This article has Open Peer Review reports available.
A new predisposing factor for trigemino-cardiac reflex during subdural empyema drainage: a case report
© Spiriev et al; licensee BioMed Central Ltd. 2010
Received: 21 June 2010
Accepted: 30 November 2010
Published: 30 November 2010
The trigemino-cardiac reflex is defined as the sudden onset of parasympathetic dysrhythmia, sympathetic hypotension, apnea, or gastric hypermotility during stimulation of any of the sensory branches of the trigeminal nerve. Clinically, trigemino-cardiac reflex has been reported to occur during neurosurgical skull-base surgery. Apart from the few clinical reports, the physiological function of this brainstem reflex has not yet been fully explored. Little is known regarding any predisposing factors related to the intraoperative occurrence of this reflex.
We report the case of a 70-year-old Caucasian man who demonstrated a clearly expressed form of trigemino-cardiac reflex with severe bradycardia requiring intervention that was recorded during surgical removal of a large subdural empyema.
To the best of our knowledge, this is the first report of an intracranial infection leading to perioperative trigemino-cardiac reflex. We therefore add a new predisposing factor for trigemino-cardiac reflex to the existing literature. Possible mechanisms are discussed in the light of the relevant literature.
For more than a century, it has been well known that electrical, chemical, or mechanical stimulation of the trigeminal nerve leads to trigemino-respiratory reflexes followed by cardiac arrhythmias . In the early 20th century, this phenomenon gained increased clinical attention in the form of the oculocardiac reflex (OCR), which represents the cardiac response associated with stimulation of the ophthalmic division of the trigeminal nerve during ocular surgery . In 1999, Schaller  demonstrated for the first time that a similar reflex occurs with stimulation of the intracranial (central) portion of the trigeminal nerve during skull-base surgery and subsummarized all these trigemino-depressor responses under the term "trigemino-cardiac reflex (TCR)" . He also defined the TCR in a way that is now generally accepted. Later, his group also described the TCR for intraoperative stimulation of the peripheral portion .
Since then, there has been increasing discussion about the TCR itself, its provoking factors, and its treatment during intracranial or extracranial neurosurgical procedures. Several predisposing factors for intraoperative occurrence of TCR have been described [6–8], but until now no case of intracranial infection in combination with intraoperative TCR has been reported.
A 70-year-old Caucasian man was admitted for the second time to the Department of Neurosurgery at our hospital. His personal history included symptomatic epilepsy and chronic anemia after nephrectomy because of kidney carcinoma two years before admission to our clinic.
The patient underwent surgery several days after this second hospitalization. No pre-operative antibiotics were given. The patient fasted for eight hours prior to surgery. Routine monitoring during surgery included electrocardiography (ECG), end-tidal (ET) concentration of CO2 and sevoflurane, and pulse oximetry. All hemodynamic parameters were monitored continuously and recorded throughout the neurosurgical procedure. Anesthesia was induced with midazolam (1 mg total dosage) and propofol (2 mg/kg) followed by suxamethonium chloride (1.1 mg/kg), atracurium (0.6 mg/kg), and fentanyl (100 μg total dosage). After the trachea was intubated, the lungs were mechanically ventilated (S/5 Aespire Config; Datex-Ohmeda Ins., Madison, WI, USA) with a mixture of air and O2. Anesthesia was maintained with sevoflurane (1%). An additional 50 mg of propofol and 1 mg of midazolam were applied during the intervention when necessary.
Surgical technique and postoperative management
The presented case report is unique and adds a new and important risk factor for the intraoperative occurrence of TCR to the existing literature. It seems that infected intracranial tissue may be a new predisposing factor in combination with surgical manipulation on the meninges, a routine surgical operative technique that has never been described before to be associated with TCR occurrence.
It has already been shown that mechanical stimulation of the cerebral falx results in hyperactivity of trigeminal ganglion, thereby triggering the TCR . The neural supply of the cranial dura mater involves mainly the three divisions of the trigeminal nerve, the first three cervical spinal nerves, and the cervical sympathetic trunk. A case of immediate, reproducible, and reflexive response of asystole upon stimulation of the cerebral falx during operative resection of a parafalcine meningioma was previously reported , being most likely related to bilateral trigeminal stimulation of the falx. According to the studies of Penfield and McNaughton , the nervus tentorii, a recurrent branch of the ophthalmic branch of the trigeminal nerve bilaterally innervates the tentorium cerebelli, the dura of the parieto-occipital region, the posterior third of the falx, and the adjacent sinuses. In our present case, however, the subdural empyema was located in the middle cranial fossa that is predominantly innervated by the V2 and V3 branches of trigeminal nerve . However, it has been previously shown by us and others that surgical procedures at the anterior, middle, and posterior skull base (any branch of the central part of trigeminal nerve) may elicit the TCR.
In this special case, one may suggest that the patient had simply a (physiological) Cushing reflex with consecutive elevated MABP before operation that only normalized after elevation of the mass lesion. But the Cushing reflex is not a possible explanation of the MABP and HF drop as seen in our case. In our case, the intraoperative phenomenon was reproducible, which would be not the case if there were a Cushing reflex. Our case shows, therefore, a clear cause-and-effect relationship necessary for the TCR and as described earlier in detail .
Different retrospective studies have shown an incidence of TCR ranging from 8%  to 18%  using all the same inclusion criteria as defined earlier by us . However, it seems that TCR is often unrecognized intraoperatively, so the identification of possible provoking factors is important but often elusive. There are several reports for the provoking factor for the peripheral initiation and central initiation of the TCR. To date, several risk factors for the intraoperative occurrence of TCR have been identified, such as light general anesthesia, childhood, and the nature of the provoking stimulus (strength and duration of stimulus) [3, 8]. In addition, there are several known provoking drugs such as potent narcotic agents (sufentanil and alfentanil), β-blockers, and calcium channel blockers [3, 8]. Until now, no report for intracranial infections as a provoking factor for intraoperative TCR occurrence has been identified.
Intracranial infections, as in the current case of subdural empyema, could lead to a pathological process called sensitization of trigeminal afferents in the dura mater . It was demonstrated that chemical stimulation of dural receptive fields with inflammatory mediators such as prostaglandin E2, bradykinin, or histamine directly excite the neurons and enhance their mechanical sensitivity [1, 5], such that they can be easily activated by mechanical stimuli that initially had evoked little or no response [14, 15]. It seems that meningeal sensory innervation is not known to subserve multiple sensory modalities [10, 14]. Meningeal afferents are thought to become activated only under potentially harmful or pathological conditions . However, although the dural afferent population does not appear to mediate distinct sensory modalities, it shows a pattern of variation in mechanosensitivity as a function of conduction velocities [10, 16]. Mechanical response properties of dura are attributed to A and C primary afferent neurons. Such exaggerated mechanical sensitivity and manipulation of the dura mater could play a role in the initiation of TCR in our case.
To the best of our knowledge, this is the first report of an intracranial infection with the intra-operative occurrence of TCR during a routine neurosurgical maneuver. Infected (intracranial) tissue may be a new and important predisposing factor for the occurrence of TCR, a phenomenon that is different from the falcine TCR caused by bilateral stimulation of tentorial nerve that was described earlier. Further laboratory and clinical investigations are needed to clarify this new information about TCR.
Written informed consent was obtained form the patient for publication of this case report and accompanying images. A copy of the written consent is available for review by the Editor-in-chief of this journal.
- Angell-James JE, Daly MB: Nasal reflexes. Proc R Soc Med. 1969, 62: 1287-1293.PubMedPubMed CentralGoogle Scholar
- Ashner B: Über einen bisher noch nicht beschriebenen Reflex, vom Auge auf Kreislauf und Atmung. Verschwinden des Radialispulses bei Druck auf das Auge. Wien Klin Wochenschr. 1908, 21: 1529-1530.Google Scholar
- Schaller B, Probst R, Strebel S, Gratzl O: Trigeminocardiac reflex during surgery in the cerebellopontine angle. J Neurosurg. 1999, 90: 215-220. 10.3171/jns.1999.90.2.0215.View ArticlePubMedGoogle Scholar
- Schaller B: Trigeminocardiac reflex: a clinical phenomenon or a new physiological entity?. J Neurol. 2004, 251: 658-665. 10.1007/s00415-004-0458-4.View ArticlePubMedGoogle Scholar
- Schaller BJ, Filis A, Buchfelder M: Trigemino-cardiac reflex in humans initiated by peripheral stimulation during neurosurgical skull-base operations: its first description. Acta Neurochir (Wien). 2008, 150: 715-717. 10.1007/s00701-008-1602-1.View ArticleGoogle Scholar
- Blanc VF, Hardy JF, Milot J, Jacob JL: The oculocardiac reflex: a graphic and statistical analysis in infants and children. Can Anaesthet Soc J. 1983, 30: 360-369. 10.1007/BF03007858.View ArticleGoogle Scholar
- Schaller B, Cornelius JF, Prabhakar H, Koerbel A, Gnanalingham K, Sandu N, Ottaviani G, Filis A, Buchfelder M, Trigemino-Cardiac Reflex Examination Group (TCREG): The trigemino-cardiac reflex: An update of the current knowledge. J Neurosurg Anesthesiol. 2009, 21: 187-195. 10.1097/ANA.0b013e3181a2bf22.View ArticlePubMedGoogle Scholar
- Bauer DF, Youkilis A, Schenck C, Turner CR, Thompson BG: The falcine trigeminocardiac reflex: case report and review of the literature. Surg Neurol. 2005, 63: 143-148. 10.1016/j.surneu.2004.03.022.View ArticlePubMedGoogle Scholar
- Penfield W, McNaughton F: Dural headache and innervation of the dura mater. Arch Neurol Psychiatr. 1940, 44: 43-75.View ArticleGoogle Scholar
- Strassman AM, Raymond SA, Burstein R: Sensitization of meningeal sensory neurons and the origin of headaches. Nature. 1996, 384: 560-564. 10.1038/384560a0.View ArticlePubMedGoogle Scholar
- Jeker A, Martins C, Rhoton AL: Meningeal Anatomy. Meningiomas. Edited by: Pamir MN, Black MP, Fahlbusch R. 2010, Amsterdam: ElsevierGoogle Scholar
- Koerbel A, Gharabaghi A, Samii A, Gerganov V, von Gösseln H, Tatagiba M, Samii M: Trigeminocardiac reflex during skull base surgery: mechanism and management. Acta Neurochir (Wien). 2005, 147: 727-733. 10.1007/s00701-005-0535-1.View ArticleGoogle Scholar
- Schaller B: Trigemino-cardiac reflex during microvascular trigeminal decompression in cases of trigeminal neuralgia. J Neurosurg Anesthesiol. 2005, 17: 45-48.PubMedGoogle Scholar
- Strassman AM, Levy D: Response properties of dural nociceptors in relation to headache. J Neurophysiol. 2006, 95: 1298-1306. 10.1152/jn.01293.2005.View ArticlePubMedGoogle Scholar
- Harriott AM, Gold MS: Electrophysiological properties of dural afferents in the absence and presence of inflammatory mediators. J Neurophysiol. 2009, 101: 3126-3134. 10.1152/jn.91339.2008.View ArticlePubMedPubMed CentralGoogle Scholar
- Strassman AM, Levy D: Mechanical response properties of A and C primary afferent neurons innervating the rat intracranial dura. J Neurophysiol. 2002, 88: 3021-3031. 10.1152/jn.00029.2002.View ArticlePubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (<url>http://creativecommons.org/licenses/by/2.0</url>), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.