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Deborah J.C. Ramsey, David G. Smithard and Lalit Kalra Early Assessments of Dysphagia and Aspiration Risk in Acute Stroke Patients Print ISSN: 0039-2499. Online ISSN: 1524-4628 Copyright © 2003 American Heart Association, Inc. All rights reserved. is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231 Stroke doi: 10.1161/01.STR.0000066309.06490.B8 2003;34:1252-1257; originally published online April 3, 2003; Stroke. http://stroke.ahajournals.org/content/34/5/1252 World Wide Web at: The online version of this article, along with updated information and services, is located on the http://stroke.ahajournals.org//subscriptions/ is online at: Stroke Information about subscribing to Subscriptions: http://www.lww.com/reprints Information about reprints can be found online at: Reprints: document. Permissions and Rights Question and Answer process is available in the Request Permissions in the middle column of the Web page under Services. Further information about this Once the online version of the published article for which permission is being requested is located, click can be obtained via RightsLink, a service of the Copyright Clearance Center, not the Editorial Office. Stroke in Requests for permissions to reproduce figures, tables, or portions of articles originally published Permissions: by guest on October 16, 2014 http://stroke.ahajournals.org/ Downloaded from by guest on October 16, 2014 http://stroke.ahajournals.org/ Downloaded from

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Page 1: Early Assessments of Dysphagia and Aspiration Risk in Acute Stroke Patients

Deborah J.C. Ramsey, David G. Smithard and Lalit KalraEarly Assessments of Dysphagia and Aspiration Risk in Acute Stroke Patients

Print ISSN: 0039-2499. Online ISSN: 1524-4628 Copyright © 2003 American Heart Association, Inc. All rights reserved.

is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231Stroke doi: 10.1161/01.STR.0000066309.06490.B8

2003;34:1252-1257; originally published online April 3, 2003;Stroke. 

http://stroke.ahajournals.org/content/34/5/1252World Wide Web at:

The online version of this article, along with updated information and services, is located on the

  http://stroke.ahajournals.org//subscriptions/

is online at: Stroke Information about subscribing to Subscriptions: 

http://www.lww.com/reprints Information about reprints can be found online at: Reprints:

  document. Permissions and Rights Question and Answer process is available in the

Request Permissions in the middle column of the Web page under Services. Further information about thisOnce the online version of the published article for which permission is being requested is located, click

can be obtained via RightsLink, a service of the Copyright Clearance Center, not the Editorial Office.Strokein Requests for permissions to reproduce figures, tables, or portions of articles originally publishedPermissions:

by guest on October 16, 2014http://stroke.ahajournals.org/Downloaded from by guest on October 16, 2014http://stroke.ahajournals.org/Downloaded from

Page 2: Early Assessments of Dysphagia and Aspiration Risk in Acute Stroke Patients

Early Assessments of Dysphagia and Aspiration Risk inAcute Stroke Patients

Deborah J.C. Ramsey, MRCP; David G. Smithard, MD; Lalit Kalra, PhD

Background and Purpose—Dysphagia is common after stroke and is a marker of poor prognosis. Early identification isimportant. This article reviews the merits and limitations of various assessment methods available to clinicians.

Methods—An electronic database search was performed of MEDLINE, EMBASE, and the Cochrane database using suchterms as stroke, aspiration, dysphagia, and assessment; extensive manual searching of articles was also conducted.

Results—Bedside tests are safe, relatively straightforward, and easily repeated but have variable sensitivity (42% to 92%),specificity (59% to 91%), and interrater reliability (��0 to 1.0). They are also poor at detecting silent aspiration.Videofluoroscopy gives anatomic and functional information and allows testing of therapeutic techniques. However,swallowing is assessed under ideal conditions that are different from clinical settings, and reliability is often poor (��0to 0.75) in the absence of assessor training. Fiberoptic endoscopy allows swallow assessment and sensory testing butrequires specialized staff and equipment. Oxygen desaturation during swallowing may be predictive of aspiration(sensitivity, 73% to 87%; specificity, 39% to 87%) but is more useful in combination with bedside testing than inisolation. Other methods of swallow testing are invasive and require specialized staff and equipment.

Conclusions—Although bedside tests remain an important early screening tool for dysphagia and aspiration risk, furtherrefinements are needed to improve their accuracy. (Stroke. 2003;34:1252-1257.)

Key Words: aspiration � deglutition disorders � dysphagia � process assessment (health care) � stroke

Dysphagia after stroke is common, and its detection is animportant part of acute stroke management. The litera-

ture suggests that swallowing difficulties can affect 22% to65% of patients, depending on methods of assessmentused,1–7 and may persist in some patients for many months.8,9

Dysphagia in acute stroke patients is a marker of poorprognosis, increasing the risks of chest infection, malnutri-tion, persistent disability, prolonged hospital stay, institution-alization on discharge, and mortality.1,5–7,9,10

In some patients with poorly coordinated swallowing,material subsequently enters the airway below the level of thevocal cords (aspiration), making oral feeding a significantrisk. In some patients, aspiration causes no outward signs ofdistress. This is called silent aspiration,2–4,10,11 the long-termsignificance of which is unclear.4,10 The aim of this study wasto identify the methods of swallow assessment available andto consider their relative merits and limitations, particularlywith reference to management of acute stroke patients. Anelectronic database search was performed of MEDLINE,EMBASE, and the Cochrane Library using terms includingdysphagia, aspiration, assessment methods, and stroke. Theresultant information was supplemented by extensive manualsearching of references.

Assessment of SwallowingThe most frequently used swallow test is the bedside swallowassessment, which covers a number of techniques used in award environment. For further assessment, videofluoroscopy(VF) is usually the next investigation of choice although othermethods have been used.

Bedside Assessment of SwallowSeveral forms of bedside swallow assessment are used toevaluate patients with an acute or recent cerebrovascularevent. Some studies have involved patients with other neu-rological impairments, but the most common subgroup re-mains stroke disease.

Linden and Siebens12 looked for clinical factors correlatingwith aspiration on VF. They performed a sensorimotorexamination, observed swallowing and related movements,and found a high incidence of impaired pharyngeal gag anddysphonia in patients exhibiting laryngeal penetration.Splaingard et al13 monitored swallowing of various volumesand consistencies of food while watching for respiratorydistress and compared the results with VF findings.

Horner and colleagues11,14 used similar methods in a smallsample of patients and found that a weak cough and dyspho-nia correlated with aspiration on VF.11 Regression analysis on

Received October 9, 2002; final revision received November 21, 2002; accepted November 25, 2002.From the Department of Stroke Medicine, Guy’s King’s & St. Thomas’ School of Medicine, King’s College, London (D.J.C.R., L.K.), and Health Care

of Older People Department, William Harvey Hospital, Ashford, Kent (D.J.C.R., D.G.S.), UK.Correspondence to Dr D.J.C. Ramsey, Department of Stroke Medicine, GKT Medical School, Bessemer Rd, London, SE5 9PJ UK. E-mail

[email protected]© 2003 American Heart Association, Inc.

Stroke is available at http://www.strokeaha.org DOI: 10.1161/01.STR.0000066309.06490.B8

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a larger sample showed that abnormal voluntary cough andabsent gag were independently associated with aspiration.14

Stanners et al15 also studied voluntary cough, gag reflex, anddysphonia but found an association only between weakvoluntary cough and aspiration. These studies are limited bysmall patient numbers, variable times between stroke onsetand assessment, and limited statistical analyses.

DePippo et al16 compared a 3-oz water swallow test withVF, showing that patients who coughed during or afterswallowing or developed a wet or hoarse voice were at risk ofaspiration. They proposed the Burke Dysphagia ScreeningTest,17 which also considered features such as stroke site anddifficulty with meals. Timed tests of swallow capacity havenoted the time and number of swallows required to swallow150 mL water and have shown that delayed swallowing,coughing, or dysphonia indicated swallowing problems.7

Linden et al18 used a clinical “Dysarthria/Dysphagia Bat-tery”—a clinical battery of questions about respiration, anat-omy, drooling, and parenteral feeding. Factors predictive ofsubglottic penetration on VF included recumbent posture,abnormal phonation, abnormal laryngeal elevation, abnormalpalatal gag, wet spontaneous cough, and impaired swallowingof secretions, although these predicted only two thirds ofcases of subglottic penetration in a discriminant analysis.

Daniels and colleagues19 performed an oropharyngeal ex-amination and a clinical swallowing assessment using differ-ent volumes of water while monitoring laryngeal elevation,voice quality, and coughing. The presence of �2 of 6 features(dysphonia, dysarthria, abnormal volitional cough, coughafter swallow, abnormal gag reflex, and voice change afterswallow) predicted greater dysphagia severity on VF. Logis-tic regression identified abnormal volitional cough and coughwith swallow as independent predictors of aspiration.3

McCullough et al20 used a similar assessment and found 2reliable items for detection of aspiration: cough duringswallowing and clinical estimate of the presence ofaspiration.

Many researchers have assessed difficulty in drinkingsmall volumes of water.1,6,21 Smithard and colleagues4 used5-mL aliquots and then a larger volume (60 mL), looking fordribbling, laryngeal movement, cough, dysphonia, and thetime taken to finish the drink. Logistic regression identifiedimpaired consciousness level and weak voluntary cough asindependent predictors for aspiration.

Addington et al22 used a reflex cough test that evaluated thelaryngeal cough reflex with nebulized tartaric acid; a weak orabsent cough was regarded as predictive of aspiration risk.Teramoto and Fukuchi23 studied patients with aspirationpneumonia and a nonrecent stroke. They developed a 2-stepswallowing provocation test that involved injecting boluses(0.4 and 2 mL) of water into the suprapharynx of a supinepatient and noting the latent time for swallowing. The testidentified patients with aspiration pneumonia, but samplesizes were small.

Gag Reflex and Laryngopharyngeal SensationAn absent gag reflex has been suggested as predictive ofaspiration in some studies3,12,14,18 but refuted in others.4,11,15,20

Acute and nonacute stroke patients were studied, as werepatients dysphagic from other causes, and sample sizes variedconsiderably. Davies and colleagues24 have demonstrated thatup to 30% of healthy younger adults and 44% of healthy olderadults may have unilateral or bilateral absent gag reflexes.

Absent pharyngeal sensation appears rare in normal sub-jects,24 and Kidd et al2 found abnormal pharyngeal sensation(tested with an orange stick) in all stroke patients aspiratingon VF. However, sensation was also abnormal in 40% ofthose not aspirating, and normal swallowing can occur withcomplete local anesthesia.25 Aviv and colleagues26 havedeveloped a method of testing laryngopharyngeal sensationby stimulating the mucosa endoscopically with air pulses anddetermining sensory discrimination thresholds. Most dys-phagic patients tested (predominantly stroke or chronic neu-rological disease) had sensory deficits, and aspiration orpenetration was more common in those with severe deficits.Sensory deficits were also demonstrated in acute strokepatients without clinical dysphagia,27 and it has been sug-gested that silent sensory deficits may predispose to silentaspiration.

Validity, Sensitivity, Specificity, and ReliabilityThe validity for most swallow tests has been determined bycomparison with VF. Detection of aspiration by bedsidetesting has been variable (Table 1), with sensitivities between42% and 92% and specificities between 59% and91%.4,13,16,19,28 Positive predictive values for bedside swallowtesting range from 50% to 75%; negative predictive valuesrange from 70% to 90%.4,13,28

Interobserver and intraobserver reliability levels for clini-cal examination vary considerably between studies, with

TABLE 1. Sensitivity, Specificity, and Predictive Values for Bedside SwallowTests Compared With VF

ResearchersPatients

Studied, nSensitivity,

%Specificity,

%

PositivePredictiveValue, %

NegativePredictiveValue, %

Smithard et al4 83 47 86 50 85

DePippo et al16 44 76 59

Smith et al28 53 80 68 50 90

Splaingard et al13 107 42 91 75 70

(87 strokes)

Daniels et al19 59 92 67

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values of ��0 to 1.0 quoted.4,29–31 Mann et al29 calculatedvalues of ��0.82�0.09 and 0.75�0.09 for interobserveragreement on diagnosis of dysphagia or aspiration, respec-tively, by 2 speech pathologists. The study by Smithard et al4

found better agreement between assessments by speech ther-apists (��0.79; 95% CI, 0.55 to 1.0) than between doctors(��0.5; 95% CI, 0.26 to 0.73). Values for agreement betweena doctor and a therapist ranged from only ��0.24 to 0.42.

Ellul and Barer30 looked at interobserver reliability for abedside swallow test performed predominantly by nursingstaff and found more variable values (��0.19 to 1.0).McCullough et al31 studied reliability between speech pathol-ogists performing a clinical swallow examination and againfound wide-ranging values, from ��0 to 1.0 for both inter-judge and intrajudge reliability for the measures studied.

VideofluoroscopyVF (or modified barium swallow) is often regarded as theassessment of choice in testing swallowing ability.32 Thepatient stands or sits at 45° to 90° and consumes foods orliquids of different consistencies impregnated with bariumwhile their swallow is imaged in lateral and anteroposteriorprojections. VF provides a dynamic study in which thetherapist or radiologist can examine the anatomic structuresand the function of the oral and pharyngeal phases ofswallowing, as well as testing potential compensatorytechniques.

Although VF has been proposed as the gold standard forswallow testing,11,32 this view is not accepted universally. Itcannot be undertaken in patients unable to sit upright withoutthe use of a specialized chair, which does not replicatephysiological conditions. VF protocols vary, with someworkers using a standardized protocol for all patients andothers performing more functional, tailor-made studies.32 Theradiation exposure for VF, although regarded as acceptable,32

makes frequent test repetition inappropriate. The limitedprocedure duration underestimates the time required for somepatients to eat and makes patient fatigue less obvious.Test-test variability has been found within normal subjectsundergoing VF33; the differences were nonsignificant, butrepeated trials of each food consistency are advised.

VF is a relatively complex task to interpret, and interjudgeagreement can be very variable. Smithard et al4 calculatedpercentage agreement between 2 radiologists for VF assess-ments as 76% (��0.48; 95% CI, 0.2 to 0.76), whereasWilcox and colleagues34 found only limited agreement on VFfeatures among 10 speech and language pathologists, possiblyreflecting their variable experience. Mann et al29 looked atagreement between a speech pathologist and a radiologist andobtained statistics of ��0.75�0.09 for VF diagnosis ofdysphagia and ��0.41�0.09 for aspiration.

McCullough et al35 examined common VF measures andfound that statistics for interjudge reliability ranged from��0 to 0.478; percentage agreement (calculated when � wasnot possible) reached 92% on some variables. Intrajudgereliability has been greater in some studies but not inothers.35,36 Reliability ratios in 1 study were highest foraspiration, particularly for solids, and lowest for functionalswallowing components.36 Levels of agreement in ratings

correlate with assessor experience37 and improve with groupdiscussion among assessors38; similar methods of training tocriteria may form a way to improve reliability.35

Pulse OximetryPulse oximetry provides a noninvasive method of bedsideswallow testing. Most studies have found a good correlationbetween oxygen saturations and arterial blood samples inhigher saturation ranges, with correlation coefficients quotedat 0.82 to 0.99.39 The manufacturer’s accuracy for themonitors is �2% within the 50% to 100% saturation range. Ithas been suggested that aspiration causes reflex bronchocon-striction and therefore ventilation-perfusion imbalance, lead-ing to hypoxia and desaturation.40 Others have suggested thatabnormal swallowing leads to poor breathing and ventilation-perfusion mismatching because of reduced inspiratoryvolumes.41

Initial reports of hypoxemia during oral feeding in neuro-logically disabled individuals noted associations with certainfood textures, postulated to be secondary to aspiration ofthose foods.42,43 Zaidi et al40 subsequently found greaterdesaturation after swallowing water in acute stroke patientsthan in matched control subjects, and the degree of desatu-ration correlated with clinical assessment of aspiration risk,although statistical criticisms have been leveled at theiranalyses.44 Sherman et al45 performed pulse oximetry duringVF and demonstrated significant desaturation in patients whosuffered aspiration of material or penetration without clearingcompared with those in whom penetration occurred withclearing or not at all, but patient numbers were small and agewas very variable. Some studies have found no clear rela-tionship between desaturation and aspiration,44,46 but 1 studydemonstrated persistently lower saturations in aspirators thannonaspirators.44

Other workers have found that desaturation of �2% frombaseline predicted aspiration on VF.28,47 Sensitivity valuesranged from 73% to 87%, and specificity values ranged from39% to 87% (Table 2) with poor positive predictive valuesand possibly lower values in older subjects and those withlung disease.47 Using an end point of penetration or aspirationrather than aspiration alone gave higher specificity andpositive predictive values.28 Another study compared oxygensaturation predictions with aspiration detected by fiberopticendoscopy rather than VF and obtained better specificitiesand predictive values.48 Two studies combined predictionsfrom bedside testing and saturation monitoring and achievedgood sensitivity and specificity values, particularly withaspiration or penetration as end points.28,48

Fiberoptic EndoscopyFiberoptic endoscopic evaluation of swallowing (FEES) cangive information on anatomy, the swallow process, pharyn-geal motility, and sensory deficits.26,49 Although aspirationcannot be seen directly, it can be inferred from residue leftafter swallowing or ejection of material out of the tracheaafter coughing.

On comparison with VF in a small sample of dysphagicpatients, FEES gave sensitivity values of �0.88 for 3 of 4parameters49: specificity ranged from 0.50 to 0.92, positive

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predictive values were 0.69 to 0.88, and negative predictivevalues ranged from 0.63 to 1.00. One study found feweraspiration pneumonias after a negative FEES result than anegative VF result although this was not statistically signif-icant.50 The assessment can be conducted at bedside, can bevideotaped if required, and is safe and well tolerated.51 It is,however, dependent on a skilled operator and specializedequipment, and limited information is available about the oraland esophageal stages.

Other MethodsCervical auscultation of the mechanical and/or respiratorycomponents of swallowing, combined with bedside testing,has been compared with VF52 and revealed significant agree-ment for detection of aspiration. It can be performed atbedside, but research into sound patterns is ongoing andtechnique reliability is unclear.

Lateral cervical soft tissue radiographs have been usedafter swallowing contrast,53 but poor head posture causesproblems, and reporting is difficult for the inexperienced.Ultrasonography is safe and moderately portable, but mostultrasound probes are too small to visualize the wholeswallow54 and are limited to nonbony areas.

Pharyngeal or esophageal manometry can provide usefulinformation, particularly when combined with VF,55 andother methods tried include scintigraphy56 and electromyo-graphy.57 These techniques cannot be used at bedside, areinvasive, and require specialized staff and equipment, so theyhave principally remained research tools.

ConclusionsDysphagia is common in acute stroke patients, but swallowrecovers in �80% of patients within 2 to 4 weeks of strokeonset.1,8 The most important consideration initially is aspira-tion risk and suitability for oral feeding. Although a detailedexamination of swallowing mechanisms may be desirable, itis usually difficult and often unnecessary to subject patientsto such procedures, which may have greater relevance inpatients with persistent dysphagia. The challenge is to de-velop simple bedside assessments that can be administered bya range of professionals in day-to-day clinical practice.

A variety of bedside assessments have been proposed thatdepend on the ability to swallow foods of various consisten-

cies. The features most predictive of aspiration risk include awet voice, weak voluntary cough, cough on swallowing,prolonged swallow, or some combination of these. Althoughabnormal gag reflex and reduced laryngopharyngeal sensa-tion are associated with swallowing difficulties, they do notappear to predict aspiration risk in isolation. Bedside swallowtests are safe, therefore repeatable, and relatively straightfor-ward to perform. However, sensitivities and specificities arevery variable, with many methods missing silent aspiration,and assessments of reliability have been wide ranging.

All bedside swallow assessments have limitations, neces-sitating pragmatic dysphagia management that takes availablefacilities and user experience into consideration. In our unit,all acute stroke patients undergo swallow screening bytrained nursing staff. The protocol assesses consciousnesslevel, posture, ability to cooperate with the test, and grossoromotor function. Patients deemed safe are tested with sipsof water while monitoring for coughing or respiratory dis-tress, voice changes, and laryngeal movement. Those withoutobvious difficulties are offered a larger volume of water,yoghurt, and normal foods and again are monitored. Patientswithout problems receive a normal diet while we watch theiroral intake and respiratory status for 48 hours. Patients whofind eating effortful or with significant food residues aregiven a soft, smooth diet and referred to speech and languagetherapy. Any patient failing the test is kept nil by mouth andreferred to a speech and language therapist for a detailedassessment, including VF if appropriate.

VF has advantages over bedside methods, especially inassessing swallow mechanics and testing compensatory tech-niques. However, the information provided is dependent onoperating procedures and the training of assessors to interpretresults. Limitations are imposed by patient cooperation,availability and timing of studies, and the ability to generalizeto clinical settings. The radiation exposure involved makes itan inappropriate test to repeat frequently to monitor changes.The level of supervision and attention to posture during theexamination (rarely possible on general wards) means thatsome patients considered safe on VF may remain at risk ofaspiration in clinical settings.

Pulse oximetry is straightforward and noninvasive, andsignificant desaturation during feeding may correlate withaspiration in dysphagic individuals. Although specificity and

TABLE 2. Sensitivity, Specificity, and Predictive Values for DesaturationCompared With Aspiration on VF or Fiberoptic Endoscopy

ResearchersPatients

Studied, nEndPoint

Sensitivity,%

Specificity,%

PositivePredictiveValue, %

NegativePredictiveValue, %

Collins and Bakheit47 54 Asp 73 87

Smith et al28 53 Asp 87 39 36 88

Asp/Pen 86 54 69 76

Combined with BSA Asp 73 76 55 88

Combined with BSA Asp/Pen 65 96 95 70

Lim et al48* 50 Asp 77 83 83 77

Combined with BSA Asp 100 71 79 100

Asp indicates aspiration; Pen, penetration; and BSA, bedside swallow assessment.*Compared with fiberoptic endoscopic assessment rather than VF.

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predictive values for the technique are relatively poor inisolation, they appear better when used together with bedsideswallow testing. Patients with significant dysphagia may bedetected even if they do not aspirate; predictive values arebetter for aspiration or penetration than aspiration alone.FEES provides useful swallow information and is portableand safe, but specialized staff and equipment are required.

The limitations of the existing bedside tests that form thecornerstone of early assessment of aspiration risk in strokemust stimulate continued efforts to improve the accuracy andrepeatability of swallow assessment methods. More reliablebedside tests would allow swallow screening by a range ofprofessionals who may be in earlier contact with strokepatients than speech and language therapists. This shouldreduce the number of patients who are not fed or are fedinappropriately while awaiting assessment for dysphagia andare therefore at risk of aspiration pneumonia or malnutrition.

AcknowledgmentThe research was funded by Action Research.

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