Epidemiological, Clinical, and Histopathological Features of Salivary Gland Tumors among 150 Sudanese Patients: 10 Years’ Experience : Journal of Microscopy and Ultrastructure

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Original Article

Epidemiological, Clinical, and Histopathological Features of Salivary Gland Tumors among 150 Sudanese Patients: 10 Years’ Experience

Hamid, Somaya T. S.1; Abdalla, Mohammed A. M.2; Zulfu, Azza A.1; Ramadan, Azza3; Ahmed, Musaab4; Ahmed, Mohamed H.5,

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Journal of Microscopy and Ultrastructure 11(2):p 92-96, Apr–Jun 2023. | DOI: 10.4103/jmau.jmau_113_20
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Abstract

Background and Objectives: 

Salivary gland tumors (SGTs) are serious challenges to pathologists. Herein, we aimed to assess epidemiological and histopathological characteristics of SGTs among Sudanese patients.

Materials and Methods: 

This retrospective descriptive study was undertaken at The pathology department in Khartoum State between 2008 and 2018. Patient records, histopathological reports, and slides were retrieved; and re-examined by two histopathologists. Diagnoses were reclassified according to the 2017 WHO classification of SGTs.

Results: 

Overall, 150 cases of Sudanese patients with SGT were included (90 [60%] males and 60 [40%] females). Among these, 105 were benign (70%) and 45 were malignant (30%). The parotid glands were the most common site for both benign and malignant tumors (77/150; 51%: 59 benign (76.6%) and 18 malignant [23.4%]). The next common site was the submandibular gland (54 [36%]: 38 benign [70.3%] and 16 malignant [29.7%]), followed by minor salivary glands (19 [12.7%]: 8 benign and 11 malignant [57.9%]). Benign gland entities included pleomorphic adenoma (88/105; 83.7%), oncocytoma (5/105; 4.8%), myoepithelioma (4/105; 3.8%), Whartin tumors (3/105; 2.9%), basal cell adenoma (3/105; 2.9%), and sialolipoma (2/105; 1.9%). Malignant gland entities included adenoid cystic carcinoma (12; 26.7%), mucoepidermoid carcinoma (10; 22,2%), acinic cell carcinoma (6; 13.3%), poorly differentiated carcinoma (4; 8.9%), adenocarcinoma NOS (not otherwise specified) (4; 8.9%), basal cell adenocarcinoma (3; 6.7%), carcinoma ex pleomorphic adenoma (3; 6.7%), polymorphous adenocarcinoma (2; 4.4%), salivary duct carcinoma (1; 2.2%), and epithelial–myoepithelial carcinoma (2.2%).

Conclusions: 

SGTs shared several epidemiological and histopathological features, exhibiting high incidence in the parotid and submandibular glands, lower prevalence in minor glands, and greater male predominance.

INTRODUCTION

Salivary gland tumors (SGTs) are a complex group of heterogeneous entities that pose serious challenges to pathologists, surgeons, and oncologists.[1–3] SGTs are rare neoplasms with an overall incidence of 0.3–4/100,000 individuals/year.[1] Malignant SGTs are extremely rare, with reported incidences of approximately 1.2–1.3 cases/100,000, representing nearly 3% of all head-and-neck cancers.[3]

The morphological diversity, complexity, and overlapping features of SGTs, along with the recognition of new entities with relevant therapeutic and prognostic implications, have added numerous challenges for histopathologists.[2] Therefore, it is necessary to state that accurate diagnosis and categorization are the cornerstones for guiding treatment.[3] Globally, accumulated data regarding SGTs are well categorized, either analyzing SGTs from a holistic standpoint or focusing on specific characteristics, such as epidemiological data, anatomical localization, diagnostic approaches, tumor type, distribution of benign and malignant tumors, histological entities, and therapeutic approaches.[1]

In Sudan, SGTs have mostly been reported within the oral cancer category.[4] Several reports have been published regarding SGTs in Sudan, and to our knowledge, no longitudinal follow-up study has been reported for the last 10 years.[5–7] Toombak (chewing tobacco, widely used in Sudan) has been reported as a risk factor for SGTs in Sudan.[8] Notably, most studies performed in Sudan assessed SGTs in Khartoum or central Sudan from Gezira State.[8–12] Given the increasing prevalence of different types of cancer in Sudan, the objective of this study was to review the clinicopathological and epidemiological profiles of SGTs among Sudanese patients within the last 10 years.

MATERIALS AND METHODS

Patient records (from four governmental health institutes: The National Health Laboratory, Soba University Hospital, Khartoum Teaching Hospital, and the Khartoum State Laboratory Directorate) were searched for demographic data and histopathology reports on SGTs; relevant slides, formalin-fixed, paraffin-embedded (FFPE) blocks of patients were retrieved for the period between 2008 to 2018. All cases with available clinical data, tissue section slides, or FFPE blocks were included in the study. Cases with missing clinical data or blocks were excluded. Slides for included SGTs were reviewed by two histopathologists. Tumor entities were reclassified according to the World Health Organization (WHO) classification of SGTs (2017). Data were analyzed using SPSS version 31 (IBM Corp., Chicago, IL, USA). This study received ethical approval from the research ethics committee, faculty of medicine, Omdurman Islamic University, Sudan (dated 12/9/2018 with reference No 2018/9/33). The sample collections and patients consent were done according to Helsinki Declaration.

RESULTS

Sociodemographic features and location of tumors

The present study included 150 patients with SGT, of which 60% were males and 40% were females. As shown in Table 1, the age groups ranged between 1 and 10 years old up to ≥70 years old. The tumors were primarily located in three glands (parotid, submandibular, and minor salivary glands). The parotid glands were most affected by benign and malignant tumors, while minor salivary glands were least affected [Table 2]. A predominance of parotid tumors (51.3%) was noted, followed by submandibular tumors (36%) and minor salivary glands (12.7%).

T1
Table 1:
Age and gender distribution of salivary gland tumors
T2
Table 2:
Distribution of benign and malignant tumors according to site

Importantly, 30% of the total tumors affecting all the glands were malignant, and the rest were benign, with a benign to malignant ratio of 2.3:1. In addition, SGTs were predominantly observed in male patients, both benign (60/105, 57.1%) and malignant tumors (30/45) (66.7%). Approximately 33.3% (30/90) of all male patients were diagnosed with malignant tumors when compared with 25% (15/60) of all female patients [Table 3]. Among patients with minor SGTs, 57% (8/14) had malignant tumors; hence, a patient with a minor SGT was more likely to be malignant than benign, especially male patients.

T3
Table 3:
Distribution of benign and malignant tumors and location by gender

Histological types of salivary gland tumors and their distribution (benign and malignant tumors)

Among all benign tumors, the most frequent histological diagnosis was pleomorphic adenoma (88/105; 83.7%) [Table 4 and Figure 1], comprising 58.7% (88/150) of all benign and malignant tumors in this series. The second most common benign tumor was oncocytoma (4.8%), as shown in Figure 2, followed by myoepithelioma (3.8%), Warthin tumor (2.9%), basal cell adenoma (2.9%), and sialolipoma (1.9%). The site most affected by benign tumors was the parotid gland (56.2%), followed by the submandibular gland (36.2%), and then minor salivary glands (7.6%). As shown in Figure 3, adenoid cystic carcinoma was the most commonly encountered malignant tumor (26.7%) [Table 5]. Overall, 41.7% of adenoid cystic carcinoma originated from the parotid gland, 33.3% from the submandibular gland, and 25% from minor salivary glands. The second most common malignancy was mucoepidermoid carcinoma [Figure 4], accounting for 22.2% of malignant SGTs. The third most frequent malignant SGT was acinic cell carcinoma (13.3%), as shown in Figure 5, while the fourth was poorly differentiated carcinoma and adenocarcinoma NOS (not otherwise specified; 8.9%). Basal cell adenocarcinoma, adenocarcinoma NOS, and carcinoma ex pleomorphic were ranked fifth (6.7%), followed by polymorphous adenocarcinoma (4.4%). The least common malignant SGTs in these series were epithelial–myoepithelial carcinoma and salivary duct carcinoma (2.2%). Approximately 24.4% of all malignant tumors arose from minor salivary glands, whereas 35.6% and 40% of malignant tumors originated from the submandibular and parotid glands, respectively.

T4
Table 4:
Distribution of benign tumors by site
F1
Figure 1:
Pleomorphic adenoma: Tumor showing a mixture of epithelial and stromal elements, with stroma exhibiting cartilaginous differentiation. H and E, ×40
F2
Figure 2:
Oncocytoma of the parotid gland: Tumor featuring oncocytic cells with abundant eosinophilic cytoplasm arranged in a solid growth pattern. H and E, ×40
F3
Figure 3:
Adenoid cystic carcinoma: The classical cribriform pattern consisting of basaloid epithelial cells, forming sharply demarcated nests containing multiple extracellular spaces. H and E, ×40
T5
Table 5:
Distribution of malignant tumors by site
F4
Figure 4:
Mucoepidermoid carcinoma: Tumor showing multiple cell types such as squamous cells, mucous cells, cuboidal intermediate cells, and basaloid cells. H and E, ×40
F5
Figure 5:
Acinic cell carcinoma: Tumor cells resemble the serous cells of the normal parotid gland, with fine granular, basophilic cytoplasm, clear cells also seen, with a solid growth pattern. H and E, ×40

DISCUSSION

The present study included 150 cases of SGTs in Sudanese patients, comprising 105 benign (70%) and 45 malignant (30%) tumors. The parotid glands were the most common site for both benign and malignant tumors (77/150; 51%), exhibiting 59 benign tumors (76.6%) and 18 malignant tumors (23.4%). The second most frequent site for SGTs was the submandibular glands (54 cases; 36%), presenting 38 benign (70.3%) and 16 malignant (29.7%) tumors. SGTs in minor salivary glands were detected in 19 (12.7%) cases, with 8 benign and 11 malignant (57.9%) cases. Despite the growing prevalence of different types of cancer in Sudan, the parotid glands were most affected by SGTs among Sudanese populations, as evidenced in current and previous studies.[5–7] Interestingly, we used the 2017 WHO classification of SGTs, which included approximately 30 entities, whereas most previous studies conducted in Sudan used the old classification of SGTs.

Furthermore, Suleiman et al. have shown that in a cohort of Sudanese patients with SGTs, 52.4% had benign tumors, and 46.6% presented malignant tumors, with a very high ratio of benign to malignant tumors when compared with our series (70% to 30%). Almost all benign tumors were pleomorphic adenomas, consistent with the present study. The authors found that malignant tumors were possibly adenocarcinoma and adenoid cystic carcinoma.[7] However, based on data from central Sudan (Gezira state), squamous cell carcinoma appears to be the most common oral malignancy (66.5%), followed by SGTs (14.7%). The authors reported that the only benign SGT detected was pleomorphic adenoma (144 cases; 7.5%), along with 183 cases of malignant SGTs (7.2%). Moreover, they classified five types of malignant SGTs as follows: 25 (1.3%) salivary carcinoma, 41 (2.1%) adenoid cystic carcinoma, 17 (0.9%) mucoepidermoid carcinoma, 53 (2.8%) adenocarcinoma, and 2 (0.1%) acinic cell carcinoma.[9] Idris et al. have reported a higher proportion of malignant tumors when compared with our series (49%:51% vs. 30%:70%, respectively). This discrepancy could be attributed to the fact that these authors used the previous tumor classification.[8] Ahmed et al. have shown similar results in the Sudanese population, with pleomorphic adenoma documented as the most common benign tumor. In addition, the authors reported that adenoid cystic carcinoma was the most common malignancy, followed by mucoepidermoid carcinoma, acinic cell carcinoma, squamous cell carcinoma, and a single case of myoepithelial carcinoma. Similar to the findings of the present study, Ahmed et al. have reported a predominance of benign tumors when compared with malignant tumors, with pleomorphic adenoma being the most common tumor and adenoid cystic carcinoma documented as the most common malignant tumor. However, the authors did not include the site of affected glands.[12]

Importantly, our results share many similarities with worldwide epidemiological data, presenting some differences when compared with studies conducted across different countries. For example, Galdirs et al. have published a literature review on SGTs, based on data collected from 30 different countries, from 51 resources from 1981 to 2018. The authors revealed that patient age ranged from 2.5 to 92 years, mean age ranged from 41.9 to 43 years, and the male-to-female ratio ranged from 1:1.09 to 1:1.8. Between 60% and 84.2% of all tumors were detected in the parotid glands, while 16% were within the submandibular gland. Minor SGTs accounted for 24%–39.3% of cases. Pleomorphic adenoma was reportedly the most common benign tumor, while the most common malignant tumors were adenoid cystic carcinoma, mucoepidermoid carcinoma, and acinic cell carcinoma. Most results obtained in the present corroborate the data extracted by Galdris et al.[1] Furthermore, our data showed similar outcomes to the data obtained from different countries, including Uganda, Jordan, Iran, and Brazil, demonstrating similarities in most aspects.[13–17] Therefore, it is possible to conclude that despite the increased prevalence of cancer in Sudan, the clinicopathological and epidemiological profile of SGTs in Sudan did not change when compared with previous studies conducted in both Sudan and other countries.

The limitations of the present study need to be addressed. It should be noted that not all SGTs were referred or reported at the central laboratory in the capital Khartoum; this can be attributed to the fact that Sudan is a large country, and cases in remote areas may not be diagnosed, or patients may die before the diagnosis has been established. However, despite these limitations, our study is novel, especially given the use of the 2017 WHO classification of salivary tumors, and undoubtedly showed no change in the epidemiology and histopathological pattern of SGTs in Sudan over the last 10 years.

CONCLUSIONS

The present study presented epidemiological, clinical, and histopathological aspects of SGTs in Sudan from 2010 to 2018, based on histopathological data and records and histopathological features. A high incidence of SGTs was documented in the parotid gland, followed by the submandibular and minor glands, with greater prevalence in males.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

Acknowledgment and Dedication

The authors of this manuscript dedicates the effort and work in this manuscript for the first author (Dr Somaya T Hamid) who died few months after the submission of this manuscript. May Allah grant her heaven.

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              Keywords:

              Histopathology; salivary glands tumors; Sudan

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