AbstractObjectives. A novel J-shaped anterolateral thigh (ALT) flap reconstruction technique was developed to simultaneously restore swallowing and speech functions in patients following total laryngopharyngectomy. This study aimed to assess the outcomes and surgical complications in patients who underwent J-flap reconstruction over time.
Methods. Patients who underwent J-shaped ALT flap phonatory tube reconstruction were enrolled. Surgical morbidities and outcomes were evaluated every 3 months post-surgery for a period of 12 months or until death.
Results. Of the 36 patients, 13 underwent circumferential pharyngeal wall resection (circumferential defect [CD] group), and 23 underwent partial resection (partial defect [PD] group). After 12 months, 97% of the patients were able to resume oral intake without the need for a nasogastric tube, and 50% achieved fluent speech using the reconstructed phonatory tube. The CD group experienced a higher rate of delayed healing than the PD group (30.8% vs. 0%, p=0.012). Additionally, the PD group showed significantly higher percentages of individuals consuming solid food at both the 3- and 12-month intervals than the CD group (81.0% vs. 23.1% and 78.9% vs. 40%, respectively).
Conclusions.This study investigated the progression of speech and swallowing functions over time after reconstruction of the voice tube with a J-flap. Using a J-shaped ALT flap phonatory tube effectively restored both speech and swallowing functions, providing long-term benefits, regardless of whether the defect was circumferential or partial.
INTRODUCTIONWith the advent of organ-preservation treatments, total laryngopharyngectomy (TLP) has become the preferred management option for advanced laryngopharyngeal cancers. Although it is possible to effectively remove tumors with adequate safety margins, reconstructing and restoring throat function continues to be a significant challenge. The variety in the types and sizes of defects necessitates specific reconstruction plans, and outcomes may differ even when the same free flaps are used for different defects [1,2].
Traditionally, most pharyngolaryngeal defects have been reconstructed using either radial forearm or free jejunal flaps [2-4]. Disa et al. [2] recommended free jejunal flap reconstruction for circumferential defects and radial forearm flap reconstruction for partial defects. However, due to significant donor site morbidity associated with jejunal flaps and a high fistula rate in radial forearm flap reconstructions, the anterolateral thigh (ALT) flap has become increasingly popular for pharyngolaryngeal reconstruction. It is versatile enough to be used for both types of defects [5-9]. Despite this, conventional reconstruction methods have primarily focused on restoring the food conduits, often overlooking the need for voice restoration. Our team has developed a novel approach using a J-shaped ALT flap [10]. This innovative technique not only aims to restore swallowing and speaking functions in patients who have undergone TLP but is also suitable for reconstructing both circumferential and partial hypopharyngeal defects [10-12].
Postoperative morbidity can vary depending on the type of hypopharyngeal defect. A previous study reported that patients who underwent ALT food conduit reconstruction experienced a higher fistula rate when they had partial defects compared to those with circumferential defects [9]. This could lead to long-term swallowing complications. These findings suggest that the presence of residual hypopharyngeal mucosa following radical TLP may affect functional outcomes.
To thoroughly assess the effectiveness of J-flap reconstruction, a prospective follow-up study is essential. This study would monitor changes in speech, swallowing performance, and quality of life. The current study aimed to evaluate and compare changes in speech and swallowing function over time in patients with circumferential and partial laryngopharyngeal defects following J-flap reconstruction, providing valuable insights for clinical practice.
MATERIALS AND METHODSThis study was approved by the Institutional Review Board of the Chang Gung Medical Foundation (No. 202102100B0, 202002169B0, and 201701936B0). It adhered to the Helsinki Declaration, safeguarding the human rights of its subjects. Prior to participation, informed consent was obtained, ensuring understanding of the study’s purpose and potential risks. Measures were in place to prevent coercion and protect the privacy of all participants. The study upheld strict ethical standards, prioritizing the welfare and dignity of all individuals involved.
Patients diagnosed with laryngopharyngeal cancer underwent TLP with J-shaped ALT flap phonatory tube (PT) reconstruction at a tertiary referral medical center between 2018 and 2022. Patient outcomes were evaluated, including various complications such as delayed healing at the neopharynx anastomosis, esophageal leakage, flap necrosis, and esophageal stenosis, within the first year following surgery. A prospective evaluation of speech, swallowing status, and related quality of life was conducted for up to 12 months post-surgery.
Flap reconstruction and pharyngeal wall preservationThe J-shaped ALT flap consists of two parts: a trapezoidal section (TS) for pharyngeal reconstruction and a distal phonatory tube section (PS) for phonatory tube creation (Fig. 1A). The PS was deepithelialized to create a curved central slip with a widened tail, and the de-epithelialized flap was tubularized into the shape of a J, forming the voice tube. A catheter was then inserted to maintain tract patency during the healing process (Fig. 1B). The proximal end was connected to the neopharynx, and the distal part of the tube was fixed laterally (either left or right) to the stoma. The TS design for food conduit reconstruction was based on defects in the pharyngeal wall. In cases with partial defects in the residual hypopharyngeal mucosa, the TS flap was anastomosed side to side with a patched pharyngeal wall (Fig. 1C and D). In the circumferential hypopharyngeal wall resection subjects, the TS flap was rolled up as a tube transversely and approximated with distal and proximal stumps (Fig. 2). For detailed information, please refer to our previous studies [10-12].
While producing sound, the patient blocked the stoma’s opening with their thumb, redirecting air into the PT (Fig. 3). The vibrations of air movements within the PT and neopharynx then resonated along its walls. The sound then conducted to the oral cavity, where the movements of the tongue and lips formed it into intelligible speech. A video showing a patient performing the “Happy Birthday” song following J-flap reconstruction for a laryngopharyngeal defect is provided (Supplementary Video 1).
AlimentationThe patients’ post-reconstruction dietary intake and status were documented by observing whether they followed an oral diet or relied on a nasogastric tube (NG tube) for feeding. Additionally, we recorded the number of patients in both groups who consumed a regular oral diet without limitations or need special preparation after surgery.
Quality of life measurementsPatients’ quality of life was measured using the EORTC QLQ-H&N35, a 35-item questionnaire specifically designed by the European Organization for Research and Treatment of Cancer (EORTC) to assess symptoms in patients with malignant head and neck tumors. The questionnaire includes seven multi-item scales and 11 single-item symptom scales. All questions were stored and analyzed using a scoring system ranging from 0 to 100. For the symptom scales, a score of 100 signified a heavy burden, indicating severe symptoms or difficulties in that aspect of life. These versions have been approved as valid measurement tools [13].
The scales for swallowing, speech, and social eating in the EORTC QLQ-H&N35 questionnaire were selected to specifically assess difficulties in swallowing and speech, particularly after surgical interventions. The swallowing scale encompasses four items that assess different degrees of swallowing challenges: problems with swallowing liquids, pureed foods and solid foods, and the occurrence of choking while swallowing, denoted as hn5–hn8, respectively. The speech scale evaluates hoarseness and communication difficulties in talking to other people or on the phone, designated hn16, hn23, and hn24, respectively. Additionally, the social eating scale consisted of four items, including trouble eating, trouble eating in front of family, trouble eating in front of others, and trouble enjoying meals, indicated as hn19–hn22, respectively.
Statistical analysisSPSS for Mac 21.0 (IBM Corp.) was used for the statistical analysis. Data are expressed as mean±standard deviation. The Mann-Whitney U-test was used to compare continuous data, and Fisher’s exact test was used to compare categorical data between groups. The overall survival rates of the three groups were compared using the Kaplan-Meier method, and differences were measured using the log-rank test. Statistical significance was set at P<0.05.
RESULTSThirty-six consecutive patients were enrolled and continuously followed up after surgery for a minimum of 12 months, with an average follow-up duration of 31.44±15.03 months and a maximum of 56.5 months. Among these patients, five had primary laryngopharyngeal cancer, while the remaining 31 had recurrent cancer. During the surgical procedures, 23 patients underwent partial resection of the posterior pharyngeal wall (partial defect group [PD group]), and 13 underwent circumferential resection of the same area (circumferential defect group [CD group]). Patient characteristics, including tumor site and stage, preoperative tracheostomy, feeding tube dependency, and preoperative and postoperative radiotherapy status, are detailed in Table 1. In the PD group, nine patients (39.1%) were diagnosed with hypopharyngeal cancer, with the rest diagnosed with laryngeal cancer. All 13 patients (100%) in the CD group had tumors originating in the hypopharynx. No significant differences were found between the two groups regarding the percentages of primary versus recurrent cases, tumor stage, or preoperative and postoperative chemoradiotherapy status (P=0.63, P=0.14, P=1.0, and P=0.69, respectively).
The rate of preoperative feeding tube dependency was significantly higher in the CD group than in the PD group, at 53.8% compared to 13.0% (P=0.018). However, the preoperative tracheostomy rates showed no significant difference between the two groups. Flap sizes were notably larger in the CD group than in the PD group, with the total flap size measuring 201.85±26.20 cm² in the CD group and 163.30±22.22 cm² in the PD group (P<0.001). Specifically, regarding flap design, the TS component used for pharyngeal reconstruction was significantly larger in the CD group than in the PD group (91.08±14.53 vs. 57.30±13.29, P<0.001) (Figs. 1 and 2). Conversely, in the creation of PT, the size of the PS flap showed a significant difference between the two groups. The 3-year overall survival rates were 81% in the PD group and 63% in the CD group (P=0.55).
The occurrence of individuals capable of fluent speech, indicating effective communication through PT speech, was compared between two groups at 3, 6, 9, 12, 18, and 24 months post-surgery. Although the rate was slightly higher in the PD group than in the CD group within the first 12 months postoperatively, the incidence was comparable between the two groups at 18 months, with a higher prevalence observed in the PD group at 24 months. However, these differences were not statistically significant (Fig. 4A). Four patients in the CD group demonstrated delayed healing at the neopharynx anastomosis, as indicated by an esophagogram conducted two weeks post-surgery, which revealed barium leakage; however, no such cases were observed in the PD group (30.8% vs. 0%, P=0.012). Nevertheless, all patients had recovered spontaneously by the 1-month follow-up exam. Episodes of esophageal fistula requiring surgical repair within 1 year post-surgery were also more frequent in the CD group than in the PD group (30.8% vs. 4.3%, P=0.047). One patient in the study initially experienced delayed healing at the neopharynx anastomosis and subsequently developed episodes of esophageal fistula during the 1-year follow-up period. The percentage of patients with esophageal stenosis within 1 year post-surgery was not significantly different between the CD and PD groups (13.0% vs. 15.4%, P≥0.05) (Fig. 4B).
After 12 months, 97% of the patients were able to resume oral intake without relying on an NG tube. In terms of individuals consuming a regular oral diet without limitations or the need for special preparation, the PD group exhibited significantly higher percentages at both 3 and 12 months post-surgery compared to the CD group (81.0% vs. 23.1% and 78.9% vs. 40%, P=0.001 and P=0.047, respectively) (Fig. 4C). The swallowing, speech, and social eating scales in the EORTC QLQ-H&N35 pertain to difficulties with swallowing and speech (Table 2). Measurements of quality of life related to speech and swallowing showed no statistically significant differences between the CD and PD groups during follow-up.
DISCUSSIONReconstruction was performed based on the surgical defect following laryngopharynx excision. According to Disa’s classification, the surgical defects were categorized as partial (less than 50% loss), circumferential, and extensive [2]. Reconstruction of the alimentation tract for each type of defect can be achieved using a specific free flap [2]. However, complications at the donor site, such as abdominal spasm or contracture, persist, and an ideal soft tissue flap has not yet been identified. Since its introduction, the ALT flap [5,6] has become the preferred tissue for head and neck reconstruction. The advantages of an ALT flap include reliable and consistent anatomy, a long vascular pedicle, a considerable distance from the ablative site, allowing for a two-team approach, and minimal donor site morbidity [14]. Even in cases of extensive pharyngolaryngeal defects, the ALT flap can be effectively used for reconstruction [6].
Previous reports have shown that autologous tissue laryngopharyngeal reconstruction has primarily been aimed at restoring the food conduit [2,9,15-17], disregarding the need for voice reconstruction. Various techniques have been developed to restore voice and speech functions in patients after laryngopharyngectomy. These include esophageal speech, tracheoesophageal prostheses (TEPs), and external voice devices such as the electrolarynx, which have been in use for many years. More recently, there has been growing discussion about the use of microsurgical free flaps for the restoration of speech and voice functions [10,18,19]. The ability to communicate verbally after surgery plays a crucial role in a patient’s reintegration into social life, which is a significant concern prior to surgery. Consequently, recent advances in reconstruction and the restoration of speech functions have increased patients’ willingness to undergo radical laryngopharyngectomy. The J-flap was specifically designed to simultaneously restore speech and swallowing functions, offering a promising avenue for improving patients’ quality of life. Previous studies have extensively analyzed voice characteristics and compared them with those of pneumatic devices and TEPs [10-12]. The advantages and disadvantages of J-shaped ALT flap reconstruction, based on personal experiences, are detailed in Table 3.
The outcomes and performances post-reconstruction have been reported to vary among different types of laryngopharyngeal defects [1,9,20,21]. In our cohort, we observed a significantly higher incidence of delayed healing in the CD group compared to the PD group following J-flap reconstruction. Additionally, leakage from the esophageal fistula tended to occur more frequently in the CD group than in the PD group, which is contrary to previous reports [7,9]. According to the initial experiences reported by Yu et al., after ALT alimentary reconstruction, the esophageal fistula rate was higher in patients with partial defects (29%) than in those with circumferential defects (8%) [9]. However, a larger cohort series study reported a lower fistula rate and found no significant differences between the groups [7]. Our results are consistent with those of a recent meta-analysis on ALT alimentary tract reconstruction, which showed a higher fistula rate in patients with CD (19.2%) compared to those with PD (9.4%) [1]. In patients with a partial hypopharyngeal defect, the J-flap was placed over the residual mucosa and secured with sutures on both sides, as well as at the upper and lower end anastomoses. We hypothesized that the blood perfusion from the remaining hypopharyngeal mucosa provides a more favorable microenvironment for the cutaneous-mucosa connection, a feature that is absent in circumferential defect reconstruction (Fig. 2). Furthermore, for circumferential defect reconstruction, the TS required for food conduit reconstruction must be larger. However, despite the increased demand for tissue, the available blood perfusion is often insufficient to adequately nourish a larger tissue supply, potentially leading to delayed healing or fistula formation. This may be one of the factors contributing to the lower rate of regular oral diet consumption without limitations or the need for special preparations in patients with CD (Fig. 4C).
The mode of communication differs between patients who undergo total laryngectomy (TL) and those who undergo TLP [22], indicating that the size of the defect and the methods of reconstruction can affect speech and voice production. Patients can regain their ability to communicate verbally using voice prostheses, TEP, or autologous tissue reconstruction [18]. TEP is commonly used for laryngeal communication. A previous report [7] found that 55% of patients were unable to undergo TEP following laryngopharyngectomy with ALT alimentary tract reconstruction, citing various medical or social reasons. The use of TEP is further constrained by complications such as Candida infection, tracheoesophageal leakage, and the necessity for frequent replacements [23]. After laryngopharyngectomy, the intelligibility of speech in patients with TEP is lower than in those who have undergone TL, leading to a diminished quality of life [20].
From our study on J-flap hypopharyngeal reconstruction, 97% of patients resumed oral diets, and 50% achieved fluent speech by the 12-month follow-up, comparable to patients with TEP [1,7,23,24]. The results indicated that speech and swallowing functions were similar to or better than those observed with other methods, without associated drawbacks [1,4]. Additionally, the speech- and swallowing-related quality of life, assessed using the EORTC H&N35, showed no significant differences between the two groups. We propose that the surgeon’s experience and preferences continue to play a crucial role in the excision and reconstruction processes. Some surgeons opt for a circumferential excision of the entire hypopharyngeal mucosa in cases of advanced laryngopharyngeal cancers [25]. However, findings from this study indicate that preserving the pharyngeal mucosa aids in the healing of the J-flap and reduces morbidity. Considering the lower morbidity rate observed in patients with PD, we recommend, where feasible, that preserving the pharyngeal mucosa is beneficial for patients prior to undergoing TLP.
This is the first prospective study to compare outcomes following J-flap reconstruction for both circumferential and partial hypopharyngeal defects. However, several limitations should be noted. First, the findings are based on the experience of a single team and should be cautiously extrapolated. A well-coordinated surgical team can reduce morbidity rates. As with other innovative techniques, it is crucial to ensure that the procedure is performed by well-trained individuals. Second, although there appeared to be a higher rate of alimentary morbidity following
J-flap reconstruction in the CD group than in the PD group, this observation may be limited by our sample size. A study with a larger sample size and a longer follow-up period is necessary. However, when there are no oncological reasons necessitating complete circumferential excision of the hypopharyngeal mucosa, preserving adequate mucosa can be beneficial for flap wound healing.
This study examines the longitudinal changes in speech and swallowing function following reconstruction with a J-flap voice tube. Compared to the conventional jejunal or fasciocutaneous flap with TEP, the speech outcomes in this cohort were comparable to those reported previously. The J-flap provides numerous advantages for laryngopharyngeal reconstruction. It effectively restores both speech and swallowing functions, whether the defect is circumferential or partial, offering sustained benefits.
HIGHLIGHTS▪ J-flap reconstruction effectively restores both speech and swallowing functions in patients with laryngopharyngeal cancer.
▪ Patients with partial and circumferential defects showed similar speech/swallowing improvements post-surgery.
▪ Preserving the pharyngeal mucosa during surgery facilitated the healing of the J-flap and reduced complications.
▪ Longitudinal follow-up has demonstrated the benefits of J-flap reconstruction on speech and swallowing functions.
NotesAUTHOR CONTRIBUTIONS Conceptualization: CKT, TJF. Methodology: YAL, HFC, TJF. Formal analysis: YAL, LJH, TJF. Data curation: YAL, CKT, TJF. Visualization: YAL, TJF, CKT. Project administration: LJH, TJF. Funding acquisition: TJF, CKT. Writing–original draft: YAL, TJF. Writing–review & editing: YAL, CKT, TJF. All authors read and agreed to the published version of the manuscript. ACKNOWLEDGMENTSThis research was supported by a Ministry of Science and Technology grant (MOST110-2314-B-182A-144, MOST111-2314-B-182A-107, and MOST112-2314-B-182A-025-MY3 for data analysis and MOST112-2314-B-182A-025-MY3 for language editing).
The authors thank Miss Xin-Ci Zhan, Li-Yun Lin, and Chia-Chun Lee (Department of Otolaryngology-Head and Neck Surgery, Linkou Chang Gung Memorial Hospital, Taoyuan, Taiwan) for collecting the data.
SUPPLEMENTARY MATERIALSSupplementary materials can be found via https://doi.org/10.21053/ceo.2024.00109.
Table 1.
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