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Abstract

Objective

Parotid tumors are rare neoplasms in adults but are exceedingly infrequent in adolescents. We aimed to determine the clinical characteristics and outcomes of parotid tumors in adolescents under 20 years old.

Methods

Between 1999 and 2020, 979 cases of benign parotid tumors and 236 cases of malignant parotid tumors were treated surgically in our department. Of these, 12 benign cases (1.2%) and 9 malignant cases (3.8%) were in adolescents. There were no benign or malignant cases for those aged under 10 years.

Results

Regarding the histological type, all benign tumors were pleomorphic adenomas. About half of malignant tumors were mucoepidermoid carcinomas, and excluding one high-grade case, the grade of malignancy was all low/intermediate. The accuracy of fine-needle aspiration cytology among adolescents showed no significant difference with that of adults. In contrast to adults, adolescent benign tumor cases showed a markedly high rate of pleomorphic adenomas and no postoperative facial nerve palsy. Malignant tumors in adolescents had a different trend than adults; low/intermediate-grade malignancies were common and thus few symptoms/signs of malignancy could be observed. As well, the accuracy of fine-needle aspiration cytology was poor. All cases had a good prognosis and are disease-free survival.

Conclusion

Parotid tumors in adolescents are rare but have several characteristics that are distinct from adults. As long-term observation is required posttreatment in adolescent patients, recurrence in benign pleomorphic adenomas and poor long-term prognosis in malignant tumors, especially for those with low/intermediate-grade malignancy, are more likely to be observed.

Keywords

parotid tumor adolescents pleomorphic adenoma grade of malignancy

Introduction

Around 3–10% of all head and neck tumors occur in children, and about 5% of these are salivary gland tumors.^1,2 The majority (60–80%) of pediatric salivary gland tumors are benign and are generally pleomorphic adenomas.³ Among all pediatric malignancies, .5% are salivary gland tumors.⁴ Malignant salivary gland tumors are reported to be more common in children than in adults; the proportion of malignant salivary gland tumors is 25–50% in children compared with 15–25% in adults.⁵

Pleomorphic adenomas are known to recur despite their benign nature, with recurrence occurring in 1–4% for superficial parotidectomy and 40–50% for enucleations.⁶ Recurrent pleomorphic adenoma occurs a mean of 7 to 10 years after initial surgery, and long-term observation is required in pediatric cases. As such, the importance of definitive removal of the tumor has more relevance than in adults.⁷ Additionally, long-term observation cases are reported to have a higher risk of malignant transformation of pleomorphic adenomas.⁸ On the other hand, malignant tumors in children tend to have a lower grade of malignancy than in adults, with low/intermediate grades being the most common.⁹ The long-term prognosis is important for low/intermediate-grade malignant tumors because of the long time to recurrence. As long-term prognosis needs to be considered in children and adolescents, this leads to the issue of whether the intensity of treatment should be the same as in adults. In adults, postoperative radiotherapy is generally performed for advanced cancer and high-grade malignancies, but indications for adjuvant radiation treatment remain unclear for pediatric cases.

Thus, parotid tumors in children have somewhat distinct characteristics from those in their adult counterparts. Due to its low incidence, the accumulation of cases requires a long time. Reaching an accurate conclusion is also challenging unless the diagnosis and treatment strategies are consistent over the collection period. In our department, 979 cases of benign parotid tumors and 236 cases of malignant parotid tumors were treated in the past 21 years, and the diagnosis and treatment strategies have been consistent over this period. Here, we categorized patients under 20 years old as adolescents and examined their clinical characteristics to discuss issues that exist in pediatric cases.

Materials and Methods

Patients

We treated 1215 cases of parotid tumors in our department from September 1999 to December 2020, including 979 benign tumors and 236 malignant tumors. Adolescents were defined as aged under 20 years; there were 12 adolescent cases of benign tumors and 9 adolescent cases of malignant tumors. Benign tumors were included when the final pathology was confirmed by surgery. Inflammatory diseases of the parotid gland (such as lymphadenitis, granuloma, and Kimura’s disease) were excluded. Malignant tumor cases were included when the final pathology was able to be confirmed by surgery or incisional biopsy. Intraparotid metastatic lymph nodes were excluded. Histopathologically, benign tumors were all pleomorphic adenomas, and malignant tumors included 4 mucoepidermoid carcinomas, 2 each of adenoid cystic carcinoma and secretory carcinoma, and one malignant lymphoma. (Table 1). Lymphomas were only included the cases with solitary intra- or peri-parotid node swelling. ETV6-NTRK3 gene fusion analysis for 31 cases diagnosed with acinic cell carcinomas and secretory carcinomas by standard histological analyses were performed to determine each histological type.

Table 1.

Histological type of benign and malignant tumors (adults and adolescents) in the study population


Benign tumor
	≥20 n=967	<20 n=12
Pleomorphic adenoma	635	12
Warthin tumor	235	0
Basal cell adenoma	56	0
Other	41	0
Malignant tumor
	≥20 n=967	<20 n=12
Mucoepidermoid carcinoma	56	4
Carcinoma ex pleomorphic adenoma	30	0
Adenoid cystic carcinoma	23	2
Salivary duct carcinoma	22	0
Secretory carcinoma	14	2
Acinic cell carcinoma	15	0
Lymphoma	14	1
Basal cell carcinoma	11	0
Epithelial-myoepithelial carcinoma	11	0
Other	31	0

Methods

Benign and malignant tumors were compared in adolescents and adults. For benign tumors, we assessed age, sex, tumor diameter, tumor location, symptoms/signs, surgery, and postoperative facial nerve palsy in adolescent and adult patients. For malignant tumors, we assessed age, sex, symptoms/signs, grade of malignancy, preservation/sacrifice of facial nerves, lymph node metastasis, and outcome in adolescent and adult patients.

Fine-needle aspiration cytology (FNAC) was performed preoperatively, and the results were classified according to the Osaka Medical College (OMC) system.¹⁰ The OMC system classifies cytology results into 11 categories: the FNAC diagnosis (ie, OMC System) was evaluated in 979 benign tumors and 236 malignant tumors, and they were compared between adolescents and adults. Patient background, symptoms, pathology, treatment, and outcomes were examined for adolescent tumor cases for both benign tumors (12 cases) and malignant tumors (9 cases).

Statistical Analysis

The Mann–Whitney U test was used to compare differences between the 2 groups (adults and adolescents) because the following variables did not show a normal distribution: sex, tumor diameter, tumor location, symptoms/signs, operation time, bleeding volume, grade of malignancy, preservation/sacrifice of facial nerves, lymph node metastasis, and outcome. For all analyses, P <.05 was considered statistically significant.

Results

Comparison of Adolescent and Adult Cases

For benign tumors, adolescent cases differed from adults in that there was a higher number of male patients, no deep lobe tumors, and no cases of postoperative facial nerve palsy. However, due to the small sample size of adolescents, a significant difference was seen only for tumor location (P=.041). For malignant tumors, differences between adolescents and adults included a higher number of low/intermediate-grade malignant tumors, which also led to fewer symptoms/signs of malignancy, and the survival of all patients as the outcome. None of these differences were statistically significant due to the small sample size of adolescents (Table 2).

Table 2.

Patient demographics and presentation


Benign tumor
	≥20 n=967	<20 n=12	P value
Age, years	52.9	16.2
Sex, male:female	419:548	8:4	0.143
Tumor diameter, mm	26.1	26.6	0.887
Tumor location
Superficial:lower:deep	539:229:205	11:1:0	0.041
Pain/tenderness	71 (7.3%)	3 (25.0%)	0.056
Adhesion
Mobile:limited:fixed	884:76:7	11:1:0	1.000
Operation time, min	123.5	113.2	0.495
Bleeding volume, ml	22.1	12.9	0.237
Postoperative facial nerve palsy	205 (21.2%)	0 (0%)	0.082
Malignant tumor
	≥20 n=227	<20 n=9	P value
Age, years	57.1	16.4
Sex, male:female	125:102	5:4	1.000
Pain/tenderness	121 (53.3%)	3 (33.3%)	0.156
Adhesion
Mobile:limited:fixed	90:102:35	5:3:1	0.730
Facial nerve palsy	41 (18.1%)	0 (0%)	0.366
Grade, high:intermediate/low	94:133	1:8	0.885
Facial nerve
Preserve:partial sacrifice:total sacrifice	103:47:58	6:1:2	0.743
Lymph node metastasis	48/213 (22.5%)	2/8 (25.0%)	1.000
Outcome
Alive:recurrence:dead	163:13:48	9:0:0	0.331

Fine-Needle Aspiration Cytology (OMC Classification) in Adolescents and Adults

In adults with benign tumors, a diagnosis of benign histology was obtained by the OMC system (Category 4-1) in 741 (76.6%) of 967 patients. In adolescents, 11 (91.7%) of 12 patients resulted in a diagnosis of benign histology (all pleomorphic adenomas). Twelve (1.2%) adults were diagnosed as malignant (Category 6), but no adolescent benign cases were diagnosed as malignant.

In contrast, for malignant tumors, 132 (58.6%) of 225 adult patients were diagnosed as malignant by the OMC system (Category 6), while only 4 (44.4%) of 9 adolescent patients were diagnosed as malignant (Table 3).

Table 3.

Cytopathology results categorized by the Osaka Medical College (OMC) system after fine-needle aspiration cytology


Benign tumor
	≥20	<20
OMC category	n=967	n=12
1-1	107	0
1-2	7	0
2	19	0
3	12	0
4-1	741	11
4-2	44	0
5	25	1
6-1	3	0
6-2	4	0
6-4	5	0
Malignant tumor
	≥20	<20
OMC category	n=225	n=9
1-1	24	2
1-2	3	0
2	5	0
3	2	0
4-1	15	1
4-2	15	1
5	29	1
6-1	18	0
6-2	20	0
6-3	30	1
6-4	64	3

Adolescent Patients With Benign Tumors

Table 4 shows the characteristics of the 12 adolescent patients with benign tumors. All patients were aged between 12 and 19 years, and 8 were male and 4 were female. The duration of disease ranged from 1 month to 7 years, and there were 2 cases of recurrent pleomorphic adenoma. The tumors were all located in the superficial lobe except for 1 case in the lower pole. Extracapsular dissection (ECD) was performed for patients with recurrence (case no.1 and no.8), but otherwise, partial superficial parotidectomy (PSP) was performed. Including recurrent cases, there were no cases with transient postoperative facial nerve palsy.

Table 4.

Characteristics and treatment of benign parotid tumors in adolescents

#	Age	Sex	Duration of disease	FNAC	Final pathology	Operation	Operation time (min)	Bleeding volume (ml)	Location	Tumor diameter (mm)	Postoperative facial nerve palsy
1	12 17	F	3m Recurrence	pleomorphic adenoma pleomorphic adenoma	pleomorphic adenoma pleomorphic adenoma	PSP ECD	120 30	20 10	S S	23 12	—
2	12	F	1m	pleomorphic adenoma	pleomorphic adenoma	PSP	75	10	S	19	—
3	13	F	2m	pleomorphic adenoma	pleomorphic adenoma	PSP	110	10	L	30	—
4	13	M	1y	pleomorphic adenoma	pleomorphic adenoma	PSP	220	10	S	56	—
5	16	M	7y	pleomorphic adenoma	pleomorphic adenoma	PSP	93	10	S	25	—
6	17	M	2m	pleomorphic adenoma	pleomorphic adenoma	PSP	100	20	S	26	—
7	17	M	7m	pleomorphic adenoma	pleomorphic adenoma	PSP	140	10	S	20	—
8	17 20	M	3m Recurrence	pleomorphic adenoma pleomorphic adenoma	pleomorphic adenoma pleomorphic adenoma	PSP ECD	140 20	10 10	S S	27 10	—
9	18	M	1m	Indeterminate	pleomorphic adenoma	PSP	150	10	S	29	—
10	19	F	1y	pleomorphic adenoma	pleomorphic adenoma	PSP	95	10	S	25	—
11	19	M	2m	pleomorphic adenoma	pleomorphic adenoma	PSP	135	25	S	24	—
12	19	M	2y	pleomorphic adenoma	pleomorphic adenoma	PSP	100	10	S	32	—

F: female; M: male; m: month; y: year; ECD: extracapsular dissection; PSP: partial superficial parotidectomy; L: lower pole; S: superficial lobe;

Adolescent Patients With Malignant Tumors

Table 5 shows the characteristics of the 9 adolescent patients with malignant tumors. The patients were aged between 11 and 19 years, and 5 were male and 4 were female. The histological types were mucoepidermoid carcinoma in 4 cases, secretory carcinoma in 2 cases, adenoid cystic carcinoma in 2 cases, and malignant lymphoma in one case. All were low/intermediate-grade malignancies except for 1 high-grade case (mucoepidermoid carcinoma). Regarding symptoms/signs of malignancy, pain occurred in 3 cases and mobility restriction in 4 cases, but no facial nerve palsy was observed. The histological type was able to be confirmed by FNAC only for the high-grade mucoepidermoid carcinoma. Types of surgery included 4 cases of PSP, 2 cases of superficial parotidectomy, and 1 case each of subtotal parotidectomy and total parotidectomy. The facial nerve was preserved in 6 cases, partial sacrifice was conducted in 1 case, and total sacrifice in 2 cases. Postoperative radiotherapy was performed in 2 cases. The postoperative observation period ranged from 1 year to 20 years, and all are surviving to date without recurrence.

Table 5.

Characteristics and treatment of malignant parotid tumors in adolescents

#	Age	Sex	Duration disease	FNAC	Final pathology	T	N	Pain/tenderness	Facial nerve palsy	Adhesion	Operation (facial nerve)	pN positive	RT	Follow-up	Outcome
1	11	M	2M	ML	ML	2	0	−	−	mobile	OB (preserve)	−	−	1	alive
2	14	F	10y	Low	SC	2	0	−	−	mobile	SP (preserve)	−	−	11	alive
3	15	F	2y	pleomorphic adenoma	SC	2	0	+	−	mobile	PSP (preserve)	−	−	5	alive
4	17	M	1y	benign	MEC (low)	2	0	−	−	mobile	PSP (preserve)	−	+	20	alive
5	17	M	1y	benign	AdCC (inter.)	2	0	+	−	fixed	TP (TS)	−	+	2	alive
6	18	M	1m	MEC	MEC (high)	3	0	−	−	limited	STP (TS)	+	−	20	alive
7	19	F	10y	malignant	AdCC (inter.)	4a	0	+	−	limited	PSP (preserve)	−	−	5	alive
8	19	F	1m	inadequate	MEC (low)	2	0	−	−	limited	SP (PS)	−	−	16	alive
9	19	M	3y	benign	MEC (low)	4a	1	−	−	mobile	PSP (preserve)	+	−	4	alive

Discussion

In overseas reports summarizing a large number of cases, parotid tumors in children are reported as rare and occurring in only around 2%.^1,2 Moreover, when pediatric parotid tumors are categorized as children (<10 years old) and adolescents (10 to <20 years old), more than 90% occur among adolescents.² In the current study, both benign and malignant tumors were all seen in adolescents. Adolescent cases consisted of 12 (1.2%) of all 979 benign tumors. However, when limited to benign pleomorphic adenomas, adolescent cases made up 12 (1.9%) of 647 cases, indicating a slightly higher incidence than for overall benign tumors. In addition, there were no cases of Warthin tumor in those under 20 years old. In contrast, 9 (3.8%) of 236 patients were adolescents for malignant tumors, showing a proportion 3.1 times higher than benign tumors.⁵ When classified by the grade of malignancy, high-grade malignant tumors accounted for 40.3% of all malignant tumors, while only 1 case out of 9 was high-grade in adolescents.

For preoperative diagnosis, the same diagnostic method as that used in adults was used in all cases because this study included only those aged 12 years or older. When a parotid tumor was suspected on inspection and palpation, this was further examined using ultrasound echo and guided FNAC. In our department, FNAC is performed preoperatively in all patients. Of the 12 pleomorphic adenomas, 11 were diagnosed as pleomorphic adenomas by preoperative FNAC. Regarding pleomorphic adenoma in adults, FNAC diagnosed pleomorphic adenoma correctly in about 85% of cases,¹¹ with a similar rate observed among pediatric cases. On the other hand, only 4 adolescent cases among 9 were correctly diagnosed as malignant by FNAC. The high number of low/intermediate-grade malignant tumors seemed to be the cause; thus, the accuracy rate was lower than that in adults.¹²

A systematic review of pediatric malignant tumors, including 427 parotid tumors in patients 0 to 19 years old, reported that 53% were mucoepidermoid carcinoma, 29% were acinic cell carcinoma, and 5% were adenoid cystic carcinoma.⁹ Similarly, another systematic review of patients 0 to 19 years old with parotid tumors found that 58% of 2215 patients had mucoepidermoid carcinoma and 25% had adenoid cystic carcinoma.¹³ These data are further supported by a database review by Radomski et al,¹⁴ which found that 50% of 220 cases of parotid tumors were mucoepidermoid carcinoma, 40% were acinic cell carcinoma, and 3% were adenoid cystic carcinoma. In our study, mucoepidermoid carcinoma also accounted for half of all cases, and the rest were adenoid cystic carcinoma, secretory carcinoma, and malignant lymphoma. In our department, fusion gene testing is performed for all cases of acinic cell carcinoma to distinguish secretory carcinoma. We found that approximately 50% of acinic cell carcinomas proved to be secretory carcinomas. In addition, secretory carcinomas occurred significantly more than acinic cell carcinomas in adolescents.¹⁵ Therefore, it is possible that about half of the acinic cell carcinomas in previous studies were secretory carcinomas.

Previous studies suggest that malignant parotid tumors in adolescents are frequently low/intermediate-grade, with a high-grade rate of approximately 15%.^9,14 Among the 9 cases included in this study, 5 cases were low-grade (mucoepidermoid carcinoma and acinic cell carcinoma), 3 cases were intermediate-grade (cribriform type adenoid cystic carcinoma and lymphoma), and only 1 case was high-grade (mucoepidermoid carcinoma). The observation period ranged from 1 to 20 years, and all patients are surviving cancer-free at the time of this writing. Children generally have a favorable prognosis because the grade of malignancy is often low or intermediate. However, long-term observation is still required for low/intermediate-grade malignant tumors, and Cockerill et al¹⁶ found that when 52 adolescent cases (including 49 parotid tumors) were followed up for a maximum of 60 years, recurrence occurred in 15 (29%) of 52 patients. It should be noted that for most recurrences, the initial surgery was enucleation. As the longest time to recurrence was 45 years in the above study, treatment that takes long-term prognosis into consideration is especially important in pediatric cases.

Pleomorphic adenomas are found at a high rate in pediatric benign tumors, and all cases of benign parotid tumors were pleomorphic adenomas in our study. Among the 967 adult benign parotid tumors, 635 (65.7%) were pleomorphic adenomas, indicating that the rate of pleomorphic adenomas was higher in children. However, there were 17 patients with intraparotid nodules during the same observation period. Surgery revealed them to have inflammatory disease, and 3 of these patients were under 20 years old. Cases of inflammatory parotid nodules likely exist among those who do not undergo surgery. Therefore, inflammatory diseases are an important differentiation to pleomorphic adenoma. Since inflammatory diseases are often accompanied by pain/tenderness, and about half of malignant parotid tumors have pain/tenderness, it is also important to distinguish between inflammatory diseases and malignant tumors.¹⁷

Existing issues of pleomorphic adenoma include recurrence and malignant transformation. Recurrence often occurs 10–15 years after surgery, and a .45% risk of recurrence per year after surgery has been reported for pediatric pleomorphic adenoma.¹⁸ The risk of malignant transformation of pleomorphic adenoma is also thought to increase with time during long-term observation.⁸ From this perspective, more attention should be paid to recurrence and malignant transformation in pediatric cases because they require a long follow-up observation than adult cases do. Recurrence is generally thought to be more common in cases of enucleation.⁶ In pediatric cases, limited surgery may be selected more often for protection of the facial nerve and aesthetic issues. However, definitive removal may be more desirable because long-term observation is required. The standard operative method would be to perform a PSP where the facial nerve is identified and preserved. It should be noted that 2 of 12 patients with pleomorphic adenoma had recurrences in our study, and the time to recurrence took only 3 years and 5 years, which are relatively short periods of time. The initial surgery was conducted at our department in both patients, and both underwent PSP as with other cases. There were 635 adult cases of pleomorphic adenoma that were operated on within the same time period, of which 34 (5.4%) had recurrences, but the initial surgery was performed at our department in only 2 of these cases.⁶ The 2 pediatric cases with a recurrent pleomorphic adenoma in our study were recurrences with single tumor in the superficial parotid gland and were not multiple recurrences by dissemination.

Conclusion

Adolescent patients, defined as under 20 years old, comprised 12 (1.2%) of 979 patients with benign parotid tumors and 9 (3.8%) of 236 patients with malignant parotid tumors; thus, showing relatively more malignant cases. Histopathologically, benign tumors were all pleomorphic adenomas, and mucoepidermoid carcinoma was common among the malignant tumors. Pleomorphic adenomas are known to be associated with recurrence and malignant transformation, and the appropriate resection is desirable in pediatric cases because they require a long-term observation. Although the malignant tumors in this study were of low/intermediate malignancy grade, except for one case, and the prognosis was favorable, further observation over longer periods is required.

Footnotes

Author Contributions

HK, TT, SH, and RK: study designHK, YI, and RK: writing of the manuscriptIK, YA, and AO: literature searchIK, SO, and MH: data analysisRK: final approval of the manuscriptAll authors read and approved the final manuscript.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Ethical Approval

This study was approved by our Institutional Review Board (Osaka Medical College; #2621-1,2020).

ORCID iD

Masaaki Higashino

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Characteristics and Outcomes of Parotid Gland Tumors in Adolescents

Abstract

Objective

Methods

Results

Conclusion

Keywords

Introduction

Materials and Methods

Patients

Methods

Statistical Analysis

Results

Comparison of Adolescent and Adult Cases

Fine-Needle Aspiration Cytology (OMC Classification) in Adolescents and Adults

Adolescent Patients With Benign Tumors

Adolescent Patients With Malignant Tumors

Discussion

Conclusion

Footnotes

Author Contributions

Declaration of conflicting interests

Funding

Ethical Approval

ORCID iD

References