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Ann Thorac Surg 2005;80:2026-2031
© 2005 The Society of Thoracic Surgeons

Original article: General thoracic

Risk of Pleural Recurrence After Needle Biopsy in Patients With Resected Early Stage Lung Cancer

Haruhisa Matsuguma, MD a , b , * , Rie Nakahara, MD a , b , Tetsuro Kondo, MD a , b , Yukari Kamiyama, MD a , b , Kiyoshi Mori, MD a , b , Kohei Yokoi, MD a , b

a Division of Thoracic Surgery, Tochigi Cancer Center, Utsunomiya, Tochigi, Japan
b Division of Thoracic Diseases, Tochigi Cancer Center, Utsunomiya, Tochigi, Japan

Accepted for publication June 27, 2005.

* Address correspondence to Dr Matsuguma, Division of Thoracic Surgery, 4-9-13 Yohnan, Utsunomiya, Tochigi 320-0834, Japan (Email: hmatsugu{at}tcc.pref.tochigi.jp).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: Concerning the complications resulting from percutaneous needle biopsy (PNB), although cases of tumor seeding into the needle track have occasionally been reported, there were only two cases of pleural recurrences to date. The aim of this study was to elucidate the real risk of pleural recurrence after needle biopsy in patients with resected early stage lung cancer.

METHODS: Between 1986 and 2000, 335 patients with stage I nonsmall cell lung cancer underwent complete resection of the lung tumor. We retrospectively reviewed their medical records and investigated the relationship between the diagnostic methods used and the cancer recurrence patterns.

RESULTS: Preoperative diagnoses were obtained for 290 patients; 220 were diagnosed by bronchoscopy and 66 by PNB. Among the patients without a preoperative diagnosis, 27 were diagnosed by intraoperative needle biopsy and 14 by wedge resection of the lung. Tumors diagnosed by needle biopsy including PNB and intraoperative needle biopsy were smaller and showed less vessel invasion than those diagnosed by other methods (p < 0.01). After surgical resection, 9 patients had pleural recurrence and 1 patient, needle track implantation. Seven of these 10 patients were diagnosed by needle biopsy using 18G cutting type needle. Pleural recurrence or needle track implantation was observed for 8.6% of the patients who underwent a needle biopsy, whereas it was 0.9% for patients who were examined using other diagnostic modalities (p = 0.0009).

CONCLUSIONS: Needle biopsy especially using a cutting-type biopsy needle can cause a pleural recurrence in addition to needle track implantation.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Percutaneous needle biopsies (PNB) are widely used for the histologic diagnosis of a peripheral indeterminate pulmonary nodule. The overall sensitivity and specificity for diagnosing peripheral lung cancers were 90% and 97% respectively by meta-analysis [1], and even for tumors less than 2 cm in diameter the sensitivity was also as high as 91%.

Although fine-needle aspiration (FNA) is widely used method for performing PNB around the world, automated or semiautomated cutting needles have been tested to increase the diagnostic yield [2–8]. We also previously reported on the usefulness of computed tomographic fluoroscopy-guided transthoracic needle biopsy using an 18G automatic biopsy gun for diagnosing pulmonary lesions, particularly benign lesions [9].

The most frequent complication of PNB is pneumothorax, which occurs for 25% to 30% of patients [10]. For fatal complications of PNB, air embolism and tumor seeding have been previously documented to occur. Cases of needle track implantation accounted for almost all of the cases of tumor seeding, and have been documented to occur at a rate of 0% to 3% [11–13]. Although pleural recurrence due to tumor seeding is a possible adverse event that may occur after PNB [14], only two such cases have been reported [15]. Pleural recurrence after PNB tends to be ascribed to the advanced disease itself a priori, but not to PNB, because malignant pleural effusion or tumor dissemination in the pleural cavity can be seen after usual lung surgery without performing a needle biopsy, especially for patients with locally advanced nonsmall cell lung cancer (NSCLC). Thus, in the present study we investigated the risk of pleural recurrence after needle biopsy for patients with pathologic stage I NSCLC, who were thought unlikely to experience recurrence in the pleural cavity after resection.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
Patients
Between October 1986 and December 2000, 687 patients with NSCLC underwent surgical resection of the lung at our hospital. Among them, 335 had pathologic stage I disease, and they constituted the study population. Two hundred patients were men, and the median age was 67 years (range, 35 to 85). The majority of the patients underwent a lobectomy with systematic nodal dissection (n = 256, 76%). Histologic types were adenocarcinoma (n = 222), squamous cell carcinoma (n = 89), and others (n = 24), including large cell carcinoma, large cell neuroendocrine carcinoma, adenosquamous carcinoma, carcinoid, and carcinosarcoma. Primary tumors were classified as T1 in 210 patients and T2 in 125 patients.

Treatment Policy
Our routine diagnostic strategies for patients with an indeterminate pulmonary nodule were as follows. First, we obtained a histologic or cytologic diagnosis using fiberoptic bronchoscopy. If this failed or was difficult, the patients were then scheduled for diagnosis using PNB under computed tomography (CT) guidance. Almost all biopsies have been performed using an 18G, spring-loaded, automatic biopsy gun with a modified Tru-Cut type needle (Monopty; Bard Radiology, Convington, Georgia) since 1994 (n = 37), while the Tokyo Medical College needle (n = 12) and the Sure-Cut needle (n = 8) were frequently used before that time. If the state of the nodule remained undetermined, a diagnostic thoracotomy or thoracoscopy was subsequently performed. Some patients underwent intraoperative needle biopsy (INB) whereas the others underwent wedge resection of the lung. If a tumor was diagnosed as NSCLC by intraoperative pathology, the patient subsequently underwent complete resection of the tumor with curative intent. After surgery, the patients were scheduled for checkups, chest radiography, and measurement of serum tumor markers every 1 to 3 months for the first 2 years and every 6 months thereafter. When recurrence was discovered, intrathoracic and extrathoracic lesions were always surveyed.

Assessment of Recurrence and Clinicopathologic Features
We reviewed the medical records of all patients to confirm that recurrence had developed. Pleural recurrence was defined as pleural nodule or malignant effusion or both in the hemithorax of the operated side at the first relapse. Malignant effusion was diagnosed cytologically and pleural dissemination was diagnosed if multiple enhanced pleural nodules were observed on chest CT. Patients with any other site of recurrence in combination with pleural recurrence at the first relapse were included among the pleural recurrence cases, because we can not determine which recurrence preceded and caused the other recurrence. To elucidate the difference of tumor characteristics in each diagnostic group, we reviewed the CT images if available (n = 298) and classified these tumors into two categories according to their locations. When the center of a tumor shadow fell within the inner half of the lung, the tumor was classified as being central; and when the center of a tumor shadow fell within the outer half of the lung, the tumor was classified as being peripheral. We checked whether the tumor shadow was touching the pleura or not on the CT image and then examined the pathologic tumor characteristics such as tumor size, lymphatic invasion, and vascular invasion in the tumor in relation to the diagnostic method used. Pathologic stages were classified according to the criteria set forth by the International System for Staging Lung Cancer [16], and histologic typing was determined according to the World Health Organization classification [17].

Statistical Analysis
Correlations between the diagnostic methods used and the tumor characteristics were examined using the {chi}2 test and Fisher's exact test. The unpaired t test was used to examine the relationship between the diagnostic methods used and the log-transformed tumor sizes because of their skewed distribution. All statistical analyses were carried out using STATA software [18].


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
Among the 335 patients, 290 were diagnosed as having NSCLC preoperatively. Among them, the definitive diagnostic methods used were bronchoscopy for 220, PNB for 66, and sputum cytology for 4. Among the 45 patients with a pulmonary nodule without definitive preoperative diagnosis, INB was performed on 27, wedge resection of the lung on 14, and lung resection with curative intent without definitive diagnosis on 4.

Tumor Characteristics and Diagnostic Methods
The relationships between the methods used to obtain pathologic diagnoses and tumor characteristics are shown in Table 1. Tumors diagnosed by PNB showed less lymphatic invasion and were smaller than those diagnosed by bronchoscopy, and tumors diagnosed by INB were smaller and less invasive than those diagnosed by PNB. When we divided the tumors into two groups according to whether needle biopsy was conducted or not, we found that the needle biopsy group was associated with peripheral location, a smaller tumor size, and a lower occurrence of lymphatic and vascular invasion. Although tumors in the patients of the needle biopsy group were located in more peripheral areas, the numbers of tumors touching the pleura were almost identical. Furthermore, the incidence of pleural invasion of the tumors, which was thought to be associated with pleural recurrence, was lower for the needle biopsy group.


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  		Table 1. Relationships Between Diagnostic Methods Used and Clinicopathologic Tumor Characteristics
 
Recurrence
Two hundred and ninety-seven patients (88.7%) were followed up until February 29, 2004. Among the 38 patients not followed-up, 34 completed their follow-up after the 5-year anniversary of surgery. The median length of the follow-up period was 80 months, and the relationships between the methods used for histologic diagnosis and the recurrence patterns are shown in Table 2. Seventy-three patients were diagnosed as having recurrence, where the recurrence pattern was distant for 53 and local for 23. Among them, 3 had distant and local recurrence. Nine patients died of unknown causes; and as 1 patient was diagnosed with distant recurrence at an other hospital, we did not know whether pleural recurrence had developed. For the patients with local recurrence, 10 had pleural recurrence or needle track implantation. The percentage of cases for which distant recurrence had developed was similar between patients diagnosed by bronchoscopy and those diagnosed by PNB (18.5% versus 15.2%). However, the rate of pleural recurrence for the cases diagnosed by PNB was significantly higher than for the cases diagnosed by bronchoscopy (9.1% versus 1.0%, p < 0.0028). The rate of distant recurrence for the cases diagnosed by INB was small at 3.7%, but the proportion with pleural recurrence among the cases diagnosed by INB was as high as that for the cases diagnosed by PNB, at 7.4%. Combining the cases diagnosed by PNB with those diagnosed by INB into the needle biopsy group, the percentage of those affected by pleural recurrence for the needle biopsy group was significantly higher than that for the cases diagnosed using other diagnostic modalities (8.6% versus 0.9%, p = 0.0009).


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  		Table 2. Number of Cases According to Recurrence Pattern and Diagnostic Methods Used
 
The details of these 10 cases are shown in Table 3. All 10 tumors were adenocarcinoma; and the diagnostic methods used were PNB for 6, INB for 2, and fiberoptic bronchoscopy for 2 patients. Two tumors diagnosed by bronchoscopy showed pleural and vessel invasion that may have been related to pleural recurrence. On the other hand, all 5 pleural recurrence cases showing neither pleural invasion nor vessel invasion in the primary tumor were diagnosed by PNB or INB. The average size of the tumors was 2.7 cm with a range from 1.5 cm to 4.8 cm, and the depth from the visceral pleura to the tumor surface on the needle track during needle biopsy ranged from 0 cm to 2.5 cm. Only 1 patient underwent needle biopsy directly through the pleura attached to the tumor, and for only 2 (cases 1 and 4) the distances were less than 1 cm. In regard to surgical procedures carried out in the 10 patients, lobectomy was performed in 7 patients and segmentectomy in 3 patients (cases 3, 7, and 10). Video-assisted thoracic surgery approach was applied in only 1 INB case; however, subsequent resection was carried out under an open thoracotomy. Concerning the pneumothorax and hemothorax after PNB, 2 cases of pneumothoraces were observed among the 6 patients who underwent PNB. Their relapses occurred 12 to 69 months after surgery, and only 2 patients (cases 4 and 8) with a short follow-up period remained alive with the recurrence.


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  		Table 3. Clinicopathologic Characteristics of 9 Cases With Pleural Recurrence and Needle Track Implantation
 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
A number of needle track implantation cases have been reported, and the incidences were reported at 0% to 3% [12, 13, 19–22]. This rate was considered as negligible by some researchers [12, 23, 24] and as important by the others [15, 25, 26]. On the other hand, pleural recurrence after PNB has not been recognized as a real risk of PNB, although it is theoretically possible adverse event. Only two cases of pleural recurrence after PNB were previously reported [15]. Is the real risk of pleural recurrence due to PNB extremely low? We thought that many cases of pleural recurrence due to PNB may have not been reported because of the difficulty in proving its cause. We therefore conducted this investigation to elucidate the real risk of pleural recurrence after PNB. We hypothesized that pleural recurrence among patients with resected p-stage I NSCLC, especially with no pleural invasion, lymphatic invasion, and vascular invasion, was less likely to occur after surgery. Pleural recurrence, however, was noted in 9 patients. In addition, 1 case of needle track implantation was found. Among them, 5 cases without pleural and vessel invasion were diagnosed by needle biopsy, and for all an 18G cutting-type needle was used. These results suggested that PNB using this type of needle can cause a plural recurrence in addition to needle track implantation.

Another possible explanation for this high rate of pleural recurrence among the patients in the needle group is the difference in tumor biology between the two groups. Some investigators may believe that tumors diagnosed by PNB are in a peripheral location, and that this may be related to the high rate of pleural recurrence. From our results, we actually found that a peripheral location was more frequently observed for patients in the needle biopsy group. However, the numbers of tumors touching the pleura seen by chest CT were similar for both groups, and pathologic pleural invasion was less frequently observed for those in the needle group. We thought that the smaller size of the tumors for the needle biopsy group contributed to these results, which suggested that the differences in the tumor characteristics did not influence the results. However, we can not exclude the possibility that other tumor characteristics that we did not investigate in this study may have influenced the differences we observed.

The type of the needle we used could influence our high incidence of pleural recurrence. Large-bore cutting needles were replaced by FNA to reduce complications. During the 1990s, since the emergence of the automated and semiautomated cutting needle with an 18G to 20G bore, the cutting needle was used again because of its easy handling and its greater harvest of tissue [3–8]. Some studies compared the accuracy of cutting needle biopsy with FNA and concluded that cutting needle biopsy greatly increases the diagnostic accuracy for cases of benign pulmonary disease [4–6, 8]. On the other hand, for malignant lesions, FNA has the same high diagnostic accuracy as a cutting needle when on-site cytopathology is available [8, 27–29]. In our institute, the automated cutting type biopsy needle was conducted from 1994, and we reported its usefulness for benign lesions [9]. However, in the results from our current study, we encountered one case of needle track implantation among the 66 needle biopsy cases. Although, the incidence of needle track implantation at 1.5% was within the range of the reported incidence, it was on the high side. That the highest incidence of needle track implantation was reported by Harrison and coworkers [21], who used cutting type biopsy needle, suggested that cutting type needle usage could contribute to the tumor seeding. Conversely, more than 10 cases of needle track implantation after FNA have been reported [19, 20, 24, 30–34] since the first reported case by Sinner and Zajicek [13]. Ayar and colleagues [35] conducted a questionnaire study to elucidate the predictive factor for needle track implantation. They collected data on more than 60,000 needle biopsy cases. Among the 8 needle track implantation cases discovered in this study, 5 needle track implantations occurred after the use of 19G to 22G needles, and they concluded that they could not find any predictive factor including needle bore size. The thoroughness of our follow-up could have been related to our high incidence of tumor seeding. Our early stage of this study population has also affected the results. Needle track implantation in patients with early stage lung cancer may be more noticeable when compared with those in patients with more advanced disease because other recurrences may precede and obscure the implanted lesions. The occurrence of pneumothorax or hemithorax after PNB might be associated with the development of pleural recurrence. However, the incidence of hemothorax and pneumothorax among the pleural recurrence cases was 0% and 33 % (2 of 6 patients), and these incidences were not higher than the incidences that we previously reported (0% and 42%) [9].

Only one similar investigation that dealt with the risk of pleural recurrence was reported by Sawabata and colleagues [36]. This group studied 239 patients with completely resected NSCLC of less than 3 cm in maximum diameter and reported that no pleural carcinomatosis occurred for 45 patients who underwent PNB by FNA and wedge resection of the lung. The difference between their study and ours was that their study population included only 22 cases diagnosed by needle biopsy and 71 (30%) with stage II or more advanced disease for which other forms of recurrence could have obscured pleural recurrence.

To avoid the tumor seeding, some researchers have used a coaxial method for which aspiration or the cutting needle passes through an outer needle that stick into the normal lung [5, 6, 28, 37]. However, the effectiveness of this method has not been demonstrated.

The retrospective approach of this study is a weak point. Therefore, we can not conclude from this study that needle biopsy should be avoided. However, the results call doctor's attention to the potential risks faced by needle biopsy and suggest the need for further investigations focusing on pleural recurrence after needle biopsy. To elucidate the real risk of needle biopsy concerning the tumor seeding according to the type of needle or needle size, pleural recurrence and needle track implantation have to be investigated prospectively for patients with early stage lung cancer in multi-institutional setting. Randomized control trial is an ideal method, if possible. When the real risks of pleural recurrence and needle track implantation are discovered, this information will be indispensable for patients who would undergo this needle biopsy.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
We thank Satoshi Honjo, MD, of the Epidemiology Unit of the Tochigi Cancer Center for his statistical review, and Yukio Tsuura, MD, of the Pathology Unit of the Tochigi Cancer Center for his pathology review.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

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