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Blumfield et al.
Ultrasound of Pediatric Appendicitis
Pediatric Imaging
Original Research

FOCUS ON:

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JOURNAL CLUB:

JOURNA L

CLUB

Einat Blumfield1
Gopi Nayak 2
Ramya Srinivasan1
Matthew Tadashi Muranaka3
Netta M. Blitman 4
Anthony Blumfield5
Terry L. Levin 6
Blumfield E, Nayak G, Srinivasan R, et al.

Keywords: pediatric, perforated appendicitis, ultrasound


DOI:10.2214/AJR.12.9801
Received August 17, 2012; accepted after revision
October 24, 2012.
1
Department of Radiology, Jacobi Medical Center, Albert
Einstein College of Medicine, 1400 Pelham Pkwy S, Bronx,
NY 10461. Address correspondence to E. Blumfield
(Einat.blumfield@nbhn.net; Einat_blumfield@hotmail.com).
2

Department of Radiology, Montefiore Medical Center,


Albert Einstein College of Medicine, Bronx, NY.
3
Department of Radiology, University of Hawaii,
Honolulu, HI.
4
Department of Radiology, Albany Medical Center,
Albany Medical College, Scarsdale, NY.
5

Radnostics, Scarsdale, NY.

6
Department of Radiology, Childrens Hospital at
Montefiore Medical Center, Albert Einstein College of
Medicine, Bronx, NY.

AJR 2013; 200:957962


0361803X/13/2005957
American Roentgen Ray Society

Ultrasound for Differentiation


Between Perforated and
Nonperforated Appendicitis
in Pediatric Patients
OBJECTIVE. Acute appendicitis is the most common condition requiring emergency
surgery in children. Differentiation of perforated from nonperforated appendicitis is important because perforated appendicitis may initially be managed conservatively whereas nonperforated appendicitis requires immediate surgical intervention. CT has been proved effective in identifying appendiceal perforation. The purpose of this study was to determine
whether perforated and nonperforated appendicitis in children can be similarly differentiated
with ultrasound.
MATERIALS AND METHODS. This retrospective study included 161 consecutively
registered children from two centers who had acute appendicitis and had undergone ultrasound and appendectomy. Ultrasound images were reviewed for appendiceal size, appearance
of the appendiceal wall, changes in periappendiceal fat, and presence of free fluid, abscess, or
appendicolith. The surgical report served as the reference standard for determining whether
perforation was present. The specificity and sensitivity of each ultrasound finding were determined, and binary models were generated.
RESULTS. The patients included were 94 boys and 67 girls (age range, 120 years; mean,
11 4.4 [SD] years) The appendiceal perforation rate was significantly higher in children
younger than 8 years (62.5%) compared with older children (29.5%). Sonographic findings
associated with perforation included abscess (sensitivity, 36.2%; specificity, 99%), loss of
the echogenic submucosal layer of the appendix in a child younger than 8 years (sensitivity,
100%; specificity, 72.7%), and presence of an appendicolith in a child younger than 8 years
(sensitivity, 68.4%; specificity, 91.7%).
CONCLUSION. Ultrasound is effective for differentiation of perforated from nonperforated appendicitis in children.

cute appendicitis is the most common condition in children that requires emergency surgery and is
one of the most common causes of
hospitalization. Perforation occurs with rates
ranging between 23% and 73% [1]. With the
trend toward conservative management of perforated appendicitis [24] as opposed to immediate appendectomy for nonperforated appendicitis, differentiation between the two conditions
has become increasingly important. Because
clinical differentiation is not always possible,
clinicians often rely on imaging findings [58].
CT, although effective in the diagnosis of
acute appendicitis, exposes patients to ionizing radiation [9, 10]. CT signs suggesting
perforation include defects within the appendiceal wall, abscess, extraluminal air, ileus,
and the presence of an extraluminal appendicolith [68]. Ultrasound is also effective in

diagnosing acute appendicitis [11], but there


have been few published reports of the reliability of ultrasound in the diagnosis on appendiceal perforation [12, 13], and no results, to our knowledge, are current.
The imaging capabilities of ultrasound
have improved substantially. Although the
site of perforation is typically, over the last
two decades, not identified with ultrasound,
we hypothesized that the size of the appendix,
changes in the appendiceal wall, and findings
of a large amount of inflamed fat around the
appendix are associated with perforation. We
therefore undertook a retrospective study to
assess the effectiveness of ultrasound in diagnosing appendiceal perforation in children
and to determine which sonographic findings
or combination of findings would be most
useful in differentiating perforated from nonperforated appendicitis. We compared the re-

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Blumfield et al.
TABLE 1: Sonographic Findings

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Finding

Description

Transverse diameter of appendix

Largest diameter, based on longitudinal image of the appendix (Fig. 1)

Appendicolith

Present or absent (Fig. 2)

Loss of the echogenic submucosal layer

Present or absent (Fig. 3)

Presence and amount of periappendiceal echogenic fat

No echogenic fat, small amount, moderate amount, or large amount (Fig. 4)a

Free fluid

No free fluid, free fluid in right lower quadrant or distant free fluid (e.g., in the Morrison pouch or
in the pelvis)

Abscessb

Present or absent (Fig. 5)

aSmall amount, small area of echogenic fat seen on one side of the appendix; moderate, echogenic fat surrounding the entire circumference of the appendix; large, large

amount of echogenic fat occupying a large region in the right lower quadrant or extending to the pelvis (Fig. 4).

bCollection of complex material with increased blood flow at its walls and no flow at its center in color Doppler examination.

Clinical data, including age, sex, and findings in surgical and pathologic reports, were collected from
computerized medical charts.

Ultrasound Examinations

Fig. 13-year-old girl with acute nonperforated


appendicitis. Ultrasound image shows measurement
of appendiceal diameter (calipers) from serosa to
serosa.

sults with results of previous studies in which


ultrasound and CT images were evaluated for
findings of perforation.
Materials and Methods
Patient Data
This retrospective study, approved by our institutional review board (informed consent waived),
included pediatric patients from two medical centers: a level 1 trauma center with a pediatric emergency department and a childrens hospital. At
both centers patients were identified in the radiology PACS. The medical charts were then evaluated to determine which patients would be included. Inclusion criteria were ultrasound diagnosis of
acute appendicitis, appendectomy, and pathologic review of the appendix. The records of 72 patients consecutively registered at the trauma center between November 2005 and November 2011
and of 91 patients consecutively registered at the
childrens hospital between January 2008 and July
2009 were identified. Two patients were excluded
because it was unclear from the surgical reports
whether appendiceal perforation had occurred.

958

Ultrasound examinations were performed with


one of two scanners (HDI 5000 or IU 22, Philips
Healthcare) by certified ultrasound technologists.
The graded compression technique was used. The
diagnostic criteria for appendicitis were based on
previous reports [14, 15].
All ultrasound images were reviewed by one of
two experienced pediatric radiologists blinded to
the surgical and pathologic results. The radiologists reviewed the imaging findings detailed in Table 1, which included transverse diameter of the
appendix (Fig. 1), presence or absence of an appendicolith (Fig. 2), evaluation of the submucosal
layer of the appendix (Fig. 3), amount of periappendiceal echogenic fat (Fig. 4), and presence or
absence of an abscess (Fig. 5) or free fluid.
The surgical report served as the reference standard for determining appendiceal perforation. When
the surgical report documented perforation that was
not confirmed in the pathology report, it was assumed that the pathologic specimen did not include
the site of perforation. When the pathology report
documented perforation that was not evident at surgery, it was assumed that the perforation occurred
during surgery or during handling of the specimen
or that it was a microperforation (which for the purpose of management would not be different from
nonperforation). In a subset of five children who
underwent delayed elective appendectomy, the diagnosis of perforation was based on imaging findings. In these patients, ultrasound followed by CT
showed appendicitis and periappendicular abscesses. The patients were treated conservatively with IV
antibiotics and percutaneous drainage of abscesses.

Further analysis for specificity and sensitivity of


the models and of isolated variables was performed
with Microsoft Excel software. The Pearson chisquare test was performed to evaluate the statistical
significance of various sonographic findings and to
determine the statistical significance of the perforation rate difference between the two age groups resulting from the Eureqa Formulize analysis.

Results
The study included 161 pediatric patients
(94 boys, 67 girls; age range, 120 years;
mean, 11 4.4 [SD] years). A final diagnosis
of perforated appendicitis was made in 58 cases (36.0%); 103 patients (64%) had nonperforated appendicitis. Table 2 details the distribution of age, sex, and sonographic findings in
the study group. The results of the Eureqa Formulize analysis showed that abscess was associated with perforation and that in children
younger than 8 years, appendicolith and loss
of the echogenic submucosal layer were independently associated with perforation.
The sensitivity and specificity of various
sonographic findings and their statistical sig-

Statistical Analysis
Data modeling was performed with Eureqa Formulize (Nutonian) [16] tuned to seek binary models to diagnose perforation with high specificity.

Fig. 211-year-old girl with acute perforated


appendicitis. Ultrasound image shows shadowing
appendicolith (arrow) in appendiceal lumen.

AJR:200, May 2013

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Ultrasound of Pediatric Appendicitis

Fig. 3Submucosal echogenic layer.


A, 10-year-old boy with acute nonperforated appendicitis. Ultrasound image shows submucosal echogenic
layer (arrowheads) in inflamed appendix.
B, 9-year-old boy with acute perforated appendicitis. Ultrasound image shows region of normal submucosal
layer (black arrowhead) in inflamed appendix but loss of echogenic submucosal layer (white arrowheads) in
distal segment of appendix.

nificance as determined with p values are


detailed in Table 3. Presence of an abscess,
presence of an intraluminal appendicolith,
and loss of the echogenic submucosal layer
of the appendiceal wall were statistically significant findings associated with appendiceal
perforation (p < 0.001, p = 0.001, and p =
0.002). Although the presence of an abscess
was highly specific for perforation (specificity, 99%), the sensitivity was low (36%). The
presence of an appendicolith and loss of the
echogenic submucosal layer of the appendix
were neither sensitive nor specific when the
entire study population was evaluated; how-

ever, the sensitivity and specificity of both


findings increased if the child was younger
than 8 years (sensitivity, 68.4% and 100%;
specificity, 91.7% and 72.7%).
The finding of free fluid distant from the
appendix (p = 0.12) and the presence of a
large amount of echogenic fat around the appendix (p = 0.13) were found not to have a
statistically significant association with appendiceal perforation. These findings had
moderately high specificities (78.4% and
89.3%). The finding of free fluid in the right
lower quadrant and the presence of a small to
moderate amount of periappendiceal echo-

genic fat had low sensitivity and specificity


(sensitivity, 32.8% and 73.7%; specificity,
54.9% and 45.6%).
When the presence of more than one sonographic finding was evaluated, the combined
specificities and sensitivities were either negatively affected or not improved substantially compared with the separate analysis of
each finding. For example, the combination
of age younger than 8 years and appendicolith or loss of the echogenic submucosal layer
resulted in sensitivity of 95% and specificity of 75%. The combination of age younger
than 8 years, appendicolith, and loss of the
echogenic submucosal layer resulted in sensitivity of 68.8% and specificity of 90.9%.
The perforation rate in young children was
significantly higher than that in older children. Perforation was found in 20 of 32 children younger than 8 years (62.5%) while only
38 of 129 children 8 years and older (29.5%).
This difference was statistically significant
(p< 0.001) perforated. The sensitivity and
specificity were 34.5% and 88.3%. Of the 38
older children with perforation, 17 had an abscess at presentation (44.7%), while only 4 of
20 (20%) younger children with perforation
had an abscess. Most of the patients 8 years
or older without an abscess did not have perforation (91/112, 81.3%).
Discussion
In children with acute appendicitis, the risk
of appendiceal perforation ranges from 23% to
73% [1]. Lee et al. [17] reported that perforation occurred with greater incidence in children

Fig. 4Periappendiceal echogenic fat.


A, 17-year-old boy with acute nonperforated appendicitis. Ultrasound image shows inflamed appendix with small amount of periappendiceal echogenic fat (arrowheads)
on only one side of appendix.
B, 10-year-old girl with acute nonperforated appendicitis. Ultrasound image shows moderate amount of echogenic fat (arrowheads) encircling appendix (calipers).
C, 10-year-old boy (same patient as in Fig. 3A). Ultrasound image shows large amount of periappendiceal echogenic fat (arrowheads) encircling appendix and extending
peripherally.

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Blumfield et al.
TABLE 2: Distribution of Age, Sex, and Sonographic Findings
Characteristic
No. of patients

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Age (y)

Perforated

Nonperforated

58

103

9.3 4.5

12 4

Sex
Girls

22

45

Boys

36

58

1.2 0.36

1.1 0.3

Appendicolith

31 (53)

30 (29)

Loss of echogenic submucosal layer

38 (75)

48 (47)

Appendix diameter (cm)

Patients excludeda
Amount of echogenic fat
Fig. 55-year-old girl with acute perforated
appendicitis. Ultrasound image shows outline of
walled-off fluid collection (calipers), internal echoes,
and foci of gas consistent with abscess.

younger than 5 years and that abscess formation at presentation occurred more commonly
in children older than 10 years. Our results
concur with those in that report. We found a
significantly higher rate of perforation in children younger than 8 years (62.5%) than in older children (29.5%). Similarly, older children
had a higher incidence of abscess at presentation (44.7%) than did younger children (20%).
Once the diagnosis of appendicitis is made,
differentiation of perforated from nonperforated appendicitis becomes important. Emergency surgery is indicated for nonperforated
appendicitis, whereas the initial therapy for
perforated appendicitis may be nonsurgical
because nonsurgical treatment has a lower
complication rate [24]. Thus to avoid delay
of a required surgical procedure, diagnosing
perforated appendicitis with high specificity
is desired. In our study, the findings of an abscess, an intraluminal appendicolith, and loss
of the submucosal echogenic layer of the appendix were found to be associated with appendiceal perforation. These associations are

None

9 (16)

24 (23)

Small

6 (11)

23 (22)

Moderate

31 (54)

45 (44)

Large

11 (19)

11 (11)

Patients excludedb

Free fluid
None

28 (48)

56 (55)

Right lower quadrant

11 (19)

24 (24)

Distant

19 (33)

22 (22)

Appendix identified

54 (93)

103 (100)

Abscess

21 (36)

1 (1)

Patients excludedc

Patients excludedc

NoteExcept for age and size, values are numbers of patients. Values in parentheses are percentages.
aExcluded because ultrasound images were suboptimal, appendiceal walls were not adequately visualized.
bAppendix and surrounding fat not visualized.
cUltrasound study included only images of the appendix; presence of an abscess and distant free fluid could
not be determined.

statistically significant (p< 0.001, p= 0.001,


and p= 0.002). The finding of an abscess was
associated with perforation with high specificity (99.0%) but low sensitivity (36.2%).
The finding of an appendicolith in a child
younger than 8 years also had high specificity (91.7%). This concurs with the findings of

a 2012 study [18] that showed an increased


incidence of necrosis and perforation of the
appendix when an appendicolith was present.
Although loss of the echogenic submucosal
layer was found to be highly sensitive for perforation in young children (100%), the specificity was low (72.7%). Therefore we do not

TABLE 3: Sensitivity and Specificity of Sonographic Findings


Finding
Abscess

No. of Patients

pa

Sensitivity (%)

Specificity (%)

160

< 0.001

36.2

99.0

Loss of echogenic submucosal layer

153

0.001

74.5

52.9

Appendicolith

160

0.002

54.4

70.9

Free fluid distant from the appendix

160

0.12

32.8

78.4

Large amount of echogenic fat around the appendix

160

0.13

19.3

89.3

Loss of the echogenic submucosal layer and age < 8 y

28

< 0.001

Appendicolith and age < 8 y

31

0.14

100
68.4

72.7
91.7

aPearson chi-square test.

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AJR:200, May 2013

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Ultrasound of Pediatric Appendicitis


recommend relying solely on this sonographic
finding because it can lead to false diagnosis
of perforation and delay needed surgery. The
findings of a large amount of periappendiceal
echogenic fat and of free fluid distant from the
appendix have limited diagnostic value (sensitivity, 32.8% and 19.3%; specificity, 78.4%
and 89.3%). Findings with no significant diagnostic value include appendix size, presence
of a small or moderate amount of periappendiceal echogenic fat, and free fluid in the right
lower quadrant.
In a 1992 study by Quillin et al. [13], sonographic findings of perforated appendicitis were evaluated in 71 children. Those investigators suggested an association between
perforation of the appendix and loss of the
echogenic submucosal layer. However, the
specificity and sensitivity of this finding were
very low, in part because the appendix was not
identified in most of the patients with perforation. In our study, we identified the appendix
in 54 of 58 patients with perforated appendicitis and found that loss of the echogenic submucosal layer had a higher diagnostic value
in young patients. Similarly, although Quillin et al. reported no association between appendicolith and perforation, our study showed
that in children younger than 8 years, the presence of an appendicolith correlated with perforation. In 1990, Borushok et al. [12] evaluated the sonographic findings of perforated
appendicitis in 100 adults and children. They
found that a combination of pericecal collections, loss of the echogenic submucosal layer
of the appendix, and prominent pericecal fat
had moderately high sensitivity (86%) but low
specificity (60%) for perforation.
The discrepancies between our study and
the previous studies may be explained by the
technologic advances in sonographic imaging that have occurred since the early 1990s.
In addition, our sample size was larger and
allowed separate analysis of different pediatric age groups.
We compared our results with those of
studies of the effectiveness of CT in diagnosing perforated appendicitis [8, 19] and
found that the sensitivities of our sonographic findings (19100%) are comparable to
the reported CT sensitivities of various findings (2164%). Although the specificities of
our sonographic findings, ranging between
72.7% and 99%, are lower than the reported
specificities of CT findings (93100%), the
finding of an appendicolith in a young child
and the finding of an abscess at any age had
comparable specificities (91.7% and 99%).

The limitations of our study included small


sample size of the younger age group (<8
years, 32 patients) and omission of Doppler
findings due to inconsistent settings in this retrospective study.
CT is currently the modality of choice for
differentiating perforated from nonperforated appendicitis because this differentiation cannot be made accurately on a clinical
basis. Even in the group of young children
(< 8 years), who tend to experience perforation more frequently, a substantial number
presented with nonperforated appendicitis
(12/32). Our study showed that ultrasound
of children is effective in diagnosing perforation of the appendix, thus it has the potential to replace and thereby reduce the number
of CT examinations commonly performed in
this situation. The diagnosis of perforated
appendicitis can be reliably made when an
abscess is detected with ultrasound. In children younger than 8 years, who tend to have
perforation without abscess formation, the
differentiation is more complicated. In that
age group, the findings of an appendicolith,
loss of the appendiceal echogenic submucosal layer, a large amount of periappendiceal
echogenic fat, and free fluid in the Morrison
pouch or pelvis are associated with perforation in a decreasing order of significance.
Conclusion
In children, ultrasound is useful in the diagnosis of perforated appendicitis and should
suffice as the modality of choice whenever the
appendix is identified. The decision to perform
appendectomy or to treat a patient conservatively should be made in association with clinical findings. CT should be reserved for complicated cases in which the appendix is not
identified or the presence or absence of perforation cannot be determined with ultrasound.
References
1. Sivit CJ. Imaging the child with right lower quadrant pain and suspected appendicitis: current concepts. Pediatr Radiol 2004; 34:447453
2. Oliak D, Yamini D, Udani VM, et al. Nonoperative
management of perforated appendicitis without periappendiceal mass. Am J Surg 2000; 179:177181
3. Simillis C, Symeonides P, Shorthouse AJ, Tekkis
PP. A meta-analysis comparing conservative treatment versus acute appendectomy for complicated
appendicitis (abscess or phlegmon). Surgery 2010;
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4. Henry MC, Gollin G, Islam S, et al. Matched
analysis of nonoperative management vs immediate appendectomy for perforated appendicitis. J

Pediatr Surg 2007; 42:1923


5. Oliak D, Yamini D, Udani VM, et al. Can perforated appendicitis be diagnosed preoperatively
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6. Alaedeen DI, Cook M, Chwals WJ. Appendiceal
fecalith is associated with early perforation in pediatric patients. J Pediatr Surg 2008; 43:889892
7. Tsuboi M, Takase K, Kaneda I, et al. Perforated
and nonperforated appendicitis: defect in enhancing appendiceal walldepiction with multi-detector row CT. Radiology 2008; 246:142147
8. Bixby SD, Lucey BC, Soto JA, Theysohn JM,
Ozonoff A, Varghese JC. Perforated versus nonperforated acute appendicitis: accuracy of multidetector CT detection. Radiology 2006; 241:780
786; erratum, 2007; 243:302
9. Brenner DJ, Hall EJ. Computed tomography: an
increasing source of radiation exposure. N Engl J
Med 2007; 357:22772284
10. Pearce MS, Salotti JA, Little MP, et al. Radiation
exposure from CT scans in childhood and subsequent risk of leukaemia and brain tumours: a retrospective cohort study. Lancet 2012; 380:499505
11. Goldin AB, Khanna P, Thapa M, McBroom JA,
Garrison MM, Parisi MT. Revised ultrasound criteria for appendicitis in children improve diagnostic accuracy. Pediatr Radiol 2011; 41:993999
12. Borushok KF, Jeffrey RB Jr, Laing FC, Townsend
RR. Sonographic diagnosis of perforation in patients
with acute appendicitis. AJR 1990; 154:275278
13. Quillin SP, Siegel MJ, Coffin CM. Acute appendicitis in children: value of sonography in detecting
perforation. AJR 1992; 159:12651268
14. Ramarajan N, Krishnamoorthi R, Barth R, et al.
An interdisciplinary initiative to reduce radiation
exposure: evaluation of appendicitis in a pediatric
emergency department with clinical assessment
supported by a staged ultrasound and computed
tomography pathway. Acad Emerg Med 2009;
16:12581265
15. Kaiser S, Frenckner B, Jorulf HK. Suspected appendicitis in children: US and CTa prospective
randomized study. Radiology 2002; 223:633638
16. Schmidt M, Lipson H. Distilling free-form natural laws from experimental data. Science 2009;
324:8185
17. Lee SL, Stark R, Yaghoubian A, Shekherdimian
S, Kaji A. Does age affect the outcomes and management of pediatric appendicitis? J Pediatr Surg
2011; 46:23422345
18. Azok JT, Kim DH, Munoz Del Rio A, et al. Intraluminal air within an obstructed appendix: a CT
sign of perforated or necrotic appendicitis. Acad
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19. Horrow MM, White DS, Horrow JC. Differentiation of perforated from nonperforated appendicitis at CT. Radiology 2003; 227:4651

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APPENDIX 1: AJR Journal Club

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Study Guide

Ultrasound for Differentiation Between Perforated and Nonperforated


Appendicitis in Pediatric Patients
Alan Mautz, Margaret Mulligan, Joseph J. Budovec*
Medical College of Wisconsin, Milwaukee, WI
amautz@mcw.edu, mmulliga@mcw.edu, jbudovec@mcw.edu
Introduction
1. What is the clinical question being asked? What is the authors hypothesis? How would you state the alternative hypothesis?
2. What is the current reference standard for the evaluation of appendicitis in children? How sensitive, specific, and accurate is that test?
Methods
3. What were the inclusion criteria for the study? What were the exclusion criteria?
4. Does the study address potential discrepancies between surgical and pathologic findings related to perforation appropriately?
5. What are the limitations of this study? Are these limitations adequately discussed?
6. Were appropriate statistical tools used to determine the significance of the sensitivities and specificities of the imaging findings in
appendicitis?
Results
7. Were the research questions answered? Were the hypotheses resolved?
8. Was the sample size large enough to draw conclusions on the basis of patient age with respect to rates of appendiceal perforation?
9. What demographic and sonographic findings are associated with increased rates of perforation in appendicitis?
Physics
10. What is the normal sonographic appearance of the appendix? How does graded compression sonography contribute to the diagnostic test?
What is the accuracy of compression sonography in diagnosing appendicitis?
Discussion
11. At your institution, how frequently is ultrasound used as the first-line imaging modality in pediatric patients with right lower quadrant
pain? Do you recommend or plan on recommending ultrasound instead of CT for such situations in the future?
12. What is the average CT dose for pediatric patients undergoing CT for possible appendicitis at your institution? How do CT and ultrasound
compare at your institution for evaluation of appendicitis?
13. What outcomes data might augment the power of this study? Is the study designed well enough and powerful enough to evoke change in
managing pediatric patients for whom appendicitis is a concern?
Background Reading
1. Goldin AB, Khanna P, Thapa M, McBroom JA, Garrison MM, Parisi MT. Revised ultrasound criteria for appendicitis in children improve diagnostic accuracy. Ped
Radiol 2011; 41: 993999
2. Kaise S, Frenckner B, Jorulf HK. Suspected appendicitis in children: US and CTa prospective randomized study. Radiology 2002: 223:633638

*Please note that the authors of the Study Guide are distinct from those of the companion article.

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