Homeostatic joint amplification of pulsatile and 24-hour rhythmic cortisol secretion by fasting stress in midluteal phase women: Concurrent disruption of cortisol-growth hormone, cortisol-luteinizing hormone, and cortisol-leptin synchrony

M. Bergendahl, A. Iranmanesh, C. Pastor, W. S. Evans, J. D. Veldhuis

Research output: Contribution to journalArticle

12 Scopus citations

Abstract

Short-term fasting as a metabolic stress evokes prominent homeostatic reactions of the reproductive, corticotropic, thyrotropic, somatotropic, and leptinergic axes in men and women. Although reproductive adaptations to fasting are incompletely studied in the female, nutrient deprivation can have major neuroendocrine consequences in the follicular phase. Unexpectedly, a recent clinical study revealed relatively preserved sex steroid and gonadotropin secretion during short-term caloric restriction in the midluteal phase of the menstrual cycle. This observation suggested that female stress-adaptive responses might be muted in this sex steroid-replete milieu. To test this hypothesis, we investigated the impact of fasting on daily cortisol secretion in healthy young women during the midluteal phase of the normal menstrual cycle. Eight volunteers were each studied twice in separate and randomly ordered short-term (2.5-day) fasting and fed sessions. Pulsatile cortisol secretion, 24-h rhythmic cortisol release, and the orderliness of cortisol secretory patterns were quantified. Within-subject statistical comparisons revealed that fasting increased the mean serum cortisol concentration significantly from a baseline value of 8.0 ± 0.61 to 12.8 ± 0.85 μg/dL (P = 0.0003). (For Systeme International conversion to nanomoles per L, multiply micrograms per dL value by 28.) Pulsatile cortisol secretion rose commensurately, viz. from 101 ± 11 to 173 ± 16 μg/dL/day (P = 0.0025). Augmented 24-h cortisol production was due to amplification of cortisol secretory burst mass from 8.2 ± 1.5 to 12.9 ± 2.0 μg/dL (P = 0.017). In contrast, the estimated half-life of endogenous cortisol (104 ± 9 min), the calculated duration of underlying cortisol secretory bursts (16 ± 7 min) and their mean frequency (14 ± 2/day) were not altered by short-term fasting. The quantifiable orderliness of cortisol secretory patterns was also not influenced by caloric restriction. Nutrient deprivation elevated the mean of the 24-h serum cortisol concentration rhythm from 12.4 ± 1.3 to 18.4 ± 1.9 μg/dL (P = 0.0005), without affecting its diurnal amplitude or timing. Correlation analysis disclosed that fasting reversed the positive relationship between cortisol and LH release evident in the fed state, and abolished the negative association between cortisol and GH as well as between cortisol and leptin observed during nutrient repletion (P < 0.001). Pattern synchrony between cortisol and GH as well as that between cortisol and LH release was also significantly disrupted by fasting stress. In summary, short-term caloric deprivation enhances daily cortisol secretion by 1.7-fold in healthy midluteal phase young women by selectively amplifying cortisol secretory burst mass and elevating the 24-h rhythmic cortisol mean. Augmentation of daily cortisol production occurs without any concomitant changes in cortisol pulse frequency or half-life or any disruption of the timing of the 24-h rhythmicity or orderliness of cortisol release. Fasting degrades the physiological coupling between cortisol and LH, cortisol and GH, and cortisol and leptin secretion otherwise evident in calorie-sufficient women. We conclude that the corticotropic axis in the young adult female is not resistant to the stress-activating effects of short-term nutrient deprivation, but, rather, evinces strong adaptive homeostasis both monohormonally (cortisol) and bihormonally (cortisol paired with GH, LH, and leptin).

Original languageEnglish (US)
Pages (from-to)4028-4035
Number of pages8
JournalJournal of Clinical Endocrinology and Metabolism
Volume85
Issue number11
DOIs
StatePublished - Dec 1 2000

ASJC Scopus subject areas

  • Endocrinology, Diabetes and Metabolism
  • Biochemistry
  • Endocrinology
  • Clinical Biochemistry
  • Biochemistry, medical

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