Ann Thorac Surg 2003;76:967-972
© 2003 The Society of Thoracic Surgeons
Review
Endobronchial presentation of Hodgkin lymphoma: a review of the literature
Bahram Kiani, BSa,
Cynthia M. Magro, MDb,
Patrick Ross, Jr, MD, PhDc*
a Department of Pathology, The Ohio State University College of Medicine and Public Health, Columbus, OH USA
b Department of Department of Pathology Columbus, OH USA
c Department of Cardiothoracic Surgery, The Ohio State University Medical Center, Columbus, Ohio USA
* Address reprint requests to Dr Ross, Department of Cardiothoracic Surgery, Ohio State University, N816 Doan Hall, 410 West 10th Avenue, Columbus, OH 43210, USA
e-mail: ross-3{at}medctr.osu.edu
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Abstract
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Endobronchial presentation of Hodgkin lymphoma is exceedingly rare and can be confused clinically with pulmonary small cell carcinoma. Because of the dramatic implications in treatment and prognosis, endobronchial Hodgkin lymphoma, despite its uncommon occurrence, should be considered in the differential of small cell carcinoma and necrotizing vasculitides with pulmonary involvement, especially in a relatively young patient with cough, hemoptysis, atelectasis, and hilar or mediastinal lymphadenopathy. The use of photodynamic laser therapy or stent placement for palliative treatment of life-threatening airway obstruction may be required prior to or as an initial adjunct to tumor-specific therapy.
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Introduction
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Hodgkin lymphoma usually involves the mediastinum of newly diagnosed patients [1, 2]. Hilar and mediastinal lymphadenopathy are common radiographic manifestations [3, 4], whereas pulmonary involvement in Hodgkin lymphoma is less common and can be seen in the lymph nodes, parenchyma, and tracheobronchial tree, usually in association with hilar or mediastinal adenopathy [4–8]. Despite the more common occurrence of bronchial Hodgkin lymphoma in autopsy data [5, 9–12], antemortem endobronchial involvement in Hodgkin lymphoma is rare [5, 13–16], usually manifesting in patients with established disease. The resulting gross appearance of the lesion along with the patient’s clinical presentation may mimic small cell carcinoma. Unrecognized, the result can include understaging of the disease that can compromise the cure, devastating the patient emotionally with a less favorable diagnosis, and subjecting the patient to needlessly aggressive treatments.
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Material and methods
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Cases of endobronchial Hodgkin lymphoma were identified in the literature from 1966 by a National Library based Pub Med search. Cases antedating 1966 were identified from references alluded to in articles published in 1966 and beyond. Following the criteria of Tredaniel and coworkers [14], the recognition of endobronchial presentation of Hodgkin lymphoma required histologically proven Hodgkin lymphoma with bronchoscopic visualization of the tumor at the time of the initial diagnosis. We excluded reports for which no tumor was bronchoscopically visualized, even if extrinsic compression was seen. In addition, we excluded reports of endotracheal involvement that had no concomitant endobronchial involvement, because those cases are not so easily confused with small cell carcinoma. This gives a total of 26 patients of endobronchial presentation of Hodgkin lymphoma in the English-written literature. Two additional non-English publications from beyond 1966 describe endobronchial Hodgkin lymphoma [17, 18].
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Comment
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Hodgkin lymphoma is unique as a lymphoma in that the neoplastic cell component is associated with a variant inflammatory host response comprising lymphocytes, plasma cells, and eosinophils. Hodgkin lymphoma is divided into: (1) classic Hodgkin lymphoma, the spectrum of which encompasses nodular sclerosing, mixed cellularity, and lymphocyte-depleted forms; and (2) nodular/diffuse lymphocyte-predominant Hodgkin lymphoma. The neoplastic cell is a large monocytoid cell with frequent binucleation whose histogenesis was questioned for many years. It has now been established to represent a B-cell lymphoma, manifesting a characteristic phenotype of B-cell and or null-cell phenotype with CD30 positivity. Coexpression of CD15 is typical for cases of classic Hodgkin lymphoma whereas the neoplastic cells in lymphocyte-predominant Hodgkin lymphoma are CD15 negative.
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Clinical features at initial presentation
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Occlusion of a main bronchus in endobronchial Hodgkin lymphoma may give a patient a variety of nonspecific respiratory symptoms, including dry or productive cough, hemoptysis, dyspnea, wheezing, chest pain or discomfort, and stridor. Although it is rare, endobronchial Hodgkin lymphoma is an important diagnosis because early intervention can be curative [13] (Table 1).
Twenty-six patients presenting with endobronchial Hodgkin lymphoma, fulfilling the criteria mentioned above have now been reported in the English-written literature [6, 11, 13, 14, 16, 19–25]. A number of these reports were published decades ago and contain less data than more recent ones. The average age of presentation in these patients is 42.3 years with a slight male preponderance.
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Respiratory signs
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Respiratory signs were noted in the majority of patients with cough being the most frequent sign. In those patients with cough, hemoptysis was observed in almost half of cases and, although a relatively nonspecific sign, it is an unusual occurrence in Hodgkin lymphoma without endobronchial or endotracheal presentation [14, 26]. Dyspnea was observed in almost one-third of patients. Less common symptoms included wheezing, chest discomfort, and stridor.
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Bronchoscopic findings
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Every patient bronchoscopically demonstrated endobronchial invasion with the most frequent presentation being one of an obstructing polypoid lesion. Endobronchial lymphomas have also been reported in the form of superficially ulcerated mucosal plaquelike infiltrates [9, 10, 27–29], hence simulating bronchogenic carcinoma. There was a slightly higher incidence of right bronchial tree involvement compared with the left bronchial tree, and in a minority of patients, both the right and left bronchial trees were involved. Concomitant tracheal involvement occurred but was very uncommon being reported in only about 10% of cases. Endobronchial biopsies were conclusive of Hodgkin lymphoma in roughly two-thirds of the patients. Of the remaining patients, half had endobronchial biopsies that were histologically similar to that of the final diagnostic specimens (mostly lymph nodes), but were still ultimately inconclusive for a definitive diagnosis.
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Radiographic features
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Radiographically mediastinal or hilar lymphadenopathy or mass was present in about two-thirds of patients. Atelectasis, present in almost half of patients with endobronchial Hodgkin lymphoma, is far more frequent in endobronchial Hodgkin lymphoma than in cases of intrathoracic Hodgkin lymphoma; in the series by Filly and colleagues [3], only 1/164 patients (0.6%) of intrathoracic Hodgkin lymphoma exhibited radiographic evidence of atelectasis and consolidation. Atelectasis may be an indicator of endobronchial Hodgkin lymphoma, but it may also result from extrinsic compression of the bronchial tree by a nodal or tumor mass. Pleural effusion was another radiographic abnormality and was present in less than 20% of patients. Rarely patients characterized no radiographic abnormality.
Hilar and mediastinal lymphadenopathy are common radiographic manifestations of newly diagnosed patients with Hodgkin lymphoma [1, 2]; 67% to 87% of patients had radiographic evidence of intrathoracic lymph node involvement in two studies [3, 4]. Pulmonary involvement in Hodgkin lymphoma is less common, with some series estimating a 40% frequency [5, 24] versus 8% to 11.6% in more recent radiographic studies [3, 4]. The sites of pulmonary involvement may include the lymph nodes, parenchyma, and tracheobronchial tree are most often associated with hilar or mediastinal lymphadenopathy [4, 6, 8, 23]. Additional reported radiographic features of endobronchial Hodgkin lymphoma include discrete nodules, fibronodular infiltrations, homogeneous confluent infiltrates, and consolidation [30].
Other manifestations of disease included: cavitation of right upper lobe (1 patient); supraclavicular and cervical nodes (9 patients [34.7%]; scalene nodes (2 patients), infraclavicular nodes (1 patient), and inguinal nodes (1 patient); leukocytosis (5 patients [19.2%], 2 with neutrophilia, 2 with lymphopenia); bone involvement (2 patients); abdominal involvement (3 patients); clubbing of the fingers (1 patient); pneumomediastinum (1 patient). At the Ohio State University’s James Cancer Center there was one patient with endobronchial presentation of Hodgkin lymphoma with a concomitant endobronchial necrotizing vasculitis.
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Pathology
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Of the 17 patients for which histologic subtype data was available, 8 (47.1%) had nodular sclerosis, 6 (35.3%) had mixed cellular, and 3 (17.6%) had lymphocyte-depleted Hodgkin lymphoma. Staging data was available for 14 patients, all but 1 patient were stage IV (9 stage IVB, 3 stage IVA, 1 stage IIEA, and 1 stage IIE). However, none of those patients, except the present report, were staged with Cotswolds modification of the Ann Arbor classification [31]. B symptoms (fever, drenching night sweats, or weight loss) 31 were present in 13 patients (50%).
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Treatment
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Eleven patients were treated with combined chemotherapy and radiation therapy (combined modality treatment), 8 patients were treated with chemotherapy alone, 4 patients were treated with radiation therapy alone, and 2 patients were treated surgically. The chemotherapy usually consisted of nitrogen mustard/mustine, mechlorethamine, vincristine, procarbazine, prednisone (MOPP), chlorambucil, vinblastine, procarbazine, prednisone (ChlVPP), or adriamycin, bleomycin, vinblastine, procarbazine (ABVP), while the radiation therapy was typically mantle irradiation. Eight of 10 patients (80%) who received combined modality therapy were alive and well on follow-up while 2 patients died (20%); 1 patient had no follow-up data. Five of 6 patients (83.3%) with known follow-up data who received chemotherapy alone were alive and well on follow-up whereas 1 patient died 6-months later; an additional 2 patients had no follow-up data. All 3 patients who received radiation therapy alone, and had known follow-up data, were alive and well on follow-up; the fate of the fourth is unknown to us. Both patients who were not treated with chemotherapy or radiotherapy died within a few days postoperatively, one after biopsy [6, 24] and the other after receiving a pneumonectomy [6]. Death occurred in 5 patients (19.2%) altogether, including one after a familial bone transplantation before ever having achieved a complete remission. Four of the deceased five had B symptoms (80%).
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Incidence of endobronchial disease in Hodgkin lymphoma
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Based on autopsy data, endobronchial Hodgkin lymphoma can be as high as 14% [9], but most frequently develops during the course of the disease [14]. Large bronchi are less commonly involved relative to the more peripheral bronchi and bronchioles [10]. Harper and colleagues summarize from p. 150 [23] the autopsy data on endobronchial Hodgkin: "Forty percent of the Hodgkin patients in a postmortem series had mediastinal involvement, 14 to 38% local lung infiltration, 5 to 16% isolated nodules, and 23 to 80% discrete hilar nodes alone."
In contrast to autopsy data [5, 9–12] antemortem endobronchial involvement in Hodgkin lymphoma is rare [5, 13–16] usually manifesting in patients with established disease. A relatively recent series reported a 1.9% frequency among patients with newly diagnosed Hodgkin lymphoma [14]. However, as the authors note, bronchoscopy was performed only in those patients who presented with respiratory symptoms or bulky mediastinum. The presence of respiratory symptoms in patients with intrathoracic disease is rarer in adults than in children [32], because the lymph nodes in adults are soft relative to the cartilaginous skeleton of the trachea and proximal bronchi [33]. The incidence of endobronchial presentation of Hodgkin lymphoma could be more frequent in adults than the current data suggests. In a series of patients who underwent systematic fiberoptic bronchoscopy during the initial staging, Gallagher and colleagues [34] found 3/12 previously untreated Hodgkin patients to have histologically proven endobronchial lymphoma. Furthermore, bronchial wall infiltration with erosion of the bronchial mucosa and destruction of the cartilaginous plates was noted in 8 of 15 patients with primary pulmonary Hodgkin lymphoma [35].
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Differential diagnosis of endobronchial Hodgkin lymphoma
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The endobronchial presence of Hodgkin lymphoma is rarely identified in adults because bronchoscopic biopsy often fails to obtain adequate tissue, even when there is gross evidence of endobronchial tumor [13, 20, 24, 29]. The failure to obtain adequate tissue for diagnosis can be a diagnostic and treatment problem. If a diagnostic specimen cannot be obtained from bronchoscopy or from lymph nodes, then a more invasive procedure, such as thoracotomy or a video associated thorascopic biopsy, may be warranted in order to establish a proper diagnosis, especially considering the more favorable prognosis of endobronchial Hodgkin lymphoma relative to small cell carcinoma [16]. Several reports of endobronchial Hodgkin lymphoma described an erroneous initial diagnosis or impression of small cell carcinoma [11, 13, 16, 22–25]. In a few other reports, bronchial adenoma and asthma were mistaken early impressions due to the resultant wheezing and dyspnea from partial occlusion of a main bronchus [13, 23]. These incorrect initial diagnoses underscore the importance of obtaining adequate tissue for histologic examination.
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Pathogenesis of endobronchial Hodgkin lymphoma
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The pathogenesis of endobronchial Hodgkin lymphoma is unclear. Rosenberg and Kaplan’s theory [36] of contiguous nodal spread indicates that patients with intrathoracic disease alone have a small risk of systemic involvement due to the limited extent of the disease. The initial sites of extrathoracic extension would be to the clavicular or cervical nodes, followed later by spread to subdiaphragmatic sites [36]. Presumably, endobronchial lesions may arise in mucosa-associated lymphoid tissue (MALT) or from other possible sources including adjacent nodal spread or hematogenous spread from an undiagnosed primary site [23]. In a study by Gallagher and coworkers [34], endoluminal Hodgkin lymphoma most often presented as direct invasion of the main stem bronchi by adjacent nodal masses, whereas patients with non-Hodgkin’s lymphoma had multiple submucosal masses at the sites of bronchial-associated lymphoid tissue, located at each bronchial division.
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Staging and prognosis
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Whether endobronchial involvement denoted stage IV disease or contiguous extranodal spread used to be an unsettled question [15]. With the current Cotswolds staging, involvement of extra lymphatic tissue on one side of the diaphragm by limited direct extension from an adjacent nodal site is classified as extranodal extension (E) with the implicit expectation of a prognosis equivalent to that for treatment of nodal disease of the same anatomic extent [31]. Therefore, endobronchial infiltration by contiguous nodal disease is not, in and of itself, enough to denote stage IV disease. An article on massive mediastinal Hodgkin’s disease concluded that the presence of a large mediastinal mass is a more dominant determinant of prognosis than Ann Arbor staging or other clinical prognostic factors, including age, sex, B symptoms, number of extranodal sites, lactate dehydrogenase levels, erythrocyte sedimentation rate, or platelet count [37]. Thus, endobronchial involvement alone, without massive mediastinal involvement, might not indicate a poor prognosis.
Careful staging and optimal treatment can lead to cure for approximately 75% of patients with Hodgkin lymphoma [38]. Conventional therapy for any Hodgkin patient who presents with poor prognostic factors, especially bulky mediastinal disease, is the use of chemotherapy with or without radiation therapy [39, 40]. Though the sample size of the reported cases of endobronchial presentation of Hodgkin lymphoma is very small, 8 of 10 survived combined modality treatment, 5 of 6 survived chemotherapy alone, and 3 of 3 survived radiation therapy alone and remained in complete remission after a mean follow-up duration of 40.4 months. The overall survival for the reported patients then is 16 of 21 (76.2%), or 16 of 19 (84.2%) for those receiving chemotherapy with or without radiation therapy with known follow-up data. The range of survival percentages roughly corresponds with what has been published previously [37, 40]. More recent clinical trials may reveal more effective treatment modalities [41] and may improve survival rate among Hodgkin patients in general, but understandably have yet to be reported in the rare patient population with endobronchial presentation of Hodgkin lymphoma. In a recent case report, the patient underwent successful chemotherapy treatment, without radiation, with adriamycin, bleomycin, vincristine, and dacarbazine, and after 4 months demonstrated no lung or mediastinal abnormality by CT [21]. We similarly experienced a patient who underwent successful treatment with adriamycin, bleomycin, vincristine, and dacarbazine, without the use of radiation, and remained disease-free at 4 months.
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Surgical treatment of endobronchial Hodgkin lymphoma
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Although lymphoma is not considered a surgical disease, there is a role for surgical intervention in the management of patients with endobronchial lymphoma, primarily in the context of those patients presenting with critical airway obstruction [26, 42]. Such intervention includes laser therapy with neodymium:yttrium-aluminum garnet laser (Nd:YAG), photodynamic laser therapy (PDT), rigid bronchoscopy, and mechanical stent placement.
Thermal laser vaporization treatment using the Nd:YAG laser has been reported as a successful method of relieving airway obstruction secondary to malignancy [43, 44]. Pierce and colleagues [43] report the results of 28 patients treated with Nd:YAG laser, more than half with small cell carcinoma, but all with tumor localization and respiratory symptoms similar to endobronchial Hodgkin lymphoma. Fourteen of 17 patients experienced moderate to marked symptomatic relief of dyspnea. Hemoptysis markedly improved in 2 of 3 patients and tests of respiratory function improved in most. Reexpansion of an atelectatic lobe occurred in 7 of 8 patients, with 6 of those receiving the laser therapy prior to tumor-specific therapy. There was associated mortality when the obstruction was bilateral, and morbidity included laryngeal edema requiring intubation, atrial fibrillation, bronchospasm, and acute pulmonary edema. Overall, the results support the use of laser therapy to relieve symptoms of respiratory obstruction in proximal endobronchial tumors.
Taber and coworkers [44] also report the successful use of the Nd:YAG laser in 83 patients with malignant endobronchial obstruction with overall results similar to Pierce. Complication rates were similar between the two authors, with Taber and colleagues adding massive hemoptysis as a cause of two of five deaths within 13 days of laser treatment, along with the other three deaths due to respiratory failure. The study also made a useful comparison of results between the Nd:YAG laser and PDT. The two modalities were similar in terms of successful short-term symptom palliation, morbidity, and mortality. However, the authors preferred PDT because of its technical ease, potential for being safer, and its ability to be performed without the use of general anesthesia, which one author has suggested avoids life-threatening airway obstruction in patients because of the high frequency of exacerbation of obstruction in such patients [31].
Photodynamic therapy has been proven to be an effective modality for treating endoluminal bronchogenic carcinoma [45–48], esophageal carcinoma [49, 50], skin, head, neck, and oral lesions [49], age-related macular degeneration [50], and certain metastatic carcinomas including renal cell carcinoma and breast carcinoma. Photodynamic therapy involves the selective retention of a porphyrin by tumor cells. When activated by laser light at the proper wavelength (630 nm), this agent generates toxic oxygen-free radicals, which in turn cause tumor necrosis [45, 51]. In our experience, PDT has been effective in over 70% of patients who present with symptoms related to endobronchial obstruction, similar to previous studies. We have recently implemented PDT therapy to treat a patient with endobronchial Hodgkin lymphoma with impending airway obstruction. Amelioration of the obstructive symptoms was achieved after three treatments over a 96-hour period, following which the patient underwent tumor-specific chemotherapy and has experienced 4-month remission thus far.
Endobronchial stenting is another option recently implemented in the palliative management of airway stenosis [52–54], including those secondary to lymphoma [55, 56]. Stenting is a palliative procedure for rapidly progressing dyspnea and is followed by tumor-specific therapy. A recent article explored the role for temporary airway stenting in 5 consecutive patients with dyspnea secondary to malignant lymphoma (non-Hodgkin’s lymphoma, n = 3; Hodgkin’s lymphoma, n = 2). Nine stents were implanted into the trachea or main bronchi prior to the induction of tumor-specific therapy (chemotherapy, n = 4; percutaneous radiotherapy, n = 1). Following stent implantation, each of the 5 patients experienced clinical improvement of respiratory symptoms. Stent removal following tumor-specific therapy was successfully and easily performed in 4 patients, who achieved reduction of stenosis after a mean interval of 26 days (14 to 52 days). One patient died during chemotherapy 6 days after stenting. These results compare with published results of stenting for airway obstruction from a variety of diseases [52–54]. Advantages of stenting include ease of insertion under radiologic control, self-expansion, and the lack of major complications [53, 54]. However, there is a risk of stent migration as the tumor responds to specific therapy. This often necessitates a second, more challenging procedure, to remove the stent.
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Conclusions
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Because of the dramatic implications in treatment and survival of the patient, endobronchial presentation of Hodgkin lymphoma, despite its uncommon occurrence, should be considered in the differential of small cell carcinoma and necrotizing vasculitides with pulmonary involvement, especially in a relatively young patient with cough, hemoptysis, atelectasis, hilar, or mediastinal lymphadenopathy. The importance of adequate tissue sampling and the appropriate microscopic and laboratory studies is obvious and cannot be overstated. Prior to tumor-specific therapy, palliative treatment to relieve respiratory symptoms of critical airway obstruction has generally been successful in patients with malignant airway obstruction, a few of which include endobronchial Hodgkin lymphoma.
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Abstract
Introduction
