Pediatr Radiol DOI 10.1007/s00247-014-2873-8
ORIGINAL ARTICLE
Perforated appendicitis: an underappreciated mimic of intussusception on ultrasound Beverley Newman & Matthew Schmitz & Rakhee Gawande & Shreyas Vasanawala & Richard Barth
Received: 17 October 2013 / Accepted: 6 January 2014 # Springer-Verlag Berlin Heidelberg 2014
Abstract Background We encountered multiple cases in which the US appearance of ruptured appendicitis mimicked intussusception, resulting in diagnostic and therapeutic delay and multiple additional imaging studies. Objective To explore the clinical and imaging discriminatory features between the conditions. Materials and methods Initial US images in six children (age 16 months to 8 years; 4 boys, 2 girls) were reviewed independently and by consensus by three pediatric radiologists. These findings were compared and correlated with the original reports and subsequent US, fluoroscopic, and CT images and reports. Results All initial US studies demonstrated a multiple-ringlike appearance (target sign, most apparent on transverse views) with diagnostic consensus supportive of intussusception. In three cases, US findings were somewhat discrepant with clinical concerns. Subsequently, four of the six children had contrast enemas; two were thought to have partial or complete intussusception reduction. Three had a repeat US examination, with recognition of the correct diagnosis. None of the US examinations demonstrated definite intralesional lymph nodes or mesenteric fat, but central echogenicity caused by debris/appendicolith was misinterpreted as fat. All showed perilesional hyperechogenicity that, in retrospect, represented inflamed fat “walling off” of the perforated appendix. There were four CTs, all of which demonstrated a double-ring appearance that correlated with the US target appearance, with B. Newman (*) : M. Schmitz : R. Gawande : S. Vasanawala : R. Barth Department of Radiology, Stanford University, Lucile Packard Children’s Hospital, 725 Welch Road, MC 5913, Stanford, CA 94305, USA e-mail: [email protected]
inner and outer rings representing the dilated appendix and walled-off appendiceal rupture, respectively. All six children had surgical confirmation of perforated appendicitis. Conclusion Contained perforated appendicitis can produce US findings closely mimicking intussusception. Clinical correlation and careful multiplanar evaluation should allow for sonographic suspicion of perforated appendicitis, which can be confirmed on CT if necessary.
Keywords Children . Appendicitis . Intussusception . Ultrasound . Computed tomography
Introduction Acute appendicitis and ileocolic intussusception are common causes of acute abdominal pain in young children. Timely and accurate diagnosis of these conditions is essential for prompt, appropriate treatment and minimization of patient morbidity. Imaging evaluation of abdominal pain in children often begins with a sonogram of the abdomen and pelvis [1]. The typical sonographic appearances of acute appendicitis and intussusception have been well illustrated [2–4]. Several potential mimics of intussusception on imaging have been described [1, 5, 6]. Little, however, has been written regarding the confusion of the sonographic appearances of ruptured appendicitis and intussusception. We consider ruptured appendicitis to be an important mimic of intussusception, with potential for delayed diagnosis or misdiagnosis. We also suggest that careful examination of specific findings on a sonogram can help in differentiating the conditions in a timely fashion.
Pediatr Radiol
Materials and methods The peer-review missed-case process identified six children over a 7-year period (2006–2013) who presented to the emergency room (ER) with abdominal symptoms including pain and had an initial sonographic diagnosis of intussusception but subsequent diagnosis of ruptured appendicitis. In all cases initial US images were obtained in the emergency room; these included gray-scale, cine and color Doppler images acquired by US technologists trained in adult and pediatric sonography. In two cases, the children were also scanned by a pediatric fellow (n=1) or attending physician (n=1). Most US studies were obtained on a GE Logiq E9 scanner (GE Healthcare, Milwaukee, WI), with one initial and several follow-up US studies on a Siemens Sequoia unit (Siemens Healthcare, Mountainview, CA). Two of the three follow-up studies were obtained in the pediatric sonography unit with dedicated pediatric technologists. All three repeat US studies were scanned by a faculty pediatric radiologist. Three pediatric radiologists (2 faculty, each with over 30 years of experience in pediatric radiology, 1 fellow) independently and with subsequent consensus evaluated the initial US studies in a non-blinded fashion. These evaluations were compared with the formal reports of the initial and follow-up US studies. Reviewers, aware of the final diagnosis of ruptured appendicitis, were asked whether they would have accepted the initial US diagnosis of intussusception and what US findings were most suggestive of the correct diagnosis. The images and reports of subsequent contrast enemas and CT scans were reviewed and correlated with the US images. Demographic data, clinical presentation and management, and surgical findings were obtained from a review of the patients’ charts; IRB permission was obtained for image and chart review.
Results The number of cases scanned in the same hospital ER for appendicitis or intussusception over the exact time period is not known. However a report from the same hospital noted that approximately 1,200 children were evaluated in the ER for suspected appendicitis during a 5-year period between 2003 and 2008 [7]. The six children described in the current report (Table 1) (2006–2013) ranged in age from 16 months to 8 years (mean age 4.4 years); there were 4 boys and 2 girls (Table 1). All six children presented with abdominal pain; four of the six had a history of fever or were febrile in the ER; three of six had an elevated white blood cell count (Table 1). Three children (ages 6–8 years) were older than the typical age for pediatric ileocolic intussusception, and in two cases clinical symptoms of periumbilical- to right-lower-quadrant pain were more typical of appendicitis than intussusception.
Table 1 Ruptured appendicitis mimicking intussusception Demographic data n=6
Age: 16 months–8 years, mean 4.4 years 4 boys, 2 girls
Clinical findings n=6
Abdominal pain—6 Fever—4 Elevated WBC—3 Idiopathic ileocolic intussusception—4 Intussuscepting calcified ileocolic mass—1 Ileoileal intussusception—1 Suggested ruptured appendicitis—3 (additional clinical information and consultation available, all three scanned directly by radiologist, one case after negative enema Normal—1 Pericolic inflammation, loculated free air—1 (suggestive of ruptured appendicitis) Intussusception reduced—2 (partial in 1) All diagnostic of ruptured appendicitis
Initial US diagnosis n=6 Repeat US n=3
Contrast enema interpretation n=4 Contrast-enhanced CT n=4 Surgery n=6
Acute laparoscopic appendectomy—3 Percutaneous abscess drainage—1 Antibiotics and interval appendectomy—2
WBC white blood cell count
The initial US images were obtained in the ER and were preliminarily interpreted by a radiology resident (1) or pediatric radiology fellow (2), with final interpretation (the same day in four and the next day in two cases) by various faculty pediatric radiologists with a wide range of experience. In all six cases sonographic diagnoses of right mid- to lowerquadrant mass consistent with intussusception were suggested. This was thought to be ileocolic and idiopathic in four cases (Figs. 1 and 2) (Table 1). In one child, the lesion was noted to contain a large central shadowing calcification that was interpreted as a probable pathological calcified mass and the lead point of an intussusception (Fig. 3). In a second child, the interpreting pediatric radiologist recommended a CT scan because of the patient’s age (8 years) and clinical symptoms of pain and fever, although the US findings were thought to be consistent with ileocolitis and an ileoileal intussusception. A third child, 23 months old, with an emergency-room US diagnosis of intussusception had repeated US imaging in the ER with real-time scanning by the pediatric radiologist prior to a planned air-reduction enema. Recognition of marked perilesional inflammatory changes and fluid led to a change in the suggested diagnosis and cancellation of the enema. Independent and consensus review of the six initial US examinations produced diagnostic agreement among the three reviewing pediatric radiologists that the initial diagnosis of intussusception was reasonably supported by the imaging appearance. Each case exhibited a right lower abdominal mass with an alternating hypoechoic and echogenic ring-like appearance, suggesting bowel within bowel (Figs. 1, 2 and 3).
Pediatr Radiol Fig. 1 Ruptured appendicitis in a 3-year-old girl who presented with cramping abdominal pain, was afebrile and had normal white blood cell count. a Anteroposterior abdominal radiograph shows multiple dilated bowel loops and a paucity of gas in the right lower quadrant. The properitoneal fat appears normal, and the cecum is not visualized. Clinical and imaging findings are most suggestive of intussusception. b Transverse US image demonstrates a mass in the right lower quadrant with multiple alternating layers suggestive of intussusception. Eccentric internal echogenicity (arrows) was thought to be suggestive of mesenteric fat. In retrospect, moderate perilesional echogenicity (inflammation) can be seen. c, d Axial contrast enhanced CT (c) and coronal reconstruction (d). The CT was obtained after a normal water soluble contrast enema followed by repeat US which showed the mass to be unchanged. The CT (c, d) demonstrated a complex mass in the right lower quadrant with central enhancing appendix (arrows) containing an appendicolith and surrounding fluid and inflammation, consistent with perforated appendicitis
This US appearance was considered too complex to simply represent thickened cecum. Subsequently four of the six children underwent contrast enemas for intussusception reduction. Experienced attending pediatric radiologists performed these studies. One enema in a 3-year-old was interpreted as normal; a repeat US demonstrated a persistent mass; the possibility of perforated appendicitis was considered and a CT scan was recommended (Fig. 1) (Table 1). A water-soluble enema in a 16-month-old child revealed a small bubble of air adjacent to the cecum in the right lower quadrant as well as pericecal inflammatory changes, suggesting ruptured appendicitis. However, in two 6-yearold children, the pediatric radiologists performing the enema examinations were convinced that intussusception had been present; one was thought to have been rapidly reduced (Fig. 2), and in the other case it was thought to have been incompletely reduced with a residual right lower quadrant
mass (Fig. 3). The child who was thought to have had an intussusception reduced on enema had progressive clinical symptoms of right lower quadrant pain and fever. He underwent a repeat US with direct scanning by an attending pediatric radiologist and discussion with the pediatric surgeon. Although the US appearance was similar to that of the prior study, marked echogenicity was recognized around the mass, suggesting inflammation, leading to the conclusion that ruptured appendicitis was probably a more likely diagnosis. This resulted in a confirmatory CT scan and prevented a planned repeat enema for intussusception reduction (Fig. 2). A total of four children had contrast-enhanced CTs demonstrating ruptured appendicitis. All the CT examinations demonstrated a double-ring appearance correlating with the US findings of the target sign, with inner and outer rings representing the dilated appendix and walled-off appendiceal rupture, respectively (Figs. 1, 2 and 3), with variable
Pediatr Radiol Fig. 2 Abdominal pain and perforated appendicitis mimicking ileocolic intussusception in a 6-year-old boy. a, b Transverse (with color Doppler) (a) and longitudinal (b) US images of the right lower quadrant demonstrate a 3.5×3-cm mass with sonolucent and hyperechoic layers thought to represent an intussusception. A central partially shadowing echogenic focus (arrows) was misinterpreted as central fat (fat should not be expected to shadow to this extent). c Fluoroscopic image from a water-soluble enema at which an intussusception was thought to have been rapidly reduced. There are mild right-side pericolic inflammatory changes, but no mass is evident. The appendix is not filled. d, e CT scan with IV contrast the next day, after repeat US suggested possible ruptured appendicitis. Axial (d) and coronal reconstruction (e) images show a central dilated fluid-filled appendix (arrows) with wall enhancement and periappendiceal fluid collection or abscess, suggestive of acute perforated appendicitis. There is residual bowel contrast from the prior enema. An appendicolith can be seen at the base of the appendix (arrow in e) and there is an additional fluid collection in the pelvis
surrounding phlegmon or fluid. Reaching the correct diagnosis of ruptured appendicitis took between 3 h and 24 h in these six children, with a mean of 10.5 h. All six children eventually had surgical confirmation of ruptured appendicitis with no evidence of appendiceal or other intussusception; in three cases laparoscopic appendectomy and drainage were performed acutely. One of these children developed subsequent adhesive small-bowel obstruction
requiring additional surgery. One child underwent percutaneous abscess drainage by interventional radiology, developed a colocutaneous fistula and had a subsequent interval appendectomy and drain removal. Two other children were treated with antibiotics acutely with interval appendectomy (Table 1). Upon further review of the initial US examinations, all six children demonstrated an appearance suggesting multiple concentric rings of bowel (target sign, most apparent on
Pediatr Radiol
Fig. 3 Ruptured appendicitis in a 6-year-old girl. a Initial US, transverse view, shows a mass (4.7×4 cm) consisting of multiple concentric rings with a central echogenic shadowing focus (arrow) that was initially interpreted as an intussusception, with a calcified mass as the likely lead point. b An air enema later the same day demonstrates reflux of air into the small bowel with mass effect on the cecum (arrows) thought to
represent a residual unreduced intussusception with air having escaped into small bowel past the mass. c Axial post-contrast CT the same day demonstrates ruptured appendicitis with a central fluid-filled appendix and appendicolith (arrow) and surrounding fluid and inflammation corresponding to the multiple layers seen on ultrasonography
transverse views), but none demonstrated typical echogenic crescentic central mesenteric fat or intralesional lymph nodes. Focal central echogenicity on US was misinterpreted in some cases as possible fat but proved to be debris or appendicoliths. All six of our cases had surrounding thick hyperechoic echogenicity that, in retrospect, likely represented inflamed fat walling off the perforated appendix. In five of six children the size of the mass on US ranged from 3 cm to 4.7 cm, with a mean size of 3.7 cm by 3 cm, similar to typical ileocolic intussusception (3–5 cm). Mass size was 2 cm by 2 cm in one child thought to have ileoileal intussusception.
The clinical presentations of children with acute appendicitis (including ruptured appendicitis) or intussusception can overlap, with both conditions capable of resulting in leukocytosis, fever and acute abdominal pain. A palpable mass in the right flank or lower abdomen is also common to both entities. Idiopathic intussusception is most often seen in children, mostly boys, between 6 months and 3 years of age and is considered to be related to hypertrophy of bowel lymphoid tissue (Peyer patches), often triggered by a preceding gastrointestinal illness. Intussusception in neonates, as well as older children, is less likely to be idiopathic and is frequently associated with a pathological lead point such as a Meckel diverticulum, duplication cyst, appendicitis, inspissated meconium (in cystic fibrosis), or a neoplasm such as a polyp or lymphoma [8]. Small-bowel intussusception can be a transient incidental finding on imaging, but symptomatic cases might require operative management, especially in postoperative patients, in association with small-bowel obstruction and with a longer segment of involvement [9, 10]. US examination is often the first imaging study performed in children with an acute abdominal presentation. Because of concerns for radiation exposure, especially in young children, CT is reserved for cases in which US findings are equivocal or non-diagnostic [1, 7]. The classic sonographic appearance of ileocolic intussusception is well-established [1–3, 5]. US is considered a very good imaging study for the detection of intussusception, with reported sensitivity of 100% and
Discussion Acute abdominal pain in children is a common diagnostic dilemma, with acute appendicitis and intussusception representing two of the most important diagnostic considerations [1, 6]. The classic symptoms of acute appendicitis include anorexia, periumbilical pain followed by right lower quadrant pain, and vomiting, which can be present in many other causes of acute abdominal pain in children. Classic symptoms of intussusception include intermittent abdominal pain and irritability with later diarrhea, bloody stools and lethargy, although approximately half of patients do not present with typical symptoms [1, 5].
Pediatr Radiol
specificity of 88%. The target, bull’s-eye, or doughnut sign of multiple hypoechoic concentric rings caused by edematous bowel walls, lymph nodes, and blood vessels with a crescentic hyperechoic focus of mesenteric fat between the two layers of bowel are well-known sonographic findings (Fig. 4) [2, 3]. The transverse appearance of a “crescent in a doughnut” is considered almost pathognomonic [3, 5] for intussusception. On longitudinal scans, the intussusception lesion is ovoid in shape, with different tissues appearing layered longitudinally and often referred to as a “sandwich” or “pseudokidney” sign (Fig. 4) [2]. Intralesional lymph nodes are commonly seen in ileocolic intussusception [10]. Other conditions can mimic the appearance of intussusception on US, including enterocolitis, volvulus, inflammatory bowel disease and other causes of edematous or hemorrhagic bowel, as well as feces-filled colon and even psoas hematoma [2, 5, 11]. Small-bowel intussusception has the same appearance but is usually more central in location, smaller than the typical 3- to 5-cm size of the mass in ileocolic intussusception and containing less mesenteric fat and fewer lymph nodes [1, 10]. Appendicitis can occur at any age but is relatively uncommon in younger infants. Appendiceal intussusception is very unusual, occurring either as an isolated entity or very rarely as part of an ileocolic intussusception [12, 13]. Appendiceal intussusception in children is associated with appendicitis or an appendiceal mass. None of our cases had surgical evidence of appendiceal or other intussusception. The classic sonographic appearance of acute appendicitis has been well-described. A blind-ending tubular structure arising from the base of the cecum measuring greater than 6 mm in diameter and having hyperemic walls as well as surrounding hyperechoic fat, free fluid or enlarged lymph nodes while being non-compressible is diagnostic of acute appendicitis [1, 4, 7]. Appendiceal rupture is particularly common in children [1]. Ruptured appendicitis can prove to be a difficult diagnosis, both clinically and sonographically. Sonographic signs of appendiceal perforation include loss of the echogenic mucosa, increased periappendiceal Fig. 4 Imaging in a 17-monthold boy who presented with cramping abdominal pain and ileocolic intussusception. Transverse (a) and sagittal (b) US images show the typical appearance of ieocolic intussusception, with a multilayered multiple-ring appearance with central echogenic fat and intralesional hypoechoic nodes (arrows). Note the absence of surrounding echogenic inflamed fat. The child underwent a successful airreduction enema
echogenicity from surrounding inflammation, and a complex mass or focal fluid collection [4]. The appendix itself might not be seen at all or be difficult to distinguish from surrounding inflammation, fluid and gas. We found that sonographic appearances of ruptured appendicitis can very closely mimic the sonographic findings of intussusception; we recognize that our sample size of six cases is small and that the unblinded methodology used to reevaluate the US studies is biased, but it still confirms that this misinterpretation can readily occur. Careful imaging, clinical correlation and an astute radiologist are required to distinguish the entities. The correct diagnosis is most likely to be considered when there is real-time visualization of the lesion in multiple planes by a pediatric radiologist, with recognition of surrounding echogenicity caused by inflamed fat, and the absence of central mesenteric fat or intralesional nodes. Lesion size was not helpful in our cases because the mass sizes were close to those expected in typical ileocolic intussusception, with the exception of one case, which was thought to be ileoileal intussusception. Clinical presentation and features such as fever and leukocytosis that might raise suspicion for appendicitis were not present in several of our cases. Also, the detailed clinical information was usually not available to the radiologist at the time of initial US examination. Because the US imaging of intussusception is typically highly reliable, the diagnosis was readily accepted and then acted on by clinicians. One result was a delay in diagnosis and treatment; mean diagnostic delay was 10.5 h but was as long as 24 h in one case. Another consequence was the addition of multiple imaging studies, including four contrast enemas, three repeat US studies and four CT scans. Very few prior reports of this misdiagnosis are in the literature, although we have encountered and been confounded by this problem on multiple occasions, as have other experienced pediatric radiologists (personal communications). A published review of emergency pediatric US imaging illustrates a case of ruptured appendicitis in a 7-year-old that closely mimicked an intussusception on US; he underwent
Pediatr Radiol
what was deemed an unsuccessful air-enema reduction and was only correctly diagnosed at surgery, similar to our cases [1]. Another case report detailed misdiagnosis of ruptured appendicitis on both US and CT as probable appendiceal intussusception in an 11-year-old girl [12]. In another case report an appendiceal hematoma in an 8-year-old girl with von Willebrand disease was originally thought to be an intussusception on US but was later identified as a hematoma on CT [11]. These individual reports suggest that the most helpful differential features were older patient age and smaller size of the lesion compared to that of typical idiopathic intussusception. The CT scans obtained in our cases were diagnostic of ruptured appendicitis with no confusion with intussusception (Figs. 1, 2 and 3). In situations where US or enema findings are unusual or at odds with the clinical picture, radiation concerns should not prevent the appropriate move to CT for clarification. MR is being used more commonly for the diagnosis of acute appendicitis and might also be an appropriate alternative in suitable patients. Our cases illustrate that ruptured appendicitis can appear as a rounded, mass-like structure with multiple rings that can be easily mistaken for intussusception. Awareness of the possibility of this confusion should encourage more detailed, thoughtful scrutiny of the initial images, with a greater consideration of the possibility of complicated appendicitis.
Conclusion Ruptured appendicitis is an important mimic of intussusception on US examination. Being mindful of ruptured appendicitis as a diagnostic possibility in children with atypical age or clinical features and US findings suggestive of intussusception should allow for careful attention to subtle differences in the sonographic appearances between the entities. Particular attention should be paid to evaluating the presence of surrounding inflamed fat in appendicitis and intralesional hypoechoic lymph nodes in ileocolic intussusception. An inner crescent of echogenic mesenteric fat between bowel loops is a virtually pathognomonic feature of intussusception that was not definitely present in our cases of ruptured appendicitis, although it was misinterpreted as such when central
echogenic debris or appendicolith was present. Real-time US imaging by a radiologist in multiple planes and direct communication with clinicians were useful in suggesting the correct diagnosis or correcting an erroneous one. CT was diagnostic in all four cases in which it was employed and should be considered promptly when there are equivocal US features or there is a discrepancy between US and clinical findings.
Conflict of interest None
References 1. Cogley JR, O’Connor SC, Houshyar R et al (2012) Emergent pediatric US: what every radiologist should know. Radiographics 32: 651–665 2. Anderson DR (1999) The pseudokidney sign. Radiology 211:395– 397 3. Del-Pozo G, Albillos JC, Tejedor D (1996) Intussusception: US findings with pathologic correlation—the crescent-in-doughnut sign. Radiology 199:688–692 4. Sivit CJ (1993) Diagnosis of acute appendicitis in children: spectrum of sonographic findings. AJR Am J Roentgenol 161:147–152 5. Daneman A, Navarro O (2003) Intussusception. Part 1: a review of diagnostic approaches. Pediatr Radiol 33:79–85 6. Van Breda Vriesman AC, Puylaert JB (2006) Mimics of appendicitis: alternative nonsurgical diagnoses with sonography and CT. AJR Am J Roentgenol 186:1103–1112 7. Krishnamoorthi R, Ramarajan N, Wang NE et al (2011) Effectiveness of a staged US and CT protocol for the diagnosis of pediatric appendicitis: reducing radiation exposure in the age of ALARA. Radiology 259:231–239 8. Williams H (2008) Imaging and intussusception. Arch Dis Child Educ Pract Ed 93:30–36 9. Ko SF, Lee TY, Ng SH et al (2002) Small bowel intussusception in symptomatic pediatric patients: experiences with 19 surgically proven cases. World J Surg 26:438–443 10. Lioubashevsky N, Hiller N, Rozovsky K et al (2013) Ileocolic versus small-bowel intussusception in children: can US enable reliable differentiation? Radiology 269:266–271 11. Tejani C, Phatak T, Sivitz A (2012) Right lower-quadrant pain— more than one diagnosis. Pediatr Emerg Care 28:1224–1226 12. Christianakis E, Sakelaropoulos A, Papantzimas C et al (2008) Pelvic plastron secondary to acute appendicitis in a child presented as appendiceal intussusception. A case report. Cases J 1:135 13. Dietz KR, Merrow AC, Podberesky DJ et al (2013) Beyond acute appendicitis: imaging of additional pathologies of the pediatric appendix. Pediatr Radiol 43:232–242, quiz 259
ORIGINAL ARTICLE
Perforated appendicitis: an underappreciated mimic of intussusception on ultrasound Beverley Newman & Matthew Schmitz & Rakhee Gawande & Shreyas Vasanawala & Richard Barth
Received: 17 October 2013 / Accepted: 6 January 2014 # Springer-Verlag Berlin Heidelberg 2014
Abstract Background We encountered multiple cases in which the US appearance of ruptured appendicitis mimicked intussusception, resulting in diagnostic and therapeutic delay and multiple additional imaging studies. Objective To explore the clinical and imaging discriminatory features between the conditions. Materials and methods Initial US images in six children (age 16 months to 8 years; 4 boys, 2 girls) were reviewed independently and by consensus by three pediatric radiologists. These findings were compared and correlated with the original reports and subsequent US, fluoroscopic, and CT images and reports. Results All initial US studies demonstrated a multiple-ringlike appearance (target sign, most apparent on transverse views) with diagnostic consensus supportive of intussusception. In three cases, US findings were somewhat discrepant with clinical concerns. Subsequently, four of the six children had contrast enemas; two were thought to have partial or complete intussusception reduction. Three had a repeat US examination, with recognition of the correct diagnosis. None of the US examinations demonstrated definite intralesional lymph nodes or mesenteric fat, but central echogenicity caused by debris/appendicolith was misinterpreted as fat. All showed perilesional hyperechogenicity that, in retrospect, represented inflamed fat “walling off” of the perforated appendix. There were four CTs, all of which demonstrated a double-ring appearance that correlated with the US target appearance, with B. Newman (*) : M. Schmitz : R. Gawande : S. Vasanawala : R. Barth Department of Radiology, Stanford University, Lucile Packard Children’s Hospital, 725 Welch Road, MC 5913, Stanford, CA 94305, USA e-mail: [email protected]
inner and outer rings representing the dilated appendix and walled-off appendiceal rupture, respectively. All six children had surgical confirmation of perforated appendicitis. Conclusion Contained perforated appendicitis can produce US findings closely mimicking intussusception. Clinical correlation and careful multiplanar evaluation should allow for sonographic suspicion of perforated appendicitis, which can be confirmed on CT if necessary.
Keywords Children . Appendicitis . Intussusception . Ultrasound . Computed tomography
Introduction Acute appendicitis and ileocolic intussusception are common causes of acute abdominal pain in young children. Timely and accurate diagnosis of these conditions is essential for prompt, appropriate treatment and minimization of patient morbidity. Imaging evaluation of abdominal pain in children often begins with a sonogram of the abdomen and pelvis [1]. The typical sonographic appearances of acute appendicitis and intussusception have been well illustrated [2–4]. Several potential mimics of intussusception on imaging have been described [1, 5, 6]. Little, however, has been written regarding the confusion of the sonographic appearances of ruptured appendicitis and intussusception. We consider ruptured appendicitis to be an important mimic of intussusception, with potential for delayed diagnosis or misdiagnosis. We also suggest that careful examination of specific findings on a sonogram can help in differentiating the conditions in a timely fashion.
Pediatr Radiol
Materials and methods The peer-review missed-case process identified six children over a 7-year period (2006–2013) who presented to the emergency room (ER) with abdominal symptoms including pain and had an initial sonographic diagnosis of intussusception but subsequent diagnosis of ruptured appendicitis. In all cases initial US images were obtained in the emergency room; these included gray-scale, cine and color Doppler images acquired by US technologists trained in adult and pediatric sonography. In two cases, the children were also scanned by a pediatric fellow (n=1) or attending physician (n=1). Most US studies were obtained on a GE Logiq E9 scanner (GE Healthcare, Milwaukee, WI), with one initial and several follow-up US studies on a Siemens Sequoia unit (Siemens Healthcare, Mountainview, CA). Two of the three follow-up studies were obtained in the pediatric sonography unit with dedicated pediatric technologists. All three repeat US studies were scanned by a faculty pediatric radiologist. Three pediatric radiologists (2 faculty, each with over 30 years of experience in pediatric radiology, 1 fellow) independently and with subsequent consensus evaluated the initial US studies in a non-blinded fashion. These evaluations were compared with the formal reports of the initial and follow-up US studies. Reviewers, aware of the final diagnosis of ruptured appendicitis, were asked whether they would have accepted the initial US diagnosis of intussusception and what US findings were most suggestive of the correct diagnosis. The images and reports of subsequent contrast enemas and CT scans were reviewed and correlated with the US images. Demographic data, clinical presentation and management, and surgical findings were obtained from a review of the patients’ charts; IRB permission was obtained for image and chart review.
Results The number of cases scanned in the same hospital ER for appendicitis or intussusception over the exact time period is not known. However a report from the same hospital noted that approximately 1,200 children were evaluated in the ER for suspected appendicitis during a 5-year period between 2003 and 2008 [7]. The six children described in the current report (Table 1) (2006–2013) ranged in age from 16 months to 8 years (mean age 4.4 years); there were 4 boys and 2 girls (Table 1). All six children presented with abdominal pain; four of the six had a history of fever or were febrile in the ER; three of six had an elevated white blood cell count (Table 1). Three children (ages 6–8 years) were older than the typical age for pediatric ileocolic intussusception, and in two cases clinical symptoms of periumbilical- to right-lower-quadrant pain were more typical of appendicitis than intussusception.
Table 1 Ruptured appendicitis mimicking intussusception Demographic data n=6
Age: 16 months–8 years, mean 4.4 years 4 boys, 2 girls
Clinical findings n=6
Abdominal pain—6 Fever—4 Elevated WBC—3 Idiopathic ileocolic intussusception—4 Intussuscepting calcified ileocolic mass—1 Ileoileal intussusception—1 Suggested ruptured appendicitis—3 (additional clinical information and consultation available, all three scanned directly by radiologist, one case after negative enema Normal—1 Pericolic inflammation, loculated free air—1 (suggestive of ruptured appendicitis) Intussusception reduced—2 (partial in 1) All diagnostic of ruptured appendicitis
Initial US diagnosis n=6 Repeat US n=3
Contrast enema interpretation n=4 Contrast-enhanced CT n=4 Surgery n=6
Acute laparoscopic appendectomy—3 Percutaneous abscess drainage—1 Antibiotics and interval appendectomy—2
WBC white blood cell count
The initial US images were obtained in the ER and were preliminarily interpreted by a radiology resident (1) or pediatric radiology fellow (2), with final interpretation (the same day in four and the next day in two cases) by various faculty pediatric radiologists with a wide range of experience. In all six cases sonographic diagnoses of right mid- to lowerquadrant mass consistent with intussusception were suggested. This was thought to be ileocolic and idiopathic in four cases (Figs. 1 and 2) (Table 1). In one child, the lesion was noted to contain a large central shadowing calcification that was interpreted as a probable pathological calcified mass and the lead point of an intussusception (Fig. 3). In a second child, the interpreting pediatric radiologist recommended a CT scan because of the patient’s age (8 years) and clinical symptoms of pain and fever, although the US findings were thought to be consistent with ileocolitis and an ileoileal intussusception. A third child, 23 months old, with an emergency-room US diagnosis of intussusception had repeated US imaging in the ER with real-time scanning by the pediatric radiologist prior to a planned air-reduction enema. Recognition of marked perilesional inflammatory changes and fluid led to a change in the suggested diagnosis and cancellation of the enema. Independent and consensus review of the six initial US examinations produced diagnostic agreement among the three reviewing pediatric radiologists that the initial diagnosis of intussusception was reasonably supported by the imaging appearance. Each case exhibited a right lower abdominal mass with an alternating hypoechoic and echogenic ring-like appearance, suggesting bowel within bowel (Figs. 1, 2 and 3).
Pediatr Radiol Fig. 1 Ruptured appendicitis in a 3-year-old girl who presented with cramping abdominal pain, was afebrile and had normal white blood cell count. a Anteroposterior abdominal radiograph shows multiple dilated bowel loops and a paucity of gas in the right lower quadrant. The properitoneal fat appears normal, and the cecum is not visualized. Clinical and imaging findings are most suggestive of intussusception. b Transverse US image demonstrates a mass in the right lower quadrant with multiple alternating layers suggestive of intussusception. Eccentric internal echogenicity (arrows) was thought to be suggestive of mesenteric fat. In retrospect, moderate perilesional echogenicity (inflammation) can be seen. c, d Axial contrast enhanced CT (c) and coronal reconstruction (d). The CT was obtained after a normal water soluble contrast enema followed by repeat US which showed the mass to be unchanged. The CT (c, d) demonstrated a complex mass in the right lower quadrant with central enhancing appendix (arrows) containing an appendicolith and surrounding fluid and inflammation, consistent with perforated appendicitis
This US appearance was considered too complex to simply represent thickened cecum. Subsequently four of the six children underwent contrast enemas for intussusception reduction. Experienced attending pediatric radiologists performed these studies. One enema in a 3-year-old was interpreted as normal; a repeat US demonstrated a persistent mass; the possibility of perforated appendicitis was considered and a CT scan was recommended (Fig. 1) (Table 1). A water-soluble enema in a 16-month-old child revealed a small bubble of air adjacent to the cecum in the right lower quadrant as well as pericecal inflammatory changes, suggesting ruptured appendicitis. However, in two 6-yearold children, the pediatric radiologists performing the enema examinations were convinced that intussusception had been present; one was thought to have been rapidly reduced (Fig. 2), and in the other case it was thought to have been incompletely reduced with a residual right lower quadrant
mass (Fig. 3). The child who was thought to have had an intussusception reduced on enema had progressive clinical symptoms of right lower quadrant pain and fever. He underwent a repeat US with direct scanning by an attending pediatric radiologist and discussion with the pediatric surgeon. Although the US appearance was similar to that of the prior study, marked echogenicity was recognized around the mass, suggesting inflammation, leading to the conclusion that ruptured appendicitis was probably a more likely diagnosis. This resulted in a confirmatory CT scan and prevented a planned repeat enema for intussusception reduction (Fig. 2). A total of four children had contrast-enhanced CTs demonstrating ruptured appendicitis. All the CT examinations demonstrated a double-ring appearance correlating with the US findings of the target sign, with inner and outer rings representing the dilated appendix and walled-off appendiceal rupture, respectively (Figs. 1, 2 and 3), with variable
Pediatr Radiol Fig. 2 Abdominal pain and perforated appendicitis mimicking ileocolic intussusception in a 6-year-old boy. a, b Transverse (with color Doppler) (a) and longitudinal (b) US images of the right lower quadrant demonstrate a 3.5×3-cm mass with sonolucent and hyperechoic layers thought to represent an intussusception. A central partially shadowing echogenic focus (arrows) was misinterpreted as central fat (fat should not be expected to shadow to this extent). c Fluoroscopic image from a water-soluble enema at which an intussusception was thought to have been rapidly reduced. There are mild right-side pericolic inflammatory changes, but no mass is evident. The appendix is not filled. d, e CT scan with IV contrast the next day, after repeat US suggested possible ruptured appendicitis. Axial (d) and coronal reconstruction (e) images show a central dilated fluid-filled appendix (arrows) with wall enhancement and periappendiceal fluid collection or abscess, suggestive of acute perforated appendicitis. There is residual bowel contrast from the prior enema. An appendicolith can be seen at the base of the appendix (arrow in e) and there is an additional fluid collection in the pelvis
surrounding phlegmon or fluid. Reaching the correct diagnosis of ruptured appendicitis took between 3 h and 24 h in these six children, with a mean of 10.5 h. All six children eventually had surgical confirmation of ruptured appendicitis with no evidence of appendiceal or other intussusception; in three cases laparoscopic appendectomy and drainage were performed acutely. One of these children developed subsequent adhesive small-bowel obstruction
requiring additional surgery. One child underwent percutaneous abscess drainage by interventional radiology, developed a colocutaneous fistula and had a subsequent interval appendectomy and drain removal. Two other children were treated with antibiotics acutely with interval appendectomy (Table 1). Upon further review of the initial US examinations, all six children demonstrated an appearance suggesting multiple concentric rings of bowel (target sign, most apparent on
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Fig. 3 Ruptured appendicitis in a 6-year-old girl. a Initial US, transverse view, shows a mass (4.7×4 cm) consisting of multiple concentric rings with a central echogenic shadowing focus (arrow) that was initially interpreted as an intussusception, with a calcified mass as the likely lead point. b An air enema later the same day demonstrates reflux of air into the small bowel with mass effect on the cecum (arrows) thought to
represent a residual unreduced intussusception with air having escaped into small bowel past the mass. c Axial post-contrast CT the same day demonstrates ruptured appendicitis with a central fluid-filled appendix and appendicolith (arrow) and surrounding fluid and inflammation corresponding to the multiple layers seen on ultrasonography
transverse views), but none demonstrated typical echogenic crescentic central mesenteric fat or intralesional lymph nodes. Focal central echogenicity on US was misinterpreted in some cases as possible fat but proved to be debris or appendicoliths. All six of our cases had surrounding thick hyperechoic echogenicity that, in retrospect, likely represented inflamed fat walling off the perforated appendix. In five of six children the size of the mass on US ranged from 3 cm to 4.7 cm, with a mean size of 3.7 cm by 3 cm, similar to typical ileocolic intussusception (3–5 cm). Mass size was 2 cm by 2 cm in one child thought to have ileoileal intussusception.
The clinical presentations of children with acute appendicitis (including ruptured appendicitis) or intussusception can overlap, with both conditions capable of resulting in leukocytosis, fever and acute abdominal pain. A palpable mass in the right flank or lower abdomen is also common to both entities. Idiopathic intussusception is most often seen in children, mostly boys, between 6 months and 3 years of age and is considered to be related to hypertrophy of bowel lymphoid tissue (Peyer patches), often triggered by a preceding gastrointestinal illness. Intussusception in neonates, as well as older children, is less likely to be idiopathic and is frequently associated with a pathological lead point such as a Meckel diverticulum, duplication cyst, appendicitis, inspissated meconium (in cystic fibrosis), or a neoplasm such as a polyp or lymphoma [8]. Small-bowel intussusception can be a transient incidental finding on imaging, but symptomatic cases might require operative management, especially in postoperative patients, in association with small-bowel obstruction and with a longer segment of involvement [9, 10]. US examination is often the first imaging study performed in children with an acute abdominal presentation. Because of concerns for radiation exposure, especially in young children, CT is reserved for cases in which US findings are equivocal or non-diagnostic [1, 7]. The classic sonographic appearance of ileocolic intussusception is well-established [1–3, 5]. US is considered a very good imaging study for the detection of intussusception, with reported sensitivity of 100% and
Discussion Acute abdominal pain in children is a common diagnostic dilemma, with acute appendicitis and intussusception representing two of the most important diagnostic considerations [1, 6]. The classic symptoms of acute appendicitis include anorexia, periumbilical pain followed by right lower quadrant pain, and vomiting, which can be present in many other causes of acute abdominal pain in children. Classic symptoms of intussusception include intermittent abdominal pain and irritability with later diarrhea, bloody stools and lethargy, although approximately half of patients do not present with typical symptoms [1, 5].
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specificity of 88%. The target, bull’s-eye, or doughnut sign of multiple hypoechoic concentric rings caused by edematous bowel walls, lymph nodes, and blood vessels with a crescentic hyperechoic focus of mesenteric fat between the two layers of bowel are well-known sonographic findings (Fig. 4) [2, 3]. The transverse appearance of a “crescent in a doughnut” is considered almost pathognomonic [3, 5] for intussusception. On longitudinal scans, the intussusception lesion is ovoid in shape, with different tissues appearing layered longitudinally and often referred to as a “sandwich” or “pseudokidney” sign (Fig. 4) [2]. Intralesional lymph nodes are commonly seen in ileocolic intussusception [10]. Other conditions can mimic the appearance of intussusception on US, including enterocolitis, volvulus, inflammatory bowel disease and other causes of edematous or hemorrhagic bowel, as well as feces-filled colon and even psoas hematoma [2, 5, 11]. Small-bowel intussusception has the same appearance but is usually more central in location, smaller than the typical 3- to 5-cm size of the mass in ileocolic intussusception and containing less mesenteric fat and fewer lymph nodes [1, 10]. Appendicitis can occur at any age but is relatively uncommon in younger infants. Appendiceal intussusception is very unusual, occurring either as an isolated entity or very rarely as part of an ileocolic intussusception [12, 13]. Appendiceal intussusception in children is associated with appendicitis or an appendiceal mass. None of our cases had surgical evidence of appendiceal or other intussusception. The classic sonographic appearance of acute appendicitis has been well-described. A blind-ending tubular structure arising from the base of the cecum measuring greater than 6 mm in diameter and having hyperemic walls as well as surrounding hyperechoic fat, free fluid or enlarged lymph nodes while being non-compressible is diagnostic of acute appendicitis [1, 4, 7]. Appendiceal rupture is particularly common in children [1]. Ruptured appendicitis can prove to be a difficult diagnosis, both clinically and sonographically. Sonographic signs of appendiceal perforation include loss of the echogenic mucosa, increased periappendiceal Fig. 4 Imaging in a 17-monthold boy who presented with cramping abdominal pain and ileocolic intussusception. Transverse (a) and sagittal (b) US images show the typical appearance of ieocolic intussusception, with a multilayered multiple-ring appearance with central echogenic fat and intralesional hypoechoic nodes (arrows). Note the absence of surrounding echogenic inflamed fat. The child underwent a successful airreduction enema
echogenicity from surrounding inflammation, and a complex mass or focal fluid collection [4]. The appendix itself might not be seen at all or be difficult to distinguish from surrounding inflammation, fluid and gas. We found that sonographic appearances of ruptured appendicitis can very closely mimic the sonographic findings of intussusception; we recognize that our sample size of six cases is small and that the unblinded methodology used to reevaluate the US studies is biased, but it still confirms that this misinterpretation can readily occur. Careful imaging, clinical correlation and an astute radiologist are required to distinguish the entities. The correct diagnosis is most likely to be considered when there is real-time visualization of the lesion in multiple planes by a pediatric radiologist, with recognition of surrounding echogenicity caused by inflamed fat, and the absence of central mesenteric fat or intralesional nodes. Lesion size was not helpful in our cases because the mass sizes were close to those expected in typical ileocolic intussusception, with the exception of one case, which was thought to be ileoileal intussusception. Clinical presentation and features such as fever and leukocytosis that might raise suspicion for appendicitis were not present in several of our cases. Also, the detailed clinical information was usually not available to the radiologist at the time of initial US examination. Because the US imaging of intussusception is typically highly reliable, the diagnosis was readily accepted and then acted on by clinicians. One result was a delay in diagnosis and treatment; mean diagnostic delay was 10.5 h but was as long as 24 h in one case. Another consequence was the addition of multiple imaging studies, including four contrast enemas, three repeat US studies and four CT scans. Very few prior reports of this misdiagnosis are in the literature, although we have encountered and been confounded by this problem on multiple occasions, as have other experienced pediatric radiologists (personal communications). A published review of emergency pediatric US imaging illustrates a case of ruptured appendicitis in a 7-year-old that closely mimicked an intussusception on US; he underwent
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what was deemed an unsuccessful air-enema reduction and was only correctly diagnosed at surgery, similar to our cases [1]. Another case report detailed misdiagnosis of ruptured appendicitis on both US and CT as probable appendiceal intussusception in an 11-year-old girl [12]. In another case report an appendiceal hematoma in an 8-year-old girl with von Willebrand disease was originally thought to be an intussusception on US but was later identified as a hematoma on CT [11]. These individual reports suggest that the most helpful differential features were older patient age and smaller size of the lesion compared to that of typical idiopathic intussusception. The CT scans obtained in our cases were diagnostic of ruptured appendicitis with no confusion with intussusception (Figs. 1, 2 and 3). In situations where US or enema findings are unusual or at odds with the clinical picture, radiation concerns should not prevent the appropriate move to CT for clarification. MR is being used more commonly for the diagnosis of acute appendicitis and might also be an appropriate alternative in suitable patients. Our cases illustrate that ruptured appendicitis can appear as a rounded, mass-like structure with multiple rings that can be easily mistaken for intussusception. Awareness of the possibility of this confusion should encourage more detailed, thoughtful scrutiny of the initial images, with a greater consideration of the possibility of complicated appendicitis.
Conclusion Ruptured appendicitis is an important mimic of intussusception on US examination. Being mindful of ruptured appendicitis as a diagnostic possibility in children with atypical age or clinical features and US findings suggestive of intussusception should allow for careful attention to subtle differences in the sonographic appearances between the entities. Particular attention should be paid to evaluating the presence of surrounding inflamed fat in appendicitis and intralesional hypoechoic lymph nodes in ileocolic intussusception. An inner crescent of echogenic mesenteric fat between bowel loops is a virtually pathognomonic feature of intussusception that was not definitely present in our cases of ruptured appendicitis, although it was misinterpreted as such when central
echogenic debris or appendicolith was present. Real-time US imaging by a radiologist in multiple planes and direct communication with clinicians were useful in suggesting the correct diagnosis or correcting an erroneous one. CT was diagnostic in all four cases in which it was employed and should be considered promptly when there are equivocal US features or there is a discrepancy between US and clinical findings.
Conflict of interest None
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