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Incidence of trigeminocardiac reflex in maxillofacial surgery: A retrospective

study

Article in Journal of Health Specialties · January 2016

DOI: 10.4103/1658-600X.179818

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Original Article

Incidence of trigeminocardiac reflex in

maxillofacial surgery: A retrospective study
Hanan Ghazi Shanab1, Hamed Hassan Albargi2
Department of Oral and Maxillofacial Surgery, King Khalid National Guard Hospital, 2Department of Oral and Maxillofacial Surgery,
1

Dr. Suliman Fakeeh Hospital, Jeddah, Saudi Arabia

ABSTRACT
Introduction: The trigeminocardiac reflex (TCR) is a brainstem reflex that has attracted the attention of many clinical researchers,
including neurosurgeons, anaesthetists, ophthalmologists, and general, plastic, and craniomaxillofacial surgeons. However,
more maxillofacial surgery studies related to TCR need to be conducted in order to better understand this phenomenon.
Aim: The aim of this study was to evaluate the occurrence of TCR during maxillofacial procedures performed between
2008 and 2012 including trauma, orthognathic, and reconstructive surgeries. Additionally, with a literature review provide
information regarding its incidence, predisposing factors and management.
Subjects and Methods: A five-year retrospective study was conducted to evaluate the charts of 56 healthy patients (classified as
American Society of Anaesthesiologists class I) admitted in the Department of Oral and Maxillofacial Surgery from 2008 through
2012 at King Abdulaziz Medical City (formerly known as King Khalid National Guard Hospital), Jeddah. Information regarding the
different types of procedures and occurrence of TCR in each case was collected. SPSS (V 11.5) was used to analyse the data
collected.
Results: The overall incidence of TCR was 20% of all the cases, with the highest percentage occurring during mid face
trauma repair followed by upper face reconstructive surgeries.
Conclusions: TCR can be fatal and must be taken in consideration. All craniomaxillofacial surgeons are advised to follow
guidelines for the management of TCR illustrated by Arasho et al. in 2009.

Keywords: Oculocardiac reflex, orthognathic, reconstruction, trauma, trigeminocardiac reflex

INTRODUCTION SUBJECTS AND METHODS

The purpose of the study was to evaluate the
incidence of trigeminocardiac reflex (TCR) during
maxillofacial procedures over a time period in
specific types of procedures in order to increase TCR
awareness in terms of its diagnosis and management
in addition to reviewing literature for information
regarding its incidence, predisposing factors and
management.
Address for correspondence:
Dr. Hanan Ghazi Shanab, King Abdulaziz Medical City,
National Guard Hospital, Jeddah, Saudi Arabia.
E-mail: dr_aureus@hotmail.com
56 patients have been operated by oral and maxillofacial
surgeons in the National Guard Hospital located in
Jeddah from 2008 through November 2012. Data
were retrieved from the patients’ medical records and
operative notes. Anaesthesia charts were also reviewed.
All of the patients were healthy (American Society of
Anaesthesiologists class I).
The inclusion criteria were as follows: All cases were
admitted as trauma, orthognathic, and reconstruction of
facial hard tissues. Whereas, the rest of the procedures,
other than the three aforementioned mentioned, which

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DOI: How to cite this article: Shanab HG, Albargi HH. Incidence of trigeminocardiac
10.4103/1658-600X.179818 reflex in maxillofacial surgery: A retrospective study. J Health Spec
2016;4:151-6.

© 2016 Journal of Health Specialties | Published by Wolters Kluwer ‑ Medknow 151

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Shanab and Albargi: TCR
involved soft tissue were excluded. Each category was
subdivided according to the different parts of the face;
based on the anatomical difference as well as different
nerve supply into procedures involving the upper,
middle and lower parts of the face and then divided into
TCR positive (+ve) and TCR negative (−ve).
Data were collected, recorded and statistically analysed
using SPSS Inc., 233 South Wacker Drive, 11th Floor,
Chicago, IL 60606-6412, USA (V 11.5). The frequency,
incidence and percentage were calculated for each
procedure type.
RESULT
In this study, 77% of the patients were males. The most
conducted procedures were middle facial trauma repair
(32%), upper facial reconstruction (30.4%), lower facial
trauma repair (17.9%), maxillary orthognathic surgery
(12.5%), upper face reconstruction (3.6%) and lower
face reconstruction (3.6%), respectively.
Among 56 cases, 20% had TCR.
The percentages of TCR incidence in each procedure
were evaluated. The procedure that had the highest
incidence of TCR was the upper face reconstruction
(36.4%), followed by middle face trauma repair (27.3%),
lower face trauma repair (18.2%) and equal percentages
of maxillary and mandibular orthognathic surgeries
(9.1%) [Graph 1].
All the cases of TCR were treated conservatively by stop
manipulation without the need for any medications.
DISCUSSION
Literature review
In 1908, TCR was first described as oculocardiac (OC)
reflex by Bernard Asher and Giuseppe Dagnini. [1]
Graph 1: Illustration of the incidence of trigeminocardiac reflex in each
procedure. Notice that trigeminocardiac reflex was higher in upper
face reconstruction (36.4%) while it was equal in orthognathic surgery
for both maxilla and mandible (9.1%) as the lowest incidence over all
152
This reflex occurred only as a result of mechanical
stimulation of ocular and periocular structures that
are innervated by the ophthalmic nerve. [2] It was
given a name of blepharocardiac reflex in Marcus
Gunn syndrome by Kwik in 1980.[3] In 1868, Joseph
Breuer, described the relationship between the vagus
nerve and breathing control.[4] In 1870, TCR was first
described as trigeminocardiac and trigeminorespiratory
reflexes by Kratschmer, who reported the incidence of
bradycardia, bradypnea, apnea and variable changes
in blood pressure of a cat and rabbit with stimulation
of the nasal mucous membrane. Throughout the
literature, it has been given different names like
“trigeminal depressor” in 1977 by Kumada et al.[5] and
trigeminovagal reflex by two anaesthetists; Shelly and
Church in 1988.[4] However, similar incidences were
reported in craniofacial reconstruction surgeries since
1978. In 1987, Bainton and Lizi, and Loewinger et al.,
suggested that TCR could happen by stimulation of
any afferent branch of the trigeminal nerve including
maxillary and mandibular divisions other than the
ophthalmic nerve that was previously known to
induce that reflex.[6] Moreover, peripheral branches, for
example, the anterior ethmoidal nerve that innervates
the face and nasal passages which is responsible for the
diving reflex, was found to be the triggering factor for
TCR during transsphenoidal surgery.[5,7] The concept
now generalised to be TCR being OC reflex is one of
its variant.
Definition
TCR is defined as the sudden onset of sinus bradycardia
(heart rate [HR] <60 beats/min and mean arterial pressure
>20% lower than the baseline).[8] Because this definition
cannot be applicable to all cases including those with a
<20% value and to avoid the underestimation caused by
this definition, Abdulazim et al., in their neurosurgery
updates regarding TCR definition came with a more
inclusive and simplified version as “any sudden onset
of relative bradycardia upon the stimulation of any of
the 3 branches of the trigeminal nerve”.[5]
Manifestation
It can be manifested as bradycardia terminating asystole,
asystole with no preceding bradycardia, arterial
hypotension, apnea and gastric hypermobility during
stimulation of any of the sensory branches of trigeminal
nerve, either whether it is central or peripheral.[9]
Diving reflex, an example of the peripheral reflex,
induces a nasopharyngeal reflex; vagally-mediated
bradycardia with associated electrocardiogram (ECG)
abnormality showing clinical effect of the vagus on the
heart in the form of short QT interval, atrioventricular
nodal rhythm, ventricular ectopic beats and wandering
pacemaker.[10,11]
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Shanab and Albargi: TCR
The role of trigeminocardiac reflex
TCR is considered to play a neuroprotective role against
brain ischaemia as one of a group defined by Wolf as
an “oxygen-conserving reflex”. Whenever there is a
drop in cerebral blood flow or oxygen, immediately
there will be an endogenous physiologic mechanism
involving cerebral vasodilation induced by those oxygen
sensitive brainstem neurons in rostral ventrolateral
medulla (RVLM) to rapidly perfuse the brain with
adequate blood supply. All of that returns to normal
when stimuli disappears. This reflex protects the brain
against ischaemic damage (ischaemic tolerance) in case
of very low levels of cerebral blood flow as in diving
and hibernation.[4,12] On the other hand, vagal escape
(fatigue) is a state of unresponsiveness to repeated and
excessive vagal stimulation. It is considered to be a
physiologically protective mechanism as it reduces the
intensity of the ophthalmocardiac reflex (OCR), and is
responsible for recovering from the reflex.[2]
Types of trigeminocardiac reflex
TCR is an unknown reflex with centrally located
(brainstem) reflex arc because of the findings of
persistent cardiac responses to TCR in decerebrated
animals. In 1999, Schallar et al., was the first in
presenting the systematic study for the incidence of
TCR during manipulation of the central part of the
trigeminal nerve in addition to the peripheral TCR as
a common and well accepted concept during tumour
surgery in the cerebellopontine angle.[13]
Based on the anatomical differences in terms of the
stimulus site and properties, peripheral stimulation differs
from the central in the possibility for the HR to rebound
and produce a delayed tachycardia. That is explained
by the synergistic action of both, the sympathetic nerve
with the positive inotropic effect and the vagus nerve
with the negative chronotropic effect to the heart in
order to maintain a greater cardiac output, efficient stroke
volume and arterial pressure giving a longer duration of
time for ventricular filling and a strong contraction of
the myocardium. On the other hand, central stimulation
produces a pure cardiac vagal nerve activity.[11]
The central type induced by stimulation of the
gasserian ganglion will produce bradycardia, apnea
and hypotension. Each type of the above - mentioned
reflexes has a different afferent pathways, but all share
the same efferent pathway which is through the motor
nucleus of the vagus nerve.[5]
The peripheral has 3 subtypes, which are the OCR, MCR
(both inducing bradycardia, apnea and normotension)
and the third type, which is a diving reflex stimulated
by the anterior ethmoidal nerve inducing bradycardia,
apnea and hypertension.
Journal of Health Specialties / April 2016 / Vol 4 | Issue 2
Pathophysiology
The exact physiology of this phenomenon is not well
understood unlike the OC reflex, which is considered
a subtype of TCR, which is a widely investigated
and well-established clinical phenomenon that is
induced by mechanical stimulation of ocular and
periocular structures innervated by the ophthalmic
nerve. [12]
Trigeminal nerve is the largest cranial nerve with
three major branches; two sensory branches named
ophthalmic (CN V1), maxillary (CN V2), and a mixed
sensomotor nerve named mandibular (CN V3). [14]
TCR is caused by stimulation of any of the sensory
branches of the trigeminal nerve. However, each
branch shows some variation in the projection pattern
according to the type, strength, and site of the noxious
stimulus.[5,7,15] TCR can be subdivided according to the
causative branch into; OCR and maxillomandibular
reflex.[5]
They all converge on the trigeminal ganglion (gasserian
ganglion) located within the Meckel’s cave in the
petrous part of the temporal bone in the middle fossa
(which is a triggering site). From the trigeminal ganglion,
a single large sensory root enters the brainstem in the
floor of the fourth ventricle to the pons in its midway
of its lateral side; at the same level, a smaller motor root
emerges.[14] This afferent pathway continues along the
short internuncial nerve fibres in the reticular formation
where the connection between the afferent with the
efferent pathway originates from the motor nucleus of
the vagal nerve. The efferent pathway sends depressor
fibres to the myocardium inducing the reflex.[12]
The sensory branches of trigeminal nerve first relay
in the ventral superficial medullary dorsal horn based
on the previous animal study. So, the autonomic
nervous system must be mediated by the trigeminal
nerve in the lower brainstem to explain the relationship
between the bradycardia induced parasympathetic
and vasoconstriction induced sympathetic in addition
to the central respiratory inhibition (apnea).[7,12] The
projection of sensory fibres of spinal trigeminal nerve
extends to certain brainstem sites are known to be
involved in cardiovascular regulation which are pars
caudalis (Sp5C) that projects directly or indirectly to
lateral parabrachial nucleus, RVLM and the caudal A5
catecholaminergic cell group (it is sympathoexcitatory
for central cardiovascular regulation, especially,
the baroreceptor reflex mechanism).[7,15] Allen and
Pronych identified these sites in 1996 when they used
cobalt chloride or lidocaine (local anaesthesia) as
microinjection into specific sites in the brainstem. The
pressor response was markedly attenuated following
injection of chemical blocker into RVLM.[15]
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Shanab and Albargi: TCR
Types of stimulus
There are different types of stimulations that can be
reflexogenic and these can be categorised into electrical,
chemical and mechanical types.[7] Certain types can
modify the TCR incidence electrically like high voltage
of electrical stimulation reaching up to 20 - 30 Hz in order
to stimulate the vagus nerve. Mechanical stimulation
in the form of sudden and sustained onset of traction
can be more triggering than a gradual and gentle one.[2,6]
Chemical stimulation is similar to the microinjection of
a presynaptic blocker or local anaesthesia like lidocaine
which blocks the synaptic transmission by acting on
active voltage sensitive sodium channels on neuronal
cell bodies.[15] Either tobacco or vapor is also considered
a stimulus for nasopharyngeal reflex. [11] Another
chemical stimulation is H2O2 in chemical sensitization
of the dura mater that is related to the oxygen liberated
in addition to the exothermic reaction of the H2O2 and
the liberated energy could be a volume expander upon
the vital structures and a potential triggering factor for
TCR.[14] Several factors account for the TCR occurrence,
but hypercarbia is considered a significant factor even
in weak stimulus.[2]
Incidence of trigeminocardiac reflex
It varies according to the type of stimulus and location.
In the literature, 90% of TCR occur most frequently in
ophthalmic surgery, followed by 8 - 18% in skull base
surgery and the least incidence in craniofacial surgery,
1 - 2%.[7]
In ophthalmic surgery, higher incidence of OCR was
found to be in corrective surgeries for strabismus
reaching 32 - 90%.[2,10] Eighteen cases of OCR were
reported by Blank including pressure on the globe,
retrobulbar block, massage of the eye after the block,
intraorbital haematoma, pressure from post-enucleation
haemorrhage and midface disimpaction.[16] Lateral and
medial recti muscles were reported to induce higher
incidence of OCR. However, there was no statistical
difference in reflex intensity between each of them,
on stimulating the same eye. In recent studies, medial
rectus is not considered refloxegenic, but fatigue
resistant more than any other extraocular muscle.[2]
Neurosurgeons have reported incidences of TCR
during surgery of skull base lesions,[17] cerebellopontine
angle tumours,[8,13] giant chronic subdural haematoma
removal[14] and transection of sensory roots of the
trigeminal nerve (rhizotomy).[18]
In 1967, Tessier (a plastic surgeon) was the first
to mention the incidence of TCR in craniofacial
reconstruction.[6] TCR has been mentioned in several
maxillofacial procedures including:
154
Trauma
• Midface disimpactions which was first reported
by Roubideaux in 1978 in an attempt to correct
posteriorly displaced midface post-trauma. [16]
In 1989, Reaume and MacNicol reported OCR
during Le Fort 1 osteotomy in a patient with
mandibulofacial dysostosis.[4]
• Elevation of zygomatic arch fracture; two cases
of bradycardia were reported by Shearer et al., in
1987 and Loewinger et al., in 1987.[19,20] One case of
asystole was reported by Bainton et al., 1987.[21]
• Nasoethmoid fracture reduction, Baxandall et al., in
1989.[21]
• Panfacial fracture. A case of sinus arrest was reported
by Bainton et al., in 1990 complicating a bitemporal
approach in the treatment of the panfacial fracture.
[22]
• Sires et al., in 1999 reported an incidence of
OCR during repair of an orbital floor trapdoor
fracture with incarcerated orbital soft tissue in
the maxillary sinus and/or entrapment of inferior
rectus muscle. The latter type of fracture is
commonly seen in children and young adults who
show bone resiliency; these patients experienced a
triad of bradycardia, nausea and syncope following
an orbital injury.[23]
• Periorbital laceration manipulation, another case of
asystole was reported by Osborn et al., in 2008.[22]
• In a patient with stable zygomaticomaxillary
complex fracture with temporal artery laceration, a
case was reported by Siddharth et al., in 2012, when
the incidence of asystole occurred even without any
surgical intervention for fixing the fracture. It was
thought to be from the high vagal tone the patient
had because he was an athlete, in addition to the
oedema over the trigeminal nerve.[24]
Orthognathic surgery
• During Le Fort 1 osteotomy reported by Ragano et al.,
in 1989,[22] three cases of asystole were reported by
Lang et al., in 1991 including Le Fort 1 and bilateral
sagittal split osteotomy.[1] Campbell et al., in 1994
reported an incidence of asystole during splitting
a maxillary tuberosity in an orthognathic case of
Le Fort 1 and Hofer’s osteotomies.[25] Precious et al.,
in 1990 reported an incidence of 1.6% of either
asystole or bradycardia seen in 6 patients during
maxillary advancement.[26]
Temporomandibular joint surgery
• Distraction or insufflations of the temporomandibular
joint (TMJ) in arthroscopy, reported by Gomez et al.,
in 1991.[27] In 1996, Morey and Bjoraker reported a
similar incidence during TMJ arthrotomy.[22] That
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Shanab and Albargi: TCR
was because of the auriculotemporal nerve lying
being medial to the mandibular condyle, which
is afferent for the reflex.[4] Precious et al., in 1990
reported either bradycardia or systole in 2 patients
during manipulation of temporalis muscle in
correcting total bony ankylosis.[26]
Reconstruction and cosmetic surgery
• 25 patients out of 100 cases of blepharoplasty
experienced OCR during traction on one of the
orbital fat compartment, Matarasso 1989.[28]
• Orbital reconstruction in orbital blowout fractures
was reported by Chesley and Shapiro, in 1989,
Ziccardi et al., in 1991, Hirjak et al., in 1993 and
Vasudev and Reddy, in 2011.[22]
• Slade and Cohen in 1999 reported a case of OCR
due to retraction of levator-superior rectus complex
during endoscopic forehead lift surgery.[29]
• Nasal fracture reconstruction, Locke et al., in 1999.[17]
• Blepharoplasty, a case of asystole reported by
Rippmann et al., in 2008.[22]
Dentoalveolar
• Mesiodens removal, a case reported by Webb et al.,
in 2007.[21,22]
• Extraction, Arekere et al., in 2010.[22]
Management
The most important way to treat the occurrence of the
reflex is to stop the procedure and interrupt the eliciting
mechanism. It can be reversed within 20 s after ceasing
the manipulation. Subsequently the surgeon can resume
the procedure after modifying his/her manoeuvre.
Sometimes, there is a need to apply anticholinergic
medications but a surgeon’s modification would be
more than enough.[17] Atropine and glycopyrrolate are
commonly used anticholinergic medications to reverse
the cardiac inhibitory vagal effect and regain the normal
sinus rhythm.[18]
Local anaesthesia or anticholinergic medications can
be used for recurrent or refractory cases, respectively.
Cardiac massage that accompanies serious morbidity
should be reserved for last after all measures fail.[25]
Complication
The outcome from the reflex postoperatively can be
awful and associated with lifelong impairments because
of the ischaemic complications from the massive drop of
arterial pressure, especially in those patients with poor
vascularity due to atherosclerosis or tumour encasement
and may lead to subsequent cardiac or cerebral
infarctions.[8] One of the ischaemic effects reported
was of hearing function complication in a patient who
Journal of Health Specialties / April 2016 / Vol 4 | Issue 2
developed TCR during vestibular schwannoma surgery.
TCR can develop a very serious outcome. There has been
a reported deaths following this reflex.[19] One report
indicated there were 60 deaths from OCR.[25]
In the literature, most of the articles were case reports or
study of TCR in a particular type of surgery. This study
is unique because of the number of cases included and
more than one type of procedure involved. There was a
high percentage of trauma surgeries due to the location
of the hospital by the highway that received trauma
cases frequently. The close percentage of both trauma
and reconstructive surgeries is because reconstructive
surgeries were mainly to repair the defects secondary
to trauma. Similar studies must be conducted in other
institutions with low trauma interest.
Reconstructive surgeries had the highest incidence
of TCR, and they were all orbital reconstructions
which still support the literature mentioning strong
relationship between orbital surgeries and TCR more
than that in the maxillomandibular area.
The included cases were considered to carry a high risk
for the occurrence of TCR. So another study is needed to
evaluate the incidence of TCR in maxillofacial surgery
involving the soft tissue of the middle and lower face
as well as surgeries involving TMJ. In this study, we did
not discuss the possible risk factors affecting TCR or
if prophylactic medications have been used and their
rules in preventing the occurrence of TCR. So another
study in this regard is needed.
CONCLUSION
Ophthalmic surgeries including strabismus, orbital
exenteration and fractures in children with cardiac
disease are considered to be high risk procedures while
skull base surgery falls in the middle zone of the risk
band. Finally, insufflations of TMJ, Lefort 1 osteotomy
and elevation of zygomatic fractures are considered low
risk surgeries.[21]
TCR is a significant reflex and should be taken in to
consideration because of its potential complications
and morbidities.
Surgeons must strictly follow guidelines for managing
TCR as illustrated by Arasho et al., in 2009 as following:
1. Avoidance of the risk factors using gentle and
delicate operating techniques.
2. Prophylactic intravenous (IV) sympathomimetics
or peripheral nerve block in peripheral trigeminal
nerve manipulation.
3. Close monitoring of the patient during anaesthesia in
those high risks for TCR, including the use of ECG.
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Shanab and Albargi: TCR
4. Early detection and recognition.
5. Treatment includes:
a. Stopping of the procedures that provoke the
reflex.
b. Administration of IV vagolytics.
c. Local anaesthesia as an afferent blocker of the
reflex arc for refractory cases.
All of these points could help manage the patient
safely from very harmful and fatal events.[6] There were
more than 60 deaths reported from OCR regardless
of the use of local anaesthesiologist. These can be
prevented with the cooperation of the surgeon and
the anaesthesiologist.[1,2] Maxillofacial surgeons must
be aware of the time zone for repairing facial fracture,
which is critical and must be undertaken on the
same day as much as possible not only to prevent
life-threatening cardiac arrhythmias but also the
permanent deformities (restrictive strabismus) arising
from ischemic necrosis of the muscles.[23]
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
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Journal of Health Specialties / April 2016 / Vol 4 | Issue 2