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myocutaneous flaps—a multicenter study
Int. J. Oral Maxillofac. Surg. 2007; 36: 601–609 doi:10.1016/j.ijom.2007.01.014, available online at http://www.sciencedirect.com
Clinical Paper Head & Neck Oncology
Factors influencing postoperative speech function of tongue cancer patients following reconstruction with fasciocutaneous/myocutaneous flaps—a multicenter study
Y. Matsui1,2, K. Ohno2, Y. Yamashita3, K. Takahashi3 1 Department of Oral and Maxillofacial Surgery, Graduate School of Medicine, Yokohama City University, Yokohama 2360004, Japan; 2Department of Oral and Maxillofacial Surgery, School of Dentistry, Showa University, Tokyo 145-8515, Japan; 3 Department of Oral Rehabilitation, Showa Dental Hospital, Showa University, Tokyo 1458515, Japan
Y. Matsui, K. Ohno, Y. Yamashita, K. Takahashi: Factors influencing postoperative speech function of tongue cancer patients following reconstruction with fasciocutaneous/myocutaneous flaps—a multicenter study. Int. J. Oral Maxillofac. Surg. 2007; 36: 601–609. # 2007 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved. Abstract. This study investigated postoperative speech function in tongue cancer patients following reconstruction with fasciocutaneous/myocutaneous flaps, to clarify the factor(s) influencing outcome. Eighty-one patients, enrolled from 11 Japanese institutions, were classified into three groups by the site of resection: lateral (N = 51), anterior (N = 17) and combined (N = 13). The lateral group was divided into three subgroups and the anterior group into two subgroups by the size of resection. Mandibulectomy had been performed in 43 patients and radiation therapy in 24 patients. Reconstruction was accomplished by radial forearm flap (N = 50), rectus abdominis myocutaneous flap (N = 18), pectoralis major myocutaneous flap (N = 11), latissimus dorsi myocutaneous flap (N = 1) or scapula flap (N = 1). Speech function was evaluated with two objective tests and three self-reporting questionnaires. The influence of tongue mobility, age at operation and examination, time interval to examination, and type of flap reconstruction on the functional results was also investigated. Better results were obtained with lateral type resections, smaller excisions, greater tongue mobility, younger patients and longer interval to examination. Mandibulectomy and radiation therapy were negative factors. Type of flap reconstruction had no effect on functional outcome. A treatment method with less functional interference should be developed, particularly for patients anticipated to be in poor functional state postoperatively.
0901-5027/070601 + 09 $30.00/0
Key words: speech function; reconstruction; tumour surgery; tongue. Accepted for publication 10 January 2007 Available online 23 March 2007
# 2007 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
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Surgical ablation of tongue cancer often causes severe postoperative speech impairment because the tongue is a primary active articulator. While recent progress in reconstructive surgery offers new therapeutic options suitable for the complex anatomy and function of the tongue, the numerous studies that have evaluated postoperative speech function subjectively and objectively1,3,4,5,8,9,12 often involved a wide range of resected sites in a limited number of patients. Few studies have assessed in detail the factors influencing functional outcome of speech with a large number of subjects. The present multicenter study investigated postoperative speech function of tongue cancer patients following reconstruction with fasciocutaneous/myocutaneous flaps so as to clarify the influencing factor(s).
Patients and methods Subjects
From 232 patients who had undergone reconstruction with fasciocutaneous/ myocutaneous flaps after ablative surgery at 11 Japanese institutions, a total of 81 patients (28 women and 53 men; mean age at examination, 59.1 years; range, 23–82 years) with proven malignant tumour of the tongue and/or floor of the mouth were enrolled in the study. Reconstruction with a flap was one of the criteria for selection. General information about the participants was collected by the responsible surgeon under a standard protocol including several surgical variables: age, T stage, extent of resection, radiotherapy and type of flap reconstruction. Staging was T1 in 5 patients, T2 in 44, T3 in 21 and T4 in 11.
Fig. 1. Classification of area reconstructed with flaps.
Site and size of resection
Subjects were classified into three main anatomical groups according to the resected site: lateral (N = 51), anterior (N = 17) and combined (N = 13). The lateral group was further divided into three subgroups according to the size of resection: partial excisions of the anterior two thirds of the lateral border of the tongue (group L1; N = 10), half resections of the anterior two thirds of the lateral border of the tongue (group L2; N = 24) and complete hemiglossectomies (group L3; N = 17). All patients in the lateral subgroups underwent resection of the floor of the mouth to some extent, but this never exceeded the midline. The anterior group all had some excision of the bilateral floor of the mouth with resection of the tongue, and this group was subdivided into two
Factors influencing postoperative speech function Table 1. Number of patients Group L1
L2
L3
A1
A2
C
Total
Total Radiation therapy
10 2
24 9
17 2
6 2
11 4
13 5
81 24
Mandibulectomy Marginal Segmental
5 0
6 2
10 1
4 1
4 3
6 1
35 8
according to depth of resection: resection of anterior floor of the mouth not deeper than one-third full thickness of the midline up to the mylohyoid muscle plane (group A1; N = 6) and resection of anterior floor of the mouth deeper than one-third and up to two-thirds full thickness of the midline (group A2; N = 11). Subjects who underwent subtotal hemiglossectomy and/or resection of the anterior floor of the mouth deeper than two-thirds full thickness of the midline were categorized as the combined group (group C; N = 13) (Fig. 1 and Table 1). None of the 81 patients had undergone resection of the soft palate or tonsillar region. Radiotherapy
A total of 24 patients had received radiotherapy; 15 preoperatively and 9 postoperatively. Irradiated dose ranged from 18 to 90 Gy (Table 1). Neither age, time interval, resected site nor incidence of mandibulectomy differed significantly between non-irradiated and irradiated patients (x2 test). Mandibulectomy
Mandibulectomy had been performed in 43 patients; marginal in 35 and segmental in 8 (Table 1). There was no significant difference between the two types of mandibulectomy in terms of age, time interval, site and size of resection, or incidence of radiotherapy. After segmental osteotomy, the mandible had been reconstructed with a titanium plate at the ablative surgery in all patients except one, who underwent simultaneous reconstruction with a scapula flap. Three of seven subsequently underwent mandibular reconstruction using bone harvested from the ilium. Type of flap reconstruction
In group L1, all patients except one underwent reconstruction with a free radial forearm flap (RFF). In the remaining patient, a vascularized pectoralis major myocutaneous flap (PMMCF) was used. In group L2, the most popular flap type
was the RFF, but some patients underwent reconstruction with a free rectus abdominis myocutaneous flap (RAMCF). In group L3, reconstruction involved an RFF in nine patients, a PMMCF in five and an RAMCF in three. In group A1, reconstruction involved an RFF in four patients, a PMMCF in one and a RAMCF in one. In group A2, surgeons used an RFF in six patients, an RAMCF in three and a PMMCF in two. In group C, flaps used were an RAMCF in seven patients, an RFF in five and a PMMCF in one. Methods for evaluation
Two objective tests and three self-assessment questionnaires were performed for functional evaluation. The speech intelligibility test (SIT) and conversational understandability test (CUT) were used for objective evaluation of speech function. The SIT was conducted in Japanese. Each subject was instructed to pronounce 100 syllables listed, and pronunciation was recorded. Ten untrained volunteers with normal hearing, who did not know the patient, then listened to the tape and transcribed the sounds as Japanese syllables that they believed they had heard. The intelligibility score was expressed as the percentage of correct responses7. In the CUT, an audio recording of a 5-min conversation with an interviewer was evaluated by a group of five untrained volunteers with normal hearing for conversational understandability using a 5point scale: 5, all speech is understood; 4, sometimes not understood; 3, can be understood when conversational content is already known; 2, sometimes understood and 1, nothing is understood15. For each objective test, the mean score was calculated for each patient and used in subsequent analysis. Self-assessment of speech function was performed using three selfreporting questionnaires relating to three situations involving functional spoken communication: with families, on the telephone and when first meeting someone (at first contact). Responses to each questionnaire were scored on the same 5-point scale. These questionnaires were mailed
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with instructions to the subjects, who returned the responses directly to the authors. Time interval between surgical treatment and completion of the selfreporting questionnaires ranged from 5 to 201 months (mean 35.9 29.0 months, mode 44 months, median 26 months). On the same occasion as the objective and subjective functional tests, the tongue mobility test was performed by observing protrusion or elevation of the tip and dorsum. Each movement was evaluated using a 3-point scale. For protrusion: 2, tongue tip can contact the lip; 1, can contact the dental arch; 0, only remains inside the dental arch. For elevation of the tip and dorsum: 2, tongue tip can contact the palate; 1, can elevate, but not contact the palate; 0, cannot elevate. The sum of the scores for the three motions was then calculated. Correlations between tongue mobility and both objective and subjective results were analyzed to evaluate the accuracy and clinical values of these assessments. It was also investigated whether other factors, i.e. mandibulectomy, radiation therapy including a comparison between pre- and postoperative irradiation, age at operation and examination, time interval between operation and examination, and type of flap reconstruction, influenced the objective functional results. Speech therapy intervention, which might have been available in some institutions, was not included in the investigated factors because relevant information could not be obtained. Statistical analyses
Statistical analyses were performed using Stat View 5.0 J software (SAS Institute Inc., USA). An independent samples t-test was used for comparing the objective and subjective results in each pair of subgroups with regard to site and size of resection, mandibulectomy, and radiotherapy (for pre- and postoperative irradiation). Sample coefficient correlation (CC) was used to examine the relationship between tongue mobility and both objective and subjective results. The effect of age at operation and examination, and that of time interval on the objective results were also investigated with CC. The influence of type of flap reconstruction was analyzed by a Mann– Whitney U-test as follows: in subgroup L2, RFF versus RAMCF; in subgroup L3, RFF versus PMMC, RFF versus RAMCF and PMMC versus RAMCF; in subgroup A2, RFF versus RAMCF and in group C, RFF versus RAMCF. A P-value less than 0.05 was considered significant.
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Matsui et al. Table 2.1. Results of self-assessment (communication with families) Score
L1
L2
L3
A1
A2
C
1 2 3 4 5
0 0 2 5 3
0 1 10 5 8
0 0 6 7 4
0 1 3 1 1
0 0 5 4 2
0 0 8 3 2
groups. Group C scored lowest. The difference between the L subgroups and A subgroups had widened, with almost all subgroups showing a significant difference in scores (Fig. 3). Subjective assessment with questionnaires
Fig. 2. Results of speech intelligibility test (SIT). Better functional outcome was obtained for lateral type and smaller excisions. Group C had the lowest values, and differed significantly from all lateral group values.
Results Objective evaluation with SIT and CUT
In the SIT, group L1 scored highest (mean 1SD: 75.3 8.6) and group C lowest (41.5 20.2). Lateral subgroups scored higher than A subgroups and group
C. Wider resection resulted in a lower intelligibility score within the L and A groups. Group C, the lowest scoring group, showed a significant difference when compared to all lateral subgroups (Fig. 2). Similarly, in the CUT, L subgroups scored higher than the A and C
With regard to self-reported speech function, almost all patients scored more than 3 on the questionnaire concerning communication with families. There was no statistical difference between any groups, although more patients had higher scores in the L subgroups compared to the A subgroups and group C (Table 2.1). In all groups, some patients scored themselves as less than 2 for communication on the telephone and at first contact. The difference between the L subgroups and other two groups had increased, with a significant difference seen for group C patients and all L subgroups for both communication on the telephone and at first contact (Tables 2.2 and 2.3). Tongue mobility test
Group L1 scored highest on each tongue mobility test. No subject in that group scored 0 in any of the movements. Lateral subgroups scored higher than A subgroups and the C group. Statistically significant differences were found for almost all sets between L and A subgroups and between L and C groups, except with respect to dorsum elevation (Tables 3.1–3.4). CCs between objective results and subjective assessment
All CCs between objective results and subjective assessments were statistically significant (P < 0.01). ‘First contact’ scored highest: 0.65 with SIT and 0.51 with CUT, and ‘families’ scored lowest: 0.53 with SIT and 0.46 with CUT.
Fig. 3. Results of conversational understandability test (CUT). Lower scores indicate better function on CUT. Scores differed significantly between almost all L groups and group C and both A subgroups.
CCs between tongue mobility test and functional results
Each category of tongue mobility test had statistically significant CCs with all
Factors influencing postoperative speech function Table 2.2. Results of self-assessment (communication on the telephone)
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objective and subjective results. Total score and tip elevation showed particularly high CCs (Table 4). Effect of other factors on the functional results
Radiation therapy (Table 5)
Table 2.3. Results of self-assessment (communication at first contact)
The irradiated group had poorer subjective and objective evaluation scores than the non-irradiated group for all measurements: mean scores 1SD for the respective non-irradiated and irradiated groups were 3.89 0.82 and 3.5 0.86 for communication with families, 3.62 0.89 and 3.04 1.22 for on the telephone, 3.63 0.94 and 3.12 1.03 for at first contact, 66.0 18.6 and 52.5 24.9 in the SIT and 1.57 0.83 and 1.93 1.06 in the CUT. Subdivision of the irradiated group into pre- and post-irradiated groups showed no differences in terms of functional speech results. Mandibulectomy (Table 6)
For all self-assessment categories and the SIT, the non-resection group scored highest and the segmental group lowest. Mean scores 1SD of the respective non-resection, marginal and segmental groups were 4.04 0.77, 3.6 0.85 and 3.14 0.9 for communication with families; 3.79 0.83, 3.26 0.98 and 2.57 1.27 for on the telephone; 3.79 0.89, 3.2 0.96 and 3 1.15 for at first contact and 66.3 21.5, 59.2 21.8 and 53.4 17.3 in the SIT. The segmental group also had the lowest CUT value: mean score 1SD was 1.61 0.93 in the non-resection group, 1.6 0.84 in the marginal group and 2.31 0.89 in the segmental group. Table 3.1. Results of tongue mobility (protrusion)
Age and time intervals
Older patients at the time of operation and at the time of examination had significantly lower quality postoperative speech: CC was 0.31 in the SIT and 0.34 in the CUT for age at operation, and 0.25 in the SIT and 0.29 in the CUT for age at examination. Longer time interval between operation and examination was associated with better postoperative CUT results; the logarithmic regression curve gradually plateaued with increasing interval (data not shown). The effect on SIT results was unclear (P = 0.20) (Table 7). Type of flap
The RFF exhibited a better objective score than the RAMCF in all subgroups. There
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Table 3.2. Results of tongue mobility (tip elevation)
Table 3.3. Results of tongue mobility (dorsum elevation)
were no significant differences in type of flap reconstruction within individual subgroups (Table 8). Discussion
In the present study, the subjects were divided into three groups by the site of resection (groups L, A and C). The L and A groups were further divided into three and two subgroups, respectively, to investigate in detail the influence of site and size of resection and type of flap reconstruction on speech function. Certain previous reports that investigated postoperative speech function of tongue cancer patients included subjects who
had undergone resection of the oropharynx (soft palate or tonsillar region). Such subjects were excluded here because they might have velopharyngeal incompetence; a distinct and separate causative factor of speech disorder5,9. The results of the SIT and CUT assessments showed correlations between the site and size of resection and functional speech outcome. Better functional outcomes were obtained for lateral type resection and smaller excisions. These results are in good agreement with former reports4,9,12. The larger significant difference between the L subgroups and A subgroups in the CUT than in the SIT is attributable to the fact that the CUT
requires more skilful tongue movements than the SIT. In terms of functional speech outcome in relation to site and size of resection, subjective assessment revealed no significant difference among the groups for communication with families. Self-evaluations did differ significantly between the L subgroups and groups A and C for communication on the telephone and at first contact. Thus, subjective assessment of speech function differed according to the communicative situation. Patients in groups A and C might have overestimated their performance in communication with families, but it is also plausible that frequent opportunities to contact others, especially within families, helps the patients to cope with speech difficulties, because this category had statistical significance on the objective tests. The tongue is the key structure for pronunciation. Certain plosives and affricates can only be pronounced by tongue elevation, with the tongue contacting or approaching the alveolar ridge or palate4,8. In the tongue mobility test, lateral subgroups scored higher than A subgroups and the C group. The results were very similar to those of the SIT and CUT. In fact, tongue mobility tests had very high CC with the objective tests. Thus, surgeons should be cognizant of the best approaches to maintain mobility of the residual tongue during surgery, especially when suturing a flap to the surgical margin such as the floor of the mouth. The subjective questionnaires and tongue mobility test showed high correlations with the SIT and CUT. These subjective tests have clinical value because they can be much more easily utilized in clinical situations than the objective tests considered to be the ‘gold standard’. In the present study, of the five tests performed, two — the SIT and a subjective assessment — showed significantly negative effects of irradiation on speech outcome. The effect of radiation therapy on speech is controversial. PAULOSKI et al.11 reported that overall speech function did not differ between irradiated and non-irradiated patients. In contrast, NICO9 LETTI et al. found radiation to have a significantly negative effect by objective and subjective analyses. They attributed this effect to the greater extent of surgical damage experienced by patients who undergo radiotherapy. In the present study, the distribution of patients among the irradiated and non-irradiated groups was similar with respect to site and size of resection. Fibrosis would be a possible negative factor because irradiation forms
Factors influencing postoperative speech function Table 3.4. Results of tongue mobility (total score)
Table 4. CCs between tongue mobility and functional results SIT Protrusion Tip elevation Dorsum elevation Total score **
CUT
0.63** 0.65** 0.60** 0.73**
0.58** 0.62** 0.50** 0.67**
Families
Telephone
First contact
0.35** 0.31** 0.39** 0.41**
0.45** 0.39** 0.35** 0.46**
0.44** 0.46** 0.45** 0.53**
Telephone
First contact
P < 0.01.
Table 5. Effect of radiation therapy on functional results Radiation (+) vs. ( ) *
SIT
CUT
Families
0.0074**
0.074
0.014*
0.081
0.072
Telephone
First contact
P < 0.05. P < 0.01.
**
Table 6. Effect of mandibulectomy on functional results No resect. vs. marginal No resect. vs. segmental Marginal vs. segmental *
SIT
CUT
Families
0.084 0.061 0.24
0.49 0.044* 0.042*
0.011* 0.019* 0.13
0.0069** 0.022* 0.11
0.0039** 0.064 0.34
P < 0.05. P < 0.01.
**
Table 7. CCs between age and time intervals on functional results SIT Age at operation Age at examination Time interval *
P < 0.05. P < 0.01.
**
0.31** 0.25* 0.20
CUT 0.34* 0.29* 0.31*
Families 0.12 0.10 0.06
Telephone 0.16 0.10 0.06
First contact 0.10 0.13 0.03
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fibrotic tissue which interferes with tongue mobility11. The comparison between preand postoperative radiation therapy showed no differences. This might be attributed to a wide variation in radiotherapy characteristics such as dose and duration in both groups. A well-structured prospective study is accordingly needed in the future to elucidate this point. Mandibulectomy, and particularly segmental osteotomy, severely impacted postoperative speech function. Mandibulectomy often results in loss of the attachments of the extrinsic muscles (genioglossus, geniohyoid and mylohyoid muscles). Together with the intrinsic muscles of the tongue, the integrity and function of the extrinsic muscles is a very important factor influencing functional outcome9. Age at operation and at examination were found to be negative factors, possibly resulting from the decreasing capacity of older individuals to compensate for speech deficits after surgical eradication2,6,10,14. With regard to time intervals, various studies used a 12-month interval as the termination point because postoperative quality of life had reached pretreatment levels by 1 year9. The 12-month interval has also been used as a predictor of outcome after primary surgery13. In the present study, the time interval for most subjects was longer than 12 months (mean 35.9 29.0 months, mode 44 months, median 26 months), and the CUT clearly showed postoperative recovery after 1 year, with gradual plateau of the logarithmic regression curve. Thus, accurate evaluation of functional postoperative speech function might require a period longer than 1 year. Type of flap reconstruction is determined mainly by the expected size of the defect. It is generally said that the RFF is the first choice for reconstruction because of its thin and pliable nature, and that free myocutaneous flaps such as the RAMCF are needed for larger volume defects12. In the present study, different types of flap were used in each group, which made it possible to compare the functional outcome of various types of flaps in a similar defect. The results indicated that no one type of flap was significantly superior with respect to functional outcome4,9. Suturing a flap to the surgical margin to maintain the mobility of the remaining structure is important in patients who had a relatively small defect involving the floor of the mouth. In relatively large defects, the type of flap should be determined individually in consideration of a variety of factors including defect
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Table 8. Data on type of flap reconstruction Self-assessment Group
Flap type
Families
Telephone
First contact
SIT
CSU
L2
RFF RAMCF
3.9 0.9 4.2 1.0
3.7 0.9 3.8 0.8
3.5 0.9 3.8 0.8
73.6 14.6 66.2 20.0
1.2 0.4 1.4 0.4
L3
RFF RAMCF PMMC
4.0 0.7 3.3 0.6 4.0 1.0
3.9 0.8 3.0 1.0 4.0 1.0
3.9 0.9 3.3 0.6 4.0 1.0
71.4 16.9 62.4 20.8 60.6 17.8
1.3 0.4 1.9 0.8 1.4 0.6
A2
RFF RAMCF
4.0 0.9 3.7 0.6
3.7 0.8 3.3 1.2
3.8 1.5 3.0 1.0
55.0 25.1 54.9 19.5
1.9 1.1 2.0 0.6
C
RFF RAMCF
2.6 0.5 3.6 0.8
2.6 0.5 2.9 0.9
2.8 0.4 3.0 0.8
44.0 17.8 36.7 22.3
2.5 1.5 2.7 1.4
3.
4.
Values are means 1SD.
volume at the recipient site, available volume at the donor site, skill of the surgeon and donor site morbidity, because available volume in the same donor site differs from patient to patient. A treatment method that causes less functional interference is required, particularly for patients anticipated to be in a poor functional state postoperatively. Acknowledgements. The authors would like to express sincere gratitude to the following doctors: Kiyohide Fujita, Satoshi Umino and Ryoichi Kawabe, Department of Oral and Maxillofacial Surgery, Yokohama City University School of Medicine, Yokohama Japan; Satoru Ozeki, Section of Oral Oncology, Department of Oral & Maxillofacial Surgery, Division of Oral & Medical Management, Fukuoka Dental College, Fukuoka, Japan, Kazunari Oobu, Section of Oral and Maxillofacial Oncology, Division of Maxillofacial Diagnostic and Surgical Sciences. Faculty of Dental Science, Kyushu University, Fukuoka, Japan; Sadao Okabe, Department of Oral Surgery, Saitama Cancer Center, Saitama, Japan; Yukihiko Kinoshita, Institute for Frontier Oral Science, Kanagawa Dental College, Yokosuka, Japan: Masaru Hosoda, Department of Oral and Maxillofacial Surgery, Kawasaki Medical College, Kurashiki, Japan; Mikihiko Kogo, Tomomi Yamamoto, Seiji Iida, Masaya Ohkura, First Department of Oral and Maxillofacial Surgery, Osaka University Graduate School of Dentistry, Ohsaka University; Kan-ichi Seto, First Department of Oral and Maxillofacial Surgery, School of Dental Medicine, Tsurumi University, Yokohama, Japan; Katsunori Ishibashi, Kouichi Asada and Toru Sato, Second Department of Oral and Maxillofacial Surgery, School of Dental Medicine, Tsurumi University, Yokohama, Japan; Masaro Matsuura, Sec-
tion of Oral Implantology, Department of Oral Rehabilitation, Division of Clinical Dentistry, Fukuoka Dental College, Fukuoka, Japan; Takaomi Satomi and Hiroshige Chiba, Department of Oral and Maxillofacial Surgery, Tokyo Medical University, Tokyo, Japan; Teruo Amagasa, Shoji Yamashiro and Jyun-ichi Ishii, Maxillofacial Surgery, Maxillofacial Reconstruction and Function, Division of Maxillofacial and Neck Reconstruction, Graduate School, Tokyo Medical and Dental University, Tokyo, Japan; Hidemi Yoshimasu, Department of Community Oral Health Care Science, School of Oral Health Care Sciences, Faculty of Dentistry, Tokyo Medical and Dental University; Koji Fujibayashi and Yutaka Imai, Department of Oral and Maxillofacial Surgery, Dokkyo University School of Medicine, Tochigi, Japan; Kenichi Tomitsuka, Department of Oral and Maxillofacial Surgery, Course of Metabolic and Regenerative Medicine, School of Medicine, Faculty of Medicine, Yamagata University, Yamagata, Japan; Mitsunobu Ono, Kanchu Tei and Yasunori Totsuka, Oral and Maxillofacial Surgery, Department of Oral Pathobiological Science, Graduated School of Dental Medicine, Hokkaido University, Sapporo, Japan and Ken-ichi Michi, Yukihiro Michiwaki and Satoko Imai, Department of Oral and Maxillofacial Surgery, School of Dentistry, Showa University, Tokyo, Japan.
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Disorder. Tokyo: Igakushoin 1966: 37– 38. Address: Yoshiro Matsui Department of Oral and Maxillofacial Surgery Graduate School of Medicine
Yokohama City University 3-9 Fukuura Kanazawa-ku Yokohama 236-0004 Japan Tel: +81 45 787 2659 Fax: +81 45 785 8438 E-mail: [email protected]
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Clinical Paper Head & Neck Oncology
Factors influencing postoperative speech function of tongue cancer patients following reconstruction with fasciocutaneous/myocutaneous flaps—a multicenter study
Y. Matsui1,2, K. Ohno2, Y. Yamashita3, K. Takahashi3 1 Department of Oral and Maxillofacial Surgery, Graduate School of Medicine, Yokohama City University, Yokohama 2360004, Japan; 2Department of Oral and Maxillofacial Surgery, School of Dentistry, Showa University, Tokyo 145-8515, Japan; 3 Department of Oral Rehabilitation, Showa Dental Hospital, Showa University, Tokyo 1458515, Japan
Y. Matsui, K. Ohno, Y. Yamashita, K. Takahashi: Factors influencing postoperative speech function of tongue cancer patients following reconstruction with fasciocutaneous/myocutaneous flaps—a multicenter study. Int. J. Oral Maxillofac. Surg. 2007; 36: 601–609. # 2007 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved. Abstract. This study investigated postoperative speech function in tongue cancer patients following reconstruction with fasciocutaneous/myocutaneous flaps, to clarify the factor(s) influencing outcome. Eighty-one patients, enrolled from 11 Japanese institutions, were classified into three groups by the site of resection: lateral (N = 51), anterior (N = 17) and combined (N = 13). The lateral group was divided into three subgroups and the anterior group into two subgroups by the size of resection. Mandibulectomy had been performed in 43 patients and radiation therapy in 24 patients. Reconstruction was accomplished by radial forearm flap (N = 50), rectus abdominis myocutaneous flap (N = 18), pectoralis major myocutaneous flap (N = 11), latissimus dorsi myocutaneous flap (N = 1) or scapula flap (N = 1). Speech function was evaluated with two objective tests and three self-reporting questionnaires. The influence of tongue mobility, age at operation and examination, time interval to examination, and type of flap reconstruction on the functional results was also investigated. Better results were obtained with lateral type resections, smaller excisions, greater tongue mobility, younger patients and longer interval to examination. Mandibulectomy and radiation therapy were negative factors. Type of flap reconstruction had no effect on functional outcome. A treatment method with less functional interference should be developed, particularly for patients anticipated to be in poor functional state postoperatively.
0901-5027/070601 + 09 $30.00/0
Key words: speech function; reconstruction; tumour surgery; tongue. Accepted for publication 10 January 2007 Available online 23 March 2007
# 2007 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
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Surgical ablation of tongue cancer often causes severe postoperative speech impairment because the tongue is a primary active articulator. While recent progress in reconstructive surgery offers new therapeutic options suitable for the complex anatomy and function of the tongue, the numerous studies that have evaluated postoperative speech function subjectively and objectively1,3,4,5,8,9,12 often involved a wide range of resected sites in a limited number of patients. Few studies have assessed in detail the factors influencing functional outcome of speech with a large number of subjects. The present multicenter study investigated postoperative speech function of tongue cancer patients following reconstruction with fasciocutaneous/myocutaneous flaps so as to clarify the influencing factor(s).
Patients and methods Subjects
From 232 patients who had undergone reconstruction with fasciocutaneous/ myocutaneous flaps after ablative surgery at 11 Japanese institutions, a total of 81 patients (28 women and 53 men; mean age at examination, 59.1 years; range, 23–82 years) with proven malignant tumour of the tongue and/or floor of the mouth were enrolled in the study. Reconstruction with a flap was one of the criteria for selection. General information about the participants was collected by the responsible surgeon under a standard protocol including several surgical variables: age, T stage, extent of resection, radiotherapy and type of flap reconstruction. Staging was T1 in 5 patients, T2 in 44, T3 in 21 and T4 in 11.
Fig. 1. Classification of area reconstructed with flaps.
Site and size of resection
Subjects were classified into three main anatomical groups according to the resected site: lateral (N = 51), anterior (N = 17) and combined (N = 13). The lateral group was further divided into three subgroups according to the size of resection: partial excisions of the anterior two thirds of the lateral border of the tongue (group L1; N = 10), half resections of the anterior two thirds of the lateral border of the tongue (group L2; N = 24) and complete hemiglossectomies (group L3; N = 17). All patients in the lateral subgroups underwent resection of the floor of the mouth to some extent, but this never exceeded the midline. The anterior group all had some excision of the bilateral floor of the mouth with resection of the tongue, and this group was subdivided into two
Factors influencing postoperative speech function Table 1. Number of patients Group L1
L2
L3
A1
A2
C
Total
Total Radiation therapy
10 2
24 9
17 2
6 2
11 4
13 5
81 24
Mandibulectomy Marginal Segmental
5 0
6 2
10 1
4 1
4 3
6 1
35 8
according to depth of resection: resection of anterior floor of the mouth not deeper than one-third full thickness of the midline up to the mylohyoid muscle plane (group A1; N = 6) and resection of anterior floor of the mouth deeper than one-third and up to two-thirds full thickness of the midline (group A2; N = 11). Subjects who underwent subtotal hemiglossectomy and/or resection of the anterior floor of the mouth deeper than two-thirds full thickness of the midline were categorized as the combined group (group C; N = 13) (Fig. 1 and Table 1). None of the 81 patients had undergone resection of the soft palate or tonsillar region. Radiotherapy
A total of 24 patients had received radiotherapy; 15 preoperatively and 9 postoperatively. Irradiated dose ranged from 18 to 90 Gy (Table 1). Neither age, time interval, resected site nor incidence of mandibulectomy differed significantly between non-irradiated and irradiated patients (x2 test). Mandibulectomy
Mandibulectomy had been performed in 43 patients; marginal in 35 and segmental in 8 (Table 1). There was no significant difference between the two types of mandibulectomy in terms of age, time interval, site and size of resection, or incidence of radiotherapy. After segmental osteotomy, the mandible had been reconstructed with a titanium plate at the ablative surgery in all patients except one, who underwent simultaneous reconstruction with a scapula flap. Three of seven subsequently underwent mandibular reconstruction using bone harvested from the ilium. Type of flap reconstruction
In group L1, all patients except one underwent reconstruction with a free radial forearm flap (RFF). In the remaining patient, a vascularized pectoralis major myocutaneous flap (PMMCF) was used. In group L2, the most popular flap type
was the RFF, but some patients underwent reconstruction with a free rectus abdominis myocutaneous flap (RAMCF). In group L3, reconstruction involved an RFF in nine patients, a PMMCF in five and an RAMCF in three. In group A1, reconstruction involved an RFF in four patients, a PMMCF in one and a RAMCF in one. In group A2, surgeons used an RFF in six patients, an RAMCF in three and a PMMCF in two. In group C, flaps used were an RAMCF in seven patients, an RFF in five and a PMMCF in one. Methods for evaluation
Two objective tests and three self-assessment questionnaires were performed for functional evaluation. The speech intelligibility test (SIT) and conversational understandability test (CUT) were used for objective evaluation of speech function. The SIT was conducted in Japanese. Each subject was instructed to pronounce 100 syllables listed, and pronunciation was recorded. Ten untrained volunteers with normal hearing, who did not know the patient, then listened to the tape and transcribed the sounds as Japanese syllables that they believed they had heard. The intelligibility score was expressed as the percentage of correct responses7. In the CUT, an audio recording of a 5-min conversation with an interviewer was evaluated by a group of five untrained volunteers with normal hearing for conversational understandability using a 5point scale: 5, all speech is understood; 4, sometimes not understood; 3, can be understood when conversational content is already known; 2, sometimes understood and 1, nothing is understood15. For each objective test, the mean score was calculated for each patient and used in subsequent analysis. Self-assessment of speech function was performed using three selfreporting questionnaires relating to three situations involving functional spoken communication: with families, on the telephone and when first meeting someone (at first contact). Responses to each questionnaire were scored on the same 5-point scale. These questionnaires were mailed
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with instructions to the subjects, who returned the responses directly to the authors. Time interval between surgical treatment and completion of the selfreporting questionnaires ranged from 5 to 201 months (mean 35.9 29.0 months, mode 44 months, median 26 months). On the same occasion as the objective and subjective functional tests, the tongue mobility test was performed by observing protrusion or elevation of the tip and dorsum. Each movement was evaluated using a 3-point scale. For protrusion: 2, tongue tip can contact the lip; 1, can contact the dental arch; 0, only remains inside the dental arch. For elevation of the tip and dorsum: 2, tongue tip can contact the palate; 1, can elevate, but not contact the palate; 0, cannot elevate. The sum of the scores for the three motions was then calculated. Correlations between tongue mobility and both objective and subjective results were analyzed to evaluate the accuracy and clinical values of these assessments. It was also investigated whether other factors, i.e. mandibulectomy, radiation therapy including a comparison between pre- and postoperative irradiation, age at operation and examination, time interval between operation and examination, and type of flap reconstruction, influenced the objective functional results. Speech therapy intervention, which might have been available in some institutions, was not included in the investigated factors because relevant information could not be obtained. Statistical analyses
Statistical analyses were performed using Stat View 5.0 J software (SAS Institute Inc., USA). An independent samples t-test was used for comparing the objective and subjective results in each pair of subgroups with regard to site and size of resection, mandibulectomy, and radiotherapy (for pre- and postoperative irradiation). Sample coefficient correlation (CC) was used to examine the relationship between tongue mobility and both objective and subjective results. The effect of age at operation and examination, and that of time interval on the objective results were also investigated with CC. The influence of type of flap reconstruction was analyzed by a Mann– Whitney U-test as follows: in subgroup L2, RFF versus RAMCF; in subgroup L3, RFF versus PMMC, RFF versus RAMCF and PMMC versus RAMCF; in subgroup A2, RFF versus RAMCF and in group C, RFF versus RAMCF. A P-value less than 0.05 was considered significant.
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Matsui et al. Table 2.1. Results of self-assessment (communication with families) Score
L1
L2
L3
A1
A2
C
1 2 3 4 5
0 0 2 5 3
0 1 10 5 8
0 0 6 7 4
0 1 3 1 1
0 0 5 4 2
0 0 8 3 2
groups. Group C scored lowest. The difference between the L subgroups and A subgroups had widened, with almost all subgroups showing a significant difference in scores (Fig. 3). Subjective assessment with questionnaires
Fig. 2. Results of speech intelligibility test (SIT). Better functional outcome was obtained for lateral type and smaller excisions. Group C had the lowest values, and differed significantly from all lateral group values.
Results Objective evaluation with SIT and CUT
In the SIT, group L1 scored highest (mean 1SD: 75.3 8.6) and group C lowest (41.5 20.2). Lateral subgroups scored higher than A subgroups and group
C. Wider resection resulted in a lower intelligibility score within the L and A groups. Group C, the lowest scoring group, showed a significant difference when compared to all lateral subgroups (Fig. 2). Similarly, in the CUT, L subgroups scored higher than the A and C
With regard to self-reported speech function, almost all patients scored more than 3 on the questionnaire concerning communication with families. There was no statistical difference between any groups, although more patients had higher scores in the L subgroups compared to the A subgroups and group C (Table 2.1). In all groups, some patients scored themselves as less than 2 for communication on the telephone and at first contact. The difference between the L subgroups and other two groups had increased, with a significant difference seen for group C patients and all L subgroups for both communication on the telephone and at first contact (Tables 2.2 and 2.3). Tongue mobility test
Group L1 scored highest on each tongue mobility test. No subject in that group scored 0 in any of the movements. Lateral subgroups scored higher than A subgroups and the C group. Statistically significant differences were found for almost all sets between L and A subgroups and between L and C groups, except with respect to dorsum elevation (Tables 3.1–3.4). CCs between objective results and subjective assessment
All CCs between objective results and subjective assessments were statistically significant (P < 0.01). ‘First contact’ scored highest: 0.65 with SIT and 0.51 with CUT, and ‘families’ scored lowest: 0.53 with SIT and 0.46 with CUT.
Fig. 3. Results of conversational understandability test (CUT). Lower scores indicate better function on CUT. Scores differed significantly between almost all L groups and group C and both A subgroups.
CCs between tongue mobility test and functional results
Each category of tongue mobility test had statistically significant CCs with all
Factors influencing postoperative speech function Table 2.2. Results of self-assessment (communication on the telephone)
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objective and subjective results. Total score and tip elevation showed particularly high CCs (Table 4). Effect of other factors on the functional results
Radiation therapy (Table 5)
Table 2.3. Results of self-assessment (communication at first contact)
The irradiated group had poorer subjective and objective evaluation scores than the non-irradiated group for all measurements: mean scores 1SD for the respective non-irradiated and irradiated groups were 3.89 0.82 and 3.5 0.86 for communication with families, 3.62 0.89 and 3.04 1.22 for on the telephone, 3.63 0.94 and 3.12 1.03 for at first contact, 66.0 18.6 and 52.5 24.9 in the SIT and 1.57 0.83 and 1.93 1.06 in the CUT. Subdivision of the irradiated group into pre- and post-irradiated groups showed no differences in terms of functional speech results. Mandibulectomy (Table 6)
For all self-assessment categories and the SIT, the non-resection group scored highest and the segmental group lowest. Mean scores 1SD of the respective non-resection, marginal and segmental groups were 4.04 0.77, 3.6 0.85 and 3.14 0.9 for communication with families; 3.79 0.83, 3.26 0.98 and 2.57 1.27 for on the telephone; 3.79 0.89, 3.2 0.96 and 3 1.15 for at first contact and 66.3 21.5, 59.2 21.8 and 53.4 17.3 in the SIT. The segmental group also had the lowest CUT value: mean score 1SD was 1.61 0.93 in the non-resection group, 1.6 0.84 in the marginal group and 2.31 0.89 in the segmental group. Table 3.1. Results of tongue mobility (protrusion)
Age and time intervals
Older patients at the time of operation and at the time of examination had significantly lower quality postoperative speech: CC was 0.31 in the SIT and 0.34 in the CUT for age at operation, and 0.25 in the SIT and 0.29 in the CUT for age at examination. Longer time interval between operation and examination was associated with better postoperative CUT results; the logarithmic regression curve gradually plateaued with increasing interval (data not shown). The effect on SIT results was unclear (P = 0.20) (Table 7). Type of flap
The RFF exhibited a better objective score than the RAMCF in all subgroups. There
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Table 3.2. Results of tongue mobility (tip elevation)
Table 3.3. Results of tongue mobility (dorsum elevation)
were no significant differences in type of flap reconstruction within individual subgroups (Table 8). Discussion
In the present study, the subjects were divided into three groups by the site of resection (groups L, A and C). The L and A groups were further divided into three and two subgroups, respectively, to investigate in detail the influence of site and size of resection and type of flap reconstruction on speech function. Certain previous reports that investigated postoperative speech function of tongue cancer patients included subjects who
had undergone resection of the oropharynx (soft palate or tonsillar region). Such subjects were excluded here because they might have velopharyngeal incompetence; a distinct and separate causative factor of speech disorder5,9. The results of the SIT and CUT assessments showed correlations between the site and size of resection and functional speech outcome. Better functional outcomes were obtained for lateral type resection and smaller excisions. These results are in good agreement with former reports4,9,12. The larger significant difference between the L subgroups and A subgroups in the CUT than in the SIT is attributable to the fact that the CUT
requires more skilful tongue movements than the SIT. In terms of functional speech outcome in relation to site and size of resection, subjective assessment revealed no significant difference among the groups for communication with families. Self-evaluations did differ significantly between the L subgroups and groups A and C for communication on the telephone and at first contact. Thus, subjective assessment of speech function differed according to the communicative situation. Patients in groups A and C might have overestimated their performance in communication with families, but it is also plausible that frequent opportunities to contact others, especially within families, helps the patients to cope with speech difficulties, because this category had statistical significance on the objective tests. The tongue is the key structure for pronunciation. Certain plosives and affricates can only be pronounced by tongue elevation, with the tongue contacting or approaching the alveolar ridge or palate4,8. In the tongue mobility test, lateral subgroups scored higher than A subgroups and the C group. The results were very similar to those of the SIT and CUT. In fact, tongue mobility tests had very high CC with the objective tests. Thus, surgeons should be cognizant of the best approaches to maintain mobility of the residual tongue during surgery, especially when suturing a flap to the surgical margin such as the floor of the mouth. The subjective questionnaires and tongue mobility test showed high correlations with the SIT and CUT. These subjective tests have clinical value because they can be much more easily utilized in clinical situations than the objective tests considered to be the ‘gold standard’. In the present study, of the five tests performed, two — the SIT and a subjective assessment — showed significantly negative effects of irradiation on speech outcome. The effect of radiation therapy on speech is controversial. PAULOSKI et al.11 reported that overall speech function did not differ between irradiated and non-irradiated patients. In contrast, NICO9 LETTI et al. found radiation to have a significantly negative effect by objective and subjective analyses. They attributed this effect to the greater extent of surgical damage experienced by patients who undergo radiotherapy. In the present study, the distribution of patients among the irradiated and non-irradiated groups was similar with respect to site and size of resection. Fibrosis would be a possible negative factor because irradiation forms
Factors influencing postoperative speech function Table 3.4. Results of tongue mobility (total score)
Table 4. CCs between tongue mobility and functional results SIT Protrusion Tip elevation Dorsum elevation Total score **
CUT
0.63** 0.65** 0.60** 0.73**
0.58** 0.62** 0.50** 0.67**
Families
Telephone
First contact
0.35** 0.31** 0.39** 0.41**
0.45** 0.39** 0.35** 0.46**
0.44** 0.46** 0.45** 0.53**
Telephone
First contact
P < 0.01.
Table 5. Effect of radiation therapy on functional results Radiation (+) vs. ( ) *
SIT
CUT
Families
0.0074**
0.074
0.014*
0.081
0.072
Telephone
First contact
P < 0.05. P < 0.01.
**
Table 6. Effect of mandibulectomy on functional results No resect. vs. marginal No resect. vs. segmental Marginal vs. segmental *
SIT
CUT
Families
0.084 0.061 0.24
0.49 0.044* 0.042*
0.011* 0.019* 0.13
0.0069** 0.022* 0.11
0.0039** 0.064 0.34
P < 0.05. P < 0.01.
**
Table 7. CCs between age and time intervals on functional results SIT Age at operation Age at examination Time interval *
P < 0.05. P < 0.01.
**
0.31** 0.25* 0.20
CUT 0.34* 0.29* 0.31*
Families 0.12 0.10 0.06
Telephone 0.16 0.10 0.06
First contact 0.10 0.13 0.03
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fibrotic tissue which interferes with tongue mobility11. The comparison between preand postoperative radiation therapy showed no differences. This might be attributed to a wide variation in radiotherapy characteristics such as dose and duration in both groups. A well-structured prospective study is accordingly needed in the future to elucidate this point. Mandibulectomy, and particularly segmental osteotomy, severely impacted postoperative speech function. Mandibulectomy often results in loss of the attachments of the extrinsic muscles (genioglossus, geniohyoid and mylohyoid muscles). Together with the intrinsic muscles of the tongue, the integrity and function of the extrinsic muscles is a very important factor influencing functional outcome9. Age at operation and at examination were found to be negative factors, possibly resulting from the decreasing capacity of older individuals to compensate for speech deficits after surgical eradication2,6,10,14. With regard to time intervals, various studies used a 12-month interval as the termination point because postoperative quality of life had reached pretreatment levels by 1 year9. The 12-month interval has also been used as a predictor of outcome after primary surgery13. In the present study, the time interval for most subjects was longer than 12 months (mean 35.9 29.0 months, mode 44 months, median 26 months), and the CUT clearly showed postoperative recovery after 1 year, with gradual plateau of the logarithmic regression curve. Thus, accurate evaluation of functional postoperative speech function might require a period longer than 1 year. Type of flap reconstruction is determined mainly by the expected size of the defect. It is generally said that the RFF is the first choice for reconstruction because of its thin and pliable nature, and that free myocutaneous flaps such as the RAMCF are needed for larger volume defects12. In the present study, different types of flap were used in each group, which made it possible to compare the functional outcome of various types of flaps in a similar defect. The results indicated that no one type of flap was significantly superior with respect to functional outcome4,9. Suturing a flap to the surgical margin to maintain the mobility of the remaining structure is important in patients who had a relatively small defect involving the floor of the mouth. In relatively large defects, the type of flap should be determined individually in consideration of a variety of factors including defect
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Matsui et al.
Table 8. Data on type of flap reconstruction Self-assessment Group
Flap type
Families
Telephone
First contact
SIT
CSU
L2
RFF RAMCF
3.9 0.9 4.2 1.0
3.7 0.9 3.8 0.8
3.5 0.9 3.8 0.8
73.6 14.6 66.2 20.0
1.2 0.4 1.4 0.4
L3
RFF RAMCF PMMC
4.0 0.7 3.3 0.6 4.0 1.0
3.9 0.8 3.0 1.0 4.0 1.0
3.9 0.9 3.3 0.6 4.0 1.0
71.4 16.9 62.4 20.8 60.6 17.8
1.3 0.4 1.9 0.8 1.4 0.6
A2
RFF RAMCF
4.0 0.9 3.7 0.6
3.7 0.8 3.3 1.2
3.8 1.5 3.0 1.0
55.0 25.1 54.9 19.5
1.9 1.1 2.0 0.6
C
RFF RAMCF
2.6 0.5 3.6 0.8
2.6 0.5 2.9 0.9
2.8 0.4 3.0 0.8
44.0 17.8 36.7 22.3
2.5 1.5 2.7 1.4
3.
4.
Values are means 1SD.
volume at the recipient site, available volume at the donor site, skill of the surgeon and donor site morbidity, because available volume in the same donor site differs from patient to patient. A treatment method that causes less functional interference is required, particularly for patients anticipated to be in a poor functional state postoperatively. Acknowledgements. The authors would like to express sincere gratitude to the following doctors: Kiyohide Fujita, Satoshi Umino and Ryoichi Kawabe, Department of Oral and Maxillofacial Surgery, Yokohama City University School of Medicine, Yokohama Japan; Satoru Ozeki, Section of Oral Oncology, Department of Oral & Maxillofacial Surgery, Division of Oral & Medical Management, Fukuoka Dental College, Fukuoka, Japan, Kazunari Oobu, Section of Oral and Maxillofacial Oncology, Division of Maxillofacial Diagnostic and Surgical Sciences. Faculty of Dental Science, Kyushu University, Fukuoka, Japan; Sadao Okabe, Department of Oral Surgery, Saitama Cancer Center, Saitama, Japan; Yukihiko Kinoshita, Institute for Frontier Oral Science, Kanagawa Dental College, Yokosuka, Japan: Masaru Hosoda, Department of Oral and Maxillofacial Surgery, Kawasaki Medical College, Kurashiki, Japan; Mikihiko Kogo, Tomomi Yamamoto, Seiji Iida, Masaya Ohkura, First Department of Oral and Maxillofacial Surgery, Osaka University Graduate School of Dentistry, Ohsaka University; Kan-ichi Seto, First Department of Oral and Maxillofacial Surgery, School of Dental Medicine, Tsurumi University, Yokohama, Japan; Katsunori Ishibashi, Kouichi Asada and Toru Sato, Second Department of Oral and Maxillofacial Surgery, School of Dental Medicine, Tsurumi University, Yokohama, Japan; Masaro Matsuura, Sec-
tion of Oral Implantology, Department of Oral Rehabilitation, Division of Clinical Dentistry, Fukuoka Dental College, Fukuoka, Japan; Takaomi Satomi and Hiroshige Chiba, Department of Oral and Maxillofacial Surgery, Tokyo Medical University, Tokyo, Japan; Teruo Amagasa, Shoji Yamashiro and Jyun-ichi Ishii, Maxillofacial Surgery, Maxillofacial Reconstruction and Function, Division of Maxillofacial and Neck Reconstruction, Graduate School, Tokyo Medical and Dental University, Tokyo, Japan; Hidemi Yoshimasu, Department of Community Oral Health Care Science, School of Oral Health Care Sciences, Faculty of Dentistry, Tokyo Medical and Dental University; Koji Fujibayashi and Yutaka Imai, Department of Oral and Maxillofacial Surgery, Dokkyo University School of Medicine, Tochigi, Japan; Kenichi Tomitsuka, Department of Oral and Maxillofacial Surgery, Course of Metabolic and Regenerative Medicine, School of Medicine, Faculty of Medicine, Yamagata University, Yamagata, Japan; Mitsunobu Ono, Kanchu Tei and Yasunori Totsuka, Oral and Maxillofacial Surgery, Department of Oral Pathobiological Science, Graduated School of Dental Medicine, Hokkaido University, Sapporo, Japan and Ken-ichi Michi, Yukihiro Michiwaki and Satoko Imai, Department of Oral and Maxillofacial Surgery, School of Dentistry, Showa University, Tokyo, Japan.
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Disorder. Tokyo: Igakushoin 1966: 37– 38. Address: Yoshiro Matsui Department of Oral and Maxillofacial Surgery Graduate School of Medicine
Yokohama City University 3-9 Fukuura Kanazawa-ku Yokohama 236-0004 Japan Tel: +81 45 787 2659 Fax: +81 45 785 8438 E-mail: [email protected]
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