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Pediatric Radiology

, Volume 48, Issue 9, pp 1337–1347 | Cite as

A review of neuroblastoma image-defined risk factors on magnetic resonance imaging

  • Alan M. Chen
  • Andrew T. Trout
  • Alexander J. Towbin
Pediatric Body MRI

Abstract

Neuroblastoma is the most common extracranial solid malignancy in children. Historically, neuroblastoma has been staged using the International Neuroblastoma Staging System (INSS), which relies on surgical staging. This is problematic because surgical resection can vary among surgeons and tumors and occurs at interval times from diagnosis. In 2009 the International Neuroblastoma Risk Group (INRG) created a new staging system that relies on preoperative imaging for staging. The INRG staging system consists of 20 image-defined risk factors (IDRF) across multiple organ systems, which help predict surgical outcomes/adequacy of resection and can be combined with clinical data to provide up-front risk stratification. The purpose of this review is to describe both the INSS and INRG staging systems and their limitations and to illustrate the definitions and IDRFs that comprise the INRG staging system.

Keywords

Children Image-defined risk factors Magnetic resonance imaging Neuroblastoma Oncology Staging 

Introduction

Neuroblastoma is the most common extracranial solid malignancy in children [1]. In children younger than 1 year, 50% of all tumors are neuroblastic, including ganglioneuroma, ganglioneuroblastoma and neuroblastoma. Most of these tumors are neuroblastoma, which has a median age of diagnosis of 22 months [2, 3]. Although neuroblastoma constitutes 8% of overall childhood cancers, it causes about 15% of pediatric cancer deaths [1].

Neuroblastoma is a malignant tumor composed of primitive neural crest cells with neuroblastic cells (small round blue cells) and Schwannian stromal cells [2, 3]. Although most children diagnosed with neuroblastoma have sporadic disease, some specific syndromes are associated with a higher incidence of disease, including neurofibromatosis type 1, Beckwith–Wiedemann syndrome, Hirschsprung disease, fetal hydantoin syndrome and DiGeorge syndrome [1, 3].

People diagnosed with neuroblastoma most commonly present with a painless abdominal mass [4]. Primary neuroblastoma can arise from anywhere along the sympathetic nervous system chain from neck to pelvis [5]. The most common locations of primary disease are the adrenal gland (48%), the extra-adrenal retroperitoneum (25%) and the thorax (16–20%) [6]. Because up to 70% of children have metastatic disease at the time of diagnosis, they can have other clinical symptoms. These include blue or purple marks caused by skin metastases (“blueberry muffin” syndrome), bruising around the eyes (“raccoon eyes”) caused by skull base metastases, and hepatomegaly caused by liver metastases [2, 7]. The most common site of metastatic disease is the bone and bone marrow [8, 9]. Children with bony metastatic disease can present with limping and irritability, also known as Hutchinson syndrome [3]. Neuroblastoma with metastatic disease is associated with high rate of relapse and thus a poor prognosis [1, 8, 9].

Neuroblastic tumors have variable outcomes, ranging from spontaneous resolution without therapy to death despite maximal therapy [10]. Clinical stage is the most important prognostic risk factor. Other prognostic factors include age, histological tumor grade, the presence of MYCN oncogene amplification, an aberration at the 11q allele, and tumor ploidy [10, 11, 12]. Increased copies of the MYCN oncogene and deletion of 1p and 11q alleles are associated with a worse prognosis, whereas near-triploid deoxyribonucleic acid (DNA) index is associated with a better prognosis [2].

Imaging strategies

The imaging workup for children with neuroblastic tumors varies depending on the pathway from initial clinical presentation to diagnosis [1]. Radiographs and ultrasound might be the first imaging studies performed in the setting of a palpable abdominal mass. Radiographs are often nonspecific but can show a soft-tissue mass or mass effect on bowel, occasionally with remodeling of bones. Occasionally, extremity radiographs can identify a metastasis, appearing as an aggressive lytic or permeative lesion, which prompts a search for a primary malignancy.

The primary utility of ultrasound is to determine whether a mass is truly present and, if present, the organ of origin of the mass. Ultrasound is insufficient to assess all of the image-defined risk factors and is insufficient for tumor therapy or response assessment [6].

Functional imaging with nuclear scintigraphy plays an essential role in the workup and management of neuroblastoma, particularly the detection of metastatic disease. I-123 metaiodobenzylguanidine (I-123 MIBG) is the mainstay of functional imaging of neuroblastoma and has a high sensitivity (approximately 90%) and specificity (nearly 100%) for MIBG-avid disease [8]. A small percentage of neuroblastic tumors do not uptake MIBG because of low expression of the norepinephrine transporter [13]. MIBG scintigraphy is limited by low spatial resolution, particularly of planar imaging [10, 13]. Single photon emission computed tomography (SPECT) and fusion with CT provide improved spatial resolution and better localize abnormal uptake of MIBG [13].

Imaging with 18-F fluoro-deoxyglucose positron emission tomography (18-F FDG PET) is occasionally used in the workup of neuroblastoma [9, 10]. The contribution of FDG PET in the workup of children with neuroblastoma has not been fully defined. FDG PET has higher spatial resolution than I-123 MIBG, which might be of value in detecting small lesions [9]. FDG PET also plays a role in neuroblastic tumors that weakly accumulate MIBG. The major disadvantage of FDG PET, compared to MIBG scintigraphy, is its lower tumor-to-nontumor uptake ratio, which might increase false negatives [14]. Prior studies have shown that FDG PET is superior to MIBG for soft-tissue lesions and INSS stage 1 and 2 lesions, whereas MIBG is superior for detecting bone and skull lesions [14].

Because response assessment for neuroblastoma is based on size criteria, the attenuation-correction and localization CTs typically performed as part of functional imaging exams are inadequate to fully characterize treatment response, and a diagnostic-quality contrast-enhanced CT or MRI — performed as part of the functional exam or independently — is still required.

After a tumor is confirmed to be present, further imaging with CT or MRI is needed for accurate staging and treatment planning [6]. CT has the advantages of accessibility and speed. It is considered the best modality to evaluate a thoracic tumor’s effect on the trachea or bronchi, and it is the best modality for assessing the rare parenchymal lung metastasis. On CT, neuroblastomas often heterogeneously enhance and show calcifications. In fact, 80–90% of neuroblastomas show calcifications when examined on CT [1]. Areas of low attenuation within the mass might reflect necrosis. CT can be used to assess IDRFs but might incompletely characterize spinal canal extension [4] and infiltrative metastatic disease to bone [15].

MRI has the advantage of improved soft-tissue contrast resolution and thus is optimal for evaluating spinal canal involvement [1]. However MRI has the disadvantage of requiring sedation/anesthesia in young children to avoid motion artifact during the relatively long exam. MRI is also limited in its utility for detecting small deposits of calcium. The need for gadolinium-based contrast material at diagnosis or during follow-up is controversial. Table 1 [16] summarizes our institutional protocol for evaluating neuroblastoma by MRI.
Table 1

Sample MR protocol for staging neuroblastoma

Field strength: 1.5 T or 3 T

Coils: Cardiac, body array, or phased-array spine coil (depending on patient size and coil availability)

Gadolinium dose: 0.1–0.2 mmol/kg

Sequence

Rationale

Coronal T1-weighted fast spin echo

Global view of anatomy, marrow disease assessment

Coronal T2-weighted fast spin echo

Global view of tumor extent

Axial T2-weighted fat-suppressed spin echo

Detailed evaluation of tumor extent

Axial diffusion-weighted imaging (DWI)

Problem-solving sequence with increased lesion–tissue contrast with high b values [16]

Axial pre- and post-contrast T1-weighted fast spin echo with fat saturation

Detailed evaluation of tumor enhancement characteristics, extent and metastatic disease

Coronal post-contrast T1-weighted with fat saturation

Detailed evaluation of tumor enhancement characteristics, extent and metastatic disease

The signal characteristics of neuroblastoma normally follow the expected patterns of a solid abdominal malignancy. Namely, tumors have heterogeneous, intermediate signal on T1-weighted images and heterogeneous increased signal on T2-weighted images [1]. There is variable and heterogeneous enhancement after intravenous contrast administration. Neuroblastomas show restricted diffusion because of their dense cellularity, and recent studies have suggested that diffusion-weighted imaging might be able to distinguish among neuroblastic tumor types [17, 18, 19]. Speckled or globular susceptibility artifact can be seen on gradient-echo imaging, representing calcification or blood breakdown products within the tumor.

Evolution of neuroblastoma staging

Neuroblastoma has been staged according to the International Neuroblastoma Staging System (INSS) since 1988. The INSS is based on the extent of surgical excision and is still widely used in clinical practice today [5]. However, pretreatment risk assessment and comparisons across clinical trials are difficult using this classification system, especially in children with localized disease, because it focuses solely on surgical and pathological findings [5, 20, 21].

In 2004, the International Neuroblastoma Risk Group (INRG) task force developed the INRG staging system (INRGSS) to address the need for a standardized presurgical staging system [5, 6, 11]. Used in parallel with the INSS, the INRGSS uses a consistent imaging strategy for staging children with neuroblastoma [6].

Image-defined risk factors are the backbone of the INRGSS [6]. IDRFs are features that are definable by objective and subjective imaging characteristics and are associated with a high risk of surgical complications [5, 6, 20].

The INRGSS dichotomizes the primary tumor based on the presence or absence of any image-defined risk factor [6, 21] (Table 2). A localized tumor without any IDRF is considered to be stage L1, while a local-regional tumor with any IDRF is considered to be stage L2 [6, 20]. Metastatic disease is stratified like the INSS, with children with distant metastatic disease considered to be stage M [6]. The INRGSS, like the INSS, creates a special staging category for people with metastatic disease isolated to the skin, liver or bone marrow, stage MS. The INRGSS stage MS differs from the INSS stage 4S in that children can be up to 547 days (18 months) of age instead of 12 months of age [6]. Stage MS disease has a more favorable prognosis than stage M [6].
Table 2

International Neuroblastoma Risk Group tumor stages

Tumor stage

Description

L1

Localized tumor not involving vital structures (no IDRFs) and confined to one body compartment

L2

Local-regional tumor with presence of one or more IDRFs

M

Distant metastatic disease (except stage MS tumor)

MS

Metastatic disease in a child younger than 18 months, with metastases confined to skin, liver and/or bone marrow

Reprinted from [6] with permission

IDRF image-defined risk factor, M metastasis, MS metastasis special

Imaging characteristics of image-defined risk factors (IDRFs)

It is important to define the terms used in the INRGSS because these definitions allow the radiologist to characterize the presence of IDRFs correctly. The INRG task force uses the following specific terms (summarized in Table 3):
  • Separation (Fig. 1): “visible layer of tissue, usually fat, is present between the tumor and the neighboring structure” [6]. An IDRF is not present if there is separation from a vital structure [6].

  • Contact (Fig. 2): “no visible layer is present between the tumor and the neighboring structure” [6]. Pertaining to the arteries, contact is defined as being present if less than 50% of the vessel’s circumference is enveloped by the tumor [6]. For veins, the term flattened can be used when there is decreased diameter as a result of contact with the tumor but a lumen remains partly visible. An IDRF is not present if a tumor is contacting an organ or vessels, except for renal vessels [6].

  • Encasement (Fig. 3): “the neighboring structure is surrounded by the tumor” [6]. This definition differs between an artery and a vein. For an artery, encasement is present if more than 50% of the vessel’s circumference is enveloped by the tumor, whereas for a vein, encasement is used when the lumen is no longer visible [6]. An IDRF is present when any of these qualifiers is met [6].

  • Compression (Fig. 4): “tumor is in contact with the airways and causes the short axis of the airways to be reduced” [6]. It should be noted that this term is reserved for the airways [6]. An IDRF is present when this qualifier is met.

  • Infiltration (Fig. 5): “extension into a neighboring organ, causing the margins between the tumor and the infiltrated structure to be lacking or ill defined” [6]. It should be noted that this term is reserved for non-vascular structures. An IDRF is present if the tumor causes infiltration [6].

  • Invasion (Fig. 6): This term is reserved for describing the effect of a tumor on the renal pedicle. Invasion is present if the tumor is in contact (see contact definition) with the renal artery, renal vein or renal pelvis. Studies have shown that renal invasion often requires nephrectomy or leads to segmental renal infarction as a result of surgery [22]. The risk for nephrectomy or renal infarct was twice as high in people who underwent up-front tumor resection compared to those who had neoadjuvant chemotherapy before surgical resection [22]. An IDRF is present if the tumor causes invasion [6].

Table 3

Summary of terms to describe relationships between primary tumor and vital structures, relevant to presence of image-defined risk factors (IDRFs) [6]

Term

Qualifiers

IDRF?

Separation

Visible layer of normal tissue (usually fat) between tumor and neighboring structure

No

Contact

No visible layer of normal tissue between tumor and neighboring structure

Less than 50% of vessel circumference involved

Noa

Flattened

Contact with tumor causes decreased diameter of vein but with partly visible lumen

No

Encasement

No visible layer of normal tissue between tumor and neighboring vessel

Greater than 50% of vessel circumference involved

Flattened vein with no visible lumen

Yes

Compression

Reserved for the trachea

Reduced short-axis diameter of the trachea

Yes

Infiltration

Growth of tumor into organ causing ill-defined or absent margins

Yes

Invasion

Reserved for the renal pedicle

Contact or encasement of the renal vessels

Yes

aA tumor in contact with the renal artery, renal vein or renal pelvis is said to be invading the kidney and is considered IDRF-positive

Fig. 1

Neuroblastoma in a 2-year-old boy illustrating separation. a Coronal T2-weighted MR image shows a small left suprarenal mass (arrow). There is a clear fat plane (arrowhead) separating the tumor from the spleen. b Axial T1-weighted MR image shows a larger component of the left-side mass (arrows). Again, there is a clear fat plane (arrowhead) separating the mass from the left kidney

Fig. 2

Neuroblastoma in a 1-day-old boy diagnosed in utero, an example of contact. a Longitudinal ultrasound of the left upper quadrant shows a hyperechoic solid mass (arrows) immediately cranial to the left kidney. The mass is in contact (arrowheads) with the kidney, and there is no clear plane of separation between the mass and the kidney. b, c Coronal T1- (b) and T2-weighted (c) images show the left suprarenal mass (arrows) in contact (arrowheads) with the left kidney. The left kidney is displaced inferiorly and distorted. There is no plane of separation between the mass and the left kidney

Fig. 3

Neuroblastoma in an 8-month-old girl, an example of contact and infiltration. a Axial T2-weighted image of the thoracic spine shows a lobulated left paraspinal tumor (arrowheads). The tumor is said to be in contact with the aorta (arrow). b In this girl, the tumor (yellow) surrounds less than 50% of the diameter of the aorta (red circle). Thus the tumor is said to be in contact with the aorta. In this instance, an IDRF is not present. c Coronal T1-weighted MR image shows a left-side paraspinal tumor (arrows) extending from T6 through T10. d, e Coronal T1-weighted (d) and sagittal T1-weighted (e) MR images of the spine show tumor (arrows) infiltrating the costovertebral junction between T7 and T10. Tumor that is infiltrating the costovertebral junction between T9 and T12 is considered to be IDRF-positive. IDRF image-defined risk factor

Fig. 4

Neuroblastoma in a 1-month-old boy exhibiting compression. a Axial chest CT shows tumor abutting the right side of the mediastinum and compressing the trachea (arrow). b Coronal chest CT shows the tumor compressing the distal trachea and right mainstem bronchus (arrow). Airway compression is an IDRF that might be better evaluated on CT. IDRF image-defined risk factor

Fig. 5

Neuroblastoma in a 5-year-old boy, an example of encasement, infiltration, and invasion. a Axial T2-weighted image with fat saturation shows a large tumor extending from the abdomen, through the diaphragmatic crus (arrowheads) and into the thoracic cavity. The tumor encases the aorta (solid arrow) as it passes through the diaphragmatic crus. In addition, there is infiltration of the liver, with tumor (dashed arrow) extending along the right posterior portal triad. b, c Axial T2-weighted (b) and T1-weighted (c) post-contrast MR images with fat saturation show tumor infiltrating the renal parenchyma (white arrowheads), encasing the renal vasculature (black arrows) and encasing the aorta (dashed white arrows). Peritoneal metastases (solid white arrows) are also present. The tumor is in contact with the inferior vena cava (black arrowheads). It flattens its lumen, but flow is still visible. Encasement of the aorta, infiltration of the kidney, and invasion of the renal pedicle are all considered to be image-defined risk factors

Fig. 6

Neuroblastoma in a 3-year-old boy, an example of contact, encasement, infiltration, and invasion. ac Axial T1-weighted (a), T1-weighted post-contrast with fat saturation (b) and T2-weighted (c) MR images of the abdomen show a large, lobulated central abdominal neuroblastoma (white arrows). The tumor invades the renal pedicle (white arrowheads), causing left-side renal obstruction. Fluid–debris (a and c) and fluid–contrast (b) levels are visible within the left renal collecting system. The tumor also invades the right kidney, with encasement of the right renal artery (black arrowhead in b). In addition to affecting the kidneys, the tumor also encases the aorta (dashed arrows) and the superior mesenteric artery (black arrows). The renal pedicle invasion, encasement of the aorta, and encasement of the superior mesenteric artery are all considered IDRFs. The inferior vena cava (black arrowhead in c) is in contact with the tumor. The vessel is flattened with a visible lumen. d Axial T2-weighted MR image shows invasion of the tumor (arrow) into the porta hepatis. In addition, the tumor encases the celiac axis (arrowhead) at its origin. Both features are IDRFs. e Coronal T1-weighted post-contrast MR image with fat saturation shows the aorta (arrowhead) and iliac arteries (arrows) surrounded by tumor. f On axial T2-weighted MR image, encasement of the iliac arteries (arrows) is confirmed. The encasement of the aorta and of the iliac arteries are both considered to be IDRFs. IDRF image-defined risk factor

Image-defined risk factors based on anatomical location

Table 4 summarizes the IDRFs recognized by the INRG task force based on anatomical location [6].
Table 4

Description of image-defined risk factors (IDRFs)

Anatomical region

Description

Multiple body compartments

Ipsilateral tumor extension within two body compartments (e.g., neck and chest, chest and abdomen, or abdomen and pelvis)

Neck

Tumor encasing carotid artery, vertebral artery, and/or internal jugular vein

Tumor extending to skull base

Tumor compressing trachea

Cervicothoracic junction

Tumor encasing brachial plexus roots

Tumor encasing subclavian vessels, vertebral artery, and/or carotid artery

Tumor compressing trachea

Thorax

Tumor encasing aorta and/or major branches

Tumor compressing trachea and/or principal bronchi

Lower mediastinal tumor infiltrating costovertebral junction between T9 and T12 vertebral levels

Thoracoabdominal junction

Tumor encasing aorta and/or vena cava

Abdomen and pelvis

Tumor infiltrating porta hepatis and/or hepatoduodenal ligament

Tumor encasing branches of superior mesenteric artery at mesenteric root

Tumor encasing origin of celiac axis and/or origin of superior mesenteric artery

Tumor invading one or both renal pedicles

Tumor encasing aorta and/or vena cava

Tumor encasing iliac vessels

Pelvic tumor crossing sciatic notch

Intraspinal tumor extension

Intraspinal tumor extension (above L2) provided that (any of the following):

More than one-third of spinal canal in axial plane is invaded

Perimedullary leptomeningeal spaces are not visible

Spinal cord signal intensity is abnormal

Infiltration of adjacent organs and structures

Pericardium

Diaphragm

Kidney

Liver

Duodenopancreatic block

Mesentery

Modified from [6] with permission

Multiple body compartments

Most primary neuroblastic tumors are found predominantly in one anatomical compartment with some extending into neighboring compartments. Contiguous ipsilateral extension of the primary tumor into an adjacent body compartment is considered an IDRF (Figs. 5 and 7).
Fig. 7

Neuroblastoma with thoracic cavity extension in a 3-year-old girl. a Anteroposterior abdominal radiograph shows a left upper quadrant mass (arrows) with speckled calcification (arrowhead) displacing loops of bowel inferiorly. b Coronal image from an I-123 MIBG scan shows uptake of the radiopharmaceutical within the primary mass (arrow). There is contiguous nodal extension of tumor (arrowhead) into the thoracic cavity. c Coronal T2-weighted MRI shows the large left suprarenal mass (arrowheads) and contiguous nodal extension of tumor (arrow) into the thoracic cavity. d Sagittal T1-weighted MR image shows bone/bone marrow metastases (arrowheads) within multiple vertebral bodies. The presence of distant metastases makes this INRGSS stage M disease. The ipsilateral extension of tumor within two body compartments is an image-defined risk factor. INRGSS International Neuroblastoma Risk Group staging system, MIBG metaiodobenzylguanidine

Multifocal noncontiguous primary disease is rare at presentation but is mainly found in people with syndrome-associated with neuroblastic tumors. If this is found, the neoplasm should be staged based on the site of the largest primary tumor. Multifocality should be documented, but this alone is not considered an IDRF [6].

Neck

Primary cervical neuroblastoma is uncommon [2]. The superior cervical sympathetic chain is the site of origin for cervical tumors [6]. IDRFs in the neck include tumors that encase the carotid or vertebral arteries, encase the jugular vein, compress the trachea, or extend to the skull base (Fig. 8) [6].
Fig. 8

Neuroblastoma with skull base extension in a 4-year-old girl, an example of encasement. a, b Coronal T1-weighted MR image after contrast administration (a) and sagittal T2-weighted MR image (b) show a large heterogeneous left cervical neuroblastoma (arrows) with extension to the skull base (arrowheads). c Axial T1-weighted MR image after contrast administration shows encasement and displacement of the left common carotid artery (arrow). The encasement of the vessel is an image-defined risk factor

Cervicothoracic junction

Cervicothoracic primary tumors are uncommon. These tumors are normally located above the subclavian artery at the level of the origin of the vertebral artery, arising from the stellate ganglion. IDRFs at this location include tumors that encase the subclavian vessels, the carotid or vertebral arteries, the jugular vein, or the brachial plexus roots; or compress the trachea [6].

Thorax

Thoracic neuroblastomas account for 16–20% of all neuroblastomas [23]. Typically these tumors arise from the paraspinal sympathetic chain found in the posterior mediastinum or from the periaortic sympathetic plexuses. Intraspinal extension of tumor is common, with spinal cord compression occurring in 25% [24]. IDRFs in the thorax include tumors that encase the aorta or its major branches, compress the trachea or bronchi, or infiltrate the diaphragm or pericardium [6].

Thoracoabdominal junction

Spinal cord ischemia is a particular surgical risk for lower thoracic paraspinal tumors, specifically those between T9 and T12, because the anterior spinal artery could be compromised during tumor resection. Thus tumors at the costovertebral junction between T9 and T12 are considered to be IDRF-positive [6].

Regional lymph nodes from primary abdominal tumors can extend through the diaphragmatic crus into the thorax. Contiguous nodal extension of tumor is not considered to represent tumor within multiple compartments, and is thus not an IDRF. However, contiguous nodal extension between the chest and abdomen is considered loco-regional tumor and upstages the disease to L2 [6].

Other IDRFs at the thoracoabdominal junction include tumors that encase the descending aorta or inferior vena cava (Figs. 3 and 5) [6].

Abdomen and pelvis

The majority of neuroblastic tumors (65–70%) arise in the abdomen from the adrenal gland, sympathetic ganglia, or sympathetic plexuses [23]. Because of their site of origin and the proximity of vascular structures, these tumors often encase one or more of the following vessels: the inferior vena cava, the aorta, the celiac axis, superior and inferior mesenteric arteries, renal arteries and veins, iliac arteries and veins, and portal vein. Encasement of any of these structures is considered an IDRF, except for the inferior mesenteric artery, which rarely causes complications if compromised during surgery [6].

Other IDRFs in the abdomen include invasion of the renal pedicle, infiltration of the porta hepatis, and infiltration of other abdominal organs such as the diaphragm, kidney, liver, duodenopancreatic block or mesentery (Figs. 5, 6 and 9).
Fig. 9

Neuroblastoma with renal involvement in a 3-month-old boy, an example of encasement, infiltration, and invasion. a Axial T2-weighted MRI shows a large left-side tumor (solid arrows) infiltrating the renal capsule. The tumor invades the renal pedicles with encasement of the renal vessels (dashed arrow). Tumor also encases the aorta (arrowhead). Although tumor is in contact with the nearby inferior vena cava, it does not have any effect on its lumen. Renal infiltration, renal pedicle invasion, and encasement of the aorta are IDRFs. b Axial T1-weighted post-contrast MR image with fat saturation shows the tumor compressing the enhancing renal parenchyma (arrows). At surgery, this tumor was shown to have infiltrated the renal capsule and was compressing the renal parenchyma within the Gerota fascia. IDRF image-defined risk factor

Lumbar and pelvic neuroblastic tumors are much less common than abdominal neuroblastoma and account for approximately 4% of cases of neuroblastoma [6]. Pelvic tumors typically arise from the hypogastric sympathetic plexus or the presacral sympathetic ganglia [6].

IDRFs in the pelvis include tumors that encase the iliac arteries or veins or cross the sciatic notch (Figs. 6 and 10). The boundary of the greater sciatic foramen is a sagittal-oblique line between the spine of the ischium and the lateral margin of the sacrum.
Fig. 10

Neuroblastoma extending outside the pelvis in a 16-month-old boy, an example of encasement. a Axial T2-weighted MR image shows tumor (arrow) extending outside the pelvis beyond the sagittal-oblique line connecting the spine of the ischium and the lateral margin of the sacrum. This is an IDRF-positive feature. b Axial T2-weighted MR image at a more cranial position shows tumor (solid arrow) extending into the spinal canal through the left-side S2 neural foramina (not shown). The tumor occupies more than one-third of the spinal canal and displaces the thecal sac (arrowhead) to the right. Tumor extension into the spinal canal below the level of L2 is not considered an IDRF because it cannot compress the spinal cord. However the tumor encases the external iliac artery (dashed arrow). This is considered an IDRF. IDRF image-defined risk factor

Spinal extension

Paraspinal tumors of the neck, chest, abdomen and pelvis can extend through neural foramina and into the spinal canal. A tumor that (1) occupies more than one-third of the spinal canal in the axial plane above the level of L2, (2) causes effacement of the perimedullary leptomeningeal spaces above the level of L2 or (3) causes abnormal spinal cord signal intensity is considered to be IDRF-positive (Fig. 11) [6]. Extension of tumor into the spinal canal below the level of L2 (even if it involves more than one-third the diameter of the spinal canal) is not considered to be an IDRF because the spinal cord is not present below this level (Fig. 10). Complications from tumor removal below this level are thus rare, and emergent tumor decompression is usually not required [6].
Fig. 11

Recurrent metastatic neuroblastoma in an 8-year-old girl. Axial T2-weighted MRI shows tumor (solid arrows) extending through both neural foramina at this level. The spinal cord (arrowhead) is compressed, and there is no visible cerebral spinal fluid surrounding the cord. Spinal extension with effacement of the leptomeningeal space or tumor occupying more than one-third of the spinal canal is considered IDRF-positive disease. In this girl, there are also extensive liver metastases (example, dashed arrow), making this stage M disease. IDRF image-defined risk factor

Conclusion

Even though the INRG staging system has been in use since 2009, many pediatric radiologists remain unfamiliar with its definitions and application. To adequately and accurately stratify children with neuroblastoma, reproducible imaging criteria developed by the INRG should be used, and knowledge of their definitions and rationale are crucial for implementation.

Notes

Compliance with ethical standards

Conflicts of interest

None

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Alan M. Chen
    • 1
  • Andrew T. Trout
    • 1
  • Alexander J. Towbin
    • 1
  1. 1.Department of RadiologyCincinnati Children’s HospitalCincinnatiUSA

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