Published online before print September 27, 2006, 10.1148/radiol.2412051020
(Radiology 2006;241:589-594.)
© RSNA, 2006
Vascular and Interventional Radiology |
Pleural Mesothelioma: Sensitivity and Incidence of Needle Track Seeding after Image-guided Biopsy versus Surgical Biopsy1
Prachi P. Agarwal, MD2,
Jean M. Seely, MD,
Fred R. Matzinger, MD,
Robert M. MacRae, MD,
Rebecca A. Peterson, MD,
Donna E. Maziak, MD and
Carole J. Dennie, MD
1 From the Departments of Diagnostic Imaging (P.P.A., J.M.S., F.R.M., R.A.P., C.J.D.), Radiation Oncology (R.M.M.), and Thoracic Surgery (D.E.M.), Ottawa Hospital, Civic Campus, 1053 Carling Ave, Ottawa, ON, Canada K1Y 4E9. Received June 17, 2005; revision requested August 18; revision received September 26; accepted October 12; final version accepted January 2, 2006.
Address correspondence to J.M.S. (e-mail: jeseely{at}ottawahospital.on.ca).
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ABSTRACT
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Purpose: To retrospectively compare the sensitivity of image-guided core-needle biopsy, thoracoscopy, and thoracotomy in the diagnosis of malignant pleural mesothelioma and to retrospectively determine the incidence of needle track seeding after these procedures.
Materials and Methods: Institutional review board approval was obtained, and informed consent was not required. The study included 100 consecutive patients (81 men, 19 women; average age, 65.8 years) with pathologically proved malignant pleural mesothelioma who were treated between 1994 and 2002. A total of 23 core-needle biopsies were performed in 22 patients, and 11 of these biopsies were coupled with fine-needle aspiration biopsy. A coaxial technique was used, and biopsy was performed with fluoroscopic (12 biopsies), computed tomographic (10 biopsies), or ultrasonographic (one biopsy) guidance. Sixty-nine patients underwent surgical biopsy in the form of thoracoscopy (n = 51) and/or thoracotomy (n = 21). Patients were followed up clinically for any evidence of needle track seeding after image-guided or surgical procedures. The sensitivity of diagnostic procedures and the incidence of needle track seeding as a result of intervention were calculated.
Results: Sensitivity was 86% for image-guided core-needle biopsy, 94% for thoracoscopy, and 100% for thoracotomy. The incidence of needle track seeding was 4% for image-guided core-needle biopsy and 22% for surgical biopsy.
Conclusion: Image-guided core-needle biopsy in patients with malignant pleural mesothelioma has a lower incidence of needle track seeding than surgical biopsy and has a high sensitivity for diagnosis.
© RSNA, 2006
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INTRODUCTION
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The diagnosis of malignant pleural mesothelioma can be very challenging and difficult to confirm histologically. Pleural fluid cytologic analysis has a low diagnostic yield (1,2). Traditionally, pleural biopsy in the presence of an effusion could be performed without imaging guidance by using a reverse-bevel needle (such as an Abrams or Cope needle), which snags the pleura while gently exerting pressure against the pleura. This technique, however, is associated with the potential for complications, including pneumothorax, hemothorax, and empyema, and can (though rarely) be fatal (3–5). If blind needle biopsy is performed, the diagnostic yield of pleural biopsy over that of pleural fluid cytologic analysis is increased by only 7%–26% (5,6). Thoracoscopy has become the favored diagnostic procedure for patients suspected of having mesothelioma. It has a sensitivity of 91%–98% in the diagnosis of malignant pleural mesothelioma but is both costly and invasive (7,8).
An important aspect of malignant pleural mesothelioma is that it has a propensity to spread along the tracks of chest tubes, thoracoscopy trocars, surgical incisions, and biopsy needles (9). Tumor seeding manifests as subcutaneous nodules that are extremely painful and that markedly diminish the quality of life in patients. Furthermore, these nodules are particularly difficult to treat with surgery or radiation therapy. Therefore, the preferred diagnostic intervention is one that is minimally invasive, has a high sensitivity, and has the least likelihood of producing tumor seeding in the chest wall.
There are some studies in the literature that evaluate the diagnostic accuracy of (10–16) and the incidence of needle track seeding after (11,12) image-guided biopsy in patients with malignant pleural mesothelioma (10–15). On the basis of our experience, we hypothesized that image-guided core-needle biopsy has a high sensitivity for the diagnosis of mesothelioma and a lower incidence of needle track seeding than surgical biopsy. Therefore, the purpose of our study was to retrospectively compare the sensitivity of image-guided core-needle biopsy, thoracoscopy, and thoracotomy in the diagnosis of malignant pleural mesothelioma and to retrospectively determine the incidence of needle track seeding after these procedures.
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MATERIALS AND METHODS
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Patients and Biopsy Procedures
This retrospective study included 100 consecutive patients (81 men, 19 women; age range, 37–88 years; average age, 65.8 years) with pathologically diagnosed pleural mesothelioma who presented to our hospital between 1994 and 2002. The cancer center database at our hospital was reviewed by one author (P.P.A.) who used the key word "mesothelioma" to obtain a list of patients. The patients' charts were then reviewed by the same author. The diagnosis of mesothelioma in these patients was established at surgical biopsy, image-guided biopsy, blind biopsy, and/or fluid cytologic analysis. The research ethics board at our hospital approved this study, and informed consent was not required. Informed consent was, however, obtained from all patients prior to any procedure.
Sixty-nine of 100 patients underwent surgical biopsy in the form of thoracoscopy (51 of 69 patients) and/or thoracotomy (21 of 69 patients). These procedures were performed by three thoracic surgeons from our institution who had experience ranging from 10 to 20 years. Three patients had a nondiagnostic result at thoracoscopy and had to undergo repeat thoracotomy for diagnosis. Thirty-one of 100 patients underwent image-guided biopsy. Of these 31 patients, 22 underwent core-needle biopsy, while nine underwent fine-needle aspiration biopsy only.
We did not classify patients who underwent core-needle biopsy coupled with fine-needle aspiration as having undergone two diagnostic procedures because both procedures were performed with one introducer needle. Of the 22 patients who underwent image-guided core-needle biopsy, 18 underwent only one biopsy procedure, one underwent repeat core-needle biopsy, and three underwent subsequent surgical procedures (thoracoscopy in two patients and thoracotomy in one patient). Thus, a total of 23 core-needle biopsies were performed in 22 patients, and 11 of these biopsies were coupled with fine-needle aspiration biopsy. Biopsy was performed with fluoroscopic guidance (12 biopsies), computed tomographic (CT) guidance (10 biopsies), or ultrasonographic (US) guidance (one biopsy). The choice of imaging guidance was dependent on the extent of pleural thickening and operator preference. CT was preferred for pleural thickening that could not be seen well with other modalities.
A diagnostic unenhanced CT scan of the chest was obtained prior to all biopsy procedures (range, 0–27 days; mean, 9.2 days). For CT-guided biopsies, we determined the approach and biopsy site on the basis of the scan that was obtained at the time of the procedure. For fluoroscopic- and US-guided biopsies, we targeted the site of maximal pleural thickening, as seen on the recent CT scan of the chest. There were no immediate complications in the image-guided biopsy or surgical biopsy groups. In the image-guided biopsy group, no pneumothorax that required pneumocatheter insertion was encountered.
Biopsy Techniques
Image-guided core-needle biopsy of the pleura was performed as an outpatient procedure unless the patient was already admitted for a comorbid condition. Biopsy was performed by one of four thoracic radiologists who had 4–20 years of experience in thoracic biopsy procedures (J.M.S., F.R.M., R.A.P., or C.J.D.). A coaxial technique was used during which a larger (13- or 19-gauge) introducer needle was inserted into the target lesion. A thinner (14–20-gauge) cutting needle was then placed through the introducer needle to obtain the core sample. An automated spring-loaded core biopsy device (Pro-Mag Ultra; Medical Device Technologies, Gainesville, Fla) with a sampling notch of 22 mm was used in all procedures.
We obtained samples from different areas of the tumor by angling and placing torque on the introducer needle during acquisition of each sample. We advanced the introducer needle parallel to the plane of greatest pleural thickening in order to maximize the size of the core sample acquired. The number of core samples obtained was dependent on the macroscopic appearance of the core and ranged from two to 12 (average, 6.6). When core-needle biopsy was preceded by fine-needle aspiration biopsy of the pleura, we inserted a 22-gauge needle through the introducer needle to obtain the sample. For the nine patients in whom only fine-needle aspiration biopsy was performed, a 22-gauge needle was used, and the number of passes was dictated by the adequacy of the sample, as determined by the on-site cytotechnologist. The number of passes performed ranged from two to three, with a mean of 2.4. A cytotechnologist was present at the time of biopsy for all 20 procedures during which fine-needle aspiration biopsy was performed either alone (nine procedures) or in conjunction with core-needle biopsy (11 procedures).
Specimen Preparation and Analysis
Core samples were embedded in formalin and sent to a pathologist. In case of fine-needle aspiration biopsy, the aspirated material was placed on labeled slides, smeared, and stained with phosphate-buffered thiazine and eosin solutions (Hemacolor 2 and 3; EM Science, Gibbstown, NJ). The sample was then immediately examined with a microscope by a cytotechnologist. The needle and syringe were rinsed in normal saline, and the slides and rinsed material were sent to the cytopathology laboratory for analysis. Different pathologists reported fine-needle aspiration biopsy results and core-needle biopsy findings independently. A true-positive result was recorded for only those patients in whom a conclusive diagnosis of mesothelioma could be made. When the diagnosis was consistent with (but not diagnostic of) mesothelioma and when further diagnostic tests were required, this was considered a false-negative result.
Tumor Seeding Determination
Patients were clinically followed up in the oncology clinics for any evidence of seeding that was attributable to the diagnostic procedure (surgical biopsy or image-guided core-needle biopsy). Patients were assessed every 3 months by means of a physical examination and chest radiograph. If there were any new clinical symptoms, the patients were imaged with thoracic CT. One author (P.P.A.) used the clinical notes in the patients' charts to determine the site of tumor seeding. Seeding that occurred in the visible scars from thoracoscopy, thoracotomy, or chest tubes was attributed to that particular procedure. In case of painful subcutaneous nodules that were not associated with a visible scar, correlation with a prior biopsy or thoracocentesis site (determined by the radiologist's and/or clinician's notes) was performed. To ensure adequate follow-up duration, we excluded patients in whom mesothelioma was diagnosed after December 2002. The time interval from the diagnostic procedure to tumor seeding, treatment of seeding, and the patient's response to treatment were determined.
Patient Follow-up
Eighty-nine patients were followed up until death for a mean of 11.97 months (range, 1.5–53 months). Of the 11 living patients, six were followed up for a mean of 64.8 months (range, 16–105 months). Five patients were followed up for a mean of 3.4 months (range, 1–7 months) before being lost to follow-up. Of the five patients who were lost to follow-up, two underwent image-guided biopsy and three underwent surgical biopsy.
Statistical Analysis
Statistical analysis included calculation of the sensitivity of the diagnostic procedure and the incidence of needle track seeding. The 95% confidence intervals for these sensitivities were calculated for a proportion based on the efficient score method (17). Sensitivities were compared with the results of the 
2 test. Overall survival was compared by using the Kaplan-Meier method along with the log-rank test (Statistica, version 6.1; StatSoft, Tulsa, Okla). P values less than .05 were considered to indicate a statistically significant difference.
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RESULTS
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Patients and Biopsy Procedures
A total of 106 image-guided biopsies (core-needle biopsy with or without fine-needle aspiration biopsy and fine-needle aspiration biopsy alone) and surgical diagnostic procedures (thoracoscopy or thoracotomy) were performed. These procedures consisted of 23 core-needle biopsies (11 of which were coupled with fine-needle aspiration biopsy), nine fine-needle aspiration biopsies, 53 thoracoscopies, and 21 thoracotomies. Eighty patients underwent one diagnostic procedure, while 13 patients underwent two diagnostic procedures (median, one procedure; range, one to two procedures). Malignant pleural mesothelioma was diagnosed definitively in 88 of 100 patients by using image-guided core-needle biopsy, thoracoscopy, or thoracotomy. In the remaining 12 patients, diagnosis was achieved by means of fine-needle aspiration biopsy alone (five of 12 patients), fluid cytologic evaluation (six of 12 patients), or blind biopsy (one of 12 patients) (Table 1).
In the 22 patients who underwent image-guided core-needle biopsy (Table 2), diagnosis was achieved during the first attempt in 18 patients (82%). Of the four patients who had a nondiagnostic result at core-needle biopsy, one underwent repeat image-guided core-needle biopsy, two underwent thoracoscopy, and one underwent thoracotomy for definitive diagnosis. All four nondiagnostic biopsies were performed with fluoroscopic guidance.
Thoracoscopy was performed in 51 patients, was diagnostic during the first attempt in 46 patients (90%), and was diagnostic during the second attempt in two patients. The three patients with false-negative results at thoracoscopy underwent thoracotomy for definitive diagnosis, which required another hospital admission. Thoracotomy was diagnostic in all 21 patients (100%).
Tumor Seeding
Of the 21 patients who underwent diagnostic thoracotomy, five (24%) developed tumor seeding in the scar. The rate of tumor seeding at the site of the thoracoscopic scar was 16% (eight of 51 patients). All patients in the surgical group had chest tubes placed after the surgical procedure.
Tumor seeding at the chest tube site as a result of thoracoscopy or thoracotomy was seen in five (7%) of 69 patients. Of the 55 patients who had thoracentesis documented in their clinical charts, two (4%) developed needle track seeding. Both patients underwent surgical biopsy and experienced seeding at the site of the surgical scars. In the image-guided biopsy group, only one (5%) of 22 patients had seeding secondary to core-needle biopsy. This patient underwent core-needle biopsy performed by using a 17-gauge introducer needle with a coaxial technique, and six core samples were obtained. Of the patients with tumor seeding, five had seeding at more than one site. Thus, a total of 16 patients had malignant seeding secondary to various diagnostic procedures (Table 3). One of these 16 patients underwent two procedures (nondiagnostic thoracoscopy followed by thoracotomy), with seeding at the site of the thoraoscopic scar.
Patient Follow-up
The time interval between the diagnostic procedure and tumor seeding varied from 2 to 16 months, with a mean of 7.3 months. The interval for seeding in scars was approximately 8.1 months for pleuroscopy, 5.5 months for thoracotomy, 8.4 months for chest tube placement, 7.0 months for needle biopsy, and 6.0 months for thoracocentesis. There was no major difference in the postprocedural survival time until last follow-up. In the image-guided biopsy group, this period was approximately 14.7 months; in the surgical biopsy group, this period was 15.3 months (P = .98) (Figure).
All 16 patients with tumor seeding presented with subcutaneous nodules and varying degrees of pain. Surgical resection was not feasible in any of these patients, and all patients underwent palliative radiation therapy. A total of 2000–4000 cGy was given in 10–15 fractions. Fourteen of the 16 patients experienced pain relief after radiation therapy. Two of the 16 patients died soon after the initiation of palliative treatment. An actual decrease in the size of the nodules was seen in three patients, two of whom showed partial response and one of whom showed complete disappearance of the tumor implant.
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DISCUSSION
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In different parts of the world, the incidence of mesothelioma has either reached a peak or continues to increase, depending on the history of asbestos use (14). In the United States, it is thought that the peak of malignant pleural mesothelioma was reached in the year 2000, and the most severely affected cohort, which was born in 1925–1929, is estimated to have a lifetime risk of one in 500 (13). An early and accurate diagnosis for prognostic purposes and symptom control is therefore desirable, with a minimum of invasive procedures. The results of selected case series have demonstrated long-term survival in patients with mesothelioma that is treated aggressively by means of extrapleural pneumonectomy, chemotherapy, and hemithoracic radiation therapy (18,19).
The use of immunostaining allows for pathologic diagnosis of malignant pleural mesothelioma by using a relatively small tissue sample, which can be provided by means of image-guided core-needle biopsy (14). In contrast to thoracoscopy, core-needle biopsy is a less expensive and minimally invasive procedure that can be performed on an outpatient basis with a local anesthetic. Although fine-needle aspiration biopsy may yield a diagnosis of malignant pleural mesothelioma, it is not advocated that this technique be used alone because of the marked difficulty in differentiating malignant pleural mesothelioma from metastatic pleural disease, the dependence of fine-needle aspiration biopsy on an experienced cytologist, and the low sensitivity of the technique. In our study, the sensitivity of fine-needle aspiration biopsy was only 56% (five of nine), whereas the sensitivity of core-needle biopsy was 86% (19 of 22).
Malignant tumor seeding is a common complication of various diagnostic and therapeutic procedures for malignant pleural mesothelioma. These subcutaneous nodules are exceedingly painful and often impair the patient's capacity to sleep and enjoy a reasonable quality of life (9). In the literature, there is marked variation (ranging from 2% to 51%) in the incidence of tumor seeding in patients with mesothelioma (9). Seeding along the track after video-assisted thoracoscopic surgery may occur in up to half of patients (20), whereas the highest reported incidence of seeding after image-guided biopsy is only 22% (11). In our study, one (5%) of 22 patients had needle track seeding after core-needle biopsy, in contrast to 15 (22%) of 69 patients who had needle track seeding after surgical biopsy. Further research at multiple centers with larger numbers of patients is warranted to confirm this finding as being statistically significant. We believe that the use of a coaxial technique may further reduce the incidence of needle track metastases by restricting the number of skin and chest wall puncture sites to one. This is a hypothesis that needs further investigation to be proved.
Few researchers have examined the incidence of needle track seeding after image-guided pleural biopsy (11,12). Metintas et al (11) reported a rate of 22% and performed CT-guided biopsy by using 11-gauge Ramel or 8-gauge Abrams needles. Patients were observed for at least 6 months after core-needle biopsy, and the maximum time interval between core-needle biopsy and tumor seeding was determined to be 7 months. Heilo et al (12), on the other hand, did not encounter any tumor seeding after biopsy (apart from two patients who experienced seeding after pleural fluid drainage). The mean patient observation time in their study varied from 1 month to 10 years.
In theory, a potential discrepancy in the rate of tumor seeding between the two groups (image-guided biopsy and surgical biopsy groups) could have occurred if survival after surgical biopsy was considerably longer, thereby allowing more time for seeding to become clinically apparent in the surgical group. This situation might have occurred if the surgical group had a higher proportion of early-stage disease, with smaller tumor bulk that was potentially unsuitable for image-guided core-needle biopsy. In our study, however, there was no major difference in the postprocedural survival time until last follow-up (image-guided biopsy group, 14.66 months; surgical biopsy group, 15.33 months; P = .98).
Our study had some limitations. We do not know whether other factors, such as tumor subtype, tumor stage, variations in treatment type, or variations in diagnostic procedures, may have affected the development of tumor seeding. Histologic subtyping and staging of mesothelioma was available in only a small number of patients in our study and was therefore not used for analysis. Furthermore, because patients were not randomly assigned to the surgical or imaging-guided biopsy group, selection bias may have resulted. Another limitation of our study was the possibility of underreporting tumor seeding. These lesions, however, manifest as exceedingly painful nodules and are almost always symptomatic. There was a theoretic possibility of missing small asymptomatic nodules at clinical examination, but the clinical significance of such lesions, which do not compromise the quality of life, is questionable.
Although our study included a sizeable number of patients with mesothelioma (n = 100), we were unable to demonstrate a statistically significant difference between the sensitivities of different diagnostic methods (core-needle biopsy vs surgical biopsy) or of needle track seeding. This suggests that larger numbers of patients should be studied and multiple centers should be included. We clearly observed comparable sensitivities between diagnostic methods and nominally lower needle track seeding in the core-needle biopsy group, but this deserves confirmation with further research.
In summary, image-guided core-needle biopsy, thoracoscopy, and thoracotomy have sensitivities of 86%, 94%, and 100%, respectively, in the detection of malignant pleural mesothelioma, and image-guided core-needle biopsy has a much lower propensity to cause needle track seeding (4%) compared with surgical biopsy (22%).
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ADVANCES IN KNOWLEDGE
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- Image-guided core-needle biopsy has a lower incidence of needle track seeding (4%) compared with surgical biopsy (22%) in patients with malignant pleural mesothelioma.
- Although not significantly different (P = .18), the sensitivity of image-guided core-needle biopsy is 86%, while the sensitivities of thoracoscopy and thoracotomy are 94% and 100%, respectively.
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ACKNOWLEDGMENTS
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We acknowledge Wayne Kendal, MD, PhD, for his help with statistical analysis.
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FOOTNOTES
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2 Current address: Department of Thoracic Radiology, University of Michigan Health System, Ann Arbor 
Authors stated no financial relationship to disclose.
Author contributions: Guarantor of integrity of entire study, P.P.A.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, P.P.A., J.M.S., R.M.M.; clinical studies, R.M.M., R.A.P.; statistical analysis, P.P.A.; and manuscript editing, J.M.S., F.R.M., R.M.M., R.A.P.
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ABSTRACT
INTRODUCTION
