Trigeminocardiac reflex: A MaxFax literature reviewBehnam Bohluli, DMD, MS,a Abbas Kazemi Ashtiani, MD, MS,b Anahita Khayampoor, DDS,c

and Pooyan Sadr-Eshkevari, DDS,d Tehran, IranAZAD UNIVERSITY OF TEHRAN, IRAN UNIVERSITY OF MEDICAL SCIENCES, BEHESHTI UNIVERSITY OFMEDICAL SCIENCES, AND PRIVATE PRACTICE

Trigeminocardiac reflex (TCR) is a shocking event in the course of operation involving the maxillofacial area.The authors have tried to present an overview on the history, clinical implications, literature review, anatomic andbiologic basis, predisposing and triggering factors, and management of the event. Being familiar with the presentations,preventive measures, and management procedures are seemingly the most important aspects of the TCR to oral and

maxillofacial surgeons and anesthesiologists. (Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2009;108:184-188)

Trigeminocardiac reflex, previously known as oculo-cardiac reflex, may serve as a shocking event in thecourse of operation involving the head and neck regionboth for surgeons and anesthesiologists.1 A better un-derstanding of this phenomenon would then be of par-amount importance to the profession. This idea was thebasis for the development of the current article.

THE TRIGEMINOCARDIAC STORYJoseph Breuer described the self-regulation of

breathing through the vagus nerves in 1868, and FlorianKratschmer described the influences of reflexes of thenasal mucosa on breathing and circulatory in 1870.1

These are considered as the first steps in the descriptionof trigeminal-mediated bradycardia or asystole, which iswell known especially for anesthetists and surgeons deal-ing with the craniomaxillofacial structures.2,3 Based onthe studies of Kratschmer on cats and rabbits, a suddendevelopment of cardiac dysrhythmia up to asystole,arterial hypotension, apnea, and gastric hypermotilitywas observed on manipulation of the nasal mucosa.3 In1969, it was confirmed that the stimulation of nasalmucosa causes bradypnea, bradycardia, and blood pres-sure turbulence in dogs under anesthesia. These re-flexes were fully abolished while local anesthetics wereapplied to the divisions of the trigeminal nerves.4 Thetrigeminocardiac reflex (TCR) was first described as

aAssistant Professor of Oral and Maxillofacial Surgery, School ofDental Medicine, Azad University of Tehran, Tehran, Iran.bAssociate Professor of Plastic and Reconstructive Surgery, IranUniversity of Medical Sciences (IUMS), Tehran, Iran.cResident of Oral and Maxillofacial Surgery, Taleghani Hospital,Beheshti University of Medical Sciences (BUMS), Tehran, Iran.dPrivate Practice Dentistry, Tehran, Iran.Received for publication Feb 1, 2009; returned for revision Mar 10,2009; accepted for publication Mar 20, 2009.1079-2104/$ - see front matter© 2009 Published by Mosby, Inc.

doi:10.1016/j.tripleo.2009.03.050

184

“oculocardiac reflex” (OCR) in 1908.2,5 They attributedthis response to a pressure-induced neural reflex thatcauses cardiac depression through the stimulation of thevagal nerve.5 Today oculocardiac response is defined asa sudden decrease in heart rate (HR) of more than 20%of the baseline value, dysrhythmias, or sinoatrial arrest.The oculorespiratory reflex (ORR) is the abrupt reduc-tion of tidal volume (VT) and respiratory rate (RR).6 In1988, the term “trigeminocardiac reflex” was describedby 2 anesthetists, Shelly and Church.7

Since the development of modern reconstructiveplastic surgery techniques in 1967, new intraoperativeanesthetic complications have been described in thisfield.4 This phenomenon may be generated as a resultof procedures or conditions that increase intraocularpressure,5 strabismus surgery,2 nasal packing after rhi-noplasty,8 the reduction of zygoma and zygomatic archfractures,5 elevation of bone flap or osteotomies, reflec-tion of a palatal flap for removal of a mesiodens,9

during Le Fort I downfractures, sagittal split ramusretraction,5 midface disimpaction,10 cutting maxillarytuberosity,9 and temporomandibular joint (TMJ) arthro-scopy.5 Because the reflex does not appear to be limitedto the ophthalmic branch and in order to be moreinclusive and anatomically descriptive of the response,Shelly and Church7 suggested changing the name totrigeminocardiac (TCR) or trigeminovagal reflex(TVR).

PROBLEM STATEMENTDysrhythmias as a result of surgical manipulation of

the eye and relevant orbital structures have been welldocumented in the ophthalmology literature5; however,the occurrence of this reflex during other maxillofacialsurgeries is not as recognized and no review article hasdiscussed this phenomenon based on oral and maxillo-facial surgery literature. To the best of our knowledge,

about 23 cases of sudden bradycardia and/or asystole

OOOOEVolume 108, Number 2 Bohluli et al. 185

thought to be attributed to trigeminal-mediated reflexduring craniomaxillofacial surgery have been discussedin the craniomaxillofacial literature since 1978.

MAXILLOFACIAL LITERATURE REVIEWIn 1987, Bainton and Lizi11 reported a case of car-

diac asystole complicating the operation of a zygomaticarch fracture. Another case of bradycardia during theelevation of a zygomatic arch fracture was reported inthe same year by Loewinger et al.12 Also Shearer andWensione13 reported episodes of bradycardia duringelevations of zygomatic fractures in 1987. Robideaux10

documented a case of a sudden decrease in heart rate(from 90 to 54 beats per minute) consonant with sur-gical disimpaction of a fractured maxilla in a 22-year-old healthy male. These case reports aimed to alert oraland maxillofacial surgeons and also anesthesiologiststo the possible hazards during surgical elevation of afractured zygomatic arch. They suggested that trigemi-nocardiac reflexes (TCR) can be elicited by stimulatingafferent paths other than the ciliary nerves (branches ofV1of the trigeminal nerve), which are classically asso-ciated with OCR.11,12 Reaume and MacNicol14 areamong the first who noticed the occurrence of thisphenomenon in maxillofacial osteotomies. In 1988 theymentioned this reflex as a complication encounteredduring LeFort I osteotomy in a patient with mandibu-lofacial dysostosis. In 1989, Matarasso,15 a plastic sur-geon, reported a case of oculocardiac reflex in blepha-roplasty surgery. He describes this phenomenon as anintraoperative bradycardia exceeding 10% of the pre-operative heart rate or any dysrhythmia during ocularmanipulation. He introduced this reflex as a trigeminal-vagal-mediated reflex arc. Based on his observations,oculocardiac reflex occurs in 25% of the patients un-dergoing blepharoplasty. In the same year, Stott16 dis-cussed reflex bradycardia in facial surgeries through hiscase report. He mentioned that using the term “oculo-cardiac reflex” is inappropriate, because traction on, orstretching of, any structure innervated by the trigeminalnerve, most of which are extraocular, is associated withthe occurrence of this reflex and slowing of the pulse.He emphasized that this phenomenon can also causeproblems in surgery of the face and cranium. Ragno etal.17 described several episodes of extreme ventricularasystole in a single patient occurred during down-frac-ture of maxilla in Le Fort I osteotomy. In 1990, Baintonet al.18 reported a case of sinus arrest (cessation ofactivity of the sinuatrial node) complicating a bitempo-ral approach to the treatment of pan-facial fractures. Inthe same year, Precious and Skulsky19 admitted thatcardiac asystole, bradycardia, and other dysrhythmiasassociated with the surgery of the craniofacial and

maxillofacial structures have been discussed frequently

in ophthalmology literature but less attention has beenpaid to this problem in maxillofacial surgery. Theyreported a series of 8 patients, 6 men and 2 women,with the occurrence of either asystole or bradycardiaduring maxillofacial surgeries. This number of caseswas equal to 1.6% of the total number of patientstreated during a 16-month period in their center (500cases). Six of 8 patients demonstrated either asystole orbradycardia as a result of soft tissue stretching withadvancement of maxilla after bony mobilization. Twoother patients experienced either asystole or bradycar-dia caused by the manipulation of the temporalis mus-cle during surgery for the correction of total bonyankylosis of the TMJ. Lang et al.2 in 1991 presented 3additional cases confirming that reflex bradycardic re-sponses can occur after stimulation of sensory branchesof the maxillary (V2) and mandibular (V3) divisions ofthe trigeminal nerve. Combinations of bradycardia andventricular asystole were encountered in response tosurgical stimuli in the distribution of the maxillary andmandibular divisions of the trigeminal nerve in 3 oth-erwise healthy individuals undergoing maxillary ormandibular osteotomies. They assumed that conductionabnormalities and a ventricular septal defect in 1 case,preoperative nadolol in the other 2 cases and the use ofintraoperative narcotics in all 3 patients may have pre-disposed them to the development of reflex bradycardicepisodes. In 1990, Barnard and Bainton20 reported 2cases and further discussed the association of bradycar-dia and the trigeminal nerve. In 1992, Matarasso21

commented on the reports of Precious and Skulsky anddiscussed cardiac dysrhythmias complicating maxillo-facial surgery. Even a case of asystole during thyroidresection was reported by Delap et al.22 in 1995. Rob-erts et al.5 in 1999 reported a case of trigeminocardiacreflex during TMJ arthroscopy. This case of sudden-onset bradycardia involved a 29-year-old white woman.TCR occurred during the lysis of adhesions and dis-traction of the mandibular condyle during left TMJarthroscopy. They believed that the auriculotemporalnerve adjacent to the mandibular condyle was the af-ferent arc of the reflex. As they reported, stimulationoccurred upon manipulating the condyle and instru-menting the superior joint space with a blunt trocar.The first case of oculocardiac reflex elicitation duringendoscopic forehead lift surgery was reported by Sladeand Cohen in 1999.23 Manipulation of the supraorbitalnerve was described as the cause of this elicitation.Kosaka et al.24 reported a unique case of oculocardiacreflex induced by zygomatic fracture. The initial diag-nosis of his dysrhythmia was a total A-V block due toinjury. Dysrhythmia did not improve spontaneously,and the patient underwent cardiac pacing. After repair

of the fracture, his arrhythmia completely disappeared

OOOOE186 Bohluli et al. August 2009

and the pacemaker was removed on the first postoper-ative day. This was clearly indicative of associatedtrigeminal branch injury and trigeminocardiac reflex.Cha et al25 in 2002 experienced two unexpected epi-sodes of asystole after transection of the sensory rootsof the trigeminal nerves. The trigeminocardiac reflexwas reported to have occurred during the rhizotomies ofboth sides of the dorsal sensory roots of the trigeminalnerves for palliation of intractable trigeminal pain in a2-year-old male patient with hemangioma near the sellaturcica. This was considered a confirmation proof to thecentral role of the trigeminal nerve as the afferentpathway of the reflex arc. In 2007, Webb and Unkel9

reported a unique example of the trigeminovagal reflexwhere the afferent impulses were caused by stimulationof the nasopalatine nerve. In this case, the nasopalatinenerve was infiltrated preoperatively to achieve localanesthesia, which should have blocked the responsetheoretically. The authors however believed that localanesthetic used to prevent the reflex was not sufficientconsidering the traction on the nerve. They also em-phasized that caution should be exerted while raising aflap to remove an impacted canine in children.

ANATOMIC DESCRIPTIONThe afferent limb of the oculocardiac reflex arc is via

the ophthalmic division of the trigeminal nerve. It be-gins with afferent fibers of the long and short ciliarynerves that travel with the ophthalmic division of thetrigeminal nerve, continues to the gasserian ganglion,and then joins the main sensory nucleus of the trigem-inal nerve in the floor of the fourth ventricle. Shortinternuncial fibers in the reticular formation connectthem with the efferent pathway from the motor nucleusof the vagus nerve to the depressor nerve. Depressorfibers of the vagus nerve end in the myocardium. How-ever, as previously mentioned, the ophthalmic divisionis not the only afferent pathway.2-4,9 Because of inner-vation patterns, it was argued that the ophthalmic nervecould be the afferent limb when maxillary manipula-tions are performed.2 However, reports of the occur-rence of the reflex during mandibular osteotomies orTMJ surgery confirms that the maxillary and mandib-ular divisions of the trigeminal nerve serve as alterna-tive reflex pathways for trigeminocardiac reflex.

BIOLOGIC RELEVANCEThere are endogenous physiological protective mecha-

nisms detected in brain against ischemia. The TCR isseemingly an example of these protective physiologicentities.3 It may be part of a group of related responsesgenerally defined as “oxygen-conserving reflexes.”Within seconds after the initiation of such a reflex,

there is a powerful and differentiated activation of

sympathetic nerves and consequently a primary cere-brovascular vasodilatation. The hibernation and isch-emic tolerance appear to involve at least partially sim-ilar physiological mechanisms3,26; however, theseseemingly physiologic functions may become exagger-ated and put the patients at risk. During the initialperiod of vagal stimulation, the resultant cardiac de-pression reaches a peak level, and it is at this criticaltime that sinus arrest, asystole, or ventricular fibrillationcan occur.5 Also nasogastric reflex has been recentlydescribed in a case report by Shoja et al.27 Opposed tothe opinion of Schaller,28 they believe that nasogastricreflex is “not exactly the trigemino-cardiac reflex.”29

Diving response, or nasopulmonary and sinopulmonaryreflexes are other brainstem reflexes detected in themiddle decades of last century.30,31 The chains of brainstem reflexes most probably do not end in these re-flexes, which are based on the connections betweentrigeminal and vagus nerves.3

PREDISPOSING AND TRIGGERING FACTORSIt is well known that hypercarbia, hypoxemia, and

insufficient anesthesia are predisposing factors in theoccurrence of OCR. Also, the nature of the provokingstimulus, meaning its strength and duration, contributeto the significance of the HR and blood pressure de-crease.2 On the other hand, OCR occurs more pro-nouncedly in children.6,32 This is attributed to thehigher resting vagal tone.3 The relation of these factorsand the incidence of TCR have not been addressedthrough the craniomaxillofacial surgery literature.Pharmacological agents such as potent narcotics likesufentanil and alfentanil, beta-blockers, and calciumchannel blockers may predispose to OCR. It has beenclaimed that OCR normally fatigues with repetitivestimuli.2,6 Despite little evidence available, these factsmost probably apply to the TCR as well, but needconfirmation through further studies.

CLINICAL IMPLEMENTATION ANDMANAGEMENT

As Schaller and Buchfelder26 have mentioned, “Theclinical importance of the TCR lies in the fact that itsclinical features range from sudden onset of sinus bra-dycardia, bradycardia terminating asystole, asystolewith no preceding bradycardia, arterial hypotension,apnea, and gastric hypermobility.” Recognition of bra-dycardia is the first step in treatment. Avoidance ofpredisposing or triggering factors, halting the surgicalstimulus, IV administration of atropine or glycopyrro-late, and complementary anesthesia of the afferentnerves are mentioned as management protocol for thisreflex. Local anesthetic infiltration or afferent nerve

blockade applies to the persistent cases that do not

OOOOEVolume 108, Number 2 Bohluli et al. 187

respond to primary management.2,5,9 Fortunately, mostcases are associated with only a 10% to 50% heart ratereduction and sinus rhythm usually returns to baselineupon stimuli cessation.5 Most cases of TCR will there-fore resolve spontaneously without any other therapeu-tic measures. If resolution does not happen during areasonable amount of time after cessation of the evolv-ing surgical maneuver (refractory bradycardia, asystole,or the development of bradycardia with hypotension),atropine or glycopyrrolate should be administered in-travenously.2,5 Atropine would be given before epi-nephrine only if bradycardia was thought to be attrib-utable to vagal stimulation and not some other causesuch as hypoxia.9 No case of transthoracic cardiacpacing to manage reflex bradycardia attributed to TCRhas thus far been reported.5 Cardiac massage should bereserved for the cases in which routine treatment mea-sures fail to reestablish the expected cardiac activity.Only 2 cases of asystole have been reported to bemanaged by cardiac massage throughout the litera-ture.33

PREVENTIVE MEASURESIt has been shown that OCR, airway irritability, and

ventilatory interventions occur with lower incidence inspontaneously breathing children undergoing strabis-mus correction with 1.3 MAC sevoflurane in N2O thanwith halothane. Baseline heart rate and respiratory rateare higher with sevoflurane. Also, considerably fewerdysrhythmias are observed in children receivingsevoflurane than in those receiving halothane. It is thenconcluded that a comparatively greater depression ofvagal activity by sevoflurane may lead to a less pro-nounced bradycardia on stimulation of the OCR. Thismay be attributed to the lack of effect of sevoflurane onmyocardial conduction compared with halothane.6 Onthe other hand, some others claim that the initial base-line heart rate has no influence on the incidence of theoculocardiac reflex and tachycardia is therefore notprotective.2 Again, further studies are needed to gener-alize these discussions to TCR. Most importantly,preoperative infiltration of the possible afferent path-way to achieve local anesthesia should block theresponse and is highly recommended in craniomax-illofacial surgeries involving manipulation of thetrigeminal nerve branches.9

CONCLUSIONSBeing familiar with the presentations, preventive

measures, and management procedures are seeminglythe most important aspects of the TCR to oral andmaxillofacial surgeons and anesthesiologists. Furtherstudies, preferably with a multicenter design, are nec-

essary to confirm the nature, description, predisposing

and triggering factors, and other aspects of this seem-ingly physiologic phenomenon.

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2001;127:89-91.2. Lang S, Lanigan DT, van der Wal M. Trigeminocardiac reflexes:

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3. Schaller B. Trigeminocardiac reflex. A clinical phenomenon or anew physiological entity? J Neurol 2004;25:658-65.

4. Blanc VF. Trigeminocardiac reflexes. Can J Anaesth 1991;38:696-9.

5. Roberts RS, Best JA, Shapiro RD. Trigeminocardiac reflex dur-ing temporomandibular joint arthroscopy: report of a case. J OralMaxillofac Surg 1999;57:854-6.

6. Allison CE, De Lange JJ, Koole FD, Zuurmond WW, Ros HH,van Schagen NT. A comparison of the incidence of the oculo-cardiac and oculorespiratory reflexes during sevoflurane or halo-thane anesthesia for strabismus surgery in children. AnesthAnalg 2000;90:306-10.

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8. Nirmala J, Dilip KK, Padmaja D, Gopinath R. “Kratschmer”reflex during rhinoplasty. Anesth Analg 2006;103:1337-8.

9. Webb MD, Unkel JH. Anesthetic management of the trigemino-cardiac reflex during mesiodens removal—a case report. AnesthProg 2007;54:7-8.

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