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ORIGINAL ARTICLE
Year : 2022  |  Volume : 18  |  Issue : 3  |  Page : 612-616

Submandibular gland in squamous cell carcinoma of the tongue: Can preservation during neck dissection be a pragmatic option?


Department of Head and Neck Surgery, Advanced Centre for Treatment Research and Education in Cancer, Tata Memorial Centre, Homi Bhabha National Institute, Navi Mumbai, Maharashtra, India

Date of Submission21-Nov-2020
Date of Acceptance19-Jun-2021
Date of Web Publication15-Jun-2022

Correspondence Address:
Poonam Joshi
Department of Head and Neck Surgery, Advanced Centre for Treatment Research and Education in Cancer, Tata Memorial Centre, Homi Bhabha National Institute, Navi Mumbai - 410 210, Maharashtra
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcrt.JCRT_1661_20

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 > Abstract 


Context: The submandibular glands (SMGs) excision during head-and-neck oncosurgeries lead to significant morbidity and degradation of quality of life (QOL). The preservation of SMGs during head-and-neck oncosurgeries, without affecting oncological safety, will improve QOL by preventing xerostomia in these patients.
Aims: The aim of this retrospective study was to assess the involvement of SMG by malignancy during neck dissection being done for the squamous cell carcinoma (SCC) of tongue and to evaluate oncological safety of SMG preservation in SCC of the tongue.
Settings and Design: The study design was a retrospective analytical study.
Subjects and Methods: The study included 391 patients of SCC of tongue operated at Quaternary oncological center from January 2016 to February 2020. The treatment records of 371 patients were reviewed for demographical data, nodal metastasis, and histopathological involvement of SMG by SCC. The statistical analysis was done using SPSS 22.
Results: A total of 555 necks dissected were assessed, out of which 95 necks dissected were positive for nodal metastasis at level Ib. The SMG was involved by SCC in only two cases, both of which were poorly differentiated SCC. No intraglandular lymph nodes were detected in any of the SMG dissected.
Conclusions: The study showed that involvement of the SMG by SCC of the tongue is not very common, and it may be possible to preserve the SMG during neck dissection in selected cases in SCC of the tongue. The preservation will definitely improve QOL of the patients, as excision of the SMG is one of the prominent factors, resulting in xerostomia.

Keywords: Squamous cell carcinoma, submandibular gland, tongue, xerostomia


How to cite this article:
Joshi KD, Joshi P, Bhati M, Nair S, Chaturvedi P. Submandibular gland in squamous cell carcinoma of the tongue: Can preservation during neck dissection be a pragmatic option?. J Can Res Ther 2022;18:612-6

How to cite this URL:
Joshi KD, Joshi P, Bhati M, Nair S, Chaturvedi P. Submandibular gland in squamous cell carcinoma of the tongue: Can preservation during neck dissection be a pragmatic option?. J Can Res Ther [serial online] 2022 [cited 2022 Aug 10];18:612-6. Available from: https://www.cancerjournal.net/text.asp?2022/18/3/612/347674




 > Introduction Top


The saliva has multiple important roles, which include buffering the oral pH, maintenance of oral and dental health, digestion, lubrication, and microbial action. Almost 90% of total saliva produced is contributed by the major salivary glands and approximately 10% is contributed by minor salivary glands.[1] The submandibular salivary gland (SMG) is a major paired salivary gland, located bilaterally in the posterior portion of the submandibular triangle of the neck. The SMG produces both serous and mucinous secretions, but the majority of the secretion is mucinous.[2] SMG is responsible for the majority of saliva in the unstimulated state, producing almost 70% of total salivary production. However, in a stimulated state, parotid produces 50% of total saliva.[1],[2],[3] The excision of SMG glands can have a tremendous effect on the quality of life (QOL) of the patients. Various studies have reported xerostomia as the major complication after the removal of the SMG.[4],[5]

Conventionally, the SMG is excised in all forms of prophylactic and therapeutic neck dissections being performed for oral cavity squamous cell carcinomas (OCSCCs). Even though the conservative surgeries are constantly replacing the more radical procedures, the conservation of salivary glands has never been included in any of the current nomenclatures. At present, the elective neck dissection is preferred over therapeutic neck dissection in our center. Even N Zero necks in the early stage of OCSCC are being subjected to neck dissection to ascertain higher overall and disease-free survival.[6] This further necessitates the need for preservation of structures that can be spared without jeopardizing the oncological safety in such staging neck dissection procedures.

The aim of present study is to assess the involvement of SMG by malignancy during neck dissection being done for the SCCs of the tongue and to evaluate oncological safety of SMG preservation in SCC of the tongue.


 > Subjects and Methods Top


This retrospective analytical study included 391 patients of SCC of the tongue, operated at a TATA memorial center Mumbai, a quaternary health-care center during the period of January 2016 to February 2020. The online records of all the patients were reviewed for the demographic details, stage of the tongue carcinoma, surgical details, and histopathological findings. The patients with OCSCC of the subsites other than the tongue, previous history of head-and-neck surgery, irradiation, or chemotherapy were excluded from the study. The permission from institutional ethical committee was obtained. The data were recorded and analyzed using SPSS 2.0 software (IBM SPSS® Statistics, New York USA).


 > Results Top


Demographic and other details of the patients included in the study are given in [Table 1]. The appropriate neck dissection was done for all the patients, and contralateral neck was also addressed in 164 patients. A total of 95 necks out of 555 neck dissections were positive for nodal metastasis at level IB and 460 necks were negative for Ib metastasis. The mean number of lymph node detected at Level IB was 3.5 (standard deviation – 1.95, range minimum 0 to maximum 14 lymph nodes). The extracapsular spread at Ib was detected in 60 cases out of 555 necks dissected.
Table 1: Demographic and other details of the patients

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The submandibular gland (SMG) was involved in only two cases [Table 2], and no SMG involvement was detected in 553 cases. Both the cases showing the involvement of SMG had poorly differentiated SCC.
Table 2: Details of cases with submandibular gland involvement by tongue squamous cell carcinoma

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There were no intraglandular lymph nodes detected in any of the specimens. Other pathologies detected in SMG were sialadenitis (1), atrophic gland (1), and lymphocytic infiltration (01).


 > Discussion Top


The cervical lymph nodes have been classified in a manner that correlates with the biology of cervical lymph nodes metastases to achieve standardization of oncological procedures. Level I of cervical lymph nodes is subdivided into Sublevel Ia (submental) and IB (submandibular nodes). This division is on the basis of their different oncobiological significance.[7],[8] The level IB is further subdivided into preglandular, prevascular (anterior to facial vein), retrovascular, retroglandular, and deep mandibular group.[9] Some authors have described the presence of intraglandular group of submandibular lymph nodes.[10] However, the majority of authors could not detect the presence of intraglandular lymph nodes, similar to our finding.[9],[11]

Even though level Ib is one of the primary echelons for nodal metastases for tongue carcinoma, its involvement is less common than other oral cavity subsites and less common than level II involvement.[12] In the tongue SCC, Patil et al. have shown Ib involvement in 14.3% of cases as compared to 71.4% involvement in level II. When compared to other subsites, lower alveolus has the highest rate of Ib involvement (66.7%), followed by buccal mucosa (36.4%) and RMT (35.7%).[13] Fives et al. have mentioned that the tongue SCC has level I involvement in only six percent case, in contrast to other subsites.[11] Malik et al. have shown that 40% (24 out of 60 necks dissected) of dissected necks show Ib positivity. The highest rate of Ib level involvement was present in SCC of the buccal mucosa (75%), while only 37.5% of cases of Ib level metastasis were SCC of the tongue.[14] Similarly, in their audit of IB periglandular lymph nodes in the tongue SCC, Subramaniam et al. found 24% of the patients of OCSCC have their involvement, affecting 40 out of 138 (28.9%), the tongue SCC patients while Nithya et al. found 18% of cases had Level Ib positivity.[15],[16] In our study, 17.2% of the patients of the SCC of the tongue had Ib involvement with 66.7% of these having ECS. Stage I malignancy had no Ib lymph nodes positive, but Stage II, III, and IV had two (0.3%), 11 (1.9%), and 81 (14.6%) Ib level nodes positivity for SCC metastasis, respectively.

The involvement of SMG by the SCC of the oral cavity is not very common. In our study, only two (0.36%) cases of all neck dissection specimens examined were having SMG involvement [Table 2].

There is extensive literature available on the SMG involvement by SCC of the oral cavity. The proposed mechanism is by direct extension/invasion (66%–100%), from lymph node metastases in level Ib (0%–1.5%), extension along Wharton's duct, and hematogenous route.[9],[11] The incidence of SMG involvement in literature is given in [Table 3].
Table 3: Literature review for submandibular gland involvement in squamous cell carcinoma of the oral cavity

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The SMG excision can have a tremendous effect on QOL after surgery. Jaguar et al. have shown in their study that submandibular excision has a more significant effect on unstimulated salivary flow as compared to radiotherapy and/or chemotherapy group. In their study, xerostomia was more common in surgery group.[21] Similar effects have been shown by Cumming DM et al.[22] It is imperative that an effort should be made to preserve SMG in head-and-neck carcinoma patients, when it is not involved by malignancy.

Seikaly-Jha procedure (SJP) has been described for sparing the SMG, particularly in oropharyngeal and hypopharyngeal cancers.[23] The SJP constitutes transferring the SMG to submental area by free microvascular transfer or based on distal blood flow.[3],[24],[25] This salivary gland preservation technique is effective against xerostomia by preserving the gland and preventing radiation injury.[23],[26] The modification of the SJP is more suitable for the SCC of the oral cavity with due consideration to oncological safety and sparing the gland more effectively. In this procedure, the SMG is transferred to the parotid region.[27] A minimally invasive intraoral technique has also been described, which can be utilized if neck dissection is being performed by a nonconventional method or primary radiotherapy is being planned.[28]

Zhang et al. have utilized the conventional SJP in cases of the oral cavity, oropharynx, and nasopharynx, in which 8.3% of patients developed cervical node metastases in the transferred side with no recurrence in the submental area. The xerostomia and thus QOL were significantly better in patients on whom SJP was performed.[29] Zeng et al. also preserved the SMG in the SCC of the oral cavity and utilized the SMG flap for reconstruction of oral cavity defect in the 15 cases, without any recurrence during a follow-up period of 14.2 months.[30]

Lanzer et al. have raised several concerns about recurrence-free survival in their study. They did not found intragladular lymph nodes but found lymph vessels in proximity to the SMG. The role of these lymph vessels as a reservoir of the cancer cells is a possibility to be considered. They also postulate incomplete removal of perifacial lymph nodes if the SMG preservation is carried out. The possibility of leaving an involved SMG is also there. Their further argument about the futility of sparing the SMG (which will eventually have permanent dysfunction after radiotherapy) requires more evidence.[31]

There are concerns that transferred the SMG cannot be completely spared from conventional radiation. However, there are evidence that gland functions recover partially, if not fully following the conclusion of radiotherapy.[32],[33] With the advent of newer technologies such as IMRT and IGRT, SMG preservation may be tried. Juloori et al. have tried preservation of SMG function by selectively sparing the SMG when Level Ib is included in radiation target volume with IMRT without any Level Ib failure.[34]

One concern regarding the presence of intraglandular lymph node in transferred SMG and causing nodal failure subsequently can be mitigated by careful preoperative imaging. Even though the presence of intraglandular lymph node is not established, few studies mention their existence.[10] High-frequency ultrasound can be an efficient and cost-effective tool for this purpose.[35]

Despite several studies on the subject, a clear direction is yet to be formed for the SMG preservation in head-and-neck carcinomas. We propose that the SMG preservation may be tried in carefully selected patients of the SCC of the tongue. It is clear from the above literature that, among oral cavity subsites, the tongue seems to have the lowest level Ib nodal metastases and the SMG invasion from level Ib metastases is a common route for SMG involvement. Hence, it might be feasible to preserve the SMG in carefully selected patients of the SCC of the tongue compared to other oral cavity subsites. In bilateral neck dissection, the opportunity to save the contralateral SMG should be sought, especially in N0 neck.


 > Conclusion Top


The SMG can be preserved in early stage carcinoma where chances of nodal metastases are minimal, where R0 resection is possible even after preservation of the SMG, with cost-effective utilization of imaging and intraoperative frozen section.

Certain conditions where it is not advisable to preserve SMG presently due to insufficient evidences are:

  • Node positive neck
  • Advanced malignancy with high-risk features
  • Intragladular lymph node detected in preoperative imaging.
  • Ipsilateral SMG in advanced CA Tongue
  • Atrophic gland/Sjorgen disease/Sialadenitis
  • Patient with the previous history of radiotherapy
  • In the presence of distant metastases.


The present study has tried to provide the necessary inputs for future prospective research work in the field of the SMG preservation in head-and-neck carcinomas, especially SCC of the tongue.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
 > References Top

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Malik A, Joshi P, Mishra A, Garg A, Mair M, Chakrabarti S, et al. Prospective study of the pattern of lymphatic metastasis in relation to the submandibular gland in patients with carcinoma of the oral cavity: Pattern of Lymphatic Metastasis in Relation to the Submandibular Gland. Head Neck 2016;38:1703-7.  Back to cited text no. 14
    
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Subramaniam N, Balasubramanian D, Reddy R, Rathod P, Murthy S, Vidhyadharan S, et al. Determinants of level Ib involvement in oral squamous cell carcinoma and implications for submandibular gland-sparing neck dissection. Int J Oral Maxillofac Surg 2018;47:1507-10.  Back to cited text no. 15
    
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