Impact of Expert Pathologic Review of Lymphoma Diagnosis: Study of Patients From the French Lymphopath Network.

Purpose To prospectively assess the clinical impact of expert review of lymphoma diagnosis in France. Materials and Methods From January 2010 to December 2013, 42,145 samples from patients with newly diagnosed or suspected lymphomas were reviewed, according to the 2008 WHO classification, in real time by experts through the Lymphopath Network. Changes in diagnosis between referral and expert review were classified as major or minor according to their potential impact on patient care. Results The 42,145 reviewed samples comprised 36,920 newly diagnosed mature lymphomas, 321 precursor lymphoid neoplasms, 314 myeloid disorders, and 200 nonhematopoietic neoplasms, with 4,390 benign lesions. There were 4,352 cutaneous and 32,568 noncutaneous lymphomas. The most common mature noncutaneous lymphomas were diffuse large B-cell lymphomas (32.4%), follicular lymphomas (15.3%), classic Hodgkin lymphomas (13%), peripheral T-cell lymphomas (6.3%) of which angioimmunoblastic T-cell lymphomas (2.3%) were the most frequent, and mucosa-associated lymphoid tissue lymphomas (5.8%). A diagnostic change between referral and expert review occurred in 19.7% of patients, with an estimated impact on patient care for 17.4% of patients. This rate was significantly higher for patients sent with a provisional diagnosis seeking expert second opinion (37.8%) than for patients sent with a formal diagnosis (3.7%). The most frequent discrepancies were misclassifications in lymphoma subtype (41.3%), with 12.3% being misclassifications among small B-cell lymphoma entities. Fewer than 2% of changes were between benign and malignant lymphoid conditions. Minor changes (2.3%) mostly consisted of follicular lymphoma misgrading and diffuse large B-cell lymphoma subtype misclassification. Conclusion To our knowledge, this study provides the largest ever description of the distribution of lymphoma entities in a western country and highlights how expert review significantly contributes to a precise lymphoma diagnosis and optimal clinical management in a proportion of patients.

Thomas Filleron | Jean-François Michiels | Peggy Dartigues | Bettina Fabiani | Camille Laurent | Pierre Brousset | Diane Damotte | Thierry Jo Molina | Jean-Michel Picquenot | Françoise Berger | C. Copie-Bergman | T. Molina | P. Gaulard | G. Salles | F. Berger | P. Brousset | L. Xerri | J. Picquenot | M. Copin | T. Petrella | I. Soubeyran | N. Brousse | G. Delsol | C. Haioun | A. Moreau | D. Damotte | C. Chassagne‐Clément | Antoine Martin | H. Sevestre | T. Filleron | M. Rousselet | J. Michiels | F. Charlotte | Pierre Dechelotte | Marie-Christine Copin | Gilles Salles | J. Brière | Isabelle Quintin-Roué | Henri Sevestre | C. Bossard | Philippe Gaulard | P. Dechelotte | Corinne Haioun | B. Fabiani | Georges Delsol | Christiane Copie-Bergman | Laurent Martin | Patrick Tas | B. Fabre | P. Dartigues | F. Arbion | Nicole Brousse | Flavie Arbion | Marc Maynadié | C. Laurent | Tony Petrella | M. Parrens | P. Tas | Marine Baron | Nadia Amara | Mylène Dandoit | Marie Parrens | Beatrice Vergier | Alexandra Traverse-Glehen | Marie-Christine Rousselet | Josette Brière | Fréderic Charlotte | Catherine Chassagne-Clement | Thérèse Rousset | Luc Xerri | Anne Moreau | Antoine Martin | Isabelle Soubeyran | Michel Peoch | Antoine de Mascarel | Céline Bossard | Martine Patey | Blandine Fabre | Cécile Le Naoures | Marie-Pierre Chenard-Neu | Claire Bastien | Sylvie Thiebault | Manuela Delage | I. Quintin-Roué | Laurent Martin | S. Thiébault | N. Amara | M. Patey | B. Vergier | A. de Mascarel | M. Chenard-Neu | A. Traverse-Glehen | T. Rousset | M. Péoch | Cécile le Naoures | C. Bastien | M. Delage | M. Maynadie | Mylène Dandoit | M. Baron | Patrick Tas

[1]  R. Advani,et al.  The World Health Organization Classification of Lymphoid Neoplasms , 2013 .

[2]  G. Salles,et al.  Survival impact of rituximab combined with ACVBP and upfront consolidation autotransplantation in high-risk diffuse large B-cell lymphoma for GELA , 2011, Haematologica.

[3]  T. Molina,et al.  Angioimmunoblastic T-cell lymphoma is the most common T-cell lymphoma in two distinct French information data sets , 2015, Haematologica.

[4]  P. Gaulard,et al.  Efficacy of L-asparaginase with methotrexate and dexamethasone (AspaMetDex regimen) in patients with refractory or relapsing extranodal NK/T-cell lymphoma, a phase 2 study. , 2011, Blood.

[5]  A. Advani,et al.  Current status of antibody therapy in ALL , 2015, British journal of haematology.

[6]  Michael L. Wang,et al.  Targeting BTK with ibrutinib in relapsed or refractory mantle-cell lymphoma. , 2013, The New England journal of medicine.

[7]  B. Coiffier,et al.  Therapeutic options in relapsed or refractory peripheral T-cell lymphoma. , 2014, Cancer treatment reviews.

[8]  S. Banerjee,et al.  Audit of tumour histopathology reviewed by a regional oncology centre. , 1995, Journal of clinical pathology.

[9]  J. Lester,et al.  The clinical impact of expert pathological review on lymphoma management: a regional experience , 2003, British journal of haematology.

[10]  R. Champlin,et al.  Targeting Bruton's tyrosine kinase with ibrutinib in B‐cell malignancies , 2015, Clinical pharmacology and therapeutics.

[11]  Andrew Lister,et al.  Rituximab maintenance for 2 years in patients with high tumour burden follicular lymphoma responding to rituximab plus chemotherapy (PRIMA): a phase 3, randomised controlled trial , 2011, The Lancet.

[12]  Alexandra G. Smith,et al.  Lymphoma incidence, survival and prevalence 2004–2014: sub-type analyses from the UK's Haematological Malignancy Research Network , 2015, British Journal of Cancer.

[13]  S. Swerdlow WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues , 2017 .

[14]  Shuangge Ma,et al.  Racial differences in three major NHL subtypes: descriptive epidemiology. , 2015, Cancer epidemiology.

[15]  B. Nathwani,et al.  A clinical evaluation of the International Lymphoma Study Group Classification of non-Hodgkin's lymphoma: a report of the Non-Hodgkin's Lymphoma Classification Project , 1997 .

[16]  N. Bartlett,et al.  Brentuximab Vedotin and Crizotinib in Anaplastic Large-Cell Lymphoma , 2012, Cancer journal.

[17]  E. Hawkes,et al.  Programmed cell death-1 inhibition in lymphoma. , 2015, The Lancet. Oncology.

[18]  C. Messa,et al.  Crizotinib in anaplastic large-cell lymphoma. , 2011, The New England journal of medicine.

[19]  Y. Hao,et al.  Treatment patterns and duration in post-menopausal women with HR+/HER2− metastatic breast cancer in the US: a retrospective chart review in community oncology practices (2004–2010) , 2015, Current medical research and opinion.

[20]  P. Gaulard,et al.  Peripheral T-cell lymphomas: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. , 2015, Annals of oncology : official journal of the European Society for Medical Oncology.

[21]  M. Davids,et al.  Ibrutinib: a first in class covalent inhibitor of Bruton's tyrosine kinase. , 2014, Future oncology.

[22]  A. LaCasce,et al.  Comparison of referring and final pathology for patients with non-Hodgkin's lymphoma in the National Comprehensive Cancer Network. , 2008, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[23]  O Lin,et al.  Expert second-opinion pathology review of lymphoma in the era of the World Health Organization classification. , 2012, Annals of oncology : official journal of the European Society for Medical Oncology.

[24]  W. Klapper,et al.  Addition of high-dose cytarabine to immunochemotherapy before autologous stem-cell transplantation in patients aged 65 years or younger with mantle cell lymphoma (MCL Younger): a randomised, open-label, phase 3 trial of the European Mantle Cell Lymphoma Network , 2016, The Lancet.

[25]  B. Coiffier,et al.  Rituximab versus observation after high-dose consolidative first-line chemotherapy with autologous stem-cell transplantation in patients with poor-risk diffuse large B-cell lymphoma. , 2009, Annals of oncology : official journal of the European Society for Medical Oncology.

[26]  B. Wilkins,et al.  Pitfalls in lymphoma pathology: avoiding errors in diagnosis of lymphoid tissues , 2011, Journal of Clinical Pathology.

[27]  C. Copie-Bergman,et al.  MYC-IG rearrangements are negative predictors of survival in DLBCL patients treated with immunochemotherapy: a GELA/LYSA study. , 2015, Blood.

[28]  A. Feldman,et al.  Adult systemic anaplastic large-cell lymphoma: recommendations for diagnosis and management , 2016, Expert review of hematology.

[29]  F. Passamonti,et al.  Investigational therapies targeting lymphocyte antigens for the treatment of non-Hodgkin’s lymphoma , 2015, Expert opinion on investigational drugs.

[30]  M. Jerkeman,et al.  Real-world data on prognostic factors and treatment in peripheral T-cell lymphomas: a study from the Swedish Lymphoma Registry. , 2014, Blood.

[31]  P. Hassa,et al.  Novel drug targets for personalized precision medicine in relapsed/refractory diffuse large B-cell lymphoma: a comprehensive review , 2015, Molecular Cancer.

[32]  G. Robert,et al.  Successful re-treatment of a relapsed V600E mutated HCL patient with low-dose vemurafenib , 2014, Oncoscience.

[33]  Alan Ramsay,et al.  Importance of expert central review in the diagnosis of lymphoid malignancies in a regional cancer network. , 2011, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[34]  D. Poller,et al.  Referrals for second opinion in surgical pathology: implications for management of cancer patients in the UK. , 2001, European journal of surgical oncology : the journal of the European Society of Surgical Oncology and the British Association of Surgical Oncology.

[35]  D. Weisenburger,et al.  Epidemiology of the non-Hodgkin's lymphomas: distributions of the major subtypes differ by geographic locations. Non-Hodgkin's Lymphoma Classification Project. , 1998, Annals of oncology : official journal of the European Society for Medical Oncology.

[36]  Lixin Wei,et al.  Distribution of lymphoid neoplasms in China: analysis of 4,638 cases according to the World Health Organization classification. , 2012, American journal of clinical pathology.

[37]  Juthamas Sukbuntherng,et al.  Targeting BTK with ibrutinib in relapsed chronic lymphocytic leukemia. , 2013, The New England journal of medicine.

[38]  N. Rothman,et al.  Subtype-specific incidence rates of lymphoid malignancies in Hong Kong compared to the United States, 2001-2010. , 2016, Cancer Epidemiology.

[39]  Outside case review of surgical pathology for referred patients: the impact on patient care. , 2013, Archives of pathology & laboratory medicine.

[40]  T. Molina,et al.  Mediastinal gray zone lymphoma: clinico-pathological characteristics and outcomes of 99 patients from the Lymphoma Study Association , 2017, Haematologica.

[41]  Kai Fu,et al.  Lymphoma diagnosis at an academic centre: rate of revision and impact on patient care , 2014, British journal of haematology.

[42]  P. Gaulard,et al.  Breast implant-associated anaplastic large cell lymphoma: two distinct clinicopathological variants with different outcomes. , 2016, Annals of oncology : official journal of the European Society for Medical Oncology.

[43]  D. Weisenburger,et al.  Lymphoma incidence patterns by WHO subtype in the United States, 1992-2001. , 2006, Blood.

[44]  B. Coiffier,et al.  SUVmax reduction improves early prognosis value of interim positron emission tomography scans in diffuse large B-cell lymphoma. , 2011, Blood.