Ultrasound presentation of abdominal non-Hodgkin lymphomas in pediatric patients

Abstract

Introduction

Burkitt's lymphoma accounts for approximately 25% of lymphomas diagnosed in children of developmental age. The tumor is localized mainly in the intestine (usually in the ileocecal region), mesenteric lymph nodes and extraperitoneal space. The clinical symptoms are non-specific and include: abdominal pain, vomiting, gastrointestinal bleeding, and acute abdomen suggesting appendicitis or intestinal intussusception. On ultrasound examination, Burkitt's lymphoma may manifest itself in various ways, depending on the origin of the lesion.

Aim

The aim of this paper was to review the ultrasound manifestation of abdominal Burkitt's lymphoma in children.

Material and methods

The analysis included 15 pediatric patients with Burkitt's non-Hodgkin lymphoma in the abdominal cavity. The mean age of the patients was 9.5. Abdominal and gastrointestinal ultrasound examinations were conducted using a Siemens scanner with a convex transducer of 3.5–5 MHz and linear array transducer of L4 – 7.5 MHz.

Results

Ultrasound examinations conducted in the group of 15 patients revealed pathological masses localized in the gastric wall in 3 patients (20%), in the ileocecal region in 10 patients (67%) and a disseminated process in 2 patients (13%). In 12 patients with a diagnosed Burkitt's non-Hodgkin lymphoma in an extragastric localization, differences in the morphology of the lesions were observed.

Conclusions

The clinical and ultrasound picture of abdominal Burkitt's lymphoma in children is variable. A careful ultrasound assessment of all abdominal organs conducted with the use of convex and linear probes increases the chances of establishing an adequate diagnosis.

Introduction

Burkitt's lymphoma accounts for 25–50% of non-Hodgkin lymphomas that occur in childhood^{(1, 2)}. It occurs endemically in African children in whom it is localized mainly in the mandibular and maxillary bones. The abdominal form of Burkitt's lymphoma is more frequently found in non-African children⁽³⁾. The extranodal localization of lymphoma is usually the small intestine, with a tendency to occur in the ileocecal region. The gastric wall is a very rare site of origin in children⁽⁴⁾. Within the abdominal cavity, lymphoma may also be localized in the mesenteric lymph nodes and extraperitoneal space⁽⁵⁾. Patients seek medical advice due to non-specific symptoms of abdominal pain, gastrointestinal bleeding and anemia or with symptoms of acute abdomen suggestive of appendicitis, bowel obstruction or intestinal intussusception⁽⁶⁾. The ultrasound (US) presentation of gastrointestinal non-Hodgkin lymphoma is ambiguous and should be differentiated from other pathologies, such as inflammatory lesions in the intestine, appendicitis or intestinal intramural hematoma.

Burkitt's lymphoma that originates from lymph follicles of the terminal ileum submucosa spreads along the wall, which on US examination is manifested by fragmentary thickening with low echogenicity and a blurred layered structure. Wall infiltration may be asymmetrical and the bowel lumen may be normal or narrowed⁽⁷⁾. Single or multifocal and oval areas of low echogenicity surrounded by hyperechoic mesentery are characteristic of abdominal lymph node involvement by lymphoma.

In physiological conditions, there is no lymphatic tissue in the gastric mucosa. A chronic inflammatory process, e.g. infection with Helicobacter pylori, may facilitate the development of the lymphatic tissue, which, in turn, may transform into a neoplasm. In the adult population, non-Hodgkin lymphomas of the stomach are usually of the MALT type (mucosa-associated lymphoid tissue). In children, they are usually Burkitt's non-Hodgkin lymphoma⁽⁸⁾. MALT-lymphoma is not typical of the stomach and its malignancy is low. However, Burkitt's lymphoma may be highly malignant. Depending on the extent of the lesion, US examination helps to assess the thickening of individual layers of the gastric wall, which is usually of low echogenicity, with or without a preserved layered structure.

The initial diagnosis of the character of the infiltration in the gastrointestinal tract may be determined on the basis of ultrasound presentation. However, a histopathological analysis of a collected sample constitutes a decisive examination.

Material and methods

From 2000 to 2012, 15 pediatric patients (one girl and 14 boys) were diagnosed and treated for abdominal Burkitt's non-Hodgkin lymphoma in the Department of Pediatric Radiology and in the Department of Pediatric Hematology and Oncology, Medical University of Lublin, Poland. The patients were aged between 2 and 17 (mean age was 9 years and 6 months). The clinical symptoms of abdominal pain, weight loss, vomiting and general malaise prevailed. Additionally, 2 patients presented with yellowed skin and 2 had gastrointestinal bleeding and anemia. A pathological mass was palpable in the abdomen in all patients. In one case, the only symptom of the neoplasm was an enlarged lymph node localized on the medial surface of the right thigh.

Ultrasound examinations were conducted with the use of a Siemens scanner with a convex transducer of 3.5–5 MHz and a high-frequency linear array transducer of L4 – 7.5 MHz. The following modes were used: B-mode, color and power Doppler as well as tissue harmonic imaging (THI). The gastrointestinal tract was assessed using an ultrasound set-up for organs located superficially (set-up “small parts”).

During the diagnostic process, all patients underwent laboratory tests, biochemical examinations (LDH level), bone marrow examination as well as abdominal and pelvic computed tomography.

Results

Ultrasound examinations conducted in the group of 15 patients revealed pathological masses localized in the gastric wall in 3 patients (20%), in the ileocecal region in 10 patients (67%) and a disseminated process in 2 patients (13%).

In the group of 3 patients in which the lesion originated from the gastric wall, the body of the stomach and prepyloric region were involved. In 2 patients, a pathological mass with heterogeneous echogenicity protruded into the gastric lumen and narrowed it considerably; in one patient we observed polycyclic margins of a lesion of low echogenicity that extended beyond the gastric wall. In 2 patients, the pyloric canal was patent and in one case, its lumen was narrow. The size of the lesions ranged from 63 × 56 to 94 × 101 mm. Gastroscopy, which was conducted in these patients, confirmed the presence of an infiltration in the gastric wall. In a histopathological examination of the collected samples, Burkitt's lymphoma was diagnosed in 2 patients and MALT lymphoma in one patient. The urease test for Helicobacter pylori was negative in all discussed cases.

Fig. 1.

US examination, epigastric region. A low echogenicity mass originating from the gastric wall. The hyperechoic reflection corresponds to constricted gastric lumen

Fig. 2.

US examination, right iliac fossa. Thickened wall of the terminal ileum with low echogenicity. Intestinal dilation

Fig. 3.

US examination, right lumbar region. A low echogenicity tissue area with calcifications – a lymph node affected by lymphoma

In 12 patients with a diagnosed Burkitt's non-Hodgkin lymphoma in an extragastric localization, differences in the morphology of the lesions were observed in US images and the patients were thus divided into three groups:

• Group I – in 2 patients (17%), a “target” pattern was observed in US images in the subhepatic region, which is characteristic of ileocecal intussusception; in the center, the intussusception had low echogenicity and the lymph nodes were round.

• Group II – in 8 patients (66%), US examination revealed well-circumscribed areas of low echogenicity that were connected to the adjacent intestinal loops. In one patient, the lesion was extensive and reached the hepatic hilum, which caused bile duct dilation. In all patients, the intestinal wall was 9–23 mm thick, presented low echogenicity and lacked any layered structure. One patient manifested a dilated intestinal lumen and in all remaining cases, the lumen was narrow but did not cause obstruction. In 4 patients, power Doppler demonstrated the rich vascularity of the altered intestinal wall.

• Group III – in 2 patients (17%), US examination revealed numerous lymph nodes in the epigastric and umbilical regions, ranging in size from 8–21 mm, with low echogenicity and without a vascular hilum.

Additionally, in 2 patients, fluid was present between the intestinal loops and in the vesicorectal space. Moreover, colon polyps were observed in the girl and confirmed by colonoscopy.

The final diagnosis was established on the basis of a histopathological examination of the sample collected intraoperatively in 8 patients and during gastroscopy in 3 patients. In a further 3 cases, a diagnosis was made based on the clinical picture and changes in the bone marrow.

Five patients with lesions in the ileocecal region qualified for surgical treatment due to acute stomach. Hemicolectomy was conducted in 4 cases and a stoma was performed in one patient.

The patients underwent chemotherapy according to the protocols appropriate for each type of lesion.

In 2 cases, the process was disseminated at the time of admission to hospital. The bone marrow and nervous system were involved. These patients died before the end of therapy.

The remaining patients completed the treatment. The disease is currently in remission and these patients are undergoing periodic follow-up examinations.

Discussion

Malignant non-Hodgkin lymphomas constitute a diverse group of neoplasms of the lymphatic system. In children, the abdominal form is dominant, i.e. Burkitt's lymphoma, with the tendency to occur in the ileocecal region in 25–50% of cases^{(1, 2)}. Neoplasms of this type are highly malignant; they may double their mass within 24 hours⁽⁸⁾. Due to their non-specific clinical and radiological signs, the diagnosis of gastrointestinal lymphomas in children is difficult. This is because the common and most frequent abdominal symptoms, such as abdominal pain, loss of appetite, flatulence, diarrhea, constipation, hepato- and splenomegaly, are usually associated with infectious diseases (e.g. appendicitis) rather than oncological causes⁽⁴⁾. The process of conducting abdominal US examinations in frequently agitated children may also be challenging and may result in overlooking lesions in the intestinal loops. Such an assessment, however, is essential since the gastrointestinal tract, and the ileocecal region in particular, is the most common localization of extranodal non-Hodgkin lymphomas. During the examination, one should assess the thickness of the intestinal wall, the presence or absence of the layered wall structure and the degree of intestinal dilation⁽⁷⁾. Such a manifestation of lymphoma was observed in 5 patients in our study. Depending on the degree of wall thickening and exophytic proliferation, lesions may narrow the lumen of the gastrointestinal tract (to various degrees) or cause its compression, leading to obstruction. In the case of circular wall thickening, however, the presence or even the dilation of the intestinal lumen is apparent. In certain patients, the first sign of lymphoma may be ileocecal intussusception with tumor acting as its front^{(9, 10)}. In our patients, lymphoma caused ileocecal intussusception in 3 cases. Intestinal intussusception frequently occurs in young children and is called “spontaneous intussusception” and is associated with peristalsis, elongation of the intestinal mesentery or lymph node enlargement. In older children, intussusception may be caused by the presence of pathological lesions, such as lymphoma, or intestinal polyps. In one girl of the analyzed group who was diagnosed with lymphoma, numerous polyps of the large bowel were also observed and confirmed endoscopically.

Conclusions

Persisting non-specific abdominal pain in children requires differential diagnosis between inflammatory and neoplastic diseases. In each child with abdominal symptoms, abdominal US examination is the first test, and provides physicians with information that is valuable in the diagnostic and therapeutic process. The application of high-frequency transducers enables the assessment of the gastrointestinal wall, the degree and extent of its thickening, and whether or not the lymph nodes are enlarged. A thorough US assessment of all abdominal organs conducted using convex and linear probes increases the chances of establishing an adequate diagnosis.

Conflict of interest

The authors do not report any financial or personal links with other persons or organizations, which might affect negatively the content of this publication and/or claim authorship rights to this publication.