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ABSTRACT |
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ABSTRACT
INTRODUCTION
METHODS
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DISCUSSION
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We describe 12 cases of AIDS-related primary pulmonary lymphoma occurring between 1986 and 1996 in a large French cohort of HIV-infected patients. Diagnostic criteria were: (1) histologically proven lymphomatous pulmonary involvement; (2) absence of mediastinal and/or hilar adenopathy on chest radiography; (3) absence of extrathoracic lymphoma extension. All patients were severely immunodeficient at the time of diagnosis. All but one patient presented with B and/or nonspecific respiratory symptoms. Chest radiography showed one or more marginated nodule(s) or large mass. CT scan showed a cavitary lesion in five patients. No lymph node enlargement or specific pleural effusion was detected. Transthoracic needle biopsies were performed in 10 patients and avoided open-lung biopsy for the diagnosis of lymphoma in five patients. All but one of the primary pulmonary lymphoma were high-grade B-cell non-Hodgkin's lymphomas. Using antilatent membrane protein-1 antibodies and an Epstein-Barr-Virus-encoded RNA transcript-specific probe, latent EBV infection of tumor cells was demonstrated in every case. All but one of the patients received chemotherapy. The median survival time was 4 mo, and no patient was still alive at the cut-off date for this analysis. Progessive pulmonary lymphoma was the main cause of death, but infections were also frequent.
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INTRODUCTION |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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HIV infection predisposes patients to several cancers, especially Kaposi's sarcoma (KS), non-Hodgkin's lymphoma (NHL), and intraepithelial cervical or anal neoplasia (1, 2). Possible increases in other malignancies such as seminomas, malignant melanoma, myeloma, and non-small-cell lung cancer have also been noted (1, 2). Some of these tumors such as Epstein-Barr virus (EBV)-positive large-cell NHL and KS may have a viral cause (1).
KS and NHL are frequently responsible for lung disease in HIV-infected patients, but primary pulmonary involvement is rare (3). Cancers were responsible for only 0.3 to 0.6 episodes of respiratory disease per 100 person-years in a recent prospective cohort study, with 12 and eight cases of KS and lung carcinoma, respectively (5). No respiratory manifestations were attributed to pulmonary NHL. Clinical and/or necropsy series have shown pulmonary involvement in 1 to 71% of patients with disseminated AIDS-related NHL (4, 6- 10). This is usually associated with other sites of disease and is found during the staging process. The lung is rarely the initial or only site of involvement, and only a few case reports of AIDS-related primary pulmonary lymphoma (PPL) have been published (11). The aim of this study was to describe the clinical characteristics, pathologic findings, and role of EBV infection in 12 cases of histologically proven AIDS- related PPL.
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METHODS |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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Study Design
In December 1996, standardized questionnaires were sent to the heads of all clinical units and pathology laboratories treating HIV- infected adults in the Centre d'Information et de Soins de l'Immunodeficience Humaine (CISIH) de l'Est Parisien to collate all cases of PPL diagnosed between January 1986 and December 1996. AIDS- related PPL was defined by the following criteria, adapted from Cordier and colleagues (25): (1) histologically proven lymphomatous pulmonary involvement; (2) absence of mediastinal and/or hilar adenopathy on chest radiographic examination; (3) absence of extrathoracic lymphoma extension diagnosed before, during, or 3 mo after the diagnosis of pulmonary lymphoma, using a standardized evaluation, including negative results of abdominal ultrasound or CT scan and bone marrow examination. Primary or secondary central nervous system (CNS) lymphoma was also ruled out by normal neuroradiologic studies and lumbar puncture when indicated. One questionnaire per case was completed by the same clinician (P.R.) using the patient's medical charts.
To identify cases of PPL previously published in the medical literature, a Medline search was performed from 1980 to 1996 with the following keywords: lung neoplasm and HIV, AIDS-related lymphomas, HIV, and Epstein-Barr virus. Only well-documented reports of AIDS-related PPL were analyzed.
Collection of Patients' Characteristics and Follow-up
The following epidemiologic data were recorded at the time of PPL diagnosis: sex, age, HIV transmission category, CD4+ lymphocyte count, prior AIDS-defining conditions, previous treatment, and prophylaxis. The clinical features of PPL and other HIV-related diseases were recorded, together with EBV serologic status when available. In addition, chest radiography, chest CT scan, and fiberoptic bronchoscopy findings were reviewed to characterize the bronchopulmonary aspects of PPL. Total and differential blood cell counts, serum protein electrophoresis, and lactate dehydrogenase (LDH) plasma levels were also recorded.
Data on initial treatment and maintenance therapy were noted. Clinical and radiologic pulmonary responses were assessed 3 mo after initiation of therapy, when possible, according to World Health Organization criteria. The follow-up data were also recorded in each case until death. The cutoff date for the survival analysis was November 1997.
Histopathologic Analysis
All tissue samples were reviewed by the same pathologist (M.A.).
PPL was classified according to the updated Kiel classification (26),
and equivalents in the NCI Working Formulation (27) on the basis of
routine sections stained with hematoxylin-eosin and Giemsa. Histologic evaluation was completed on paraffin sections by immunohistochemical analysis using the streptavidin biotin peroxidase method.
The following T-cell, B-cell, and epithelial cell markers were studied:
anti-CD20, CD3, CD45, CD30 (DAKO, Trappes, France), antibodies
and anti-KL1 (Immunotech, Marseille, France) and anti-EMA antibodies (DAKO), respectively. In some cases additional immunohistochemical studies were done on frozen sections by using anti-CD19,
CD2, CD4, CD5, CD7, and CD8 antibodies (DAKO). Tumor cell immunoglobulin (Ig) expression was assessed on paraffin sections by
means of immunohistochemistry (IHC) (
and 
light and 
, 
, µ heavy Ig chains) (DAKO) and/or in situ hybridization (ISH) ( and light Ig chains) (DAKO). Genotypic evaluation based on Ig or T-cell
receptor gene rearrangement analysis was not performed because of
the retrospective nature of the study.
Latent EBV infection was tested for in all tumors by using, as previously described: (1) ISH with a specific probe for EBV-encoded RNA transcripts (EBER-1) (28) and (2) EBV-encoded latent membrane protein-1 (LMP-1) cell surface expression analysis by IHC (29). In nine cases, bcl-2 expression was also evaluated on frozen sections by means of IHC (DAKO).
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RESULTS |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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Twelve cases of PPL were included in this study. Five other cases were not included because the patients presented with both pulmonary and extrapulmonary lymphoma. During the same period 4,700 HIV-infected patients were seen in the CISIH de l'Est Parisien. This corresponded to an estimated standardized incidence rate of AIDS-related PPL of 0 to 0.3 per 100 person-yr in our HIV cohort.
Patient Characteristics
The general characteristics of the patients are given in Table 1.
All patients were known to be HIV-infected and were receiving Pneumocystis carinii prophylaxis. All but one had received
antiretroviral therapy. Although three patients had not developed an AIDS-defining condition (Table 1) prior to the diagnosis of PPL, all 12 patients had AIDS if the newer criterion
of absolute CD4 count 
200/µl is used. The mean time between the diagnosis of HIV seropositivity and PPL was 5 yr (1 to 8 yr), and the mean CD4+ cell count was 17/µl (4 to 50/µl).
All but one of the patients presented with B and/or pulmonary
symptoms. Only one case of PPL was discovered incidentally,
on a routine chest radiograph (Patient 7). The mean duration
of symptoms prior to the diagnosis of PPL was 2 mo (3 d to 4 mo), and onset was acute in two cases (Patients 9 and 10). Hematologic abnormalities were common (n = 9) but moderate
(data not shown) and nonspecific. The LDH plasma level was > 1.5 normal value in four patients. Serum protein electropheresis was always normal. No evidence of recent reactivation or primary EBV infection was found on the basis of available EBV serologic records (n = 5).
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Radiologic Features
The most common pattern observed on the chest radiograph
was a well-defined and rapidly progressive nodule (diameter
2 cm) or mass (> 2 cm) in the subpleural area (Table 1 and
Figure 1A). Multiple lesions were oberved in eight patients
and were unilateral in five patients. Chest radiography showed
no mediastinal lymphadenopathy or pleural effusion. Chest
CT scans were available in each case. Analysis of the mediastinum revealed no nodes exceeding 1 cm in diameter. Cavitary
lesions were observed in five patients (Figure 1B), and an air
bronchogram was seen in two. In one patient (Patient 11), the
PPL presented as a pseudo-liquid mass of the left cardiophrenic angle. In one patient (Patient 2), recent P. carinii
pneumonia (PCP) caused ground-glass attenuation on the
lung CT scan, which later disappeared. In one case (Patient
10), a small pleural effusion was seen on the CT scan; analysis
of the pleural fluid failed to reveal malignant cells.
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Diagnostic Procedures and Histologic Findings
Bronchoscopy with bronchoalveolar lavage (BAL) was performed in 11 of the 12 patients. There were no endobronchial abnormalities, and routine bronchial biopsies were negative. BAL identified intercurrent pulmonary PCP in one case (Patient 2) and malignant hematologic cells in another (Patient 12). Pulmonary transbronchial biopsies (TBB) were negative in three patients.
In two patients, the diagnosis of NHL was obtained directly by open lung biopsy (OLB) (n = 1) or necropsy (n = 1). Transthoracic needle biopsies (TTNB) of the pulmonary mass were performed in the other 10 patients. Histologic analysis led to the diagnosis of NHL in five patients. In the other five the diagnosis of NHL was finally obtained by OLB. A malignancy had been suspected on TTNB in three of these patients, but the precise nature of the tumor, i.e., epithelial or lymphoid, could not be ascertained. Pathologic findings are summarized in Table 2. The macroscopic aspect of the tumor was analyzed on tissue specimens from the six OLBs and four autopsies. The PPL presented as whitish or yellowish solid nodules or masses in the eight patients, centered by a large area of necrosis in three (Figure 2). Histologically, the lymphomatous process widened, distorted, and invaded the alveolar septa and vascular walls in every case (Figure 3A). Necrosis was observed microscopically in nine patients. Although all the PPLs were high-grade NHL, six were difficult to classify cytologically. They were considered as "high-grade not otherwise specified" (HGNOS) (n = 5) or "polymorph lymphoid proliferation" (PLP) (n = 1) according to the updated Kiel classification (30). All but one were of the B-cell phenotype (Patient 3) (Figure 3B). In this latter case, examination of the paraffin sections was inconclusive and required studies on frozen sections to conclude to a nul-type anaplastic lymphoma. Immunoglobulin expression by tumor cells was detected by means of IHC and/or ISH in six patients, of which two had a monotypic expression (Patients 2 and 8). By contrast, latent EBV infection was detected in tumor cells in every case, either by LMP-immunostaining expression and/or by EBV-ISH analysis (Table 2) (Figures 4A and 4B). Furthermore, bcl-2 expression was also detected by immunostaining in seven of the nine tumors examined (Figure 4C).
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Follow-up Data
One patient died before treatment (Patient 8). The other 11 patients were initially treated with chemotherapy (Table 3). All but one of these 11 patients received hematopoietic growth factors because of severe hematologic toxicity. Bacterial and opportunistic infections developed during treatment in seven cases. Objective responses had been evaluated at 3 mo in only seven patients, the other five having died. There were two complete responses, three partial responses, and two cases of progression during chemotherapy. All patients were dead in November 1997. The median survival time after the diagnosis of PPL was 4 mo (< 1 to 17 mo). Death was associated with PPL progression in the 12 patients, but six had intercurrent conditions, comprising acute respiratory failure (n = 1), wasting (n = 3), and infections (n = 2).
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DISCUSSION |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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AIDS-related PPL seems to be rare. The standardized incidence rate was estimated at 0 to 0.3 per 100 person-yr in our cohort of 4,700 HIV-infected adults, and, using the same diagnostic criteria as in this study, we found only 16 such cases in the literature between 1980 and 1996 (11, 22). One of the latter cases was included in the present series (Patient 10) (11). Two published cases were not taken into account because of their particular histologic type (one lymphoma of mucosa-associated lymphoid tissue and one lymphomatoid granulomatosis) (23, 24).
In our series, AIDS-related PPL had features very similar to those of previously published cases (Table 4). AIDS-related PPL occurred in the later stages of HIV disease. The immune deficiency was severe, as reflected by a very low CD4+ cell count (< 50/µl) and previous AIDS-defining conditions in the majority of cases (Tables 1 and 4. Subacute respiratory and B symptoms were present in almost all the patients, but they were nonspecific. Chest pain and/or dyspnea led to the diagnosis of pulmonary embolism in three of our patients (Patients 5, 9, and 10), but this was not confirmed by pulmonary angiogram and/or ventilation-perfusion radionuclide lung scan. Two patients, one described in the literature (22) and one in the present series (Patient 7), were asymptomatic. Physical findings were also nonspecific. Crackles, coarse inspiratory or expiratory rales, dullness on percussion, and decreased breath sounds have been described (14, 15, 19). Laboratory investigations showed hematologic abnormalities such as anemia, thrombopenia, and/or leukopenia, which were difficult to attribute to the PPL or to HIV disease or therapy, as almost all the patients were receiving antiretroviral drugs or prophylactic treatments. Contrary to disseminated AIDS-related NHL (4), LDH plasma levels are rarely and usually only moderately elevated in AIDS-related PPL.
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Virtually all cases of AIDS-related PPL involved one or multiple nodules or a large mass in the subpleural area, possibly explaining the chest pain reported by 40% of patients. Furthermore, in more than 40% of our cases nodular opacities were centered by a necrotic cavity confirmed histologically. The radiologic pattern was less uniform in the literature, other abnormalities, including laterotracheal opacity (14), interstitial infiltrates (13, 21), and thoracic empyema (16). These features differ slightly from radiologic findings in disseminated AIDS-related NHL (4, 30). Mediastinal involvement and pleural effusion were absent on chest radiography and CT in patients with PPL, but they were observed in 21 to 54% and 44 to 73% of patients with disseminated AIDS-related NHL (4, 30). In addition, disseminated AIDS-related NHL is less frequently responsible for nodules or masses, and cavitary lesions are very unusual (4) relative to PPL.
The first diagnosis raised was usually pulmonary infection (21, 31), and BAL was done for microbiologic evaluation in the vast majority of patients. It did not lead to a diagnosis of PPL, but it sometimes disclosed intercurrent pulmonary infections (Table 1) (13, 17, 21, 22). Bronchial biopsy during fiberoptic bronchoscopy was noncontributory to the diagnosis of AIDS-related PPL, except in two reported cases with visible endobronchial lesions (14, 20). Open-lung biopsy was performed in 56% of cases, and yielded the diagnosis of PPL in every case. However, TTNB, a less invasive and relatively sensitive diagnostic procedure, led to a firm diagnosis of PPL in 50% of our patients and thus avoided the need for OLB in these patients.
Five cases of AIDS-related PPL published in the literature
were of the T-cell lineage (12, 15, 18, 19, 21). This is unexpected, as T-cell lymphoma accounts for only a few percent of
all cases of AIDS-related NHL (1, 2). Four cases in the literature were described as diffuse, mixed (small and large) cell
NHL, according to the Working Formulation (18) or as
intermediate or high-grade malignant lymphomas in the updated Kiel classification. By contrast, almost all our cases of
AIDS-related PPL were high-grade B-cell NHL. About 60%
of cases were HGNOS or immunoblastic (IB), whereas no
cases of Burkitt-like lymphoma were observed. This may be
due to the severe immune deficiency in patients with AIDS-related PPL (see above). Few data have been published on immunoglobulin expression in AIDS-related NHL, and none on
PPL (29, 32, 33). As in AIDS-related NHL, Ig expression by
tumor cells was detected in about 50% of our cases of PPL
(32), but only two patients showed monotypic Ig expression
(one IgA and the other IgA) (Table 2). One of the most interesting findings in this series was the detection of latent
EBV infection in tumor cells from all our patients with AIDS-related PPL, based on the detection of EBV early region
(EBER-1) transcripts by means of ISH. Moreover, they also
expressed LMP-1 protein, which has transforming potential in
vitro (1). This protein interacts with members of the tumor necrosis factor receptor protein family, which are involved in proliferation/apoptosis cell regulation and also induce the expression of bcl-2, an oncoprotein that also inhibits apoptosis
(1). In this context, it should be underlined that bcl-2 expression was demonstrated in seven of the nine tumors tested in
our series. Latent EBV infection has never previously been
described in AIDS-related PPL. However, a similar pattern of
EBV infection has been observed in about 50% of cases of
AIDS-related NHL, and in virtually all cases of IB and/or primary CNS lymphoma (1, 28, 29, 32). In these latter cases,
LMP-1 and bcl-2 expression were also closely associated (34).
All but one of the patients in our series received chemotherapy, as recommended for patients with AIDS-related NHL and severe immune deficiency (35). The median survival time of 4 mo in our series is similar to that of the six patients treated with chemotherapy in the literature (3 mo; range, 1 to 18 mo). It is lower than that described for all forms of AIDS-related NHL, but comparable to that of patients with factors of poor prognosis, i.e., prior AIDS, low CD4+ cell count, Karnofsky performance status less than 70%, and bone marrow involvement or primary CNS lymphoma (1, 2, 6, 7, 35). The evaluable survival time of the four untreated patients described in the literature was 6, 19, 13, and 8 mo (16, 19, 20, 22). In our series and in previously reported cases, PPL progression was the major cause of death (Table 3) (14, 15, 19, 20, 22, 35), but opportunistic (Table 3) (12, 17, 20, 21) and bacterial infections also occurred frequently (Table 3) (13, 14, 16, 20).
Although rare, AIDS-related PPL appears to be a homogeneous clinical, radiologic, and pathologic entity differing from AIDS-related NHL with pulmonary dissemination. The differences between these two distinct entities should be known since diagnostic strategy, prognosis, and treatment should strongly differ. PPL seems to be related to severe immune deficiency and reactivation of latent EBV infection within the lung, as in AIDS-related primary CNS lymphoma. Given the grim prognosis, noninvasive diagnostic procedures such as transthoracic needle biopsy and less toxic treatment protocols should be considered first, including an effective treatment of the HIV disease by a combination of three antiretroviral drugs.
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Footnotes |
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Correspondence and requests for reprints should be addressed to Pr. J. Cadranel, Service de Pneumologie et de Réanimation Respiratoire, Hôpital Tenon, 4 rue de la Chine, 75020-Paris, France.
(Received in original form January 15, 1998 and in revised form May 13, 1998).
Acknowledgments: The writers thank C. Bonnement (UPRES EA 1531, Hôpital Tenon, UFR Saint-Antoine), F. Commo, and M. Perdereau (Service d'Anatomie Pathologique, Hôpital Tenon) for their technical assistance. They also thank Drs. F.-P. Chatelet and C. Normand (Service d'Anatomie Pathologique, Hôpital Rotschild, Paris), C. Danel (Service d'Anatomie Pathologique, Hôpital Laënnec, Paris), and C. Sagan (Service d'Anatomie Pathologique, Hôpital Laënnec, Nantes) for contributing pathologic specimens, and the members of the CISIH de l'Est Parisien for their collaboration.
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References |
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DISCUSSION
REFERENCES
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