Introduction
Being introduced by Martin et al (1) in 1993, the submental artery island flap (SMIF) has seen a lot of experimentation ever since. While it is possible to use the SMIF as a free flap, it is usually harvested as a pedicled regional flap (2). Due to the proximity of the donor site, reconstruction of oral cavity defects is the most frequently used application for the pedicled variant (3,4). However, the pedicle length allows for reconstructing defects from the hypopharynx up to the upper areas of the face as well as the cervical skin (2,3,5-7).
Although the lateral oropharynx and especially the tonsillar region is well within reach of the pedicled submental flap, reconstruction of oropharyngeal defects still remains dominated by free radial forearm flaps, mainly because of them being thinner and offering more flexibility (8,9). Yet, free flaps require a microvascular anastomosis, resulting in an extended duration of time in general anesthesia. A high percentage of head and neck cancer patients are frail or have severe cardiac or pulmonary comorbidities, sometimes limiting the therapeutic options due to increased risk of therapy-associated complications (10,11). Several studies could extensively demonstrate the relationship between comorbidities and complications during and after extended surgical procedures (12-14). Those patients with comorbidities would presumably profit from a reduced duration of surgery and thereby reduced time in general anesthesia. Several studies, including 2 systematic reviews, could already demonstrate a shorter duration of surgery for oral cavity or lateral skull base defects reconstructed with SMIF compared to free flaps (15-21). The same studies could also show no difference between free flaps and SMIF regarding flap loss, partial flap necrosis, donor site dehiscence, wound healing disorder or rate of recurrence (15-21). While the free radial forearm flap still is the working horse for most of head and neck reconstruction, several studies indicate that reconstruction with a SMIF is an almost equivalent alternative in many areas of reconstruction (15,17,22). Moreover, reconstructions using a SMIF were shown to also decrease health care costs compared to free flaps, at least for oral cancer (19). For oropharyngeal reconstruction using a SMIF, however, data is very limited and rarely centered around functionality like swallowing.
Hence, the aim of the present study was to evaluate the oncologic safety and functional outcome regarding swallowing for patients with lateral oropharyngeal carcinoma who were not deemed good candidates for free flap transfer due to severe anesthesiological comorbidities and were therefore reconstructed with a SMIF.
Discussion
This study investigated the use of submental artery island flaps for reconstruction of defects after resection of lateral oropharyngeal carcinoma in patients with severe anesthesiological risk factors. Results were evaluated regarding oncologic outcomes and swallowing function.
Surgical resection of many oropharyngeal carcinoma results in defects that require reconstruction, often because of exposed neck vessels or insufficient soft palate tissue. Several surgical techniques have been developed to reconstruct these defects, with free flaps like the radial forearm flap and the anterolateral thigh flap representing the mainstay because of being thin and pliable (25,26). However, the required microvascular anastomosis leads to a longer duration of surgery, which not every patient can tolerate due to low performance status or severe comorbidities, thus needing a different approach with a regional flap (16).
The SMIF represents an easily available alternative for radial forearm flaps, since its arc of rotation allows for good reconstruction of the lateral oropharynx (2,3). This was reflected in the present study as well, where all locations of the tumor resection could be comfortably reached. No flap loss was seen in this collective, confirming the reliability of the SMIF documented by other authors (2,5,27). The rate of complications (bleeding, partial flap necrosis, donor site healing disorder) was comparable to data in literature regarding both SMIF and RFFF (28), supporting the safety of the SMIF in usage for head and neck defects. This also aligns with previous studies showing no relevant differences in complications between SMIF and RFFF (15,17,22), therefore rendering the SMIF a viable option in head and neck reconstruction.
In the collective investigated, all tumors could be removed with clear margins of at least 5 mm. Accordingly, no local or regional recurrence was observed. There have been discussions about the oncologic safety of the SMIF in oral cancer reconstruction, because the pedicle contains tissue and therefore possibly small lymph nodes of the Level Ib, the main way of lymphatic spread of cancers of the tongue or the floor of mouth (20,27,29). However, until now all available literature hints at no increased risk of local or regional recurrence (20,21,29). For lateral oropharyngeal tumors, even this risk does not apply because of the different levels of nodal spread in this entity, where Level Ib is rarely involved. Hence, the oncologic safety of the SMIF for oropharyngeal cancer seems to be comparable to free flap transfer.
A main focus of the present study was the need for shorter durations of surgery for frail patients with poor performance status or ones with severe comorbidities. With an average of 235 min in general anesthesia (e.g. from intubation until extubation), the duration of surgery was much shorter than compared to standard free flap transfer, even when taking two-team approaches into consideration. Most authors confirm the reduced surgical duration when using a SMIF compared to free flap transfer (15,16,19). A lot of studies could already demonstrate the strong relationship between perioperative complications and comorbidities as well as extensive surgery (14,30,31). Thus, it can be assumed that these patients at risk for perioperative complications due to comorbidities or poor performance status should clearly benefit from using a SMIF rather than free flap transfer in oropharyngeal cancer reconstruction.
Data regarding functional outcomes of reconstruction of oropharyngeal defects with a SMIF remains scarce. While several studies indicate comparable functional results when using a SMIF or a RFFF (16,22), most used dependency on a gastric tube as a surrogate parameter for swallowing function, if any. Phoniatric swallowing examinations were rarely ever conducted. In the present study, 80% of the patients could achieve complete oral intake 10-14 days after surgery and maintained complete oral intake without the need for a gastric tube even during adjuvant radiation. Accordingly, in phoniatric swallowing assessment they achieved a PAS-Score of 2 or better immediately after surgery as well as 1 or better 6 month after surgery. The 2 patients with a PAS Score of 2 and 4 respectively 10-14 days after surgery required a gastric tube which stayed in place during radiation. Main problems were the decreased elevation of the base of tongue and the impaired oropharyngeal transport due to the initially voluminous flap. 6 months after surgery these impairments were greatly reduced with a PAS Score of 1 or better and at least partial oral intake, which completely normalized 12 months after surgery. These functional assessments show that a consistently good swallowing function can be achieved when using a SMIF for lateral oropharyngeal reconstruction.
One factor to note, however, should be the hair growth on the flap in male patients. Most flaps, free or pedicled have some kind of hair growth in man. Due to being in the region of facial beard growth, the donor site of the SMIF has a very thick and dense hair growth. The patient refusing the recommended adjuvant treatment developed dense hair growth enorally with the hair extending into the laryngeal space, causing dysphagia and coughing. This required regular trimming of this enoral hair growth, which is inconvenient for the patient, but at least completely removed the resulting swallowing disorder. Therefore, if using a SMIF, male patients should be restricted to those who, according to the tumor stage, will require postoperative radiation, thereby removing the hair growth in nearly all cases.
The limitations of the present study are its retrospective design with a limited sample size. Also, no control group with similar patients receiving a free flap was included, so the conclusion of non-inferiority is solely based on literature. Hence we can primarily state that the SMIF is a good option for these patients without definitively proving an inferiority/non-inferiority compared to free flaps. Therefore, future comparative prospective studies are required to explore this further. Although a selection bias cannot be excluded, all patients at our institution with these ASA- and ECOG-Scores are primarily treated with pedicled flaps, if the defect can be reached safely with them, reducing this bias as far as possible. The rate of p16-positive tumors (70%) was also higher than in most other collectives, which could be attributed to the high number of non-smoking females in this collective. Additionally, the follow-up of at least 12 months cannot project the oncologic outcome in the following years, though it has to be noted that the vast majority of recurrence occurs in the first 12 months after initial therapy.
We conclude that the SMIF is a viable alternative to the RFFF in reconstructing defects of the lateral oropharynx after tumor surgery, both oncologically and functionally. Additionally, this flap decreases the duration of surgery, making it ideal for patients with high risks of perioperative complications. This could be demonstrated by noting no serious perioperative complications in this collective despite all patients having an ASA-Score of at least 3 and ECOG-Scores of 2 or more. Further studies, preferably in a prospective and randomized design, are recommended to investigate the suitability of the SMIF in high-risk patients.