life
Article
Botox Therapy for Hypertrophy of the Masseter Muscle Causes
a Compensatory Increase of Stiffness of Other Muscles of
Masticatory Apparatus
4,
Dorota Mierzwa 1,† , Cyprian Olchowy 1, *,† , Anna Olchowy 2 , Izabela Nawrot-Hadzik 3 , Paweł Dabrowski
˛
5
1
1
1
Sławomir Chobotow , Kinga Grzech-Leśniak
, Paweł Kubasiewicz-Ross and Marzena Dominiak
1
2
3
4
5
Citation: Mierzwa, D.; Olchowy, C.;
*
†
Department of Oral Surgery, Wroclaw Medical University, 50-425 Wroclaw, Poland;
dorota.mierzwa@umw.edu.pl (D.M.); kinga.grzech-lesniak@umw.edu.pl (K.G.-L.);
pawel.kubasiewicz-ross@umw.edu.pl (P.K.-R.); marzena.dominiak@umw.edu.pl (M.D.)
Department of Experimental Dentistry, Wroclaw Medical University, 50-425 Wroclaw, Poland;
ania.olchowy@gmail.com
Department of Pharmaceutical Biology and Botany, Wroclaw Medical University, 50-556 Wroclaw, Poland;
izabela.nawrot-hadzik@umw.edu.pl
Division of Normal Anatomy, Department of Human Morphology and Embryology,
Wroclaw Medical University, 50-368 Wroclaw, Poland; pawel.dabrowski@umw.edu.pl
Department of General Radiology, Provincial Specialist Hospital in Legnica, 59-220 Legnica, Poland;
slavek1@gmail.com
Correspondence: cyprian.olchowy@gmail.com
These authors contributed equally to this work.
Olchowy, A.; Nawrot-Hadzik, I.;
Dabrowski,
˛
P.; Chobotow, S.;
Grzech-Leśniak, K.;
Kubasiewicz-Ross, P.; Dominiak, M.
Botox Therapy for Hypertrophy of
the Masseter Muscle Causes a
Compensatory Increase of Stiffness of
Other Muscles of Masticatory
Apparatus. Life 2022, 12, 840.
https://doi.org/10.3390/
life12060840
Academic Editors: Nicola Smania,
Po-Hsiang Tsui, Yung-Liang Wan
and Bao-Yu Hsieh
Abstract: Little is known about the nature of masseter muscle hypertrophy. We investigated the
masseter muscle stiffness change after a single intra-masseteric session of Botox injections in people
with benign bilateral masseter hypertrophy and the effect of the treatment on the stiffness of the
temporalis muscle. Stiffness of the muscles was measured with shear-wave elastography at baseline
and 3 weeks after Botox injections in 22 otherwise healthy people. Before the treatment, the stiffness
of the masseter was lower than of the temporalis muscle (10.18 ± 1.67 kPa vs. 11.59 ± 1.54 kPa;
p = 0.002). After the treatment, this difference increased (6.38 ± 1.34 vs. 13.10 ± 1.92; p < 0.0001).
The drop in the stiffness of the masseter muscle was symmetrical (left side by 3.78 kPa; right side by
3.83 kPa). No differences between the left and right sides of the face in terms of muscle stiffness were
observed. The study shows that Botox injections reduce stiffness of the masticatory muscles which,
in turn, increases the stiffness of the temporalis muscles. Due to the knock-on effect of the change in
the masseter function on the other masticatory muscles, simultaneous evaluation and treatment of
the temporalis muscle may be required to ensure the desired functional and cosmetic effect.
Received: 11 February 2022
Accepted: 30 May 2022
Published: 6 June 2022
Keywords: masseter muscle; temporalis muscle; shear-wave elastography; stiffness; muscle hypertrophy
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1. Introduction
Little is known about the nature and characteristics of masseter muscle hypertrophy.
It can affect one side or both sides of the face and is characterized by an increase in the
volume of the muscle tissue, resulting in the change in the contour of the face. In the
literature, masseter muscle hypertrophy is often described as a concomitant condition to
the hypertrophy of other masticatory muscles, as this condition affects masseteric and
temporalis muscles [1] or even medial pterygoid hypertrophy [2]. Patients with unilateral masseter muscle hypertrophy are often consulted by an esthetic surgeon due to face
asymmetry [3,4]. Bilateral enlargement of the masseter muscles is more common, but
constitutes a smaller esthetic problem maintaining the symmetry of the face [1]; however, it
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Life 2022, 12, 840. https://doi.org/10.3390/life12060840
https://www.mdpi.com/journal/life
Life 2022, 12, 840
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is more often associated with other symptoms, such as bruxism [2,5], temporomandibular disorders, malocclusion, pain, otalgia, nighttime trismus [6], emotional stress [1,3,6],
and oral parafunctions, including unilateral chewing and excessive chewing gum [2,7].
Furthermore, together with the increased muscle mass, changes in the adjacent bone tissue
may occur, such as a thickened cortex of the angle and ramus of the mandible, temporal
fossa, and zygomatic arch with a corresponding decrease in marrow area or prominent
exostoses at the angle of the mandible, visible in the CT scans [3,5].
Idiopathic etiology is common among patients with masseter muscle hypertrophy [6].
Some researchers divide this condition into congenital and acquired [8], while others consider all cases congenital with a variable presentation [9]. Unilateral enlargement of the
masseter muscles is less frequently prevalent and maybe associated with other pathologies [10,11]. Although the exact etiology of acquired masseter muscle hypertrophy is not
known, there are several factors associated with its development, such as bruxism, oral
parafunctions, or malocclusions [2,5,7], but it is not clear whether they are causative or
resultant factors. As shown in previous research, intensive chewing gum can increase
the stiffness of the masseter muscle [12] and lead to bilateral masseter hypertrophy [7].
Most patients report slow but progressive nature of the condition [2,3,5,13]. The muscle
tone pathophysiology in patients with masseter muscle hypertrophy has not been investigated. However, sensory biofeedback may play a role in its development. Due to the lack
thereof, the patient may have difficulties with optimizing movements with a subsequent
increase in muscle contraction around the joints [14].
Epidemiology data on masseter muscle hypertrophy are limited. Rispoli et al. mention
a review of 108 cases which found that affected patients were 30 years old on average, 57%
were males, 60% had bilateral pathology, and only 5% had concurrent temporalis muscle
hypertrophy [6]. Masseter muscle hypertrophy is rare in children [15]. The incidence of
masseter muscle hypertrophy is considered higher in Asians who are, at the same time,
more sensitive about their lower face contouring [4].
Patients usually seek medical advice because of dissatisfaction with their appearance;
however, some of them experience problems caused by hypertrophy that include chronic
pain of the frontal and temporal area of the head [1,7]. Treatment includes surgery and
botulinum toxin type A (Botox) injections [16,17]. Botox injections are common and may
have some advantages over surgical treatment. Despite effectiveness of Botox injections in
people with bilateral masseter hypertrophy being well documented, none of the studies
uses objective methods to document and monitor treatment effects, such as shear wave
elastography (SWE).
Measurement of stiffness of masticatory muscles using SWE is gaining attention in
dentistry [18]. Elastography is a type of imaging technique utilizing a probe that generates mechanical vibration resulting in propagation of low-frequency shear waves inside
tissues, creating two intense plane shear waves [19]. These shear waves distort soft tissues
to a degree corresponding to their stiffness. Next, they are detected and registered by
an ultrafast scanner. The stiffness of the tissues can be mapped quantitatively from this
propagation image by inversion algorithms; thus, this technique allows determining the
actual elastic modulus of soft tissues in the set region of interest (ROI). SWE can quantitatively record tissue stiffness in kPa. To date, normal values of the stiffness of the masseter
muscle have already been established [20,21]. This study further investigates stiffness of
the masseter muscle in pathological conditions. In the present study, we investigated a
degree of a reduction in the masseter muscle stiffness after a single intra-masseteric session
of Botox injections in people with benign bilateral masseter hypertrophy. Furthermore, we
intended to investigate whether a drop of the masseter stiffness would be bilaterally
equal. Symmetry of the injection grid should be crucial to ensure satisfactory aesthetic outcomes [22]; however, in daily practice, injecting the medication into five mirror sites of both
masseters and equally dividing the dose into those five injections still poses a challenge.
Another interesting issue is the potential influence of iatrogenic reduction in the masseter
muscle stiffness on other muscles of the masticatory apparatus; however, hypertrophy of
Life 2022, 12, 840
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the temporalis muscles is considered an esthetic problem, particularly when hypertrophy is
only unilateral [2,23,24]. The pterygoid muscles are not easily accessible for the ultrasound
and elastography examination, therefore, we focused on the temporalis muscles.
2. Materials and Methods
2.1. Participants
We enrolled adults (individuals over 18 years of age) with idiopathic bilateral masseter
muscle hypertrophy. All participants gave their informed consent for participation in the
study. Patients treated previously with Botox injections for masseter muscle hypertrophy
were not considered. This longitudinal single-arm study was conducted according to the
Declaration of Helsinki and was approved by the Bioethical Committee at Wroclaw Medical
University (KB—633/2020).
Exclusion criteria were as follows: concomitant pathological conditions affecting
masseter muscles such as temporomandibular disorders (evaluated based on the Diagnostic
Criteria for Temporomandibular Disorders protocol [25]), neuromuscular disorders and
inflammatory diseases of this region, prior surgery for masseter muscle hypertrophy,
the presence of malignant or benign lesions of this area, pain within masseter muscles,
parafunctional oral habits reported by the patients, systemic diseases treated with drugs
affecting muscle functioning as well as breastfeeding and pregnancy.
2.2. Study Procedure
Before SWE measurement, an ultrasound examination of both masseter muscles was
performed to exclude any local occult pathologies, such as parotid enlargement. The study
protocol was based on the experience of the Kim’s team [26], who reported the use of Botox
in a large group of patients with masseter muscle hypertrophy. Immediately after SWE, a
Botox injection was administered. The next SWE was performed after 3 weeks. We also
validated the measurements against the values obtained from an elasticity QA Phantom
model 049A (Computerized Imaging Reference Systems, Inc, Norfolk, VA, USA). The study
design is schematically shown in Figure 1.
Figure 1. Study procedure.
2.3. Botox Treatment
For the Botox treatment, BOTOX® Cosmetic (onabotulinumtoxinA, Allergan USA Inc.,
Madison, NJ, USA) was used. Each patient received three or four injections (20–25 Ul in
total) into each masseter muscle depending on the degree of his/her muscle hypertrophy.
Injections were made manually and based on the operator experience. Injections were
planned to be symmetrical on both sides of the face due to the fact that all participants
suffered from bilateral masseter muscle hypertrophy.
Botox injections were conducted with caution and with consideration of anatomical
structures of the masseter muscle. Patients who received four injections were injected
according to the Kim et al. method [26]. Patients who received three injections were
injected according to the modified method developed in our institution. The principles of
the methods are as follows: the effect of Botox is 1 cm; the puncture area is marked by three
intersecting lines creating a safe area 15–20 mm above the edge of the mandible; and the
drug is divided into three parts in a 2:1:1 ratio, with the highest dose at the highest point.
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2.4. Shear Wave Elastography
Qualified participants were referred for the SWE examination. The methodology of
SWE was described elsewhere [27]. Briefly, the probe was placed parallel to the longitudinal
axis of the masseter muscle in the middle part of the muscle in the belly. The middle of
the masseter muscle was identified as the widest part of the muscle during clenching
as the most protruding fragment of the masseter muscle. On the temporalis muscle, the
probe was placed on the muscle just above the zygomatic arch and parallel to the fibers of
the temporalis muscle. Our previous experience shows that such placement of the probe
allows for easy identification of the target area and for obtaining accurate and repeatable
measurements (Figure 2). An ROI of 4-mm was used. Participants were asked to lie in a
relaxed, supine position and refrain from swallowing.
Figure 2. Placement of the probe on the masseter muscle during shear wave elastography examination
(reproduced from Olchowy et al. [20]).
The SWE measurements of the masseter muscle were taken three times; an averaged
result was analyzed. We used the Aixplorer Ultimate device (SuperSonic Imagine, Aix-enProvence, France) using a high-frequency linear probe SL 18-5 (5–18 MHz). Shear waves
propagate in the tissues with a speed of 1 m/s–10 m/s which corresponds to elasticity of
1–300 kPa. We validated the measurements with the elasticity QA Phantom model 049A
(Computerized Imaging Reference Systems, Inc., Nor-folk, VA, USA). All examinations
were performed by a radiologist with eight years of experience in shear wave elastography,
including experience in masticatory muscles evaluation.
2.5. Statistical Analysis
Statistical analysis was carried out with MedCalc v. 19.5.3 (MedCalc Software Ltd.,
Ostend, Belgium). The Shapiro–Wilk test was used to check for the normality of the data.
Means with standard deviations were calculated. Normality was checked and was rejected
for all variables. The Mann–Whitney U was used to compare independent samples and the
Wilcoxon test was used for repeated measures. A probability value lower than 0.05 was
considered statistically significant.
3. Results
The study included 23 people with an average age of 49 ± 8 years (15 women and
8 men). One woman was excluded because she developed an inflammatory condition of
the molar with a denticle.
The comparison between the overall muscle stiffness before and after Botox injections
is shown in Figure 3. Before the treatment, the overall stiffness of the masseter muscle was
significantly lower than the overall stiffness of the temporalis muscle (10.18 ± 1.67 kPa vs.
11.59 ± 1.54 kPa; p = 0.002). The difference in stiffness between the muscles was greater
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after the treatment with Botox (6.38 ± 1.34 vs. 13.10 ± 1.92; p < 0.0001). The interaction
effect (difference of differences) for the masseter muscle was 3.80 kPa and for the temporalis
− 1.55 kPa (p < 0.001). Furthermore, the drop in the stiffness of the masseter muscle
muscle −
was similar (symmetrical) on both sides. It was 3.78 kPa for the left side and 3.83 kPa for
the right side. No differences between the left and right sides of the face in terms of muscle
stiffness were observed. Detailed comparisons are shown in Table 1.
Figure 3. Comparison of the stiffness before and after the treatment with Botox.
Table 1. Elasticity values before and after massage (data are shown in kPa).
N = 23
Before Botox
After Botox
p-Value
Masseter muscle
Left masseter
10.16 ± 1.74
6.38 ± 1.36
<0.0001
Right masseter
10.20 ± 1.65
6.37 ± 1.34
<0.0001
p-value
0.6302
1.000
Temporalis muscle
Left temporalis
11.57 ± 1.55
13.12 ± 1.96
0.0002
Right temporalis
11.62 ± 1.57
13.09 ± 1.92
0.0013
p-value
0.9813
0.9813
4. Discussion
Our study showed a significant drop in the stiffness of the masseter muscle after
3 weeks following Botox injection with a parallel increase in the stiffness of the temporalis
muscle. Patients were satisfied with the physical appearance of the lower contour of the
face as a result of the reduction of muscle volume; however, we did not use any cosmetic
scale to make a quantitative measure. All patients included in the study suffered from
bilateral masseter muscle hypertrophy. This is well reflected in the stiffness results as the
obtained results are symmetrical with an almost equal drop in stiffness on both sides (by
3.78 kPa for the left masseter and by 3.83 kPa for the right masseter). Regarding the masseter
muscle, the overall stiffness of the hypertrophic masseter muscle was 10.18 ± 1.67 kPa in
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comparison to our previously conducted studies on healthy adults where the stiffness of
the masseter muscle ranged from 10.54 kPa to 11.46 kPa [12,18,27].
Botox injections into masseter muscle tissue for masseter muscle hypertrophy have
been used since 1994, since Smyth described such treatment in seven patients with bilateral masseter muscle hypertrophy [28]. A systematic review on the use of Botox for
bilateral benign masseter hypertrophy conducted by Fedorowicz et al. in 2013 stated that
the evidence on the efficacy and safety of intra-masseteric injections of Botox was still
insufficient to draw reliable conclusions [17]. However, recent reports confirm advances
in this field and present a tailored approach which increases effectiveness and reduces
complication rate [29]. In a randomized controlled study conducted by Hong et al. (2021),
the effective dose range for a reduction of the masseter muscle ranged from 48 to 72 units.
They also found that gradual reduction was observed up until 12 weeks and after that
period, reinjection should be considered for maintaining satisfactory cosmetic effect [30].
Up until now, the effectiveness of the treatment with Botox is assessed using several
tools. The most common is ultrasound, used for measuring muscle thickness. It also helps
to evaluate the condition of the masseter muscle and surrounding tissues, thus, differential
diagnosis. Ultrasound measures muscle thickness which is helpful for the determination of
the optimal dose of Botox [26,30–33]. Magnetic resonance and computerized tomography
of the masseter regions are performed commonly for the purpose of differential diagnosis
with some attempts to use them for assessments of treatment effects [34]. Apart from
the condition of the masseter muscle, it can provide information on the structure and
shape of the mandible, and help to evaluate parotid and submandibular glands [2,5,31].
Many physicians make standardized photographs with the muscles relaxed and with
patients grinding or serial photographs to document the effects of treatment [26,33,35].
Monitoring and documenting the effects of treatment is particularly important because
there is only one scale to classify masseteric hypertrophy and cosmetic results of its treatment [4]. Shear wave elastography has not been used for this purpose. However, apart from
monitoring the desired decrease in muscle tonus, is can be used for evaluation of side effects
such as fatigue and muscle weakness (associated with too much drop in muscle tonus)
which can be associated with inadequately tailored Botox dose [36]. There are ongoing
projects on the determination of desired values of masseter muscle stiffness as measured by
shear wave elastography [37]. Advantages of shear wave elastography include simplicity,
reliability, and repeatability. It can objectively measure tissue and organ stiffness. It is
characterized by good diagnostic accuracy in measuring masseter muscle stiffness [18].
It is also found to be a reliable and repeatable method for the assessment of muscle stiffness [38]. SWE proved to be a sensitive tool for monitoring changes of masseter muscle
stiffness so that it can help identify treatment failure or asymmetry occurring during Botox
treatment due to inadequate dose of Botox, odontogenic inflammation, or misdiagnosis.
Previous studies showed that masseter muscle stiffness changes after treatment or exercise
regardless of baseline values [12,27] which makes it particularly useful for evaluation of
conducted treatment. Furthermore, it can be used by physicians of all specialties [18].
Besides the masseter muscle, hypertrophy of masticatory muscles may involve the
temporalis muscle and medial pterygoid muscle as well. Enlargement of other muscles
is usually observed at the diagnosis. Guruprasad et al. reported coexistent enlargement
of the medial pterygoid muscle in addition to the masseter muscle hypertrophy, which is
rare [2]. Graziano et al. treated a series of patients some of which had unilateral or bilateral
masseteric and temporalis muscle hypertrophy. Such patients received Botox injections into
both affected muscles [1]. The present study included patients with isolated hypertrophy
of the masseter muscle. Any other pathologies of adjacent muscles were not seen.
During Botox treatment for masseter muscle hypertrophy, enlargement of other masticatory muscles may occur because the temporalis muscle can take over the functions
of the paralyzed muscles lifting the mandibula. In the present study, we observed that
the temporalis muscle became slightly enlarged on the second follow-up visit after treatment with Botox. Furthermore, a compensatory increase in the temporal muscle stiffness
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(p < 0.005 for both sides) was observed; however, the differences in terms of the magnitude
of the stiffness increase were observed among patients. These differences may be due to
many factors, including chewing patterns and diet. Preliminary reports from the literature
suggest that different foods exert differentiated effect on the activity of the masseter and
temporalis muscle [39]; further research is required in this scope. It can also be hypothesized that the long-term increase in tonus of the temporalis muscle (some patients undergo
a Botox treatment repeatedly) may result in hypertrophy of the temporalis muscle belly
and, as a result, a change in the proportion/oval of the face. Perhaps, after identifying
the factors influencing a greater increase in the temporalis muscle stiffness in subsequent
studies, administration of Botox should be considered in patients with risk factors for the
temporalis muscle hypertrophy. It may also be possible that all patients with masseter
muscle hypertrophy should be subjected to a simultaneous Botox treatment of the temporalis muscle. The Botox treatment of the masseter muscle affects remaining masticatory
muscles as well, but they are not easy to evaluate with shear-wave elastography as the
medial pterygoid muscle or play a little role in the lifting of the jaw as the lateral pterygoid muscle. For these reasons, the impact of Botox injections into the masseter muscle is
difficult to assess. However, these muscles have a relatively small volume and, therefore,
little strength, and have no effect on the face oval. Given the above, it should be noted
that the masticatory system works like a system of communicating vessels and treatment
of a single pathology may disturb the balance resulting in the development of another
pathology. For this reason, careful assessment of all masticatory muscles is recommended
during long-term treatment to ensure that the entire contour of the face is satisfactory to
the patient. Using shear wave elastography during follow-up visits, we are able to detect
increasing stiffness of other muscles of the masticatory system even before the muscle
enlargement is visible and palpable.
5. Limitations
Several limitations of this study should be mentioned. The study group included
a small number of people with a single pathology. For this reason, it was relatively
homogeneous, which did not allow investigation of the relationships among all masticatory
muscles. Next, we did not use any other tool to assess the muscle condition or cosmetic
effect achieved by treatment. However, the overall evidence on masseteric hypertrophy
is limited as is the availability of other methods. In the future studies, researchers should
focus on the use of safe and convenient methods such as shear wave elastography and
validate them against previously used objective methods which may expose the patient to
radiation or contrast use such as panoramic radiography, computed tomography, magnetic
resonance imaging. Furthermore, the reference values of masticatory muscles have not
been established yet, so we are able to monitor stiffness in one patient on subsequent
visits. Although several studies were published on the use of shear wave elastography
for measuring the masseter muscle stiffness [12,18,27,37], other muscles of the masticatory
system still need to be investigated. Finally, shear wave elastography can give information
only on the muscle stiffness without explaining physiology of the muscle tone. For this
reason, it cannot be used to investigate the causes of masseter muscle hypertrophy that
could be useful for the development of tailored treatments.
6. Conclusions
This study allowed for drawing several valuable conclusions. First, a drop in the
stiffness of the masseter muscles after a single session of Botox injections was symmetrical
despite the manual division of the application between 3–4 injection sites. This indicates
that some discrepancies are acceptable. It also suggests that the effectiveness of the dose
in each patient simply means that a certain field of work on dose reduction in subsequent
studies is open, so as to determine the lowest effective dose in all patients. Second, the
function of the masseter muscles, as a part of the whole masticatory muscle system, may
have an effect on other masticatory muscles. The study shows that an iatrogenic reduction
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of the masseter muscle stiffness results in a compensatory increase in the temporal muscle
stiffness (p < 0.005 for both sides). For this reason, a simultaneous Botox treatment of the
temporalis muscle may be required in all or selected patients undergoing treatment for
masseter hypertrophy. However, further research is needed to investigate the role of risk
factors for temporalis hypertrophy.
Shear wave elastography can help to monitor treatment effect with Botox of masseter
muscles in muscle hypertrophy and other conditions (e.g., TMD, bruxism). In comparison
to currently used methods, it offers additional benefits for the patient, such as better dose
adjustment and prompt information about the condition of other non-treated masticatory
muscles. This preliminary study shows the potential of shear wave elastography, but further
research is required to gain experience and determine stiffness values of hypertrophic
masticatory muscles. Furthermore, studies on muscle physiology can help determine the
usefulness of shear wave elastography.
The study should be considered preliminary. Further research is needed on larger
groups of patients and with longer follow-up to fully evaluate the effectiveness of the
proposed treatment and changes in the muscle stiffness.
Author Contributions: Conceptualization, C.O., A.O. and M.D.; data curation, D.M., C.O., A.O.
and P.D.; formal analysis, D.M., C.O., I.N.-H. and K.G.-L.; investigation, D.M., C.O., A.O., I.N.-H.,
S.C. and P.K.-R.; methodology, D.M., C.O., A.O., I.N.-H. and M.D.; supervision, C.O. and A.O.;
visualization, C.O.; writing—original draft, A.O.; writing—review and editing, D.M., C.O., I.N.-H.,
P.D., S.C., K.G.-L., P.K.-R. and M.D. All authors have read and agreed to the published version of
the manuscript.
Funding: This research was founded by Wroclaw Medical University (grant no SUB.B040.21.049).
Institutional Review Board Statement: The study was conducted according to the guidelines of the
Declaration of Helsinki, and approved by Bioethical Committee at the Wroclaw Medical University
(protocol code KB—633/2020 issued on 12 October 2020).
Informed Consent Statement: Informed consent was obtained from all subjects involved in the study.
Data Availability Statement: The data presented in this study are openly available in FigShare.
Conflicts of Interest: The authors declare no conflict of interest.
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