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Functional outcome after partial glossectomy with reconstruction using radial forearm free flap
Auris Nasus Larynx 40 (2013) 303–307
Contents lists available at SciVerse ScienceDirect
Auris Nasus Larynx journal homepage: www.elsevier.com/locate/anl
Functional outcome after partial glossectomy with reconstruction using radial forearm free flap Young-Hoon Joo, Se-Hwan Hwang, Jun-Ook Park, Kwang-Jae Cho, Min-Sik Kim * Department of Otolaryngology – Head and Neck Surgery, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea
A R T I C L E I N F O
A B S T R A C T
Article history: Received 23 April 2012 Accepted 14 July 2012 Available online 10 August 2012
Objective: The purpose of this study was to investigate the relationship between the radial forearm free flap (RFFF) volume changes and speech and swallowing outcomes. Methods: The study included 18 subjects with squamous cell carcinoma of the oral tongue. Results: Average percentage changes in flap volume between 3 and 12 months was 19.2%. Postoperative free flap volume changes were significantly and negatively correlated with the word and sentence intelligibility (Y = 0.338X + 43.641, r2 = 0.383, p = 0.006 and Y = 0.246X + 34.322, r2 = 0.321, p = 0.014, respectively). A significant positive correlation was also found between word and sentence intelligibility and floor of mouth resected, postoperative irradiation. Postoperative flap volume changes between 3 and 12 months were correlated with reduced posterior bolus movement by tongue (p = 0.002), reduced tongue base to posterior pharyngeal wall contact (p = 0.002), reduced laryngeal elevation (p = 0.005), increased aspiration (p = 0.005), delayed oral (p = 0.010) and pharyngeal transit time (p = 0.011). Floor of mouth resected, tongue base resected, and postoperative irradiation also influenced the swallowing outcomes. Conclusions: This study shows that postoperative flap volume changes are significantly related to speech and swallowing outcomes in patients undergoing partial glossectomy reconstructed with RFFF. ß 2012 Elsevier Ireland Ltd. All rights reserved.
Keywords: Surgical flaps Organ size Computer-assisted image processing Tongue Treatment outcome
1. Introduction Restoration of function following glossectomy is one of the great remaining challenges for head and neck reconstructive surgeons. The extent of surgical resection, particularly, the amount of oral tongue and tongue base resected, has been implicated as the primary correlate of swallowing impairment in postsurgical oral and oropharyngeal cancer patients [1–4]. Some studies have suggested that swallowing function depends on the method of reconstruction rather than on the degree of resection [5–7]. The principal goal of tongue reconstruction is to re-establish the functions of speech, mastication, and swallowing, and thus, microvascular tissue transfer has been regularly employed since the 1990s. The advantages of microvascular reconstruction of the tongue are; freedom of flap placement without tethering, the possibility of bone reconstruction, and the possibility to model and design the desired form [8]. It is now recognized that immediate reconstruction at the time of tumor resection optimizes functional results [9]. Furthermore, because the volume of the reconstructed tongue affects functional outcomes,
* Corresponding author at: Department of Otolaryngology – HNS, 505 Banpodong Seochogu Seoul St. Mary’s Hospital, The Catholic University of Korea, Seoul 137-040, Republic of Korea. Tel.: +82 2 2258 6211; fax: +82 2 595 1354. E-mail addresses: [email protected], [email protected] (M.-S. Kim). 0385-8146/$ – see front matter ß 2012 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.anl.2012.07.012
such as, swallowing function and speech intelligibility, changes observed in the neotongue after a long-term follow-up require investigation [1,10,11]. As we previously reported, overcorrection with a 40% greater radial forearm free flap (RFFF) volume is recommended for the reconstruction of tumor-related defects in the head and neck [12]. RFFF is the most commonly used sensate flap in the head and neck. The thin, pliable nature of the fasciocutaneous flaps is ideally suited for head and neck reconstructions, especially when the defect involves multiple sites, such as the pharyngeal wall, soft palate, and tongue base. In our experience, reconstruction with the RFFF is a safe and effective method associated with the restoration of the functional outcome among patients undergoing partial glossectomy. The purpose of this study was to estimate postoperative RFFF volume changes and evaluate the relationship between free flap volume changes and speech and swallowing functions in patients after partial glossectomy. 2. Materials and methods 2.1. Patient population The clinical and pathological data of 40 consecutive patients diagnosed with tongue cancer that underwent partial glossectomy
304
Y.-H. Joo et al. / Auris Nasus Larynx 40 (2013) 303–307
followed by RFFF reconstruction at the Department of Otolaryngology – HNS, the Catholic University of Korea, Seoul, from May 2003 to July 2008, were reviewed. Enrolment criteria included the availability of a CT scan at 3–4 and 11–13 months postoperatively. Twenty-two patients were excluded because of a history of tumor recurrence after treatment or the absence of follow up CT scans. The study population therefore consisted of 18 patients. All free flap reconstructions were performed by the same surgeon (the last author). Speech and swallowing analyses were completed on average 21.6 months after the operation (range: 12–65 months). The Institutional Review Board of the Seoul St. Mary’s Hospital (Seoul) approved this retrospective review of medical records. 2.2. CT image acquisition Routine neck CT scans were performed using a SOMATOM Volume ZoomTM (Siemens, Forchheim, Germany) in spiral mode. Technical factors were; 120 kV, 240 mA, 3 mm slice thickness, and 1 s scanning time. The field of view used was 215 215 mm, and this resulted in a 512 512 matrix. Imaging data were stored in a DICOM (Digital Imaging and Communication in Medicine) file, imported to a personal computer, and then using 3D-DOCTOR software (Able Software Corp, 5 Appletree Lane, Lexington, MA), we reconstructed 3-D images in accordance with anatomic boundaries (Fig. 1). The window widths and centers were varied, depending on the type of tissue being examined. 2.3. Flap volume measurements The maximum diameter of each reconstructed tongue on CT images was determined using the software and a mouse controlled cursor. In each case, the flap borders of the reconstructed tongue were traced manually on the screen using a mouse-controlled cursor on an axial image. The software then generated a 3D model and directly calculated reconstructed tongue volume. 2.4. Speech intelligibility assessment A speech-language pathologist assessed the word and sentence intelligibility using the Korean Urimal Test of Articulation and Phonology1 published by the Korean Academy of SpeechLanguage Pathology and Audiology. The Korean Urimal Test of Articulation and Phonology1 measured the percentage of consonants correct. It was designed on the basis of the Peabody Picture Vocabulary Test – Revised and standardized on Korean. Twentytwo picture cards were used to elicit 43 Korean consonants in word initial syllable, word medial syllable, word final syllable position (Table 1). 2.5. Swallowing assessment Videofluoroscopic images were recorded and analyzed with a KayPentax Digital Swallowing Workstation (model 7200; Kay Pentax, Lincoln Park, NJ). The recordings were completed by a radiologist in the Radiology Department at our hospital. Three consistencies of food were given to each patient: water mixed with liquid barium (Polibar Plus liquid, barium sulfate suspension; Therapex) in a 3:1 ratio presented in a cup; approximately 10 mL of pudding mixed with paste barium (Esobar, barium sulfate cream; Therapex) in a 3:1 ratio presented in a spoon; and one quarter of a digestive cookie coated with barium paste. Two trials of each consistency were consumed while videofluoroscopic recording took place. All patients consumed as many of the 3 consistencies of food as possible, with some consistencies excluded for certain patients because of anatomic constraints
Fig. 1. CT sections of a tongue reconstructed using a radial forearm free flap and 3-D reconstructed radial forearm free flap images; A: axial image, B: reconstructed image at 3 months post-glossectomy, and C: reconstructed image at 12 months.
(i.e., absence of dentition) or clinician perceived clinical risk to the patient. Posterior bolus movement by tongue, inflow of barium into the pharynx before swallowing, tongue base to posterior pharyngeal wall contact, pharyngeal wall contraction, laryngeal elevation, stasis in the epiglottic vallecula, stasis in the oral cavity after swallowing, and laryngeal aspiration, were evaluated. Swallowing
Y.-H. Joo et al. / Auris Nasus Larynx 40 (2013) 303–307
305
Table 1 The grade for consonant articulation was assigned using a picture consonant articulation test. Bilabial plosive [b]
[p]
Alveolar plosive [ph]
[d]
[t]
Velar plosive [th]
[g]
[k]
Fricative [kh]
[s]
Nasal sound [ss]
[h]
[m]
[n]
Liquid sound [h]
[l]
I M F I, initial consonant; M, medial consonant; F, final consonant.
was also assessed quantitatively. Oral transit time and pharyngeal transit time were measured. Oral transit time was defined as the time required for the barium to move through the oral cavity, measured from the first backward movement of the barium until the start of the barium passed the lowest point of the mandibular ramus. Pharyngeal transit time was defined as the time required for the barium to move through the pharynx, measured from the time that the start of the barium passed the lowest point of the mandibular ramus until the end of the barium left the cricopharyngeal region.
radiotherapy was administered to 7 (38.9%) patients. Regarding flap shape, 3 (16.7%) were unilobed free flaps and 15 (83.3%) were multilobed free flaps. Ten (55.6%) patients had resected floor of mouth and eight (44.4%) had tongue base. Mean flap size was 65.4 cm2 (range from 28 to 108 cm2). Ten (55.6%) patients received a sensate flap. The computer-estimated changes in reconstructed flap volumes post-glossectomy between 3 and 12 months scans were 19.2%.
2.6. Statistical analysis
The mean percentages of word and sentence intelligibility were 72.33 15.62% and 61.56 19.65%, respectively. Postoperative free flap volume changes were significantly and negatively correlated with the word and sentence intelligibility (Y = 0.338X + 43.641, r2 = 0.383, p = 0.006 and Y = 0.246X + 34.322, r2 = 0.321, p = 0.014, respectively) (Fig. 2). Floor of mouth resected and postoperative irradiation were significantly correlated with the word and sentence intelligibility (p = 0.027, p = 0.028 and p = 0.003, p = 0.010, respectively). A significant positive correlation was found between word intelligibility and floor of mouth resected (p = 0.027), tongue base resected (p = 0.002), and postoperative irradiation (p = 0.003). A significant positive correlation was found between sentence intelligibility and floor of mouth resected (p = 0.028), postoperative irradiation (p = 0.010). No relation was found between age, gender, primary tumor stage, flap shape, flap size, or a sensate flap and speech intelligibility. In multivariate analysis, there was no significant factor correlated with word and sentence intelligibility.
The t-test was used to identify statistically significant associations among continuous variables. The correlation between function including speech and swallowing and treatment variables was analyzed with Spearman correlation coefficient. Statistical significance was accepted for p values of <0.05. All calculations were performed using SPSS software ver. 13.0 (SPSS, Chicago, IL). 3. Results 3.1. Patients demographics (Table 2) Mean subject age was 54 (range from 30 to 76 years), and there were 14 (77.8%) males and 4 (22.2%) females. Regarding their pathological stages, there were 10 (55.6%) and 8 (44.4%) patients with stage T2 and T3 cancers, respectively. Postoperative Table 2 Demographic profiles of patients with partial glossectomy followed by radial forearm free flap reconstruction. Parameter
No
Age (year) Gender Male Female T stage T2 T3 Floor of mouth resected Yes No Tongue base resected Yes No Postoperative irradiation Yes No Flap shape Unilobed Multilobed Flap size (cm2) Sensate flap Yes No Flap volume change between 3 and 12 months (%)
54 (30–76)
% of the subjects
14 4
77.8 22.2
10 8
55.6 44.4
10 8
55.6 44.4
8 10
44.4 55.6
7 11
38.9 61.1
3 15 65.4 (28–108)
83.3 16.7
10 8 19.2 (3.3–36.9)
55.6 44.4
3.2. Speech outcomes (Table 3)
3.3. Swallowing outcomes (Table 4) Sixteen (88.9%) patients could eat a normal solid diet, 2 (11.1%) patients were eating a pureed diet. A trend towards correlation was noted between floor of mouth resected, tongue base resected, postoperative irradiation, or postoperative flap volume changes and most of the swallowing variables. Postoperative flap volume changes between 3 and 12 months were correlated with reduced posterior bolus movement by tongue (p = 0.002), reduced tongue base to posterior pharyngeal wall contact (p = 0.002), reduced laryngeal elevation (p = 0.005), increased aspiration (p = 0.005),
Table 3 Variables and their associations with speech outcomes. Parameter
Word intelligibility
Sentence intelligibility
Age Gender T stage Floor of mouth resected Tongue base resected Postoperative irradiation Flap shape Flap size Sensate flap Flap volume change
0.442 0.826 0.534 0.027* 0.002* 0.003* 0.938 0.213 0.127 0.006*
0.964 0.484 0.973 0.028* 0.150 0.010* 0.444 0.101 0.089 0.014*
*
Significant at p < 0.05.
Y.-H. Joo et al. / Auris Nasus Larynx 40 (2013) 303–307
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Fig. 2. Relationship between postoperative flap volume change between 3 and 12 months and speech outcomes; A: word intelligibility (Y = p = 0.006) and B: sentence intelligibility (Y = 0.246X + 34.322, r2 = 0.321, p = 0.014).
0.338X + 43.641, r2 = 0.383,
Table 4 Variables and their associations with swallowing outcomes. Parameter
Posterior bolus movement
Inflow of barium into the pharynx
Tongue base contraction
Pharyngeal wall contraction
Laryngeal elevation
Stasis in vallecula
Stasis in oral cavity
Laryngeal aspiration
Oral transit time
Pharyngeal transit time
Age Gender T stage Floor of mouth resected Tongue base resected Postoperative irradiation Flap shape Flap size Sensate flap Flap volume change
0.689 0.814 0.693 0.013* 0.693 0.073 0.693 0.935 0.018* 0.002*
0.570 0.709 0.104 0.005* 0.017* 0.523 1.000 0.888 0.531 0.452
0.870 0.453 0.531 0.104 0.017* 0.004* 0.201 0.953 0.201 0.002*
0.362 0.888 0.814 0.045* 0.009* 0.002* 0.339 0.571 0.183 0.237
0.284 0.888 0.405 0.045* 0.009* 0.002* 0.339 0.381 0.814 0.005*
0.061 0.453 0.104 0.104 0.017* 0.097 0.201 0.479 0.531 0.171
0.065 0.709 0.755 0.104 0.000* 0.097 0.201 0.200 0.755 0.569
0.284 0.888 0.405 0.045* 0.009* 0.002* 0.339 0.381 0.814 0.005*
0.224 0.179 0.440 0.065 0.075 0.000* 0.661 0.101 0.827 0.010*
0.484 0.686 0.259 0.119 0.095 0.010* 0.681 0.675 0.803 0.011*
*
Significant at p < 0.05.
and delayed oral (p = 0.010) and pharyngeal transit time (p = 0.011). Multivariate analysis failed to identify any factor that affected swallowing variables. 4. Discussion The ultimate goal of tongue reconstruction is to duplicate the form and function of the normal part. However, the complexity of the anatomy and the sophistication of available reconstructive techniques interact to provide a realistic definition of those goals. Free-flap reconstruction allows a wider tumor resection and adaptation of flap to defect, to minimize tethering of remaining structures. The multiple factors beyond the control of reconstructive surgeons when attempting to rehabilitate a patient following partial glossectomy, as described by Urken et al. are: (1) the quantity of residual tongue following ablation, (2) the integrity of the motor and sensory nerve supply to residual tissue, (3) the degree of scarring and fibrosis of the residual tongue musculature following surgery and radiation, and (4) a multitude of other patient factors, such as, age, medical condition, and motivation, which have a tremendous impact on the extent of rehabilitation [8]. According to previous reports, large reconstructed tongues have better functional outcomes in terms of swallowing function and speech intelligibility [1,10,11,13]. Therefore, to supplement an assumed volume contraction and enlarge flap volume, flaps that
are larger and thicker than actual defects should be designed. Kimata et al. suggested that wider and thicker flaps, designed to be approximately 20–30% larger than the actual defects, should be used for reconstruction of the tongue after glossectomy [14]. Yun et al. recommended overcorrection with sufficient flap volume to improve oral intake owing following flap volume loss caused by postoperative radiotherapy [15]. We previously reported that the computer-determined change in reconstructed RFFF volumes between 3 months and 5 years was 42.7% and postoperative irradiation was correlated with free flap volume changes [12]. In the present study, average percentage volume changes between 3 and 12 months post-glossectomy were 19.2%. We investigated the changes in the volume of reconstructed tongues and their functional outcomes such as swallowing and speech function in patients with partial tongue defects. Patients who had small flap volume loss from 3 to 12 months had better swallowing and speech. We attribute these results to the fact that the flap adds bulk to the tongue. In addition, many other factors were involved in swallowing and speech outcomes after glossectomy with reconstruction using RFFF, such as floor of mouth resected, tongue base resected, postoperative irradiation, and sensory innervations in similar to several previous studies [16–19]. In a multivariate analysis, however, these clinical factors were not found to have any significance in the swallowing and speech functions after glossectomy in the current study. There are two possible
Y.-H. Joo et al. / Auris Nasus Larynx 40 (2013) 303–307
explanations for this result. First, the sample size of glossectomy patients with reconstruction using RFFF was relatively small to draw a statistically significant power in the multivariate analysis. Second, it is likely that postoperative flap volume changes between 3 and 12 months was not found to be significant because a 1-year period may not be enough time in which to assess the ultimate flap volume change. Nowadays we reconstructed the partial glossectomy defect with RFFF at least 40% larger in volume than the actual defect. Furthermore, in cases with floor of mouth resected, and tongue base resected, and postoperative irradiation our findings indicate that more over sizing is needed. The present study has some limitations that should be mentioned. The main limitation was the retrospective analysis. Second limitation was the small number of patients recruited with a follow up CT scan after tongue reconstruction. Third, the resected tongue volumes were not equally distributed. Lastly, the median follow-up time of this study was rather short. Accordingly, we suggest that an additional prospective investigation be conducted in a larger number of patients. 5. Conclusion Our results indicate that reconstructed RFFF volume after partial glossectomy was found to reduce with time and postoperative speech and swallowing outcomes is related to the volume changes of the reconstructed tongue. Conflict of interest None. References [1] Hirano M, Kuroiwa Y, Tanaka S, Matsuoka H, Sato K, Yoshida T. Dysphagia following various degrees of surgical resection for oral cancer. Ann Otol Rhinol Laryngol 1992;101:138–41. [2] McConnel FM, Logemann JA, Rademaker AW, Pauloski BR, Baker SR, Lewin J, et al. Surgical variable affecting postoperative swallowing efficiency in oral cancer patients: a pilot study. Laryngoscope 1994;104:87–90. [3] Fujimoto Y, Hasegawa Y, Nakayama B, Matsuura H. Usefulness and limitation of cricopharyngeal myotomy and laryngeal suspension after wide resection of the tongue or oropharynx. Nippon Jibiinkoka Gakkai Kaiho 1998;101:307–11.
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[4] Gagnebin J, Jaques B, Pasche P. Reconstruction of the anterior floor of mouth by surgical flap microanastomosis: oncologic and functional results. Schweiz Med Wochenschr Suppl 2000;116:39–42. [5] Haribhakti V, Kavarana NM, Tibrewala AN. Oral cavity reconstruction: an objective assessment of function. Head Neck 1993;15:119–24. [6] Mah SM, Durham JS, Anderson DW, Irvine RA, Chow C, Fache JS, et al. Functional results in oral cavity reconstruction using reinnervated versus nonreinnervated free fasciocutaneous grafts. J Otolaryngol 1996;25: 75–81. [7] Salibian AH, Allison GR, Armstrong WB, Krugman ME, Strelzow VV, Kelly T, et al. Functional hemitongue reconstruction with microvascular ulnar forearm flap. Plast Reconstr Surg 1999;104:654–60. [8] Urken ML, Moscoso JF, Lawson W, Biller HF. A systematic approach to functional reconstruction of the oral cavity following partial and total glossectomy. Arch Otolaryngol Head Neck Surg 1994;120:589–601. [9] Salibian AH, Allison GR, Strezow VV, Krugman ME, Rappaport I, McMicken BL, et al. Secondary microvascular tongue reconstruction: functional results. Head Neck 1993;15:389–97. [10] Fredrickson JM, Haughey BH. The latissimus dorsi donor site. Current use in head and neck reconstruction. Arch Otolaryngol Head Neck Surg 1991;117:1129–34. [11] Yamamoto Y, Sugihara T, Furuta Y, Fukuda S. Functional reconstruction of the tongue and deglutition muscles following extensive resection of tongue cancer. Plast Reconstr Surg 1998;102:993–8. [12] Joo YH, Hwang SH, Sun DI, Park JO, Cho KJ, Kim MS. Assessment of volume changes of radial forearm free flaps in head and neck cancer: long-term results. Oral Oncol 2011;47:72–5. [13] Yanai C, Kikutani T, Adachi M, Thoren H, Suzuki M, Iizuka T. Functional outcome after total and subtotal glossectomy with free flap reconstruction. Head Neck 2008;30:909–18. [14] Kimata Y, Sakuraba M, Hishinuma S, Ebihara S, Hayashi R, Asakage T, et al. Analysis of the relations between the shape of the reconstructed tongue and postoperative functions after subtotal or total glossectomy. Laryngoscope 2003;113:905–9. [15] Yun IS, Lee DW, Lee WJ, Lew DH, Choi EC, Rah DK. Correlation of neotongue volume changes with functional outcomes after long-term follow-up of total glossectomy. J Craniofac Surg 2010;21:111–6. [16] Brown L, Rieger JM, Harris J, Seikaly H. A longitudinal study of functional outcomes after surgical resection and microvascular reconstruction for oral cancer: tongue mobility and swallowing function. J Oral Maxillofac Surg 2010;68:2690–700. [17] Pauloski BR, Logemann JA, Colangelo LA, Rademaker AW, McConnel FM, Heiser MA, et al. Surgical variables affecting speech in treated patients with oral and oropharyngeal cancer. Laryngoscope 1998;108:908–16. [18] Pauloski BR, Rademaker AW, Logemann JA, Rademaker AW, McConnel FM, Heiser MA, et al. Surgical variables affecting swallowing in patients treated for oral/oropharyngeal cancer. Head Neck 2004;26: 625–36. [19] Archontaki M, Athanasiou A, Stavrianos SD, Korkolis DP, Faratzis G, Papadopoulou F, et al. Functional results of speech and swallowing after oral microvascular free flap reconstruction. Eur Arch Otorhinolaryngol 2010;267: 1771–7.
Contents lists available at SciVerse ScienceDirect
Auris Nasus Larynx journal homepage: www.elsevier.com/locate/anl
Functional outcome after partial glossectomy with reconstruction using radial forearm free flap Young-Hoon Joo, Se-Hwan Hwang, Jun-Ook Park, Kwang-Jae Cho, Min-Sik Kim * Department of Otolaryngology – Head and Neck Surgery, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea
A R T I C L E I N F O
A B S T R A C T
Article history: Received 23 April 2012 Accepted 14 July 2012 Available online 10 August 2012
Objective: The purpose of this study was to investigate the relationship between the radial forearm free flap (RFFF) volume changes and speech and swallowing outcomes. Methods: The study included 18 subjects with squamous cell carcinoma of the oral tongue. Results: Average percentage changes in flap volume between 3 and 12 months was 19.2%. Postoperative free flap volume changes were significantly and negatively correlated with the word and sentence intelligibility (Y = 0.338X + 43.641, r2 = 0.383, p = 0.006 and Y = 0.246X + 34.322, r2 = 0.321, p = 0.014, respectively). A significant positive correlation was also found between word and sentence intelligibility and floor of mouth resected, postoperative irradiation. Postoperative flap volume changes between 3 and 12 months were correlated with reduced posterior bolus movement by tongue (p = 0.002), reduced tongue base to posterior pharyngeal wall contact (p = 0.002), reduced laryngeal elevation (p = 0.005), increased aspiration (p = 0.005), delayed oral (p = 0.010) and pharyngeal transit time (p = 0.011). Floor of mouth resected, tongue base resected, and postoperative irradiation also influenced the swallowing outcomes. Conclusions: This study shows that postoperative flap volume changes are significantly related to speech and swallowing outcomes in patients undergoing partial glossectomy reconstructed with RFFF. ß 2012 Elsevier Ireland Ltd. All rights reserved.
Keywords: Surgical flaps Organ size Computer-assisted image processing Tongue Treatment outcome
1. Introduction Restoration of function following glossectomy is one of the great remaining challenges for head and neck reconstructive surgeons. The extent of surgical resection, particularly, the amount of oral tongue and tongue base resected, has been implicated as the primary correlate of swallowing impairment in postsurgical oral and oropharyngeal cancer patients [1–4]. Some studies have suggested that swallowing function depends on the method of reconstruction rather than on the degree of resection [5–7]. The principal goal of tongue reconstruction is to re-establish the functions of speech, mastication, and swallowing, and thus, microvascular tissue transfer has been regularly employed since the 1990s. The advantages of microvascular reconstruction of the tongue are; freedom of flap placement without tethering, the possibility of bone reconstruction, and the possibility to model and design the desired form [8]. It is now recognized that immediate reconstruction at the time of tumor resection optimizes functional results [9]. Furthermore, because the volume of the reconstructed tongue affects functional outcomes,
* Corresponding author at: Department of Otolaryngology – HNS, 505 Banpodong Seochogu Seoul St. Mary’s Hospital, The Catholic University of Korea, Seoul 137-040, Republic of Korea. Tel.: +82 2 2258 6211; fax: +82 2 595 1354. E-mail addresses: [email protected], [email protected] (M.-S. Kim). 0385-8146/$ – see front matter ß 2012 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.anl.2012.07.012
such as, swallowing function and speech intelligibility, changes observed in the neotongue after a long-term follow-up require investigation [1,10,11]. As we previously reported, overcorrection with a 40% greater radial forearm free flap (RFFF) volume is recommended for the reconstruction of tumor-related defects in the head and neck [12]. RFFF is the most commonly used sensate flap in the head and neck. The thin, pliable nature of the fasciocutaneous flaps is ideally suited for head and neck reconstructions, especially when the defect involves multiple sites, such as the pharyngeal wall, soft palate, and tongue base. In our experience, reconstruction with the RFFF is a safe and effective method associated with the restoration of the functional outcome among patients undergoing partial glossectomy. The purpose of this study was to estimate postoperative RFFF volume changes and evaluate the relationship between free flap volume changes and speech and swallowing functions in patients after partial glossectomy. 2. Materials and methods 2.1. Patient population The clinical and pathological data of 40 consecutive patients diagnosed with tongue cancer that underwent partial glossectomy
304
Y.-H. Joo et al. / Auris Nasus Larynx 40 (2013) 303–307
followed by RFFF reconstruction at the Department of Otolaryngology – HNS, the Catholic University of Korea, Seoul, from May 2003 to July 2008, were reviewed. Enrolment criteria included the availability of a CT scan at 3–4 and 11–13 months postoperatively. Twenty-two patients were excluded because of a history of tumor recurrence after treatment or the absence of follow up CT scans. The study population therefore consisted of 18 patients. All free flap reconstructions were performed by the same surgeon (the last author). Speech and swallowing analyses were completed on average 21.6 months after the operation (range: 12–65 months). The Institutional Review Board of the Seoul St. Mary’s Hospital (Seoul) approved this retrospective review of medical records. 2.2. CT image acquisition Routine neck CT scans were performed using a SOMATOM Volume ZoomTM (Siemens, Forchheim, Germany) in spiral mode. Technical factors were; 120 kV, 240 mA, 3 mm slice thickness, and 1 s scanning time. The field of view used was 215 215 mm, and this resulted in a 512 512 matrix. Imaging data were stored in a DICOM (Digital Imaging and Communication in Medicine) file, imported to a personal computer, and then using 3D-DOCTOR software (Able Software Corp, 5 Appletree Lane, Lexington, MA), we reconstructed 3-D images in accordance with anatomic boundaries (Fig. 1). The window widths and centers were varied, depending on the type of tissue being examined. 2.3. Flap volume measurements The maximum diameter of each reconstructed tongue on CT images was determined using the software and a mouse controlled cursor. In each case, the flap borders of the reconstructed tongue were traced manually on the screen using a mouse-controlled cursor on an axial image. The software then generated a 3D model and directly calculated reconstructed tongue volume. 2.4. Speech intelligibility assessment A speech-language pathologist assessed the word and sentence intelligibility using the Korean Urimal Test of Articulation and Phonology1 published by the Korean Academy of SpeechLanguage Pathology and Audiology. The Korean Urimal Test of Articulation and Phonology1 measured the percentage of consonants correct. It was designed on the basis of the Peabody Picture Vocabulary Test – Revised and standardized on Korean. Twentytwo picture cards were used to elicit 43 Korean consonants in word initial syllable, word medial syllable, word final syllable position (Table 1). 2.5. Swallowing assessment Videofluoroscopic images were recorded and analyzed with a KayPentax Digital Swallowing Workstation (model 7200; Kay Pentax, Lincoln Park, NJ). The recordings were completed by a radiologist in the Radiology Department at our hospital. Three consistencies of food were given to each patient: water mixed with liquid barium (Polibar Plus liquid, barium sulfate suspension; Therapex) in a 3:1 ratio presented in a cup; approximately 10 mL of pudding mixed with paste barium (Esobar, barium sulfate cream; Therapex) in a 3:1 ratio presented in a spoon; and one quarter of a digestive cookie coated with barium paste. Two trials of each consistency were consumed while videofluoroscopic recording took place. All patients consumed as many of the 3 consistencies of food as possible, with some consistencies excluded for certain patients because of anatomic constraints
Fig. 1. CT sections of a tongue reconstructed using a radial forearm free flap and 3-D reconstructed radial forearm free flap images; A: axial image, B: reconstructed image at 3 months post-glossectomy, and C: reconstructed image at 12 months.
(i.e., absence of dentition) or clinician perceived clinical risk to the patient. Posterior bolus movement by tongue, inflow of barium into the pharynx before swallowing, tongue base to posterior pharyngeal wall contact, pharyngeal wall contraction, laryngeal elevation, stasis in the epiglottic vallecula, stasis in the oral cavity after swallowing, and laryngeal aspiration, were evaluated. Swallowing
Y.-H. Joo et al. / Auris Nasus Larynx 40 (2013) 303–307
305
Table 1 The grade for consonant articulation was assigned using a picture consonant articulation test. Bilabial plosive [b]
[p]
Alveolar plosive [ph]
[d]
[t]
Velar plosive [th]
[g]
[k]
Fricative [kh]
[s]
Nasal sound [ss]
[h]
[m]
[n]
Liquid sound [h]
[l]
I M F I, initial consonant; M, medial consonant; F, final consonant.
was also assessed quantitatively. Oral transit time and pharyngeal transit time were measured. Oral transit time was defined as the time required for the barium to move through the oral cavity, measured from the first backward movement of the barium until the start of the barium passed the lowest point of the mandibular ramus. Pharyngeal transit time was defined as the time required for the barium to move through the pharynx, measured from the time that the start of the barium passed the lowest point of the mandibular ramus until the end of the barium left the cricopharyngeal region.
radiotherapy was administered to 7 (38.9%) patients. Regarding flap shape, 3 (16.7%) were unilobed free flaps and 15 (83.3%) were multilobed free flaps. Ten (55.6%) patients had resected floor of mouth and eight (44.4%) had tongue base. Mean flap size was 65.4 cm2 (range from 28 to 108 cm2). Ten (55.6%) patients received a sensate flap. The computer-estimated changes in reconstructed flap volumes post-glossectomy between 3 and 12 months scans were 19.2%.
2.6. Statistical analysis
The mean percentages of word and sentence intelligibility were 72.33 15.62% and 61.56 19.65%, respectively. Postoperative free flap volume changes were significantly and negatively correlated with the word and sentence intelligibility (Y = 0.338X + 43.641, r2 = 0.383, p = 0.006 and Y = 0.246X + 34.322, r2 = 0.321, p = 0.014, respectively) (Fig. 2). Floor of mouth resected and postoperative irradiation were significantly correlated with the word and sentence intelligibility (p = 0.027, p = 0.028 and p = 0.003, p = 0.010, respectively). A significant positive correlation was found between word intelligibility and floor of mouth resected (p = 0.027), tongue base resected (p = 0.002), and postoperative irradiation (p = 0.003). A significant positive correlation was found between sentence intelligibility and floor of mouth resected (p = 0.028), postoperative irradiation (p = 0.010). No relation was found between age, gender, primary tumor stage, flap shape, flap size, or a sensate flap and speech intelligibility. In multivariate analysis, there was no significant factor correlated with word and sentence intelligibility.
The t-test was used to identify statistically significant associations among continuous variables. The correlation between function including speech and swallowing and treatment variables was analyzed with Spearman correlation coefficient. Statistical significance was accepted for p values of <0.05. All calculations were performed using SPSS software ver. 13.0 (SPSS, Chicago, IL). 3. Results 3.1. Patients demographics (Table 2) Mean subject age was 54 (range from 30 to 76 years), and there were 14 (77.8%) males and 4 (22.2%) females. Regarding their pathological stages, there were 10 (55.6%) and 8 (44.4%) patients with stage T2 and T3 cancers, respectively. Postoperative Table 2 Demographic profiles of patients with partial glossectomy followed by radial forearm free flap reconstruction. Parameter
No
Age (year) Gender Male Female T stage T2 T3 Floor of mouth resected Yes No Tongue base resected Yes No Postoperative irradiation Yes No Flap shape Unilobed Multilobed Flap size (cm2) Sensate flap Yes No Flap volume change between 3 and 12 months (%)
54 (30–76)
% of the subjects
14 4
77.8 22.2
10 8
55.6 44.4
10 8
55.6 44.4
8 10
44.4 55.6
7 11
38.9 61.1
3 15 65.4 (28–108)
83.3 16.7
10 8 19.2 (3.3–36.9)
55.6 44.4
3.2. Speech outcomes (Table 3)
3.3. Swallowing outcomes (Table 4) Sixteen (88.9%) patients could eat a normal solid diet, 2 (11.1%) patients were eating a pureed diet. A trend towards correlation was noted between floor of mouth resected, tongue base resected, postoperative irradiation, or postoperative flap volume changes and most of the swallowing variables. Postoperative flap volume changes between 3 and 12 months were correlated with reduced posterior bolus movement by tongue (p = 0.002), reduced tongue base to posterior pharyngeal wall contact (p = 0.002), reduced laryngeal elevation (p = 0.005), increased aspiration (p = 0.005),
Table 3 Variables and their associations with speech outcomes. Parameter
Word intelligibility
Sentence intelligibility
Age Gender T stage Floor of mouth resected Tongue base resected Postoperative irradiation Flap shape Flap size Sensate flap Flap volume change
0.442 0.826 0.534 0.027* 0.002* 0.003* 0.938 0.213 0.127 0.006*
0.964 0.484 0.973 0.028* 0.150 0.010* 0.444 0.101 0.089 0.014*
*
Significant at p < 0.05.
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Fig. 2. Relationship between postoperative flap volume change between 3 and 12 months and speech outcomes; A: word intelligibility (Y = p = 0.006) and B: sentence intelligibility (Y = 0.246X + 34.322, r2 = 0.321, p = 0.014).
0.338X + 43.641, r2 = 0.383,
Table 4 Variables and their associations with swallowing outcomes. Parameter
Posterior bolus movement
Inflow of barium into the pharynx
Tongue base contraction
Pharyngeal wall contraction
Laryngeal elevation
Stasis in vallecula
Stasis in oral cavity
Laryngeal aspiration
Oral transit time
Pharyngeal transit time
Age Gender T stage Floor of mouth resected Tongue base resected Postoperative irradiation Flap shape Flap size Sensate flap Flap volume change
0.689 0.814 0.693 0.013* 0.693 0.073 0.693 0.935 0.018* 0.002*
0.570 0.709 0.104 0.005* 0.017* 0.523 1.000 0.888 0.531 0.452
0.870 0.453 0.531 0.104 0.017* 0.004* 0.201 0.953 0.201 0.002*
0.362 0.888 0.814 0.045* 0.009* 0.002* 0.339 0.571 0.183 0.237
0.284 0.888 0.405 0.045* 0.009* 0.002* 0.339 0.381 0.814 0.005*
0.061 0.453 0.104 0.104 0.017* 0.097 0.201 0.479 0.531 0.171
0.065 0.709 0.755 0.104 0.000* 0.097 0.201 0.200 0.755 0.569
0.284 0.888 0.405 0.045* 0.009* 0.002* 0.339 0.381 0.814 0.005*
0.224 0.179 0.440 0.065 0.075 0.000* 0.661 0.101 0.827 0.010*
0.484 0.686 0.259 0.119 0.095 0.010* 0.681 0.675 0.803 0.011*
*
Significant at p < 0.05.
and delayed oral (p = 0.010) and pharyngeal transit time (p = 0.011). Multivariate analysis failed to identify any factor that affected swallowing variables. 4. Discussion The ultimate goal of tongue reconstruction is to duplicate the form and function of the normal part. However, the complexity of the anatomy and the sophistication of available reconstructive techniques interact to provide a realistic definition of those goals. Free-flap reconstruction allows a wider tumor resection and adaptation of flap to defect, to minimize tethering of remaining structures. The multiple factors beyond the control of reconstructive surgeons when attempting to rehabilitate a patient following partial glossectomy, as described by Urken et al. are: (1) the quantity of residual tongue following ablation, (2) the integrity of the motor and sensory nerve supply to residual tissue, (3) the degree of scarring and fibrosis of the residual tongue musculature following surgery and radiation, and (4) a multitude of other patient factors, such as, age, medical condition, and motivation, which have a tremendous impact on the extent of rehabilitation [8]. According to previous reports, large reconstructed tongues have better functional outcomes in terms of swallowing function and speech intelligibility [1,10,11,13]. Therefore, to supplement an assumed volume contraction and enlarge flap volume, flaps that
are larger and thicker than actual defects should be designed. Kimata et al. suggested that wider and thicker flaps, designed to be approximately 20–30% larger than the actual defects, should be used for reconstruction of the tongue after glossectomy [14]. Yun et al. recommended overcorrection with sufficient flap volume to improve oral intake owing following flap volume loss caused by postoperative radiotherapy [15]. We previously reported that the computer-determined change in reconstructed RFFF volumes between 3 months and 5 years was 42.7% and postoperative irradiation was correlated with free flap volume changes [12]. In the present study, average percentage volume changes between 3 and 12 months post-glossectomy were 19.2%. We investigated the changes in the volume of reconstructed tongues and their functional outcomes such as swallowing and speech function in patients with partial tongue defects. Patients who had small flap volume loss from 3 to 12 months had better swallowing and speech. We attribute these results to the fact that the flap adds bulk to the tongue. In addition, many other factors were involved in swallowing and speech outcomes after glossectomy with reconstruction using RFFF, such as floor of mouth resected, tongue base resected, postoperative irradiation, and sensory innervations in similar to several previous studies [16–19]. In a multivariate analysis, however, these clinical factors were not found to have any significance in the swallowing and speech functions after glossectomy in the current study. There are two possible
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explanations for this result. First, the sample size of glossectomy patients with reconstruction using RFFF was relatively small to draw a statistically significant power in the multivariate analysis. Second, it is likely that postoperative flap volume changes between 3 and 12 months was not found to be significant because a 1-year period may not be enough time in which to assess the ultimate flap volume change. Nowadays we reconstructed the partial glossectomy defect with RFFF at least 40% larger in volume than the actual defect. Furthermore, in cases with floor of mouth resected, and tongue base resected, and postoperative irradiation our findings indicate that more over sizing is needed. The present study has some limitations that should be mentioned. The main limitation was the retrospective analysis. Second limitation was the small number of patients recruited with a follow up CT scan after tongue reconstruction. Third, the resected tongue volumes were not equally distributed. Lastly, the median follow-up time of this study was rather short. Accordingly, we suggest that an additional prospective investigation be conducted in a larger number of patients. 5. Conclusion Our results indicate that reconstructed RFFF volume after partial glossectomy was found to reduce with time and postoperative speech and swallowing outcomes is related to the volume changes of the reconstructed tongue. Conflict of interest None. References [1] Hirano M, Kuroiwa Y, Tanaka S, Matsuoka H, Sato K, Yoshida T. Dysphagia following various degrees of surgical resection for oral cancer. Ann Otol Rhinol Laryngol 1992;101:138–41. [2] McConnel FM, Logemann JA, Rademaker AW, Pauloski BR, Baker SR, Lewin J, et al. Surgical variable affecting postoperative swallowing efficiency in oral cancer patients: a pilot study. Laryngoscope 1994;104:87–90. [3] Fujimoto Y, Hasegawa Y, Nakayama B, Matsuura H. Usefulness and limitation of cricopharyngeal myotomy and laryngeal suspension after wide resection of the tongue or oropharynx. Nippon Jibiinkoka Gakkai Kaiho 1998;101:307–11.
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