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AJR 2000; 174:1141-1145
© American Roentgen Ray Society


Original Report

Nasal T-Cell/Natural Killer Cell Lymphoma

CT and MR Imaging Features of a New Clinicopathologic Entity

G. C. Ooi1, C. S. Chim2, R. Liang2, K. W. T. Tsang2 and Y. L. Kwong2

1 Department of Diagnostic Radiology, The University of Hong Kong, Rm. 405, Block K, Queen Mary Hospital, Pokfulam, Hong Kong SAR, China.
2 Department of Medicine, The University of Hong Kong, Queen Mary Hospital, Pokfulam, Hong Kong SAR, China.

Received April 19, 1999; accepted after revision September 9, 1999.

 
Address correspondence to G. C. Ooi.


Abstract
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
OBJECTIVE. Nasal T-cell/natural killer cell lymphoma is a new clinicopathologic entity with a characteristic immunophenotypic profile and distinct clinical features. This study describes the radiologic features of nine cases of proven nasal T-cell/natural killer cell lymphoma.

CONCLUSION. Nasal T-cell/natural killer cell lymphoma is often a locally destructive (T stages 3 and 4) disease, typically presenting with obliteration of the nasal passages and maxillary sinuses. Involvement of the adjacent alveolar bone, hard palate, orbits, and nasopharynx is found in more than 50% of cases and is associated with extensive soft-tissue masses. Presence of bone erosion is suggestive but not diagnostic of the disease.


Introduction
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Natural killer cell lymphoma is a new distinct clinicopathologic entity, currently classified as angiocentric lymphoma in the revised European-American lymphoma classification system [1]. However, in the proposed World Health Organization classification of lymphoid malignancies, these tumors are more clearly classified as nasal-type extranodal T-cell/natural killer (T/NK) cell lymphoma and natural killer cell leukemia [2]. They are characterized immunophenotypically by the expression of CD2, CD3{epsilon} (but not CD3 and the T-cell receptor), and CD56. Genotypically, the T-cell receptor gene in germline configuration classifies them. T/NK-cell lymphomas can be divided into three types according to the predominant sites involved. Most cases occur in the nose and upper aerodigestive system and are referred to as nasal T/NK-cell lymphoma. Few cases occur in areas other than the nose and are referred to as non—nasal-type T/NK-cell lymphoma. Rarely, the disease presents with a leukemia phase and is referred to as T/NK-cell lymphoma/leukemia [3, 4].

Nasal T/NK-cell lymphomas have been known by various names, including lethal midline granuloma, polymorphic reticulosis, and other more obscure terms such as progressive lethal granulomatous ulceration, malignant granuloma, nonhealing granuloma, and midline malignant reticulosis [5, 6]. All these diseases were destructive lesions involving the nasal cavity, oropharynx, upper palate, and larynx. However, with the advent of immunophenotyping, these lesions were found to be lymphoid in nature and so should now be regarded as nasal lymphoma [7]. Most nasal lymphomas are of T/NK-cell lineage, although some of these lymphomas could be of B- or T-cell lineage [4]. Nevertheless, B- and T-cell lymphomas of the nose are rarely primary tumors and usually represent metastases from other lymph node sites [4]. On the other hand, nasal T/NK-cell lymphomas are predominantly primary tumors [3, 4].

Both nasal and nonnasal T/NK-cell lymphoma pursue an aggressive clinical course but little is known of the imaging features [3, 4]. We have therefore performed this study to evaluate and summarize pertinent imaging features of nasal T/NK-cell lymphoma. The CT and MR imaging findings of nine cases of nasal T/NK-cell lymphoma are described.


Materials and Methods
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
The records of all patients with nasal T/NK-cell lymphoma who were treated at our institution, a university-based tertiary referral center for lymphoma, over a 12-year period (1987-1998) were reviewed. Records were retrieved from the division of hematology's computerized database, which classifies all lymphomas according to histologic and immunophenotypic data. Nasal T/NK-cell lymphoma was defined as primary nasal lymphoma with an NK-cell phenotype determined from histologic and immunophenotypic diagnosis [2, 3, 7]. Patients presenting with hard-palate ulceration and with involvement of the nasal cavity were also included. All patients presented with lesions or symptoms that were predominantly nasal on presentation [3]. The Ann Arbor staging system was used for clinical staging: stage I, confined to one lymph node site; stage II, confined to more than one lymph node site but on one side of the diaphragm; stage III, confined to lymphatic tissue or spleen but on both sides of the diaphragm; stage IV, bone marrow or liver involvement or extranodal sites with widespread involvement; and subscript E, extranodal site with localized involvement. All patients underwent routine hematologic screening, bilateral marrow trephine biopsy, chest radiography, CT of the abdomen, and panendoscopy for staging purposes.

The database search yielded 36 cases of nasal T/NK-cell lymphoma. Of these cases, CT or MR images or both were available for evaluation in only nine cases (six men and three women; mean age ± SD, 56.5 ± 14 years). Few images were available because in most cases chemotherapy was instituted immediately after histologic diagnosis and Ann Arbor staging. Local tumor staging is not mandatory for the Ann Arbor staging system. Eight patients underwent axial or coronal CT examination of the sinonasal area, six with IV contrast medium. One patient underwent unenhanced MR examination of the sinonasal area only, and two patients had both enhanced CT and MR examinations of the sinonasal area. CT examinations were performed on either of two scanners: a 9800 or a HiSpeed Advantage (General Electric Medical Systems, Milwaukee, WI). MR imaging was performed using a 1.5-T system (Signa; General Electric Medical Systems). CT images were obtained in soft-tissue and bone algorithms and filmed in the respective window settings. Both CT and MR images were evaluated for site and extent of disease and for pattern of involvement of adjacent sites. A modified local tumor (T) staging system for nasal cell lymphoma was devised based on previous criteria [8]: T1, tumor confined to the nasal cavity; T2, extension of tumor to the maxillary antra, anterior ethmoidal sinus, or hard palate; T3, extension to the posterior ethmoidal sinus, sphenoidal sinus, orbit, superior alveolar bone, cheeks, or superior buccinator space; and T4, tumor involvement of the inferior alveolar bone, inferior buccinator space, infratemporal fossa, nasopharynx, or cranial fossa.


Results
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Presenting symptoms in seven of the nine patients with stage IE disease were nasal obstruction (n = 7), epistaxis (n = 1), nasal or palatal ulceration (n = 3), and nasal discharge (n = 3). A patient with stage IIE presented with proptosis, nasal obstruction, and opthalmoplegia, and a patient with stage IVE disease had nasal symptoms with liver metastases. Mean duration of symptoms before presentation was 3.2 ± 1.9 months (range, 6 weeks to 6 months). Currently, there are six survivors, with an overall mean survival of 23 ± 19 months (range, 1-58 months). Local tumor stage was at stage 3 (n = 4) or 4 (n = 2) for most cases. In the three patients with either T1 or T2 staging, complete response to treatment (chemotherapy or radiotherapy or both) was noted, with median survival of 57 months. In the remaining six patients, treatment response was poor.

Site of Disease
Six patients had disease primarily in the nasal cavity with a soft-tissue mass (with or without bony erosion) of the nasal septum and turbinates. Of these, two patients had disease confined solely to the nasal cavity, and four patients had disease extension into the paranasal sinuses (n = 4), alveolar bones (n = 2), hard palate (n = 1), and subcutaneous tissues of the nasal ala, cheek, and buccinator spaces (n = 3) (Figs. 1A,1B,1C and 2). In two patients, the disease site was in the superior nasal cavity with adjacent orbital, ethmoidal, and maxillary sinus involvement (Fig. 3). Extensive infratemporal space and nasopharyngeal involvement was found in the first patient, a 62-year-old woman (Fig. 3). In the second patient, a 37-year-old man, disease was present in the hard palate with a nasal component, nasopharynx, and anterosuperior alveolar bone, with soft-tissue involvement of the buccinator spaces, infratemporal fossa, and temporalis muscle. No significantly enlarged parapharyngeal or cervical lymph nodes were noted in any case.



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Fig. 1A. —71-year-old man with 6-month history of nasal blockage caused by nasal T-cell/natural killer cell lymphoma. Contrast-enhanced axial CT scan shows large mass filling entire nasal cavity with erosion and deviation of nasal septum, extending anteriorly into nasal ala (arrows).

 


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Fig. 1B. —71-year-old man with 6-month history of nasal blockage caused by nasal T-cell/natural killer cell lymphoma. Coronal CT scan using bone algorithm shows bone erosion of medial maxillary walls, bilateral turbinates, and left ethmoidal sinus.

 


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Fig. 1C. —71-year-old man with 6-month history of nasal blockage caused by nasal T-cell/natural killer cell lymphoma. Contrast-enhanced axial CT scan caudad to A shows erosion (E) of anterior aspects of superior alveolar bone.

 


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Fig. 2. —76-year-old man with 3-month history of nasal blockage and epistaxis caused by nasal T-cell/natural killer cell lymphoma. Unenhanced axial CT scan shows soft-tissue mass in anterior aspects of left nasal cavity that is destroying nasal septum and adjacent left nasal turbinate. Note extensive soft-tissue involvement in left nasal ala and left buccinator space with focal erosion of adjacent left anterior maxillary wall (arrowhead).

 


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Fig. 3. —62-year-old woman with 6-week history of nasal blockage and discharge and right cheek swelling caused by stage T4 nasal T-cell/natural killer cell lymphoma. Contrast-enhanced axial CT scan shows disease extension into infratemporal fossa involving masseter (M) and temporalis (T) muscles, pterygoid fossa (P), and right parapharyngeal space (S).

 

Bone Involvement
Bone erosion with no osteoblastic (sclerotic) destruction was present in seven patients. Erosion of the medial maxillary wall was present in all patients with maxillary antra extension, whereas posterior wall destruction was seen in only one patient with tumor spread to the infratemporal space and temporalis muscle (Fig. 3). Anterior maxillary wall erosion was found in only one of three patients with tumor extension into the nasal ala, cheek, and lips (Fig. 2). Orbital floor and lamina papyracea were destroyed in both patients with orbital and ethmoidal tumor involvement, a 62-year-old woman and a 40-year-old woman. Both women also had maxillary antra involvement. Alveolar bone erosion was present in three patients with extensive soft-tissue infiltration of the buccinator space. In two of these patients, the adjacent hard palate was also involved (Fig. 4D).



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Fig. 4D. —47-year-old man with nasal T-cell/natural killer cell lymphoma who presented with nasal blockage and hard palate ulcer. Contrast-enhanced T1-weighted spin-echo MR image (660/20) shows enhancing tissue (arrowheads) in gingivobuccal recesses and in hard palate, which is partially eroded (E).

 

Soft-Tissue Involvement
MR imaging was superior to CT in characterizing soft-tissue involvement. In the three patients with MR images, tumoral tissue appeared isointense to muscle on T1-weighted sequences, with mild-to-moderate hyperintensity to muscle on T2-weighted sequences (Fig. 4A,4B,4C,4D). Mild-to-moderate heterogeneous enhancement occurred in all involved soft tissues on CT and MR imaging. Fluid retention or mucosal thickening or both were noted in apparently uninvolved paranasal sinuses of five patients. Fluid was nonenhancing and markedly hyperintense to muscle on T2-weighted images (Fig. 4A,4B,4C,4D), whereas mucosal thickening could be differentiated from tumor by both its homogenous hyperintensity with respect to muscle on T2-weighted images and its homogeneous enhancement. In one patient, enhancing inflammatory polypoid lesions, which were hyperintense to muscle on T2-weighted images, were noted in both maxillary sinuses (Fig. 4A,4B,4C,4D). In another patient, hemorrhagic fluid, which appeared hyperdense on CT and hyperintense and isointense to muscle on T1- and T2-weighted images, respectively, was noted in a maxillary sinus of a 40-year-old woman.



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Fig. 4A. —47-year-old man with nasal T-cell/natural killer cell lymphoma who presented with nasal blockage and hard palate ulcer. Axial T1-weighted spin-echo MR image (TR/TE, 900/9) shows isointense soft-tissue mass (M) involving nasal cavity. Note extension to nasal ala, left inferior turbinate, and both medial maxillary walls.

 


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Fig. 4B. —47-year-old man with nasal T-cell/natural killer cell lymphoma who presented with nasal blockage and hard palate ulcer. T2-weighted fast spin-echo MR image (5000/84) shows abnormal tissue as heterogeneously hyperintense (arrows), whereas both maxillary antra are markedly hyperintense because of retained secretions.

 


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Fig. 4C. —47-year-old man with nasal T-cell/natural killer cell lymphoma who presented with nasal blockage and hard palate ulcer. Contrast-enhanced T1-weighted spin-echo MR image (660/20) shows enhancing inflammatory polyps and mucosa (arrows). Note nonenhancing fluid in maxillary antra. Tumor tissue enhances heterogeneously.

 


Discussion
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Nasal T/NK-cell lymphoma is rare in the United States and Europe but common in Asia, South and Central America, and Mexico. This study reviews the imaging features of nine ethnic Chinese adults with this disease. Our results illustrate that nasal T/NK-cell lymphoma is often locally destructive with bone erosion and a soft-tissue mass, which obliterates the nasal passages and maxillary sinuses. Involvement of the adjacent alveolar bones, hard palate, orbits, and nasopharynx occurs in more than 50% of cases and is invariably associated with an extensive soft-tissue mass. These imaging features, however, are not specific and bone erosion, although suggestive of the diagnosis, could be caused by other aggressive neoplasms. MR imaging of malignant tumors is useful in delineating the extent of soft-tissue infiltration and in differentiating inflamed from tumoral tissue and fluid from soft-tissue thickening.

Recently, immunophenotype has been shown to significantly influence survival and prognosis of patients with nasal lymphoma [4]. Patients with nasal T/NK-cell lymphoma have the worst prognosis, with a young median age of presentation (50 years), compared with those with B- and T-cell nasal lymphoma [4]. It is not clear whether similar differences can be found in the radiologic features of the three different immunophenotypes of nasal lymphoma because, to our knowledge, no such comparative studies have been performed. However, in two previous series evaluating sinonasal non-Hodgkin's lymphoma, CT evidence of bone destruction was reported in 40% of the cases, despite the presence of disease on both sides of a bony boundary [9, 10]. In comparison, bone erosion in our nasal T/NK-cell patients was present in 78%, the most common sites being the medial maxillary wall, nasal septum, and lamina papyracea. Palatal and alveolar margin erosions were associated with tumor spread to the buccinator space, whereas posterior maxillary wall destruction was found with disease extension into the infratemporal space. Despite marked soft-tissue involvement of the midface region, the anterior maxillary wall was rarely involved. However, compared with sinonasal squamous cell carcinoma, which has been reported to destroy at least one maxillary wall in 85% of cases [11], bone destruction in the cases of nasal T/NK-cell lymphoma we studied was less severe.

Radiologic differential diagnoses of nasal T/NK-cell lymphoma include other causes of sinonasal destruction such as Wegener's granulomatosis, other non-Hodgkin's lymphoma, granulomatous infections, adenoid cystic carcinoma, olfactory neuroblastoma, malignant melanoma, and squamous cell carcinoma. Wegener's granulomatosis is a systemic disorder with involvement of the kidneys and lungs. It is also more localized and rarely, if ever, involves the palate, alveolar bone, or skin. We have already illustrated that bone permeation reported in non-Hodgkin's lymphoma is not a feature consistent with T/NK-cell lymphoma [11]. With granulomatous infections such as allergic aspergillosis, linear interlacing high densities and bone remodeling and thickening are common CT features [12]. Squamous cell carcinoma of the sinuses remains an important radiologic differential diagnosis and may be distinguished from nasal T/NK-cell lymphoma by the presence of more severe bone destruction, lack of enhancement on CT, and a predilection for the maxillary sinuses [11].

In conclusion, the imaging features of nasal T/NK-cell lymphoma are nonspecific, sharing similarities with other aggressive lesions. However, features that may suggest the diagnosis are large soft-tissue masses obliterating the nasal cavity with bone erosion and frequent involvement of the maxillary sinuses. Extensive midface soft-tissue, oropharyngeal, infratemporal, and orbital involvement are common at presentation and are indicative of advanced (T stages 3 and 4) disease. CT and MR imaging are complementary techniques in evaluating the local stage of this aggressive form of lymphoma.


References
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 

  1. Harris NL, Jaffe ES, Stein H, et al. A revised European-American classification of lymphoid neoplasms: a proposal from the International Lymphoma Study Group. Blood 1994;84: 1361 -1392[Free Full Text]
  2. Jaffe ES, Harris NL, Diebold J, Diebold J, Muller-Hermelink H. World Health Organization classification of neoplastic diseases of the hematopoietic and lymphoid tissues: a progress report. Am J Clin Pathol 1999;111(suppl 1): S8-S12[Medline]
  3. Kwong YL, Chan ACL, Liang R, Chiang AKS, Chim CS, Chan TK. CD56+ NK lymphomas: clinicopathologic features and prognosis. Br J Haematol 1997;97: 821 -829[Medline]
  4. Cheung MMC, Chan JKC, Lau WH, et al. Primary non-Hodgkin's lymphoma of the nose and nasopharynx: clinical features, tumor immunophenotype, and treatment outcome in 113 patients. J Clin Oncol 1998;16: 70 -77[Abstract/Free Full Text]
  5. Eichel BS, Harrison EG, Devine KD, Scanlon PW, Brown HA. Primary lymphoma of the nose including a relationship to lethal midline granuloma. Am J Surg 1996;112: 597 -605
  6. Stewart JP. Progressive lethal granulomatous ulceration of the nose. J Laryngol Otol 1993;48: 657 -701
  7. Jaffe ES. Classification of natural killer (NK) cell and NK-like T-cell malignancies. Blood 1996;87: 1207 -1210[Free Full Text]
  8. Robbins KT, Fuller M, Vlasak M, et al. Primary lymphomas of the nasal cavity and paranasal sinuses. Cancer 1985;56: 814 -819[Medline]
  9. Marsot-Dupuch K, Cabane J, Raveau V, Aoun N, Tubiana JM. Lethal midline granuloma: impact of imaging studies on the investigation and management of destructive mid facial disease in 13 patients. Neuroradiology 1992;34: 155 -161[Medline]
  10. Kondo M, Hashimoto T, Shiga H, et al. Computed tomography of sinonasal non-Hodgkin lymphoma. J Comput Assist Tomogr 1984;8: 216 -219[Medline]
  11. Kondo M, Horiuchi M, Shiga H, et al. Computed tomography of malignant tumors of the nasal cavity and paranasal sinuses. Cancer 1982;50: 226 -231[Medline]
  12. Centeno RS, Bentson JR, Mancuso AA. CT scanning in rhinocerebral mucormycosis and aspergillosis. Radiology 1981;140: 383 -389[Abstract/Free Full Text]

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