ORIGINAL ARTICLE

Measurement of the trapezius muscle volume: A new assessment strategy of shoulder dysfunction after neck dissection for the treatment of head and neck cancers Jae-Gu Cho, MD, PhD, Naree Lee, MD, Min-Woo Park, MD, Seung-Kuk Baek, MD, PhD, Soon-Young Kwon, MD, PhD, Kwang-Yoon Jung, MD, PhD, Jeong-Soo Woo, MD, PhD* Department of Otorhinolaryngology–Head and Neck Surgery, Korea University College of Medicine, Seoul, Korea.

Accepted 21 February 2014 Published online 3 April 2014 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/hed.23646

ABSTRACT: Background. The purpose of this study was to determine the actual degree of shoulder muscle change and its relation to symptoms after neck dissection for head and neck cancers. Methods. Forty-two patients who underwent unilateral neck dissection were selected. Data obtained from each subject were trapezius muscle volume ratio and a Shoulder Disability Questionnaire (SDQ) score. Patients who had undergone neck dissection with spinal accessory nerve (SAN) preservation were compared with those who had received radical neck dissection. The preservation group was further separated into subgroups by the extent of neck dissection. Results. Trapezius muscle volume ratio was higher and SDQ score was significantly lower in the SAN preservation group compared to

INTRODUCTION Neck dissection is an important part of the surgical treatment for head and neck cancers, improving the cancer cure rate, and the prognosis. However, complications of neck dissection are common, including shoulder dysfunction, chronic regional pain, cosmetic problem, and paresthesia. Especially shoulder dysfunction, consisting of shoulder pain, limited range of motion, and deformity, is a major complication affecting postoperative quality of life (QOL). It is mainly caused by denervation change of the trapezius muscle innervated by the spinal accessory nerve (SAN), which has a major role in shoulder movement.1 Notwithstanding more conservative approaches, such as modified radical neck dissection (MRND), selective neck dissection (SND), and many other surgical modifications, that have been carried out, some patients still complain of various degrees of shoulder dysfunction.2–4

*Corresponding author: J.-S. Woo, Department of Otorhinolaryngology–Head and Neck Surgery, Guro Hospital, Korea University College of Medicine, 80 Guro-dong, Guro-gu, Seoul 152-703, South Korea. E-mail: [email protected] Contract grant sponsor: This study was supported by a grant of the Korea Health technology R&D Project, Ministry of Health and Welfare, Republic of Korea (A090084).

the radical neck dissection group. However, the SAN preservation subgroups did not differ from each other. In addition, a good correlation between the muscle volume ratio and SDQ score was observed. Conclusion. With trapezius muscle volume ratio, clinicians may be able to diagnose shoulder dysfunction after neck dissection. Further research on the subject is warranted. This suggests a novel strategy for assessing C 2014 Wiley Periodicals, Inc. Head the degree of shoulder dysfunction. V Neck 37: 619–623, 2015

KEY WORDS: muscles, shoulder, dysfunction, neck dissection

A number of studies have been conducted to assess the effect of the SAN injury on shoulder dysfunction after various types of neck dissections. Most were studies using electromyography that found action potentials of the involved shoulder muscles innervated by SAN.3,5–7 As far as we know, few studies of the actual muscle volume change and the relation with shoulder morbidity has been reported. Our study focused on the volume change of the trapezius muscle in the follow-up CT scan of patients with head and neck cancer who received different types of neck dissections in relation to their shoulder dysfunction, as evaluated with a survey.

MATERIALS AND METHODS Forty-two patients with head and neck cancer who underwent unilateral neck dissection from January 2003 to April 2011 were recruited and agreed to participate in this study. None declined participation. The patients who had bilateral neck dissection or recurrences, incomplete medical record, and no postoperative CT scan 1 year after the operation were excluded. Informed consent was obtained from all patients and the study protocols were approved by the Institutional Review Board of Guro Hospital, Korea University (MD12008). Data regarding the patients’ age, sex, primary tumor site, N classification, performed surgery, types of neck dissection, and postoperative radiation therapy (RT) were HEAD & NECK—DOI 10.1002/HED

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TABLE 1. Clinical characteristics of the patients. Characteristic

Age, mean (SD) Sex Male Female Primary site Thyroid Tonsil Tongue Floor of mouth Larynx Submandibular gland Parotid gland Metastasis of unknown origin N classification N0 N1 N2a N2b N2c N3 Method of dissection RND MRND SND Postoperative RT Yes No

No. of patients (%)

55.57 (13.17) 22 (52.4) 20 (47.6) 10 (23.9) 14 (33.3) 7 (16.6) 1 (2.4) 3 (7.1) 2 (4.8) 3 (7.1) 2 (4.8) 8 (19) 17 (40.8) 3 (7.1) 10 (23.9) 4 (9.5) 0 (0) 10 (23.9) 9 (21.4) 23 (54.7) 19 (45.2) 23 (54.8)

Abbreviations: RND, radical neck dissection; MRND, modified radical neck dissection; SND, selective neck dissection; RT, radiation therapy.

collected from their medical records and are described in Table 1. The patients were separated by the types of neck dissection into 2 groups, SAN sacrifice (radical neck dissection [RND]) and the SAN preservation group, and the 2 groups were compared with each other. The SAN preservation group was further separated into MRND and SND subgroups by the extent of neck dissection. These subgroups were compared also. Of each group, 60% from the RND group, 88.9% from the MRND group, and 21.7%% from the SND group had received postoperative RT on their neck. All patients were checked with preoperative CT scan and postoperative CT scan, which was obtained 1 year after the surgery, in accord to the protocol of our institution (Figure 1). Their CT scans were evaluated by a radiologist who was a specialist of the head and neck region. He decided the image numbers showing the upper and lower borders of the trapezius muscles bilaterally. The volume of trapezius muscle was calculated on neck CT, using Picture Archiving and Communication System (PACS, Piview STAR, INFINITT, Korea). One of our authors used free-handed drawing to draw the region of the trapezius muscles on the axial images previously indicated by the radiologist, got an area of the muscle, added the numerical value, and calculated a trapezius muscle volume on each side (Figure 2). The untreated side was used as the control. For the comparison between different types of neck dissection, we used the mean value of the trapezius muscle volume ratio and SD, which is a ratio of the treated to untreated sides. 620

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FIGURE 1. Preoperative (A) and postoperative (B) CT scans showing the trapezius muscle in untreated (white asterisk) and treated (white arrow) sides of the neck. Atrophied trapezius muscle is observed in the treated side (B)

Also, the patients completed the Shoulder Disability Questionnaire (SDQ).8 It consists of 22 items that the patients answered “yes” or “no.” The score ranges from 0 (no disability) to 22 (maximal disability). The minimum

FIGURE 2. An axial CT scan image showing 2 freehanded drawings (white arrows) of the trapezius muscle in both sides of the neck. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

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obtained at times ranging from 1.1 to 9.2 years (median, 5 years) of follow-up. In a comparison of the SAN preservation group and the sacrifice (RND) group, no difference of trapezius muscle volume ratio between the 2 groups in the preoperative CT scan was confirmed (p 5 .415). However, in the postoperative CT scan, the ratio in the SAN preservation group (0.91 6 0.14) was significantly higher than that of the RND group (0.37 6 0.18; p 5 .005). The SDQ score for the SAN preserving group (1.82 6 2.96) was significantly lower (better) than the RND group (10.90 6 4.75; p 5 .008). When we compared the MRND and SND subgroups, there was no significant differences in trapezius volume ratio or SOQ score (Figure 3 and Table 2). The majority of the patients who underwent MRND and SND did not complain about shoulder symptoms. Three patients (9.4%) of the SAN preservation group (MRND and SND) scored above 5 (minimum disability cutoff point score). In contrast, 9 patients (90%) of the SAN sacrifice group (RND) scored above 5. Furthermore, for the sample as a whole, there was a statistically significant correlation between the trapezius muscle volume ratio and SDQ score (Spearman rank correlation coefficient 5 0.591; p < .001).

DISCUSSION FIGURE 3. Trapezius muscle volume ratio (A) and Shoulder Disability Questionnaire (SDQ) score (C) comparing the spinal accessory nerve (SAN) sacrifice group versus the SAN preservation group. Trapezius muscle volume ratio (B) and SDQ score (D) comparing modified radical neck dissection and selective neck dissection subgroups. Numbers are mean values. *p < .05

significant score cutoff point was determined to be 5 points.8 Previous researchers have noted a significant association between the SDQ and a QOL measure.2,9,10 Statistical analyses of data using the 2-tailed test were performed. Wilcoxon rank sum test was used because of the small sample size and non-normal data with SPSS version 19.0 (SPSS, IBM, Chicago, IL). The p values < .05 were considered significant. Additionally, Spearman’s rank correlation coefficient was obtained to evaluate the association between the trapezius muscle volume ratio and the SDQ score.

RESULTS Baseline characteristics and assessments by the types of neck dissection are shown in Table 1. The postoperative shoulder dysfunction assessments (SDQ scores) were

Shoulder dysfunction is one of the most serious morbidities after neck dissection for the treatment of head and neck cancers because of SAN injury. SAN injury results in scapula droop and winged deformity. These morbidities are based on anatomy, in that SAN provides motor innervation from the central nervous system to 2 muscles of the neck: the sternocleidomastoid muscle and the trapezius muscle. Therefore, the 2 muscles can be used to evaluate shoulder dysfunction after neck dissection except in the case of RND, which includes sternocleidomastoid removal. The purpose of this study was to evaluate the influences of SAN injury during different types of neck dissection on postoperative shoulder dysfunction by measuring the trapezius muscle volume from a CT scan and from a questionnaire of shoulder disability. The results showed that the trapezius muscle volume reduction and shoulder dysfunction were significantly less affected in the MRND and SND group compared to those in the RND group. These findings correspond to an earlier study that reported that SAN preservation surgery significantly decreases postoperative shoulder syndrome.11 Concerning methods of evaluating of SAN injury, previous reports have used clinical inspection of shoulder droop or protraction and scapular flaring, physical test of arm abduction or strength and motion tests, goniometric

TABLE 2. Trapezius muscle volume ratio and Shoulder Disability Questionnaire score by type of neck dissection.

Trapezius muscle volume ratio SDQ

SAN sacrifice (RND)

SAN preservation (MRND and SND)

p value

MRND

SND

p value

0.37 (0.18) 10.90 (4.75)

0.91 (0.14) 1.82 (2.96)

.0005 .0008

0.87 (0.14) 2.22 (1.92)

0.94 (0.15) 1.52 (3.14)

.109 .157

Abbreviations: SAN, spinal accessory nerve; RND, radical neck dissection; MRND, modified radical neck dissection; SND, selective neck dissection; SDQ, Shoulder Disability Questionnaire. Data are mean (SD), unless otherwise stated.

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measurement, electromyography of the trapezius or sternocleidomastoid muscle, SAN electroneuronography, and QOL and pain questionnaires.2,3,5,7,10 Even though these methods have fairly reflected the degree of SAN injury, clinical inspection and physical test are subjective and inconsistent. Even though the electromyography, electroneuronography, and goniometric measurement produce objective results, they need extra work over the routine follow-up tests, such as CT or MRI, after head and neck cancer treatment. These shortcomings led our attention to the finding that the trapezius muscle was atrophied and reduced in its volume after neck dissection, especially RND. These changes could be noticed in the routine follow-up imaging tool, CT scan. Hence, we tried to measure the trapezius muscle volume using a software program from the postoperative CT scan for evaluation of the outcomes of the SAN injury. This new evaluation method worked well and was consistent with previous studies.12,13 It provided us with objective, coherent results. Furthermore, it did not require extra time or costs over the routine follow-up tests and needed no needle work. Also, our results showed no difference in the trapezius muscle volume ratio and SDQ score between the MRND and SND subgroups. When the SAN was preserved, patients did not complain of shoulder dysfunction whether neck dissection was extensive or not. Our study conflicts with other studies, which reported shoulder morbidities and decreased electromyography records in the neck dissection including level IIb or V. Erisen et al14 and Heald et al15 reported that even if the SAN was preserved, SAN function was electrophysiologically impaired in all patients who underwent neck dissection, although clinical function was better in the preserved group than in those whose nerve was sacrificed. This discrepancy among studies might originate from the difference of evaluation time after neck dissection. The decreased electromyography activities and shoulder symptoms of the other studies were obtained several weeks or months after neck dissection and recovered in a year or later. Conversely, our result was obtained at least a year after neck dissection. Consequently, SAN manipulating neck dissection could result in temporary muscle weakness caused by neuropraxia of SAN. However, it did not cause nerve degeneration and permanent muscle dysfunction. Overall, careful SAN manipulation and microtrauma during surgery does not seem to influence patients’ perceptions of shoulder problems. In our study, not all patients who had SAN-preserving neck dissection were free from the symptoms of shoulder dysfunction. Three of 32 patients had an SDQ score over 5, suggesting meaningful levels of shoulder dysfunction. Also, K€ oybasioglu et al16 suggested that even if SAN was preserved, temporary or permanent dysfunction of the nerve could result. From these results, we can consider other possible causes of the SAN injury, such as severe traction, excessive skeletonization of the nerve, ischemia, microtrauma, and postoperative fibrosis, or other causes of cervical pain. Therefore, the surgeon should try his or her best to take care of nerve manipulation or handling and dissect meticulously when performing the SANpreserving neck dissections. Likewise, not all patients who sacrificed SAN during RND developed shoulder dysfunction. One of 10 patients 622

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who had RND showed an SDQ score of 1 in this study. Lloyd17 reported not all patients who sacrificed SAN during RND developed shoulder syndrome. These results suggest the possibility that the deltoid muscle also supports the shoulder function. Many earlier studies demonstrated that shoulder syndrome correlates with preserving SAN. There have been relatively fewer reports that studied the trapezius muscle. Because the trapezius muscle is innervated by not only the SAN but also the cervical plexus (C2–C4), the intactness of the cervical plexus, which could be overlooked during neck dissection, must also be considered.18–20 On the contrary, a study demonstrated that the cervical plexus only contributes sensory innervation of the neck and had no negative effect on shoulder pain.21 These findings merit further study. Furthermore, we can conclude that the degree of trapezius muscle atrophy reflects well the degree of shoulder dysfunction perceived by patients based on the statistically significant correlation between the trapezius muscle volume ratio and SDQ score. This suggests that measurement of the trapezius muscle volume change from a follow-up CT scan might be a useful strategy for assessing the degree of shoulder dysfunction of the patients. To our knowledge, this study is the first report that calculates the volume change of the trapezius muscle in relationship to the SAN. However, some limitations of this study bear mention. First, this is not a prospective study. Second, this study is limited by its small sample size. Third, this study did not rule out other possible causes influencing shoulder function, such as intactness of cervical plexus; postoperative RT, or chemotherapy, physical therapy and rehabilitation; or arthritis. Fourth, there might be a source of error in the data because of freehand drawings of axial imaging of CT scans, the possibility of some preoperative asymmetry between the shoulders, and the variability of the time when the SDQ score was obtained according to different follow-up periods. In further study, these factors attributed to shoulder dysfunction, morphologic, and functional change of the trapezius muscle after neck dissection should be included. Large sample sized studies that assess at which points in time changes in trapezius muscle volume are most evident, and how changes in muscle volume might be related to other objective parameters or QOL outcomes would be needed. Despite these limitations, there were some benefits of estimating the degree of shoulder disability of the patients who had neck dissection for head and neck cancer treatment from their postoperative CT scan. Therefore, head and neck surgeons should remember to check the patients’ shoulder disability when they check the locoregional recurrence on the postoperative CT scan.

Acknowledgments The authors thank Dr. Soo-Hyung Lee who assisted with the research and the researchers who participated in this study.

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TRAPEZIUS 3. Cappiello J, Piazza C, Giudice M, De Maria G, Nicolai P. Shoulder disability after different selective neck dissections (levels II–IV versus levels II– V): a comparative study. Laryngoscope 2005;115:259–263. 4. Carr SD, Bowyer D, Cox G. Upper limb dysfunction following selective neck dissection: a retrospective questionnaire study. Head Neck 2009;31: 789–792. 5. Cheng PT, Hao SP, Lin YH, Yeh AR. Objective comparison of shoulder dysfunction after three neck dissection techniques. Ann Otol Rhinol Laryngol 2000;109(8 Pt 1):761–766. 6. Koybas¸ioglu A, Bora Tokc¸aer A, Inal E, Uslu S, Koc¸ak T, Ural A. Accessory nerve function in lateral selective neck dissection with undissected level IIb. ORL J Otorhinolaryngol Relat Spec 2006;68:88–92. 7. Lima LP, Amar A, Lehn CN. Spinal accessory nerve neuropathy following neck dissection. Braz J Otorhinolaryngol 2011;77:259–262. 8. Croft P, Pope D, Zonca M, O’Neill T, Silman A. Measurement of shoulder related disability: results of a validation study. Ann Rheum Dis 1994;53: 525–528. 9. van der Heijden GJ, Leffers P, Bouter LM. Shoulder disability questionnaire design and responsiveness of a functional status measure. J Clin Epidemiol 2000;53:29–38. 10. Stuiver MM, van Wilgen CP, de Boer EM, et al. Impact of shoulder complaints after neck dissection on shoulder disability and quality of life. Otolaryngol Head Neck Surg 2008;139:32–39. 11. Orhan KS, Demirel T, Baslo B, et al. Spinal accessory nerve function after neck dissections. J Laryngol Otol 2007;121:44–48. 12. Umeda M, Shigeta T, Takahashi H, et al. Shoulder mobility after spinal accessory nerve-sparing modified radical neck dissection in oral cancer

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patients. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2010;109: 820–824. Caversaccio M, Negri S, Nolte LP, Zb€aren P. Neck dissection shoulder syndrome: quantification and three-dimensional evaluation with an optoelectronic tracking system. Ann Otol Rhinol Laryngol 2003;112: 939–946. Erisen L, Basel B, Irdesel J, et al. Shoulder function after accessory nervesparing neck dissections. Head Neck 2004;26:967–971. Heald SL, Riddle DL, Lamb RL. The shoulder pain and disability index: the construct validity and responsiveness of a region-specific disability measure. Phys Ther 1997;77:1079–1089. K€ oybasioglu A, Tokcaer AB, Uslu S, Ileri F, Beder L, Ozbilen S. Accessory nerve function after modified radical and lateral neck dissections. Laryngoscope 2000;110:73–77. Lloyd S. Accessory nerve: anatomy and surgical identification. J Laryngol Otol 2007;121:1118–1125. Tubbs RS, Shoja MM, Loukas M, et al. Study of the cervical plexus innervation of the trapezius muscle. J Neurosurg Spine 2011;14:626–629. Selcuk A, Selcuk B, Bahar S, Dere H. Shoulder function in various types of neck dissection. Role of spinal accessory nerve and cervical plexus preservation. Tumori 2008;94:36–39. Pu YM, Tang EY, Yang XD. Trapezius muscle innervation from the spinal accessory nerve and branches of the cervical plexus. Int J Oral Maxillofac Surg 2008;37:567–572. Dilber M, Kasapoglu F, Erisen L, Basut O, Tezel I. The relationship between shoulder pain and damage to the cervical plexus following neck dissection. Eur Arch Otorhinolaryngol 2007;264:1333–1338.

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Measurement of the trapezius muscle volume: A new assessment strategy of shoulder dysfunction after neck dissection for the treatment of head and neck cancers.

The purpose of this study was to determine the actual degree of shoulder muscle change and its relation to symptoms after neck dissection for head and...
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