Bioengineering tools to aid the study of oral processing deficiencies: a 1 pathway to tailored food products

8 This review surveys the bioengineering tools available to measure and characterize the oral 9 process during food intake. The human oral forces applied whilst eating constitute a research 10 gap and some of these tools help to characterize the different actions involved in both 11 mastication and swallowing.


Introduction
With advancing age, the loss of dental pieces, lower muscle force or a lack of coordination can hinder oral processing, making ordinary eating difficult.This situation usually gets worse over time, leading to unhealthy food choices and bad culinary practices.It was first reported some years ago that individuals with incomplete dentures had a low intake of raw vegetables [1]; the participants in that study reported avoiding vegetables because they were difficult to eat, resulting in a vitamin-deficient diet.Later [2] it was also pointed out that subjects with eating deficiencies need to overcook vegetables to make them softer, again leading to a low intake of thermolabile vitamins.As all of these changes occur naturally with age, the elderly are one of the most vulnerable populations.Previous research has shown that malnutrition in elderly people will encourage infections and that a loss of feeding ability is partly responsible for deterioration in their quality of life [3].Some years ago, the concept of "eating capability" was proposed to measure the difficulty that individuals experience during the eating process [4].In this latter study, a set of measurements was performed in subjects who were then asked about the difficulty they perceived when eating.This same method has been used with a range of products [5,6].Although measuring eating capability helps in understanding eating difficulties, it does not provide information regarding the individuals' oral forces.
To cast light on new solutions for individuals with difficulties in eating, the present paper reviews some bioengineering tools to measure and characterize the oral process during food intake, which might be useful for tailoring food on the basis of these parameters.Firstly, it explains the different actions that take place during oral processing according to the physical state of the food (solid or semisolid) and how this has traditionally been measured in food science.It then describes the different methods for measuring human oral forces whilst eating and identifies the research gaps.

Oral actions when eating food: biting, chewing and swallowing
The way that individuals manipulate food in their mouths depends very much on the physical (mechanical and structural) properties of the food product.

The first bite (solid) and the first spoonful (semisolid)
A one-bite sized piece of solid food (for example, a piece of steak cut on the plate) is normally placed directly inside the mouth.If the piece of food is bigger than a one-bite size (for example, a whole apple), a suitable portion size is bitten off with the teeth.The latter involves occlusion of the opposing edges of the upper and lower incisors [7].During this first bite, sensory food information will be captured thanks to the displacement of the periodontal ligament and the sound emitted (if any) [8], affecting the speed of the bite, the force exerted [9] and the subsequent mastication process.Consequently, the whole masticatory strategy is decided at this first bite, unconsciously of course.
For a semisolid food product such as a cream or puree, the tongue (rather than the teeth) plays an important role in perception of the food texture and the decision about how to handle it in the mouth.For any food system, mechanoreceptors and chemoreceptors located on the tongue surface are constantly capturing food texture and taste features [10], contributing to the adaptation of oral forces to the food bolus and to food enjoyment.

Mastication of solid food
After the first bite of a solid food, the chewing cycles follow a sequence.The actions include a pattern of rhythmic jaw-opening followed by jaw-closing movements [11].During this period, the chewing action is constantly adapting to the physical properties of the food as it is being reduced to smaller and smaller particles and, with the help of the saliva, is formed into a cohesive, deformable mixture (the food bolus) [12].Throughout this process, not only the jaw but also the tongue move against the palate to assist in the formation of the food bolus and provide extra sensory information regarding food texture and taste recognition [7], as described above.

Oral processing of semi-solid food
Semisolid foods like purees are habitually given to individuals with impaired oral processing.When these kinds of food are given to patients with swallowing disorders, their nutritional status and their hydration levels have been shown to improve [13].Since mastication (teeth) is not involved, tongue movements together with some subtle mandibular movements are the key to enjoying these food products.
Besides the movements of the oral organs themselves, other factors such as food temperature, saliva composition and enzyme levels are also continuously changing the mechanical properties of the food, so the oral movements and forces are constantly adapting to these changes.

Swallowing the food bolus
When the food particles are small enough and sufficiently lubricated (after chewing down in the case of a solid food and tongue manipulation in the case of a semisolid food) and a food bolus is created [14], the swallowing centre, located in the brainstem (medulla oblongata) [15,16] is triggered.This action requires the proper coordination of twenty-five different muscles located along the mouth, pharynx, larynx and oesophagus [10].

Measurable food properties in relation to oral processing
Food properties at the first bite.To ascertain the initial mechanical properties of a food (before eating), food scientists have used a variety of devices (such as the Texture Analyser by Stable Microsystems or the Universal testing machine manufactured by Instron) to register the resistance of a food material to compression or breaking as it deforms.The force is exerted by a probe attached to the mobile arm of the equipment.Probes of different geometries (normally well-defined regular solids) are available depending on the test to be performed.A curve of resistance to deformation or breakage as a function of time is normally recorded.
From this curve, a series of mechanical parameters can be extracted to characterize the mechanical properties of the food piece.Stróżyk & Bałchanowski (2018) [17] have recently fixed dentures (upper and lower incisors and canines) to the instrument to mimic the human bite.However, having only one force point for the whole denture might not be representative of humans, in whom forces are created along the entire mandible.Hence, the normal practice in food texture analysis is to select the probe that best suits the type of action to be applied to the food piece (cutting, compression, puncture, bending, breaking), which normally depends on the aim of the study, and correlate the instrumental measurement with sensory perception.
Food properties during mastication.Different mechanical masticators have been developed to mimic human mastication, such as the AM 2 [18] to study bolus mechanical properties or bolus aroma release [19].However, none of these allow for ongoing adaptation to oral bolus transformation [20] or provide information about human oral forces whilst eating.
However, the study of boli formed in individuals' mouths and expectorated is a good tool for understanding how some food characteristics evolve whilst eating.The analysis of boli formed in vivo presents some difficulties, as a bolus is partly swallowed before the final swallow event (Hiiemae et al., 1996).However, this method has been used in a number of studies of solid food products like cheeses [22][23][24], bread and crackers [25,26] and meat [27,28], as well as in semisolid food products [29,30] and to compare different food matrices [12].
Food properties after mastication.It is generally agreed that food properties at the end of the mastication process (expectorated bolus) are the same as those of food at the beginning of the swallowing process, as no further chemical reaction or mechanical event will happen except for some bolus elongation.Also, once the food has travelled through the mouth to the oesophagus it is difficult to recover it in order to study the bolus properties at this point.
Nonetheless, due to the swallowing difficulties that individuals experience, especially in old age, there is research to be done on further understanding the food swallowing process.For example, ultrasound measurement has been proposed as a non-invasive method for studying the food whilst swallowing [31,32].
Food researchers have also made efforts to mimic swallowing through experimental model systems, proposing different in vitro arrangements such as a two-roll coating configuration [33] or a roller attached to a pivoting arm to mimic the tongue when propelling a bolus [34].However, the systems proposed up to now only work for flowing materials (such as thickened liquids or purees).

Incisal bite force while eating
The maximum force that can be applied by the incisors has frequently been quantified to gauge the efficacy of dentures or replacement teeth.One of the most frequently-used devices is a system that has a thin sensor (Flexiforce, Tekscan) coupled to a calibrated transducer which transforms the resistance into a measurable force [35,36].This tool has been used widely in assessing the eating capability of elderly individuals [5,37] and has proved sufficiently discriminatory to assess the different forces exerted by individuals with natural teeth, dentures or fixed teeth.The sensor has been validated for use in daily dental practice [38].
However, these measurements still fail to capture the force exerted when biting different food products.As this force depends on the properties (shape) of the sensor and the number of teeth involved, it would be useful in the future to have sensors located on each tooth whilst analysing the force required to take the first bite of different food products.

Tongue force
As explained above, the tongue plays a key role in oral food processing and the initiation of swallowing.Tongue force is one of the most common measurements in a swallowing functionality assessment [39].
The different devices designed to capture the force exerted by the tongue against the palate can be divided into those that consist of only one bulb (like the device by IOPI) [40] or of several bulbs [41] fixed to the palatal plates.However, although these bulbs provide plenty of information about individuals' oral motor functionality, they are not yet adequate for measuring tongue forces when eating food.Therefore, a palate sensor that can be easily stuck to the palate and does not interfere with oral food processing would be the most suitable for understanding tongue forces whilst eating [39].

Masticatory muscle strength
One of the most widely used devices to measure muscle activation whilst eating is the electromyography [42,43].Electrodes are easily positioned on some facial muscles, such as the masseter and the suprahyoid muscle group, where the sensors do not interfere with the eating process.This method is quite widely used by food scientists with the aim of increasing their understanding of food texture appraisal during mastication.However, it only measures the muscle activity, not the force exerted when eating [44].
The use of intraoral bite force sensors has also been proposed to measure the mastication force whilst chewing.Carrot pieces of different sizes have been used to register pain and the biting force exerted [45].This study was performed for medical purposes but the tool has potential for adoption in food science to understand and measure oral food breakage forces.

Measurement of swallowing response
Great efforts have been made to understand the food swallowing process, both by clinicians and by food scientists.Due to the importance of the swallowing process and the health risk of impaired swallowing, clinical research has been conducted in depth.Food swallowing has been studied through videofluoroscopy, fibre optic endoscopy and ultrasound techniques.
Electroglottography, normally used in speech therapy, has also been used to identify swallowing events during eating [46].It is similar to electromyography and works by locating sensors on the skin over either side of the thyroid cartilage to detect muscular contractions; allowing the different stages of the swallowing process to be identified [47].However, no non-invasive technique has yet been developed that enables the physical characteristics of the food product to be measured jointly with human-derived parameters.
Table 1 summarizes the types of measurement that can be made in the food material and some of the available bioengineering tools for measuring human actions in different food states and sizes.

Conclusion
This short review has shown the potential of some biomedical data acquisition methods for measuring human actions related to oral food processing and deficiencies in oral processing.It has discussed some existing bioengineering tools, normally used in clinical areas, which are suitable for studying human forces in different food breakdown and oral trajectories.These tools should be able to measure tongue force and masticatory force.Others, such as for the study of the swallowing process, are yet to be developed.

Table 1 .
Summary of possible measurements in the food material and in humans whilst eating foods in different states and sizes