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Annals of Surgical Oncology 9:688-695 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

Mucoepidermoid Carcinoma of the Salivary Glands: Clinicopathologic Review of 108 Patients Treated at the National Cancer Institute of Milan

Marco Guzzo, MD, Salvatore Andreola, MD, Grazia Sirizzotti, BiolSc and Giulio Cantu, MD

From the Departments of Head and Neck Surgery (MG, GC) and Pathology (SA, GS), Istituto Nazionale per lo Studio e la Cura dei Tumori, Milan, Italy.

Correspondence: Address correspondence and reprint requests to: M. Guzzo, MD, Head and Neck Surgery Department, Istituto Nazionale per lo Studio e la Cura dei Tumori, Via Venezian, 1, 20133 Milan, Italy; Fax: 39-02-2390-371; E-mail: marco.guzzo1{at}tin.it


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Mucoepidermoid carcinoma (MEC) can have a variety of clinical outcomes, but prognosis seems to be related to the tumor grade. The system proposed by Auclair and Goode is useful, and our data lend further support to its application and validity in clinical practice.

Methods: We have clinicopathologically reviewed 108 cases of MEC originating in major (MASG) and minor (MISG) salivary glands that were treated at the National Cancer Institute of Milan between 1975 and 1995. Following the methods of Auclair and Goode, a quantitative grading system was used. The relationships between clinical and pathologic characteristics and survival rate were investigated.

Results: Twenty-six (44%) cases located in MASG and 19 (39%) cases in MISG were categorized as high-grade tumors. In patients with MASG tumors, the 5-year disease-free survival rate was 22.5% when the tumor was high grade and 97.0% if the tumor was low grade (P < .0001). For patients with a tumor of the MISG, the percentages were 35.3% for high-grade and 80.0% for low-grade tumors (P = .0066).

Conclusions: Our study confirms that in MEC, tumor grade, subdividing cases into low and high grade by using the criteria delineated by Auclair and Goode, correlates well with prognosis.

Key Words: Salivary gland cancer • Mucoepidermoid carcinoma • Therapy • Surgery


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
When the surveys performed in the United Kingdom are excluded, mucoepidermoid carcinoma (MEC) represents 29% to 34% of all carcinomas developing in the major (MASG) and minor (MISG) salivary glands.1–3 Data show that MEC is the most common malignant histotype in these sites.

MEC is well known to display a variety of biological behaviors and, consequently, a variable natural history. Many investigators have, therefore, tried to define histological features that have prognostic significance.4–8 Auclair et al.9 and Goode et al.10 have recently identified the histological characteristics of MEC which are predictive of patients’ outcome. These authors have proposed that an intracystic component of <20%, 4 or more mitotic figures in 10 high-power fields, and the presence of neural invasion, necrosis, and cellular anaplasia are distinctive features of high-grade tumors. From their findings they have developed a quantitative grading system based on allocating a point score for each feature identified. By using the system developed in these recent studies, we performed a clinicopathologic review 108 of cases of MEC that were treated at National Cancer Institute of Milan.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
One hundred thirty-one cases of salivary-gland MEC treated at our institute between 1975 and 1995 were reviewed. Twenty-three patients were excluded from this study: 2 patients because of the identification of distant metastases during diagnosis and 21 patients who had received previous treatment in other institutes. Thus, 108 new cases were considered in this study.

Complete clinical data were collected and classified by sex, age, tumor site and size, therapy, and patient outcome. All cases were histopathologically reviewed by a pathologist who was blinded with regard to the final outcome of the patients. All cases fulfilled the criteria proposed by the World Health Organization in 1991 for the diagnosis of salivary-gland MEC.11 Pathologic findings such as intracystic component, neural invasion, necrosis, mitosis, and anaplasia were evaluated, and a quantitative grading system was used that was based on allocation of points for each of the five features and subsequent assignment of low (score 0–4), intermediate (score 5–6), and high (score 7–14) grades (Table 1). Vascular invasion was also considered as an additional parameter.


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  		TABLE 1. Grading parameters and point values10
 
Clinical and histological findings were compared, and the Kaplan-Meier method13 was used to plot survival curves for each putative prognostic factor. The prognostic effect of a variable was tested with the log-rank test.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
General Characteristics
The study population comprised 64 men and 44 women aged between 13 and 85 years (average, 56 years). MASG and MISG were involved in 59 (54.6%) and 49 (45.4%) cases, respectively. Site distribution is listed in Table 2. Tumors were staged according to the International Union Against Cancer classification12 as listed in Table 3.


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  		TABLE 2. Site distribution of 108 cases of MEC
 

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  		TABLE 3. Stage grouping (UICC, 1997)
 
Grading Relationships
Eighty percent of women (35 of 44 cases) had a low-grade disease, whereas in men the prevalence of high- and low-grade disease was similar (36 and 28 cases, respectively). Twenty-six (44%) of the 59 cases in which the tumor was located in the MASG and 19 (39%) of 49 cases with a tumor of the MISG were classified as high-grade tumors. When the submaxillary gland was considered alone, three of four tumors fell in the high-grade category. The relationships between grading and tumor stage are listed in Table 4.


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  		TABLE 4. Relationship of grading by tumor T stage (UICC, 1997)
 
The percentage of patients with nodal involvement increased according to the tumor stage both in MASG and MISG (Tables 5 and 6). In MASG, 50% of the high-grade and 3% of the low-grade tumors had cervical metastases at diagnosis. In MISG, high-grade tumors presented with cervical metastases in 68% of cases, whereas in low-grade tumors they were in 20%.


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  		TABLE 5. Major salivary glands: relationship between tumor stages and nodal status at first presentation (UICC, 1997)
 

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  		TABLE 6. Minor salivary glands: relationship between tumor stage and nodal status at first presentation (UICC, 1997)
 
Therapy
The delay before first therapy averaged 9 months for tumors located in MISG and 26 months for those located in MASG. Two patients were first treated with radiotherapy (RT) alone, whereas 106 cases underwent surgery.

Surgery
Surgical treatments are listed in Table 7. Thirteen of the 50 parotidectomies performed resulted in the partial or complete sacrifice of the facial nerve. Eleven of these cases were high-grade tumors.


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  		TABLE 7. Surgical treatment of 106 cases
 
With the exception of one case (craniomaxillofacial resection), surgery of the primary tumor combined with neck dissection was performed consistently whenever cervical metastases were detected clinically. Elective (prophylactic) neck dissection was always undertaken if the T stage and site of occurrence made this appropriate. Fifteen elective neck dissections were performed: 7 of 45 cases in MASG and 8 of 29 cases in MISG. In the former group, three (43%) of seven were positive cases (all of them had a tumor stage of more than T1), whereas in the latter no micrometastases were found. Neck metastases were detected pathologically in all of the clinically positive cases.

In clinically N0 patients who had not undergone a neck dissection, cervical relapses were observed only in patients with high-grade tumors, both in MASG and in MISG. In particular, relapses occurred in three (38%) of eight cases in the former group and in the only one case of the latter group. The median time of recurrence was 15 and 13 months, respectively. Moreover, all of these patients had a tumor stage more advanced than T1.

Complete elimination of disease was achieved in 92 of the patients who received operations: 50 (85%) of 59 had a tumor of the MASG, and 42 (89%) of 47 had a tumor of the MISG. Fourteen patients had positive margins of resection (4 of these received preoperative RT): 11 (79%) of 14 were considered as high grade. When negative margins were found, only 33 (36%) of 92 cases displayed a high-grade tumor.

Vascular invasion was found in 20% (10 cases) of the MISG tumors; 4 cases were high grade, and the remaining 6 were low grade. In MASG, 10 cases (17%) presented with vascular invasion; 9 of these were considered as high-grade tumors.

Postoperative RT
Twenty-four (41%) patients with MASG tumors and 11 (23%) patients with MISG tumors received postoperative RT (35 patients; 33%). In the former group, high- and low-grade tumors accounted for 14 and 10 cases, respectively; there were 8 patients with microscopic residual disease and 16 with advanced disease. In the latter group, high- and low-grade tumors accounted for seven and four cases, respectively; two patients had microscopic residual disease, and nine had advanced locoregional disease.

Outcome
The patients’ average follow-up period was 139 months (range, 42–274 months) for tumors located in MASG and 88 months (range, 44–166 months) when tumors were located in MISG. None of the patients was lost to follow-up.

Three patients had tumor progression after their first treatment: two after surgery and one after RT. All died as a result of the disease.

Thirty-eight (36%) of 105 (3 cases were never free of disease) patients had recurrences (Table 8). There were 28 (62%) high-grade and 10 (16%) low-grade tumors.


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  		TABLE 8. Complete series: site of recurrence (n = 38)
 
Recurrences
Local relapses developed in 24 (63%) of 38 cases. Eight of these cases were low-grade tumors, and 16 were high-grade tumors. Distant metastases were found in five patients, four of whom had a high-grade tumor.

Locoregional recurrences without distant metastases occurred in 33 patients. Fourteen (42%) of these patients underwent salvage surgery. Eight of 14 patients had tumors in MASG; in 6 patients the tumor occurred in MISG. Eight patients were considered as having high-grade tumors and six as having low-grade tumors. After a 5-year follow-up period, six (43%) of the patients who received operations were free of disease, two of whom had high-grade disease and four of whom had low-grade disease. Sixteen of 33 patients received only symptomatic therapy because they were considered unsuitable for surgery (inoperable), had received RT before, or both. The remaining three patients were treated by RT alone, but none of them was ever rendered free of disease.

Survival
The 5- and 10-year overall survival rates of the series were 60.6% and 51.2%, respectively. The rate of disease-free survival (DFS) accounted for 65.4% after a 5-year period and 58.4% after a 10-year period. Five-year DFS was 72.9% and 66.8% for MASG and MISG, respectively (P = .2417).

Women had a 5-year DFS of 83.8%, whereas for men it was 52.2% (P = .0014). Histological grade was one of the factors that strongly influenced prognosis (Fig. 1). Five- and 10-year DFS varied from 22.8% to 88.9% and 22.6% to 78.8% in high- and low-grade tumors, respectively (P < .0001). Similar figures were obtained when grading was considered by site of occurrence (Figs. 2 and 3). Patients with a tumor in a MASG had a 5-year DFS of 22.5% when the tumor was high grade and 97.0% when it was low grade (P < .0001). Those patients with a neoplasm in a MISG had a 35.3% and 80.0% DFS for high- and low-grade tumors, respectively (P = .0066).



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  		FIG. 1. Whole series: disease-free survival by grading.

 


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  		FIG. 2. Major salivary glands: disease-free survival by grading.

 


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  		FIG. 3. Minor salivary glands: disease-free survival by grading.

 
Vascular infiltration does not seem to have any effect on survival rate; the 5-year DFS rates were 44.9% and 68.7%, respectively, whether infiltration was present or not (P = .1027). Tumor-node-metastasis staging influenced survival the most when the tumor was located in a MASG. The 5-year DFS was 87% in T1 (n = 23), 70% in T2 (n = 20), 40% in T3 (n = 8), and 20.8% in T4 (n = 11; P < .0001; Fig. 4). For tumors of a MISG, survival varied from 76.5% in T1 (n = 17) to 63.2% in T2 (n = 23) to 37.5% in T3 tumors (n = 8; P = .2021).



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  		FIG. 4. Major salivary glands: disease-free survival by T stage (tumor-node-metastasis system; International Union Against Cancer, 1997).

 
Patients without lymph node involvement at diagnosis (Fig. 5) had better survival rates (82.5% vs. 21.6%; P < .0001). Clinical staging consequently showed a strong effect on prognosis (Figs. 6 and 7). For tumors of MASG, the 5-year DFS rate was 82.9% combining stage I with stage II (n = 41) and was 21.3% combining stage III with stage IV (n = 18; P < .0001). Similar figures have been found for tumors of MISG, where combined stages I and II (n = 27) had an 88.6% DFS versus a 32.5% DFS for clinical stages III and IV (n = 22; P = .0009).



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  		FIG. 5. Whole series: disease-free survival by nodal involvement.

 


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  		FIG. 6. Major salivary glands: disease-free survival by staging: stage I and II versus III and IV.

 


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  		FIG. 7. Minor salivary glands: disease-free survival by staging: stage I and II versus III and IV.

 
Significant differences in survival rates were found depending on the nature of the resection margins. Those cases with clear margins had a 5-year DFS of 71.8%, whereas in cases with positive margins, the survival rate decreased to 28.6% (P = .0006; Fig. 8).



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  		FIG. 8. Patients who received operations (n = 106): disease-free survival by surgical margins.

 
Better clinical results (5-year DFS, 77.1%) have been obtained with surgery alone. Patients who underwent postoperative RT had a 5-year DFS rate of 48.8% (P = .0052). Two patients received RT alone: one had uncontrolled disease (nasopharynx), and the other developed local recurrence (larynx) and was successfully treated with surgery.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
MEC is well known to have various biological behaviors, and many investigators have consequently tried to identify histological grading criteria4–6 and clinical findings2 that have some prognostic importance. We believe that the system proposed by Auclair et al.9 and Goode et al.10 is useful, and this study lends further support to its validity.

Using the grading classification proposed in these studies, we clinicopathologically reviewed 108 cases of MEC. The relationship between clinical and pathologic features and survival rate was investigated with univariate statistical analyses.

However, in our experience, even if the same histological criteria were applied, only two tumor grades could be distinguished: high and low grade. Consequently, we found 39% and 44% high-grade tumors in MISG and MASG, respectively. Different figures have been reported by Goode et al.10 in MASG (13%) and by Auclair et al.9 in MISG (oral cavity alone, 7%). In these articles, even if high-grade and intermediate-grade tumors are combined, the total seems to be less than was found in our series (22% in MISG and 16% in MASG). Hicks et al.15 and Plambeck et al.16 reported data similar to ours; however, the histological grading criteria used by these authors were different from ours.

With respect to the age and the sites of MEC occurrence, our series confirms the data reported in the literature.2,5,9,14 In our study, women accounted for 40% of the cases, which is less than in other reports.2,6,16,17

In line with the findings of Clode et al.,14 we found 5- and 10-year overall survival rates of 60.6% and 51.2%, respectively. Hamper et al., 17 Plambeck et al., 16 and Auclair et al.9 reported survival results that were slightly better.

According to Hamper et al.17 and Hosokawa et al.,18 the 5- and 10-year DFS rates were 65.4% and 58.4%, respectively. Also, no differences in DFS were found when MASG and MISG were considered separately.

The tumor size seems to have an influence on prognosis (P = .0001) in MASG, but not in MISG, tumors. This could be due to the different prognoses related to the location of MISG tumors (oral cavity, 57%; oropharynx, 32.8%). In both MASG and MISG, the stage of disease seems to strongly influence survival, suggesting a crucial influence of nodal status.

Surgery was the main treatment in 106 patients, and parotidectomy (n = 50) was the most frequent surgical approach. It is of interest that in 13 of 50 parotidectomies, it was necessary to resect 1 nerve branch or more, and 11 of these cases were considered as having high-grade tumors. These figures are confirmed by other authors2 and seem to be related to the grade of the tumor.

The risk of nodal involvement seems to increase according to the stage of the tumor. In T2 tumors, cervical lymphadenopathies were found in 20% of the cases in MASG and 43% in MISG. These figures match the distribution of grading well across the T stages and seem to be consistent with the better outcome observed for patients with smaller tumors.

Neck dissection was always performed in combination with surgery of the primary tumor when cervical nodes were detected clinically in both MASG and MISG. All of these cases were found with metastatic disease in the neck during histological examination. Furthermore, in three (all high grade and more than T1 tumors) of seven patients with a tumor of the MASG who underwent elective neck dissection, occult lymph node involvement was confirmed. In patients with high-grade disease who did not undergo neck dissection, nodal recurrences were observed in three of eight patients with a MASG tumor more than T1. These results strongly suggest the need for neck dissection in those cases that are more than T1 with high-grade MEC of the MASG. This policy also seems to be supported by the high percentage of occult2 and clinically evident nodal metastasis reported by other authors.6,15,19,20

According to the literature,2,15 the 5-year DFS rate in MEC varies from 21.6% to 82.5% in cases with or without nodes detected clinically during diagnosis, but the figures seem to depend on grading. In both MASG and MISG, we also found that most patients with neck metastases had a high-grade MEC.

Vascular invasion showed a similar distribution both in tumors arising in MASG and in those originating in MISG, even though in the former group it seemed to be related to high-grade disease. In contrast with the findings of Nascimento et al.,5 this characteristic did not seem to influence survival rate.

Our experience, similar to that reported by Evans,6 suggests that positive margins are associated with high-grade disease and confirms the prognostic relevance of radical surgery.15,16,18 Local and locoregional recurrences were the most frequent causes of failure, and they seemed to be related to positive resection margins and high-grade tumors. According to the literature,2,4,6,10 no differences in recurrence have been found between MASG and MISG.

The high percentage (42%; n = 14) of salvage surgery is interesting. Forty-three percent (n = 6) of these patients were rendered free of disease, and four had low-grade tumors. These data suggest that locoregional recurrence should be re-treated with surgery, particularly in those cases involving-low grade disease.

MEC has been thought to be a radioresistant tumor, but recent articles suggest an increase in local control with adjunctive RT.18 Our data fail to demonstrate the role of RT, because it was given for unfavorable cases such as advanced locoregional disease, high-grade tumors, and tumors with positive margins of resection. We agree with others15 that this bias has led to misunderstanding of the real effectiveness of postoperative RT. Taking into account that positive margins and histological high grade indicate an increased risk of recurrence and eventually of bad prognosis, adjunctive RT in selected patients should always be considered.

Histological grading seems to have a strong effect on survival rate. The 5-year DFS dramatically decreased from 88.9% to 27.8% in low- and high-grade tumors, respectively (P < .0001). Similar figures are reported in the literature.2,5,14 Grading also affects prognosis when MASG and MISG tumors are considered separately. Moreover, grading seems to be associated with a better prognosis in women and in patients younger than 40 years. In fact, according to the literature,2,5,15,18 in the former group, low-grade tumors account for 80% of the cases, whereas in the latter they amount to 94%.

Tumor-node-metastasis grading currently represents the standard system for evaluating prognosis. Our data suggest that stage and grading are strictly correlated with each other.

Our experience demonstrates that subdivision of MECs into low and high grade by using the criteria delineated by Auclair et al.9 and Goode et al.10 correlates well with prognosis. This study also confirms the principle that neck dissection should be performed in cases of positive nodes and cases of tumor stages T2 to T4 in MASG MEC.


   Footnotes
 
We studied treatment results and grading relationships for mucoepidermoid carcinoma of the salivary glands.

Received for publication December 18, 2001. Accepted for publication April 10, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Spitz MR, Batsakis JG. Major salivary gland carcinoma. Descriptive epidemiology and survival of 498 patients. Arch Otolaryngol 1984; 110: 45–8.[Abstract]
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  3. Eveson JW, Cawson RA. A review of 2410 cases with particular reference to histological types, site age and sex distribution. J Pathol 1985; 146: 51–8.[CrossRef][Medline]
  4. Thordvalsson SE, Beahrs OH, Woolner LB, Simons JN. Mucoepidermoid tumors of the major salivary glands. Am J Surg 1978; 120: 432–8.
  5. Nascimento AG, Amaral LP, Prado LA, Kligerman J, Silveira TR. Mucoepidermoid carcinoma of salivary glands: a clinico-pathologic study of 46 cases. Head Neck Surg 1986; 8: 409–17.[Medline]
  6. Evans HL. Mucoepidermoid carcinoma of salivary glands: a study of 69 cases with special attention to histologic grading. Am J Clin Pathol 1984; 81: 696–701.[Medline]
  7. Suzuki M, Ichimya I, Matsushita F, Mogi G. Histological features and prognosis of patients with mucoepidermoid carcinoma of the parotid gland. J Laryngol Otol 1998; 112: 944–7.[Medline]
  8. Skalova A, Lehtonen H, von Boguslawsky K, Leivo I. Prognostic significance of cell proliferation in mucoepidermoid carcinomas of the salivary gland: clinicopathological study using MIB 1 antibody in paraffin sections. Hum Pathol 1994; 25: 929–35.[CrossRef][Medline]
  9. Auclair PL, Goode RK, Ellis GL. Mucoepidermoid carcinoma of intraoral salivary glands. Evaluation and application of grading criteria in 143 cases. Cancer 1992; 69: 2021–30.[CrossRef][Medline]
  10. Goode RK, Auclair PL, Ellis GL. Mucoepidermoid carcinoma of the major salivary glands. Clinical and histopathologic analysis of 234 cases with evaluation of grading criteria. Cancer 1998; 82: 1217–24.[CrossRef][Medline]
  11. Seifert G. Histological Typing of Salivary Gland Tumours. 2nd ed. Berlin: Springer Verlag, 1991.
  12. Sobin LH, Wittekind CH. International Union Against Cancer (UICC). TNM Classification of Malignant Tumours. 5th ed. New York: Wiley, 1997.
  13. Kaplan EL, Meier P. Nonparametric estimation from incomplete observations. J Am Stat Assoc 1958; 53: 457–81.[CrossRef]
  14. Clode AL, Fonseca I, Santos JR, Soares J. Mucoepidermoid carcinoma of salivary glands: a reappraisal of the influence of tumor differentiation on prognosis. J Surg Oncol 1991; 46: 100–6.[Medline]
  15. Hicks MJ, El-Naggar AK, Byers RM, Flaitz M, Luna MA, Batsakis JG. Prognostic factors in mucoepidermoid carcinomas of major salivary glands: a clinicopathologic and flow cytometric study. Eur J Cancer B Oral Oncol 1994; 30B: 329–34.
  16. Plambeck K, Friedrich RE, Hellner D, Donath K, Schmelzle R. Mucoepidermoid carcinoma of salivary gland: clinical data and follow-up in 52 patients. J Cancer Res Clin Oncol 1996; 122: 177–80.[Medline]
  17. Hamper K, Schimmelpenning H, Caselitz J, et al. Mucoepidermoid tumors of salivary glands. Correlation of cytophotometrical data and prognosis. Cancer 1989; 63: 708–17.[Medline]
  18. Hosokawa Y, Shirato H, Kagei K, et al. Role of radiotherapy for mucoepidermoid carcinoma of salivary gland. Oral Oncol 1999; 35: 105–11.[Medline]
  19. Jacobsson PA, Blanck C, Eneroth CM. Mucoepidermoid carcinoma of the parotid gland. Cancer 1968; 22: 111–24.[CrossRef][Medline]
  20. Olsen KD, Devine KD, Weiland LH. Mucoepidermoid carcinoma of the oral cavity. Otolaryngol Head Neck Surg 1981; 89: 783–91.[Medline]



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