nutrients Article Assessment of Swallowing Disorders, Nutritional and Hydration Status, and Oral Hygiene in Students with Severe Neurological Disabilities Including Cerebral Palsy Alicia Costa 1,2,3, *, Alberto Martin 1,4 , Viridiana Arreola 1,4 , Stephanie A. Riera 1 , Ana Pizarro 5 , Cristina Carol 6 , Laia Serras 7 and Pere Clavé 1,4,8, * 1 Unitat d’Exploracions Funcionals Digestives CSdM-UAB, Hospital de Mataró, 08304 Mataró, Spain; amartinma@csdm.cat (A.M.); oarreola@csdm.cat (V.A.); eriera@csdm.cat (S.A.R.) 2 Unitat de Dietètica i Nutrició, Hospital de Mataró, 08304 Mataró, Spain 3 Departament de Medicina, Universitat Autònoma de Barcelona, 08035 Cerdanyola del Vallès, Spain 4 Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Instituto de Salut Carlos III, 28029 Madrid, Spain 5 Departament de Periodòncia, Facultat d’Odontologia de Barcelona UIC, 08195 Sant Cugat del Vallès, Spain; od079353@uic.es 6 Escola l’Arboç, Fundació El Maresme, 08301 Mataró, Spain; ccarol@fundaciomaresme.cat 7 Unitat de Suport Tècnic, Fundació El Maresme, 08301 Mataró, Spain; lserras@fundaciomaresme.cat 8 Fundació de Recerca en Gastroenterologia (Furega), 08008 Barcelona, Spain * Correspondence: acosta@csdm.cat (A.C.); pere.clave@ciberehd.org (P.C.); Tel.: +34-93-741-77-00 (A.C. & P.C.)   Abstract: Background: Special needs schools (SNS) educate children and young people with major Citation: Costa, A.; Martin, A.; neurological disabilities who are at high risk of oropharyngeal dysphagia (OD) and malnutrition Arreola, V.; Riera, S.A.; Pizarro, A.; (MN). We aimed to assess the prevalence of OD, MN, dehydration (DH), and oral health (OH) in Carol, C.; Serras, L.; Clavé, P. students at an SNS. Methods: A cross-sectional observational study was conducted at SNS L’Arboç, Assessment of Swallowing Disorders, Catalonia, Spain. We assessed (a) demographics, health status, comorbidities, and gross motor Nutritional and Hydration Status, function classification system (GMFCS), (b) swallowing function, oral-motor evaluation, masticatory and Oral Hygiene in Students with capacity, and EDACS classification for eating and drinking abilities, (c) nutritional and DH status Severe Neurological Disabilities (anthropometry, bioimpedance and dietary records), and (d) OH (Oral Hygiene Index Simplified). Including Cerebral Palsy. Nutrients Results: A total of 33 students (mean age 13.3 years; 39.4% level V of GMFCS) were included. Main 2021, 13, 2413. https://doi.org/ 10.3390/nu13072413 diagnosis was cerebral palsy at 57.6%. All students presented OD, 90.6% had impaired safety, 68.7% were at levels II–III of EDACS, and 31.3% required PEG; furthermore, 89.3% had chronic MN, 21.4% Academic Editor: Cheng-Chia Yu had acute MN, 70% presented intracellular DH, and 83.9% presented impaired OH. Conclusion: MN, DH, OD, and poor OH are highly prevalent conditions in students with cerebral palsy and Received: 28 May 2021 other neurological disabilities and must be specifically managed through nutritional and educational Accepted: 7 July 2021 strategies. The multidisciplinary team at SNS should include healthcare professionals specifically Published: 14 July 2021 trained in these conditions. Publisher’s Note: MDPI stays neutral Keywords: neurological disability; cerebral palsy; dysphagia; malnutrition; dehydration; dietary with regard to jurisdictional claims in intakes; swallowing disorders; feeding difficulties; oral health published maps and institutional affil- iations. 1. Introduction Special needs schools (SNS) for children and young people with major neurological Copyright: © 2021 by the authors. disabilities (ND) and cerebral palsy (CP) have as a main objective the promotion to the Licensee MDPI, Basel, Switzerland. highest degree of students’ personal autonomy and social integration by developing their This article is an open access article physical, affective, cognitive, communicative, moral, civic, and social insertion abilities. distributed under the terms and Multidisciplinary teams at SNS in Catalonia (Spain) are composed of educational staff conditions of the Creative Commons including special education teachers, social educators, SLP teachers and physiotherapists. Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ L’Arboç SNS also has a social worker, a nurse, a neurologist, and a psychologist. SNS edu- 4.0/). cate children with major associated health problems (musculoskeletal disorders, intellectual Nutrients 2021, 13, 2413. https://doi.org/10.3390/nu13072413 https://www.mdpi.com/journal/nutrients Nutrients 2021, 13, 2413 2 of 30 disability, epilepsy, swallowing disorders, and malnutrition (MN)). In early childhood and adolescence, these populations are more likely to suffer from poor nutrition than during adulthood because of the high nutritional demands needed for growth and development. Providing adequate nutrition and hydration to these students is essential to promote their maximal level of both physical and cognitive development [1]. Oropharyngeal dysphagia (OD) is an extremely common digestive disorder amongst children with ND and CP, with a reported prevalence in excess of 90% [2,3]. The main complications of OD include res- piratory infections, aspiration pneumonia, MN, and dehydration (DH) [4,5]. Respiratory diseases are the leading cause of death in patients with severe intellectual disability and severe developmental disability [6–8]. Feeding and swallowing difficulties in children with ND and CP severely affect nutrient intake, which leads to MN, DH, alterations in linear growth, and micronutrient deficiency [2–5]. Poor nutritional status may detrimentally impact health and physical and cognitive development [5–8]. CP describes a group of permanent disorders of movement and posture development attributed to nonprogressive disturbances that occurred in the developing fetal or infant brain [3]. CP can be caused by injury to the brain at birth, during the early stages of development in the womb, or during the first two years of life. Head injuries, infections such as meningitis, and other forms of brain damage occurring in the first months or years of life are the main causes of acquired CP [1]. Up to four types of CP have been described, determined by timing, site, type, and extent of the brain lesion: (a) spastic, the most common form (70–80%) affecting motor cortex, (b) dyskinetic arising from the basal ganglia and affecting less than 10% of cases, (c) ataxic arising from cerebellum damage, also affecting less than 10% of cases, and (d) mixed types with a combination of damage [1]. The prevalence of CP in Europe is 2.08 per 1000 live births [9], and CP is considered a relatively rare disorder there [1]. Primary neurological impairments might influence not only physical and mental capacities but also neural pathways leading to dysphagia, vomiting, swallowing deficits, gastroesophageal reflux, aspiration, and constipation [10–14]. Motor disorders in CP are often accompanied by alterations in sensation, cognition, and communication, as well as by secondary musculoskeletal problems [15], and they are classified by the GMFCS into five subgroups according to their severity [16]. The severity of GMFCS also correlates with the severity of swallowing difficulties [17,18]. The most severe complication of swallowing disorders is respiratory infection, which occurs when food, liquid, or oropharyngeal secretions, together with microorganisms, are aspirated into the respiratory tract [19,20]. OH is closely related to OD because the oropharynx is a constant source and reservoir of microorganisms responsible for respiratory infections in patients with OD [19,20]. In general, young people and children with ND present greater oral pathology with poorer OH and gingival health and a higher incidence of dental caries than children without ND [21]. The severity of neurological impairment correlates with increased risk of developing dental disease [22]. For these reasons, it is recommended that children with ND are assessed for OD to avoid safety impairments, and they should receive early and regular dental care, in order to minimize the reservoir of oral pathogens [21]. Regarding MN, studies have shown high prevalence among children and young people with ND compared to the general population [23,24]. MN has been observed in 46% and 90% of children with CP [25,26] and, in the most severe types, the prevalence increases due to the severity of cognitive and motor impairments, OD, and alterations in orolingual facial motricity leading to eating difficulties [13,14,26–29]. Higher rates of MN are reported among children with bilateral spasticity, dyskinesia, and spastic quadriplegia [23,26,30,31]. Poor nutritional status is associated with growth impairment, increased spasticity, and irritability [14,30], in addition to further risk of adverse cognitive and health outcomes including respiratory complications and mortality. The etiology of MN in children with neurological impairment is multifactorial, and one of the major contributors is OD and subsequent insufficient caloric and nutrient intake [32,33]. When nutritional intake is insuf- ficient to cover nutritional requirements or the oral route is not safe, children need enteral Nutrients 2021, 13, 2413 3 of 30 nutrition through percutaneous endoscopic gastrostomy (PEG) to feed. The prevalence of children with CP with a gastrostomy tube is 11% in European countries [34]. Nutritional assessment and support are an essential part of the care of people with ND and CP who have extremely complex and challenging needs [24]. Adequate nutritional support may restore linear growth, normalize weight, decrease irritability and spasticity, improve wound healing, reduce the frequency of hospitalization, and increase social participation, thus improving overall health and quality of life [35]. Early screening and management through nutritional and compensatory strategies of OD and MN in SNS can be an effective strategy to improve physical and intellectual development, clinical outcomes, and quality of life for their students [36–38]. L’Arboç is an SNS for children and young people with multiple and major ND, located in the city of Mataró, Catalonia, Spain. The school takes care of 50 students, from 3 to 23 years of age, with CP, severe ND, and psychomotor disabilities that interfere with their development and learning processes [39]. Awareness and management of OD, MN, and OH in SNS in Spain is scarce and must be improved. As most students have severe neurological impairments, we hypothesized that most of them would have dysfunctional swallowing. We believe the introduction of a program mainly based on the management of OD and MN in children attending these schools and the education of their caregivers in the same will improve students’ hydration and nutritional status, reduce complications associated with OD (respiratory infections and hospital readmissions), and improve the knowledge of parents, caregivers, and professionals at these schools on the management of these relevant conditions. The aim of this study was to assess the prevalence of swallowing and feeding disorders and oral health impairments in students at L’Arboç SNS and their relation to students’ nutritional and hydration status. This is the first step of a program that includes (a) a transversal descriptive study that will be repeated at the end of each school year, assessing OD, nutritional status, and oral health, (b) the implementation of a nutritional intervention including adaptations in texture, caloric and protein content, and palatability during meals at school and at home, (c) a hydration program including regular services, fluid-thickening agents, and special cups at school and home, and (d) an educational program on the clinical relevance and management of OD and MN in these children for parents, caregivers, and all professionals at L’Arboç school (Supplementary Material S1). 2. Patients and Methods 2.1. Study Design A cross-sectional observational study was conducted between 1 February 2019 and 30 May 2019 in an SNS, L’Arboç School, (Mataró, Catalonia, Spain). Assessments and classifications included (a) demographics, health status, comorbidities, medication, and GMFCS, (b) swallowing function (with the Volume Viscosity Swallowing Test (V-VST)), and oral-motor evaluation, masticatory capacity, and EDACS for eating and drinking ability, (c) OH status according to the Oral Hygiene Index Simplified (OHIS), and (d) nutri- tional and hydration status (anthropometry, bioimpedance (BIA) and dietary records). The multidisciplinary team for these assessments included a dietitian, a speech and language therapist, a nurse, and a dentist. 2.2. Inclusion Criteria Main inclusion criteria were to be students of L’Arboç School (Mataró, Catalonia, Spain) and to have informed consent of the parents or legal guardians. Exclusion criteria were children whose parents or caregivers did not provide informed consent. The study protocol was approved by the ethics review board of the Hospital de Mataró (code 01/19). 2.3. Demographics, Health Status, Comorbidities, Medication, and GMFCS Data on demographics (age, gender, reference health center, educational level, and social class of the parents or main caregiver), clinical factors (neurological diagnosis, Nutrients 2021, 13, 2413 4 of 30 comorbidities, GMFCS level and associated impairments, and hospital admissions during last 12 months), and chronic pharmacologic treatments were collected from the electronic medical records (HC3). The GMFCS is a five-level classification that differentiates children with CP on the basis of the child’s current gross motor abilities, limitations in gross motor function, and need for assistive technology and wheeled mobility [40]. The GMFCS applies to all types of CP and all levels of severity, and it takes into account the age of the person; a higher level in GMFCS denotes more severe CP [41]. In our study, GMFCS was performed by a neurologist. 2.4. Oral-Motor Evaluation, Masticatory Capacity, and Swallowing Function The SLP assessed (a) oral-motor assessment and meal observation, (b) prevalence and severity of OD by clinical swallowing evaluation using the V-VST, (c) severity of their feeding impairment following the EDACS, and (d) masticatory capacity. 2.4.1. Oral-Motor Evaluation and Meal Observation Prior to the evaluation of the oral-motor capacity, the parents or the person responsible for feeding the students were interviewed about (a) the length of time it takes the students to eat, (b) the posture of students when meals are administered, and (c) the students’ degree of autonomy. In children who were reported to be able to eat some food in pieces, a direct ob- servation was made for (a) food aversion, (b) impaired lip seal, (c) tongue protrusion, (d) accumulation of the bolus in the mouth, (e) uncontrolled bolus spillage into the pharynx with three viscosities (low, medium, and high), (f) hyperreactivity at mealtimes, (g) feeding rhythm (slow, medium and quick), (h) eating autonomy, and (i) cervical hyperextension during the meal. The difficulties with sucking, swallowing, chewing, drooling, independent feeding, and feeding problems were graded as “present” or “absent”. Tongue, jaw and mouth function, swallowing function [42], swallowing assessment [43,44], aspiration, and choking were also evaluated during the intakes. Food texture provided to each student by their families and teachers was classified into four groups: Texture B (thin purée, traditional food processed, diluted) through PEG, Texture C (thick purée), Texture E (fork-mashable) from the National Descriptors for Texture Modification by the British Dietetic Association [45], and normal diet (diets without any textural modification). Data of those students who were fed with specific products for oral enteral nutrition were also collected. Following the evaluation, textures consumed by the students were compared with the textures recommended for each of the students to check their suitability. 2.4.2. Clinical Swallow Evaluation for OD (V-VST) The V-VST is a validated clinical assessment tool for OD that uses three volumes (5, 10, and 20 mL) and viscosities (middle (250 mPa·s), low (liquid), and high (800 mPa·s)). In this case, taking into account the age, the high comorbidity of the students, and the risk of premature bolus spillage into the pharynx, it was decided to adapt the V-VST by applying 5, 10, and 15 mL. It uses a pulse-oximeter to detect silent aspirations, to evaluate clinical signs of impaired efficacy and safety of swallow [46,47]. Diagnostic sensitivity and specificity for OD are 90% and 80%, respectively, and the reliability of V-VST is also high with an overall Kappa value of 0.77 (95% CI 0.65–0.89) [47]. For the V-VST evaluation, Nutilis Clear thickener was used (Nutilis Clear, Nutricia N.V., Zoetermeer, the Netherlands). It is a xanthan-gum-based thickener mixed with maltodextrin and guar gum. Viscosity levels (250 mPa·s and 800 mPa·s) were chosen in accordance with a clinical trial performed by our group [48]. For those students who were exclusively fed and hydrated by PEG, the last videofluoroscopy (VFS) was taken into account to determine their swallowing status. Nutrients 2021, 13, 2413 5 of 30 2.4.3. Eating and Drinking Ability Classification System (EDACS) The EDACS describes the functional eating and drinking abilities of children with CP aged 3 years and older, using five distinct levels. It refers to key features of ‘safety’ (aspiration and choking) and ‘efficiency’ (amount of food lost and time taken to eat) [16,49]. The EDACS provides a valid and reliable system for classifying eating and drinking performance of people with CP, for use in both clinical and research contexts, classified according to the following levels: Level I, eats and drinks safely and efficiently; Level II, eats and drinks safely but with some limitations to efficiency; Level III, eats and drinks with some limitations to safety, maybe limitations to efficiency; Level IV, eats and drinks with significant limitations to safety; Level V, unable to eat or drink safely, whereby tube feeding may be considered to provide nutrition. EDACS was developed in four stages in consultation with individuals with CP, parents, and health professionals: Stage1, drafting informed by the literature and clinical experience; Stage 2, modification by nominal groups; Stage 3, refinement in an international Delphi survey; Stage 4, testing of agreement and reliability between classifications made by SLPs, as well as between SLPs and parents [16,49]. 2.4.4. Masticatory Capacity Some items evaluated during meal observation (tongue protrusion, masticatory and tongue movements, and mouth pocketing and duration) and some questions of the care- givers interview (duration and fatigue) were used to help define the masticatory capacity of our participants. To complement it, in cases where students were eating a regular diet or type E, a more exhaustive assessment was conducted in order to evaluate the capacity of the participants to chew and grind food prior to swallowing. They were given one-quarter of a Marie-type biscuit to observe their chewing efficiency, taking into account if there was visible activity of the tongue and rotational mobility of the jaw, if there were bilateral and alternate chewing cycles, and if they made lingual movements before swallowing. Lastly, it was also observed if several swallows were needed for the small proportion of the biscuit given and if oral residue remained, as well as the total time taken to eat the piece of biscuit. 2.5. Oral Health (OH) Assessment Oral examinations were performed by a dentist and included occlusion assessment, oral hygiene, and periodontal assessment, as described in our previous studies on adults [50,51]. 2.5.1. Occlusion Assessment Facial and malocclusion analysis were analyzed by Angle’s classification of malocclu- sion [52]. This classification is based on the relationship between the mesiobuccal cusp of the maxillary first permanent molar and the buccal groove of the mandibular first permanent molar. According to this classification, three types of malocclusion were obtained. 2.5.2. Oral Hygiene Oral hygiene examination was evaluated according to the simplified Oral Hygiene Index (OHI-s). It is composed of the sum of two indices, Debris Index (DI-S) and Calculus Index (CI-S). Six indicator teeth are examined for soft deposits and calculus. DI-S and CI-S values range from 0–3 depending on the coverage of each tooth. The final value of OHI-s is obtained by adding DI-S and CI-S, for a score between 0 and 6 [53]. 2.5.3. Periodontal Assessment Periodontal assessment was evaluated according to the new classification of peri- odontal and peri-implant conditions [54]. Stage I to IV of periodontitis is defined on the basis of severity (primarily periodontal breakdown with reference to root length and periodontitis-associated tooth loss), complexity of management (pocket depth, infrabony defects, furcation involvement, tooth hypermobility, masticatory dysfunction), and extent (localized or generalized). Grade of periodontitis is estimated with direct or indirect evi- Nutrients 2021, 13, 2413 6 of 30 dence of progression rate in three categories: slow, moderate, and rapid progression (Grade A–C) [55]. 2.6. Nutritional and Hydration Assessment The assessment of nutritional and hydration status included anthropometric measure- ments, BIA studies, and dietary intake registries, which were assessed by nutritionists. 2.6.1. Anthropometric Measurements (a) Body weight and height: The students’ weight was measured using a wheelchair scale (Detecto, Model 6550 Fold-up Portable Wheelchair Scale, Webb City, MO, USA, 2010), the weight of which was later subtracted. Other children were weighed together with a parent and then the parent’s weight was subtracted. Following ESPGHAN guidelines, height was estimated from the knee height by using the Almond equation [56] for children younger than 12 years (n = 15) and the Chumlea equation [57,58] for students over 12 years of age. The knee height was measured with the child seated or in a supine position, with the knee and ankle at a 90◦ angle. Body mass index (BMI) was calculated from the weight and height of the student (BMI = weight (kg)/height (m2 )). (b) Skinfold thickness: Subscapular skinfold thickness, triceps skinfold thickness, and abdomen skinfold thickness were measured using a skinfold caliper (0.2 mm precision) (Holtain® skinfold caliper, London, UK), averaging the three measurements. Triceps and subscapular skinfolds and bioimpedance (BIA) have been shown to be accurate and non- invasive methods to estimate body fat percentage in children with CP [59]. Slaughter equations based on the triceps and subscapular skinfolds were used to estimate body fat percentage for each individual [60]. Cutoffs for body fat (%) were based on the National Health and Nutrition Examination Survey (NHANES) [61]. 2.6.2. Bioimpedance Body composition and hydration status were assessed with a body composition analyzer (InBody S10® ; Biospace Co., Ltd., Seoul, Korea). This device is based on multifre- quency bioelectrical impedance analysis, BIA (1 kHz, 5 kHz, 50 kHz, 250 kHz, 500 kHz, and 1000 kHz) and contains eight-point tactile electrodes that were attached to the left and right thumb, middle finger, and ankles [62]. All children were explored 2 h after they finished their breakfast. The majority of children were evaluated while sitting in their own wheelchair, whereas some were lying on a bed. Main compartments analyzed were (a) skeletal muscle mass, body fat mass, and fat-free mass, and (b) body water (intracellular; extracellular; total; body water ratio, ECW/TBW), body cell mass, and phase angle (PhA). Reference values of mean PhA in healthy children were obtained from the Nogueira and Bosy-Westphal studies [63,64]. The normal range of the overall population was obtained from the mean of the normality intervals according to age provided by the BIA for each student [62]. 2.6.3. Nutritional and Food Intake Assessment. Dietary Records Food intake was registered with 24 h recall and 7 day feeding history and used to quantify the calorie and nutrient intake. Dietary habits were assessed by means of a food frequency questionnaire. The results were compared with the recommendations for a student’s balanced diet according to the Mediterranean Diet [65]. 2.7. Data Analysis of Nutritional Variables To assess the nutritional status and to identify those students with MN, we used (a) growth charts based on z-score (WHO) [66], (b) growth charts based on percentiles [27], and (c) Waterlow classification [67]. Nutrients 2021, 13, 2413 7 of 30 2.7.1. Grow Charts Based on z-Score (WHO) for Healthy Children This analysis indicates the ideal growth based on a standardized reference population (WHO growth standards) [66]. z-Scores from three standard indices were used to assess nutritional status: (a) weight for age z-score (WAZ) to measure overall nutritional status, (b) height for age z-score (HAZ) to measure chronic MN, and (c) BMI for age (BAZ) to measure acute MN. The z-score for weight was calculated using WHO Anthro (version 3.2). WHO Anthro analyzes children up to 10 years old, as the weight of children above this age group is influenced by their height [66]. The z-scores for height and BMI were calculated using WHO AnthroPlus software, to monitor the growth of school-age children and adolescents from 5 to 19 years old. The calculated z-scores for each of the indices were classified into three categories according to WHO cutoff points to measure the severity of MN among students: (a) overnutrition (>+3 SD); (b) normal (+2 SD to −2 SD); (c) moderate undernutrition (<−2 SD to −3 SD); (d) severe undernutrition (<−3 SD) [14,33]. 2.7.2. Growth Charts Based on Percentiles (Brooks) for Children with CP The anthropometric profile was also calculated through the specific growth curves for children with CP based on GMFCS according to Brooks references. Weight/age, height/age, and BMI expressed in percentiles were calculated from anthropometric measurements. Low weight was defined as BMI ≤p10 and nutritional risk if weight/age was less than p5 (in children with GMFCS I and II) or less than p20 (in children with GMFCS III to V). These growth charts proposed cutoff points of the weight/age index associated with higher morbidity and mortality [27]. 2.7.3. Waterlow Classification The Waterlow Index is a system for classifying protein-energy MN in children. It is a widely used index in clinical practice for children with neurological impairment. It allows for the distinction between “wasting” (reflects acute MN and is based upon weight-for-height) and “stunting” (which reflects chronic MN and is based upon height- for-age). Cases with MN were further categorized in terms of severity on the basis of percentage weight-for-height (normal (≥90%), mild (80–89%), moderate (70–79%), severe (<70%)) and percentage height-for-age (normal (≥95%), mild (90–94%), moderate (85–89%), severe (<85%)) parameters [14,33]. The anthropometric red-flag warning signs for MN recommended by the European Society for Pediatric Gastroenterology, Hepatology, and Nutrition (ESPGHAN) work group for children with neurological impairment were also considered [32]. 2.7.4. Assessment of Energy Expenditure Basal metabolic rate (BMR) was obtained using the Schofield equation on the basis of weight and height and according to age [68]. The BMR resulting from BIA was not used because it estimates needs with the Harris–Benedict equation, a formula not indicated for the participants of this study. The calculation of total energy requirements (TEE) was made with (a) Culley’s equa- tion [69], a height-based method specific for children with CP, and (b) a simplified equa- tion [70] to calculate dietary reference standards for typically developing children, as recommended by ESPGHAN. The catch-up growth requirements were also calculated [71]. 2.7.5. Quantitative and Qualitative Assessment of Food Intake Food intake registers were analyzed using PCN Pro v.1.0® software according to Food Composition Tables by Farran A [72] and the Food Frequency Questionnaire through a custom-designed tool (Microsoft Access). Caloric and protein intake was compared to recommended dietary allowances (RDAs) for age and weight [70] according to typically developing children. Carbohydrates were compared to dietary reference intakes (DRIs) for typically developing children (130 g/day) and 50–60% of total daily energy requirements. Fat intake was compared to 30% of total Nutrients 2021, 13, 2413 8 of 30 daily energy requirements [73]. Sugar consumption was compared to ESPGHAN rec- ommendations of less than 5% of total daily energy requirements [74]. Fiber intake was assessed on the basis of DRI for age (25–30 g/day) [73]. Basal water requirements were assessed using the Holliday–Segar equation [75], which calculates water requirements for weight, and daily liquid recommendations through the European Food Safety Authority (EFSA) guidelines [76]. Vitamins and minerals were assessed on the basis of the Spanish Reference Dietetic Intake [76]. The dietary pattern was compared with the school healthy eating guidelines [77]. 2.8. Statistical Analysis Categorical variables were presented as relative and absolute frequencies and analyzed with the chi-square test or the Fisher exact test. Continuous variables were presented as mean ± standard deviation and compared with the t-test. For those variables that did not follow a normal distribution, we used the nonparametric Mann–Whitney U-test. Results were described and interpreted according to the obtained p-values. Statistical significance was accepted if p-values were less than 0.05. Statistical analysis was performed using GRAPHPAD PRISM 6 (San Diego, CA, USA). 3. Results 3.1. Demographic, Clinical, and Educational Characteristics of Study Group 3.1.1. Health Status, Medical Conditions, Medication Thirty-three students with severe neurological impairment with a mean age of 13.3 ± 4.9 years were included in this study, of whom 36.4% were female. Demographic and clinical characteristics are summarized in Table 1. Main diagnosis was CP in 57.6% (19), of which 18 were spastic and one was mixed type. Furthermore, 15.2% (five) had hereditary diseases (Sd. Cornelia de Lange, Sd. Smith-Lemli-Optiz, Sd. Pallister-Killian, Pompe disease, and hypermagnesemia), 12.1% (four) had epileptic encephalopathy, and 15.2% (five) had other disorders (ependymoma, meningoencephalitis), while 30.3% (10) of the study group had gastrointestinal comorbidities, 45.5% had epilepsy, and 27.3% had orthopedic disorders. Table 1. Anthropometric characteristics of students according to age group. Variable, Mean (SD) Total (n = 33) Group 5–12 years (n = 16) Group 13–23 years (n = 17) p Mean age, years 13.3 (4.9) 9.1 (3.8) 17.2 (2.8) - GMFCS (Median IQ range) 5 (2–5) 4 (3–5) 4.5 (2–5) 0.806 II 21.2 12.5 29.4 III 15.2 25 5.9 0.235 IV 24.2 31.3 17.7 V 39.4 31.3 47.1 Mean body weight, kg 28.8 (13) 21.6 (6) 35.5 (14.3) 0.001 Mean height, cm 127.2 (19.5) 115.3 (15.1) 138.4 (16.7) 0.001 Mean knee length, cm 38.5 (7.2) 34.1 (5.8) 42.7 (5.7) 0.001 BMI mean, kg/m2 17 (4) 16.1 (2.2) 18.1 (5.1) 0.195 MUAC, cm 20.4 (4.2) 20 (4) 20.8 (4.4) 0.3 Skinfold measurements, mm Subscapular s. 9.1 (7.4) 7.5 (5.4) 10.8 (9) 0.066 Triceps s. 9.3 (5.3) 9.1 (3.6) 9.5 (6.6) 0.439 Abdominal s. 7.4 (7) 6.1 (4.4) 8.8 (8.8) 0.649 GMFCS: gross motor function classification system; MUAC: mid upper arm circumference; BMI: body mass index; s: skinfolds. Nutrients 2021, 13, 2413 9 of 30 Chronic pharmacologic treatments included benzodiazepines in 51.5% of students (17), antiepileptics in 42.4% (14), and muscle relaxant compounds in 24.2% (eight). Moreover, 15.2% (five) took proton pump inhibitors, as well as vitamin and mineral supplements. Other drugs used were inhaled corticoids (12.1%), inhaled beta-adrenergic agonists (9.1%), antipsychotics (6.1%), inhaled anticholinergics (6.1%), and systemic antihistamines, opioids, and systemic anticholinergics (3%). During the year prior to the study, 10 of these students required visits to an acute hospital emergency department. Of these, seven had to go for respiratory infection, two went for orthopedic or traumatology causes, and one went for irritability. Furthermore, eight required hospital admission, the main causes being pneumonia (three) and orthopedic or traumatology causes (three); other causes of admission were epilepsy (n = 1) or placement of a PEG (n = 1). In the previous year, the mean number of visits per student to the emergency department was 1.9, and the mean hospitalization time was 2.3 days. 3.1.2. Gross Motor Function (GMFCS) and Social Factors The assessment of the GMFCS and functional abilities described a severely impaired study group: 13 patients (39.4%) were classified as GMFCS level 5, eight (24.2%) were classified as GMFCS level 4, five (15.2%) were classified as GMFCS level 3, and seven (21.2%) were classified as GMFCS level 2. None had GMFCS level 1. Grouping these results showed that 63.6% (21) students had GMFCS 4/5 and 36.3% (12) students had GMFCS 2/3. Those with a higher score had a greater need of PEG for feeding (38.1% (eight) vs. 16.7% (two); not significant). Following this same categorization and taking into account that the prevalence of OD was very high, it was observed that students with a lower GMFCS had a significantly lower prevalence of impaired safety of swallowing (75% (nine) vs. 100% (21); p = 0.040). If we analyze those who could ingest food orally, with or without PEG, individuals with GMFCS 4/5 were more dependent for eating (83.3% (10) vs. 66.7% (eight); not significant), needed more textural adaptation of the diet (83.3% (10) vs. 33.3% (four), p = 0.036), higher premature and uncontrolled spillage to the pharynx (83.3% (eight) vs. 16.7% (two), p = 0.036), and less ability to perform chewing movements (8.3% (one) vs. 41.7% (five), p = 0.027) than those with GMFCS 2/3. Students and their families represented the ethnic, racial, and socioeconomic diversity of the demographics of the Maresme Region in Catalonia, Spain. Arboç school has a large range of cultural diversity (48% of the students come from different countries or have parents from countries other than Spain) and a disadvantaged socioeconomic condition (50%). The level of absenteeism at school was very high (22% in a year) mainly due to family and/or social issues related to the complex management of students, family decisions to prevent illness especially during the fall and winter seasons, and/or illness itself. 3.2. Oral-Motor Evaluation and Meal Observation, Swallowing Function (V-VST), EDACS, and Masticatory Capacity 3.2.1. Oral-Motor Assessment Results and Meal Observation Swallowing assessment was performed on all 32 students. According to oral-motor assessment, 81.2% (26) showed mastication impairment and 53.1% (17) had premature spillage of the bolus into the pharynx; 50% (16) of students had impaired tongue thrust, 31.2% (10) showed impaired bolus formation, and 12.5% (4) presented drooling. Up to 41.7% (10) presented spontaneous neck hyperextension when swallowing during mealtimes. The oral-motor evaluation was carried out on the 24 students who were eating by mouth. During meal observation, the most relevant results were impaired lip seal with loss of food in 54.2% (13), excessive tongue protrusion in 66.7% (16), accumulation of the bolus in the mouth in 45.8% (11), slow food management rhythm (>30 min) in 41.7% (10), and drooling in 16.7% (four). In addition, 70.8% (17) presented uncontrolled premature spillage of the bolus into the pharynx: 41.7% (10) at low viscosity (<50 mPa·s), 25% (six) at medium viscosity (250 mPa·s), and 4.2% (one) at high viscosity (800 mPa·s). Moreover, 76.5 (13) had (22/24) were fed and hydrated orally and 8.33% (2/24) were fed and hydrated orally, a well as using a PEG tube. Signs of impaired efficacy and safety of swallow were found i 100% (24/24) and 87.5% (21/24) of students, respectively. Nutrients 2021, 13, 2413 Results from the V‐VST showed higher prevalence of unsafe swallows 10 of 30with thi liquid viscosity (76.5%) (p < 0.0001) vs. 250 mPa∙s (70.8%) and 800 mPa∙s (4.4%). The safe viscosity was 800 mPa∙s, with significant differences when compared with thin liqui (4.4% vs. 76.5% adequate postureunsafe swallows, for feeding, p < 0.0001; 29.3 (seven) n = 17)with were eating andautonomy, 250 mPa∙s and(4.4% only vs. one70.8% had unsaf hyperactivity. None had an aversion to food. swallows, p < 0.0479; n = 24) (Figure 1). When we analyzed the effect of volume on th Regarding prevalence the feeding of unsafe method swallows, weused, up to 75% observed (24) students significant were fedbetween differences orally and liquid an 31.3% (10) had a gastrostomy. Of the latter, 12.1% (two) combined oral feeding with PEG. 800 mPa∙s in 5 mL, 10 mL, and 15 mL, respectively (41.2% vs. 0%, p < 0.0083; 40% vs. 4.2% Only 21.9% (seven) of evaluated students were independent feeders and the rest needed p professional < 0.019; 33.3% vs. 0%, p < 0.0369). We also found significant differences between 5 m assistance. 250 mPa∙s and thin liquid (12.5% vs. 41.2%, p < 0.0044). The most prevalent clinical sign o 3.2.2. Prevalence unsafe swallow was of OD and Effect cough, of Bolus observed inVolume and Viscosity 54.2% (13) (V-VST) during V‐VST. (Figur of the students 2). According to theincluded All the students GLM, we found in the SLP aassessment significant(32)effect of viscosity had OD; those whoon thebe could prevalence fed o orally underwent oral-motor evaluation, masticatory capacity, and clinical students with safe swallow (p = 0.004 at 5 mL, p = 0.035 at 10 mL, and p = 0.178 at 20 mL) assessment of swallowing Regarding function (V-VST) impaired at the school. efficacy Thosewe of swallow, fedfound and hydrated exclusively by a high prevalence in PEG all the teste (25% (eight)) were previously evaluated by VFS at the hospital. Considering all diagnostic viscosities: 100% at 250 mPa∙s (n = 24), 95.8% at thin liquid viscosity (n = 24), and 82.4% a methods together, up to 90.6% (29/32) had impaired safety of swallow and all of them had 800 mPa∙s efficacy (n = 24), with impairments. no significant Twenty-four studentsdifferences between were assessed by thethem. V-VST,Itofwas whom observed 91.7% that, a the volume increased with medium and high (22/24) were fed and hydrated orally and 8.33% (2/24) were fed and hydrated orally,ofasimpaire viscosity, the prevalence efficacy of swallow well as using also Signs a PEG tube. increased. Low efficacy of impaired viscosityandfollowed a similarwere safety of swallow trend except found in for th 100% (24/24) and 87.5% (21/24) of students, respectively. 10 mL volume, which had a lower prevalence than the 5 mL volume (Figure 2). The mo Results prevalent from thesign clinical V-VST ofshowed impaired higher prevalence efficacy was of unsafe swallows observed oral residue, with thin liquidin 71.2% o viscosity (76.5%) (p < 0.0001) vs. 250 mPa·s (70.8%) and 800 mPa·s (4.4%). The safest students, followed by pharyngeal residue in 58.3% of cases. Summarizing, V‐VST resul viscosity was 800 mPa·s, with significant differences when compared with thin liquid showed high prevalence of clinical signs of impaired safety of swallow with thin liquid (4.4% vs. 76.5% unsafe swallows, p < 0.0001; n = 17) and 250 mPa·s (4.4% vs. 70.8% unsafe (<50 mPa∙s)p