British Journal of Radiology (2004) 77, 111-115
© 2004 British Institute of Radiology
doi: 10.1259/bjr/53555208
MRI of neck nodes in non-Hodgkin's lymphoma of the head and neck
A D King, FRCR1,
K I Lei, MRCP2 and
A T Ahuja, FRCR1
1 Department of Diagnostic Radiology and Organ Imaging and 2 Department of Clinical Oncology, Faculty of Medicine, The Chinese University of Hong Kong, Prince of Wales Hospital, Shatin, New Territories, Hong Kong SAR, China
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Abstract
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The aim of this study is to describe the imaging features of neck nodes in non-Hodgkin's lymphoma (NHL). The MR scans of 61 patients undergoing staging of a primary extranodal NHL of the head and neck were reviewed retrospectively. Those MR images with nodal disease were assessed for (a) the pattern of nodal disease, (b) presence of nodal necrosis and (c) presence of extracapsular neoplastic spread (ENS) and nodal matting. The features of the nodal disease were analysed in relationship to the sites of the primary NHL (palatine tonsil (PT) n=23, nasal cavity (NC) n=24, nasopharynx (NP) n=6, other extralymphatic sites (OES) n=8), and histology (natural killer/T-cell (NK/T) n=26, diffuse large cell (DLC) n=24, other subtypes (OS) n=11). Nodal disease was present in 26 patients (43%) and occurred in NHL of the PT n=16 (70%), NP n=3 (50%), NC n=5 (21%) and OES n=2 (25%) and in DLC n=15 (63%), NK/T n=6 (23%) and OS n=5 (45%). Nodal disease was significantly more frequent in DLC than NK/T lymphomas (p=0.0053). Nodal disease spread in a contiguous fashion in 25 (96%) patients with nodes. Necrosis was present in 7 of 26 (27%) being present in DLC of the PT in 5, NK/T of the NP in one and NK/T of the NC in one. ENS and matting were present in 19 (73%) and 13 (50%) patients with nodes, respectively. ENS was found in DLC, NK/T, OS, NC, NP, PT, OES (11, 4, 4,1, 2, 14, 2, respectively) and matting was found in DLC, NK/T, OS, NC, NP, PT, OES (9, 3, 1, 0, 2, 10, 1, respectively). Nodal NHL spreads in a contiguous fashion and is most commonly associated with DLC lymphoma of the NP and PT in Waldeyer's ring. Extracapsular nodal spread is frequent and found in most histological subtypes especially those arising from Waldeyer's ring. Necrosis is more common than previously believed.
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Introduction
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The imaging features of cervical lymphadenopathy from head and neck cancer have been the subject of extensive research. However, much of the literature has concentrated on metastatic nodes from squamous cell carcinomas with little attention focused on nodal disease associated with primary non-Hodgkin's lymphoma (NHL) of the head and neck. The aim of this report was to review all cases of primary NHL of the head and neck that have been staged using MR and evaluate the features of associated nodal disease. In particular, we wanted to document the frequency of nodal necrosis, which based on a previously published small series of NHL arising from the palatine tonsil [1], may be more frequent than commonly believed.
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Patients and methods
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The MR scans of the head and neck in 61 consecutive patients (males=38, females=23, age range 1689 years old, mean age 52 years old) with newly diagnosed or relapsed head and neck lymphoma undergoing staging investigation were reviewed retrospectively. The primary head and neck NHL was extranodal in origin and the site of origin was determined from clinical presentation. All patients were staged according to the Ann Arbor system [2] with modification for extranodal lymphoma. Clinical staging procedures included history, physical examination, complete blood count, blood chemistry studies, serum lactate dehydrogenase, plain chest radiography, CT scan of head and neck, abdomen and pelvis and bone marrow aspiration biopsy. CT scan of the thorax was performed only in the presence of an abnormal chest radiograph. None of the patients underwent a staging laparotomy or lymphangiography. The primary NHL of the head and neck was the site of first presentation of NHL in 54 patients and the site of relapse in 7 patients (the original sites being palatine tonsil (2), nasal cavity (2), nasopharynx (1), breast (1) and vagina (1)). All scans were performed before treatment and none of the patients had recent infection, radiotherapy or surgery. The diagnosis of NHL was made histologically from biopsy of the primary tumour. The diagnosis of nodal involvement by NHL was made radiologically on the demonstration of one or more of the following criteria; necrosis (focal area of low T1 signal intensity with a surrounding rim of enhancement, with or without a corresponding focal area of high T2 signal intensity), extracapsular neoplastic spread (ENS) (presence of indistinct nodal margins, irregular nodal capsular enhancement or infiltration into the adjacent fat or muscle) or size (shortest axial diameter equal or greater than 5 mm in the retropharyngeal region, 11 mm in the jugulodigastric region, and 10 mm in all other regions of the neck) [35].
Images were obtained on a 1.5 T MR unit using either a Philips Gyroscan, Eindhoven, the Netherlands (60 patients) or Siemens magnetom sonata, Erlangen, Germany (one patient) with a head coil (30 cm diameter). All patients underwent a T1 weighted spin-echo sequence (repetition time (TR)/echo time (TE) 500/20; field of view 22 cm, slice thickness 4 mm, with no interslice gap; and matrix size of 256 or 512), before and after a bolus injection of 0.1 mmol kg-1 gadodiamide (Nycomed, Oslo, Norway), and a T2 weighted turbo spin-echo sequence (TR/TE 2500/100, echo train length 14, field of view 22 cm, slice thickness 4 mm, with no interslice gap; and matrix size of 256) and/or a fat-suppressed T2 weighted sequence (TR/TE 2500/100 ms, echo train length of 15, field of view 22 cm, slice thickness 4 mm, with no interslice gap; and matrix size of 256). Images were obtained in at least two planes.
The hard copy MR images were assessed for (a) the pattern of nodal disease, (b) presence of nodal necrosis and (c) presence of ENS, nodal matting and nodal "sheets". Nodal "matting" was defined as a conglomeration of two or more nodes with ENS; nodal "sheets" were defined as extensive conglomerations of nodes where there was almost complete loss of any discernible underlying nodal architecture.
The features of the nodal disease were analysed in relationship to the site and histology of the primary NHL. Contiguous spread was defined according to the routes of spread as described by Rouviere [6], using the landmarks decribed by Som [7], to identify nodal groups. Comparison of radiological features between groups was performed using Fisher's exact test.
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Results
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The results of nodal disease in relationship to the site and histology of primary NHL are shown in Tables 1 and 2
, respectively. Nodal disease was significantly more frequent in the diffuse large cell lymphomas than NK/T-cell lymphoma (63% vs 23%; p=0.0053). Examples of nodal necrosis and ENS are shown in Figures 1 and 2
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Figure 1. Nodal necrosis (arrows) shown on (a) axial T1 weighted image post contrast and (b) axial T2 weighted image with fat suppression.
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Figure 2. Axial T1 weighted image post contrast of (a) matted nodes with extracapsular neoplastic spread (arrows) and (b) "sheets" of lymphomatous nodes where the underlying nodal structures is almost completely destroyed (arrows).
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Discussion
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The spread of a primary head and neck NHL to cervical lymph nodes is generally believed to adversely affect survival [8, 9]. Regional tumour spread to cervical lymph nodes was present in 43% of patients in this study which is in keeping with a previously reported incidence of around 50% [10, 11]. However, the incidence varied with the site of the primary NHL and the histological subtype. This study showed that the incidence of nodal disease increased as the primary site of NHL descended from the nasal cavity, to the nasopharynx, to the palatine tonsil, the latter being associated with nodal NHL in 70% of all cases. The numbers of patients with nodal NHL arising from other primary sites (salivary glands, thyroid, larynx and paranasal sinus) were too small to identify for any trend but when grouped together had an incidence that was lower than that from Waldeyer's ring. This is in keeping with clinical studies, where NHL arising from Waldeyer's ring has a greater frequency of nodes [9, 12] especially for tonsillar lymphoma [13]. The study showed also that nodal disease was significantly more frequent in the DLC than NK/T-cell lymphoma suggesting that diffuse large cell lymphoma has a higher tendency to spread via the lymphatic system. Indeed, in contrast to DLC, NK/T-cell lymphomas tend to show haematogenous dissemination to distant tissues/organs such as the skin, liver and lung [14, 15]. Evaluation of the pattern of nodal disease showed that while metastases from NHL tend to disseminate throughout the body in a non-contiguous fashion [16], spread through nodal groups in the neck proceeded along an orderly contiguous route. Nodal lymphoma arising from tumours in the nasal cavity and nasopharynx had bilateral disease while those lower down in the palatine tonsil were bilateral in just over 50% of cases.
Necrosis in lymphomatous nodes is well described in Hodgkin's disease where necrosis is found in around a quarter of mediastinal and abdominal nodes with preponderance in the sclerotic forms of the disease [17, 18]. The presence of necrosis is even more frequent after therapy and thought to indicate a favourable response [18]. On the other hand, although NHL of the head and neck comprises a diverse group of distinct clinicopathologic entities [19], necrosis in lymph nodes from NHL is considered to be uncommon [20, 21]. In the absence of treatment the detection of necrotic cervical nodes would usually suggest other pathology rather than NHL. This current study has shown that necrosis is more common than previously believed being found in 27% of all cases, a finding which is in accordance with two recent studies by Saito et al [22] and Wang et al [23] which also found a higher incidence of 25% and 75%, respectively. Nodal necrosis was found most commonly in the diffuse large cell lymphomas in the palatine tonsil. It was less commonly seen in natural killer/T-cell lymphomas and not found in the small number of other histological subtypes. Nodal necrosis is not only important in suggesting the likely cause of lymphadenopathy but it also has the potential to be a prognostic indicator in NHL with a study by Saito et al [22] showing that necrotic nodes had a greater prevalence in advanced stage lymphomas.
Finally, the study evaluated ENS which has received scant attention in the literature in NHL. In this study ENS was a very common feature of nodal disease being found in 73% of all patients with nodes, in nearly 70% of these nodes the ENS was extensive leading to confluent masses from the matting of multiple nodes. Extracapsular neoplastic spread and matting were particularly common with NHL of Waldeyer's ring and almost 90% of patients with nodes arising from a palatine tonsil NHL showed these features. Extracapsular neoplastic spread was encountered frequently with both DLC and NK/T-cell lymphomas. It is known that ENS is an important prognostic indicator for squamous cell carcinoma of the head and neck, where the presence of ENS increases the risk of local failure and distant metastases, and decreases survival [2428]. However, to the authors' knowledge the prognostic significance of ENS in NHL has never been addressed. This issue could not be addressed in the current study because of the small numbers of patients, but it is of interest to note there were two patients in this study with extreme examples of ENS, where nodes formed sheets of lymphomatous tissue with almost complete loss of any discernable underlying nodal architecture. In one case the follow-up period was too short (1 month) to allow any meaningful evaluation of outcome, but in the other case the patient had a very poor prognosis and died within 4 months of the scan.
There are several limitations to this study. First, the diagnosis of nodal disease was based on imaging criteria rather than pathology, an unavoidable circumstance given that these patients do not undergo neck dissection. Second, it is known from data from CT that tumour deposits within a metastatic node from squamous cell carcinoma [3, 4] or lymphoma [20] may produce a focal area of abnormality with an enhancing rim similar to necrosis. Using the criteria set out in this study nodal necrosis was diagnosed by MR in one patient because of an area of low signal intensity with an enhancing rim on the post contrast T1 weighted images. However, there was no corresponding area of very high signal intensity on the T2 weighted images and it is possible that this appearance was due to focal lymphoma deposit rather than necrosis. Third, while the total number of patients is reasonably large when the numbers are broken down according to site and histology some of the groups are too small for statistical analysis.
In conclusion, nodal disease spreads in a contiguous fashion and most commonly arises from NHL of Waldeyer's ring, being significantly more frequent with diffuse large cell rather than natural killer/T-cell lymphomas. Extracapsular neoplastic spread is very frequent particularly with nodal disease from Waldeyer's ring. Necrosis is more common than previously believed and is associated both diffuse large cell and natural killer/T-cell lymphomas.
Received for publication June 20, 2003.
Revision received September 22, 2003.
Accepted for publication November 12, 2003.
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