Exercise,Hypoglycemia,and Type 1 Diabetes

Wahren J , Felig P , Ahlborg G , Jorfeldt L : Glucose metabolism during leg exercise in man. J Clin Invest, 1971; 50:2715–2725.

Felig P , Wahren J : Fuel homeostasis in exercise. N Engl J Med, 1975; 293:1078–1084.

Wasserman DH , Williams PE , Lacy DB , Green DR , Cherrington AD : Importance of intrahepatic mechanisms to gluconeogenesis from alanine during exercise and recovery. Am J Physiol, 1988; 254:E518–E525.

Coggan AR , Swanson SC , Mendenhall LA , Habash DL , Kien CL : Effect of endurance training on hepatic glycogenolysis and gluconeogenesis during prolonged exercise in men. Am J Physiol, 1995; 268:E375–E383.

Wolfe RR , Nadel ER , Shaw JH , Stephenson LA , Wolfe MH : Role of changes in insulin and glucagon in glucose homeostasis in exercise. J Clin Invest, 1986; 77:900–907.

Andersen P , Saltin B : Maximal perfusion of skeletal muscle in man. J Physiol, 1985; 366:233–249.

Nesher R , Karl IE , Kipnis DM : Dissociation of effects of insulin and contraction on glucose transport in rat epitrochlearis muscle. Am J Physiol, 1985; 249:C226–C232.

Yeh JI , Gulve EA , Rameh L , Birnbaum MJ : The effects of wortmannin on rat skeletal muscle. Dissociation of signaling pathways for insulin- and contraction-activated hexose transport. J Biol Chem, 1995; 270:2107–2111.

Lee AD , Hansen PA , Holloszy JO : Wortmannin inhibits insulin-stimulated but not contraction-stimulated glucose transport activity in skeletal muscle. FEBS Lett, 1995; 361:51–54.

Lund S , Holman GD , Schmitz O , Pedersen O : Contraction stimulates translocation of glucose transporter GLUT4 in skeletal muscle through a mechanism distinct from that of insulin. Proc Natl Acad Sci U S A, 1995; 92:5817–5821.

Wasserman DH , Johnson JL , Bupp JL , Lacy DB , Bracy DP : Regulation of gluconeogenesis during rest and exercise in the depancreatized dog. Am J Physiol, 1993; 265:E51–E60.

Wasserman DH , Mohr T , Kelly P , Lacy DB , Bracy D : Impact of insulin deficiency on glucose fluxes and muscle glucose metabolism during exercise. Diabetes, 1992; 41:1229–1238.

Wasserman DH , Williams PE , Lacy DB , Goldstein RE , Cherrington AD : Exercise-induced fall in insulin and hepatic carbohydrate metabolism during muscular work. Am J Physiol, 1989; 256:E500–E509.

Schiavon M , Hinshaw L , Mallad A , Dalla Man C , Sparacino G , Johnson M , Carter R , Basu R , Kudva Y , Cobelli C , Basu A : Postprandial glucose fluxes and insulin sensitivity during exercise: a study in healthy individuals. Am J Physiol Endocrinol Metab, 2013; 305:E557–E566.

Friedlander AL , Casazza GA , Horning MA , Huie MJ , Brooks GA : Training-induced alterations of glucose flux in men. J Appl Physiol, 1997; 82:1360–1369.

Friedlander AL , Casazza GA , Horning MA , Huie MJ , Piacentini MF , Trimmer JK , Brooks GA : Training-induced alterations of carbohydrate metabolism in women: women respond differently from men. J Appl Physiol, 1998; 85:1175–1186.

Perseghin G , Price TB , Petersen KF , Roden M , Cline GW , Gerow K , Rothman DL , Shulman GI : Increased glucose transport-phosphorylation and muscle glycogen synthesis after exercise training in insulin-resistant subjects. N Engl J Med, 1996; 335:1357–1362.

Horton TJ , Grunwald GK , Lavely J , Donahoo WT : Glucose kinetics differ between women and men, during and after exercise. J Appl Physiol, 2006; 100:1883–1894.

Tarnopolsky LJ , MacDougall JD , Atkinson SA , Tarnopolsky MA , Sutton JR : Gender differences in substrate for endurance exercise. J Appl Physiol, 1990; 68:302–308.

Friedlander AL , Casazza GA , Horning MA , Buddinger TF , Brooks GA : Effects of exercise intensity and training on lipid metabolism in young women. Am J Physiol, 1998; 275:E853–E863.

Suh SH , Casazza GA , Horning MA , Miller BF , Brooks GA : Luteal and follicular glucose fluxes during rest and exercise in 3-h postabsorptive women. J Appl Physiol, 2002; 93:42–50.

Suh SH , Casazza GA , Horning MA , Miller BF , Brooks GA : Effects of oral contraceptives on glucose flux and substrate oxidation rates during rest and exercise. J Appl Physiol, 2003; 94:285–294.

Casazza GA , Jacobs KA , Suh SH , Miller BF , Horning MA , Brooks GA : Menstrual cycle phase and oral contraceptive effects on triglyceride mobilization during exercise. J Appl Physiol, 2004; 97:302–309.

Devries MC , Hamadeh MJ , Graham TE , Tarnopolsky MA : 17β-Estradiol supplementation decreases glucose rate of appearance and disappearance with no effect on glycogen utilization during moderate intensity exercise in men. J Clin Endocrinol Metab, 2005; 90:6218–6225. Erratum in J Clin Endocrinol Metab 2006;91:1217.

Richter EA , Garetto LP , Goodman MN , Ruderman NB : Muscle glucose metabolism following exercise in the rat: increased sensitivity to insulin. J Clin Invest, 1982; 69:785–793.

Richter EA , Ruderman NB , Gavras H , Belur ER , Galbo H : Muscle glycogenolysis during exercise: dual control by epinephrine and contractions. Am J Physiol, 1982; 242:E25–E32.

Holloszy JO , Narahara HT : Studies of tissue permeability. X. Changes in permeability to 3-methylglucose associated with contraction of isolated frog muscle. J Biol Chem, 1965; 240:3493–3500.

Ivy JL , Holloszy JO : Persistent increase in glucose uptake by rat skeletal muscle following exercise. Am J Physiol, 1981; 241:C200–C203.

Garetto LP , Richter EA , Goodman MN , Ruderman NB : Enhanced muscle glucose metabolism after exercise in the rat: the two phases. Am J Physiol, 1984; 246:E471–E475.

Richter EA , Garetto LP , Goodman MN , Ruderman NB : Enhanced muscle glucose metabolism after exercise: modulation by local factors. Am J Physiol, 1984; 246:E476–E482.

Holloszy JO , Coyle EF : Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J Appl Physiol, 1984; 56:831–838.

Wallberg-Henriksson H , Holloszy JO : Activation of glucose transport in diabetic muscle: responses to contraction and insulin. Am J Physiol, 1985; 24:C233–C237.

Constable SH , Favier RJ , Cartee GD , Young DA , Holloszy JO : Muscle glucose transport: interactions of in vitro contractions, insulin, and exercise. J Appl Physiol, 1988; 64:2329–2332.

Wallberg-Henriksson H , Constable SH , Young DA , Holloszy JO : Glucose transport into rat skeletal muscle: interaction between exercise and insulin. J Appl Physiol, 1988; 65:909–913.

Zorzano A , Balon TW , Goodman MN , Ruderman NB : Glycogen depletion and increased insulin sensitivity and responsiveness in muscle after exercise. Am J Physiol, 1986; 251:E664–E669.

Gulve EA , Cartee GD , Zierath JR , Corpus VM , Holloszy JO : Reversal of enhanced muscle glucose transport after exercise: roles of insulin and glucose. Am J Physiol, 1990; 259:E685–E691.

Greiwe JS , Hickner RC , Hansen PA , Racette SB , Chen MM , Holloszy JO : Effects of endurance exercise training on muscle glycogen accumulation in humans. J Appl Physiol, 1999; 87:222–226.

Friedman JE , Sherman WM , Reed MJ , Elton CW , Dohm GL : Exercise training increases glucose transporter protein GLUT-4 in skeletal muscle of obese Zucker (fa/fa) rats. FEBS Lett, 1990; 268:13–16.

Ploug T , Stallknecht BM , Pedersen O , Kahn BB , Ohkuwa T , Vinten J , Galbo H : Effect of endurance training on glucose transport capacity and glucose transporter expression in rat skeletal muscle. Am J Physiol, 1990; 259:E778–E786.

Rodnick KJ , Holloszy JO , Mondon CE , James DE : Effects of exercise training on insulin-regulatable glucose-transporter protein levels in rat skeletal muscle. Diabetes, 1990; 39:1425–1429.

Host HH , Hansen PA , Nolte LA , Chen MM , Holloszy JO : Glycogen supercompensation masks the effect of a traininginduced increase in GLUT-4 on muscle glucose transport. J Appl Physiol, 1998; 85:133–138.

Ren JM , Semenkovich CF , Gulve EA , Gao J , Holloszy JO : Exercise induces rapid increases in GLUT4 expression, glucose transport capacity, and insulin-stimulated glycogen storage in muscle. J Biol Chem, 1994; 269:14396–14401.

Short KR , Vittone JL , Bigelow ML , Proctor DN , Rizza RA , Coenen-Schimke JM , Nair KS : Impact of aerobic exercise training on age-related changes in insulin sensitivity and muscle oxidative capacity. Diabetes, 2003; 52:1888–1896.

Treebak JT , Taylor EB , Witczak CA , An D , Toyoda T , Koh HJ , Xie J , Feener EP , Wojtaszewski JF , Hirshman MF , Goodyear LJ : Identification of a novel phosphorylation site on TBC1D4 regulated by AMP-activated protein kinase in skeletal muscle. Am J Physiol Cell Physiol, 2010; 298:C377–C385.

Jessen N , An D , Lihn AS , Nygren J , Hirshman MF , Thorell A , Goodyear LJ : Exercise increases TBC1D1 phosphorylation in human skeletal muscle. Am J Physiol Endocrinol Metab, 2011; 301:E164–E171.

Funai K , Schweitzer GG , Sharma N , Kanzaki M , Cartee GD : Increased AS160 phosphorylation, but not TBC1D1 phosphorylation, with increased postexercise insulin sensitivity in rat skeletal muscle. Am J Physiol Endocrinol Metab, 2009; 297:E242–E251.

Proctor DN , Shen PH , Dietz NM , Eickhoff TJ , Lawler LA , Ebersold EJ , Loeffler DL , Joyner MJ : Reduced leg blood flow during dynamic exercise in older endurance-trained men. J Appl Physiol, 1998; 85:68–75.

Zinker BA , Lacy DB , Bracy DP , Wasserman DH : Role of glucose and insulin loads to the exercising limb in increasing glucose uptake and metabolism. J Appl Physiol, 1993; 74:2915–2921.

Coyle EF , Hagberg JM , Hurley BF , Martin WH , Ehsani AA , Holloszy JO : Carbohydrate feeding during prolonged strenuous exercise can delay fatigue. J Appl Physiol Respir Environ Exerc Physiol, 1983; 55:230–235.

Fritzsche RG , Switzer TW , Hodgkinson BJ , Lee SH , Martin JC , Coyle EF : Water and carbohydrate ingestion during prolonged exercise increase maximal neuromuscular power. J Appl Physiol, 2000; 88:730–737.

Febbraio MA , Chiu A , Angus DJ , Arkinstall MJ , Hawley JA : Effects of carbohydrate ingestion before and during exercise on glucose kinetics and performance. J Appl Physiol, 2000; 89:2220–2226.

Coyle EF , Hamilton MT , Alonso JG , Montain SJ , Ivy JL : Carbohydrate metabolism during intense exercise when hyperglycemic. J Appl Physiol, 1991; 70:834–840.

Fahey AJ , Paramalingam N , Davey RJ , Davis EA , Jones TW , Fournier PA : The effect of a short sprint on postexercise whole-body glucose production and utilization rates in individuals with type 1 diabetes mellitus. J Clin Endocrinol Metab, 2012; 97:4193–4200.

Essen B , Hagenfeldt L , Kaijser L : Utilization of blood-borne and intramuscular substrates during continuous and intermittent exercise in man. J Physiol, 1977; 265:489–506.

Essen B , Kaijser L : Regulation of glycolysis in intermittent exercise in man. J Physiol, 1978; 281:499–511.

Christmass MA , Dawson B , Arthur PG : Effect of work and recovery duration on skeletal muscle oxygenation and fuel use during sustained intermittent exercise. Eur J Appl Physiol Occup Physiol, 1999; 80:436–447.

Christmass MA , Dawson B , Passeretto P , Arthur PG : A comparison of skeletal muscle oxygenation and fuel use in sustained continuous and intermittent exercise. Eur J Appl Physiol Occup Physiol, 1999; 80:423–435.

Mackenzie R , Maxwell N , Castle P , Elliott B , Brickley G , Watt P : Intermittent exercise with and without hypoxia improves insulin sensitivity in individuals with type 2 diabetes. J Clin Endocrinol Metab, 2012; 97:E546–E555.

Maran A , Pavan P , Bonsembiante B , Brugin E , Ermolao A , Avogaro A , Zaccaria M : Continuous glucose monitoring reveals delayed nocturnal hypoglycemia after intermittent high-intensity exercise in nontrained patients with type 1 diabetes. Diabetes Technol Ther, 2010; 12:763–768.

Riddell MC , Milliken J : Preventing exercise-induced hypoglycemia in type 1 diabetes using real-time continuous glucose monitoring and a new carbohydrate intake algorithm: an observational field study. Diabetes Technol Ther, 2011; 13:819–825.

Yardley JE , Kenny GP , Perkins BA , Riddell MC , Malcolm J , Boulay P , Khandwala F , Sigal RJ : Effects of performing resistance exercise before versus after aerobic exercise on glycemia in type 1 diabetes. Diabetes Care, 2012; 35:669–675.

Yardley JE , Kenny GP , Perkins BA , Riddell MC , Balaa N , Malcolm J , Boulay P , Khandwala F , Sigal RJ : Resistance versus aerobic exercise: acute effects on glycemia in type 1 diabetes. Diabetes Care, 2013; 36:537–542.

Chimen M , Kennedy A , Nirantharakumar K , Pang TT , Andrews R , Narendran P : What are the health benefits of physical activity in type 1 diabetes mellitus? A literature review. Diabetologia, 2012; 55:542–551.

Tonoli C , Heyman E , Roelands B , Buyse L , Cheung SS , Berthoin S , Meeusen R : Effects of different types of acute and chronic (training) exercise on glycaemic control in type 1 diabetes mellitus: a meta-analysis. Sports Med, 2012; 42:1059–1080.

Standards of medical care in diabetes—2013. Diabetes Care, 2013; 36(Suppl 1):S11–S66.

Hwang JH , Perseghin G , Rothman DL , Cline GW , Magnusson I , Petersen KF , Shulman GI : Impaired net hepatic glycogen synthesis in insulin-dependent diabetic subjects during mixed meal ingestion. A ¹³C nuclear magnetic resonance spectroscopy study. J Clin Invest, 1995; 95:783–787.

Petersen KF , Price TB , Bergeron R : Regulation of net hepatic glycogenolysis and gluconeogenesis during exercise: impact of type 1 diabetes. J Clin Endocrinol Metab, 2004; 89:4656–4664.

Enoksson S , Caprio SK , Rife F , Shulman GI , Tamborlane WV , Sherwin RS : Defective activation of skeletal muscle and adipose tissue lipolysis in type 1 diabetes mellitus during hypoglycemia. J Clin Endocrinol Metab, 2003; 88:1503–1511.

Yardley JE , Iscoe KE , Sigal RJ , Kenny GP , Perkins BA , Riddell MC : Insulin pump therapy is associated with less post-exercise hyperglycemia than multiple daily injections: an observational study of physically active type 1 diabetes patients. Diabetes Technol Ther, 2013; 15:84–88.

Elleri D , Allen JM , Kumareswaran K , Leelarathna L , Nodale M , Caldwell K , Cheng P , Kollman C , Haidar A , Murphy HR , Wilinska ME , Acerini CL , Dunger DB , Hovorka R : Closed-loop basal insulin delivery over 36 hours in adolescents with type 1 diabetes: randomized clinical trial. Diabetes Care, 2013; 36:838–844.

Breton M , Farret A , Bruttomesso D , Anderson S , Magni L , Patek S , Dalla Man C , Place J , Demartini S , Del Favero S , Toffanin C , Hughes-Karvetski C , Dassau E , Zisser H , Doyle FJ 3rd , De Nicolao G , Avogaro A , Cobelli C , Renard E , Kovatchev B ; International Artificial Pancreas Study Group: Fully integrated artificial pancreas in type 1 diabetes: modular closed-loop glucose control maintains near normoglycemia. Diabetes, 2012; 61:2230–2237.

Russell SJ , El-Khatib FH , Nathan DM , Magyar KL , Jiang J , Damiano ER : Blood glucose control in type 1 diabetes with a bihormonal bionic endocrine pancreas. Diabetes Care, 2012; 35:2148–2155.

Boulé NG , Weisnagel SJ , Lakka TA , Tremblay A , Bergman RN , Rankinen T , Leon AS , Skinner JS , Wilmore JH , Rao DC , Bouchard C ; HERITAGE Family Study: Effects of exercise training on glucose homeostasis: the HERITAGE Family Study. Diabetes Care, 2005; 28:108–114.

Olsen RH , Krogh-Madsen R , Thomsen C , Booth FW , Pedersen BK : Metabolic responses to reduced daily steps in healthy nonexercising men. JAMA, 2008; 299:1261–1263.

van Bon AC , Verbitskiy E , von Basum G , Hoekstra JB , DeVries JH : Exercise in closed-loop control: a major hurdle. J Diabetes Sci Technol, 2011; 5:1337–1341.

Hinshaw L , Man CD , Nandy DK , Saad A , Bharucha AE , Levine JA , Rizza RA , Basu R , Carter RE , Cobelli C , Kudva YC , Basu A : Diurnal pattern of insulin action in type 1 diabetes: implications for a closed loop system. Diabetes, 2013; 62:2223–2229.