Institute of Physiology, University of Lausanne Medical School, 1005 Lausanne, Switzerland
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ABSTRACT |
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The effects of the
sympathetic activation elicited by a mental stress on insulin
sensitivity and energy expenditure (O2) were studied in 11 lean and 8 obese women during a
hyperinsulinemic-euglycemic clamp. Six lean women were restudied under
nonselective
-adrenergic blockade with propranolol to determine the
role of
-adrenoceptors in the metabolic response to mental stress.
In lean women, mental stress increased
O2 by 20%, whole body glucose
utilization ([6,6-2H2]glucose) by 34%, and
cardiac index (thoracic bioimpedance) by 25%, whereas systemic
vascular resistance decreased by 24%. In obese women, mental stress
increased energy expenditure as in lean subjects, but it neither
stimulated glucose uptake nor decreased systemic vascular resistance.
In the six lean women who were restudied under propranolol, the rise in
O2, glucose uptake, and cardiac output
and the decrease in systemic vascular resistance during mental stress
were all abolished. It is concluded that 1) in lean
subjects, mental stress stimulates glucose uptake and energy
expenditure and produces vasodilation; activation of
-adrenoceptors
is involved in these responses; and 2) in obese patients,
the effects of mental stress on glucose uptake and systemic vascular
resistance, but not on energy expenditure, are blunted.
obesity; sympathetic nervous system; thermogenesis; glucose uptake; insulin resistance
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INTRODUCTION |
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THE SYMPATHETIC NERVOUS SYSTEM (SNS) exerts complex effects on insulin sensitivity and energy metabolism. This complexity is illustrated by the observation that various conditions known to elicit SNS activation have markedly different metabolic effects. A lower body negative pressure (LBNP) decreases insulin-mediated glucose disposal (17) but does not significantly alter resting energy expenditure (26). In contrast, mental stress acutely enhances insulin-induced glucose utilization (14, 20, 27). Whether it affects energy expenditure has, to our knowledge, not been documented. These divergent metabolic effects of LBNP and mental stress may correspond to a compartmentalization of the SNS, with activation of distinct sympathetic fibers according to the mode of SNS activation. Thus it has been observed that LBNP increases muscle, but not skin, sympathetic nerve activity (29) while mental stress stimulates SNS in both muscle and skin (28).
The hemodynamic effects of LBNP and mental stress differ in several
respects. LBNP results in a decrease in leg blood flow, related with
2-adrenergic receptor-mediated vasoconstriction (12).
In contrast, mental stress acutely stimulates limbs blood flow through
mechanisms incompletely elucidated but which involve endothelial NO
release (7, 15) and
-adrenoceptor activation (10,
18). Since alterations of muscle blood flow may modulate insulin
sensitivity by altering the rate of delivery of both glucose and
insulin itself to skeletal muscle (1), these hemodynamic effects of LBNP and mental stress may be involved in the regulation of
insulin-mediated glucose disposal.
Several reports indicate the presence of alterations of SNS activity in obese patients. In obese Pima Indians, reduced norepinephrine turnover has been observed, suggesting an overall decrease in SNS activity. No such alteration was observed in obese Caucasians (5). In contrast, obese Pima Indians and Caucasians have an increased muscle sympathetic nerve activity related to their increased body fat (21, 22).
To further evaluate the role of the SNS in metabolic control and the possible relationship between metabolic and hemodynamic actions of SNS, we evaluated the effects of mental stress in lean and obese subjects. The specific aims were to further delineate the effects of mental stress on insulin sensitivity and energy expenditure in healthy lean females and to assess whether the metabolic effects of mental stress were altered in obesity.
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SUBJECTS AND METHODS |
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Subjects
Two groups of subjects were selected to take part in this study. Group 1 consisted of eight obese women with a mean age of 25.5 ± (SD) 0.7 yr (r = 24-27), body mass index (BMI) 33.9 ± 2.2 kg/m2 (r = 29-47), percentage of body fat (determined from skinfold thickness measurement; Ref. 8) 33.4 ± 1.3% (r = 28-40), and fat-free mass (FFM) 60.9 ± 1.9 kg (r = 56-70). Group 2 consisted of 11 lean women with a mean age of 24.6 ± 0.8 yr (r = 20-28), BMI 21.8 ± 0.4 kg/m2 (r = 20-24), percentage of body fat 17.6 ± 0.8% (r = 14-23), and FFM 50.5 ± 1.1 kg (r = 45-56). All subjects were in good physical condition and were nonsmokers. They were not currently taking any medication and had no family history of diabetes or hypertension. The experimental protocol was approved by the Ethical Committee of the Lausanne University Medical School, and every subject provided informed written consent.General Procedure
Experiments began in the morning after an overnight fast. Subjects were requested not to consume caffeine- or alcohol-containing drinks for at least 24 h before the study; furthermore, they were asked not to get involved in any strenuous physical activity during the 3 days preceding the study. All the women were studied during the follicular phase of the menstrual cycle.Each subject took part in one or two protocols aimed at assessing the metabolic and hemodynamic effects of mental stress during euglycemic hyperinsulinemic clamp. On the arrival of the subjects in the metabolic laboratory, one indwelling venous cannula was inserted into a vein of their right wrist. The right hand was subsequently placed into a thermostabilized box heated at 56°C to achieve partial arterialization of venous blood. Blood samples were periodically collected through this catheter. A second indwelling cannula was inserted into an antecubital vein of the contralateral arm for infusion of glucose tracer, insulin, glucose, and propranolol.
In protocol 1, aimed at assessing the metabolic effects of
mental stress during hyperinsulinemia, a primed continuous infusion of
[6,6-2H2]glucose (MassTrace, Woburn, MA; 11.1 µmol/kg bolus, 111 nmol · kg1 · min
1
continuous) was started at 7:30 AM. Sixty minutes after the beginning of the [6,6-2H2]glucose infusion, a
hyperinsulinemic-euglycemic clamp (0.4 mU · kg
1 · min
1; Ref. 6)
was started (time 0). The exogenous glucose was labeled with
1.25% [6,6-2H2]glucose to avoid dilution of
the tracer by the glucose infusion. After 150 min of euglycemic
hyperinsulinemia, a mental stress was applied for 30 min while the
clamp was continued. Mental stress consisted of a succession of 5-min
periods of mental arithmetic (20) and 5-min periods of
Stroop's color conflict test (10) for 30 min. The latter
consists of presenting color words written in an incongruent color ink,
the subject having to tell the color of the ink and to make abstraction
of the writing of the word. Blood samples were collected at 5-min
intervals for monitoring of plasma glucose concentrations and at 30-min
intervals between 0 and 150 min and then at 5-10-min intervals
between 150 and 180 min for measurements of plasma hormones, substrate
concentrations, and [2H2]glucose enrichment.
Heart rate (ECG), blood pressure, and cardiac index (estimated with
thoracic bioimpedancemetry (BioMed NCCOM3-R7 CDDP system, BioMed
Medical Manufacturing, Irvine, CA; Ref. 23) were recorded every 5 min.
Thoracic bioimpedance has been shown to be a reliable method to assess
cardiac output semiquantitatively. As such, it is suitable for
monitoring changes in hemodynamics over time; however, it does not
allow for reliable comparison of cardiac output of obese and lean
patients because of differences in body composition (31).
Respiratory gas exchanges were continuously monitored by means of
indirect calorimetry with the use of a ventilated hood system (13). Because we observed a sharp increase in respiratory
exchange ratio during mental stress followed by a marked drop below
prestress values, and because this pattern strongly suggests
significant hyperventilation, we did not calculate energy expenditure
or substrate oxidation from respiratory gas exchanges, and present only
O2 uptake (O2) values as an
index of energy expenditure.
To assess the type of adrenoceptors involved in response to mental
stress, six lean subjects [mean age 24.5 ± 0.9 yr
(r = 20-28), BMI 22.3 ± 0.9 kg/m2
(r = 21-24), percent body fat 18.7 ± 0.9% (r = 16-23), FFM 50 ± 1 kg
(r = 46-55)] were restudied in a second protocol.
This protocol was identical to the first one, except that a propranolol infusion (80 µg/kg bolus, 1 µg · kg1 · min
1
continuous) was started 30 min before the beginning of the mental stress and was carried out until the end of the test. Protocols 1 and 2 were carried out in a randomized order.
Analysis
Plasma glucose concentration was determined with a Beckman glucose analyzer 2 (Beckman Instruments, Fullerton, CA). Plasma lactate concentration was measured with a lactate analyzer (Yellow Springs Instruments, Yellow Springs, OH). Plasma epinephrine and norepinephrine concentrations were determined by high-performance liquid chromatography (11). Plasma insulin concentration was determined by RIA (kit from Biodata, Guidoni, Montecello, Italy). Isotopic enrichment of glucose was determined by gas chromatography-mass spectrometry (GC 5890-MS 5971, Hewlett-Packard, Palo Alto, CA) after preparation of pentoacetyl derivates.Calculations
Glucose appearance and utilization were calculated from [6,6-2H2]glucose dilution analysis using "hot infusion" equations (9). Endogenous glucose production was calculated as glucose appearance minus glucose perfusion. Systemic vascular resistance was calculated as the ratio between mean arterial pressure and cardiac index and was expressed in terms of arbitrary units (U).Statistics
All results are given as means ± SE. The effect of mental stress on all parameters mentioned was assessed with analysis of variance for repeated measurements. Between-group comparisons were done by a two-way analysis of variance and Fisher's protected least significant difference (PLSD) tests. ![]() |
RESULTS |
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Cardiovascular Parameters
Protocol 1.
As shown in Table 1, Baseline data were
similar in lean and obese subjects. Mental stress caused a significant
increase in heart rate, mean blood pressure, and cardiac index in both
groups. The increase in cardiac index was, however, 25% smaller
(P < 0.05), and the increase in mean blood pressure was
18% higher (P < 0.05) in the obese group compared
with the lean group (Table 1). Systemic vascular resistance decreased
by 24% in the lean group (P < 0.05) but not in the obese
group.
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Protocol 2.
As shown in Table 2, propranolol
decreased baseline heart rate (P < 0.05) and cardiac
index (P < 0.05), but systolic and diastolic blood pressure
did not change. Mental stress thereafter increased mean blood pressure
(P < 0.05), but heart rate, cardiac index, and
systemic vascular resistance remained unchanged (Table 2).
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Hormones and Substrates
Protocol 1.
Basal plasma insulin concentration was 59 ± 9 pmol/l in the lean
group and 132 ± 27 pmol/l (P < 0.02) in the
obese group. During the hyperinsulinemic clamp, plasma insulin
concentration was 250 ± 16 pmol/l in the control group and
366 ± 66 pmol/l (P < 0.05) in the obese group
and remained stable through the experiment (Fig.
1). Plasma glucose concentrations were
4.94 ± 0.03 mmol/l (coefficient of variation 2%) and 4.96 ± 0.02 mmol/l (coefficient of variation 2%) in lean and obese
individuals, respectively. Plasma potassium concentrations decreased
slightly, from 3.7 ± 0.1 and 3.8 ± 0.1 meq/l in the basal
state to 3.5 ± 0.1 and 3.6 ± 0.1 meq/l during
hyperinsulinemia in lean and obese subjects, respectively. Mental
stress caused a significant increase in plasma epinephrine
concentration in both lean and obese groups and a nonsignificant
increase in norepinephrine 10 min after the beginning of the mental
stress (min 160; Fig. 2).
Plasma insulin, glucose, and potassium concentrations remained
unchanged, but blood lactate increased from 1.08 ± 0.05 to
1.43 ± 0.13 mmol/l, (P < 0.01) in lean subjects and
from 1.05 ± 0.07 to 1.45 ± 0.07 mmol/l, (P < 0.01) in obese patients.
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Protocol 2.
Propranolol infusion did not alter hormones and substrates
concentrations (Fig. 3). The peak
increase in epinephrine (from 0.14 ± 0.01 to 0.24 ± 0.02 nmol/l) and norepinephrine (from 1.51 ± 0.17 to 1.85 ± 0.19 nmol/l) observed was also comparable with those recorded in the same
subjects under control conditions. Propranolol abolished the rise in
lactate [from 0.99 ± 0.06 to 1.02 ± 0.07 mmol/l,
non-significant (NS)].
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Glucose Utilization
In lean subjects, mental stress increased the rate of glucose infusion required to maintain euglycemia (from 24.0 ± 2.3 µmol · kg FFMIn obese patients, both the rate of glucose infusion (20.9 ± 2.6 µmol · kg FFM1 · min
1)
and glucose utilization (22.7 ± 2.4 µmol · kg
FFM
1 · min
1) were
similar to those observed in lean subjects. Endogenous glucose
production was nearly completely suppressed by hyperinsulinemia (0.9 ± 0.5 µmol · kg
FFM
1 · min
1). After mental stress,
the increases in both glucose infusion and glucose utilization were
markedly blunted (Fig. 1). As in lean subjects, mental stress did not
increase glucose production.
Protocol 2.
In the study without propranolol, the stimulation of glucose
utilization during mental stress was not completely compensated by the
increase in glucose infusion, resulting in a slight, transient drop in
glycemia (from 4.91 ± 0.9 mmol/l to 4.78 ± 0.04, P < 0.05). Baseline clamp parameters were not affected
by propranolol, but the stimulation of glucose uptake elicited by
mental stress was abolished (from 25.0 ± 3.1 to 26.8 ± 3.2 µmol · kg lean
mass1 · min
1, NS) compared with the
data obtained in the same subjects without propranolol (from 25.3 ± 2.7 to 33.6 ± 2.6 µmol · kg lean
mass
1 · min
1, P < 0.05; Fig. 3). Endogenous glucose production remained suppressed throughout the tests.
Oxygen Consumption
Protocol 1.
Mental stress increased O2 by 20% (from
192 ± 5 to 229 ± 6 ml/min, P < 0.0001) in the
control group and by 21% in the obese group (from 248 ± 15 to
299 ± 12 ml/min, P < 0.0001). There was no
difference in the amplitude of the
O2
increase between obese and lean patients (Fig.
4).
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Protocol 2.
Basal O2 was not significantly altered
by propranolol, but mental stress increased
O2 by only 6% (from 189 ± 8 to
201 ± 8 ml/min, NS), which was significantly less
(P < 0.05) than the increase observed without
propranolol in the same subjects (from 191 ± 8 to 227 ± 11 ml/min, P < 0.001) (Fig.
5).
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DISCUSSION |
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Mental stress acutely increases insulin-stimulated glucose utilization in healthy lean humans. The major new observation of this study is that this effect is abolished in obese nondiabetic patients.
In lean subjects, mental stress elicited an increase in glucose uptake in the forearm, as already reported by Jern (14), and at the whole body level, as reported by Moan et al. (20) and Touma et al. (27). This effect of mental stress differs from that observed during other sympathetic activation procedures. It has indeed been observed that a LBNP decreases glucose uptake (17). This difference may be explained by the hemodynamic effects of mental stress. In our study, as in previous reports that used either mental arithmetic (20) or the color word conflict test (10), mental stress increased cardiac index and decreased peripheral vascular resistance, presumably in skeletal muscle.
Several studies have documented an increase in limb blood flow during
mental stress in humans. This effect was completely inhibited by
-adrenergic antagonists (10, 18) and by inhibitors of
NO synthase, indicating that endothelial NO release was involved (4, 7, 15). There is no definitive explanation for this inhibition of vasodilation by both
-adrenergic antagonists and NO
synthase inhibitors. The vascular responses to mental stress may be
complex, with simultaneous vasodilation through activation of
-adrenergic receptors and endothelial NO release. Alternatively, it
is possible that stimulation of
-adrenergic receptors is involved in
endothelial NO release in this condition. The recent observation that
NO release contributes to
-adrenergic-mediated vasodilation would be
consistent with this explanation (19).
It has been proposed that stimulation of muscle blood flow enhances
insulin actions in humans during mental stress (20). The
inhibition of both vasodilation and stimulation of insulin sensitivity
by -adrenergic antagonists further supports this hypothesis.
Furthermore, mental stress failed to stimulate insulin sensitivity in
obese patients. This was concomitant with an absent vasodilatory
response already reported by other investigators (25). It
was not related to a lower sympathetic stimulation, because the
increase in plasma epinephrine and norepinephrine, the stimulation of
heart rate, and the increase in
O2 were
all similar to what was recorded in lean subjects. These observations indicate a specific impairment of the vascular response to mental stress in obesity. Obese patients also have impaired vasodilation in
response to other NO-dependent vasodilatory stimuli such as hyperinsulinemia and intra-arterial cholinergic agonists
(24). It is, therefore, likely that these impaired
responses to mental stress were related to endothelial dysfunction
associated with obesity. Because insulin was infused according to body
weight rather than lean body mass, plasma insulin concentrations during the clamp were 46% higher in obese patients than in lean subjects. This is likely to account for the similar glucose utilization observed
in the two groups of subjects. The higher insulin concentrations attained in obese subjects is, however, unlikely to affect our conclusions. Although insulin has potent vasodilatory properties, it is
unlikely that a vasodilation induced by the higher insulin concentrations in obese patients marked the effects of a subsequent mental stress, because insulin vasodilatory actions have been shown to
be markedly blunted in obesity (16, 30).
The second new observation of this study is that mental stress elicits
a significant 20% increase in energy expenditure that was sustained
during 30 min. This stimulation was secondary to an endogenous
activation of the SNS, because it was associated with increases in
plasma norepinephrine and epinephrine concentrations. Moreover, this
stimulation was abolished by propranolol. Interestingly, mental stress
elicited a comparable increase in energy expenditure in obese and lean
subjects. This observation suggests that the stimulation of the SNS by
mental stress and the metabolic effectors responsible for the increased
O2 activated by the SNS are not altered
in obesity. This contrasts with the observation that thermogenesis induced by norepinephrine infusion is blunted in obese patients (2, 3). The reason for these differing effects of
exogenously administered and endogenously released catecholamines on
energy expenditure in obese patients remains unclear.
In summary, our data indicate that a mental stress performed during
moderate hyperinsulinemia in healthy volunteers stimulates insulin-mediated glucose disposal, possibly in relation to a decreased systemic vascular resistance; in addition, it increases energy expenditure. These two effects are abolished by -adrenergic receptor antagonists. In obese patients, the stimulation of insulin-mediated glucose disposal and the decrease in vascular resistance by mental stress are both abolished, possibly in relationship with endothelial cell dysfunction. In contrast, the thermogenic effect of mental stress
is retained in obesity.
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ACKNOWLEDGEMENTS |
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This study was supported by Grant no. 32-45387.95 (E. Jéquier) from the Swiss National Science Foundation.
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FOOTNOTES |
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Address for reprint requests and other correspondence: L. Tappy, Institut de Physiologie, 7 Rue du Bugnon, 1005 Lausanne, Switzerland (E-mail: Luc.Tappy{at}iphysiol.unil.ch).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 24 November 1999; accepted in final form 2 May 2000.
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REFERENCES |
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![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
1.
Baron, AD.
Cardiovascular actions of insulin in humans. Implications for insulin sensitivity and vascular tone.
Baillieres Clin Endocrinol Metab
7:
961-987,
1993[ISI][Medline].
2.
Blaak, EE,
Van Baak MA,
Kemerink GJ,
Pakbiers MT,
Heidendal GA,
and
Saris WH.
Beta-adrenergic stimulation of energy expenditure and forearm skeletal muscle metabolism in lean and obese men.
Am J Physiol Endocrinol Metab
267:
E306-E315,
1994
3.
Blaak, EE,
Van Baak MA,
Kemerink GJ,
Pakbiers MT,
Heidendal GA,
and
Saris WH.
Beta-adrenergic stimulation of skeletal muscle metabolism in relation to weight reduction in obese men.
Am J Physiol Endocrinol Metab
267:
E316-E322,
1994
4.
Cardillo, C,
Kilcoyne CM,
Quyyumi AA,
Cannon OR, III,
and
Panza JA.
Role of nitric oxide in the vasodilator response to mental stress in normal subjects.
Am J Cardiol
80:
1070-1074,
1997[ISI][Medline].
5.
Christin, L,
O'Connell M,
Bogardus C,
Danforth EJ,
and
Ravussin E.
Norepinephrine turnover and energy expenditure in Pima Indian and White men.
Metabolism
42:
723-729,
1993[ISI][Medline].
6.
DeFronzo, RA,
Tobin JD,
and
Andres R.
Glucose clamp technique a method for quantifying insulin secretion and resistance.
Am J Physiol Endocrinol Metab Gastrointest Physiol
237:
E214-E223,
1979
7.
Dietz, NM,
Rivera JM,
Eggener SE,
Fix RT,
Warner OD,
and
Joyner MJ.
Nitric oxide contributes to the rise in forearm blood flow during mental stress in humans.
J Physiol (Lond)
480:
361-368,
1994[Abstract].
8.
Durnin, JVGA,
and
Womersley J.
Body fat assessment for total body density and its estimation from skinfold thickness: measurement of 481 men and women from 16 to 72 years.
Br J Nutr
32:
77-97,
1979.
9.
Finegood, DT,
Bergman RN,
and
Vranic M.
Estimation of endogenous glucose production during hyperinsulinemic euglycemic glucose clamps: comparison of labelled and unlabelled glucose infusates.
Diabetes
36:
914-924,
1987[Abstract].
10.
Freyschuss, U,
Hjemdahl P,
Juhlin-Dannfelt A,
and
Linde B.
Cardiovascular and sympathoadrenal responses to mental stress: influence of -blockade.
Am J Physiol Heart Circ Physiol
255:
H1443-H1451,
1988
11.
Hallman, J,
Farnebo OL,
Hamberger B,
and
Jonsson G.
A sensitive method for determination of plasma catecholamines using liquid chromatography with electrochemical detection.
Life Sci
23:
1049-1052,
1978[ISI][Medline].
12.
Jacobsen, TN,
Converse RLJ,
and
Victor RG.
Contrasting effects of propranolol on sympathetic nerve activity and vascular resistance during orthostatic stress.
Circulation
85:
1072-1076,
1992[Abstract].
13.
Jallut, D,
Tappy L,
Kohot M,
Bloesch D,
Monger R,
Schotz Y,
Chioléro R,
Felber JP,
Livio JJ,
and
Jéquier E.
Energy balance in elderly patients after surgery for a femoral neck fracture.
J Parenter Enter Nutr
14:
563-568,
1990[Abstract].
14.
Jern, S.
Effects of insulin on vascular responses to mental stress and norepinephrine in human forearm.
Hypertension
24:
686-694,
1994[Abstract].
15.
Joyner, MJ,
and
Dietz NM.
Nitric oxide and vasodilation in human limbs.
J Appl Physiol
83:
1785-1796,
1997
16.
Laakso, M,
Edelman SV,
Brechtel G,
and
Baron AD.
Decreased effect of insulin to stimulate skeletal muscle blood flow in obese man.
J Clin Invest
85:
1844-1852,
1990[ISI][Medline].
17.
Lembo, G,
Capaldo B,
Rendina V,
Iaccarino G,
Napoli R,
Goida R,
Trimarco B,
and
Sacca L.
Acute noradrenergic activation induces insulin resistance in human skeletal muscle.
Am J Physiol Endocrinol Metab
266:
E242-E247,
1994
18.
Linde, B,
Hjemdahl P,
Freyschoss U,
and
Johlin-Dannfelt A.
Adipose tissue and skeletal muscle blood flow during mental stress.
Am J Physiol Endocrinol Metab
256:
E12-E18,
1989
19.
Majmodar, NG,
Anomba D,
Robson SC,
and
Ford GA.
Contribution of nitric oxide to 2-adrenoceptor-mediated vasodilatation in human forearm arterial vasculature.
Br J Clin Pharmacol
47:
173-177,
1999[ISI][Medline].
20.
Moan, A,
Hoieggen A,
Nordby G,
Os I,
Eide I,
and
Kjeldsen SE.
Mental stress increases glucose uptake during hyperinsulinemia: associations with sympathetic and cardiovascular responsiveness.
Metabolism
44:
1303-1307,
1995[ISI][Medline].
21.
Scherrer, U,
Randin D,
Tappy L,
Vollenweider P,
Jéquier E,
and
Nicod P.
Body fat and sympathetic nerve activity in healthy subjects.
Circulation
89:
2634-2640,
1994[Abstract].
22.
Spraul, M,
Anderson EA,
Bogardus C,
and
Ravussin E.
Muscle sympathetic nerve activity in response to glucose ingestion.
Diabetes
43:
191-196,
1994[Abstract].
23.
Sramek, BB.
Thoracic electrical bioimpedance measurement of cardiac output.
Crit Care Med
22:
1337-1339,
1994[ISI][Medline].
24.
Steinberg, OH,
Chaker H,
Leaming R,
Johnson A,
Brechtel G,
and
Baron AD.
Obesity/insulin resistance is associated with endothelial dysfunction. Implications for the syndrome of insulin resistance.
J Clin Invest
97:
2601-2610,
1996
25.
Sung, BH,
Wilson MF,
Izzo JL, Jr,
Ramirez L,
and
Dandona P.
Moderately obese, insulin-resistant women exhibit abnormal vascular reactivity to stress.
Hypertension
30:
848-853,
1997
26.
Tappy, L,
Girardet K,
Schwaller N,
Vollenweider L,
Jéquier E,
Nicod P,
and
Scherrer U.
Metabolic effects of an increase of sympathetic activity in healthy humans.
Int J Obes
19:
419-422,
1995[ISI].
27.
Touma, T,
Takishita S,
Kimura Y,
Muratani H,
and
Fukiyama K.
Mild mental stress increases insulin sensitivity in healthy young men.
Clin Exp Hypertens
18:
1105-1114,
1996[ISI][Medline].
28.
Vallbo, AB,
Hagbarth KE,
Torebjörk HE,
and
Wallin BG.
Somatosensory, proprioceptive, and sympathetic activity in human peripheral nerves.
Physiol Rev
59:
919-957,
1919.
29.
Vissing, SF,
Scherrer U,
and
Victor RG.
Relation between sympathetic outflow and vascular resistance in calf during perturbations in central venous pressure. Evidence for cardiopulmonary afferent regulation of calf vascular resistance in humans.
Circ Res
65:
1710-1717,
1989[Abstract].
30.
Vollenweider, P,
Tappy L,
Randin D,
Schneiter P,
Jéquier E,
Nicod P,
and
Scherrer U.
Differential effects of hyperinsulinemia and carbohydrate metabolism on sympathetic nerve activity and muscle blood flow in humans.
J Clin Invest
92:
147-154,
1993[ISI][Medline].
31.
Wilson, MF,
Sung BH,
Pincomb GA,
and
Lovallo WR.
Simultaneous measurement of stroke volume by impedance cardiography and nuclear ventriculography: comparisons at rest and exercise.
Ann Biomed Eng
17:
475-482,
1989[ISI][Medline].
32.
Wolfe, RR.
Tracers in Metabolic Research Radioisotope and Stable Isotope/Mass Spectrometry Methods. New York: Liss, 1984.