|Year : 2013 | Volume
| Issue : 3 | Page : 416-421
Endobronchial ultrasound-guided transbronchial needle aspiration for the diagnosis of intrathoracic lymphadenopathy in patients with extrathoracic malignancy: A study in a tuberculosis-endemic country
M Akif Özgül1, Erdogan Çetinkaya1, Nuri Tutar2, Güler Özgül1, Hilal Onaran1, Semra Bilaçeroglu3
1 Department of Pulmonary Medicine, Yedikule Chest Disease and Surgery Training and Research Hospital, Istanbul, Turkey
2 Department of Pulmonary Medicine, Erciyes University School of Medicine, Kayseri, Turkey
3 Department of Pulmonary Medicine, Izmir Training and Research Hospital for Thoracic Medicine and Surgery, Izmir, Turkey
|Date of Web Publication||8-Oct-2013|
Department of Pulmonary Medicine, Erciyes University School of Medicine, Kayseri, Postal code: 38038
Source of Support: None, Conflict of Interest: None
Background: Mediastinal lymphadenopathy in patients with malignancy is a common clinical problem in tuberculosis-endemic countries. The recently developed endobronchial ultrasound-guided transbronchial needle aspiration (EBUS-TBNA) procedure enables direct and real-time aspiration of mediastinal and hilar lymph nodes. The aim of the study was to determine the efficacy of EBUS-TBNA results in the evaluation of mediastinal lymph nodes in patients with extrathoracic malignancy.
Materials and Methods: Retrospective analysis was performed in 40 patients with proven (n = 38) or suspected metastasis of unknown origin (n = 2) who underwent EBUS-TBNA between July 2007 and August 2011.
Results: All 40 patients successfully underwent EBUS-TBNA and no complications were observed. EBUS-TBNA diagnosed metastasis from extrathoracic malignancy in 16 (40%) patients, new lung cancer in 2 (5%), reactive lymph node in 9 (22.5%), sarcoidosis in 5 (12.5%), anthracosis in 5 (12.5%) and tuberculosis in 3 (7.5%). The diagnostic sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV) and accuracy of EBUS-TBNA based on the number of patients were 90.0%, 100%, 100%, 90.9% and 95.0%, respectively. In 33 patients with available data of fluorodeoxyglucose positron emission tomography (PET)/computed tomography (CT) scans, the diagnostic sensitivity, specificity, PPV, NPV and accuracy of PET/CT scan based on the number of patients were 94.7%, 35.7%, 66.6%, 83.3%, and 69.6%, respectively. The association between larger lymph node size on EBUS and malignancy of lymph node sample on pathological examination was statistically significant (P = 0.018).
Conclusions: EBUS-TBNA is a sensitive, specific, minimally invasive and a safe procedure for the diagnosis of mediastinal and hilar metastasis from extrapulmonary malignancy in a tuberculosis-endemic country.
Keywords: Endobronchial ultarsonography, lymphadenopathy, metastasis
|How to cite this article:|
Özgül M A, Çetinkaya E, Tutar N, Özgül G, Onaran H, Bilaçeroglu S. Endobronchial ultrasound-guided transbronchial needle aspiration for the diagnosis of intrathoracic lymphadenopathy in patients with extrathoracic malignancy: A study in a tuberculosis-endemic country. J Can Res Ther 2013;9:416-21
|How to cite this URL:|
Özgül M A, Çetinkaya E, Tutar N, Özgül G, Onaran H, Bilaçeroglu S. Endobronchial ultrasound-guided transbronchial needle aspiration for the diagnosis of intrathoracic lymphadenopathy in patients with extrathoracic malignancy: A study in a tuberculosis-endemic country. J Can Res Ther [serial online] 2013 [cited 2019 Dec 16];9:416-21. Available from: http://www.cancerjournal.net/text.asp?2013/9/3/416/119323
| > Introduction|| |
Mediastinal lymphadenopathy in patients with malignancy is a common clinical problem in tuberculosis-endemic countries. Endobronchial ultrasound-guided transbronchial needle aspiration (EBUS-TBNA) procedure enables direct and real-time aspiration of mediastinal and hilar lymph nodes and is a less invasive alternative to mediastinoscopy.  In a review, for nodal staging of non-small cell lung cancer (NSCLC), EBUS-TBNA had a pooled sensitivity of 93%. 
In patients with proven or suspicious extrapulmonary malignancy who had mediastinal and hilar lymphadenopathy, the differentiation between metastasis of the primary site and new development of secondary malignancy, such as lung cancer, is important for the prognosis and future treatment plan.  Also, granulomatous diseases and pneumoconiosis can be the causes of mediastinal or hilar lymphadenopathy.  F-18 fluorodeoxyglucose positron emission tomography/computed tomography (fluorodeoxyglucose positron emission tomography (FDG PET)/(computed tomography) CT) provides functional information about tumor metabolism and has been used as a non-invasive alternative to contrast-enhanced CT for nodal staging in NSCLC.  However, abnormal FDG uptake is believed to frequently occur in granulomatous and inflammatory diseases.  Therefore, histopathologic confirmation is required for the treatment plan. Mediastinoscopy remains the gold standard for evaluation of the mediastinum, but it requires general anesthesia and has a morbidity rate of 1% and a mortality rate of 0.05%; furthermore, it cannot evaluate the hilar lymph nodes.  The role of EBUS-TBNA in the diagnosis of mediastinal or hilar metastasis from extrapulmonary malignancy has been established in several recent studies. ,,, In the present study, we described the diagnostic utility of EBUS-TBNA for the clarification of intrathoracic lymphadenopathy in patients with extrathoracic malignancy in a tuberculosis-endemic country. Furthermore, we evaluated the diagnostic utility of FDG PET/CT results in these patients.
| > Materials and Methods|| |
Between July 2007 and August 2011, 858 patients underwent endobronchial ultrasound studies for a variety of clinical indications. We retrospectively analyzed the data from 44 patients who underwent EBUS-TBNA because of suspected mediastinal or hilar metastasis of a previously known and treated or concurrent extrathoracic malignancy, or a suspected metastatic cancer of unknown origin. Four patients were excluded due to insufficient data hence only 40 patients were eventually included in the study. The patients underwent EBUS-TBNA because of a suspected mediastinal metastasis according to CT (short axis of lymph node >1 cm) or FDG uptake on PET/CT.
Endobronchial ultrasound-guided transbronchial needle aspiration procedure
Endobronchial ultrasonography was conducted using a fiberoptic ultrasound bronchoscope (Convex Probe EBUS; BF-UC 160F-OL8; Olympus Medical Systems, Tokyo, Japan). The location, shape, and structure of the lesions were examined with ultrasound. The location of the station was named and numbered using the lymph node map proposed by Mountain.  After the bronchoscope was guided to the target area, during real-time imaging a 22-gauge aspirating needle with a syringe connected proximally (Model NA-201SX-4022, Olympus, manufactured for this purpose) was pushed out from the distal tip of the bronchoscope and samples consisting of cells or tissue fragments were obtained as previously described.  The aspirate was smeared onto glass slides, air dried or fixed immediately with 95% alcohol, and stained with hematoxylin and eosin (H and E). Histological cores were fixed with 10% neutral buffered formalin and stained with H and E. Immunohistochemical staining was also performed when considered necessary. A rapid onsite cytopathological examination was not performed. Cyto-pathological specimens were categorized as (i) malignant (adequate sample with presence of malignant cells) or (ii) benign (sample consisting of mature lymphocytes, granulomas with necrosis and neutrophils or without necrosis). All procedures were conducted by a single bronchoscopist. Because a pathologist was not present for rapid on-site evaluation, it was not possible to evaluate whether the material contained enough cells. The bronchoscopist evaluated whether the procedure was sufficient for each sampled area. Patients diagnosed with benign or reactive lymphadenopathy by EBUS-TBNA subsequently underwent mediastinoscopy or were followed up clinically and radiologically for at least 6 months.
Integrated endobronchial ultrasound-guided transbronchial needle aspiration imaging
After fasting for at least 6 h before PET/CT examination, the patients received an intravenous injection of 370 MBq of 18F-FDG and then rested for 45 min before undergoing imaging. Image acquisition was performed using an integrated PET/CT device (Discovery LS, GE Healthcare, Milwaukee, WI). Lymph nodes were classified as malignancy-positive on PET/CT if FDG uptake was ≥2.5 SUVmax. 
Descriptive statistics are presented in frequency, percentage, median, minimum and maximum values. The diagnostic sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), and accuracy of EBUS-TBNA and the PET/CT scan were calculated by standard definitions. The Mann-Whitney U test was used for independent measurements of the differences between the groups as metastatic lymphadenopathy positive and negative. The Logistic Regression Analysis was used to evaluate the independent risk factors for metastatic lymphadenopathy. The results of the logistic regression analysis were interpreted by odds ratios and 95% confidence intervals (95% CI). A P value < 0.05 was considered to be significant. The data were entered into a database and analyzed with the SPSS statistical software package (SPSS 18.0 Chicago, Illinois, USA).
| > Results|| |
Patient characteristics and indications for endobronchial ultrasound-guided transbronchial needle aspiration
All 40 patients successfully underwent EBUS-TBNA and no complications were observed. The patient characteristics are summarized in [Table 1]. The median age of the patients was 54 years (range 31-79 years). There were 38 (95%) patients with a definite diagnosis of extrathoracic malignancy and two (5%) patients with a suspected mediastinal lymph node metastasis of unknown origin. The most common extrathoracic malignancies observed were breast, urogenital and head and neck carcinomas. Indications for EBUS-TBNA were to determine mediastinal metastasis in patients with existing extrapulmonary malignancy (n = 29, 72.5%), to evaluate disease relapse in patients with a previous history of extrapulmonary malignancy (n = 9, 22.5%), and to obtain a pathological diagnosis in patients with suspected extrapulmonary malignancy (n = 2, 5%).
Details related to mediastinal and hilar lymph nodes
The characteristics of hilar and mediastinal lymph nodes assessed by EBUS-TBNA are shown in [Table 2]. Sixty-nine nodes were sampled in 40 patients. The median size of the lymph nodes seen at EBUS-TBNA was 13 mm (range: 5-40 mm) and a median of two passes (range: 1-4) was performed for each nodal site. The subcarinal lymph node station was the most aspirated site in the present study.
|Table 2: Characteristics of 69 lesions sampled by endobronchial ultrasound-guided transbronchial needle aspiration|
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Diagnostic results by endobronchial ultrasound-guided transbronchial needle aspiration and mediastinoscopy
In 16 (40%) patients, EBUS-TBNA confirmed metastasis of extrathoracic malignancy. Two (5%) patients were diagnosed as new lung cancer by EBUS-TBNA. Of the 22 (55%) cases, in which EBUS-TBNA provided a benign or reactive diagnosis, mediastinoscopy was performed in four (18.1%) and a median of 10 (6-12) months of clinical and radiological follow-up was carried out in the remaining 18. Granuloma (n = 1), metastasis of renal cell carcinoma (n = 1), NSCLC (n = 1) and reactive lymph node (n = 1) were found in four patients by mediastinoscopy. The EBUS-TBNA results of these four patients were granuloma (n = 1) and reactive lymph node (n = 3), respectively.
Final diagnostic results
The final diagnosis of intrathoracic lesions showed malignancy in 20 (50%) of the 40 patients. Three (7.5%) of them were newly diagnosed with NSCLC and 17 (42.5%) of them had metastasis from an extrathoracic malignancy. Sarcoidosis and tuberculosis were found in five (12.5%) and three (7.5%) patients, respectively. The results of the EBUS-TBNA procedure and the final diagnoses are shown in [Figure 1].
Diagnostic performances of endobronchial ultrasound-guided transbronchial needle aspiration and positron emission tomography/computed tomography
The diagnostic performances of EBUS-TBNA and FDG PET/CT for the diagnosis of mediastinal and hilar metastasis from extrapulmonary malignancies are shown in [Table 3]. The diagnostic sensitivity, NPV and accuracy of EBUS-TBNA as per number of patients were 90.0%, 90.9% and 95.0%, respectively. Data about FDG PET/CT scans were available in 33 patients. The diagnostic sensitivity, specificity, PPV, NPV and accuracy of FDG PET/CT scan as per number of patients were 94.7%, 35.7%, 66.6%, 83.3%, and 69.6%, respectively. Sixty-nine lymph nodes were sampled by EBUS-TBNA.
|Table 3: Diagnostic performances of endobronchial ultrasound-guided transbronchial needle aspiration and F-18 fluorodeoxyglucose positron emission tomography/ computed tomography|
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Relation of malignancy with sampled lymph node size and number
The lymph node size and number of lymph nodes sampled were analyzed in metastatic lymphadenopathy positive and negative patients. There was a statistically significant association between larger lymph node size and presence of malignant lymphadenopathy (P = 0.018). The association between the number of lymph nodes sampled and presence of malignant lymphadenopathy was not statistically significant (P > 0.05). In the logistic regression analyses, larger lymph node size remained significantly associated with malignant lymphadenopathy (P = 0.023, OR = 1.14, %95 CI, 1.01-1.28). However, there was no statistically significant association between the number of lymph nodes sampled and malignant lymphadenopathy (P > 0.05).
| > Discussion|| |
The present retrospective study showed that EBUS-TBNA is a sensitive, accurate and safe modality for the evaluation of nodal metastases from extrapulmonary malignancy. In addition, we showed that FDG PET-CT had a low PPV (66.6%) in patients with metastasis from an extrathoracic malignancy.
The investigation of mediastinal lymphadenopathy etiology is a subject that chest physicians are commonly faced with. The detection, in particular, of enlarged mediastinal lymphadenopathy in patients with extrathoracic malignancy is important to plan further treatment. Mediastinoscopy is considered the gold standard procedure in this clinical scenario. However, it requires general anesthesia, and there is the possibility of significant complications. , Additionally, mediastinoscopy can only sample nodal stations of 1-4, 7; accessing hilar nodal stations can be difficult and the procedure cannot be repeatedly used on the same patient. ,
On the other hand, EBUS-TBNA is an established modality for sampling mediastinal lymph nodes and is a minimally invasive technique. Earlier studies of its application in mediastinal staging or restaging of NSCLC showed high diagnostic rates for EBUS-TBNA, with sensitivity and PPVs of more than 90% and specificity of 100%. ,, Recently, EBUS-TBNA was performed to evaluate intrathoracic lymphadenopathy in patients with extrathoracic malignancy. A large study of 161 suspected metastases from extrathoracic malignancy patients undergoing EBUS-TBNA demonstrated a sensitivity rate of 87%.  Other studies also showed a sensitivity rate of 85-96.3%. ,, In the present study, similar to other reports, the sensitivity of EBUS-TBNA in suspected metastases from extrathoracic malignancy patients was 90%. Additionally, NPV was 90.9% in this study, which was superior to other studies that reported rates of between 73-85%. ,, Two cases were diagnosed as malignancy after mediastinoscopy in spite of EBUS-TBNA results being negative. Therefore, the negative results by EBUS-TBNA should be verified by surgical methods or by other means in the follow-up.
EUS-FNA is another procedure to evaluate the mediastinal lymphadenopathy. The NPV and sensitivity of this method are 72% and 69-86%, respectively in patients with extrathoracic malignancy. , Our results and those of most other studies using EBUS-TBNA showed higher sensitivity and NPV when compared with EUS-FNA. ,, However, EUS is more suitable for the assessment of lymph node stations 8 and 9.  Because both procedures give good results in different nodal stations, EBUS-TBNA and EUS-FNA are recommended as complementary procedures in diagnosing mediastinal and hilar lymphadenopathy. ,
Of note in the present study are the low specificity (35.7%) and PPV (66.6%) of FDG PET/CT, which need to be discussed. Song et al. investigated the diagnostic value of EBUS-TBNA and PET/CT in patients with extrapulmonary malignancy. They reported PET/CT specificity and PPV were both 89%.  But, it should be noted that FDG is not a cancer-specific diagnostic method and thus, false positive findings in benign diseases have been reported. ,, Infectious diseases (mycobacterial, fungal, bacterial infection), sarcoidosis, radiation pneumonitis and post-operative surgical conditions have shown intense uptake on PET scan.  Zheng et al. reported that only in 1 of 25 patients with histopathologically diagnosed pulmonary tuberculoma, FDG uptake was negative on PET/CT scan.  Sarcoidosis is another disease that shows intense FDG uptake and it has been suggested that intensity of FDG uptake may reflect disease activity.  In addition, pneumoconiosis, such as anthracosis, shows hypermetabolic activity in FDG PET/CT. ,, In developing countries like ours, anthracosis may be another cause of mediastinal lymphadenopathy. , In the present study, 4 of 5 sarcoidosis, 2 of 5 anthracosis, 2 of 3 tuberculosis and 1 of 7 reactive lymph nodes showed false-positive FDG uptake in PET/CT that led to a low specificity and a PPV.
Another important point is the association between granulomatous inflammation and cancer. Many hypotheses exist such as immunological dysfunction related to cancer and sarcoidosis, a side effect of cancer therapy and "antigenic shedding" from the tumor leading to granuloma formation. , In a recent report, EBUS-TBNA identified non-caseating granuloma in 15/161 (9.3%) patients with intrathoracic lymphadenopathy and extrathoracic malignancy.  Also malignancies and the instituted therapies for their management seem to create the proper environment for either the reactivation of a latent TB infection or, more rarely, for the acquisition of a primary mycobacterial infection.  Immunosuppression, especially depression of the T-cell defense mechanisms, is associated with mycobacterial infections. , Song et al. identified tuberculosis in 1/57 (1.7%) in patients with extrathoracic malignancy by EBUS-TBNA.  In the present study, sarcoidosis and tuberculosis were determined respectively in 12.5% (5/40) and 7.5% (3/40) of patients with extrathoracic malignancy. These results show that sarcoidosis and tuberculosis have a considerable role in the etiology of intrathoracic lymphadenopathy in patients with extrathoracic malignancy.
Memoli et al. reported that the increasing size of lymph nodes on EBUS was associated with increasing malignancy risk in NSCLC patients.  Navani et al. investigated the association between presence of metastatic lymphadenopathy in patients with extrathoracic malignancy and lymph node size, number of passes per node, and number of lymph nodes sampled by EBUS.  They reported an association only between increasing lymph node size and presence of metastatic lymphadenopathy. In harmony with the other studies, we also found a statistically significant relationship between larger lymph node size and presence of metastatic lymphadenopathy in the present study.
The present study had several limitations. It was retrospective in design and involved a relatively small number of patients. Additionally, some of the patients did not undergo FDG PET/CT scans. A prospective study with a large number of patients and with well-defined inclusion and exclusion criteria could overcome these limitations.
In conclusion, benign diseases such as tuberculosis, sarcoidosis and anthracosis should also be kept in mind for the etiology of intratoracic lymphadenopathy in patients with extrathoracic malignancy. Furthermore, it should be noted that FDG PET/CT can show positive results in malignant and also benign diseases. Thus, histopathologic confirmation of mediastinal and hilar lymphadenopathy is mandatory. In this regard, EBUS-TBNA is a sensitive, specific, minimally invasive and safe procedure for the diagnosis of mediastinal and hilar metastasis from extrapulmonary malignancy.
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[Table 1], [Table 2], [Table 3]