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 Table of Contents  
ORIGINAL ARTICLE
Year : 2015  |  Volume : 28  |  Issue : 1  |  Page : 43-48

Bilateral central lymph node dissection with thyroidectomy for papillary thyroid cancer


1 Department of Surgery, Faculty of Medicine, Menoufia University, Menoufia, Egypt
2 Department of Surgery, Nile Insurance Hospital, Shupra El-Khaima, Egypt

Date of Submission25-Feb-2014
Date of Acceptance24-Mar-2014
Date of Web Publication29-Apr-2015

Correspondence Address:
Tarek H.A. Abu El-Nasr
20 Walii El-Ahd Extension St, Hadayek El-Koppa, Cairo
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1110-2098.155938

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  Abstract 

Objectives
The aims of the study were to evaluate the frequency and pattern of central neck lymph node metastasis in papillary thyroid cancer and its relation to the lateral neck lymph node metastasis. Also, this study aimed to evaluate the complications of central neck dissection.
Background
The indications and extent of central lymph node dissection (CLND) in the treatment of papillary thyroid carcinoma remain controversial, and its therapeutic effect remains debatable.
Patients and methods
A total of 30 patients diagnosed with papillary thyroid cancer were treated from 2011 to 2013. All patients underwent total thyroidectomy and bilateral central neck dissection. In patients with positive central lymph node metastases in frozen section, we performed ipsilateral lateral lymph node dissection removing levels II to V. Central lymph node metastases were analyzed. In addition, we investigated postoperative complications after total thyroidectomy and CLND.
Results
Among 30 patients, 12 (40%) had central lymph node metastases, with the ipsilateral paratracheal lymph nodes most commonly affected (40%). Of the 12 patients with positive central lymph node metastases, only two had positive lateral lymph node metastases. The frequency of temporary hypocalcemia, permanent hypocalcemia, and temporary vocal cord paralysis was 16.7, 6.7, and 6.7%, respectively.
Conclusion
CLND prevents nodal recurrence in the central compartment, which carries a high incidence of morbidity during surgery for recurrence. In addition, CLND, in good hands, does not contribute to the morbidity of total thyroidectomy (hypoparathyroidism and recurrent laryngeal nerve injury). We propose that total thyroidectomy and bilateral CLND are the least-recommended surgical treatments. Also, in clinically negative lateral nodes, we conclude that lateral lymph node dissection is not important even if central lymph nodes were positive for metastases.

Keywords: Central, lymph node metastases, papillary, thyroid


How to cite this article:
El-Kased AF, El-Foll HA, El-Gammal AS, Abu El-Nasr TH. Bilateral central lymph node dissection with thyroidectomy for papillary thyroid cancer. Menoufia Med J 2015;28:43-8

How to cite this URL:
El-Kased AF, El-Foll HA, El-Gammal AS, Abu El-Nasr TH. Bilateral central lymph node dissection with thyroidectomy for papillary thyroid cancer. Menoufia Med J [serial online] 2015 [cited 2019 Jun 27];28:43-8. Available from: http://www.mmj.eg.net/text.asp?2015/28/1/43/155938


  Introduction Top


Thyroid cancer accounts for ~1% of all malignancies in developed countries, with an estimated annual incidence of 122 000 cases worldwide [1]. In Egypt, it represents 2.2% of total cancers. It constitutes 30% of endocrine malignancies and 12-49% of head and neck tumors. Most cases occur between 25 and 65 years of age, but it can also occur in very young patients and in elderly patients [2,3]. Papillary thyroid cancer (PTC) is the most common histologic subtype, accounting for 80% of cancer [4] and more than 90% of differentiated thyroid cancer [5]. PTC shows mild biological behavior and has an excellent prognosis. Adequate management leads to a survival rate of excess of 90%. Death because of PTC is very rare [6]. However, cervical lymph node metastases are frequent, occurring in 30-80% of patients with PTC [7]. Lymph node metastases are associated with a significant probability for locoregional recurrence of the disease, even in low-risk patients. As a result, a rapid shift in patient care from a focus on overall survival to a focus on recurrence-free survival has been noted recently. These considerations led to renewed controversy on the role and the extent of lymphadenectomy at the time of thyroidectomy [8]. The central compartment of the neck, also known as level VI, is most frequently involved [9]. Many patients present with subclinical nodal disease that is not detectable by ultrasonography or physical examination [7]. Clinical examination may detect lymph node involvement in 15-30% of patients [10]. It is widely accepted that current surgical therapy for PTC should include total thyroidectomy and therapeutic central neck dissection in those patients who present with clinically evident positive lymph nodes [7]. The management of level VI lymph nodes is even less clear. There are multiple conflicting studies in this area. For example, some studies show that positive lymph nodes have no effect on recurrence or survival, whereas other studies show that nodal metastases are risk factors for increased disease-specific mortality, local recurrence, and distant metastatic spread [11]. This debate may be because of the lack of hard proof of its potential benefits and the increased rate of complications associated with the procedure [12]. Current recommendations range from selective dissection for high-risk patients to unilateral dissection to routine bilateral dissection [13]. Despite the high incidence of cervical lymph node metastases in PTC, the reported rates of locoregional recurrence range between 3 and 30% for low-risk PTC [14]. Even for high-risk cases, the rates are only 59%, often in patients with evidence of macroscopically involved nodes [15]. The surgeon should recognize that local nodal recurrence is a significant problem for patients, associated with a poor prognosis and high morbidity and mortality rates, usually because of invasion of the trachea or the great vessels or recurrent laryngeal nerve involvement [15]. Reoperation is a traumatic event and may be associated with unacceptably high complication rates, such as injury to the recurrent laryngeal nerve, hypoparathyroidism, and unsightly surgical scars [16]. In selecting the optimal management, an in-depth understanding of the biological behavior of cervical lymph node metastases is required. Ideally, surgical treatment should be radical enough to achieve complete eradication of the disease, while, at the same time, minimizing treatment-related and disease-related morbidity. Routine total thyroidectomy with central lymph node dissection (CLND) would be the ideal operation theoretically. However, this surgical approach may represent overtreatment in a large percentage of patients [6]. The aim of this study is to evaluate the frequency and pattern of central neck lymph node metastasis in PTC and its relation to lateral neck lymph node metastasis. Also, this study aims to evaluate the complications of central neck dissection.


  Patients and methods Top


A total of 30 unselected patients with PTC were treated in Menoufia University from 2011 to 2013; all were treated for curative intent. Approval for this research was obtained from the ethical committee at the Faculty of Medicine, Menoufia University. Also, informed consents were obtained from all patients who participated in this research. The study included seven men and 23 women. Their age ranged from 21 to 68 years at initial treatment. All patients underwent a thorough clinical examination and neck ultrasound. All patients were diagnosed with PTC by FNAC or by frozen section biopsy during surgery. Patients with nonpapillary cancer, recurrent disease, and distant metastasis were excluded from this study. All patients underwent total thyroidectomy, pretracheal, prelaryngeal (Delphian), and bilateral paratracheal lymph node dissection. Then, the specimens were sent for frozen section histopathology examination. If the lymph nodes were positive in the frozen section, we proceeded to ipsilateral lateral neck lymph node dissection. The central compartment was limited by the hyoid bone superiorly, the innominate vein inferiorly, the carotid sheaths both sides laterally, and the prevertebral fascia dorsally, and was divided into three node sites: pretracheal and prelaryngeal lymph nodes, ipsilateral paratracheal lymph nodes, and contralateral paratracheal lymph nodes. We defined the pretracheal, prelaryngeal, and ipsilateral paratracheal lymph nodes as the ipsilateral central compartment and contralateral paratracheal lymph nodes as the contralateral central compartment, in accordance with the proposed definition of laterality by Esnaola et al. [16]. The CLND was extended superior to the hyoid bone, inferior to the innominate vein, lateral to the carotid sheaths, and dorsal to the prevertebral fascia. The specimens were evaluated pathologically with the thyroid gland. The frequency and pattern of lymph node metastasis in the central compartment were analyzed and interpreted. Postoperative hypocalcaemia and recurrent laryngeal nerve injury were also evaluated. Postoperative hypocalcaemia was defined as at least one event of hypocalcemia symptoms (perioral numbness, or paresthesia of the hands and feet) or at least one event of biochemical hypocalcemia (ionized Ca level <1.0 mmol/l or total Ca level <8.0 mg/dl). Ionized Ca level and/or total Ca level were checked at follow-up. Permanent hypocalcemia was defined as persistent symptoms or persistent biochemical hypocalcemia for more than 6 months. Postoperative recurrent laryngeal nerve palsy was also investigated. Vocal fold mobility was evaluated by routine laryngoscopy immediately after thyroidectomy. Patients with postoperative vocal fold palsy were examined using a laryngoscope at every follow-up.

Statistical analysis

Data were analyzed using IBM SPSS Advanced Statistics (version 20.0; SPSS Inc., Chicago, Illinois, USA). The c2 -test (Fisher's exact test) was used to examine the relation between qualitative variables. A P value of less than 0.05 was considered significant.


  Results Top


The study involved 30 patients with thyroid cancer. The mean age of the studied group was 45.9 ± 11.7 years. Their age ranged from 21 to 68 years. The majority of patients were women (23 cases, 76.7%). [Table 1] shows the tumor characteristics. Bilateral tumors were found in five (16.7%) cases and eight (26.7%) patients had multiple masses. Seventy-percent of the tumors were grade II. Extracapsular invasion was found in five (16.7%) cases, whereas extrathyroid extension was found in 17 (56.7%) patients. The median diameter of the largest mass was 2.8 cm, ranging from 0.8 to 5.5 cm. In eight (26.7%) patients, clinically palpable lymph nodes were detected. During CLND, the median number of dissected nodes was 14 (range 9-22). Positive central nodes were found in 12 (40%) cases. The median number of positive nodes in these cases was six (range 3-11). Contralateral central nodes were positive only in four (13.3%) cases; all of these cases had ipsilateral positive nodes [Table 2]. During lateral neck dissection of the 12 cases with positive central nodes, positive lateral nodes were found only in two (16.7%) cases; one patient had four and the other had five positive nodes, and the median number of dissected nodes was 22 (range 18-28). We found that five (16.7%) cases had temporary hypocalcemia and only two cases had permanent hypocalcemia. Also, temporary vocal cord dysfunction was found in only two (6.7%) cases.
Table 1: Characteristics of the tumors studied

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Table 2: Central lymph node dissection fi ndings in the group studied

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Ipsilateral central lymph node involvement was not associated significantly with the patients' sex (P = 0.392). However, there was apparently higher lymph node involvement in men. It was found in 57.1% of men and 34.8% of women.

Ipsilateral central lymph node involvement was absent in grade I tumors. In contrast, 83.3% of the six grade III tumors were associated with ipsilateral central lymph node involvement. In addition, 33.3% of grade II tumors had ipsilateral central lymph node involvement [Table 3]. Statistical comparison between grade II and III cases only showed a positive association of higher grade with ipsilateral central lymph node involvement (P = 0.043).
Table 3: Relation between tumor grade and ipsilateral central lymph node involvement

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Ipsilateral central lymph node involvement was associated significantly with thyroid capsule invasion of the tumor [Table 4]. The five tumors with thyroid capsule invasion had positive ipsilateral central lymph nodes. About 30% of tumors with no thyroid capsule invasion had positive ipsilateral central lymph nodes (P = 0.006).
Table 4: Relation between thyroid capsule invasion of the tumor and ipsilateral central lymph node involvement

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Ipsilateral central lymph node involvement was apparently more common among patients with clinically positive nodes. Five (62.5%) tumors with clinically positive nodes had positive ipsilateral central lymph nodes compared with seven (31.8%) of patients with negative nodes. However, the difference was not statistically significant (P = 0.210).

Ipsilateral central lymph nodes involvement was apparently more common among patients with multiple tumors. Five (62.5%) patients with multiple tumors had positive ipsilateral central lymph nodes compared with seven (31.8%) patients with a single tumor. However, the difference was not statistically significant (P = 0.210) [Table 5].


  Discussion Top


The rationale for introducing CLND in PTC was similar to that emphasized for treating medullary carcinoma of the thyroid gland: preventing local recurrences in the central compartment where reoperation is difficult and, eventually, reducing the mortality rate particularly in high-risk patients [6]. Most of the literature has reported the pattern of cervical lymph nodal metastasis without separation of the ipsilateral or the contralateral central compartment in PTC patients [17]. Although CLND appears to have no impact on the survival of the patients, its omission may be associated with locoregional recurrence rates, which may have a negative impact on patients' quality of life [6].

The current study showed that 40% (12/30) of patients had lymph node metastasis; the central compartment was involved in all of them. This is similar to a study by Moo and Fahey [7], who reported that central compartment lymph node metastases are found in 40-90% of cases. Even in papillary microcarcinoma, the rate of lymph node metastases has been reported to be 25-45% of cases. The ipsilateral central compartment was involved in all of them. This is different from a study by Pereira et al. [12], who reported in their study that the prevalence of nodal metastasis in the central compartment was 60%.

In our study, the ipsilateral central compartment lymph nodes were affected in all patients with metastatic lymphadenopathy (12/30). These results are in agreement with a study carried out by Wada et al. [18], who found ipsilateral central compartment nodal involvement in 36.3% of patients in a larger series (n = 259). Ipsilateral central lymph node metastasis was found in 73% of patients in a study by Koo et al. [17].

We found that associated contralateral central compartment lymph node metastases were present in four (13.3%) patients. Isolated contralateral central compartment lymph node metastasis was not found in our study. These results may be in agreement with the results of Machens et al. [19], who found that the rate of contralateral central compartment lymph node metastases for the primary and reoperative PTC was 5-31%. Wada et al. [18] reported in their study in 2003 that contralateral central lymph node metastasis was found in 18.9% of their patients. Also, 25% of patients were found to have contralateral lymph node metastases in a study by Sadowski et al. [11]. Koo et al. [17] reported a higher rate of contralateral central lymph node metastasis of 34%.

In our study, we found that all patients with metastatic contralateral central lymph nodes had metastatic ipsilateral central lymph node metastases (no skip metastases). This is different from the study of Sadowski et al. [11], who found that 5% of all patients undergoing bilateral CLND had positive contralateral lymph node metastases without evidence of spread to the ipsilateral central lymph nodes. The difference between our results and other results may be because of the small number of our patients.

Some investigators suggest that a CLND should be performed only selectively in high-risk patients, specifically those with large tumors (>1 cm) [18].

In our study, ipsilateral central lymph node involvement was apparently more common among patients with clinically positive nodes. Eight of 30 (26.7%) patients had macroscopic evidence or suspicion of node positivity (clinically positive), and a primary therapeutic lymphadenectomy was performed. Pathologic examination indicated true positive (pN+) in five of 30 (62.5%) and pN0 (false positive) in two patients. Gemsenjager et al. [20] found in their study that 26% (42/159) of patients had clinically positive nodes, of whom 41/159 (98%) proved to have pathologically positive nodes. Also, they found that 18% (29/159) of patients had clinically negative nodes, of whom 14% (4/29) had pathologically positive nodes (false negative) and 86% (25/29) had pathologically negative nodes.

In our study, the lateral compartment of the ipsilateral neck was dissected in 12 patients with positive central lymph nodes. Positive lateral nodes were found in only two (16.7) cases. No skip metastases were found in our study. Our results are different from those of a study by Vergez et al. [21], who found that 31% of patients had metastatic invasion of the central and lateral compartment lymph nodes and 14.5% had metastatic invasion to the central nodal compartment only, with no skip metastases. In a study by Wada et al. [22], it was found that 193 patients showed lymph node metastases in the neck. Among them, 42 (21.8%) had only central lymph node metastases compared with 10/12 (83.3%) patients in our study; they also found that 134 (69.4%) patients had both central and lateral lymph node metastases compared with 2/12 (16.7%) patients in our study. This difference between our study and their study may be because of the small number of patients we studied compared with the number of their patients. They also found that 17 (8.8%) patients had skip metastases. None of our patients had skip metastases because we only performed lateral lymph node dissection for cases with positive central lymph nodes.

The relationship between central and lateral lymph node metastases may provide an evidence base for clinical decision making on completion lymph node dissection in patients with central node-positive PTC, especially when cervical ultrasonography is not indicative of lymph node metastases in the lateral neck.

We found that the primary tumor size, patient age, or sex did not affect the frequency of lymph node metastases. Wang et al. [23] reported that factors such as patients' age and sex showed no significant difference in nodal metastasis. This means that the application of CLND should not be limited by patients' age or sex. These results are agreement with the results of Vegez et al. [21], who reported that patients' age, sex, and tumor size did not influence the risk of node invasion.

In our study, ipsilateral central lymph node involvement was absent in grade I tumors. In contrast, 83.3% of the six grade III tumors were associated with ipsilateral central lymph node involvement. In addition, 33.3% of grade II tumors had ipsilateral central lymph node involvement. Statistical comparison showed a positive association of higher grade with ipsilateral central lymph node involvement (P = 0.043).

Five out of 30 (16.7%) patients were found to have thyroid capsule invasion; all of them had lymph node metastasis. About 30% of tumors with no thyroid capsule invasion had positive ipsilateral central lymph nodes (P = 0.006). So et al. [24] found that thyroid capsule invasion was an independent predictor of subclinical central lymph node metastases. Wada et al. [22] found that central lymph node metastases showed a weak relation to thyroid capsule invasion, which is not in agreement with our results.

In our study, ipsilateral central lymph node involvement was apparently more common among patients with multiple tumors. Five (62.5%) patients with multiple tumors had positive ipsilateral central lymph nodes compared with seven (31.8%) patients with a single tumor. This result is similar to a result of a study carried out by Wang et al. [23], which showed that multifocality (P = 0.02) was significantly positively associated with central lymph node metastasis. Shi et al. [25] reported that the rate of nodal metastasis was higher in patients with multifocality than in those with a single lesion (P < 0.001). Univariate analysis showed multifocality as a significant risk factor for nodal metastases.

Lymph node dissection remains controversial in PTC. The current treatment is to complete the total thyroidectomy by radioiodine ablation without lymph node dissection in the absence of lymph nodes at ultrasound examination or during preoperative palpation. However, radioactive iodine treatment can be inefficient for some tumors without radioiodine uptake (25-30% of cases) [26]. It has been shown that neck lymph node metastases are present in 20-50% of cases, even if the tumor is small and located in the thyroid gland [27]. However, elective prophylactic lymph node dissection is controversial in the absence of a preoperative suspicion of lymph node involvement [8]. Therapeutic CLND decreases the frequency of locoregional recurrences, and lymph node invasion appears to be an independent variable affecting the prognosis of T1-T2 tumors [28].

In our study, five (16.7%) patients developed temporary hypocalcemia, two (6.7%) patients developed permanent hypocalcemia, and two (6.7%) patients developed temporary vocal cord dysfunction. Wang et al. [23] showed in their study that the incidence of postoperative complications was 5.3% (10/188); all of these were transient and there were no permanent complications, which included nine (4.8%) cases of hypocalcemia and one (0.53%) case of recurrent laryngeal nerve injury. In a study by So et al. [24], it was found that transient hypocalcemia, permanent hypocalcemia, and temporary vocal cord dysfunction developed in 27.6, 1.1, and 3.8% of patients, respectively.

Our results on temporary hypocalcemia are different from those of a recent study by Moo and Fahey [7], who found temporary hypocalcemia in 31% of patients in their series. These differences may be because of the small number of our patients.

Currently, an increasing number of studies support routine CLND in synchronization; some scholars even consider central lymph node as important as the primary tumor [29]. The significances lie in:

  1. Timely lymph node dissection can improve the cure rate in patients with clinically positive nodes
  2. Complete radical treatment of the primary tumor and CLND should be performed at one time
  3. During the first surgery, it has a clear anatomical structure, which enables thorough cleaning
  4. If lateral cervical lymph node metastasis is present.


CLND need not be performed later, which can reduce the damage to recurrent laryngeal nerve and parathyroid caused by an altered anatomical structure [23].


  Conclusion Top


CLND prevents nodal recurrence in the central compartment, which carries a high incidence of morbidity during surgery for this recurrence. In addition, CLND, in good hands, does not contribute to the morbidity of total thyroidectomy (hypoparathyroidism and recurrent laryngeal nerve injury). We propose that total thyroidectomy and bilateral CLND is the least-recommended surgical treatment. Also, in clinically negative lateral compartment lymph nodes, we conclude that lateral lymph node dissection is not important even if central lymph nodes were positive for metastases.


  Acknowledgements Top


Conflicts of interest

There are no conflicts of interest.

 
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