VOL.

123,

No.

2

RADIOISOTOPE

SCINTIGRAPHY

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OF THOMAS

By

BARRETT’S

H.

BERQUIST,

STEPHENS,

NICHOLAS

and

HARLEY

ROCHESTER,

I

1950, Barrett2 first described a condition in which the lower esophagus was lined with columnar epithelium resembling that of the stomach, instead of the normal stratified squamous epithelium. Morphologically, the epithelium in Barrett’s esophagus contains mucus-secreting goblet cells, enterochromatin cells, and, in about onehalf of the cases, parietal cells.’’6’8’9”4’1’ Diagnosis of this entity may be strongly suspected roentgenographically by the combination of mid-esophageal stricture and esophageal hiatal hernia together with normal esophageal motility, except at the level of the stricture.’2 Mucosal electrical potentials and esophageal motility have also been studied in attempts to diagnose Barrett’s 14 Although these various techniques may suggest this condition, the diagnosis must currently be confirmed by endoscopic biopsy. We report a new approach to the diagnosis of Barrett’s esophagus, which is based upon the principle that radioactive (TcIIm) pertechnetate

is selectively

taken

710

up

by

in Barrett’s visualized

the

gastric

The

Technique fasting

Patients

suspected

were

scintignaphy,

of

or

the as

into

conventional

of

at

the

Department Rochester,

Seventy-fourth

injection

of Diagnostic Minnesota.

and

patient

between

termination

of

is

in-

the

time

the

pro-

this is facilitated by use of a dental type of oral aspirator. The patient stands during the examination in order to lessen the possibility of reflux of contents from the stomach into the esophagus, and is placed in front of the gamma camera (Searle, model HP) with his arms resting on it to minimize motion. Scintigraphic imaging is performed at 30 and 6o minutes following injection; these intervals allow the isotope concentrations in the blood pool todiminish. For each image, 6oo,ooo counts are accumulated. After the scan, the patient swallows barium and a roent-

type

genogram

This

is taken

serves

in

to define

for

upright

the

position.

location

made

with

in the

the

same

of

j unc-

esophagogastric

comparison

are

the

better

roentgenographic

scintigrams,

position.

Barrett’s RESULTS

radioisotope barium

Annual

the

to swallow

cedure;

The appearance of the scintigram in the normal subject is seen in Figure I, which demonstrates not only intense concentration of isotope by the stomach but also the lack of radionuclide uptake by the esophagus. Evidence of activity is also seen in the cardiac blood pool.

roent-

genography, and endoscopy plus biopsy. They were selected for study if all of the following criteria were satisfied: (i) clinical symptoms of esophagitis or dysphagia; (2) roentgenographic evidence of stricture of the esophagus, with or without associated * Presented 25-28, 5973. From the Foundation,

and () ulceration or without stric-

juice),

not

which

having

hernia; with

gastric

structed

esophagus and by scintigraphic

with

H.

Scintigraphy. mci Tc99#{176}’ intravenously. No perchlorblocking agent is used. Because is secreted into saliva (as well

other isotope

ate

METHOD

studied

DAVID

of Radioisotope patient is given

pertechnetate

tion

esophagus

M.D.

ture.

the AND

M.D.,

CARLSON,

esophageal hiatal of the esophagus,

11

MATERIAL

G. NOLAN, C.

MINNESOTA

N

ofmucosa found that it can be

DIAGNOSIS

ESOPHAGUS*

M.D., M.D.,

IN

Meeting

Roentgenology

of

the and

American the

Section

401

Roentgen of

Ray

Diagnostic

Society, Nuclear

Montreal, Medicine,

P.Q., Mayo

Canada, Clinic

September and

Mayo

-

Berquist,

402

Nolan,

Stephens

and

Carlson

Fitire

4

2,

characteristic

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- ::-‘

. -‘:

-,#{149}-

-

. .‘

,

‘‘:

gra)hic

features

The hiatal

roentgenogram hernia and

passg slight and

.4

margill

of

uptake

with

of

eso)hageal the mid-

particular the peristaltic

patient, wave

hernia,

the

of

considered

by

the

concentration

the

up

sponds

esophagus

stomach the iso-

of

to

al)Proximately

to

esopli agogastnic in Figure 2B

activity

continuous

tope

esophagus. an

roen tgeflogra)hic The scintigrarn

shows -.‘..i

the scinti-

the stricture, with only at the level ofthe stricture, continuation down to the

through

be the junction.

.a

Barrett’s

shows a stricture

In this showed

1975

demonstrates

and

of

hesitation then its

upper

B,

and roentgenographic

esophagus. fluoroscopy

Hiatus

FEBRUARY,

level

a

to

that

that the

of

correstnic-

‘4’

ture

the

on

indicates 11G.

I . ‘Fc’9’

men

lIId

isotope

there junction

pertechnetate

scan

thorax

lower

is concentrated

is

no

in

uptake

A small

of

in the

amount

upper subject.

gastric

the

above

cardiac poo1. (Reproduced Mayo Clin. Proc4)

the

normal

of isotope

mucosa, esophagogastric

remains

permission

with

abdo‘l’he but in

the

up

adjacent

extension esophagus studied 6

the \Ve

esophagus, mucosa

111

in the

ages

of to the PatientS

All

ranged

the

patients

from

were

“

,

‘

1.4,;._

!,

‘:‘

:

.

‘

-

gastric proved

men

whose

Dysphagia

.quamocoIumnar ,

.

junction

_,,

r

‘‘,(

-..,

4ophogeal

“..

.‘-#..t ‘F’-’

-

mucosa stricture. Barrett’s

ectopic was

37 to 69 years.

-‘

this

gastric level of with

all of whom lower esophagus

histologically.

from

roentgenogram;

e,Itric

jwcosa

;.;,

‘\‘

‘0 Fi;.

2. (ii) Barium swallow of isotope extends cephalad on the roentgenogram.

and

(B) beyond

ic”

pertechnetate the

esophagogastric

scan

in patient unction

to

with the

level

Barrett’s

esophagus.

corresponding

Uptake to

stricture

VOL.

123,

No.

and

heartburn

senting

Radioisotope

2

were

the

most

common

in

Barrett’s

felt

also

down

A #{231}6 year old man was referred bea 5 year history of nocturnal heartburn; he experienced a burning retrosternal pain when supine. ibis was relieved by sitting up, sleepilig with the head of the bed elevated, and by taking antacids. ‘Fhe history was otherwise normal. Results of the physical examination were unremarkable. Fluoroscopically, 1 stricture of the mid-esophagus was observed. The stripping wave was noted to pass through the stricture and down to the level of the hiatus,

cults’

with

where

Just

CASES

I.

CASE

cause

the

tion

roen

was

tgenologic

located.

esophagogastric

Scintigraphy

with

been

gastric

absence

of parietal

CASE

phagia that

II. for

solid

old man 6 months.

had noted dvsHe had noted

gradually

began

to

stick

1)e at

the

raphy

denonstrated by the stoiiach

level

wall

of

he had

region

had

There

the

for

lower

that

Isotope

of

the

uptake a level on the

the

to

stricture

B).

Biopsy

stricture

taken

demon-

as

epithelium;

were

pertech-

continuous

esophagus

of

and to scintig-

Tc99”

of

1 ai1

4,

level

the

columnar

cells

hiatus.

with

the

apparently

mid-esophagus was deteriined

in

Case

I,

absent.

III. A 69 year old nian had a i year of progressive diflicultv in swallowing foods. Dysphagia only occurred with solid foods but his symptoms were 1)econling niore frequent. He had no difficulty in swallowing liquids ln(l no other symptoms. Results of the physical examination were un remarkable. l”luoroscopicallv, there was a stricture of the mid-esophagus with no associated esoph ageal CASE

history solid

in

hiatal

hernia;

the

esophagogastric

junction

was

-________________

-

- . ,.5quomocoIumnar

,:

‘:‘‘

-;a.:

junction

,_.

#{149}aI

0 FIG.

3. Case

i.

(A)

of isotope

a

l”luoroscopically,

uptake

(l”ig.

below

strated parietal

of

to

roentgenogram

Cells.

A ‘ear the previous foods

for

eating.

correspotling

the

except

esophagus;

retrosternal

until the food appeared to conthe esophagus, but he had no liquids an(.I had not experienced

after

1))’ the

per-

mucosa,

the

no weight

netate

technetate showed that the isotope concentrated in the stonach, with continuous extension ofuptake cephalad in the esophagus to the approximate level of the roen tgenographic stricture (Fig. .3, A and B). Biopsy specimens taken just below the level of the stricture all demonstrated

in

loss or nielena. there was stricture of the the esophagogastric junction

j unc‘I’cih1

period,

voIiiting

of

403

to be tIle upper

pain

short tinue

OF

Esophagus

seemed

what

pre-

complaints. REPORT

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Scintigraphv

Barium swallow and (B) Tcssm pertechnetate in lower esophagus to the level corresponding

scan.

Scintigram

to stricture

demonstrates

concentration

on the roentgenogram.

Berquist,

404

Nolan,

Stephens

and

Carlson

FEBRUARY,

1975

I

squonocoiumnar

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.

unction

,_--“‘

.a’r

-

‘,

: -

-

--

FIG.

above

determined

and level

B). of

type

mucosa

CASE of

(l”ig. A

level

62

old

hiatal

vention,

recurrent

man,

c, 4 the

gastric

9

at

hernia had Despite pyrosis

noted that

operative symptoms

retro-

developed,

of

the

and interincreas-

Scintigraphy

with

concentration extension level on

an

Tc99”

ofthe

into

the

specimens stricture

epithelium

to

roentgenogram

taken revealed

with

no

the

stomach

esophagus

that

of the

(Fig.

7,

Just

for

ii

below

the

gastric

type

parietal

cells.

stricture

stricture and conto the hiatus. Scans uptake

of

interval. in

the

Biopsy

stricture

was

case,

was

pool,

of the

revealed

much

which taken

less

allowed

on

the

below

just

epithelium cells were

columnar

in which

4 of the

esophagus

specimens

areas

instead

There

cardiac

delineation

with several present.

scan

in this

of the (Fig. ‘,

parietal

and to seen

B). Biopsy level of the of columnar

and

level

peristaltic

revealed

delayed

minute

better

the

revealed

by the

The injection

background

esophageal hiatal mid-esophagus.

pertechnetate

isotope

cephalad corresponding

the

the

the

obtained

scilitigraln.

of

esophageal

through

B).

examination

denionstrated

the

post-

demon-

at

-1 and 6o

a stricture

l”luoroscopy

level

usual

examination hernia and

of

continued

the isotope in the esophagus to the stricture as seen on the roentgenogram

ing during the 2 years before the current examination. The patient had also noted tarry stools on several occasions. The results of physical l”luoroscopic

course

noted

esophagus

the esophagus pertechnetate

down ‘I’c99”

after

unreii,arkable.

the

patient

of the arch;

passed

hours

were

In

the

heartburn.

aortic

with

an

evaluation.

follow-up a stricture

wave tinued

time

been detected the surgical

medical

strated

complained

had

years;

hernia

after

stricture

A ,37 year old iian presented with and dysphagia. An esophageal was found, and this was repaired

v.

hiatal

of

below

who

depression,

for

surgically.

CASE

heartburn

esopha-

Uptake of isotope extends on the roentgenogram.

scintigram.

to esophageal

of

year

and

repaired

hiatus. up-

(l”ig.

immediatel’ demonstrated

pertechnetate

comparable

level

-4-

__________

________

Tcssm

6).

burning

esophageal

(B)

and to the

roentgenogram

taken stricture

nervousness

sternal

the

oti

Biopsy the

IV.

swallow junction

be at the level of the scm tigraphy demonstrated the stomach and by the that corresponded to the

to

Radioisotope take, both by gus, to a level the stricture

,

-

:

Case II. (A) Barium the esophagogastric

4.

‘t,,

4

CASE

a

VI.

A 69 s’ear

iionth

history

of

sternal

l)urning

that

occurred after when lying down. loss, or vomiting. it

old

white

heartl)urn. seemed

meals The

noted

to reach

and

He had

had

ian

He

seemed no

findings

his

an retrothroat;

to be worse

dysphagia,

of the

weight

physical

iS

VOL.

No.

123,

Radioisotope

I

Scintigraphy

in

Barrett’s

Esophagus

405

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SquamocOlumnar

Esophag.al Gastric

-

mucosd

1’

-‘1

‘.‘

7

‘ --

10 FIG.

Case

.

(4)

III.

Barium

swallow

and

above the esophagogastric junction (Reproduced with permission from examination a

were

large

tion

at

tional the

its

level

of

scintigram

the

hiatal

concentration

the

stomach

and

the

scan.

Concentration

to esophageal

stricture

of isotope

extends

on the roentgenogram.

Proc.4)

ulcera-

at least 2 addijust proximal to junction. The

and

esophagogastric by

C/in. revealed

with

esophagus

demonstrated

pertechnetate

Mayo

hernia

margin

in the

to the level comparable

I’luoroscopy

hiatal

superior

ulcers

geal

normal.

esophageal

(B) Tc99m pertechnetate

may

also

nosis,

be

logically,

as

through CASE

ofTc99” esopha-

of value in excluding this cannot be done

when

exemplified

the diagroentgeno-

Cases

by

vii

ix. VII.

A 78

year

old man

presented

specimen

obtained

with

there was also an area of inin the region of the lower ulcer at the superior margin of the esophageal hiatal hernia and another superior to this, corresponding to the level of the ulcers in the esophagus (Fig. 9, ii and B). Biopsy specimens demonstrated islands ofgastric mucosa in the esophacreased

gus

hernia;

uptake

with

hum

inflamed,

stratified,

surrounding

represents a variant termed Barrett’s one or more islands is

esophagus

with

Comment. technetate

esophagus tion of

in

is

Cases

of

the

otherwise

The

epithe-

SqUamOUS

these areas. This condition of Barrett’s esophagus and ulcer. It is characterized by gastric

usefulness the diagnosis

demonstrated i through

mucosa

vi.

in an

epithelium.

normal

of TcI9m perof Barrett’s by The

consideratechnique

I’IG.

b.

ately strating

reduced from

Lase

III.

below gastric

thopsy

level

of esophageal mucosa.

stricture,

(Hematoxylin

from X64.) (Reproduced Mayo C/in. Proc.4)

with

immedi-

demonand Eosin permission

a

Berquist,

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406

Nolan,

Stephens

and

Carlson

FEBRUARY,

1975

0 ‘I- -

J.

-

‘;i

4;’

Esophag.oI

I

.; - --

-‘

FIG.

7. Case

IV.

(A)

Barium agus

to

swallow the level

and (B) Tcssm corresponding

,c:

0

_

pertechnetate

to stricture

scan.

on

the

Isotope uptake roentgenogram.

-

in esoph-

4’-’’

,--‘

-

is evident

Esophag.oI

--

Gaitric mucosa

‘>-

--‘f

FIG.

8. Case

injection

Note

V. reveals

essentially

(A)

Barium swallow and (B) Tcssm pertechnetate scan. uptake of isotope in esophagus to level corresponding no background in cardiac pool.

Scintigram

obtained

to stricture

on

the

hours

roentgenogram.

after

VOL.

113,

No.

Radioisotope

I

Scintigraphy

in

Barrett’s

Esophagus

.

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-

407

#{149}1

t’,-’:;

‘.:-

.

*.s -.

:

..“

-

--p

‘

.

c_

- -

‘

I

‘

!l;,:

.

.

Hiatol

H.rnlo

.

;,‘ ,

-

;‘i;’1

‘

I

-

:

..

:

‘-.-

.

‘

:-‘

-:;

-

-

*

c.-’ i---

4

‘

--

44 lIG,

“

-

oi_________j

9 Case vt (1) Barium swallow and (B) ‘Ic99” pertechnetate scan. Uptake is increased in left upper portion of esophageal hiatal hernia (corresponds to lowest of ulcers on roentgenogram); uptake in esophagus corresponds to areas of ulceration above hiatal hernia on the roentgenogram. year

with

history

of

postprandial

an associated

tenor

chest.

regurgitation,

burning

‘I’he

sensation

patient

noted

burning

or

lowing,

no

stricture strated

of the mid-esophagus I)y fluoroscopy; no

hernia

was

graphic

level

regurgitation, weight

hiatus.

take of isotope in the esophagus aid of the scan, Barrett’s

means

taken stricture

rett’s stratified,

mucosa.

no

the

hiatal

was and

at

the

etiology

apparent roentgenodemonstrated up-

which

immediately

below

the

conhi’med

esophagus squamous

was

roentgenogram

by

scan

the

possible Biopsy

level

demonstrating epithelium,

of

in excluding but

I 1,

the

Barinflamed,

no gastric

(io

lb.).

the

l’luoroscopy of

4

B).

and

A

IX.

taken

below no

the

level

stratified,

gastric

man

but (Fig.

inflamed,

old

year

52

stomach,

esophagus

but

of

demon-

lower

revealed

epitheliuin,

CASE

tigram

l))T the

the

Biopsy

stricture

a stricture

scm

isotope in

with after

of gastric he had lost 4.5

revealed The

radioactivity the

regurgitation past year

frequent

I)uring

5(lt1ai11S

had

mucosa. a history

of

anemia and weight loss. He had noted increasing fatigue for i year, but no melena, dysphagia, or

not alone.

with

man presented and bloating

of

the mid-esophagus. sti’ated uptake

of

bY the stomach, but no activity (l”ig. io, ‘1 and B). \Vith the one could rule out the presence the

kg.

no

roentgeno-

signihcance

were not scintigram

A

year old belching

72

history

contents.

demon-

A

\‘III.

a To year meals

in swilmelena.

junction

The

an-

nocturnal

was esophageal

and

esophagus,

of

no

difficulty

and

esophagogastric

of the

the stricture graphically. The

by

loss,

visualized

of

of

no

CASE

in the

heartburn

polvpoid was

thought

demonsti’ated the stomach, (l”ig. 12, 4 adenocarcinoma

l”luoroscopy

.

lesion to

of be

the

and

The of

the

uptake in the B). Biopsy specimens of the stomach with no

a

esophagus;

a carcinoma.

concentration

but

demonstrated

lower

this

scintigram isotope

esophagus revealed extension

in

Berquist,

408

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r

Nolan,

Stephens

I

----,

and

.-

Carlson

FEBRUARY,

1975

--t’-

:

.

-

‘

‘

,

c-’;’

‘

Hiatus ,‘,-

,v’

.

“

:

‘

‘--‘

-

;‘_.

-‘

.

‘

-:

:

i--’

,‘

-.- .-

---k--

;-

w!

-‘ - ;-‘-

Case

FIG.

10.

FIG.

I I . Case

the

vii. (A) Barium swallow but no uptake of isotope

VIII.

stomach

(A) Barium (and some

and above

swallow and in the cardiac

(B) TctBm pertechnetate the esophagogastric

(B) Tc” pertechnetate pool), but no uptake

scan. junction

:

Uptake at the

scintigram. above the

‘

‘--‘

of isotope in the level of hiatus.

stomach,

There is uptake of isotope esophagogastric junction.

in

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VOL.

123,

No.

stomach and the esophagus.

into up

were have An

the lower in

the

Radioisotope

2

less

uptake

esophagus.

malignant

neop.astic

Isotope gastric

however,

can

roentgenographically scintigraphic

not concentrate

and

that Tcssm

it

of the

there

that would esophagus. of

resemble

and evidence

area

in Barrett’s

was not taken tissue

no roentgenographic features been confused with Barrett’s early, infiltrating carcinoma

esophagus,

does

in the

Scintigraphy

is helpful

malignant

the this

midentity

to

have

tissue

pertechnetate.

DISCUSSION

To date, 9 patients have been studied with TcI9m pertechnetate scintignaphy of the esophagus. In patients, a diagnosis of Barrett’s esophagus was made on the basis of abnormal uptake of Tc9Im pertechnetate by the lower esophagus, as seen on the scans. In each instance, the diagnosis was confirmed by tissue biopsy. In i additional patient who had the rare variant of Barrett’s esophagus named Barrett’s ulcer, the radioisotope was concentrated in the areas of esophageal ulceration; in this patient, too, diagnosis was confirmed by biopsy. Three patients with esophageal conditions

stomach,

t.t

Esophagus

no uptake

409

in the

region

c.

..etumor

in

other than Barrett’s esophagus or Barrett’s ulcer were also studied; scintigrams showed no esophageal uptake of pertechnetate, and biopsies confirmed absence of gastric mucosa in the esophagus of each patient. In addition to our scintigraphic studies in these 9 patients, we have performed autoradiographs of the gastric mucosa in a group of dogs and rats in an attempt to localize the site of Tc99m pertechnetate concentration. In our initial investigation, it was thought that autoradiographs of the gastric mucosa from i dog demonstrated uptake of Tc9Im pertechnetate in panietal cells.* Subsequently, numerous studies in dogs and rats revealed that the findings in our initial study were invalid. These later studies demonstrated intense uptake in the surface epithelial cells with essentially no activity observed in any other cell type. This finding is in conflict with the reports S Oral treal,

presentation.

September,

American 1973.

Roentgen

Ray

Society,

Mon-

Berquist,

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410

Nolan,

Stephens

of many authors who have stated that Tc99m pertechnetate is probably concentrated and secreted by panietal cells.3’4’7”#{176}’1’ None of these studies, however, included autoradiographic verification. Set#{228}l#{227} and colleagues’3 were the first to state that Tc99m pertechnetate was apparently concentrated in mucoid cells of the stomach in man, but they did not confirm this hypothesis by autoradiognaphy. The finding that histologic localization is confined to the surface epithelial cell is fully consistent with the scintigraphic evidence for technetium uptake by gastric mucosa-both in situ and in extragastnic locations-because this cell type is present in all types of gastric mucosa, irrespective of its anatomic location. A major objection to the proposal that concentration of this radionuclide is a property ofparietal cells has been the frequent failure to histologically identify parietal cells in biopsies

from

patients

in

whom

and

epithelium after this

Carlson

FEBRUARY,

and tissue

one has

that is undergone

not

197$

observed malignant

transformation.

CONCLUSIONS Scanning of the esophagus with Tc99m pertechnetate for the diagnosis of Barrett’s esophagus appears to be useful both in making the diagnosis and in helping to exclude it. The technique offers a noninvasive approach to the identification of columnar epithelium lining the lower esophagus and promises to be useful in better understanding the etiology of the disorder. Thomas H. Berquist, M.D. Departmen t of Diagnostic Roen Mayo Clinic Rochester, Minnesota 55901

tgenology

Barrett’s

esophagus had, in fact, accumulated Tc99m pertechnetate as evidenced by scintigraphy. A review of the surgical specimens from our 6 histologically proven cases of Barrett’s esophagus, in all of whom the scans were abnormal, revealed complete absence of parietal cells in all but one. By contrast, the gastric type of surface epithelial cells was present in every case. Thus, the finding of cellular uptake by gastric surface epithelial cells is fully in accord with the histopathologic and scintigraphic findings and offers a more satisfying explanation than could be obtained from parietal cell localization. Carcinoma of the stomach has been studied with Tc99m pertechnetate scintigraphy, and the uptake of Tc99m pertechnetate is relatively low in neoplastic areas as compared with the surrounding normal gastric tissue.”3 In Case ix, there was a relatively decreased uptake of Tc99m pertechnetate in the neoplastic region of the stomach and no uptake by the malignant gastric tissue that invaded the lower esophagus. Thus, uptake of Tc99m pertechnetate in the esophagus appears to be a characteristic of benign ectopic gastric

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