Original Article

Laboratory Animals
0(0) 1–9
! The Author(s) 2019
Warming and cooling device using Article reuse guidelines:
sagepub.com/journals-permis-
thermoelectric Peltier elements tested sions
DOI: 10.1177/0023677219873687
on male mice journals.sagepub.com/home/lan

Nodir Madrahimov1,* , Ruslan Natanov1,*, Abdurasul Khalikov1,

Erin C Boyle1,2, Danny Jonigk3, Ann-Katrin Knoefel1,
Thierry Siemeni1 and Axel Haverich1

Abstract
Hypothermia is a treatment strategy for different clinical conditions and an essential part of cardiopulmonary
bypass in complex cardiac procedures. Clinically, cooling patients is achieved via a mattress and heat exchan-
ger integrated into a membrane oxygenator connected to a waterbed using a refrigerator system based on
volatile and toxic liquids. Peltier elements are known as environmentally friendly thermoelectric generators
that enable rapid warming and cooling. In this paper, we describe the construction of a novel device for rapid
and precise control of mouse warming and cooling using thermoelectric Peltier elements. Six male BALB/c
mice were subjected to deep hypothermia and were rewarmed under full physiological monitoring. After
rewarming, all animals were observed for two hours, and pathology was evaluated in several organs. All
animals tolerated the rapid cooling process well and remained active after rewarming. Temperature-relevant
changes were seen via electrocardiography, with heart-rate patterns showing a strong linear correlation to
body temperature. No myocardial ischaemia was seen. However, two animals experienced bradycardic atrial
fibrillation which spontaneously converted to normal sinus rhythm during rewarming. No histological damage
was seen in the heart, liver, kidney or lungs. Our device can effectively be used for heat shock and hypother-
mia studies in mice, and we foresee no obstacles for its application to other small rodents such as hamsters
and young rats. In comparison to known experimental and clinical methods of hypothermia, our device is
environmentally friendly, cost-effective and easy to handle, allowing precise control and maintenance of body
temperatures ranging from 18 C to 42 C.

Keywords
mouse, hypothermia, warming, temperature control, thermoelectric Peltier elements
Date received: 19 February 2019; accepted: 11 August 2019

Introduction
1
Small-animal surgical research is important for under- Department of Cardiothoracic, Transplantation and Vascular
Surgery, Hannover Medical School, Hannover, Germany
standing various pathophysiological processes and for 2
Institute of Laboratory Animal Science, Hannover Medical School,
the development of innovative surgical procedures. Hannover, Germany
During experimental surgery, animals are prone to 3
Department of Pathology, Hannover Medical School, Hannover,
hypothermia in both thoracic and abdominal proced- Germany
ures due to their high surface area to mass ratio.1,2 *These authors equally contributed to this work.
Hypothermia may affect various physiological processes
such as blood clotting,3,4 haemodynamics5,6 and Corresponding author:
Nodir Madrahimov, Department of Cardiothoracic and Thoracic
pharmacological availability of various substances.7,8 Vascular Surgery, University Hospital Würzburg, Würzburg,
Therefore, intraoperative temperature management of Germany.
the animal plays a pivotal role in postoperative Email: Madrahimov_N@ukw.de
2 Laboratory Animals 0(0)
outcome.9 On the other hand, certain small-animal sur-
geries require, test or model therapeutic hypothermia
(TH; also known as targeted temperature management
or protective hypothermia). TH is used clinically in
cardiac surgery and is a neuroprotective strategy with
many clinical indications, including the treatment of car-
diac arrest and stroke survivors, traumatic head injuries,
newborn hypoxic–ischaemic encephalopathy and neuro-
surgery, and has been applied in cases of acute respira-
tory distress syndrome (ARDS).10 During human
procedures, cooling is achieved via a mattress and heat
exchanger integrated into the membrane oxygenator
connected to a waterbed. Such systems use chlorofluoro-
carbons, also known as ‘vapour’ or R-12 in the refriger-
ator manufacturing industry. These substances are
classified as volatile, toxic and ozone-depleting, and
most of them are now forbidden or severely regulated
since the adoption of the Montreal Protocol in 1987.
We recently developed a model of cardiopulmonary
bypass (CPB) in mice whereby moderate hypothermia
was achieved by topically cooling the animals with
gauze soaked in a cold saline solution.11 This com-
monly used method lacks precise temperature control.
To optimise experimental CPB procedures with extra-
corporeal circulation and hypothermic phases in small
animals, precise temperature modulation is needed. The
use of clinically used cooling systems in this context is
limited in its application due to its size, costs and com-
plicated maintenance. Therefore, an environmentally
friendly, cost-effective and easy-to-handle device for
temperature management in small animals is needed.
In this paper, we describe the construction of a novel
device for rapid and precise control of mouse warming
and cooling using thermoelectric Peltier elements.
Materials and methods
Animals
Six male BALB/c mice were obtained from Charles
River. Animals weighing between 25 and 35 g were uti-
lised for the experiments. This study was conducted in
compliance with the German Animal Protection Law.
The animal protection committee of the local authori-
ties (Lower Saxony State Department for Food Safety
and Animal Welfare (LAVES)) approved all experi-
ments (Approval: 33.12-42502-04-14/1556).
Device construction
A square aluminium plate (20 cm  30 cm  0.7 mm)
was used as the main board for cooling and warming
the animal. A 12 V/60 W thermoelectric Peltier cooler/
heater (TEC1-12706; Hebei IT Co. Ltd) was glued to
the backside of the plate using thermic glue (Thermal
Adhesive; MG Chemicals). Adjacent to the thermal
element, seven copper plates equal in size to the alu-
minium board were adhered. The copper plates were
joined together using small round-shaped aluminium
pads (30 mm  1 mm) that allowed enough space
between the metal plates for proper heat dissipation.
Usually, as one side of the Peltier element heats, the
other side cools and vice versa. Therefore, it was
important to avoid backside overheating of the thermal
element during cooling of the animal. Therefore, to
increase heat dissipation further, all copper plates
were connected to an aluminium heat sink (Xilence;
AM2.HP) using thermic glue and were ventilated by
three cooling fans. This allowed for effective and
stable deep cooling of the main aluminium board for
several hours. For temperature regulation, an NTC 1 K
temperature sensor (Vishay BC Components, Vishay
Intertechnology, Inc.) was connected between a tem-
perature controller (ITC-1000; Inkbird Tech. Co. Ltd)
and the aluminium board. A second temperature sensor
was coated with a polymerised resin and connected to a
second temperature controller (ITC-1000; Inkbird
Tech. Co. Ltd). This was used as a rectal probe. A
reversible switch was placed between the power
supply and the Peltier element for convenient switching
from cooling to heating. For an illustration of
the heating/cooling pad, see Figure 1. For detailed spe-
cifications of device components, see Supplemental
Table S1.
Anaesthesia
Animals were anaesthetised with isoflurane in an induc-
tion chamber. After successful anaesthesia was
achieved, animals were placed onto the thermal plate.
Further maintenance of anaesthesia throughout the
experiment was achieved using mask inhalation of
vaporised isoflurane under control of spontaneous
breathing. The concentration of isoflurane anaesthesia
was maintained between 1.3% and 2.5% in oxygen,
depending on the stage of the procedure, with a con-
stant flow rate of 0.5 L/min.
Experimental set-up
After induction of anaesthesia, animals were placed on
the thermal plate and initially kept at normothermia.
Electrocardiography (ECG), rectal temperature and
invasive pressure were monitored using a Multichannel
Data Acquisition System (Hugo Sachs Elektronik
GmbH). ECG needle electrodes were placed subcutane-
ously in the right and left forelimb and in the left thor-
acic wall. Afterwards, a 5 mm incision was made in the
left inguinal area, and the femoral artery was separated
from the femoral nerve and vein in a sharp and blunt
Madrahimov et al. 3

Figure 1. Schematic design of (a) the heating/cooling small-animal pad and (b) the final device.

Figure 2. Surgical set-up using real-time electrocardiography, invasive arterial pressure and temperature control.

manner under a microscope at 16–25  magnification.
The distal part of the artery was ligated, and the prox-
imal part was temporarily ligated using a slip knot with
an 8-0 silk suture. After incision of the anterior wall of
the artery, a 1 Fr polyurethane cannula (Instechlabs,
Inc.) was inserted and moved towards the iliac artery.
Afterwards, the invasive pressure tubing was then con-
nected to a pressure transducer. Visualisation of the sur-
gical set-up is displayed in Figure 2. Cooling of the
animal was initiated by setting the heating/cooling pad
to 15 C. Under stable haemodynamic conditions, the
temperature of the animal was lowered to deep hypo-
thermia (down to 20 C). This temperature was kept for a
further 10 minutes. Next, the animal was rewarmed to
normal core body temperature. During rewarming, the
difference between the plate and rectal temperature was
kept <6–8 C (similar to the clinical guidelines of <10 C
for CPB) to avoid air micro-embolisation of the
animal.12 After the animal regained normal body tem-
perature with stable haemodynamic conditions,
4 Laboratory Animals 0(0)
anaesthesia was terminated, and the animal was allowed
to wake up.
Clinical observation
Postoperative observation included assessment of the
behaviour, activity and examination of the body of
the animal for two hours after waking up.13
Organ harvesting and histology
Two hours after waking up, all animals were subjected
to isoflurane euthanasia followed by exsanguination
and organ harvesting. To assess potential organ
damage, the heart, lung, liver and kidneys were har-
vested for routine histology. All organs were fixed in
4% formalin and were subjected to paraffinisation and
hematoxylin and eosin (H&E) staining. Organs were
evaluated for signs of acute cold or heat damage in
the form of cell death, inflammatory cell infiltration,
thrombosis or oedema.
Statistical analysis
All data obtained using ISOHEART Software (Harvard
Apparatus) were analysed using GraphPad Prism 5.0
(GraphPad Software, Inc.), and the correlation between
parameters was calculated after Pearson analysis.
Results
Animal rectal temperature and plate
temperature
During the experiments, the temperature of both the
animal and the thermal pad was monitored
Figure 3. Animal and pad temperature (SD) over time during the cooling and rewarming period of the experiment.
Animals were rewarmed in a gradual manner to prevent air micro-embolisation.
continuously in real time (Figure 3). The average initial
animal temperature was 35.52  0.51 C and fell to
20.35  1.05 C within 40 minutes of the initiation of
cooling. The maximal cooling rate was 0.4 C/min.
The rewarming of the animal lasted more than 65 min-
utes, with animals reaching 35.05  0.18 C during this
time. It should be noted that the increase in plate tem-
perature was performed in a stepwise manner, thus
keeping the difference in plate and body temperature
well below 10 C (6–8 C). During rapid cooling, the
maximal temperature difference was 14.79 C, while
during rewarming it did not exceed 6.73 C. Stepwise
warming of the animal was easily managed by changing
the setting temperature on the controller every
10 minutes.
Haemodynamic monitoring
Haemodynamics were monitored in real time during
the course of experiments. At the start of the experi-
ment, the average heart rate was 612.83  89.24 bpm
and dropped during deep hypothermia to
232.33  33.69 bpm (Figure 4(a)). After rewarming,
the average heart rate was 692.33  72.11 bpm
(Figure 4(a)). No myocardial ischaemia was seen on
ECG during the experiments. Nevertheless, in two of
six animals, bradycardic atrial fibrillation was
observed at the deepest point of cooling, which spon-
taneously converted to a normal rhythm after rewarm-
ing the animal. Heart-rate patterns showed a strong
linear correlation to body temperature by Pearson
analysis (r ¼ 0.857, p < 0.0001; Figure 4(b)). Invasive
blood-pressure measurements showed a stable mean
arterial pressure (MAP) throughout the whole experi-
ment. During normothermic conditions, deepest hypo-
thermia and at the end of the rewarming period,
Madrahimov et al.
Figure 4. Haemodynamic monitoring during hypothermia and rewarming. Values are expressed as means  SD. (a) Heart
rate over time, (b) the relationship between heart rate and rectal temperature, (c) mean arterial pressure (MAP) and (d)
variables normalised to initial measurements (time ¼ 0 min). n ¼ 6. Pearson analysis showed a correlation between heart
rate and temperature (r ¼ 0.0857, p < 0.0001).
MAP averaged 85.75  3.64, 84.35  2.35 and 85.7 
2.86 mmHg, respectively (Figure 4(c)). Figure 4(d)
shows the data normalised to initial measurements
(time ¼ 0 minutes).
Clinical condition after waking up
All animals fully recovered 30 minutes after narcosis
was terminated. No changes in activity, including
drinking and eating behaviour, were observed during
the two-hour observation time. Upon investigation of
the body, special attention was given to the assessment
of the backside of the animal that had a large surface
contact to the cooling/heating board. No lesions or
changes in the fur pattern or skin were detected in
any of the animals.
Histological evaluation
Histological investigation of H&E sections revealed no
detectable changes to the heart, lung, liver or kidney.
There were no signs of organ oedema, necrosis, micro-
thrombosis or cellular infiltration which would be
expected upon organ damage (Figure 5).
5
Discussion
We have developed and tested a novel temperature-
controlled heating and cooling plate for preclinical
murine research. It allows for precise thermoregulation
and was proven safe for animals undergoing deep hypo-
thermia and rewarming. Tight control of the heating/
cooling plate is crucial, as seen by Roehl et al.14 who
observed renal injury in rats undergoing surgery due to
accidental overheating of a thermal heating plate.
Although only tested on male BALB/c mice, we foresee
no obstacles for its application to other strains of mice,
female mice or other small rodents such as hamsters
and young rats. In addition, the plate could easily be
made bigger to accommodate larger rodents such as
adult rats and rabbits.
To date, methods to achieve small-animal hypother-
mia have required surgery or intervention15 (Figure 6),
and in all cases, precise thermoregulation was not pos-
sible. Furthermore, hypothermia requiring surgical
intervention makes it less suitable for immunological
research, as any kind of surgical procedure initiates
cytokine production and possibly a humoral
response.16,17 In the study by Leker et al.,18 the use of
6 Laboratory Animals 0(0)
Figure 5. Hematoxylin and eosin staining of (a) murine myocardium, (b) lung tissue, (c) kidney and (d) liver after hypo-
thermia and rewarming. 200  magnification.
cannabinoid agonist HU-210 to induce hypothermia
showed significant side effects. There are also safety
concerns in the model used by Florian et al.19 where
a hydrogen sulphite/air mixture was applied for inhal-
ation in rats. Xue et al.20 used a neurotensin receptor
agonist to develop therapeutic hypothermia in a rat
stroke model. However, only mild hypothermia was
achieved. They used an ice pad to achieve mild hypo-
thermia for 10 hours in rats, and the rewarming process
lasted more than two hours. We would argue, however,
that it is still difficult to control body temperature using
precooled pads. In contrast, using our device, tempera-
ture changes in the animals can be adjusted individu-
ally, depending on their size, weight, age and strain.
All cooling devices used in clinical practice are based
on standard refrigerating systems connected to a water
bath. Powerful pumps maintain circulation of the toxic,
volatile liquids through a cooling bed with the help of a
tubing system. Such devices are big, consume a lot of
energy and have the problem of excessive heat produc-
tion. The thermoelectric effect was first described by
French physicist Jean Charles Athanase Peltier in 1834
who discovered heat or cold could be generated between
two different materials under an electric charge cur-
rent.21–23 Recently, the production of thermoelectric
coolers or freezers has gained popularity, and thermo-
electric elements are common in laboratory polymerase
chain reaction thermocyclers where quick changes in
temperature are required. We based our murine heat-
ing/cooling device on thermoelectric Peltier elements,
as they are cost and energy efficient, versatile, reliable,
durable and of minimal size. Having non-moving parts,
they require minimal maintenance, are completely noise
and vibration-free and contain no flammable materials.
Importantly, reversal from cooling to heating is
achieved by simply changing the polarity of the cur-
rent.24 Prior research showed effective thermoregulation
of brain tissue using Peltier elements.25
Our device has numerous other benefits. The con-
struction of our murine heating/cooling plate used min-
imal resources, with all required parts easily available
and inexpensive. It was designed as an operating table
that facilitates performance of any surgical intervention
with thermoregulation between 18 C and 42 C.
Moreover, it can be successfully applied in heat shock
models. Unlike other models of hypothermia, it does
not require any surgical intervention, and therefore no
tissue damage occurs prior to initiating the experiment.
Hence, all animals subjected to thermoelectric hypo-
thermia tolerated the procedure well and recovered
fully after rewarming. Mice cooled below 20 C risk
both cardiac and respiratory arrest.26 As our animals
did not have extracorporeal support, animals were kept
no longer than 10 minutes after achieving our goal tem-
perature of 20 C. Usually, patients on cardiopulmon-
ary bypass can be cooled down to 18 C or even 16 C
Madrahimov et al.
Figure 6. Overview of the available methods of small-animal hypothermia induction.
for several hours, depending on the type of surgery. In
the future, we will use this device to test the effect of
therapeutic hypothermia (<20 C for up to one hour)
on the prevention of multi-organ damage in a murine
model of extracorporeal circulation.11,27
Acknowledgements
We thank Slavica Schümann for her excellent technical assist-
ance in this project.
Declaration of conflicting interests
The author(s) declared no potential conflicts of interest with
respect to the research, authorship and/or publication of this
article.
Funding
The author(s) disclosed receipt of the following financial sup-
port for the research, authorship and/or publication of this
article: This research was internally funded by the
7
Department of Cardiothoracic, Transplantation, and
Vascular Surgery at the Hannover Medical School.
ORCID iD
Nodir Madrahimov https://orcid.org/0000-0001-8434-
7324
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Résumé
L’hypothermie est une stratégie de traitement pour différentes conditions cliniques qui constitue une partie
essentielle de la circulation extracorporelle lors des interventions de chirurgie cardiaque complexes. Sur le
plan clinique, le refroidissement des patients s’effectue par l’intermédiaire d’un matelas et d’un échangeur de
chaleur intégré dans un oxygénateur à membrane connecté à un lit à eau à l’aide d’un système de réfrigéra-
tion reposant sur des liquides toxiques et volatiles. Les modules Peltier sont connus pour constituer des
générateurs thermoélectriques respectueux de l’environnement permettant un réchauffement et un refroi-
dissement rapides. Dans ce document, nous décrivons la construction d’un nouveau dispositif de contrôle
rapide et précis du réchauffement et du refroidissement des souris à l’aide de modules Peltier thermoélec-
triques. Six souris BALB/c mâles ont été soumises à une hypothermie profonde et réchauffées sous surveil-
lance physiologique complète. Après réchauffement, tous les animaux ont été observés pendant deux heures
et la pathologie a été évaluée dans plusieurs organes. Les animaux ont tous bien toléré le processus de
refroidissement rapide et sont restés actifs après le réchauffement. Les changements de température ont été
Madrahimov et al. 9

relevés par électrocardiographie avec des rythmes cardiaques montrant une forte corrélation linéaire à la
température du corps. Aucune ischémie myocardique n’a été observée mais deux animaux ont souffert d’une
fibrillation auriculaire avec bradycardie qui s’est spontanément transformée en un rythme sinusal normal
pendant le réchauffement. Aucun dommage histologique n’a été observé au niveau du cœur, du foie, des reins
ni des poumons. Notre appareil peut effectivement être utilisé pour des études sur l’hypothermie et le choc
thermique chez les souris et nous ne prévoyons aucun obstacle à son application à d’autres petits rongeurs
tels que les hamsters et les jeunes rats. En comparaison aux méthodes expérimentales et cliniques de
l’hypothermie, notre appareil est respectueux de l’environnement, rentable et facile à manipuler ce qui
permet un contrôle précis et le maintien de la température du corps de 18 à 42 C.

Abstract
Hypothermie ist eine Behandlungsstrategie für verschiedene klinische Zustände und ein wesentlicher
Bestandteil des kardiopulmonalen Bypasses bei komplexen Herzeingriffen. Die Kühlung der Patienten erfolgt
klinisch über eine Matratze und einen Wärmetauscher, die in einen Membranoxygenator integriert sind, der mit
einem Wasserbett verbunden ist und ein auf flüchtigen und giftigen Flüssigkeiten basierendes Kühlsystem
verwendet. Peltier-Elemente gelten als umweltfreundliche thermoelektrische Generatoren, die eine schnelle
Erwärmung und Abkühlung ermöglichen. In diesem Artikel beschreiben wir den Aufbau eines neuartigen
Geräts zur schnellen und präzisen Steuerung der Erwärmung und Abkühlung von Mäusen mithilfe von thermo-
elektrischen Peltier-Elementen. Sechs männliche BALB/c-Mäuse wurden einer tiefen Hypothermie ausgesetzt
und unter umfassender physiologischer Überwachung wieder erwärmt. Nach dem Wiedererwärmen wurden
alle Tiere zwei Stunden lang beobachtet und die Pathologie mehrerer Organe wurde bewertet. Alle Tiere
vertrugen die schnelle Abkühlung gut und blieben nach dem Aufwärmen aktiv. Temperaturrelevante
Veränderungen wurden mittels Elektrokardiographie mit Herzfrequenzmustern beobachtet, die eine starke
lineare Korrelation zur Körpertemperatur zeigten. Es wurde keine myokardiale Ischämie beobachtet, jedoch
trat bei zwei Tieren bradykardes Vorhofflimmern auf, das während des Erwärmens spontan in einen normalen
Sinusrhythmus überging. Es wurden keine histologischen Schäden an Herz, Leber, Niere oder Lunge festges-
tellt. Unser Gerät kann effektiv für Hitzeschock- und Hypothermiestudien an Mäusen verwendet werden, und
wir sehen keine Hindernisse für seinen Einsatz bei anderen kleinen Nagetieren wie Hamstern und jungen
Ratten. Gegenüber bekannten experimentellen und klinischen Methoden der Hypothermie ist unser Gerät
umweltfreundlich, kostengünstig und einfach zu handhaben und ermöglicht die präzise Kontrolle und
Einhaltung von Körpertemperaturen im Bereich von 18 bis 42 C.

Abstracto
La hipotermia es una estrategia de tratamiento para diferentes condiciones clı́nicas y una parte esencial del
bypass cardiopulmonar en procedimientos cardı́acos complejos. Clı́nicamente, el enfriamiento de los pacientes
se consigue mediante un colchón y un intercambiador de calor integrado en un oxigenador de membrana que va
conectado a un colchón de agua mediante un sistema de refrigeración basado en lı́quidos volátiles y tóxicos. Los
elementos Peltier se conocen como generadores termoeléctricos respetuosos con el medio ambiente que
permiten un calentamiento y enfriamiento rápidos. En este artı́culo describimos la construcción de un dispo-
sitivo novedoso para el control rápido y preciso del calentamiento y enfriamiento de ratones mediante elemen-
tos Peltier termoeléctricos. Seis ratones macho BALB/c fueron sometidos a hipotermia profunda y recalentados
bajo control fisiológico completo. Después del recalentamiento, todos los animales fueron observados durante
dos horas y se evaluó la patologı́a en varios órganos. Todos los animales toleraron bien el rápido proceso de
enfriamiento y permanecieron activos después del recalentamiento. Los cambios relevantes para la temper-
atura se observaron mediante electrocardiografı́a con patrones de frecuencia cardı́aca que muestran una fuerte
correlación lineal con la temperatura corporal. No se observó isquemia miocárdica, sin embargo, dos animales
experimentaron fibrilación auricular bradicárdica que se convirtió espontáneamente en ritmo sinusal normal
durante el recalentamiento. No se observó ningún daño histológico en el corazón, hı́gado, riñón o pulmones.
Nuestro dispositivo puede ser utilizado eficazmente para estudios de choque térmico e hipotermia en ratones y
no prevemos inconvenientes para su aplicación en otros roedores pequeños como hámsters y ratas jóvenes. En
comparación con los métodos experimentales y clı́nicos conocidos de la hipotermia, nuestro dispositivo es
respetuoso con el medio ambiente, económico y fácil de manejar, lo que permite un control preciso y el
mantenimiento de las temperaturas corporales entre los 18 y los 42 C.