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 412 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. References 1. 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Eur J Appl Physiol Occup Physiol 70: 207–212 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
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