Rare Disease — Nodular Lymphocyte-Predominant Hodgkin’s Lymphoma: Literature Review and Own Data

E.A. Demina, G.S. Tumyan, A.A. Chekan, M.Yu. Kichigina, A.S. Antipova, N.A. Probatova, A.I. Pavlovskaya, N.V. Kokosadze, A.M. Kovrigina, O.P. Trofimova, E.A. Osmanov,

DOI:

https://doi.org/10.21320/2500-2139-2014-7-4-522-532

Nodular lymphocyte-predominant Hodgkin’s lymphoma (NLPHL) is a rare disorder; it constitutes only 5 % of all cases of Hodgkin’s lymphoma (the morbidity rate is 1.5 per one million). The disease differs from classical Hodgkin’s lymphoma (cHL) in both immunohistochemical (marked CD20 expression in LP cells) and clinical features (prevalence of the early stage disease, indolent course with delayed relapses and trends toward transformation into diffuse large B cell lymphoma). Since the number of patients in prospective NLPHL-focused trials is limited, treatment algorithms have been based on retrospective data; these are usually obtained from cHL and indolent B cell lymphoma treatment strategies. Patients rarely die from NLPHL; in fact, secondary malignancies and other treatment related toxicities generally contribute to overall mortality. Over the past decade, there has been a series of NLPHL-related publications describing prescription of rituximab for newly diagnosed diseases and for relapses, including patients at high risk of diseases transformation. Besides, the role of the “wait and watch”, radiation treatment, and chemotherapy has been discussed. Our own experience in the use of rituximab in NLPLH patients demonstrated its efficacy at different stages and at different phases of the disease.

  • E.A. Demina N.N. Blokhin Russian Cancer Research Center, 24 Kashirskoye sh., Moscow, Russian Federation, 115478 ; ФГБУ «Российский онкологический научный центр им. Н.Н. Блохина», Каширское ш., д. 24, Москва, Российская Федерация, 115478
  • G.S. Tumyan N.N. Blokhin Russian Cancer Research Center, 24 Kashirskoye sh., Moscow, Russian Federation, 115478 ; ФГБУ «Российский онкологический научный центр им. Н.Н. Блохина», Каширское ш., д. 24, Москва, Российская Федерация, 115478
  • A.A. Chekan N.N. Blokhin Russian Cancer Research Center, 24 Kashirskoye sh., Moscow, Russian Federation, 115478 ; ФГБУ «Российский онкологический научный центр им. Н.Н. Блохина», Каширское ш., д. 24, Москва, Российская Федерация, 115478
  • M.Yu. Kichigina N.N. Blokhin Russian Cancer Research Center, 24 Kashirskoye sh., Moscow, Russian Federation, 115478 ; ФГБУ «Российский онкологический научный центр им. Н.Н. Блохина», Каширское ш., д. 24, Москва, Российская Федерация, 115478
  • A.S. Antipova N.N. Blokhin Russian Cancer Research Center, 24 Kashirskoye sh., Moscow, Russian Federation, 115478 ; ФГБУ «Российский онкологический научный центр им. Н.Н. Блохина», Каширское ш., д. 24, Москва, Российская Федерация, 115478
  • N.A. Probatova N.N. Blokhin Russian Cancer Research Center, 24 Kashirskoye sh., Moscow, Russian Federation, 115478 ; ФГБУ «Российский онкологический научный центр им. Н.Н. Блохина», Каширское ш., д. 24, Москва, Российская Федерация, 115478
  • A.I. Pavlovskaya N.N. Blokhin Russian Cancer Research Center, 24 Kashirskoye sh., Moscow, Russian Federation, 115478 ; ФГБУ «Российский онкологический научный центр им. Н.Н. Блохина», Каширское ш., д. 24, Москва, Российская Федерация, 115478
  • N.V. Kokosadze N.N. Blokhin Russian Cancer Research Center, 24 Kashirskoye sh., Moscow, Russian Federation, 115478 ; ФГБУ «Российский онкологический научный центр им. Н.Н. Блохина», Каширское ш., д. 24, Москва, Российская Федерация, 115478
  • A.M. Kovrigina Hematology Research Center under the Ministry of Health of the Russian Federation, 4а Novyi Zykovskii pr-d, Moscow, Russian Federation, 125167 ; ФГБУ «Гематологический научный центр» МЗ РФ, Новый Зыковский пр-д, д. 4а, Москва, Российская Федерация, 125167
  • O.P. Trofimova N.N. Blokhin Russian Cancer Research Center, 24 Kashirskoye sh., Moscow, Russian Federation, 115478 ; ФГБУ «Российский онкологический научный центр им. Н.Н. Блохина», Каширское ш., д. 24, Москва, Российская Федерация, 115478
  • E.A. Osmanov N.N. Blokhin Russian Cancer Research Center, 24 Kashirskoye sh., Moscow, Russian Federation, 115478 ; ФГБУ «Российский онкологический научный центр им. Н.Н. Блохина», Каширское ш., д. 24, Москва, Российская Федерация, 115478
  1. Jackson H., Parker F. Hodgkin’s disease II. Pathology. N. Engl. J. Med. 1944; 231: 35–44. DOI: https://doi.org/10.1056/NEJM194407132310201
  2. Lukes R., Butler J., Hicks E. Natural history of Hodgkin’s disease as related to its pathological picture. Cancer. 1966; 19: 317–44. DOI: https://doi.org/10.1002/1097-0142(196603)19:3<317::AID-CNCR2820190304>3.0.CO;2-O
  3. Harris N.L., Jaffe E.S., Stein H. A revised European-American classification of lymphoid neoplasms: a proposal from the International Lymphoma Study Group. Blood. 1994; 84: 1361–92. DOI: https://doi.org/10.1182/blood.V84.5.1361.bloodjournal8451361
  4. Jaffe E.S., Harris N.L., Stein H. et al. Pathology and genetics of tumors of hematopoietic and lymphoid tissues. Lyon: IARC Press, 2001: 240–3.
  5. Swerdlow S.H., Campo E., Harris N.L. et al. (eds.) WHO classification of tumors of hematopoietic and lymphoid tissues. Lyon: IARC Press, 2008.
  6. Diehl V., Sextro M., Franclin J. et al. Clinical presentation, course, and prognostic factors in lymphocyte predominant Hodgkin’s disease: report from European Task Force on Lymphoma (ETFL) Project on lymphocyte-predominant Hodgkin’s disease. J. Clin. Oncol. 1999; 17: 776–83. DOI: https://doi.org/10.1200/JCO.1999.17.3.776
  7. Saarinen S., Pukkala E., Vahteristo P. et al. High Familial Risk in Nodular Lymphocyte-Predominant Hodgkin Lymphoma. JCO. 2013; 31(7): 938–43. DOI: https://doi.org/10.1200/JCO.2012.43.5958
  8. Mason D.Y., Banks P.M., Chan J. et al. Nodular lymphocyte-predominant Hodgkin’s disease. A distinct clinicopathological entity. Am. J. Surg. Pathol. 1994; 18: 526–30. DOI: https://doi.org/10.1097/00000478-199405000-00014
  9. Engert A., Horning S.J. (eds.) Hodgkin Lymphoma: A Comprehensive Update on Diagnostics and Clinics (Hematologic Malignancies). Springer, 2011. DOI: https://doi.org/10.1007/978-3-642-12780-9
  10. Ковригина А.М., Пробатова Н.А. Лимфома Ходжкина и крупнокле- точные лимфомы. Медицинское информационное агентство, 2007. [Kovrigina A.M., Probatova N.A. Limfoma Khodzhkina i krupnokletochnye limfomy. (Hodgkin’s lymphoma and larg cell lymphomas.) Meditsinskoe informatsionnoe agentstvo Publ.; 2007.]
  11. Nogova L., Reineke T., Brillant C. et al. Lymphocyte-predominant and classical Hodgkin’s lymphoma: a comprehensive analysis from the German Hodgkin Study Group. J. Clin. Oncol. 2008; 26: 434–9. DOI: https://doi.org/10.1200/JCO.2007.11.8869
  12. Лимфома Ходжкина. Российские клинические рекомендации по диагностике и лечению лимфопролиферативных заболеваний. Под ред. И.В. Поддубной, В.Г. Савченко. Современная онкология. Экстравыпуск. 2013: 11–5. [Poddubnaya I.V., Savchenko V.G., eds. Limfoma Khodzhkina. Rossiiskie klinicheskie rekomendatsii po diagnostike i lecheniyu limfoproliferativnykh zabolevanii. (Hodgkin’s lymphoma. Russian clinical guidelines in diagnosis and treatment of lymphoproliferative disorders.) Sovremennaya onkologiya. Additional release; 2013. pр. 11–5.]
  13. Fanale M. Lymphocyte-predominant Hodgkin lymphoma: what is the optimal treatment? Hematology (EHA 2013 Education book). 2013: 406–16. DOI: https://doi.org/10.1182/asheducation-2013.1.406
  14. Kuppers R., Rajewsky K., Zhao M. et al. Hodgkin disease: Hodgkin and Reed–Sternberg cells picked from histological sections show clonal immunoglobulin gene rearrangements and appear to be derived from B-cells at various stages of development. Proc. Natl. Acad. Sci. USA. 1994; 91: 10962–6. DOI: https://doi.org/10.1073/pnas.91.23.10962
  15. Marafioti T., Hummel M., Anagnostopoulos I. et al. Origin of nodular lymphocyte-predominant Hodgkin’s disease from a clonal expansion of highly mutated germinal center B-cells. N. Engl. J. Med. 1997; 337(7): 453–8. DOI: https://doi.org/10.1056/NEJM199708143370703
  16. Isaacson P.G. Malignant lymphomas with a follicular growth pattern. Histopathology. 1996; 28(6): 487–95. DOI: https://doi.org/10.1046/j.1365-2559.1996.d01-473.x
  17. Brune V., Tiacci E., Pfeil I. et al. Origin and pathogenesis of nodular lymphocyte-predominant Hodgkin lymphoma as revealed by global gene expression analysis. J. Exp. Med. 2008; 205(10): 2251–68. DOI: https://doi.org/10.1084/jem.20080809
  18. Mottok A., Renne C., Willenbrock K. et al. Somatic hypermutation of SOCS1 in lymphocyte-predominant Hodgkin lymphoma is accompanied by high JAC2 expression and activation of STAT6. Blood. 2007; 110(9): 3387–90. DOI: https://doi.org/10.1182/blood-2007-03-082511
  19. Schumacher A.M., Schmitz R., Brune V. et al. Mutations in the genes coding for den NJ-kB regulation factors IkBa and A20 are uncommon in nodular lymphocyte-predominant Hodgkin lymphoma. Haematologica. 2010; 95: 153–7. DOI: https://doi.org/10.3324/haematol.2009.010157
  20. Liso A., Capello D., Marafiotti T. et al. Aberrant somatic hypermutation in tumor cells of nodular-lymphocyte-predominant and classic Hodgkin lymphoma. Blood. 2006; 108(3): 1013–20. DOI: https://doi.org/10.1182/blood-2005-10-3949
  21. Rahemtullah A., Reichard K.K., Preffer F.I. et al. A double-positive CD4+CD8+ T-cells population is commonly found in nodular lymphocyte predominant Hodgkin lymphoma. Am. J. Clin. Pathol. 2006; 125(5): 153–7. DOI: https://doi.org/10.1309/Y8KD32QGRYFN1XQX
  22. Henry-Amar M. Second cancer after treatment for Hodgkin’s disease: a report from the International Database on Hodgkin’s disease. Ann. Oncol. 1992; 3(Suppl. 4): 117. DOI: https://doi.org/10.1093/annonc/3.suppl_4.S117
  23. Saad J., Sirop S.J., Habermann T.M. et al. Diffuse Large B-Cell Transformation in Nodular Lymphocyte Predominant Hodgkin Lymphoma: Incidence, Risk Factors and Outcomes After a Forty-Year Experience From a Single Institution. Blood (ASH Annual Meeting Abstracts). 2012; 120: 1525. DOI: https://doi.org/10.1182/blood.V120.21.1525.1525
  24. Al-Mansour M., Connors J.M., Gascoyne R.D. et al. Transformation to Aggressive Lymphoma in Nodular Lymphocyte-Predominant Hodgkin’s Lymphoma. J. Clin. Oncol. 2010; 28: 793–9. DOI: https://doi.org/10.1200/JCO.2009.24.9516
  25. Bennett M.H., MacLennan K.A., Vaughan Hudson G. et al. Non-Hodgkin’s lymphoma arising in patients treated for Hodgkin’s disease in the BNLI: A 20- year experience—British National Lymphoma Investigation. Ann. Oncol. 1991; 2(Suppl. 2): 83–92. DOI: https://doi.org/10.1093/annonc/2.suppl_2.83
  26. Orlandi E., Lazzarino M., Brusamolino E. et al. Nodular lymphocyte predominance Hodgkin’s disease: Long-term observation reveals a continuous pattern of recurrence. Leuk. Lymphoma. 1997; 26: 359–68. DOI: https://doi.org/10.3109/10428199709051786
  27. Wickert R.S., Weisenburger D.D., Tierens A. et al. Clonal relationship between lymphocytic predominance Hodgkin’s disease and concurrent or subsequent large-cell lymphoma of B lineage. Blood. 1995; 86: 2312–20. DOI: https://doi.org/10.1182/blood.V86.6.2312.bloodjournal8662312
  28. Hell K., Hansmann M.L., Pringle J.H. et al. Combination of Hodgkin’s disease and diffuse large cell lymphoma: An in situ hybridization study for immunoglobulin light chain messenger RNA. Histopathology. 1995; 27: 491–9. DOI: https://doi.org/10.1111/j.1365-2559.1995.tb00319.x
  29. Greiner T.C., Gascoyne R.D., Anderson M.E. et al. Nodular lymphocytepredominant Hodgkin’s disease associated with large-cell lymphoma: Analysis of Ig gene rearrangements by V-J polymerase chain reaction. Blood. 1996; 88: 657–66. DOI: https://doi.org/10.1182/blood.V88.2.657.bloodjournal882657
  30. Sirop S.J., Habermann T.M., Macon W.R. et al. Diffuse Large B-Cell Transformation in Nodular Lymphocyte Predominant Hodgkin Lymphoma: Incidence, Risk Factors and Outcomes After a Forty-Year Experience From a Single Institution. Blood (ASH Annual Meeting Abstracts). 2012; 120(21): Abstract 1525. DOI: https://doi.org/10.1182/blood.V120.21.1525.1525
  31. Farrell K., Mckay P., Leach M. Nodular Lymphocyte Predominant Hodgkin Lymphoma behaves as a Distinct Clinical Entity with Good Outcome: Evidence from 14 year Follow-up from the West of Scotland Cancer Network. Ann. Oncol. 2011; 22(Suppl. 4): Abstract 291. DOI: https://doi.org/10.3109/10428194.2011.584993
  32. Pappa V.I., Norton A.J., Gupta R.K. et al. Nodular type of lymphocyte predominant Hodgkin’s disease. A clinical study of 50 cases. Ann. Oncol. 1995; 6(6): 559–65. DOI: https://doi.org/10.1093/oxfordjournals.annonc.a059244
  33. Connors J.M. Lymphocyte predominant Hodgkin’s lymphoma. ASH (Education Program Book). 2001: 1: 187–90.
  34. Borg-Grech A., Radford J.A., Crowther D., Swindell R., Harris M. A comparative study of the nodular and diffuse variants of lymphocytepredominant Hodgkin’s disease. J. Clin. Oncol. 1989; 7(9): 1303–9. DOI: https://doi.org/10.1200/JCO.1989.7.9.1303
  35. Regula D.P. Jr., Hoppe R.T., Weiss L.M. Nodular and diffuse types of lymphocyte predominance Hodgkin’s disease. N. Engl. J. Med. 1988; 318(4): 214–9. DOI: https://doi.org/10.1056/NEJM198801283180404
  36. Crennan E., D’Costa I., Liew K.H. et al. Lymphocyte predominant Hodgkin’s disease: a clinicopathologic comparative study of histologic and immunophenotypic subtypes. Int. J. Radiat. Oncol. Biol. Phys. 1995; 31(2): 333–7. DOI: https://doi.org/10.1016/0360-3016(94)E0136-8
  37. Hansmann M.L., Zwingers T., Boske A., Loffler H., Lennert K. Clinical features of nodular paragranuloma (Hodgkin’s disease, lymphocyte predominance type, nodular). J. Cancer Res. Clin. Oncol. 1984; 108(3): 321–30. DOI: https://doi.org/10.1007/BF00390466
  38. Bodis S., Kraus M.D., Pinkus G. et al. Clinical presentation and outcome in lymphocyte-predominant Hodgkin’s disease. J. Clin. Oncol. 1997; 15(9): 3060–6. DOI: https://doi.org/10.1200/JCO.1997.15.9.3060
  39. Pellegrino B., Terrier-Lacombe M.J., Oberlin O. et al. Lymphocytepredominant Hodgkin’s lymphoma in children: therapeutic abstention after initial lymph node resection — a study of the French Society of Pediatric Oncology. J. Clin. Oncol. 2003; 21: 2948–52. DOI: https://doi.org/10.1200/JCO.2003.01.079
  40. Murphy S.B., Morgan E.R., Katzenstein H.M. et al. Results of little for not treatment for lymphocyte-predominant Hodgkin disease in children and adolescents. J. Pediatr. Hematol. Oncol. 2003; 25: 684–7. DOI: https://doi.org/10.1097/00043426-200309000-00003
  41. Mauz-Koerholz С., Hasenclever D., Gorde-Grosjean S. et al. Surgical resection alone in children with limited stage lymphocyte predominant Hodgkin’s lymphoma — the experience of the EuroNet-PHL group [abstract]. Blood (ASH Annual Meeting Abstracts). 2006; 108(11): 2470. DOI: https://doi.org/10.1182/blood.V108.11.2470.2470
  42. Appel B., Ehrich P., Chen L. et al. Treatment of pediatric stage IA lymphocyte-predominant Hodgkin’s lymphoma with surgical resection alone: A report from the Children’s Oncology Group. J. Clin. Oncol. 2012; 30: 9524. DOI: https://doi.org/10.1200/jco.2012.30.15_suppl.9524
  43. Biasoli I., Stamatoullas A., Meignin V. et al. Nodular, LymphocytePredominant Hodgkin’s Lymphoma. Cancer. 2010; 116: 631–9. DOI: https://doi.org/10.1002/cncr.24819
  44. Schlembach P., Wilder R., Jones D. et al. Radiotherapy alone for lymphocyte-predominant Hodgkin’s disease. Cancer J. 2002; 8(5): 377–83. DOI: https://doi.org/10.1097/00130404-200209000-00008
  45. Wirth A., Yuen K., Barton M. et al. Long-term outcome after radiotherapy alone for lymphocyte-predominant Hodgkin lymphoma: a retrospective multicenter study of the Australian Radiation Oncology Lymphoma Group. Cancer. 2005; 104(6): 1221–9. DOI: https://doi.org/10.1002/cncr.21303
  46. Chen R.C., Chin M.S., Ng A.K. et al. Early stage, lymphocyte-predominant Hodgkin’s lymphoma: patient outcomes from a large, single-institution series with long follow-up. J. Clin. Oncol. 2010; 28(1): 136–41. DOI: https://doi.org/10.1200/JCO.2009.24.0945
  47. Nogova L., Reineke T., Eich H.T. et al. Extended field radiotherapy, combined modality treatment or involved field radiotherapy for patient with stage IA lymphocyte-predominant Hodgkin’s lymphoma: a retrospective analysis from the German Hodgkin Study Group (GHSG). Ann. Oncol. 2005; 16(10): 1683–7. DOI: https://doi.org/10.1093/annonc/mdi323
  48. Eichenauer D.A., Fuchs M., Pluetschow A. et al. Phase 2 study of rituximab in newly diagnosed stage IA nodular lymphocyte-predominant Hodgkin lymphoma: a report from the German Hodgkin Study Group. Blood. 2011; 118(16): 4363–5. DOI: https://doi.org/10.1182/blood-2011-06-361055
  49. Canellos G.P., Mauch P. What Is the Appropriate Systemic Chemotherapy for Lymphocyte-Predominant Hodgkin’s Lymphoma? J. Clin. Oncol. 2010; 28(1): е8. DOI: https://doi.org/10.1200/JCO.2009.26.3293
  50. Fanale M.A., Lai C.M., McLaughlin P. et al. Outcomes of Nodular Lymphocyte Predominant Hodgkin’s Lymphoma (NLPHL) Patients Treated with R-CHOP. Blood (ASH Annual Meeting Abstracts). 2010; 116(21): Abstract 2812. DOI: https://doi.org/10.1182/blood.V116.21.2812.2812
  51. Advani R.H., Hope R.T. How I treat lymphocyte predominant Hodgkin Lymphoma. Blood. 2013; 122(26): 4182–8. DOI: https://doi.org/10.1182/blood-2013-07-453241
  52. Karuturi M., Hosing C., Fanale M. et al. High-dose chemotherapy and autologous stem cell transplantation for nodular lymphocyte-predominant Hodgkin lymphoma. Biol. Blood Marrow Transplant. 2013; 19(6): 991–4. DOI: https://doi.org/10.1016/j.bbmt.2013.03.008
  53. Bierman P., Naushad H., Loberiza F. et al. High-dose chemotherapy followed by autologous hematopoietic stem cell transplantation (AHSCT) for lymphocyte predominant Hodgkin’s disease [abstract]. Blood. 2006; 108(11): Abstract 3061. DOI: https://doi.org/10.1182/blood.V108.11.3061.3061
  54. Jackson C., Sirohi B., Cunningham D. et al. Lymphocyte-predominant Hodgkin lymphoma — clinical features and treatment outcomes from a 30-year experience. Ann. Oncol. 2010; 21(10): 2061–8. DOI: https://doi.org/10.1093/annonc/mdq063
  55. Eichenauer D.A., Fuchs M., Pluetschow A. et al. Phase 2 study of rituximab in newly diagnosed stage IA nodular lymphocyte-predominant Hodgkin lymphoma: a report from the German Hodgkin Study Group. Blood. 2011; 118(16): 4363–5. DOI: https://doi.org/10.1182/blood-2011-06-361055
  56. Park H.C., Jung S.H., Ahn J.S. et al. Rituximab plus ifosfamide, carboplatin and etoposide for T-cell/histiocyte-rich B-cell lymphoma arising in nodular lymphocyte-predominant Hodgkin’s lymphoma. Case Rep. Oncol. 2012; 5(2): 413–9. DOI: https://doi.org/10.1159/000341562
  57. Ekstrand B.C., Lucas J.B., Horwitz S.M. et al. Rituximab in lymphocytepredominant Hodgkin disease: results of a phase 2 trial. Blood. 2003; 101(11): 4285–9. DOI: https://doi.org/10.1182/blood-2002-08-2644
  58. Schulz H., Rehwald U., Morschhauser F. et al. Rituximab in relapsed lymphocyte-predominant Hodgkin lymphoma: long-term results of a phase 2 trial by the German Hodgkin Lymphoma Study Group (GHSG). Blood. 2008; 111(1): 109–11. DOI: https://doi.org/10.1182/blood-2007-03-078725
  59. Advani R.H., Buggy J.J., Sharman J.P. et al. Bruton tyrosine kinase inhibitor ibrutinib (PCI-32765) has significant activity in patients with relapsed/ refractory B-cell malignancies. J. Clin. Oncol. 2013; 31(1): 88–94. DOI: https://doi.org/10.1200/JCO.2012.42.7906
  60. Advani R.H., Horning S.J., Hope RT. et al. Mature results of a Phase II Study of Rituximab Therapy for Nodular Lymphocyte-Predominant Hodgkin Lymphoma. J. Clin. Oncol. 2014; 32(9): 912–8. DOI: https://doi.org/10.1200/JCO.2013.53.2069

Keywords:

nodular lymphocyte-predominant Hodgkin’s lymphoma, diagnosis, clinical characteristics, treatment, rituximab

License

Copyright (c) 2014 Clinical Oncohematology

Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.

Downloads

Download data is not yet available.

For Contact

  • E.A. Demina, DSci, Professor, N.N. Blokhin Russian Cancer Research Center, 24 Kashirskoye sh., Moscow, Russian Federation, 115478, ФГБУ «Российский онкологический научный центр им. Н.Н. Блохина», Каширское ш., д. 24, Москва, Российская Федерация, 115478, e-mail: drdemina@yandex.ru
2014-4

Downloads

Published

01.10.2014

Issue

Vol. 7 No. 4 (2014)
LYMPHOID MALIGNANCIES

How to Cite

Demina E.A., Tumyan G.S., Chekan A.A., et al. Rare Disease — Nodular Lymphocyte-Predominant Hodgkin’s Lymphoma: Literature Review and Own Data. Clinical Oncohematology. Basic Research and Clinical Practice. 2014;7(4):522–532. doi:10.21320/2500-2139-2014-7-4-522-532.

Most read articles by the same author(s)

1 2 3 4 5 6 7 8 9 > >>