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ª Springer Science+Business Media New York 2016 Abdom Radiol (2016)

Abdominal DOI: 10.1007/s00261-016-0862-0

Radiology

The role of preoperative graded compression


ultrasound in detecting acute appendicitis and
influencing the negative appendectomy rate
Bader Hamza Shirah,1 Hamza Asaad Shirah,2 Wael Awad Alhaidari,3
Mohamed Ali Elraghi,4 Mohammad Azam Chughtai4
1
King Abdullah International Medical Research Center, King Saud bin Abdulaziz University for Health Sciences, P.O.Box 65362,
Jeddah 21556, Saudi Arabia
2
Department of General Surgery, Al Ansar General Hospital, Medina, Saudi Arabia
3
Department of Accidents and Emergency, Al Ansar General Hospital, Medina, Saudi Arabia
4
Department of Radiology, Al Ansar General Hospital, Medina, Saudi Arabia

Abstract ing true positive cases of acute appendicitis, and thus


reducing the negative appendectomy rate. Values of
Purpose: The diagnosis of acute appendicitis is mainly 100% specificity, and 8.4% negative appendectomy rate,
clinical and is correct in about 80% of patients, but 20– or better, could be achieved, when an experienced
33% present with atypical findings, which resulted in a surgeon and a professional radiologist collaborate in
negative appendectomy rate of 20–30%. The graded the diagnosis of acute appendicitis.
compression ultrasound method in the diagnosis of acute
appendicitis was reported with a sensitivity of 89%, and
Key words: Acute appendicitis—
specificity of 95%. In this study, we aim to evaluate the
Ultrasound—Graded compression
graded compression ultrasonography in the diagnosis of
technique—Diagnosis—Appendectomy—
acute appendicitis, its influence on the clinical judgment
Negative appendectomy
to operate, and its role in lowering the negative appen-
dectomy rate.
Methods: 1073 patients treated surgically for acute
appendicitis between January 2005 and December 2014 Acute appendicitis is the most common emergency acute
were reviewed. Ultrasound findings, histopathological surgical abdomen with a lifetime risk of 8.6% in males
diagnosis, and positive or negative appendectomy rates and 6.7% in females, and a lifetime risk of appendectomy
were analyzed. of 12% in males and 25% in females. The incidence is
Results: 647 (60.3%) patients were males and 426 (39.7%) approximately 233/100,000 population, and it manifests
females. The mean age was 26.5 years. Positive ultra- most frequently during the second and third decades of
sound findings were recorded in 892 (83.13%), while life with the highest affected age group being between 10
negative findings were recorded in 181 (16.87%). Positive and 19 years of age, but it can occur at any age, with
appendectomy was recorded in 983 (91.6%), while 1.4:1 reported male-to-female ratio [1, 2].
negative appendectomy was recorded in 90 (8.4%). The The clinical judgment makes the diagnosis in about
sensitivity was 83%, specificity was 100%, and the rate of 80% of the cases. It depends on a good medical history
negative appendectomy was 8.39%. (right iliac fossa pain, nausea, and vomiting) and proper
Conclusion: Graded compression technique of ultra- physical examination (right iliac fossa tenderness and
sound is a useful modality, in addition to the clinical positive rebound tenderness). Nevertheless, in some pa-
judgment of the surgeon and clinical findings, in detect- tients, it becomes a difficult call to the surgeon causing a
diagnostic dilemma especially in making a decision to
operate or wait. The diagnostic certainty is dependent on
the clinical presentation of the patient, but the picture
Correspondence to: Bader Hamza Shirah; email: shirah007@ksau-hs. could be misleading by the varying positions of the
edu.sa
B. H. Shirah et al.: Graded compression ultrasound in acute appendicitis

appendix, and it was estimated that about 20–33% of the accuracy of ultrasound in the diagnosis of acute appen-
patients suspected as acute appendicitis cases could pre- dicitis was statistically found to be superior compared to
sent with atypical nonconclusive findings [3]. that of the surgeon’s clinical judgment (P < .0001).
The clinical outcome of a missed diagnosis of While 24% of the patients with normal ultrasound find-
appendicitis could be catastrophic. Therefore, the safest ings were found to have appendicitis at operation,
surgical practice is to operate on uncertain cases instead showing that ultrasound cannot be considered a reliable
of waiting to reach a certainty of the diagnosis, which led tool to the exclusion of the surgeon’s careful and re-
to an average increase in negative appendectomy rate of peated evaluation.
20–30% putting in mind the strategy of open and see In this study, we aim to analyze and evaluate the role
which considers the fact that an unnecessary operation is of graded compression ultrasound used as a diagnostic
safer than a perforation. The cost of negative appen- tool preoperatively, its influence on the clinical judgment
dectomies to the patient and the health care system is to operate, and whether it has any role in decreasing the
rather large, and a complication rate after removal of negative appendectomy rate.
normal appendices was reported to be up to 6.1% [4–6].
In 1986, Puylaert introduced the ultrasound graded Materials and methods
compression technique in the diagnosis of acute appen-
dicitis. It implies that when a steady pressure is applied in A retrospective database analysis of the treatment out-
the right iliac fossa by the ultrasound transducer, the come of 1073 patients treated surgically for acute
normal or gas-filled intestinal loops will be moved away appendicitis between January 2005 and December 2014
from the field of vision or become compressed between in a public health referral general hospital of 200 bed
the anterior and posterior abdominal walls. On the other capacity serving a population of 2.4 millions was done.
hand, the inflamed appendix, which is incompressible, The study inclusion criteria included adult patients
will be clearly visualized as a blind-ended tubular struc- (12 year old and above as per national health policy),
ture that has a laminated wall which arises from the base diagnosed clinically in the emergency department as
of the caecum, incompressible, a peristaltic, and having a acute appendicitis, had graded compression ultrasound
diameter of more than 6 mm with possible appearance of done in the emergency department and operated as a case
faecolith as a bright echogenic focus having a distal of urgency within 6 h of admission. The exclusion crite-
acoustic shadow, and an increased periappendiceal fat ria included all patients admitted for observation and
echogenicity. The tenderness elicited by the ultrasound treated conservatively, all cases diagnosed by the ultra-
probe can lead the patient to localize the most tender sound as a perforated appendix, appendicular mass, and
point and the site of the inflamed appendix. Puylaert gynecological cases (pregnancy, ovarian cyst, and ectopic
reported a sensitivity of 89% and specificity of 100% [7, pregnancy). The collected data included age, sex, pre-
8]. senting symptoms, physical examination findings, fever,
In 1996, Lim and Quillin outlined the usefulness of leukocytosis, graded compression ultrasound findings,
color Doppler in detecting the inflamed appendix, in intraoperative findings, histopathological findings, and
which the inflamed thick walled, incompressible appen- positive or negative appendectomy. Data were recorded
dix that is fixed in position by the compressing trans- on a database-computerized file for analysis.
ducer will show circumferential color in contrast to the The ultrasound method used was unified to all radi-
healthy gut which appears thin walled and compliant ologists by a clinical pathway protocol guidelines. All the
with frequent peristalsis transmitting no or minimum patients had the same ultrasound examination performed
signals [9]. The graded compression ultrasound technique by the two sonographic radiologists involved in our
could decrease the rate of the healthily removed appen- study (authors 4 and 5) using a Philips HD11 XE
dices, particularly in ovulating females where about 40% Ultrasound System. The protocol consisted of using a
of appendectomy specimens show no pathologic proof of high-frequency linear and curvilinear probes transducers,
inflammation [10–12]. variable or short focal zone, and a frequency of 3–
Khairy [13] reported negative appendectomy of 9.2% 9 MHz. The horizontal scan technique of the abdomen
in 852 patients and concluded that despite the advances started at the lower edge of the liver and going down to
in the diagnostic and imaging techniques, the rates of the the right iliac fossa, identification of the ascending colon,
findings of negative appendectomy have not decreased proceeding down until reaching the tip of the caecum
much. In another study, Al Thoubaity [14] reported that where the patients were instructed to localize the point of
the prevalence of advanced appendicitis was about maximum tenderness. A slow uniform compression was
13.7%, and the negative appendectomy rate was about conducted to squeeze the bowel loops. The appendix
27.2%. The accuracy rate of appendicitis with Alvarado looked as a blind-ended, a peristaltic, tubular structure,
scale was 67.7%, with the ultrasound was 57.9%, and arising from the tip of the caecum. It was carefully
with computed tomography (CT) scan was 66.7%. A examined and scanned through all access and
randomized study by Wade [15] stated that the overall length, measuring the anteroposterior dimension of the
B. H. Shirah et al.: Graded compression ultrasound in acute appendicitis

appendix. A color Doppler ultrasound was also per- was calculated as the percentage of operated cases with a
formed to all the patients to detect the blood flow signal normal appendix by histopathology. The statistical
using an L12–3 Broadband Linear-Array Transducer, analysis was performed using the Statistical Package for
12–3 MHz extended frequency range, 35 mm effective Social Science (SPSS) software program (Release 22).
aperture length, 10° of trapezoidal imaging, and steerable
pulsed wave.
The ultrasound findings were recorded in a database-
Results
structured file and saved on an external hard drive for 1073 Saudi Arabian patients treated surgically for acute
analysis, classified as positive or negative for acute appendicitis between January 2005 and December 2014
appendicitis. The features of a positive test included a were included. 647 (60.3%) patients were males, and 426
proven visualization of an incompressible tubular, blind- (39.7%) patients were females. The male-to-female ratio
ended, a peristaltic structure, with a diameter of 6 mm or in our study was 1.32:1. The mean age was 26.5 years in
more in the right iliac fossa. The presence of appendic- the range of 13–37. Right lower abdominal pain and
ular faecolith, probe tenderness, increased echogenicity right iliac fossa tenderness in all patients (100%), fever in
of the periappendiceal fat, free intraperitoneal fluid 821 (76.5%), and leukocytosis in 937 (87.3%) were re-
particularly in the right iliac fossa or pelvis, and cir- corded (Fig. 3).
cumferential color on Doppler ultrasound were addi- Positive ultrasound findings were recorded in 892
tional criteria of positivity. The features of a negative test (83.13%), while negative results were reported in 181
included no visualization of the appendix, visualization (16.87%). Positive appendectomy has been recorded in
of a normal appendix, and the presence of alternative 983 (91.6%), while negative appendectomy has been
diagnosis (Figs. 1, 2). documented in 90 (8.4%) (Fig. 4).
The operative findings were recorded in a database- The true positive was defined as patients with a
structured file and saved on an external hard drive for positive disease and positive ultrasound results (892
analysis, classified as positive and negative. Positive patients). The true negative was defined as patients
appendectomy was defined as an appendix showing acute with a negative disease and negative ultrasound results
inflammatory changes intraoperatively and on (90 patients). The false negative was defined as patients
histopathology. Negative appendectomy was defined as with a positive disease and negative ultrasound results
the absence of acute inflammation on histopathology. (91 patients). The false positive was defined as indi-
The collected data were subjected to statistical analysis to viduals with a negative disease and positive ultrasound
determine the accuracy of graded compression ultra- results (0 patient) (Table 1).
sound technique calculating the sensitivity, the speci- The sensitivity was 83%, and the specificity was 100%.
ficity, the false negative and positive values, and the The false negative rate was 93%, and the false positive
predictive values. The rate of negative appendectomy rate was 0. The positive predictive value was 90%, and

Fig. 1. Features of acute appendicitis in graded compression ultrasound.


B. H. Shirah et al.: Graded compression ultrasound in acute appendicitis

Fig. 2. Features of acute


appendicitis in color
Doppler.

Presenng symptoms, signs, fever, and leukocytosis Paents %


1200
100
1000
90
80
800 70
60
Paents

600
%

50
40
400
30
200
20
10
0 0
Right lower Right iliac
abdominal fossa Rebound Posive Negave Posive Negave
Nausea Voming Fever tenderness leukocytosis
pain tenderness ultrasound ultrasound appendicectomy appendicectomy
Paents No. 1073 849 472 821 1073 904 937 Paents % 83.13 16.87 91.6 8.4

Fig. 3. Presenting symptoms, signs, fever, and leucocytosis. Fig. 4. Positive and negative ultrasound and appendicitis.

interval before the study period (i.e., from January 1995


the negative predictive value was 49%. The rate of neg- to December 2004). In our study, the rate of negative
ative appendectomy was 8.39%. The prevalence of acute appendectomy was 8.39% compared to 16.4% in the
appendicitis among the study population was 91.6% previous 10 years. Positive ultrasound findings were re-
(Table 2). corded in our study in 83.13% compared to 62.8% in the
The graded compression technique was adopted in last 10 years (Fig. 5).
our hospital by a quality care protocol and clinical
pathway starting from January 2005. Since then, it has Discussion
been the standard method. As a result, we compared the
result of our study with the result documented in the data In our study, the specificity is significantly high being
system of our quality care program for the 10 years 100%. It is reflected in low false positive rate and
B. H. Shirah et al.: Graded compression ultrasound in acute appendicitis

Table 1. True and negative values


Value Acute appendicitis+ (D+) Acute appendicitis- (D-) Total

USG diagnosis+ (T+) 892 (TP) 0 (FP) 892 (all test positive)
USG diagnosis- (T-) 91 (FN) 90 (TN) 181 (all test negative)
Total 983 (all diseased) 90 (all disease free) 1073 (grand total)

USG ultrasonography, T+ positive test, T- negative test, D+ positive diagnosis, D- negative diagnosis, TP true positive, FP false positive, FN false
negative, TN true negative

Table 2. Sensitivity, specificity, and statistical analysis results difficult to scan adequately with a poorly penetrating,
Sensitivity 83% linear array, small-parts transducer. We believe that the
Specificity 100% crucial factor is a transducer with a variable or short
False negative rate 9.3%
False positive rate 0%
focal zone and with a frequency between 5 and 9 MHz.
Positive predictive value 90% The mean age of our study population was 26.5 years
Negative predictive value 49% in the range of 13–37, which is the average age distri-
Rate of negative appendectomy 8.39%
bution for appendicitis in our local community. In fact,
we only encountered two cases of appendicitis in patients
above 40 years of age in the last 20 years.
90 The most widely studied diagnostic modalities are CT
80 scan, ultrasonography, and laparoscopy [8–10]. In our
70 study, we have selected the graded compression ultra-
60 sound, because it is the standard diagnostic modality in
50 our emergency department and thus, it is available all the
40 time, and all our radiologists are well trained in per-
30 forming the technique, as it is simple and non-invasive.
January 2005 to
December 2014 20 Usefulness of graded compression ultrasound in the
January 1995 to 10 diagnosis of acute appendicitis is now established. When
December 2004 0 Puylaert first introduced his graded compression method,
he reported a sensitivity of 89% and specificity of 100%
Negave Posive
appendectomy ultrasound [8]. Many other studies, later on, reproduced the same
rate findings findings [9, 10, 12, 15]. The graded compression ultra-
sound technique is an inexpensive, fast and noninvasive
Fig. 5. Comparison between our study results and data from method with an accuracy rate of 71–90% for the diag-
the previous 10 years. nosis of acute appendicitis (sensitivity 75–90% and
specificity 86–100%) with positive and negative predic-
consequently low negative appendectomy rate. Predictive tive values of 91–94 and 89–97%, respectively. However,
values, both positive (90%) and negative (49%) were on there is no certainty regarding the effect of ultrasonog-
the high side, an observation which reflects the usefulness raphy on the clinical outcomes of patients. Also, the
of graded compression ultrasound based on statistical clinical judgment should not be abandoned because of
analysis. The improved performance parameters were the lack of ultrasound findings in patients with a high
translated into better clinical outcome as negative probability of acute appendicitis [16].
appendectomy rate was low (8.39%). Exclusion criteria Incorporation of graded compression ultrasound led
for a perforated appendix and other conditions may have to a decrease in the negative appendectomy rate, which is
had contributed to the result of very high specificity, in accordance with many other reports where preopera-
taking into consideration that all the cases of right lower tive ultrasound improved the clinical outcome [17].
quadrant abdominal pain (suspected appendicitis) are Many authors had reported increased diagnostic accu-
scheduled for ultrasound examination as a standard racy when ultrasound was added to the clinical workup
policy in our hospital. of these patients. Puig et al. [18] in 2003 have reported
In our protocol, we used both the high-frequency 36.6% negative appendectomy rate without ultrasound
linear probes and curvilinear probes. We have found that and 13.2% after an ultrasound.
curvilinear probes give equal results to the linear probes Ultrasound has been reported more helpful in clini-
in many patients but provide a slightly larger field of cally equivocal cases because of false positive and false
view and greater penetration, which was of considerable negative results. It has been observed that the policy of
benefit in some of the obese patient with whom it was selective usage of diagnostic adjuncts only in equivocal
B. H. Shirah et al.: Graded compression ultrasound in acute appendicitis

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