DOI: 10.1148/rg.275065157
RadioGraphics 2007;27:1335-1354
© RSNA, 2007
Multimodality Imaging of Hodgkin Disease and Non-Hodgkin Lymphomas in Children1
Paolo Toma, MD,
Claudio Granata, MD,
Andrea Rossi, MD, and
Alberto Garaventa, MD
1 From the Departments of Radiology (P.T., C.G.), Neuroradiology (A.R.), and Oncology (A.G.), Giannina Gaslini Children’s Hospital, Largo Gaslini 5, 16147 Genoa, Italy. Presented as an education exhibit at the 2005 RSNA Annual Meeting. Received August 24, 2006; revision requested November 14 and received February 28, 2007; accepted March 26. All authors have no financial relationships to disclose.
Address correspondence to C.G. (e-mail: cgranata{at}sirm.org).
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Abstract
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Lymphomas account for 10%–15% of all childhood cancers and include a number of different pathologic subtypes, which arise from the constituent cells of the immune system or from their precursors. All organ systems may be involved at some stage of the disease, including the central nervous system, head and neck, thorax, abdomen, gonads, and bone. However, at onset, nodal and splenic involvement are more common in Hodgkin disease, whereas extranodal involvement is more frequent in non-Hodgkin lymphomas. Diagnostic imaging modalities have a fundamental role in the staging of lymphomas and, owing to major advances during the past two decades, make surgical staging unnecessary in most cases. Conventional, sonographic, and cross-sectional imaging techniques are excellent tools for evaluating the extent and sites of disease in childhood lymphomas. Familiarity with the spectrum of imaging findings in lymphomas is essential for radiologists to enable them to provide guidance for the treating physicians.
© RSNA, 2007
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LEARNING OBJECTIVES FOR TEST 3
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After reading this article and taking the test, the reader will be able to:- Describe the typical features of HD and NHL at conventional, sonographic, and cross-sectional imaging in each anatomic subsection.
- Discuss the current status of imaging in the assessment of HD and NHL.
- Identify the imaging features that may be useful in differentiating HD from NHL.
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Introduction
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Lymphomas arise from the constituent cells of the immune system or from their precursors and are the consequence of genetic aberrations that impair proliferation, differentiation, and ability to undergo apoptosis of lymphatic cells. Hodgkin disease (HD) and non-Hodgkin lymphomas (NHLs) constitute 10%–15% of all childhood cancers in developed countries and are third in frequency after acute leukemias and brain tumors (1).
The purpose of the article is to familiarize the reader—after a brief review of the pertinent clinical features of these conditions—with the spectrum of imaging findings obtained with conventional, ultrasonographic (US), and cross-sectional techniques. Those findings are discussed in detail for each anatomic subsection, including the central nervous system (CNS), head and neck, thorax, abdomen, gonads, and bone, and the role of diagnostic imaging in diagnosis, staging, and monitoring of HD and NHLs is highlighted.
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Clinical Considerations
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Epidemiologic Features
HD has a bimodal age distribution: In developed countries the first peak occurs in the middle to late 20s and the second peak after the age of 50 years, whereas in developing countries the early peak occurs before adolescence. HD is very rare in children younger than 5 years. The prevalence in males and females is roughly the same (2).
The prevalence of NHLs differs greatly from country to country, being much higher in developing countries. Unlike in HD, the prevalence of NHLs increases steadily with age throughout life. NHLs are twice as frequent in male children as in females (3).
Pathologic Features
The Reed-Sternberg cell is the malignant cell in HD: Its identification, against the appropriate background of inflammatory cells and fibrosis, is required to make the diagnosis of HD. Molecular biology studies support the concept that Reed-Sternberg cells are generally activated pre-B cells (4). Four histologic subtypes of HD are described: lymphocytic predominance, mixed cellularity, lymphocytic depletion, and nodular sclerosis (5). Nodular sclerosis is the most common subtype, affecting about 60% of children, whereas the lymphocytic depletion subtype is very rare.
Historically, in both adults and children, the prognosis of the first three subtypes was correlated with the ratio of lymphocytes to abnormal cells. However, nowadays the development of highly curative treatment regimens makes all histologic subtypes of HD equally responsive to therapy.
NHLs typically arise from primitive cell lines. In children, the most common subtypes of NHL are Burkitt lymphoma (with the jaw and abdomen as the most common involved sites); Burkitt-like lymphomas and large B-cell lymphomas (with the abdomen and peripheral, intrathoracic, and intraabdominal lymph nodes as the most common sites); lymphoblastic lymphoma (with the mediastinum, lymph nodes, and bone marrow as the most common sites); anaplastic large cell lymphoma (with the lymph nodes, skin, soft tissue, and bone as the most common sites); and other peripheral T-cell lymphomas. All lymphoid neoplasms may manifest as diffuse involvement of bone marrow, thus addressing the relationship between leukemia and lymphomas. An arbitrary criterion of greater than 25% of neoplastic cells at bone marrow biopsy is required for a diagnosis of leukemia, although no biologic or prognostic significance has been defined. However, in children with lymphomas, bone marrow involvement is a sign of extensive disease rather than an indication of a different disease (6).
Clinical Features
Children with HD usually present with painless cervical or, less frequently, supraclavicular lymphadenopathy. More rarely, inguinal or axillary lymphadenopathy is the first presenting sign. The growth rate of the affected lymph nodes is often less rapid than in NHLs.
At diagnosis, at least two-thirds of affected children have some degree of mediastinal involvement, which may cause compression of the trachea and bronchi. Fatigue, weight loss, fever, pruritus, and drenching night sweats may be associated (7). Primary disease appearing in a subdiaphragmatic site is rare and occurs in about 3% of cases (8).
In children with NHLs, the clinical presentation is much more often extranodal than in adults, the most frequently involved sites being intraabdominal and intrathoracic. Acute abdomen with symptoms mimicking those of acute appendicitis is a relatively frequent presentation of NHL in children. Intussusception resulting from the intraluminal projection of a small tumoral mass is also not unusual. Laparotomy usually leads to correct diagnosis and resection of the tumor. In other cases, a rapidly growing lymphomatous mass may encroach on adjacent vital structures. In the abdomen, urinary tract obstruction, obstructive jaundice and pancreatitis, bowel obstruction, inferior vena caval compression, and gastrointestinal bleeding may be observed. Life-threatening respiratory or cardiac complications may develop as a consequence of compression of the trachea, lungs, and superior vena cava by mediastinal or pharyngeal masses or massive pleural or pericardial effusion. More rarely, paraplegia due to epidural infiltration and raised intracranial pressure by intracranial lymphoma may develop. Unlike in HD, systemic symptoms such as fever and weight loss are relatively uncommon (8).
As lymphomas can involve almost any organ in the body, the differential diagnosis is enormous. In children, it should include the majority of benign and malignant neoplastic conditions and many inflammatory disorders. Therefore, lymphoma should be considered in the differential diagnosis of any puzzling lesion.
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Diagnostic Imaging Work-up
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Histologic analysis remains the primary mode of definitive diagnosis for a patient with suspected lymphoma. Once the diagnosis of lymphoma is made, the extent and sites of disease must be determined to assess prognosis and to plan therapy.
US has a definite role in both initial evaluation and follow-up of involvement of superficial lymph nodes, and it is also the best method to detect testicular infiltration (9). US may also yield useful information about the possible involvement of bowel loops, abdominal nodes, and parenchymatous organs. However, US examination may be affected by the patient’s obesity or bowel meteorism and cannot replace a cross-sectional study of the abdomen for staging purposes.
Chest radiography provides preliminary information about involvement of the mediastinum and lungs. Computed tomography (CT) allows detailed evaluation of the mediastinum, chest wall, pulmonary parenchyma, and pleura or pericardium. Contrast-enhanced chest CT is always recommended, as up to 50% of previously untreated patients may have disease discovered with CT that had been missed with plain radiography (10).
CT of the neck should be performed in any patient with cervical node involvement in order to better evaluate the Waldeyer ring (11).
Abdominal CT is effective in detecting enlarged abdominal and pelvic nodes and involvement of the liver, spleen, kidneys, mesentery, and peritoneum. Unlike US, it is not affected by bowel gas interference; however, the lack of retroperitoneal fat in children may make it more difficult to evaluate the extent of abdominal and pelvic disease. It requires administration, if possible, of both oral and intravenous contrast media to accurately distinguish lymphadenopathy from other infradiaphragmatic structures.
Magnetic resonance (MR) imaging is particularly useful for evaluating the CNS. However, CNS involvement is very rare at disease presentation in children; therefore, it is generally not included as part of a standard staging system unless symptoms or signs suggest CNS disease.
A technetium 99m bone scan for assessment of skeletal metastases should be recommended only in children with bone pain and elevated alkaline phosphatase concentration, and it should be associated with corresponding plain radiographs of abnormal areas (8).
Gallium 67 scanning may provide a useful whole-body screen as both diagnostic and monitoring modality, especially in HD, Burkitt lymphoma, and Burkitt-like lymphoma, which avidly take up the isotope (12). Whole-body 67Ga imaging is 95% sensitive in detecting lymphoma and 98% sensitive in detecting its recurrence (13). However, this modality does not allow differentiation of inflammatory from lymphomatous lesions, and normal thymus may take up the isotope as well. False positives in children have been observed in up to 43% of cases (14).
Fluorodeoxyglucose (FDG) positron emission tomography (PET) has a proved role for HD in adults (15). In HD, it is important to detect all sites initially involved by the disease at presentation to correctly plan radiation therapy and thus maximize cure rates. PET results modify disease stage in a percentage of patients in comparison with CT and/or MR imaging alone, and PET is currently used in children with HD, although to date no prospective studies have demonstrated that its use improves outcome. However, in the follow-up of children with HD after chemotherapy completion, FDG PET could play a major role in determining the indication for radiation therapy. Preliminary results in children show that use of an FDG PET–based stratification—in addition to the established CT and MR imaging evaluation—could dramatically increase the number of nonirradiated patients owing to the capability of FDG PET to allow differentiation between benign residual masses and active disease (16).
In childhood NHLs, where high cure rates result from risk-adapted chemotherapy without radiation therapy, it is superfluous to detect every site of small-bulk disease. Therefore, routine use of FDG PET is unnecessary in staging NHLs in children. In these patients, however, FDG PET may be useful to assess the speed of response and to confirm posttherapy remission (17). Speediness in achieving complete remission with treatment might define a better-prognostic subgroup in which therapy could be reduced. In both HD and NHLs, a residual mass at CT or MR imaging may suggest persisting disease. FDG PET may be used in children to differentiate active residual disease from nonpathologic tissue (18). However, FDG avidity related to other nonmalignant conditions may on occasion confound interpretation of tumor response. Transient FDG avidity can be observed in the spine, pelvis, long bones, and spleen of patients treated with growth factor support and in patients recovering from an infection or inflammatory process (19).
Table 1 summarizes the recommended steps in the diagnostic imaging work-up of children with lymphoma.
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Staging
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Staging systems for childhood lymphomas were designed to identify patients who belong in different prognostic risk categories and to determine optimal therapy.
In HD, the Ann Arbor staging system is based on the observation that the disease spreads along contiguous lymph nodes until late in the course of the disease (Table 2) (20).
In the 1970s, laparotomy with splenectomy was mandatory for staging assessment. Since the late 1990s, the increasing use of systemic therapy and the advances in diagnostic imaging technologies have made it possible to avoid surgical staging.
The St Jude staging system is the scheme adopted for NHLs (Table 3) (6). It is applicable to all histologic subtypes and differentiates patients with low-stage disease from those with extensive intrathoracic or intraabdominal disease. However, NHLs are often disseminated (at least microscopically) at the time of initial disease presentation, and this makes staging less useful (21). Furthermore, with the evolution of more intensive therapeutic protocols, it was increasingly clear that this staging system had become less effective in assessing prognosis (18). At present, probably there is no way other than initial response to therapy to identify patients destined to relapse or die of the disease, although the risk of relapse and death is also correlated with tumor burden (6).
The CNS, head and neck, thorax, abdomen, gonads, and bone may be affected by both HD and NHLs, although with different prevalence. Table 4 summarizes the usually involved sites in children and the relative prevalence of involvement.
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Central Nervous System
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Primary involvement of the CNS by lymphoma occurs almost exclusively with NHLs and is uncommon in children. It may manifest as cranial nerve palsy or spinal cord compression. Unlike in adults, primary cerebral lymphomas manifesting as discrete masses or infiltrations involving the corpus callosum are very rare in the pediatric age group (22). Uncommon intracranial locations include the pituitary stalk, in which case affected children present with central diabetes insipidus and growth hormone deficit. At MR imaging, a relative decrease in signal intensity on both T1-weighted and T2-weighted images probably reflects hypercellularity (23).
Meningeal infiltration can also be seen (Fig 1). Subarachnoid nodules, diffuse leptomeningeal carcinomatosis, or both can be seen on postcontrast MR images (23).
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Figure 1. NHL of the neck in a 4-year-old boy. Coronal contrast-enhanced T1-weighted MR image shows a large laterocervical mass (M) involving the parapharyngeal space. Infiltration of the left cavernous sinus (arrow) and dural involvement with intracranial extension are evident. (Reprinted, with permission, from (23).
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Intramedullary spinal cord involvement by either HD or NHL is rare and is usually a manifestation of widespread disease (Fig 2).
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Figure 2a. HD in a 6-year-old girl. (a) Coronal T2-weighted MR image shows a left-sided paraspinal mass (arrowhead). The second, third, and fourth lumbar vertebrae and first sacral vertebra show infiltration (*). (b) Axial contrast-enhanced T1-weighted MR image shows extension into the spinal canal (arrows) and compression of the dural sac (arrowhead).
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Figure 2b. HD in a 6-year-old girl. (a) Coronal T2-weighted MR image shows a left-sided paraspinal mass (arrowhead). The second, third, and fourth lumbar vertebrae and first sacral vertebra show infiltration (*). (b) Axial contrast-enhanced T1-weighted MR image shows extension into the spinal canal (arrows) and compression of the dural sac (arrowhead).
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Head and Neck
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Jaw
The jaw is a frequent site of disease in African children with Burkitt lymphoma, whereas disease in this location is very uncommon in white patients. In African patients, the jaw is the initial site of disease in 50% of cases, and involvement often begins at the angle of the mandible. Radiography shows loss of the lamina dura and osteolysis of medullary and cortical bone, with a concomitant periosteal reaction producing lamellar and perpendicular spicules of new bone in the mandible or maxilla. An extraosseous soft-tissue mass usually develops in parallel with bone destruction (11).
Paranasal Sinuses
The paranasal sinuses are very rarely involved in children. At CT or MR imaging, lymphomatous infiltration appears as a nonspecific soft-tissue mass partially or completely obscuring the involved lumen. Destruction of the surrounding bone may be associated.
Waldeyer Ring
The Waldeyer ring comprises a network of lymphoid tissue in the nasopharynx, base of the tongue, and tonsils including the soft palate. Involvement of the Waldeyer ring is rather rare in children and is more frequently observed in large B-cell NHL, whereas HD very rarely involves the Waldeyer ring. The lymphomatous mass may involve all sites of the Waldeyer ring or may be localized in one site, most commonly the faucial tonsils, followed by the nasopharynx and the base of the tongue (Fig 3). At CT, it appears as an isoattenuating to muscle, homogeneous, submucosal mass most often associated with enlarged lymph nodes in the neck. At MR imaging, the lymphomatous mass usually has low signal intensity on T1-weighted images and intermediate signal intensity on T2-weighted images (11).
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Figure 3. Burkitt lymphoma of the palatine tonsils in
a 3-year-old boy. Sagittal contrast-enhanced T1-weighted MR image shows a
huge, well-defined mass (M) of the soft tissues of the
rhinopharynx that penetrates into the nasal choanae. (Reprinted, with
permission, from (23).
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Cervical Lymph Nodes
In children, the cervical nodes are the most common sites of HD manifestation. HD is typically confined to this area in up to 80% of cases. In contrast, NHL manifesting as cervical adenopathy is frequently more widespread (6). In lymphomas, involved lymph nodes are enlarged and painless. The nodal groups in the upper neck, especially the internal jugular and spinal accessory nodes, are more commonly enlarged than those in the lower neck.
However, enlargement of the cervical lymph nodes is a very common finding in children and, in most cases, is a benign, reactive condition secondary to inflammatory processes in the lymphoid tissue of the nasopharynx and tonsils. US is probably the imaging technique best suited to studying enlarged superficial lymph nodes. Several US features have been described for differentiating reactive lymphadenopathy from lymphomatous involvement. Enlargement, round shape, absent or eccentric hilum, hypoechoic parenchyma, absence of calcifications, tendency to aggregate into a mass, and distorted branching and amputation of nodal vascularization are US characteristics that can often be observed in lymphomatous nodes (Figs 4, 5) (24). However, not rarely and especially in children, similar findings may also be observed in reactive, benign lymph nodes, thus making differential diagnosis very difficult. Therefore, in the presence of dubious findings, only biopsy makes diagnosis possible (25).
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Figure 4a. HD of the cervical lymph nodes in a 12-year-old girl. (a) US scan shows lymphomatous infiltration of a cervical lymph node, which appears enlarged, nonhomogeneous, and partially hyperechoic. (b) Three-dimensional power Doppler US scan of the same lymph node shows distorted vascular branching and vessel amputation.
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Figure 4b. HD of the cervical lymph nodes in a 12-year-old girl. (a) US scan shows lymphomatous infiltration of a cervical lymph node, which appears enlarged, nonhomogeneous, and partially hyperechoic. (b) Three-dimensional power Doppler US scan of the same lymph node shows distorted vascular branching and vessel amputation.
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Figure 5. HD of the cervical lymph nodes in a 10-year-old girl with a right lateral cervical mass. US scan shows multiple roundish, hypoechoic lymph nodes with a tendency to aggregate. The nodal hila are not visualized or appear eccentric (arrowheads).
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At CT, the involved lymph nodes may be discretely enlarged or appear as a soft-tissue mass. Necrosis in lymphomatous nodes is very rare both before and after treatment and appears as central areas of lower attenuation. Intravenous contrast enhancement greatly facilitates distinction of vessels from the adjacent lymph nodes and detection of solid organ involvement. Similarly to US, CT may show findings similar to those of inflammatory adenopathy, and tissue sampling is often required for diagnosis (25).
At MR imaging, lymph nodes show low to intermediate signal intensity on T1-weighted images and intermediate to high signal intensity on T2-weighted images. The multiplanar capability and superb soft-tissue contrast resolution of MR imaging make it an excellent modality for assessing both nodal and extranodal disease in the neck region. MR imaging is also valuable for assessing lower cervical nodes near the clavicles, where beam-hardening artifacts at CT often obscure the complex anatomy (26).
Salivary Glands
All salivary glands can be affected by lymphoma, although in children this is a very rare event. The most frequently involved gland is the parotid (Fig 6). Salivary gland lymphoma is almost invariably secondary to diffuse disease. Lymphoma of the parotid gland lymph nodes has the nonspecific appearance of a single mass or multiple masses, and the gland may be displaced (26).
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Figure 6a. NHL in a 10-year-old girl. (a) US scan of the right parotid gland shows infiltration, which appears as an ill-defined, nonhomogeneous hypoechoic area (arrowheads). (b) Coronal T1-weighted MR image shows that the infiltrated gland (M) is isointense relative to the neck muscles.
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Figure 6b. NHL in a 10-year-old girl. (a) US scan of the right parotid gland shows infiltration, which appears as an ill-defined, nonhomogeneous hypoechoic area (arrowheads). (b) Coronal T1-weighted MR image shows that the infiltrated gland (M) is isointense relative to the neck muscles.
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Chest
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Involvement of the chest is a common finding in children with HD or NHLs. Mediastinal enlargement, hilar lymphadenopathy, and involvement of the pulmonary parenchyma, chest wall, pleura, and pericardium may be observed.
Mediastinum
In children with NHLs, the anterior mediastinum is the second most likely primary site. In children with HD, anterior mediastinal involvement is more often associated with the nodular sclerosis subtype. At CT, the typical finding is a hypoattenuating, nonhomogeneous, lobulated mediastinal mass (Fig 7). In NHL, the mass is mainly thymic in origin, whereas in HD thymic involvement is associated with hilar lymphadenopathy in most cases. Hilar lymphadenopathy occurs more frequently in HD than in NHL and is usually bilateral (27).
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Figure 7. HD in a 17-year-old boy. Contrast-enhanced CT scan obtained at diagnosis shows a large mediastinal mass (M) that extends to the right pulmonary apex and the right side. The trachea (T) is compressed, and the great vessels (arrowheads) are displaced.
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In children, the size and shape of the normal thymus are quite variable. During the first decade of life, the thymus demonstrates mildly convex lateral borders and homogeneous attenuation at CT. After puberty, the thymus becomes triangular with concave margins and the attenuation may become slightly nonhomogeneous because of fatty infiltration (28). The normal thymus does not cause mass effect. Occasionally, the thymus may be large enough to cause mild mass effect on adjacent structures, although in such a situation follow-up imaging is advisable to rule out early lymphoma (29). A diseased thymus appears enlarged, nodular, and lobulated and may distort and clearly displace the adjacent structures; superior vena caval and airway compression are well-recognized problems in NHLs, whereas they are unusual in HD. At CT, a lymphomatous thymus frequently appears grossly nonhomogeneous, with internal areas of low attenuation that correspond to areas of necrosis and cyst formation (Fig 8). Calcifications can also be seen (Fig 9).
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Figure 8. NHL in a 14-year-old boy. Contrast-enhanced CT scan obtained at diagnosis shows a large anterior mediastinal mass (M) that originates from the thymus. A few cysts with central low attenuation and a peripheral enhancing ring are present (arrowheads).
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Figure 9. NHL in a 13-year-old boy. Contrast-enhanced CT scan obtained at diagnosis shows a large anterior mediastinal mass (M) that originates from the thymus. A cluster of calcifications is present (arrowheads).
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Children with HD and "bulky" mediastinal disease do worse than patients with a reduced tumor volume. Historically, bulky disease was defined at chest radiography as a ratio of maximum tumor diameter to chest diameter at the level of the diaphragmatic dome of greater than one-third (30). Although CT can more accurately show tumor burden (31), this historical criterion persists.
Tumor bulk does not appear to influence outcome in children with NHLs (18).
Lung
In HD, the prevalence of pulmonary involvement in patients of all ages is 5%–10% at the time of diagnosis, usually in association with hilar or mediastinal lymphadenopathy (32). In adults, pulmonary involvement is found in 50%–90% of cases with the nodular sclerosis subtype of HD and in only 5%–15% of cases with other histologic subtypes (33). The presence of pulmonary disease is characteristic of stage IV disease and significantly alters prognosis and therapy.
In NHLs, lung involvement at the time of diagnosis is observed in less than 5% of cases and may occur without concomitant hilar or mediastinal disease (32). In both HD and NHLs, the most common mechanisms of disease spreading into the lungs are hematogenous and lymphangitic dissemination and less frequently direct invasion (34).
At imaging, three patterns of lung infiltration may be observed in children. The first pattern—the most common—is the presence of single or multiple pulmonary nodules with irregular borders and sometimes central cavitation. The second pattern is a reticular interstitial pattern of infiltration, which results from venous or lymphatic obstruction caused by hilar or mediastinal adenopathy or from interstitial tumor deposition. The third pattern is lobar or segmental consolidation, which may mimic that of pneumonia (32). These patterns may also be found in association (Figs 10–12).
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Figure 10. HD in a 10-year-old boy. CT scan obtained below the carina shows multiple nodular lesions and interstitial thickening in both lungs. Enlarged hilar lymph nodes (LN) are present.
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Figure 11. HD in a 12-year-old boy. CT scan obtained through the bases of the lungs shows a large infiltrate (solid arrow) with a cavitary lesion (open arrow) in the right lower lobe. Small nodules (arrowheads) are present in the left lower lobe.
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Figure 12. HD in a 10-year-old boy. CT scan obtained at diagnosis shows consolidation (arrow) of the anterior basal segment of the right lower lobe and the lateral segment of the right middle lobe, a finding that mimics pneumonia.
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Pleural effusion may also be observed and is sometimes large enough to cause mediastinal shift and pulmonary atelectasis. The effusion typically results from lymphatic obstruction (34).
Residual Mediastinal Mass, Thymic Rebound, and Recurrent Mediastinal Disease
Disease response is characteristically associated with a decrease in size of the mediastinal mass and a decrease in lymphadenopathy. In the most recently completed treatment protocols, the definition of complete response in children was a decrease in tumor volume by at least 70% and the absence of residual gallium uptake (30).
In children with HD, a residual mediastinal mass may be present in as many as 88% of patients after completion of therapy; it is usually benign and is typically composed of areas of necrosis, fibrosis, and inflammation. A residual mass is most often associated with the nodular sclerosis subtype of HD because of its abundant fibrotic component (14). Residual mediastinal enlargement may also occur in NHL, although more rarely (35). However, a recurrent mediastinal mass raises concern about the possibility of recurrent disease.
In HD, recurrent enlargement of the thymus—the so-called thymic rebound—is typically observed within 6–12 months after suspension of therapy in 25% of affected children, although it can occur as soon as 1 week after completion of therapy (36). Thymic rebound is due to lymphatics undergoing a reactive hyperplasia in response to withdrawal of myelosuppressive therapy and is usually self-limiting and reversible. However, 67Ga uptake may persist in children with thymic rebound for up to 60 months (37). In dubious cases, functional imaging with FDG PET may play a critical role in evaluation of tumor response. Regression or resolution of metabolic tumor activity as determined with FDG PET may serve to distinguish active residual tumor from nonpathologic tissue. Although false-positive results may occur with FDG PET as well, this technique may be used in children to guide the choice between performance of biopsy and a wait-and-see policy (16,18).
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Abdomen
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Gastrointestinal Tract
The gastrointestinal tract is the most common site of manifestation of NHLs in children. The stomach (Fig 13) and duodenum (Fig 14) are very rarely involved, whereas the distal ileum, cecum, appendix, and ascending colon are the most frequently involved sites (38). The tumor usually spreads circumferentially throughout the intestinal submucosa, progressively infiltrating the bowel wall. Multifocal involvement is not uncommon. The lumen may be narrowed or dilated because of mucosal infiltration and excavation, with an aneurysmal aspect due to replacement of the muscular layers by tumor spread. Intussusception may be a complication of lymphoma.
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Figure 14. NHL in a 12-year-old boy. Radiograph from a barium meal study shows narrowing and distortion of the first portion of the duodenum (arrow) as a result of lymphomatous infiltration.
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At US, lymphomatous involvement of the bowel produces severe and hypoechoic bowel wall thickening with loss of stratification (Fig 15a) or a focal hypoechoic or complex mass with large anechoic areas secondary to necrosis (39). At CT, common findings are marked bowel wall thickening in a focal or diffuse distribution with mesenteric lymphadenopathies. The infiltrated bowel wall usually demonstrates soft-tissue attenuation with minimal enhancement (40) (Fig 15b).
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Figure 15a. NHL in a 14-year-old boy. (a) US scan of an infiltrated small bowel loop shows severe thickening, loss of stratification, hyperemia, and aneurysmal dilatation. (b) Contrast-enhanced CT scan shows conglomeration of the bowel, mesentery, and mesenteric vessels into a huge lymphomatous mass. Aneurysmal dilatation of a bowel loop (arrowhead) is also seen.
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Figure 15b. NHL in a 14-year-old boy. (a) US scan of an infiltrated small bowel loop shows severe thickening, loss of stratification, hyperemia, and aneurysmal dilatation. (b) Contrast-enhanced CT scan shows conglomeration of the bowel, mesentery, and mesenteric vessels into a huge lymphomatous mass. Aneurysmal dilatation of a bowel loop (arrowhead) is also seen.
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Bowel wall thickening is also observed in children with Crohn disease. However, the US features of bowel thickening observed in Crohn disease are usually different, as loss of stratification is usually a late finding and the thickness of the involved bowel segment is usually less significant than that observed in cases of lymphomatous infiltration. Furthermore, unlike in lymphomatous involvement, in which the lumen of the affected segment may be stenotic or dilated, in Crohn disease fibrotic changes of the bowel wall usually cause stenosis only.
Mesenteric and Retroperitoneal Lymph Nodes
Lymphomatous involvement of retroperitoneal lymph nodes, individually or in groups, can be found in children with HD. It may also be observed in children with NHLs, particularly in association with primaries in the small bowel. Nodal involvement and extranodal extension may produce loss of definition of individual nodes within a confluent mass. A single central mass may be found along the abdominal great vessels, retroperitoneum, and mesentery. Alternatively, relatively symmetrical bilateral masses may be observed in the prevertebral area.
Further progression of the disease may form a confluent mass crossing the prevertebral area and encompassing the paravertebral regions from side to side. The aorta and inferior vena cava may be completely encased and displaced with possible impairment of venous circulation in the lower limbs. Encasement of the root of the mesentery and the superior mesenteric artery by a lymphomatous mass originating from multiple enlarged and confluent lymph nodes may produce the so-called "sandwich sign," which is demonstrable with both US and CT (Fig 16) (41). The ureters and kidneys may also be displaced or encased with possible obstructive uropathy (Fig 17) (42).
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Figure 16a. NHL in an 11-year-old boy. (a) US scan shows encasement of the mesenteric vessels by a lymphomatous mass that originates from multiple enlarged and confluent lymph nodes (the sandwich sign) (arrowheads). The splenic vein (arrow) is in close contact with the mass. (b) Contrast-enhanced CT scan shows the large lymphomatous mass (M) encasing the mesenteric vessels (arrow).
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Figure 16b. NHL in an 11-year-old boy. (a) US scan shows encasement of the mesenteric vessels by a lymphomatous mass that originates from multiple enlarged and confluent lymph nodes (the sandwich sign) (arrowheads). The splenic vein (arrow) is in close contact with the mass. (b) Contrast-enhanced CT scan shows the large lymphomatous mass (M) encasing the mesenteric vessels (arrow).
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Spleen
In patients of all ages, splenic involvement in HD is present in about 35% of cases, whereas in NHL it is present in about 15% of cases. Lymphomatous involvement of the spleen can cause diffuse splenic infiltration resulting in splenomegaly or can appear as solitary or multiple nodules. The affected spleen may also not be enlarged, and conversely—although rarely—it may manifest as mild to moderate splenomegaly without lymphomatous involvement. Associated lymphadenopathy may be noted in the splenic hilum (43). In general, however, the overall accuracy of all imaging modalities in disease detection is low, especially in cases of diffuse infiltration.
At US, splenic involvement may appear as homogeneous splenomegaly or as solitary or multiple nodular masses, which are usually hypoechoic with respect to normal splenic parenchyma (44); CT findings range from splenic enlargement alone to solitary or multiple nonenhancing, low-attenuation masses (Fig 18). Calcifications have also been reported (45). CT is probably better than US for detection of splenic disease, although the overall sensitivity is about 40% (46). The yield of MR imaging is similar to that of CT. Lymphomatous infiltration has T1 and T2 relaxation times similar to those of normal splenic parenchyma (47). However, on T2-weighted images, infiltration may have a spotted appearance caused by the presence of associated fibrosis, hemorrhage, edema, or necrosis (48). In the absence of these features, splenic involvement may be very difficult to identify. Nevertheless, despite the low accuracy of these imaging modalities, staging laparotomy is not needed in most cases owing to the use of systemic therapy.
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Figure 18a. HD in a 12-year-old girl. (a) US scan shows splenic infiltration, which has a diffusely nonhomogeneous appearance with small hypoechoic nodules. (b) Contrast-enhanced CT scan shows an enlarged spleen with a diffusely nonhomogeneous appearance.
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Figure 18b. HD in a 12-year-old girl. (a) US scan shows splenic infiltration, which has a diffusely nonhomogeneous appearance with small hypoechoic nodules. (b) Contrast-enhanced CT scan shows an enlarged spleen with a diffusely nonhomogeneous appearance.
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Liver
In both adults and children, the liver is rarely involved without associated involvement of the spleen. Lymphomatous involvement is more often secondary to NHLs than to HD. Hepatic infiltration is most commonly in the form of diffuse infiltration, although nodular disease may also be observed. Not unlike in splenic involvement, hepatomegaly alone is a nonspecific finding: about 50% of patients with hepatomegaly have no histologic evidence of lymphoma, whereas patients with normal-sized livers can have extensive lymphomatous infiltration. CT findings are similar to those in the spleen (26). US findings include discrete hypoechoic or anechoic nodules and hepatomegaly (Fig 19) (49). However, the accuracy of all imaging modalities in detection of liver disease is low, not unlike that observed in the spleen.
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Figure 19a. NHL in a 16-year-old girl. (a) US scan shows a large hypoechoic nodule (M) in the right hepatic lobe. K = kidney, L = liver. (b) Contrast-enhanced CT scan shows low-attenuation nodular lesions (arrowheads). A few discrete lesions are evident in both hepatic lobes, with small nodules in the spleen and right kidney.
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Figure 19b. NHL in a 16-year-old girl. (a) US scan shows a large hypoechoic nodule (M) in the right hepatic lobe. K = kidney, L = liver. (b) Contrast-enhanced CT scan shows low-attenuation nodular lesions (arrowheads). A few discrete lesions are evident in both hepatic lobes, with small nodules in the spleen and right kidney.
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Pancreas
Pancreatic involvement in childhood lymphoma is unusual. It may occur with widely disseminated preterminal disease. Diffuse enlargement of the entire gland has been reported, which may be due to direct infiltration. Occasionally, peripancreatic retroperitoneal lymph nodes may enlarge and invade or distort the pancreas. At US, pancreatic infiltration may appear as focal or diffuse hypoechoic areas of enlargement (Fig 20) (50).
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Figure 20. NHL in a 16-year-old boy with disseminated preterminal disease. On a US scan, parts of the pancreatic body and tail are enlarged and hypoechoic (arrowheads) owing to lymphomatous infiltration.
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Peritoneum and Omentum
Peritoneal and omental involvement is not very frequent in children and is most often associated with extensive bowel or mesenteric infiltration or with disseminated lymphoma. At US, the areas of involvement may appear relatively hypoechoic (Fig 21). At CT, the areas of involvement may appear as soft-tissue masses: the so-called omental cakes lying between the bowel and the abdominal wall (44,51). Ascites is frequently observed.
Kidney
The kidney is almost always a secondary location for disease, as only 3% of renal lymphomas are primary in patients of all ages. Renal infiltration is often present in terminal phases of NHL. In children, Burkitt lymphoma has the highest frequency of infiltration of the kidneys. Renal involvement is very rare in HD. Three patterns of infiltration are known: bilateral multiple small nodules (60%–70%), a solitary mass (10%–20%), and diffuse infiltration (5%–10%). Hematogenous dissemination is the most common source of renal lymphoma, although infiltration from adjacent lymph nodes is another relatively common form of involvement (10%–20%) (52).
At US, lymphomatous renal masses appear in the form of homogeneous and hypoechoic or anechoic nodules, which may distort the normal intrarenal architecture (Fig 22). Hyperechoic nodules can be observed very rarely. Anechoic lesions can simulate renal cysts, but in most instances the absence of distal enhancement should suggest that the mass is solid (52).
At CT, intrarenal lymphoma is hypoattenuating with respect to the surrounding renal parenchyma and shows minimal enhancement (Figs 23, 24). Focal lower attenuation representing necrosis or hemorrhage may also be seen in larger lesions (53).
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Gonads
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Primary involvement of testes or ovaries by NHL may rarely occur in children; genital involvement is more likely a component of widely disseminated disease. NHL of the ovary may be a source of pelvic retroperitoneal masses completely engulfing the internal female genitalia. Testicular involvement may manifest as enlargement of the testes and may also be associated with retroperitoneal lymphadenopathy.
At US, lymphoma of the ovary may appear as a discrete hypoechoic mass or a large confluent aggregate mass that may fill the pelvis. CT may reveal low-attenuation solid masses involving the uterus or confluent masses displacing or engulfing the pelvic organs (54).
US of a testicular lymphoma may reveal diffuse replacement by a relatively hypoechoic process; discrete hypoechoic nodules may also be seen. The mediastinum testis may be obscured. Hyperemia is often observed (Fig 25) (55). Retroperitoneal lymphadenopathy is well evaluated with CT.
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Figure 25a. NHL in a 14-year-old boy. (a) US scan shows an enlarged testis with diffuse and nonhomogeneous lymphomatous infiltration. The mediastinum testis is not visualized. (b) Color Doppler US scan shows intense hyperemia of the testis.
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Figure 25b. NHL in a 14-year-old boy. (a) US scan shows an enlarged testis with diffuse and nonhomogeneous lymphomatous infiltration. The mediastinum testis is not visualized. (b) Color Doppler US scan shows intense hyperemia of the testis.
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Bone
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Lymphomas may involve the bone marrow or the cortical bone. At disease presentation in children, bone marrow involvement is very rare in HD, whereas it is more frequent in NHLs (6). Conventional imaging is not sensitive for bone marrow involvement, whereas MR imaging is extremely sensitive. Bone marrow infiltration appears as low signal intensity on T1-weighted images and high signal intensity on T2-weighted images and enhances with gadolinium chelates.
HD infiltrates the bone by direct extension; thus, the thoracic and lumbar spines are most frequently affected (Fig 2a). Unlike in NHLs, HD may be more often sclerotic or mixed sclerotic and lytic. Primary cortical bone infiltration is almost always caused by NHLs, with a permeative osteolytic pattern in about 75% of cases (Fig 26). Primary NHLs most frequently involve the appendicular skeleton, in particular the metaphysis of the femur, humerus (Fig 27), or tibia, whereas secondary bone lymphoma more frequently involves the spine (26).
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Figure 26a. NHL at onset in an 11-year-old boy. (a) CT scan shows thickening of cortical bone in the right ilium with irregular periosteal and endosteal reaction (arrowheads). (b) Axial contrast-enhanced T1-weighted MR image shows nonhomogeneity of the right iliac bone (*) with enhancement of the adjacent soft tissues (arrowheads).
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Figure 26b. NHL at onset in an 11-year-old boy. (a) CT scan shows thickening of cortical bone in the right ilium with irregular periosteal and endosteal reaction (arrowheads). (b) Axial contrast-enhanced T1-weighted MR image shows nonhomogeneity of the right iliac bone (*) with enhancement of the adjacent soft tissues (arrowheads).
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Figure 27a. NHL in an 8-year-old boy. MR images of the right humerus show diffuse involvement of the bone, a finding suggestive of malignant growth. (a) T1-weighted image shows abnormally hypointense tissue in the shaft and both metaphyses, findings suggestive of infiltration. (b, c) On T2-weighted (b) and contrast-enhanced T1-weighted (c) images, the abnormal tissue is nonhomogeneously hyperintense (* in c). There is an associated soft-tissue mass (arrowheads) growing through the periosteum.
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Figure 27b. NHL in an 8-year-old boy. MR images of the right humerus show diffuse involvement of the bone, a finding suggestive of malignant growth. (a) T1-weighted image shows abnormally hypointense tissue in the shaft and both metaphyses, findings suggestive of infiltration. (b, c) On T2-weighted (b) and contrast-enhanced T1-weighted (c) images, the abnormal tissue is nonhomogeneously hyperintense (* in c). There is an associated soft-tissue mass (arrowheads) growing through the periosteum.
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Figure 27c. NHL in an 8-year-old boy. MR images of the right humerus show diffuse involvement of the bone, a finding suggestive of malignant growth. (a) T1-weighted image shows abnormally hypointense tissue in the shaft and both metaphyses, findings suggestive of infiltration. (b, c) On T2-weighted (b) and contrast-enhanced T1-weighted (c) images, the abnormal tissue is nonhomogeneously hyperintense (* in c). There is an associated soft-tissue mass (arrowheads) growing through the periosteum.
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Conclusions
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Cross-sectional, sonographic, and conventional imaging techniques are excellent tools for evaluating the extent and site of disease in childhood lymphomas. Familiarity with the spectrum of imaging findings in lymphomas is essential for radiologists to enable them to provide guidance for the treating physicians.
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Footnotes
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Abbreviations: CNS = central nervous system, FDG = fluorodeoxyglucose, HD = Hodgkin disease, NHL = non-Hodgkin lymphoma
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D. M. Biko, S. A. Anupindi, A. Hernandez, L. Kersun, and R. Bellah
Childhood Burkitt Lymphoma: Abdominal and Pelvic Imaging Findings
Am. J. Roentgenol.,
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Abstract
LEARNING OBJECTIVES FOR TEST...
