Fine needle aspiration biopsy: Has its time come?

Fine Needle Aspiration Biopsy

Has Its Time Come?

KENT BOTTLES, M.D. THEODORE R. MILLER, M.D. MICHAEL 6. COHEN, M.D. BRITT-MARIE LJUNG, M.D. San Francisco, California

From the Departments of Pathology, San Fran- cisco General Hospital and the University of Cali- fornia, San Francisco, School of Medicine, San Francisco, California. Requests for reprints should be addressed to Dr. Kent Bottles, Depart- ment of Anatomic Pathology, HSW 501, Univer- sity of California, School of Medicine, San Fran- cisco, California 94143. Manuscript submitted April 30, 1985, and accepted May 2, 1985.

Fine needle aspiration biopsy has been undergoing a revival in the United States, but a recent survey showed that many clinicians were uncertain how to utilize this test. The scope of fine needle aspiration biopsy as practiced at the University of California, San Francisco, and the San Francisco General Hospital is described. The relevant accuracy data available in the world literature on this procedure are also reviewed.

Although fine needle aspiration biopsy has been successfully used for 35 years in Europe, it is only in the last IO years that renewed interest has been expressed in the procedure by American physicians.

A recent survey of 369 private practice clinicians in San Francisco revealed that most physicians are unsure of the utility of fine needle aspiration biopsy in a variety of clinical settings. Even though these physicians were unsure how to utilize the procedure, 83 percent antici- pated that the method would be used more extensively in the future [I].

The purpose of this report is to describe how fine needle aspiration biopsy is used at the University of California, San Francisco, and San Francisco General Hospital and to review the world literature on the clinical applications and accuracy of this method. The best available criteria to evaluate the procedure are those described by Galen and Gambino [2]. The University of California, San Francisco, and San Francisco General Hospital fine needle aspiration biopsy services have a combined experience of 8,000 aspirations; we have a combined person- al experience of over 15,000 of these procedures.

THE PROCEDURE

Fine needle aspiration biopsy utilizes 22- to 25gauge needles for biopsy of masses without anesthesia. For palpable masses, the needle (attached to a syringe mounted onto a syringe holder) is introduced through alcohol- wiped skin into the mass. One hand manipulates the syringe holder, and the other hand fixes the mass between two fingers. The lesion is sampled by moving the needle back and forth within the mass while exerting full suction on the syringe. The negative pressure is released by letting the plunger of the syringe return to the resting position before removing the needle. While an assistant applies pressure to the puncture site to avoid bruising or hematoma formation, the aspirator prepares air-dried slides for May Grunwald Giemsa staining and alcohol-fixed slides for Papanico- laou staining [3-51. For abdominal and chest masses, computed tomo- graphic scanning, ultrasound, and fluoroscopy are utilized to precisely localize the biopsy site.

Although simple to describe, the procedure is actually difficult to

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FINE NEEDLE ASPIRATION BIOPSY-BOTTLES ET AL

master. It has been estimated that 200 aspirations should be performed in a short period of time under expert guidance before attempting to independently utilize the technique for patient care; the same authors also recom- mend that the aspirator perform at least 10 procedures a week [6]. Smearing the aspirate onto the glass slides, a task casually performed by many, has been described as perhaps “the most important manuever in the whole range of steps in the aspiration [5].” Anyone utilizing this technique must be adept at the four basic smearing methods that have been developed to handle the different consistencies of aspirate fluid [7]. A properly smeared aspirate usually contains thousands of cells, including numerous cohesive clusters; improperly smeared aspirates yield scant or distorted specimens that preclude accurate diagnoses.

At the University of California, San Francisco, and San Francisco General Hospital, the majority of aspirations are performed, smeared, and interpreted by experienced attending cytopathologists; the radiologically guided fine needle aspiration procedures are usually performed by the radiologists, and the cytopathologist smears and ex- amines a fast stain of the specimen to ensure the adequa- cy of the biopsy. Although any physician can learn to properly aspirate and smear specimens, the attending cytopathologist is in the unique position of constantly adjusting biopsy and smear techniques based on what he or she sees microscopically. Many medical centers have reported greater accuracy in diagnoses when the same person performs, smears, and interprets the fine needle aspiration biopsy [8- 1 I].

HISTORY OF FINE NEEDLE ASPIRATION BIOPSY

The roots,of fine needle aspiration biopsy, as practiced today, extend back to the last half of the 19th century when scattered case reports were published [12]. The first significant study usually cited is that of Greig and Gray [ 131 who, in 1904, demonstrated trypanosomal organ- isms in lymph nodes. Hirschfeld [ 141 published results of aspiration smears of various tumors in 19 19, and Guthrie [15] published results of a series of lymph node aspirations in 192 1.

In 1925, several physicians at Memorial Hospital in New York investigated the use of aspiration smears on a large scale. This experience culminated in the landmark publications of Martin and Ellis [16] who reported 65 cases in 1930 and 1,400 cases in 1934 [ 171, and Stew- art [18] who reported 2,500 cases in 1933. The procedure described in these reports utilized skin incisions, anesthesia, 18-gauge needles, air-dried thick smears, and staining with hematoxylin and eosin.

In Europe in the 1940s a new branch of aspiration biopsy developed that emphasized thin needles and care- fully prepared, thin, air-dried smears stained with May Grunwald Giemsa stain. The pioneers of this branch were

clinicians such as Paul Lopes-Cardozo, Nils Soderstrom, and Sixten Franzen [ 191. Franzen and his associates (Josef Zajicek and Torsten Lowhagen) at the Karolinska Hospital in Stockholm have been especially instrumental in improving the technique by reporting large series of various tumors, conducting workshops, and developing specialized instruments. The University of California, San Francisco, and San Francisco General Hospital fine needle aspiration biopsy services are modeled after the Karo- linska Service; several of the San Francisco cytopathologists have trained with Franzen and Lowhagen.

Fine needle aspiration biopsy in the United States has undergone a revival in the last 10 years. One gauge of the increased popularity of the procedure is the increase in the number of articles on fine needle aspiration biopsy published in Acta Cytolosica (from seven in 1972 to 49 in 1984).

ADVANTAGES OF FINE NEEDLE ASPIRATION BIOPSY

Fine needle aspiration biopsy enjoys several advantages when compared with more conventional methods of performing biopsy of masses. Several studies have documented that this procedure is less expensive than surgical biopsy [20-231, and fine needle aspiration biopsy is especially attractive in view of diagnostic-related groups reim- bursement programs [22]. Kaminsky [20] estimated that fine needle aspiration biopsy can provide a diagnosis for 10 to 30 percent of the cost of surgical biopsy. In some situations, diagnosis of unresectable disease by fine needle aspiration biopsy can prevent unnecessary laparotomy or thoracotomy [ 191.

Fine needle aspiration biopsy can also be performed as an outpatient procedure and yields results more quickly than surgical biopsy. The actual procedure takes only a few minutes, and immediate results can be obtained within 20 minutes. This speed of diagnosis can relieve patient anxiety, aid the clinician in convincing the patient of the necessity of immediate treatment or hospitalization, and streamline the patient’s initial work-up [5]. In a county hospital setting like San Francisco General Hospital in which patients frequently miss follow-up appointments, the advantages of performing biopsy of a mass on the initial visit are obvious. Clinicians have also reported that fine needle aspiration biopsy has increased their skill in examining patients by providing immediate feedback on the cause of the masses they palpate [5].

Fine needle aspiration biopsy is also a safe procedure with low complication rates, Livraghi et al’s [24] literature review of 11,700 abdominal fine needle aspiration biopsies revealed one death due to pancreatitis (0.008 percent) and six patients with major complications (0.05 percent). Laparotomies in dogs subjected to abdominal fine needle aspiration biopsies revealed no significant complications [25]. A series of 17,000 transrectal pros-

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tate fine needle aspiration biopsies demonstrated one death and three major complications [3]. The incidence of pneumothorax following pulmonary fine needle aspiration biopsy ranges from 6 to 57 percent, but the majority of these complications resolve without treatment. When the procedure is performed in elderly and inoperable patients such as in the series of Berquist et al [26], the incidence of complications following pulmonary fine needle aspiration biopsy is quite high (49 percent). Although most of the 27 reported deaths after transthoracic needle biopsies of the lung have been due to large bore needles, there is one reported case in which fine needle aspiration biopsy did result in a death [27]. Complication rates for superfi- cial organs such as thyroid, lymph nodes, and breast are even lower.

Fears of implanting tumor cells along the needle tract and of decreasing survival rates by hematogenous spread of tumor cells are not valid based on the results of hundreds of thousands of procedures performed world- wide. There have been only three cases of documented needle tract implants due to fine needle aspiration biopsy [28-301, and survival rates for patients with breast [9,31,32], lung [33-351, and kidney malignancies [36] diagnosed by this procedure have been similar to those in control groups in whom diagnosis was made by open surgical biopsy. Evaluation of complication rates must take into account the size of the needle used; when needles larger than the 22- or 23-gauge needle used in fine needle aspiration biopsy are utilized, complication rates for every organ are higher [8].

TARGET SITES

Thyroid. At the University of California, San Francisco, and the San Francisco General Hospital, fine needle aspiration biopsy is used to evaluate palpable thyroid nodules. Crile et al [37] have estimated that 82 percent of all thyroid surgery can be avoided by the preoperative use of this aspiration method. The major goal of the procedure is to separate those patients who require surgical explora- tion from those who do not, but specific diagnoses can often be rendered. We have made the following specific diagnoses on fine needle aspiration biopsy: benign thyroid nodule, hyperthyroidism, subacute thyroiditis, Hashimo- to’s disease, follicular neoplasm, Hut-thle cell tumor, papillary carcinoma, medullary carcinoma, undifferentiated carcinoma, and lymphoma.

The largest series of evaluation of thyroid nodules by fine needle aspiration biopsy was a European cooperative study with 522 cancers, 75 false-negative reports (14 percent), and five false-positive reports (1 percent) [ 191. Another series [ 191 of 641 consecutive thyroid fine needle aspiration biopsies contained 103 malignant tumors, 18 false-negative results (17.5 percent), and four false- positive results (0.7 percent). The false-negative rates were higher in these European series than in the Ameri-


can series because of differences in definitions of benign thyroid nodule, follicular adenoma, and carcinoma. Frable [33] has reported four false-positive and six false-negative results in a series of 260 satisfactory aspirates, and Koss et al [ 191 reported one false-positive and two false- negative results in 134 consecutive thyroid fine needle aspiration biopsies. Some have emphasized the difficulty of interpreting results of thyroid fine needle aspiration biopsy and have urged limiting its use to confirming obvi- aus cases of carcinoma and to confirming suspected medullary carcinoma [38], but many cytopathologists and endocrinologists believe it is a useful test [ 1,3-6,191. Salivary Glands. At the University of California, San Francisco, and San Francisco General Hospital, salivary gland masses routinely undergo fine needle aspiration biopsy. We have rendered the following specific diagnoses: benign salivary gland tissue, lipoma, sialosis, sia- locoele, paraganglioma, acute and chronic sialadenitis, pleomorphic adenoma, mucoepidermoid carcinoma, monomorphic adenoma, Warthin’s tumor, adenoid cystic carcinoma, and acinic cell carcinoma.

Interpretation of results of fine needle aspiration biopsy of salivary glands is one of the most difficult tasks a cytopathologist faces, and the accuracy rates reflect the difficulty of this endeavor. Cystic lesions pose the greatest difficulties and some authors who emphasize the numerous types of salivary gland tumors do not advocate this procedure for preoperative diagnosis of salivary gland neoplasms [38].

Others have been impressed by the statistics reported by Kline et al [39] and Frable [40]. Kline et al’s series of 47 salivary gland masses studied by both fine needle aspiration biopsy and histologic examination properly cat- egorized 79 percent of the cases into benign non-neoplastic, benign neoplastic, and malignant groups; diagnosed 15 percent of the cases as suggestive of malignan- cy; and misdiagnosed 6 percent of the cases as benign non-neoplastic disease when, in fact, they were Warthin’s tumor. In this series, substantially correct preoperative diagnoses were made by fine needle aspiration biopsy in 42 of 47 patients (92 percent). Frable [40] reported a sensitivity of 93 percent for salivary gland tumor and a specificity of 99 percent for absence of tumor. Lymph Nodes. Fine needle aspiration biopsy is often the first step in the evaluation of lymphadenopathy at the University of California, San Francisco, and San Francis- co General Hospital. We have made the following specific diagnoses on the basis of this procedure: benign hyperplasia, sarcoid, metastatic adenocarcinoma, metastatic squamous cell carcinoma, metastatic small cell carcinoma, Kaposi’s sarcoma, mycobacterial and bacterial infec- tion, Hodgkin’s disease, and non-Hodgkin’s lymphoma.

Fine needle aspiration biopsy of lymph nodes has yielded impressive statistical results in detecting metastatic disease. Several series [3,21,41,42] have estab-


FINE NEEDLE ASPIRATION BIOSPY-BOTTLES ET AL

lished an accuracy rate of 76 to 90 percent for detecting metastatic disease in lymph nodes; these series have also often been able to identify the specific type of metastatic tumor.

The results of using fine needle aspiration biopsy to make a primary diagnosis of lymphoma are mixed. One viewpoint is summarized by Deeley [43] who wrote, “If lymphoma is diagnosed clinically, it is preferable to remove a lymph node rather than to attempt to make a diagnosis on the specimen obtained by needle biopsy.” Others point out that fine needle aspiration biopsy in patients with suspected lymphoma has revealed diagnos- able infectious and metastatic causes of lymphadenopathy, and a study has shown that previous -fine needle aspiration biopsy of lymph nodes does not appear to hamper the histologic interpretation of subsequent surgical biopsy material [44].

Orell and Skinner [45] reported full agreement between cytologic and histologic classification of 44 of 53 non-Hodgkin’s lymphomas, and they correctly assigned 48 of 49 cases of lymphoma diagnosed by fine needle aspiration biopsy to good or bad prognostic groups. They concluded that this procedure is valuable in four clinical settings: (1) to establish a definitive diagnosis in patients with advanced disease who would require major surgery to obtain a histologic diagnosis, (2) to assess the extent of lymph npde involvement following histologic diagnosis, (3) to select a representative node for surgical biopsy, and (4) to detect recurrent disease in patients whose initial diagnosis was established by histologic examination. Those who advocate the use of fine needle aspiration biopsy point out that the material aspirated can be used for enzyme histochemical study, immunoperoxidase stains, culture, and antigen stimulation. Friedman et al [46] and Desmet et al [47] have reported good results in using fine needle aspiration biopsy to manage patients with Hodgkin’s disease. Breast. Fine needle aspiration biopsy is extensively used at the University of California, San Francisco, and San Francisco General Hospital to sample breast masses. Smears obtained by this procedure are interpreted as benign, malignant, suspicious, or insufficient for diagnosis. Specific diagnoses have included fat necrosis, gyne- comastia, fibrocystic disease, lactating adenoma, tubular adenoma, fibroadenoma, papillary lesion, ductal carcinoma, lobular carcinoma, apocrine carcinoma, mutinous carcinoma, medullary carcinoma, metaplastic carcinoma, malignant fibrous histiocytoma, and radiation-induced changes.

In expert hands, fine needle aspiration biopsy is an accurate method for evaluating breast masses. In several centers, the diagnostic accuracy is such that mastecto- mies are performed without histologic confirmation of positive findings of fine needle aspiration biopsy of the

breast [8,10,20,48,49]. In aseries of 205 cases of breast aspiration at the University of California, San Francisco, there were 58 malignancies with a complete sensitivity rate of 94.5 percent, a specificity rate of 96.6 percent, a false-positive rate of zero, and a false-negative rate of 5.5 percent [23]. False-negative rates in the literature range from 1.8 percent to 26.3 percent [19]. Factorsthat affect the false-negative rate include experience of those performing fine needle aspiration biopsy and interpreting its results, and the size and nature of the tumor. Zajicek [3] demonstrated that experience decreased the Karolinska’s false-negative rate from 9.9 percent to 1.8 percent. In patients who undergo a coordinated program of clinical examination, mammography, and fine needle aspiration biopsy, 99 percent of those with breast cancer will be detected, but a few patients with cancer will still be missed [50,51]. Clinicians must realize that a negative result of fine needle aspiration biopsy or surgical biopsy does not necessarily rule out the presence of cancer. Prostate. Transrectal fine needle aspiration biopsy can be successfully used to evaluate palpable abnormalities of the prostate gland. With the patient in the dorsal lithoto- my position, the mass is palpated by the tip of the index finger during rectal examination. The mass is aspirated with the aid of a needle guide placed on the index finger, and long 23-gauge needles. Patients with known prostatitis, rheumatoid arthritis, and diabetes mellitus appear to be at a high risk for septicemia [3]. Using this technique, we have made the following specific diagnoses: prostatitis, granulomatous prostatitis, hyperplasia, and adenocar- cinema. The cancer cases can be graded into well, mod- erately, and poorly differentiated tumors.

In expert hands, transrectal fine needle aspiration biopsy is safer and more accurate than large-core transperineal needle biopsy. In Esposti’s [52] series of 350 consecutive patients who underwent both fine needle aspiration biopsy and large-core biopsy, the specificity for benign disease was 93 percent by the former procedure, and the overall accuracy was 96 percent. The false- positive and false-negative rates for the fine needle aspiration biopsy portion of this study were 2 percent and 5 percent, respectively. In Ljung et al’s [53] prostate series of 103 aspirates, fine needle aspiration biopsy had a sensitivity rate of 95 percent and a specificity rate of 97 percent; one case of well-differentiated cancer diagnosed by fine needle aspiration biopsy was not confirmed by histologic examination, and the false-negative rate for this method was 5 percent. In this study, simultaneous large core biopsy evaluation revealed a sensitivity rate of 76 percent and a false-negative rate of 24 percent. These fine needle aspiration biopsy statistics compare favorably with the overall accuracy of transperineal large-core needle biopsy, which has been reported as 60 percent [54]. It must be emphasized that fine needle aspiration biopsy of



the prostate requires considerable skill and experience in performing and interpreting the smears. Lung. At the University of California, San Francisco, and San Francisco General Hospital, fine needle aspiration biopsy is used to evaluate lung masses that cannot be diagnosed by sputum cytologic testing and bronchoscopy. The biopsy is usually performed in the fluoroscopy suite by the radiologist; the cytopathologist attends the procedure to examine a fast stain of the specimen. We have made the following diagnoses on the basis of fine needle aspiration biopsy: squamous cell carcinoma, small cell carcinoma, adenocarcinoma, carcinoid, giant cell carcinoma, abscess, metastatic adenocarcinoma, metastatic mesenchymal tumors, and metastatic malignant melano- ma. It is almost always possible to differentiate small cell carcinoma from non-small cell carcinomas; it is not always possible to separate poorly differentiated squamous cell carcinomas from poorly differentiated adenocarcinomas. These latter tumors are reported as non-small cell carcinomas.

The accuracy rate in the literature for fine needle aspiration biopsy of pulmonary lesions ranges from 72 percent [55] to 97 percent [56]. In a series of 1,100 consecutive cases of fine needle aspiration biopsy of the lung at the Szczecin Medical Academy in Poland, cancer was accurately diagnosed in 89.9 percent of the cases with two false-negative and two false-positive cases [ 191. Lalli et al [57] repot-ted a series of 1,296 lung fine needle aspiration biopsies with an 85 percent accuracy rate, and Sinner [58] described 2,726 patients with a 91 percent accuracy rate. Several studies comparing the accuracy of this type of biopsy with sputum cytologic testing and bronchoscopy also concluded that fine needle aspiration biopsy was a valuable method of diagnosing pulmonary malignancies [59-621. Some of these studies concluded that fine needle aspiration biopsy is especially effective in diagnosing small (less than 2 cm) lesions, peripheral lesions, and lesions not originating in the airways. Intra-Abdominal Masses. Radiologically guided fine needle aspiration biopsy can sample intra-abdominal masses. At the University of California, San Francisco, and San Francisco General Hospital, the majority of such cases have been aspiration biopsies of the liver and pancreas. Specific diagnoses of liver masses have included hepatocellular carcinoma, metastatic adenocarcinoma, metastatic squamous cell carcinoma, metastatic small cell carcinoma, metastatic leiomyosarcoma, and metastatic carcinoid. Pancreatic masses have been mostly adenocarcinomas. Other intra-abdominal targets have included adrenal, renal, and retroperitoneal masses.

Statistical evaluation of the accuracy of fine needle aspiration biopsy of abdominal masses is hampered by the dearth of large series with histologic confirmation, Lundquist’s [63] series of 74 patients with histologically

proved primary or metastatic tumors of the liver documented a 77 percent accuracy rate on fine needle aspiration biopsy. A similar series of 83 patients reported an accuracy rate of 92 percent on fine needle aspiration biopsy of the liver [64]. There are series in which five of six, 17 of 21, 22 of 29, 16 of 18, 24 of 26, and 29 of 33 patients with documented adenocarcinoma of the pancreas had correct diagnoses by radiologically guided fine needle aspiration biopsy [19,65]. Such a diagnosis in a patient with widespread disease in whom surgety is not curative can prevent laparotomy merely to establish the diagnosis. A series of 22 patients with adrenal masses sampled by fine needle aspiration biopsy correctly classi- fied the adrenal tumors by this form ‘of biopsy in 90 percent of all the cases [66]. Miscellaneous Sites. Fine needle aspiration biopsy can also be used to sample masses of the skin, the bone, the eye globe, the orbit, and the central nervous system [3,5,19,33].

RESEARCH ON AND FUTURE APPLICATIONS OF FINE NEEDLE ASPIRATION BIOPSY

Fine needle aspiration biopsy can remove a sample of cells (viable and nonviable) from diseased and normal living tissue. A number of sophisticated ways to analyze these cells are being developed. These specialized techniques include transmission electron microscopy [67,68], scanning electron microscopy [69], microspectrophoto- metric and flow cytometric quantitation of DNA [70-741, computer-based image analysis of cells [ 191, measure- ments of DNA synthesis [ 191, enzyme histochemical stains [75], peroxidase-antiperoxidase sandwich techniques for tumor markers [76,77], and monoclonal antibodies to lymphoid [78,79] and other human tumors [80-821. In Sweden, stereotactic fine needle aspiration biopsy of nonpalpable breast masses discovered by mammography has diagnosed carcinoma in 13 percent of the patients examined [ 191. When fully developed, these techniques may allow us to more precisely identify tumors by fine needle aspiration biopsy and to more precisely predict tumor biologic behavior on the basis of these sophisticated biopsy characteristics.

CONCLUSION

This review has described the scope of pathology-based fine needle aspiration biopsy services at the University of California, San Francisco, and San Francisco General Hospital and summarized accuracy data available in the world literature. Fine needle aspiration biopsy is a cost- effective, accurate, and safe procedure whose time has come [83]. For it to be fully and accurately utilized, clinicians must understand not only the strengths and weaknesses of the procedure, but also the technical difficulties involved in obtaining diagnostic material.



REFERENCES

1.

2.

3.

8.

9.

10.

11.

12.

13.

14.

15.

16.

17.

18.

19.

20.

21.

22.

23.

24.

25.

26.

Bottles K, Cohen MB, Sacks ST: Clinician perceptions of fine needle aspiration cytology. Diagn Cytopathol 1986; 1: 249-254.

Galen R, Gambino SR: Beyond normality: the predictive value and efficiency of medical diagnosis. New York: John Wiley and Sons, 1975.

Zajicek J: Aspiration biopsy cytology, part I. Cytology of supradiaphragmatic organs. Monogr Clin Cytol 1974; 4: l-150.

Frable WJ: Thin-needle aspiration biopsy. Am J Clin Pathol 1976; 65: 168-182.

Linsk JA, Franzen S: Clinical aspiration cytology. Philadel- phia: JB Lippincott, 1983.

Van Herle AJ, Rich P, Ljung BM, et al: The thyroid nodule. Ann Intern Med 1982; 96: 222-232.

Abele JS, Miller TR, King EB, et al: Smearing techniques for the concentration of particles from fine needle aspiration biopsies. Diagn Cytopathol 1985; 1: 59-65.

Feldman PS, Covell JL: Fine needle aspiration cytology and its clinical applications: breast and lung. Chicago: Ameri- can Society of Clinical Pathologists Press, 1985.

Franzen S, Zajicek J: Aspiration biopsy in diagnosis of palpable lesions of breast. Acta Radio1 Ther Phys Biol 1968; 7: 241-262.

Zajdela A, Ghossein NA, Pilleron JP, et al: The value of aspiration cytology in the diagnosis of breast cancer. Cancer 1975; 35: 499-506.

Cornillot M, Verhaeghe M, Cappelarere P, et al: Place de la cytologic par ponction dans le diagnotic des tummeurs du sein (2267 examens cytologiques). Lille Med 1971; 16: 1027-1031.

Webb AJ: Through a glass darkly (the development of needle aspiration biopsy). Bristol Med Chir J 1974; 89: 59-68.

Greig EDW, Gray ACH: Note on the lymphatic glands in sleeping sickness. Lancet 1904; I: 1570.

Hirschfeld H: Bericht ueber einige histologischmikrosko- pische und experimentelle arbeiten bei den boesartigen geschwuelsten. Z Krebsforsch 1919; 16: 33-39.

Guthrie CG: Gland puncture as a diagnostic measure. Bull Johns Hopkins Hosp 1921; 32: 266-269.

Martin HE, Ellis EB: Biopsy by needle puncture and aspiration. Ann Surg 1930; 62: 169-181.

Martin HE, Ellis EB: Aspiration biopsy. Surg Gynecol Obstet 1934; 59: 578-589.

Stewart FW: The diagnosis of tumors by aspiration. Am J Pathol 1933; 9: 801-813.

Koss LG, Woyke S, Olszewski W: Aspiration biopsy: cytologic interpretation and histologic bases. New York: Igaku-Shoin, 1984.

Kaminsky DB: Aspiration biopsy for the community hospital. New York: Masson Publishing, 1981.

Frable MA, Frable WJ: Fine needle aspiration biopsy revisit- ed. Laryngoscope 1982; 92: 1414-1418.

Kaminsky DB: Aspiration biopsy in the context of the new medicare fiscal policy. Acta Cytol 1984; 28: 333-336.

Abele JS, Miller TR, Goodson WH Ill, et al: Fine needle aspiration of palpable breast masses. Arch Surg 1983; 118: 859-863.

Livraghi T, Damascelli B, Zombardi C, et al: Risk in fine- needle abdominal biopsy. J Clin Ultrasound 1983; 11: 77-81.

Goldstein HM, Zornoza J, Wallace S, et al: Percutaneous fine needle aspiration biopsy of pancreatic and other abdominal masses. Radiology 1977; 123: 319-322.

Berquist TH, Bailey PB, Cortese DA, et al: Transthoracic needle biopsy. Accuracy and complications in relation to location and type of lesion. Mayo Clin Proc 1980; 55: 475-48 1.

27.

28.

29.

30.

31.

32.

33.

34.

35.

36.

37.

38.

39.

40.

41.

42.

43.

44.

45.

46.

47.

48.

49.

50.

51.

Flower CDR, Verney GI: Percutaneous needle biopsy of thoracic lesions-an evaluation of 300 biopsies. Clin Radio1 1979; 30: 215-218.

Ferrucci JT Jr, Wittenberg J, Margolies MN, et al: Malignant seeding of the tract after thin needle aspiration biopsy. Radiology 1979; 130: 345-346.

Smith FP, MacDonald JS, Schein S, et al: Cutaneous seeding of pancreatic cancer by skinny needle aspiration biopsy. Arch Intern Med 1980; 140: 855.

Sinner WN, Zajicek J: Implantation metastasis after percutaneous transthoracic needle aspiration biopsy. Acta Radio1 Diagn 1976; 17: 473-480.

Robbins GF, Brothers JH, Eberhart WF, et al: Is aspiration biopsy of breast cancer dangerous to the patient? Cancer 1954; 7: 774-778.

Berg JW, Robbins G: A late look at the safety of aspiration biopsy. Cancer 1962; 15: 826-827:

Frable WJ: Thin needle aspiration biopsy. Philadelphia: WB Saunders, 1983.

Sinner WN: Complications of percutaneous transthoracic needle aspiration biopsy. Acta Radio1 Diagn 1976; 17: 813-828.

Sage1 SS, Ferguson TB, Forrest JV, et al: Percutaneous transthoracic aspiration needle biopsy. Ann Thorac Surg 1978; 26: 399-405.

Von Schreeb T, Arner 0, Skousted G, et al: Renal adenocar- cinema. Is there risk of spreading tumor cells in diagnostic puncture? Stand J Urol Nephrol 1967; 1: 270-276.

Crile G Jr, Esselstyn CB Jr, Hawk WA: Needle biopsy in the diagnosis of thyroid nodules appearing after radiation. N Engl J Med 1979; 301: 997-999.

Hajdu SI, Melamed MR: Limitations of aspiration cytology in the diagnosis of primary neoplasms. Acta Cytol 1984; 28: 337-345.

Kline TS, Merriam JM, Shapshay SM: Aspiration biopsy cytology of the salivary gland. Am J Clin Pathol 1981; 76: 263-269.

Frable WJ: Fine needle aspiration biopsy: a review. Hum Pathol 1983; 14: 9-28.

Kline TS, Neal HS: Needle aspiration biopsy: diagnosis of subcutaneous nodules and lymph nodes. JAMA 1976; 235: 2848-2850.

Cardozo PL: The cytologic diagnosis of lymph node punc- tures. Acta Cytol 1964; 8: 194-204.

Deeley TJ: Needle biopsy. Glasgow: Butterworth and Com- pany, 1974.

Behm FG, O’Dowd GJ, Frable WJ: Fine needle aspiration effects on benign lymph node histology. Am J Clin Pathol 1984; 82: 195-198.

Orell SR, Skinner JM: The typing of non-Hodgkin’s lymphomas using fine needle aspiration cytology. Pathology 1982; 14: 389-394.

Friedman M, Kim U, Shimaoka K, et al: Appraisal of aspiration cytology in the management of Hodgkin’s disease. Cancer 1980; 45: 1653-1663.

Desmet V, Beet? J, Reybrouck G: Value of the cytological diagnosis of Hodgkin’s disease in comparison with histo- logical findings. Sangre 1964; 9: 73-77.

Rosen P, Hajdu SI, Foote FW: Diagnosis of carcinoma of the breast by aspiration biopsy. Surg Gynecol Obstet 1972; 134: 837-838.

Kern WH: The diagnosis of breast cancer by fine needle aspiration smears. JAMA 1979; 241: 1125-l 127.

Johsen C, Bjurstam N: Diagnostic methods in breast cancer. World J Surg 1977; 1: 290-294.

Hahn P, Hallberg 0, Schnurer LB: Combination of clinical examination, mammography, and aspiration cytology in the diagnosis of carcinoma of the breast (179 cases).



52. Strahlentherapie 1980; 156: 475-479.

Esposti PL: Aspiration biopsy cytology in the diagnosis and management of prostatic carcinoma. Stockholm: Stahl and Accidenstryet, 1974.

53. Ljung BM, Cherrie R, Kaufman J: Fine needle aspiration

54.

55.

56.

57.

58.

59.

60.

61.

62.

63.

64.

65.

66.

67.

68.

69.

biopsy of the prostate gland: a study of 103 cases with histoloaical followuu. J Urol 1986: 135: 955-958.

Kaufman jJ, Rosenthal M, Goodwin WE: Methods of diagnosis of carcinoma of the prostate. J Urol 1954; 72: 450-465.

Lauby VW, Burnett WE, Rosemond GP, et al: Value and risk of biopsy of pulmonary lesions by needle aspiration. J Thorac Cardiovasc Surg 1965; 49: 159-172.

Wescott JL: Direct percutaneous needle aspiration of local- ized pulmonary lesions. Radiology 1980; 137: 31-35.

Lalli AF, McCormack LJ, Zelch M, et al: Aspiration biopsies of chest lesions. Radiology 1978; 127: 35-40.

Sinner WN: Pulmonary neoplasms diagnosed with transthoracic needle biopsy. Cancer 1979; 43: 1533-1540.

Dahlgren SE, Lind B: Comparison between diagnostic results obtained by transthoracic needle biopsy and by sputum cytology. Acta Cytol 1972; 16: 53-58.

Landman S, Burgener FA, Kim GHK: Comparison of bron- chial brushing and percutaneous needle aspiration biopsy in the diagnosis of malignant lung lesions. Radiology 1975; 115: 275-278.

Francis D, Brogeskov S: Progress in preoperative diagnosis of pulmonary lesions. Acta Cytol 1975; 19: 231-234.

Nasiell M: Diagnosis of lung cancer by aspiration biopsy and a comparison between this method and exfoliative cytology. Acta Cytol 1967; 11: 114-l 19.

Lundquist A: Fine needle aspiration biopsy of the liver. Acta Med Stand (suppl) 1971; 520: l-28.

Johansen P, Svendsen KN: Scan-guided fine needle aspiration biopsy in malignant hepatic disease. Acta Cytol 1978; 22: 292-296.

Seifert G, Kloppel G: Diagnostic value of pancreatic biopsy. Pathol Res Pratt 1979; 164: 357-384.

Katz RL, Pate1 S, MacKay B, et al: Fine needle aspiration cytology of the adrenal gland. Acta Cytol 1984: 28: 269-282,

Akhtar M, Ali MA, Owen EW: Application of electron microscopy in the interpretation of fine needle aspiration biopsies. Cancer 1981; 48: 2458-2463.

Stark P, Hildebrandt-Stark HE: Electron microscopy of cells obtained by fine needle aspiration of lung lesions. Radiol- ogy 1982; 22: 327-328.

Domagala W, Kahan AV, Koss LG: A simple method of

70.

71.

72.

73.

74.

75.

76.

77.

78.

79.

80.

81.

82.

83.

preparation and identification of cells for scanning electron microscopy. Acta Cytol 1979; 23: 140-146.

Atkin NB, Kay R: Prognostic significance of modal DNA value and other factors in malignant tumors based on 1465 cases. Br J Cancer 1979; 40: 210-221.

Gaub J, Auer G, Zetterberg A: Quantitative cytochemical aspects of a combined Feuigen naphthol yellow S staining procedure for the simultaneous determination of nu- clear and cytoplasmic proteins and DNA in mammalian cells. Exp Cell Res 1975; 92: 323-332.

Auer G, Caspersson T, Wallgren A: DNA content and survival in mammary carcinoma. Anal Quantum Cytol 1980; 2: 161-165.

Zetterberg A, Esposti P-L.: Prognostic significance of nucle- ar DNA levels in prostatic carcinoma. Stand J Urol Neph- rol 1980; 55 (suppl): 53-59.

Koss LG, Wolley RC, Schreiber K, et al: Flow microfluoro- metric analysis of nuclei isolated from various normal and malignant human epithelial tissues. J Histochem Cyto- them 1977; 25: 565-572.

Miller TR, Bottles K, Abele JS, et al: Neuroblastoma,diagnosed by fine needle aspiration biopsy. Acta Cytol 1985; 29: 461-468.

De Lellis RA, Sternberger LA, Mann RB, et al: Immunoperox- idase techniques in diagnostic pathology. Am J Clin Pathol 1979; 71: 483-488.

Falini B, Taylor CR: New developments in immunoperoxidase techniques and their applications. Arch Pathol Lab Med 1983; 107: 105-117.

Kennett RH, McKearn TJ, Bechtol KB, eds: Monoclonal antibodies hybridomas: a new dimension in biological analy- ses. New York: Plenum, 1980.

Martin SE, Zhang HZ, Magyarosy E, et al: Immunologic methods in cytology: definitive diagnosis of non-Hodg- kin’s lymphomas using immunologic markers for T- and B- cells. Am J Clin Pathol 1984; 82: 666-673.

Koprowski H, Steplewski Z, Herlyn D, et al: Study of antibodies against human melanomas produced by somatic cell hybrids. Proc Natl Acad Sci USA 1978; 75: 3405-3409.

Kennett RH, Gilbert F: Hybrid myelomas producing antibodies against a human neuroblastoma antigen present in fetal brain. Science 1979; 203: 1120-l 121.

Herlyn M, Steplenski Z, Herlyn D, et al: Colorectal carcinoma specific antigen: detection by means of monoclonal antibodies. Proc Natl Acad Sci USA 1979; 76: 1438-1442.

Koss LG: Thin needle aspiration biopsy (editorial). Acta Cytol 1980; 24: 13.


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Fine needle aspiration biopsy: Has its time come?