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Sensate Radial Forearm Free Flaps in Tongue Reconstruction
M. Abraham Kuriakose, MD;
Thom R. Loree, MD;
Alice Spies, RN, RNFA, CNOR;
Sandy Meyers, MS, OTR;
Wesley L. Hicks, Jr, MD
Arch Otolaryngol Head Neck Surg. 2001;127:1463-1466.
ABSTRACT
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Background Successful rehabilitation after ablative surgery requires not only the
reconstruction of 3-dimensional form but also the restoration of physiologic
function.
Objective To assess sensory recovery of reinnervated radial forearm flaps used
for tongue reconstruction.
Patients and Methods Seventeen patients, who underwent reconstruction of glossectomy defects
with reinnervated radial forearm free flaps, formed the study group. Recovery
of sensation was measured by both subjective and detailed objective tests
8 months after surgery. Sensory function of the flap was compared with that
of the normal residual tongue or the adjacent oral mucosa and the contralateral
forearm donor site.
Results All patients involved in this study had tongue defects of hemiglossectomy
or greater and adjacent floor of the mouth. Sensory recovery was observed
in all of the 17 patients within 8 months. Detailed sensory testing showed
that median static 2-point discrimination, moving 2-point discrimination,
and pressure sensitivity (1.2 cm, 0.8 cm, and 3.7 psi, respectively) were
subjectively greater in the innervated forearm flaps than in the contralateral
forearm donor site (2.3 cm, 1.7 cm, and 4.6 psi, respectively) (P=.064) and similar to those of the normal tongue (0.9 cm, 0.5 cm,
and 3.6 psi).
Conclusions In all modalities examined, sensate free flaps proved superior in sensory
fidelity to the native forearm donor site and closely approached that of the
normal tongue. Microsurgical reinnervation of flaps should be considered in
tongue reconstruction.
INTRODUCTION
ADVANCES AND refinements in head and neck reconstructive procedures
have shifted the aim of reconstructive surgery from closure of resection defects
to the more complex goal of restoration of form and function of the resected
parts. With the introduction of microsurgical free tissue transfer, the range
of tissues that can be transferred for the reconstruction of oral cavity defects
has dramatically increased.
Innervated free flaps in tongue reconstruction have been proposed to
improve deglutition, speech, and airway protection. The objective of this
study was to assess the level of sensory recovery that may be achieved by
the use of sensate radial forearm free flaps in tongue reconstruction.
PATIENTS AND METHODS
PATIENTS
Twenty-two consecutive patients underwent reconstruction of the tongue
and adjacent floor of the mouth with reinnervated neurofasciocutaneous radial
forearm free flaps. Five patients were excluded from the study, 4 because
of recurrent disease and 1 because of unavailability for follow-up. All patients
included in the study had undergone ablative surgery for squamous cell carcinoma
except for 1 patient with mucoepidermoid carcinoma. All glossectomy defects
were larger than hemiglossectomy according to the classification system proposed
by Urken et al.1 Eight of these patients had
received adjuvant postoperative radiotherapy, and 1 patient received preoperative
radiotherapy. The demographic details of the patients are listed in Table 1.
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Table 1. Demographic and Clinical Details of the 17 Patients
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SURGICAL TECHNIQUE
The radial forearm free flap is harvested from the nondominant arm by
previously well-described techniques2 with a
few modifications to incorporate the sensory element of the flap. A rectangular
skin paddle is designed to be centered over the radial artery and the antebrachial
cutaneous septum. The skin paddle should be confined within the overlapping
zones of the lateral antebrachial cutaneous nerve somatosome3-4
and radial artery angiosome.5-6
This extends from the flexor crease of the wrist to antecubital fossa. The
medial limit is the midline of ventral forearm and laterally over the radial
surface of the forearm to the lateral third of the dorsal surface. For sensate
forearm free flap, the skin paddle is more lateral than that of the conventional
radial forearm free flap.
Care should be taken to identify and preserve the superficial branch
of the radial nerve during the subfascial dissection on the radial side. The
lateral antebrachial cutaneous nerve is a continuation of the musculocutaneous
nerve (C5-6). It pierces the coracobrachialis muscle and runs downward and
laterally between the tendon of biceps and brachialis to reach the lateral
side of the arm. At the interepicondylar line it pierces the deep fascia on
the lateral side of the tendon of biceps and is continued into the forearm
as the lateral antebrachial cutaneous nerve of the forearm.7
The nerve can be identified medial to the cephalic vein as it courses along
with the vein distal to the antecubital fossa. Both the nerve and the vein
are traced toward the skin paddle. The nerve divides into multiple smaller
branches as it traverses distally, making it difficult to identify at this
location. After the vascular anastomosis, the antebrachial cutaneous nerve
is approximated to the cut end of the lingual nerve by interrupted epineurial
sutures.
SENSORY EVALUATION
During routine postoperative follow-up, sensory recovery was evaluated
in all patients. Ten of the 17 patients included in the study were available
for detailed objective sensory evaluation, which was carried out by an experienced
occupational therapist (S.M.). This sensory evaluation was carried out at
8 to 38 months (median, 14 months) after the surgical procedure. The following
tests were performed on the central portion of the flap: (1) subjective ability
to sense food, (2) sharp-dull discrimination, (3) pain sensation, (4) Semmes-Weinstein
monofilament (pressure) sensation, (5) static and moving 2-point discrimination,
(6) hot-cold perception, and (7) sensory recovery of the flap compared with
normal residual tongue or adjacent oral mucosa and the contralateral forearm
donor site.
The subjective assessment was carried out by asking whether the patient
could sense food on the reconstructed tongue after mastication. To determine
the sharp-dull discrimination, a 27-gauge hypodermic needle and a mirror handle
were used to probe the area to be tested. Pain sensation was tested by pinprick
with a 27-gauge needle. Serial stimulation with Semmes-Weinstein monofilament
(North Coast Medicals, Inc, Morgan Hill, Calif) was used to determine the
tactile pressure threshold. To estimate moving and static 2-point discrimination,
a disk-criminator was used. Hot-cold perception was determined with cotton
wool soaked in ethyl chloride and a warmed mirror handle.
RESULTS
All patients included in the study (N = 17) had recovery of subjective
ability to perceive food in the reinnervated free flaps. All of the patients
included in this study were seen monthly after surgery. From retrospective
analysis of the patient records, the time course to subjective recovery of
sensation was determined. In no patient was sensation present at 1 month postoperatively.
In 6 patients, sensation was present at 2 months after surgery. All patients
had sensation at 8 months. Overall, the mean and median time to sensory recovery
was 4 and 3 months, respectively.
Results of the detailed objective sensory evaluations of the study patients
are tabulated in Table 2. Restoration
of sharp-dull discrimination and perception of cold and hot sensation of the
new tongue were observed in all patients who were subjected to detailed sensory
testing (n = 10). Comparison of the thresholds for pressure sensation estimated
by Semmes-Weinstein monofilaments showed the level of recovery of the reinnervated
free flap (3.78 g/mm2) to be closer to that of the normal residual
tongue (3.61 g/mm2) and better than that of the contralateral forearm
donor site (4.56 g/mm2). A similar observation of sensory upgrading
of sensate free flaps was observed with respect to both static and moving
2-point discrimination; none of these observations reached statistical significance.
The average static 2-point discrimination of the flap, normal tongue, and
contralateral donor site were 12, 9, and 22.5 mm, and moving 2-point discrimination,
8, 5, and 17 mm, respectively. None of the patients included in the study
reported dysesthesia.
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Table 2. Results of Sensory Testing
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COMMENT
Oral mucosal sensory feedback plays a critical role in many stomatognathic
functions, such as mastication, oral hygiene, phonation, and swallowing, and
can influence patient quality of life. Kapur et al8
clearly demonstrated the detrimental effects of oral mucosal anesthesia. Their
study showed a proportionally worsening functional impact with an increasing
area of anesthesia. Restoration of sensibility should be, therefore, one of
the important components of the functional rehabilitation of glossectomy defects.
This would require transfer of a composite functional unit with its own vascular
supply (angiosome5-6) and innervated
by a sensory nerve (neurosome3-4).
Taylor et al,3 in detailed cadaveric studies,
demonstrated various neurovascular territories of the body. They observed
that cutaneous nerves often run along with blood vessels in an overlapping
distribution of angiosomes and neurosomes. This work suggests that, clinically,
many of the currently used axial or fasciocutaneous flaps can be potentially
modified as neurovascular flaps.
The successful transfer of neurosomes in extremity reconstruction is
well established.9-13
David14 first reported attempts to restore sensation
in intraoral reconstruction by means of a reinnervated deltopectoral flap.
In this procedure, he anastomosed supraclavicular nerves supplying the flap
to recipient nerves in the head and neck. He did not report results of restoration
of sensation with this technique. In 1979, Franklin et al15
reported an unsuccessful attempt to restore intraoral sensation with the use
of reinnervated dorsalis pedis flaps, where the superficial peroneal nerve
was anastomosed to the lingual nerve. Ten years later, Matloub et al,16 with the use of reinnervated lateral arm flaps, reported
the restoration of sensation in 2 of the 4 flaps used for intraoral reconstruction.
Urken et al17 reported the successful transfer
of a sensate radial forearm free flap for pharyngeal reconstruction through
the anastomosis of the antebrachial cutaneous nerves to the great auricular
nerve. With the use of the same flap, Dubner and Heller18
reported high-fidelity restoration of intraoral sensation. The most conclusive
evidence of recovery of intraoral sensation was reported by Boyd et al.19 In this prospective study of 8 radial forearm free
flaps, they observed the return of sensation in the reinnervated flaps approaching
the quality of sensation of the adjacent normal tissue. Many of the potentially
useful sensate flaps for head and neck reconstruction are listed in Table 3; some, such as the dorsalis pedis
and tensor fascia lata, are included for their historical interest only.
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Table 3. Sensate Free Flaps in Head and Neck Reconstruction
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Neurofasciocutaneous radial forearm free flaps are now considered the
ideal choice of all available flaps for subtotal tongue reconstruction. The
thin skin paddle with minimum subcutaneous tissue is well suited to contour
the glossectomy defect while, at the same time, providing adequate bulk for
reconstruction. These flaps have a very reliable vascular pedicle with an
excellent vessel caliber match to donor vessels in the neck. The radial artery
has a consistent angiosome, which is well documented in cadaveric studies.5 Rhee et al4 studied the
extent of lateral antebracheal cutaneous nerve somatosome by intraoperative
mapping. The mean ± SD surface area was 187 ± 30 cm2,
distributed in an elliptical shape. There was consistency in the 15 neurosomes
tested.
The results from this study have shown that, with reinnervated free
flaps, sensory recovery can be expected in patients as early as 8 months postoperatively.
We have documented that, by microsurgical anastomosis of the lingual nerve
to the lateral antebrachial cutaneous nerve, the sensory function of the radial
forearm free flap approximates that of the normal tongue. The phenomenon of
sensory upgrading has been previously reported in extremity reconstruction24 and in tongue reconstruction by Boyd et al.19 The quality of sensory recovery of the reinnervated
free flaps came close to that of the normal tongue as observed by Semmes-Weinstein
monofilament testing and static and moving 2-point discrimination.
The improvement in tactile pressure sensation observed in the sensate
flaps as compared with the contralateral forearm donor site can be explained
by the higher level of amplification of signals at neuronal synapses and the
larger cortical representation of the tongue in the sensory homunculus as
compared with the forearm. We believe that the improvement of 2-point discrimination
of forearm skin from 22.5 mm to 12 mm is due to the relative sophistication
of the lingual nerve as compared with the lateral antebrachial cutaneous nerve.
The capacity of the sensorium to distinguish between 2 points of stimulation
is effected through a mechanism called lateral inhibition. Virtually all sensory pathways give rise to lateral inhibitory signals
through interneurons. These limit the lateral spread of excitatory signals
and increase the degree of contrast of the sensory pattern perceived by the
sensory cortex. These inhibitory signals occur at each synaptic level: the
gasserian ganglion, thalamus, and sensory cortex. Sensory fidelity is further
augmented by inhibitory descending fibers from the cerebral cortex to these
synaptic levels.25 We believe that the lingual
nerve, with its more refined neuronal pathways, can amplify and increase the
fidelity of impulses received from the forearm skin to obtain near-normal
sensory function.
The return of sensation in noninnervated flaps has been well documented
in head and neck reconstruction.26-28
Although spontaneous reinnervation does occur in noninnervated flaps, it takes
a longer period to develop and it does not restore adequate functional sensation,
nor does it provide useful tactile sensation or 2-point discrimination.29 These sensory modalities are important in a patient's
ability to handle oral secretions and food boluses. A potential problem of
nerve anastomosis is dysesthesia. We did not observe this phenomenon in any
of our patients. Further study is necessary to determine whether better sensation
translates into improved functional outcome. The problem of replication of
the discrete motor functions of the tongue, of course, remains an enigma and
a significant challenge to future reconstructive efforts.
CONCLUSIONS
In all modalities examined, sensate neurofasciocutaneous free flaps
proved subjectively superior in sensory fidelity to the native forearm donor
site and closely approached that of the normal residual tongue. Microsurgical
reinnervation of flaps should be considered, whenever feasible, in tongue
reconstruction.
AUTHOR INFORMATION
Accepted for publication July 25, 2001.
Presented at the Joint Meeting of the Society of Head and Neck Surgeons
and American Society of Head and Neck Surgery, Palm Beach, Fla, May 16, 1998.
A special thanks to Mark DeLacure, MD, for his interest in this project
and to Nestor Rigual, MD, for his editorial expertise.
Corresponding author and reprints: Thom R. Loree, MD, Department
of Head and Neck Surgery, Roswell Park Cancer Institute, Buffalo, NY 14263.
From the Department of Head and Neck Surgery, Roswell Park Cancer Institute,
Buffalo, NY.
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