Long-Term Functional Results After Pharyngoesophageal Reconstruction With

the Radial Forearm Free Flap James P. Anthony, MD, Mark I. Singer, MD, Daniel G. Deschler, MD, E. Thomas Dougherty, PhD,

Charles G. Reed, PhD, Michael J. Kaplan, MD, San Francisco, California

For recovery to be deemed adequate, the la- ryngectomized patient requires restoration of both the ability to swallow and to speak.

Innnediate results and long-term functional re- covery after pharyngoesophageal (PE) recon- struction with the radial forearm free flap were studied in 22 consecutive patients who had un- dergone primary (n = 3) or secondary (n = 19) reconstructions after total laryngectomy. Circumferential reconstructions were done in 13 patients (mean length 10 era, range 6 to l(i) and patch reconstructions in 9 patients (defect size range 4 × 4 cm to 8 × 7 cm). Flap leak- age was evaluated for all patients, and postoper- ative diet and ability to swallow were evaluated for 16 patients with an intact tongue base. Voice was evaluated for 6 patients with circum- ferential reconstructions who had later under- gone tracheoesophageal puncture with place- ment of a Blom-Singer voice prosthesis, and the results compared with those of a control group of 5 voice-restored patients who had undergone laryngectomy with prhnary closure of the pharyngoesophagns.

All 22 flaps survived and none of the patients died. Althongh 7 (32%) reconstructions leaked, all but I closed spontaneously. Fourteen (88%) of the patients with an intact tongue base have no dysphagia and are on a regular diet, and 2 remain on an oral liquid diet. Compared with controls, patients with a radial free-flap recon- struction had similar loudness with soft speech (43 dB for controls versus 52 dB for radial pa- tients) and loud speech (61 dB versus 63 dB), comparable fundamental frequencies (136 Hz versus 125 Hz), and increased jitter (2% versus 5%). Speech intelligibility was judged by un- trained listeners as excellent for 4 of the pa- tients with radial flaps and good for the other 2.

From the Division of Plastic and Reconstructive Surgery, Department of Surgery (JPA), and the Department of Otolaryngology 0VIIS, DGD, MJK), the University of California at San Francisco, and the Department of Speech and Audiology, San Francisco Veterans Hospital (ETD, CGR).

Requests for reprints should be addressed to James P. Anthony, MD. Division of Plastic Surgery. University of California, San Francisco, 350 Parnassus, Suite 509, San Francisco. California 94143-0932.

Presented at the joint meeting of the Society of Head and Neck Surgeons and the European Organization for Research and Treatment of Cancer (EORTC), Pads, France. May 25-28, 1994.

The radial free flap offers the advantages of rapid harvest, high flap reliability, and minimal donor-site and patient morbidity. Leakage rate and deglutition restoration were similar to those of other reconstructions, including the free jeju- nal flap. Speech rehabilitation in patients secon- darily reconstructed with the radial free flap was nearly equivalent to that of total laryngectomy patients who have primary closure of the phar- ynx and was superior to that reported with other popular PE reconstructions, including the gastric pull-up and the free jejunal flap.

M " ost patients considered for cervical pharyngeal and • esophageal reconstruction have also had a total la-

ryngectomy. For a successful and complete rehabilitation, these patients require the restoration of both swallowing and voice. The restoration of an adequate speaking voice is vitally important, since many laryngectomized patients consider the loss of speech to be a more socially debili- tating problem than loss of the ability to take food orally. Pharyngeal reconstructive efforts following laryngopha- ryngectomy have traditionally focused only on the restora- tion of normal swallowing, and postoperative voice reha- bilitation has been a secondary consideration. While that is in part attributable to the limited success of older voice restorative techniques (including the artificial electrolar- ynx and esophageal speech), newer methods of postlaryn- gectomy voice rehabilitation can provide greatly improved speech acquisition and intelligibility.

Over the past decade, tracheoesophageal puncture (TEP) has become the surgical method of choice for voice reha- bilitation following total laryngectomy. I'~ The speech pro- duced after TEP and voice prosthesis placement is superior to that produced with either esophageal speech or the arti- ficial electrolarynx. 7 The technique has also been used for patients undergoing pharyngeal reconstruction using a vari- ety of flaps, including the pectoralis major, gastric or colonic "pull-up" procedures, and free jejunum or colon flaps. 813 Voice restoration has also been reported for a patient with a radial free flap used for pharyngeal reconstruction. ~4 We have noted that patients who have undergone TEP with pha- ryngeal reconstructions that lined the pharynx with skin (namely, the deltopectoral and pectoralis major flaps) have superior speech results compared with patients reconstructed with enteric flaps (the gastric pull-up flap or free jejunum flap). Unfortunately, these pedicled skin and myocutaneous flaps have other problems relating to their reliability and ex- cess bulk, and so forth, and in many centers the free jeju- nal flap has gradually emerged as the reconstructive tech- nique of choice for the cervical esophagus. 15-t8

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Figure 1. Anatomy of the radial free flap relevant to esophageal re- construction. The width of the flap should be at least 9 cm to ensure an adequate lumen in the reconstructed segment. This wider flap al- lows the routine incorporation of the cephalic vein, providing additional venous drainage from the flap and enhancing flap reliability. From Anthony et al, 24 with permission.

Our initial experience with the use of the free radial fore- arm flap was for intraoral reconstructions) 92~ In these re- constructions, we were impressed with the reliability, ver- satility, and low donor-site morbidity of this flap. In early 1991, we began using the radial forearm free flap as the flap of choice for patients requiring partial 22 and full cir- cumferential reconstructions 23 of the pharyngoesophagus. The purpose of this study was to analyze the immediate postoperative results and long-term functional recovery of speech and swallowing in patients undergoing radial free- flap reconstruction of the pharyngoesophagus following laryngectomy.

PATI ENTS AND M E T H O D S From January I, 1991 to December 31, 1993, 22 con-

secutive patients at the University of California, San Francisco, and affiliated hospitals underwent radial free- flap reconstructions of the pharyngoesophagus. Their av- erage age was 67 years (range 46 to 79) and 15 (68%) were men. All had undergone total laryngectomy for squa- mous carcinoma and all had received irradiation to the neck prior to their reconstruction. Reconstuctions were per- formed primarily (at the time of tumor removal) for 3 pa- tients and secondarily for 19 patients. All secondary re- constructions were performed either for strictures alone (15

patients) or for pharyngocutaneous fistulas with strictures (4 patients). Prior to surgery, 7 secondarily reconstucted patients were unable to take nutrition orally and the other 12 were unable to swallow solid food. In addition, all 19 of the secondarily reconstructed patients were also unable to receive adequate speech rehabilitation since their pha- ryngeal strictures or fistulas precluded use of either esophageal speech or a voice prosthesis.

In each case, the radial forearm flap was harvested to in- clude the forearm fascia, the radial artery and vena comi- tans, and the cephalic vein (Figures 1 and 2). For cir- cumferential reconstructions, the radial forearm flap was designed to be 9 cm in width and then tubed upon itself. The rationale for this flap design, the specifics of radial forearm flap harvest, and the methods used to tailor this flap for pharyngoesophageal (PE) reconstruction have been previously described 24 and will not be reviewed here. Receptor vessels used for the microsurgical revasculariza- tion of these flaps included the transverse cervical, supe- rior thyroid, facial, and external carotid arteries, and the anterior, internal, and external jugular veins. In all cases, a minimum of two venous anastomoses, usually the cephalic vein and one vena comitans, were performed. The skin of the radial free flap was sewn to the pharynx using a two-layer closure of absorbable sutures. After several pa- tients treated early in this series developed strictures at the junction of the flap and the pharynx remnant, a Z-plasty type of closure, interposing a triangle of skin from the flap into the pharynx, was incorporated into the upper and lower suture lines of all circumferential reconstructions. The forearm donor sites were all covered by unmeshed split- thickness skin grafts harvested from the thigh.

Circumferential reconstructions were performed in 13 pa- tients. The mean length of these circumferential recon- structions was 10 cm (range 6 to 16). Nine patients had patch reconstructions for defects ranging from 4 × 4 cm to 8 × 7 cm. Arm donor sites were covered with an unmeshed split- thickness skin graft. Postoperatively, the arm was splinted for 5 days. Each patient underwent a barium swallow ex- amination at 7 to 14 days. If a fistula was present, patients were given nothing to take by mouth until subsequent bar- ium swallows documented closure of the fistula or until sur- gical closure was performed. Once adequate healing was demonstrated, the patient's diet was advanced as tolerated. TEP and placement of a voice prosthesis was done 6 weeks after the reconstruction. All patients were free of tumor at the time of their functional studies.

Average time for the reconstructive procedure and post- operative morbidity were determined for all patients. Since resection of the tongue base will also impair swallowing, only the 16 patients with an intact tongue base were se- lected for swallowing evaluations with final postoperative diet and dysphagia assessments.

Eleven patients, 7 circumferential and 4 patch recon- structions, underwent TEP and placement of a voice prosthesis. Six of the circumferentially reconstructed patients underwent quantitative and qualitative voice analysis an average of 4 months after prosthesis place- ment. Only patients with circumferential pharyngeal loss were selected for voice study. In the patients stud- ied, voice loudness, intelligibility, fundamental fre-

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Figure 2. The tubed radial free flap. Note the long pedicle lenglfl and wide separation between the radial vessels (below) and the cephalic vein (above). This distance between the flap vessels can facilitate microsurgical anastomoses when the receptor artery and veins are widely separated,

quency, and jitter were determined and compared with a control group of 5 patients who had undergone total laryngectomy with immediate primary closure of the pharyngoesophagus, followed by later TEP. Control pa- tients had all undergone tumor resection with primary closure of the pharyngeal remnant and had had their voice prostheses an average of 16 months at the time of voice testing.

Voice testing was directed by two trained speech pathol- ogists (ETD and CGR) and performed using a standard- ized set of vocal tasks. Patients were first asked to pro- duce a sustained "a," and a 1-second sample from the middle of the phonation was used to calculate loudness and jitter. Patients then read "The Rainbow Passage" and "The Grandfather Passage," standardized passages that allow the listener to rate speech intelligibility and con- tent. Finally, patients read from one of four standardized lists of phonetically balanced single-syllable words con- taining a distribution of phonemes proportional to their incidence in the English language. Voice signal record- ings were taken via a Bruel Kjaer 1-inch condenser mi- crophone (cartridge type 4132) placed 30 cm from the speaker's mouth. Acoustic signals were fed into a mi- crophone amplifier, processed by a Sony PCM-501ES digital processor, and stored on a Panasonic AG-1900 video cassette recorder. Data acquisition was done with the analog-to-digital convertor of a Creative Technology, Ltd Sound Blaster 16 ASP analog and digital I/O system in a Vanguard 486 personal computer. All signals were sampled at 44.1 kHz.

Amplitude, dynamic range, fundamental frequency, and jitter were analyzed for each voice sample, and mean value and range were calculated for each parameter for the two groups. The recordings taken from each study subject were then used to evaluate speech intelligibility. Speech intelli- gibility was determined by a group of six independent, un- trained listeners unaware of the type of reconstruction that had been performed.

R E S U L T S All 22 radial free flaps were successfully revascularized

and remained viable. The average time for flap harvest, in-

set, and microsurgical revascularization averaged 5.1 hours (range 2.5 to 7.5). Because flap harvest began with the tu- mor ablation or exposure of the pharyngeal fistula or steno- sis, the free-flap reconstruction actually added only 1.5 to 4.5 hours to each procedure.

The average length of follow-up for the 22 patients in this series was 12 months. Postoperatively, none of the pa- tients died and no significant wound complications devel- oped. Overall, 7 (32%) of these reconstructions (5 cir- cumferential, 2 patch) had radiographically demonstrated pharyngeal leakage. Minor diffuse cellulitis of the neck de- veloped in 3 other patients, and they may have had small, undetected leaks although their barium swallows were nor- mal. These 3 patients responded to treatment with antibi- otics and took nothing by mouth, and none developed a fistula. After a week of this treatment, all 3 tolerated an oral diet without further incident. All 7 radiologically proven leaks developed in the horizontal proximal or dis- tal suture lines and not along the vertical suture lines where circumferential flaps had been tubed upon themselves or where patch flaps were sewn to the remaining posterior pharyngeal wall. Patients with documented leaks were placed on tube feedings, and all but one leak dosed spon- taneously within 3 weeks. The single patient who failed to respond to this conservative treatment developed a pharyn- gocutaneous fistula, which was debrided and closed suc- cessfully at a second operation 5 weeks after the initial re- constructive procedure.

Two patients (9%) have required dilations of their radial forearm flap pharyngeal reconstructions. Both had under- gone circumferential pharyngeal reconstructions, and both strictures occurred at the inferior junction of the flap and the esophagus. These two strictures occurred early in our experience, prior to our adoption of a Z-plasty technique to suture the flap to the tongue base above and the esophageal remnant below.

Following radial free-flap harvest, there was excellent take of the forearm skin graft in 21 patients (95%). One patient had a 10% area of skin-graft loss over the flexor carpi radialis tendon. This wound was treated with local care and kept moist, and it epithelialized within 4 weeks. There were no complications at the thigh skin-graft donor

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TABLE Voice Analysis in Laryngectomized Patients With a

Radial Free Flap Reconstruction or Primary Closure (Controls} of the Pharynx

Controls Radial Flap (Primary Closure)

In = 6) In = 5) Loudness (in dB)

Soft speech 52 43 Loud speech 63 61

Fundamental frequency(in Hz) 125 136 Jitter 5% 2% d13 = decibels; Hz = hertz.

sites. Hyperesthesia over the sensory branches of the ra- dial nerve developed in 3 patients (14%); it resolved within 6 months for 2 patients, but 1 patient required resection of a neuroma of this nerve and is now pain-free.

When questioned an average of 8 months after recon- struction, 14 of the 16 patients (88%) with an intact tongue base had no dysphagia and were on a regular diet of solid food. The other 2 patients have required pha- ryngeal dilations for recurrent strictures and are primar- ily on a liquid diet. None of these patients is dependent upon tube feedings.

Patients have tolerated their voice prostheses well after ra- dial free-flap reconstructions. Prostheses are typically placed a centimeter below the inferior end of the flap, into the na- tive esophagus, although they have also been placed into the flap itself when the flap extends below the level of the tra- cheostomy. Speech results for the 6 tested patients with ra- dial free-flap reconstructions were very similar to those for the 5 control patients who had undergone primary closure of the pharynx after laryngectomy (Table). Compared with controls, patients with circumferential radial free-flap re- constructions demonstrated similar loudness with soft speech (average 43 dB for control patients and 52 dB for radial free-flap patients) and with loud speech (61 dB and 63 dB, respectively). Fundamental frequencies were also comparable (136 Hz for controls versus 125 Hz for free-flap patients), although the flap patients had increased jitter (5% compared with 2% for controls). Naive listeners judged speech intelligibility of all 5 controls to be excellent. Among the 6 patients who had a radial free-flap reconstruction of the pharynx, these same listeners judged speech intelligi- bilty to be excellent for 4 patients and good for 2.

C O M M E N T S Over the past several decades, many methods of PE re-

construction have been developed. While no one method will be optimal for all patients, we believe the radial fore- ann free flap has a number of advantages that combine to make it the reconstructive method of choice for most pa- tients after pharyngolaryngectomy. Attributes of the radial forearm flap include a rapid harvest, high flap reliability, low donor morbidity, and as the present study has shown, excellent restoration of both speech and swallowing.

The radial forearm flap offers the combined advantages of rapid harvest, a long, large-caliber vascular pedicle, a high flap viability rate, and the possibility of customization

to fit virtually any size pharyngeal defect. This flap is long enough to reconstruct every defect in the cervical esopha- gus and will reach well into the chest. The longest flap used in this series was 16 cm, although we have used radial free flaps as long as 18 cm in extremity reconstructions, and even longer flaps can be designed if needed. From the time of its initial description, 19-2° the radial free flap has had one of the highest success rates of any microvascular free flap, generally more than 95% in most series, including our own. 23,25 This exceptional flap reliability is due to a com- bination of a large (2 to 2.5 mm) artery and several avail- able veins within the flap. The multiple veins allow several venous anastomoses to be routinely performed. That is par- ticularly important to avoid free-flap failure, since such fail- ures are usually the result of venous obstruction or throm- bosis. 26.27 In this series the routine performance of two or more venous anastomoses allowed us to avoid flap failure, even though all patients were irradiated and most (86%) had undergone previous neck surgery, both factors believed by some to increase the incidence of flap failure. 2s,29 In comparison with the radial free flap, the free jejunal flap preferred by many for pharyngeal reconstruction has one of the lowest success rates of any flap, averaging only 88% in a review of I0 of the largest recent series. Is

The donor morbidity of the radial forearm flap is also relatively low. 21 In comparison, jejunal harvest requires a laparotomy followed by a bowel resection and reanasto- mosis, and thus carries a much higher morbidity than the radial forarm flap/s Furthermore, complications relating to jejunal harvest, including bowel anastomotic leakage, bowel obstruction, and abdominal wound dehiscence, tend to be much more severe and may even be fatal. Is.3°

Leakage and stricture rates and postoperative restoration of swallowing with the radial free flap described in the present series are comparable with reports of other series of pharyngeal reconstructions using the jejunal free flap.IS Careful technique and a two-layer closure of the tubed ra- dial free flaps have lowered the leakage rates since this flap was initially described. 23 As with other types of PE reconstructive techniques, when radial forearm recon- structions leak postoperatively, they do so from the hori- zontal upper or lower pharyngeal flap suture lines and not from the vertical suture lines, probably because of higher tension along these horizontal suture lines. When radial free flaps do leak, the leaks tend to be minor and, because of the excellent flap vascularity, they generally close quickly with only conservative treatment. These results with the radial forearm flap and our prior experience with the free jejunal flap have led us to conclude that neck com- plications and postoperative swallowing rehabilitation are roughly equivalent for the two flaps.

In this study, speech rehabilitation in patients secondar- ily, circumferentially reconstructed with the radial free flap was nearly equivalent to that of total laryngectomy patients who have primary closure of the pharynx after partial-cir- cumference resections. In contrast, voice acquisition after free jejunal reconstruction tends to be poor, with placement of a voice prosthesis generally resulting in a soft, gurgling, often unintelligible voice/7.Is While more sophisticated testing may detect subtle speech differences between pa- tients with radial free-flap reconstructions and those with

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primary closure of the pharynx, speech rehabilitation after the radial free flap is clearly excellent 31 and superior to that of patients reconstructed with the free jejunum.

Most patients in this series were reconstructed secondar- ily after attempts at primary closure of the pharyngeal rem- nant resulted in a fistula or stricture, or both. Primary ra- dial free-flap reconstructions should be considered for previously irradiated patients or for cases in which the di- ameter of the pharyngeal remnant will be less than 2.5 cm after tumor resection. Such immediate reconstructions gen- erally add no more than 2 to 3 hours to the ablative pro- cedure and allow swallowing and voice rehabilitation to begin soon after surgery.

The results of this study indicate that the radial forearm free flap is an excellent choice for pharyngeal reconstruc- tion in most patients. This flap has proven itself to be one of the most reliable free flaps, has a low donor morbidity, and can be quickly and easily customized for use as either a simple patch or tubed upon itself for circumferential re- pairs. These flaps allow the restoration of deglutition in most patients, with an acceptably low incidence of fistula and stricture development. The speech results obtained with the patients studied indicate that the radial forearm free flap, unlike most other methods of pharyngeal recon- struction, allows patients to benefit from the best available methods of voice restoration.

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