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Ann Thorac Surg 2003;75:1607-1611
© 2003 The Society of Thoracic Surgeons

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Original article: general thoracic

Videothoracoscopic management of the solitary pulmonary nodule: a single-institution study on 429 cases

^a Thoracic Surgery Unit, Carlo Forlanini Hospital, Rome, Italy
^b The Biostatistics Service, Clinical Epidemiology Unit, Istituto Dermopatico dell’Immacolata, Rome, Italy

Accepted for publication November 13, 2002.

^* Address reprint requests to Dr Cardillo, Thoracic Surgery Unit, Carlo Forlanini Hospital, Via Portuense 332, 00149 Rome, Italy
e-mail: gcardillo{at}scamilloforlanini.rm.it

	Abstract

Top Abstract Introduction Patients and methods Operative technique Statistical analysis Results Comment Acknowledgments References

 
BACKGROUND: Solitary pulmonary nodules (SPNs) sometimes are malignant. We evaluated our 9-year experience in the videothoracoscopic (VATS) management of indeterminate SPNs in order to identify malignant nodules on the basis of clinical and radiologic characteristics.

METHODS: From July 1992 to May 2001, 429 patients (276 men and 153 women) were treated by VATS because of a SPN.

RESULTS: Three hundred and seventy lesions were benign (86.24%): mean age, 49 years; mean diameter, 1.8 cm; evidence of calcifications, 43 cases (11.62%); smokers, 201 cases (54.32%); history of previous cancer, 11 cases (2.97%). Fifty-nine lesions (13.75%) were malignant (52 NSCLC and seven metastases): mean age, 59 years; mean diameter, 2.31 cm; evidence of calcifications, two cases (3.38%); smokers, 40 cases (67.79%); history of previous cancer, 12 cases (20.33%). Solitary pulmonary nodules were succesfully resected by VATS in 333 (77.62%) cases (309 benign and 24 malignant). Minithoracotomy was necessary to locate the SPNs in 93 (21.67%) cases (61 benign and 32 malignant). Multivariate analysis showed that age greater than 55 years (OR 4.9), diameter of the lesion greater than 2 cm (OR 4.7), history of previous cancer (OR 17.7), and need for conversion to thoracotomy (OR 6.6) to locate the nodule were statistically significant factors in order to identify malignant SPNs.

CONCLUSIONS: VATS represents the approach of choice for both diagnosis and treatment of SPNs. The probability of malignancy for SPNs increases with size of the lesion, age of the patients, history of previous cancer, and the need for thoracotomy to locate the nodule.

	Introduction

Top Abstract Introduction Patients and methods Operative technique Statistical analysis Results Comment Acknowledgments References

 
A solitary pulmonary nodule (SPN) is defined as a round intraparenchimal lung lesion less than 3 cm in size, not associated with atelectasis or adenopathy [1]. In the past, lesions up to 6 cm in diameter were classified as nodules, but there is now an appreciation that an upper limit of 3 cm may be more useful; whereas any lesion greater than 3 cm is considered a solitary mass lesion [1].

Although most SPNs have benign causes (about 50% to 70%), many represent stage I lung cancer and must be distinguished from other benign nodules [2, 3]. Hamartomas are the most common benign lung tumor, comprising 75% of all benign tumors of the lung. On the other hand, malignant causes constitute about 35% to 50% of all SPNs [4–6], most of the cases being due to stage I lung cancers. Therefore, newly detected SPNs must be assumed to be malignant until proven otherwise. Furthermore, the evidence of a previous cancer may affect the probability of malignancy in SPNs.

In the present article, we evaluate our 9-year experience in the videothoracoscopic treatment of 429 patients with SPNs in order to confirm the diagnostic and therapeutic role of VATS and to identify factors able to predict the probability of malignancy of an indeterminate SPN on the basis of clinical and radiologic characteristics.

	Patients and methods

Top Abstract Introduction Patients and methods Operative technique Statistical analysis Results Comment Acknowledgments References

 
From July 1, 1992 to May 1, 2001, 2,377 VATS procedures were performed at the Thoracic Surgery Unit, Carlo Forlanini Hospital, Rome. Of these, 429 (18.0%) patients underwent VATS for the treatment of an indeterminate SPN. We excluded from surgery those SPNs with chest roentgenogram (or computed tomography [CT]) stability longer than 3 years.

There were 276 male (64.3%) and 153 female (35.6%) patients; the mean age was 49 years (range, 19 to 76 years). Of the 429 patients in the study, 23 (5.3%) had a history of cancer, and 406 (94.6%) had no known cancer at the time of VATS. A smoker was defined as a patient who smoked at least 20 packs per year. Two hundred and forty-one patients (56.1%) were smokers.

Routine chest roentgenograms (posteroanterior and lateral views), and high-resolution, low-dose/standard-dose chest CT scans were performed for all patients. Computed tomography was performed with a variety of different scanners, both helical and nonhelical, by using a section thickness of 5.0 to 10.0 mm. Positron emission tomography using 18-fluorodeoxyglucose as a marker was performed in 8 patients (1.8%). Before surgery, 295 (68.7%) patients underwent bronchoscopy, achieving no diagnosis in all cases. Methylene blue injection and CT-guided wire placement to localize small and deep SPNs were used in 10 cases (2.3%). Transthoracic fine-needle aspiration biopsy (FNAB) was performed in 21 patients (4.8%). Any minithoracotomy, even if performed only to palpate the lung, was defined as a conversion. The great majority of the procedures (401/429, 93.4%) were performed by one surgeon (MM).

Selection criteria for thoracoscopic resection of SPNs included a position in the outer third of the lung parenchyma, in a fissure, or in the hilum of the lung.

	Operative technique

Top Abstract Introduction Patients and methods Operative technique Statistical analysis Results Comment Acknowledgments References

 
All procedures were performed with the patient under general anesthesia and single-lung ventilation. The patient was placed in the lateral position with the arm abducted to allow superior displacement of the scapula. The first incision was always placed in the fifth or sixth intercostal space in the midaxillary line. A "0" degree telescope connected to a video camera was introduced through the first trocar, and two further trocars were introduced under thoracoscopic control. Carbon dioxide was never used. The lung was inspected and gently palpated by instrumental probing to localize the lesion. Enucleation was performed by the endoscopic cautery: in some cases, a no-knife stapler (NSB 45; Ethicon Endosurgery, Cincinnati, OH) was used to achieve hemostasis or aerostasis in the area of enucleation. Wedge excision was performed by an endoscopic stapling device (TSB 45/ATB 45; Ethicon Endosurgery). In most cases, the specimen was removed from the pleural cavity using a protective bag. In all cases, specimens were sent for intraoperative frozen section, and if a primary lung malignancy was proved, the procedure was converted to open thoracotomy for conventional lung resection and mediastinal lymph node dissection. At the end of the VATS procedure, if the water seal revealed a major air leak, the lung was routinely reinspected by the thoracoscope.

	Statistical analysis

Top Abstract Introduction Patients and methods Operative technique Statistical analysis Results Comment Acknowledgments References

 
Data analysis was performed using the SPSS/Windows (release 8.0) and STATA/Windows (release 4.0) statistical packages (SPSS Inc, Chicago, IL).

Odds ratios (OR) and 95% confidence intervals (CI) were calculated for age, diameter, smoking habits, evidence of calcifications, surgical procedure, and history of previous cancer using unconditional logistic regression models. Logistic regression models were built to allow for multiple adjusting of confounding, and thus, to identify variables independently associated with malignancy. In all models, age was considered as a categorical variable. Age and diameter, which were measured on a continuous scale, were dichotomizing by dividing in thirds the distributions of exposed controls, then adjacent categories were collapsed, when appropriate. For each variable, the reference category was the most favorable level of exposure.

	Results

Top Abstract Introduction Patients and methods Operative technique Statistical analysis Results Comment Acknowledgments References

 
There were neither intraoperative nor postoperative deaths in our series. No intraoperative complications were detected.

Morbidity included 13 cases (3.0%) of prolonged air leak (> 5 days), one case (0.2%) of apical detachment, three cases (0.6%) of subcutaneous emphysema, and two cases (0.4%) of bloody pleural effusion, resolved by thoracentesis. No case of wound infection was reported. One patient (0.2%) with prolonged air leak underwent redo VATS; aerostasis was achieved by means of fibrin glue. In 11 (2.5%) patients who underwent enucleation of a benign nodule either by VATS (seven cases) or by muscle-sparing mini-thoracotomy (four cases), no chest tube was left in situ.

Postoperative pain was graded as mild to moderate in 362 patients (84.4%), and severe in 37 (8.6%), excruciating in 12 (2.8%); no pain was assessed in 18 patients (4.2%). The average time of chest tube removal was 3.5 days (range, 2 to 11 days). Mean hospital stay was 4.6 days. Three hundred ninenty-six patients (92.3%) were able to return to work within 3 weeks after surgery

Pathologic examination of the resected specimen showed 370 (86.2%) benign lesions and 59 (13.7%) malignant lesions. Benign lesions included 309 (83.5%) hamartomas (benign mesenchymoma), 27 tuberculosis lesions (7.3%), 21 fibrous scars (5.7%), seven from granulomatous disease (1.9%), two fungal lesions (0.5%), two rheumatoid nodules (0.5%), and two amyloid tumors (0.5%)

Malignant lesions included 52 (12.1%) non–small cell lung cancers (NSCLCs) (31 acinar adenocarcinoma, 13 bronchioloalveolar adenocarcinoma, six typical carcinoid, one atypical carcinoid, one squamous cell carcinoma), and seven (1.6%) solitary pulmonary metastases. Treatment included 51 lobectomies and one bilobectomy plus radical mediastinal lymphadenectomy, in all cases through muscle-sparing thoracotomy.

Pathologic staging of the 52 resected NSCLCs showed T1N0 in 39 cases (75%), T1N1 in 10 cases (19.2%), and T1N2 in three cases (5.7%). Solitary pulmonary metastases showed origin from colorectal cancer in three cases, from malignant melanoma in three cases, and from kidney cancer in one case.

Of the 21 patients who underwent preoperative transthoracic FNAB, 18 (4.1%) showed a nondiagnostic result and 3 (0.6%) had a cytologic diagnosis of hamartoma. In the first group (nondiagnostic result), intraoperative examination of the resected specimen showed four NSCLCs and 14 benign lesions. In the latter group (cytologic diagnosis of hamartoma), intraoperative examination showed one unexpected adenocarcinoma and confirmed two hamartomas.

Among benign lesions, 43 SPNs (11.6%) showed evidence of calcification and 327 (88.3%) did not. Among malignant lesions, two SPNs (3.3%) showed evidence of calcification and 57 (96.6%) did not.

Among malignant lesions, 42 patients (71.1%) were older than 55 years, and 17 (28.8%) were younger; the mean age was 59 years. Among benign lesions, 118 patients (31.8%) were older than 55 years, and 252 (68.1%) were younger; the mean age was 48 years.

Among malignant lesions, 39 SPNs (66.1%) had a size greater than 2 cm and 20 (33.8%) had a size equal to or less than 2 cm; the mean size was 2.31 cm. Among benign lesions, 83 (22.4%) had a size greater than 2 cm and 287 (77.5%) had a size equal to or less than 2 cm; the mean size was 1.88 cm.

Among malignant lesions, 40 patients (67.7%) were smokers and 19 (32.2%) were not. Among benign lesions, 201 patients (54.3%) were smokers and 169 (45.6%) were not. Among malignant lesions, 12 (20.3%) patients (seven solitary pulmonary metastases and five NSCLCs) had an history of previous malignancy and 47 (79.6%) did not. Among benign lesions, 11 patients (2.9%) had an history of previous malignancy and 359 (97.0%) did not.

Among malignant lesions, 24 nodules (40.6%) were identified at VATS and 35 (59.3%) lesions could not be identified at VATS and required conversion to minithoracotomy. In the first group (24 VATS), 22 cases were converted to muscle-sparing thoracotomy in order to perform a formal lung resection plus radical mediastinal lymphadenectomy because of evidence of a primary NSCLC, and two cases underwent a VATS wedge resection with histologically proven free margins because of intraoperative evidence of a solitary pulmonary metastases. In the latter group (35 minithoracotomies), 30 patients underwent formal lung resection plus radical mediastinal lymphadenectomy because of evidence of a primary NSCLC, and 5 patients underwent wedge resection for solitary pulmonary metastases.

Among benign lesions, 309 nodules (83.5%) were identified at VATS, and 61 (16.4%) required conversion to minithoracotomy to locate the lesion.

All patients were included in the follow-up program, which ended on February 28, 2002, and included clinical history, physical examination, and chest radiographs every 6 months in all patients. Spirometry was performed only if judged to be necessary by the examining physician. No significant impairment of respiratory status was found in this series of patients.

Total-body CT scan was performed every year in cancer patients. Nineteen patients (4.4%) were lost during follow-up. The mean follow-up was 45 months (median, 43 months; range, 9 to 93 months).

Among 370 patients with benign lesions, 3 patients (0.8%) developed primary lung cancer, 2 in the same lung and 1 in the contralateral lung, respectively, 42 months, 53 months, and 73 months after surgical treatment of a hamartoma, and were successfully operated on. One patient died of myocardial infarction 39 months after surgery. Among 52 patients with NSCLC, 42 (80.7%) were alive with no evidence of disease, namely 36 T1N0 patients and T1N1 6 patients. Of the remaining 10 patients, 4 died of cancer (T1N1, 2 patients; T1N2, 2 patients), respectively, 40, 31, 12, and 9 months after surgery. One patient died of myocardial infarction (T1N0) 21 months after surgery, and 5 are alive with disease (T1N0, 2 patients; T1N1, 2 patients, T1N2, 1 patient).

Among 7 patients with solitary pulmonary metastases, 3 are alive with no evidence of disease (3 with colorectal cancer), 2 died of disease (kidney cancer and malignant melanoma), respectively, 9 and 11 months after surgery, 1 is alive with local and distant disease (melanoma), and 1 underwent thoracotomy because of local recurrence (melanoma).

	Comment

Top Abstract Introduction Patients and methods Operative technique Statistical analysis Results Comment Acknowledgments References

 
Several options are available in the diagnosis and treatment of a newly discovered SPN: observation for growth, biopsy, and resection. The appropriateness of each option depends largely on the assessment of a number of factors: the radiologic characteristics along with significant findings from patient’s history (age, smoking habits, history of previous cancer) and physical examination [7]. Evaluation of specific morphologic features of a SPN with conventional imaging techniques can help differentiate benign from malignant nodules and obviate further costly assessment. Small size and smooth, well-defined margins are suggestive of, but not diagnostic for, benignity.

Lobulated contour as well as an irregular or speculated margin with distortion of adjacent vessels are typically associated with malignancy. The presence of intranodular fat is a reliable indication of a hamartoma [2]. Some reports have stressed the value of contrast enhancement in differentiating between benign and malignant nodules, with relatively high sensitivity and moderately high specificity when enhancement thresholds of about 15 to 20 HU are used. The absence of significant lung nodule enhancement ( < 15 HU) is strongly predictive of benignity, even if further refiniments of this technique are needed [8–10].

The presence and pattern of calcification can help in differentiation if specific patterns of calcium deposition are manifest: diffuse, central, laminar, or popcorn. The popcorn-type calcification is pathognomonic for hamartomas. However, the mere presence of calcium in a lesion is inadequate to presume a benign origin, and our data confirm such hypothesis: two SPNs with evidence of calcification (diffuse and central) proved to be primary NSCLC.

The growth rate is also of paramount importance in evaluating SPNs, and a 2–3 year stability is traditionally considered an indicator of benignity [3, 11]. The application of a biological marker (18-fluorodeoxyglucose) in positron emission tomography (PET) scanning has offered the most accurate method of noninvasive diagnosis to date, with a reported predictive value varying between 77% and 100% accuracy [12–14].

There is considerable overlap in the internal characteristics of benign and malignant nodules, and the initial clinical evaluation often results in nonspecific findings, in which case, the nodules are classified as indeterminate and require further evaluation [2].

Traditional nonoperative diagnostic approaches to the indeterminate SPN include transthoracic FNAB. Although such a procedure is widely practiced, it is contraindicated or very difficult to perform in small lesions less than 1 to 2 cm. In addition, if the indeterminate SPN is considered benign or nondiagnostic on FNAB, the incidence of malignancy has been reported to be subsequently as high as 29% [15]. These data have been confirmed by our series, in which the nondiagnostic rate was as high as 85.71% (18/21); furthermore, 1 patient with an FNAB diagnosis of hamartoma achieved an intraoperative diagnosis of NSCLC.

Indeed, the practice of FNAB is often unnecessary in patients with small solitary pulmonary nodules, unless one is attempting to obtain a diagnosis in a patient unfit for surgery, or who is inoperable [16].

VATS has changed the management of SPNs. This procedure readily reveals the exact diagnosis, and offers an alternative approach to the traditional diagnostic methods, with the advantage of being 100% sensitive and specific, with no mortality and minimal morbidity [17–25]. Intraoperative frozen section determines the further surgical approach: if a lung cancer is documented, we proceed to thoracotomy with anatomic lung resection and mediastinal lymph node dissection. In metastatic disease, a VATS wedge resection with free surgical margins may represent the treatment of choice.

In the statistical analysis of our series, age greater than 55 years, diameter of the SPN greater than 2 cm, smoking habits (at least 20 packs/year), history of previous malignancy, presence of calcification in the pulmonary nodule, and type of procedure needed to identify the SPN (videothoracoscopy only or videothoracoscopy plus conversion to minithoracotomy) were considered as potential prognostic factors for a clinical prediction model in order to identify the possibility of a SPN to be malignant.

Univariate analysis of our series (Table 1) showed that the possibility for a SPN to be malignant is statistically significantly related to age greater than 55 years (OR 5.3; 95% CI 2.9 to 9.7), diameter greater than 2 cm (OR 6.7; 95% CI 3.7 to 12.2), smoking habits (OR 1.8; 95% CI 1.0 to 3.2), evidence of a previous malignancy (OR 8.3; 95% CI 3.5 to 19.9), and need of conversion to thoracothomy to find out the nodule (OR 7.4; 95% CI 4.1 to 13.3). The presence of calcification in the nodule was shown not to be statistically significant (OR 0.3; 95% CI 0.1 to 1.1), even if there is a trend towards a protective effect against malignancy. Multivariate analysis (Table I) confirmed age (OR 4.9), diameter (OR 4.7), smoking habits (OR 1.9), history of previous cancer (OR 17.7), and conversion to thoracothomy to locate the lesion (OR 6.6) to be statistically significant factors in order to identify malignant SPNs. The presence of calcification showed an OR adjusted to 0.3 (95% CI 0.1 to 1.5), with no statistically significant role.

	Acknowledgments

Top Abstract Introduction Patients and methods Operative technique Statistical analysis Results Comment Acknowledgments References

 
This study was partially supported by the "Progetto Finalizzato Ministero della Salute 2000." We wish to thank thoracic specialty nurses Daniela Colasanti, Amalia Barbato, and Alessandro Spano.

	References

Top Abstract Introduction Patients and methods Operative technique Statistical analysis Results Comment Acknowledgments 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): Giuseppe Cardillo Mohamed Regal Massimo Martelli Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Cardillo, G. Articles by Martelli, M. Search for Related Content PubMed PubMed Citation Articles by Cardillo, G. Articles by Martelli, M. Related Collections Lung - cancer