
==== Front
Medicine (Baltimore)
Medicine (Baltimore)
MD
Medicine
0025-7974
1536-5964
Lippincott Williams & Wilkins Hagerstown, MD

39312306
MD-D-24-07794
00007
10.1097/MD.0000000000039760
3
5700
Research Article
Systematic Review and Meta-Analysis
Comparison of electromagnetic navigation bronchoscopy localization and CT-guided percutaneous localization in resection of lung nodules: A protocol for systematic review and meta-analysis
Tan Yan MD 55902570@qq.com
a
Shen Shuijun MD 71574993@qq.com
a
Wang Canyun MD 313763562@qq.com
a
Zhou Qiaojuan MD 124691695@qq.com
a
https://orcid.org/0009-0004-8384-0976
Jing Qifeng MD a*
a Department of Radiology, Xiaoshan Affiliated Hospital of Wenzhou Medical University, Hangzhou, Zhejiang, China.
* Correspondence: Qifeng Jing, Department of Radiology, Xiaoshan Affiliated Hospital of Wenzhou Medical University, Hangzhou, Zhejiang 311200, China (e-mail: lief2002@163.com).
20 9 2024
20 9 2024
103 38 e3976009 7 2024
27 8 2024
29 8 2024
Copyright © 2024 the Author(s). Published by Wolters Kluwer Health, Inc.
2024
https://creativecommons.org/licenses/by-nc/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial License 4.0 (CCBY-NC), where it is permissible to download, share, remix, transform, and buildup the work provided it is properly cited. The work cannot be used commercially without permission from the journal.

Background:

This study aimed to evaluate the efficacy and safety between electromagnetic navigational bronchoscopy (ENB) and computed tomography (CT)-guided percutaneous localization before resection of pulmonary nodules.

Methods:

Pubmed, Embase, Web of Science, and the Cochrane Library databases were searched from January 1, 2000 to April 30, 2022, for relevant studies. Two reviewers conducted the search, selection, and extraction of data from eligible studies. The risk of bias was assessed using the Newcastle–Ottawa Scale. The primary outcome was the localization success rate, and the secondary outcomes were the pneumothorax incidence and localization time. The meta-analysis was performed by Review Manager 5.4. The protocol for the meta-analysis was registered on PROSPERO (Registration number: CRD42022345972).

Results:

Five cohort studies comprising 441 patients (ENB group: 185, CT group: 256) were analyzed. Compared with the CT-guided group, the ENB-guided group was associated with lower pneumothorax incidence (relative ratio = 0.16, 95% confidence interval [CI]: 0.04–0.65, P = .01). No significant differences were found in location success rates (relative ratio = 1.01, 95% CI: 0.98–1.05, P = .38) and localization time (mean difference = 0.99, 95% CI: −5.73 to 7.71, P = .77) between the ENB group and CT group.

Conclusion:

Both ENB and CT-guided are valuable technologies in localizing lung nodules before video-assisted thoracoscopic surgery based on current investigations. ENB achieved a lower pneumothorax rate than the CT-guided group. In our opinion, there is no perfect method, and decision-making should be given the actual circumstances of each institute. Future prospective studies in the form of a randomized trial are needed to confirm their clinical value.

CT-guided
electromagnetic navigation bronchoscopy
localization
pulmonary nodule
video-assisted thoracic surgery
OPEN-ACCESSTRUE
SDCT
==== Body
pmc1. Introduction

The U.S.-based National Lung Screening Trial recently confirmed that mortality at a median follow-up of 5.5 and 6.0 years was as much as 19% lower with computed tomography (CT) screening than with chest radiography.[1] In addition, the NELSON study, a Dutch–Belgian lung cancer screening trial, demonstrated a notable reduction in lung cancer mortality among high-risk individuals who underwent CT screening compared to those who did not undergo screening.[2] Such screening has been shown to increase the detection of lower-staged lung nodules.[3–5] Although detection of early-stage lung cancer improves the prognosis,[6] it can be challenging to localize small peripheral lung nodules during video-assisted thoracoscopic surgery (VATS).[7]

Therefore, various methods have been developed to localize these small lesions before undergoing thoracic surgery. One of the most common localization methods for lung resection is CT-guided percutaneous localization, which has been established to be a safe, time-saving, and effective approach.[8–10] However, several studies have shown that the CT-guided percutaneous marking technique leads to many complications, including pneumothorax (<25%),[8,11] wire dislodgement (<33%),[12,13] and air embolism,[14–17] which are sometimes potentially fatal. Patients in the CT-guided percutaneous localization group required transportation from the CT room to the operating room (OR), thereby heightening the potential risks of the whole localization process.

In recent years, the use of electromagnetic navigation bronchoscopy (ENB)-guided localization has become increasingly popular.[18] ENB system is a new technology using a catheter with locatable guidance to reach the peripheral pulmonary lesions.[19] An increasing body of evidence suggests that ENB-guided marking is effective at localizing small pulmonary nodules for resection.[20–22] The advantages of ENB-guided localization include a lower risk of complications, including pneumothorax (<10%),[20,23] and it can be performed in the OR. Dr Shinagawa and Dr Sato expected the ENB technique to be one of the useful methods available for bronchoscopic localization, but some limitations were mentioned such as a complicated setting, no way to precisely confirm the position of the localization, and the high cost of disposal equipment.[24]

Each technique has its advantages and disadvantages. The use of ENB-guided localization versus CT-guided localization has not previously been assessed systematically. Accordingly, we decided to conduct a meta-analysis of the available literature based on ENB versus CT in the localization of lung nodules.

2. Methods

2.1. Protocol and registration

This meta-analysis was conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) guidelines for systematic reviews and meta-analyses.[25] The PRISMA checklist is given in Supplementary Table, Supplemental Digital Content, http://links.lww.com/MD/N602. The protocol for the meta-analysis was registered on PROSPERO (Registration number: CRD42022345972).

2.2. Eligibility criteria

Included studies had to meet the following criteria: prospective or retrospective studies of ≥20 subjects with lung nodules that reported complication and location success rates associated with hook-wire and ENB before resection; adequate monitoring of complications during the procedure; studies were published in English; either randomized controlled trials or cohort studies. Studies were excluded if they: were case reports; were systematic reviews or meta-analyses; reviews and studies without full text; and studies without sufficient data. The related article’s function was used to expand the search, and all studies, abstracts, and citations obtained were reviewed. References of the relevant reviews, meta-analyses, and systematic reviews were also searched by hand.

2.3. Search strategy

A literature search was performed from January 1, 1990 to April 30, 2022, on Pubmed, Embase, Web of Science, and the Cochrane Library, using the search terms: (Electromagnetic navigation*) AND (Computed tomography-guided OR CT-guided) AND (pulmonary nodule OR lung nodule) AND (localization) AND (video-assisted thoracic surgery OR VATS).

2.4. Study selection

The retrieved articles were reviewed for eligibility by 2 investigators (Y.T. and Q.J.) independently. Each of them independently read the titles and abstracts of the literature, removed duplicates and excluded literature that did not meet the inclusion criteria, and read the full text of the literature that did meet the criteria. To reach a consensus, 2 researchers checked the results with each other, carried out quality assessments, and consulted a third researcher if there were any disagreements.

2.5. Data extraction

From the eligible articles, we extracted data including publication year, country, study type, number of patients, nodule size, marking methods, and outcomes of marking methods, including location success rates, pneumothorax incidence, and localization time.

2.6. Ethical statement

This study did not require ethical approval since data from previously published studies involving informed consent were retrieved and analyzed.

2.7. Quality assessment and risk bias

The methodological quality of the studies was assessed using the Newcastle–Ottawa Scale, leading to an overall score of 0 to 9.[26] Two investigators (Y.T. and Q.J.) independently scored the studies, and any study with a score of 5 or greater was deemed high quality.[26]

2.8. Data synthesis and statistical analysis

We listed the success rate of localization, pneumothorax incidence, and localization time per study. Subsequently, we calculated the pooled location success rate, pneumothorax incidence, localization time, and the corresponding 95% confidence interval (CI) using the random effect model. The relative risk (RR) and mean difference were used to clarify which localization method was preferable in each study. Forest plots were generated to visualize the results. Heterogeneity among studies was tested and quantified using the Q test and I2 statistic.[27] I2 values >50% represented significant heterogeneity.[28] The P value for heterogeneity was set at <.05. Review Manager 5.4 was utilized to conduct the present meta-analysis.

3. Results

3.1. Study selection and characteristics

The initial literature retrieval process yielded 474 studies with 165 duplicates. In total, 309 titles and abstracts were reviewed for eligibility. Seven studies met the criteria for full-text assessment. Of these eligible studies, 5 cohort studies were chosen in the meta-analysis (Fig. 1). The characteristics of the included studies were compiled in Tables 1 and 2. These 5 studies enrolled a total of 441 participants (ENB 185, CT 256). Given the complexity of the ENB-guided localization and CT-guided localization, the table presents the characteristics of the ENB group and CT group, including the type of study, demographics of the 2 groups, nodule size, and marking technology.

Table 1 Characteristics of included studies in the ENB group.

Author	Year	Country	Study type	Mean age (yr)	Participants (female) [n (%)]	Nodule mean size (mm)	Marking technology	Pneumothorax incidence	
ENB group	ENB group	ENB group	ENB group	
Yang et al[29]	2021	China	Cohort study	Not given	8 (66.7)	11	ICG/iopamidol	0	
Hung et al[30]	2020	Taiwan, China	Cohort study	Not given	13 (52)	10	Patent blue/indocyanine green	Not given	
Tian et al[31]		China	Cohort study	Not given	21 (40.4)	Not given	Methylene blue	0	
Kuo et al[32]	2019	Taiwan, China	Cohort study	54.4	5 (29.5)	10	Patent blue vital	1	
Bolton et al[33]	2017	American	Cohort study	65	52 (64.2)	15.9	Methylene blue	0	
ENB = electromagnetic navigation bronchoscopy.

Table 2 Characteristics of included studies in the CT group.

Author	Year	Country	Study type	Mean age (yr)	Participants (female) [n (%)]	Nodule mean size (mm)	Marking technology	Pneumothorax incidence	
CT group	CT group	CT group	CT group	
Yang et al[29]	2021	China	Cohort study	Not given	35 (74.3)	7	ICG/iopamidol	5	
Hung et al[30]	2020	Taiwan, China	Cohort study	Not given	25 (50)	9	Hook-wire/microcoil	17	
Tian et al[31]	2020	China	Cohort study	Not given	105 (45.7)	Not given	Hook-wire	12	
Kuo et al[32]	2019	Taiwan, China	Cohort study	56.3	6 (20)	11	Patent blue vital	11	
Bolton et al[33]	2017	American	Cohort study	62	21 (58.3)	12.7	Hook-wire	Not given	
CT = computed tomography.

Figure 1. PRISMA flowchart of the article selection process. PRISMA = Preferred Reporting Items for Systematic Reviews and Meta-Analyses.

3.2. Quality assessment and risk bias

According to the Newcastle–Ottawa criteria, there were 3 studies with a low risk of bias and 2 with a moderate risk of bias. Detailed assessments of the risk of bias are listed in Table 3.

Table 3 Quality assessment of included studies.

Study	Selection	Comparability	Outcome	Total		
Representativeness of the sample	Selection of the nonintervention cohort	Ascertainment of exposure	Demonstration that outcome of interest was not present at the start of the study	Comparability based on design and analysis	Assessment of outcome	Was follow-up long enough for outcomes to occur	Adequacy of follow-up of cohorts	Assessment	
Yang et al[29]	1	1	1	1	2	1	1	1	9	good	
Hung et al[30]	1	1	0	1	2	0	1	1	7	good	
Tian et al[31]	1	1	0	1	2	1	0	1	7	good	
Kuo et al[32]	1	1	1	1	2	1	1	1	9	good	
Bolton et al[33]	1	1	1	1	2	1	1	1	9	good	

3.3. Synthesis of results

The technical aspects of the procedures across studies are outlined in Table 4, including the study period, nodule size, nodule type, localization time, localization success rate, and pneumothorax incidence.

Table 4 Study localization technology procedure details.

Study	Study period	Nodule size (mm)	Nodule type	Localization time (min)	Localization success rate, n (%)	Pneumothorax incidence, n (%)	
ENB group	CT group	ENB group	CT group	ENB group	CT group	ENB group	CT group	ENB group	CT group	
Yang et al[29]	January 2018–December 2019	11 (7–18)	7 (3–20)	GGN, solid	GGN, solid	Not given	Not given	12 (100)	33 (94.3)	0	5 (14)	
Hung et al[30]	January 2018–May 2019	10 (8–12.5)	9 (7–12)	GGN, solid	GGN, solid	Not given	45–74.8	24 (96)	50 (100)	Not given	17 (34)	
Tian et al[31]	January 2016–December 2019	5–12	5–12	GGN	GGN	21.29 ± 4	15.15 ± 3.7	52 (100)	99 (94.3)	0	12 (11.4)	
Kuo et al[32]	January 2016–May 2018	10 ± 5 (6–15)	11 ± 6 (5–18)	GGN, solid	GGN, solid	21.8 ± 12.5	26.3 ± 14	14 (93.3)	27 (90)	1 (4.2)	11 (22.9)	
Bolton et al[33]	July 2011–May 2015	15.9 ± 8.1	12.7 ± 8.7	GGN, solid	GGN, solid	25 ± 9	26 ± 14	81 (100)	36 (100)	Not given	Not given	
CT = computed tomography, ENB = electromagnetic navigation bronchoscopy, GGN = ground-glass opacity nodule.

3.3.1. Location success rates

The technical success rate was the primary outcome of our study. Data about the technical success rate were reported in all studies.[29–33] The RR was 1.01 (95% CI: 0.98–1.05, P = .38), with no significant heterogeneity (I2 = 5%, P = .38) (Fig. 2). A sensitivity analysis indicated no statistically significant difference among the studies.

Figure 2. Combined RR of location success rates: ENB group versus CT group. CT = computed tomography, ENB = electromagnetic navigation bronchoscopy, RR = relative ratio.

3.3.2. Pneumothorax incidence

Pneumothorax incidence and localization time were the secondary outcomes of this study. All studies provided data on the pneumothorax rate.[29–33] The pooled RR was 0.16 (95% CI: 0.04–0.65, P = .01), with no significant heterogeneity (I2 = 0, P = .83) (Fig. 3). A sensitivity analysis demonstrated no statistically significant difference among the studies.

Figure 3. Combined RR of pneumothorax rates: ENB group versus CT group. CT = computed tomography, ENB = electromagnetic navigation bronchoscopy, RR = relative ratio.

3.3.3. Localization time

Three studies reported on the localization time (16–18). The mean difference was 0.99 (95% CI: −5.73 to 7.71, P = .77), with significant heterogeneity (I2 = 85%, P = .001) (Fig. 4). We subsequently explored potential sources of heterogeneity. When 1 study was removed,[31] the heterogeneity significantly decreased (I2 = 0%, P = .47).

Figure 4. Combined MD of localization time: ENB group versus CT group. CT = computed tomography, ENB = electromagnetic navigation bronchoscopy, MD = mean difference.

4. Discussion

This study showed that the 2 preoperative localization methods yielded high successful marking rates with no significant difference in localization time. However, the ENB-guided group was associated with a lower pneumothorax incidence than the CT-guided group.

Percutaneous needle localization before VATS was first reported in Plunkett et al.[34] Various localization approaches have been developed to identify small pulmonary nodules.[35–38] CT-guided localization is the most widely used method for localizing small lung nodules for resection. This approach requires percutaneous placement of metal markers, especially hook wires or microcoils.[39,40] ENB-guided localization is a newer technique of lung nodule localization favorable for difficult-to-reach areas of the lung.[41] This technique reportedly has high accuracy in detecting and marking small pulmonary nodules and is associated with no major complications.[42] To our knowledge, no meta-analysis has hitherto compared ENB-guided versus CT-guided for localization of lung nodules. We conducted this systematic review to assess the efficacy and safety of these localization methods.

Meta-analyses have shown no significant differences in localization success rate. CT-guided localization is the most common method for VATS resection, with a localization rate of 93.7% to 98%.[41] However, the risk of dislodgement or migration of hook-wire after localization is a major limitation of this technique.[43] In our meta-analysis, localization failure was observed in 6 patients in the CT-guided group due to deviation of the hook-wire position. ENB-guided localization is also reportedly safe and successful in localizing small lung lesions.[19,23] Makris et al[23] reported location success rates of 98% for ENB localization of pulmonary lesions. In our study, only 1 patient in the ENB group experienced pneumothorax, leading to localization failure.

Complications such as pneumothorax remain the major concern in pulmonary nodule localization. The rate of pneumothorax associated with the transthoracic procedure was 15% to 30%.[8,10,44,45] Pneumothorax induced by pleural puncture is a major disadvantage of the percutaneous approach, which may lead to localization failure of multiple lesions. In our study, 16.5% of patients who underwent CT-guided localization developed a pneumothorax, but none required chest tube placement. The pneumothorax incidence (1.3%) was significantly lower in the ENB-guided group than in the CT-guided group. The pneumothorax risk is reportedly correlated with the localization method and the lung condition of the patients.[32] Furthermore, it offers improved patient comfort since it is performed under general anesthesia, and there is no need for patients to change settings between localization and surgery, thus minimizing the risk and duration of the procedure. However, the disadvantages of navigational tools are low cost-effectiveness, labor and experience requirements, and resource consumption. Since ENB has been associated with a lower incidence of pneumothorax, it is recommended for patients with chronic obstructive pulmonary disease or emphysematous lung disease.[46,47]

The localization time was also a secondary outcome of this study. ENB-guided localization can be performed in the OR before surgery[33,48,49] and helps reduce patient tension associated with invasive procedures. However, it is a newer method that requires training and specialized equipment.[18] CT-guided localization is an accurate, widely available, and reproducible technique. CT-guided technology can be performed by most chest radiologists and was deemed more practical. Our analysis showed no significant difference in localization time between the 2 groups.

5. Limitations

There were certain limitations in this meta-analysis. First, all studies included were retrospective cohort studies since no randomized controlled trials studies have been conducted. Second, it was difficult to assess for selection bias in studies, as it was unclear if study patients were representative of the patients undergoing ENB-guided or CT-guided localization in clinical practice, although we collected as many articles as possible that met the inclusion and exclusion criteria. Third, the Q test and I2 statistic were used to test and quantify heterogeneity among studies. However, in the case of a small number of studies, the power of the Q test is low, which decreases the strength of our findings to a certain extent. Finally, the propensity matching process was only conducted in 2 studies to minimize bias. Parameters affecting the localization success rate, pneumothorax incidence, and localization time, such as tumor operator experience, tumor depth, and tumor size, were not considered. Indeed, publication bias could have led to an overestimation of the localization success rate, pneumothorax incidence, and localization time. Accordingly, more randomized controlled trials with larger samples are necessary to provide a more high-quality research base for the secondary evaluation.

6. Conclusion

Our meta-analysis demonstrated that both ENB and CT-guided are valuable technologies in localizing lung nodules before VATS based on current investigations. ENB achieved a lower pneumothorax rate than the CT-guided group. In our opinion, there is no perfect method, and decision-making should be given the actual circumstances of each institute. Future prospective studies in the form of large-scale randomized control trials are needed to confirm their clinical value.

Author contributions

Conceptualization: Yan Tan, Qifeng Jing.

Data curation: Yan Tan, Shuijun Shen, Canyun Wang, Qiaojuan Zhou, Qifeng Jing.

Formal analysis: Yan Tan, Shuijun Shen, Canyun Wang, Qifeng Jing.

Writing—original draft: Yan Tan, Canyun Wang, Qifeng Jing.

Methodology: Shuijun Shen, Canyun Wang.

Investigation: Qiaojuan Zhou.

Supervision: Qiaojuan Zhou.

Supplementary Material

Abbreviations:

95% CI 95% confidence interval

CT computed tomography

ENB electromagnetic navigation bronchoscopy

NOS Newcastle–Ottawa Scale

PRISMA Preferred Reporting Items for Systematic Reviews and Meta-Analyses

VATS video-assisted thoracic surgery

The authors have no funding and conflicts of interest to disclose.

All data generated or analyzed during this study are included in this published article [and its supplementary information files].

Supplemental Digital Content is available for this article.

How to cite this article: Tan Y, Shen S, Wang C, Zhou Q, Jing Q. Comparison of electromagnetic navigation bronchoscopy localization and CT-guided percutaneous localization in resection of lung nodules: A protocol for systematic review and meta-analysis. Medicine 2024;103:38(e39760).

This manuscript was previously posted to Research Square as a preprint: doi: https://doi.org/10.21203/rs.3.rs-2069587/v1.
==== Refs
References

[1] National Lung Screening Trial Research Team. Lung cancer incidence and mortality with extended follow-up in the national lung screening trial. J Thorac Oncol. 2019;14 :1732–42.31260833
[2] de Koning HJ van der Aalst CM de Jong PA . Reduced lung-cancer mortality with volume CT screening in a randomized trial. N Engl J Med. 2020;382 :503–13.31995683
[3] Patel VK Naik SK Naidich DP . A practical algorithmic approach to the diagnosis and management of solitary pulmonary nodules: part 2: pretest probability and algorithm. Chest. 2013;143 :840–6.23460161
[4] Callister ME Baldwin DR Akram AR . British Thoracic Society Pulmonary Nodule Guideline Development Group. British Thoracic Society guidelines for the investigation and management of pulmonary nodules. Thorax. 2015;70 (Suppl 2 ):ii1–54.26082159
[5] Naidich DP Bankier AA MacMahon H . Recommendations for the management of subsolid pulmonary nodules detected at CT: a statement from the Fleischner Society. Radiology. 2013;266 :304–17.23070270
[6] Aberle DR Adams AM Berg CD . National Lung Screening Trial Research Team. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med. 2011;365 :395–409.21714641
[7] Saito H Minamiya Y Matsuzaki I . Indication for preoperative localization of small peripheral pulmonary nodules in thoracoscopic surgery. J Thorac Cardiovasc Surg. 2002;124 :1198–202.12447187
[8] Chen S Zhou J Zhang J . Video-assisted thoracoscopic solitary pulmonary nodule resection after CT-guided hookwire localization: 43 cases report and literature review. Surg Endosc. 2011;25 :1723–9.21181200
[9] Kastl S Langwieler TE Krupski-Berdien G Demir E Izbicki JR . Percutaneous localization of pulmonary nodules prior to thoracoscopic surgery by CT-guided hook-wire. Anticancer Res. 2006;26 :3123–6.16886644
[10] Pittet O Christodoulou M Pezzetta E Schmidt S Schnyder P Ris HB . Video-assisted thoracoscopic resection of a small pulmonary nodule after computed tomography-guided localization with a hook-wire system. Experience in 45 consecutive patients. World J Surg. 2007;31 :575–8.17318707
[11] Chen YR Yeow KM Lee JY . CT-guided hook wire localization of subpleural lung lesions for video-assisted thoracoscopic surgery (VATS). J Formos Med Assoc. 2007;106 :911–8.18063512
[12] Davini F Gonfiotti A Vaggelli L De Francisci A Gigli P Janni A . Thoracoscopic localization techniques for patients with solitary pulmonary nodule: radioguided surgery versus hookwire localization. J Cardiovasc Surg (Torino). 2006;47 :355–9.
[13] Thaete FL Peterson MS Plunkett MB Ferson PF Keenan RJ Landreneau RJ . Computed tomography-guided wire localization of pulmonary lesions before thoracoscopic resection: results in 101 cases. J Thorac Imaging. 1999;14 :90–8.10210479
[14] Park CH Han K Hur J . Comparative effectiveness and safety of preoperative lung localization for pulmonary nodules: a systematic review and meta-analysis. Chest. 2017;151 :316–28.27717643
[15] Sakiyama S Kondo K Matsuoka H . Fatal air embolism during computed tomography-guided pulmonary marking with a hook-type marker. J Thorac Cardiovasc Surg. 2003;126 :1207–9.14566279
[16] Horan TA Pinheiro PM Araújo LM Santiago FF Rodrigues MR . Massive gas embolism during pulmonary nodule hook wire localization. Ann Thorac Surg. 2002;73 :1647–9.12022575
[17] Yi JH Choi PJ Bang JH Jeong SS Cho JH . Systemic air embolism after computed tomography-guided hook wire localization: two case reports and literature review. J Thorac Dis. 2018;10 :E59–64.29600106
[18] Schwarz Y Greif J Becker HD Ernst A Mehta A . Real-time electromagnetic navigation bronchoscopy to peripheral lung lesions using overlaid CT images: the first human study. Chest. 2006;129 :988–94.16608948
[19] Leong S Ju H Marshall H . Electromagnetic navigation bronchoscopy: a descriptive analysis. J Thorac Dis. 2012;4 :173–85.22833823
[20] Awais O Reidy MR Mehta K . Electromagnetic navigation bronchoscopy-guided dye marking for thoracoscopic resection of pulmonary nodules. Ann Thorac Surg. 2016;102 :223–9.27157054
[21] Bolton WD Howe H 3rd Stephenson JE . The utility of electromagnetic navigational bronchoscopy as a localization tool for robotic resection of small pulmonary nodules. Ann Thorac Surg. 2014;98 :471–5; discussion 475.24968769
[22] Krimsky WS Minnich DJ Cattaneo SM . Thoracoscopic detection of occult indeterminate pulmonary nodules using bronchoscopic pleural dye marking. J Community Hosp Intern Med Perspect. 2014;4 .
[23] Makris D Scherpereel A Leroy S . Electromagnetic navigation diagnostic bronchoscopy for small peripheral lung lesions. Eur Respir J. 2007;29 :1187–92.17360724
[24] Saito Y . Recent advances in electromagnetic navigation bronchoscopy for localization of peripheral pulmonary nodules. J Thorac Dis. 2022;14 :802–4.35572872
[25] Page MJ McKenzie JE Bossuyt PM . The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Syst Rev. 2021;10 :89.33781348
[26] Stang A . Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25 :603–5.20652370
[27] Higgins JP Thompson SG Deeks JJ Altman DG . Measuring inconsistency in meta-analyses. BMJ. 2003;327 :557–60.12958120
[28] Ioannidis JP Patsopoulos NA Evangelou E . Uncertainty in heterogeneity estimates in meta-analyses. BMJ. 2007;335 :914–6.17974687
[29] Yang YL Li ZZ Huang WC . Electromagnetic navigation bronchoscopic localization versus percutaneous CT-guided localization for thoracoscopic resection of small pulmonary nodules. Thorac Cancer. 2021;12 :468–74.33398925
[30] Hung CT Chen CK Chang YY . Electromagnetic navigation-guided versus computed tomography-guided percutaneous localization of small lung nodules before uniportal video-assisted thoracoscopic surgery: a propensity score-matched analysis. Eur J Cardiothorac Surg. 2020;58 (Suppl_1 ):i85–91.32105307
[31] Tian Y Wang C Yue W Lu M Tian H . Comparison of computed tomographic imaging-guided hook wire localization and electromagnetic navigation bronchoscope localization in the resection of pulmonary nodules: a retrospective cohort study. Sci Rep. 2020;10 :21459.33293605
[32] Kuo SW Tseng YF Dai KY Chang YC Chen KC Lee JM . Electromagnetic navigation bronchoscopy localization versus percutaneous CT-guided localization for lung resection via video-assisted thoracoscopic surgery: a propensity-matched study. J Clin Med. 2019;8 :379.30889927
[33] Bolton WD Cochran T Ben-Or S . Electromagnetic navigational bronchoscopy reduces the time required for localization and resection of lung nodules. Innovations. 2017;12 :333–7.28777130
[34] Plunkett MB Peterson MS Landreneau RJ Ferson PF Posner MC . Peripheral pulmonary nodules: preoperative percutaneous needle localization with CT guidance. Radiology. 1992;185 :274–6.1523323
[35] Lee NK Park CM Kang CH . CT-guided percutaneous transthoracic localization of pulmonary nodules prior to video-assisted thoracoscopic surgery using barium suspension. Korean J Radiol. 2012;13 :694–701.23118567
[36] Bellomi M Veronesi G Trifirò G . Computed tomography-guided preoperative radiotracer localization of nonpalpable lung nodules. Ann Thorac Surg. 2010;90 :1759–64.21095303
[37] Kondo R Yoshida K Hamanaka K . Intraoperative ultrasonographic localization of pulmonary ground-glass opacities. J Thorac Cardiovasc Surg. 2009;138 :837–42.19660350
[38] Doo KW Yong HS Kim HK Kim S Kang EY Choi YH . Needlescopic resection of small and superficial pulmonary nodule after computed tomographic fluoroscopy-guided dual localization with radiotracer and hookwire. Ann Surg Oncol. 2015;22 :331–7.25008029
[39] Ichinose J Kohno T Fujimori S Harano T Suzuki S . Efficacy and complications of computed tomography-guided hook wire localization. Ann Thorac Surg. 2013;96 :1203–8.23895891
[40] Hu L Gao J Chen C Zhi X Liu H Hong N . Comparison between the application of microcoil and hookwire for localizing pulmonary nodules. Eur Radiol. 2019;29 :4036–43.30631924
[41] Cornella KN Repper DC Palafox BA . A surgeon’s guide for various lung nodule localization techniques and the newest technologies. Innovations (Phila). 2021;16 :26–33.33124923
[42] Liu B Gu C . Expert consensus workshop report: guidelines for preoperative assisted localization of small pulmonary nodules. J Cancer Res Ther. 2020;16 :967–73.33004736
[43] Zaman M Bilal H Woo CY Tang A . In patients undergoing video-assisted thoracoscopic surgery excision, what is the best way to locate a subcentimetre solitary pulmonary nodule in order to achieve successful excision? Interact Cardiovasc Thorac Surg. 2012;15 :266–72.22572410
[44] Zhang Z Liao Y Ai B Liu C . Methylene blue staining: a new technique for identifying intersegmental planes in anatomic segmentectomy. Ann Thorac Surg. 2015;99 :238–42.25440279
[45] Lin MW Tseng YH Lee YF . Computed tomography-guided patent blue vital dye localization of pulmonary nodules in uniportal thoracoscopy. J Thorac Cardiovasc Surg. 2016;152 :535–44.e2.27189890
[46] Eberhardt R Morgan RK Ernst A Beyer T Herth FJ . Comparison of suction catheter versus forceps biopsy for sampling of solitary pulmonary nodules guided by electromagnetic navigational bronchoscopy. Respiration. 2010;79 :54–60.19648733
[47] Gex G Pralong JA Combescure C Seijo L Rochat T Soccal PM . Diagnostic yield and safety of electromagnetic navigation bronchoscopy for lung nodules: a systematic review and meta-analysis. Respiration. 2014;87 :165–76.24401166
[48] Abbas A Kadakia S Ambur V Muro K Kaiser L . Intraoperative electromagnetic navigational bronchoscopic localization of small, deep, or subsolid pulmonary nodules. J Thorac Cardiovasc Surg. 2017;153 :1581–90.28314525
[49] Geraci TC Ferrari-Light D Kent A . Technique, outcomes with navigational bronchoscopy using indocyanine green for robotic segmentectomy. Ann Thorac Surg. 2019;108 :363–9.30980818
