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  Vol. 127 No. 7, July 2001 TABLE OF CONTENTS
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Tubed Gastro-omental Free Flap for Pharyngoesophageal Reconstruction

Eric M. Genden, MD; Matthew R. Kaufman, MD; Brian Katz, MD; Anthony Vine, MD; Mark L. Urken, MD

Arch Otolaryngol Head Neck Surg. 2001;127:847-853.

ABSTRACT

Background  Malignant lesions of the pharyngoesophagus often require total laryngopharyngectomy and mediastinal dissection. As a result of the current treatment paradigms for advanced laryngopharyngeal cancers, it is common that the surgical field has been previously irradiated or exposed to systemic chemotherapy, resulting in fistula rates as high as 78% and mortality as high as 8%. The free vascularized tubed gastric antrum and the accompanying greater omentum offer a single-staged method of pharyngoesophageal reconstruction, with the added benefit of protection of the great vessels, the tracheal stump, and the mediastinal contents in a high-risk surgical field.

Objective  To assess the gastro-omental free flap as a method of pharyngoesophageal reconstruction in patients who have been previously treated with multimodality therapy.

Methods  Five consecutive cases of gastro-omental free flap reconstruction after total laryngopharyngectomy were retrospectively reviewed. Each case was assessed for intraoperative, perioperative, and postoperative complications at the primary site of reconstruction and the donor site. Patients were also evaluated for their ability to maintain an oral diet. Patients were followed up for a minimum of 6 months after surgery.

Results  Five patients aged 44 to 70 years (mean, 59 years) underwent gastro-omental free flap reconstruction after total laryngopharyngectomy. Five patients had received previous external beam irradiation, 2 had received systemic chemotherapy, and 4 had undergone previous surgery. There were no fistulae or flap complications. Three patients were successfully treated with esophageal dilation for strictures sustained 2 to 5 months after surgery, and a third patient was successfully treated with conservative management for a partial gastric outlet obstruction sustained 2 months after surgery. One patient died 3 months after surgery of distant metastatic disease. The remaining 4 patients currently tolerate an oral diet.

Conclusion  The tubed gastro-omental free flap offers a safe method of reconstructing the pharyngoesophageal segment in a surgical field compromised by previous multimodality therapy.



INTRODUCTION
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RECONSTRUCTION of circumferential pharyngoesophageal (PE) defects has historically represented one of the most challenging dilemmas for the head and neck reconstructive surgeon. For many years, the inability to primarily reestablish continuity of the cervical esophagus resulted in strategies involving staged procedures and the need for a chronic pharyngocutaneous fistula, often leading to infection and a poor functional outcome. Czerny,1 Mikulicz,2 and Trotter3 attempted early on to remedy this problem by using cervical skin flaps in staged reconstruction. This approach, however, was unreliable and was commonly associated with a high rate of morbidity as a result of flap necrosis, wound breakdown, and mediastinal infection. Nearly half a century later, Wookey4 reintroduced this technique, redesigning the cervical flaps with a more broad-based pedicle, which resulted in more reliable 2-staged reconstruction. Although this was an improvement, more than 90% of patients reconstructed in this manner sustained some form of postoperative complication related to the reconstruction.5 Salivary contamination of the mediastinum commonly led to disseminated infection and, occasionally, fatal vascular erosion. The limitations associated with random pattern skin flaps led to the application of the deltopectoral flap and, soon thereafter, the pectoralis major myocutaneous flap.

The deltopectoral flap offered reconstructive surgeons a source of reliable, well-vascularized tissue from a regional site, which was particularly useful in irradiated patients. This technique was an improvement over previous reconstructive efforts; however, the disadvantages of a staged procedure and the need to create a pharyngostome resulted in an unacceptably high complication rate and a prolonged course before instituting oral nutrition.5 The drive to primarily reconstruct the pharyngoesophagus influenced Withers et al6 and Baek et al7 to report on the use of a tubed pectoralis major flap as a method of "immediate" reconstruction of circumferential defects of the pharynx and cervical esophagus. However, the bulky nature of the pectoralis flap prevented the comfortable creation of a circumferential skin tube. As a result, most tube-shaped pectoralis major PE reconstructions required formation of a controlled fistula, either at the time of the primary reconstruction or as a result of a postoperative wound dehiscence.

In an effort to address the problems associated with delayed reconstruction, and the requirement for thin, pliable tissue, a variety of pedicled visceral flaps were introduced.8-10 The theoretical advantages of the gastric pull-up include a single anastomosis with less potential for anastomotic failure; a source of thin, pliable, nonirradiated tissue; and the opportunity for single-staged reconstruction. However, these advantages did not translate into an extremely safe and reliable method of reconstruction. Surkin et al5 found that mortality occurred at a rate of 15%, and 50% of patients sustained major abdominal, medical, or thoracic complications; however, the gastric pull-up procedure remains a vital part of the reconstructive surgeon's armamentarium for management of esophageal defects that extend to the thoracic esophagus.

Although microvascular free tissue transfer has been widely applied in contemporary head and neck reconstruction, its impact on primary reconstruction of the pharyngoesophagus has been profound. The drive to circumvent staged reconstructions and the morbidity associated with postoperative wound dehiscence has led to widespread application of free tissue transfer for PE reconstruction. A host of donor sites have been described for the reconstitution of circumferential defects, including the free colon segment,11 the tubed cutaneous free flap,12 and the tubed gastro-omental free flap.13 Colonic segments have been used as free flaps based on the ileocolic, middle colic, and sigmoid arteries. Although this donor site is no longer the primary choice for reconstruction of the pharyngoesophagus, the mucosa-lined colon offers an inner lining similar to the native pharynx.

Application of the free jejunal segment serves as a particularly interesting landmark in head and neck reconstructive surgery. In 1959, Seidenberg et al14 reported the first case of immediate PE reconstruction using a revascularized free jejunal segment. Although the patient survived for only 5 days after surgery as a result of a cerebrovascular accident, the accomplishment of Seidenberg et al marked the beginning of the current era in microvascular reconstruction. The free jejunal segment provided an alternative to the gastric pull-up; however, early in its application, ischemia and pharyngocutaneous fistulae were not uncommon. Hypothermia, pharmacotherapy, and a variety of harvesting techniques were reported in an effort to prevent distal necrosis of the jejunal segment; however, the results have been variable.15-17 As alluded to earlier, flap necrosis, and the resulting pharyngocutaneous fistulae, is a particular problem in PE segment reconstruction because of the risk associated with the adjacent great vessels and the potential access of secretions to the mediastinum. Shangold et al18 reported a meta-analysis of 633 cases of free jejunal transfer in which salivary fistulae occurred in 18% of cases. Two thirds of the fistulae healed with conservative management; however, the perioperative mortality in this review was 4.4%. Although the jejunal segment offers an excellent source of vascularized tissue for PE segment reconstruction, the risk of salivary fistulae and the attendant morbidity remains a significant concern, particularly in the patient who has been previously exposed to radiation and chemotherapy.

Harii et al19 were the first to report their success using the tube-shaped cutaneous radial forearm flap for PE reconstruction, which offered an attractive alternative to the necessity for a laparotomy and the attendant morbidity to harvest a visceral flap. Several different cutaneous flaps have since been applied in a similar manner, including the lateral thigh20 and ulnar forearm flaps.21 Tube-shaped cutaneous free flaps offer a source of thin and pliable tissue. In many ways this is ideal for the primary reconstruction of PE defects limited to the neck. Although uncommon in patients with hypopharyngeal cancer, obesity might play a role in the decision-making process. On rare occasions, cutaneous free flaps might be too thick to create a tube, and, therefore, visceral flaps represent the most suitable reconstructive alternative.

Although complication rates associated with PE reconstruction have significantly improved since implementation of free tissue transfer, postoperative salivary fistulae remain common, particularly in patients who have received preoperative radiation, chemotherapy, or both.22 The adverse effects of radiation and chemotherapy on wound healing have been well documented and often complicate salvage surgery and reconstruction.23 Patients who present with extensive disease of the hypopharynx often require bilateral neck dissections and a mediastinal dissection. Salivary contamination of the mediastinum, as a result of an anastomotic dehiscence, particularly in a patient who previously received radiation or chemotherapy, commonly leads to prolonged hospitalization and the potential for a fatal complication. Consequently, dermal grafts, muscle flaps, and staged reconstructions, have been used to prevent such complications; however, most surgeons have achieved only marginal success using these techniques.

The gastro-omental free flap is a composite flap consisting of a segment of tubed gastric antrum in continuity with the greater omentum. First described by Baudet24 in 1979, the gastro-omental free flap was originally reported as a method for secondary closure of a pharyngostome. Subsequently, it has been applied to PE reconstruction.25 The gastro-omental free flap offers several advantages over jejunal or fasciocutaneous free flap methods of reconstruction. In particular, the richly vascularized omentum, which has been considered the "policeman of the abdomen" for its unique ability to protect against the spread of intra-abdominal infection, can be used to cover and protect the mediastinum and great vessels from salivary contamination in the event of a salivary or tracheal fistula. We present a retrospective review of 5 consecutive cases of tubed gastro-omental free flap reconstruction after total laryngopharyngectomy in patients with previous external beam irradiation, chemotherapy, or both.


PATIENTS AND METHODS
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A retrospective review was performed of 5 consecutive patients undergoing tubed gastro-omental free flap reconstruction of 5 total laryngopharyngectomy defects between May 1997, and November 1999. Patients were evaluated for intraoperative, perioperative, and postoperative recipient site and donor site complications and postoperative diet.

Five patients (3 men and 2 women) aged 44 to 70 years (mean, 59 years) underwent PE reconstruction with a tubed gastro-omental free flap after total laryngopharyngectomy (Table 1). All of the patients had locally advanced cancer of the pharyngoesophagus. Four patients had bilateral neck dissections. Two patients had mediastinal dissections performed in conjunction with manubrial and bilateral clavicular head resection. Diagnoses included squamous cell carcinoma of the larynx (n = 3), fibrosarcoma invading the trachea and larynx (n = 1), and liposarcoma involving the visceral compartment (n = 1). All 5 patients were treated with preoperative external beam radiation, and 2 patients received preoperative concomitant systemic chemotherapy (Table 1). Four patients had undergone previous surgery at the primary site.


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Pharyngoesophageal Reconstruction With a Gastro-omental Free Flap*


In all cases, the gastro-omental free flaps were harvested using a 2-team approach. The general surgery team performed a laparotomy incision and isolation of the gastric antrum and its accompanying omentum. The dominant vascular supply to the greater curvature of the stomach is the right and left gastroepiploic artery and vein. The right gastroepiploic artery is derived from the gastroduodenal artery, and the left gastroepiploic artery is derived from the splenic artery. Although both arteries give rise to a series of corporeal branches that supply the stomach and omentum, the right gastroepiploic artery is usually dominant and, therefore, used for the microvascular anastomosis. Once the appropriate segment of gastric antrum was isolated, a stapling device was used to harvest the free flap. It is imperative not to harvest gastric mucosa in the area of the pylorus to avoid gastric outlet obstruction. A longer pedicle might be obtained by more proximal dissection and by harvesting the mucosal flap at a greater distance from the pylorus. Once the mucosal flap is harvested, the laparotomy incision is closed by the general surgery team while the gastroepiploic vessels are isolated and prepared on a separate table.


RESULTS
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All 5 patients had unremarkable intraoperative courses. A 2-team approach was used in all cases to perform the surgical extirpation while simultaneously harvesting the tubed gastro-omental free flap. There were no perioperative complications, including wound infection, pharyngocutaneous fistulae, flap necrosis, or microvascular anastomosis complications. In all cases, a segment of the omentum was exteriorized for monitoring and was eventually excised. After surgery, 3 patients required esophageal dilation for strictures that developed 2 to 5 months after surgery at the distal anastomosis. One patient was treated conservatively for a partial gastric outlet obstruction that manifest 2 months after surgery. Currently, 4 patients tolerate an unrestricted oral diet, and 1 patient has died of distant metastatic disease. The following case presentation illustrates the value of the greater omentum as a protective barrier for vital structures in the neck and mediastinum.

A 70-year-old man with a history of a T3 N0 M0 squamous cell carcinoma of the supraglottic larynx was initially diagnosed and treated with primary external beam radiation. After radiation therapy, persistent disease necessitated total laryngectomy. Eleven months after surgery, the patient presented to The Mount Sinai Medical Center, New York, NY, with a stomal recurrence and was treated with cervical pharyngoesophagectomy, stomal resection including 4 cm of the trachea, bilateral clavicular head and partial sternal resection, and resection of peristomal skin (Figure 1). Mediastinal dissection was also performed in conjunction with left radical and right modified neck dissection (Figure 2). After the distal margins were determined to be free of disease on frozen section, a gastro-omental composite free flap was harvested through a midline laparotomy incision.



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Figure 1. Specimen after resection of stomal recurrence in conjunction with mediastinal dissection, bilateral clavicular head resection, and partial sternal resection.




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Figure 2. Postablative surgical field demonstrating exposure of the carotid arteries and mediastinum.


The pharyngoesophagus was reconstructed using tubed gastro-omental mucosa harvested with a tissue stapling device. The omentum was draped over the great vessels, around the tracheal stump and the enteric anastomoses (Figure 3). The peristomal cutaneous defect and the distal tracheal remnant were reconstructed using a fenestrated pectoralis myocutaneous flap. After surgery, the distal aspect of the pectoralis flap sustained necrosis that required intraoperative debridement (Figure 4). The underlying great vessels and the tracheal remnant were protected by the greater omentum, which had contracted around the underlying structures, keeping them from exposure. During the following several weeks, wet to dry dressings were applied to the exposed omentum as it contracted around the tracheal stoma (Figure 5). On postoperative day 14, the patient was discharged from the hospital with an oral diet (Figure 6).



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Figure 3. The greater omentum is draped over the carotid arteries and around the tracheal stump. The greater curvature of the stomach is used to reconstruct the pharyngoesophagus.




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Figure 4. Necrosis of the distal aspect of the fenestrated pectoralis myocutaneous flap. After debridement of the distal portion of the pectoralis flap, the underlying greater omentum prevented great vessel exposure and stomal breakdown.




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Figure 5. Contraction of the peristomal tissues and the greater omentum 4 weeks after surgery.




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Figure 6. Barium swallow on postoperative day 14 depicting a patent pharyngoesophageal segment.



COMMENT
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Carcinoma of the hypopharynx is characteristically aggressive and often extensive at the time of diagnosis.26 Hypopharyngeal carcinoma notoriously spreads submucosally to adjacent structures commonly involving the medial wall of the piriform sinus, the aryepiglottic fold, or the glottic larynx at the time of diagnosis.26-27 The rich lymphatic and vascular supply within this region of the aerodigestive tract accounts for the high rates of local spread early in the disease process. At the time of diagnosis, 60% to 75% of patients have detectable metastatic disease in the middle and lower jugular chains and occult metastases in the paratracheal and retropharyngeal lymph nodes.28-29

Surgical treatment of hypopharyngeal carcinoma has evolved considerably during the past 40 years. In the early 1960s, surgery was the primary modality of therapy. With the introduction of regional flaps and the colonic interposition, surgical therapy was more widely applied in the late 1960s and 1970s, using radiation therapy as an adjuvant modality. Poor long-term results led Biller et al,30 Ogura and Mallen31 and Ogura et al32 to consider preoperative irradiation at 2000 to 4500 rad (20-45 Gy) followed by surgical therapy. This treatment strategy became the standard of care in the early 1970s. However, by the mid-1970s, unacceptably high morbidity and mortality rates as a result of wound breakdown, mediastinitis, and a negligible improvement in disease control prompted several prospective studies33-34 evaluating the role of surgery and preoperative irradiation. The failure to achieve a therapeutic advantage with these treatment strategies, coupled with the introduction of microvascular free tissue transfer for head and neck reconstruction, led to the introduction of wide-field resection and primary reconstruction, followed by postoperative radiation therapy.34 Early studies35-36 demonstrated that the combination of surgery followed by postoperative irradiation did not improve the 5-year survival rate; however, it did affect the pattern of recurrence, increasing the rate of distant metastatic disease. Consequently, preoperative chemotherapy has been more commonly instituted in an effort to reduce the rate of distant metastatic disease.

Currently, organ preservation protocols are commonly applied to the treatment of hypopharyngeal carcinoma and extensive stomal recurrence. As a result, patients commonly are primarily treated with chemotherapy and radiation, with surgical therapy reserved for salvage. Although a definitive improvement in disease-free survival has not yet been established, it is clear that this form of nonsurgical therapy results in a compromise in wound healing.23 Despite the advantage of transferring vascularized tissue into a compromised recipient bed, fistula rates, wound breakdown, and peristomal dehiscence after microvascular reconstruction of the pharyngoesophagus remain unacceptably high.37 Similarly, surgery for stomal recurrence represents a difficult reconstructive dilemma, particularly in a patient who has been previously exposed to radiation, chemotherapy, or both. Wound breakdown in this area after ablative surgery can lead to disastrous consequences.

For more than half a century, surgeons have used the gastric mucosa for PE reconstruction as either a reversed gastric tube or a gastric pull-up. In 1961, Hiebert and Cummings38 were the first to successfully transfer a segment of gastric antrum for primary cervical esophageal reconstruction. Although this method of reconstruction did not include the gastric omentum, in 1979 Baudet24 recognized the utility of the omentum and transferred a composite gastro-omental flap for the secondary closure of a pharyngostome. The greater omentum has intrigued physicians for centuries. Referred to as the "abdominal policeman" because of its superb defense against abdominal infection and its unique absorptive capabilities, omental flaps were initially used for repairing intraperitoneal defects and chest wall defects, reconstructing pelvic fistulae, and reinforcing the aortic graft.39 The rich vascularity and pliability of the omentum allows for contouring and minimal scar formation. Microvascular transfer of the greater omentum was first achieved in a clinical setting by McLean and Buncke40 for reconstruction of a scalp defect after tumor resection. Baudet's application of the combined gastro-omental patch graft for PE reconstruction shortly thereafter provided a composite flap consisting of mucosa for esophageal lining and a vascularized omental graft that could be used to protect the surrounding great vessels and the tracheal stump from the potential risk of salivary contamination. Since Baudet's original description of the gastro-omental free flap, which was used as a patch graft, there have been few studies41-42 related to use of this donor site for PE reconstruction.

In our series of 5 patients with PE defects who underwent reconstruction with a tubed gastro-omental free flap, all 5 had failed previous multimodality therapy. To guard against the associated risk of fistula formation and great vessel exposure, the omentum was used as a protective wrap, draped over the great vessels and around the tracheal stump. The vascular nature of the omentum provided an adequate bed for placement of a split-thickness skin graft, providing a protective barrier around the enteric anastomosis and vital structures in the neck and mediastinum should a salivary fistula occur. Panje et al43 previously demonstrated that the omentum serves as an excellent source of carotid coverage and that the omentum will often atrophy by as much 50% of its original volume. We found that the omentum served an important role in the reconstruction and the final clinical outcome. Protection of the great vessels, the tracheal stump, and the mediastinum is particularly important in a patient who has previously been exposed to multimodality therapy. The greater omentum provides a protective barrier for the development of a salivary fistula from the PE segment by wrapping the pharyngogastric and gastroesophageal anastomoses. In addition, it can also provide a significant protective barrier around the trachea from the seeding of the neck and mediastinum with tracheal secretions, especially in the case of a short tracheal stump. The thinness, maneuverability, and vascularity of the greater omentum are the key features that distinguish this tissue and provide for a greater protective capability than any other tissue currently available. Although muscle is often useful for this purpose, it lacks the pliability characteristic of the greater omentum. It is clearly the key element of this composite flap, which we believe distinguishes it from other visceral flaps such as the free jejunum or tubed cutaneous flaps and justifies performance of a laparotomy with its attendant morbidity.

In our series, there were no complications with regard to graft failure, fistula formation, great vessel exposure, or stomal dehiscence despite the compromised wound bed. Before surgery, 1 patient sustained a gastric outlet obstruction as a result of harvesting a segment of stomach that was too close to the pylorus in the harvest segment. Three patients sustained mild esophageal stenoses at the junction of the inferior anastomosis; however, all 3 patients responded to serial dilation, and 4 patients currently tolerate an unrestricted oral diet. We have since modified the distal anastomosis by opening a larger component of the distal anastomotic border and "fish mouthing" the proximal thoracic esophagus to increase the surface area of the esophagogastric repair.

The gastro-omental free flap can be harvested using a 2-team approach without difficulty. Although the volume of omentum associated with the gastric harvest varies in individuals,44 the rich vascular network allows for trimming and tailoring of the omentum with minimal risk of vascular compromise. The greater curvature of the stomach can be harvested according to the length and width of tissue needed to achieve the PE reconstruction. However, it is imperative not to narrow or alter the anatomical features of the pylorus in the harvest because gastric outlet obstruction might occur. We prefer to harvest the antrum using a stapling device, which provides a mechanism to simultaneously prepare the gastric segment for transfer and achieve closure of the remaining portion of the stomach. This harvest technique reduces the surgical risk of intra-abdominal sepsis. It is imperative that the harvest of the stomach not commence before the distal frozen section is obtained. Oncologic clearance of the cancer in the neck is critical to document before harvest of the greater curvature because gastric pull-up is eliminated as a reconstructive option. Should replacement of the thoracic esophagus be required after a free gastro-omental flap, use of the colon interposition would be required.

There are several contraindications to using this donor site, including previous gastric surgery and active peptic ulcer disease. Although only 1 patient in our series sustained a donor site complication, intra-abdominal complications, such as peritonitis, gastric leak, intra-abdominal abscess, and gastric outlet obstruction, are potential complications. In addition, performance of a laparotomy results in more difficult recovery, with respiratory complications more prevalent in the early postoperative period.

In conclusion, the tubed gastro-omental free flap offers a safe method of reconstructing the pharyngoesophagus in a surgical field compromised by previous chemotherapy, radiation, and previous surgery. The unique properties of the omentum protect the great vessels, the tracheal stump, and the mediastinum, transforming a surgical procedure with high morbidity and mortality rates into a relatively safe procedure. Because of the inherent properties of the greater omentum, this composite flap is our reconstructive method of choice, especially when the dissection and impaired wound healing predispose to mediastinal sepsis and disruption of the tracheocutaneous anastomosis in the creation of a permanent laryngostome.


AUTHOR INFORMATION
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Accepted for publication March 15, 2001.

Presented at the annual meeting of the American Head and Neck Society, Fifth International Conference on Head and Neck Cancer, San Francisco, Calif, July 30, 2000.

Corresponding author: Eric M. Genden, MD, Department of Otolaryngology–Head and Neck Surgery, Box 1189, The Mount Sinai School of Medicine, One Gustave L. Levy Place, New York, NY 10029.

From the Departments of Otolaryngology–Head and Neck Surgery (Drs Genden, Kaufman, and Urken) and Surgery (Drs Katz and Vine), Mount Sinai School of Medicine, New York, NY.


REFERENCES
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26. Harrison DF. Pathology of hypopharyngeal cancer in relation to surgical management. J Laryngol Otol. 1970;84:349-367. PUBMED
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28. Biller HF, Davis WH, Ogura JH. Delayed contralateral cervical metastases with laryngeal and laryngopharyngeal cancers. Laryngoscope. 1971;81:1499-1502. FULL TEXT | WEB OF SCIENCE | PUBMED
29. Ogura JH, Biller HF, Wette R. Elective neck dissection for pharyngeal and laryngeal cancers: an evaluation. Ann Otol Rhinol Laryngol. 1971;80:646-650. WEB OF SCIENCE | PUBMED
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31. Ogura JH, Mallen RW. Partial laryngopharyngectomy for supraglottic and pharyngeal carcinoma. Trans Am Acad Ophthalmol Otolaryngol. 1965;69:832-845. PUBMED
32. Ogura JH, Marks JE, Freeman RB. Results of conservation surgery for cancers of the supraglottis and pyriform sinus. Laryngoscope. 1980;90:591-600. WEB OF SCIENCE | PUBMED
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