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Aspiration cytology of head and neck masses
Aspiration Cytology of Head and Neck Masses Joseph E. Russ, MD,* Evanston, Illinois Edward F. Scanlon, MD, Evanston, Illinois Miriam A. Christ, MD, Evanston, Illinois
A perplexing diagnostic and therapeutic dilemma is often presented by masses involving glandular and nodal structures of the head and neck-lymph nodes, thyroid glands, and salivary glands. Formal open surgical biopsy will yield a definitive histopathologic diagnosis but may mandate an extensive operative approach which may be inappropriate for best management. Furthermore, when malignant disease is discovered during an open biopsy, the surgeon may be unprepared or be incapable of proceeding with adequate management. Fine needle aspiration biopsy of such masses is a rapid, direct, and safe adjunctive surgical procedure for obtaining material for cytologic analysis. An intelligent diagnosis and therapeutic rationale thus evolve. Clinical Material and Methods
Between mid-1974 and 1976,213 aspirations of cervical masses were performed at Evanston Hospital, Northwestern University McGaw Medical Center. The cytologic diagnoses as reported were reviewed in all cases and compared with the histologic diagnoses in 109 cases in which corresponding tissue was available. The clinicalrecords of these patients were examined to determine the indications for aspiration and the therapeutic advantages. Technic. Fine needle aspiration biopsy is an established procedure [1-3] which has been modified in our hands [4]. It is usually performed as an outpatient test and requires no special preparation. It is important to emphasize that this procedure yields cellular material for cytologic examination. This is in contradistinction to core needle biopsy, in which tissue for histologic examination is obtained. The patient is placed in the supine position with the neck extended and turned for best exposure of the mass. A shoulder roll is sometimes indicated. A 20 cc disposable From the Divisionof Surgical Oncology and the Cancer Center, Northwestern University Medical School, and the Departments of Surgery and Pathology, Evanston Hospital, Evanston, Illinois. This work was supported in part by the Margaret H. McGrath Memorial Fund. Reprint requests should be addressed to Edward F. Scanlon, MD, Evanston Hospkal. 2650 Ridge Avenue, Evanston, Illinois 60201. *Surgical Oncology Fellow, American Cancer Society
342
plastic Luer-Lock syringe is fitted securely into a Cameco Syringe Pistol (Precision Dynamics Corporation, 3031 Thorton Avenue, Burbank, CA 91504). Depending on the character of the mass, either an 18 or a 23 gauge needle is used. The needle is attached to the syringe and 2 cc of air is aspirated into the barrel. This facilitates expulsion of the specimen at the conclusion of the procedure and obviates the necessity of disconnecting the needle. The skin is prepped with an alcohol swab, and the physician fixes the mass with his free hand. No local anesthesia is required. The patient is cautioned not to swallow. The mass is then entered and full suction easily applied. The needle is manipulated in various directions within the mass, traversing it several times, so that maximal sampling is obtained. Suction is released and the needle withdrawn. The aspirated material is then expelled from the needle onto a glass slide; smears are made using a second slide, as one would make a blood smear. One slide is immediately immersed in Papanicolaou fixative while the other is allowed to airdry. May-Grtinwald-Giemsa and Papanicolaou stains are routinely used. It is important to keep the needle tip below the skin surface while applying negative pressure so as not to aspirate the specimen into the syringe barrel. The procedure should be performed as quickly as possible to limit bloody contamination of the aspirate. If blood is aspirated into the syringe, it should be allowed to clot and sent for histologic examination after Formalin@ fixation. If fluid is obtained from the mass, it should be spun down and the sediment examined cytologically. After decompressing a cystic mass, any residual solid component can be reaspirated with clean equipment. With experience, careful technics, and preparation, adequate specimens can be obtained from favorably located masses as small as 1 cm. Results
Of the 213 aspirations performed, a specimen adequate for cytologic interpretation was obtained in 203 (95 per cent). The tissues examined came from the thyroid, parotid, and submaxillary glands, and cervical and supraclavicular lymph nodes. Table I lists the correlation of the cytologic and histologic diagnoses. The characteristic cytologic features of a
The American Journal of Surgery
Aspiration
TABLE
I
Correlation of Cytologic and Histologic Diagnoses ____ - -_ - ._,__--
Thyroid (85) Sa ivary glands (31) Lyrnph nodes (87) Total (203) ___
__.
of Head and Neck Masses
_~___
Cytologic Diagnosis Benign Malignant Benign Malignant Benign Malignant Benign Malignant
No. of Aspirations 77
a
27 4 39 48 143 60
No. of Biopsies 21 8 13 4 15 48 49 60
Histologic Diagnosis Benign Malignant ._~___ 18 0 11 2 14 2 43 4-__
3 8 2 2
1 46 6 56
colloid nodule, thyroiditis, papillary thyroid carcinoma, Hodgkin’s lymphoma, metastatic squamous cell carcinoma, and mixed tumor of the parotid gland are demonstrated in Figures l-6. Thyroid. Eighty-five thyroid aspiration specimens were diagnosed cytologically: normal follicular epithelium (10); colloid nodule (35); follicular adenoma (15); thyroiditis (17); and carcinoma (8). Seventyseven specimens were diagnosed as benign and eight as malignant. All specimens diagnosed as malignant cytologically were verified histologically, whereas only twenty-one of the benign specimens were examined histologically. The remainder were either thought to be benign clinically, or contraindications to surgery were present. There were three falsenegative diagnoses: an inaccurate sample miss and two erroneous cytologic diagnoses. In two cases, the clinical indications prompted immediate surgical therapy; however, a delay in treatment occurred in the third case because the wrong cytologic diagnosis substantiated the benign clinical impression. The direct correlation of cytologic and histologic diagnoses was 90 per cent. When clinical criteria and cytologic diagnoses were taken together, the accuracy increased to 97 per cent.
Salivary Glands. Cytologic studies of twenty parotid and eleven submaxillary gland tumors were carried out: normal gland (4); inflammation (6); benign mixed tumor (12); Warthin’s tumor (3); carcinoma (4); and miscellaneous (2). Histologic correlation was 76 per cent, in the seventeen t,umors that were biopsied. (Table I.) There were two false-negative and two false-positive diagnoses. In no case did the cytologic results overrule the clinical decision to operate. Neck and Supraclavicular Nodes. Seventy-eight aspiration specimens from nodal masses in the neck and nine from the supraclavicular area were examined cytologically: normal lymph node (4); lymphadenitis (18); cyst (10); lymphoma (9); metastatic carcinoma (39); and miscellaneous (7). Fifty per cent of the neck and all of the supraclavicular aspiration specimens were malignant. The most common indication was lymphadenopathy in patients with known malignant, disease. The upper aerodigestive tract and lung were the major primary sites. (Table II.) A positive cytologic diagnosis obviated the need for
Figure 1. Colloid nodule of fhyroid. Sheet of uniform follicular cells wlfh collokl and foamy hisflocyfes in background. ( Glemsa stain; magnlficaflon X25, reduced 47per cenf.)-
Figure 2. Hashimofo’s fhyroidifis. Loose cluster of oxyphilic cells surrounded by lymphocyfes and plasma cells. ( Glemsa stain; magnificafion X40, reduced 50 per cenf, )-
Volume 136, September 1976
343
Russ, Scanlon, and Christ
Figure 3. Papillary carcinoma of thyroid. Several pap/Mary groups of pleomorphic cells with psammoma bodies. ( Glemsa &a/n; magnification X25, reduced 54 percent.)-
open biopsy in twenty-three patients with metastatic carcinoma. One supraclavicular and eight neck specimens were interpreted as lymphoma: five Hodgkin’s disease and four non-Hodgkin’s lymphoma. All of these lymph nodes were subsequently biopsied, and the diagnosis was confirmed histologically in seven. Reactive hyperplasia was interpreted as lymphoma in two instances. The only false-negative result occurred in a large hemorrhagic node containing metastatic thyroid carcinoma and thought clinically to be a branchial cleft cyst. A microscopic primary in the thyroid was found. The diagnostic accuracy of cytology in evaluating nodal masses of the neck and supraclavicular areas was 95 per cent. Comments
Figure 4. Hodgkin’s disease of cervical lymph node. Reed-Sternberg cells of lacunar type surrounded by lymphocytes. (Giemsa stain; magnification X40, reduced 54 per cent. )
Although the technic of aspiration biopsy has been in existence for half a century, its general use in this country is being enhanced by the increasing experience and sophistication of cytopathologists. More than 90 per cent accuracy can be achieved and specific tumor diagnoses can usually be made. The present report outlines the clinical applicability of this procedure as an adjunct in evaluating cervical masses involving the thyroid and salivary glands and lymph nodes. Although the cytologic-histologic correlation in this series was 91 per cent, only one patient had surgery delayed because of a false-negative diagnosis. Follow-up for up to two years of those patients with benign cytologic diagnoses who did not have subsequent biopsies and histologic confirmation disclosed no other patient who had cancer. The clinical indications for surgery must not be altered when the cytologic result is in disagreement.
Figure 5. Squamous cell carcinoma metastatic to cervical lymph node. Numerous keratinized squamous cells and acute inflammatory cells. (Papanicolaou stain; magntftcation X 10, reduced 54 per cent. )
Figure 6. Mixed tumor of parotid gland. Groups of epithelial cells and fibrillar myxoid stroma. (Papanicolaou stain; magnlficatlon X 10, reduced 54 per cent. )
344
The American Journal of Surgery
Aspiration of Head and Neck Masses
The procedure has not been a difficult one to master. Certainly an awareness of the cervical anatomy is necessary. It is imperative that the pathologist be knowledgeable in surgical pathology so that he may better interpret the cytologic specimens. There were no significant complications in this series, although an occasional minor ecchymosis was noted. Proper positioning of the patient, careful aspiration, and meticulous specimen handling will ensure maximum diagnostic potential. Favorably located nodules as small as 1 cm have been aspirated. Only 5 per cent of the aspiration specimens could not be interpreted by the pathologist. If hemorrhagic, necrotic, or inadequate material is obtained, reaspiration or open biopsy is required. Skepticism of the value of aspiration cytology has been raised because of the rate of false-negative diagnoses. Of the sixty-one malignant histologic diagnoses in this series, six (10 per cent) were falsenegative. This is compatible with the experience of others [5-71. Most often this reflects sampling error as well as the hesitancy of the pathologist to diagnose malignancy without unquestionable cytologic criteria. This fact again emphasizes the necessity of surgical biopsy when clinical grounds suggest malignancy. Two of the six aspiration specimens with falsenegative diagnoses were obtained from the parotid gland. Zajicek and Eneroth [7] summarized their experience with 100 consecutive salivary gland carcinomas. Cytologic accuracy was approximately 70 per cent, reflectzing the difficulty in interpreting salivary gland disease. When dealing with salivary gland tumors, the decision to operate should not be based on cytologic results; however, for those patients with positive cytologic results, a more knowledgeable treatment program can be established. The efficacy of preoperative radiation can be assessed. Both the surgeon and the patient can be adequately prepared should sacrifice of the facial nerve or radical neck dissection be required. In some cases, the clinical differentiation between a small parotid tumor and an intraparotid hyperplastic lymph node can be very difficult, and aspiration biopsy can be quite helpful. In some patients with a cytologic diagnosis of Warthin’s tumor, surgery has not been done and the patients have been followed clinically without adverse effect. The greatest cytologic accuracy was found in cervical and supraclavicular nodes which accounted for the largest number of aspirations. There was a 95 per cen.t histologic correlation, and of the forty-seven malignant diagnoses, only one false-negative diagnosis (2 per cent) occurred. This high degree of ac-
Volume 136, September 1976
TABLE II
Primary Sltes of Metastatic
Neck Nodes Epidermoid head and neck Lung Breast Thyroid Melanoma Carcinoid Sarcoma Supraclavlcular Nodes Lung Breast Kidnev
Adenopathy
17 5 2 3
1 1 2 5 2 1
curacy for lymph node aspirations is common [5,6]. The presence of metastatic squamous cell carcinoma in an enlarged lymph node can almost always be verified by an adequate cytologic aspiration. When the nodal aspiration demonstrates metastatic disease, the need for surgical biopsy is often unnecessary. Furthermore, aspiration biopsy is an important step in the initial evaluation of the cervical node of an unknown primary tumor. Aspiration biopsy allows acceptable evaluation of nodal disease without subjecting the patient to possible surgical morbidity or tumor fungation. Lymphomas diagnosed by cytologic aspiration must always be surgically biopsied since it is impossible to identify the specific histologic type by cytologic study. It is, however, occasionally possible to differentiate Hodgkin’s disease from non-Hodgkin’s lymphoma. Furthermore, the cytologically benign diagnosis of clinically benign adenopathy allows for a more relaxed observation period. In the present study, more than 90 per cent of the thyroid aspirations were performed to verify the benign nature of clinically benign thyroid nodules. Radionuclide scans alone are of limited value as a basis for a treatment plan. The expectant approach of thyroid suppression as currently practiced does not seem acceptable when a cytologic diagnosis can be made on the patient’s initial visit. Concrete grounds for management can thereby be established. Patients with unsuspected malignant disease are referred for earlier surgery, whereas patients with benign disease are not operated on unnecessarily if their nodules do not completely regress with suppression. Only 27 per cent of patients with benign aspiration specimens underwent surgery in this series, and many of these had a history of previous irradiation which prompted surgery on that basis alone. The cytologic diagnosis of follicular adenoma must be verified surgically
345
Russ, Scanlon, and Christ
because of the inability of the cytopathologist to rule out well differentiated carcinoma. Combining thyroid aspiration cytology with scans and ultrasonography can further improve the diagnostic accuracy in assessing and treating thyroid nodules [8,9]. In an occasional case, thyroid carcinoma has been diagnosed from cytologic study of lymph node aspirations when the primary tumor was not suspected clinically. Fears of tumor implantation along the needle tract have been overrated, and reports of this occurring have been anecdotal. Engzell et al [IO] reviewed seven reports describing eight patients in whom tumor spread along a core needle tract was noted. Their survey of the literature, however, disclosed no reports of this occurring with thin needle aspiration biopsy. In their investigations of lymph node metastases in rabbits, they found no tumor cells in the efferent blood or lymph after thin needle aspiration. However, when the nodes were massaged, tumor cells were found in two experiments. Berg and Robbins [11] found no differences in long-term survival rates in breast cancer patients whose tumors had been aspirated versus controls whose tumors were not aspirated. Martin and Ellis [1,2] in their original series of more than 1,400 aspirations did not observe any dissemination clinically. It seems reasonable that should any implantation occur, subsequent oncologic therapy would be sufficient in controlling these cells as well. This is much more acceptable than violating
BENIGN CLINICAI,LY
(ALL INADEQUATE, HEMORRHAGIC, NECROTIC ASPIRATIONS SHOULD NE FURTHER EVALUATED)
346
normal tissue to obtain diagnostic material as is done in open biopsies. Conclusions
Fine needle aspiration biopsy and cytologic examination of head and neck masses is indicated in the following situations: (1) to verify the benign nature of a clinically benign mass that is to be followed; (2) to prompt earlier surgery for a clinically benign mass with malignant or atypical cytology; (3) to obtain a pathologic diagnosis of a suspicious mass to guide further diagnostic evaluation and treatment; (4) to confirm metastases of known malignant disease; (5) to follow treated malignant disease with a suspected recurrence; and (6) to allow a planned therapeutic approach to malignant disease. A flow diagram demonstrating the role of aspiration cytology in treatment decisions is outlined in Figure 7. We have’come to view aspiration cytology as an extension of physical diagnosis. Not only can it be easily performed with no significant morbidity on an outpatient basis, but it can give immediate definitive information which can be utilized in determining the direction of further evaluation and
MALIGNANT CLIN1CALL.Y
Figure 7. Role of aspiration cytology in evaluation and treatment.
The American Journal of Surgery
Aspiration of Head and Neck Masses
The patient’s approach is excellent. therapy.
acceptance
of such a positive
Summary
Fine needle aspiration biopsy and cytologic examination of the aspirate were performed on 203 masses involving glandular and nodal structures of the head and neck: thyroid gland (85); salivary glands (31); and lymph nodes (87). Overall cytologic-histologic correlation was 91 per cent, with a 10 per cent false-negative rate. The ease of the procedure coupled with the rapidity of obtaining a pathologic diagnosis allows a more intelligent therapeutic approach. References 1. Martin HE, Ellis EB: Biopsy by needle puncture and aspiration. Ann Surg 92: 169, 1930. 2. Martin HE, Ellis EB: Aspiration biopsy. Surg Gynecol Obstet 59:
Volume 136, September
1976
578, 1934. 3. Stewart FW: The diagnosis of tumors by aspiration. Am J Pat/w/ 9: 601, 1933. 4. Russ JE, Winchester DP, Scanlon EF, Christ MA: Cytologic findings of aspiration of tumors of the breast. Surg Gynecol Obstet 146: 407, 1976. 5. Hajdu SI. Melamed MR: The diagnostic value of aspiration smears. Am J C/in Path01 59: 350, 1973. 6. Frable WJ: Thin-needle aspiration biopsy. Am J C/in Pathol65: 166, 1975. 7. Zajicek J, Eneroth CM: Cytological diagnosis of salivary gland carcinomata from aspiration biopsy smears. Acta Otolaryngo1263: 183, 1970. 8. Einhorn J, Franzen S: Thin-needle biopsy in the diagnosis of thyroid disease. Acta Radio/ 58: 321, 1962. 9. Walfish PG, Strawbridge HTG, Miskin M, Rosen IB: Evaluation of combined ultrasonography and needle aspiration biopsy in the assessment of the hypofunctioning thyroid nodule. Presented at the Combined Meeting of the Society of Head and Neck Surgeons and the Society of Surgical Oncology, Hilton Head Island, South Carolina, May 4-7, 1977. 10. Engzell U, Esposti PL, Rubio C, et al: Investigation on tumour spread in connection with aspiration biopsy. Acta Radio/ 10: 385,197l. 11. Berg JW, Robbins GF: A late look at the safety of aspiration biopsy. Cancer 15: 662, 1962.
347
A perplexing diagnostic and therapeutic dilemma is often presented by masses involving glandular and nodal structures of the head and neck-lymph nodes, thyroid glands, and salivary glands. Formal open surgical biopsy will yield a definitive histopathologic diagnosis but may mandate an extensive operative approach which may be inappropriate for best management. Furthermore, when malignant disease is discovered during an open biopsy, the surgeon may be unprepared or be incapable of proceeding with adequate management. Fine needle aspiration biopsy of such masses is a rapid, direct, and safe adjunctive surgical procedure for obtaining material for cytologic analysis. An intelligent diagnosis and therapeutic rationale thus evolve. Clinical Material and Methods
Between mid-1974 and 1976,213 aspirations of cervical masses were performed at Evanston Hospital, Northwestern University McGaw Medical Center. The cytologic diagnoses as reported were reviewed in all cases and compared with the histologic diagnoses in 109 cases in which corresponding tissue was available. The clinicalrecords of these patients were examined to determine the indications for aspiration and the therapeutic advantages. Technic. Fine needle aspiration biopsy is an established procedure [1-3] which has been modified in our hands [4]. It is usually performed as an outpatient test and requires no special preparation. It is important to emphasize that this procedure yields cellular material for cytologic examination. This is in contradistinction to core needle biopsy, in which tissue for histologic examination is obtained. The patient is placed in the supine position with the neck extended and turned for best exposure of the mass. A shoulder roll is sometimes indicated. A 20 cc disposable From the Divisionof Surgical Oncology and the Cancer Center, Northwestern University Medical School, and the Departments of Surgery and Pathology, Evanston Hospital, Evanston, Illinois. This work was supported in part by the Margaret H. McGrath Memorial Fund. Reprint requests should be addressed to Edward F. Scanlon, MD, Evanston Hospkal. 2650 Ridge Avenue, Evanston, Illinois 60201. *Surgical Oncology Fellow, American Cancer Society
342
plastic Luer-Lock syringe is fitted securely into a Cameco Syringe Pistol (Precision Dynamics Corporation, 3031 Thorton Avenue, Burbank, CA 91504). Depending on the character of the mass, either an 18 or a 23 gauge needle is used. The needle is attached to the syringe and 2 cc of air is aspirated into the barrel. This facilitates expulsion of the specimen at the conclusion of the procedure and obviates the necessity of disconnecting the needle. The skin is prepped with an alcohol swab, and the physician fixes the mass with his free hand. No local anesthesia is required. The patient is cautioned not to swallow. The mass is then entered and full suction easily applied. The needle is manipulated in various directions within the mass, traversing it several times, so that maximal sampling is obtained. Suction is released and the needle withdrawn. The aspirated material is then expelled from the needle onto a glass slide; smears are made using a second slide, as one would make a blood smear. One slide is immediately immersed in Papanicolaou fixative while the other is allowed to airdry. May-Grtinwald-Giemsa and Papanicolaou stains are routinely used. It is important to keep the needle tip below the skin surface while applying negative pressure so as not to aspirate the specimen into the syringe barrel. The procedure should be performed as quickly as possible to limit bloody contamination of the aspirate. If blood is aspirated into the syringe, it should be allowed to clot and sent for histologic examination after Formalin@ fixation. If fluid is obtained from the mass, it should be spun down and the sediment examined cytologically. After decompressing a cystic mass, any residual solid component can be reaspirated with clean equipment. With experience, careful technics, and preparation, adequate specimens can be obtained from favorably located masses as small as 1 cm. Results
Of the 213 aspirations performed, a specimen adequate for cytologic interpretation was obtained in 203 (95 per cent). The tissues examined came from the thyroid, parotid, and submaxillary glands, and cervical and supraclavicular lymph nodes. Table I lists the correlation of the cytologic and histologic diagnoses. The characteristic cytologic features of a
The American Journal of Surgery
Aspiration
TABLE
I
Correlation of Cytologic and Histologic Diagnoses ____ - -_ - ._,__--
Thyroid (85) Sa ivary glands (31) Lyrnph nodes (87) Total (203) ___
__.
of Head and Neck Masses
_~___
Cytologic Diagnosis Benign Malignant Benign Malignant Benign Malignant Benign Malignant
No. of Aspirations 77
a
27 4 39 48 143 60
No. of Biopsies 21 8 13 4 15 48 49 60
Histologic Diagnosis Benign Malignant ._~___ 18 0 11 2 14 2 43 4-__
3 8 2 2
1 46 6 56
colloid nodule, thyroiditis, papillary thyroid carcinoma, Hodgkin’s lymphoma, metastatic squamous cell carcinoma, and mixed tumor of the parotid gland are demonstrated in Figures l-6. Thyroid. Eighty-five thyroid aspiration specimens were diagnosed cytologically: normal follicular epithelium (10); colloid nodule (35); follicular adenoma (15); thyroiditis (17); and carcinoma (8). Seventyseven specimens were diagnosed as benign and eight as malignant. All specimens diagnosed as malignant cytologically were verified histologically, whereas only twenty-one of the benign specimens were examined histologically. The remainder were either thought to be benign clinically, or contraindications to surgery were present. There were three falsenegative diagnoses: an inaccurate sample miss and two erroneous cytologic diagnoses. In two cases, the clinical indications prompted immediate surgical therapy; however, a delay in treatment occurred in the third case because the wrong cytologic diagnosis substantiated the benign clinical impression. The direct correlation of cytologic and histologic diagnoses was 90 per cent. When clinical criteria and cytologic diagnoses were taken together, the accuracy increased to 97 per cent.
Salivary Glands. Cytologic studies of twenty parotid and eleven submaxillary gland tumors were carried out: normal gland (4); inflammation (6); benign mixed tumor (12); Warthin’s tumor (3); carcinoma (4); and miscellaneous (2). Histologic correlation was 76 per cent, in the seventeen t,umors that were biopsied. (Table I.) There were two false-negative and two false-positive diagnoses. In no case did the cytologic results overrule the clinical decision to operate. Neck and Supraclavicular Nodes. Seventy-eight aspiration specimens from nodal masses in the neck and nine from the supraclavicular area were examined cytologically: normal lymph node (4); lymphadenitis (18); cyst (10); lymphoma (9); metastatic carcinoma (39); and miscellaneous (7). Fifty per cent of the neck and all of the supraclavicular aspiration specimens were malignant. The most common indication was lymphadenopathy in patients with known malignant, disease. The upper aerodigestive tract and lung were the major primary sites. (Table II.) A positive cytologic diagnosis obviated the need for
Figure 1. Colloid nodule of fhyroid. Sheet of uniform follicular cells wlfh collokl and foamy hisflocyfes in background. ( Glemsa stain; magnlficaflon X25, reduced 47per cenf.)-
Figure 2. Hashimofo’s fhyroidifis. Loose cluster of oxyphilic cells surrounded by lymphocyfes and plasma cells. ( Glemsa stain; magnificafion X40, reduced 50 per cenf, )-
Volume 136, September 1976
343
Russ, Scanlon, and Christ
Figure 3. Papillary carcinoma of thyroid. Several pap/Mary groups of pleomorphic cells with psammoma bodies. ( Glemsa &a/n; magnification X25, reduced 54 percent.)-
open biopsy in twenty-three patients with metastatic carcinoma. One supraclavicular and eight neck specimens were interpreted as lymphoma: five Hodgkin’s disease and four non-Hodgkin’s lymphoma. All of these lymph nodes were subsequently biopsied, and the diagnosis was confirmed histologically in seven. Reactive hyperplasia was interpreted as lymphoma in two instances. The only false-negative result occurred in a large hemorrhagic node containing metastatic thyroid carcinoma and thought clinically to be a branchial cleft cyst. A microscopic primary in the thyroid was found. The diagnostic accuracy of cytology in evaluating nodal masses of the neck and supraclavicular areas was 95 per cent. Comments
Figure 4. Hodgkin’s disease of cervical lymph node. Reed-Sternberg cells of lacunar type surrounded by lymphocytes. (Giemsa stain; magnification X40, reduced 54 per cent. )
Although the technic of aspiration biopsy has been in existence for half a century, its general use in this country is being enhanced by the increasing experience and sophistication of cytopathologists. More than 90 per cent accuracy can be achieved and specific tumor diagnoses can usually be made. The present report outlines the clinical applicability of this procedure as an adjunct in evaluating cervical masses involving the thyroid and salivary glands and lymph nodes. Although the cytologic-histologic correlation in this series was 91 per cent, only one patient had surgery delayed because of a false-negative diagnosis. Follow-up for up to two years of those patients with benign cytologic diagnoses who did not have subsequent biopsies and histologic confirmation disclosed no other patient who had cancer. The clinical indications for surgery must not be altered when the cytologic result is in disagreement.
Figure 5. Squamous cell carcinoma metastatic to cervical lymph node. Numerous keratinized squamous cells and acute inflammatory cells. (Papanicolaou stain; magntftcation X 10, reduced 54 per cent. )
Figure 6. Mixed tumor of parotid gland. Groups of epithelial cells and fibrillar myxoid stroma. (Papanicolaou stain; magnlficatlon X 10, reduced 54 per cent. )
344
The American Journal of Surgery
Aspiration of Head and Neck Masses
The procedure has not been a difficult one to master. Certainly an awareness of the cervical anatomy is necessary. It is imperative that the pathologist be knowledgeable in surgical pathology so that he may better interpret the cytologic specimens. There were no significant complications in this series, although an occasional minor ecchymosis was noted. Proper positioning of the patient, careful aspiration, and meticulous specimen handling will ensure maximum diagnostic potential. Favorably located nodules as small as 1 cm have been aspirated. Only 5 per cent of the aspiration specimens could not be interpreted by the pathologist. If hemorrhagic, necrotic, or inadequate material is obtained, reaspiration or open biopsy is required. Skepticism of the value of aspiration cytology has been raised because of the rate of false-negative diagnoses. Of the sixty-one malignant histologic diagnoses in this series, six (10 per cent) were falsenegative. This is compatible with the experience of others [5-71. Most often this reflects sampling error as well as the hesitancy of the pathologist to diagnose malignancy without unquestionable cytologic criteria. This fact again emphasizes the necessity of surgical biopsy when clinical grounds suggest malignancy. Two of the six aspiration specimens with falsenegative diagnoses were obtained from the parotid gland. Zajicek and Eneroth [7] summarized their experience with 100 consecutive salivary gland carcinomas. Cytologic accuracy was approximately 70 per cent, reflectzing the difficulty in interpreting salivary gland disease. When dealing with salivary gland tumors, the decision to operate should not be based on cytologic results; however, for those patients with positive cytologic results, a more knowledgeable treatment program can be established. The efficacy of preoperative radiation can be assessed. Both the surgeon and the patient can be adequately prepared should sacrifice of the facial nerve or radical neck dissection be required. In some cases, the clinical differentiation between a small parotid tumor and an intraparotid hyperplastic lymph node can be very difficult, and aspiration biopsy can be quite helpful. In some patients with a cytologic diagnosis of Warthin’s tumor, surgery has not been done and the patients have been followed clinically without adverse effect. The greatest cytologic accuracy was found in cervical and supraclavicular nodes which accounted for the largest number of aspirations. There was a 95 per cen.t histologic correlation, and of the forty-seven malignant diagnoses, only one false-negative diagnosis (2 per cent) occurred. This high degree of ac-
Volume 136, September 1976
TABLE II
Primary Sltes of Metastatic
Neck Nodes Epidermoid head and neck Lung Breast Thyroid Melanoma Carcinoid Sarcoma Supraclavlcular Nodes Lung Breast Kidnev
Adenopathy
17 5 2 3
1 1 2 5 2 1
curacy for lymph node aspirations is common [5,6]. The presence of metastatic squamous cell carcinoma in an enlarged lymph node can almost always be verified by an adequate cytologic aspiration. When the nodal aspiration demonstrates metastatic disease, the need for surgical biopsy is often unnecessary. Furthermore, aspiration biopsy is an important step in the initial evaluation of the cervical node of an unknown primary tumor. Aspiration biopsy allows acceptable evaluation of nodal disease without subjecting the patient to possible surgical morbidity or tumor fungation. Lymphomas diagnosed by cytologic aspiration must always be surgically biopsied since it is impossible to identify the specific histologic type by cytologic study. It is, however, occasionally possible to differentiate Hodgkin’s disease from non-Hodgkin’s lymphoma. Furthermore, the cytologically benign diagnosis of clinically benign adenopathy allows for a more relaxed observation period. In the present study, more than 90 per cent of the thyroid aspirations were performed to verify the benign nature of clinically benign thyroid nodules. Radionuclide scans alone are of limited value as a basis for a treatment plan. The expectant approach of thyroid suppression as currently practiced does not seem acceptable when a cytologic diagnosis can be made on the patient’s initial visit. Concrete grounds for management can thereby be established. Patients with unsuspected malignant disease are referred for earlier surgery, whereas patients with benign disease are not operated on unnecessarily if their nodules do not completely regress with suppression. Only 27 per cent of patients with benign aspiration specimens underwent surgery in this series, and many of these had a history of previous irradiation which prompted surgery on that basis alone. The cytologic diagnosis of follicular adenoma must be verified surgically
345
Russ, Scanlon, and Christ
because of the inability of the cytopathologist to rule out well differentiated carcinoma. Combining thyroid aspiration cytology with scans and ultrasonography can further improve the diagnostic accuracy in assessing and treating thyroid nodules [8,9]. In an occasional case, thyroid carcinoma has been diagnosed from cytologic study of lymph node aspirations when the primary tumor was not suspected clinically. Fears of tumor implantation along the needle tract have been overrated, and reports of this occurring have been anecdotal. Engzell et al [IO] reviewed seven reports describing eight patients in whom tumor spread along a core needle tract was noted. Their survey of the literature, however, disclosed no reports of this occurring with thin needle aspiration biopsy. In their investigations of lymph node metastases in rabbits, they found no tumor cells in the efferent blood or lymph after thin needle aspiration. However, when the nodes were massaged, tumor cells were found in two experiments. Berg and Robbins [11] found no differences in long-term survival rates in breast cancer patients whose tumors had been aspirated versus controls whose tumors were not aspirated. Martin and Ellis [1,2] in their original series of more than 1,400 aspirations did not observe any dissemination clinically. It seems reasonable that should any implantation occur, subsequent oncologic therapy would be sufficient in controlling these cells as well. This is much more acceptable than violating
BENIGN CLINICAI,LY
(ALL INADEQUATE, HEMORRHAGIC, NECROTIC ASPIRATIONS SHOULD NE FURTHER EVALUATED)
346
normal tissue to obtain diagnostic material as is done in open biopsies. Conclusions
Fine needle aspiration biopsy and cytologic examination of head and neck masses is indicated in the following situations: (1) to verify the benign nature of a clinically benign mass that is to be followed; (2) to prompt earlier surgery for a clinically benign mass with malignant or atypical cytology; (3) to obtain a pathologic diagnosis of a suspicious mass to guide further diagnostic evaluation and treatment; (4) to confirm metastases of known malignant disease; (5) to follow treated malignant disease with a suspected recurrence; and (6) to allow a planned therapeutic approach to malignant disease. A flow diagram demonstrating the role of aspiration cytology in treatment decisions is outlined in Figure 7. We have’come to view aspiration cytology as an extension of physical diagnosis. Not only can it be easily performed with no significant morbidity on an outpatient basis, but it can give immediate definitive information which can be utilized in determining the direction of further evaluation and
MALIGNANT CLIN1CALL.Y
Figure 7. Role of aspiration cytology in evaluation and treatment.
The American Journal of Surgery
Aspiration of Head and Neck Masses
The patient’s approach is excellent. therapy.
acceptance
of such a positive
Summary
Fine needle aspiration biopsy and cytologic examination of the aspirate were performed on 203 masses involving glandular and nodal structures of the head and neck: thyroid gland (85); salivary glands (31); and lymph nodes (87). Overall cytologic-histologic correlation was 91 per cent, with a 10 per cent false-negative rate. The ease of the procedure coupled with the rapidity of obtaining a pathologic diagnosis allows a more intelligent therapeutic approach. References 1. Martin HE, Ellis EB: Biopsy by needle puncture and aspiration. Ann Surg 92: 169, 1930. 2. Martin HE, Ellis EB: Aspiration biopsy. Surg Gynecol Obstet 59:
Volume 136, September
1976
578, 1934. 3. Stewart FW: The diagnosis of tumors by aspiration. Am J Pat/w/ 9: 601, 1933. 4. Russ JE, Winchester DP, Scanlon EF, Christ MA: Cytologic findings of aspiration of tumors of the breast. Surg Gynecol Obstet 146: 407, 1976. 5. Hajdu SI. Melamed MR: The diagnostic value of aspiration smears. Am J C/in Path01 59: 350, 1973. 6. Frable WJ: Thin-needle aspiration biopsy. Am J C/in Pathol65: 166, 1975. 7. Zajicek J, Eneroth CM: Cytological diagnosis of salivary gland carcinomata from aspiration biopsy smears. Acta Otolaryngo1263: 183, 1970. 8. Einhorn J, Franzen S: Thin-needle biopsy in the diagnosis of thyroid disease. Acta Radio/ 58: 321, 1962. 9. Walfish PG, Strawbridge HTG, Miskin M, Rosen IB: Evaluation of combined ultrasonography and needle aspiration biopsy in the assessment of the hypofunctioning thyroid nodule. Presented at the Combined Meeting of the Society of Head and Neck Surgeons and the Society of Surgical Oncology, Hilton Head Island, South Carolina, May 4-7, 1977. 10. Engzell U, Esposti PL, Rubio C, et al: Investigation on tumour spread in connection with aspiration biopsy. Acta Radio/ 10: 385,197l. 11. Berg JW, Robbins GF: A late look at the safety of aspiration biopsy. Cancer 15: 662, 1962.
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