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Ann Thorac Surg 2005;79:443-449
© 2005 The Society of Thoracic Surgeons

Original article: General thoracic

Transthoracic Endosonography for the Intraoperative Localization of Lung Nodules

Sandro Mattioli, MDa,*, Franco D’Ovidio, MDa, Niccolò Daddi, MDa, Luca Ferruzzi, MDa, Vladimiro Pilotti, MDa, Alberto Ruffato, MDa, Roberto Bolzani, PhDb, Giampaolo Gavelli, MDc

a Department of Surgery, Intensive Care, and Organ Transplantation
b Department of Psychology
c Department o fRadiology and Pathology, University of Bologna, Bologna, Italy

Accepted for publication July 14, 2004.

* Address reprint requests to Dr Mattioli, Dipartimento di Discipline Chirurgiche, Rianimatorie e dei Trapianti, Università di Bologna, Via Massarenti, 9, 40138 Bologna, Italy; (E-mail: s.mattioli{at}orsola-malpighi.med.unibo.it).

Presented at the Fortieth Annual Meeting of The Society of Thoracic Surgeons, San Antonio, TX, Jan 26–28, 2004.


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 DISCUSSION
 References
 
BACKGROUND: Transthoracic ultrasonography has been advocated for the localization of lung nodules during video-assisted thoracoscopic surgery (VATS) for nonperipheral nodules.

METHODS: Video-assisted thoracoscopic surgery for lung nodules was performed in 54 consecutive patients. Preoperative computed tomography (CT) diagnosed 65 lesions. Positron emission tomography (PET) identified 2 lesions not revealed by CT. All nodules were judged whether visible and/or palpable. Diameter and distance of the nodule from the anterior, lateral, and posterior chest wall were measured on CT scan and served in a discriminant analysis to predict which nodule would be neither visible nor palpable. The deflectable multifrequency (7.5 to 10 MHz) endosonography probe was used to identify the nonvisible and nonpalpable nodules.

RESULTS: Resected nodules were 69; 67 diagnosed preoperatively, and 2 intraoperatively by ultrasonography. At VATS exploration 16 of 65 (25%) of the CT diagnosed nodules were nonvisible and nonpalpable. The discriminant analysis failed to predict correctly whether nodules would be visible and/or palpable in 33% because of surrounding severe emphysema, proximity to a fissure, or to the hylum. The endosonography identified 15 out of 16 of the nonvisible and nonpalpable nodules, thus conversion to thoracotomy was necessary for one nodule. The combination of video, palpatory, and endosonographic inspections had 98% sensitivity and 100% specificity in localizing the nodules.

CONCLUSIONS: Intraoperative transthoracic ultrasonography is useful to guide VATS resection of lung nodules. It is a bedside tool, not requiring planning and coordination with the interventional radiology suite, thus you use it if you need it. It has no related morbidity, and may also have a role in revealing lesions occult at preoperative work-up.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 DISCUSSION
 References
 
The evaluation and management of solitary pulmonary nodules create diagnostic and therapeutic challenges. Contrast enhanced computed tomography, positron emission tomography, and the combination of the two have been adopted although false negative and false positive results in determining the nature of the lesion have been reported with these techniques [1–4].

Fine needle aspiration biopsy may help avoid surgical intervention if a benign diagnosis is obtained, however, there is a significant risk of a false negative result and also a significant incidence of complications [5, 6]. Certainly caution must be exercised in accepting a benign diagnosis of a solitary pulmonary nodule on the basis of partial information, thus surgical biopsy is frequently required.

With the ongoing effort to limit morbidity related to diagnostic and therapeutic procedures in the past decade, the role of video-assisted thoracoscopic surgery in the management of lung nodules has been widely accepted. The limitation to its application has been the frequent need of localization techniques in order to provide an intraoperative aim for the surgical resection, particularly for nodules that on preoperative imaging appear to be nonsubpleural tumors. Multiple localization methods such as methylene blue staining and hook wire techniques have been advocated for this purpose, although they have been found to be at times cumbersome in their application and characterized by a high failure rate, along with risks of pneumothorax and intraparenchymal hemorrhage [7–9]. A more recently proposed adjunct to video-assisted thoracoscopic lung resection, for both diagnostic and staging purposes, has been proven to be the intraoperative transthoracic ultrasonography providing good results in localizing lung nodules occult at first intraoperative inspection [10–12].

In this report it is our intention to further investigate the utility of transthoracic ultrasonography during video-assisted thoracoscopic surgery for lung nodules. Furthermore, we provide criteria that may be of help to preoperatively identify the cases in which its application may be necessary.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 DISCUSSION
 References
 
Fifty-four consecutive patients were submitted to video-assisted thoracoscopic resection of single or multiple lung nodules for diagnostic or therapeutic reasons. Preoperatively, all patients underwent chest roentgenogram, posterior and anterior view, and high-resolution spiral computed tomographic (CT) scan of the chest (Marconi Mx Twin - Philips Best, Netherlands) that diagnosed 65 lesions with a median diameter of 15 mm and a range of 3 to 35 mm. Whole body positron emission tomographic scan (PET; Advance NXi – General Electrical, Buc, France) was adopted in 11 patients and was diagnostic for 2 lesions not revealed by the CT. Overall, a total of 67 lesions were documented at preoperative work-up.

Patient positioning was as per an axillary thoracotomy. Three 10 mm trocars were inserted independently of the location of the nodule, respectively through the fifth and seventh intercostal space on the midaxillary line, and through the sixth intercostal space on the anterior axillary line. This approach was preferred to a more selective trocar placement in order to correctly insert chest tubes (sixth and seventh space) and if necessary convert the fifth space thoracostomy incision in a vertical axillary thoracotomy.

The video camera was usually introduced through the port placed in the seventh intercostal space although it could be switched from this port to another. In all patients the nodules were judged intraoperatively using the video thoracoscope, whether visible or not. They were then judged whether palpable or not after a thorough direct finger palpation and using a laparoscopic 5 mm retractor to perform an indirect palpation of the lung. At first the area of the lung where the nodule was seen, or where it should allegedly be, was approached with the finger of the surgeon by lifting the lung with a Duval endograsper (Ethicon, Cincinnati, OH). If the maneuver was ineffective, the entire lobe was indirectly palpated with the retractor.

In the initial phase of our experience with the transthoracic intraoperative ultrasonography, the instrument was used in order to identify the nodules or to confirm the localization of the nodule within the parenchyma and to study the sonographic patterns of the lesions even if the nodule was visible or palpable [13]. Thereafter the intraoperative ultrasonography was performed when the nodule was not visible, or not localized, with direct or indirect palpation or at times when in doubt to confirm the video and/or palpatory findings.

The deflectable multifrequency (7.5 to 10 MHz) endosonography linear probe (LP13A, Laparoscopic Probe 7.5/10 MHz, ESAOTE S.p.a, Genova, Italy, www.esaote.com/products/ultrasound/au5/intraop.htm) was used along with the portable Hitachi-Esaote Spazio machine (ESAOTE, Genova, Italy). The diameter of the probe is adequate usage by a 10 mm thoracoscopic port. The flexible tip of the probe (two directions, ± 90 degrees both longitudinal and transversal) makes the probe easy to use and adequate to gather diagnostic information following the contour of the deflated lung within the chest (Fig 1).



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  		Fig 1. The deflectable multifrequency (7.5 to 10 MHz) endosonography linear probe (LP13A, Laparoscopic Probe 7.5/10 Mhz, ESAOTE S.p.a, Genova, Italy, www.esaote.com/products/ultrasound/au5/intraop.htm). The flexible tip of the probe (two directions, ± 90 degrees both longitudinal and transversal) makes the probe easy to use and adequate to gather diagnostic information.

 
The sonographic window was optimized by complete lung collapse after double lumen endotracheal tube positioning and lung exclusion from ventilation with selective bronchial mild continuous suction (Figs 1 and 2). In order to shorten the procedure time the lung was excluded from ventilation immediately after positioning the patient in the lateral decubitus on the operative table.



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  		Fig 2. Intraoperative image of the endosonography linear probe exploration of the lung parenchyma.

 
In all patients the diameter of the nodules and their orthogonal distance from the anterior, lateral, and posterior chest wall was measured on the preoperative CT chest scan. The intraoperative evaluation, visible or nonvisible, and palpable or nonpalpable, along with the metric measurements calculated on the CT scans, were used within a discriminant analysis. This was computed in order to identify which metric measurement correctly classified nodules whether they would be visible and/or palpable or nonvisible and nonpalpable. The statistical analysis was performed using the SPSS 11 software package (SPSS Inc, Chicago, IL) (RB).

Sensitivity and specificity of intraoperative localization by video, palpatory and transthoracic endosonographic approach of pulmonary nodules detected preoperatively by CT scan was determined. False positive identification of the nodules was determined based on the pathological documentation of the nodule within the wedge resection. The appropriate resection was also confirmed by the follow-up CT scan of the chest.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 DISCUSSION
 References
 
Sixty-nine nodules were resected with a median diameter of 15 mm and a range of 3 to 30 mm as documented by the pathology report (Table 1). Two nodules, not diagnosed at preoperative work-up, were identified during sonographic exploration of the pulmonary parenchyma. These were 4 and 7 mm in diameter. The first one was identified in a patient with poor pulmonary function while searching for CT scan diagnosed nodules suspicious for a fibrosarcoma metastasis. At pathology the metastatic nature of the nodules was confirmed. The second one was a satellite nodule in a patient with 2 nodules identified at preoperative work-up; all three lesions were judged as benign on quick section.


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  		Table 1. Findings at Pathology
 
Conversion to an axillary thoracotomy was performed in 7 patients; in 6 to perform an anatomic lung resection and in one because the nodule could not be localized other than with manual palpation. In 12 patients the fifth intercostal space thoracostomy was converted in a minithoracotomy; in 7 patients to perform a video thoracoscopic lobectomy, in 4 patients a wide wedge resection was performed for non-small cell lung cancer (NSCLC) in patients with poor respiratory function, and in 1 patient to manage a postresection (mechanical) hematoma.

Table 2 documents the dimensional characteristics of the 65 nodules identified by the preoperative CT scan of the chest; furthermore the visible and/or palpable characteristics at the video thoracoscopic inspection are shown. The nodules classified as visible and palpable were 36 of 65 (55%) and their median diameter as per CT scan measures, was 15 mm (range, 5 to 35). The nonvisible but palpable nodules were 13 of 65 (20%) and their median diameter was 14 mm (range, 3 to 30). Those that were found to be nonvisible and nonpalpable were 16 of 65 (25%) with a median diameter of 15 mm (range, 4 to 22).


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  		Table 2. Computed Tomographic Scan Diameter and Intraoperative Findings
 
Intraoperatively, 45 of the preoperatively diagnosed nodules were investigated by ultrasonography and 42 were identified thus with a sensitivity of 93%. The median time of ultrasonographic inspection was 15 minutes (range, 9 to 35).

Of the three nodules that were not identified by transthoracic echography [13], one was 15 mm in diameter embedded in a severely emphysematous parenchyma although it resulted as palpable and was successfully resected. The second one was a 5 mm nodule, not visible although palpable at thoracoscopic assessment, and the third one was a 20 mm nodule that resulted as neither visible nor palpable and required, for the purpose of identification, conversion to an open procedure.

When considering the nodules judged not visible and not palpable the ultrasonography identified 15 of 16 of the nodules preoperatively diagnosed by the CT scan of the chest, thus with a sensitivity of 95%. In total, the nonvisible and nonpalpable nodules were 19 of 69. Sixteen were diagnosed preoperatively by CT scan of the chest; 2 by PET, only one of which was a NSCLC and one a pulmonary sequestration, and 1 was identified intraoperatively during the endosonographic exploration of the lung parenchyma while searching for a preoperatively diagnosed nodule and at pathology was found to be an inflammatory nodule. Table 3 shows the findings at pathology of all the nonvisible and nonpalpable nodules.


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  		Table 3. Nonvisible and Nonpalpable Nodules
 
The sensitivity of the video, palpatory, and ultrasonographic approaches for the intraoperative identification of the nodules that were diagnosed preoperatively by the CT scan was 98.5%. In the entire series none of the wedge resections resulted in a negative result at the pathological quick section; in other words no false positive resections were performed. Furthermore, the postoperative CT scan of the chest confirmed in all cases the appropriateness of the resection. Therefore, the specificity of the video, palpatory, and endosonographic approaches was 100%, and thus also the specificity of transthoracic endosonography in identifying the nodules was 100%.

The presence of severe emphysema, the proximity to a fissure or to the hylum caused, in 33% of the nodules, an error in predicting the need of a dedicated localization procedure on the basis of the discriminant analysis function: -1.52587 + (0.13243 x CT diameter of the nodule in mm) – (0.03091 x shortest distance to the chest wall in mm). The discriminant function had a threshold that was at –0.207. Above the threshold, with increasing probability, the nodule is classified as visible and or palpable while below that threshold is classified as nonvisible and nonpalpable.


   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
DISCUSSION
 References
 
The evaluation and management of solitary pulmonary nodules is a challenging problem in pulmonary medicine because the diagnosis may range from benign granulomas to lung cancer. A solitary pulmonary nodule is defined as an intraparenchymal mass less than 3 cm in diameter, not associated with telecasts or adenopathy [14, 15].

The so-called Bayesian approach in the management of pulmonary nodules estimates the prevalence of malignancy in the population, assesses risk factors predictive of malignancy as demonstrated by history and chest radiography, and selects a management strategy based on the adjusted probability of malignancy [15]. In adjunct to the probability of malignancy, consideration must be given to the surgical risk for the patient. Diagnostic techniques should be applied only if a negative result will be sufficient for the clinician to elect a strategy of observation rather than intervention. These considerations are fundamental both for de novo diagnosis of solitary pulmonary nodules and for cases of multiple nodules suspicious for metastasis.

Computed tomography, along with densitometry, transthoracic needle aspiration biopsy, bronchoscopy, and PET all come into the equation in the diagnostic process, although all are characterized by significant false negative results, low yield, or complications depending on the nature and position of the nodule, and the characteristics of the surrounding parenchyma [2–4], [15, 16].

Video-assisted thoracoscopic surgery is a minimally invasive technique that has become available for the evaluation of indeterminate pulmonary nodules and is associated with virtually no mortality and minimal morbidity [17–19]. Its role within the management of indeterminate solitary pulmonary nodules or of NSCLC in patients with poor lung function is well accepted. Debated is, instead, its application towards the management of intrathoracic metastases [18, 20, 21]. Potential disadvantages in all contexts include the inability to identify deep parenchymal lesions, to not be able to manually examine the lungs, as well as the need to reposition the patient for a bilateral exploration [20–22].

As already discussed in the literature, failure to identify a malignant nodule during thoracoscopic exploration is certainly a possibility. Multiple techniques to appropriately aim the thoracoscopic resection have been reported [23–28]. Most require invasive procedures to locate the nodules and cumbersome logistics with coordination between the interventional radiology suite and the operating room. Failure of the localization technique applied by interventional radiology has been reported, ranging from 13% for the methylene blue to 47% with the hook wire technique and an overall failure to localize the nodule intraoperatively during video-assisted thoracoscopic surgery of 7.5% as reported in two large multicenter trials [7, 8].

In our institution we adopted the intraoperative transthoracic ultrasonography to be applied during the thoracoscopic procedure. It proved to be a versatile instrument for the localization of nodules. The collapsed lung at echographic inspection has the same appearance of a solid organ, permitting the inspection of the parenchyma (Fig 3). The probe that we adopted is particularly user friendly due to the flexibility of the sonographic head permitting adequate inspection of the contours of the lung. After an initial learning curve, performed in collaboration with the radiology house staff, our sonographic inspection time became acceptable. Currently, we perform the transthoracic ultrasonography only when the nodule is not visible and not palpable.



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  		Fig 3. (A) Shown is the echographic image of the collapsed lung that assumes solid organ echogenicity. (B) Shown is the echographic evidence of a lung nodule.

 
As observed in Table 4 the need for a localization method, other than the visual and palpatory inspection, was required in about 30% of the nodules similar to what others have observed [29]. Thus, the majority of cases do not require any type of localization method. For the nodules that at thoracoscopic visual inspection along with indirect palpation were neither visible nor palpable, the sensitivity and specificity of the endosonographic inspection was 94% and 100%, respectively.


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  		Table 4. Discriminant Analysis Classification Matrix
 
The overall sensitivity and specificity for the intraoperative video-palpatory-ultrasonographic approach for the identification of the nodules preoperatively diagnosed by CT scan was 98.5% and 100%, respectively; for only one nodule (1.5%) the approach failed to identify the lesion thus requiring a conversion to the open procedure to localize the nodule. This is significantly better than what has been reported by the multicenter trials for other localization methodologies [7, 8, 30].

Recent literature has proposed various algorithms using metric measurements calculated on the CT scan images in order to predict the need for a localization method [9, 31]. Using similar predicting methodology we found that the presence of severe emphysema or the proximity to a fissure or to the hilum caused an error in predicting the necessity of a dedicated localization procedure in 33% of the cases. This problem is easily overcome by the significant advantage of the transthoracic endosonography bedside availability compared to the other methods. In other words, you use it when you need it, thus avoiding the effort to plan and coordinate any interventional radiology suite, staff, and procedure. It also avoids any morbidity related to the interventional localization method. You do need the support of the radiology department to provide the expertise to read the scan, which is certainly of a lesser logistic impact.

A potential downside in adopting this technology is that the probe has an initial substantial cost. On the other hand it could be easily absorbed within a surgical department that may use it also for laparoscopic abdominal solid organ inspection.

In conclusion intraoperative transthoracic ultrasonography is a useful tool to guide video thoracoscopic resection of lung nodules, being highly efficient and with absolutely no morbidity related. It has the potential to reveal lesions occult at the preoperative imaging and may play a future role as the tool to adequately inspect the lung as per a good oncologic approach before any type of video thoracoscopic resection, whether a wedge or a lobectomy. The application of this technology to substitute the manual inspection of the thoracic organs during video thoracoscopic procedures dedicated to neoplastic diseases, whether primary or secondary, should be further investigated with a multicenter trial.

The need of a localization method in order to accomplish video-assisted thoracoscopic resection of pulmonary nodules is difficult to accurately predict on the basis of the computed tomography of the chest. Therefore, the possibility of adopting an intraoperative method only if truly necessary provides the opportunity to reduce health care costs and help the daily routine, particularly within a busy general thoracic surgery division.


   DISCUSSION
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 DISCUSSION
References
 
DR MICHAEL T. JAKLITSCH (Boston, MA): I congratulate you on an excellent study. We played with this for a little bit in our operating room on patients who actually came to open metastasectomy. We had a different machine than you had. We, basically, were using the ultrasound probe that they use to look for plaques on ascending aortas, so we had 10 MHz and 12 MHz. I noticed that you commented that you need complete atelectasis of the lung. Even a little bit of lung, and the alveoli, produce considerable scatter, so it made it really hard for us to find what we were interested in, which was small nodules, less than a centimeter, more than a centimeter away from the surface of the lung; in other words, the small nodule that you can't feel, that’s too small to put a wire into by CT-guided probes. For complete atelectasis, sometimes it takes an exceedingly long time. So that was one problem that we felt with it. Secondly, I think the small, deep nodule is the area where we need help with this kind of technology. Have you tried to expand this clinical work now back to the laboratory? We have not pursued this, but it seemed to us that if you had some method of maybe flooding the segmental airway with saline from a bronchoscopic-placed catheter that then could reduce your scatter and might improve your ability to detect these very small nodules. I congratulate you again on a great paper.

DR DADDI: Can you please repeat the first question again? I didn’t understand it.

DR JAKLITSCH: The amount of time required for complete atelectasis and what type of maneuvers you can utilize to speed that process, and, secondly, our perception that there’s diminishing returns on your ability to detect, which is a function of both diameter size in the subcentimeter range and distance away from the pleura.

DR DADDI: Thank you Dr Jaklitsch for your comments. In response to your first question regarding the amount of time required for complete atelectasis, we usually start, following intubation with a double lumen tube before patient positioning, to collapse the lung of choice by adding a mild suction within the airway using an endotracheal suction catheter. By using this strategy we have found that, for adequate lung collapse, 40 minutes of total time are usually necessary, but actually only about 10 minutes of true operative time from when we gain access to the pleural cavity. This is our experience in emphysematous patients that generally require longer times. In nonemphysematous patients lung collapse is obtained in less than 30 minutes. We experienced extended length of lung collapse time only in one case.

With regards to your second question the purpose of this study was to investigate the use of preoperative work-up information given by the CT scan of the chest in order to predict the need of dedicated intraoperative techniques for the localization of the aimed pulmonary nodules. Furthermore, to study the validity of the intraoperative approach of visual inspection, indirect palpation and echographic inspection might be necessary to complete the search of target nodule and thus, whenever possible, VATS resection might be performed.

Also, our findings suggest a poor predictability using the CT scan information on whether or not a localization technique is required, and in most cases this is due to inadequate information on the distance from the target nodule to the fissure and on the relationship with the vascular structures when the nodule is close to the hilum. Obviously if the pulmonary nodule is too close to hilum or too deep, we proceed through the standard thoracotomy. I don’t know if there is any other information you would like to know.

DR DEMEESTER (Los Angeles, CA): He asked about flooding the bronchus with saline or something.

DR DADDI: This is a good point, but actually we didn’t utilize this technique. It’s a nice idea, but we didn’t do that.

DR FRANK C. DETTERBECK (Chapel Hill, NC): Is there a learning curve associated with this technique, and did you experiment first either in other patients or open procedures or something like that to get that learning curve behind you?

DR DADDI: Yes, we did. In the first 35 patients we always used the intraoperative ultrasound probe localization of lung nodules, of which a consistent percentage were visible and palpable. This first period of our experience was previously described (Eur Radiol. 2003;13:2358–64). That study was focused on peripheral nodules, clearly visible on VATS, first to have our radiologists gain experience with the methodology and second, for us, this first period was particularly important to learn how to maneuver the probe efficiently. So to answer your question, yes to use this kind of instrument you surely need a learning curve as for all new techniques, in order to avoid a fishing expedition.

DR DOMINIQUE GRUNENWALD (Paris, France): I enjoyed your excellent presentation. One thing is to localize the nodules and another thing is to resect them. How did you resect these nonvisible, nonpalpable, small nodules that are deeply inside the lung? Did you convert for that?

DR DADDI: Well, as I mentioned before, our approach to the lung nodules follows a precise protocol. We analyze the clinical data, and perform a visual and palpatory exploration of the parenchyma. If the nodule is not identified we then use the transthoracic ultrasonography. This is also used at times to confirm the visual and palpatory findings, particularly if the nodule is suggested to be deep into the parenchyma, thus too close to the hilar vascular structures. If the nodule was too deep into the parenchyma and too close to the hilum and this was confirmed by the endosonography we converted to an open procedure. In our case series 7 patients were converted to an axillary thoracotomy. As part of our protocol we always also investigate the rest of the parenchyma using the visual, palpatory, and endosonographic approach. Particularly in a patient with metastatic disease, extended investigation should be adopted.

All wedge resections are immediately sent to the pathologist, and, if on quick section a NSCLC is diagnosed, a lobectomy is favored either by VATS or by full thoracotomy along with a complete lymph node dissection.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 DISCUSSION
 References
 

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