Neuroendocrine responses to glucose ingestion in man. Specificity, temporal relationships, and quantitative aspects
Open accessAbstract
The mechanisms of postprandial glucose counterregulation-those that blunt late decrements in plasma glucose, prevent hypoglycemia, and restore euglycemia-have not been fully defined. To begin to clarify these mechanisms, we measured neuroendocrine and metabolic responses to the ingestion of glucose (75 g), xylose (62.5 g), mannitol (20 g), and water in ten normal human subjects to determine for each response the magnitude, temporal relationships, and specificity for glucose ingestion. Measurements were made at 10-min intervals over 5 h. By multivariate analysis of variance, the plasma glucose (P < 0.0001), insulin (P < 0.0001), glucagon (P < 0.03), epinephrine (P < 0.0004), and growth hormone (P < 0.01) curves, as well as the blood lactate (P < 0.0001), glycerol (P < 0.001), and beta-hydroxybutyrate (P < 0.0001) curves following glucose ingestion differed significantly from those following water ingestion. However, the growth hormone curves did not differ after correction for differences at base line. In contrast, the plasma norepinephrine (P < 0.31) and cortisol (P < 0.24) curves were similar after ingestion of all four test solutions, although early and sustained increments in norepinephrine occurred after all four test solutions. Thus, among the potentially important glucose regulatory factors, only transient increments in insulin, transient decrements in glucagon, and late increments in epinephrine are specific for glucose ingestion. They do not follow ingestion of water, xylose, or mannitol. Following glucose ingestion, plasma glucose rose to peak levels of 156+/-6 mg/dl at 46+/-4 min, returned to base line at 177+/-4 min, reached nadirs of 63+/-3 mg/dl at 232+/-12 min, and rose to levels comparable to base line at 305 min, which was the final sampling point. Plasma insulin rose to peak levels of 150+/-17 muU/ml (P < 0.001) at 67+/-8 min. At the time glucose returned to base line, insulin levels (49+/-12 muU/ml) remained fourfold higher than base line (P < 0.01); thereafter they declined but never fell below base line. Plasma glucagon decreased from 95+/-14 pg/ml to nadirs of 67+/-11 pg/ml (P < 0.001) at 84+/-9 min and then rose progressively to peak levels of 114+/-17 pg/ml (P < 0.001 vs. nadirs) at 265+/-12 min. Plasma epinephrine, which was 18+/-4 pg/ml at base line, did not change initially and then rose to peak levels of 119+/-20 pg/ml (P < 0.001) at 271+/-13 min. These data indicate that the glucose counterregulatory process late after glucose ingestion is not solely due to the dissipation of insulin and that sympathetic neural norepinephrine, growth hormone, and cortisol do not play critical roles. They are consistent with, but do not establish, physiologic roles for the counterregulatory hormones-glucagon, epinephrine, or both-in that process.
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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 [8]
The Introduction and Discussion support a role for counterregulatory factors after glucose ingestion, the postprandial setting addressed by this paper. But the Introduction says that the extent to which findings about hypoglycemic counterregulation can be extrapolated to nonhypoglycemic counterregulation is unknown. The paper therefore does not establish that the principles are fundamentally the same, and it does not study the postabsorptive state (section labels supplied without page numbers). (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe same principles apply to nonhypoglycemic glucose counterregulation.
“More recently it has been shown that the same principles apply to nonhypoglycemic glucose counterregulation”
From Epinephrine supports the postabsorptive plasma glucose concentration and prevents hypoglycemia when glucagon secretion is deficient in man (1984) · cites this paper as [8]
The Introduction (page unavailable) says that glucagon is primary and epinephrine compensates when glucagon is deficient in hypoglycemic counterregulation, but explicitly says it is unknown whether those findings extend to nonhypoglycemic counterregulation. The Discussion (page unavailable) finds hormone changes consistent with a counterregulatory role after glucose ingestion; it does not establish that the same principles apply. (LLM, conf=0.87)
Experimental — accuracy not yet measuredGlucose counterregulatory systems are involved in the prevention, as well as the correction, of hypoglycemia in humans.
“These findings provide further support for the concept, based upon physiological and clinical evidence (1–6), that glucose counterregulatory systems are involved in the prevention, as well as the correction, of hypoglycemia in humans.”
From Glycemic thresholds for activation of glucose counterregulatory systems are higher than the threshold for symptoms. (1987) · cites this paper as [3]
Cortisol secretion is unaltered.
“cortisol secretion is unaltered (1).”
The transition from exogenous glucose delivery to endogenous glucose production late after glucose ingestion is not solely attributable to dissipation of insulin and must also involve factors that actively raise plasma glucose concentration (glucose counterregulatory factors).
“Our study of the specificity, temporal relationships, and quantitative aspects of the neuroendocrine responses to glucose ingestion (1) indicates that this transition is not solely the result of the dissipation of insulin and, therefore, must also involve a factor or factors that actively raise the plasma glucose concentration— glucose counterregulatory factors.”
Resumption of glucagon secretion and late epinephrine secretion are both specific for glucose ingestion and temporally related to the counterregulatory process.
“resumption of glucagon secretion (after initial suppression) and late epinephrine secretion are both specific for glucose ingestion and temporally related to the counterregulatory process (1).”
Growth hormone secretion is temporally related but of marginal specificity.
“growth hormone secretion is temporally related but of marginal specificity (1)”
Sympathetic neural norepinephrine release is not specific for glucose ingestion and does not occur in temporal relation to the counterregulatory process.
“sympathetic neural norepinephrine release is not specific for glucose ingestion and does not occur in temporal relation to the counterregulatory process (1)”
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Self-citationAging delays the suppression of lipolysis and fatty acid oxidation in the postprandial period
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The Prevention and Correction of Hypoglycemia
Cryer, P. E. (2001) · Comprehensive physiology · doi:10.1002/j.2040-4603.2001.tb01481.x
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InfluentialSelf-citationGlucose counterregulation, hypoglycemia, and intensive insulin therapy in diabetes mellitus
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Self-citation
- Authors
- Tse, T. F., Clutter, W. E., Shah, S. D., Miller, J. P., & Cryer, P. E.
- Affiliations
- Washington University in St. Louis (US)
- ORCID
- Miller, J. Philip
- Venue
- Journal of Clinical Investigation
- Published
- 1983-07-01
- Volume
- 72
- Issue
- 1
- Pages
- 270-277
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC1129182
- OpenAlex
- W2022190611
- Cited by
- 68
- References
- 47
- Citations by year
- 2024: 1 · 2023: 1 · 2017: 1 · 2016: 1
- FWCI
- 7.84
- 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
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Keywords
- glucose ingestion, neuroendocrine response, insulin, glucagon, epinephrine, growth hormone, norepinephrine, cortisol, xylose, mannitol, blood lactate, beta-hydroxybutyrate, glycerol, hypoglycemia prevention, normoglycemia, plasma glucose, carbohydrate metabolism
- MeSH terms
- Adult, Blood Glucose, Epinephrine, Female, Glucagon, Glucose, Glycerol, Humans, Hydroxybutyrates, Insulin, Kinetics, Lactates, Male, Mannitol, Norepinephrine, Growth Hormone, Xylose, Lactic Acid, 3-Hydroxybutyric Acid
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