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An “alternative finger” in robotic-assisted thoracic surgery: intraoperative ultrasound localization of pulmonary nodules


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Original papers

DOI: 10.11152/mu-1053

An “alternative finger” in robotic-assisted thoracic surgery:

intraoperative ultrasound localization of pulmonary nodules

Zhenyu Zhou


, Zhitian Wang


, Zhelan Zheng


, Jinlin Cao


, Chong Zhang


, Zhehao He


, Wang Lv


, Jian Hu


1Department of Thoracic Surgery, 2Department of Ultrasound Imaging, the First Affiliated Hospital, College of Medi- cine, Zhejiang University, Hangzhou, China

Received 22.03.2017 Accepted 11.06.2017 Med Ultrason

2017, Vol. 19, No 4, 374-379 Corresponding author: Jian Hu

Department of Thoracic Surgery, the First Affiliated Hospital, College of Medicine, Zhejiang University,

79 Qingchun Road, Shangcheng District, Hangzhou, 310003, China

Phone: +86 13750801974 Email: [email protected]


Currently, lung cancer is the most common cancer worldwide and is associated with the highest incidences of cancer-related morbidity and mortality [1-4]. In vari- ous populations, the increasing popularity of physical ex- aminations and improvements in health care awareness

have led to tremendous changes in the epidemiology of lung cancer (e.g., prevalence and prognosis) [5]. Current- ly, chest computed tomography (CT) is used as a primary means of lung cancer screening, and has been credited as contributing to 20% of the decrease in lung cancer-relat- ed mortality related to early lung lesion detections [6,7].

Additionally, surgical resection has become the preferred treatment for lung cancer, follow-up studies demonstrat- ing that surgical treatment will maximize the quality of life of patients with non-advanced non-small cell lung cancer (NSCLC)[8,9].

Ultimately, the widespread application of video- assisted thoracoscopy brought lung surgery into the minimally invasive era. The advent of the da Vinci ro- botic surgical system has provided novel opportunities for the development of minimally invasive thoracic sur- gery procedures [10-14]. However, the development and Abstract

Aim: Robotic-assisted thoracic surgery (RATS) has become a promising treatment for pulmonary neoplasms. During RATS, intraoperative ultrasonography can act as an “alternative finger” to “touch” and locate lesions, especially pulmonary nodules. This study was aimed to investigate the efficacy of intraoperative ultrasonographic localization during da Vinci RATS procedures. Material and methods: Patients with pulmonary nodules were randomly divided into an Experimental Group and Control Group in which nodules were respectively located using intraoperative ultrasonography or by the surgeon’s anatomic knowledge. The success rates and relevant localization factors were compared between the groups and analyzed to conclude the efficacy of intraoperative ultrasonography. Additionally, the intraoperative ultrasonography learning curve was analyzed to evaluate each surgeon’s ability to independently perform intraoperative ultrasonography. Results: Thirty-four patients were included in the study (n = 17/group). Respectively, the Experimental Group and Control Group comprised 41.2% and 58.9%

women (p= 0.937), and had average ages of 55.5 and 55.8 years. In the Experimental group, ultrasonographic localization for mixed ground-glass nodules with CT values of -500 to -100 Hounsfield units had an efficacy of 87.5%. By contrast, the locali- zation efficacy in Control Group was 20.0% (p=0.032). A single surgeon without prior experience performed intraoperative ultrasonography in 20 cases, and the latter 10 procedures required significantly less time relative to the former 10 procedures (p=0.000). Conclusions: During RATS, the use of intraoperative ultrasonography as an “alternative finger” to “touch” and find the accurate location of pulmonary nodules, especially mixed ground-glass nodules, is warranted.

Keywords: intraoperative ultrasonography; robotics; pulmonary nodule; ground-glass nodule


maturation of this new robotic surgical system cannot be considered apart from other relevant technology [12]. At present, the lack of tactile feedback while using this ro- botic system remains a major disadvantage because sur- geons are unable to accurately locate lesions (e.g., small nodules) with a finger or device, as they would during in video-assisted thoracic surgery (VATS). The resulting pathological uncertainty will have a detrimental effect on subsequent treatment, especially if a resected lesion can- not be located in vitro. However, an invasive technique such as CT-guided hook-wire localization would not be suitable for all cases, as such procedures would be highly risky if the nodule is near the diaphragm, mediastinum or scapula [15-19]. This scenario thereby provides a new opportunity to implement intraoperative ultrasonography as a noninvasive and repeatable localization technique during robotic-assisted pulmonary surgery [20].

A few non-controlled studies with small sample sizes have reported the application of ultrasonography during robotic-assisted thoracic surgery (RATS) [21,22]. Given its characteristics of noninvasiveness, real-time feedback and repeatability, intraoperative ultrasonography could provide valuable pathologic information based on mor- phological features such as the shape, edge, echo level, blood flow, acoustic shadow and compression simultane- ously with lesion location [23,24]. Notably, these benefits have already been confirmed in other areas of surgery.

Accordingly, we conducted this prospective, ran- domized controlled study to explore the application of ultrasonography for lesion localization during RATS.

This study therefore aimed to investigate the effective- ness and applicability of intraoperative ultrasonography for the localization of small pulmonary nodules, and to clarify the relationship between ultrasonography and ex- isting, commonly used means of localization.

Material and methods

The study was conducted in compliance with the principles of the Declaration of Helsinki. The protocol was approved by the Ethics Committee of the First Affili- ated Hospital, College of Medicine, Zhejiang University (2017/104). Written informed consent was obtained from all participants during preoperative communication.


Eligible patients included those with CT scan-iden- tified peripheral pulmonary nodules, with no history of thoracic surgery, and who met the criteria for RATS re- section. Patients with pulmonary nodules larger than 3 cm in diameter were excluded from the present study.

The eligible patients were prospectively enrolled after providing written informed consent.

Devices and settings

A newly developed robotic dedicated convex array ultrasound probe (ProART-8826, Brüel & Kjær Sound

& Vibration Measurement A/S, Skodsborgvej 307, DK- 2850 Nærum, Denmark) and color Doppler ultrasound scanning diagnostic apparatus (flexFocus 800) were used for this study.

The ultrasound devices were connected to the ro- bot console using a DVI signal cable. After equipment placement, the surgeon physician logged in, selected the

“Video” menu and “Display Preferences” submenu, and switched the “TilePro” option from “OFF” to “3D”. This allowed the ultrasonographic images to be presented syn- chronously in 3D mode below the original surgical field, as shown in figure 1.

Study protocol

All procedures were performed while the patient was under general anesthesia with single lung ventilation through a double-lumen endotracheal intubation.

In the Experimental Group, the ultrasound probe was initially fed into the chest through the auxiliary hole by the assistant surgeon. The probe was then fixed with a bipo- lar clamp and moved along the pulmonary surface with a slightly more force by the chief surgeon. Another assistant surgeon measured the following ultrasonographic features of nodules that appeared on images: long diameter, echo- genicity, border sharpness and sound shadow. Indispen- sable on-site guidance was provided by an experienced sonologist during the initial stage of the study. Cases in the Experimental group that did not contain detectable nodules of interest were transferred to the Control Group.

In the Control Group, the approximate nodule loca- tion was determined by surgeons who had experience with preoperative CT images.

In both groups, RATS resection was performed after ultrasonographic attempts or empirical localization.

All RATS procedures were performed or supervised by a single thoracic surgeon who had no formal experi- ence with ultrasonography.

Fig 1. Ultrasonographic images from the surgeon’s viewpoint.


Data collection

Preoperative patient data (age and sex), surgical parameters (lesion distribution, operation time, and es- timated blood loss), localization parameters (duration and outcome), and postoperative hospital data (drainage time, length of stay, and postoperative complications) were collected.

Statistical analysis

Experimental data were deposited into a database us- ing Microsoft Excel (Microsoft Corporation, Redmond, WA, USA). All statistical calculations were performed using SPSS 20.0 software (IBM Corporation, Armonk, NY, USA). Measurement data were compared using the Student’s t-test or the Mann-Whitney U test, and discrete data were compared using the chi-square test or Fisher’s exact test. Differences were considered statistically sig- nificant at a p value <0.05. Figures were drawn using GraphPad Prism 5.0 software (GraphPad Software Inc., La Jolla, CA, USA).


Baseline characteristics

Thirty-four patients were enrolled in the present study over 9 operation days. The patients included 17 women and 17 men with ages ranging from 19 to 80 years. Each patient had one pulmonary nodule. The patients were randomly distributed into the Experimental Group and Control Groups, which did not differ significantly in terms of age, sex or lesion distribution (Table I).

Safety verification

In the Experimental Group, 2 – 15 minutes were re- quired for ultrasonography, and no related complications were observed. The operation time ranged from 44 to 237 min, and the estimated blood loss ranged from 5 to 50 ml. The drainage time and lengths of hospital stay ranged from 2 to 11 days and from 3 to 16 days, respectively.

Table I. Demographic characteristics and distribution of nod- ules

Experimen- tal group (n=17)

Control group (n=17)


Age (years) mean±SD 55.5±11.9 55.8±9.7 0.937

Sex–male 10 7 0.254

Distribution 0.513

Left upper lobe 3 4

Left lower lobe 4 3

Right upper lobe 2 5

Right middle lobe 2 2

Right lower lobe 6 3

SD – standard deviation

Table II. Safety parameters associated with intraoperative lo- calization.

Experimen- tal group (n=17)

Control group (n=17)

p-value Surgery duration (min),

mean±SD 92±44 99±25 0.591

Blood loss (ml),

median 89 104 0.041*

Drainage time (days),

mean±SD 4.5±2.8 4.6±2.3 0.895

Hospital stay (days),

mean±SD 5.8±3.6 6.9±2.4 0.289

Complications (Chylo-

thorax) 1 0 1.000

SD – standard deviation

Table III. Outcomes of intraoperative localization and related factors.


Group Control

Group P-value

Nodules confirmed 0.271

Number (Total) 13 (17) 10 (17) Distance from Pleura

Within 1 cm 11 (11) 9 (10) 0.476

Within 2 cm 13 (14) 10 (15) 0.169

Long Diameter on CT

Within 1 cm 3 (4) 2 (6) 0.524

Within 2 cm 10 (13) 7 (14) 0.236

CT Value

-500 HU and lower 0 (1) 0 (3)

-500 to–100 HU 7 (8) 1 (5) 0.032*

-100 HU and higher 6 (8) 9 (9) 0.206 CT–computed tomography, HU–Hounsfield unit

One patient developed postoperative chylothorax and re- covered after conservative treatment.

In the Control Group, the estimated blood loss ranged from 20 to 100 ml. The operation time, drainage time and lengths of hospital stay ranged from 59 to 140 min, 3 to 12 days, and 4 to 13 days respectively. No patients devel- oped postoperative complications.

None of these differences were statistically signifi- cant except for a significantly lower blood loss in Experi- ment Group, as shown in Table II.

Outcomes of localization

We attempted to locate a total of 34 nodules in the two groups, and successfully located 13/17 nodules in the Experiment Group and 10/17 in the Control Group. The remaining nodules were confirmed in vitro after wedge resection according to the anatomical location. The ana- lyzed outcomes included the tumor long diameter, dis- tance from pleura, and CT value on the preoperative CT scan (Table III).


Time required for intraoperative ultrasonography Between a pilot study and the current former study, a single surgeon without former experience performed intra- operative ultrasonography in 20 cases. Significantly less time was required to perform ultrasonography in the latter 10 cases, compared with the former 10 cases (fig 2). In addition, the use of intraoperative ultrasonography did not prolong the operation time in the Experimental Group.


Although ultrasonographic applications are not novel with respect to surgical clinical practice, the lung, a gas- bearing tissue, has been “restricted” from the traditional viewing methods used by most surgeons, including tho- racic surgeons [25]. Furthermore, experienced surgeons could achieve relatively satisfactory localization using touch during traditional thoracotomy and VATS proce- dures, thus, reducing the demand for ultrasonographic techniques [21]. In addition, the role and value of ultra- sonography in pulmonary surgery remain controversial [26,27]. In summary, the application of intraoperative ultrasonography during pulmonary surgery has not yet received sufficient attention or undergone extensive de- velopment.

The introduction of the Da Vinci robotic surgical system has created new potential applications for pulmo- nary ultrasonography. RATS, the result of an inevitable trend of development is similarly complicated by a lack of tactile feedback. Accordingly, thoracic surgeons now require an intraoperative localization method to replace the traditional finger-based tactile procedure. The present study aimed to address this clinical problem by imple- menting intraoperative ultrasonography to serve as an

“alternative finger” during RATS and thus compensate

for deficiencies in localization and guidance for follow- up clinical decisions.

Our study has fully validated the safety of intraopera- tive ultrasonography in RATS. Specifically, patients in the Experimental Group did not experience an increased operation time, estimated blood loss, postoperative drainage time, or length of hospital stay. Once the rel- evant technology had been mastered, each intraoperative ultrasonographic procedure required only approximately 4 minutes. Additionally, intraoperative ultrasonography not only improved the accuracy of nodule localization, but also provided information about nodule pathology [22]. Accordingly, surgeons were able to reduce trauma and operation time by clear targeting, accurate lesion re- section, and easy verification in isolated tissues.

A CT value of -100 HU is considered a typical clinical soft tissue value [28]. Pulmonary nodules with CT values exceeding this value are generally considered to be solid pulmonary nodules (SPN), which are not difficult to find intraoperatively. Correspondingly, nodules with CT val- ues less than -100 HU are considered subsolid pulmo- nary nodules (SSPN). This latter category includes pure ground-glass nodules (pGGN) with CT values less than -500 HU, which are difficult to identify intraoperatively in vivo, and mixed ground-glass nodules (mGGN) with CT values between -500 HU and -100 HU, which are eas- ily palpated.

The results of our study demonstrated that SPNs were generally located with a high level of accuracy, which did not differ significantly between the groups. In con- trast, the use of intraoperative ultrasonography led to a significantly better ability to locate mGGNs in Experi- mental Group, thus demonstrating the usefulness of this

“alternative finger”.

Although intraoperative ultrasonography during RATS can be performed quickly, safely, noninvasively, accurately, and repeatably, the need for a single ultra- sonographic specialist would require too much addition- al time and expenditure and would counteract the listed advantages. We found the performance of intraoperative ultrasonography by one thoracic surgeon within the team to be the optimal application. Our findings demonstrated that experience with 20 cases was sufficient for the re- search team to master the basic performance of intraop- erative ultrasonography during RATS. Furthermore, the latter 10 cases required significantly less performance time than did the former 10 cases. We must note some inevitable insufficiencies of this preliminary exploratory research study. It was difficult to quantify the advantage of accuracy in the Experimental Group because intraop- erative ultrasonographic localization was so accurate in practice, whereas empirical localization was ambiguous.

Fig 2. Time required for intraoperative localization.


Furthermore, as the main endpoint was an initial assess- ment of the value of intraoperative ultrasonography for lesion localization during RATS, the sample size was not sufficiently large to analyze the ultrasonographic prop- erties and thus infer the pathological nature of nodules [8,29]. A semi-quantitative diagnostic model, such as a nomogram, should be established to determine whether a lesion is benign or malignant, based on the ultrasono- graphic properties of a particular nodule [30].


In this study, we confirmed that intraoperative ul- trasonography could act as an “alternative finger” with which to accurately localize pulmonary nodules, espe- cially mixed ground-glass nodules, during RATS. These findings support the worthiness of this technique and warrant further studies to explore its use for detecting the pathological properties of these nodules.

Acknowledgements: This study was supported by the Major Science and Technology Projects of Zhejiang Province (grant no. 2014C03032).

Conflicts of interest: None to declare.


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