Pediatric Appendiceal Ultrasound
Pediatric Appendiceal Ultrasound
Pediatric Appendiceal Ultrasound
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ORIGINAL ARTICLE
Received: 14 February 2015 / Revised: 8 May 2015 / Accepted: 7 July 2015 / Published online: 18 August 2015
# Springer-Verlag Berlin Heidelberg 2015
emergency department evaluations, delayed or unneces- US, presence of right-lower-quadrant (RLQ) pain, wheth-
sary surgeries and increased perforation rates [2–4]. Imag- er sonography was performed on-call or off-call, US re-
ing can play an important role in evaluation of acute ap- sults, pathological findings and clinical follow-up for chil-
pendicitis, especially when classic signs and symptoms are dren who did not undergo surgery.
absent [5]. Imaging with US, CT and more recently MRI
have been used [6, 7], and there continues to be a debate Imaging protocol
over which modality is best [8–10]. US evaluation for
acute appendicitis was first described by Puylaert [11] The US examinations were performed supine with graded
and was quickly applied to pediatric patients [12]. The compression of the RLQ using the most current GE Logiq
American College of Radiology considers US to be the platform scanners, presently E-9 (GE Healthcare, Fair-
most appropriate imaging modality for the initial evalua- field, CT) and high-frequency linear and sector probes.
tion of acute appendicitis because of its lack of ionizing Static transverse and longitudinal images as well as mul-
radiation [13], high sensitivity [14] and low cost [15]. tiple cine clips throughout the RLQ with and without
However CT has demonstrated higher specificity (94% graded compression are routinely obtained. The imaging
vs. 88%) with similar sensitivity (95% vs. 94%) compared protocol did not change during the course of the study.
to US [14]. MRI for acute appendicitis has also shown Studies obtained during routine hours (off-call, Monday–
excellent sensitivity and specificity [6, 7]. There is a wide Friday 7 am–5 pm) were performed by any one of more
range of sensitivities and specificities reported with US than 50 general sonographers. These studies are reviewed
[14, 16], and this is thought to be a result of operator by one of several pediatric radiologists with a Certificate
dependence and patient and system factors. It has been of Added Qualification, prior to patient discharge. If the
suggested that CT might be a better first-line imaging normal appendix was not visualized, the radiologist would
modality in obese patients and those with short symptom typically rescan the child. The reviewing radiologist may
duration [17, 18]. The diagnostic yield of appendiceal US also choose to rescan patients to clarify imaging findings.
has been found to be poor when performed by technolo- Studies conducted outside of the routine hours (on-call)
gists with little pediatric experience [16, 19], at institu- were performed by one of four on-call sonographers with
tions where it is not the initial imaging study and when an average of more than 20 years of sonographic
the appendiceal visualization rate is low [16]. Thus in experience.
some practices and for some patients, CT may be chosen
over US for the initial assessment of acute appendicitis. US report categorization
The purpose of this report is to assess the impact of patient
and system factors on the accuracy and indeterminate study We categorized the US reports in the patients’ record at
rate on pediatric appendiceal US and to investigate how inde- the time of the decision to operate or discharge. These
terminate results impact patient outcomes. include six revised reports of the 581 on-call studies ini-
tially interpreted by radiology residents and subsequently
reviewed by a staff pediatric radiologist. The US reports
Materials and methods were retrospectively categorized (by K.M.L.U. and
L.A.B.) as follows:
Patient population
& US-0, no appendicitis: Normal appendix visualized from
Our institutional review board approved this retrospective base to tip. Rarely, a small portion of the appendix might
review of all pediatric (<18 years old) abdominal US re- have been obscured by cecal gas but the radiologist’s im-
ports performed at Mayo Clinic Rochester between Janu- pression was no appendicitis. There was no recommenda-
ary 2010 and June 2014. We included all studies ordered tion for CT or clinical follow-up.
for the evaluation of acute abdominal symptoms. Children & US-1, no appendicitis: Appendix not visualized. No sec-
were identified for inclusion based on a search of all ab- ondary signs of appendicitis, including periappendiceal fat
dominal US reports that contained the words “appendix” thickening, increased echogenicity or hyperemia. The
or “appendicitis.” Children were excluded if they previ- presence of pain with transducer pressure was evaluated
ously had an appendectomy or a CT scan for acute appen- but not incorporated into the US categorization because of
dicitis prior to the US, if the US was performed at an the variability in patients’ ability to report pain and the
outside institution, and if the child did not undergo an highly subjective nature of this finding. There was no
appendectomy and had no clinical follow-up after dis- recommendation for CT or clinical follow-up.
charge. We recorded patient age, gender, height, weight, & US-2, appendicitis: Abnormal appendix visualized and
body mass index (BMI), symptom duration at the time of interpreted as consistent with acute appendicitis. There
1936 Pediatr Radiol (2015) 45:1934–1944
was no recommendation for CT or clinical follow-up. for evaluation of continuous variables such as BMI-FAP;
Standard signs for appendicitis were used and included: the chi square and Fisher exact tests were used for com-
appendiceal diameter greater than 6 mm and non-com- parison of discrete variables, such as accuracy off-call vs.
pressible, loss of appendiceal wall architecture, hyperemia on-call. Statistical significance was set at P < 0.05. The
and presence of an appendicolith as well as presence of the following definitions were used for assessment of diag-
secondary signs listed in US-1. nostic performance:
& US-3, equivocal: Appendix visualized but the appearance
was thought to be indeterminate. Includes cases where the & True positive (TP): US-2 and P-1, P-2 or P-3
appendiceal diameter was >6 mm or non-compressible or & True negative (TN): US-0 or US-1 and P-0 or P-X
there was RLQ fluid but the studies were not thought to be & False positive (FP): US-2 and P-0 or P-X
diagnostic of acute appendicitis. CT or clinical follow-up & False negative (FN): US-0 or US-1 and P-1, P-2 or P-3
was sometimes recommended. & Indeterminate-positive (IP): US-3, US-4 or US-5 and
& US-4, equivocal: Appendix not visualized and acute P-1, P-2 or P-3
appendicitis not ruled out. These reports differ from & Indeterminate-negative (IN): US-3, US-4 or US-5 and
US-1 in that the initial radiologist’s report did not P-0 or P-X
specifically describe the absence of periappendiceal
findings. CT or clinical follow-up was sometimes Determination of the diagnostic yield of US for acute
recommended. appendicitis was performed using the intention-to-
& US-5, technically inadequate: The RLQ was insufficiently diagnose calculations [20], including all 790 US studies,
evaluated because of bowel gas. as follows: accuracy=(TP+TN)/(TP+TN+FP+FN+IP+IN),
sensitivity=TP/(TP+FN+IP) and specificity=TN/(TN+FP+
IN). A second set of calculations was performed exclud-
Pathology report categorization ing the equivocal (US-3 and US-4) or technically inade-
quate (US-5) studies. This was done because these inde-
Pathology reports were categorized as follows based on the terminate studies do not contribute to the decision to
initial reading: operate or discharge in our practice [21]. The diagnostic
performance of US was then calculated as follows:
& P-0, negative: Normal appendix. sensitivity=TP/(TP+FN), specificity=TN/(TN+FP) and
& P-1, minimal/early appendicitis: The terms minimal or accuracy=(TP+TN)/(TP+TN+FP+FN).
early were used in the report. This typically indicates neu-
trophilic infiltration, predominately of the appendiceal
epithelium.
& P-2, appendicitis: Abnormal with detailed description of Results
microscopic findings of acute appendicitis with neutro-
philic infiltration of the appendiceal epithelial and muscu- During the study period 849 US reports included the
lar layers. terms appendix or appendicitis. Studies were excluded
& P-3, perforated appendix: Acute appendicitis with gross as follows: no clinical follow-up (n=20), duplicate or-
perforation of the appendiceal wall. ders (n=17), not performed at Mayo Clinic Rochester
& P-X, patients who did not undergo surgery and did not (n=11), performed to clarify CT findings (n=6) or per-
have acute appendicitis on clinical follow-up. formed in children with a prior appendectomy (n=5). A
total of 790 examinations met inclusion criteria and in-
cluded 452 girls (57%) and 338 boys (43%). The mean
Statistical analysis age was 10.4+/−4.5 years. BMI was available in 622
(79%) children and averaged 19.8+/−4.8. BMI-FAP is
Using SAS© (version 9.2; SAS Institute, Cary, NC) for defined for children older than 2 years and was avail-
analysis, group statistics are presented as mean/standard able in 571 (72%) children, distributed as follows: 3%
deviation (SD) for continuous variables and n (%) for underweight (<5th percentile) and 23% overweight
categorical variables. The Cochran-Armitage trend test (>85th percentile) indicating a slightly overweight bias
was used to detect trends in accuracy, appendiceal visual- in our study group [22]. Most studies (581, or 73%)
ization and determinacy across years of study as well as were performed on-call; 209 (27%) studies were per-
accuracy among groups categorized by age, BMI for age formed off-call. There were 146 cases of acute appen-
percentile (BMI-FAP), symptom duration, pathology dicitis for an overall prevalence of 18.5%, which was
grade or symptom duration. The Student’s t-test was used similar for off-call and on-call studies, with off-call
Pediatr Radiol (2015) 45:1934–1944 1937
Table 1 Group 1 (definitive US) vs. group 2 (indeterminate US) Table 3 Diagnostic yield of US
Appendiceal visualization
Fig. 2 US accuracy and body mass index. Graph shows that US accuracy Fig. 4 US accuracy and pathological grade of appendicitis. Graph shows
is independent of body mass index for age percentile (BMI-FAP). The that US accuracy is independent of pathological grade. The trend of
study group was skewed slightly toward overweight, with 22% of the higher accuracy with increasing severity of appendicitis did not reach
children above the 85th percentile statistical significance
Pediatr Radiol (2015) 45:1934–1944 1939
considered negative [23, 24]. In this group, there were five US accuracy and determinacy
false-negative studies, yielding a 98% negative predictive val-
ue. The decisions to operate in the five false-negative children Despite decades of clinical experience with US for the evalu-
were based on CT in one and on clinical findings in four. ation of acute appendicitis, controversy remains. Its sensitivity
There was a single false-negative case of acute appendicitis and specificity have been reported to be approximately 90%
where the appendix was visualized and thought to be normal [14], but certain patient and system factors have been reported
(US-0). The resected appendix measured 5 mm in diameter to reduce its accuracy [17–19]. Its diagnostic yield has been
Table 4 Appendiceal
visualization Visualized (US 0, 2, 3) Not visualized (US 1, 4) Totala P-value
Age (years)
n 368 381 749 0.27
Mean (SD) 10.6 (4.3) 10.2 (4.6)
Range 0.0–17.0 0.0–17.0
Gender
Male 158 160 318 (42%) 0.58
Female 208 223 431 (58%)
Call status
On-call 288 263 551 (74%) 0.004
Off-call 80 118 198 (26%)
BMI
n 290 301 591 0.23
Mean (SD) 19.4 (4.2) 20.1 (5.3) 19.7 (4.8)
Range 12.0–36.0 12.0–52.0 12.0–52.0
BMI-FAP
n 283 287 570 0.08
Mean (SD) 61.1 (26.5) 64.1 (28.5) 62.6 (27.6)
Median 64 71 66.5
Range 3–99 3–99 3–99
reported to be well below reported accuracies because of rel- confidently interpreted as negative for appendicitis. Had all
atively high rates of indeterminate results [21]. Although such studies been re-categorized, our negative predictive val-
appendiceal US exams may be indeterminate in clinical prac- ue would have decreased from 0.979 to 0.940, indicating a
tice, the definition of what makes a study indeterminate is not slight increase in false-negative reports. This would substan-
standard. Lack of complete visualization of the appendix has tially reduce the indeterminate rate but could also result in a
been considered to be indeterminate for acute appendicitis, small increase in the number of false-negative studies. In these
and with this definition Krishnamoorthi et al. [25] reported a patients our false-negative rate was 2%, similar to other au-
47% indeterminate study rate. Prior to determining the accu- thors [23, 26], and was not significantly different from the
racy and diagnostic yield of US in acute appendicitis, the false-negative rate when a normal appendix was visualized,
decision of how to categorize indeterminate studies must be 0.5%. It is important to note that none of the five children with
made because the manner in which these studies are included false-negative US studies was discharged from the emergency
in statistical analyses has a great effect on the diagnostic yield department with unrecognized acute appendicitis; all were
of US. Authors may choose a best-case scenario (indetermi- further assessed and underwent an appendectomy where acute
nate studies included as true positive and true negative) or a appendicitis was confirmed. With these findings, we have
worst-case scenario (studies included as false positive and since implemented a US report template that includes docu-
false negative) or both [14, 16]. Trout et al. [19] included mentation of the presence or absence of secondary signs of
exams that were indeterminate as “positive” because at their acute appendicitis, and in the absence of such findings the
institution, sonography that did not exclude the diagnosis of study is considered negative for acute appendicitis. An addi-
acute appendicitis could result in additional imaging or appen- tional strategy to decrease indeterminacy is the adoption of a
dectomy. This led to an increase in the number of false- binary reporting template that requires the interpreting radiol-
positive studies and decreased accuracy [19]. ogist to categorize the study as definitively positive or nega-
We analyzed the data two ways. In the first analysis, inde- tive for acute appendicitis. Using this strategy, Nielsen et al.
terminate studies were excluded and US was shown to have an [27] found their non-diagnostic rate to decrease from 48% to
accuracy of 96%. This analysis reflects the fact that in our 0.1% and found an increase in both sensitivity (67% to 92%)
practice indeterminate studies are not viewed as positive or and negative predictive value (89% to 98%).
negative and do not directly result in patient discharge, admis-
sion or operation [20]. The second analysis used the intention- Increasing accuracy
to-treat method and included indeterminate studies and
assessed the diagnostic yield of appendiceal US [21]. Our Although our accuracy rate of 96% is high when a definitive
indeterminate study rate of 28% is similar to other reports diagnosis is made, increases might be achieved with changes
[17, 18]. Including indeterminate studies in the statistical anal- to the standard US technique of supine RLQ graded compres-
ysis conveys to clinicians the proportion of patients with sion that increase appendiceal visualization [28, 29]. Increased
suspected acute appendicitis whose US study has not yielded visualization might allow re-categorization of US-4 cases to
definitive information and who need additional clinical or im- US-2 and increase the number of true-positive studies. How-
aging follow-up. ever, increased appendiceal visualization might not result in
improved accuracy [16]. Our appendiceal visualization rate
Decreasing indeterminacy increased steadily throughout the 5-year study period, but
US accuracy and the proportion of definitive US diagnoses
From a clinician’s standpoint, the need to reduce the number did not (Fig. 6). These observations suggest that the relation-
of indeterminate US studies is significant. If a relatively high ship between appendiceal visualization and accuracy is com-
proportion of US evaluations for acute appendicitis is indeter- plex. This may be because of the acute appendicitis cases that
minate, CT might be chosen as the initial imaging study or are always non-visualized (deep in the pelvis) or have minimal
patients might undergo unnecessary laparotomies. A diagnos- histological changes are still deemed acute appendicitis by the
tic test, no matter how accurate when a definitive diagnosis is pathologist. It is important to note that a reduction in the num-
given, is not clinically useful if the indeterminate rate is too ber of false-positive exams could be achieved if the US criteria
high. We have identified several strategies that can be used to for diagnosing acute appendicitis required the demonstration
reduce indeterminacy. The biggest reduction in the number of of thickening and increased echogenicity of the
indeterminate results with an increase in true-negative studies periappendiceal fat and did not rely solely on an increased
might be achievable by increasing the emphasis placed on the appendiceal diameter [24]. The US diagnosis of acute appen-
significance of the presence or absence of secondary signs of dicitis in 15 of our 17 false-positive studies relied solely on a
acute appendicitis. When a thorough RLQ US examination minimal increase of appendiceal diameter above 6 mm with-
has been performed, the absence of appendiceal visualization out any periappendiceal inflammatory changes. Appendiceal
and any secondary findings for acute appendicitis can be diameter in isolation is a poor predictor of acute appendicitis,
Pediatr Radiol (2015) 45:1934–1944 1941
Age
Body habitus
Symptom duration
illness.” Our US accuracy was unaffected by symptom dura- frequently than general sonographers [19]. We found no dif-
tion, indicating that additional imaging confirmation of nega- ference in the accuracy of off-call and on-call US examina-
tive US findings in patients with symptoms less than 24 h tions, at 99% and 95% respectively, P=0.08. However, we
should not be routinely obtained. found that on-call studies had higher rates of appendiceal vi-
sualization (52% vs. 40%, P=0.0042) and determinacy (75%
Pathological grade vs. 67%, P=0.03). This likely reflects the increased experi-
ence of the on-call sonographers at our institution.
The relationship between the diagnostic yield of
appendiceal US and the pathological grade of acute ap- The negative clinical impact of indeterminate studies
pendicitis might be complicated by the relatively subjec-
tive nature of pathological grading. Bachur et al. [18] One of the major reasons for imaging children who are
found that US sensitivity was greater for perforated than suspected of having acute appendicitis is to reduce the
non-perforated acute appendicitis. We had similar sensi- need for CT imaging and the negative appendectomy rate.
tivities for early/mild appendicitis (88%), appendicitis The negative appendectomy rate based on the clinical eval-
(94%) and perforated (100%) appendicitis, P=0.37. uation alone can be reduced with the addition of US.
Karakas et al. [35] found the rate to decrease from 13%
US accuracy: system factors and appendiceal visualization to 8% with the addition of US. When using a standardized
and validated US reporting template that required the
Trout et al. [19] noted increasing US accuracy and rates of interpreting radiologist to make a definitive diagnosis,
appendiceal visualization in the later years of their 5-year ret- Nielsen et al. [27] found the rate of negative appendecto-
rospective review, suggesting that the progressively improv- mies to be reduced four-fold and the follow-up CT rate
ing performance might be a result of increasing technical and reduced five-fold compared to studies that were reported
interpretive expertise attained during the study. Specifically, without following the template and could yield indetermi-
appendiceal visualization rates increased from 6% in the first nate results. Our results confirm these findings; we found a
year of their review to 29% in the fifth year. We also found an two-fold reduction in the negative appendectomy rate and
increasing appendiceal visualization rate over time, 32% visu- a four-fold reduction in the rate of follow-up CT studies
alization in the first year and 51% in the fifth, P=0.01. A wide when definitive US interpretations were made.
range of pediatric appendiceal US visualization rates have
been reported. Lee et al. [34] noted a 98% visualization rate Limitations
in patients of all ages with the use of posterior manual
compression in addition to standard supine compression, There are several limitations to our study. First, the US scores
but this high level has not been repeated in North America. were based on the interpretations of the US studies by several
Rompel et al. [29] increased their appendiceal visualization pediatric radiologists at the time care was given and were
rate from 86% to 93% with the addition of harmonic im- reviewed and retrospectively categorized. The vast majority
aging to the standard protocol. Mittal et al. [16] found the of the initial interpretations clearly fell into one of the US
visualization rate to be lower at hospitals where US is used categories but approximately 40 studies did not; this occurred
less frequently or is less available (25%) than at hospitals almost entirely when the US interpretation indicated that there
where it is available at all times and is the primary imaging were no secondary signs of acute appendicitis but there was a
test for acute appendicitis (56%). Chang et al. [28] in- lack of visualization of the normal appendix. These studies
creased the appendiceal visualization rate from 35%, when were initially interpreted as indeterminate but were catego-
they used supine graded compression US, to 59% when left rized in this study as negative for acute appendicitis, US-1,
posterior oblique imaging of the right flank was added to rather than indeterminate, US-4.
supine imaging. A second potential limitation is the lack of dedicated
Trout et al. [19] found that sensitivity and accuracy of follow-up in children who did not have surgery for acute ap-
appendiceal US was greater during off-call hours (when stud- pendicitis. If their clinical charts indicated any form of follow-
ies were performed by dedicated pediatric sonographers and up after the initial acute appendicitis evaluation, with no indi-
staffed by pediatric radiologists) than on-call hours (when cation of an interval appendectomy, the children were consid-
studies were performed by general sonographers and staffed ered negative for acute appendicitis. The lack of dedicated
by non-pediatric radiologists). They also found that the dedi- follow-up, such as phone calls at 24 h after discharge, could
cated pediatric sonographers identified the appendix more result in under-reporting of missed cases of acute appendicitis.
Pediatr Radiol (2015) 45:1934–1944 1943
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