A relevant search of English literature was conducted in PubMed, SpringerLink, ScienceDirect, Scopus, and Google Scholar for distant metastasis from major salivary gland tumours.

Results

This retrospective study included 148 reported cases. Among them, 79 patients were male and 69 were female. The mean age of the patients was 53 ± 14. The parotid gland was the most frequently metastatic salivary gland, and various bones were the most common metastatic sites, followed by the lungs. Adenoid cystic carcinoma was the most common histological tumour type. The time interval between the development of a primary tumour and the diagnosis of the metastatic lesion ranged from 2 to 600 months. In most patients, the secondary lesion was diagnosed in less than 127 months. In 103 cases, the patient was alive at the time of reporting.

Conclusion

1 Introduction

Major salivary gland tumours constitute 6% of all malignant tumours in the head and neck region and 0.3% of all malignancies [1]. They exhibit a wide spectrum of clinical, histological, and biological features and have a varied rate of local, regional, and distant metastases [2, 3]. The prevalence has been estimated to be between 8.7% and 50%, depending on histological types and tumour sites [4].

Metastasis is an important biological behaviour of salivary gland tumours that complicates treatment and is associated with poor prognosis [3, 5]. The lungs, bones, brain, and liver are the most common metastatic sites [3]. Undifferentiated carcinoma, followed by adenocarcinoma, is the most common tumours with distant metastasis (DM) [6]. A previous study has indicated that distant metastasis is more frequent in tumours arising in the submandibular gland than in those arising in the parotid gland [7]. Salivary gland tumours comprise a heterogeneous histological group with variable biological behaviour. Metastatic lesions are the main cause of cancer-related deaths in humans [3].

The identification of clinicopathological characteristics of salivary gland tumours associated with DM is crucial for therapeutic planning. The aim of this retrospective study was to analyse the clinicopathological characteristics of cases of major salivary gland tumours linked to distant metastasis.

2 Materials & Methods

2.1 Searching Strategy

A relevant search of English literature was conducted in PubMed, SpringerLink, ScienceDirect, Scopus, and Google Scholar. The keywords: “major salivary glands”, and “distant metastasis” were searched in the title/abstract of publications, limited to the years 1970–2024. Only related case reports were included. Figure 1 illustrates the flow of the number of articles identified, included, and excluded at different stages.

Details are in the caption following the image — **FIGURE 1**
Open in figure viewer PowerPoint

The flow diagram of the current review.

All variables such as age, gender, primary and secondary tumour sites, histological type of tumour, time interval between detection of the primary tumour and diagnosis of metastasis, and survival status were analysed using the Chi-square test and Fisher's exact test.

2.2 Quality Assessment & Data Analysis

For a more comprehensive understanding, all data were categorised into two groups: lesions in males and lesions in females. To perform statistical analysis, metastatic sites with ≤ 6 cases were combined into the miscellaneous group. In addition, histologic types with ≤ 6 cases were grouped as the miscellaneous group. All bones as metastatic sites were classified as one group: various bones.

3 Results

This retrospective study included 148 reported cases. Among them, 79 patients were male and 69 were female. The mean age of the patients was 53 ± 14 (ranging from 10 to 91 years). The parotid gland was the most frequently metastatic salivary gland (n = 105; 70%), and various bones were the most common metastatic sites (n = 31; 20%), followed by the lungs (n = 25; 16%). Adenoid cystic carcinoma (AdCC) was the most common histological tumour type (n = 40; 27%), followed by metastasizing pleomorphic adenoma (MPA) (n = 31; 20%). Interestingly, all histological types were more frequent with distant metastases from the parotid gland except for AdCC, which was more frequent with distant metastases from the submandibular glands (n = 18 vs. n = 19). The time interval between the development of a primary tumour and the diagnosis of the metastatic lesion ranged from 2 to 600 months, with a mean of 127 months. In most patients, the secondary lesion was diagnosed in less than 127 months (n = 84). In 103 cases, the patient was alive at the time of reporting.

Regarding the demographic data for males, the age ranged from 22 to 91 years, with a mean age of 54 ± 13. Additionally, the parotid gland was the most common primary site, with 58 cases, while the sublingual gland was the least frequent primary site, with 4 cases. The most frequent metastatic sites were various bones (17 cases), followed by the lungs (14 cases). The kidney was the least common metastatic site (1 case). Adenoid cystic carcinoma was the most common metastatic histologic type (n = 18), while acinic cell carcinoma was the least metastatic tumour type (n = 3). In most patients (n = 51; 34.46%), metastatic disease was found in less than 127 months. The number of patients who were alive at the time of reporting was 54.

Considering the demographic details of females, the mean age was 52 ± 15 years (ranging from 10 to 83). Additionally, the parotid gland was the most common primary site (n = 47; 31.8%), while the sublingual gland was the least common primary gland (n = 1). Various bones were the most common metastatic sites (n = 14; 9.5%). The lymph nodes were the least common metastatic site (n = 1). The most common histologic type was AdCC (n = 22; 14.9%). In 33 cases (22.3%), the time interval between the development of a malignancy and the diagnosis of the metastatic tumour was less than 127 months, and 49 patients were alive at the time of reporting.

All details are provided in Tables 1 and 2.

TABLE 1. A summary of distant metastasis from salivary gland tumours in males.

Primary site (type of gland)	Metastatic site	Age range (years)	Histological type	The time interval from the detection of the primary tumour to the diagnosis of metastasis	Survival status after diagnosis till the report of case	References
Parotid	Lung	26	AdCC	10 years	Alive	[8]
Parotid	Lung, bones, muscles, skin	40	AdCC	15 years	Died after 2 months	[9]
Parotid	Eyes	52	AdCC	Same time	Alive	[10]
Parotid	Eye	64	AdCC	5 years	Alive	[11]
Parotid	Brain	60	AdCC	10 years	Died after 8 months	[12]
Parotid	Brain	62	AdCC	12 years	Alive	[13]
Parotid	Brain	52	AdCC	27 years	Alive	[14]
Parotid	Skin	39	AdCC	8 years	Alive	[15]
Parotid	Splenium, corpus callosum	43	AdCC	5 years	Alive	[16]
Parotid	Lung	58	MPA	34 years	Alive	[17]
Parotid	Lung	55	MPA	39 years	Alive	[18]
Parotid	Lung, liver	57	MPA	7 years	Alive	[19]
Parotid	Skin	31	MPA	8 years	Alive	[20]
Parotid	Skin	56	MPA	8 years	Alive	[21]
Parotid	Supraclavicular LN	61	MPA	28 years	Alive	[22]
Parotid	Back of the neck	36	MPA	18 years	Alive	[23]
Parotid	Maxillary gingiva, bone	36	MPA	21 years	Alive	[24]
Parotid	Maxillary sinus	32	MPA	12 years	Alive	[25]
Parotid	Spine	65	MPA	7 years	Alive	[26]
Parotid	Calvaria	33	MPA	16 years	Alive	[27]
Parotid	Lung, spleen	66	CaXPA	3 years	Alive	[28]
Parotid	Eyes	34	CaXPA	1 year	Alive	[29]
Parotid	Eye	65	CaXPA	6 months	Died after 2 years	[30]
Parotid	Brain	36	CaXPA	19 months	Died after 2 months	[31]
Parotid	Abdomen	72	CaXPA	15 months	Died after 3 months	[32]
Parotid	Liver	55	CaXPA	Same time	Died after 3 months	[33]
Parotid	Colon	78	CaXPA	Same time	Alive	[34]
Parotid	Skin	40	SDC	18 months	Alive	[35]
Parotid	Skin	71	SDC	2 years	Alive	[36]
Parotid	Skin	69	SDC	2 months	Alive	[36]
Parotid	Lung	65	SDC	12 years	Alive	[37]
Parotid	Stomach	67	SDC	1 year	Died after 8 months	[38]
Parotid	Mandibular gingiva	67	SDC	11 months	Died after 1 month	[39]
Parotid	Spine	44	SDC	3 years	Died after 7 months	[40]
Parotid	Eye	43	SDC	6 years	Alive	[41]
Parotid	Eye	56	SDC	Same time	Alive	[42]
Parotid	Bones, liver, CLN	68	SDC	Same time	Alive	[43]
Parotid	Brain	61	SDC	4 years	Alive	[44]
Parotid	Bulbar conjunctiva	65	MEC	10 months	Alive	[45]
Parotid	Cerebellopontine	72	MEC	4 years	Died after 9 months	[46]
Parotid	Colon	59	MEC	10 years	Alive	[47]
Parotid	Eyes	45	NOS	1 year	Alive	[48]
Parotid	Eye	91	NOS	2 years	Died after 5 months	[49]
Parotid	Endobronchial	43	NOS	9 months	Alive	[50]
Parotid	Lung	64	MyCa	Several months	Alive	[51]
Parotid	Kidney	56	MyCa	22 months	Alive	[52]
Parotid	Cavernous sinus	46	MyCa	3 years	Alive	[53]
Parotid	Iliac crest	No data	ACC	3 years	Alive	[54]
Parotid	Vertebra	40	ACC	4 months	Alive	[55]
Parotid	Skull	53	ACC	7 years	Alive	[56]
Parotid	CLN	74	CyAd	1 year	Alive	[57]
Parotid	Intra-parotid LN	47	CyAd	2 years	Alive	[57]
Parotid	Lung, brain	32	BCA	5 years	Alive	[58]
Parotid	Hand	67	BCA	2 years	Alive	[59]
Parotid	Lung	63	EMC	14 years	Alive	[60]
Parotid	CLN	47	CaS	Same time	Died after a few months	[61]
Parotid	Cerebellopontine Angle	61	OC	6 months	Died after 1 year	[62]
Submandibular	Liver	55	AdCC	1 year	Died after 3 years	[63]
Submandibular	Liver	76	AdCC	5 years	Alive	[64]
Submandibular	Spine	45	AdCC	11 years	Alive	[65]
Submandibular	Spine	62	AdCC	7 years	Died after a few months	[66]
Submandibular	Lung	53	AdCC	5 years	Alive	[8]
Submandibular	Great toes	52	AdCC	12 years	Alive	[67]
Submandibular	Sternum	52	AdCC	10 years	Alive	[68]
Submandibular	Lungs	49	MPA	11 years	Alive	[69]
Submandibular	Pelvis	59	MPA	44 years	Alive	[70]
Submandibular	Spine	35	CaXPA	Same time	Died after a few months	[71]
Submandibular	Kidney	63	CaXPA	30 years	Alive	[72]
Submandibular	Vertebra	67	OC	30 years	Alive	[73]
Submandibular	CLN	47	OC	Same time	Alive	[74]
Submandibular	Lung	51	EMC	3 years	Died after 30 months	[75]
Submandibular	Choroid plexus	46	NOS	5 months	Alive	[76]
Submandibular	CLN	69	CyAd	7 months	Alive	[57]
Submandibular	Skin	22	MyCa	No data	Alive	[77]
Submandibular	Spine	50	BCA	5 years	Alive	[78]
Sublingual	Lung	52	AdCC	20 years	Died after 2 years	[79]
Sublingual	Liver	70	AdCC	3 years	Alive	[80]
Sublingual	Brain	64	CaXPA	11 months	Died after 6 months	[81]
Sublingual	Pituitary gland	52	NOS	6 years	Alive	[82]

Abbreviations: ACC, acinic cell carcinoma; AdCC, adenoid cystic carcinoma; BCA, basal cell adenocarcinoma; CaS, carcinosarcoma; CaXPA, carcinoma ex pleomorphic adenoma; CLN, cervical lymph node; CyAd, cystadenocarcinoma; EMC, epithelial- myoepithelial carcinoma; LN, lymph node; MEC, mucoepidermoid carcinoma; MPA, metastasizing pleomorphic adenoma; MyCa, myoepithelial carcinoma; NOS, not otherwise specified; OC, oncocytic carcinoma; SDC, salivary duct carcinoma.

TABLE 2. A summary of distant metastasis from salivary gland tumours in females.

Primary site (type of gland)	Metastatic site	Age range (years)	Histological type	The time interval from the detection of the primary tumour to the diagnosis of metastasis	Survival status after diagnosis till the report of case	References
Parotid	Lung	45	MPA	17 years	Alive	[21]
Parotid	Lungs	33	MPA	23 years	Alive	[83]
Parotid	Lungs	40	MPA	12 years	Alive	[84]
Parotid	Lung	54	MPA	3 years	Died after 5 years	[85]
Parotid	Kidney	40	MPA	16.9 years	Alive	[86]
Parotid	Kidney	68	MPA	28 years	Alive	[87]
Parotid	Kidney	49	MPA	29 years	Alive	[88]
Parotid	Kidney	62	MPA	13 years	Alive	[89]
Parotid	Liver	65	MPA	20 years	Alive	[90]
Parotid	Liver	28	MPA	11 years	Alive	[91]
Parotid	Mediastinal ln	43	MPA	27 years	Alive	[92]
Parotid	Cervical area	36	MPA	15 years	Alive	[93]
Parotid	Brain	10	MPA	3 years	Alive	[94]
Parotid	Sacrum	75	MPA	25 years	Alive	[95]
Parotid	Supraspinatus muscle	65	MPA	24 years	Died after 5 months	[96]
Parotid	Liver	60	AdCC	3 years	Died after 2 years	[97]
Parotid	Liver	30	AdCC	10 years	Alive	[98]
Parotid	Kidney	21	AdCC	7 years	Alive	[99]
Parotid	Kidney	40	AdCC	5 years	Died after 10 years	[100]
Parotid	Skin	63	AdCC	4 years	Died after 2 months	[101]
Parotid	Intrasellar area	78	AdCC	4 years	Alive	[102]
Parotid	Brain	43	AdCC	15 years	Alive	[103]
Parotid	Spine	71	AdCC	37 years	Alive	[104]
Parotid	Pituitary gland	72	AdCC	26 years	Alive	[105]
Parotid	Lung	53	ACC	2 years	Died after 6 months	[106]
Parotid	Lung	65	ACC	No data	Died after 2 years	[107]
Parotid	Pancreas	46	ACC	7 years	Alive	[108]
Parotid	Eye	54	ACC	Same time	Alive	[109]
Parotid	Skin	59	ACC	20 years	Alive	[110]
Parotid	Vertebra	72	ACC	6 years	Alive	[111]
Parotid	Spine	71	ACC	15 months	Died after 8 months	[112]
Parotid	Ilium	78	ACC	1 year	Alive	[113]
Parotid	Mandible	41	CaXPA	Same time	Alive	[114]
Parotid	Brain	66	CaXPA	40 years	Died after 18 months	[115]
Parotid	Kidney	32	CaXPA	3 years	Died after 2 years	[116]
Parotid	Lung	80	SDC	Same time	Died after 11 months	[117]
Parotid	Uterus	61	SDC	3 years	Alive	[118]
Parotid	Brain	52	PDC	1 year	Alive	[119]
Parotid	Pelvic, femur	19	PDC	8 months	Alive	[120]
Parotid	Spine	41	EMC	1 year	Alive	[121]
Parotid	Vertebra	65	EMC	18 months	Alive	[122]
Parotid	Skull	55	MEC	6 years	Alive	[123]
Parotid	Ovaries, peritoneum	28	MEC	11 years	Died after 14 months	[124]
Parotid	Lung	52	NOS	Same time	Died after 15 months	[125]
Parotid	Skin	83	NOS	50 years	Died after 1 month	[126]
Parotid	Scalp	58	BCA	2 years	Alive	[127]
Submandibular	Eyes	45	AdCC	11 years	Died after 5 weeks	[128]
Submandibular	Eyes	56	AdCC	2 years	Died after 6 weeks	[129]
Submandibular	Eyes	51	AdCC	2 years	Alive	[130]
Submandibular	Eye	50	AdCC	5 years	Died after 4 months	[131]
Submandibular	Liver	51	AdCC	2 years	Alive	[132]
Submandibular	Liver	52	AdCC	30 years	Alive	[133]
Submandibular	Ovary	30	AdCC	10 years	Alive	[134]
Submandibular	Lung, choroid	43	AdCC	5 years	Alive	[135]
Submandibular	Larynx	46	AdCC	9 years	Alive	[136]
Submandibular	Spine	54	AdCC	17 years	Alive	[137]
Submandibular	Breast	67	AdCC	5 years	Died after a few months	[138]
Submandibular	Toe	62	AdCC	8 years	Alive	[139]
Submandibular	Skin	57	MPA	3 months	Alive	[140]
Submandibular	Vertebra	35	MPA	11 years	Alive	[21]
Submandibular	Lung, sternum	40	MPA	7 years	Alive	[141]
Submandibular	Breast	64	SDC	3 years	Alive	[142]
Submandibular	Bone marrow	33	PDC	3 years	Alive	[143]
Submandibular	Vertebra, lung	39	PDC	4 months	Alive	[144]
Submandibular	Brain, vertebra	60	NOS	41 months	Alive	[119]
Submandibular	Skin	68	MyCa	5 years	Died after 1 year	[145]
Submandibular	Eyes	52	MEC	6 years	Died after 5 months	[146]
Sublingual	Lung	66	AdCC	No data	Alive	[147]

Abbreviations: ACC, acinic cell carcinoma; AdCC, adenoid cystic carcinoma; BCA, basal cell adenocarcinoma; CaXPA, carcinoma ex pleomorphic adenoma; EMC, epithelial- myoepithelial carcinoma; LN, lymph node; MEC, mucoepidermoid carcinoma; MPA, metastasizing pleomorphic adenoma; MyCa, myoepithelial carcinoma; NOS, not otherwise specified; PDC, poorly differentiated carcinoma; SDC, salivary duct carcinoma.

Table 3 summarises statistically significant results based on Chi-square and Fisher's exact tests.

TABLE 3. Details of statistically significant results based on Chi-Square Test and Fisher's Exact Test.

Variable 1	Variable 2	p
Gender	Age	0.001*
Gender	Type of tumour	0.012*
Gender	Time interval	0.015*
Age	Type of tumour	0.001*
Age	Time interval	0.001*

*Denotes statistical significance.

4 Discussion

Distant metastasis is a complex process and a late event in tumour progression. It results from the seeding of circulating tumour cells in certain organs. According to Paget' theory, the distribution of metastatic cells in specific organs is not random, leading to the proposing of the seed and soil theory [148].

Due to the rarity of salivary gland tumours, knowledge about the progression of these tumours is limited [149]. In the present study, similar to a prior study, DM was predominantly found in males (64% vs. 53% in females) [4]. This finding may suggest that men present with more advanced stages of tumours at the time of diagnosis.

In the current analysis, the mean age of the patients was 53 ± 14; however, in a prior study, the mean age of the patients was 61 years (range, 15–88) [4]. Furthermore, it has been established that DM is more common in elderly cancer patients (65 years and older) [150]; nonetheless, in the current series, only 29 patients were older than 65 years (19.5%). Notably, 32 patients (21.6%) were 40 years old or younger. A previous investigation showed that DM is not correlated with gender and age but is related to the tumour site [9]. However, the current study demonstrated a relationship between gender and age with other studied variables (see Table 3).

In the present series, the parotid was the most common salivary gland with DM (70.9%), but a previously published work found the submandibular gland to be the most prevalent salivary gland metastasising to other organs (42%). The metastatic route of parotid tumours is unclear, but it is suggested that the maxillary artery, which travels through the parotid gland, may serve as a vascular spread route [114]. A prior study on 103 cases of parotid tumours found DM in 24% of cases, primarily in the lungs (68%), followed by the bones (24%) [15]. However, the current series indicated metastases to the bones and lungs in 20.9% and 16.9% of cases, respectively. It is generally accepted that the lungs and bones are the two most common sites for distant metastasis [16]. A very recent systematic review found 19 cases of spinal metastasis with a mean age of 54 years. The most common histopathological subtypes were ACC, followed by AdCC [151]. The current study identified 10 cases of spinal metastasis with a mean age of 53.6 (range, 35–71). The most common salivary gland tumour with spinal metastasis was AdCC with 4 cases. Spinal metastasis from ACC was reported in one case.

Metastasis is not a random process; before the spread of cancer cells, a premetastatic niche, a supportive environment, must be established. For example, VEGF receptor 1 (VEGFR1)-positive BM-derived haematopoietic progenitor cells accumulate in the premetastatic tissue before the arrival of cancer cells [152].

Rarely, head and neck cancer spreads via blood vessels. Therefore, cervical lymph node metastasis is expected to be the most common event [2]; nevertheless, the present case series found that metastasis to the cervical lymph nodes occurred in 3.4% of patients. A prior systematic analysis on cervical lymph node metastases from AdCC identified only 4 studies showing cervical lymph node metastasis in 17% of patients. Additionally, this systematic review found that AdCC from minor salivary glands has a higher rate of cervical lymph node metastasis. The authors concluded that elective neck dissection is not necessary for patients with major salivary gland AdCC [153].

In this investigation, various bones were the most frequent metastatic sites (21%), followed by the lungs (16.9%). These findings are not consistent with a previous study that showed the lungs as the most prevalent metastatic sites, followed by the bones [154].

In the current analysis, the most common histotype with DM was AdCC with 40 cases (27%), followed by MPA with 31 cases (20.1%). Additionally, AdCC was the most common histological tumour type metastasising to various tissues in both genders. The incidence of DM from AdCC varies between 5% and 54.9%, and the lungs, bones, liver, and brain are the most common sites for metastases. AdCC accounts for approximately 10% of salivary gland neoplasms and affects both the parotid and submandibular glands [155]. In this review, AdCCs metastasised mainly from submandibular glands, not the parotids (47% vs. 45%). It has been suggested that submandibular AdCCs have a greater ability to induce tumour angiogenesis [156]. Furthermore, it has been documented that the myoepithelial cells in submandibular AdCC have a higher rate of proliferation and are less differentiated than those in the parotid AdCC. These findings may explain the increased aggression of the submandibular AdCC [157]. Notably, AdCC has the ability to invade adjacent structures as well as to demonstrate DM. In addition, a unique characteristic of AdCC that differentiates it from other salivary tumours is perineural invasion [157].

In the present analysis, there were 31 cases (21%) of DM from MPA with 18 cases in females (12.1%). Among these, 26 cases (17.6%) were from parotid tumours. Moreover, in 9 cases (6%) DM from MPA occurred in the lungs, and in 6 cases (4%), it occurred in various bones. There are several reports of locally aggressive pleomorphic adenomas that metastasised to regional lymph nodes and exhibited DM, despite their benign histologic appearance. PA may undergo malignant transformation in 2% to 9% of cases, whether a long-standing primary tumour or a recurrent tumour. It is suggested that the proliferation of myoepithelial cells may alter the tumour's nature [20]. It is unclear how a benign tumour such as PA metastasises to other organs. Perhaps the most accepted hypothesis is the accumulation of key genetic alterations that cause histological and biological changes. For example, the cumulative loss of chromosomal loci at 3p, 9p, and 17p has been observed in MPAs [85]. Additionally, it has been proposed that prior radiation of the primary tumour or surgical manipulation allows tumour cells to enter blood vessels [141]. These findings suggest that cases histologically diagnosed as AdCC or MPA are the most significant candidates for further follow-up.

5 Conclusion

Adenoid cystic carcinoma and metastasising pleomorphic adenoma are highly aggressive major salivary gland tumours characterised by rapid growth and distant metastasis. Although distant metastasis from major salivary gland tumours is uncommon, it signifies a poor prognosis, with death occurring within months of detection. Therefore, greater attention should be paid to major salivary gland tumours. Understanding the clinical history and histopathologic characteristics of salivary metastatic tumours is critical for achieving an accurate diagnosis, which is essential for appropriate patient management.

Acknowledgements

The author would like to thank Hamadan University of Medical Sciences for continued support. Open access publishing facilitated by Griffith University, as part of the Wiley - Griffith University agreement via the Council of Australian University Librarians.

Conflicts of Interest

The author declares no conflicts of interest.

Open Research

Data Availability Statement

The author has nothing to report.

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Early View

Online Version of Record before inclusion in an issue

A Comprehensive Review of 148 Cases of Major Salivary Gland Tumours: Critical Insights Into Metastatic Patterns, Prognostic Factors, and Treatment Outcomes

ABSTRACT