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Bedside diagnosis of dysphagia: A systematic review
Author(s)
John C. O'Horo, MD, MPH
Nicole Rogus‐Pulia, PhD, CCC‐SLP
Lisbeth Garcia‐Arguello, MD
JoAnne Robbins, PhD
Nasia Safdar, MD, PhD

Dysphagia is a serious medical condition that can lead to aspiration pneumonia, malnutrition, and dehydration.[1] Dysphagia is the result of a variety of medical etiologies, including stroke, traumatic brain injury, progressive neurologic conditions, head and neck cancers, and general deconditioning. Prevalence estimates for dysphagia vary depending upon the etiology and patient age, but estimates as high as 38% for lifetime prevalence have been reported in those over age 65 years.[2]

To avoid adverse health outcomes, early detection of dysphagia is essential. In hospitalized patients, early detection has been associated with reduced risk of pneumonia, decreased length of hospital stay, and improved cost‐effectiveness resulting from a reduction in hospital days due to fewer cases of aspiration pneumonia.[3, 4, 5] Stroke guidelines in the United States recommend screening for dysphagia for all patients admitted with stroke.[6] Consequently, the majority of screening procedures have been designed for and tested in this population.[7, 8, 9, 10]

The videofluoroscopic swallow study (VFSS) is a commonly accepted, reference standard, instrumental evaluation technique for dysphagia, as it provides the most comprehensive information regarding anatomic and physiologic function for swallowing diagnosis and treatment. Flexible endoscopic evaluation of swallowing (FEES) is also available, as are several less commonly used techniques (scintigraphy, manometry, and ultrasound). Due to availability, patient compliance, and expertise needed, it is not possible to perform instrumental examination on every patient with suspected dysphagia. Therefore, a number of minimally invasive bedside screening procedures for dysphagia have been developed.

The value of any diagnostic screening test centers on performance characteristics, which under ideal circumstances include a positive result for all those who have dysphagia (sensitivity) and negative result for all those who do not have dysphagia (specificity). Such an ideal screening procedure would reduce unnecessary referrals and testing, thus resulting in cost savings, more effective utilization of speech‐language pathology consultation services, and less unnecessary radiation exposure. In addition, an effective screen would detect all those at risk for aspiration pneumonia in need of intervention. However, most available bedside screening tools are lacking in some or all of these desirable attributes.[11, 12] We undertook a systematic review and meta‐analysis of bedside procedures to screen for dysphagia.

METHODS

Data Sources and Searches

We conducted a comprehensive search of 7 databases, including MEDLINE, Embase, and Scopus, from each database's earliest inception through June 9, 2014 for English‐language articles and abstracts. The search strategy was designed and conducted by an experienced librarian with input from 1 researcher (J.C.O.). Controlled vocabulary supplemented with keywords was used to search for comparative studies of bedside screening tests for predicting dysphagia (see Supporting Information, Appendix 1, in the online version of this article for the full strategy).

All abstracts were screened, and potentially relevant articles were identified for full‐text review. Those references were manually inspected to identify all relevant studies.

Study Selection

A study was eligible for inclusion if it tested a diagnostic swallow study of any variety against an acceptable reference standard (VFSS or flexible endoscopic evaluation of swallowing with sensory testing [FEEST]).

Data Extraction and Quality Assessment

The primary outcome of the study was aspiration, as predicted by a bedside exam, compared to gold‐standard visualization of aspirated material entering below the vocal cords. From each study, data were abstracted based on the type of diagnostic method and reference standard study population and inclusion/exclusion characteristics, design, and prediction of aspiration. Prediction of aspiration was compared against the reference standard to yield true positives, true negatives, false positives, and false negatives. Additional potential confounding variables were abstracted using a standard form based on the Preferred Reporting Items for Systematic Reviews and Meta‐Analysis[13] (see Supporting Information, Appendix 2, in the online version of this article for the full abstraction template).

Data Synthesis and Analysis

Sensitivity and specificity for each test that identified the presence of dysphagia was calculated for each study. These were used to generate positive and negative likelihood ratios (LRs), which were plotted on a likelihood matrix, a graphic depiction of the logarithm of the +LR on the ordinate versus the logarithm of the LR on the abscissa, dividing the graphic into quadrants such that the right upper quadrant is tests that can be used for confirmation, right lower quadrant neither confirmation nor exclusion, left lower quadrant exclusion only, and left upper quadrant an ideal test with both exclusionary and confirmatory properties.[14] A good screening test would thus be on the left half of the graphic to effectively rule out dysphagia, and the ideal test with both good sensitivity and specificity would be found in the left upper quadrant. Graphics were constructed using the Stata MIDAS package (Stata Corp., College Station, TX).[15]

RESULTS

We identified 891 distinct articles. Of these, 749 were excluded based on abstract review. After reviewing the remaining 142 full‐text articles, 48 articles were determined to meet inclusion criteria, which included 10,437 observations across 7414 patients (Figure 1). We initially intended to conduct a meta‐analysis on each type, but heterogeneity in design and statistical heterogeneity in aggregate measures precluded pooling of results.

Figure 1
Preferred Reporting Items for Systematic Reviews and Meta‐Analysis flow diagram. Abbreviations: FEEST, flexible endoscopic evaluation of swallowing with sensory testing; VFSS, videofluoroscopic swallow study.

Characteristics of Included Studies

Of the 48 included studies, the majority (n=42) were prospective observational studies,[7, 8, 14, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49, 50, 51, 52, 53] whereas 2 were randomized trials,[9, 54] 2 studies were double‐blind observational,[9, 16] 1 was a case‐control design,[55] and 1 was a retrospective case series.[56] The majority of studies were exclusively inpatient,[7, 8, 9, 14, 17, 18, 19, 21, 22, 24, 25, 26, 31, 32, 33, 35, 36, 38, 41, 43, 44, 45, 46, 47, 49, 51, 52, 53, 55, 57] with 5 in mixed in and outpatient populations,[20, 27, 40, 55, 58] 2 in outpatient populations,[23, 41] and the remainder not reporting the setting from which they drew their study populations.

The indications for swallow evaluations fit broadly into 4 categories: stroke,[7, 8, 9, 14, 21, 22, 24, 25, 26, 31, 33, 34, 35, 38, 40, 41, 42, 43, 45, 48, 52, 56, 58] other neurologic disorders,[17, 18, 23, 28, 39, 47] all causes,[16, 20, 27, 29, 30, 36, 37, 44, 46, 49, 51, 52, 53, 54, 58] and postsurgical.[19, 32, 34] Most used VFSS as a reference standard,[7, 8, 9, 14, 16, 17, 18, 19, 21, 22, 23, 25, 26, 27, 28, 29, 30, 34, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 50, 51, 52, 53, 54, 56, 57, 58] with 8 using FEEST,[20, 24, 31, 32, 33, 35, 49, 55] and 1 accepting either videofluoroscopic evaluation of swallow or FEEST.[48]

Studies were placed into 1 or more of the following 4 categories: subjective bedside examination,[8, 9, 18, 19, 31, 34, 48] questionnaire‐based tools,[17, 23, 46, 53] protocolized multi‐item evaluations,[20, 21, 22, 25, 30, 33, 34, 37, 39, 44, 45, 52, 53, 57, 58] and single‐item exam maneuvers, symptoms, or signs.[7, 9, 14, 16, 24, 26, 27, 28, 29, 30, 31, 32, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 47, 48, 49, 50, 51, 56, 58, 59] The characteristics of all studies are detailed in Table 1.

Characteristics of Included Studies
Study Location Design Mean Age (SD) Reason(s) for Dysphagia Indx Test Description Reference Standard Sample Size, No. of Patients Sample Size, No. of Observations

  • NOTE: Abbreviations: BSA, bedside assessment; EAT‐10, Eating Assessment Tool; FEES, flexible endoscopic evaluation of swallowing; FEEST, flexible endoscopic evaluation of swallowing with sensory testing; NR, not reported; SD, standard deviation; VFSS, videofluoroscopic swallow study; WST, Water swallow test. *SD not available. Median provided instead of mean.

Splaingard et al., 198844 Milwaukee, WI, USA Prospective observational study NR Multiple Clinical bedside swallow exam Combination of scored comprehensive physical exam, history, and observed swallow. VFSS 107 107
DePippo et al., 199243 White Plains, NY, USA Prospective observational study 71 (10) Stroke WST Observation of swallow. VFSS 44
Horner et al., 199356 Durham, NC, USA Retrospective case series 64* Stroke Clinical bedside swallow evaluation VFSS 38 114
Kidd et al., 199342 Belfast, UK Prospective observational study 72 (10) Stroke Bedside 50‐mL swallow evaluation Patient swallows 50 mL of water in 5‐mL aliquots, with therapist assessing for choking, coughing, or change in vocal quality after each swallow. VFSS 60 240
Collins and Bakheit, 199741 Southampton, UK Prospective observational study 65* Stroke Desaturation Desaturation of at least 2% during videofluoroscopic study. VFSS 54 54
Daniels et al., 199740 New Orleans, LA, USA Prospective observational study 66 (11) Stroke Clinical bedside examination 6 individual bedside assessments (dysphonia, dysphagia, cough before/after swallow, gag reflex and voice change) examined as predictors for aspiration risk. VFSS 59 354
Mari et al., 199739 Ancona, Italy Prospective observational study 60 (16) Mixed neurologic diseases Combined history and exam Assessed symptoms of dysphagia, cough, and 3‐oz water swallow. VFSS 93 372
Daniels et al., 19987 New Orleans, LA, USA Prospective observational study 66 (11) Stroke Clinical bedside swallow evaluation Describes sensitivity and specificity of several component physical exam maneuvers comprising the bedside exam. VFSS 55 330
Smithard et al., 19988 Ashford, UK Prospective observational study 79* Stroke Clinical bedside swallow evaluation Not described. VFSS 83 249
Addington et al., 199938 Kansas City, MO, USA Prospective observational study 80* Stroke NR Reflex cough. VFSS 40 40
Logemann et al., 199937 Evanston, IL, USA Prospective observational study 65 Multiple Northwestern Dysphagia Check Sheet 28‐item screening procedure including history, observed swallow, and physical exam. VFSS 200 1400
Smith et al., 20009 Manchester, UK Double blind observational 69 Stroke Clinical bedside swallow evaluation, pulse oximetry evaluation After eating/drinking, patient is evaluated for signs of aspiration including coughing, choking, or "wet voice." Procedure is repeated with several consistencies. Also evaluated if patient desaturates by at least 2% during evaluation. VFSS 53 53
Warms et al., 200036 Melbourne, Australia Prospective observational study 67 Multiple Wet voice Voice was recorded and analyzed with Sony digital audio tape during videofluoroscopy. VFSS 23 708
Lim et al., 200135 Singapore, Singapore Prospective observational study NR Stroke Water swallow test, desaturation during swallow 50‐mL swallow done in 5‐mL aliquots with assessment of phonation/choking afterward; desaturation >2% during swallow, FEEST 50 100
McCullough et al., 200134 Nashville, TN, USA Prospective observational study 60 (10) Stroke Clinical bedside swallow evaluation 15‐item physical exam with observed swallow. VFSS 2040 60
Rosen et al., 2001[74] Newark, NJ, USA Prospective observational study 60 Head and Neck cancer Wet voice Observation of swallow. VFSS 26 26
Leder and Espinosa, 200233 New Haven, CT, USA Prospective observational study 70* Stroke Clinical exam Checklist evaluation of cough and voice change after swallow, volitional cough, dysphonia, dysarthria, and abnormal gag. FEEST 49 49
Belafsky et al., 200332 San Francisco, CA, USA Prospective observational study 65 (11) Post‐tracheostomy patients Modified Evans Blue Dye Test 3 boluses of dye‐impregnated ice are given to patient. Tracheal secretions are suctioned, and evaluated for the presence of dye. FEES 30 30
Chong et al., 200331 Jalan Tan Tock Seng, Singapore Prospective observational study 75 (7) Stroke Water swallow test, desaturation during, clinical exam Subjective exam, drinking 50 mL of water in 10‐mL aliquots, and evaluating for desaturation >2% during FEES. FEEST 50 150
Tohara et al., 200330 Tokyo, Japan Prospective observational study 63 (17) Multiple Food/water swallow tests, and a combination of the 2 Protocolized observation of sequential food and water swallows with scored outcomes. VFSS 63 63
Rosenbek et al., 200414 Gainesville, FL, USA Prospective observational study 68* Stroke Clinical bedside swallow evaluation Describes 5 parameters of voice quality and 15 physical examination maneuvers used. VFSS 60 1200
Ryu et al., 200429 Seoul, South Korea Prospective observational study 64 (14) Multiple Voice analysis parameters Analysis of the/a/vowel sound with Visi‐Pitch II 3300. VFSS 93 372
Shaw et al., 200428 Sheffield, UK Prospective observational study 71 Neurologic disease Bronchial auscultation Auscultation over the right main bronchus during trial feeding to listen for sounds of aspiration. VFSS 105 105
Wu et al., 200427 Taipei, Taiwan Prospective observational study 72 (11) Multiple 100‐mL swallow test Patient lifts a glass of 100 mL of water and drinks as quickly as possible, and is assessed for signs of choking, coughing, or wet voice, and is timed for speed of drinking. VFSS 54 54
Nishiwaki et al., 200526 Shizuoaka, Japan Prospective observational study 70* Stroke Clinical bedside swallow evaluation Describes sensitivity and specificity of several component physical exam maneuvers comprising the bedside exam. VFSS 31 248
Wang et al., 200554 Taipei, Taiwan Prospective double‐blind study 41* Multiple Desaturation Desaturation of at least 2% during videofluoroscopic study. VFSS 60 60
Ramsey et al., 200625 Kent, UK Prospective observational study 71 (10) Stroke BSA Assessment of lip seal, tongue movement, voice quality, cough, and observed 5‐mL swallow. VFSS 54 54
Trapl et al., 200724 Krems, Austria Prospective observational study 76 (2) Stroke Gugging Swallow Screen Progressive observed swallow trials with saliva, then with 350 mL liquid, then dry bread. FEEST 49 49
Suiter and Leder, 200849 Several centers across the USA Prospective observational study 68.3 Multiple 3‐oz water swallow test Observation of swallow. FEEST 3000 3000
Wagasugi et al., 200850 Tokyo, Japan Prospective observational study NR Multiple Cough test Acoustic analysis of cough. VFSS 204 204
Baylow et al., 200945 New York, NY, USA Prospective observational study NR Stroke Northwestern Dysphagia Check Sheet 28‐item screening procedure including history, observed swallow, and physical exam. VFSS 15 30
Cox et al., 200923 Leiden, the Netherlands Prospective observational study 68 (8) Inclusion body myositis Dysphagia questionnaire Questionnaire assessing symptoms of dysphagia. VFSS 57 57
Kagaya et al., 201051 Tokyo, Japan Prospective observational study NR Multiple Simple Swallow Provocation Test Injection of 1‐2 mL of water through nasal tube directed at the suprapharynx. VFSS 46 46
Martino et al., 200957 Toronto, Canada Randomized trial 69 (14) Stroke Toronto Bedside Swallow Screening Test 4‐item physical assessment including Kidd water swallow test, pharyngeal sensation, tongue movement, and dysphonia (before and after water swallow). VFSS 59 59
Santamato et al., 200955 Bari, Italy Case control NR Multiple Acoustic analysis, postswallow apnea Acoustic analysis of cough. VFSS 15 15
Smith Hammond et al., 200948 Durham, NC, USA Prospective observational study 67.7 (1.2) Multiple Cough, expiratory phase peak flow Acoustic analysis of cough. VFSS or FEES 96 288
Leigh et al., 201022 Seoul, South Korea Prospective observational study NR Stroke Clinical bedside swallow evaluation Not described. VFSS 167 167
Pitts et al., 201047 Gainesville, FL, USA Prospective observational study NR Parkinson Cough compression phase duration Acoustic analysis of cough. VFSS 58 232
Cohen and Manor, 201146 Tel Aviv, Israel Prospective observational Study NR Multiple Swallow Disturbance Questionnaire 15‐item questionnaire. FEES 100 100
Edmiaston et al., 201121 St. Louis, MO, USA Prospective observational study 63* Stroke SWALLOW‐3D Acute Stroke Dysphagia Screen 5‐item screen including mental status; asymmetry or weakness of face, tongue, or palate; and subjective signs of aspiration when drinking 3 oz water. VFSS 225 225
Mandysova et al., 201120 Pardubice, Czech Republic Prospective observational study 69 (13) Multiple Brief Bedside Dysphagia Screening Test 8‐item physician exam including ability to clench teeth; symmetry/strength of tongue, facial, and shoulder muscles; dysarthria; and choking, coughing, or dripping of food after taking thick liquid. FEES 87 87
Steele et al., 201158 Toronto, Canada Double blind observational 67 Stroke 4‐item bedside exam Tongue lateralization, cough, throat clear, and voice quality. VFSS 400 40
Yamamoto et al., 201117 Kodaira, Japan Prospective observational study 67 (9) Parkinson's Disease Swallowing Disturbance Questionnaire 15‐item questionnaire. VFSS 61 61
Bhama et al., 201219 Pittsburgh, PA, USA Prospective observational study 57 (14) Post‐lung transplant Clinical bedside swallow evaluation Not described. VFSS 128 128
Shem et al., 201218 San Jose, CA, USA Prospective observational study 42 (17) Spinal cord injuries resulting in tetraplegia Clinical bedside swallow evaluation After eating/drinking, patient is evaluated for signs of aspiration including coughing, choking, or "wet voice." Procedure is repeated with several consistencies. VFSS 26 26
Steele et al., 201316 Toronto, Canada Prospective observational study 67 (14) Multiple Dual‐axis accelerometry Computed accelerometry of swallow. VFSS 37 37
Edmiaston et al., 201452 St. Louis, MO, USA Prospective observational study 63 (15) Stroke Barnes Jewish Stroke Dysphagia Screen 5‐item screen including mental status; asymmetry or weakness of face, tongue, or palate; and subjective signs of aspiration when drinking 3 oz water. VFSS 225 225
Rofes et al., 201453 Barcelona, Spain Prospective observational study 74 (12) Mixed EAT‐10 questionnaire and variable viscosity swallow test Symptom‐based questionnaire (EAT‐10) and repeated observations and measurements of swallow with different thickness liquids. VFS 134 134

Subjective Clinical Exam

Seven studies reported the sensitivity and specificity of subjective assessments of nurses and speech‐language pathologists in observing swallowing and predicting aspiration.[8, 9, 18, 19, 31, 34, 48] The overall distribution of studies is summarized in the likelihood matrix in Figure 2. Two studies, Chong et al.[31] and Shem et al.,[18] were on the left side of the matrix, indicating a sensitive rule‐out test. However, both were small studies, and only Chong et al. reported reasonable sensitivity with incorporation bias from knowledge of a desaturation study outcome. Overall, subjective exams did not appear reliable in ruling out dysphagia.

Figure 2
Likelihood matrix for curve for subjective clinical exam. Each point corresponds to a study as follows: 1 = Smithard et al., 1998; 2 = Smith et al., 2000; 3 = McCullough et al., 2001; 4 = Chong et al., 2003; 5 = Smith‐Hammond et al., 2009; 6 = Bhama et al., 2012; 7 = Shem et al., 2012. LUQ = Left upper quadrant, LRP = Positive likelihood ratio, RUQ = Right upper quadrant, LLQ = Left lower quadrant, RLQ = Right lower quadrant, LRN = Negative likelihood ratio.

Questionnaire‐Based Tools

Only 4 studies used questionnaire‐based tools filled out by the patient, asking about subjective assessment of dysphagia symptoms and frequency.[17, 23, 46, 53] Yamamoto et al. reported results of using the swallow dysphagia questionnaire in patients with Parkinson's disease.[17] Rofes et al. looked at the Eating Assessment Tool (EAT‐10) questionnaire among all referred patients and a small population of healthy volunteers.[53] Each was administered the questionnaire before undergoing a videofluoroscopic study. Overall, sensitivity and specificity were 77.8% and 84.6%, respectively. Cox et al. studied a different questionnaire in a group of patients with inclusion body myositis, finding 70% sensitivity and 44% specificity.[23] Cohen and Manor examined the swallow dysphagia questionnaire across several different causes of dysphagia, finding at optimum, the test is 78% specific and 73% sensitive.[46] Rofes et al. had an 86% sensitivity and 68% specificity for the EAT‐10 tool.[53]

Multi‐Item Exam Protocols

Sixteen studies reported multistep protocols for determining a patient's risk for aspiration.[9, 20, 21, 22, 25, 30, 33, 34, 37, 39, 44, 45, 52, 53, 57, 58] Each involved a combination of physical exam maneuvers and history elements, detailed in Table 1. This is shown in the likelihood matrix in Figure 3. Only 2 of these studies were in the left lower quadrant, Edmiaston et al. 201121 and 2014.[52] Both studies were restricted to stroke populations, but found reasonable sensitivity and specificity in identifying dysphagia.

Figure 3
Likelihood matrix of multi‐item protocols. 1 = Splaingard et al., 1988; 2 = Mari et al., 1997; 3 = Logemann et al., 1999; 4 = Smith et al., 2000; 5 = McCullough et al., 2001; 6 = Leder et al., 2002; 7 = Tohara et al., 2003; 8 = Ramsey et al., 2006; 9 = Baylow et al., 2009; 10 = Martino et al., 2009; 11 = Leigh et al., 2010; 12 = Mandysova et al., 2011; 13 = Steele et al., 2011 (speech language pathology assessment); 14 = Edmiaston et al., 2011; 15 = Steele et al. (nurse assessment); 16 = Edmiaston et al., 2014; 17 = Rofes et al., 2014. LUQ = Left upper quadrant, LRP = Positive likelihood ratio, RUQ = Right upper quadrant, LLQ = Left lower quadrant, RLQ = Right lower quadrant, LRN = Negative likelihood ratio.

Individual Exam Maneuvers

Thirty studies reported the diagnostic performance of individual exam maneuvers and signs.[7, 9, 14, 16, 24, 26, 27, 28, 29, 30, 31, 32, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 47, 48, 49, 50, 51, 54, 56, 58] Each is depicted in Figure 4 as a likelihood matrix demonstrating the +LR and LR for individual maneuvers as seen in the figure; most fall into the right lower quadrant, where they are not diagnostically useful tests. Studies in the left lower quadrant demonstrating the ability to exclude aspiration desirable in a screening test were dysphonia in McCullough et al.,[34] dual‐axis accelerometry in Steele et al.,[16] and the water swallow test in DePippo et al.[43] and Suiter and Leder.[49]

Figure 4
Likelihood matrix of individual exam maneuvers. Studies in the LLQ demonstrating the ability to exclude aspiration were 56 = Kidd et al., 1993 (abnormal pharyngeal sensation); 96 = McCullogh et al., 2001 (dysphonia); 54 = Steele et al., 2013 (dual axis accelerometry); 121 = DePippo et al., 1992 (water swallow test); and 118 = Suiter and Leder et al., 2008 (water swallow test). (See Supporting Information, Appendix 3, in the online version of this article for the key to other tests). LUQ = Left upper quadrant, LRP = Positive likelihood ratio, RUQ = Right upper quadrant, LLQ = Left lower quadrant, RLQ = Right lower quadrant, LRN = Negative likelihood ratio.

McCullough et al. found dysphonia to be the most discriminatory sign or symptom assessed, with an area under the curve (AUC) of 0.818. Dysphonia was judged by a sustained/a/and had 100% sensitivity but only 27% specificity. Wet voice within the same study was slightly less informative, with an AUC of 0.77 (sensitivity 50% and specificity 84%).[34]

Kidd et al. verified the diagnosis of stroke, and then assessed several neurologic parameters, including speech, muscle strength, and sensation. Pharyngeal sensation was assessed by touching each side of the pharyngeal wall and asking patients if they felt sensation that differed from each side. Patient report of abnormal sensation during this maneuver was 80% sensitive and 86% specific as a predictor of aspiration on VFSS.[42]

Steele et al. described the technique of dual axis accelerometry, where an accelerometer was placed at the midline of the neck over the cricoid cartilage during VFSS. The movement of the cricoid cartilage was captured for analysis in a computer algorithm to identify abnormal pharyngeal swallow behavior. Sensitivity was 100%, and specificity was 54%. Although the study was small (n=40), this novel method demonstrated good discrimination.[58]

DePippo et al. evaluated a 3‐oz water swallow in stroke patients. This protocol called for patients to drink the bolus of water without interruption, and be observed for 1 minute after for cough or wet‐hoarse voice. Presence of either sign was considered abnormal. Overall, sensitivity was 94% and specificity 30% looking for the presence of either sign.[43] Suiter and Leder used a similar protocol, with sensitivity of 97% and specificity of 49%.[49]

DISCUSSION

Our results show that most bedside swallow examinations lack the sensitivity to be used as a screening test for dysphagia across all patient populations examined. This is unfortunate as the ability to determine which patients require formal speech language pathology consultation or imaging as part of their diagnostic evaluation early in the hospital stay would lead to improved allocation of resources, cost reductions, and earlier implementation of effective therapy approaches. Furthermore, although radiation doses received during VFSS are not high when compared with other radiologic exams like computed tomography scans,[60] increasing awareness about the long‐term malignancy risks associated with medical imaging makes it desirable to reduce any test involving ionizing radiation.

There were several categories of screening procedures identified during this review process. Those classified as subjective bedside exams and protocolized multi‐item evaluations were found to have high heterogeneity in their sensitivity and specificity, though a few exam protocols did have a reasonable sensitivity and specificity.[21, 31, 52] The following individual exam maneuvers were found to demonstrate high sensitivity and an ability to exclude aspiration: a test for dysphonia through production of a sustained/a/34 and use of dual‐axis accelerometry.[16] Two other tests, the 3‐oz water swallow test[43] and testing of abnormal pharyngeal sensation,[42] were each found effective in a single study, with conflicting results from other studies.

Our results extend the findings from previous systematic reviews on this subject, most of which focused only on stroke patients.[5, 12, 61, 62] Martino and colleagues[5] conducted a review focused on screening for adults poststroke. From 13 identified articles, it was concluded that evidence to support inclusion or exclusion of screening was poor. Daniels et al. conducted a systematic review of swallowing screening tools specific to patients with acute or chronic stroke.[12] Based on 16 articles, the authors concluded that a combination of swallowing and nonswallowing features may be necessary for development of a valid screening tool. The generalizability of these reviews is limited given that all were conducted in patients poststroke, and therefore results and recommendations may not be generalizable to other patients.

Wilkinson et al.[62] conducted a recent systematic review that focused on screening techniques for inpatients 65 years or older that excluded patients with stroke or Parkinson's disease. The purpose of that review was to examine sensitivity and specificity of bedside screening tests as well as ability to accurately predict pneumonia. The authors concluded that existing evidence is not sufficient to recommend the use of bedside tests in a general older population.[62]

Specific screening tools identified by Martino and colleagues[5] to have good predictive value in detecting aspiration as a diagnostic marker of dysphagia were an abnormal test of pharyngeal sensation[42] and the 50‐mL water swallow test. Daniels et al. identified a water swallow test as an important component of a screen.[7] These results were consistent with those of this review in that the abnormal test of pharyngeal sensation[42] was identified for high levels of sensitivity. However, the 3‐oz water swallow test,[43, 49] rather than the 50‐mL water swallow test,[42] was identified in this review as the version of the water swallow test with the best predictive value in ruling out aspiration. Results of our review identified 2 additional individual items, dual‐axis accelerometry[16] and dysphonia,[34] that may be important to include in a comprehensive screening tool. In the absence of better tools, the 3 oz swallow test, properly executed, seems to be the best currently available tool validated in more than 1 study.

Several studies in the current review included an assessment of oral tongue movement that is not described thoroughly and varies between studies. Tongue movement as an individual item on a screening protocol was not found to yield high sensitivity or specificity. However, tongue movement or range of motion is only 1 aspect of oral tongue function; pressures produced by the tongue reflecting strength also may be important and warrant evaluation. Multiple studies have shown patients with dysphagia resulting from a variety of etiologies to produce lower than normal maximum isometric lingual pressures,[63, 64, 65, 66, 67, 68] or pressures produced when the tongue is pushed as hard as possible against the hard palate. Tongue strengthening protocols that result in higher maximum isometric lingual pressures have been shown to carry over to positive changes in swallow function.[69, 70, 71, 72, 73] Inclusion of tongue pressure measurement in a comprehensive screening tool may help to improve predictive capabilities.

We believe our results have implications for practicing clinicians, and serve as a call to action for development of an easy‐to‐perform, accurate tool for dysphagia screening. Future prospective studies should focus on practical tools that can be deployed at the bedside, and correlate the results with not only gold‐standard VFSS and FEES, but with clinical outcomes such as pneumonia and aspiration events leading to prolonged length of stay.

There were several limitations to this review. High levels of heterogeneity were reported in the screening tests present in the literature, precluding meaningful meta‐analysis. In addition, the majority of studies included were in poststroke adults, which limits the generalizability of results.

In conclusion, no screening protocol has been shown to provide adequate predictive value for presence of aspiration. Several individual exam maneuvers demonstrate high sensitivity; however, the most effective combination of screening protocol components is unknown. There is a need for future research focused on the development of a comprehensive screening tool that can be applied across patient populations for accurate detection of dysphagia as well as prediction of other adverse health outcomes, including pneumonia.

Acknowledgements

The authors thank Drs. Byun‐Mo Oh and Catrionia Steele for providing additional information in response to requests for unpublished information.

Disclosures: Nasia Safdar MD, is supported by a National Institutes of Health R03 GEMSSTAR award and a VA MERIT award. The authors report no conflicts of interest.

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  35. Lim SH, Lieu PK, Phua SY, et al. Accuracy of bedside clinical methods compared with fiberoptic endoscopic examination of swallowing (FEES) in determining the risk of aspiration in acute stroke patients. Dysphagia. 2001;16(1):1–6.
  36. Warms T, Richards J. “Wet Voice” as a predictor of penetration and aspiration in oropharyngeal dysphagia. Dysphagia. 2000;15(2):84–88.
  37. Logemann JA, Veis S, Colangelo L. A screening procedure for oropharyngeal dysphagia. Dysphagia. 1999;14(1):44–51.
  38. Addington WR, Stephens RE, Gilliland K, Rodriguez M. Assessing the laryngeal cough reflex and the risk of developing pneumonia after stroke. Arch Phys Med Rehabil. 1999;80(2):150–154.
  39. Mari F, Matei M, Ceravolo MG, Pisani A, Montesi A, Provinciali L. Predictive value of clinical indices in detecting aspiration in patients with neurological disorders. J Neurol Neurosurg Psychiatry. 1997;63(4):456–460.
  40. Daniels SK, McAdam CP, Brailey K, Foundas AL. Clinical assessment of swallowing and prediction of dysphagia severity. Am J Speech Lang Pathol. 1997;6(4):17–24.
  41. Collins MJ, Bakheit AM. Does pulse oximetry reliably detect aspiration in dysphagic stroke patients? Stroke. 1997;28(9):1773–1775.
  42. Kidd D, Lawson J, Nesbitt R, MacMahon J. Aspiration in acute stroke: a clinical study with videofluoroscopy. Q J Med. 1993;86(12):825–829.
  43. DePippo KL, Holas MA, Reding MJ. Validation of the 3‐oz water swallow test for aspiration following stroke. Arch Neurol. 1992;49(12):1259–1261.
  44. Splaingard ML, Hutchins B, Sulton LD, Chaudhuri G. Aspiration in rehabilitation patients: videofluoroscopy vs bedside clinical assessment. Arch Phys Med Rehabil. 1988;69(8):637–640.
  45. Baylow HE, Goldfarb R, Taveira CH, Steinberg RS. Accuracy of clinical judgment of the chin‐down posture for dysphagia during the clinical/bedside assessment as corroborated by videofluoroscopy in adults with acute stroke. Dysphagia. 2009;24(4):423–433.
  46. Cohen JT, Manor Y. Swallowing disturbance questionnaire for detecting dysphagia. Laryngoscope. 2011;121(7):1383–1387.
  47. Pitts T, Troche M, Mann G, Rosenbek J, Okun MS, Sapienza C. Using voluntary cough to detect penetration and aspiration during oropharyngeal swallowing in patients with Parkinson disease. Chest. 2010;138(6):1426–1431.
  48. Smith Hammond CA, Goldstein LB, Horner RD, et al. Predicting aspiration in patients with ischemic stroke: comparison of clinical signs and aerodynamic measures of voluntary cough. Chest. 2009;135(3):769–777.
  49. Suiter DM, Leder SB. Clinical utility of the 3‐ounce water swallow test. Dysphagia. 2008;23(3):244–250.
  50. Wakasugi Y, Tohara H, Hattori F, et al. Screening test for silent aspiration at the bedside. Dysphagia. 2008;23(4):364–370.
  51. Kagaya H, Okada S, Saitoh E, Baba M, Yokoyama M, Takahashi H. Simple swallowing provocation test has limited applicability as a screening tool for detecting aspiration, silent aspiration, or penetration. Dysphagia. 2010;25(1):6–10.
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Article PDF
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Journal of Hospital Medicine - 10(4)
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Journal of Hospital Medicine
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256-265
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Reviews
Author(s)
John C. O'Horo, MD, MPH
Nicole Rogus‐Pulia, PhD, CCC‐SLP
Lisbeth Garcia‐Arguello, MD
JoAnne Robbins, PhD
Nasia Safdar, MD, PhD
Author(s)
John C. O'Horo, MD, MPH
Nicole Rogus‐Pulia, PhD, CCC‐SLP
Lisbeth Garcia‐Arguello, MD
JoAnne Robbins, PhD
Nasia Safdar, MD, PhD
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Supporting Information (1)
Supporting Information Appendices (2)
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Supporting Information (1)
Supporting Information Appendices (2)
Article PDF
jhm2313.pdf
Article PDF
jhm2313.pdf

Dysphagia is a serious medical condition that can lead to aspiration pneumonia, malnutrition, and dehydration.[1] Dysphagia is the result of a variety of medical etiologies, including stroke, traumatic brain injury, progressive neurologic conditions, head and neck cancers, and general deconditioning. Prevalence estimates for dysphagia vary depending upon the etiology and patient age, but estimates as high as 38% for lifetime prevalence have been reported in those over age 65 years.[2]

To avoid adverse health outcomes, early detection of dysphagia is essential. In hospitalized patients, early detection has been associated with reduced risk of pneumonia, decreased length of hospital stay, and improved cost‐effectiveness resulting from a reduction in hospital days due to fewer cases of aspiration pneumonia.[3, 4, 5] Stroke guidelines in the United States recommend screening for dysphagia for all patients admitted with stroke.[6] Consequently, the majority of screening procedures have been designed for and tested in this population.[7, 8, 9, 10]

The videofluoroscopic swallow study (VFSS) is a commonly accepted, reference standard, instrumental evaluation technique for dysphagia, as it provides the most comprehensive information regarding anatomic and physiologic function for swallowing diagnosis and treatment. Flexible endoscopic evaluation of swallowing (FEES) is also available, as are several less commonly used techniques (scintigraphy, manometry, and ultrasound). Due to availability, patient compliance, and expertise needed, it is not possible to perform instrumental examination on every patient with suspected dysphagia. Therefore, a number of minimally invasive bedside screening procedures for dysphagia have been developed.

The value of any diagnostic screening test centers on performance characteristics, which under ideal circumstances include a positive result for all those who have dysphagia (sensitivity) and negative result for all those who do not have dysphagia (specificity). Such an ideal screening procedure would reduce unnecessary referrals and testing, thus resulting in cost savings, more effective utilization of speech‐language pathology consultation services, and less unnecessary radiation exposure. In addition, an effective screen would detect all those at risk for aspiration pneumonia in need of intervention. However, most available bedside screening tools are lacking in some or all of these desirable attributes.[11, 12] We undertook a systematic review and meta‐analysis of bedside procedures to screen for dysphagia.

METHODS

Data Sources and Searches

We conducted a comprehensive search of 7 databases, including MEDLINE, Embase, and Scopus, from each database's earliest inception through June 9, 2014 for English‐language articles and abstracts. The search strategy was designed and conducted by an experienced librarian with input from 1 researcher (J.C.O.). Controlled vocabulary supplemented with keywords was used to search for comparative studies of bedside screening tests for predicting dysphagia (see Supporting Information, Appendix 1, in the online version of this article for the full strategy).

All abstracts were screened, and potentially relevant articles were identified for full‐text review. Those references were manually inspected to identify all relevant studies.

Study Selection

A study was eligible for inclusion if it tested a diagnostic swallow study of any variety against an acceptable reference standard (VFSS or flexible endoscopic evaluation of swallowing with sensory testing [FEEST]).

Data Extraction and Quality Assessment

The primary outcome of the study was aspiration, as predicted by a bedside exam, compared to gold‐standard visualization of aspirated material entering below the vocal cords. From each study, data were abstracted based on the type of diagnostic method and reference standard study population and inclusion/exclusion characteristics, design, and prediction of aspiration. Prediction of aspiration was compared against the reference standard to yield true positives, true negatives, false positives, and false negatives. Additional potential confounding variables were abstracted using a standard form based on the Preferred Reporting Items for Systematic Reviews and Meta‐Analysis[13] (see Supporting Information, Appendix 2, in the online version of this article for the full abstraction template).

Data Synthesis and Analysis

Sensitivity and specificity for each test that identified the presence of dysphagia was calculated for each study. These were used to generate positive and negative likelihood ratios (LRs), which were plotted on a likelihood matrix, a graphic depiction of the logarithm of the +LR on the ordinate versus the logarithm of the LR on the abscissa, dividing the graphic into quadrants such that the right upper quadrant is tests that can be used for confirmation, right lower quadrant neither confirmation nor exclusion, left lower quadrant exclusion only, and left upper quadrant an ideal test with both exclusionary and confirmatory properties.[14] A good screening test would thus be on the left half of the graphic to effectively rule out dysphagia, and the ideal test with both good sensitivity and specificity would be found in the left upper quadrant. Graphics were constructed using the Stata MIDAS package (Stata Corp., College Station, TX).[15]

RESULTS

We identified 891 distinct articles. Of these, 749 were excluded based on abstract review. After reviewing the remaining 142 full‐text articles, 48 articles were determined to meet inclusion criteria, which included 10,437 observations across 7414 patients (Figure 1). We initially intended to conduct a meta‐analysis on each type, but heterogeneity in design and statistical heterogeneity in aggregate measures precluded pooling of results.

Figure 1
Preferred Reporting Items for Systematic Reviews and Meta‐Analysis flow diagram. Abbreviations: FEEST, flexible endoscopic evaluation of swallowing with sensory testing; VFSS, videofluoroscopic swallow study.

Characteristics of Included Studies

Of the 48 included studies, the majority (n=42) were prospective observational studies,[7, 8, 14, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49, 50, 51, 52, 53] whereas 2 were randomized trials,[9, 54] 2 studies were double‐blind observational,[9, 16] 1 was a case‐control design,[55] and 1 was a retrospective case series.[56] The majority of studies were exclusively inpatient,[7, 8, 9, 14, 17, 18, 19, 21, 22, 24, 25, 26, 31, 32, 33, 35, 36, 38, 41, 43, 44, 45, 46, 47, 49, 51, 52, 53, 55, 57] with 5 in mixed in and outpatient populations,[20, 27, 40, 55, 58] 2 in outpatient populations,[23, 41] and the remainder not reporting the setting from which they drew their study populations.

The indications for swallow evaluations fit broadly into 4 categories: stroke,[7, 8, 9, 14, 21, 22, 24, 25, 26, 31, 33, 34, 35, 38, 40, 41, 42, 43, 45, 48, 52, 56, 58] other neurologic disorders,[17, 18, 23, 28, 39, 47] all causes,[16, 20, 27, 29, 30, 36, 37, 44, 46, 49, 51, 52, 53, 54, 58] and postsurgical.[19, 32, 34] Most used VFSS as a reference standard,[7, 8, 9, 14, 16, 17, 18, 19, 21, 22, 23, 25, 26, 27, 28, 29, 30, 34, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 50, 51, 52, 53, 54, 56, 57, 58] with 8 using FEEST,[20, 24, 31, 32, 33, 35, 49, 55] and 1 accepting either videofluoroscopic evaluation of swallow or FEEST.[48]

Studies were placed into 1 or more of the following 4 categories: subjective bedside examination,[8, 9, 18, 19, 31, 34, 48] questionnaire‐based tools,[17, 23, 46, 53] protocolized multi‐item evaluations,[20, 21, 22, 25, 30, 33, 34, 37, 39, 44, 45, 52, 53, 57, 58] and single‐item exam maneuvers, symptoms, or signs.[7, 9, 14, 16, 24, 26, 27, 28, 29, 30, 31, 32, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 47, 48, 49, 50, 51, 56, 58, 59] The characteristics of all studies are detailed in Table 1.

Characteristics of Included Studies
Study Location Design Mean Age (SD) Reason(s) for Dysphagia Indx Test Description Reference Standard Sample Size, No. of Patients Sample Size, No. of Observations

  • NOTE: Abbreviations: BSA, bedside assessment; EAT‐10, Eating Assessment Tool; FEES, flexible endoscopic evaluation of swallowing; FEEST, flexible endoscopic evaluation of swallowing with sensory testing; NR, not reported; SD, standard deviation; VFSS, videofluoroscopic swallow study; WST, Water swallow test. *SD not available. Median provided instead of mean.

Splaingard et al., 198844 Milwaukee, WI, USA Prospective observational study NR Multiple Clinical bedside swallow exam Combination of scored comprehensive physical exam, history, and observed swallow. VFSS 107 107
DePippo et al., 199243 White Plains, NY, USA Prospective observational study 71 (10) Stroke WST Observation of swallow. VFSS 44
Horner et al., 199356 Durham, NC, USA Retrospective case series 64* Stroke Clinical bedside swallow evaluation VFSS 38 114
Kidd et al., 199342 Belfast, UK Prospective observational study 72 (10) Stroke Bedside 50‐mL swallow evaluation Patient swallows 50 mL of water in 5‐mL aliquots, with therapist assessing for choking, coughing, or change in vocal quality after each swallow. VFSS 60 240
Collins and Bakheit, 199741 Southampton, UK Prospective observational study 65* Stroke Desaturation Desaturation of at least 2% during videofluoroscopic study. VFSS 54 54
Daniels et al., 199740 New Orleans, LA, USA Prospective observational study 66 (11) Stroke Clinical bedside examination 6 individual bedside assessments (dysphonia, dysphagia, cough before/after swallow, gag reflex and voice change) examined as predictors for aspiration risk. VFSS 59 354
Mari et al., 199739 Ancona, Italy Prospective observational study 60 (16) Mixed neurologic diseases Combined history and exam Assessed symptoms of dysphagia, cough, and 3‐oz water swallow. VFSS 93 372
Daniels et al., 19987 New Orleans, LA, USA Prospective observational study 66 (11) Stroke Clinical bedside swallow evaluation Describes sensitivity and specificity of several component physical exam maneuvers comprising the bedside exam. VFSS 55 330
Smithard et al., 19988 Ashford, UK Prospective observational study 79* Stroke Clinical bedside swallow evaluation Not described. VFSS 83 249
Addington et al., 199938 Kansas City, MO, USA Prospective observational study 80* Stroke NR Reflex cough. VFSS 40 40
Logemann et al., 199937 Evanston, IL, USA Prospective observational study 65 Multiple Northwestern Dysphagia Check Sheet 28‐item screening procedure including history, observed swallow, and physical exam. VFSS 200 1400
Smith et al., 20009 Manchester, UK Double blind observational 69 Stroke Clinical bedside swallow evaluation, pulse oximetry evaluation After eating/drinking, patient is evaluated for signs of aspiration including coughing, choking, or "wet voice." Procedure is repeated with several consistencies. Also evaluated if patient desaturates by at least 2% during evaluation. VFSS 53 53
Warms et al., 200036 Melbourne, Australia Prospective observational study 67 Multiple Wet voice Voice was recorded and analyzed with Sony digital audio tape during videofluoroscopy. VFSS 23 708
Lim et al., 200135 Singapore, Singapore Prospective observational study NR Stroke Water swallow test, desaturation during swallow 50‐mL swallow done in 5‐mL aliquots with assessment of phonation/choking afterward; desaturation >2% during swallow, FEEST 50 100
McCullough et al., 200134 Nashville, TN, USA Prospective observational study 60 (10) Stroke Clinical bedside swallow evaluation 15‐item physical exam with observed swallow. VFSS 2040 60
Rosen et al., 2001[74] Newark, NJ, USA Prospective observational study 60 Head and Neck cancer Wet voice Observation of swallow. VFSS 26 26
Leder and Espinosa, 200233 New Haven, CT, USA Prospective observational study 70* Stroke Clinical exam Checklist evaluation of cough and voice change after swallow, volitional cough, dysphonia, dysarthria, and abnormal gag. FEEST 49 49
Belafsky et al., 200332 San Francisco, CA, USA Prospective observational study 65 (11) Post‐tracheostomy patients Modified Evans Blue Dye Test 3 boluses of dye‐impregnated ice are given to patient. Tracheal secretions are suctioned, and evaluated for the presence of dye. FEES 30 30
Chong et al., 200331 Jalan Tan Tock Seng, Singapore Prospective observational study 75 (7) Stroke Water swallow test, desaturation during, clinical exam Subjective exam, drinking 50 mL of water in 10‐mL aliquots, and evaluating for desaturation >2% during FEES. FEEST 50 150
Tohara et al., 200330 Tokyo, Japan Prospective observational study 63 (17) Multiple Food/water swallow tests, and a combination of the 2 Protocolized observation of sequential food and water swallows with scored outcomes. VFSS 63 63
Rosenbek et al., 200414 Gainesville, FL, USA Prospective observational study 68* Stroke Clinical bedside swallow evaluation Describes 5 parameters of voice quality and 15 physical examination maneuvers used. VFSS 60 1200
Ryu et al., 200429 Seoul, South Korea Prospective observational study 64 (14) Multiple Voice analysis parameters Analysis of the/a/vowel sound with Visi‐Pitch II 3300. VFSS 93 372
Shaw et al., 200428 Sheffield, UK Prospective observational study 71 Neurologic disease Bronchial auscultation Auscultation over the right main bronchus during trial feeding to listen for sounds of aspiration. VFSS 105 105
Wu et al., 200427 Taipei, Taiwan Prospective observational study 72 (11) Multiple 100‐mL swallow test Patient lifts a glass of 100 mL of water and drinks as quickly as possible, and is assessed for signs of choking, coughing, or wet voice, and is timed for speed of drinking. VFSS 54 54
Nishiwaki et al., 200526 Shizuoaka, Japan Prospective observational study 70* Stroke Clinical bedside swallow evaluation Describes sensitivity and specificity of several component physical exam maneuvers comprising the bedside exam. VFSS 31 248
Wang et al., 200554 Taipei, Taiwan Prospective double‐blind study 41* Multiple Desaturation Desaturation of at least 2% during videofluoroscopic study. VFSS 60 60
Ramsey et al., 200625 Kent, UK Prospective observational study 71 (10) Stroke BSA Assessment of lip seal, tongue movement, voice quality, cough, and observed 5‐mL swallow. VFSS 54 54
Trapl et al., 200724 Krems, Austria Prospective observational study 76 (2) Stroke Gugging Swallow Screen Progressive observed swallow trials with saliva, then with 350 mL liquid, then dry bread. FEEST 49 49
Suiter and Leder, 200849 Several centers across the USA Prospective observational study 68.3 Multiple 3‐oz water swallow test Observation of swallow. FEEST 3000 3000
Wagasugi et al., 200850 Tokyo, Japan Prospective observational study NR Multiple Cough test Acoustic analysis of cough. VFSS 204 204
Baylow et al., 200945 New York, NY, USA Prospective observational study NR Stroke Northwestern Dysphagia Check Sheet 28‐item screening procedure including history, observed swallow, and physical exam. VFSS 15 30
Cox et al., 200923 Leiden, the Netherlands Prospective observational study 68 (8) Inclusion body myositis Dysphagia questionnaire Questionnaire assessing symptoms of dysphagia. VFSS 57 57
Kagaya et al., 201051 Tokyo, Japan Prospective observational study NR Multiple Simple Swallow Provocation Test Injection of 1‐2 mL of water through nasal tube directed at the suprapharynx. VFSS 46 46
Martino et al., 200957 Toronto, Canada Randomized trial 69 (14) Stroke Toronto Bedside Swallow Screening Test 4‐item physical assessment including Kidd water swallow test, pharyngeal sensation, tongue movement, and dysphonia (before and after water swallow). VFSS 59 59
Santamato et al., 200955 Bari, Italy Case control NR Multiple Acoustic analysis, postswallow apnea Acoustic analysis of cough. VFSS 15 15
Smith Hammond et al., 200948 Durham, NC, USA Prospective observational study 67.7 (1.2) Multiple Cough, expiratory phase peak flow Acoustic analysis of cough. VFSS or FEES 96 288
Leigh et al., 201022 Seoul, South Korea Prospective observational study NR Stroke Clinical bedside swallow evaluation Not described. VFSS 167 167
Pitts et al., 201047 Gainesville, FL, USA Prospective observational study NR Parkinson Cough compression phase duration Acoustic analysis of cough. VFSS 58 232
Cohen and Manor, 201146 Tel Aviv, Israel Prospective observational Study NR Multiple Swallow Disturbance Questionnaire 15‐item questionnaire. FEES 100 100
Edmiaston et al., 201121 St. Louis, MO, USA Prospective observational study 63* Stroke SWALLOW‐3D Acute Stroke Dysphagia Screen 5‐item screen including mental status; asymmetry or weakness of face, tongue, or palate; and subjective signs of aspiration when drinking 3 oz water. VFSS 225 225
Mandysova et al., 201120 Pardubice, Czech Republic Prospective observational study 69 (13) Multiple Brief Bedside Dysphagia Screening Test 8‐item physician exam including ability to clench teeth; symmetry/strength of tongue, facial, and shoulder muscles; dysarthria; and choking, coughing, or dripping of food after taking thick liquid. FEES 87 87
Steele et al., 201158 Toronto, Canada Double blind observational 67 Stroke 4‐item bedside exam Tongue lateralization, cough, throat clear, and voice quality. VFSS 400 40
Yamamoto et al., 201117 Kodaira, Japan Prospective observational study 67 (9) Parkinson's Disease Swallowing Disturbance Questionnaire 15‐item questionnaire. VFSS 61 61
Bhama et al., 201219 Pittsburgh, PA, USA Prospective observational study 57 (14) Post‐lung transplant Clinical bedside swallow evaluation Not described. VFSS 128 128
Shem et al., 201218 San Jose, CA, USA Prospective observational study 42 (17) Spinal cord injuries resulting in tetraplegia Clinical bedside swallow evaluation After eating/drinking, patient is evaluated for signs of aspiration including coughing, choking, or "wet voice." Procedure is repeated with several consistencies. VFSS 26 26
Steele et al., 201316 Toronto, Canada Prospective observational study 67 (14) Multiple Dual‐axis accelerometry Computed accelerometry of swallow. VFSS 37 37
Edmiaston et al., 201452 St. Louis, MO, USA Prospective observational study 63 (15) Stroke Barnes Jewish Stroke Dysphagia Screen 5‐item screen including mental status; asymmetry or weakness of face, tongue, or palate; and subjective signs of aspiration when drinking 3 oz water. VFSS 225 225
Rofes et al., 201453 Barcelona, Spain Prospective observational study 74 (12) Mixed EAT‐10 questionnaire and variable viscosity swallow test Symptom‐based questionnaire (EAT‐10) and repeated observations and measurements of swallow with different thickness liquids. VFS 134 134

Subjective Clinical Exam

Seven studies reported the sensitivity and specificity of subjective assessments of nurses and speech‐language pathologists in observing swallowing and predicting aspiration.[8, 9, 18, 19, 31, 34, 48] The overall distribution of studies is summarized in the likelihood matrix in Figure 2. Two studies, Chong et al.[31] and Shem et al.,[18] were on the left side of the matrix, indicating a sensitive rule‐out test. However, both were small studies, and only Chong et al. reported reasonable sensitivity with incorporation bias from knowledge of a desaturation study outcome. Overall, subjective exams did not appear reliable in ruling out dysphagia.

Figure 2
Likelihood matrix for curve for subjective clinical exam. Each point corresponds to a study as follows: 1 = Smithard et al., 1998; 2 = Smith et al., 2000; 3 = McCullough et al., 2001; 4 = Chong et al., 2003; 5 = Smith‐Hammond et al., 2009; 6 = Bhama et al., 2012; 7 = Shem et al., 2012. LUQ = Left upper quadrant, LRP = Positive likelihood ratio, RUQ = Right upper quadrant, LLQ = Left lower quadrant, RLQ = Right lower quadrant, LRN = Negative likelihood ratio.

Questionnaire‐Based Tools

Only 4 studies used questionnaire‐based tools filled out by the patient, asking about subjective assessment of dysphagia symptoms and frequency.[17, 23, 46, 53] Yamamoto et al. reported results of using the swallow dysphagia questionnaire in patients with Parkinson's disease.[17] Rofes et al. looked at the Eating Assessment Tool (EAT‐10) questionnaire among all referred patients and a small population of healthy volunteers.[53] Each was administered the questionnaire before undergoing a videofluoroscopic study. Overall, sensitivity and specificity were 77.8% and 84.6%, respectively. Cox et al. studied a different questionnaire in a group of patients with inclusion body myositis, finding 70% sensitivity and 44% specificity.[23] Cohen and Manor examined the swallow dysphagia questionnaire across several different causes of dysphagia, finding at optimum, the test is 78% specific and 73% sensitive.[46] Rofes et al. had an 86% sensitivity and 68% specificity for the EAT‐10 tool.[53]

Multi‐Item Exam Protocols

Sixteen studies reported multistep protocols for determining a patient's risk for aspiration.[9, 20, 21, 22, 25, 30, 33, 34, 37, 39, 44, 45, 52, 53, 57, 58] Each involved a combination of physical exam maneuvers and history elements, detailed in Table 1. This is shown in the likelihood matrix in Figure 3. Only 2 of these studies were in the left lower quadrant, Edmiaston et al. 201121 and 2014.[52] Both studies were restricted to stroke populations, but found reasonable sensitivity and specificity in identifying dysphagia.

Figure 3
Likelihood matrix of multi‐item protocols. 1 = Splaingard et al., 1988; 2 = Mari et al., 1997; 3 = Logemann et al., 1999; 4 = Smith et al., 2000; 5 = McCullough et al., 2001; 6 = Leder et al., 2002; 7 = Tohara et al., 2003; 8 = Ramsey et al., 2006; 9 = Baylow et al., 2009; 10 = Martino et al., 2009; 11 = Leigh et al., 2010; 12 = Mandysova et al., 2011; 13 = Steele et al., 2011 (speech language pathology assessment); 14 = Edmiaston et al., 2011; 15 = Steele et al. (nurse assessment); 16 = Edmiaston et al., 2014; 17 = Rofes et al., 2014. LUQ = Left upper quadrant, LRP = Positive likelihood ratio, RUQ = Right upper quadrant, LLQ = Left lower quadrant, RLQ = Right lower quadrant, LRN = Negative likelihood ratio.

Individual Exam Maneuvers

Thirty studies reported the diagnostic performance of individual exam maneuvers and signs.[7, 9, 14, 16, 24, 26, 27, 28, 29, 30, 31, 32, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 47, 48, 49, 50, 51, 54, 56, 58] Each is depicted in Figure 4 as a likelihood matrix demonstrating the +LR and LR for individual maneuvers as seen in the figure; most fall into the right lower quadrant, where they are not diagnostically useful tests. Studies in the left lower quadrant demonstrating the ability to exclude aspiration desirable in a screening test were dysphonia in McCullough et al.,[34] dual‐axis accelerometry in Steele et al.,[16] and the water swallow test in DePippo et al.[43] and Suiter and Leder.[49]

Figure 4
Likelihood matrix of individual exam maneuvers. Studies in the LLQ demonstrating the ability to exclude aspiration were 56 = Kidd et al., 1993 (abnormal pharyngeal sensation); 96 = McCullogh et al., 2001 (dysphonia); 54 = Steele et al., 2013 (dual axis accelerometry); 121 = DePippo et al., 1992 (water swallow test); and 118 = Suiter and Leder et al., 2008 (water swallow test). (See Supporting Information, Appendix 3, in the online version of this article for the key to other tests). LUQ = Left upper quadrant, LRP = Positive likelihood ratio, RUQ = Right upper quadrant, LLQ = Left lower quadrant, RLQ = Right lower quadrant, LRN = Negative likelihood ratio.

McCullough et al. found dysphonia to be the most discriminatory sign or symptom assessed, with an area under the curve (AUC) of 0.818. Dysphonia was judged by a sustained/a/and had 100% sensitivity but only 27% specificity. Wet voice within the same study was slightly less informative, with an AUC of 0.77 (sensitivity 50% and specificity 84%).[34]

Kidd et al. verified the diagnosis of stroke, and then assessed several neurologic parameters, including speech, muscle strength, and sensation. Pharyngeal sensation was assessed by touching each side of the pharyngeal wall and asking patients if they felt sensation that differed from each side. Patient report of abnormal sensation during this maneuver was 80% sensitive and 86% specific as a predictor of aspiration on VFSS.[42]

Steele et al. described the technique of dual axis accelerometry, where an accelerometer was placed at the midline of the neck over the cricoid cartilage during VFSS. The movement of the cricoid cartilage was captured for analysis in a computer algorithm to identify abnormal pharyngeal swallow behavior. Sensitivity was 100%, and specificity was 54%. Although the study was small (n=40), this novel method demonstrated good discrimination.[58]

DePippo et al. evaluated a 3‐oz water swallow in stroke patients. This protocol called for patients to drink the bolus of water without interruption, and be observed for 1 minute after for cough or wet‐hoarse voice. Presence of either sign was considered abnormal. Overall, sensitivity was 94% and specificity 30% looking for the presence of either sign.[43] Suiter and Leder used a similar protocol, with sensitivity of 97% and specificity of 49%.[49]

DISCUSSION

Our results show that most bedside swallow examinations lack the sensitivity to be used as a screening test for dysphagia across all patient populations examined. This is unfortunate as the ability to determine which patients require formal speech language pathology consultation or imaging as part of their diagnostic evaluation early in the hospital stay would lead to improved allocation of resources, cost reductions, and earlier implementation of effective therapy approaches. Furthermore, although radiation doses received during VFSS are not high when compared with other radiologic exams like computed tomography scans,[60] increasing awareness about the long‐term malignancy risks associated with medical imaging makes it desirable to reduce any test involving ionizing radiation.

There were several categories of screening procedures identified during this review process. Those classified as subjective bedside exams and protocolized multi‐item evaluations were found to have high heterogeneity in their sensitivity and specificity, though a few exam protocols did have a reasonable sensitivity and specificity.[21, 31, 52] The following individual exam maneuvers were found to demonstrate high sensitivity and an ability to exclude aspiration: a test for dysphonia through production of a sustained/a/34 and use of dual‐axis accelerometry.[16] Two other tests, the 3‐oz water swallow test[43] and testing of abnormal pharyngeal sensation,[42] were each found effective in a single study, with conflicting results from other studies.

Our results extend the findings from previous systematic reviews on this subject, most of which focused only on stroke patients.[5, 12, 61, 62] Martino and colleagues[5] conducted a review focused on screening for adults poststroke. From 13 identified articles, it was concluded that evidence to support inclusion or exclusion of screening was poor. Daniels et al. conducted a systematic review of swallowing screening tools specific to patients with acute or chronic stroke.[12] Based on 16 articles, the authors concluded that a combination of swallowing and nonswallowing features may be necessary for development of a valid screening tool. The generalizability of these reviews is limited given that all were conducted in patients poststroke, and therefore results and recommendations may not be generalizable to other patients.

Wilkinson et al.[62] conducted a recent systematic review that focused on screening techniques for inpatients 65 years or older that excluded patients with stroke or Parkinson's disease. The purpose of that review was to examine sensitivity and specificity of bedside screening tests as well as ability to accurately predict pneumonia. The authors concluded that existing evidence is not sufficient to recommend the use of bedside tests in a general older population.[62]

Specific screening tools identified by Martino and colleagues[5] to have good predictive value in detecting aspiration as a diagnostic marker of dysphagia were an abnormal test of pharyngeal sensation[42] and the 50‐mL water swallow test. Daniels et al. identified a water swallow test as an important component of a screen.[7] These results were consistent with those of this review in that the abnormal test of pharyngeal sensation[42] was identified for high levels of sensitivity. However, the 3‐oz water swallow test,[43, 49] rather than the 50‐mL water swallow test,[42] was identified in this review as the version of the water swallow test with the best predictive value in ruling out aspiration. Results of our review identified 2 additional individual items, dual‐axis accelerometry[16] and dysphonia,[34] that may be important to include in a comprehensive screening tool. In the absence of better tools, the 3 oz swallow test, properly executed, seems to be the best currently available tool validated in more than 1 study.

Several studies in the current review included an assessment of oral tongue movement that is not described thoroughly and varies between studies. Tongue movement as an individual item on a screening protocol was not found to yield high sensitivity or specificity. However, tongue movement or range of motion is only 1 aspect of oral tongue function; pressures produced by the tongue reflecting strength also may be important and warrant evaluation. Multiple studies have shown patients with dysphagia resulting from a variety of etiologies to produce lower than normal maximum isometric lingual pressures,[63, 64, 65, 66, 67, 68] or pressures produced when the tongue is pushed as hard as possible against the hard palate. Tongue strengthening protocols that result in higher maximum isometric lingual pressures have been shown to carry over to positive changes in swallow function.[69, 70, 71, 72, 73] Inclusion of tongue pressure measurement in a comprehensive screening tool may help to improve predictive capabilities.

We believe our results have implications for practicing clinicians, and serve as a call to action for development of an easy‐to‐perform, accurate tool for dysphagia screening. Future prospective studies should focus on practical tools that can be deployed at the bedside, and correlate the results with not only gold‐standard VFSS and FEES, but with clinical outcomes such as pneumonia and aspiration events leading to prolonged length of stay.

There were several limitations to this review. High levels of heterogeneity were reported in the screening tests present in the literature, precluding meaningful meta‐analysis. In addition, the majority of studies included were in poststroke adults, which limits the generalizability of results.

In conclusion, no screening protocol has been shown to provide adequate predictive value for presence of aspiration. Several individual exam maneuvers demonstrate high sensitivity; however, the most effective combination of screening protocol components is unknown. There is a need for future research focused on the development of a comprehensive screening tool that can be applied across patient populations for accurate detection of dysphagia as well as prediction of other adverse health outcomes, including pneumonia.

Acknowledgements

The authors thank Drs. Byun‐Mo Oh and Catrionia Steele for providing additional information in response to requests for unpublished information.

Disclosures: Nasia Safdar MD, is supported by a National Institutes of Health R03 GEMSSTAR award and a VA MERIT award. The authors report no conflicts of interest.

Dysphagia is a serious medical condition that can lead to aspiration pneumonia, malnutrition, and dehydration.[1] Dysphagia is the result of a variety of medical etiologies, including stroke, traumatic brain injury, progressive neurologic conditions, head and neck cancers, and general deconditioning. Prevalence estimates for dysphagia vary depending upon the etiology and patient age, but estimates as high as 38% for lifetime prevalence have been reported in those over age 65 years.[2]

To avoid adverse health outcomes, early detection of dysphagia is essential. In hospitalized patients, early detection has been associated with reduced risk of pneumonia, decreased length of hospital stay, and improved cost‐effectiveness resulting from a reduction in hospital days due to fewer cases of aspiration pneumonia.[3, 4, 5] Stroke guidelines in the United States recommend screening for dysphagia for all patients admitted with stroke.[6] Consequently, the majority of screening procedures have been designed for and tested in this population.[7, 8, 9, 10]

The videofluoroscopic swallow study (VFSS) is a commonly accepted, reference standard, instrumental evaluation technique for dysphagia, as it provides the most comprehensive information regarding anatomic and physiologic function for swallowing diagnosis and treatment. Flexible endoscopic evaluation of swallowing (FEES) is also available, as are several less commonly used techniques (scintigraphy, manometry, and ultrasound). Due to availability, patient compliance, and expertise needed, it is not possible to perform instrumental examination on every patient with suspected dysphagia. Therefore, a number of minimally invasive bedside screening procedures for dysphagia have been developed.

The value of any diagnostic screening test centers on performance characteristics, which under ideal circumstances include a positive result for all those who have dysphagia (sensitivity) and negative result for all those who do not have dysphagia (specificity). Such an ideal screening procedure would reduce unnecessary referrals and testing, thus resulting in cost savings, more effective utilization of speech‐language pathology consultation services, and less unnecessary radiation exposure. In addition, an effective screen would detect all those at risk for aspiration pneumonia in need of intervention. However, most available bedside screening tools are lacking in some or all of these desirable attributes.[11, 12] We undertook a systematic review and meta‐analysis of bedside procedures to screen for dysphagia.

METHODS

Data Sources and Searches

We conducted a comprehensive search of 7 databases, including MEDLINE, Embase, and Scopus, from each database's earliest inception through June 9, 2014 for English‐language articles and abstracts. The search strategy was designed and conducted by an experienced librarian with input from 1 researcher (J.C.O.). Controlled vocabulary supplemented with keywords was used to search for comparative studies of bedside screening tests for predicting dysphagia (see Supporting Information, Appendix 1, in the online version of this article for the full strategy).

All abstracts were screened, and potentially relevant articles were identified for full‐text review. Those references were manually inspected to identify all relevant studies.

Study Selection

A study was eligible for inclusion if it tested a diagnostic swallow study of any variety against an acceptable reference standard (VFSS or flexible endoscopic evaluation of swallowing with sensory testing [FEEST]).

Data Extraction and Quality Assessment

The primary outcome of the study was aspiration, as predicted by a bedside exam, compared to gold‐standard visualization of aspirated material entering below the vocal cords. From each study, data were abstracted based on the type of diagnostic method and reference standard study population and inclusion/exclusion characteristics, design, and prediction of aspiration. Prediction of aspiration was compared against the reference standard to yield true positives, true negatives, false positives, and false negatives. Additional potential confounding variables were abstracted using a standard form based on the Preferred Reporting Items for Systematic Reviews and Meta‐Analysis[13] (see Supporting Information, Appendix 2, in the online version of this article for the full abstraction template).

Data Synthesis and Analysis

Sensitivity and specificity for each test that identified the presence of dysphagia was calculated for each study. These were used to generate positive and negative likelihood ratios (LRs), which were plotted on a likelihood matrix, a graphic depiction of the logarithm of the +LR on the ordinate versus the logarithm of the LR on the abscissa, dividing the graphic into quadrants such that the right upper quadrant is tests that can be used for confirmation, right lower quadrant neither confirmation nor exclusion, left lower quadrant exclusion only, and left upper quadrant an ideal test with both exclusionary and confirmatory properties.[14] A good screening test would thus be on the left half of the graphic to effectively rule out dysphagia, and the ideal test with both good sensitivity and specificity would be found in the left upper quadrant. Graphics were constructed using the Stata MIDAS package (Stata Corp., College Station, TX).[15]

RESULTS

We identified 891 distinct articles. Of these, 749 were excluded based on abstract review. After reviewing the remaining 142 full‐text articles, 48 articles were determined to meet inclusion criteria, which included 10,437 observations across 7414 patients (Figure 1). We initially intended to conduct a meta‐analysis on each type, but heterogeneity in design and statistical heterogeneity in aggregate measures precluded pooling of results.

Figure 1
Preferred Reporting Items for Systematic Reviews and Meta‐Analysis flow diagram. Abbreviations: FEEST, flexible endoscopic evaluation of swallowing with sensory testing; VFSS, videofluoroscopic swallow study.

Characteristics of Included Studies

Of the 48 included studies, the majority (n=42) were prospective observational studies,[7, 8, 14, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49, 50, 51, 52, 53] whereas 2 were randomized trials,[9, 54] 2 studies were double‐blind observational,[9, 16] 1 was a case‐control design,[55] and 1 was a retrospective case series.[56] The majority of studies were exclusively inpatient,[7, 8, 9, 14, 17, 18, 19, 21, 22, 24, 25, 26, 31, 32, 33, 35, 36, 38, 41, 43, 44, 45, 46, 47, 49, 51, 52, 53, 55, 57] with 5 in mixed in and outpatient populations,[20, 27, 40, 55, 58] 2 in outpatient populations,[23, 41] and the remainder not reporting the setting from which they drew their study populations.

The indications for swallow evaluations fit broadly into 4 categories: stroke,[7, 8, 9, 14, 21, 22, 24, 25, 26, 31, 33, 34, 35, 38, 40, 41, 42, 43, 45, 48, 52, 56, 58] other neurologic disorders,[17, 18, 23, 28, 39, 47] all causes,[16, 20, 27, 29, 30, 36, 37, 44, 46, 49, 51, 52, 53, 54, 58] and postsurgical.[19, 32, 34] Most used VFSS as a reference standard,[7, 8, 9, 14, 16, 17, 18, 19, 21, 22, 23, 25, 26, 27, 28, 29, 30, 34, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 50, 51, 52, 53, 54, 56, 57, 58] with 8 using FEEST,[20, 24, 31, 32, 33, 35, 49, 55] and 1 accepting either videofluoroscopic evaluation of swallow or FEEST.[48]

Studies were placed into 1 or more of the following 4 categories: subjective bedside examination,[8, 9, 18, 19, 31, 34, 48] questionnaire‐based tools,[17, 23, 46, 53] protocolized multi‐item evaluations,[20, 21, 22, 25, 30, 33, 34, 37, 39, 44, 45, 52, 53, 57, 58] and single‐item exam maneuvers, symptoms, or signs.[7, 9, 14, 16, 24, 26, 27, 28, 29, 30, 31, 32, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 47, 48, 49, 50, 51, 56, 58, 59] The characteristics of all studies are detailed in Table 1.

Characteristics of Included Studies
Study Location Design Mean Age (SD) Reason(s) for Dysphagia Indx Test Description Reference Standard Sample Size, No. of Patients Sample Size, No. of Observations

  • NOTE: Abbreviations: BSA, bedside assessment; EAT‐10, Eating Assessment Tool; FEES, flexible endoscopic evaluation of swallowing; FEEST, flexible endoscopic evaluation of swallowing with sensory testing; NR, not reported; SD, standard deviation; VFSS, videofluoroscopic swallow study; WST, Water swallow test. *SD not available. Median provided instead of mean.

Splaingard et al., 198844 Milwaukee, WI, USA Prospective observational study NR Multiple Clinical bedside swallow exam Combination of scored comprehensive physical exam, history, and observed swallow. VFSS 107 107
DePippo et al., 199243 White Plains, NY, USA Prospective observational study 71 (10) Stroke WST Observation of swallow. VFSS 44
Horner et al., 199356 Durham, NC, USA Retrospective case series 64* Stroke Clinical bedside swallow evaluation VFSS 38 114
Kidd et al., 199342 Belfast, UK Prospective observational study 72 (10) Stroke Bedside 50‐mL swallow evaluation Patient swallows 50 mL of water in 5‐mL aliquots, with therapist assessing for choking, coughing, or change in vocal quality after each swallow. VFSS 60 240
Collins and Bakheit, 199741 Southampton, UK Prospective observational study 65* Stroke Desaturation Desaturation of at least 2% during videofluoroscopic study. VFSS 54 54
Daniels et al., 199740 New Orleans, LA, USA Prospective observational study 66 (11) Stroke Clinical bedside examination 6 individual bedside assessments (dysphonia, dysphagia, cough before/after swallow, gag reflex and voice change) examined as predictors for aspiration risk. VFSS 59 354
Mari et al., 199739 Ancona, Italy Prospective observational study 60 (16) Mixed neurologic diseases Combined history and exam Assessed symptoms of dysphagia, cough, and 3‐oz water swallow. VFSS 93 372
Daniels et al., 19987 New Orleans, LA, USA Prospective observational study 66 (11) Stroke Clinical bedside swallow evaluation Describes sensitivity and specificity of several component physical exam maneuvers comprising the bedside exam. VFSS 55 330
Smithard et al., 19988 Ashford, UK Prospective observational study 79* Stroke Clinical bedside swallow evaluation Not described. VFSS 83 249
Addington et al., 199938 Kansas City, MO, USA Prospective observational study 80* Stroke NR Reflex cough. VFSS 40 40
Logemann et al., 199937 Evanston, IL, USA Prospective observational study 65 Multiple Northwestern Dysphagia Check Sheet 28‐item screening procedure including history, observed swallow, and physical exam. VFSS 200 1400
Smith et al., 20009 Manchester, UK Double blind observational 69 Stroke Clinical bedside swallow evaluation, pulse oximetry evaluation After eating/drinking, patient is evaluated for signs of aspiration including coughing, choking, or "wet voice." Procedure is repeated with several consistencies. Also evaluated if patient desaturates by at least 2% during evaluation. VFSS 53 53
Warms et al., 200036 Melbourne, Australia Prospective observational study 67 Multiple Wet voice Voice was recorded and analyzed with Sony digital audio tape during videofluoroscopy. VFSS 23 708
Lim et al., 200135 Singapore, Singapore Prospective observational study NR Stroke Water swallow test, desaturation during swallow 50‐mL swallow done in 5‐mL aliquots with assessment of phonation/choking afterward; desaturation >2% during swallow, FEEST 50 100
McCullough et al., 200134 Nashville, TN, USA Prospective observational study 60 (10) Stroke Clinical bedside swallow evaluation 15‐item physical exam with observed swallow. VFSS 2040 60
Rosen et al., 2001[74] Newark, NJ, USA Prospective observational study 60 Head and Neck cancer Wet voice Observation of swallow. VFSS 26 26
Leder and Espinosa, 200233 New Haven, CT, USA Prospective observational study 70* Stroke Clinical exam Checklist evaluation of cough and voice change after swallow, volitional cough, dysphonia, dysarthria, and abnormal gag. FEEST 49 49
Belafsky et al., 200332 San Francisco, CA, USA Prospective observational study 65 (11) Post‐tracheostomy patients Modified Evans Blue Dye Test 3 boluses of dye‐impregnated ice are given to patient. Tracheal secretions are suctioned, and evaluated for the presence of dye. FEES 30 30
Chong et al., 200331 Jalan Tan Tock Seng, Singapore Prospective observational study 75 (7) Stroke Water swallow test, desaturation during, clinical exam Subjective exam, drinking 50 mL of water in 10‐mL aliquots, and evaluating for desaturation >2% during FEES. FEEST 50 150
Tohara et al., 200330 Tokyo, Japan Prospective observational study 63 (17) Multiple Food/water swallow tests, and a combination of the 2 Protocolized observation of sequential food and water swallows with scored outcomes. VFSS 63 63
Rosenbek et al., 200414 Gainesville, FL, USA Prospective observational study 68* Stroke Clinical bedside swallow evaluation Describes 5 parameters of voice quality and 15 physical examination maneuvers used. VFSS 60 1200
Ryu et al., 200429 Seoul, South Korea Prospective observational study 64 (14) Multiple Voice analysis parameters Analysis of the/a/vowel sound with Visi‐Pitch II 3300. VFSS 93 372
Shaw et al., 200428 Sheffield, UK Prospective observational study 71 Neurologic disease Bronchial auscultation Auscultation over the right main bronchus during trial feeding to listen for sounds of aspiration. VFSS 105 105
Wu et al., 200427 Taipei, Taiwan Prospective observational study 72 (11) Multiple 100‐mL swallow test Patient lifts a glass of 100 mL of water and drinks as quickly as possible, and is assessed for signs of choking, coughing, or wet voice, and is timed for speed of drinking. VFSS 54 54
Nishiwaki et al., 200526 Shizuoaka, Japan Prospective observational study 70* Stroke Clinical bedside swallow evaluation Describes sensitivity and specificity of several component physical exam maneuvers comprising the bedside exam. VFSS 31 248
Wang et al., 200554 Taipei, Taiwan Prospective double‐blind study 41* Multiple Desaturation Desaturation of at least 2% during videofluoroscopic study. VFSS 60 60
Ramsey et al., 200625 Kent, UK Prospective observational study 71 (10) Stroke BSA Assessment of lip seal, tongue movement, voice quality, cough, and observed 5‐mL swallow. VFSS 54 54
Trapl et al., 200724 Krems, Austria Prospective observational study 76 (2) Stroke Gugging Swallow Screen Progressive observed swallow trials with saliva, then with 350 mL liquid, then dry bread. FEEST 49 49
Suiter and Leder, 200849 Several centers across the USA Prospective observational study 68.3 Multiple 3‐oz water swallow test Observation of swallow. FEEST 3000 3000
Wagasugi et al., 200850 Tokyo, Japan Prospective observational study NR Multiple Cough test Acoustic analysis of cough. VFSS 204 204
Baylow et al., 200945 New York, NY, USA Prospective observational study NR Stroke Northwestern Dysphagia Check Sheet 28‐item screening procedure including history, observed swallow, and physical exam. VFSS 15 30
Cox et al., 200923 Leiden, the Netherlands Prospective observational study 68 (8) Inclusion body myositis Dysphagia questionnaire Questionnaire assessing symptoms of dysphagia. VFSS 57 57
Kagaya et al., 201051 Tokyo, Japan Prospective observational study NR Multiple Simple Swallow Provocation Test Injection of 1‐2 mL of water through nasal tube directed at the suprapharynx. VFSS 46 46
Martino et al., 200957 Toronto, Canada Randomized trial 69 (14) Stroke Toronto Bedside Swallow Screening Test 4‐item physical assessment including Kidd water swallow test, pharyngeal sensation, tongue movement, and dysphonia (before and after water swallow). VFSS 59 59
Santamato et al., 200955 Bari, Italy Case control NR Multiple Acoustic analysis, postswallow apnea Acoustic analysis of cough. VFSS 15 15
Smith Hammond et al., 200948 Durham, NC, USA Prospective observational study 67.7 (1.2) Multiple Cough, expiratory phase peak flow Acoustic analysis of cough. VFSS or FEES 96 288
Leigh et al., 201022 Seoul, South Korea Prospective observational study NR Stroke Clinical bedside swallow evaluation Not described. VFSS 167 167
Pitts et al., 201047 Gainesville, FL, USA Prospective observational study NR Parkinson Cough compression phase duration Acoustic analysis of cough. VFSS 58 232
Cohen and Manor, 201146 Tel Aviv, Israel Prospective observational Study NR Multiple Swallow Disturbance Questionnaire 15‐item questionnaire. FEES 100 100
Edmiaston et al., 201121 St. Louis, MO, USA Prospective observational study 63* Stroke SWALLOW‐3D Acute Stroke Dysphagia Screen 5‐item screen including mental status; asymmetry or weakness of face, tongue, or palate; and subjective signs of aspiration when drinking 3 oz water. VFSS 225 225
Mandysova et al., 201120 Pardubice, Czech Republic Prospective observational study 69 (13) Multiple Brief Bedside Dysphagia Screening Test 8‐item physician exam including ability to clench teeth; symmetry/strength of tongue, facial, and shoulder muscles; dysarthria; and choking, coughing, or dripping of food after taking thick liquid. FEES 87 87
Steele et al., 201158 Toronto, Canada Double blind observational 67 Stroke 4‐item bedside exam Tongue lateralization, cough, throat clear, and voice quality. VFSS 400 40
Yamamoto et al., 201117 Kodaira, Japan Prospective observational study 67 (9) Parkinson's Disease Swallowing Disturbance Questionnaire 15‐item questionnaire. VFSS 61 61
Bhama et al., 201219 Pittsburgh, PA, USA Prospective observational study 57 (14) Post‐lung transplant Clinical bedside swallow evaluation Not described. VFSS 128 128
Shem et al., 201218 San Jose, CA, USA Prospective observational study 42 (17) Spinal cord injuries resulting in tetraplegia Clinical bedside swallow evaluation After eating/drinking, patient is evaluated for signs of aspiration including coughing, choking, or "wet voice." Procedure is repeated with several consistencies. VFSS 26 26
Steele et al., 201316 Toronto, Canada Prospective observational study 67 (14) Multiple Dual‐axis accelerometry Computed accelerometry of swallow. VFSS 37 37
Edmiaston et al., 201452 St. Louis, MO, USA Prospective observational study 63 (15) Stroke Barnes Jewish Stroke Dysphagia Screen 5‐item screen including mental status; asymmetry or weakness of face, tongue, or palate; and subjective signs of aspiration when drinking 3 oz water. VFSS 225 225
Rofes et al., 201453 Barcelona, Spain Prospective observational study 74 (12) Mixed EAT‐10 questionnaire and variable viscosity swallow test Symptom‐based questionnaire (EAT‐10) and repeated observations and measurements of swallow with different thickness liquids. VFS 134 134

Subjective Clinical Exam

Seven studies reported the sensitivity and specificity of subjective assessments of nurses and speech‐language pathologists in observing swallowing and predicting aspiration.[8, 9, 18, 19, 31, 34, 48] The overall distribution of studies is summarized in the likelihood matrix in Figure 2. Two studies, Chong et al.[31] and Shem et al.,[18] were on the left side of the matrix, indicating a sensitive rule‐out test. However, both were small studies, and only Chong et al. reported reasonable sensitivity with incorporation bias from knowledge of a desaturation study outcome. Overall, subjective exams did not appear reliable in ruling out dysphagia.

Figure 2
Likelihood matrix for curve for subjective clinical exam. Each point corresponds to a study as follows: 1 = Smithard et al., 1998; 2 = Smith et al., 2000; 3 = McCullough et al., 2001; 4 = Chong et al., 2003; 5 = Smith‐Hammond et al., 2009; 6 = Bhama et al., 2012; 7 = Shem et al., 2012. LUQ = Left upper quadrant, LRP = Positive likelihood ratio, RUQ = Right upper quadrant, LLQ = Left lower quadrant, RLQ = Right lower quadrant, LRN = Negative likelihood ratio.

Questionnaire‐Based Tools

Only 4 studies used questionnaire‐based tools filled out by the patient, asking about subjective assessment of dysphagia symptoms and frequency.[17, 23, 46, 53] Yamamoto et al. reported results of using the swallow dysphagia questionnaire in patients with Parkinson's disease.[17] Rofes et al. looked at the Eating Assessment Tool (EAT‐10) questionnaire among all referred patients and a small population of healthy volunteers.[53] Each was administered the questionnaire before undergoing a videofluoroscopic study. Overall, sensitivity and specificity were 77.8% and 84.6%, respectively. Cox et al. studied a different questionnaire in a group of patients with inclusion body myositis, finding 70% sensitivity and 44% specificity.[23] Cohen and Manor examined the swallow dysphagia questionnaire across several different causes of dysphagia, finding at optimum, the test is 78% specific and 73% sensitive.[46] Rofes et al. had an 86% sensitivity and 68% specificity for the EAT‐10 tool.[53]

Multi‐Item Exam Protocols

Sixteen studies reported multistep protocols for determining a patient's risk for aspiration.[9, 20, 21, 22, 25, 30, 33, 34, 37, 39, 44, 45, 52, 53, 57, 58] Each involved a combination of physical exam maneuvers and history elements, detailed in Table 1. This is shown in the likelihood matrix in Figure 3. Only 2 of these studies were in the left lower quadrant, Edmiaston et al. 201121 and 2014.[52] Both studies were restricted to stroke populations, but found reasonable sensitivity and specificity in identifying dysphagia.

Figure 3
Likelihood matrix of multi‐item protocols. 1 = Splaingard et al., 1988; 2 = Mari et al., 1997; 3 = Logemann et al., 1999; 4 = Smith et al., 2000; 5 = McCullough et al., 2001; 6 = Leder et al., 2002; 7 = Tohara et al., 2003; 8 = Ramsey et al., 2006; 9 = Baylow et al., 2009; 10 = Martino et al., 2009; 11 = Leigh et al., 2010; 12 = Mandysova et al., 2011; 13 = Steele et al., 2011 (speech language pathology assessment); 14 = Edmiaston et al., 2011; 15 = Steele et al. (nurse assessment); 16 = Edmiaston et al., 2014; 17 = Rofes et al., 2014. LUQ = Left upper quadrant, LRP = Positive likelihood ratio, RUQ = Right upper quadrant, LLQ = Left lower quadrant, RLQ = Right lower quadrant, LRN = Negative likelihood ratio.

Individual Exam Maneuvers

Thirty studies reported the diagnostic performance of individual exam maneuvers and signs.[7, 9, 14, 16, 24, 26, 27, 28, 29, 30, 31, 32, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 47, 48, 49, 50, 51, 54, 56, 58] Each is depicted in Figure 4 as a likelihood matrix demonstrating the +LR and LR for individual maneuvers as seen in the figure; most fall into the right lower quadrant, where they are not diagnostically useful tests. Studies in the left lower quadrant demonstrating the ability to exclude aspiration desirable in a screening test were dysphonia in McCullough et al.,[34] dual‐axis accelerometry in Steele et al.,[16] and the water swallow test in DePippo et al.[43] and Suiter and Leder.[49]

Figure 4
Likelihood matrix of individual exam maneuvers. Studies in the LLQ demonstrating the ability to exclude aspiration were 56 = Kidd et al., 1993 (abnormal pharyngeal sensation); 96 = McCullogh et al., 2001 (dysphonia); 54 = Steele et al., 2013 (dual axis accelerometry); 121 = DePippo et al., 1992 (water swallow test); and 118 = Suiter and Leder et al., 2008 (water swallow test). (See Supporting Information, Appendix 3, in the online version of this article for the key to other tests). LUQ = Left upper quadrant, LRP = Positive likelihood ratio, RUQ = Right upper quadrant, LLQ = Left lower quadrant, RLQ = Right lower quadrant, LRN = Negative likelihood ratio.

McCullough et al. found dysphonia to be the most discriminatory sign or symptom assessed, with an area under the curve (AUC) of 0.818. Dysphonia was judged by a sustained/a/and had 100% sensitivity but only 27% specificity. Wet voice within the same study was slightly less informative, with an AUC of 0.77 (sensitivity 50% and specificity 84%).[34]

Kidd et al. verified the diagnosis of stroke, and then assessed several neurologic parameters, including speech, muscle strength, and sensation. Pharyngeal sensation was assessed by touching each side of the pharyngeal wall and asking patients if they felt sensation that differed from each side. Patient report of abnormal sensation during this maneuver was 80% sensitive and 86% specific as a predictor of aspiration on VFSS.[42]

Steele et al. described the technique of dual axis accelerometry, where an accelerometer was placed at the midline of the neck over the cricoid cartilage during VFSS. The movement of the cricoid cartilage was captured for analysis in a computer algorithm to identify abnormal pharyngeal swallow behavior. Sensitivity was 100%, and specificity was 54%. Although the study was small (n=40), this novel method demonstrated good discrimination.[58]

DePippo et al. evaluated a 3‐oz water swallow in stroke patients. This protocol called for patients to drink the bolus of water without interruption, and be observed for 1 minute after for cough or wet‐hoarse voice. Presence of either sign was considered abnormal. Overall, sensitivity was 94% and specificity 30% looking for the presence of either sign.[43] Suiter and Leder used a similar protocol, with sensitivity of 97% and specificity of 49%.[49]

DISCUSSION

Our results show that most bedside swallow examinations lack the sensitivity to be used as a screening test for dysphagia across all patient populations examined. This is unfortunate as the ability to determine which patients require formal speech language pathology consultation or imaging as part of their diagnostic evaluation early in the hospital stay would lead to improved allocation of resources, cost reductions, and earlier implementation of effective therapy approaches. Furthermore, although radiation doses received during VFSS are not high when compared with other radiologic exams like computed tomography scans,[60] increasing awareness about the long‐term malignancy risks associated with medical imaging makes it desirable to reduce any test involving ionizing radiation.

There were several categories of screening procedures identified during this review process. Those classified as subjective bedside exams and protocolized multi‐item evaluations were found to have high heterogeneity in their sensitivity and specificity, though a few exam protocols did have a reasonable sensitivity and specificity.[21, 31, 52] The following individual exam maneuvers were found to demonstrate high sensitivity and an ability to exclude aspiration: a test for dysphonia through production of a sustained/a/34 and use of dual‐axis accelerometry.[16] Two other tests, the 3‐oz water swallow test[43] and testing of abnormal pharyngeal sensation,[42] were each found effective in a single study, with conflicting results from other studies.

Our results extend the findings from previous systematic reviews on this subject, most of which focused only on stroke patients.[5, 12, 61, 62] Martino and colleagues[5] conducted a review focused on screening for adults poststroke. From 13 identified articles, it was concluded that evidence to support inclusion or exclusion of screening was poor. Daniels et al. conducted a systematic review of swallowing screening tools specific to patients with acute or chronic stroke.[12] Based on 16 articles, the authors concluded that a combination of swallowing and nonswallowing features may be necessary for development of a valid screening tool. The generalizability of these reviews is limited given that all were conducted in patients poststroke, and therefore results and recommendations may not be generalizable to other patients.

Wilkinson et al.[62] conducted a recent systematic review that focused on screening techniques for inpatients 65 years or older that excluded patients with stroke or Parkinson's disease. The purpose of that review was to examine sensitivity and specificity of bedside screening tests as well as ability to accurately predict pneumonia. The authors concluded that existing evidence is not sufficient to recommend the use of bedside tests in a general older population.[62]

Specific screening tools identified by Martino and colleagues[5] to have good predictive value in detecting aspiration as a diagnostic marker of dysphagia were an abnormal test of pharyngeal sensation[42] and the 50‐mL water swallow test. Daniels et al. identified a water swallow test as an important component of a screen.[7] These results were consistent with those of this review in that the abnormal test of pharyngeal sensation[42] was identified for high levels of sensitivity. However, the 3‐oz water swallow test,[43, 49] rather than the 50‐mL water swallow test,[42] was identified in this review as the version of the water swallow test with the best predictive value in ruling out aspiration. Results of our review identified 2 additional individual items, dual‐axis accelerometry[16] and dysphonia,[34] that may be important to include in a comprehensive screening tool. In the absence of better tools, the 3 oz swallow test, properly executed, seems to be the best currently available tool validated in more than 1 study.

Several studies in the current review included an assessment of oral tongue movement that is not described thoroughly and varies between studies. Tongue movement as an individual item on a screening protocol was not found to yield high sensitivity or specificity. However, tongue movement or range of motion is only 1 aspect of oral tongue function; pressures produced by the tongue reflecting strength also may be important and warrant evaluation. Multiple studies have shown patients with dysphagia resulting from a variety of etiologies to produce lower than normal maximum isometric lingual pressures,[63, 64, 65, 66, 67, 68] or pressures produced when the tongue is pushed as hard as possible against the hard palate. Tongue strengthening protocols that result in higher maximum isometric lingual pressures have been shown to carry over to positive changes in swallow function.[69, 70, 71, 72, 73] Inclusion of tongue pressure measurement in a comprehensive screening tool may help to improve predictive capabilities.

We believe our results have implications for practicing clinicians, and serve as a call to action for development of an easy‐to‐perform, accurate tool for dysphagia screening. Future prospective studies should focus on practical tools that can be deployed at the bedside, and correlate the results with not only gold‐standard VFSS and FEES, but with clinical outcomes such as pneumonia and aspiration events leading to prolonged length of stay.

There were several limitations to this review. High levels of heterogeneity were reported in the screening tests present in the literature, precluding meaningful meta‐analysis. In addition, the majority of studies included were in poststroke adults, which limits the generalizability of results.

In conclusion, no screening protocol has been shown to provide adequate predictive value for presence of aspiration. Several individual exam maneuvers demonstrate high sensitivity; however, the most effective combination of screening protocol components is unknown. There is a need for future research focused on the development of a comprehensive screening tool that can be applied across patient populations for accurate detection of dysphagia as well as prediction of other adverse health outcomes, including pneumonia.

Acknowledgements

The authors thank Drs. Byun‐Mo Oh and Catrionia Steele for providing additional information in response to requests for unpublished information.

Disclosures: Nasia Safdar MD, is supported by a National Institutes of Health R03 GEMSSTAR award and a VA MERIT award. The authors report no conflicts of interest.

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References
  1. Clave P, Rofes L, Carrion S, et al. Pathophysiology, relevance and natural history of oropharyngeal dysphagia among older people. Nestle Nutr Inst Workshop Ser. 2012;72:57–66.
  2. Roy N, Stemple J, Merrill RM, Thomas L. Dysphagia in the elderly: preliminary evidence of prevalence, risk factors, and socioemotional effects. Ann Otol Rhinol Laryngol. 2007;116(11):858–865.
  3. Perry L, Hamilton S, Williams J. Formal dysphagia screening protocols prevent pneumonia. Stroke. 2006;37(3):765.
  4. Odderson IR, Keaton JC, McKenna BS. Swallow management in patients on an acute stroke pathway: quality is cost effective. Arch Phys Med Rehabil. 1995;76(12):1130–1133.
  5. Martino R, Pron G, Diamant N. Screening for oropharyngeal dysphagia in stroke: insufficient evidence for guidelines. Dysphagia. 2000;15(1):19–30.
  6. Jauch EC, Saver JL, Adams HP, et al. Guidelines for the early management of patients with acute ischemic stroke: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2013;44(3):870–947.
  7. Daniels SK, Brailey K, Priestly DH, Herrington LR, Weisberg LA, Foundas AL. Aspiration in patients with acute stroke. Arch Phys Med Rehabil. 1998;79(1):14–19.
  8. Smithard DG, O'Neill PA, Park C, et al. Can bedside assessment reliably exclude aspiration following acute stroke? Age Ageing. 1998;27(2):99–106.
  9. Smith HA, Lee SH, O'Neill PA, Connolly MJ. The combination of bedside swallowing assessment and oxygen saturation monitoring of swallowing in acute stroke: a safe and humane screening tool. Age Ageing. 2000;29(6):495–499.
  10. Edmiaston J, Connor LT, Loehr L, Nassief A. Validation of a dysphagia screening tool in acute stroke patients. Am J Crit Care. 2010;19(4):357–364.
  11. Perry L, Love CP. Screening for dysphagia and aspiration in acute stroke: a systematic review. Dysphagia. 2001;16(1):7–18.
  12. Daniels SK, Anderson JA, Willson PC. Valid items for screening dysphagia risk in patients with stroke: a systematic review. Stroke. 2012;43(3):892–897.
  13. Moher D, Liberati A, Tetzlaff J, Altman DG, Grp P. Preferred Reporting Items for Systematic Reviews and Meta‐Analyses: The PRISMA Statement. Ann Intern Med. 2009;151(4):264–269, W64.
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  22. Leigh JH, Lim JY, Han MK, Bae HJ, Paik NJ. Bedside screening and subacute reassessment of post‐stroke dysphagia: a prospective study. Int J Stroke. 2010;5:200.
  23. Cox FM, Verschuuren JJ, Verbist BM, Niks EH, Wintzen AR, Badrising UA. Detecting dysphagia in inclusion body myositis. J Neurol. 2009;256(12):2009–2013.
  24. Trapl M, Enderle P, Nowotny M, et al. Dysphagia bedside screening for acute‐stroke patients: the Gugging Swallowing Screen. Stroke. 2007;38(11):2948–2952.
  25. Ramsey DJC, Smithard DG, Kalra L. Can pulse oximetry or a bedside swallowing assessment be used to detect aspiration after stroke? Stroke. 2006;37(12):2984–2988.
  26. Nishiwaki K, Tsuji T, Liu M, Hase K, Tanaka N, Fujiwara T. Identification of a simple screening tool for dysphagia in patients with stroke using factor analysis of multiple dysphagia variables. J Rehabil Med. 2005;37(4):247–251.
  27. Wu MC, Chang YC, Wang TG, Lin LC. Evaluating swallowing dysfunction using a 100‐ml water swallowing test. Dysphagia. 2004;19(1):43–47.
  28. Shaw JL, Sharpe S, Dyson SE, et al. Bronchial auscultation: an effective adjunct to speech and language therapy bedside assessment when detecting dysphagia and aspiration? Dysphagia. 2004;19(4):211–218.
  29. Ryu JS, Park SR, Choi KH. Prediction of laryngeal aspiration using voice analysis. Am J Phys Med Rehabil. 2004;83(10):753–757.
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Issue
Journal of Hospital Medicine - 10(4)
Issue
Journal of Hospital Medicine - 10(4)
Page Number
256-265
Page Number
256-265
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Journal of Hospital Medicine
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Journal of Hospital Medicine
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Bedside diagnosis of dysphagia: A systematic review
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Bedside diagnosis of dysphagia: A systematic review
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© 2015 Society of Hospital Medicine
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Nasia Safdar, MD, PhD
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Address for correspondence and reprint requests: Nasia Safdar, MD, University of Wisconsin–Madison, MFCB 5221 Section of Infectious Diseases, 1685 Highland Avenue, Madison, WI 53705; Telephone: 608‐263‐1545; Fax: 608‐263‐4464; E‐mail: ns2@medicine.wisc.edu
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