TONGUE RECONSTRUCTION WITH THE GRACILISMYOCUTANEOUS FREE FLAP

LUCA CALABRESE, M.D.,1* AKIRA SAITO, M.D., Ph.D.,2 VALERIA NAVACH, M.D.,1 ROBERTO BRUSCHINI, M.D.,1

NORIKO SAITO, M.D., Ph.D.,2 VALERIA ZURLO, B.Sc.,1 ANGELO OSTUNI, M.D.,1 and CRISTINA GARUSI, M.D.3

We describe our experience in tongue reconstruction using the transverse gracilis myocutaneous (TMG) free flap after major demolitivesurgery for advanced cancer. This technique was used in 10 patients: seven underwent total glossectomy and three partial glossectomy. Ineight patients we performed motor reinnervation attempting to maintain muscular trophism and gain long-term volumetric stability. Thefollow-up period ranged from 6 to 28 months. The overall flap survival was 100%. Nine out of 10 patients resumed oral intake. Our prelimi-nary experience shows that this flap is a good reconstructive option for total glossectomy patients, whereas it is less suited for reconstruc-tion of hemiglossectomy defects. Functional and objective evaluation of the tongue reconstructed with TMG free flap requires further andstandardized evaluation. VVC 2011 Wiley-Liss, Inc. Microsurgery 31:355–359, 2011.

Total or subtotal resection of the tongue leads to clini-

cally significant swallowing and speech impairment.

Numerous reconstructive techniques including local and

free flaps have been advocated for tongue reconstruction

after total or subtotal glossectomy.1 The rectus abdominis

myocutaneous (RAM) free flap is often used as it pro-

vides an adequate reconstruction volume.2 However in

this literature, there are few reports describing tongue

reconstruction using the transverse gracilis myocutaneous

(TMG) free flap.3–7 In this article, we describe our expe-

rience with the TMG free flap for tongue reconstruction

after total or partial glossectomy.8

PATIENTS AND METHODS

Between June 2007 and May 2009, 10 patients (nine

male and one female) underwent reconstruction of tongue

and floor of the mouth defects after resection of advanced

squamous cell carcinomas. All reconstructions were per-

formed with the TMG flap. The patients’ age ranged

from 26 to 61 years with a mean age of 50.3 years old.

Written informed consent was obtained from all patients.

Total glossectomy was performed in seven patients,

whereas partial glossectomy was performed in the

remaining three. One patient presented with bone inva-

sion and underwent a segmental mandibulectomy in addi-

tion to the glossectomy. Bilateral neck dissection was

performed in all of the patients. In accord with National

Comprehensive Cancer Network guidelines and with our

Institute’s clinical practice guidelines, no patient received

preoperative chemoradiotherapy as all tumors were con-

sidered resectable. Postoperative treatments were dis-

cussed and decided on by our Institute’s multidisciplinary

Tumor Board (Head & Neck Surgery, Radiation Onco-

logy and Medical Oncology).

Table 1 lists the patients (numbered 1–10) and the

details of the treatments rendered. Patient 1 received

standard postoperative radiotherapy (RT) after radical

resection of a T4N0 primary tumor. Patients 2–8 (with

positive lympnodes) were treated with major demolitive

surgery followed by postoperative chemoradiation. Patient

9 presented with a local recurrence; she was previously

treated (outside institution) with transoral surgery and

neck dissection plus postoperative RT and her primary

treatment mode was major demolitive surgery only.

Patient 10 was a previously treated patient (outside insti-

tution, transoral resection), who was treated with major

demolitive surgery followed by postoperative chemoradia-

tion (positive margins).

Motor reinnervation of the flap was performed in

eight patients (coaptation between a branch of the obturator

nerve and the hypoglossal nerve) to maintain muscle tro-

phism. In two patients, the hypoglossal stump was too short

and the reinnervation procedure could not be performed.

Surgical Technique

All reconstructions of the tongue were performed with

a TMG free flap. Demolition and flap harvest took place

simultaneously and were performed by dedicated surgical

teams. In demolition, when possible the hypoglossal nerve

stump was preserved to allow coaptation with the motor

nerve of the gracilis muscle. The neuromotor supply to

the gracilis muscle is a branch of the anterior division

of the obturator nerve, and it runs proximal to the vascular

pedicle. The flap was raised using the conventional

technique described by Yousif et al.9 and included the

1Division of Head and Neck Surgery, European Institute of Oncology (IEO),Milano, Italy2Department of Plastic and Reconstructive Surgery Hokkaido, Hokkaido Uni-versity, Japan3Division of Plastic and Reconstructive Surgery, European Institute of Oncol-ogy (IEO), Milano, Italy

*Correspondence to: Luca Calabrese, M.D., Division of Head and Neck Sur-gery, European Institute of Oncology, Via Ripamonti 435, 20141 Milano, Italy.E-mail: luca.calabrese@ieo.it

Received 1 September 2010; Accepted 23 December 2010

Published online 18 April 2011 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/micr.20885

VVC 2011 Wiley-Liss, Inc.

entire muscle, vascular pedicle, and motor nerve (Fig. 1).

After the primary tumor was resected and the recipient ves-

sels prepared the pedicle was separated and the flap was

transferred to the oral cavity. The muscle was oriented lon-

gitudinally between the anterior part of the mandible and

the hyoid bone. The distal part of gracilis muscle was

folded and placed on the floor of mouth (Fig. 2). The hyoid

bone was suspended from the mandibular ramus laterally

with two absorbable sutures (Fig. 3). Microvascular anasto-

moses were performed between the vascular pedicle of the

flap and the available recipient vessels: in all cases arterial

anastomoses were ‘‘end-to-end’’ with the facial artery and

venous anastomoses were ‘‘end-to-side’’ with the internal

jugular vein. When possible, the hypoglossal nerve was

coapted to the cut end of the obturator nerve branch. Intra-

operative washing with papaverine was performed on the

sutured vessels. The skin portion of the flap was sutured to

the mucosal defect at the base of tongue: the two opposing

lobes were sutured to the tonsilar pillars and the central

(medial) lobe was used to reconstruct the tip of neotongue.

The skin paddle was drawn as a three lobed flap, and

the resulting donor site defect was closed primarily using

a ‘‘T’’-configuration: the greatest length hidden in the in-

guinal fold and the short vertical part along the internal

surface of the thigh.

Postoperative Care

The flap was monitored clinically every 2 hours for the

first 48 hours, initially by a surgeon and subsequently by

trained nursing staff. Subsequent monitoring of the flap

occurred three times daily for the first postoperative week.

Clinical monitoring consisted of evaluation of the color,

refill-time, bleeding, and tactile temperature of the flap.

Doppler ultrasound evaluation of the vascular pedicle was

performed depending on clinical need. Enoxaparine 4000

UI/day was administered to all patients the night before sur-

gery and in the first seven postoperative days. Postoperative

speech rehabilitation began on the 5th day and swallowing

rehabilitation on the 7th day. Swallowing evaluation was

performed with video-fluoroscopy for all patients. Barium

based meals of different consistency were employed to

evaluate laryngeal penetration and aspiration. All patients

received perioperative antibiotic therapy that was continued

postoperatively for 5 days or longer if clinically indicated.

RESULTS

All flaps survived and partial necrosis was not

observed. All patients but one regained oral intake and

none of the patients required total laryngectomy. Two

patients developed minor fistula, and one of them required

surgical revision for closure. One patient developed an

infection of the neck that was treated surgically and with

Table

1.Patients

Classificatio

n,Treatm

ent,Feeding,andDiseaseStatus

Number

Age

Sex

TNM

Typeofresection

Reinnervation

Radiationtherapy

Food

Complications

Complicationtreatm

ent

Diseasestatus

161

MpT4apN0

Totalglossectomy

Yes

Yes

PEG

Minorfistula

Dressings

NED

252

MpT4apN2b

Partialleftglossectomy

Yes

Yes

Norm

al

NED

353

MpT4apN2b

Totalglossectomy

No

Yes

Norm

al

Recurrence

457

MpT4apN2c

Totalglossectomy

þmandibularresection

No

Yes

Norm

al

Neck

infection

Surgicalrevision

Death

MI

542

MpT4apN2b

Partialleftglossectomy

Yes

Yes

Norm

al

NED

640

FpT4apN1

Totalglossectomy

Yes

Yes

Pureed

Minorfistula

Surgicalrevision

NED

762

MpT4apN2b

Rightpartialglossectomy

Yes

Yes

Norm

al

NED

849

MpT4apN2b

Totalglossectomy

Yes

Yes

Norm

al

NED

967

FpT4N0

Totalglossectomy

Yes

Preop

Pureed

NED

10

26

MpT4aN0

Totalglossectomy

Yes

Yes

Norm

al

NED

TNM,internationalclassificationoftumours;T,primary

sitetumour;N,lim

phnodesinvo

lvment;M,distantmetastasis;PEG,percoutaneousgastrostomy;NED,noevidenceofdisease;MI,myo

cardialinfarction.

356 Calabrese et al.

Microsurgery DOI 10.1002/micr

additional antibiotic intravenous therapy without compro-

mise of the TMG flap.

Video-fluoroscopy with barium meals of different con-

sistency was performed 1 week after surgery to evaluate

bolus propulsion, aspiration, and palato-glossal contact. All

patients but one (patient 1) showed absence of significant

aspiration phenomena with liquid meals and a good neo-

tongue palatal contact with a small deficit of bolus propul-

sion in the posterior portion of the oral cavity for semisolid

meals. Patient 1 showed 10% aspiration and inadequate

palatal contact; therefore, a feeding gastrostomy (percouta-

neous gastrostomy) was placed. The patient with anterior

mandibulectomy (patient 4) showed oral incontinence;

however, effective swallowing was achieved with compen-

satory manouvers (extended head). Seven patients resumed

normal consistency diet; whereas, two patients resumed a

pureed diet. All patients recovered intelligible speech.

The TMG flap provided good tongue contour with

sufficient bulk following total glossectomy (Fig. 4). Volu-

metrically the flaps remained stable during the follow-up

period without clinical atrophy in all patients, and no vol-

untary movements of the reconstructed tongue observed.

Sensory return was not assessed because a motor reinner-

vation was performed.

Clinical follow-up ranged from 6 to 28 months with an

average of 15 months. One death was recorded 2 years af-

ter surgery without evidence of disease (myocardial infarc-

tion), and one patient developed a local recurrence 18

months after surgery. At the last follow-up evaluation, the

remaining patients did not show any evidence of disease.

DISCUSSION

Tongue reconstruction after major demolitive surgery

has advanced significantly with the use of free tissue trans-

fer. However, a completely functional tongue reconstruction

Figure 4. One-month postoperative appearance of the recon-

structed tongue. [Color figure can be viewed in the online issue,

which is available at wileyonlinelibrary.com.]

Figure 1. Harvested flap including the whole muscle. [Color

figure can be viewed in the online issue, which is available at

wileyonlinelibrary.com.]

Figure 2. Insetting of the flap in the oral cavity. The muscle is ori-

ented longitudinally between the anterior part of the mandible and

the hyoid bone. The distal part is folded and placed on the floor of

mouth (as indicated by the arrow). [Color figure can be viewed in

the online issue, which is available at wileyonlinelibrary.com.]

Figure 3. Suspension of the hyoid bone from the mandibular ramus

laterally with two absorbable sutures (suspension direction indi-

cated by arrows).

Tongue Reconstruction with TMG Free Flap 357

Microsurgery DOI 10.1002/micr

cannot be performed with current methods and, to achieve

better results, refinements of the available surgical techni-

ques are still necessary.10

Tissue bulk is important when approaching recon-

struction after total or subtotal glossectomy;7 however,

the ablative defect cannot be considered simply as a

volumetric unit to be filled. The components of each

reconstructive flap (fat, muscular tissues, and tendinous

structures) must be taken into account as they can afford

dynamic qualities (pliability, rigidity, ability to be sus-

pended, and volumetric stability over time) to the volume

they recreate. Naturally donor site morbidity must also

be taken into account, as it can be readily visible and

debilitating.

Among the reconstructive options available, the RAM

flap is most frequently indicated after total or subtotal

glossectomy.11–13 It requires a sophisticated surgical tech-

nique, and it is limited in the amount of muscle that can

be harvested. This is particularly true in patients with an

important cough reflex or history of chronic obstructive

pulmonary disease in whom flap harvest may weaken the

abdominal wall significantly. These limitations led us to

avoid using the RAM flap for tongue reconstruction and

to date we have no direct experience in its use.

The anterolateral thigh (ALT) flap has been our work-

horse in reconstruction of total and subtotal glossectomy

defects as it fulfills the requirements of what we consider

ideal: an adequate volume when compared with the abla-

tive defect, a reliable vascular pedicle, the ability to be

harvested as a compound flap, and a moderate morbid-

ity.14 In Caucasian patients, the ALT flap offers a good

volume of adipose and subcutaneous tissue, affording the

ability to harvest a portion of the vastus lateralis muscle

and the strong and flat fascia lata. The muscular compo-

nent can be reinnervated and it is often inset in the floor

of the mouth region to improve the tongue volume. It

offers a stiffer texture and has a reasonable long-term

volumetric stability of the reconstructed defect. The fas-

cia lata is used to suspend the flap to fixed structures

such as the mandible and the hyoid bone in an attempt to

recreate a dynamic suspension.

Our clinical experience with the ALT flap showed

that, particularly for total glossectomies, a larger amount

of tissue was necessary to provide the patient with better

glossopalatal contact and bolus propulsion. We hypothe-

sized that a larger initial reconstructive volume may com-

pensate for the unavoidable flap atrophy that can nega-

tively impact the patient’s swallowing ability. We chose

the reinnervated TMG flap because it allowed harvest of

a larger amount of tissue when compared with the ALT

flap, we could achieve a more aesthetic scar at the donor

site and we further hypothesized that the reinnervated

muscular component of the flap might remain trophic and

therefore maintain a more stable volume over time.

In the available scientific literature, there are few

studies evaluating the usefulness of the TMG flap for

tongue reconstruction.3–7 The published data is encourag-

ing; however, it is characterized by heterogeneity in the

flap insetting techniques and what is termed a ‘‘func-

tional evaluation’’ of the TMG flap is far from standar-

dized.15,16 Yousif et al. reported eight cases of a reinner-

vated gracilis muscle transfer after total glossectomy.

The muscle was suspended from the mandibular ramus

laterally and centrally to the hyoid bone. Electromyo-

graphic evaluation of the neotongue was performed in

two patients: one patient had active elevation of the neo-

tongue with a demonstrated motor action potential; the

other patient had partial reinnervation on electromyogra-

phy but with minimal clinical flap movement. In this se-

ries, seven out of eight patients regained oral intake;

however, placement of a feeding gastrostomy was neces-

sary to supplement the daily caloric intake.3 In a case

report, Yoleri et al. described the innervated gracilis

myocutaneous flap to reconstruct a total glossectomy

defect. The muscle was placed longitudinally and anch-

ored from the remaining tongue base and pharynx to the

mandible; it was folded onto itself and suspended to the

hyoid bone. The patient was able to resume oral feeding

without aspiration.4 Sharma et al. reported on two

patients who underwent tongue reconstruction with two

different free flaps simultaneously. The authors tried to

provide movement and elevation to the neotongue using

the reinnervated TMG flap, and attempted to add a secre-

tory component to maintain lubrication of the oral cavity

by transferring simultaneously a gastro-omental flap

including gastric-mucosa. The glossopalatal contact was

recreated using the gastric flap; however, the patients

also required a laparotomy. The gracilis flap was har-

vested as a muscular flap only and used to reconstruct

the floor of the mouth. Electromyographic results showed

effective innervation of the gracilis muscle with active

generation of motor unit potentials when the patient

attempted to elevate the tongue.5 Kropf et al.6 reported

on a clinical case where the TMG flap was used to

reconstruct a partial glossectomy defect; however, the

postoperative functional results were not described in

detail. Yu and Robb presented a series of 94 defects af-

ter total or near-total glossectomy reconstructed with dif-

ferent flaps including two cases that employed the graci-

lis flap. The authors suggested that all patients who had

undergone postoperative RT showed significant atrophy

and fibrosis of the reconstructed tongue.7

We performed tongue reconstruction with the TMG

free flap in 10 patients. When compared with Yousif

et al., we used a different insetting of the flap: the mus-

cle was oriented longitudinally between the mandibular

body and the hyoid bone to form a sling and the distal

portion of the gracilis muscle was folded to recreate the

358 Calabrese et al.

Microsurgery DOI 10.1002/micr

remaining portion of the floor of mouth or the tip of the

tongue. Suturing the flap to the hyoid bone guarantees an

efficient suspension of the larynx during swallowing

movements. The flap was successfully able to provide

adequate bulk for the neotongue; the quality of the mus-

cle and its ribbon shape are ideal to create a sufficiently

stiff yet adequately mobile structure for the floor of

mouth. Nine out of 10 patients regained complete oral

intake without necessity of gastrostomy support and all

patients regained intelligible speech.

The available literature shows that there is not a clear

definition as to what constitutes a ‘‘functional reconstruc-

tion’’ of the tongue. Most evalutations focus differently on

the ability to resume oral feeding, meal consistency, avoid-

ance of aspiration, gastrostomy, and laryngectomy.17–19

The assessment of speech intelligibility in postablative sur-

gery patients is also lacking standard, homogeneous, objec-

tive, and reproducible evaluation.17–19 In light of these

considerations, our own assessment was simple and limited

to the ability to resume oral feeding without aspiration and

a subjective recording of intelligible speech patterns.

In this series, flaps were harvested with a motor nerve

component; however, in two cases, it was not possible to

perform the nerve coaptation as the hypoglossal nerve

stump was too short. Contrary to our initial hypothesis,

we didn’t notice a faster atrophy of the flap in the non-

reinnervated flaps; however, this aspect needs to be eval-

uated over a longer period of time. Despite the reported

reliability in the isolation and the quality of the vascular

pedicle, we have found that at times it can be very short

and the vein caliber small. Furthermore, the flap is too

bulky for reconstruction of hemiglossectomy defects as a

result of the considerable thickness of the subcutaneous

adipose tissue, particularly in overweight patients.

CONCLUSION

The TMG flap is an uncommon choice for tongue

reconstruction; however, our preliminary experience, in

agreement with the available published literature, shows

that this flap is a good reconstructive option for patients

who undergo a total glossectomy. For partial glossec-

tomy, we discourage the use of this flap because it is too

bulky. The functional and objective evaluation of the

tongue reconstructed with the TMG free flap requires fur-

ther and standardized studies on larger patient cohorts.

REFERENCES

1. Haddock NT, DeLacure MD, Saadeh PB. Functional reconstructionof glossectomy defects: the vertical rectus abdominus myocutaneousneotongue. J Reconstr Microsurg 2008;24:343–350.

2. Yamamoto Y, Sugihara T, Furuta Y, Fukuda S. Functional reconstruction ofthe tongue and deglutition muscles following extensive resection of tonguecancer. Plast Reconstr Surg 1998;102:993–998; discussion 999–1000.

3. Yousif NJ, Dzwierzynski WW, Sanger JR, Matloub HS, CampbellBH. The innervated gracilis musculocutaneous flap for total tonguereconstruction. Plast Reconstr Surg 1999;104:916–921.

4. Yoleri L, Mavioglu H. Total tongue reconstruction with free func-tional gracilis muscle transplantation: A technical note and review ofthe literature. Ann Plast Surg 2000;45:181–186.

5. Sharma M, Iyer S, Kuriakose MA, Vijayaraghavan S, Arun P, SudhirVR, Chatni SS, Sharan R. Functional reconstruction of near totalglossectomy defects using composite gastro omental-dynamic graci-lis flaps. J Plast Reconstr Aesthet Surg 2009;62:1277–1280.

6. Kropf N, Cordeiro CN, McCarthy CM, Hu QY, Cordeiro PG. Thevertically oriented free myocutaneous gracilis flap in head and neckreconstruction. Ann Plast Surg 2008;61:632–636.

7. Yu P, Robb GL. Reconstruction for total and near-total glossectomydefects. Clin Plast Surg 2005;32:411–419, vii.

8. Calabrese L, Giugliano G, Bruschini R, Ansarin M, Navach V,Grosso E, Gibelli B, Ostuni A, Chiesa F Compartmental surgery intongue tumors: Description of a new surgical technique. Acta Otorhi-nolaryngol Ital 2009;29:259–264.

9. Yousif NJ, Matloub HS, Kolachalam R, Grunert BK, Sanger JR. The trans-verse gracilis musculocutaneous flap. Ann Plast Surg 1992;29:482–490.

10. Kimata Y, Sakuraba M, Namba Y, Hayashi R, Ebihara S. Functionalreconstruction with free flaps following ablation of oropharyngealcancer. Int J Clin Oncol 2005;10:229–233.

11. Wechselberger G, Schoeller T, Bauer T, Schwabegger A, Ninkovic M,Rainer C,,Ninkovic M. Surgical technique and clinical application of thetransverse gracilismyocutaneous free flap. Br J Plast Surg 2001;54:423–427.

12. Lyos AT, Evans GR, Perez D, Schusterman MA. Tongue reconstruc-tion: Outcomes with the rectus abdominis flap. Plast Reconstr Surg1999;103:442–447.

13. Nakatsuka T, Harii K, Yamada A, Asato H, Ebihara S. Versatility ofa free inferior rectus abdominis flap for head and neck reconstruc-tion: Analysis of 200 cases. Plast Reconstr Surg 1994;93:762–769

14. Yu P. Reinnervated anterolateral thigh flap for tongue reconstruction.Head Neck 2004;26:1038–1044.

15. Huemer GM, Bauer T, Wechselberger G, Schoeller T. Gracilis mus-cle flap for aesthetic reconstruction in the head and neck region.Microsurgery 2005;25:196–202.

16. Wechselberger G, Schoeller T, Bauer T, Schwabegger A, Ninkovic M,Rainer C, Ninkovic M. Surgical technique and clinical application of thetransverse gracilismyocutaneous free flap. Br J Plast Surg 2001;54:423–427.

17. Archontaki M, Athanasiou A, Stavrianos SD, Korkolis DP, FaratzisG, Papadopoulou F, Kokkalis G, Rapidis AD. Functional results ofspeech and swallowing after oral microvascular free flap reconstruc-tion. Eur Arch Otorhinolaryngol 2010;267:1771–1777.

18. Yanai C, Kikutani T, Adachi M, Thoren H, Suzuki M, Iizuka T.Functional outcome after total and subtotal glossectomy with freeflap reconstruction. Head Neck. 2008;30:909–918.

19. Hsiao HT, Leu YS, Lin CC. Tongue reconstruction with free radialforearm flap after hemiglossectomy: A functional assessment.J Reconstr Microsurg 2003;19:137–142.

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