ARTICLE IN PRESS

Journal of Biomechanics 43 (2010) 1667–1673

Contents lists available at ScienceDirect

journal homepage: www.elsevier.com/locate/jbiomech

Journal of Biomechanics

0021-92

doi:10.1

n Corr

Unite d

Tel.: +3

E-m

peyron@

www.JBiomech.com

Development and validation of a mastication simulator

A. Woda a,b, A. Mishellany-Dutour a,c, L. Batier d, O. Franc-ois a, J-P. Meunier c, B. Reynaud e,M. Alric c, M-A. Peyron f,n

a Clermont Universite, Universite d’Auvergne, EA 3847, Deficiences incapacites et desavantages en sante orale, BP 10448, F-63000 Clermont-Ferrand, Franceb CHU Clermont-Ferrand, Service d’Odontologie, F-63001, Clermont-Ferrand, Francec Clermont Universite, Universite d’Auvergne, ERT 18, Conception ingenierie et developpement de l’aliment et du medicament, BP 10448, F-63000 Clermont-Ferrand, Franced Poly’Tech, avenue des Landais, F-63170 Aubi�ere, Francee Nestle Research Center, PO Box 44, CH-1000 Lausanne 26, Switzerlandf INRA, UMR 1019, UNH, CRNH Auvergne, F-63000 Clermont-Ferrand, France; Clermont Universite, Universite d’Auvergne, Unite de Nutrition Humaine, BP 10448, F-63000

Clermont-Ferrand, France

a r t i c l e i n f o

Article history:

Accepted 4 March 2010More and more research are being done on food bolus formation during mastication. However, the

process of bolus formation in the mouth is difficult to observe. A mastication simulator, the Artificial

Keywords:

Mastication

Simulator

Food bolus

Chewing

Engineering

90/$ - see front matter & 2010 Elsevier Ltd. A

016/j.jbiomech.2010.03.002

esponding author at: INRA Institut National d

e Nutrition Humaine, 63122 Saint-Gen �es-Cha

3 04 73 17 73 84; fax: +33 04 73 17 73 88.

ail addresses: marie-agnes.peyron@clermont.i

clermont.inra.fr (M.-A. Peyron).

a b s t r a c t

Masticatory Advanced Machine (AM2) was developed to overcome this difficulty and is described here.

Different variables can be set such as the number of masticatory cycles, the amplitude of the

mechanical movements simulating the vertical and lateral movements of the human lower jaw, the

masticatory force, the temperature of the mastication chamber and the injection and the composition of

saliva. The median sizes of the particles collected from the food boluses made by the AM2 were

compared with those of human boluses obtained with peanuts and carrots as test foods. Our results

showed that AM2 mimicked human masticatory behavior, producing a food bolus with similar

granulometric characteristics.

& 2010 Elsevier Ltd. All rights reserved.

1. Introduction

Mastication transforms a food into a bolus suitable forswallowing (Lillford, 1991; Prinz and Lucas, 1995; Woda et al.,2006). Mastication also forms the first step in the digestionprocess. Direct evidence is lacking, but there are some clues thatpoor mastication is linked to poor nutrition and poor generalhealth (Morais et al., 2003; Ngom and Woda, 2002; Sheiham et al.,2001). Despite its importance, the process of bolus formation isunder-researched. For example, the physical and chemicalproperties of food change as it is transformed into a bolus, andthe mass exchange during mastication are unknown.

Studying the food bolus is hampered by the mere fact that itsformation occurs inside the mouth. A few artificial mouthssimulating mastication have been developed. Only one of these(Salles et al., 2007) allows the control and setting of some of themasticatory variables described in the literature (Peyron et al.,2002; Woda et al., 2006). Another one allows several variables tobe replicated, but only for the first bite (Meullenet and

ll rights reserved.

e la Recherche Agronomique,

mpanelle, France.

nra.fr,

Gandhapuneni, 2006). Most of the existing prototypes usecompressive forces with teeth that have anatomical shapes.However, the complex shapes of natural teeth are operantbecause of the action of the peripheral and central nervoussystems involving sophisticated feedback loops based on theperiodontal, muscular and mucosal receptors that control muscleactivities. In most machines only one functional variable, e.g.,speed, deformation or piston movement, can be controlled at atime. This is so for the texturometers of General Foods (Friedmanet al., 1963) and INRA (Sale et al., 1984) and other tools (Olthoffet al., 1984; Wang and Stohler, 1990; Slagter et al., 1992; Peyronet al., 1994; Heintze and Cavalleri, 2006). Many devices aredesigned to measure the flavour release from foods duringchewing (Nassl et al., 1995; Van Ruth et al., 1995). Othersoriented towards mechanical properties make no attempt toreproduce the conditions in which foods are prepared within aclosed mouth (Hoebler et al., 2002; Usui et al., 2003; Conservaet al., 2008). Mathematical models have also been proposed (Katoet al., 1988; Peleg and Normand, 1982; Van der Bilt et al., 1992;Daumas et al., 2005; Pap et al., 2005).

A new simulator, the Artificial Masticatory Advanced Machine(AM2) has been developed.1 Its purpose was to simulate the result

1 License 0706519 – 2007/17/09; http://masticateur.u-clermont1.fr/.

ARTICLE IN PRESS

A. Woda et al. / Journal of Biomechanics 43 (2010) 1667–16731668

of mastication, i.e. to produce a food bolus with properties similarto those produced by natural mastication, and not to duplicate theanatomical features of the teeth and mouth. However, the basickinetic characteristics of jaw movement were mimicked.

The pre-swallow bolus is characterised by a specific particlesize distribution that is similar across individuals (Lucas and Luke,1986; Peyron et al., 2004; Mishellany et al., 2006; Jalabert-Malboset al., 2007). This narrow variability may be explained by the vitalneed to reach a required pre-swallow bolus state because of thedanger of swallowing an unprepared bolus (Anderson, 1977). Theimportance of obtaining an adequate particle size explains whygranulometry has to date been by far the most frequently usedmeasure of bolus conformity although the rheological propertiesare also important (Coster and Schwartz, 1987). Normal mastica-tion was recently described using an indicator based on the pre-swallow bolus particle size (Woda et al., 2010). Accordingly, inthis study a calibration–validation procedure was based oncomparison between the particle size values of food bolusesobtained in subjects with good masticatory apparatus and thoseobtained with the AM2.

2. Materials and methods

2.1. Biomechanical principles for reproduction of human jaw movements and

teeth action

Jaw movement properties have been extensively analysed (Koolstra et al.,

1988;Gallo et al., 1997). The purpose of our project was not to reproduce the

continuously changing three-dimensional movements during mastication, but

rather the action of teeth on food. Thus to simulate basic jaw kinematics, we

focused on a simple kinetic model (Salaorni and Palla, 1994). We combined a

translational and a rotational movement in the machine, since they co-occur in the

mouth (Posselt, 1952).

Movement of the lower jaw during human mastication can be described as a

repetition of many cycles (�10–60), each stroke being composed of a vertical

opening and a vertical closing movement causing food compression between teeth.

Fig. 1. General view of the AM2 with the opened mastication chamber represented up

chamber are formed by the stationary ‘‘maxillary disk’’ (14) and the moving ‘‘mandibula

the central axis of the cylinder. 1: Frame. 2: Mastication chamber. 3: Fixed jaw sea

5: Mastication chamber plug for food introduction. 6: Heater regulating the inside t

Translation ball screw spindle. 11: Translation motor. 12: Rotation motor. 13: Moving

Simultaneously the jaw makes a lateral movement, which applies a shear stress to

the food. In the AM2, the vertical and lateral movements are obtained by translation

and rotation of a piston actuated by two computer-controlled motors (Fig. 1).

Fully functional dental arches are mostly observed in anthropological studies

in individuals from non-Western societies who display markedly worn teeth

(Kaidonis, 2008) with flattened chewing surfaces. In these subjects, chewing is

performed by confronting upper and lower flat occlusal surfaces. During the

occlusion, the lower molars slide against the upper molars through continuous

movement mostly directed forward and inward (Woda et al., 1979; Morel et al.,

1991). We thus did not take into account the shape of natural teeth, but only the

continuous chewing surface made, in each hemi-arch, by the five cheek teeth.

2.2. Description and functioning of the apparatus

In the human mouth, food undergoes shearing and compressive forces

between the opposing tooth arcades (Strait, 1997). The food particles are gathered

up by accurate, synchronised movements of the tongue, cheeks and lips. In the

AM2, these two actions are performed by two identically shaped surfaces (Fig. 2A)

whose active masticatory surface area is similar to the summed masticatory

surface areas of three contiguous premolar and molar teeth (170 mm2). During

continuous rotation, the surfaces of the mandibular disk meet the maxillary disk in

the three different positions (Fig. 2B to D). In position B, each active masticatory

surface meets the base of the opposing disk, applying compressive forces. In

position C, the active surfaces of the mandibular disk meet the active surfaces of

the maxillary disk, the bevelled edge of the masticatory surfaces sliding over their

opposing counterparts. When the mandibular disk meets the maxillary disk, it

applies a force on it, pressing it back against the spring fitted behind it. Thus the

force generated during the stroke depends on the stiffness of the spring. The

amplitude of the retraction of the maxillary disk is equal to the height of the active

masticatory surfaces. In this position, shear forces are applied that depend on the

strength of the spring, which can be varied by changing the spring. In position 2D,

the active masticatory surfaces are opposed and the spring is maximally

compressed. Every tooth stroke travels through positions B, C and D on the way

up, and then C and B again on the way back down. Position B allows the gathering

and transport of food particles towards the active masticatory surfaces where they

are crushed. In position B, there is a gap between the two disk bases, which

corresponds to the maximal void volume of the mouth (�15 cm3) during chewing.

A general view of the AM2 is given in Fig. 1. Three operating modes can be

selected. In the continuous mode, the number of tooth strokes/minute depends on

the uniform rotation speed. In the alternate mode, the rotation of the disk stops after

each stroke and an optic sensor re-sets the disk to position A (Fig. 2). In this mode

per left. The masticatory chamber (2) is a cylindrical cavity. The two ends of the

r disk’’ (13). The mandibular disk can move back and forth along and rotate around

t from which the bolus is extracted after opening. 4: Fixed jaw locking clamp.

emperature. 7: Saliva injection port. 8: Transmission shaft. 9: Force sensor. 10:

mandibular disk. 14: Stationary maxillary disk.

ARTICLE IN PRESS

A. Woda et al. / Journal of Biomechanics 43 (2010) 1667–1673 1669

the mandibular masticatory surface slides over the maxillary masticatory surface

only once per stroke (positions B and C). In the pressure mode the mandibular disk

acts by pressing against the maxillary jaw through a purely translational movement.

Electronics and a computer program control the many variables that enable

eaters to adjust their mastication to food properties. The main variables that may

influence the masticatory process are: number of strokes, duration of the

masticatory sequence from food intake to swallowing, amplitude of the masticatory

force, amplitude of the opening movement of the lower jaw, amplitude of the lateral

movement of the lower jaw and stroke frequency during the masticatory sequence.

Temperature and saliva production are also factors that can be simulated in the

artificial oral cavity. Artificial saliva (Hutteau and Mathlouthi, 1998; Van Ruth et al.,

1995) is injected through an opening (7 in Fig. 1) placed away from the masticatory

space, in a small spurt (about 0.05 ml) when the mandibular disk is in its most

retracted position during the stroke. The values of saliva flow range from 0.5 to

5 ml/min (Ben-Aryeh et al., 1986). The control of the AM2, performed in a closed

feedback loop design, is shown schematically in Fig. 3.

2.3. In vivo experiment

Young male (n¼15) and female (n¼15) subjects were recruited (22–29 years).

The inclusion criteria were: healthy complete dentition except for third molars,

normal maxillo-mandibular relationship, no previous orthodontic treatment, no

pharmacological drug liable to modify salivary secretion, no allergy to the

System links:

Computer Logic controller : Ethernet connexion . AM2 driving : parameters transComputer Force sensor : Analog acquisition .Logic controller Translation drive : Motor driving (closed loop ) « axis commandLogic controller Translation drive : serial link RS 232 (drive supervising ).Logic controller Rotation drive : Motor driving (closed loop) « axis command ».Logic controller Rotation drive : serial link RS 232 (drive supervising ).Logic controller Pump control unit : serial link RS 232 – pump driving .Logic controller Temperature controller : Serial link RS 232. Temperature contro

Analog acquisition

Ethernet connexion

PCDigital I/O

Serial ports server

RS-232

RS-232

Fig. 3. Schematic representat

Fig. 2. Maxillary and mandibular disks shown in the differe

test-foods, no pain in the area (temporo-mandibular joint and masticatory

muscles), no bruxism and no removable dentures. Crowns, bridges and other

fixed restorations were accepted when limited.

Portions were five nuts (3.5 g) and samples of raw carrots (height 1 cm,

diameter 2 cm, 4 g). There were three sessions. Session 1 was used for training,

during which the subjects chewed eight samples of each food. The first two

samples were swallowed to train the subjects to feel the time for a normal

swallow. The six other samples were used to train them to expectorate when the

swallowing time was reached. In session 2, the subjects also chewed eight samples

of each food, but the last two boluses of each food were kept for particle size

analysis. For the two swallowed samples, the experimenter counted the number of

masticatory cycles. The masticatory sequence ended when the subjects raised

their hand to signal they were ready to expectorate. The number of cycles obtained

during these two sequences was averaged and considered as the mean value until

swallowing. In session 3, the subjects were asked to deliver two boluses for

particle size analysis, one expectorated after 20 cycles and the other after 10

cycles. This protocol complies with the Declaration of Helsinki. It was approved by

the local Ethics Committee, and the subjects gave their informed written consent.

2.4. Particle size determination

The in vivo and in vitro boluses were characterized by their d50, the theoretical

sieve through which 50% of the particle weight could pass (Van der Bilt et al.,

fer & driving.

».

ller driving .

Drive Translation

Drive Rotation

Axis

com

man

d

Dig

italI

/O

CPJForce sensor

Dig

italI

/O

S-HDPump control

unit

RS

-232

Dig

italI

/O

Temperature controller

RS

-232

Dig

italI

/O

Programmable Logic Controller

Axi

sco

mm

and

Dig

italI

/O

ion of the AM2 controls.

nt positions during operation (see explanation in text).

ARTICLE IN PRESS

A. Woda et al. / Journal of Biomechanics 43 (2010) 1667–16731670

1993; Ngom et al., 2007). Expectorated and in vitro boluses were rinsed through a

100 mm sieve in running water and placed in an incubator (UFE 400–800,

Memmert, Germany) at 37 1C for 1 h (carrots) or 2 h (peanuts). The dried particles

were spread on a transparent plastic sheet and a scan shot taken (Epson Perfection,

4990 Photo). Computerized image analysis (Powdershapes, Innovative Sintering

Technologies, Ltd., Switzerland) then yielded the d50 of the particle size

distribution.

0

1

2

3

4

5

02selcyc01ovivniovivni 8.31 2.81

p

30

10 3

30

0

1

2

3

4

5

6

7

8

9

10

cyc02selcyc01ovivniovivni 2.812.81 5.32 52

3010

22 30

2

0

1

2

3

4

5

peanuts 26 cycles carrohtiwhtiw tuohtiw

10 10

10

0

1

2

3

4

5

02selcyc01ovivniovivni 8.31 2.81

p

d50

(mm

) 30

10 3

30

0

1

2

3

4

5

6

7

8

9

10

cyc02selcyc01ovivniovivni 2.812.81 5.32 52

3010

22 30

2

d50

(mm

)d5

0 (m

m)

0

1

2

3

4

5

peanuts 26 cycles carrohtiwhtiw tuohtiw

10 10

10

Fig. 4. Median particle sizes (d50) measured in vivo and in vitro (with different springs)

(A) and carrots (B). Black bars indicate the mean value obtained in vivo and the closest m

and temperature control’’ condition (C) were obtained using the 18.2 and 25 N/mm sp

2.5. In vitro experiment

For the in vitro experiment with the AM2, the variables of the AM2 took into

account a pilot study result indicating that number of cycles and stiffness of the

springs were the two main variables modifying the d50 of the boluses. Variations

in the d50 induced by different values of spring stiffness (variation of the forces)

were observed at three different stages during the chewing process (10 cycles, 20

selcyc62selcycovivni 8.318.31 2.812.81

eanuts

103

60 103

selcyc33selovivni

carrots

2.81 5.325.32 2.535252

10 260

102

2

4

ts 33 cyclestuohtiw

10

selcyc62selcycovivni 8.318.31 2.812.81

eanuts

103

60 103

selcyc33selovivni

carrots

2.81 5.325.32 2.535252

10 260

102

2

4

ts 33 cyclestuohtiw

10

at 10 cycles, 20 cycles and at the moment of swallowing for food boluses of peanuts

ean value obtained in vitro (see Table 2). Data recorded for with or without ‘‘saliva

rings for peanuts and carrots, respectively.

ARTICLE IN PRESS

Table 2Median particle size (d50) observed in vivo and in vitro at 10 cycles, 20 cycles and

at deglutition time for food boluses of peanuts and carrots. The in vitro values were

obtained with springs of ranging stiffness (N/mm: force developed per unit

compression distance). The spring values used in C for peanuts and carrots were

18.2 and 25.0 N/mm, respectively. The in vitro d50 values closest to the in vivo d50

are indicated in bold. This indicated the spring that had to be chosen to reproduce

the bolus particle size. n: number of repeats.

Number of cycles Spring STRENGTH (N/mm) d50 mean SD n

A Peanuts

10 cycles In vivo 2.49 0.58 30

13.8 2.34 0.23 10

18.2 2.00 0.52 3

20 cycles In vivo 1.39 0.17 30

13.8 1.66 0.25 3

18.2 1.36 0.12 10

26 cycles In vivo 1.39 0.19 60

13.8 1.36 0.15 3

18.2 1.38 0.11 10

A. Woda et al. / Journal of Biomechanics 43 (2010) 1667–1673 1671

cycles and swallowing, i.e. 26 for peanuts and 33 for carrots in reference to the

mean in vivo values). Temperature was set to room temperature, and 1.5 ml of tap

water was added before the beginning of the masticatory sequence. In other trials,

(Fig. 4C), the d50 values obtained with an artificial saliva at 37 1C were compared

with those obtained with tap water and at room temperature. Table 1 indicates the

values other than number of cycles and spring stiffness chosen to program

the AM2.

2.6. AM2 calibration–validation and statistical analyses

The calibration–validation was based on comparison between the in vivo and

in vitro values. Analyses were performed using SPSS software (v.14Windows, SPSS

Inc., USA). A three-way-ANOVA was performed with the three factors: type of food,

in vivo–in vitro and number of cycles. A two-way-ANOVA was then computed with

the two factors: temperature-saliva and food. In both cases, Student tests were

carried out for each food to compare the in vivo and in vitro values. To test the

reliability of the apparatus, a three-way-ANOVA was computed with the three

factors: repetition, type of food and number of cycles. Values were given as

mean7standard deviation (SD) and Po5% was chosen.

Number of cycles Spring strength (N/mm) d50 mean SD nB Carrots

10 cycles In vivo 6.74 1.34 30

18.2 6.49 0.91 10

23.5 5.55 0.35 2

25.0 4.60 0.56 2

20 cycles In vivo 3.88 0.96 30

18.2 4.30 0.14 2

23.5 3.67 0.38 10

25.0 3.55 0.21 2

33 cycles In vivo 2.78 0.60 60

18.2 3.30 0.28 4

23.5 2.55 0.07 2

25.0 2.73 0.30 10

35.2 2.10 0.00 2

Food & number of cycles Sal. temp d50 mean SD nC Saliva & Temperature

Peanuts 26 cycles with 1.24 0.08 10

Peanuts 26 cycles without 1.38 0.11 10

Carrots 33 cycles with 2.51 0.14 10

Carrots 33 cycles without 2.73 0.30 10

3. Results

The d50 values obtained from the particle size distributions forboluses collected in vivo at three times during the chewingprocess (10, 20 cycles and swallowing) are displayed in Fig. 4. Thenumber of masticatory cycles at swallowing was 2677.8 forpeanuts and 33711.05 for carrots. A significant decrease in thed50 along the three boluses collection times was observed exceptfor peanuts between 20 and 26 cycles. No significant differencebetween the repeats corresponding to the two boluses collectedfrom each subject was observed.

The calibration–validation was in two steps: calibration andcomparisons between in vitro and in vivo boluses. To calibrate theAM2, we determined the correct spring to be used by comparingthe mean d50 found with different springs with the in vivo d50.

This was done after 10 cycles, 20 cycles and at swallowing(26 cycles for peanuts, 33 for carrots). Two, three, four or tenboluses were obtained (Table 2). Table 2A and B shows the meanvalues of d50. Two springs were tested for peanuts. For carrots,three springs were tested when boluses were obtained after tenand twenty cycles and four springs were tested when boluseswere collected at swallowing. Ten boluses were obtained for eachof the chosen springs (best approximation to the in vivo valuesshown in bold in Table 2 and in black in Fig. 4). The second stepwas performed with these chosen springs by comparing in vivo

and in vitro values. This was done using the d50 obtained in the 60boluses (30 subjects) with the d50 obtained with the AM2 at thethree mastication times and for two foods. There was no effect ofthe in vitro/in vivo factor; a significant effect (Po0.001) was noted

Table 1Values of in vitro variables chosen for AM2 programming for peanuts and carrots

at three different times during the chewing process: 10 and 20 cycles for both

foods and 26 and 33 cycles for peanuts and carrots, respectively.

Food tests variables Peanuts–carrots

Function type Alternate

Temperature control temperature set point(degree C)

Off or on room or 371

Saliva controlSaliva modeVolume (ml)

On mono-injection 1.5

Cycle number 10, 20 and 26 or 33

Start angle (degree) 20

Stop angle (degree) 270

Retract length (mm) 20

Translation speed (mm/s) 100

Rotation speed (degree/s) 140

Sample rate (Hz) 200

for both food and number of cycles [three-way ANOVA,F(1.288)¼1.1;P¼0.29]. No interaction was noted between thein vivo–in vitro factor and either food or number of cycles. Nosignificant difference between in vitro and in vivo values was foundfor any of the six corresponding Student tests (0.26oPo0.92).

A possible effect of temperature and artificial saliva was testedfor peanuts and carrots by comparing the d50 obtained in theseassociated conditions with the d50 obtained with tap water at roomtemperature. Values of d50 obtained with or without the associationof temperature at 37 1C and saliva are given in Table 2C. The resultsindicate a significant effect of the temperature–saliva factor(artificial saliva at 37 1C versus tap water at room temperature)[two-way ANOVA, F(1.36)¼9.5;Po0.01] although it was observedonly for peanuts (Po0.01). A significant difference was notedbetween foods but no interaction was observed between food andthe association of temperature at 37 1C and artificial saliva.

The reliability of the AM2 was tested by searching for repeats-related differences between the d50 obtained with all the springsand at all the mastication times. No difference was found betweenrepetitions [three-way ANOVA, F(9.265)¼0.4; P¼0.95], althougha significant difference was evidenced between the two foods andthe three numbers of cycles (Po0.001). No interaction was notedbetween the repeat factor and the other two factors.

4. Discussion

The AM2 makes a bolus similar to the boluses produced byhumans chewing peanuts and carrots. It is reliable, and its variabilityis low, with no difference between repeats. The differences in

ARTICLE IN PRESS

A. Woda et al. / Journal of Biomechanics 43 (2010) 1667–16731672

particle size between foods or between different times within themasticatory sequence were reproduced. However, this involvedchanging the strength of mastication by changing the spring.Another validation approach could use a different property of thefood bolus such as its rheological behavior.

Why use the AM2 rather than human-produced boluses? Thisquestion arises since the mastication device has to be adjusted,recalibration being needed to match changes observed in bolusesat different time points during the masticatory sequence, fordifferent foods types (Peyron et al., 2004) and for groups ofsubjects such as animal or non-healthy human chewers(Mishellany-Dutour et al., 2008; Woda et al., 2010). Thislimitation might be overcome if a feedback system could beadded. Meanwhile, there are many practical uses for the AM2: (i)about half of the bolus mass is lost by the time the ready-to-swallow bolus is collected (Mishellany-Dutour et al., 2008),probably as a result of intermediary deglutitions (Hiiemae andPalmer, 1999), which may change the bolus characteristics bymodifying the proportion of saliva, food fluids and nutrients(Bourdiol et al., 2004). Consequently, the study of food transfor-mation by mastication is biased when the analyses are conductedon boluses collected from subjects. Simulation of mastication bythe AM2 allows the whole nutrient content, including the liquidphase, to be collected at any time during the masticationsequence; although rinsing is technically required for granulo-metric measures, chemical analysis of the bolus liquid phaseproduced by the simulator would not imply rinsing. (ii) The AM2allows bolus formation to be mimicked for non-communicanthuman subjects who frequently have nutritional problems ordysphagia or both. It can also be used to study mastication inother mammals. A rough evaluation of in vivo boluses would beneeded before programming the simulator for studying the effectsof different formulations of the manufactured food on bolusproperties. This would imply a method of bolus collection adaptedto the considered population. (iii) The force sensor monitors forcesdue to both the spring and food resistance. The modifications of theforce due to food resistance can therefore be evaluated. (iv) TheAM2 allows many repeated chewing sequences independentlyof any changes in experimental conditions induced by subjects’compliance limits.

Conflict of interest statement

No conflict of interest.

Acknowledgements

This study was supported by the IFN ‘‘Prix jeune chercheurBernard Beaufr�ere 2006’’ and by the Conseil Regional d’Auvergne.We thank R. Ryan, F. Gallardo and C. Hartmann for their help indrafting.

References

Anderson, D.L., 1977. Death from improper mastication. International DentalJournal 27, 349–354.

Ben-Aryeh, H., Shalev, A., Szargel, R., 1986. The salivary flow rate and compositionof whole and parotid resting and stimulated saliva in young and old healthysubjects. Biomechanical Medicine and Metabolic Biology 36, 260–265.

Bourdiol, P., Mioche, L., Monier, S., 2004. Effect of age on salivary flows obtainedunder feeding and non-feeding conditions. Journal of Oral Rehabilitation 31,445–452.

Conserva, E., Menini, M., Tealdo, T., Bevilacqua, M., Pera, F., Ravera, G., Pera, P.,2008. Robotic chewing simulator for dental material testing on a sensor-equipped implant setup. International Journal of Prosthodontic 21, 501–508.

Coster, S.T., Schwartz, W.H., 1987. Rheology and the swallow-safe bolus. Dysphagia 1,113–117.

Daumas, B., Xu, W.L., Bronlund, J., 2005. Jaw mechanism modelling and simulation.Mechanism Machine Theory 40, 821–833.

Friedman, H.H., Whitney, H., Szczesniak, A.S., 1963. The texturometer — a newinstrument for objective texture measurement. Journal of Food Science 28,390–403.

Gallo, L.M., Airoldi, G.B., Airoldi, R.L., Palla, S., 1997. Description of Mandibularfinite helical axis pathways in asymptomatic subjects. Journal of DentalResearch 76, 704–713.

Heintze, S.D., Cavalleri, A., 2006. Retention of restorationss placed in noncariouscervical lesions after centric and eccentric occlusal loading in a chewingsimulator – a pilot study. Journal of Adhesive Dentistry 8, 169–174.

Hiiemae, K.M., Palmer, J.B., 1999. Food transport and bolus formation duringcomplete feeding sequences on foods of different initial consistency.Dysphagia 14, 31–42.

Hoebler, C., Lecannu, G., Belleville, C., Devaux, M.F., Popineau, Y., Barry, J.L., 2002.Development of an in vitro system simulating bucco-gastric digestion to assessthe physical and chemical changes of food. International Journal of FoodSciences and Nutrition 53, 389–402.

Hutteau, F., Mathlouthi, M., 1998. Physicochemical properties of sweeteners inartificial saliva and determination of hydrophobicity scale for some sweet-eners. Food Chemistry 63, 199–206.

Jalabert-Malbos, M.L., Mishellany-Dutour, A., Woda, A., Peyron, M.A., 2007. Particlesize distribution in the food bolus after mastication of natural foods. FoodQuality and Preference 18, 803–812.

Kaidonis, J.A., 2008. Tooth wear: the view of the anthropologist. Clinical OralInvestigations 12, S21–S26.

Kato, I., Takanisi, A., Asari, K., Tani, T., 1988. Development of artificial masticationsystem. Construction of one degree of freedom antagonistic muscle modelWJ-O. Anatomischer Anzieger Jena 165, 187–203.

Koolstra, J.H., van Eijden, T.M., Weijs, W.A., Naeije, M., 1988. A three-dimensionalmathematical model of the human masticatory system predicting maximumpossible bite forces. Journal of Biomechanics 21, 563–576.

Lillford, P.J., 1991. Texture and acceptability of human foods. In: Vincent, J.F.V.,Lillford, P.J. (Eds.), Feedings and the Texture of Food. Cambridge UniversityPress, Cambridge, pp. 231–243.

Lucas, P.W., Luke, D.A., 1986. Is food particle size a criterion for the initiation ofswallowing? Journal of Oral Rehabilitation 13 127–136.

Meullenet, J.F., Gandhapuneni, R.K., 2006. Development of the BITE Master II andits application to the study of cheese hardness. Physiology and Behavior 89,39–43.

Mishellany, A., Woda, A., Labas, R., Peyron, M.A., 2006. The challenge ofmastication: preparing a bolus suitable for deglutition? Dysphagia 21 87–94.

Mishellany-Dutour, A., Renaud, J., Peyron, M.A., Rimek, F., Woda, A., 2008. Is thegoal of mastication reached in young dentates, aged dentates and aged denturewearers? British Journal of Nutrition 99 121–128.

Morais, J.A., Heydecke, G., Pawliuk, J., Lund, J.P., Feine, J.S., 2003. The effects ofmandibular two-implant overdentures on nutrition in elderly edentulousindividuals. Journal of Dental Research 82, 53–58.

Morel, A., Albuisson, E., Woda, A., 1991. A study of human jaw movements deducedfrom scratches on occlusal wear facets. Archives of Oral Biology 36, 195–202.

Nassl, K., Kropf, F., Klostermeyer, H., 1995. A method to mimic and to study therelease of flavour compounds from chewed food. Zeitschrift fur Lebensmittel-Untersuchung und -Forschung 201, 62–68.

Ngom, I., Woda, A., 2002. Influence of impaired mastication on nutrition. Journal ofProsthetic Dentistry 87, 667–673.

Ngom, P.I., Diagne, F., Aıdara-Tamba, A.W., Sene, A., 2007. Relationship betweenorthodontic anomalies and masticatory function in adults. American Journal ofOrthodontics and Dentofacial Orthopedics 131, 216–222.

Olthoff, L.W., Van der Bilt, A., Bosman, F., Kleizen, H.H., 1984. Distribution ofparticle sizes in food comminuted by human mastication. Archives of OralBiology 29, 899–903.

Pap, J.S., Xu, W.L., Bronlund, J., 2005. A robotic human masticatory system:kinematics simulations. International Journal of Intelligent TechnologyApplication 1, 3–17.

Peleg, M., Normand, M.D., 1982. A computer assisted analysis of some theoreticalrate effects in mastication and in deformation testing of foods. Journal of FoodSciences 47, 1572–1578.

Peyron, M.A., Mioche, L., Culioli, J., 1994. Bite force and sample deformation duringhardness assessment of viscoelastic models of foods. Journal of Texture Studies25, 59–76.

Peyron, M.A., Lassauzay, C., Woda, A., 2002. Effects of increased hardness on jawmovement and muscle activity during chewing of viscoelastic model foods.Experimental Brain Research 142, 41–51.

Peyron, M.A., Mishellany, A., Woda, A., 2004. Particle size distribution of foodboluses after mastication of six natural foods. Journal of Dental Research 83,578–582.

Posselt, U., 1952. Studies on the mobility of the human mandible. ActaOdontologica Scandinavica 10, 19–160.

Prinz, J.F., Lucas, P.W., 1995. Swallow thresholds in human mastication. Archives ofOral Biology 40, 401–403.

Salaorni, C., Palla, S., 1994. Condylar rotation and anterior translation in healthyhuman temporomandibular joints. Schweiz Monatsschr Zahnmed 104, 415–422.

Salles, C., Tarrega, A., Mielle, P., Maratray, J., Gorria, P., Liaboeuf, J., Liodenot, J.J.,2007. Development of a chewing simulator for food breakdown and theanalysis of in vitro flavor compound release in a mouth environment. Journal ofFood Engineering 82, 189–198.

ARTICLE IN PRESS

A. Woda et al. / Journal of Biomechanics 43 (2010) 1667–1673 1673

Sale, P., Noel, Y., Lasteyras, A., Oleon, C., 1984. A sinusoidal compression system tostudy rheological properties of foods in the transient state. Journal of TextureStudies 15, 103–114.

Sheiham, A., Steele, J.G., Marcenes, W., Lowe, C., Finch, S., Bates, C.J., Prentice, A.,Walls, A.W., 2001. The relationship among dental status, nutrient intake, andnutritional status in older people. Journal of Dental Research 80, 408–413.

Slagter, A.P., Van der Glas, H.W., Bosman, F., Olthoff, L.W., 1992. Force-deformationproperties of artificial and natural foods for testing chewing efficiency. Journalof Prosthetic Dentistry 68, 790–799.

Strait, S.G., 1997. Tooth use and the physical properties of food. EvolutionaryAnthropology, 199–211.

Usui, T., Maki, K., Toki, Y., Shibasaki, Y., Takanobu, H., Tanakanishi, A., Hatcher, D.,Miller, A., 2003. Measurement of mechanical strain on mandibular surfacewith mastication robot: influence of muscle loading direction and magnitude.Orthodontic and Craniofacial Research 6 (Suppl. 1), 163–167 discussion179–182.

Van der Bilt, A., Van der Glas, H.W., Bosman, F., 1992. A computer simulation of theinfluence of selection and breakage of food on the chewing efficiency of humanmastication. Journal of Dental Research 1, 458–465.

Van der Bilt, A., Olthoff, L.W., Van der Glas, H.W., Van der Weelen, K., Bosman, F.,1993. A comparison between data analysis methods concerning particle sizedistributions obtained by mastication in man. Archives of Oral Biology 38,423–429.

Van Ruth, S.M., Roozen, J.P., Cozijnsen, J.L., 1995. Volatile compounds of rehydratedFrench beans, bell peppers and leeks. Part 1. Flavour release in the mouth andin three mouth model systems. Food Chemistry 53, 15–22.

Wang, J.S., Stohler, C.S., 1990. Force-time breakage characteristics of food duringstimulated initial phase of mastication. Proceedings of the National ScienceCouncil B Roc. 14, 228–232.

Woda, A., Vigneron, P., Kay, D., 1979. Nonfunctional and functional occlusalcontacts: a review of the literature. The Journal of Prosthetic Dentistry 42,335–341.

Woda, A., Foster, K., Mishellany, A., Peyron, M.A., 2006. Adaptation of healthymastication to factors pertaining to the individual or to the food. Physiologyand Behavior 89, 28–35.

Woda, A., Nicolas E., Mishellany-Dutour A., Hennequin M., Mazille M.N., VeyruneJ.L., Peyron M.A., 2010. A new indicator of abnormal masticatory function: theMNI. Journal of Dental Research 89, 281–285.