Surgeon's detection of lung nodules with intraoperative ultrasound during thoracoscopic surgery: experience of a single centre.

doi:10.21203/rs.3.rs-1739498/v1

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Surgeon's detection of lung nodules with intraoperative ultrasound during thoracoscopic surgery: experience of a single centre.

https://doi.org/10.21203/rs.3.rs-1739498/v1

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OBJECTIVE

Video-Assisted Thoracic Surgery (VATS) resection, of deep-seated and nodules smaller than 3 cm, is very hard.

Solitary, small and deep-seated pulmonary nodules are difficult to palpate or to see during VATS.

We aimed to evaluated the validity of Intraoperative lung ultrasound (ILU) to visualize solitary and deep-seated pulmonary nodules smaller than 3 cm to enhance knowledge on the ultrasound morphological patterns.

RESULTS

US processor was inserted by expert ultrasound surgeon into the chest through the operating hole, and the mediastinal, costal and diaphragmatic surfaces of the lung were explored.

VATS- Ultrasound (VATS-US) allows to identify size, localization and Ultrasound (US) pattern of the lesions of interest.

Accuracy of Intraoperative Lung Ultrasound for the detection of pulmonary nodules was calculated-

comparing the two groups; the first group in which the patients did not undergo intraoperative ultrasound and the second group in which the patients underwent intraoperative ultrasound.

Student's t-test (p<0,0001) showed that the accuracy of intraoperative ultrasound by comparing detection time of nodules in the two groups.

Intracavitary VATS-US is a reliable, feasible, real-time and effective method of localization of parenchymal lung nodules during selected wedge resection procedures.

intraoperative ultrasound

lung nodules

VATS

thoracic surgery

Today, with the increased use of low dose Computed Tomography (CT), a great number of pulmonary nodules are detected; the ones with features of malignancy undergo surgical treatment.

Surgery, with radical intent, is the cornerstone of early stage non-small cell lung cancer therapy [1]; anatomical lobectomy followed by sampling or dissection of mediastinal lymph nodes, is believed as the present surgical standard treatment. Limited resections are reserved for patients with poor performance status [2].

Video-Assisted Thoracic Surgery (VATS) lobectomy, as current evidences suggest, is a suitable treatment for early-stage Non-Small Cell Lung Cancer (NSCLC) in terms of safety, local control of cancer and survival [3, 4].

Successfull VATS identification of pulmonary nodules depends on intraoperative nodule researching by direct visualization or palpation. The nodules, found out by screening CT scan and requiring resection, are nowdays smaller and smaller [5] and detection of nodules smaller than 3 cm is very hard [6].

Solitary and deep-seated pulmonary nodules are difficult to palpate or to see during VATS [7].

This is a retrospective single-center observational study whose primary aim was to confirm the validity of ILU as a safe and effective localization method to visualize nodules smaller than 3 cm during VATS.

Forty-one patients with solitary and deep-seated pulmonary nodules were included in our study from November 2019 to December 2021 at the Thoracic Surgery Department of the Vanvitelli University of Naples.

All patients underwent pre-operative high-resolution computed-tomography (HRCT), contrast- enhanced computed-tomography (CT), and positron emission tomography, integrated with computed tomography (18F-FDG PET/CT) to record the localization and size of the lesions.

The study was led in compliance with the principles of the Declaration of Helsinki; written informed consent was obtained from all participants during preoperative communication and the protocol was approved by the Ethics Committee of the University of ‘Luigi Vanvitelli’ of Naples (32655/2021).

The inclusion criteria were: a single pulmonary lesion indicated for VATS; age > 18 years; no contraindications for surgery. The exclusion criteria were: recent myocardial infarction or unstable angina; severe neurologic problems; a prolonged prothrombin time (PT-INR) > 1.5 or a platelet count < 30,000; impossibility to tolerate single lung ventilation and pregnancy; enphisema and patients with nodules close to the hilar zone.

Patients were placed in lateral decubitus position, general anesthesia was induced, and double-lumen endotracheal intubation with contralateral single lung ventilation was performed; patients underwent ultrasound-guided fascial blocks of the chest wall using long-lasting local anesthetics in order to reduce post-operative pain.

Lung specimens were not ventilated but rather semi-inflated and inflated.

The VATS approach employed is the anterior triportal approach according to Hansen et al. [8], which consists in two 1–1.5 cm lower access incisions, located in the 7th or 8th intercostal space, in the posterior and anterior axillary line respectivel, for 2 thoracoscopic ports and a 4–5 cm port incision, placed in the 4th intercostal space, in the anterior axillary for a utility incision [9].

The exam was focused on the localization of small lung nodules.

VATS procedure were performed by thoracic surgeons with ultrasound experience.

The Ultrasound (US) processor used for localization of small lung nodules was the BK 5000. A sterile intracavitary laparoscope probe with 38 cm length, 10-mm diameter and a flexible tip, equipped with a convex array transducer with frequencies ranging from 4 to 12 MHz, was introduced through one of the VATS ports. A setting for superficial tissue with tissue harmonics, electronic focusing at the interface level and gain < 50%, were used. [Fig. 1]

US processor was inserted by expert ultrasound surgeon into the chest through the operating hole, and the mediastinal, costal and diaphragmatic surfaces of the lung were explored.

Small lung nodules can be visualized only when the lung is completely deflated. Expert ultrasound surgeon, appling light pressure on the lung surface with the ultrasound probe, reducing residual air, localizes deeper nodules if possible. During the examination, the probe was perpendicular to the pulmonary surface and a warm sterile saline was used to improve surface contact. [Fig. 2]

VATS-US allows to identify size, localization and US pattern of the lesions of interest.

The pulmonary nodules were found and their ultrasound characteristics were recorded.

The surface of the nodules was cauterized with a cautery stick, then a wedge resection with a 2 cm margin was performed; the specimen was sent to the departmentof pathology to confirm the accuracy of excision, therefore all patients were undergoing to lobectomy with mediastinal node dissection according to the pathology results.

ULTRASOUND PARAMETERS OF PULMONARY NODULES

The nodules were classified: according to their margins in “well defined” or “jagged”, according to their shape in “regular” or “irregular” and, according to their echogenicity, in hypoechoic or hyperechoic. [Fig.S1]

The presence or absence of inner hyperechoic striae and/or spots was assessed.

“Size” was defined as the mean between the maximum and minimum diameter of the nodule.

Intraoperative lung ultrasound (ILU) allows the morphological characterization of lung nodules according to their histological benign or malignant nature [10]. [Fig.S2-S3]

Statistic Analysis

Accuracy of Intraoperative Lung Ultrasound for the detection of pulmonary nodules was calculated as rate of detected lesions in percentage comparing the two groups; the first group in which the patients did not undergo intraoperative ultrasound and the second group in which the patients underwent intraoperative ultrasound.

Student's t-test (p < 0,0001) showed that the accuracy of intraoperative ultrasound by comparing detection time of nodules in the two groups. [Fig.S4]

All forty-one patients who underwent thoracoscopic surgery between October 2019 and Dicember 2021 in the Department of Thoracic Surgery of Vanvitelli of Naples due to isolated solitary and deep-seated pulmonary nodules smaller than 3 cm were enrolled into the study.

Inclusion criteria were: no signs of previous malignant disease; patients with suspected pulmonary nodules less than 3 cm; all patients with a good cardiopulmonary function; patients had not previously had a biopsy before operation.

Exclusion criteria: patients with enphisema and patients with nodules close to the hilar zone.

In this study a total of 41 patients with suspected pulmonary nodules undergoing a wedge resection;

18 patients in the first group without intraoperative ultrasound and 23 patients in the second group, with intraoperative ultrasound.

In the first group 18 patients: 11 men, 7 women, median age 64. There were 6 nodules located in the right upper lobe, 4 left lower lobe, 2 middle lobe, 3 right lower lobe and 3 left upper lobe. The median diameter of the nodules was 21 mm, the distance from the visceral pleura was 15 mm, the median time to identify the nodule was 11 minutes; histology. 12 squamous carcinoma, 4 adenocarcinoma, 1 colon metastasis, 1 breast metastasis. Therefore, 1 patient underwent a wedge resection lower lobe of the left lung; 1 patient underwent a wedge resection of the right upper lobe; 3 patients underwent left lower lobectomy; 5 underwent upper right lobectomy; 2 underwent medium lobectomy; 3 unnderwent lower right lobectomy; 3 underwent upper left lobectomy.

In the second group 23 patients: 14 men, 9 women, median age 61.; There were 8 nodules located in the right upper lobe, 6 left lower lobe, 3 middle lobe, 1 right lower lobe and 5 left upper lobe. the median diameter of the nodules was 19 mm, the distance from the visceral pleura was 16 mm, the median time to identify the nodule was 7,5 minutes; histology. 16 squamous carcinoma, 5 adenocarcinoma, 1 breast metastasis, 1 prostate metastasis.

Therefore: 1 pazient underwent a wedge resection of left lower lobe; 1 patient underwent a wedge resection right upper lobe; 7 patient underwent right upper lobectomy; 5 patients underwent left lower lobectomy; 3 patients underwent medium lobectomy; 1 patient underwent right lower lobectomy and 5 patients underwent left upper lobectomy. [ Tab. 1]

In one patients of first group we enlarged the utility incision of about 2 cm, in order to consent the insertion of the hand and the localization of the nodule by fingers palpation, since the spatial relationships of the nodule to landmarks are changed by intentional collapse of the lung during operation. It will increase the difficulty of operation, too [11].

There were no complications.

Student's t-test (p < 0,0001) showed that the accuracy of intraoperative ultrasound by comparing detection time of nodules in the two groups.

Table 1

Characteristics of patients
Characteristics	Group 1 (n = 18)	Group 2 (n = 23)
Age, years (median)	64	62
Sex (male), n (%)	60	61
Side of lung nodules, n (%) RUL LLL ML RLL LUL	6 (33%) 4 (22%) 2 (11%) 3 (17%) 3 (17%)	8 (35%) 6 (26%) 3 (13%) 1 (4%) 5 (22%)
Nodule diameter (mm) median	21	19
Distance from the visceral pleura (mm) median	15	16
Time to identify the nodule (minutes) median	11	7.5
Histology, n (%) Squamous carcinoma Adenocarcinoma Colon metastasis Breast metastasis Prostate metastasis	12 (67%) 4 (23%) 1 (5%) 1 (5%) -	16 (70%) 5 (22%) 1 (4%) - 1 (4%)
Surgical resections n (%) LLL wedge resection RUL wedge resection LUL VATS lobectomy LLL VATS lobectomy RUL VATS lobectomy ML VATS lobectomy RLL VATS lobectomy	1 (6%) 1 (6%) 3 (17%) 3 (17%) 5 (28%) 2 (10%) 3 (17%)	1 (4%) 1 (4%) 5 (22%) 5 (22%) 7 (30%) 3 (13%) 1 (4%)
LLL, left lower lobe; RUL, right lower lobe; LUL, left upper lobe; ML, medium lobe; RLL, right lower lobe; VATS, video assisted thoracic surgery.

Failure of localization of pulmonary nodules less than 3 cm in VATS is reported in up to 17.1% of cases; the minimally invasive surgery is converted to open thoracotomy in up to 54% of cases [12, 13].

Different preoperative techniques have the purpose of marking the nodule favoring its localitation, such as microcoiling, indocyanine tattooing [14], radiolabeling and hooking [15].

These methods have a success rate up to 100% and may avoid open thoracotomy in over 50% of cases [16], the complication as: pneumothorax, air embolism intraparenchymal and bleeding, is about 16.7% [17, 18],

Besides, hook wire dislodgment, from the pulmonary parenchyma, was noted from time to time; it requires two different spaces including: the computed tomographic facility and the operating room.

Successes are operator-dependent and require a multidisciplinary approach that often involves a high-cost.

Advances in imaging technology in ultrasound (US) have resulted in a higher rate of utilization of this procedure [19]. VATS with a triportal approach reduces post-operative complications, such as functional impairment, pain and mortality, decreased operation time and intraoperative hemorrhage when compared to open surgery [20, 21].

However, VATS’ main limit is that palpation of the lung surface is not always possible, in particular in cases of small or deep lesions [22]. Therefore, we employ additional techniques to discover the nodules [23].

The benefits of VATS are reduced by missing the localization of target lesion or by spending a lot of time searching it [24].

According Yue-Long Hou1 et all, the palpation method was considered to have failed if it took more than 12 minutes [25] .

Therefore intra-operatory lung ultrasound (ILU) is a complementing method of localization of small nodules, in real-time and safely [26].

Intraoperative lung ultrasound (ILU) is a new technique that deserves to be developed about its ability to exactly localize invisible or non-palpable pulmonary nodules in real-time during VATS [27], so that surgeons can perform biopsies with higher histological diagnostic and clear surgical margins [28, 29].

No complications were reported in patients undergoing intraoperative ultrasound.

The introduction of minimally invasive thoracic surgery and consequently the intraoperative localization of small pulmonary nodules has become very important for early lung cancer, video-assisted thoracoscopic surgery (VATS) has been adopted as an important tool in the treatment of this devastating disease through minimal invasive surgery [30].

However, lung palpation could be difficult during VATS due to the limited area that can be reached by finger’s operator and the increased risk of major complications; furthermore, these technical limitations restrict the potential of VATS in identifying millimeters lesions, that have not been visualized during the pre-operative studies (CT, PET).

Intracavitary VATS-US is a reliable, feasible, real-time and effective method of localization of parenchymal lung nodules during selected wedge resection procedures [31, 32].

To our knowledge, this study that has systematically applied US during VATS procedures with the aim to visualize solitary and deep-seated pulmonary nodules smaller than 3 cm to enhance knowledge on the ultrasound morphological patterns, ultrasound has the potential to provide a definite limit between the nodules and lung parenchyma to guide surgical resection.

Intraoperative lung ultrasound (ILU) requires a lot of training and experience, as well as the problems associated with the collapsed lung.

Therefore, surgeons, with proper learning, will be able to use with precision intraoperative lung ultrasound in VATS.

Intraoperative lung ultrasoung requires experience and is operator-dependent. Additional cases are needed to corroborate this technique.

VATS

Video-Assisted Thoracic Surgery

ILU

Intraoperative Lung Ultrasound

Ultrasound

VATS-US

Video-Assisted Thoracic Surgery – Ultrasound

NSCLC

Non-Small Cell Lung Cancer

Computed Tomografy

HRCT

High-Resolution Computed-Tomography

18F-FDG PET/TC

18fluorine-fluorodeoxyglucose (¹⁸F-FDG) positron emission tomography/computed tomography

LLL

Left Lower Lobe

RUL

Right Lower Lobe

LUL

Left Upper Lobe

Medium Lobe

RLL

Right Lower Lobe

Ethics approval and consent to partecipate: 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 led in compliance with the principles of the Declaration of Helsinki; written informed consent was obtained from all participants during preoperative communication and the protocol was approved by the Ethics Committee of the University of ‘Luigi Vanvitelli’ of Naples (32655/2021).

Consent to publish: written informed consent for publication was obtained from all participants.

Availability of data and materials: Authors can confirm that all relevant data are included in the article and/or its supplementary information files.

Competing interests: The authors declare that they have no competing interests.

Funding: University of Campania L. Vanvitelli.

Authors’ contributions: Conception and design, GM, MB, AN; administrative support, FC, MF; provision of study materials or patients, AF, GV, MS; collection and assembly of data, MP, FP, GN, SF, AZ, GO, VDF, MC; data analysis and interpretation, RP, MF, MM, CMDC, BL; manuscript writing: all authors; final approval of manuscript: all authors.

Acknowledgement: nothing to declare.

Conflicts of interest: all authors have completed the ICMJE uniform disclosure form. The authors have no conflicts of interest to declare.

Vannucci F, Gonzalez-Rivas D. Is VATS lobectomy standard of care for operable non-small cell lung cancer? Lung Cancer 2016; 100:114–119.
Ismail M, Swierzy M, Nachira D, Ruckert JC, Gonzalez-Rivas D. Uniportal video-assisted thoracic surgery for major lung resections: pitfalls, tips and tricks. J Thorac Dis 2017; 9(4):885–897.
Kaiser LR.Video-assisted thoracic surgery. Current state of the art. Ann Surg 1994; 220(6):720–734.
Yan TD, Black D, Bannon PG, et al. Systematic review and meta-analysis of randomized and nonrandomized trials on safety and efficacy of video-assisted thoracic surgery lobectomy for early-stage non-small-cell lung cancer. J Clin Oncol 2009; 27:2553-62.
Sperandeo M, Venuti M, Quarato C. Uniportal versus multiportal video-assisted thoracic surgery for lung cancer: safety and advantages in employing complementary intraoperative lung ultrasound. Journal of Thoracic Disease 2020; 12(6): 3013-3017.
Kondo R, Yoshida K, Hamanaka K et al. Intraoperative ultrasonographic localization of pulmonary ground-glass opacities. J Thorac Cardiovasc Surg 2009; 138 (4): 837–42.
Fiorelli A, Messina G, Frongillo E et al. The use of ultrasound in detecting and defining ground-glass opacities: Results of an ex vivo evaluation. Interact Cardiovasc Thorac Surg 2018; 26 (4): 551–8.
Hansen HJ, Petersen RH. Video-assisted thoracoscopic lobectomy using a standardized three-port anterior approach - The Copenhagen experience. Ann Cardiothorac Surg 2012; 1:70-6.
Messina G, Bove M, Noro A, Opromolla G, Natale G, Leone F, Di Filippo V, Leonardi B, Martone M, Pirozzi M, Caterino M, Facchini S, Zotta A, Vicidomini G, Santini M, Fiorelli A, Corte Carminia D, Ciardiello F, Fasano M. Prediction of preoperative intrathoracic adhesions for ipsilateral reoperations: sliding lung sign. J Cardiothorac Surg. 2022 May 4;17(1):103.
Sperandeo M, Frongillo E, Dimitri L, 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. Journal of Ultrasound 2019; 23(1): 105-112.
Smelt JLC, Suri T, Valencia O, Jahangiri M, Rhode K, Nair A, Bille A. Operative planning in thoracic surgery: a pilot study comparing imaging techniques and three-dimensional printing. Ann Thorac Surg 2019; 107(2):401–406.
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(2):386–392.
Santini M, Fiorelli A, Messina G, Mazzella A, Accardo M. The Feasibility of LigaSure to Create Intestinal Anastomosis: Results of Ex Vivo Study. Surg Innov 2015; 22(3):266-73.
Luo K, Lin Y, Lin X et al. Localization of peripheral pulmonary lesions to aid surgical resection: A novel approach for electromagnetic navigation bronchoscopic dye marking. Eur J Cardiothorac Surg 2017; 52 (3): 516–21.
Shennib H. Intraoperative localization techniques for pulmonary nodules. Ann Thorac Surg 1993; 56(3):745–748.
Khereba M, Ferraro P, Duranceau A et al. Thoracoscopic localization of intraparenchymal pulmonary nodules using direct intracavitary thoracoscopic ultrasonography prevents conversion of VATS procedures to thoracotomy in selected patients. J Thorac Cardiovasc Surg 2012; 144 (5):1160–5
Fiorelli A, Accardo M, Carelli E. Harmonic technology versus neodymium-doped yttrium aluminium garnet laser and electrocautery for lung metastasectomy: an experimental study. Interact Cardiovasc Thorac Surg. 2016; 23(1):47-56
Fiorelli A, Messina G, Capaccio D, Santini M. Recurrent spontaneous pneumomediastinum: a rare but possible event! J Thorac Dis 2012; 4(4):431-3.
John TG, Greig JD, Crosbie JL, Miles WF, Garden OJ. Superior staging of liver tumors with laparoscopy and laparoscopic ultrasound. Ann Surg 1994; 220(6):711–719.
DeCamp MM Jr, Jaklitsch MT, Mentzer SJ, Harpole DH Jr, Sugarbaker DJ. The safety and versatility of video-thoracoscopy: a prospective analysis of 895 consecutive cases. J Am Coll Surg 1995; 181(2):113–120.
Bendixen M, Licht PB. Video-assisted thoracoscopic surgery versus open lobectomy for lung cancer: time for a randomized trial. Eur J Cardio Thorac Surg 2017; 52(2):398.
Matsumoto S, Hirata T, Ogawa E et al. Ultrasonographic evaluation of small nodules in the peripheral lung during video-assisted thoracic surgery (VATS). Eur J Cardiothorac Surg 2004; 26 (3): 469–73.
Nguyen W, Meyer KC. Surgical lung biopsy for the diagnosis of interstitial lung disease: a review of the literature and recommendations for optimizing safety and efcacy. Sarcoidosis Vasc Difuse Lung Dis 2013; 30(1):3–16.
Patrini D, Panagiotopoulos N, Lawrence D, Scarci M. Surgical management of lung metastases. Br J Hosp Med 2017; 78(4):192– 198.
Yue-Long Hou, Yan-Dong Wang, Hong-Qi Guo, YuKun Zhang, YongKuan Guo & HongLi Han. Thoracic Cancer 2020; 11(5):1354-1360
Wada H, Anayama T, Hirohashi K et al. Thoracoscopic ultrasonography for localization of subcentimetre lung nodules. Eur J Cardiothorac Surg 2016; 49 (2): 690–7.
Ujiie H, Kato T, Hu HP et al. Evaluation of a new ultrasound thoracoscope for localization of lung nodules in ex vivo human lungs. Ann Thorac Surg 2017; 103 (3): 926–34.
Tinti MG, Frongillo E, Sperandeo M. Lung fissures detection with transthoracic ultrasound: is it simply a matter of artifacts? Chest 2018; 154(2):453–455.
Cozzolino I, Ronchi A, Messina G et al. Adequacy of Cytologic Samples by Ultrasound-Guided Percutaneous Transthoracic Fine-Needle Aspiration Cytology of Peripheral Pulmonary Nodules for Morphologic Diagnosis and Molecular Evaluations: Comparison With Computed Tomography–Guided Percutaneous Transthoracic Fine-Needle Aspiration Cytology. Arch Pathol Lab Med 2020;144(3):361-369.
Alecu L, Lungu C, Pascu A et al. Intraoperative ultrasonography during laparoscopic surgery. Chirurgia (Bucur) 2000; 95 (6): 557–64.
Sperandeo M, Filabozzi P, Varriale A, Carnevale V, Piattelli ML, Sperandeo G, Brunetti E, Decuzzi M. Role of thoracic ultrasound in the assessment of pleural and pulmonary diseases. J Ultrasound 2008;11(2):39–46.
Yue-Long Hou, Yan-Dong Wang, Hong-Qi Guo, YuKun Zhang, YongKuan Guo and HongLi Han. Ultrasound location of pulmonary nodules in video-assisted thoracoscopic surgery for precise sublobectomy. Thorac Cancer. 2020;11(5):1354-1360.

FigS1copia.png
Figure S1: Lung Nodule with irregular shape, hypoechoic, absence of inner hyperechoic striae.
FigS2copia.png
Figure S2: Subcentimetric hypoechoic nodule at the lower right lobe.
FigS3copia.png
Figure S3: Lung Nodule with irregular shape, hypoechoic, presence of inner hyperechoic striae.
FigS4copia.png
Figure S4: Student's t-test (p<0,0001 ) showed that the accuracy of intraoperative ultrasound comparing detection time of nodules in the two groups.

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Surgeon's detection of lung nodules with intraoperative ultrasound during thoracoscopic surgery: experience of a single centre.

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Version 1

Abstract

Figures

Introduction

Objective

Materials And Methods

ULTRASOUND PARAMETERS OF PULMONARY NODULES

Statistic Analysis

Results

Discussion

Conclusion

Limitations

Abbreviations

Declarations

References

Supplementary Files

Status:

Version 1