The Nutritional Challenges in Dysphagia: Not Only a Matter of Nutrients

Abstract

Oropharyngeal dysphagia can significantly affect food ingestion. Texture-modified foods and thickened fluids are proposed to alleviate this difficulty. The nutritional density of adapted foods is often insufficient to maintain adequate nutritional intakes. The current scientific knowledge relies on a weak correlation between clinical assessment and meals consumed by patients as well as few clinical trials to support the efficacy of any treatment. The negative organoleptic perceptions associated with dysphagia diets further exacerbate undernutrition and malnutrition. Over the years, scientist in food science, nutritionists, psychologists and other health professionals have proposed parameters when formulating novel foods for the treatment of dysphagia. Beyond the nutritional composition of adapted foods for the treatment of dysphagia, this chapter will present multidimensional factors affecting food intake, sensory evaluations, rheological parameters as well as the available research to date with respect to optimizing nutritional treatment of dysphagia. To date, extrapolation to everyday food formulations remains a real challenge. To ensure success, thorough, individualized nutritional care plans need to be implemented and monitored regularly. An international knowledge transfer database must be considered to help document the innovations proposed in texture-modified foods and thickened fluids in order to benefit patients of all ages and origins.

1. Introduction

The contextual application and impact of nutritional interventions in the clinical treatment of dysphagia have been studied in the scientific literature [1, 2, 3, 4]. Articles published as early as 1946 are presenting difficulties in swallowing due to either tonsillectomy, achalasia, myasthenia gravis, dysphagia lusoria—vascular compression of the esophagus—malignant causes and focused mainly on the esophageal phase of food ingestion [5, 6, 7, 8]. An interest in difficulty in chewing and eating was also brought forward in the 1960s by the challenges of swallowing in neurological diseases or post-stroke patients [9, 10, 11]. Nearly 60 years later, the complexity of food ingestion in adults afflicted by deglutition disorders, more specifically dysfunctions of the oral and oropharyngeal regions, continues to be an important clinical challenge. The multifaceted aspects of food perception, mastication, preparation and propulsion of the bolus for an effective deglutition is still a major preoccupation for patients, families and caregivers.

The natural and reflex driven act of feeding one-self in adulthood is in fact an intricate emotional, sensory and neuromuscular achievement. It is directed by visual, olfactory, tactile and gustatory stimulations leading to pleasure and social interactions. Feeding one-self needs to meet much more than just pure physiological goals, particularly in healthcare.

“In spite of food fads, fitness programs, and health concerns, we must never lose sight of a beautifully conceived meal.”

– Julia Child.

The difficulty to chew and swallow foods and liquids, known as dysphagia, often leads to malnutrition, impaired immune system and pneumonia [12, 13, 14, 15]. In fact, presbyphagia (gradual and subtle decrease in swallowing capacity) and persistent undernutrition have been linked to sarcopenia and, more specifically pulmonary sarcopenia [16, 17, 18, 19, 20].

Several medical conditions such as head and neck cancers, cerebrovascular accidents, dementia, neurodegenerative diseases and aging could lead to dysphagia. Contingent to the underlying etiology and the evaluation/reporting method, reported prevalence of oropharyngeal dysphagia vary greatly, ranging from 11.4 to 91.7% in various assessed populations [21, 22]. Finally, dysphagia could improve, remain stable or worsen, needing recurrent assessments and adaptation of nutritional treatments (Figure 1). The conditions presenting some of the highest prevalence rates are observed in the very old frail populations presenting neurodegenerative conditions [21, 22].

Figure 1.

Nutritional intervention route in dysphagia context.

2. Nutritional interventions

The past century has seen a remarkable evolution for human nutrition. Nutritional requirements for various population groups were adopted for different parts of the world and used to assess quality of food intake or food service delivery of well balanced meals in hospitals, schools, or daycare as well as or nutrition labeling of commercial food products [23, 24, 25]. Detailed nutritional values and composition of foods can now be more comprehensively assessed. Therefore, menus’ macro and micronutrients are regularly being calculated for individual needs. Additionally, several databases exist to assess food intake in a wide array of clienteles (infants, children, athletes, elderly, etc.), food types or food service contexts [26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38].

It is regularly stated that, dysphagia leads to diminished food intake, poor functional status and increased risk of pneumonia. To improve the situation, foods and liquids are gradually adapted in texture or consistency to offer softer, moist and cohesive boluses and meet the needs of the patients’ changing medical condition. In fact, it is now internationally recognized that various texture-modified foods (TMF) and thickened fluids (TF) are considered the cornerstone of clinical treatment and should be carefully evaluated [39]. Interestingly, in research studies investigation appetite and food intake in relationship to food oral processing, a meta-analysis published by Krop and colleagues noted that increased food oral processing (chewing) reduced food intake (−0.28 effect size; 95% CI: −0.36, 0.19; I2 statistic = 61.52%) and curbed appetite (−0.20 effect size; 95% CI: −0.30, 0.11; I2 statistic = 0%) [40]. Given this evidence, the decreased oral processing required to ingest TMF should be linked to improved oral food intake which is mostly sought after in dysphagia nutritional intervention. Additionally, thickening agents used to increase the consistency and reduce flow velocity are known to contribute to nutritional density [41]. So, shall we see an instant improvement? Not, according to the literature.

For the past 20 years, nutrient composition of institutional diets or TMF dysphagia diets have been repeatedly identified as deficient in energy and macro- or micronutrients [42, 43, 44, 45, 46, 47, 48, 49, 50, 51, 52] and remain a well known contributing factor of undernutrition and sarcopenia. Internationally, professional organizations are suggesting guidelines for better healthcare nutrition, including dysphagia nutritional care plans [53, 54, 55, 56, 57]. Fortification in energy, protein content or micronutrients of TMF, and the use of snacks are suggested to improve nutritional status [58, 59, 60]. But, sensory characteristics of TMF and TF such as taste, mouthfeel and appearance are regularly perceived negatively [61, 62, 63, 64, 65] and this nutritional treatment is seen as a psychosocial burden by staff and patients [66, 67, 68, 69, 70, 71]. The challenge lies in adapting the foods offered to patients presenting dysphagia to optimize/improve nutritional content while maintain acceptable sensory characteristics!

Very few randomized clinical trials looking at comprehensive food intake reports for MTD and TF are found in the literature [72, 73, 74]. They were conducted in elderly populations, for a limited assessment time and are of small sample sizes. They did take in consideration complete dietary intakes, including oral nutritional supplements (ONS), meals and snacks. Detailed quantitative dietary assessments using weighed food records and done over several days in order to reflect usual intake are complex and time consuming [75]. This could explain the paucity of publications.

First in 2006, a small randomized controlled trial of 12 weeks was conducted by Germain et al. in frail elderly residents in a long-term care (LTC) facility (Treatment Group: n = 8; age: 82.5 ± 4.41 years, weight 55.9 ± 12.1 kg, BMI 22.4 ± 3.93; Control Group: n = 9; age, 84.6 ± 3.81 years, weight 54.3 ± 7.49 kg, BMI 21.2 ± 2.31). Prior to randomization, all participants were assessed for oropharyngeal of dysphagia and TMF and TF were prescribed as needed. The control group received usual TMF and the treatment group received reshaped pureed or minced foods. Intakes were calculated using 3-day weighed food records at Baseline, Midway and End points. The average weight in the treated group augmented compared to the control group (3.90 ± 2.30 vs. −0.79 ± 4.18 kg; p = 0.02). Furthermore, the treated group had an improved intake of total energy, proteins, fats, total saturated fats, monounsaturated fats, potassium, magnesium, calcium, phosphorus, zinc, vitamin B-2, and vitamin D compared to control subjects (p ≤ 0.05) [72].

In 2017, following a 20-week intervention, Côté et al. also demonstrated improved intakes in a multi-center study of 15 elderly LTC residents (Treatment Group: n = 7). In this study, participants were assessed for oropharyngeal dysphagia to ensure adequate prescription level of TMF and TF. The control group received institutional TMF and the treatment group received reshaped pureed or minced foods (Épikura©). Proportions of food intakes were measured by comparing pictures of the content of the tray, before and after the meals (2 consecutive days; lunch and supper meals; excluding supplements and drinks). Although participants’ body weights remained unchanged, the an increase in energy (p = 0.004), carbohydrate (p = 0.04) and lipid (p = 0.001) intakes in the treated group was documented [73].

Lastly in 2019, Reyes-Torres et al. implemented a controlled TMF and TF diet (n = 20 participants) to be compared to isocaloric standard diet (n = 20 participants) for 12 weeks. All participants received instructions in regards to swallowing rehabilitation techniques. Daily energy and protein intakes were assessed by 24-h multiple-step recalls and calculated using Food Processor Nutrition Analysis^® software. In the intervention group, results revealed improved energy intakes (29 ± 10 to 40 ± 15 kcal/kg, p = 0.009) and protein intakes (1.3 ± 0.6 to 1.8 ± 0.7 g/kg, p = 0.03). Likewise, body weight were increased (56 ± 10 to 60 ± 10 kg, p < 0.001) as well as handgrip strength (18 ± 11 to 21 ± 13 kg, p = 0.004). Control group parameters remained unchanged. Therefore it appears that, although isocaloric to the standard pureed diet, better texture controlled pureed foods and TF allowed for improved dietary intakes and overall physical health status.

More recently, in a 12-week intervention study involving 50 elderly individuals living in a LTC facility (age: 89.12 ± 4.18 years), Rondanelli and colleagues also demonstrated that meal appreciation and nutritional status can be improved with tailored pureed texture meals [76]. This research team assessed meal intake with the Comstock Method of visual estimations of food waste [77] as an alternative to weighed dietary intake measures. It is noteworthy to mention that digital imaging methods to assess food intakes in various contexts (school cafeterias, restaurants, hospitals, etc.) have improved since their development in the early 1980s [78]. Visual estimations increasing used in research as they have the potential to help document food intake in larger groups with excellent agreement with the direct observational method, good agreement for between observers assessments comparison and presents very high intra-rater agreements [79, 80, 81, 82, 83].

Finally, in a case-crossover study published in 2022, Bayne et al. implemented sensory-enhanced, fortified snacks (quick-dissolving crisps, puree dips, and dry soup blends) for 8 weeks. The snacks improved the quality of nutritional intake among nursing home residents [84].

The presence and severity of dysphagia should prompt an individualized, nutritionally adequate and texture/consistency adapted nutritional interventions care plan to maintain or improve nutritional status and overall health of these patients. Although intuitively sound, few randomized clinical trials or interventions studies can be found using a clearly identified adapted nutritional intervention in association to specific severity of dysphagia. These rare and modest investigations seem to confirm that, other than using oral nutritional supplements, maintaining or improving nutritional density of foods provided by food services is possible. However, given the unfortunate poor quality of the research to date, systematic reviews repeatedly request more and better investigations [50, 54, 85, 86].

Admittedly, several confounding variables affect any nutritional research protocols: age groups, oropharyngeal or esophageal dysphagia, sample sizes, clinical settings, cultural reality, foods and ONS offered, number of meals assessed, dietary intake assessment method, duration of study, initial nutritional and clinical status, disparity in assessment approaches and measured outcomes, etc. The impact of nutritional interventions is challenging to measure (Table 1) [13, 76, 87, 88, 89]. Often, assessments have been conducted in elderly populations, possibly due to the convenience of studying cohorts in a more controlled environment. Conversely, clinical conclusions on the efficacy of these trials in younger populations should carefully extrapolated.

Sources	Participants	Assessment	Conclusion
Vucea et al. [13]; (2018); Canada	Cross-sectional study; Multi-center; n = 337; Regular diet; n = 139; Minced diet; n = 68; Pureed diet; Age = 86.8 ± 7.8 y; 32 LTC facilities	MNA-SF; InterRAI LTCF Cognitive Scale; Ed-FED	MNA-SF score were lower for patients on MTF, dementia, ONS, assistance to fed or poor oral health; MNA-SF score were higher for patients with micronutrient supplements or family assistance for meals.; Malnutrition risk increased when diet texture prescription was changed from regular to minced diet; Malnutrition risk increased when diet texture prescription was changed from regular to pureed diet
Shimizu et al. [87]; (2020); Japan	Retrospective cohort; Single-center; n = 218 with pneumonia; Age = 82.9 ± 9.8 y; TMD group; Multiple stages TMD (M-TMD) group	Food Intake Level Scale; Japan TMD Scale; MNA-SF	The M-TMD were related to the maintenance or improvement of swallowing capacity and nutritional status; Note: Nutritional intake not assessed; Dysphagia severity not assessed
Razalli et al. [88]; (2021); Malaysia	Cross-sectional study; Single-center; n = 95; TMF diet; Age: 64.2 ± 16.7 y; Blended diet; Mixed porridge diet; Minced diet	1 day lunch (L) + dinner(D); Food waste; Food appreciation; Clinical/external factors such as appetite, assistance, time to eat, oral nutritional support	Blended diet; Food waste—lunch: 68.8%; Food waste—dinner: 63.3%; Correlated with variety of food, time to eat meal and appetite; Mixed porridge diet: Food waste—lunch: 36.3%; Food waste—dinner: 33.9%; Correlated with texture and temperature; Minced diet: Food waste—lunch: 57.9%; Food waste—dinner: 55.5%; Correlated with appearance, taste, vegetables and chicken/meat/fish; Note: Nutritional intake not assessed; Dysphagia severity not assessed
Endo et al. [89]; (2021); Japan	Longitudinal study; Multi-center; n = 284; Regular diet; n = 171; TMF diet; Age = 86.5 ± 7.8 y; Duration = 1 year; 25 LTC facilities	Severity of dysphagia; Weight; Barthelet Index; Total energy intake; Food form	ADL and change in food from regular to TMD form were associated to weight loss
Rondanelli et al. [76]; (2021); Italy	Intervention study; Single-center; n = 25 pureed diet; 1223 kcal and 44 g protein per meal; n = 25 consistency; controlled MTD; 1400 kcal and 53 g protein per meal; All beverages are thickened; Age = 89.2 ± 4.6 y	Meal satisfaction; Food intake; MNA; Arm- and calf-circumferences; Handgrip; Blood chemistry; Dysphagia Outcome and; Severity Scale (DOSS) as inclusion criteria	Significant improvements were observed for food intake, meal appreciation,; BMI, arm- and calf-circumferences, MNA, handgrip; Prealbumin and albumin; Folic acid, vitamin D and ionized calcium; PCR and TNF-alpha; Note: Dysphagia severity was assessed but not used to stratify data

Table 1.

Selected nutritional trials in adult patients presenting dysphagia.

Regrettably, dysphagia is too often considered as present or not present in research investigations. As an adapted nutritional individualized treatment, TMF and TF should be selected according to the level of severity of dysphagia. This variable is frequently ignored when evaluating the impact nutritional of treatments whether it is TMF, TF or ONS. Likewise, the severity level of the dysphagia is often extrapolated in observational or epidemiological studies by reporting descriptive aspects of TMF being served to patients [13, 90]. This premise could falsely assume that all participants had been properly assessed or monitored or that all foods were optimally controlled for their texture, consistency or nutrient density. Poorly assessing, documenting and reporting dysphagia severity scale in publications undoubtedly leads to inconsistent results and interpretation. An analogy with optometry assessments can be made. Optometrists will not report poor or good vision. Optometrists will report myopia or presbyopia in well-defined optical units called diopters. Individualized prescription will be proposed and corrective lenses will be provided. Although such precision in dysphagia severity assessment is still difficult to measure for all patients, it must be maintain as part of the assessment evaluation when conclusions are drawn from different trials.

Various dysphagia assessment tools exist: screening tools, bedside assessments or more sophisticated instrumental investigation methods such as surface electromyography (sEMG) biofeedback, manometry, videofluoroscopy or fiberoptic endoscopy evaluations. Clientele, clinical context or availability of expertise and equipment to conduct these tests will determine if they can used or not. Their usefulness and their validity continue to be challenged [91, 92, 93, 94, 95, 96, 97]. The protocols for each evaluation differ. Bolus types and quantities consumed to perform the tests also differ. Additionally, diverse texture modifiers [65, 98] are used to change bolus consistency and texture of TMF and TF. In a clinical context, medications can also require consistency or texture modifications rendering new formulations which are also poorly understood [99]. Finally, and perhaps even more pertinent for nutritional interventions, no publication to date can be found providing a clear relationship between the various boluses provided during these assessments, the modification of consistency and texture occurring during the oropharyngeal phase of swallow and the multitude of foods possibly available at meals. Therefore, these investigation techniques must remain surrogate assessment methods of swallowing capacity and direct extrapolation of the capacity to prepare and swallow various types of bolus can only truly be monitored using a careful diagnostic process and impact of therapeutic approaches, in realistic contextual mealtime conditions, over time (Figure 2).

Figure 2.

Key factors for a meaningful nutritional intervention trial in dysphagia context.

Keeping these limitations in mind, scales evaluating severity of oropharyngeal dysphagia have been validated with various clienteles. Examples of such scales would be the 7-point Dysphagia Outcome and Severity Scale (DOSS) [100], the 7-point Functional Oral Intake Scale (FOIS) [101], the Eating Assessment Tool (EAT-10) [102] and the 10-point observer-rating scale Food Intake LEVEL Scale (FILS) [103] (Table 2). Dysphagia severity scales are hardly ever applied in nutritional interventions or trials. But in 2006, Clavé et al. found a strong correlation between malnutrition and the dysphagia inventory score in 46 participants with brain damage, 46 participants with neurodegenerative diseases and eight healthy volunteers [104]. It could be helpful in future research focused on nutritional interventions to include a severity scale and determine if a correspondence is detectable between nutritional status and dysphagia severity.

Dysphagia Outcome and Severity Scale [100]; (1999); (United States)	DOSS	Design intended population: adult, post-stroke; For videofluoroscopy or fiberendoscopy swallow study; Full per-oral nutrition (P.O): normal diet; Level 7: normal in all situations; Normal diet; No strategies or extra time needed; Level 6: within functional limits/modified independence; Normal diet, functional swallow; Patient may have mild oral or pharyngeal delay, retention or trace epiglottal undercoating but independently and spontaneously compensates/clears; May need extra time for meal; Have no aspiration or penetration across consistencies; Full P.O.: modified diet and/or independence; Level 5: mild dysphagia: distant supervision, may need one diet consistency restricted; May exhibit one or more of the following; Aspiration of thin liquids only but with strong reflexive cough to clear completely; Airway penetration midway to cords with one or more consistency or to cords with one consistency but clears spontaneously; Retention in pharynx that is cleared spontaneously; Mild oral dysphagia with reduced mastication and/or oral retention that is cleared spontaneously; Level 4: mild–moderate dysphagia: Intermittent supervision/cueing, one or two consistencies restricted; May exhibit one or more of the following; Retention in pharynx cleared with cue; Retention in the oral cavity that is cleared with cue; Aspiration with one consistency, with weak or no reflexive cough; Or airway penetration to the level of the vocal cords with cough with two consistencies; Or airway penetration to the level of the vocal cords without cought with one consistency; Level 3: moderate dysphagia: Total assist, supervision, or strategies, two or more diet consistencies restricted; May exhibit one or more of the following; Moderate retention in pharynx, cleared with cue; Moderate retention in oral cavity, cleared with cue; Airway penetration to the level of the vocal cords without cough with two or more consistencies; Or aspiration with two consistencies, with weak or no reflexive cough; Or aspiration with one consistency, no cough and airway penetration to cords with one, no cough; Non-oral nutrition necessary; Level 2: moderately severe dysphagia: Maximum assistance or use of strategies with partial P.O. only (tolerates at least one consistency safely with total use of strategies); May exhibit one or more of the following; Severe retention in pharynx, unable to clear or needs multiple cues; Severe oral stage bolus loss or retention, unable to clear or needs multiple cues; Aspiration with two or more consistencies, no reflexive cough, weak volitional cough; Or aspiration with one or more consistency, no cough and airway penetration to cords with one or more consistency, no cough; Level 1: severe dysphagia: NPO: Unable to tolerate any P.O. safely; May exhibit one or more of the following; Severe retention in pharynx, unable to clear; Severe oral stage bolus loss or retention, unable to clear; Silent aspiration with two or more consistencies, nonfunctional volitional cough; Or unable to achieve swallow
Functional Oral Intake Scale [101]; (2005); (United States)	FOIS	Design intended population: adult, post-stroke; Tube dependent; Level 1: No oral intake; Level 2: Tube dependent with minimal/inconsistent oral intake; Level 3: Tube supplements with consistent oral intake; Total oral intake; Level 4: Total oral intake of a single consistency; Level 5: Total oral intake of multiple consistencies requiring special preparation; Level 6: Total oral intake with no special preparation, but must avoid specific foods or liquid items; Level 7: Total oral intake with no restrictions
Eat Assessment Tool [102]; (2008); (United States)	EAT-10	Design intended population: adult, various clinical diagnoses; Developed by Expert Panel; 10 questions pertaining to eating difficulty EAT-10 score of 3 or higher: abnormal
Food Intake LEVEL Scale [103]; (2013); (Japan)	FILS	Design intended population: palliative care patients; No oral intake; Level 1: No swallowing training is performed except for oral care.; Level 2: Swallowing training not using food is performed.; Level 3: Swallowing training using a small quantity of food is performed.; Oral intake and alternative nutrition; Level 4: Easy-to-swallow food less than the quantity of a meal (enjoyment level) is ingested orally.; Level 5: Easy-to-swallow food is orally ingested in one to two meals, but alternative nutrition is also given.; Level 6: The patient is supported primarily by ingestion of easy-to-swallow food in three meals, but alternative nutrition is used as a complement.; Oral intake alone; Level 7: Easy-to-swallow food is orally ingested in three meals. No alternative nutrition is given.; Level 8: The patient eats three meals by excluding food that is particularly difficult to swallow.; Level 9: There is no dietary restriction, and the patient ingests three meals orally, but medical considerations are given.; Level 10: There is no dietary restriction, and the patient ingests three meals orally (normal).

Table 2.

Scales of severity of dysphagia - assessment tools.

Given all the existent caveats limiting the bedside and clinical assessment of dysphagia, nutritional interventions need to be prescribed to alleviate and compensate for the decrease in food intake. Notwithstanding the possible enteral nutritional avenue, texture modified diets, oral nutritional supplements, enriched snacks are some of the options proposed [21, 50, 60, 76, 85, 86, 101, 105, 106, 107, 108, 109, 110, 111, 112, 113, 114, 115, 116, 117].

3. Influential factors associated to eating

Eating is indispensable for subsistence. Therefore, it is a crucial component of the evolution of the human kind. As part of the essential evolutionary process, eating has taken various forms and adaptation has been linked to our survival.

Food choices and eating patterns are affected by several key elements such as biological influences (appetite, taste, hunger), psychological influences (mood or stress), socio-cultural determinants (family, peers, income, skills) and learnt behaviors [118, 119]. Côté et al. have depicted multiple factors to consider when providing adapted foods to the elderly. These factors remain intact, if not more important, once dysphagia becomes symptomatic (Figure 3) [120].

Figure 3.

Interaction model of key factors affecting feeding in the context of dysphagia in the older adult population.

In the context of texture-modified foods and thickened fluids for the nutritional treatment of dysphagia, the appreciation of foods is often described as a burden [49, 66, 70, 71, 86, 121]. The reasons behind this present state of affairs are very complex and possibly imbedded in human survival programming itself.

4. Starting at the beginning: human evolution and food intake

The need of water and food was stated as a key necessity in the Maslow Hierarchy of Needs [122]. As humanoids evolved, the feeding techniques and the human chewing capabilities have evolved and adapted through time. Paleoanthropologist Dr. Rick Potts is the founder of the Human Origins Program at the Smithsonian’s National Museum of Natural History, Washington, DC [123]. Potts describes the evolution of the human cranium developing from a small brain case and slope-like face to our current species with the largest brain case and the smallest face. The mandibular bone (not shown on the video) would have also changed in shape and strength affecting the capacity to chew foods and prepare the food bolus for swallowing.

Ledogar and colleagues [124] studied the morphology and the facial biomechanics of cranium specimens from various regions around the globe. Using computational biology, the research group created a model (named ALL-HUM) incorporating several characteristics of crania to which they allocated human bone tissue and masticatory muscle force values in order to predict cranial mechanics and calculate strains and bites forces of our ancestors. The masticatory gracilization over time of the human face was less stiff than the chimpanzee comparatives but were efficient in bite force application. These findings support the hypothesis that consumption of less mechanically challenging foods or the origination of extra-oral processing techniques (tools and cooking) accompanied these morphological changes. Humans adapted in several ways to evolved in various regions of the globe. One impressive adaptation was food preparation as well as feeding and chewing techniques as it is essential to survival of the species.

4.1 Taste perception

The biomechanics of human masticatory abilities are definitely important elements of feeding. However, feeding evolution is not only linked to our capacity to mechanically break down or process foods. It is associated to an array of sensations which also guide humans in accepting or refusing the ingestion of substances. It is believed that taste perception is an adaptive response [125] to assessing nutritional content or toxicity of foods. Initially believed to be spatially mapped on the tongue, it is now understood that taste receptors are found across the tongue [126]. In fact, located in the oropharyngeal region, the primary tastes of sweet, bitter, salty, sour and umami receptors could have helped humans in detecting acceptable foods sources. One type of taste receptor cell was identified for each of the sweet and umami tastes. For salt and sour tastes, possibly more than one are involved. However, bitter taste is detected by 25 different types of cell receptors [127, 128]. Therefore, primates and humans are capable to detect bitterness which prevents the consumption of possible toxic plants [129]. Animal studies have shown that, although specific taste buds regenerated at a high turnover rate, they maintain the capacity to reconnect to the central nervous system due to labeled line wiring. Essentially, labeled line wiring allows the bitter taste center to convey and perceive only bitter peripheral signal or the sweet center carry only sweet signal. The molecules responsible for directing these gustatory nerves are known as semaphorins and are proteins involved in neuronal axon guidance which permit high specificity [130, 131, 132, 133]. Consequently in humans, taste perception is highly regulated and neurologically wired to allow innocuous ingestion of a wide array of substances.

New investigations pertaining to the microbiome have associated oral microbiota composition and with taste perception and reported food intake. Although providing exploratory results, it is proposed that the oral microbiota could also be affecting taste and smell perception as well as overall appetite [134, 135, 136, 137, 138, 139, 140].

4.2 Mouthfeel and texture perception

Ingestion of food is also guided by mouthfeel and texture perceptions as well as appreciation of the masticated bolus. Oral processing is a complex progression of neuromuscular interactions which prepares and assess food prior to swallowing. As food is being broken down and imbibed with saliva, it is in contact with the oral sensory receptors and an integrated sensory evaluation of tastes, volatile compounds and texture will occur [141, 142].

Electromyography (EMG) has been used to assess electric activity of the main masticatory muscles in healthy participants. Coupled to chewing cycle counts, tongue mobility, tongue pressure, salivation or videofluoroscopy studies, the mechanistic involved pre- and peri-swallowing can be assessed [143, 144, 145, 146, 147, 148]. In a study looking at gels and sols, muscle activity required until swallowing appeared to be well correlated with the required force deployed for large compression deformation which occurs at the initiation of mastication [145]. Tournier and colleagues observed large inter-participant variation both for salivation and oral processing after 5 healthy participants masticated 4 breads of different textures and compositions [146]. Mori and colleagues studied the laterality of the posterior tongue movement in 20 young and health adults by [147]. Gummy jelly, sponge cake and mashed potatoes were assessed as representative of gradient mastication intensity requirements at the initiation, middle and end of mastication stages. For the purpose of the study, the participants were asked to masticate only on the right side or only on the left side. They measured a more intense EMG activity on the side of mastication for the gummy jelly and documented that tongue activity was affected by the food texture. Finally, Matsuo and colleagues investigated the masticatory function of 22 young participants an 32 community-dwelling older individuals of either normal or oral hypofunction. For their investigation, the test samples were a control meatloaf, meatloaf containing lotus root, control chicken ball or chicken ball with almonds slivers (10 g per bite). The documented mean EMG amplitudes and integrated EMG activity were lower for control samples which were softer test foods. Oral functions, including dental condition, appeared to decline with age and would have influenced the assessed mastication capacity [148].

The characterization of the biomechanics of bolus preparation and its impact on swallowing capacity is still being investigated [149, 150, 151] and remains limited in application for daily clinical investigations or association to diversified menu items around the globe. Few foods have been assessed. However, the variability in bolus process are highlighted and the impact could be important.

Individual physiognomy, quality of dentition and capacity to prepare foods for deglutition are only one part of the complex equation. The foods and liquids consumed bring their share of complexity. The lubrication of the bolus is also dependent on salivation. Intra-oral assessment of bolus texture and correlation to sensory perceptions are challenging.

5. Development of adapted texture-modified foods

5.1 Sensory evaluation

Acceptance by consumers of food products is a main priority for the food industry. Development of new products is time consuming and costly. However, the formal study of sensory evaluation of foods is a science with a relatively recent history. As stated by M.A. Drake, sensory evaluation is a “collection of techniques that seek to differentiate between a range of products based on all of their sensory characteristics and to determine a quantitative description of all the sensory attributes that can be identified, not just the defects” [152]. Methods such as discrimination testing (Is there a difference between 2 formulations?), acceptability (Which food would you prefer? Rating scales of relative dislike and like), descriptive sensory evaluation (How can we discriminate between a range of products based on all of their sensory characteristics?) have provided additional tools for application in research, product development, and marketing [152, 153]. Important developments in the science of sensory evaluation were initially triggered in the U.S. by the desire to optimize food intake in U.S. armed forces [152, 154, 155, 156]. With the creation of the food acceptance program in 1945, the U.S. Army Quartermaster Food and Container Institute (Chicago) had four main divisions which were food habit studies, psycho-physiological studies, organoleptic studies and statistical theory. In 1949 and 1950, psychologists David Peryam and Norman Girardot were hired to lead the Food Acceptance Research Branch. As measurement is essential to building comparative datasets, the staple nine-point hedonic scale (Table 3) was developed to assess food acceptance and preference [157, 158]. This scale remains in use today to asses customers appreciation of assorted food products such as chips [159], beef sausage using pigeon pea as binding agent [160] or yoghurt [161].

Like extremely; Like very much; Like moderately; Like slightly; Neither like nor dislike; Dislike slightly; Dislike moderately; Dislike very much; Dislike extremely

Table 3.

9-point hedonic scale [157].

In the past, food development for the treatment of dysphagia customarily stemmed from clinical settings [44, 72, 162]. Researchers state that TMF and TF are deemed to be at the core of the nutritional treatment for dysphagia diets [65, 163], therefore, it is essential to evaluate the sensory profile if optimal ingestion is to be achieved. Limited publications have assessed sensory characteristics of TMF or TF. Pureed peaches [164], pureed carrots [165, 166, 167], meats [166, 167], soups, pates and timbales [167] were assessed primarily by healthy young adult for sensory perception. Thickened fluids have been studied more extensively: water with and without barium, lemon flavored water, juices, milk and infant formula [63, 168, 169]. But, even fewer publications have included participants with impaired swallowing [164, 166]. Studies are mainly conducted with the participation of young healthy adults. To be fair, several neurological diseases affect oral expression or comprehension of instructions which could render consumer assessments difficult. However, when recommending approaches to improve nutritional intakes and adherence to a proposed dysphagia diet, customer appreciation—likes and aversions of patients—should be at the core of the plan. More sensory research should be done with TMF and TF to help in developing complete, nutritious, appetizing and varied menu plans.

5.2 Rheological evaluation

Nutritional interventions for the treatment of dysphagia can take various forms and should progress with the medical conditions. Foods are molecularly and structurally elaborate and diverse. Oral nutritional supplements, texture-modified foods and thickened fluids often require the addition of the texture modifying agents which only adds to the complexity of these matrices. Comparing foods items is challenging in clinical trials. Over time, terminology and assessment methods have been proposed [170]. Two major milestones in the evolution of dysphagia diets development were the National Dysphagia Diet (NDD) [171] in 1999 and the International Dysphagia Diet Standardization Initiative (IDDSI) [39] in 2015.

Based on the work of food scientists Russell H. Mills [172] and Don Tymchuck [173], the NDD was the first diet to propose a quantifiable measure to assess flow of TF. Viscosity ranges were determine to discern different 3 different levels of consistency for fluids. Concepts of food texture such as adhesiveness, cohesiveness, firmness and springiness were also suggested to describe and classify TMF in 3 categories (Table 4).

NDD1—terminology		IDDSI2—terminology
Fluids units		Drinks units; (ml after 10 s)
Thin; Nectar-like; Honey-like; Spoon-thick	1–50 cP3; 50–350 cP; 351–1750 cP; ≥1750 cP	Thin—level—0; Slightly thick—level—1; Mildly thick—level—2 Moderately thick—level—3; Extremely thick—level—4	≤1 ml; 1–4 ml; 4–8 ml; 8–10 ml; ≥10 ml
Foods		Foods
NDD level 1: dysphagia-pureed		Liquidized—level—3	8–10 ml
NDD level 2: dysphagia-mechanical altered		Pureed—level—4	≥10 ml
NDD level 3: dysphagia-advanced		Minced & moist—level—5	Transitional foods
Regular		Soft & bite-sized—level—6
		Easy to chew-regular—level—7

Table 4.

Terminology and rheological parameters associated to various levels of dysphagia diets.

¹

National dysphagia diet.

²

International dysphagia diet standardization initiative.

³

centiPoise.

After an extensive literature review and consultation among researchers, clinicians and industry leaders, the IDDSI group propose a more extensive descriptive framework and classification of the liquids with 5 levels to distinguish fluids and 5 levels for the MTF. A gravity flow test using a syringe is propose to measure liquid flow and 4 levels are recommended (Table 4). The syringe was preferred to other methods such as shear viscosity measurements or the use of empirical tests such as the Bostwick consistometer [174] or the line spread test due to the accessibility and ease of use of the syringe. But, velocity results obtained for various fluids using the IDDSI syringe and the Bostwick consistometer are unexpected and the discriminating capacity of the IDDSI levels remain to be demonstrated (Figure 4). The food texture descriptive parameters are still suggested to explain the MTF. However, other guidelines such as particle size, spoon-tilt test, drip test, fork pressure test and visual cues were added.

Figure 4.

Bostwick flow test and syringe flow test of common products (AAFC—Saint-Hyacinthe Research and Development Center (Canada)—unpublished data).

Both frameworks had important repercussions in the research and industrial arenas. By proposing a standardized terminology and food classification systems, these approaches helped researchers, clinicians, patients as well as the food industry to classify foods and allow better description of clinical protocols and comparison of interventions. Still, clinical trials will be required to assess their impact on nutritional status of patients suffering from dysphagia. The main novelty of these proposed frameworks was the use of rheology.

Rheology is the science of deformation and flow of matter [175]. In the context of oropharyngeal dysphagia, fluids and semi-solid foods are the object of interest. Two (2) extensive reviews helped the understanding of the science of rheology specifically in the perspective of oropharyngeal dysphagia treatment [176, 177].

First, the review published by Gallegos et al. [176] focused on the rheology of fluids. Providing a short review of basic rheological concepts, they present fundamental parameters impacting the flow of fluids such as stress, strain and strain rate (Table 5), type of fluids Newtonian, non-Newtonian, viscoplastic fluids as well as time-dependent viscous flow behavior, shear viscosity and extensional viscosity. In light of their work, it becomes evident that a bolus will undergo major pressure and deformation before and during the course of deglutition. The various forces applied (i.e. shear rates) throughout swallowing are challenging to measure and have not been clearly established. For the moment, a shear rate of 50 s⁻¹ is generally used in the literature. Salivary alpha-amylase and the presence of contrast fluids (barium) are also addressed since their presence impacts the bolus texture parameters and rheological behavior as the bolus is being processed orally prior or during swallowing.

Variable	Description	Units
Stress (τ or σ)	Force per unit area	Pascals (Pa)
Strain (ϒ)	Relative variation of position in the flow direction	Non dimensional
Strain rate (‘ϒ)	Strain variation over time	s^−1

Table 5.

Fundamental dynamic and kinematic variables of flow [176].

These variables are temperature, pH, pressure and time dependent in Non-Newtonian fluids.

Swallowing imposes a stress on the bolus and deformation of the fluid occurs. The composition of the bolus will influenced its rheological behavior.

Raheem and colleagues proposed a comprehensive review of the publications addressing the TMF. They present the various tests, both sensory and instrumental, available to the food industry to measure textural characteristics of foods. Similarly to the work done with TF, the rheological assessment of TMF is scare in the literature. According to this review, a better understanding of the complex food matrices used in the nutritional treatment of dysphagia, by all stakeholders, must take place to improve TMF.

5.3 Bridging the gaps

As early as 1963, Dr. Alina Szczesniak [178, 179] led the food industry in bridging the gap between the emerging technologies of the times and the sensory evaluations of foods. By developing standard rating scale to describe the mechanical characteristics of foods that were now assessed by texturemeters, Dr. Szczesniak demonstrated that although more repeatable and quantifiable, the data obtained for instruments remained insignificant in product development if they were not linked to human assessment and ratings. This vision of correlating instrumental and sensory assessments should inspire more future research in nutritional treatment for dysphagia. The recent ‘mouthfeel wheel’ terminology should be a step in the right direction [180].

6. Conclusion

Dysphagia is a condition affecting dietary intake. Although often underestimated, chronic undernutrition can exacerbate frailty and can lead to poor physical condition, declined immune system, sarcopenia and pneumonia. In view of the current literature, nutritional content, texture and consistency as well as appearance of texture-modified foods should be improved. An assortment of foods and fluids should be investigated to reflect more realistic food intake patterns. Above all, a personalized nutritional intervention is essential to prevent health decline.

Eating is indispensable to subsistence in addition to being a critical part of the social aspect of life. New texture-modified foods should be developed with the involvement of individuals affected by dysphagia to improve taste, textural profiles and overall acceptability. Clinical trials should improve documentation of the dysphagia severity level, nutritional intervention (foods/fluids offered) and food intake prescribed, nutrient density, satisfaction of meals and adaptation to patients nutritional needs. Research done to date, although essential to understanding this complex health issue, is still theoretical and lacks integration of expertise. We must improve clients/patients consultation. A large number of foods and fluids are required to build an nutritious and appealing menu which is an essential element to improve intakes. An open-sourced international clinical database for nutritional interventions in dysphagia, similar to existing food composition databases [181, 182, 183, 184], would be a valuable tool to build a strong resource base. While archiving details of various food or fluids formulations, nutritional values and rheological parameters (when available), this compendium would support knowledge transfer and benefit food/pharmaceutical industries, researchers, clinicians as well as clients.

Finally, clinicians and research teams must continue to progress in bridging the knowledge gap between the foods used to evaluate dysphagia severity (with and without barium), the foods and the fluids available for nutritional interventions and recommendations for the development of commercial foods available for oropharyngeal dysphagia treatment.

Acknowledgments

First, I wish to thank Sophie Turcot for her support in organizing and maintaining our laboratory facilities as well as her reliability and diligence in her scientific work. I wish to acknowledge Francis Villeneuve for his methodical approach in the multiple rheological tests conducted. Finally, I wish to extend my most sincere gratitude to Amélie Giroux, Patricia Décarie and Vivianne Chagnon of the Association professionnelle des nutritionnistes experts en dysphagie for their patient-centered approach to clinical nutrition.

Conflict of interest

The authors declare no conflict of interest.

Notes/thanks/other declarations

The author is co-inventor of the CA2467625C patent. The current assignee of this patent is Her Majesty the Queen in Right of Canada.