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Citations to this article

Hypoglycemia-associated autonomic failure in insulin-dependent diabetes mellitus. Recent antecedent hypoglycemia reduces autonomic responses to, symptoms of, and defense against subsequent hypoglycemia.
S E Dagogo-Jack, … , S Craft, P E Cryer
S E Dagogo-Jack, … , S Craft, P E Cryer
Published March 1, 1993
Citation Information: J Clin Invest. 1993;91(3):819-828. https://doi.org/10.1172/JCI116302.
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Hypoglycemia-associated autonomic failure in insulin-dependent diabetes mellitus. Recent antecedent hypoglycemia reduces autonomic responses to, symptoms of, and defense against subsequent hypoglycemia.

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Abstract

We hypothesize that in patients with insulin-dependent diabetes mellitus (IDDM), recent antecedent iatrogenic hypoglycemia is a major cause of hypoglycemia-associated autonomic failure, a disorder distinct from classical diabetic autonomic neuropathy (CDAN), and that hypoglycemia-associated autonomic failure, by reducing both symptoms of and defense against developing hypoglycemia, results in recurrent iatrogenic hypoglycemia, thus creating a vicious cycle. We used the hyperinsulinemic (12.0 pmol.kg-1.min-1) stepped hypoglycemic clamp technique to assess autonomic and symptomatic responses to hypoglycemia and the insulin infusion test (4.0 pmol.kg-1.min-1) to assess defense against hypoglycemia on mornings before and after clamped afternoon hypoglycemia (approximately 2.8 mmol/liter) and hyperglycemia (approximately 11.1 mmol/liter) in patients with IDDM. Compared with nondiabetic subjects, IDDM with or without CDAN exhibited reduced epinephrine (P = 0.0222 and 0.0040) and pancreatic polypeptide (P = 0.0083 and 0.0056) responses to hypoglycemia. After afternoon hypoglycemia, lower plasma glucose concentrations were required to elicit autonomic and symptomatic responses during morning hypoglycemic clamps in patients without CDAN. At the 2.8 mmol/liter step, mean (+/- SE) epinephrine levels were 1,160 +/- 270 and 2,040 +/- 270 pmol/liter (P = 0.0060), pancreatic and total symptom scores were 22 +/- 3 and 41 +/- 7 (P = 0.0475) after afternoon hypoglycemia and hyperglycemia, respectively. During morning insulin infusion tests after afternoon hypoglycemia, nadir plasma glucose concentrations were 2.6 +/- 0.2 mmol/liter compared with 3.3 +/- 0.3 mmol/liter (P < 0.001) at the corresponding time points after afternoon hyperglycemia. Thus, we conclude: (a) elevated glycemic thresholds for autonomic responses to hypoglycemia are a feature of IDDM per se, not classical diabetic autonomic neuropathy; and (b) a single episode of afternoon hypoglycemia results in both elevated glycemic thresholds for autonomic and symptomatic responses to hypoglycemia and impaired physiological defense against hypoglycemia the next morning in IDDM.

Authors

S E Dagogo-Jack, S Craft, P E Cryer

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HM Rooijackers, EC Wiegers, CJ Tack, M der Graaf, BE de Galan
Cellular and Molecular Life Sciences 2015
Dual-hormone treatment with insulin and glucagon in patients with type 1 diabetes: Dual-Hormone Treatment in Type 1 Diabetes
HK Reiband, S Schmidt, A Ranjan, JJ Holst, S Madsbad, K Nørgaard
Diabetes/Metabolism Research and Reviews 2015
Avoiding or coping with severe hypoglycemia in patients with type 2 diabetes
JS Yun, SH Ko
The Korean Journal of Internal Medicine 2015
Counter-regulatory hormone responses to hypoglycaemia in people with type 1 diabetes after 4 weeks of treatment with liraglutide adjunct to insulin: a randomized, placebo-controlled, double-blind, crossover trial
TR Pieber, S Deller, S Korsatko, L Jensen, E Christiansen, J Madsen, SR Heller
Diabetes Obesity and Metabolism 2015
Hypoglycemia-Associated Autonomic Failure in Diabetes: Maladaptive, Adaptive, or Both?: Figure 1
PE Cryer
Diabetes 2015
International Textbook of Diabetes Mellitus: DeFronzo/International Textbook of Diabetes Mellitus, Fourth Edition
RN Bergman, M Ader
International Textbook of Diabetes Mellitus: DeFronzo/International Textbook of Diabetes Mellitus, Fourth Edition 2015
Plasma insulin profiles after subcutaneous injection: how close can we get to physiology in people with diabetes?
PD Home
Diabetes Obesity and Metabolism 2015
Recurrent Hypoglycemia Increases Anxiety and Amygdala Norepinephrine Release During Subsequent Hypoglycemia
E McNay
Frontiers in Endocrinology 2015
Philip E. Cryer, MD: Seminal Contributions to the Understanding of Hypoglycemia and Glucose Counterregulation and the Discovery of HAAF (Cryer Syndrome)
S Dagogo-Jack
Diabetes care 2015
Impaired Awareness of Hypoglycemia in Adults With Type 1 Diabetes Is Not Associated With Autonomic Dysfunction or Peripheral Neuropathy
SE Olsen, MR Bjørgaas, BO Åsvold, T Sand, M Stjern, BM Frier, KB Nilsen
Diabetes care 2015
Endocrinology and Diabetes
R Ajjan, SM Orme
2015
Hypothalamic glucose sensing: making ends meet
VH Routh, L Hao, AM Santiago, Z Sheng, C Zhou
Frontiers in systems neuroscience 2014
The clinical impact of inpatient hypoglycemia
E Brutsaert, M Carey, J Zonszein
Journal of Diabetes and its Complications 2014
Defective Glucagon Secretion During Hypoglycemia After Intrahepatic But Not Nonhepatic Islet Autotransplantation: Autoislets and Defective Glucagon Secretion
MD Bellin, S Parazzoli, E Oseid, LD Bogachus, C Schuetz, ME Patti, T Dunn, T Pruett, AN Balamurugan, B Hering, G Beilman, DE Sutherland, RP Robertson
American Journal of Transplantation 2014
Increased Risk of Severe Hypoglycemic Events with Increasing Frequency of Non-severe Hypoglycemic Events in Patients with Type 1 and Type 2 Diabetes
S Sreenan, M Andersen, BL Thorsted, ML Wolden, M Evans
Diabetes Therapy 2014
Hypoglycemia-Associated Changes in the Electroencephalogram in Patients With Type 1 Diabetes and Normal Hypoglycemia Awareness or Unawareness
AS Sejling, TW Kjær, U Pedersen-Bjergaard, SS Diemar, CS Frandsen, L Hilsted, J Faber, JJ Holst, L Tarnow, MN Nielsen, LS Remvig, B Thorsteinsson, CB Juhl
Diabetes 2014
Diabetische Notfallsituationen – die Hypoglykämie
T Siegmund, PM Schumm-Draeger
Der Diabetologe 2014
Clinical Autonomic Dysfunction
J Colombo, R Arora, NL DePace, AI Vinik
2014
Diabetologie kompakt
H Schatz, AF Pfeiffer
2014
Glycaemic variability in diabetes: a tool for assessing the quality of glycaemic control and the risk of complications
VV Klimontov, NE Myakina
Diabetes mellitus 2014
Increased brain transport and metabolism of acetate in hypoglycemia unawareness
BI Gulanski, HM de Feyter, KA Page, R Belfort-DeAguiar, GF Mason, DL Rothman, RS Sherwin
The Journal of clinical endocrinology and metabolism 2013
Increased brain lactate concentrations without increased lactate oxidation during hypoglycemia in type 1 diabetic individuals
HM de Feyter, GF Mason, GI Shulman, DL Rothman, KF Petersen
Diabetes 2013
Role of Synaptic Plasticity and EphA5-EphrinA5 Interaction Within the Ventromedial Hypothalamus in Response to Recurrent Hypoglycemia
B Szepietowska, TL Horvath, RS Sherwin
Diabetes 2013
Lactate and the Mechanism of Hypoglycemia-Associated Autonomic Failure in Diabetes
AM Arbelaez, PE Cryer
Diabetes 2013
2. Hypoglycemia Detection
Routh VH, Donovan CM, Ritter S
Translational endocrinology & metabolism 2013
Diabetic status and the relation of the three domains of glycemic control to mortality in critically ill patients: an international multicenter cohort study
JS Krinsley, M Egi, A Kiss, AN Devendra, P Schuetz, PM Maurer, MJ Schultz, RT van Hooijdonk, M Kiyoshi, IM Mackenzie, D Annane, P Stow, SA Nasraway, S Holewinski, U Holzinger, JC Preiser, JL Vincent, R Bellomo
Critical Care 2013
Hypoglycemia in Patients with Type 1 Diabetes: Epidemiology, Pathogenesis, and Prevention
O Awoniyi, R Rehman, S Dagogo-Jack
Current Diabetes Reports 2013
The Role of Bromocriptine-QR in the Management of Type 2 Diabetes Expert Panel Recommendations
AJ Garber, L Blonde, ZT Bloomgarden, Y Handelsman, S Dagogo-Jack
Endocrine Practice 2013
Mechanisms of Hypoglycemia-Associated Autonomic Failure in Diabetes
DL Longo, PE Cryer
New England Journal of Medicine 2013
Hypoglycaemia in Clinical Diabetes
IA Macdonald, P King
Hypoglycaemia in Clinical Diabetes 2013
Diabetes, insulin-mediated glucose metabolism and Sertoli/blood-testis barrier function
MG Alves, AD Martins, JE Cavaco, S Socorro, PF Oliveira
Tissue Barriers 2013
Hypoglycemia and diabetes: a report of a workgroup of the American Diabetes Association and the Endocrine Society
ER Seaquist, J Anderson, B Childs, P Cryer, S Dagogo-Jack, L Fish, SR Heller, H Rodriguez, J Rosenzweig, R Vigersky
Diabetes care 2013
Lack of association between residual insulin production and glucagon response to hypoglycemia in youth with short duration of type 1 diabetes
J Sherr, D Xing, KJ Ruedy, RW Beck, C Kollman, B Buckingham, NH White, L Fox, E Tsalikian, S Weinzimer, AM Arbelaez, WV Tamborlane,
Diabetes care 2013
Amelioration of hypoglycemia via somatostatin receptor type 2 antagonism in recurrently hypoglycemic diabetic rats
JT Yue, MC Riddell, E Burdett, DH Coy, S Efendic, M Vranic
Diabetes 2013
Restoration of Self-Awareness of Hypoglycemia in Adults With Long-Standing Type 1 Diabetes: Hyperinsulinemic-hypoglycemic clamp substudy results from the HypoCOMPaSS trial
L Leelarathna, SA Little, E Walkinshaw, HK Tan, A Lubina-Solomon, K Kumareswaran, AP Lane, T Chadwick, SM Marshall, J Speight, D Flanagan, SR Heller, JA Shaw, ML Evans
Diabetes care 2013
Lack of Association Between Residual Insulin Production and Glucagon Response to Hypoglycemia in Youth With Short Duration of Type 1 Diabetes
J Sherr, D Xing, KJ Ruedy, RW Beck, C Kollman, B Buckingham, NH White, L Fox, E Tsalikian, S Weinzimer, AM Arbelaez, WV Tamborlane
Diabetes care 2013
Treating type 1 diabetes: from strategies for insulin delivery to dual hormonal control
A L McCall, L S Farhy
Minerva endocrinologica 2013
Hypoglycemia and Diabetes: A Report of a Workgroup of the American Diabetes Association and The Endocrine Society
ER Seaquist, J Anderson, B Childs, P Cryer, S Dagogo-Jack, L Fish, SR Heller, H Rodriguez, J Rosenzweig, R Vigersky
The Journal of clinical endocrinology and metabolism 2013
Endocrinology of Physical Activity and Sport
N Constantini, AC Hackney
2013
Minireview: Glucagon in the Pathogenesis of Hypoglycemia and Hyperglycemia in Diabetes
PE Cryer
Endocrinology 2012
Impact of Hypoglycemia in Hospitalized Patients
M Carey, L Boucai, J Zonszein
Current Diabetes Reports 2012
The importance of hypoglycemia in diabetic patients
G Shafiee, M Mohajeri-Tehrani, M Pajouhi, B Larijani
Journal of Diabetes & Metabolic Disorders 2012
Glucagon secretion and signaling in the development of diabetes
HY Gaisano, PE Macdonald, M Vranic
Frontiers in physiology 2012
Insight into hypoglycemia in pediatric type 1 diabetes mellitus
KE Lehecka, VS Renukuntla, RA Heptulla
International Journal of Pediatric Endocrinology 2012
The impact of premorbid diabetic status on the relationship between the three domains of glycemic control and mortality in critically ill patients :
JS Krinsley, G Meyfroidt, G Berghe, M Egi, R Bellomo
Current Opinion in Clinical Nutrition & Metabolic Care 2012
Recurrent spontaneous hypoglycaemia causes loss of neurogenic and neuroglycopaenic signs in infants with congenital hyperinsulinism : Silent hypoglycaemia in CHI
HT Christesen, K Brusgaard, K Hussain
Clinical Endocrinology 2012
Nocturnal Hypertension and Special - Period Hypertension in Type 1 Diabetes Mellitus
C Cobuz, M Cobuz
Romanian Journal of Diabetes Nutrition and Metabolic Diseases 2012
Pharmacokinetic and pharmacodynamic modeling for the effect of sodium-glucose cotransporter inhibitors on blood glucose level and renal glucose excretion in db/db mice
K Yamaguchi, M Kato, K Ozawa, T Kawai, T Yata, Y Aso, M Ishigai, S Ikeda
Journal of Pharmaceutical Sciences 2012
The dead in bed syndrome revisited: a review of the evidence
PJ Weston
Diabetes Management 2012
NMDA receptor blockade by memantine does not prevent adaptation to recurrent hypoglycaemia in healthy men
J Klement, I Pais, J Strube, H Lehnert, A Peters, M Hallschmid, J Born
Diabetes, Obesity and Metabolism 2012
Opioid receptor blockade prevents exercise-associated autonomic failure in humans
S Milman, J Leu, H Shamoon, S Vele, I Gabriely
Diabetes 2012
Moderate Recurrent Hypoglycemia Markedly Impairs Set-Shifting Ability in a Rodent Model: Cognitive and Neurochemical Effects
V Jahagirdar, J Ramcharitar, VE Cotero, EC McNay
The Open Diabetes Journal 2012
2. Hypoglycemia Detection
VH Routh, CM Donovan, S Ritter
2012
Type 1 Diabetes
I Gallen
2012
Autonomic imbalance: prophet of doom or scope for hope?
AI Vinik, RE Maser, D Ziegler
Diabetic Medicine 2011
BAD Modulates Counterregulatory Responses to Hypoglycemia and Protective Glucoprivic Feeding
MA Osundiji, ML Godes, ML Evans, NN Danial
PloS one 2011
Handbook of Clinical Neurology
T Ashizawa, PS Sarkar
Muscular Dystrophies 2011
Applications of Microdialysis in Pharmaceutical Science
I Smolders, R Clinckers, Y Michotte
Applications of Microdialysis in Pharmaceutical Science 2011
Modeling the Consistency of Hypoglycemic Symptoms: High Variability in Diabetes
NN Zammitt, G Streftaris, GJ Gibson, IJ Deary, BM Frier
Diabetes Technology & Therapeutics 2011
Hypoglycemia Risk and Glucose Variability Indices Derived from Routine Self-Monitoring of Blood Glucose Are Related to Laboratory Measures of Insulin Sensitivity and Epinephrine Counterregulation
AN Pitsillides, SM Anderson, B Kovatchev
Diabetes Technology & Therapeutics 2011
The effect of antecedent hypoglycaemia on β2-adrenergic sensitivity in healthy participants with the Arg16Gly polymorphism of the β2-adrenergic receptor
BJ Schouwenberg, P Smits, CJ Tack, BE de Galan
Diabetologia 2011
Recurrent hypoglycemia increases oxygen glucose deprivation-induced damage in hippocampal organotypic slices
KR Dave, A Pileggi, AP Raval
Neuroscience Letters 2011
Hypoglycaemia unawareness
J Elliott, S Heller
Practical Diabetes International 2011
Hypoglycemia unawareness
SO Bakatselos
Diabetes Research and Clinical Practice 2011
Brain glycogen content and metabolism in subjects with type 1 diabetes and hypoglycemia unawareness
G Öz, N Tesfaye, A Kumar, DK Deelchand, LE Eberly, ER Seaquist
Journal of Cerebral Blood Flow & Metabolism 2011
Recent Advances in the Prevention of Hypoglycemia in Type 1 Diabetes
JM Realsen, HP Chase
Diabetes Technology & Therapeutics 2011
Hypoglycemia in sepsis: Biomarker, mediator, or both?* :
R Bellomo, M Egi
Critical Care Medicine 2011
Exercise-related hypoglycemia in diabetes mellitus
LM Younk, M Mikeladze, D Tate, SN Davis
Expert Review of Endocrinology & Metabolism 2011
Williams Textbook of Endocrinology
DW Cooke, SA Divall, S Radovick
Williams Textbook of Endocrinology 2011
The Effect of Glycemic Variability on Counterregulatory Hormone Responses to Hypoglycemia in Young Children and Adolescents with Type 1 Diabetes
N Alghothani, KM Dungan
Diabetes Technology & Therapeutics 2011
Optimizing reduction in basal hyperglucagonaemia to repair defective glucagon counterregulation in insulin deficiency
LS Farhy, AL McCall
Diabetes Obesity and Metabolism 2011
Opioid receptor blockade improves hypoglycemia-associated autonomic failure in type 1 diabetes mellitus
S Vele, S Milman, H Shamoon, I Gabriely
The Journal of clinical endocrinology and metabolism 2011
Adrenergic Mediation of Hypoglycemia-Associated Autonomic Failure
R Ramanathan, PE Cryer
Diabetes 2011
Glycemic Control in the ICU
M Egi, S Finfer, R Bellomo
Chest 2011
BAD Modulates Counterregulatory Responses to Hypoglycemia and Protective Glucoprivic Feeding
MA Osundiji, ML Godes, ML Evans, NN Danial, OS Shirihai
PloS one 2011
Patient-Specific Modeling in Tomorrow's Medicine
A Gefen
2011
Brain Insulin Action Regulates Hypothalamic Glucose Sensing and the Counterregulatory Response to Hypoglycemia
KA Diggs-Andrews, X Zhang, Z Song, D Daphna-Iken, VH Routh, SJ Fisher
Diabetes 2010
Mini-review: impact of recurrent hypoglycemia on cognitive and brain function
EC McNay, VE Cotero
Physiology & Behavior 2010
Hypoglycemia in Type 1 Diabetes Mellitus*
PE Cryer
Endocrinology and metabolism clinics of North America 2010
Textbook of Diabetes
PM Jones, SJ Persaud
Textbook of Diabetes 2010
A Practical Manual of Diabetes in Pregnancy
FH Einstein
A Practical Manual of Diabetes in Pregnancy 2010
Silent Myocardial Infarction and Hypoglycaemia
HK Goh, M Chia, YW Ooi, DE Chew
The Endocrinologist 2010
Hypoglycemia induced behavioural deficit and decreased GABA receptor, CREB expression in the cerebellum of streptozoticin induced diabetic rats
A Sherin, KT Peeyush, G Naijil, R Chinthu, CS Paulose
Brain Research Bulletin 2010
Neuroendocrine Responses to Hypoglycemia
N Tesfaye, ER Seaquist
Annals of the New York Academy of Sciences 2010
Improving Epinephrine Responses in Hypoglycemia Unawareness With Real-Time Continuous Glucose Monitoring in Adolescents With Type 1 Diabetes
TT Ly, J Hewitt, RJ Davey, EM Lim, EA Davis, TW Jones
Diabetes care 2010
Insulin Reciprocally Regulates Glucagon Secretion in Humans
BA Cooperberg, PE Cryer
Diabetes 2010
Neuropathy: The Crystal Ball for Cardiovascular Disease?
AI Vinik, RE Maser, D Ziegler
Diabetes care 2010
Odyssey between Scylla and Charybdis through storms of carbohydrate metabolism and diabetes: a career retrospective
M Vranic
American journal of physiology. Endocrinology and metabolism 2010
Pulmonary surfactant: an immunological perspective
ZC Chroneos, Z Sever-Chroneos, VL Shepherd
Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology 2009
Evaluation and Management of Adult Hypoglycemic Disorders: An Endocrine Society Clinical Practice Guideline
PE Cryer, L Axelrod, AB Grossman, SR Heller, VM Montori, ER Seaquist, FJ Service
The Journal of clinical endocrinology and metabolism 2009
Guidelines on the current best practice for the management of type 1 diabetes, sport and exercise
E Perry, IW Gallen
Practical Diabetes International 2009
Endocrine Emergencies
WR Furman
ASA Refresher Courses in Anesthesiology 2009
Brain insulin infusion does not augment the counterregulatory response to hypoglycemia or glucoprivation
KK Ishihara, SC Haywood, D Daphna-Iken, EC Puente, SJ Fisher
Metabolism 2009
What is a NICE-SUGAR for patients in the intensive care unit?
R Bellomo, M Egi
Mayo Clinic proceedings. Mayo Clinic 2009
What Is a NICE-SUGAR for Patients in the Intensive Care Unit?
R Bellomo, M Egi
Mayo Clinic Proceedings 2009
Hormones, Brain and Behavior
J Bernal
Hormones, Brain and Behavior 2009
Attenuated Sympathoadrenal Responses, but Not Severe Hypoglycemia, During Aggressive Glycemic Therapy of Early Type 2 Diabetes
SA Amiel, PE Cryer
Diabetes 2009
Diabetes-Related Medication-Induced Hypoglycemia
KL Tackett, CS Lancaster, KL Tackett, MK L.
Journal of Pharmacy Practice 2009
Hypoglycemia-Associated Autonomic Failure Is Prevented by Opioid Receptor Blockade
J Leu, MH Cui, H Shamoon, I Gabriely
The Journal of clinical endocrinology and metabolism 2009
Blunted counterregulatory hormone responses to hypoglycemia in young children and adolescents with well-controlled type 1 diabetes.
Tsalikian E, Tamborlane W, Xing D, Becker DM, Mauras N, Fiallo-Scharer R, Buckingham B, Weinzimer S, Steffes M, Singh R, Beck R, Ruedy K, Kollman C
Diabetes care 2009
The selective serotonin reuptake inhibitor sertraline enhances counterregulatory responses to hypoglycemia
NM Sanders, CW Wilkinson, GJ Taborsky, S Al-Noori, W Daumen, A Zavosh, DP Figlewicz
American journal of physiology. Endocrinology and metabolism 2008
Diabetic neuropathy: mechanisms to management
JL Edwards, AM Vincent, HT Cheng, EL Feldman
Pharmacology & Therapeutics 2008
Glucagon is absorbed from the rectum but does not hasten recovery from hypoglycaemia in patients with type 1 diabetes
DR Parker, GD Braatvedt, A Bargiota, PG Newrick, S Brown, G Gamble, RJ Corrall
British Journal of Clinical Pharmacology 2008
Prevention of Hypoglycemia While Achieving Good Glycemic Control in Type 1 Diabetes: The role of insulin analogs
P Rossetti, F Porcellati, GB Bolli, CG Fanelli
Diabetes care 2008
Increased GABAergic Tone in the Ventromedial Hypothalamus Contributes to Suppression of Counterregulatory Reponses After Antecedent Hypoglycemia
O Chan, H Cheng, R Herzog, D Czyzyk, W Zhu, A Wang, RJ McCrimmon, MR Seashore, RS Sherwin
Diabetes 2008
The Barrier of Hypoglycemia in Diabetes
PE Cryer
Diabetes 2008
The effect of long-term insulin treatment with and without antecedent hypoglycemia on neuropeptide and corticosteroid receptor expression in the brains of diabetic rats
KE Inouye, O Chan, JT Yue, M Andrews, Q Li, SG Matthews, M Vranic
Brain Research Bulletin 2008
Lower levels of circulating IGF-I in Type1 diabetic women with frequent severe hypoglycaemia during pregnancy
LR Nielsen, A Juul, U Pedersen-Bjergaard, B Thorsteinsson, P Damm, ER Mathiesen
Diabetic Medicine 2008
Antecedent Hypoglycemia Impairs Autonomic Cardiovascular Function: Implications for Rigorous Glycemic Control
GK Adler, I Bonyhay, H Failing, E Waring, S Dotson, R Freeman
Diabetes 2008
Hospitalization and Discharge Education of Emergency Department Patients With Hypoglycemia
AA Ginde, DJ Pallin, CA Camargo
The Diabetes Educator 2008
Regional Brain Activation during Hypoglycemia in Type 1 Diabetes
G Musen, DC Simonson, NR Bolo, A Driscoll, K Weinger, A Raji, J Théberge, PF Renshaw, AM Jacobson
The Journal of clinical endocrinology and metabolism 2008
Type 2 Diabetes Mellitus
MN Feinglos, MA Bethel
2008
Vzaimosvyaz' mezhdu avtonomnoy nevropatiey i bessimptomnymi gipoglikemiyami u patsientov s sakharnym diabetom 1 tipa
OV Svetlova, IV Gur'eva, SN Puzin, OY Vasilenko, EV Orlova
Diabetes mellitus 2008
Modeling the Effect of Blood Glucose and Physical Exercise on Plasma Adrenaline in People with Type 1 Diabetes
J Kildegaard, TF Christensen, MD Johansen, J Randløv, OK Hejlesen
Diabetes Technology & Therapeutics 2007
Insulin Therapy and Hypoglycemia in Type 2 Diabetes Mellitus
PE Cryer, I E., MM Karl
Insulin 2007
Attenuation of counterregulatory responses to recurrent hypoglycemia by active thalamic inhibition: a mechanism for hypoglycemia-associated autonomic failure
AM Arbelaez, WJ Powers, TO Videen, JL Price, PE Cryer
Diabetes 2007
Type 1 Diabetes in Adults: Principles and Practice
J Cropsey, M Fineman
Type 1 Diabetes in Adults: Principles and Practice 2007
Attenuation of Amydgala and Frontal Cortical Responses to Low Blood Glucose Concentration in Asymptomatic Hypoglycemia in Type 1 Diabetes: A New Player in Hypoglycemia Unawareness?
JT Dunn, I Cranston, PK Marsden, SA Amiel, LJ Reed
Diabetes 2007
A Role for the Forebrain in Mediating Time-of-Day Differences in Glucocorticoid Counterregulatory Responses to Hypoglycemia in Rats
LM Gorton, AM Khan, MA Bohland, G Sanchez-Watts, CM Donovan, AG Watts
Endocrinology 2007
Mechanisms of sympathoadrenal failure and hypoglycemia in diabetes
PE Cryer
Journal of Clinical Investigation 2006
Antecedent Hindbrain Glucoprivation Does Not Impair the Counterregulatory Response to Hypoglycemia
NM Sanders, GJ Taborsky, CW Wilkinson, W Daumen, DP Figlewicz
Diabetes 2006
Hypoglycemia
JM Guettier, P Gorden
Endocrinology & Metabolism Clinics of North America 2006
Physical activity, sport, and pediatric diabetes
MC Riddell, KE Iscoe
Pediatric Diabetes 2006
Effect of chronic hypoglycaemia on glucose concentration and glycogen content in rat brain: a localized13C NMR study
H Lei, R Gruetter
Journal of Neurochemistry 2006
Feeding and neuroendocrine responses after recurrent insulin-induced hypoglycemia
NM Sanders, DP Figlewicz, GJ Taborsky, CW Wilkinson, W Daumen, BE Levin
Physiology & Behavior 2006
From bedside to bench and back again: research issues in animal models of human disease
NC Tkacs, HJ Thompson
Biological research for nursing 2006
Antecedent hypoglycemia does not alter increased epinephrine-induced lipolysis in type 1 diabetes mellitus
RP Hoffman
Metabolism 2006
Type 1 Diabetes and Vigorous Exercise: Applications of Exercise Physiology to Patient Management
MC Riddell, BA Perkins
Canadian Journal of Diabetes 2006
Hormonal, subjective, and neurocognitive responses to brief hypoglycemia in postmenopausal women and age-matched men with type 2 diabetes mellitus
JP Bremer, M Baron, H Peters, KM Oltmanns, W Kern, HL Fehm, J Born, B Schultes
Metabolism 2006
Antecedent hypercortisolemia is not primarily responsible for generating hypoglycemia-associated autonomic failure
Philip A Goldberg, Ram Weiss, Rory J McCrimmon, Ellen V Hintz, James D Dziura, Robert S Sherwin
Diabetes 2006
Effects of Insulin Treatment without and with Recurrent Hypoglycemia on Hypoglycemic Counterregulation and Adrenal Catecholamine-Synthesizing Enzymes in Diabetic Rats
KE Inouye, JT Yue, O Chan, T Kim, EM Akirav, E Park, MC Riddell, E Burdett, SG Matthews, M Vranic
Endocrinology 2006
The effect of pramlintide on hormonal, metabolic or symptomatic responses to insulin-induced hypoglycaemia in patients with type 1 diabetes
SA Amiel, SR Heller, IA Macdonald, SL Schwartz, LJ Klaff, JA Ruggles, C Weyer, OG Kolterman, DG Maggs
Diabetes, Obesity and Metabolism 2005
Hypoglycaemia and cognitive function
RE Warren, BM Frier
Diabetes, Obesity and Metabolism 2005
Preserved inhibitory effect of recurrent hypoglycaemia on the male gonadotrophic axis
KM Oltmanns, A Peters, W Kern, HL Fehm, J Born, B Schultes
Clinical Endocrinology 2005
Epidemiology of Type 2 Diabetes: Focus on Ethnic Minorities
LE Egede, S Dagogo-Jack
Medical Clinics of North America 2005
Antecedent hypoglycaemia attenuates vascular endothelial growth factor response to subsequent hypoglycaemia in healthy men
V Merl, A Peters, KM Oltmanns, W Kern, C Hubold, HL Fehm, J Born, B Schultes
Diabetic Medicine 2005
Brain glucose concentrations in healthy humans subjected to recurrent hypoglycemia
AB Criego, I Tkac, A Kumar, W Thomas, R Gruetter, ER Seaquist
Journal of Neuroscience Research 2005
Hypoglycemia, Hypoglycemia Unawareness and Counterregulation in Children and Adolescents with Type 1 Diabetes Mellitus
Ε Böber, Α Büyükgebiz, Α Verrotti, F Chiarelli
Journal of Pediatric Endocrinology and Metabolism 2005
Subcutaneous insulin: pharmacokinetic variability and glycemic variability
B Guerci, JP Sauvanet
Diabetes & Metabolism 2005
International Review of Neurobiology
ZT Bloomgarden
International review of neurobiology 2005
Differential adaptation of neurocognitive brain functions to recurrent hypoglycemia in healthy men
B Schultes, W Kern, K Oltmanns, A Peters, S Gais, HL Fehm, J Born
Psychoneuroendocrinology 2005
Brain glucose concentrations in poorly controlled diabetes mellitus as measured by high-field magnetic resonance spectroscopy
ER Seaquist, I Tkac, G Damberg, W Thomas, R Gruetter
Metabolism 2005
Effects of diabetes and recurrent hypoglycemia on the regulation of the sympathoadrenal system and hypothalamo-pituitary-adrenal axis
KE Inouye, O Chan, JT Yue, SG Matthews, M Vranic
American journal of physiology. Endocrinology and metabolism 2005
Insulin therapy and hypoglycaemia: the size of the problem
CG Fanelli, F Porcellati, S Pampanelli, GB Bolli
Diabetes/Metabolism Research and Reviews 2004
Hypoglycemia in Type 1 Diabetes Mellitus
S Dagogo-Jack
Treatments in Endocrinology 2004
Practical Management of Type 1 Diabetes Mellitus in Adolescent Patients
RP Hoffman
Treatments in Endocrinology 2004
Brain glucose concentrations in patients with type 1 diabetes and hypoglycemia unawareness
AB Criego, I Tkac, A Kumar, W Thomas, R Gruetter, ER Seaquist
Journal of Neuroscience Research 2004
Hypoglycemia in type 2 diabetes
S Banarer, PE Cryer
Medical Clinics of North America 2004
Morbidity of hypoglycemia in type 1 diabetes
BM Frier
Diabetes Research and Clinical Practice 2004
Unstable and Brittle Diabetes
B Ravikumar, R Taylor
Unstable and Brittle Diabetes 2004
Differences between nighttime and daytime hypoglycemia counterregulation in healthy humans
V Merl, W Kern, A Peters, KM Oltmanns, S Gais, J Born, HL Fehm, B Schultes
Metabolism 2004
Hypoglycemia and the sympathoadrenal system: neurogenic symptoms are largely the result of sympathetic neural, rather than adrenomedullary, activation
MA DeRosa, PE Cryer
American journal of physiology. Endocrinology and metabolism 2004
Transplantation of the Pancreas
RW Gruessner, DE Sutherland
2004
International Textbook of Diabetes Mellitus
RA DeFronzo, L Mandarino, E Ferrannini
International Textbook of Diabetes Mellitus 2003
Modulation of hunger by plasma glucose and metformin
B Schultes, KM Oltmanns, W Kern, HL Fehm, J Born, A Peters
The Journal of clinical endocrinology and metabolism 2003
NOCTURNAL HYPOGLYCEMIA: CLINICAL MANIFESTATIONS AND THERAPEUTIC STRATEGIES TOWARD PREVENTION
KV Allen, BM Frier
Endocrine Practice 2003
Monocarboxylate transporters contribute to the adaptation of neuronal activity to repeated glucose deprivation in the rat lateral septal nucleus
H Hasuo, T Akasu
Synapse (New York, N.Y.) 2003
Come prevenire e trattare l’ipoglicemia e la sindrome dell’“hypoglycaemia unawareness” nel diabete mellito di tipo 1
GB Bolli, F Porcellati
L'Endocrinologo 2003
Pediatric Diabetes
RK Menon, MA Sperling
Pediatric Diabetes 2003
Role of Hypolipidemic Drug Clofibrate in Altering Iron Regulatory Proteins IRP1 and IRP2 Activities and Hepatic Iron Metabolism in Rats Fed a Low-Iron Diet
HL Huang, NS Shaw
Toxicology and Applied Pharmacology 2002
Residual insulin secretion is not coupled to a maintained glucagon response to hypoglycaemia in long-term type 1 diabetes
S Sjoberg, B Ahren, J Bolinder
Journal of Internal Medicine 2002
Maternal hypoglycemia during pregnancy in type 1 diabetes: maternal and fetal consequences
EW Braak, IM Evers, DW Erkelens, GH Visser
Diabetes/Metabolism Research and Reviews 2002
Does insulin lispro preserve the physiological defences to hypoglycaemia during intensive insulin therapy with a conventional basal bolus regimen?
SR Heller, SA Amiel, ML Evans, MF Kong, IA Macdonald, SR Peacey
Diabetes, Obesity and Metabolism 2002
Modest contribution of psychosocial variables to hypoglycaemic awareness in Type 1 diabetes
S Broers, KP van Vliet, W Everaerd, SL Cessie, JK Radder
Journal of Psychosomatic Research 2002
Fisiopatología de la hipoglucemia en la diabetes mellitus
A Rovira
Endocrinología y Nutrición 2002
Limited impact of vigorous exercise on defenses against hypoglycemia: relevance to hypoglycemia-associated autonomic failure
VP McGregor, JS Greiwe, S Banarer, PE Cryer
Diabetes 2002
Intraislet hyperinsulinemia prevents the glucagon response to hypoglycemia despite an intact autonomic response
S Banarer, VP McGregor, PE Cryer
Diabetes 2002
Hypoglycemia-Associated Autonomic Failure in Advanced Type 2 Diabetes
SA Segel, DS Paramore, PE Cryer
Diabetes 2002
Diabetes Impairs Hypothalamo-Pituitary-Adrenal (HPA) Responses to Hypoglycemia, and Insulin Treatment Normalizes HPA but not Epinephrine Responses
O Chan, S Chan, K Inouye, K Shum, SG Matthews, M Vranic
Diabetes 2002
Elevated endogenous cortisol reduces autonomic neuroendocrine and symptom responses to subsequent hypoglycemia
VP McGregor, S Banarer, PE Cryer
American journal of physiology. Endocrinology and metabolism 2002
Effects of recurrent hyperinsulinemia with and without hypoglycemia on counterregulation in diabetic rats
K Inouye, K Shum, O Chan, J Mathoo, SG Matthews, M Vranic
American journal of physiology. Endocrinology and metabolism 2002
Symptoms of hypoglycaemia in people with diabetes
V McAulay, IJ Deary, BM Frier
Diabetic Medicine 2001
Bystanders or Bad Seeds? Many Autoimmune-target Cells May Be Transforming to Cancer and Signalling “Danger” to the Immune System
BP Reines
Autoimmunity 2001
Sexual dimorphism in counterregulatory responses to hypoglycemia after antecedent exercise
P Galassetti, AR Neill, D Tate, AC Ertl, DH Wasserman, SN Davis
The Journal of clinical endocrinology and metabolism 2001
Effect of Acute and Antecedent Hypoglycemia on Sympathetic Neural Activity and Catecholamine Responsiveness in Normal Rats
WI Sivitz, JA Herlein, DA Morgan, BD Fink, BG Phillips, WG Haynes
Diabetes 2001
Cardiac responses to insulin-induced hypoglycemia in nondiabetic and intensively treated type 1 diabetic patients
RR Russell, D Chyun, S Song, RS Sherwin, WV Tamborlane, FA Lee, MA Pfeifer, F Rife, FJ Wackers, LH Young
American journal of physiology. Endocrinology and metabolism 2001
Hypoglycemia-associated autonomic failure in diabetes
PE Cryer
American journal of physiology. Endocrinology and metabolism 2001
Brain glucosensing and the KATP channel
BE Levin, AA Dunn-Meynell, VH Routh
Nature Neuroscience 2001
Effects of antecedent hypoglycemia, hyperinsulinemia, and excess corticosterone on hypoglycemic counterregulation
K Shum, K Inouye, O Chan, J Mathoo, D Bilinski, SG Matthews, M Vranic
American journal of physiology. Endocrinology and metabolism 2001
Klinische Endokrinologie und Stoffwechsel
PP Nawroth, R Ziegler
2001
Klinische Diabetologie
BO Böhm, KD Palitzsch, C Rosak, GA Spinas
2001
Physiological responses during hypoglycaemia induced by regular human insulin or a novel human analogue, insulin glargine
S Dagogo-Jack, H Askari, B Morrill, LL Lehner, B Kim, X Sha
Diabetes, Obesity and Metabolism 2000
Hypoglycemia: A Complication of Diabetes Therapy in Children
DJ Becker, CM Ryan
Trends in Endocrinology & Metabolism 2000
Changes of glucose transporters in the cerebral adaptation to hypoglycemia
DH Lee, MY Chung, JU Lee, DG Kang, YW Paek
Diabetes Research and Clinical Practice 2000
HYPOGLYCEMIA
G Herbel, PJ Boyle
Endocrinology and metabolism clinics of North America 2000
Preserved hypothermic response to hypoglycemia after antecedent hypoglycemia
B Fruehwald-Schultes, W Kern, D Dantz, J Born, HL Fehm, A Peters
Metabolism 2000
Gender-Related Differences in Counterregulatory Responses to Antecedent Hypoglycemia in Normal Humans1
SN Davis, C Shavers, F Costa
The Journal of clinical endocrinology and metabolism 2000
Diabetic hypoglycaemia
SR Heller
Best Practice & Research Clinical Endocrinology & Metabolism 1999
SYMPTOMS OF HYPOGLYCEMIA, THRESHOLDS FOR THEIR OCCURRENCE, AND HYPOGLYCEMIA UNAWARENESS
PE Cryer
Endocrinology & Metabolism Clinics of North America 1999
Hypoglycemiais the limiting factor in the management of diabetes
PE Cryer
Diabetes/Metabolism Research and Reviews 1999
Impaired Counterregulation of Glucose in a Patient with Hypothalamic Sarcoidosis
F Féry, L Plat, P de Borne, E Cogan, J Mockel
New England Journal of Medicine 1999
Protective effect of insulin against hypoglycemia-associated counterregulatory failure
B Fruehwald-Schultes, W Kern, E Deininger, P Wellhoener, W Kerner, J Born, HL Fehm, A Peters
The Journal of clinical endocrinology and metabolism 1999
Kompendium Diabetologie
PP Nawroth
1999
Counterregulatory Mechanisms to Insulin-Induced Hypoglycemia in Humans: Relevance to the Problem of Intensive Treatment of IDDM
GB Bolli
Journal of Pediatric Endocrinology and Metabolism 1998
Diabetes teaching program improves glycemic control and preserves perception of hypoglycemia
A Fritsche
Diabetes Research and Clinical Practice 1998
Decreased Epinephrine Responses to Hypoglycemia during Sleep
TW Jones, P Porter, RS Sherwin, EA Davis, P O'Leary, F Frazer, G Byrne, S Stick, WV Tamborlane
New England Journal of Medicine 1998
INTENSIVE TREATMENT OF TYPE 1 DIABETES
IB Hirsch
Medical Clinics of North America 1998
Prevention of an increase in plasma cortisol during hypoglycemia preserves subsequent counterregulatory responses
SN Davis, C Shavers, B Davis, F Costa
Journal of Clinical Investigation 1997
Basal serum pancreatic polypeptide is dependent on age and gender in an adult population
MB Damholt, BK Rasmussen, L Hilsted, R Jensen, J Hilsted
Scandinavian Journal of Clinical & Laboratory Investigation 1997
Strategies for maintaining good glycaemic control without recurrent hypoglycaemia
IA MacDonald
Proceedings of the Nutrition Society 1997
Urinary excretion of adrenaline and noradrenaline during hypoglycaemic clamp in diabetic and non-diabetic adolescents
M Bjørgaas, T Vik, G Sager, E Sagen, R Jorde
Scandinavian Journal of Clinical & Laboratory Investigation 1997
IMPLICATIONS AND RESULTS OF THE DIABETES CONTROL AND COMPLICATIONS TRIAL
WV Tamborlane, JA Ahern
Pediatric Clinics of North America 1997
Resistance to Neuroglycopenia: An Adaptative Response during Intensive Insulin Treatment of Diabetes1
TW Jones, WP Borg, MA Borg, SD Boulware, G McCarthy, D Silver, WV Tamborlane, RS Sherwin
The Journal of clinical endocrinology and metabolism 1997
Role of cortisol in the pathogenesis of deficient counterregulation after antecedent hypoglycemia in normal humans
SN Davis, C Shavers, F Costa, R Mosqueda-Garcia
Journal of Clinical Investigation 1996
Time course of the defective α-cell response to hypoglycemia in diabetic BB rats
RJ Jacob, J Dziura, JP Morgen, GI Shulman, RS Sherwin
Metabolism 1996
Prolactin and β-endorphin responses to hypoglycemia are reduced in well-controlled insulin-dependent diabetes mellitus
BT Kisley, CJ Levy, DC Simonson
Metabolism 1996
Long-term intensive insulin therapy in IDDM: effects on HbA1c, risk for severe and mild hypoglycaemia, status of counterregulation and awareness of hypoglycaemia
S Pampanelli, C Fanelli, C Lalli, M Ciofetta, PD Sindaco, M Lepore, F Modarelli, AM Rambotti, L Epifano, AD Vincenzo, L Bartocci, B Annibale, P Brunetti, GB Bolli
Diabetologia 1996
Impact of the Diabetes Control and Complications Trial (DCCT) on Management of Insulin-Dependent Diabetes Mellitus: A Pediatric Perspective
WV Tamborlane, N Attia, R Saif, N Sakati, AA Ashwal
Annals of Saudi medicine 1996
Glucagon secretory response to hypoglycaemia, adrenaline and carbachol in streptozotocindiabetic rats
B Ahrén, JS Stern, RL Gingerich, DL Curry, PJ Havel
Acta Physiologica Scandinavica 1995
Surgical removal of insulinoma restores glucose recovery from hypoglycaemia but does not normalize insulin action
SV de Kreutzenberg, A Riccio, M Dorella, A Avogaro, MC Marescotti, A Tiengo, SD Prato
European Journal of Clinical Investigation 1995
Diabetic autonomic neuropathy
V Spallone, L Uccioli, G Menzinger
Diabetes / Metabolism Reviews 1995
Reduced β-adrenergic sensitivity in healthy volunteers induced by hypoglycemia
TS Trovik, R Jaeger, R Jorde, G Sager
Fundamental & Clinical Pharmacology 1995
Brain Glucose Uptake and Unawareness of Hypoglycemia in Patients with Insulin-Dependent Diabetes Mellitus
PJ Boyle, SF Kempers, AM O'Connor, RJ Nagy
New England Journal of Medicine 1995
A Practical Guide to Intensive Insulin Therapy
PJ Campbell, ME May
The American Journal of the Medical Sciences 1995
Lack of preservation of higher brain function during hypoglycaemia in patients with intensively-treated IDDM
A Maran, J Lomas, IA Macdonald, SA Amiel
Diabetologia 1995
Cardiovascular response to exercise in diabetic patients: influence of autonomic neuropathy of different severity
P Bottini, C Tantucci, L Scionti, ML Dottorini, E Puxeddu, G Reboldi, GB Bolli, G Casucci, F Santeusanio, CA Sorbini, P Brunetti
Diabetologia 1995
Prolonged but partial impairment of the hypoglycaemic physiological response following short-term hypoglycaemia in normal subjects
E George, N Harris, C Bedford, IA Macdonald, CA Hardisty, SR Heller
Diabetologia 1995
Adaptation in brain glucose uptake following recurrent hypoglycemia
PJ Boyle, RJ Nagy, AM O'Connor, SF Kempers, RA Yeo, C Qualls
Proceedings of the National Academy of Sciences 1994
Exaggerated epinephrine response to hypoglycemia in a physically fit, well-controlled IDDM subject
SN Davis, RE Goldstein, AD Cherrington, L Price
Diabetes Research and Clinical Practice 1994
Advances in Pharmacology
B Drenger, Y Ginosar, Y Gozal
Advances in Pharmacology 1994
Long-term recovery from unawareness, deficient counterregulation and lack of cognitive dysfunction during hypoglycaemia, following institution of rational, intensive insulin therapy in IDDM
C Fanelli, S Pampanelli, L Epifano, AM Rambotti, AD Vincenzo, F Modarelli, M Ciofetta, M Lepore, B Annibale, E Torlone, G Perriello, PD Feo, F Santeusanio, P Brunetti, GB Bolli
Diabetologia 1994
Reversibility of Unawareness of Hypoglycemia in Patients with Insulinomas
A Mitrakou, C Fanelli, T Veneman, G Perriello, S Calderone, D Platanisiotis, A Rambotti, S Raptis, P Brunetti, P Cryer, J Gerich, G Bolli
New England Journal of Medicine 1993
Diabetic Neuropathy
AI Winegrad
New England Journal of Medicine 1972

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