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Ann Thorac Surg 2000;70:1847-1852
© 2000 The Society of Thoracic Surgeons

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Original article: general thoracic

Transxiphoid video-assisted pulmonary metastasectomy: relevance of helical computed tomography occult lesions

^a Department of Thoracic Surgery, Tor Vergata University, Rome, Italy
^b Department of General Surgery, Calai Hospital, Gualdo Tadino, Italy

Address reprint requests to Dr Mineo, Cattedra di Chirurgia Toracica, Università Tor Vergata, P.le Umanesimo, 10, 00144 Rome, Italy
e-mail: mineo{at}med.uniroma2.it

Presented at the Thirty-sixth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 31–Feb 2, 2000.

	Abstract

Top Abstract Introduction Patients and methods Results Comment Acknowledgments Discussion References

 
Background. The new transxiphoid video-assisted approach allows manual palpation of both lungs, thus permitting better evaluation of helical computed tomography (CT) in detection of pulmonary metastases.

Methods. From December 1995 to May 1999, 22 patients underwent a transxiphoid video-assisted pulmonary metastasectomy. Manual palpation of both lungs was possible in 18 patients, whereas only 13 had radiologic evidence of unilateral disease. Primaries were colon-rectum (n = 8), kidney (n = 3), uterus (n = 2), larynx (n = 2), limb osteosarcoma (n = 2), and one each of breast, skin melanoma, prostate, fibrosarcoma, and ovary.

Results. No perioperative death occurred. Fifty-eight lesions, 49 metastatic, were resected, whereas only 46 had been predicted by helical CT scan. Twelve occult lesions were discovered, eight of which were malignant. Overall sensitivity for proved metastases was 83.7% (41 of 49) and 75.8% (22 of 29) for those less than or equal to 5 mm. Mean follow-up was 15.27 months. Only 2 patients had pulmonary relapse at 6 and 12 months.

Conclusions. Despite helical CT, occult metastases may still be identified in almost one-third of the patients. The transxiphoid approach allows routine bilateral palpation and safe resection, and overcomes this critical limitation of video-assisted metastasectomy.

	Introduction

Top Abstract Introduction Patients and methods Results Comment Acknowledgments Discussion References

 
Resection of pulmonary metastases remains the standard of care for selected patients with resectable metastases isolated to the lungs, and is associated with a 5-year survival rate of 21% to 68% [1, 2]. Frequently, radiologically occult metastases are discovered intraoperatively by manual palpation of the lung, and this observation [3] has led to the suggestion of intentional bilateral exploration in selected patients [4–7]. Nevertheless, the usefulness of aggressive bilateral approaches has been questioned in patients with radiologically unilateral disease [8]. Moreover, there is some evidence that the new generation of helical computed tomography (CT) scans may improve preoperative detection of pulmonary metastases so as to potentially preclude manual palpation of the lung [9–11].

Recently, video-assisted thoracic surgery (VATS) has been proposed as a less invasive approach for resection of unilateral metastases in selected patients [12]. Unfortunately, without manual palpation, the probability of missing occult metastases during VATS procedures is very high [3]. To overcome this limitation, we recently developed a transxiphoid approach that allows bilateral manual palpation of the lung at VATS metastasectomy [13]. The minimal invasiveness and the safety of this approach allowed us to routinely carry out bilateral manual palpation of the lung even in patients with radiologically unilateral disease.

We assessed the reliability of transxiphoid bilateral manual palpation of the lung in detecting occult metastases after preoperative helical CT.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment Acknowledgments Discussion References

 
Study population
Between December 1995 and May 1999, pulmonary metastasectomy of the lungs was performed in 36 patients. Informed consent was obtained from all patients. Twenty-two patients, 16 men and 6 women, with mean age of 61.77 years, were explored through the transxiphoid video-assisted approach. The primary tumors resected were carcinoma of the colon-rectum (n = 8), kidney (n = 3), uterus (n = 2), larynx (n = 2), limb osteosarcoma (n = 2), and one each of breast, skin melanoma, prostate, back fibrosarcoma, and ovary.

Preoperative investigations
For most patients, the presence of metastases was first discovered during routine chest roentgenogram examination or CT scan carried out during a follow-up program. Most of the patients were asymptomatic (n = 16). Main symptoms were dyspnea (n = 5) and weight loss (n = 4). The mean disease-free interval was 36.95 months (range 0 to 204 months). After the discovery of lung metastases, all patients underwent further examination to exclude primary or extrapulmonary recurrence. The lung lesions were also restaged immediately before planned surgery by the means of helical chest CT scan (Tomoscan SR 7000; Philips Medical Systems, Eindhoven, The Netherlands). Mean interval between helical CT scan and surgical exploration was 8 days (range 4 to 15 days). The scanning protocol included a tube voltage of 120 kVp, tube current of 250 mA, slice thickness of 5 mm, and table increment of 5 mm per rotation. No intravenous contrast medium was administered. Reconstruction was performed at 5-mm intervals, and images were printed at window center -530 H, and window width 1,500 H.

The number of the lesions was independently evaluated from hard copies by three experienced radiologists and recorded in a specific form also indicating the maximal size in millimeters and segmental localization according to the slice position. Possible nature of the lesion, either malignant or benign (ie, vascular images, chondroma and scar tissue), was recorded as discriminators for postsurgical evaluation. Results were eventually discussed in a mixed panel of radiologists and thoracic surgeons during preoperative conference. Both the panel consensus (Table 1) and separate opinions of the physicians involved (Table 2) were used to formulate the tests of significance.

Operative details
After general anesthesia was induced, and a double-lumen endotracheal tube positioned, the patient was rotated 60 degrees from supine. Exploration was begun on the side with the greater number of metastases or when a more difficult resection was anticipated. After the exploration by thoracoscopic trocar inserted at the fourth intercostal space midway between midclavicular and anterior axillary lines, another two ports were performed in the fifth and seventh intercostal spaces along the posterior and midaxillary lines, respectively (Fig 1). A midtransverse arcuate skin incision was performed just along the inferior margin of the rib cage and the xiphoid was resected without entering the peritoneal cavity. The rectus abdominis muscles were separated along the linea alba for a few centimeters to facilitate hand introduction. Under thoracoscopic visualization, the assistant introduced one hand below the sternum and dissected bluntly the retrosternal areolar tissue. The mediastinal pleura was incised by a thoracoscopic dissector, thus allowing the whole hand to enter the cavity. The entire lung, either partially inflated or totally deflated, was carefully palpated between thumb and forefinger (Fig 1) according to a precise sequence regardless of radiological findings and thoracoscopic appearance. Thereafter, all areas identified by helical CT to be sites of metastases were specifically explored. All palpated nodules were resected with minimal resection by an endoscopic stapling device or laser beam. Size and exact location of the resected nodules were recorded immediately in the same form used for the radiographic localization of the metastases. All resected nodules were sent separately for histologic analysis.

View larger version (45K): [in this window] [in a new window]   Fig 1. Palpation through transxiphoid approach and setup of surgical instruments.

Follow-up
Adjuvant chemotherapy was performed in all patients with osteosarcoma and with laryngeal cancer. After pulmonary metastasectomy, patients underwent total body CT twice per year for the first 2 years; ultrasound, bone scan, and laboratory examination were also performed when symptoms of recurrence occurred.

	Results

Top Abstract Introduction Patients and methods Results Comment Acknowledgments Discussion References

 
There was no operative mortality nor major morbidity. The mean hospital stay was 4.6 ± 1.89 days (range 3 to 10 days), and this is significantly shorter than the time to discharge in our patients who underwent single-wedge resection through a thoracotomy (6.1 ± 2.02 days). According to the visual analogue scale (score 0 to 10), mean basal pain was scored 4.5 at 6, 3.2 at 12, and 1.5 at 24 hours postoperatively, points analogous to those scored after a normal VATS. Fifty-eight nodules were palpated and resected; only 46 had been predicted by CT. Forty-nine nodules contained metastasis at histologic examination. Twenty-three nodules were located in the upper lobes (12 right, 11 left), 28 in the lower lobes (12 right, 16 left), and seven in the middle lobe. Five lesions were located in the visceral pleura. The mean diameter of the resected nodules was 10.00 ± 8.91 mm, and for histology-proved metastatic was 10.36 ± 9.54 mm. Size for nodules and metastases are showed in Table 1. Mean operative time for procedures including bilateral exploration was 118.9 ± 26.39 minutes (range 95 to 170 minutes). There was no need of conversion to thoracotomy with spreading of the ribs. Twenty-three lesions were resected by laser and 35 by stapler.

There were 7 patients with occult metastasis (31.8%). Five patients (5 of 13) who had predicted unilateral metastases at CT scan were confirmed to be unilateral, whereas 4 (4 of 13) were proved bilateral. In another 4 patients with unilateral lesions, contralateral exploration was not possible because of the adhesions.

Bilateral palpation allowed the discovery of 12 unexpected, radiologically occult, lesions (Table 1); 8 of these were malignant at pathological review. Sensitivity and positive predictive value for the size and location of the lesions and for the different CT radiologists are shown in Tables 1 and 2. CT scan images were reviewed by the radiologists on the basis of the operative notes. Seven of eight false negatives were correlated to small sized lesions difficult to visualize or to discriminate from blood vessels (Table 2). The last case was represented by a 10-mm mass sited on the visceral pleura and judged to be of inflammatory origin.

Because of the lack of precise radiological features identifying a benign lesion, the true negatives and related parameters (ie, specificity and negative predicted value) were not considered for statistical analysis. The radiological opacities predicted benign and confirmed at histology were four, two, and six for each of the single radiologist, and four for the panel consensus. In these cases, lesions were chondrohamartoma (n = 4) and chronic inflammation (n = 2). False positives had a wide variation for each radiologist (Table 2), and in most instances, it was not possible to palpate any abnormality. On the basis of the panel consensus, there were five false positives and they were likely related to pleural scar (n = 2) and benign nodules (n = 2). The last one, not palpable, was retrospectively attributed to cross section of a small blood vessel. Both the benign nodules were enlarged at CT examination repeated 6 months after the first.

Lesions greater than or equal to 5 mm and those situated in the visceral pleural had the higher numbers of both false negatives and positives (Table 2). According to the panel consensus, sensitivity for the smaller metastases was rated 75.8% (22 of 29) versus 95% (19 of 20) for the others, and 60% for pleural metastases versus 86.3% for those that were intrapulmonary.

After a mean follow-up of 15.27 ± 9.31 months (range 2 to 42 months), no patients had a subxiphoid incisional hernia. Only 2 patients developed pulmonary metastases at 6 and 12 months, respectively; 1 of these belonged to the group of patients with unexplored hemithorax, and metastasis grew in this specific area. We also found 1 patient who relapsed with brain metastasis at 24 months from the pulmonary metastasectomy and another patient who had a pelvic recurrence after 6 months from the metastasectomy and after 22 months from a left hemicolectomy for a rectal carcinoma.

	Comment

Top Abstract Introduction Patients and methods Results Comment Acknowledgments Discussion References

 
Accurate thoracic imaging of patients with pulmonary metastases is critical to select those patients for whom resection is suitable, and palliate those patients for whom resection carries more risk than benefit [14, 15]. Furthermore, reliable prediction of the metastatic disease in one or both lungs allows the surgeon to select the most appropriate surgical approach. Sternotomy would be preferred for bilateral metastases of any histology and for all sarcomas, and single thoracotomy or VATS may be considered for selected patients with unilateral metastases.

Imaging accuracy for pulmonary metastasectomy is critically important when considering VATS techniques [16]. Indeed, VATS presents a suitable modality for diagnosis of most undefined peripheral pulmonary nodules including pulmonary metastasis [12]. However, VATS does not allow manual (eg, thumb-forefinger) palpation, which still remains the most accurate method of detection of metastases [3]. Accurate and high-resolution CT remains the main guide to metastasectomy. Unfortunately, in all studies that have correlated imaging prediction to surgical exploration (which, implies manual palpation, see Table 3), the risk of missing lesions is very high [17–19]. A prospective study undertaken to compare the VATS capability in detecting unexpected metastases with that of CT and open thoracotomy was prematurely closed to accrual, showing a 50% probability to miss metastases by a combination of CT plus VATS [3]; this observation was likely because of the impossibility of performing manual palpation during VATS procedures.

Waters and colleagues [10] reached similar conclusions from a radiological-pathological study performed in an animal model: 4 dogs affected with osteosarcoma in which a total of 132 lung metastases were found at pathological examination. In this study, sensitivity for metastases greater than 5 mm was 90.9%, whereas for metastases less or equal than 5 mm, the sensitivity was 44.4%.

The confidence and reliability that we have acquired with the transxiphoid VATS approach for lung metastasectomy [13] allow us to propose routine manual palpation of both lungs regardless of the presence of unilateral or bilateral nodules on preoperative radiographic imaging. The VATS approach proved safe and effective, with advantages such as less postoperative pain, shorter in-hospital stay, and easier patient acceptance. All the lung regions can be palpated as during a median sternotomy. Compared with this approach, difficult resections, such as for metastases located in the left lower lobe, can be facilitated having one hand guided by the camera device with the patient lying in a nearly lateral decubitus.

With routine bilateral palpation of both lungs, we examined whether a bilateral but less invasive technique may be justified in patients with radiologically unilateral metastases. Using this technique, we tested the reliability of helical CT in detecting lung metastases of different sizes. In our selected population, manual palpation was able to identify 20% (12 of 58) of helical CT occult or misdiagnosed lesions; 67% (8 of 12) of them proved metastatic at histologic examination, (three from renal carcinoma and only two from sarcoma). On the other hand, 11% (5 of 46) of the lesions deemed metastatic by the CT were benign. These findings are concordant with those reported by McCormack and colleagues [3] in a prospective trial, where the error rate of conventional CT is estimated to be 50%, even in the case of patients with only one lesion diagnosed. A more important outcome would be the probability of missing an occult contralateral metastasis based upon preoperative radiographic evidence of only unilateral metastases. Four patients who had predicted unilateral at CT scan were proved to have bilateral metastases. One of the 2 patients who developed pulmonary metastases belonged to the group of patients in which the hemithorax, diagnosed as clear of metastases, was not explored because of adhesions.

Single radiologist variability was consistent (Table 2), leading to a panel consensus opinion for the CT sensitivity. A subjective capability of detecting more metastases may lead to an overestimation of the number of metastases in smaller lesions.

Even with the limits in evidencing lesions with a diameter less than 3 mm [10] and centrally located nodules [11] and the incapacity in differentiating benign from malignant nodules, manual palpation followed by surgical exploration represents the standard evaluation for determining CT accuracy. Indeed, palpation allows to identify and physically characterize very small nodules before resection, and resection of benign nodules should not be interpreted as a limitation of the technique, as it is capable of more precisely determining the extent of the disease. We consider surgical exploration necessary for diagnostic purposes; indeed, it has been our observation that benign lesions may enlarge during evaluation, thus mimicking metastasis.

In conclusion, despite the introduction of helical CT, failure to image small and pleural metastases still occurs. One-third of our patients presented occult lesions at palpation. Manual palpation of lung parenchyma between the thumb and forefinger allows for detection of these occult nodules. This technique is consistent and reliable. The transxiphoid VATS approach allows selected patients routine bilateral palpation of the lung. We found that this technique reduces the chance of missing CT occult metastases and minimizes the risk of false-positive imaging.

	Acknowledgments

Top Abstract Introduction Patients and methods Results Comment Acknowledgments Discussion References

 
This study has been carried out within the Research Fellowship Program Dottorato di Ricerca in Oncologia Toracica, appointed by Tor Vergata University of Rome, and it was supported by a grant from MURST (60%).

	Discussion

Top Abstract Introduction Patients and methods Results Comment Acknowledgments Discussion References

 
DR JOE B. PUTNAM (Houston, TX): Doctor Ambrogi, I enjoyed your presentation and agree with your comments that CT scans, even our high-resolution CT scans, are often inadequate in identifying occult metastasis. Only 22 patients had this procedure over a 4-year period. I would like to know your selection criteria for these patients and why these particular patients were selected. How many patients in total had resection of pulmonary metastases during this period?

Secondly, how often did you convert from the subxiphoid approach to thoracotomy for complications, such as bleeding or other organ injury? Finally, have you attempted to use this technique for greater resections, such as lobectomy or pneumonectomy? Thank you.

DR AMBROGI: I showed you, Dr Putnam, the criteria we included. Twenty-two is quite a low number, and it represents almost one half of the entire population of the patients who underwent metastasectomy. This probably should be the limit. For the moment we did not try to do lobectomy through this approach, but I guess there is no reason not to consider it in the future. I did not grasp the second question.

DR PUTNAM: Once you got in there with your hand in the chest, did you have to extend the operation to include a lateral thoracotomy or median sternotomy for some other problem?

DR AMBROGI: There is this possibility. I think that inserting the hand inside the chest allows you to explore the whole lung and reduce conversion rate. Because of the strict selection criteria, we did not have the necessity of performing lateral thoracotomies but, when required, there is also the possibility for performing small thoracotomies by joining two port incisions.

DR DOUGLAS E. WOOD (Seattle, WA): I have just a simple technical question. I have no trouble with the ease with which one could reach the right middle lobe and lower lobe, but I am having trouble visualizing what it would be like to reach either upper lobe or the left lower lobe through this approach. Can you just describe to me how easy or difficult that is? I know from a median sternotomy, when I am working on the left lower lobe, I have to wait until the anesthesiologist is looking away.

DR AMBROGI: One of the limits of the technique could be cardiomegaly. If you have a big heart, we do not recommend this procedure because it is difficult to reach the lower lobe, the left lower lobe, but to do palpation with a normal heart in the side position is quite acceptable. We have no difficulties reaching even a lesion located at the level of the pulmonary ligament in the left.

DR WOOD: But you must need your whole arm in the chest to reach the upper lobe. I can picture getting it up to the wrist, but I have trouble picturing my forearm getting in that far.

DR AMBROGI: I know that it is probably difficult to believe, but at the highest level you cut, it is only necessary to insert the wrist. At the most, a few centimeters after the wrist, you can reach the top of the lung, depending on the size of the patient. Believe me, it is possible.

	References

Top Abstract Introduction Patients and methods Results Comment Acknowledgments Discussion References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Vincenzo Ambrogi Tommaso Claudio Mineo Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Ambrogi, V. Articles by Mineo, T. C. Search for Related Content PubMed PubMed Citation Articles by Ambrogi, V. Articles by Mineo, T. C.