Role of Fine-Needle Aspiration Cytology in the Management of Thyroid Nodules: Review of Experience With 1,925 Cases Helio Bisi, M.D., Ph.D., Rosalinda Y. Asato de Camargo, Adhemar Longatto Filho, M.S.

In this review article, the authors present their experience with the management of thyroid nodules usingfine-needle aspiration cytology as the primary method of investigation. Diagn Cytopathol 1992;8:504-510. 0 1992 wiiey-Liss, Inc Key Words: Thyroid gland; Thyroid cancer; Thyroid disorders

Fine-needle aspiration cytology (FNAC) of the thyroid nodules is a well-known method used to obtain tissue fragments, fluid specimens, or smears. ‘-I6 The first studies on the usefulness of FNAC were performed more than a halfcentury ago, but only recently has this procedure been used in Brazil. ’’-I9 FNAC is easy, of low cost, and very safe.’ An additional advantage is the avoidance of unnecessary surgery, along with a high accuracy in differentiating benign and malignant lesions. 2 , 13,20-46 The efficacy of FNAC depends on various factors: experience in selecting and aspirating the palpable thyroid nodules in order to obtain a representative cellularity of the smears, proper preparation of the smears, as fixation and staining, and finally, a good knowledge and familiarity with the histopathology of the thyroid lesions. Since our group had a great interest in and much previous experience with thyroid necropsy and surgical techniques (unpublished data), we decided to undertake FNAC studies. We reviewed a total of 4,703 (3.6%) cases of thyroid lesions from the 131,466 necropsies of the Pathology Department files, Medical School, Sao Paulo University. From this large amount of autopsy information we identified 4,358 cases of non-neoplastic lesions (3.3%) and Received July 31, 1991. Accepted December 13, 1991. From the Pathology Department, Medical School of Sao Paulo University; Endocrinology Clinics, Sao Paulo County Hospital; and Division of Pathology, Adolfo Lutz Institute, Sao Paulo, Brazil. Address reprint requests to Prof. Dr. Helio Bisi, Pathology Department (FMUSP), Av. Dr. Arnaldo-455, CEP 01246, Sao Paulo-SP, B r a d


Diagnostic Cyiopaihology, Vol 8, No 5



345 cases of neoplastic lesions (0.26%) distributed as follows: 12 1 adenomas, 109 primary malignant neoplasias, and 1 15 metastatic neoplasias. We also reviewed the surgical material from the same Pathology Department which had similar numbers of cases. With this past experience we decided to introduce FNAC as a routine method in the thyroid lesions seen in the County Hospital. We also decided to report our diagnosis according to “cellular patterns,” which informs the diagnosis with great accuracy; these cytologic findings, when associated with clinical findings, have been helpful in the evaluation of thyroid nodules. With this clinico-pathologic correlation we suggest to the clinician the possible entity in the thyroid, and also suggest the thyroid lesions correlated with these “cellular patterns,” whenever possible. The “cellular patterns” and the cytological criteria used in our study are outlined below.

Inflammatory Pattern UP) Hushimoto ’s Diseuse The smears reveal lymphocytic infiltration with different degrees of cell maturation, plasma cells, and macrophages; multinucleated giant cells are observed occasionally. Epithelial cells with oxyphilic and granular cytoplasm are frequent (Hiirthle cells). These cells can exhibit large hyperchromatic nuclei, coarse chromatin, and prominent nucleoli. On the other hand, some large and reactive lymphocytes with typical and/or atypical mitosis are seen. Both findings can be misinterpreted as malignancY-48-57

Nonspecijk Lymphocytic Thyroiditis In contrast with Hashimoto’s disease, the smears reveal rare or absent Hurthle cells; in addition, one sees a great


1992 W I L t k L I S . I N C


number of mature lymphocytes, follicular cells, and high concentrations of colloid.


Subacute Thyroiditis The smears exhibit lymphocytes, macrophages, and frequently multinucleated giant cells, associated with neutrophils and normal epithelial cells; oxyphilic cells (Hiirthle) are scanty. 53

Medullary Pattern (MP) Out of the classical M P plasma cell-like, with granular and oxyphilic cytoplasm (Hiirthle cell-like), the diagnosis of this group is usually done by a process of elimination.

General Considerations The follicular pattern has been the great dilemma of the FNAC method in thyroid nodules, because it can be diagnosed both as adenomatous goiter and as follicular well-differentiated neoplasm (Fig. 1). Adenomatous goiter has a multifocal follicular origin 66; its evolution distorts the gland architecture, compressing the blood vessels and leading to an ischemic necrosis and hemorrhagic cysts. In FNAC it is represented by a F P and numerous macrophages with hemossider in pigments, and abundant colloid proteic substrate. The collagen denaturation due to necrosis leads to distrophic calcification detectable by X-ray or ultrasound. These areas must be excluded in FNAC since they are not representative for study. In a recent study, we could also observe that some follicles are lined by Hiirthle cells and/or small oxyphilic cells67; in FNAC, smears presenting only these cells can lead to a misinterpretation as a Hiirthle cell neoplasm. Well differentiated follicular neoplasms are of monoclonal origin. 66 The solitary nodules have follicle cells resembling those of the adenomatous goiter. In Brazil, where the goiter incidence is very high, 69 the FP detected by FNAC is frequently synonymous with goiter; in countries where goiter is rare, FP will correspond to differentiated neoplasms, as adenomas or carcinomas. 70*7' In our experience, from the cases of FP, we misled the diagnosis in only 2.4%. The high incidence of goiter in Brazil is an alert to the cytopathologist to a more attentive interpretation of this pattern, to avoid wrong diagnosis (Tables I, 11). 2092',23,24,30359-65

Papillary Pattern (PP) The epithelial cells are seen in a papillary arrangements; inflammatory and plasma cells could be present and the colloid is scanty. The classic nuclear appearance is significant and fundamental for the diagnosis, mainly in cases in which the papilliform projections are absent. Round or oval nuclei are seen with nuclear inclusions and/or nuclear crease 5657; follicular arrangements can be found in some cases." The cytoplasm of these cells is frequently abundant; Hiirthle cells are rare in papillary projections. Psammoma bodies have been described but were rarely found in our material.

Follicular Pattern (FP) Epithelial cells are distributed in solid clusters or in follicular arrangements; isolated cells are frequently observed. The cytoplasm is scanty and rarely oxyphilic. The nuclei are round or oval with dense or slightly granular chromatin; nucleoli could be observed in cases with a granulous aspect of the nucleus. This pattern can be found in follicular neoplasms (benign and malignant) and adenomatous goiter. In our experience, a dense and homogeneous nuclear aspect suggests goiter; when the chromatin margin is granular and the nuclei irregular, we consider it to be a neoplastic condition.

Hiirthle Pattern (HP) The Hiirthle cells are present in trabecullar or follicular arrangement or in isolated distribution. The nuclei are mono- or pleomorphic, single or double. Granulous chromatin and prominent nucleoli are seen. The colloid is frequently scanty. In the H P are included Hiirthle cell adenoma and Hiirthle cell carcinoma. Cytoplasm of these cells is voluminous, oxyphilic, and slightly granular.

Undifferentiated Pattern (UP) Small, large multinucleated, and fusiform cells are the predominant elements in this pattern. Atypical mitosis is more frequently seen in the presence of fusiform and large multinucleated cells. In the case of an UP mainly composed Of there is no association with Other types, and the tumor exhibits a homogeneous patterns.

Table I.

Cytologic Pattern Diagnosis in Thyroid F N A C

Cytologic patterri


Accir rucy

of' ca.res


Medullary~' Undifferentiated Papillary Hiirthle Inflammatory Follicular

55 146 1,234



2 8

Oh 1 OOh


looh 81h

9X.7h 97.6'

"Papillary carcinoma. Misdiagnosed as medullary due to ah\riice of inc1usion5. hCorrect diagnosi5 confirmed by h~stopathology. 'Correct diagnosis confirmed by clinical and laboratory findings predominantly, and histopathology.

Diagnostic Cytopathology, Vol 8, No 5



Diugnostic Cytoputhology, Vol 8. No 5

FNA IN MANAGEMENT OF THYROID NODULES Table 111. FNAC of Thyroid Gland, Selected Pitfalls

Table 11. Other Findinas in FNAC

Cytologic findings


Number oJ cases



Metastatic neoplasm Others (lipoma, calcification) Suspicious for malignancy Cysts (hemorrhagic, thyrogloss, thymic, serose, epidermoid inclusion) Insufficient material

3 5 34


217 168





Final surgical pathology diagnosis

Cause oJfalse diagnosis (cytologic pirfalls)


Papillary carcinoma

Immuno peroxidase-calcitonin (IC) was false-positive due to number of isolated plasma-cell like elements


Papillary carcinoma

IC negative, congo red stain positive projections, absence of papillary projections


Papillary occult carcinoma

Aspiration of peri-neoplastic area


Hashimoto's disease

The FNAC was performed in an area without inflammatory cell arrangements of large nodule goiter


Papillary carcinoma

Nuclear classic signs of papillary carcinoma were absent (also in the surgicalspecimen); presence of great number of Hiirthle cells


Abenomatous goiter

The inflammatory infiltrate of mature lymphocytes associated with small oxyphilic cells was misinterpreted as Hashimoto's Disease


Papillary carcinoma Hashimoto's disease

The FNAC only reached the inflammatory. .part of the lesion




aCorrect diagnosis based in surgical pathology and/or clinical follow up. hData not included in index accuracy.

The pure Hurthle pattern invariably suggests neoplasm (Fig. 2), but pitfalls exist. In 60% of dyshormonogenic goiter studied in our department (unpublished data), we found follicles lined by Hurthle cells that can lead to a false-positive diagnosis in some instances. Adenomatous goiter can also present with Hiirthle cells lining the follicles, but in these cases we observed a great concentration of proteic colloid substrate, macrophages with hemossiderin, and normal follicular cells. When the FNAC obtains only Hurthle cells, the differential diagnosis between benign or malignant lesions is impossible. 67 Papillary and undifferentiated patterns, in general, present no major difficulties for interpretation; our FNAC results were 100% in accordance with the biopsies (Figs. 3-6). When a suspicious medullary pattern exists, it is essential to stain with congo red or immunoperoxidase. 72,73 In the immunostaining, the hemorrhagic areas of lesions must be carefully interpreted, in order to avoid falsepositive results, 74 as could happen in the macrophages with the haemossiderin. In cases of medullary carcinoma without amiloid, the congo red stain does not aid in the diagnosis. The smears showing small cells do not present difficulties to a diagnosis of malignancy (Fig. 7); in addition, immunoperoxidase stain can differentiate carcinoma from lymphomas. Inflammatory pattern (Figs. 8, 9) can lead to false-negative diagnosis when the punction removes only the inflammatory cells, releasing the epithelial clusters (Table 111). 75976

Original cytologic pattern






As described in the literature, careful attention should be paid when dealing with cystic lesions. 7740 In a previous study, we found 44% of papillary carcinomas with cysts. " Our procedure is to drain these cysts, to provide material for cytological interpretation, and for therapeutic value. We do not use saline or tetracycline injection for sclerosing purposes, as indicated in the literature, 82-R4 since this procedure can complicate the long follow-up that is essential in these cases. The role of FNAC in the management of nodules of the thyroid gland on an outpatient basis is well established (Table IV). It should be used as the first procedure in the

Fig. 1. Follicular pattern (follicular carcinoma). Follicular cells arranged in acinus-like fashion with hyperchromatic nuclei (Papanicolau, X 500). Fig. 2. Hiirthle pattern. Small group of a Hiirthle cell tumor. Eccentric hyperchromatic nuclei with coarsely granular chromatin and granular cytoplasm (Leishmann, X 500). Fig. 3. Papillary pattern (papillary carcinoma). Sheet of cells with nuclear creases (arrow) (hematoxylin-eosin, X 800). Fig. 4. Papillary pattern (papillary carcinoma). Papillary configuration with intranuclear cytoplastic inclusions (isolated) and ground-glass nuclei (hematoxylin-eosin, X 500). Fig. 5. Undifferentiated pattern (undifferentiated carcinoma). Giant cell carcinoma: prominent nucleoli and atypical mitosis (arrow) (hematoxylineosin, x 800). Fig. 6. Undifferentiated carcinoma (giant cell carcinoma). Giant pleomorphic nuclei hyperchromatic with coarse chromatin and large nucleoli (arrow) (hematoxylin-eosin, x 800). Fig. 7. Medullary pattern (medullary carcinoma). Solid sheet of oval (sometimes polygonal or spindle) cells dispersed in homogeneous eosiriophilic amyloid (arrow) (hematoxylin-eosin, x 600). Fig. 8. Inflammatory pattern (Hashimoto's disease). Lymphocytic characteristic infiltration (hematoxylin-eosin, x 200). Fig. 9. Inflammatory pattern (Hashimoto's disease). Lymphocytic infiltration and large Hiirthle cell (arrow) with characteristic granular cytoplasm and hyperchromatic nuclei (hematoxylin-eosin, x 500).

Diagnostic Cytopathology, Vol 8, No 5



FNAC’s Literature Review (1979-1990)” Inadequacy






(ref. 20) Friedman et al., 1979 (USA) (ref. 5) Chu et al., 1979 (USA) (ref. 4) Colacchio et al., 1980 (USA) (ref. 21) Frable and Frable, 1980 (USA) (ref. 12) Varhaug et al., 1981 (Norway) (ref. I ) Schwartz et al., 1982 (USA) (ref. 2) Belanger et al., 1983 (Canada) (ref. 22) Rubenfeld et al., 1982 (USA) (ref. 23) Block et al., 1983 (USA) (ref. 24) Suen and Quenville 1983 (USA) (ref. 25) Brauer and Silver 1984 (USA) (ref. 26) Christensen et al., 1984 (Sweden) (ref. 27) Riestra et al., 1986 (Puerto Rico) (ref. 3) Bugis et al., 1986 (Canada) (ref. 28) Hsu and Boey, 1987 (Hong Kong) (ref. 29) Pandit and Kinare 1986 (India) (ref. 30) Andreoli et al., 1986 (Italy) (ref. 31) Squartini and Coscio 1986 (Italy) (ref. 32) Frable, 1986 (USA) (ref. 33) Silverman et al., 1986 (USA) (ref. 34) Goellner et al., 1987 (USA) (ref. 35) Hall et al., 1989 (USA) (ref. 13) Glinoer et al., 1987 (Belgium) (ref. 36) Gabrielli et al., 1989 (Italy) (ref. 37) Altavilla et al., 1990 (Italy) (ref. 92) Jones et al. 1990 (United Kingdom) Present series (Brazil)

265 109 300 I68 2 64 102 63 156 I21 304 224

8 0 0 6.5 16.3 9.8 9.0 5.0 16.5 5.0 0



43 I98 555 84 3,038 3,023 9 60 309 6,346 795 600 I39 2,433 175 1,925

99 96 97 96

95 90 2 86 99 98 98 97 96 84 90 94 9x 97 98 98 94 98 90 90 85 6 95.09 93.5 97.2

0 3.0 2.2 4.7 7 25.2 8 0 20 16.5 5 0 16.11 14 8.7

Rate (%) Fake negative positive

(n (n (n (n (n (n

(n = I ) (n = 2) (n = 4) (n = 2) 0 3.3 (n = 3) 1.6 (11 = 1) 0 0.9 (n = 1) 1.9 (n = 6) 0.7 (n = I ) 0 14 (n = 6) 1.5 (n = 3) 0.6 (n = 3) 0 0 0 0.8 ( n = 7 ) 0 0.3 (n = 1) 0.4 (n = 3) 5 (n = 7) 7.5 (n = 11) 0 8 (n = I ) 0

0.4 1.8 1.0 2.4 4.1 6.5 12.7 0.64 1.9 0.6 7.0 1.1 2.3 8.6 4.6 1.2 3.6 1.4 1.1

2.4 1.3 2.0 6.4 28.7 8 0.3


= 1)

2) = 3) = 4) = 9) = 6) = 8) =

(11 =


2) (n = 2) (n = 3) (n = 1) (n = 1) (n = 17) (n = 24) (n = I ) (n = 5) (n = 3) (n-11) 0 (n = 8) (n = I ) (n = 3) (n = 9) (n = 8) (n = 1) (n = 7) (11 =

0.4 1.8 1.3 1.2

Sensitivity (%)


98 92 86 95 74 45 92 98 70 97 88 80 93 43 81 89 83 94 92

99 97 98 97


98 89 77 88.7 71.4 92 95



96 84 100

98 98 99 I00 79 93 99 100

I00 100 99 100

99 88 93 81.3 100

85 I00

“In the works that have no statistical index, we calculated it based on data mentioned by the authors








48 HS




Fig. 10. Flowchart

evaluation of the nodule. We believe that FNAC of the thyroid is a useful examination that provides essential information to the clinician. The use of immunoperoxidase techniques 72-75 and other information obtained


Diagnostic Cytopathology, Vol 8, No 5

through nuclear medicine (uptake of radioisotopes), scintscan, 8 5 and ultrasound could increase the accuracy of the evaluation of thyroid nodules when associated with FNAC. 88-92 (Fig. lo). %zX7


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5 10

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77. 78. 79.








87. 88. 89. 90. 9 1.


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Role of fine-needle aspiration cytology in the management of thyroid nodules: review of experience with 1,925 cases.

Role of Fine-Needle Aspiration Cytology in the Management of Thyroid Nodules: Review of Experience With 1,925 Cases Helio Bisi, M.D., Ph.D., Rosalinda...
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