DIAGNOSIS ISSUES FOR SINONASAL TRACT LYMPHOMA: REVIEW OF LITERATURE AND CLINICAL CASE

DOI: 10.22138/2500-0918-2024-21-4-346-366

E.R. Sharipova¹, T.M. Yanborisov¹, E.E. Savelyeva¹,
A.T. Mugallimov², D.Yu. Semenova¹

¹Bashkir State Medical University of the Ministry of Health of the Russian Federation, Ufa, Russian Federation;
²Educational and Methodical Center for Quality and Safety in Medicine of G.G. Kuvatov State Medical University, Ufa, Russian Federation

Abstract. The paper presents the analysis of sinonasal lymphomas including epidemiological aspects of this disease, predisposing factors for its occurrence, clinical manifestations, methods of diagnosis and treatment. The purpose of scientific research: to analyze the most common lymphomas of the nose and paranasal sinuses – sinonasal diffuse large B-cell lymphoma and sinonasal natural killer/T-cell lymphoma. Material and methods. We analyzed modern data from Russian and foreign researchers and a clinical case that occurred in the department of otorhinolaryngology of the G.G.Kuvatov Republican Clinical Hospital of Ufa to study sinonasal lymphomas. The results of the study showed how nonspecific the picture of this disease is and what sometimes unobvious clinical approaches it requires. Sinonasal lymphomas is a multidisciplinary problem: it is difficult to suspect a tumor for any doctor who is approached by patients with symptoms caused by it. Despite the predominance of ophthalmological complaints, knowledge about the clinical manifestations of the tumor can lead the otorhinolaryngologist to think about this pathology. Conclusion. Thus, the role of the otorhinolaryngologist in making a timely diagnosis can be decisive: the possibility and effectiveness of antitumor treatment, and therefore life expectancy and quality of the patient may depend on him.

Keywords: sinonasal lymphoma, sinonasal diffuse large B-cell lymphoma, sinonasal NK/T-cell lymphoma

There is no conflict of interest.
Contact details of the corresponding author:
Elmira R. Sharipova
рeppy14@rambler.ru
Received: 01.09.2024
For citation: Sharipova E.R., Yanborisov T.M., Savelyeva E.E., Mugallimov A.T., Semenova D.Yu. Diagnosis issues for sinonasal tract lymphoma: review of literature and clinical case. [Online] Vestn. Ural. Med. Akad. Nauki. = Journal of Ural Medical Academic Science. 2024, Vol. 21, no. 4, pp. 346–366. DOI: 10.22138/2500-0918-2024-21-4-346-366 (In Russ)

REFERENCES
1. Jamil A., Mukkamalla S.K.R. Lymphoma. Treasure Island (FL): StatPearls Publishing, 2024; PMID: 32809661.
2. Lewis W.D., Lilly S., Jones K.L. Lymphoma: Diagnosis and Treatment. Am Fam Physician. 2020; 101(1):34-41.
3. Isaacson P.G., Chott A., Nakamura S., Muller-Hermelink H.K., Harris N.L., Swerdlow S.H. Extranodal marginal zone lymphoma of mucosaassociated lymphoid tissue (MALT lymphoma) In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al., editors. WHO classification of tumours of haematopoietic and lymphoid tissues. Lyon: IARC, 2008; 214–7.
4. Shirazi N., Bist S.S., Puri N., Harsh M., Ahmad S. Primary sinonasal lymphoma in immunocompetent patients: A 10 years retrospective clinicopathological study. J Oral Maxillofac Pathol. 2018; 22(2):280-281. doi:10.4103/jomfp.JOMFP_45_17.
5. Chiu B.C., Hou N. Epidemiology and etiology of non-hodgkin lymphoma. Cancer Treat Res. 2015; 165:1-25. doi:10.1007/978-3-319-13150-4_1.
6. Evans L.S., Hancock B.W. NonHodgkin lymphoma. Lancet. 2003; 362(9378):139–46. doi:10.1016/S01406736(03)138688.
7. Peng K.A., Kita A.E., Suh J.D. et al. Sinonasal lymphoma: case series and review of the literature. Int Forum Allergy Rhinol. 2014; 4(8):670–4. doi:10.1002/alr.21337.
8. Lund V.J., Stammberger H., Nicolai P., Castelnuovo P., Beal T., Beham A., Bernal-Sprekelsen M., Braun H., Cappabianca P., Carrau R., Cavallo L., Clarici G., Draf W., Esposito F., Fernandez-Miranda J., Fokkens W., Gardner P., Gellner V., Hellquist H., Hermann P., Hosemann W., Howard D., Jones N., Jorissen M., Kassam A., Kelly D., Kurschel-Lackner S., Leong S., McLaughlin N., Maroldi R., Minovi A., Mokry M., Onerci M., Ong Y.K., Prevedello D., Saleh H., Sehti D.S., Simmen D., Snyderman C., Solares A., Spittle M., Stamm A., Tomazic P., Trimarchi M., Unger F., Wormald P.J., Zanation A.; European Rhinologic Society Advisory Board on Endoscopic Techniques in the Management of Nose, Paranasal Sinus and Skull Base Tumours. European position paper on endoscopic management of tumours of the nose, paranasal sinuses and skull base. Rhinol Suppl. 2010; 22:1-143.
9. Vidal R.W., Devaney K., Rinaldo A. et al. Sinonasal malignant lymphomas: a distinct clinicopathological category. Ann OtolRhinol Laryngol. 1999; 108(4):411–9. doi:10.1177/000348949910800417.
10. Eide J.G., Kshirsagar R.S., Birkenbeuel J.L., Abello E.H., Hobday S., Herzberg S., Wang B.Y., Palmer J.N., Adappa N.D., Kuan E.C. Primary sinonasal lymphoma: A multi-institutional experience of clinical presentation, treatment, and outcomes. Int Forum Allergy Rhinol. 2023; 13:1492–502. doi:10.1002/alr.23102.
11. Takahara M., Kishibe K., Bandoh N., Nonaka S., Harabuchi Y. P53, N- and K-Ras, and beta-catenin gene mutations and prognostic factors in nasal NK/T-cell lymphoma from Hokkaido, Japan. Hum Pathol. 2004; 35:86-95.
12. Brown H.J., Varelas E.A., Ganti A., Papagiannopoulos P., Mark M., Kuan E.C., Tajudeen B.A. Prognostic Indicators of Survival in Sinonasal Diffuse Large B-Cell Lymphoma: A National Cancer Database Analysis. Laryngoscope. 2022; 132(8):1515-1522. doi:10.1002/lary.29864.
13. Dubal P.M., Dutta R., Vazquez A., Patel T.D., Baredes S., Eloy J.A. Acomparative population-based analysis of sinonasal diffuse largeB-cell and extranodal NK/T-cell lymphomas. Laryngoscope. 2015; 125:1077–83. doi:10.1002/lary.25111.
14. Hung L.Y., Chang P.H., Lee T.J., Hsu Y.P., Chen Y.W., Fu C.H., Huang C.C. Extranodal natural killer/T-cell lymphoma, nasal type: clinical and computed tomography findings in the head and neck region. Laryngoscope. 2012; 122(12):2632-9. doi:10.1002/lary.23531.
15. He M., Tang Z., Qiang J., Xiao Z., Zhang Z. Differentiation between sinonasal natural killer/T‐cell lymphomas and diffuse large B‐cell lymphomas by RESOLVE DWI combined with conventional MRI. Magn Reson Imaging. 2019; 62:10‐17. doi:10.1016/j.mri.2019.06.011.
16. Vazquez A., Khan M.N., Blake D.M., Sanghvi S., Baredes S., Eloy J.A. Extranodal natural killer/T-cell lymphoma: a population-based comparison of sinonasal and extranasal disease. Laryngoscope. 2014; 124:888-895. doi:10.1002/lary.24371.
17. Huang Y., Jia B., Jiang S., Zhou S., Yang J., Liu P., Gui L., He X., Qin Y., Sun Y., Shi Y. Different clinical characteristics and treatment strategies for patients with localized sinonasal diffuse large B cell lymphoma and extranodal NK/T cell lymphoma. J Hematol Oncol. 2017; 10(1):7. doi:10.1186/s13045-016-0368-9.
18. Vockerodt M., Yap L.F., Shannon-Lowe C., Curley H., Wei W., Vrzalikova K., Murray P.G. The Epstein-Barr virus and the pathogenesis of lymphoma. J Pathol. 2015; 235(2):312-22. doi:10.1002/path.4459.
19. Sehn L.H., Salles G. Diffuse Large B-Cell Lymphoma. N Engl J Med. 2021; 384(9):842-858. doi:10.1056/NEJMra2027612.
20. Cerhan J.R., Kricker A., Paltiel O., Flowers C.R., Wang S.S., Monnereau A., Blair A., Dal Maso L., Kane E.V., Nieters A., Foran J.M., Miligi L., Clavel J., Bernstein L., Rothman N., Slager S.L., Sampson J.N., Morton L.M., Skibola C.F. Medical history, lifestyle, family history, and occupational risk factors for diffuse large B-cell lymphoma: the InterLymph Non-Hodgkin Lymphoma Subtypes Project. J Natl Cancer Inst Monogr. 2014; 2014(48):15-25. doi:10.1093/jncimonographs/lgu010.
21. Shannon-Lowe C., Rickinson A.B., Bell A.I. Epstein-Barr virus-associated lymphomas. Philos Trans R Soc Lond B Biol Sci. 2017; 372(1732):20160271. doi:10.1098/rstb.2016.0271.
22. Gregory S. C, Wan-Ju L, Todd A. L, Glen T. S, Brian C-H. C. Risk of Non-Hodgkin Lymphoma Following Treatment of Inflammatory Conditions with Tumor Necrosis Factor-Alpha Inhibitors. Blood. 2015; 126 (23): 2653. doi:10.1182/blood.v126.23.2653.2653.
23. Shi X., Wallach J.D., Ma X., Rogne T. Autoimmune diseases and risk of non-Hodgkin lymphoma: A Mendelian randomisation study. medRxiv [Preprint]. 2024; 22:2024.01.20.24301459. doi:10.1101/2024.01.20.24301459.
24. Bitner B.F., Htun N.N., Wang B.Y., Brem E.A., Kuan E.C. Sinonasal lymphoma: A primer for otolaryngologists. Laryngoscope Investig Otolaryngol. 2022; 7(6):1712-1724. doi:10.1002/lio2.941.
25. Shah J.P., Patel S.G., Singh B., Wong R. Jatin Shah’s Head and Neck Surgery and Oncology. 5 ed. New York: Elsevier, 2019; 896.
26. Lombard M., Michel G., Rives P., Moreau A., Espitalier F., Malard O. Extranodal non‐Hodgkin lymphoma of the sinonasal cavities: a 22‐case report. Eur Ann Otorhinolaryngol Head Neck Dis. 2015;132(5):271‐274. doi:10.1016/j.anorl.2015.08.015.
27. Steele T.O., Buniel M.C., Mace J.C., El Rassi E., Smith T.L. Lymphoma of the Nasal Cavity and Paranasal Sinuses: A Case Series. American Journal of Rhinology & Allergy. 2016; 30(5):335-339. doi:10.2500/ajra.2016.30.4347.
28. Yen T.T., Wang R.C., Jiang R.S., Chen S.C., Wu S.H., Liang K.L. The diagnosis of sinonasal lymphoma: a challenge for rhinologists. Eur Arch Oto‐Rhino‐Laryngol. 2012; 269(5):1463‐1469. doi:10.1007/s00405-011-1839-9.
29. Goldenberg D., Golz A., Fradis M., Mârtu D., Netzer A., Joachims H.Z. Malignant tumors of the nose and paranasal sinuses: a retrospective review of 291 cases. Ear Nose Throat J. 2001; 80(4):272‐277. doi:10.1177/014556130108000417.
30. Tanaka H., Mori E., Akutsu T., Saito S., Tei M., Otori N. Characteristics of Extranodal NK/T-Cell Lymphoma, Nasal Type, Compared with Nasal Diffuse Large B-cell Lymphoma. Clin Med Insights Oncol. 2023; 17:11795549231156692. doi:10.1177/11795549231156692.
31. Yasumoto M., Taura S., Shibuya H., Honda M. Primary malignant lymphoma of the maxillary sinus: CT and MRI. Neuroradiology. 2000; 42:285 9.
32. Lee G.W., Go S.I., Kim S.H., Hong J., Kim Y.R., Oh S., Kim S.Y., Do Y.R., Lee H., Lee S.I., Bae S.H., Oh S.Y., Song M.K., Lee W.S., Lee B., Kim J.S., Kim M.K., Kang H.J., Ahn J.S., Yhim H.Y., Kim H.J., Kim S.J., Kim W.S., Suh C.; Consortium for Improving Survival of Lymphoma (CISL) study group. Clinical outcome and prognosis of patients with primary sinonasal tract diffuse large B-cell lymphoma treated with rituximab-cyclophosphamide, doxorubicin, vincristine and prednisone chemotherapy: a study by the Consortium for Improving Survival of Lymphoma. Leuk Lymphoma. 2015; 56(4):1020-6. doi:10.3109/10428194.2014.946027.
33. Cho H.J., Jang M.S., Hong S.D., Kim S.J., Ahn Y.C., Oh D., Ko Y.H., Kim H.Y., Dhong H.J., Chung S.K., Kim W.S. Nasal endoscopic evaluation and its impact on survival in patients with stage I/II extranodal natural killer/T-cell lymphoma, nasal type. Int Forum Allergy Rhinol. 2015; 5(10):960-6. doi:10.1002/alr.21564.
34. Woo J.S., Kim J.M., Lee S.H., Chae S.W., Hwang S.J., Lee H.M. Clinical analysis of extranodal non‐Hodgkin’s lymphoma in the sinonasal tract. Eur Arch Oto‐Rhino‐Laryngol. 2004; 261(4):197‐201. doi:10.1007/s00405-003-0627-6.
35. Li S., Young K.H., Medeiros L.J. Diffuse large B‐cell lymphoma. Pathology. 2018; 50(1):74‐87. doi:10.1016/j.pathol.2017.09.006.
36. Brudno J., Tadmor T., Pittaluga S., Nicolae A., Polliack A., Dunleavy K. Discordant bone marrow involvement in non‐Hodgkin lymphoma. Blood. 2016; 127(8):965‐970. doi:10.1182/blood-2015-06-651968.
37. Loddenkemper C., Anagnostopoulos I., Hummel M., Jöhrens-Leder K., Foss H.D., Jundt F., Wirth T., Dörken B., Stein H. Differential Emu enhancer activity and expression of BOB.1/OBF.1, Oct2, PU.1, and immunoglobulin in reactive B-cell populations, B-cell non-Hodgkin lymphomas, and Hodgkin lymphomas. J Pathol. 2004; 202(1):60-9. doi:10.1002/path.1485.
38. Azarpira N., Ashraf M.J., Monabati A., Makarempour A., Khademi B., Hakimzadeh A., Abedi E., Valibeigi B. Primary lymphoma of nasal cavity and paranasal sinuses. Lab Med. 2012; 43(6):294‐299. doi:10.1309/LMKH083QCXFUUIGS.
39. Suzuki R., Takeuchi K., Ohshima K., Nakamura S. Extranodal NK/T‐cell lymphoma: diagnosis and treatment cues. Hematol Oncol. 2008; 26(2):66‐72. doi:10.1002/hon.847.
40. McKelvie P.A., Climent F., Krings G., Hasserjian R.P., Abramson J.S., Pilch B.Z., Harris N.L., Ferry J.A., Zukerberg L.R., Sohani A.R. Small-cell predominant extranodal NK/T cell lymphoma, nasal type: clinicopathological analysis of a series of cases diagnosed in a Western population. Histopathology. 2016; 69(4):667-79. doi:10.1111/his.12990.
41. Lisowska G., Zięba N., Stryjewska‐Makuch G., Ścierski W., Miśkiewicz‐Orczyk K., Misiołek M. Natural killer (NK)//T‐cell lymphoma, nasal type, with periorbital involvement: a case report and literature review. Am J Case Rep. 2020; 21:1‐7. doi:10.12659/AJCR.926599.
42. Tu Z., Xiao Z., Zheng Y., Huang H., Yang L., Cao D. Benign and malignant skull‐involved lesions: discriminative value of conventional CT and MRI combined with diffusion‐weighted MRI. Acta Radiol. 2019; 60(7):880‐886. doi:10.1177/0284185118773541.
43. Nakamura K., Uehara S., Omagari J., Kunitake N., Kimura M., Makino Y., Murakami J., Jingu K., Masuda K. Primary non-Hodgkin lymphoma of the sinonasal cavities: correlation of CT evaluation with clinical outcome. Radiology. 1997; 204(2):431-5. doi:10.1148/radiology.204.2.9240531.
44. Yasumoto M., Taura S., Shibuya H., Honda M. Primary malignant lymphoma of the maxillary sinus: CT and MRI. Neuroradiology. 2000; 42(4):285‐289. doi:10.1007/s002340050887.
45. Gufler H., Laubenberger J., Gerling J., Nesbitt E., Kommerell G., Langer M. MRI of lymphomas of the orbits and the paranasal sinuses. J Comput Assist Tomogr. 1997; 21(6):887‐891. doi:10.1097/00004728-199711000-00007.
46. King A.D., Lei K.I.K., Ahuja A.T., Lam W.W.M., Metreweli C. MR imaging of nasal T‐cell/natural killer cell lymphoma. Am J Roentgenol. 2000; 174(1):209‐211. doi:10.2214/ajr.174.1.1740209.
47. Sandner A., Surov A., Bach A.G., Kösling S. Primary extranodal non‐Hodgkin lymphoma of the orbital and paranasal region – a retrospective study. Eur J Radiol. 2013; 82(2):302‐308. doi:10.1016/j.ejrad.2012.03.036.
48. Koch B.L., Hamilton B.E., Hudgins P.A., Harnsberger H.R. Diagnostic Imaging: Head and Neck. Elsevier. 2017; 1247. doi:10.1016/B978-0-323-44301-2.50421-3.
49. Ooi G.C., Tsang K.W.T. Nasal T‐cell/natural killer cell lymphoma: CT and MR imaging features of a new clinicopathologic entity. AJR Am J Roentgenol. 2000; 174:1141‐1145. doi:10.2214/ajr.174.4.1741141.
50. Han M.H., Chang K.H., Kim I.O., Kim D.K., Han M.C.. Non‐Hodgkin lymphoma of the central skull base: MR manifestations. J Comput Assist Tomogr. 1993; 17(4):567‐571. doi:10.1097/00004728-199307000-00009.
51. Hen Y., Wang X., Li L., Li W., Xian J. Differential diagnosis of sinonasal extranodal NK/T cell lymphoma and diffuse large B cell lymphoma on MRI. Neuroradiology. 2020; 62(9):1201. doi:10.1007/s00234-020-02488-8.
52. Hsu Y.‐P., Chang P.‐H., Lee T.‐J., Hung L.‐Y., Huang C.‐C. Extranodal natural killer/T‐cell lymphoma nasal type: detection by computed tomography features. Laryngoscope. 2014; 124(12):2670‐2675. doi:10.1002/lary.24876.
53. Wang X., Zhang Z., Chen Q., Li J., Xian J. Effectiveness of 3 T PROPELLER DUO diffusion‐weighted MRI in differentiating sinonasal lymphomas and carcinomas. Clin Radiol. 2014; 69(11):1149‐1156. doi:10.1016/j.crad.2014.07.003.
54. Cheson B.D., Fisher R.I., Barrington S.F., Cavalli F., Schwartz L.H., Zucca E., Lister T.A.; Alliance, Australasian Leukaemia and Lymphoma Group; Eastern Cooperative Oncology Group; European Mantle Cell Lymphoma Consortium; Italian Lymphoma Foundation; European Organisation for Research; Treatment of Cancer/Dutch Hemato-Oncology Group; Grupo Español de Médula Ósea; German High-Grade Lymphoma Study Group; German Hodgkin’s Study Group; Japanese Lymphorra Study Group; Lymphoma Study Association; NCIC Clinical Trials Group; Nordic Lymphoma Study Group; Southwest Oncology Group; United Kingdom National Cancer Research Institute. Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol. 2014; 32(27):3059-68. doi:10.1200/JCO.2013.54.8800.
55. Yamaguchi M., Miyazaki K. Current treatment approaches for NK/T‐cell lymphoma. J Clin Exp Hematop. 2017; 57(3):98‐108. doi:10.3960/jslrt.17018.
56. Barrington S.F., Mikhaeel N.G., Kostakoglu L., Meignan M., Hutchings M., Müeller S.P., Schwartz L.H., Zucca E., Fisher R.I., Trotman J., Hoekstra O.S., Hicks R.J., O’Doherty M.J., Hustinx R., Biggi A., Cheson B.D. Role of imaging in the staging and response assessment of lymphoma: consensus of the International Conference on Malignant Lymphomas Imaging Working Group. J Clin Oncol. 2014; 32(27):3048-58. doi:10.1200/JCO.2013.53.5229.
57. Kharuzhyk S.A., Zhavrid E.A., Dzyuban A.V., Poddubnyy K.V., Sukolinskaya E.V., Kalenik O.A. Whole-Body Diffusion-Weighted Magnetic Resonance Imaging and Positron Emission Tomography Combined with Computed Tomography in the Staging of Lymphomas [Diffuzionno-vzveshennaja magnitno-rezonansnaja tomografija vsego tela i pozitronnaja jemissionnaja tomografija, kombinirovannaja s komp’juternoj tomografiej, pri stadirovanii limfom]. Journal of radiology and nuclear medicine= Vestnik rentgenologii i radiologii. 2019; 100(6):321-334. (In Russ). doi:10.20862/0042-4676-2019-100-6-321-334.
58. Cheson B.D., Fisher R.I., Barrington S.F., Cavalli F., Schwartz L.H., Zucca E., Lister T.A.; Alliance, Australasian Leukaemia and Lymphoma Group; Eastern Cooperative Oncology Group; European Mantle Cell Lymphoma Consortium; Italian Lymphoma Foundation; European Organisation for Research; Treatment of Cancer/Dutch Hemato-Oncology Group; Grupo Español de Médula Ósea; German High-Grade Lymphoma Study Group; German Hodgkin’s Study Group; Japanese Lymphorra Study Group; Lymphoma Study Association; NCIC Clinical Trials Group; Nordic Lymphoma Study Group; Southwest Oncology Group; United Kingdom National Cancer Research Institute. Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol. 2014; 32(27):3059-68. doi:10.1200/JCO.2013.54.8800.
59. Kanumuri V.V., Khan M.N., Vazquez A., Govindaraj S., Baredes S., Eloy J.A. Diffuse large B-cell lymphoma of the sinonasal tract: analysis of survival in 852 cases. Am J Otolaryngol — Head Neck Med Surg. 2014; 35(2):154-158.

Authors

Elmira R. Sharipova
Bashkir State Medical University of the Ministry of Health of the Russian Federation
PhD, Associate Professor of the Department of Otorhinolaryngology
Ufa, Russian Federation
рeppy14@rambler.ru
ORCID 0009-0002-1402-8541

Timur M. Yanborisov
Bashkir State Medical University of the Ministry of Health of the Russian Federation
PhD, Associate Professor of the Department of Otorhinolaryngology
Ufa, Russian Federation
timurlor@gmail.com
ORCID 0009-0003-2885-4454

Elena E. Savelyeva
Bashkir State Medical University of the Ministry of Health of the Russian Federation
DM, Associate Professor, Head of the Department of Otorhinolaryngology
Ufa, Russian Federation
surdolog@yandex.ru
ORCID 0000-0002-2009-8469
Artur T. Mugallimov
Educational and Methodical Center for Quality and Safety in Medicine of G.G.Kuvatov State Medical University
Head of the Department of Otorhinolaryngology
Ufa, Russian Federation
glavbuh-89@mail.ru
ORCID 0009-0001-8962-4666

Daria Yu. Semenova
Bashkir State Medical University of the Ministry of Health of the Russian Federation
Resident at the Department of Otorhinolaryngology
Ufa, Russian Federation
drlordaria@gmail.com
ORCID 0009-0005-7726-7509