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Factors affecting volume change of myocutaneous flaps in oral cancer
YIJOM-3408; No of Pages 5
Int. J. Oral Maxillofac. Surg. 2016; xxx: xxx–xxx http://dx.doi.org/10.1016/j.ijom.2016.04.014, available online at http://www.sciencedirect.com
Clinical Paper Reconstructive Surgery
Factors affecting volume change of myocutaneous flaps in oral cancer A. Hiraki, T. Yamamoto, R. Yoshida, M. Nagata, K. Kawahara, Y. Nakagawa, Y. Matsuoka, T. Tanaka, A. Hirosue, D. Fukuma, T. Ikebe, M. Shinohara, H. Nakayama: Factors affecting volume change of myocutaneous flaps in oral cancer. Int. J. Oral Maxillofac. Surg. 2016; xxx: xxx–xxx. # 2016 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
Abstract. After oral cancer resection with flap reconstruction, the volume of the flap decreases over time. The purpose of this study was to estimate the volume change in myocutaneous flaps and to identify the clinical factors associated with this volume decrease. Postoperative computed tomography scans and magnetic resonance images of 30 patients, obtained at 1, 6, and 12 months after oral cancer resection with myocutaneous flap reconstruction, were reviewed retrospectively. Changes in the volume of the flaps over time were assessed. The residual flap ratio was calculated using the flap volume at 1 month after reconstruction as the denominator. The residual ratios in relation to clinical factors were compared at 6 and 12 months using the Student t-test. Overall, the flap residual ratio was 78.1% (range 64.1– 93.9%) at 6 months and 71.4% (range 48.8–87.2%) at 12 months. Hypertension, diabetes mellitus, and postoperative radiotherapy were significantly associated with volume changes at 6 months, and postoperative infection and decreased serum albumin levels were associated with volume changes at both 6 months (P = 0.015 and P = 0.001, respectively) and 12 months (P = 0.026 and P = 0.017, respectively). Flap reconstruction must be performed with postoperative flap atrophy in mind in order to preserve optimum speech and swallowing function.
Tissue defects after the resection of oral cancer have a major effect on speech and swallowing and on cosmetic appearance, all of which contribute greatly to postoperative quality of life.1–7 Currently, free flaps and pedicle flaps are used widely for reconstruction after the resection of oral cancer, and reconstructive procedures appropriate for each case can be selected. Myocutaneous flaps including the rectus 0901-5027/000001+05
abdominis myocutaneous (RAM) flap, pectoralis major myocutaneous (PMMC) flap, and latissimus dorsi myocutaneous (LDM) flap are frequently used for the restoration of large tissue defects.7 A flap of optimal volume is very important for swallowing function and speech intelligibility. Flap volume is known to decrease gradually over time due to muscle atrophy, infection, radiation, and the
A. Hiraki1, T. Yamamoto2, R. Yoshida2, M. Nagata2, K. Kawahara2, Y. Nakagawa2, Y. Matsuoka2, T. Tanaka2, A. Hirosue2, D. Fukuma2, T. Ikebe1, M. Shinohara2,3, H. Nakayama2 1
Section of Oral Oncology, Department of Oral and Maxillofacial Surgery, Fukuoka Dental College, Fukuoka, Japan; 2 Department of Oral and Maxillofacial Surgery, Sensory and Motor Organ Sciences, Faculty of Life Sciences, Kumamoto University, Kumamoto, Japan; 3Itoh DentoMaxillofacial Hospital, Kumamoto, Japan
Keywords: oral cancer; reconstruction; myocutaneous flap; volume change; latissimus dorsi myocutaneous flap; pectoralis major myocutaneous flap; rectus abdominis myocutaneous flap; residual ratio. Accepted for publication 21 April 2016
patient’s nutritional status.8–11 Therefore, it is important to select the type and volume of myocutaneous flap for reconstruction under the assumption of an eventual volume decrease. Although studies have compared different types of flaps, such as the RAM flap, forearm flap, and anterolateral thigh (ALT) flap, none of these studies appears to have investigated three myocutaneous flaps alone.
# 2016 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Hiraki A, et al. Factors affecting volume change of myocutaneous flaps in oral cancer, Int J Oral Maxillofac Surg (2016), http://dx.doi.org/10.1016/j.ijom.2016.04.014
YIJOM-3408; No of Pages 5
Hiraki et al.
A retrospective study was performed to investigate the long-term volume changes in myocutaneous flaps after oral cancer resection with flap reconstruction and to determine the clinical factors with the greatest effect on the volume decrease. Materials and methods Patient characteristics
The cases of 30 patients treated for oral cancer with resection and myocutaneous flap reconstruction in the department of oral and maxillofacial surgery of a university hospital in Kumamoto between 2004 and 2013 were reviewed retrospectively. Twenty-one of the patients were men and nine were women. Their mean age was 64.1 years (range 28–83 years). Cases of local and regional recurrence were excluded. The primary site was the tongue in 11 patients, the lower gingiva in 10, the upper gingiva in two, the buccal mucosa in three, the oral floor in three, and the hard palate in one. The histopathological diagnosis was squamous cell carcinoma in 28 cases and adenoid cystic carcinoma in two. A RAM flap was used in 10 patients, a PMMC flap in 10, and a LDM flap in 10. Clinical characteristics including the tumour and node classifications and the pathological stage are summarized in Table 1. In all cases, the same operator at the same hospital performed the tumour resection, neck dissection, and myocutaneous flap reconstruction.
Measurements
The patients underwent a routine computed tomography (CT) examination at 1, 5– 7, and 11–13 months (1, 6, and 12 months) to monitor for the recurrence of oral cancer. Magnetic resonance imaging (MRI) was performed as needed. The CT scans were performed using an Aquilion ONE scanner (Toshiba Medical Systems, Tochigi, Japan) and the MRI using an Achieva 3T scanner (Philips, Amsterdam, Netherlands) with a slice interval of <3 mm. The areas of the RAM, PMMC, and LDM flaps were calculated on each axial CT slice and the flap volume was then measured by integration using Quest/ ViewC software (Yokogawa Medical Solutions Corporation, Tokyo) at the three time points. For greater accuracy, detailed information was gathered from the operator on the extent of resection, and the CT values of the boundary line were used. Furthermore, the MRI data were referred to. The area of measurement was above the body of the hyoid bone, and the residual volume ratios
Table 1. Patient characteristics. n or mean (range)
Characteristic Sex Male Female Age, years Flap type Rectus abdominis myocutaneous flap Pectoralis major myocutaneous flap Latissimus dorsi myocutaneous flap Primary site Tongue Lower gingiva Upper gingiva Buccal mucosa Oral floor Hard palate T classification T2 T3 T4 N classification N0 N1 N2b N2c Pathological stage III IVA
21 9 64.1 (28–83) 10
history of postoperative infection, and postoperative radiotherapy. The serum albumin level was classified into two groups depending on whether it increased or decreased compared with the preoperative value. A postoperative infection was considered to be present in cases where a purulent discharge from the transplanted flap persisted for longer than 1 month.
10 Statistical analysis
10
All statistical analyses were performed using JMP 9 statistical software (SAS Institute Inc., Cary, NC, USA). Residual ratios at 6 and 12 months according to the clinical factors were compared using the Student t-test. A P-value of <0.05 indicated statistical significance.
11 10 2 3 3 1
Results
1 8 21 5 5 18 2 2 28
T, tumour; N, node.
at 6 and 12 months were calculated using the 1-month value as the denominator. Three double-blind measurements were performed for each CT image by three experienced clinicians and the average value was used in the analysis. Clinical factors
The associations of clinical factors with the volume change were also examined, including sex, age, flap type, hypertension, diabetes mellitus, smoking habit, body mass index (BMI), serum albumin level,
Residual rao (%)
2
The mean reconstruction volume for the 30 cases was 60.1 cm3 (range 18.9– 136.3 cm3). The overall residual ratio was 78.1% (range 64.1–93.9%) at 6 months and 71.4% (range 48.8–87.2%) at 12 months (Fig. 1). The correlations between the volume change of the flaps and clinical factors are shown in Table 2. The residual ratio at 6 months was significantly lower in patients with hypertension (81.7% vs. 75.3%, P = 0.016), diabetes mellitus (88.9% vs. 76.9%, P = 0.006), and a history of postoperative radiotherapy (68.8% vs. 79.1%, P = 0.019), and the residual ratio was also significantly lower in patients with a history of postoperative infection than in those without at both 6 months (70.9% vs. 79.5%, P = 0.015) and 12 months (58.8% vs. 73.9%, P = 0.001) (Fig. 2). For patients with increased vs. decreased serum albumin levels, the residual ratio at 6 months was 82.0% vs. 75.6% (P = 0.026) and at 12 months was 77.4% vs. 67.8% (P = 0.017) (Fig. 3). Thus, a
100 95 90 85 80 75 70 65 60 55 50 1 month
6 months
12 months
Fig. 1. Overall residual ratio. The overall residual ratio was 78.1% at 6 months (n = 30) and 71.4% at 12 months (n = 30). Error bars represent the standard deviation.
Please cite this article in press as: Hiraki A, et al. Factors affecting volume change of myocutaneous flaps in oral cancer, Int J Oral Maxillofac Surg (2016), http://dx.doi.org/10.1016/j.ijom.2016.04.014
YIJOM-3408; No of Pages 5
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Volume change of myocutaneous flaps Table 2. Clinical parameters affecting flap volume change. Parameter
n
Total Sex Male Female Age, years <65 65 Flap type RAM PMMC LDM Hypertension Yes No Diabetes mellitus Yes No Smoking status Smoker Non-smoker BMI, kg/m2 <25 25 Albumin (6 months/12 months) D Alb 0 D Alb < 0 Postoperative infection Yes No Postoperative radiotherapy Yes No
30
Volume at 1 month, cm 3 60.1
Residual ratio at 6 months
P-value
78.1%
Residual ratio at 12 months 71.4%
0.258 21 9
66.4 45.6
78.7% 76.7%
14 16
63.5 57.2
79.1% 77.2%
10 10 10
63.5 46.0 70.9
79.9% 78.9% 75.4%
13 17
54.2 64.7
81.7% 75.3%
3 27
71.4 58.9
88.9% 76.9%
13 17
56.5 63.0
81.1% 75.8%
27 3
59.9 62.2
77.6% 82.3%
11/10 17/16
54.0/55.2 63.7/62.6
82.0% 75.6%
5 25
82.8 55.6
70.9% 79.5%
3 27
75.6 58.4
68.8% 79.1%
P-value 0.700
70.8% 72.9% 0.501
0.848 71.8% 71.1%
0.382
0.237 74.9% 72.0% 67.3%
0.016
0.076 75.2% 68.6%
0.006
0.155 79.3% 70.5%
0.052
0.113 74.8% 68.9%
0.309
0.794 71.3% 72.9%
0.026
0.017 77.4% 67.8%
0.015
0.001 58.8% 73.9%
0.019
0.114 62.7% 72.4%
RAM, rectus abdominis myocutaneous flap; PMMC, pectoralis major myocutaneous flap; LDM, latissimus dorsi myocutaneous flap; BMI, body mass index; Alb, serum albumin level.
history of postoperative infection and reduced serum albumin levels were both associated with increased rates of postoperative flap volume reduction at 6 and 12 months. In terms of the flap type, the residual ratios for RAM, PMMC, and LDM flaps were 79.9% vs. 78.9% vs. 75.4% at 6 months (P = 0.382) and
74.9% vs. 72.0% vs. 67.3% at 12 months (P = 0.237). Discussion
Flap volume is known to decrease over time after the resection of oral cancer with reconstruction.6,8–13 This progressive
Fig. 2. Residual ratio in patients with a history of postoperative infection. The residual ratios at 6 months and 12 months in patients with (solid line, n = 5) and without (dotted line, n = 25) a postoperative infection are shown. Error bars represent the standard deviation.
change in volume may lead to swallowing and speech dysfunction, reduced calorie intake, and aspiration pneumonia. Therefore, it is important to select the type and volume of the reconstruction flap with this volume decrease in mind. In this study, the volume change over time was estimated for three types of myocutaneous flap (RAM, PMMC, and LDM) that are frequently used for the restoration of large defects after the resection of oral cancers. Clinical factors that may influence the volume decrease were identified, namely a history of postoperative infection and reduced serum albumin levels. It is hoped that the results of this study will help with the selection of reconstructive procedures. The results of this study showed an overall residual flap volume of 78.1% at 6 months and 71.4% at 12 months. This is consistent with previous reports. In a series of 17 patients who underwent free flap reconstruction, Yamaguchi et al. reported an overall residual flap volume of approximately 82.2%,7 while Cho et al. reported an overall residual volume of 75.2% for ALT flaps and 89.2% for PMMC flaps,9 and Sakamoto et al. reported an overall
Please cite this article in press as: Hiraki A, et al. Factors affecting volume change of myocutaneous flaps in oral cancer, Int J Oral Maxillofac Surg (2016), http://dx.doi.org/10.1016/j.ijom.2016.04.014
YIJOM-3408; No of Pages 5
4
Hiraki et al.
Fig. 3. Residual ratio according to serum albumin levels. The residual ratios at (A) 6 months and (B) 12 months in patients with increased (solid line, n = 11 and n = 10, respectively) and decreased (dotted line, n = 17 and n = 16, respectively) serum albumin levels are shown. Error bars represent the standard deviation.
residual volume of 76.9% for RAM flaps.10 The postoperative decrease in flap volume is primarily attributed to muscle atrophy,8–12 which is generally due to denervation, ischaemia, oedema, inflammation, wound tension, and a long-term reduction in calorie intake.9,10 Creating anastomoses with motor nerves in the donor area is an effective means of preventing muscle atrophy.7 The fat volume in the flap may increase or decrease depending on the individual’s dietary and health condition.5,9,14 There have been very few studies on the clinical factors influencing the change in flap volume. Cho et al. did not find any correlation between sex, age, smoking status, alcohol consumption, hypertension, diabetes mellitus, or postoperative radiotherapy and the change in flap volume after ALT or PMMC flap reconstruction, and only the flap type was significantly related to the flap volume change.9 Similarly, in the present study, sex, age, and smoking status were not related to the changes in flap
volume at 6 or 12 months, although hypertension and diabetes mellitus did show a significant correlation with the volume change at 6 months. On reviewing the flap type, the residual ratio at 6 and 12 months was greatest for the RAM flap, followed by the PMMC flap and then the LDM flap. Although there was no significant difference according to the flap type, RAM flaps, which have better perfusion and more fatty tissue, maintained a greater volume. Radiotherapy resulted in a statistically significant decrease in the residual ratio at 6 months, but there was no significant effect at 12 months. The relationship between changes post-radiotherapy and changes in flap volume remains controversial.9–11,13–16 Further studies with larger patient populations will be necessary to resolve this issue. Several other authors have examined the relationship between the patient’s nutritional status and flap volume.9–11 Although Yamaguchi et al. reported a trend towards an association between flap volume and
BMI, the correlation was not statistically significant.7 In the present study, when the flap volume was examined in terms of increased or decreased serum albumin levels after surgery, a significant association between albumin levels and flap volume was found at both 6 months (P = 0.026) and 12 months (P = 0.017) postoperatively. This suggests that the patient’s nutritional state can have a major effect on the maintenance of flap volume. Moreover, as noted, flap volume was significantly reduced at both 6 and 12 months in patients with a history of postoperative infection at the site of reconstruction. With regard to the measurement method, MRI is superior to CT for distinguishing between the original tissue and the transplanted myocutaneous flap. In this study, additional measures were taken to increase the accuracy of distinguishing between the two. First, detailed information about the extent of resection was gathered from the operator. Second, CT values of the boundary line were measured in comparison with those on the preoperative CT images. Third, the MRI data were referred to. (In the authors’ department, patients are examined by CT to monitor the recurrence of oral cancer once every 3 months and MRI is performed as needed.) Lastly, the measurement area was restricted to the region above the body of the hyoid bone to reduce error. This study identified several clinical factors associated with an increased loss of flap volume over time after resection of oral cancer with myocutaneous flap reconstruction. However, there may be confounding factors and other underlying factors, such as the small sample size. In this study, these factors that may influence flap volume change were not investigated. Further investigations over a longer study period, with a larger number of patients and with a prospective randomized study design will be required to confirm these results and to determine the impact of flap volume loss on speech and swallowing function. Funding
This study received no funding. Competing interests
There are no conflicts of interest to declare. Ethical approval
This retrospective study and the clinical record reviews were approved by the
Please cite this article in press as: Hiraki A, et al. Factors affecting volume change of myocutaneous flaps in oral cancer, Int J Oral Maxillofac Surg (2016), http://dx.doi.org/10.1016/j.ijom.2016.04.014
YIJOM-3408; No of Pages 5
Volume change of myocutaneous flaps Institutional Review Board of Kumamoto University (No. 1021). Patient consent
6.
Written informed consent for inclusion in the study was obtained from all participants. Acknowledgements. We would like to thank Editage (http://www.editage.jp) for the English language editing.
7.
8.
References 1. Urken ML, Moscoso JF, Lawson W, Biller H. A systematic approach to functional reconstruction of the oral cavity following partial and total glossectomy. Arch Otolaryngol Head Neck Surg 1994;120:589–601. 2. 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. 3. 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. 4. 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. 5. Sakuraba M, Asano T, Miyamoto S, Hayashi R, Yamazaki M, Miyazaki M, et al. A new
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flap design for tongue reconstruction after total or subtotal glossectomy in thin patients. J Plast Reconstr Aesthet Surg 2009;62: 795–9. Yun IS, Lee DW, Lee WJ, Lew DH, Choi EC, Rah DK. Correlation of neotongue volume changes with functional outcomes after longterm follow-up of total glossectomy. J Craniofac Surg 2010;21:111–6. Yamaguchi K, Kimata Y, Onoda S, Mizukawa N, Onoda T. Quantitative analysis of free flap volume changes in head and neck reconstruction. Head Neck 2012;34:1403–7. Fujioka M, Masuda K, Imamura Y. Fatty tissue atrophy of free flap used for head and neck reconstruction. Microsurgery 2011;31:32–5. Cho KJ, Joo YH, Sun DI, Kim MS. Perioperative clinical factors affecting volume changes of reconstructed flaps in head and neck cancer patients: free versus regional flaps. Eur Arch Otorhinolaryngol 2011;268: 1061–5. Sakamoto Y, Takahara T, Ota Y, Aoki T, Yamazaki H, Otsuru M, et al. MRI analysis of chronological changes in free-flap volume in head and neck reconstruction by volumetry. Tokai J Exp Clin Med 2014;39:44–50. Chatterjee JS, Lee A, Anderson W, Baker L, Stevenson JH, Dewar JA, et al. Effect of postoperative radiotherapy on autologous deep inferior epigastric perforator flap volume after immediate breast reconstruction. Br J Surg 2009;96:1135–40. Shin YS, Koh YW, Kim SH, Jeong JH, Ahn S, Hong HJ, et al. Radiotherapy deteriorates postoperative functional outcome after partial
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glossectomy with free flap reconstruction. J Oral Maxillofac Surg 2012;70:216–20. Bittermann G, Tho¨nissen P, Poxleitner P, Zimmerer R, Vach K, Metzger MC. Microvascular transplants in head and neck reconstruction: 3D evaluation of volume loss. J Craniomaxillofac Surg 2015;43:1319–24. Mucke T, Rau A, Weitz J, Ljubic A, Rohleder N, Wolff KD, et al. Influence of irradiation and oncologic surgery on head and neck microsurgical reconstructions. Oral Oncol 2012;48:367–71. Higgins KM, Erovic BM, Ravi A, Yeung R, Lee JW, Yao C, et al. Volumetric changes of the anterolateral thigh free flap following adjuvant radiotherapy in total parotidectomy reconstruction. Laryngoscope 2012; 122:767–72. Steel BJ, Cope MR. A brief history of vascularized free flaps in the oral and maxillofacial region. J Oral Maxillofac Surg 2015;73:786. e1-786.e11.
Address: Akimitsu Hiraki Section of Oral Oncology Department of Oral and Maxillofacial Surgery Fukuoka Dental College 2-15-1 Tamura Sawara-ku Fukuoka 814-0193 Japan Tel.: +81 92 801 0411 Fax: +81 92 801 1288 E-mail: [email protected]
Please cite this article in press as: Hiraki A, et al. Factors affecting volume change of myocutaneous flaps in oral cancer, Int J Oral Maxillofac Surg (2016), http://dx.doi.org/10.1016/j.ijom.2016.04.014
Int. J. Oral Maxillofac. Surg. 2016; xxx: xxx–xxx http://dx.doi.org/10.1016/j.ijom.2016.04.014, available online at http://www.sciencedirect.com
Clinical Paper Reconstructive Surgery
Factors affecting volume change of myocutaneous flaps in oral cancer A. Hiraki, T. Yamamoto, R. Yoshida, M. Nagata, K. Kawahara, Y. Nakagawa, Y. Matsuoka, T. Tanaka, A. Hirosue, D. Fukuma, T. Ikebe, M. Shinohara, H. Nakayama: Factors affecting volume change of myocutaneous flaps in oral cancer. Int. J. Oral Maxillofac. Surg. 2016; xxx: xxx–xxx. # 2016 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
Abstract. After oral cancer resection with flap reconstruction, the volume of the flap decreases over time. The purpose of this study was to estimate the volume change in myocutaneous flaps and to identify the clinical factors associated with this volume decrease. Postoperative computed tomography scans and magnetic resonance images of 30 patients, obtained at 1, 6, and 12 months after oral cancer resection with myocutaneous flap reconstruction, were reviewed retrospectively. Changes in the volume of the flaps over time were assessed. The residual flap ratio was calculated using the flap volume at 1 month after reconstruction as the denominator. The residual ratios in relation to clinical factors were compared at 6 and 12 months using the Student t-test. Overall, the flap residual ratio was 78.1% (range 64.1– 93.9%) at 6 months and 71.4% (range 48.8–87.2%) at 12 months. Hypertension, diabetes mellitus, and postoperative radiotherapy were significantly associated with volume changes at 6 months, and postoperative infection and decreased serum albumin levels were associated with volume changes at both 6 months (P = 0.015 and P = 0.001, respectively) and 12 months (P = 0.026 and P = 0.017, respectively). Flap reconstruction must be performed with postoperative flap atrophy in mind in order to preserve optimum speech and swallowing function.
Tissue defects after the resection of oral cancer have a major effect on speech and swallowing and on cosmetic appearance, all of which contribute greatly to postoperative quality of life.1–7 Currently, free flaps and pedicle flaps are used widely for reconstruction after the resection of oral cancer, and reconstructive procedures appropriate for each case can be selected. Myocutaneous flaps including the rectus 0901-5027/000001+05
abdominis myocutaneous (RAM) flap, pectoralis major myocutaneous (PMMC) flap, and latissimus dorsi myocutaneous (LDM) flap are frequently used for the restoration of large tissue defects.7 A flap of optimal volume is very important for swallowing function and speech intelligibility. Flap volume is known to decrease gradually over time due to muscle atrophy, infection, radiation, and the
A. Hiraki1, T. Yamamoto2, R. Yoshida2, M. Nagata2, K. Kawahara2, Y. Nakagawa2, Y. Matsuoka2, T. Tanaka2, A. Hirosue2, D. Fukuma2, T. Ikebe1, M. Shinohara2,3, H. Nakayama2 1
Section of Oral Oncology, Department of Oral and Maxillofacial Surgery, Fukuoka Dental College, Fukuoka, Japan; 2 Department of Oral and Maxillofacial Surgery, Sensory and Motor Organ Sciences, Faculty of Life Sciences, Kumamoto University, Kumamoto, Japan; 3Itoh DentoMaxillofacial Hospital, Kumamoto, Japan
Keywords: oral cancer; reconstruction; myocutaneous flap; volume change; latissimus dorsi myocutaneous flap; pectoralis major myocutaneous flap; rectus abdominis myocutaneous flap; residual ratio. Accepted for publication 21 April 2016
patient’s nutritional status.8–11 Therefore, it is important to select the type and volume of myocutaneous flap for reconstruction under the assumption of an eventual volume decrease. Although studies have compared different types of flaps, such as the RAM flap, forearm flap, and anterolateral thigh (ALT) flap, none of these studies appears to have investigated three myocutaneous flaps alone.
# 2016 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Hiraki A, et al. Factors affecting volume change of myocutaneous flaps in oral cancer, Int J Oral Maxillofac Surg (2016), http://dx.doi.org/10.1016/j.ijom.2016.04.014
YIJOM-3408; No of Pages 5
Hiraki et al.
A retrospective study was performed to investigate the long-term volume changes in myocutaneous flaps after oral cancer resection with flap reconstruction and to determine the clinical factors with the greatest effect on the volume decrease. Materials and methods Patient characteristics
The cases of 30 patients treated for oral cancer with resection and myocutaneous flap reconstruction in the department of oral and maxillofacial surgery of a university hospital in Kumamoto between 2004 and 2013 were reviewed retrospectively. Twenty-one of the patients were men and nine were women. Their mean age was 64.1 years (range 28–83 years). Cases of local and regional recurrence were excluded. The primary site was the tongue in 11 patients, the lower gingiva in 10, the upper gingiva in two, the buccal mucosa in three, the oral floor in three, and the hard palate in one. The histopathological diagnosis was squamous cell carcinoma in 28 cases and adenoid cystic carcinoma in two. A RAM flap was used in 10 patients, a PMMC flap in 10, and a LDM flap in 10. Clinical characteristics including the tumour and node classifications and the pathological stage are summarized in Table 1. In all cases, the same operator at the same hospital performed the tumour resection, neck dissection, and myocutaneous flap reconstruction.
Measurements
The patients underwent a routine computed tomography (CT) examination at 1, 5– 7, and 11–13 months (1, 6, and 12 months) to monitor for the recurrence of oral cancer. Magnetic resonance imaging (MRI) was performed as needed. The CT scans were performed using an Aquilion ONE scanner (Toshiba Medical Systems, Tochigi, Japan) and the MRI using an Achieva 3T scanner (Philips, Amsterdam, Netherlands) with a slice interval of <3 mm. The areas of the RAM, PMMC, and LDM flaps were calculated on each axial CT slice and the flap volume was then measured by integration using Quest/ ViewC software (Yokogawa Medical Solutions Corporation, Tokyo) at the three time points. For greater accuracy, detailed information was gathered from the operator on the extent of resection, and the CT values of the boundary line were used. Furthermore, the MRI data were referred to. The area of measurement was above the body of the hyoid bone, and the residual volume ratios
Table 1. Patient characteristics. n or mean (range)
Characteristic Sex Male Female Age, years Flap type Rectus abdominis myocutaneous flap Pectoralis major myocutaneous flap Latissimus dorsi myocutaneous flap Primary site Tongue Lower gingiva Upper gingiva Buccal mucosa Oral floor Hard palate T classification T2 T3 T4 N classification N0 N1 N2b N2c Pathological stage III IVA
21 9 64.1 (28–83) 10
history of postoperative infection, and postoperative radiotherapy. The serum albumin level was classified into two groups depending on whether it increased or decreased compared with the preoperative value. A postoperative infection was considered to be present in cases where a purulent discharge from the transplanted flap persisted for longer than 1 month.
10 Statistical analysis
10
All statistical analyses were performed using JMP 9 statistical software (SAS Institute Inc., Cary, NC, USA). Residual ratios at 6 and 12 months according to the clinical factors were compared using the Student t-test. A P-value of <0.05 indicated statistical significance.
11 10 2 3 3 1
Results
1 8 21 5 5 18 2 2 28
T, tumour; N, node.
at 6 and 12 months were calculated using the 1-month value as the denominator. Three double-blind measurements were performed for each CT image by three experienced clinicians and the average value was used in the analysis. Clinical factors
The associations of clinical factors with the volume change were also examined, including sex, age, flap type, hypertension, diabetes mellitus, smoking habit, body mass index (BMI), serum albumin level,
Residual rao (%)
2
The mean reconstruction volume for the 30 cases was 60.1 cm3 (range 18.9– 136.3 cm3). The overall residual ratio was 78.1% (range 64.1–93.9%) at 6 months and 71.4% (range 48.8–87.2%) at 12 months (Fig. 1). The correlations between the volume change of the flaps and clinical factors are shown in Table 2. The residual ratio at 6 months was significantly lower in patients with hypertension (81.7% vs. 75.3%, P = 0.016), diabetes mellitus (88.9% vs. 76.9%, P = 0.006), and a history of postoperative radiotherapy (68.8% vs. 79.1%, P = 0.019), and the residual ratio was also significantly lower in patients with a history of postoperative infection than in those without at both 6 months (70.9% vs. 79.5%, P = 0.015) and 12 months (58.8% vs. 73.9%, P = 0.001) (Fig. 2). For patients with increased vs. decreased serum albumin levels, the residual ratio at 6 months was 82.0% vs. 75.6% (P = 0.026) and at 12 months was 77.4% vs. 67.8% (P = 0.017) (Fig. 3). Thus, a
100 95 90 85 80 75 70 65 60 55 50 1 month
6 months
12 months
Fig. 1. Overall residual ratio. The overall residual ratio was 78.1% at 6 months (n = 30) and 71.4% at 12 months (n = 30). Error bars represent the standard deviation.
Please cite this article in press as: Hiraki A, et al. Factors affecting volume change of myocutaneous flaps in oral cancer, Int J Oral Maxillofac Surg (2016), http://dx.doi.org/10.1016/j.ijom.2016.04.014
YIJOM-3408; No of Pages 5
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Volume change of myocutaneous flaps Table 2. Clinical parameters affecting flap volume change. Parameter
n
Total Sex Male Female Age, years <65 65 Flap type RAM PMMC LDM Hypertension Yes No Diabetes mellitus Yes No Smoking status Smoker Non-smoker BMI, kg/m2 <25 25 Albumin (6 months/12 months) D Alb 0 D Alb < 0 Postoperative infection Yes No Postoperative radiotherapy Yes No
30
Volume at 1 month, cm 3 60.1
Residual ratio at 6 months
P-value
78.1%
Residual ratio at 12 months 71.4%
0.258 21 9
66.4 45.6
78.7% 76.7%
14 16
63.5 57.2
79.1% 77.2%
10 10 10
63.5 46.0 70.9
79.9% 78.9% 75.4%
13 17
54.2 64.7
81.7% 75.3%
3 27
71.4 58.9
88.9% 76.9%
13 17
56.5 63.0
81.1% 75.8%
27 3
59.9 62.2
77.6% 82.3%
11/10 17/16
54.0/55.2 63.7/62.6
82.0% 75.6%
5 25
82.8 55.6
70.9% 79.5%
3 27
75.6 58.4
68.8% 79.1%
P-value 0.700
70.8% 72.9% 0.501
0.848 71.8% 71.1%
0.382
0.237 74.9% 72.0% 67.3%
0.016
0.076 75.2% 68.6%
0.006
0.155 79.3% 70.5%
0.052
0.113 74.8% 68.9%
0.309
0.794 71.3% 72.9%
0.026
0.017 77.4% 67.8%
0.015
0.001 58.8% 73.9%
0.019
0.114 62.7% 72.4%
RAM, rectus abdominis myocutaneous flap; PMMC, pectoralis major myocutaneous flap; LDM, latissimus dorsi myocutaneous flap; BMI, body mass index; Alb, serum albumin level.
history of postoperative infection and reduced serum albumin levels were both associated with increased rates of postoperative flap volume reduction at 6 and 12 months. In terms of the flap type, the residual ratios for RAM, PMMC, and LDM flaps were 79.9% vs. 78.9% vs. 75.4% at 6 months (P = 0.382) and
74.9% vs. 72.0% vs. 67.3% at 12 months (P = 0.237). Discussion
Flap volume is known to decrease over time after the resection of oral cancer with reconstruction.6,8–13 This progressive
Fig. 2. Residual ratio in patients with a history of postoperative infection. The residual ratios at 6 months and 12 months in patients with (solid line, n = 5) and without (dotted line, n = 25) a postoperative infection are shown. Error bars represent the standard deviation.
change in volume may lead to swallowing and speech dysfunction, reduced calorie intake, and aspiration pneumonia. Therefore, it is important to select the type and volume of the reconstruction flap with this volume decrease in mind. In this study, the volume change over time was estimated for three types of myocutaneous flap (RAM, PMMC, and LDM) that are frequently used for the restoration of large defects after the resection of oral cancers. Clinical factors that may influence the volume decrease were identified, namely a history of postoperative infection and reduced serum albumin levels. It is hoped that the results of this study will help with the selection of reconstructive procedures. The results of this study showed an overall residual flap volume of 78.1% at 6 months and 71.4% at 12 months. This is consistent with previous reports. In a series of 17 patients who underwent free flap reconstruction, Yamaguchi et al. reported an overall residual flap volume of approximately 82.2%,7 while Cho et al. reported an overall residual volume of 75.2% for ALT flaps and 89.2% for PMMC flaps,9 and Sakamoto et al. reported an overall
Please cite this article in press as: Hiraki A, et al. Factors affecting volume change of myocutaneous flaps in oral cancer, Int J Oral Maxillofac Surg (2016), http://dx.doi.org/10.1016/j.ijom.2016.04.014
YIJOM-3408; No of Pages 5
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Hiraki et al.
Fig. 3. Residual ratio according to serum albumin levels. The residual ratios at (A) 6 months and (B) 12 months in patients with increased (solid line, n = 11 and n = 10, respectively) and decreased (dotted line, n = 17 and n = 16, respectively) serum albumin levels are shown. Error bars represent the standard deviation.
residual volume of 76.9% for RAM flaps.10 The postoperative decrease in flap volume is primarily attributed to muscle atrophy,8–12 which is generally due to denervation, ischaemia, oedema, inflammation, wound tension, and a long-term reduction in calorie intake.9,10 Creating anastomoses with motor nerves in the donor area is an effective means of preventing muscle atrophy.7 The fat volume in the flap may increase or decrease depending on the individual’s dietary and health condition.5,9,14 There have been very few studies on the clinical factors influencing the change in flap volume. Cho et al. did not find any correlation between sex, age, smoking status, alcohol consumption, hypertension, diabetes mellitus, or postoperative radiotherapy and the change in flap volume after ALT or PMMC flap reconstruction, and only the flap type was significantly related to the flap volume change.9 Similarly, in the present study, sex, age, and smoking status were not related to the changes in flap
volume at 6 or 12 months, although hypertension and diabetes mellitus did show a significant correlation with the volume change at 6 months. On reviewing the flap type, the residual ratio at 6 and 12 months was greatest for the RAM flap, followed by the PMMC flap and then the LDM flap. Although there was no significant difference according to the flap type, RAM flaps, which have better perfusion and more fatty tissue, maintained a greater volume. Radiotherapy resulted in a statistically significant decrease in the residual ratio at 6 months, but there was no significant effect at 12 months. The relationship between changes post-radiotherapy and changes in flap volume remains controversial.9–11,13–16 Further studies with larger patient populations will be necessary to resolve this issue. Several other authors have examined the relationship between the patient’s nutritional status and flap volume.9–11 Although Yamaguchi et al. reported a trend towards an association between flap volume and
BMI, the correlation was not statistically significant.7 In the present study, when the flap volume was examined in terms of increased or decreased serum albumin levels after surgery, a significant association between albumin levels and flap volume was found at both 6 months (P = 0.026) and 12 months (P = 0.017) postoperatively. This suggests that the patient’s nutritional state can have a major effect on the maintenance of flap volume. Moreover, as noted, flap volume was significantly reduced at both 6 and 12 months in patients with a history of postoperative infection at the site of reconstruction. With regard to the measurement method, MRI is superior to CT for distinguishing between the original tissue and the transplanted myocutaneous flap. In this study, additional measures were taken to increase the accuracy of distinguishing between the two. First, detailed information about the extent of resection was gathered from the operator. Second, CT values of the boundary line were measured in comparison with those on the preoperative CT images. Third, the MRI data were referred to. (In the authors’ department, patients are examined by CT to monitor the recurrence of oral cancer once every 3 months and MRI is performed as needed.) Lastly, the measurement area was restricted to the region above the body of the hyoid bone to reduce error. This study identified several clinical factors associated with an increased loss of flap volume over time after resection of oral cancer with myocutaneous flap reconstruction. However, there may be confounding factors and other underlying factors, such as the small sample size. In this study, these factors that may influence flap volume change were not investigated. Further investigations over a longer study period, with a larger number of patients and with a prospective randomized study design will be required to confirm these results and to determine the impact of flap volume loss on speech and swallowing function. Funding
This study received no funding. Competing interests
There are no conflicts of interest to declare. Ethical approval
This retrospective study and the clinical record reviews were approved by the
Please cite this article in press as: Hiraki A, et al. Factors affecting volume change of myocutaneous flaps in oral cancer, Int J Oral Maxillofac Surg (2016), http://dx.doi.org/10.1016/j.ijom.2016.04.014
YIJOM-3408; No of Pages 5
Volume change of myocutaneous flaps Institutional Review Board of Kumamoto University (No. 1021). Patient consent
6.
Written informed consent for inclusion in the study was obtained from all participants. Acknowledgements. We would like to thank Editage (http://www.editage.jp) for the English language editing.
7.
8.
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Address: Akimitsu Hiraki Section of Oral Oncology Department of Oral and Maxillofacial Surgery Fukuoka Dental College 2-15-1 Tamura Sawara-ku Fukuoka 814-0193 Japan Tel.: +81 92 801 0411 Fax: +81 92 801 1288 E-mail: [email protected]
Please cite this article in press as: Hiraki A, et al. Factors affecting volume change of myocutaneous flaps in oral cancer, Int J Oral Maxillofac Surg (2016), http://dx.doi.org/10.1016/j.ijom.2016.04.014