- Email: [email protected]
Functional comparison after reconstruction with a radial forearm free flap or a pectoralis major flap for cancer of the tongue
Functional comparison after reconstruction with a radial forearm free flap or a pectoralis major flap for cancer of the tongue WAN-FU SU,
MD,
YI-JAN HSIA,
DDS, MDSC,
YEN-CHINE CHANG,
DDS, MDSC,
SHYI-GEN CHEN,
MD,
and HWA SHENG,
PhD,
Taipei,
Taiwan OBJECTIVE: Numerous patients in Taiwan with tongue carcinoma require tongue reconstruction. We compared the abilities of 2 methods of tongue reconstruction to reserve tongue function. STUDY DESIGN AND SETTING: Sixty patients underwent resection of the tumors and reconstruction with a pectoralis major flap or a radial forearm flap. The Chinese articulation test was used to evaluate the place and manner of error production, and a questionnaire on dietary habits was used to evaluate deglutition 6 months to 10 years after reconstruction. RESULTS: Patients with the free flap had more intelligible speech. The questionnaire study showed no significant difference between the 2 groups in swallowing rating. Motility caused by flap pliability increased speech intelligibility more than it did on swallowing function. CONCLUSION: Our experience in a few selected patients shows that the functional outcome of tongue surgery is related to the reconstruction methods used (for speech) and to the extent of tongue resection (for swallowing). (Otolaryngol Head Neck Surg 2003;128:412-8.)
C arcinoma of the tongue is the most common cancer of the oral cavity in Taiwan. The Cancer Registry Annual Report of the Republic of China reported in 1999 that nearly 27 patients per million population in Taiwan develop carcinoma of the From the Departments of Otolaryngology–Head and Neck Surgery (Dr Su), Oral and Maxillofacial Surgery (Drs Hsia and Chang), and Plastic Surgery (Dr Chen), Tri-Service General Hospital, National Defense Medical Center; and the Department of Speech and Hearing Disorder and Science, National Taipei College of Nursing (Ms Sheng). Reprint requests: Wan-Fu Su, MD, Department of Otolaryngology-Head and Neck Surgery, Tri-Service General Hospital, 325, Sec 2, Chen-Kung Road, Taipei, Taiwan 114; e-mail, [email protected]. Copyright © 2003 by the American Academy of Otolaryngology–Head and Neck Surgery Foundation, Inc. 0194-5998/2003/$30.00 ⫹ 0 doi:10.1067/mhn.2003.38 412
tongue each year.1 Treatment strategy consists of radiation therapy alone, surgery alone, or combined surgery and radiotherapy depending on the size of the tumor, the extent of tumor infiltration, and the physician’s preference.2-4 The range of the surgical options available for reconstruction for the patient with cancer of the oral cavity has changed markedly during the past decade. For example, in 1994, Urken and Biller5 designed a bilobed sensate radial forearm flap (RFF) to preserve tongue motility. Although the management of segmental defects of the mandible has been the focus of much attention during the past several decades, it is the soft tissue reconstruction of the oral cavity and, in particular, the tongue that is the most critical factor in achieving a successfully functional result. The tongue uniquely serves a multitude of varied functions, including articulation, mastication, deglutition, and taste. There have been a number of recent reports6,7 that have attempted to define a battery of functional tests for assessment of the rehabilitative outcome after surgery in the patient with cancer of the oral cavity. After reconstructive surgery, the tongue should be evaluated as a single organ even though it serves different functions and may have been reconstructed with different methods and with resulting surgical defects of different sizes. Although the mobile tongue and tongue base serve different purposes in deglutition and speech, they coordinate with each other, especially after surgery. Therefore they should be evaluated together. We report on 60 patients with carcinoma of the tongue base or mobile tongue who underwent 25% to 100% full-thickness resection, and we compare the functional results between the pectoralis major flap (PMF) and RFF reconstructions. The patients were evaluated clinically for speech and swallowing function to determine the flap best suited to restoring speech and swallowing. Particular em-
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Table 1. Patient profile Reconstruction type
Tongue base (n)
Mobile tongue (n)
Hemiglossectomy (n)*
Total glossectomy (n)
Total
Pectoralis major flap Radial forearm flap
1 3
8 5
14 22
3 4
26 34
*Hemiglossectomy indicates surgical defect involving both the base and mobile portions of the tongue.
phasis is placed on the restoration of articulation after RFF transfer.
tent disease or died from concurrent disease and were excluded from this study.
PATIENTS AND METHODS Between July 1988 and July 1999, 76 consecutive patients (61 men and 15 women) with cancer of the tongue underwent resection of the tongue and reconstruction using a PMF, free RFF transfer, or primary closure. None underwent segmental mandibulectomy. Patients were assigned to one procedure or the other on the basis of the size of the defect and physician’s preference. Seventeen patients required a marginal resection of the mandible, which did not influence the continuity, and 60 patients underwent a median or paramedian mandibulotomy for exposure. None of the patients required a laryngectomy for tumor invasion. Partial laryngoplasty was performed in all 7 patients undergoing total glossectomy. A concomitant neck dissection was carried out in every patient undergoing flap reconstruction. Seventy-two patients were previously untreated, and 4 patients with recurrent tumor received combined therapy (radiotherapy, chemotherapy, or partial glossectomy). Sixty selected patients were evaluated for swallowing and speech functions 6 months to 10 years after PMF reconstruction or the radial forearm free flap. Twenty-six pedicled flaps and 34 free flaps were used to reconstruct tongue defects of varying sizes (Table 1). Pectoralis major flaps were used in 3 patients undergoing total glossectomy, 14 patients undergoing hemiglossectomy (both the tongue base and mobile tongue), and 9 patients undergoing partial glossectomy (tongue base in 1 and mobile tongue in 8). Free flaps were used in 4 patients undergoing total glossectomy, 22 patients undergoing hemiglossectomy, and 8 patients undergoing partial glossectomy (tongue base in 3 and mobile tongue in 5). The remainder of the 16 patients repaired by primary closure had a persis-
Surgical Technique Ablative procedure. Small resections of mo-
bile tongue (classified as “one-quarter glossectomy” in Urken’s classification scheme)6 may be primarily closed. However when the defect extends to the floor of mouth, then primary closure leads to tethering of the tongue. Since the splitthickness skin is unreliable, we prefer the use of a forearm flap or a PMF to provide bulk of the tongue, as well as epithelial coverage for the oral cavity. In this study, when both tongue base and mobile tongue were involved, resection was classified as hemiglossectomy, unless the defect was smaller than 3 cm and primarily could be closed without significant disturbance in function. We thought that defects of the tongue base are hard to manage by tongue flap reconstruction and led to great disturbances in tongue shape, volume, position, mobility, and, ultimately, function. For patients undergoing reconstruction of the entire tongue or who were left with a nonfunctional residual remnant, the tongue base was always resected down to the hyoid bone, including the hypoglossal nerve and lingual artery, as well as varying portions of the vallecula and pharyngeal wall. Partial laryngoplasty was done to ensure protection against aspiration. Reconstructive procedure. Our surgeons first tended to use the PMF because of its simplicity in design, ease of dissection, and high reliability, especially when bulk is beneficial, such as after subtotal or total glossectomy. Preference for this method was challenged by an increase in the use of microsurgical transfer of a free RFF for intraoral reconstruction. The RFF and its use in intraoral reconstruction have been described in many reports.5,7 In this study there was no attempt to restore neurologic function.
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Table 2. Comparison between Chinese consonant phonemes and phonemes of the international phonetic alphabet Stop
Affricate
Place/manner
U
Interlabial Interdental Apical-alveolars Apical-palatals Laminal-palatals Lingua-velars
p
ph
t
h
g
A
U
A
ts
tsh
ts tc¸
tsh tc¸ h
t
k
Nasals
Fricatives
n z c¸ h
s
Apical, tongue tip; laminal, dorsal surface of tongue; U, Unaspiration; A, aspiration.
Clinical evaluation of deglutition included a questionnaire on dietary habits and a swallowing rating of 1 to 7,8 in which swallowing ability was rated 7 to indicate no complaints; 6, minimal complaints and totally able to swallow a bolus without difficulty; 5, minimal complaints and totally able to swallow without a bolus (dry swallowing) without difficulty; 4, moderate complaints and difficulty swallowing a bolus; 3, moderate complaints and difficulty dry swallowing; 2, severe complaints and difficulty swallowing a bolus and dry swallowing; and 1, severe complaints and unable to swallow. Food consistency between the Chinese diet and Western diet is somewhat different. Thus, the Chinese diet is classified into liquid, semisolid (noodle), and solid food (rice). One experienced speech pathologist, one head and neck surgeon, and patients’ spouses performed a perceptual analysis of the patients’ speech. The evaluated functions included speech intelligibility and Chinese articulation. Intelligibility was determined by the evaluation of the speech pathologist who reviewed and graded a tape of the patient’s speech on a scale of 1 to 7 and by the spouse who interviewed the patient. Intelligibility was rated as 7 to indicate no sound errors are noticed in continuous speech and speech can be understood by spouse easily; 6, sound errors are occasionally noticed in continuous speech and spouse understands every time; 5, speech is intelligible, although noticeably in error, and spouse understands only after listening twice; 4, speech is intelligible with careful listening and spouse understands after listening more than 3 times; 3, speech intelligibility is difficult and the spouse understands after listening more than 3
times and from body language; 2, speech is usually unintelligible and spouse communicates only by body language and guessing; and 1, speech is unintelligible and spouse cannot understand. Chinese consonant phonemes9 (Table 2), compared with phonemes of IPA (international phonetic alphabet), were used to test patients’ articulation because the consonants are the carrier of intelligibility. Each patient’s articulation test score is correlated with the intelligibility scores. The articulation test divides speech errors into 3 types: manner, place, and vocal production. Statistical significance of difference between the 2 groups was determined by using the Student’s t test and Fisher’s exact test. RESULTS Complications consisted of orocutaneous fistulas in 15 patients (8 with pedicled flap and 7 with free flap), infections in 6 patients, and flap skin losses in 13 patients. The fistulas healed with local wound care in 12 patients, and closure with PMF was performed in 3 patients. Eleven patients died from persistent diseases. Donor-site complications included loss of the entire forearm skin flap due to infection in 3 patients who required a second skingrafting procedure. Speech After hemiglossectomy, the main subject of this study, and then PMF transfer, the intelligibility rating fell to category 6 in 1 patient, 5 in 3 patients, 4 in 8 patients, and 3 in 2 patients (Table 3). The average score reached 4.21. After total glossectomy, the PMF transfer did not restore the speech of any patient, with an average score of
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Table 3. Intelligibility and articulation test results according to reconstructive type and primary extent of surgery Primary extent Tongue base* Reconstruction
PMF RFF One-tailed t-test P value
n
Mean score
1 3
6 6.67 —
Mobile tongue SD
n
— 8 0.58 5
Mean score
4.88 5.80 0.087
Hemiglossectomy SD
n
1.25 14 0.84 22
Mean score
4.21 6.23 0.000
SD
Total glossectomy* n
0.80 3 0.81 4
Mean score
SD
1.33 2.75 —
0.58 0.50
PMF, Pectoralis major flap; RFF, radial forearm flap. *The samples were too small to perform a statistical test.
1.33. In those patients receiving RFF transfer, the intelligibility rating fell to 7 in 9 patients, 6 in 10 patients, 5 in 2 patients, and 4 in 1 patient after hemiglossectomy; the average score was 6.23, which was significantly better than the score of 4.21 for PMF transfers (P ⫽ 0.000). Even after total glossectomy, patients receiving RFF transfer were more understandable (category 2 for 1 patient and category 3 for 3 patients) than those receiving PMF transfer. Table 4 indicates that after PMF transfer, patients developed obvious handicaps in the production of apical-alveolar stop, apical-palatal, and lingua-velar consonants. Compared with PMF transfer, all of the parameters in Table 4 were better in RFF transfer recipients, especially in the production of apical-alveolar and apical-palatal consonants, with significant difference. Neither transfer was very successful in restoring lingua-velar contact. The consonants g, k and h were perceived as distorted but intelligible. The distortion of apical-palatal consonant is much more than that of the interdental consonant in PMF groups (P ⫽ 0.016 for nonaspirated affricate and P ⫽ 0.027 for aspirated affricate). Bilabial consonants were less affected by the surgical intervention in both groups because those neck dissections had not injure the marginal branch of facial nerve, except for 3 patients in the PMF group and 2 patients in the RFF group. Swallowing In patients with total glossectomy, liquid diet was the only choice regardless of the flap that was
used (Table 5). In patients with hemiglossectomy, PMF transfer helped 4 patients to eat a regular diet (grade 6), 6 patients to eat a semisolid diet (grade 5), and 4 patients to eat a semiliquid diet with difficulty (grade 4). The average swallowing rating fell to 5.0 only because 5 patients had orocutaneous fistulas, which affected their swallowing ability (grade 4). One of them (secondary reconstruction), whose preoperative diet was limited to liquids, was able to eat noodles after surgery (grade 5). In patients undergoing hemiglossectomy, RFF helped 7 patients to eat regular diets (grade 6), 12 patients to eat a semisolid diet (grade 5), and 3 patients to eat a semiliquid diet with moderate complaint (grade 4). The average swallowing rating fell to 5.43 because of 4 patients with orocutaneous fistulas (grade 4). One of them was able to eat a semisolid diet after secondary reconstruction (grade 5). There was no significant difference between 2 reconstructive methods (P ⫽ 0.061). In the other patients undergoing partial glossectomy, regardless of the flap that was used, they were able to eat regular or semisolid diets only if no complications occurred. DISCUSSION The oral tongue is responsible for oral manipulation of food for the swallow, and the basal tongue is responsible for the oral initiation of the swallow. Thus every effort should be made to reconstruct the oral cavity to permit as much range and coordination of tongue motion as possible. In assessing 12 patients with cancer of the tongue, Freelander et al10 found no differences as far as patients were concerned in the functional outcome
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Table 4. Articulation test results of hemiglossectomy patients after pectoralis major flap (PMF) and radial forearm flap (RFF) transfers Stop (U) ⴙ
Interlabial
Interdental
Apical-alveolars
Apical-palatal
Laminal-palatals
Lingual-velars
PMF RFF P value PMF RFF P value PMF RFF P value PMF RPP P value PMF RFF P value PMF RFF P value
Stop (U) ⴚ
11 19
3 3
Stop (A) ⴙ
Stop (A) ⴚ
11 20
Affricate (U) ⴙ
Affricate (U) ⴚ
3 2
(0.431)
(0.287) 7 16
7 6 (0.152)
2 18
12 4
3 18
11 4
(0.000)
(0.001) 1 13
13 9 (0.002)
7 18
7 4 (0.050)
3 12
11 10
3 12
11 10
(0.051)
(0.051)
U, Unaspiration; A, aspiration; ⫹, correct pronunciation; ⫺, error or distorted pronunciation. A significant difference was found between PMF and RFF groups by using one-tailed Fisher’s exact test only in the production of apical-alveolar and apical-palatal consonants.
Table 5. Swallowing test results according to reconstruction type and primary extent Primary extent Tongue base* Reconstruction
PMF RFF One-tailed t test P value
n
Mean score
1 3
7 5.33 —
Mobile tongue SD
n
— 8 0.58 5
Mean score
5.38 5.40 0.475
Hemiglossectomy† SD
n
0.74 14 0.55 22
Mean score
5.00 5.50 0.061
SD
Total glossectomy* n
0.78 3 1.10 4
Mean score
SD
1 1.25 —
0.00 0.50
PmF, Pectoralis major flap; RFF, radial forearm flap. *The samples were too small to perform a statistic test. †The swallowing score was given for the patients with orocutaneous fistulas only after they were closed via secondary intent or secondary reconstruction.
of pedicled flap versus free flap reconstruction. In that report, only the multiple sites of the oral cavity involvement were given, and neither objective functional analysis nor the tumor size and surgical defect were documented. In our series, the size of the surgical defect determined the consistency of the diet regardless of the reconstructive type that was used; furthermore, the orocutaneous fistulas significantly affected future outcome. McConnel et al11 documented that the tongue provides the major driving force for swallowing liq-
uid. The residual tongue can urge either the free or pedicled flap to approximate the palate and pharyngeal wall. Therefore as more residual tongue is preserved, oral manipulation and swallowing improve. In this study, the patients undergoing total glossectomy can consume only a liquid diet. Patients undergoing hemiglossectomy or partial glossectomy (without complications) can eat regular or semisolid diets. Although bulkiness and contour of the flap are important, the functional amount of the residual tongue plays a more sig-
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Table 4. Continued Affricate (A) ⴙ
Affricate (A) ⴚ
9 18
Nasals ⴙ
Nasals ⴚ
Frictives ⴙ
Frictives ⴚ
5 4 (0.214) 1 18
13 4 (0.000)
3 13
11 9
2 14
7 4
7 18
(0.029) 7 18
12 8 (0.004)
(0.050)
7 4 (0.050)
4 12
10 10 (0.118)
nificant role in swallowing function. It is not known what critical volume of the tongue base is needed to achieve contact with the pharyngeal wall to cause the epiglottis to prolapse over the endolarynx and to generate a driving force on the bolus through the pharynx. In addition, the spontaneously healed orocutaneous fistula may cause shrinkage and inferior displacement of the flap, limiting the final bulkiness and motility of the residual tongue. The tongue base excursion was significantly limited, especially after healing of the fistulas. This study conclusively showed that volume of residual tongue base and absence of tethering from severe scars played a major role in the deglutition. The intrinsic muscles of the tongue are a less well-defined, interlacing network of fiber bundles. These complex sets of muscles provide the tongue with a unique and almost limitless array of voluntary and involuntary movements. With extrinsic muscles these muscles work in a concerted fashion to not only change the position of the tongue within the oral cavity but also alter its shape. In this study, the articulation test demonstrated the significance of this sophisticated work of the tongue. The ingenious contacts between tongue and teeth, alveolar, and palate produce various kinds of stop, affricate, nasal, and fricative conso-
nants. By introducing thin and supple tissue RFF, the residual tongue could maintain its maximum mobility and pliability, which facilitates articulation and improved intelligibility ratings. Several studies12 have demonstrated that lesions in the anterior oral cavity were likely to cause significant problems with speech and tongue motility. Posterior cavity lesions were more likely to result in significant problems with deglutition. In this study, patients with pliable free flap reconstruction had a higher intelligibility rating than those with pedicled flap reconstruction, especially in hemiglossectomy patients, who formed the focus of this study. Even the 4 patients with total glossectomees in the free flap group had better intelligibility than those in the pedicled flap group. However, all patients in the hemiglossectomy group demonstrated various difficulties with velar stop consonants regardless of which flap was used. It might be due to surgical damage to tongue elevators (ie, styloglossus or palatoglossus). The distortion of apical-alveolar and apical-palatal consonants can be detected in the hemiglossectomy group, especially after PMF transfer. The tethering and adynamia of the tongue tip might be the causes. The distortion of apical-palatal consonant is much greater than that of the interdental consonant in PMF groups. It may be because the production of
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418 SU et al
the apical-palatal consonant needs more sophisticated tongue movement and it is a curled consonant. However, the pliability of the RFF provides better assistance for curled consonant production. Therefore, no significant difference can be found between interdental and apical-palatal consonant production with RFF and there was a significant difference between the PMF and RFF groups in the production of apical-alveolar and apical-palatal consonants. Although limited by the small number of subjects, this study showed that the residual tongue has an important function in both anterior and posterior oral cavities and that the motility from flap pliability plays a more important role in speech than in swallowing. The tense-lax distinction between vowel pairs is often used to describe differences in voice quality mainly found in some Germanic languages, particular English, North German, and Dutch (thus, [I:, y:, u:, e:, a:] are characterized as tense and [I, y, u, ε, a] as lax.).13 The terminology tense-lax has also been applied to a vocalic opposition found in a number of Asiatic languages but not in Chinese mandarin according to Shieh.9 Therefore the oral tongue plays a more significant role in English than in Chinese mandarin in this aspect. There is relatively less deterioration of articulation in Chinese mandarin than English after the same surgical intervention, although we do not have the comparative group to prove it. Furthermore, there are no uvula consonants in Chinese mandarin phonemes9 such as can be heard in English phonemes, like /N/, /R/. Since neither reconstructive method can provide much assistance with lingua-velar consonants. English consonants are theoretically more influenced by tongue surgery with styloglossus or palatoglossal fold involvement compared with Chinese mandarin consonants. All of these differences need future study. CONCLUSIONS Most other series were designed to evaluate functional sequelae in various oral cavity cancers with surgical defects involving multiple subsites in the oral cavity. This study was designed primarily to provide a subjective evaluation of the
functional results obtained in patients with various surgical defects solely involving tongue. Our experience with a small number of selected patients showed that the functional outcome of tongue surgery was highly related to the methods of reconstruction especially in speech function and the extent of tongue resection especially in swallowing. We thank statisticians Dr Lu Pai, PhD, and C. C. Lin for the precise calculations and judicious direction. REFERENCES
1. Chan CS. Cancer Registry Annual Report Republic of China. Taipei: Department of Health, The Executive Yuan; 1999. p. 7. 2. Salibian AH, Allison GR, Krugman ME, et al. Reconstruction of the base of the tongue with the microvascular ulnar forearm flap: a functional assessment. Plast Reconstr Surg 1995;96:1081-9. 3. Riley RW, Fee WE, Goffinet D, et al. Squamous carcinoma of the base of the tongue. Otolaryngol Head Neck 1983;91:143-50. 4. Weber RS, Gidley P, Morrison WH. Treatment selection for carcinoma of the base of the tongue. Am J Surg 1990;160:415. 5. Urken ML, Biller HF. A new bilobed design for the sensate radial forearm flap to preserve tongue mobility following significant glossectomy. Arch Otolaryngol Head Neck Surg 1994;120:26-31. 6. Urken ML, Moscoso JF, Lawson W, et al. A systemic approach to functional reconstruction of the oral cavity following partial and total glossectomy. Arch Otolaryngol Head Neck Surg 1994;120:589-601. 7. Soutar DS, McGregor AI. The radial forearm flap in intraoral reconstruction: the experience of 60 consecutive cases. Plast Reconstr Surg 1986;78:1-8. 8. Teichgraeber J, Bowman J, Goepfert H. New test series for the functional evaluation of oral cavity cancer. Head Neck Surg 1985;8:9-20. 9. Shieh KP. Yu Yin Hsueh. In: Shieh KP, editor. Yu Yen Hsueh Kai Lun. 2nd ed. Taipei: San Min Shu Chu; 2000. p. 53-91.[In Chinese] 10. Freedlander E, Espie CA., Campsie LM, et al. Functional implications of major surgery for intraoral cancer. Br J Plast Surg 1989;42:266-9. 11. McConnel FMS, Cerenko D, Mendelsohn M. Manofluorographic analysis of swallowing. Otolaryngol Clin North Am 1988;21:625-35. 12. Hufnagle J, Pullon P, Hufnagle K. Speech considerations in oral surgery: speech characteristics of patients following surgery for oral malignancy. Oral Surg 1978;46:35461. 13. Jørgensen EF. Intrinsic Fo in tense and lax special reference to German. Phonetica 1990;47:99-140.
MD,
YI-JAN HSIA,
DDS, MDSC,
YEN-CHINE CHANG,
DDS, MDSC,
SHYI-GEN CHEN,
MD,
and HWA SHENG,
PhD,
Taipei,
Taiwan OBJECTIVE: Numerous patients in Taiwan with tongue carcinoma require tongue reconstruction. We compared the abilities of 2 methods of tongue reconstruction to reserve tongue function. STUDY DESIGN AND SETTING: Sixty patients underwent resection of the tumors and reconstruction with a pectoralis major flap or a radial forearm flap. The Chinese articulation test was used to evaluate the place and manner of error production, and a questionnaire on dietary habits was used to evaluate deglutition 6 months to 10 years after reconstruction. RESULTS: Patients with the free flap had more intelligible speech. The questionnaire study showed no significant difference between the 2 groups in swallowing rating. Motility caused by flap pliability increased speech intelligibility more than it did on swallowing function. CONCLUSION: Our experience in a few selected patients shows that the functional outcome of tongue surgery is related to the reconstruction methods used (for speech) and to the extent of tongue resection (for swallowing). (Otolaryngol Head Neck Surg 2003;128:412-8.)
C arcinoma of the tongue is the most common cancer of the oral cavity in Taiwan. The Cancer Registry Annual Report of the Republic of China reported in 1999 that nearly 27 patients per million population in Taiwan develop carcinoma of the From the Departments of Otolaryngology–Head and Neck Surgery (Dr Su), Oral and Maxillofacial Surgery (Drs Hsia and Chang), and Plastic Surgery (Dr Chen), Tri-Service General Hospital, National Defense Medical Center; and the Department of Speech and Hearing Disorder and Science, National Taipei College of Nursing (Ms Sheng). Reprint requests: Wan-Fu Su, MD, Department of Otolaryngology-Head and Neck Surgery, Tri-Service General Hospital, 325, Sec 2, Chen-Kung Road, Taipei, Taiwan 114; e-mail, [email protected]. Copyright © 2003 by the American Academy of Otolaryngology–Head and Neck Surgery Foundation, Inc. 0194-5998/2003/$30.00 ⫹ 0 doi:10.1067/mhn.2003.38 412
tongue each year.1 Treatment strategy consists of radiation therapy alone, surgery alone, or combined surgery and radiotherapy depending on the size of the tumor, the extent of tumor infiltration, and the physician’s preference.2-4 The range of the surgical options available for reconstruction for the patient with cancer of the oral cavity has changed markedly during the past decade. For example, in 1994, Urken and Biller5 designed a bilobed sensate radial forearm flap (RFF) to preserve tongue motility. Although the management of segmental defects of the mandible has been the focus of much attention during the past several decades, it is the soft tissue reconstruction of the oral cavity and, in particular, the tongue that is the most critical factor in achieving a successfully functional result. The tongue uniquely serves a multitude of varied functions, including articulation, mastication, deglutition, and taste. There have been a number of recent reports6,7 that have attempted to define a battery of functional tests for assessment of the rehabilitative outcome after surgery in the patient with cancer of the oral cavity. After reconstructive surgery, the tongue should be evaluated as a single organ even though it serves different functions and may have been reconstructed with different methods and with resulting surgical defects of different sizes. Although the mobile tongue and tongue base serve different purposes in deglutition and speech, they coordinate with each other, especially after surgery. Therefore they should be evaluated together. We report on 60 patients with carcinoma of the tongue base or mobile tongue who underwent 25% to 100% full-thickness resection, and we compare the functional results between the pectoralis major flap (PMF) and RFF reconstructions. The patients were evaluated clinically for speech and swallowing function to determine the flap best suited to restoring speech and swallowing. Particular em-
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Table 1. Patient profile Reconstruction type
Tongue base (n)
Mobile tongue (n)
Hemiglossectomy (n)*
Total glossectomy (n)
Total
Pectoralis major flap Radial forearm flap
1 3
8 5
14 22
3 4
26 34
*Hemiglossectomy indicates surgical defect involving both the base and mobile portions of the tongue.
phasis is placed on the restoration of articulation after RFF transfer.
tent disease or died from concurrent disease and were excluded from this study.
PATIENTS AND METHODS Between July 1988 and July 1999, 76 consecutive patients (61 men and 15 women) with cancer of the tongue underwent resection of the tongue and reconstruction using a PMF, free RFF transfer, or primary closure. None underwent segmental mandibulectomy. Patients were assigned to one procedure or the other on the basis of the size of the defect and physician’s preference. Seventeen patients required a marginal resection of the mandible, which did not influence the continuity, and 60 patients underwent a median or paramedian mandibulotomy for exposure. None of the patients required a laryngectomy for tumor invasion. Partial laryngoplasty was performed in all 7 patients undergoing total glossectomy. A concomitant neck dissection was carried out in every patient undergoing flap reconstruction. Seventy-two patients were previously untreated, and 4 patients with recurrent tumor received combined therapy (radiotherapy, chemotherapy, or partial glossectomy). Sixty selected patients were evaluated for swallowing and speech functions 6 months to 10 years after PMF reconstruction or the radial forearm free flap. Twenty-six pedicled flaps and 34 free flaps were used to reconstruct tongue defects of varying sizes (Table 1). Pectoralis major flaps were used in 3 patients undergoing total glossectomy, 14 patients undergoing hemiglossectomy (both the tongue base and mobile tongue), and 9 patients undergoing partial glossectomy (tongue base in 1 and mobile tongue in 8). Free flaps were used in 4 patients undergoing total glossectomy, 22 patients undergoing hemiglossectomy, and 8 patients undergoing partial glossectomy (tongue base in 3 and mobile tongue in 5). The remainder of the 16 patients repaired by primary closure had a persis-
Surgical Technique Ablative procedure. Small resections of mo-
bile tongue (classified as “one-quarter glossectomy” in Urken’s classification scheme)6 may be primarily closed. However when the defect extends to the floor of mouth, then primary closure leads to tethering of the tongue. Since the splitthickness skin is unreliable, we prefer the use of a forearm flap or a PMF to provide bulk of the tongue, as well as epithelial coverage for the oral cavity. In this study, when both tongue base and mobile tongue were involved, resection was classified as hemiglossectomy, unless the defect was smaller than 3 cm and primarily could be closed without significant disturbance in function. We thought that defects of the tongue base are hard to manage by tongue flap reconstruction and led to great disturbances in tongue shape, volume, position, mobility, and, ultimately, function. For patients undergoing reconstruction of the entire tongue or who were left with a nonfunctional residual remnant, the tongue base was always resected down to the hyoid bone, including the hypoglossal nerve and lingual artery, as well as varying portions of the vallecula and pharyngeal wall. Partial laryngoplasty was done to ensure protection against aspiration. Reconstructive procedure. Our surgeons first tended to use the PMF because of its simplicity in design, ease of dissection, and high reliability, especially when bulk is beneficial, such as after subtotal or total glossectomy. Preference for this method was challenged by an increase in the use of microsurgical transfer of a free RFF for intraoral reconstruction. The RFF and its use in intraoral reconstruction have been described in many reports.5,7 In this study there was no attempt to restore neurologic function.
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Table 2. Comparison between Chinese consonant phonemes and phonemes of the international phonetic alphabet Stop
Affricate
Place/manner
U
Interlabial Interdental Apical-alveolars Apical-palatals Laminal-palatals Lingua-velars
p
ph
t
h
g
A
U
A
ts
tsh
ts tc¸
tsh tc¸ h
t
k
Nasals
Fricatives
n z c¸ h
s
Apical, tongue tip; laminal, dorsal surface of tongue; U, Unaspiration; A, aspiration.
Clinical evaluation of deglutition included a questionnaire on dietary habits and a swallowing rating of 1 to 7,8 in which swallowing ability was rated 7 to indicate no complaints; 6, minimal complaints and totally able to swallow a bolus without difficulty; 5, minimal complaints and totally able to swallow without a bolus (dry swallowing) without difficulty; 4, moderate complaints and difficulty swallowing a bolus; 3, moderate complaints and difficulty dry swallowing; 2, severe complaints and difficulty swallowing a bolus and dry swallowing; and 1, severe complaints and unable to swallow. Food consistency between the Chinese diet and Western diet is somewhat different. Thus, the Chinese diet is classified into liquid, semisolid (noodle), and solid food (rice). One experienced speech pathologist, one head and neck surgeon, and patients’ spouses performed a perceptual analysis of the patients’ speech. The evaluated functions included speech intelligibility and Chinese articulation. Intelligibility was determined by the evaluation of the speech pathologist who reviewed and graded a tape of the patient’s speech on a scale of 1 to 7 and by the spouse who interviewed the patient. Intelligibility was rated as 7 to indicate no sound errors are noticed in continuous speech and speech can be understood by spouse easily; 6, sound errors are occasionally noticed in continuous speech and spouse understands every time; 5, speech is intelligible, although noticeably in error, and spouse understands only after listening twice; 4, speech is intelligible with careful listening and spouse understands after listening more than 3 times; 3, speech intelligibility is difficult and the spouse understands after listening more than 3
times and from body language; 2, speech is usually unintelligible and spouse communicates only by body language and guessing; and 1, speech is unintelligible and spouse cannot understand. Chinese consonant phonemes9 (Table 2), compared with phonemes of IPA (international phonetic alphabet), were used to test patients’ articulation because the consonants are the carrier of intelligibility. Each patient’s articulation test score is correlated with the intelligibility scores. The articulation test divides speech errors into 3 types: manner, place, and vocal production. Statistical significance of difference between the 2 groups was determined by using the Student’s t test and Fisher’s exact test. RESULTS Complications consisted of orocutaneous fistulas in 15 patients (8 with pedicled flap and 7 with free flap), infections in 6 patients, and flap skin losses in 13 patients. The fistulas healed with local wound care in 12 patients, and closure with PMF was performed in 3 patients. Eleven patients died from persistent diseases. Donor-site complications included loss of the entire forearm skin flap due to infection in 3 patients who required a second skingrafting procedure. Speech After hemiglossectomy, the main subject of this study, and then PMF transfer, the intelligibility rating fell to category 6 in 1 patient, 5 in 3 patients, 4 in 8 patients, and 3 in 2 patients (Table 3). The average score reached 4.21. After total glossectomy, the PMF transfer did not restore the speech of any patient, with an average score of
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Table 3. Intelligibility and articulation test results according to reconstructive type and primary extent of surgery Primary extent Tongue base* Reconstruction
PMF RFF One-tailed t-test P value
n
Mean score
1 3
6 6.67 —
Mobile tongue SD
n
— 8 0.58 5
Mean score
4.88 5.80 0.087
Hemiglossectomy SD
n
1.25 14 0.84 22
Mean score
4.21 6.23 0.000
SD
Total glossectomy* n
0.80 3 0.81 4
Mean score
SD
1.33 2.75 —
0.58 0.50
PMF, Pectoralis major flap; RFF, radial forearm flap. *The samples were too small to perform a statistical test.
1.33. In those patients receiving RFF transfer, the intelligibility rating fell to 7 in 9 patients, 6 in 10 patients, 5 in 2 patients, and 4 in 1 patient after hemiglossectomy; the average score was 6.23, which was significantly better than the score of 4.21 for PMF transfers (P ⫽ 0.000). Even after total glossectomy, patients receiving RFF transfer were more understandable (category 2 for 1 patient and category 3 for 3 patients) than those receiving PMF transfer. Table 4 indicates that after PMF transfer, patients developed obvious handicaps in the production of apical-alveolar stop, apical-palatal, and lingua-velar consonants. Compared with PMF transfer, all of the parameters in Table 4 were better in RFF transfer recipients, especially in the production of apical-alveolar and apical-palatal consonants, with significant difference. Neither transfer was very successful in restoring lingua-velar contact. The consonants g, k and h were perceived as distorted but intelligible. The distortion of apical-palatal consonant is much more than that of the interdental consonant in PMF groups (P ⫽ 0.016 for nonaspirated affricate and P ⫽ 0.027 for aspirated affricate). Bilabial consonants were less affected by the surgical intervention in both groups because those neck dissections had not injure the marginal branch of facial nerve, except for 3 patients in the PMF group and 2 patients in the RFF group. Swallowing In patients with total glossectomy, liquid diet was the only choice regardless of the flap that was
used (Table 5). In patients with hemiglossectomy, PMF transfer helped 4 patients to eat a regular diet (grade 6), 6 patients to eat a semisolid diet (grade 5), and 4 patients to eat a semiliquid diet with difficulty (grade 4). The average swallowing rating fell to 5.0 only because 5 patients had orocutaneous fistulas, which affected their swallowing ability (grade 4). One of them (secondary reconstruction), whose preoperative diet was limited to liquids, was able to eat noodles after surgery (grade 5). In patients undergoing hemiglossectomy, RFF helped 7 patients to eat regular diets (grade 6), 12 patients to eat a semisolid diet (grade 5), and 3 patients to eat a semiliquid diet with moderate complaint (grade 4). The average swallowing rating fell to 5.43 because of 4 patients with orocutaneous fistulas (grade 4). One of them was able to eat a semisolid diet after secondary reconstruction (grade 5). There was no significant difference between 2 reconstructive methods (P ⫽ 0.061). In the other patients undergoing partial glossectomy, regardless of the flap that was used, they were able to eat regular or semisolid diets only if no complications occurred. DISCUSSION The oral tongue is responsible for oral manipulation of food for the swallow, and the basal tongue is responsible for the oral initiation of the swallow. Thus every effort should be made to reconstruct the oral cavity to permit as much range and coordination of tongue motion as possible. In assessing 12 patients with cancer of the tongue, Freelander et al10 found no differences as far as patients were concerned in the functional outcome
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Table 4. Articulation test results of hemiglossectomy patients after pectoralis major flap (PMF) and radial forearm flap (RFF) transfers Stop (U) ⴙ
Interlabial
Interdental
Apical-alveolars
Apical-palatal
Laminal-palatals
Lingual-velars
PMF RFF P value PMF RFF P value PMF RFF P value PMF RPP P value PMF RFF P value PMF RFF P value
Stop (U) ⴚ
11 19
3 3
Stop (A) ⴙ
Stop (A) ⴚ
11 20
Affricate (U) ⴙ
Affricate (U) ⴚ
3 2
(0.431)
(0.287) 7 16
7 6 (0.152)
2 18
12 4
3 18
11 4
(0.000)
(0.001) 1 13
13 9 (0.002)
7 18
7 4 (0.050)
3 12
11 10
3 12
11 10
(0.051)
(0.051)
U, Unaspiration; A, aspiration; ⫹, correct pronunciation; ⫺, error or distorted pronunciation. A significant difference was found between PMF and RFF groups by using one-tailed Fisher’s exact test only in the production of apical-alveolar and apical-palatal consonants.
Table 5. Swallowing test results according to reconstruction type and primary extent Primary extent Tongue base* Reconstruction
PMF RFF One-tailed t test P value
n
Mean score
1 3
7 5.33 —
Mobile tongue SD
n
— 8 0.58 5
Mean score
5.38 5.40 0.475
Hemiglossectomy† SD
n
0.74 14 0.55 22
Mean score
5.00 5.50 0.061
SD
Total glossectomy* n
0.78 3 1.10 4
Mean score
SD
1 1.25 —
0.00 0.50
PmF, Pectoralis major flap; RFF, radial forearm flap. *The samples were too small to perform a statistic test. †The swallowing score was given for the patients with orocutaneous fistulas only after they were closed via secondary intent or secondary reconstruction.
of pedicled flap versus free flap reconstruction. In that report, only the multiple sites of the oral cavity involvement were given, and neither objective functional analysis nor the tumor size and surgical defect were documented. In our series, the size of the surgical defect determined the consistency of the diet regardless of the reconstructive type that was used; furthermore, the orocutaneous fistulas significantly affected future outcome. McConnel et al11 documented that the tongue provides the major driving force for swallowing liq-
uid. The residual tongue can urge either the free or pedicled flap to approximate the palate and pharyngeal wall. Therefore as more residual tongue is preserved, oral manipulation and swallowing improve. In this study, the patients undergoing total glossectomy can consume only a liquid diet. Patients undergoing hemiglossectomy or partial glossectomy (without complications) can eat regular or semisolid diets. Although bulkiness and contour of the flap are important, the functional amount of the residual tongue plays a more sig-
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Table 4. Continued Affricate (A) ⴙ
Affricate (A) ⴚ
9 18
Nasals ⴙ
Nasals ⴚ
Frictives ⴙ
Frictives ⴚ
5 4 (0.214) 1 18
13 4 (0.000)
3 13
11 9
2 14
7 4
7 18
(0.029) 7 18
12 8 (0.004)
(0.050)
7 4 (0.050)
4 12
10 10 (0.118)
nificant role in swallowing function. It is not known what critical volume of the tongue base is needed to achieve contact with the pharyngeal wall to cause the epiglottis to prolapse over the endolarynx and to generate a driving force on the bolus through the pharynx. In addition, the spontaneously healed orocutaneous fistula may cause shrinkage and inferior displacement of the flap, limiting the final bulkiness and motility of the residual tongue. The tongue base excursion was significantly limited, especially after healing of the fistulas. This study conclusively showed that volume of residual tongue base and absence of tethering from severe scars played a major role in the deglutition. The intrinsic muscles of the tongue are a less well-defined, interlacing network of fiber bundles. These complex sets of muscles provide the tongue with a unique and almost limitless array of voluntary and involuntary movements. With extrinsic muscles these muscles work in a concerted fashion to not only change the position of the tongue within the oral cavity but also alter its shape. In this study, the articulation test demonstrated the significance of this sophisticated work of the tongue. The ingenious contacts between tongue and teeth, alveolar, and palate produce various kinds of stop, affricate, nasal, and fricative conso-
nants. By introducing thin and supple tissue RFF, the residual tongue could maintain its maximum mobility and pliability, which facilitates articulation and improved intelligibility ratings. Several studies12 have demonstrated that lesions in the anterior oral cavity were likely to cause significant problems with speech and tongue motility. Posterior cavity lesions were more likely to result in significant problems with deglutition. In this study, patients with pliable free flap reconstruction had a higher intelligibility rating than those with pedicled flap reconstruction, especially in hemiglossectomy patients, who formed the focus of this study. Even the 4 patients with total glossectomees in the free flap group had better intelligibility than those in the pedicled flap group. However, all patients in the hemiglossectomy group demonstrated various difficulties with velar stop consonants regardless of which flap was used. It might be due to surgical damage to tongue elevators (ie, styloglossus or palatoglossus). The distortion of apical-alveolar and apical-palatal consonants can be detected in the hemiglossectomy group, especially after PMF transfer. The tethering and adynamia of the tongue tip might be the causes. The distortion of apical-palatal consonant is much greater than that of the interdental consonant in PMF groups. It may be because the production of
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the apical-palatal consonant needs more sophisticated tongue movement and it is a curled consonant. However, the pliability of the RFF provides better assistance for curled consonant production. Therefore, no significant difference can be found between interdental and apical-palatal consonant production with RFF and there was a significant difference between the PMF and RFF groups in the production of apical-alveolar and apical-palatal consonants. Although limited by the small number of subjects, this study showed that the residual tongue has an important function in both anterior and posterior oral cavities and that the motility from flap pliability plays a more important role in speech than in swallowing. The tense-lax distinction between vowel pairs is often used to describe differences in voice quality mainly found in some Germanic languages, particular English, North German, and Dutch (thus, [I:, y:, u:, e:, a:] are characterized as tense and [I, y, u, ε, a] as lax.).13 The terminology tense-lax has also been applied to a vocalic opposition found in a number of Asiatic languages but not in Chinese mandarin according to Shieh.9 Therefore the oral tongue plays a more significant role in English than in Chinese mandarin in this aspect. There is relatively less deterioration of articulation in Chinese mandarin than English after the same surgical intervention, although we do not have the comparative group to prove it. Furthermore, there are no uvula consonants in Chinese mandarin phonemes9 such as can be heard in English phonemes, like /N/, /R/. Since neither reconstructive method can provide much assistance with lingua-velar consonants. English consonants are theoretically more influenced by tongue surgery with styloglossus or palatoglossal fold involvement compared with Chinese mandarin consonants. All of these differences need future study. CONCLUSIONS Most other series were designed to evaluate functional sequelae in various oral cavity cancers with surgical defects involving multiple subsites in the oral cavity. This study was designed primarily to provide a subjective evaluation of the
functional results obtained in patients with various surgical defects solely involving tongue. Our experience with a small number of selected patients showed that the functional outcome of tongue surgery was highly related to the methods of reconstruction especially in speech function and the extent of tongue resection especially in swallowing. We thank statisticians Dr Lu Pai, PhD, and C. C. Lin for the precise calculations and judicious direction. REFERENCES
1. Chan CS. Cancer Registry Annual Report Republic of China. Taipei: Department of Health, The Executive Yuan; 1999. p. 7. 2. Salibian AH, Allison GR, Krugman ME, et al. Reconstruction of the base of the tongue with the microvascular ulnar forearm flap: a functional assessment. Plast Reconstr Surg 1995;96:1081-9. 3. Riley RW, Fee WE, Goffinet D, et al. Squamous carcinoma of the base of the tongue. Otolaryngol Head Neck 1983;91:143-50. 4. Weber RS, Gidley P, Morrison WH. Treatment selection for carcinoma of the base of the tongue. Am J Surg 1990;160:415. 5. Urken ML, Biller HF. A new bilobed design for the sensate radial forearm flap to preserve tongue mobility following significant glossectomy. Arch Otolaryngol Head Neck Surg 1994;120:26-31. 6. Urken ML, Moscoso JF, Lawson W, et al. A systemic approach to functional reconstruction of the oral cavity following partial and total glossectomy. Arch Otolaryngol Head Neck Surg 1994;120:589-601. 7. Soutar DS, McGregor AI. The radial forearm flap in intraoral reconstruction: the experience of 60 consecutive cases. Plast Reconstr Surg 1986;78:1-8. 8. Teichgraeber J, Bowman J, Goepfert H. New test series for the functional evaluation of oral cavity cancer. Head Neck Surg 1985;8:9-20. 9. Shieh KP. Yu Yin Hsueh. In: Shieh KP, editor. Yu Yen Hsueh Kai Lun. 2nd ed. Taipei: San Min Shu Chu; 2000. p. 53-91.[In Chinese] 10. Freedlander E, Espie CA., Campsie LM, et al. Functional implications of major surgery for intraoral cancer. Br J Plast Surg 1989;42:266-9. 11. McConnel FMS, Cerenko D, Mendelsohn M. Manofluorographic analysis of swallowing. Otolaryngol Clin North Am 1988;21:625-35. 12. Hufnagle J, Pullon P, Hufnagle K. Speech considerations in oral surgery: speech characteristics of patients following surgery for oral malignancy. Oral Surg 1978;46:35461. 13. Jørgensen EF. Intrinsic Fo in tense and lax special reference to German. Phonetica 1990;47:99-140.