The Trigeminocardiac Reflex – a Comparison with the Diving Reflex in Humans
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State of the art paper The trigeminocardiac reflex – a comparison with the diving reflex in humans Frederic Lemaitre1, Tumul Chowdhury2, Bernhard Schaller3 1Faculty of Sports Sciences, University of Rouen, Mont-Saint-Aignan, France Corresponding author: 2Department of Anesthesia and Perioperative Medicine, University of Manitoba, Dr Tumul Chowdhury MD, DM Winnipeg, Canada Department of Anesthesia 3Department of Neurosurgery, University Hospital Paris, Paris, France and Perioperative Medicine 2nd Floor, Herry Medovy House Submitted: 19 March 2013 671-William’s Ave Accepted: 30 June 2013 Health Sciences Center University of Manitoba Arch Med Sci 2015; 11, 2: 419–426 Winnipeg, Canada R3E 0Z2 DOI: 10.5114/aoms.2015.50974 Phone: (204) 298 5912 Copyright © 2015 Termedia & Banach Fax: (204) 787 4291 E-mail: [email protected] Abstract The trigeminocardiac reflex (TCR) has previously been described in the literature as a reflexive response of bradycardia, hypotension, and gas- tric hypermotility seen upon mechanical stimulation in the distribution of the trigeminal nerve. The diving reflex (DR) in humans is characterized by breath-holding, slowing of the heart rate, reduction of limb blood flow and a gradual rise in the mean arterial blood pressure. Although the two reflexes share many similarities, their relationship and especially their functional purpose in humans have yet to be fully elucidated. In the present review, we have tried to integrate and elaborate these two phenomena into a unified physiological concept. Assuming that the TCR and the DR are closely linked functionally and phylogenetically, we have also highlighted the significance of these reflexes in humans. Key words: reflexes, oxygen-conserving effects, breath-hold, brain, trigeminocardiac reflex, diving reflex. Introduction The trigeminal cardiac reflex (TCR) and diving reflex (DR) are neuro- genic reflexes that share many similarities in their clinical presentations and mechanisms of action; however, their relationship and especial- ly their functional purpose in humans have yet to be fully elucidated [1–10]. In the present review, we have tried to integrate and elaborate these two phenomena into a unified physiological concept. We have also highlighted the significance and current role of these reflexes in humans. Definitions The trigeminocardiac reflex The TCR is a well-established neurogenic reflex which manifests as bradycardia, hypotension, and gastric hypermotility seen upon mechan- ical stimulation in the distribution of the trigeminal nerve [1–3]. Initial reports were based on animal experiments; however, TCR in neurosurgi- cal patients was first elaborated by Schaller et al. in 1999 [3–6]. In their key work, Schaller et al. meticulously defined TCR, and their observa- tions are still used and commonly appreciated by researchers worldwide Frederic Lemaitre, Tumul Chowdhury, Bernhard Schaller [1–3, 5–7]. The incidence of the TCR in neurosur- elaborate the similarities as well as dissimilarities gical procedures involving or near the trigeminal between these two unique reflexes and therefore nerve vicinity was reported to be about 10–18% possibly integrate these into one common mecha- [7, 8]. These studies have usually taken a 20% nism. We assume that partially, if not substantial- decrease in hemodynamic changes as the cut-off ly, the TCR and the DR are closely linked function- limit to define TCR; therefore the true incidence ally as well as phylogenetically and represent old may be even higher. Moreover, the intensity of TCR reflexes that are physiological in humans in the is also a factor of the intensity of stimuli like the first few months of life. DR, which increases proportionally to decreasing water temperature [1–8]. At the molecular level, General similarities TCR is believed to be a physiological oxygen con- There are obvious strong links between the serving reflex which when incited initiates a pow- TCR and the DR that are generally accepted. Both erful sympathetic system response (within a few reflexes are based on the integrity of the trigem- seconds) and thus increases the cerebral blood inal-brain stem reflex arc [2, 3]. In both, brady- flow (CBF). This regional elevation of CBF without cardia is a common manifestation and is induced accompanying changes in the cerebral metabolic via reflex centers located in the medulla oblon- rate of oxygen or glucose rapidly provides oxygen gata [1, 28]. Efferent parasympathetic pathways to the brain in a more efficient manner. External mediate bradycardia and similarly efferent sym- stimuli and individual factors have a variable influ- pathetic pathways mediate peripheral vasocon- ence on inciting the TCR in humans [8]. striction. The diving reflex General differences The diving reflex in humans is characterized The TCR occurs due to either peripheral or cen- by breath-holding, slowing of the heart rate, a de- tral stimulation [3]. Stimulation of the trigeminal crease in cardiac output with sympathetic mediat- nerve anywhere along the face including the nose, ed peripheral vasoconstriction, an increase in mean orbit, eyeball and scalp (the area supplied by the arterial blood pressure (MABP) and splenic contrac- trigeminal nerve) up to the gasserian ganglion tion [9–16]. Blood is re-directed to more vital or- (entry into the intracranial compartment) is con- gans (heart, brain and lung) while at the peripheral sidered as a peripheral TCR. The DR can be consid- level poor irrigation of tissues manifests as lactate ered as a peripheral TCR. The gasserian ganglion accumulation. A simultaneous splenic contraction to the brainstem constitutes the rest of the tri- is also observed which indeed increases the stat- geminal nerve course, and stimulation along this ic apnea duration and helps in further resurgence part is considered as the central TCR. Peripheral of red blood cells in the blood circulation [17, 18]. TCR stimulation may present with bradycardia These phenomena also exist during repeated epi- with or without hypotension, whereas central TCR sodes of dynamic apnea [13]. Diving reflex is firstly stimulation is usually followed by severe bradycar- triggered by breath-holding and is augmented fur- dia/asystole and hypotension [3, 8]. What differs ther by immersion of the face into cold water [19, is that in the TCR there is a secondary decrease 20]. This response is also very prompt; therefore, in MABP, whereas in the DR the MABP gradually it can be considered as a reflex. The inhibition of increases. The difference might simply reflect the the respiratory centers and the absence of afferent fact that the stimulus in the DR is not ceased as input from pulmonary stretch receptors increase immediately as in the TCR. At present it is still not vasomotor and cardio-inhibitory activity [21–23]. clear whether this increase in MABP is specific for All these modifications allow economizing of the all peripheral TCRs or only for a subgroup. oxygen stores for the breath-hold diver (BHD) [18, 21, 24–27]. Similar to the TCR, the DR also acts as Bradycardia a protective oxygen-conserving reflex (OCR) and aims to keep the body alive during cold water im- It is a well-established fact that during breath- mersion. Thus it protects the vital organs (the heart hold diving, the heart rate (HR) becomes slower. and the brain) from extreme hypoxia. The DR in hu- The reduction in HR is brought about by the in- mans is modifiable by various factors including wa- volvement of both central inspiratory and phasic ter temperature, exercise, partial pressure of arte- pulmonary afferent mechanisms [29]. Similarly, rial oxygen (PaO2), carbon dioxide tension (PaCO2) it has been reported that tracheal intubation im- and psychological factors [22]. posed during surgical procedures may give some Though the two reflexes share a lot of similar- protection against activation of the TCR [30]. Ba- ities, their relationship and especially their func- bies under 6 months of age are excellent swim- tional purpose in humans have not yet been fully mers due to their DR: a baby’s air passage blocks elucidated. In the present article, we have tried to in contact with water, which explains the common 420 Arch Med Sci 2, April / 2015 The trigeminocardiac reflex – a comparison with the diving reflex in humans observation of babies “swimming” under water that progressively formed in the course of evolu- with open mouths. tion in order to increase cardiorespiratory survival. Both reflexes, the TCR and the DR, have a well- This hypothesis is further underlined by the fact known reciprocal influence on cardiac vagal and that the two main divisions of the autonomic sympathetic activity in adults resulting in bra- nervous system – the sympathetic and parasym- dycardia [31, 32]. Despite the above-mentioned pathetic system – support different types of ex- brainstem changes, the striking age-related de- change with the external environment. The main cline in occurrence of the TCR/DR in adults could function of the sympathetico-adrenal system is be the result of increased arterial stiffness [32]. to organize the function of the visceral organs In fact, in some instances the HR may rebound for an action to be performed by the organism to produce a delayed tachycardia being indicative of in response to the (unexpected) requirements of a temporal difference in the activation of the auto- the environment (“fight or flight”). On the other nomic outflows with the increase in cardiac sympa- hand, the role of the parasympathetic system is thetic activity outlasting