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ORIGINAL CONTRIBUTIONS

Age- and sex-related differences in


masseter size and its role in oral
functions
Chia-Shu Lin, DDS, DPhil; Ching-Yi Wu, DDS, PhD; Shih-Yun ABSTRACT
Wu, DDS; Kai-Hsiang Chuang, DDS; Hsiao-Han Lin, MSc;
Dong-Hui Cheng, DDS; Wen-Liang Lo, DDS, PhD Background. The masseter muscle plays a key structural
and functional role in the stomatognathic system. Re-
searchers’ cumulative evidence has suggested that the

T
he masseter muscle plays a key functional and variation in the size of a person’s masseter muscle may be a
structural role in the stomatognathic system. critical factor related to individual differences in oral
Masseter muscle activity is associated with functions. However, researchers have not yet investigated
chewing behavior1 and swallowing,2 and disrup- systematically the effect of a person’s age and sex on
tion in its activity may be linked to temporomandibular masseter muscle size and the association of masseter
disorders.3 The masseter is the largest jaw elevator muscle size with other clinical metrics, including mastica-
muscle and the major contributor of the strength of jaw tory performance (MP) and salivary flow rate (SFR). Using
closure,4 and its size is associated closely with bite T1-weighted magnetic resonance imaging (MRI) data
force.5,6 Cumulative evidence suggests that variation in provides a noninvasive method for assessing masseter
masseter muscle size may be a critical factor related to muscle volume (MMV).
individual differences in oral functions.4-6 Methods. Using T1-weighted MRI data, the authors
Researchers have used masticatory performance (MP) developed a voxel-based method to assess MMV and
and salivary flow rate (SFR) as the clinical metrics for investigated the associations among MMV, MP, and
evaluating chewing and swallowing abilities. Both a SFR.
person’s age and sex contribute in a critical manner to Results. The authors acquired T1-weighted MRI data
the individual differences found in MP and SFR.7,8 from scans of the heads of 62 healthy adults and assessed
However, researchers have not yet investigated system- MMV by means of using a voxel-based approach. The
atically the effect of age and sex on masseter muscle size authors’ assessment results had acceptable rates of inter-
and the association of masseter muscle size with other rater and intrarater reliability. MMV was significantly
clinical metrics. Investigators of previously published lower in the older subgroup and in the female subgroup. In
studies have reported that magnetic resonance imaging addition, the correlation for MMV was significantly posi-
(MRI) data can be used for assessing the morphology of tive with MP and stimulated SFR.
orofacial muscles9,10 with good validity.11-13 In our study, Conclusions. The study results revealed evidence that
we reasoned that T1-weighted MRI data of the head, the authors’ voxel-based approach, which they designed on
which can be acquired commonly during a brain scan, the basis of T1-weighted MRI data, would be a reliable
can be a suitable and convenient source for assessing method for quantifying MMV.
masseter muscle volume (MMV). Practical Implications. The findings suggest that the
We had 3 major goals for our study. First, we aimed to variation in masseter muscle size may be a critical factor to
develop a voxel-based approach for assessing MMV, assess individual differences in oral functions.
using T1-weighted MRI data. Second, because the Key Words. Aging; magnetic resonance imaging;
investigators of previously published studies focused mastication; masseter muscle.
JADA 2017:-(-):---
http://dx.doi.org/10.1016/j.adaj.2017.03.001
Copyright ª 2017 American Dental Association. All rights reserved.

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ORIGINAL CONTRIBUTIONS

mainly on younger adults and used smaller sample We defined the right and left masseter muscle
sizes,14-17 we determined that, by means of collecting data separately.
from a larger sample, we could investigate the age- - Primarily, we based the delineation of the region of

and sex-related effects on MMV. Because previous interest (ROI) of the masseter muscle on the anatomic
investigators’ findings revealed age-related differences in landmarks that we could clearly and repeatedly identify
the masseter cross-sectional area18 and sex-related dif- in a T1-weighted image (Figure 1A). First, we delineated
ferences in the masseter muscle thickness,19 we hypoth- the border of the ROI on the sagittal view from the
esized that a reduced MMV would be associated with lateral to the medial position (Figure 1A).
older age (hypothesis 1) and female sex (hypothesis 2). - We examined the resulting masseter ROI from the

Third, we investigated the association between MMV axial view and the coronal view.
and the major clinical metrics of oral functions: MP, - Using another software tool (fslstats, Oxford Centre

unstimulated SFR (uSFR), and stimulated SFR (sSFR). for Functional MRI of the Brain), we quantified the
We hypothesized that MMV would correlate positively muscle volume for each side according to the number of
with MP (hypothesis 3) and that an increased MMV voxels within the defined masseter ROI. We determined
would be associated with increased sSFR7 (hypothesis 4). the MMV value by means of calculating the average of
the muscle volume from both sides.
METHODS Reliability of the MMV assessment. To evaluate the
Study group. We recruited 62 healthy study participants intrarater reliability of the method, 1 of the authors
(39 women and 23 men; age range, 23-74 years) to receive (K.-H.C.) independently assessed the MRI data of 20
a T1-weighted MRI scan and assessments of oral func- study participants, by means of using the same protocol.
tions, including MP, uSFR, and sSFR. We recruited To evaluate the intrarater test-retest reliability, 1 of the
volunteers by advertising in local community centers and authors (C.-S.L.) performed a second assessment of the
the Taipei Veterans General Hospital (Taiwan). We MRI data of 20 study participants 1 month after the first
excluded from participation volunteers who had a his- assessment. We quantitatively assessed both of the reli-
tory of major physical or psychiatric disorders, brain ability tests, by means of using the intraclass correlation
injury, or brain surgery, as well as those who were unable coefficient (ICC), and we qualitatively assessed the tests,
to undergo MRI owing to physical or psychological by means of using the Bland-Altman plot.
contraindications. We received written informed consent Assessment of MP. Using the colorimetric method,
from all participants before the experiment initiated. The we assessed MP.21 After receiving the scan, each partic-
institutional review boards of National Yang-Ming ipant chewed a piece of color-changeable chewing gum
University (Taipei, Taiwan) and Taipei Veterans General (Lotte) for 3 minutes.22,23 We digitized the chewed gum,24
Hospital approved the study. and we assessed the color change by means of using the
Acquisition of head T1-weighted MRI. Using a 3 L*a*b* chromatic system.22
Tesla Siemens MRI scanner (Siemens Magnetom Trio, Assessment of SFR. We collected saliva by means of
A Tim System, Siemens), we performed all of the modifying procedures that investigators had described
T1-weighted MRIs at the 3T MRI Laboratory of National previously.25 The study participants refrained from
Yang-Ming University. We acquired the images by eating, drinking, or toothbrushing for an hour before
means of using a 32-channel head coil, using the we collected the samples. Among all the participants
magnetization prepared rapid gradient-echo sequence (N ¼ 62), we excluded the results or did not perform an
(repetition time, 2,530 milliseconds; echo time, 3.03 ms; assessment in 26 participants, because those participants
flip angle, 7 ; matrix size, 256  256  192; voxel size, 1  had eaten a meal or had a drink right before the
1  1 cubic millimeters), which we based on the protocol assessment. To collect unstimulated saliva, we asked
that we reported in our previous studies.20 participants to drool saliva passively into a tube, the
Protocol for the MMV assessment. We assessed weight of which we measured, for 10 minutes after
MMV using a voxel-based approach, which we based on swallowing the remaining saliva. We limited study par-
the following protocol: ticipants’ movements of the head and neck regions, and
- Originally, we stored the acquired images according we asked them to limit their speech. To obtain samples of
to the Digital Imaging and Communications in Medicine participants’ stimulated saliva, we asked the participants
standard and then transformed the images to the
Neuroimaging Informatics Technology Initiative data
format. We performed all investigations by means of
ABBREVIATION KEY. MMV: Masseter muscle volume.
using the imaging tool FSLView 3.2.0 (Oxford Centre for MP: Masticatory performance. MRI: Magnetic resonance
Functional MRI of the Brain). imaging. MW: Mann-Whitney U test. Q1: Lower quartile. Q3:
- One author (C.-S.L.) manually defined the anatomic
Upper quartile. ROI: Region of interest. SFR: Salivary flow rate.
region of the masseter muscle without additional sSFR: Stimulated salivary flow rate. SW: Shapiro-Wilk. uSFR:
between-image registration or intensity normalization. Unstimulated salivary flow rate.

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ORIGINAL CONTRIBUTIONS

Interrater assessment 6
RATER 2 – RATER 1, cm3

Mean + 2 SD
of MMV Mean – 2 SD
(K.-H. CHUANG), cm3

50 4
Mean of difference
40 2
RATER 2

30 0
20 0 10 20 30 40 50
–2
10
–4
0
0 10 20 30 40 50 –6
RATER 1 (C.-S. LIN), cm3 (RATER 1 + RATER 2)/2, cm3
TIME POINT 2 – TIME POINT 1, cm3

6
Interrater assessment Mean + 2 SD
of MMV 4 Mean – 2 SD
TIME POINT 2, cm3

50 Mean of difference
40 2
30 0
20 0 10 20 30 40 50
–2
10
–4
0
0 10 20 30 40 50 –6

B TIME POINT 1, cm3 (TIME POINT 1 + TIME POINT 2)/2, cm3

Figure 1. Manual delineation and assessment of the masseter muscle from the head T1-weighted magnetic resonance imaging scan. A. The
upper panels show the surrounding structures identified at a lower position (near the mandibular ramus, the upper left panel) and a higher position
(near the mandibular condyle, the upper right panel). The lower panel shows the sagittal view of the delineated masseter region (red) from 1
participant, from the lateral position (upper left) to the medial position (lower right). B. The results of interrater and intrarater reliability analyses.
The authors’ analyses found strong correlation of the estimated masseter muscle volume (MMV) between raters and between 2 time points. Results
of the Bland-Altman plots revealed that the difference in the MMV between raters and between time points were consistent, generally with a
standard deviation (SD) in the range of 2. cm3: Cubic centimeters.

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TABLE 1 Wilk test. We considered the distribu-


Results of demographic data and clinical metrics. tion of scores to be normal if the P
value of the test was greater than .05.
VARIABLE AGE, Y MP* MMV,† cubic uSFR,‡ milliliters sSFR,§ Owing to the nonnormal distribution
centimeters per minute mL/min
of the results (see the Results section of
Total
this article and Table 1), we performed
N 62 62 62 36 36
nonparametric tests for the statistical
SW¶ test < .001 < .001 .007 .001 .011
analysis. To compare results between
Mean 50.1 71.9 24.9 0.32 1.94
participants’ sex-related or age-related
Standard 17.1 2.8 7.2 0.25 1.19
deviation subgroups, we performed the 2-tailed,
Median 55.5 72.3 22.9 0.26 1.72 Mann-Whitney U test. Using the
Q3# 64.0 73.6 29.0 0.42 2.29 Spearman rank correlation, we assessed
Q1** 30.0 71.1 19.3 0.14 1.33 the strength of the association between
Maximum 74.0 76.5 44.9 1.21 4.93 the clinical metrics. For each hypothe-
Minimum 23.0 63.5 11.7 0.05 0.12 sis, we considered the result of the
Younger
statistical tests to be significant if the
Subgroup a level was .05.
N 31 31 31 26 26
Median 30.0 73.1 27.0 0.30 1.94 RESULTS
Q3 51.0 74.5 31.3 0.49 2.59 Reliability of the MMV assessment.
Q1 25.5 72.0 19.6 0.22 1.61 For the interrater reliability, we found
Older that the results of the ICC test (2-way
Subgroup
mixed model, average measurement
N 31 31 31 10 10
for absolute agreement) had a strong
Median 64.0 71.2 21.8 0.13 1.29
reliability (ICC, 0.996; P < .001).
Q3 67.0 72.6 26.3 0.23 1.52
For the intrarater reliability, we found
Q1 60.0 69.5 19.1 0.06 0.59
††
that the results of the ICC test (2-way
MW test < .001 < .001 .043 .022 .004
mixed model, average measurement
Female
Subgroup
for consistency) had a strong
N 39 39 39 22 22
reliability (ICC, 0.997; P < .001)
Median 56.0 72.0 20.1 0.23 1.60
(Figure 1B).
Q3 62.5 73.1 24.0 0.36 1.96
Demographic profile and clinical
Q1 33.5 70.9 18.6 0.14 0.91
metrics. Tables 1 and 2 show the
Male Subgroup
results of descriptive analysis of the
N 23 23 23 14 14
demographic data and clinical metrics.
Median 54.0 72.7 31.2 0.38 2.38
Consistent with the previous find-
7,27
Q3 64.5 74.5 36.0 0.62 4.02
ings, we found that the correlation
Q1 30.0 71.4 26.3 0.17 1.61
for age was significantly negative
MW test .953 .079 < .001 .098 .014
with MP (r, 0.53; P < .001), stimu-
* MP: Masticatory performance (change in L*a*b* chromatic system).
lated SFR (r, 0.52; P ¼ .001),
† MMV: Masseter muscle volume. and unstimulated SFR (r, 0.48;
‡ uSFR: Unstimulated salivary flow rate. P ¼ .003). We found that the correla-
§ sSFR: Stimulated salivary flow rate.
¶ SW: Shapiro-Wilk. The authors evaluated normality on the basis of the results of the Shapiro- tion between sSFR and uSFR was
Wilk test. The number denotes the P value of the test. significantly positive (r, 0.60; P < .001)
# Q3: Upper quartile. (Figure 2). We found that, among all
** Q1: Lower quartile.
†† MW: Mann-Whitney U test. The authors conducted between-group differences on the basis the participants, the correlation for
of the results of the Mann-Whitney U test. The number denotes the P value of the test. MMV was significant with MP (r, 0.29;
P ¼ .02) (Figure 3), which confirmed
to chew paraffin wax (GC) for 3 minutes during saliva hypothesis 3. We also found that the correlation for
collection. Next, we weighed the tube to calculate the MMV was significantly positive with sSFR (r, 0.33; P ¼
weight of saliva, and then we calculated the volume of .02) but not uSFR (r, 0.15; P ¼ .40) (Table 2), which
saliva, assuming that the density of saliva was 1 gram per confirmed hypothesis 4. In addition, we found that the
milliliter.26 correlation for MP was significantly positive with sSFR
Statistical analysis. We examined all the clinical (r, 0.41; P ¼ .014) but not uSFR (r, 0.26; P ¼ .13)
metrics for normality, by means of using the Shapiro- (Table 2).

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Sex- and age-related differences in the clinical significantly positive with sSFR (r, 0.51; P ¼ .014)
metrics. In terms of age-related effects, MMV was (Figure 2B).
significantly lower in the older subgroup compared
with the younger subgroup (younger, 27.0 [median] DISCUSSION
[19.6 (lower quartile) to 31.3 (upper quartile)] cm3; older, Summary of the major findings. With the results of this
21.8 [19.1 to 26.3] cm3; P ¼ .043), confirming hypothesis 1. study, we have provided new evidence regarding the age-
In addition, we found that the older subgroup had a and sex-related differences in the MMV of healthy
significant decrease in MP (younger, 73.1 [72.0 to 74.5]; adults. First, we established the voxel-based approach for
older, 71.3 [69.9 to 73.0]; P ¼ .005), uSFR (younger, 0.30 assessing MMV, which we based on the T1-weighted
[0.22 to 0.49] mL/min; older, 0.13 [0.06 to 0.23] mL/min; MRI data from scans of the head. We found that, by
P ¼ .022), and sSFR (younger, 1.94 [1.61 to 2.59] mL/min; means of using the approach, we had an acceptable
older, 1.29 [0.59 to 1.52] mL/min; P ¼ .004) compared interrater and intrarater reliability. Second, related to
with the younger subgroup (Table 1). MMV, we found a significant sex-related and age-related
In terms of sex-related effects, MMV was significantly difference, which was smaller in the female subgroup
higher in the male subgroup compared with the and the older subgroup. Finally, we found a positive
female subgroup (male, 31.2 [26.3 to 36.0] cm3; female, correlation between MMV and MP as well as stimulated
20.1 [18.6 to 24.0] cm3; P < .001), confirming hypothesis SFR. The findings suggest that there is a substantial as-
2. In addition, sSFR was significantly higher in the male sociation between the anatomic signature of stomatog-
subgroup compared with the female subgroup (male, 2.38 nathic system and the clinical metrics of oral functions.
[1.61 to 4.02] mL/min; female, 1.60 [0.91 to 1.96] mL/min; Voxel-based assessment of the MMV. Investigators
P ¼ .014) (Table 1). We also investigated whether an of previously published studies have suggested that
interactional effect existed between the age- and sex- MRI data can be used to evaluate the morphology of
related factors. For both age subgroups, we found an age- masticatory muscle.9,10 Our findings also revealed that
related difference (that is, a higher level of MMV in the T1-weighted MRI data from scans of the head, which
the male subgroup than in the female subgroup). In are used widely for assessing brain morphology in
contrast, for both the male and female subgroups, we did neurologic examinations, can be a suitable and conve-
not find a significant difference among the age sub- nient source for assessing MMV. The mean MMV (24.9
groups. The findings revealed a main effect related to cm3) that we assessed using our approach is similar to
male or female sex in MMV and no evidence of an the previously published findings from investigators in
interaction between age and male or female sex. different geographic regions, including a sample from the
Age-related differences in the association between Netherlands (N ¼ 31; mean age, 24 years; mean MMV,
the clinical metrics. Table 2 summarizes the results of 23.8 cm3),14 samples from Japan (N ¼ 25; mean age, 23
age-related differences related to the clinical metrics. In years; mean MMV, 24.7 cm3; and N ¼ 10; 20-30 years,
the older group, we found that the correlation for age median MMV, 29.2 cm3),15,16 and a sample from
was significantly negative with MP (r, 0.49; P < .005) Singapore (N ¼ 12; 20-25 years; mean MMV, 29.5 cm3).17
(Figure 2A) but not MMV. In contrast, in the younger Also, our results are similar to those of investigators
group, we found that the correlation for age was signif- who assessed the wet contractile muscle volume in post-
icantly positive with MMV (r, 0.45; P ¼ .011) (Figure 3A) mortem samples (20.1 cm3).28 Although ethnic and
but not MP. In addition, in the younger group, we found regional factors may have contributed to substantial in-
that the correlations between uSFR and sSFR were dividual variations, in general, we found that our results
significantly positive (r, 0.69; P < .001) (Figure 2A). had a convergent result of the estimated MMV.
Sex-related differences in the association between In terms of the reliability of the approach, our results
the clinical metrics. Table 2 summarizes the results of show both acceptable interrater and intrarater reliability.
the sex-related differences among the clinical metrics. In This good level of reliability may be attributed to the
both sex-related subgroups, we found that the correlation masseter’s homogeneity in terms of its composition of
for age was significantly negative with MP (female: muscle fibers29 and its lateral position to the teeth. The
r, 0.57; P < .001; male: r, 0.49; P ¼ .018) and sSFR latter (the masseter’s lateral position to the teeth) is
(female: r, 0.58; P ¼ .005; male: r, 0.58; P ¼ .029) crucial to the assessment, because the magnetic reso-
(Figure 2B). We found that both groups had a signifi- nance signal can be disturbed severely by intraoral metal
cantly positive correlation between uSFR and sSFR restorations. In terms of the validity of the approach,
(female: r, 0.50; P ¼ .019; male: r, 0.72; P ¼ .004) investigators have reported widely about the convergence
(Figure 2B). In addition, in the male subgroup, we found between the MRI-based methods and other methods.
that the correlation for age was significantly negative The investigators of previously published studies have
with uSFR (r, 0.67; P ¼ .008) (Figure 2B). In the female reported a high level of correlation between the muscle
subgroup, we found that the correlation for MP was volume assessed using MRI and that assessed using

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TABLE 2
Association between clinical metrics.
CLINICAL TOTAL YOUNGER SUBGROUP OLDER SUBGROUP
METRIC
N [ 62 N [ 36 N [ 31 N [ 26 N [ 31
MP* MMV,† cubic uSFR,‡ sSFR,§ MP MMV, cm3 uSFR, sSFR, MP MMV, cm3
centimeters milliliters mL/min mL/min mL/min
per minute
Age 0.525¶ 0.074 0.476¶ 0.518¶ 0.008 0.452# 0.325 0.307 0.494¶ 0.163
MP –** 0.293 #
0.257 0.406 #
– 0.185 0.146 0.231 – 0.214
MMV – – 0.145 0.334# – – 0.264 0.279 – –
uSFR – – – 0.595¶ – – – 0.689¶ – –
* MP: Masticatory performance (change in L*a*b* chromatic system).
† MMV: Masseter muscle volume.
‡ uSFR: Unstimulated salivary flow rate.
§ sSFR: Stimulated salivary flow rate.
¶ P < .01.
# P < .05.
** Dashes indicate data not applicable.

ultrasonography12 and from postmortem dissection.13 size and tension.30,31 Our results echoed a finding pub-
Researchers using animal models also have reported a lished in 2017 in which investigators compared the oral
high level of consistency between the volume of the functions of people who were elderly and in robust health
tongue assessed using MRI and the wet weight of the with people who were elderly and in frail or near-frail
tongue.11 Notably, the muscle thickness obtained using health. According to the results of that study, investigators
ultrasonography may be smaller than that obtained using only found age-related decrease in muscle thickness in the
MRI, owing to the compression of muscle during the study participants who were in near-frail health, but not
ultrasonography scan.12 In contrast, we acquired the MRI the in the study participants who were in robust health.31
of the head when each study participant was lying in a We found that male or female sex was a major
fixed position and undisturbed. Therefore, MMV contributing factor to the variation in MMV (Figure 3B).
assessed using MRI may be a better indicator of the Investigators found consistently higher masticatory
masseter size under a natural and resting condition. muscle thickness in men compared with women.19 On a
Age- and sex-related differences in the MMV. Our functional level, investigators also found that male or
results are consistent with previously published findings, female sex was a major contributing factor to individual
which show that there are great individual differences in differences in maximal bite force.32 We found that such a
MMV. On average, study participants in the older sub- sex-related effect did not intersect with age. This finding
group had a lower MMV compared with participants in from our study results implies that, compared with age,
the younger subgroup (Table 1). However, when we male or female sex may be a more predominant
combined the results of participants from both sub- contributing factor to individual variations in MMV.
groups, we did not find an age-related decline in MMV Clinical implications. Among all study participants,
(Table 2 and Figure 3A). This result is inconsistent with we found a significantly positive correlation between
the previously published finding in which investigators MMV and MP. Investigators have found that individual
noted a negative correlation between age and masseter differences in MP are associated with the number of
muscle thickness.18 A potential methodological explana- functional teeth and bite force.33 Because the participants
tion is that thickness may increase when the muscle we recruited for our study had a sound posterior contact
contracts.12 Therefore, the age-related decline in (either with natural teeth or restoration), we reasoned
muscle thickness may be confounded by the decline of that the higher MP may have been associated with a
muscle tension. In contrast, in our study, we assessed higher MMV. We did not directly assess the participants’
the muscle volume when it was in a relaxed state, at bite force. Nevertheless, the investigators of previously
which time we thought muscle volume would be less published studies have revealed that jaw muscle size was
disturbed by muscle tension. Another potential expla- a major factor that explained most of the variation in
nation is related to the physical and dental conditions of bite force6 and that masticatory muscle thickness corre-
the sample. Our study participants were physically lated positively with bite force.5 The evidence we found
robust and dentally sound in posterior contact. In- in our study suggests that there is a coupling between
vestigators have reported that a lack of physical fitness structure (muscle size) and function (bite force) in the
and a loss of posterior contact are associated with muscle stomatognathic system.

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TABLE 2 (CONTINUED)

OLDER SUBGROUP FEMALE SUBGROUP MALE SUBGROUP


N [ 10 N [ 39 N [ 22 N [ 23 N [ 14
3 3
uSFR, sSFR, MP MMV, cm uSFR, sSFR, MP MMV, cm uSFR, sSFR,
mL/min mL/min mL/min mL/min mL/min mL/min
0.286 0.333 0.571¶ 0.066 0.373 0.580¶ 0.490# 0.172 0.673¶ 0.582#
0.024 0.511 – 0.155 0.049 0.514 #
– 0.306 0.459 0.240
0.659# 0.322 – – 0.353 0.128 – – 0.191 0.095
– 0.122 – – – 0.496# – – – 0.719¶

80 80
PERFORMANCE

PERFORMANCE
MASTICATORY

MASTICATORY
75 75

70 70

65 65
Younger Older Male Female
60 60
20 30 40 50 60 70 80 20 30 40 50 60 70 80
AGE (YEAR) AGE (YEAR)
1.6 1.6
UNSTIMULATED SFR

UNSTIMULATED SFR

1.4 1.4
1.2 1.2
(mL/min)

(mL/min)

1.0 1.0
0.8 0.8
0.6 0.6
0.4 0.4
0.2 0.2
0.0 0.0
20 30 40 50 60 70 80 20 30 40 50 60 70 80
AGE (YEAR) AGE (YEAR)
5 5
STIMULATED SFR
STIMULATED SFR

4 4
(mL/min)
(mL/min)

3 3

2 2

1 1

0 0
20 30 40 50 60 70 80 20 30 40 50 60 70 80
AGE (YEAR) AGE (YEAR)
5 5
STIMULATED SFR

STIMULATED SFR

4 4
(mL/min)

(mL/min)

3 3
2 2
1 1

0 0
0.0 0.5 1.0 1.5 0.0 0.5 1.0 1.5
A UNSTIMULATED SFR (mL/min) B UNSTIMULATED SFR (mL/min)

Figure 2. The association among the clinical metrics other than masseter muscle volume. A. The results were labeled differentially as the younger
(red) and the older (blue) subgroups. B. The results were labeled differentially as the male (red) and the female (blue) subgroups. Masticatory
performance: Change in L*a*b* chromatic system. mL: Milliliters. SFR: Salivary flow rate.

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older subgroup, we did


MASSETER MUSCLE 50 80 not find a positive cor-
relation between uSFR

PERFORMANCE
VOLUME (cm3)
40

MASTICATORY
75 and sSFR or between
30
sSFR and MP. We
70 recommend that this
20 negative finding be
65 interpreted cautiously,
10 because in the older
Younger Older
0 60 subgroup, the sample
20 30 40 50 60 70 80 0 10 20 30 40 50 size for saliva assessment
was relatively small
AGE (YEAR) MASSETER MUSCLE (N ¼ 10), which may
A VOLUME (cm ) 3
have increased the risk of
developing a type II
50 80 error.
MASSETER MUSCLE

Both chewing and

PERFORMANCE
VOLUME (cm3)

40

MASTICATORY
75 saliva secretion are
30 crucial to swallowing. In
70 patients with xerostomia
20 (for example, patients
10
65 with Sjögren syndrome
Male Female or patients who are
0 60 receiving chemoradiation
20 30 40 50 60 70 80 0 10 20 30 40 50 therapy), investigators
AGE (YEAR) MASSETER MUSCLE commonly have seen
B VOLUME (cm ) 3 dysphagia and insuffi-
cient bolus preparation
and a substantially
Figure 3. The association between masseter muscle volume (in cubic centimeters) and age-related and delayed phase of oropha-
masticatory performance. Both panels included all participants (N ¼ 62). A. The results were labeled differentially ryngeal swallowing.36,37
as the younger (red) and the older (blue) subgroups. B. The results were labeled differentially as the male (red)
and the female (blue) subgroups. Masticatory performance: Change in L*a*b* chromatic system. Our results indicate that
as age increases, both MP
and SFR also could
We should note that, apart from MMV, other factors decline. In addition, our findings suggest that it is critical
could contribute to MP, such as the secretion of saliva. for clinicians to evaluate systematically the mastication
Of note in our study, we adopted the chewing-gum and saliva secretion of people who are elderly as part of the
approach for assessing MP, which we thought would assessment of dysphagia.
better characterize one’s “mixing ability” instead of the MRI is not an examination that clinicians primarily
“cutting ability” of mastication.34 As a critical intraoral consider to assess patients’ oral functions. Nevertheless,
lubricant, saliva plays a key role in the mixing procedure. clinicians in geriatric medicine widely recommend that
In our study, we found that the association between patients undergo MRIs, especially when they are diag-
mastication and saliva secretion could be evidenced by nosing a patient’s neurological and psychiatric diseases.
the positive correlation between uSFR and sSFR and These MRI data comprise not only the brain area but
between sSFR and MP, especially in the younger group also the orofacial and neck area; therefore, an MRI scan
(Table 2). Because we collected sSFR levels when the could be an available and convenient source of results for
study participants were chewing paraffin wax, we a clinician to use when assessing a patient’s masseter
determined that this finding implies that the individual muscle. Neuroimaging evidence from study results have
differences in masticatory ability could be a contributing shown that age-related frailty or cognitive impairment
factor to the transition of saliva secretion from the were associated with regional alterations in the brain38,39
resting condition (unstimulated) to the chewing condi- and that chewing ability may be associated with one’s
tion (stimulated). In line with our findings, other in- cognitive functions.40,41 Therefore, for adults who are
vestigators have noted that SFR has correlated positively elderly, especially those who have physical frailty or
with maximal bite force27 and has been associated with cognitive dysfunction, concurrent assessments of MMV
the masticatory–parotid salivary reflex.35 In our study’s (on the basis of available MRI data), MP, and SFR may

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ORIGINAL CONTRIBUTIONS

provide more information for clinicians to use when 8. Percival RS, Challacombe SJ, Marsh PD. Flow rates of resting whole
and stimulated parotid saliva in relation to age and sex. J Dent Res. 1994;
evaluating the patients’ health conditions. 73(8):1416-1420.
9. Farrugia ME, Bydder GM, Francis JM, Robson MD. Magnetic reso-
nance imaging of facial muscles. Clin Radiol. 2007;62(11):1078-1086.
CONCLUSIONS 10. Schellhas KP. MR imaging of muscles of mastication. AJR Am J
Roentgenol. 1989;153(4):847-855.
The evidence from our study results revealed that 11. Lauder R, Muhl ZF. Estimation of tongue volume from magnetic
the voxel-based approach, which is based on T1- resonance imaging. Angle Orthod. 1991;61(3):175-184.
weighted MRI data, could be a reliable method for 12. Raadsheer MC, Van Eijden TM, Van Spronsen PH, Van Ginkel FC,
Kiliaridis S, Prahl-Andersen B. A comparison of human masseter muscle
quantifying MMV. Using this method, we identified thickness measured by ultrasonography and magnetic resonance imaging.
both age- and sex-related differences in MMV. Our Arch Oral Biol. 1994;39(12):1079-1084.
findings suggested a close relationship between the 13. Wu EX, Tang H, Tong C, Heymsfield SB, Vasselli JR. In vivo MRI
structure (the masseter muscle) and the function quantification of individual muscle and organ volumes for assessment of
anabolic steroid growth effects. Steroids. 2008;73(4):430-440.
(masticatory performance and saliva secretion) in 14. Boom HP, van Spronsen PH, van Ginkel FC, et al. A comparison of
study participants’ stomatognathic systems. n human jaw muscle cross-sectional area and volume in long- and short-face
subjects, using MRI. Arch Oral Biol. 2008;53(3):273-281.
Dr. Chia-Shu Lin is an associated professor, Department of Dentistry, 15. Goto TK, Tokumori K, Nakamura Y, et al. Volume changes in human
School of Dentistry, National Yang-Ming University, No. 155, Sec. 2, Linong masticatory muscles between jaw closing and opening. J Dent Res. 2002;
St., Taipei, 11221 Taiwan (ROC), e-mail winzlin@ym.edu.tw. Address cor- 81(6):428-432.
respondence to Dr. Chia-Shu Lin. 16. Kitai N, Fujii Y, Murakami S, Furukawa S, Kreiborg S, Takada K. Human
Dr. Ching-Yi Wu is an assistant professor, Institute of Oral Biology, masticatory muscle volume and zygomatico-mandibular form in adults with
School of Dentistry, National Yang-Ming University, and a training mandibular prognathism. J Dent Res. 2002;81(11):752-756.
physician, Division of Family Dentistry, Department of Stomatology, Taipei 17. Ng HP, Foong KW, Ong SH, et al. Quantitative analysis of human
Veterans General Hospital, Taipei, Taiwan. masticatory muscles using magnetic resonance imaging. Dentomaxillofac
Dr. Shih-Yun Wu is a visiting staff member, Division of Family Dentistry, Radiol. 2009;38(4):224-231.
Department of Stomatology, Taipei Veterans General Hospital, and an 18. Newton JP, Yemm R, Abel RW, Menhinick S. Changes in human jaw
adjunct lecturer, Department of Dentistry, School of Dentistry, National muscles with age and dental state. Gerodontology. 1993;10(1):16-22.
Yang-Ming University, Taipei, Taiwan. 19. Ohara Y, Hirano H, Watanabe Y, et al. Masseter muscle tension
Dr. Chuang is a graduate student of prosthodontics, Department of and chewing ability in older persons. Geriatr Gerontol Int. 2013;13(2):
Dentistry, School of Dentistry, National Yang-Ming University, Taipei, 372-377.
Taiwan. 20. Lin CS, Wu SY, Wu LT. The anterior insula and anterior cingulate
Dr. Hsiao-Han Lin is a research assistant, Department of Dentistry, cortex are associated with avoidance of dental treatment based on
School of Dentistry, National Yang-Ming University, Taipei, Taiwan. prior experience of treatment in healthy adults. BMC Neurosci. 2015;16(88):
Dr. Cheng is a visiting staff member, Division of Prosthodontics, 1-17.
Department of Stomatology, Taipei Veterans General Hospital, Taipei, 21. Hayakawa I, Watanabe I, Hirano S, Nagao M, Seki T. A simple
Taiwan. method for evaluating masticatory performance using a color-changeable
Dr. Lo is the division chair, Division of Oral and Maxillofacial Surgery, chewing gum. Int J Prosthodont. 1998;11(2):173-176.
Department of Stomatology, Taipei Veterans General Hospital, and an 22. Hama Y, Kanazawa M, Minakuchi S, Uchida T, Sasaki Y. Reliability
adjunct associate professor, Department of Dentistry, School of Dentistry, and validity of a quantitative color scale to evaluate masticatory perfor-
National Yang-Ming University, Taipei, Taiwan. mance using color-changeable chewing gum. J Med Dent Sci. 2014;61(1):1-6.
23. Kikutani T, Tamura F, Nishiwaki K, et al. Oral motor function and
Disclosure. None of the authors reported any disclosures. masticatory performance in the community-dwelling elderly. Odontology.
2009;97(1):38-42.
This study was funded by grant 103-2314-B-010-025-MY3 awarded to Dr. 24. Schimmel M, Christou P, Herrmann F, Muller F. A two-colour
C.-S. Lin by the Ministry of Science and Technology of Taiwan (Taipei). chewing gum test for masticatory efficiency: development of different
This study also was supported in part by the 3T MRI Core Facility in assessment methods. J Oral Rehabil. 2007;34(9):671-678.
National Yang-Ming University, Taipei, Taiwan. 25. Navazesh M, Kumar SK; University of Southern California School of
Dentistry. Measuring salivary flow: challenges and opportunities. JADA.
1. Iguchi H, Magara J, Nakamura Y, et al. Changes in jaw muscle activity 2008;139(suppl):35S-40S.
and the physical properties of foods with different textures during chewing 26. Rohleder N, Wolf JM, Maldonado EF, Kirschbaum C. The psycho-
behaviors. Physiol Behav. 2015;152(Pt A):217-224. social stress-induced increase in salivary alpha-amylase is independent of
2. Hiraoka K. Changes in masseter muscle activity associated with saliva flow rate. Psychophysiology. 2006;43(6):645-652.
swallowing. J Oral Rehabil. 2004;31(10):963-967. 27. Yeh C-K, Johnson DA, Dodds MWJ, Sakai S, Rugh JD, Hatch JP.
3. Mapelli A, Zanandrea Machado BC, Giglio LD, Sforza C, De Association of salivary flow rates with maximal bite force. J Dent Res. 2000;
Felicio CM. Reorganization of muscle activity in patients with chronic 79(8):1560-1565.
temporomandibular disorders. Arch Oral Biol. 2016;72:164-171. 28. Van Eijden TM, Korfage JA, Brugman P. Architecture of the human
4. McComas AJ. Oro-facial muscles: internal structure, function and jaw-closing and jaw-opening muscles. Anat Rec. 1997;248(3):464-474.
ageing. Gerodontology. 1998;15(1):3-14. 29. Hannam AG, McMillan AS. Internal organization in the human jaw
5. Raadsheer MC, van Eijden TM, van Ginkel FC, Prahl-Andersen B. muscles. Crit Rev Oral Biol Med. 1994;5(1):55-89.
Contribution of jaw muscle size and craniofacial morphology to human 30. Gaszynska E, Godala M, Szatko F, Gaszynski T. Masseter muscle ten-
bite force magnitude. J Dent Res. 1999;78(1):31-42. sion, chewing ability, and selected parameters of physical fitness in elderly
6. Sasaki K, Hannam AG, Wood WW. Relationships between the size, care home residents in Lodz, Poland. Clin Interv Aging. 2014;9:1197-1203.
position, and angulation of human jaw muscles and unilateral first molar 31. Watanabe Y, Hirano H, Arai H, et al. Relationship between frailty and
bite force. J Dent Res. 1989;68(3):499-503. oral function in community-dwelling elderly adults. J Am Geriatr Soc. 2017;
7. Ikebe K, Matsuda K, Kagawa R, et al. Association of masticatory 65(1):66-76.
performance with age, gender, number of teeth, occlusal force and salivary 32. Palinkas M, Nassar MS, Cecilio FA, et al. Age and gender influence
flow in Japanese older adults: is ageing a risk factor for masticatory on maximal bite force and masticatory muscles thickness. Arch Oral Biol.
dysfunction? Arch Oral Biol. 2011;56(10):991-996. 2010;55(10):797-802.

JADA ( )
- - http://jada.ada.org - 2017 9
ORIGINAL CONTRIBUTIONS

33. Hatch JP, Shinkai RS, Sakai S, Rugh JD, Paunovich ED. Determinants 37. Rogus-Pulia NM, Logemann JA. Effects of reduced saliva production
of masticatory performance in dentate adults. Arch Oral Biol. 2001;46(7): on swallowing in patients with Sjogren’s syndrome. Dysphagia. 2011;26(3):
641-648. 295-303.
34. Weijenberg RA, Scherder EJ, Visscher CM, Gorissen T, 38. Bharath S, Joshi H, John JP, et al. A multimodal structural and
Yoshida E, Lobbezoo F. Two-colour chewing gum mixing ability: functional neuroimaging study of amnestic mild cognitive impairment. Am
digitalisation and spatial heterogeneity analysis. J Oral Rehabil. 2013; J Geriatr Psychiatry. 2017;25(2):158-169.
40(10):737-743. 39. Chen WT, Chou KH, Liu LK, et al. Reduced cerebellar gray matter is
35. Hector MP, Linden RW. The possible role of periodontal mechano- a neural signature of physical frailty. Hum Brain Mapp. 2015;36(9):3666-3676.
receptors in the control of parotid secretion in man. Q J Exp Physiol. 1987; 40. Lexomboon D, Trulsson M, Wardh I, Parker MG. Chewing ability
72(3):285-301. and tooth loss: association with cognitive impairment in an elderly pop-
36. Rogus-Pulia NM, Larson C, Mittal BB, et al. Effects of change in ulation study. J Am Geriatr Soc. 2012;60(10):1951-1956.
tongue pressure and salivary flow rate on swallow efficiency following 41. Ono Y, Yamamoto T, Kubo KY, Onozuka M. Occlusion and brain
chemoradiation treatment for head and neck cancer. Dysphagia. 2016;31(5): function: mastication as a prevention of cognitive dysfunction. J Oral
687-696. Rehabil. 2010;37(8):624-640.

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