Study participants

Patients with morbid obesity scheduled for bariatric surgery between September 2005 and March 2007 were proposed for inclusion. Morbid obesity has been defined as a body mass index exceeding 40 kg /m2 (or ≥35 kg/m2 with a serious factor of co- morbidity) [34]. Patients with mental, cognitive or neurological diseases, infectious oral diseases such as caries or periodontal disease, or without dentures despite having fewer than four dental functional units, were not included. All patients received instructions on diet, food consumption and advices on chewing activity in accordance of international guidelines [6].

Study Criteria

Data analysis

Statistical analysis was performed using IBM®-SPSS®19 software; statistical significance was set at p <0.05. Mean CT, CC, CF, and D50 values were calculated for each group of obese subjects before and after surgery. Verified check was performed on whether each variable was normally distributed. To assess the impact of dental status on the ability to chew and to evaluate whether the chewing pattern was modified by the instructions on increasing chewing activity, statistical analysis was carried out to detect any differences in mean chewing parameters between the subgroups of patients. For inter-group comparisons of mean presurgical D50, CT, CC and CF values, a General Linear Model procedure (dependant factors: D50, CT, CC and CF; fixed factors: dental status, type of food) followed by the post-hoc Student Newman-Keuls (SNK) were applied. The mean D50, CC, CT and CF values measured pre- and post-operatively were compared using Student's paired t-test to evaluate the impact of surgery period on chewing parameters. An ANOVA was applied to assess the impact of dental status on mean % BMI variations.

BMI variations and dental status

This study was conducted under experimental conditions that did not allow the evaluation of spontaneous changes in either food intakes, satiety feelings or nutrient availability. The BMI variations recorded three months after surgery ranged were in the same range as those reported in other studies [37], [38] and did not differ between groups with different dental status, despite a difference in chewing behaviour and bolus granulometry. To explain the lack of difference in chewing behaviour with different BMI values, it could be argued that most of the variation in the post-surgery period is directly related to surgery. The consequences of dental status on weight and nutrition in obese patients after BS need to be evaluated over longer periods than 3 months after surgery. The modest sample size of the cohort and the low follow-up rate are the limitations for such analyses, although BMI variation was not the primary goal of the study.

Effects of food properties on ability to change chewing

Hypothesis 2 was verified for carrot bolus but not for peanuts. After BS, the fully dentate subjects produced a peanut bolus with a higher median particle size despite having chewed peanuts for a longer time and for a higher number of cycles than before BS. The influence of food characteristics on the chewing process has already been described [28], [29], [39]. There are other food bolus characteristics than particle size that may help explain the time chosen for swallowing. The moderate correlation between the number of cycles and pre-swallow d50 that was seen in several studies [40], [41] may also reflect a need to reach certain rheological states, for example of viscosity, cohesiveness or stickiness, independently of particle size, in the final bolus [42], [43]. During chewing, the food pieces are reduced in size while saliva is produced to moisten the food until it reaches the ideal plasticity and cohesiveness for swallowing. Dry and hard products require more chewing cycles before swallowing than moist and soft products [24]. Peanut contain less water than carrot (around 0.5% vs 88.3 % respectively), and the consequences on bolus composition of an increase in chewing activity differ between carrot and peanuts. The increase in carrot chewing could produce juice that compensates for the additional decrease in particle size in order to satisfy the required plasticity of the pre-swallowing carrot bolus. This phenomenon did not occur with peanuts. In the absence of liquid release from the food, an increase in peanut comminution would lead to an increase of the viscosity of the peanut bolus, incompatible with the swallowing threshold. Faced with this problem, it could be hypothesized that the subjects adopt another strategy, consisting of replacing the “comminution-cycles” (chewing cycles that aim to crush the food between the teeth and to reduce the particle size) with “manipulation-cycles” (chewing cycles that aim to manipulate the food between the tongue and the palate, and to mix it with saliva and food juices). During manipulation-cycles, the peanuts particles are not crushed while saliva production is stimulated to allow the bolus to reach the ideal rheological properties to be swallowed. Each of these different strategies could possibly be interpreted as chewing cycles on video recordings. If this hypothesis could be verified for fully dentate subjects in further studies, the inability of both PD and DW groups to adapt their chewing behaviour to the food properties suggests again that dentally impaired patients with obesity should restrict their range food choices.

Ability for changing kinematics

The ability to increase chewing activity following surgery results from a voluntary, conscious motion that depends on both dental status and food. Both groups with natural teeth (PD and FD groups) increased chewing time and the number of chewing cycles for carrot, peanut, apple and banana while they did not change significantly for jelly, as was also the case for denture wearers for apple and banana. Edentulous individuals lack an important source of tactile sensory input to the central nervous system (CNS), the periodontal mechanoreceptors. Periodontal mechanoreception provides feedback on the magnitude, direction, and rate of occlusal load application for sensory perception and motor function. In addition, intradental mechanoreception provides subtle modulation of occlusal loading for further refinement of neuromotor control of jaw function. When teeth are lost, these fine proprioceptive control mechanisms are absent. The presence or absence of periodontal mechanoreception necessarily has a direct bearing on tactile discrimination. [44]. It has been shown that the discrimination threshold for micro-thickness detection is lower for natural teeth compared with prosthetic teeth. This threshold is clearly dependent on the precision provided by periodontal mechanoreception (8–20 µm), which is higher for osseointegrated implant bridges (50 µm) and significantly higher for complete-denture wearers (100 µm). It therefore appears that denture wearers cannot modify their chewing strategy with soft samples because their ability to discriminate is poor, particularly with brittle foods such as carrots and peanuts. Furthermore, wearing a denture could modify the lingual praxis required during the ingestion of soft foods such as apple and banana, particularly for upper dentures with a resin palate.

Improving dental status or changing food texture

Interactions of both food texture and dental status on chewing abilities have implications for the preventive /or therapeutical choices that could concern obese patients facing BS. Including a patient with fewer than six natural FUs in a therapeutic nutritional programme could expose him or her to a high risk of failure to chew, with adverse consequences on dietary behaviour. The solutions for compensating for missing teeth and restoring chewing function imply economic resources (for example, for implants and fixed prosthetics), that are not available for the majority of obese patients [45], [46]. The alternative to efficient mastication is artificial food comminution. Under these oral and economic conditions, the food texture would have to be adapted to the dental status. In some borderline cases, a rational approach would be to propose mixed or soft foods. These solutions could in turn induce modifications in eating behaviour that would have to be monitored and managed. Advice for preparing meals with mixed food may not be pertinent as it has low sensory, particularly textural, properties. The cephalic phase of digestion could therefore be negatively affected. Further research is needed to develop and improve such foods that should be, at the same time be sufficiently plastic and cohesive to be swallowed and sufficiently hard and resistant to induce sensorial inputs and muscular activity in order to trigger the cephalic reflex for initiating digestion.

Increasing chewing or food manipulation for improving nutrition

Considering that increased chewing activity has no effect on bolus granulometry in either fully dentate patients or denture wearers, giving instructions to increase chewing seems to lack a rationale for such patients. The cephalic phase of digestion refers to a set of physiological, endocrine and autonomous responses of the digestive system which result from the stimulation of the sensory systems in the oropharyngeal cavity. Since Pavlov's work showing that sensory exposure to food in dogs triggers the secretion of gastric acid and pepsin, it has since become common knowledge that chemo-sensory stimuli exert a great influence on metabolism during food intake. The dorsal medulla oblongata contains the hub of the central nervous system that produces vagal cephalic-phase reflexes. The preganglionic motor neurons controlling these cephalic responses of digestion and metabolism are organized in longitudinal columnar subnuclei in the dorsal motor nucleus of the vagus nerve innervating the gastrointestinal tract [47].These mechanisms can be activated either directly by visceral afferents [47]–[49] or indirectly by peripheral inputs from the oral receptors that activate the brain centres. During manipulation of food in the mouth, the sensory properties perceived by receptors localized in the oral mucosa and around the teeth are conveyed by the trigeminal (Vth) nerve, while somatic sensory information from the pharynx and the posterior part of the tongue and taste information is transmitted by the glossopharyngeal (IXth) and vagus (Xth) cranial nerves.

Cephalic phase reflexes are designed to optimize and amplify gastrointestinal responses. The application of therapeutic mastication has proven effective in reducing visceral fat in leptin-deficient and leptin-resistant obese animals [50]. In humans, it has been shown that increasing the number of chewing cycles during almond mastication could increase the bioaccessibility of lipids from the nut, thereby increasing the amount of energy available to the body, thus contributing to a positive energy balance. In contrast, the increased presence of lipids in the small intestine may result in increased secretion of several hormones associated with stronger feelings of satiety [51]. In elderly subjects, it was demonstrated that post-prandial whole-body protein metabolism after a meat meal is influenced by chewing efficiency [52] and that oral functional training might activate the feeding function, possibly facilitating nutrient bioavailability [53]. Certain cephalic phase reflexes are also expected to fulfil a role in feeding behaviour by acting on the mechanisms of hunger and satiety [54], [55]. Eating with a pause between bites significantly reduces energy intake compared with eating with a soupspoon and taking pauses between spoonfuls and without a pause [56]. It was shown in an experimental setting that eating with small bite sizes rather than with large bite sizes and increasing oral processing time significantly decreases food intake [57].

Increasing the number of chewing cycles leads to an increase in the time food is manipulated in the mouth that, in turn, could possibly trigger the cephalic reflexes. Consequently, advice to increase chewing activity is pertinent for obese patients with healthy teeth, although this motion would have no effect on the bolus granulometry. For obese patients with poor dental status, the advice on increasing chewing should be changed for advices to firstly, recommendations about preparing soft foods and, secondly, guidance on increasing the manipulation time of food in the mouth. An increase in time for soft food manipulation in the mouth could be part of the optimisation of the nutrition process. This last solution should be explored in further clinical studies.

Conclusion

Patients with obesity complied with the advice on increasing chewing after bariatric surgery, whatever their dental status. The interactions between dental status and food properties may affect the consequences of changes on chewing activities on the pre-swallowed bolus composition. The relationships between dental status, chewing behaviour, feeding attitudes and nutrition are complex and further studies are required to obtain a better understanding of the impact of dental status on feeding behaviour and nutrition in obese patients. In further studies, collection of data including not only granularity but also rheological properties of the food bolus should be undertaken to gain a better understanding of the link between physiological properties and final D50 values observed at the swallowing time. Despite these limitations, this study emphasizes the need for a comprehensive approach regarding patients scheduled for gastric bypass surgery, including the use of dental status as a predictive criterion for failure or success in changing chewing behaviour and feeding attitudes. The debate is now open on supplementing guidelines for therapeutic decisions that could be applied to obese patients with poor dental status.