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Tall cell papillary thyroid cancer: Incidence and prognosis
Tall Cell Papillary Thyroid Cancer: Incidence and Prognosis James H. Terry, MD, Susan A. St. John, MD, Brooklyn, New York, Frederick J. Karkowski, MD, New York, New York, Jorge R. Suarez, MD, Brooklyn, New York, Naguib H. Yassa, MD, New York, New York, Corneliu D. Platica, MD, Jose R. Marti, MD, Brooklyn, New York
BACKGROUND: T h e tall cell variant (TCV) o f papillary thyroid c a n c e r is reported to h a v e a p o o r prognosis. This study e x a m i n e s the incidence and end result o f surgical treatment o f TCV. METHODS: In this study, 2 4 0 thyroid c a n c e r s treated o v e r a 2 3 - y e a r period at two hospital centers are reviewed. A total o f 1 5 3 patients with papillary c a n c e r w e r e available for f o n o w up. All m i c r o s c o p i c slides w e r e r e - e x m n i n e d . RESULTS: O f t h e total 1 8 3 papillary c a n c e r s , 1 9 ( 1 0 . 4 % ) w e r e TCV. T h e r e m a i n d e r w e r e usual papillary o r o t h e r papillary c a n c e r variants. Patient age, t u m o r size, l y m p h n o d e and soft-tissue i n v o l v e m e n t , r e c u r r e n c e , and d e a t h rates w e r e evaluated. Multivariate statistical analysis disclosed that TCV histology, as well as age and t u m o r size, w e r e significant p r e d i c t o r s of recurrence. CONCLUSION: Despite a high rate o f r e c u r r e n c e in TCV cases o v e r age 5 0 (6/9), there were n o recurrent TCVs in cases under age 5 0 (0/8). Pathologists and surgeons must develop an increased awareneuss o f this entity and implications for m o r e radical treatment in the older age group.
The criteria for the diagnosis of TCV were: (1) ceils twice as tall as they were wide, (2) eosinophilie cytoplasm, and (3) hyperchromatic basilar nuclei and prominent papillary pattern (Figure). At least 30% of the specimen had to fulfill these criteria for it to be called TCV. 9,1° The TCV and other papillary carcinomas (OPC) groups were then compared for: (1) age of onset, (2) sex of patient, (3) size of tumor, and (4) presence of nodal metastases and/or local soft-tissue invasion. All patients whose charts were reviewed were contacted by the authors, either directly or through their own physicians, to ascertain their status with regard to recurrences, presence of residual disease, and time and cause of death. The TCV group was then compared to the OPC group with regard to these parameters. Using the chi-square method, P values were obtained. A multivariate analysis using multiple logistic regression was used to determine the significance of patient age and tumor size in the recurrence rates for patien)s with TCV and with OPC.
RESULTS Two hundred forty cases of thyroid carcinoma were reviewed, with 183 cases being some variant of papillary carcinoma. There were 19 cases of TCV---only 2 of which he tall cell variant (TCV) of papillary carcinoma of the were recognized as such by pathologists at the time of surgery. The remaining specimens were usual papillary thyroid was first described in April 1967, by Hazard) Since that time, 3 major series of TCV cases have been (118 cases), follicular variant (19 cases), encapsulated (5 reported in the pathology and endocrine literature, the cases), occult (18 cases), and diffuse sclerosing (4 cases). There was no difference in the age of onset between the largest consisting of 18 cases. 2-4 In addition, 4 individual case reports have been published, 5"8 for a grand total of 51 TCV and OPC groups in this series. There was a precases of TCV. In this report, 19 cases of TCV were col- dominance of female patients in both groups, but the lected from the surgical services of two hospital centers in male:female ratio was higher in the TCV group than in the OPC group (1:2 versus 1:4). The sex difference was New York City. not statistically significant. The tumor size at the time of resection was significantly larger in the TCV group verMETHODS The records of 240 cases of surgically treated thyroid sus the OPC group (average diameter, 4.2 versus 2.8 cm; cancers were reviewed. These cases were divided into pap- P <0.05). Within the TCV group, the tumor size was illary and nonpapillary types. The original pathology re- greater in the 50-and-over age group than in the under-50 ports of all papillary cases were reviewed, and over 100 age group (5.6 versus 2.7 cm; P <0.05). There was no significant difference between the TCV and sets of original slides were examined by pathologists who OPC groups with regard to presence of nodal metastases were unaware of the clinical outcome. alone or soft-tissue invasion alone, However, the TCV group had a significantly higher incidence of both characFrom the Departments of Surgery (JilT, SASJ, JRM) and Pathology teristics combined (26.3% [5/19] versus 10.4% [17/164]; (JRS, CDP), The Brooklyn Hospital Center, Brooklyn, and the Depart- P _<0.05). ments of Surgery (FJK) and Pathology(NHY),The St. Luke's Roosevelt Two cases of TCV and 28 cases of OPC were lost to folHospital Center, New York, New York. Request for reprints should be addressed to James H. Terry, MD. low-up. The average follow-up for the remaining TCV Department of Surgery, The Brooklyn Hospital Center, 115 East 61st cases was 62.6 months (range 2 to 165) and 93.6 months for the OPC cases (range 2 to 265). Street, New York, New York 10012. Presented at thejoint meetingof the Societyof Headand Neck Surgeons Of the 153 cases available for follow-up, 4 cases were and the European Organization for Research and Treatment of Cancer eliminated from multivariate analysis since tumor size data (EORTC), Pads, France, May 25-28, 1994.
T
THE AMERICANJOURNALOF SURGERY® VOLUME168 NOVEMBER1994 459
TALL CELL PAPILLARY THYROID CANCER/TERRYET AL
Figure. A l O x enlargement of a photomicrograph of a typical tall cell specimen demonstrates tall epithelial cells, basal nuclei, partial clearing of granular cytoplasm, and regular cell alignment about empty spaces (hematoxylin-eosin stain using a 4 0 x lens with l O x objective).
TABLE Results of Multivariate Analysis of Patients Available for Follow-up Size (cm) <4 ~
Age (y)
Cancer Type
% of Recurrence
<50
TCV 0 OPC 2 >50 -----..... TCV 50 OPC 3 >4 ~ <50 TCV 0 OPC 5 " " >50 TCV 80 OPC 14 This table shows the numberand percentageof recurrencesof cancer utilizingfactors of size, age, and cancer type. "Fourof the 153 patientsavailablefor follow-upwere elimiatedfrom multivariateanalysissince tumor size data were not available. TCV = tall cell variant; OPC = other papillarycancers.
were not available. There was a 35.3% (6/17) recurrence rate in the TCV group, as compared to a 3.8% (5/132) recurrence rate for the OPC group (P <0.05). In the TCV group, there was 1 death from disease (5.9%), and 3 patients (17.6%) were alive with disease at the time of this writing. Two other patients were successfully treated for recurrence. In the OPC group, there was 1 death from disease (0.8%) and 2 patients were alive with disease (1.5%). Because of the small number of deaths, those differences are not statistically significant. When sorted by age into a 50-and-over group and an under-50 group, all TCV recurrences were in the 50-and-over group. Those patients 50-and-over who recurred are currently alive with disease or dead of disease compared with the under-50 age group in which all 3 patients treated for recurrence are now disease free. The multivariate analysis of the data (Table) shows that age over 50, tumor size greater than 4 cm, and presence of TCV histology are all independent predictors of recurrence. COMMENTS There are a number of problems that are encountered in a study such as this. Indeed, prior studies could not develop 460
# of Patients" 0/6 1/63 2/4 1/33 0/2 1/22 4/5 2/14
significant statistics by multivariate analysis incriminating the TCV histology as a factor in poor prognosis. 3.4.t~ This study is the first to use multivariate analysis to show that tall cell histology affects the recurrence rate. The other factors used in this analysis (ie, size and age) are known predictors of recurrence, n2 However, Johnson et al 3 used ageand sex-matched pairs of tall cell and usual papillary carcinoma patients. They found a significantly higher incidence of distant metastases, recurrences, and disease-specific mortality in TCV patients as compared to OPC patients. This method was not used in the present study because of possible bias in the selection of pairs. The reason TCV is associated with high recurrence rates is unknown. It has been shown that TCV is associated with high levels of type IV collagenase, n3 which may be a factor, and that DNA-ploidy does not differ between TCV a n d OCP. 14 The presence of higher mitotic rates is controversial ~5 in TCV. The comparatively small number of patients who died of all types of papillary thyroid carcinoma, the long duration of the study (up to 23 years), and the difficulty of followup are all factors that contribute to the problems of statistical analysis. Many surgeons (36) and several different
THE AMERICANJOURNALOF SURGERY® VOLUME 168 NOVEMBER 1994
TALL CELL PAPILLARY THYROID CANCER/TERRYEl' AL types of operations (10) were involved. A significant number of patients died of other causes (8), were lost to follow-up (30), or were omitted from results analysis because of short follow-up. Several of the physicians involved (14) are now deceased, retired, or moved from the area. Other authors 5,6,s,IJ have described the occurence of other types of thyroid cancer with TCV. These include clear and Htirthle cell, columnar cell, anaplastic, spindle cell, squamous, and mucin-producing types. Indeed, three of the present cases exhibited association with other types. One was associated with anaplastic, another with squamous cell, and the third with a mucin-producing carcinoma. CONCLUSIONS AND RECOMMENDATIONS The incidence of TCV of papillary thyroid carcinoma is significant (19/183 [10%]) in this series. This incidence rate compares to the rates of 10% to 12% reported in previous series. While the recurrence rate of TCV cases is significantly higher than in the other types of papillary carcinoma, the higher recurrence rate of TCV is confined to the 50-and-over age group. Tumor size in the TCV versus OPC groups is statistically larger (P =0.05), and within the tall cell group, tumor size is significantly larger in the 50-and-over age group as compared to the under50 age group (P <0.05). Multivariate analysis demonstrates that age-of-50-and-over group, tumor size greater than 4 cm, and TCV histology are all independently valid predictors of recurrence. In light of these results, the authors propose the following recommendations: (1) the pathologist's report should include the type of papillary carcinoma of the thyroid in the diagnosis (ie, usual type, follicular variant, TCV, columnar cell variant, or sclerosing variant [encapsulated or diffuse]); (2) surgeons should be aware that TCV has a poorer prognosis than OPC, especially in patients aged 50 and over who have tumors greater than 4 cm in size; (3) patients in this high-risk group should be considered for more aggressive therapy (ie, more radical surgery and postoperative radioiodine) in the hope of reducing the high recurrence rate; and (4) further study of this material is necessary
in order to follow these patients and to develop efitefia:for type of surgery and/or postoperative radioiodine treatment. REFERENCES 1. Hazard JB. Nomenclature of thyroid tumors. In: Young S, Inman DR, eds. Proceedings of the 2nd Imperial Cancer Research Fund Symposium. New York, NY: Academic Press; 1968. 2. Robbins J, Merino MJ, Boice JD, et al. Thyroid cancer: a lethal endocrine neoplasm. Ann hzt Med. 1991;115:133-147. 3. Johnson TL, Lloyd RV, Thompson NW, et al. Prognostic implications of the tall cell variant of papillary thyroid carcinomas. Am J Surg Pathol. 1988;12:22-27. 4. Hawk WA, Hazard JB. The many appearances of papillary carcinoma of the thyroid. Cleve Clin Q. 1976;45:207-216. 5. Dickersin GR, Vickery AL, Smith SB. Papillary carcinoma of the thyroid oxyphil-cell type, clear cell variant. Am J Surg Pathol. 1980; 4:501-509. 6. Akslen LA, Varhany JE. Thyroid carcinoma with mixed tall cell and columnar cell features. Am J Clin Pathol. 1990;94:442--445. 7. Yao T. FNA cytology of tall cell variant of papillary thyroid carcinoma. Acta Cytol. 1994;38:282-283. 8. Bronner MP, Livolsi VA. Spindle cell squamous carcinoma of the thyroid: an unusual anaplastic tumor associated with tall cell papillary cancer. Modem Pathol. 1991;4(5):637--643. 9. Rosai J, Carcangiu ML, Delellis RA. Tumors of the thyroid gland. In: Atlas of Tumor Pathology. Washington DC: Armed Forces Institute of Pathology; 1992:114-121. 10. Hicks MJ, Batsakis JG. Tall cell carcinoma of the thyroid gland. Ann Otol Rhh~ol Laryngol. 1993;102:402--403. 11. Livolsi V. Papillary neoplasms of the thyroid: pathologic and prognostic features. Am J Clin Pathol. 1992;3:426-434. 12. Shah JP, Loree TR, Dharker D, et al. Prognostic factors in differential carcinoma of the thyroid gland. Am J Surg. 1992; 164: 658-661. 13. Campo E, Merino MJ, Liotta L, et al. Distribution of the 72-kd type 1V collagenase in nonneoplastic and neoplastic thyroid tissue. Hum Pathol. 1992;23:1395-1401. 14. Flint A, Davenport RO, Lloyd RV. The tall cell variant of papillary carcinoma of the thyroid gland: comparison with the common form of papillary carcinoma by DNA and morphometric analysis. Arch Pathol Lab Med. 1991;115:169-171. 15. Sobrinho-Simoes M, Sambada C, Nesland JM. Letter to the editor. Am J Surg Pathol. 1989;13:79-80.
THE AMERICANJOURNALOF SURGERY® VOLUME 168 NOVEMBER1994 4,61
BACKGROUND: T h e tall cell variant (TCV) o f papillary thyroid c a n c e r is reported to h a v e a p o o r prognosis. This study e x a m i n e s the incidence and end result o f surgical treatment o f TCV. METHODS: In this study, 2 4 0 thyroid c a n c e r s treated o v e r a 2 3 - y e a r period at two hospital centers are reviewed. A total o f 1 5 3 patients with papillary c a n c e r w e r e available for f o n o w up. All m i c r o s c o p i c slides w e r e r e - e x m n i n e d . RESULTS: O f t h e total 1 8 3 papillary c a n c e r s , 1 9 ( 1 0 . 4 % ) w e r e TCV. T h e r e m a i n d e r w e r e usual papillary o r o t h e r papillary c a n c e r variants. Patient age, t u m o r size, l y m p h n o d e and soft-tissue i n v o l v e m e n t , r e c u r r e n c e , and d e a t h rates w e r e evaluated. Multivariate statistical analysis disclosed that TCV histology, as well as age and t u m o r size, w e r e significant p r e d i c t o r s of recurrence. CONCLUSION: Despite a high rate o f r e c u r r e n c e in TCV cases o v e r age 5 0 (6/9), there were n o recurrent TCVs in cases under age 5 0 (0/8). Pathologists and surgeons must develop an increased awareneuss o f this entity and implications for m o r e radical treatment in the older age group.
The criteria for the diagnosis of TCV were: (1) ceils twice as tall as they were wide, (2) eosinophilie cytoplasm, and (3) hyperchromatic basilar nuclei and prominent papillary pattern (Figure). At least 30% of the specimen had to fulfill these criteria for it to be called TCV. 9,1° The TCV and other papillary carcinomas (OPC) groups were then compared for: (1) age of onset, (2) sex of patient, (3) size of tumor, and (4) presence of nodal metastases and/or local soft-tissue invasion. All patients whose charts were reviewed were contacted by the authors, either directly or through their own physicians, to ascertain their status with regard to recurrences, presence of residual disease, and time and cause of death. The TCV group was then compared to the OPC group with regard to these parameters. Using the chi-square method, P values were obtained. A multivariate analysis using multiple logistic regression was used to determine the significance of patient age and tumor size in the recurrence rates for patien)s with TCV and with OPC.
RESULTS Two hundred forty cases of thyroid carcinoma were reviewed, with 183 cases being some variant of papillary carcinoma. There were 19 cases of TCV---only 2 of which he tall cell variant (TCV) of papillary carcinoma of the were recognized as such by pathologists at the time of surgery. The remaining specimens were usual papillary thyroid was first described in April 1967, by Hazard) Since that time, 3 major series of TCV cases have been (118 cases), follicular variant (19 cases), encapsulated (5 reported in the pathology and endocrine literature, the cases), occult (18 cases), and diffuse sclerosing (4 cases). There was no difference in the age of onset between the largest consisting of 18 cases. 2-4 In addition, 4 individual case reports have been published, 5"8 for a grand total of 51 TCV and OPC groups in this series. There was a precases of TCV. In this report, 19 cases of TCV were col- dominance of female patients in both groups, but the lected from the surgical services of two hospital centers in male:female ratio was higher in the TCV group than in the OPC group (1:2 versus 1:4). The sex difference was New York City. not statistically significant. The tumor size at the time of resection was significantly larger in the TCV group verMETHODS The records of 240 cases of surgically treated thyroid sus the OPC group (average diameter, 4.2 versus 2.8 cm; cancers were reviewed. These cases were divided into pap- P <0.05). Within the TCV group, the tumor size was illary and nonpapillary types. The original pathology re- greater in the 50-and-over age group than in the under-50 ports of all papillary cases were reviewed, and over 100 age group (5.6 versus 2.7 cm; P <0.05). There was no significant difference between the TCV and sets of original slides were examined by pathologists who OPC groups with regard to presence of nodal metastases were unaware of the clinical outcome. alone or soft-tissue invasion alone, However, the TCV group had a significantly higher incidence of both characFrom the Departments of Surgery (JilT, SASJ, JRM) and Pathology teristics combined (26.3% [5/19] versus 10.4% [17/164]; (JRS, CDP), The Brooklyn Hospital Center, Brooklyn, and the Depart- P _<0.05). ments of Surgery (FJK) and Pathology(NHY),The St. Luke's Roosevelt Two cases of TCV and 28 cases of OPC were lost to folHospital Center, New York, New York. Request for reprints should be addressed to James H. Terry, MD. low-up. The average follow-up for the remaining TCV Department of Surgery, The Brooklyn Hospital Center, 115 East 61st cases was 62.6 months (range 2 to 165) and 93.6 months for the OPC cases (range 2 to 265). Street, New York, New York 10012. Presented at thejoint meetingof the Societyof Headand Neck Surgeons Of the 153 cases available for follow-up, 4 cases were and the European Organization for Research and Treatment of Cancer eliminated from multivariate analysis since tumor size data (EORTC), Pads, France, May 25-28, 1994.
T
THE AMERICANJOURNALOF SURGERY® VOLUME168 NOVEMBER1994 459
TALL CELL PAPILLARY THYROID CANCER/TERRYET AL
Figure. A l O x enlargement of a photomicrograph of a typical tall cell specimen demonstrates tall epithelial cells, basal nuclei, partial clearing of granular cytoplasm, and regular cell alignment about empty spaces (hematoxylin-eosin stain using a 4 0 x lens with l O x objective).
TABLE Results of Multivariate Analysis of Patients Available for Follow-up Size (cm) <4 ~
Age (y)
Cancer Type
% of Recurrence
<50
TCV 0 OPC 2 >50 -----..... TCV 50 OPC 3 >4 ~ <50 TCV 0 OPC 5 " " >50 TCV 80 OPC 14 This table shows the numberand percentageof recurrencesof cancer utilizingfactors of size, age, and cancer type. "Fourof the 153 patientsavailablefor follow-upwere elimiatedfrom multivariateanalysissince tumor size data were not available. TCV = tall cell variant; OPC = other papillarycancers.
were not available. There was a 35.3% (6/17) recurrence rate in the TCV group, as compared to a 3.8% (5/132) recurrence rate for the OPC group (P <0.05). In the TCV group, there was 1 death from disease (5.9%), and 3 patients (17.6%) were alive with disease at the time of this writing. Two other patients were successfully treated for recurrence. In the OPC group, there was 1 death from disease (0.8%) and 2 patients were alive with disease (1.5%). Because of the small number of deaths, those differences are not statistically significant. When sorted by age into a 50-and-over group and an under-50 group, all TCV recurrences were in the 50-and-over group. Those patients 50-and-over who recurred are currently alive with disease or dead of disease compared with the under-50 age group in which all 3 patients treated for recurrence are now disease free. The multivariate analysis of the data (Table) shows that age over 50, tumor size greater than 4 cm, and presence of TCV histology are all independent predictors of recurrence. COMMENTS There are a number of problems that are encountered in a study such as this. Indeed, prior studies could not develop 460
# of Patients" 0/6 1/63 2/4 1/33 0/2 1/22 4/5 2/14
significant statistics by multivariate analysis incriminating the TCV histology as a factor in poor prognosis. 3.4.t~ This study is the first to use multivariate analysis to show that tall cell histology affects the recurrence rate. The other factors used in this analysis (ie, size and age) are known predictors of recurrence, n2 However, Johnson et al 3 used ageand sex-matched pairs of tall cell and usual papillary carcinoma patients. They found a significantly higher incidence of distant metastases, recurrences, and disease-specific mortality in TCV patients as compared to OPC patients. This method was not used in the present study because of possible bias in the selection of pairs. The reason TCV is associated with high recurrence rates is unknown. It has been shown that TCV is associated with high levels of type IV collagenase, n3 which may be a factor, and that DNA-ploidy does not differ between TCV a n d OCP. 14 The presence of higher mitotic rates is controversial ~5 in TCV. The comparatively small number of patients who died of all types of papillary thyroid carcinoma, the long duration of the study (up to 23 years), and the difficulty of followup are all factors that contribute to the problems of statistical analysis. Many surgeons (36) and several different
THE AMERICANJOURNALOF SURGERY® VOLUME 168 NOVEMBER 1994
TALL CELL PAPILLARY THYROID CANCER/TERRYEl' AL types of operations (10) were involved. A significant number of patients died of other causes (8), were lost to follow-up (30), or were omitted from results analysis because of short follow-up. Several of the physicians involved (14) are now deceased, retired, or moved from the area. Other authors 5,6,s,IJ have described the occurence of other types of thyroid cancer with TCV. These include clear and Htirthle cell, columnar cell, anaplastic, spindle cell, squamous, and mucin-producing types. Indeed, three of the present cases exhibited association with other types. One was associated with anaplastic, another with squamous cell, and the third with a mucin-producing carcinoma. CONCLUSIONS AND RECOMMENDATIONS The incidence of TCV of papillary thyroid carcinoma is significant (19/183 [10%]) in this series. This incidence rate compares to the rates of 10% to 12% reported in previous series. While the recurrence rate of TCV cases is significantly higher than in the other types of papillary carcinoma, the higher recurrence rate of TCV is confined to the 50-and-over age group. Tumor size in the TCV versus OPC groups is statistically larger (P =0.05), and within the tall cell group, tumor size is significantly larger in the 50-and-over age group as compared to the under50 age group (P <0.05). Multivariate analysis demonstrates that age-of-50-and-over group, tumor size greater than 4 cm, and TCV histology are all independently valid predictors of recurrence. In light of these results, the authors propose the following recommendations: (1) the pathologist's report should include the type of papillary carcinoma of the thyroid in the diagnosis (ie, usual type, follicular variant, TCV, columnar cell variant, or sclerosing variant [encapsulated or diffuse]); (2) surgeons should be aware that TCV has a poorer prognosis than OPC, especially in patients aged 50 and over who have tumors greater than 4 cm in size; (3) patients in this high-risk group should be considered for more aggressive therapy (ie, more radical surgery and postoperative radioiodine) in the hope of reducing the high recurrence rate; and (4) further study of this material is necessary
in order to follow these patients and to develop efitefia:for type of surgery and/or postoperative radioiodine treatment. REFERENCES 1. Hazard JB. Nomenclature of thyroid tumors. In: Young S, Inman DR, eds. Proceedings of the 2nd Imperial Cancer Research Fund Symposium. New York, NY: Academic Press; 1968. 2. Robbins J, Merino MJ, Boice JD, et al. Thyroid cancer: a lethal endocrine neoplasm. Ann hzt Med. 1991;115:133-147. 3. Johnson TL, Lloyd RV, Thompson NW, et al. Prognostic implications of the tall cell variant of papillary thyroid carcinomas. Am J Surg Pathol. 1988;12:22-27. 4. Hawk WA, Hazard JB. The many appearances of papillary carcinoma of the thyroid. Cleve Clin Q. 1976;45:207-216. 5. Dickersin GR, Vickery AL, Smith SB. Papillary carcinoma of the thyroid oxyphil-cell type, clear cell variant. Am J Surg Pathol. 1980; 4:501-509. 6. Akslen LA, Varhany JE. Thyroid carcinoma with mixed tall cell and columnar cell features. Am J Clin Pathol. 1990;94:442--445. 7. Yao T. FNA cytology of tall cell variant of papillary thyroid carcinoma. Acta Cytol. 1994;38:282-283. 8. Bronner MP, Livolsi VA. Spindle cell squamous carcinoma of the thyroid: an unusual anaplastic tumor associated with tall cell papillary cancer. Modem Pathol. 1991;4(5):637--643. 9. Rosai J, Carcangiu ML, Delellis RA. Tumors of the thyroid gland. In: Atlas of Tumor Pathology. Washington DC: Armed Forces Institute of Pathology; 1992:114-121. 10. Hicks MJ, Batsakis JG. Tall cell carcinoma of the thyroid gland. Ann Otol Rhh~ol Laryngol. 1993;102:402--403. 11. Livolsi V. Papillary neoplasms of the thyroid: pathologic and prognostic features. Am J Clin Pathol. 1992;3:426-434. 12. Shah JP, Loree TR, Dharker D, et al. Prognostic factors in differential carcinoma of the thyroid gland. Am J Surg. 1992; 164: 658-661. 13. Campo E, Merino MJ, Liotta L, et al. Distribution of the 72-kd type 1V collagenase in nonneoplastic and neoplastic thyroid tissue. Hum Pathol. 1992;23:1395-1401. 14. Flint A, Davenport RO, Lloyd RV. The tall cell variant of papillary carcinoma of the thyroid gland: comparison with the common form of papillary carcinoma by DNA and morphometric analysis. Arch Pathol Lab Med. 1991;115:169-171. 15. Sobrinho-Simoes M, Sambada C, Nesland JM. Letter to the editor. Am J Surg Pathol. 1989;13:79-80.
THE AMERICANJOURNALOF SURGERY® VOLUME 168 NOVEMBER1994 4,61