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1 Role of Surgery in the Treatment of Primary Pulmonary B-Cell Lymphoma Frederic Vanden Eynden, MD, Elie Fadel, MD, Marc de Perrot, MD, MS, Vincent de Montpreville, MD, Sacha Mussot, MD, and Philippe Dartevelle, MD Department of Thoracic and Vascular Surgery and Heart-Lung Transplantation, Marie Lannelongue Hospital, Le Plessis Robinson, France Background. The purpose of this study was to define the role of surgery in the treatment of primary pulmonary lymphoma (PPL). Methods. We reviewed all patients presenting with a pathologic diagnosis of PPL in our institution during the past 20 years. We analyzed the outcome and determined the impact of complete versus incomplete surgical resection on survival. Results. The study included 17 patients with PPL confined to the pulmonary parenchyma. Pathologic diagnosis was low-grade B-cell PPL in 14 patients, high-grade B-cell PPL in 2, and lymphomatoid granulomatosis in 1. A complete resection was performed in 8 patients presenting with low-grade B-cell PPL and in 2 patients with high-grade B-cell PPL. The overall survival of patients presenting with low-grade B-cell PPL was 63% at 10 years; however, survival at 10 year tended to be better when a complete resection was performed (87.5% vs 25%, respectively; p 0.08). Gender, bilateral disease, or adjuvant therapy did not affect survival. Both patients presenting with high-grade B-cell PPL are alive and free of disease 22 and 36 months after the surgery, respectively. The patient presenting with lymphomatoid granulomatosis is alive after 2 years of follow-up. Conclusions. PPL is a rare disease that may be localized or diffuse in one or both lungs. Surgery should be the treatment of choice in the localized form of PPL if complete resection can be achieved. A complete resection is associated with an excellent long-term survival of almost 90%. If the lesions are diffuse or involve both lungs, medical therapy should then be the treatment of choice. (Ann Thorac Surg 2007;83:236 40) 2007 by The Society of Thoracic Surgeons Thoracic surgeons are seldom confronted with hematologic malignancies, except for biopsy purposes; however, some hematologic diseases can be limited to the lung parenchyma and may be best treated with surgery. Primary pulmonary lymphoma (PPL) is defined by clonal lymphoid proliferation affecting one or both lungs (parenchyma or bronchi, or both) in a patient with no detectable extrapulmonary involvement at diagnosis or during the subsequent 3 months [1]. PPL is a rare entity accounting for only 0.5% to 1% of all lung malignancies and less than 1% of non-hodgkin lymphomas [1]. Histologically, most PPL are classified as mucosa-associated lymphoid tissue (MALT) according to the latest classification of the World Health Organization (WHO) Classification [2], and can be referred to as BALTOMAs (for bronchial-associated lymphoid tissue affection) or pulmonary MALTOMA [3]. MALT lymphomas are low-grade B-cell lymphoma, formerly known as pseudolymphoma because of its indolent course. However, a higher-grade of B-cell lymphoma (large cell lymphoma) can occasionally be seen in association with MALT. In the literature, MALT lymphoma accounts for 58% to 87% of all PPL [1]. Despite the similarities with gastric MALTOMAs, where a chronic antigenic stimulation related to Helicobacter pylori infection has been demonstrated, no such relationship has been established for low-grade B-cell PPL in the lung. High-grade B-cell PPL is less frequent, 11% to 19% of the PPLs in published series [4, 5], and has a worse prognosis than low-grade PPL. It usually occurs in immunosuppressed patients, is often seen in HIV patients or transplant recipients, and is related to Epstein-Barr virus infection [6]. Lymphomatoid granulomatosis is very rare ( 1000 cases reported in the literature) and has a very variable course, ranging from spontaneous remission to death. Treatment is essentially medical, and the surgeon is only involved for diagnostic purposes [7, 8]. To increase the reports on this rare disease and to define the role of surgery in the treatment of PPL, we reviewed all patients presenting with a pathologic diagnosis of PPL in our institution during the past 20 years. We analyzed the outcome and determined the impact of a complete versus incomplete surgical resection on survival. Accepted for publication Aug 18, Address correspondence to Dr Fadel, Department of Thoracic and Vascular Surgery and Heart-Lung transplantation, Marie Lannelongue Hospital, 133 Avenue de la Résistance, Le Plessis Robinson, France; fadel@ccml.com. Material and Methods We performed a computer search in our pathology database to identify patients with a biopsy-proven PPL operated on in our institution between 1985 and For all 2007 by The Society of Thoracic Surgeons /07/$32.00 Published by Elsevier Inc doi: /j.athoracsur
2 Ann Thorac Surg VANDEN EYNDEN ET AL 2007;83: SURGERY FOR PRIMARY PULMONARY B CELL LYMPHOMA 237 Fig 1. Low-grade primary pulmonary lymphoma. (A) Gross aspect of a surgical specimen shows a parenchymal infiltrative homogeneous soft and nonnecrotic mass surrounding the bronchi of a middle lobe. (B) Histologic appearance of the interstitial and peribronchovascular nodular proliferation of small and regular lymphocytes (hematein and eosin stain.) at original magnification 40. (C) Original magnification 400. patients in the study cohort, an individual chart review was performed, with approval obtained from the Institutional Review Board, which waived the need for informed consent. The diagnosis of PPL was based on characteristic histologic and immunophenotypical features according to the Kiel classification and the WHO classification [2]. Immunophenotyping was determined by immunohistochemical staining, and clonality was characterized according to the type of immunoglobulin on the malignant cell surface. Malignant cells were tested for CD3, CD5, CD10, L26 (CD20), and UCHLl (CD45RO) antigen expression. The records of the patients fulfilling criteria for PPL were reviewed, and clinical data were collected as well as medical history, laboratory data, radiologic findings at the time of diagnostic, diagnostic procedure, treatment, and follow-up. Duration of follow-up was calculated from the date of diagnosis to the date of death or to the last follow-up visit. Patient survival was estimated using the Kaplan- Meier method. Differences in survival were compared using the log-rank test. A value of p 0.05 was considered significant. Results We identified 17 patients (11 men, 6 women) fulfilling the criteria for PPL, with a median age of 60 years (range, 33 Fig 2. High-grade primary pulmonary lymphoma. Histologic appearance of the large atypical tumor cells invading bronchial mucosa (hematein and eosin stain). (A) Original magnification 100, and (B) 400.
3 238 VANDEN EYNDEN ET AL Ann Thorac Surg SURGERY FOR PRIMARY PULMONARY B CELL LYMPHOMA 2007;83: Table 1. Clinical Characteristics Characteristic Patients, n (%) Median age at diagnosis 60 years Pathologic features Low-grade B-cell lymphoma 14 (82) High-grade B-cell lymphoma 2 (11) Lymphomatoid granulomatosis 1 (5) Sex Male 11 (65) Female 6 (35) Smoking history 8 (47) Associated autoimmune disease 1 (5) Gastric MALT lymphoma 2 (11) Incidental findings 4 (23) Pulmonary findings 9 (52) Cough 5 (30) Chest pain 1 (5) Dyspnea 2 (11) Hemoptysis 1 (5) Systemic symptoms 4 (23) Weight loss 1 (5) Fever 3 (17) MALT mucosa-associated lymphoid tissue. to 71 years). Pathologic diagnosis was low-grade B-cell PPL (MALT lymphoma) in 14 patients (82%; Fig 1) and high-grade B-cell lymphoma in 2 patients (11%; Fig 2). Lymphomatoid granulomatosis was observed in 1 patient. The mean follow-up was 4.3 years (range, 10 weeks to 15 years). Clinical Characteristics Clinical characteristics are presented in Table 1. Two patients with low-grade B-cell PPL had been treated for gastric MALTOMA 5 and 9 years before the diagnosis of PPL. One patient with low-grade B-cell PPL had been exposed to asbestos, 1 had been infected with tuberculosis in childhood, and 1 patient had rheumatoid arthritis. Four patients were asymptomatic, 9 presented with pulmonary symptoms, and 4 had systemic symptoms such as fever (n 3) or weight loss (n 1). Both patients with high-grade B-cell PPL were symptomatic. Radiologic Characteristics All patients had a chest roentgenogram and a computed tomography (CT) scan as part of the preoperative work-up. Four patients presented with bilateral disease, and 13 had unilateral disease. Unilateral PPL was characterized by parenchymal infiltrates in 10 patients, hilar enlargement in 2, or lobar consolidation in 1. The staging was completed postoperatively with abdominal and head and neck CT scans and a bone marrow biopsy. The extrathoracic staging was always negative to fit the criteria for PPL. Treatment Sixteen patients had a thoracotomy (Table 2). One patient presenting with bilateral disease underwent a thoracoscopic lung biopsy. Patients presenting with low-grade B-cell PPL underwent wedge resections (n 6), lobectomy (n 6), or lobectomy associated with wedge resection (n 2). Complete resection was achieved in 8 patients. The resection was incomplete in 6 patients because of diffuse involvement of both lungs (n 3) or multiple lobes within the same lung (n 3). Table 2. Operative Procedure and Status at Last Follow-Up Histology Bilateral Procedure Complete Resection Status (follow-up) Lymphoma type Low-grade B-cell Yes Lobectomy contralateral wedge resection Yes Alive (18 months) Low-grade B-cell Yes Wedge resection No Dead (21 months) Low-grade B-cell Yes Wedge resection No Alive (53 months) Low-grade B-cell No Lobectomy Yes Dead (121 months) Low-grade B-cell No Wedge resection No Alive (10 months) Low-grade B-cell No Wedge resection No Dead (43 months) Low-grade B-cell No Lobectomy Yes Dead (13 months) Low-grade B-cell No Lobectomy Yes Alive (182 months) Low-grade B-cell No Wedge resection Yes Alive (90 months) Low-grade B-cell No Lobectomy wedge resection Yes Alive (67 months) Low-grade B-cell No Lobectomy Yes Alive (55 months) Low-grade B-cell No Lobectomy Yes Alive (26 months) Low-grade B-cell No Llobectomy No Dead (25 months) Low-grade B-cell Yes Wedge resection No Alive (12 months) High-grade No Pneumectomy Yes Alive (22 months) High-grade No Pneumectomy SVC reconstruction Yes Alive (36 months) Lymphomatoid granulomatosis No Lung biopsy No Alive (24 months) SVC superior vena cava.
4 Ann Thorac Surg VANDEN EYNDEN ET AL 2007;83: SURGERY FOR PRIMARY PULMONARY B CELL LYMPHOMA 239 Fig 3. Life-table graphs of survival rates after surgery in patients with primary pulmonary low-grade B-cell lymphoma according to surgical resection status (complete versus incomplete resection; p 0.08). Both patients presenting with high-grade B-cell lymphoma underwent pneumonectomy to achieve complete resection. The pneumonectomy was associated with superior vena cava resection and reconstruction in the first patient. The second patient had a lung biopsy and underwent induction chemotherapy before the pneumonectomy. Adjuvant chemotherapy was given to both patients with high-grade B-cell lymphoma. Six patients (43%) with low-grade B-cell lymphoma received adjuvant chemotherapy (n 3), adjuvant radiation therapy (n 2), or adjuvant chemoradiation therapy (n 1). Eight patients with low-grade B-cell lymphoma who underwent complete resection did not receive any adjuvant therapy. The patient presenting with lymphomatoid granulomatosis did not receive any postoperative treatment after lung wedge resection. Survival The overall survival of patients presenting with lowgrade B-cell PPL was 63% at 10 years; however, the 10-year survival rates reached 87.5% in patients who had complete resection and tended to be better than in patients who had an incomplete resection (10-year survival, 25%; p 0.08; Fig 3). Gender, bilateral disease, or the administration of adjuvant therapy did not affect survival. During follow-up, 5 patients died, 1 from disease-related cause and 4 from unrelated causes. Nine patients with low-grade B-cell PPL are alive and free of disease. Both patients presenting with high-grade B-cell PPL are alive and free of disease at 22 and 36 months after the surgery, respectively. The patient presenting with lymphomatoid granulomatosis is alive after 2 years. Comment Primary pulmonary lymphomas are uncommon cancers arising from the lymphoreticular system of the lung and are estimated to occur in approximately 0.5% of all primary lung tumors [9]. They include solitary plasmocytoma, primary Hodgkin disease, and non-hodgkin lymphoma of the lung. Primary pulmonary non-hodgkin lymphoma is the most common PPL and is almost always of the B-cell type. B-cell PPL arises from bronchusassociated lymphoid tissue (BALT lymphoma) or from mucosa-associated lymphoid tissue (MALT lymphoma). Most are low-grade B-cell PPL [10]. The natural history and the prognosis of B-cell PPL is similar to that of MALT lymphoma seen in the gastric mucosa. Chronic inflammatory factors have been advocated to explain the development of MALT lymphoma, such as H pylori infection in the gastric location [10]. Chronic infection, smoking, or autoimmune disease may play a role in the development of B-cell PPL. Interestingly, 2 of our patients had been previously treated for gastric MALT lymphoma. Our data are consistent with the literature regarding patient age and the proportion of low-grade to highgrade PPL [4, 9, 11, 12]; however, we observed a larger proportion of symptomatic patients than in other series [13]. Both patients with high-grade lymphoma and 10 of 14 patients with low-grade lymphoma were symptomatic in our experience. The diagnosis is often made at the time of surgery because radiologic signs are usually not specific and bronchoscopy has a low diagnostic yield [4]. The presence of lymphocytic alveolitis with more than 10% of B cells in bronchoalveolar lavage can be diagnostic [14]. Preoperative CT-guided fine needle aspiration biopsy allows diagnosis of PPL in only 25% of patients [8]. The diagnosis is thus often made intraoperatively on frozen section and confirmed postoperatively by immunostaining. A preoperative or postoperative work-up should be performed in all patients, including abdominal and head and neck CT scans and a bone marrow biopsy. By definition, all patients should have negative results on extrathoracic imaging and the bone marrow study to meet the criteria for PPL. If significant ( 1 cm) mediastinal lymph nodes are found on a preoperative chest CT scan, a mediastinoscopy should be performed first to obtain a diagnosis. If the diagnosis of PPL is made on frozen section, a mediastinal lymph node dissection should be performed at the time of surgery, even though in our experience the result was negative in most patients. Although survival is worse for patients with highgrade PPL than in those with low-grade PPL, published reports show that more than half of patients with highgrade PPL can achieve survivals of 8 to 10 years [15]. Both of our patients with high-grade lymphoma are currently alive, with no recurrence 22 and 36 months after pneumonectomy performed to achieve complete resection. In both cases, the decision to perform a pneumonectomy was based on the possibility to perform a complete resection in the absence of response to chemotherapy. The natural history of low-grade lymphoma appears to be slow, and its treatment is controversial [16]. Some authors advocate no therapy because of its indolent course, whereas others recommend surgery or chemotherapy, or both [1, 17]. Recent series did not demonstrate any difference in survival between surgery and chemotherapy or a combination [4, 9, 11, 12, 18]. The treatment was not
5 240 VANDEN EYNDEN ET AL Ann Thorac Surg SURGERY FOR PRIMARY PULMONARY B CELL LYMPHOMA 2007;83: always detailed, however, and the follow-up varied according to the series. In addition, the type of treatment may be influenced by the presence of multifocal or bilateral disease. The number of patients with multifocal disease varies between 24% and 70% according to the reported series [13, 19, 20]. We believe surgery should be the treatment of choice if a complete resection can be achieved. A complete resection was associated with a 10-year survival of almost 90% in our series, and survival tended to be better than in patients who underwent partial resection only. Patients presenting with diffuse involvement of one or both lungs should be treated with chemotherapy or chemoradiation therapy. Although some authors have recommended a pneumonectomy for multiple lesions of low-grade PPL involving one lung, in our view this option may be too aggressive because of the indolent course of the disease. We find, however, that a complete resection is an option in limited bilateral disease, as in one of our patients. In conclusions, PPL is a rare disease that may be localized or diffuse in one or both lungs. Surgery should be the treatment of choice in the localized form of PPL if complete resection can be achieved. A complete resection was associated with a 10-year survival of almost 90% in our series. If the lesions are diffuse or involve both lungs, medical therapy should then be the treatment of choice. References 1. Cadranel J, Wislez M, Antoine M. Primary pulmonary lymphoma. Eur Respir J 2002;20: Harris NL, Jaffe ES, Stein H, et al. A revised European- American classification of lymphoid neoplasms: a proposal from the International Lymphoma Study Group. Blood 1994; 84: Li G, Hansmann ML, Zwingers T, Lennert K. Primary lymphomas of the lung: morphological, immunohistochemical and clinical features. Histopathology 1990;16: Cordier JF, Chailleux E, Lauque D, et al. Primary pulmonary lymphomas. A clinical study of 70 cases in nonimmunocompromised patients. Chest 1993;103: Fiche M, Caprons F, Berger F, et al. Primary pulmonary non-hodgkin s lymphomas. Histopathology 1995;26: Abehsera M, Estenne M, Antoine M, Gevenois PA. [Pulmonary opacity and heart transplant. Primary pulmonary lymphoma (large-cell anaplastic)]. Rev Med Brux 1992;13: Fauci AS, Haynes BF, Costa J, Katz P, Wolff SM. Lymphomatoid granulomatosis. Prospective clinical and therapeutic experience over 10 years. N Engl J Med 1982;306: Pisani RJ, DeRemee RA. Clinical implications of the histopathologic diagnosis of pulmonary lymphomatoid granulomatosis. Mayo Clin Proc 1990;65: Kim JH, Lee SH, Park J, et al. Primary pulmonary non- Hodgkin s lymphoma. Jpn J Clin Oncol 2004;34: Graham BB, Mathisen DJ, Mark EJ, Takvorian RW. Primary pulmonary lymphoma. Ann Thorac Surg 2005;80: Ahmed S, Kussick SJ, Siddiqui AK, et al. Bronchialassociated lymphoid tissue lymphoma: a clinical study of a rare disease. Eur J Cancer 2004;40: Ferraro P, Trastek VF, Adlakha H, Deschamps C, Allen MS, Pairolero PC. Primary non-hodgkin s lymphoma of the lung. Ann Thorac Surg 2000;69: Kurtin PJ, Myers JL, Adlakha H, et al. Pathologic and clinical features of primary pulmonary extranodal marginal zone B-cell lymphoma of MALT type. Am J Surg Pathol 2001;25: Davis WB, Gadek JE. Detection of pulmonary lymphoma by bronchoalveolar lavage. Chest 1987;91: L Hoste RJ Jr, Filippa DA, Lieberman PH, Bretsky S. Primary pulmonary lymphomas. A clinicopathologic analysis of 36 cases. Cancer 1984;54: Lee DK, Im JG, Lee KS, et al. B-cell lymphoma of bronchusassociated lymphoid tissue (BALT): CT features in 10 patients. J Comput Assist Tomogr 2000;24: Addis BJ, Hyjek E, Isaacson PG. Primary pulmonary lymphoma: a re-appraisal of its histogenesis and its relationship to pseudolymphoma and lymphoid interstitial pneumonia. Histopathology 1988;13: Habermann TM, Ryu JH, Inwards DJ, Kurtin PJ. Primary pulmonary lymphoma. Semin Oncol 1999;26: Wislez M, Cadranel J, Antoine M, et al. Lymphoma of pulmonary mucosa-associated lymphoid tissue: CT scan findings and pathological correlations. Eur Respir J 1999;14: Zinzani PL, Tani M, Gabriele A, et al. Extranodal marginal zone B-cell lymphoma of MALT-type of the lung: singlecenter experience with 12 patients. Leuk Lymphoma 2003; 44:821 4.
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