Comparison of Partial Versus Superficial or Total Parotidectomy for Superficial T1-2 Primary Parotid Cancers
Article information
Abstract
Objectives.
This study aimed to compare the oncological outcomes of partial versus superficial or total parotidectomy for superficial T1 or T2 primary parotid cancers and investigate their prognostic factors and recurrence patterns.
Methods.
The medical records of 77 patients with T1–2 primary parotid malignancies between May 2003 and March 2022 were retrospectively reviewed. Univariate and multivariate analyses were performed to evaluate the prognostic factors associated with overall survival, disease-free survival, and local and distant recurrence.
Results.
The average follow-up duration was 70.2 months (range, 12–202 months). The 5-year overall and disease-free survival rates were 88.7% and 77.1%, respectively. Twenty-two patients underwent partial parotidectomy, and 55 underwent superficial or total parotidectomy. There were no significant differences in the disease recurrence (P=0.320) and mortality rates (P=0.884) of the partial and superficial or total parotidectomy groups. The mean duration of surgery was shorter and the overall complication rates were significantly lower in the partial group than in the superficial or total parotidectomy group (P=0.049). Sixteen cases of recurrence occurred during the study period (20.8%). Univariate analyses showed that high-grade tumors (P=0.006), lymphovascular invasion (P=0.046), and regional lymph node metastasis (P=0.010) were significant risk factors for disease recurrence. Multivariate analysis identified regional lymph node metastasis as an independent prognostic factor for disease recurrence (P=0.027), and lymphovascular invasion as an independent prognostic factor for overall survival (P=0.033).
Conclusion.
The conservative surgical approach of partial parotidectomy can yield oncological outcomes comparable to those of superficial or total parotidectomy with careful patient selection in T1-2 parotid cancers.
INTRODUCTION
Parotid cancer accounts for 1%–3% of head and neck tumors [1]. However, primary parotid cancer is rare and has diverse histological characteristics, which has led to varied perspectives on the appropriate surgical extent and indications for adjuvant therapy for parotid cancer. Generally, the surgical extent is based on the extent of the tumor and the invasion of the surrounding structures, and various ranges of parotidectomy can be performed.
Parotidectomy is classified based on the range of excised parotid tissue and is a relatively standardized technique for facial nerve dissection. Total parotidectomy involves the removal of the entire parotid tissue, whereas superficial parotidectomy refers to the complete removal of the parotid tissue that lies superficial to the facial nerve. Partial parotidectomy involves the partial excision of the superficial lobe of the parotid gland, including the tumor and surrounding normal tissues [2].
Conservative partial parotidectomy has been reported to be effective for benign tumors of the parotid gland, as it requires shorter surgery and has lower morbidity, such as facial nerve injury, than superficial parotidectomy, which requires full facial nerve dissection [3,4]. For high-grade or advanced-stage parotid cancer, a radical surgical strategy is preferred; however, for small tumors (T1–2) confined to the superficial lobe of the parotid gland, the efficacy of conservative partial parotidectomy remains unclear. Therefore, this study aimed to compare the clinical outcomes of partial parotidectomy and radical surgical treatment, including superficial or total parotidectomy, for the management of T1–2 primary parotid cancers.
MATERIALS AND METHODS
Study population and variables
The medical records of 77 patients with T1–2 primary parotid malignancies between May 2003 and March 2022 were reviewed retrospectively. Patients with tumor extension into the deep lobes, facial nerve invasion during surgery, or preoperative facial nerve palsy were excluded. Patients with incomplete medical records, those with no specific description of the surgical extent of the parotid gland, or those with a history of previous parotid gland treatment were also excluded. Clinical characteristics, including age, sex, tumor size, T stage, preoperative biopsy results, extent of surgery, duration of surgery, tumor histology, tumor pathological data (extracapsular extension, perineural invasion, lymphovascular invasion [LVI], and resection margin status), postoperative complications, and postoperative radiation therapy were analyzed. Partial excision of the superficial lobe of the parotid gland, including the tumor and surrounding normal tissues, was defined as partial parotidectomy. Total resection of all parotid tissues was defined as total parotidectomy, and complete removal of the superficial part of the parotid gland, which was defined as superficial parotidectomy, involved the full dissection of the facial nerve. According to the World Health Organization classification, the histologic grade of each cancer was classified as low/intermediate or high [5]. The pathological stages were evaluated according to the American Joint Committee on Cancer TNM staging system (8th edition) [6]. The overall survival was defined as the duration from the date of surgery to the date the patient died or was last known to be alive. Disease-free survival was defined as the duration from the date of surgery to the date of recurrence.
Approval for this study was obtained from the Institutional Review Board of Hallym University Dongtan Sacred Heart Hospital (No. 2022-07-005-002), and the requirement for informed consent was waived.
Statistical analysis
Fisher’s exact test and Pearson’s chi-square test were used to analyze categorical variables. Student t-test or the Wilcoxon rank-sum test was used to analyze the continuous and ranked variables, such as age, which were expressed as mean±standard deviation. Kaplan-Meier analyses were used to visualize the overall and disease-free survival rates. To assess the differences between the survival curves, the log-rank test was used for each predictor and covariate. A multivariate Cox proportional hazards regression model was used to assess the prognostic factors for overall and disease-free survival. All data were analyzed using IBM SPSS ver. 25.0 (IBM Corp.). For all cases, a P-value of <0.05 was considered statistically significant.
RESULTS
Clinical and histopathological characteristics
Table 1 summarizes the clinical and histopathological characteristics of the patients included in this study. The grades were low or intermediate for 50 tumors (64.9%) and high for 27 tumors (35%). Histologically, mucoepidermoid carcinomas were the most common (n=30, 38.9%); four of them were high-grade cancers. Of the 69 tumors for which fine-needle aspiration cytology or core needle biopsy was performed preoperatively, 45 (65.2%) were malignant. The remaining 24 (34.8%) were benign or indeterminate and were unexpectedly diagnosed as parotid cancer based on postoperative pathology.
Clinical and histopathological characteristics of the parotid tumors (n=77)
Surgical extent of parotidectomy and neck dissection
Twenty-two patients (28.6%) underwent partial parotidectomy, and 55 (71.4%) underwent superficial or total parotidectomy. The total duration of partial parotidectomy, excluding the duration of neck dissection, was 143.2±80.0 minutes, which was significantly shorter than that of superficial or total parotidectomy, at 225.5±112.3 minutes (P=0.004). There was no significant difference in the resection margin positivity between the two groups (P=0.765). Postoperative facial nerve palsy occurred in 11 patients, and all but one patient recovered completely between 3 and 6 months after surgery. Frey syndrome occurred in six patients, and seroma occurred in six patients after surgery; however, they were cured spontaneously with repeated aspiration. The postoperative facial nerve palsy rate was lower in the partial group than in the superficial or total parotidectomy group (4.5% vs. 18.2%, P=0.122), although the difference was not significant. The complication rate was significantly lower in the partial group than for the superficial or total parotidectomy group (13.6% vs. 36.4%, P=0.049). There was no significant difference in disease recurrence or mortality between the partial and superficial or total parotidectomy groups (P=0.320 and P=0.884, respectively).
Neck dissection was performed for 47 patients. Therapeutic modified radical neck dissection was performed in nine patients with clinically positive nodes. Occult metastases developed in nine (23.7%) of 38 patients who underwent elective neck dissection. Among them, eight had high-grade tumors (38.1%, 8/21; P=0.020).
Survival rate and prognostic factors
The mean follow-up duration for all the patients was 70.2 months (range, 12–202 months). The 5-year overall and disease-free survival rates were 88.7% and 77.1%, respectively (Fig. 1). The univariate analyses showed that histological grade (P=0.006), LVI (P=0.046), and pathologic cervical lymph node metastasis (P=0.010) were significantly associated with disease recurrence. However, age, sex, tumor size, resection margin, and postoperative radiation therapy were not significantly associated with recurrence (Table 2). Multivariate analyses showed that pathologic cervical lymph node metastasis was significantly associated with disease recurrence (P=0.027) (Table 3). LVI (P<0.001) and age (P=0.017) were significantly associated with overall survival in the univariate analyses (Table 2). Only LVI was significantly associated with overall survival in the multivariate analyses (P= 0.003) (Table 3). Regarding the prognostic factors according to the recurrence patterns, histopathological grade (P=0.033) showed a significant association with local recurrence, and LVI (P=0.021) showed a significant association with distant metastasis (Fig. 2).
Survival curves of patients with T1-2 primary parotid cancers. (A) Overall survival rates. (B) Disease-free survival rates.
Results of univariate analysis for prognostic factors on disease-free survival and overall survival in T1-2 parotid gland cancer
Results of multivariate Cox regression analysis for prognostic factors on disease-free survival and overall survival in T1-2 parotid gland cancer
Survival curves of recurrence patterns. (A) Local recurrence-free survival rates according to the histopathological grade. (B) Distant metastasis-free survival rates according to lymphovascular invasion (LVI).
Recurrences and cause of death
Sixteen cases of recurrence occurred during the study period (20.8%). The mean duration from initial treatment to disease relapse was 27.6 months. Seven cases were high-grade (25.9%, 7/27), and nine were low-grade (18%, 9/50). There were six cases of local recurrence, four cases of regional recurrence, one case of loco-regional recurrence, and five cases of distant metastasis. Of the five patients with distant metastasis, four died due to disease progression during the study period.
DISCUSSION
The efficacy of partial parotidectomy has been reported in previous studies, including randomized clinical trials, mainly for the treatment of benign tumors [3,4]. Conservative partial parotidectomy has been reported to be advantageous for functional preservation of the facial nerve over complete superficial parotidectomy or total parotidectomy for malignant tumors of the parotid gland [7]. However, there has not yet been a randomized clinical trial on the oncological outcomes of partial parotidectomy, and comparative studies conducted under the same conditions have not yet been reported. Partial parotidectomy is acceptable for the treatment of superficial T1–2 low-grade parotid cancers because of the low recurrence rate after complete excision, similar to that of other benign salivary neoplasms [8]. Additionally, in cases where there are no adverse histopathological features, studies have suggested favorable oncological outcomes after complete tumor excision alone without adjuvant treatment, despite close surgical margins [9-11].
Until now, total parotidectomy has been preferred for the treatment of high-grade parotid cancer [12,13] because the rate of lymph node metastasis for high-grade parotid cancer is high. Additionally, the parotid gland is considered a lymphatic basin, and there are intraparotid lymph nodes in the deep lobe of the parotid gland to which tumors can metastasize. Therefore, total resection, including the deep lobe, is considered appropriate [14]. However, Lim et al. [15] reported favorable results of conservative parotidectomy in 43 patients with parotid gland cancer, including high-grade malignancies (37%, 16/43), with 5-year overall survival and disease-free rates of 88% and 79%, respectively. Furthermore, Park et al. [16] reported no significant differences in the treatment outcomes of patients who underwent and those who did not undergo total parotidectomy for T1–2 high-grade parotid gland cancers. Lee and Chuang [17] reported that, according to their analysis of the Surveillance, Epidemiology, and End Results Program database, total parotidectomy did not significantly increase disease-specific survival and overall survival relative to partial parotidectomy in early-stage adenoid cystic carcinoma. In this study, partial parotidectomy also showed no significant differences in recurrence and survival relative to superficial or total parotidectomy. The incidence of facial palsy was lower in the partial group than in the total or superficial parotidectomy group (4.5% vs. 18.2%). The rate of complications, including Frey syndrome, was also significantly lower for the partial group than for the total or superficial parotidectomy group.
In this study, patients who underwent extracapsular dissection (ECD) were excluded. ECD is a surgical technique that involves removing the tumor with a capsule and thin rim of surrounding glandular tissue, without planned facial nerve identification. Although it has been reported that there was no significant difference in survival or recurrence between ECD and superficial parotidectomy in unexpected malignancy cases misdiagnosed as a benign tumor before surgery, there are concerns about resection margin involvement or a close margin [18].
The comparable recurrence and survival rates of partial parotidectomy and superficial or total parotidectomy may be attributed to the role of adjuvant radiation therapy after surgery. In this study, nine of the 11 patients developed local or regional recurrence, even though their resection margins were negative. In contrast, all 16 patients with positive resection margins received radiation therapy after surgery, and only two of them showed loco-regional recurrence; therefore, postoperative radiation therapy appears to be effective for local control. In early-stage adenoid cystic carcinoma of the parotid gland, total parotidectomy did not show superior oncological outcomes over partial parotidectomy [17]. Postoperative radiation therapy is thought to have contributed to this, as it is mostly administered because of the characteristics of adenoid cystic carcinoma.
Even for high-grade parotid cancers with adverse features that are likely to metastasize to the intraparotid lymph nodes, the benefit of radical parotid surgery is diminished because the extent of postoperative radiation therapy includes the remaining parotid gland. Furthermore, if total parotidectomy is performed and adverse features are observed in postoperative pathology results, adjuvant radiation cannot be omitted. Additionally, determining the histological risk grade through preoperative biopsies or intraoperative frozen section pathology results is challenging. This study suggests that partial parotidectomy can be an acceptable surgical option for selected cases, including high-grade parotid cancer, if it is limited to the superficial lobe of the parotid gland and an appropriate surgical margin can be obtained.
Previous studies have reported that tumor grade, tumor size, histopathological adverse features, facial nerve invasion, and regional or distant metastasis affect the recurrence and survival rates of parotid cancer [19,20]. In this study, the histological grade, LVI, and regional metastasis were significantly associated with disease recurrence in the univariate analysis, but only regional metastasis was a significant factor for recurrence in the multivariate analysis. Therefore, neck node management is important for prognostication, even for early-stage parotid cancer. In terms of recurrence patterns, high histopathological grades were associated with local recurrence, and LVI was significantly associated with distant metastasis. Therefore, close observation of local recurrence along with postoperative radiotherapy should be considered for patients with high-grade tumors. Patients with evidence of LVI require careful follow-up for distant metastasis. Some reports have stated that adjuvant concurrent chemoradiotherapy had no survival benefit relative to adjuvant radiotherapy alone; however, additional research is needed on the application of systemic therapy for selected patients, such as those who are positive for LVI [21,22].
This study had some limitations; therefore, caution is required when generalizing our results. This was a retrospective study involving a relatively small sample of patients. Parotid cancer has a low prevalence and various histological characteristics, and it requires a long follow-up duration to observe recurrence. Several reports have compared the extent of surgery for the treatment of parotid cancer; however, this study is the first to compare less than superficial parotidectomy and superficial or total parotidectomy [16,17]. Although there has been no randomized trial, if data from settings similar to that of this study are reported and shared by multiple centers, subgroup analyses could be performed to establish clinical recommendations based on higher-quality evidence.
We compared the clinical outcomes of conservative partial parotidectomy with those of more aggressive superficial or total parotidectomy in patients with T1–2 primary parotid cancer limited to the superficial lobe of the parotid gland. With careful patient selection, the conservative approach of partial parotidectomy yielded oncological and clinical outcomes comparable to those of superficial or total parotidectomy. In clinical practice, approximately one-third of parotid malignancies are unexpectedly diagnosed after surgery. Additionally, determining the histopathological grade using frozen sections during surgery is challenging, and the diagnostic accuracy of malignancy is only approximately 70%. For these cases, it is not easy to opt for aggressive surgical ablation of the parotid gland as the initial treatment; therefore, the results of this study are valuable for decision-making regarding the treatment of early-stage primary parotid cancer. Adjuvant radiation therapy is recommended and active follow-up for recurrence is necessary when postoperative histopathology shows a high-grade cancer, positive resection margins, or LVI.
HIGHLIGHTS
▪ Partial parotidectomy may be a safe and effective alternative to superficial or total parotidectomy in patients with superficially located small primary parotid cancers.
▪ Partial parotidectomy has the potential to minimize surgical morbidity without compromising oncological outcomes.
▪ Regional lymph node metastasis was an independent prognostic factor for disease recurrence, and lymphovascular invasion was an independent prognostic factor for overall survival.
Notes
No potential conflict of interest relevant to this article was reported.
AUTHOR CONTRIBUTIONS
Conceptualization: SHH, ISP. Data curation: SHH, JL, JWK, HK, DJL, JHK. Formal analysis: SHH. Methodology: SHH, JL. Writing–original draft: SHH. Writing–review & editing: all authors.
Acknowledgements
This research was supported by Hallym University Research Fund (No. HURF-2022-28).