Cambios en Masticacion Asociados A Edad
Cambios en Masticacion Asociados A Edad
Cambios en Masticacion Asociados A Edad
Review
Age-related changes in mastication
M. A. PEYRON*, A. WODA†, P. BOURDIOL† & M. HENNEQUIN†‡ *Human Nutrition Unit,
Institut National de la Recherche Agronomique, Saint Genes-Champanelle, †Universite Clermont Auvergne, CROC, Clermont-Ferrand, and
‡
CHU Clermont-Ferrand, Clermont-Ferrand, France
SUMMARY The paper reviews human mastication, adaptation possibilities remain operant. The third
focusing on its age-related changes. The first part part reports on very aged subjects, who display
describes mastication adaptation in young healthy frequent systemic or local diseases. Local and/or
individuals. Adaptation to obtain a food bolus general diseases such as tooth loss, salivary defect,
ready to be swallowed relies on variations in or motor impairment are then indistinguishably
number of cycles, muscle strength and volume of superimposed on the effects of very old age. The
emitted saliva. As a result, the food bolus displays resulting impaired function increases the risk of
granulometric and rheological properties, the aspiration and choking. Lastly, the consequences
values of which are maintained within the for eating behaviour and nutrition are evoked.
adaptive range of deglutition. The second part KEYWORDS: mastication, food bolus, granulometry,
concerns healthy ageing. Some mastication swallowing, ageing, nutrition
parameters are slightly modified by age, but ageing
itself does not impair mastication, as the Accepted for publication 22 December 2016
The paper reviews the mechanisms by which mastica- passage through the upper oesophageal sphincter dur-
tion adapts to varied conditions in healthy individu- ing deglutition. During food selection, visual and
als. It goes on to describe how this adaptation occurs olfactory cues are compared with already acquired
in healthy ageing people, and in aged people with cognitive eating-related knowledge and habits. After
accompanying local or general pathological condi- selection, the food is portioned into mouthfuls, indi-
tions. Lastly, the consequences of impaired mastica- rectly with fingers or an implement (knife, fork,
tion on eating behaviour and nutrition are briefly sticks, etc.), or directly using the front teeth. Once in
discussed. the mouth, a mouthful undergoes a four-step
sequence which was first described by Hiiemae and
Palmer (1). The first step is transport from the front
Adaptation of mastication in young
teeth to the molars (stage I transport). The mouthful
healthy individuals
is analysed by taste, retronasal olfaction and oral
Mastication serves the main purpose of preparing a receptors of the somatosensory system. Crucial chemi-
food bolus acceptable for swallowing and also acts to cal and rheological properties of the food are sensed,
initiate various digestive and metabolic activities and the brainstem mastication centre is programmed,
either within the mouth itself, such as starch diges- or the food is rejected if perceived as noxious or
tion by amylase, or through cephalic phase reflexes, undesirable. In the second step, the food is trans-
which prepare the digestive tract for the arrival of formed into a food bolus by the actions of the teeth,
food. Mastication must, however, be included in the with the aid of saliva and lingual and facial muscles;
broader concept of ingestion, which starts with the this is mastication proper, also termed trituration. In
choice and selection of a food and ends with its the third step, the chewed food is transported
rearward through the fauces to the oropharyngeal swallowing an unprepared bolus due to aspiration,
surface of the tongue (stage II transport) where it choking or increasing load on the digestive system
reaches the valleculae and is accumulated. The fourth (10, 11).
step is deglutition proper, with opening of the upper To be swallowed safely, and above all without risk
oesophageal sphincter. Steps 2 and 3 actually occur to of aspiration, the food bolus must also possess certain
a large extent simultaneously, the bolus being moved physical characteristics, such as sufficient plasticity to
cyclically upward and forward on the tongue surface, be easily deformable, a surface lubricated enough to
returning through the fauces into the oral cavity be easily moved, and a sufficiently cohesive structure
while the mastication proper is taking place. This ini- to avoid particle dispersion and be hazard-free. The
tial description (1) emphasises the complexity of the need to obtain a critical, optimal particle size before
many subfunctions in the oral part of the ingestion swallowing (7, 12, 13) and to reach the required food
process and the intimate relationships between them. bolus state by whatever means are available explains
A very high proportion of the mastication studies in the broad variability of physiological parameters
humans have focused on mastication proper. How- (13–15). It is noteworthy that subjects do not stop
ever, a comprehensive view of the effect of age must chewing to trigger deglutition merely after the
encompass the entire process. required mean particle size has been reached. They
From the above description, we see that ingestion actually masticate longer, increasing the number of
of food comes under a three-checkpoint control by cycles, because they need to achieve all the rheologi-
which food may be consciously refused. Food selec- cal conditions described above, that is viscosity, cohe-
tion is first made by individuals expressing their per- siveness and stickiness of the final bolus (16–18), by
sonal choice when shopping for food or when mixing the solid particles with saliva and juice
accepting or declining food offers. A second check- expelled from the crushed food. This probably
point is crossed during stage I transport, and a third accounts for the weak correlation between number of
one triggers step 4, that is the deglutition proper. cycles and pre-swallow median particle size (8, 19). A
After this last barrier, food is irreversibly delivered to recent study demonstrated the role of these rheologi-
the gastrointestinal tract and can be partly refused cal factors in prolonging mastication, even though the
only by vomiting. final/optimal particle size had already been reached
To cross the last checkpoint, that is the deglutition (20). If these several required food bolus properties
proper, a food bolus needs the deglutition centre’s cannot be attained, subjects either avoid eating the
‘go-ahead’, signalling that the bolus is sufficiently well food, which they deem difficult to chew, or they
prepared to be harmless and easily swallowable. It is swallow insufficiently destructured/disrupted foods.
well prepared when a certain degree of mechanical
degradation of the food has been reached in the
mouth. For example, a mouthful of hard, brittle food
must be broken down into many small particles. Col-
lecting the food bolus just before swallowing is
accordingly crucial to exploring mastication. An
important characteristic used to describe the bolus just
before swallowing is its median particle size (2–4).
Importantly, several converging studies have pointed
to the narrow variability of particle size in the pre-
swallow food bolus (Fig. 1), unlike the broad variabil-
ity of some physiological parameters such as duration
of the sequence, number of strokes, and the elec-
tromyographic activity of masticatory muscles (Fig. 2) Fig. 1. Relationship between particle size (d50) and number of
cycles for peanuts. The medians of the particle size were
(3, 5–8). Similar low between-subject variability was
obtained from 30 boluses (30 subjects) collected after 10 cycles
also observed with other types of food such as meat (white dots in the vertical dashed box) and from 60 boluses (30
(9). The narrow variability of pre-swallow bolus parti- subjects) collected at the deglutition time (black dots in the hori-
cle size may be explained by the vital risk of zontal dashed box) (from Mishellany-Dutour et al.) (8).
Table 1. Mastication adaptation. Responses of the major electromyographic and kinematic parameters to the main subject and food
characteristics (effects on masticatory parameters: downward arrow indicates a decrease; gently or steeply upward-pointing arrows
indicate a slight or strong increase; an equal sign indicates no change). The two bold equal signs emphasise the diagnostic interest of
the corresponding physiological responses (from Woda et al.) (15)
component are affected (51). Despite all these slow, proportion of recruited muscle fibres compared with
incremental changes, ageing alone has little impact on the total number of motor units. The jaw closing mus-
the ability of subjects to grind brittle foods into small cles of older people are thus probably working closer to
particles, (14, 37, 52, 53). During healthy oral ageing
with no marked oral disorders, old persons still produce
a food bolus ready for swallowing. Contrary to what
might be expected, the sizes of particles in a bolus felt
ready to swallow by the subjects do not increase with
age (54) and indeed tend to decrease, at least for some
foods (13, 14). It is not clear why elderly people still
achieve maximal comminution (pulverization) before
swallowing these foods. In sum, it appears that only
minor adaptations are needed to compensate for the
physiological changes induced by ageing in subjects in
good health (14, 15, 24, 55). The main adaptation of
the masticatory process to healthy ageing is an
increased number of masticatory cycles (13, 14, 56–
60). This gradual increase adds about three more cycles
per sequence every 10 years (59) (Fig. 3). Despite a Fig. 3. Age-related increase in masticatory cycle number. Each
decrease in the maximal bite force (37, 44, 61) and point represents age and the number of cycles collected from
masticating a soft elastic model food until deglutition by one
muscle mass (43), the EMG activity recorded for mas-
subject. The regression line is represented. Linear regression
seter and temporalis muscles in each cycle did not vary analysis showed that the total number of cycles in a sequence
with age in fully dentate aged subjects chewing brittle increased significantly with age (P = 00001), but gender had no
foods (13, 59). This is thought to be due to an enhanced effect (P = 0202) (from Woda et al.) (15).
their maximum capacity than those of younger sub- chewing efficiency. Two similar analyses showed that
jects. It was also found that EMG activity was still chewing efficiency decreased with the number of
adjusted to food hardness, showing that elderly persons occlusal contacts (24, 67, 68), confirming many previ-
with a good oral state maintained their potential for ous reports (14, 69, 70). Several studies also showed a
adaptation of mastication to food properties (59) strong negative effect of periodontal disease on masti-
(Table 1). The larger functional areas of the tooth arch cation efficiency (68, 71, 72). The ultimate condition is
observed in the fully dentate elderly is caused by occlu- represented by full denture wearers, who strive to
sal dental wear. It may help maintain masticatory effi- adapt to their lack of natural teeth (13, 24, 73). In this
ciency in these dentate subjects (62, 63). Masticatory group of subjects, masticatory efficiency was decreased
frequency was also shown to remain constant through- by 50–85% compared with subjects with intact denti-
out normal ageing (56, 59). The transformation of food tion (55, 69, 74–77). This effect was fully confirmed by
into a bolus actually requires an increase in the energy analysing the particle size distribution of the food bolus
spent by muscles to produce a food bolus that can be just before swallowing. Denture wearers make a much
safely swallowed (60, 64), as elderly persons need more coarser bolus than dentate subjects (13, 52, 53, 78–80).
time and more strokes. Old persons with satisfactory Mastication by denture wearers reflects an effort to
oral health therefore maintain their ability to produce a adapt to their deficient masticatory apparatus, even
food bolus made of small particles and adjusted for with an easy-to-chew food. An increase in the number
safe swallowing (13, 14). These conclusions are of chewing cycles, duration of mastication sequence
drawn from studies conducted with brittle foods and and EMG activity per sequence is found in studies with
may apply only partly to other types of food such as denture wearers chewing various foods (21, 73, 74, 80,
meat. The decreased EMG activity per cycle observed 81). Concerning the EMG value per cycle, comparisons
with tough meat is insufficiently compensated for by with dentates have variously found no significant dif-
an increase in the duration of the sequence and total ference, (64), an increase (73) or a decrease (78, 82,
EMG activity, leading to a decreased masticatory effi- 83). This suggests that the level of EMG activity per
ciency and a less well-prepared food bolus than in cycle reflects an optional process used by aged denture
young subjects (65). wearers to strive, in a food-dependent manner, to make
a satisfactory bolus. Despite their deficiency, they are
still able to adapt their mastication to an increase in
Effect of ageing on mastication in the
hardness of certain foods by increasing the number of
elderly with accompanying local and
cycles and thereby the total muscular activity during
systemic conditions
the masticatory sequence (73, 74, 83). However, this
Three factors have a major impact on masticatory func- adaptation may not suffice for very hard-to-chew foods
tion in elderly persons: the number of natural antago- such as raw carrots (13). In these cases, subjects reject
nist teeth, the quantity or/and quality of saliva and the food or display a markedly decreased EMG activity
impairment of the motor apparatus. These factors are, (83), indicating that non-prepared pieces of food are
however, relatively independent of ageing, as evi- being swallowed. These different findings suggest that
denced by the broad variability in the number of natu- the adaptation ability of denture wearers was over-
ral teeth in the elderly, for example (38). Nevertheless, stretched and that many full denture wearers lie out-
each of these three factors is largely correlated with side the normal physiological range. Full denture
ageing, and from a pragmatic point of view need to be wearers must therefore be considered as a group of sub-
included when considering mastication in the elderly. jects with strongly impaired mastication (84, 85).
Dental wear can also be an important component
of masticatory efficiency (47), as it increases the sur-
Dental state
face area of occlusal contact. Contacting surfaces,
A covariance structure model used in a study of masti- which depend on occlusal wear, are closely related to
catory performance carried out with 631 subjects (37), masticatory performance (70, 86). Consequently, the
and multiple regression analysis carried out after quality of the fit between upper and lower teeth may
observing 1288 subjects (66), showed that the number improve in an ageing population with healthy dental
of posterior teeth was a key factor in predicting arcades, as dental wear progresses with time (87, 88).
Although not specific to elderly persons, tooth of the total saliva flow, is preferentially stimulated by
replacement by implants or implant-retained dentures mastication. It maintains its level of saliva output
is commonly found in these subjects. Several reviews until the mean life expectancy is reached, unlike sub-
point to greatly improved mastication and patient sat- mandibular/sublingual secretion, the flow rate of
isfaction over a long period (25, 89). Masticatory per- which decreased with ageing when recorded after
formance as measured by granulometry and maximal 5 min of stimulation (96–99). The pooling of the two
bite forces reached values similar to those found in saliva secretions explains why in normal conditions
dentate controls. Furthermore, the adaptation of mas- saliva output decreases only slightly with age (96, 99–
tication returned to near normal, as shown by the 101) particularly when induced by citric acid, a stimu-
decrease in the number of cycles and muscle activi- lation that preferentially activates submandibular/sub-
ties. The return to normal was, however, incomplete, lingual glands (98). In the short term, less than
probably owing to the lack of periodontal receptors 5 min, no direct age effect is observed on the total
(90) and possibly also to a lack of chewing training salivary flow rate at rest or during parafilm or meat
(91), as patients may go on using old praxis with new chewing stimulation (62, 91, 100, 102).
anatomy.
Motor impairment
Salivation
Dysfunction of tongue motor skills and lack of tonic-
The common complaint among the elderly of a sen- ity of muscles involved in masticatory movements
sation of mouth dryness may have several causes also reduce masticatory efficiency (103–105). The
(25, 65, 92). Many therapies, more frequent in an tongue plays an important role in the collection of
ageing population, may have xerostomia as a side sensory information and in motor activity. It can
effect. This is the case for chemotherapy, radiother- crush food on its dorsal side against the hard palate,
apy and psychotropic or other types of drug known sort particles that are ready to be swallowed, gather
to induce dryness of the mouth. Elderly persons them into a food bolus, mix them with saliva and
also suffer more frequently than younger subjects help clean the mouth and teeth after food has been
from autoimmune diseases such as Sj€ ogren’s syn- consumed (103). Impaired function of lingual, jaw
drome, characterised by a paucity of saliva flow and other oral muscles involved in mastication can
(93). Tooth loss has also been reported to induce be observed in many conditions, most of them being
xerostomia. There are conditions such as burning more prevalent in elderly persons than in younger
mouth syndrome in which the subjective report of subjects. Parkinson (106, 107), stroke (108), Alzhei-
a dry mouth sensation conflicts with a normal sali- mer (109) and other neurodegenerative diseases are
vary flow rate. The sensation of xerostomia may good examples. Edentate subjects with insufficiently
then be due to a neuropathic modification of oral trained masticatory muscles are other common
mucosa nerve terminals or a modification of saliva examples (15, 25).
composition (93).
Xerostomia and other dysfunctions related to saliva
Swallowing: age-related changes
supply may influence the masticatory process nega-
tively by making it impossible to gather food into a In healthy young subjects, swallowing involves a cas-
bolus before swallowing. In normal conditions, for cade of oropharyngeal muscle contractions in a closely
example in healthy ageing persons, measures made at coordinated sequence (110, 111). In ageing adults,
rest, during parafilm and meat chewing, showed that changes in the swallowing function occur through
chewing increased the salivary flow rate at all ages as adaptation of the temporal features of this muscular
a component of the adaptation of the masticatory contraction sequence. Ageing brings a deterioration of
activity to food texture (62). It is assumed that older the tactile sensations (112, 113), and also a significant
adults compensate for their loss of muscular force decrease in perceptions of bolus viscosity, because of
and/or teeth by chewing for a longer sequence, as this either an aged-related loss in the density of the sen-
increases their salivary output (79, 94, 95). It is note- sory receptors involved in viscosity perception, or a
worthy that parotid secretion, which accounts for half higher sensory threshold of these receptors (28, 114,
115). The decreased perception of bolus viscosity noticeable at the upper oesophageal sphincter, which
could help explain the changes observed in swallow- takes longer to relax after swallowing, and undergoes
ing function in aged people, as bolus viscosity may a modification of its contraction pressure (121, 131).
influence the timing of deglutition (27, 28). All three The oesophagus itself is marked by an increase in its
stages of deglutition, oral, pharyngeal and oesopha- non-propulsive peristaltic movements and a delay in
geal, are concerned by the temporal modifications emptying. These mild alterations do not present any
due to the ageing process. Although these temporal danger to the ageing individual, and more pro-
modifications remain sometimes hardly noticeable in nounced disorders are always connected with an
healthy individuals, ageing brings a reduction in mus- underlying pathology or a deterioration in general
cle mass related to sarcopenia (116–119), which may health (132). Conclusions on the effects of age on
be responsible for some deterioration in the swallow- oesophageal motility remain conflicting (133–138),
ing process (120, 121). Slowing of swallowing as a but dysphagia nevertheless remains more frequently
whole, or in some of its motor events, has been encountered in the elderly than in young adults
repeatedly reported (111, 122–124), see review in (121, 139).
Gleeson (125). For instance, parallelizing a bite force
demotion related to ageing in old adults, the tongue
Indicators for a healthy masticatory
thrust, characterizing the main act of swallowing,
function and effect of ageing on
tends to slow down (123), adapting to a diminution
mastication-related deficient nutrition
of the maximal pressure it can develop (126). Modifi-
cations in the cerebral white matter tracts, observed Adequate indicators must be used for each stage in
with magnetic resonance imaging, are considered the eating process. Kinetic and dynamic features of
indicative of a slowed swallowing syndrome or pres- mastication have been evaluated with the usual
byphagia (127). The initial measures of tongue pres- physiological methods such as electromyography, jaw
sure on the hard palate seemed to echo what is movement tracking, video-recording or bite force
known about the forces in play during mastication in recording. The quality of mastication completion has
the elderly. The forces applied during the function been evaluated using at least five different methods:
were first described as similar to those in younger (i) self-administered questionnaires, which can be
subjects. However, the difference from the maximal used in large epidemiological studies and in well-
force was smaller in the elderly, suggesting that the characterised populations, but are limited by their
older persons were working closer to their maximum tendency to be overoptimistic, and be weakly corre-
‘to maintain the critical pressures necessary for safe lated with objective evaluation methods (70, 81,
and effective bolus passage through the oropharynx’ 140); (ii) median particle size determined by food
(128). More recent studies using ultra-thin sensors bolus granulometry (14), an objective measure of
indicate age-related differences in tongue pressure mastication outcome that also offers a cut-off value
production during swallowing (129). It can be con- of normality, the masticatory normative indicator
cluded that further weakening of the function by age- (MNI), which has been determined with raw carrots
related illness may put geriatric patients at higher risk or artificial food (84, 85), and it is, however, too
of dysphagia. demanding to be routinely used in a dental surgery
The pharyngeal stage of deglutition is apparently and in large epidemiological studies; (iii) a much
delayed and shortened, with a short opening dura- easier and promising test under development based
tion of the pharyngo-oesophageal sphincter, a slow- on the calibration of a scale of defaults assessed after
ing down of the pharyngeal peristalsis movements mixing a two-coloured chewing gum (91, 141, 142);
(amplitude and speed), hypotony of the vocal cords (iv) measurement of sugar extracted from chewing
and a weakened cough reflex. Nevertheless, ageing is gum (139, 143), although its reliability is debatable,
not in itself the main source of swallowing disorders, as sucking will extract sugar as well as chewing; and
even though hypotonia and muscle strength reduc- (v) the number of functional teeth participating in
tion are influencing factors (129, 130). The oesopha- the chewing function expressed as functional units
gus stage of the swallowing function is apparently (144), which appears to be a key predictor of masti-
not modified by ageing. Few modifications are catory performance (37).
Evaluation of mastication must take into account means that incomplete information about food being
wider concepts such as the possible links between oral processed is sent to the brain. As a result, the
health and nutrition. Evaluation of oral health is a mouth/brain/digestive tract reflexes cannot anticipate
useful indicator in the elderly population. El Osta the arrival of the food at the upper organs of the
et al. (145) suggested that the perception of xerosto- digestive tract. A few reports have shown decreased
mia, the number of functional units present in the oesophagus clearance and stomach emptying with
mouth, and the score obtained with the Geriatric Oral insufficiently chewed foods. Similarly, the morbid
Health Assessment Index (GOHAI) (42, 146) should consequences on the digestive organs of sending
be considered as the most appropriate oral health large particles to the stomach has not been fully
indicators. Such evaluation of oral health could be evaluated, see reviews in Mioche et al. (47), Feine
combined with the MNA (Mini Nutritional Assess- and Lund (89), Peyron et al. (24), van der Bilt (25),
ment) to identify elderly persons at high risk of mal- Remond et al. (34).
nutrition reliably and easily (147, 148). The measure It has been stated for decades that despite over-
of bioavailability of nutrients in the blood (149–151) whelming evidence of a correlation between mastica-
must finally be emphasised, as it is a gold standard for tory deficiency and malnutrition (152, 153), a causal
the role of mastication in nutrition. relationship remains to be demonstrated (34, 65).
The prevalence of malnutrition and risk of malnu- Based on a systematic review with 11 studies using
trition in the elderly were evaluated in a systematic a multivariate approach, van Lancker et al. (154)
review. The mean prevalence of malnutrition concluded that tentative evidence supported an inde-
depended on whether the elderly persons were living pendent association between oral health status and
in an institution (2% for malnutrition, 9% for risk malnutrition in elderly residents of a long-term care
of malnutrition) or independently (24% and 45%) facility. One study showed that diet depended on
(147). The role of impaired mastication in the diges- masticatory function according to number of teeth
tive process and nutrient availability has long been (149). However, little modification was seen in nutri-
repeatedly suggested. However, proof of a causal ent concentrations in blood. A causal relationship
relationship between mastication and malnutrition is between masticatory function and blood availability
still awaited. Figure 4 schematises the ways in which of nutrients was shown in a trial design comparing
age can be related to masticatory-induced malnutri- full dentures with and without supporting implants
tion. Several points emerge as follows: (i) the effects (150). Further research is needed to seek evidence
of ageing may be seen in many different ways, for a causal relationship between mastication, oral
sometimes directly but more often indirectly through health and malnutrition. Several points must, how-
comorbid events. The corollary is that no single ever, be clarified for this approach. The common
cause explains more than a small part of the total assumption that the oral stage of eating is a minor
effect of masticatory-related age effects on nutrition, function gainsays the obvious vital role of feeding.
(ii) mastication deficiency through ageing can result Eating is so important that evolution has given us
from three main mechanisms: fewer contacts overlapping functions shared by several segments of
between natural antagonist teeth (functional units), the upper digestive tract. In this way, failure of any
xerostomia and decreased oral muscle activities, (iii) one organ does not mean starvation. Hence, mouth
defective mastication may lead to decreased nutrient and stomach may be considered as performing a
bioavailability through dietary changes; again, there number of redundant mechanical activities. For this
are many other possible causes of modified diet and reason, mouth function may have been underesti-
eating behaviour in general, so masticatory defi- mated.
ciency can explain only a part of the role of diet in
malnutrition and (iv) swallowing an insufficiently
Conclusion
prepared food bolus is a frequent occurrence, the
digestive consequences of which have been incom- This review finds that (i) fuller knowledge has been
pletely studied on either digestive diseases or nutri- gained on the control of mastication in healthy
tional outcome. If it travels too rapidly through the adults; for example, physiological adaptation to dif-
oral cavity, food bypasses the cephalic phase. This ferent external influences and internal changes has
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