J Appl Physiol 98: 1334-1340, 2005.
First published December 3, 2004; doi:10.1152/japplphysiol.00859.2004
8750-7587/05 $8.00
Reproducibility of the cold-induced vasodilation response in the human finger
Catherine O'Brien
Thermal and Mountain Medicine Division, United States Army Research Institute of Environmental Medicine, Natick, Massachusetts
Submitted 9 August 2004
; accepted in final form 27 November 2004
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ABSTRACT
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Cold-induced vasodilation (CIVD) is a cyclic oscillation in blood flow that occurs in the extremities on cold exposure and that is likely associated with reduced risk of cold injury (e.g., frostbite) as well as improved manual dexterity and less pain while working in the cold. The CIVD response varies between individuals, but the within-subject reproducibility has not been adequately described. The purpose of this study was to quantify the within-subject variability in the CIVD response under standardized conditions. Twenty-one volunteers resting in a controlled environment (27°C) immersed the middle finger in warm water (42°C) for 15 min to standardize initial finger temperature and then in cold water (4°C; CWI) for 30 min, on five separate occasions. Skin temperature (Tf) and blood flow (laser-Doppler; expressed as percent change from warm-water peak) responses that describe CIVD were identified, including initial nadir reached during CWI, onset time of CIVD, initial apex during CIVD, time of that apex, and overall mean during CWI. Within-subject coefficient of variation for Tf across the five tests for the nail bed and pad, respectively, were as follows: nadir, 9 and 21%; onset, 18 and 19%; apex, 12 and 17%; apex time, 23 and 24%; mean 10 and 15%. For blood flow, these values were as follows: nadir 52 and 64%; onset, 6 and 5%; apex, 33 and 31%; apex time 9 and 8%; and mean 43 and 34%. Greater variability was found in the temperature response of the finger pad than the nail bed, but for blood flow the variability was similar between locations. Variability in onset and apex time between sites was similar for both temperature and blood flow responses. The reproducibility of the time course of CIVD suggests this methodology may be of value for further studies examining the mechanism of the response.
vasoconstriction; blood flow; laser-Doppler
COLD-INDUCED VASODILATION (CIVD) is a cyclic oscillation in blood flow on cold exposure that commonly occurs in the extremities (hands, feet) and in the face (cheeks, nose, and ears). The initial response to cold exposure is a sympathetically mediated peripheral vasoconstriction, resulting in reduced local tissue temperature. With continued cold exposure, this vasoconstriction may be interrupted, resulting in periods of vasodilation that correspond to an increase in tissue temperature. The vasodilation is typically transient, followed after several minutes by another vasoconstriction, and a characteristic cyclic pattern of increasing and decreasing blood flow may be displayed (15). By maintaining higher tissue temperatures, CIVD is associated with improved dexterity (9) and less pain (1, 10) when working in the cold, and it is also believed to have a protective role against peripheral cold injury (30).
Certain physiological factors have a dramatic effect on CIVD, such as whole body cooling, during which CIVD is blunted (6, 21), or peripheral cold acclimatization, which generally produces an earlier onset of CIVD and higher mean tissue temperatures (1, 12–14, 26). More subtle changes may be difficult to detect due to the variability in the response both between and within subjects. Limited data have been published on the reproducibility of the CIVD response. Yoshimura and Iida (32) evaluated temperature responses to 30-min ice-water finger immersion. Rather than comparing individual variables such as nadir temperature, onset of vasodilation and mean finger temperature, they calculated a "resistance index" based on a point system for each of these three variables according to whether the value was within ±1 standard deviation (SD) of the mean or outside that range. Although this resistance index was reproducible (32), the range used for point determination meant that a subject's response for any one variable could vary within 2 SDs without being reflected by a change in the index; therefore, the value of the index is restricted to characterizing individuals by broad categories of response. Their research did highlight many conditions that influence the magnitude of the CIVD response, such as time of day, recent food intake, recent exercise, ambient temperature, subject's body temperature, sleep deprivation, and fasting.
Meehan (17) compared responses to finger immersion in ice water in four subjects over 5–6 days and found mean nail bed temperature during the last 25 min of immersion to be within a range of ±0.6°C, and nadir temperature to be within a range of ±0.8°C. However, Meehan's subjects showed limited magnitude of CIVD, with mean finger temperature during the last 25 min of immersion only 
1°C higher than the nadir temperature, and several subjects showing no CIVD response at all (17). Daanen (5) examined temperature response in the fingertip of eight subjects during cold-water (6°C) hand immersion on three separate days and found within-subject standard deviations (SD) to be 0.7°C for the nadir [8% coefficient of variation (CV)] and 1.0°C for mean finger temperature (10% CV). Although this is greater variability than Meehan reported, the magnitude of CIVD elicited in Daanen's protocol was greater, with mean finger temperature 2°C higher than nadir temperature (5). Greater variability would be expected with larger fluctuations in blood flow. Daanen suggested the reproducibility may have been reduced by insufficient control over certain methodological factors, including body heat content, hand immersion depth, hand or body movement during the test, and physical activity before the test. Thus it could be expected that reproducibility would improve when these factors were better controlled.
The present study systematically evaluated the CIVD response under standard conditions, and it quantified both between- and within-subject variability in finger skin temperature and blood flow. It was anticipated that, compared with previous studies, reproducibility would be improved by controlling factors known to modify the response, including ambient temperature, time of day, posture, body heat content, recent exercise and food intake, and use of nicotine and alcohol. The data also establish norms for the CIVD response elicited by using similar methodology, and it will be useful for interpreting the physiological significance of differences observed under conditions in which vasomotor responses to cold are altered.
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METHODS
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Test volunteers.
Twenty-one individuals (19 men, 2 women) completed this study, which was approved by the United States Army Research Institute of Environmental Medicine Scientific and Human Use Review Committees. Written, informed consent was obtained from each subject who volunteered to participate after being informed of the purpose, experimental procedures, and known risks of the study. Investigators adhered to Army Regulation 70-25 and US Army Medical Research and Materiel Command Regulation 70-25 on the Use of Volunteers in Research.
The protocol used a repeated-measures design, with each subject completing five tests, with the exception of one female subject who only completed four tests due to a schedule conflict. Female volunteers were tested only during the early follicular phase (days 1–6) of their cycle when estrogen and progesterone levels are low to avoid confounding the CIVD data by skin blood flow changes that may occur due to fluctuations in the concentrations of these hormones across the menstrual cycle (2). Tests were scheduled 1 wk apart for male subjects, 1 mo apart for female subjects. Because core temperature is known to influence CIVD (21), five tests with core temperature within 0.2°C of the mean were used. Two subjects had to complete an additional test because the core temperature was out of this range on one of the original five tests; in one case the subject had symptoms of a cold, and in the other case the subject had slept poorly the night before.
Experimental conditions.
All CIVD tests were conducted at the same time of day, between 0700 and 0900, to avoid confounding effects of circadian-related variations in body temperature regulation. Test conditions were maintained at a constant temperature (27°C) and humidity (50% relative humidity) (4). Volunteers were instructed to refrain from alcohol intake and vigorous exercise for 24 h and from caffeine and tobacco usage for 12 h before each test. They did not eat breakfast the morning of a test. Before the first test, volunteers were familiarized with the instrumentation, body position, chamber environment, and water temperatures used for the tests. During the tests volunteers wore standardized clothing, consisting of shorts, T-shirt, shoes, and socks. They reclined in a semisupine posture and minimized movement and talking during the experiments.
On the morning of each test, the volunteer reported to the laboratory and was given 8 oz of fruit juice. The volunteer then placed a rectal probe (model ESO-1, Physiotemp Instruments, Clifton, NJ) 10 cm past the anal sphincter, or an esophageal probe (model RET-1, Physiotemp Instruments) to a depth of one-quarter of the subject's height for measurement of core temperature (25). The volunteer was allowed to choose which type of core temperature probe they would use; however, the same probe was thereafter used for all of their tests. Thermocouples (Concept Engineering, Old Saybrook, CT) were attached to four skin sites (calf, thigh, chest, triceps) for calculation of mean weighted skin temperature. A wire thermocouple (type T, 24 gauge, time constant <2 s) was attached with thin tape (Tegaderm, 3M, St. Paul, MN) in the groove alongside the nail bed, and another was placed on the pad of the middle finger of the immersion hand to measure skin temperature. Blood flow was measured by using infrared (780 nm) laser-Doppler flowmetry (MicroFlo DSP, Oxford Optronix, Oxford, UK). One submersible laser-Doppler probe (model MSP110T) was attached using double-sticking tape to the pad of the middle finger, immediately proximal to the finger crease, for measurement of skin blood flow, and a second laser-Doppler probe (model MSP310T) was attached to the dorsal aspect of the middle finger, immediately proximal to the base of the nail. A separate piece of tape was loosely placed around both probes to ensure security, and probe wires were attached to the back of the hand to provide strain relief. A finger blood pressure cuff was attached to the middle finger of the contralateral hand for continuous blood pressure measurement using photoplethysmography (Ohmeda 2300, Finapres). Both hands were positioned at the approximate level of the heart.
Data collection began after the volunteer was completely instrumented and had rested quietly for 15 min. The volunteer then immersed the middle finger to the middle phalanx in warm (42°C) water. This temperature was intended to abolish vasoconstriction, similarly to observations in forearm blood flow measurements (23) and to standardize initial finger temperature before cold water finger immersion. After 15 min in warm water, the volunteer immediately transferred the finger to a cold (4°C) water bath for 30 min. Volunteers were asked to rate their finger pain each minute for the first 10 min of cold-water immersion (CWI) using a continuous pain scale (7) with anchors of "no pain at all" and "intolerable pain" (representing 100%), and pain was expressed as a percentage of maximum. Temperatures, skin blood flow, and blood pressure were recorded every 6 s. At the end of the immersion period, the volunteer withdrew the finger, and instrumentation was removed.
Measurements and calculations.
Mean skin temperature was calculated according to the weighting 0.20·(calf + thigh) + 0.3·(chest + triceps) (20). Mean arterial pressure (MAP) was calculated as ·(systolic – diastolic) + diastolic pressure. Laser-Doppler flow was used as an index of skin blood flow, and cutaneous vascular conductance (CVC; mV/mmHg) was calculated as the ratio of skin blood flow (mV) to MAP (mmHg) (23). Relative blood flow response is expressed as the percent change in CVC from peak CVC elicited during warm-water immersion (WWI) (representing 100%).
Statistical analysis.
Reproducibility of the CIVD test was assessed by examining within-subject variability for each of the following variables across the five separate CIVD tests: temperature at the first nadir, onset time of CIVD, temperature at the next apex, the time of apex temperature, and average finger skin temperature during CWI (see Fig. 1). For comparison to previous studies, the average finger skin temperature between 5 and 30 min of CWI is also presented. A three-point running average was used to smooth temperature data before identifying CIVD variables using a change of 0.5°C as the criterion. Equivalent variables were identified for CVC response after Loess curve fitting was used to smooth CVC data (Microsoft Excel: nearest neighbors, 100 intervals, 0.1-sampling proportion, 5th-order polynomial). An analysis of variance with repeated measures (StatSoft Statistica) was used to determine whether there were any significant (P < 0.05) main or interactive effects across tests, and Tukey's honestly significant difference post hoc analysis was applied when significant differences were found (22). The P values presented are formain effects, with post hoc P values presented only when they were notably different from the main effect P value. For each variable, data are presented for within-subject SD and %CV across the five tests. Overall mean and between-subjects SD are also calculated based on data from all five tests. A CV of 10% or less is suggested to represent "good" reproducibility.
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Fig. 1. Schematic of the variables identified for cold-induced vasodilation (CIVD) analysis are shown using data from the finger pad of subject 18. Top solid line represents finger pad skin temperature and uses the right-hand axis. Cutaneous vascular conductance is shown in gray, with the Loess smoothing curve superimposed, both using the left-hand axis. Warm-water immersion (WWI) of 15 min is followed by 30-min cold-water immersion. Variables of interest include initial nadir temperature achieved on cold-water immersion, the onset time of cold-induced vasodilation, the subsequent apex temperature, and the time of the apex temperature. For cutaneous vascular conductance, in addition to those variables, the peak value during WWI is identified.
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RESULTS
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Mean core temperature across the five tests was 36.7°C, between-subject SD 0.2°C, within-subject SD 0.1°C, and CV 3%. Mean skin temperature across tests was 33.3°C, between-subject SD 0.5°C, and within-subject SD 0.3°C, and CV 0.8%. Mean skin temperature was 0.3°C lower (P = 0.021) on test 5 (33.1°C), compared with test 1 (33.4°C). Mean heart rate across the five tests was 63 beats/min, between-subject SD 8 beats/min, within-subject SD 3 beats/min, and CV 5%. Heart rate was lower (P = 0.003) on test 5 (60 beats/min), compared with test 1 (65 beats/min), test 2 (63 beats/min), test 3 (63 beats/min) and test 4 (63 beats/min). During CWI, mean MAP was 85 mmHg, with between-subject SD 7 mmHg, within-subject SD 5 mmHg, and CV 6%. There was no difference in MAP across tests (P = 0.760); however, MAP was 2–4 mmHg higher (P = 0.001) during CWI than during WWI.
The average responses of conductance and skin temperature for all subjects on each of the five tests are shown on Fig. 2 for the nail bed and Fig. 3 for the pad. Because the peak, nadir, and apex conductance and skin temperatures did not occur at the same time for all subjects, those values are dampened by the effect of averaging all subjects together on the graphs. There were no differences between tests for any CIVD variable in either nail bed or pad skin temperature, with the exception of the apex temperature achieved in the pad (P = 0.051), which was higher on test 3 (18.65), compared with test 1 (15.96°C) (post hoc P = 0.027). Skin temperature data for the CIVD variables are shown in Table 1. Mean skin temperature calculated over the last 25 min of CWI is included for comparison to previous studies (eg. Refs. 16, 17, 27, 28, 32) that excluded the initial fall in skin temperature on CWI from their calculations.
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Fig. 2. Nail bed cutaneous vascular conductance expressed as percent change from peak during WWI (top) and finger skin temperature (bottom) averaged over all subjects on each of the 5 tests. Pain ratings obtained during the first 10 min of cold water immersion and averaged across trials are shown at bottom using the scale on the right-hand axis (see text for statistical analysis).
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The nail bed and pad CVC data are shown on Table 2. In the nail bed, peak CVC during WWI was higher (P = 0.028) on test 2 (3.29 mV/mmHg), compared with test 3 (2.50 mV/mmHg, post hoc P = 0.050). No differences were found across tests for peak CVC in the finger pad, and there were no differences across tests in either site for mean values during WWI or CWI. In the finger pad, there was an earlier onset of vasodilation (P = 0.017) as measured by CVC on test 1 (2.6 min), compared with tests 4 and 5 (both 3.6 min, post hoc P = 0.051), and a higher apex (P = 0.014) in relative CVC on test 5 (87%), compared with tests 1 (59%) and 2 (56%) (Fig. 3). There were no differences across tests for any other CIVD variable in the finger nail bed or pad as described by percent change in CVC from WWI.
Pain ratings varied widely, with six subjects reporting no pain at all during any test. For the remaining subjects, there was a significant main effect for tests (P = 0.009), where average pain on test 1 (37% of maximum) was greater than on test 2 or test 4 (both 28% of maximum). There was also a significant time effect (P = 0.000), where pain at minute 4 was higher than at minutes 7–10 (Fig. 2, bottom). At minute 4, mean pain was 45% of maximum, between-subjects SD 25% of maximum, within subject SD 12% of maximum, and within-subjects CV 48%.
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DISCUSSION
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This was the first study to evaluate the day-to-day reproducibility of both skin temperature and blood flow responses during CIVD induced by cold-water finger immersion. Factors known to influence skin blood flow and the CIVD response were carefully controlled. The results characterize the CIVD response in both the finger nail bed and pad, and they describe the day-to-day variability between and within subjects. The main findings from this study are 1) reproducibility of skin temperature during CIVD was better in the nail bed (nadir: 9% CV; apex: 12% CV) than in the pad (nadir: 21% CV; apex: 17% CV); 2) onset and apex times for the skin temperature response were similar in the nail bed and pad, but their reproducibility was poor (onset: 18–19% CV; apex: 23–24% CV); 3) onset and apex times associated with nadir and apex CVC during the CIVD response had good reproducibility in both sites (onset: 5–6% CV; apex time: 8–9% CV); and 4) the magnitude of CVC, expressed as percent of peak during WWI, was similar between nail bed and pad for nadir, apex, and overall mean, but it had poor reproducibility (31–64% CV).
Daanen (5) measured reproducibility of finger temperature responses (measured at the fingertip) and mean blood flow during hand immersion in cold (6°C) water, and he reported within-subject CV for nadir, apex and mean temperatures of 8, 11, and 10%, respectively, and 13% for onset time. These values are similar to what was measured for temperatures of the nail bed in the present study, but they are lower than the reproducibility obtained for onset time in the nail bed or for temperature response in the finger pad. The protocol used to induce CIVD affects both the magnitude and time course of the response. In the present study, single-finger immersion in 4°C water was chosen as a model that was cold enough to reliably elicit CIVD without being too painful for the volunteers. Daanen's protocol of whole hand immersion (analogous to the cold pressor test) produces a greater sympathetic response and delayed CIVD with lower finger temperatures, compared with single-finger immersion (28). Daanen reports an onset of CIVD (6.9 min) that was later than the present study (4.5 min), and an amplitude (3.4°C) that was similar to that of the nail bed (3.6°C) in the present study but much lower than the finger pad (9.2°C). The greater sympathetic stimulus of whole hand immersion may result in reduced variability compared with single finger immersion. Indeed, Sendowski et al. (27) showed that between-subject variability in finger temperature variables was twice as great during single-finger immersion as during whole hand immersion.
Differences in CIVD response and reproducibility could also be due to measurement site. Higher blood flow and skin temperature in the finger pad, yet a similar time course of response in the nail bed, suggest that structural morphology could be a factor. Arteriovenous anastomoses (AVA) are prevalent in the fingertip, nail bed, and pad, but not in the dorsal finger (8), and the location of the nail bed Doppler probe (just proximal to the nail bed) may have been in a region of few AVAs compared with the pad. Central control of AVAs results in synchronous opening and closing (3); thus the similar pattern of blood flow response between nail bed and pad in 50% of the subjects (see Fig. 4) could support a role for AVAs in the CIVD response. Unfortunately, the laser-Doppler method used to assess blood flow does not discriminate between AVA and capillary blood flow. The most reproducible measure in the present study was the time course of blood flow response during CIVD (onset and apex times), which, along with the similarity between nail bed and pad, suggests central control, whereas the variability in the magnitude of the response may reflect influence of local factors, particularly because there are numerous mechanistic differences in control of blood flow between glabrous and nonglabrous skin. Placement of the laser-Doppler probe could also be a factor in this variability, because small variations in location could move the probe into a region with a different density or depth of blood vessels (11). This may also explain why reproducibility was poorer for blood flow than for skin temperature.
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Fig. 4. Example of classic hunting response in both the nail bed (top) and pad (bottom) of subject 6 during 1 test. The period and relative amplitude are very similar between the 2 skin sensor locations. Absolute cutaneous vascular conductance values are shown in light gray, with the smoothing effect of the Loess transformation superimposed. Finger skin temperature is also shown, using the right-hand axis.
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In addition to being sensitive to probe location, skin blood flow as assessed by laser-Doppler has the disadvantage of not quantifying absolute flow. Therefore, relative change in blood flow is calculated from a theoretically stable value, which in this study was chosen to be the peak temperature elicited during WWI. Although it was expected that maximal vasodilation would be achieved with the rapid tissue heating of immersing the finger in warm water, finger blood flow did not achieve steady state, but more typically it peaked at 6 min of immersion (Table 2). In the forearm, local heating has been shown to produce a biphasic increase in blood flow, with an initial vasodilation that is attributed to axon reflexes and peaks within a few minutes, followed, after a brief nadir, by a secondary vasodilation that is dependent on nitric oxide (19). It is not clear whether blood flow in the finger would have exhibited a similar response had the WWI been longer, nor is there evidence to suggest that a later peak would have been more reproducible. For characterizing within-subject variability, both absolute and relative blood flow yielded similar results in the present study, suggesting that any improvement in reproducibility during WWI may not have notable effect on reproducibility of blood flow during CWI.
The procedure of WWI was also intended to standardize finger temperature before CWI. Enander (7) noted wide variability in baseline finger temperature in subjects who rested quietly for 60 min, and baseline finger temperature was negatively correlated to the rate of finger cooling during cold-air exposure. Although WWI standardized finger temperatures, local tissue heating may have masked subtle differences in body thermic state or local vasomotor function. In a thermoneutral environment, Raynaud's patients have similar mean skin temperatures, but lower finger temperatures (24) and higher norepinephrine levels (31), compared with controls. Clearly such differences in sympathetic control between subjects are important and would be expected to affect the CIVD response during CWI, but they would not be observed during WWI. Therefore, a need remains for a method of standardizing initial finger temperature that is reproducible within subjects.
Patterns of response have been described by several investigators (7, 16, 18, 29) but generally fall into three categories: no CIVD; classic hunting response (Fig. 4); and "proportional control," which is an sustained temperature after the first CIVD (Fig. 5, bottom). In the present study, 30% of subjects showed proportional control, and the remaining 70% had more of a classic hunting response, with varying period. It is possible that the subjects with a response described as proportional control simply had a period that was longer than 25 min, such that the next nadir did not appear within the 30-min CWI measurement period. An interesting observation was that the variability in the CIVD response across tests for each subject was not due to a change in the pattern of response, but was due to a shift in period and/or amplitude. For example, Fig. 5, top, shows a classic hunting response on test 1, the period then varies across the tests, and on test 5 the temperature is sustained for the second half of CWI. Sensitivity of the vasoconstrictor response and factors that modulate the response may influence the individual variability in the pattern of response.
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Fig. 5. Top: example of classic hunting response in subject 6 which shows shifts in both amplitude and period over the 5 tests. Bottom: example of "proportional control" in subject 1 which shows similar period, but changes in amplitude.
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There was some evidence to suggest there may have been an effect of familiarization after the first test. Mean skin temperature was 0.3°C lower on test 5, compared with test 1. Heart rate was also lower (3–4 beats/min) on test 5, compared with tests 1, 2, and 4. In the finger pad, apex temperature was lower on test 1 (15.96°C) than on test 3 (18.65°C), apex CVC was higher on test 5 (87.3% WWI) compared with test 1 (58.7%) and test 2 (56.4%), and onset of CVC occurred later on tests 4 and 5 (3.6 min), compared with test 1 (2.6 min). Acclimatization is typically associated with a higher nadir, earlier onset, and higher apex (1); therefore, the higher pad apex CVC on test 5 could reflect acclimatization, but the delayed onset time would not. Acclimatization has been demonstrated in subjects who immersed their finger in ice water for 20 min 4 times per day for a month but not in those who only completed two immersions per day (1); thus it seemed unlikely that any acclimatization would occur with a single 30-min immersion once per week. That nearly all the significant differences found in the present study involved test 1 compared with other tests suggests familiarization should be considered when conducting studies involving repeated cold-water finger immersion.
This study has demonstrated that, under well-controlled conditions, finger skin temperatures (i.e., nadir, apex, and mean) are reproducible in the nail bed, but not in the pad, and that the time course of the CIVD response (i.e., onset and apex time) is reproducible for blood flow but not skin temperature. Identifying treatments or conditions that enhance the CIVD response is of interest for improving thermal comfort, manual dexterity, and risk of cold injury in people who work in the cold and is also important for individuals with Raynaud's phenomenon who experience a severe and painful vasoconstriction even with very mild cold exposure. However, the ability to detect differences is hindered by the poor reproducibility, and further improvements in reproducibility do not seem likely without a better understanding of the mechanisms involved. The most reproducible characteristic of the CIVD response in the present study was the time course of the blood flow response. This is important, because timely administration of vasodilator or vasoconstrictor substances or receptor agonist or antagonist substances represents one approach that could be used.
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DISCLOSURES
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The views, opinions and/or findings contained in this publication are those of the author(s) and should not be construed as an official Department of the Army position, policy or decision unless so designated by other documentation. The investigators have adhered to the policies for the protection of human subjects as prescribed in Army Regulation 70-25, and the research was conducted in adherence with the provisions of 45 CFR Part 46.
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FOOTNOTES
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Address for reprint requests and other correspondence: C. O'Brien, Thermal and Mountain Medicine Div., U.S. Army Research Institute of Environmental Medicine Natick, MA 01760-5007 (E-mail: kate.obrien{at}us.army.mil)
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.
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K.J.S. Anand MBBS DPhil
Analgesia for skin-breaking procedures in newborns and children: What works best?
Can. Med. Assoc. J.,
July 1, 2008;
179(1):
11 - 12.
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Copyright © 2005 by the American Physiological Society.
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ABSTRACT
METHODS
P = 0.030, apex cutaneous vascular conductance test 1 vs. test 5; and P = 0.015, test 2 vs. test 5. 
P = 0.027, apex temperature test 1 vs. test 3.