Division of Reconstructive Surgery, Head and Neck Institute, Amrita Institute of Medical Siences, Kochi , Kerala, India

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1 Free full text on Reconstruction of the laryngopharynx Daxesh Patel, Moni Abraham Kuriakose, Subramania Iyer Division of Reconstructive Surgery, Head and Neck Institute, Amrita Institute of Medical Siences, Kochi , Kerala, India Address for correspondence: Dr. Subramania Iyer, Division of Reconstructive Surgery, Amrita Institute of Medical Sciences, Kochi , India. subu@aims.amrita.edu ABSTRACT KEY WORDS Defects in the laryngopharynx following surgical excision of the tumors can be involving either part or full of the circumference of the lumen. The methods of reconstruction use skin or mucosal lined surface, which have their own merits and demerits. Advent of free ß aps have given the surgeon choice of multiple ß aps which could take their place instead of a gastric pull up which entails mediastinal dissection. The article reviews the methods available and discusses the relative merits and indications of these, in partial and full lumen reconstruction of the laryngopharynx. Loss of the capacity to speak is a grave morbidity associated with these procedures and there have been signiþ cant advances in the rehabilitation of speech after laryngectomy. The current status of the methods of speech rehabilitation is discussed in detail. The reader will at the end, be presented with an algorithmic approach to choose the method of reconstruction depending on the size and site of the defect, as practiced the authors service. Laryngopharyngeal cancers, laryngopharynx reconstruction, post laryngectomy speech rehabilitation C Carcinoma of the laryngopharynx is one of the common head and neck cancers accounting for 10-14% of head and neck cancers. Surgical treatment remains the mainstay of the treatment in a large number of cases, though the early lesions can be treated with radiation therapy with or without chemotherapy, thereby preserving the function of the larynx. The surgical treatment entails removing the larynx, functionally one of the most developed and intricate organs of the body. Reconstructive surgery of the laryngopharyngeal defects needs a thorough understanding of the anatomical and functional requirements of the defects created, as well as judicious application of reconstructive methods. Finally, functional rehabilitation also requires good knowledge of the methods of rehabilitation of voice production. This review will aim to address these issues in brief. ANATOMY OF THE LARYNGOPHARYNX The laryngopharynx is defined as the area of the pharynx starting from the level of the inferior border of the tonsils to the inferior border of the cricoid cartilage and has the pyriform fossa of either side, lateral pharyngeal wall or the post cricoid region as the subsites. The pharyngeal tube in this area mainly comprises anatomically the mucosa and the circumferential pharyngeal musculature, namely the middle and inferior constrictor with the cricopharyngeal sphincter forming the lowermost portion of the latter. The larynx projects into the laryngopharynx from the front thereby forming the pyriform fossa on either side. Even though a separate region from the oncological aspect, the larynx is anatomically and functionally intimately related with the pharynx. Loss of its function is certain in most S44 44 CMYK

2 Laryngopharyngeal reconstruction instances of surgical treatment of the cancers. The history of laryngopharyngeal reconstruction starts with Wookey in 1942 who described a procedure using the neck skin tabularized in two stages to form the food conduit. [1] The next significant advancement was the description of the deltopectoral flap by Bakamjian in 1965, [2] which also was a two-staged method. The pectoralis major myocutaneous flap, which was described in 1979, [3] soon became the workhorse and still remains so in many centres. There was simultaneous progress in the use of visceral flaps like colon and stomach, which necessitated an oesophagectomy also, often benefiting the clearing of the disease. The next significant development was the advent of free flaps, both cutaneous and visceral, like radial forearm, anterolateral thigh and jejunum, which dominate the literature now. [4-10] ANATOMICAL AND FUNCTIONAL REQUIREMENTS The surgical treatment of laryngopharyngeal cancers leads to two major anatomical defects i.e., defect of the pharyngeal lumen leading to a partial or total discontinuity of the alimentary passage and removal of the larynx resulting in the total discontinuity of the airway. The former results in the impairment of deglutition. The removal of the larynx results in the loss of the function of speech and the cessation of nasal breathing. It also leads to a creation of a permanent tracheotomy. The reconstruction of the alimentary tract for either a patch defect or a full circumferential defect has become easier and more definite, with the progresses made in reconstructive surgery. No method has been evolved to replace all the functional aspects of the larynx, especially the restoration of nasal airways and avoiding a permanent tracheotomy. Much progress has been made in the rehabilitation of the function of speech after laryngectomy. The goals of reconstruction, hence can be discussed as: A) Reconstruction of the pharyngeal defects 1) Partial defects (patch defects) 2) Circumferential defects B) Reconstruction and rehabilitation of speech Total laryngectomy done for cancer of the larynx usually leads only to a partial pharyngeal defect, which can be closed primarily. But when the disease involves the surrounding laryngopharyngeal mucosa of the pyriform fossa and lateral pharyngeal wall the resultant defect in the pharyngeal wall will be larger and need reconstruction of a patch of mucosa. Another uncommon indication for reconstruction of a patch of pharyngeal wall is defects resulting from resection of an isolated posterior pharyngeal wall cancer. But disease arising from the post cricoid region or involving it extensively may require replacement of the full circumference of the pharyngeal tube. Reconstruction of partial defects Partial defects of the pharyngeal lumen can be covered by a small patch of skin or mucosa. [4,11] The ideal requirement is mucosa, but skin patches also work well provided the flap does not have too much of hair growth. The skin flaps which can be used include a pectoralis major myocutaneous flap (PMM) or free flaps like the radial forearm or anterolateral thigh flap. The advantage of a PMM flap is that the muscle pedicle often helps to cover the great vessels of the neck exposed in the neck dissection as well as the fact that it is much quicker to execute. The flap is quite reliable because of the limited length of movement required for the pedicle to reach the Laryngopharynx, thus permitting the siting of the skin paddle on vascular areas over the muscle [Figures 1a, b]. The immediate and long-term morbidity for use of this flap has been reported to be much less when compared to free flaps and hence is the method of choice in these defects in most of the reports. [11] The advantage of using free flaps like the radial forearm flap is only in situations where the defect is extensive or when there is a composite defect needing skin cover also [Figures 2 a, b]. If the PMM flap is used in such instances where bipaddling is necessary, a more safe method is to use split-thickness skin grafts over the surface of the muscle for the skin cover. Reconstruction of circumferential defects Circumferential defects result after total laryngopharyngectomy performed for post cricoid cancers or extensive pyriform fossa cancers. The reconstruction needs creation of a full tube of mucosa or skin from usually the base tongue region to the level of the manubrium. The methods of reconstruction available can be grouped into those which provide mucosa or skin, both of which could be either as free or pedicled transfer. Mucosal tubes Pedicled- Free Gastric pull-up jejunum; colon S45 CMYK45

3 Patel, et al. Figure 1a: PMM ß ap outlined for covering a patch defect in the hypopharynx Figure 1b: PMM ß ap being inset in the patch defect Skin tubes Pedicled Free Mucosal flaps Advantages Lubricated Tubed PMM flap RFF; ALT flap Less chances of stricture Hair growth is not a problem Disadvantages Need of abdominal surgery More morbid Skin-lined flaps Advantages Can be pedicled or free Surgical and donor morbidity is much less Figure 2a: Recurrent laryngopharyngeal lesion needing full-thickness excision Figure 2b: The resultant defect covered with bipaddled radial forearm ß ap Disadvantages Immediate leaks more Delayed problems of hair growth and stricture VISCERAL MUCOSAL TUBES Mucosal flaps provide a lubricated food passage and hence show better swallowing function. [12] The problem of hair growth that is present in skin-lined tubes is avoided and chances of stricture may be lesser. But the major disadvantage of using the visceral mucosal tubes is that it requires an abdominal surgery leading to an increased morbidity and with gastric pull-up procedures the attendant mediastinal dissection adds to the morbidity. The viscera are less tolerant to ischemia and hence while using them as free flaps considerable experience needs to be gained before they are accepted as the method of choice of reconstruction S46 46 CMYK

4 Laryngopharyngeal reconstruction to be performed by the surgeon. Stomach pull-up The technique of gastric pull-up has been one of the oldest methods described and is commonly practised for post laryngopharyngectomy reconstruction. [13] The stomach is mobilized and based only on the right gastro-epiploic and right gastric vessels, the hiatus in the diaphragm is enlarged and the oesophagus is mobilized from its bed through dissection from above and below. The resected larynx and the oesophagus are now pulled into the neck and transected at the gastroesophagial junction, and the tumour-bearing larynx/pharynx with the oesophagus is removed [Figure 3]. The stomach is pulled up to make its fundus reach the upper pharyngostome. The cut end of the oesophagogastric junction is relatively narrow and has presence of sphincter. Hence this is closed and a new opening is made in the region of the fundus sufficiently wide to match the large pharyngeal cut end, and anastomosis of the stomach to the pharyngeal opening is done. Mediastinal complications are the most worrying problems associated with gastric pull-up. A postoperative chest radiograph is mandatory and insertion of a chest tube may be needed. In order to reduce the mediastinal morbidity, the use of a stripper has been described to separate the oesophagus thus avoiding blunt dissection. [14] A technical problem may arise infrequently due to the inadequate length of the gastric tube, making it difficult to achieve a tension-free suture with the upper pharyngostome. This may be avoided with further careful mobilization of the stomach and careful surgical lengthening of the stomach. The main advantage of stomach pull-up over other methods is that there is only one bowel suture line with least chances of stricture formation and providing a wide lumen [Figure 4]. The entire oesophagus is removed allowing removal of any skip lesions, which have been reported up to 58% [15] and it requires no vascular anastomosis. But the major disadvantage in long-term follow-up is the reflux of gastric contents, which will be more in these patients as all the sphincters become stretched or removed. [16] Jejunal segment transfer Transfer of jejunal loop based on its vessels was first described for hypopharyngeal reconstruction by Seidenberg in 1959 [6] and later put into clinical practice by Jurkiewicz. [7] A loop of jejunum is selected which will give an adequate length and has a clear arcade of vessels arising from a branch of the superior mesenteric artery and vein [Figures 5 a-d]. A sentinel loop can be fashioned, supplied by one of the branches of the same arcade, which is kept outside for monitoring. Care is taken to keep the jejunal segment in an isoperistaltic way in the neck. The jejunal flaps do not stand ischemia for a long time; hence the transfer has to be accomplished without unnecessary delays. The flaps do less well than gastric pull-up in relation to stricture formation. Excess visible peristalsis and mucous production are minor disadvantages for jejunal flaps. Other visceral flaps that have been described for pharygolaryngeal reconstruction include ascending colon with the appendix used as a speech conduit [9] and tubed gastro omental flaps. The gastro omental flaps have been reported to be the flaps of choice in salvage of chemoirradiated patients, since the omentum acts as a sturdy protective cover to prevent vascular and anastomostic problems. [11,17] Figure 3: Total laryngopharyngectomy with oesophagectomy specimen Figure 4: Post gastric pull-up barium swallow S47 CMYK47

5 Patel, et al. Figure 5a: Defect after total laryngopharyngectomy Figure 5b: Jejunal segment identiþ ed on appropriate arcade of vessels SKIN-LINED TUBES Both pedicled flaps like pectoralis major myocutaneous flaps and free cutaneous flaps like radial forearm or anterolateral thigh flaps have been widely reported to reconstruct circumferential defects of the pharynx, to provide a skin-lined tube. Figure 5c: Defect bridged by jejunal segment with a sentinel loop for monitoring Figure 5d: Post - operative barium swallow Pectoralis major myocutaneous flap The PMM flap is a versatile provider of skin for pharyngeal luminal reconstruction. The advantages include easy availability and harvesting and reliability with no added problems associated with microvascular transfers. Also, the muscle pedicle gives good cover to the neck vessels exposed in the dissection. The width of the flap needs to be cm to tabularize it and hence adequate mobilization of the tissues will be necessary to achieve a primary closure of the donor area. Satisfactory return of swallowing function with a low morbidity of stricture has been reported by Johnathan et al., in a large series of cases. [11] But its use in circumferential defects is less favoured because of the technical difficulties in tubularizing it when the flap is thick and in females, as well as the less predictable primary healing, stricture formation and poor speech rehabilitation. Free cutaneous flaps Both RFF and ALT flaps have been reported to be useful for pharyngeal tube reconstruction giving good functional results. [8,11,12] The ALT flap has been of much use for head and neck reconstruction because of the availability of large amounts of tissue from an expendable area. Several reports support the use of tabularized skin flaps with comparable or even superior results S48 48 CMYK

6 Laryngopharyngeal reconstruction in swallowing and speech rehabilitation over the free jejunal flap, considered to be the gold standard in reconstruction of the circumferential defects. [12] While using the free skin flaps one of the problems has been the difficulty to monitor these buried flaps. A small segment of the skin could be exteriorized for monitoring, but this has been reported to be increasing the incidence of fistula formation. [8] Use of a handheld Doppler has been suggested, but this also is known to give fallacious results due to the abundance of blood vessels in the neck. Hence it will be necessary to mark the site to be evaluated by the Doppler, at the time of surgery and also to evaluate the venous hum and to ascertain the patency of anastamosis. The ALT flap is more favoured than the radial forearm flap and has become the method of choice in many centres for circumferential hypopharyngeal reconstruction. SPEECH REHABILITATION AFTER LARYNGOPHARYNGECTOMY Removal of the larynx, the organ of speech production, is necessary when a total laryngopharyngectomy is carried out. Rehabilitation of the speech function after removal of the larynx has shown considerable progress in the last two decades. The methods available include: Artificial electro larynx This handheld device has a vibratory diaphragm which when applied to the neck skin produces sound which is then articulated to intelligible content by the patient. The major drawback is that the sound that is emitted has a bad mechanical quality which is disliked by many of the users [Figure 6]. Tracheoesophagial puncture Tracheoesophageal puncture (TEP) initially popularized by Singer and Blom [16] has been the most significant advance made in the rehabilitation of speech after laryngectomy. A puncture is made in the posterior tracheal wall into the oesophagus and a one-way valve is introduced to connect the oesophageal and tracheal lumen. The oneway valve allows egress of air from the trachea (when the external orifice is closed using the finger) into the oesophagus which is used by the patient to produce the speech. The valve prevents ingress of the oesophageal content into the tracheal lumen. The puncture can be made at the primary surgery itself or after a lapse of six months as a secondary procedure [Figure 7]. After laryngopharyngectomy whatever method is used for the luminal reconstruction, the speech rehabilitation is less satisfactory than when isolated laryngectomy is done. But successful TEP speech has been reported after either gastric pull-up, jejunal transfer or cutaneous flaps. [7,8,12] The quality of speech is usually inferior with stomach or the jejunum while compared to the normal TEP speech and the excess mucous secretion causes the speech to be more gurgling in nature. [12] In these instances the puncture if it goes through the jejunal or stomach wall will have increased chances of peri valve leaks and widening of the puncture site. Speech production with the skin-lined tubes has been found to be very satisfactory in many reports with more than 80% of patients achieving satisfactory phonation both with RFF and ALT flaps while it is 50-60% in cases of jejunal flaps. [12,18] Figure 6: Electrolarynx device Figure 7: Variety of speech valves S49 CMYK49

7 Patel, et al. Table 1: Functional outcome with various reconstructive techniques Stricture (%) Swallowing (%) TE speech (%) Normal Satisfactory Poor/PEG dependent Good Poor Tubed PMMF 0-12 [11,20] 59 [20] 32 [20] 9-19 [11,20] Radial forearm ß ap [21] 51 [4] Anterolateral thigh ß ap [11,12] 23 [12] 55 [12] 18 [12] [8,12] 11 [12] Jejunum 5-19 [4,12,21] [4,12] 19 [12] 26 [12] 63 [12] 38 [12] Table 2: Algorithm for laryngopharyngeal reconstruction COMPLICATIONS AND FUNCTIONAL OUTCOME WITH VARIOUS METHODS OF LARYNGOPHARYNGEAL RECONSTRUCTION The morbidity associated with these procedures depends upon the extent of the resection and the method of reconstruction. The immediate complications include fistulae leading to salivary leaks, hypocalcaemia and flap losses. Swallowing problems and stricture formation are the major delayed complications observed. The rate of fistula formation has been found to be ranging from 20-35% [11] and is more with circumferential defects. Depending on the method of reconstruction, there has been wide variation in the incidence of fistula with reports showing the incidence about 13-35% with tubed pectoralis major flaps, about 15-48% for gastric pull-up; 4-18% for jejunal flaps; 37-53% for radial forearm flaps and 7-9% for ALT flaps. [11,12,19-21] An interesting observation reported is the difference in timing of the fistula formation between the cutaneous and visceral flaps, with the cutaneous flaps showing a delayed fistula formation. This is attributed to the initial partial necrosis of the skin edges and the delayed dehiscence of the suture line. Stricture formation is the most common delayed complication and the reported incidence varies from 12% in PMM flaps, 15-22% in jejunal flaps, 29% in gastric pull-up to 5-40% with cutaneous free flaps. [9-11,15,18,22,23] The difficulty in swallowing may be apart from the strictures, due to reasons like dysmotility of the segment, redundancy of the flap in case of jejunum and the lack of propulsion from the tongue base. Overall successful swallow restoration has been reported to be varying from 60-93% with various reconstructive methods [Table 1]. CHOICE OF METHOD OF THE RECONSTRUCTION In general the choice of methods is dictated partly by the expertise available and partly by the type of defect. For a patch defect of the mucosal lining the authors choice is a pectoralis major flap. When the patch defect involves full-thickness loss including mucosa and skin a bipaddled radial forearm flap is the choice. With defects requiring the reconstruction of the circumferential defects the choice of the author is between gastric pull-up, jejunum, ALT flap and occasionally tubed pectoralis major flap. The decision for using a gastric pull-up is made intraoperatively when the extent of the tumour in its upper and lower aspects is done and the lower resected margin cannot be limited to the neck. If the lower extent is well within the neck or the upper extent is quite high up into the base tongue a jejunal segment is used. A tubed ALT may be a good alternative in these cases and is slowly gaining more acceptance since the morbidity is less and results are good. In cases where the reconstruction needs to be simpler, quicker and less expensive, due to various patient-related and resourcerelated issues, a tubed pectoralis major is still in use in the authors service. The algorithm depicted currently guides the choice of reconstruction in the authors service [Table2]. REFERENCES 1. Wookey H. Surgical treatment of the carcinoma of the pharynx S50 50 CMYK

8 Laryngopharyngeal reconstruction and upper esophagus. Surg Gynecol Obst 1942;75: Bakamjian VY. A two stage method for primary reconstruction of pharyngoesophagial reconstruction with a primary pectoral skin ß ap. Plast Reconstr Surg 1965;36: Ariyan S. The pectoralis major myocutaneous ß ap. A versatile ß ap for reconstruction of head and neck. Plast Reconstr Surg 1979;63: Disa JJ, Pusic AL, Hidalgo DA, Cordeiro PG. Microvascular reconstruction of the hypopharynx: Defect classiþcation, treatment algorithm and functional outcome based on 165 consecutive cases. Plast Reconstr Surg 2003;111:652-60, Gollingher JC, Robin IG. Use of left colon for reconstruction of pharynx and esophagus after pharyngectomy. Br J Surg 1954;42: Seidenberg B, Rosenak S, Hurwitt ES. Immediate reconstruction of the cervical esophagus by a revascularised isolated jejunal segment. Ann Surg 1959;142: Jurkiewicz MJ. Vascularized intestinal graft for reconstruction of the cervical esophagus and pharynx. Plast Reconstr Surg 1965;361: Peirong Yu Geoffrey L Robb. Pharyngoesophageal Reconstruction with the anterolateral thigh ßap: A clinical and functional outcomes study. Plast Reconstr Surg 2005;116: Baek CH, Kim BS, Son YI, Ha B. Pharyngoesophageal reconstruction with lateral thigh free ßap. Head Neck 2002;24: Scharpf J, Esclamado RM. Reconstruction with radial forearm ß aps after ablative surgery for hypopharyngeal cancer. Head Neck 2003;25: Clark JR, Gilbert R, Irish J, Brown D, Neligan P, Gullane PJ. Morbidity after ß ap reconstruction of hypopharyngeal defects. Laryngoscope 2006;116: Lewin JS, Barringer DA, May AH, Gillenwater AM, Arnold KA, Roberts DB, et al. Functional outcomes after circumferential pharyngoesophageal reconstruction. Laryngoscope 2005;115: Ong GB, Lee TC. Pharyngogastric anastamosis after esophagopharyngectomy for carcinoma of the hypopharynx and cervical Author Help: Sending a revised article esophagus. Br J Surg 1960;48: Rajan R, Rajan N, Pal US. Gastric pull-up by eversion stripping of esophagus. J Laryngol Otol 1993;107: Ho CM, Ng WF, Lam KH, Wei WJ, Yuen AP. Submucosal tumor extension in hypopharyngeal cancer. Arch Otolaryngol Head Neck Surg 1997;123: Singer MI, Blom ED, Hamaker RC. Voice Rehabilitation after total laryngectomy. J Otolaryngol 1983:12: Use of tubed gastro-omental free ßap for hypopharynx and cervical esophagus reconstruction after total laryngo-pharyngectomy. Eur Arch Otorhinolaryngol 2005;262: Schusterman MA, Shestak K, de Vries EJ, Swartz W, Jones N, Johnson J, et al. Reconstruction of the cervical esophagus: Free jejunal transfer versus gastric pull-up. Plast Reconstr Surg 1990;85: Ullah R, Bailie N, Kinsella J, Anikin V, Primrose WJ, Brooker DS. Pharyngo-laryngo-oesophagectomy and gastric pull-up for postcricoid and cervical oesophageal squamous cell carcinoma. J Laryngol Otol 2002;116: Spriano G, Pellini R, Roselli R. Pectoralis major myocutaneous ß ap for hypopharyngeal reconstruction. Plast Reconstr Surg 2002;110: Nakatsuka T, Harii K, Asato H, Ebihara S, Yoshizumi T, Saikawa M. Comparative evaluation in pharyngo-oesophageal reconstruction: Radial forearm ßap compared with jejunal ßap. A 10-year experience. Scand J Plast Reconstr Surg Hand Surg 1998;32: Reece GP, Schusterman MA, Miller MJ, Kroll SS, Robb GL, Baldwin BJ, et al. Morbidity and functional outcome of free jejunal transfer reconstruction for circumferential defects of the pharynx and cervical esophagus. Plast Reconstr Surg 1995;96: Anthony JP, Singer MI, Mathes SJ. Pharyngoesophageal reconstruction using the tubed free radial forearm ß ap. Clin Plast Surg 1994;21: Source of Support: Nil, Conflict of Interest: None declared. 1) Include the referees remarks and point to point clarification to those remarks at the beginning in the revised article file itself. In addition, mark the changes as underlined or coloured text in the article. Please include in a single file a. referees comments b. point to point clarifications on the comments c. revised article with text highlighting the changes done 2) Include the original comments of the reviewers/editor with point to point reply at the beginning of the article in the Article File. To ensure that the reviewer can assess the revised paper in timely fashion, please reply to the comments of the referees/editors in the following manner. There is no data on follow-up of these patients. Authors Reply: The follow up of patients have been included in the results section [Page 3, para 2] Authors should highlight the relation of complication to duration of diabetes. Authors Reply: The complications as seen in our study group has been included in the results section [Page 4, Table] S51 CMYK51