Jaw-stretch reflex is weaker in patients afterorthognathic surgery

Yi Luo a, Peter Svensson b,c, Janek Dalsgaard Jensen d, Thomas Jensen d,Bjarne Neumann d, Lars Arendt-Nielsen a, Kelun Wang a,d,*

aCenter for Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Faculty of Medicine,

Aalborg University, Fredrik Bajers Vej 7 D2, 9220 Aalborg, Denmarkb Section of Clinical Oral Physiology, School of Dentistry, University of Aarhus, Vennelyst Boulevard 9, DK-8000

Aarhus C, DenmarkcCenter of Functionally Integrative Neuroscience (CFIN), MindLab, Aarhus University Hospital, 44 Norrebrogade,

Aarhus, DenmarkdDepartment of Oral & Maxillofacial Surgery, Aalborg Hospital, Aalborg, Denmark

a r c h i v e s o f o r a l b i o l o g y 5 9 ( 2 0 1 4 ) 1 3 2 1 – 1 3 2 7

a r t i c l e i n f o

Article history:

Accepted 8 August 2014

Keywords:

Jaw-stretch reflex

Orthognathic surgery

Dentofacial deformities

Physiology

Masticatory muscles

Electromyography

a b s t r a c t

Objectives: The jaw-stretch reflex (JSR) was studied in both patients and healthy participants

in order to investigate the possible long-term impact of orthognathic surgery on the motor

function of the masticatory system.

Design: JSR was measured in patients before surgery (PC), 1 year after surgery (PS) and in

healthy controls (HC) (N = 31 in each group). JSR was evoked by a standardized stretch device

and recorded bilaterally from masseter and anterior temporalis muscles using surface

electromyography (EMG).

Results: The peak-to-peak amplitude (which was normalized to pre-stimulus EMG activity)

of JSRs in PC and PS were significantly smaller than in HC (P < 0.001; P < 0.001). The onset

latency in PS was significantly longer compared with HC (P < 0.05). The duration of JSR in PS

was significantly longer than in HC and PC (P < 0.001; P < 0.05).

Conclusion: Patients with dentofacial deformities are characterized by reduced JSR ampli-

tude. The delayed onset and elongated duration of JSR might be potential indicators of a

long-term surgical impact on the motor function of the masticatory system.

# 2014 Elsevier Ltd. All rights reserved.

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1. Introduction

The jaw-stretch reflex (JSR) is a short-latency monosynaptic

reflex serving to maintain posture and to fine-tune the

voluntary movements of the mandible.1,2 JSR is described as

the brisk twitch of the jaw-closing muscles as a response to a

sudden stretch of the muscles. The major receptors to the

* Corresponding author at: Center for Sensory-Motor Interaction (SMI), DAalborg University, Fredrik Bajers Vej 7 D2, 9220 Aalborg, Denmark. T

E-mail address: kelun@hst.aau.dk (K. Wang).http://dx.doi.org/10.1016/j.archoralbio.2014.08.0060003–9969/# 2014 Elsevier Ltd. All rights reserved.

stretch are the muscle spindles which are composed of

intrafusal muscle fibres and embedded in the bulky extrafusal

muscle fibres of the jaw-closing muscles. When stimulated,

the muscle spindle afferent signals are transmitted to many a-

motor neurons innervating the extrafusal muscle fibres via the

brain stem trigeminal motor nucleus and a brief synchronous

activation of the jaw-closing muscle motor units ensues.1 The

evaluation of JSR can provide essential information on the

epartment of Health Science and Technology, Faculty of Medicine,el.: +45 9940 8745; fax: +45 9815 4008.

a r c h i v e s o f o r a l b i o l o g y 5 9 ( 2 0 1 4 ) 1 3 2 1 – 1 3 2 71322

motor control of the muscular performance. JSR can be evoked

by tapping on the chin with a tendon hammer in a clinical

setting. More accurately, JSR can be induced by a standardized

jaw-stretch device which has been intensively used to study

JSR and allows a high degree of control with the stretch

stimulus.3,4

It has been suggested that several factors, such as

background electromyography (EMG) activity and bite posi-

tion, may affect JSR.4 The presence of chronic orofacial painful

conditions and experimental acute muscle pain has also been

well documented to facilitate JSR.5–7 The peak-to-peak ampli-

tude of JSR has been observed to increase during pain

condition. It has been suggested that the facilitation of JSR

in pain condition serves as a protective function since it may

reduce the jaw mobility, which as a result may reduce the

muscle pain.7–9

However, so far no studies have reported JSR recordings in

patients with dentofacial deformities or in patients after

orthognathic surgery (OS). Compared with healthy individua-

ls, patients with dentofacial deformities are characterized by

disharmonious dental and skeletal structures. It has been

reported that these patients tend to report more frequent

headache and more pain in the orofacial region.10,11 However,

it is not clear whether the different anatomic structures and

the presence of pain have certain influence on the JSR of these

patients. OS aims to improve the occlusal relationship, the

function of the masticatory system and the facial aesthetics in

these patients. After OS inevitable changes of structures take

place in various tissues of the masticatory system. In addition,

a somatosensory function alteration in the trigeminal region is

a common complication following OS.10,12 It has been

indicated that 15%–20% of patients reported ongoing pain 6

months to 1 year after OS.13,14

The aims of the present study were to investigate: (1) the

influence of dentofacial deformities on JSR, (2) the possible

long-term surgical impact of OS on JSR, and (3) the influence of

pain on JSR.

2. Materials and methods

2.1. Participants

Thirty-one patients (16 women and 15 men, mean age

28.2 years) were recruited 1 year after OS, subsequently

mentioned as the surgical patient group (PS). Thirty-one

age- and gender-matched patients were recruited before OS

and served as the patient control group (PC). Further, thirty-

one age- and gender-matched healthy participants served as

the healthy control group (HC).

Table 1 – Numbers of patients with various subgroups of den

Group Skeletal classification

Class I Class II Class III D

PS 2 18 11

PC 3 14 14

PC = patient control (patient before surgery); PS = surgical patient (patien

All the patients were recruited from the Department of Oral

and Maxillofacial Surgery, Aalborg Hospital, Denmark. Inclu-

sion criteria for both PS and PC group: a developmental dento-

skeleto-facial disharmony; complete dentitions (with the

exception of premolars in some cases due to orthodontic

treatment needs and with the exception of the third molars in

some cases); aged between 18 and 40 years; scheduled for a

combined orthodontic–orthognathic treatment. Exclusion

criteria for both PS and PC group: A congenital anomaly

(i.e., cleft lip and palate) or acute trauma; previous facial

surgery; pregnant at baseline; a medical condition associated

with systemic neuropathy (i.e., diabetes, hypertension, kidney

problems). The types of dentofacial deformities were well-

matched between PS and PC groups (Table 1). In the PS group,

twenty patients had been treated with Le Fort I maxillary

osteotomy (Le Fort I) in combination with bilateral sagittal split

ramus osteotomy (BSSRO) and eleven patients had received

single jaw surgery (six patients had undergone Le Fort I and

five patients had undergone BSSRO). All PS patients had

finished their orthodontic treatment and were without braces.

All PC patients were in the stage before or just at the beginning

of their orthodontic treatment, free of braces.

All healthy participants in the HC group were recruited

among students at Aalborg University. Inclusion criteria for

the HC group: complete dentitions (with the exception of third

molars in some cases); Class I skeletal and dental relation-

ships; aged between 18 and 40 years. Exclusion criteria for the

HC group: Previous facial surgery; jaw muscle/temporoman-

dibular joint (TMJ) pain, headaches, other symptoms of pain in

the craniofacial region or other parts of the body during the

past year; any jaw dysfunction (checked at the clinical

examination and by means of the questionnaires Research

Diagnostic Criteria for Temporomandibular Disorders (RDC/

TMD))15; pregnant at baseline; a medical condition associated

with systemic neuropathy (i.e., diabetes, hypertension, kidney

problems).

This study was approved by the local ethics committee

(Project number: N-2008-0057) in accordance with the Helsinki

Declaration II. Written informed consent was obtained from

all participants before they were included in the study. All

participants were identified by means of numbers only.

2.2. Self-reported pain and sensory testing

All patients were assessed using clinical examinations and the

questionnaires RDC/TMD.15 Further, they were diagnosed

with a corresponding subtype of TMD when applicable. For

patients with orofacial pain, the pain intensity of the last 6

months and at the time of the experiment was rated on a

numerical rating scale from 0 to 10 where 0 was ‘no pain’ and

tofacial deformities.

Vertical morphology abnomality Facial asymmetry

olichofacial Brachyfacial

8 2 3

9 3 3

t 1 year after surgery).

a r c h i v e s o f o r a l b i o l o g y 5 9 ( 2 0 1 4 ) 1 3 2 1 – 1 3 2 7 1323

10 was ‘the worst pain imaginable’. Furthermore, quantitative

sensory testing (including measurement of warm detection

threshold (WDT), cold detection threshold (CDT), heat pain

threshold (HPT), cold pain threshold (CPT), pressure pain

threshold (PPT), vibration detection threshold (VDT)) were

performed on the facial skin innervated by the trigeminal

second and third branches in patients after surgery to detect

possible sensory alterations other than pain. Data of HC group

were also recorded and set as reference. Then the percentage

of sensory alterations was counted for PS groups based on the

reference data. Detailed methods of quantitative sensory

testing in the orofacial region were described by our previous

study.16

2.3. Jaw-stretch reflex recording

JSR was evoked by the standardized jaw muscle stretch device

described by Miles.3 Briefly, a stainless-steel bite-bar was

mounted on a frame attached to the floor. A powerful

electromagnetic vibrator (Ling Dynamic Systems, model 406,

UK) imposed servo-controlled displacements of the lower jaw

bar. The displacement of the vibrator probe was measured

with a linear potentiometer (Sakae Type 20 FLP 30A-5 K, Japan)

mounted in parallel with the probe. Acceleration in the

vertical plane was measured by an accelerometer (Delta Tron1

Accelerometer Type 4399, Bruel & Kjær, Denmark) mounted on

the lower jaw bar.6 JSR was recorded from the masseter and

the anterior temporalis muscles on both sides. Bipolar

disposable surface electrodes (4 � 7 mm recording area, 720-

01-k, Neuroline; Medicotest) were placed 10 mm apart along

the central part of the masseter and the anterior temporalis

muscles on both sides. A reference electrode was attached to

the right wrist. Before the JSR recording the average

electromyography (EMG) value of the maximal voluntary

contraction (MVC) of the left masseter muscle was obtained

and was arbitrarily set as the 100% value for the subsequent

visual feedback. During JSR recording each participant was

instructed to bite on the jaw bars of the stretch device with the

incisors, exerting a 15% level of the EMG-MVC. The participant

achieved this by receiving visual feedback from markers

changing from red to green on a computer screen. When this

was achieved, the jaw bars were automatically triggered to

stretch the jaws. The initial distance between the jaw bars was

Fig. 1 – Electromyography

4.0 mm. The displacement between the bars was set as 1 mm

with a ramp time of 10 ms. For each individual, 20 sweeps of

stretch were averaged for analysis. The EMG signals were

amplified 2000–5000 times (Counterpoint MK2, DK), filtered

with bandpass 20 Hz to 1 kHz, sampled at 4 kHz and stored for

off-line analysis.

A special-purpose computer programme (Aalborg Univer-

sity) was subsequently used to analyze the JSR responses. All

the reflex parameters were determined objectively by using

the computer programme.4,6,9 The pre-stimulus EMG activity

was calculated from the rectified recordings of the 100 ms

interval prior to the stretch stimulus. The onset latency,

duration, and the peak-to-peak amplitude of JSR were

calculated from the non-rectified recordings. The peak-to-

peak amplitude was then normalized through the formula:

Normalized peak-to-peak amplitude = (peak-to-peak ampli-

tude/pre-stimulus EMG activity) � 100%. The purpose of the

normalization was to rule out the influence of different

background of pre-stimulus EMG activity and to eliminate the

influence of other factors which influence the absolute

magnitude of an EMG (skin thickness, skin impedance, muscle

size etc.) (Fig. 1 shows detailed components of JSR).

2.4. Statistical analysis

Pain frequencies were analyzed using the Chi-square test, and

pain scores were analyzed by an independent t-test. The data

of JSR parameters were analyzed using four-way repeated

measure ANOVA, with group and the presence of pain as

between-subject factors, and muscle (masseter, temporalis)

and side (left, right) as within-subject factors. Sphericity was

checked for between-subject factors before each repeated

measure ANOVA analysis. When sphericity was rejected, the

result of a Greenhouse–Geisser test was read instead. The

Bonferroni test was employed as the post hoc test. The

significance level was set as 0.05.

In order to demonstrate the size of the differences between

the two patient groups independently of the different units of

the JSR parameters, Z-transformation of data was conducted.

The data of healthy control group were set as the reference

data for Z-score transformation, and all the patients data were

transformed based on the reference data. The units of

parameters were eliminated after the transformation. The

of jaw-stretch reflex.

Table 2 – Frequency and intensity of pain.

Group Number ofpatients

Pain of last 6months

(mean � SD)

Pain now (mean � SD) RDC/TMD diagnosis (frequencya)

Total Pain Average Average

PS 31 6 3.3 � 1.2 2.0 � 1.1 Ia (3), Ib (1), IIa (2)

PC 31 11 3.8 � 1.3 3.1 � 1.7 Ia (8), Ib (2), IIa (1), IIIa (2)

x2 p = 0.155 t-test p = 0.45 p = 0.17

PC = patient control; PS = surgical patient. Chi-square test showed that there was no correlation between treatment status (before or after

surgery) and the frequency of pain in the two patient groups. There was no significant difference between groups in pain scores (0–10) over the

last 6 months and at the time of the experiment (t-test). Ia: myofascial pain; Ib: myofascial pain with limited opening; IIa: disc displacement

with reduction; IIIa: arthralgia.a When IIa or IIIa was diagnosed on both left and right sides in the same subject, the frequency was counted as two.

a r c h i v e s o f o r a l b i o l o g y 5 9 ( 2 0 1 4 ) 1 3 2 1 – 1 3 2 71324

aim of this transformation was to more clearly demonstrate

the deviation of the patients from the healthy subjects.

Regardless of the original distribution of the data, the shift by

Z-transformation always produces a distribution with a mean

of 0 and a standard deviation of 1. A Z-score which is a score

indicating how many standard deviations an observation is

from the mean of the distribution could then be calculated. Z-

scores were calculated for each individual patient in the PS

and PC groups. The formula was: Z-score = (individual value –

meanHC)/SDHC. If the resulting Z-score exceeded �1.96

(outside the 95% confidence interval), it was deemed an

abnormal value. A Z-score above zero was defined as

strengthening of JSR, while a Z-score below zero was defined

as weakening of JSR. Signs of Z-scores of JSR parameters were

adjusted according to this definition.

3. Results

3.1. Self-reported pain and sensory alteration

Pain frequency and intensity of PS and PC groups are shown in

Table 2. No significant difference was found for pain frequency

(P = 0.155) or pain intensity (P > 0.17) between the PS and PC

groups. Myofascial pain was the dominant subtype in pain

patients in both PS and PC groups. Compared with HC group,

64.5% (20 out of 31) patients in PS group exhibited sensory

alteration at least in one parameter on one testing site. PS

patients with or without pain were both characterized by

similar sensory alteration pattern which demonstrated sen-

sory loss in thermal parameters (WDT, CDT, HPT, CPT) and

non-nociceptive mechanical parameters (VDT), and sensory

gain in nociceptive mechanical parameters (PPT).

3.2. Jaw-stretch reflex

Group differences were found in normalized peak-to-peak

amplitude (P < 0.001) (Fig. 2A). The post hoc test indicated that

the normalized peak-to-peak amplitudes in PC and PS were

significantly smaller compared with HC (P < 0.001; P < 0.001).

However, no significant difference was found between PC and

PS (Fig. 2A). Significant differences were found between

masseter muscle and temporalis muscle in normalized

peak-to-peak amplitude (P = 0.002), with masseter muscle

showing higher values (Fig. 2A). No significant difference was

detected between patients with or without pain. No significant

difference was detected between left and right sides.

Group differences were also found in the onset latency

(P = 0.002) (Fig. 2B) and the duration (P < 0.001) (Fig. 2C) of JSR.

The onset of JSR in PS was significantly delayed compared with

HC (P = 0.001), but no significant difference was found between

PS and PC or between PC and HC (Fig. 2B). The duration in PS

was significantly longer than in HC and PC (P < 0.001;

P = 0.045), but no significant difference was found between

HC and PC (Fig. 2C). Significant difference was found between

masseter muscle and temporalis in the duration (P = 0.006),

with masseter muscle showing lower values (Fig. 2C), but this

was not detected in the onset latency. No significant difference

was detected between patients with or without pain. No

significant difference was detected between left and right

sides in the above parameters.

3.3. Individual Z-score and percentage of abnormal Z-score

Z-scores were calculated for muscle and side. Abnormal Z-

scores were detected at 30 sides in the masseter muscle

(48.4%) and at 24 sides in the temporalis muscle (38.7%) in PS

patients (62 sides in total for each muscle). Likewise, abnormal

Z-scores were detected at 11 sides in the masseter muscle

(17.7%) and at 13 sides in the temporalis muscle (21.0%) in PC

patients (62 sides in total for each muscle). Data of individual

and average values of patients from both groups are shown in

Fig. 3A–D. Positive Z-scores higher than 1.96 were scarcely

found in any parameters in both groups. However, negative Z-

scores lower than �1.96 were mostly found in parameters of

onset latency and duration in the PS group and with larger

deviations in the PS group. Percentages of abnormal Z-score of

the two groups were stacked for each parameter in Fig. 3E and

F, with the PS group showing an overall higher percentage of

abnormal value.

4. Discussion

For the first time JSR has been studied between two groups of

patients with dentofacial deformities before and after OS. The

main findings of the present study suggest that patients in

Fig. 2 – Data of jaw-stretch reflex parameters. Normalized peak-to-peak amplitude (A), onset latency (B) and duration (C)

(mean W SE) of jaw-stretch reflex in healthy subjects (HC), patients before surgery (PC) and patients one year after

orthognathic surgery (PS). *Significant group difference. n.s. = not significant.

a r c h i v e s o f o r a l b i o l o g y 5 9 ( 2 0 1 4 ) 1 3 2 1 – 1 3 2 7 1325

both groups demonstrate the weakening of JSR, which is

independent of treatment. Compared with healthy partici-

pants, patients with dentofacial deformities before OS are

characterized by reduced JSR amplitude. Patients after OS are

also characterized by reduced JSR amplitude. In addition, the

delayed onset and elongated duration of JSR in patients after

OS might indicate impairment of the motor circuitry. Howev-

er, its clinical significance for the function of the masticatory

system remains unknown from the present study. Further, the

presence of pain did not show significant modification on JSR.

4.1. Influence of dentofacial deformity

Since all PC patients were brace free when they participated in

this experiment, the confounding effect of orthodontic treat-

ment on JSR could be ruled out. Other factors that might affect

JSR during isometric contractions such as biting position,

stretch displacement, ramp time and clenching level4 were all

carefully controlled in this study. The background EMG activity

was also carefully controlled through normalization of the

reflex amplitude as JSR amplitude has been found to be

proportional to the level of pre-stimulus EMG activity to a

given stimulus.4 Therefore, the condition of dentofacial

deformity most likely had a major influence on JSR resulting

in smaller JSR amplitude in patients before OS. Similarly, a

previous study of patients with facial asymmetry17 demon-

strated a negative correlation between abnormal skeletal

structure and masseter vibration reflex activity. The smaller

amplitude might be due to less excitability of the muscle

spindles, fewer activated a-motor neurons and, as a result,

fewer motor units recruited in the jaw muscles. It is unclear

whether the weak JSR in these patients was a compromise in the

motor control function or a functional adaptation to the

abnormal anatomic structures. In addition, it needs to be

Fig. 3 – Individual and average Z-scores and percentage of abnormal Z-score of jaw-stretch reflex parameters in patients

(counted by side). PC = patient control (total sides n = 62); PS = surgical patient (total sides n = 62). (A) Z-score of masseter

muscle in PS patients; (B) Z-score of masseter muscle in PC patients; (C) Z-score of temporalis muscle in PS patients; (D) Z-

score of temporalis muscle in PC patients; (E) stacked percentage of abnormal Z-score for masseter muscle in PS and PC

groups; (F) stacked percentage of abnormal Z-score for temporalis muscle in PS and PC groups. Norm P–P = normalized

peak-to-peak amplitude.

a r c h i v e s o f o r a l b i o l o g y 5 9 ( 2 0 1 4 ) 1 3 2 1 – 1 3 2 71326

further elucidated whether different skeletal abnormalities

affect JSR differently, to which direction and to what extent.

4.2. Surgical impact

Three-dimensional mass structure changes take place after

OS. In order to take adaptation and relapse into account, the

data of the PS group were collected 1 year after OS. On the one

hand, due to the improvement of skeletal structures the

changes in position, orientation and length of muscles

towards normal range might affect the jaw muscle tone,

which might affect JSR. On the other hand, the invasive

surgical procedure and its complications, such as tissue

injuries and swelling, might also impact JSR. Reduced

amplitude and delayed onset of blink reflex have been

observed after OS due to damage to the mental nerve.18

Damage to the lingual nerve can lead to no or delayed jaw-

opening reflexes in rats.19 The mechanism of JSR is different

from the above reflexes, but it is similar that the cause of the

weakening of the JSR (reduced peak-to-peak amplitude and

delayed onset) might be due to the potential direct or indirect

surgical injuries to the nerve conduction pathway. The major

receptors of JSR are muscle spindles innervated by g-motor

neurons and the afferent signals are transmitted to the brain

stem by type Ia and II afferent fibres.20 Those fibres are

responsible for detecting information of changes in the muscle

length. The efferent signals from the trigeminal motor nucleus

then lead to an increase in the a-motor neuron innervated

muscle activity.1 It is possible that damage or modulation in

some parts of the circuit loop caused by OS might slow down

the nerve conduction, which might lead to the delaying of the

reflex. In turn, the synchronization of the action potentials in

different nerve fibres would be reduced, which might

consequently reduce the peak-to-peak amplitude and in-

crease the duration of the response.

4.3. Influence of pain

The presence of jaw muscle pain has been well documented to

facilitate JSR resulting in increased JSR amplitude.5,6 Although

a r c h i v e s o f o r a l b i o l o g y 5 9 ( 2 0 1 4 ) 1 3 2 1 – 1 3 2 7 1327

PC and PS patients reported TMJ/muscle pain, no significant

facilitation of JSR amplitude was found. This might be due to

the finding that the pain intensity of these patients was too

low (pain scores were around 2–3 out of 10) to modulate JSR.

Also, the total number of patients with pain might be relatively

small to show a significant difference. Another possible

explanation could be that the condition of dentofacial

deformities might serve as a more potent influential factor

on JSR which may offset the effect of pain.

5. Conclusions

In conclusion, the present results suggest that, compared with

healthy subjects, a weakening of JSR exists in patients both

before and after OS. Patients with dentofacial deformity are

characterized by reduced JSR amplitude. The delayed onset

and longer duration of JSR might be potential indicators of

long-term surgical impact on the motor function of the

masticatory system.

Funding

This study was supported by Det Obelske Familiefond of

Denmark (grant no. BG/mp 20112-16860 C1).

Competing interests

The authors declare no conflicts of interest.

Ethical approval

This study was approved by the Regional Ethical Committee of

North Jutland, Denmark. The Project number is N-2008-0057.

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