Ji-Bin Archie Philip

Liu, MD #{149}Larry S. Miller, MD A. Alexander, MD #{149}Laurence J. Klenn, MD #{149}Carl L. Millward,

Transnasal Morphologic

catheter-based ultratransducers can be inserted into the esophagus transnasally to evaluate esophageal wall structures. Studies were performed in two sheep esophagus specimens in vitro, in 17 healthy human subjects, and in 16 patients with esophageal abnormalities (eight with achalasia, four with scieroderma, three with esophageal carcinoma, and one with esophagitis). In the sheep specimens, endoluminal US delineated seven layers of the esophageal wall; these results correlated closely with histologic findings. Real-time US of the normal esophageal wall was performed during resting and swallowing. Muscles at the lower esophageal sphincter (LES) were shown to be thicker than muscles in the body of the esophagus. Thickening of the muscular layers at the LES in achalasia, dilated blood vessels within the submucosa in esophagitis, and fibrotic changes within the muscular layers in scieroderma were demonstrated. Extramural structures adjacent to the esophagus were also seen. These preliminary results suggest that transnasal esophageal US may become an important diagnostic tool in evaluation of the esophagus. Index terms: Achalasia, 71.745 #{149}Catheters and catheterization, technology #{149} Esophagitis, 71.291 #{149} Esophagus, diseases, 71.291, 71.321, 71.613, 71.745 . Esophagus, US, 71.12981 #{149} Sderoderma, 71.613 #{149}Ultrasound (US), technology 1992;

B. Goldberg,

MD

184:721-727

P

I From the Division of Diagnostic Ultrasound, Department of Radiology (J.B.L., B.B.G., R.I.F., A.A.A., L.N.), Department of Gastroenterology (L.S.M., D.O.C.), and Department of Pathology and Cell Biology (P.J.K., C.L.M.), Thomas Jef-

University

Hospital,

Rick I. Feld, MD 0. Castell, MD

#{149}

Seventh

Floor,

Main

Bldg. 132 S 10th St. Philadelphia, PA 19107-5244. Received August 9, 1991; revision requested October 7; revision received March 30, 1992; accepted April 7. Address reprint requests tOJ.B.L. C RSNA, 1992

Preliminary

of an endoluminab ultrasound (US) transducer into the rectum to evaluate the wall of the bowel (in an attempt to identify malignant tumors) was first reported by Wild and Reid in 1956 (1). Since that time, a number of researchers have been working on the further development of endoluminal sonography. In 1976, Lutz and R#{246}sch(2) reported using a US probe passed through the accessory channel of an endoscope. They obtained A-mode images to evaluate the cystic versus solid characteristics of lesions deforming the gastric wall. In the early 1980s, the concept of combining a flexible endoscope with a US transducer to image the gastrointestinal tract was developed and results were published by Fukuda et al (3) and DiMagno et al (4). With use of relatively high-frequency transducers (7-12.5 MHz), it was possible to image not only the walls of the gastrointestinal tract but, also structures adjacent to the tract LACEMENT

(5). This

approach

has

proved

useful

in preoperative diagnosis and staging of esophageal and gastric cancers (6,7). In 1989, Silverstein et al (8) deveboped a 20-MHz linear-array US probe that could be passed through the biopsy channel of a flexible endoscope to evaluate the gastrointestinal tract wall. More recently, ROsch and Classen (9) used a 7.5-MHz, 3.7-mmdiameter US probe in an attempt to image the esophagus, stomach, and duodenum by means of the working channel of a gastroscope. Over the past several years, flexible US transducer-containing (4.8-9 F), originally

ferson

MD Donald

#{149}

US ofthe Esophagus: and Function Studies’

High-frequency sound (US)

Radiology

#{149} Barry

Needleman, BS

designed

catheters for intra-

vascular US applications, have become available (10,11). During the past 2 years, these miniature catheter-based transducers have been used to evabuate nonvascular lumina, including the genitourinary tract, endometrial canab, bile ducts, and bronchial tree (1216). We report our use of these transducers to image the esophagus.

MATERIALS US

AND

METHODS

System The imaging

available Milpitas, catheters length)

system

used

in this study

is

commercially (IVUS; Diasonics, Calif). Specially developed 6.2-F (2 mm in diameter, 95 cm in containing 20-MHz transducers

are used

(Sonicath; Medi-tech/Boston SciWatertown, Mass) (Fig 1). The singbe-ebement US transducer is mounted on the end of a wire (core), which is conentific,

nected to a motor on the US instrument. The 1 .35-mm-diameter core is inserted into the flexible catheter, and the motor is rotated to produce a 360#{176} transaxiab real-

time image.

Sterile

introduced

eter

water

between

to eliminate

(0.5-1.0

the

core

air, which

mL) is

and

the

could

with transmission of the ultrasound The transducer sends and receives trasound pendicubar

cath-

interfere

beam. the ub-

signal at an angle 10#{176} from perto the long axis of the catheter

(Fig 2). The operating

frequency

of 20

MHz results in an axial resolution mm and a penetration of about

of 0.1 2.0 cm.

Real-time images are recorded on videotape for later evaluation, and individual frozen images are stored on a digital imager disk system (3M Medical Imaging Systems,

St Paul).

Animal

Studies

Whole sheep

esophagus

were

specimens

studied

in vitro.

specimens were placed The transducer-containing inserted

into

the

lumen

from the proximal was

advanced

ious

layers

imaged

two

fresh

in a water bath. catheter was of the

end.

from The

esophagus

As the catheter

at intervals of 3 cm, the varof the esophageal wall were and measured. The echogenicity

of the various

layers

of the esophagus

was

also evaluated. To eliminate near-field transducer artifacts, 15 mL of saline was injected into the lumen of the esophagus

and the imaging procedure After sonographic imaging, were fixed in 10% formalin

was repeated. the specimens and imbedded

CSM = circular smooth muscle, LES = lower esophageal sphincter, LSM = longitudinal smooth muscle, TM = total muscle. Abbreviations:

721

in paraffin. Histologic cross sections were prepared that corresponded to the US image

planes.

Finally,

tified

wall structures

those

depicted

Human

the histologically

were

iden-

correlated

with

on the US images.

Studies

Seventeen healthy volunteers (10 men and seven women, 21-85 years old with a mean age of 40 years) and 16 patients (seven men and nine women, 32-73 years old with a mean age of 43 years) were included in the study. Each of the 16 patients had a known diagnosis: Eight had achalasia, four had scleroderma, three had esophageal carcinoma, and one had reflux esophagitis. All four scberoderma patients had heartburn, and three had dysphagia. The time course of the disease was 1-15 years. The diagnosis of scleroderma was based on typical clinical features and results of serologic tests. All achalasia patients had their disease diagnosed on the basis of typical manometric findings (high residual pressures in the lower esophageal sphincter [LES] and absent peristabsis) and radiographic appearances (barium esoph-

agogram showing dilatation of the esophageal body and narrowing at the LES). Clinical symptoms included dysphagia, regurgitation,

cough. With

weight

the subject

a 16-F nasogastric through the was advanced

loss,

and

in a sitting

nocturnal

position,

tube was inserted

nose. As the nasogastric to the pharyngobaryngeal

tube

level, the subject was asked to drink 5-10 mL of water to aid the passage of the tube into the esophagus. As soon as the nasogastric tube entered the stomach (an event easily recognized by means of aspiration

of gastric ing

the

contents), US

through

the catheter

transducer

the

tube

was

contain-

1. II

Figures

1, 2.

(1) Endoluminal

US transducer

Figure

3.

Schematic

the catheter-based transnasally (NG) into

the

representation

transducer

(Fig 3). The

through the esophagus.

nasogastric

subject

were

slowly

withdrawn from the stomach to the LES. The esophageal wall was imaged during the resting state at the level of the LES and 5-10 cm above the LES. The subject was then asked to drink 5-10 mL of water

while real-time US was performed to evaluate swallowing. In the 17 healthy subjects and the eight achalasia patients, three images were selected from the level of the LES. In addi-

digitally

stored

subjects

three

the area

in a computer

im-

5-10

selected

cm

were

system

the CSM,

722

the LSM, and an intermuscubar tissue layer) was measured at octants by two independent U.B.L., L.S.M.). In the control

Radiology

#{149}

was determined by using a Pearson correbation coefficient. Intraobserver variability was determined by means of repeat measurement on the original images by each

independent

investigator

the first reading. carried out with

tion coefficient.

3 months

Analysis of the use of a Pearson

Muscle

layer

after

data was correla-

thicknesses

at the LES in control subjects were compared with muscle layer thicknesses at the LES in achalasia patients. The Student test was used for analysis of the data.

(Mi-

croSonic, Indianapolis). On each image, the thickness of the circular smooth muscle (CSM), longitudinal smooth muscle (LSM), and total muscle (TM) (including connective eight radial investigators

wire

pa-

the LES. Interobserver variability between the mean wall thickness measurements made by each independent investigator

tion, in the 17 healthy

of a drive

was

The US imaging tube

ages were selected from above the LES. All images

end

tube

manometric

nasogastnc

the

shows

patients, muscle layer thicknesses at the LES were compared with the thicknesses of the corresponding layers 5-10 cm above

examination.

on

(T) passed

tients, and the scleroderma patients, the distance from the nose to the LES region was previously established by means of and

is mounted

inserted

then placed in a supine position. For all volunteers, the achalasia

catheter

(arrow)

(core), which is housed in a 6.2-F catheter. Sterile water (0.5-1.0 mL) is injected with a 27gauge needle through the sealed catheter tip to eliminate any air around the transducer. (2) The transducer (T) rotates clockwise, producing a 360#{176} cross-sectional real-time US image at an angle of 10#{176} from the perpendicular. A, Longitudinal view; B, cross-sectional view corresponding to the scanning plane.

RESULTS Animal

Studies

With use of the 20-MHz catheterbased transducer, it was possible to delineate seven layers of the esophageab wall in the two sheep specimens.

Correlation with the innermost sented

of the histologic US images showed layer (hyperechoic) the

squamous

findings that the repre-

epithelium

September

and

1992

b. Figure

4.

(a) The

20-MHz

wall. (b) Close correlation

US transducer

between

C.

(T) located

within

the cross-sectional

the

saline-distended

sheep

esophagus

delineates

seven

layers

of the

esophageal

histologic

slice and the US image in a can be seen. (c) Schematic drawing identifies esophageal wall structures in cross section. In a-c, I = squamous epithelium and lamina propria, 2 = muscularis mucosae, 3 = submucosa, circular muscle, 5 = intermuscular connective tissue, 6 = longitudinal muscle, 7 = adventitia.

cosa),

a hyperechoic

hypoechoic

and

longitudinal),

intermuscular between hyperechoic

p.

Catheter-based US transducer (T) positioned within the LES region (a) and 8 cm above the LES (b) in a healthy volunteer delineates the various normal layers of the esophageal wall. Note that the thicknesses of the muscular layers in the LES region are different from the thicknesses of those in the body of the esophagus. 1 = mucosa, 2 = submucosa, 3 = circular muscle, 4 = intermuscular connective tissue, 5 = longitudinal muscle, 6 = adventitia. Figure

5.

the

adventitia Volume

(Fig 184

3

Subjects

In all control subjects, the crosssectional US images were obtained at various bevels, including the LES region and the middle and upper portions of the esophagus. There was a moderately echogenic mucosa (including

lamina

4).

#{149} Number

Control

the

squamous

propria,

and

epithelium,

muscularis

mu-

layers

a thin connective two muscle adventitia

4

=

two (circular

echogenic tissue

layers, (Fig

layer

and

a

5). Be-

cause the esophageal lumen in the resting state is collapsed and folded together, the muscubaris mucosae could not be clearly seen. When the esophageal lumen was distended with water, it was possible to delineate seven esophageal wall layers similar to those seen in vitro in the sheep esophagus. Measurements of muscle thickness at the LES in the control group are shown in Table 1. Measurements of muscle thickness 5-10 cm above the LES in the control group are shown in Table 2. The CSM, LSM, and TM were significantly thicker at the LES than in the esophageal body (P < .001 for all three comparisons) (Fig 5). Interobserver

lamina propria, the second layer (hypoechoic) the muscularis mucosae, the third layer (hyperechoic) the submucosa, the fourth layer (hypoechoic) the circular muscle, the thin fifth layer (hyperechoic) the intermuscular connective tissue, the sixth layer (hypoechoic) the longitudinal muscle, and the seventh layer (hyperechoic) the

submucosa,

muscular

the

variability

for

mea-

surements at the LES was r = .98 and P < .01 for the CSM, r = .73 and P < .01 for the LSM, and r = .98 and P < .01 for the TM. Interobserver variability for measurements in the body of the esophagus was r = .94 and P < .01 for the CSM, r = .67 and P < .01 for the LSM, and r = .97 and P < .01 for the TM. Intraobserver variability for measurements at the LES for investigator 1 was r = .99 and P < .01 for the CSM, r = .89 and P < .01 for the LSM, and r = .96 and P < .01 for the TM. Intraobserver variability for measurements in the body of the esophagus for investigator 1 was r = .94 and P < .01 for the CSM, r = .71 and P < .01 for the LSM, and r = .98 and P < .01 for the TM. Intraobserver variability for measurements at the LES for investigator 2 was r = .98 and P < .01 for the CSM, r = .84 and P < Radiology

#{149} 723

Figure

6.

(a) Catheter-based

(T) located within shows a hypoechoic x 0.49 cm (cursors), The predominantly an artery (pulsation real-time

imaging).

US transducer

the distal esophageal body structure measuring 0.91 which is a lymph node. anechoic area (arrows) is could be seen during (b) Cross-sectional

US

image obtained at the gastroesophageal lion shows a hypoechoic region (arrows) jacent to the esophageal wall, representing the diaphragm.

juncad-

.01 for the LSM, and r = .95 and P .01 for the TM. Intraobserver variability

for

measurements

in the

body

Transnasal US of the esophagus: preliminary morphologic and function studies.

High-frequency catheter-based ultrasound (US) transducers can be inserted into the esophagus transnasally to evaluate esophageal wall structures. Stud...
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