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1 Geriatric Research, Local warming of
skin induces vasodilation by unknown mechanisms. To test whether nitric
oxide (NO) is involved, we examined effects of NO synthase (NOS)
inhibition with
NG-nitro-L-arginine
methyl ester (L-NAME) on
vasodilation induced by local warming of skin in six subjects. Two
adjacent sites on the forearm were instrumented with intradermal
microdialysis probes for delivery of
L-NAME and sodium
nitroprusside. Skin blood flow was monitored by
laser-Doppler flowmetry (LDF) at microdialysis sites. Local temperature
(Tloc) of the skin at both sites
was controlled with special LDF probe holders. Mean arterial pressure (MAP; Finapres) was measured and cutaneous vascular conductance calculated (CVC = LDF/MAP = mV/mmHg). Data collection began with a
control period (Tloc at both sites = 34°C). One site was then warmed to 41°C while the second was
maintained at 34°C. Local warming increased CVC from 1.44 ± 0.41 to 4.28 ± 0.60 mV/mmHg (P < 0.05). Subsequent L-NAME
administration reduced CVC to 2.28 ± 0.47 mV/mmHg
(P < 0.05 vs. heating), despite the
continued elevation of Tloc. At a
Tloc of 34°C,
L-NAME reduced CVC from 1.17 ± 0.23 to 0.75 ± 0.11 mV/mmHg
(P < 0.05). Administration of sodium
nitroprusside increased CVC to levels no different from those induced
by local warming. Thus NOS inhibition attenuated, and sodium
nitroprusside restored, the cutaneous vasodilation induced by elevation
of Tloc; therefore, the mechanism
of cutaneous vasodilation by local warming requires NOS generation of NO.
skin blood flow; skin temperature; vasodilation; laser-Doppler
flowmetry; microdialysis
IN HUMANS, CUTANEOUS BLOOD VESSELS are controlled by
both neurogenic reflexes and local factors (11, 17). In nonglabrous, or
"hairy," skin, reflex control of the cutaneous vasculature is
mediated by two sympathetic pathways: a noradrenergic vasoconstrictor system and an active vasodilator system that involves cholinergic cotransmission (14). Nitric oxide (NO) production is also involved in
cutaneous active vasodilation (13, 20). A powerful local factor that
controls the cutaneous vasculature is the local temperature (Tloc) of skin blood vessels
(17). Local cooling of the skin causes a localized vasoconstriction
that can reduce skin blood flow (SkBF) to minimal levels (17). This
vasoconstriction is mediated by an axon reflex mechanism and requires
norepinephrine release from vasoconstrictor nerve terminals (17). Local
warming of the skin causes a localized vasodilation that is graded with Tloc that can reach maximal levels
if skin temperature is increased to 42°C for 20-40 min (12,
21). Thus Tloc control mechanisms can augment vasodilator effects of the neurogenic active
vasoconstrictor system during exposure to high ambient temperatures.
This will facilitate thermal homeostasis.
The degree of vasodilation induced by local warming of the skin has
been proposed as a clinical tool for evaluation of vasomotor dysfunction in diabetes and other disease states (3, 18), despite the
fact that the mechanism that mediates the effects of local warming on
the cutaneous vasculature is not fully defined. The initial increase in
SkBF during local warming may be caused by a reduced effectiveness of
noradrenergic vasoconstriction through decreased affinity of
Recent work showed that NO synthase (NOS) production of NO is required
for full expression of active vasodilation of the skin during
hyperthermia (13, 20). Other work in humans showed that NO donors can
increase SkBF directly (22) and that NO contributes to a basal dilator
tone in forearm and finger skin (4). Furthermore, Goldsmith et al. (10)
found that intradermal injection of either NG-nitro-L-arginine-methyl
ester (L-NAME) or
NG-monomethyl-L-arginine
(L-NMMA) attenuates the
cutaneous vasodilation produced by 30 s of forearm immersion in
45°C water. The observations that NOS production of NO plays a
significant role in the cutaneous vasculature suggests that NO could be
involved in the cutaneous vasodilation caused by increases in the
temperature of the skin. We sought to examine this possibility by
testing the hypothesis that the cutaneous vasodilation effected by
local warming of the skin requires NOS production of NO.
To test our hypothesis, we locally administered a NOS inhibitor to
forearm skin while monitoring SkBF. The approach we chose was to
combine NOS inhibition by local administration of
L-NAME by intradermal
microdialysis with local SkBF measurements with laser-Doppler flowmetry
(LDF) from a small volume of skin (~1 mm3). Intradermal microdialysis
permitted local administration of L-NAME directly into the
interstitial space of a small area of dermis. Monitoring LDF over a
site instrumented with an intradermal microdialysis probe permitted
monitoring of local drug effects with high local concentrations without
risking confounding systemic effects. Because there is no question
about the locus of measurement or the locus of drug delivery, the
combination of LDF with local administration of
L-NAME provided a direct
approach to study the role of NO in the local control of SkBF.
Six subjects (5 men and 1 woman) participated in this study. Their
average age was 31 ± 4 (SE) yr, average weight was 66 ± 5 kg,
and average height was 173 ± 3 cm. All subjects were normotensive, in good health, and taking no medications. All subjects gave their informed consent to participate in these institutionally approved studies. There was no caffeine intake on the day of the study, and all
subjects were nonsmokers. The menstrual phase was not assessed in the
female subject.
On arrival in the laboratory, each subject had two intradermal
microdialysis probes placed on the ventral aspect of one forearm. The
probes are made in our laboratory from borosilicate glass tubing and a
1-cm length of capillary microdialysis membrane (200-µm diameter,
molecular weight cutoff 20) reinforced by a 51-µm-diameter coated
stainless steel wire placed in the lumen of the membrane and tubing
(Fig. 1). Microdialysis probes were placed
at least 5 cm apart on the forearm so that manipulations at one site
did not influence the other. Probes were inserted at each site as follows. A 25-gauge needle was inserted through the dermis by using
sterile technique. Entry and exit points were ~2-3 cm apart. The
microdialysis probe was threaded through the internal lumen of the
needle, the needle was then withdrawn, and the probe was left in place.
The microdialysis membrane was entirely within the dermis, with entry
and exit through the skin via the borosilicate tubing. Ultrasound
measurements showed that probes were placed 0.3-1.0 mm under the
epidermal surface and thus were within the dermis. After probe
insertion, subjects waited for ~2 h or more to permit resolution of
needle insertion trauma before additional instrumentation was placed.
Anderson et al. (1) reported that the injury caused by insertion of the
needle required to place an intradermal microdialysis probe resolves
during a period of 90-135 min, thus permitting in vivo studies
without the confounding effects of trauma.
ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
INTRODUCTION
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
2-receptors for norepinephrine
(5). This mechanism appears to contribute no more than 10% of the
maximal skin vasodilation caused by prolonged local warming to 42°C
(17). Given these observations, and that local warming of forearm
causes a vasodilation far greater than that caused by blockade of
noradrenergic vasoconstrictor nerves alone, mechanisms other than
alteration of noradrenergic vasoconstriction must be involved (7, 17, 23). For example, it was postulated that the effects of local warming
could be mediated through axon reflex mechanisms and that local warming
elicits vasodilation through activation of the same nerves and
neurotransmitters that cause active thermoregulatory vasodilation (17).
This appears not to be the case on the basis of the observation that
botulinum toxin abolishes neurogenic active vasodilation during heat
stress but does not alter the vasodilation induced by local skin
warming (14). Furthermore, the observation that the vasodilation caused
by local warming is preserved in skin denervated by burns and in skin
grafts suggests that the process might not be neurally mediated at all
(2, 9). Alternatively, endothelial factors such as NO may be involved
in the vasodilation.
METHODS
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Fig. 1.
Illustration of microdialysis probe for use in human in vivo studies.
Probe is made from borosilicate tubing with a 1-cm length of capillary
microdialysis membrane (200-µm diameter, molecular weight cutoff 20)
reinforced by a 0.0015-in.-diameter coated stainless steel wire. Probe
can be used to sample or deliver drugs in dermal, subcutaneous,
adipose, or skeletal muscle tissues. Our intradermal microdialysis
procedure is performed as follows: a 25-gauge needle is inserted
through dermis by using sterile technique. Microdialysis probe is
threaded through internal lumen of needle. Needle is then withdrawn,
leaving membrane in place. Microdialysis probe is perfused at a rate of
0.2-10 µl/min by using a microinfusion pump.
After needle trauma had resolved, subjects were placed in the supine position and instrumented to measure LDF from skin at the two microdialysis sites (MBF3D dual-channel flowmeter, Moor Instruments, Devon, UK). Cutaneous LDF measurements are a reliable index of SkBF and are uninfluenced by blood flow in the underlying skeletal muscle (19). Mean arterial pressure (MAP) was recorded continuously from a finger (Finapres blood pressure monitor, Ohmeda, Madison, WI). LDF probes were held in special probe holders that permit LDF measurements and control of Tloc (14). After placement of the LDF probes, both microdialysis probes were perfused with Ringer solution at a rate of 2 µl/min by using a microinfusion pump (Harvard 22 syringe pump, Harvard Apparatus, South Natick, MA).
As illustrated in Fig. 2, data collection
began with a 10-min control period with
Tloc held constant at 34°C.
Tloc was then increased at one of
the LDF microdialysis sites to 41°C. This temperature was chosen to
avoid any activation of pain fibers as occasionally happens with local
warming to 42°C. After LDF measurements had increased and
stabilized, both microdialysis probes were perfused with a 5 mM
solution of L-NAME (Sigma
Chemical, St. Louis, MO) dissolved in Ringer solution. This dose was
chosen on the basis of preliminary studies. In those studies, we
examined the effect of 1.25, 2.5, 5, 10, and 20 mM
L-NAME doses on the vasodilation
induced by local warming of the skin and found no difference in the
responses induced by the three highest doses. Given that >5
mM L-NAME doses had no added effect on cutaneous vascular conductance (CVC), it appeared that NOS blockade was complete;
thus a 5 mM concentration was chosen for our formal study.
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After perfusion with L-NAME, both microdialysis probes were perfused with 28 mM sodium nitroprusside (SNP; Sigma Chemical) in Ringer solution for 20-40 min to effect vasodilation by an endothelium-independent mechanism (15). This dose was chosen on the basis of preliminary studies. In those studies, we examined the effect of increasing doses of SNP. A dose of 28 mM was found to reproducibly cause a maximal vasodilation, indistinguishable from that caused by local warming of the skin to 41°C.
On a separate day, subjects returned to the laboratory and the above protocol was repeated except that no L-NAME was administered: microdialysis probes were perfused with Ringer solution only. This series of studies tested for any effects of microdialysis in responses to local warming of the skin to 41°C.
Data are presented as means ± SE. For data analysis, CVC was indexed as LDF (in mV) divided by MAP (in mmHg) to control for any changes in blood pressure during data collection. Vasomotor responses were analyzed by comparing the average levels of CVC over the last 5 min of each period. CVC responses were analyzed by repeated-measures ANOVA followed by specific means comparisons.
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DISCUSSION
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Figure 3 summarizes the results of the
study with L-NAME
administration. During the initial control period, before any local warming or L-NAME perfusion, CVC
values did not differ significantly between the two microdialysis sites
(1.44 ± 0.41 and 1.17 ± 0.23 mV/mmHg;
P > 0.05 between sites). During
local warming to 41°C, CVC increased to 4.28 ± 0.60 mV/mmHg
(P < 0.05 vs. initial control). Local warming of one site did not influence the normothermic site.
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Perfusion with L-NAME significantly reduced CVC at both the normothermic and the locally warmed sites. At a Tloc of 34°C, L-NAME perfusion reduced CVC to 0.75 ± 0.11 mV/mmHg (P < 0.05). At a Tloc of 41°C, CVC fell from 4.28 ± 0.60 to 2.28 ± 0.47 mV/mmHg (P < 0.05) during perfusion with L-NAME.
Perfusion with SNP increased CVC at both the normothermic and locally warmed sites. At a Tloc of 34°C, SNP perfusion increased CVC to 4.05 ± 0.79 mV/mmHg (P < 0.05 vs. initial control and L-NAME at Tloc = 34°C). At a Tloc of 41°C, CVC increased to 4.02 ± 0.63 mV/mmHg (P < 0.05 vs. initial control and L-NAME at Tloc = 41°C; P > 0.05 vs. 41°C alone) during perfusion with SNP. Overall, the levels of CVC achieved with SNP perfusion did not differ between sites with Tloc values of 34 and 41°C (P > 0.05).
Figure 4 summarizes the results of the
study without L-NAME
administration, i.e., with perfusion of the microdialysis probes with
Ringer solution only. After 30 min of local warming to 41°C, CVC
had increased significantly (P < 0.05 vs. initial control) and remained unchanged for a total of 90 min
of warming. Subsequent perfusion with SNP did not change CVC from
levels achieved with local warming alone. At a
Tloc of 34°C, perfusion with
Ringer solution alone for 90 min did not alter CVC from initial levels (P > 0.05); however, SNP perfusion
increased CVC significantly (P < 0.05, Ringer
vs. SNP).
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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The results of this study show that NOS production of NO participates in the vasodilation induced by local warming of the skin. This conclusion is based on the observation that blockade of NOS by L-NAME greatly attenuates the local increase in CVC as effected by local warming of the skin to 41°C. No such changes in CVC occurred during perfusion of microdialysis fibers with Ringer solution alone; thus effects of microdialysis are not responsible for the observed changes in CVC with L-NAME perfusion. The abolition is not likely due to any antimuscarinic effects of L-NAME (3) because the local vasodilation is not altered by atropine blockade of muscarinic receptors or blockade of cholinergic nerves by botulinum toxin (14).
When L-NAME was infused at the microdialysis site with a Tloc of 34°C, there was a significant reduction in CVC, showing that NO generation by NOS contributes a tonic vasodilator tone to cutaneous blood vessels under normothermic conditions. No such changes occurred during administration of Ringer solution alone. A similar finding was reported by Coffman (4), who recorded reductions in LDF during intra-arterial infusion of L-NMMA under normothermic conditions. Dietz et al. (6) also reported that forearm blood flow (FBF) was reduced during infusion of L-NMMA into the brachial artery under normothermic conditions. Although FBF measurements cannot distinguish between blood flow to skin and skeletal muscle, their results lend support to a tonic vasodilator effect of NO. In contrast, Noon et al. (16) reported that intra-arterial infusion of L-NMMA at doses of 1, 2, and 4 µM/min 1) reduced FBF, 2) reduced LDF from skin on the glabrous skin of the finger, and 3) had no effect on LDF from skin on the dorsum of the finger. These different findings may be attributable to cooler thermal conditions in the study by Noon et al. because NOS inhibition does not reduce SkBF under cool conditions (4). Overall, results from our study favor a contribution by NO generated by NOS in the basal tone in nonglabrous skin in normothermia.
In response to the initial warming of the skin, during the perfusion with Ringer solution only, CVC increased greatly. This demonstrates that the ability of the cutaneous vessels to respond to increases in Tloc persisted after microdialysis probe placement. Thus trauma associated with placement of the probes did not render the vessels incapable of responding to local thermal factors.
After CVC had increased and stabilized at a high level with Tloc held at 41°C, L-NAME blockade on NOS activity produced a significant reduction in CVC to levels not statistically different from those with a Tloc of 34°C. Subsequent perfusion with SNP, an endothelium-independent NO donor, restored CVC to the levels achieved with a Tloc of 41°C before L-NAME perfusion. These results show that NOS activity is required for full expression of cutaneous vasodilation as it is for full expression of neurogenic active vasodilation during hyperthermia (13, 20). However, in the case of local warming, NOS activity, and presumably generation of NO, appears required for most of the vasodilation to occur. In the case of neurogenic reflex vasodilation, mediated by cutaneous cholinergic cotransmission, only ~30% of the vasodilation appears to be NO dependent (13, 20).
Although our results demonstrate that NO generation by NOS plays a
major role in the vasodilation induced by prolonged local warming, this
may not be the sole vasodilator mechanism involved that can be
activated by local application of heat, particularly when pain fibers
are activated. In our preliminary studies,
Tloc was increased to 42°C to
maximally dilate the skin vessels (21); however, three subjects
reported pain at the locally warmed sites as
Tloc approached 42°C.
Tloc was immediately reduced to
41°C, with prompt resolution of pain in all subjects. The overall
duration of the sensation of pain was very brief, varying from ~5 to
20 s. All subjects described the pain as "mild."
Subsequent perfusion with L-NAME
at doses up to 20 mM failed to reduce CVC; however, CVC did fall in
response to subsequent perfusion with a 10 mM norepinephrine in Ringer
solution. This verified that the vessels had not been "damaged"
by the painful temperature and were still capable of vasoconstriction.
Figure 5 illustrates this phenomenon in one
subject. The failure of L-NAME
to reduce CVC at locally warmed sites after pain had been reported,
even for the briefest of moments, suggests that another mechanism could
be involved in cutaneous vasodilation after nociceptors have been
activated. Some evidence suggests that prostaglandins could be
generated by nociceptor activation and could effect an NO-independent
vasodilation (22). Alternatively, it is possible that activation of
pain fibers increased NOS activity greatly, perhaps by release of
substance P. In our studies, in which the subjects experienced pain,
relatively high doses of L-NAME
(up to 20 mM) did not reduce CVC. It is possible that NOS activity had
increased to such a level that even this relatively high dose did not
give complete NOS blockade; thus we are not able to say whether the
mechanism related to pain is an NO-dependent process or whether
NO-independent pathways are involved.
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The foregoing observations suggest a number of possible roles for NO in the vasodilation induced by local warming, although current data do not distinguish among those possibilities. For example, studies in the rabbit ear suggest that NO produced by endothelial cells acts in conjunction with a neurotransmitter released during hyperthermia to effect increases in ear blood flow (8). According to this scheme, tonic generation of NO by endothelial cells mediates production of a tonic level of cGMP, which is required for neurogenic reflex active vasodilation. Farrell and Bishop (8) speculated that humans may possess mechanisms other than NO that maintain the level of cGMP so that, even with complete NOS blockade, the level of cGMP would be sufficient to permit vasodilation. Our observation that the vasodilation induced by local warming alone can be altered by NOS blockade, but that the vasodilation appears to be resistant to NOS blockade after pain fiber activation, is consistent with this proposal.
In summary, we found that blockade of NOS with L-NAME reduces SkBF under normothermic conditions, demonstrating that this system contributes a basal vasodilator tone to cutaneous blood vessels. In addition, blockade of NOS abolishes the cutaneous vasodilation induced by local warming of the skin in humans. Thus NO generation by NOS is involved in the mechanism of vasodilation induced by local warming of the skin in humans.
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ACKNOWLEDGEMENTS |
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The authors thank Dr. David Boggett of Moor Instruments, Ltd., for generous support of our studies. The authors are grateful to the volunteers for their participation in these studies and to Dr. Craig G. Crandall for thoughtful advice.
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FOOTNOTES |
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This research was supported by American Heart Association, Texas Affiliate, Grants 94G374 and 96R374.
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. §1734 solely to indicate this fact.
Address for reprint requests: D. L. Kellogg, Jr., Divs. of Geriatrics and Gerontology and of Clinical Pharmacology, Dept. of Medicine, Univ. of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr., San Antonio, TX 78284 (E-mail: kelloggd{at}uthscsa.edu).
Received 8 July 1998; accepted in final form 10 December 1998.
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RESULTS
DISCUSSION
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J. E. Wingo, D. A. Low, D. M. Keller, R. M. Brothers, M. Shibasaki, and C. G. Crandall Effect of elevated local temperature on cutaneous vasoconstrictor responsiveness in humans J Appl Physiol, February 1, 2009; 106(2): 571 - 575. [Abstract] [Full Text] [PDF]
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L. A. Sokolnicki, N. A. Strom, S. K. Roberts, S. A. Kingsley-Berg, A. Basu, and N. Charkoudian Skin blood flow and nitric oxide during body heating in type 2 diabetes mellitus J Appl Physiol, February 1, 2009; 106(2): 566 - 570. [Abstract] [Full Text] [PDF]
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 G. J. Hodges, W. A. Kosiba, K. Zhao, and J. M. Johnson The involvement of heating rate and vasoconstrictor nerves in the cutaneous vasodilator response to skin warming Am J Physiol Heart Circ Physiol, January 1, 2009; 296(1): H51 - H56. [Abstract] [Full Text] [PDF]
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M. Shibasaki, D. A. Low, S. L. Davis, and C. G. Crandall Nitric oxide inhibits cutaneous vasoconstriction to exogenous norepinephrine J Appl Physiol, November 1, 2008; 105(5): 1504 - 1508. [Abstract] [Full Text] [PDF]
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M. A. Black, D. J. Green, and N. T. Cable Exercise prevents age-related decline in nitric-oxide-mediated vasodilator function in cutaneous microvessels J. Physiol., July 15, 2008; 586(14): 3511 - 3524. [Abstract] [Full Text] [PDF]
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G. J. Hodges, W. A. Kosiba, K. Zhao, and J. M. Johnson The involvement of norepinephrine, neuropeptide Y, and nitric oxide in the cutaneous vasodilator response to local heating in humans J Appl Physiol, July 1, 2008; 105(1): 233 - 240. [Abstract] [Full Text] [PDF]
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D. L. Kellogg Jr., J. L. Zhao, and Y. Wu Endothelial nitric oxide synthase control mechanisms in the cutaneous vasculature of humans in vivo Am J Physiol Heart Circ Physiol, July 1, 2008; 295(1): H123 - H129. [Abstract] [Full Text] [PDF]
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J. M. Stewart, I. Taneja, N. Raghunath, D. Clarke, and M. S. Medow Intradermal angiotensin II administration attenuates the local cutaneous vasodilator heating response Am J Physiol Heart Circ Physiol, July 1, 2008; 295(1): H327 - H334. [Abstract] [Full Text] [PDF]
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D. Sigaudo-Roussel, B. Fromy, and J. L. Saumet In vivo vasodilating mechanisms: who's NOS involved? J. Physiol., February 1, 2008; 586(3): 689 - 690. [Full Text] [PDF]
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D. L. Kellogg Jr, J. L. Zhao, and Y. Wu Neuronal nitric oxide synthase control mechanisms in the cutaneous vasculature of humans in vivo J. Physiol., February 1, 2008; 586(3): 847 - 857. [Abstract] [Full Text] [PDF]
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J. M. Stewart, I. Taneja, J. Glover, and M. S. Medow Angiotensin II type 1 receptor blockade corrects cutaneous nitric oxide deficit in postural tachycardia syndrome Am J Physiol Heart Circ Physiol, January 1, 2008; 294(1): H466 - H473. [Abstract] [Full Text] [PDF]
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F. Yamazaki, K. Takahara, R. Sone, and J. M. Johnson Influence of hyperoxia on skin vasomotor control in normothermic and heat-stressed humans J Appl Physiol, December 1, 2007; 103(6): 2026 - 2033. [Abstract] [Full Text] [PDF]
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 L. A. Sokolnicki, S. Khosla, and N. Charkoudian Effects of testosterone and estradiol on cutaneous vasodilation during local warming in older men Am J Physiol Endocrinol Metab, November 1, 2007; 293(5): E1426 - E1429. [Abstract] [Full Text] [PDF]
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C. Demiot, F. Dignat-George, J.-O. Fortrat, F. Sabatier, C. Gharib, I. Larina, G. Gauquelin-Koch, R. Hughson, and M.-A. Custaud WISE 2005: chronic bed rest impairs microcirculatory endothelium in women Am J Physiol Heart Circ Physiol, November 1, 2007; 293(5): H3159 - H3164. [Abstract] [Full Text] [PDF]
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G. J. Hodges, W. A. Kosiba, K. Zhao, G. E. Alvarez, and J. M. Johnson The role of baseline in the cutaneous vasoconstrictor responses during combined local and whole body cooling in humans Am J Physiol Heart Circ Physiol, November 1, 2007; 293(5): H3187 - H3192. [Abstract] [Full Text] [PDF]
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J. M. Stewart, M. S. Medow, C. T. Minson, and I. Taneja Cutaneous neuronal nitric oxide is specifically decreased in postural tachycardia syndrome Am J Physiol Heart Circ Physiol, October 1, 2007; 293(4): H2161 - H2167. [Abstract] [Full Text] [PDF]
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A. H. Eid, K. Maiti, S. Mitra, M. A. Chotani, S. Flavahan, S. R. Bailey, C. S. Thompson-Torgerson, and N. A. Flavahan Estrogen increases smooth muscle expression of {alpha}2C-adrenoceptors and cold-induced constriction of cutaneous arteries Am J Physiol Heart Circ Physiol, September 1, 2007; 293(3): H1955 - H1961. [Abstract] [Full Text] [PDF]
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 H. Gunawardena, N. D. Harris, C. Carmichael, and N. J. McHugh Maximum blood flow and microvascular regulatory responses in systemic sclerosis Rheumatology, July 1, 2007; 46(7): 1079 - 1082. [Abstract] [Full Text] [PDF]
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B. W. Wilkins, E. A. Martin, S. K. Roberts, and M. J. Joyner Preserved reflex cutaneous vasodilation in cystic fibrosis does not include an enhanced nitric oxide-dependent mechanism J Appl Physiol, June 1, 2007; 102(6): 2301 - 2306. [Abstract] [Full Text] [PDF]
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L. A. Holowatz and W. L. Kenney Up-regulation of arginase activity contributes to attenuated reflex cutaneous vasodilatation in hypertensive humans J. Physiol., June 1, 2007; 581(2): 863 - 872. [Abstract] [Full Text] [PDF]
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 R. J. Widmer, R. H. Stewart, M. F. Young, J. E. Laurinec, G. A. Laine, and C. M. Quick Application of local heat induces capillary recruitment in the Pallid bat wing Am J Physiol Regulatory Integrative Comp Physiol, June 1, 2007; 292(6): R2312 - R2317. [Abstract] [Full Text] [PDF]
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K. Kimura, D. A. Low, D. M. Keller, S. L. Davis, and C. G. Crandall Cutaneous blood flow and sweat rate responses to exogenous administration of acetylcholine and methacholine J Appl Physiol, May 1, 2007; 102(5): 1856 - 1861. [Abstract] [Full Text] [PDF]
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D. A. Low, M. Shibasaki, S. L. Davis, D. M. Keller, and C. G. Crandall Does local heating-induced nitric oxide production attenuate vasoconstrictor responsiveness to lower body negative pressure in human skin? J Appl Physiol, May 1, 2007; 102(5): 1839 - 1843. [Abstract] [Full Text] [PDF]
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L. A. Sokolnicki, S. K. Roberts, B. W. Wilkins, A. Basu, and N. Charkoudian Contribution of nitric oxide to cutaneous microvascular dilation in individuals with type 2 diabetes mellitus Am J Physiol Endocrinol Metab, January 1, 2007; 292(1): E314 - E318. [Abstract] [Full Text] [PDF]
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B. J. Wong and C. T. Minson Neurokinin-1 receptor desensitization attenuates cutaneous active vasodilatation in humans J. Physiol., December 15, 2006; 577(3): 1043 - 1051. [Abstract] [Full Text] [PDF]
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 M. J. Stark, L. Dierkx, V. L. Clifton, and I. M. R. Wright Alterations in the Maternal Peripheral Microvascular Response in Pregnancies Complicated by Preeclampsia and the Impact of Fetal Sex Reproductive Sciences, December 1, 2006; 13(8): 573 - 578. [Abstract] [PDF]
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M. Salvat-Melis, P. H. Carpentier, C. T. Minson, A. Boignard, G. R. McCord, A. Paris, A. Moreau-Gaudry, and J.-L. Cracowski Digital thermal hyperaemia impairment does not relate to skin fibrosis or macrovascular disease in systemic sclerosis Rheumatology, December 1, 2006; 45(12): 1490 - 1496. [Abstract] [Full Text] [PDF]
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J. Bellien, M. Iacob, L. Gutierrez, M. Isabelle, A. Lahary, C. Thuillez, and R. Joannides Crucial Role of NO and Endothelium-Derived Hyperpolarizing Factor in Human Sustained Conduit Artery Flow-Mediated Dilatation Hypertension, December 1, 2006; 48(6): 1088 - 1094. [Abstract] [Full Text] [PDF]
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 D. Roosterman, T. Goerge, S. W. Schneider, N. W. Bunnett, and M. Steinhoff Neuronal control of skin function: the skin as a neuroimmunoendocrine organ. Physiol Rev, October 1, 2006; 86(4): 1309 - 1379. [Abstract] [Full Text] [PDF]
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G. R. McCord, J.-L. Cracowski, and C. T. Minson Prostanoids contribute to cutaneous active vasodilation in humans Am J Physiol Regulatory Integrative Comp Physiol, September 1, 2006; 291(3): R596 - R602. [Abstract] [Full Text] [PDF]
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R. J. Widmer, J. E. Laurinec, M. F. Young, G. A. Laine, and C. M. Quick Local heat produces a shear-mediated biphasic response in the thermoregulatory microcirculation of the Pallid bat wing Am J Physiol Regulatory Integrative Comp Physiol, September 1, 2006; 291(3): R625 - R632. [Abstract] [Full Text] [PDF]
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G. J. Hodges, K. Zhao, W. A. Kosiba, and J. M. Johnson The involvement of nitric oxide in the cutaneous vasoconstrictor response to local cooling in humans J. Physiol., August 1, 2006; 574(3): 849 - 857. [Abstract] [Full Text] [PDF]
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D. L. Kellogg Jr In vivo mechanisms of cutaneous vasodilation and vasoconstriction in humans during thermoregulatory challenges J Appl Physiol, May 1, 2006; 100(5): 1709 - 1718. [Abstract] [Full Text] [PDF]
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B. L. Houghton, J. R. Meendering, B. J. Wong, and C. T. Minson Nitric oxide and noradrenaline contribute to the temperature threshold of the axon reflex response to gradual local heating in human skin J. Physiol., May 1, 2006; 572(3): 811 - 820. [Abstract] [Full Text] [PDF]
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N. T. Cable Unlocking the secrets of skin blood flow J. Physiol., May 1, 2006; 572(3): 613 - 613. [Full Text] [PDF]
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 R. Yamamoto and Y. Aso Synergistic Association of Metabolic Syndrome and Overt Nephropathy With Elevated Asymmetric Dimethylarginine in Serum and Impaired Cutaneous Microvasodilation in Patients With Type 2 Diabetes Diabetes Care, April 1, 2006; 29(4): 928 - 930. [Full Text] [PDF]
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K. Lee and G. W. Mack Role of nitric oxide in methacholine-induced sweating and vasodilation in human skin J Appl Physiol, April 1, 2006; 100(4): 1355 - 1360. [Abstract] [Full Text] [PDF]
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 D. J. Green, A. J. Maiorana, J. H. J. Siong, V. Burke, M. Erickson, C. T. Minson, W. Bilsborough, and G. O'Driscoll Impaired skin blood flow response to environmental heating in chronic heart failure Eur. Heart J., February 1, 2006; 27(3): 338 - 343. [Abstract] [Full Text] [PDF]
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B. J. Wong, S. J. Williams, and C. T. Minson Minimal role for H1 and H2 histamine receptors in cutaneous thermal hyperemia to local heating in humans J Appl Physiol, February 1, 2006; 100(2): 535 - 540. [Abstract] [Full Text] [PDF]
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F. Yamazaki, R. Sone, K. Zhao, G. E. Alvarez, W. A. Kosiba, and J. M. Johnson Rate dependency and role of nitric oxide in the vascular response to direct cooling in human skin J Appl Physiol, January 1, 2006; 100(1): 42 - 50. [Abstract] [Full Text] [PDF]
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B. J Wong, N. J Tublitz, and C. T Minson Neurokinin-1 receptor desensitization to consecutive microdialysis infusions of substance P in human skin J. Physiol., November 1, 2005; 568(3): 1047 - 1056. [Abstract] [Full Text] [PDF]
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 M. S. Medow, C. T. Minson, and J. M. Stewart Decreased Microvascular Nitric Oxide-Dependent Vasodilation in Postural Tachycardia Syndrome Circulation, October 25, 2005; 112(17): 2611 - 2618. [Abstract] [Full Text] [PDF]
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J. Cui, A. Arbab-Zadeh, A. Prasad, S. Durand, B. D. Levine, and C. G. Crandall Effects of Heat Stress on Thermoregulatory Responses in Congestive Heart Failure Patients Circulation, October 11, 2005; 112(15): 2286 - 2292. [Abstract] [Full Text] [PDF]
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 C. Joukhadar, P. Dehghanyar, F. Traunmuller, R. Sauermann, B. Mayer-Helm, A. Georgopoulos, and M. Muller Increase of Microcirculatory Blood Flow Enhances Penetration of Ciprofloxacin into Soft Tissue Antimicrob. Agents Chemother., October 1, 2005; 49(10): 4149 - 4153. [Abstract] [Full Text] [PDF]
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J. R. Meendering, B. N. Torgrimson, B. L. Houghton, J. R. Halliwill, and C. T. Minson Menstrual cycle and sex affect hemodynamic responses to combined orthostatic and heat stress Am J Physiol Heart Circ Physiol, August 1, 2005; 289(2): H631 - H642. [Abstract] [Full Text] [PDF]
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J. M. Johnson, T. C. Yen, K. Zhao, and W. A. Kosiba Sympathetic, sensory, and nonneuronal contributions to the cutaneous vasoconstrictor response to local cooling Am J Physiol Heart Circ Physiol, April 1, 2005; 288(4): H1573 - H1579. [Abstract] [Full Text] [PDF]
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D. L. Kellogg Jr., J. L. Zhao, U. Coey, and J. V. Green Acetylcholine-induced vasodilation is mediated by nitric oxide and prostaglandins in human skin J Appl Physiol, February 1, 2005; 98(2): 629 - 632. [Abstract] [Full Text] [PDF]
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S. Durand, S. L. Davis, J. Cui, and C. G. Crandall Exogenous nitric oxide inhibits sympathetically mediated vasoconstriction in human skin J. Physiol., January 15, 2005; 562(2): 629 - 634. [Abstract] [Full Text] [PDF]
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J. Stewart, A. Kohen, D. Brouder, F. Rahim, S. Adler, R. Garrick, and M. S. Goligorsky Noninvasive interrogation of microvasculature for signs of endothelial dysfunction in patients with chronic renal failure Am J Physiol Heart Circ Physiol, December 1, 2004; 287(6): H2687 - H2696. [Abstract] [Full Text] [PDF]
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S. Golay, C. Haeberli, A. Delachaux, L. Liaudet, P. Kucera, B. Waeber, and F. Feihl Local heating of human skin causes hyperemia without mediation by muscarinic cholinergic receptors or prostanoids J Appl Physiol, November 1, 2004; 97(5): 1781 - 1786. [Abstract] [Full Text] [PDF]
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B. J Wong, B. W Wilkins, and C. T Minson H1 but not H2 histamine receptor activation contributes to the rise in skin blood flow during whole body heating in humans J. Physiol., November 1, 2004; 560(3): 941 - 948. [Abstract] [Full Text] [PDF]
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B. W. Wilkins, L. H. Chung, N. J. Tublitz, B. J. Wong, and C. T. Minson Mechanisms of vasoactive intestinal peptide-mediated vasodilation in human skin J Appl Physiol, October 1, 2004; 97(4): 1291 - 1298. [Abstract] [Full Text] [PDF]
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D. O. Warner, M. J. Joyner, and N. Charkoudian Nicotine increases initial blood flow responses to local heating of human non-glabrous skin J. Physiol., September 15, 2004; 559(3): 975 - 984. [Abstract] [Full Text] [PDF]
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D. P. Stephens, A. R. Saad, L. A. T. Bennett, W. A. Kosiba, and J. M. Johnson Neuropeptide Y antagonism reduces reflex cutaneous vasoconstriction in humans Am J Physiol Heart Circ Physiol, September 1, 2004; 287(3): H1404 - H1409. [Abstract] [Full Text] [PDF]
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 L. M. Peltonen and A. Pyornila Local action of exogenous nitric oxide (NO) on the skin blood flow of rock pigeons (Columba livia) is affected by acclimation and skin site J. Exp. Biol., July 1, 2004; 207(15): 2611 - 2619. [Abstract] [Full Text] [PDF]
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L. Stoner, M. Sabatier, K. Edge, and K. McCully Relationship between blood velocity and conduit artery diameter and the effects of smoking on vascular responsiveness J Appl Physiol, June 1, 2004; 96(6): 2139 - 2145. [Abstract] [Full Text] [PDF]
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 I. M. Steiner, H. Langenberger, C. Marsik, B. X. Mayer, M. Fischer, A. Georgopoulos, M. Muller, G. Heinz, and C. Joukhadar Effect of norepinephrine on cefpirome tissue concentrations in healthy subjects J. Antimicrob. Chemother., March 1, 2004; 53(3): 506 - 511. [Abstract] [Full Text] [PDF]
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L. A. T Bennett, J. M Johnson, D. P Stephens, A. R Saad, and D. L Kellogg Jr Evidence for a Role for Vasoactive Intestinal Peptide in Active Vasodilatation in the Cutaneous Vasculature of Humans J. Physiol., October 1, 2003; 552(1): 223 - 232. [Abstract] [Full Text] [PDF]
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T. A. Munce and W. L. Kenney Age-specific modification of local cutaneous vasodilation by capsaicin-sensitive primary afferents J Appl Physiol, September 1, 2003; 95(3): 1016 - 1024. [Abstract] [Full Text] [PDF]
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B. J. Wong, B. W. Wilkins, L. A. Holowatz, and C. T. Minson Nitric oxide synthase inhibition does not alter the reactive hyperemic response in the cutaneous circulation J Appl Physiol, August 1, 2003; 95(2): 504 - 510. [Abstract] [Full Text] [PDF]
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T. E. Wilson, M. Shibasaki, J. Cui, B. D. Levine, and C. G. Crandall Effects of 14 days of head-down tilt bed rest on cutaneous vasoconstrictor responses in humans J Appl Physiol, June 1, 2003; 94(6): 2113 - 2118. [Abstract] [Full Text] [PDF]
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C. G. Crandall, M. Shibasaki, T. E. Wilson, J. Cui, and B. D. Levine Prolonged head-down tilt exposure reduces maximal cutaneous vasodilator and sweating capacity in humans J Appl Physiol, June 1, 2003; 94(6): 2330 - 2336. [Abstract] [Full Text] [PDF]
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S. R. Colberg, H. K. Parson, D. R. Holton, T. Nunnold, and A. I. Vinik Cutaneous Blood Flow in Type 2 Diabetic Individuals After an Acute Bout of Maximal Exercise Diabetes Care, June 1, 2003; 26(6): 1883 - 1888. [Abstract] [Full Text] [PDF]
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D. L. Kellogg Jr., J. L. Zhao, C. Friel, and L. J. Roman Nitric oxide concentration increases in the cutaneous interstitial space during heat stress in humans J Appl Physiol, May 1, 2003; 94(5): 1971 - 1977. [Abstract] [Full Text] [PDF]
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 N. Charkoudian Skin Blood Flow in Adult Human Thermoregulation: How It Works, When It Does Not, and Why Mayo Clin. Proc., May 1, 2003; 78(5): 603 - 612. [Abstract] [PDF]
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B. W Wilkins, L. A Holowatz, B. J Wong, and C. T Minson Nitric oxide is not permissive for cutaneous active vasodilatation in humans J. Physiol., May 1, 2003; 548(3): 963 - 969. [Abstract] [Full Text] [PDF]
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J. M. Pierzga, A. Frymoyer, and W. L. Kenney Delayed distribution of active vasodilation and altered vascular conductance in aged skin J Appl Physiol, March 1, 2003; 94(3): 1045 - 1053. [Abstract] [Full Text] [PDF]
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M. Shibasaki, T. E. Wilson, J. Cui, and C. G. Crandall Acetylcholine released from cholinergic nerves contributes to cutaneous vasodilation during heat stress J Appl Physiol, December 1, 2002; 93(6): 1947 - 1951. [Abstract] [Full Text] [PDF]
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C. T. Minson, L. A. Holowatz, B. J. Wong, W. L. Kenney, and B. W. Wilkins Decreased nitric oxide- and axon reflex-mediated cutaneous vasodilation with age during local heating J Appl Physiol, November 1, 2002; 93(5): 1644 - 1649. [Abstract] [Full Text] [PDF]
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D. L. Kellogg Jr., Y. Liu, K. McAllister, C. Friel, and P. E. Pergola Bradykinin does not mediate cutaneous active vasodilation during heat stress in humans J Appl Physiol, October 1, 2002; 93(4): 1215 - 1221. [Abstract] [Full Text] [PDF]
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N. Charkoudian, A. Vella, A. S. Reed, C. T. Minson, P. Shah, R. A. Rizza, and M. J. Joyner Cutaneous vascular function during acute hyperglycemia in healthy young adults J Appl Physiol, October 1, 2002; 93(4): 1243 - 1250. [Abstract] [Full Text] [PDF]
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R. Joannides, A. Costentin, M. Iacob, P. Compagnon, A. Lahary, and C. Thuillez Influence of vascular dimension on gender difference in flow-dependent dilatation of peripheral conduit arteries Am J Physiol Heart Circ Physiol, April 1, 2002; 282(4): H1262 - H1269. [Abstract] [Full Text] [PDF]
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N. Charkoudian, J. H. Eisenach, J. L. D. Atkinson, R. D. Fealey, and M. J. Joyner Effects of chronic sympathectomy on locally mediated cutaneous vasodilation in humans J Appl Physiol, February 1, 2002; 92(2): 685 - 690. [Abstract] [Full Text] [PDF]
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 V. L. Clifton, R. Crompton, R. Smith, and I. M. R. Wright Microvascular Effects of CRH in Human Skin Vary in Relation to Gender J. Clin. Endocrinol. Metab., January 1, 2002; 87(1): 267 - 270. [Abstract] [Full Text] [PDF]
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S. Shastry and M. J. Joyner Geldanamycin attenuates NO-mediated dilation in human skin Am J Physiol Heart Circ Physiol, January 1, 2002; 282(1): H232 - H236. [Abstract] [Full Text] [PDF]
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M. J. Joyner, N. M. Dietz, and J. T. Shepherd From Belfast to Mayo and beyond: the use and future of plethysmography to study blood flow in human limbs J Appl Physiol, December 1, 2001; 91(6): 2431 - 2441. [Abstract] [Full Text] [PDF]
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D. L. Kellogg Jr., Y. Liu, and P. E. Pergola Genome and Hormones: Gender Differences in Physiology: Selected Contribution: Gender differences in the endothelin-B receptor contribution to basal cutaneous vascular tone in humans J Appl Physiol, November 1, 2001; 91(5): 2407 - 2411. [Abstract] [Full Text] [PDF]
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C. T. Minson, L. T. Berry, and M. J. Joyner Nitric oxide and neurally mediated regulation of skin blood flow during local heating J Appl Physiol, October 1, 2001; 91(4): 1619 - 1626. [Abstract] [Full Text] [PDF]
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D. P. Stephens, N. Charkoudian, J. M. Benevento, J. M. Johnson, and J. L. Saumet The influence of topical capsaicin on the local thermal control of skin blood flow in humans Am J Physiol Regulatory Integrative Comp Physiol, September 1, 2001; 281(3): R894 - R901. [Abstract] [Full Text] [PDF]
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M Shibasaki, N Kondo, and C G Crandall Evidence for metaboreceptor stimulation of sweating in normothermic and heat-stressed humans J. Physiol., July 15, 2001; 534(2): 605 - 611. [Abstract] [Full Text] [PDF]
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N. Charkoudian, B. Fromy, and J.-L. Saumet Reflex control of the cutaneous circulation after acute and chronic local capsaicin J Appl Physiol, May 1, 2001; 90(5): 1860 - 1864. [Abstract] [Full Text] [PDF]
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C. G. Crandall and D. A. MacLean Cutaneous interstitial nitric oxide concentration does not increase during heat stress in humans J Appl Physiol, March 1, 2001; 90(3): 1020 - 1024. [Abstract] [Full Text] [PDF]
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S. Shastry, C. T. Minson, S. A. Wilson, N. M. Dietz, and M. J. Joyner Effects of atropine and L-NAME on cutaneous blood flow during body heating in humans J Appl Physiol, February 1, 2000; 88(2): 467 - 472. [Abstract] [Full Text] [PDF]
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N. Charkoudian, D. P. Stephens, K. C. Pirkle, W. A. Kosiba, and J. M. Johnson Influence of female reproductive hormones on local thermal control of skin blood flow J Appl Physiol, November 1, 1999; 87(5): 1719 - 1723. [Abstract] [Full Text] [PDF]
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