Role of Epinephrine-mediated β-Adrenergic Mechanisms in Hypoglycemic Glucose Counterregulation and Posthypoglycemic Hyperglycemia in Insulin-dependent Diabetes Mellitus
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Initially euglycemic (overnight insulin-infused) patients with insulin-dependent diabetes mellitus (IDDM), compared with nondiabetic controls, exhibit similar, but somewhat delayed plasma glucose nadirs, delayed glucose recovery from hypoglycemia, and posthypoglycemic hyperglycemia after the rapid intravenous injection of 0.075 U/kg of regular insulin. These abnormalities are associated with and potentially attributable to markedly diminished glucagon secretory responses, partially reduced epinephrine secretory responses and delayed clearance of injected insulin in the diabetic patients. Because glucagon normally plays a primary role in hypoglycemic glucose counterregulation and enhanced epinephrine secretion largely compensates for glucagon deficiency, we hypothesized that patients with IDDM, who exhibit diminished glucagon secretory responses to hypoglycemia, would be more dependent upon epinephrine to promote glucose recovery from hypoglycemia than are nondiabetic persons. To test this hypothesis, glucose counterregulation during beta-adrenergic blockade with propranolol was compared with that during saline infusion in both nondiabetic controls and in patients with IDDM. Glucose counterregulation was unaffected by beta-adrenergic blockade in controls. In contrast, glucose recovery from hypoglycemia was significantly impaired during beta-adrenergic blockade in diabetic patients. This finding confirms the hypothesis that such patients are more dependent upon epinephrine-mediated beta-adrenergic mechanisms to promote glucose recovery from hypoglycemia and indicates that the measured deficiency of glucagon secretion is functionally important in patients with IDDM. Further, in the time frame of these studies, posthypoglycemic hyperglycemia was prevented by beta-adrenergic blockade in these patients. There was considerable heterogeneity among the diabetic patients with respect to the degree to which beta-adrenergic blockade limited the posthypoglycemic rise in plasma glucose. This rise was directly related to the degree of residual glucagon secretion and inversely related to plasma-free insulin concentrations.THUS, WE CONCLUDE: (a) that patients with IDDM are, to varying degrees, dependent upon epinephrine-mediated beta-adrenergic mechanisms to promote glucose recovery from hypoglycemia and that the degree of this dependence upon epinephrine is an inverse function of the residual capacity to secrete glucagon in response to hypoglycemia in individual patients; (b) that sympathoadrenal activation, coupled with the inability to secrete insulin, plays an important role in the pathogenesis of posthypoglycemic hyperglycemia in patients with IDDM.
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Glucagon plays a primary counterregulatory role.
“Glucagon plays a primary counterregulatory role; epinephrine compensates largely for deficient glucagon secretion.”
From Epinephrine supports the postabsorptive plasma glucose concentration and prevents hypoglycemia when glucagon secretion is deficient in man (1984) · cites this paper as [6]
Epinephrine compensates largely for deficient glucagon secretion.
“Glucagon plays a primary counterregulatory role; epinephrine compensates largely for deficient glucagon secretion.”
From Epinephrine supports the postabsorptive plasma glucose concentration and prevents hypoglycemia when glucagon secretion is deficient in man (1984) · cites this paper as [6]
The principles of hypoglycemic glucose counterregulation and those of nonhypoglycemic glucose counterregulation in both the postprandial and postabsorptive states are fundamentally the same.
“Thus, the principles of hypoglycemic glucose counterregulation (1-7) and those of nonhypoglycemic glucose counterregulation in both the postprandial (8, 9) and the postabsorptive states are fundamentally the same.”
From Epinephrine supports the postabsorptive plasma glucose concentration and prevents hypoglycemia when glucagon secretion is deficient in man (1984) · cites this paper as [6]
Glucose recovery is not due solely to dissipation of insulin.
“Glucose recovery is not due solely to dissipation of insulin.”
From Epinephrine supports the postabsorptive plasma glucose concentration and prevents hypoglycemia when glucagon secretion is deficient in man (1984) · cites this paper as [6]
Glucose recovery fails to occur only in the absence of both glucagon and epinephrine.
“Glucose recovery fails to occur only in the absence of both glucagon and epinephrine.”
From Epinephrine supports the postabsorptive plasma glucose concentration and prevents hypoglycemia when glucagon secretion is deficient in man (1984) · cites this paper as [6]
In both hypoglycemic glucose counterregulation and another model of nonhypoglycemic glucose counterregulation, adrenomedullary epinephrine, but not sympathetic neural norepinephrine, compensates for deficient glucagon secretion.
“Second, in both hypoglycemic glucose counterregulation (1-7) and in another model of nonhypoglycemic glucose counterregulation (9), adrenomedullary epinephrine, but not sympathetic neural norepinephrine, compensates for deficient glucagon secretion.”
From Epinephrine supports the postabsorptive plasma glucose concentration and prevents hypoglycemia when glucagon secretion is deficient in man (1984) · cites this paper as [6]
Cites
Immunoassay of insulin with insulin-antibody precipitate
Hales, C. N., & Pj, R. (1963) · Biochemical Journal · doi:10.1042/bj0880137 · Cited by 2,640 · see citing works
Effect of Ischemia on Known Substrates and Cofactors of the Glycolytic Pathway in Brain
Lowry, O. H., Passonneau, J. V., Hasselberger, F. X., & Schulz, D. W. (1964) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)51740-3 · Cited by 2,222 · see citing works
Hormone-fuel interrelationships during fasting.
Cahill, G. F., Herrera, M. G., Morgan, A. P., Soeldner, J. S., Steinke, J., Levy, P. L., Reichard, G. A., & Kipnis, D. M. (1966) · Journal of Clinical Investigation · doi:10.1172/jci105481 · Cited by 1,036 · see citing works
Gerich, J. E., Langlois, M., Noacco, C., Karam, J. H., & Forsham, P. H. (1973) · Science · doi:10.1126/science.182.4108.171 · Cited by 688 · see citing works
A Sensitive Double Antibody Immunoassay for Human Growth Hormone in Plasma
Schalch, P., & PARKER, M. L. (1964) · Nature · doi:10.1038/2031141a0 · Cited by 635 · see citing works
Determination of Free and Total Insulin and C-Peptide in Insulin-treated Diabetics
Kuzuya, H., BLIX, P. M., Horwitz, D. L., Steiner, D. F., & Rubenstein, A. H. (1977) · Diabetes · doi:10.2337/diab.26.1.22 · Cited by 603 · see citing works
Role of Glucagon, Catecholamines, and Growth Hormone in Human Glucose Counterregulation
Rizza, R. A., Cryer, P. E., & Gerich, J. E. (1979) · Journal of Clinical Investigation · doi:10.1172/jci109464 · Cited by 421 · see citing works
Self-citationAdrenergic Mechanisms for the Effects of Epinephrine on Glucose Production and Clearance in Man
Rizza, R. A., Cryer, P. E., Haymond, M. W., & Gerich, J. E. (1980) · Journal of Clinical Investigation · doi:10.1172/jci109714 · Cited by 340 · see citing works
Self-citationGlucose Counterregulation in Man
Cryer, P. E. (1981) · Diabetes · doi:10.2337/diab.30.3.261 · Cited by 270 · see citing works
Self-citationAdrenergic receptor control mechanism for growth hormone secretion
Blackard, W. G., & Heidingsfelder, S. A. (1968) · Journal of Clinical Investigation · doi:10.1172/jci105832 · Cited by 259 · see citing works
Lager, I., Blohmé, G., & Smith, U. (1979) · The Lancet · doi:10.1016/s0140-6736(79)90821-3 · Cited by 194 · see citing works
Hormonal mechanisms of recovery from insulin-induced hypoglycemia in man.
Gerich, J., Davis, J., Lorenzi, M., Rizza, R., Bohannon, N., Karam, J., Lewis, S., Kaplan, R., Schultz, T., & Cryer, P. (1979) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1979.236.4.e380 · Cited by 183 · see citing works
Self-citationPlasma Cortisol Determination: Radioimmunoassay and Competitive Protein Binding Compared
Farmer, R. W., & Pierce, C. E. (1974) · Clinical Chemistry · doi:10.1093/clinchem/20.4.411 · Cited by 170 · see citing works
Plasma catecholamines in diabetes
Cryer, P. E., Silverberg, A. B., Santiago, J. V., & SHAH, S. D. (1978) · The American Journal of Medicine · doi:10.1016/0002-9343(78)90220-6 · Cited by 169 · see citing works
Self-citationSANTIAGO, J. V., CLARKE, W. L., SHAH, S. D., & CRYER, P. E. (1980) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-51-4-877 · Cited by 166 · see citing works
Self-citationCRYER, P. E., SANTIAGO, J. V., & SHAH, S. (1974) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-39-6-1025 · Cited by 155 · see citing works
Self-citationCryer, P. E., Rizza, R. A., Haymond, M. W., & Gerich, J. E. (1980) · Metabolism · doi:10.1016/0026-0495(80)90019-0 · Cited by 115 · see citing works
Self-citationHormonal, Metabolic, and Cardiovascular Responses to Hypoglycemia in Diabetic Autonomic Neuropathy
Hilsted, J., Madsbad, S., Krarup, T., Sestoft, L., Christensen, N. J., Tronier, B., & Galbo, H. (1981) · Diabetes · doi:10.2337/diab.30.8.626 · Cited by 104 · see citing works
Glucagon and Catecholamine Secretion During Hypoglycemia in Normal and Diabetic Man
Benson, J. W., Johnson, D. G., Palmer, J. P., Werner, P. L., & Ensinck, J. W. (1977) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-44-3-459 · Cited by 82 · see citing works
Uncontrolled diabetes mellitus and hyperglucagonemia associated with an islet cell carcinoma
Leichter, S. B., Pagliara, A. S., Greider, M. H., Pohl, S. L., Rosaí, J., & KIPNIS, D. M. (1975) · The American Journal of Medicine · doi:10.1016/0002-9343(75)90579-3 · Cited by 74 · see citing works
Adrenergic mechanisms in recovery from hypoglycemia in man: adrenergic blockade.
Clarke, W. L., Santiago, J. V., Thomas, L., Ben-Galim, E., Haymond, M. W., & Cryer, P. E. (1979) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1979.236.2.e147 · Cited by 73 · see citing works
Self-citationLack of Glucagon Response to Hypoglycemia in Diabetic Autonomic Neuropathy
Maker, T. D., Tanenberg, R. J., Greenberg, B. Z., Hoffman, J. E., DOE, R. P., & Goetz, F. C. (1977) · Diabetes · doi:10.2337/diab.26.3.196 · Cited by 72 · see citing works
Cholinergic Stimulation of Norepinephrine Release in Man
Leveston, S. A., SHAH, S. D., & Cryer, P. E. (1979) · Journal of Clinical Investigation · doi:10.1172/jci109471 · Cited by 50 · see citing works
Self-citationDefective blood glucose counter-regulation in diabetics is a selective form of autonomic neuropathy.
Campbell, L. V., Kraegen, E. W., & Lazarus, L. (1977) · BMJ · doi:10.1136/bmj.2.6101.1527 · Cited by 41 · see citing works
Viberti, G. C., KEEN, H., & Bloom, S. R. (1980) · Metabolism · doi:10.1016/0026-0495(80)90126-2 · Cited by 29 · see citing works
Viberti, G. C., KEEN, H., & Bloom, S. R. (1980) · Metabolism · doi:10.1016/0026-0495(80)90127-4 · Cited by 22 · see citing works
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Sorted by citations
Dagogo-Jack, S. E., Craft, S., & Cryer, P. E. (1993) · Journal of Clinical Investigation · doi:10.1172/jci116302 · Cited by 471 · see citing works
Self-citationAbnormal angiogenesis in diabetes mellitus
Martin, A., Komada, M. R., & Sane, D. C. (2002) · Medicinal Research Reviews · doi:10.1002/med.10024 · Cited by 465 · see citing works
White, N. H., Skor, D. A., Cryer, P. E., Levandoski, L. A., Bier, D. M., & Santiago, J. V. (1983) · New England Journal of Medicine · doi:10.1056/nejm198303033080903 · Cited by 391 · see citing works
Self-citationGlucose counterregulation, hypoglycemia, and intensive insulin therapy in diabetes mellitus
Epstein, F. H., Cryer, P. E., & Gerich, J. E. (1985) · New England Journal of Medicine · doi:10.1056/nejm198507253130405 · Cited by 273 · see citing works
Self-citationSimonson, D. C., Tamborlane, W. V., DeFRONZO, R. A., & SHERWIN, R. S. (1985) · Annals of Internal Medicine · doi:10.7326/0003-4819-103-2-184 · Cited by 173 · see citing works
Abnormal Glucose Counterregulation after Subcutaneous Insulin in Insulin-Dependent Diabetes Mellitus
Bolli, G. B., Dimitriadis, G., Pehling, G. B., Baker, B. A., Haymond, M. W., Cryer, P. E., & Gerich, J. E. (1984) · New England Journal of Medicine · doi:10.1056/nejm198406283102605 · Cited by 164 · see citing works
Self-citationBolli, G. B., Tsalikian, E., Haymond, M. W., Cryer, P. E., & Gerich, J. E. (1984) · Journal of Clinical Investigation · doi:10.1172/jci111359 · Cited by 108 · see citing works
Self-citationWhy should people with type 1 diabetes exercise regularly?
Codella, R., Terruzzi, I. M., & Luzi, L. (2017) · Acta Diabetologica · doi:10.1007/s00592-017-0978-x · Cited by 103 · see citing works
Insulin and glucagon in prevention of hypoglycemia during exercise in humans.
Hirsch, I. B., Marker, J. C., Smith, L., Spina, R., Parvin, C., Holloszy, J., & Cryer, P. (1991) · American Journal of Physiology · doi:10.1152/ajpendo.1991.260.5.e695 · Cited by 104 · see citing works
Self-citationNocturnal Blood Glucose Control in Type I Diabetes Mellitus
Bolli, G. B., Perriello, G., Fanelli, C. G., & Feo, P. D. (1993) · Diabetes Care · doi:10.2337/diacare.16.3.71 · Cited by 86 · see citing works
Bolli, G. B., Gottesman, I. S., Campbell, P. J., Haymond, M. W., Cryer, P. E., & Gerich, J. E. (1984) · New England Journal of Medicine · doi:10.1056/nejm198411083111904 · Cited by 84 · see citing works
Self-citationRegulation of glucose metabolism by sympathochromaffin catecholamines
Clutter, W. E., Rizza, R. A., Gerich, J. E., & Cryer, P. E. (1988) · Diabetes/Metabolism Reviews · doi:10.1002/dmr.5610040104 · Cited by 80 · see citing works
Self-citationVariable Deterioration in Cortical Function During Insulin-induced Hypoglycemia
Herold, K. C., Polonsky, K. S., Cohen, R. M., Levy, J., & Douglas, F. L. (1985) · Diabetes · doi:10.2337/diab.34.7.677 · Cited by 78 · see citing works
Role of hepatic autoregulation in defense against hypoglycemia in humans.
Bolli, G. B., Feo, P. D., Perriello, G., Cosmo, S. D., Ventura, M. M., Campbell, P., Brunetti, P., & Gerich, J. E. (1985) · Journal of Clinical Investigation · doi:10.1172/jci111869 · Cited by 77 · see citing works
Powell, A. M., Sherwin, R. S., & Shulman, G. I. (1993) · Journal of Clinical Investigation · doi:10.1172/jci116883 · Cited by 73 · see citing works
Burge, M. R. (1998) · JAMA · doi:10.1001/jama.279.2.137 · Cited by 71 · see citing works
Tse, T. F., Clutter, W. E., Shah, S. D., Miller, J. P., & Cryer, P. E. (1983) · Journal of Clinical Investigation · doi:10.1172/jci110966 · Cited by 68 · see citing works
Self-citationMeyer, C., Hering, B. J., Gromann, R., Brandhorst, H., Brandhorst, D., Gerich, J., Federlin, K., & Bretzel, R. G. (1998) · Transplantation · doi:10.1097/00007890-199807270-00017 · Cited by 66 · see citing works
Hirst, J. A., Farmer, A. A., Feakins, B. G., Aronson, J. K., & Stevens, R. (2014) · British Journal of Clinical Pharmacology · doi:10.1111/bcp.12543 · Cited by 64 · see citing works
Overview of counterregulation and its abnormalities in diabetes mellitus and other conditions
Gerich, J. E., & Campbell, P. J. (1988) · Diabetes/Metabolism Reviews · doi:10.1002/dmr.5610040202 · Cited by 64 · see citing works
Lager, I., Attvall, S., Blohmé, G., & Smith, U. (1986) · Diabetic Medicine · doi:10.1111/j.1464-5491.1986.tb00772.x · Cited by 64 · see citing works
Relation of Counterregulatory Responses to Hypoglycemia in Type I Diabetics
Polonsky, K. S., Bergenstal, R. M., Pons, G. M., Schneider, M., Jaspan, J. B., & Rubenstein, A. H. (1982) · New England Journal of Medicine · doi:10.1056/nejm198210283071802 · Cited by 64 · see citing works
The human sympathochromaffin system
Shah, S. D., Tse, T. F., Clutter, W. E., & Cryer, P. E. (1984) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1984.247.3.e380 · Cited by 64 · see citing works
Self-citationThe physiology and pathophysiology of the neural control of the counterregulatory response
Beall, C., Ashford, M. L., & McCrimmon, R. J. (2012) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00531.2011 · Cited by 63 · see citing works
Hoelzer, D. R., Dalsky, G. P., Clutter, W. E., SHAH, S. D., Holloszy, J. O., & Cryer, P. E. (1986) · Journal of Clinical Investigation · doi:10.1172/jci112279 · Cited by 61 · see citing works
Self-citationRetractedCatecholamines in prevention of hypoglycemia during exercise in humans
Marker, J. C., Hirsch, I. B., Smith, L. J., Parvin, C. A., Holloszy, J. O., & Cryer, P. E. (1991) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1991.260.5.e705 · Cited by 60 · see citing works
Self-citationKeller, U., Schnell, H., Girard, J., & Stauffacher, W. (1984) · Diabetologia · doi:10.1007/bf00281115 · Cited by 55 · see citing works
Hypoglycemia induced by excessive rebound secretion of insulin after removal of pheochromocytoma
Akiba, M., Kodama, T., Ito, Y., Obara, T., & Fujimoto, Y. (1990) · World Journal of Surgery · doi:10.1007/bf01658514 · Cited by 55 · see citing works
Liver Fat Content and Hepatic Insulin Sensitivity in Overweight Patients With Type 1 Diabetes
Llauradó, G., Sevastianova, K., Sädevirta, S., Hakkarainen, A., Lundbom, N. M. I., Orho‐Melander, M., Groop, P., Forsblom, C. M., & Yki‐Järvinen, H. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-3050 · Cited by 55 · see citing works
Glucose counterregulation during prolonged hypoglycemia in normal humans
Bolli, G. B., Gottesman, I. S., Cryer, P. E., & Gerich, J. E. (1984) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1984.247.2.e206 · Cited by 52 · see citing works
Self-citationMechanisms of Insulin Resistance After Insulin-Induced Hypoglycemia in Humans: The Role of Lipolysis
Lucidi, P., Rossetti, P., Porcellati, F., Pampanelli, S., Candeloro, P., Andreoli, A. M., Perriello, G., Bolli, G. B., & Fanelli, C. G. (2010) · Diabetes · doi:10.2337/db09-0745 · Cited by 47 · see citing works
Diabetes education in pediatrics: How to survive diabetes
Ergun-Longmire, B., Clemente, E. G., Maravolo, P. V., Roberts, C., Buth, K., & Greydanus, D. E. (2021) · Disease-a-Month · doi:10.1016/j.disamonth.2021.101153 · Cited by 46 · see citing works
Heller, S. R., Macdonald, I. A., & Tattersall, R. B. (1987) · Diabetologia · doi:10.1007/bf00295875 · Cited by 43 · see citing works
CRYER, P. E., WHITE, N. H., & SANTIAGO, J. V. (1986) · Endocrine Reviews · doi:10.1210/edrv-7-2-131 · Cited by 43 · see citing works
Self-citationPrevention and Correction of Hypoglycemia
Cryer, P. E. (2003) · Humana Press eBooks · doi:10.1007/978-1-59259-310-1_7 · Cited by 42 · see citing works
Self-citationIs There a Role for Beta‐blockers in Hypertensive Diabetic Patients?
Tse, W. Y., & Kendall, M. J. (1994) · Diabetic Medicine · doi:10.1111/j.1464-5491.1994.tb02009.x · Cited by 42 · see citing works
Rosen, S. G., Clutter, W. E., Berk, M. A., Shah, S. D., & Cryer, P. E. (1984) · Journal of Clinical Investigation · doi:10.1172/jci111226 · Cited by 41 · see citing works
Self-citationCryer, P. E., Tse, T. F., Clutter, W. E., & SHAH, S. D. (1984) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1984.247.2.e198 · Cited by 39 · see citing works
Self-citationEarly posthypoglycemic insulin resistance in man is mainly an effect of beta-adrenergic stimulation.
Attvall, S., Eriksson, B. M., Fowelin, J., von Schenck, H., Lager, I., & Smith, U. (1987) · Journal of Clinical Investigation · doi:10.1172/jci113091 · Cited by 39 · see citing works
Tordjman, K. M., Havlin, C. E., Levandoski, L. A., White, N. H., Santiago, J. V., & Cryer, P. E. (1987) · New England Journal of Medicine · doi:10.1056/nejm198712173172502 · Cited by 38 · see citing works
Self-citationCatecholamine responses and their interactions with other glucoregulatory hormones
Vranić, M., Gauthier, C., Bilinski, D., Wasserman, D. H., El-Tayeb, K. M. A., Hetenyi, G., Jr., & Lickley, H. L. A. (1984) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1984.247.2.e145 · Cited by 37 · see citing works
The Effect of Asymptomatic Nocturnal Hypoglycemia on Glycemic Control in Diabetes Mellitus
Perriello, G., Feo, P. D., Torlone, E., Calcinaro, F., Ventura, M. M., Basta, G., Santeusanio, F., Brunetti, P., Gerich, J. E., & Bolli, G. B. (1988) · New England Journal of Medicine · doi:10.1056/nejm198811103191901 · Cited by 36 · see citing works
Raskin, P. (1984) · Archives of Internal Medicine · doi:10.1001/archinte.144.4.781 · Cited by 35 · see citing works
Powell, A. M., & Sherwin, R. S. (1993) · Cited by 34 · see citing works
Adamson, U., LINS, P.-E. S., Efendić, S., Hamberger, B., & Wajngot, A. (1984) · Acta Medica Scandinavica · doi:10.1111/j.0954-6820.1984.tb03795.x · Cited by 33 · see citing works
BERLIN, I., GRIMALDI, A., LANDAULT, C., ZOGHBI, F., THERVET, F., PUECH, A. J., & LEGRAND, J. C. (1988) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-66-2-273 · Cited by 32 · see citing works
Glucose counterregulation in diabetes secondary to chronic pancreatitis
Larsen, S., Hilsted, J., Philipsen, E., Tronier, B., Christensen, N. J., Nielsen, M. D., & WORNING, H. (1990) · Metabolism · doi:10.1016/0026-0495(90)90066-l · Cited by 32 · see citing works
Excessive Insulin Therapy: Biochemical Effects and Clinical Repercussions
Wilson, D. E. (1983) · Annals of Internal Medicine · doi:10.7326/0003-4819-98-2-219 · Cited by 32 · see citing works
CLAUSEN‐SJÖBOM, N., LINS, P.-E. S., Adamson, U., Curstedt, T., & Hamberger, B. (1987) · Acta Medica Scandinavica · doi:10.1111/j.0954-6820.1987.tb09929.x · Cited by 31 · see citing works
Regulation of Carbohydrate Metabolism and Response to Hypoglycemia
Butler, P. C., & Rizza, R. A. (1989) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/s0889-8529(18)30386-4 · Cited by 27 · see citing works
Adrenal catecholamine metabolism and myocardial adrenergic receptors in streptozotocin diabetic rats
Bitar, M. S., Koulu, M., Rapoport, S. I., & Linnoila, M. (1987) · Biochemical Pharmacology · doi:10.1016/0006-2952(87)90407-2 · Cited by 27 · see citing works
Defective glucose counterregulation limits intensive therapy of diabetes mellitus
Santiago, J. V., White, N. H., Skor, D. A., Levandoski, L. A., Bier, D. M., & Cryer, P. E. (1984) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1984.247.2.e215 · Cited by 24 · see citing works
Self-citationThe Prevention and Correction of Hypoglycemia
Cryer, P. E. (2001) · Comprehensive Physiology · doi:10.1002/cphy.cp070235 · Cited by 23 · see citing works
Self-citationInsulin in the Somogyi Phenomenon
Wallaert, B., Aerts, C., Bonniere, P., Cortot, A., Tonnel, A., Paris, J., & Voisin, C. (1985) · New England Journal of Medicine · doi:10.1056/nejm198502143120715 · Cited by 23 · see citing works
Diagnosis and treatment of ‘insulinoma’
Fajans, S. S., & Vinik, A. I. (1984) · Cancer treatment and research · doi:10.1007/978-1-4613-2849-0_11 · Cited by 22 · see citing works
Attvall, S., Fowelin, J., von Schenck, H., Lager, I., & Smith, U. (1987) · Diabetologia · doi:10.1007/bf00296990 · Cited by 22 · see citing works
Effects of Antihypertensive Drugs on Endocrine Function
Brass, E. P. (1984) · Drugs · doi:10.2165/00003495-198427050-00004 · Cited by 19 · see citing works
Pathophysiology and management of hypoglycemia in diabetes
RANGEL, E. S., Deajon-Jackson, J. D., & Hwang, J. J. (2022) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.14904 · Cited by 18 · see citing works
Duration of type I diabetes affects glucagon and glucose responses to insulin-induced hypoglycemia.
(1984) · PubMed Central · Cited by 17 · see citing works
Hypoglycemia and embryonic heart development
Smoak, I. W. (2002) · Frontiers in bioscience · doi:10.2741/a776 · Cited by 17 · see citing works
Glucagon Responses to Hypoglycemia in Children and Adolescents With IDDM
Singer-Granick, C. J., Hoffman, R. P., Kerensky, K. M., DRASH, A. L., & Becker, D. J. (1988) · Diabetes Care · doi:10.2337/diacare.11.8.643 · Cited by 17 · see citing works
Shamoon, H., & Sherwin, R. S. (1984) · Diabetologia · doi:10.1007/bf00252404 · Cited by 16 · see citing works
Hypoglycemic glucose counterregulation in patients with insulin-dependent diabetes mellitus.
Cryer, P. E. (1982) · PubMed · Cited by 16 · see citing works
Self-citationProlonged insulin resistance following insulin-induced hypoglycaemia
Clore, J. N., Brennan, J. R., Gebhart, S. S. P., Newsome, H. H., Nestler, J. E., & Blackard, W. G. (1987) · Diabetologia · doi:10.1007/bf00274793 · Cited by 15 · see citing works
β-Adrenoceptor regulation in insulin-dependent diabetes mellitus
Sager, G., Slørdal, L., Huseby, N. E., & Florholmen, J. R. (1991) · Scandinavian Journal of Clinical and Laboratory Investigation · doi:10.3109/00365519109091616 · Cited by 15 · see citing works
Adrenergic blockade and hypoglycaemia
Lager, I. (1983) · Acta Medica Scandinavica · doi:10.1111/j.0954-6820.1983.tb01615.x · Cited by 13 · see citing works
Somogyi and dawn phenomena: Mechanisms
Feo, P. D., Perriello, G., & Bolli, G. B. (1988) · Diabetes/Metabolism Reviews · doi:10.1002/dmr.5610040106 · Cited by 13 · see citing works
Potential approaches to prevent hypoglycemia-associated autonomic failure
Lontchi-Yimagou, E., You, J. Y., Carey, M., Gabriely, I., Shamoon, H., & Hawkins, M. (2018) · Journal of Investigative Medicine · doi:10.1136/jim-2017-000582 · Cited by 12 · see citing works
Dual‐hormone treatment with insulin and glucagon in patients with type 1 diabetes
Reiband, H. K., Schmidt, S., Ranjan, A. G., Holst, J. J., Madsbad, S., & Nørgaard, K. (2014) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.2632 · Cited by 12 · see citing works
Glucose counterregulation during recovery from neuroglucopenia: Which mechanism is important?
Asplin, C. M., Raghu, P., Koerker, D. J., & Palmer, J. P. (1985) · Metabolism · doi:10.1016/0026-0495(85)90053-8 · Cited by 12 · see citing works
A biphasic serum glucose response in mice to inoculation with pertussis vaccine
Kreeftenberg, J. G., de Kappelle, I. V. S.-V., Wildt, D. J. D., Terlingen, J. B. A., Peters, P. W. J., & Walvoort, H. C. (1984) · Journal of Biological Standardization · doi:10.1016/s0092-1157(84)80048-7 · Cited by 12 · see citing works
Kollind, M., Adamson, U., LINS, P.-E. S., & Curstedt, T. (1988) · Acta Medica Scandinavica · doi:10.1111/j.0954-6820.1988.tb15781.x · Cited by 11 · see citing works
Ohara, K., Katayama, M., & Nagai, K. (2018) · Neuroscience Letters · doi:10.1016/j.neulet.2018.06.057 · Cited by 10 · see citing works
Hypoglycemia: a pitfall of insulin therapy.
(1983) · PubMed Central · Cited by 9 · see citing works
Jiang, H., Niu, J.-J., Zhang, W., Huang, W., Zhou, M.-Y., Sha, W., Li, J., Li, F., Zhu, T., Xia, X., et al. (2014) · Journal of Chinese Integrative Medicine · doi:10.1016/s2095-4964(14)60008-x · Cited by 8 · see citing works
Impaired glucose disposal following mild hypoglycemia in nondiabetic and type I diabetic humans
DAVIS, M. R., & Shamoon, H. (1992) · Metabolism · doi:10.1016/0026-0495(92)90156-5 · Cited by 8 · see citing works
Cryer, P. E. (1983) · Advances in metabolic disorders · doi:10.1016/b978-0-12-027310-2.50025-6 · Cited by 8 · see citing works
Self-citationLager, I., von Schenck, H., & Smith, U. (1984) · Diabetologia · doi:10.1007/bf00266033 · Cited by 8 · see citing works
Pathophysiology of sympathoadrenal system
GIORGINO, R. (1988) · Journal of Endocrinological Investigation · doi:10.1007/bf03350236 · Cited by 7 · see citing works
Cersósimo, E., Zaitseva, I. N., & Ajmal, M. (1998) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1998.275.5.e792 · Cited by 7 · see citing works
Increased lipid oxidation but normal muscle glycogen response to epinephrine in humans with IDDM
Cohen, N., Halberstam, M., Rossetti, L., & Shamoon, H. (1996) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1996.271.2.e284 · Cited by 7 · see citing works
Kollind, M., Adamson, U., Lins, P. E., & Hamberger, B. (1988) · Diabetologia · doi:10.1007/bf00264767 · Cited by 7 · see citing works
Physiological insulin action is opposed by beta-adrenergic mechanisms in dogs
Werther, G. A., Joffe, S. N., Artal, R., & Sperling, M. A. (1988) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1988.255.1.e33 · Cited by 7 · see citing works
Pereira, L. R. L., Foss‐Freitas, M. C., Peres, H. A., & Martínez, E. Z. (2015) · Journal of Bioanalysis & Biomedicine · doi:10.4172/1948-593x.1000186 · Cited by 5 · see citing works
Recurrent hypoglycaemia in a toddler on β-blocker therapy
Pépin, V., Gagné, N., & Rottembourg, D. (2018) · Cardiology in the Young · doi:10.1017/s1047951117002724 · Cited by 5 · see citing works
Hypoglycaemia: glucose counterregulation, cardiovascular responses and immunoregulation
Cryer, P. E. (1983) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.1983.tb00055.x · Cited by 5 · see citing works
Self-citationMatsumura, S., Eguchi, A., Kitabayashi, N., Tanida, M., Shen, J., Horii, Y., Nagai, K., Tsuzuki, S., Inoue, K., & Fushiki, T. (2010) · Neuroscience Research · doi:10.1016/j.neures.2010.03.010 · Cited by 4 · see citing works
Glucagon as a Counterregulatory Hormone
Gerich, J. E. (1983) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-69019-8_15 · Cited by 4 · see citing works
The Sympathochromaffin System and the Pituitary-Adrenocortical Response to Hypoglycemia
Cryer, P. E. (1986) · Science · doi:10.1126/science.3001939 · Cited by 4 · see citing works
Self-citationVaughan, N. J. A., Rao, R. H., Kurtz, A. B., Buckell, H. M., & Spathis, G. S. (1986) · Metabolism · doi:10.1016/0026-0495(86)90114-9 · Cited by 4 · see citing works
Glucose counterregulation in normal and diabetic man
Cryer, P. E. (1985) · Clinical Physiology · doi:10.1111/j.1365-2281.1985.tb00012.x · Cited by 4 · see citing works
Self-citationSympathetic nervous system and metabolism
Carlson, G., & Little, R. (1999) · Springer eBooks · doi:10.1007/978-88-470-2901-9_6 · Cited by 3 · see citing works
EFFECT OF SODIUM SALICYLATE ON HORMONAL RESPONSES TO HYPOGLYCAEMIA IN TYPE II DIABETICS
Brass, E. P., Halter, J. B., Ensinck, J. W., & Robertson, R. P. (1984) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1984.tb01407.x · Cited by 3 · see citing works
(2015) · Elsevier eBooks · doi:10.1016/b978-0-444-53717-1.00376-0 · Cited by 3 · see citing works
Contrainsulin Hormones: Biochemical and Physiological Aspects
Gerich, J. E., & Cryer, P. E. (1991) · Springer eBooks · doi:10.1007/978-1-4684-0400-5_6 · Cited by 3 · see citing works
Self-citationMedical perspectives on pediatric sports medicine–Selective topics
Cabral, M. D., Patel, D. R., Greydanus, D. E., Deleon, J., Hudson, E., & Darweesh, S. (2022) · Disease-a-Month · doi:10.1016/j.disamonth.2022.101327 · Cited by 2 · see citing works
Counterregulatory Deficiencies in Diabetes
McCrimmon, R. J. (2013) · Wiley eBooks · doi:10.1002/9781118695432.ch3 · Cited by 2 · see citing works
Modulation of catecholamine effects during hypoglycaemia in man by urapidil and propranolol
Petersen, K. ‐., Katschker, P., & Kerp, L. (1989) · European Journal of Clinical Pharmacology · doi:10.1007/bf00558294 · Cited by 2 · see citing works
Hypoglycemia in the Critically Ill Patient
Liggett, S. B., & Cryer, P. E. (1986) · Journal of Intensive Care Medicine · doi:10.1177/088506668600100305 · Cited by 1 · see citing works
Self-citationLack of β2-adrenoceptor induced long-acting effect on glucose tolerance in type 2 diabetic patients
Petersen, K.-G., Khalaf, A.-N., & Kerp, L. (1991) · Diabetes Research and Clinical Practice · doi:10.1016/0168-8227(91)90029-d · Cited by 1 · see citing works
- Authors
- Popp, D. A., Shah, S. D., & Cryer, P. E.
- Affiliations
- Washington University in St. Louis (US)
- Venue
- Journal of Clinical Investigation
- Published
- 1982-02-01
- Volume
- 69
- Issue
- 2
- Pages
- 315-326
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC370981
- OpenAlex
- W2039193863
- Cited by
- 112
- References
- 26
- Citations by year
- 2025: 1 · 2024: 1 · 2022: 2 · 2021: 1 · 2018: 2 · 2017: 2 · 2015: 2 · 2014: 4 · 2013: 1 · 2012: 1
- FWCI
- 15.45
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Management and Research
- Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Treatment and Management
- Keywords
- type 1 diabetes, hypoglycemic counterregulation, epinephrine, beta-adrenergic blockade, propranolol, glucagon secretion, insulin-induced hypoglycemia, insulin clearance
- MeSH terms
- Adrenergic beta-Agonists, Adult, Blood Glucose, Blood Pressure, Diabetes Mellitus, Epinephrine, Female, Glucagon, Heart Rate, Humans, Hydrocortisone, Hyperglycemia, Hypoglycemia, Insulin, Male, Norepinephrine
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