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Fine needle cytologic diagnosis of thyroid nodules
Fine Needle Cytologic Diagnosis of Thyroid Nodules Review and Report of 300 Cases
Thomas A. Colacchio, MD, New York, New York Paul LoGerfo, MD, New York, New York Carl R. Felnd, MD, New York, New York
Nontoxic nodular goiter is a relatively common disorder in North America, affecting about 4 to 7 percent of the population [1,2]. Despite this, the incidence of thyroid cancer is low, comprising only 0.5 percent of all malignancies [3]. Most series report about a 4 to 5 percent malignancy rate [4,5] in thyroid nodules that are surgically excised. Given this large population requiring evaluation and the relatively low incidence of malignancy, we need reliable criteria to identify patients with thyroid nodules who are likely to have a neoplasm. Clinical assessment, thyroid function tests, response to suppression, scanning techniques and ultrasonography have been poor parameters for assessing solid nodules. Similarly, screening programs using serum thyroglobulin levels have failed to identify patients requiring excision [6]. Based on all of these criteria, the incidence of neoplasm at operation has been only 1 to 35 percent
[7,81. Coarse needle biopsy and more recently fine needle biopsy with cytologic diagnosis have been reported successful in evaluating thyroid nodules. To evaluate the sensitivity of these methods, we performed fine needle biopsy with cytologic evaluation in 300 consecutive thyroid nodules seen by the thyroid group of the General Surgery Service at Columbia-Presbyterian Medical Center. The diagnoses were then From the Department of Surgery, Columbla College of Physicians and Surgeons ColumblaPresbyterian Medical Center, New York, New York Requests for reprints should be addressed to Thomas A Colacchio. MD. Department of Surgery, Columbia College of physicians and Surgeons, Columbii-Presbyter~an Medical Center, 630 West 168th Street, New York, New York 10032 Presented at the 26th Annual Meeting of the Soctety of Head and Neck Surgeons, San Francisco, California. May 14-17, 1980
568
confirmed by either coarse needle biopsy, surgical excision, clinical follow-up or a combination of the three. Material
and Methods
Three hundred patients with thyroid nodules seen by the thyroid group of the General Surgery Service at Columbia-presbyterian Medical Center were evaluated. Each patient had had thyroid scanning that showed the nodule to be hypofunctioning. Sixteen percent of the patients were male and 84 percent female. The age range was 14 to 80 years; however, 60 percent of the patients were between 30 and 60 years of age. All 300 patients underwent fine needle aspiration cytologic diagnosis of their nodules. Coarse needle biopsy with or without surgical excision was then performed in 225 patients. Twenty-five of the remaining 75 patients also underwent surgery. The technique for fine needle biopsy is as follows. With the patient lying supine, the neck is extended and the skin and thyroid capsule overlying the nodule are infiltrated with a local anesthetic. A 22 gauge needle on a 5 cc syringe is passed through the nodule from medial to lateral in a plane parallel to the trachea in order to avoid the sternocleidomastoid muscle. This is done three to six times with separate smears obtained each time. If cyst fluid was found, it was centrifuged and sent for cytologic analysis. If the patient was then to undergo coarse needle biopsy, this was done through the same infiltrated area with a Tru-cute trocar biopsy needle in the standard manner and the specimens were sent for histopathologic evaluation. The cytologic specimens were prepared with Papanicolaou staining techniques and evaluated by a cytopathologist. The cytologic diagnostic categories were: malignant, highly suspicious for malignancy, atypical, benign, adenoma and thyroiditis. The patients then began either Ts or T4 thyroid hormone replacement therapy and
The American Journal ol Surgery
Fine Needle Cytologic Diagnosis of Thyroid Nodules
TABLE I
Results of Cytologic DlagnoSls Compared With the Final Diagnosis
Cytologic Diagnosis
Cancer
Malignant or suspicious Adenoma Atypical or benign Thyroiditis
19 1 3
Total
23
..
Adenoma
Final Diagnosis Nontoxic Nodular Goiter
. .
2 1 232 6
32
241
22 10
awaited the results of cytologic evaluation and biopsy, at which time the decision was made as to the mode of treatment and follow-up. The patients were followed up for 6 months to 4 years.
Thyroiditis
Total
2
. .
22 24 246 6
4
300
.. 3
There were no complications with the fine needle biopsy technique. Coarse needle biopsy resulted in one hematoma that did not require hospitalization or treatment.
Results All 300 fine needle biopsies had adequate specimens for cytologic evaluation. Of the 300 nodules biopsied, 33 (11 percent), were cystic, 21 (7 percent) partially cystic, and 246 (82 percent) solid. Table I shows the results of cytologic diagnosis compared with the final diagnosis. In 80 patients the final diagnosis was based on surgical removal of the nodule, in 170 the diagnosis was confirmed by coarse needle biopsy and clinical follow-up, and in 50 the diagnosis was confirmed by clinical follow-up only. The latter group contains 33 patients whose nodules were cystic and disappeared without recurrence after aspiration and 17 patients whose nodules had decreased in size or disappeared with suppression therapy. All of the coarse needle biopsy patients not undergoing surgery were also placed on suppression therapy, and none had an increase in the size of the nodule or evidence of new nodule growth. In the 300 nodules, there were 23 cancers (7.7 percent), and 32 adenomas, for an 18 percent incidence of neoplasia. Of the 248 patients with a benign cytologic diagnosis, 3 had false-negative findings on fine needle biopsy. Of these three, one had a coarse needle biopsy that showed microfollicular adenoma versus carcinoma, another with a coarse needle biopsy showing nontoxic nodular goiter had pulmonary metastases and markedly elevated serum thyroglobulin, and the third was unable to have coarse needle biopsy but had a microscopic carcinoma at operation. Therefore, the coarse needle biopsy diagnosis differed from the fine needle diagnosis in only 1 case in 300. Similarly, there were four false-positive results, three of which proved to be nontoxic nodular goiter and one thyroiditis. Three of these patients underwent surgery, and in one had coarse needle biopsy demonstrated adenomatous hyperplasia in nontoxic nodular goiter and not adenoma.
volume140, octobef 1980
Comments The management of patients with thyroid nodules has traditionally been difficult due to the magnitude of the problem and the relative insensitivity of the commonly available tests used to evaluate them. It is estimated that 4 to 7 percent of the population in North America has nontoxic nodular goiter [1,2]. However, thyroid cancer accounts for only 0.5 percent of all malignancies in the United States [3], and most series show that only 4 to 5 percent of thyroid nodules biopsied are cancerous. Most clinicians agree that all nodules that are malignant, and probably those which are true adenomas, should have some form of surgical excision. However, the use of clinical assessment, response to thyroid suppression, thyroid scans and ultrasonography have in the past resulted in only a 10 to 35 percent incidence of true neoplasm (carcinoma or adenoma) among surgically removed nodules (unpublished data: Columbia-Presbyterian Medical Center series). In an attempt to decrease the number of unnecessary thyroid operations, some groups began to use needle biopsy of nodules to determine malignancy. Cutting needle biopsies (for example, Vim Silverman) were performed in 135 patients by Crile and Hawk [4] at the Cleveland Clinic. Of this group, 102 had solid nodules and would have undergone operation; however, needle biopsy gave a diagnosis of cancer in 5 patients or 4 percent. Only seven patients underwent surgery, three of whom had benign goiter. Based on these findings, they estimate that needle biopsy will decrease thyroid operations by 90 percent. Wang et al [9] reported more than 1,000 coarse needle biopsies with a 90 percent adequate specimen rate. Of 906 biopsies, 816 nodules were benign and 90 underwent surgical excision. The needle biopsy diagnoses were confirmed in 81 patients (90 percent) at
569
Colacchio et al
operation, with four false-negative results in patients with follicular carcinoma whose biopsies were thought to show follicular adenoma. There were no false-positive results. Opponents of this technique argue that the procedure is hazardous and carries with it the possibility of implanting tumor cells along the needle tract. In 2,000 such biopsies at the Cleveland Clinic, however, only one case of tumor implantation was found, and there was only one complication, a chest wall ecchymosis. In the series of Wang et al [9] there was also one case of tumor implantation in the needle tract which was not a primary thyroid carcinoma, however, but a metastatic renal tumor. Similarly, Kirstaedter et al [5] reported on 900 needle biopsies with no case of tumor implantation and no complications. Despite these results, needle biopsy does carry some risk and also requires a fair amount of expertise for adequate sampling. Because of this, fine needle aspiration with cytology, which has been enthusiastically promoted for many organs by Scandinavian investigators [lo], has become increasingly popular in the United States. Several recent reports have stressed both the reliability of sampling and the sensitivity of cytologic diagnosis. Schnurer and Widstrom [II] reported that of 303 patients undergoing surgery, 284 (94 percent) had interpretable cytology by fine needle biopsy, and 27 of 28 cases of cancer were diagnosed as either malignant or highly suspicious. In a much earlier series, Einhorn and Franzer [12] were able to cytologically identify 48 of 52 thyroid cancers. Gershengorn et al [13] reported that of 33 patients undergoing excisional biopsy, 32 (97 percent) had interpretable cytology, with one false-negative and three false-positive results. Walfish et al [14] studied 150 solitary hypofunctioning nodules, 90 of which underwent surgical excision and histologic comparison with the fine needle biopsy diagnosis. Adequate cytologic diagnosis was obtained in 92 percent of the excised lesions, with an overall diagnostic accuracy of 95 percent for solid lesions and 88 percent for cystic or mixed lesions. Malignant lesions were diagnosed correctly 71 percent of the time with no false-positive results but 5 of 17 false-negative results. The important finding was that the overall incidence of neoplasm (adenoma and carcinoma) among the surgical specimens was 66 percent. Thus they were able to halve the number of unnecessary thyroid operations with fine needle biopsy and cytology and assert that the false-negative biopsies were primarily due to inadequate or unrepresentative material and not misinterpretation by the cytologist. The thyroid group at Columbia-Presbyterian
570
Medical Center has been performing both fine and coarse needle biopsy for 4 years, and it is our aim to review our data and arrive at a reasonable approach to patients with a thyroid nodule. Most patients seen by our group have already been evaluated by thyroid function studies and thyroid scan. Those with hyperfunctioning nodules usually are not referred for evaluation since they are considered to be at minimal risk for developing malignancy [15]. Thus we are left with the patients with hypofunctioning thyroid nodules. Given this group, it is our goal to identify the patients with a neoplasm as expeditiously as possible in order to perform surgical excision. The remaining patients will be placed on thyroid hormone suppression therapy and followed up clinically. To this end, all patients underwent fine needle biopsy with cytologic evaluation. For this series, in an attempt to corraborate our cytologic diagnoses, all but 75 patients also underwent coarse needle biopsy with histopathologic evaluation. The patients with cystic nodules that had no residual after aspiration or whose nodules were too small (1 cm) or in a difficult location were not subjected to coarse needle biopsy. Based on this evaluation, 80 of these patients came to some form of surgical excision. Our criteria for surgical excision were (1) malignancy, (2) cells suspicious for malignancy, (3) adenoma, (4) growth on suppression, and (5) new nodule growth on suppression. When there was a discrepancy between the fine and coarse needle biopsy diagnoses, the more grave of the two was considered correct. Of the 22 nodules considered malignant or suspicious based on cytologic diagnosis, 3 were benign, and of the 24 patients with a preoperative diagnosis of adenoma, 1 had nontoxic nodular goiter. Of the 249 patients with a benign diagnosis, one patient had coarse needle biopsy showing microfollicular adenoma versus carcinoma, one had a microscopic cancer in a nodule too small for coarse needle biopsy, and one patient had metastatic disease and markedly elevated serum thyroglobulin from a small carcinoma in a multinodular gland. Thus of the 24 cancers in our series, 19 were diagnosed by fine needle biopsy alone for a diagnostic yield of 83 percent; of the 300 cytologies, 4 patients were incorrectly recommended for surgery, for a false-positive rate of 1 percent. Of the 249 benign cytologic diagnoses, there were 3 cancers, for a false-negative rate of 1 percent. The diagnostic accuracy for adenomas is somewhat less: 22 of 32 adenomas (68 percent) were diagnosed with fine needle biopsy cytology alone. The distinction between a true adenoma and adenomatous hyperplasia in nontoxic nodular goiter is difficult for the cytologist to make and accounts for this 30 percent
The American Journal of Surgery
Fine Needle Cytologic
inaccuracy. Even though the background cell appearance of hyperplasia (with white blood cells, histiocytes and dead cell debris) is helpful, coarse needle biopsy is more reliable with these nodules. As in other reports, we found it difficult to distinguish between a follicular adenoma and a well differentiated follicular carcinoma [9,14]. The final group, which is very difficult to identify with fine needle biopsy, is the patients with thyroiditis; they also require coarse needle biopsy for greater accuracy. Nevertheless, based only on fine needle biopsy with cytologic diagnosis, our incidence of neoplasm found at operation was 69 percent. This is double our previous incidence before fine needle biopsy was performed and reflects the decreased number of unnecessary thyroid excisions done at our institution. We now perform fine needle biopsy in the following groups of patients: those with cytologic diagnosis of adenoma or thyroiditis, and all patients whom we intend to follow on suppression therapy with lesions large enough to allow coarse needle biopsy. The latter group is included in an attempt to identify the 1 percent of false-negative diagnoses made by fine needle biopsy alone. Based on this evaluation, our criteria for surgery remain the same, and we believe that a 70 percent incidence of neoplasm at time of operation is most acceptable. It is important to note, however, that these results depend on the experience of the sampler, the expertise of the cytopathologist and the follow-up evaluation performed by the same clinician. Summary Three hundred patients with thyroid nodules were evaluated with fine needle biopsy and cytologic evaluation. Nineteen of 23 cancers were diagnosed by fine needle biopsy alone, for a yield of 83 percent.
Volume 140, Octokr IS80
Diagnosis
of Thyroid Nodules
Four of 300 diagnoses (1 percent) were false-positive, and the incidence of neoplasm at operation was 68 percent. We believe that fine needle biopsy will greatly decrease the number of unnecessary thyroid resections.
References 1. Vander JB, Gaston EA, Dawber TR. Significance of nontoxic thyroid nodules: preliminary report N Engl J Med 1954;251: 970-3. 2. Stoffer RP, Welch JW, Hellwig CA, Chesky VE, McCuster EN. Nodular goiter: incidence. morphology before and after iodine prophylaxis and clinical diagnosis. Arch Intern Med 1980; 106:10-4. 3. Shimaoka K, Sokal JE. Thyroid cancer In: Ccnn HF, ed. Current therapy. Philadelphia: WB Saunders, 1988:438-40. 4. Crile G, Hawk WA. Aspiration biopsy of thyroid nodules. Surg Gynecol Obstet 1973;138:241-5. 5. Kirstaedter HJ, Gehrmann C, Schulzke R. Die percutane felnnadel-aspirationsbiopsie und cytolcgie tastbarer tumore. Verh Dtsch Ges Inn Med 1972;78:282-5. 8. Schneider AB. Favus MI, Stachura ME, et al. Plasma thyroglobulin in detecting thyroid carcinoma after childhood head and neck irradiation. Ann Intern Med 1977;88:29-34. 7. Miller JM, Hamburger JI, Kini S. Diagnosis of thyroid nodules. JAMA 1979;241:481-4. 8. Hill L. Thyroid suppression. Arch Surg 1974;108:403-5. 9. Wang C, Vickery AL, Maloof F. Needle biopsy of the thyroid. Surg Gynecol Obstet 1978;143:385-8. 10. Soderstrom N. Fine needle aspiration biopsy. New York: Grune & Stratton, 1988:98-102. 11. Schnuer L. Wktstrom A. Fine needle blopsy of the thyroid gland. Ann Dtol 1978,87:224-7. 12. Einhorn J, Franzer S. Thin needle biopsy in the diagnosis of thyroid disease. Acta Radio1 (Stockh) 1982;58:321-38. 13. Gershengom MC, McClurg MR. Chu EW, Hanson TA, Weintraub BD, Robbins J. Fine needle aspiration cytology in the preoperative diagnosis of thyroid nodules Ann Intern Med 1977;87:285-9. 14. Walfish PG, Hazani E, Strawbridge HT, Miskin M, Rosen IB. Combined ultrasound and needle aspiration cytology in the assessment and management of hypofunctioning thyroid nodules Ann Intern Med 1977;87:270-4. 15. Miller JM, Hamburger JI The thyroid scintiscan. I. The hot nodule. Radiology 1985;84:88-74.
571
Thomas A. Colacchio, MD, New York, New York Paul LoGerfo, MD, New York, New York Carl R. Felnd, MD, New York, New York
Nontoxic nodular goiter is a relatively common disorder in North America, affecting about 4 to 7 percent of the population [1,2]. Despite this, the incidence of thyroid cancer is low, comprising only 0.5 percent of all malignancies [3]. Most series report about a 4 to 5 percent malignancy rate [4,5] in thyroid nodules that are surgically excised. Given this large population requiring evaluation and the relatively low incidence of malignancy, we need reliable criteria to identify patients with thyroid nodules who are likely to have a neoplasm. Clinical assessment, thyroid function tests, response to suppression, scanning techniques and ultrasonography have been poor parameters for assessing solid nodules. Similarly, screening programs using serum thyroglobulin levels have failed to identify patients requiring excision [6]. Based on all of these criteria, the incidence of neoplasm at operation has been only 1 to 35 percent
[7,81. Coarse needle biopsy and more recently fine needle biopsy with cytologic diagnosis have been reported successful in evaluating thyroid nodules. To evaluate the sensitivity of these methods, we performed fine needle biopsy with cytologic evaluation in 300 consecutive thyroid nodules seen by the thyroid group of the General Surgery Service at Columbia-Presbyterian Medical Center. The diagnoses were then From the Department of Surgery, Columbla College of Physicians and Surgeons ColumblaPresbyterian Medical Center, New York, New York Requests for reprints should be addressed to Thomas A Colacchio. MD. Department of Surgery, Columbia College of physicians and Surgeons, Columbii-Presbyter~an Medical Center, 630 West 168th Street, New York, New York 10032 Presented at the 26th Annual Meeting of the Soctety of Head and Neck Surgeons, San Francisco, California. May 14-17, 1980
568
confirmed by either coarse needle biopsy, surgical excision, clinical follow-up or a combination of the three. Material
and Methods
Three hundred patients with thyroid nodules seen by the thyroid group of the General Surgery Service at Columbia-presbyterian Medical Center were evaluated. Each patient had had thyroid scanning that showed the nodule to be hypofunctioning. Sixteen percent of the patients were male and 84 percent female. The age range was 14 to 80 years; however, 60 percent of the patients were between 30 and 60 years of age. All 300 patients underwent fine needle aspiration cytologic diagnosis of their nodules. Coarse needle biopsy with or without surgical excision was then performed in 225 patients. Twenty-five of the remaining 75 patients also underwent surgery. The technique for fine needle biopsy is as follows. With the patient lying supine, the neck is extended and the skin and thyroid capsule overlying the nodule are infiltrated with a local anesthetic. A 22 gauge needle on a 5 cc syringe is passed through the nodule from medial to lateral in a plane parallel to the trachea in order to avoid the sternocleidomastoid muscle. This is done three to six times with separate smears obtained each time. If cyst fluid was found, it was centrifuged and sent for cytologic analysis. If the patient was then to undergo coarse needle biopsy, this was done through the same infiltrated area with a Tru-cute trocar biopsy needle in the standard manner and the specimens were sent for histopathologic evaluation. The cytologic specimens were prepared with Papanicolaou staining techniques and evaluated by a cytopathologist. The cytologic diagnostic categories were: malignant, highly suspicious for malignancy, atypical, benign, adenoma and thyroiditis. The patients then began either Ts or T4 thyroid hormone replacement therapy and
The American Journal ol Surgery
Fine Needle Cytologic Diagnosis of Thyroid Nodules
TABLE I
Results of Cytologic DlagnoSls Compared With the Final Diagnosis
Cytologic Diagnosis
Cancer
Malignant or suspicious Adenoma Atypical or benign Thyroiditis
19 1 3
Total
23
..
Adenoma
Final Diagnosis Nontoxic Nodular Goiter
. .
2 1 232 6
32
241
22 10
awaited the results of cytologic evaluation and biopsy, at which time the decision was made as to the mode of treatment and follow-up. The patients were followed up for 6 months to 4 years.
Thyroiditis
Total
2
. .
22 24 246 6
4
300
.. 3
There were no complications with the fine needle biopsy technique. Coarse needle biopsy resulted in one hematoma that did not require hospitalization or treatment.
Results All 300 fine needle biopsies had adequate specimens for cytologic evaluation. Of the 300 nodules biopsied, 33 (11 percent), were cystic, 21 (7 percent) partially cystic, and 246 (82 percent) solid. Table I shows the results of cytologic diagnosis compared with the final diagnosis. In 80 patients the final diagnosis was based on surgical removal of the nodule, in 170 the diagnosis was confirmed by coarse needle biopsy and clinical follow-up, and in 50 the diagnosis was confirmed by clinical follow-up only. The latter group contains 33 patients whose nodules were cystic and disappeared without recurrence after aspiration and 17 patients whose nodules had decreased in size or disappeared with suppression therapy. All of the coarse needle biopsy patients not undergoing surgery were also placed on suppression therapy, and none had an increase in the size of the nodule or evidence of new nodule growth. In the 300 nodules, there were 23 cancers (7.7 percent), and 32 adenomas, for an 18 percent incidence of neoplasia. Of the 248 patients with a benign cytologic diagnosis, 3 had false-negative findings on fine needle biopsy. Of these three, one had a coarse needle biopsy that showed microfollicular adenoma versus carcinoma, another with a coarse needle biopsy showing nontoxic nodular goiter had pulmonary metastases and markedly elevated serum thyroglobulin, and the third was unable to have coarse needle biopsy but had a microscopic carcinoma at operation. Therefore, the coarse needle biopsy diagnosis differed from the fine needle diagnosis in only 1 case in 300. Similarly, there were four false-positive results, three of which proved to be nontoxic nodular goiter and one thyroiditis. Three of these patients underwent surgery, and in one had coarse needle biopsy demonstrated adenomatous hyperplasia in nontoxic nodular goiter and not adenoma.
volume140, octobef 1980
Comments The management of patients with thyroid nodules has traditionally been difficult due to the magnitude of the problem and the relative insensitivity of the commonly available tests used to evaluate them. It is estimated that 4 to 7 percent of the population in North America has nontoxic nodular goiter [1,2]. However, thyroid cancer accounts for only 0.5 percent of all malignancies in the United States [3], and most series show that only 4 to 5 percent of thyroid nodules biopsied are cancerous. Most clinicians agree that all nodules that are malignant, and probably those which are true adenomas, should have some form of surgical excision. However, the use of clinical assessment, response to thyroid suppression, thyroid scans and ultrasonography have in the past resulted in only a 10 to 35 percent incidence of true neoplasm (carcinoma or adenoma) among surgically removed nodules (unpublished data: Columbia-Presbyterian Medical Center series). In an attempt to decrease the number of unnecessary thyroid operations, some groups began to use needle biopsy of nodules to determine malignancy. Cutting needle biopsies (for example, Vim Silverman) were performed in 135 patients by Crile and Hawk [4] at the Cleveland Clinic. Of this group, 102 had solid nodules and would have undergone operation; however, needle biopsy gave a diagnosis of cancer in 5 patients or 4 percent. Only seven patients underwent surgery, three of whom had benign goiter. Based on these findings, they estimate that needle biopsy will decrease thyroid operations by 90 percent. Wang et al [9] reported more than 1,000 coarse needle biopsies with a 90 percent adequate specimen rate. Of 906 biopsies, 816 nodules were benign and 90 underwent surgical excision. The needle biopsy diagnoses were confirmed in 81 patients (90 percent) at
569
Colacchio et al
operation, with four false-negative results in patients with follicular carcinoma whose biopsies were thought to show follicular adenoma. There were no false-positive results. Opponents of this technique argue that the procedure is hazardous and carries with it the possibility of implanting tumor cells along the needle tract. In 2,000 such biopsies at the Cleveland Clinic, however, only one case of tumor implantation was found, and there was only one complication, a chest wall ecchymosis. In the series of Wang et al [9] there was also one case of tumor implantation in the needle tract which was not a primary thyroid carcinoma, however, but a metastatic renal tumor. Similarly, Kirstaedter et al [5] reported on 900 needle biopsies with no case of tumor implantation and no complications. Despite these results, needle biopsy does carry some risk and also requires a fair amount of expertise for adequate sampling. Because of this, fine needle aspiration with cytology, which has been enthusiastically promoted for many organs by Scandinavian investigators [lo], has become increasingly popular in the United States. Several recent reports have stressed both the reliability of sampling and the sensitivity of cytologic diagnosis. Schnurer and Widstrom [II] reported that of 303 patients undergoing surgery, 284 (94 percent) had interpretable cytology by fine needle biopsy, and 27 of 28 cases of cancer were diagnosed as either malignant or highly suspicious. In a much earlier series, Einhorn and Franzer [12] were able to cytologically identify 48 of 52 thyroid cancers. Gershengorn et al [13] reported that of 33 patients undergoing excisional biopsy, 32 (97 percent) had interpretable cytology, with one false-negative and three false-positive results. Walfish et al [14] studied 150 solitary hypofunctioning nodules, 90 of which underwent surgical excision and histologic comparison with the fine needle biopsy diagnosis. Adequate cytologic diagnosis was obtained in 92 percent of the excised lesions, with an overall diagnostic accuracy of 95 percent for solid lesions and 88 percent for cystic or mixed lesions. Malignant lesions were diagnosed correctly 71 percent of the time with no false-positive results but 5 of 17 false-negative results. The important finding was that the overall incidence of neoplasm (adenoma and carcinoma) among the surgical specimens was 66 percent. Thus they were able to halve the number of unnecessary thyroid operations with fine needle biopsy and cytology and assert that the false-negative biopsies were primarily due to inadequate or unrepresentative material and not misinterpretation by the cytologist. The thyroid group at Columbia-Presbyterian
570
Medical Center has been performing both fine and coarse needle biopsy for 4 years, and it is our aim to review our data and arrive at a reasonable approach to patients with a thyroid nodule. Most patients seen by our group have already been evaluated by thyroid function studies and thyroid scan. Those with hyperfunctioning nodules usually are not referred for evaluation since they are considered to be at minimal risk for developing malignancy [15]. Thus we are left with the patients with hypofunctioning thyroid nodules. Given this group, it is our goal to identify the patients with a neoplasm as expeditiously as possible in order to perform surgical excision. The remaining patients will be placed on thyroid hormone suppression therapy and followed up clinically. To this end, all patients underwent fine needle biopsy with cytologic evaluation. For this series, in an attempt to corraborate our cytologic diagnoses, all but 75 patients also underwent coarse needle biopsy with histopathologic evaluation. The patients with cystic nodules that had no residual after aspiration or whose nodules were too small (1 cm) or in a difficult location were not subjected to coarse needle biopsy. Based on this evaluation, 80 of these patients came to some form of surgical excision. Our criteria for surgical excision were (1) malignancy, (2) cells suspicious for malignancy, (3) adenoma, (4) growth on suppression, and (5) new nodule growth on suppression. When there was a discrepancy between the fine and coarse needle biopsy diagnoses, the more grave of the two was considered correct. Of the 22 nodules considered malignant or suspicious based on cytologic diagnosis, 3 were benign, and of the 24 patients with a preoperative diagnosis of adenoma, 1 had nontoxic nodular goiter. Of the 249 patients with a benign diagnosis, one patient had coarse needle biopsy showing microfollicular adenoma versus carcinoma, one had a microscopic cancer in a nodule too small for coarse needle biopsy, and one patient had metastatic disease and markedly elevated serum thyroglobulin from a small carcinoma in a multinodular gland. Thus of the 24 cancers in our series, 19 were diagnosed by fine needle biopsy alone for a diagnostic yield of 83 percent; of the 300 cytologies, 4 patients were incorrectly recommended for surgery, for a false-positive rate of 1 percent. Of the 249 benign cytologic diagnoses, there were 3 cancers, for a false-negative rate of 1 percent. The diagnostic accuracy for adenomas is somewhat less: 22 of 32 adenomas (68 percent) were diagnosed with fine needle biopsy cytology alone. The distinction between a true adenoma and adenomatous hyperplasia in nontoxic nodular goiter is difficult for the cytologist to make and accounts for this 30 percent
The American Journal of Surgery
Fine Needle Cytologic
inaccuracy. Even though the background cell appearance of hyperplasia (with white blood cells, histiocytes and dead cell debris) is helpful, coarse needle biopsy is more reliable with these nodules. As in other reports, we found it difficult to distinguish between a follicular adenoma and a well differentiated follicular carcinoma [9,14]. The final group, which is very difficult to identify with fine needle biopsy, is the patients with thyroiditis; they also require coarse needle biopsy for greater accuracy. Nevertheless, based only on fine needle biopsy with cytologic diagnosis, our incidence of neoplasm found at operation was 69 percent. This is double our previous incidence before fine needle biopsy was performed and reflects the decreased number of unnecessary thyroid excisions done at our institution. We now perform fine needle biopsy in the following groups of patients: those with cytologic diagnosis of adenoma or thyroiditis, and all patients whom we intend to follow on suppression therapy with lesions large enough to allow coarse needle biopsy. The latter group is included in an attempt to identify the 1 percent of false-negative diagnoses made by fine needle biopsy alone. Based on this evaluation, our criteria for surgery remain the same, and we believe that a 70 percent incidence of neoplasm at time of operation is most acceptable. It is important to note, however, that these results depend on the experience of the sampler, the expertise of the cytopathologist and the follow-up evaluation performed by the same clinician. Summary Three hundred patients with thyroid nodules were evaluated with fine needle biopsy and cytologic evaluation. Nineteen of 23 cancers were diagnosed by fine needle biopsy alone, for a yield of 83 percent.
Volume 140, Octokr IS80
Diagnosis
of Thyroid Nodules
Four of 300 diagnoses (1 percent) were false-positive, and the incidence of neoplasm at operation was 68 percent. We believe that fine needle biopsy will greatly decrease the number of unnecessary thyroid resections.
References 1. Vander JB, Gaston EA, Dawber TR. Significance of nontoxic thyroid nodules: preliminary report N Engl J Med 1954;251: 970-3. 2. Stoffer RP, Welch JW, Hellwig CA, Chesky VE, McCuster EN. Nodular goiter: incidence. morphology before and after iodine prophylaxis and clinical diagnosis. Arch Intern Med 1980; 106:10-4. 3. Shimaoka K, Sokal JE. Thyroid cancer In: Ccnn HF, ed. Current therapy. Philadelphia: WB Saunders, 1988:438-40. 4. Crile G, Hawk WA. Aspiration biopsy of thyroid nodules. Surg Gynecol Obstet 1973;138:241-5. 5. Kirstaedter HJ, Gehrmann C, Schulzke R. Die percutane felnnadel-aspirationsbiopsie und cytolcgie tastbarer tumore. Verh Dtsch Ges Inn Med 1972;78:282-5. 8. Schneider AB. Favus MI, Stachura ME, et al. Plasma thyroglobulin in detecting thyroid carcinoma after childhood head and neck irradiation. Ann Intern Med 1977;88:29-34. 7. Miller JM, Hamburger JI, Kini S. Diagnosis of thyroid nodules. JAMA 1979;241:481-4. 8. Hill L. Thyroid suppression. Arch Surg 1974;108:403-5. 9. Wang C, Vickery AL, Maloof F. Needle biopsy of the thyroid. Surg Gynecol Obstet 1978;143:385-8. 10. Soderstrom N. Fine needle aspiration biopsy. New York: Grune & Stratton, 1988:98-102. 11. Schnuer L. Wktstrom A. Fine needle blopsy of the thyroid gland. Ann Dtol 1978,87:224-7. 12. Einhorn J, Franzer S. Thin needle biopsy in the diagnosis of thyroid disease. Acta Radio1 (Stockh) 1982;58:321-38. 13. Gershengom MC, McClurg MR. Chu EW, Hanson TA, Weintraub BD, Robbins J. Fine needle aspiration cytology in the preoperative diagnosis of thyroid nodules Ann Intern Med 1977;87:285-9. 14. Walfish PG, Hazani E, Strawbridge HT, Miskin M, Rosen IB. Combined ultrasound and needle aspiration cytology in the assessment and management of hypofunctioning thyroid nodules Ann Intern Med 1977;87:270-4. 15. Miller JM, Hamburger JI The thyroid scintiscan. I. The hot nodule. Radiology 1985;84:88-74.
571