Stress-induced hyperthermia in the rat: Comparison of classical and novel recording methods

Abstract

Stress causes a rise in body temperature in laboratory animals (stress-induced hyperthermia). However, the direct effect of common stressors in animal research, i.e. transportation between holding and test rooms or isolation of animals, on body temperature has not been investigated to its full extent. To address this question, it is important to have a reliable and simple monitoring technique, which does not induce stress itself. In the present study, we investigated stress-related changes in body temperature of F344/Hw rats after (1) moving the cage within the holding room, (2) moving the cage from the holding room to another test room and (3) social deprivation (isolation). A combination of two different body temperature recording methods was used to clarify their accuracy and stress-inductive character: rectal temperature recording and peritoneal implanted temperature sensors (Thermochron iButtons).
The results demonstrate that (1) different stressors induce a significant rise in body temperature, (2) which is detectable for more than 60 min and (3) it is of importance to standardize temperature recording methods in order to avoid confounding effects of the recording method itself. Furthermore, Thermochron iButtons are more accurate and reliable for body temperature studies than rectal recordings.

Full text

Stress-induced hyperthermia in the rat:
comparison of classical and novel
recording methods
R Dallmann
1,3
, S Steinlechner
1
, S von Ho¨ rsten
2
and T Karl
2,4
1
Institute of Zoology, School of Veterinary Medicine, 30559 Hannover, Germany;
2
Department of
Functional and Applied Anatomy, Hannover Medical School, 30623 Hannover, Germany;
3
Department
of Zoology, University of Toronto, Toronto Ontario, M5R 3G5 Canada;
4
Neuroscience Institute for
Schizophrenia and Allied Disorder, Darlinghurst, NSW 2010, Australia
Summary
Stress causes a rise in body temperature in laboratory animals (stress-induced hyperthermia).
However, the direct effect of common stressors in animal research, i.e. transportation
between holding and test rooms or isolation of animals, on body temperature has not been
investigated to its full extent. To address this question, it is important to have a reliable and
simple monitoring technique, which does not induce stress itself. In the present study, we
investigated stress-related changes in body temperature of F344/Hw rats after (1) moving the
cage within the holding room, (2) moving the cage from the holding room to another test
room and (3) social deprivation (isolation). A combination of two different body temperature
recording methods was used to clarify their accuracy and stress-inductive character: rectal
temperature recording and peritoneal implanted temperature sensors (Thermochron
iButtons).
The results demonstrate that (1) different stressors induce a significant rise in body
temperature, (2) which is detectable for more than 60 min and (3) it is of importance to
standardize temperature recording methods in order to avoid confounding effects of the
recording method itself. Furthermore, Thermochron iButtons are more accurate and reliable
for body temperature studies than rectal recordings.
Keywords Body temperature; rectal measurement; Thermochron iButton;
transportation stress; isolation stress
A wide range of studies show that different
types of stress (e.g. introduction to an open
field, cage switch, immobil ity, rectal body
temperature measurement, handling,
removal of littermates from home cage or
electric foot shock) induce an increase of
core body temperature (T
b
) (Poole &
Stephenson 1977, Eikelboom 1986, Long
et al. 1990, Van der Heyden et al. 1997, Kask
et al. 2001, Oka et al. 2001, Verleye &
Gillardin 2004). This stress-induced rise in
T
b
or so-called stress-induced hyperthermia
(SIH) is a robust, reproducible, long-lasting
and stable phenomenon, which can be
suppressed by prior anxiolytic treatment (e.g.
diazepam and flesinoxan) (Borsini et al.
1989, Zethof et al. 1994).
Importantly, increases in T
b
are
accompanied by elevations in plasma
ACTH, corticosterone and glucose levels
(Groenink et al. 1994). Furthermore, the
cardiovascular system is stimulated
Accepted 15 July 2005 r Laboratory Animals Ltd. Laboratory Animals (2006) 40, 186–193
Correspondence: Tim Karl, Neuroscience Institute of
Schizophrenia and Allied Disorders, 384 Victoria Street,
Darlinghurst, NSW 2010, Australia.
Email: t.karl@garvan.org.au

(Nakamori et al. 1993) and both brain and
pituitary opioids are mobilized (increase in
release – Vidal et al. 1984). Oka and
co-workers (2001) have taken this potent and
important impact of T
b
elevations on an
organism’s physiology into consideration
and classified an increase in T
b
resulting
from disturbance or stress as ‘psychogenic
fever’. Thus, the impact of various stressors
such as transpor tation or isolation can be
determined, for example by monitoring body
temperature dynamics of the test animal.
Blasig and colleagues found an increase in
T
b
after transportation of rats (from indoors
to outdoors and back) (Blasig et al. 1978). In
addition, transportation of rats between
buildings has a great impact on
gonadotropin-releasing hormone and
follicle-stimulating hormone levels
(Bieglmayer et al. 1980). Neither study
examined the effects of the most common
situations in animal research, i.e.
transferring animals from a holding to a
testing room. Thus, no valid recommen-
dation on the duration of a habituation
period after such a procedure can be given at
this time. Therefore, it is of great interest to
investigate the impact of stress aroused by
short-time transport on a given stress-related
parameter, i.e. body temperature. The
present study addresses this question and
investigates the influence of transportation
of laboratory animals between rooms, of
isolation and of body temperature recording
itself on T
b
and indirectly on the animal’s
physiology. A stress-induced increased T
b
is
likely to be already established after
approximately 10 min but is a long-lasting
effect for at least 30–60 min (Van der Heyden
et al. 1997).
In this context, radio telemetry has
provided the method of choice for stress-free
recording of core body temperature in recent
years. In contrast to rectal T
b
recording
repeated measurements are easily possible
and do not result in an increase of T
b
(Poole
& Stephenson 1977, Van der Heyden et al.
1997). However, disadvantages of implanted
transponders compared with rectal
measurement are high set-up costs, the
inability to record from multiple animals
housed together and the necessary surgery.
Here, we adapted a new industrial technique
for behavioural research and used
Thermochron iButtons (DS1921H-F50:
Maxim/Dallas Semiconductor, USA) for T
b
recording. Thermochron iButtons require no
telemetric recording devices and have
therefore low set-up costs, are reusable, have
a reasonable temperature resolution
(0.1251C) and range (15–461C) and, in
contrast to most telemetric systems, allow
synchronous measuring of T
b
from several
animals per cage.
Thus, in this study , we used three different
stress paradigms (rectal T
b
measurement
versus transportation versus isolation) and
two different recording methods (rectal
measurement versus Thermochron iButtons)
to investigate (i) the effect of common
stressors on the animal’s T
b
and (ii) the impact
of different recording methods on the animal’s
T
b
within these different stress paradigms.
Materials and methods
Animals
Age (710 days of age) and body weight
(330740 g) matched six-month-old, handled,
male F344/Hw rats were group-housed (2–3
animals per cage) at the Institute of
Laboratory Animal Science of the Medical
School, Hannover (sub-line code: Ztm) and
maintained under artificial light from 07:00
to 19:00 h in a separated minimal barrier
sustained room. The animals were kept in
Makrolon type III cages (Techniplast, Italy)
with standard bedding (Lignocel: Altromin,
Lage, Germany). Food (Altromin Standard
Diet 1320: Altromin) and tap water were
available ad libitum. Ambient temperature
was automatically regulated at 21721C and
relative humidity was 55 75% with an air
change rate of 15 times per hour. The animal
rooms were operated with a positive air
pressure of 0.6 Pa. Routine microbiological
monitoring according to the Federation of
European Laboratory Animal Associations
(FELASA) recommendations (Nicklas et al.
2002) did not reveal any evidence of
infections with common murine pathogens
except for Pasteurella pneumotropica and
Staphylococcus aureus. All research and
Laboratory Animals (2006) 40
Body temperature recording methods 187

animal care procedures were approved by the
Review Board for the Care of Animal
Subjects of the district government,
Hannover, Germany, and were performed
according to international guidelines for the
use of laboratory animals (for details see:
Institute for Laboratory Animal Research,
ILAR http://books.nap.edu/html/labrats/).
Rats were randomly assigned to three
different recording groups:
(1) ‘rec’: rectal body temperature (T
rec
)
was recorded by inserting a digital
thermistor probe (n ¼ 10);
(2) ‘iBut’: core body temperature (T
core
)
was recorded automatically by
Thermochron iButtons (n ¼ 10);
(3) ‘rec þ iBut’: both methods were used to
assess core and rectal body temperature
at the same time (n ¼ 9).
Implantation of Thermochrom iButtons
The Thermochron iButtons were implanted
into the peritoneal cavity. The animals were
anaesthetized with an intramuscular
injection of ketamine hydrochloride (0.1 mL/
100 g body weight – concentration: 100 mg/
mL; Albrecht, Aulendorf, Germany) and
medetomidine (Domitor
s
, Novartis,
Ontario, Canada) (0.01 mL/100 g body weight
– concentration: 20 mg/mL; Pfizer,
Karlsruhe, Germany). Domitor, having an
analgesic-like effect as well, was not
reversed in order to provide postoperative
analgesia. The lower ventral part of the
abdomen was shaved and a 1.5–2 cm long
incision was made in the skin and the
peritoneal wall. The silicone-coated iButton
was then inser ted into the peritoneal cavity
and the peritoneum and the skin were closed
separately with absorbable suture (Softcat
plain – 3.5 metric, Braun, Germany). After
surgery, animals were pair-housed and
allowed to recover for 10 days before
behavioural experiments started. Two
months after the experiments animals were
sacrificed by an overdose of ketamine
hydrochloride and iButtons were recovered
from the peritoneal cavity. Simultaneously,
we checked for any signs of injury of internal
organs caused by the iButtons.
Recording of body temperature
Rectal recording
The same person, who
handled the animals prior to the experi-
ments, carried out body temperature record-
ings in the stable thermal environment of
the holding and/or testing room. The rectal
temperature was measured by gently insert-
ing a digital thermistor probe (CMA/150
Temperature Controller: CMA/Microdialy-
sis, Solna, Sweden) to a length of 4–5 cm
intrarectal until a stable reading was ob-
tained or for up to 20 s. For this, rats were
restrained manually at the base of the tail
and the thermistor probe was dipped into
Vaseline before inserting. The temperature
was determined with a resolution of 0.11C,
and the accuracy of the thermistor was
within 0.11C of the respective calibrated
mercury thermometer. The time interval
between rectal temperature measurements
of individual rats was 1 min.
Thermochron iButton recording The core
body temperature was automatically re-
corded by i.p. implanted Thermochron
iButtons. The iButtons weigh 3.1 g (dia-
meter: 16 mm; thickness: 6 mm). Prior to
implanting, iButtons were coated with a thin
layer of silicone (734 RTV: Dow Corning,
Wiesbaden, Germany) in order to exclude
ingress of moisture and tissue adhesions.
Each iButton can store up to 2048
temperature readings in a user-defined
time-interval. The onset of measurement is
user-definable. Here, we used a 3 min
interval resulting in a measurement period
of more than 4 days. The implanted iButtons
started recording of core body temperature
36 h prior to the experiments. The
temperature resolution of the iButtons was
0.1251C, thus, with an accuracy of less than
0.11C after calibration against a mercury
thermometer.
Stress paradigms
Basal T
b
(‘basal’) Starting 4 h before onset
of the dark phase home cages of rats of all
three experimental groups were trans-
ported within the holding room to a desk and
the cage lids of all cages were removed.
Laboratory Animals (2006) 40
188 R Dallmann et al.

Following this, animals’ rectal T
b
was
measured every 30 min during 120 min in
the ‘rec’ and ‘rec þ iBut’ groups (as described
above). Afterwards, the cage lid was placed
back onto the cage and the cage was put back
onto the rack.
T
b
after room transfer (‘transport
stress’)
Twenty-four hours after the ‘basal’
measurement, rats’ T
b
was measured fol-
lowing the same procedure as described
above. In contrast, however, after the first T
b
recording in the holding room animals
were transferred in their home cages through
a noisy corridor (constant background
noise caused by ventilation and pig
holding rooms on the other side of the
corridor) to a nearby testing room. T
b
was
measured again 30 and 60 min later.
Afterwards, animals were returned to the
holding room.
T
b
after isolation (‘isolation stress’)
Twenty-four hours after the ‘transport stress’
experiment using the same procedure, rats
were individually housed in Makrolon type II
cages without bedding material after being
transferred to the testing room. Animals were
kept isolated for the followi ng 60 min, during
which T
b
was measured twice (after 30 and
60 min).
Statistical analysis
Body temperature data were assessed by
analysis of variance (ANOVA) for repeated
measures. In repeated measures ANOVA the
variable recording method was used as the
between factor for body temperature
differences between the three recording
groups ‘rec’, ‘iBut’ and ‘rec þ iBut’ and the
two different sets of data in the ‘rec þ iBut’
group (rectal and iButton measurements).
The compact variable stressor was used as
the within factor for body temperature
differences in each recording group in
between the various experiments. In case
of significant differences with regard to the
between or within factor, one-way
ANOVAs were used split by the dimension
of the continuous response variable.
One-way ANOVAs were followed by the
Fisher-PLSD-test for post hoc comparison
if appropriate.
The accuracy of the different recording
methods in measuring T
b
was analysed in
the ‘basal’ experiment between the two data-
sets of the ‘rec þ iBut’ group and between the
‘rec’ and ‘rec þ iBut’ group (using the
Thermochron iButton recording data-set).
The analysis of influences of different
recording methods on T
b
was done in the
‘basal’ experiment between the ‘rec þ iBut’
(using the Thermochron iButton data-set)
and the ‘iBut’ group. The effect of transport
and isolation stress on T
b
(and its increase)
was calculated within and the influence of
the recording method on the effect of
transport and isolation stress was calculated
between the different T
b
recording groups. In
order to evaluate the effects of the stressful
situations to the T
b
rhythm we calculated
the timing of the nightly rise (onset) and fall
(offset) of body temperature for all animals
with iButtons (n ¼ 19). Therefore, we
calculated the 24 and 3 h running averages of
the raw data. The intercept points of these
two running averages were defined as on-
and offset of T
b
(Meerlo et al. 1997).
Differences were regarded as statistically
significant if Po0.05. The number of
animals per T
b
recording group (n) was 9–10.
All data are presented as means7standard
error of the mean (SEM).
Results
Localization of iButtons
All iButtons were found on the right side of
the peritoneal cavity, just posterior to the
liver upon removal, showing that the
position of the thermistor was very stable.
Comparison of different T
b
recording
methods
Repeated measures ANOVA revealed
significant T
b
differences between the two
recording methods within the ‘rec þ iBut’
group and between this group and the ‘rec’
group in the ‘basal’ experiment (P ¼ 0.001).
One-way ANOVA revealed significantly
higher T
b
levels by iButton recording
Laboratory Animals (2006) 40
Body temperature recording methods 189

compared with the rectal measurement in
the same animals at 0 min (35.3 70.2 1C
versus 36.870.21C, Po0.0001) and 60 min
(36.570.21C versus 37.670.21C, P ¼ 0.006)
(Figure 1) of the ‘rec þ iBut’ group, and also
compared with T
b
of the ‘rec’ group (data not
shown). In order to compare for reliability of
the measurements we compared the
standard deviation of the rectal and iButton
recordings of the basal experiment for the
‘rec þ iBut’ group. Rectal temperature
recordings showed a higher mean standard
variation (0.94) compared with iButton
values (0.47).
Influence of different recording methods on
basal T
b
Comparison of the two iButton recording
groups ‘iBut’ and ‘rec þ iBut’ revealed no
statistically significant differences between
these two groups in the ‘basal’ experiment.
In both groups a significant elevation of T
b
can be observed over time (repeated
ANOVA: Po0.0001).
Influence of different stress paradigms on T
b
In all three experiments the treatment of the
animals significantly increa sed T
b
as
confirmed by repeated ANOVA (‘basal’:
Po0.0001; ‘transfer’: Po0.0001; ‘isolation’:
Po0.0001) (Figure 2). The increase of T
b
during the various experiments is presented
in Table 1.
Influence of different recording methods on
the effect of stress paradigms on T
b
Repeated ANOVA showed a significantly
lower T
b
in the ‘rec’ group in the ‘basal’
(P ¼ 0.0001) and the ‘transfer’ (P ¼ 0.003)
experiments. But no significant effects of
the rectal measurement could be found
when T
b
of the ‘iBut’ and the ‘rec þ iBut’
group were analysed for the different
stress paradigms.
Laboratory Animals (2006) 40
190 R Dallmann et al.
0 30 60 90 120
36
37
**
***
Rectal
iButton
Temperature [°C]
Time [min]
Figure 1 Body temperature (1C) development by
rectal and Thermochron iButton recording within the
‘rec þ iBut’ group during the ‘basal’ experiment at
given times. Results are shown as means7SEM
(n ¼ 9–10). Significant T
b
differences between
recording methods (rectal versus Thermochron
iButton recording) are indicated by stars (

Po0.01;

Po0.001)
Figure 2 Body temperature (1C) development for the different stress paradigms (a: ‘basal’; b: ‘transfer’;
c: ‘isolation’) at given times. Results are shown as means7SEM (n ¼ 9–10). For details see text

Influence of stress on daily T
b
rhythm
As depicted in Figure 3, the rats showed a
clear diurnal rhythm of body temperature
with low values during the inactive light
phase (36.970.11C) and high values at the
active dark phase (37.470.11C) in both
implanted groups (‘iBut’ and ‘rec þ iBut’).
As analysed in detail above, the body
temperature experiments had a dramatic
acute effect on T
b
, which was as high as the
rise at the beginning of the night, although
the peaks were clearly distinct from the
onset of the nightly temperature rise.
However, the experiments did not alter
either the onset (64723 min after lights off)
or offset (21719 min after lights on) of the
nightly rise in temperature.
Discussion
This study was undertaken to investigate
the influence of different common stressors
on the body temperature (T
b
) of laboratory
rats and to validate a new method for T
b
measurement. We have demonstrated that
different stressors such as (i) moving the
home cage within the holding rooms, (ii)
transferring animals between holding and
test room or (iii) isolation of animals after
such a transfer each have a strong increasing
impact on the animals T
b
for at least the
following 60 min. Furthermore, we found
that a new industrial technique
(Thermochron iButtons) delivers much more
accurate and reliable T
b
data than rectal T
b
recording.
Moving the rats within their home cage in
the holding room resulted in a significant
elevation in T
b
of more than 0.51C for the
following 120 min (‘iBut’ group). Thus,
moving cages within the holding room, i.e.
transferring the cage from a rack to a table,
has to be regarded as a stressor itself. This
finding is in accordance with studies
Laboratory Animals (2006) 40
Body temperature recording methods 191
Table 1 Average increase of body temperature (1C) compared with the initial T
b
value (0 min) within the
three recording groups ‘rec’, ‘iBut’, and ‘rec+iBut’ during the various experiments at given times
Experiment Recording time (min) ‘rec’ ‘iBut’ ‘rec + iBut’
‘Basal’ 30 1.270.27 0.5470.08 0.8070.14
60 0.9070.43 0.6370.09 0.7770.16
90 1.170.26 0.5670.10 0.5470.15
120 1.170.32 0.5370.11 0.6870.15
‘Transfer’ 30 0.9470.28 0.8770.10 0.7670.14
60 0.7670.23 0.9270.12 0.8370.13
‘Isolation’ 30 1.370.21 1.070.13 0.7670.12
60 1.470.15 1.170.11 0.8770.13
Results are shown as means7SEM (n=9–10)
24 48 72 96 120
36.5
37.0
37.5
38.0
Temperature [°C]
Time [h]
Figure 3 Time course of body temperature for all implanted animals (‘iBut’
and ‘rec þ iBut’ group; n ¼ 19) shown as means (black) and SEM (grey). The
arrows indicate the start of the different stress paradigms. Note the T
b
peak in
the early day after the first night. This was due to cage changing

showing that cage switching and even gentle
handling of animals results in a significant
rise in T
b
(Briese & De Quijada 1970, Long
et al. 1990). The knowled ge that this rise in
temperature is not simply the result of
metabolic changes but a regulated process
with associated changes in physiology (Long
et al. 1990, Nakamori et al. 1993, Groenink
et al. 1994) shows that standardized and
gentle handling procedures are of great
importance in animal research using rats
(see also: Eikelboom 1986). The other two
stress paradigms (transportation and/or
isolation) were shown to be effective in
increasing T
b
over time and these elevations
lasted for at least 60 min. Thus, the
commonly used habituation period of 60 min
after transportation is very likely a too brief
period between transport/isolation and
testing. Since the T
b
elevation lasted for at
least 120 min in the ‘basal’ test, habituation
periods of up to 120 min or even longer seem
to be necessary.
Furthermore, we compared different
methods for measuring body temperature
in rats. Thermochron iButton recording
revealed higher T
b
values than when rectally
recorded. These findings are based on the
fact that iButtons are located much closer to
the liver, which is the main heat-producing
organ in the abdomen (Birnie & Grayson
1952), than the rectally inserted probe.
Furthermore, the higher variation in rectal
measurements compared with iButton
values in the basal experiments suggests that
rectal measurements are less reliable.
Besides this overall difference between the
two recording methods we could not detect
any major influence of the two recording
methods on the different stress paradigms as
the relative T
b
rise was comparable in the
rectal (‘rec þ iBut’) and iButton recording
groups (‘iBut’).
Rectal measurement only slightly affected
T
b
of rats compared with for example
moving the cage within the holding room.
This finding is contradictory to other studies
showing marked elevations of T
b
in rats
(Poole & Stephenson 1977) and mice (Van
der Heyden et al. 1997) after rectal
measurement. In our study, however,
animals were habituated to handling prior to
the experiments and the rectal recording of
T
b
was limited to 20 s, which might have
reduced its effect on T
b
development. The
two main problems of standardization in
rectal recording of T
b
are variations in the
necessary handling of the animals and the
depth of the probe insertion and thus, the
distance to the liver, which has been
previously reported (Lomax 1966, Van der
Heyden et al. 1997). Furthermore, it has to
be mentioned that although main stress
effects can also be detected by rectal
recordings the Thermochron iButtons are
more precise and measure the T
b
at the same
location within the peritoneal cavity each
time. Thermochron iButtons avoid these
standardization difficulties and can be an
alternative, highly standardized recording
method assuring correct T
b
recordings. Main
stress effects can also be detected by rectal
recording but Thermochron iButtons are
more precise and the time resolution of the
model used in our study has recently been
improved as a new model of Thermochron
iButtons (DS1922T) became available. This
model can store more data (4-fold compared
with the model used in our study) and offers
an even higher temperature resolution.
Therefore, it could be used for long-term
measurements (e.g. in chronobiological
studies) and thereby corrects for a former
major disadvantage of telemetric systems
(Davidson et al. 2003). This advantage of
using iButtons for a longer period of time
offers the possibility to continuously control
for disturbances of the animals as these
disturbances can have an influence on the
animal’s performance in for example
behavioural tests. For example, in our study
the weekly cage cleaning by the animal
caretaker resulted in a T
b
rise in the morning
of the ‘basal’ test day, which was as high as
the one caused by the ‘basal’ test itself.
In conclusion, we demonstrate that
different stress paradigms result in
significant T
b
elevations. These increases in
T
b
last for longer than 60 min, suggesting
that long periods of habituation (e.g. to a
testing room) are necessary for baseline
measures. Importantly, moving the cage
within the holding room results in
significant elevations in T
b
, as well, showing
Laboratory Animals (2006) 40
192 R Dallmann et al.

the importance of gentle and standardized
handling of laboratory animals (Levine
1957). The use of Thermochron iButtons for
recording body temperature results in more
precise and more standardized data although
rectal recording is still a valuable tool for
single but not repeated T
b
studies. Thus, this
new technique provides a good alternative
for better standardized T
b
measurements in
rodents. Ongoing studies will not only
investigate specific stress levels induced by
the various procedures (e.g. plasma
corticosterone levels or other parameters)
but also modify the time course by
measuring T
b
of test animals for up to
180 min after stress induction.
Acknowledgements The authors thank Frank
Scherbarth and Michael Stephan for assistance with
the surgery and recovery of the iButtons. The DFG
(Graduiertenkolleg 705 and Forschungsstipendium Ka
1837/1-1) supported this work. The critical comments
by Nicholas Mrosovsky, Liesl Duffy, Patricia
Hedenqvist, two anonymous reviewers, and Jerry
Tanda on the manuscript are gratefully acknowledged.
This work was carried out at the Institute of
Laboratory Animal Science, Hannover Medical
School, 30623 Hannover, Germany.
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