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Adaptation of healthy mastication to factors pertaining to the individual or to the food
Physiology & Behavior 89 (2006) 28 – 35
Adaptation of healthy mastication to factors pertaining to the individual or to the food A. Woda a,⁎, K. Foster a,b , A. Mishellany a , M.A. Peyron c a
b
DIDO, Dental Faculty, University of Auvergne, 11 bd Charles-de-Gaulle, 63000 Clermont-Ferrand, France Institute of Food, Nutrition and Human Health, Massey University, Private Bag 102 904, North Shore Mail Centre, Auckland, New Zealand c Institut National de la Recherche Agronomique, Unité de Nutrition Humaine, Theix, 63122 Saint-Genès Champanelle, France Received 22 November 2005; received in revised form 17 February 2006; accepted 20 February 2006
Abstract Mastication is a physiological process controlled by the central nervous system and modulated by inputs from the mouth. Both the intrinsic characteristics of the subject and the extrinsic characteristics of the chewed food are responsible for variations of the masticatory function. Age, gender and dental state constitute the most studied intrinsic factors whereas hardness, rheological characteristics such as plasticity or elasticity, and food size are the better known extrinsic factors. These factors cause physiological adaptations which can occur during individual cycles or the whole sequence of mastication. Electromyographic and jaw movements (kinematic) recordings are commonly used to study mastication, from which, several variables can be measured. Vertical and lateral amplitudes and, velocities of jaw movements, are only given by kinematic recordings. Bioelectrical activities per cycle or per sequence are closely linked to masticatory forces and are measured from electromyographic recordings. Number of cycles, sequence duration and masticatory frequency can be measured from both types of recordings. The objective of this review is to provide an overview of the variations of the measured masticatory variables that occur when mastication adapts to changes in characteristics of the individual or the food. © 2006 Elsevier Inc. All rights reserved. Keywords: Rheological behaviour; Model food; Elastic or plastic food texture; Masticatory adaptation
1. Introduction A sequence of mastication begins with the introduction of a piece of food into the mouth and finishes with the deglutition of the food bolus. Each sequence is made by a succession of chewing cycles. Each cycle is formed by one jaw-opening followed by one jaw-closing movement. Because of the regular succession of cycles, rhythm is a major characteristic of mastication. The rhythm of mastication is generated by a brain stem central pattern generator (CPG) [1], which activates a motor program coordinating the activities of the jaw, tongue and facial muscles [2]. The masticatory program adapts its output to the properties of the food being chewed, including the size of the food sample introduced in the mouth, its hardness and other physical properties that cause the sensations of texture [3–11]. Adaptation of the motor program also occurs continuously ⁎ Corresponding author. Tel.: +33 4 73 17 73 27; fax: +33 4 73 17 73 09. E-mail address: [email protected] (A. Woda). 0031-9384/$ - see front matter © 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.physbeh.2006.02.013
throughout the chewing sequence as the food properties are modified by mastication. The food acts as a stimulus exciting several types of receptor (periodontal, muscle spindle, mucosal). The sensory messages, which are conveyed to the brain stem, are used in one or several feedback loops allowing continual adaptation of the motor activities to the mechanical properties of the food which are progressively changing during the sequence [2,12]. This leads to the formation of a bolus ready-to-swallow. Finally, adaptation of the motor program is also needed throughout an individual's life to cope with the changes that occur as a result of ageing and tooth loss. The aim of this review is to describe the variations of both the jaw movements and the masticatory muscle activities observed while different groups of individuals are chewing different types of foods. The factors that induce variations in the masticatory parameters are related to either the food (sample size, hardness or rheological behaviour) or the individual (age, gender or dental health). They will be called extrinsic and intrinsic factors respectively. The term “rheological behaviour”
A. Woda et al. / Physiology & Behavior 89 (2006) 28–35
refers to the science of rheology. This science is a branch of physics that studies the stress/strain relationship of materials. It describes properties such as elasticity, plasticity or brittleness. Other factors such as the time of day, appetite, liking/disliking of food, flavour, previous experiences, education and many others that also modulate the masticatory function will not be considered in this article. 2. Recording mastication Many methods can be used to record masticatory function. Most frequently, mastication is monitored by kinematic and electromyographic (EMG) recordings. The former gives information about jaw movements and the later follows bioelectrical activities of the masticatory muscles which are known to be closely related to the forces developed during the course of mastication [13,14]. The use of videography to record mastication has been validated in different groups of subjects [15,17]. It offers the advantage of being less intrusive than EMG or kinematic recordings which is particularly important for anxious or other special patients. It is also easier to use in a dental clinical setting and it gives information about the soft tissues functions such as lip closure [16,17]. The function of the jaw muscles during chewing can also be inferred by recording the force during chewing [see Ref. [18]] or during maximal biting [19]. The function of the tongue and
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other soft tissues was recently observed with videofluorography [20], by observing the orientation of non edible material in the mouth [21] or by observing the mixing or positioning of differently colored materials [22,23]. Recently, ultrasonic echo-sonography was used to observe the soft tissues [24]. All these recordings illustrate the rhythmical nature of mastication. During one sequence, the recordings often show intermediate and final deglutitions as well as changes of the masticatory side (i.e. from left to right or vice versa) (Fig. 1). They also indicate that a clearance stage exists which starts after the final deglutition and is characterized by non periodic muscle activity [25,26]. 3. Grinding and crushing the food At the end of the sequence, the food bolus must be smooth, deformable and cohesive [7,11]. This is required to facilitate harmless passage of the bolus through the aero-digestive crossing and then through the esophagus. To obtain such a food bolus, the food must be transformed into many small-sized particles bound together by a mixture of saliva and liquids derived from the food itself [7]. Recent studies [27,28] or reviews [29] in young healthy subjects have shown that the particle size distribution of ready-to-swallow food boluses displays no significant intra-individual variability and only a very small inter-individual variability. This shows that a food
a masticatory cycle
right
10 5
lateral
mandibular movement (mm)
0 -5
left -10 close
vertical
✳
✳
30 20 10
open
swallowing
0 4 3
right masseter
●
●
2 1 0 4 3
EMG activity (mV)
left masseter
2 1 0 4 3
right temporalis
2 1 0 4 3
left temporalis
2 1 0 0
1
2
3
4
5
6
7
8
9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43
masticatory sequence
Time (s)
Fig. 1. Example of a complete masticatory sequence recording obtained during chewing of a plastic food product. The six traces are, top to bottom, lateral and vertical mandibular movements, electromyographic (EMG) activity of right and left masseters, and right and left temporalis muscles. Black circles (●) indicate larger EMG activity probably corresponding to intermediate swallowings. Stars (⁎) mark contro-lateral mandibular deviation due to re-positioning of the food bolus.
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A. Woda et al. / Physiology & Behavior 89 (2006) 28–35
bolus has to meet precise conditions before swallowing can be triggered. These conditions may be considered as a vital requirement, since dysfunctional deglutition, which is known to be linked to a high morbidity level [30,31], can otherwise occur. In contrast to this small intra- and inter-individual variability that occurs during the formation of the food bolus, is the large amount of variability that exists in masticatory parameters as a result of the many factors which have been shown to influence mastication. 4. Effects of intrinsic factors 4.1. Inter- and intra-individual variations of masticatory parameters Numerous researchers have described a large variation between individuals for all physiological parameters of mastication (number of cycles, total electromyographic activity during a sequence, sequence duration, masticatory frequency, vertical and lateral amplitudes of the mandibular movement) [32–35]. There are, however, no significant differences between the values of the masticatory parameters for a given individual who is asked to chew the same food several times. The large variation between individuals and the lack of a significant difference for the same individual, after several repetitions, have been clearly shown by using well controlled food stimuli and strict inclusion criteria in order to exclude, as much as possible, non-controllable factors which could explain some interindividual variability [32,35]. 4.2. The effects of gender on mastication There are differences between genders for several parameters: males display higher EMG activities per cycle and per sequence, higher vertical amplitudes and a slightly higher masticatory frequency during a sequence. No difference between males and females has been noted for the total number of cycles constituting a masticatory sequence [36–39]. 4.3. The effects of ageing on mastication The consequence of ageing on masticatory function must be separated from confounding factors such as missing teeth or other independent illnesses. In spite of a known decrease of the maximal bite force [40–42] and a loss of masticatory muscle mass [43], ageing alone has little impact on the ability of subjects to reduce food into small particles [42,44–48]. Thus, the purpose of chewing, which is to make a smooth, deformable and cohesive food bolus [7], is still achieved despite ageing of the masticatory apparatus. There are, however, some adaptations that occur with age which result in a modification of the masticatory parameters. The number of cycles [49] and the total EMG activity during a sequence increases with age [39]. The EMG activity per cycle does not change with age and still adjusts to the hardness of the food [39]. The frequency of the cycles during a masticatory sequence also remains constant with age [39,50].
4.4. The effects of dental state on mastication The number of teeth and the quality of the contacts, between teeth belonging to the lower and upper jaws, is of course of primary importance. Decreased masticatory performance or impaired chewing function have been described in subjects with either dental malocclusion [51,52], temporo-mandibular disorders [53] or a decreased number of teeth [44–47,54–56]. When all natural teeth have been replaced by a removable prosthetic device, denture wearing individuals failed to adapt to this new situation in spite of an increase in the number of chewing cycles, duration of a masticatory sequence and EMG activity per sequence [48,56–59] compared to subjects with natural teeth. In addition, denture wearers did not adapt to an increase in food hardness, had a slower masticatory frequency compared to dentate subjects [48] and may choose not to eat some hard foods such as meat [60]. 5. Effects of extrinsic factors 5.1. Food is a complex stimulus The central command of mastication is modulated by peripheral inputs [[1,61–64] and see reviews [5,12]] so that the masticatory motor output adapts to the characteristics of the chewed food [63,65–67]. Food is, however, a very complex stimulus since many of its characteristics, for example, texture, flavour, size, shape, influence mastication. In addition, food is difficult to reduce to a single physical dimension as can be done, for example, with light or vibration in studies about vision or proprioception. A first step toward simplification is to only consider the mechanical properties of the food. It is for this reason that hardness has frequently been chosen as the studied food property. Many authors have used natural foods placed on a graded scale for hardness [60,66,68,69]. Hardness is, however, a loose term and it is not clear whether the masticatory response to a particular product is in response to the hardness of the product and/or to some other textural property (elasticity, plasticity, stickiness, brittleness to name a few). To better control these food properties, non alimentary models, usually made with elastomers or waxes were used [70–76]. Since these artificial products are impossible to swallow and, as a result, may modify some events in the masticatory process, their use strongly limits the observation of natural chewing. 5.2. The effects of hardness versus rheological behaviour on mastication: the use of model foods So far, two approaches have been used to improve the understanding of the natural food stimulus/masticatory response link. The first approach attempted to link food properties with food breakdown during mastication. The ratio of the square roots of toughness and modulus of elasticity was proposed to best express the resistance to food breakdown during mastication [69,77]. These authors strongly suggested that this mechanical index might well reflect the sensory stimulus utilized in the ongoing modulation of the central pattern
A. Woda et al. / Physiology & Behavior 89 (2006) 28–35
different hardness levels [66,78–82]. Recently, a better control of the rheological properties was obtained by using brittle food products in the form of three tablets exhibiting different hardness [75] and visco-elastic (predominantly elastic) gelatine based model foods with a four point scale of hardness [10,35]. In these studies, differences in masticatory parameters between several model foods could be related directly to the hardness because the other textural properties of the food were constant. It was, however, not possible to reveal in a single experiment the independent adaptation of masticatory function to changes in the rheological behaviour of the foods versus hardness. This has
generator. The second approach attempted to uncover the changes in the masticatory parameters that are produced by a relatively pure, single rheological stimulus. This was done by developing edible model foods that allowed the dissociation of hardness from other textural properties. These model foods had to display rheological behaviours that were as pure as possible, e.g.: brittleness, elasticity or plasticity. In addition they had to display a homogeneous structure, a reproducible texture, constant shape and size and had to exhibit a full hardness scale. A first step towards this goal was reached when some authors used natural chewing gums sometimes with two Elastic
A
Plastic
B
70
70
60
60
50
50
40
40
30
30
20
20
10
***
***
*
MLR: Hardness
***
F=105
***
P=0.0001
**
10
0
31
0 E1
E2
E3
P1
E4
P2
P3
P4
R2=0.495
Total EMG activity/sequence (mV.s)
C
D 14
14
12
12
10
10
8
8
*
6
4
2
2
0
0 E2
E3
Rheology
***
F=32
6
4
E1
MLR:
P=0.0001 R2=0.232
E4
P1
P2
P3
P4
Mean lateral amplitude (mm)
E
F 30
30
25
25
20
20
**
***
15
10
5
5
0
0 E2
E3
Rheology
15
10
E1
MLR: **
***
F=39 P=0.0001
E4
P1
P2
P3
P4
R2=0.266
Mean vertical amplitude (mm)
G
H 80
80
70
70
60
60
***
50 40
40
30
30
20
20
10
10
0
0 E1
E2
MLR:
***
***
50
E3
E4
Closing velocity
Rheology F=20 P=0.0001 P1
P2
P3
P4
R2=0.160
(mm.s-1)
Fig. 2. Mean values and S.E.M. observed for total EMG activity per sequence, mean lateral and vertical amplitudes, and closing velocities during chewing of an elastic (in A, C, E and G respectively) or a plastic (in B, D, F and H respectively) product. E1, E2, E3, E4 and P1, P2, P3, P4 are products of increasing hardness with elastic or plastic rheological characteristics, respectively. Black columns represents elastic (E4) and plastic (P2) food products of comparable mechanical hardness values. The results of Multiple Linear Regression (MLR) analyses, performed with hardness and type of rheological behaviour as explanatory variables, are presented in front of the corresponding masticatory parameters. ⁎: p < 0.05; ⁎⁎: p < 0.01; ⁎⁎⁎: p < 0.001.
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A. Woda et al. / Physiology & Behavior 89 (2006) 28–35
been done recently in an experiment using two sets of model foods displaying different rheological behaviours, i.e., elasticity and plasticity, with each model food being presented on a four point graded scale of hardness [83]. These two model foods were manufactured to display well known rheological behaviours. They were jellied confectioneries for elastic products and hard caramel confectioneries for plastic products. The range of hardness and the rheological behaviour were both verified and controlled using a compression test and the range of hardness was further evaluated using a visual analogue scale. The values obtained with the two hardness measurements were shown to be closely correlated. It was, therefore, possible to selectively study the impact of the elasticity vs. plasticity on a variety of recorded variables, which all describe the characteristics of the chewing motor behaviour. The results showed that variables associated with the jaw muscle activity (number of cycles, duration of the sequence, EMG activity during each cycle or during the whole sequence) were primarily related to the hardness of the test foods, while the shape of the movement trajectories (vertical amplitude, lateral amplitude, closing velocity) and the masticatory frequency were preferentially adapted to differences in the rheological behaviour between the elastic vs. plastic products (Fig. 2). 5.3. The effects of food sample size on mastication The thickness of the food sample and the volume of the initial mouthful have an effect on many parameters of the
masticatory function. Most of the parameters increase with the size, weight or volume, of the mouthful but those related to mandibular movements are the most influenced. The most obvious change induced by an increase in the food size is an increase in vertical amplitude [6,84–89]. 6. Masticatory frequency may be a key parameter for the evaluation of an individual's masticatory function A summary of the effects of the different factors on the main parameters of mastication is shown in Table 1. In a healthy subject, mastication is able to adjust to various individual and/or environmental conditions so that the masticatory function is satisfactorily achieved. When mastication is not able to fully adapt, the masticatory function may not be fulfilled resulting in an insufficiently prepared bolus. The particle size distribution of the food bolus is shifted towards coarser particles [29]. The consequences on the general health of an individual with impaired mastication have not been fully explored yet, but recent reviews suggest that they are serious [90,91] and there is a strong suspicion that a reduced nutrient availability occurs [92]. Two criteria may be proposed to detect an impaired mastication. The first criteria could be the detection of a large change in the distribution of the food bolus particle sizes. The second criteria could rely on a change in cycle frequency. Frequency is the chewing parameter with the most repeatable values between trials in a single individual [10,35,38,48].
Table 1 Schematic representation of the adaptation of mastication
Number of cycles
Sequence duration
EMG activity EMG activity Masticatory /sequence /cycle frequency
Vertical amplitude
Lateral amplitude
Closing velocity
9, 10, 69, 79, 83, 84
10, 81, 98
10, 32
83
83
83
6, 71, 85, 89
85, 89
Extrinsic factors
Hardness (from soft to hard)
10, 65, 66, 79, 81, 83
10, 25, 79, 83, 100
10, 65, 79, 83
(from elastic to plastic)
Sample size
83
6, 84–86
83
6
83
10, 79, 80, 83
83
83
82, 85, 88
6, 87, 89
Depends on food
Age Intrinsic factors
10, 65, 78, 83
Physical properties
39, 44, 49
39, 44, 49
39, 49
39, 49
39
39
38, 39
36, 38, 39, 94
39, 50
Gender (from female to male) 36–39
39
39
Depends on food
Tooth loss (edentate) 48, 101
48
48
48, 56, 99
36–39
36
36,37
* 48, 56, 101, 102
101
Responses of the major electromyographic and kinematic parameters to the main extrinsic (three top lines) and intrinsic (three bottom lines) factors. Four signs are used to display the effects of the extrinsic and intrinsic factors on masticatory parameters: downward pointing arrows indicate a decrease, slightly or strongly upward pointing arrows indicate a slight or strong increase in the values of the masticatory parameters. An equal sign indicates no change. ⁎There is more decrease with harder foods.
A. Woda et al. / Physiology & Behavior 89 (2006) 28–35
Frequency has been shown to vary only slightly if at all when a given individual is chewing a given food. It remains constant even when the hardness of the food is increased, so long as the rheological behaviour of the food is constant [10,39,56,83,93]. The lack of variation in the masticatory frequency also applies when the intensity of the taste of the food varies [26]. Contrasting with the almost complete stability of the chewing frequency for a given food and a single healthy individual, are all other parameters of mastication which are modulated by an increase in hardness. For example, ageing brings about a change in all variables related to muscle work (number of cycles, sequence duration, EMG per sequence, EMG per cycle) although masticatory frequency is not modified [39,48] (Table 1). It therefore appears that mastication frequency is the only parameter of mastication that does not adapt to neither a change in food hardness nor ageing. The stability of chewing frequency only applies to healthy persons because individuals wearing full dentures [48], suffering from temporo-mandibular disorders [53] or disabled persons with Down's syndrome [15], all display varying levels of decreased mastication frequency compared with healthy controls. The stability of this masticatory parameter in healthy subjects indicates that it could be a key parameter for the evaluation of an individual's masticatory function. It has been suggested that a lack of change in mean frequency could be used as a criterion of good masticatory health and alternatively, a large variation from the mean frequency values could be indicative of an impaired masticatory function [48]. It is important to note, however, that the use of frequency as a criterion for masticatory function could only be applied to a given population and for a given food because cycle frequency displays a large inter-individual variability, [35,65], significant differences between men and women [38,39,94] and changes with mouthful size or the rheological characteristics of natural foods [20,65,83,94–97]. 7. Future directions Considered as a whole, these results constitute a database that summarize our understanding of the modulation of mastication in response to changes in the individual's oral physiology and food texture. Many of these results were obtained from healthy individuals, using controlled stimuli giving reproducible responses. These results provide a controlled tool for studying other groups of individuals. In particular, subjects with impaired mastication can now be studied in comparison with a control group characterised by a known physiology of mastication. This should lead to the development of masticatory function tests which should be easy to use in a clinical environment. These data will also assist in the development of a robotic device which could be either calibrated or trained to simulate the physiological function. Such a device would allow researchers to perform experiments difficult to carry out in humans. This type of device could be used to predict human texture perceptions of new foods, once the masticatory adaptations to changes in food texture are completely understood. It could also be used to create an
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[51] Ngom IP, Diagne F, Aidara-Tamba AW, Sene A. Relationship between orthodontic anomalies and masticatory function in adult subjects. Am J Orthod Dentofacial Orthop in press. [52] English JD, Buschang PH, Throckmorton GS. Does malocclusion affect masticatory performance? Angle Orthod 2002;72:21–7. [53] Sato S, Ohta M, Goto S, Kawamura H, Motegi K. Electromyography during chewing movement in patients with anterior disc displacement of the temporomandibular joint. Int J Oral Maxillofac Surg 1998; 27:274–7. [54] Kapur KK, Soman S, Yurkstas A. Tests foods for measuring masticatory performance of denture wearers. J Prosthet Dent 1964;14:483–91. [55] Garcia RI, Perlmuter LC. Effects of dentition status and personality on masticatory performance and food acceptability. Dysphagia 1989;4: 121–6. [56] Slagter AP, Bosman F, Van der Glas HW, Van der Bilt A. Human jawelevator muscle activity and food comminution in the dentate and edentulous state. Arch Oral Biol 1993;38:195–205. [57] Wayler AH, Muench ME, Kapur KK, Chauncey HH. Masticatory performance and food acceptability in persons with removable partial dentures, full dentures and intact natural dentition. J Gerontol 1984; 39:284–9. [58] Slagter AP, Olthoff LW, Steen WHA, Bosman F. Comminution of food by complete-denture wearers. J Dent Res 1992;71:380–6. [59] Veyrune JL, Lassauzay C, Nicolas E, Peyron MA. Mastication of model products in complete denture wearers submitted for publication. [60] Veyrune JL, Mioche L. Complete denture wearers: electromyography of mastication and texture perception whilst eating meat. Eur J Oral Sci 2000;108:83–92. [61] Lavigne G, Kim JS, Valiquette C, Lund JP. Evidence that periodontal pressoreceptors provide positive feedback to jaw closing muscles during mastication. J Neurophysiol 1987;58:342–58. [62] Ottenhoff FAM, van der Bilt A, van der Glas HW, Bosman F. Periphally induced anticipating elevator muscle activity during simulated chewing in humans. J Neurophysiol 1992;67:75–83. [63] Ottenhoff FAM, van der Bilt A, van der Glas HW, Bosman F. Control of elevator muscle activity during simulated chewing with varying food resistance in humans. J Neurophysiol 1992;68:933–44. [64] van der Bilt A, Weijnen FG, Ottenhoff FAM, van der Glas HW, Bosman F. The role of sensory information in the control of rhythmic open–close movements in humans. J Dent Res 1995;74:1658–64. [65] Steiner JE, Michman J, Litman A. Time sequence of the activity of the temporal and masseter muscles in healthy young human adults during habitual chewing of different test foods. Arch Oral Biol 1974;19:29–34. [66] Sakamoto H, Harada T, Matsukubo T, Takaesu Y, Tazaki M. Electromyographic measurement of textural changes of foodstuffs during chewing. Agric Biol Chem 1989;53:2421–33. [67] Wang JS, Stohler CS. Predicting foodstuff from jaw dynamics during masticatory crushing in man. Arch Oral Biol 1991;36:239–44. [68] Duizer LM, Gullett EA, Findlay CJ. The effect of masticatory patterns as measured by time-intensity and electromyography on the perception of bovine muscle tenderness. J Sens Stud 1994;9:33–46. [69] Agrawal KR, Lucas PW, Bruce IC, Prinz JF. Food properties that influence neuromuscular activity during human mastication. J Dent Res 1998;77:1931–8. [70] Olthoff LW, van der Bilt A, de Boer A, Bosman F. Comparison of forcedeformation characteristics of artificial and several foods for chewing experiments. J Texture Stud 1986;17:275–89. [71] van der Bilt A, van der Glas HW, Olthoff LW, Bosman F. The effect of particle size reduction on the jaw gape in human mastication. J Dent Res 1991;70:931–7. [72] Slagter AP, van der Glas HW, Bosman F, Olthoff LW. Force-deformation properties of artificial and natural foods for testing chewing efficiency. J Prosthet Dent 1992;68:790–9. [73] Mioche L, Peyron MA. Bite force displayed during assessment of hardness in various texture contexts. Arch Oral Biol 1995;40:415–23. [74] Buschang PH, Throckmorton GS, Travers KH. The effects of bolus size and chewing rate on masticatory performance with artificial test foods. J Oral Rehab 1997;24:522–6. [75] Shiau YY, Peng CC, Hsu CW. Evaluation of biting performance with standardized test-foods. J Oral Rehab 1999;26:447–52.
A. Woda et al. / Physiology & Behavior 89 (2006) 28–35 [76] Fontijn-Tekamp FA, Van Der Bilt A, Abbink JH, Bosman F. Swallowing threshold and masticatory performance in dentate adults. Physiol Behav 2004;83:431–6. [77] Agrawal KR, Lucas PW, Prinz JF, Bruce IC. Mechanical properties of foods responsible for resisting food breakdown in the human mouth. Arch Oral Biol 1997;42:1–9. [78] Plesh O, Bishop B, McCall W. Effect of gum hardness on chewing pattern. Exp Neurol 1986;92:502–12. [79] Horio T, Kawamura Y. Effects of texture of food on chewing patterns in the human subject. J Oral Rehabil 1989;16:177–83. [80] Bishop B, Plesh O, McCall WD. Effects of chewing frequency and bolus hardness on human incisor trajectory and masseter muscle activity. Arch Oral Biol 1990;35:311–8. [81] Takada K, Miyawaki S, Tatsuta M. The effects of food consistency on jaw movement and posterior temporalis and inferior orbicularis oris muscle activities during chewing in children. Arch Oral Biol 1994;39:793–805. [82] Anderson K, Throckmorton GS, Buschang PH, Hayasaki H. The effects of food bolus hardness on masticatory kinematics. J Oral Rehabil 2002; 29:689–96. [83] Foster K , Woda A , Peyron MA. Effect of texture of plastic and elastic model foods on the parameters of mastication. J Neurophysiol in press. [84] Lucas PW, Ow RKK, Ritchie GM, Chew CL, Keng SB. Relationship between jaw movement and food breakdown in human mastication. J Dent Res 1986;65:400–4. [85] Diaz-Tay J, Jayasinghe N, Lucas PW, McCallum JC, Jones JT. Association between surface electromyography of human jaw-closing muscle and quantified food breakdown. Arch Oral Biol 1991;36:893–8. [86] Ottenhoff FAM, van der Bilt A, van der Glas HW, Bosman F. Control of human jaw elevator muscle activity during simulated chewing with varying bolus size. Exp Brain Res 1993;96:501–12. [87] Miyawaki S, Ohkochi N, Kawakami T, Sugimura M. Effect of food size on the movement of the mandibular first molars and condyles during deliberate unilateral mastication in humans. J Dent Res 2000;79: 1525–1531. [88] Miyawaki S, Ohkochi N, Kawakami T, Sugimura M. Changes in masticatory muscle activity according to food size in experimental human mastication. J Oral Rehabil 2001;28:778–84. [89] Bhatka R, Throckmorton AM, Wintergerst AM, Hutchins B, Buschang PH. Bolus size and unilateral chewing cycle kinematics. Arch Oral Biol 2004;49:559–66.
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[90] Hutton B, Feine J, Morais J. Is there an association between edentulism and nutritional state? J Can Dent Assoc 2002;68:182–7. [91] Ngom PI, Woda A. Influence of impaired mastication on nutrition. J Prosthet Dent 2002;87:667–73. [92] Sheiham A, Steele JG, Marcenes W, Lowe C, Finch S, Bates CJ, et al. The relationship among dental status, nutrient intake, and nutritional status in older people. J Dent Res 2001;80:408–13. [93] Jemt T, Hedegard B. Reproducibility of chewing rhythm and of mandibular displacements during chewing. J Oral Rehabil 1982;9:531–7. [94] Nagasawa T, Yanbin X, Tsuga K, Abe Y. Sex difference of electromyogram of masticatory muscles and mandibular movement during chewing of food. J Oral Rehabil 1997;24:605–9. [95] Nakamura T, Inoue T, Ishigaki S, Morimoto T, Maruyama T. Differences in mandibular movements and muscle activities between natural and guided chewing cycles. Int J Prosthodont 1989;2:249–53. [96] Kohyama K, Mioche L, Bourdiol P. Influence of age and dental status on chewing behavioural studied by EMG recordings during consumption of various food samples. Gerodontol 2003;20:15–23. [97] Gavião MB, Engelen L, Van Der Bilt A. Chewing behaviour and salivary secretion. Eur J Oral Sci 2004;112:19–24.
Further reading [1] Mizumori T, Tsubakimoto T, Iwasaki M, Nakamura T. Masticatory laterality — evaluation and influence of food texture. J. Oral Rehabil 2003;30:995–9. [2] Shi CS, Ouyang G, Guo TW. A comparative study of mastication between complete denture wearers and dentate subjects. J Prosthet Dent 1991;66:505–9. [3] Feine JS, Maskawi K, De Grandmont P, Donohue WB, Tanguay R, Lund JP. Within-subject comparisons of implant-supported mandibular prostheses: evaluation of masticatory function. J Dent Res 1994;73:1646–56. [4] Jemt T. Chewing patterns in dentate and complete denture wearers recorded by light emitting diodes. Swed Dent J 1981;5:199–205. [5] Jemt T, Karlsson S. Mandibular movements during mastication before and after rehabilitations with new complete dentures recorded by lightemitting-diodes. Swed Dent J 1980;4:195–200.
Adaptation of healthy mastication to factors pertaining to the individual or to the food A. Woda a,⁎, K. Foster a,b , A. Mishellany a , M.A. Peyron c a
b
DIDO, Dental Faculty, University of Auvergne, 11 bd Charles-de-Gaulle, 63000 Clermont-Ferrand, France Institute of Food, Nutrition and Human Health, Massey University, Private Bag 102 904, North Shore Mail Centre, Auckland, New Zealand c Institut National de la Recherche Agronomique, Unité de Nutrition Humaine, Theix, 63122 Saint-Genès Champanelle, France Received 22 November 2005; received in revised form 17 February 2006; accepted 20 February 2006
Abstract Mastication is a physiological process controlled by the central nervous system and modulated by inputs from the mouth. Both the intrinsic characteristics of the subject and the extrinsic characteristics of the chewed food are responsible for variations of the masticatory function. Age, gender and dental state constitute the most studied intrinsic factors whereas hardness, rheological characteristics such as plasticity or elasticity, and food size are the better known extrinsic factors. These factors cause physiological adaptations which can occur during individual cycles or the whole sequence of mastication. Electromyographic and jaw movements (kinematic) recordings are commonly used to study mastication, from which, several variables can be measured. Vertical and lateral amplitudes and, velocities of jaw movements, are only given by kinematic recordings. Bioelectrical activities per cycle or per sequence are closely linked to masticatory forces and are measured from electromyographic recordings. Number of cycles, sequence duration and masticatory frequency can be measured from both types of recordings. The objective of this review is to provide an overview of the variations of the measured masticatory variables that occur when mastication adapts to changes in characteristics of the individual or the food. © 2006 Elsevier Inc. All rights reserved. Keywords: Rheological behaviour; Model food; Elastic or plastic food texture; Masticatory adaptation
1. Introduction A sequence of mastication begins with the introduction of a piece of food into the mouth and finishes with the deglutition of the food bolus. Each sequence is made by a succession of chewing cycles. Each cycle is formed by one jaw-opening followed by one jaw-closing movement. Because of the regular succession of cycles, rhythm is a major characteristic of mastication. The rhythm of mastication is generated by a brain stem central pattern generator (CPG) [1], which activates a motor program coordinating the activities of the jaw, tongue and facial muscles [2]. The masticatory program adapts its output to the properties of the food being chewed, including the size of the food sample introduced in the mouth, its hardness and other physical properties that cause the sensations of texture [3–11]. Adaptation of the motor program also occurs continuously ⁎ Corresponding author. Tel.: +33 4 73 17 73 27; fax: +33 4 73 17 73 09. E-mail address: [email protected] (A. Woda). 0031-9384/$ - see front matter © 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.physbeh.2006.02.013
throughout the chewing sequence as the food properties are modified by mastication. The food acts as a stimulus exciting several types of receptor (periodontal, muscle spindle, mucosal). The sensory messages, which are conveyed to the brain stem, are used in one or several feedback loops allowing continual adaptation of the motor activities to the mechanical properties of the food which are progressively changing during the sequence [2,12]. This leads to the formation of a bolus ready-to-swallow. Finally, adaptation of the motor program is also needed throughout an individual's life to cope with the changes that occur as a result of ageing and tooth loss. The aim of this review is to describe the variations of both the jaw movements and the masticatory muscle activities observed while different groups of individuals are chewing different types of foods. The factors that induce variations in the masticatory parameters are related to either the food (sample size, hardness or rheological behaviour) or the individual (age, gender or dental health). They will be called extrinsic and intrinsic factors respectively. The term “rheological behaviour”
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refers to the science of rheology. This science is a branch of physics that studies the stress/strain relationship of materials. It describes properties such as elasticity, plasticity or brittleness. Other factors such as the time of day, appetite, liking/disliking of food, flavour, previous experiences, education and many others that also modulate the masticatory function will not be considered in this article. 2. Recording mastication Many methods can be used to record masticatory function. Most frequently, mastication is monitored by kinematic and electromyographic (EMG) recordings. The former gives information about jaw movements and the later follows bioelectrical activities of the masticatory muscles which are known to be closely related to the forces developed during the course of mastication [13,14]. The use of videography to record mastication has been validated in different groups of subjects [15,17]. It offers the advantage of being less intrusive than EMG or kinematic recordings which is particularly important for anxious or other special patients. It is also easier to use in a dental clinical setting and it gives information about the soft tissues functions such as lip closure [16,17]. The function of the jaw muscles during chewing can also be inferred by recording the force during chewing [see Ref. [18]] or during maximal biting [19]. The function of the tongue and
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other soft tissues was recently observed with videofluorography [20], by observing the orientation of non edible material in the mouth [21] or by observing the mixing or positioning of differently colored materials [22,23]. Recently, ultrasonic echo-sonography was used to observe the soft tissues [24]. All these recordings illustrate the rhythmical nature of mastication. During one sequence, the recordings often show intermediate and final deglutitions as well as changes of the masticatory side (i.e. from left to right or vice versa) (Fig. 1). They also indicate that a clearance stage exists which starts after the final deglutition and is characterized by non periodic muscle activity [25,26]. 3. Grinding and crushing the food At the end of the sequence, the food bolus must be smooth, deformable and cohesive [7,11]. This is required to facilitate harmless passage of the bolus through the aero-digestive crossing and then through the esophagus. To obtain such a food bolus, the food must be transformed into many small-sized particles bound together by a mixture of saliva and liquids derived from the food itself [7]. Recent studies [27,28] or reviews [29] in young healthy subjects have shown that the particle size distribution of ready-to-swallow food boluses displays no significant intra-individual variability and only a very small inter-individual variability. This shows that a food
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Fig. 1. Example of a complete masticatory sequence recording obtained during chewing of a plastic food product. The six traces are, top to bottom, lateral and vertical mandibular movements, electromyographic (EMG) activity of right and left masseters, and right and left temporalis muscles. Black circles (●) indicate larger EMG activity probably corresponding to intermediate swallowings. Stars (⁎) mark contro-lateral mandibular deviation due to re-positioning of the food bolus.
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bolus has to meet precise conditions before swallowing can be triggered. These conditions may be considered as a vital requirement, since dysfunctional deglutition, which is known to be linked to a high morbidity level [30,31], can otherwise occur. In contrast to this small intra- and inter-individual variability that occurs during the formation of the food bolus, is the large amount of variability that exists in masticatory parameters as a result of the many factors which have been shown to influence mastication. 4. Effects of intrinsic factors 4.1. Inter- and intra-individual variations of masticatory parameters Numerous researchers have described a large variation between individuals for all physiological parameters of mastication (number of cycles, total electromyographic activity during a sequence, sequence duration, masticatory frequency, vertical and lateral amplitudes of the mandibular movement) [32–35]. There are, however, no significant differences between the values of the masticatory parameters for a given individual who is asked to chew the same food several times. The large variation between individuals and the lack of a significant difference for the same individual, after several repetitions, have been clearly shown by using well controlled food stimuli and strict inclusion criteria in order to exclude, as much as possible, non-controllable factors which could explain some interindividual variability [32,35]. 4.2. The effects of gender on mastication There are differences between genders for several parameters: males display higher EMG activities per cycle and per sequence, higher vertical amplitudes and a slightly higher masticatory frequency during a sequence. No difference between males and females has been noted for the total number of cycles constituting a masticatory sequence [36–39]. 4.3. The effects of ageing on mastication The consequence of ageing on masticatory function must be separated from confounding factors such as missing teeth or other independent illnesses. In spite of a known decrease of the maximal bite force [40–42] and a loss of masticatory muscle mass [43], ageing alone has little impact on the ability of subjects to reduce food into small particles [42,44–48]. Thus, the purpose of chewing, which is to make a smooth, deformable and cohesive food bolus [7], is still achieved despite ageing of the masticatory apparatus. There are, however, some adaptations that occur with age which result in a modification of the masticatory parameters. The number of cycles [49] and the total EMG activity during a sequence increases with age [39]. The EMG activity per cycle does not change with age and still adjusts to the hardness of the food [39]. The frequency of the cycles during a masticatory sequence also remains constant with age [39,50].
4.4. The effects of dental state on mastication The number of teeth and the quality of the contacts, between teeth belonging to the lower and upper jaws, is of course of primary importance. Decreased masticatory performance or impaired chewing function have been described in subjects with either dental malocclusion [51,52], temporo-mandibular disorders [53] or a decreased number of teeth [44–47,54–56]. When all natural teeth have been replaced by a removable prosthetic device, denture wearing individuals failed to adapt to this new situation in spite of an increase in the number of chewing cycles, duration of a masticatory sequence and EMG activity per sequence [48,56–59] compared to subjects with natural teeth. In addition, denture wearers did not adapt to an increase in food hardness, had a slower masticatory frequency compared to dentate subjects [48] and may choose not to eat some hard foods such as meat [60]. 5. Effects of extrinsic factors 5.1. Food is a complex stimulus The central command of mastication is modulated by peripheral inputs [[1,61–64] and see reviews [5,12]] so that the masticatory motor output adapts to the characteristics of the chewed food [63,65–67]. Food is, however, a very complex stimulus since many of its characteristics, for example, texture, flavour, size, shape, influence mastication. In addition, food is difficult to reduce to a single physical dimension as can be done, for example, with light or vibration in studies about vision or proprioception. A first step toward simplification is to only consider the mechanical properties of the food. It is for this reason that hardness has frequently been chosen as the studied food property. Many authors have used natural foods placed on a graded scale for hardness [60,66,68,69]. Hardness is, however, a loose term and it is not clear whether the masticatory response to a particular product is in response to the hardness of the product and/or to some other textural property (elasticity, plasticity, stickiness, brittleness to name a few). To better control these food properties, non alimentary models, usually made with elastomers or waxes were used [70–76]. Since these artificial products are impossible to swallow and, as a result, may modify some events in the masticatory process, their use strongly limits the observation of natural chewing. 5.2. The effects of hardness versus rheological behaviour on mastication: the use of model foods So far, two approaches have been used to improve the understanding of the natural food stimulus/masticatory response link. The first approach attempted to link food properties with food breakdown during mastication. The ratio of the square roots of toughness and modulus of elasticity was proposed to best express the resistance to food breakdown during mastication [69,77]. These authors strongly suggested that this mechanical index might well reflect the sensory stimulus utilized in the ongoing modulation of the central pattern
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different hardness levels [66,78–82]. Recently, a better control of the rheological properties was obtained by using brittle food products in the form of three tablets exhibiting different hardness [75] and visco-elastic (predominantly elastic) gelatine based model foods with a four point scale of hardness [10,35]. In these studies, differences in masticatory parameters between several model foods could be related directly to the hardness because the other textural properties of the food were constant. It was, however, not possible to reveal in a single experiment the independent adaptation of masticatory function to changes in the rheological behaviour of the foods versus hardness. This has
generator. The second approach attempted to uncover the changes in the masticatory parameters that are produced by a relatively pure, single rheological stimulus. This was done by developing edible model foods that allowed the dissociation of hardness from other textural properties. These model foods had to display rheological behaviours that were as pure as possible, e.g.: brittleness, elasticity or plasticity. In addition they had to display a homogeneous structure, a reproducible texture, constant shape and size and had to exhibit a full hardness scale. A first step towards this goal was reached when some authors used natural chewing gums sometimes with two Elastic
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Fig. 2. Mean values and S.E.M. observed for total EMG activity per sequence, mean lateral and vertical amplitudes, and closing velocities during chewing of an elastic (in A, C, E and G respectively) or a plastic (in B, D, F and H respectively) product. E1, E2, E3, E4 and P1, P2, P3, P4 are products of increasing hardness with elastic or plastic rheological characteristics, respectively. Black columns represents elastic (E4) and plastic (P2) food products of comparable mechanical hardness values. The results of Multiple Linear Regression (MLR) analyses, performed with hardness and type of rheological behaviour as explanatory variables, are presented in front of the corresponding masticatory parameters. ⁎: p < 0.05; ⁎⁎: p < 0.01; ⁎⁎⁎: p < 0.001.
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been done recently in an experiment using two sets of model foods displaying different rheological behaviours, i.e., elasticity and plasticity, with each model food being presented on a four point graded scale of hardness [83]. These two model foods were manufactured to display well known rheological behaviours. They were jellied confectioneries for elastic products and hard caramel confectioneries for plastic products. The range of hardness and the rheological behaviour were both verified and controlled using a compression test and the range of hardness was further evaluated using a visual analogue scale. The values obtained with the two hardness measurements were shown to be closely correlated. It was, therefore, possible to selectively study the impact of the elasticity vs. plasticity on a variety of recorded variables, which all describe the characteristics of the chewing motor behaviour. The results showed that variables associated with the jaw muscle activity (number of cycles, duration of the sequence, EMG activity during each cycle or during the whole sequence) were primarily related to the hardness of the test foods, while the shape of the movement trajectories (vertical amplitude, lateral amplitude, closing velocity) and the masticatory frequency were preferentially adapted to differences in the rheological behaviour between the elastic vs. plastic products (Fig. 2). 5.3. The effects of food sample size on mastication The thickness of the food sample and the volume of the initial mouthful have an effect on many parameters of the
masticatory function. Most of the parameters increase with the size, weight or volume, of the mouthful but those related to mandibular movements are the most influenced. The most obvious change induced by an increase in the food size is an increase in vertical amplitude [6,84–89]. 6. Masticatory frequency may be a key parameter for the evaluation of an individual's masticatory function A summary of the effects of the different factors on the main parameters of mastication is shown in Table 1. In a healthy subject, mastication is able to adjust to various individual and/or environmental conditions so that the masticatory function is satisfactorily achieved. When mastication is not able to fully adapt, the masticatory function may not be fulfilled resulting in an insufficiently prepared bolus. The particle size distribution of the food bolus is shifted towards coarser particles [29]. The consequences on the general health of an individual with impaired mastication have not been fully explored yet, but recent reviews suggest that they are serious [90,91] and there is a strong suspicion that a reduced nutrient availability occurs [92]. Two criteria may be proposed to detect an impaired mastication. The first criteria could be the detection of a large change in the distribution of the food bolus particle sizes. The second criteria could rely on a change in cycle frequency. Frequency is the chewing parameter with the most repeatable values between trials in a single individual [10,35,38,48].
Table 1 Schematic representation of the adaptation of mastication
Number of cycles
Sequence duration
EMG activity EMG activity Masticatory /sequence /cycle frequency
Vertical amplitude
Lateral amplitude
Closing velocity
9, 10, 69, 79, 83, 84
10, 81, 98
10, 32
83
83
83
6, 71, 85, 89
85, 89
Extrinsic factors
Hardness (from soft to hard)
10, 65, 66, 79, 81, 83
10, 25, 79, 83, 100
10, 65, 79, 83
(from elastic to plastic)
Sample size
83
6, 84–86
83
6
83
10, 79, 80, 83
83
83
82, 85, 88
6, 87, 89
Depends on food
Age Intrinsic factors
10, 65, 78, 83
Physical properties
39, 44, 49
39, 44, 49
39, 49
39, 49
39
39
38, 39
36, 38, 39, 94
39, 50
Gender (from female to male) 36–39
39
39
Depends on food
Tooth loss (edentate) 48, 101
48
48
48, 56, 99
36–39
36
36,37
* 48, 56, 101, 102
101
Responses of the major electromyographic and kinematic parameters to the main extrinsic (three top lines) and intrinsic (three bottom lines) factors. Four signs are used to display the effects of the extrinsic and intrinsic factors on masticatory parameters: downward pointing arrows indicate a decrease, slightly or strongly upward pointing arrows indicate a slight or strong increase in the values of the masticatory parameters. An equal sign indicates no change. ⁎There is more decrease with harder foods.
A. Woda et al. / Physiology & Behavior 89 (2006) 28–35
Frequency has been shown to vary only slightly if at all when a given individual is chewing a given food. It remains constant even when the hardness of the food is increased, so long as the rheological behaviour of the food is constant [10,39,56,83,93]. The lack of variation in the masticatory frequency also applies when the intensity of the taste of the food varies [26]. Contrasting with the almost complete stability of the chewing frequency for a given food and a single healthy individual, are all other parameters of mastication which are modulated by an increase in hardness. For example, ageing brings about a change in all variables related to muscle work (number of cycles, sequence duration, EMG per sequence, EMG per cycle) although masticatory frequency is not modified [39,48] (Table 1). It therefore appears that mastication frequency is the only parameter of mastication that does not adapt to neither a change in food hardness nor ageing. The stability of chewing frequency only applies to healthy persons because individuals wearing full dentures [48], suffering from temporo-mandibular disorders [53] or disabled persons with Down's syndrome [15], all display varying levels of decreased mastication frequency compared with healthy controls. The stability of this masticatory parameter in healthy subjects indicates that it could be a key parameter for the evaluation of an individual's masticatory function. It has been suggested that a lack of change in mean frequency could be used as a criterion of good masticatory health and alternatively, a large variation from the mean frequency values could be indicative of an impaired masticatory function [48]. It is important to note, however, that the use of frequency as a criterion for masticatory function could only be applied to a given population and for a given food because cycle frequency displays a large inter-individual variability, [35,65], significant differences between men and women [38,39,94] and changes with mouthful size or the rheological characteristics of natural foods [20,65,83,94–97]. 7. Future directions Considered as a whole, these results constitute a database that summarize our understanding of the modulation of mastication in response to changes in the individual's oral physiology and food texture. Many of these results were obtained from healthy individuals, using controlled stimuli giving reproducible responses. These results provide a controlled tool for studying other groups of individuals. In particular, subjects with impaired mastication can now be studied in comparison with a control group characterised by a known physiology of mastication. This should lead to the development of masticatory function tests which should be easy to use in a clinical environment. These data will also assist in the development of a robotic device which could be either calibrated or trained to simulate the physiological function. Such a device would allow researchers to perform experiments difficult to carry out in humans. This type of device could be used to predict human texture perceptions of new foods, once the masticatory adaptations to changes in food texture are completely understood. It could also be used to create an
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Further reading [1] Mizumori T, Tsubakimoto T, Iwasaki M, Nakamura T. Masticatory laterality — evaluation and influence of food texture. J. Oral Rehabil 2003;30:995–9. [2] Shi CS, Ouyang G, Guo TW. A comparative study of mastication between complete denture wearers and dentate subjects. J Prosthet Dent 1991;66:505–9. [3] Feine JS, Maskawi K, De Grandmont P, Donohue WB, Tanguay R, Lund JP. Within-subject comparisons of implant-supported mandibular prostheses: evaluation of masticatory function. J Dent Res 1994;73:1646–56. [4] Jemt T. Chewing patterns in dentate and complete denture wearers recorded by light emitting diodes. Swed Dent J 1981;5:199–205. [5] Jemt T, Karlsson S. Mandibular movements during mastication before and after rehabilitations with new complete dentures recorded by lightemitting-diodes. Swed Dent J 1980;4:195–200.