THE AMERICAN JOURNAL OF OTOLOGY/VOLUME 5, NUMBER 5 luiy 1984

REVIEW ARTICLE

ROLE OF THE NEUROTOLOGIST IN THE DIAGNOSIS

OF BRAIN ISCHEMIA

Glen D. Dobbeti, M.D.* and Galdino E. Valvassori, M.D.i

Hindbrain problems resulting from pom

blood circulation in ihe vertebral arteries are now

well recognized. The most dramatic problems are

the deaths thai have occurred following chiroprac

tic manipulation ol the neck. Tlie.se patients de

velop a dazed state, are vertiginous with nausea, lose

vision, and have auditory tinnitus before death.

Abnormality oi' the vertebra] artery may in

clude ultima damage with clots, static or sienosed

sites ofatherosclerosis, narrowing produced by cervical spondylosis, and the heniodynainic obstruc

tion associated with rotation and extension of the

head. The hemodynamk: problem has been well

documented in cadavers by Tatlowand collc-agues!l

and DeKleyn and Versicegli.1" The same has been

vended in live patients bySheehan and others.

Neurotologists are foeusing more on vascular

ischemia, as they are seeing many of these pa

tients.1' Many patients do not have peripheral disease, such as Meniere's disease, acoustic trauma,

or a retrocochlear acoustic neuroma.

Permanent or transient reduction of blood

flow to the end-organs and to the hindbrain is the

single major anise of vestibular disorders and a

common cause of sensorineiiral hearing loss. Re

versible deafness in some patients may be due to

temporary obstruction or stasis within the capil

laries in the stria vascularis, which produces stria!

hypoxia, resulting in a reduction in the endoiym-

phatic potential, with subsequent hearing loss.Bailey and associates have shown reversal of

netnosensory hearing loss, most probably by im

proved circulation or collateral supply to the stria

vasciilaris. The vascular anatomy and territories of

circulation in these areas are well demonstrated

bin not necessarily understood.1!'---

1 his paper reviews the methods of assessing

the hindbrain (or target site) circulation so revaacu-

lar bypass surgery or medical treatment may be

planned. Vertebral artery surgery for vascular im

provement of the hindbrain is available in someneurovascular centers, Carney has done over 102

cases in 1981 and Keifferof Paris over 60 cases.

J With the training of more neurovascular surgeons this procedure will he available at more clin

ical sites. The role of neuroiologic studies in iden

tifying suspected early hindbrain ischemia U also

discussed.

The methods of assessing the target circulation

of the brain have included isotope studies and

dynamic computed tomography (CT) studies with

xenon and iodinated contrast. In the future, nu

clear magnetic resonance (NMR) flow analysis may

be the method of choice.

The cerebral radionuclide angiogram (CRAG)

isotope includes multiple rapid images of the brainand neck in a frontal projection. The images of

the neck show both arterial and venous structuresthat can be confusing to interpret. The supraten-

torial detail shows the anterior and middle cerebralvessels. The posterior fossa or hindbrain and the

vertebral arteries cannot be evaluated by the

technique, since the overlapping neck, scalp musculature, and blood supply obscure useful informa

tion. In addition to the noise of this technique, itgives no brain tissue information regarding flow.

The "flip-flop'1 image of middle cerebral arterystenosis and delayed collateral circulation over the

brain to supply the depleted territory is well recog

nized and indicative of this single vessel anomaly.

I his. however, is not a common isotope diagnosis.Buell and coworkers:1:' have shown recently

•Professor, Departments <>f Radiology and Neurosurgery, University of Illinois Sdmnl of Medicine,Chicago, Illinois

tProfessor, Departments of Radiology and Qtolaryngology, University of Illinois School of Medicine,Chicago, Illinois

Reprini requests: Department <>i Radiology, University ol Illinois sdiool ol Medicine, Chicago, 1LB06ia (Dr. !)bb)

Publisher: Thieme-Stratton Inc.. :iHl Park Avenue South, New York. XV 10016 397

THE AMERICAN JOURNAL OF OTOLOGY/VOLUME 5, NUMBER 5 luly 1984

that the diagnostic accuracy of detecting supraten-

torial blood flow alternations is improved by

CRAG, if combined with carotid artery directional

Doppler sonography. Thus, vascular changes in

either the extracranial carotid vessels or supraten-

torial vessels are assessed and produce a diagnostic

sensitivity of 93.3 percent.

Lassen and Ingvar34 in 1961 first used inertradioactive gas to measure regional blood flow.

Intravascular radioactive xenon studies, although

laborious and costly, when done for the total brain

are useful in defining territories that need revas-

cularization. For clinical regional cerebral blood

flow studies, the133 xenon intracarotid injection

method has been used abundantly, and several

hundred papers have been published from many

centers. This method has not been readily accepted

because of the need for an invasive injection of

the carotid artery.

The CT dynamic scan has been used with in

halation of inert xenon gas to saturate the brain

and subsequently follow its washout from the brain

after stopping the breathing of this gas. This

technique has produced quantitative brain flow

measurement. With proper patient monitoring,

this study shows great possibility. The application

of the CT scanner and inhalation studies has been

best applied by Meyer and colleagues.'5"45 Afterinhalation, xenon diffuses rapidly from the lungs

into the arterial blood and brain tissue. The gas

acts as a tracer that can be measured as it diffuses

through tissue. The resulting changes in CT units

have been used for measurements of local cerebral

blood flow. Stable xenon is lipid soluble; hence, it

is more soluble in white matter than in grey matter.

In pathologic stales such as brain edema, infarc

tion, gliosis, and tumor, local tissue solubility is

altered. These abnormal changes in tissue solubility

may therefore be measured by CT scanning during

xenon inhalation.

The positron emission tomography (PET) scan

is a high cost, sophisticated instrument, which re

quires an associated cyclotron to produce krypton-

77, "C-iodoantipyrine, 18F-fluoroethanol, I8F-nicotine. Experienced specialty personnel are

needed for proper operation. Using the PET scan

ner and a commercially available nondiffusible

tracer, <>8GA-EDTA, measurement of the transit

time in the brain can be made. This technique is

not a quantitative measurement of cerebral blood

flow, but is similar to the dynamic CT circulation

study. The latter, however, is less costly and does

not require a radioactive tracer. This research will

help understanding of brain circulation, but it does

not appear to be of practical clinical use.

We have the greatest personal experience with

the dynamic CT scan circulation study. l'~:><> It isthe most practical and most available technique

that only requires a rapid intravenous injection of

nonradioactive iodinaled contrast material. The

passage of the contrast through a section of the

398 brain may be plotted. To calculate the mean transit

time of tissue, such as brain, from dynamic CT

performed after a bolus injection of intravenous

contrast material, the time dependence of the con

trast material to the tissue must be "deconvolved"

from the observed time course of the tissue contrast

enhancement. If the approximate shape of the

curve of the tissue response to an instantaneous

injection of contrast material is assumed, the width

of this curve that gives the best fit to the observed

tissue response can be used to find a value for the

tissue mean transit lime. Axel/1'"'"' by applyingthis technique to dynamic CT scans of two normal

volunteers, yielded values comparable to those in

the literature for other techniques. The method

has the advantages of being simple to implement,

relatively insensitive to noise, and of acceptable

detail.34""9 The method does not require any curvefitting to correct for recirculation. Two injections

are usually needed, with one through the hindbrain

and the other through the forebrain. The sections

give good representative data regarding circulation

to the anterior and posterior sides of the circle of

Willis. Patients who are sensitive to iodinated con

trast cannot use this method or need premedica-

tion. Another limitation is the random selection

for the level of testing which may not correspond

to the level of poor circulation.

The CT dynamic scanner offers a practical

and readily assessible circulation study to the

neurolologist. Many patients (87 percent) with

hindbrain ischemia present with the common

symptom of dizziness and visual disturbances such

as blurred or tunnel vision. Partial or complete

blindness accounts from 44 percent of cases. Our

experience shows ataxia in 32 percent, spontaneous

nystagmus in 27 percent, and sensorineural hear

ing loss in 22 percent.

In office practice, the neurologist is able to

identify patients who have problems of the hind

brain and occipital lobes. The EEC extends over

the cortical forebrain surface, but it is limited within

the hindbrain. The abnormal vestibular, brainstem,

auditory or visual office tests have to be explained.

The abnormal brainstem auditory evoked response

test records multiple reflex complex sites. Vestibu

lar testing gives a more diffuse central response.

A more complete battery of testing should be de

veloped to cover as many reflex complexes as pos

sible for a reasonable cost.

Aschan and Hugosson1'" in 1966 reported a

case of a 53-year-old woman who had ligation of

both common carotid arteries for bilateral carotid

cavernous fistulas. This was a rare "experimental"

situation in a human subject to demonstrate the

dependence upon the vertebral arteries for the

brain blood flow, and the opportunity to study the

pre- and post-operative otoneurologic conditions.

Electronystagmography before the ligation showed

no nystagmus, but neck rotation afterward pro

voked nystagmus. Positional testing without rota

tion of the neck gave no nystagmus. This shows

the importance of studing the hemodynamic

REVIEW ARTICLE/Dobben, Valvassori

changes about the circle of Willis. These

pathophysiologic changes are not usually studied

when doing vertebral angiography and are often

missed.

In 1979, Causse and Caussefil emphasized theimportance of nystagmography to elicit subclavical

vertebrobasilar insufficiency and poor cochleoves-

tibular vascularization. This is based upon the fact

that inequality in the vascularization of the balance

mechanism, the two posterior labyrinths, can creat

a nystagmus well in advance of the appearance of

dizziness, deafness, orbrainstem neurologic signs.

Today, a separation of central6"63 fromperipheral abnormalities is usually quite easy. Cen

tral lesions or tumors can be excluded with high

definition CT studies. In 1981 Kumar64 further

defined the value of vestibular decruitment studies

to determine "peripheral" or "central" lesions. In

an analysis of 139 cases where vestibular decruit

ment was recorded, Torok6o(5(i found 105 patientswith central or intracranial disorders. Most of the

cases showed normal neurologic and conventional

radiologic studies. Out of 72 consecutive cases with

central vestibular findings, 66 had intracranial

anomalies. Thus, the combination of electronystag-

mographic studies and CT dynamic circulation

studies produced a diagnostic verification of 92

percent.

CASE REPORTS OF HINDBRAIN ISCHEMIA

Subclavian Artery Steal Syndrome

Case one: A 55-year-old female presented

with a chief complaint of persistent vertigo since

revision of a stapedectomy. No semicircular canal

fistula or middle ear disease was evident. The ver

tigo remained undiagnosed for eight years. A CT

circulation study demonstrated normal tissue mean

transit times over the anterior aspect of the sup-

ratentorial sections and delay times over the occip

ital lobes and the infratentorial areas (Fig. 1). This

was consistent with poor circulation to areas

supplied by the vertebral arteries.

An aortic arch angiogram demonstrated com

plete occlusion of the left subclavian artery. When

the right vertebral artery was injected, the contrast

descended into the left vertebral artery to fill the

left subclavian artery beyond the occlusion. This

subclavian steal was surgically treated with a subcla

vian bypass graft. This corrected the patient's ver

tigo (Fig. 2).

Carotid-Vertebral Artery Disease

Case two: A 55-year-old male was seen for a

sudden onset of left-sided sensorineural hearing

Figure 1. Case one: Pre-

operative CT dynamic section

of the posterior fossa of 9-11-

81. The graph shows symmetri

cal areas of the posterior cere

bellum which demonstrate a

delayed tissue transit time of 22

and 24 seconds. The normal

time is 16 seconds. 399

THE AMERICAN JOURNAL OF OTOLOGY/VOLUME 5, NUMBER 5 luly 1984

Figure 2. Case one: Post

operative CT dynamic section

of the posterior fossa of 9-29-81

after surgical correction of the

subclavian artery steal. The

graph shows the symmetrical

areas of the posterior cerebel

lum and a normal tissue transit

time of 16 seconds.

loss and tinnitus. The patient had no other symp

toms or vestilmlar abnormalities.

The audiogram showed a pure tone within

normal limits in the right ear through 2000 Hz,

and dropped sharply to a severe high frequency

hearing loss with a notched configuration. The

poorest threshold was at 4000 Hz. The speech

reception threshold was in good agreement with

the pure tone findings. The left ear demonstrated

a relatively flat sensorineural hearing loss (Fig. 3).

Speech awareness threshold was in agreement with

the pure tone findings.

Polytomographs of the inner ears showed par

tial obliteration of the left vestibular aqueduct. The

cochlear capsules were normal. A CT dynamic

study showed delayed circulation along the left

side of the fourth ventricle, and the remaining

areas were normal (Fig. 4).

Because of the CT dynamic study, a four-vessel

neck and brain angiogram was obtained. This dem

onstrated a left internal carotid artery narrowing

to about 50 percent of its normal diameter. No

left vertebral artery was found except that distal

portion at the level of Cl. This remained open by

supply from collateral muscular branches (Fig. 5A).

The patient was treated with left carotid artery

endarterectomy and vein patch angioplasty. A left

common carotid artery to distal left vertebral artery

bypass was performed from the vein patch angio

plasty to the vertebral artery with an isolated vein

segment from the left thigh (Fig. 5B).

The sensorineural hearing loss remained un

changed; however, the tinnitus disappeared. The

400 patient was grateful for the relief of the tinnitus.

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250 500 1.000 2,000 4.000 8.000

Frequency in Hz _— ^ Boner.—-c-Right

Conductions—3-LeftAir Conduction

Figure 3. Case two: Pure tone audiogram of the right

ear (o) is normal through 2000 Hz and drops sharply for

a severe high frequency hearing loss. The left ear (X) dem

onstrated a flat, moderate to severe sensorineural hearing

loss.

REVIEW ARTICLE/Dobben, Valvassori

Figure 4. Case two: A CT

dynamic section of the post

erior fossa with comparison of

areas. The right side (white box)

numbers one and two show a

normal tissue transit time of 16

seconds. The left side (no box)

show a tissue transit time delay

of 20 seconds. This is consis

tent with a unilateral hindbrain

circulation problem.

B

Figure 5. Case two: A, Composite lateral drawing of

the left carotid angiogram and left subclavian angiogram.

The internal carotid artery is narrowed to about 50 percent

of its normal diameter by arteriosclerotic plaque formation.

The left vertebral artery is occluded except for the distal

Cl segment which remains open by collateral ascending

cervical vascular blood supply. B, Drawing of neurovascu-

lar operative procedure of the left carotid artery endarterec-

tomy and a vein patch angioplasty. A left distal vertebral

artery bypass vein graft was added to this.401

THE AMERICAN JOURNAL OF OTOLOGY/VOLUME 5, NUMBER 5 July 1984

Vertebral Artery Bypass Surgery

Case three: A 67-year-old woman complained

of a "floating" sensation of several weeks duration

whenever she stood up. The symptoms progressed

and eventually she was unable to walk without sup

port. She had no complaints of hearing loss; how

ever, a pure tone audiogram showed a symmetrical,

high frequency sensorineural hearing loss of mild

to moderate severity (Fig. 6).

The vestibular caloric test showed bilateral

type II decruitment (Fig. 7). She had a positive

Romberg test. The standard CT scan was normal,

although the circulation study indicated verte-

brobasilar insufficiency (Fig. 8). The angiogram

showed an obstructed right internal carotid, left

vertebral, and left subclavian arteries.

The surgical reconstruction of the right inter

nal carotid artery and the left vertebral artery was

done. The left subclavian artery was decompressed.

Two months following surgery, the patient was

asymptomatic.

Diagnosis Of Hindbrain Disorders

Case four: A 65-year-old male presented with

"dizziness" for several weeks and a feeling of being

"light-headed". The symptoms were aggravated by

movement. He had a known cardiac arrhythmia.

A noninvasive evaluation with auditory evoked

brainsteni potentials showed the absolute latency

of wave V to be normal for the right ear and

prolonged for the left. Also, there was a prolonged

III to V inlerpeak latency consistent with an abnor

mal upper auditory brainsteni pathway dysfunction

for the left side (Fig. 9).

The CT circulation study confirmed delayed

circulation about the left paraventricular area

within the posterior fossa (Fig. 10).

The patient remains under treatment with

beta-blocker medications to correct the cardiac ar

rhythmia and improve the stroke output of the

heart. The patient is asymptomatic.

CONCLUSION

With the technological advances in the tools

of the neurotologist to assess the reflex responses

of the hindbrain, early ischemic changes are more

easily detected. Whenever an abnormal vestibular,

brainsteni, auditory, or visual evoked response po

tential study is not specific for a definite condition,

hindbrain ischemia should be considered.

The present noninvasive CT dynamic circula

tion studies are an effective way to include or

CALORIC TEST RIGHT

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250 500 1,000 2,000 4,000Frequency in Hz

8,000

Air Conduction

Figure 6. Case three: Although the patient had com

plaints of a hearing loss, a pure tone audiogram showed

a symmetrical high frequency, mild to moderate sen-

402 sorineural hearing loss.

y/^Ay^^^^

I 12 ' 11 I1 CULMINATION: 23 '

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Figure 7. Case three: The vestibular caloric test

showed a bilateral type II decruitment. (Reprinted with

permission from Kumar A: Reliability of central vestibular

signs in identification of posterior fossa pathology, Ad

vances in Neurology, Volume 30, Raven Press, 1981.)

REVIEW ARTICLE/Dobben, Valvassori

Figure 8. Case three: The

CT dynamic posterior fossa

study shows a normal tissue

transit time; however, the

peaks of the area about the

fourth ventricle are depressed

(C2, C12). This is indicative of

hindbrain poor circulation.

ULVTAl LEFT RIGHT

Figure 9. Case four:

Brainstem auditory evoked re

sponse showed the absolute la

tency of wave V to be normal

for the right ear and prolonged

for the left. A prolonged III to

V interpeak is consistent with

an abnormal upper auditory

brainstem pathway dysfunction

for the left side.

A3

B2

A1

III

MSEC 403

THE AMERICAN JOURNAL OF OTOLOGY/VOLUME 5, NUMBER 5 luly 1984

Figure 10. Case four: CT

dynamic graphs of the posteriorfossa, Graph A is an area to the

left of the 4th ventricle andshows a delay in tissue transittime of 26 seconds. Graph B is

the normal transit time of the

basilar artery of 14 seconds.Graph C is the normal transit

time of a cortical vermian vein

of 22 seconds. These graphs

demonstrate a focal area of

poor circulation in the posterior

fossa.

404

exclude ischemia of the hindbrain. If these studies

are positive for a circulation problem, then it is

necessary to decide if medical or surgical treatmentis needed.

If carotid-vertebral bypass surgery is needed,an invasive angiogram will be done to plan thesurgical approach.

NMR ' scanning may play an added role for

hindbrain ischemic problems. It produces imageswithout the use of radiation or injected contrast

materials. The images are the result of magnetic

movement of hydrogen nuclei, which emit specific

energies from their location in the section of thebody being studied.

This technology permits measurement ofblood flow in vessels. When high magnetic fields

are used, tissue chemical spectroscopy in vivo ispossible.

NMR will be an added important testing tool

to analyze the circulation problems of the brainand heart.

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We express our appreciation for the advice and

clinical information made available by Drs. A. Carney,

C. Hart, J. Hughes, A. Kumar, and J. Stopka. The prep

aration of the text was the work of Patricia C. Zelenka.

406