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Received: 17 July 2018    Revised: 30 August 2018    Accepted: 26 September 2018

DOI: 10.1111/joor.12733

ORIGINAL ARTICLE

Effectiveness of mobilisation of the upper cervical region and

craniocervical flexor training on orofacial pain, mandibular
function and headache in women with TMD. A randomised,
controlled trial

Letícia B. Calixtre1  | Ana Beatriz Oliveira1 | Lianna Ramalho de Sena Rosa1 | 

Susan Armijo-Olivo2,3 | Corine M. Visscher4 | Francisco Alburquerque-Sendín5

1
Laboratory of Clinical and Occupational
Kinesiology (LACO), Department of Physical Summary
Therapy, Federal University of São Carlos Background: Studies exploring interventions targeting the cervical spine to improve
(UFSCar), São Carlos, Brazil
2
symptoms in patients with temporomandibular disorders (TMD) are limited.
Faculty of Rehabilitation
Medicine, University of Alberta, Edmonton, Objectives: To determine whether mobilisation of the upper cervical region and
Alberta, Canada
craniocervical flexor training decreased orofacial pain, increased mandibular func-
3
Institute of Health Economics, Edmonton,
tion and pressure pain thresholds (PPTs) of the masticatory muscles and decreased
Alberta, Canada
4
Department of Oral Kinesiology, Academic headache impact in women with TMD when compared to no intervention.
Centre for Dentistry Amsterdam Methods: In a single-­blind randomised controlled trial, 61 women with TMD were
(ACTA), University of Amsterdam and Vrije
Universiteit Amsterdam, Amsterdam, The randomised into an intervention group (IG) and a control group (CG). The IG received
Netherlands upper cervical mobilisations and neck motor control and stabilisation exercises for
5
Department of Sociosanitary Sciences, 5 weeks. The CG received no treatment. Outcomes were collected by a blind rater at
Radiology and Physical Medicine, University
of Córdoba, Córdoba, Spain baseline and 5-­week follow-­up. Orofacial pain intensity was collected once a week. A
mixed ANOVA and Cohen’s d were used to determine differences within/between
Correspondence
Letícia B. Calixtre, Departamento de groups and effect sizes.
Fisioterapia, Universidade Federal de São Results: Pain intensity showed significant time-­by-­group interaction (P < 0.05), with
Carlos, São Carlos, Brazil.
Email: lecalixtre@hotmail.com significant between-­group differences at four and five weeks (P < 0.05), with large
effect sizes (d > 0.8). The decrease in orofacial pain over time was clinically relevant
Funding information
Fundação de Amparo à Pesquisa do Estado only in the IG. Change in headache impact was significantly different between
de São Paulo, Grant/Award Number: groups, and the IG showed a clinically relevant decrease after the treatment. No ef-
2014/05276 7
fects were found for PPT or mandibular function.
Conclusion: Women with TMD reported a significant decrease in orofacial pain and
headache impact after 5 weeks of treatment aimed at the upper cervical spine com-
pared to a CG.

KEYWORDS
manual therapy, neck exercises, neck mobilisation, randomised controlled trial,
temporomandibular joint disorders

Register Number: RBR-6c7rq4

J Oral Rehabil. 2018;1–11. © 2018 John Wiley & Sons Ltd |  1

wileyonlinelibrary.com/journal/joor  
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2       CALIXTRE et al.
1 |  I NTRO D U C TI O N
Temporomandibular disorder (TMD) is a collective term for a num-
ber of clinical problems involving the masticatory musculature,
temporomandibular joints (TMJs) and associated structures.1 Thirty-­
nine per cent of the general population present at least one sign
or symptom of TMD, 2 with females showing greater prevalence of
TMD than males.3 Although orofacial pain is the main complaint of
patients with TMD, earache and neck pain can also be associated
with TMD, as well as the decrease in the sensibility of the masti-
catory muscles.4 Joint noises, reduction in bite force, limitations in
mouth opening and deviation of the mandible during mandibular
movements are also common5 and could lead to a reduction in the
mandibular function.
The comorbidity of TMD and headache has been reported
as frequent, 6 and approximately 70% of the general population
who suffer from headache also present symptoms of TMD.7
Furthermore, the degree of disability associated with the headache
has been reported to be higher in patients with TMD compared to
asymptomatic subjects, 8 showing some impact of headache on pa-
tients with TMD.
Several physiotherapy modalities have been used to reduce TMD
symptoms.9 However, clinical trials of high methodological quality
are still required to strengthen the evidence for the effect of phys-
iotherapy interventions on TMD.9–11 A systematic review10 found
that a combination of manual therapy and exercises for the cervical
spine shows promise in the treatment of TMD. In addition, a recent
evidence compilation of randomised controlled trials highlighted
that there is emerging evidence supporting the use of cervical spine
treatment through neck exercises plus cervical mobilisations to im-
prove pain.12 This promising evidence could be related to the fact
that several studies have specifically reported that subjects with
TMD present abnormalities of the endurance and performance of
13
the neck flexors and extensors muscles. In particular, stabilisa-
tion exercises for the neck in combination with manual therapy for
the upper cervical spine14,15 have been found to increase maximum
mouth opening and to raise pressure pain threshold (PPT) in the
masticatory muscles in subjects with TMD. Nevertheless, because
of their methodological limitations (including lack of a control or a
placebo group), these studies provided limited evidence. A recent
11
systematic review of randomised controlled trials that applied
manual therapy techniques to treat TMD suggested that techniques
applied to the upper cervical spine are effective in reducing orofacial
pain. Still, the evidence from the included studies was mainly poor,
and the authors of the systematic review concluded that further
studies of higher methodological quality are needed to strengthen
the evidence regarding the effectiveness of manual therapy for man-
aging TMD.
In summary, the anatomical, neurophysiological, biomechani-
cal and clinical relationship between the upper cervical spine and
the orofacial region is an example of a regional interdependency
model,16 which justifies the importance of looking at cervical spine
and stomatognathic system as a functional entity when evaluating
and treating subjects with TMD.17 In fact, it is not uncommon that
clinicians plan exercises for the cervical spine in patients with
TMD based on their intuition, their own experience, but without
knowledge of the existence of impairment in the cervical spine
and its muscles.13 Thus, more research is needed to explore the
implications of the treatment focused on cervical spine and mus-
cles in TMD.
The aims of the present study were as follows: (a) to determine
whether mobilisation of the upper cervical region and craniocervical
flexor training over a 5-­week period can improve orofacial pain in
women with TMD when compared to a control group (CG); and (b) to
determine the differences between the intervention group (IG) and
the CG in terms of PPT of masticatory muscles, mandibular function
and headache impact at the end of the 5-­week treatment.
It was hypothesised that, after 5 weeks, the IG would experience
significantly reduced orofacial pain and headache impact and would
have significantly improved mandibular function and increased PPTs
of the masticatory muscles in comparison with the CG.
2 | M E TH O DS
2.1 | Study design
This was a single-­blind randomised controlled trial. To ensure ran-
dom concealment of allocation, opaque envelopes (sealed and num-
bered) were prepared by one of the researchers not involved in the
recruitment or the assessment of the subjects. All eligible subjects
were allocated to one of two groups: the IG or the CG.
2.2 | Subjects
Participants were recruited from August 2015 to July 2016 through
announcements in local and social media. Inclusion criteria were as
follows: female; aged between 18 and 40 years old; orofacial pain for
at least 3 months (considered as chronic pain, according to the IASP);
baseline pain score ≥3 on a ten-­point Numerical Pain Rating Scale
(NPRS); and diagnosis of orofacial myalgia (Ia and Ib) or mixed TMD
of Ia/Ib and groups IIa/IIb/IIIc (disc displacements) and IIIa (TMJ ar-
thralgia) according to the Research Diagnostic Criteria for TMD.18 In
addition, the participants self-­reported the presence and intensity
of neck pain according to a NPRS and completed the Portuguese
version of the Neck Disability Index19 at baseline to allow charac-
terisation of the sample. Patient examinations were conducted by a
physiotherapist (PT1) with 5 years of clinical experience in musculo-
skeletal disorders.
Potential participants were excluded if they met any of the fol-
lowing criteria: pregnancy; diagnosis of fibromyalgia or rheumatic
or neurologic issues; history of neck or jaw fracture; dental loss
(except for third molars, when extracted more than 6 months ago);
and previous orofacial treatment (such as orthodontics or physio-
therapy in the previous 6 months). Participants who had been using
occlusal splints or regular medication for more than 6 months were
CALIXTRE et al.
not excluded from the study. However, if they wanted to start any
new treatment during the study, they would be excluded. All ex-
cluded patients received appropriate counselling and physiotherapy
treatment.
The trial was approved by the relevant ethics committee prior
to data collection (CAE: 41837015.4.0000.5504). All participants
gave their written informed consent. The study was registered in
the Brazilian Register of Clinical Trials (ensaiosclinicos.gov.br; RBR-­
6c7rq4). The trial was reported according to CONSORT guidelines. 20
2.3 | Outcome measures
All outcomes were collected by a second physiotherapist (PT2), who
was blinded to the allocation, at baseline and at 5 weeks after the
baseline measurement in the case of the CG, and not more than
2 days after the final physiotherapy session in the case of the IG.
The primary outcome measure for this study was orofacial pain in-
tensity, which was also collected once a week during the study to
verify changes in current, maximum and minimum pain. The sec-
ondary outcomes measures were pain sensitivity, functionality and
headache impact described below.
2.3.1 | Orofacial pain intensity
The following outcomes were measured in centimetres using a 0-­10
Visual Analogue Scales (VAS): (a) current orofacial pain at the mo-
ment of the evaluation, (b) maximum orofacial pain in the last week
and (c) minimum orofacial pain in the last week. The reliability of VAS
measurements is considered fair to good (ICC: 0.55-­0.83). 21 In addi-
tion, 30% of pain reduction has been considered clinically meaning-
ful for individuals with chronic pain. 22
The primary outcomes were also collected once a week during
the 5-­week study period to verify changes in current, maximum and
minimum pain during the study period. The CG was reminded by the
PT1, once a week, to complete the pain scale at home. The IG was
asked by the PT to complete the VAS once a week before the treat-
ment session. The mean of the 3 scores was used to estimate orofa-
cial pain intensity for each week.
2.3.2 | PPT of masticatory muscles
Pressure pain thresholds were measured with a digital algometer
(ITO—Physiotherapy & Rehabilitation, OE-­220, Japan) with a 1-­
cm2 rubber tip. In order to determine the PPTs for each one of the
muscles of interest, the pressure was applied perpendicular to the
point with a 1 kg/s speed on the following spots: 1 cm superior and
2 cm anterior from the mandibular right and left angles (masseter
muscles), and 2 cm above the zygomatic arch in the middle part
between lateral edge of the eye and the anterior part of the helix
(anterior portion of right and left temporal muscles).15 Each spot
was tested three times in a random fashion, and the mean of the
three collected data points was used for data analysis. This proce-
dure has shown good construct validity4 and fair to good reliability
|
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on previous studies (ICC between 0.64 and 0.78). 23 Since there was
no difference between left and right muscles, the mean of right and
left masseters and the mean of right and left temporalis were used
on the statistical analysis. Minimum detectable change (MDC) for
general PPTs has been considered to range from 0.45 to 1.13 kg/
cm2. 24
2.3.3 | Headache Impact Test (HIT-­6)
HIT-­6™ is a brief tool for assessing the impact of headache in both
clinical research and practice. This tool is composed of six questions
that approach pain, functionality, social impact, energy and fatigue,
as well as cognition and emotional stress in people with headaches.
They can be answered with “never”—6 points, “rarely”—8 points,
“sometimes”—10 points, “very often”—11 points and “always”—13
points. The subject can score from 36 to 78 points while scores ≤49
represent little or no impact; scores between 50 and 55 represent
some impact; scores between 56 and 59 represent substantial im-
pact; and scores ≥60 indicate severe impact. 25 Subjects who scored
at least 50 points at baseline were re-­assessed on follow-­up in order
to verify changes in headache impact. The test-­retest reliability has
been demonstrated to be good (ICC: 0.76-­0.80). 26 The optimal cut-­
off point for the MCID is 8 points. 27 HIT-­6 has been translated and
validated for the population of the study. 28
2.3.4 | Mandibular function impairment
questionnaire
The mandibular function impairment questionnaire (MFIQ) was ap-
plied on both groups in order to verify possible functional alterations
and classify patients with TMD according to the severity of their
mandibular functional limitation. 29 This questionnaire is composed
of 17 questions, each one scoring between 0 and 4. The higher the
score, the greater the functional impairment on mandibular function.
The sum of the responses was used in the statistical analysis. The
Portuguese version used in this study has shown better reliability
when items 1, 2, 6 and 7 were not considered on the final score so
total score was 52 instead of 68.30 The smallest detectable differ-
ence (SDD) for this questionnaire for the total score of 68 has been
established to be 8 points.31
2.4 | Intervention
The description of the intervention followed the TIDieR checklist.32
The IG received 10 sessions of physiotherapy over 5 weeks,
twice a week with at least 48 hours apart.14,15 PT1 (the physiother-
apist who carried out the screening) was responsible for delivering
the treatment to the participants. The treatment was delivered
face-­to-­face and individually, on the health centre of the univer-
sity. All participants from IG received the same intervention, which
consisted of non-­manipulative manual techniques and neck motor
control/stabilisation exercises with biofeedback, as described in
Figure 1 and are as follows:
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4       CALIXTRE et al.
(a) (b)
(c)
(d)
2.4.1 | Suboccipital inhibition technique
The subject was supine, whereas the PT was seated behind the patient’s
head with the elbows resting on the surface of the table. The PT placed
both hands behind the subject’s head, with the palms facing upwards,
the fingers flexed, and the finger pads positioned on the posterior arch of
the atlas, to allow the occiput to rest in the palm of the hands (Figure 2A).
A force was applied with the finger pads over the atlas in the direction
of the ceiling with slight traction in a cranial direction for 2 minutes.33
2.4.2 | Passive anterior-­posterior upper cervical
mobilisation
The subject was supine with a neutral position of the cervical spine. The
PT held the occipital region of the patient with one hand to stabilise and
maintain the position of the upper cervical structures, while applying a
posteriorly directed force on the frontal region of the patient (anterior
to posterior force) with the other hand. The mobilisation was applied at
a slow rate of approximately 1 oscillation per 2 seconds controlled by
the PT who was trained previously. Mobilisation was applied in three
series of 2 minutes, with 30 seconds of rest in between, resulting in a
total of 7 minutes.34 The intensity of the technique was chosen by the
PT according to tissue resistance (Figure 2B).
F I G U R E   1   Physiotherapy techniques
applied during the treatment: A,
suboccipital inhibition technique; B,
passive anterior-­posterior upper cervical
mobilisation; C, sustained natural
apophyseal glide mobilisation with
rotation on C1-­C2 vertebras; D, Neck
stabilisation exercises with biofeedback
2.4.3 | Sustained natural apophyseal glide (SNAG)
mobilisation with rotation on C1-­C2 vertebras
First of all, the PT performed a flexion-­rotation test, which is a
well-­described and reliable procedure35 to identify limitations on
C1-­C2 segments of the spine. Then, the technique was applied on
the side of the higher impairment, or to both sides if they were both
impaired, according to Mulligan’s guideline. While the patient was
seated on a chair, a horizontal, anteriorly directed force was ap-
plied with the distal phalanx of the thumbs over the C1 transverse
process on the contralateral side of the limited rotation. While sus-
taining this glide, the patient actively rotated the head in the direc-
tion of the limitation, based on the flexion-­rotation test, as seen in
Figure 2C. This procedure was repeated 10 times to each side on
subsequent visits, ceasing when full range was acchieved. 36 Again,
the intensity of the technique was chosen by the PT according to
tissue resistance.
2.4.4 | Craniocervical flexor stabilisation exercise
Lying down in a supine position, the subject was instructed to
perform craniocervical flexion movements (Figure 2D). The head
was in contact with the supporting surface to facilitate activation
CALIXTRE et al. |
      5

F I G U R E   2   Flow chart of the study according to CONSORT Statement (Consolidated Standards of Reporting Trials). TMD,
temporomandibular disorders; PPT, pressure pain threshold; MFIQ, mandibular function impairment questionnaire; HIT-­6, headache impact
test; ITT, intention to treat; wk, weeks; n, number of participants

of deep neck flexors, with minimal activity of the superficial neck
flexor muscles. This contraction was monitored using a pres-
sure sensor (Stabilizer; Chattanooga Group, Inc., Chattanooga,
TN) while the PT monitored any contraction of superficial neck
flexor muscles with palpation of the anterior neck region to ensure
that the exercise was being correctly performed. Initially, each
craniocervical flexion produced a pressure ranging from 20 to
22 mm Hg. The subjects were instructed to maintain that pressure
using visual feedback for 10 seconds with no contraction of super-
ficial neck flexor muscles. This procedure was repeated 10 times
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6       CALIXTRE et al.

TA B L E   1   Baseline demographic and diagnostic characteristics of maximum pain, with a standard deviation of 1.5 and 2.1, respec-
each group tively). With these estimates, an analysis of variance (ANOVA)

Control group Intervention test was applied (α = 0.05; β = 80%), and the sample size calcula-
  (n = 31) group (n = 30) P-­value tion indicated that 52 participants were needed in total. Taking
into account a likely dropout rate of 15%, 61 participants were
Age (y) 26.3 (4.6) 26.1 (5.7) 0.269
targeted.
BMI (kg/cm2) 23.1 (3.7) 22.8 (3.2) 0.208
Visual inspection of histograms and Kolmogorov-­Smirnov normal-
Years of pain 5 (1.5-­10) 4 (2-­9.3) 0.805
(y)* ity tests were used to assess continuous data distribution. The primary
and secondary outcomes were considered to be normally distributed
Orofacial pain 7 (5.5-­7 ) 7 (6-­8) 0.625
(NPRS, 0-­10)* (P > 0.05) and were described in terms of their means and standard

Neck pain 7 (2-­8) 6 (2-­7.8) 0.457 deviations. The diagnostic and demographic characteristics of the two
(NPRS, 0-­10)* groups were compared using a two-­sample t test, the Mann-­Whitney
NDI (score 8 (6.5-­13) 9.5 (6.3-­12) 0.960 U test or the chi-­square test, according to their distribution.
0-­50)* For both primary and secondary outcomes, a mixed ANOVA with
Maximum 33.1 (9.2) 36.3 (8.8) 0.555 repeated measures was conducted, with time (baseline and follow-­up)
mouth as the within-­subject factor and group (IG and CG) as the between-­
opening (mm)
subject factor. The group-­by-­time interaction indicates whether there
Headache (n 29 (93.5%) 29 (96.7%) 1.00 were differences in outcomes between the groups over time, thus
and %)
addressing the aims of the study. In case of a significant interaction,
Splint therapy 9 (29%) 12 (40%) 0.371
Tukey’s post hoc test was used to verify whether a difference was
(n and %)
present between the groups and/or within groups. Orofacial pain
RDC/TMD
scores collected once a week were analyzed using a repeated mea-
Bilateral pain 16 (51.6%) 17 (56.7%) 0.695
sures ANOVA with time (six evaluations) as the within-­subject factor
(n and %)
and group (CG and IG) as the between-­subject factor. The same inter-
Unilateral 15 (48.4%) 13 (43.4%) 0.616
pain (n and action effect was verified, and post hoc tests were carried out.
%) Both available-­case and intention-­to-­treat analyses were per-
Orofacial 31 (100%) 30 (100%) 1.00 formed. Available-­case analysis included all participants up to the
myalgia (n point when they dropped out of the study; intention-­to-­treat anal-
and %) yses imputed missing data on the continuous measures using the
Arthralgia (n 10 (32.3%) 11 (36.7%) 0.719 expectation maximisation method. This method computes missing
and %)
values based on maximum-­likelihood estimates by using observed
n, number of subjects; %, percentage of the total sample of the group; y, data in an interactive process.37 The total percentage of imputed
years; BMI, body mass index; NPRS, Numeric Pain Rating Scale; NDI, data was 10% for the IG and 6.5% for the CG. All participants who
neck disability index; RDC/TMD, research diagnostic criteria for tempo-
were randomised were included in the statistical analyses, and
romandibular disorders.
Parametric outcomes are described as mean (standard deviation), and available-­case and intention-­to-­treat methods of analysis yielded the
non-­parametric outcomes (*) are described as median (25%-­75% same results. Only the results of the intention-­to-­treat analysis were
quartiles). therefore reported.
Cohen’s d index was calculated to determine the between-­
in each session. Load increase was used to progress the exercise. group and within-­group effect sizes (ESs) for all outcomes. An ES
The number of repetitions and duration of each contraction were greater than 0.8 was considered large, 0.5 moderate and less than
constant across the sessions.14 0.2 small.
The CG received neither intervention nor counselling for
5 weeks. For ethical reasons, patients in the CG group were of-
fered physiotherapy treatment and counselling after the follow-­up 3 | R E S U LT S
evaluation.
Sixty-­one women were included in the study. Their demographic and
diagnostic characteristics are described in Table 1. No differences
2.5 | Data processing and statistical analysis
between groups were identified at baseline in any of the variables
Sample size was determined using ENE 3.0 software (P > 0.05). Figure 2 shows the flow chart of the study. Five partici-
(GlaxoSmithKline, Madrid, Spain). The sample size calculations pants did not complete the study: two (one from the CG and one
were based on the minimum clinically important difference from the IG) dropped out for personal reasons, and three (one from
(MCID) of 30% from the baseline orofacial pain intensity VAS val- the CG and two from the IG) were excluded during the study be-
ues22 obtained from a pilot study (4.0 for current pain and 6.0 for cause they had started to take psychoactive drugs.
CALIXTRE et al.       7 |
TA B L E   2   Baseline and follow-­up outcomes for control and intervention groups

Post hoc Post hoc

Baseline Follow-­up within-­group Within-­group between-­group Between-­group

Outcomes Groups n Mean (SD) Mean (SD) MD (95% CI) ES (95% CI) MD (95% CI) ES (95% CI)

Primary
Curr. painb CG 31 3.1 (2.7) 3.1 (2.3) 0.0 (−1.3; 1.2) −0.02 (−0.5; 0.5) −1.9 (−3.1; −0.7)a −0.81 (−1.3; 0.3)
IG 30 4.0 (2.6) 2.1 (2.2) 1.9 (0.6; 3.1)** 0.76 (0.2; 1.3)
Max. painb CG 31 6.2 (1.7) 5.8 (2.2) 0.3 (−0.8; 1.5) 0.14 (−0.3; 0.6) −1.7 (−2.8; −0.5)a −0.75 (−1.3; −0.2)
IG 30 6.1 (2.1) 4.0 (2.4) 2.0 (1.0; 3.0)*** 1.02 (0.5; 1.6)
Min. painb CG 31 1.5 (1.5) 1.6 (1.6) −0.1 (−0.9; 0.7) −0.07 (−0.6; 0.4) −1.0 (−1.8; −0.1)a −0.58 (−1.1; −0.1)
IG 30 1.9 (1.7) 1.1 (1.4) 0.9 (0.0; 1.7)* 0.53 (0.0; −1.0)
Secondary
PPT temp CG 31 1.2 (0.4) 1.3 (0.5) −0.1 (−0.4; 0.1) −0.30 (−0.8; 0.2) 0.0 (−0.1; 0.2) 0.15 (−0.3; 0.6)
IG 30 1.3 (0.7) 1.4 (0.5) −0.1 (−0.4; 0.2) −0.16 (0.7; 1.3)
PPT mass CG 31 1.1 (0.4) 1.1 (0.5) −0.1 (−0.3; 0.2) −0.14 (−0.6; 0.4) −0.1 (−0.2; 0.1) −0.25 (−0.7; 0.3)
IG 30 1.1 (0.6) 1.2 (0.5) −0.1 (−0.4; 0.2) −0.23 (−0.7; 0.3)
HIT-­6b CG 29 62.5 (6.1) 60.0 (6.6) 2.5 (−0.9; 5.8) 0.38 (−0.1; 0.9) 6.8 (2.7; 10.5)*** 0.86 (0.3; 1.4)
IG 29 61.4 (6.0) 52.1 (8.5) 9.3 (4.4; 14.1)*** 1.23 (0.5; 1.9)
MFIQb CG 31 21.9 (8.7) 22 (8.9) −0.1 (−4.6; 4.4) −0.01 (−0.5; 0.5) 3.8 (0.7; 6.9)** 0.62 (0.1; 1.1)
IG 30 18.7 (9.7) 15 (10) 3.7 (−1.4; 8.8)** 0.37 (−0.1; 0.9)

n, number of subjects; MD, mean difference; ES, effect size; Curr, current; Max, maximum; Min, minimum; PPT, pressure pain threshold; Temp, tempo-
ralis; Mass, masseters; HIT-­6, headache impact test; MFIQ, mandibular function impairment questionnaire; CG, control group; IG, intervention group;
SD, standard deviation; CI, confidence interval.
Post hoc means differences and 95% CI of within-­group and between-­group comparisons and effect sizes and their 95% CI of within-­group and
between-­group analyses are shown. The primary outcome was collected in centimetres (0-­10 cm), while PPTs of masticatory muscles were collected in
kg/cm2 and each questionnaire on their scale.
a
Statistically significant difference for post hoc analysis (P < 0.05); **<P < 0.01;***P < 0.001.
b
ANOVA group-­by-­time interaction (P < 0.05).

Adverse events: None of the participants in this trial reported any
adverse events.
Compliance with treatment: Participants were treated in the clinic,
and all treatments were provided onsite. Participants were not
obliged to practice at home. Attendance at sessions was therefore
taken as compliance with the treatment protocol.
Co-interventions: There were no co-­interventions in either group.
Primary and secondary outcomes at baseline and at the 5-­week
follow-­up for both IG and CG groups are shown in Table 2, together
with mean differences and ES.
3.1 | Primary outcomes
Current pain showed a significant group-­by-­time interaction
(P < 0.01, F = 10.25, df = 1). The post hoc analysis showed signifi-
cant within-­group effect for IG but not for the CG. Also, there was a
significant difference between the groups at the 5-­week follow-­up.
The within-­group ES for the IG and the between-­group ES were
large (≥0.80), favouring the intervention. The ES of the CG was null.
Maximum pain showed a significant group-­by-­time interaction
(P < 0.01, F = 8.72, df = 1). On the within-­group post hoc analysis,
the IG showed a significant improvement, whereas the CG showed
no difference. There was also a significant between-­group differ-
ence at the 5-­week follow-­up: the within-­group ES was large for the
IG and small for the CG. The between-­group ES was moderate, as
the IG experienced less pain than the CG.
Minimum pain showed significant group-­by-­time interaction
(P = 0.03, F = 5.25, df = 1). The post hoc analysis showed significant
within-­group difference for the IG, but not for the CG. There was a
significant between-­group difference at the 5-­week follow-­up. The
within-­group ES for the IG and the between-­group ES were both mod-
erate (>0.50), thus favouring the intervention. The ES of the CG was
null.
The weekly average scores of the three pain intensity measures
are presented in Figure 3. A significant interaction between time
and group was found (P < 0.01, F = 5.29, df = 5). The within-­group
post hoc analysis showed that the mean pain intensity scores
from the IG obtained in week 4 (P < 0.01) and week 5 (P < 0.01)
differed from baseline (P < 0.01). For the CG, no differences from
baseline were found. The post hoc analysis demonstrated that the
between-­group difference was significant from the fourth week of
the protocol.
 |
8       CALIXTRE et al.
3.2 | Secondary outcomes
3.2.1 | PPT
The PPT of the masticatory muscles showed little variation either
between groups or over time. Consequently, no significant group-­
by-­time interaction was found (P = 0.58, F = 0.31, df = 1 for tem-
poralis; P = 0.34, F = 0.93, df = 1 for masseters) nor were there any
main effects of time and between groups. ES was also irrelevant.
3.2.2 | HIT-­6
Twenty-­nine participants from each group scored more than 50
points on HIT-­6 at baseline, 25 and headache impact for those par-
ticipants was therefore analyzed. There was a significant group-­by-­
time interaction on headache impact according to HIT-­6 (P = 0.02,
F = 11.14, df = 1). Post hoc analysis showed significant within-­group
difference for the IG (9.3). The CG had a difference of 2.5, which
was not statistically significant (P = 0.09). Significant between-­group
differences were found at follow-­up. The within-­group ES for the
IG and the between-­group ES were large (>0.85), which favours the
intervention. The ES for the CG was small.
3.2.3 | Mandibular function
There was a significant group-­by-­time interaction for mandibular
function (P = 0.02, F = 5.96, df = 1), with a significant between-­
group difference at follow-­up in the post hoc analysis. The IG
F I G U R E   3   Average score between maximum, minimum and
current pain (VAS) scores collected once a week from intervention
(black line) and control (grey line) groups. * indicates statistically
significant differences between the groups, and # indicates
significant difference between baseline and the other evaluations
on the intervention group
showed a significant within-­group difference, while the CG showed
no significant difference from baseline to follow-­up (P = 0.93). The
within-­group ES for the CG was small; the ES for the IG and the
between-­group ES were moderate.
4 | D I S CU S S I O N
A treatment regimen of manual therapy applied to the upper cer-
vical spine and neck motor control/stabilisation exercises over a
5-­week period was found to decrease orofacial pain and headache
impact in women with TMD. Significant improvement in orofacial
pain intensity was found from the fourth week of the intervention.
The changes obtained on PPT of the masticatory muscles were not
significant. Although there was an improvement in mandibular func-
tion, the differences were below the minimum detectable change
(MDC). The hypothesis of the study was therefore partially con-
firmed. No adverse effects were reported, and no dropouts were
due to the intervention. To our knowledge, this is the first study to
analyze the effects of a combination of manual therapy and motor
control/stabilisation exercises in participants with TMD in a single-­
blind randomised controlled trial.
4.1 | Orofacial pain
The clinically relevant cut-­off for changes in pain scores in par-
ticipants with chronic pain was set at 30%. 22 The percentage of
participants in the IG who reported more than 30% of orofacial
pain relief was greater than that in the CG for current pain (53%
for the IG; 32% for the CG) and for maximum pain (60% in the
IG; 16% in the CG). The IG showed a tendency to reduced pain
from the first week, and this was statistically significant after the
four and 5 weeks of treatment, which indicates that the treatment
was already successful at the fourth week. The CG, in contrast,
experienced progressively increasing orofacial pain from baseline
to the fourth week; the pattern changed at the 5-­week follow-­up,
becoming a statistically non-­significant tendency to decreasing
orofacial pain by the end of the study. This pattern arguably repre-
sents the natural fluctuation of TMD symptoms over time, owing
to psychosocial, hormonal and other factors. 38 The follow-­up pe-
riod was not long enough to establish whether the pain scores
would have decreased further, stabilised or even returned to their
original level.
Previous studies have reported a reduction in orofacial pain fol-
lowing application of manual therapy techniques to the upper cer-
vical spine and stabilisation exercises for the neck.14,15 One study36
applied the same SNAG mobilisation as the present study, combined
with thoracic manipulation, dry needling of myofascial trigger points
and local mobilisations on the TMJ. Significant and clinically import-
ant improvements were reported in terms of orofacial pain inten-
sity, mandibular range of movement and disability, both immediately
and at the 2-­month follow-­up. Although the studies used dissimilar
methods and comparison is therefore difficult, the evidence for the
CALIXTRE et al.
effect of neck treatment on TMD complaints is growing,10 and the
present study is in line with that.
The regional interdependency between the jaw and the upper
cervical spine is not fully understood. It has been suggested, how-
ever, that stimulation of the inhibitory downward path through the
39
cervical spine may reduce pain in the trigeminal area, although
other mechanisms, such as neurobiomechanical connections be-
tween the cervical spine and the TMJ,34,40,41 and general predispos-
42
ing to musculoskeletal diseases might be behind these effects.
The literature has shown that subjects with TMD have poor per-
formance when carrying out the craniocervical flexion test (CCFT),
presenting increased electromyographic activity of the superficial
cervical flexor muscles.43 These results highlight the fact that alter-
ations of the endurance capacity of the neck flexor muscles could be
implicated in the neck-­shoulder disturbances observed in patients
with TMD and thus this deficit of activation (inhibition or delay) of
the deep neck flexor muscles could be addressed with stabilisation
43
exercises, as performed in the present study.
4.2 | Sensitivity of the masticatory muscles
In the present study, PPTs of the masticatory muscles were not
altered after treatment which is in agreement with the reports of
previous studies that found small33,34 or nonexistent44 effects when
PPTs were assessed immediately after intervention. When com-
45
pared to data obtained from healthy subjects, the temporalis and
masseter muscles of our sample showed low PPTs at baseline and at
follow-­up. Low PPTs in TMD patients have been partly attributed
to neurological complex processes in these patients, such as cen-
41
tral sensitisation. Although the presence of central sensitisation
cannot be verified in the present sample, it can be suggested that
peripheral pain sensitivity on the orofacial region did not change im-
mediately after an intervention protocol consisting of mobilisation of
the upper cervical region and craniocervical flexor training in women
with TMD. Future studies aiming to modulate sensitivity alterations
in this population should use longer follow-­ups.
Furthermore, a recent study46 showed that cervical and oro-
facial treatment was more effective than cervical treatment alone
to increase PPTs in the trigeminal area of patients with TMD and
migraine. Thus, treating solely the neck, as we did on the present
study, is probably not enough to enhance sensibility of the masti-
catory muscles, but associating techniques on the stomatognathic
system and on the neck would be more effective.
4.3 | Headache impact
Women from the IG showed a reduction in HIT-­6 score greater
than the MCID of eight points. 27 In accordance with these results,
previous studies have shown that isolated upper cervical manual
47
techniques, including SNAG mobilisation and suboccipital muscle
inhibition,48 caused significant reduction in headache severity com-
pared to a placebo group when applied to subjects with cervicogenic
and tension-­t ype headaches. The application of manual therapy
|
      9
techniques to the cervical spine in combination with exercise has
been shown to be effective in reducing pain in patients with tension-­
type headaches,49 with cervicogenic headache,50 with migraine,46
but, to the best of our knowledge, remains unknown for secondary
headache attributed to TMD.
The common neurophysiological alterations associated with
chronic orofacial pain and primary headaches, together with the
interdependency of the craniocervical-­mandibular regions, 51 may
explain the comorbidity of the two conditions52 and the success of
the intervention in the present study in decreasing headache impact.
4.4 | Mandibular functionality
The mandibular function was statistically different between the
groups, but it was not higher than the MDC.31 A small number of
studies14,53 have applied physiotherapy interventions and evaluated
mandibular function with questionnaires. Although they found simi-
lar results, further studies are required to strengthen the evidence.
Improvement in mandibular function is to be expected as a con-
sequence of decrease in pain. However, the present sample consisted
of young women who did not necessarily present with significant lim-
itations in mouth opening or severe dysfunction at baseline. Their low
impairment may have contributed to the ceiling effect at the 5-­week
follow-­up, thus making it unlikely that differences would exceed the
MDC. The therapy applied in the current study might have different ef-
fects on subjects with more severe functional limitations. Nevertheless,
patients with similar characteristics to our sample in terms of age and
severity of dysfunction are common in clinical practice, and it there-
fore remains appropriate to include them in clinical trials.
4.5 | Limitations of the study
Our participants were recruited using advertisements. This can be
considered as a source of selection bias that could hamper the exter-
nal validity of the study, because the participants were not patients
from a specialised health service. Performance bias may also be an
issue, as participants were not blinded to the intervention, and the
influence of a placebo effect was not assessed. Also, PT1 gave more
attention to IG than to CG during the 5 weeks of protocol. This may
increase therapeutic alliance and expectations of the therapy on IG.
This study presents a short-­term analysis that verified effects
on primary and secondary outcomes, immediately after 5 weeks of
the selected therapy. However, there was no follow-­up assessment
after the intervention period. Thus, a long-­term analysis would be
necessary to yield information about the therapy’s ongoing effects.
Furthermore, since our sample size calculation was based on the pri-
mary outcome, the analyses of the secondary outcomes, perhaps,
could not reach statistically significant results due to a type II error.
A standard manual therapy protocol was applied without tak-
ing into account the needs of individual participants, in order to
guarantee that each participant was subject to the same treatment
techniques. However, the treatment in this study is not comparable
to treatments available in general clinical practice, where manual
 |
10       CALIXTRE et al.
therapy techniques are applied according to individual needs and
on the basis of continuous evaluation. In this study, the intervention
was applied by one experienced physiotherapist at a particular uni-
versity clinic, and this may hamper the external validity of the study.
Finally, in terms of the scope of the study, headache type was not
captured or explored in the present analysis. Also, our sample con-
sisted of younger females, and our results might not be generalisable
to men or to older females.
Given these limitations, further investigation is needed, including
placebo/simulation groups, longer follow-­ups, samples from other age
and gender groups, and the inclusion of patients suffering from differ-
ent types of headache and with greater degrees of TMD functional
impairment. Studies applying the same techniques in combination
with a more personalised treatment strategy would also be of value.
5 |  CO N C LU S I O N
Manual therapy and stabilisation exercises targeted to the neck
showed to decrease orofacial pain and headache impact in women
with TMD when compared with a CG after 5 weeks of intervention.
No significant effects of the treatment protocol on mandibular func-
tion or PPT of the masticatory muscles were found. These results
provide preliminary and promising evidence of the use of neck ther-
apy in patients with TMD.
AC K N OW L E D G M E N T S
The trial was approved by the relevant ethics committee prior to
data collection (CAE: 41837015.4.0000.5504). It was supported by
the São Paulo Research Foundation (Grant #2014/05276-­7).
C O N FL I C T O F I N T E R E S T
No conflict of interest to be declared.
ORCID
Letícia B. Calixtre  http://orcid.org/0000-0003-3384-9839
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How to cite this article: Calixtre LB, Oliveira AB, de Sena Rosa LR,
Armijo-Olivo S, Visscher CM, Alburquerque-Sendín F.
Effectiveness of mobilisation of the upper cervical region and
craniocervical flexor training on orofacial pain, mandibular
function and headache in women with TMD. A randomised,
controlled trial. J Oral Rehabil. 2018;00:1–11. https://doi.
org/10.1111/joor.12733