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Вопросы гематологии/онкологии и иммунопатологии в педиатрии. 2023; 22: 156-164

Прогрессивная трансформация герминативных центров или нодулярная лимфома Ходжкина с лимфоцитарным преобладанием? Вопросы дифференциальной диагностики на примере клинического случая

Сенченко М. А., Абрамов Д. С., Мякова Н. В., Коновалов Д. М.

https://doi.org/10.24287/1726-1708-2023-22-1-156-164

Аннотация

Прогрессивная трансформация герминативных центров (ПТГЦ) – доброкачественная реактивная лимфаденопатия, которая может быть самостоятельным заболеванием или возникать ассоциированно с другими лимфомами, самым частым вариантом из которых является нодулярная лимфома Ходжкина с лимфоцитарным преобладанием (НЛХЛП). На сегодняшний день окончательно не выяснено, как взаимосвязаны между собой ПТГЦ и НЛХЛП, несмотря на обилие представленных работ на эту тему. ПТГЦ может предшествовать НЛХЛП, возникать с ней синхронно или развиваться после проведенного курса терапии у пациентов с НЛХЛП. Несмотря на схожие клинико-морфологические признаки, подход к лечению и ведению пациентов отличается. В случае НЛХЛП одной из терапевтических опций является проведение химиотерапии, что не показано для пациентов с ПТГЦ. В настоящей статье представлен клинический случай парциального поражения лимфатического узла НЛХЛП, ассоциированной с ПТГЦ, на примере которого будут рассмотрены основные вопросы дифференциальной диагностики ПТГЦ и НЛХЛП. Пациент и его законные представители дали согласие на использование информации, в том числе фотографий ребенка, в научных исследованиях и публикациях.

Список литературы

1. Hicks J., Flaitz C. Progressive transformation of germinal centers: Review of histopathologic and clinical features. Int J Pediatr Otorhinolaryngol 2002; 65 (3): 195–202. DOI: 10.1016/S0165-5876(02)00176-3

2. Özkan M.C., Özsan N., Hekimgil M., Saydam G., Töbü M. Progressive Transformation of Germinal Centers: Single-Center Experience of 33 Turkish Patients. Clin Lymphoma Myeloma Leuk 2016; 16: S149–51. DOI: 10.1016/j.clml.2016.03.010

3. Kojima M., Nakamura S., Motoori T., Itoh H., Shimizu K., Yamane N., et al. Progressive transformation of germinal centers: A clinicopathological study of 42 Japanese patients. Int J Surg Pathol 2003; 11 (2): 101–7. DOI: 10.1177/106689690301100205

4. Furqan Shaikh R.G., Ngan B.-Y., Alexander S. Progressive transformation of germinal centers in children and adolescents: an intriguing cause of lymphadenopathy. Pediatr Blood Cancer 2013; 60 (1): 26–30. DOI: 10.1002/pbc.24234

5. Hansmann M.L., Fellbaum C., Hui P.K., Moubayed P. Progressive transformation of germinal centers with and without association to Hodgkin’s disease. Am J Clin Pathol 1990; 93 (2): 219–26. DOI: 10.1093/ajcp/93.2.219

6. Hartmann S., Winkelmann R., Metcalf R.A., Treetipsatit J., Warnke R.A., Natkunam Y., et al. Immunoarchitectural patterns of progressive transformation of germinal centers with and without nodular lymphocyte-predominant Hodgkin lymphoma. Hum Pathol 2015; 46 (11): 1655–61. DOI: 10.1016/j.humpath.2015.07.006

7. Lim M.S., Straus S.E., Dale J.K., Fleisher T.A., Stetler-Stevenson M., Strober W., et al. Pathological findings in human autoimmune lymphoproliferative syndrome. Am J Pathol 1998; 153 (5): 1541–50. DOI: 10.1016/S0002-9440(10)65742-2

8. Sato Y., Inoue D., Asano N., Takata K., Asaoku H., Maeda Y., et al. Association between IgG4-related disease and progressively transformed germinal centers of lymph nodes. Mod Pathol 2012; 25 (7): 956–67. DOI: 10.1038/modpathol.2012.54

9. Nguyen N.L., Ferry J.A., Harris N.L. Progressive Transformation of Germinal Centers and Nodular Lymphocyte Predominance Hodgkin’s Disease. Am J Surg Pathol 1999; 23 (1): 27–33.

10. Good D.J., Gascoyne R.D. Atypical Lymphoid Hyperplasia Mimicking Lymphoma. Hematol Oncol Clin North Am 2009; 23 (4): 729–45. DOI: 10.1016/j.hoc.2009.04.005

11. Nam-Cha S.H., Roncador G., SanchezVerde L., Montes-Moreno S., Acevedo A., Domínguez-Franjo P., et al. PD-1, A follicular T-cell marker useful for recognizing nodular lymphocyte-predominant Hodgkin lymphoma. Am J Surg Pathol 2008; 32 (8): 1252–7. DOI: 10.1097/PAS.0b013e318165b0d6

12. Braeuninger A., Küppers R., Strickler J.G., Wacker H.H., Rajewsky K., Hansmann M.L. Hodgkin and Reed-Sternberg cells in lymphocyte predominant Hodgkin disease represent clonal populations of germinal center-derived tumor B cells. Proc Natl Acad Sci U S A 1997; 94 (17): 9337–42. DOI: 10.1073/pnas.94.17.9337

13. Mason D.Y., Banks P.M., Chan J., Cleary M.L., Delsol G., de Wolf Peeters C., et al. Nodular lymphocyte predominance Hodgkin’s disease. A distinct clinicopathological entity. Am J Surg Pathol 1994; 18 (5): 526–30. DOI: 10.1097/00000478-199405000-00014

14. Uherova P., Valdez R., Ross C.W., Schnitzer B., Finn W.G. Nodular lymphocyte predominant Hodgkin lymphoma: An immunophenotypic reappraisal based on a single-institution experience. Am J Clin Pathol 2003; 119 (2): 192–8. DOI: 10.1309/38RK238FCDCH5R22

15. Falini B., Bigerna B., Pasqualucci L., Fizzotti M., Martelli M.F., Pileri S., et al. Distinctive expression pattern of the BCL-6 protein in nodular lymphocyte predominance Hodgkin’s disease. Blood 1996; 87 (2): 465–71. DOI: 10.1182/blood.v87.2.465.bloodjournal872465

16. Anagnostopoulos I., Hansmann M.L., Franssila K., Harris M., Harris N.L., Jaffe E.S., et al. European Task Force on Lymphoma project on lymphocyte predominance Hodgkin disease: Histologic and immunohistologic analysis of submitted cases reveals 2 types of Hodgkin disease with a nodular growth pattern and abundant lymphocytes. Blood 2000; 96 (5): 1889–99. DOI: 10.1182/blood.V96.5.1889

17. Kiil K., Bein J., Schuhmacher B., Thurner L., Schneider M., Hansmann M.-L., et al. A high number of IgG4-positive plasma cells rules out nodular lymphocyte predominant Hodgkin lymphoma. Virchows Arch 2018; 473 (6): 759–64. DOI: 10.1007/s00428-018-2460-8

18. Aguilera D.G., Vaklavas C., Tsimberidou A.M., Wen S., Medeiros L.J., Corey S.J. Pediatric therapy-related myelodysplastic syndrome/acute myeloid leukemia: the MD Anderson Cancer Center experience. J Pediatr Hematol Oncol 2009; 31 (11): 803–11. DOI: 10.1097/MPH.0b013e-3181ba43dc

19. Josting A., Wiedenmann S., Franklin J., May M., Sieber M., Wolf J., et al. Secondary myeloid leukemia and myelodysplastic syndromes in patients treated for Hodgkin’s disease: A report from the German Hodgkin’s Lymphoma Study Group. J Clin Oncol 2003; 21 (18): 3440–6. DOI: 10.1200/JCO.2003.07.160

20. Nogová L., Reineke T., Brillant C., Sieniawski M., Rüdiger T., Josting A., et al. Lymphocyte-predominant and classical Hodgkin’s lymphoma: A comprehensive analysis from the german Hodgkin study group. J Clin Oncol 2008; 26 (3): 434–9. DOI: 10.1200/JCO.2007.11.8869

21. Mauz-Körholz C., Gorde-Grosjean S., Hasenclever D., Shankar А., Dörffel W., Hamish Wallace W., et al. Resection alone in 58 children with limited stage, lymphocyte-predominant Hodgkin lymphoma-experience from the European network group on pediatric Hodgkin lymphoma. Cancer 2007; 110 (1): 179–85. DOI: 10.1002/cncr.22762

22. Mauz-Körholz C., Lange T., Hasenclever D., Burkhardt B., Feller A.C., Dörffel W., et al. Pediatric Nodular Lymphocyte-predominant Hodgkin Lymphoma: Treatment Recommendations of the GPOH-HD Study Group. Klin Padiatr 2015; 227 (6–7): 314–21. DOI: 10.1055/s-0035-1559664

23. Couronné L., Schneider P., Picquenot J.M., Laberge S., Bastard C., Vannier J.P. Refractory nodular lymphocyte predominant hodgkin lymphoma transformed to T-cell/histiocyte-rich B-cell lymphoma in an adolescent: Salvage therapy with allogeneic bone marrow transplantation. J Pediatr Hematol Oncol 2008; 30 (12): 959–62. DOI: 10.1097/MPH.0b013e31818a9564

24. Biasoli I., Stamatoullas A., Meignin V., Delmer A., Reman O., Morschhauser F., et al. Nodular, lymphocyte-predominant Hodgkin lymphoma: A long-term study and analysis of transformation to diffuse large B-cell lymphoma in a cohort of 164 patients from the adult lymphoma study group. Cancer 2010; 116 (3): 631–9. DOI: 10.1002/cncr.24819

25. Hall G.W., Katzilakis N., Pinkerton C.R., Nicolin G., Ashley S., McCarthy K., et al. Outcome of children with nodular lymphocyte predominant Hodgkin lymphoma – A Children’s Cancer and Leukaemia Group report. Br J Haematol 2007; 138 (6): 761–8. DOI: 10.1111/j.1365-2141.2007.06736.x

26. Shankar A., Hall G.W., Gorde-Grosjean S., Hasenclever D., Leblanc T., Hayward J., et al. Treatment outcome after low intensity chemotherapy [CVP] in children and adolescents with early stage nodular lymphocyte predominant Hodgkin’s lymphoma - An Anglo-French collaborative report. Eur J Cancer 2012; 48 (11): 1700–6. DOI: 10.1016/j.ejca.2011.10.018

Pediatric Hematology/Oncology and Immunopathology. 2023; 22: 156-164

Progressive transformation of germinal centers or nodular lymphocyte-predominant Hodgkin lymphoma? Issues of differential diagnosis: a clinical case

Senchenko M. A., Abramov D. S., Myakova N. V., Konovalov D. M.

https://doi.org/10.24287/1726-1708-2023-22-1-156-164

Abstract

Progressive transformation of germinal centers (PTGC) is a benign reactive lymphadenopathy, which can be an independent disease or occur in association with other lymphomas, the most common variant of which is nodular lymphocyte predominant Hodgkin lymphoma (NLPHL). To date, it has not been definitively clarified how PTGC and NLPHL are interconnected, despite the abundance of works presented on this topic. PTGC may precede NLPHL, occur synchronously with it, or develop after a course of therapy in patients with NLPHL. Despite similar clinical and morphological features, the approach to the treatment and management of patients is different. In the case of NLPHL, one of the therapeutic options is chemotherapy, which is not used in patients with PTGC. This article presents a clinical case of partial lymph node lesion of NLPHL associated with PTGC, on the example of which the main issues of differential diagnosis of PTGC and NLHLP will be considered. The patient's parents gave their consent to the use of their child's data, including photographs, for research purposes and in publications.

References

1. Hicks J., Flaitz C. Progressive transformation of germinal centers: Review of histopathologic and clinical features. Int J Pediatr Otorhinolaryngol 2002; 65 (3): 195–202. DOI: 10.1016/S0165-5876(02)00176-3

2. Özkan M.C., Özsan N., Hekimgil M., Saydam G., Töbü M. Progressive Transformation of Germinal Centers: Single-Center Experience of 33 Turkish Patients. Clin Lymphoma Myeloma Leuk 2016; 16: S149–51. DOI: 10.1016/j.clml.2016.03.010

3. Kojima M., Nakamura S., Motoori T., Itoh H., Shimizu K., Yamane N., et al. Progressive transformation of germinal centers: A clinicopathological study of 42 Japanese patients. Int J Surg Pathol 2003; 11 (2): 101–7. DOI: 10.1177/106689690301100205

4. Furqan Shaikh R.G., Ngan B.-Y., Alexander S. Progressive transformation of germinal centers in children and adolescents: an intriguing cause of lymphadenopathy. Pediatr Blood Cancer 2013; 60 (1): 26–30. DOI: 10.1002/pbc.24234

5. Hansmann M.L., Fellbaum C., Hui P.K., Moubayed P. Progressive transformation of germinal centers with and without association to Hodgkin’s disease. Am J Clin Pathol 1990; 93 (2): 219–26. DOI: 10.1093/ajcp/93.2.219

6. Hartmann S., Winkelmann R., Metcalf R.A., Treetipsatit J., Warnke R.A., Natkunam Y., et al. Immunoarchitectural patterns of progressive transformation of germinal centers with and without nodular lymphocyte-predominant Hodgkin lymphoma. Hum Pathol 2015; 46 (11): 1655–61. DOI: 10.1016/j.humpath.2015.07.006

7. Lim M.S., Straus S.E., Dale J.K., Fleisher T.A., Stetler-Stevenson M., Strober W., et al. Pathological findings in human autoimmune lymphoproliferative syndrome. Am J Pathol 1998; 153 (5): 1541–50. DOI: 10.1016/S0002-9440(10)65742-2

8. Sato Y., Inoue D., Asano N., Takata K., Asaoku H., Maeda Y., et al. Association between IgG4-related disease and progressively transformed germinal centers of lymph nodes. Mod Pathol 2012; 25 (7): 956–67. DOI: 10.1038/modpathol.2012.54

9. Nguyen N.L., Ferry J.A., Harris N.L. Progressive Transformation of Germinal Centers and Nodular Lymphocyte Predominance Hodgkin’s Disease. Am J Surg Pathol 1999; 23 (1): 27–33.

10. Good D.J., Gascoyne R.D. Atypical Lymphoid Hyperplasia Mimicking Lymphoma. Hematol Oncol Clin North Am 2009; 23 (4): 729–45. DOI: 10.1016/j.hoc.2009.04.005

11. Nam-Cha S.H., Roncador G., SanchezVerde L., Montes-Moreno S., Acevedo A., Domínguez-Franjo P., et al. PD-1, A follicular T-cell marker useful for recognizing nodular lymphocyte-predominant Hodgkin lymphoma. Am J Surg Pathol 2008; 32 (8): 1252–7. DOI: 10.1097/PAS.0b013e318165b0d6

12. Braeuninger A., Küppers R., Strickler J.G., Wacker H.H., Rajewsky K., Hansmann M.L. Hodgkin and Reed-Sternberg cells in lymphocyte predominant Hodgkin disease represent clonal populations of germinal center-derived tumor B cells. Proc Natl Acad Sci U S A 1997; 94 (17): 9337–42. DOI: 10.1073/pnas.94.17.9337

13. Mason D.Y., Banks P.M., Chan J., Cleary M.L., Delsol G., de Wolf Peeters C., et al. Nodular lymphocyte predominance Hodgkin’s disease. A distinct clinicopathological entity. Am J Surg Pathol 1994; 18 (5): 526–30. DOI: 10.1097/00000478-199405000-00014

14. Uherova P., Valdez R., Ross C.W., Schnitzer B., Finn W.G. Nodular lymphocyte predominant Hodgkin lymphoma: An immunophenotypic reappraisal based on a single-institution experience. Am J Clin Pathol 2003; 119 (2): 192–8. DOI: 10.1309/38RK238FCDCH5R22

15. Falini B., Bigerna B., Pasqualucci L., Fizzotti M., Martelli M.F., Pileri S., et al. Distinctive expression pattern of the BCL-6 protein in nodular lymphocyte predominance Hodgkin’s disease. Blood 1996; 87 (2): 465–71. DOI: 10.1182/blood.v87.2.465.bloodjournal872465

16. Anagnostopoulos I., Hansmann M.L., Franssila K., Harris M., Harris N.L., Jaffe E.S., et al. European Task Force on Lymphoma project on lymphocyte predominance Hodgkin disease: Histologic and immunohistologic analysis of submitted cases reveals 2 types of Hodgkin disease with a nodular growth pattern and abundant lymphocytes. Blood 2000; 96 (5): 1889–99. DOI: 10.1182/blood.V96.5.1889

17. Kiil K., Bein J., Schuhmacher B., Thurner L., Schneider M., Hansmann M.-L., et al. A high number of IgG4-positive plasma cells rules out nodular lymphocyte predominant Hodgkin lymphoma. Virchows Arch 2018; 473 (6): 759–64. DOI: 10.1007/s00428-018-2460-8

18. Aguilera D.G., Vaklavas C., Tsimberidou A.M., Wen S., Medeiros L.J., Corey S.J. Pediatric therapy-related myelodysplastic syndrome/acute myeloid leukemia: the MD Anderson Cancer Center experience. J Pediatr Hematol Oncol 2009; 31 (11): 803–11. DOI: 10.1097/MPH.0b013e-3181ba43dc

19. Josting A., Wiedenmann S., Franklin J., May M., Sieber M., Wolf J., et al. Secondary myeloid leukemia and myelodysplastic syndromes in patients treated for Hodgkin’s disease: A report from the German Hodgkin’s Lymphoma Study Group. J Clin Oncol 2003; 21 (18): 3440–6. DOI: 10.1200/JCO.2003.07.160

20. Nogová L., Reineke T., Brillant C., Sieniawski M., Rüdiger T., Josting A., et al. Lymphocyte-predominant and classical Hodgkin’s lymphoma: A comprehensive analysis from the german Hodgkin study group. J Clin Oncol 2008; 26 (3): 434–9. DOI: 10.1200/JCO.2007.11.8869

21. Mauz-Körholz C., Gorde-Grosjean S., Hasenclever D., Shankar A., Dörffel W., Hamish Wallace W., et al. Resection alone in 58 children with limited stage, lymphocyte-predominant Hodgkin lymphoma-experience from the European network group on pediatric Hodgkin lymphoma. Cancer 2007; 110 (1): 179–85. DOI: 10.1002/cncr.22762

22. Mauz-Körholz C., Lange T., Hasenclever D., Burkhardt B., Feller A.C., Dörffel W., et al. Pediatric Nodular Lymphocyte-predominant Hodgkin Lymphoma: Treatment Recommendations of the GPOH-HD Study Group. Klin Padiatr 2015; 227 (6–7): 314–21. DOI: 10.1055/s-0035-1559664

23. Couronné L., Schneider P., Picquenot J.M., Laberge S., Bastard C., Vannier J.P. Refractory nodular lymphocyte predominant hodgkin lymphoma transformed to T-cell/histiocyte-rich B-cell lymphoma in an adolescent: Salvage therapy with allogeneic bone marrow transplantation. J Pediatr Hematol Oncol 2008; 30 (12): 959–62. DOI: 10.1097/MPH.0b013e31818a9564

24. Biasoli I., Stamatoullas A., Meignin V., Delmer A., Reman O., Morschhauser F., et al. Nodular, lymphocyte-predominant Hodgkin lymphoma: A long-term study and analysis of transformation to diffuse large B-cell lymphoma in a cohort of 164 patients from the adult lymphoma study group. Cancer 2010; 116 (3): 631–9. DOI: 10.1002/cncr.24819

25. Hall G.W., Katzilakis N., Pinkerton C.R., Nicolin G., Ashley S., McCarthy K., et al. Outcome of children with nodular lymphocyte predominant Hodgkin lymphoma – A Children’s Cancer and Leukaemia Group report. Br J Haematol 2007; 138 (6): 761–8. DOI: 10.1111/j.1365-2141.2007.06736.x

26. Shankar A., Hall G.W., Gorde-Grosjean S., Hasenclever D., Leblanc T., Hayward J., et al. Treatment outcome after low intensity chemotherapy [CVP] in children and adolescents with early stage nodular lymphocyte predominant Hodgkin’s lymphoma - An Anglo-French collaborative report. Eur J Cancer 2012; 48 (11): 1700–6. DOI: 10.1016/j.ejca.2011.10.018