Thoracic Needle Biopsy

Thoracic Needle Biopsy· Improved Results Utilizing a Team Approach Dewey] Conces.]«, M.D., F:C.C.~;t G. Rudolph Schwenk,]r:, M.D.;+ Philip R. Doering, M.D.;t and Michael D. Glant, M.D.+

Transthoracic needle aspiration biopsy (TNAB) is a useful diagnostic technique in the evaluation of thoracic disease. Previous reports have shown that this technique has a high positive but a low negative predictive value. The latter has limited the clinical usefulness of a negative biopsy. To improve the reliability of a negative TNAB, a series of thoracic needle biopsies was done using a team approach, having a cytopathologist, with the necessary equipment to

Transthoracic needle aspiration biopsy (TNAB) is a reliable diagnostic technique which has been useful in the diagnosis of both benign and malignant lesions of the chest. 1-5 Typically, after the collection of the biopsy, the sample is sent to pathology for interpretation at a later time. H the sample was inadequate, the patient returned for a repeat biopsy. The use of rapid cytologic evaluation has been reported to decrease the number of pleural punctures and consequently the incidence of pneumothorax. 6 This involved immediate transport of the biopsy specimen to pathology, where it was stained and reviewed by the pathologist, who then communicated with the radiologist. We believe that rapid cytologic evaluation of the biopsy material is advantageous in that it determines both the adequacy of the specimen and any need for special processing. To achieve this, we have employed a team approach to TNAB. This involved a cytopathologist being present at the biopsy with the necessary equipment to allow immediate evaluation of the biopsy specimen. We report a series of biopsies performed using this team approach. MATERIALS AND METHODS

From January 1983 to December 1985, a total of222 TNABs were performed, using a team approach, on 204 patients of whom 61 percent were male and 39 percent were female. Their ages ranged from 17 to 94 years, with an average age of 57 years. The indications for TNAB were possible primary neoplasm of lung or mediastinum in 116 patients, possible metastatic lesion in 66 patients, possible infection in 31 patients, possible recurrence of lymphoma in eight patients, and to confirm the presence of a cyst in one patient. Of this group of patients, 16 had more than one biopsy. These included repeat biopsies of the same lesion in six patients and biopsies of additional thoracic lesions in ten patients. Two had three *From Indiana University School of Medicine, Indianapolis. tDepartment of Radiology. +Department of Pathology. Manuscript received August 15; revision accepted October 28.

examine the biopsy specimens, in attendance at the biopsy.

As biopsy specimens were obtained, they were reviewed to

ensure an adequate and representative sampling. The positive predictive value was 98.6 percent and the negative predictive value was 96.7 percent. The high negative predictive value obtained using this approach allows clinical decisions to be based on the results of a negative TNAB.

lesions biopsied. A variety of thoracic lesions were biopsied: parenchymal nodules (148), mediastinal or hilar adenopathy (28), infiltrates (23), pleural masses (13), cavitary lesions (nine), and a cyst (one). The size of the lesions biopsied ranged from 0.7 to 10 em, with an average size of3.6 em. Fluoroscopic guidance was employed in 192 of the biopsies. Computed tomography (CT) was used to guide 30 biopsies of lesions which were not well visualized by 8uoroscopy. The skin over the biopsy site was prepared and draped. Local anesthetic was infiltrated into the chest wall. All biopsies were performed with a coaxial system employing a 19-9auge outer guide needle and either a 22-gauge or 23-gauge inner biopsy needle (DGBS-l or DGBS-2, Cook). The inner biopsy needle was a Greene needle, which has a circumferential cutting edge. The guide needle with stylet was advanced through the pleura during suspended respiration. Using intermittent 8uoroscopy or repeat cr scanning, the guide needle was advanced until it was either in the lesion or immediately adjacent. The stylet was removed from the biopsy needle and the needle was attached to a 100ml syringe. The biopsy needle was then advanced to the end of the guide needle or to the edge of the lesion depending on the location of the guide needle tip. Suction was then applied and the biopsy needle advanced into the lesion with multiple rapid, short reciprocating movements. Suction was then released and the biopsy needle removed. Suction was immediately stopped if blood appeared in the biopsy needles hub to minimize blood dilution. The stylet was placed back into the guide needle which was left in place. The radiologist then expressed the specimen onto a slide, and smears were prepared by the cytology team. The cytology team was composed of a cytopathologist and a cytotechnologist. They employed a mobile cart equipped to permit rapid evaluation of the biopsy specimens. The equipment included: microscope, DifI-Quik stain (Dade Diagnostics), sterile slides, cell culture media for cell suspension, Bollins solution for histologic samples, 3 percent glutaraldehyde for electron microscopy samples and microbiologic culture media. Sterile slides were used so that if the biopsy needle touched the slide, it could be used for subsequent sampling. The number of slides made depended on the size of the sample. lYPically, more than two slides could be made from a given sample. Some slides were airdried for immediate staining in our-Quik stain and for later use with special stains. Other slides were immediately placed in 95 percent ethyl alcohol for later staining with Papanicolaou stain and special stains. Staining with DifI-Quik stain took approximately one minute. The slide was then immediately reviewed by the cytopathologist. An CHEST I 91 I 8 I JUNE, 1987

813

interpretation was rendered as to the presence or absence of malignant cells. If malignant cells were present, the cytopathologist determined how many additional samples were obtained to provide additional material for cytologic evaluation, as well as for special stains, histologic evaluation, or electron microscopy. Additional samples were readily obtained, since the guide needle remained in its original position. If no malignant cells were present, additional samples were obtained with the needle tip being repositioned one or more times to ensure that a representative sample was obtained. In the presence of an inflammatorybackground and no malignant cells, additional samples were obtained for microbiologic culture. When the cytopathologist had determined that he had adequate biopsy material, the guide needle was removed. The patient then had a chest radiograph examined for pneumothorax. If a pneumothorax was present and was large, increasing, or the patient was symptomatic, a chest tube was inserted, usually by the radiologist. Biopsy follow-up employed verification criteria as previously proposed by Caya et al." RESULTS

The results of the 222 TNABs can be divided into four groups: inadequate, definite malignancy, suspicious for malignancy and definite benign (Table 1). A biopsy was deemed inadequate if it was not completed due to the patient's inability to cooperate, if absolute confirmation could not be made of the tip of the biopsy needle being within the lesion, or if the sample contained only blood or normal pulmonary tissue. There were 18 inadequate biopsies (8.1 percent). Since these biopsies were inadequate, they had no impact on clinical decision making. A diagnosis of definite malignancy was made in 139 of the TNABs (62.6 percent). The specific diagnoses are listed in Table 2. Of this group, 104 had clinical follow-up, while 35 had surgical confirmation. In this group there were two false positive diagnoses of definite malignancy. In the first patient, with a wellcircumscribed nodule in the anterior segment of the right upper lobe, a diagnosis of low-grade papillary adenocarcinoma was made by the cytopathologist. At surgery, a pleural based tumor was found, which, on histologic examination, proved to be a benign mixed fibrous and epithelial mesothelioma. The second patient was an elderly woman with a small, ill-defined, somewhat nodular density in the left upper lobe. The TNAB was interpreted as adenocarcinoma. The histology of the resected lesion revealed abundant enlarged Table l-Reaults of!2! TNAB. in 204 Patienta Confirmed Diagnosis

No.

Malignant

143

Benign

61

TNAB Diagnosis

No.

Definite malignancy Suspicious for malignancy Definite benign Definite benign Definite malignancy

137 4 2 59 2

Inadequate sample (no diagnosis made)

814

18

Predictive Value, % 98.6

96.7

Table 2-Diagnoaia ofMalignancy Diagnosis

No.

Adenocarcinoma Squamous cell carcinoma Small cell undifferentiated carcinoma Large cell undifferentiated carcinoma Sarcoma Bronchoalveolar carcinoma Adenosquamous carcinoma Lymphoma-Hodgkin's Non-Hodgkins Germ cell tumors Melanoma Thymoma Carcinoid Mesothelioma Adenoid cystic carcinoma 'lhmsitional cell carcinoma Malignant-type unknown Suspicious for malignancy

49 27 20

6 6 5 5 5 3

4

2 2

1 1 1 1 1 4

reactive pneumocytes consistent with a resolving pneumonitis. The TNAB of four patients was interpreted as suspicious for malignancy. Three patients had surgery performed, with malignancy being confirmed in all cases. The fourth patient refused surgery. Clinical follow-up of the lesion showed progression consistent with malignancy. A diagnosis of definite benign was made in 61 of the TNABs. The specific diagnoses are listed in Table 3. This group is divided into two categories: those with a specific benign diagnosis (65 percent) and those with a nonspecific benign diagnosis (35 percent). The nonspecific benign diagnoses were predominantly nonspecific Table 3-Diagnoaia ofDefinite Benign Diagnosis

No.

Benign, nonspecific Granuloma Infarct Pseudolymphoma Lipoid pneumonia Hamartoma Scar Cyst Infection Aspergillus* Phycomycetes Cryptococcus Nocardia* Blastomycosis Histoplasmosis Candida Ustilago Legionella

20

Mycobacterium kansasii Pseudomonas aeroginosa Serratia marcescens

a-Streptococcus nongroup D

14 3

2

1 1 1 1

4 2 2 2

1 1 1 1 1 1

1 1 1

*One patient had both organisms. Thoracic NeedleBiopsy (ConeN at 81)

inflammation and fibrosis. Follow-up was clinical in 53, surgical in five, and a repeated biopsy was performed in three. In this group there were two false definite benign interpretations. The first patient was an elderly female with a pancreatic mass and basilar interstitial infiltrates. The TNAB of the infiltrate was interpreted as reactive alveolar lining cells. These cells, however, were identical in appearance to those of the pancreatic biopsy specimen subsequently obtained. The pancreatic mass was diagnosed histologically as a well-differentiated clear cell adenocarcinoma. The second patient presented with several parenchymal lung masses. The TNAB of a lung mass was interpreted as reactive lymphoid hyperplasia, either pseudolymphoma or plasma cell granuloma. Open biopsy revealed plasmacytoid lymphocytic lymphoma. Of the 204 patients, 16 (7.8 percent) had at least a second biopsy. Only four (1.9percent) of these patients had the same lesion biopsied because the initial biopsy was inadequate and nondiagnostic. In two patients with renal transplants the same lesion was biopsied to determine the persistence of a fungal infection. The remaining ten patients had different thoracic lesions biopsied. The most commonly occurring complication was pneumothorax, which occurred following 61 of the TNABs (27 percent). The majority of these (19 percent) were observed and resolved. 'Ireatment was required in 8 percent of the patients. This was done either with a standard tube thoracostomy or with a small-caliber tube attached to a Heimlich valve (TPT-l, Cook). Contusion around the biopsied lesion developed in 11 percent of the patients. Hemoptysis occurred in 2 percent of the biopsies and was self-limited. The biopsies in which an adequate sample was obtained resulted in the following therapeutic decisions: observation (69), chemotherapy (54), surgery (43), antibiotics (19), radiation (17), and repeat biopsy (two). Of the 204 biopsies which were thought to be adequate only 43 patients subsequently went to surgery. Of this group, 34 patients had surgery performed as the primary method of therapy or to provide further staging. In only nine patients was surgery performed to confirm the diagnosis made by TNAB. In this series of 222 TNABs, clinically useful diagnostic information was obtained in 204 biopsies. The inadequate biopsies were of no clinical value. Thus, the diagnostic yield was 92 percent. A diagnosis of definite malignancy or suspicious for malignancy was made on 143 of the TNABs, two of these proving to be false positives. Thus, the predictive value of a positive result was 98.6 percent. Sensitivity of a diagnosis of definite malignancy or suspicion of malignancy was 98.6 percent. Specificity was 96.7 percent. The negative predictive value is 96.7 percent.

DISCUSSION

The positive predictive value of TNAB has been shown to be very high for malignant disease." In this series it was 98.6 percent, which is comparable to previous experience. 8 The negative predictive value of TNAB has been much loweI; approximately 71 percent. 8 The low negative predictive value has led to clinical uncertainty as to the reliability of a negative biopsy. As a result, patients have been sent to thoracotomy to confirm the absence of neoplasm. Several different approaches have been recommended to improve the negative predictive value of TNAB. Repeated biopsy of lesions negative for malignancy has been advocated.Y" Another approach has been to obtain supplemental tissue cores which could be evaluated histologically," Both of these approaches resulted in an increase in the reliability of a negative biopsy. This series of TNABs, which employed a team approach, had a negative predictive value of 96.7 percent. In addition, a specific benign diagnosis was made in 65 percent of the biopsies. The high predictive value of a negative biopsy proves the reliability of a negative biopsy by this approach, allowing clinical decisions based on a negative TNAB. This is demonstrated in this group of patients, in that only nine of204 patients who had adequate samples on TNAB were taken to surgery to confirm the diagnosis. Close cooperation between the radiologist and cytopathologist in the performance ofTNAB has been recommended, 6,11.12 The team approach optimizes this by having the cytopathologist in attendance at each biopsy. The team approach has several aspects which account for both the high positive and high negative predictability. When considering the procurement and processing of aspiration biopsies, there are four main goals which should be achieved. First, tissue should be acquired which is representative of the pathologic process. Second, enough tissue should be acquired to allow definition of the cellular process and cell type. These goals are achieved by obtaining multiple samples which are monitored by the cytopathologist. Use of a coaxial needle system allows multiple samples to be obtained with a single placement of the guide needle. The cytologist, by being present at the biopsy, is able to check the samples as they are obtained to ensure that adequate material is obtained from which a diagnosis can be made. The third goal is to process the limited specimen volume obtained by TNAB in a manner most likely to define the cellular process and cell type. Many stains are now available for use in the evaluation of cytologic specimens. These include a variety of histochemical and immunochemical stains which may require immediate special processing. The cytopathologist, by exCHEST I 91 I 6 I JUNE, 1987

815

amining rapid stained specimens at the time of biopsy, is able to determine which, if any, of these stains will be of value and ensure that additional samples are obtained and properly processed for staining by these special stains. If the samples reviewed by the cytopathologist demonstrate an inflammatory process, samples can be obtained for microbiologic staining and culture. The fourth goal is to obtain a diagnostic biopsy without increased overall expense or patient complication. In this series only four patients had rebiopsy because the initial samples were inadequate. By monitoring the biopsy samples, the adequacy of the biopsy can be ensured. Use ofthe coaxialbiopsy system allows multiple samples to be obtained without multiple punctures, saving time and limiting the incidence of pneumothorax. In addition, the reduced resistance of the biopsy needle allows the perception of tissue resistance by the individual performing the biopsy. Multiple sampling is advantageous in that it reduces sampling error. Obtaining multiple samples allows greater flexibility in the types of processing that can be performed. The cytopathologist, by having additional material to examine, is better able to define the nature of both benign and malignant processes. There are three main areas where error can occur during needle biopsies: (1) sampling errors, (2) processing errors, and (3) analyzer errors. The use of the team approach helps to minimize these errors. Sampling errors are reduced by the multiple samples obtained, which are screened by the cytopathologist to ensure adequacy of the sample. Processing errors are reduced because the actual slide preparation is per-

In summary, TNAB is a very useful diagnostic technique which has the advantages of being inexpensive and having high patient acceptance. The use of a team approach in TNABs helps to ensure that the goals of procurement and processing are achieved and that potential sources of error are minimized. This results in both high positive and high negative predictive values for the biopsy results. Clinical decisions can then be reliably based on a TNAB diagnosis of either benign or malignant disease.

of the stains to be performed. Analyzer error is minimized by the fact that the cytopathologist is specially trained in the handling and analysis of minute cytologic specimens. The active participation of the cytopathologist in the biopsy procedure gives him a better understanding of the clinical situation, which is advantageous in the analysis of the specimens.

10 Greene R, Szyfelbein WM, Isler RI, Stark E Jantsch H. Supplementary tissue-core histology from fine-needle transthoracic aspiration biopsy. AJR 1985;144:787-92 11 Sinner WN. Fine-needle biopsy of hamartomas of the lung. AJR 1982; 138:65-69 12 Macintosh PIC, Bonfiglio TA. Technical considerations of interventional radiology: unit design on coordination of diagnostic pathology services. Radiol Coo North Am 1979; 17:623-36

formed by the cytopathologist, as is the determination

816

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Thoracic Needle Biopsy (Conces et til)