大韓放용↑線흩§學會픔 第 26 卷 第 4 號 pp. 672 - 681, 1990 Journal of Korean Radiolog ica l Society. 26(4) 672 - 681 , 1990

Aspiration in Cerebrovascular Accident Patients: Videofluoroscopic Findings

Suk Hyun Joo , M.D. , Tae Sub Chung, M.D. , Jung Ho Suh, M.D. ,

Dong Ik Kim , M.D. , Il Seng Choi , M.D. *, Myung Sik Lee , M.D. * Department o[ Diagnostic Radiology, Yonsei University, College o[ Medicine

〈국문초록〉

뇌졸증 환자의 기도훔입 :

Videofluoroscopy 소견

연세 대 학교 의과대학 진단방사선과학교실

주 석 현 ·정 태 섭 ·서 정 호·김 동 익 ·최 일 생*이 명 식*

흡인성 폐렴은 뇌 졸증 환자에서 심각한 병발층으로 흔히 발생하며， 반복발생 하게되면 이로 인

한 치료기간의 연장， 사망률의 증가를 초래할 수 있다. 따라서 뇌졸증의 장기적인 치료대책으로

흡입성 폐렴의 발생기전， 정도를 미 리 파악하여야만 적절한 장기치료방침을 세울 수 있을 것으로

사료된다. 이에 저자들은 1988년 1 2월에서 1 989년 2월까지 본 의료원에 입원 가료중인 20'정의 뇌

졸증 환자들에서 회복기에 videofl uo roscopy를 이용하여 barium 현탁액을 삼킬 때 정면 ， 측면을

촬영하므로서 기도 흡입의 정도， 양상 ， 기전을 연구하고자 하였다.

1 ) 흡입 의 빈도와 강도

a ) 2명의 Wallenberg 증후군 환자와 가구연수 마비 ( pseudobulbar palsy ) 환자에서는 중퉁도

이상의 심한 기도 흡입을 보였다.

b ) 6명의 소와뇌경색 ( lacun a r in farctio n ) 환자들 중 1 명만이 흡입을 보였으며 그 환자의 흡입

의 정도는 경도였다.

c ) 3명의 기저핵 경색증 환자들과 4명의 중뇌동맥 영역 경색증 환자들이 경도에서 중증도에

이르기까지 다양한 흡입양상을 보였다.

2) 흡입의 시 기는 연하의 후기 구강기에서 후기 식도기 사이에 어 디서나 일어날 수 있었으나 중증

도의 흡입은 후기 구강기와 후기 식도기에서만 나타났다.

3 ) 흡입 의 기전은 주로 후기 구강기에서는 혀 운동의 감소 ( 3/ 11 ) 와 연하 반사지연 ( 3/ 11 ) 에 의해

일어났으며， 후두기에서는 후두개의 불완전 폐쇄 (8/ 11 ) , 후두개의 편측운동 ( 9/11 ) , 후두개

고정 (1 /11 ) , 그리고 초기 식도기에서는 후두개골( vall ecu lae ) 과 이 상동 ( pyriform sinus l 에 서

• 연세 대 학교 의과대 학 신경과학교실

• Department o[ Neurology, Yonsei University , Col1ege o[ Medicine 본 논문은 1 989년도 연세대학교 의과대학 교수연구비 보조로 이루어 졌음.

이 논문은 1 990년 5월 22일 접수하여 1990년 7월 23일에 채택되었음. … “

- Suk Hyun Joo. el al. Aspi ration in Cerebrovascul ar Acc ident Pali ents: Vid eo fl uoroscopic Findings -

음식이 넘쳐서 흡입 이 이루어졌으나(2/ 11 ) 모든 환자에 서는 복합적인 기 전에 의해서 발생되었

다.

4 ) 11 명의 흡입 환자중 9명이 l 단계 설골운동을， 2명이 2 단계 설골운동을 보여서 설골운동이

흡입의 간접적 증거로 사용할 수는 있으나， 정확한 흡입의 역동적 평가는 video fl uoroscopy로

만 가능하였다.

위의 결과들을 종합하여 저 자들은 뇌 졸중 환자들에 서 의 vid eofluoroscopy를 이 용한 역동적 검

사를 시행 함으로써 흡입의 빈도， 기전을 알 수가 있어 ， 흡입의 위험도가 높은 환자들을 선별하여

예방적 치 료 방침 설정 에 큰 도움이 될 것으로 사료된 다.

Index Words: Brain , infarction(l 3. 78 1. 14.781)

Brain , hemorrhage(l 3.782 , 14.781)

Larynx , rad iography(27.1299)

Introduction

One of the complications frequently dealt in

cerebrovascular accident(CVA) patients was

pneumonia caused by aspiration. According to

Arms et al. , the most common cause of aspira­

tion pneumonia was impaired conciousness

(70%). especially vascular disorders 1). Also Hor­

ner et a l. stated that among the stroke patients

about 51 % suffered from aspiration of oral con­

tents during swallowing , and that about 54% of

these patients had silent aspiration2). Veis and

Logemann stated that most of their CVA pa tients

encountered deglutition problems most frequen­

tly during the pharyngeal phase of the swallo­

wing process . They also stated that the most ap­

propriate and accurate method of evaluating the­

se problems was video f1uoroscopy3J. The purpose

of our study was to select high risk group of sil­

ent aspiration among the cerebrovascular acci­

dent patients , thus preventing major pulmonary

complications during long term follow-up . Also to

evaluate the mechanism of aspiration such that

the clinicians can provide better preventive mea

sure for these patients.

Subjects and Methods

Twenty CVA patients admitted to the Yonsei

Medical Center during December 1988 through

February 1989 were involved in our study. All

the patients were in their recovery phase. The

male to female ratio was 11 to 9 and their ages

ranged from 33 to 76 years. There were two

cases of Wallenberg syndrome , one pseudobulbar

palsy, six lacunar infarction , one thalamic in

farction , seven middle cerebral artery(MCA) terri

tory infarction , and three basal ganglia infarc­

tion .

Video f1uoroscopy was performed using the U­

matic videorecorder capable of performing 30

frames-잉ec ， while the patients swallowed the

barium sulfate suspension in both AP and lateral

positions. The items observed were degree and

onset of aspiration , tongue motion , swallowing

re f1ex , and epiglottic motions. Cough re f1 ex and

the hyoid bone motion were also evaluated with

the idea that they might provide indirect in­

formation about the possible existance of aspira

tion. The hyoid bone motion was evaluated for

eith er one-step or two-step hyo id bone motion4J

We defined the degree of aspi ration as 1) mild

degree of aspirat ion when the bolus was not

blocked by the epiglottis , but was effectively

견

( h U

大韓放M綠흩융등섣會등f . 第 26 환 第 4 號 1990

blocked by the true and false vacal cord .

2)moderate when the bolus was initially blocked

by the vocal cords during the pharyngeal phase

of swallowing , but afterward the bolus passed

through the airway during the esophageal

phase. 3) severe when the epiglottis , true and

false vocal cords could not act as an effective bar­

rier at all. The onset of aspiration was divided

into the late oral phase , the pharyngeal

phase(early, middle , late) , and the late

esophageal phase.

Items such as reduced tongue motion , swal

lowing reflex(normal is less than 1 second) , and

epiglottic motion were evaluated as the possible

mechanism of aspiration in these CVA patients.

The epiglottic motion was further divided into

unilateral motion , incomplete closure , fixed epig

lottis , and finally normal epiglottic motion. Also

the overflow of residual barium sulfate suspen

sion from the two pharyngeal process(the valle­

culae and the pyriform sinuses) into the larynx

was studied , because th ey also caused aspiration

in CVA patients.

Results

berg syndrome(two cases) , pseudobulbar pal­

sy(one case ), and the basal ganglia infarction­

(three cases) had laryngeal aspiration. There

were six cases with lacunar infarction in our

study , but only one case had aspiration detected

in our study. Among the seven cases of MCA

territory infarction , four cases showed aspira­

tion. There was one case of thalamic infarction

but no aspiration detected.

There were three cases with mild degree of

aspiration , four cases with moderate degree , and

four cases with severe degree of aspiration

among the total of 11 patients(Table 1). Mild to

moderate degree of aspiration usually happened

during the pharyngeal phase of swallowing.

However, severe degree of aspiration occurred be­

fore or after the pharyngeal phase except for one

patient. He aspirated in two steps , a minimal

amount in the early pharyngeal phase and main

aspiration due to overflow from the pyriform

sinus in the late esophageal phase.

The two cases of Wallenberg syndrome all de­

veloped severe degree of aspiration(Fig. 1). The

case of pseudobulabar palsy had moderate degree

(Fig.2 ), and the lacunar infarction case had mild

degree of aspiration. MCA territory and basal

1. Dise ase and aspirat ion ganglia infarction cases had even distribution

among the three degrees of aspiration(Table 2)

A total of 20 cases were involved in our study The onset of aspiration occurred either from

with six different entities of CVA manifesta- the late oral phase, the pharyngeal phase or the

tions(Table 1) . Among them 11 cases had late esophageal phase of swallowing. The aspira-

laryngeal aspiration. All the patients with Wallen- tion occurring after the pharγngeal phase due t。

Table 1. Lesion Descriptions

Lesion aspiration TotaVAspiration Degree

Mild h‘oderate Severe

Wallenberg syndrome 2 / 2 0 o 2 Pasudobular p외sy 1 / 1 0 l 0 Lacunar infarction 6 / 1 o o Thalamic infarction 1 / 0

MCA territory infarction 7 / 4 2 8asal ganglia infarction 3 / 3

- 674 -

- Suk Hyu n J o。‘ et al. . Aspirat ion in Cerebrovascular Acciden t Pati ents: Videofl uoroscopic Find ings

a b

c

overflowing from the pyriform sinus or the valle­

culae were seen in the cases with Wallenberg

syndrome. The pseudobulabar palsy case had its

aspiration starting in the oral phase of swallow­

ing and ending in the ear1y stage of the phary-

Fig. 1. This Wallenberg syndrome case showed normal CT scan fin dings( a ) and severe degree of as­piration into the trachea( b) due to fixed epiglottis(a rrow)(IC) and over­flow of contrast media from pyri­form sinus on videofluoroscopy(ar­row h eads lCd).

ngeal phase. In the patient with lacunar infarc­

tion , the aspiration occurred during the mid­

stage of the pharyngeal phase. The MCA territory

infarction caSes had aspiration mainly occurring

in the early or mid-stage of the pharyngeal

Table 2. Relationship Between Degree of Aspirition and Onset of Aspiration during Swallowing

Onset Late Pharyngeal phase Late oral esopphhaasgeeal

Degree \\ phase Early Middle Late

Mild O 3 o O o Modera te l l 2 0 0

Severe 2 o 0 0 2

- 675

- 大韓放射線醫學會픔 : 第 26 卷 第 4 號 1990 -

c

phase. but one case had its onset in the oral

phase of the swallowing. The basal ganglia in­

farction cases all had aspiration happening dur­

ing the early or mid-stage pharyngeal phase.

2. Mechanism of aspiration

There were three cases of aspiration due to de­

layed swallowing re f1ex and three cases due to

reduced tongue motion. As for the aspiration

due to abnormal epiglottic motion . there were

nine cases of unilateral motion of epiglotis. eight

incomplete closure of epiglottis. two fixed epiglot­

tiS. and one case of normal epiglottic motion

Also there was one case of b arium sulfate sus­

pension overf1owing from the pyriform sinus and

another where the barium overf1owed from the

valleculae(Table 3) .

The Wallenberg syndrome cases aspirated due

to combined effect of incomplete closure or un­

ilateral motion of epiglottis and overf1ow of the

barium sulfate solution from the pyriform sinus

or the valleculae . Aspiration of the pseudobulbar

palsy case occurred due to combination of de­

layed swallowing re f1ex and the reduced tongue

motion. The aspiration in the lacunar infarction

Fig. 2. A pseudobulbar palsy case with multiple infarction of the pons(arrow)(a) and left basal gan ­glia(arrow)(b). On videoDuoroscopy moderate degree of aspirtaion is demonstrated(c~ )

case was due to abnormal epiglottic motion(in­

complete closure and unilateral m ‘Jtion of epig­

lottis with some contribution from abnormalities

of the oral phase such as delayed swallowing re­

f1ex and tongue base weakness(Table 4)(Fig. 4).

Table 3. Analysis of Complex of Aspiration

Mechanism

Mechanism No. of cases

Late oral phase : 6

a . Delayed swallowing reDex- 3

b. Reduced tongue motion-- 3

Pharyngeal phase : 20

a . Unilateral motion of epiglot tis 9

b. Incomplete c10sure of epiglottis 8

c. Fixed epiglottis 2

d. Normal epiglottic motion

Late esophageal phase : OverDow."

2

2

• :Normal is less than 1 second •• :Reduction of tongue control during the oral phase ••• :Over f1ow of barium from pyriform sinus or vale­cullae

% ” h U

Aspiration in Cerebrovascul ar Accident Pat ients: Videoflu oroscopic Findings Suk Hyun Joo ‘ et al

Table 4. Relationship Between CVA Lesions and Mechanism of Aspiration

LEP

OF

PP

ICE

LOP

FE

Wallenberg syndrome

Pseudobulbar palsy

Lacunar infarction

MCA territory infarction

Basal ganglia infarction

qι nv

nu

nu

nu

1i

nu

nu

--nU

1

。

1

3

2

UME l

o l

3

2

RTM O

l

o --

DSR nU

1A

nu

-i nU

Lesion

LOP: Late oral phase. PP: Pharyngeal phase. LEP: Late esophageal phase QSR : Delayed swallowing reflex , RTM: Reduced tongue motion ,

UME : Unilateral motion of epiglottis. ICE : Incomplete closure of epiglottis , FE: Fixed epiglottis , OF : Overflow of barium from pyriform sinus or valleculae

Fig. 3. Unilateral motion of epi­glottis(open arrows)(a) and incom plete closure of epiglottis(b) is de­monstrated in this lacunar infar­ction case. Smal amount of con­trast media is seen in the un der-surface of the epiglottis(ar­row).

j녘 l 』‘­a

Table 5. Other Indicators of Aspiration 3. Other indicator of aspiration

Aspirtion( - )

Cough Reflex

(+)

(-)

Hyoid bone motion

One-step motion'

Two-step motion"

Not

Evaluated

O

9

Aspiration( +)

4‘

[/

9

2

lndic2tor Of the 11 cases with aspiration. only four

cases had cough reflex initiated. The patients

without aspiration were not studied for the pre­

sence of cough rellex. Nine cases with aspiration

demonstrated one step hyoid bone motion and

two cases had two step hyoid bone motion. AlI

the nine cases without aspiration displayed two

step hyoid bone motion(Table 5).

• :Movemont of the hyoid bone in the anteriocarinal direction only ‘

.. :Movement of the hyoid bone initially in the post­eriocarinal direction followed by anterior direction displacement

- 677-

the ln

Discussion

processed mainly 15 Deglutition

-j;:韓放射線훌§學會픔 : 第 26 卷 第 4 號 1990

a

b Fig. 4. MCA infarction case illustrating contrast media dripping into the trachea during the late oral phase before the swa110wing reflex is activa ted due to reduced tongue motion(arrow)(Al . But no con­trast media is seen passing into the trachea through laryI1X during pharyngea1 phase(Bl .

oral cavity to the esophagus through th e

oropharynx and the hypopharynx. The swallow­

ing can be divided into oral, pharγngeal ， and

esophageal phases. The oral and the pharyngeal

phases are voluntary processes. But the

esophageal phase in an involuntary process 5.61

During the late oral and the pharyngeal

phases , the larynx is closed to prevent penetra­

tion of food material into the airway. This is

achieved in consecutive steps. first , the leaf of

the epiglottis is tilted backward by the elevation

of the laI)πlX and the hyoid bone. Second , the

backward and rocking motion of the arytenoid

cartilage closes the glottis and narrows the vesti­

bule. Third , the cricothyroid visor is opened to

allow arytenoid to tilt further forward . Fourth,

the thyrohyoid approximation a llows buldging

backward of the vestibular portion of the epiglot­

tis allowing the obliteration of the vestibular cav­

ity. Finally the leaf of the epiglottis is turned

downward71 . These suggest that the above men­

tioned action of the pharynx and the laI)πlX is a

rapid process happening simultaneously and not

seperately. 81 Because , as the tongue is backward­

ly elevated to push the bulous back, the swallow­

ing re f1ex is activated when the bulous reaches

the anterior faucial arch. At that time , the larynx

is elevated and laryngeal closure begins91 . This is

possible through the coordination of the muscles

and cranial nerves suppling the pharynx and the

larynx(Fig. 5). They are intum indirectly con­

nected to the cerebral cortex by various conduct­

ing pathways such as corticobulbar and tectobul­

bar tracts 1 이 • Therefore any pathology involving

the brain and the brain stem can affect t h e

pharyngeal and laryngeal function , especially the

orpharγnx and the hypopharγnx. The pharyngo- cerebrovascular disease which is associated with

laryngeal junction is located within the neuronal death .

hypopharynx. The process of deglutition is a very Veis and Logemann , Lazarus and Logemann

compound and synchronized motion. A total of studied swallowing defects in CVA and closed

26 muscles and six cranial nerves a re involved in head trauma patients. They found that all

this process of transportation of food from the aspiration occurred during the pharyngeal phase

- 678 -

Suk Hyun Joo . el al. : Aspiralio n in Cerebrovascul ar Accidenl Palienls Videofluoroscopic F indings -

Fig. 5. Schematic illustrat ion of th e sequential ac­tion of the pharynx and larynx during swallowing 1 . Elevation of tongue 2. Posterior displacement of the tongue base to

pus h the bolus into the oropharynx. and the activation of the swallowing re f1ex.

3 . The soft palate and uvula is elevated to close th e nasopharynx

4. Larynx is elevated to narrow the vestibule. 5 and 6. Elevation of the hyoid bone in the postero­

carinal direction to lift the epiglottic base to tilt the epiglottic leaf backward. followed by anterior displacement of the hyoid bone to turn the epig­lottic leaf downward to a110w safe passage of the bolus into the esophagus

of swallowing. In these s tudies aspiration occur­

red due to complex of swallowing motility prob­

lem rather than due to any single mechanism

defect. This correlated well wi th our own study

Our patients also aspirated due to complex of

m ech a nis m defec t. lt may be due to the fact that

reduced tongu e control will delay activation of

swallowing re f1ex. also laryngeal elevation and

closure is possible only with activation of swal

lowing re f1ex. 91 But in our study. we placed our

atten s ion more on the laryngeal problems. espe­

cially th e epiglottic functions. It turned out that

the m ain problem wi th the larynx was due e ither

to incomple te closure or un ila teral motion of

ep iglottis

Lazarus and Logemann tried to define the

severity of the aspiration. According to them

mild degree of aspiration is when trace to less

than 20% of the bolus was aspirated. moderate

when 20-30% of the bolus was aspirated. and

severe when greater than 30% of the bolus

aspirated. 11 1 This criteria was subjected to great

deal of interobserver variations. Thus we used

our own m ethod of grading severity of aspiration

using the epiglottis. true and false vocal cords as

the deciding facto r. The true and false vocal

cords act as a secondary protection valves during

swallowing in normal subjects 991. Our criteria

did not deal with the actual amount of aspira­

tion. In the end. however. it correlated well with

the amount of aspiration and clinical outcome

Two of the patients suffering with severe degree

aspiration were affected by aspiration pneumo­

nia. one p atient being affected at the time of

thestudy and another patient developed pneumo­

nia one week a fter the videofluoroscopiC evalua­

tion.

The onset of aspiration h a d relationship with

the severity of aspiration. Aspirations had its

onset anywhere between the late oral phase and

the late esophageal phase. But patients with se­

vere degree of aspiration aspirated either late in

the late oral phase or in the late esophageal

phase. or both. At which time n either epiglottis

nor the true and false vocal cord could act as a

protection valve. They included two Wallenberg

syndrome patients. one MCA infarction patient.

and one basal ganglia infarction p a tien t. Wh ile

the patients with mild and moderate degree of

aspiration occurred during the pharyngeal

phase. Pseudobulbar palsy p a tient. 12.cunar in­

fa rction patient . three MCA infa rction patients.

and two basal ganglia pa tients fell into this

category. This su ggest that the aspiration of CVA

patients are related to various conducting path­

ways and the nucleus of the cranial nerves with

in the brain stem involved

- 679-

大歸放캉H훌옆융걷용會~. : 第 26 卷 第 4 號 1990 -

Many authors said that video f1uoroscopic

study of both the pharynx and the larynx was

the only diagnostic modality that could accurate­

ly evaluate the dynamics of swallowing

abnormalities3.1 1. 12J , and that cough and gag re­

f1ex were unreliable indicator of aspiration due to

presence of silent aspiration 2.1 3.1 4’. We also had

seven patients out of 11 who aspirated , but did

not cough. This implies that cough and gag re­

f1ex are unreliable indicator of laryngeal aspira­

tion. Only the dynamic video f1uoroscopic study

of the pharynx and larynx could accurately evalu

ate the degree and mechanism of aspiration

Ekberg evaluated hyoid bone motion in 50 nor­

mal volunteers and found that 40 patients(80%)

showed two-step hyoid bone motion , and only 10

patients(20%) showed one-step hyoid bone

motion 41 .1ψo-step hyoid bone motion cosists of

initial posterocarinal movement followed by

anterior displacement of the hyoid bone. The

one-step hyoid bone motion consists only of

anterocranial displacement of the hyoid bone

due to weakness of the styloglossus and stylohy­

oideus muscles. We evaluated the hyoid bone

motion in our patients to see if hyoid motion

could be used as an indirect indicator of aspira

tion. ln our study, nine out of 11 patients with

aspiration had one-step hyoid bone motion and

only two patients showed two-step hyoid bone

motion . Therefore we think that hyoid bone mo

tion could be used as an indirect indicator of

aspiration.

Conclusion

We conclude that , in CVA patients , aspiration

of food material into the respiratory tract due to

swallowing problems could be a potential hazard

with sometimes fatal outcomes. The main prob­

lem with aspiration was abnormal closure of the

larynx allowing the food material to be intro­

duced into the airways. To accurately evaluate

this problem , video f1uoroscopic study of the

pharynx and larynx during swallowing is neces­

sary. Only video f1uoroscopic examination could

provide the accurate dynamic information con­

cerning the specific swallowing problems. This

could provide valuable information to the clini­

cians when planning the aspiration prevention

therapy program to their patients. The hyoid

bone motion could be used as a warning sign of

impending aspiration problem and a scereening

method to select patients indicated for videof­

luoroscopic examination.

REFERENCES

1. Arms RA, Dines DE , Tinsman TC. Aspiration

pneumonia. Chest 1974; 65: 136-139

2. Horner J , Massey EW. Silent aspiration follow­

ing stroke. Neurology 1988 ; 38: 317-318

3. Veis SL , Logemann J A. Swallowing disorders in

persons with cerebrovascular accidents. Arch

Phys Med Rehabil 1985 ; 68: 372-375

4 . Ekberg O. The normal movement of the hyoid

bone during swallowing. Invest Radiol 1986 ; 21

: 408-410

5. Donner MW, Bosma JF, Robertson DL. Ana­

tomy and physiology of pharynx. Gastrointest

Radiol 1985 ; 10 ‘ 196-212

6. Ekberg 0 , Nylander G. Cineradiology of the

pharyngeal phase of deglutition in 250 patients

with dysphagia. Br J Radiol 1982 ; 55 : 258-262

7. Arden GM ‘ Kemp Fh. The mechanism of laηπpι

Part 11. The epiglottis and the closure of

larynx. Br J Radiol 1967 ; 94 : 299-307

8. Donner MW, Siegel CI. The evaluation of phary­

ngeal neuromuscular disorders by cinef­

luorography. AJR 1965; 94: 299-307

9. Logemann JA Evaluation and treatment of

swallowing disorders. 1st ed. San Diego: Col­

lege-Hill , 1983: 9-125

10. deGroot J , Chusid JG. Correlative neuroana­

tomy. 12th ed. East Norwalk: Appleton and

Lange , 1988 ‘ 113-209

11. Lazarus C, Logemann JA. Swallowing disorders

m w

- S uk Hyun j oo , et a l. Aspirat ion in Cerebrovascul ar Accide nt Patients: Videofluoroscop ic Fi ndings

in closed h ead trauma patients. Arch Phys Med following s troke: Clinical correlates and out-

Reh abil 1987 ; 68: 79-84 com e. Neurology 1988; 38: 1359- 1362

12. Curtis DJ , Hudson T . La ryngotrachea l aspira- 14. Linden P, Siebens AA. Dysph agia: Predicting

tion: Analys is of specific n euromuscula r fac- laryngeal p en etration. Arch Phys Med Reh abil

tors. Radiology 1983 ; 149 : 517-522 1983 ; 64: 281-284

13 . Horner J , Massey EW, Ris ki J E et a l. As piration

- 681 -