Artificial pleural effusion-assisted intraoperative ultrasound for the localization of pulmonary tumors during video-assisted thoracic surgery

Introduction

The World Health Organization estimated that lung cancer had the second highest incidence of tumors, with the highest mortality rate in the male population (1). With the development of minimally invasive techniques, video-assisted thoracic surgery (VATS) has become one of the main treatment modalities for pulmonary tumors compared with conventional open chest surgery, and one-lung ventilation (OLV) has been widely used in VATS (2-4). However, during VATS, surgeons do not have enough workspace to explore by digital palpation, so some lesions lack palpation feedback. Preoperative localization of the lesions is required, which is achieved by either the placement of metallic materials such as hook wire and spring coil, or injections of dyes such as methylene blue (5). Nonetheless, these localization techniques bear the risk of pneumothorax, pain, dye diffusion, displacement, and dislodgement of the localizers, all of which are impediments to implementation during surgery (6).

Intraoperative ultrasound (IOUS) has been widely used in endoscopic surgery because of its advantages of real-time, noninvasive, and accurate localization (7). Although OLV has been used in VATS, gas residue remains in some patients (e.g., those with chronic obstructive pulmonary disease) and causes image artifacts, which makes it more challenging to localize pulmonary nodules (PNs) with IOUS (8,9). To address this limitation, we found that artificial pleural effusion (APE) combined with OLV could not only better accelerate lung collapse, but also had a better acoustic window to obtain clearer sonograms. However, little is known about the feasibility of APE-assisted IOUS localization of PNs at present.

Therefore, we conducted a study to investigate the technical feasibility and performance of IOUS combined with APE for the localization of PNs in order to provide an accurate and rapid method to visualize PNs in VATS. We present this article in accordance with the STARD reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-663/rc).

Methods

Study design

The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Ethics Committee of Wuhan Jingyintan Hospital affiliated to Tongji Medical College of Huazhong University of Science and Technology and informed consent was provided by all individual participants. We included 16 PNs from 15 patients who underwent VATS between December 2023 and August 2024 at the Department of Thoracic Surgery, Jinyintan Hospital, Tongji Medical College, Huazhong University of Science and Technology.

The inclusion criteria were as follows: (I) PNs were diagnosed by preoperative computed tomography (CT); (II) tumor diameter was ≤3.0 cm; (III) the included PNs were peripheral lesions; (IV) cardiopulmonary function could tolerate surgical resection of lung lobes or segments; (V) did not receive preoperative puncture biopsy and localization.

Study hypothesis

APE-assisted IOUS during VATS could accurately localize PNs. The primary endpoint was the feasibility of APE-assisted with IOUS in VATS. The secondary endpoint was the accurate localization and characterization of PNs on IOUS.

The procedures of APE-assisted IOUS

Patients were placed in the lateral position, and the procedure was performed using a single-port thoracoscopic operation with general anesthesia in double-lumen endotracheal intubation. Fiberoptic bronchoscopy was performed to confirm the intubation position and ventilation of one side of the healthy lung. A 3–5 cm incision was made in the fifth intercostal space in the anterior axillary line and an incision retraction protector was placed.

The procedures for creating APE were as follows: 37 ℃ normal saline was injected through the incision retraction protector according to the preoperative prediction of the degree of desired lung atrophy and actual lung atrophy. Oval forceps were used to gently press the lobe to completely submerge the target lobe in normal saline and promote lung atrophy. The volume of APE and the time to localize the nodules by APE-assisted IOUS were recorded intraoperatively.

All examinations were performed using a Mindray M11 color Doppler ultrasound machine, equipped with a luminal LAP13-4Cs convex array probe (operating rod diameter 10 mm, length 338 mm, frequency 2.8–12.2 MHz) (Figure 1). The luminal convex array probe was used to move to the area of the pulmonary lobe where the lesion was located in the normal saline with the guidance of thoracoscopy. The probe did not directly touch the surface of the lobe, and real-time monitoring was implemented to assess the lung atrophy situation and explore the suspected lesions. After identifying the suspicious lesion, it was recorded using the gray-scale ultrasound and color Doppler flow imaging. We used an electric hook to cauterize the lung surface where the lesion was located. Pulmonary resection was performed using a laparoscopic articulating linear cutting stapler (Cartridge: GST60B). All examinations on APE-assisted IOUS were performed by an experienced radiologist with more than 15 years of experience, who worked under aseptic conditions in concert with the thoracic surgeon.

Figure 1 The LAP13-4Cs laparoscopic probe used during VATS. VATS, video-assisted thoracic surgery.

Statistical analysis

Continuous variables were expressed as mean ± standard deviation (SD) or the median (Q1, Q3). Categorical variables were expressed as numbers and percentages. Given the small sample size, Spearman’s correlation analysis was used to assess the correlation between the maximum diameter of pulmonary lesions on preoperative CT and on IOUS, and the Bland-Altman plot was used to analyze the consistency. All statistical analyses were performed using the software SPSS 25.0 (IBM Corp., Armonk, NY, USA) and GraphPad Prism version 10.1.2 (GraphPad Software, San Diego, CA, USA). The difference was considered statistically significant at P<0.05.

Results

The results of clinical features and APE-assisted IOUS

We included 16 nodules from 15 patients who underwent APE-assisted IOUS. The cases comprised 10 males (66.7%) and 5 females (33.3%). The average age of the patients was 53.20±9.64 years. According to the preoperative chest CT, the maximum diameter of the nodules was 1.60±0.63 cm, and the shortest distance from the pleura for the nodules was 1.49±0.71 cm. Only one of these patients had a history of previous resection of adenocarcinoma of the left upper lung.

Complete atrophy of the lungs was achieved in 14 of all included lesions (n=16) with the assistance of APE combined with OLV, and all lesions (n=16) were visualized on IOUS. After the completion of APE injection in the above 14 lesions, the lesions were determined within 3 minutes in 11 lesions and within 5 minutes in 2 lesions. The location of a lesion was clarified at 15 minutes in only 1 patient. In this patient, the lesion was smaller in size (0.8 cm × 0.7 cm) on IOUS, with an ill-defined border and the echogenicity of periphery in the lesion that was similar to that of normal pulmonary parenchyma, which may have contributed to the long intraoperative localization time. The lesions of the other 2 patients with suboptimal lung atrophy assisted by APE combined with OLV were also shown clearly within 1 minute. With APE-assisted IOUS, the maximum diameter of the lesions was 1.38±0.54 cm. Spearman’s correlation analysis was used to assess the correlation between the maximum diameter of pulmonary lesions on preoperative CT and on IOUS, and a significant correlation was found between the two (ρ=0.889, P<0.01). The Bland-Altman plot revealed a mean difference between preoperative CT and IOUS measurements of −0.22 cm. The 95% confidence interval (CI) was −0.89 to +0.45 cm (Figure 2). Details of the patients are presented in Table 1.

Figure 2 Consistency analysis of preoperative CT and IOUS in measuring the maximum diameter of pulmonary lesions. (A) The scatter plot showing the relationship between preoperative CT and IOUS measurements of the maximum diameter of pulmonary lesions. (B) The Bland-Altman plot of the maximum diameter of pulmonary lesions between preoperative CT and IOUS. CT, computed tomography; IOUS, intraoperative ultrasound; SD, standard deviation.

Finally, the pathology-based results showed 8 (50.0%) malignant lesions and 8 (50.0%) benign lesions. There were 7 invasive adenocarcinomas and 1 carcinoma in situ among the malignant lesions. We found that most of the malignant lesions (7/8) on APE-assisted IOUS were hypoechoic, internally heterogeneous in echogenicity, and poorly demarcated. Only 1 patient showed a patchy hyperechoic lesion. The benign lesions included 1 fungal infection, 1 branchial dilatation with mucus plug formation,
1 organizing pneumonia, and 5 tuberculosis. IOUS in benign lesions showed that both well- and ill-defined borders could exist. Beyond that, there was no clear specificity in the echogenicity of the lesions, and both hypo- and hyper-echogenicity could be observed. Necrosis in the center of the lesion with the central anechoic area was observed in 2 cases of tuberculosis.

Ultimately, we concluded that all lesions (n=16) were visualized on APE-assisted IOUS, and the localization success rate was 100%. In addition, none of the patients had complications during APE-assisted IOUS localization. The details of the characterizations of malignant and benign lesions with APE-assisted IOUS are presented in Table 2.

Malignant cases

Figure 3 shows the images of a 51-year-old male patient with a right upper lung nodule that was ultimately pathologically diagnosed as a moderately-to-highly differentiated invasive adenocarcinoma. Preoperative CT showed a subsolid ground-glass nodule (1.2 cm × 1.1 cm) in the upper lobe of the right lung, with a shortest distance of 1.2 cm from the pleura on CT (Figure 3A). APE was injected in a volume of 1,500 mL. After the lung where the lesion was located had completely atrophied, it took approximately 2 minutes to identify the lesion using APE-assisted IOUS. At this point, APE-assisted IOUS showed that the shortest distance of the lesion from the pleura was 0.2 cm. The nodule showed a central hypoechoic and peripheral isoechoic pattern on IOUS, with internal echogenic heterogeneity and poor demarcation from the surrounding lung tissue (Figure 3B).

Figure 3 A case of invasive adenocarcinoma of the upper lobe of the right lung. (A) Axial CT images of the lung window and mediastinal window. (B) Artificial pleural effusion-assisted IOUS demonstrated the lesion with central hypoechogenicity and peripheral isoechogenicity. CT, computed tomography; IOUS, intraoperative ultrasound.

In another patient, preoperative CT revealed an irregular mass-like nodule (2.6 cm × 2.3 cm) in the upper lobe of the right lung with blurred borders (Figure 4A). CT revealed that the shortest distance of the lesion from the pleura was 2.3 cm. APE was injected in a volume of 1,500 mL. After complete lung atrophy, the time to identify nodules using IOUS was 2 minutes. On APE-assisted IOUS, this lesion appeared as smooth-surfaced, ill-defined, flaky, and slightly hyperechoic (Figure 4B). It was diagnosed as highly-to-moderately differentiated invasive adenocarcinoma by pathology.

Figure 4 A case of invasive adenocarcinoma of the upper lobe of the right lung. (A) Axial CT images of the lung window and mediastinal window. (B) Artificial pleural effusion-assisted IOUS showed the lesion to be smooth-surfaced, poorly defined, and slightly hyperechoic. CT, computed tomography; IOUS, intraoperative ultrasound.

Benign cases

A 34-year-old female patient had a nodule in the lower lobe of the right lung. Preoperative CT showed a ground-glass nodule (0.6 cm × 0.5 cm) in the lower lobe of the right lung with a vacuolar sign (Figure 5A). CT revealed that the nodule was 2.1 cm from the pleura at its closest distance and 0.8 cm from the interlobar fissure. APE was injected in a volume of 1,000 mL. After complete lung atrophy, APE-assisted IOUS was used to determine the time of the nodule, which took 2 minutes. APE-assisted IOUS of this lesion showed a slightly hyperechoic periphery with a gas-like strong echo in the center, poorly defined borders, and uneven internal echogenicity (Figure 5B). The shortest distance of the lesion from the pleura on IOUS was 0.4 cm. The gas described above was significantly expelled 8 minutes after the nodule was identified, at which time the IOUS sonogram of the lesion changed significantly. The whole lesion was slightly hyperechoic at this point compared to the surrounding normal lung tissue (Figure 5C). Small focal bronchiectasis with mucus plug formation in the lung tissue was eventually confirmed pathologically.

Figure 5 A case of lower lobe nodule in the right lung confirmed by pathology small focal bronchiectasis with mucus plug formation. (A) Axial CT images of the lung window and mediastinal window. (B) The image showing the lesion of artificial pleural effusion-assisted IOUS localization. (C) Artificial pleural effusion-assisted intraoperative ultrasound image 8 minutes after localizing the nodule. CT, computed tomography; IOUS, intraoperative ultrasound.

A 45-year-old male patient had a postoperative pathologically confirmed tuberculous granuloma. Preoperative CT showed a solid nodule measuring 1.6 cm × 1.3 cm in the lower lobe of the right lung with a shortest distance from the pleura of 2.6 cm. APE was injected in a volume of 1,000 mL during VATS. APE-assisted IOUS recognized the above nodule 1 minute after complete lung atrophy. IOUS showed that the lesion had a well-defined border and smooth surface. It was hypoechoic, with a few anechoic areas visible inside the lesion. The shortest distance between the lesion and the pleura was 0.3 cm using APE-assisted IOUS (Figure 6).

Figure 6 A case of tuberculous granuloma in the lower lobe of the right lung. (A) Axial CT images of the lung window and mediastinal window. (B) Artificial pleural effusion-assisted IOUS revealed a hypoechoic lesion containing scattered anechoic areas, with well-defined borders and a smooth surface. CT, computed tomography; IOUS, intraoperative ultrasound.

Discussion

With the rising incidence of small PNs and the popularity of minimally invasive techniques, VATS has been widely used due to the advantages of reduced postoperative pain, faster recovery time, and lower complication rate (10,11). However, intraoperative visualization and localization of PNs are particularly important due to the limited operating space in VATS, especially for non-subpleural PNs. At present, the most commonly clinically used localization methods are hook wire, microcoil, and medical dye under CT guidance preoperatively. However, hook wire and microcoil positioning rely on CT-guided puncture, which carries risks such as pneumothorax and displacement. Medical dye (such as methylene blue) is inexpensive, but diffuses quickly (requiring surgery within 2–4 hours), does not show deep nodules well, and is difficult to locate. IOUS is necessary as a real-time, easy, and effective localization method in order to minimize the possibility of conversion of VATS to conventional open chest surgery. IOUS has been used initially in laparoscopic surgery, and several studies have confirmed the importance of laparoscopic ultrasound in the evaluation of abdominal tumors (12-14).

For pulmonary lesions, ultrasound beam produces image artifacts due to high differences in the acoustic impedance at the soft tissue/air interface. However, IOUS theoretically has some potential to observe PNs after gradual atrophy of the lungs using OLV. Previous studies have predominantly remained purely focused on the ability of IOUS to localize PNs (15-17). Sperandeo et al. (18) included 14 patients in whom IOUS was applied during VATS, initially confirming that IOUS was an effective method for localization of PNs. In the OLV-only condition, there are still some patients for whom it is not possible to collapse the lung completely due to retention of sputum in the airway and other reasons, which compounds the challenge of intraoperative localization. Image artifacts are incurred by pulmonary inflation, obscuring the visualization of partial anatomical structures such as pulmonary vessels and bronchi. APE has been widely used in laparoscopic surgery, and the visualization of lesions in difficult areas (e.g., the hepatic dome) on gray-scale ultrasound has been improved with the assistance of APE (19-22). In this study, the application of APE prompted a more complete lung atrophy with OLV, leading to better localization of pulmonary lesions using IOUS.

To the best of our knowledge, this study is the first systematic study of APE combined with IOUS to localize PNs, demonstrating the feasibility of APE-assisted IOUS in VATS. Although APE could be limited by pleural adhesions, especially in patients with a history of previous surgery, it was successfully performed in all lesions (n=16) in this study. It not only aids the OLV in accelerating lung atrophy but also provides a better ultrasonic field of view. Even in the presence of conditions of incomplete lung atrophy or nodules located deep in the lung parenchyma, the lesions could be better visualized, and the quality of ultrasound images could be improved. Hou et al. (23) considered the palpation method of a duration exceeding 12 minutes as a failure in a population with no previous history of malignancy. Although the above palpation method was not used in our study, the innovative use of APE-assisted IOUS was used to localize PNs and our study included patients with a previous history of lobectomy or segmental resection. The median time for localization of PNs after waiting for lung atrophy in this study was only 1.00 (1.00, 2.00) minutes. Not only that, all 16 lesions in 15 patients in our study were successfully localized with a 100% localization success rate. In only 1 case, although intraoperative localization was successful, the localization time of the nodule was almost 15 minutes. The reasons for the long localization time were considered as follows: The lesion in this patient was small in size, and the IOUS showed that it had a maximum diameter of 0.8 cm, with an unclear border. In addition, this patient had a previous history of PN resection, resulting in pleural adhesions that required additional detachment. In all patients, no serious adverse reactions occurred intraoperatively. Although our research results indicated that APE-assisted IOUS during VATS showed the promising results, we acknowledged that the conclusions regarding its relative effectiveness at this stage still needed to be verified through larger-scale multi-center trials and comparisons with techniques such as hook wire and medical dye. We also found that APE-assisted IOUS was not only able to better localize the lesions, but also better for the characterization of the nodules (e.g., size, echogenicity, borders, calcification). The CT of a 53-year-old male patient showed a solid nodular mass in the upper lobe of the right lung (Figure 7A). On APE-assisted IOUS, the lesion was well-defined and arc-shaped strong echogenicity and posteriorly accompanied by a broad acoustic shadow (Figure 7B). IOUS suggested that the lesion could be benign and may be associated with an internal calcareous deposit. The final pathology suggested tuberculosis with calcium deposition. We believed that the IOUS characteristics of the lesions were closely related to the degree of lung atrophy. As mentioned above in the benign case, 8 minutes of observation after successful localization showed a change in the echogenicity of the lesion as the gas inside the lesion was discharged, showing an overall hyperechoic pattern. In addition to this, in this study with APE-assisted IOUS, malignant lesions were mostly shown to present poorly defined borders, non-smooth surfaces, hypo-echogenicity, and internal echogenic heterogeneity.

Figure 7 The case of tuberculosis with calcium deposition. (A) Axial CT images of the lung window and mediastinal window. (B) Artificial pleural effusion-assisted IOUS demonstrated a well-defined, arc-shaped lesion with strong echogenicity and a broad posterior acoustic shadow. CT, computed tomography; IOUS, intraoperative ultrasound.

The study has some limitations. Firstly, this was an exploratory study to assess the feasibility of APE-assisted IOUS. Due to the limitations of being conducted in a single center and the early stage of technology, the sample size was limited; a larger sample size is needed to validate the diagnostic efficacy of this technology. Second, due to the large difference in acoustic impedance of the soft tissue/air interface, which can cause image artefacts, IOUS was not performed on lesions without the assistance of APE. In response to the above, this study did not compare the APE and non-APE groups, and further intraoperative data would be collected to describe this in detail in the future. Lastly, color Doppler flow imaging was affected by factors such as cardiac pulsation, resulting in poor blood flow imaging. In order to better display the microcirculation perfusion status inside the lesions, we would use contrast-enhanced ultrasonography to characterize PNs in the future to further confirm the feasibility of IOUS assisted by APE for detecting PNs during VATS.

Conclusions

APE-assisted IOUS is feasible and effective in localizing PNs during VATS. Furthermore, localization of PNs in our preliminary study was entirely successful and effective in characterizing the lesions (e.g., depth, size, solid component). We believe that in daily clinical use, it can significantly help thoracic surgeons to quickly localize the lesion, shorten the operation time, and increase the success rate of the operation. It is sincerely hoped that this new technology will lead to its adoption by more thoracic surgeons.

Acknowledgments

The authors would like to sincerely thank all the staff involved in this study.

Footnote

Reporting Checklist: The authors have completed the STARD reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-663/rc

Data Sharing Statement: Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-663/dss

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-663/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 and its subsequent amendments. The study was approved by the Ethics Committee of Wuhan Jingyintan Hospital affiliated to Tongji Medical College of Huazhong University of Science and Technology and informed consent was taken from all individual participants.

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. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin 2021;71:209-49. [Crossref] [PubMed]
2. Bendixen M, Jørgensen OD, Kronborg C, Andersen C, Licht PB. Postoperative pain and quality of life after lobectomy via video-assisted thoracoscopic surgery or anterolateral thoracotomy for early stage lung cancer: a randomised controlled trial. Lancet Oncol 2016;17:836-44. [Crossref] [PubMed]
3. Sihoe ADL. Video-assisted thoracoscopic surgery as the gold standard for lung cancer surgery. Respirology 2020;25:49-60. [Crossref] [PubMed]
4. Fischer GW, Cohen E. An update on anesthesia for thoracoscopic surgery. Curr Opin Anaesthesiol 2010;23:7-11. [Crossref] [PubMed]
5. McDermott S, Fintelmann FJ, Bierhals AJ, Silin DD, Price MC, Ott HC, Shepard JO, Mayo JR, Sharma A. Image-guided Preoperative Localization of Pulmonary Nodules for Video-assisted and Robotically Assisted Surgery. Radiographics 2019;39:1264-79. [Crossref] [PubMed]
6. Mayo JR, Clifton JC, Powell TI, English JC, Evans KG, Yee J, McWilliams AM, Lam SC, Finley RJ. Lung nodules: CT-guided placement of microcoils to direct video-assisted thoracoscopic surgical resection. Radiology 2009;250:576-85. [Crossref] [PubMed]
7. Machi J, Sigel B, Zaren HA, Schwartz J, Hosokawa T, Kitamura H, Kolecki RV. Technique of ultrasound examination during laparoscopic cholecystectomy. Surg Endosc 1993;7:544-9. [Crossref] [PubMed]
8. Keating J, Singhal S. Novel Methods of Intraoperative Localization and Margin Assessment of Pulmonary Nodules. Semin Thorac Cardiovasc Surg 2016;28:127-36. [Crossref] [PubMed]
9. Sperandeo M, Rotondo A, Guglielmi G, Catalano D, Feragalli B, Trovato GM. Transthoracic ultrasound in the assessment of pleural and pulmonary diseases: use and limitations. Radiol Med 2014;119:729-40. [Crossref] [PubMed]
10. Long H, Tan Q, Luo Q, Wang Z, Jiang G, Situ D, Lin Y, Su X, Liu Q, Rong T. Thoracoscopic Surgery Versus Thoracotomy for Lung Cancer: Short-Term Outcomes of a Randomized Trial. Ann Thorac Surg 2018;105:386-92. [Crossref] [PubMed]
11. Boffa DJ, Kosinski AS, Furnary AP, Kim S, Onaitis MW, Tong BC, Cowper PA, Hoag JR, Jacobs JP, Wright CD, Putnam JB Jr, Fernandez FG. Minimally Invasive Lung Cancer Surgery Performed by Thoracic Surgeons as Effective as Thoracotomy. J Clin Oncol 2018;36:2378-85. [Crossref] [PubMed]
12. Kose E, Kahramangil B, Purysko AS, Aydin H, Donmez M, Sasaki K, Kwon CHD, Quintini C, Aucejo F, Berber E. The utility of laparoscopic ultrasound during minimally invasive liver procedures in patients with malignant liver tumors who have undergone preoperative magnetic resonance imaging. Surg Endosc 2022;36:4939-45. [Crossref] [PubMed]
13. Gülşen M, Özden E, Çamlıdağ İ, Öner S, Bostancı Y, Yakupoğlu YK, Yılmaz AF, Sarıkaya Ş. Intraoperative Ultrasound Can Facilitate Laparoscopic Partial Nephrectomy in Adherent Perinephric Fat. J Laparoendosc Adv Surg Tech A 2023;33:480-6. [Crossref] [PubMed]
14. Wakelin SJ, Deans C, Crofts TJ, Allan PL, Plevris JN, Paterson-Brown S. A comparison of computerised tomography, laparoscopic ultrasound and endoscopic ultrasound in the preoperative staging of oesophago-gastric carcinoma. Eur J Radiol 2002;41:161-7. [Crossref] [PubMed]
15. Gruppioni F, Piolanti M, Coppola F, Papa S, Di Simone M, Albini L, Mattioli S, Gavelli G. Intraoperative echography in the localization of pulmonary nodules during video-assisted thoracic surgery. Radiol Med 2000;100:223-8.
16. Piolanti M, Coppola F, Papa S, Pilotti V, Mattioli S, Gavelli G. Ultrasonographic localization of occult pulmonary nodules during video-assisted thoracic surgery. Eur Radiol 2003;13:2358-64. [Crossref] [PubMed]
17. Wada H, Anayama T, Hirohashi K, Nakajima T, Kato T, Waddell TK, Keshavjee S, Yoshino I, Yasufuku K. Thoracoscopic ultrasonography for localization of subcentimetre lung nodules. Eur J Cardiothorac Surg 2016;49:690-7. [Crossref] [PubMed]
18. Sperandeo M, Frongillo E, Dimitri LMC, Simeone A, De Cosmo S, Taurchini M, Cipriani C. Video-assisted thoracic surgery ultrasound (VATS-US) in the evaluation of subpleural disease: preliminary report of a systematic study. J Ultrasound 2020;23:105-12. [Crossref] [PubMed]
19. Koda M, Ueki M, Maeda Y, Mimura K, Okamoto K, Matsunaga Y, Kawakami M, Hosho K, Murawaki Y. Percutaneous sonographically guided radiofrequency ablation with artificial pleural effusion for hepatocellular carcinoma located under the diaphragm. AJR Am J Roentgenol 2004;183:583-8. [Crossref] [PubMed]
20. Kondo Y, Yoshida H, Tateishi R, Shiina S, Kawabe T, Omata M. Percutaneous radiofrequency ablation of liver cancer in the hepatic dome using the intrapleural fluid infusion technique. Br J Surg 2008;95:996-1004. [Crossref] [PubMed]
21. Zhang D, Liang P, Yu X, Cheng Z, Han Z, Yu J, Liu F. The value of artificial pleural effusion for percutaneous microwave ablation of liver tumour in the hepatic dome: a retrospective case-control study. Int J Hyperthermia 2013;29:663-70. [Crossref] [PubMed]
22. Long Y, Zeng Q, He X, Ye H, Su Y, Zheng R, Yu J, Xu E, Li K. One-lung ventilation for percutaneous thermal ablation of liver tumors in the hepatic dome. Int J Hyperthermia 2020;37:49-54. [Crossref] [PubMed]
23. Hou YL, Wang YD, Guo HQ, Zhang Y, Guo Y, Han H. Ultrasound location of pulmonary nodules in video-assisted thoracoscopic surgery for precise sublobectomy. Thorac Cancer 2020;11:1354-60. [Crossref] [PubMed]