13
ORIGINAL ARTICLE Blood pressure and thermal responses to repeated whole body cold exposure: effect of winter clothing Yue Li Hisham Alshaer Geoff Fernie Accepted: 13 August 2009 / Published online: 29 August 2009 Ó Springer-Verlag 2009 Abstract The effect of outdoor clothing and repeated cold exposure on blood pressure, heart rate, skin temperature, and thermal sensation was studied in 16 young (18–34 years) and 8 middle-aged (35–51 years) normotensive participants. Four winter clothing ensembles were used: regular winter clothing without a hat, with a hat, with an extra pair of pants, and with a hat and an extra pair of pants. The participants were exposed four times to -5°C for 15 min wearing dif- ferent clothing ensembles in counterbalanced order and each cold exposure was followed by 25 min of rewarming at 25°C. The results showed that systolic and diastolic blood pressure increased in cold and increased more when a hat was not used. Wearing hats not only reduced the blood pressure response during cold exposure, but also promoted faster recovery of forehead skin temperature and blood pressure. These findings are encouraging and warrant further investigations to better understand the benefits of wearing appropriate clothing in the winter, especially among older people and patients with cardiovascular diseases. Keywords Winter Cold exposure Blood pressure Skin temperature Hat Warm clothing Introduction It is well known that an increase in mortality is associated with exposure to low outdoor temperatures, primarily due to cardiovascular diseases, in particular from myocardial infarction and stroke (Marchant et al. 1993; Na ¨yha ¨ 2002; Schneider et al. 2008). Though the associations between cardiovascular diseases and temperature are well docu- mented, the underlying mechanisms behind these associa- tions are in general not very well understood. One mechanism could be that these exposures act on the car- diovascular system by elevating blood pressure. Cold exposure is known to increase blood pressure by activation of the sympathetic nervous system (Young 1996). Since elevated blood pressure is a major risk factor for a range of cardiovascular diseases (Jackson et al. 2005; Kim et al. 2003), it seems reasonable to explore how environmental exposure affects blood pressure both experimentally and on the population level. The results of several large population studies of the effects of the season and temperature on systolic blood pressure show strong, statistically significant effects for both factors (Madsen and Nafstad 2006). The effect of season, however, disappeared in a model that also con- tained outdoor temperature, which suggests that a major component of the seasonal change in blood pressure, and hence cardiovascular disease risk, is due to temperature (Barnett et al. 2007). Improvements in central indoor heating are not consistently associated with a reduction in seasonal differences in mortality from cardiovascular dis- ease (Keatinge et al. 1989; Wilkinson et al. 2004; Barnett et al. 2005). Therefore, Keatinge et al. (1989, 1997) place more emphasis on personal behaviors and have argued that many excess winter mortalities are related to exposure to cold from ‘‘brief excursions outdoors rather than to low indoor temperatures’’. A study by Perez-Lloret et al. (2006) contributed further supporting evidence that seasonal dif- ferences in blood pressure do exist, but are largely confined to the daytime. Causative mechanisms, such as the time Y. Li (&) H. Alshaer G. Fernie iDAPT Technology R&D Team, Toronto Rehabilitation Institute, 550 University Avenue, Toronto, ON M5G 2A2, Canada e-mail: [email protected] 123 Eur J Appl Physiol (2009) 107:673–685 DOI 10.1007/s00421-009-1176-5

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Page 1: Blood pressure and thermal responses to repeated whole body cold exposure: effect of winter clothing

ORIGINAL ARTICLE

Blood pressure and thermal responses to repeated whole bodycold exposure: effect of winter clothing

Yue Li Æ Hisham Alshaer Æ Geoff Fernie

Accepted: 13 August 2009 / Published online: 29 August 2009

� Springer-Verlag 2009

Abstract The effect of outdoor clothing and repeated cold

exposure on blood pressure, heart rate, skin temperature, and

thermal sensation was studied in 16 young (18–34 years)

and 8 middle-aged (35–51 years) normotensive participants.

Four winter clothing ensembles were used: regular winter

clothing without a hat, with a hat, with an extra pair of pants,

and with a hat and an extra pair of pants. The participants

were exposed four times to -5�C for 15 min wearing dif-

ferent clothing ensembles in counterbalanced order and each

cold exposure was followed by 25 min of rewarming at

25�C. The results showed that systolic and diastolic blood

pressure increased in cold and increased more when a hat

was not used. Wearing hats not only reduced the blood

pressure response during cold exposure, but also promoted

faster recovery of forehead skin temperature and blood

pressure. These findings are encouraging and warrant further

investigations to better understand the benefits of wearing

appropriate clothing in the winter, especially among older

people and patients with cardiovascular diseases.

Keywords Winter � Cold exposure � Blood pressure �Skin temperature � Hat � Warm clothing

Introduction

It is well known that an increase in mortality is associated

with exposure to low outdoor temperatures, primarily due

to cardiovascular diseases, in particular from myocardial

infarction and stroke (Marchant et al. 1993; Nayha 2002;

Schneider et al. 2008). Though the associations between

cardiovascular diseases and temperature are well docu-

mented, the underlying mechanisms behind these associa-

tions are in general not very well understood. One

mechanism could be that these exposures act on the car-

diovascular system by elevating blood pressure. Cold

exposure is known to increase blood pressure by activation

of the sympathetic nervous system (Young 1996). Since

elevated blood pressure is a major risk factor for a range of

cardiovascular diseases (Jackson et al. 2005; Kim et al.

2003), it seems reasonable to explore how environmental

exposure affects blood pressure both experimentally and on

the population level.

The results of several large population studies of the

effects of the season and temperature on systolic blood

pressure show strong, statistically significant effects for

both factors (Madsen and Nafstad 2006). The effect of

season, however, disappeared in a model that also con-

tained outdoor temperature, which suggests that a major

component of the seasonal change in blood pressure, and

hence cardiovascular disease risk, is due to temperature

(Barnett et al. 2007). Improvements in central indoor

heating are not consistently associated with a reduction in

seasonal differences in mortality from cardiovascular dis-

ease (Keatinge et al. 1989; Wilkinson et al. 2004; Barnett

et al. 2005). Therefore, Keatinge et al. (1989, 1997) place

more emphasis on personal behaviors and have argued that

many excess winter mortalities are related to exposure to

cold from ‘‘brief excursions outdoors rather than to low

indoor temperatures’’. A study by Perez-Lloret et al. (2006)

contributed further supporting evidence that seasonal dif-

ferences in blood pressure do exist, but are largely confined

to the daytime. Causative mechanisms, such as the time

Y. Li (&) � H. Alshaer � G. Fernie

iDAPT Technology R&D Team,

Toronto Rehabilitation Institute,

550 University Avenue,

Toronto, ON M5G 2A2, Canada

e-mail: [email protected]

123

Eur J Appl Physiol (2009) 107:673–685

DOI 10.1007/s00421-009-1176-5

Page 2: Blood pressure and thermal responses to repeated whole body cold exposure: effect of winter clothing

course of increases in blood pressure in response to chan-

ges in ambient temperature, individual differences in these

responses, and the potential importance of improved out-

door clothing during winter all require further experimental

study.

Donaldson et al. (2001) surveyed more than 6,500 par-

ticipants from two age groups (50–60 and 65–74 years) and

found that there was large variation between regions in the

wearing of gloves, hats, and scarves. Furthermore, their

data showed that regional variations in the average wearing

of these three items (gloves, hats, and scarves) were sig-

nificantly related to excess winter mortality in those

regions. People do not always wear a hat during winter.

According to Donaldson et al. (2001), of the 6,583 people

who were interviewed, 2,678 (41%) wore a hat, and only

1,042 (16%) wore all three items. Furthermore, little is

known regarding the extent to which differences in the

thermoregulatory function mirror clothing effectiveness,

especially the insulation of the head.

According to an epidemiological survey, in North

America, people spent approximately 10% of their time

outdoors in summer and about 2–4% of their time outdoors

in winter (Leech et al. 2002). Numerous studies have been

conducted to demonstrate the effects of long-term exposure

to cold (Leppaluoto et al. 2001; Makinen et al. 2006;

Reynolds et al. 2007). On the other hand, investigations of

the effects of short-term repeated cold exposures on health

and physiological responses are limited in number (Ozaki

et al. 1998, 2001; Tochihara 2005; Kim et al. 2007).

However, these short cold exposures are very common in

daily life during winter and have become more increasingly

common in industry. In general, people are not exposed to

severe cold for long periods of time in the winter, but

instead, they have to go in and out of the cold environment

frequently.

To date, only one study conducted by Gavhed (2003),

has attempted to examine the extent to which personal

protection (e.g., wearing hats) is related to the cold-induced

rise in blood pressure in controlled laboratory conditions.

Gavhed (2003) found that wearing headgear with ear pro-

tection tended to reduce the systolic blood pressure

response among young healthy male participants. This

study was initiated to verify the findings of Gavhed, as well

as to investigate the effect of repeated brief cold exposures

on physiological responses across a broader range of ages

by including middle-aged participants. Accordingly, the

purpose of the present study was to examine the combined

effects of wearing different winter clothing and repeated

cold exposure on thermophysiological responses in 18

young (18–34 years) and 6 middle-aged (35–51 years)

normotensive participants under controlled laboratory

conditions.

Methods

Participants

A total of 24 adults (8 male, 16 female), mainly university

students and staff, participated in this study. Participants

were self-selected in response to printed advertisements.

The average and standard deviation of their baseline

characteristics are provided in Table 1. All participants

were normotensive, nonsmokers, and not taking any med-

ications that might alter the cardiovascular or thermoreg-

ulatory responses to cooling. The protocol was approved by

the Toronto Rehabilitation Institute Research Ethics Board.

Prior to data collection, each participant was provided a

clear description of what was required for participation and

thereafter was asked to carefully read and sign the consent

form. Participants were given the right to withdraw from

the study at any stage.

Instrumentation

After giving informed consent, physiological recording

devices and sensors were attached for the measurements of

blood pressure, heart rate and skin temperature. Systolic

blood pressure (SBP), diastolic blood pressure (DBP) and

heart rate were measured every 2.5 min before, during and

after cold exposure by a validated oscillometric BP monitor

(PhysioLogicTM Auto Inflate Blood Pressure Monitor,

AMG Medical Inc., Canada). The cuff was placed on the

left upper arm and worn throughout the trial. The skin

temperatures were measured using thermistors (Mon-a-

therm Temperature Probe, Nellcor Puritan Bennett Inc.,

Pleasanton, CA, USA) from seven sites: forehead, lower

back, right forearm, back of right hand, right thigh, right

lower leg, and right foot instep. Skin temperature values

were recorded throughout the experiment at 8-s intervals

Table 1 Demographic and

baseline hemodynamic

characteristics of the 24

participants

Age

(years)

Height

(cm)

Body

mass (kg)

Body

mass index

SBP

(mmHg)

DBP

(mmHg)

HR

(bmp)

Average 27.1 165.9 63.1 22.4 111.5 69.3 71.1

SD 9.0 9.2 13.3 3.1 9.6 7.6 8.0

Range 18–51 152–183 42–91 18–31 94–129 55–85 54–85

674 Eur J Appl Physiol (2009) 107:673–685

123

Page 3: Blood pressure and thermal responses to repeated whole body cold exposure: effect of winter clothing

with a data logger (Smartreader 8?, ACR Systems,

Canada). The tip of each thermistor was in direct contact

with the participant’s bare skin. Each thermistor tip was

covered with a 3-cm strip of 3 M TransporeTM tape (3 M

Health Care, USA) to help minimize the effect of the

ambient air on the reading. The system (data logger and 7

thermistors) was calibrated in accordance with ISO 17025

by an accredited calibration facility (Alpha Controls

And Instrumentation, Markham, Canada) with an accuracy

of ± 0.1�C over the temperature range of -30 to 40�C.

The mean skin temperature was calculated using an area-

weighting formula: mean skin temperature Tsk = 4.655 ?

0.114 forehead ? 0.027 lower arm ? 0.068 hand ? 0.262

lower back ? 0.152 thigh ? 0.172 lower leg ? 0.076 foot

temperature. (Nielsen and Nielsen 1984).

Clothing ensembles

The present study was aimed at simulating normal winter-

time outdoor cold exposure in Southern Ontario, Canada.

Clothing plays an important role in adjusting thermal

comfort and it is classified according to its insulation value.

The unit normally used for measuring clothing insulation is

the clo unit (1 clo = 0.155 m2 K/W). A regular Toronto-

nian winter ensemble normally includes a shirt, trousers and

a winter coat, which has a total insulation of 1.3 clo, in

agreement with a survey study that showed the average

clothing insulation to be 1.3 ± 0.3 clo in South Finland

(Donaldson et al. 2001). A total of four different ensembles

that correspond to normal winter clothing were evaluated.

The ensembles included a base-ensemble and four winter

clothing ensembles. The base-ensemble consisted of a vest

(knitted lycra material), long-sleeved shirt, briefs (for

female participants: panties and bra), trousers, ankle socks,

and running shoes. As shown in Table 2 and Fig. 1, the four

winter clothing ensembles were base-ensemble plus varied

winter items. None-ensemble consisted of the base-

ensemble, a thigh length coat, a scarf, and a pair of fleece

gloves. In the tuque-ensemble, a tuque (knitted hat) was

added to the none-ensemble. In the pants-ensemble, a pair

of tear-away pants (windpants with metal snaps running the

length of both legs) was added to the none-ensemble. In the

both-ensemble, a tuque and a pair of tear-away pants were

added to the none-ensemble. The total dry insulation was

calculated from these garments (ISO 1994; Donaldson et al.

2001) and was expressed in clo units. The estimated clo

values for each ensemble are listed in Table 2. The tuque-

ensemble corresponded to normal winter clothing, which

included all three items (hat, scarf, gloves) (Donaldson et al.

2001). To control for the repeated exposure effect that can

Table 2 Characteristics of experimental clothing ensembles

Base-ensemble None-ensemble Tuque-ensemble Pants-ensemble Both-ensemble

Items Clo Items Clo Items Clo Items Clo Items Clo

Briefsa 0.03 Baseb 0.605 Base 0.605 Base 0.605 Base 0.605

Vest 0.09 Coat 0.6 Coat 0.6 Coat 0.6 Coat 0.6

Shirt 0.2 Gloves 0.025 Gloves 0.025 Gloves 0.025 Gloves 0.025

Socks 0.025 Scarf 0.02 Scarf 0.02 Scarf 0.02 Scarf 0.02

Shoes 0.02 Hat 0.02 Pants 0.24 Hat 0.02

Trousers 0.24 Pants 0.24

Total clo 0.605 1.250 1.270 1.490 1.510

a For female participants: panties (0.02 clo) and bra (0.01 clo)b Base is base-ensemble

Fig. 1 Line drawing

illustrations of base-ensemble

(a) and the four winter clothing

ensembles (b–e) (illustration by

Jamie Ibbett, MFA)

Eur J Appl Physiol (2009) 107:673–685 675

123

Page 4: Blood pressure and thermal responses to repeated whole body cold exposure: effect of winter clothing

result from repeated testing, we used a counterbalancing

technique in which the order of the clothing ensembles was

counterbalanced for order across participants.

Experimental protocols

The study was performed during the winter from January to

April 2008 (mean monthly outdoor air temperature -2.1,

-5.3, -1.7 and 9.5�C) in the climate chamber at the

Toronto Rehabilitation Institute in Toronto. Each partici-

pant evaluated the four clothing ensembles under the same

environmental conditions (air temperature, Ta -5.8 ±

0.2�C, relative air humidity 72 ± 4%). Trials were con-

ducted on the same day to minimize between-day varia-

tions and were conducted during the winter/early spring

months to minimize the effects of cold acclimatization. The

testing for each participant was conducted by the same

investigators and started at the same time of day to reduce

possible confounding effects. Attempts were made to

standardize pre-trial behaviors of participants (i.e., general

exercise; timing and content of the meal (own choice) and

water consumed at mealtimes preceding the test session;

refraining from drinking alcoholic and caffeinated bever-

ages the day before trial). On the test day, participants

reported to the laboratory fully hydrated, having completed

their lunch 2.0–2.5 h prior to the starting time of the test.

The laboratory protocol involved four 15-min cold

exposures (C1–C4) in different winter ensembles in

counterbalanced order. Before each cold exposure, there

was a 10-min baseline period (B1–B4). Each cold exposure

was followed by a 15-min recovery period (R1–R4). The

total time of exposure to cold was 60 min. The total

rewarming time between two successive cold exposures

was 25 min. The experimental protocol is described in

Fig. 2. During the baseline period, the participants wore

the base-ensemble. They sat quietly for 10 min on a chair

in a thermally neutral room with air temperature at

24.4 ± 1.0�C, air velocity less than 0.2 m/s, and relative

air humidity of 25 ± 6%. Thereafter, the participants wore

one of the four winter ensembles and walked slowly 10 m

to a climatic chamber. The participants sat quietly in the

climatic chamber (air temperature at -5.8 ± 0.2�C, air

velocity less than 0.2 m/s, and relative air humidity of

72 ± 4%) on a chair for 15 min. The walls, ceiling and

floor of the climatic chamber were at the same temperature

as the air. After the cold exposure, the participants walked

slowly back to the thermally neutral room and removed

their winter ensemble. Then they sat quietly for 25 min

(15-min recovery period plus 10-min baseline period for

the next trial) wearing base-ensemble. Subjective ratings of

temperature sensation and thermal comfort were made at

the end of each baseline, cold exposure, and recovery

periods. Temperature sensations for the whole body were

assessed using a 9-degree subjective judgment scale (ISO

1995), ranging from very hot to very cold. Thermal com-

fort was assessed using a 5-degree scale ranging from

extremely uncomfortable to comfortable (ISO 1995) (as

shown in Fig. 3). Participants were asked to report each

temperature sensation separately by marking on a linear

100-mm line rating scale. A vertical line drawn at the

center of the scale indicated ‘‘neutral’’. The temperature

sensation and thermal comfort scales were labeled with

warm 25 min

cold 15 min

Base ensemble

Winter ensemble

Base ensemble

Winter ensemble

Base ensemble

Winter ensemble

Base ensemble

Winter ensemble

Base ensemble

C1R1

warm25 min

cold 15 min

C2R2

warm25 min

cold 15 min

C3R3

cold 15 min

C4R4B2 B3 B4

warm 10 min

warm15 min

B1

Trial 1 Trial 2 Trial 3 Trial 4

Fig. 2 Study design. A total of

24 participants performed the

tests in four consecutive trials at

cold (-5�C) and warm (?24�C)

conditions

(a) Temperature sensation scale

(b) Thermal comfort scale

Very cold

Very hot

Cold Cool Slightlycool

Neutral Slightlywarm

Warm Hot

Extremely uncomfortable

ComfortableSlightly uncomfortable

UncomfortableVery uncomfortable

Fig. 3 Illustration of (a)

temperature sensation and (b)

thermal comfort scale

676 Eur J Appl Physiol (2009) 107:673–685

123

Page 5: Blood pressure and thermal responses to repeated whole body cold exposure: effect of winter clothing

descriptions as shown in Fig. 3. The length from the left

end point to the point marked by the participant was

measured and quantified as the rating score of either tem-

perature sensation or thermal comfort. Participants repe-

ated the cold exposure wearing different winter ensembles

and the whole experiment lasted for about 4 h, including

setup of devices and electrodes.

Statistical analysis

All skin temperature data were stored as 5-min averages.

All index values were expressed as mean ± standard

deviation. Trial baseline values were computed for each

physiological response by averaging data from the 10-min

baseline period (B1–B4). The effect of repeated cold

exposure on baseline values of BP, HR, skin temperatures

and thermal response was tested by a one-way repeated-

measures ANOVA (within factor: trial 1–4) to test whether

the order of presentation of clothing ensembles had a sig-

nificant impact on thermophysiological responses. If the

impact was negligible for any of the measurements, the

analyses were collapsed over order and the effect of

clothing ensemble on that measurement was examined by a

one-way repeated-measures ANOVA (within factor: four

winter ensembles). Data from each of the 15- min of cold

exposure (C1–C4) and the 15 min of recovery (R1–R4)

were averaged to compute means for BP, HR, and skin

temperatures in each trial. Temperature sensation and

thermal comfort rating scores were also obtained after each

cold exposure and recovery period. Changes due to cold

exposure were calculated as the difference between trial

baseline value and the mean cold exposure period values,

C1–C4. For example, the change in SBP in trial i during

cold exposure was calculated as:

CDSBPðiÞ ¼ SBPCðiÞ � SBPBðiÞ:

Changes during recovery were defined as the difference

between trial baseline value and the mean recovery period

values R1–R4. For example, the change in SBP in trial i

during recovery was calculated as:

RDSBPðiÞ ¼ SBPRðiÞ � SBPBðiÞ:

The effect of clothing ensemble and repeated cold

exposure on changes in BP, HR, skin temperatures, and

thermal response was tested by a two-way ANOVA (four

ensembles 9 four trials) for cold exposure and recovery

period separately. Tukey’s HSD post hoc test was

employed if significant main effects were observed.

For each cold period (C1–C4) and baseline period (B1–

B4), the maximal and minimal values of SBP and DBP

were calculated. The BP surge due to cold exposure was

calculated as the difference between the maximal BP

during cold exposure and the minimal BP obtained during

the baseline period. For example, the SBP surge in trial

i was calculated as:

DSBPðiÞ ¼ SBPmax CðiÞ � SBPmin BðiÞ:

The effect of clothing ensemble on SBP and DBP surge

was examined by a one-way repeated-measures ANOVA

(within factor: four winter ensembles). Tukey’s HSD post

hoc test was employed if significant main effects were

observed.

All BP and HR data during the 15-min cold exposure

and recovery were also calculated as 5-min averages,

which were then compared with the trail baseline value to

examine how fast BP and HR reacted to cold and whether

BP returned to trial baseline level after 5, 10, or 15 min of

rewarming using paired sample t tests. The same test was

performed on 5-min averages of skin temperature data.

Results

Effect of repeated cold exposure on baseline values

There was no repeated cold exposure effect on baseline

values of SBP, DBP, and thermal comfort TC (p [ 0.11).

As shown in Fig. 4, repeated cold exposure had a sig-

nificant effect on baseline HR (p = 0.002), mean skin

temperature Tsk (p \ 0.001) and temperature sensation TS

(p = 0.01). Baseline HR was significantly higher before

the first cold exposure than before the third and fourth

exposures (p = 0.03 and p = 0.002, respectively). Base-

line Tsk decreased significantly through the repeated cold

exposures, from 33.7 ± 0.4�C before the first cold expo-

sure to 31.9 ± 0.6�C before the fourth cold exposure

(p = 0.0001). Baseline TS was significantly higher

before the first cold exposure than before the fourth cold

exposure (p = 0.006), decreased from 56 ± 11 (between

neutral and slightly warm) to 46 ± 9 (between slightly

cool and neutral). Further analysis confirmed that there

were no significant differences between clothing ensem-

bles in any of these baseline measures (p [ 0.54). Table 3

presents trial baseline values (SBP/DBP, HR, Tsk, TS, and

TC) for each clothing ensemble trial before cold

exposure.

Blood pressure and heart rate during cold exposure

and recovery period

Overall, cold exposure resulted in a significant increase in

SBP and DBP (p \ 0.0001). Mean baseline SBP/DBP

was 113.8 ± 9.5/72.0 ± 7.6 mmHg, which increased to

124.5 ± 9.8/82.0 ± 8.0 mmHg during cold exposure and

then returned to the trial baseline level during recovery

(116.3 ± 9.5). There were significant differences in

Eur J Appl Physiol (2009) 107:673–685 677

123

Page 6: Blood pressure and thermal responses to repeated whole body cold exposure: effect of winter clothing

average BP between trial baseline and cold exposure

(p \ 0.0001), and between cold exposure and recovery

(p \ 0.0001). However, there was no significant difference

between trial baseline and recovery (p [ 0.07). SBP reac-

ted to the cold in the first 5 min and did not change sig-

nificantly through the rest of the cold exposure across all

four clothing ensemble groups (Fig. 6). DBP showed

similar pattern. Clothing ensembles and repeated cold

exposure had no significant effect on average increases in

SBP and DBP during cold exposure (p [ 0.05) (Table 4).

Since there was no repeated cold exposure effect on

baseline and cold exposure values of SBP and DBP through

the four trials, the BP surges due to cold exposure were

compared among the four winter ensemble conditions. The

SBP surge was significantly higher in none-ensemble

condition (22.9 ± 6.5 mmHg) than in pants-, tuque- and

both-ensemble conditions (19.7 ± 6.5 mmHg, p = 0.03;

18.7 ± 5.6 mmHg, p = 0.03; and 19.3 ± 7.1 mmHg,

p = 0.04, respectively) (Fig. 5). Clothing ensembles had

no significant effect on DBP surge. Although the partici-

pants were all wearing base-ensemble during the recovery

period, the evidence suggests that the effect of different

clothing ensembles that they wore during the cold exposure

still tended to have an impact on the recovery of their SBP

and DBP (p = 0.06). Wearing hats during cold exposure

resulted in a faster recovery in SBP and DBP than wearing

no hats during cold exposure. The results showed that

blood pressure reached the trial baseline level after 5 min

of rewarming in tuque- and both-ensemble trials and after

10 min of rewarming in pants-ensemble trials (Fig. 6).

When the participants were not wearing a hat or extra pair

of pants (none-ensemble trial) during cold exposure, it took

20 min of rewarming for SBP and DBP to reach the trial

baseline level. Overall, during the 15-min recovery period,

the average RDSBP/DBP in tuque- and both-ensemble

trials was only 1.0 ± 5.7/0.2 ± 5.4 and 1.3 ± 5.7/1.1 ±

5.6 mmHg higher than the baseline level (Table 4). But

the average RDSBP/DBP in none-ensemble trial was

4.6 ± 5.9/3.8 ± 5.2 mmHg higher than the baseline level.

There was no interaction between clothing ensemble and

repeated cold exposure on changes in BP during cold

exposure and recovery.

Heart rate decreased slightly from 66.1 ± 8.2 to

64.4 ± 7.6 bpm during the cold exposure and then to

62.4 ± 7.3 bpm during recovery. There were no significant

differences in average HR between trial baseline and cold

exposure (p = 0.15) or between cold exposure and recov-

ery (p = 0.06). However, there was a significant difference

0

10

20

30

40

50

60

70

80

90

HR (bpm) mean skin temperature (°C) temperature sensation

* *

* **

*

# #

$

B 1 B 3 B 2 B 4 B 1 B 3 B 2 B 4 B 1 B 3 B 2 B 4

Fig. 4 Baseline values through

four trials. *p \ 0.05: in

comparison to B1, #p \ 0.05:

in comparison to B2, $p \ 0.05:

in comparison to B3

Table 3 Trial baseline values for each clothing ensemble trial

Clothing ensemble Systolic BP Diastolic BP HR Mean skin temperature Temperature sensation Thermal comfort

Mean SD Mean SD Mean SD Mean SD Mean SD Mean SD

None 112.8 9.8 71.3 7.4 65.6 7.0 32.6 0.8 51 10 80 21

Pants 113.1 9.5 71.3 8.4 65.9 8.8 32.7 0.8 52 13 82 20

Tuque 114.9 10.1 72.9 8.2 66.4 9.6 32.6 0.9 50 8 74 20

Both 114.2 9.2 72.4 6.8 66.4 7.6 32.5 0.8 49 10 81 18

Total 113.8 9.5 72.0 7.6 66.1 8.2 32.6 0.8 50 11 79 20

678 Eur J Appl Physiol (2009) 107:673–685

123

Page 7: Blood pressure and thermal responses to repeated whole body cold exposure: effect of winter clothing

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9.3

-2

.0to

18

.7-

2.8

to1

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-1

3.0

to1

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to1

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sto

lic

BP

Mea

n9

.47

.97

.56

.83

.82

.90

.21

.1

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6.3

3.4

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75

.22

.95

.45

.6

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ge

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23

.80

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HR M

ean

-1

.3-

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-1

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-3

.6-

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-3

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SD

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4.0

4.9

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4.6

4.4

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ge

-1

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3.3

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Eur J Appl Physiol (2009) 107:673–685 679

123

Page 8: Blood pressure and thermal responses to repeated whole body cold exposure: effect of winter clothing

between trial baseline and recovery (p = 0.001). It took

25 min of rewarming for HR to reach the trial baseline

level. No effects of clothing ensemble on average changes

in HR were observed during cold exposure and recovery.

However, repeated cold exposure had a significant effect

on HR decreases. The cold-induced decreases of HR

were greater during the first cold exposure (CDHR =

-3.5 ± 3.4 bpm) than during the fourth cold exposure

(CDHR = -0.7 ± 4.9 bpm) (p = 0.02) (Table 5). The

decreases of HR during the 15-min recovery were greater

in the first trial (RDHR = -6.3 ± 4.0 bpm) than in the

second (RDHR = -2.7 ± 3.9 bpm, p = 0.02) and fourth

trials (RDHR = -1.9 ± 4.3 bpm, p = 0.003) (Table 5).

There was no interaction between clothing ensemble and

repeated cold exposure on changes in HR.

Skin temperature during cold exposure and recovery

period

Tsk showed a significant decrease from 32.6 ± 0.8 to

30.2 ± 1.0�C (p \ 0.01) during cold exposure. There were

significant clothing ensemble effects in mean skin tem-

perature (p \ 0.0001) during cold exposure. Overall, the

decrease of Tsk was significantly greater in the none-

ensemble condition than in tuque-, pants- and both-

ensemble conditions (p \ 0.002) (Table 4). The decrease

in Tsk was significantly smaller in the both-ensemble con-

dition than in the tuque- and pants-ensemble conditions

(p \ 0.03). The repeated cold exposure had no significant

effect on CDTsk (p = 0.80).

During the recovery period, Tsk increased significantly

compared to the cold exposure period, but was still

significantly lower compared to the baseline value

(p \ 0.001). The effect of different clothing ensembles that

participants wore during cold exposure had significant

impact on the recovery of their Tsk during the 15-min

recovery period. The decreases in mean skin tempera-

ture were significantly greater in none-ensemble trials

(CDTsk = -1.7 ± 0.3�C) than in both-ensemble trials

(CDTsk = -1.2 ± 0.4�C) (p \ 0.008) (Table 4). The repe-

ated cold exposure also had significant effect on the recovery

of Tsk. The recovery of Tsk was smaller in the first

trial (CDTsk = -1.8 ± 0.4�C) than in the second, third,

and fourth trials (CDTsk = -1.4 ± 0.5�C, CDTsk =

-1.4 ± 0.4�C, and CDTsk = -1.2 ± 0.3�C, respectively)

(p \ 0.002) (Table 5). There was no interaction between

clothing ensemble and repeated cold exposure on CDTsk.

There were significant clothing ensemble effects on

changes in forehead skin temperature (RDTfh) during cold

exposure and recovery (p \ 0.0001), but there was no

difference in the changes in Tfh between trials. During cold

exposure, the decreases in forehead skin temperature were

significantly smaller while wearing a hat (tuque-ensemble:

0

5

10

15

20

25

30

35

None Tuque Pants Both

Winter ensemblesS

BP

su

rge (

mm

Hg

) * **

Fig. 5 SBP surge due to cold

exposure across four winter

clothing ensembles. *p \ 0.05:

in comparison to none-ensemble

-4

-2

0

2

4

6

8

10

12

14

trialbaseline

5 min 10 min 15 min 5 min 10 min

Ch

ang

e in

SB

P (

mm

Hg

)

-None

-Pants

-Both

-Tuque

*

$

* *

# # #

Cold exposure Recovery

15 min

Fig. 6 Systolic blood pressure after 5-, 10, and 15-min of cold

exposure and recovery across four winter clothing ensembles (values

are mean differences between 5-min averages and trial baseline

values). #p \ 0.05: 5-min average value in comparison to baseline

value in all four cloth ensembles. *p \ 0.05: 5-min average value in

comparison to baseline value in none-ensemble. $p \ 0.05: 5-min

average value in comparison to baseline value in pants-ensemble

680 Eur J Appl Physiol (2009) 107:673–685

123

Page 9: Blood pressure and thermal responses to repeated whole body cold exposure: effect of winter clothing

Ta

ble

5C

han

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0.4

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6.0

5.3

4.9

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ge

-3

.3to

29

.3-

1.0

to2

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-7

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26

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3.5

Dia

sto

lic

BP

Mea

n9

.08

.06

.77

.83

.11

.91

.31

.6

SD

5.5

5.0

6.4

5.3

5.0

4.5

4.9

5.8

Ran

ge

-2

.7to

21

.20

.0–

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.8-

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to2

0.0

-4

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15

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.5to

11

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.5to

10

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.1to

11

.9

HR M

ean

-3

.5-

1.7

-1

.7-

0.7

*-

6.3

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-3

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3.4

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ge

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to3

.3-

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.3to

13

.3-

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.0-

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.8to

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2.3

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2.5

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0.8

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Eur J Appl Physiol (2009) 107:673–685 681

123

Page 10: Blood pressure and thermal responses to repeated whole body cold exposure: effect of winter clothing

RDTfh = -3.5 ± 0.7�C; both-ensemble: RDTfh = -3.6 ±

1.0�C) than when no hat was worn (none-ensemble:

RDTfh = -8.7 ± 1.5�C; pants-ensemble: RDTfh = -8.8 ±

2.1�C) (p \ 0.0002). During recovery, although the mean

and forehead skin temperature did not reach the trial

baseline level after 15 min of rewarming in any of the

winter ensemble trials, Tfh was higher in the tuque- and

both-ensemble trials than in the pants- and none-ensemble

trials. There was no interaction between clothing ensemble

and repeated cold exposure on RDTfh.

Temperature sensation and thermal comfort during cold

exposure and recovery period

At 15 min after exposure to -5�C, temperature sensation

and thermal comfort decreased significantly from 50 ± 11

(neutral) to 16 ± 12 (cold) and from 79 ± 20 (slightly

uncomfortable) to 31 ± 22 (very uncomfortable), respec-

tively. By the end of the 15-min recovery period, TS and

TC increased to 48 ± 12 (neutral) and 77 ± 21 (slightly

uncomfortable), respectively, which were not significantly

different from the baseline values. No effects of clothing

ensemble and repeated cold exposure on overall changes in

temperature sensation and thermal comfort were observed

(Tables 4, 5).

Discussion

Effect of wearing a hat on cold responses

The present study provides for the first time information

about the effects of winter clothing and repeated cold

exposure on BP responses in normotensive participants

exposed to cold in a way that is similar to normal outdoor

exposure in winter. Our results show that wearing a

hat reduced SBP surge from 22.9 ± 6.5 mmHg (none-

ensemble) to 18.7 ± 5.6 mmHg (tuque-ensemble) and

19.3 ± 7.1 mmHg (both-ensemble) during the cold expo-

sure period. These results are consistent with a previous

study, which showed that the magnitude of the blood

pressure response was attenuated by wearing hats (Gavhed

2003). Gavhed (2003) reported that wearing headgear with

ear protection tended to reduce the systolic blood pressure

response, but heart rate was similar with and without a hat.

A study in Europe found that the geographical variation in

cold-related mortality may be explained by differences in

the outdoor clothing worn (Donaldson et al. 2001). The

authors suggested that gloves, hats, and scarves are the

most important clothing items, because they cover those

areas of the body most involved in determining the blood

pressure response to cold. Stevens and Choo (1998) ana-

lyzed the detection thresholds for heating and cooling in 13

body regions of 60 adults between the ages of 18 and

88 years. They found that thermal sensitivity varies

100-fold over the body surface, the face being most sen-

sitive and the extremities least sensitive. Cutaneous ther-

mal receptors are not distributed equally throughout the

body surface. In primates, including humans, non-hairy

skin on the face and hands contains many more thermal

receptors than other skin areas (Pittman 2003). The fifth

cranial nerve, the trigeminal nerve, supplies all of the

anterior sensory fibers to the skin of the head. Various

types of noxious stimuli to the trigeminal region were

shown to result in a reflex pattern characterized by rises in

muscle sympathetic nerve activity, blood pressure, and

bradycardia (Heindl et al. 2004; Smith et al. 1997; Collins

1990): a pattern of both sympathetic and parasympathetic

activation similar to our findings in subjects who did not

wear a hat during cold exposure. Our data are also con-

gruent with previous works showing that local cooling of

the forehead provoked a fast increase of sympathetic acti-

vation, and high levels of diastolic blood pressure (LeBlanc

and Mercier 1992; Trouerbach et al. 1994; Walsh et al.

1995) that are even more profound than with cooling of the

hand (Heindl et al. 2004). Our results demonstrate that

wearing a hat during cold exposure kept the forehead skin

temperature at a higher level. Therefore, the skin of the

forehead represents an important region for the adaptation

of the cardiovascular system to cold exposure. The sym-

pathetic activation observed during cold exposure is

probably mediated by trigeminal cold-sensitive afferents in

the skin (Heindl et al. 2004; Collins 1990). The present

study showed that HR decreased during cold exposure and

decreased further during the recovery period in young

adults. However, no significant differences were observed

in the heart rate for different clothing conditions, sug-

gesting that wearing hats per se did not influence the

parasympathetic responses to the cold. It can be concluded

that wearing a hat that covers the forehead and ears could

alleviate the sympathetically mediated surge in BP in

young adults.

It is worth noting that the impact of wearing a hat during

cold exposure lasted through the recovery period when the

participants were all wearing the same base clothing

ensemble. The results showed that blood pressure reached

the trial baseline level faster when a tuque or a pair of

overpants was worn singly or in combination. During

recovery, the forehead skin temperatures were higher in

tuque- and both-ensemble trials than in pants- and none-

ensemble trials. Therefore, the higher forehead skin tem-

perature during rewarming may be responsible for the

faster recovery of blood pressure. Compared to wearing

hats, the effect of wearing an extra pair of pants on low-

ering SBP surge and speeding up BP recovery was less

prominent, but was still significant. Since wearing an extra

682 Eur J Appl Physiol (2009) 107:673–685

123

Page 11: Blood pressure and thermal responses to repeated whole body cold exposure: effect of winter clothing

pair of pants increased lower extremity skin temperatures

but not forehead temperatures, these results suggest that

keeping the legs warm could also play an important role in

hemodynamic responses to cold exposure. These findings

are encouraging and warrant further investigations to better

understand the benefits of wearing appropriate clothing in

the winter.

The effect of wearing a hat on attenuating cold-induced

SBP surge and encouraging faster recovery was significant

in the young and middle-aged normotensive individuals in

the present study. Since only healthy, young, and middle-

aged participants were included in the present study, the

results cannot be extrapolated to patients with various

disorders or to the general older population. However,

Keatinge et al. (2000) have indicated that the enhanced

pressor response to cold stress with other circulatory

reflexes might be one mechanism explaining the excess

winter mortality in the elderly population. Aging is asso-

ciated with many changes in autonomic nervous system

function that often lead to impairments in the normal

ability to respond to physiological stressors commonly

encountered in daily life (Collins et al. 1985; Sheth et al.

1999; Smith and Fasler 1983; Smolander 2002). One of the

most serious complications in older people is the tendency

toward hypertension in cold ambient temperatures (Wagner

and Horvath 1985). In healthy elderly people, whole body

cooling has been shown to produce a greater increase in

arterial blood pressure and a reduced bradycardia com-

pared to younger adults (Collins 1990; Collins et al. 1995).

Since the risks of cardiac strain after exposure to the cold

probably increase with age, sufficient winter clothing that

includes head covering should be a recommended practice

in cold environment for older people, especially for older

people with underlying cardiac conditions. Further studies

on the effect of keeping head and lower extremities warm

in cold temperatures are needed to examine the role of

winter clothing on thermoregulatory and non-thermoregu-

latory responses (hemodynamics, cardiac function, respi-

ration, autonomic nervous function) to cold stress in older

people. The second stage of this project is currently

underway to examine whether wearing a hat would have

similar effect on older adults.

Effect of repeated cold exposures

on thermophysiological responses

The present study simulated normal wintertime outdoor

cold exposure in Southern Ontario, Canada. The effect of

repeated cold exposure on blood pressure was not signi-

ficant in this study. The results showed that SBP and

DBP were 121.9/78.3, 122.1/79.1, 123.4/80.0, and 124.5/

82.0 mmHg after the first, second, third, and fourth cold

exposures, respectively. The level of maximal blood

pressure was reached 5 min after the starting of the cold

exposure, and blood pressure stayed almost at the same

level during the 15-min cold exposure. SBP and DBP

responses in the present study were in accordance with

previous studies (Ozaki et al. 1998, 2001), which have been

carried out with normotensive participants in warmer

winter clothing (2.3 clo) under colder test conditions. SBP

has been reported to increase from 118 to 126, 129, and

128.5 mmHg after the first, second and third 20-min

exposure to -25�C with 20-min warm up in 30�C between

two cold exposures (Ozaki et al. 1998).

Previous studies suggested that chronic and repeated

cold exposures causing marked whole body cooling result

in more pronounced physiological responses, including

enhanced vasoconstriction and metabolic rate (Hammel

et al. 1959; Young 1996). However, repeated brief expo-

sures to cold not involving marked whole body cooling are

suggested to result in habituation (Leppaluoto et al. 2001).

When being habituated to cold, shivering and the vaso-

constrictor response are blunted, stress responses are

reduced, and the sensations of cold are less intense. These

responses can develop even after only a few repeated cold

exposures to cold air (Leppaluoto et al. 2001). Leppaluoto

et al. (2001) demonstrated that the thermal sensations

became habituated after the first or second daily cold air

exposure, but the other responses became variably habit-

uated as late as after four daily exposures, and hemocon-

centration was not affected until the end of the 11-day

experiment. In the present study, the changes in blood

pressure, skin temperatures, and thermal sensations were

similar through the four cold exposures. Hence, no habit-

uation process was observed, which may be due to the short

durations of our cold exposures. However, the measure-

ments from this study showing that the decreases in heart

rate in the fourth cold exposure were less pronounced

compared to the first (Table 5). Therefore, when the cold

exposures were repeated, the reduction in heart rate was

slightly blunted. A recent study suggested that the reduc-

tion in heart rate could be an indicator for increased

parasympathetic activity in the cold (Makinen et al. 2008).

The same study also suggested that at the sinus node level,

the sympathetic activation due to cold exposure was

blunted during cold acclimation, and replaced to some

extent by increased parasympathetic influence. Thus, the

brief moderate cold air exposure in this study was not a

sufficient stimulus to achieve a general habituation to cold,

but might have elicited a shift in the autonomic nervous

system toward parasympathetic activity to some extent.

Autonomic nervous system response can be further studied

by assessing heart rate variability (HRV) while being

exposed to repeated cold, which may also provide further

insight into the assessment of autonomic cardiovascular

regulation and the mechanisms that are involved.

Eur J Appl Physiol (2009) 107:673–685 683

123

Page 12: Blood pressure and thermal responses to repeated whole body cold exposure: effect of winter clothing

Conclusions

The present study has shown that protection of the head

from cold reduces the sympathetically mediated surge in

BP in young adults. Systolic and diastolic blood pressures

increased more profoundly when a hat was not worn by

normotensive individuals during cold exposure. Wearing

hats also promoted faster recovery of forehead skin tem-

perature and blood pressure during the recovery period.

This is an important finding, since elevated blood pressure

is a major risk factor for a range of cardiovascular diseases.

This defensive measure against cold-induced surges in BP

might be even more important in susceptible populations,

such as older people with and without underlying cardio-

vascular diseases. More studies should be carried out to

determine whether a positive health outcome could be

achieved by such lifestyle interventions. Our ongoing

projects are examining the effective use of warm clothing,

especially headgear to protect older and at-risk populations

in controlled laboratory conditions.

Acknowledgments This research was funded by the National

Institute on Disability and Rehabilitation Research (NIDRR) through

the Rehabilitation Engineering Research Centre on Universal Design

and the Built Environment (grant #H133E050004-08A), a partnership

with the Centre for Inclusive Design and Environmental Access

(IDEA). The authors acknowledge the support of the Toronto Reha-

bilitation Institute, which receives funding under the Provincial

Rehabilitation Research Program from the Ministry of Health and

Long-Term Care in Ontario. Equipment and space were funded, in

part, with grants from the Canada Foundation for Innovation and the

Province of Ontario. The authors wish to express their gratitude to

Jennifer Hsu, Stephanie Soo, and Christine Yen for their invaluable

assistance in data collection. The authors would also like to thank all

the participants for their time and effort.

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