Full Article - Medical Ultrasonography Journal

Original papers
Medical Ultrasonography
2009, Vol. 11, no. 3, 7–18
Ultrasonographic diagnosis of acute appendicitis
Călin Moş1, Teodor Ile2, Monica Hălbac2, Laura Chiş2, Sorin Vesa2, Ştefan Andor2
1
2
University of Oradea, Faculty of Medicine and Pharmacy, Romania
County Hospital, Beiuş, Romania
Abstract
Introduction. Appendectomy, the most frequent surgical intervention, has 20-30% rate of negative appendectomy mostly
because of 30-45% cases with unspecific clinical examination. The objective of this study was to determine the contribution of
ultrasonography in acute appendicitis (AA) diagnosis in patients with abdominal pain in the right lower quadrant.
Material and method. A number of 262 patients with clinical suspicion of AA were investigated. The positive diagnosis
criteria were considered to be the appendix external diameter >6 mm, appendix wall thickness >3 mm, partial or total absence of
wall stratification, coprolites or/and liquid in excess in the appendix lumen, hypervascularization of appendix wall, echogenicity enhanced and hyperemia in periappendicular mesenteric fat, periappendicular collection (abscess) or peritoneal collection
(peritonitis).
Results. Appendix was identified by ultrasonography in 199 out of 262 of patients (75.9%). Normal appendix was less visualized (in 61.9%) comparing to pathologic appendix (91.3%). Ultrasonography demonstrated an 89.4% sensibility, 95.2% specificity, positive predictable value 95.5% and negative predictable value 88.9% in the detection of AA. Preoperative ultrasonographic
examination in patients with abdominal pain of the right lower quadrant leads to 9.9% negative rate of appendectomies.
Conclusions. In cases of abdominal pain located in the right lower quadrant, ultrasonography is a quick non-invasive and low
cost method which can contribute to an early positive diagnosis and also a decrease in the number of unnecessary appendectomies.
Key-words: acute appendicitis, ultrasound, diagnosis
Rezumat
Introducere. Apendicectomia, cea mai frecventă intervenţie chirurgicală, are o rată de 20-30% de apendicectomii negative,
in primul rind deoarece in aproximativ 30-45% cazuri examenul clinic este nespecific. Scopul studiului este de a determina
contribuţia ecografiei în diagnosticul apendicitei acute la cazurile cu sindrom dureros de fosă iliacă dreaptă.
Material şi metodă. S-au evaluat ecografic 262 de pacienţi cu suspiciunea clinică de apendicită acută. Criteriile ecografice
de diagnostic pozitiv au fost: diametrul extern al apendicelui peste 6 mm, grosimea a peretelui peste 3 mm, dispariţia parcelară
sau totală a stratificării pereţilor, prezenţa în lumen a coproliţilor şi/sau a lichidului în exces, hipervascularizaţia peretelui apendicular, creşterea ecogenităţii şi hiperemia grăsimii mezenterice periapendiculare, prezenţa unei colecţii periapendiculare (abces)
sau peritoneale (peritonită).
Rezultate. Apendicele a fost identificat ecografic la 199 dintre cei 262 de pacienţi (75,9%). Apendicele normal a fost mai rar
vizualizat (61,9%) comparativ cu cel patologic (91,3%). Ecografia are sensibilitate de 89,4%, specificitate de 95,2%, acurateţe de
94,3%, valoare predictivă pozitivă de 95,5% şi valoare predictivă negativă de 88,9% în detectarea apendicitei acute. Examinarea
ecografică preoperatorie a pacienţilor cu suspiciunea clinică de apendicită acută a dus la o rata de apendicectomii negative de
doar 9,9%.
Concluzii. În cazul unei simptomatologii dureroase de fosă iliacă dreaptă, ecografia este o metodă neinvazivă, rapidă şi cu
preţ de cost scăzut care poate să contribuie la un diagnostic pozitiv precoce, la diminuarea ratei de apendicectomii cu apendice
normal şi la clarificarea diagnosticului diferenţial.
Cuvinte cheie: apendicită acută, ecografie, diagnostic
Address for correspondence: Dr. Călin Moş
Str. Andrei Şaguna nr.1
415200, Beiuş,
jud. Bihor, România
e-mail: drcalinmos@yahoo.com
Acute appendicitis (AA) is the most common acute
surgical condition [1], about 7% of the population having
an appendectomy during their lifetime [2]. Maximum incidence is between 6 and 30 years [3,4]. In about 30-45%
of cases the clinical evaluation is unspecific [5].
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Călin Moş et al
The appendix is a worm-shaped pouch originating
from the lowest part of cecum. It usually has an intraperitoneal position (anterior or retrocecal) in contact with the
anterior parietal peritoneum. A wide mesentary permits
the appendix rotation in several positions. So in 30% of
cases the appendix is placed in the pelvis, retrocecal or
retroperitoneal. These positions can modify clinical signs
and symptoms of AA [6].
AA are caused by obstruction of the appendix lumen
through several causes: lymph hyperplasia (especially in
children and young adults in viral infections, mononucleosis, gastroenteritis or ileocolitis), coprolites, parasites,
foreign body, Crohn’s disease or neoplasm [5,7,8,9].
If the diagnosis of AA is based only on clinical and
laboratory findings, about 20-30% of appendectomies
are not confirmed at pathologic examination [9,10,11].
In AA an early diagnosis is crucial to reduce the risk of
complications (perforation, occlusion, sepsis) which can
increase the mortality especially at extreme ages [1].
In a small number of patients with AA (between 1-10%)
the appendix inflammation is discrete, clinical signs are
blurred and rapidly subsided, and the clinical evolution
is rapidly to spontaneous remission. These are called
abortive appendicitis, limited appendicitis or spontaneous healing appendicitis [12,13]. In atypical cases of AA,
the surgeon have to choose between instant and delayed
surgery. The ultrasonography (US) of abdomen and appendix region can help the surgeon to take the proper
decision.
The advantages of US in AA diagnosis are the low
cost, the lack of irradiation, and the possibility to examine carefully and repetitively the maximum sensibility
zone. The main disadvantage of the US is the operatordependence and the difficulty in scanning obese patients.
[14,15,16]. An experienced operator, with the aid of a
modern devices (with high resolution probe), could have
a sensitivity, accuracy and specificity around 90% in US
diagnostic of AA. Also, in the patients with appendicitislike symptoms, US can reveal the correct diagnosis in
almost 70-80% of cases [17].
The aim of our study was to evaluate the contribution
of the US for the positive and differential diagnosis of the
AA, in patients with abdominal pain localized in the right
lower quadrant.
Material and method
The study comprised 262 patients (136 males, 126
females, aged between 4–73) presenting with right lower
quadrant abdominal pain at the Beius County Hospital
between December 2007 and July 2009. They all had
clinical suspicion of AA. US was performed by a doc-
Ultrasonographic diagnosis of acute appendicitis
tor (CM) with experience in gastrointestinal tract US.
A Voluson 730 PRO General Electric Kretz Technik ultrasound machine with multifrequence probe (1.5-18.5
MHz) was used.
The examination protocol, based on graded compression describe by Puylaert [18] included:
1. Convex probe use. The US examination started
with an abdominal general scanning (to exclude an extraappendicular pathology) using a 1.5-4.5 MHz or 4.08.5 MHz convex probe, depending on body weight. For
obese patients the same convex probe was used for appendix region examination.
2. Linear probe use. For the examination of the appendix region we used a 5-18.5 MHz linear probe. According to the Puylaert technique [18,19] a graded compression was exerted with the transducer, to dislocate the
air and to identify the most painful region. The landmarks
of the region (cecum, last portion of the ileum, iliopsoas
muscle, iliac vessels and appendix) were identified. The
examination began with sections from the ascending colon to the cecum. After the identification of the cecum
base, longitudinal sections from the lateral to the median
part of the cecum were made. Usually the appendix was
identified in the maximum painful zone. If the appendix
was not identified in its normal position, the examination
continued to explore the retrocecal, retrocolic, pelvic and
retroileal regions using the appendix base as a landmark
(always the base was situated in the same position).
We used US in gray scale for morphological analysis
and Doppler US for the examination of appendix vascularization (with a small velocity scale and 70-120 Hz
parietal filter).
US exclusion criteria for AA were an US unidentifiable appendix or a compressible appendix, oval shape in
transverse section, with external diameter under 6 mm,
wall thickness under 3 mm, wall layers and normal periappendicular mesenteric fat. US positive diagnosis criteria for AA were considered the external diameter of the
appendix over 6 mm, the appendix wall thickness over 3
mm, total or partial wall layers nonvisualisation, coprolites and/or fluid excess into appendix lumen, hypervascularization of the appendix wall, enhance of echogenicity and hyperemia of the periappendicular mesenteric fat,
periappendicular collection (abscess) or peritoneal collection (peritonitis).
The histopathological examination of the appendix
was performed in all surgical cases.
The result was considered true positive when the US
diagnosis concurred with the histopathological findings
and true negative when the histopathology for AA was
negative or there was no relapse in 2 weeks of follow up
of the nonsurgical patients.
Medical Ultrasonography 2009; 11(3): 7–18
The result was considered false positive when there
was a US diagnosis of AA with normal histopathological findings in the appendix, and false negative when US
found a normal or unidentifiable appendix with positive
histopathology for AA.
A 2x2 table and χ2 test were used for the evaluation of
the results. The sensitivity, specificity, accuracy, positive
and negative predictive values were determinate (PPV,
NPV). The confidence interval was 95%.
Results
In the majority of the cases the appendix was identi-
fied in about 1-3 minutes. An unidentified US appendix
was considered a normal appendix. From 262 examined
patients, 141 were submitted to appendicectomy. In 127
patients there was a histological confirmation of AA. In
14 patients the histological examination was negative
resulting 9.9% appendicectomies for a normal appendix
(tab I, tab II).
The clinical situations which led to false positive and
false negative results are presented in table III.
The statistical data analysis shows 89% sensibility, 95.2% specificity, 94.3% accuracy, 95.5% PPV and
88.9% NPV of the US in diagnosis of AA.
Table I. US identification of the appendix and the therapy of the patients with pain in the right lower quadrant (RLQ);
AA – acute appendicitis
US findings
Number of patients with pain Patients with appendectomy Patients with conservative therapy US diagnosis of AA
RLQ (total 262)
(total 141)
(total 120)
(total 118)
Identified
appendix
199
(75,9%)
120
(89,4%)
79
(65,8%)
103
(87,3%)
Unidentified
appendix
63
(24.1%)
21
(10,6%)
41
(34,2%)
15
(12,7%)
Table II. US diagnosis and the therapy of the patients with pain in the right lower quadrant (RLQ); AA- acute appendicitis
US diagnosis
Number of patients with pain Patients with appendectomy Patients with conservative therapy US diagnosis of AA
in RLQ (total 262)
(total 141)
(total 120)
(total 118)
AA
127
(48,5%)
127
(90,1%)
0
(0%)
112
(94,9%)
Without AA
135
(51,5%)
14
(9,9%)
120
(100%)
6
(5,1%)
Table III. The causes of false positive or false negative results at US
Outcome type
False
positive
The cause of false outcome
Number of cases
• hydrosalpings
• mucocele with pseudomyxoma peritonei in small quantity
• terminal ileum segmental necrosis
• Meckel’s diverticulitis
• cecal diverticulitis
• ovarian torsion
Total
False
negative
Appendix lack of identification without real associated pathology
• obesity
• appendix point position
• difficulties in practicing graded compression
• pain absence at compression in right lower quadrant
Appendix lack of identification with associated pathology
• cecum neoplasm
• infectious ileitis
• hyperplastic cholecystosis with subhepatic abscess produced by appendix perforation
• perforated appendix for an appendix and cecum located in left lower quadrant
Total
1
1
1
1
1
1
6
5
2
3
1
1
1
1
1
15
3
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Călin Moş et al
Discussions
Ultrasonographic diagnosis of acute appendicitis
The detection by US of the normal appendix vary in
published papers between 0% and 95% [18,20,21,22,23,
24,25,26], depending mostly on the US machines’ performances. For example, Puylaert in 1986 (in a study describing the graded compression technique for appendix
examination) mentions the lack of normal appendix visualization [18]. In a recent paper in 2005 [26] the detection
rate of the normal appendix increased to 82%.
The main examination technique is one of the graded
compression [18]. Some authors consider that anterior
graded compression combined with posterior compression can increase significantly the rate of appendix detection [24]. The appendix examination must be performed
in its entire length because there are situations with focal
inflammation, especially on the tip of appendix. The incomplete examination of the appendix can generate false
results [27].
On longitudinal scan, the normal appendix is a compressible tubular blind-ending structure, without peristaltic movements, no mucosal stripes and usually without
visible hypervascularization. External maximum diameter is considered to be 4.7±1.2 mm [28] but in exceptional cases can increase up to 8-11 mm [28]. Most of the
authors considered a diameter of 6 mm as the superior
value for a normal appendix (fig 1, fig 2) [29,30].
Normal appendix lumen can occasionally be filled
with noninflammatory content (faecals, mucus) achieving an uncompressible appendix and an external diameter
over 6 mm (up to 10-11 mm) [30,31,32]. For this reason
there are authors who consider that the parietal thickness
(the distance from the hyperechoic serosa to the hyperechoic lumen, normal<3 mm) is a more specific criteria
for appendix evaluation [33, 34]. A normal appendix contains intraluminal gas (linear or punctiform image with
reverberation shadow) in 75-85% of cases (fig.3, fig 4)
[35, 36].
Fig 1. Normal appendix, longitudinal scan (tubular blind-ending structure with laminal layer structure).
Fig 3. Normal appendix with non-inflammatory content (faecal,
mucus, gas), longitudinal scan.
Fig 2. Normal appendix, transverse scan (ovoid laminal layer
structure).
Fig 4. Normal appendix, transverse scan (intraluminal gas is a
punctiform image with reverberations shadow).
Medical Ultrasonography 2009; 11(3): 7–18
The appendix compression is considered to be adequate when in the transverse section the appendix become oval and the anteroposterior diameter of the contiguous ileum has no more than 4 mm [19]. An incomplete
oval appendix is a normal appendix in 86% of cases and
a complete oval appendix excludes AA [37].
The normal appendix wall has a laminar layer structure with echoic submucosal and serosa layers and hypoechoic mucosa and muscular layers [38,39]. Periappendicular mesenteric fat is an echogenic structure in which
some spots of vascularization can be detected. Normal
small bowel loops are visualized as tubular structures
with mucosal folds, thin walls (<2 mm) and peristaltic
movements. The colon is a large tubular structure with
haustra, thick walls (2-5 mm), mixed content and with
occasionally peristaltic movements [40,25].
Deutch et al. [41] described in 1981 an inflamed appendix for the first time. US identification of inflamed
appendix is high (80-99%) [42,43]. The phlegmonous
and gangrenous appendicitis are always identified while
catarrhal appendicitis have a smaller rate of identification
[44].
Dimensions, structure, localisation and absence of
peristaltic movements contribute to differentiate an inflamed appendix from the small intestine or cecum. An
inflamed appendix is characterized by the absence of
peristaltic movement, diameter over 6 mm, tubular finger
tip shape in longitudinal section and target appearance in
cross section (fig 5, fig 6) [40,45,46].
Himeno et al. [42] and Takada et al. [44] had established the US criteria for the three histopathological
forms of AA: 1) catarrhal appendicitis: normal appendix
wall structure with mucosa oedema; 2) phlegmonous appendicitis: a less clear structure of appendix wall layers
with transverse diameter over 10 mm; 3) gangrenous appendicitis: the absence of parietal layers and marked appendix thickening. These criteria were in accordance with
the histopathological findings in 61.2% of cases [44]. In
our opinion these criteria are restrictive. We examined
numerous cases with an appendix having a calibre <1 cm
and a phlegmonous or gangrenous histopathological aspect. That is why in our study we took also the vascularization criteria into account.
The pathologic appendix wall is a hypoechoic structure, >3 mm thickness (fig 7).
Fig 5. Inflamed appendix, longitudinal scan (tubular finger tip
structure with diameter >6 mm).
Fig 7. AA at the onset (continuous central echoic line).
Fig 6. Inflamed appendix, transverse scan (round target appearance). Note the hyperechoic periappendicular fat surrounding
the appendix.
First, at the onset of an AA, the continuous hyperechoic line of the submucosa becomes discontinued [29,
40]. Than, as a consequence of the necrosis, dishomogenicity and hypoecogenicity of the submucosa appear (fig
8, fig 9) [47].
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Călin Moş et al
Fig 8. AA with fluid, appendicolite with posterior acoustic
shadow and echogenic submucosa absence at the tip of the appendix due to necrosis.
Ultrasonographic diagnosis of acute appendicitis
In the advanced stage (gangrenous stage) the stratification of the appendix wall completely disappears (fig
10) [44].
In the appendix the content could be anechoic (fluid)
or echoic (air, appendicolite). The air is less frequently
observed (15%) than in the normal appendix [35]. Appendicolite (an intraluminal hyperechoic image with or
without acoustic shadow), represents a mixture of inorganic salts and undissolved stools. The presence of an
appendicolite makes the appendicectomy imperious even
when the appendix diameter is normal [48, 49, 50] .Real
appendicular stones are less common but are often associated with perforation [49]. The inflammation of the
periappendicular fat produces an enhancement of its
echogenicity [51]. So, an inflamed and hypoechoic appendix is surrounded with hyperechoic fat.
Fig 9. AA with fluid, appendicolite (arrow) and echogenic submucosa disappearance as a consequence of the necrosis.
Fig 11. Small perforation of the appendix (arrows) – loss of the
submucosal echogenicity near the perforation.
Fig 10. AA with fluid in the lumen and gas in the anterior wall
(arrow). The stratification of the appendix wall is completely
disappeared (gangrenous appendicitis).
Fig 12. Periappendicular collection. Note that the thick echogenic fat and the cecum delimitate the collection.
Medical Ultrasonography 2009; 11(3): 7–18
Fig 13. A diffuse collection in the right iliac fossa (periappendicular phlegmon).
Appendix perforation is suggested by the presence of
a periappendicular collection (periappendicular abscess),
submucosal discontinuity zones, asymmetric appendix
walls thickening with possible intramural air, periappendicular fat thickening >10 mm (fig 11, fig 12, fig 13).
Sometimes, there is no significant pain during examination (due to decreased pressure following appendix
rupture) [47, 52]. The most specific feature is the presence of the pericecal abscess, with impure fluid content
and small echoes inside and mass effect on the nearby
intestinal ansae [52]. In small perforations, an emergency
appendicectomy is necessary. In cases with periappendicular phlegmons, an initial conservative therapy followed
by postponed appendicectomy is preferred. For well defined abscesses a US guided drainage can be performed
before appendicectomy [52, 53, 54, 55, 56, 57].
In abortive appendicitis (7-10% of cases) the appendix usually does not contains coprolites, no periappendicular abscess or inflammatory signs are detected,
and the average the appendix diameter is 8.5 mm [12,
13]. Recurrence rate after an abortive appendicitis is 38%
after 3 months and 70% after 1 year. The recurrence is
significantly enhanced if the appendix diameter is >8 mm
under compression [13].
The position of the appendix can influence its detection. A retrocecal appendix is better visualized from
coronal sections (with the probe direction from lateral to
medial). A pelvic appendix can be detecting by using an
endovaginal probe. An unidentified appendix is suggestive but not revealing for a normal appendix
In the differential diagnosis of AA, miscellaneous
abdominal and extrabdominal pathology should be taken
into account (tab IV).
In the last years, new techniques for the improvement
of the US images have been used. In a recent study [58]
the use of Spatial Compounding Imaging (cross beam)
and Tissue Harmonic Imaging increased the rate of detection of the appendix by 19%.
The examiner’s experience in appendix US is very
important. During this study the improvement in examiner’s abilities, especially for normal appendix identification, were recorded.
The normal appendicular vessels are of small calibres with slow blood velocities. The normal appendix
does not usually present distinguishable vascularization
at Doppler US. In AA the vascular diameters and blood
velocities are increased, being easy to detect in Doppler
US (fig 14, fig 15, fig 16) [59, 60]
Table IV. Differential diagnosis of the acute appendicitis
Differential diagnosis
Obstetrical and gynaecologic diseases
Pelvic inflammatory disease, ovarian cyst rupture, tubular pregnancy, tubular pathology,
endometriosis
Gastrointestinal diseases
Ulcer, diverticulitis, Chron’s disease, infectious enteritis, ileocecitis, ileitis, tuberculosis,
intestinal occlusion, intestinal infarction, invagination, volvulus, tumors,
acute pancreatitis, mesenteric adenitis, mesenteric infarction
Urinary diseases
Renal colic, renal abscess, pyelonephritis, prostatitis testicular torsion
Liver and gallbladder diseases
Hepatic abscess, acute cholecystitis
Muscle diseases
Iliopsoas muscle abscess or haematoma, rectus abdominis muscle sheath haematoma
Epiploon diseases
Infarction, torsion, appendagitis
Pulmonary diseases
Pneumonia, pulmonary infarction
Parasitic infections
Ascaridiosis
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Călin Moş et al
Fig 14. AA: hypervascularization on color Doppler.
Ultrasonographic diagnosis of acute appendicitis
Fig 17. AA vascularization: arterial and venous signal (triplex
mode).
In evolution, the vascular signal could become difficult to detect (or only the arterial signal is detected) due
to parietal necrosis. The extension of the parietal necrosis
in the gangrenous AA leads to the absence of appendix
vascularization with periappendicular fat hyperemia (fig
18) [59, 64, 65].
Fig 15. AA: hypervascularization on power Doppler.
Fig 18. AA with discrete appendicular vascularization due of
parietal necrosis and periappendicular hyperemia.
Fig 16. AA with high appendicular and periappendicular hypervascularization.
Some authors consider that inflammatory activity
is proportional to the quantity of color signal found in
the appendix wall [61,62]. The hypervascularization is
present from the onset of AA. Both arterial and venous
vascular signals could be detected. (fig17) [63].
In abortive appendicitis, at the onset a parietal hypervascularization can be recorded (fig 19), hypervascularization reversible in evolution [59, 62]. The appendix
could be hypervascularizated also in ileocecal inflammatory diseases [66] or if the appendix orifice is obstructed by a cecal tumour [67]. A recent study suggests that
Power Doppler in combination with contrast agents is
the most sensitive method for AA diagnosis (sensitivity
100%) [68].
The role of the 3D/4D US for appendix evaluation
has not been evaluated yet. This study does not concern
Medical Ultrasonography 2009; 11(3): 7–18
Fig 19. Abortive appendicitis with parietal hypervascularization. After 24 hours the patient had a quickly spontaneous favourable course and appendectomy was not necessary.
itself with this evaluation but we do confirm that in some
cases the 3D reconstruction did improve the US description of the lesions (fig 20, fig 21, fig 22, fig 23 fig 24).
Fig 20. Appendicular and perriappendicular findings in AA
evaluated in 3 orthogonal projections
Fig 21. Small periappendicular collection due to appendix perforation. The site of perforation and the extension of collection
are better visible on C plane.
Fig 22. Periappendicular abscess view with tomographic ultrasound imaging technique – serial tomographic sections
Fig 23. Tridimensional reconstruction of a periappendicular
abscess
Fig 24. Tridimensional reconstruction of the vascularization of
inflamed appendix
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Călin Moş et al
Our statistical analysis results are in concordance
with those from the literature. The majority of studies
showed a sensibility between 64-96%, specificity between 88-99%, accuracy between 82-97%, PPV between
79-99% and NPV between 75-97% of the US in AA diagnosis [18, 25, 40, 60, 69, 70, 71, 72]. Our study confirms
that nowadays, with modern devices and an experienced
operator, it is possible to achieve the most accurate results.
The sensibility of the method was lower than the specificity because of the uncontrolled factors responsible
for the majority of the false negative results (obesity,
unspecific localization of appendix and associated diseases).
It must be mentioned that the US in our study was
performed only after clinical examination and laboratory
tests. The use of the US as a diagnostic method, together
with clinical examination and laboratory tests decreased
significantly the rate of unnecessary appendicectomies
from 20-30% [9, 10, 11, 70] to 9.9%.
Conclusion
Ultrasonography is a sensitive and specific method for
AA diagnosis. In patients with right lower quadrant abdominal pain the US can identify the source of the painappendicular or non-appendicular. US has an important
role in the AA management and also implications in the
therapeutic decision. US examination could considerably
decrease the number of unnecessary appendicectomies.
Acknowledgments
Special thanks to Mr. Sebastien Eckert, chairman of
Medisys Societe, Paris, France for his priceless help.
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