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Original Research: INTERVENTIONAL PULMONOLOGY |

Release of Metal Particles From Needles Used for Transbronchial Needle Aspiration FREE TO VIEW

Valérie Gounant, MD; Vincent Ninane, MD, PhD; Xavier Janson, Tech; Magali Colombat, MD; Marie Wislez, MD, PhD; Dominique Grunenwald, MD, PhD; Jean François Bernaudin, MD, PhD; Jacques Cadranel, MD, PhD; Jocelyne Fleury-Feith, MD, PhD
Author and Funding Information

From the Service de Pneumologie et Réanimation (Drs Gounant, Wislez, and Cadranel), the Service de Chirurgie Thoracique (Drs Gounant and Grunenwald), the Service d’Anatomie Pathologique (Dr Colombat), and the Service d’Histologie et Biologie Tumorale (Drs Bernaudin and Fleury-Feith), Hôpital Tenon, AP-HP, Faculté de Médecine, Université Pierre et Marie Curie, Paris, France; the Service de Pneumologie (Dr Ninane), Hôpital Saint Pierre, Brussels, Belgium; and the Laboratoire d’Etude des Particules Inhalées (Mr Janson and Dr Fleury-Feith), Paris, France.

Correspondence to: Valérie Gounant, MD, Service de Chirurgie Thoracique, Hôpital Tenon, 4 Rue de la Chine, 75020 Paris, France; e-mail: valerie.gounant@tnn.aphp.fr


Reproduction of this article is prohibited without written permission from the American College of Chest Physicians (http://www.chestpubs.org/site/misc/reprints.xhtml).


© 2011 American College of Chest Physicians


Chest. 2011;139(1):138-143. doi:10.1378/chest.10-0371
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Background:  Although mediastinoscopy is still the gold standard for diagnosis of mediastinal lymphadenopathy, minimally invasive procedures have been developed: transbronchial needle aspiration (TBNA) using a flexible bronchoscope (conventional TBNA) or linear echoendoscope (endobronchial ultrasound [EBUS]) allowing real-time guided lymph node aspiration. The observation of contamination of samples by foreign particles led us to determine the frequency and the nature of this material and to identify its origin.

Methods:  From June 2007 to November 2008, 141 consecutive patients underwent conventional TBNA (n = 84) or EBUS-guided TBNA (EBUS-TBNA) (n = 57). All cytologic samples were reviewed in blinded fashion, and contamination was assessed semiquantitatively. Mineral analysis using a transmission electron microscope equipped with an energy dispersive x-ray spectrometer was performed on the solution obtained after rinsing unused needles and on four samples of calf thymuses punctured with EBUS needles.

Results:  Foreign material, different from anthracosis, was identified in samples obtained with five different batches of needles, only from EBUS-TBNA (P < .0001). The contamination score was correlated to the number of passes (P = .035). Mineral analyses of the rinsing solutions from conventional TBNA needles were negative, whereas metal alloys of iron, titanium, nickel, and chromium were released with EBUS needles. The same contamination was identified in three of the four punctured calf thymuses.

Conclusions:  Dedicated EBUS-TBNA needles are able to release metal particles, probably by friction between the stylet and the needle, with a potential risk to inject particles into nodes. The long-term consequences are unknown, but the need for safety measures should be evaluated.

Figures in this Article

Mediastinoscopy is currently considered to be the gold standard for diagnosis of mediastinal lymphadenopathy for lung cancer staging and for the diagnosis of granulomatous diseases or lymphoma. High diagnostic yields have been reported in lung cancer staging with an average sensitivity of 80%.1 However, mediastinoscopy is an invasive procedure requiring general anesthesia and is associated with a morbidity of 2% and even 0.08% mortality.1 Mediastinoscopy is also often unable to access posterior subcarinal nodes.

Alternative minimally invasive procedures have been developed. Conventional transbronchial needle aspiration (TBNA) using a flexible bronchoscope has a diagnostic yield that varies considerably between series, ranging from 36% to 84%, mainly because lymph node aspiration is not real-time guided.2 Linear echoendoscopes (endobronchial ultrasound [EBUS]) can be used to aspirate lymph nodes under real-time visual control. This echoendoscope can be used to aspirate upper and lower paratracheal and subcarinal mediastinal lymph nodes and has a very high sensitivity exceeding 90%3 and a very low morbidity with no reported mortality. The diagnosis is usually based on cytologic material, whereas tissue cores are obtained less frequently.4,5 The clinical implications of this technique include a marked reduction of additional more invasive procedures.

Since 2007, real-time EBUS-guided TBNA (EBUS-TBNA) has been introduced as an alternative procedure to conventional TBNA in our center. Cytologists have been intrigued by the finding of foreign material deposits on some slides. This study was therefore designed to determine the frequency and the nature of this foreign material and to identify its origin.

Tenon Cohort

From June 2007 to November 2008, 141 consecutive patients (107 men and 34 women, aged 17–88 years, mean 60 years) underwent conventional TBNA (n = 84) or EBUS- TBNA (n = 57) for assessment of enlarged mediastinal lymph nodes. All patients provided informed consent. The samples were collected according to French legislation, and the ethical rules of our institution at the time the experiments were carried out.

Sampling Procedures

Specimens were obtained with a 19- or 21-gauge needle for conventional TBNA (Conmed; Billerica, Massachusetts; Boston Scientific; Boston, Massachusetts; Olympus Ltd; Tokyo, Japan) and a 22-gauge dedicated needle equipped with a stylet for EBUS-TBNA (ViziShot NA-201SX; Olympus Ltd). The same procedure was used for both techniques: briefly, the needle, in the operating channel of the scope, was introduced into the target through the airway wall using the “jabbing” method,6 and for EBUS-TBNA the stylet was subsequently removed for aspiration. One to three smears were performed for each aspirate. Successive passes were made using the same needle for each site, and for EBUS-TBNA the stylet was always reintroduced into the needle between passes. One to nine (mean four) needle passes were performed for each patient. After the last aspirate, the needle was washed with culture medium.

Cytologic Analysis

Smears were air-dried and stained by the May-Grünwald-Giemsa (MGG) method. Two cytospins were performed from the cell suspension, and then the cell suspension was stored at −80°C. Cytospins from the 141 needle rinse samples were submitted to blind review and the presence of particles was noted. All the smears of 35 randomly selected specimens from samples containing foreign deposits were reviewed; contamination was assessed on each slide by a score from 0 to 4 (0, none; 1, few particles on the smear; 2, some foci of particles scattered on the slide; 3, large foci of particles; and 4, slide entirely covered by foreign deposits), and a mean contamination score was calculated for each pass.

External Samples

All smears obtained by EBUS-TBNA from 12 patients from the Chest Department of Saint Pierre Hospital (Brussels, Belgium) were reviewed. These 12 cases were selected at random, and EBUS-TBNA was performed for the same indications as those reported above over a brief period of time (July and August 2008). Examinations were performed according to a standardized procedure described by this center similar to that used by the Tenon center.

Mineral Analysis

Mineral analysis was performed on the liquid obtained after rinsing the two types of new unused needles with sterile distilled water. The EBUS-dedicated needle was rinsed twice: once immediately after stylet removal and again after four successive introductions and withdrawals of the stylet as regularly performed between each EBUS-TBNA pass.

Mineralogic analysis was performed using an analytical transmission electron microscope (Jeol JEM 1200; JEOL Ltd; Tokyo, Japan) equipped with an energy dispersive x-ray spectrometer (EDS 6251; Oxford Instruments; Bucks, England) as previously described.7 For each sample, particles were analyzed at ×200 to ×600 magnification for morphology and elementary chemical composition in randomly selected fields. Images were captured with an Erlangshen camera (Gatan; Grandchamp, France) using digital micrograph software (Gatan), and chemical composition was analyzed by Linkisis software (Oxford Instruments). This experiment was realized three times.

Experimental Study

Two calf thymuses were used as non-particle-contaminated lymphoid tissue. They were cut with a plastic knife into samples of about 1 cm3. Four random samples were selected for needle aspiration with EBUS-TBNA-dedicated needles. Puncture was performed with a new needle by sample. A total of four passes were made by sample as performed in the patients. At the end of experiment, each needle was rinsed with distilled water and the rinse product was analyzed for mineral particle detection as described above. The four needle aspiration punctured samples and four control samples were submitted to mineral analysis. Briefly, samples were treated with sodium hypochlorite for 2 h at room temperature to digest all organic material and then concentrated by filtration and prepared for mineral analysis as described above for rinsed needles.

Statistics

Statistical analyses were performed using Statview software (Abacus Inc; Lexington, Kentucky): χ2 test to test for a relationship between the presence of foreign material and the type of needle used, a Kruskal-Wallis nonparametric test to compare the contamination score between various batches of needles, and a nonparametric Friedman test to compare the contamination score between the various needle passes. The level of significance was P < .05.

Extracellular Particle Deposits Were Observed on TBNA Samples

A variable cell density was observed on the aspirates. Evidence of lymph node sampling was assessed by the presence of characteristic lymphoid cells in 85% of patients. Some aspirates also contained obvious extracellular black particles consisting of scattered or aggregated small particles measuring 0.64 to 5.33 μm long (mean length 1.91 ± 0.91) that were highly suggestive of metal particles (Fig 1). These particles were always extracellular (Fig 1A) and differed from dusts or anthracosis, which often have a granular structure and are usually observed inside or close to macrophages (Fig 1B).

Figure Jump LinkFigure 1. A, Smear from endobronchial ultrasound-guided transbronchial needle aspiration (EBUS-TBNA) with a high density (score 4) of particles mixed with mucus and tumor cells. The black spots of varying sizes correspond to mineral particle deposits (May-Grünwald-Giemsa [MGG] stain, original magnification ×40). B, Smear from conventional TBNA aspiration showing tumor cells on a clear background and anthracosis in one macrophage (MGG stain, original magnification ×40).Grahic Jump Location
Particles Deposits Were Observed Only in EBUS-TBNA Samples and Their Proportion Increased With the Number of Passes

Foreign deposit was identified with a variable intensity in the cytospins of 57 of the 141 samples assessed under blind conditions. All samples performed by real-time guided EBUS-TBNA (57/57, 100%) were contaminated, whereas no deposit was observed on samples from the conventional TBNA (0/84) (P < .0001). Similar metal particles were also observed in samples from the 12 patients assessed by real-time guided EBUS-TBNA performed in the external center.

Mineral deposits were found with all the tested batches of ViziShot needles and not with the other types of needles (Table 1). The contamination scores of needles from five different batches used to obtain these specimens were not significantly different (P = .59). Interestingly, a statistically significant relationship was found between the contamination score and the number of passes during the procedure, as the fourth pass was associated with the highest score (P = .039) (Fig 2).

Table Graphic Jump Location
Table 1 —Types of Needles Used

EBUS = endobronchial ultrasound; EBUS-TBNA = endobronchial ultrasound-guided transbronchial needle aspiration; TBNA = transbronchial needle aspiration.

Figure Jump LinkFigure 2. Relationship between contamination score (mean rank determined by the nonparametric Friedman test) and the number of aspirations (N). A significant increase in contamination score was observed during consecutive aspirations until the fourth aspiration (P = .039).Grahic Jump Location
Particles Released Are Metal Alloys Used in the Needle Manufacture

Mineral analyses of rinsing solutions from the two types of unused sterile needles showed marked differences (Fig 3). In contrast to the control filter and the rinsing solution from conventional TBNA needles for which no particles were detected (Figs 3A, 3B), the rinsing solution from dedicated EBUS needles revealed black particles similar to the deposits observed on samples obtained by the EBUS-TBNA procedure. These particles were observed in the first rinsing solution (Fig 3C) and were more numerous in rinsing solutions after successive introduction and withdrawal of the stylet (Fig 3D). Mineral analysis by energy dispersive radiograph demonstrated that these particles were composed of metal alloys containing a mixture of iron, titanium, nickel, and chromium (Fig 4).

Figure Jump LinkFigure 3. Transmission electron microscope analysis of the rinsing solution of unused needles. A, No particles were observed on the control filter of a conventional TBNA (bar = 50 μm). B, No particles were observed in the rinsing solution of a conventional TBNA (bar = 50 μm). C, D, The rinsing solution of the EBUS-TBNA needle contains metal particles (dense black spots or small points), (bar = 20 μm). C, The first rinse. D, A higher density after three passes of the stylet. See Figure 1 legend for expansion of abbreviations.Grahic Jump Location
Figure Jump LinkFigure 4. Mineralogical analysis of rinsing solution from unused Vizishot needles: particles are composed of alloys of Ti, Fe, Cr, and Ni. The copper peak corresponds to the transmission electron microscope grids. Cr = chromium; Cu = copper; Fe = iron; Ni = nickel; Si = silicon; Ti = titanium.Grahic Jump Location
Particles Released by EBUS-TBNA Needles Are Able to Contaminate Lymph Nodes

Mineral analysis of control calf thymuses did not find any particles, whereas in three out of the four samples punctured with TBNA-EBUS-dedicated needles, few metallic alloys were detected, which were also compounds of iron, chromium, nickel, and titanium. All rinsing products of needles contained abundant metallic alloys.

This study clearly identified the systematic contamination of samples obtained during EBUS-TBNA by foreign particles. The role of EBUS-TBNA Vizishot needles was suggested by finding similar deposits in the solution obtained after rinsing unused needles, whereas no deposits were observed after rinsing conventional TBNA needles. We hypothesized that the contamination comes from the friction between the needle and the stylet. Our experimental results suggested that the EBUS-TBNA needle may induce deposition of particles into the lymph node in vivo.

Observation of particles on slides from TBNA samples may have two origins: exogenous or endogenous. Particles could be introduced from outside sources, including stains, preserving fluids, or airborne dusts. For example, potential paraffin contamination by asbestos fibers has been described.8 However, this contamination from outside sources should also have been observed in the conventional TBNA samples as a similar procedure was used with the two types of aspiration techniques, and the extent of this contamination remained constant throughout the 18 months of the study.

Endogenous source of particles in mediastinal lymph node samples is mostly anthracosis. However, anthracosis is mostly located inside macrophages or, if “scratched” during spreading of the smear, has a granular appearance and remains associated with dust-filled macrophages, an appearance contrasting with the exclusive extracellular distribution and random pattern of particle deposition observed in the present study.

The contamination scores and transmission electron microscope analyses of rinsing solutions demonstrated increasing particle release with the number of passes (ie, after repeatedly introducing and withdrawing the stylet). It is therefore likely that reintroduction of the stylet into the needle creates friction between the two surfaces, causing release of metal particles. This hypothesis is also supported by the finding that the particles found in mineral analysis of the needle-rinsing solutions were composed of identical alloys to those of the needles (iron and chromium) and stylet (titanium and nickel). It is important to stress that contaminating particles were found with Vizishot needles coming from all the lots that were used, in the leading center but also in the other center, an observation that suggests the contamination problem was common to all needles and not linked to a transient manufacturing problem.

Surprisingly, the observation of metal contamination of samples has never been previously reported with this needle, although at the study time Vizishot (Olympus) was the only dedicated EBUS-TBNA needle available. A center bias, for example related to incorrect use of the stylet and needle, seems unlikely as review of samples from the external cohort examined in another experienced center5,9 confirmed the presence of similar deposits. Because some particles derived from airborne dust are usually observed on smears of mediastinal lymph node samples, one hypothesis is that the additional metal particles from EBUS-TBNA were misinterpreted as anthracosis, and this explanation was confirmed by the pathologists from the other center.

Different sampling techniques could also explain differences in observations between laboratories. For example, when using liquid-based cytology, cells are directly collected into cell fixative and particles can fall and stay in the fixative during smear preparations. Moreover, in our laboratory, we usually performed cytospins from the rinsing product of needles from various punctures as transthoracic needle aspiration or superficial lymph node punctures; we have never observed such material deposited on slides.

The present findings have potential clinical implications. The first concerns a risk of inaccurate examination of slides covered with contaminating particles, leading to a misinterpretation as anthracosis and incorrect assessment of the quality of lymph node sampling. However, most authors10-12 rely on identification of lymphocytes in the sample to confirm that the aspirate is representative of lymph node material.

A second potentially harmful implication is related to the release of abraded metal particles into the bronchial wall and lymph node during repeated aspiration. As described previously, mediastinal lymph nodes are often rich in dust-laden macrophages, which make it difficult to find released particles from the needle. This is the reason that in the present study we used lymphoid tissue devoid of any aero contamination. From these results, a potential risk associated with particle release from the needle during the EBUS-TBNA procedure is hypothesized. Even if a small amount of exogenous particles may be injected into a lymph node, their metabolic activity, different from the already present particles, may modify the microenvironment. Indeed, the particles already present in the background noise of the mediastinal lymph nodes have been previously inhaled, phagocyted by alveolar macrophages, and then transported by the lymphatic to nodes, which is in contrast with particles potentially directly released from the needle into the node.

The health consequences must be considered cautiously, as the long-term effects of direct metal particle contamination of lymph nodes remain unknown. This metal particle deposition could be associated with a potential risk of granulomatous inflammatory reaction or a carcinogenic risk. Epithelioid granulomas on the entry points of needles used for acupuncture, venipuncture, or tattoos, or systemic sarcoidosis with cutaneous manifestations, have already been described.13-17 Moreover, releases of particulate debris, generated at the primary bearing surfaces of arthroplasty (hip or knee) prostheses, have been extensively studied in vivo and in vitro.18-21 in vitro studies evaluating the effect of metal particles on the release of inflammatory mediators showed that cells exposed to particulate debris release a large number of cytokines and prostanoid inflammatory mediators.22-24

In vivo a localized argyria has been reported as a result of abrasion of silver from a tracheal cannula worn for many years, but no pathologic consequence was described.25 The carcinogenic risk is another source of concern, as it depends on the type of foreign material, the host, and the interaction between the two. For the International Agency for Research on Cancer (http://www.iarc.fr/), “implanted foreign bodies of chromium-based and titanium-based alloys, stainless steel are not classifiable as to their carcinogenicity to humans (Group 3).” However, the toxicity, particularly the true carcinogenic risk of metal particles in lymph nodes, is unknown.

EBUS-TBNA is becoming an investigation of choice for the diagnosis of mediastinal lymphadenopathy and lung cancer staging. This study shows that the use of a dedicated EBUS-TBNA Vizishot needle (Olympus) is clearly associated with metal particle deposition composed of a mixture of iron, titanium, nickel, and chromium in samples, and that the level of contamination increases with repeated introduction of the stylet within the needle. Additional experiments have shown a potential risk to inject some particles into nodes during successive passes, but long-term consequences on health remain to be evaluated.

However, safety measures may be rapidly required without questioning the value of EBUS per se. In the hypothesis of failure in quality controls, the present findings were reported to the Agence Française de Sécurité Sanitaire des Produits de Santé (AFSSAPS) (French Health Products Safety Agency) and to the Olympus company, which took into account our remarks.

Author contributions: Drs Gounant and Fleury-Feith had full access to all of the data in the study and take full responsibility for the integrity of the data and the accuracy of the data analysis.

Dr Gounant: contributed to performing TBNA of patients from Tenon Hospital.

Dr Ninane: contributed to performing TBNA of patients from Saint Pierre Hospital and contributed to manuscript preparation and review.

Mr. Janson: contributed to performing mineral analysis.

Dr Colombat: contributed to sample analysis and manuscript preparation and review.

Dr Wislez: contributed to patients’ management and manuscript preparation and review.

Dr Grunenwald: contributed to patients’ management and manuscript preparation and review.

Dr Bernaudin: contributed to sample analysis and manuscript preparation and review.

Dr Cadranel: contributed to patients’ management and manuscript preparation and review.

Dr Fleury-Feith: contributed as the cytopathologist responsible for TBNA samples and performed statistical analysis.

Financial/nonfinancial disclosures: The authors have reported to CHEST that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

Other contributions: We thank the nurses of the endoscopic unit for their technical assistance, the chest physicians of the department of the respiratory medicine, the “ligue contre le cancer” and the “Amis des Centres des Tumeurs de Tenon” for their support, and the butcher who supplied the calf thymuses. This work was performed at the Hôpital Tenon, APHP, Paris, France.

Additional information: The e-Appendix 1 can be found in the Online Supplement at http://chestjournal.chestpubs.org/content/139/1/138/suppl/DC1.

EBUS

endobronchial ultrasound

EBUS-TBNA

endobronchial ultrasound-guided transbronchial needle aspiration

MGG

May-Grünwald-Giemsa

TBNA

transbronchial needle aspiration

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Holty JE, Kuschner WG, Gould MK. Accuracy of transbronchial needle aspiration for mediastinal staging of non-small cell lung cancer: a meta-analysis. Thorax. 2005;6011:949-955. [CrossRef] [PubMed]
 
Varela-Lema L, Fernández-Villar A, Ruano-Ravina A. Effectiveness and safety of endobronchial ultrasound-transbronchial needle aspiration: a systematic review. Eur Respir J. 2009;335:1156-1164. [CrossRef] [PubMed]
 
Lee HS, Lee GK, Lee HS, et al. Real-time endobronchial ultrasound-guided transbronchial needle aspiration in mediastinal staging of non-small cell lung cancer: how many aspirations per target lymph node station? Chest. 2008;1342:368-374. [CrossRef] [PubMed]
 
Plat G, Pierard P, Haller A, et al. Endobronchial ultrasound and positron emission tomography positive mediastinal lymph nodes. Eur Respir J. 2006;272:276-281. [CrossRef] [PubMed]
 
Mehta AC, Kavuru MS, Meeker DP, Gephardt GN, Nunez C. Transbronchial needle aspiration for histology specimens. Chest. 1989;966:1228-1232. [CrossRef] [PubMed]
 
Pairon JC, Billon-Galland MA, Iwatsubo Y, et al. Biopersistence of nonfibrous mineral particles in the respiratory tracts of subjects following occupational exposure. Environ Health Perspect. 1994;102suppl 5:269-275. [PubMed]
 
Dodson RF, O’Sullivan M, Hammar SP. Quality control analysis of the potential for asbestos contamination during tissue processing in pathology laboratories. Arch Pathol Lab Med. 2004;1287:781-784. [PubMed]
 
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Figures

Figure Jump LinkFigure 1. A, Smear from endobronchial ultrasound-guided transbronchial needle aspiration (EBUS-TBNA) with a high density (score 4) of particles mixed with mucus and tumor cells. The black spots of varying sizes correspond to mineral particle deposits (May-Grünwald-Giemsa [MGG] stain, original magnification ×40). B, Smear from conventional TBNA aspiration showing tumor cells on a clear background and anthracosis in one macrophage (MGG stain, original magnification ×40).Grahic Jump Location
Figure Jump LinkFigure 2. Relationship between contamination score (mean rank determined by the nonparametric Friedman test) and the number of aspirations (N). A significant increase in contamination score was observed during consecutive aspirations until the fourth aspiration (P = .039).Grahic Jump Location
Figure Jump LinkFigure 3. Transmission electron microscope analysis of the rinsing solution of unused needles. A, No particles were observed on the control filter of a conventional TBNA (bar = 50 μm). B, No particles were observed in the rinsing solution of a conventional TBNA (bar = 50 μm). C, D, The rinsing solution of the EBUS-TBNA needle contains metal particles (dense black spots or small points), (bar = 20 μm). C, The first rinse. D, A higher density after three passes of the stylet. See Figure 1 legend for expansion of abbreviations.Grahic Jump Location
Figure Jump LinkFigure 4. Mineralogical analysis of rinsing solution from unused Vizishot needles: particles are composed of alloys of Ti, Fe, Cr, and Ni. The copper peak corresponds to the transmission electron microscope grids. Cr = chromium; Cu = copper; Fe = iron; Ni = nickel; Si = silicon; Ti = titanium.Grahic Jump Location

Tables

Table Graphic Jump Location
Table 1 —Types of Needles Used

EBUS = endobronchial ultrasound; EBUS-TBNA = endobronchial ultrasound-guided transbronchial needle aspiration; TBNA = transbronchial needle aspiration.

References

Detterbeck FC, Jantz MA, Wallace M, Vansteenkiste J, Silvestri GA. American College of Chest Physicians American College of Chest Physicians Invasive mediastinal staging of lung cancer: ACCP evidence-based clinical practice guidelines (2nd edition). Chest. 2007;1323suppl:202S-220S. [CrossRef] [PubMed]
 
Holty JE, Kuschner WG, Gould MK. Accuracy of transbronchial needle aspiration for mediastinal staging of non-small cell lung cancer: a meta-analysis. Thorax. 2005;6011:949-955. [CrossRef] [PubMed]
 
Varela-Lema L, Fernández-Villar A, Ruano-Ravina A. Effectiveness and safety of endobronchial ultrasound-transbronchial needle aspiration: a systematic review. Eur Respir J. 2009;335:1156-1164. [CrossRef] [PubMed]
 
Lee HS, Lee GK, Lee HS, et al. Real-time endobronchial ultrasound-guided transbronchial needle aspiration in mediastinal staging of non-small cell lung cancer: how many aspirations per target lymph node station? Chest. 2008;1342:368-374. [CrossRef] [PubMed]
 
Plat G, Pierard P, Haller A, et al. Endobronchial ultrasound and positron emission tomography positive mediastinal lymph nodes. Eur Respir J. 2006;272:276-281. [CrossRef] [PubMed]
 
Mehta AC, Kavuru MS, Meeker DP, Gephardt GN, Nunez C. Transbronchial needle aspiration for histology specimens. Chest. 1989;966:1228-1232. [CrossRef] [PubMed]
 
Pairon JC, Billon-Galland MA, Iwatsubo Y, et al. Biopersistence of nonfibrous mineral particles in the respiratory tracts of subjects following occupational exposure. Environ Health Perspect. 1994;102suppl 5:269-275. [PubMed]
 
Dodson RF, O’Sullivan M, Hammar SP. Quality control analysis of the potential for asbestos contamination during tissue processing in pathology laboratories. Arch Pathol Lab Med. 2004;1287:781-784. [PubMed]
 
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