Positive selective brain cooling method: a novel, simple, and

Acta Neurochir (2006) [Suppl] 96: 409–412
6 Springer-Verlag 2006
Printed in Austria
Positive selective brain cooling method: a novel, simple,
and selective nasopharyngeal brain cooling method
K. Dohi1, H. Jimbo2, T. Abe2, and T. Aruga1
1 Department of Emergency and Critical Care Medicine, Showa University School of Medicine, Tokyo, Japan
2 Department of Neurosurgery, Showa University School of Medicine, Tokyo, Japan
Summary
Brain damage is worsened by hyperthermia and prevented by hypothermia. Conventional hypothermia is a non-selective brain cooling method that employs cooling blankets to achieve surface cooling.
This complicated method sometimes induces unfavorable systemic
complications. We have developed a positive selective brain cooling
(PSBC) method to control brain temperature quickly and safely following brain injury.
Brain temperature was measured in patients with a ventriculostomy CAMINO catheter. A Foley balloon catheter was inserted to
direct chilled air (8 to 12 L/min) into each side of the nasal cavity.
The chilled air was exhaled through the oral cavity. In most patients,
PSBC maintained normal brain temperature. This new technique
provides quick induction of brain temperature control and does not
require special facilities.
Keywords: Brain damage; hypothermia; selective brain cooling.
Introduction
Neurons are more vulnerable to hyperthermia compared to other types of cells [21]. Brain temperature
(Tb) elevates during the early phase of severe brain
damage caused by cerebral vascular accidents or severe head injury [7] for many reasons, including hypothalamic injury, abnormal release of catecholamines,
and production of endogenous pyrogens [7, 8]. Brain
cooling mechanisms become unbalanced and dysfunctional from the heat production and loss that occurs
during hyperthermia caused by brain damage. Hyperthermia caused by brain damage induces secondary
brain damage [6]. Induction of mild brain hypothermia (33 to 35 C) or normothermia (35 to 37 C) by
body surface cooling blankets has been shown to be
neuroprotective in patients [2, 8, 11, 12, 17, 20]. Slight
alterations in temperature have profound e¤ects on ischemic cell injury and stroke outcome. Elevated Tb,
even if slight, may exacerbate neuronal injury and
worsen outcome, whereas hypothermia is potentially
neuroprotective. Maintenance of normothermia is the
most commonly recommended treatment for stroke
and neurotrauma [14, 15]. However, conventional hypothermia is a complicated method that sometimes induces systemic complications [12]. A safe and e¤ective
brain cooling method is needed to treat patients with
brain damage.
Mammals, including humans [1, 3, 4, 13, 16, 18, 19],
have selective brain cooling (SBC) systems [9, 10, 19],
one of which is nasopharyngeal cooling. Nasopharyngeal cooling was recently used to reduce cortical
and subcortical temperatures rapidly and selectively
without a¤ecting the systemic circulation after resuscitation in the rat [10]. In this brief technical note, we
describe a simple and selective nasopharyngeal brain
cooling method that does not employ cooling blankets.
Methods
Method of positive selective brain cooling (PSBC)
Tb was measured directly in brain-injured patients with a ventriculostomy CAMINO catheter (ICP and Tb sensor; 4HMT, Integra
NeuroCare, Hampshire, UK). The PSBC method was performed to
cool the brain rapidly. A 16F Foley catheter (Temperature-Sensing
Foley Catheter, C.R. Bard, Inc., Murray Hill, NJ) was inserted to
blow chilled air (8 to 12 L/min) directly into the nasopharyngeal passage. To direct air from there into the oral cavity, one nasal cavity
was occluded by an epistaxis balloon (Eschman Healthcare, Inc.,
Malaysia) at the inlet. Chilled air (24 to 26 C) was expelled through
K. Dohi et al.
410
Fig. 1. Positive selective brain cooling (PSBC ) performed by
nasopharyngeal cooling. Artificial nasopharyngeal circulation with
chilled air (24 C, 8 to 12 L/min). Chilled air cooled nasal mucosa
and nasal mucosa veins (A). Chilled air also cooled the brain and
CSF directly (B). Cerebral blood is also chilled by heat exchange between the internal carotid artery (ICA) and cavernous sinus (CS)
the oral cavity (Fig. 1, arrows a and b). Nasal and pharyngeal mucosa were kept clean by irrigation with physiologic saline. We also
cooled the patient’s head with an electric fan.
Contraindications of PSBC
PSBC is contraindicated in cases of sinusitis or skull base fracture.
The procedure should be performed in sedated patients. The procedure may cause an oppressive feeling due to the high volume of circulating air.
Results
Brain temperature
Elevated Tb dropped to within the range of normothermia (37 C > Tb) in most patients. The initial temperatures of the nasal cavities and exhaust air were
very high despite the flow of chilled air. However,
these temperatures fell within a short time.
Fig. 2. (a) The change in brain temperature (Tb) after PSBC induction in a tracheal intubated patient with subarachnoid hemorrhage.
Tb was decreased to 34 C without employing surface cooling. (b)
The change in brain temperature (Tb) after PSBC induction in a tracheal intubated patient with severe neurotrauma. Tb was elevated to
39 C and decreased to 37 C without the use of surface cooling. Exhaust temperature (Tex) was also elevated before the induction of
PSBC
Case illustrations
Case 1
A 62-year-old woman was admitted to our hospital.
She was comatose (Glasgow Coma Scale; E1V1M2).
Computed tomography of the brain revealed di¤use,
thick, subarachnoid hemorrhage. Nasopharyngeal
brain cooling by PSBC was performed immediately.
Initial Tb was 37.8 C, and Tb rapidly decreased to
34.0 C 45 minutes after induction (Fig. 2a).
Case 2
Complications of PSBC
In general, PSBC was performed for a short period.
Several patients developed erosion localized to the nasal foramen. Sinusitis, tympanic membrane injury, and
dysosmia were not observed.
A 26-year-old man admitted to our hospital was
diagnosed with severe neurotrauma. PSBC by nasopharyngeal cooling was performed immediately. Initial Tb was 39.0 C, which rapidly decreased to 37.0 C
120 minutes after induction. Exhaust air temperature
Positive selective brain cooling method: a novel, simple, and selective nasopharyngeal brain cooling method
(Tex) was also elevated on induction and decreased
rapidly (Fig. 2b).
Discussion
SBC system in humans
Mammals have a natural SBC system [9, 10, 19]. Tb
is controlled by a balance between heat production/
acquisition and heat loss. Heat loss occurs through
heat transference from the core of the brain through
blood flow, evaporative heat loss through breathing
and sweating, and non-evaporative heat loss through
breathing. Moreover, heat exchange between the internal carotid artery and venous plexus or cavernous sinus is simple and e¤ectively functions like a radiator.
The importance of each cooling mechanism di¤ers
among animal species. For example, heat exchange
and evaporative heat loss through breathing is the
main mechanism in dogs, which have a small number
of sweat glands. Mechanisms of SBC in humans are
not well-developed in comparison to other mammals.
The human brain is believed to have 3 cooling mechanisms. One is cooling of venous blood through the entire skin surface, which in turn cools the arterial blood
supply to the brain. A second is cooling by heat loss
through the skin via the venous sinuses and diploic
and emissary veins. The third mechanism of cooling is
heat loss from the upper airways [4, 5, 9, 10, 13, 16, 18,
19].
As stated above, SBC as a treatment for hyperthermia in humans has been proposed but is controversial
[1, 3, 5]. Cabanac [5] criticized the use of SBC in humans for the following reasons: 1) SBC masks the error
signal which activates defense against hyperthermia; 2)
unlike other animals, humans do not pant and thus do
not possess a powerful heat sink near the brain; 3) humans do not have a carotid rete, the countercurrent
heat exchanger between the arterial and venous bloods
flowing in and out of the brain; 4) the high and constant arterial blood flow in the brain is su‰cient to
cool the brain under all conditions; and 5) the relatively low tympanic temperature recorded in hyperthermic humans is not indicative of SBC but of low
head skin temperature. Alternatively, many reports
support SBC in humans. The internal carotid artery
in humans is surrounded anatomically by a cavernous
sinus. The blood temperature of the cavernous sinus
decreases in response to chilled venous blood. Arterio-
411
lovenular anastomosis is also e‰cacious in SBC. Emissary and angular veins, the upper respiratory tract,
the tympanic cavity, and cerebrospinal fluid are also
thought to be components of the SBC system in humans [4, 19]. SBC e‰ciency is increased by evaporation of sweat from the head and by ventilation through
the nose. Moreover, craniofacial features such as thick
lips, broad nasal cavity, and large paranasal sinuses,
which provide greater evaporating surface, may be anatomical adaptations for e¤ective SBC in hyperthermia [13]. Some of these cooling systems are destroyed
by severe brain damage resulting in elevation of Tb.
Respiratory ataxia and elevation of venous temperature are the main targets of brain damage, which results in hyperthermia. In addition, tracheal intubation
blocks the physiological heat loss systems, thus maintaining the cycle of brain damage and brain hyperthermia. Destruction of the physiological and SBC system
worsens thermo-pooling in the brain and secondary
brain damage in patients with acute neuronal diseases.
We have demonstrated that SBC mechanisms are
important in the control of Tb in humans. We also employed face and head fanning with an electrical fan together with PSBC. Brinnel et al. [4] reported that face
fanning maintained tympanic temperature 0.57 C
lower than the esophageal temperature. Face and head
fanning might be a safe and e¤ective method of brain
cooling. This is the first report which demonstrates
SBC in humans by direct measurement of Tb rather
than by measurement of tympanic temperature.
Mechanisms of PSBC
We have developed and introduced PSBC, which is
an artificial physiological SBC system using circulating
chilled air. PSBC promotes heat loss from the nasal
cavity and cools through the venous circulation in the
nasal mucosa. Chilled venous blood flows into the cavernous sinus through the angular vein and selectively
cools the brain by means of a counter-current heat
exchange mechanism with the arterial blood. While
human nasal mucosa veins are not as developed as in
other mammals, the nasal mucosa blood flow increases
3-fold in humans with hyperthermia [22].
Bone in the skull base is only a few millimeters thick.
Many important anatomical structures (the pre-optic
tract, hypothalamus, hypophysis, and brainstem)
control thermoregulation in the basal brain. PSBC
prevents hyperthermia in these sites by directly cooling the nasal cavity. Furthermore, CSF chilled at the
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K. Dohi et al.: Positive selective brain cooling method: a novel, simple, and selective nasopharyngeal brain cooling method
basal cistern cools the whole brain through the CSF
circulation.
In the present study, we cooled the head and face of
patients by nasopharyngeal cooling. Thermoradiation
through the head and face is an important mechanism
of brain cooling in hyperthermic states. Head and face
cooling is also an important means of heat exchange
between venous and arterial blood. Blood chilled by
head and face cooling flows to deep veins in the cavernous sinus and nasal mucosa. Cerebral blood is e¤ectively cooled by heat exchange. Joint use of both methods may result in e¤ective and selective brain cooling.
In conclusion, PSBC is a novel, simple, and selective
blood cooling method. PSBC is a safe and e¤ective
method expected to be widely applicable in patients
who require external control of Tb.
Acknowledgments
This research was partially supported by the Ministry of Education, Science, Sports and Culture, Grant-in-Aid for Scientific Research (C), 16591815, 2004.
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Correspondence: Kenji Dohi, Department of Emergency and
Critical Care Medicine, Showa University School of Medicine, 1-58 Hatanodai, Shinagawa-ku, Tokyo, Japan. e-mail: kdop@med.
showa-u.ac.jp