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773
Sonographic Normal and
Michel
Rioux1
Detection Abnormal
of the Appendix
A prospective study of 170 patients with suspected appendicitis was performed assess the value of sonography in detecting the normal and abnormal appendix. wall thickness (normal, s3 mm), compressibility of the appendix, and echogenicity surrounding
fat were
the
primary
criteria
used
to determine
the
status
of the
to The of
appendix.
Of 60 patients who underwent surgery, appendicitis was proved in 45. The remaining I 10 patients who did not have surgery, contacted by telephone at the end of the study, had no clinical follow-up evidence of acute appendicitis. A normal appendix was clearly identified
in 102
(82%)
of
125
patients
without
acute
appendicitis.
The
sensitivity
of
sonographic examination in detecting appendicitis was 93%, the specificity was 94%, and the accuracy was 94%. The predictive value of a positive test was 86%; that of a negative test was 98%. Ruptured appendicitis was predicted in all cases (11/11). Sonography is useful in detecting acute appendicitis and can clearly show the normal appendix more frequently than previously reported. AJR
158:773-778,
April
1992
Since the original report by in the diagnosis of appendicitis 1 2]. Sonographic findings of scribed; inability to visualize normal appendix. However,
appendicitis
is reported
Puylaert [1] in 1 986, the use of sonography as a tool has become the subject of considerable study [2the abnormal appendix have been previously dethe appendix has been considered diagnostic of a the sensitivity of sonography in the detection of
to be between
80% and 94%, and basically,
more than
50% of patients (who had surgery or not) in previous studies [1 2, 5-8, 1 2] were considered by the sonographer to have a normal appendix. Clinicians remain aware that a normal sonographic examination does not completely rule out appendicitis, and they still face the same dilemma in about 50% of their patients, regardless of the sonographer’s conclusion. The goals of the study were to optimize visualization of the appendix in all patients with suspected acute appendicitis and to evaluate whether visualization improved the overall accuracy of sonography in the diagnosis of a normal or abnormal appendix. ,
Subjects
Received June 1 7, 1991 ; accepted after revision October29, 1991. I Department of Radiology, H#{244}pitalSaint-Frangois d’Assise,
10, rue do l’Espinay,
Qu#{233}bec,Qu#{233}requests to
bec, Canada G1 L 3L5. Address reprint M. Rioux. 0361 -803X/92/1 584-0773 C American Roentgen Ray Society
and Methods
From June 1 988 to September 1989, 170 consecutive patients with clinically suspected appendicitis had sonography of the right side of the abdomen. All patients were selected by
the general physician surgeon.
in the emergency department. Most of them also were evaluated by a was aware of the sonographic diagnosis in all cases, but the decision was not known at the time of sonography. This study group comprised 100
The
surgeon
to operate females and 70 males 4-73 years old (mean, 26.5 years). A complete examination of the abdomen and the pelvis was performed in all patients by using a 3.5-MHz sector scan transducer (Acuson 1 25, Mountain View, CA). The right hemiabdomen was then examined specifically with a 5-MHz linear-array transducer (Acuson
774
RIOUX
1 25);
in a few
cases
a 5- or 7.5-MHz
sector-scan
transducer
(Diason-
criteria
400, Milpitas, CA) was used. The 5-MHz linear-array transducer was placed transversely below the edge of the right hepatic lobe, in front ofthe right kidney. Moving slowly downward to the right
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iCs DRF
iliac
fossa,
in every
we
searched
patient
as the
wall.
The colon
more
frequently,
peristalsis
for
was full
was
the
largest
either
ascending
round
Colon.
or oval
full of fluid
structure
helpful
helpful
by its fatty The
by a
or anechoic)
or,
of feces (hypereChoiC). The absence of vigorous
often
in differentiating
or cecum. the vicinity
recognized
delimited
(hypoechoic
in distinguishing
colon
The ileocecal valve was then identified. distinguished
It was
component.
The
an enlarged
appendix
was
finally
sought
from
was
collapsed
in the transverse
ileum plane
in
from
the
Cecum
Scanning
was
position,
which
for about
for 10 mm. Even though
continued
to identify on transverse could
done was
with
often
be
identified
the patient
supine
helpful
in patients
On the basis of our previous nation
of
patients
and
the appendix
was easiest
images, the origin of the appendix
pathologic
with
experience specimens
on
longitudinal
a retrocecal
decubitus
appendix.
with sonographic of
the
arising images.
in the left lateral
appendix,
identifying
a normal
tubular,
for
blind-ended
structure;
serosa)
of 3 mm
examiour
or less,
appendix
included
wall thickness
with
or without
A diagnosis
of appendicitis
pressibility was reduced thickness was greaterthan echogenicity
was
made
April1992
a compressible,
(lumen
interface
to
echogenic
material (gas and or feces); absence of peristalsis; echoic surrounding fat [2] (Fig. 1).
decreased
bowel.
of penstalsis
degree
appendix
small
valve was often
10 mm, by using the graded compression technque previously described [1 ]. The search was made while the patient had a full bladder. If the appendix was not clearly visualized, the patient was asked to empty the bladder and scanning
of the cecum
from
Bowin’s
AJR:158,
when
intraluminal and normal hyper-
appendiceal
corn-
or absent, or when the transverse wall 3 rnrn. Other signs ofappendicitis included of the surrounding
fat or the presence
of a
defined hypoechoic round or oval structure, adjacent to the cecurn and independent of loops of bowel. Criteria for appendiceal rupture were clear asymmetry in wall poorly
thickness
with
indistinctness
of wall
layer
or the
presence
or fluid collection around the appendix (Fig. 2). Although the number of cases in which the appendix visualized
was tabulated,
for statistical
purposes,
of an air
was not
an appendix
was
considered
normal if it was not visualized. Sixty patients had surgery within 24 hr of the sonographic exarnination. Surgical specimens in 25 patients with appendicitis and nine patients with normal appendices were studied with the same sonographic transducers after the specimens were submerged in a water bath. With the assistance of a pathologist, a section of the specimen was obtained for histology at the site of optimal sonographic visualization ofwail thickening or at a specific point of interest(e.g., ruptured
Fig. 1.-Normal
appendixes.
A, Axial sonogram across two sactions of normal but tortuous appendix (black arrows). Wall has typical three-
ring appearance.
Hyperechoic
inter-
face (i) of collapsed lumen and inner hypoechoic ring of mucosa is indicated (lower white line). Serosa (5) (upper whltellne)ls defined as outer boundary of hypoechoic ring of muscularis propria. Wall thickness (2.2 mm) Is dlstance between these two levels. B, Photograph of histologic specimen (transverse section) shows differant layers of wall of appendix seen in A: m = mucosa, sm submucosa, mp = muscularls proprla, L = lymphold folhide. Wall thickness is measured between luminal interface (i) and serosa (a).
C, Sonogram of normal appendix seen both transversely (solid arrow) and longitudinally(arrowheads)in a 13year-old boy. Inner hypoechoic ring (open arrow) is thicker than usual because of lymphoid hyperplasia. w = abdominal wall, i = iliac vessel D, Sonogram clearly shows normal appendix in longitudinal section (arrowheads).
AJR:158,
area). The actual findings
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SONOGRAPHY
April 1992
by this
wall thickness
was correlated
OF
NORMAL
with sonographic
technique.
The 11 0 patients who did not have surgery were all contacted by telephone at the end of the study (mean, 8.6 months) to ascertain whether they had undergone surgery for appendicitis at another hospital.
Results Patients
Who Had Surgery
Of the 170 patients clinically suspected of having appendicitis, 60 underwent surgery. Forty-five had pathologically proved appendicitis, including five cases with histologic evidence of chronic inflammation with superimposed acute signs of inflammation of the appendix (Fig. 3). Of these patients, appendicitis was correctly diagnosed preoperatively by sonography in 42. Histologic and sonographic correlation was done in 25 cases of appendicitis. The proximal part of the appendix was the most accurate site for measuring wall thickness, and hyperechoic fat made the submucosa a useful
Fig. 2.-Ruptured
appendix.
A, Axial sonogram of enlarged appendix (arrow). Right half of appendix (starting at level of arrowheads) shows asymmetric hypoechoic wall without hyperechoic submucosal layer. This area represents inflammatory necrosis
of wall with rupture. B, Longitudinal sonogram of distal part of same appendix shows a hypeechoic, poorly defined tubular structure (arrows) without distinct wall vlsualization. w = abdominal wall
Fig.
3.-Chronic
appendicitis
diag-
nosed on basis of sonographic findings and medical history, despite resolution of pain and leukocytosis at time of sonography and surgery. A, Longitudinal sonogram shows enlarged uncompressible appendix (arrows). w = abdominal wall. B, Photograph of magnified transverse histologic section of appendix shows atrophied mucosa (m). Chronic inflammation is shown by replacement of fat in submucosa (am) by extensive fibrosis, which extends also into muscularis propria (mp). Arrows identify borders between mucosa and submucosa and between submucosa and
muscularis
propria.
AND
ABNORMAL
APPENDIX
775
landmark for identifying the wall on sonography. Clear distinction ofthe layers of the wall allowed an accurate measurement in 21 cases. The wall thickness on sonography varied between 3.3 and 7.5 mm (mean, 4.55 mm). Corresponding values by histopathology varied between 3.5 and 7.7 mm (mean, 4.58). Thirteen cases of appendicitis had advanced wall inflammation in the distal half, which was indistinguishable on sonography from hypoechoic intraluminal pus. Similarly, the appendiceal wall was not clearly visualized in four other cases, and noncompressibility as well as findings of periappendicitis were criteria used to diagnose appendicitis. Three studies were incorrectly interpreted as normal. One false-negative examination occurred with nonvisualization of a retrocecal appendix in an obese patient, although pain occurred with transducer compression in the right lower quadrant. Another case involved an initial interpretive error; retrospectively, the sonogram showed classic signs of appendicitis with a wall thickness of 4.5 mm and hypoechoic surrounding fat with a small amount of ascites (Fig. 4). In the third case, only the proximal half of a normal appendix was
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echoic mass was seen at sonography and confused with appendicitis; this error in diagnosis has been previously described [3] (Fig. 6). Finally, one patient had a small pericecal abscess due to cecal perforation by a foreign body. The hypoechoic mass contained increased central echoes that were falsely interpreted as a ruptured appendix (Fig. 7). This pitfall also has been described before [4]. In addition to this last case, perforation of the appendix was suggested by sonography in 1 1 cases and confirmed surgically in all cases.
seen on sonography. Because of persistent symptoms, the patient underwent surgery and was found to have inflammatory changes in the distal appendix. Of the 60 patients who had surgery, 1 5 were found to have a normal appendix at the time of the operation. Twelve cases were correctly diagnosed by sonography. Of these, a normal appendix was identified in nine cases showing identical correlation between the histopathologic specimen and such sonographic findings as clear wall distinction (nine cases), wall thickness (varying in both techniques between 0.5 and 3 mm; mean, 1 .8 mm), the presence of enlarged lymphoid hyperplasia in the wall (two cases), a complete luminal collapse (three cases), or a lumen fully distended by feces (six cases); this correlation suggested that the structure visualized at sonography was indeed the appendix. In the other three cases, the appendix was not clearly identified, but was considered to be normal by sonography for statistical purposes. Three patients with normal appendixes at surgery had abnormal sonographic findings. Of note, a pericecal inflammatory process was found during surgery in all three. One patient had Meckel peridiverticulitis with a fecalith (Fig. 5), a condition easily confused with necrotized appendicitis containing a fecalith. Another patient had chronic inflammation of the right salpinx and ovary adjacent to a normal appendix. A tubular, poorly defined, hypo-
Patients
Who Did Not Have Surgery
All 1 10 patients who did not have surgery had clinical followup over a period varying between 1 and 1 4 months (mean, 8.6 months). Of these, 89 normal appendixes were clearly seen at sonography and another 1 7 cases were considered normal on sonography although the appendix was not visualized. At follow-up, none of these 1 06 patients had recurrent pain in the right lower quadrant. Diagnoses in four patients who did not have surgery but had abnormal sonographic findings were considered false positive for appendicitis by sonography. Sonography in all four showed the typical threering appearance of the appendix in transverse views, a wall thickness greater than 3 mm, and absence of compressibility.
Fig. 4.-Appendicitis
penap-
with
pendicitis. A, Axial sonogram
ring appearance (solid
arrows).
shows multipleof enlarged appendix
Although
hyperechoic
ring of submucosa (open arrow) is proserved, asymmetric hypoechoic region (arrowheads) represents muscular layerwith periappendicitls. w = abdomlnal wall, p = psoas. B, Longitudinal
sonogram
of same
enlarged appendix (solid arrows). Thick hypoechoic layer represents muscularls propria and periappendiitie (open arrows). w = abdominal wall.
,
-
‘
__:_. #{163}
Ac;.
a.. F .
-sm
..‘
k
4
ii,
_____
Fig. 5.-Meckel peridiverticulitis caused by fecalith misdiagnosed as appendicitis with fecalith in 39-year-old woman. A, Axial sonogram of right abdominal
fossa, inferior to cecum, shows hypeechoic, poorly defined mass (arrowheads) containing a fecalfth (arrow). B, Photograph of histologic section of corresponding specimen shows antimesenteric wall of ileum (I = lumen, m = mucosa sm = submucosa, mp =
muscularis
propna).
diverticulum
(arrow).
Inflamed F
=
fecalith.
Meckel
AJR:158,
Fig. 6.-Pseudoappendicitis.
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SONOGRAPHY
April 1992
OF
NORMAL
AND
ABNORMAL
I
Longi-
777
APPENDIX -:-:
‘
I
tudinal sonogram shows hypoechoic, poorly defined sausagelike mass (solid arrows) without distinct walls adjacent to gas-filled (open arrows) cecum (C) mimicking appendicitis. A chronic in-
1’
.i..,.
.
V.
-&-
---
_
flammatory process of right salplnx and ovary unexpectedly located inferior to cecum was noted at surgery.
Fig. 7.-Pseudoappendicltis with rupture. Under collapsed cecum (c) (arrowheads) sonogram shows oval, hypoechoic, poorly defined mass (arrows) containing hyperechoic material and suggesting ruptured appendix. At surgery, a cecal perforation from foreign body with small infracecal abscess was found.
However, because the symptoms resolved almost completely within a few hours after sonography, the patients were released without surgery. Three of them had a chronic history of recurrent pain in the right iliac fossa. All three patients still reported recurrent episodes of abdominal pain lasting from 4 to 1 0 hr at the time of follow-up. The last patient with an enlarged appendix at sonography who did not have surgery had no recurrence of symptoms. Of 125 patients without appendicitis, a normal appendix was clearly visualized in 1 02 cases (82%). On the other hand, our entire study group included 21 cases (1 2%) in which the appendix was not seen on sonography. Sonography in 170 patients enabled the diagnosis of acute appendicitis with a sensitivity of 93%, a specificity of 94%, a positive predictive value of 86%, a negative predictive value of 98%, and an accuracy of 94%.
Discussion Preoperative diagnosis of acute appendicitis remains a difficult clinical problem. Barium enema examination is considered to be an unreliable test for acute appendicitis because of its large percentage of false-positive and false-negative results [1 3]. Laparoscopy is invasive and has limited use in patients who have had surgery or patients with retrocecal appendixes. Recently, CT has been used as a diagnostic tool to identify patients with appendicitis, but it is not always readily available and requires ionizing radiation and the use of IV contrast material [1 4]. Sonography is a readily available, inexpensive, noninvasive test, with a reported sensitivity of 80-94% in the detection of acute appendicitis [1 2, 5, 6, 8, 1 0, 12]. Significant obesity and overlying loops of gas-filled bowel may give sonography a lower sensitivity in some cases. The most frequent sonographic findings in acute appendicitis are noncompressibility of the appendix with a wall diameter greater than 6 mm [5]. However, as visualization of a normal appendix was unusual in many reported series, a nonvisualized appendix was considered normal. Recently, Vigneault et al. [1 2] reported the sonographic visualization of ,
a normal appendix (diameter, 6 mm) in 1 0 oftheir 35 patients without appendicitis. In our study, we identified the normal appendix by sonography in 1 02 (82%) of 1 25 patients without surgically proved appendicitis. Complete sonographic and histologic correlation in nine resected normal appendixes suggested that the structure identified at sonography was indeed the appendix. Our success in visualizing the normal appendix by sonography may be related to added effort and time spent in searching for the cecum and the appendix. Examination of patients with a full bladder and then after micturition was helpful in localizing the normal appendix in many cases, but was not useful in any case of acute appendicitis. The point of maximal tenderness was not always related to the position of the appendix in normal cases, but was useful in locating all cases of appendicitis. Finally, our early experience with sonographic inspection of surgical (colectomy and right hemicolectomy) specimens by submersion in a water bath was helpful in recognizing the sonographic appearances of the colon, the ileocecal valve, and the normal appendix. In our series, sonography had a sensitivity of 93% and specificity of 94% in detecting acute appendicitis, comparable to those in previous studies [1 -8, 12]. Identification of a normal appendix in 82% of patients and a negative predictive value of 98% had a major impact on our surgeons in increasing test credibility. We had only two false-negative cases (1 .9%) out of 104 normal sonographic diagnosis with clear sonographic visualization of the appendix. On the other hand, of 21 normal sonographic diagnoses without sonographic visualization of the appendix, we had one false-negative finding (4.8%). Comparing the number of false-negative cases in our group of normal sonographic diagnoses with good visualization of the appendix (two of 104), and the number of false-negative cases coming from the whole group with normal sonographic diagnosis without visualization of the appendix (30 of 345) found in previous studies [1 2, 5, 6, 8, 12], we found a significant difference between the two groups (chi-square value 5.538, df 1 p .01 9). On the other hand, when we compared the number of false-negative cases in our group of normal sonographic diagnoses without visual,
=
=
,
=
778
RIOUX
ization of the appendix (one of 21 ), and the corresponding value from the latter group (30 of 345), we found no difference between groups (chi-square value 0.31 5, df 1, p .53). Therefore, visualization of the normal appendix on sonography appears advantageous in reducing the percentage of false-negative cases; it allowed a negative predictive value of 98% in our study. Our sonographic criteria for a normal appendix were reliable because the appendix was compressible, surrounded by normal-appearing fat, and had a distinct wall less than 3 mm thick. It is also noteworthy that six normal appendixes had a full transverse diameter of more than 6 mm because of luminal dilatation by feces, although they had a very thin wall and were compressible. Had other established criteria been used, these appendixes might have been considered abnormal because of their overall diameter. In 35 of 42 cases of appendicitis diagnosed by sonography, the wall was clearly visualized in at least one area and was more than 3 mm thick. In the seven other cases, wall detection was difficult because the advanced mural inflammation led to a similar appearance with hypoechoic luminal contents. For that reason, the presence of a hypoechoic oval, round, or tubular noncompressible structure with indistinct borders with modified surrounding fat located in the vicinity of the cecum was used for the sonographic diagnosis of appendicitis (Fig. 2B). Detailed analysis of our three false-negative cases of appendicitis by sonography demonstrated the importance of complete visualization of the entire appendix, because only part of it might be involved by the inflammatory process. It also indicated that in such studies, echogenicity in some patients may be inadequate, usually owing to obesity or ileus, to allow 1 00% safety in ruling out disease in the abdomen with sonography. The positive predictive value of sonography for appendicitis (86%) is slightly lower than that found in other studies (between 89% and 93%) [1 , 2, 5, 6, 8, 10, 1 2]. Of the seven patients with false-positive results, three underwent laparotomy and had inflammatory processes requiring surgery. Appendicitis was incorrectly diagnosed by sonography because of the findings of an uncompressible, hypoechoic, round or tubular structure surrounded by abnormal fat near the cecum. In none was the appendiceal wall clearly visualized. These observations raise the possibility that the diagnosis in these three cases would not have been made if the sonographer had restricted the diagnosis of appendicitis to only those cases showing a classical appearance of an enlarged appendix (i.e., three well-visualized distinct wall rings on transverse views). Our additional abdominal sonographic criteria for appendicitis (excluding the wall thickness) may have slightly decreased our specificity for appendicitis, but they seem quite accurate in detecting other abnormalities mimicking appendicitis and also requiring treatment by surgery. Four other cases were false positive on sonography, each having a noncompressible appendix clearly visualized by sonography with a wall thickness greater than 3 mm. These patients did not have surgery because of their rapidly resolving symptoms and also because three of them had previous episodes of abdominal pain with rapid resolution. The three
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=
=
AJR:158,
April 1992
patients still reported recurrent episodes of pain in the same location when they were contacted at the end of the study. None has been operated on so far, and none has undergone subsequent sonographic evaluation. In retrospect, we suggest that they might represent cases of subacute or chronic appendicitis [1 5]. To further support that hypothesis, this study reports five other similar patients who underwent surgery. Four of them were asymptomatic with a normal WBC count shortly before surgery. All patients had histologic evidence of chronic inflammation with superimposed acute signs of inflammation with various degrees of severity. We suggest that the decision for surgery in such cases was in large part conditioned by the fact that the patients were examined in the last 6 months of the study, a period correlating with the surgeon’s increased confidence in our sonographic criteria for appendicitis. In conclusion, our results suggest that a normal appendix can be visualized sonographically far more frequently than previously suspected. The wall thickness of the appendix appeared to be a useful index of the status of the appendix. The 98% negative predictive value of sonography for appendicitis in conjunction with actual visualization of the normal appendix in most cases may increase the confidence of surgeons in the use of sonography for their occasionally difficult clinical situations. In our study, a search for sonographic visualization of the normal as well as the abnormal appendix seems to significantly reduce our percentage of false-negative cases, this being one of our major goals. REFERENCES 1
.
Puylaert JBCM. sion. Radiology
2. Abu-Yousef Metcalf
Acute
appendicitis:
US evaluation
using graded
compres-
1986:158:355-360 MM, Bleichaer JJ, Maher JW, Urdaneta LF, Franken EA Jr,
AM.
High
resolution
sonography
of
acute
appendicitis.
AJR
1987;149:53-58 3. Terry J, Forest T. Sonographic demonstration of salpingitis: potential confusion with appendicitis. J Ultrasound Med 1989;8:39-41 4. Machan L, Pons MS, Wood BJ, Wong AD. The “coffee bean” sign in periappendiceal and pendiverticular abscess. J Ultrasound Med
1987;6:373-375 5. Jeffrey
RB Jr, Laing
FC, Townsend
RR. Acute
appendicitis:
sonographic
criteria based on 250 cases. Radiology 1988;167:327-329 6. Jeffrey RB Jr, Laing FC, Lewis FR. Acute appendicitis: high resolution realtime USfindings. Radiology 1987;163:11-14 7. Gaensler EHL, Jeffrey RB Jr, Laing FC, Townsend RR. Sonography in patients with suspected acute appendicitis: value in establishing alternative diagnosis. AiR 1989;1 52:49-51 8. Kang WM, Lee CH, Chou YH, et al. A clinical evaluation of ultrasonography in the diagnosis of acute appendicitis. Surgery 1989;1 05:154-159 9. Fa EM, Cronan JJ. Compression as an aid in the differential diagnosis of appendicitis. Surg Gynecol Obstet 1989;169:290-298 10. Bilbey JH, Gibney RG, Cooperberg PL. tJtrasonography in acute appendicitis. J Can Assoc Radiol 1989;40:22-24 1 1 . Poole GV. Appendicitis: the diagnostic challenge continues. Am Surg
1988;54:609-612 1 2.
Vigneault F, Filiatrault 0, Brandt ML, et al. Acute appendicitis in children: evaluation with US. Radiology 1990;176:501-504 13. Rajagopalan AE, Manson JH, Kennedy M, Pawlikowski J. The value of the baryum enema in the diagnosis of acute appendicitis. Arch Surg 1977;1 12:531 -533 14. Balthazar EJ, Megibow AJ, Siegel SE, et al. Appendicitis: prospective evaluation with high-resolution CT. Radiology 1991;180:21-24 1 5. Oachman AH, Nichols JB, Patrick PH, et al. Natural history of the obstructed rabbit appendix: observation with radiography, sonography, and CT. AJR 1987;148:281-284
773
Sonographic Normal and
Michel
Rioux1
Detection Abnormal
of the Appendix
A prospective study of 170 patients with suspected appendicitis was performed assess the value of sonography in detecting the normal and abnormal appendix. wall thickness (normal, s3 mm), compressibility of the appendix, and echogenicity surrounding
fat were
the
primary
criteria
used
to determine
the
status
of the
to The of
appendix.
Of 60 patients who underwent surgery, appendicitis was proved in 45. The remaining I 10 patients who did not have surgery, contacted by telephone at the end of the study, had no clinical follow-up evidence of acute appendicitis. A normal appendix was clearly identified
in 102
(82%)
of
125
patients
without
acute
appendicitis.
The
sensitivity
of
sonographic examination in detecting appendicitis was 93%, the specificity was 94%, and the accuracy was 94%. The predictive value of a positive test was 86%; that of a negative test was 98%. Ruptured appendicitis was predicted in all cases (11/11). Sonography is useful in detecting acute appendicitis and can clearly show the normal appendix more frequently than previously reported. AJR
158:773-778,
April
1992
Since the original report by in the diagnosis of appendicitis 1 2]. Sonographic findings of scribed; inability to visualize normal appendix. However,
appendicitis
is reported
Puylaert [1] in 1 986, the use of sonography as a tool has become the subject of considerable study [2the abnormal appendix have been previously dethe appendix has been considered diagnostic of a the sensitivity of sonography in the detection of
to be between
80% and 94%, and basically,
more than
50% of patients (who had surgery or not) in previous studies [1 2, 5-8, 1 2] were considered by the sonographer to have a normal appendix. Clinicians remain aware that a normal sonographic examination does not completely rule out appendicitis, and they still face the same dilemma in about 50% of their patients, regardless of the sonographer’s conclusion. The goals of the study were to optimize visualization of the appendix in all patients with suspected acute appendicitis and to evaluate whether visualization improved the overall accuracy of sonography in the diagnosis of a normal or abnormal appendix. ,
Subjects
Received June 1 7, 1991 ; accepted after revision October29, 1991. I Department of Radiology, H#{244}pitalSaint-Frangois d’Assise,
10, rue do l’Espinay,
Qu#{233}bec,Qu#{233}requests to
bec, Canada G1 L 3L5. Address reprint M. Rioux. 0361 -803X/92/1 584-0773 C American Roentgen Ray Society
and Methods
From June 1 988 to September 1989, 170 consecutive patients with clinically suspected appendicitis had sonography of the right side of the abdomen. All patients were selected by
the general physician surgeon.
in the emergency department. Most of them also were evaluated by a was aware of the sonographic diagnosis in all cases, but the decision was not known at the time of sonography. This study group comprised 100
The
surgeon
to operate females and 70 males 4-73 years old (mean, 26.5 years). A complete examination of the abdomen and the pelvis was performed in all patients by using a 3.5-MHz sector scan transducer (Acuson 1 25, Mountain View, CA). The right hemiabdomen was then examined specifically with a 5-MHz linear-array transducer (Acuson
774
RIOUX
1 25);
in a few
cases
a 5- or 7.5-MHz
sector-scan
transducer
(Diason-
criteria
400, Milpitas, CA) was used. The 5-MHz linear-array transducer was placed transversely below the edge of the right hepatic lobe, in front ofthe right kidney. Moving slowly downward to the right
Downloaded from www.ajronline.org by Grand Valley State University on 10/29/13 from IP address 148.61.13.133. Copyright ARRS. For personal use only; all rights reserved
iCs DRF
iliac
fossa,
in every
we
searched
patient
as the
wall.
The colon
more
frequently,
peristalsis
for
was full
was
the
largest
either
ascending
round
Colon.
or oval
full of fluid
structure
helpful
helpful
by its fatty The
by a
or anechoic)
or,
of feces (hypereChoiC). The absence of vigorous
often
in differentiating
or cecum. the vicinity
recognized
delimited
(hypoechoic
in distinguishing
colon
The ileocecal valve was then identified. distinguished
It was
component.
The
an enlarged
appendix
was
finally
sought
from
was
collapsed
in the transverse
ileum plane
in
from
the
Cecum
Scanning
was
position,
which
for about
for 10 mm. Even though
continued
to identify on transverse could
done was
with
often
be
identified
the patient
supine
helpful
in patients
On the basis of our previous nation
of
patients
and
the appendix
was easiest
images, the origin of the appendix
pathologic
with
experience specimens
on
longitudinal
a retrocecal
decubitus
appendix.
with sonographic of
the
arising images.
in the left lateral
appendix,
identifying
a normal
tubular,
for
blind-ended
structure;
serosa)
of 3 mm
examiour
or less,
appendix
included
wall thickness
with
or without
A diagnosis
of appendicitis
pressibility was reduced thickness was greaterthan echogenicity
was
made
April1992
a compressible,
(lumen
interface
to
echogenic
material (gas and or feces); absence of peristalsis; echoic surrounding fat [2] (Fig. 1).
decreased
bowel.
of penstalsis
degree
appendix
small
valve was often
10 mm, by using the graded compression technque previously described [1 ]. The search was made while the patient had a full bladder. If the appendix was not clearly visualized, the patient was asked to empty the bladder and scanning
of the cecum
from
Bowin’s
AJR:158,
when
intraluminal and normal hyper-
appendiceal
corn-
or absent, or when the transverse wall 3 rnrn. Other signs ofappendicitis included of the surrounding
fat or the presence
of a
defined hypoechoic round or oval structure, adjacent to the cecurn and independent of loops of bowel. Criteria for appendiceal rupture were clear asymmetry in wall poorly
thickness
with
indistinctness
of wall
layer
or the
presence
or fluid collection around the appendix (Fig. 2). Although the number of cases in which the appendix visualized
was tabulated,
for statistical
purposes,
of an air
was not
an appendix
was
considered
normal if it was not visualized. Sixty patients had surgery within 24 hr of the sonographic exarnination. Surgical specimens in 25 patients with appendicitis and nine patients with normal appendices were studied with the same sonographic transducers after the specimens were submerged in a water bath. With the assistance of a pathologist, a section of the specimen was obtained for histology at the site of optimal sonographic visualization ofwail thickening or at a specific point of interest(e.g., ruptured
Fig. 1.-Normal
appendixes.
A, Axial sonogram across two sactions of normal but tortuous appendix (black arrows). Wall has typical three-
ring appearance.
Hyperechoic
inter-
face (i) of collapsed lumen and inner hypoechoic ring of mucosa is indicated (lower white line). Serosa (5) (upper whltellne)ls defined as outer boundary of hypoechoic ring of muscularis propria. Wall thickness (2.2 mm) Is dlstance between these two levels. B, Photograph of histologic specimen (transverse section) shows differant layers of wall of appendix seen in A: m = mucosa, sm submucosa, mp = muscularls proprla, L = lymphold folhide. Wall thickness is measured between luminal interface (i) and serosa (a).
C, Sonogram of normal appendix seen both transversely (solid arrow) and longitudinally(arrowheads)in a 13year-old boy. Inner hypoechoic ring (open arrow) is thicker than usual because of lymphoid hyperplasia. w = abdominal wall, i = iliac vessel D, Sonogram clearly shows normal appendix in longitudinal section (arrowheads).
AJR:158,
area). The actual findings
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SONOGRAPHY
April 1992
by this
wall thickness
was correlated
OF
NORMAL
with sonographic
technique.
The 11 0 patients who did not have surgery were all contacted by telephone at the end of the study (mean, 8.6 months) to ascertain whether they had undergone surgery for appendicitis at another hospital.
Results Patients
Who Had Surgery
Of the 170 patients clinically suspected of having appendicitis, 60 underwent surgery. Forty-five had pathologically proved appendicitis, including five cases with histologic evidence of chronic inflammation with superimposed acute signs of inflammation of the appendix (Fig. 3). Of these patients, appendicitis was correctly diagnosed preoperatively by sonography in 42. Histologic and sonographic correlation was done in 25 cases of appendicitis. The proximal part of the appendix was the most accurate site for measuring wall thickness, and hyperechoic fat made the submucosa a useful
Fig. 2.-Ruptured
appendix.
A, Axial sonogram of enlarged appendix (arrow). Right half of appendix (starting at level of arrowheads) shows asymmetric hypoechoic wall without hyperechoic submucosal layer. This area represents inflammatory necrosis
of wall with rupture. B, Longitudinal sonogram of distal part of same appendix shows a hypeechoic, poorly defined tubular structure (arrows) without distinct wall vlsualization. w = abdominal wall
Fig.
3.-Chronic
appendicitis
diag-
nosed on basis of sonographic findings and medical history, despite resolution of pain and leukocytosis at time of sonography and surgery. A, Longitudinal sonogram shows enlarged uncompressible appendix (arrows). w = abdominal wall. B, Photograph of magnified transverse histologic section of appendix shows atrophied mucosa (m). Chronic inflammation is shown by replacement of fat in submucosa (am) by extensive fibrosis, which extends also into muscularis propria (mp). Arrows identify borders between mucosa and submucosa and between submucosa and
muscularis
propria.
AND
ABNORMAL
APPENDIX
775
landmark for identifying the wall on sonography. Clear distinction ofthe layers of the wall allowed an accurate measurement in 21 cases. The wall thickness on sonography varied between 3.3 and 7.5 mm (mean, 4.55 mm). Corresponding values by histopathology varied between 3.5 and 7.7 mm (mean, 4.58). Thirteen cases of appendicitis had advanced wall inflammation in the distal half, which was indistinguishable on sonography from hypoechoic intraluminal pus. Similarly, the appendiceal wall was not clearly visualized in four other cases, and noncompressibility as well as findings of periappendicitis were criteria used to diagnose appendicitis. Three studies were incorrectly interpreted as normal. One false-negative examination occurred with nonvisualization of a retrocecal appendix in an obese patient, although pain occurred with transducer compression in the right lower quadrant. Another case involved an initial interpretive error; retrospectively, the sonogram showed classic signs of appendicitis with a wall thickness of 4.5 mm and hypoechoic surrounding fat with a small amount of ascites (Fig. 4). In the third case, only the proximal half of a normal appendix was
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echoic mass was seen at sonography and confused with appendicitis; this error in diagnosis has been previously described [3] (Fig. 6). Finally, one patient had a small pericecal abscess due to cecal perforation by a foreign body. The hypoechoic mass contained increased central echoes that were falsely interpreted as a ruptured appendix (Fig. 7). This pitfall also has been described before [4]. In addition to this last case, perforation of the appendix was suggested by sonography in 1 1 cases and confirmed surgically in all cases.
seen on sonography. Because of persistent symptoms, the patient underwent surgery and was found to have inflammatory changes in the distal appendix. Of the 60 patients who had surgery, 1 5 were found to have a normal appendix at the time of the operation. Twelve cases were correctly diagnosed by sonography. Of these, a normal appendix was identified in nine cases showing identical correlation between the histopathologic specimen and such sonographic findings as clear wall distinction (nine cases), wall thickness (varying in both techniques between 0.5 and 3 mm; mean, 1 .8 mm), the presence of enlarged lymphoid hyperplasia in the wall (two cases), a complete luminal collapse (three cases), or a lumen fully distended by feces (six cases); this correlation suggested that the structure visualized at sonography was indeed the appendix. In the other three cases, the appendix was not clearly identified, but was considered to be normal by sonography for statistical purposes. Three patients with normal appendixes at surgery had abnormal sonographic findings. Of note, a pericecal inflammatory process was found during surgery in all three. One patient had Meckel peridiverticulitis with a fecalith (Fig. 5), a condition easily confused with necrotized appendicitis containing a fecalith. Another patient had chronic inflammation of the right salpinx and ovary adjacent to a normal appendix. A tubular, poorly defined, hypo-
Patients
Who Did Not Have Surgery
All 1 10 patients who did not have surgery had clinical followup over a period varying between 1 and 1 4 months (mean, 8.6 months). Of these, 89 normal appendixes were clearly seen at sonography and another 1 7 cases were considered normal on sonography although the appendix was not visualized. At follow-up, none of these 1 06 patients had recurrent pain in the right lower quadrant. Diagnoses in four patients who did not have surgery but had abnormal sonographic findings were considered false positive for appendicitis by sonography. Sonography in all four showed the typical threering appearance of the appendix in transverse views, a wall thickness greater than 3 mm, and absence of compressibility.
Fig. 4.-Appendicitis
penap-
with
pendicitis. A, Axial sonogram
ring appearance (solid
arrows).
shows multipleof enlarged appendix
Although
hyperechoic
ring of submucosa (open arrow) is proserved, asymmetric hypoechoic region (arrowheads) represents muscular layerwith periappendicitls. w = abdomlnal wall, p = psoas. B, Longitudinal
sonogram
of same
enlarged appendix (solid arrows). Thick hypoechoic layer represents muscularls propria and periappendiitie (open arrows). w = abdominal wall.
,
-
‘
__:_. #{163}
Ac;.
a.. F .
-sm
..‘
k
4
ii,
_____
Fig. 5.-Meckel peridiverticulitis caused by fecalith misdiagnosed as appendicitis with fecalith in 39-year-old woman. A, Axial sonogram of right abdominal
fossa, inferior to cecum, shows hypeechoic, poorly defined mass (arrowheads) containing a fecalfth (arrow). B, Photograph of histologic section of corresponding specimen shows antimesenteric wall of ileum (I = lumen, m = mucosa sm = submucosa, mp =
muscularis
propna).
diverticulum
(arrow).
Inflamed F
=
fecalith.
Meckel
AJR:158,
Fig. 6.-Pseudoappendicitis.
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SONOGRAPHY
April 1992
OF
NORMAL
AND
ABNORMAL
I
Longi-
777
APPENDIX -:-:
‘
I
tudinal sonogram shows hypoechoic, poorly defined sausagelike mass (solid arrows) without distinct walls adjacent to gas-filled (open arrows) cecum (C) mimicking appendicitis. A chronic in-
1’
.i..,.
.
V.
-&-
---
_
flammatory process of right salplnx and ovary unexpectedly located inferior to cecum was noted at surgery.
Fig. 7.-Pseudoappendicltis with rupture. Under collapsed cecum (c) (arrowheads) sonogram shows oval, hypoechoic, poorly defined mass (arrows) containing hyperechoic material and suggesting ruptured appendix. At surgery, a cecal perforation from foreign body with small infracecal abscess was found.
However, because the symptoms resolved almost completely within a few hours after sonography, the patients were released without surgery. Three of them had a chronic history of recurrent pain in the right iliac fossa. All three patients still reported recurrent episodes of abdominal pain lasting from 4 to 1 0 hr at the time of follow-up. The last patient with an enlarged appendix at sonography who did not have surgery had no recurrence of symptoms. Of 125 patients without appendicitis, a normal appendix was clearly visualized in 1 02 cases (82%). On the other hand, our entire study group included 21 cases (1 2%) in which the appendix was not seen on sonography. Sonography in 170 patients enabled the diagnosis of acute appendicitis with a sensitivity of 93%, a specificity of 94%, a positive predictive value of 86%, a negative predictive value of 98%, and an accuracy of 94%.
Discussion Preoperative diagnosis of acute appendicitis remains a difficult clinical problem. Barium enema examination is considered to be an unreliable test for acute appendicitis because of its large percentage of false-positive and false-negative results [1 3]. Laparoscopy is invasive and has limited use in patients who have had surgery or patients with retrocecal appendixes. Recently, CT has been used as a diagnostic tool to identify patients with appendicitis, but it is not always readily available and requires ionizing radiation and the use of IV contrast material [1 4]. Sonography is a readily available, inexpensive, noninvasive test, with a reported sensitivity of 80-94% in the detection of acute appendicitis [1 2, 5, 6, 8, 1 0, 12]. Significant obesity and overlying loops of gas-filled bowel may give sonography a lower sensitivity in some cases. The most frequent sonographic findings in acute appendicitis are noncompressibility of the appendix with a wall diameter greater than 6 mm [5]. However, as visualization of a normal appendix was unusual in many reported series, a nonvisualized appendix was considered normal. Recently, Vigneault et al. [1 2] reported the sonographic visualization of ,
a normal appendix (diameter, 6 mm) in 1 0 oftheir 35 patients without appendicitis. In our study, we identified the normal appendix by sonography in 1 02 (82%) of 1 25 patients without surgically proved appendicitis. Complete sonographic and histologic correlation in nine resected normal appendixes suggested that the structure identified at sonography was indeed the appendix. Our success in visualizing the normal appendix by sonography may be related to added effort and time spent in searching for the cecum and the appendix. Examination of patients with a full bladder and then after micturition was helpful in localizing the normal appendix in many cases, but was not useful in any case of acute appendicitis. The point of maximal tenderness was not always related to the position of the appendix in normal cases, but was useful in locating all cases of appendicitis. Finally, our early experience with sonographic inspection of surgical (colectomy and right hemicolectomy) specimens by submersion in a water bath was helpful in recognizing the sonographic appearances of the colon, the ileocecal valve, and the normal appendix. In our series, sonography had a sensitivity of 93% and specificity of 94% in detecting acute appendicitis, comparable to those in previous studies [1 -8, 12]. Identification of a normal appendix in 82% of patients and a negative predictive value of 98% had a major impact on our surgeons in increasing test credibility. We had only two false-negative cases (1 .9%) out of 104 normal sonographic diagnosis with clear sonographic visualization of the appendix. On the other hand, of 21 normal sonographic diagnoses without sonographic visualization of the appendix, we had one false-negative finding (4.8%). Comparing the number of false-negative cases in our group of normal sonographic diagnoses with good visualization of the appendix (two of 104), and the number of false-negative cases coming from the whole group with normal sonographic diagnosis without visualization of the appendix (30 of 345) found in previous studies [1 2, 5, 6, 8, 12], we found a significant difference between the two groups (chi-square value 5.538, df 1 p .01 9). On the other hand, when we compared the number of false-negative cases in our group of normal sonographic diagnoses without visual,
=
=
,
=
778
RIOUX
ization of the appendix (one of 21 ), and the corresponding value from the latter group (30 of 345), we found no difference between groups (chi-square value 0.31 5, df 1, p .53). Therefore, visualization of the normal appendix on sonography appears advantageous in reducing the percentage of false-negative cases; it allowed a negative predictive value of 98% in our study. Our sonographic criteria for a normal appendix were reliable because the appendix was compressible, surrounded by normal-appearing fat, and had a distinct wall less than 3 mm thick. It is also noteworthy that six normal appendixes had a full transverse diameter of more than 6 mm because of luminal dilatation by feces, although they had a very thin wall and were compressible. Had other established criteria been used, these appendixes might have been considered abnormal because of their overall diameter. In 35 of 42 cases of appendicitis diagnosed by sonography, the wall was clearly visualized in at least one area and was more than 3 mm thick. In the seven other cases, wall detection was difficult because the advanced mural inflammation led to a similar appearance with hypoechoic luminal contents. For that reason, the presence of a hypoechoic oval, round, or tubular noncompressible structure with indistinct borders with modified surrounding fat located in the vicinity of the cecum was used for the sonographic diagnosis of appendicitis (Fig. 2B). Detailed analysis of our three false-negative cases of appendicitis by sonography demonstrated the importance of complete visualization of the entire appendix, because only part of it might be involved by the inflammatory process. It also indicated that in such studies, echogenicity in some patients may be inadequate, usually owing to obesity or ileus, to allow 1 00% safety in ruling out disease in the abdomen with sonography. The positive predictive value of sonography for appendicitis (86%) is slightly lower than that found in other studies (between 89% and 93%) [1 , 2, 5, 6, 8, 10, 1 2]. Of the seven patients with false-positive results, three underwent laparotomy and had inflammatory processes requiring surgery. Appendicitis was incorrectly diagnosed by sonography because of the findings of an uncompressible, hypoechoic, round or tubular structure surrounded by abnormal fat near the cecum. In none was the appendiceal wall clearly visualized. These observations raise the possibility that the diagnosis in these three cases would not have been made if the sonographer had restricted the diagnosis of appendicitis to only those cases showing a classical appearance of an enlarged appendix (i.e., three well-visualized distinct wall rings on transverse views). Our additional abdominal sonographic criteria for appendicitis (excluding the wall thickness) may have slightly decreased our specificity for appendicitis, but they seem quite accurate in detecting other abnormalities mimicking appendicitis and also requiring treatment by surgery. Four other cases were false positive on sonography, each having a noncompressible appendix clearly visualized by sonography with a wall thickness greater than 3 mm. These patients did not have surgery because of their rapidly resolving symptoms and also because three of them had previous episodes of abdominal pain with rapid resolution. The three
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=
=
AJR:158,
April 1992
patients still reported recurrent episodes of pain in the same location when they were contacted at the end of the study. None has been operated on so far, and none has undergone subsequent sonographic evaluation. In retrospect, we suggest that they might represent cases of subacute or chronic appendicitis [1 5]. To further support that hypothesis, this study reports five other similar patients who underwent surgery. Four of them were asymptomatic with a normal WBC count shortly before surgery. All patients had histologic evidence of chronic inflammation with superimposed acute signs of inflammation with various degrees of severity. We suggest that the decision for surgery in such cases was in large part conditioned by the fact that the patients were examined in the last 6 months of the study, a period correlating with the surgeon’s increased confidence in our sonographic criteria for appendicitis. In conclusion, our results suggest that a normal appendix can be visualized sonographically far more frequently than previously suspected. The wall thickness of the appendix appeared to be a useful index of the status of the appendix. The 98% negative predictive value of sonography for appendicitis in conjunction with actual visualization of the normal appendix in most cases may increase the confidence of surgeons in the use of sonography for their occasionally difficult clinical situations. In our study, a search for sonographic visualization of the normal as well as the abnormal appendix seems to significantly reduce our percentage of false-negative cases, this being one of our major goals. REFERENCES 1
.
Puylaert JBCM. sion. Radiology
2. Abu-Yousef Metcalf
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appendicitis:
US evaluation
using graded
compres-
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AM.
High
resolution
sonography
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AJR
1987;149:53-58 3. Terry J, Forest T. Sonographic demonstration of salpingitis: potential confusion with appendicitis. J Ultrasound Med 1989;8:39-41 4. Machan L, Pons MS, Wood BJ, Wong AD. The “coffee bean” sign in periappendiceal and pendiverticular abscess. J Ultrasound Med
1987;6:373-375 5. Jeffrey
RB Jr, Laing
FC, Townsend
RR. Acute
appendicitis:
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criteria based on 250 cases. Radiology 1988;167:327-329 6. Jeffrey RB Jr, Laing FC, Lewis FR. Acute appendicitis: high resolution realtime USfindings. Radiology 1987;163:11-14 7. Gaensler EHL, Jeffrey RB Jr, Laing FC, Townsend RR. Sonography in patients with suspected acute appendicitis: value in establishing alternative diagnosis. AiR 1989;1 52:49-51 8. Kang WM, Lee CH, Chou YH, et al. A clinical evaluation of ultrasonography in the diagnosis of acute appendicitis. Surgery 1989;1 05:154-159 9. Fa EM, Cronan JJ. Compression as an aid in the differential diagnosis of appendicitis. Surg Gynecol Obstet 1989;169:290-298 10. Bilbey JH, Gibney RG, Cooperberg PL. tJtrasonography in acute appendicitis. J Can Assoc Radiol 1989;40:22-24 1 1 . Poole GV. Appendicitis: the diagnostic challenge continues. Am Surg
1988;54:609-612 1 2.
Vigneault F, Filiatrault 0, Brandt ML, et al. Acute appendicitis in children: evaluation with US. Radiology 1990;176:501-504 13. Rajagopalan AE, Manson JH, Kennedy M, Pawlikowski J. The value of the baryum enema in the diagnosis of acute appendicitis. Arch Surg 1977;1 12:531 -533 14. Balthazar EJ, Megibow AJ, Siegel SE, et al. Appendicitis: prospective evaluation with high-resolution CT. Radiology 1991;180:21-24 1 5. Oachman AH, Nichols JB, Patrick PH, et al. Natural history of the obstructed rabbit appendix: observation with radiography, sonography, and CT. AJR 1987;148:281-284
