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Ann Thorac Surg 1999;67:911-916
© 1999 The Society of Thoracic Surgeons

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Original Articles

Microvascular prefabricated free skin flaps for esophageal reconstruction in difficult patients

^a Department of Surgery, Chang Gung Memorial Hospital, Taipei, Taiwan
^b Department of Surgery, National Taiwan University Hospital, Taipei, Taiwan

Accepted for publication October 8, 1998.

Address reprint requests to Dr Tang, 6F-1, 28, Hang-chow N Rd, Taipei, Taiwan

	Abstract

Top Abstract Introduction Patients and methods Results Comment References

 
Background. Reconstruction of the esophagus for complicated benign stricture or after resection of malignant lesion is still a challenge for surgeons. When abdominal viscera cannot be used, skin flaps are selected for esophageal reconstruction. However, skin flaps for esophageal reconstruction are notorious for leakage, and have not been widely accepted. Prefabrication before microvascular transfer to its final site can improve the result of esophageal reconstruction when skin flaps are used.

Methods. Eight patients with complicated corrosive esophagitis had been treated with prefabricated skin flaps for esophageal reconstruction. The procedures are described in detail.

Results. All patients healed well without leakage. The barium study showed smooth passage. There was no dysphasia or regurgitation after education. Pulmonary complication happened in only 1 patient. Revision for the distal anastomosis was required in 1 patient due to narrowing. When the skin tube is long, the patients need water (or soup) to facilitate swallowing and occasionally use their hand to help the food passage. This method has the following advantages: (1) healing of the long suture line before transfer to withstand the intestinal juice; (2) reliable viability in the distal part of the flap, especially when an extended length of the flap is required; (3) more length of stable tissue for two-layered, tension-free anastomosis at the junction of skin and gastrointestinal mucosa to prevent leakage; and (4) the flap can be placed in the substernal position to meet the aesthetic requirement of young patients. The disadvantage was the staged operations. However, after prefabrication the transfer becomes safe and free of leakage. The overall morbidity is minimal.

Conclusions. In rare situations when skin flaps are used for esophageal reconstruction, prefabrication provides advantages over conventional one-stage methods, although it needs additional procedures. This method is a combination of conventional technique and microsurgery.

	Introduction

Top Abstract Introduction Patients and methods Results Comment References

 
Leakage is a serious complication in esophageal reconstruction, which may result in morbidity or even mortality of the patients. The leakage may be caused by many factors: (1) inadequate blood supply of the tissue used for esophageal reconstruction at the anastomotic site; (2) pressure from coughing or the accumulated saliva and gastrointestinal secretions; (3) tension at the anastomotic site; (4) difficulty in healing with different tissue across the anastomotic site (eg, high leak rate at the anastomosis between mucosa and skin flap); and (5) infection.

Using skin flaps for esophageal reconstruction has the following disadvantages: (1) it is vulnerable to leakage due to difficult healing between the skin and the mucosa; (2) it may not be long enough if the esophageal defect is long; and (3) the skin tube does not provide motility; its functional result is not as good as the gastrointestinal tract in esophageal replacement.

Prefabrication before microvascular free tissue transfer has been applied in the following ways [1]: (1) pretransfer delay; (2) pretransfer expansion; (3) addition of other components (cartilage, skin grafts, etc.); and (4) vascular pedicle implantation. Leakage is a major concern when skin flaps are used for esophageal reconstruction. We present a new application of the prefabrication principles to this field. It prevents leakage when skin flaps are used to replace a part or the entire length of the esophagus.

The basic anatomy of tensor fascia lata flap [2, 3] and radial forearm flap [4] has been well documented.

The tensor fascia lata musculocutaneous flap is supplied by the transverse branch of the lateral circumflex femoral artery. The pedicle is 5 cm in length, with an external diameter of 1.5 to 2 mm. The vascular anatomy is constant. It is found between rectus femoris and vastus lateralis muscles. The overlying skin is supplied by multiple musculocutaneous perforators. The territory of the flap is located at upper two-thirds of the thigh.

The vessel enters the tensor fascia lata muscle at 6 cm distal to the anterosuperior iliac spine on an axis from the anterosuperior iliac spine to the lateral condyle of the tibia. The sensory nerves innervating this territory are the lateral cutaneous branch of T-12 nerve and the lateral cutaneous nerve of the thigh (L2–C3) (Fig 1A ).

View larger version (15K): [in this window] [in a new window]   Fig 1. (A) The diagram shows the vascular pedicle, and regular dimensions of the tensor fascia lata flap. (A = anterior superior iliac spine; B = lateral condyle of tibia; 1 = ascending branch of the lateral femoral circumflex artery; 2 = transverse branch; 3 = descending branch.) (B) The diagram shows the vascular pedicle and dimensions of the radial forearm flap. (BA = brachial artery; RA = radial artery.)

View larger version (100K): [in this window] [in a new window]   Fig 2. (A) Prefabrication for the tensor fascia lata flap. A flap (40 by 10 cm) is required to obtain reliable viability of the extended length. It also ensures healing of the long suture line before transfer. The flap was partially raised. The skin was inverted to become the inner lining of the esophagus. After healing of the long suture line, this flap would not be affected by saliva and intestinal juices. Note the long suture line. (AB = the length of the tensor fascia lata flap; BC = the extended length of the flap when a delay procedure is performed.) The pedicle artery was the transverse branch of the lateral femoral circumflex artery. (B) Method of tubing the flap to ensure healing of the suture line. Two-layered sutures were performed. (AB = the shaded area is the zone that was still attached to the thigh; 1 = the first layer of skin suture; 2 = the second layer suture through the fascia.) Two weeks later the flap was raised completely and transferred to reconstruct the esophagus. The recipient artery was the right thoracoacromial artery and the recipient vein was its concomitant vein. The upper end of the prefabricated skin tube was joined to the cervical esophagus. The lower end of the skin tube was anastomosed with jejunum. (C) Esophagogram showing the smooth passage of the contrast medium at 2 years of follow-up.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment References

The first stage is partial elevation of the flap. The flap is designed around the central axis of tensor fascia lata. The flap dissection is started at the inferior margin. The fascia lata muscle and iliofibial tract are incised. A strip of the middle third of the flap is left attached to the donor site. With the pretransfer delay procedure the length of the flap can be longer than the proximal two-thirds of the thigh if distal extension is required for a long defect of the esophagus. The skin flap is rolled up with the skin facing the lumen and suturing it to form a tube with two-layered sutures. The pedicle of the flap is not dissected in the first stage operation.

The second stage is done two weeks later when there is good healing of the long suture line. At that time the pedicle (transverse branch of lateral femoral circumflex artery and vein) is dissected and the flap is then completely raised as a free flap. The skin flap is elevated with the fascia from distally to proximally. Finally, the muscle is divided to isolate the flap on its pedicle. It is transferred to the recipient site with microsurgical technique. The recipient artery is the thoracoacromial artery, the traverse cervical artery, or the superior thyroid artery. The recipient vein is the concomitant vein or a branch of external jugular vein. There is sufficient tissue available beyond the two ends of the skin tube for two-layered sutures to the pharynx and intestine. Drain tubes are inserted both inside and outside the esophageal lumen to ensure wound healing.

Prefabricated radial forearm flap for reconstruction of cervical esophagus
The first stage is the partial flap elevation. The forearm flap for cervical esophagus reconstruction does not need to have an extended length, but the surgeon has to wait until healing of the suture line before the transfer. During flap dissection the ulnar border of the flap is incised first, and the deep fascia is included in the flap. The distal veins are ligated. The flap is raised toward the radial side. The paratenon of the flexor tendons should be preserved to facilitate skin grafting later on. A zone of this flap can be attached to the donor site for easy wound care. The flap is rolled up to form a tube. If proximal extension of the forearm flap is necessary, it can be raised partially in the way as that of the tensor fascia lata flap. The suture line of the skin tube is allowed to heal before transfer.

The second stage is the transfer of the flap to the neck. This is performed with microvascular technique for reconstruction of cervical esophagus. When the suture line has healed at 2 weeks, it can be transferred to the neck. The flap is raised completely for transfer. Passing over flexor capri radialis, the lateral intermuscular septum is found and the radial artery is exposed. The flap can now be elevated in a distal to proximal direction. The skin flap can be transferred when the recipient site is ready. As for closure of the donor site, the defect of the radial artery can be repaired with a vein graft if necessary. The donor site can be grafted with split or full-thickness skin graft.

	Results

Top Abstract Introduction Patients and methods Results Comment References

 
In all patients the wound healed well without leakage. The mean follow-up time was 27 months. Only 1 patient had partial loss of the skin graft at the donor site, which healed after the second skin graft. Two patients had subcutaneous hematoma, which required incision and drainage. None of them developed leakage. One patient complained of the bulkiness of the reconstructed esophagus, and another patient complained of the donor site appearance.

Functional evaluations, such as transit time, consistency of diet, regurgitation, and pulmonary infection, are listed in Table 2. The barium study showed smooth passage. There was no dysphagia, except in 1 patient who received revision of distal anastomosis due to narrowing one year later. Only V to Y advancement was required for relief of the narrowing and this patient could eat smoothly again. Transit time was performed in 6 patients. It was slightly longer than normal due to lack of peristalsis. The functional result is not as good as using the gastrointestinal tract for esophageal replacement. The patients were educated to assume head-up position while sleeping so that there was no problems of regurgitation. One patient was diagnosed with aspiration pneumonia, which subsided after conservative treatment including antibiotics. When the skin tube is long, the patient needs water or soup for lubrication while taking a solid diet. Occasionally the patients use their hand to help in the food passage (Table 2).

In the first stage reconstruction, a prefabricated tensor fascia lata flap (40 by 10 cm) was partially raised to form a long skin tube at the left thigh. A longitudinal strip of the flap was left attached to the thigh. It was partially raised so that the distal part of the flap was able to survive and to develop more neovascularization as a delay phenomenon. This was designed to ensure complete survival of the whole flap on subsequent elevation, and to ensure healing of the suture line before transfer. It was prepared for safe transfer to replace the removed colon segment. Porcine skin was applied to the raw surface of the left thigh for temporary coverage.

Two weeks later, the prefabicated tensor fascia lata skin tube was completely raised. The pedicle was dissected and the flap was transferred with microsurgery to reconstruct the esophagus in a subcutaneous tunnel. The recipient artery was the right thoracoacromial artery. The recipient vein was its concomitant vein. The total ischemic time was 50 minutes. The upper end of the prefabricated skin tube was joined to the cervical esophagus. The lower end of the skin tube was anastomosed with the jejunum. Two No. 16 nasogastric tubes were used for drainage and splinting. The donor site was closed as far as possible, and the residual skin defect of the left thigh was covered with split skin graft. To be careful, the patient had total parenteral nutrition for 1 month after operation, and then gradually advanced to a regular diet by mouth. At 2 years of follow-up she reported regular eating with remarkable increase of body weight from 37 kg to 50 kg. Esophagogram showed smooth passage of the contrast medium without stricture. The transit time with 20 mL of liquid barium suspension was 18 seconds. She married again and returned to normal life after esophageal reconstruction.

Patient 2
Prefabricated radial forearm flap for reconstruction of the cervical esophagus
In a suicide attempt a 32-year-old woman hesitated swallowing a corrosive agent and eventually spit it out. However, this had resulted in injury to the pharynx and cervical esophagus around the cricoid level. Repeated bouginage failed to bring about improvement. Therefore, she underwent reconstruction 1 year after injury. She had a history of adhesion ileus from a previous operation for perforated peptic ulcer. The intestinal obstruction was relieved after conservative treatment. After discussion with the patient, she preferred not to open the abdomen again. Therefore, a forearm flap instead of jejunum was used for reconstruction of the pharynx and cervical esophagus. To avoid leakage a prefabricated forearm flap was designed. In the first stage it was raised partially from the left forearm but the pedicle was left intact; therefore, the suture line could heal before the transfer. Two weeks later it was transferred with microsurgery to reconstruct the cervical esophagus. The recipient artery was the transverse cervical artery, and the recipient vein was a branch of external jugular vein. The ischemic time of the free flap was 2 hours, and the wound healed well. There was no leakage and the patient was able to assume a liquid diet at 4 weeks, which was gradually advanced to solid food. At 4 years of follow-up, the patient was eating normally and the esophagogram showed patency of the esophagus with smooth passage of the contrast medium. The transit time with 20 mL of liquid barium suspension was 14 seconds.

	Comment

Top Abstract Introduction Patients and methods Results Comment References

 
Reconstruction of the esophagus after injury can be difficult. There are two major procedures currently being used for reconstruction. One uses the alimentary tract such as a colon segment interposition or free jejunum transfer; the other is the inverted skin tube composed of either a skin flap or a myocutaneous flap [5–8]. If all gastrointestinal tract conduits have been exhausted, the skin flap is a last resort. However, skin flaps are prone to develop leakage due to slow healing of mucosa, and the long suture line of the skin tube is easy to break on exposure to gastrointestinal secretions. When multiple procedures including jejunum and colon interposition fail eventually, the prefabricated skin flap for esophageal reconstruction is a good solution for these difficult patients. The selection of a particular skin flap depends on the length of the esophageal defect.

Orticochea [9] was the first to use the method of flap prefabrication. Taylor and Palmer [10] described the vascular territories (angiosomes) of the body to identify a block of tissue including skin that is normally supplied by a single vessel or a system of vessels from a single muscle. Adjacent angiosomes do not overlap under normal physiologic conditions, but they do so on demand when the vessels supplying the adjacent vascular territories become disrupted or occluded. The delay phenomenon is initiated when several adjacent perforating vessels are disrupted, such as flap elevation that triggers perfusion into the devascularized area. The delay procedure stimulates an anatomic dilatation and reorientation of vessels. This can be applied clinically even after the advent of microsurgery, despite the need for additional procedures. There are instances in which prefabricated flaps provide advantages. Khouri and colleagues [1] reviewed the available clinical methods of flap prefabrication and their respective indications as well as advantages. Our method is a combination of conventional technique and microsurgery.

Previous prefabricated flaps can be classified depending on the underlying principles used in the prefabrication process: (1) pretransfer delay, (2) pretransfer expansion, (3) pretransfer grafting or addition of other components [11–13], and (4) the vascular induced flap through staged transfer. Now we present another category, which is secured healing of cutaneous suture line with stable vascularity of the flap before skin flap transfer for esophageal reconstruction. The prefabrication of the flap allows us to build exactly what is required for reconstruction, and in this way a great deal of refinement can be achieved. Our prefabrication method uses microsurgical reconstruction of esophagus. The leak rates of one-stage free forearm flap used to replace the cervical esophagus without prior tubing was 30% in our series, which is similar to the study by Harii and colleagues [14]. The leak was due to the postoperative cough, which could break the long suture line.

Nahai [2] described the tensor fascia lata flap as a reliable transposition or island flap vascularized by the lateral circumflex femoral artery that enters the muscle on its deep surface approximately 8 cm distal to the anterosuperior iliac spine. The muscle with a large island of skin may be elevated. The vascular pedicle of the tensor fascia lata supplies only the proximal two-thirds of the thigh. If a longer length is required, pretransfer delay is necessary to ensure complete survival of the entire flap. The skin of the lateral thigh is vascularized by musculocutaneous vessels and distally by fasciocutaneous perforating vessels from the fascia lata [3]. The distal one-third of an extended tensor fascia lata flap has a supplementary vascular supply by the posterior perforators from the deep femoral artery and anterior musculocutaneous perforators from the vastus lateralis muscle. Therefore, the distal part of the flap is almost a random pattern flap, and a delay procedure for the distal thigh skin is advocated. This is significant especially for esophageal reconstruction in which leakage is of major concern. With this method a large flap of 40 by 12 cm can be used for esophageal reconstruction. It prevents the complications of leakage and stricture, and increases the realm of esophageal reconstruction. In our opinion, the main advantage of this method is to obtain reliable vascularized tissue, with a large skin territory for the creation of a long skin tube. With this prefabrication, neovascularization from an underlying muscle occurs by capillary budding that establishes vascular connection with the existing vessels in the overlying skin. Also the long suture line has healed before transfer; therefore, it can defend the intestinal juice after transfer to avoid fistula formation.

The donor site is closed with split skin graft, which can be excised at a later date if the patient so requests. Liposuction or a debulking procedure can be used to reduce the bulkiness of some skin flaps such as tensor fascia lata flap at the neck [8]. Patients who have corrosive injury of the esophagus are usually skinny due to inadequate nutritional supply from jejunostomy feeding. Thus, bulkiness is not a serious problem. The donor site may have intermittent pain, which disappears gradually. No walking impairment was noted. Cosmetically a long skin tube in the subcutaneous tunnel is often bulky. If the long suture line has healed before transfer it can be placed in the substernal position without the risk of mediastinitis. This technique of skin flaps also allows improvement of cosmetic result.

In conclusion, prefabrication of skin flap is a good choice for difficult patients with esophageal defects due to: (1) secure suture line healing before transfer to withstand the intestinal juice, (2) achieving complete viability of the distal part if the flap has to be extended beyond its regular length, and (3) extra tissue available with good vascularity for two-layered anastomosis at the junction of skin and mucosa to prevent leakage.

The need to wash food down with water or to manually compress food down a skin tube is certainly less than ideal. This should be emphasized. The microvascular transfer of a previously fashioned skin tube to replace the esophagus adds to the armaments of methods to reestablish alimentary tract continuity. However, the indications are rare. It is the "last ditch" procedure when all else for esophageal replacement have failed.

	References

Top Abstract Introduction Patients and methods Results Comment References

 

1. Khouri R.K., Upton J., Shaw W.W. Principles of flap prefabrication. Clin Plast Surg 1992;19:763-771.[Medline]
2. Nahai F. The tensor fascia lata flap. Clin Plast Surg 1980;7:51-56.[Medline]
3. Nahai F., Hill L., Hester T.R. Experiences with the tensor fascia lata flap. Plast Reconstr Surg 1979;63:788-799.[Medline]
4. Song R., Gao Y., Song Y., et al. The forearm flap. Chin Plast Surg 1982;9:21-26.
5. Chen H.C., Tang Y.B., Noordhoff M.S. Reconstruction of the entire esophagus with "chain flaps" in a case of complicated corrosive injury. Plast Reconstr Surg 1989;84:980-984.[Medline]
6. Chen H.C., Tang Y.B., Noordhoff M.S. Posterior tibial artery flap for reconstruction of the esophagus. Plast Reconstr Surg 1991;88:980-986.[Medline]
7. Chen H.C., Tang Y.B., Noordhoff M.S., Chang C.H., Chang J.P., Lee M.T. Patch esophagoplasty with free forearm flap for focal stricture of pharyngoesophageal junction and cervical esophagus. Plast Reconstr Surg 1992;90:45-52.[Medline]
8. Nakayama Y., Endo T. Pharyngoesophageal reconstruction with a tensor fascia lata free flap. Plast Reconstr Surg 1995;95:400-405.[Medline]
9. Orticochea M. A new method for total reconstruction of nose, the ear as donor site. Br J Plast Surg 1971;24:225-232.[Medline]
10. Taylor G.I., Palmer J.H. The vascular territories (angiosomes) of the body: experimental study and clinical application. Br J Plast Surg 1987;40:113-141.[Medline]
11. Anderson J.E. CT-scanning in the preoperative planning of osseointegrated implants in the maxilla. Int J Oral Maxillofac Surg 1988;17:33-35.[Medline]
12. Erikson E., Branemark P.I. Osseointegration from the perspective of the plastic surgeon. Plast Reconstr Surg 1994;93:626-637.[Medline]
13. Hidalgo D.A. Aesthetic improvements in free-flap mandible reconstruction. Plast Reconstr Surg 1991;88:574-585.[Medline]
14. Harii K., Ebihara S., Ono I., Saito H., Terui S., Takato T. Pharyngoesophageal reconstruction using a fabricated forearm free flap. Plast Reconstr Surg 1985;75:463-474.[Medline]

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