Transesophageal endosonography in the diagnosis of sarcoidosis: a narrative review
Review Article

Transesophageal endosonography in the diagnosis of sarcoidosis: a narrative review

Yuka Shinohara, Masahide Oki

Department of Respiratory Medicine, NHO Nagoya Medical Center, Nagoya, Japan

Contributions: (I) Conception and design: Both authors; (II) Administrative support: M Oki; (III) Provision of study materials or patients: Both authors; (IV) Collection and assembly of data: Y Shinohara; (V) Data analysis and interpretation: Y Shinohara; (VI) Manuscript writing: Both authors; (VII) Final approval of manuscript: Both authors.

Correspondence to: Masahide Oki, MD. Department of Respiratory Medicine, NHO Nagoya Medical Center, 4-1-1 Sannomaru, Naka-ku, Nagoya 460-0001, Japan. Email: masahideo@aol.com.

Background and Objective: Transesophageal endosonography, including endoscopic ultrasound-guided fine-needle aspiration (EUS-FNA) and endoscopic ultrasound with bronchoscope-guided fine-needle aspiration (EUS-B-FNA), has been applied to the diagnosis of benign as well as malignant diseases. This narrative review summarizes the recent use of EUS-(B)-FNA in diagnosing sarcoidosis.

Methods: A comprehensive and systematic online literature search of PubMed was conducted using the keywords (“sarcoidosis”), and (“EUS” OR “EUS-FNA” OR “EUS-B” OR “EUS-B-FNA” OR “endoscopic ultrasound guided fine needle aspiration” OR “endoscopic ultrasound using the EBUS scope guided fine needle aspiration” OR “endoscopic ultrasound using the EBUS bronchoscope” OR “transesophageal” OR “transesophageal endoscopic ultrasound guided fine needle aspiration” OR “transesophageal bronchoscopic ultrasound guided fine needle aspiration”).

Key Content and Findings: Most EUS-FNA procedures were performed under moderate sedation, primarily using midazolam, with 22-gauge needles. The diagnostic sensitivity of sarcoidosis in mediastinal lymph node sampling is as high as 75−100% for EUS-FNA and 70−86% for EUS-B-FNA, much higher than that of traditional bronchoscopic procedures, such as transbronchial lung biopsy (TBLB) and conventional transbronchial needle aspiration (TBNA). The complications associated with EUS-(B)-FNA have thus far included only a few cases of mediastinitis, successfully treated with antibiotics, as well as lymph node hematoma, and sore throat.

Conclusions: EUS-FNA and EUS-B-FNA provide high diagnostic yields in patients with sarcoidosis. The safety profile is acceptable, although there is a slight risk of infectious complications. EUS-B-FNA, a minimally invasive and well-tolerated procedure, offers a viable alternative to endobronchial ultrasound-guided TBNA (EBUS-TBNA) for the diagnosis of sarcoidosis, particularly in patients with cough and poor respiratory function; this procedure can easily be performed by pulmonologists.

Keywords: Endoscopic ultrasound-guided fine-needle aspiration (EUS-FNA); endoscopic ultrasound with bronchoscope-guided fine-needle aspiration (EUS-B-FNA); sarcoidosis

Received: 22 July 2024; Accepted: 25 October 2024; Published online: 04 December 2024.

doi: 10.21037/med-24-37

Introduction

The clinical manifestations of sarcoidosis are often non-specific. The granulomatous inflammation seen in sarcoidosis is also associated with other diseases that present with similar findings, including tuberculosis, fungal infections, lymphoma, lung cancer, and berylliosis, all of which must be excluded (1,2). Thus, to avoid false-positive results, a definitive diagnosis requires both clinical and radiologic confirmation, including evidence of noncaseating granuloma of the involved tissue (3).

In patients with lesions that do not involve the skin or peripheral lymph nodes and thus cannot be easily sampled, transbronchial lung biopsy (TBLB) was recommended in the previous American Thoracic Society guidelines published in 1999 (2). However, the diagnostic yield of this procedure is only ~65% (40−90%) and a pathological diagnosis cannot be made in one-third of the cases (4,5). In addition, TBLB is occasionally associated with pneumothorax (incidence of 1−5%) and bleeding (9%) (6). Transbronchial needle aspiration (TBNA), as a conventional bronchoscopic approach, has a diagnostic yield similar to that of TBLB (42−76%) (7-9). Mediastinoscopy was once the next step in patients not diagnosed by TBLB or TBNA, as the reported diagnostic yield is as high as 82–97% (10-12), but the procedure is invasive and requires hospitalization and general anesthesia.

The development of endosonography, including endoscopic ultrasound-guided fine-needle aspiration (EUS-FNA) and endobronchial ultrasound-guided TBNA (EBUS-TBNA), has dramatically changed the evaluation of hilar-mediastinal lesions. The high accuracy and safety of endosonography for diagnosing benign as well as malignant lesions is now well established (13,14). As sarcoidosis is characterized by enlarged hilar and mediastinal lymph nodes, endosonography has proven useful in obtaining tissue specimens for its diagnosis, as demonstrated in several studies. The advantages of EBUS-TBNA are that it allows real-time TBNA and the locations of the needle and the target lesion on ultrasound images can be simultaneously confirmed. Given its high diagnostic yield (71−94%) and excellent safety (15-23), EBUS-TBNA is now recommended as the first-line method of tissue sampling in patients with suspected sarcoidosis (3). Although the reported diagnostic accuracy of EUS-FNA for accessible mediastinal lesions is comparable to that of EBUS-TBNA, a recent guideline (3) did not refer to its use for tissue sampling in sarcoidosis. This narrative review summarizes the current application of EUS-FNA and endoscopic ultrasound with bronchoscope-guided fine-needle aspiration (EUS-B-FNA) in diagnosing thoracic sarcoidosis. We present this article in accordance with the Narrative Review reporting checklist (available at https://med.amegroups.com/article/view/10.21037/med-24-37/rc).

Methods

A comprehensive and systematic online literature search of PubMed was conducted using the keywords (“sarcoidosis”), and (“EUS” OR “EUS-FNA” OR “EUS-B” OR “EUS-B-FNA” OR “endoscopic ultrasound guided fine needle aspiration” OR “endoscopic ultrasound using the EBUS scope guided fine needle aspiration” OR “endoscopic ultrasound using the EBUS bronchoscope” OR “transesophageal” OR “transesophageal endoscopic ultrasound guided fine needle aspiration” OR “transesophageal bronchoscopic ultrasound guided fine needle aspiration”). From the initially identified 35,324 articles related to sarcoidosis, 296 articles were retrieved. After the exclusion of those that did not include mediastinal disease, 258 articles remained. Editorials, comment, letters, proceedings, books, and abstracts were also excluded. The majority of the articles were related to EBUS-TBNA. After the list was narrowed to articles with at least 10 cases of sarcoidosis diagnosed by EUS-FNA and EUS-B-FNA, 15 articles were finally reviewed. The search strategy is summarized in Table 1.

Table 1

Search strategy summary

Items Specification
Date of search May 18, 2024
Databases and other sources searched PubMed
Search terms used (“sarcoidosis”), and (“EUS” OR “EUS-FNA” OR “EUS-B” OR “EUS-B-FNA” OR “endoscopic ultrasound guided fine needle aspiration” OR “endoscopic ultrasound using the EBUS scope guided fine needle aspiration” OR “endoscopic ultrasound using the EBUS bronchoscope” OR “transesophageal” OR “transesophageal endoscopic ultrasound guided fine needle aspiration” OR “transesophageal bronchoscopic ultrasound guided fine needle aspiration”)
Timeframe January 1, 1938 to May 18, 2024
Inclusion and exclusion criteria Inclusion criteria: original article, research article, full paper, English language
Exclusion criteria: editorial, comments, letters, proceedings, books, abstracts, non-English papers, less than 10 cases of sarcoidosis diagnosed
Selection process First author conducted the selection process, initial literature review, assessed all of the identified studies based on the eligibility criteria. Both authors reviewed the final list of studies included in the review

EUS, endoscopic ultrasound; EUS-FNA, endoscopic ultrasound-guided fine-needle aspiration; EUS-B-FNA, endoscopic ultrasound with bronchoscope-guided fine-needle aspiration; EBUS, endobronchial ultrasound.

Procedures

The results regarding the use of EUS-FNA and EUS-B-FNA in diagnosing sarcoidosis are summarized in Table 2 (18,24-35) and Table 3 (36-38). In most studies, EUS-FNA was performed with the patients under moderate sedation, mainly using midazolam, but in a few studies the patients were placed under deep sedation using propofol. Because EUS endoscopes have a larger working channel than EBUS bronchoscopes, a variety of needles are available. The reliability of the cytological diagnosis of sarcoidosis has been well established. In most studies, 22-gauge needles were used, but a few studies used 19-gauge needles. In a prospective study, Iwashita et al. prepared cytological and histological specimens obtained using a 19-gauge needle, and each specimen was blindly evaluated by pathologists (29). The sensitivity of histological specimens in EUS-FNA was significantly higher than that of cytological specimens (94.4% vs. 77.8%, P=0.0444). The subcarinal lymph nodes were the most frequently examined, followed by the left paratracheal lymph nodes. The subaortic, para-esophageal, and intra-abdominal lymph nodes, which are inaccessible by EBUS-TBNA, were evaluated only rarely.

Table 2

Studies using EUS-FNA in patients with suspicion of sarcoidosis

Author Year Study design Sedation Needle size (G) Size of LN, mm† No. of passes LN examined Stage No. of patients examined No. of patients with sarcoidosis No. of patients with sarcoidosis diagnosed by EUS-FNA Sensitivity for diagnosing sarcoidosis, % Complications Other
Fritscher-Ravens (24) 2000 Retrospective Moderate sedation 22 NA NA NA NA 153 16 16 100 No False positive result: 1
Fritscher-Ravens (25) 2000 Prospective NA 22 24 [10–41] NA #4R, #5, #7, #8 I, II, III 19 18 18 100 No False positive result: 1
Wildi (26) 2004 Retrospective NA 22 18 [5–40] ≥4 Subcarinal, AP window, paratracheal, para-aortal NA 124 28 25 89 No
Annema (27) 2005 Prospective Moderate sedation 22 25 [5–40] Mean 3 Lt paratracheal, AP window, subcarinal, para-esophageal I, II 51 50 41 82 No
Michael (28) 2008 Retrospective Moderate/deep sedation 22/25 NA Mean 5.3 per lesion Subcarinal/mediastinal/intra-abdominal NA 21 21 18 86 Mild sore throat: 1 Intra-abdominal LN: 7
Iwashita (29) 2008 Prospective Moderate sedation 19 19 [5–42] Mean 2.4 Subcarinal, left/right hilar, left paratracheal I 41 36 34 94.4 Mediastinitis: 1
Tournoy (18) 2010 Prospective Moderate/deep sedation 22 NA NA NA NA 18 17 16 94 No TBB + EBB/TBNA: 121; EBUS-TBNA: 54
von Bartheld (30) 2010 Retrospective Moderate sedation 22 NA Mean 3.9 #2R, #4L, #4R, #5, #7, #8 I, II 100 91 79 87 Mediastinitis: 1; local hematoma: 1; sore throat: 1
Fritscher-Ravens (31) 2011 Prospective NA 22 [5–42] ≥3 (2 for cytology, 1 for bacteriological analysis) Mostly subcarinal, AP window I, II 71 30 30 100 No False positive result: 3
von Bartheld (32) 2013 Randomized Moderate/deep sedation 22 NA Mean 5.21 NA I, II 102 NA NA 88 Mediastinal abscess EBUS-TBNA: 56; bronchoscopy:
149
Jamil (33) 2014 Retrospective NA 19/22/25 15 [7–33] Median 3 NA NA 160 32 25 78.1 NA
Gnass (34) 2015 Randomized Moderate sedation 22 ≥10 3–5 NA I, II 36 35 31 88.6 No EBUS-TBNA: 36; TBNA: 43
Kocoń (35) 2017 Randomized Moderate sedation 22 NA 3–6 #4L, #7 I, II 51 NA NA 75 No EBUS-TBNA: 55

†, mean or median [range]. #2R, right upper paratracheal; #4R, right lower paratracheal; #4L, left lower paratracheal; #5, subaortic; #7, subcarinal; #8, paraesophageal. EUS-FNA, endoscopic ultrasound-guided fine-needle aspiration; G, gauge; LN, lymph nodes; NA, not available; AP, aortopulmonary; Lt, left; TBB, transbronchial biopsy; EBB, endobronchial biopsy; TBNA, transbronchial needle aspiration; EBUS-TBNA, endobronchial ultrasound-guided-transbronchial needle aspiration.

Table 3

Studies on EUS-B-FNA in patients suspected of sarcoidosis

Author Year Study design Sedation Needle size (G) Size of LN, mm† No. of passes LN examined Stage No. of patients examined No. of patients with sarcoidosis No. of patients with sarcoidosis diagnosed by EUS-FNA Sensitivity for diagnosing sarcoidosis, % Complications Other
Oki (36) 2013 Prospective Moderate sedation 21 13.6 [6.8–28.7] Mean 3.3 per lesion #2L, 3p, #4R/L, #7, #8, #10L I, II 33 29 25 86 No
Filarecka (37) 2020 Prospective Moderate sedation 22 15.2 3–5 #2R/L, #4R/L, #7, #8 I, II 50 47 33 70.21 No
Crombag (38) 2022 Randomized Moderate/deep sedation 22/25 18 [15–22] ≥5 #2R, #4R/L, #7, #8, #9 I, II 358 141 115 82 No EBUS-TBNA: 185

†, mean or median [range]. #2L, left upper paratracheal; #2R/L, right/left upper paratracheal; 3p, retrotracheal; #4R/L, right/left lower paratracheal; #7, subcarinal; #8, paraesophageal; #9, pulmonary ligament; #10L, left hilar. EUS-B-FNA, endoscopic ultrasound with bronchoscope-guided fine-needle; G, gauge; LN, lymph node; EUS-FNA, endoscopic ultrasound-guided fine-needle aspiration; EBUS-TBNA, endobronchial ultrasound-guided-transbronchial needle aspiration.

Diagnostic performance of EUS-FNA

In 1999, Mishra et al. published the first report of the usefulness of EUS-FNA in diagnosing sarcoidosis (39), based on the cytological diagnosis of sarcoidosis in 6 of 108 patients who underwent EUS-FNA of the mediastinal lymph nodes. Subsequently, several investigators reported the diagnostic efficacy of EUS-FNA in patients with sarcoidosis. In 13 studies, 4 involving patients with mediastinal lymphadenopathy (24,26,31,33) and 9 limited to patients with suspected sarcoidosis (18,25,27-30,32,34,35), the reported sensitivities ranged from 75% to 100% (Table 2). The results are comparable to those obtained with EBUS-TBNA [71–94% (15-22)] or mediastinoscopy [82–97% (10-12)].

Three studies evaluated the diagnostic yield of EUS-FNA in patients with negative bronchoscopy results. Tournoy et al. performed EUS-FNA in 18 patients with negative bronchoscopy [TBLB, TBNA, endobronchial biopsy (EBB)] for sarcoidosis and reported a sensitivity of 94% in 16 patients (18). In a crossover study, Gnass et al. performed EUS-FNA in 21 patients with negative TBNA or EBUS-TBNA results; sarcoidosis was diagnosed in 9 patients whereas EBUS-TBNA did not identify any additional cases among 5 patients with negative EUS-FNA results (34). In a crossover study, Kocoń et al. reported that EUS-FNA was of diagnostic utility in 7 of 8 patients with negative bronchoscopy results (combined EBUS-TBNA, TBLB, EBB and TBNA), and EBUS-TBNA in 2 of 8 patients with negative bronchoscopy results (combined EUS-FNA, TBLB, EBB and TBNA) (35).

As granulomatous inflammation is associated with many diseases besides sarcoidosis, including tuberculosis and fungal infections, there is a risk of false-positive results, but such cases are rare. In a study investigating the usefulness of EUS-FNA in differentiating between tuberculosis and sarcoidosis, including 30 cases of sarcoidosis and 28 cases of tuberculosis, 3 tuberculosis cases were initially misdiagnosed as sarcoidosis based on the cytology obtained with EUS-FNA (31).

Diagnostic performance of EUS-B-FNA

Despite the high diagnostic utility of mediastinal lymph node biopsy by EUS-FNA, the procedure is limited by the need for a skilled endoscopist and specialized equipment, such as an ultrasound endoscope and needle. An EBUS bronchoscope, equipped with a miniaturized convex probe at its tip, shares a mechanism similar to an EUS endoscope. Therefore, the transesophageal EUS-FNA procedure can be performed using an EBUS bronchoscope; this technique is termed EUS-B-FNA (40). Considering the familiarity of pulmonologists with EBUS bronchoscopy, they may find it easier to perform EUS-B-FNA than to perform EUS-FNA. In addition, EUS-FNA is better tolerated and less invasive than EBUS-TBNA (41).

The results obtained with EUS-B-FNA in diagnosing sarcoidosis are summarized in Table 3. Oki et al. evaluated the diagnostic utility of EUS-B-FNA in a prospective study of 33 patients with suspected stage I/II sarcoidosis; they reported a diagnostic yield of 86% (36). Filarecka et al. evaluated EBUS-TBNA followed by EUS-B-FNA in 50 patients with suspected stage I/II sarcoidosis. The sensitivity of EBUS-TBNA, EUS-B-FNA, and its combination was 76.6%, 70.2%, and 91.7%, respectively (37). Crombag et al. published a large multicenter international randomized trial in 2022 that included 358 patients with suspected stage I/II sarcoidosis. The study randomized 185 patients to EBUS-TBNA and 173 to EUS-B-FNA; 306 patients (86%) were ultimately diagnosed with sarcoidosis. The detection rate and sensitivity based on the detected granulomas were 70% and 78% for EBUS-TBNA and 68% and 82% for EUS-B-FNA, respectively; the differences between the two groups were not significant (38).

Safety of EUS-FNA and EUS-B-FNA

Of the 13 studies on EUS-FNA, a small number of cases reported serious complications, including mediastinitis (2 cases) and mediastinal abscess (1 case) (29,30,32). Although the safety of EUS-FNA has been well established, the risk of infectious complications in sarcoidosis patients should be kept in mind. In a case series of 252 patients with sarcoidosis who underwent EUS-FNA, 5 developed mediastinal abscess, with 4 patients requiring surgical treatment (42). The other reported complications associated with EUS-FNA were all minor ones, such as sore throat and hematoma.

In three studies of EUS-B-FNA, no complications were reported. Severe cough or oxygen desaturation, which often occur during EBUS-TBNA, are less common during EUS-B-FNA. In the study by Oki et al., oxygen desaturation occurred in only 6% of patients (36). Pulmonologists unfamiliar with transesophageal procedures should be cautious when performing EUS-B-FNA in patients with suspected esophageal varices, esophagitis, and esophageal stenosis (43). These conditions may increase the risk of complications during the procedure.

Will EUS-FNA become the method of choice for tissue sampling in sarcoidosis?

As sarcoidosis often involves the hilar-mediastinal lymph nodes and lungs, patients are often managed by pulmonologists. However, while pulmonologists are able to easily perform bronchoscopy, including EBUS-TBNA, TBLB, TBNA, and EBB, they are often not familiar with the handling of an EUS endoscope. The diagnostic performance of EUS-FNA is comparable to that of EBUS-TBNA; consequently, under certain circumstances, such as the availability of experienced endoscopists and an EUS-endoscope or sampling from EUS- but not EBUS-accessible lesions, it is a useful alternative to EBUS-TBNA when diagnosing sarcoidosis. EUS-B-FNA overcomes the limitation of EUS-FNA and offers an alternative to EBUS-TBNA (44,45). Although there is a learning curve, pulmonologists experienced in EBUS-TBNA can learn and perform EUS-B-FNA relatively easily (46,47). Pulmonology trainees should gain experience with EBUS, EUS-B-FNA, and EUS-FNA techniques (40). EUS-B-FNA offers the advantages of being minimally invasive and well-tolerated, even in patients with cough and poor respiratory function. Given the high tolerability and diagnostic efficacy of EUS-B-FNA, it is an effective technique available to pulmonologists when mediastinal sampling is required.

Conclusions

EUS-FNA and EUS-B-FNA are highly accurate procedures for diagnosing sarcoidosis. The reported safety profile is acceptable, although the risk of infectious complications should be considered. In particular, given its ease of performance by pulmonologists, EUS-B-FNA offers a useful alternative to EBUS-TBNA in the diagnosis of sarcoidosis.

Acknowledgments

Funding: None.

Footnote

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at https://med.amegroups.com/article/view/10.21037/med-24-37/rc

Peer Review File: Available at https://med.amegroups.com/article/view/10.21037/med-24-37/prf

Conflicts of Interest: Both authors have completed the ICMJE uniform disclosure form (available at https://med.amegroups.com/article/view/10.21037/med-24-37/coif). M.O. reports receiving speaker fees from Olympus Corporation and Fujifilm Corp. as a guest speaker at academic medical meetings. The other author has no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

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doi: 10.21037/med-24-37
Cite this article as: Shinohara Y, Oki M. Transesophageal endosonography in the diagnosis of sarcoidosis: a narrative review. Mediastinum 2024;8:50.

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