Uniportal video-assisted thoracic surgery resection of subsolid or millimetric nodules using an innovative micro-coil technique: our experience

Introduction

Uniportal video-assisted thoracic surgery (U-VATS) technique provides advantages in terms of lower postoperative pain and morbidity compared to multiportal video-assisted thoracic surgery (VATS) (1). However, every so often it can be very hard to pinpoint subsolid, small or deep nodules with a mininvasive approach and the rate of conversion for subcentimetric nodules can reach up to 65% (2).

Ground-glass opacity (GGO) is defined as a hazy grey opacity with an area of increased attenuation that does not obscure the underlying bronchial structures or pulmonary vessels on high-resolution computed tomography (HRCT) imaging (3). The detection of GGOs and indeterminate nodules has become more frequent since the increased use of HRCT of the chest and the implementation of lung cancer screening programs [low-dose computed tomography (CT) scan]. GGOs can represent benign, pre-cancerous or cancerous lesions and usually CT alone is not adequate to address their proper nature. In addition, the subsolid nature of these lesions reduces also the diagnostic accuracy of bronchoscopy and image-guided biopsy realized preoperatively to identify the presence of neoplastic cells (4) or, what’s more in evaluating the grade of invasively of the heteroformation has been determine by adenocarcinoma classification (5). Therefore, the high false negative rates and the low diagnostic accuracy of non-invasive biopsies frequently make the surgical excision necessary in this type of lesions.

Furthermore, the role of lobectomy in this scenario is still debate as some authors believe that wedge resection or segmentectomy could be more indicated for these small and indolent-growth lesions (6,7). On the other hand, limited resection for GGOs and subcentimetric deep nodules with U-VATS technique can be very challenging without preliminary localization of the lesion. In this scenario, preoperative localization with fiducials can be an appropriate method for assisting VATS in patients with unpalpable nodules (8-10).

This study aims to present and evaluate our experience with U-VATS resections following preoperative cone beam CT (CBCT)-guided micro-coil placement in the lung parenchyma near GGOs and small lesions, focusing on safety and effectiveness. Additionally, it seeks to identify potential factors that may predict coil-assisted U-VATS failures. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-628/rc).

Methods

The clinical, radiological, and surgical data of 117 patients who underwent U-VATS resection following CBCT-guided micro-coil localization of GGOs and small deep nodules between January 2017 and February 2023 were retrospectively analyzed. The inclusion criteria based on CT scan characteristics were as follows:

• Pure GGO or lesions with minimal solid components and a maximum long axis diameter of less than 30 mm;
• Newly appeared subcentimetric lesions, and
• Lesions located more than 5 mm away from the visceral pleura.

Surgical indications included:

• Nodule enlargement;
• Persistence of a nodule with a solid component of 5 mm or greater at CT follow-up;
• Newly appeared nodules during oncological follow-up, or
• A positive history of multifocal tumors.

Each case was evaluated by two expert thoracic surgeons (S.M. and M.T.C.) if it was anticipated that the nodules would not be visible intraoperatively during VATS, along with an interventional chest radiologist (R.I.) with over 10 years of experience in pulmonary procedures, to determine the feasibility of micro-coil placement before U-VATS resection. The main contraindications for micro-coil localization included:

• Previous chemical pleurodesis;
• Nodules located near hilar structures, and
• Severe bullous disease, which increased the risk of pneumothorax.

Characteristics of micro-coil

The micro-coils (Nester Embolization Coils, COOK MEDICAL LLC, Bloomington, USA) used for pulmonary localization are platinum wires for vessel embolization in vascular intervention surgery.

They main advantages of these micro-coils are:

• The coils are commonly used, easy to acquire and inexpensive.
• The platinum wire is a clinically proven material that can be retained in the human body safely for a long time and it is radiopaque.

After implantation in lung parenchyma, the coil provides the lung with a certain degree of hardness.

• The helicoidal shape permits elasticity for breathing and in case of pneumothorax.
• Fuzzy synthetic thrombogenic fibers totally cover the coils promoting clot formation and avoiding parenchymal hemorrhage during the positioning procedure.
• The positioning is uncomplicated and has good repeatability.

Radiological technique

All the CBCT-guided micro-coil placement procedures were performed during the 24 hours before surgery in an angiographic suite under local anesthesia using fluoroscopy and image guidance software (Integris Allura FD 20, Philips Medical Systems, Best, The Netherlands). In particular, if the surgery was performed in the afternoon, the localization by micro-coil was performed during the morning of the same day. In case of surgery was planned as the first in the morning, the micro-coil was placed in the afternoon of the day before. All the micro-coil placement were performed by a total of three operators: R1 and R2 with more than 10 years of experience in pulmonary procedures, and R3 with 5 years of experience. Patient monitoring and anesthesiologist assistance were routinely performed.

In detail, once the patient was positioned on the angiographic table in an appropriate position (either supine or prone depending on the location of the lesion), a CBCT scan was performed to identify the location of the nodule and plan the access route. This planning also took into account the surgical approach and determined the transpulmonary needle path, which was visible on the fluoroscopy monitor to guide the interventional radiologist. The distance between the nodule and the nearest pleural surface was also measured (Figure 1). After sterilizing the skin around the puncture site and administering local anesthesia (2% mepivacaine), an 18-gauge percutaneous needle (150 mm in length) was inserted under fluoroscopic guidance, based on the CBCT plan. Once the needle tip was confirmed to be within the nodule, the stylet was removed, and a micro-coil was deployed using a hydrophilic guidewire. The micro-coil was positioned beneath the nodule, extending partially along the transpulmonary path towards the pleural space, with its distal end left above the visceral pleura to guide the surgeon (Figure 2). After needle removal, another CBCT scan was taken to confirm the correct deployment of the micro-coil, verify its final position, and check for any complications such as pneumothorax or intraparenchymal hemorrhage.

Figure 1 Fluoroscopy and detection of the nearest distance from the pleura.

Figure 2 CBCT appearance of the nodule and the coil. CBCT, cone beam computed tomography.

Surgical technique

The procedure was carried out under general anesthesia, using a left double-lumen endotracheal tube. The patient was positioned laterally, with the operating table flexed and a rolled blanket placed under the thorax, while the arms were extended toward the head. The surgeon and assistants stood on the ventral side of the surgical table, facing the patient, and shared the same screen to maintain synchronized movements. A single intercostal incision of 2–3 cm was made between the 4th and 5th intercostal spaces, depending on the lesion’s location to ensure optimal exposure and management. A wound protector was utilized to create more space for instruments, reduce camera soiling, and minimize the risk of wound contamination or infection. A 10 mm/30° thoracoscope was inserted through the upper part of the incision. Once inside the chest cavity, the surgeon immediately visualized the distal end of the micro-coil on the visceral pleural surface (Figure 3).

Figure 3 Intraoperative appearance of the coil.

A wedge resection, including the coil-marked nodule, was performed using an endo-stapler, ensuring clear margins. One benefit of this technique is that the surgeon can accurately assess the distance from the coil tail on the pleural surface to the stapler line, as measured by the CBCT (from the coil tail on the visceral pleura to the deeper part of the localizer beneath the lesion). If needed, palpation could be done to confirm the micro-coil’s presence in the specimen and to ensure clear margins.

Typically, the lesion was first removed via thoracoscopic wedge resection, and the resected specimen was sent for immediate frozen section analysis. The placement of the micro-coil just below the lesion ensured that the nodule remained intact for pathological examination. If the pathology indicated a benign lesion or sub-centimetric carcinoma with safe margins, the wedge resection was considered final, and the chest was closed, with a chest tube inserted through the same incision. In cases of minimally invasive adenocarcinomas, additional lymph node sampling was conducted. However, if the pathology revealed invasive carcinoma, an anatomical resection (segmentectomy or lobectomy with lymph node dissection) followed the initial wedge resection. For patients with prior contralateral lobectomy, compromised respiratory function, or multifocal tumors, only wedge resection was performed to prevent further functional impairment.

Pathology

For the histological diagnosis of GGOs, pathologists adhered to the classification system provided by the International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society International Multidisciplinary Classification of Lung Adenocarcinoma (11). Lung carcinomas were categorized as preinvasive lesions [including atypical adenomatous hyperplasia (AAH) and adenocarcinoma in situ (AIS)], minimally invasive adenocarcinoma (MIA), and invasive adenocarcinoma (IA). For diagnosing other nodules, the pathologists followed the most recent version of relevant guidelines.

Statistical analysis

Statistical analysis was performed using PASW Statistics for Windows, Version 18.0 (SPSS Inc., Chicago, IL, USA). Continuous variables were expressed as mean ± standard deviation (SD). Categorical variables were reported as n (%).

Ethical statement

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The approval of “Comitato Etico Territoriale Lazio Area 3 – Fondazione Policlinico Universitario “A. Gemelli” IRCCS – Università Cattolica del Sacro Cuore” Ethical Committee was not necessary because this is a retrospective study that did not change the routine clinical treatment of patients. Informed consent was obtained from all the patients.

Results

All 117 patients were asymptomatic, with the nodules being incidentally detected during chest CT scans conducted for other purposes, or as part of screening programs or oncological surveillance. The group consisted of 58 males (49.5%) and 59 females (50.5%), with a mean age of 65.5±11.7 years. Among them, 51 patients (43.6%) were former smokers, while 29 (24.8%) were current smokers. The lesions were distributed as follows: right upper lobe (n=48; 41%), left upper lobe (n=29; 24.8%), right lower lobe (n=18; 15.4%), left lower lobe (n=17; 14.5%), and middle lobe (n=5; 4.3%). Additionally, 29 patients (24.8%) had a history of previous malignancies.

Radiological characteristics

Among the 117 resected lesions, there were 68 (58.1%) GGOs and 49 (41.9%) small or deep nodules. The mean diameter of all 117 lesions was 11.89±5.81 mm. Fifty-four patients (46.1%) underwent PET scan before the procedure, positive in 32/54 (59.3%), with mean SUV of 4.2±2.4. All 117 (technical success: 100%) subjects underwent CBCT-guided localization of the nodule by micro-coils placement close to the lesions (Figures 2,3).

The mean distance from the lesion to the parietal pleural surface was 18.60±12.48 mm. The mean length of the needle pathway was 68.7±10.78 mm. The mean time taken for the procedure was 28±14 minutes.

Surgery

One hundred and eight (92.3%) coil-labeled lesions were identified and removed by U-VATS (on a meantime of 32±15 min) with no conversion to thoracotomy, while 9/117 (7.7%) required conversion because of micro-coil displacement. Wedge resection was performed in 80 patients (68.4%), while 31 (26.5%) underwent segmentectomy and 6 (5.1%) underwent lobectomy. Forty-four patients (37.6%) had lymphadenectomy, and the average number of lymph nodes removed was 6.8±5.4. Complications during VATS occurred in 12 patients (10.2%) (Table 1). The mean hospitalization time after VATS was 5.00±4.10 days and three patients (2.6%) were discharged with pleural drainage. Three patients (2.6%) had hemothorax, two requiring re-intervention for hemostasis revision.

Procedural complications

Complications occurred in 32 (27.4%) patients (Table 2), mostly represented by slight pneumothorax (24/32, 75%) <2 cm in the maximum distance, not requiring a chest drain, detected at the CT at the end of the procedure to verify the coil right position. Only 2 (1.7%) patients required chest tube for pneumothorax.

In four cases the control scan showed perilesional bleeding, in all cases it was possible to identify the nodule in the new patchy ground glass density shadow. In two cases a pleural drainage for pneumothorax was necessary for pain and respiratory distress: two cases of vagal reaction and one of subcutaneous emphysema only in supraclavicular area not requiring cutaneous incisions. In one case the coil was retained into the chest wall because it did not reach the pleural cavity (Figure 4).

Figure 4 Coil retained into the chest wall (red arrow).

Pathology

Ninety-seven (82.9%) lesions were malignant. The final pathological characteristics of nodules are described in Table 3. All the specimen showed a radical resection, with free margins (R0).

Potential factors for failure

We analyzed the subgroup of unsuccessful coils, with the aim to identify potential factors related to failure (Table 4).

We evaluated procedure distribution in three different periods: preliminary previous published experience (2017–2018—group 1), intermediate period (2019–2020—group 2), last period (2021–2023—group 3). We reported 0 dislocation in group 1 (0/21, 0%), 6 in group 2 (6/33; 18.2%), and 3 in the group 3 (3/63, 4.8%).

Indeed, when we analyzed the procedures related to the expertise of the operator, we found that only one of the failed coil placements was done by the first operator (R1: 1/9, 11%), 3 by R2, and 5 by R3 (R2 + R3: 8/9, 89%). In detail, the technique was developed by R1 together with the thoracic surgical staff; R1 performed all the procedures in the first phase of enrollment [2017–2018] and 43 out of 96 of the procedures in group 2 (20/33) and group 3 (23/63). R2 (well experienced in pulmonary procedures) and R3 (less experienced operator) performed a total of 28 (7 in group 2 and 21 in group 3) and 25 (6 in group 2 and 19 in group 3), respectively. When combining operators and period groups, it was obtained that 0 and 1 (R1), 2 and 1 (R2), and 4 and 1 (R3) coil displacements were registered in groups 1, 2, and 3, respectively.

Regarding the possibility that the depth of the nodule could influence the success of the procedure, it seems that, in the dislocation subgroup, more the nodule is far from the pleural surface more the risk of failure decreases (22% for nodule deeper than 10 mm versus 78% for distance ranging from 5 to 10 mm). The decubitus of the patient seems to influence the outcome of the procedure: patients in supine decubitus (3 dislocated coils in supine position and 6 in lateral decubitus).

Discussion

The extensive application of multi-detector CT scans for lung cancer screening or monitoring has led to an increase in the identification of GGOs and small uncertain nodules. Clinical guidelines for the removal of GGOs are relatively common and diverse. For example, at our center, patients with new lung nodules and a previous or coexisting malignancy, are discussed in a dedicated multidisciplinary board, and, in the suspect of a primary or secondary lesion, or if the growth of a pre-existing lung nodule is observed in an oncologic patient, the surgical removal of the lesion is recommended. The rationale is to address the patient to the less invasive and definitive possible procedure thanks to a minimally invasive approach and a lung-sparing resection. Nowadays, a mini-invasive approach with lung-sparing techniques is preferable for patients with small nodules or pre-invasive adenocarcinoma, considering the very high oncological outcome, to permit fast recovery and preserve lung functionality (12). However, pure GGOs, with a diameter <10 mm, are usually difficult to be detected either for the surgeon by VATS without a preprocedural localization, or for the pathologists in the frozen sections. Millimetric solid nodules and GGOs are not visible during pleural inspection and are difficult to palpate in minimally invasive surgery, especially in lungs affected by hyperinflation and emphysema. In this scenario, a pre-procedural localization of the lesion can prevent a conversion from VATS to thoracotomy, as reported by Suzuki (2). The Author evaluated the probability of failure to detect the lesions in biportal VATS based on two parameters, the tumor size and the distance to the pleural surface. In both patients whose lesions were lower than 10 mm in diameter, and the distance to the pleural surface was greater than 10 mm, the lesions were not detected. Instead, when the distance to the pleural surface was greater than 5 mm in cases of lesions of less than 10 mm in size, the probability of failure to detect the nodule was 63%.

At the Thoracic Surgery Department of Fondazione Policlinico Universitario “Agostino Gemelli” IRCCS, since May 2016, U-VATS has supplanted both open surgery and triportal VATS for nearly all surgical procedures, including major anatomical lung resections (13,14). U-VATS enables pulmonary resections through a 3 cm incision, and if the lesion proves invasive during a frozen section analysis, lobectomy or segmentectomy can be carried out using the same approach. Various techniques have been reported for facilitating VATS resections of pulmonary nodules during the last decades. Intraoperative imaging techniques include ultrasonography (15), CT-fluoroscopy (16,17), electromagnetic navigation bronchoscopy (18), and combined techniques in hybrid theatre (19), but the limit of these procedures is the necessity of special equipment and professional training. Other authors proposed a lot of techniques including pre-operative injection of drugs, dyes (20), radionuclides (21), and contrast medium injection (Lipiodol, Barium) (22,23). There are a lot of disadvantages for these procedures such as the necessity (I) to perform surgery immediately after the localization procedure; (II) color might be difficult to be visualized in patients with silicosis; (III) the use of contrast medium (e.g., barium) could influence the final diagnosis because it induces inflammatory modifications in the lung parenchyma; and (IV) lipiodol requires the use of fluoroscopy to be localized into the lung parenchyma. In a recent review, Park compared the success and complication rates associated with hookwire, micro-coil, and Lipiodol localization before VATS (24): even if all the methods had successful targeting rates, micro-coil localization showed the lowest complication rates in respect to hookwires and Lipiodol. Along with the application of various localization methods and the increased operators’ experience, more reports have admitted progressively that physical methods, such as hookwire or micro-coils localization, showed excellent superiority compared with other localization techniques (25,26). Among mechanical methods, the dislodgement of hookwires occurs more frequently during lung manipulation in VATS surgery (25), compared to CT-guided coil. Micro-coils are meant for vessels embolization but have some advantages for being used for localization purposes: they are ordinarily used in interventional radiology, easy to acquire, low-priced compared to other fiducials such as radionuclide (27), also relatively easy to release under CBCT guidance. Micro-coils can be safely remain in the human body for days, are radiopaque, and can be identified like a certain degree of denseness in the lung parenchyma; all these three aspects can help surgeons in finding their position by visual inspection, digital palpation, and, if required, fluoroscopy. Moreover, the presence of a thrombogenic coat on the platinum wire avoids the hemorrhage around the nodule which can compromise the histological evaluation by the pathologist.

At the beginning of our experience with U-VATS, we put a micro-coil into the nodule, with the aim to make it more “solid”, taking inspiration from the procedure described by Asamura (28) in 1994; the author first reported the use of a platinum microcoil placed into the nodule for a small pulmonary lesion in one case. Resection was performed by triportal VATS with the use of fluoroscopy to identify the position of micro-coil in the lung.

However, this technique had two great limits: the complete disruption of the specimen by the coil inside the nodule which makes very hard or sometimes invaluable the frozen section and the necessity to enlarge the incision to 4–5 cm, in order to give the possibility to locate with the finger the invisible coil on the pleural surface.

We previously described our initial experience with this technique (29); we treated 30 patients with GGO localized using a platinum coil placed with the distal tail beyond the visceral pleura surface and with the proximal end immediately beneath or very close to the nodule. All the CT-localization procedures have been concluded successfully, and the nodules identified and resected through U-VATS.

In the present study, micro-coil localization technique was similar to that described by Sui et al. (30) who modified the Asamura’s technique and proposed to leave the proximal end of the micro-coil on the visceral pleura; unlike Sui, who performed conventional triportal thoracoscopy with fluoroscopy used to confirm the integrity of the coil, we did not use fluoroscopy because, according to our technique, the distal part of the coil was left on the surface of the visceral pleural for allowing its identification by only visual inspection. As explained before, palpation is not mandatory to perform a wedge resection of free margins, although feasible in case of necessity. Therefore, there was no requirement for the involvement of additional facilities such as a fluoroscopy, also preserving surgeons from receiving any radiation exposure, since the extremity of the coil is immediately visible on the pleural surface. At the same time, the nodule is totally intact, and pathologic specimen of the resected nodule showed the micro-coil rolled on the pleural surface and extending beneath the semisolid nodule; in particular, the advantage for pathologist is the absence of parenchymal hemorrhage in the specimen due to the thrombogenic fuzz on the fiber-coat micro-coil.

Furthermore, unlike the other available techniques, all the nodules were resected without the use of fluoroscopy. According to this technique, the micro-coil is immediately identified by visual inspection alone during U-VATS. This method resulted in only 8 cases (6.84%) of conversion to thoracotomy due to coil dislodgement.

We also analyzed the subgroup of unsuccessful coil placement, with the aim to identify potential factors related to failure (Table 4).

In the previous work, all the procedures performed from 2017 to 2018 were successfully executed by the same interventional radiologist (who set up the procedure with thoracic staff in our hospital); subsequently, from 2019, he started a training program addressed to other 2 interventional radiologists, with less expertise at the time of the study, and this reason could explain the increase rate of coil displacement. In particular, based on operator and group distribution, a significant number of failures was registered in the first 5 procedures for the experienced interventional radiologist (R2) (2/5, 40% vs. 1/23, 4.3%), and the first 10 procedures for the younger interventional radiologist (R3) (5/10, 50% vs. 1/15, 6.7%). This number of procedures seems to be considered an adequate threshold to overcome the learning curve to make the procedure safer and more effective regardless the operator’s expertise and skill.

Regarding the distance of the coil from the pleural surface, the lower risk of dislocation in the deeper nodules is probably due to the ability of the fiber coat to hook up into the lung when the distance is longer because the fibers on the coil surface create a friction force that fixes the micro-coil in the lung parenchyma (31,32).

The decubitus of the patient seems also to influence the outcome of the procedure: patients in supine decubitus during the coil positioning are more stable than those in lateral position and this prevents small movements in particular when the micro-coil was pushed into the needle.

A recent experience (33) confirmed our results reporting differences between intra-cavity (coil tail was located in the pleural cavity) and extra-cavity (coil tail was located outside the pleural cavity and in the soft tissue of chest wall) groups in terms of complications and success rates during VATS, with lower rates of complications and conversion in the intracavitary group.

The present study has some limitations: the retrospective nature (I) in a single center experience exposes results to potential bias related to patients’ selection; moreover, this study does not compare (II) preoperative micro-coils localization outcomes with other preoperative localization techniques; finally, all the localization procedures were performed by different operators (III) but with very high level of expertise in the field.

Conclusions

Preoperative CT-guided micro-coil localization is a safe and not expensive procedure. It allows detection of GGOs, small or deep nodules in U-VATS with low rate of conversion to thoracotomy and few complications, without any use of intraoperatory radiations. Our results suggest that the CBCT-guided coil localization technique is effective and safe for localizing small pulmonary nodules and GGOs in VATS, reducing the rate of conversion if the procedure is performed by expert hands.

Multicenter randomized trials are required to compare the different methods of localization for GGOs and unpalpable nodules with the aim of identifying the most effective technique.

Acknowledgments

Funding: None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-628/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-628/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-628/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-628/coif). The authors have 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. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The approval of “Comitato Etico Territoriale Lazio Area 3 – Fondazione Policlinico Universitario “A. Gemelli” IRCCS – Università Cattolica del Sacro Cuore” Ethical Committee was not necessary because this is a retrospective study that did not change the routine clinical treatment of patients. Informed consent was obtained from all the patients.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

References

1. Harris CG, James RS, Tian DH, et al. Systematic review and meta-analysis of uniportal versus multiportal video-assisted thoracoscopic lobectomy for lung cancer. Ann Cardiothorac Surg 2016;5:76-84. [Crossref] [PubMed]
2. Suzuki K, Nagai K, Yoshida J, et al. Video-assisted thoracoscopic surgery for small indeterminate pulmonary nodules: indications for preoperative marking. Chest 1999;115:563-8. [Crossref] [PubMed]
3. Matsunaga T, Suzuki K, Takamochi K, et al. What is the radiological definition of part-solid tumour in lung cancer?. Eur J Cardiothorac Surg 2017;51:242-7. [Crossref] [PubMed]
4. Elicker BM, Kallianos KG. Biopsy of Subsolid Nodules Suspicious for Adenocarcinoma: Counterpoint-Biopsy Has Limited Utility in the Diagnostic Evaluation of Subsolid Nodules. AJR Am J Roentgenol 2021;217:815-6. [Crossref] [PubMed]
5. Ma Z, Han H, Cao H, et al. Pathological and radiological T descriptors in invasive lung adenocarcinoma: from correlations to prognostic significance. Transl Lung Cancer Res 2023;12:2181-92. [Crossref] [PubMed]
6. Zhang C, He Z, Cheng J, et al. Surgical Outcomes of Lobectomy Versus Limited Resection for Clinical Stage I Ground-Glass Opacity Lung Adenocarcinoma 2 Centimeters or Smaller. Clin Lung Cancer 2021;22:e160-8. [Crossref] [PubMed]
7. Saji H, Okada M, Tsuboi M, et al. Segmentectomy versus lobectomy in small-sized peripheral non-small-cell lung cancer (JCOG0802/WJOG4607L): a multicentre, open-label, phase 3, randomised, controlled, non-inferiority trial. Lancet 2022;399:1607-17. [Crossref] [PubMed]
8. Wang Y, Jing L, Liang C, et al. Comparison of the safety and effectiveness of the four-hook needle and hook wire for the preoperative positioning of localization ground glass nodules. J Cardiothorac Surg 2024;19:35. [Crossref] [PubMed]
9. Voulaz E, Giudici VM, Lanza E, et al. Percutaneous Computed Tomography (CT)-Guided Localization with Indocyanine Green for the Thoracoscopic Resection of Small Pulmonary Nodules. J Clin Med 2023;12:6149. [Crossref] [PubMed]
10. Shinohara Y, Oki M. Need for preoperative marking of pulmonary nodules and a more useful technique. J Thorac Dis 2023;15:1548-50. [Crossref] [PubMed]
11. Travis WD, Brambilla E, Noguchi M, et al. International association for the study of lung cancer/american thoracic society/european respiratory society international multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol 2011;6:244-85. [Crossref] [PubMed]
12. Zhang Y, Ma X, Shen X, et al. Surgery for pre- and minimally invasive lung adenocarcinoma. J Thorac Cardiovasc Surg 2022;163:456-64. [Crossref] [PubMed]
13. Nachira D, Meacci E, Petracca Ciavarella L, et al. Uniportal video-assisted thoracic surgery Roman experience-a report of the first 16-month Roman experience. J Thorac Dis 2018;10:S3678-85. [Crossref] [PubMed]
14. Meacci E, Nachira D, Zanfrini E, et al. Uniportal VATS approach to sub-lobar anatomic resections: literature review and personal experience. J Thorac Dis 2020;12:3376-89. [Crossref] [PubMed]
15. Huang YH, Chen KC, Chen JS. Ultrasound for intraoperative localization of lung nodules during thoracoscopic surgery. Ann Transl Med 2019;7:37. [Crossref] [PubMed]
16. Powell TI, Jangra D, Clifton JC, et al. Peripheral lung nodules: fluoroscopically guided video-assisted thoracoscopic resection after computed tomography-guided localization using platinum microcoils. Ann Surg 2004;240:481-8; discussion 488-9. [Crossref] [PubMed]
17. Toba H, Kondo K, Miyoshi T, et al. Fluoroscopy-assisted thoracoscopic resection after computed tomography-guided bronchoscopic metallic coil marking for small peripheral pulmonary lesions. Eur J Cardiothorac Surg 2013;44:e126-32. [Crossref] [PubMed]
18. Kuo SW, Tseng YF, Dai KY, et al. 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. [Crossref] [PubMed]
19. Yu H, Tian W, Sun Y, et al. Localization of small peripheral pulmonary nodules for surgical resection: a new intraoperative technique in hybrid operating room. J Cardiothorac Surg 2022;17:241. [Crossref] [PubMed]
20. Endo M, Kotani Y, Satouchi M, et al. CT fluoroscopy-guided bronchoscopic dye marking for resection of small peripheral pulmonary nodules. Chest 2004;125:1747-52. [Crossref] [PubMed]
21. Chella A, Lucchi M, Ambrogi MC, et al. A pilot study of the role of TC-99 radionuclide in localization of pulmonary nodular lesions for thoracoscopic resection. Eur J Cardiothorac Surg 2000;18:17-21. [Crossref] [PubMed]
22. Mogi A, Yajima T, Tomizawa K, et al. Video-Assisted Thoracoscopic Surgery after Preoperative CT-Guided Lipiodol Marking of Small or Impalpable Pulmonary Nodules. Ann Thorac Cardiovasc Surg 2015;21:435-9. [Crossref] [PubMed]
23. Lee NK, Park CM, Kang CH, et al. CT-guided percutaneous transthoracic localization of pulmonary nodules prior to video-assisted thoracoscopic surgery using barium suspension. Korean J Radiol 2012;13:694-701. [Crossref] [PubMed]
24. Park CH, Han K, Hur J, et al. Comparative Effectiveness and Safety of Preoperative Lung Localization for Pulmonary Nodules: A Systematic Review and Meta-analysis. Chest 2017;151:316-28. [Crossref] [PubMed]
25. Rostambeigi N, Scanlon P, Flanagan S, et al. CT Fluoroscopic-Guided Coil Localization of Lung Nodules prior to Video-Assisted Thoracoscopic Surgical Resection Reduces Complications Compared to Hook Wire Localization. J Vasc Interv Radiol 2019;30:453-9. [Crossref] [PubMed]
26. Park CH, Lee SM, Lee JW, et al. Hook-wire localization versus lipiodol localization for patients with pulmonary lesions having ground-glass opacity. J Thorac Cardiovasc Surg 2020;159:1571-1579.e2. [Crossref] [PubMed]
27. Galetta D, Bellomi M, Grana C, et al. Radio-Guided Localization and Resection of Small or Ill-Defined Pulmonary Lesions. Ann Thorac Surg 2015;100:1175-80. [Crossref] [PubMed]
28. Asamura H, Kondo H, Naruke T, et al. Computed tomography-guided coil injection and thoracoscopic pulmonary resection under roentgenographic fluoroscopy. Ann Thorac Surg 1994;58:1542-4. [Crossref] [PubMed]
29. Congedo MT, Iezzi R, Nachira D, et al. Uniportal VATS Coil-Assisted Resections for GGOs. J Oncol 2019;2019:5383086. [Crossref] [PubMed]
30. Sui X, Zhao H, Yang F, et al. Computed tomography guided microcoil localization for pulmonary small nodules and ground-glass opacity prior to thoracoscopic resection. J Thorac Dis 2015;7:1580-7. [Crossref] [PubMed]
31. Huang ZG, Wang CL, Sun HL, et al. CT-guided microcoil localization of pulmonary nodules: the effect of the position of microcoil proximal end on the incidence of microcoil dislocation. Br J Radiol 2022;95:20200381. [Crossref] [PubMed]
32. Xu Y, Ma L, Sun H, et al. CT-guided microcoil localization for pulmonary nodules before VATS: a retrospective evaluation of risk factors for pleural marking failure. Eur Radiol 2020;30:5674-83. [Crossref] [PubMed]
33. An J, Dong Y, Li Y, et al. CT-guided placement of microcoil end in the pleural cavity for video-assisted thoracic surgical resection of ground-glass opacity: a retrospective study. J Cardiothorac Surg 2022;17:316. [Crossref] [PubMed]