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 Table of Contents  
ORIGINAL ARTICLE
Year : 2015  |  Volume : 11  |  Issue : 6  |  Page : 161-167

Squamous cell carcinoma of cervical lymph nodes from an unknown primary site: The impact of neck dissection


1 Department of Head and Neck Surgery, Zhejiang Cancer Hospital, Hangzhou, Zhejiang 310022, China
2 Department of Radiation Oncology, Zhejiang Cancer Hospital, Hangzhou, Zhejiang 310022, China

Date of Web Publication26-Oct-2015

Correspondence Address:
Liang Guo
Department of Head and Neck Surgery, Zhejiang Cancer Hospital, Hangzhou, Zhejiang 310022
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0973-1482.168178

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 > Abstract 

Objective: To investigate the treatment strategies of squamous cell carcinoma of cervical lymph nodes from an unknown primary site (SCCUP) and the value of neck dissection (ND).
Materials and Methods: The study included 133 patients referred to the Zhejiang Cancer Hospital from 2001 to 2012, with 109 males and 24 females. Distribution of patients by N status was as follows: N1 – 14 cases; N2a – 21 cases; N2b – 78 cases; N2c – 7 cases; and N3 – 13 cases. 104 patients underwent surgeries of ND while 29 patients underwent nonsurgical treatment. Among 104 patients, 24 underwent classic radical ND, 16 modified ND, 53 selective ND, and 11 extended ND. The selection of surgical strategy was determined by the extent and location of disease. According to the range of ND, 50 patients underwent ND for Levels I-V, 46 for Levels II-V, 4 for Levels I-III, 3 for Levels II-VI, and 1 for Levels I-VI. The data were analyzed with SPSS version 16.0. The differences between groups were calculated by χ2 tests. The actual overall survival (OS) rates were calculated by the Kaplan–Meier method. Different factors affecting the OS were determined by the log-rank test on univariate analysis. Cox regression was used to evaluate the multivariate analysis.
Results: The 5-year OS rate of the whole cohort was 67.1%; and the median survival time was 70.0 months. The 5-year OS of ND group and of the non-ND group were 71.3% and 53.2%, respectively (P = 0.061). Cox analysis indicated that N stage (P = 0.000), bilateral neck metastasis (P = 0.001), extracapsular spread (ES) (P = 0.016), and ND (P = 0.028) were independent prognostic factors for the OS of SCCUP. 25 patients (18.8%) had neck recurrence or residue. The locoregional failure rate of ND group and of the non-ND group were 13.5% and 37.9%, respectively (P = 0.003). Logistic regression analysis indicated that higher N stage was the main risk factor for locoregional failure (P = 0.015).
Conclusion: N stage, bilateral neck metastasis, ES, and ND were the main factors for the survival rate of SCCUP. N3 stage was the independent risk factor for locoregional failure. ND could significantly increase the locoregional control and may benefit the survival rate.

Keywords: Carcinoma, lymphatic metastasis, neoplasms, radical neck dissection, squamous cell, unknown primary


How to cite this article:
Lou J, Wang S, Wang K, Chen C, Zhao J, Guo L. Squamous cell carcinoma of cervical lymph nodes from an unknown primary site: The impact of neck dissection. J Can Res Ther 2015;11:161-7

How to cite this URL:
Lou J, Wang S, Wang K, Chen C, Zhao J, Guo L. Squamous cell carcinoma of cervical lymph nodes from an unknown primary site: The impact of neck dissection. J Can Res Ther [serial online] 2015 [cited 2017 Oct 21];11:161-7. Available from: http://www.cancerjournal.net/text.asp?2015/11/6/161/168178


 > Introduction Top


Cervical lymph nodes from an unknown primary site (CUP) represents 2–9% of head and neck cancers, with squamous cell histology constituting 53–77% of this kind of tumors.[1],[2],[3],[4] Squamous cell carcinoma of CUP (SCCUP) in the head and neck is defined as: (1) Being diagnosed as having squamous cell carcinoma of cervical lymph nodes by pathological testing or fine-needle aspiration (FNA); (2) without prior history of cancer or the excision of unknown tumor; (3) without multiple metastases outside the neck during the treatment; and (4) failure to identify the site of origin by various workups such as clinics, labs, imaging, and panendoscopy. As a result of the recent improvement in diagnostic procedures and imaging techniques, its number has decreased.[5] However, the therapeutic options of CUP remain controversial due to the lack of randomized clinical trials,[6] especially the indication of neck dissection (ND) and the extent of radiation. This study is a retrospective review of the clinical data and the follow-ups of 133 patients with SCCUP, treated at Zhejiang Cancer Hospital between 2001 and 2012. We mainly analyzed the clinical characteristics, treatment strategies, and prognosis of these patients to assess the treatment value and impact of ND in SCCUP patients.


 > Materials and Methods Top


Patient characteristics

Among the total of 133 patients, there were 109 males and 24 females. Their ages ranged from 19 to 77 years. The median age, when diagnosed, was 55 years. Left neck metastatic lymph node was involved in 76 patients, right neck in 50 patients, and bilateral neck in 7 patients. Level II was the most common site of the initial nodal involvement (77 patients), followed by Levels I, III, IV, and V in 15, 13, 12, and 2 patients, respectively. There were 14 patients whose site of nodal involvement could not be determined. All the patients underwent the examination of laryngoscopy, nasopharyngoscopy, and gastroscopy before they were treated in our hospital. Among the 133 patients, 26 cases underwent tonsil excision and biopsies of the oropharynx, 35 cases were performed with biopsies of the nasopharynx, while 11 cases were performed with biopsies of the hypopharynx. But the primary tumor site was not identified through panendoscopy. All the patients were examined with computed tomography and/or magnetic resonance imaging (MRI) of the neck in order to determine the extent of the disease, and computed tomography scan of the chest and abdomen at least to exclude the distant metastasis. Forty-eight patients had positron emission tomography examination, but the primary tumor site was not identified by imaging techniques. The Epstein–Barr virus (EBV) of the blood plasma was tested in 95 patients showing negative. Among all the patients in our study, 87 had undergone FNA of neck lymph node revealing squamous cell carcinoma; 46 had undergone biopsy and the histologic pathology of squamous cell carcinoma determined. Neck nodal staging was done according to the UICC on Cancer system for nodal disease in head and neck region (6th edition, 2002): N1 in 14 patients; N2a in 21; N2b in 78; N2c in 7; and N3 in 13. Extracapsular spread (ES) was detected in 36 patients. The pathologic grade was as follows: Grade I in 11 patients, Grade II in 36, and Grade III in 86.

Treatment methods

One hundred four patients underwent surgery of ND while 29 patients underwent nonsurgical treatment. Biopsy is not included in this kind of surgery. Among the former 104 patients, 46 cases underwent surgery only, 20 surgery plus chemoradiotherapy (CRT), 10 surgery plus radiotherapy (RT), 5 surgery plus chemotherapy (CT), 11 CRT followed by surgery, 10 inductive CT followed by surgery plus postoperative RT, and 2 inductive CT followed by surgery. Among the latter 29 patients, 13 cases underwent RT only, 11 CRT, 2 CT, and 3 biopsy of simply nodal excision [Table 1].
Table 1: Distribution of N stage in different treatment modalities (n)

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Surgery

Among 104 patients, 24 underwent classic radical ND (RND), 16 modified ND, 53 selective ND, and 11 extended ND. The selection of surgical strategy was determined by the extent and location of disease. According to the range of ND, 50 patients underwent ND for Levels I-V, 46 for Levels II-V, 4 for Levels I-III, 3 for Levels II-VI, and 1 for Levels I-VI.

Radiotherapy

Seventy-five patients underwent RT single or combined with other treatment. Radiation therapy was delivered using linear accelerator with 6–8 MV photons. All patients were delivered using a daily dose of 2 Gy per fraction, 5 days/week. The total effective dose is 50–80 Gy, the median dose is 60 Gy. 15 cases underwent bilateral neck irradiation and 23 ipsilateral neck irradiation. 37 cases underwent extensive-field irradiation. Extensive field irradiation selectively includes oral cavity, Waldeyer's ring lymph node, oropharynx, nasopharynx, hypopharynx, larynx, and bilateral neck according to the location of metastatic cervical lymph nodes.

Chemotherapy and other treatment

Fifty-three patients underwent CT including systemic CT, thermo CT, and artery infusion CT. CT regimen is based on the cisplatin plus 5-fluorouracil. Cycle ranges from 1 to 5, and mean is 2.8 cycles. Five received nimotuzumab injection targeted therapy, four received artery infusion CT, and two thermo CT.

Follow-up and statistical analysis

Patients were followed-up at regular interval. Follow-up were completed by telephone calls, letters, and out-patient review. The survival/locoregional control was measured from the date of diagnosis to the last day of follow-up or to death/relapse. Data were analyzed with SPSS version 16.0 (SPSS Inc., Chicago, IL, USA). The differences between groups were calculated by χ2 tests. The actual overall survival (OS) rates were calculated by the Kaplan–Meier method. Different factors affecting the OS were determined by the log-rank test on univariate analysis. Cox regression was used to evaluate the multivariate analysis. A P ≤ 0.05 was considered as significant.


 > Results Top


Up to June 2014, the median follow-up time was 39 months, with the range of 6 to 120 months. Six patients were lost to follow-up, and the rate of follow-up was 95.5%. Lost to follow-up cases were as a sectional tail in data processing.

Survival analysis

At the time of this analysis, 91 of 133 patients were alive, 36 died, and 6 lost to follow-up. The causes of 36 deaths are as follows: 20 cases died of neck recurrence or residue, 6 of the primary tumor, 2 of distant metastasis, and 8 of other reasons. Kaplan–Meier survival analysis indicated that the total 5-year actuarial OS rate was 67.1%. The median survival time (MST) was 70 months [Figure 1]. Univariate analysis showed that age, N staging of the lymph nodes, bilateral lymphatic metastasis, and ES were significant factors affecting the survival rate [Table 2]. The 5-year survival rate of ND group and the non-ND group was 71.3% and 53.2%, respectively (P = 0.061). Cox analysis indicated that nodal stage (P = 0.000), bilateral neck lymphatic metastasis (P = 0.001), ES (P = 0.016), and ND (P = 0.028) were the main independent prognostic factors for the survival of SCCUP [Table 3].
Figure 1: Kaplan–Meier survival curve for the 133 squamous cell carcinoma of cervical lymph nodes from an unknown primary site patients

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Table 2: The univariate factor analysis for the survival of 133 SCCUP patients

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Table 3: Cox analysis for the survival rate of 133 cases of SCCUP patients

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Local control

18.8% (25/133) of the whole cohort had neck recurrence or residue. Among the 25 patients, 16 had ipsilateral neck recurrence, 2 had contra lateral neck recurrence, and 7 cases had lymph node residue. The relapse time was 3 to 50 months (median time was 14 months). Univariated analysis showed N staging of the lymph nodes, pathological grading, ES, ND, and the combined treatment of surgery and RT were significant factors affecting the relapse or failure rate [Table 4]. The recurrence and residue rate of ND group and the non-ND group was 13.5% (14/104) and 37.9% (11/29), respectively (P = 0.003). Logistic regression indicated that higher N stage was the sole risk factor for neck recurrence or residue (P = 0.015) [Table 5].
Table 4: Univariate analysis for the neck recurrence or failure of control

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Table 5: Logistic regression analysis for neck recurrence or failure of control

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Distant metastasis

Five patients (3.8%) developed distant metastasis. The median time of developing into distant metastasis was 12 months, ranged from 3 to 32 months after treatment. The most common site of the metastasis was lung (3 patients), followed by bone and liver (1 patient) and mediastinal lymph node regions (1 patient). At the time when the follow-up was over, 2 died, and 3 were still alive with the tumor.

Appearance of the primary tumor

In our study, 21.8% (29/133) of patients had been found the primary tumor within 3 to 96 months after treatment (median time was 15 months). Primary tumor was found in only (10.8%) 4 out of 37 patients who irradiated by extensive-field while in (26.0%) 25 out of 96 patients who were not administered with enlarged-field irradiation therapy; that indicate the appearance rate of primary tumor site in the group with enlarged-field therapy was lower (χ2 = 3.634, P = 0.057). The characteristics of these patients as well as the primary site, the salvage treatment, and the initial treatment are presented in [Table 6].
Table 6: Appearance of primary tumor site

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 > Discussion Top


CUP is a special type of tumor. According to the mechanism of tumor spread and metastasis, all metastases should have a primary tumor. The reasons why it is difficult to detect the primary tumor site may be as follows: The primary tumor site is hidden, or the microenvironment in which the primary tumor makes it grow so slowly that it cannot be detected by existing diagnostic technique; the primary tumor may be eliminated by the immune system, or wiped out during the treatment of ND and RT; the patient dies before the primary tumor site is detected.[7] With the improvement of diagnostic techniques, the incidence of the CUP has decreased and accounted for approximately 3% of head and neck malignancies.[5]

CUPs mainly are squamous cell carcinomas. The diagnostic approaches of SCCUPs were proposed not only including physical examination, modern imaging, and panendoscopy, but also surgical biopsy (such as tonsillectomy), molecular profiling of an FNA sample for human papillomavirus and/or EBV.[5] The most common primary tumors are in the nasopharynx, then tonsils, the base of tongue, and hypopharynx according to most China literature. Of the 133 patients of SCCUP, 29 (21.8%) primary tumor sites were detected during follow-up. 10 (7.5%) were detected in the nasopharynx, 9 (6.8%) in hypopharynx and larynx, 6 (4.5%) in the oropharynx. Because of the high incidence rate of nasopharyngeal carcinoma among Chinese, EBV testing, nasopharynx MRI and the random biopsy by the nasopharyngoscopy were recommended in the process of diagnosis. Since the detection and incidence rate of oropharynx primary tumor especially tonsil carcinoma are relatively lower in Chinese population, the function of regular Western practice such as tonsillectomy needs further studied in oriented population.

The treatment of CUP includes the treatment of cervical lymph node metastasis and potential primary tumor. Owing to the lack of randomized trials, a standard therapy model has not been identified yet. Although ND followed by postoperative RT is the most generally accepted approach, other curative options such as ND alone, nodal excision followed by postoperative RT or RT alone can be used in some patients.[8],[9] Most scholars suggest that individualized comprehensive treatment plan be made according to the site of lymphatic metastasis, N stage, and pathological type.[8],[9],[10] ND is effective to the control of cervical lymph nodes of most patients of CUP, and maybe possible to prolong patient's survival.[11] However, it cannot eliminate primary tumor in general. RT is significant to local control, the reservation of the functions, the cancellation of both cervical lymph metastasis and contralateral subclinical foci, and the extinction of possible hidden primary tumor. Appropriate extensive field RT should cover the oral cavity, Waldeyer's ring, oropharynx, nasopharynx, larynx, hypopharynx, or bilateral neck totally or selectively according to the post-ND nodal stage and location of cervical lymphatic metastasis; while RT to neck only is also feasible in selective patients. Patel et al.[12] reported a study of 70 patients of SCCUP: 10 patients received single ND, while the other 60 patients received surgery and adjuvant postoperative RT. The study suggested that the combination of surgery and RT be benefit for patients with ES and pN2/N3. Shoushtari et al.[13] also reported that for those patients with T0N1 or nonbulky T0N2a disease with no ES, the combination of intensity modulated RT (IMRT) and ND was effective to control lymph node and improve the OS, with tolerant toxicity. However, there still remain controversies on the benefit and toxicity of the extensive RT and concurrent CT.[14],[15],[16],[17]

Of the 133 patients in our study, 104 (78.2%) patients underwent ND. Among them, 69 patients underwent modified or selective ND. On the premise of the integrity of radical surgery, we should retain jugular vein, sternocleidomastoid, accessory nerve, and/or other tissues as possible as we could in order to improve patients' quality of life. Since Level I or V has relatively lower lymph node metastasis, selective ND might be considered as an option to facilitate preservation of the submandibular gland and accessory nerve without compromising oncological outcome in patients without preoperative evidence of disease in Levels I or V.[18] However, to those who had extensive metastasis of multiple lymph nodes and tumor invasive to adjacent tissues, the RND or even the extended RND should be operated to enhance the locoregional control rate. For SCCUP patients, ipsilateral ND was usually performed. Bilateral ND was only used for those with bilateral lymphatic metastasis. Single neck lymph nodes biopsy is not recommended for the unknown cervical tumor. Even if a biopsy is really needed, we should use frozen section with the preparation for ND simultaneously.

In our study, 75 patients received RT. Among them, 40 received RT after surgery. 37 received extensive field RT, 15 received bilateral neck RT, and 23 had ipsilateral neck RT. The indications of neck RT after surgery were all the patients with N3 and part of the patients with N2, patients who had metastatic cervical nodes with poor differentiation, extensive metastases, ES, or solely biopsy. The extension of RT depends on the pathological type of tumor, the location of cervical lymphatic metastasis and the suspected sites of the primary tumor. Toxicity of the extensive field RT, the possibility of treatment risk and complication and patients' general conditions should be considered before making the choice.

In our study, 53 patients were administered with CT at different stages of treatment. The main indications of CT were the patients who have good performance status with N3 stage and part of N2 stage who had extensive lymph node metastasis, ES, or positive/risky margin.

According to reports in the recent literature, the main factors affecting the prognosis contain N stage, location, pathological characteristics, and treatment strategies of the lymphatic metastasis.[13],[16] The recurrence or residue of the cervical lymphatic metastasis was the main cause of treatment failure and the death of the patients. Patel et al.[12] reported that disease-specific survival and OS rate at 5 years were 62% and 56%, respectively. The 5-year control rates were 84% in the ipsilateral (dissected) neck and 93% in the contralateral (undissected) neck. Primary tumor sites subsequently emerged in 8 patients (11%). Lu et al.[14] reported that the 5-year OS rate of 60 SCCUP patients was 68.5%, and N stage was the main factor affecting the survival rate (P = 0.032). The emergence of the occult primary was observed in 21.2% of these patients after treatment.

Of the 133 SCCUP patients in this study, the 5-year OS was 67.1%. The MST was 70 months, which was similar to other literature from China. Cox analysis indicated that N stage, bilateral lymphatic metastasis, ES, and ND were the independent factors for the survival rate of SCCUP. Logistic regression indicated N3 stage was the independent risky factor for the nodal recurrence or residue. In the cases we reviewed, 25 (18.8%) had neck recurrence or residue, while the rate of recurrence after ND group is 13.5% only, which proved that ND was effective to treat SCCUP.

The emergence of the occult primary was observed in 21.8% of patients after treatment in our study which was similar to Lu et al.[14] reported, but higher than what other literature reported.[19],[20] The emergence of occult primary among those who had extensive field irradiation was 10.8%, which was significantly lower than the total emergence rate of primary tumor site (P = 0.057). Eldeeb and Hamed.[20] reviewed 40 patients treated with CRT as a curative approach, emergence of the occult primary was very limited (1 patient only), which suggest that extensive irradiation of both sides of the neck and pharyngeal mucosa with concurrent CT results in a lower emergence of primary tumor, and an attempt at cure should always be made. However, the toxic side effect of extensive field irradiation could not be neglected. It could affect the further treatment after the emergence of primary tumor site and be difficult to deliver the radiation dose in the re-irradiation situation, or for healing of the wound after surgery. Therefore, we should be cautious to make the clinic practice. IMRT can reduce the toxic side effect of RT, and has been widely used in the treatment of head and neck squamous cell carcinoma. However, it was difficult to set the target region for suspected sites of SCCUP. In our study, neck recurrence or residue was the main cause of death, while the appearance of the primary tumor may not affect OS given by salvaged treatment. Therefore, whether to irradiate extensive field or neck only after ND of SCCUP is controversial.


 > Conclusion Top


Our series demonstrates that N stage, ES, and ND were the main factors affecting the survival rate of SCCUP. Higher N stage was the independently risky factor affecting the neck recurrence or failure of control. ND could lead to higher control rate of the cervical lymph node, and improve the survival rate of the patients.

Acknowledgments

This study is supported by the Natural Science Foundation of Zhejiang Province of China (grant no. LY12H16033) and Medical Scientific Research Foundation of Zhejiang Province of China (grant no. 2015 KYA036).

Financial support and sponsorship

This study is supported by the Natural Science Foundation of Zhejiang Province of China (grant no. LY12H16033) and Medical Scientific Research Foundation of Zhejiang Province of China (grant no. 2015 KYA036).

Conflicts of interest

There are no conflicts of interest.

 
 > References Top

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