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Cystic metastases of the neck from occult thyroid adenocarcinoma
Cystic Metastases of the Neck From Occult Thyroid Adenocarcinoma Isaac Levy,
MD,
Yehiel Barki,
In 9 of 118 patients with differentiated thyroid carcinomas, a solitary cystic lateral cervical mass simulating a branchial cleft anomaly was the sole presenting sign of the disease. These masses were nodal metastases of occult papillary adenocarcinoma of the thyroid that underwent liquefaction necrosis. Sonographically, the masses presented a complex pattern. Accordingly, it is suggested that, in patients presenting with an asymptomatic solitary lateral cystic cervical mass, the possibility of metastasis from an occult thyroid malignancy should be considered, and consent for definitive surgery should be obtained. The ultrasonic pattern of the cystic mass is of importance in the differentiation of a cavitated lymph node from a branchial cleft cyst.
MD,
Ferit Tovi,
MD,
Beer-Seva,Israel
ymph node metastases of head and neck carcinomas L may present as the sole manifestation of the disease [I-5]. Regardless of the site of the initial tumor, the nodal metastases usually appear in the lateral neck as a solid nodule and sometimes in the form of a cystic mass [4,5]. Although cystic nodal metastases have been known to pathologists for many years [a, this entity is seldom mentioned in the literature or in current textbooks of surgery. In this study, we describe a series of cervical cystic lymph node metastases from occult thyroid papillary adenocarcinoma that clinically simulated a branchial cleft cyst. The pathogenesis and the ultrasonic aspects of this entity are discussed. PATIENTS AND METHOD
The records of 118 patients treated for differentiated thyroid carcinoma at the Departments of Otolaryngology-Head and Neck Surgery and General Surgery of Soroka Medical Center, Beer-Z&a, Israel, were reviewed. The time span covers 10 years, from 1978 to 1988. In 11 of these patients, the presenting sign of the disease was an asymptomatic solitary lateral cervical mass. No palpable abnormality in the thyroid gland was found in any of these patients. The patients ranged in age from 21 to 45 years with a median age of 34 years. In addition to a physical examination, all patients underwent endoscopic examination of the upper aero-digestive tract, cheat roentgenogram, I 131thyroid scan, and ultrasonographic study of the cervical mass. Fineneedle aspiration biopsy of the mass was performed only in five patients. Excisional biopsy of the lateral cervical mass was performed in all patients, and the specimens were histologically studied. RESULTS
From the Denartment of Surgery “B” (IL), Ultrasound Unit (YB), and Otolaryngol&y and Head and-Neck‘Su&ry (IT), Soroka Medical Center, Faculty of Health Sciences, Ben Gurion University of the Negev, Beer-Seva, Israel. Requests for reprints should be addressed to Isaac Levy, MD, Department of Surgery “B”, Soroka Medical Center, P.O.B. 151, BeerSeva 84101, Israel. Manuscript submitted September 10,1990, and accepted in revised form January 14,199l.
298
THE AMERICAN JOURNAL OF SURGERY
In a series of 118 cases of differentiated thyroid carcinoma, 11 patients (9.3%) initially presented with a solitary lateral cervical mass, clinically distinct from the thyroid gland, as the sole sign of the disease. In nine of these patients, the mass was of cystic consistency. In one of the nine patients, the cystic mass was of huge diiension (12 X 8 cm). Physical examination showed no other abnormality in the head or neck. Endoscopic studies revealed no abnormality in the aero-digestive tract. Chest roentgenogram and the 1131thyroid scan were reported as normal. The ultrasonography of the cervical mass revealed a solid structure in two patients and a cystic structure with solid components in the cystic wall in the other nine patients. Fine-needle aspiration biopsy of the cystic masses was contributory to diagnosis in only one patient, suggesting a papillary adenocarcinoma. In all instances, the histologic features of the excised masses were compatible with
VOLUME 163 MARCH 1992
METASTASES OF THE NECK
lymph node metastasis of thyroid papillary adenocarcinoma. Cystic cavitation of the lymph node was noted in nine specimens that showed the same morphologic pattern in ultrasound. Upon the histologic diagnosis, the patients underwent total thyroidectomy and functional neck dissection, Unilocular or multilocular occult papillary carcinoma was demonstrated in all the thyroidectomy specimens. In two patients, the tumor appeared in the form of sclerosing carcinoma. COMMENTS Carcinoma of the thyroid gland usually appears as a nodule in the anterior aspect of the lower neck. Less frequently, the primary tumor in the thyroid gland is occult, and the lymph node metastases present as the sole manifestation of the disease [I ,3]. The vast majority of thyroid carcinomas are well-differentiated tumors. Papillary adenocarcinoma is by far the most common malignant tumor of this gland, comprising at least 80% of the thyroid malignancies in patients less than 40 years old and approximately 60% of overall thyroid neoplasms [ 71. Although it occurs most commonly in women, it is more virulent in older men [8]. The tumor is typically uncapsulated and often multifocal. It usually shows a slow growth rate and a favorable prognosis. But this relatively benign behavior is not constant. The growth rate may accelerate at any stage, and the tumor may become locally aggressive [9]. Lymph node metastases occur frequently [10,11]. These secondary tumors appear commonly in the lateral neck in the form of solid nodules, and, in 10% to 13% of patients, they are the sole manifestation of the disease [12,13]. The rapid growth of the tumoral process within the metastatic lymph node may result in liquefaction necrosis [24,15], transforming the lymph node into a fluid-filled mass, as occurred in the present series. Cystic degeneration of a metastatic lymph node has also been described in nodal secondary tumors of other malignancies in the head and neck, such as in tonsillar cancers, in malignant salivary gland tumors, and in nasopharyngeal carcinomas [4,5]. When the primary tumor is undiagnosed, the cystic metastatic lymph nodes may be confused with branchial cleft cysts [4]. Indeed, both entities share the same location and usually present as asymptomatic lateral cervical masses. It is worthwhile to mention that cystic nodal metastases tend to occur in young adults [4,5], as ob served in our series. Fine-needle aspiration biopsy contributed to the diagnosis in only one of five patients who underwent this procedure. This method, although important in the diagnosis of solid nodules, has not always been rewarding in the diagnosis of cystic lesions [4]. In our patients, attention was drawn to the thyroid gland only after excisional biopsy of the cervical mass showed a metastatic papillary adenocarcinoma. Ii3i thyroid scans in the present series did not detect the occult lesion in the thyroid gland. Indeed, this modality of investigation is unable to detect thyroid lesions less than 1 cm in diameter 1161. Ultrasonography of the lateral cervical mass was of
value, not only in confirming the cystic nature of this lesion, but also in demonstrating its complex pattern, indicated by the presence of solid elements in the cyst wall. This finding eliminates the possibility of a true cyst [ 171, which basically manifests with a homogenous echofree ultrasonic configuration and strong posterior wall echoes (“through transmission”) [28,29]. Ultrasonically, lymph nodes present as well-defined homogenous, hypoechoic, solid structures [20]. Malignant lymph nodes usually become enlarged and may show a heterogenous echogenicity corresponding to their nonhomogenous histologic pattern [21]. In the case of diffuse liquefaction necrosis, the impedance of the nodal structure to the ultrasonic beam will decrease. Total necrosis of tumors in lymph nodes is by no means rare [22]. Almost always, some viable tissue remains within the node. Since the necrotic and viable tissues are of different acoustic impedance, the sound beam that encounters this interface reflects echoes, which in turn produce the complex ultrasonic pattern of the cystic metastatic lymph node [17]. In conclusion, the presence of a solitary, asymptomatic lateral cystic cervical mass with a complex ultrasonic pattern should alert the physician to the possibility of a nodal metastasis from an occult regional malignancy including papillary adenocarcinoma of the thyroid gland. The latter condition should be considered, especially in young adults among whom this tumor occurs most often. Consent for a possible thyroidectomy and neck dissection must be obtained, and frozen section examination of the cystic mass should be planned, in order to carry out the definitive surgical treatment. REFERENCES 1. Clay RC, Blackman SS Jr. Lateral aberrant thyroid:metastasis to lymph nodes from primary carcinoma of the thyroid gland. Arch Surg 1944; 48: 223-8. 2. Martin H. Untimely lymph node biopsy. Am J Surg 1961; 102: 17-8. 3. Maceri R, Babyak J, Ossakow SJ. Lateral neck mass. Sole presenting sign of metastatic thyroid cancer. Arch Otolaryngol Head Neck Surg 1986; 12: 47-9. 4. Cinberg JZ, Silver CE, Mohnar JJ, Vogl SE. Cervical cysts: cancer until proven otherwise. Laryngoscope 1982; 92: 27-30. 5. Micheau C, Cachin Y, Caillou B. Cystic metastases in the neck revealing occult carcinoma of the tonsil. Cancer 1974; 33: 228-33. 6. Ackerman KV. Surgical pathology. 4th ed. St. Louis: CV Mosby, 1968: 782. 7. Woolner LB, Beahrs OH, Black BM, et al. Classification and prognosis of thyroid carcinoma. Am J Surg 1961; 102: 354-87. 8. Crile G Jr. Survival of patients with papillary carcinoma of thyroid after conservative operations. Am J Surg 1964; 108: 862-6. 9. Tovi F, Goldstein J. Locally aggressive differentiated thyroid carcinoma. J Surg Oncol 1985; 29: 99-104. 10. Wcolner LB. Occult papillary carcinoma of the thyroid gland. A study of 140 cases in a 30-year period. J Clin Endocrinol Metab 1968; 20: 89-105. 11. Lindahl F. Papillary thyroid carcinoma in Denmark. Cancer 1975; 36: 540-52. 12. Crile G Jr. The fallacy of the conventional radical neck dissection for papillary carcinoma of the thyroid. Ann Surg 1957; 145: 317-20. 13. Wade H. The treatment and preoperative diagnosis of differen-
THE AMERICAN JOURNAL OF SURGERY
VOLUME 163 MARCH 1992
299
LEVY ET AL
tiated thyroid carcinoma presenting as a clinically solitary nodule. Br J Surg 1989; 67: 728-31. 14. Tovi F, Zirkin H. Solitary lateral cervical cyst: presenting symptom of papillary thyroid adenocarcinoma. Ann Gtol Rbinol Laryngol 1983; 92: 521-4. 15. Searls HH, Davies 0, Lindsay S. Metastatic carcinoma of the thyroid gland as the initial manifestation of the disease. Calif Med 1952; 76: 62-S. 16. Katsutaro S, Sokol J. Differentiation of benign and malignant thyroid nodules. Arch Intern Med 1964; 114: 36-9. 17. Tovi F, Barki Y, Zirkin H. Ultrasonic diagnosis of a metastatic cystic lymph node. Ann Gtol Rhino1 Laryngol 1987; 96: 716-7. 18. McCurdy JA, Nadalo LA, Yii DWS. Evaluation of extra-
300
THE AMERICAN JOURNAL OF SURGERY
thyroid masses of the head and neck with grey scale ultrasound. Arch Gtolarynol 1980; 106: 83-7. 19. Bimholz JC. Sonic differentiation of cysts and homogenous solid masses. Radiology 1973; 108: 699-702. 20. Marchal G, Gyen R, Verschakelen J, et al. Sonographic ag pearance of normal lymph nodes. J Ultrasound Med 1985; 4: 417-9. 21. Bruneton JN, Roux P, Caramella E, Demard F, et al. Ear, nose and throat cancer: ultrasound diagnosis of metastasis to cervical lymph nodes. Radiology 1984; 152: 771-3. 22. Symmers W St C. The lymphoreticular system. In: Symmers W St C. Systemic pathology. 2nd ed. Edinburgh: Churchill-Livingstone, 1978: 551-3.
VOLUME 163 MARCH 1992
MD,
Yehiel Barki,
In 9 of 118 patients with differentiated thyroid carcinomas, a solitary cystic lateral cervical mass simulating a branchial cleft anomaly was the sole presenting sign of the disease. These masses were nodal metastases of occult papillary adenocarcinoma of the thyroid that underwent liquefaction necrosis. Sonographically, the masses presented a complex pattern. Accordingly, it is suggested that, in patients presenting with an asymptomatic solitary lateral cystic cervical mass, the possibility of metastasis from an occult thyroid malignancy should be considered, and consent for definitive surgery should be obtained. The ultrasonic pattern of the cystic mass is of importance in the differentiation of a cavitated lymph node from a branchial cleft cyst.
MD,
Ferit Tovi,
MD,
Beer-Seva,Israel
ymph node metastases of head and neck carcinomas L may present as the sole manifestation of the disease [I-5]. Regardless of the site of the initial tumor, the nodal metastases usually appear in the lateral neck as a solid nodule and sometimes in the form of a cystic mass [4,5]. Although cystic nodal metastases have been known to pathologists for many years [a, this entity is seldom mentioned in the literature or in current textbooks of surgery. In this study, we describe a series of cervical cystic lymph node metastases from occult thyroid papillary adenocarcinoma that clinically simulated a branchial cleft cyst. The pathogenesis and the ultrasonic aspects of this entity are discussed. PATIENTS AND METHOD
The records of 118 patients treated for differentiated thyroid carcinoma at the Departments of Otolaryngology-Head and Neck Surgery and General Surgery of Soroka Medical Center, Beer-Z&a, Israel, were reviewed. The time span covers 10 years, from 1978 to 1988. In 11 of these patients, the presenting sign of the disease was an asymptomatic solitary lateral cervical mass. No palpable abnormality in the thyroid gland was found in any of these patients. The patients ranged in age from 21 to 45 years with a median age of 34 years. In addition to a physical examination, all patients underwent endoscopic examination of the upper aero-digestive tract, cheat roentgenogram, I 131thyroid scan, and ultrasonographic study of the cervical mass. Fineneedle aspiration biopsy of the mass was performed only in five patients. Excisional biopsy of the lateral cervical mass was performed in all patients, and the specimens were histologically studied. RESULTS
From the Denartment of Surgery “B” (IL), Ultrasound Unit (YB), and Otolaryngol&y and Head and-Neck‘Su&ry (IT), Soroka Medical Center, Faculty of Health Sciences, Ben Gurion University of the Negev, Beer-Seva, Israel. Requests for reprints should be addressed to Isaac Levy, MD, Department of Surgery “B”, Soroka Medical Center, P.O.B. 151, BeerSeva 84101, Israel. Manuscript submitted September 10,1990, and accepted in revised form January 14,199l.
298
THE AMERICAN JOURNAL OF SURGERY
In a series of 118 cases of differentiated thyroid carcinoma, 11 patients (9.3%) initially presented with a solitary lateral cervical mass, clinically distinct from the thyroid gland, as the sole sign of the disease. In nine of these patients, the mass was of cystic consistency. In one of the nine patients, the cystic mass was of huge diiension (12 X 8 cm). Physical examination showed no other abnormality in the head or neck. Endoscopic studies revealed no abnormality in the aero-digestive tract. Chest roentgenogram and the 1131thyroid scan were reported as normal. The ultrasonography of the cervical mass revealed a solid structure in two patients and a cystic structure with solid components in the cystic wall in the other nine patients. Fine-needle aspiration biopsy of the cystic masses was contributory to diagnosis in only one patient, suggesting a papillary adenocarcinoma. In all instances, the histologic features of the excised masses were compatible with
VOLUME 163 MARCH 1992
METASTASES OF THE NECK
lymph node metastasis of thyroid papillary adenocarcinoma. Cystic cavitation of the lymph node was noted in nine specimens that showed the same morphologic pattern in ultrasound. Upon the histologic diagnosis, the patients underwent total thyroidectomy and functional neck dissection, Unilocular or multilocular occult papillary carcinoma was demonstrated in all the thyroidectomy specimens. In two patients, the tumor appeared in the form of sclerosing carcinoma. COMMENTS Carcinoma of the thyroid gland usually appears as a nodule in the anterior aspect of the lower neck. Less frequently, the primary tumor in the thyroid gland is occult, and the lymph node metastases present as the sole manifestation of the disease [I ,3]. The vast majority of thyroid carcinomas are well-differentiated tumors. Papillary adenocarcinoma is by far the most common malignant tumor of this gland, comprising at least 80% of the thyroid malignancies in patients less than 40 years old and approximately 60% of overall thyroid neoplasms [ 71. Although it occurs most commonly in women, it is more virulent in older men [8]. The tumor is typically uncapsulated and often multifocal. It usually shows a slow growth rate and a favorable prognosis. But this relatively benign behavior is not constant. The growth rate may accelerate at any stage, and the tumor may become locally aggressive [9]. Lymph node metastases occur frequently [10,11]. These secondary tumors appear commonly in the lateral neck in the form of solid nodules, and, in 10% to 13% of patients, they are the sole manifestation of the disease [12,13]. The rapid growth of the tumoral process within the metastatic lymph node may result in liquefaction necrosis [24,15], transforming the lymph node into a fluid-filled mass, as occurred in the present series. Cystic degeneration of a metastatic lymph node has also been described in nodal secondary tumors of other malignancies in the head and neck, such as in tonsillar cancers, in malignant salivary gland tumors, and in nasopharyngeal carcinomas [4,5]. When the primary tumor is undiagnosed, the cystic metastatic lymph nodes may be confused with branchial cleft cysts [4]. Indeed, both entities share the same location and usually present as asymptomatic lateral cervical masses. It is worthwhile to mention that cystic nodal metastases tend to occur in young adults [4,5], as ob served in our series. Fine-needle aspiration biopsy contributed to the diagnosis in only one of five patients who underwent this procedure. This method, although important in the diagnosis of solid nodules, has not always been rewarding in the diagnosis of cystic lesions [4]. In our patients, attention was drawn to the thyroid gland only after excisional biopsy of the cervical mass showed a metastatic papillary adenocarcinoma. Ii3i thyroid scans in the present series did not detect the occult lesion in the thyroid gland. Indeed, this modality of investigation is unable to detect thyroid lesions less than 1 cm in diameter 1161. Ultrasonography of the lateral cervical mass was of
value, not only in confirming the cystic nature of this lesion, but also in demonstrating its complex pattern, indicated by the presence of solid elements in the cyst wall. This finding eliminates the possibility of a true cyst [ 171, which basically manifests with a homogenous echofree ultrasonic configuration and strong posterior wall echoes (“through transmission”) [28,29]. Ultrasonically, lymph nodes present as well-defined homogenous, hypoechoic, solid structures [20]. Malignant lymph nodes usually become enlarged and may show a heterogenous echogenicity corresponding to their nonhomogenous histologic pattern [21]. In the case of diffuse liquefaction necrosis, the impedance of the nodal structure to the ultrasonic beam will decrease. Total necrosis of tumors in lymph nodes is by no means rare [22]. Almost always, some viable tissue remains within the node. Since the necrotic and viable tissues are of different acoustic impedance, the sound beam that encounters this interface reflects echoes, which in turn produce the complex ultrasonic pattern of the cystic metastatic lymph node [17]. In conclusion, the presence of a solitary, asymptomatic lateral cystic cervical mass with a complex ultrasonic pattern should alert the physician to the possibility of a nodal metastasis from an occult regional malignancy including papillary adenocarcinoma of the thyroid gland. The latter condition should be considered, especially in young adults among whom this tumor occurs most often. Consent for a possible thyroidectomy and neck dissection must be obtained, and frozen section examination of the cystic mass should be planned, in order to carry out the definitive surgical treatment. REFERENCES 1. Clay RC, Blackman SS Jr. Lateral aberrant thyroid:metastasis to lymph nodes from primary carcinoma of the thyroid gland. Arch Surg 1944; 48: 223-8. 2. Martin H. Untimely lymph node biopsy. Am J Surg 1961; 102: 17-8. 3. Maceri R, Babyak J, Ossakow SJ. Lateral neck mass. Sole presenting sign of metastatic thyroid cancer. Arch Otolaryngol Head Neck Surg 1986; 12: 47-9. 4. Cinberg JZ, Silver CE, Mohnar JJ, Vogl SE. Cervical cysts: cancer until proven otherwise. Laryngoscope 1982; 92: 27-30. 5. Micheau C, Cachin Y, Caillou B. Cystic metastases in the neck revealing occult carcinoma of the tonsil. Cancer 1974; 33: 228-33. 6. Ackerman KV. Surgical pathology. 4th ed. St. Louis: CV Mosby, 1968: 782. 7. Woolner LB, Beahrs OH, Black BM, et al. Classification and prognosis of thyroid carcinoma. Am J Surg 1961; 102: 354-87. 8. Crile G Jr. Survival of patients with papillary carcinoma of thyroid after conservative operations. Am J Surg 1964; 108: 862-6. 9. Tovi F, Goldstein J. Locally aggressive differentiated thyroid carcinoma. J Surg Oncol 1985; 29: 99-104. 10. Wcolner LB. Occult papillary carcinoma of the thyroid gland. A study of 140 cases in a 30-year period. J Clin Endocrinol Metab 1968; 20: 89-105. 11. Lindahl F. Papillary thyroid carcinoma in Denmark. Cancer 1975; 36: 540-52. 12. Crile G Jr. The fallacy of the conventional radical neck dissection for papillary carcinoma of the thyroid. Ann Surg 1957; 145: 317-20. 13. Wade H. The treatment and preoperative diagnosis of differen-
THE AMERICAN JOURNAL OF SURGERY
VOLUME 163 MARCH 1992
299
LEVY ET AL
tiated thyroid carcinoma presenting as a clinically solitary nodule. Br J Surg 1989; 67: 728-31. 14. Tovi F, Zirkin H. Solitary lateral cervical cyst: presenting symptom of papillary thyroid adenocarcinoma. Ann Gtol Rbinol Laryngol 1983; 92: 521-4. 15. Searls HH, Davies 0, Lindsay S. Metastatic carcinoma of the thyroid gland as the initial manifestation of the disease. Calif Med 1952; 76: 62-S. 16. Katsutaro S, Sokol J. Differentiation of benign and malignant thyroid nodules. Arch Intern Med 1964; 114: 36-9. 17. Tovi F, Barki Y, Zirkin H. Ultrasonic diagnosis of a metastatic cystic lymph node. Ann Gtol Rhino1 Laryngol 1987; 96: 716-7. 18. McCurdy JA, Nadalo LA, Yii DWS. Evaluation of extra-
300
THE AMERICAN JOURNAL OF SURGERY
thyroid masses of the head and neck with grey scale ultrasound. Arch Gtolarynol 1980; 106: 83-7. 19. Bimholz JC. Sonic differentiation of cysts and homogenous solid masses. Radiology 1973; 108: 699-702. 20. Marchal G, Gyen R, Verschakelen J, et al. Sonographic ag pearance of normal lymph nodes. J Ultrasound Med 1985; 4: 417-9. 21. Bruneton JN, Roux P, Caramella E, Demard F, et al. Ear, nose and throat cancer: ultrasound diagnosis of metastasis to cervical lymph nodes. Radiology 1984; 152: 771-3. 22. Symmers W St C. The lymphoreticular system. In: Symmers W St C. Systemic pathology. 2nd ed. Edinburgh: Churchill-Livingstone, 1978: 551-3.
VOLUME 163 MARCH 1992