dysphagia in unilateral cerebral lesions

Journal of Neurology, Neurosurgery, and Psychiatry, 1973, 36, 853-860

Dysphagia in unilateral cerebral lesionsJ. C. MEADOWS

From the National Hospital, Queen Square, London

SUMMARY Dysphagia may in rare instances be a presenting feature of unilateral cerebral lesions.Normally, bilateral lesions are necessary to cause neurological disturbance of swallowing but thereappear to be occasional subjects where this is not so. Cases are presented and the literature reviewedto illustrate this. The dysphagia may occur in isolation and is not necessarily accompanied bydysarthria, facial apraxia, or obvious paralysis. The lesion may be on either side and usually involvesthe low posterior frontal region. Cases that have come to necropsy have shown involvement of thelowest part of the precentral gyrus or the posterior part of the inferior frontal gyrus.

When dysphagia occurs in neurological diseaseit is usually accompanied by dysarthria, and,whatever level of the central nervous system isinvolved, it is generally held that a bilateraldisturbance must be present. So far as descend-ing pathways are concerned, this means that asingle structural lesion is likely to cause dys-phagia only if it affects the brain-stem, wherepathWays on the two sides are in close proximity.In general, it can be assumed that if there is asupratentorial cause for dysphagia, this must bebilateral and is therefore probably either vascularor degenerative.The purpose of this paper is to point out that

in rare instances a unilateral cerebral lesion maybe responsible for dysphagia. Three cases aredescribed in which dysphagia was an initialsymptom of a space-occupying lesion affectingone cerebral hemisphere, and a number of otherrelevant cases are discussed. It is not intended toimply that this is a common occurrence butmerely to indicate that exceptions do occur towhat is generally a sound rule.

CASE 1

(A.56173) A 70 year old right-handed man beganto notice difficulty in swallowing liquids some 10months before admission. This became worse so thata cup of tea was cold before he had finished it and ahalf-pint (265 ml.) glass of beer took up to half anhour to drink. He said it was 'as if a flap came downat the back of the throat'. Solids presented ratherless difficulty. He was seen first at the Royal National

Throat, Nose and Ear Hospital where a bariumswallow showed no structural abnormality but 'con-siderable hesitancy in swallowing' was described.Direct laryngoscopy was normal.He was admitted to the National Hospital. There

he complained of occasional urgency and inconti-nence of faeces with less marked urgency of mic-turition for about two months. He felt depressed.Although both he and his family at first denied anyintellectual change, his wife subsequently stated thathe had recently started to sleep in the afternoons,was coming home late, and did not always attend formeals.

General examination was normal. Neurologicalexamination four months before admission had beenreported normal but in the intervening period he haddeveloped a mild left supranuclear facial palsy. Theonly other abnormal finding was that the rightplantar response was less clearly flexor than the left.

Clinical testing of intellect was normal. His speechwas fluent and there was no difficulty in naming or inrepetition. Articulation was at all times normal andthere was no facial apraxia; he could whistle, blowout his cheeks to command, show his teeth, put outhis tongue, and imitate sounds articulated by theexaminer. The palate moved briskly and centrally onboth phonation and reflex testing, and tongue move-ments were full and rapid to command.When he attempted to drink from a glass of water,

this was done slowly, in single gulps which were re-tained in the mouth often for many seconds beforebeing swallowed. Cinefluorography showed thatthere was great hesitancy in initiating the pharyngealphase of swallowing, contrast (whether liquid orsemi-solid) lapping incoordinately back and forth

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FIG. 1. Tumour blush outlined on right carotid angiogram in case 1.

within the oral cavity while the palate also movedirregularly until, after a variable period, it suddenlyelevated to close off the nasopharynx and thetongue simultaneously propelled the contrast intothe pharynx. While lying on his back, so that gravitycarried the contrast into the pharynx, there was nodelay. These studies were kindly carried out atUniversity College Hospital by Dr. D. G. Shaw.

Psychological testing (Wechsler) revealed a VerbalIQ of 127 and a Performance IQ of 116. Radiographsof the skull and chest were normal. An electro-encephalogram (EEG) showed some mainly post-central excess of slow activity, with right-sidedemphasis. A technetium scan showed increased up-take in the right subfrontal area. Right carotidangiography demonstrated a large meningiomaarising from the right sphenoidal ridge (Fig. la, b)and causing a shift of the pericallosal artery andinternal cerebral vein.At operation the meningioma was mushrooming

deeply into the brain but was removed successfullyafter resection of some frontal cortex anterolaterally.Histology confirmed a typical meningioma. Withina few days he was ambulant but the dysphagia wasunchanged. He died suddenly from a pulmonaryembolus six days postoperatively.

Post mortem examination revealed a depressionon the posterolateral aspect of the inferior part ofthe right frontal lobe of the brain, partially filledwith blood clot. Much of the posterior part of the

inferior frontal gyrus was destroyed but at itsposterior end there was a narrow strip which ap-peared healthy, separating the necrotic area from thelowest part of the precentral gyrus. The precentralgyrus itself appeared to be intact but was notexamined microscopically. There was some tentorialherniation on the right and some subfalcine hernia-tion. The brain was sectioned throughout and theextent of the local cerebral damage can be seen in thefrontal slices (Fig. 2). No other focal lesions wereseen. Microscopic examination of the nucleusambiguus on each side revealed no abnormality.

CASE 2

(M.H. A.6686) This patient was under the care ofProfessor R. W. Gilliatt at the Middlesex Hospital.A 36 year old right-handed storeman was admitted

for investigation in May 1972. His right eye had beenenucleated after an illness in early childhood. Other-wise he had been well until two years previously whenhe began complaining of intermittent headache, atfirst occipitally and later either bitemporally or con-fined to the right temple. For about a year he had haddifficulty in swallowing liquids. He would take smallsips and would then have great difficulty in trans-ferring the liquid to the back of his throat; it wouldregurgitate into his nose or even be ejected out of hismouth. This dysphagia varied in severity. On occas-ions it would take 15 to 20 minutes to drink a glass

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Dysphagia in unilateral cerebral lesions

of water, and at one time it reached such severity thathe telephoned his doctor in a panic. In contrast,swallowing of solids was little if at all affected. Forthree months before admission he had noticed im-paired concentration and felt that his balance wasimperfect. There had been a single episode ofparaesthesiae in the left hand lasting a few minutes.He had been examined by neurologists on several

occasions but no abnormality was found until April1972 when it was noted that saliva was pooling at theback of his mouth and that the palatal and pharyngealreflexes were absent, although sensation was pre-served. On phonation the palate moved well butslightly to the left of the midline. When admitted amonth later there was thought, in addition, to beevidence of mild intellectual impairment and alsominimal slurring of speech. Early papilloedema wasnoted. A mild upper motor neurone facial weaknesswas present on the left, and the right plantar responsewas thought by some observers to be extensor. Ten-

FIG. 2. Successive sections through the frontal lobesin case 1, the most posterior being at the level of theheads of the caudate nuclei.

FIG. 3. Radioisotope brain scan demonstratingtumour site in case 2.

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FIG. 4. Iophendylate and air pyogram in case 3, the estimated outline of the abscess cavity is dotted.

don reflexes were symmetrically brisk but there wereno other findings. In particular, the jaw jerk was notincreased, and there was no limitation of tonguemovements or facial apraxia.A brain scan with technetium (Fig. 3) showed up-

take in the right posterior frontal region and carotidarteriography confirmed a large right frontal tumourwhich extended to the surface and was thought toextrude onto the lower part of the frontal convexity.There was 2 cm shift of midline structures. At opera-tion a hard tumour with a large cystic componentoccupied much of the right posterior frontal region.It was incompletely removed. Histology was that ofan astrocytoma grade II. Postoperatively his swallow-ing difficulty disappeared.

CASE 3

A 59 year old right-handed man was admitted toanother hospital with a four week history of difficultyin swallowing, saying that food stayed in his mouth.Three years earlier he had had a Polya gastrectomyand the following year perforated an anastomaticulcer; he had been well since then. Abdominalexamination was reported as normal and no defectwas noted in his speech.Radiographs of the chest were normal. A barium

swallow showed no structural abnormality but it wasnoted that 'the patient's difficulty appeared to bemainly in the mouth, barium remaining for con-siderable periods' before swallowing began.

The swallowing difficulty became more severe butno cause for it was found. A low-grade pyrexia de-veloped. After 10 days it was noted that the leftplantar response was extensor and over the next fourdays he became confused with a left hemianopia andflaccid hemiplegia. His neck was rigid and lumbarpuncture revealed turbid fluid containing 2,875cells/cu. mm (80% polymorphs, 20% lymphocytes).Culture was sterile. He was treated with antibioticsbut continued to deteriorate and three days later wascomatose. Urgent transfer to the National Hospital,Maida Vale, was arranged.On arrival he was comatose with a flaccid left

hemiplegia. His temperature was 38.30 C (1010 F)and he had bronchopneumonia. Carotid angio-graphy disclosed an avascular mass deep in the rightcerebral hemisphere which proved to be an abscessdue to Staphylococcus aureus. A pyogram outlinedthe abscess cavity (Fig. 4).With medical and surgical treatment his condition

improved progressively. Two months later, whenfinally discharged, he was swallowing normally andeating well but had a residual right hemiparesis.

ADDITIONAL CASES

Since being alerted to the fact that dysphagia mayoccur in exceptional patients with unilateral cerebrallesions, the author has seen, in addition to thosereported above, three further cases where difficulty inswallowing has been a minor feature, and they are

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reported at this point simply to draw attention to thesite of the lesions. All were seen at the NationalHospital, Maida Vale. In two patients with largefrontal mass lesions, dysphagia occurred (eclipsed byforgetfulness and frontal gait disturbance) for somemonths before diagnosis. One had a large rightpterion meningioma (M.V.H. 68957), the other aright frontal arachnoid cyst (M.V.H. 70400); neithershowed overt pseudobulbar palsy but the formerpatient had mild dysarthria. Another patient (M.V.H.72254) developed first right facial weakness and thendysphasia and focal sensory seizures affecting theright arm. He finally developed severe dysphagiarequiring nasogastric feeding. A malignant glioma ofthe left posterior frontal region was found oninvestigation.

DISCUSSION

There are a few previously reported cases ofsevere dysphagia occurring in patients withlesions confined to one cerebral hemisphere.Bastian (1898) described a patient in whom therewas sudden onset of aphasia and right hemi-plegia associated with difficulty in swallowingand in protruding the tongue, both of whichsubsequently improved. The patient finally diedand at necropsy the brain was found to behealthy 'except at two limited spots, of which thechief was the posterior part of the third frontalconvolution on the left side. Here was a softenedand almost diffluent patch, about three-quartersof an inch in breadth, reaching from the highestpart of the third convolution backwards anddownwards to the fissure of Sylvius. The softenedpart was not actually the most posterior part ofthe convolution for there was a narrow, un-softened strip between it and the ascendingfrontal convolution. On cutting into the brain asecond small patch of softening was seen in thecentre of the left hemisphere, external to andrather above the corpus striatum, and extendingtowards the posterior extremity of the fissure ofSylvius.'

Pussep and Levin (1923) reported a womanwho developed severe dysphagia and anarthriaabruptly, and had to initiate swallowing bypushing food manually to the back of thethroat, throwing her head back until foodcame into contact with the pharynx, where-upon swallowing proceeded normally. Necropsy

showed two areas of softening, one in the leftsupramarginal gyrus, the other in the lower partof the left precentral gyrus. A similar patient,described by Tuch and Nielsen (1941) developedsudden complete aphagia and anarthria, beingunable to swallow even saliva. There wasapraxia of the facial musculature but the onlyother neurological sign described was a slightdroop of the right side of the mouth. Necropsyrevealed softening of the lower part of the leftpre- and post-central gyri.

Unlike these patients, two of the present threecases had dysphagia as the sole initial symptom.The other case had a past history of headaclhebut again dysphagia was severe and for sometime led to a mistaken diagnosis of posteriorfossa tumour. Cases 1 and 2 were very similarclinically. In both there was selective dysphagiafor fluids, facial apraxia was absent, the tonguemoved fully and freely to command, the jawjerk was not increased, and the palate elevatedwell on phonation. However, case 2 differed inthat the palatal and pharyngeal reflexes wereabsent bilaterally, although sensation was pre-served. This was not recorded in the other casesmentioned above and the reason for it is notclear. The lesion in both cases 1 and 2 was atumour in the right postero-inferior frontalregion. Case 1 died of pulmonary embolus sixdays postoperatively and the brain was examinedat necropsy. The findings were complicated bythe effects of operation, but the main site ofdamage was the posterior part of the inferiorfrontal gyrus and the white matter deep to it.The precentral gyrus did not look damagedmacroscopically, but the meningioma as demon-strated radiologically (Fig. 1) almost certainlyencroached close onto the lowest part of thisgyrus.

In case 3, the lesion (an abscess) was moredeeply placed. However, this patient was notexamined by the author or investigated neuro-logically until some weeks after the initial onsetof dysphagia, by which time he had lapsed intocoma. There had probably been considerableextension of the abscess during this period. Itwas the only case where the lesion was deeplyplaced and, since the first symptom was a similardifficulty in the initial stage of swallowing tocases 1 and 2, it is possible that the abscess mayhave interrupted either afferent or efferent con-

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nections with the cortical area affected in theother patients.The low posterior frontal region was involved

on one or other side in all the other cases, butthe precise site of the lesion requires furtherdiscussion. The necropsy findings in case 1

showed that the precentral gyrus was macro-

scopically spared and that the major site ofdamage was further forward in the inferiorfrontal gyrus. However, it is likely that in lifethe lowest part of the precentral gyrus was sub-ject to considerable pressure and distortion.Necropsies were not performed in the othertumour cases and the available information isnot sufficient for precise localization within thisgeneral area. On the other hand the three cases

with vascular disease had discrete cortical lesionsat necropsy. In two cases the lowest part of theprecentral gyrus was involved but in the thirdthe lesion was apparently confined to the inferiorfrontal gyrus. If these descriptions are to bebelieved it appears that a lesion either of theprecentral gyrus or the posterior part of theinferior frontal gyrus may cause dysphagia.However, only in Bastian's case was the inferiorfrontal gyrus said to be involved in isolation.

Penfield and Jasper (1954) have shown thatstimulation of the lower part of either precentralgyrus at operation causes swallowing, vocaliza-tion, and movement of the face and jaw, and thisaccords with the above localization. However,there is normally bilateral representation of thecranial musculature in the primary motor cortex,and bilateral lesions are usually required tocause permanent disturbance of speech or

swallowing. Bilateral, symmetrical cortical les-ions are rare in man, but aphagia was reported,for example, by Foix, Chavany, and Marie (1926)in a case where softening of the lowest part ofboth precentral gyri and the posterior part of theinferior frontal gyri was found at necropsy.

Similarly, bilateral corticobulbar tract lesions incerebrovascular disease cause pseudobulbarpalsy, where dysphagia is a prominent symptom.

In contrast, unilateral lesions are not usuallyassociated with significant dysphagia. Strokescausing hemiplegia occasionally give rise totransient hesitancy in swallowing but this onlyvery rarely causes the patient concern. However,Penfield and Jasper (1954) found that significantdysphagia may occur transiently after unilateral

cortical ablations: the patient may 'seem toforget how to swallow for a few days ... andmouth and tongue may be used awkwardly for atime in forming words, after a lesion of the lowerRolandic region, even on the side opposite tothe localization of speech'.On the basis of these observations it therefore

seems likely that the dysphagia seen in thepresent patients relates to damage at or close tothe lowest part of the precentral gyrus. Analternative explanation in the tumour casesmight be that dysphagia is a false localizingfeature due in some way to raised intracranialpressure or distortion of intracranial structures,but if this were so it is remarkable that the site ofthe lesions was always approximately the same.It is possible that a tumour at this site causes uni-lateral damage and that contralateral damageoccurs as a false localizing feature, perhaps bypressure against the opposite tentorial edge. It isnotable that the plantar response ipsilaterally tothe tumour in cases 1 and 2 was questionablyabnormal, which would support this view. Butit cannot explain the vascular cases. In the vascu-lar cases, unsuspected damage on the oppositeside might be postulated but this was not foundin the cases reported above that came to necropsy.We are left with the suggestion that there are rareindividuals in whom the pathways in a singlehemisphere are incapable of alone supportingthe swallowing process.Tuch and Nielsen (1941) discussed their

patient under the title 'Apraxia of swallowing'.However, the use of the term 'apraxia' in thiscontext is arguable and it may be more correctto regard the dysphagia as a more elementarymotor disturbance. Dysphagia is not usually afeature of the more generalized apraxia of thebulbar musculature known as facial apraxia.Thus, facial apraxia typically affects the tongue,which cannot be protruded to command yet maybe protruded spontaneously a few momentslater to lick the lips. No such apraxia occurredin cases 1 and 2, for example, yet in case 1incoordinated movement of the tongue wasdemonstrated radiologically during attemptedswallowing. It is true that dysphagia and facialapraxia may coexist as in Tuch and Nielsen'scase, but it is questionable whether they aremanifestations of the same disorder rather thanmerely neighbourhood symptoms. The fact that

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dysphagia may occur with either right or left-sided lesions, which is very rarely the case withfacial apraxia, casts further doubt on theirrelationship.

This leads us to a consideration of the ana-tomical pathways subserving these functions.The pathway for linguofacial movements tocommand is linked to cerebral speech dominanceand its likely route from Wernicke's area for-ward in the arcuate fasciculus to the associationcortex anterior to the left face area and thence toboth primary motor representations has beendiscussed by Geschwind (1965). Interruptionanywhere from Wernicke's area to the left pre-motor cortex will cause facial apraxia. On theother hand, the central pathway for swallowingis normally bilateral, is not linked to speech, andat its simplest may consist of little more than anafferent projection from the periphery to theprimary sensory cortex bilaterally, thence by theabundant connections known to exist in primates(Bailey, Bonin, and McCulloch, 1940; Jones andPowell, 1969) to the primary motor cortex (per-haps via premotor cortex) and finally to thepyramidal tracts. Premotor cortex may beinvolved, for bilateral excision of the inferiorfrontal gyri caused persistent dysphagia anddysarthria in a patient reported by the Columbia-Greystone associates (1949). Also, the limiteddescription of the necropsy findings in Bastian'scase suggests that the primary motor region wasspared. However, it cannot be certain in thesecases that dysphagia was not due to secondarydamage to the motor pathway, for bilateralexcisions of the anterior, middle, and posteriorparts of the inferior frontal gyri in other patientsin the Columbia-Greystone study did not causedysphagia.The anencephalic infant may suckle success-

fully as long as the brain-stem is intact (Gamper,1926; Utter, 1928), indicating that cortical func-tion is not essential for swallowing. However,the situation in the infant is different from theadult, for the teat or nipple extends well back intothe oral cavity so that milk is carried directly bythe sucking reflex into the pharynx, from wherereflex swallowing follows. In the adult, food hasto be propelled actively through the oral cavity,the tongue pressing upward and forwardsagainst the hard palate so that the bolus issqueezed backward like toothpaste from a tube

(Ardran and Kemp, 1951). At the same time, thenasopharynx is closed off. It is this process,presumably learned during weaning, that isdefective in the present cases. It is a stereotypedsemi-automatic act which once learned may re-quire little cortical intervention other than in itsinitiation, some control being necessary to rejectunpalatable items or to deal with the variedfoods encountered in everyday life; liquids areswallowed without delay but solids require firsta variable degree of mastication. Why swallow-ing of liquids should be so much more affected inat least some of the cases of dysphagia associatedwith unilateral cerebral lesions is not clear butpossibly these act as a less effective stimulus ininitiating the process.

Finally, it is interesting to note that, accordingto Heilbronner (quoted by Nathan, 1947), reflexswallowing may persist when higher control isdefective. He claims that the advanced 'apractic'who cannot swallow normally retains the suckingreflex and can be satisfactorily nourished bybottle like an infant.

I am grateful to Dr. J. N. Blau, Professor R. W.Gilliatt, and Professor John Marshall for permissionto report these cases, to Dr. P. W. Nathan for hishelpful comments on the manuscript, and to Pro-fessor William Blackwood for his help with theneuropathological aspects.

REFERENCES

Ardran, G. M., and Kemp, F. H. (1951). The mechanism ofswallowing. Proceedings of the Royal Society of Medicine,44, 1038-1040.

Bailey, P., Bonin, G. von, and McCulloch, W. S. (1950). TheIsocortex of the Chimpanzee. University of Illinois Press:Urbana.

Bastian, H. C. (1898). A Treatise on Aphasia and OtherSpeech Defects, p. 87. Lewis: London.

Columbia-Greystone Associates (1949). Selective PartialAblation of the Frontal Cortex. Edited by F. A. Mettler.Hoeber: New York.

Foix, Ch., Chavany, J.-A., and Marie, J. (1926). Diplegiefacio-linguo-masticatrice d'origine cortico sous-corticalesans paralysie des membres. Revue Neurologique, ler sem.,214-219.

Gamper, E. (1926). Bau und Leistungen eines menschlichenMittelhirnwesens (Arhinencephalie mit Encephalocele).Zugleich ein Beitrag zur Teratologie und Fasersystematik.Zeitschrift gesamte fur die Neurologie und Psychiatrie, 102,154-235.

Geschwind, N. (1965). Disconnexion syndromes in animalsand man. Brain, 88, 585-644.

Jones, E. G., and Powell, T. P. S. (1969). Connexions of the

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somatic sensory cortex of the rhesus monkey. 1. Ipsilateral praxie). Zeitschrift fur die gesamte Neurologie und Psychi-cortical connexions. Brain, 92, 477-502. atrie, 87, 441-450.

Nathan, P. W. (1947). Facial apraxia and apraxic dysarthria. Tuch, B. E., and Nielsen, J. M. (1941). Apraxia of swallowing.Brain, 70, 449-478. Bulletin of the Los Angeles Neurological Society, 6, 52-54.

Pussep, L., and Levin, L. (1923). Zur Frage der Storungen Utter, 0. (1928). Ein Fall von Anenzephalie. ActaPsychiatricades Schluckens von apraktischem Charakter (Aphago- et Neurologica, 3, 281-318.



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