Head and Neck Epstein-Barr Virus Mucocutaneous Ulcer: Case Report and Literature Review
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1 The Laryngoscope VC 2016 The American Laryngological, Rhinological and Otological Society, Inc. Case Report Head and Neck Epstein-Barr Virus Mucocutaneous Ulcer: Case Report and Literature Review Joshua K. Au, MD; Jonathan W. Said, MD; Ali R. Sepahdari, MD; Maie A. St. John, MD, PhD Objectives/Hypothesis: To report the clinical presentation, treatment, and management outcomes of patients with Epstein-Barr virus-positive mucocutaneous ulcer (EBVMCU) of the head and neck, which is a newly characterized pathologic entity with aggressive morphology but follows an indolent, self-limiting clinical course. Study Design: Case report and literature review. Methods: A case of EBVMCU of the base of tongue is reported and a retrospective review of all cases of EBVMCU of the head and neck at a single academic institution was conducted between January 1, 1986 and April 1, The MEDLINE database was additionally queried from January 1, 1950 to April 1, 2015 for all reports of EBVMCU of the head and neck, and all pertinent clinical data were extracted. Results: The clinical presentation, treatment, and response of a patient with EBVMCU of the base of tongue are presented. Interim follow-up of the patient has revealed a complete remission with discontinuation of immunosuppression and therapy. A review of the literature supports conservative management and reduction of immunosuppression. Overall, 96.6% of patients with follow-up greater than 2 months achieved complete remission with conservative management. The current study is the largest series to report on the clinical presentation and treatment outcomes of EBVMCU of the head and neck. Conclusions: EBVMCU tends to follow an indolent and self-limiting clinical course, responding to reduction of immunosuppression and conservative treatment. It is imperative for clinicians to consider EBVMCU in the differential diagnosis of mucocutaneous ulcers of the head and neck to avoid excessive treatment. Key Words: Epstein-Barr virus, Epstein-Barr virus mucocutaneous ulcer. Laryngoscope, 126: , 2016 From the Department of Head and Neck Surgery (J.K.A., M.A.S.), University of California Los Angeles Medical Center, Los Angeles, California; Department of Pathology and Laboratory Medicine (J.W.S.), University of California Los Angeles Medical Center Medical Center, Los Angeles, California; University of California Los Angeles Head and Neck Cancer Program (J.W.S., A.R.S., M.A.S.), University of California Los Angeles David Geffen School of Medicine, Los Angeles, California; Department of Radiology (A.R.S.), University of California Los Angeles Medical Center, Los Angeles, California; Jonsson Comprehensive Cancer Center (J.W.S., M.A.S.), University of California Los Angeles, David Geffen School of Medicine, Los Angeles, California. Editor s Note: This Manuscript was accepted for publication March 7, Part of this study was presented as a poster at the Combine Sections Meeting of the Triological Society, Miami Beach, Florida, U.S.A., January 22 24, The authors have no funding, financial relationships, or conflicts of interest to disclose. Send correspondence to Maie A. St. John, MD, UCLA Department of Head and Neck Surgery, Le Conte Ave, CHS , Los Angeles, CA mstjohn@mednet.ucla.edu DOI: /lary INTRODUCTION Epstein-Barr virus (EBV) infection is ubiquitous, affecting more than 90% of the world population. 1 Following primary infection, cell-mediated immunity prevents subsequent infection. However, the virus develops lifelong latency in the memory B cells. Immunosuppression allows EBV-infected cells to proliferate, resulting in a group of immunodeficiency-associated lymphoproliferative disorders. EBV-positive mucocutaneous ulcer (EBVMCU) is a recently described clinicopathologic diagnosis usually resulting from iatrogenic or age-related immunosuppression. 2 It presents as a well-circumscribed ulcer of the aerodigestive tract or skin. Histologic analysis usually reveals a polymorphous infiltrate of atypical large B cells and Hodgkin s or Reed-Sternberg like (HRS-like) cells. The condition tends to resolves spontaneously with reduction of the immunosuppression. We report a case of EBVMCU of the base of tongue that had evaded diagnosis by multiple tertiary referral centers and present a review of the known literature of EBVMCU of the head and neck. MATERIALS AND METHODS Case Report A 72-year-old female with a long-standing history of wellcontrolled Crohn s disease on azathioprine presented with a 6- month history of a base of tongue ulcerative mass with resultant progressive severe odynophagia requiring gastrostomy tube placement. Prior biopsies by head and neck surgeons at two
2 other tertiary referral centers did not demonstrate carcinoma but were otherwise inconclusive. A positron emission tomography (PET) scan revealed hypermetabolic lesions of the right base of tongue as well as the upper and lower lobes of the right lung. Directed deep biopsies of the base of tongue at the University of California Los Angeles (UCLA) revealed an atypical polymorphous lymphoid proliferation with CD20 and EBV-positive abnormal cells compatible with EBVMCU (Figs. 1A C). As the patient s Crohn s disease had been well controlled for years, her azathioprine was discontinued. She began a 2-month course of and acyclovir to prevent EBV viral shedding. Upon 3 month follow-up, the patient had resumed an oral diet. Computed tomography (CT) imaging of the neck and chest revealed resolution of her prior lesions (Figs. 2A F). Literature Review and Data Extraction The MEDLINE database was searched from January 1, 1950 to April 1, 2015 with key words Epstein-Barr virus and mucocutaneous ulcer. The search strategy aimed to identify all reported cases of EBVMCU of the head and neck. In addition, the UCLA Department of Pathology database was queried for all documented cases of EBVMCU of the head and neck between January 1, 1986 and April 1, Specifically, information regarding age, gender, presentation, site of lesions, treatment course, response to treatment, and duration of clinical follow-up was collected when available. RESULTS A total of 19 articles were culled from the MED- LINE search. Review of all 19 articles indicated that eight articles contained nonoverlapping patient case information and were included in the analysis. This collection yielded a total of 33 previously reported cases of EBVMCU of the head and neck in the literature. The UCLA Pathology Database query garnered two patients including the one reported. A total of 35 cases of EBVMCU of the head and neck were identified (Table I). Cases have been categorized as age-related or iatrogenically immunosuppressed. 2 The mean age in the immunosuppressed subgroup was less than the agerelated subgroup (59.9 vs. 78, P > 0.001). Females accounted for 63% of patients with EBVMCU of the head and neck. Half of the cases of EBVMCU of the head and neck were related to iatrogenic immunosuppression (18/35). The majority of cases of EBVMCU of the head and neck presented on mucosal surfaces (31/35, 89%), most commonly in the oral cavity and oropharynx. Five cases of cutaneous EBVMCU of the head and neck were reported, with the eyelid most commonly affected (2/5). One case presented with concurrent mucosal and skin lesions. Regional and distant disease was present including three advanced-age patients with cervical and two immunosuppressed patients with lung lesions. Overall, 96.6% of patients with follow-up greater than 2 months achieved complete remission. Of the 18 patients who were managed conservatively with reduction of immunosuppression or observation, 94.1% resulted in complete remission. Only one of these patients developed a relapsing-remitting clinical course. All 11 patients who were treated resulted in complete Fig. 1. (A) Histologic section showing epithelial ulceration and a dense atypical lymphoid infiltrate underlying the mucosa. Original magnification (B) Atypical lymphoid infiltrate showing pleomorphic lymphoid cells in a background of small lymphocytes and histiocytes. The infiltrate includes multinucleated cells, some of which resemble Hodgkin s or Reed-Sternberg cells. Original magnification (C) Section stained for Epstein-Barr virus (EBV)- encoded RNA (EBER) by in situ hybridization shows a spectrum of small and large cells staining positive for EBV. Original magnification [Color figure can be viewed in the online issue, which is available at remission. Treatment included chemotherapy (R-CHOP:, cyclophosphamide, doxorubicin, vincristine, and prednisolone) or radiation therapy among age- 2501
3 Fig. 2. (A) T1-weighted axial image magnetic resonance imaging (MRI) at initial presentation shows a large, infiltrative mass at the right base of tongue (short arrow). Local mass effect is noted (long arrow). (B) T1-weighted axial MRI image obtained 2 months after presentation shows a new region of ulceration (short double arrows). (C) Axial noncontrast computed tomography (CT) image obtained 3 months after presentation shows progressive and new posterior oropharyngeal wall soft tissue abnormality (*). (D) Axial fused CT 18Fluorinefluorodeoxyglucose positron emission tomography, obtained 6 months after presentation and 1 month prior to treatment, shows marked hypermetabolic activity within the regions of soft tissue abnormality seen in (A-C). (E) Axial contrast-enhanced CT image, obtained 1 month after treatment, shows right base of tongue scar-like retraction and resolution of posterior pharyngeal wall mass (short arrow) and lingual volume loss (long arrow). (F) Axial contrast-enhanced CT image, 3 months after treatment, shows stable findings. [Color figure can be viewed in the online issue, which is available at related EBVMCU patients, and or surgical excision among immunosuppressed EBVMCU patients. None of the patients in this cohort died of their disease, though five patients died from unrelated causes. There is no statistical difference in remission rates between conservative management and active treatment of EBVMCU of the head and neck (v , P 5.426). DISCUSSION EBVMCU is a recently proposed clinicopathologic diagnosis describing an immunosuppression-induced EBV-positive B-cell lymphoproliferative disorder with a mucosal or cutaneous well-circumscribed ulcer, a polymorphous background infiltrate, HRS-like cells, numerous T cells especially at the rim of the ulcer, and plasmacytoid apoptotic bodies. 2 An extensive review of the Western literature revealed 33 cases in the head and neck. With the addition of two cases from our institution, this current study is the largest series to report the characteristics of EBVMCU of the head and neck. As with all analyses conducted on EBVMCU, the current study is limited by the small sample size, precluding generalizable analysis beyond descriptive statistics The pathophysiology of the localized mucocutaneous ulcers in EBVMCU is not well understood. Within the head and neck, EBVMCU vastly favors ulceration of mucosal epithelium (89%), especially the oral cavity and oropharynx. It has been suggested that a reduction in immune surveillance against EBV in sites that are rich in EBV-infected B cells, such as Waldeyer s ring, may predispose the development of these lesions in these areas. 2 Other areas of mucosal ulceration include the tongue, buccal mucosa, tongue, and gingiva and may be subject to chronic irritation, resulting in ulceration and a localized proliferation of EBV-infected B cells. 3 Whereas local disease is the norm, 9% of patients presented with cervical and 6% presented with lung lesions consistent with an associated EBVrelated lymphoproliferative disorder. It is interesting to note that patients with associated cervical presented with ipsilateral lesions, suggesting the possibility of spread by vial lymphatic shedding. The diagnosis of EBVMCU requires correlation with clinical, morphologic, and immunophenotypic parameters. EBVMCU has distinctive clinicopathologic features including the appearance of a circumscribed superficial lesion, and characteristic architecture with a
4 TABLE I. EBVMCU of the Head and Neck: Patient Presentations, Treatments, and Outcomes. Case Age (yr) Gender Source of Immunosuppression Site of Lesions Treatment Outcome Follow-up (mo) Reference 1 72 F AZA Base of tongue, Ipsilateral lung Reduction of IS, CR 3 UCLA, case report 2 80 M MTX Tongue N/A N/A N/A Dojcinov M AZA Oral mucosa N/A N/A N/A Dojcinov F CSA Tongue Reduction of IS CR 24 Dojcinov F MTX Lip Reduction of IS CR 72 Dojcinov F AZA Esophagus Reduction of IS CR 17 Dojcinov F P Gingiva, ear skin, lung Reduction of IS, CR 24 Au M MMF, P Tongue Reduction of IS CR 15 Hart M MMF, P Esophagus Reduction of IS CR 16.5 Hart M MMF, P, T Tonsil Reduction of IS, CR 14 Hart F MMF, P, CSA Gingiva Reduction of IS CR 8 Hart M CSA, P Lip Reduction of IS, surgical excision CR 111 Hart F AZA, P Buccal mucosa Reduction of IS CR 13 McGinness F MTX Eyelid skin Reduction of IS CR 24 Yamakawa F MTX Buccal mucosa Reduction of IS ND 1 Yamakawa F MTX Eyelid skin Reduction of IS CR 37 Yamakawa M MMF Gingiva N/A N/A N/A Kanemitsu F MTX Floor of mouth Reduction of IS CR 12 Attard F Old age Base of tongue, bilateral cervical RT CR 9 UCLA M Old age Cheek skin None DNED 25 Dojcinov M Old age Lip None CR N/A Dojcinov F Old age Lip None RR N/A Dojcinov F Old age Base of tongue None DNED 24 Dojcinov F Old age Palate mucosa RT CR 60 Dojcinov M Old age Tonsil CT DNED 12 Dojcinov M Old age Base of tongue None CR 12 Dojcinov F Old age Tongue, floor of mouth None DNED 5 Dojcinov F Old age Tonsil, ipsilateral cervical CT CR 24 Dojcinov 2 and RT F Old age Base of tongue RT DNED 15 Dojcinov F Old age Tonsil N/A N/A N/A Dojcinov M Old age Tonsil, tongue None DNED 12 Dojcinov F Old age Tongue, ipsilateral cervical None CR 36 Dojcinov F Old age Tonsil RT CR 3 Dojcinov M Old age Base of tongue N/A N/A N/A Dojcinov F Old age Neck skin CT CR 24 Sadiku 9 AZA 5 azathioprine; CR 5 complete remission; CSA 5 cyclosporine; CT 5 chemotherapy; DNED 5 died, no evidence of disease; EBVMCU 5 Epstein- Barr virus-positive mucocutaneous ulcer; F 5 female; IS 5 immunosuppression; M 5 male; MMF 5 mycophenolate; MTX 5 methotrexate; N/A 5 not available; ND 5 not determined; P 5 prednisone; RR 5 relapsing remitting; RT 5 radiation therapy; T 5 tacrolimus; UCLA 5 University of California Los Angeles. well-demarcated base with inflammatory cells, particularly reactive T lymphocytes. 2 The atypical HRS-like cells in EBVMCU, which show reduced CD20 expression while retaining PAX5 positivity, are usually present in a polymorphic background, and may mimic classical Hodgkin s lymphoma (chl). Additionally, similar to HRS cells, the large blasts in EBVMCU may show loss of transcription factors such as Bob-1. However, clinically, 2503
5 chl generally presents with lymph node involvement, and rarely, if ever, primarily involves mucocutaneous surfaces. Unlike HRS cells, the blast cells in EBVMCU are usually positive for CD45. 2 Furthermore, in EBVMCU, the cell staining for CD20 and EBV-encoded RNA (EBER) by in situ hybridization range from small lymphocytes, immunoblasts, and large HRS-like cells; whereas, in chl, EBER is limited to the HRS cells, which are generally negative for CD20. 2 Finally, EBVMCU histologically observes plasmacytoid apoptotic bodies. This is in contrast to chl, in which EBV provides CD40-mediated survival stimuli, evading apoptosis. This final point suggests the persistence of normal cellular control mechanisms in EBVMCU, absent in EBV-positive lymphomas such as chl. 2 EBVMCU may occur in the post-transplant setting and may be considered a category of post-transplant lymphoproliferative disorder (PTLD). Hart et al. identified seven cases of EBVMCU (five of the head and neck) within a cohort of 70 immunosuppressed transplant recipients. Four patients, including two with EBVMCU of the head and neck, were previously diagnosed as monomorphic or polymorphic PTLD prior to recognizing the diagnosis as EBVMCU. 4 They noted the lack of quantifiable EBV viremia, despite strong EBER positivity in EBVMCU tissue, to be a statistically significant distinguishing feature of EBVMCU from other forms of PTLD. 4 This report suggests that EBVMCU may presently be misdiagnosed as other forms of PTLD in the post-transplant population, thereby under-reporting the prevalence of EBVMCU. Distinguishing EBVMCU from other forms of PTLD may prevent exposure of these patients from the unnecessary risks of chemotherapy. When possible, treatment outcomes overwhelmingly favor a conservative approach in EBVMCU of the head and neck, with an overall 96.6% complete remission rate. Additionally, 94.1% of those managed conservatively by reduction of immunosuppression or observation achieved complete remission. Such clinical behavior suggests that EBVMCU may develop in patients with a partial reduction in immunosurveillance over EBV, resulting in a localized proliferation, which is then sequestered by a brisk T-cell reaction and resolved by the natural wound-healing response when immunosuppression is reduced. 2 Patients under iatrogenic immunosuppression benefitted from the reduction of their immunosuppression with or without additional treatment. However, because this disorder appears to be self-limiting, and patients who are not treated with often achieve regression, some clinicians do not support molecular targeting agents like as primary therapy. Age-related EBVMCU patients elected for chemotherapy or radiation therapy with successful remission rates similar to conservative management by observation alone. These results suggest that treatments including, chemotherapy, and radiation therapy should be reserved for refractory cases in which a period of conservative management has been trialed. CONCLUSION Despite the paucity of EBVMCU in the medical literature, our patient case underlines the importance of recognizing the diagnosis of EBVMCU of the head and neck to avoid excessive and unnecessary treatment, as the lesions tend to follow an indolent and self-limiting clinical course. The lesions readily respond to reduction of immune suppression and conservative management. With this addition of two cases from our institution, this current study is, to date, the largest series to report on the clinical presentation and treatment outcomes of EBVMCU of the head and neck. As the diagnosis in the reported case was indeterminate upon review by two other tertiary care referral centers, it is imperative for clinicians to consider EBVMCU in the differential diagnosis of mucocutaneous ulcers of the head and neck and to manage patients accordingly. BIBLIOGRAPHY 1. Cohen J. Epstein-Barr virus infection. N Engl J Med 2000;343: Dojcinov S, Venkataraman G, Raffeld M, Pittaluga S, Jaffe E. EBV positive mucocutaneous ulcer a study of 26 cases associated with various sources of immunosuppression. Am J Surg Pathol 2010;34: McGinness J, Spicknall K, Mutasim D. Azathioprine-induced EBV-positive mucocutaneous ulcer. J Cutan Pathol 2012;39: Hart M, Thakral B, Yohe S, et al. EBV-positive mucocutaneous ulcer in organ transplant recipients. Am J Surg Pathol 2014;38: Au W, Loong F, Wan T, Tong A. Multi-focal EBV-mucocutaneous ulcer heralding late-onset T-cell immunodeficiency in a woman with lupus erythematosus. Int J Hematol 2011;94: Yamakawa N, Fujimoto M, Kawabata D, et al. A clinical, pathological, and genetic characterization of methotrexate-associated lymphoproliferative disorders. J Rheumatol 2013;41: Kanemitsu M, John D, Lim A, Jaffe E, Aoki J. Clonal Epstein-Barr viruspositive mucocutaneous ulcer mimicking a mature B-cell lymphoma in a patient with mycophenolate-induced immune suppression. Leuk Lymphoma 2015;56: Attard A, Praveen P, Dunn P, James G. Epstein-Barr virus-positive mucocutaneous ulcer of the oral cavity: the importance of having a detailed clinical history to reach a correct diagnosis. Oral Surg Oral Med Oral Pathol Oral Radiol 2012;114:e37 e Sadiku S, Kurshumliu F, Krasniqi X, et al. Age-related Epstein-Barr virus-positive cutaneous ulcer arising after a self-limited subcutaneous abscess: a case report. J Med Case Rep 2012;6:
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