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The physiology of habitual bone strains
de Jong, W.C.
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Citation for published version (APA):de Jong, W. C. (2011). The physiology of habitual bone strains.
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Download date: 17 Aug 2019
CHAPTER 5
THE ROLE OF
MASTICATORY MUSCLES
IN THE CONTINUOUS LOADING
OF THE MANDIBLE
Chapter 5
~ 86 ~
§ 5.1 Abstract
Muscles are considered to play an important role in the ongoing daily loading of bone,
especially in the masticatory apparatus. Currently, there are no measurements describing
this role over longer periods of time. We made simultaneous and wireless in-vivo recordings
of habitual strains of the rabbit mandible and masseter muscle and digastric muscle activity
up to ~25 hours. The extent to which habitually occurring bone strains were related to
muscle-activity bursts in time and in amplitude is described.
The data reveal the masseter muscle to load the mandible almost continuously
throughout the day, either within cyclic activity bouts or with thousands of isolated muscle
bursts. Mandibular strain events rarely took place without simultaneous masseter activity,
whereas the digastric muscle only played a small role in loading the mandible. The average
intensity of the masseter-muscle activity bouts was strongly linked to the average amplitude
of the concomitant bone-strain events. However, within cyclic loading bouts, individual
pairs of muscle bursts and strain events showed no relation in amplitude. Larger bone-strain
events, presumably related to larger muscle-activity levels, had more constant principal-
strain directions. Finally, muscle-to-bone force transmissions were detected to take place at
frequencies up to 15 Hz.
We conclude that in the ongoing habitual loading of the rabbit mandible, the
masseter muscle plays an almost non-stop role. In addition, our results support the
possibility that muscle activity is a source of low-amplitude, high-frequency bone loading.
Masticatory Muscles and Bone Strain
~ 87 ~
§ 5.2 Introduction
A relationship exists between skeletal muscle activity and the morphology and composition
of bone (Shaw and Stock, 2009). Contractions of skeletal muscles are believed to have the
most prominent and dynamic role in the habitual loading environment of bone tissue (Burr,
1997; Schoenau and Fricke, 2006). Profound changes in skeletal-muscle recruitment illustrate
this muscle-bone relationship. For example, not only does the playing arm of tennis players
have hypertrophied muscles, its humerus also has a higher bone-mineral density (Kannus et
al., 1994). In addition, the increase in playing-arm muscle size is correlated with the increase
in several bone-strength-indicating parameters (Daly et al., 2004). Conversely, muscle
paralysis has been shown to lead to cortical and trabecular bone mass decrease (Warner et
al., 2006; Poliachik et al., 2010). The muscle-bone relationship might also exist on a more
delicate level; the radius of the arm dominant in habitual everyday activities has a greater
mass and volume than that of the non-dominant arm (MacIntyre et al., 1999). It is unclear,
however, to what extent in time and in amplitude the daily activity of skeletal muscles is
related to the daily loading of bone.
A suitable musculoskeletal system to study the muscle-bone relationship is the
masticatory apparatus. As the mandible is not weight bearing and the gravitational forces
working on it are small, the origin of the daily loads mandibular bone experiences can be
assumed to lie mainly in muscle contractions and the resulting reaction forces. Several
muscle groups insert on the mandible, but the masticatory muscles—due to their strength
and functional relation to the jaw bones—may be considered the most important loaders.
Paralysis of the masseter muscle, for example, results in both its own atrophy and in the
subsequent atrophy, or growth retardation, of the mandible it inserts on (Matic et al., 2007;
Kim et al., 2008).
The role of masticatory muscles in the mechanical loading of the mandible has been
studied predominantly within the context of chewing behaviour using electromyography
together with bone-load sensors (Weijs and De Jongh, 1977; Hylander et al., 1987; Teng and
Herring, 1998). Extensive analyses have been performed on the relation of masticatory-
muscle biopotentials with mandibular strain amplitudes within chewing cycles (Hylander
and Johnson, 1989, 1993; Liu et al., 2004). Outside of these bouts of chewing behaviour the
role of masticatory muscles in the everyday habitual loading of the mandible has been
neglected mostly. Here, we hypothesise that the role of masticatory muscles in the habitual
Chapter 5
~ 88 ~
loading of the mandible might be near-continuous; expanding beyond the boundaries of
mastication. Previous long-term measurements of habitual bone strain in the mandible
revealed the existence of numerous isolated bone-strain events, occurring between bouts of
more cyclic bone loading, which also contribute to the daily bone strain history (De Jong et
al., 2010a, 2010c).
Here we describe the habitual relationship between masticatory muscle activity
and mandibular bone strain, without confining to chewing behaviour. The hypothesis that
daily bone strains are associated mainly with the activity of muscles—in terms of both time
and amplitude—is tested. To this end, co-appearance of muscle activity and bone strain is
analysed from long-term electromyograms of masseter and digastric muscle activity and
simultaneously recorded mandibular bone strain. Also, amplitude distributions of habitual
masseter and digastric activity bursts and bone-strain events are compared. The masseter
muscles are the rabbit’s main jaw closers, whereas the digastric muscles function as jaw
openers (Schumacher and Rehmer, 1960; Weijs and Dantuma, 1981). We, therefore, expect a
relation in time and in amplitude for masseter activity and mandibular strains. Habitual
masseter-burst amplitudes and counts are compared to the co-appearing compressive
principal-strain amplitudes and counts. Digastric activity is expected to elicit measurable
bone strains, but without a relation in amplitude, as jaw opening will not result in reaction
forces as large as during jaw closing.
§ 5.3 Materials and methods
Laboratory animals
Ten adult (~4 months old) male New Zealand white rabbits (Oryctolagus cuniculus) weighing
3.7 ± 0.2 kilograms were used for the experiments. Rabbits were used as they are large
enough to house both a bone-strain and an electromyography transmitter. The animals were
kept in 73 x 73 x 46 cm cages, received food and water ad libitum, daily portions of hay, and a
wooden block that served as an extra gnawing object. Lights were dimmed between 18.00 h
and 6.00 h. The rabbits were allowed at least two weeks of acclimatisation before
implantation of the transmitters. The experiments were approved by the Animal Ethics
Masticatory Muscles and Bone Strain
~ 89 ~
Committee of the Academic Medical Centre of the University of Amsterdam and executed
in accordance with Dutch legislation.
Wireless electromyography (EMG) and bone-surface strain measurement
Masticatory-muscle biopotentials and bone-surface strain were recorded wirelessly using
implantable transmitters (Langenbach et al., 2002; Van Wessel et al., 2006; De Jong et al.,
2010b). An overview of their main features follows below.
Two-channel TL11M2-F20-EET implants from Data Sciences International (DSI, St.
Paul, Minnesota, USA) recorded masseter and digastric muscle biopotentials with two
indwelling electrodes per channel. Each electrode consisted of a silicone-tubed stainless steel
double-helix wire with a diameter of 0.2 mm. The inter-electrode distance once placed in the
sampled muscle was approximately 6 mm and the effective electrode length was 4 mm. The
bipolar recordings were transmitted on a carrier frequency of 455 kHz to nearby DSI
receivers (RMC-1). A DSI Data Exchange Matrix collected the data from the receivers and
stored them onto a computer. The sample frequency was 250 Hz per channel. In five animals
only masseter activity was recorded, in two others only digastric activity, and in three
animals both masseter and digastric activity were recorded. All electrodes were placed
unilaterally, at the left side. In the masseter muscle, electrodes were placed at the antero-
ventral side of the superficial masseter, near the motor end plates (Widmer et al., 1997). In
the digastric muscle, electrodes were placed in the middle of its muscle belly (Figure 5.1).
Variability in the electrode location was kept at a minimum.
A customised MicroStrain V-Link (Williston, Vermont, USA) connected to a
stacked triple-gauge rosette (L2A-06-031WW-350, Vishay, Malvern, Pennsylvania, USA) was
used for the wireless bone-strain measurements. Strain measurements were transmitted on a
carrier frequency of 2.4 GHz to a nearby MicroStrain USB Base Station, which stored the
data on a desktop computer. Bone strain was sampled at a frequency of 617 Hz and
measured in all ten rabbits. The gauge rosette was positioned on the left lateral surface of
the mandibular corpus, anteriorly of the masseter insertion and inferiorly of the molars. The
orientations of the three gauges were rostroventral (A), vertical (B), and caudoventral (C),
with an angle of 45° between gauges A and B and between gauges B and C (Figure 5.1).
Chapter 5
~ 90 ~
Figure 5.1 Schematic drawings of the rabbit skull with some skeletal muscles (top and middle
drawings) and a detail depicting the orientations of the strain gauges (A, B, and C) in the gauge rosette
(bottom drawing). The circles in the top and middle drawings indicate the locations of the pairs of wire
electrodes in the masseter and digastric muscles. The rectangle in the lateral view depicts the location of
the strain-gauge rosette on the mandibular corpus, which in vivo is partly covered by the bulging
masseter muscle.
superficial temporal
posterior deep masseter
posterior superficial masseter
superficial masseter
superficial masseter
medial pterygoid
mylohyoid
stylohyoid
digastric
lateral view
ventral view
stacked triple-gauge rosette detail
A
B
C45° 45°
Masticatory Muscles and Bone Strain
~ 91 ~
Surgical procedure and medications
The day before and the day after the aseptic surgical placement of the two implants, rabbits
received 5.0 mg/kg enrofloxacin (Baytril, Bayer, Mijdrecht, the Netherlands) to suppress
infections. Before surgery, rabbits were administered a subcutaneous dose of 0.03 mg/kg
buprenorphine (Temgesic, Schering-Plough, Utrecht, the Netherlands), an analgesic.
General anaesthesia was started with a subcutaneous dose of 15 mg/kg ketamine (Nimatek,
EuroVet Animal Health, Bladel, the Netherlands) combined with 0.40 mg/kg
dexmedetomidine (Dexdomitor, Orion Pharma, Espoo, Finland). The rabbit’s eyes were
covered with Oculentum Simplex (Pharmachemie B.V., Haarlem, the Netherlands) to
prevent them from dehydrating. Anaesthesia was maintained through intratracheal dosage
of 0.8-1.2 % isoflurane in a 1:1 mixture of oxygen and air. Spirometry and oxymetry
monitored breathing frequency and oxygen saturation of the blood, respectively. Body
temperature was kept at 37 °C using heating pads.
An incision was made in the rabbit’s neck fold through which subcutaneous
pockets were made to house the transmitters. The EMG electrodes and the wired strain-
gauge rosette were led subcutaneously to a second incision in the mandibular region. Here,
the electrodes were placed in either the masseter or the digastric or both muscles, using a
longitudinally-ground hypodermic needle as a slide (Nuijens et al., 1997). Electrodes were
anchored at the muscle surface with a single suture. To attach the strain-gauge rosette, a
mandibular bone-surface area of about 1 cm2 was cleared of the surrounding soft tissues and
periosteum. The bone surface was cleaned with sterile swabs, degreased with an 80 %
ethanol solution, and dried to the air. The gauge rosette was glued to the bone with
Histoacryl (B. Braun, Tuttlingen, Germany) and pressed firmly onto it for several minutes
(Cochran, 1972).
Following surgery, the animal was given a subcutaneous dose of 2 mg/kg
carprofen (Rimadyl, Pfizer Animal Health B.V., Capelle aan den IJssel, the Netherlands) to
suppress inflammation and pain. After collection of the measurements, rabbits were
sacrificed with an overdose of pentobarbital sodium (Euthesate, CEVA Santé Animale,
Maassluis, the Netherlands).
Chapter 5
~ 92 ~
Data analysis
Bone-strain recordings and electromyograms were analysed using the software program
Spike2 (version 5.21, Cambridge Electronic Design Limited, Cambridge, UK). Masseter and
digastric electromyograms were rectified and smoothed by calculating the moving root-
mean-square value over ∆t = 0.040 s. In each recording, the highest biopotential peak served
as the 100 % activity level of the sampled muscle as rabbits cannot be ordered to give a
maximum muscle contraction. All other peaks were expressed as a percentage of that
biopotential. Distribution histograms were made of the EMG-peak amplitudes, or burst
amplitudes, that crossed the 5 % activity level of the recording. Histograms of muscle-burst
amplitudes had a bin width of 2.5 %.
Bone-strain recordings were rid of drift by subtracting the average of all data
points from t - 3600 s to t + 3600 s from each data point at time t. The three drift-free strain-
gauge recordings were used to calculate the compressive and tensile principal-strain signals.
In the sections of the Results describing associations in time between masseter and digastric
muscle bursts and mandibular strain, the tensile principal strain is used in the figures for
clarity purposes (deviations from zero pointing upwards). Distribution histograms were
made of the principal-strain amplitudes of all strain events of which the base of the peak lay
below the threshold of 20 microstrain (µε) and the peak maximum crossed the threshold of
30 µε, safely above noise. These histograms had a bin width of 12.5 µε.
For further analysis of the relation between masseter muscle activity and
mandibular deformations, the compressive principal strain was used as compression at the
site of measurement was expected to have a more clear relation to contractions of the
masseter than tension. For six amplitude levels of compressive principal strain (10 ± 3 µε, 35
± 3 µε, 75 ± 10 µε, 150 ± 10 µε, 300 ± 10 µε, and 500 ± 10 µε) accompanying masseter-burst
amplitudes were collected. Amplitudes of compressive principal strain greater than 500 µε
were very rare and could not be included in the analysis. For each of the strain levels 11
masseter bursts were collected by searching a strain event with the specific amplitude (e.g., -
10 ± 3 µε), writing down the accompanying muscle-burst amplitude, and doing so at 11 time
points divided evenly over the length of the entire measurement per rabbit.
To evaluate whether the masseter muscle plays different roles in more intense
(including feeding-behaviour-related) versus less intense loading of the mandible, the
average number of masseter-muscle bursts per hour was compared to the average number
Masticatory Muscles and Bone Strain
~ 93 ~
of bone-strain events per hour. This comparison was made for two amplitude domains
which represented the more intense and less intense parts of loading. Chewing is a more
intense cyclic masticatory behaviour eliciting compressive principal bone strains with
amplitudes of 149 - 320 µε on the working side of the mandible (Weijs and De Jongh, 1977).
Using the masseter activity levels found with compressive principal strains of 150 ± 10 µε, a
division was made in the total count of masseter bursts above and below the mV level
associated with this compressive principal-strain magnitude for each rabbit. The number of
masseter bursts per strain event was assumed to be an indication of the role of the masseter
in these two ranges of mandibular loading.
To quantify variation in the direction of the principal strains, the angle φ between
the direction of the first principal strain and the orientation of gauge A of the strain-gauge
rosette was calculated for 70 bone-strain events per rabbit. These strain events were
collected from seven sites evenly divided over each mandibular bone-strain recording—
including 10 successive strain events at each site. In this strain-event collection some care
was taken to include larger strain events (i.e., compressive principal strain > 150 µε), which
in practice meant ‘scrolling’ through the strain recordings away from a site to nearby large
strain peaks. The direction of the first principal strain is oriented at an angle of 90° from the
direction of the second principal strain. However, for eight rabbits, we simply used the
angle ϕ (without adding or subtracting 90°) to plot against the second principal-strain
amplitude in scatter distributions. The following formulas were used for the calculation of
angle ϕ and the second principal strain:
� � 12 tan� �2 � � � � � � � � �
� � 12 � � � �� � 12 �� � � ��� � �2 � � � � ���
in which εA, εB, and εC were the drift-removed strain values measured by the individual
gauges A, B, and C from the gauge rosette (Figure 5.1) and ε2 is the second principal strain,
i.e, the compressive principal strain.
The relation between digastric muscle activity and bone strain was too weak and
therefore no such analyses were done for this muscle.
Chapter 5
~ 94 ~
Statistics
The EMG amplitudes co-appearing with the various levels of compressive strain were tested
for differences using two-tailed paired t-tests. Differences in mean EMG amplitude per
compressive-strain level were considered significant when P ≤ 0.05.
§ 5.4 Results
The rabbits recovered quickly from the placement of the two transmitters and started
feeding and exploring as soon as three hours after surgery. Simultaneous telemetric
recordings of masticatory muscle activity and mandibular bone strain were started on the
day of surgery. The average simultaneous recording length of muscle activity and bone
strain was 16.6 ± 6.6 h (n = 10).
Throughout all recordings, longer and shorter bouts of activity of the masseter
muscle coincided clearly with bouts of mandibular bone strain. The time between these
bouts was filled with multitudes of isolated muscle bursts and co-appearing strain events
(Figure 5.2A). The co-appearance was especially pronounced for periods of higher muscle-
activity levels and larger bone-strain amplitudes (> 150 µε), which included chewing
(personal observation, W.C. de Jong). On a smaller time scale the co-appearance of muscle-
activity bouts and strain-event bouts, as well as of the isolated bursts and events, is
illustrated even more clearly (Figure 5.2B). Within bouts there was no correspondence
between the individual muscle-burst amplitudes—in raw or root-mean-squared form—and
the bone strain-event amplitudes (Figure 5.2C). Occasionally, the level of an entire masseter-
activity bout did not correspond at all with the amplitude of the accompanying strain-event
series (Figure 5.3). Between the bouts of more intense repetitive and rhythmic mandibular
loading thousands of isolated strain events occurred, which were almost always
accompanied by masseter muscle bursts (Figure 5.4).
The relation in time between activity of the digastric muscle and mandibular bone
strain was not as pronounced as between the masseter muscle and mandibular bone strain.
There were no clearly delineated bouts of digastric activity and bone strain (Figure 5.5A and
B). A one-on-one co-appearance of digastric bursts and strain events was present only
Masticatory Muscles and Bone Strain
~ 95 ~
Figure 5.2 Representative stretches of unprocessed masseter electromyogram (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
Panels B and C have identical y-axes. Note the co-appearance throughout the recordings of masseter-
activity bouts and strain-event episodes (A and B). This co-appearance persists to the level of individual
muscle bursts and strain events (C). Negative values in the tensile principal strain graphs are an artefact
of the drift-removal procedure which was applied before calculation of the principal strains.
occasionally (Figure 5.5B). A relationship in the amplitudes of co-appearing digastric muscle
bursts and bone-strain events was absent (Figure 5.5C).
In some instances, neither masseter nor digastric activity seemed to have a clear
relation to the simultaneously recorded mandibular strain events (Figure 5.6).
Passages of co-appearing rhythmic masseter muscle bursts and strain events were
manifold for the frequency of 5 Hz (Figure 5.2C), well known as the frequency at which food
is chewed and possibly a frequency used for all sorts of oral behaviours in the rabbit.
Incidentally, masseter muscle bursts were found to coincide with the strain events they
elicited up to frequencies of 15 Hz (Figure 5.7). This illustrates that high-frequency muscular
contractions may cause bone deformations with the same frequency.
6 hrs
8 min 7 s
250 µε
1.5 mV
1.5 mV
A
B C
0
0
0
250 µε
0
Chapter 5
~ 96 ~
Figure 5.3 Two 25-minute examples that include discordances in amplitude between co-appearing
episodes of masseter activity and bone-strain events. The examples in A and B were taken from two
different rabbits. In both A and B the upper graph is the electromyogram (processed with a root-mean-
square function over ∆t = 0.040 s) and the lower graph is the tensile principal bone strain. Horizontal
braces indicate where strain amplitudes are lower compared to those co-appearing with muscle-activity
bouts of the same burst activity level. Negative values in the tensile principal strain graphs are an
artefact of the drift-removal procedure which was applied before calculation of the principal strains.
Note that panels A and B have different y-axes.
Figure 5.4 Representative 5-min stretches of root-mean-squared (∆t = 0.040 s) masseter
electromyograms (upper graphs in A and B) and the simultaneously recorded mandibular tensile
principal strain. Panels A and B were taken from different rabbits. Mandibular bone-strain events,
although outside of cyclic loading bouts, are primarily the result of masseter activity.
A
B
25 min
200 µε
0.4 mV
400 µε
0.3 mV
0
0
0
0
5 min
0.15 mV
0.20 mV
75 µε
75 µε
0
0
0
0
A
B
Fig
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
Panels B and C have identical y
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
Figure
recorded tensile and compressive principal strains. The EMGs are root
Here, neither masseter nor digastric activity corresponds clearly with the bon
although some co
minutes.
Figure
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
Panels B and C have identical y
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
Figure
recorded tensile and compressive principal strains. The EMGs are root
Here, neither masseter nor digastric activity corresponds clearly with the bon
although some co
minutes.
5.5
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
Panels B and C have identical y
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
5.6
recorded tensile and compressive principal strains. The EMGs are root
Here, neither masseter nor digastric activity corresponds clearly with the bon
although some co
minutes.
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
Panels B and C have identical y
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
Two 17
recorded tensile and compressive principal strains. The EMGs are root
Here, neither masseter nor digastric activity corresponds clearly with the bon
although some co
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
Panels B and C have identical y
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
Two 17-
recorded tensile and compressive principal strains. The EMGs are root
Here, neither masseter nor digastric activity corresponds clearly with the bon
although some co-
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
Panels B and C have identical y
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
-min stretches of masseter and digastric electromyograms with the simultaneously
recorded tensile and compressive principal strains. The EMGs are root
Here, neither masseter nor digastric activity corresponds clearly with the bon
-appearance of muscle bursts and bone
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
Panels B and C have identical y
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
in stretches of masseter and digastric electromyograms with the simultaneously
recorded tensile and compressive principal strains. The EMGs are root
Here, neither masseter nor digastric activity corresponds clearly with the bon
appearance of muscle bursts and bone
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
Panels B and C have identical y
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
in stretches of masseter and digastric electromyograms with the simultaneously
recorded tensile and compressive principal strains. The EMGs are root
Here, neither masseter nor digastric activity corresponds clearly with the bon
appearance of muscle bursts and bone
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
Panels B and C have identical y-axes. On a larger time scale (A)
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
in stretches of masseter and digastric electromyograms with the simultaneously
recorded tensile and compressive principal strains. The EMGs are root
Here, neither masseter nor digastric activity corresponds clearly with the bon
appearance of muscle bursts and bone
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
axes. On a larger time scale (A)
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
in stretches of masseter and digastric electromyograms with the simultaneously
recorded tensile and compressive principal strains. The EMGs are root
Here, neither masseter nor digastric activity corresponds clearly with the bon
appearance of muscle bursts and bone
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
axes. On a larger time scale (A)
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
in stretches of masseter and digastric electromyograms with the simultaneously
recorded tensile and compressive principal strains. The EMGs are root
Here, neither masseter nor digastric activity corresponds clearly with the bon
appearance of muscle bursts and bone
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
axes. On a larger time scale (A)
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
in stretches of masseter and digastric electromyograms with the simultaneously
recorded tensile and compressive principal strains. The EMGs are root
Here, neither masseter nor digastric activity corresponds clearly with the bon
appearance of muscle bursts and bone
~
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
axes. On a larger time scale (A)
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
in stretches of masseter and digastric electromyograms with the simultaneously
recorded tensile and compressive principal strains. The EMGs are root
Here, neither masseter nor digastric activity corresponds clearly with the bon
appearance of muscle bursts and bone
~ 97
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
axes. On a larger time scale (A)
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
in stretches of masseter and digastric electromyograms with the simultaneously
recorded tensile and compressive principal strains. The EMGs are root
Here, neither masseter nor digastric activity corresponds clearly with the bon
appearance of muscle bursts and bone
97 ~
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
axes. On a larger time scale (A)
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
in stretches of masseter and digastric electromyograms with the simultaneously
recorded tensile and compressive principal strains. The EMGs are root
Here, neither masseter nor digastric activity corresponds clearly with the bon
appearance of muscle bursts and bone
Masticatory Muscles and Bone Strain
~
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
axes. On a larger time scale (A)
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
in stretches of masseter and digastric electromyograms with the simultaneously
recorded tensile and compressive principal strains. The EMGs are root
Here, neither masseter nor digastric activity corresponds clearly with the bon
appearance of muscle bursts and bone-strain events can be seen in the first six
Masticatory Muscles and Bone Strain
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
axes. On a larger time scale (A)
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
in stretches of masseter and digastric electromyograms with the simultaneously
recorded tensile and compressive principal strains. The EMGs are root
Here, neither masseter nor digastric activity corresponds clearly with the bon
strain events can be seen in the first six
Masticatory Muscles and Bone Strain
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
axes. On a larger time scale (A) some relation in time between digastric
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
in stretches of masseter and digastric electromyograms with the simultaneously
recorded tensile and compressive principal strains. The EMGs are root
Here, neither masseter nor digastric activity corresponds clearly with the bon
strain events can be seen in the first six
Masticatory Muscles and Bone Strain
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
some relation in time between digastric
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
in stretches of masseter and digastric electromyograms with the simultaneously
recorded tensile and compressive principal strains. The EMGs are root-mean
Here, neither masseter nor digastric activity corresponds clearly with the bon
strain events can be seen in the first six
Masticatory Muscles and Bone Strain
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
some relation in time between digastric
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
in stretches of masseter and digastric electromyograms with the simultaneously
mean
Here, neither masseter nor digastric activity corresponds clearly with the bon
strain events can be seen in the first six
Masticatory Muscles and Bone Strain
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
some relation in time between digastric
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
in stretches of masseter and digastric electromyograms with the simultaneously
mean-squared (∆t = 0.040 s).
Here, neither masseter nor digastric activity corresponds clearly with the bone-
strain events can be seen in the first six
Masticatory Muscles and Bone Strain
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
some relation in time between digastric
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
in stretches of masseter and digastric electromyograms with the simultaneously
squared (∆t = 0.040 s).
-strain recording,
strain events can be seen in the first six
Masticatory Muscles and Bone Strain
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
some relation in time between digastric
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
in stretches of masseter and digastric electromyograms with the simultaneously
squared (∆t = 0.040 s).
strain recording,
strain events can be seen in the first six
Masticatory Muscles and Bone Strain
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
some relation in time between digastric
activity and mandibular bone strain can be detected. On smaller time scales (B and C), co-appearance of
digastric bursts and strain events can also be seen, but there is no relation in amplitude.
in stretches of masseter and digastric electromyograms with the simultaneously
squared (∆t = 0.040 s).
strain recording,
strain events can be seen in the first six
Masticatory Muscles and Bone Strain
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
some relation in time between digastric
appearance of
in stretches of masseter and digastric electromyograms with the simultaneously
squared (∆t = 0.040 s).
strain recording,
strain events can be seen in the first six
Masticatory Muscles and Bone Strain
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
some relation in time between digastric
appearance of
in stretches of masseter and digastric electromyograms with the simultaneously
squared (∆t = 0.040 s).
strain recording,
strain events can be seen in the first six
Masticatory Muscles and Bone Strain
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
each time window) and tensile principal bone strain (lower graphs). mV = millivolt, µε = microstrain.
some relation in time between digastric
appearance of
in stretches of masseter and digastric electromyograms with the simultaneously
squared (∆t = 0.040 s).
Masticatory Muscles and Bone Strain
Representative stretches of unprocessed digastric electromyograms (EMG, upper graphs in
some relation in time between digastric
appearance of
A
B
150
0.7
A
B
20
0.6
150 µε
0.7 mV
20 µε
0.6 mV
0
0
0
0
0
0
0
0
9 min9 min
CC
10 s
3 hrs
10 s
3 hrs
Chapter 5
~ 98 ~
Figure 5.7 Two 5-s example recordings of high-frequency force transmission. Note that the amplitude scales differ between panels A and B. The examples were taken from two different rabbits. In both A and B the upper graphs are raw masseter electromyograms, used here as the root-mean-square function mostly removes high-frequency content, and the lower graphs are the tensile principal strain. In A the masseter muscle strains the mandible at a frequency of 8 Hz and in B the masseter muscle strains the mandible at a frequency of 15 Hz. mV = millivolt, µε = microstrain.
In most rabbits, significantly increasing masseter-burst amplitudes were found with larger
compressive principal-strain amplitudes (Table 5.1). However, masseter bursts eliciting
compressive principal strains of 500 µε were not larger than those co-appearing with
compressive principal strains of 300 µε (Table 5.1). Above and below the masseter muscle
activity level associated with the principal-strain amplitude of -150 µε, the burst-number-to-
strain-event ratio was the same (Table 5.2). On average, per hour, three times more masseter
bursts were detected above the 5 % activity level than strain events above the 30 µε level.
The interindividual variation was large, however, and in one rabbit 10 times more masseter
bursts than strain events were registered, both above and below the -150 µε level.
5 s
masseter EMG
masseter EMG
bone strain
bone strain
f = 8 Hz
f = 15 Hz
70 µε
0.3 mVA
B0
0
60 µε
0.2 mV
0
0
Masticatory Muscles and Bone Strain
~ 99 ~
Figure 5.8 Average amplitude distributions of habitual masseter muscle bursts (n = 8), digastric muscle
bursts (n = 5), and bone-strain events (n = 10). µε = microstrain. Note that the y-axes have log scales. The
thin bars indicate the standard deviations. Per hour, there are more masseter bursts above the 20 %
activity level than digastric bursts. Negative strain amplitudes refer to compressive strain.
Table 5.1 Masseter burst amplitudes, from EMGs root-mean-squared over ∆t = 0.040 s, co-appearing
with amplitudes of compressive principal bone strain. Masseter activity is expressed as a percentage of
the peak burst voltage. Shown are means ± standard deviations (SD) of 11 muscle bursts per bone-strain
amplitude per rabbit. A ‘-‘ indicates that not enough strain events were found for that specific
amplitude level. µε = microstrain.
individual compressive principal-strain amplitude level [µε]
10 35 75 150 300 500
mas
seter muscle activity ±
SD
[% of pea
k voltag
e]
1 5.5 ± 2.7 6.1 ± 1.1 16.9 ± 7.5* 29.3 ± 6.8* 41.0 ± 8.4* 44.3 ± 10.1
2 3.8 ± 2.0 11.1 ± 5.8* 19.4 ± 6.9* 14.9 ± 3.8 33.4 ± 5.5* 27.9 ± 6.2
3 2.0 ± 1.6 6.5 ± 2.5* 5.4 ± 3.3 - - -
4 3.2 ± 1.5 9.4 ± 5.6* 19.8 ± 11.0* 40.9 ± 12.1* 48.9 ± 14.0 -
5 4.3 ± 1.3 14.2 ± 3.1* 13.3 ± 4.6 18.2 ± 6.6* 27.2 ± 7.5* 32.3 ± 5.1
6 7.1 ± 4.6 32.8 ± 10.1* 54.5 ± 21.8* 50.6 ± 9.6 - -
7 5.3 ± 3.7 12.8 ± 5.4* 37.5 ± 14.8* 75.0 ± 12.3* - -
8 5.3 ± 2.8 9.0 ± 3.5* 15.6 ± 3.7* 28.0 ± 6.5* - -
mean ± SD 4.5 ± 1.6 12.7 ± 8.6 22.8 ± 15.7 36.7 ± 20.9 37.6 ± 9.4 34.8 ± 8.5
* Significantly larger than the EMG amplitudes from that rabbit accompanying the first lower bone
compression level; P < 0.05.
1
10
100
1000
10000
8 20 33 45 58 70 83 95
bursts/ hour
% of peak voltage
1
10
100
1000
10000
8 20 33 45 58 70 83 95
bursts/ hour
% of peak voltage
1
10
100
1000
-500 -375 -250 -125 0 125 250 375 500
events/ hour
principal strain amplitude [µε]
masseter activity
n = 8
digastric activity
n = 5
bone-strain events
n = 10
Chapter 5
~ 100 ~
Distribution histograms of the amplitudes of masseter and digastric activity bursts and of
bone-strain events displayed an exponential decrease in occurrence of larger amplitudes,
but there was no clear resemblance between the muscle-burst and bone-strain amplitude
distributions (Figure 5.8). Compared to the digastric muscle, masseter muscle activity
contained more bursts for amplitudes above 20 % of the peak voltage. Using the
compressive principal bone strain, more strain events could be detected above the 30 µε
level, as evidenced by the larger area occupied by the event counts on the negative, i.e.,
compression amplitude half of the histogram compared to the positive, i.e., tension
amplitude half.
Greater amplitudes of compression were related to more constant values for the
principal-strain orientation (Figure 5.9). In most rabbits there was a tendency for angle ϕ to have values between 20 - 30° for second principal-strain amplitudes below -150 µε.
Therefore, the direction of the second principal strain was more horizontal than the
orientation of gauge C when compression amplitudes exceeded the 150 µε level.
Table 5.2 Counts per hour of compressive strain events below and above the level of 150 µε, and
masseter-muscle bursts below and above the mV level causing a compressive principal strain of 150 µε.
Only strain events with amplitudes greater than 30 µε and muscle bursts above the 5 % activity level are
included in the counts (see Material and methods section). In individual 3, no distinction could be made
in the masseter bursts as there were not enough large strain events to measure the masseter burst level
causing a compressive principal strain of 150 µε (see Table 5.1). µε = microstrain, mV = millivolt.
individual events/ h
≤ 150 µε
bursts/ h
≤ mV150 µε
bursts/
events
events/ h
> 150 µε
bursts/ h
> mV150 µε
bursts/
events
1 1462 1440 1.0 213 277 1.3
2 981 496 0.5 130 257 2.0
3 159 - - 4 - -
4 512 757 1.5 103 207 2.0
5 586 1117 1.9 254 541 2.1
6 322 3094 9.6 8 81 10.1
7 769 4771 6.2 6 8 1.3
8 665 656 1.0 22 41 1.9
mean ± SD 3.1 ± 3.5 3.0 ± 3.2
Masticatory Muscles and Bone Strain
~ 101 ~
Figure 5.9 Scatter distributions of the angle ϕ plotted against the second principal-strain amplitude.
Each dot indicates one bone-strain event. Positive angles are oriented counter clockwise from the
rostroventrally orientated gauge A, negative angles clockwise. The numbers in the lower left corners of
each graph indicate the rabbit individuals. Note the tendency of ϕ to have more constant values with
increasing amplitude of bone compression.
-40
-20
0
20
40
-400 -300 -200 -100 0
-40
-20
0
20
40
-400 -300 -200 -100 0
-40
-20
0
20
40
-400 -300 -200 -100 0
-40
-20
0
20
40
-400 -300 -200 -100 0
-40
-20
0
20
40
-400 -300 -200 -100 0
-40
-20
0
20
40
-400 -300 -200 -100 0
-40
-20
0
20
40
-400 -300 -200 -100 0
-40
-20
0
20
40
-400 -300 -200 -100 0
second principal strain ε2 [µε]
angle Φ
[ °]
# 8# 7
# 1 # 2
# 3 # 4
# 5 # 6
Chapter 5
~ 102 ~
§ 5.5 Discussion
Our measurements reveal masseter muscle contractions to be a primary contributor to the
ongoing loading history of the rabbit mandible. The role of the masseter muscle was not
confined to bouts of more intense cyclic loading, which include chewing, but also comprised
thousands of isolated loading events with amplitudes mostly smaller than those of the bouts
of cyclic loading. Masseter electromyograms greatly resembled mandibular bone-strain
recordings in terms of co-appearing muscle bursts and strain events throughout entire
recordings. However, the average number of masseter bursts per hour was greater than the
average number of bone strain events per hour (Table 5.2). One explanation is the exclusion
from our analysis of strain events with principal amplitudes smaller than 30 µε, although
this does not explain the larger number of more intense masseter bursts compared to the
number of strain events with principal amplitudes greater than 150 µε. It is possible that not
all registered masseter bursts resulted in a measurable mandibular bone strain.
Occasions where bone-strain events were not accompanied by a masseter activity
burst were rare. Both larger and smaller bone-strain events featured co-appearing masseter
bursts, almost without exception, suggesting equal roles of the masseter muscle in both
high-intensity and low-intensity loading. Greater amplitudes of mandibular bone strain
were related to both greater amplitudes of masseter activity and to a more constant
orientation of the principal-strain directions. During large-amplitude loading events the
direction of the second principal strain in the surface of the mandibular corpus was aligned
more horizontally. This could mean that the working line of the masseter muscle becomes
more constant when the muscle exerts larger forces. This, however, is disputable as no other
jaw-closing muscles were sampled and their contribution to larger strain events is unknown.
Other masticatory muscles than the masseter and the digastric will load the
mandible as well, but no electromyograms were made of these muscles. Although the loads
they exert on the mandible may cause strain events not accompanied by a registered
masseter burst, the majority of their contractions are likely paralleled by the activity of the
sampled masseter muscle. Especially during chewing, masticatory muscles primarily work
in triplets: the masseter and medial pterygoid muscles of one side and the temporal muscle
of the contralateral side (Langenbach and Van Eijden, 2001). Although chewing is the main
function of the masticatory apparatus, the daily loading history of the mandible includes
much more than the short bouts of this behaviour. In all these oral behaviours the masseter
Masticatory Muscles and Bone Strain
~ 103 ~
muscle seems to play a main role as indicated by the close fit between its activity and the
mandibular bone strain throughout the day.
An amplitude relation between masseter activity and mandibular strain was
present only on a coarse scale, evidenced by the visually matching amplitudes of complete
bouts of muscle activity and bone strain and the increasing EMG amplitudes found for
increasing compressive bone-strain levels. On a fine amplitude scale, amplitudes of
individual masseter bursts were unrelated to those of their strain-event counterparts. This
can be explained firstly by bone deformation being the result of several loads, of which
masseter activity is only one. The activity of the other masticatory muscles, the facial
muscles, the suprahyoid muscles, as well as additional reaction forces from incisors, molars,
and temporomandibular joints will load the mandible also. Secondly, concerning chewing
bouts, the level of activation of each of the masticatory muscles and their exact activation
pattern in time will vary from cycle to cycle, as the position and mechanical properties of the
masticated food will change continuously (Morimoto et al., 1985). In Figure 5.3, the
discordance of masseter EMG amplitudes and bone-strain amplitudes of complete activity
bouts might simply be the result of a switch of working side and balancing side during
mastication. Thirdly, we sampled only the superficial part of the masseter muscle. As the
rabbit masseter is extremely compartmentalised by aponeuroses (Schumacher and Rehmer,
1960; Weijs and Dantuma, 1981; Widmer et al., 1997), the magnitudes and directions of its
contractions cannot always be captured by one or two EMG channels. Obviously, reaction
forces on the mandible from outside the rabbit—which would occur when the animal were
to, e.g., scratch its head—might also have caused bone-strain events. Video registrations of
the laboratory animal might have explained the behaviour behind some of those events.
However, earlier attempts to film rabbit behaviours made clear that many activities of the
masticatory muscles were simply invisible from the outside of the animal.
Amplitudes of digastric muscle activity resembled very weakly or not at all those
of mandibular bone strain. Digastric muscles are jaw openers and jaw opening generally
does not need large muscle forces (Weijs and Muhl, 1987), nor does it bring about large
reaction forces. The reaction forces that are present during opening arise from passive
tensions in the soft tissues that cover the mandible and from the loads in the jaw joints.
These loads are small and far away from the site of strain measurement and will therefore
only elicit small bone strains near and underneath the gauge rosette. In contrast, the
masseter is active mainly when the mandible cannot close any further, which results in
Chapter 5
~ 104 ~
larger bone-strain amplitudes. In addition, digastric muscles have small cross-sectional
areas and lower weights compared to the masseter and pterygoid muscles (Weijs and
Dantuma, 1981; Langenbach and Weijs, 1990) and, consequently, can exert only smaller
maximal forces on the mandible. Situations in which the digastric muscles are more active
than the masseter muscles, such as during grooming and limb licking (Yamada et al., 1993),
could have given rise to instances of better resemblance between digastric activity and
mandibular bone strain.
The data presented in this paper illustrate that the mechanical link between jaw-
muscle activity and loading of the mandibular bone is strong. This strong mechanical link
might explain the known functional relation between jaw-muscle activity and mandibular
bone growth, modelling, and maintenance. During growth in utero the presence of active
masticatory muscles is known to be essential to a proper shaping of the mandible (Rot-
Nikcevic et al., 2006). Impaired force output of masticatory muscles during post-natal
growth results in a retarded mandibular bone growth as well (Kwon et al., 2007; Matic et al.,
2007). In adulthood, the functionality of the mechanical relation between masticatory muscle
activity and mandibular bone morphology remains. Botulinum-toxin treatment of the
masseter muscle in adult rats, e.g., induces architectural changes in the mandible (Tsai et al.,
2010). As injection of botulinum toxin type A into the masseter muscle is a procedure
performed more and more, either for aesthetic (Kim et al., 2010; Wu, 2010) or medical
purposes (Daelen et al., 1997; Tan and Jankovic, 2000), this might be of some consideration
to the clinic.
Low-magnitude, high-frequency mechanical loads have been associated with
anabolic effects on bone (Rubin et al., 2001; Midura et al., 2005; Goodship et al., 2009). Our
data unveil that masticatory muscle bursts at 5 % of peak activity are associated with small
strains in the mandibular bone (Table 5.1). We found that masseter and digastric bursts at
that activity level may take place at least 1000 times per hour (Figure 5.8 and Table 5.2),
which is in accordance with earlier publications (Van Wessel et al., 2005). Also, the
frequency component of muscle activity is still very strong above 5 Hz and even 15 Hz force
transmissions to bone were detected (Figure 5.7). Therefore, the present study supports the
possibility that part of all habitually occurring high-frequency bone strains might have their
origin in muscle activity and that these strains quite possibly stimulate homeostatic bone
turnover (Rubin et al., 1990; Turner et al., 1995; Fritton et al., 2000; Judex and Rubin, 2010).
Masticatory Muscles and Bone Strain
~ 105 ~
This study demonstrates that wireless and simultaneous measurement of muscle activity
and bone-surface strain in vivo is feasible for middle-sized and larger animals up to about
one day. However, our methodology has limitations. Firstly, muscle activity and bone strain
were recorded with two separate systems. Due to minute periods of signal dropout and
variation in hardware clock rates the two signals could not always be synchronised.
Secondly, the synchronisation of the strain recordings and electromyograms was performed
visually. Although a matching between a series of muscle-activity bursts and bone-strain
events can be attained fairly easily, the exact relation in time of an individual pair of one
muscle burst and the subsequent bone-strain event could not be studied objectively.
Excitation-contraction lag times are known to be short for jaw-closing muscles, though,
commonly featuring values from ~13 ms to peak twitch tension in the cat masseter (Taylor
et al., 1973), to ~30 ms in the macaque masseter (Hylander and Johnson, 1993), to ~43 ms in
the pig temporal muscle (Teng and Herring, 1998). An implantable transmitter with sensors
able to capture both muscle biopotentials and bone deformation would be more effective in
quantifying the role of muscle activity in the daily habitual loading of bone.
To conclude, our results reveal that in the masticatory apparatus of the rabbit, jaw muscles
play the main role in the ongoing habitual loading of the mandible. Not only is the mandible
loaded by jaw muscles during repetitive behaviours, like chewing, but also almost
continuously throughout the day outside of these cyclic bouts. Most bone-strain events are
accompanied by masseter-muscle activity. Activity of the digastric muscle corresponds only
weakly with the occurrence of mandibular strain events. A relation in masseter
electromyogram amplitudes and bone-strain amplitudes exists on a coarse scale.
Furthermore, muscle forces can dynamically strain the mandible up to frequencies of ~15
Hz. The orientation of the principal strains becomes more constant with increasing strain
amplitude. This might indicate that the muscles loading the mandible during such high-
intensity events have more constant working-line directions during larger force output.
Chapter 5
~ 106 ~
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