Piecemeal and subjects and in - Journal of Neurology ... · piecemeal deglutition or as a sign...

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J7ournal of Neurology, Neurosurgery, and Psychiatry 1996;61:491-496 Piecemeal deglutition and dysphagia limit in normal subjects and in patients with swallowing disorders Cumhur Ertekin, Ibrahim Aydogdu, Nur Yuceyar Department of Clinical Neurophysiology and Neurology, Ege University Medical School Hospital, Bornova, Izmir, 35100, Tiirkiye C Ertekin, I Aydogdu N Yuceyar Correspondence to: Professor Cumhur Ertekin, Department of Neurology and Clinical Neurophysiology, Ege University Medical School Hospital, Bomova, Izmir 35100, Turkey. Received 26 March 1996 and in revised form 5 June 1996 Accepted 27 June 1996 Abstract Objective-Before the advanced evalua- tion of deglutition and selection of a treat- ment method, objective screening methods are necessary for patients with dysphagia. In this study a new electroclin- ical test was established to evaluate patients with dysphagia. Methods-This test is based on determin- ing piecemeal deglutition; which is a physiological phenomenon occurring when a bolus of a large volume is divided into two or more parts which are swal- lowed successively. The combined elec- trophysiological and mechanical method used to record laryngeal movements detected by a piezoelectric transducer, and activities of the related submental integrated EMG (SM-EMG)-and some- times the cricopharyngeal muscle of the upper oesophageal sphincter (CP- EMG)-were performed during swallow- ing. Thirty normal subjects and 66 patients with overt dysphagia of neuro- genic origin were investigated after detailed clinical evaluation. Twenty patients with a potential risk of dyspha- gia, but who were normal clinically at the time of investigation, were also evaluated to determine the specificity of the test. All subjects were instructed to swallow doses of water, gradually increasing in quantity from 1 ml to 20 ml, and any recurrence of the signals related to swallowing within the eight seconds was accepted as a sign of dysphagia limit. Results-In normal subjects as well as in the patients without dysphagia, piecemeal deglutition was never seen with less than 20 ml water. This volume was therefore accepted as the lower limit of piecemeal deglutition. In patients with dysphagia, dysphagia limits were significantly lower than those of normal subjects. Conclusion-The method is a highly spe- cific and sensitive test for the objective evaluation of oropharyngeal dysphagia even in patients with suspected dysphagia of neurogenic origin. It can also be safely and simply applied in any EMG labora- tory. (7 Neurol Neurosurg Psychiatry 1996;61:491-496) Keywords: oropharyngeal dysphagia; piecemeal deglu- tition; dysphagia limit If a large amount of material is put into the mouth at one time, piecemeal deglutition usu- ally occurs in all normal adult human subjects. Piecemeal deglutition refers to division of the bolus into two or three swallows successively rather than swallowing the entire bolus in one.' Various aspects of piecemeal deglutition are unknown. First of all what is the upper limit of the amount of material that can be swallowed in one portion in normal adult subjects? So far, this has not been determined. Therefore one aim of the study was to delineate the upper limit of amount of liquid that is swal- lowed as one portion in the normal population and in patients with overt and suspected dysphagia, and to establish any difference between the two groups. It was hoped that this may provide a useful test for the evaluation of patients with dysphagia. The second aim was to understand which mechanism underlies the phenomenon of piecemeal deglutition. There is no known satis- factory explanation as to which physiological factors are involved, but some ideas are put forward based on our clinical and electrophys- iological findings. Although they are different from each other in the clinical sense, we generally preferred to use of the term "dysphagia limit" instead of "piecemeal deglutition" because, even in some normal subjects "a kind of choking sensation" was experienced if they attempted to drink or to swallow the larger amounts of water used. A preliminary account of this study has been reported elsewhere.2 Materials and methods Investigations were made on 30 normal adult subjects (10 women, 20 men) most of whom were hospital staff and colleagues who did not have any oropharyngeal or gastrointestinal problems. They ranged in age from 20 to 71 (mean age 43T0 (SD 17 6)). Sixty six patients with overt dysphagia or suspected dysphagia were investigated both clinically and electrophysiologically. The patients ranged in age from 20 to 82 (mean age 55-7 (SD 17 3)). Overt dysphagia is defined when the patient needs a nasogastric catheter. The term suspected dysphagia is used for the patients who describe dysphagic complaints' but who can still swallow without any auxillary aid. Another group of 20 patients with neurological disorders (10 women, 10 men, mean age 46-9 (SD 14 2), age range 491 on June 1, 2020 by guest. Protected by copyright. http://jnnp.bmj.com/ J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.61.5.491 on 1 November 1996. Downloaded from

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Page 1: Piecemeal and subjects and in - Journal of Neurology ... · piecemeal deglutition or as a sign ofdysphagia limit. In some normal subjects the amount of liquid increased up to 35 ml.

J7ournal ofNeurology, Neurosurgery, and Psychiatry 1996;61:491-496

Piecemeal deglutition and dysphagia limit innormal subjects and in patients with swallowingdisorders

Cumhur Ertekin, Ibrahim Aydogdu, Nur Yuceyar

Department of ClinicalNeurophysiology andNeurology, EgeUniversity MedicalSchool Hospital,Bornova, Izmir,35100, TiirkiyeC Ertekin,I AydogduN YuceyarCorrespondence to:Professor Cumhur Ertekin,Department of Neurologyand ClinicalNeurophysiology, EgeUniversity Medical SchoolHospital, Bomova, Izmir35100, Turkey.Received 26 March 1996and in revised form5 June 1996Accepted 27 June 1996

AbstractObjective-Before the advanced evalua-tion of deglutition and selection of a treat-ment method, objective screeningmethods are necessary for patients withdysphagia. In this study a new electroclin-ical test was established to evaluatepatients with dysphagia.Methods-This test is based on determin-ing piecemeal deglutition; which is aphysiological phenomenon occurringwhen a bolus of a large volume is dividedinto two or more parts which are swal-lowed successively. The combined elec-trophysiological and mechanical methodused to record laryngeal movementsdetected by a piezoelectric transducer,and activities of the related submentalintegrated EMG (SM-EMG)-and some-times the cricopharyngeal muscle of theupper oesophageal sphincter (CP-EMG)-were performed during swallow-ing. Thirty normal subjects and 66patients with overt dysphagia of neuro-genic origin were investigated afterdetailed clinical evaluation. Twentypatients with a potential risk of dyspha-gia, but who were normal clinically at thetime of investigation, were also evaluatedto determine the specificity of the test. Allsubjects were instructed to swallow dosesof water, gradually increasing in quantityfrom 1 ml to 20 ml, and any recurrence ofthe signals related to swallowing withinthe eight seconds was accepted as a sign ofdysphagia limit.Results-In normal subjects as well as inthe patients without dysphagia, piecemealdeglutition was never seen with less than20 ml water. This volume was thereforeaccepted as the lower limit of piecemealdeglutition. In patients with dysphagia,dysphagia limits were significantly lowerthan those ofnormal subjects.Conclusion-The method is a highly spe-cific and sensitive test for the objectiveevaluation of oropharyngeal dysphagiaeven in patients with suspected dysphagiaof neurogenic origin. It can also be safelyand simply applied in any EMG labora-tory.

(7 Neurol Neurosurg Psychiatry 1996;61:491-496)

Keywords: oropharyngeal dysphagia; piecemeal deglu-tition; dysphagia limit

If a large amount of material is put into themouth at one time, piecemeal deglutition usu-ally occurs in all normal adult human subjects.Piecemeal deglutition refers to division of thebolus into two or three swallows successivelyrather than swallowing the entire bolus inone.'

Various aspects of piecemeal deglutition areunknown. First of all what is the upper limit ofthe amount of material that can be swallowedin one portion in normal adult subjects? Sofar, this has not been determined. Thereforeone aim of the study was to delineate theupper limit of amount of liquid that is swal-lowed as one portion in the normal populationand in patients with overt and suspecteddysphagia, and to establish any differencebetween the two groups. It was hoped that thismay provide a useful test for the evaluation ofpatients with dysphagia.The second aim was to understand which

mechanism underlies the phenomenon ofpiecemeal deglutition. There is no known satis-factory explanation as to which physiologicalfactors are involved, but some ideas are putforward based on our clinical and electrophys-iological findings.

Although they are different from each otherin the clinical sense, we generally preferred touse of the term "dysphagia limit" instead of"piecemeal deglutition" because, even in somenormal subjects "a kind of choking sensation"was experienced if they attempted to drink orto swallow the larger amounts of water used.A preliminary account of this study has

been reported elsewhere.2

Materials and methodsInvestigations were made on 30 normal adultsubjects (10 women, 20 men) most of whomwere hospital staff and colleagues who did nothave any oropharyngeal or gastrointestinalproblems. They ranged in age from 20 to 71(mean age 43T0 (SD 17 6)).

Sixty six patients with overt dysphagia orsuspected dysphagia were investigated bothclinically and electrophysiologically. Thepatients ranged in age from 20 to 82 (meanage 55-7 (SD 17 3)). Overt dysphagia isdefined when the patient needs a nasogastriccatheter. The term suspected dysphagia isused for the patients who describe dysphagiccomplaints' but who can still swallow withoutany auxillary aid. Another group of 20 patientswith neurological disorders (10 women, 10men, mean age 46-9 (SD 14 2), age range

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Ertekin, Aydogdu, Yiiceyar492

Normal subjectWater swallow

1 ml Laryngeal sensor signal

SM-EMG

3 ml

5ml

10 ml

20 ml

1000ms 50 lV

25-76) were also separately examined eitherbecause they had no dysphagia, or they hadrecovered from dysphagia and were com-

pletely normal at the time of investigation fordeglutition. Thus 86 patients in total were

examined (33 women, 53 men). Their ages

ranged from 20 to 82 (mean age 53 7 (SD17-0)), and they were selected from theDepartments of Neurology and Gastro-enterology. The table gives the list of clinicaldiagnoses.

All patients were diagnosed using CT,MRI, EMG, and other appropriate methods inaddition to clinical criteria. Time between theonset of the medical-neurological problem andthe investigation ranged from seven days to 35years. Time between the onset of dysphagiaand investigation ranged from seven days to

10 years. Informed consent was obtained fromall patients and the study was accepted by thelocal ethics committee.The normal subjects and patients sat on an

examination couch and were instructed to

hold their heads in a natural upright position.Then the electrophysiological method de-scribed previously3 was applied. In brief, EMGactivity was recorded on a Medelec modelMS-20 EMG apparatus using bipolar silverchloride EEG electrodes taped under the chinover the mylohyoid-geniohyoid-anterior digas-tric muscle complex (SM-EMG). The EMGsignals were band pass filtered (100 Hz-10

kHz), amplified, rectified, and integrated.For detection of laryngeal movements

(upward and downward) a mechanical sensor

that consisted of a simple piezoelectric waferwith a 4 x 2-5 mm rubber bulge fixed at its

centre was placed on the coniotomy regionbetween the cricoid and thyroid cartilages at

the midline. 1 4The sensor output was con-

nected to another channel of the EMG appa-

ratus. The sensor amplifier output was also

band pass filtered (cut off frequencies0-01-20 Hz). The sensor gave two deflectionsof generally opposing polarity during eachswallow, the first of which was often a positive(downward on the screen as in fig 1) deflectionor vice versa. The leading or trailing edge of

the first deflection was used to trigger the

delay line circuitry of the recording apparatusso that all signals were time locked to the sameinstant. The first deflexion of the laryngealsensor signal represents the upward movementof the larynx and the second deflection, itsdownward movement.3

Because the SM-EMG activity coincidedwith the laryngeal upward movement, the rec-tified-integrated SM-EMG activity was alsotime locked to the laryngeal sensor signals.The total sweep time was set at 10 secondsand the delay line was started two secondsafter the onset of the single sweep of the oscil-loscope. Therefore after an amount of waterwas drunk, the effect of the bolus was followedup for eight seconds. Occasionally, an analysistime of 18 seconds was used.Normal control subjects and patients were

each given 1, 3, 5, 10, 15, and 20 ml of water ina stepwise manner, and began to swallowimmediately after being instructed to do so bythe examiner. After the water was deliveredinto the mouth by a graduated syringe; swal-lows were initiated with the water positionedon the tongue and the tongue tip touching theupper incisors.' Oscilloscopic traces werestarted at the examiner's order to swallow. Inthis way laryngeal sensor signals and integratedsignals of SM-EMG activity were recorded atthe beginning of the long sweeps (two secondsafter the onset of each sweep). As each volumeof liquid was swallowed, single sensor and SM-EMG signals were usually recorded at thebeginning of the recording, and any recurrenceof the two signals together within the eight sec-ond period of the recording was accepted aspiecemeal deglutition or as a sign of dysphagialimit. In some normal subjects the amount ofliquid increased up to 35 ml. In patients withdysphagia the examination was stopped if thepatient showed any piecemeal deglutition orany sign of subglottic aspiration such as cough-ing or wet voice. If there was any suspicion ofpiecemeal deglutition, the same procedure wasrepeated and recorded for a second time withthe same quantity of water.The EMG of the cricopharyngeal muscle of

the upper oesophageal sphincter was alsorecorded in five normal subjects and in somepatients (40 out of 66 dysphagic patients andfive out of 20 non-dysphagic patients) inaddition to the SM-EMG recordings. Thecricopharyngeal muscle EMG was recordedusing concentric needle electrodes (Medelecdisposable needle electrode DMC-37; diameter0-46 mm, recording area 0 07 mm2). The nee-dle electrode was inserted through the skin atthe level of the cricoid cartilage, about 1 5 cmlateral to its palpable lateral border in the pos-teromedial direction. High frequency, tonicEMG activity appeared on the oscilloscopicscreen as the electrode penetrated the muscle.During swallowing of dry and liquid material,this tonic activity disappeared for a short time(400 ms-500 ms).3 Activity of the cricopharyn-geal muscle was also rectified-integrated dur-ing all types of swallowing. The filter settingswere the same as those used for the SM-EMGactivity recording. The specificity and sensitiv-ity of this method were also calculated.,

Figure 1 Laryngealsensor signals (top traces ineach pair) and integratedsubmental EMG activities(lower traces in each pair)during swallowing differentamounts of water,increasing in quantity stepby step from 1 to 20 ml.Note that all volumes wereswallowed at one go up to20 ml. Time calibrationmarks are 1000 ms in alltraces and the amplitudevalue relates to muscleactivity, in this and allsubsequent figures.

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Piecemzeal deglutition and dysphagia limit in normal subjects anid in patienzts with swallowing disorders

Figure 3 Dysphagialimits ofpatients withdysphagia. Note the peakof dysphagia limits ofpatients showing signs ofaspiratiotn whileszvallowing I ml water,and the peak of dysphagialimits ofpatiemits zvithoutsignjificant aspirationi whileswallowing 10 mmml water or

mtiore.

Normal subjectWater swa ow

Laryngeal sensor signal1 ml

CP-EMG

3 m l ^

V-

20 ml

5c¾1v

__

30 ml

ResultsAs all signals were time locked and stabilisedon the screen by triggering the oscilloscopewith the leading edge of first deflection, itbecame possible to determine whether theamount of the liquid was swallowed at once,or divided into two parts, or aspirated during a

period of eight seconds after the first degluti-tion. Figure 1 shows the swallowing behaviourof a normal subject for different amounts ofbolus from 1 ml to 20 ml. Whatever theamount of water drunk, there was no piece-meal deglutition and all water was swallowedat one go at the beginning of the oscilloscopictraces within eight seconds. The durationbetween the onset points of the two sensor sig-nals and the duration of the SM-EMGincreased with the increase of the bolus vol-ume. This is a well known phenomenonrelated to the longer relocation time of thelarynx and the longer lasting pulling effect ofthe submental muscles with larger bolusvolume.

In all normal subjects, piecemeal deglutitionwas never found within the amount of 20 mlwater swallowed. But with more than 20 mlwater, some normal subjects could not swal-low the material all at once and the bolus vol-ume was divided into two aliquots andsuccessively swallowed (fig 2). In the normalsubject depicted in fig 2, piecemeal deglutitionwas found with 30 ml water. The importantfeature of normal piecemeal deglutition was

that the divided piece of material was swal-

16-

14 L12 D

0

z 10 ecm,: 8

*Z 6 C-XL 4

2-0 L

i Without

aspiration= With

aspiration"I,

, %...

1 ml 3 ml1 5m1lml 1

Dysphagia limit

15 ml

Amyotrophic lateral sclerosis

Water swallowLaryngeal sensor signal

1 ml

3 ml

5 ml 50 pV1000

10 ml

Figure 4 Latynmgeal sen1sor signials (upper traces ini eachpai)r) anid integrated activities of cricophar-xvngeal muiiiscle ofthe upper oesophageal sphincter (CP-EA'IG) (lozver- tr-acesin? each pair) recordedfrom a case of amyvotrophic lateralsclerosis wAhile swallowing differenit amoflunts of zvaterinlcreasintg i.n quantity step by step fromii 1 to 10 mil. Notethe doublc swallows zvheni drinking 10 ml weater. (Eachlinle just below the CP-EMG trace at 10 ml waterszvallowzinlg intdicates the disappearance of the to11iC activitylof the cricophatyngeal muscle which reptesenits swallowingactioni.)

lowed successively without a significant timeinterval. Figure 2 shows that the successiveswallowing of the material of deglutition couldalso be accompanied by successive EMGpauses of the cricopharyngeal muscle, whichnormally occur with increased SM-EMGactivity.'

Swallowing 20 ml water was accepted as thelower limit of piecemeal deglutition in all 30normal subjects and the term of "dysphagia

Myasthenia gravisWater swallow

1 mlLaryngeal sensor signal

SM-EMG

50 pV3ml 1000OMs

5m1 /'v-vY'

r

Figure 5 Laiyngeal scmisor sigmials (top ti-aces in each

pail) anid intlegr-ated submental E.AIG activities (7owerti-aces in each pair) recorded.fi-omn a patielit zw'ithinvasthenia gravis with overt dv,sphagia while swallowhingdifterent aimmounts of water, immcreasing in quianitity step by

step fromn 1 to 5 mmml. Whlile swallowing 5 idil weater thepatieiit begami to couigh ii additiomi to exhhibitinlg piccmlcaldeglltitioni. This imidicates larnugeal aspirationm. Notc the

20 ml prolomiged semisor artefacts i-elated to coughina which zsct-calso clinicalb' iioted (the lliec juist belozw thme sensor signlall at5 iml zwate- swallowing,g).

Figure 2 Asfig 1 exceptthe lower traces, whichshow initegrated EMGactivities fromti thecricopharyngeal muscle ofthe upper oesophagealsphinlcter (CP-EMG).Note that with mtiore thant20 ml zwater, this normalsubject divided the bolusinto two aliquots zvhichwere swallozwedsuccessively; this constitutespiecemeal deglutition.(Each lisle just below theCP-EMG trace atswallowing 30 mnl waterindicates the disappearaniceof the tonic activity of thecricopharyngeal musclewhich representsswallowinlg action.)

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Ertekin, Aydogdu, Yuceyar

Dysphagia limits obtained from all the patients with and without dysphagia

Dysphagia limits (ml water) *

NormialGroups ofpatienits (No) 1 3 5 10 15 20 limitt Total

ALS (13) + 2 2 1 4 1 0 0 103 3

Myasthenia gravis (19) + 3 3 1 1 0 0 1 910 10

Polymyositis dermatomyositis (7) + 3 1 0 0 0 0 1 52 2

Myotonic dystrophy (4) + 0 0 0 1 0 2 0 3- ~ ~~~~~~~~~~~~~11

Stroke (16)t + 5 2 2 6 0 1 0 160 0

Pseudobulbar palsy (11) + 2 1 3 2 2 1 0 110 0

Movement disorders (13)§ + 1 1 1 2 0 3 1 94 4

Basis cranii compression (3) + 0 0 2 1 0 0 0 30 0

Total + 16 10 10 17 3 7 3 66- 0 0 0 0 0 0 20 20

*Volumes swallowed in two or more stages.tVolumes (20 ml or more) swallowed at one go, same as in normal subjects.tMainly vertebrobasilar infarction (12).§Parkinson's disease (nine cases); oromandibular dystonia (two); Huntington'sALS = amyotrophic lateral sclerosis; + = with dysphagia; - = without dysphagia.

limit" was used even for the normal subjects.In the range of 25-40 ml, the amount of waterwhich could not be drunk in one bolus variedfrom subject to subject, and whenever piece-meal deglutition was found, the subject experi-enced some kind of unpleasant sensation,although liquid was never aspirated.

In all but three of the 66 patients with overtor suspected dysphagia; the dysphagia limitswere consistently lowered, by between 20 mland 1 ml (fig 3). The dysphagia limits wereseverely reduced to 1 ml water in patients fedby nasogastric tube. In the patients with sus-pected dysphagia but who were still feedingwithout aid, dysphagia limits were lowered to1 ml-20 ml with a peak of 10 ml. Anotherqualitative feature of "piecemeal deglutition"in dysphagic patients was that the dividedamounts swallowed were considerably sepa-

Polymyositis

Water swallow

Before treatment After corticosteroid treatment

1 ml 3 ml Laryngeal sensor signal

3ml 5ml X

51 -OmI5 ml lo1m ml m

i ~~~1000M 1000M

Figure 6 Laryngeal sensor signals (top traces in each pair) and integrated submentalEMG activities (lower traces in each pair) recordedfrom a patient with polymyositis beforeand after treatment. The patient was swallowing different amounts of water, increasing inquantity step by step. Note the piecemeal deglutition which began to occur even at 1 ml ofwater before treatment. The patient could swallow all the volumes from 3 ml to 20 ml whenshe recoveredfrom dysphagia after treatment. (Lines just below the SM-EMG activity at1-10 ml water drinking indicate the swallowing actions after thefirst one.)

chorea (one); Chorea-acanthocytosis (one).

rated from each other in time and oftendivided into more than two swallows (fig 4).An important finding was the occurrence oflaryngeal aspiration during the piecemealdeglutition with amounts of water less than 10ml, especially in patients with overt dysphagiaand with nasogastric catheters. This has some-times been recorded clinically and graphically(fig 5).

In 20 patients without dysphagia, dysphagialimits were the same as the normal controlgroups (table). These patients could all easilyswallow the different amounts of water includ-ing the 20 ml dose. They had recovered fromthe dysphagic period in the course of their dis-eases for example, myasthenia gravis, stroke,or polymyositis-or they had shown no dys-phagia up to the present investigation as inthree patients with amyotrophic lateral sclerosiswithout bulbar symptoms and in somepatients with Parkinson's disease.The specificity and sensitivity of this

method were 100% and 95 4% respectively.The method of "dysphagia limit" seemed to

be useful in following up the patient's dyspha-gia. Dysphagia limits rose into the normalrange as patients recovered (fig 6).

DiscussionThe objective evaluation of dysphagia isimportant for the selection of a treatmentmethod.' Videofluoroscopic and manometricevaluations may be indicated for such patients,but these methods are expensive and time con-suming, and care of the neurologicallyimpaired patient during examination is some-times difficult. It has therefore been necessaryto develop clinical screening methods to iden-tify patients with suspected or established dys-phagia who are at risk of aspiration. Thebedside swallowing evaluation has long beencriticised for its lack of accuracy for patientswith dysphagia and aspiration. It has beenreported that even the most experienced clini-cians fail to identify about 40%-50% of aspi-

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Piecemeal deglutition and dysphagia limit in normal subjects and in patients with swallowing disorders

rating patients during a bedside examination.' 8It was recently found that several clinical fac-tors correctly predict about two thirds of boththose who aspirate and those who do not.9Some simple screening tests have recently

been developed for use before further radio-logical, manometric, and advanced electro-physiological evaluation of deglutition inpatients with overt or suspected dysphagia andsilent aspiration.8 10-14 Most of these tests usu-ally depend on clinical findings and subjectiveevaluations while patients are drinking a cupof water varying considerably in amount from50 ml to 200 ml. Basically, careful observa-tions were made of the timing of swallowing orthe amount swallowed, or laryngeal move-ments were counted for each swallow, using astopwatch and a medicine container. Clinicalresults such as coughing and signs of aspira-tion were noted. These methods proved to besomewhat better than bedside examination forevaluation and diagnosis of dysphagia; butthey have not approached the diagnostic valueof videofluoroscopy for example. Besides this;continuous drinking of such a large amount ofwater in patients with overt or silent aspirationor in uncooperative patients may carry somerisks. Therefore these methods could not beeasily performed in such patients. Increasingamounts of water up to a teaspoonful as toler-ated by the patient's capabilities have beenjudged by an examiner in one study.8 Thismethod is similar to ours in respect of presen-tation of water step by step in increasingamounts. This technique is safer than othersmentioned above.

In our method of diagnosis by "dysphagialimit" there is a combination of both clinicaland electrophysiological tests for drinkingbehaviour. Therefore the results are objective,recordable, and obviously repeatable at anytime. Due to the gradual increase of the quan-tity of water, from 1 ml to 20 ml, which areconsiderably smaller amounts than in theother water drinking tests except those ofSplaingard et al,8 the method is safer and couldalso be used for the patients with overt dys-phagia. Both sensitivity and specificity of thismethod are very high (100% specific and95-4% sensitive), and the dysphagia limitswere below 20 ml in all but three of 66patients with overt dysphagia or suspecteddysphagia in whom clinical longitudinal stud-ies showed the problem of dysphagia becom-ing overt. On the other hand; clinically normalpatients without dysphagia at the time ofinvestigation and normal subjects were capa-ble of drinking an amount of 20 ml or more.As a result; the clinical/electrophysiologicalmethod of "dysphagia limit" can be a rapid,specific and sensitive test for diagnosingoropharyngeal dysphagia with neurogenicorigin.What is the mechanism for piecemeal deg-

lutition and dysphagia limits? It is well knownthat when oropharyngeal swallowing isimpaired but compensated, such patientscould change their eating habits-that is,frequent small meals make eating easier, andthe patient may reduce the individual bolus

size. Swallowing for a second time with eachbolus helps to clear retained material from thepharynx.'5 Besides the voluntary compensa-tions for impaired swallowing of which thepatient may be aware, the compensation isalso "involuntary"-that is, it takes placethrough adjustments in the swallowing appara-tus itself.'5 Thus patients with a subclinicalswallowing impairment may subconsciouslyalter the consistency of ingested food and thespeed of eating and drinking and there may beno overt symptoms of dysphagia. 16

Occasionally, abnormal deglutition occursphysiologically even in healthy young adults.'7Indeed, most of our normal control subjectscould not easily tolerate more than 20 mlwater. Above their tolerance level they swal-lowed twice but successively. Therefore theremust be a physiological limit for the volume ofeach swallow. It has been reported that a nor-mal single swallow of water for an adult aver-ages about 17 ml, varying from 14 ml forwomen to 21 ml for men.'8 These results arevery close to our upper limit of 20 ml for eachswallow in both sexes of normal adults.A high density of mechanical or chemical

receptors implicates the tongue as the mainsensory region for determining the size of thebolus.'920 This kind of sensation in the tongueand the other tissues around the entrance ofthe pharynx could be important for piecemealdeglutition because the entrance of theoropharyngeal region can cause an adjustmentin the neural mechanism according to the sizeof bolus, dividing it into two pieces. Thus theperipheral determinants of bolus size couldgive rise to a very important fast peripheralfeedback mechanism that would affect thecentral motor programme of swallowing in thebrainstem.

This opinion is supported by the SM-EMG, which did not usually change in shapeor size as piecemeal deglutition occurred.However, this proposed mechanism probablycould not operate in the case of purely muscu-lar disorders with dysphagia, because therewere no known abnormalities related to oralsensation in these patients. They may not havehad a strong capability to keep or to drive thebolus in one portion, even in small sizes; there-fore, some escaped bolus pieces could stay inoral or pharyngeal spaces and be swallowedinvoluntarily some considerable time after thefirst swallow. Therefore, the successivelyoccurring two or more swallows for one boluswould have longer intervals in cases of oropha-ryngeal dysphagia.The swallowing centre is defined as a group

of neurons the coordinated action of whichproduces a stereotyped response. Three prop-erties exist for the functional centre.20

(1) The neurons of the centre are triggeredinto action by a specific sensory pattern sug-gesting an afferent portal of the centre.

(2) The inherent organisation of these neu-rons reproduces the patterned responsethrough effective inhibition and excitation ofmotor neurons.

(3) The neurons of the centre have a pre-emptory command of the motor neurons that

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Page 6: Piecemeal and subjects and in - Journal of Neurology ... · piecemeal deglutition or as a sign ofdysphagia limit. In some normal subjects the amount of liquid increased up to 35 ml.

Ertekio, Ajdokdu, Yuceyar

supersedes other synaptic influences such asthe respiratory drive.

In the light of the findings of dysphagia lim-its and piecemeal deglutition the followingfacts regarding the swallowing centre and itsapparatus are important.

(1) Swallowing jitter can be adjusted fromone swallow to another according to theperipheral conditions.'

(2) Sensory feedback to the centre is onemechanism which prolongs the duration ofpharyngeal swallowing processes withincreased bolus volume. 721 21

(3) If the bolus is big enough, it is not suffi-cient to change the jitter and to increase thetime of swallowing events; instead, it becomesnecessary to divide the bolus and swallow itsuccessively in piecemeal deglutition.

(4) All these arrangements must be oper-ated by the sensory-motor integration of theswallowing centre.

(5) If there is any disturbance in the neuro-muscular or sensory-motor system of the swal-lowing apparatus, swallowing may be adaptedby modification of piecemeal deglutition andreduction of the dysphagia limit to less than 20ml bolus size.

Despite this attempt to compensate, theresidual bolus volume remaining in the spacesof the pharynx will escape either into the air-way or down through the upper oesophagealsphincter opened for a second time a consider-able interval after the first swallow.

Apart from its use in studying the physio-logical nature of piecemeal deglutition, thedysphagia limit is a very useful, reliable, andrecordable electroclinical test for patients withswallowing disorders. It can be a pragmaticcandidate for a screening test before the evalu-ation of videofluoroscopic investigations forselected patients with dysphagia.

'1'hils study xvas supported by a grant from the 'T'urkishScientific aind Technological Rcsearch Council (TUBI'AIK)project No:TBAG-U' 17- 4.

Logcman J. E l9Xl3:76tio,tad rCltttttett swalltwittg disorders.Austin T'X, Pro-cd, 1983:76.

2 Ertekin C, Aydogdu I, Yuceyar N. Dvsphagia limiiits i7l titttttalsubjects anid paticnts zwith d4ysphagia. 13th national congressof clinical neurophysiology, Istanbul, Turkey, 1995;summary book 118.

3 Ertekin C, Pehlivan M, Aydogdu I, et al/. An electrophysio-logical investigation of deglutition in man. Muscle Nerve1995;18:1 177-86.

4 Pehlivan M, Yucevar N, Ertekin C, et al. An electronic tec-niquc measuring the frequency of spontaneous swallow-ing (digital phagometer). Dysphagia 1996 (in press).

5 Dantas RO, IKern MK, Massev BT, et a!. Effect of swal-lowed bolus variables on oral and pharyngeal phases ofswallowing. Ant Y Phvysiol 1990;258:G675-8 1.

6 Nirkko AC, R6sler KM, Hess CW. Sensitivity and speci-ficitv of needle electromyography: a prospective studycomparing automated interferences pattern analysis withsingle motor unit potential analysis. E/lectroencephalogrCl/iit Neurophysiol 1995;97:1-10.

7 Ertekin C, Aydogdu I, Pehlivan M, et al. Eff?ets of bol/ts vol-itittt t)tt tihe orphat3atigeal swclloztiig: att electroplh'sitOlogiealstucdy iii ntiatt. 13th national congress of clinical neuro-physiology, Istanbul, Turkey, 1995; summary book 1 16.

8 Splaingard ML, Hutchins B, Sulton LD, Chaudri G.Aspiration in rehabilitation patients: videofluoroscopy vsbedside clinical assesment. Aelch PhYss Med Rehabil1 988;69:637 --40.

9 Linden P, Kuhlemeier 1KV, Patterson C. The probability ofcorrectly predicting subglottic penetration from clinicalobservations. Dvsplhagia 1993;8: 170-9.

1 0 Gordon C, Hewer RL, Wade DT. Dysphagia in acutestroke. BAI1y 1987;295:41 1-4.

11 Depippo KL, Holas MA, Reding MJ. Validation of the 3-ozwater swallowv test for aspiration following stroke. Altch"cbutcl 1992;49:1259--61.

12 Nathadwarawala IKM, Nicklin J, Wiles CM. A timed test ofswallowing capacity for neurological patients. Y7 NeurolN'eurtsurg Psvechiatr, 1 992;55:822 5.

13 Nilsson H, Ekberg 0, Sjoberg S, Olsson R. Pharyngealconstrictor paresis: an indicator of neurological disease?Dssphlagia 1993;8:239--43.

14 Hughes TAT, W;les CM. Clinical measurement of swal-lowing in health and in neurogenic dysphagia. Q 7 Med1996;89:109- 16.

15 Bucholz DW, Bosma JF, Donner MW. Adaptation, com-pensation and decompensation of the pharyngeal swval-low. Gastroiwtest Radi0tl 1985;10:235-9.

16 Jones B, Ravich WJ, Donner MW, Kramer SS, Hendrix'I'R. Pharyngoesophageal interrelationships: observationsand working concepts. Gatsttoinltest Racdiol 1985;10:225- 33.

17 Felson B, Klatte EC. Pharyngeal and upper esophagealdysphagia. JAMA 1976;235:2643 -6.

18 Jones DV, Work CE. Volume of a swallow. Atl .7 Dis Child1961 ;102:427.

19 Darian-Smith I. The trigeminal system. In: Iggo A, ed.HIIatdbook of senisor' phls'siOltsgy. Vol 2. New. York:Springer Verlag, 1973:271-314.

20 Miller AJ. Deglutition. Phvsiol Rev 1982;62:129--84.21 Kahrilas PJ, Iogemann JA. Volume accommodation during

swallowing. Dysphagia 1993;8:259--65.22 Kahrilas PJ, Dodds WJ, Dent J, et al. Upper esophageal

sphincter function during deglutition. Gastroewterologv1988;95:52 -62.

23 Kahrilas PJ, Lin S, Iogemann JA, et a!. Deglutitive tongueaction: volume accommodation and bolus propulsion.Gastrositetreloogj 1993;104:152--62.

24 Jacob P, Kahrilas PJ, Logemann JA, et a!. Upperesophageal sphincter opening and m)odulation duringswallowing. Gastroelttterologv 1989;97:1469-78.

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