582263
research-article2015
IJSXXX10.1177/1066896915582263International Journal of Surgical PathologyDi Napoli et al
Case Report
Nodular Lymphocyte-Predominant Hodgkin Lymphoma in a Warthin Tumor of the Parotid Gland: A Case Report and Literature Review
International Journal of Surgical Pathology 2015, Vol. 23(5) 419–423 © The Author(s) 2015 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1066896915582263 ijs.sagepub.com
Arianna Di Napoli, MD, PhD1, Giuseppe Mallel, MD1, Armando Bartolazzi, MD, PhD1, Elena Cavalieri, MD1, Roberto Becelli, MD1, Claudia Cippitelli, BS1, and Luigi Ruco, MD1
Abstract Hodgkin lymphoma (HL) associated with Warthin tumor (WT) is extremely rare, accounting for only 3 cases of classical HLs. Here, we report for the first time the occurrence of a nodular lymphocyte-predominant Hodgkin lymphoma (NLPHL) involving the lymphoid stroma of a WT of the parotid gland. Pathogenesis of WT is controversial, with both a nodal and a parenchymal possible origin. On the other hand, extranodal involvement by HLs is uncommon. In our case, the coexistence of a WT and of a NLPHL within its stroma and in cervical lymph node emphasizes the importance of a careful evaluation of the lymphoid tissue in WT in order to exclude the possibility of an associated lymphoid malignancy. Keywords nodular predominant Hodgkin lymphoma, Warthin tumor, parotid gland, collision tumor
Introduction Warthin tumor (WT) is a salivary gland adenoma, which occurs almost exclusively in the parotid gland. It is composed of a variable number of cysts lined by oncocytic bilayered epithelium forming papillae and lymphoid reactive stroma.1 Rarely, within WT, the epithelial benign component coexists with a lymphoma. To date, in the English literature, there are 26 reported cases of WT-associated lymphomas.2-22 Most of them are nonHodgkin B-cell lymphomas with a prevalence of follicular lymphomas.2,4-8,11,12,14,15 The simultaneous occurrence of Hodgkin lymphoma with WT is extremely rare with only 3 reported cases.9,13,21 All of them are classical Hodgkin lymphomas. We report the first case of nodular lymphocyte-predominant Hodgkin lymphoma (NLPHL) associated with a WT of the parotid gland.
Case Report A 73-year-old man was admitted to Sant’Andrea Hospital of Rome, Italy, because of a 2-month history of a painless left laterocervical mass with no other symptoms. Past clinical history consisted of a large bowel adenoma with low-grade dysplasia, 2 chondroid hamartomas of the left lung, a basal cell carcinoma of the chin region,
and hypertension. On physical examination the left parotid gland appeared to be considerably enlarged and a firm well-circumscribed mass was palpable in its context. Blood tests fell within normal ranges. The patient underwent surgical resection of the parotid mass including a single adjacent lymph node. The gross specimen consisted of a 4.5-cm well-circumscribed tumor of the left parotid, adjacent to a 1-cm lymph node. The specimens were formalin fixed and paraffin embedded for routine histological examination. Immunohistochemistry was performed with an automatic immunostainer (AutosteinerLink48, Dako, Glostrup, Denmark), using the following antibodies: CD20, CD79a, CD3, CD30, CD15, BCL6, EMA, CD10, CD21, LMP-1, Ki67 (Dako, Glostrup, Denmark), and PD1 (Abcam, Cambridge, UK). Histologically, the parotid lesion showed multiple papillae within cystic spaces composed of typical bilayered oncocytic epithelium and lymphoid stroma consistent with a Warthin Tumor (Figure 1). However, the lymphoid stroma 1
Sant’Andrea Hospital, Sapienza University, Rome, Italy
Corresponding Author: Arianna Di Napoli, Department of Clinical and Molecular Medicine, Pathology Unit, Sant’Andrea Hospital, Sapienza University of Rome, Via di Grottarossa 1035, 00189 Rome, Italy. Email:[email protected]
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International Journal of Surgical Pathology 23(5)
Figure 1. Warthin tumor of the parotid gland. Papillary epithelial projections into cystic spaces surrounded by lymphoid stroma (A, hematoxylin and eosin [H&E], 40×). Characteristic bilayered oncocytic columnar epithelium (B, H&E, 300×).
associated with the tumor was quite unusual; it was abundant with a vague nodularity (Figure 2A and B), and it was mainly composed of small lymphocytes intermingled with isolated large-size cells. The latter showed lobated nuclei with a “popcorn” appearance, prominent nucleoli, and scant cytoplasm reminiscent of lymphocyte-predominant cells (LP cells) (Figure 2C). Immunohistochemical analysis revealed that LP cells were positive for CD20, CD79a, BCL6, and EMA (Figure 2D-G), occasionally positive for CD30, negative for CD3, CD15, CD10, and LMP-1, and formed rosettes with PD1-positive reactive T cells (Figure 2H). A diagnosis of NLPHL coexisting with a WT of the parotid gland was made. The lymph node adjacent to the parotid gland was also found to be involved by NLPHL on histological examination. Computed tomography scan revealed the presence of multiple enlarged lymph nodes in the left submandibular and cervical region. Positron emission tomography examination showed high uptake of 18F-FDG in left cervical lymph nodes (maximum standardized uptake value [SUVmax] = 6.19) and in the right parotid gland (SUVmax = 5.49). Bone marrow biopsy showed no evidence of lymphoma infiltration. According to Ann Arbor staging system, the disease was considered to be stage IIA. The patient was treated with 6 doses of rituximab and radiotherapy and achieved complete remission.
Discussion Warthin tumor is the second most common benign tumor of the salivary glands accounting for 4% to 25% of all salivary gland neoplasms. It involves almost exclusively the parotid gland. It has a slight predilection for males (male to female ratio of about 1.3), and it is most frequently diagnosed in the fifth and sixth decade of life.1 Microscopically, WT is composed of a variable number of cysts lined by a tipical bilayered oncocytic epithelium surrounded by a
lymphoid stroma with frequent reactive follicular hyperplasia.1 Its pathogenesis is controversial and several theories have been proposed. The prevailing view is that WT derives from an entrapment of salivary duct remnants in an intraparotid or periparotid lymph node. In alternative, it was proposed that WT consists of a salivary duct proliferation capable of evoking a prominent lymphocyte reaction.1 The association of WT with a lymphoma is very rare, with only 26 reported cases in the English literature.2-22 Most cases were B cell lymphoma of follicular centre origin,2,4-8,11,12,14,15 with only 2 cases of T-cell lymphoma.17-20 MALT (mucosa-associated lymphoid tissue) B cell lymphomas were never observed in the lymphoid stroma of WT, whereas they are the most common tumor in salivary glands involved by autoimmune diseases.23-30 Indeed, only in a single case it was reported the coexistence of a synchronous WT and MALT lymphoma in the same parotid gland, but as distinct diseases.16 Altogether, these findings seem to indicate that the pathogenetic mechanisms leading to the development of a malignant lymphomas within the lymphoid stroma of a WT are different from those usually observed in autoimmune sialoadenitis. The presence of Hodgkin lymphoma (HL) in the lymphoid component of WT was reported in 3 cases and all of them were classified as classical HL (cHL).9,13,21 To the best of our knowledge, this is the first report of an association of WT with a NLPHL. Salivary gland involvement by NLPHL is exceedingly rare;32,33 in addition, most cases reported in the literature appeared to be confined to intra-glandular nodes, with no direct infiltration of the salivary gland.1 These findings seem to support the hypothesis that parotid HL is de facto a nodal-based disease. Intraglandular lymph nodes or WT lymphoid stroma might be either the site of origin of the lymphoma or the site of secondary involvement by disseminated disease.20,21 The possibility for the lymphoma to originate in the lymphoid tissue of WT
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Di Napoli et al
Figure 2. Nodular predominant Hodgkin lymphoma associated with Warthin tumor (WT) of the parotid gland. WT with a prominent vaguely nodular lymphoid stroma (A, hematoxylin and eosin [H&E], 6×). CD21 immunostaining highlights the follicular dendritic cells meshwork within the lymphoid nodules (B, 6×). Lymphocyte-predominant cells (C, H&E, 400×) stained for EMA (D, 400×), CD20 (E, 400×), CD79a (F, 400×), BCL6 (G, 400×), and surrounded by PD1-positive T-cell rosettes (H, 400×).
is supported by several reports indicating that WT-associated lymphoma may remain a localized disease for long periods of time.5-7,14-16,19 Concerning the site of origin of HL
evidences are inconclusive; in our case and in 2 of the 3 reported cases, the disease was simultaneously present in WT and in cervical lymph nodes9,21 whereas, in the
Downloaded from ijs.sagepub.com at DEAKIN UNIV LIBRARY on August 10, 2015
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remaining case it exclusively involved an intraparotid lymph node.13 In conclusion, the present study shows that the lymphoid stroma of WT may be the site of NLPHL and hence, it has to be carefully investigated, considering that the histological diagnosis of NLPHL may be very insidious especially in the context of another disease such as WT. Authors’ Note Authors Arianna Di Napoli and Giuseppe Mallel contributed equally to this work.
Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.
References 1. Ellis GL, Auclair PL. Tumors of the salivary glands. In: AFIP Atlas of Tumor Pathology. Silver Spring, MD: ARP Press; 2008:85-100. 2. Colby TV, Dorfman RF. Malignant lymphomas involving the salivary glands. Pathol Annu. 1979;14(pt 2):307-24. 3. Reiner M, Goldhirsch A, Luscieti PR, Pedrinis E, Kaplan E, Cavalli E. Warthin’s tumor with Sjogren’s syndrome and nonHodgink’s lymphoma. Ear Nose Throat J. 1979;58:345-350. 4. Seifert G, Bull HG, Donath K. Histologic subclassification of the cystoadenolymphoma of the parotid gland. Analysis of 275 cases. Virchows Arch A Pathol Anat Histol. 1980;388:13-38. 5. Miller R, Yanagihara ET, Dubrow AA, Lukes RJ. Malignant lymphoma in the Warthin’s tumor. Report of a case. Cancer. 1982;50:2948-2950. 6. Banik S, Howell JS, Wright DH. Non-Hodgkin’s lymphoma arising in adenolymphoma—a report of two cases. J Pathol. 1985;146:167-77. 7. Hall G, Tesluk H, Baron S. Lymphoma arising in an adenolymphoma. Hum Pathol. 1985;16:424-427. 8. Griesser GH, Hansmann ML, Bogman MJ, Pielsticker K, Lennert K. Germinal center derived malignant lymphoma in cystadenolymphoma. Virchows Arch A Pathol Anat Histol. 1986;408:491-496. 9. Melato M, Falconieri G, Fanin R, Baccarani M. Hodgink’s disease occurring in a Warthin’s tumor: first case report. Pathol Res Pract. 1986;181:615-620. 10. Bunker ML, Locker J. Warthin’s tumor with malignant lymphoma. DNA analysis of paraffin embedded tissue. Am J Clin Pathol. 1989;91:341-344. 11. Giardini R, Mastore M. Follicular non Hodgkin’s lymphoma in adenolymphoma: report of a case. Tumori. 1990;76: 212-215.
12. Medeiros LJ, Rizzi R, Lardelli P, Jaffe ES. Malignant lymphoma involving a Warthin’s tumor: a case with immunophenotypic and gene rearrangement analysis. Hum Pathol. 1990;21:974-977. 13. Badve S, Evans G, Mady S, Coppen M, Sloane J. A case of Warthin’s tumor with coexistent Hodgkin’s disease. Histopathology. 1993;22:280-281. 14. Shikhani AH, Shikhani LT, Kuhajda FP, Allam CK. Warthin’s tumor-associated neoplasms: report of two cases and review of the literature. Ear Nose Throat J. 1993;72: 264-269, 272-273. 15. Park CK, Manning JT Jr, Battifora H, Medeiros LJ. Follicle center lymphoma and Warthin tumor involving the same anatomic site. Report of two cases and review of the literature. Am J Clin Pathol. 2000;113:113-119. 16. Marioni G, Marchese-Ragona R, Marino F, et al. MALTtype lymphoma and Warthin’s tumor presenting in the same parotid gland. Acta Otolaryngol. 2004;124:318-323. 17. Pescarmona E, Perez M, Faraggiana T, Granati L, Baroni CD. Nodal peripheral T-cell lymphoma associated with Warthin’s tumor. Histopathology. 2005;47:221-222. 18. Saxena A, Memauri B, Hasegawa W. Initial diagnosis of small lymphocytic lymphoma in parotidectomy for Warthin tumor, a rare collision tumor. J Clin Pathol. 2005;58: 331-333. 19. Gorai S, Numata T, Kawada S, Nakano M, Tamaru J, Kobayashi T. Malignant lymphoma arising from heterotopic Warthin’s tumor in the neck: case report and review of the literature. Tohoku J Exp Med. 2007;212:199-205. 20. Giaslakiotis K, Androulaki A, Panagoulis G, et al. T cell lymphoblastic lymphoma in parotidectomy for Warthin’s tumor: case report and review of the literature. Int J Hematol. 2009;89:359-364. 21. Liu YQ, Tang QL, Wang LL, Liu QY, Fan S, Li HG. Concomitant lymphocyte-rich classical Hodgkin’s lymphoma and Warthin’s tumor. Oral Surg Oral Med Oral Pathol Oral Radiol. 2013;116:117-120. 22. Ozkök G, Taşlı F, Ozsan N, Oztürk R, Postacı H. Diffuse large B-cell lymphoma arising in Warthin’s tumor: case study and review of the literature. Korean J Pathol. 2013;47:579-582. 23. Paliga A, Farmer J, Bence-Bruckler I, Lamba M. Salivary gland lymphoproliferative disorders: a Canadian tertiary center experience. Head Neck Pathol. 2013;7:381-388. 24. Royer B, Cazals-Hatem D, Sibilia J, et al. Lymphomas in patients with Sjögren’s syndrome are marginal zone B-cell neoplasms, arise in diverse extranodal and nodal sites, and are not associated with viruses. Blood. 1997;90:766-775. 25. Dunn P, Kuo TT, Shih LY, et al. Primary salivary gland lymphoma: a clinicopathologic study of 23 cases in Taiwan. Acta Haematol. 2004;112:203-208. 26. Nakamura S, Ichimura K, Sato Y, et al. Follicular lymphoma frequently originates in the salivary gland. Pathol Int. 2006;56:576-583. 27. Kojima M, Shimizu K, Nishikawa M, et al. Primary salivary gland lymphoma among Japanese: a clinicopathological study of 30 cases. Leukemia Lymphoma. 2007;48: 1793-1798.
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Di Napoli et al 28. Roh JL, Huh J, Suh C. Primary non-Hodgkin’s lymphomas of the major salivary glands. J Surg Oncol. 2008;97: 35-39. 29. MacDermed D, Thurber L, George TI, Hoppe RT, Le QT. Extranodal nonorbital indolent lymphomas of the head and neck: relationship between tumor control and radiotherapy. Int J Radiat Oncol Biol Phys. 2004;59:788-795. 30. Triantafillidou K, Dimitrakopoulos J, Iordanidis F, Gkagkalis A. Extranodal non-Hodgkin lymphomas of the oral cavity and maxillofacial region: a clinical study of 58
cases and review of the literature. J Oral Maxillofac Surg. 2012;70:2776-2785. 31. Arida M, Barnes EL, Hunt JL. Molecular assessment of allelic loss in Warthin tumors. Mod Pathol. 2005;18: 964-948. 32. Yencha MW. Primary parotid gland Hodgkin’s lymphoma. Ann Otol Rhinol Laryngol. 2002;111:338-342. 33. Masuda M, Segawa Y, Joe AK, Hirakawa N, Komune S. A case of primary Hodgkin’s lymphoma of the parotid gland. Auris Nasus Larynx. 2008;35:440-442.
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research-article2015
IJSXXX10.1177/1066896915582263International Journal of Surgical PathologyDi Napoli et al
Case Report
Nodular Lymphocyte-Predominant Hodgkin Lymphoma in a Warthin Tumor of the Parotid Gland: A Case Report and Literature Review
International Journal of Surgical Pathology 2015, Vol. 23(5) 419–423 © The Author(s) 2015 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1066896915582263 ijs.sagepub.com
Arianna Di Napoli, MD, PhD1, Giuseppe Mallel, MD1, Armando Bartolazzi, MD, PhD1, Elena Cavalieri, MD1, Roberto Becelli, MD1, Claudia Cippitelli, BS1, and Luigi Ruco, MD1
Abstract Hodgkin lymphoma (HL) associated with Warthin tumor (WT) is extremely rare, accounting for only 3 cases of classical HLs. Here, we report for the first time the occurrence of a nodular lymphocyte-predominant Hodgkin lymphoma (NLPHL) involving the lymphoid stroma of a WT of the parotid gland. Pathogenesis of WT is controversial, with both a nodal and a parenchymal possible origin. On the other hand, extranodal involvement by HLs is uncommon. In our case, the coexistence of a WT and of a NLPHL within its stroma and in cervical lymph node emphasizes the importance of a careful evaluation of the lymphoid tissue in WT in order to exclude the possibility of an associated lymphoid malignancy. Keywords nodular predominant Hodgkin lymphoma, Warthin tumor, parotid gland, collision tumor
Introduction Warthin tumor (WT) is a salivary gland adenoma, which occurs almost exclusively in the parotid gland. It is composed of a variable number of cysts lined by oncocytic bilayered epithelium forming papillae and lymphoid reactive stroma.1 Rarely, within WT, the epithelial benign component coexists with a lymphoma. To date, in the English literature, there are 26 reported cases of WT-associated lymphomas.2-22 Most of them are nonHodgkin B-cell lymphomas with a prevalence of follicular lymphomas.2,4-8,11,12,14,15 The simultaneous occurrence of Hodgkin lymphoma with WT is extremely rare with only 3 reported cases.9,13,21 All of them are classical Hodgkin lymphomas. We report the first case of nodular lymphocyte-predominant Hodgkin lymphoma (NLPHL) associated with a WT of the parotid gland.
Case Report A 73-year-old man was admitted to Sant’Andrea Hospital of Rome, Italy, because of a 2-month history of a painless left laterocervical mass with no other symptoms. Past clinical history consisted of a large bowel adenoma with low-grade dysplasia, 2 chondroid hamartomas of the left lung, a basal cell carcinoma of the chin region,
and hypertension. On physical examination the left parotid gland appeared to be considerably enlarged and a firm well-circumscribed mass was palpable in its context. Blood tests fell within normal ranges. The patient underwent surgical resection of the parotid mass including a single adjacent lymph node. The gross specimen consisted of a 4.5-cm well-circumscribed tumor of the left parotid, adjacent to a 1-cm lymph node. The specimens were formalin fixed and paraffin embedded for routine histological examination. Immunohistochemistry was performed with an automatic immunostainer (AutosteinerLink48, Dako, Glostrup, Denmark), using the following antibodies: CD20, CD79a, CD3, CD30, CD15, BCL6, EMA, CD10, CD21, LMP-1, Ki67 (Dako, Glostrup, Denmark), and PD1 (Abcam, Cambridge, UK). Histologically, the parotid lesion showed multiple papillae within cystic spaces composed of typical bilayered oncocytic epithelium and lymphoid stroma consistent with a Warthin Tumor (Figure 1). However, the lymphoid stroma 1
Sant’Andrea Hospital, Sapienza University, Rome, Italy
Corresponding Author: Arianna Di Napoli, Department of Clinical and Molecular Medicine, Pathology Unit, Sant’Andrea Hospital, Sapienza University of Rome, Via di Grottarossa 1035, 00189 Rome, Italy. Email:[email protected]
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International Journal of Surgical Pathology 23(5)
Figure 1. Warthin tumor of the parotid gland. Papillary epithelial projections into cystic spaces surrounded by lymphoid stroma (A, hematoxylin and eosin [H&E], 40×). Characteristic bilayered oncocytic columnar epithelium (B, H&E, 300×).
associated with the tumor was quite unusual; it was abundant with a vague nodularity (Figure 2A and B), and it was mainly composed of small lymphocytes intermingled with isolated large-size cells. The latter showed lobated nuclei with a “popcorn” appearance, prominent nucleoli, and scant cytoplasm reminiscent of lymphocyte-predominant cells (LP cells) (Figure 2C). Immunohistochemical analysis revealed that LP cells were positive for CD20, CD79a, BCL6, and EMA (Figure 2D-G), occasionally positive for CD30, negative for CD3, CD15, CD10, and LMP-1, and formed rosettes with PD1-positive reactive T cells (Figure 2H). A diagnosis of NLPHL coexisting with a WT of the parotid gland was made. The lymph node adjacent to the parotid gland was also found to be involved by NLPHL on histological examination. Computed tomography scan revealed the presence of multiple enlarged lymph nodes in the left submandibular and cervical region. Positron emission tomography examination showed high uptake of 18F-FDG in left cervical lymph nodes (maximum standardized uptake value [SUVmax] = 6.19) and in the right parotid gland (SUVmax = 5.49). Bone marrow biopsy showed no evidence of lymphoma infiltration. According to Ann Arbor staging system, the disease was considered to be stage IIA. The patient was treated with 6 doses of rituximab and radiotherapy and achieved complete remission.
Discussion Warthin tumor is the second most common benign tumor of the salivary glands accounting for 4% to 25% of all salivary gland neoplasms. It involves almost exclusively the parotid gland. It has a slight predilection for males (male to female ratio of about 1.3), and it is most frequently diagnosed in the fifth and sixth decade of life.1 Microscopically, WT is composed of a variable number of cysts lined by a tipical bilayered oncocytic epithelium surrounded by a
lymphoid stroma with frequent reactive follicular hyperplasia.1 Its pathogenesis is controversial and several theories have been proposed. The prevailing view is that WT derives from an entrapment of salivary duct remnants in an intraparotid or periparotid lymph node. In alternative, it was proposed that WT consists of a salivary duct proliferation capable of evoking a prominent lymphocyte reaction.1 The association of WT with a lymphoma is very rare, with only 26 reported cases in the English literature.2-22 Most cases were B cell lymphoma of follicular centre origin,2,4-8,11,12,14,15 with only 2 cases of T-cell lymphoma.17-20 MALT (mucosa-associated lymphoid tissue) B cell lymphomas were never observed in the lymphoid stroma of WT, whereas they are the most common tumor in salivary glands involved by autoimmune diseases.23-30 Indeed, only in a single case it was reported the coexistence of a synchronous WT and MALT lymphoma in the same parotid gland, but as distinct diseases.16 Altogether, these findings seem to indicate that the pathogenetic mechanisms leading to the development of a malignant lymphomas within the lymphoid stroma of a WT are different from those usually observed in autoimmune sialoadenitis. The presence of Hodgkin lymphoma (HL) in the lymphoid component of WT was reported in 3 cases and all of them were classified as classical HL (cHL).9,13,21 To the best of our knowledge, this is the first report of an association of WT with a NLPHL. Salivary gland involvement by NLPHL is exceedingly rare;32,33 in addition, most cases reported in the literature appeared to be confined to intra-glandular nodes, with no direct infiltration of the salivary gland.1 These findings seem to support the hypothesis that parotid HL is de facto a nodal-based disease. Intraglandular lymph nodes or WT lymphoid stroma might be either the site of origin of the lymphoma or the site of secondary involvement by disseminated disease.20,21 The possibility for the lymphoma to originate in the lymphoid tissue of WT
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Figure 2. Nodular predominant Hodgkin lymphoma associated with Warthin tumor (WT) of the parotid gland. WT with a prominent vaguely nodular lymphoid stroma (A, hematoxylin and eosin [H&E], 6×). CD21 immunostaining highlights the follicular dendritic cells meshwork within the lymphoid nodules (B, 6×). Lymphocyte-predominant cells (C, H&E, 400×) stained for EMA (D, 400×), CD20 (E, 400×), CD79a (F, 400×), BCL6 (G, 400×), and surrounded by PD1-positive T-cell rosettes (H, 400×).
is supported by several reports indicating that WT-associated lymphoma may remain a localized disease for long periods of time.5-7,14-16,19 Concerning the site of origin of HL
evidences are inconclusive; in our case and in 2 of the 3 reported cases, the disease was simultaneously present in WT and in cervical lymph nodes9,21 whereas, in the
Downloaded from ijs.sagepub.com at DEAKIN UNIV LIBRARY on August 10, 2015
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International Journal of Surgical Pathology 23(5)
remaining case it exclusively involved an intraparotid lymph node.13 In conclusion, the present study shows that the lymphoid stroma of WT may be the site of NLPHL and hence, it has to be carefully investigated, considering that the histological diagnosis of NLPHL may be very insidious especially in the context of another disease such as WT. Authors’ Note Authors Arianna Di Napoli and Giuseppe Mallel contributed equally to this work.
Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.
References 1. Ellis GL, Auclair PL. Tumors of the salivary glands. In: AFIP Atlas of Tumor Pathology. Silver Spring, MD: ARP Press; 2008:85-100. 2. Colby TV, Dorfman RF. Malignant lymphomas involving the salivary glands. Pathol Annu. 1979;14(pt 2):307-24. 3. Reiner M, Goldhirsch A, Luscieti PR, Pedrinis E, Kaplan E, Cavalli E. Warthin’s tumor with Sjogren’s syndrome and nonHodgink’s lymphoma. Ear Nose Throat J. 1979;58:345-350. 4. Seifert G, Bull HG, Donath K. Histologic subclassification of the cystoadenolymphoma of the parotid gland. Analysis of 275 cases. Virchows Arch A Pathol Anat Histol. 1980;388:13-38. 5. Miller R, Yanagihara ET, Dubrow AA, Lukes RJ. Malignant lymphoma in the Warthin’s tumor. Report of a case. Cancer. 1982;50:2948-2950. 6. Banik S, Howell JS, Wright DH. Non-Hodgkin’s lymphoma arising in adenolymphoma—a report of two cases. J Pathol. 1985;146:167-77. 7. Hall G, Tesluk H, Baron S. Lymphoma arising in an adenolymphoma. Hum Pathol. 1985;16:424-427. 8. Griesser GH, Hansmann ML, Bogman MJ, Pielsticker K, Lennert K. Germinal center derived malignant lymphoma in cystadenolymphoma. Virchows Arch A Pathol Anat Histol. 1986;408:491-496. 9. Melato M, Falconieri G, Fanin R, Baccarani M. Hodgink’s disease occurring in a Warthin’s tumor: first case report. Pathol Res Pract. 1986;181:615-620. 10. Bunker ML, Locker J. Warthin’s tumor with malignant lymphoma. DNA analysis of paraffin embedded tissue. Am J Clin Pathol. 1989;91:341-344. 11. Giardini R, Mastore M. Follicular non Hodgkin’s lymphoma in adenolymphoma: report of a case. Tumori. 1990;76: 212-215.
12. Medeiros LJ, Rizzi R, Lardelli P, Jaffe ES. Malignant lymphoma involving a Warthin’s tumor: a case with immunophenotypic and gene rearrangement analysis. Hum Pathol. 1990;21:974-977. 13. Badve S, Evans G, Mady S, Coppen M, Sloane J. A case of Warthin’s tumor with coexistent Hodgkin’s disease. Histopathology. 1993;22:280-281. 14. Shikhani AH, Shikhani LT, Kuhajda FP, Allam CK. Warthin’s tumor-associated neoplasms: report of two cases and review of the literature. Ear Nose Throat J. 1993;72: 264-269, 272-273. 15. Park CK, Manning JT Jr, Battifora H, Medeiros LJ. Follicle center lymphoma and Warthin tumor involving the same anatomic site. Report of two cases and review of the literature. Am J Clin Pathol. 2000;113:113-119. 16. Marioni G, Marchese-Ragona R, Marino F, et al. MALTtype lymphoma and Warthin’s tumor presenting in the same parotid gland. Acta Otolaryngol. 2004;124:318-323. 17. Pescarmona E, Perez M, Faraggiana T, Granati L, Baroni CD. Nodal peripheral T-cell lymphoma associated with Warthin’s tumor. Histopathology. 2005;47:221-222. 18. Saxena A, Memauri B, Hasegawa W. Initial diagnosis of small lymphocytic lymphoma in parotidectomy for Warthin tumor, a rare collision tumor. J Clin Pathol. 2005;58: 331-333. 19. Gorai S, Numata T, Kawada S, Nakano M, Tamaru J, Kobayashi T. Malignant lymphoma arising from heterotopic Warthin’s tumor in the neck: case report and review of the literature. Tohoku J Exp Med. 2007;212:199-205. 20. Giaslakiotis K, Androulaki A, Panagoulis G, et al. T cell lymphoblastic lymphoma in parotidectomy for Warthin’s tumor: case report and review of the literature. Int J Hematol. 2009;89:359-364. 21. Liu YQ, Tang QL, Wang LL, Liu QY, Fan S, Li HG. Concomitant lymphocyte-rich classical Hodgkin’s lymphoma and Warthin’s tumor. Oral Surg Oral Med Oral Pathol Oral Radiol. 2013;116:117-120. 22. Ozkök G, Taşlı F, Ozsan N, Oztürk R, Postacı H. Diffuse large B-cell lymphoma arising in Warthin’s tumor: case study and review of the literature. Korean J Pathol. 2013;47:579-582. 23. Paliga A, Farmer J, Bence-Bruckler I, Lamba M. Salivary gland lymphoproliferative disorders: a Canadian tertiary center experience. Head Neck Pathol. 2013;7:381-388. 24. Royer B, Cazals-Hatem D, Sibilia J, et al. Lymphomas in patients with Sjögren’s syndrome are marginal zone B-cell neoplasms, arise in diverse extranodal and nodal sites, and are not associated with viruses. Blood. 1997;90:766-775. 25. Dunn P, Kuo TT, Shih LY, et al. Primary salivary gland lymphoma: a clinicopathologic study of 23 cases in Taiwan. Acta Haematol. 2004;112:203-208. 26. Nakamura S, Ichimura K, Sato Y, et al. Follicular lymphoma frequently originates in the salivary gland. Pathol Int. 2006;56:576-583. 27. Kojima M, Shimizu K, Nishikawa M, et al. Primary salivary gland lymphoma among Japanese: a clinicopathological study of 30 cases. Leukemia Lymphoma. 2007;48: 1793-1798.
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Di Napoli et al 28. Roh JL, Huh J, Suh C. Primary non-Hodgkin’s lymphomas of the major salivary glands. J Surg Oncol. 2008;97: 35-39. 29. MacDermed D, Thurber L, George TI, Hoppe RT, Le QT. Extranodal nonorbital indolent lymphomas of the head and neck: relationship between tumor control and radiotherapy. Int J Radiat Oncol Biol Phys. 2004;59:788-795. 30. Triantafillidou K, Dimitrakopoulos J, Iordanidis F, Gkagkalis A. Extranodal non-Hodgkin lymphomas of the oral cavity and maxillofacial region: a clinical study of 58
cases and review of the literature. J Oral Maxillofac Surg. 2012;70:2776-2785. 31. Arida M, Barnes EL, Hunt JL. Molecular assessment of allelic loss in Warthin tumors. Mod Pathol. 2005;18: 964-948. 32. Yencha MW. Primary parotid gland Hodgkin’s lymphoma. Ann Otol Rhinol Laryngol. 2002;111:338-342. 33. Masuda M, Segawa Y, Joe AK, Hirakawa N, Komune S. A case of primary Hodgkin’s lymphoma of the parotid gland. Auris Nasus Larynx. 2008;35:440-442.
Downloaded from ijs.sagepub.com at DEAKIN UNIV LIBRARY on August 10, 2015
