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 Table of Contents  
ORIGINAL ARTICLE
Year : 2016  |  Volume : 29  |  Issue : 4  |  Page : 936-943

Effect of sleep deprivation on vascular reactivity in male rats


1 Physiology Department, Faculty of Medicine, Al-Azhar University, Cairo, Egypt
2 Clinical Physiology Department, Faculty of Medicine, Menoufia University, Cairo, Egypt

Date of Submission11-Feb-2015
Date of Acceptance10-Apr-2015
Date of Web Publication21-Mar-2017

Correspondence Address:
Ahmad M Gaafar
Clinical Physiology Department, Faculty of Medicine, Menoufia University, Shibin Elkom, 32511
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1110-2098.202530

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  Abstract 

Objective
The aim of this study was to evaluate the effect of sleep deprivation on vascular reactivity in adult male albino rats.
Background
Sleep deprivation can be due to either insufficient duration of sleep or a fragmented sleep period or a combination of both factors.
Materials and methods
This study was conducted on 140 adult male rats. Rats were divided into four groups: group 1, the control group; group 2, the sleep-deprived group; group 3, the 24-h sleep recovery group; and group 4, the 48-h sleep recovery group. Arterial blood pressure was measured. Vascular reactivity to noradrenaline, indomethacin, vasopressin, ACh, and sodium nitroprusside and the levels of serum adrenaline, noradrenaline, adrenocorticotropic hormone, cortisone, and C-reactive protein (CRP) were studied.
Results
Induction of sleep deprivation was associated with a significant increase in arterial blood pressures and vascular reactivity to noradrenaline, vasopressin, and indomethacin. The percentage of vasodilation to ACh significantly decreased. Serum levels of adrenaline, noradrenaline, ACTH, cortisone, and CRP significantly increased. In the 24-h recovery group, arterial blood pressures significantly elevated. Vascular reactivity to noradrenaline, vasopressin, and indomethacin were still significantly high. CRP was also still significantly elevated, whereas adrenaline and noradrenaline returned to control levels. In the 48-h recovery group, blood pressure, vascular reactivity, CRP, adrenaline, and noradrenaline returned to control levels.
Conclusion
Twenty-four-hour recovery period was not sufficient to restore normal vascular reactivity, whereas 48-h recovery period was essential to restore normal vascular reactivity after acute total sleep deprivation.

Keywords: sleep deprivation, sleep disorder, vascular reactivity


How to cite this article:
Abdel-Latif MA, Hazzaa SM, Naguib YM, Gaafar AM. Effect of sleep deprivation on vascular reactivity in male rats. Menoufia Med J 2016;29:936-43

How to cite this URL:
Abdel-Latif MA, Hazzaa SM, Naguib YM, Gaafar AM. Effect of sleep deprivation on vascular reactivity in male rats. Menoufia Med J [serial online] 2016 [cited 2020 Feb 16];29:936-43. Available from: http://www.mmj.eg.net/text.asp?2016/29/4/936/202530


  Introduction Top


Sleep is a regular, recurrent, easily reversible state that is characterized by relative quiescence and a great increase in the threshold of response to external stimuli relative to the waking state [1].

The international classification of sleep disorders includes a specific disorder of voluntary but unintentional sleep deprivation called 'insufficient sleep syndrome' that occurs in an individual who persistently fails to obtain sufficient nocturnal sleep required to support normally alert wakefulness. Criteria for the diagnosis have been established on the basis of data obtained from polysomnography (nocturnal sleep studies) and the multiple sleep latency test, which attempt to objectively quantify the degree of daytime sleepiness [2].

Although the specific functions of sleep remain a topic of scientific debate, there are significant behavioral and physiologic consequences of sleep deprivation [3].

The present work was carried out to test the effect of sleep deprivation on the following:

  • Vascular reactivity to noradrenaline, acetylcholine, indomethacin, vasopressin, and sodium nitroprusside
  • Twenty-four-hour and 48-h recovery on the vascular reactivity
  • The changes in adrenocorticotrophic hormone, cortisone, adrenaline, noradrenaline, and C-reactive protein (CRP) in the same conditions
  • The changes in arterial blood pressure in the same conditions.



  Materials and Methods Top


Animals

This study was conducted on 140 adult male albino rats (200 ± 10 g). The animals were maintained in the normal light–dark cycle and housed in cages measuring 70 × 70 × 60 cm (five animals/cage) and at room temperature (24–25°C) throughout the study period. Food and water were available ad libitum throughout the whole procedure. Rats were divided into four groups: group 1, the control group, which included 20 male albino rats; group 2, the 'sleep-deprived group', which included 40 male albino rats that were subjected to total sleep deprivation for 96 h; group 3, the '24-h sleep recovery' group, which included 40 male albino rats that were sleep deprived for 96 h and returned to home cages and were left undisturbed for 24 h; and group 4, the '48-h sleep recovery group', which included 40 male albino rats that were sleep deprived for 96 h and were returned to home cages and were left undisturbed for 48 h.

Equipment

  • A physiograph MK III-S (four channels, universal coupler; Narco Biosystem, Texas, USA)
  • Force displacement transducer 0.5–5 g (Grass, USA, St Louis, MO, USA)
  • Isolated organ bath, 10 ml capacity (Harvard, Cambourne, Cambridge, UK)
  • Spectrophotometer (Shimadzu/double beam spectrophotometer UV 150; Germany, Merck, Schuchardt, Germany)
  • Centrifuge (Narco-Biosystem, Cambridge, UK).


Chemicals

  • Noradrenaline powder (El-Gomhoria Company, Egypt): Noradrenaline (10–5 mol/l) solution was freshly prepared by dissolving a gram mol of noradrenaline powder in 1 l of distilled water for preparing 1 mol/l solution, and then diluted 1 : 10 with distilled water five times for preparing 10–5 mol/l solution
  • Acetylcholine (ACh) powder (El-Gomhoria Company): ACh (10–6 mol/l) solution was freshly prepared by dissolving a gram mol of ACh powder in 1 l of distilled water for preparing 1 mol/l solution, and then diluted 1: 10 with distilled water six times for preparing 10–6 mol/l solution
  • Sodium nitroprusside powder (Novartis Company, Egypt): Na nitroprusside (10–6 mol/l) solution was freshly prepared by dissolving a gram mol of Na nitroprusside powder in 1 l of distilled water for preparing 1 mol/l solution, and then diluted 1 : 10 with distilled water six times for preparing 10–6 mol/l solution
  • Vasopressin powder (Sigma-Aldrich Company, Cairo, Egypt): Vasopressin (10–6 mol/l) solution was freshly prepared by dissolving a gram mol of vasopressin powder in 1 l of distilled water for preparing 1 mol/l solution, and then diluted 1 : 10 with distilled water six times for preparing 10–6 mol/l solution
  • Indomethacin (Sigma-Aldrich Company): Indomethacin (10–6 mol/l) solution was freshly prepared by dissolving a gram mol of indomethacin powder in 1 l of distilled water for preparing 1 mol/l solution, and then diluted 1 : 10 with distilled water six times for preparing 10–6 mol/l solution
  • Kits for the estimation of serum adrenaline, noradrenaline, cortisol, and adrenocorticotropic hormone (ACTH) (ElAab Science Co. Ltd., Wuhan, China)
  • Kits for the estimation of C-reactive protein (CRP) (Omega Diagnostic, Egypt).


Methods

  • Blood samples were obtained for ACTH, cortisone, adrenaline, noradrenaline, and CRP estimations
    • Induction of sleep deprivation: Sleep deprivation was induced by keeping the rat for 96 h using the platform-over-water technique. Rats were individually placed on a circular platform (6.5 cm in diameter) in a cage (23 × 23 × 29 cm) filled with water up to 1 cm below the platform level. During paradoxical sleep, rats tended to fall off the platform because of muscular atonia and awakened on contact with water. Moreover, before the commencement of the paradoxical sleep deprivation protocol, all sleep-deprived animals received a habituation period on the platform – that is, 1 h/day for 3 days [4]. Food and water were provided ad libitum. Water in the bottles was changed daily, and food intake was not modified during sleep deprivation
    • All four experimental groups were subjected after the period of the experiment to the following measurements:
    • Invasive blood pressure recording
    • Measurement of aortic vascular reactivity (isolated rat aortic ring technique) [5]: The rat aortic ring preparation was used for the estimation of changes in vascular reactivity in response to noradrenaline, acetylcholine, indomethacin, vasopressin, and sodium nitroprusside
    • Blood sampling [6]: Blood samples were collected from retro-orbital venous plexus of the rat, using a fine nonheparinized capillary tube introduced into the medial epicanthus of the rat's eye. Two milliliters of blood was collected in a graduated tube, centrifugated, and left for clotting at 25°C for 15 min. The supernatant serum was collected in two dry tubes and kept at −80°C for assay within 1 month for the following:
      • Measurement of CRP [7]
      • Measurement of adrenaline [8]
      • Measurement of noradrenaline [8]
      • Measurement of cortisol [9]
      • Measurement of adrencocorticotropic hormone [10].


Statistical analysis

All results were presented as the mean ± SD. The data were analyzed using SPSS program version 12 (SPSS Inc, Chicago, Illinois: U.S.A). For comparison of statistical significance between different groups, a one-way analysis of variance with the post-hoc of Tukey's multiple comparison tests was used. A P value of less than 0.05 was considered statistically significant.


  Results Top


The mean arterial blood pressure, systolic blood pressure, and diastolic blood pressure of the sleep-deprived group were 101 ± 5.35, 150.7 ± 2.9, and 77 ± 3.22 mmHg, respectively, which were significantly higher than the corresponding values in the control group. The same parameters of the 24-h recovery group were 93.2 ± 3.33, 124.7 ± 4.8, and 74 ± 4.7 mmHg, respectively, which were significantly higher than the corresponding values in the adult control group. In the 48-h recovery group, these parameters were 80.5 ± 3.31, 101 ± 3.31, and 66 ± 3.75, respectively, which were nonsignificant when compared with the corresponding values in the adult control group. The mean CRP of the sleep-deprived and the 24-h recovery group was 23.70 ± 2.95 and 22.40 ± 2.5, respectively, which was significantly higher than the corresponding value in the control group. However, the CRP of the 48-h recovery group was 6.60 ± 1.71, which was nonsignificant when compared with the corresponding value in the adult control group ([Table 1]).
Table 1 The mean±SD of systolic, diastolic, and mean arterial blood pressure, and C-reactive protein in control, sleep-deprived, 24-h recovery, and 48-h recovery groups

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The mean vascular reactivity (mg tension) to indomethacin in the sleep-deprived group and the 24-h recovery group was 81.60 ± 3.27 and 80.30 ± 3.68, respectively, which was significantly higher than the corresponding values in the control group. However, the mean vascular reactivity of the 48-h recovery group was 62.50 ± 4.03, which was nonsignificant when compared with the corresponding value in the adult control group. The mean vascular reactivity to norepinephrine in the sleep-deprived group and the 24-h recovery group was 81.50 ± 3.98 and 80.30 ± 1.89, which was significantly higher than the corresponding values in the control group, whereas that of the 48-h recovery group was 61.70 ± 2.67, which was nonsignificant when compared with the corresponding value in the adult control group. The mean vascular reactivity (mg tension) to norepinephrine in the sleep-deprived group was 81.50 ± 3.98, which was significantly higher than the corresponding value in the control group. The mean vascular reactivity in the 24-h recovery group was 80.30 ± 1.89, which was significantly higher when compared with the corresponding value in the adult control group. In the 48-h recovery group, the mean vascular reactivity was 61.70 ± 2.67, which was nonsignificant when compared with the corresponding value in the adult control group. The mean vascular reactivity (mg tension) to vasopressin in the sleep-deprived group and the 24-h recovery group was 81.00 ± 5.93 and 81.20 ± 4.26, respectively, which were significantly higher than the corresponding values in the control group, whereas that of the 48-h recovery group was 60.40 ± 4.33, which was nonsignificant when compared with the corresponding value in the adult control group [Figure 1].
Figure 1: The mean vascular reactivity to indomethacin, norepinephrine, and vasopressin in the control, sleep-deprived, 24-h recovery, and 48-h recovery groups.

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The mean percentage of vasodilation induced by 1 × 10–6 ACh in aortic ring precontracted by 1 × 10–6 vasopressin in the sleep-deprived and 24-h recovery groups was 70 ± 3.5 and 70.2 ± 4.5, respectively, which was significantly lower than the corresponding value in the control group. In the 48-h recovery group, the mean percentage of vasodilation was 84.2 ± 2.9, which was nonsignificant when compared with the corresponding value in the control group. The mean percentages of vasodilation induced by 1 × 10–6 ACh in aortic ring precontracted by 1 × 10–6 indomethacin in the sleep-deprived and the 24-h recovery groups were 72 ± 3.4 and 70.2 ± 4.2, which were significantly lower than the corresponding value in the control group. In the 48-h recovery group, the mean percentage of vasodilation was 84.5 ± 2.9, which was nonsignificant when compared with the corresponding value in the control group. The mean percentages of vasodilation induced by 1 × 10–6 ACh in aortic ring precontracted by 1 × 10–6 norepinephrine in the sleep-deprived and 24-h recovery groups were 73 ± 3.4 and 70.2 ± 4.1, respectively, which were significantly lower than the corresponding value in the control group. In the 48-h recovery group, the mean percentage of vasodilation was 84.2 ± 2.9, which was nonsignificant when compared with the corresponding value in the control group [Figure 2].
Figure 2: Percentage of vasodilation induced 1 × 106 ACh in aortic ring precontracted by vasopressin, indomethacin, and noradrenaline in the control, sleep-deprived, 24-h recovery, and 48-h recovery groups.

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The mean percentages of vasodilation induced by 1 × 10–6 sodium nitroprusside in aortic ring precontracted by 1 × 10–5 norepinephrine in the sleep-deprived, 24-h recovery, and 48-h recovery groups were 93.30 ± 2.26, 92.60 ± 2.48, and 93.70 ± 2.21, respectively, which were nonsignificant when compared with the corresponding value in the control group. The mean percentages of vasodilation induced by 1 × 10–6 sodium nitroprusside in aortic ring precontracted by 1 × 10–5 of vasopressin in the sleep-deprived, 24-h recovery, and 48-h recovery groups were 93.30 ± 2.28, 92.60 ± 2.48, and 93.70 ± 2.23, respectively, which were nonsignificant when compared with the corresponding value in the control group. The mean percentages of vasodilation induced by 1 × 10–6 sodium nitroprusside in aortic ring precontracted by 1 × 10–5 of indomethacin in the sleep-deprived, 24-h recovery, and 48-h recovery groups were 93.70 ± 2.33, 92.90 ± 2.48, and 93.70 ± 2.21, respectively, which were nonsignificant when compared with the corresponding value in the control group [Figure 3].
Figure 3: Percentage of vasodilation induced by 1 × 106 sodium nitroprusside in aortic ring precontracted by norepinephrine, vasopressin, and indomethacin in the control, sleep-deprived, 24-h recovery, and 48-h recovery groups.

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The mean ± SD of noradrenaline in the sleep-deprived group was 1660.0 ± 3.2, which was significantly higher than the corresponding value in the control group. Noradrenaline in the 24-h recovery and 48-h recovery groups were 577.10 ± 4.3 and 483.50 ± 4.7, respectively, which were nonsignificant when compared with the corresponding control group [Figure 4].
Figure 4: The mean ± SD of noradrenaline (pg ml) in the control, 24-h recovery, and 48-h recovery groups.

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The mean ± SD of adrenaline in the sleep-deprived group was 260.20 ± 2.6, which was significantly higher than the corresponding value in the control group. The mean ± SD of adrenaline in the 24-h recovery and 48-h recovery groups was 118.90 ± 5.0 and 113.70 ± 4.4, respectively, which was nonsignificant when compared with the corresponding value in the control group [Figure 5].
Figure 5: The mean ± SD of adrenaline (pg ml) in the control, 24-h recovery, and 48-h recovery groups.

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The mean ± SD of ACTH in the sleep-deprived group was 151 ± 2.78, which was significantly higher than the corresponding value in the control group. The mean ACTH in the 24-h recovery and 48-h recovery groups was 21.50 ± 1.65 and 20.90 ± 1.79, respectively, which was significantly lower when compared with the corresponding value in the adult control group [Figure 6].
Figure 6: The mean ± SD of ACTH (ng ml) in the control, SD, 24-h recovery, and 48-h recovery groups.

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The mean ± SD of cortisone in the sleep-deprived group was 299.20 ± 4.98, which was significantly higher than the corresponding value in the control group. The mean ± SD of cortisone in the 24-h recovery and 48-h recovery groups was 62.30 ± 2.71 and 61.10 ± 0.99, respectively, which significantly lower when compared with the corresponding value in the adult control group [Figure 7].
Figure 7: The mean ± SD of cortisone (ng ml) in the control, SD, 24-h recovery, and 48-h recovery groups.

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  Discussion Top


The present study was conducted to elucidate the impact of sleep deprivation and recovery on vascular reactivity and blood pressure of adult albino rats. Sleep-deprived rats showed a significant increase in the serum level of adrenaline, noradrenaline, ACTH, and cortisol when compared with the control group. This is because sleep loss has been deemed a stressor [11]. Stress is the response of the organism to any stimulus that alters the homeostasis. The hypothalamic–pituitary–adrenal (HPA) axis is the major neuroendocrine mediator of the stress response. A stressful stimulus perceived by the senses ultimately induces the release of CRH from the paraventricular nucleus of the hypothalamus. CRH stimulates the release of ACTH from the anterior pituitary, and ACTH subsequently initiates the liberation of glucocorticoids from the adrenal cortex. In addition, the HPA axis receives relevant feedback from other areas of the brain, such as the hippocampus and amygdala [12]. An important interplay is also the excitatory reciprocal interaction between the HPA axis and the brain stem sympathetic locus coeruleus–norepinephrine system. CRH activates the locus coeruleus. In turn, at the beginning of the stress response, there is a large sympathetic activation, followed by glucocorticoid release from the adrenal cortex.

In the present work, it was noticed that mean arterial blood pressure in sleep-deprived rats was significantly higher than the corresponding value in the control group. This result is in agreement with that of Palagini et al. [13], who showed that experimental sleep deprivation, short sleep duration, and persistent insomnia are associated with increased blood pressure and increased risk for hypertension, even after controlling for other risk factors. In addition, several studies have found that experimental sleep deprivation leads to increased blood pressure [14], and even half a night of sleep loss has been reported to increase blood pressure in patients with hypertension or prehypertension [15].

Pathophysiological mechanisms underlying the association between sleep deprivation and elevated blood pressure may be related to sympathetic activation. On the basis of controlled chronobiological studies, Burgess et al. [16] found that sleep is more important for sympathetic nervous system regulation of the heart in comparison with the parasympathetic system that appeared to be more under circadian control. In that study, posture and light were strictly controlled. Sympathetic nervous system activity was assessed using the pre-ejection period estimated from impedance cardiography indices (estimating isovolumic contraction time), and parasympathetic activity was estimated using the respiratory sinus arrhythmia (based on spectral analysis of beat-to-beat cardiac intervals). Blood pressure could be increased during sleep deprivation because of increased sympathetic outflow to the heart or periphery, because of changes in baroreflex sensitivity, baroreflex resetting to a higher level, or a combination of these factors. Mechanisms that maintain cardiovascular system may respond differently depending on experimental conditions.

In addition to sympathetic activation and baroreflex sensitivity, sleep deprivation was associated with raised inflammatory markers as shown in our study. There was a significant increase in the level of CRP in the sleep-deprived group when compared with the control group. This result is in agreement with that of Hans et al. [17], who showed that sleep deprivation elevated CRP, which is an inflammatory marker of cardiovascular risk.

CRP is a pentameric hepatocyte protein and is the major marker of the acute-phase response, or the formation of plasma proteins in response to an inflammatory stimulus [18]. The hepatic production of CRP has long been used clinically as a classical acute phase response indicator. Synthesis of CRP in the liver is largely controlled by interleukin-6 (IL-6) and also by tumor necrosis factor-α and IL-1 [19]. The production of CRP is thought to reflect the activity of these cytokines, particularly IL-6 [20]. Although IL-6 levels display circadian variability, CRP levels have been shown to be quite stable across 24 h [21] and, in the absence of disease, are quite reproducible even over weeks and months [22]. CRP has been shown to promote the secretion of inflammatory mediators by vascular endothelium [23] and opsonizes low-density lipoprotein for uptake by macrophages in atherosclerotic plaques [24]. These data suggest that CRP may be directly implicated in the development of atherosclerotic lesions.

During healthy normal sleep, blood pressure drops to its lowest point in the day, and levels of endothelial markers decrease as well [25]. During experimental sleep deprivation, blood pressure and other indicators of sympathetic output have been found to increase [14]. It has been argued that shear stresses or physical stress forces, associated with increased blood pressure, may activate inflammatory mediators [26].

This could occur through increased endothelial activation and production of inflammatory mediators such as IL-6. Other changes associated with sleep loss may have also contributed to the increases in CRP encountered in our experiments. In-vitro studies have suggested an influence of steroids in the synthesis of CRP [19]. Similarly, increased body mass has been shown to predispose to cytokinemia due to the synthesis and release of IL-6 from adipose tissue [27].

In the present study, sleep deprivation was associated with a significant increase in vascular reactivity to noradrenaline, indomethacin, and vasopressin. Moreover, the percentage of vasodilation to ACh after addition of these vasoconstrictors showed a significant decrease. In addition, the percentage of vasodilation to sodium nitroprusside showed nonsignificant changes when compared with the control group. These results are in agreement with the findings of Sauvet et al. [28], who demonstrated that total sleep deprivation alter ACh-induced vasodilation, a sign of endothelial dysfunction. This result confirms previous studies showing endothelial dysfunction after acute sleep deprivation [29] or acute sleep restriction [30].

Moreover, Amir et al. [31] showed no significant effect of total sleep deprivation on endothelium-independent vasodilation as assessed with sodium nitroprusside delivery. These results support the view that acute total sleep deprivation in rats is sufficient stress to trigger an alteration of the endothelial-dependent vasodilation, which is a sign of endothelial dysfunction that is brought by a sympathetic independent mechanism. According to previously published studies of rats and humans, 24 h of wakefulness induces a transient increase in blood pressure and heart rate. These changes were not observed in sympathectomized rats [32]. Thus, a decrease in total sleep time produces an increase in sympathetic activity during the wakefulness period, leading to a transient rise in blood pressure and heart rate. Sympathetic activity enhancement has been involved in the decrease in endothelial-dependent vasodilation [33] and is suspected to link sleep deprivation and endothelial dysfunction [30]. However, these results showed for the first time that endothelial dysfunction induced by total sleep deprivation persists in sympathectomized rats. Thus, we may conclude that the initial endothelial dysfunction observed after 24 h of wakefulness is a sympathetic independent mechanism. This is an important result for understanding the kinetics of the vascular alterations observed after sleep loss. However, we cannot exclude that a persistent increase in sympathetic activity would favor endothelial dysfunction during repeated total sleep deprivation or prolonged sleep restriction. Amir et al. [31] and Wehrens et al. [34] showed that endothelial dysfunction after a night shift was greater in individuals with a longer history of night-shift duty and was associated with an increase in sympathetic activity. Moreover, Sgoifo et al. [35] demonstrated that sleep deprivation changes baroreflex sensitivity. In their study, the animals were exposed to an acute restraining stress, and sleep deprivation induced a blunted parasympathetic antagonism following sympathetic activation, together with an increased susceptibility to cardiac arrhythmia. Hence, when total sleep deprivation is associated with stress, we cannot exclude that a large increase in sympathetic activity could be related to endothelial dysfunction.

In the present study, 24-h recovery rats showed a significant decrease in serum ACTH and cortisone when compared with the control group, and this is in agreement with the findings of Andersen et al. [36]. Vgontzas et al. [37] hypothesized that increased slow-wave sleep after sleep deprivation is associated with decreased cortisol levels during the first recovery night compared with baseline.

This work showed that sleep deprivation was associated with increased mean arterial blood pressure and impaired vascular reactivity through the activation of the stress response system and the activation of the inflammatory system, which induced endothelial dysfunction key factors for cardiovascular risk.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
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