542 10084562

42. Wilcox G (2005) Insulin and insulin resistance. Clin Biochem Rev 26(2): 19–39. 16278749

43. Cherrington AD (1999) Banting lecture 1997. control of glucose uptake and release by the liver in vivo. Diabetes 48(5): 1198–1214. doi: 10.2337/diabetes.48.5.1198 10331429

44. Iozzo P, Geisler F, Oikonen V, Mäki M, Takala T, Solin O, et al. (2003) Insulin stimulates liver glucose uptake in humans: an 18f-fdg pet study. J Nucl Med 44(5): 682–689. 12732668

45. Basu R, Basu A, Johnson CM, Schwenk WF, Rizza RA (2004) Insulin dose-response curves for stimulation of splanchnic glucose uptake and suppression of endogenous glucose production differ in nondiabetic humans and are abnormal in people with type 2 diabetes. Diabetes 53: 2042–2050. doi: 10.2337/diabetes.53.8.2042 15277384

46. Nurjhan N, Campbell PJ, Kennedy FP, Miles JM, Gerich JE (1986) Insulin dose-response characteristics for suppression of glycerol release and conversion to glucose in humans. Diabetes 35: 1326–1331. doi: 10.2337/diab.35.12.1326 3533681

47. Groop LC, Bonadonna RC, DelPrato S, Ratheiser K, Zyck K, Ferrannini E, et al. (1989) Glucose and free fatty acid metabolism in non-insulin-dependent diabetes mellitus: Evidence for multiple sites of insulin resistance. J Clin Invest 84: 205–213. doi: 10.1172/JCI114142 2661589

48. Panunzi S, Palumbo P, De Gaetano A (2007) A discrete single delay model for the intra-venous glucose tolerance test. Theor Biol Med Model 4: 35. doi: 10.1186/1742-4682-4-35 17850652

49. Palumbo P, Panunzi S, De Gaetano A (2007) Qualitative behavior of a family of delay differential models of the glucose insulin system. Discrete and Continuous Dynamical Systems—Series B 7: 399–424.

50. Panunzi S, Mingrone G, De Gaetano A (2010) Advantages of the single delay model for the assessment of insulin sensitivity from the intravenous glucose tolerance test. Theor Biol Med Model 7: 9. doi: 10.1186/1742-4682-7-9 20298586

51. De Gaetano A, Panunzi S, Matone A, Samson A, Vrbikova J, Bendlova B, et al. (2013) Routine OGTT: A robust model including incretin effect for precise identification of insulin sensitivity and secretion in a single individual. PLoS One 8: e70875. doi: 10.1371/journal.pone.0070875 24009656

52. Rizza RA, Mandarino LJ, Gerich JE (1981) Dose-response characteristics for effects of insulin on production and utilization of glucose in man. Am J Physiol 240: E630–E639. doi: 10.1152/ajpendo.1981.240.6.E630 7018254

53. Alford FP, Bloom SR, Nabarro JD (1976) Glucagon metabolism in man, studies on the metabolic clearance rate and the plasma acute disappearance time of glucagon in normal and diabetic subjects. J Clin Endocrinol Metab 42: 830–838. doi: 10.1210/jcem-42-5-830 773949

54. Fisher M, Sherwin RS, Hendler R, Felig P (1976) Kinetics of glucagon in man: effects of starvation. Proc Natl Acad Sci USA 73: 1735–1739. doi: 10.1073/pnas.73.5.1735 1064045

55. Jaspan JB, Polonsky KS, Lewis M, Pensler J, Pugh W, Moossa AR, et al. (1981) Hepatic metabolism of glucagon in the dog: contribution of the liver to overall metabolic disposal of glucagon. Am J Physiol 240: E233–E244. doi: 10.1152/ajpendo.1981.240.3.E233 7011049

56. Konig M, Bulik S, Holzhutter HG (2012) Quantifying the contribution of the liver to glucose homeostasis: a detailed kinetic model of human hepatic glucose metabolism. PLoS Comput Biol 8. doi: 10.1371/journal.pcbi.1002577

57. Gerich J, Davis J, Lorenzi M, Rizza R, Bohannon N, Karam J, et al. (1979) Hormonal mechanisms of recovery from insulin-induced hypoglycemia in man. Am J Physiol 236: E380–E385. doi: 10.1152/ajpendo.1979.236.4.E380 434200

58. Cavallo-Perin P, Bruno A, Scaglione L, Gruden G, Cassader M, Pagano G (1993) Feedback inhibition of insulin and glucagon secretion by insulin is altered in abdominal obesity with normal or impaired glucose tolerance. Acta Diabetol 30: 154–158. doi: 10.1007/BF00572860 8111076

59. Elahi D, Nagulesparan M, Hershcopf RJ, Muller DC, Tobin JD, Blix PM, et al. (1982) Feedback inhibition of insulin secretion by insulin: relation to the hyperinsulinemia of obesity. N Engl J Med 306: 1196–1202. doi: 10.1056/NEJM198205203062002 7040963

60. Cryer PE, Davis SN, Shamoon H (2003) Hypoglycemia in diabetes. Diabetes Care 26: 1902–1912. doi: 10.2337/diacare.26.6.1902 12766131

61. GGerich JE, Langlois M, Noacco C, Karam JH, Forsham PH (1973) Lack of glucagon response to hypoglycemia in diabetes: evidence for an intrinsic pancreatic alpha cell defect. Science 182: 171–173. doi: 10.1126/science.182.4108.171

62. De Gaetano A, Panunzi S, Eliopoulos D, Hardy T, Mingrone G (2014) Mathematical modeling of renal tubular glucose absorption after glucose load. PLoS One 9: e86963. doi: 10.1371/journal.pone.0086963 24489817

63. DeFronzo RA, Barzilai N, Simonson DC (1991) Mechanism of metformin actionin obese and lean noninsulin-dependent diabetic subjects. J Clin Endocrinol Metab 73: 1294–1301. doi: 10.1210/jcem-73-6-1294 1955512

64. Stumvoll M, Nurjhan N, Perriello G, Dailey G, Gerich J (1995) Metabolic effects of metformin in non-insulin-dependent diabetes mellitus. N Engl J Med 333: 550–554. doi: 10.1056/NEJM199508313330903 7623903

65. Inzucchi SE, Maggs DG, Spollett GR, Page SL, Rife FS, Walton V, et al. (1998) Efficacy and metabolic effects of metformin and troglitazone in type ii diabetes mellitus. N Engl J Med 338: 867–872. doi: 10.1056/NEJM199803263381303 9516221

66. Kahn SE, Haffner SM, Heise MA, Herman WH, Holman RR, Jones NP, et al. (2006) Glycemic durability of rosiglitazone, metformin, or glyburide monotherapy. N Engl J Med 355:23: 2427–2443. doi: 10.1056/NEJMoa066224 17145742

67. Nichols GA, Alexander CM, Girman CJ, Kamal-Bahl SJ, Brown JB (2006) Treatment escalation and rise in hba1c following successful initial metformin therapy. Diabetes Care 29: 504–509. doi: 10.2337/diacare.29.03.06.dc05-1937 16505496

68. Brown JB, Conner C, Nichols GA (2010) Secondary failure of metformin monotherapy in clinical practice. Diabetes Care 33: 501–506. doi: 10.2337/dc09-1749 20040656

69. Tikhonov AN (1948) On the dependence of the solutions of differential equations on a small parameter. Matimaticheskii Sbornik (NS) 22 (64).

70. Artstein Z (2010) Analysis and control of coupled slow and fast systems: a review. Proceedings of the 9th Brazilian 1254–1263.

71. Zagaris A, Kaper HG, Kaper TJ (2005) Two perspectives on reduction of ordinary differential equations. Math Nachr 278: 1629–1642. doi: 10.1002/mana.200410328

72. Wang YF, Khan M, van den Berg HA (2012) Interaction of fast and slow dynamics in endocrine control systems with an application to beta-cell dynamics. Math Biosci 235: 8–18. doi: 10.1016/j.mbs.2011.10.003 22063267

73. Haffner SM, D’Agostino R Jr, Festa A, Bergman RN, Mykkänen L, Karter A, et al. (2003) Low insulin sensitivity (s(i) = 0) in diabetic and nondiabetic subjects in the insulin resistance atherosclerosis study: is it associated with components of the metabolic syndrome and nontraditional risk factors? Diabetes Care 26(10): 2796–2803. doi: 10.2337/diacare.26.10.2796 14514582

74. McGarry JD, Dobbins RL (1999) Fatty acids, lipotoxicity and insulin secretion. Diabetologia 42(2): 128–138. doi: 10.1007/s001250051130 10064091

75. Ross R, Dagnone D, Jones PJ, Smith H, Paddags A, Hudson R, et al. (2000) Reduction in obesity and related comorbid conditions after diet-induced weight loss or exercise-induced weight loss in men. Ann Intern Med 133: 92–103. doi: 10.7326/0003-4819-133-2-200007180-00008 10896648

76. Houmard JA, Tanner CJ, Slentz CA, Duscha BD, McCartney JS, Kraus WE (2004) Effect of the volume and intensity of exercise training on insulin sensitivity. J Appl Physiol 96: 101–106. doi: 10.1152/japplphysiol.00707.2003 12972442

77. Mayer-Davis EJ, D’Agostino R Jr, Karter AJ, Haffner SM, Rewers MJ, Saad M, et al. (1998) Intensity and amount of physical activity in relation to insulin sensitivity: the insulin resistance atherosclerosis study. JAMA 279: 669–674. doi: 10.1001/jama.279.9.669 9496984

78. van der Heijden GJ, Toffolo G, Manesso E, Sauer PJ, Sunehag AL (2009) Aerobic exercise increases peripheral and hepatic insulin sensitivity in sedentary adolescents. J Clin Endocrinol Metab 94(11): 4292–4299. doi: 10.1210/jc.2009-1379 19808855

79. Winnick JJ, Sherman WM, Habash DL, Stout MB, Failla ML, Belury MA, et al. (2008) Short-term aerobic exercise training in obese humans with type 2 diabetes mellitus improves whole-body insulin sensitivity through gains in peripheral, not hepatic insulin sensitivity. J Clin Endocrinol Metab 93: 771–778. doi: 10.1210/jc.2007-1524 18073312

80. Malin SK, Gerber R, Chipkin SR, Braun B (2012) Independent and combined effects of exercise training and metformin on insulin sensitivity in individuals with prediabetes. Diabetes Care 35(1): 131–136. doi: 10.2337/dc11-0925 22040838

81. Ekström N, Svensson AM, Miftaraj M, Andersson Sundell K, Cederholm J, Zethelius B, et al. (2015) Durability of oral hypoglycemic agents in drug naïve patients with type 2 diabetes: report from the swedish national diabetes register (ndr). BMJ Open Diabetes Research and Care 3: e000059. doi: 10.1136/bmjdrc-2014-000059 25815205

82. Butler AE, Cao-Minh L, Galasso R, Rizza RA, Corradin A, Cobelli C, et al. (2010) Adaptive changes in pancreatic beta cell fractional area and beta cell turnover in human pregnancy. Diabetologia 53(10): 2167–2176. doi: 10.1007/s00125-010-1809-6 20523966

83. Sjöström L, Peltonen M, Jacobson P, Ahlin S, Andersson-Assarsson J, Anveden Å, et al. (2014) Association of bariatric surgery with long-term remission of type 2 diabetes and with microvascular and macrovascular complications. JAMA 311(22): 2297–2304. doi: 10.1001/jama.2014.5988 24915261

84. Courcoulas AP, Belle SH, Neiberg RH, Pierson SK, Eagleton JK, Kalarchian MA, et al. (2015) Three-year outcomes of bariatric surgery vs lifestyle intervention for type 2 diabetes mellitus treatment a randomized clinical trial. JAMA Surg 150(10): 940. doi: 10.1001/jamasurg.2015.1534

85. Mingrone G, Panunzi S, De Gaetano A, Guidone C, Iaconelli A, Nanni G, et al. (2015) Bariatric-metabolic surgery versus conventional medical treatment in obese patients with type 2 diabetes: 5 year follow-up of an open-label, single-centre, randomised controlled trial. Lancet 386: 964–973. doi: 10.1016/S0140-6736(15)00075-6 26369473

86. Panunzi S, De Gaetano A, Carnicelli A, Mingrone G (2015) Predictors of remission of diabetes mellitus in severely obese individuals undergoing bariatric surgery: Do BMI or procedure choice matter? a meta-analysis. Ann Surg 261: 459–467. doi: 10.1097/SLA.0000000000000863 25361217

87. Panunzi S, Carlsson L, De Gaetano A, Peltonen M, Rice T, Sjöström L, et al. (2016) Determinants of diabetes remission and glycemic control after bariatric surgery. Diabetes Care 39: 166–174. doi: 10.2337/dc15-0575 26628418

88. Yokrattanasak J, De Gaetano A, Panunzi S, Satiracoo P, Lawton WM, Lenbury Y (2016) A simple, realistic stochastic model of gastric emptying. PLoS One 11(4): e0153297. doi: 10.1371/journal.pone.0153297 27057750

89. Lehmann ED, Deutsch T (1992) A physiological model of glucose-insulin interaction in type 1 diabetes mellitus. J Biomed Eng 14: 235–242. doi: 10.1016/0141-5425(92)90058-S 1588781

90. Li Y, Chow CC, Courville AB, Sumner AE, Periwal V (2016) Modeling glucose and free fatty acid kinetics in glucose and meal tolerance test. Theor Biol Med Model 13:8: 1–20.

91. Goel P, Parkhi D, Barua A, Shah M, Ghaskadbi S (2008) A minimal model approach for analyzing continuous glucose monitoring in type 2 diabetes. Front Physiol 9:673: 1–8.

92. Mason CC, Hanson RL, Knowler WC (2007) Progression to type 2 diabetes characterized by moderate then rapid glucose increases. Diabetes 56: 2054–2061. doi: 10.2337/db07-0053 17473220

93. Corkey BE (2012) Diabetes: Have we got it all wrong? Diabetes Care 35: 2432–2437.

94. Goel P (2015) Insulin resistance or hypersecretion? the βig picture revisited. J Theor Biol 384: 131–139. doi: 10.1016/j.jtbi.2015.07.033 26300065

95. Toschi E, Camastra S, Sironi A, Masoni A, Gastaldelli A, Mari A, et al. (2002) Effect of acute hyperglycemia on insulin secretion in humans. Diabetes 51S1: S130–S133. doi: 10.2337/diabetes.51.2007.S130

96. Retnakaran R, Qi Y, Harris SB, Hanley AJ, Zinman B (2011) Changes over time in glycemic control, insulin sensitivity, and beta-cell function in response to low-dose metformin and thiazolidinedione combination therapy in patients with impaired glucose tolerance. Diabetes Care 34: 1601–1604. doi: 10.2337/dc11-0046 21709296


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