Abstract
The global incidence of Warthin`s tumors (WTs) is on the rise which necessitates the need for effective management strategies. Traditionally, surgical options have been widely employed for the management of WT. Furthermore, the increased utilization of surgical options for WT can be due to uncertain diagnosis, cosmetic concerns, or the patient`s desire to remove the tumor. However, non-surgical options such as microwave ablation, radiofrequency ablation, and ultrasound-guided ethanol sclerotherapy are emerging as suitable options for selected cases. The purpose of the current review was to provide a comprehensive review of the literature regarding WT including epidemiology, clinical presentation, evaluation, and therapeutic approaches. The review also aimed to describe non-surgical options for the management of WT. For this review, comprehensive research was conducted in PubMed, Web of Science, Cochrane, and Embase libraries databases to find relevant studies that evaluated non-surgical approaches to the management of WT. Due to the paucity of relevant research, only six studies fulfilled the selection criteria. The majority of these studies had small sample sizes. Overall, our review highlights the current trends in WT management, with non-surgical options emerging as a viable alternative to surgical management.
Keywords: Parotid gland; benign tumors; cystadenolymphoma, papillary cystadenoma lymphomatosum, adenolymphoma.
1. Introduction
Warthin tumor (WT) is a frequently reported benign tumor of the parotid gland and is the second most prevalent tumor following pleomorphic adenoma [1]. Although WT is benign in most cases, it has demonstrated the capability of malignant transformation [2, 3]. The occurrence of malignant transformation in WT is reported in up to 1% of cases with a higher incidence of squamous and mucoepidermoid carcinomas [4]. There are several synonyms for WT including papillary cystadenoma lymphomatosum, adenolymphoma, lymphomatous adenoma, and cystadenolymphoma. This pathological entity was initially characterized by Dr. Aldred Scott Warthin in 1929 and accounts for a significant proportion (14% to 30%) of neoplastic lesions that affect the parotid gland [5]. Around 12% to 20% of the WTs are multicenter whereas 5% to 14% of the patients have bilateral WTs [6]. The tumor is rarely diagnosed in patients aged below 40 years (<6%) and is mostly reported in middle-aged and elderly patients (>50 years) [7]. Males have a higher predisposition for WT compared to females. It is generally located in the inferior pole of the parotid gland [8]. Histologically, WT is composed of solid and cystic areas which constitute two distinct components. The first is a bi-layered oncocytic epithelium that forms papillary projections with abnormal morphology. The second is stromal components of lymphoid tissue that have germinal centers [9]. Usually, WTs are slow-growing, painless, and non-invasive. They may occasionally occur in other salivary glands or at extra-salivary sites such as the lymph nodes or the pancreas. Wilms tumor is characterized by gradual, painless, or slightly uncomfortable growth or lump in the lower part of the parotid gland, which is soft in consistency and tends to increase in size over time [10]. Reports indicate that WTs may coexist with other benign and malignant salivary gland neoplasms [11]. A study of seventy-three cases of WTs reported that almost 37% of the patients had a malignant neoplasm. The most frequent non-salivary malignant neoplasm was squamous cell carcinoma [11]. Furthermore, WTs can originate from intra- and peri-parotid lymph nodes, resulting in the isolated involvement of extra-parotid glands in the neck [12].
2. Prevalence and Etiology of WT
In recent times, a surge in the incidence of WT has been observed across the globe. Luers et al., in their investigations spanning over two and half decades, demonstrated the upward trend in the incidence of WT compared to pleomorphic adenomas [13]. Their findings indicate a
remarkable escalation in the prevalence of WTs, with an increase from 24% of all parotid gland tumors in 1990 to 48% in 2014 [13]. Similarly, Tunç et al. assessed the incidence rate of WT for 20 years [14]. Their findings demonstrated an irregular pattern of WT incidence compared to other tumors throughout the study period.. However, the total number of parotidectomies demonstrated an upward trend during this period. The results of the study did not find a significant annual percentage change (APC) in WT during the 20-year period (APC=4.3, P=0.300) [14].
The exact etiology of WT remains unknown but several risk factors have been identified in the literature that can lead to the progression of the disease. Smoking has emerged as a clearly evident factor in the progression of WT [15]. A 40-year study conducted at the Johns Hopkins Hospital found that smoking history was positively associated with WT [16]. Individuals with a family history of salivary gland tumors may be at higher risk of developing WT. Although the connection between human papillomavirus (HPV) infection and the tumor is not firmly established, there are some cases where the tumor has been associated with such infection [17, 18]. Recently, Kadletz et al. demonstrated an association of WT with obesity [19]. In their study, they found that WT patients had significantly higher BMI (p<0.0001) compared to other parotid gland tumors. Furthermore, the metabolic syndrome-associated comorbidities were significantly higher (p<0.0001) in WT patients compared to other tumors [19].
3. Diagnosis of WT
The diagnostic process for WTs generally involves a combination of physical examination, utilization of imaging modalities, and biopsy investigations. Physically, the tumor is usually a painless mass of the parotid gland. Furthermore, clinical information including age, a history of smoking, tumor size, and location can help in the diagnosis [20]. Ultrasound, computed tomography (CT), and magnetic resonance imaging are frequently employed imaging modalities to determine the size and location of the tumor mass [21]. The biopsy is performed to rule out any other potential causes of the mass including cyst or abscess. Furthermore, multiple or bilateral tumors as well as a prior diagnosis of homo or contralateral WT are characteristic of this disease. Fine needle aspiration biopsy (FNAB) is a commonly used minimally invasive method for diagnosing WTs, however, there is controversy regarding its sensitivity and specificity [22, 23]. The reported sensitivity and specificity by So et al. on FNAB were 95.8% and 97.2%, respectively. Their findings were based on the evaluation of 177 patients. Furthermore, the sensitivity and
specificity were 100% when only patients with multifocal, bilateral, or incidental tumors were assessed [24]. Similarly, Zahran, in his retrospective study investigated the efficacy of FNAB in the diagnosis of WT. Overall, the study demonstrated a sensitivity of 93% and specificity of 94.8% whereas an accuracy of 94.6% of FNAB for WT diagnosis [25]. A combination of oncocytic cells, polymorphic lymphocytes, and a granular proteinaceous background is typically indicative of a WT. However, if only one of these elements is present, diagnosis may be difficult. Moreover, squamous and mucous cell metaplasia can mimic the appearance of a squamous cell or mucoepidermoid carcinoma [10]. Macroscopically, WTs have typically encapsulated masses with a smooth or lobulated surface, while microscopically, they exhibit papillary and cystic architecture, oncocytic epithelial elements, and lymphoid stroma. Infarction can lead to metaplastic WTs, which display various degrees of necrosis and squamous and mucocyte metaplasia [26]. Although misdiagnosis is possible, it can be rectified by identifying a non-infarcted residual focus of a WT which lacks atypical mitosis or infiltrative growth. A variant of mucoepidermoid carcinoma resembling WT may be challenging to differentiate as it has multiloculated cystic structures with prominent lymphoid stroma, a multilayered epithelium with variable eosinophilia, cellular atypia, and mitotic activity [27].
4. Surgical management of WT
Surgical intervention is the standard and effective treatment option for the management of WT. The type of surgery may vary depending on the size and location of the tumor, as well as the patient`s age and overall health [28, 29]. In some cases, the affected salivary gland may need to be partially or completely removed. The adopted surgical methods can include limited resection (partial parotidectomy) or a more extensive approach (total parotidectomy). A 10-year surgical experience from a single center revealed that a total of 110 patients underwent surgical procedures for WT. The findings also showed that the lesion was found in the parotid tail portion in 65.3% of patients, whereas it was present in the superficial lobe in 28.8% and the deep lobe in 5.9% [30]. While radiation therapy is not typically used as a primary treatment, it may be considered in rare cases where complete surgical removal is not possible or the tumor recurs after surgery [31]. Although WT is generally non-cancerous and typically does not return after surgery, it is important to closely monitor patients to ensure the tumor does not recur or become malignant. In rare cases, WT can transform into a malignant form known as Warthin`s carcinoma, which requires more
aggressive treatment [32]. The most common treatment for WT involves a partial or complete superficial parotidectomy, although there is controversy over the extent of surgery needed. More recently, extracapsular dissection has become increasingly used. The extent of surgery depends on various factors, and a general guideline for surgical approaches in different clinical settings has been suggested.
4.1 Total Parotidectomy
In recent years, there is a reduced trend of total parotidectomy. However, it can be a viable option in cases with deep lobe involvement or to minimize the risk of hidden deep lobe lesions [33]. Total parotidectomy has the advantage of removing all possible foci of the tumor and reducing the risk of second ipsilateral tumors. However, the potential postoperative morbidity, particularly in elderly patients such as facial nerve palsy, Frey`s syndrome, and poor cosmetic results tend to increase. Mantsopoulos et al. conducted a study to investigate the incidence of permanent facial palsy following different surgical techniques for unilateral multifocal WTs. The study involved a total of 203 patients, out of which, 96 were treated with multifocal extracapsular dissection (ECD) and 107 underwent total parotidectomy. The results of the study showed that the incidence of permanent facial palsy was significantly higher in patients who underwent total parotidectomy (19.6%) compared to those who underwent multifocal ECD (2.1%). [34]. Another study by Choi et al. investigated various surgical options for the management of WT in twenty cases. Their findings showed that the postoperative complication rate was much higher in the parotidectomy group compared to the enucleation group [35].
4.2 Partial Lateral Parotidectomy
Most cases of WTs are at level II which necessitates the utilization of partial lateral parotidectomy as a viable surgical option. Furthermore, partial parotidectomy offers higher chances of salvaging glandular function and avoids palsy of facial nerves. Zhang et al. in their investigation of 268 patients with (n = 163) undergoing partial parotidectomy whereas (n = 105) underwent total parotidectomy. Their findings revealed that the incidence of transient facial paralysis was significantly lower in the partial parotidectomy group compared to the total parotidectomy group [36]. Similarly, the findings from Cheung et al. in patients that underwent partial parotidectomy revealed that 4% of patients had transient facial palsy and 2% had persistent House-Brackmann grade II facial palsy [37]. The authors concluded that a partial parotidectomy
is a viable option for the management of benign parotid tumors. A randomized trial by Koh et al. compared the efficacy of partial parotidectomy versus superficial or total parotidectomy. Their findings showed that partial parotidectomy was associated with shorter surgical duration and complication rates compared to total parotidectomy [38].
4.3 Extracapsular Dissection (ECD)
Extracapsular dissection is low-risk procedure for the removal of benign tumors by blunt dissection through the tissues immediately outside the tumor capsule [39]. Extracapsular dissection has emerged as a favored method for the management of WT in recent years. A study by Lee et al. reported that surgical operation time was significantly shorter in the extracapsular dissection group than in the superficial parotidectomy group (p<.001). They investigated 44 parotid gland operations [40]. Similarly, Witt et al. reported that ECD showed satisfactory results with fewer complications. They assessed 50 cases of WTs with half treated with partial superficial parotidectomy and the other half with ECD [41]. Another retrospective study showed that an extracapsular dissection is an efficacious option in the management of solitary as well as carefully selected multicentric cystadenolymphomas [42].
5. Non-surgical management
Surgical management of WT is associated with several complications, with facial nerve injury being the most recognized adverse outcome [7]. WT is also known for its low rate of malignant transformation and recurrence. The aforementioned factors theoretically favor non- surgical management among the majority of patients. Despite the fact that non-surgical management has been used for decades for other types of neoplasms, there are few papers investigating similar modalities in patients with WT. With the scarcity of reports regarding non- surgical management, it will be of great benefit to gather the current literature concerned with the considerations and outcomes of non-surgical management of WT. This review will provide a clear view of the validity of conservative management and guide future clinical trials.
Although surgical intervention is the main treatment approach for WT, surgical procedure is associated with severe trauma and poorer cosmetic outcomes. The most common complication post-surgical intervention includes infection, salivary fistula, neurological complications, and hematoma [43]. Patients that are unable or unwilling to undergo surgical procedure due to cosmetic
concerns or fear of complications can opt for non-surgical options. Currently, there are several non-surgical modalities including microwave ablation, radiofrequency ablation, and ethanol sclerotherapy for WT. This review addresses the following questions:
• What is the safety and efficacy of different available non-surgical treatment option for WT?
• In what patient groups, the non-surgical management options are suitable and can lead to successful outcomes?
6. Methods
The protocols for this review were devised in adherence to the guidelines prescribed by the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) [44].
6.1. Search Strategy and Data Sources
For this review, comprehensive research was conducted in several databases to find relevant studies that evaluated non-surgical approaches to the management of WT. The systemic search was conducted in PubMed, Web of Science, Cochrane, and Embase libraries databases. The keyword included: Warthin tumor, adenolymphoma, cystadenolymphoma, papillary cystadenoma lymphomatosum, and lymphomatous adenoma. Furthermore, the search also included keywords indicative of conservative non-surgical treatment such as microwave ablation, radiofrequency ablation, and ethanol sclerotherapy. For the current search, case reports, case series, cohort, case control, and clinical trials were included. All the articles were inspected and filtered to include articles on non-surgical management. All age groups of both genders and various demographic characteristics were included in the study. Studies including the comparison between surgical and non-surgical modalities or reports of non-salivary gland neoplasms were included as well. Articles published before the year 2012, non-English, and mixed methodology articles were excluded from the systematic review. Non-surgical approaches that were investigated included microwave ablation, radiofrequency, ultrasound-guided ethanol sclerotherapy, and conservative management.
6.2 Data Collection Process
All the matched articles from database searches were transferred to the reference manager (EndNote, 20 Thomson Reuters) with the exclusion of duplicate and non-English titles. Thereafter,
endnote file was transferred to Rayyan, a web base software to expedite the initial screening of the search results [45]. The further process was divided into three stages: (1) Selection of studies based on title and abstract that was eligible for inclusion in the review; (2) Thorough analysis of the eligible articles keeping in view the aim of the review; (3) Further search was refined based on exclusion and inclusion criteria and data were obtained in form of notes regarding the intervention used in studies, the number of participants, and the methods used.
6.3 Flow Diagram
The study design adheres to the PRISMA flow diagram and protocol [46], outlining the systematic approach from identifying relevant articles to selecting articles that meet the eligibility criteria for further analysis (Fig 1).
7. Results
7.1 Included studies
The literature search provided 5533 potentially relevant articles from PubMed (n=1358), Web of Science (n=1794), Cochrane Library (n=24), and Embase (n=2333) databases whereas 24 articles were selected from the references area of the relevant articles. After the exclusion of duplicate studies and non-English publications, only 1582 records were further analyzed. Based
on keywords and abstracts, 1365 publications were removed from the scope of this review. Of the residual corpus of literature, a thorough assessment was performed to identify the six most relevant studies for inclusion in the scope of the current review.
7.2. Study characteristics
Out of the six studies reviewed, two studies investigated the efficacy of microwave ablation [47, 48], two assessed the safety and efficacy of radiofrequency ablation [49, 50], and two evaluated the safety and efficacy of ultrasound-guided ethanol sclerotherapy (UGES) for WT management [51, 52].
Authors (Year)
Study type
Participants
Interventions
Outcomes
Conclusion
Jin et al. (2019) [47]
Case report
73-year-old man
Ultrasound- guided percutaneous microwave ablation
The ablation procedure length was 2 min and 15 seconds. At one and three- months follow-ups, the reduction in tumor size was 53% and 82%, respectively. The tumor was completely diminished at an 8-month evaluation.
Ultrasound- guided percutaneous microwave ablation has demonstrated safety and efficacy as a non-surgical intervention.
Ji et al. (2022) [48]
Case report
82-year-old male
Ultrasound- guided Microwave Ablation
Following a period of 12 months, there was a noticeable decrease in the size of the parotid nodules on both sides without any signs of recurrence or adverse effects.
Ultrasound- guided Microwave Ablation is a safe and efficacious non-surgical procedure.
Tung et al. (2019) [49]
Case series
7 patients with biopsy- proven parotid Warthin tumors
Ultrasound- guided percutaneous
RF
using moving technique.
ablation the shot
The study found a significant decrease in the average size of tumors, from 14.6 cm3 ± 13.1 to 0.8 cm3 ± 0.5, and an improvement in a cosmetic appearance on imaging studies after RF ablation compared to before (P < .05). The reduction ratios of tumor volume were 51.2% ± 18.1%, 87.8% ± 10.6%, and 94.3% ± 2.0% at 1-2 months, 5-6 months, and 10-12 months after RF ablation, respectively.
RF ablation has demonstrated safety and efficacy as a non-surgical option.
Cha et al. (2021) [50]
Case series
10 patients with Warthin tumors
Radiofrequency ablation (RFA). The mean follow-up was 24.3 ± 13.1 months (range 7-42 months).
RFA was conducted in 11 tumor cases. The highest reduction in size was seen in cystic tumors (77.9%) compared to solid tumors (47.3%). In all patients, marked cosmetics were seen, with visible tumors becoming non-palpable masses.
RFA is a safe and effective non-surgical treatment option for WT.
Mamidi et al. (2021) [51]
Case series
2 patients
Ultrasound- guided ethanol sclerotherapy
A significant reduction in
tumor size was observed. The tumor volume reduction rate (VRR) was 67.30%, 98.32%, and
Ultrasound-
guided ethanol sclerotherapy is an efficacious non-surgical
55.73% in three treated
tumor cases. No complications were reported in both case.
intervention for
WT.
Lee et al. (2022) [52]
Case report
One patient with multifocal Warthin`s tumor.
Two cycles of ultrasound- guided ethanol sclerotherapy.
At one-month follow-up, a decrease in cyst size was observed. A temporary burning sensation was reported after the ethanol injection.
Ultrasound- guided ethanol sclerotherapy can be a viable option for WT treatment.
8. Discussion
8.1 Microwave Ablation (MWA)
Two studies were identified in the literature that discussed microwave ablation for the treatment of WT [47, 48]. A study by Jin et al. described the successful use of ultrasound-guided percutaneous microwave ablation in the treatment of a parotid gland WT. The procedure was performed without any complications and resulted in a significant reduction in tumor volume at both 1- and 3-month follow-ups, with complete resolution of the tumor at 8 months and no recurrence at 2 years. Based on these findings, the authors concluded that MWA is a viable non- surgical option in patients for which surgery is not a suitable option [47]. Similarly, Ji et al. also reported a case of walnut-sized WT in an 82-year-old male patient. The tumor was confirmed by core-needle biopsy as adenolymphoma. The patient underwent ultrasound-guided MWA. At the 12-month evaluation, the volume of WT was significantly reduced without any observable complications [48]. The literature search revealed that MWA can be an option in patients who are older and have multiple underlying comorbidities such as cirrhosis, and renal insufficiency. The findings of both case reports are promising, however, further investigation of this approach in larger patient cohorts is required to establish its efficacy and safety profile.
8.2 Radiofrequency Ablation (RFA)
Radiofrequency ablation (RFA) is a minimally invasive medical procedure used to treat a range of pathological conditions by using high-frequency alternating current to generate thermal energy in order to destroy targeted tissue [53]. This technique utilizes radiofrequency waves to create a field of high-energy electrical current that is delivered via a small, specialized electrode to the affected area. The electrical current causes the tissue to heat up rapidly, leading to cellular destruction through coagulation necrosis which ultimately results in the eradication of abnormal tissue without the need for invasive surgical procedures [54]. The procedure is typically performed under local anesthesia and requires only a small incision to allow the insertion of the electrode into the target tissue. Two case series were found in the literature search [49, 50]. Tung et al. reported a case series of seven patients with biopsy-confirmed parotid WTs who underwent ultrasound guided percutaneous radiofrequency ablation under local anesthesia. The procedures were completed without any adverse events or complications. Only one patient experienced parotitis with hematoma 12 days after the RFA procedure. No facial nerve damage was reported. At 10-12 months after RFA, all tumors showed significant reduction, with a mean volume reduction of 94.3% ± 2.0% [49]. In another case series, Cha et al. investigated the long-term efficacy of radiofrequency ablation (RFA) in WTs. They followed up ten patients for 24± 13.1 months. Their findings showed that cystic tumors demonstrated a higher reduction rate in tumor size compared to solid tumors at one month (77.9% vs. 47.3%) and at 6-months (95.1% vs. 80.6%). In their study, all residual tumors were located in the superficial lobes and depicted no increase in size [50].
8.3 Ultrasound-Guided Ethanol Sclerotherapy (UGES)
Ultrasound-guided ethanol sclerotherapy is a minimally invasive therapeutic technique that involves the injection of ethanol into targeted blood vessels under the guidance of real-time ultrasound imaging [55]. The ethanol injection causes sclerosis of the blood vessel, leading to its permanent closure and subsequent resolution of the associated symptoms. The use of ethanol as a sclerosing agent in this technique has several advantages, including its rapid and complete absorption by the body, low cost, and wide availability [56]. Mamidi et al. assessed the efficacy of ultrasound-guided ethanol sclerotherapy for the management of WT. They reported that their two cases demonstrated a significantly reduced size of WTs including 67.30%, 98.32%, and 55.73% in 3 WT masses. No complication was observed during the management of the patients [51]. In another case study by Lee et al., they represent a case of WT that was managed with partial
parotidectomy and two cycles of ultrasound-guided ethanol sclerotherapy. At one-month follow- up, a decrease in cyst size was observed, however, temporary burning sensation was reported after ethanol injection [52].
9. Conclusion
Warthin tumor is a benign tumor of the parotid gland which has demonstrated the rare possibility of malignant transformation. The tumor is slow-growing, painless, and non-invasive. Diagnosis generally involves a physical examination, imaging modalities, and biopsy investigations. Fine needle aspiration biopsy is a commonly used minimally invasive method for diagnosing WTs, although there is controversy regarding its sensitivity and specificity. Surgical intervention is the standard and effective treatment option for the management of WT. The type of surgery used may vary depending on factors such as the size and location of the tumor, as well as the patient`s age and overall health. The surgical methods can include limited resection (partial parotidectomy) or a more extensive approach (total parotidectomy). However, several minimally invasive techniques such as microwave ablation, radiofrequency ablation, and ultrasound-guided ethanol sclerotherapy have shown promising results in the management of WT. These procedures offer a safe and effective alternative to surgery in cases where surgery may not be suitable or preferred by the patient. These techniques offer several advantages, including reduced morbidity, improved cosmetic outcomes, and shortened recovery times. Patients who are unwilling to undergo surgical procedure, older age, and underlying comorbidities are several considerations for non-surgical treatment modalities. However, further studies are needed to determine the long-term efficacy and safety profile of these techniques in larger patient cohorts. Overall, these minimally invasive techniques provide alternative options for patients who are not candidates for surgical interventions or prefer less invasive treatments.
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Keywords: Parotid gland; benign tumors; cystadenolymphoma, papillary cystadenoma lymphomatosum, adenolymphoma.