Pediatric Francois Vignault, Andr#{233}eGrignon,
MD MD
#{149} Denis
Filiatrault, Ouimet, MD
#{149} Alain
Acute Appendicitis Evaluation with During a 4-month period, high-resolution ultrasonography (US) was used to prospectively evaluate 70 children with clinically suspected acute appendicitis. Thirty-five US scans showed a noncompressible appendix with maximal outer diametens greater than 6 mm. This finding was considered positive for the diagnosis of acute appendicitis. Thirty-one of these 35 patients had acute appendicitis documented by surgical and pathologic findings. The remaining four patients were observed, and their symptoms resolved. Thirty-five patients had US scans considered negative for appendicitis. Seventeen of these patients had US findings positive for other conditions including mesentenic adenitis, ileitis, intussusception, Crohn disease, and Burkitt lymphoma. In this series US enabled diagnosis of acute appendicitis with a sensitivity of 94%, a specificity of 89%, and a predictive accuracy of 91%. Diagnosis of acute appendicitis can be made with US with the same accuracy in children as has been previously reported in series of adult patients. The use of US in clinically ambiguous cases may allow earlier diagnosis, prevention of perforation, and decreased complications in the pediatric patient with acute appendicitis. Index dix,
terms: US
testinal
the
L.G.,
1990; April
176:501-504
Departments
AG.)
H#{244}pital Ste-Justine,
Montreal, cemben
Que, 8, 1989;
and
of Radiology
Surgery 3175
Canada revision
revision received 12. Address reprint
( RSNA,
gastroin-
751.291
1990;
From
#{149} Children,
1990
(M.L.B.,
C#{244}teSte
H3T 1C5. requested
(F.V.,
A.O.),
Catherine,
Received January
March 29; accepted requests to D.F.
#{149} Mary
L. Brandt,
MD
De10,
#{149} Laurent
Garel,
MD
In Children: US’ PPENDICITIS indication dominal surgery morbidity and
is the most common for emergency abin children. Both mortality are in-
creased if the appendix perforates. Therefore, the goal of the surgeon is to make an accurate diagnosis as earby as possible. In children this is not always possible. In young children, the history may be confused or unobtamable, and the clinical presentation may be confusing as well. Kottmeier reports that 1 1%-32% of patients undergoing appendectomy do not have appendicitis at surgery (1). In general, the younger the child, the more difficult it will be to make an accurate diagnosis. Perforations of the appendix tend to occur earlier in this younger age group. An accurate and reproducible method of diagnosing appendicitis with ultrasound (US) would thus be most advantageous in the younger child. Acute appendicitis is usually diagnosed on the basis of history and physical examination, with laboratory and madiobogic studies providing corroborating evidence. The first amtide describing the use of US in the diagnosis of appendicitis was pubbished by Puybaent in 1986 (2). Several other series have since been published describing the indications for and results of US studies in the diagnosis of acute appendicitis (3-9). With the exception of 21 pediatric cases reported by Kao et al (10), all of these series evaluated mainly adult patients. The sensitivity, specificity, and predictive accuracy of US in the diagnosis of acute appendicitis in children have not been evaluated previously. We present the results of a pro-
#{149} Appen-
751.291
751.1298
tract,
Radiology
D.F.,
Appendicitis,
studies,
MD
Radiology
spective study of abdominal US performed in children presenting with abdominal pain in whom the diagnosis of appendicitis was considered. We evaluated these studies to determine the sensitivity and specificity of this examination and to determine if
previously pendicitis pbicabbe
established criteria of apin adult patients were apto the pediatric population.
PATIENTS
AND
METHODS
Seventy patients during the period between May and August 1989 who presented with abdominal pain were evaluated with real-time high-resolution US. US examinations were performed by eithem one of the radiology residents or the attending staff. All patients had abdominab pain, which the surgeons believed could be secondary to appendicitis. The patient selection depended on the personal preference of the referring surgeon. We did not know prior to the US examination whether or not the patient was to undergo surgery. Ninety percent of the patients with suspected appendicitis were studied with US during this period. There were 38 boys and 32 girls, with ages ranging from 4 to 18 years (mean, 10 years). The surgeons were not blinded to the results; as a prospective study, US findings were excluded from patient management decisions. In previously published studies in adult patients, most evaluations were performed with a 5- or 7.5-MHz linear-array transducer (2-7,9,11). A linear high-resolution probe was not available, and, as the appendix is often superficial in children, we decided to image it with a high-resolution sector probe. A complete examination of the abdomen and pelvis was penformed with a 3.5- or 5-MHz annular-array
transducer
(ATL
Mark
Technology Laboratory, After this examination, for the appendix was MHz sector transducer chine
with
graded by
a i.i-cm
focus
compression
Puylaert
(2).
8; Advanced
Bothell, Wash). a careful search made with a 10on the same maarea,
technique When
the
using
the
described
appendix
was
too far to be well visualized with the 10MHz transducer, a 7.5-MHz sector transducer with a 2.1-cm focus area was used on the same machine. The right side of the abdomen was examined first in the transverse plane, then in the sagittal plane, most carefully examining the area of maximal tenderness. After locating the appendix, it was evaluated for maximal cross-sectional
distance
diameter
between
the
by
outer
measuring
walls
the
with
501
b.
a.
C.
Figure 1. US scans from a patient with surgically proved acute appendicitis. (a) Axial section through the appendix (between calipers). Note the free fluid (arrows). No free fluid was noted elsewhere. a = iliac artery. (b) Longitudinal preoperative scan of the appendix (arrows). Diameter, 12.6 mm. a iliac artery. (c) In vitro US scan of resected appendix (longitudinal section) showing correlation of size and shape.
Table 1 Comparison Outcome
of US Findings
Table 2 Correlation
and
of Pathologic
Findings
and US Patterns Diffuse
Findings at US Study Positive (n 35)
Outcome
Hypoechogenicity Diffuse
Pathologic Finding
Negative (n 35) Mean
Proved
(n33) No appendicitis follow-up (n
diameter
(mm)
Predominant
appendicitis
-
at 37)
31
2
4
33
Target
Inflammation
502
#{149} Radiology
Numbers
t Numbers
I
are
most
Pus
13.5, 18 under pressure within the appendix 0
appendix
was
involved
Appendicitis
(ii
only
intraluminally.
One
patient
underwent
later.
3
US Findings
Without (n
Perforation 22)
33) With
Perforation (n = 11)
Freefluid
9(41)
5(45)
Fecalith
1 (4)
4 (36)
Adenopathy
3(14)
2(18)
Note-Numbers
in parentheses
viewed all the pathologic reports correlations with the US patterns.
are
Normal
Appendix 37)
(n
4(11)
0 15(41)
percentages.
to make
RESULTS The
sub-
percentages.
of the
US Finding
results are summarized in Ta1-4. Thirty-five patients (50%) had US scans considered positive for appendicitis with an appendiceab diameter greater than 6 mm. The diameter of the appendix in these cases varied from 6.7 to 23 mm with an average of 10.5 mm. In all cases the diameter memained unchanged with compression (Table 1). We identified three bles
of the
mucosa, diffusion of the inflamma. tion through the wall 9(75)
are ranges.
in parentheses
14 hours
Table Other
Necrosis
Posterior
Enhancement (n 2)
13.6 (9.1-23)
within
21(11.7) in parentheses
perforation,
Focal
surgery
17)
the lumen
Perforationt electronic calipers. Other variables evaluated included the echogenicity and compnessibibity of the appendix. The presence on absence of the following were noted as well: free fluid in the abdomen, pain with compression (McBumney sign), fecalith, and adenopathy in the might lower quadrant and peniumbilical region. A lymph node was considered abnormal if it measuned more than 4 mm in its anteroposteriom diameter (12). In 12 cases, the resected appendix was placed in a plastic bag filled with saline and examined with the same US equipment to correlate the preoperative image with the image of the surgical specimen (Fig 1). It would seem logical to assume that the appendix and its diameter would be proportionally smaller in children, but this does not seem to be the case. We analyzed five appendices removed at autopsy after death from other causes in children from 4 months to 5 years of age. The appendiceal diameter was 4.5 mm in a 4month-old child and between 3.5 and 4.5 mm in the others. Therefore, we used the same criteria applied to the adult population for a positive examination, namely, a noncompressible appendix with maximal outer appendiceal diameter greater than 6 mm (7). Patients underwent surgery within 24 hours of the US examination on were observed according to the clinical judgment of the responsible surgeon and not according to US results, although the results were known to the surgeon. Patients who were observed were followed up for a minimum of 1 month. We have me-
=
8.6 (6.7-12.6)
condi-
lion
a
(n
with
Hypoechogenicity (n 12)
typical patterns of in the axial plane 2c). US scans of 21 “target” appearance, center surrounded genic line and an rim (Fig 2a). Four
echogenicity seen (Table 2) (Fig 2apatients had a or an echo-poor by an inner echoouter echo-poor of these patients
did not undergo surgery. US scans of i2 patients had a uniformly hypoechoic appearance of the appendix (Fig 2b). In two cases the appendices were uniformly hypoechoic with posterior enhancement (Fig 2c). One of these patients had a target appearance proximally with a hypoechoic pattern distally (Fig 3). In seven pa-
August
1990
b.
a.
C.
Figure 2. (a) Axial section through an inflamed appendix (between calipers) showing target appearance. Diameter, 1 1 mm. (b) Axial section (arrows) with diffuse hypoechoic appearance. Diameter, 9 mm. (c) Axial section showing hypoechoic appearance with posterior enhancement (arrows). Diameter, 18 mm between calipers.
lymph
Figure 3. Longitudinal US scan of appendix showing transition between target appeamance (diameter, 7 mm between arrows) and
diffuse
hypoechogenicity
the appendix ipers).
(diameter,
of the
14 mm
tip
of
between
lower abdomen showing the ascending coIon (arrows) and an axial section of the inflamed appendix in a retrocecal position (between calipers). Diameter, 6.7 mm.
cal-
Figure tis with
5.
US scan
fecalith
not
of perforated seen
on
plain
appendiciabdomi-
nal radiographs. Longitudinal scan of the appendix (large arrows) showing fecalith at the proximal end (between calipers) with rupture of the submucosal lining (small anrows) and localized abscess (a).
tients the appendices were seen in a netnocecal position at US, which was confirmed at surgery (Fig 4). A positive McBumney sign was elicited to some degree in all patients with a positive US scan. Free intraabdominal fluid was present on 14 of 35 (40%) of the positive US scans. The quantity amount
of fluid varied of peniappendiceal (Fig la) to a moderate or amount of fluid, usually pouch of Douglas or the
Volume
176
#{149} Number
2
from
a small liquid barge seen in the Monison
pouch. The fluid was present in nine of 22 cases (41%) of appendicitis without perforation and five of 11 cases (45%) of appendicitis with perforation (Table 3) and was, therefore, not predictive of perforation in our series. On five of 35 positive US scans (14%), a fecalith was identified (Fig 5). Three of these five fecaliths were not visible on plain abdominal radiographs. Adenopathy (lymph nodes larger than 4 mm) was found on five of 35 positive
US
scans
(14%),
with
nodes
measuring
from
4.5
to 8
mm. Thirty-one of the 35 patients with positive US scans underwent expboration and appendectomy. All patients who underwent appendectomy had surgically and pathologically proved appendicitis. The four patients who were observed had resolution of their symptoms with no mecumrence for at least i month after discharge. Repeat US examinations in these four patients showed a decrease in the appendiceal diameter to less than 6 mm at 1 month after discharge. Thirty-five patients (50%) were considered to have US findings that were negative for the diagnosis of appendicitis (Table 4). A normal appendix (diameter of 6 mm or less) was seen in 10 of these patients (29%). Thirty-three patients (94%) were observed with resolution of their symptoms, and their studies constitute the true-negative exarninations in our series. Two patients (6%) underwent appendectomy with sumgicalby and pathologically proved appendicitis, and their results represent false-negative examinations. The appendices of these two patients measuned 7 and 8 mm in diameter at sungery. Free fluid was noted in four of 33 (12%) of the true-negative exarninations. Fifteen patients with a truenegative examination had adenopathy varying from 5 to 22 mm in anteropostemior diameter. During the study period no patient with a nonmab appendix underwent exploration and appendectomy. In the 70 children examined, the diagnosis of appendicitis with use of US was made with a specificity of 89% and sensitivity of 94%. The overall accuracy was 91% with a predictive value for a positive test of 89% and a predictive value for a negative test of 94%.
Radiology
#{149} 503
DISCUSSION Appendicitis can be difficult to diagnose in some children. These patients would benefit from an early diagnosis, which could decrease their risk of appendix perforation. Three patterns of echogenicity in cases of proved appendicitis were found. The first is the target pattern previously described in the literature (2). The hypoechoic center correlated with a small amount of fluid or pus. The echogenic line represented the submucosa, and the hypoechogenic rim surrounding it was the muscular layer (13). The target sign was associated with smaller diameters of inflamed appendix and sparing of the submucosal layer. There were only two perforations in this group (11%). Accordingly, the positive examinations in patients who did not under-
go surgery
were
of the
target
pattern.
The
second pattern was one of diffuse hypoechogenicity, which seems to correlate with a more advanced stage of inflammation. On gross pathologic and histologic exarnination, the mucosa and submucosa
were
ulcerated;
city represented inflammation
wall.
The
the the process
mean
hypoechogenidiffusion through
diameter
was
of the the
banger
in this pattern, with a higher frequency of perforation (75%). In one patient (Fig 3), we could see easily the transition between the spared submucosal layer proximally and the transmural inflammation distally. There was a phlegmon of the distal tip of the appendix at pathologic examination. The third pattern, diffuse hypoechogenicity with posterior enhancement, was seen in two patients
whose pus
gery.
appendices under
The
were
pressure
wall
was
at the
very
filled time
thin,
with of sum-
and
in
one case the appendix ruptured during the operation but was outside of the patient. Therefore, theme were definite correlations between US pattenns and pathologic severity of the disease (Table 2). Two patients had false-negative findings. The first patient had an ap-
pendiceal
diameter
of 5 mm
amination at surgery
and a diameter several hours
at US ex-
of 6-7 mm later. The
second patient had air in the right lower quadrant, which was believed to represent either bowel loops or an abscess. The appendix was not seen. At surgery the patient have an appendiceal
was
placed,
#{149} Radiology
were
accurate
had
US signs
indic-
enough
that
The
Richard
authors
thank
Veilleux
photographs
and
High
Sylvie
compres-
i58:355-360.
JJ, Maher
Bleicher
JW,
EA Jr. Metcalf
sonography
AM.
of acute
ap-
pendicitis. AJR 1987; 149:53-58. Puylaert JBCM, Rutgers PH, Lalisang RI, et al. A prospective study of ultrasonogin
the
diagnosis
of appendicitis.
N
J Med 1987; 317:666-669.
Adams
DH,
Fine
C, Brooks
DC.
High-res-
olution real-time ultrasonography: a new tool in the diagnosis of acute appendicitis. Am J Sung 1988; 155:93-97. Jeffrey RB Jr. Laing FC, Lewis FR. Acute appendicitis: high-resolution real-time ultrasound
7.
1986; MM,
resolution
EngI
6.
et
ultra-
graded
LF, Franken
naphy 5.
appendicitis:
using
Radiology
Urdaneta
4.
Acute
evaluation
Abu-Yousef
In: Welch Chicago: Year
1986; 989-995.
JBCM.
findings.
11-14. Jeffrey
Radiology
RB Jn, Laing appendicitis: on 250 cases.
Acute based
1987;
163:
FC, Townsend RR. sonognaphic criteria Radiology 1988; 167:
327-329. 8.
Kang
WM,
clinical
the
10.
11.
CH,
diagnosis
Bilbey
A in
appendicitis.
Sun-
RC, Cooperberg
PL.
graphic findings. AJR 1989; 153:375-379. Caensler EH, Jeffrey RB Jr. Laing TC, Townsend RR. Sonography in patients suspected
acute
appendicitis:
alternative
value
diagnoses.
AJR
1989; 152:49-51. Puylaert JBCM. Mesentenic adenitis and acute terminal ileitis: ultrasound evaluation using graded compression. Radiology 1986;
161:691-695.
Borushok
FK, Jeffrey
Townsend
RR.
perforation dicitis.
14.
et al.
Ultnasonognaphy in acute appendicitis. Can Assoc Radiol 1989; 40:22-24. Kao SCS, Smith WL, Abu-Yousef MM, et al. Acute appendicitis in children: sono-
in establishing
13.
YH,
105:154-159.
JH. Cibney
with
12.
Chou
of ultrasonography
of acute
1989;
geny
9.
Lee
evaluation
RB Jr. Laing
Sonographic
in patients AIR
1990;
FC,
diagnosis
with
acute
of
appen-
154:275-278.
Puylaent JBCM, Van den Werf SDJ, Ulnich C, Veldhuizen RW. Crohn’s disease of the the
ileocecal appendix.
region: US visualization of Radiology 1988; 166:741-
743.
15.
Puylaert
JBCM,
Werf
litis
acute
differ-
mimicking
Pracros
appendicitis:
with graded-compression 1988; 166:737-740. JP,
Acute
Tran-Minh
VA,
US. Monin
DC,
et
intestinal
intussusception in children: contribution of ultrasonography (145 cases). Ann Radiol 1987; 30:525-530. Senen RN, Alper H, Deminci A, Dinen HB. A different sonographic “pseudokidney”
appearance phoma:
detected
with
intestinal
lym-
“hydronephrotic-pseudokidney.”
J Clin Ultrasound i8.
den
ileoco-
al.
17.
RI, van
L. Campylobacten
entiation Radiology 16.
Lalisang
SDJ, Doomnbos
Savenin
RA, Clausen
penman
M.
pendicitis.
De-
for their
Appendicitis. surgery.
Book Medical,
the surgi-
cab service is now considering the US findings, in addition to the clinical findings, in children with abdominal pain when making the diagnosis of acute appendicitis. U Acknowledgments: nyse Collins and sistance with the
Puylaent sion.
ative of Bumkitt lymphoma, that is, a strong echogenic center surrounded by a sonolucent rim corresponding to the thickened wall of the small bowel in the right iliac fossa and many adenopathies in the midline (17). All patients with a positive US scan who underwent surgery had appendicitis with an exact correlation between appendiceab diameter determined at US and measurement after resection. The four patients whose examinations were considered false positive were observed with nesolution of their symptoms. These cases may represent resolution of a true appendicitis rather than a false-positive US examination as suggested by othem authors (5,6,8,18). Therefore, the predictive value for a positive test in our patients may be higher than the calculated 89%. Our specificity and sensitivity
were
2.
3.
adminis-
encountered, for example, typical US patterns in one case of intussusception, namely, target sign in transverse section, sandwich sign in sagittab section, and continuity of the intussusception with intestinal lumen
for preparing
504
antibiotics
patient
Kottmeier PK. al, eds. Pediatric
sound
tients (28.6%). Therefore, we need to remain careful when diagnosing mesenteric adenitis. US can aid in both diagnosing appendicitis and excluding other conditions known to mimic appendicitis (14,15). We have
One
1.
was found to abscess. A drain
temed, and the patient underwent appendectomy 6 weeks later. The presence of numerous, large lymph nodes without an enlarged appendiceal lumen may support the diagnosis of mesenteric adenitis; but it is difficult to see the normal appendix, as we did in only 10 of 35 pa-
(16).
References
1989; 17:209-212. K, Martin
EW, Coo-
Chronic and recurrent apAm J Sung 1979; 137:355-357.
asTass#{233}
the manuscript.
August
1990