Abstract
Objective:
Quick, sensitive dysphagia screening tools are necessary to identify high-risk patients for further evaluation in busy multidisciplinary amyotrophic lateral sclerosis (ALS) clinics. We examined the relationship between self-perceived dysphagia using the validated Eating Assessment Tool-10 (EAT-10) and videofluoroscopic analysis of swallowing safety and efficiency.
Methods:
Individuals with ALS completed the EAT-10 and a videofluoroscopic swallowing study. Duplicate, independent, blinded analyses of the validated Dynamic Imaging Grade of Swallowing Toxicity (DIGEST) scale were performed to index swallowing safety and efficiency (mild dysphagia: DIGEST≥1, moderate dysphagia: DIGEST≥2). A between groups ANOVA with Games-Howell test for post-hoc pairwise comparisons was performed to examine EAT-10 scores across dysphagia severity levels. Receiver operator characteristic curve analysis, area under the curve (AUC), sensitivity, specificity, positive/negative predictive values (PPV, NPV), and odds ratios (OR) were derived.
Results:
435 paired EAT-10 and DIGEST scores were analyzed. Mean EAT-10 score was 8.48 (95% CI: 7.63, 9.33). Individuals with dysphagia demonstrated higher EAT-10 scores (mild: 4.1 vs. 11.3, moderate: 6.0 vs. 17.5, p<0.001). Mean EAT-10 scores increased across DIGEST levels (D0: 4.1, D1:7.9, D2: 15.1, D3: 20.4, D4: 39.0). For mild dysphagia, an EAT-10 cut score of 3 was optimal: AUC 0.74 (95% CI: 0.69–0.78; sensitivity: 77%; specificity: 53%; PPV: 71%; NPV: 60%; OR: 3.5). An EAT-10 cut score of 7 optimized detection of moderate dysphagia: AUC 0.83 (95% CI: 0.78–0.87; sensitivity: 81%; specificity: 66%; PPV: 39%; NPV: 93%; OR: 8.1).
Conclusion:
The EAT-10 is an easy-to-administer dysphagia screening tool with good discriminant ability for use in ALS clinics.
Level of Evidence:
2
Keywords: dysphagia, amyotrophic lateral sclerosis, patient reported outcome, swallowing, screening
Introduction:
Bulbar dysfunction is a hallmark feature of amyotrophic lateral sclerosis (ALS), leading to swallowing impairment (dysphagia) in over 85% of patients.1–3 Dysphagia in ALS is noted to lead to malnutrition, dehydration, aspiration, pneumonia, social isolation, and reduced quality of life.4–10 These life-threatening and psychosocial sequelae underscore the critical need for early detection and accurate ongoing monitoring of swallowing function in patients with ALS.11–13 A recent survey identified inconsistent bulbar assessment practices across ALS centers in the United States and concluded that a critical need exists for a set of standardized, pragmatic, and sensitive clinical probes for implementation in multidisciplinary ALS clinics.13 This led to the development of preliminary guidelines from the Northeast ALS Consortium bulbar committee for the assessment and monitoring of bulbar function.11 These preliminary guidelines included use of an objective and validated patient reported outcome (PRO) for swallowing.11
The Eating Assessment Tool-10 (EAT-10) is a 10 item, validated swallowing PRO indexing the perceived degree of impairment in swallowing safety and efficiency as well as swallowing-related pleasure, stress, pain, and weight loss.14 Although originally disseminated in English in 2008, the EAT-10 has since been validated in over 10 different languages, making it a widely used swallowing PRO around the world.14–22 Although the EAT-10 has received criticism regarding inherent floor effects and questionable construct validity,23–26 reports of the EAT-10’s utility as a screening tool to identify individuals who aspirate in patients with chronic obstructive pulmonary disease,27 head and neck cancer,28 neurologic disease,29,30 elderly long term care residents,31 hospitalized inpatients,32 and outpatients with suspected dysphagia33 have emerged over the past decade. Indeed, our group has previously investigated the discriminant ability of the EAT-10 PRO to identify radiographically confirmed aspiration in 70 individuals with ALS.12 An EAT-10 cut point of ≥8 conferred a sensitivity of 86%, a specificity of 72%, and a likelihood ratio of 3.1 for aspiration.12 One limitation of this previous study; however, is the focus on the clinical utility of the EAT-10 to identify impairments in swallowing safety. The EAT-10 also includes items to effectively probe swallowing efficiency (e.g., “when I swallow food sticks in my throat”), however, the ability of the EAT-10 to detect functional swallowing impairments (i.e., impairments in swallowing safety and efficiency) has not yet been examined. This is particularly relevant to explore in people with ALS because impairments in swallowing efficiency are reported to be four times more likely to emerge before the development of impairments in swallowing safety.34,35 Given recent criticisms that the EAT-10 may not have adequate sensitivity to capture early or milder swallowing impairments due to reported floor effects,23–26 we wished to examine the discriminant ability of the EAT-10 to identify functional impairments in swallowing efficiency and/or safety (i.e., pharyngeal dysphagia) in individuals with ALS.36
Materials and Methods:
Research Participants
This study was approved by the University Institutional Review Board and was conducted in accordance with the Declaration of Helsinki. Two hundred and seventy three individuals with a confirmed diagnosis of ALS (Revised El-Escorial Criteria)37 by board certified neuromuscular neurologists, with no allergies to barium, and who were still consuming some form of food or liquid oral intake were included in this study. Mean participant age was 63 years (range: 28–85, SD: 10.44), and 53.5% were males (n=146). ALS disease onset type was spinal in 55.7% (n=152), bulbar in 35.9% (n=98), mixed in 4.0% (n=11), and undetermined in 4.4% (n=12). Mean ALS Functional Rating Scale-Revised (ALSFRS-R)38 score was 35.2 (range: 12–48, SD: 7.48), and mean ALSFRS-R bulbar score was 9.2 (range: 2–12, SD: 2.31). Average disease duration from symptom onset was 25 months (range: 0–237 months, SD: 25.4). All participants provided written informed consent. Participants enrolled in this longitudinal research study attended research visits at our research laboratory every 3 months and underwent a battery of pulmonary, cough, and swallowing assessments. We included data from all research study visits where individuals with ALS completed the EAT-10 and a standardized videofluoroscopic swallow evaluation (VF).
Testing Procedures:
The Eating Assessment Tool (EAT-10)
Participants were brought into a private evaluation room and comfortably positioned (either seated or in their wheelchair). A research speech-language pathologist provided patients with the EAT-10 survey and explained its purpose and scoring rubric. The participant was then asked to complete the EAT-10 survey independently. As needed, the research speech-language pathologist offered physical assistance to those who were unable to grip a pen or select survey responses due to severe limb weakness. In these cases, the researcher sat next to the participant and selected each EAT-10 item response provided by the participant (either verbally, by pointing, or a head nod if unable to verbalize). A complete list of the EAT-10 questions can be viewed in Table 1.
Table 1:
List of questions from the Eating Assessment Tool 10 (EAT-10) questionnaire.
| Question Number | Question |
|---|---|
| 1 | My swallowing problem has caused me to lose weight. |
| 2 | My swallowing problem interferes with my ability to go out for meals. |
| 3 | Swallowing liquids takes extra effort. |
| 4 | Swallowing solids takes extra effort. |
| 5 | Swallowing pills takes extra effort. |
| 6 | Swallowing is painful. |
| 7 | The pleasure of eating is affected by my swallowing. |
| 8 | When I swallow food sticks in my throat. |
| 9 | I cough when I eat. |
| 10 | Swallowing is stressful. |
Videofluoroscopic Swallowing Evaluations (VFs)
VFs were conducted in the same room using a Phillips BV Endura fluoroscopic C-arm unit (GE OEC 9900 Elite Digital Mobile C-Arm system type 718074). Videofluoroscopic imaging data was obtained in the lateral plane using continuous fluoroscopy and recorded at 30 frames per second (FPS) via a TIMS DICOM unit with automatic bolus trial splicing (Version 3.2, TIMS Medical, TM, Chelmsford, MA). Participants underwent a standardized barium trial protocol with 13 tasks: a single saliva swallow, three 5cc thin liquid boluses via a 30cc medicine cup, one comfortable cup sip of thin liquid from a cup filled to 90cc, a sequential drinking challenge of the remaining thin liquid from the 90cc cup, three 5cc thin honey boluses via a spoon, two 5cc pudding trials via a spoon, ¼ graham cracker coated with pudding, and a 13mm barium tablet (EZ-Disk). All trials were cued except for the comfortable cup sip and sequential swallowing trials. Varibar barium sulfate products (Bracco Imaging, Monroe Township, NJ) were used for all bolus trials, which have subsequently been mapped to the International Dysphagia Diet Standardization Initiative (IDDSI) framework: thin liquid trials (IDDSI level 0), thin honey trials (IDDSI level 3), pudding trials (IDDSI level ≥4), and graham crackers (IDDSI level 7).39 To maintain safety for participants undergoing a standardized VF, bolus administration was discontinued if the participant demonstrated three episodes of aspiration or was unable to clear >75% pharyngeal residue.
EAT-10 and DIGEST Scoring Procedures
Total EAT-10 scores were calculated with scores ranging from 0 (no perceived swallowing impairment) to 40 (severe perceived swallowing impairment). Duplicate DIGEST ratings were performed by trained and blinded raters with use of consensus meetings to finalize any discrepant ratings. The validated Dynamic Imaging Grade of Swallowing Toxicity (DIGEST) scale was utilized as a functional index/metric of functional swallowing safety and efficiency36,40 using all bolus trials except the sequential bolus chug challenge task and the barium tablet trial (given the validated procedures of the DIGEST scale does not include ratings of a chug challenge task or a barium tablet). The DIGEST is a validated five-point ordinal scale created to assess both efficiency and safety of bolus flow during the entirety of a VF to determine clinically relevant categories of overall pharyngeal dysphagia severity levels.36 DIGEST total scores are a composite of two sub scores (scored 0–4) that address swallowing efficiency and swallowing safety. The swallowing efficiency score is based on the amount of the bolus remaining in the pharynx after the initial swallow (<10%, 10–49%, 50–90%, >90%) and the bolus consistency that leads to residue (liquid, pudding, cracker). The airway safety score is based on the depth and response of airway invasion (penetration-aspiration scale [PAS] score),41,42 the frequency of airway invasion (intermittent, chronic, neither), and the amount of airway invasion (trace, gross, neither). Total and sub score grades of zero indicate functional swallowing while total and sub score grades of 4 indicate life-threatening dysphagia. Utilizing previously established thresholds to indicate mild and moderate dysphagia,36,43 two cut points were examined that included a total DIGEST score of ≥1 (mild or worse dysphagia) and a score of ≥2 (moderate or worse dysphagia).
Statistical Analysis:
A between groups analysis of variance (ANOVA) was conducted to compare EAT-10 scores across DIGEST levels (0–4), with Games-Howell test used for post hoc pairwise comparisons (which accounts for unequal variances). An independent samples t-test was performed to assess potential differences in EAT-10 scores between binary dysphagia groups (e.g., dysphagia vs. no dysphagia) and to determine significant between DIGEST level differences in EAT-10 scores. Both ANOVA and t-test analyses used Welch’s correction to account for unequal variances across groups. Significance level was set at p < 0.05. To assess the discriminatory ability of the EAT-10 to identify functional swallowing safety and efficiency impairments in ALS, receiver operating characteristic (ROC) curve and bootstrapped area under the curve (AUC) analyses (95% confidence interval, CI), sensitivity, specificity, positive and negative predictive values (PPV, NPV), and odds ratios (95% confidence intervals) were conducted. Obtained data for each potential EAT-10 score were reviewed and an optimal EAT-10 score maximizing sensitivity while balancing specificity was selected.
Results:
Percent agreement for DIGEST scores across raters was 91.3% (inter-rater agreement).
EAT-10 scores across DIGEST levels:
Sample size across DIGEST levels was D-0= 172, D-1=170, D-2=54, D-3=38, D-4=1. Mean EAT-10 score increased with increasing DIGEST levels (Figure 1). A significant main effect was noted for EAT-10 and DIGEST scores, F(3,111.2)= 48.1 (Welch’s), p < 0.001. Mean EAT-10 scores (95% CI) for DIGEST (D) Levels were D-0=4.1 (2.9, 5.2); D-1= 7.9 (6.8, 9.1); D-2= 15.1 (13.0, 17.1); D-3= 20.4 (17.6, 22.8); D-4=39.0. Given the sample size for D-4 was n=1, D-4 was combined with D-3 for ANOVA analysis, with mean EAT-10 scores (95% CI) for combined D-3 and D-4 of 20.9 (18.5, 23.3). Post-hoc tests determined significant between DIGEST level differences in EAT-10 scores across all DIGEST levels (p<0.05) except for DIGEST levels 2 vs. 3/4 (p=0.054).
Figure 1:
Mean Eating Assessment Tool-10 (EAT-10) scores (95% confidence intervals) across Dynamic Imaging Grade of Swallowing Toxicity (DIGEST) levels with significant between DIGEST level differences in EAT-10 scores across all DIGEST levels (p<0.05) except for DIGEST levels 2 vs. 3/4 (p=0.054). Note: DIGEST-3 and DIGEST-4 were combined for ANOVA.
EAT −10 scores across dysphagia groups (DIGEST≥1):
VF revealed that 60% (n=263) of instrumental exam exhibited mild or worse swallowing safety and efficiency impairments and 40% (n=172) did not have dysphagia. EAT-10 scores were significantly higher for the DIGEST ≥1 dysphagia group, t= 9.7, df =420.9, p < 0.0001, mean difference 7.2 (Figure 2).
Figure 2:
Eating Assessment Tool-10 (EAT-10) scores across binary pharyngeal dysphagia groups for a) mild or worse dysphagia (DIGEST≥1) and b) moderate or worse dysphagia (DIGEST≥2) in 435 paired data-points from 273 Individuals with amyotrophic lateral sclerosis.
EAT −10 scores across dysphagia groups (DIGEST≥2):
Twenty-one percent (n=93) of radiographic tests were classified as having moderate or worse swallowing safety and efficiency impairments, with 79% (n=342) classified as not having dysphagia. EAT-10 scores were significantly higher for the DIGEST≥2 dysphagia group, t= 9.9, df = 115.2, p < 0.001, mean difference 11.5 (Figure 2).
Discriminant Ability of the EAT-10 to Detect Dysphagia Status:
ROC curve results for the EAT-10 score to detect radiographically confirmed swallowing safety and efficiency impairments (mild and moderate) are presented in Tables 2–4 and Figure 3. A DIGEST cutoff ≥1 resulted in an AUC= 0.74 (bootstrapped 95% CI: 0.69–0.78). Using a DIGEST cutoff ≥2, AUC = 0.83 (bootstrapped 95% CI: 0.78–0.87). Table 5 summarizes the sensitivity, specificity, and positive and negative predictive values for individual EAT-10 items to detect swallowing safety and efficiency impairments (mild and moderate) using a cut score of 1.
Table 2.
Summary of receiver operator characteristic curve results (95% confidence intervals) for the Eating Assessment Tool-10 (EAT-10) total score to detect mild or worse and moderate or worse swallowing safety and efficiency impairments in individuals with amyotrophic lateral sclerosis (n=435).
| DIGEST ≥1 | EAT-10 ≥ 3 | EAT-10 ≥ 4 | EAT-10 ≥ 5 | EAT-10 ≥ 6 | EAT-10 ≥ 7 | EAT-10 ≥ 8 | EAT-10 ≥ 9 | EAT-10 ≥ 10 | EAT-10 ≥ 11 |
|---|---|---|---|---|---|---|---|---|---|
| Sensitivity: | 0.77 (0.71, 0.82) |
0.69 (0.63, 0.75) |
0.65 (0.59, 0.71) |
0.61 (0.55, 0.67) |
0.57 (0.50, 0.63) |
0.53 (0.47, 0.59) |
0.49 (0.43, 0.56) |
0.48 (0.41, 0.54) |
0.44 (0.38, 0.51) |
| Specificity: | 0.53 (0.45, 0.61) |
0.61 (0.53, 0.68) |
0.65 (0.57, 0.72) |
0.69 (0.62, 0.76) |
0.76 (0.68, 0.82) |
0.81 (0.75, 0.87) |
0.83 (0.76, 0.88) |
0.85 (0.79, 0.90) |
0.88 (0.83, 0.93) |
| PPV: | 0.71 (0.66, 0.77) |
0.73 (0.67, 0.78) |
0.74 (0.68, 0.80) |
0.75 (0.69, 0.81) |
0.78 (0.71, 0.84) |
0.81 (0.75, 0.87) |
0.81 (0.74, 0.87) |
0.83 (0.76, 0.89) |
0.85 (0.78, 0.91) |
| NPV: | 0.60 (0.52, 0.68) |
0.56 (0.49, 0.64) |
0.55 (0.48, 0.62) |
0.54 (0.47, 0.61) |
0.53 (0.47, 0.60) |
0.53 (0.47, 0.59) |
0.52 (0.46, 0.58) |
0.52 (0.46, 0.58) |
0.51 (0.45, 0.57) |
| DIGEST ≥2 | EAT-10 > 3 | EAT-10 > 4 | EAT-10 > 5 | EAT-10 > 6 | EAT-10 > 7 | EAT-10 > 8 | EAT-10 > 9 | EAT-10 > 10 | EAT-10 > 11 |
| Sensitivity: | 0.95 (0.88, 0.98) |
0.90 (0.82, 0.95) |
0.85 (0.76, 0.92) |
0.82 (0.72, 0.89) |
0.81 (0.71, 0.88) |
0.76 (0.66, 0.85) |
0.74 (0.64, 0.83) |
0.72 (0.62, 0.81) |
0.70 (0.60, 0.79) |
| Specificity: | 0.43 (0.38, 0.48) |
0.52 (0.46, 0.57) |
0.56 (0.50, 0.61) |
0.60 (0.54, 0.65) |
0.66 (0.61, 0.71) |
0.70 (0.65, 0.75) |
0.73 (0.68, 0.78) |
0.76 (0.71, 0.80) |
0.79 (0.74, 0.83) |
| PPV: | 0.31 (0.26, 0.37) |
0.34 (0.28, 0.40) |
0.34 (0.28, 0.41) |
0.36 (0.29, 0.42) |
0.39 (0.32, 0.47) |
0.41 (0.34, 0.49) |
0.43 (0.35, 0.51) |
0.45 (0.37, 0.53) |
0.47 (0.39, 0.56) |
| NPV: | 0.97 (0.92, 0.99) |
0.95 (0.91, 0.98) |
0.93 (0.89, 0.96) |
0.92 (0.88, 0.95) |
0.93 (0.89, 0.96) |
0.92 (0.88, 0.95) |
0.91 (0.87, 0.94) |
0.91 (0.87, 0.94) |
0.91 (0.87, 0.94) |
DIGEST: Dynamic Imaging Grade of Swallowing Toxicity; PPV: Positive Predictive Value; NPV: Negative Predictive Value
Table 4:
Two-by-two contingency table depicting the relative frequency of individuals with amyotrophic lateral sclerosis who scored above or equal to 7 on the Eating Assessment Tool-10 (EAT-10) screen, by their instrumental videofluoroscopic swallowing exam dysphagia classification (based on a dynamic imaging grade of swallowing toxicity score ≥2).
| Instrumental Exam: | |||
|---|---|---|---|
| Dysphagia: | No Dysphagia: | ||
| EAT-10 Screen: | ≥7 EAT-10 (fail): | 75 (true +) | 116 (false +) |
| <7 EAT-10 (pass): | 18 (false −) | 226 (true −) | |
Figure 3:
Receiver operator characteristic curve results for the Eating Assessment Tool-10 (EAT-10) to detect a) mild or worse dysphagia (DIGEST≥1) and b) moderate or worse dysphagia (DIGEST≥2).
Table 5:
Receiver operator characteristic curve results (95% confidence intervals) for Eating Assessment Tool-10 (EAT-10) individual items to detect mild or worse and moderate or worse swallowing safety and efficiency impairments in individuals with amyotrophic lateral sclerosis (n=435) using a cut score of 1.
| DIGEST≥1 | AUC (95%CI) |
Sensitivity (95%CI) |
Specificity (95%CI) |
PPV (95%CI) |
NPV (95%CI) |
|---|---|---|---|---|---|
| Q1 Caused me to lose weight | 0.65 (0.61–0.68) |
0.77 (0.71–0.82) |
0.53 (0.45–0.61) |
0.71 (0.66–0.77) |
0.60 (0.52–0.68) |
| Q2 Interferes with going out | 0.64 (0.59–0.68) |
0.44 (0.38–0.50) |
0.83 (0.76–0.88) |
0.79 (0.72–0.86) |
0.49 (0.43–0.55) |
| Q3 Liquids takes extra effort | 0.66 (0.62–0.72) |
0.60 (0.54–0.66) |
0.68 (0.60–0.75) |
0.74 (0.68–0.80) |
0.53 (0.46–0.59) |
| Q4 Solids takes extra effort | 0.69 (0.64–0.73) |
0.66 (0.60–0.72) |
0.65 (0.57–0.72s) |
0.74 (0.68–0.80) |
0.56 (0.49–0.63) |
| Q5 Pills takes extra effort | 0.72 (0.67–0.76) |
0.77 (0.71–0.82) |
0.54 (0.46–0.62) |
0.72 (0.66–0.77) |
0.60 (0.52–0.68) |
| Q6 Swallowing is painful | 0.59 (0.57–0.62) |
0.19 (0.15–0.25) |
0.98 (0.95–1.00) |
0.94 (0.85–0.99) |
0.44 (0.39–0.50) |
| Q7 Eating pleasure is affected | 0.67 (0.62–0.70) |
0.54 (0.48–0.60) |
0.76 (0.68–0.82) |
0.77 (0.70–0.83) |
0.52 (0.45–0.58) |
| Q8 Food sticks in my throat | 0.70 (0.65–0.74) |
0.62 (0.56–0.68) |
0.70 (0.62–0.77) |
0.76 (0.70–0.81) |
0.55 (0.48–0.61) |
| Q9 I cough when I eat | 0.66 (0.61–0.71) |
0.66 (0.60–0.72) |
0.59 (0.51–0.66) |
0.71 (0.65–0.77) |
0.53 (0.46–0.60) |
| Q10 Swallowing is stressful | 0.67 (0.62–0.71) |
0.56 (0.49–0.62) |
0.75 (0.68–0.81) |
0.77 (0.71–0.83) |
0.52 (0.46–0.59) |
| DIGEST≥2 | AUC (95%CI) |
Sensitivity (95%CI) |
Specificity (95%CI) |
PPV (95%CI) |
NPV (95%CI) |
| Q1 Caused me to lose weight | 0.73 (0.68–0.79) |
0.60 (0.50–0.70) |
0.83 (0.79–0.87) |
0.49 (0.40–0.59) |
0.88 (0.84–0.92) |
| Q2 Interferes with going out | 0.73 (0.68–0.79) |
0.67 (0.56–0.76) |
0.76 (0.71–0.80) |
0.43 (0.35–0.51) |
0.89 (0.85–0.93) |
| Q3 Liquids takes extra effort | 0.75 (0.69–0.80) |
0.81 (0.71–0.88) |
0.60 (0.54–0.65) |
0.35 (0.29–0.42) |
0.92 (0.87–0.95) |
| Q4 Solids takes extra effort | 0.78 (0.73–0.83) |
0.85 (0.76–0.92) |
0.55 (0.49–0.60) |
0.34 (0.28–0.40) |
0.93 (0.89–0.96) |
| Q5 Pills takes extra effort | 0.79 (0.74–0.83) |
0.96 (0.89–0.99) |
0.44 (0.39–0.49) |
0.32 (0.26–0.37) |
0.97 (0.93–0.99) |
| Q6 Swallowing is painful | 0.62 (0.57–0.68) |
0.31 (0.22–0.42) |
0.93 (0.89–0.95) |
0.54 (0.40–0.67) |
0.83 (0.79–0.87) |
| Q7 Eating pleasure is affected | 0.75 (0.70–0.81) |
0.75 (0.65–0.84) |
0.67 (0.61–0.72) |
0.38 (0.31–0.45) |
0.91 (0.87–0.94) |
| Q8 Food sticks in my throat | 0.74 (0.68–0.80) |
0.75 (0.65–0.84) |
0.58 (0.52–0.63) |
0.33 (0.26–0.39) |
0.90 (0.85–0.93) |
| Q9 I cough when I eat | 0.75 (0.69–0.80) |
0.82 (0.72–0.89) |
0.51 (0.45–0.56) |
0.31 (0.25–0.37) |
0.91 (0.86–0.95) |
| Q10 Swallowing is stressful | 0.75 (0.69–0.79) |
0.76 (0.66–0.85) |
0.65 (0.60–0.71) |
0.38 (0.31–0.45) |
0.91 (0.87–0.94) |
Selection and Optimization of an EAT-10 Screening Cut Point for Dysphagia:
Inspection of Table 2 reveals that the EAT-10 score maximizing sensitivity while still preserving an acceptable level of specificity in this large ALS cohort is 3 for mild or worse dysphagia and 7 for moderate or worse dysphagia. An EAT-10 cut score of ≥3 yielded a sensitivity of 77%, specificity of 53%, PPV of 71%, and a NPV of 60%. An EAT-10 cut score of ≥7 yielded a sensitivity of 81%, specificity of 66%, PPV of 39%, and a NPV of 93%. Individuals can use the raw EAT-10 ROC data provided in Table 2 to identify what cut score best suits their needs for detecting safety and efficiency impairments across dysphagia severity levels. Individuals with ALS with an EAT-10 score ≥3 had 3.52 times higher odds of having radiographically confirmed mild dysphagia (95% CI:2.35, 5.27) while individuals with ALS with an EAT-10 score ≥7 had 8.1 times higher odds of having radiographically confirmed moderate dysphagia (95% CI: 4.63, 14.23).
Discussion:
In this dataset of 435 paired EAT-10 and VFs from 273 individuals with ALS, the EAT-10 PRO demonstrated good clinical utility for use as a dysphagia screening tool for individuals with ALS. EAT-10 scores were higher with increasing swallowing safety and efficiency impairments (DIGEST levels) and the mean EAT-10 score was approximately three times higher in ALS individuals with confirmed dysphagia compared to those without. Individuals with ALS reporting an EAT-10 score of ≥3 had 3.5 times higher odds of mild swallowing safety and efficiency impairments (DIGEST≥1) and individuals with ALS reporting an EAT-10 score of ≥7 had 8 times higher odds of having moderate swallowing safety and efficiency impairments. This conferred a sensitivity of 77% and specificity of 53% for detecting mild or worse dysphagia (DIGEST≥1), and a sensitivity of 81% and a specificity of 66% for detecting radiographically confirmed moderate or worse pharyngeal dysphagia (DIGEST ≥2).
A total of 263 VF exams from individuals with ALS exhibited mild or worse swallowing safety and efficiency impairments. Out of 263 VF exams, the EAT-10 correctly classified 202 exams with dysphagia (true positives) and misclassified 61 cases (false negatives) with a cut score of 3. In contrast, an EAT-10 cut score of 3 correctly identified the absence of dysphagia for 91 VF exams or 53% (true negatives), while 81 or 47% of VF exams without dysphagia had EAT-10 scores higher than 3 (false positives). The overall accuracy when using an EAT-10 cut score of 3 to detect mild or worse swallowing safety and efficiency impairments was 67%.
Of the 93 tests with moderate or worse dysphagia, the EAT-10 correctly classified 75 cases (true positives) but misclassified 18 cases (false negatives) using a cut score of 7. Of the 342 non-dysphagic VF exams, 226 or 66% had EAT-10 scores less than/equal to 7 (true negative), while 116 or 34% had scores higher than 7 (false positives). The overall accuracy of the EAT-10 using this assigned threshold to detect pharyngeal swallow function was 69%.
The current findings align with our previous research in a smaller ALS dataset (n=70) focusing on swallowing safety that determined that a cut score of ≥8 yielded excellent sensitivity (86%) and specificity (72%) for identifying aspirating individuals with ALS (AUC: 0.88, PPV: 43%, NPV: 96%). Here, we validated and expanded the scope of our analysis to include both swallowing safety and efficiency in a larger group of patients with ALS (435 vs. 70 paired data points) to examine the EAT-10’s ability to detect functional swallowing safety and efficiency impairments. These results hold great clinical relevance given recent data indicating that efficiency impairments are more prevalent than safety impairments in ALS and approximately four times more likely to be the initial presenting swallowing impairment.34,35
Although the EAT-10 demonstrated adequate sensitivity to detect impairments in swallowing safety and efficiency in people with ALS, 142 tests (32.6%) for detecting mild or worse dysphagia and 134 tests (30.8%) for detecting moderate or worse dysphagia were misclassified. The majority of these misclassifications (n=81, n=116) constituted false positives whereby a non-dysphagic individual with ALS was classified as an individual with dysphagia, with 61 and 18 false negatives for mild vs. moderate dysphagia respectively (incorrectly classifying a dysphagic individual as non-dysphagic). By design, and similar to other screening tools, our chosen cut point minimized false negatives due to the potential negative consequences of “missing” a subsequent dysphagia diagnosis, at the expense of increased over-referral.
Although relatively low (mild: n=61, moderate: n=18), one possible explanation for the false negatives could relate to the known high prevalence of silent aspiration in individuals with ALS.34,44–46 Because the EAT-10 is a PRO, people with ALS who silently aspirate may rate their swallowing difficulties as less severe since they do not experience overt signs and symptoms related to airway invasion (i.e., reflexive cough or throat clear). Another potential explanation for these false negatives could be the rapidly progressive nature of ALS, which may prompt subconscious use of swallowing/mealtime adaptations or modifications as swallow function gradually deteriorates (e.g., avoid certain foods/drinks, cut food into small bites, etc.).
In contrast, potential explanations for the noted false positive cases (mild: n=81, moderate: n=116, patients without swallowing safety and efficiency impairments with EAT-10 scores ≥3 or ≥7 respectively) could relate to general ALS deconditioning and limb motor impairment affecting both mealtime length, fatigue and relative effort expenditure given that three EAT-10 items (items 3, 4, 5) relate to “extra effort” that could increase overall scores due to unrelated factors. The specificity data for the item analysis of effort related questions tends to support this notion given that they ranged between 44% and 60%. Similarly, individuals with ALS are known to have a higher resting metabolic rate, burning on average, 30% more calories than non-ALS individuals with known weight loss and the need to consume more calories to maintain weight.47 Although item 1 on the EAT-10 asks a patient if their “swallowing problem has caused them to lose weight”, it is possible that the underlying hypermetabolism of ALS may inflate this item score in some ALS individuals. Finally, many individuals with ALS report difficulties leaving the home due to mobility and transportation requirements that might impact patient responses to items 2 and 10. Another important consideration when interpreting these data, is that the DIGEST scale represents a metric of swallowing safety and efficiency impairment in the pharyngeal phase of swallowing, and not in the oral or esophageal phases. It is therefore possible that some of these false positives may have been reporting issues related to an oral or esophageal dysphagia.
Future studies may consider the EAT-10’s ability to detect oropharyngeal and esophageal dysphagia in people with ALS. It would also be useful to determine the EAT-10’s clinical utility in detecting pharyngeal dysphagia in people with ALS throughout the disease course as impairments in swallowing safety and efficiency progress. To reduce patient burden, future research work could also examine the concordance of patient and caregiver EAT-10 scores to determine if caregiver ratings may serve as a valid surrogate in instances where a patient is unable to communicate due to anarthria or fatigue. Given the increased use of telehealth services for ALS health monitoring, this may be critical for future clinical services.
Limitations:
While this study included a relatively large cohort of people with ALS, it would be useful to replicate this work across multiple external sites to externally validate these findings where demographic and geographic variables may differ. Our study team selected an EAT-10 cutoff of 3 for mild or worse dysphagia and 7 for moderate or worse dysphagia, favoring sensitivity over specificity, given rapid progression of ALS and high rates of dysphagia. However, lower specificity may result in unnecessary testing procedures, leading to the potential misuse of time and resources in this vulnerable clinical patient population. However, we have included in this paper the full ROC outcomes so that clinicians may select a meaningful cut point for their intended use. Finally, the EAT-10 is only one aspect of dysphagia screening with a need for future investigation using a combination of tools that collectively may improve the discriminant ability to detect functional swallowing safety and efficiency impairments in people with ALS.
Conclusion:
The EAT-10 represents a pragmatic and low-burden PRO that demonstrates good clinical utility to identify functional swallowing safety and efficiency impairments in individuals with ALS. Given our previous and current findings, the EAT-10 along with other physiologic markers of swallowing safety and efficiency, could be included in dysphagia screening protocols to identify and triage patients for further clinical and/or instrumental swallowing evaluation. Quick, noninvasive, and accurate dysphagia screening tools such as the EAT-10 have the potential to facilitate improved dysphagia management of people with ALS via early detection of swallowing impairments and early implementation of interventions as warranted. Future work is needed to externally validate the current finding where geographic and/or demographic variables may differ.
Table 3:
Two-by-two contingency table depicting the relative frequency of individuals with amyotrophic lateral sclerosis who scored above or equal to 3 on the Eating Assessment Tool-10 (EAT-10) screen, by their instrumental videofluoroscopic swallowing exam dysphagia classification (based on a dynamic imaging grade of swallowing toxicity score ≥1).
| Instrumental Exam: | |||
|---|---|---|---|
| Dysphagia: | No Dysphagia: | ||
| EAT-10 Screen: | ≥3 EAT-10 (fail): | 202 (true +) | 81 (false +) |
| <3 EAT-10 (pass): | 61 (false −) | 91 (true −) | |
Funding:
Research reported in this publication was supported, fully or in part, by grants from the National Institute of Neurological Disorders and Stroke (NINDS, Award Number 1R01NS100859), the Amyotrophic Lateral Sclerosis Association (ALSA Clinical Management Grant), the Dr. Jon and Nancy McEwans Wilkins Fellowship for ALS Research Fund, and the University of Florida McKnight Brain Institute and BREATHING Research and Therapeutics Center. Content is solely the responsibility of the authors and does not necessarily represent the official views of these organizations.
Footnotes
Conflict of interest: We have no conflicts of interest to declare.
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