CT, MRI, and FDG PET/CT in the Assessment of Lymph Node Involvement in Pediatric Hodgkin Lymphoma: An Expert Consensus Definition by an International Collaboration on Staging Evaluation and Response Criteria Harmonization for Children, Adolescent, and Young Adult Hodgkin Lymphoma (SEARCH for CAYAHL)

Abstract

Staging of pediatric Hodgkin lymphoma is currently based on the Ann Arbor classification, incorporating the Cotswold modifications and the Lugano classification. The Cotswold modifications provide guidelines for the use of CT and MRI. The Lugano classification emphasizes the importance of CT and PET/CT in evaluating both Hodgkin lymphoma and non-Hodgkin lymphoma but focuses on adult patients. This article presents consensus guidelines that extend the traditional classifications used for adult Hodgkin lymphoma staging and provide rigorous definitions of lymph node groups based on MRI, CT, and fluorodeoxyglucose PET/CT findings. This allows consistent terminology and definitions, using metabolic and morphologic imaging to identify affected lymph nodes or extranodal regions and organs. The pattern of involvement, together with other individual risk factors, determines treatment strategy. In case of inadequate response to chemotherapy, radiation therapy is often required. Standardization of staging definitions for pediatric Hodgkin lymphoma is necessary for comparing treatment outcomes between North American and European clinical trials and a prerequisite for clear communication during tumor boards and central review. This comprehensive imaging atlas is intended to provide regional criteria for nodal involvement and to serve as a standardized guide for the anatomic assignment of lymph node involvement in pediatric Hodgkin lymphoma.

Graphical abstract

Figure 1:

Consort diagram of consensus process for establishing lymph node or nodal region definitions in pediatric Hodgkin lymphoma. SEARCH for CAYAHL (Staging Evaluation and Response Criteria Harmonization for Childhood, Adolescent and Young Adult Hodgkin Lymphoma) is an international consortium formed in 2011, focused on harmonizing staging and response criteria for pediatric Hodgkin lymphoma, with representatives from the EuroNet Pediatric Hodgkin Lymphoma committee, the Children’s Oncology Group Hodgkin Lymphoma committee, and the St Jude Consortium Pediatric Hodgkin Lymphoma Committee.

Figure 2:

Overview of independent lymph node regions used to determine the sites of involvement in pediatric Hodgkin lymphoma. Adapted from the original figure by Kaplan and Rosenberg (28) and reproduced, with permission, from references .

Figure 3:

Upper cervical lymph nodes (left and right). The upper cervical lymph node regions are shown in coronal and axial planes on a contrast-enhanced CT scan in a 17-year-old male patient in complete remission. The upper cervical (turquoise), lower cervical (yellow), and supraclavicular (blue) lymph node regions are shown together with their corresponding borders. The upper cervical lymph nodes correspond to level IIa and IIb nodal groups proposed by Grégoire et al (18).

Figure 4:

Lower cervical lymph nodes (left and right). The lower cervical lymph node region (yellow) is shown on a contrast-enhanced axial CT scan in a 17-year-old male patient. These lymph nodes correspond to level III and VIa nodal groups proposed by Grégoire et al (18).

Figure 5:

Supraclavicular lymph nodes (left and right). The supraclavicular (blue), infraclavicular (purple), and axillary (red) lymph node regions are shown on a contrast-enhanced axial CT scan in a 17-year-old male patient. These lymph nodes correspond to level IV, Vb, Vc, and VI nodal groups proposed by Grégoire et al (18).

Figure 6:

Infraclavicular and perctoral lymph nodes (left and right). The infraclavicular region (purple) is separated from the axillary lymph node region (red) by a dividing line (orange) shown on a contrast-enhanced axial CT scan in a 17-year-old male patient. The upper mediastinal lymph node region (green) is also shown. These lymph nodes correspond to level II, III, and interpectoral nodal groups proposed by Lengelé et al (20).

Figure 7:

Axillary lymph nodes (left and right). The axillary region (red) is separated from the infraclavicular lymph node region (purple) by a dividing line (orange) shown on a contrast-enhanced axial CT scan in a 17-year-old male patient. The upper mediastinal (green) and the internal mammary (turquoise) lymph node regions are also shown. These lymph nodes correspond to level 1 nodal group proposed by Lengelé et al (20).

Figure 8:

Hilar lymph nodes of the right lung. The right hilar region (blue) with medial borders (orange line to the right of midline) is shown on a contrast-enhanced axial CT scan in a 17-year-old male patient. Other regions shown are left hilar (blue), upper mediastinal (green), lower mediastinal (yellow), axillary (red), internal mammary (turquoise), and infraclavicular and pectoral (purple) lymph node regions. These lymph nodes correspond to the hilar nodal stations 10–11, subdivided into right and left hilar nodes, as defined by Chapet et al (17).

Figure 9:

Hilar lymph nodes of the left lung. The left hilar region (blue) with medial borders (orange line to the left of midline) is shown on a contrast-enhanced axial CT scan in a 17-year-old male patient. Other regions shown are right hilar (blue), upper mediastinal (green), lower mediastinal (yellow), axillary (red), internal mammary (turquoise), and infraclavicular and pectoral (purple) lymph node regions. These lymph nodes correspond to the hilar nodal stations 10–11, subdivided into right and left hilar nodes, as defined by Chapet et al (17).

Figure 10:

Upper mediastinal lymph nodes. The upper mediastinal lymph node region (green) is shown on a contrast-enhanced axial CT scan in a 17-year-old male patient. Other regions shown are left and right hilar (blue), lower mediastinal (yellow), axillary (red), and internal mammary (turquoise) lymph node regions. These lymph nodes correspond to lymph node stations 1, 2, 3, 4, 5, and 6 as proposed by Chapet et al (17).

Figure 11:

Internal mammary lymph nodes (left and right). The internal mammary lymph node region (turquoise) is shown on a contrast-enhanced axial CT scan in a 17-year-old male patient. Other regions shown are left and right hilar (blue), lower mediastinal (yellow), axillary (red), and upper mediastinal (green) lymph node regions. These lymph node stations are based on the anatomic boundaries proposed by Verhoeven et al (39) and lie within the connective tissue surrounding the left or right internal thoracic artery.

Figure 12:

Lower mediastinal lymph nodes. The lower mediastinal lymph node region (yellow) is shown on a contrast-enhanced axial CT scan in a 17-year-old male patient. Other regions shown are left and right hilum (blue) with medial borders (orange lines), axillary (red), internal mammary (turquoise), and upper mediastinal (green) lymph node regions. These lymph nodes correspond to lymph node stations 7, 8, and 9 as proposed by Chapet et al (17).

Figure 13:

Retrocrural and paravertebral lymph nodes The retrocrural and paravertebral lymph node region (yellow) is a subregion of the lower mediastinal region shown on a contrast-enhanced axial CT scan in a 17-year-old male patient. Other regions shown are splenic hilar (brown), mesenteric (green), upper para-aortic (blue), ventral supradiaphragmatic recess (purple), and porta hepatis (red) lymph node regions. This lymph node region corresponds to the inferior aspect of lymph node station 9 proposed by Chapet et al (17) and is a subregion of the lower mediastinal region defined in Figure 12.

Figure 14:

Ventral supradiaphragmatic recess (left and right). The ventral supradiaphragmatic recess (purple) is shown on a contrast-enhanced axial CT scan in a 17-year-old male patient. Other regions shown are splenic hilar (brown), mesenteric (green), upper para-aortic (blue), and retrocrural and paravertebral (yellow) lymph node regions. The ventral supradiaphragmatic recess group is the continuation of the internal mammary group from the fourth rib downwards to the diaphragm. Lymph nodes that are distinct from a mediastinal lymph node mass are sometimes located here.

Figure 15:

Splenic hilar lymph nodes. The splenic hilar lymph node region (brown) is shown on a contrast-enhanced axial CT scan in a 17-year-old male patient. Other regions shown are ventral supradiaphragmatic recess (purple), mesenteric (green), porta hepatis (red), upper para-aortic (blue), and retrocrural and paravertebral (yellow) lymph node regions.

Figure 16:

Porta hepatis lymph nodes. The porta hepatis lymph node region (red) is shown on a contrast-enhanced axial CT scan in a 17-year-old male patient. Other regions shown are mesenteric (green), splenic hilar (brown), and upper para-aortic (blue) lymph node regions. This region corresponds to the course of the hepatic artery and roughly corresponds to the level 18 lymph node group proposed by Korst et al (42).

Figure 17:

Mesenteric lymph nodes. The mesenteric lymph node region (green) is shown on a contrast-enhanced axial CT scan in a 17-year-old male patient. The upper para-aortic (blue) lymph node region is also shown. This region corresponds to the superior, central, inferior mesenteric, and ileocolic lymph nodes described by Lengelé et al (20).

Figure 18:

Upper para-aortic lymph nodes. The upper para-aortic retroperitoneal lymph node region (blue) is shown on a contrast-enhanced axial CT scan in a 17-year-old male patient. The mesenteric (green) lymph node region is also shown. This region corresponds to lymph nodes node stations I and II proposed by Lengelé et al (20).

Figure 19:

Lower para-aortic lymph nodes. The lower para-aortic retroperitoneal lymph node region (red) is shown on a contrast-enhanced axial CT scan in a 17-year-old male patient. The mesenteric (green) lymph node region is also shown. This region corresponds to lymph node level III proposed by Lengelé et al (20).

Figure 20:

Iliac chain lymph nodes (left and right). The iliac chain lymph node region (yellow) is shown on a contrast-enhanced axial CT scan in a 17-year-old male patient. The mesenteric (green) lymph node region is also shown. This region corresponds to lymph node levels I, II, III, V, and VII proposed by Lengelé et al (19).

Figure 21:

Inguinal lymph nodes (left and right). The inguinal lymph node region (purple) is shown on a contrast-enhanced axial CT scan in a 17-year-old male patient. These lymph node regions correspond to the regions proposed by Lengelé et al (19).

Figure 22:

Images in a 16-year-old male patient. (A) Axial contrast-enhanced CT scan with arms elevated, with lymph node in the infraclavicular region. (B) Axial noncontrast T1-weighted MRI scan with arms alongside the torso, with lymph node in the supraclavicular region. Depending on the arm position, the marked lymph node (arrowhead) may be assigned to different lymph node regions.

Figure 23:

Axial contrast-enhanced (A) and noncontrast (B) CT scans in a 9-year-old female patient obtained at (A) deep inspiration (end inspiration) and at (B) resting inspiration (quiet breathing). With resting inspiration (B), the mediastinal lymph node (orange arrowhead) is located above the upper sternal border and is therefore assigned to the supraclavicular region, whereas the same lesion (orange arrowhead) at deep inspiration (A) does not cross this border. An additional lymph node (turquoise arrowhead) is also reaching into the supraclavicular region at resting inspiration (B). This should be taken into consideration for radiation planning purposes.

Figure 24:

Axial contrast-enhanced (A) and noncontrast (B) CT scans in a 12-year-old female patient obtained at (A) deep inspiration (end inspiration) and at (B) resting inspiration (quiet breathing). While the right internal mammary lymph nodes (arrowhead) do not appear to be affected by inspiration (A), the mediastinal tumor mass lies broad-based against the ventral thoracic wall during resting inspiration (quiet breathing) (B).

Figure 25:

Axial T2-weighted MRI (A) and axial fused fluorodeoxyglucose (FDG) PET/CT (B) images demonstrate the anatomic location of retrocrural lymph adenopathy (arrowhead) in a 15-year-old male patient. Enlarged retrocrural lymph nodes in Hodgkin lymphoma are typically FDG-avid and should be assigned to the retrocrural and paravertebral region (see Fig 13). This is often best demonstrated and confirmed on sagittal and coronal reformatted images.