Human thermoregulatory responses during cold water immersion after artificially induced sunburn KENT B. PANDOLF, R. WILLIAM GANGE, WILLIAM A. LATZKA, IRVIN H. BLANK, ANDREW J. YOUNG, AND MICHAEL N. SAWKA US Army Research Institute of Environmental Medicine, Natick 01760-5007; and Wellman Laboratories of Photomedicine, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts 02114 Pandolf, Kent B., R. William Gange, William A. Latzka, Irvin H. Blank, Andrew J. Young, and Michael N. Sawka. Human thermoregulatory responsesduring cold water immersion after artificially induced sunburn. Am. J. Physiol. 262 (Regulatory Integrative Comp. Physiol. 31): R617-
R623, 1992.-Thermoregulatory responsesduring cold-water immersion (water temperature 22°C) were compared in 10 young men before as well as 24 h and 1 wk after twice the minimal erythemal doseof ultraviolet-B radiation that covered -885% of the body surface area. After 10 min of seatedrest in cold water, the men exercisedfor 50 min on a cycle ergometer (-51% of maximal aerobic power). Rectal temperature, regional and mean heat flow (hJ, mean skin temperature from five sites, and heart rate were measuredcontinuously for all volunteers while esophagealtemperature was measuredfor six subjects.Venous blood sampleswere collected before and after cold water immersion. The mean skin temperature was higher (P < 0.05) throughout the 60-min cold water exposureboth 24 h and 1 wk after sunburn comparedwith before sunburn. Mean h, was higher (P < 0.05) after 10 min resting immersion and during the first 10 min of exercisewhen 24 h postsunburn was comparedwith presunburn, with the difference attributed primarily to higher h, from the back and chest. While rectal temperature and heart rate did not differ between conditions, esophagealtemperature before immersion and throughout the 60 min of cold water immersionwashigher (P < 0.05) when 24 h postsunburn wascomparedwith presunburn. Plasmavolume increased (P < 0.05) after 1 wk postsunburn compared with presunburn,whereasplasmaprotein concentration wasreduced (P < 0.05). After exercisecortisol was greater (P c 0.05) 24 h postsunburn compared with either presunburn or 1 wk postsunburn. Rated perceived exertion and thermal sensation during the 60 min of cold water immersion did not differ betweenconditions. In conclusion,artificially induced sunburn impaired the ability of these men to vasoconstrict during cold water immersion, resulting in greater heat loss.These adverse thermoregulatory effects were still present 1 wk after sunburn when the associatederythema had disappeared. blood responses;exercise-cold stress; perceptual responses; physiological responses;temperature regulation; ultraviolet erythema; ultraviolet radiation SKIN DISORDERS such as miliaria rubra (heat rash) result in altered human thermoregulation and impaired exercise-heat tolerance (18, 19). Sunburn is a common skin injury and a skin disorder that results from exposure to ultraviolet (UV) radiation (UV-B, 280-320 nm). The UV-B radiation causes inflammation, which is accompanied by increased cutaneous blood flow and volume, and a higher skin temperature (14, 20, 31). The inflammatory erythema associated with sunburn suggests that UV-B radiation causes cutaneous vasodilation of the superficial blood vessels with a concomitant rise in thermal conduction. Although the microscopic changes and molecular
events of a sunburn on the skin are well described (5,9), the physiological consequences on human thermoregulation during exercise at the environmental extremes of heat and cold are not known. The companion paper (17) reports that artificially induced sunburn alters both the responsiveness and capacity of the damaged sweat gland unit during exercise in the heat. These data further suggest that mean skin temperature (Tsk), deep body temperatures and heart rate (HR) during exercise-heat exposure are not affected by sunburn. Because UV-B exposure causes the superficial cutaneous vasculature to dilate and may alter vasomotor control in the exposed skin (13), significant increased heat loss may accompany this vasodilation under the stress of cold exposure. Many sunburned individuals report feeling chilled, whereas their skin is often warm to the touch on physical examination. The purpose of this investigation is to examine human thermoregulatory responses during exercise-cold stress after artificially induced sunburn. We hypothesize that the UV-induced vasodilation and impairment of vasoconstrictor tone would increase heat loss from the body in sunburned individuals exposed to cold water immersion. Furthermore, it is hypothesized that the effects of sunburn during cold water immersion would be more pronounced 24 h rather than 1 wk after UV-B exposure. METHODS Subjects. The same 10 healthy Caucasianmen previously described(17) participated in theseexperimentsastest subjects after giving their informed consent. All experimentswere conducted in Massachusettsduring January, and all subjectswere unacclimatedto cold. Preliminary and two-MED
minimal erythemal dose (MED) determination exposure. The individual sensitivity testing to
UV-B radiation for determining MED wasreported previously (1,17). After determination of the individual MED, eachsubject wasexposedto twice the MED, which servedasthe experimental sunburn. Individual two-MED exposureswereaccomplished through the useof an Ultra-lite V4472-IV phototherapy chamber with the proceduresas reported in detail earlier (17). Protocol. Preliminary teststo determineeachvolunteer’spercent body fat and maximal aerobic power (VOW,,,) were describedin our companionpaper (17). After thesepreliminary tests, the men performed 50 min of cycling (-50% \jozmax) on a specially designedunderwater ergometer(25) while immersed to the neck in cold water (water temperature 22°C). A lo-min rest while seatedon the ergometerin cold water precededthe 50-min exerciseperiod. The cold water immersionexperiments were performed in a 36,000-liter pool that continuously circulated the water by air bubbled from the bottom. Before cold water immersion, all subjectsdressedin nylon swim suits and R617
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R618
THERMOREGULATION
IN COLD
sat quietly in a room maintained at an air temperature of -22°C. Subjects were prehydrated by drinking 400 ml of water during the 30 min before testing, but drinking was not allowed during the cold water experiments. All exercise sessions in the cold water were individually terminated, if necessary, by the predetermined end point of a rectal temperature (T,,) ~350°C. Each subject was always tested at the same time of day. This test protocol was completed 1 wk before the artificially induced sunburn, 24 h after the sunburn, and 1 wk after sunburn. Physiological and perceptual variables. Measurementsof oxygen uptake (l/min at standard temperature and pressure,dry) during the cold water experiments were made at the 5th, 30th, and 45th min of exposureusing an automated system (Sensormedics Horizon Metabolic Measurement Cart). During cold water exposure, metabolic rate was calculated from oxygen uptake and respiratory exchangeratio measurements. During the exercise-coldsessions,T,,, esophagealtemperature (T,,), and HR were determined as previously mentioned (17). Tsk and mean heat flow (h,) were obtained by skin temperature and heat flow measurementsfrom five thermistor sensor units (Concept Engineering, Old Saybrook, CT) securedto the skin of the chest, back, arm, thigh, and calf with the area weighting according to Stolwijk and Hardy (28). Thermistor sensorunits were covered with one layer of tape (Hy-tape, New York, NY). These units were calibrated by the factory with a stated accuracy of 5% of actual skin temperature and heat flow and spot calibrated for accuracy. Combined nonevaporative heat transfer (H) wascomputedas hJ(T,, - TJ. A thermistor placed -50 cm from the subject was used to monitor water temperature. All temperature and heat flow data were recorded continuously by a Zenith 286 data systemscomputer with averagevalues printed every 30 s. Rated perceived exertion (RPE) (16) and thermal sensation(TS) (32) were determined during the 5th, 30th, 45th, and 60th min of exposure. Blood analysis. Venousblood sampleswere obtained by venipuncture before and after each exposure to cold water immersion. The preexposureblood samplewas taken after 20 min of seatedrest on the cycle ergometerbefore immersionand the post-exposuresampleimmediately after the cycle ergometer was removed from the cold water. The cycle ergometer was mounted on an aluminum platform, which was raisedand lowered into the pool by an electronic hoist. Blood sampleswere immediately analyzed in triplicate for hematocrit, hemoglobin concentration, plasmaprotein content, and plasmaosmolality using techniques described earlier (17). The subjects’ plasma volumes(PVs) preexposureduring the presunburnexperiments were estimated from the equation of Retzlaff et al. (21). The other PVs were calculated by adjusting those values by the appropriate percent changein PV. Percent change in PV was calculatedfrom the appropriate hemoglobinand hematocrit values(7). Total circulating protein wascalculated from the product of PV and protein concentration. Cortisol was analyzed using a radioimmunoassaykit (Diagnostic Products) with the analysiscompleted on a gammacounter (Packard Instruments autogamma5000). Statistical analysis. The samestatistical analysespreviously described(17) wereusedto examinethesethermoregulatory and perceptual data. The 0.05 level of significance was chosen for these analyses. RESULTS
Each subject completed the entire 60-min exposure in cold water for all three experimental conditions. However, only six subjects volunteered for T,, measurements. Before each of the three cold water exposures, T,,, T,,, Tsk, h,, and H were measured in a room maintained at a constant temperature (ZZ”C, 50% relative humidity) with
WATER
AFTER
SUNBURN
Table 1. Comparison of thermoregulatory responses among presunburn, 24 h postsunburn and 1 wk postsunburn prior to cold- water immersion Presunburn 37.1 l&O.06 36.77t0.11* 32.71t0.18” 57.0t2.0* 13.2t0.8’
T re9 "C T_ es9 "C T_ sky "C hz, w/m2 H W.m-2.oC-1
24 h Postsunburn
37.10t0.08 37.16k0.12 33.54t0.23 68.2k1.9 2O.lk1.7
1 wk Postsunburn 37.09~0.05 36.95&O. 10 32.82&0.12-t 56.8+1.7t 13.4+0.6?
Glues are meansof:SE. Tre, rectal temperature;Tes,esophageal temperature;Tsk,meanskin temperature; h,, mean heat flow; H, combined nonevaporative heat transfer. * Significant difference (P < 0.05) between 24 h postsunburn and presunburn. t Significant difference (P < 0.05) between 24 h postsunburn and 1 wk postsunburn.
the mean &SE values presented in Table 1. Mean T,e did not differ (P > 0.05) among these three conditions before cold water immersion. In contrast, T,, was higher (P < 0.05) when compared 24 h postsunburn to presunburn. Furthermore, Tsk, h,, and H were higher (P < 0.05) when 24 h postsunburn was compared with either the presunburn or 1 wk postsunburn values. Metabolic rate did not differ (P > 0.05) during rest (5th min of cold water exposure) between presunburn and 24 h postsunburn; however, the 1 wk postsunburn value was lower (P < 0.05) compared with either the presunburn or 24 h postsunburn value [presunburn 269 t 24 (SE) W, 24 h postsunburn 287 t 34 W, 1 wk postsunburn 225 t 23 W]. The metabolic rate did not differ (P > 0.05) between conditions during exercise in cold water (30 min: presunburn 582 t 19 W, 24 h postsunburn 580 t 13 W, 1 wk postsunburn 579 t 14 W; 45 min: presunburn 581 t 14 W, 24 h postsunburn 582 t 15 W, 1 wk postsunburn 584 +- 14 W). The relative exercise intensity ( %Vo2 max) was constant (P > 0.05) during each of the three cold water exposures (presunburn 51.3 t 0.4%, 24 h postsunburn 51.3 t 0.4%, 1 wk postsunburn 51.4 t 0.5%). Figure 1 depicts the Tsk responses during the 60.min cold water exposures for the presunburn, 24 h postsunburn, and 1 wk postsunburn experiments. Time 0 for Fig. l-6 represents the measurement made during the first 30 OP 2; 5
Q 34.0 E z E z x C0 2 ib!
32.0 3o-o 28.0 26.0 24eo 22.0 20.0
One
I 0
I 10
I 20
I 30 TIME
40
I 50
week-post
. 60
(mid
Fig. 1. Comparison of mean skin temperature among presunburn, 24 h postsunburn, and 1 wk postsunburn during 60 min of cold water immersion. Values are means (n = 10). * Significant difference (P < 0.05) between 24 h postsunburn and presunburn. *** Significant difference (P < 0.05) between 1 wk postsunburn and presunburn.
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THERMOREGULATION
IN COLD
cu^ -c 5 8 i= s !? 800
600
400
10
20
30
40
TIME
(mid
50
60
1
++---
L 30
.800
i -Tao0
! 1
AFTER
three experimental conditions. Figure 3 showed that the back heat flow at 10, 20, and 30 min of immersion was higher (P < 0.05) when the 24 h postsunburn values were compared with either presunburn or 1 wk postsunburn values. Figure 4 illustrated that the chest heat flow was greater (P < 0.05) at 10 min of exposure when the 24 h postsunburn value was compared with either the presunburn or 1 wk postsunburn value. Back and chest heat flows at other times were not different (P > 0.05) among the three conditions. In addition, there were no differences (P > 0.05) between conditions in heat flow at the other sites (arm, thigh, and calf) during cold water immersion. Combined nonevaporative heat transfer (W rnB2 OC-l) at 0, 10, 20, and 30 min of immersion was higher (P < 0.05) when 24 h postsunburn values were compared with presunburn. In addition, H at 0, 10, and 20 min was higher (P < 0.05) when 24 h postsunburn values were compared with 1 wk postsunburn. For all three experimental conditions, H was higher (P < 0.05) when the 0-min value was compared with all succeeding lo-min interval values. Figure 5 compares the T,, responses for the three
600
l
-
2 600 i =
R619
SUNBURN
l
Fig. 2. Comparison of mean heat flow among presunburn, 24 h postsunburn, and 1 wk postsunburn during 60 min of cold water immersion. Values are means (n = 10). * Significant difference (P < 0.05) between 24 h postsunburn and presunburn. /q--i--!
WATER
400
2 m 200
lost .-post
10
20
30
TIME
40
50
60
(mid
Fig. 3. Comparison of back heat flow among presunburn, 24 h postsunburn, and 1 wk postsunburn during 60 min of cold water immersion. Values are means (n = 10). * Significant difference (P < 0.05) between 24 h postsunburn and presunburn. ** Significant difference (P < 0.05) between 24 h postsunburn and 1 wk postsunburn.
s of rest during cold water immersion. The Tsk throughout the 60 min of cold water immersion was higher (P < 0.05) when 24 h and 1 wk postsunburn values were compared with corresponding presunburn Tsk values. There were no differences (P > 0.05) between 24 h and 1 wk postsunburn throughout the 60 min of exposure. There was a decline (P < 0.05) in Tsk during the first 10 min (Oand lo-min values) of all three immersion experiments with no further changes between 20 and 60 min of immersion. Figure 2 presents the L, during the 60 min of cold water immersion for the three experimental conditions. The h, values at 10 and 20 min of cold water immersion during the 24 h postsunburn experiment were higher (P < 0.05) compared with corresponding values presunburn. Comparisons among the three conditions at other points in time during the 60-min exposure indicated no differences (P > 0.05). There was a decline (P < 0.05) in h, during the first 10 min for all three immersion experiments with no further changes between 20 and 60 min of immersion. Figures 3 and 4 display the heat flow from the back and chest sites during the 60-min cold water exposure for the
One
week-post
re-burn 0
10
20
30
40
TIME
(mid
50
60
Fig. 4. Comparison of chest heat flow among presunburn, 24 h postsunburn, and 1 wk postsunburn during 60 min of cold water immersion. Values are means (n = 10). * Significant difference (P < 0.05) between 24 h postsunburn and presunburn. ** Significant difference (P < 0.05) between 24 h postsunburn and 1 wk postsunburn.
0
10
Fig. 5. Comparison postsunburn, and immersion. Values 0.05) between 24 h
20
30
40
TIME
(mid
50
60
of esophageal temperature among presunburn, 24 h 1 wk postsunburn during 60 min of cold water are means (n = 6). * Significant differences (P < postsunburn and presunburn.
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R620
THERMOREGULATION .....** - ---
IN COLD WATER 14
Pm-burn 24 hr-post One week-post
AFTER SUNBURN m m 1-1
Pre- burn 24 hr-post One week-post
6 0.0
4
’
I
I
0
10
20 TIME
1
I
30
40
I
I
50
60
(min)
Fig. 6. Comparison of rectal temperature among presunburn, 24 h postsunburn, and 1 wk postsunburn during 60 min of cold water immersion. Values are means t SE (n = 10).
experimental conditions during the 60.min cold water exposure. The T,, throughout the 60 min of exposure was higher (P < 0.05) when the 24 h postsunburn values were compared with presunburn. The T,, measurements during the 1 wk postsunburn experiment were intermediate between but did not differ (P > 0.05) from presunburn or 24 h postsunburn values. In contrast to the T,, responses, T, did not differ (P > 0.05) among the three experimental conditions at any point in time throughout the 60-min cold water exposure (Fig. 6). There were no significant changes in T,, and T, across time during any of the three experimental conditions. HR during the 60-min cold water exposure generally did not differ (P > 0.05) among the three conditions. However, HR at 10 min was higher (P < 0.05) when compared 24 h postsunburn (87 & 4 beats/min) with either presunburn (80 t 4 beats/min) or 1 wk postsunburn (76 t 5 beats/min). After 10 min of cold water immersion, HR did not differ (P > 0.05) across time for any of these experimental conditions, averaging about 120 beats/min. Table 2 presents the PV, plasma protein (PP), total circulating protein, plasma osmolality, and cortisol concentration data from the three experimental conditions. There was no change (P > 0.05) in PV during exercisecold exposure presunburn or 24 h postsunburn, but 1 wk postsunburn the PV decreased by 7% (P < 0.05) during
5
30 TIME
60
45
(min)
Fig. 7. Comparison of rated perceived exertion among presunburn, 24 h postsunburn, and 1 wk postsunburn during 60 min of cold water immersion. Values are means t SE (n = 10).
cold water immersion. There were no changes (P > 0.05) in PP concentration during the exercise-cold exposure before or 24 h after the sunburn, but there was an increase (P < 0.05) in PP concentration during cold water immersion 1 wk postsunburn. Comparison of preimmersion PV indicated that 1 wk postsunburn, PV was increased by 10% (P < 0.05) over the presunburn and by 5% over the 24 h postsunburn values. Corresponding PP concentrations indicated a decrease (P < 0.05) at 1 wk postsunburn concomitant with the increase in PV compared with presunburn values. The total circulating protein and plasma osmolality values were not affected (P > 0.05) by sunburn or cold water exposure. While preimmersion cortisol did not differ (P > 0.05) between conditions, the postimmersion cortisol was higher (P < 0.05) for 24 h postsunburn compared with either the presunburn or 1 wk postsunburn values. Figures 7 and 8 present the RPE and TS values presunburn, 24 h postsunburn, and 1 wk postsunburn at the 5th, 3Oth, 45th, and 60th min of cold water exposure. None of the differences among these three conditions were significant for either RPE or TS at any of these points in time. However, RPE and TS were higher (P < 0.05) at 30,45, and 60 min compared with the 5-min value for all three experimental conditions. DISCUSSION
To our knowledge, the present study was the first to investigate the effects of artificially induced sunburn over
Table 2. Comparison of hematologic data among presunburn, 24 h postsunburn, and 1 wk postsunburn during cold-water immersion Post
Pre
Plasma volume, ml Plasma protein, g/100 ml Total circulating protein, g 285tl 288tlh 284tl Plasma osmolality, mosmol/kgH20 12.lt2.0f 15.0t1.7 Cortisol, pg/lOO ml 14.6t2.3 Values are means & SE for preexposure (Pre) and postexposure (Post) measured presunburn, Similar superscripts a-g indicate significant differences between values (P < 0.05). h P c 0.05 3,117&68” 8.0t0.2e 253t6
1 wk Postsunburn
24 h Postsunburn
Presunburn Pre
3,052A91Cyd 8.0&O. 1 246k7b
3,263k73b 7.8&O. 1 259t5
Post
3,155H3c 8.0tO. 1 25Ok7
Pre
3,426+7gayb 7.5kO.l” 257t4
Post
3,201+76dph 8.OkO. lh 254k6
286tl 286tl 289klh 16.8t 1.6f,g 13.7tl.2 13.6k1.78 24 h postsunburn, and 1 wk postsunburn (n = 10). vs. preexposure.
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THERMOREGULATION m m 0
IN COLD
Pre-burn 24 hr-post One week-post
Jl
5
60
TIME
(min)
Fig. 8. Comparison of thermal sensation among presunburn, sunburn, and 1 wk postsunburn during 60 min of cold water Values are means & SE (n = 10).
24 h postimmersion.
the whole body on human thermoregulation during exercise in cold water. The two-MED level for artificially induced sunburn used in the present study was characterized as a mild sunburn equivalent to 1 h of midday sun exposure during midsummer in certain north central areas of the United States such as Minneapolis, MN, and Bismarck, ND (6). Normally, humans immersed in cold water have been shown to exhibit rapid thermoregulatory adjustments including a prompt vasoconstriction of the cutaneous vasculature that increases insulation and preserves deep body temperature (29). We hypothesized that the cutaneous vasodilation, decreased vasomotor tone, and increased thermal conductance that have been observed in UV-B-damaged skin (8, 14, 20) would result in increased body heat loss in those sunburned during cold water immersion. Our findings supported this hypothesis. Twenty-four hours postsunburn, skin temperatures both in air before immersion and throughout the entire 60 min of cold water immersion were higher than corresponding values recorded before the sunburn. The elevated Tsk were still apparent 1 wk after the sunburn. Thus the effects of cutaneous vasodilation associated with sunburn erythema were not completely offset by the vasoconstrictor response elicited by cold water immersion even 1 wk after sunburn when no erythema was visible. This is consistent with the findings of Holti (13), who observed that 1 mo after UV-B exposure the irradiated skin sustained a higher skin temperature (-0.7O”C greater) during local application of cold compared with the nonirradiated skin. In addition, h, during the first 20 min of cold water immersion was higher 24 h postsunburn compared with presunburn. This indicated that the cutaneous vasoconstrictor response to cold itself was somewhat impaired. The primary areas of the body exhibiting the impaired cutaneous vasoconstrictor response to cold were the back and the chest, which we previously noted as having a slightly more pronounced inflammatory erythema after sunburn (17). It also should be noted that after 30 min of cold water immersion there were no dif-
WATER
AFTER
SUNBURN
R621
ferences in heat flow between these conditions; perhaps during this period the subcutaneous muscle shell constricted to increase insulation. Our young men also displayed higher T,, in air before and throughout the 60 min of immersion in cold water at 24 h postsunburn compared with presunburn. However, there were no significant differences in the corresponding T,, responses among the three experiments. At least three theoretical explanations can be postulated to explain the elevated T,, but unchanged T,, values 24 h postsunburn compared with presunburn. First, the chest cavity temperature as indicated by T,, may have been maintained at a higher level than other core areas such as the pelvis (rectum) during immersion in cold water. Next, the higher Tes values after sunburn might reflect warmer blood returning to the heart from the hotter (sunburned) skin. Alternatively, the inflammatory erythema of sunburn may be associated with the production of increased concentrations of prostaglandins (PGs) that caused the elevated T,,. The disparity between the T,, and T,, responses after sunburn was surprising but might be explained by several mechanisms. It is known that T,, is an approximation of central blood temperature because it is measured at a site where the heart and esophagus are in contact (4, 23, 26); however, T,, is obtained from a relatively poorly perfused body cavity (4,15,29). Other authors (30) have suggested that in cold water the pronounced sympathetic tone could have reduced blood flow to the pelvic vascular bed, which partitioned this region from the circulating heat input of arterial blood. As a result, the T,, responses observed during the present experiments might have reflected central circulatory blood temperature, whereas the T,, responses could have been more representative of the temperature of the tissues comprising the outer core or body shell. During cold water stress after sunburn, the insulation of the superficial shell (skin and subcutaneous fat) was probably decreased, which resulted in an increased reliance on the subcutaneous muscle shell for insulation. The thickening of the subcutaneous muscle shell would have caused the core to shrink and result in a reduced blood flow to the shell. As a result, central circulatory blood temperature would have been defended after sunburn (or increased slightly compared with presunburn) because of the smaller core and compartmentalization of the warm blood, whereas the outer core (pelvic or rectal area) would not have reflected this redistribution of blood flow. Others (23) have observed that, during experimentation where Tsk began at 32OC and was raised to 40°C and then lowered to 27.0°C through the use of a water-perfused garment, measurement of the temperature of the right atria1 blood followed the changes in Tsk while T,, did not. As mentioned above, T,, has been shown to be a good approximation of central blood temperature (4). Futhermore, T,, has been shown to better reflect central blood temperature (pulmonary artery and aortic arch) when directly compared with T,, both from a quantitative standpoint and also in terms of response time (26). Therefore the higher T,, observed in our experiments after sunburn may have reflected the warmer blood
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R622
THERMOREGULATION
IN COLD WATER
returning to the central core from the hotter skin compared with the presunburn condition. However, the greater heat loss that has been shown 24 h postsunburn during cold water immersion should have been expected to lower central core temperature particularly because metabolism was the same compared with presunburn. A third explanation for the higher T,, was that the artificially induced sunburn resulted in a fever. PG release has been associated with the inflammatory erythema associated with sunburn (5, 11). The PGs implicated in the production of the inflammatory erythema in human skin after sunburn included PGE2, PGF2,, and 12-HETE produced by keratinocytes, PGD2 from mast cells, and PG12 (prostacyclin) produced from endothelial cells (5, 11). Release of these PGs has been observed after UV-B exposure at MEDs ranging from one to four, and many have been shown to remain elevated for 24 h postsunburn (2,3,5, 10, 11, 12). Many of these PGs have been shown to be potent vasodilators in humans and, therefore, probably play a role in the development of sunburn erythema. In addition, PGs have been proposed to serve as neural mediators of the febrile response, the occurrence of which could have accounted for the elevated T,, observed 24 h postsunburn (27). However, because a febrile response would be expected to increase T,, as well as T,,, the first explanation presented appeared to be more plausible than the latter two. An unexpected finding was that PV progressively expanded over the 1 wk postsunburn. At 24 h postsunburn, there was a nonsignificant 5% expansion in PV, but at 1 wk postsunburn there was a significant 10% expansion. Because total circulating protein remained constant, the PV expansion was not oncotically mediated. We believed that the mechanism responsible for the hemodilution could have been the direct effect of the sunburn on the arterioles and venules in the cutaneous plexus. Because the venules lie superficial and the arterioles deeper in the skin (14), a greater amount of UV-B irradiation damage may have occurred involving the venules than arterioles. If the arterioles recovered their vasomotor tone before the venules, there might have been an increased precapillary-to-postcapillary resistance change across the cutaneous vasculature. As a result, there would have been a greater hydrostatic pressure drop across the sunburned skin’s cutaneous capillary beds, which would have favored increased fluid absorption and a PV expansion (24). In support of this hypothesis is the observation that the erythema, which was possibly caused by loss of arteriolar tone, had nearly disappeared by 48 h postsunburn. Finally, there was no evidence that the two-MED sunburn altered the capillary permeability to make it more “leaky” as the total circulating protein mass and plasma shifts were comparable between the three experimental conditions. Plasma cortisol concentration has been used as a stress indicator during cold exposure (22). In the present study, plasma cortisol levels were elevated after the exposure to cold water at 24 h postsunburn compared with either presunburn or 1 wk postsunburn. These findings suggested increased adrenocorticotropic activity representative of a classic physiological response to the combined
AFTER
SUNBURN
stress of acute sunburn and cold water immersion. These observations occurred during the period when heat loss from the body was greatest, which was during the experiment 24 h postsunburn. Although the perceptual responses (RPE and TS) for this study did not differ significantly after sunburn, they each presented some interesting new observations. The RPE during exercise showed a trend to be lower at 30 and 45 min of exposure when evaluated 24 h postsunburn during cold water immersion. Sensations associated with the active muscles and joints have been reported to influence RPE (16). The RPE may have been lower after sunburn because of the relief provided by cold water immersion to local muscular and joint discomfort associated with the cutaneous inflammatory erythema experienced by these subjects. Although TS has been shown to be influenced by Tsk (32)) the present findings suggested that alterations in Tsk associated with sunburn did not influence TS during exercise in cold water. In conclusion, these findings suggested that the degree of vasodilation before and during exercise in cold water was greater immediately after sunburn and remained greater for at least 1 wk. Our heat flow observations indicated that upon sudden immersion in cold water there was a blunted vasoconstrictor response persisting for the first 20 min of this 60-min cold water exposure. Thus our hypothesis that UV-B-induced vasodilation and impairment of vasoconstrictor tone could increase heat loss from the body during cold water immersion was supported. These observations were particularly noteworthy because the two-MED UV-B exposure used in our study induced a sunburn comparable to that experienced by only 1 h of exposure to midday summer sun in susceptible individuals. It was likely that greater impairments in thermoregulation would have been seen if more pronounced sunburn had been induced or longer cold water immersions had been studied. The authors gratefully acknowledge Edna R. Safran for expert preparation of the manuscript and Anne E. Allan, MD, and Jeffrey E. Falkel, PhD, for their scientific assistance. The views, opinions, and/or findings in this report are those of the authors and should not be construed as an official Department of the Army position, policy, or decision unless so designated by other official documentation. Investigators adhered to Army Regulation 70-25 and US Army Medical Research and Development Command Regulation 70-25 on Use of Volunteers in Research. Citations of commercial organizations and trade names in this report do not constitute an official Department of the Army endorsement or approval of the products or services of these organizations. Address for reprint requests: K. B. Pandolf, US Army Research Institute of Environmental Medicine, Natick, MA 017605007, Received 3 April 1991; accepted in final form 18 October 1991. REFERENCES Arbabi, L., R. W. Gange, and J. A. Parrish. skin from a single suberythemal dose of ultraviolet Invest.
Dermatol.
81: 78-82,
Recovery of radiation. J.
1983.
Barr, R. M., A. K. Black, A. I. Mallet, and M. W. Greaves. Levels of prostaglandins and arachidonic acid in UV-B irradiated human skin before and after topical application of benzyl-&&diacetoxybenzoate, a salicylic derivative. Prostaglandins Leukotrienes Med 9: 35-43, 1982. Black, A. K., C. N. Hensby, and M. W. Greaves. Increased levels of 6-oxo-PGF,, in human skin following ultraviolet B irradiation. Br. J. Clin. Phmmacol. 13: 351-354, 1980.
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THERMOREGULATION
IN COLD WATER
Brengelmann, G. L. Dilemma of body temperature measurements. In: Man in Stressful Environments: Thermal and Work Physiology, edited by K. Shiraki and M. K. Yousef. Springfield, IL: Thomas, 1987, p. 5-22. J., and V. A. DeLeo. Sunburn. Dermatol. Clin. 4: 5. Carvallo, 4.
181-187, 6.
Diffey, matology
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Clinical climatology. Photoder-
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Farr, P. M., and B. L. Diffey. human skin to ultraviolet radiation. 501-507,
The vascular response of Photochem.
Photobiol.
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1986.
Gilchrest, B. A., N. A. Soter, J. S. Stoff, and M. C. Mihm, Jr. The human sunburn reaction: histologic and biochemical studies. Am. Acad. Dermatol. 5: 411-422, 1981. 10. Granstein, R. D., and D. N. Sauder. Whole-body exposure to ultraviolet radiation results in increased serum interleukin- 1 activity in humans. Lymphokine Res. 6: 187-193, 1987. 11. Greaves, M. W. Ultraviolet erythema: Causes and consequences. Curr. Probl. Dermatol. 15: 18-24, 1986. 12. Hawk, J. L. M., A. K. Black, K. F. Jaenicke, R. M. Barr, N. A. Soter, A. I. Mallett, B. A. Gilchrest, C. N. Hensby, J. A. Parrish, and M. W. Greaves. Increased concentrations of arachidonic acid, prostaglandins Ez, DS, and 6-0x0-F1,,, and histamine in human skin following UVA irradiation. J. Invest. 9.
Dermatol.
80: 496-499,
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13. Holti, G. Measurements of the vascular responses in skin at various time intervals after damage with histamine and ultraviolet radiation. Clin. Sci. Lond. 14: 143-155, 1955. 14. Kelfkens, G., and J. C. van der Leun. Skin temperature changes after irradiation with UVB or UVC: Implications for the mechanism underlying ultraviolet erythema. Phys. Med. Biol. 34: 599-608,
1989.
15.
Minard,
D. Body heat content. In: Physiological and Behavioral Temperature Regulation, edited by J. D. Hardy, A. P. Gagge, and J. A. J. Stolwijk. Springfield, IL: Thomas, 1970, p. 345-357.
16.
Pandolf, K. B. Advances in the study and application of perceived exertion. In: Exercise and Sport Sciences Reviews, edited by R. L. Terjung. Philadelphia, PA: Franklin Institute, 1983, p.
17.
Pandolf, K. B., R. W. Gange, W. A. Latzka, I. H. Blank, K. K. Kraning II, and R. R. Gonzalez. Human thermoregulatory responses during heat exposure after artificially induced sunburn.
118-158.
Am.
J. Physiol.
262 (Regulatory
Integrative
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SUNBURN
R623
E. H. Munro, and R. F. 19. Pandolf, K. B., T. B. Griffin, Goldman. Heat intolerance as a function of percent of body surface involved with miliaria rubra. Am. J. Physiol. 239 (Regulatory Integrative Comp. Physiol. 8): R233-R240, 1980. 20 . Ramsay, C. A., and A. V. J. Challoner. Vascular changes in human skin after ultraviolet irradiation. Br. J. Dermatol. 94: 487493, 1976.
1984.
Dill, D. B., and D. L. Costill. Calculation of percentage changes in volumes of blood, plasma, and red cells in dehydration. J. Appl.
8.
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B. L., and 0. Larko.
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R610-R616, 1991. K. B., T. B. Griffin, E. H. Munro, and R. F. 18. Pandolf, Goldman. Persistence of impaired heat tolerance from artificially induced miliaria rubra. Am. J. Physiol. 239 (Regulatory Integrative Comp. Physiol. 8): R226-R232, 1980.
Retzlaff, J. A., W. N. Tauxe, J. M. Kiely, and C. F. Stroebel. Erythrocyte volume, plasma volume, and lean body mass in adult men and women. J. Hematol. 33: 649-661, 1969. 22. Rochelle, R. D., and S. M. Horvath. Thermoregulation in surfers and nonsurfers immersed in cold water. Undersea Biomed. 21.
Res. 5: 377-390,
1978.
and K. K. 23* Rowell, L. B., J. A. Murray, G. L. Brengelmann, Kraning II. Human cardiovascular adjustments to rapid changes in skin temperature during exercise. Circ. Res. 24: 711724, 1969.
24. Sawka, M. N. Body fluid responses and hypohydration during exercise-heat stress. In: Human Performance Physiology and Environmental Medicine at Terrestrial Extremes, edited by K. B. Pandolf, M. N. Sawka, and R. R. Gonzalez. Indianapolis, IN: Benchmark, 1988, p. 227-266. Y., B. A. Avellini, M. M. Toner, and K. B. 25. Shapiro, Pandolf. Modification of the Monark bicycle ergometer for underwater exercise. J. Appl. Physiol. 50: 679-683, 1981. 26. Shiraki, K., N. Konda, and S. Sagawa. Esophageal and tympanic temperature responses to core blood temperature changes during hyperthermia. J. Appl. Physiol. 61: 98-102, 1986. 27. Stitt, J. T. Prostaglandin E as the neural mediator of the febrile response. Yale J. Biol. Med. 59: 137-149, 1986. 28 Stolwijk, J. A. J., and J. D. Hardy. Control of body temperature. In: Handbook of Physiology. Reaction to Environmental Agents. Bethesda, MD: Am. Physiol. Sot., 1977, sect. 9, chapt. 4, p. 45-67. 2g Toner, M. M., and W. D. McArdle. Physiological adjustments ’ of man to the cold. In: Human Performance Physiology and Environmental Medicine at Terrestrial Extremes, edited by K. B. Pandolf, M. N. Sawka, and R. R. Gonzalez. Indianapolis, IN: Benchmark, 1988, p. 361-399. 3. . Toner, M. M., M. N. Sawka, W. L. Holden, and K. B. Pandolf. Comparison of thermal responses between rest and leg exercise in water. J. Appl. Physiol. 59: 248-253, 1985. Erythema: A Study of Diffusion 31. Van der Leun, J. C. Ultraviolet Processes in the Human Skin (PhD thesis). Utrecht, The Netherlands: University of Utrecht, 1966. 32. Young, A. J., M. N. Sawka, Y. Epstein, B. DeChristofano, and K. B. Pandolf. Cooling different body surfaces during upper and lower body exercise. J. Appl. Physiol. 63: 1218-1223, l
1987.
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R623, 1992.-Thermoregulatory responsesduring cold-water immersion (water temperature 22°C) were compared in 10 young men before as well as 24 h and 1 wk after twice the minimal erythemal doseof ultraviolet-B radiation that covered -885% of the body surface area. After 10 min of seatedrest in cold water, the men exercisedfor 50 min on a cycle ergometer (-51% of maximal aerobic power). Rectal temperature, regional and mean heat flow (hJ, mean skin temperature from five sites, and heart rate were measuredcontinuously for all volunteers while esophagealtemperature was measuredfor six subjects.Venous blood sampleswere collected before and after cold water immersion. The mean skin temperature was higher (P < 0.05) throughout the 60-min cold water exposureboth 24 h and 1 wk after sunburn comparedwith before sunburn. Mean h, was higher (P < 0.05) after 10 min resting immersion and during the first 10 min of exercisewhen 24 h postsunburn was comparedwith presunburn, with the difference attributed primarily to higher h, from the back and chest. While rectal temperature and heart rate did not differ between conditions, esophagealtemperature before immersion and throughout the 60 min of cold water immersionwashigher (P < 0.05) when 24 h postsunburn wascomparedwith presunburn. Plasmavolume increased (P < 0.05) after 1 wk postsunburn compared with presunburn,whereasplasmaprotein concentration wasreduced (P < 0.05). After exercisecortisol was greater (P c 0.05) 24 h postsunburn compared with either presunburn or 1 wk postsunburn. Rated perceived exertion and thermal sensation during the 60 min of cold water immersion did not differ betweenconditions. In conclusion,artificially induced sunburn impaired the ability of these men to vasoconstrict during cold water immersion, resulting in greater heat loss.These adverse thermoregulatory effects were still present 1 wk after sunburn when the associatederythema had disappeared. blood responses;exercise-cold stress; perceptual responses; physiological responses;temperature regulation; ultraviolet erythema; ultraviolet radiation SKIN DISORDERS such as miliaria rubra (heat rash) result in altered human thermoregulation and impaired exercise-heat tolerance (18, 19). Sunburn is a common skin injury and a skin disorder that results from exposure to ultraviolet (UV) radiation (UV-B, 280-320 nm). The UV-B radiation causes inflammation, which is accompanied by increased cutaneous blood flow and volume, and a higher skin temperature (14, 20, 31). The inflammatory erythema associated with sunburn suggests that UV-B radiation causes cutaneous vasodilation of the superficial blood vessels with a concomitant rise in thermal conduction. Although the microscopic changes and molecular
events of a sunburn on the skin are well described (5,9), the physiological consequences on human thermoregulation during exercise at the environmental extremes of heat and cold are not known. The companion paper (17) reports that artificially induced sunburn alters both the responsiveness and capacity of the damaged sweat gland unit during exercise in the heat. These data further suggest that mean skin temperature (Tsk), deep body temperatures and heart rate (HR) during exercise-heat exposure are not affected by sunburn. Because UV-B exposure causes the superficial cutaneous vasculature to dilate and may alter vasomotor control in the exposed skin (13), significant increased heat loss may accompany this vasodilation under the stress of cold exposure. Many sunburned individuals report feeling chilled, whereas their skin is often warm to the touch on physical examination. The purpose of this investigation is to examine human thermoregulatory responses during exercise-cold stress after artificially induced sunburn. We hypothesize that the UV-induced vasodilation and impairment of vasoconstrictor tone would increase heat loss from the body in sunburned individuals exposed to cold water immersion. Furthermore, it is hypothesized that the effects of sunburn during cold water immersion would be more pronounced 24 h rather than 1 wk after UV-B exposure. METHODS Subjects. The same 10 healthy Caucasianmen previously described(17) participated in theseexperimentsastest subjects after giving their informed consent. All experimentswere conducted in Massachusettsduring January, and all subjectswere unacclimatedto cold. Preliminary and two-MED
minimal erythemal dose (MED) determination exposure. The individual sensitivity testing to
UV-B radiation for determining MED wasreported previously (1,17). After determination of the individual MED, eachsubject wasexposedto twice the MED, which servedasthe experimental sunburn. Individual two-MED exposureswereaccomplished through the useof an Ultra-lite V4472-IV phototherapy chamber with the proceduresas reported in detail earlier (17). Protocol. Preliminary teststo determineeachvolunteer’spercent body fat and maximal aerobic power (VOW,,,) were describedin our companionpaper (17). After thesepreliminary tests, the men performed 50 min of cycling (-50% \jozmax) on a specially designedunderwater ergometer(25) while immersed to the neck in cold water (water temperature 22°C). A lo-min rest while seatedon the ergometerin cold water precededthe 50-min exerciseperiod. The cold water immersionexperiments were performed in a 36,000-liter pool that continuously circulated the water by air bubbled from the bottom. Before cold water immersion, all subjectsdressedin nylon swim suits and R617
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R618
THERMOREGULATION
IN COLD
sat quietly in a room maintained at an air temperature of -22°C. Subjects were prehydrated by drinking 400 ml of water during the 30 min before testing, but drinking was not allowed during the cold water experiments. All exercise sessions in the cold water were individually terminated, if necessary, by the predetermined end point of a rectal temperature (T,,) ~350°C. Each subject was always tested at the same time of day. This test protocol was completed 1 wk before the artificially induced sunburn, 24 h after the sunburn, and 1 wk after sunburn. Physiological and perceptual variables. Measurementsof oxygen uptake (l/min at standard temperature and pressure,dry) during the cold water experiments were made at the 5th, 30th, and 45th min of exposureusing an automated system (Sensormedics Horizon Metabolic Measurement Cart). During cold water exposure, metabolic rate was calculated from oxygen uptake and respiratory exchangeratio measurements. During the exercise-coldsessions,T,,, esophagealtemperature (T,,), and HR were determined as previously mentioned (17). Tsk and mean heat flow (h,) were obtained by skin temperature and heat flow measurementsfrom five thermistor sensor units (Concept Engineering, Old Saybrook, CT) securedto the skin of the chest, back, arm, thigh, and calf with the area weighting according to Stolwijk and Hardy (28). Thermistor sensorunits were covered with one layer of tape (Hy-tape, New York, NY). These units were calibrated by the factory with a stated accuracy of 5% of actual skin temperature and heat flow and spot calibrated for accuracy. Combined nonevaporative heat transfer (H) wascomputedas hJ(T,, - TJ. A thermistor placed -50 cm from the subject was used to monitor water temperature. All temperature and heat flow data were recorded continuously by a Zenith 286 data systemscomputer with averagevalues printed every 30 s. Rated perceived exertion (RPE) (16) and thermal sensation(TS) (32) were determined during the 5th, 30th, 45th, and 60th min of exposure. Blood analysis. Venousblood sampleswere obtained by venipuncture before and after each exposure to cold water immersion. The preexposureblood samplewas taken after 20 min of seatedrest on the cycle ergometerbefore immersionand the post-exposuresampleimmediately after the cycle ergometer was removed from the cold water. The cycle ergometer was mounted on an aluminum platform, which was raisedand lowered into the pool by an electronic hoist. Blood sampleswere immediately analyzed in triplicate for hematocrit, hemoglobin concentration, plasmaprotein content, and plasmaosmolality using techniques described earlier (17). The subjects’ plasma volumes(PVs) preexposureduring the presunburnexperiments were estimated from the equation of Retzlaff et al. (21). The other PVs were calculated by adjusting those values by the appropriate percent changein PV. Percent change in PV was calculatedfrom the appropriate hemoglobinand hematocrit values(7). Total circulating protein wascalculated from the product of PV and protein concentration. Cortisol was analyzed using a radioimmunoassaykit (Diagnostic Products) with the analysiscompleted on a gammacounter (Packard Instruments autogamma5000). Statistical analysis. The samestatistical analysespreviously described(17) wereusedto examinethesethermoregulatory and perceptual data. The 0.05 level of significance was chosen for these analyses. RESULTS
Each subject completed the entire 60-min exposure in cold water for all three experimental conditions. However, only six subjects volunteered for T,, measurements. Before each of the three cold water exposures, T,,, T,,, Tsk, h,, and H were measured in a room maintained at a constant temperature (ZZ”C, 50% relative humidity) with
WATER
AFTER
SUNBURN
Table 1. Comparison of thermoregulatory responses among presunburn, 24 h postsunburn and 1 wk postsunburn prior to cold- water immersion Presunburn 37.1 l&O.06 36.77t0.11* 32.71t0.18” 57.0t2.0* 13.2t0.8’
T re9 "C T_ es9 "C T_ sky "C hz, w/m2 H W.m-2.oC-1
24 h Postsunburn
37.10t0.08 37.16k0.12 33.54t0.23 68.2k1.9 2O.lk1.7
1 wk Postsunburn 37.09~0.05 36.95&O. 10 32.82&0.12-t 56.8+1.7t 13.4+0.6?
Glues are meansof:SE. Tre, rectal temperature;Tes,esophageal temperature;Tsk,meanskin temperature; h,, mean heat flow; H, combined nonevaporative heat transfer. * Significant difference (P < 0.05) between 24 h postsunburn and presunburn. t Significant difference (P < 0.05) between 24 h postsunburn and 1 wk postsunburn.
the mean &SE values presented in Table 1. Mean T,e did not differ (P > 0.05) among these three conditions before cold water immersion. In contrast, T,, was higher (P < 0.05) when compared 24 h postsunburn to presunburn. Furthermore, Tsk, h,, and H were higher (P < 0.05) when 24 h postsunburn was compared with either the presunburn or 1 wk postsunburn values. Metabolic rate did not differ (P > 0.05) during rest (5th min of cold water exposure) between presunburn and 24 h postsunburn; however, the 1 wk postsunburn value was lower (P < 0.05) compared with either the presunburn or 24 h postsunburn value [presunburn 269 t 24 (SE) W, 24 h postsunburn 287 t 34 W, 1 wk postsunburn 225 t 23 W]. The metabolic rate did not differ (P > 0.05) between conditions during exercise in cold water (30 min: presunburn 582 t 19 W, 24 h postsunburn 580 t 13 W, 1 wk postsunburn 579 t 14 W; 45 min: presunburn 581 t 14 W, 24 h postsunburn 582 t 15 W, 1 wk postsunburn 584 +- 14 W). The relative exercise intensity ( %Vo2 max) was constant (P > 0.05) during each of the three cold water exposures (presunburn 51.3 t 0.4%, 24 h postsunburn 51.3 t 0.4%, 1 wk postsunburn 51.4 t 0.5%). Figure 1 depicts the Tsk responses during the 60.min cold water exposures for the presunburn, 24 h postsunburn, and 1 wk postsunburn experiments. Time 0 for Fig. l-6 represents the measurement made during the first 30 OP 2; 5
Q 34.0 E z E z x C0 2 ib!
32.0 3o-o 28.0 26.0 24eo 22.0 20.0
One
I 0
I 10
I 20
I 30 TIME
40
I 50
week-post
. 60
(mid
Fig. 1. Comparison of mean skin temperature among presunburn, 24 h postsunburn, and 1 wk postsunburn during 60 min of cold water immersion. Values are means (n = 10). * Significant difference (P < 0.05) between 24 h postsunburn and presunburn. *** Significant difference (P < 0.05) between 1 wk postsunburn and presunburn.
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THERMOREGULATION
IN COLD
cu^ -c 5 8 i= s !? 800
600
400
10
20
30
40
TIME
(mid
50
60
1
++---
L 30
.800
i -Tao0
! 1
AFTER
three experimental conditions. Figure 3 showed that the back heat flow at 10, 20, and 30 min of immersion was higher (P < 0.05) when the 24 h postsunburn values were compared with either presunburn or 1 wk postsunburn values. Figure 4 illustrated that the chest heat flow was greater (P < 0.05) at 10 min of exposure when the 24 h postsunburn value was compared with either the presunburn or 1 wk postsunburn value. Back and chest heat flows at other times were not different (P > 0.05) among the three conditions. In addition, there were no differences (P > 0.05) between conditions in heat flow at the other sites (arm, thigh, and calf) during cold water immersion. Combined nonevaporative heat transfer (W rnB2 OC-l) at 0, 10, 20, and 30 min of immersion was higher (P < 0.05) when 24 h postsunburn values were compared with presunburn. In addition, H at 0, 10, and 20 min was higher (P < 0.05) when 24 h postsunburn values were compared with 1 wk postsunburn. For all three experimental conditions, H was higher (P < 0.05) when the 0-min value was compared with all succeeding lo-min interval values. Figure 5 compares the T,, responses for the three
600
l
-
2 600 i =
R619
SUNBURN
l
Fig. 2. Comparison of mean heat flow among presunburn, 24 h postsunburn, and 1 wk postsunburn during 60 min of cold water immersion. Values are means (n = 10). * Significant difference (P < 0.05) between 24 h postsunburn and presunburn. /q--i--!
WATER
400
2 m 200
lost .-post
10
20
30
TIME
40
50
60
(mid
Fig. 3. Comparison of back heat flow among presunburn, 24 h postsunburn, and 1 wk postsunburn during 60 min of cold water immersion. Values are means (n = 10). * Significant difference (P < 0.05) between 24 h postsunburn and presunburn. ** Significant difference (P < 0.05) between 24 h postsunburn and 1 wk postsunburn.
s of rest during cold water immersion. The Tsk throughout the 60 min of cold water immersion was higher (P < 0.05) when 24 h and 1 wk postsunburn values were compared with corresponding presunburn Tsk values. There were no differences (P > 0.05) between 24 h and 1 wk postsunburn throughout the 60 min of exposure. There was a decline (P < 0.05) in Tsk during the first 10 min (Oand lo-min values) of all three immersion experiments with no further changes between 20 and 60 min of immersion. Figure 2 presents the L, during the 60 min of cold water immersion for the three experimental conditions. The h, values at 10 and 20 min of cold water immersion during the 24 h postsunburn experiment were higher (P < 0.05) compared with corresponding values presunburn. Comparisons among the three conditions at other points in time during the 60-min exposure indicated no differences (P > 0.05). There was a decline (P < 0.05) in h, during the first 10 min for all three immersion experiments with no further changes between 20 and 60 min of immersion. Figures 3 and 4 display the heat flow from the back and chest sites during the 60-min cold water exposure for the
One
week-post
re-burn 0
10
20
30
40
TIME
(mid
50
60
Fig. 4. Comparison of chest heat flow among presunburn, 24 h postsunburn, and 1 wk postsunburn during 60 min of cold water immersion. Values are means (n = 10). * Significant difference (P < 0.05) between 24 h postsunburn and presunburn. ** Significant difference (P < 0.05) between 24 h postsunburn and 1 wk postsunburn.
0
10
Fig. 5. Comparison postsunburn, and immersion. Values 0.05) between 24 h
20
30
40
TIME
(mid
50
60
of esophageal temperature among presunburn, 24 h 1 wk postsunburn during 60 min of cold water are means (n = 6). * Significant differences (P < postsunburn and presunburn.
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R620
THERMOREGULATION .....** - ---
IN COLD WATER 14
Pm-burn 24 hr-post One week-post
AFTER SUNBURN m m 1-1
Pre- burn 24 hr-post One week-post
6 0.0
4
’
I
I
0
10
20 TIME
1
I
30
40
I
I
50
60
(min)
Fig. 6. Comparison of rectal temperature among presunburn, 24 h postsunburn, and 1 wk postsunburn during 60 min of cold water immersion. Values are means t SE (n = 10).
experimental conditions during the 60.min cold water exposure. The T,, throughout the 60 min of exposure was higher (P < 0.05) when the 24 h postsunburn values were compared with presunburn. The T,, measurements during the 1 wk postsunburn experiment were intermediate between but did not differ (P > 0.05) from presunburn or 24 h postsunburn values. In contrast to the T,, responses, T, did not differ (P > 0.05) among the three experimental conditions at any point in time throughout the 60-min cold water exposure (Fig. 6). There were no significant changes in T,, and T, across time during any of the three experimental conditions. HR during the 60-min cold water exposure generally did not differ (P > 0.05) among the three conditions. However, HR at 10 min was higher (P < 0.05) when compared 24 h postsunburn (87 & 4 beats/min) with either presunburn (80 t 4 beats/min) or 1 wk postsunburn (76 t 5 beats/min). After 10 min of cold water immersion, HR did not differ (P > 0.05) across time for any of these experimental conditions, averaging about 120 beats/min. Table 2 presents the PV, plasma protein (PP), total circulating protein, plasma osmolality, and cortisol concentration data from the three experimental conditions. There was no change (P > 0.05) in PV during exercisecold exposure presunburn or 24 h postsunburn, but 1 wk postsunburn the PV decreased by 7% (P < 0.05) during
5
30 TIME
60
45
(min)
Fig. 7. Comparison of rated perceived exertion among presunburn, 24 h postsunburn, and 1 wk postsunburn during 60 min of cold water immersion. Values are means t SE (n = 10).
cold water immersion. There were no changes (P > 0.05) in PP concentration during the exercise-cold exposure before or 24 h after the sunburn, but there was an increase (P < 0.05) in PP concentration during cold water immersion 1 wk postsunburn. Comparison of preimmersion PV indicated that 1 wk postsunburn, PV was increased by 10% (P < 0.05) over the presunburn and by 5% over the 24 h postsunburn values. Corresponding PP concentrations indicated a decrease (P < 0.05) at 1 wk postsunburn concomitant with the increase in PV compared with presunburn values. The total circulating protein and plasma osmolality values were not affected (P > 0.05) by sunburn or cold water exposure. While preimmersion cortisol did not differ (P > 0.05) between conditions, the postimmersion cortisol was higher (P < 0.05) for 24 h postsunburn compared with either the presunburn or 1 wk postsunburn values. Figures 7 and 8 present the RPE and TS values presunburn, 24 h postsunburn, and 1 wk postsunburn at the 5th, 3Oth, 45th, and 60th min of cold water exposure. None of the differences among these three conditions were significant for either RPE or TS at any of these points in time. However, RPE and TS were higher (P < 0.05) at 30,45, and 60 min compared with the 5-min value for all three experimental conditions. DISCUSSION
To our knowledge, the present study was the first to investigate the effects of artificially induced sunburn over
Table 2. Comparison of hematologic data among presunburn, 24 h postsunburn, and 1 wk postsunburn during cold-water immersion Post
Pre
Plasma volume, ml Plasma protein, g/100 ml Total circulating protein, g 285tl 288tlh 284tl Plasma osmolality, mosmol/kgH20 12.lt2.0f 15.0t1.7 Cortisol, pg/lOO ml 14.6t2.3 Values are means & SE for preexposure (Pre) and postexposure (Post) measured presunburn, Similar superscripts a-g indicate significant differences between values (P < 0.05). h P c 0.05 3,117&68” 8.0t0.2e 253t6
1 wk Postsunburn
24 h Postsunburn
Presunburn Pre
3,052A91Cyd 8.0&O. 1 246k7b
3,263k73b 7.8&O. 1 259t5
Post
3,155H3c 8.0tO. 1 25Ok7
Pre
3,426+7gayb 7.5kO.l” 257t4
Post
3,201+76dph 8.OkO. lh 254k6
286tl 286tl 289klh 16.8t 1.6f,g 13.7tl.2 13.6k1.78 24 h postsunburn, and 1 wk postsunburn (n = 10). vs. preexposure.
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THERMOREGULATION m m 0
IN COLD
Pre-burn 24 hr-post One week-post
Jl
5
60
TIME
(min)
Fig. 8. Comparison of thermal sensation among presunburn, sunburn, and 1 wk postsunburn during 60 min of cold water Values are means & SE (n = 10).
24 h postimmersion.
the whole body on human thermoregulation during exercise in cold water. The two-MED level for artificially induced sunburn used in the present study was characterized as a mild sunburn equivalent to 1 h of midday sun exposure during midsummer in certain north central areas of the United States such as Minneapolis, MN, and Bismarck, ND (6). Normally, humans immersed in cold water have been shown to exhibit rapid thermoregulatory adjustments including a prompt vasoconstriction of the cutaneous vasculature that increases insulation and preserves deep body temperature (29). We hypothesized that the cutaneous vasodilation, decreased vasomotor tone, and increased thermal conductance that have been observed in UV-B-damaged skin (8, 14, 20) would result in increased body heat loss in those sunburned during cold water immersion. Our findings supported this hypothesis. Twenty-four hours postsunburn, skin temperatures both in air before immersion and throughout the entire 60 min of cold water immersion were higher than corresponding values recorded before the sunburn. The elevated Tsk were still apparent 1 wk after the sunburn. Thus the effects of cutaneous vasodilation associated with sunburn erythema were not completely offset by the vasoconstrictor response elicited by cold water immersion even 1 wk after sunburn when no erythema was visible. This is consistent with the findings of Holti (13), who observed that 1 mo after UV-B exposure the irradiated skin sustained a higher skin temperature (-0.7O”C greater) during local application of cold compared with the nonirradiated skin. In addition, h, during the first 20 min of cold water immersion was higher 24 h postsunburn compared with presunburn. This indicated that the cutaneous vasoconstrictor response to cold itself was somewhat impaired. The primary areas of the body exhibiting the impaired cutaneous vasoconstrictor response to cold were the back and the chest, which we previously noted as having a slightly more pronounced inflammatory erythema after sunburn (17). It also should be noted that after 30 min of cold water immersion there were no dif-
WATER
AFTER
SUNBURN
R621
ferences in heat flow between these conditions; perhaps during this period the subcutaneous muscle shell constricted to increase insulation. Our young men also displayed higher T,, in air before and throughout the 60 min of immersion in cold water at 24 h postsunburn compared with presunburn. However, there were no significant differences in the corresponding T,, responses among the three experiments. At least three theoretical explanations can be postulated to explain the elevated T,, but unchanged T,, values 24 h postsunburn compared with presunburn. First, the chest cavity temperature as indicated by T,, may have been maintained at a higher level than other core areas such as the pelvis (rectum) during immersion in cold water. Next, the higher Tes values after sunburn might reflect warmer blood returning to the heart from the hotter (sunburned) skin. Alternatively, the inflammatory erythema of sunburn may be associated with the production of increased concentrations of prostaglandins (PGs) that caused the elevated T,,. The disparity between the T,, and T,, responses after sunburn was surprising but might be explained by several mechanisms. It is known that T,, is an approximation of central blood temperature because it is measured at a site where the heart and esophagus are in contact (4, 23, 26); however, T,, is obtained from a relatively poorly perfused body cavity (4,15,29). Other authors (30) have suggested that in cold water the pronounced sympathetic tone could have reduced blood flow to the pelvic vascular bed, which partitioned this region from the circulating heat input of arterial blood. As a result, the T,, responses observed during the present experiments might have reflected central circulatory blood temperature, whereas the T,, responses could have been more representative of the temperature of the tissues comprising the outer core or body shell. During cold water stress after sunburn, the insulation of the superficial shell (skin and subcutaneous fat) was probably decreased, which resulted in an increased reliance on the subcutaneous muscle shell for insulation. The thickening of the subcutaneous muscle shell would have caused the core to shrink and result in a reduced blood flow to the shell. As a result, central circulatory blood temperature would have been defended after sunburn (or increased slightly compared with presunburn) because of the smaller core and compartmentalization of the warm blood, whereas the outer core (pelvic or rectal area) would not have reflected this redistribution of blood flow. Others (23) have observed that, during experimentation where Tsk began at 32OC and was raised to 40°C and then lowered to 27.0°C through the use of a water-perfused garment, measurement of the temperature of the right atria1 blood followed the changes in Tsk while T,, did not. As mentioned above, T,, has been shown to be a good approximation of central blood temperature (4). Futhermore, T,, has been shown to better reflect central blood temperature (pulmonary artery and aortic arch) when directly compared with T,, both from a quantitative standpoint and also in terms of response time (26). Therefore the higher T,, observed in our experiments after sunburn may have reflected the warmer blood
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IN COLD WATER
returning to the central core from the hotter skin compared with the presunburn condition. However, the greater heat loss that has been shown 24 h postsunburn during cold water immersion should have been expected to lower central core temperature particularly because metabolism was the same compared with presunburn. A third explanation for the higher T,, was that the artificially induced sunburn resulted in a fever. PG release has been associated with the inflammatory erythema associated with sunburn (5, 11). The PGs implicated in the production of the inflammatory erythema in human skin after sunburn included PGE2, PGF2,, and 12-HETE produced by keratinocytes, PGD2 from mast cells, and PG12 (prostacyclin) produced from endothelial cells (5, 11). Release of these PGs has been observed after UV-B exposure at MEDs ranging from one to four, and many have been shown to remain elevated for 24 h postsunburn (2,3,5, 10, 11, 12). Many of these PGs have been shown to be potent vasodilators in humans and, therefore, probably play a role in the development of sunburn erythema. In addition, PGs have been proposed to serve as neural mediators of the febrile response, the occurrence of which could have accounted for the elevated T,, observed 24 h postsunburn (27). However, because a febrile response would be expected to increase T,, as well as T,,, the first explanation presented appeared to be more plausible than the latter two. An unexpected finding was that PV progressively expanded over the 1 wk postsunburn. At 24 h postsunburn, there was a nonsignificant 5% expansion in PV, but at 1 wk postsunburn there was a significant 10% expansion. Because total circulating protein remained constant, the PV expansion was not oncotically mediated. We believed that the mechanism responsible for the hemodilution could have been the direct effect of the sunburn on the arterioles and venules in the cutaneous plexus. Because the venules lie superficial and the arterioles deeper in the skin (14), a greater amount of UV-B irradiation damage may have occurred involving the venules than arterioles. If the arterioles recovered their vasomotor tone before the venules, there might have been an increased precapillary-to-postcapillary resistance change across the cutaneous vasculature. As a result, there would have been a greater hydrostatic pressure drop across the sunburned skin’s cutaneous capillary beds, which would have favored increased fluid absorption and a PV expansion (24). In support of this hypothesis is the observation that the erythema, which was possibly caused by loss of arteriolar tone, had nearly disappeared by 48 h postsunburn. Finally, there was no evidence that the two-MED sunburn altered the capillary permeability to make it more “leaky” as the total circulating protein mass and plasma shifts were comparable between the three experimental conditions. Plasma cortisol concentration has been used as a stress indicator during cold exposure (22). In the present study, plasma cortisol levels were elevated after the exposure to cold water at 24 h postsunburn compared with either presunburn or 1 wk postsunburn. These findings suggested increased adrenocorticotropic activity representative of a classic physiological response to the combined
AFTER
SUNBURN
stress of acute sunburn and cold water immersion. These observations occurred during the period when heat loss from the body was greatest, which was during the experiment 24 h postsunburn. Although the perceptual responses (RPE and TS) for this study did not differ significantly after sunburn, they each presented some interesting new observations. The RPE during exercise showed a trend to be lower at 30 and 45 min of exposure when evaluated 24 h postsunburn during cold water immersion. Sensations associated with the active muscles and joints have been reported to influence RPE (16). The RPE may have been lower after sunburn because of the relief provided by cold water immersion to local muscular and joint discomfort associated with the cutaneous inflammatory erythema experienced by these subjects. Although TS has been shown to be influenced by Tsk (32)) the present findings suggested that alterations in Tsk associated with sunburn did not influence TS during exercise in cold water. In conclusion, these findings suggested that the degree of vasodilation before and during exercise in cold water was greater immediately after sunburn and remained greater for at least 1 wk. Our heat flow observations indicated that upon sudden immersion in cold water there was a blunted vasoconstrictor response persisting for the first 20 min of this 60-min cold water exposure. Thus our hypothesis that UV-B-induced vasodilation and impairment of vasoconstrictor tone could increase heat loss from the body during cold water immersion was supported. These observations were particularly noteworthy because the two-MED UV-B exposure used in our study induced a sunburn comparable to that experienced by only 1 h of exposure to midday summer sun in susceptible individuals. It was likely that greater impairments in thermoregulation would have been seen if more pronounced sunburn had been induced or longer cold water immersions had been studied. The authors gratefully acknowledge Edna R. Safran for expert preparation of the manuscript and Anne E. Allan, MD, and Jeffrey E. Falkel, PhD, for their scientific assistance. The views, opinions, and/or findings in this report are those of the authors and should not be construed as an official Department of the Army position, policy, or decision unless so designated by other official documentation. Investigators adhered to Army Regulation 70-25 and US Army Medical Research and Development Command Regulation 70-25 on Use of Volunteers in Research. Citations of commercial organizations and trade names in this report do not constitute an official Department of the Army endorsement or approval of the products or services of these organizations. Address for reprint requests: K. B. Pandolf, US Army Research Institute of Environmental Medicine, Natick, MA 017605007, Received 3 April 1991; accepted in final form 18 October 1991. REFERENCES Arbabi, L., R. W. Gange, and J. A. Parrish. skin from a single suberythemal dose of ultraviolet Invest.
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