Comments on Selected Recent Dysphagia Literature

David W. Buchholz, MD and Stefanie Neumann, MA

Explaining Oropharyngeal Dysphagia After Unilat-eral Hemispheric StrokeHamdy S, Aziz Q, Rothwell JC, Crone R, Hughes D,Talalis RC, Thompson DGLancet 350:686–692, 1997

Hamdy et al. note, ‘‘Oropharyngeal dysphagia occurs inup to a third of patients presenting with a unilateralhemiplegic stroke, yet its neurophysiological basis re-mains unknown.’’ They continue, ‘‘Animal data indicatethat stimulation of either cortical hemisphere can initiateswallowing, which suggests that dysphagia after a strokeis due to damage either to both hemispheres or to thebrainstem swallowing centre. However, neuropathologi-cal examination of dysphagic stroke patients either atnecropsy or with magnetic resonance imaging has shownthat, in many cases, the lesion is discrete and unilateral.’’

The authors previously reported on the use oftranscranial magneto-electric stimulation (TCMS) toidentify the corticofugal projections to the muscles ofswallowing [1]. They found ‘‘that oral muscles, such asthe mylohyoids are represented symmetrically betweenthe two hemispheres, whereas muscles of the pharynxand oesophagus are represented very asymmetrically,with most individuals having a dominant swallowinghemisphere, independent of handedness.’’

Based on these earlier findings, Hamdy et al. gen-erated ‘‘two hypotheses to explain why a unilateralhemispheric stroke might cause oropharyngeal dyspha-gia.’’ They state, ‘‘First, innervation of the brainstem byboth hemispheric centres might be required to initiateswallowing, so destruction of either would leave inad-equate cortical function to evoke normal swallowing. . . .Alternatively, since there is functional asymmetry betweenthe two hemispheres for pharyngeal function, oropharyn-geal dysphagia would result from damage to the hemi-sphere where the dominant pharyngeal centre was located.This second hypothesis would also predict that swallowingshould remain normal if the dominant centre for pharyngealfunction was present on the unaffected hemisphere.’’

The authors recruited 20 patients with unilateralhemiplegic stroke within the previous 6 weeks. Patientsunderwent the following evaluations: (1) clinical exami-nation by a speech and language therapist using a stan-dardized bedside assessment, (2) standardized neurologi-cal assessment, (3) submental electromyography (EMG)of mylohyoid muscles, (4) pharyngeal EMG via an in-traluminal catheter positioned with manometric guid-ance, (5) EMG of muscles of the thenar eminence(muscles that have contralateral but symmetrical hemi-spheric representation), and (6) an experimental protocolusing TCMS to determine excitability thresholds andmotor-evoked response amplitudes and latencies.

Eight of the 20 patients had oropharyngeal dys-phagia, and the other 12 patients swallowed normally.Computed tomography of the brain revealed that 4 of thedysphagic patients had right hemisphere infarcts and 4had left hemisphere infarcts. Six of the nondysphagicpatients had right hemisphere infarcts, and 6 had lefthemisphere infarcts.

Hamdy et al. report, ‘‘Our study has shown thatpatients dysphagic after unilateral hemisphere strokehave smaller pharyngeal responses from the unaffectedhemisphere than do non-dysphagic patients, irrespectiveof the side and level (cortical or subcortical) of the le-sion. . . . Onepossible explanation for this difference isthat the smaller responses are a reflection of the asym-metrical motor representation of pharyngeal function onthe cerebral cortex. In other words, with damage to thehemisphere containing the predominant pharyngeal cen-tre, swallowing cannot be maintained by the smaller pha-ryngeal centre in the unaffected hemisphere.’’

The authors continue, ‘‘The similarity in mylo-hyoid responses between dysphagic and non-dysphagicstroke patients is consistent both with our observationthat the dysphagic patients had predominantly pharyn-geal swallowing problems, and the fact that the pharyn-geal phase of swallowing is the most important clinicaldeterminant of aspiration in stroke populations. Further-more, . . . ourfindings suggest that the cortical control of

Dysphagia 13:116–120 (1998)

© Springer-Verlag New York Inc. 1998

mylohyoid motor function is less susceptible than pha-ryngeal motor function to unilateral hemispheric injury.’’

The authors further note, ‘‘Unlike those in theunaffected hemisphere, the amplitudes of the pharyngeal,mylohyoid, and thenar responses to stimulation of theaffected hemisphere were as diminished in the dysphagicas in the non-dysphagic patients, indicating that the mo-tor excitability of the affected hemisphere, at least duringthe acute stages of a stroke, does not discriminate be-tween the presence and absence of dysphagia.’’ Theyadd, ‘‘Both stroke groups had a similar degree of corticaldamage to the region responsible for swallowing motorfunction.’’

Hamdy et al. conclude, ‘‘The results of this studyindicate that after unilateral hemispheric stroke, thosepatients who become dysphagic have smaller pharyngealresponses on the unaffected hemisphere than do thosewho retain normal swallowing. This finding is consistentwith the presence of interhemispheric asymmetry ofswallowing motor function, and suggests that damage tothe hemisphere with dominant swallowing control un-derlies the development of dysphagia.’’

CommentsThis elegant study provides us with our best understand-ing to date of not only why some (but not all) patientswith unilateral hemispheric stroke develop pharyngealdysphagia but also how control of oropharyngeal swal-lowing is distributed in the human cerebral cortex.

Reference

1. Hamdy S, Aziz Q, Rothwell JC, Singh KD, Barlow J, HughesDG, Tallis RC, Thompson DG: The cortical topography of hu-man swallowing musculature in health and disease.Nature Med2:1217–1224, 1996

Does Pulse Oximetry Reliably Detect Aspiration inDysphagic Stroke Patients?Collins MJ, Bakheit AMOStroke 28:1773–1775, 1997

Collins and Bakheit address the common problem ofsilent aspiration after stroke and the limitations of bed-side assessment, videofluorography, and endoscopy indetecting this problem. They note, ‘‘It has been sug-gested that aspiration of food or fluid into the airwayscauses reflex bronchoconstriction that leads to ventila-tion-perfusion mismatch and oxygen desaturation of ar-terial blood, which can be readily measured by pulseoximetry’’ (which is ‘‘noninvasive, simple, and repeat-able, and it does not involve exposure to radiation’’).

The authors studied 54 consecutive inpatients and

outpatients with stroke and ‘‘swallowing difficulties whowere referred to a videofluoroscopy clinic.’’ Using apulse oximeter, they obtained measurements of oxygensaturation in conjunction with simultaneous videofluo-rography in the following: (1) at baseline prior to video-fluorography, (2) during the act of swallowing, (3) dur-ing the 2 min after a test meal, and (4) 10 min aftercompletion of videofluorography. Measurements wererepeated with the patient ingesting thin liquid, pudding,and a barium-impregnated biscuit.

Videofluorography revealed aspiration in 13 menand 9 women. Collins and Bakheit report, ‘‘Seven pa-tients in each group had symptoms of coughing, choking,or spluttering while eating, and 6 men and 2 women hadsilent aspiration.’’ Pulse oximetry data revealed signifi-cantly reduced oxygen saturation 2 min after swallowingin male patients who aspirated. The authors note, ‘‘Whenthe data were analyzed according to age, there was sig-nificantly more desaturation in aspirating male patientsaged <65 years than in their older counterparts.’’ Therewas a similar trend for female aspirators, but it was notstatistically significant. There was no significant desatu-ration in nonaspirators of either sex aged 65 years orolder.

Correlating pulse oximetry and videofluoro-graphic data, Collins and Bakheit state, ‘‘44 patients(81.5%) were accurately predicted [by pulse oximetrydata] as aspirators or non-aspirators (K40.61, p<.001).Interestingly, the prediction rate in male patients <65years of age was 100%, but the rate in females of this agegroup was 67%. The sensitivity and specificity of pulseoximetry were 73% and 87%, respectively.’’

Collins and Bakheit discuss possible reasons forfalse-negative and false-positive oximetry findings in-dicative of aspiration. For various reasons aging, currentcigarette smoking, and chronic lung disease may be con-founding factors. The authors indicate that ‘‘there maybe a time delay between the onset of the hypoxic eventand its detection by pulse oximetry . . . (and) this mayhave resulted in some false-negative oximetry find-ings. . . . Delayed pulse oximetry readings (e.g., 5 min-utes after swallow/aspiration) would have probablygiven a more accurate result.’’ They also note, ‘‘Desatu-ration during meals in the absence of aspiration has beenreported in patients with chronic pulmonary disease [1],and this may also account for some of the false-positiveresults in this study.’’

Collins and Bakheit conclude, ‘‘The presentstudy has demonstrated that pulse oximetry reliably de-tects aspiration in most dysphagic patients and may beused as an adjunct to the bedside assessment of dyspha-gia. However, careful interpretation of the pulse oxime-try data is necessary in older subjects, smokers, and pos-sibly those with chronic lung disease.’’

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CommentsWe take home three messages from this paper. First, ourtraditional focus on bedside assessment, videofluorogra-phy, and endoscopy for detection of aspiration may haveled us to overlook other worthwhile techniques such aspulse oximetry. Second, we are reminded that our un-derstanding of evaluation and treatment of dysphagiacomplications would be enhanced by more input fromthe pulmonary perspective.

The third take-home message from this paper isthat pulmonary complications including not only oxygendesaturation but also chronic cough, laryngospasm, andbronchospasm can ensue from dysphagiawithoutaspira-tion. An excellent review by Cunningham et al. [2] of theneural reflexes involved in these phenomena is highlyrecommended.

References

1. Brown SE, Casciari RJ, Light RW: Arterial oxygen saturationduring meals in patients with severe chronic obstructive pulmo-nary disease.S Med J 76:194–198, 1983

2. Cunningham ET, Ravich WJ, Jones B, Donner MW: Vagal re-flexes referred from the upper aerodigestive tract: an infre-quently recognized cause of common cardiorespiratory reflexes.Ann Intern Med 116:575–582, 1992

Safe Feeding Practices for Infants and Young Chil-drenByard RW, Gallard V, Johnson A, Barbour J, Bonython-Wright B, Bonython-Wright DJ Paediatr Child Health 32:327–329, 1996

Byard et al. observe that ‘‘upper airway obstructioncaused by inhaled foreign material . . . is a particularproblem for infants and young children due to a varietyof predisposing factors.’’ These factors include ‘‘the de-velopment of incisor teeth which erupt 10 months to 2years before the second molars (at 20–30 months).’’They continue, ‘‘Thus for a significant period childrenare able to bite off portions of food without being able tosuccessfully grind the food prior to swallowing. In ad-dition, neural coordination of swallowing is not as pre-cise as in older age groups.’’

The authors reviewed inpatient records of child-hood hospital admissions in South Australia as well asthe existing literature pertaining to choking among chil-dren. They report, ‘‘The most vulnerable age for airwayblockage is between 1 and 3 years with 90% of deathsoccurring before 5 years.’’ Additionally, ‘‘While the pre-sentation of inhaled foreign material is classically of sud-den coughing, gagging or choking, followed by stridor,wheezing and reduced air entry, cases not infrequentlyoccur where there is no history suggestive of inhalation,

resulting in the diagnosis being missed for weeks ormonths.’’

Byard et al. continue, ‘‘Particular foods that haveresulted in death are often rounded in shape, with firm tohard consistencies and diameters less than 32 mm.’’ Spe-cific problem items include nuts, raw carrot sticks, piecesof raw apple, celery sticks, corn chips, grapes, popcorn,sweets, hot dogs and sausages that have not had theirskin removed and/or been cut into small pieces, and gris-tly meats. Of interest is the cultural and geographic vari-ability of offending food items, such that ‘‘watermelonseeds cause the largest number of cases in a study fromDubai,’’ ‘‘fish bones are cited as the most common for-eign bodies in Japan and pumpkin seeds were the mostfrequent inhaled foreign body (25% of all cases) in thestudy from Greece.’’

Aside from types of food, risk factors for fatalchoking include inadequate supervision and distractionswhile eating, and in this regard childcare centers may beespecially risky environments. Byard et al. conclude,‘‘Children should not be fed forcibly, and should be sit-ting quietly under observation while eating.’’ They alsorecommend education of parents and childcare workersregarding not only avoidance of dangerous foods but alsoprovision of a safe eating environment for small children.

(See Comments under ‘‘Choking IncidentsAmong Psychiatric Patients’’)

Choking Incidents among Psychiatric Patients: Ret-rospective Analysis of Thirty-one Cases from theWest Bologna Psychiatric WardsFioritti A, Glaccotto L, Melega VCan J Psychiatry 42:515–520, 1997

Fioritti et al. state, ‘‘Choking while swallowing food ordrinks is a cause of death that has long been known andstudied among the psychiatric population.’’ They reviewthe existing literature, which has implicated risk factorsincluding psychiatric medications, movement disorders,seizures, other concomitant neurologic and medicalproblems, impaired dentition, and bad eating habits.

Fioritti et al. performed a retrospective analysisof all choking incidents among psychiatric patients intwo long-stay wards, one short-stay ward, and one out-patient program. They defined an ‘‘incident’’ as ‘‘anacute episode in which the patient coughed incessantly orexperienced a colour change (with inability to speak orcough effectively) while ingesting food or drink. The solidor liquid food had to be expelled to terminate the event.’’

Eighteen patients suffering a total of 31 incidentswere identified. The authors report, ‘‘As many as 17 outof 18 patients were being treated with at least one neu-

118 D.W. Buchholz and S. Neumann: Recent Dysphagia Literature

roleptic. . . .’’ One-half of the patients were schizo-phrenic, and the others had a variety of psychiatric, neu-rologic, and medical diagnoses.

Fioritti et al. note, ‘‘What we found was thatsome cases could not easily be fitted into one singlecategory; quite often, multiple etiologic factors are dis-cerned. . . .’’ The authors express their suspicion that an-ticholinergic and antidopaminergic medication side ef-fects played a major role in choking incidents. The au-thors also stress the contribution of ‘‘bad eating habits(the so-called fast eating syndrome) . . . which can becorrected by educational and rehabilitative protocols’’[1]. The authors conclude that at least some chokingincidents among psychiatric patients are avoidable bymeasures such as correction of bad eating habits, screen-ing for swallowing problems at admission, and judicioususe of psychiatric medications with the potential to im-pair swallowing [2].

CommentsWe tend to think of swallowing problems as occurring inindividuals with dysphagia related to underlying medicalproblems affecting oral, pharyngeal, and/or esophagealfunction. Yet there are other groups at risk for swallow-ing problems including choking, as the two articles re-viewed above indicate. Even healthy adults choke andsometimes die of choking. It is worth keeping this broadperspective in mind as we deal with swallowing problems.

Reuters News Service recently reported the fol-lowing: TOKYO—Rice cakes, the silent killers of theJapanese New Year’s season, claimed 21 lives on thefirst two days of 1998, the national dailyYomiuri Shim-bun reported. The chewy and sticky rice cakes, called‘‘mochi,’’ are part of traditional New Year’s dishes, butevery year numerous people die when the cakes getlodged in their throats. In Tokyo, eight people died and10 others were rushed to emergency rooms after eatingrice cakes, compared to only four last year. ‘‘This yearhas been a particularly bad year, ’’ a fire official said.

References

1. Rosenstein LD, Price RF: Shaping a normal rate of eating usingaudiotaped pacing in conjunction with a token economy.Neu-ropsychol Rehab 4:387–398, 1994

2. Buchholz DW: Oropharyngeal dysphagia due to iatrogenic neu-rological dysfunction.Dysphagia 10:248–254, 1995

Multiple Esophageal Webs: Treatment and Follow-up of Seven PatientsLongstreth GF, Sitzer MEJ Clin Gastroenterology 24:199–202, 1997

Longstreth and Sitzer describe ‘‘seven patients with mul-tiple esophageal webs without a predisposing disorder’’

and review published reports of 26 similar cases. Theirseven patients had dysphagia for 4–26 years without‘‘skin disease, a history of ingestion of a potentiallycaustic substance, or evidence of gastroesophageal refluxdisease by history or endoscopy.’’ Dilatation relieveddysphagia in all seven patients, but it recurred in everypatient, resulting in repeated dilatation.

It is suggested that the term ‘‘ring’’ be reserved‘‘for a mucosal structure at the gastroesophageal junc-tion’’ and that the term ‘‘web’’ be used ‘‘for all otherringlike structures.’’ Webs have been described in patientsof all ages, but 29 of the 33 reported cases have involvedmales. The typical dysphagia history in patients with mul-tiple esophageal webs is of at least 5 years duration.

Longstreth and Sitzer point out ‘‘the fallibility ofbarium esophagography in the diagnosis of the disor-der.’’ They note, ‘‘Endoscopy is the most accuratemethod of diagnosis, but the webs can be missed if apediatric endoscope is used because resistance might notbe noticed in passing them.’’

The cause of multiple esophageal webs is ob-scure. Gastroesophageal reflux has been considered, butthe authors state, ‘‘Because of the atypical multiplicityand location of the webs for a reflux cause, the lack ofassociated mucosal erosion, the sketchy nature of thereported data relating to reflux, and the limited reportedeffectiveness of antireflux therapy, it seems unlikely tous that they are caused by acid reflux.’’

Instead, the authors conclude, ‘‘We find a con-genital cause to be a more compelling, albeit speculative,explanation. . . . Weconjecture that affected patients areborn with multiple fibrotic esophageal stenoses that pro-duce increasing luminal compromise at a variable ratethroughout life.’’

CommentsThose of us whose interest in dysphagia is predominantlyoral and pharyngeal should always be vigilant for coex-istent esophageal pathology, either structural or func-tional, that may be chronic and unsuspected but none-theless important [1].

Reference

1. Buchholz DW, Marsh BR: Case report: multifactorial dysphagia—looking for a second, treatable cause.Dysphagia 1:88–90, 1986

Dysphagia Induced by Chronic Ingestion of Benzodi-azepineDantas RO, Souza MANAm J Gastroenterol 92:1194–1196, 1997

A 57-year-old woman complained of dysphagia for sol-ids and liquids of 2 weeks duration, resulting in a 10-pound weight loss. She had a background of rheumatoid

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arthritis for which she was taking prednisone 10 mgdaily, and she had also been taking lorazepam (a benzo-diazepine usually prescribed as an anti-anxiety agent) 2mg daily for 2 years.

A radiologic study demonstrated partial retentionof barium in the pharynx, and this was confirmed by ascintigraphic study of oropharyngeal transit (demonstrat-ing retention of about one-half of the bolus). Esophagealmanometry was normal.

The authors report, ‘‘Lorazepam was withdrawn,and 2 weeks later the patient had no symptoms.’’ Shegained 6 pounds. The radiologic and scintigraphic stud-ies were repeated and were normal. After 1-year follow-up the patient remained asymptomatic. At no time wasthere any neurologic symptom or sign other than oropha-ryngeal dysphagia.

Dantas and Souza discuss several diagnostic con-siderations including (1) corticosteroid (prednisone)therapy causing proximal myopathy (yet the patient hadno proximal limb weakness); (2) a small brainstem in-farct (yet computed tomography [CT] of the brain wasnormal); and (3) benzodiazepine-induced dysphagia. Insupport of their belief that this patient suffered frombenzodiazepine-induced dysphagia, the authors cite a re-cent abstract [1] describing two such cases and neuro-physiologic data indicating ‘‘that benzodiazepines caninhibit discharges from interneurons in nucleus tractussolitarius or nucleus ambiguus responsible for the pha-ryngeal phase of deglutition.’’

CommentsAlthough we believe that benzodiazepines can cause orcontribute to pharyngeal dysphagia, this case report doesnot add further evidence in that regard. It is inconceiv-able to us that an individual on chronic low dosage ben-zodiazepine therapy would suddenly develop profounddysphagia as a consequence. If the patient had been re-challenged by lorazepam and dysphagia had recurred,and especially if dysphagia again resolved promptly fol-lowing elimination of lorazepam, these findings wouldbe much more persuasive.

Whenever a patient acutely develops profoundoropharyngeal dysphagia, especially if there is subse-quent, at least partial, recovery, the overwhelminglylikely diagnosis is stroke. When dysphagia is the pre-dominant or sole problem, brainstem localization shouldbe suspected. Not only CT but also magnetic resonanceimaging (MRI) may fail to detect small brainstem strokesresulting in dysphagia [2], so the diagnosis of brainstemstroke should not be ruled out by negative imaging stud-ies.

References

1. Buchholz D, Jones B, Neumann S, Ravich W: Benzodiazepine-induced pharyngeal dysphagia: report of two probable cases(Abstract).Dysphagia 10:142, 1995

2. Buchholz DW: Clinically probable brainstem stroke presentingprimarily as dysphagia and nonvisualized by MRI.Dysphagia8:235–238, 1993

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