Bilateral Cervical Lymph Node Metastases in Well-Differentiated Thyroid Cancer Masakuni Noguchi,
MD; Takeo Kumaki, MD; Takao Taniya, MD; Itsuo Miyazaki, MD
\s=b\ We analyzed the regional lymph node metastases of 98 patients with thyroid cancer who underwent bilateral modified neck dissection. Bilateral jugular lymph node metastases were frequent in patients with papillary carcinoma of the thyroid, especially in those patients with obvious carcinoma in both lobes of the gland, cancer arising in the isthmus, clinically detectable bilateral lymphadenopathy, and recurrent thyroid cancer. In patients whose cancer was clinically confined to one lobe, and where there were no obviously enlarged contralateral lymph nodes, the occurrence of contralateral jugular lymph node metastasis was significantly correlated with the contralateral paratracheal lymph node metastasis. The bilateral lymphadenectomy appears to be appropriate in these instances.
(Arch Surg. 1990;125:804-806)
management Surgi c al greatly thyroid
for patients with thyroid cancer var¬ in different institutions. Not only the amount of tissue to be resected but also the indications for, and the extent of, cervical lymph node dissection are contro¬ versial.1"3 In most Western countries, modified neck dissec¬ tion has been performed only in patients with clinically palpa¬ ble cervical lymphadenopathy or proved metastatic disease in the cervical lymph nodes.4 A "wait-and-see" policy is recom¬ mended for patients with no cervical lymphadenopathy. The subsequent appearance of enlarged lymph nodes due to meta¬ ies
static disease often requires reoperation. This postponement of the neck dissection until nodes become palpable may not affect prognosis, but reoperation in the neck is more techni¬ cally difficult than a primary procedure. To reduce lymph node recurrence and to avoid reoperation, most Japanese surgeons prefer elective modified neck dissection, including the ipsilateral cervical lymph nodes and contralateral paratracheal lymph nodes.'"7 Occult lymph node métastases are commonly found when "elective" or "prophylactic" neck dis¬ sections are performed,20*9 and the neck dissection could reduce the lymph node recurrence rate.4,5,10 However, it is likely that bilateral or contralateral cervical lymph node mé¬ tastases will be found in some patients with thyroid cancer.811 Herein, we analyze regional lymph node métastases in 98 patients with well-differentiated carcinoma of the thyroid in whom bilateral modified neck dissection was performed, and we discuss the indications for this procedure. PATIENTS AND METHODS From October 1979 to June 1988, a total of 98 patients (88 women and 10 men) with well-differentiated carcinoma of the thyroid under¬ went subtotal or total thyroidectomy, along with bilateral modified
Accepted for publication March 17,1989. From the Operation Center, Kanazawa (Japan) University Hospital (Dr Noguchi); and the Department of Surgery, School of Medicine, Kanazawa University (Drs Noguchi, Kumaki, Taniya, and Miyazaki). Reprint requests to Operation Center, Kanazawa University Hospital, Takara-machi, 13-1, Kanazawa 920, Japan (Dr Noguchi).
dissection, in the Department of Surgery (II) at Kanazawa (Japan) University Hospital. The mean age of these patients was 49 years, with a range of 27 to 78 years. The histological types of thyroid carcinoma included 88 papillary and 10 follicular carcinomas. The surgical procedure is summarized as follows. The whole thy¬ roid gland was thoroughly inspected and palpated before performing the thyroidectomy. A subtotal or total thyroidectomy, along with lymph node dissection of the central cervical compartment, was first performed en bloc. Either subtotal or total thyroidectomy was per¬ formed, depending on the extent of cancer invasion in the thyroid tissue. Then, the lateral jugular lymph nodes were resected bilateral¬ ly by a method of modified neck dissection, preserving the sternocleidomastoid muscle, internal jugular vein, transverse cervical artery, accessory nerve, brachial plexus, sympathetic trunk, and phrenic nerve. The resected specimens were examined to determine the histological types of thyroid cancer and the presence or absence of lymph node métastases. neck
RESULTS
Of 10 patients with follicular carcinoma, 7 had regional lymph node métastases. However, the nodal métastases oc¬ curred only in the central cervical compartment. From this small series, we conclude that empirically there is no need to remove the jugular lymph nodes in patients with follicular
carcinoma (Table 1). Of 88 patients with papillary carcinoma, 62 had lymph node métastases in the central and jugular compartments. Of 26 patients with tumor in both lobes of the thyroid, the rates of métastases in the central, right, and left jugular chains were 79%, 52%, and 38%, respectively. The rates were 59%, 65%, and 59%, respectively, in 17 patients with cancer located mainly in the isthmus, and 90%, 70%, and 60%, respectively, in 10 patients with recurrent thyroid cancer. In the 2 patients with cancer and clinically detectable bilateral or contralateral jugular lymph node métastases, the rates of metastasis in the central, ipsilateral, and contralateral jugular lymph nodes were 100%, 50%, and 100%, respectively. Moreover, in 33 patients with cancer clinically confined to one lobe who had no obviously involved lymph nodes in the opposite side of the neck, the rates of metastasis in the central, ipsilateral, and contralateral jugular lymph nodes were 64%, 54%, and 27%,
respectively (Table 2). In 33 patients with cancer clinically confined to one lobe who had no obviously involved lymph nodes in the opposite side of the neck, the relations between the occurrence of contralateral jugular lymph node metastasis and the location or size of the primary lesion, or the degree of ipsilateral jugular lymph node metastasis, were evaluated. The frequen¬ cies of contralateral jugular lymph node metastasis in the patients with primary lesions located in the upper part, cen¬ tral part, and lower part of the thyroid lobe, and in the entire lobe, were 23%, 30%, 14%, and 33%, respectively (Table 3). The frequencies in the patients with primary lesions of less than 1.0, 1.1 to 2.0, 2.1 to 3.0, and more than 3.1 cm in diameter, were 9%, 25%, 20%, and 60%, respectively. No
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definite correlations were found among them. There was also no correlation between the occurrence of metastasis in the contralateral jugular lymph nodes and the degree of ipsilater¬ al jugular lymph node metastasis (Table 3). We next examined the relationship between the presence of contralateral paratracheal and contralateral jugular lymph node metastasis. Of 13 patients with disease in the contralat¬ eral paratracheal nodes, 6 (46%) also had involvement of the contralateral jugular chain. Only 2 (10%) of the 20 patients without contralateral paratracheal node disease had contralateral jugular métastases. The difference was statistically
significant (Table 3). The complications in our series of 98 consecutive bilateral neck dissections included 1 case of Homer's syndrome and 4 cases of recurrent nerve palsy. In postoperative follow-up lasting 5 months to 9 years 1 month, 1 patient with lung métastases died 6 years after total thyroidectomy with neck dissection and postoperative radioactive iodine administra¬ tion, and another patient died 3 years after the operation because of an unrelated disease. The regional lymph node recurrences were found in only 2 (2%) of the other 96 patients; 1 patient had ipsilateral upper jugular lymph node recurrence and another patient had mediastinal lymph node recurrence, 7 and 3 years, respectively, after the operation. These pa¬ tients are well after reoperation. Table 1 .—Relation Between Metastasis of Contralateral Jugular Lymph Node and Histological Type of Thyroid Cancer
Histological Type No. of
Papillary
Follicular
88
10
patients
No. with métastases Central compartment
62
Jugular lymph nodes Right
23
Left Bilateral
28
COMMENT
Surgical resection is the most effective treatment for welldifferentiated thyroid cancer. There is, however, controver¬ sy concerning not only the amount of thyroid tissue to be resected but also the indication for, and the extent of, cervical lymph node dissection.1"3 It is generally accepted that lymph node métastases in the central cervical compartment have greater'2 clinical importance than métastases in the lateral chain. These central nodes, therefore, should be completely excised in all patients with operable thyroid cancer. This lymph node dissection, however, should be carefully per¬ formed to avoid damaging the recurrent laryngeal nerve or the parathyroids. In contrast, métastases of the lateral jugu¬ lar lymph nodes rarely affect life expectancy, but the dissec¬ tion can be performed by modified neck dissection, preserv¬ ing the sternocleidomastoid muscle, internal jugular vein, and spinal accessory nerve with minimal morbidity. In most Western countries, the lateral jugular lymph nodes have been dissected by modified neck dissection only in pa¬ tients with clinically palpable cervical lymphadenopathy or proved metastatic cervical lymph nodes.4 The full or classic radical neck dissection is no longer performed, with the ex¬ ception of those patients whose cancer extensively involves the lateral part of the neck.3 For patients with no cervical lymphadenopathy, a wait-and-see policy is recommended. However, it is well known that the frequency of lymph node métastases is high even in those patients in whom elective modified neck dissection is performed.2'8-9 We previously re¬ ported that the frequencies of regional lymph node metastasis in minimal and ordinary thyroid cancer were 57% and 84%, respectively.9 In these patients, the nodal métastases were found not only in the central cervical compartment but also in the jugular nodes. The prognostic value of lymph node in¬ volvement has been debated.1314 Although it is well accepted that prophylactic node dissection does not influence survival, the later development of lymph node disease often requires reoperation.4-5 These secondary procedures may be technical¬ ly difficult and associated with a higher morbidity than the primary operation. The dissection of the ipsilateral jugular lymph nodes is expected to reduce the lymph node recurrence rate in patients with thyroid cancer.4,5-10 To reduce lymph node
Table 2. —Extent of Regional Lymph Node Métastases in
State of Primary Thyroid Lesion Multicentric or grossly widespread involvement Primary lesion in isthmus Recurrent thyroid cancer
No. of Patients
No. (%) With Clinically Palpable Nodes
26
9
(35)
17
7
(41)
10
5
(50)
2
(100)
3
(9)
Papillary Carcinoma
Histologically Proved Regional Lymph Node Metastasis (%) Central compartment (79); R jugular nodes (52); L jugular nodes (38) Central compartment (59); R jugular nodes (65); L jugular nodes (59) Central compartment (90); R jugular nodes (70); L jugular nodes (60)
Degree of Lymph
Node Métastases, % of (No. Metastatic Nodes/ No. of Dissected Nodes) 13
(215/1639)
13
(124/939)
20
(162/797)
Central compartment (100); ipsilateral jugular nodes (50); contralateral jugular nodes (50)
41
(55/135)
Central compartment (64); ipsilateral jugular nodes (54); contralateral jugular nodes (24)
10
(272/2699)
Primary lesion confined to one
lobe
Clinically bilateral or contralateral
jugular lymph
node
métastases
No clinical involvement of contralateral
33
jugular lymph nodes
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Table 3. —Relation Between Metastasis of Contralateral Jugular Lymph Node and Various Other Characteristics*
Characteristic Location of primary lesion in gland
No. of Patients
No. (%) With Metastasis of Contralateral Jugular Lymph Node
Upper part
13
3
Central part Lower part
10
3 1 1
Whole lobe Maximum diameter of
lesion, cm
primary
s1.0 1.0-2.0
11 12
2.1-3.0 ==3.1
1
(9) (25) (20) 3 (60) 3 1
Degree of ipsilateral cervical lymph node metastasis, % ^10
19
11-20 21-30 >41 Metastasis in contralateral paratracheal lymph node Positive
Total "These 33
tP
MD; Takeo Kumaki, MD; Takao Taniya, MD; Itsuo Miyazaki, MD
\s=b\ We analyzed the regional lymph node metastases of 98 patients with thyroid cancer who underwent bilateral modified neck dissection. Bilateral jugular lymph node metastases were frequent in patients with papillary carcinoma of the thyroid, especially in those patients with obvious carcinoma in both lobes of the gland, cancer arising in the isthmus, clinically detectable bilateral lymphadenopathy, and recurrent thyroid cancer. In patients whose cancer was clinically confined to one lobe, and where there were no obviously enlarged contralateral lymph nodes, the occurrence of contralateral jugular lymph node metastasis was significantly correlated with the contralateral paratracheal lymph node metastasis. The bilateral lymphadenectomy appears to be appropriate in these instances.
(Arch Surg. 1990;125:804-806)
management Surgi c al greatly thyroid
for patients with thyroid cancer var¬ in different institutions. Not only the amount of tissue to be resected but also the indications for, and the extent of, cervical lymph node dissection are contro¬ versial.1"3 In most Western countries, modified neck dissec¬ tion has been performed only in patients with clinically palpa¬ ble cervical lymphadenopathy or proved metastatic disease in the cervical lymph nodes.4 A "wait-and-see" policy is recom¬ mended for patients with no cervical lymphadenopathy. The subsequent appearance of enlarged lymph nodes due to meta¬ ies
static disease often requires reoperation. This postponement of the neck dissection until nodes become palpable may not affect prognosis, but reoperation in the neck is more techni¬ cally difficult than a primary procedure. To reduce lymph node recurrence and to avoid reoperation, most Japanese surgeons prefer elective modified neck dissection, including the ipsilateral cervical lymph nodes and contralateral paratracheal lymph nodes.'"7 Occult lymph node métastases are commonly found when "elective" or "prophylactic" neck dis¬ sections are performed,20*9 and the neck dissection could reduce the lymph node recurrence rate.4,5,10 However, it is likely that bilateral or contralateral cervical lymph node mé¬ tastases will be found in some patients with thyroid cancer.811 Herein, we analyze regional lymph node métastases in 98 patients with well-differentiated carcinoma of the thyroid in whom bilateral modified neck dissection was performed, and we discuss the indications for this procedure. PATIENTS AND METHODS From October 1979 to June 1988, a total of 98 patients (88 women and 10 men) with well-differentiated carcinoma of the thyroid under¬ went subtotal or total thyroidectomy, along with bilateral modified
Accepted for publication March 17,1989. From the Operation Center, Kanazawa (Japan) University Hospital (Dr Noguchi); and the Department of Surgery, School of Medicine, Kanazawa University (Drs Noguchi, Kumaki, Taniya, and Miyazaki). Reprint requests to Operation Center, Kanazawa University Hospital, Takara-machi, 13-1, Kanazawa 920, Japan (Dr Noguchi).
dissection, in the Department of Surgery (II) at Kanazawa (Japan) University Hospital. The mean age of these patients was 49 years, with a range of 27 to 78 years. The histological types of thyroid carcinoma included 88 papillary and 10 follicular carcinomas. The surgical procedure is summarized as follows. The whole thy¬ roid gland was thoroughly inspected and palpated before performing the thyroidectomy. A subtotal or total thyroidectomy, along with lymph node dissection of the central cervical compartment, was first performed en bloc. Either subtotal or total thyroidectomy was per¬ formed, depending on the extent of cancer invasion in the thyroid tissue. Then, the lateral jugular lymph nodes were resected bilateral¬ ly by a method of modified neck dissection, preserving the sternocleidomastoid muscle, internal jugular vein, transverse cervical artery, accessory nerve, brachial plexus, sympathetic trunk, and phrenic nerve. The resected specimens were examined to determine the histological types of thyroid cancer and the presence or absence of lymph node métastases. neck
RESULTS
Of 10 patients with follicular carcinoma, 7 had regional lymph node métastases. However, the nodal métastases oc¬ curred only in the central cervical compartment. From this small series, we conclude that empirically there is no need to remove the jugular lymph nodes in patients with follicular
carcinoma (Table 1). Of 88 patients with papillary carcinoma, 62 had lymph node métastases in the central and jugular compartments. Of 26 patients with tumor in both lobes of the thyroid, the rates of métastases in the central, right, and left jugular chains were 79%, 52%, and 38%, respectively. The rates were 59%, 65%, and 59%, respectively, in 17 patients with cancer located mainly in the isthmus, and 90%, 70%, and 60%, respectively, in 10 patients with recurrent thyroid cancer. In the 2 patients with cancer and clinically detectable bilateral or contralateral jugular lymph node métastases, the rates of metastasis in the central, ipsilateral, and contralateral jugular lymph nodes were 100%, 50%, and 100%, respectively. Moreover, in 33 patients with cancer clinically confined to one lobe who had no obviously involved lymph nodes in the opposite side of the neck, the rates of metastasis in the central, ipsilateral, and contralateral jugular lymph nodes were 64%, 54%, and 27%,
respectively (Table 2). In 33 patients with cancer clinically confined to one lobe who had no obviously involved lymph nodes in the opposite side of the neck, the relations between the occurrence of contralateral jugular lymph node metastasis and the location or size of the primary lesion, or the degree of ipsilateral jugular lymph node metastasis, were evaluated. The frequen¬ cies of contralateral jugular lymph node metastasis in the patients with primary lesions located in the upper part, cen¬ tral part, and lower part of the thyroid lobe, and in the entire lobe, were 23%, 30%, 14%, and 33%, respectively (Table 3). The frequencies in the patients with primary lesions of less than 1.0, 1.1 to 2.0, 2.1 to 3.0, and more than 3.1 cm in diameter, were 9%, 25%, 20%, and 60%, respectively. No
Downloaded From: http://archsurg.jamanetwork.com/ by a New York University User on 06/22/2015
definite correlations were found among them. There was also no correlation between the occurrence of metastasis in the contralateral jugular lymph nodes and the degree of ipsilater¬ al jugular lymph node metastasis (Table 3). We next examined the relationship between the presence of contralateral paratracheal and contralateral jugular lymph node metastasis. Of 13 patients with disease in the contralat¬ eral paratracheal nodes, 6 (46%) also had involvement of the contralateral jugular chain. Only 2 (10%) of the 20 patients without contralateral paratracheal node disease had contralateral jugular métastases. The difference was statistically
significant (Table 3). The complications in our series of 98 consecutive bilateral neck dissections included 1 case of Homer's syndrome and 4 cases of recurrent nerve palsy. In postoperative follow-up lasting 5 months to 9 years 1 month, 1 patient with lung métastases died 6 years after total thyroidectomy with neck dissection and postoperative radioactive iodine administra¬ tion, and another patient died 3 years after the operation because of an unrelated disease. The regional lymph node recurrences were found in only 2 (2%) of the other 96 patients; 1 patient had ipsilateral upper jugular lymph node recurrence and another patient had mediastinal lymph node recurrence, 7 and 3 years, respectively, after the operation. These pa¬ tients are well after reoperation. Table 1 .—Relation Between Metastasis of Contralateral Jugular Lymph Node and Histological Type of Thyroid Cancer
Histological Type No. of
Papillary
Follicular
88
10
patients
No. with métastases Central compartment
62
Jugular lymph nodes Right
23
Left Bilateral
28
COMMENT
Surgical resection is the most effective treatment for welldifferentiated thyroid cancer. There is, however, controver¬ sy concerning not only the amount of thyroid tissue to be resected but also the indication for, and the extent of, cervical lymph node dissection.1"3 It is generally accepted that lymph node métastases in the central cervical compartment have greater'2 clinical importance than métastases in the lateral chain. These central nodes, therefore, should be completely excised in all patients with operable thyroid cancer. This lymph node dissection, however, should be carefully per¬ formed to avoid damaging the recurrent laryngeal nerve or the parathyroids. In contrast, métastases of the lateral jugu¬ lar lymph nodes rarely affect life expectancy, but the dissec¬ tion can be performed by modified neck dissection, preserv¬ ing the sternocleidomastoid muscle, internal jugular vein, and spinal accessory nerve with minimal morbidity. In most Western countries, the lateral jugular lymph nodes have been dissected by modified neck dissection only in pa¬ tients with clinically palpable cervical lymphadenopathy or proved metastatic cervical lymph nodes.4 The full or classic radical neck dissection is no longer performed, with the ex¬ ception of those patients whose cancer extensively involves the lateral part of the neck.3 For patients with no cervical lymphadenopathy, a wait-and-see policy is recommended. However, it is well known that the frequency of lymph node métastases is high even in those patients in whom elective modified neck dissection is performed.2'8-9 We previously re¬ ported that the frequencies of regional lymph node metastasis in minimal and ordinary thyroid cancer were 57% and 84%, respectively.9 In these patients, the nodal métastases were found not only in the central cervical compartment but also in the jugular nodes. The prognostic value of lymph node in¬ volvement has been debated.1314 Although it is well accepted that prophylactic node dissection does not influence survival, the later development of lymph node disease often requires reoperation.4-5 These secondary procedures may be technical¬ ly difficult and associated with a higher morbidity than the primary operation. The dissection of the ipsilateral jugular lymph nodes is expected to reduce the lymph node recurrence rate in patients with thyroid cancer.4,5-10 To reduce lymph node
Table 2. —Extent of Regional Lymph Node Métastases in
State of Primary Thyroid Lesion Multicentric or grossly widespread involvement Primary lesion in isthmus Recurrent thyroid cancer
No. of Patients
No. (%) With Clinically Palpable Nodes
26
9
(35)
17
7
(41)
10
5
(50)
2
(100)
3
(9)
Papillary Carcinoma
Histologically Proved Regional Lymph Node Metastasis (%) Central compartment (79); R jugular nodes (52); L jugular nodes (38) Central compartment (59); R jugular nodes (65); L jugular nodes (59) Central compartment (90); R jugular nodes (70); L jugular nodes (60)
Degree of Lymph
Node Métastases, % of (No. Metastatic Nodes/ No. of Dissected Nodes) 13
(215/1639)
13
(124/939)
20
(162/797)
Central compartment (100); ipsilateral jugular nodes (50); contralateral jugular nodes (50)
41
(55/135)
Central compartment (64); ipsilateral jugular nodes (54); contralateral jugular nodes (24)
10
(272/2699)
Primary lesion confined to one
lobe
Clinically bilateral or contralateral
jugular lymph
node
métastases
No clinical involvement of contralateral
33
jugular lymph nodes
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Table 3. —Relation Between Metastasis of Contralateral Jugular Lymph Node and Various Other Characteristics*
Characteristic Location of primary lesion in gland
No. of Patients
No. (%) With Metastasis of Contralateral Jugular Lymph Node
Upper part
13
3
Central part Lower part
10
3 1 1
Whole lobe Maximum diameter of
lesion, cm
primary
s1.0 1.0-2.0
11 12
2.1-3.0 ==3.1
1
(9) (25) (20) 3 (60) 3 1
Degree of ipsilateral cervical lymph node metastasis, % ^10
19
11-20 21-30 >41 Metastasis in contralateral paratracheal lymph node Positive
Total "These 33
tP
