Ultrasound

Ultrasound Evaluation of the Gallbladder Wall 1

Harris J. Finberg, M.D., and Jason C. Birnholz, M.D.

In a series of 526 consecutive, unprepared patients examined by ultrasound, the gallbladder

was visualized in 507 (96 %). The average wall thickness was 2 mm or less in 97 % of
asymptomatic subjects without cholelithiasis and 3 mm or greater in 45 %' of those with cho-
lelithiasis. Pathologic correlation of increased thickness and chronic cholecystitis was made
in a subgroup of 47 surgical patients. Local tenderness and mucosal thickening were found
in 8 patients with acute cholecystitis. Use of electronic sector scanning is emphasized.
INDEX TERMS: Abdomen, ultrasound studies. 7[0 ].1298. Gallbladder, diseases. Gallbladder, ultrasound studies,
7(62) .1298

Radiology 133:693-698, December 1979

UMEROUS reports have established a clinical role for

N ultrasonic cholecystography in the diagnosis of
cholelithiasis (1,2,4,6, 7, 13) but the common conditions
of acute and chronic inflammatory disease have not been
treated with equal thoroughness.
Gallbladder wall features are an essential part of the
pathologic assessment of this organ. Ultrasound visual-
ization of the wall has been reported (5, 9, 11-13) but
without systematic quantitation of wall thickness or definite
conclusion as to the diagnostic usefulness of ultrasound
wall appearance in clinical practice. In this study, a tech-
nique for evaluating the gallbladder ultrasonically with
electronic sector scanning is presented as prefatory (but
integral) to the assessment of both wall thickness and in-
spection of intraluminal contents in the clinical context.
Fig. 1. Measurement of the gallbladder wall (arrows) is made along
METHODS the axis of the ultrasound beam using the portion of the gallbladder
contiguous with the liver and including all identifiable layers. Note the
distinguishable , less echodense zone adjacent to the lumen.
The study population consists of 526 consecutive pa-
tients, without cholecystectomy, referred for abdominal
examination for a variety of indications. Specific exami- The gallbladder is sought via an intercostal, transhepatic
nation of the right upper quadrant was requested in 29 % portal, with continuous viewing as the right upper quadrant
because of pain syndromes or food intolerance , believed is examined. Gallbladder visualization is accepted as
indicative of intrinsic gallbladder disease. No preparation satisfactory when the central fluid space andthe boundary
or food intake restriction was required for any subject rim are both defined. While maintaining visualization,
initially . Single study findings were accepted for analysis overall receiver gain and transmitter output are minimized
in subjects with multiple examinations. In those cases in for suppression of acoustic artefacts. Long and short axis
which the gallbladder could not be identified, or in which views of the gallbladder are achieved by probe rotation and
it was markedly contracted , a repeat examination after the entire volume of the gallbladder reviewed in each
fasting was requested. Fatty meals were not used. projection . Additional viewing with the subject in left de-
All subjects were examined initially in the supine posi- cubitus or upright positions is at the discretion of the ex-
tion by a physician using a commercial electronic sector aminer as are ancillary static images with a manual scan
scanning ultrasound imaging system (Varian 3000) with device (Searle Phosonic) with transducer selection pred-
the following performance features: 30/sec. frame rate, icated upon minimal beam width at the depth of the gall-
85° sector 21-cm depth field of view, image line density bladder.
in excess of 1 line per degree arc, broadband 2.25 MHz In patients with right upper quadrant pain, the probe is
center frequency, and fixed-focus cylindrical lens design placed in the subcostal location most proximate to the
with 1mm axial and 3.5mm lateral resolution at the 7-10 gallbladder, and observation is continued during deep
cm focal depth. probe palpation and deep inspiratory effort (3). A positive
1 From the Department of Radiology, Harvard Medical School, and Peter Bent Brigham Hospital, Boston, MA 02115. Presentedat the Sixty-fourth
Scientific Assembly and Annual Meeting of the Radiological Society of North America, Chicago. IL, Nov. 26-Dec. 1. 1978. Submitted for publication
21 Nov. 1978; rev ision requested 13 April 1979: received 25 July and accepted 24 Aug. 1979. shan

693
694 HARRIS J. FINBERG AND JASON C. BIRNHOLZ December 1979

2 a, b

2 C, d

Fig. 2. Variations in gallbladder wall thickness in 4 patients with chole lithias is. The scale in each is the same. Pathologic
diagnoses are listed: a: 1-2 mm, chronic cholecystitis; b: 3 mm, chronic cholecystitis; c: 5 mm , chronic cholecystitis
with marked serosal fibrosis ; d: 8 mm, acute and chron ic cholecy stitis.

Murphy sign is recorded when pain is elicited only during
image-verified deformation of the gallbladder.
A general survey of the upper abdomen is also per-
formed in all patients. Particular attention is directed to the
biliary duct system. hepatic parenchyma and pancreas ,
but the spleen, kidneys, midabdominal vascular structures
and pleural and peritoneal spaces are also reviewed.
The gallbladder wall is defined as the discrete echo-
dense margin encircling the fluid-filled lumen. It is impor-
tant to note whether a relatively hypoechoic rim is identi-
fied adjacent to the luminal surface apposed to the echo-
dense zone. The entire thickness of the nearer, subhepatic
wall is measured from static Polaroid images when the
ultrasound beam is perpendicular to the wall (Fig. 1). Wall
thickness measurements from all images available for
each examination are averaged and rounded to the nearest
millimeter.
Calculi are diagnosed when discrete, echodense in-
traluminal bodies are seen and when these cast acoustic
shadows when scanned with an extrapolated beam width,
which at that depth, is no greater than the dimension of
these bodies. Layered, dependent, uniform echodense
intraluminal material without shadowing is considered
" dense" bile and is recorded separately .
Direct measurement of wall thickness is made with
calipers in surgical specimens prior to fixation or refrig-
eration . These measurements are also recorded to the
nearest millimeter.
Vol. 133 ULTRASOUND EVALUATION OF THE GALLBLADDER WALL 695 Ultrasound

TABlE I: PATHOLOGIC FINDINGS IN 40 PATIENTS

TyPE OF CHOLECYSTITIS

Ultrasound Chronic
Wall Chronic and
(mm) Chronic Active Acute Subacute Acute

1-2 15 1 3 a a
3 3 0 a 0 1
4 6 1 1 1 a
~5 3 a 4 a 1

1-2 different from ~ 5 at p <0.05

TABLE II: ADDITIONAL PATHOLOGIC FINDINGS IN 22 OF 49 PATIENTS

Intrahepatic or common bile duct obstruction 6

(Mass at proximal common bile duct-carcinoma)
Pancreatitis or pancreatic edema 5
(Pancreatic pseudocyst)
Aortic aneurysm/ectasia 2
Hepatic abscess 1
Hydronephrosis 1
Cysts: Renal, bilateral 1
Hepatic 1
Ascites 1
Pericardial effusion 1
Decreased renal parenchyma 1
Splenomegaly (lymphoma) 1
Calcified splenic granuloma 1

RESULTS

Visualization of the Gallbladder and Its Contents

The gallbladder was identified by visualization of its
lumen fluid-filled space in 507/526 patients (96 %) . The
central fluid compartment was not visualized in 19 patients.
Nine of these had shadow casting echodense material in
the region of the gallbladder fossa. Of the remaining 10,
pathologic contraction was confirmed surgically in 4;
technical factors (massive obesity, immediate postprandial
state, post-cholecystojejunostomy) were implicated in 4.
Average time required for gallbladder visualization, in-
spection, and image photography was less than 1.5 min-
utes.
Cholelithiasis
Gallstones were diagnosed in 103/477 nonsurgical
patients (28 %), and 43/49 surgical patients (88 %). In the
surgical group, there were 40 true positives, 5 true nega-
tives, 4 false negatives and no false positives for an overall
accuracy rate of cholelithiasis of 45/49 or 92% . Three of
4 false negatives were probable operator rather than
method failures. In 2, decubitus views were not obtained,
and in one stones were evident in retrospect in the cystic
duct.
Wall Thickness
Wall measurements were obtained for 507 patients with
ultrasoundvisualization. There was agreement within 1 mm
between ultrasonic and gross pathologic measurements
in 36 of the 40 cases for which both measurements could
Fig. 3. Postprandial contracted gallbladder with
mucosathrown into folds. With fasting, the gallbladder
became distended with the wall reverting to a normal
pattern of a single 2mm dense band.
be made. Of these, 19 (48 %) had a wall thickness of 1-2
mm, 13 (32%) a thickness of 3-4 mm, and 8 (20%) a
thickness of 5 mm or greater (Fig. 2). No difference in wall
appearance was seen in the surgical patients without
cholelithiasis, in whom the thickness ranged from 1 to 5
mm . Anatomic normal thickness is 1 mm.
TABLE I shows the distribution of pathologic diagnoses
other than cholelithiasis in this group. Although the num-
bers are small, the frequency as compared to chronic
cholecystitis of acute, subacute, chronic and acute, and
chronic active cholecystitis is higher in patients with walls
5 mm or greater than in those with walls 1-2 mm thick,
with significance at the p < 0.05 level by X 2 analysis.
Similar analyses for walls 3 mm or greater and 4 mm or
greater each yield less significant p values of approxi-
mately 0.10.
Increased wall thickness was seen in a similar propor-
tion of the 103 nonsurgical patients with an ultrasonic di-
agnosis of cholelithiasis: 1-2 mm (54%),3-4 mm (33%)
and 5 mm or greater (12 % ). By comparison, wall thickness
of greater than 2 mm was seen in only 3.5 % of 368 pa-
tients with otherwise normal scans. Of these only 2 % had
walls 4-5 mm thick and none was thicker. Statistical
analysis confirms that the average wall thickness is greater
in subjects with cholelithiasis than in those without stone
disease at the p < .001 level.
696 HARRIS J. FINBERG AND JASON C. BIRNHOLZ
Fig. 4. Lamellated wall in patient with clinical, radiologic
and radionuclide evidence of acute cholecystitis. The whole
wall measured 10 mm (arrows) with the relatively less
echodense inner layer (m) 8mm thick presumptively identi-
fied as mucosa.
The appearance of the gallbladder wall in this series was
almost exclusively of a single echodense annulus sur-
rounding the lumen. In 12 cases striations of the wall were
identified. In 3 of these, an inner, more echolucent ring was
noted in a markedly small gallbladder, each in a patient
within 90 minutes of taking the most recent meal. Repeat
studies with the patient fasting showed increased disten-
sion of the gallbladder with reversion of the margin to a
single echodense band (Fig. 3).
In 7 other patients, a similar less echodense zone,
measuring 2-8 mm in thickness bordering the lumen, was
identified in fasting patients (Fig. 1). Acute and chronic
cholecystitis were confirmed pathologically in 3 and sus-
pected clinically in 4, including one patient with Salmonella
septicemia (Fig. 4). Another patient in this subgroup with
pathologic confirmation of acute hemorrhagic acalculous
cholecystitis had both a low echodensity, irregularly
thickened internal annulus and echogenic debris which
partially filled the lumen (Fig. 5). The final subject with a
thick multilayered internal rim had chronic lymphocytic
leukemia without clinical symptoms referrable to the
gallbladder per se.
Additional Findings
A definite Murphy sign was elicited in 9 subjects, all of
whom had acute cholecystitis clinically. Findings outside
the gallbladder were identified during the routine upper
December 1979
Fig. 5. Acute acalculous hemorrhagic cholecystitis. The
wall (arrows) is lamellated and grossly thickened with an ir-
regular luminal surface. The inner layer (m) appears more
echodense toward the lumen due to hemorrhage in it.
Amorphous dense echoes are seen in the lumen (L) indi-
cat ing hemorrhage here. also.
abdominal survey in 22 (45 %) of the surgical group of 49
patients (TABLE II).
DISCUSSION
In the present study, nonvisualization of the gallbladder
was highly indicative of pathologic contraction. The rela-
tively high rate of confident visualization, without prepa-
ration, follows from the use of a transhepatic portal, the
use of a physically unconstrained transducer probe , and
from cont inuous ultrasound viewing as the right upper
quadrant is searched. The localization process is rapid yet
thorough. When visualized, the gallbladder is situated at
the focal depth of the array. In addition, scan orientation
is selected in which reference points of the gallbladder wall
are situated along the central axis of the image for optimal
image resolution and measurement precision. A sector
scan format is selected because of the need for intercostal
viewing. Electronic sector scanning was chosen because
of overall probe size and weight and because of its even-
tual and theoretical resolution superiority to fixed focus
single-element mechanical systems when dynamic fo-
cusing is used.
Axial measurement precision for wall thickness should
be within 0.5-1 mm in the 2-5 MHz center frequency
range.
Wall thickness is calculated on the basis of an average
soft-tissue velocity of sound of 1 540 m/sec. Velocity in
collagen is approximately 1 750 m/sec., and velocity in
Vol. 133 ULTRASOUND EVALUATION OF THE GALLBLADDER WALL
soft tissues increases with the natural logarithm of collagen
content (10). Wall thickness will therefore be underesti-
mated when the wall has extensive fibrosis; however, the
magnitude of this factor is unlikely to be significant in
clinical practice over the size ranges involved for the
gallbladder wall. Likewise, velocity gradients due to local
temperature variations are also believed to be insignificant.
Fat around the gallbladder is a potential source of mea-
surement error when it cannot be distinguished from the
wall proper. This will relate to the dynamic range of the
ultrasound system and the collagen content of the fat.
(While it appeared that the gallbladder wall could be dis-
tinguished from fat within the porta hepatis in this study,
wall thickness measurements should be assessed with
reservation in the obese subject until this factor has been
clarified by additional study.)
Chronic cholecystitis appears to evolve as a recurrent
inflammatory process. The pathology of the wall includes
variable components of mononuclear cellular infiltration
and fibrosis. Levine has subdivided chronic cholecystitis
pathologically and temporally into hypertrophic, transitional
and atrophic stages (8). The ultrasound image features
which are anticipated for any of these stages are increased
thickness of the wall corresponding to cellular infiltration
(and local muscle hypertrophy or hyperplasia) and en-
hanced reflectivity with fibrosis.
The results indicate that thickening of the gallbladder
wall as measured herein corresponds to pathologic
thickening associated with chronic cholecystitis. The
finding that average wall thickness is greater in subjects
with cholelithiasis than in those without stone disease (p
< .001) also supports the contention that this feature is a
discriminant of chronic cholecystitis, albeit indirectly. In-
creased wall thickness was noted in surgical subjects with
chronic cholecystitis alone and with combined acute and
chronic changes.
Increased wall thickness is one of the pathologic hall-
marks of chronic cholecystitis, but it is not found in half of
patients by the time of surgery. This would suggest that
ultrasound assessment would be expected to have high
specificity but low sensitivity in this diagnostic task. Cor-
relation of wall thickness and functional tests such as
Tc-99m HIDA would be of interest. No patient in the non-
surgical, noncholelithiasis group had a wall thickness
greater than 5 mm. Some 3.5 % of that group had 3-5mm
thickness which may represent either anatomic variation
or occult acalculous cholecystitis. It is also possible that,
because fasting was not required before examination,
some gallbladders may have been contracted, physio-
logically thickening the wall (Fig. 3). There was insignificant
change in wall thickness after fasting if the maximal
cross-sectional diameter of the lumen on initial study was
1.5 cm or greater. Fasting examination was required for
gallbladders with a smaller initial luminal diameter. Some
but not all, of this latter group showed increased distension
of the lumen and a thinner wall on the repeat study.
Increased reflectivity is anticipated with fibrosis and was
observed with chronic cholecystitis, but refinement of this
697 Ultrasound
feature as a diagnostic sign awaits the development of a
standardized tissue characterization technique for quan-
titating regional collagen content. Sanders and Zerhouni
(11) and Taylor et a/. (12) have noted increased reflectivity
and thickening of the wall in the presence of ascites, so
that wall thickness measurements should not be applied
diagnostically as a sign of cholecystitis in this situation.
A separate, relatively hypoechoic annulus was visual-
ized interior to the echodense gallbladder margin in several
normal but contracted gallbladders and in 8 subjects pre-
sumed to have acute cholecystitis on clinical grounds.
Pathologic confirmation was available in 3. Sanders and
Zerhouni (11) and Marchal et a/. (9) report this pattern in
some cases of acute cholecystitis. This zone is identified
tentatively as the mucosa and is distinguished from wall
thickening due to changes within the muscularis or serosa.
This identification corresponds to separation of acute in-
flammatory and infiltrative processes from chronic in-
flammation and is j~ stifled teleologically but must be
substantiated by further observation.
Attention has been directed towards the use of a high-
speed imaging device for ultrasound cholecystography.
Two operational factors require further comment. The
examination is concluded rapidly, so that it is practical to
extend the scope of the study to regions outside the right
upper quadrant when gallbladder examination is requested.
Discussion of this approach is beyond the scope of this
report, but the value of treating the ultrasound study as a
problem-oriented technique rather than as a form of re-
gional anatomic study is suggested by the findings noted
in TABLE II. Conversely, examination of the gallbladder can
be included in any abdominal/pelvic or cardiac imaging
study. This is important in the context of the present report
as a means of defining population norms not currently
available. It is assumed, for example, that cholelithiasis
is pathological; however, this may represent an artefact
of only using diagnostic detection methods in subjects with
symptomatic presentations.
The object of the present study has been to show that
gallbladder wall thickness can be measured ultrasonically
with millimeter range accuracy and that those measure-
ments correspond to well-known anatomic and pathologic
variations. Inclusion of gallbladder wall measurement in
routine ultrasound cholecystography is recommended as
a means of establishing the clinical utility of this feature
in general use.
ACKNOWLEDGMENT: We wish to thank Linda Higgins Evans for her time
and secretarial skills in preparing this manuscript.
REFERENCES
1. Anderson JC, Harned RK: Gray scale ultrasonography of the
gallbladder: an evaluation of accuracy and report of additional ultra-
sound signs. Am J RoentgenoI129:975-977, Dec 1977
2. Bartrum RJ, Crow HC. Foote SA: Ultrasonic and radiographic
cholecystography. N Engl J Med 296:538-541, 10 Mar 1977
3. Birnholz JC: Combined ultrasound imaging and physical ex-
698 HARRIS J. FINBERG AND JASON
amination: editorial review of phased array sector scanning techniques
and applications. J Beige Radiol 61:463-469, 1978
4. Crade M, Taylor KJW, Rosenfield AT, et al: Surgical and
pathologic correlation of cholecystosonography and cholecystography.
Am J Roentgenol 131:227-229, Aug 1978
5. Handler SJ: Gray scale ultrasonic detection of gallbladder wall
thickening: Its association with acute and chronic cholecystitis. (Abstract
for Presentation at AlUM 1978 Scientific Meeting.) Reflections 4:
182-183,1978
6. Lawson TL: Gray scale cholecystosonography: diagnostic
criteria and accuracy. Radiology 122:247-251, Jan 1977
7. Leopold GR, Amberg J, Gosink BB, et al: Gray scale ultrasonic
cholecystography: a comparison with conventional radiographic
techniques. Radiology 121:445-448, Nov 1976
8. Levine T: Chronic Cholecystitis: Its Pathology and the Role
of Vascular Factors in Its Pathogenesis. New York, Halsted Press, John
Wiley and Sons, 1975
9. Marchal G, Crolla 0, Baert AL, et al: Gallbladder wall thick-
ening: a new sign of gallbladder disease visualized by gray scale
cholecystosonography. J Clin Ultrasound 6: 177-179, 1978
C. BIRNHOLZ December 1979
10. O'Brien WD Jr: The role of collagen in determining ultrasonic
propagation properties in tissue. [In] Kessler LW, ed: Acoustical
Holography. New York, Plenum Press, Vol 7, 1976
11. Sanders RC, Zerhouni E: The significance of ultrasonic gall-
bladder wall thickening. (Abstract for Presentation at AlUM 1978 Sci-
entific Meeting.) Reflections 4:189, 1978
12. Taylor KJW, Rosenfield AT, DeGraaff CS: Anatomy and pa-
thology of the biliary tree as demonstrated by ultrasound. [In] Taylor
KJW, ad: Diagnostic Ultrasound in Gastrointestinal Disease. New York,
Churchill Livingstone, 1979, pp 103-121
13. Weissberg DL, Gosink B: Gray scale evaluation of the gall-
bladder. Applied Radiol 7: 113-118, 1978
Harris J. Finberg, M.D.
Department of Radiology
Harvard Medical School
25 Shattuck Street
Boston, MA 02115