Pediatric Imaging
Pictorial Essay
Childhood Burkitt Lymphoma: Abdominal and Pelvic Imaging Findings
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OBJECTIVE. Burkitt lymphoma in children can be localized or disseminated and can involve various sites. Our objective is to review the clinical presentation and abdominopelvic imaging findings of Burkitt lymphoma in the pediatric population.
CONCLUSION. Numerous abdominal and pelvic imaging findings are seen in Burkitt lymphoma affecting the gastrointestinal tract and solid organs. Recognition of the common and uncommon imaging findings is essential in the diagnosis and treatment of patients with Burkitt lymphoma because prompt therapy is critical.
Keywords: abdominal imaging, Burkitt lymphoma, pediatric imaging, pelvic imaging
| Introduction |   |
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Approximately 500 cases of childhood non-Hodgkin's lymphoma are diagnosed annually in the United States, and for unknown reasons, the average incidence has increased [1]. Burkitt lymphoma is the most frequent subtype of non-Hodgkin's lymphoma in childhood and accounts for approximately 34% of these cases. Burkitt lymphoma is the most rapidly growing tumor in children, with a doubling time of approximately 24 hours, so prompt recognition and initiation of therapy are essential [2, 3]. It occurs more often in boys than girls with male-to-female ratios ranging from 1.3:1 to 8.8:1 [4]. The median age of children with Burkitt lymphoma is 8 years (age range, 0–20 years), with children who are 5–9 years old representing more than one third of the cases [5].
Burkitt lymphoma was first described in 1958 in Uganda by a surgeon who observed rapidly enlarging tumors in children involving the jaw. Since then, Burkitt lymphoma has been categorized by the World Health Organization into three types: endemic, sporadic, and immunodeficiency-associated types [6]. The endemic form is found mostly in equatorial Africa and Papua New Guinea and is associated with the Epstein-Barr virus in 95% of cases. The sporadic (or American) form is found in North America, Northern and Eastern Europe, and the Far East and is associated with the Epstein-Barr virus in 15% of patients [6, 7]. The immunodeficiency-associated form occurs mainly in patients with HIV but can also occur in allograft recipients and patients with congenital immunodeficiencies, such as Wiskott-Aldrich syndrome, ataxia telangiectasia, or X-linked lymphoproliferative disease [1, 6].
Although Burkitt lymphoma can involve the head and neck in children, the gastrointestinal tract, genitourinary tract, gonads, mesentery, peritoneum, and retroperitoneum are also potential sites of involvement. Intrinsic involvement within the gastrointestinal tract has been reported to occur in 22.5% of cases, abdominal or pelvic masses in 45% of cases, and hepatic lesions in 17% of cases, with the predominance of these cases occurring in children [8, 9]. In this article, we discuss the clinical and imaging manifestations of Burkitt lymphoma with particular attention to the ultrasound and CT features in the abdomen and pelvis of pediatric patients. Some of the imaging findings seen in patients with Burkitt lymphoma at our institution have not been well described in the literature as specific findings of Burkitt lymphoma. We correlated these features with the imaging findings of non-Hodgkin's lymphoma.
| Clinical Features | |
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Pediatric patients typically present with Burkitt lymphoma with extranodal involvement, specifically occurring in the abdomen approximately 31% of the time [1]. The clinical presentation of Burkitt lymphoma is varied and depends on the site of involvement. Clinical manifestations in the abdomen are commonly secondary to compression, obstruction of adjacent structures, or infiltration of structures by tumor. Common presenting symptoms include abdominal pain, palpable mass, nausea and vomiting, intestinal obstruction due to bowel compression or intussusception, and acute appendicitis. Weight loss, fever, and other systemic features present more often with disseminated disease but are less commonly seen than in other types of non-Hodgkin's lymphoma in childhood [7, 10]. Children may also present with obstructive jaundice if extrahepatic bulky adenopathy compresses the biliary tree in the porta hepatis [1, 8, 11, 12]. Burkitt lymphoma involving the kidneys can result in renal failure secondary to obstruction or tumor infiltration of the kidneys or in paraneoplastic effects that manifest as glomerulonephritis, paraproteinemia, or cryoglobulinemia [13].
| Imaging Workup | |
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The diagnostic workup for Burkitt lymphoma, like any other form of non-Hodgkin's lymphoma, is definitive by tissue diagnosis. Cross-sectional imaging is necessary to determine the distribution, severity, and staging to implement appropriate therapy. Imaging techniques most often used include ultrasound, CT, PET/CT, gallium scintigraphy, and bone scintigraphy. Ultrasound is used initially if a child presents with an abdominal or pelvic mass. CT would often follow ultrasound to allow a more global assessment for bowel and visceral involvement as well as tumor staging. Because of concerns about radiation risk to oncology patients, particularly those who are children, with repeat imaging examinations, the role of MRI is likely to increase.
In the past, gallium scintigraphy was the best functional imaging technique for the evaluation of Burkitt lymphoma. Recently at our institution, PET/CT has become the preferred functional imaging technique both for initial staging and for evaluation response to treatment in children with Burkitt lymphoma because of a shorter interval between injection and imaging, completion of the studies in only a few hours, and improved image quality. PET/CT has been shown to reveal disease sites that were not previously identified, leading to upstaging of the disease [14]. PET/CT also has better dosimetry, which is particularly important when imaging children, in comparison with gallium scintigraphy [15].
| Gastrointestinal Involvement | |
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The distal small bowel, ileum, cecum, and appendix are common sites of involvement of non-Hodgkin's lymphoma including Burkitt lymphoma; however, disease involvement of the proximal gastrointestinal tract also occurs. Posterior mediastinal extension along the esophagus has been rarely reported [16].
Gastric involvement with Burkitt lymphoma is rare [17]. The most common finding of stomach involvement at CT is diffuse infiltration of the gastric wall (Figs. 1, 2A, 2B, and 2C), and an infrequent finding is a focal gastric wall mass [17–20].
Burkitt lymphoma primarily affects the ileocecal region in children younger than 16 years old. The terminal ileum is the most commonly reported location of Burkitt lymphoma in children, likely because of the high concentration of lymph tissue in that region of the bowel [8]. In that the tumor does not elicit a desmoplastic response, bowel obstruction is most often caused by intussusception [21, 22]. Imaging findings on CT include a focal mass (Fig. 3A) and diffuse thickening of the bowel wall [2, 18] (Figs. 4A and 4B). Cavitary lesions with communication with the bowel and perforation of the bowel with abscess formation can occur but are uncommon [16, 18]. Ultrasound findings in Burkitt lymphoma involving the intestines include the doughnut sign of intussusception; the pseudokidney sign, with or without intussusception, due to diffuse bowel wall thickening with a central echogenic region caused by intraluminal air [23] (Fig. 3B); or the target sign when occult tumor of the cecum invaginates into the ascending colon. Bowel wall thickening may be due to lymphedema or tumor infiltration.
The frequency of non-Hodgkin's lymphoma involving the appendix has been reported to be as low as 1–3%, and the most common clinical presentation is right lower quadrant pain and fever suggestive of acute appendicitis [24]. In our cases, we found a child who presented with perforated acute appendicitis who was diagnosed with Burkitt lymphoma postoperatively after appendectomy. Because Burkitt involvement of the appendix is so rare, it is not surprising that the imaging findings in that case are nonspecific. Findings of appendiceal lymphoma include prominent enlargement of the appendix with maintenance of its vermiform appearance and diffuse mural thickening due to lymphomatous replacement of the appendiceal wall [12, 24].
| Solid Organs | |
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Although primary hepatic lymphoma is rare, secondary hepatic involvement with non-Hodgkin's lymphoma has been reported in 14% of patients. Hepatic involvement in Burkitt lymphoma is approximately 17% [9, 25]. The most common findings on CT are discrete areas of low attenuation that may be solitary or multicentric (Fig. 5). A periportal infiltrating mass, which is low in attenuation on CT (Fig. 6A) and hypoechoic on ultrasound (Fig. 6B), has also been reported with or without distal biliary duct dilatation [9, 25, 26] (Fig. 6A).
The spleen is not often involved in Burkitt lymphoma; however, the most common radiologic finding is diffuse splenomegaly. Other radiologic findings include hypoechoic splenic lesions on ultrasound examination and low-attenuation splenic lesions on CT examination [8, 19, 16, 25] (Figs. 7A and 7B).
Non-Hodgkin's lymphoma more commonly involves the kidney than does Hodgkin's lymphoma [27]. CT findings of renal involvement of Burkitt lymphoma most commonly include nephromegaly (90%). Focal renal masses (30%) and hydronephrosis due to ureteral obstruction (50%) are also seen (Fig. 8). At ultrasound, kidneys may show increased cortical echogenicity (60%) with or without iso- or hypoechoic masses. Renal calculi, associated with tumor lysis syndrome after chemotherapy, have been observed on ultrasound and CT [28]. Although Burkitt lymphoma responds well to chemotherapy, it can progress to renal failure due to obstruction in approximately one third of the patients [13].
The pancreas is involved in Burkitt lymphoma in approximately 10% of cases [19]. CT findings included focal pancreatic enlargement with patchy areas of nonenhancement [29]. Marked dilatation of the biliary system can occur when a mass infiltrates the pancreatic head [11] (Figs. 9A, 9B, and 9C).
Only 13% of all cases of lymphoma involve the gallbladder, and approximately 11% of non-Hodgkin's lymphoma cases involve the gallbladder [30, 31]. Involvement of the gallbladder is nonspecific, and imaging features are often similar to those of other common diseases affecting the gallbladder. Clinical features are similar to acute cholecystitis [32]. Imaging findings include an intraluminal filling defect and thickening of the gallbladder wall [30, 32] (Figs. 10A and 10B).
| Mesenteric and Retroperitoneal Disease | |
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Involvement of the lymph nodes in the mesentery and retroperitoneum by Burkitt lymphoma commonly presents as abdominal and pelvic masses. These masses may be large and single or multiple in the abdomen or pelvis. Some masses may have necrotic centers containing fluid (Figs. 11A, 11B, and 12) or, in rare cases, air (Figs. 13A and 13B); encasement of the major mesenteric vessels is common. Calcification of mesenteric and retroperitoneal masses has been reported in aggressive types of non-Hodgkin's lymphoma and, specifically, in Burkitt lymphoma. Types of calcifications include small punctuate foci within nodes, small calcifications around necrotic areas, and amorphous or linear calcifications in the periphery of large masses [10, 33, 34].
| Peritoneal Seeding | |
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Ascites is a common finding that occurs in 25% of patients with Burkitt lymphoma [9]. The diagnosis of Burkitt lymphoma can often be made by paracentesis [2]. Lymphomatous involvement of the peritoneum is not frequent in children, but is usually associated with widespread bowel or mesenteric inflammation. CT findings of Burkitt lymphoma may mimic mucinous tumor in the adult population and can be confused with desmoplastic small round cell tumor in children and adolescents, which may have a similar clinical presentation [35]. The findings on CT include nodularity along the peritoneal reflections (Fig. 12) and liver capsule with peritoneal ascites. At ultrasound, peritoneal involvement appears as hypoechoic mesenteric masses or, rarely in Burkitt lymphoma, as omental cakes [10, 36].
| Gonads | |
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Testicular tumors, in general, are rare in children [37]. Involvement of the testes with Burkitt lymphoma has been reported in approximately 5% of male patients. In 4%, testicular enlargement is the main presenting sign [38, 39]. Sonography is the primary imaging technique and most often shows hypoechoic intratesticular lesions in secondary and primary Burkitt lymphoma [37, 38]. Diffuse hypoechoic replacement in the testes with or without hyperemia [10], has also been reported (Fig. 14). Sonographic imaging findings of Burkitt lymphoma involving the epididymis include a hypoechoic mass or heterogeneously increased echogenicity [39]. Burkitt lymphoma may also involve the spermatic cord and epididymis without testicular involvement. On CT, the spermatic cord may be enlarged in size and may enhance after the IV administration of contrast material (Figs. 15A, 15B, 15C, 15D, and 15E).
The ovary is the most frequent site of non-Hodgkin's lymphoma in the gynecologic tract [40]. Specifically, Burkitt lymphoma has been reported to be 19% of adnexal lymphomas [41]. Imaging findings are nonspecific but include unilateral or bilateral cystic, solid, or mixed masses that are hypoechoic on ultrasound or hypodense or mildly enhancing masses on contrast-enhanced CT [3].
| Conclusions | |
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The abdominal and pelvic imaging findings in Burkitt lymphoma affecting solid organs and the gastrointestinal tract are numerous and varied. Although ultrasound is the initial imaging study in a child with an abdominal mass, CT is often used because of the multifocality of presentation and a propensity to involve bowel and mesentery. PET/CT recently has become the preferable functional imaging technique in children because of the shorter interval between injection and imaging, completion of the studies in only a few hours, improved image quality, and better dosimetry. Recognition of the common and uncommon imaging findings is essential in the consideration of Burkitt lymphoma as a potential diagnosis to rapidly initiate therapy in patients because prompt supportive care and therapy are critical.
 View larger version (134K) | Fig. 1 —3-year-old boy with gastric findings in Burkitt lymphoma. Axial enhanced CT scan of upper abdomen shows diffuse thickening of gastric wall (arrow). |
 View larger version (154K) | Fig. 2A —6-year-old boy with Burkitt lymphoma. Axial contrast-enhanced CT image of upper abdomen shows focal gastric mass (arrow). |
 View larger version (160K) | Fig. 2B —6-year-old boy with Burkitt lymphoma. Axial contrast-enhanced CT image shows large retroperitoneal mass encasing major abdominal vasculature (arrow). |
 View larger version (89K) | Fig. 2C —6-year-old boy with Burkitt lymphoma. PET image shows focal hypermetabolic activity in upper abdomen corresponding to mass seen on CT. |
 View larger version (223K) | Fig. 3A —11-year-old boy with Burkitt lymphoma. Axial (A) and coronal (B) contrast-enhanced multiplanar reformation CT images reveal focal mass in cecum (arrows). |
 View larger version (170K) | Fig. 3B —11-year-old boy with Burkitt lymphoma. Axial (A) and coronal (B) contrast-enhanced multiplanar reformation CT images reveal focal mass in cecum (arrows). |
 View larger version (207K) | Fig. 3C —11-year-old boy with Burkitt lymphoma. Finding in A and B correlates with pseudokidney sign in absence of true intussusception seen on transverse ultrasound image. |
 View larger version (134K) | Fig. 4A —6-year-old boy with Burkitt lymphoma. Axial (A) and coronal (B) contrast-enhanced multiplanar formation CT images show concentric wall thickening with aneurysmal dilatation of several bowel segments (arrows) in absence of obstruction. |
 View larger version (174K) | Fig. 4B —6-year-old boy with Burkitt lymphoma. Axial (A) and coronal (B) contrast-enhanced multiplanar formation CT images show concentric wall thickening with aneurysmal dilatation of several bowel segments (arrows) in absence of obstruction. |
 View larger version (154K) | Fig. 5 —3-year-old boy with Burkitt lymphoma. Axial contrast-enhanced CT image of upper abdomen shows focal mass (arrowheads) in liver. |
 View larger version (154K) | Fig. 6A —3-year-old boy with Burkitt lymphoma. Axial (A) and coronal (B) contrast-enhanced multiplanar reformation CT images of abdomen show large, infiltrative, low-attenuation periportal mass (arrows) with mild intrahepatic duct dilatation. |
 View larger version (133K) | Fig. 6B —3-year-old boy with Burkitt lymphoma. Axial (A) and coronal (B) contrast-enhanced multiplanar reformation CT images of abdomen show large, infiltrative, low-attenuation periportal mass (arrows) with mild intrahepatic duct dilatation. |
 View larger version (208K) | Fig. 6C —3-year-old boy with Burkitt lymphoma. Sonographic image of liver shows hypoechoic infiltrative periportal mass (arrow). |
 View larger version (141K) | Fig. 7A —16-year-old boy with Burkitt lymphoma. Axial contrast-enhanced CT (A) and ultrasound (B) images of upper abdomen show enlarged spleen with multiple low-attenuation (arrows, A) and hypoechoic (arrowheads, B) lesions representing focal tumor. |
 View larger version (183K) | Fig. 7B —16-year-old boy with Burkitt lymphoma. Axial contrast-enhanced CT (A) and ultrasound (B) images of upper abdomen show enlarged spleen with multiple low-attenuation (arrows, A) and hypoechoic (arrowheads, B) lesions representing focal tumor. |
 View larger version (127K) | Fig. 8 —3-year-old boy with Burkitt lymphoma (same patient as in Fig. 1). Axial contrast-enhanced CT image shows multiple hypodense lesions in kidneys (arrows) and single hypodense lesion in right lobe of liver (arrowhead). |
 View larger version (114K) | Fig. 9A —13-year-old girl with Burkitt lymphoma. Delayed axial CT images of abdomen after contrast administration show large, hypodense pancreatic head mass (arrowheads, A) with dilatation of extrahepatic duct (arrow, A) and intrahepatic duct dilatation (oval, B). |
 View larger version (124K) | Fig. 9B —13-year-old girl with Burkitt lymphoma. Delayed axial CT images of abdomen after contrast administration show large, hypodense pancreatic head mass (arrowheads, A) with dilatation of extrahepatic duct (arrow, A) and intrahepatic duct dilatation (oval, B). |
 View larger version (77K) | Fig. 9C —13-year-old girl with Burkitt lymphoma. Sonographic image shows intrahepatic duct dilatation. |
 View larger version (134K) | Fig. 10A —10-year-old boy with Burkitt lymphoma. Axial contrast-enhanced CT (A) and ultrasound (B) images of upper abdomen show diffuse thickening of wall of gallbladder (arrows). |
 View larger version (163K) | Fig. 10B —10-year-old boy with Burkitt lymphoma. Axial contrast-enhanced CT (A) and ultrasound (B) images of upper abdomen show diffuse thickening of wall of gallbladder (arrows). |
 View larger version (151K) | Fig. 11A —9-year-old boy with Burkitt lymphoma. Axial (A) and coronal (B) contrast-enhanced multiplanar reformation CT images show large mesenteric mass (arrows) in right upper quadrant of abdomen with central necrosis. |
 View larger version (191K) | Fig. 11B —9-year-old boy with Burkitt lymphoma. Axial (A) and coronal (B) contrast-enhanced multiplanar reformation CT images show large mesenteric mass (arrows) in right upper quadrant of abdomen with central necrosis. |
 View larger version (221K) |
 View larger version (188K) | Fig. 13A —19-year-old man with Burkitt lymphoma. Unenhanced CT image shows large mesenteric mass in right lower quadrant of abdomen with air centrally. |
 View larger version (128K) | Fig. 13B —19-year-old man with Burkitt lymphoma. Sonographic image of same mass (cursors) in A shows shadowing; hyperechoic center consistent with air. |
 View larger version (112K) | Fig. 13C —19-year-old man with Burkitt lymphoma. FDG PET image shows right lower quadrant mass (arrow) with hypermetabolic rim and photopenic center consistent with necrosis. |
 View larger version (95K) | Fig. 14 —8-year-old boy with Burkitt lymphoma. Sonographic image of left testis shows enlarged hypoechoic testis. |
 View larger version (141K) | Fig. 15A —9-year-old boy with Burkitt lymphoma. Contrast-enhanced CT images of pelvis show enhancing lesion in right inguinal canal extending into right paratesticular tissues (arrows). |
 View larger version (135K) | Fig. 15B —9-year-old boy with Burkitt lymphoma. Contrast-enhanced CT images of pelvis show enhancing lesion in right inguinal canal extending into right paratesticular tissues (arrows). |
 View larger version (88K) | Fig. 15C —9-year-old boy with Burkitt lymphoma. Sonographic images show enlargement of right inguinal canal (oval, C) in comparison with left. |
 View larger version (85K) | Fig. 15D —9-year-old boy with Burkitt lymphoma. Sonographic images show enlargement of right inguinal canal (oval, C) in comparison with left. |
 View larger version (105K) | Fig. 15E —9-year-old boy with Burkitt lymphoma. Sonographic image shows heterogeneous mass (arrow) in right paratesticular tissues. RT = right testis, LT = left testis. |
Address correspondence to D. M. Biko ([email protected]).
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