University of Groningen. Morbidity after neck dissection in head and neck cancer patients Wilgen, Cornelis Paul van

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1 University of Groningen Morbidity after neck dissection in head and neck cancer patients Wilgen, Cornelis Paul van IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2004 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Wilgen, C. P. V. (2004). Morbidity after neck dissection in head and neck cancer patients: a study describing shoulder and neck complaints, and quality of life s.n. Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date:

2 Morbidity after neck dissection in head and neck cancer patients; a study describing shoulder and neck complaints, and quality of life. 1

3 Cover: Steffen van Bergenhenegouwen, Benjamin R. Hol The publication of this thesis was supported by: Nucletron B.V., ABBOTT B.V., Stichting Beatrixoord Noord-Nederland Wilgen, Cornelis Paul Morbidity after neck dissection in head and neck cancer patients; a study describing shoulder and neck complaints, and quality of life. 2

4 RIJKSUNIVERSITEIT GRONINGEN Morbidity after neck dissection in head and neck cancer patients; a study describing shoulder and neck complaints, and quality of life Proefschrift ter verkrijging van het doctoraat in de Medische Wetenschappen aan de Rijksuniversiteit Groningen op gezag van de Rector Magnificus, dr. F. Zwarts, in het openbaar te verdedigen op woensdag 9 juni 2004 om uur door Cornelis Paul van Wilgen geboren op 11 oktober 1967 te Groningen 3

5 Promotor: Prof. dr. J.L.N. Roodenburg Copromotor Dr. P.U. Dijkstra Beoordelingscommissie: Prof. dr. J.H.B. Geertzen Prof. dr. G.J. Hordijk Prof. dr. J.M.K.H. Wierda ISBN:

6 Contents Chapter 1 Pagina 7 Introduction Chapter 2 Pagina 19 Shoulder pain and disability in daily life, following supraomohyoid neck dissection: a pilot study. Journal of Cranio-Maxillofacial Surgery (2003) 31: Chapter 3 Pagina 29 Incidence of shoulder pain after neck dissection: a clinical explorative study for risk factors. Head and Neck (2001) Nov.: Chapter 4 Pagina 45 Shoulder complaints after nerve sparring neck dissection. Int. Journal of Oral and Maxillofacial Surgery (2004),33(3): Chapter 5 Pagina 59 Shoulder complaints after neck dissection; is the spinal accessory nerve involved? British journal of oral and maxillofacial surgery (2003),41:7-11 Chapter 6 Pagina 73 Morbidity of the neck after head and neck cancer therapy. Accepted Head and Neck (december 2003) Contents 5

7 Chapter 7 Pagina 91 Shoulder and neck morbidity in quality of life after surgery for head and neck cancer. Accepted Head and Neck (februari 2004) Chapter 8 Pagina 105 Measuring somatic symptoms with the CES-D to assess depression in cancer patients after treatment, valid or not? (Comparison between patients with head and neck, gynaecological, colo-rectal, and breast cancer) Submitted Chapter 9: General Discussion Pagina 119 Chapter 10: Summary Pagina 125 Samenvattingen Pagina 132 Dankwoord Pagina 139 Appendix 1 and 2 Pagina 142 List of publications Pagina 145 Contents 6

8 CHAPTER 1 INTRODUCTION 7

9 A century after Crile (1906) It is almost a century since Crile 1 described the radical neck dissection for patients with head and neck cancer. In that paper Crile complained about the lack of attention of other physicians concerning the surgical progress in the treatment of head and neck cancer patients. Now, almost one hundred years later, many things have changed. In his historical paper Crile described, as one of the first, the importance of removing lymphatic structures of the neck (the complete lymphatic block or radical neck dissection) in head and neck cancer patients. In great detail he described the anaesthesiology procedures, the surgical techniques, and the sacrificed structures, all illustrated with anatomical sketches. Additionally he described complications like: infections, hemorrhage, shock and collapse. In this same paper an evaluation study was presented in which he compared patients operated with a radical neck dissection (n = 12) to patients in which the lymphatic structures were not removed (n = 48). Patients operated with a radical neck dissection had a survival rate that was four times higher than patients without a radical neck dissection. Crile s paper is one of the keystones of head and neck surgery, the radical neck dissection is still the surgical standard against which various modifications are compared. Crile did not describe morbidity after surgery with radical neck dissection. Sacrificing the accessory nerve was not even mentioned in the text but only explained in one of the sketches as one of the structures to be sacrificed. Almost 50 years after the paper of Crile, Ewing (1952) was one of the first who described morbidity after radical neck dissection. 2 Several types of morbidity were mentioned: disfigurement, pain in the shoulder region, loss of strength, reduced range of motion, loss of function of the shoulder, sensory disturbance, and restrictions in daily activities. Up to 62 % of the patients, operated with a radical neck dissection, had disfigurement of the shoulder and 46 % experienced shoulder pain. Other authors described higher incidences of shoulder complaints after radical neck dissection, even up to 100 %. 3 Shoulder complaints after radical neck dissection are completely attributed to sacrificing of the spinal accessory nerve. The high morbidity rates, and the gained insight in the biological behaviour of various cancer types, to estimate if a tumour has metastasised, led to modifications on the classical radical neck dissection. Bocca (1980) Chapter 1 8

10 described the functional neck dissection 4, later to be called the modified radical neck dissection. 5 In this modified radical neck dissection one or more of the following non-lymphatic structures are preserved: spinal accessory nerve, sternocleidomastoideus muscle, and internal jugular vene. The spinal accessory nerve seemed an important structure to preserve, in order to prevent shoulder morbidity. After modified radical neck dissections, with preservation of the spinal accessory nerve, the prevalence of shoulder complaints decreased, the prevalence rates were 18% to 61%. 6,7 Further modifications in neckdissections were developed by removing only certain levels of lymphatic structures, that are prone to metastasis, instead of removing all levels. Four selective neck dissections (figure 1) are described: supraomohyoid neckdissection (levels I, II, and III), lateral neckdissection (levels II,III, and IV) posterolateral neckdissection (levels II,III,IV,and V), and anterior neckdissection (level VI). 5 In these selective neckdissections all non-lymphatic structures (spinal accessory nerve, sternocleidomastoideus muscle, and internal jugular vene) are preserved. Supraomohyoid neck dissections are often performed in case of oropharyngeal squamous cell carcinoma, with a N0 tumour status and possible sufficient in the treatment of a selected group of patients with positive nodes at level I. 8,9 Figure 1 Classification of levels used for neck dissections (1a). Anatomical structures that cross the cervical lymphatic structures and lymph nodes (1b). Situation after a radical neck dissection (1c). 1 a 1 b 1c (pictures from Mondziekten & Kaakchirurgie, B. Stegenga, A. Vissink, LGM de Bont) Chapter 1 9

11 Recently the classification of Robbins of 1991 has been updated. In this new classification the levels have been further modified. The levels I, II and V have been split into two levels, and are to be called level I a/b, level II a/b and level V a/b. 10 (figure 2) Figure 2 New classification described by Robbins et al Morbidity after selective neck dissections has been described scarcely, and the studies included relatively small samples. 3,11,12 Pinsolle described a group of 41 patients after supraomohyoid neckdissection of which 32% had minor problems, 5 % moderate and 3 % severe shoulder problems. 13 Probably shoulder morbidity rates have decreased further as a result of selective neckdissections, but the evidence is still limited. Shoulder complains after neck dissection Sacrificing the spinal accessory nerve The spinal accessory nerve is a motor nerve, innervating the sternocleidomastoideus muscle and the trapezius muscle. Resection of the spinal accessory nerve leads to denervation of the trapezius muscle. The trapezius muscle exists of an upper, middle and lower part and has two major functions, shrugging the shoulder and stabilising the scapula on the thorax. Paralysis of the trapezius muscle will lead to a lateral gliding of the scapula and a lateral rotation. 14 (figure 3) Chapter 1 10

12 View from above View from behind Figure 3 Lateral rotation of the scapula and changed shoulder joint position As a consequence of the changed scapula position its possibility to move during shoulder movements decreases. As a consequence a reduced range of motion of the shoulder, abduction and forward flexion, appears. (figure 4) A reduced range of motion of the shoulder can cause dysfunction in activities in which the shoulder is needed like lifting heavy objects or reaching above shoulder level. 6,15 Several patients also complain about pain after head and neck cancer treatment. The exact cause of this pain is not properly investigated. Several possible causes have been described like frozen shoulder 16, sternoclavicular joint hypertrophy 17, or myofascial pain as a consequence of stretching of muscles due to the changed scapula position. 18 But these hypothesised causes for shoulder pain have never been investigated properly. Is some cases, after resection of the spinal accessory nerve, the trapezius muscle function remains (partly) intact. This is due to a double innervation by the cervical plexus of the musculus trapezius in about 18% of the patients. 14 Preservation of the spinal accessory nerve Several patients after neck dissection with preservation of the spinal accessory nerve still suffer from shoulder complaints. The mechanisms of the shoulder complaints after modified or selective procedures with sparring of the spinal accessory nerve are unclear. Chapter 1 11

13 Figure 4 Scapula alata as a consequence of trapezius atrophy (4a) and a reduced abduction as a consequence of a changed scapula position (4b). 4a 4b During neck dissection the spinal accessory nerve is lifted from its surrounding structures, and its supplying blood vessels are dissected which may result in a neuropraxia or the nerve may be dissected accidentally which results in a neurotmesis (permanent deficit). In these cases preservation or presumed preservation leads to spinal accessory nerve dysfunction and as a consequence shoulder complaints. But with an intact spinal accessory nerve and trapezius muscle function still shoulder complaints may arise which are interpreted as neuropathic pain or myofascial pain. 19 Unfortunately little research has been done to substantiate these hypothesis whereas it is of great clinical importance for treatment possibilities. More morbidity after head and neck cancer treatment Beside shoulder complaints patients may suffer from other types of morbidity. Little is known about morbidity of the neck after head and neck cancer treatment. Clinically several patients complain about loss of sensation, pain, or a reduced range of motion of the cervical spine. In literature only a few papers describe this morbidity. 19,20,21 These studies are performed on small samples, often without a physical examination. Consequences of neckdissection with or without radiation therapy on range Chapter 1 12

14 of motion of the cervical spine are only described in studies that used questionnaires without actually measuring range of motion. 22 Loss of sensation is thoroughly described in only one study by Saffold, 23 although that study was primarily aiming at the results of the preservation of cervical root branches in selective neck dissections. The influence of radiation therapy on loss of sensation, and range of motion is scarcely described, although clinically patients seem to suffer from fibrosis of soft tissues which decreases range of motion. Pain is probably the most important type of morbidity of patients after head and neck cancer treatment. As mentioned before some hypotheses exist as how to explain post cancer treatment pain. Pain can be explained as neuropathic pain, pain in the clavicular or acromio-clavicular joint (probably nociceptive) and myofacial pain. The causes of pain are still hardly studied but clinically important for treatment modalities. Treatment modalities might be medication, physical therapy, and informing patients. Psychological consequences after head and neck cancer therapy After head and neck cancer treatment also psychological consequences are described. Beside the physical morbidity, psychological as well as social problems have their effect on well being and quality of life. 24 Psychological consequences may be depression, 25 distress, 26 fear of recurrence, 27 inadequate coping strategies 28 problems in reintegration in work and lack of social support. 29 After cancer treatment depression is, with a prevalence of 24 % (range 1.5 % - 50 %), an important psychological morbidity. 30 Depression has a construct in which physical and psychological domains are combined. Depression effects survival, recovery, treatment compliance, pain and quality of life. 31,32 Therefor depression should be assessed adequately in the post treatment phase. 33 Most studies describe psychological morbidity without taking physical morbidity into account. Especially in head and neck cancer patients both factors seem to be related. Therefor more studies are needed in which psychological as well as physical morbidity are analysed. Head and neck cancer and rehabilitation In the Netherlands new patients are yearly diagnosed with cancer. 34 About 10 % of these patients, mostly man, are diagnosed with head and neck cancer. 35 Although mortality rates for head and neck cancer patients are still Chapter 1 13

15 high, through early diagnosis and better treatment possibilities more patients will survive cancer. 36 In the last decade attention has been given to post cancer treatment rehabilitation. 37,38 The last year s treatments are more often multidimensional, aiming on physical and psychological problems. These programs are executed in groups to gain from peer support of fellow cancer patients. 39 Specific physical therapy programs for patients with shoulder complaints after neck dissections are proposed since (appendix 2) Only one study is performed as a controlled trial. 40 Physical therapy programs differ in content and aims. Most programs aim at gaining a full, active and passive, range of motion, strengthening of shoulder muscles to stabilise the shoulder, and training shoulder function in activities in daily life. Besides exercises a physical therapy progam may contain, relaxation or massage. Most programs are developed because of assumed spinal accessory nerve dysfunction. Several authors claim good results, but only the study of Salerno used a control group. 40 She showed that physical therapy can be helpful in the rehabilitation after neck dissection for shoulder complaints. Nevertheless before setting up a program more insight in the exact morbidity after head and neck cancer treatment should be achieved to known where the program should focus on. Aim of our study In this thesis we are aiming at more insight in morbidity after head and neck cancer treatment (resection of the primary tumour, neck dissection and preor post-operative radiation therapy). We will study shoulder complaints and the role of the spinal accessory nerve, pain and the underlying pain mechanisms, range of motion, and loss of sensation. The consequences of dysfunction such as shoulder disability and activities of daily living, but also psychological problems (depression) and quality of life will be analysed. This thesis aims at a better understanding of consequences of type of neck dissection, especially the supraomohyoid neck dissection and the influence of radiation therapy. A better understanding of morbidity after cancer treatment must lead to specific rehabilitation treatment options in the near future. Chapter 1 14

16 References 1. Crile G. Excision of cancer of the head and neck. JAMA 1906;47: Ewing MRMH. Disability following radical neck dissection. Cancer 1952;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: Bocca E, Pignataro O, Sasaki CT. Functional neck dissection. A description of operative technique. Arch.Otolaryngol. 1980;106: Robbins KT, Medina JE, Wolfe GT, Levine PA, Sessions RB, Pruet CW. Standardizing neck dissection terminology. Official report of the Academy's Committee for Head and Neck Surgery and Oncology. Arch.Otolaryngol.Head Neck Surg. 1991;117: Short SO, Kaplan JN, Laramore GE, Cummings CW. Shoulder pain and function after neck dissection with or without preservation of the spinal accessory nerve. Am.J.Surg. 1984;148: Carenfelt C, Eliasson K. Occurrence, duration and prognosis of unexpected accessory nerve paresis in radical neck dissection. Acta Otolaryngol. 1980;90: Medina JE, Byers RM. Supraomohyoid neck dissection: rationale, indications, and surgical technique. Head Neck 1989;11: Kowalski LP, Magrin J, Waksman G, Santo GF, Lopes ME, de Paula RP, Pereira RN, Torloni H. Supraomohyoid neck dissection in the treatment of head and neck tumors. Survival results in 212 cases. Arch.Otolaryngol.Head Neck Surg. 1993;119: Robbins KT, Clayman G, Levine PA, Medina J, Sessions R, Shaha A, Som P, Wolf GT. Neck dissection classification update: revisions proposed by the American Head and Neck Society and the American Academy of Otolaryngology-Head and Neck Surgery. Arch.Otolaryngol.Head Neck Surg. 2002;128: Sobol S, Jensen C, Sawyer W, Costiloe P, Thong N. Objective comparison of physical dysfunction after neck dissection. Am.J.Surg. 1985;150: Leipzig B, Suen JY, English JL, Barnes J, Hooper M. Functional evaluation of the spinal accessory nerve after neck dissection. Am.J.Surg. 1983;146: Chapter 1 15

17 13. Pinsolle V, Michelet V, Majoufre C, Caix P, Siberchicot F, Pinsolle J. [Spinal accessory nerve and lymphatic neck dissection. Rev.Stomatol.Chir.Maxillofac. 1997;98: Krause HR. Shoulder-arm-syndrome after radical neck dissection: its relation with the innervation of the trapezius muscle. Int.J.Oral Maxillofac.Surg. 1992;21: Shone GR, Yardley MP. An audit into the incidence of handicap after unilateral radical neck dissection. J.Laryngol.Otol. 1991;105: Patten C, Hillel AD. The 11th nerve syndrome. Accessory nerve palsy or adhesive capsulitis? Arch.Otolaryngol.Head Neck Surg. 1993;119: Cantlon GE, Gluckman JL. Sternoclavicular joint hypertrophy following radical neck dissection. Head Neck Surg. 1983;5: Nori S, Soo KC, Green RF, Strong EW, Miodownik S. Utilization of intraoperative electroneurography to understand the innervation of the trapezius muscle. Muscle Nerve 1997;20: Sist T, Miner M, Lema M. Characteristics of postradical neck pain syndrome: a report of 25 cases. J.Pain Symptom.Manage. 1999;18: Chaplin JM, Morton RP. A prospective, longitudinal study of pain in head and neck cancer patients. Head Neck 1999;21: Shah S, Har-El G, Rosenfeld RM. Short-term and long-term quality of life after neck dissection. Head Neck 2001;23: Schuller DE, Reiches NA, Hamaker RC, Lingeman RE, Weisberger EC, Suen JY, Conley JJ, Kelly DR, Miglets AW. Analysis of disability resulting from treatment including radical neck dissection or modified neck dissection. Head Neck Surg. 1983;6: Saffold SH, Wax MK, Nguyen A, Caro JE, Andersen PE, Everts EC, Cohen JI. Sensory changes associated with selective neck dissection. Arch.Otolaryngol.Head Neck Surg. 2000;126: White CA, Macleod U. Cancer. BMJ 2002;325: de Leeuw JR, de Graeff A, Ros WJ, Blijham GH, Hordijk GJ, Winnubst JA. Prediction of depressive symptomatology after treatment of head and neck cancer: the influence of pre-treatment physical and depressive symptoms, coping, and social support. Head Neck 2000;22: Zaza C, Baine N. Cancer pain and psychosocial factors. A critical review of the literature. J.Pain Symptom Manage. 2002;24: Lee-Jones C, Humphris G, Dixon R, Hatcher MB. Fear of cancer recurrence--a literature review and proposed cognitive formulation to explain exacerbation of recurrence fears. Psychooncology. 1997;6: Chapter 1 16

18 28. Petticrew M, Bell R, Hunter D. Influence of psychological coping on survival and recurrence in people with cancer; systematic review. BMJ 2002;325: Hassanein KA, Musgrove BT, Bradbury E. Functional status of patients with oral cancer and its relation to style of coping, social support and psychological status. Br.J.Oral Maxillofac.Surg. 2001;39: Hann D, Winter K, Jacobsen P. Measurement of depressive symptoms in cancer patients: evaluation of the Center for Epidemiological Studies Depression Scale (CES-D). J.Psychosom.Res. 1999;46: Hjerl K, Andersen EW, Keiding N, Mouridsen HT, Mortensen PB, Jorgensen T. Depression as a prognostic factor for breast cancer mortality. Psychosomatics 2003;44: Krishnan KR, Delong M, Kraemer H, Carney R, Spiegel D, Gordon C, McDonald WI, Dew MA, Alexopoulos G, Buckwalter K, Cohen PD, Evans D, Kaufmann PG, Olin J, Otey E, Wainscott C. Comorbidity of depression with other medical diseases in the elderly. Biological Psychiatry 2002;Vol 52: Bottomley A. Depression in cancer patients: a literature review. Eur.J.Cancer Care 1998;7: Visser O, Coebergh JWW, Dijck van JAAM, Siesling S. Incidence of cancer in the Netherlands in Tenth report of the Netherlands Cancer Registry. Utrecht Netherlands Cancer Registry. Head and Neck tumours in the Netherlands Lulof Almelo, Brenner H. Long-term survival rates of cancer patients achieved by the end of the 20th century: a period analysis. The Lancet 2002;360: DeLisa JA. A history of cancer rehabilitation. Cancer 2001;92: Ronson A, Body JJ. Psychosocial rehabilitation of cancer patients after curative therapy. Support.Care Cancer 2002;10: Weert van E, Hoeksta-Weebers JEHM, Grol BMF, Otter R, Arendzen JH, Postema K, Schans van der CP. Physical functioning and quality of life after cancer rehabilitation Int. J. Rehab.Res. 2004;27: Salerno G, Cavaliere M, Foglia A, Pellicoro DP, Mottola G, Nardone M, Galli V. The 11th nerve syndrome in functional neck dissection. Laryngoscope 2002;112: Chapter 1 17

19 Chapter 1 18

20 CHAPTER 2 SHOULDER PAIN AND DISABILITY IN DAILY LIFE, FOLLOWING SUPRAOMOHYOID NECK DISSECTION: A PILOT STUDY. C. Paul van Wilgen, 1,2, Pieter U. Dijkstra, 1,2, Jan M. Nauta, 2 Albert Vermey, 3 Jan L.N. Roodenburg, 2 1. Department of Rehabilitation, 2. Department of Oral and Maxillofacial Surgery, 3. Department of Surgery,Head and Neck Surgery Journal of Cranio-Maxillofacial Surgery (2003) 31,

21 Summary Introduction: the purpose of this pilot study was to assess shoulder morbidity; i.e. pain and disability in daily activities, at least one year after unilateral or bilateral supraomohyoid neck dissection. Patients and methods: 52 patients having been subjected to a supraomohyoid neck dissection filled in a questionnaire assessing pain and daily activities. Results: 14 (28%) patients complained of ipsilateral shoulder pain following supraomohyoid neck dissection. The disability perceived during daily life, because of shoulder complaints, was minor. The pain and disability experienced during daily activities led to dependency upon other people in two patients. This dependency only existed during heavy household activities. Conclusion: Despite the fact that this type of neck dissection was developed to reduce shoulder morbidity, 28% of the patients experienced shoulder pain following supraomohyoid neck dissection. The degree of disability due to shoulder complaints, however, was minor. Introduction Neck dissection is performed in the treatment of carcinoma of head and neck. In radical neck dissection (Crile, 1906) all lymphnodes at one side of the neck are resected, plus the spinal accessory nerve, the internal jugular vein, and the sternocleidomastoid muscle. Morbidity following radical neck dissection includes, disfigurement, sensory changes, shoulder pain, reduced strength of the trapezius muscle, reduced range of motion of the shoulder, disability in activities of daily life, and even loss of work (Ewing, 1952). Shoulder morbidity is probably the result of sacrificing the spinal accessory nerve, resulting in a paralysis of the trapezius muscle (Remmler et al., 1986). The latter results in a reduction of active abduction, forward flexion of the arm, shoulder pain, and disability in daily activities. The incidence of morbidity after radical neck dissection varies between 60 % and 100 % (Ewing, 1952, Short et al., 1984, Brown et al., 1988, Shone and Yardley, 1991). This is why Bocca et al. (1980) introduced the functional or modified radical neck dissection in which at least one of the nonlymphatic structures is spared; the spinal accessory nerve, internal jugular vein, or sternocleidomastoid muscle. In most cases the spinal accessory nerve is spared to prevent shoulder morbidity. However the incidence of Chapter 2 20

22 shoulder pain and disability following modified radical neck dissection were still high, varying between 36 % and 77 % (Leipzig et al., 1983, Schuller et al., 1983, Pinsolle et al., 1997). Increased insight in the biological behaviour of head and neck squamous cell carcinoma, and improved staging, led to the development of four types of selective neck dissection (Figure 1): supraomohyoid neck dissection (levels I, II, and III), lateral neck dissection (levels II, III, and IV) posterolateral neck dissection (levels II, III, IV,and V), and anterior neck dissection (level VI) (Robbins et al., 1991). With these selective neck dissections all nonlymphatic structures mentioned are spared. Supraomohyoid neck dissection is often performed for oral or oropharyngeal squamous cell carcinoma, in patients with N0 tumours and is possibly sufficient in the treatment of a selected group of patients with positive nodes at level I (Medina and Byers,1989, Kowalski et al.,1993, Kligerman et al., 1994, Spiro et al., 1996). Although supraomohyoid neck dissections are frequently performed little is published about shoulder morbidity, and the consequences for daily activities. Pinsolle et al. (1997) described 41 patients following supraomohyoid neck dissection, with 32% having minor, 5 % moderate, and 2.5% severe shoulder problems (Pinsolle et al.,1997). All patients could manage their activities of daily living independently. Figure 1 Classification of selective neck dissection Supraomohyoid (levels I,II,III) Lateral (levels II,III,IV) Postero-lateral (levels II,III,IV,V) Anterior (levels VI) Reprinted from Robbins et al In other studies, of supraomohyoid neck dissections, the sample size was small (n = 7 to 36) (Leipzig et al., 1983, Sobol et al., 1985, Cheng et al., Chapter 2 21

23 2000), the follow-up was short (6 weeks to 6 months) (Leipzig et al., 1983, Sobol et al., 1985, Cheng et al., 2000), or the impact of shoulder morbidity on daily activities was not well described (Leipzig et al., 1983, Sobol et al., 1985, Cheng et al., 2000). Remmler et al., (1986) described 103 patients, of which 76 underwent supraomohyoid neck dissection. In their study the drop out after a year was 73 %, and of the remaining 25 patients it was not reported how many had been subjected to a supraomohyoid neck dissection, and hindrance during daily activities was not described (Remmler et al.,1986). The purpose of this pilot study was to analyse the prevalence of shoulder pain and disability, following supraomohyoid neck dissection, and to determine which daily activities were disturbed. Material and methods Patients in the care of the Department of Oral and Maxillofacial Surgery (University Hospital Groningen) who had undergone supraomohyoid neck dissection, for squamous cell carcinoma of the oral cavity or oropharynx, at least 1 year previously, were asked to participate in this study. Patients who matched our criteria were asked, during a regular follow-up appointment, to participate in the study. A standardized questionnaire was used to assess pain and disability. Patients operated upon bilaterally were asked to refer to the painful shoulder only. The questionnaire was a combination of two valid and reliable questionnaires: the shoulder disability questionnaire (SDQ) (van-der Heijden et al., 2000) and the Groningen activity restriction scale (GARS) (Suurmeijer et al.1994). From these two questionnaires only questions assessing typical shoulder functions were selected. Patients who perceived shoulder pain completed the whole questionnaire while patients without pain filled out if they have perceived temporarily shoulder pain. The frequency of shoulder pain was assessed on a four point Likert scale (shoulder pain was perceived constantly, often, occasionally or never in the last month). Furthermore the questionnaire assessed: waking up because of shoulder pain, pain when lying on the affected shoulder, pain when moving the shoulder, pain when leaning on the arm or elbow, pain when reaching above shoulder level, pain when carrying heavy or light objects, and pain when reaching for the neck. Disability perceived during daily activities was also assessed on a four point Likert scale: patients filled out the level of effort Chapter 2 22

24 during daily activities or whether they were dependent on others for their daily activities (fully independently without difficulty, some difficulty, great difficulty, only able to do it with someone s help). The following daily activities were assessed: dressing, washing, washing hair, light and heavy household activities, facial care and toilet use. In addition information concerning physiotherapy, history of shoulder pain, type of surgery were asked for or collected from the medical records. Data were analysed using SPSS 10.0: chi-square analysis with a continuity correction, and t-test for independent samples Results Fifty-six patients were asked to fill in the questionnaire. Of these, 52 returned the questionnaire of which two were excluded from analysis because of missing data. Thus 50 questionnaires (27 females 23 males, mean 63 years, SD: 9) could be analysed. The mean follow-up was 2.3 years (SD: 1.3). Forty patients were operated upon unilaterally, and 10 bilaterally. All operations were between 1995 and Fourteen patients (28 %, 95% Confidence Interval: 18% - 42%) perceived shoulder pain, of which four experienced this constantly, three often, and seven experienced shoulder pain occasionally. Twenty-seven patients had received radiotherapy of which 10 (37 %) complained of shoulder pain (Table 1). Table 1 Shoulder complaints and radiation therapy, gender, follow-up and age Shoulder complaints No shoulder complaints p Radiation Therapy Yes No * Gender Male 5 18 Female * Follow-up (mean; yrs) 2.2 (SD 2.2) 2.4 (SD 1.2) 0.71 ** Age (mean; yrs) 63 (SD 8.8) 62 (SD 9.0) 0.79 ** * Results of Chi-square with continuity correction, **Results of t-test for independent sample analyses. SD = standard deviation Chapter 2 23

25 No significant relation was found between shoulder complaints and gender, follow-up interval, or age (Table 1). Of the 14 patients with shoulder complaints 8 had an were operation on their dominant side. One of the patients with shoulder pain reported shoulder pain before surgery. Activities typically provoking shoulder pain were: moving arm or shoulder, reaching above shoulder level, reaching for the neck, carrying heavy objects, and laying on the shoulder (Figure 2). Due to the shoulder complaints two patients needed help from others during heavy house-hold activities, such as washing windows, or cleaning the floor. Eight patients had difficulties with daily activities but did not require help, and of these eight some perceived difficulties with: washing their hair (five patients), washing and drying themselves (five), light household activities (five), and facial care (four). Figure 2 Shoulder pain during daily activities in 14 out of 50 patients following supraomohyoid neck dissection frequency of pain reaching for the neck carrying light objects carrying heavy objects reaching above shoulder level leaning on arm/elbow moving shoulder/arm lying on shoulder waking up never sometimes often always 0% 20% 40% 60% 80% 100% Chapter 2 24

26 The correlation between the frequency of shoulder pain and the amount of perceived disability during daily activities was r =.89 (95 % Confidence Interval: ) Only six out of 14 patients with shoulder complaints had been or were still being treated by a physiotherapist. Of the 36 patients (72%) without shoulder complaints, four patients had experienced temporary shoulder complaints following neck dissection. Discussion Fourteen of the 50 patients (28%) experienced shoulder problems, despite the preservation of the spinal accessory nerve. As the nerve is partially stripped of its vascular supply during surgery a temporary non-functional nerve or only partially functional nerve may be the result (Soo et al.,1990). Consequently the trapezius muscle may be too weak to stabilize the scapula sufficiently. Although the group interviewed was only 50 patients, 28% of these perceiving shoulder pain is a significant proportion following this selective type of neck dissection. The exact source of the post-operative shoulder pain is unknown. Many suggestions o f the possible cause have been made: secondary frozen shoulder (Patten and Hillel, 1993), hypertrophic sternoclavicular joint (Cantlon and Gluckman, 1983), and excessive stretching of the rhomboid and levator scapulae muscle (Nori, et al., 1997). Post-operative shoulder pain is not always caused by spinal accessory nerve dysfunction, Saunders et al.(1985) found a weak relationship between trapezius muscle dysfunction and subjective symptoms of shoulder pain (Saunders et al., 1985). Cutting of cutaneous sensory nerves, causing neuropathic pain, or neuromata may also cause shoulder pain (Brown et al., 1988). Most of the authors agree that an important mechanism behind the shoulder pain is the overload of the shoulder girdle as a result of the inability of the trapezius muscle to stabilize the scapula. Although supraomohyoid neck dissections seem to create less disability when compared with radical- or modified radical neck dissections, the percentage of patients (28%) with shoulder pain after a supraomohyoid neck dissection is relatively high, but considerably lower when compared with radical neck dissections (60%-100%)% (Ewing, 1952, Short et al., 1984, Chapter 2 25

27 Brown et al., 1988, Shone and Yardley, 1991) and modified radical neck dissections (36%-77%) (Leipzig et al., 1983, Schuller et al., 1983, Pinsolle et al., 1997). Despite having some difficulties in heavy household activities, most patients could perform their daily activities without the help of others. In this study radiation therapy was not significantly associated with shoulder pain or disability, confirming the statement of Chaplin and Morton (1999) that radiation therapy has no effect on shoulder pain. However others state that radiation therapy may add significantly to permanent post-operative disability (Schuller et al., 1983). These conflicting findings indicate that effects of radiation therapy on shoulder complaints need further investigation. In this study only six of 14 patients with shoulder complaints were treated with physiotherapy. Physiotherapy is often prescribed to help patients with shoulder complaints following neck dissection the aim being to reduce or prevent shoulder pain by reducing shoulder load, and to increase the strength of other scapula stabilizing muscles to compensate for loss of function of the trapezius muscle. Patients seem to benefit from these physical therapy programmes. (Saunders and Johnson, 1975, Gluckman et al., 1983, Fialka and Vinzenz, 1989, Salerno et al., 2002). Conclusion Despite the fact that the supraomohyoid neck dissection was developed to reduce shoulder morbidity, 28 % of the patients experienced shoulder pain and disability in daily activities. As this study group was relatively small, the cause and extent of morbidity requires further research. Acknowledgement The authors thank C. Bron, J.L.M. Franssen and B.G.M. de Valk for their support in developing the questionnaire for this study Chapter 2 26

28 References 1. Bocca E, Pignataro O, Sasaki CT. Functional neck dissection. A description of operative technique. Arch Otolaryngol 1980; 106: Brown H, Burns S, Kaiser CW. The spinal accessory nerve plexus, the trapezius muscle, and shoulder stabilization after radical neck cancer surgery. Ann Surg 1988; 208: Cantlon GE, Gluckman JL. Sternoclavicular joint hypertrophy following radical neck dissection. Head Neck Surg 1983; 5: Chaplin JM, Morton RP. A prospective, longitudinal study of pain in head and neck cancer patients. Head Neck 1999; 21: Cheng PT, Hao SP, Lin YH, Yeh AR. Objective comparison of shoulder dysfunction after three neck dissection techniques. Ann.Otol.Rhinol.Laryngol 2000;109: Ewing MRMH. Disability following radical neck dissection. Cancer 1952; 5: Fialka V, Vinzenz K. Zur physikalischen therapie und diagnostik der postoperativ geschädigten schulter nach radikaler neck-dissection. Dtsch Z Mund Kiefer Gesichtschir 1989; 13: Gluckman JL, Myer CM, Aseff JN, Donegan JO. Rehabilitation following radical neck dissection. Laryngoscope 1983; 93: van-der Heijden G, Leffers P, Bouter LM. Shoulder disability questionnaire design and responsiveness of a functional status measure. J Clin Epidemiol 2000; 53: Kligerman J, Lima RA, Soares JR, Prado L, Dias FL, Freitas EQ, Olivatto LO. Supraomohyoid neck dissection in the treatment of T1/T2 squamous cell carcinoma of oral cavity. Am J Surg 1994; 168: Kowalski LP, Magrin J, Waksman G, Santo GF, Lopes ME, de Paula RP, Pereira RN, Torloni H. Supraomohyoid neck dissection in the treatment of head and neck tumors. Survival results in 212 cases. Arch Otolaryngol Head Neck Surg 1993; 119: Leipzig B, Suen JY, English JL, Barnes J, Hooper M. Functional evaluation of the spinal accessory nerve after neck dissection. Am J Surg 1983; 146: Medina JE, Byers RM. Supraomohyoid neck dissection: rationale, indications, and surgical technique. Head Neck 1989; 11: Nori S, Soo KC, Green RF, Strong EW, Miodownik S. Utilization of intraoperative electroneurography to understand the innervation of the trapezius mu scle. Muscle Nerve 1997; 20: Chapter 2 27

29 15. Patten C, Hillel AD. The 11th nerve syndrome. Accessory nerve palsy or adhesive capsulitis? Arch Otolaryngol Head Neck Surg 1993; 119: Pinsolle V, Michelet V, Majoufre C, Caix P, Siberchicot F, Pinsolle J. Branche externe du nerf spinal et évidements ganglionnaires cervicaux. Rev Stomatol Chir Maxillofac 1997; 98: Remmler D, Byers R, Scheetz J, Shell B, White G, Zimmerman S, Goepfert H. A prospective study of shoulder disability resulting from radical and modified neck dissections. Head Neck Surg 1986; 8: Robbins KT, Medina JE, Wolfe GT, Levine PA, Sessions RB, Pruet CW. Standardizing neck dissection terminology. Official report of the Academy's Committee for Head and Neck Surgery and Oncology. Arch Otolaryngol Head Neck Surg 1991; 117: Salerno G, Cavaliere M, Foglia A, Pellicoro DP, Mottola G, Nardone M, Galli V. The 11th nerve syndrome in functional neck dissection. The Laryngoscope 2002; 112: Saunders WH, Johnson EW. Rehabilitation of the shoulder after radical neck dissection. Ann Otol Rhinol Laryngol 1975; 84: Schuller DE, Reiches NA, Hamaker RC, Lingeman RE, Weisberger EC, Suen JY, Conley JJ, Kelly DR, Miglets AW. Analysis of disability resulting from treatment including radical neck dissection or modified neck dissection. Head Neck Surg 1983; 6: Shone GR, Yardley MP. An audit into the incidence of handicap after unilateral radical neck dissection. J Laryngol Otol 1991; 105: Short SO, Kaplan JN, Laramore GE, Cummings CW. Shoulder pain and function after neck dissection with or without preservation of the spinal accessory nerve. Am J Surg 1984; 148: Sobol S., Jensen C., Sawyer W., Costiloe P., Thong N. Objective comparison of physical dysfunction after neck dissection. Am J Surg 1985; 150: Soo KC, Guiloff RJ, Oh A, Della RG, Westbury G. Innervation of the trapezius muscle: a study in patients undergoing neck dissections. Head Neck 1990; 12: Spiro RH, Morgan GJ, Strong EW, Shah JP. Supraomohyoid neck dissection. Am J Surg 1996; 172: Suurmeijer TP, Doeglas DM, Moum T, Briancon S, Krol B, Sanderman R, Guillemin F, Bjelle A, van den Heuvel WJ. The Groningen Activity Restriction Scale for measuring disability: its utility in international comparisons. Am J Public Health 1994; 84: Chapter 2 28

30 Chapter 3 INCIDENCE OF SHOULDER PAIN AFTER NECK DISSECTION: A CLINICAL EXPLORATIVE STUDY FOR RISK FACTORS Pieter U Dijkstra, PhD 1,2,3 C. Paul van Wilgen, BSc 1,2,3, Ron P Buijs, BSc 4, Wim Brendeke, BSc 5, Cornelis JT de Goede, BSc 6, Ad Kerst, BSc 7, Muriel Koolstra, BSc 6, Johan Marinus Msc 8, Elisabeth M Schoppink, MSc 8, Martijn M Stuiver, BSc 9, Caroline F van de Velde, MSc 10, Jan LN Roodenburg, PhD 1. 1: Dept of Oral and Maxillofacial Surgery, University Hospital Groningen, 2: Pain Center, University Hospital Groningen, 3: Dept of Rehabilitation, University Hospital Groningen, 4: University Hospital Rotterdam / Daniel, PO Box 5201, 3075 EA, Rotterdam, 5: Rijnstate Hospital Arnhem, PO Box 9555, 6800 TA, Arnhem, 6: University Hospital Vrije Universiteit Amsterdam, PO Box 7057, 1007 MB, Amsterdam, 7: University Hospital Utrecht, Heidelberglaan 100, 3584 CX, Utrecht, 8: Haaglanden Medical Center, PO Box 432, 2501 CK, Den Haag, 9: Netherlands Cancer Institute/Antoni van Leeuwenhoek Hospital, Plesmanlaan 121, 1066 CX, Amsterdam, 10: University Hospital Maastricht, PO Box 5800, 6202 AZ, Maastricht. Head and Neck (2001) Nov

31 Abstract Background It is the purpose of this study to determine the incidence of shoulder pain and restricted range of motion of the shoulder after neck dissection, and to identify risk factors for the development of shoulder pain and restricted range of motion. Methods Clinical patients who underwent a neck dissection completed a questionnaire assessing shoulder pain. The intensity of pain was assessed using a visual analog scale (100 mm). Range of motion of the shoulder was measured. Information about reconstructive surgery, and side and type of neck dissection was retrieved from the medical records. Results Of the patients (n=177, mean age 60.3 years (SD: 11.9)) 70% experienced pain in the shoulder. Forward flexion and abduction of the operated side was severely reduced compared to the non-operated side, 21 and 47 respectively. Non-selective neck dissection was a risk factor for the development of shoulder pain (9.6 mm) and a restricted shoulder abduction (55 ). Reconstruction was risk factor for a restricted forward flexion of the shoulder (24.5 ). Conclusions Shoulder pain after neck dissection is clinically present in 70% of the patients. Non-selective neck dissection is a risk factor for shoulder pain and a restricted abduction. Reconstruction is a risk factor for a restricted forward flexion of the shoulder. Chapter 3 30

32 Introduction The presence of shoulder complaints is a common problem following radical neck dissection. Accordingly, Krause 1 found that 72% of the patients suffered from shoulder complaints, whereas 44% of these patients were disabled due to the severity of these shoulder complaints. Other authors found prevalences of shoulder complaints after radical neck dissection varying from 50 to 100%. 2,3 In general shoulder complaints after radical neck dissection consist of pain in the neck-shoulder region and a restricted active range of motion of the shoulder girdle. It is assumed that these complaints are based on sacrificing the accessory nerve during the neck dissection, which results in most patients in paralysis of the descending and transverse part of the trapezius muscle. 4 Due to loss of strength of the trapezius muscle the scapula shifts downward and the inferior angle rotates medially, resulting in a downward facing of the glenoid fossa. 5 Due to this shift and downward facing, the active range of motion of forward flexion and abduction of the shoulder girdle is restricted. Additionally, during activities of the arm the scapula can not be adequately stabilized to the thorax as a result of insufficient muscle strength. The change in position of the scapula and the inadequate stabilization may lead to a mechanical overload of the shoulder causing pain. Several structures of the shoulder girdle, including the gleno-humeral joint, acromio-clavicular joint, sternoclavicular joint, levator scapula and rhomboid muscles have been held responsible for shoulder pain. 6,7 Even frozen shoulder and lesions of the brachial plexus have been reported after neck dissection. 8,9 However, if the accessory nerve is not sacrificed, as in functional or modified neck dissections, shoulder complaints are still reported by 31% to 60 % of the subjects. 2,3,10,11 Even after selective neck dissections shoulder complaints have been reported in approximately 29% to 39% of the patients. 12,13 Most studies identifying shoulder complaints after neck dissection have been performed after discharge from the hospital, at least a month after surgery, or have been performed retrospectively. Only two studies included patients before discharge from the hospital. 14,15 However, in the study of Leipzig et al. 14,no information is provided about shoulder complaints during the hospital stay. In the study of Nowak et al. 15, only the range of motion of the neck and shoulder was assessed, but shoulder pain was not investigated. Chapter 3 31

33 Therefore, little is known as to whether complaints are present immediately after the operation or whether they develop after discharge from the hospital? Another problem is that subjects with shoulder complaints before the neck dissection are not excluded in most studies, except in the study of Carentfelt et al. 16 Therefore, most studies cannot be conclusive with regard to the relationship between cause and effect, i.e., neck dissection resulting in shoulder complaints, because the shoulder pain may already be present before the dissection. 17 The aims of this explorative study were to determine the incidence of shoulder pain and restricted range of motion of the shoulder after neck dissection the day before discharge from the hospital, to analyse the effect of shoulder pain on daily activities in the clinical phase, and to identify risk factors for the development of shoulder pain and restricted range of motion of the shoulder. Material and methods In this multicentre study seven Dutch hospitals participated: Netherlands Cancer Institute/Antoni van Leeuwenhoek Hospital Amsterdam, University Hospital Groningen, University Hospital Maastricht, University Hospital Rotterdam/ Daniel, University Hospital Vrije Universiteit Amsterdam, Haaglanden Medical Center Den Haag, and Rijnstate Hospital Arnhem. Clinical patients who underwent a neck dissection because of a tumor in the head and neck area were assessed by a physical therapist the day before discharge from the hospital. The assessment consisted of a standardized questionnaire, developed for this study, which was completed by the patient. The questionnaire addressed the following information: hand dominance, the presence of preoperative complaints of the shoulders (operated and/or non-operated side) three months prior to the neck dissection and the presence of shoulder pain at the side of the neck dissection under various circumstances. These circumstances included rest, movements of the shoulder, lying on the shoulder, walking with the arm unsupported, dressing, and washing. In addition, the questionnaire assessed problems while washing, dressing, and reaching forward and the reasons for these problems (i.e., shoulder pain, stiffness, and/or loss of strength). Finally, the amount of pain in the shoulder of the operated side was assessed on a visual analog scale (100 mm). Chapter 3 32

34 The following information was retrieved from the medical records: tumor type, localization, staging, type and extent of surgery, type of reconstructive surgery, side and type of neck dissection (radical, modified, with preservation of the accessory nerve, or selective), preoperative radiotherapy, and pain medication (non opiate, mild opiates and opiates). When the study proved to be feasible, range of motion of the shoulder (forward flexion, abduction external rotation) was measured by the physical therapist using an inclinometer according to a standardized protocol. The questionnaire and the range of motion measurements became part of the standard discharge procedure. Inclusion criteria for the study were: a neck dissection for a carcinoma of the head and neck region in one of the participating hospitals, good understanding of the Dutch language and age 18 years or older. Patients with shoulder complaints (at the side of the operation) within 3 months before the neck dissection were excluded as were patients with an history of mental illness. In this way patients at risk for developing shoulder complaints as a result of the neck dissection were selected. Of the patients with a bilateral dissection the most painful side was entered in the database. The database was checked for missing data and the participating institutes were requested to provide the missing data, if available. Data analysis Data analysis in SPSS version 9 and CIA version 2 comprised descriptive statistics, 95% confidence interval calculation, t-tests for paired data, chi square tests, and product moment correlation (Pearson s r). In the univariate analyses risk factors for shoulder pain, ristrictions in forward flexion and abduction were identified. In the multivariate analyses, linear regressions (method stepwise forward), the extent of shoulder pain and range of abduction and forward flexion of the operated side were predicted on the basis of the risk factors identified in the univariate analyses. The risk factors were dissection type, preservation of cervical plexus, reconstruction, gender and age. For the analysis of differences in range of motion between the operated and the non-operated side, patients with bilateral dissections as well as patients with shoulder complaints of the non-operated side in the 3 months before the neck dissection, were excluded. Chapter 3 33

35 Table 1 Descriptive statistics of the population under study, type and stage of tumor, side and type of neck dissection, radiotherapy, reconstructive therapy, medication and days after surgery Variables (number of valid observations)* Frequency % Gender (n=171) -Women 68 40% -Men % Age in years (sd) 60.3 (12) Tumor type (n=141) -Squamous cell carcinoma % -Salivary gland tumor 12 9% -Melanoma 5 4% -Other types of cancer 15 11% # Tumor stage (n=145) -T0 6 4% -T % -T % -T % -T % -Tx 5 3% Side of dissection (n=169) -Dominant side 81 49% -Non dominant 84 48% -Bilateral dissection 4 1% Type of dissection (n=169) -Radical neck dissection 42 25% -Modified neck dissection (preserving NXI) 95 56% -Selective neck dissection 32 19% Preservation of cervical branches (n=68) -Yes 44 65% -Partial 3 4% -No 21 31% *Because of missing data the totals of the analyses do not always add up to 177. # Due to rounding of, the sum of the percentages exceeds 100. Chapter 3 34

36 Table 1 (continued) Variables (number of valid observations)* Frequency % Preoperative radiotherapy (n=170) -Yes 20 12% -No % Reconstructive surgery (n=171) -Pectoral cutaneous flap 20 12% -Radial cutaneous flap 9 5% -Other 25 15% -No % Medication (n=167) -No medication 87 52% -Non opiates (NSAIDs) 59 35% -Mild opiates 5 4% -Opiates 2 1% -Unknown 14 8% Days after surgery (sd) 13.2 (10) Median [interquartile range] 10 [7-16] *Because of missing data the totals of the analyses do not always add up to 177. Results The initial database consisted of 75 women (39%) and 119 men (61%). The mean age of the total group was 60.5 (SD: 12.1) years. After excluding the patients with shoulder complaints before the neck dissection, a cohort of 177 patients remained, consisting of 68 women (40%) and 103 men (60%) with a mean age of 60.3 (sd: 11.9) years. Gender was not recorded in 6 patients. Data of range of motion of the shoulder was available of 100 patients, after excluding patients with shoulder complaints before the operation (operated and/or non-operated side) and patients with a bilateral dissection. Descriptive statistics of the research population, type of tumor, tumor stage, type of dissection, preservation of N. XI and cervical branches, radiotherapy, reconstructive surgery, medication use and days after surgery are summarized in Table 1. Shoulder pain was experienced by 70% of the patients (mean intensity 14 mm, sd 16) (Table 2). The number of situations in which the patient experienced pain was significantly related to the intensity of pain (Pearson s r =.73; 95% CI: 0.63 to 0.80). Pain intensity was not significantly related (r =.032) to the number of days after surgery. Pain Chapter 3 35

37 medication was used by 60% of the patients experiencing shoulder pain whereas 43% of the patients without shoulder pain used pain medication. This difference in percentage was not significant (chi square = 2.77; p =.096). Table 2 Frequency and intensity of shoulder pain after neck dissection Variables Frequency (95% CI) (number of valid observation) (%) Shoulder pain present* (n=128): -Yes 89 (70%) (62% to 78%) -Intensity of shoulder pain (sd: range) 14.0 (16: 0-66) -Median [inter quartile range] 8 [0-23] Pain in the shoulder (n=177) -During rest 30 (17%) (11% to 22%) -Moving the shoulder 54 (31%) (24% to 38%) -Lying on the shoulder 49 (30%) (23% to 37%) -Walking (arm not supported) 20 (11%) (7% to 16%) -Washing the opposite arm 15 (9%) (4% to 13) -Dressing 17 (10%) (5% to 14%) Difficulties, due to pain, stiffness or weakness of the shoulder, with (n=177) -Washing 54 (31%) (24% to 38%) -Dressing 52 (30%) (13% to 37%) Number of situations in which the patients experience shoulder pain (n=177) (56%) (49% to 63%) (17%) (11% to 22%) (12%) (7% to 17%) -3 9 (5%) (3% to 9%) -4 9 (5%) (3% to 9%) -5 4 (2%) (1% to 6%) -6 5 (3%) (1% to 6%) * Pain was assessed on a 100 mm Visual Analoge scale (VAS): Presence of pain indicates pain > 0 on the VAS. Because of missing data the totals of the analyses do not always add up to 177. Chapter 3 36

38 In women as well as in men, 70% had shoulder pain. Moving the shoulder and lying on the shoulder were most frequently reported to be painful, 31% and 30% respectively. Forward flexion and abduction of the operated side was significantly reduced compared with the non-operated side, 21 and 47 respectively (Table 3). Risk factors for shoulder pain were: sacrificing the cervical plexus versus preservation of this plexus (relative risk (RR) = 1.7), radical dissection versus selective dissection (RR = 1.5) and modified radical dissection versus selective dissection (RR = 1.4). Risk factors for a restricted abduction were: sacrificing the cervical plexus versus preservation of this plexus (RR = 1.7), radical dissection versus selective dissection (RR = 2.3) and modified radical dissection versus selective dissection (RR = 1.8). Risk factors for a restricted forward flexion were: sacrificing the cervical plexus versus preservation of this plexus (RR = 1.8) and reconstructive surgery versus no reconstruction (RR = 1.8) (Table 4). In the linear regression analysis (multivariate analysis), a non selective dissections was a risk factor for the development of shoulder pain and restricted shoulder abduction. Reconstruction was a risk factor for restricted forward flexion of the shoulder (Table 5). Tabel 3 Differences in range of motion (in degrees) between operated side and non-operated side and the 95% confidence interval of the differences. (n=100) Operated side Non-operated side Mean SD Mean SD difference (95% CI) Forward flexion (14.7 to 26.6) Abduction (37.5 to 55.6) External rotation (3.6 to 7.6) Chapter 3 37

39 Table 4 Risk factors for shoulder pain, restricted abduction and restricted forward flexion Shoulder pain Restricted abduction Restricted forward flexion Cervical plexus preserved -Yes 57%* 53%* 37%* -No 95% 90% 65% Reconstructed -Yes 68% 73% 67%* -No 69% 55% 37% Radiotherapy -Yes 88% 63% 50% -No 66% 60% 46% Dissection -Radical 79% 84% 58% -Modified radical 75% 66% 49% Dissection -Radical 79%* 84%* 58% -Selective 52% 36% 32% Dissection -Modified radical 75%* 66%* 49% -Selective 52% 36% 32% Restricted abduction was defined as abduction (non-operated side) - abduction (operated side) 20. Restricted forward flexion was defined as forward flexion (non-operated side) - forward flexion (operated side) 20. Percentages differ significantly from each other (results of chi square tests). Note: during the analyses preservation of some branches of the cervical plexus was left out because of the small number of subjects. Chapter 3 38

40 Table 5 Results of the linear regression analysis to predict shoulder pain, and range of motion of abduction and forward flexion of the operated side Variable β 95% CI of β R square Shoulder pain operated side -Selective dissection -9.6 (-19.1 to -0.2) -Constant 20.1 (14.4 to 25.8).06 Abduction operated side -Selective dissection 55.0 (35.0 to 75.1) -Constant 76.1 (64.3 to 87.9).35 Forward flexion operated side -Reconstruction (-35.5 to -13.4) -Constant (141.8 to 155.1).26 In the regression analyses the following variable were entered step wise forward: Selective dissection (yes/no), preservation of the cervical plexus (yes/no) reconstruction (yes/no), gender (male /female) and age in years. Discussion Following neck dissection, 70% of the patients reported some form of shoulder pain in the clinical phase. The intensity of the pain was not excessive judged from the mean, the median and inter-quartile range of the pain score. The intensity of pain was 23 or less in 75% of the patients on a 100 mm-vas. It was striking that only 44% of the patients claimed to have pain during one or more provoking situations/activities while 70% scored shoulder pain more than zero on a VAS. This discrepancy in reporting pain might be explained that patients experience a continuous pain, resulting in a score above 0 on the VAS, which is not aggravated by the activities assessed. Our clinical finding that 79% of the patients who had a radical neck dissection reported shoulder pain is similar to the percentage reported by Krause 1 in his retrospective study in the post-clinical phase (after discharge from the hospital) (Table 4). It is possible that the shoulder is already overloaded with relative non-strenuous activities in the clinical phase. Of the patients who had been operated with preservation of the N. XI (modified Chapter 3 39

41 radical) still 65% reported pain (Table 4). This percentage is somewhat higher compared to other studies performed post-clinically. 2,3 Intensity of shoulder pain was not significantly correlated with the number of post operative days (r =.032). Intensity of the shoulder pain was significantly related (r =.73) to the number of activities in which patients experienced shoulder pain, indicating that the shoulder pain influences ADL during hospital stay considerably (53% explained variance). Range of motion was significantly and considerably affected by neck dissection. The mean difference between the operated and non operated side was 21 for forward flexion and 47 for abduction. The mean difference in external rotation was significant but small. This indicates that neck dissection has the greatest impact on shoulder abduction. The difference in impact can be explained by the fact that the trapezius muscle is active during abduction while during forward flexion the serratus anterior muscle is active. The risk factors for shoulder pain, restricted abduction and restricted forward flexion were entered in regression analyses. In the regression analysis, a selective dissection was the only variable contributing significantly to the prediction of shoulder pain. The mean difference in shoulder pain between a patient with a selective dissection and a patient with a non-selective dissection (modified or radical) was 9.6 mm on a 100 mm VAS. Thus, selective dissection is a protective factor for shoulder pain compared to nonselective dissections. Although significant, it must be noted that the strength of the protection is weak. Predicting the abduction of the operated side, again selective dissection was the only variable contributing to the equation. The mean difference in abduction between patients with a selective dissection compared to patients with non selective dissection (modified or radical) is 55. Our findings that selective dissection provides protection against shoulder pain and a restricted abduction are in agreement with the findings of post-clinical studies. 2,3,18,19 In the prediction of the forward flexion of the operated side, reconstruction contributed significantly to the regression equation. Clinically this indicates that a reconstruction reduces forward flexion with approximately 25 on the average, compared to non reconstructed patients. Probably the extent of surgery, the tunnelling of the pectoralis muscle on the side of the surgery, or pain due to the radialis flap reduces forward flexion. This finding is in agreement of Nowak et al. 17 who found that reconstruction using a pectoral Chapter 3 40

42 myo-cutaneous flap reduced range of motion of the cervical spine and forward flexion of the shoulder. Because of the hospital setting of this study our results can only be generalized to the post-clinical phase to a limited extent. Although the dissection was performed preserving the N. XI, in many subjects, still the only procedure that had a protective effect on shoulder pain was a selective dissection (Table 5). It is possible that during non-selective procedures, but with preservation of the N. XI, the nerve loses its conductive function temporarily due to stripping of the nerve from its surrounding tissues resulting in a neurapraxia. This neurapraxia may recover in the post clinical phase. 18,20 The type and extent of dissection is dictated by the tumor site, size and stage. However, when possible, surgery should be as selective as possible to reduce shoulder pain and restriction in abduction. Additionally a modified neck dissection preserving the N. XI in a clinical positive neck does not adversely affect survival and neck control. 21 A weakness of this study is the considerable amount of missing data, which in part can be attributed to incompleteness of the medical files. For instance, quite often it could not be found in the surgery reports whether the cervical plexus was preserved or not. Even the tumor type was not available in 36 cases. Strength of this study was that subjects with shoulder complaints prior to the dissection were excluded from the analysis. In a post hoc analyses, the intensity of pain (VAS score) in the group with complaints before the dissection was 39.1 mm and in the group without complaints 14.0 mm (95% CI of the difference: 10.8 to 39.3). This illustrates the impact on the results of the patients with complaints before the dissection, if they are not excluded. In conclusion, pain after neck dissection is clinically present in 70% of the patients. A risk factor for development of shoulder pain is a non-selective dissection. The pain has a considerable impact on activities of clinical daily living. Acknowledgement We would like to thank dr B Stegenga for his critical comments on previous versions of this manuscript. Chapter 3 41

43 References 1. Krause HR. Shoulder-arm-syndrome after radical neck dissection: its relation with the innervation of the trapezius muscle. Int J Oral Maxillofac Surg 1992;21: Short SO, Kaplan JN, Laramore GE, Cummings CW. Shoulder pain and function after neck dissection with or without preservation of the spinal accessory nerve. Am J Surg 1984;148: Saunders-JR J, Hirata RM, Jaques DA. Considering the spinal accessory nerve in head and neck surgery. Am J Surg 1985;150: Krause HR, Bremerich A, Herrmann M. The innervation of the trapezius muscle in connection with radical neck-dissection. An anatomical study. J Craniomaxillofac Surg 1991;19: Remmler D, Scheetz J, Byers R, et al. Morbidity of modified neck dissection. In: Larson DL, Ballantyne AJ, Guillamondegul OM, editors. Cancer in the neck. New York: Macmillan Inc.; p Saunders WH, Johnson EW. Rehabilitation of the shoulder after radical neck dissection. Ann Otol Rhinol Laryngol 1975;84: Cantlon GE, Gluckman JL. Sternoclavicular joint hypertrophy following radical neck dissection. Head Neck Surg 1983;5: Pfeifle K, Koch H. [Pain syndromes as late sequelae of neck dissection] Schmerzsyndrome als Spatfolge nach "Neck dissection". Dtsch Zahnarztl Z 1973;28: Patten C, Hillel AD. The 11th nerve syndrome. Accessory nerve palsy or adhesive capsulitis? Arch Otolaryngol Head Neck Surg 1993;119: Bocca E, Pignataro O, Sasaki CT. Functional neck dissection. A description of operative technique. Arch Otolaryngol 1980;106: Robbins KT, Medina JE, Wolfe GT, Levine PA, Sessions RB, Pruet CW. Standardizing neck dissection terminology. Official report of the Academy's Committee for Head and Neck Surgery and Oncology. Arch Otolaryngol Head Neck Surg 1991;117: Pinsolle V, Michelet V, Majoufre C, Caix P, Siberchicot F, Pinsolle J. [Spinal accessory nerve and lymphatic neck dissection] Branche externe du nerf spinal et evidements ganglionnaires cervicaux. Rev Stomatol Chir Maxillofac 1997;98: Cheng PT, Hao SP, Lin YH, Yeh AR. Objective comparison of shoulder dysfunction after three neck dissection techniques. Ann Otol Rhinol Laryngol 2000;109: Chapter 3 42

44 14. Leipzig B, Suen JY, English JL, Barnes J, Hooper M. Functional evaluation of the spinal accessory nerve after neck dissection. Am J Surg 1983;146: Nowak P, Parzuchowski J, Jacobs JR. Effects of combined modality therapy of head and neck carcinoma on shoulder and head mobility. J Surg Oncol 1989;41: Carenfelt C, Eliasson K. Radical neck dissection and permanent sequale associated with spinal accesorry nerve injury. Acta Otolaryngol 1981;91: Chaplin JM, Morton RP. A prospective, longitudinal study of pain in head and neck cancer patients. Head Neck 1999;21: Kuntz AL, Weymuller EA. Impact of neck dissection on quality of life. Laryngoscope 1999;109: Terrell JE, Welsh DE, Bradford CR, et al. Pain, quality of life, and spinal accessory nerve status after neck dissection. Laryngoscope 2000;110: Remmler D, Byers R, Scheetz J, et al. A prospective study of shoulder disability resulting from radical and modified neck dissections. Head Neck Surg 1986;8: Andersen PE, Shah JP, Cambronero E, Spiro RH. The role of comprehensive neck dissection with preservation of the spinal accessory nerve in the clinically positive neck. Am J Surg 1994;168: Chapter 3 43

45 Chapter 3 44

46 CHAPTER 4 SHOULDER COMPLAINTS AFTER NERVE SPARING NECK DISSECTION C.Paul van Wilgen, 1,2,5,Pieter U. Dijkstra, 1,2,5, Bernhard F.A.M. van der Laan, 3, John Th.M. Plukker, 4, Jan L.N. Roodenburg, 1 1. Department of Oral and Maxillofacial Surgery, 2. Department of Rehabilitation 3. Department of Otorhinolaryngology Head & Neck Surgery, 4. Department of Surgical Oncology 5. Pain Expertise Center International Journal of Oral and Maxillofacial Surgery (2004), 33 (3),

47 Abstract The purpose of the study was to analyse the prevalence of shoulder complaints after nerve sparing neck dissection at least 1 year after surgery, and to analyse the influence of radiation therapy on shoulder complaints. Patients were interviewed for shoulder complaints, and patients filled out the shoulder disability questionnaire to evaluate shoulder disability in daily activities. In total 137 patients; 51 after modified radical neck dissection (MRND), 21 after postero-lateral neck dissection (PLND), and 65 after supraomohyoid neck dissection (SOHND) were analysed. After MRND 33.3% of the patients experienced shoulder complaints, after PLND 66.7 %, and after SOHND 20 % of the patients experienced shoulder complaints. Type of neck dissection was significantly (p < 0.001) related to shoulder complaints. Outcome on the shoulder disability questionnaire also showed a significant (p< 0.01) difference in outcome for type of neck dissection. The prevalence of shoulder complaints after SOHND is low, and reduces disability in daily activities. Radiation therapy does not have a significant effect on shoulder complaints and disability. Chapter 4 46

48 Introduction Neck dissections are performed as an elective or therapeutic procedure in the treatment of carcinoma of head and neck especially in squamous cell carcinoma. There are three types of neck dissections: radical neck dissection (RND), modified radical neck dissection (MRND), and selective neck dissection (SND). 18 During RND all levels of lymph nodes on one side of the neck, and several important surrounding non-lymphatic structures are resected, including the spinal accessory nerve, internal jugular vein, and sternocleidomastoid muscle. In the MRND all levels are resected, but one or more of the nonlymphatic structures, are spared, usually the spinal accessory nerve. In the SND all non-lymphatic structures are spared. Which type of SND will be performed depends on the location and size of the primary tumour and the risk factors or presence of pathological lymph nodes in the neck. 10,11 Four types of SND are described: supraomohyoid neck dissection (SOHND; level I,II, and III), posterolateral neck dissection (PLND; level II,III,IV, and V) anterior neck dissection (AND; level VI) and lateral neck dissection (LND; level II,III, and IV). 18 Shoulder complaints can be a direct cause of neck dissections and can be presented as; pain, reduced range of motion of the neck and shoulder, loss of sensitivity and loss of shoulder function. Shoulder complaints may have an important influence on quality of life. 21 Prevalence of shoulder complaints after RND range from 47% to 100 %, and from 18% to 77% after MRND (Figure 1). 1,2,6,9,12,19,22,23 Prevalence of shoulder complaints after SND range from 31 % to 40 %. (Table 1) Kuntz concluded that all type of neck dissections affect patients quality of life differently, RND patients had a worse quality of life compared to SND. 13 But the number of studies addressing shoulder complains after SND is small. Additionally the number of patients included in those studies is limited. 3,14,17 Chapter 4 47

49 Figure 1 Prevalence of perceived shoulder pain after radical neck dissection and modified radical neck dissection. Percentages Ewing (1952) R Saunders (1985) R Brown (1988) R Carenfelt (1980) R Krause (1992) R Shone (1991) R Hillel (1989) R Authors Short (1984) R Carenfeld (1980) Mod Saunders (1985) Mod Krause (1994) RR Short (1984) Mod 61 Lower limit Point estimation Upper limit R= Radical neck dissection Mod= Modified radical neck dissection RR= Reconstruction of spinal accessory nerve The influence of radiation therapy is not often described in literature. The available literature suggests radiation therapy to be of importance for shoulder complaints. Nowak described a twenty percent reduction in active range of motion of the shoulder as a result of radiation therapy 16, and according to Schuller radiation therapy adds significantly to permanent disability. 20 The aim of this study was to analyse shoulder complaints after nerve sparing neck dissection, and it s impact on daily activities, and to analyse the influence of radiation therapy on shoulder complaints. Chapter 4 48

50 Material and methods Patients who underwent a neck dissection, in the University Hospital in Groningen, between 1994 and 2000, by either the Department of Oral and Maxillofacial Surgery, Department of Otorhinolaryngology Head & Neck surgery or the Department of Surgical Oncology participated in this study. Patients were informed about this study, by means of an information letter, a week before a standard appointment in our hospital. During this appointment patients were asked to participate in the study. Excluded from the study were patients with recurrence of the tumour at the time of the study and inability to understand the Dutch language. Data concerning the surgery (levels dissected, structures spared, reconstructions), and radiation therapy were collected from a computerized medical record and surgery reports. Shoulder complaints (pain, temporary complaints, reduced range of motion, loss of function) before and after surgery were registered by means of a structured interview. All patients filled out the Shoulder Disability Questionnaire (SDQ). The SDQ evaluates functional status limitation in patient with shoulder complaints, and covers 16 items including: complaints when lying on the affected shoulder, complaints at movements of the shoulder, leaning on the arm, reaching above shoulder level, carrying objects, and complaints when reaching for/to neck or back. The SDQ ratings range from 0 (minimum) to 100 (maximum). A high score indicates more shoulder disability. The SDQ is a reliable and valid questionnaire for Dutch patients with shoulder complaints. 23 Statistical analyses are performed in SPSS 10.0 included: Chi-square analysis t-test for independent samples, linear regression and logistic regression. Confidence intervals were calculated in statistics with confidence (2nd edition). Chapter 4 49

51 Table 1 Percentages and number of patients with shoulder complaints after selective neck dissection compared to modified radical neck dissection and radical neck dissection Follow-up SND MRND RND Leipzig (1983) n=99 6 months 31% (11/36) 36% (10/28) 60% (21/35) Pinsolle (1997) n=127 1 year 39% (16/41) 77% (36/47) 92% (36/39) Cheng (2000) n=21 6 months 29% (2/5) 56% (5/9) 100% (5/5) SND: selective neck dissection; MRND: modified radical neck dissection; RND: radical neck dissection. Results Of the 220 patients who were invited, 154 (70 %) participated in the study (103 men, 51 women), mean age of 61 years (min: 13, max: 88, SD:11.9). The following types of neck dissections were performed: 5 RND, 54 MRND, 22 PLND, 72 SOHND, and 1 Lateral Neck Dissection (LND). Excluded from the statistical analyses were patients after RND (n=5), and LND (n=1) because of the small number of patients. Additionally nine patients who had shoulder complaints before surgery (3 MRND, 5 SOHND, 1 PLND), and two patients who could not remember whether they had preoperative shoulder complaints were excluded (2 SOHND). In the statistical analyses 137 patients were included (89 men, 48 women) mean age 61 years (SD: 12.1). Location of the primary tumour and type of neck dissection are summarized in Table 2. Spinal accessory nerve was sacrificed in one case in the MRND group, and in 1 case in the PLND group. In all SOHND the spinal accessory nerve was spared. The following MRNDs were performed: type 1 (preservation of the spinal accessory nerve); 7, type 2 (preservation of the spinal accessory nerve and internal jugular vein); 5 and type 3 (preservation of the spinal accessory nerve and internal jugular vein and sternocleidomastoid muscle); 38. Chapter 4 50

52 After MRND 33.3% of the patients perceived shoulder complaints, after PLND 66.7 %, and after SOHND 20 % of the patients perceived shoulder complaints. Type of neck dissection was significantly (p <0.001) associated with postoperative shoulder complaints. Follow-up, age, and gender were not significantly related to shoulder complaints (Table 3,4). Table 2 Primary tumour with type of neck dissection and reconstruction s performed Tumor location Type of neck dissection Reconstruction MRND PLND SOHND PM Rad. Fibula Naso. Larynx (n=17) Hypopharynx (n=1) Lip (n=4) Oral Cavity, tongue (n=68) Base of tongue (n=5) Oropharynx (n=16) Thyroid (n=6) Unknown primary (n=5) Others (n=15) Sum (n=137) MRND: modified radical neck dissection, PLND: posterolateral neck dissection, SOHND: supraomohyoid neck dissection. PM: pectoralis myocutaneous flap, Rad: free radialis forearm flap, Fibula: free fibula bone and Naso: nasolabial flap After radiation therapy patients had significantly (p < 0.05) more shoulder complaints. (Table 3). Radiation therapy was given significantly more frequent after PLND (91 %) and MRND (80 %) compared to SOHND (54 %). In logistic regression analyses radiation therapy did not contribute Chapter 4 51

53 significantly to the prediction of shoulder complaints if type of surgery was entered before radiation therapy in the equation. PLND and MRND were performed more frequently on T3-T4 tumors (PLND: 68.8 % (n = 11), MRND 61.9 % (n = 26)), compared to SOHND 34 % (n = 21). Side of neck dissection or bilateral neck dissection was not significantly related to shoulder complaints (Table 3). No significant relationship was found between shoulder complaints, operation side and hand dominance. Table 3 Shoulder complaints after neck dissection: percentages and population analyses Shoulder complaints Gender -Male (n=89) 27.0 % (n=24) -Female (n=48) 41.7 % (n=20) Type of neck dissection (n=137) -MRND (n=51) 33.3 % (n=17)** -PLND (n=21) 66.7 % (n=14)** -SOHND (n=65) 20.0 % (n=13)** Radiation Therapy -RTX yes (n=95) 37.9 % (n=36)* -RTX no (n=42) 19.0 % (n=8) * Side of dissection -Left (n=52) 38.5 % (n=20) -Right (n=55) 25.5 % (n=14) -Bilateral (n=30) 33.3 % (n=10) MRND: modified radical neck dissection, PLND: posterolateral neck dissection, SOHND: supraomohyoid neck dissection * significant p < 0.05 **significant p < (result of Chi-square analyses) In this population 4 types of reconstructions were applied: nasolabial flap (n=9), pectoralis myocutaneous flap (n=9), free radialis forearm flap (n=17) and free fibula bone (n=6). (Table 2) No significant differences in shoulder complaints were found between these types of reconstructions. Chapter 4 52

54 In our population 21 patients had temporarily shoulder complaints after neck dissection, which resolved in time, 12 after MRND, 3 after PLND and 6 after SOHND. The mean scores of the SDQ were: 48.6 (SD:35.1) for the PLND, 22.2 (SD: 28.6) for the MRND, and 11.6 (SD: 26.1) for the SOHND, this difference was significant (ANOVA p < 0.01). The mean score on the SDQ were significantly higher for the patients with radiation therapy, compared to the patients without radiation therapy: mean difference 12.2 (95% CI: 2.1 to 22.3). But in the regression analyses radiation therapy did not contribute significantly to the prediction of the SDQ score. Items most frequently mentioned were: reaching above shoulder level (38 %), rubbing the shoulder more than ones a day (34 %), activities in and around the house (31%), lifting an object (31 %), reaching for the neck (29%) and lying on the affected shoulder (29%). Table 4 Means of follow up and age in patients with and without shoulder complaints after neck dissection Shoulder complaints No shoulder complaints Mean (SD) Mean (SD) 95 % CI of the differences Follow up (years) 3.2 (1.8) 2.9 (1.6) -0.8 to 0.3 Age (years) 61.1 (9.9) 60.9 (12.9) -4.3 to 4.1 Discussion Incidence of shoulder complaints after SOHND are relatively low (20%). Prevalence of shoulder complaints in western population varies from 1.9 % to 26% for subjects between years and from 5% to 34% for people above 65 years. 25 This indicates the low prevalence of shoulder complaints in the group after SOHND. It can even be discussed whether these shoulder complaints are the result of neck dissections or just the natural prevalence of shoulder complaints in the general population. In literature the reported prevalence of shoulder complaints after RND is high (47%-100%). Because of this high prevalence and the extended knowledge of biological behavior of tumours in the head and neck, RND are Chapter 4 53

55 hardly performed anymore in the University Hospital Groningen. In addition SOHND is an adequate procedure in N0 and selected N1 squamous cell carcinomas of the oral and oropharyngeal cavity. 11,15 The prevalence of shoulder complaints after PLND in this study was high. Reasons for this high prevalence may be that a PLND is more extensive (level II,III,IV,V) compared to SOHND (level I,II,III) and the spinal accessory nerve and cervical plexus are manipulated more extensively, especially in level V. It is unclear why the prevalence of shoulder complaints after PLND is much higher compared to MRND. An explanation might be that PLND are more frequently performed on large (T3-T4) tumours of the larynx. Another factor of importance might be the preservation of branches of the cervical plexus. Unfortunately in 61 % of the surgery reports information about preservation or sacrificing of branches of the cervical plexus was missing. In our study radiation therapy had no significant influence on shoulder disability, in contrast to the study of Schuller 20 in which radiation therapy added significantly to shoulder disability. An explanation for this finding is that radiation therapy is significantly associated with type of neck dissection. Neck dissection type is therefore a confounder for radiation therapy. We distinguished selective neck dissections according to Robbins 18 and showed differences in prevalence of shoulder complaints between these dissection types. Several authors did not distinguish the different types of SND. Because of the significant differences in outcome after different kind of SND, SND should be distinguished according to the levels resected during surgery. Furthermore the resected non-lymphatic structures are of importance. Although in selective neck dissections, according to Robbins, all non-lymphatic structures are supposed to be spared, in our population the spinal accessory nerve was sacrificed in one case in a PLND. Shoulder complaints were operationalized with a shoulder disability questionnaire (SDQ). A specific questionnaire to evaluate shoulder complaints is useful to give an indication of shoulder complaints. In our opinion this questionnaire gives more specific information in shoulder dysfunction compared to other often in head and neck cancer research used questionnaires, and can be used in the evaluation of rehabilitation outcome. We did not correct our data for effects of reconstruction s on shoulder complaints. The effects of reconstructions on shoulder complaints are Chapter 4 54

56 described in several studies, mostly containing consequences of pectoral myocutaneous flaps to mobility of the shoulder. Nowak et al. concluded pectoral myocutaneous flaps to have a negative influence on shoulder and neck mobility. Patients were measured pre-treatment, 10-days after surgery, before and upon completion of radiation therapy. Shoulder abduction was 5%-10% lower in the pectoral myocutaneous flap reconstruction group. 16 Haribhakti et al. concluded in a study of patients 14 months after RND, the spinal accessory nerve dysfunction as most important factor on shoulder disability. In addition, the pectoral myocutaneous flap seems to have a negative influence on shoulder abduction. 7 Dijkstra et al. described, in a study in the immediate post-operative clinical phase, a decrease in shoulder forward flexion of 24.5 % in patients with different reconstructions. 5 In our population 29 % of the patients had one of 4 types of reconstruction. No significant differences for shoulder complaints where found within these small groups. Retrospective studies generally do not correct data of post-operative shoulder complaints for pre-operative shoulder complaints. In our study all patient with pre-operative shoulder complaints, and those who did not remember if they had complaints were excluded from this study. Even though recall bias may be of influence on this selection. Patients were invited for the study by means of a letter in which the purpose of this study was explained. This way of invitation may have stimulated selection of patients with shoulder complaints to participate in the study. As a result of this the percentages of shoulder complaints in our study would be an overestimation, and the actual prevalence might be somewhat lower. The invitation was however the same for all types of neck dissection, differences in the prevalence of shoulder complaints between the types of neck dissection seem not to be influenced by this selection bias. This study contains a retrospective study based on one observation after a minimum of 1 year after neck dissection. A prospective study design would have given more information about the process of shoulder complaints in the first postoperative year. We were interested in long-term outcomes. Chapter 4 55

57 In the first year after surgery distress and risk of tumour recurrence are high and will certainly influence the perception of shoulder pain. Also the chance of recovery of shoulder complaints is higher in the first postoperative year. In our population 14 % of the patients had temporarily shoulder complaints, mostly after MRND, in the first postoperative year. If shoulder complaints are the result of neurapraxis of the spinal accessory nerve, recovery of this neurapraxis might occur even long after surgery. Improved shoulder function is mainly described in the MRND group. 13 Beside regeneration of the SAN, effective coping strategies (doing exercises, reducing heavy physical activities), physical therapy 8, and changing of psychological factors 4 may have a positive effect on shoulder complaints. This is why we chose a follow-up for a minimum of 1 year, in contrast to Cheng et al. and Leipzig et al. who used a follow up of 6 months. In conclusion, the prevalence of shoulder complaints after SOHND are low and reduce disability in daily life compared to other neck dissection types. The prevalence of shoulder complaints and disability rates after PLND are high and needs further investigation. Radiation therapy does not have a significant effect on shoulder complaints and disability. Chapter 4 56

58 References 1. Brown H, Burns S, Kaiser CW. The spinal accessory nerve plexus, the trapezius muscle, and shoulder stabilization after radical neck cancer surgery. Ann Surg 1988:208: Carenfelt C, Eliasson K. Occurrence, duration and prognosis of unexpected accessory nerve paresis in radical neck dissection. Acta Otolaryngol 1980:90: Cheng PT, Hao SP, Lin YH, Yeh AR. Objective comparison of shoulder dysfunction after three neck dissection techniques. Ann Otol Rhinol Laryngol 2000:109: de Graeff A, de Leeuw J, Ros WJ, Hordijk GJ, Blijham GH, Winnubst JA. A prospective study on quality of life of patients with cancer of the oral cavity or oropharynx treated with surgery with or without radiotherapy. Oral Oncol 1999:35: Dijkstra PU, van Wilgen PC, Buijs RP, Brendeke W, de Goede CJ, Kerst A, Koolstra M, Marinus J, Schoppink EM, Stuiver MM, de Velde CF, Roodenburg JL. Incidence of shoulder pain after neck dissection: A clinical explorative study for risk factors. Head and Neck 2001:23: Ewing MRMH. Disability following radical neck dissection. Cancer 1952:5: Haribhakti VV, Kavarana NM, Tibrewala AN. Oral cavity reconstruction: an objective assessment of function. Head Neck 1993:15: Herring D, King AI, Connelly M. New rehabilitation concepts in management of radical neck dissection syndrome. A clinical report. Phys Ther 1987:67: Hillel AD, Kroll H, Dorman J, Medieros J. Radical neck dissection: a subjective and objective evaluation of postoperative disability. J Otolaryngol 1989:18: Kligerman J, Lima RA, Soares JR, Prado L, Dias FL, Freitas EQ, Olivatto LO. Supraomohyoid neck dissection in the treatment of T1/T2 squamous cell carcinoma of oral cavity. Am J Surg 1994:168: Kowalski LP, Magrin J, Waksman G, Santo GF, Lopes ME, de Paula RP, Pereira RN, Torloni H. Supraomohyoid neck dissection in the treatment of head and neck tumors. Survival results in 212 cases. Arch Otolaryngol Head Neck Surg 1993:119: Krause HR. Reinnervation of the trapezius muscle after radical neck dissection. J Craniomaxillofac Surg 1994:22: Kuntz AL, Weymuller-EA J. Impact of neck dissection on quality of life. Laryngoscope 1999:109: Chapter 4 57

59 14. Leipzig B, Suen JY, English JL, Barnes J, Hooper M. Functional evaluation of the spinal accessory nerve after neck dissection. Am J Surg 1983:146: Medina JE, Byers RM. Supraomohyoid neck dissection: rationale, indications, and surgical technique. Head and Neck 1989:11: Nowak P, Parzuchowski J, Jacobs JR. Effects of combined modality therapy of head and neck carcinoma on shoulder and head mobility. J Surg Oncol 1989:41: Pinsolle V, Michelet V, Majoufre C, Caix P, Siberchicot F, Pinsolle J. Spinal accessory nerve and lymphatic neck dissection. Rev Stomatol Chir Maxillofac 1997:98: Robbins KT, Medina JE, Wolfe GT, Levine PA, Sessions RB, Pruet CW. Standardizing neck dissection terminology. Official report of the Academy's Committee for Head and Neck Surgery and Oncology. Arch Otolaryngol Head Neck Surg 1991:117: Saunders JR, Hirata RM, Jaques DA. Considering the spinal accessory nerve in head and neck surgery. Am J Surg 1985:150: Schuller DE, Reiches NA, Hamaker RC, Lingeman RE, Weisberger EC, Suen JY, Conley JJ, Kelly DR, Miglets AW. Analysis of disability resulting from treatment including radical neck dissection or modified neck dissection. Head Neck Surg 1983:6: Shah S, Har-El G, Rosenfeld RM. Short term and long term quality of life after neck dissection. Head and Neck 2001:nov: Shone GR, Yardley MP. An audit into the incidence of handicap after unilateral radical neck dissection. J Laryngol Otol 1991:105: Short SO, Kaplan JN, Laramore GE, Cummings CW. Shoulder pain and function after neck dissection with or without preservation of the spinal accessory nerve. Am J Surg 1984:148: van-der Heijden G, Leffers P, Bouter LM. Shoulder disability questionnaire design and responsiveness of a functional status measure. J Clin Epidemiol 2000:53: van der Windt DAWM, Croft PR. Shoulder pain. In: Crombie IK, ed.: Epidemiology of pain. Seattle: IASP press 1999: 257. Chapter 4 58

60 CHAPTER 5 SHOULDER COMPLAINTS AFTER NECK DISSECTION; IS THE SPINAL ACCESSORY NERVE INVOLVED? C.P. van Wilgen, PT 1,2, P.U. Dijkstra, PT, MT, PhD 1,2, B.F.A.M. van der Laan, MD, PhD 3, J.Th. Plukker, MD, PhD, 4 J.L.N. Roodenburg, DDS, MD, PhD 5 1. Department of Oral and Maxillofacial Surgery, 2. Department of Rehabilitation, 3. Department of Otorhinolaryngology, Head & Neck Surgery, 4. Department of Surgical Oncology, University Hospital Groningen. British journal of oral and maxillofacial surgery (2003) 41,

61 Summary The purpose of the current study was to investigate the relation between shoulder morbidity (pain and range of motion), and the function of the spinal accessory nerve after neck dissection. Identifying dysfunction of the nerve gives insight in the mechanisms of post-operative shoulder complaints. In total 112 patients after neck dissection (73 male/ 39 female), mean (SD) age 61 (13) years, participated in the study. The mean duration of follow up was 3 (2) years. Five patients had radical, 43 modified radical, 48 supraomohyoid, and 16 posterolateral neck dissection. Thirty-nine complained of shoulder pain of whom 20 (51%) had dysfunction of the spinal accessory nerve, and 19 (49%) did not. In total 29 patients (26%) had dysfunction of the spinal accessory nerve of whom 20 (69%) had shoulder pain. Shoulder pain was significantly related to dysfunction of the nerve (p < 0.001). Twenty-three patients had a difference in active range of motion in shoulder abduction of 40, of whom 22 (96%) had dysfunction of the nerve. A difference in active shoulder abduction of 40 was significantly related to loss of function of the spinal accessory nerve (p < 0.001). Conclusion: Shoulder pain after neck dissection can only be attributed to dysfunction of the spinal accessory nerve in about 50%. If patients experience shoulder pain after neck dissection examination of the trapezius muscle and active bilateral abduction of the shoulder should be made to find out if the spinal accessory nerve is involved. Chapter 5 60

62 Introduction Neck dissections are either elective or therapeutic procedures in the treatment of cancer of head and neck. Ewing was one of the first to describe shoulder complaints after radical neck dissection. 1 These complaints consisted of reduced range of motion, reduced strength in the trapezius muscle, pain, disfigurement, and disability in daily activities. In that study of 100 patients, 47% developed shoulder complaints after radical neck dissection. These were attributed to resection of the spinal accessory nerve. Other authors have described higher incidences after radical neck dissection, ranging from 47 % to 100%. 1-3 Resection of the nerve during radical neck dissection usually leads to loss of function of the trapezius muscle, but in some cases the muscle will function normally, because of the innervation by branches from the cervical plexus. Innervation from the cervical plexus may be through connections with the spinal accessory nerve, or through an independent double motor supply directly to the trapezius muscle. An independent double innervation by means of the nerve, and the cervical plexus is present in about 18 % of patients. 4 The trapezius muscle is innervated solely through the cervical plexus in 6 % of patients. 5,6 Krause stated that in about 25 %, radical neck dissection will not lead to loss of function of the trapezius muscle if enough cervical branches are preserved. 5 Because of the high incidence of shoulder complaints after radical neck dissection, modified and selective neck dissections with preservation of the spinal accessory nerve were developed. 7 However, even with preservation of the nerve, shoulder complaints developed in 18% to 77% after modified radical neck dissection, 2,8,12 and in 29% to 39% after selective dissection. 2,11,12 Shoulder complaints after nerve-preserving procedures were still attributed to dysfunction of the spinal accessory nerve. However, Cheng et al. in a small study described shoulder complaints after neck dissections with no dysfunction of the nerve. He described 5 patients after radical neck dissection who complained of shoulder pain, but only four had signs of loss of function of the trapezius muscle. Additionally in a group of 7 patients after selective neck dissection, 2 had pain with no signs of loss of function of the trapezius muscle. 2 On the other hand, loss of function of the trapezius muscle does not always affect the shoulder. Saunders et al. showed in a study of 100 patients after Chapter 5 61

63 radical and modified radical neck dissections that there was a weak relation between shoulder complaints (pain, ache, numbness, and weakness), and physical signs of loss function of the trapezius muscle (atrophy, shoulder drop, winging of the scapula, and reduced abduction). 9 The purpose of the current study was to investigate the function of the spinal accessory nerve after neck dissections, and the relation between it s function, shoulder pain, and range of motion of the shoulder. Materials and methods Patients who had a neck dissection done by the multidisciplinary Head and Neck Oncology Group of the University Hospital Groningen, during the period 1994 to 2000, were invited to participate in the study. A week before they visited the hospital for a regular follow-up appointment, all patients were sent a letter telling them about the study. During the appointment they were asked by the physician to participate in the study. After given written informed consent they were included in the study. Patients with bilateral neck dissection, recurrence of the tumour, or who were unable to understand Dutch were excluded. All patients had a follow up of at least 1 year after neck dissection. From the medical record, the following data were retrieved: date of operation, type of resection, type of neck dissection, whether the spinal accessory nerve or the cervical plexus or both were preserved, the type of reconstruction, stage and whether they had preoperative or postoperative radiotherapy. Neck dissections were classified as described by Robbins et al. 7 In this classification lymph nodes of the neck are divided into 6 anatomical levels, and types of neck dissection are divided into: radical, modified radical, and four types of selective dissections. We also looked for extended posterolateral neck dissections in which parts of the trapezius muscle and the splenius muscle are sacrificed. 13 Function of the spinal accessory nerve was assessed by examining the trapezius muscle. 5,9,14 This examination included: visual and palpable signs of atrophy of the trapezius pars descendens muscle during shrugging of the shoulders; visual signs of shoulder drop; and quantifying scapula posture by measuring the distance of the superior angle of the scapula to the spine. The side of the neck dissection was compared to the non-dissected side, and if there was a difference of 2 cm or more a change in scapula posture was recorded. Chapter 5 62

64 If a patient had two or three signs of loss of function of the trapezius muscle we assumed that the spinal accessory nerve was malfunctioning as a consequence of the neck dissection. This may be caused by neurapraxia or neurotmesis. Shoulder pain was evaluated by means of an interview. Beside pain in the shoulder on the dissected side we also recorded pain on the non-dissected side, and whether the patient had shoulder pain preoperatively. Shoulder pain was measured with a numbered visual analogue scale VAS from 0 to 10. They were asked to report their mean painscore over the last week. Active abduction of the shoulder of the dissected and non-dissected sides were measured with an inclinometer. The patient stood with the back, heels, and buttocks against the wall, and were asked to abduct both arms to the maximum of their ability. Reduced abduction was assumed if the difference between the dissected and non-dissected side was 40. All patients were measured by the same observer. Statistical analyses were made using the statistical package for the social sciences 10.0 (SPSS Inc.,Chicago) and Chi-square analysis, and Student s t-test for independent samples. Probabilities of less than 0.05 were accepted as significant. Results In total 122 patients participated in the study, (41 female/ 81 male) mean age 61 (13) years, and mean follow-up of 3 (1-7) years. All patients with shoulder complaints before operation (n=7), and patients who could not remember whether they did or did not (n=2) were excluded from further analyses. Of the remaining 113; 5 underwent radical, 43 modified radical, 48 supraomohyoid, 16 posterolateral, and 1 lateral neck dissection. Before statistical analyses the patient with the lateral neck dissection was excluded. The spinal accessory nerve was dissected in all radical neck dissections, and in one modified radical, and one posterolateral neck dissection. Chapter 5 63

65 Table 1 Characteristics of the 112 patients. Gender: -Female -Male Age (years) Mean (SD) 61 (13) Type of neck dissection: -Radical -Modified radical -Supraomohyoid -Posterolateral Radiotherapy: -Yes -No Tumour stage: -T1 -T2 -T3 -T4 -Unknown Reconstructions: -No -Nasolabial -Pectoral cutaneuos flap -Radial cutaneous flap -Fibula 39 (35) 73 (65) 5 (4) 43 (38) 48 (43) 16 (14) 75 (67) 37 (33) 17 (15) 31 (28) 15 (13) 24 (21) 25 (22) 84 (75) 5 (4) 8 (7) 13 (12) 2 (2) Data are number (%) expect were otherwise stated In total the records of 112 patients (73 male/ 39 female) mean age 61 (13) years were analysed. The mean (SD) follow-up was 3 (2) years. Their characteristics are summarised in Table 1. Table 2 shows the relation between the type of neck dissection and the signs of dysfunction of the trapezius muscle. Thirty-nine patients (35%) complained of shoulder pain of whom 19 (49%) had no dysfunction of the nerve, and 20 (51%) did. Dysfunction was present in 29 patients, of whom 20 (69%) had shoulder pain. Shoulder pain was significantly associated with Chapter 5 64

66 dysfunction of the nerve (Table 3). Sixteen (14 %) patients reported temporary shoulder complaints after neck dissection, that were no longer present at the time of the study. The cervical plexus was preserved in 30 patients (27%), sacrificed in 6 (5 %), partially sacrificed in 5 (4 %) and it was unknown in 71 (63 %) of the patients. From these data we could not analyse the contribution of the cervical plexus to the function of the trapezius muscle. Table 2 Assessment of trapezius muscle and scapula as signs of dysfunction of the spinal accessory nerve, in patients after radical, modified radical, posterolateral, and supraomohyoid neck dissection. Type of neck dissection Number of patients Atrophy of trapezius Shoulder drop Scapula distance > 2 cm Spinal accessory nerve dysfunction* Radical (100) Modified radical (28) Postero lateral (56) Supraomohyoid (6) Total (26) 33 (29) 28 (25) 29 (26 ) Data are number of patients having each type of neck dissection who were affected. Percentages of totals are in parentheses. *Two or three signs of loss of function of the trapezius muscle function present The mean (SD) VAS for patients with shoulder pain was 4.2 (2.3). Nine patients perceived shoulder pain on the non-dissected side (VAS 4.2 (2.6)). Active range of motion (abduction) was measured in 111 patients, and the mean (SD) active abduction on the operated side 146 (42 ), was significantly less than on the non-operated side 162 (26 ). There was a difference in active range of motion of 40 in 23 patients, which was significantly associated with dysfunction of the spinal accessory nerve (Table 3). Chapter 5 65

67 Table 3 Dysfunction of the spinal accessory nerve in relation to shoulder pain, and active range of motion (abduction) after neck dissection Number of patients Dysfunction No dysfunction P values Shoulder pain (51) 19 (49) No shoulder pain 73 9 (12) 64 (88) Total (26) 83 (74) Difference 40 * (96) 1 (4) Difference < (8) 81 (92) Total 111# 29(26) 82 (74) Data are number (%) of patients. Percentages are row percentages. * Difference in abduction between the dissected side and the non-dissected side # One patient was not physically examined Discussion Dysfunction of the spinal accessory nerve occurs in all cases after neck dissection with resection of the nerve and in about 22 % when it is preserved. It may cause shoulder pain but such pain may also be present in 49 % of the cases without signs of dysfunction. Shoulder pain can be attributed to dysfunction of the spinal accessory nerve in only 51% of patients. As well as by a physical examination the function of the nerve can also be investigated by an electromyography (EMG), which provides information about the extent of denervation. However there is a strong relation between EMG findings and the findings of physical examination of the shoulder girdle. 15,16 The active range of motion of the shoulder girdle decreases after neck dissection, particularly if the nerve has been resected. 17 A common way of evaluating the descending trapezius muscle is to elevate the shoulder girdle, but because the levator scapulae also elevates the shoulder girdle, this is not a valid method. A clinical interview, and simple physical examination several weeks after neck dissection is a useful way of accessing the function of the spinal accessory nerve and complaints about the shoulder. The physical examination after neck dissection should include bilateral active Chapter 5 66

68 abduction and inspection of the shoulder girdle, looking for atrophy of the trapezius muscle, changed posture of the scapulae, and shoulder drop. We assumed that the nerve was not functioning if two of three physical signs of dysfunction of the trapezius were present. Only one physical sign might be caused by postoperative immobilisation by pain, neck dissection, or the primary resection. We therefore arbitrarily choose two physical signs out of three. All patients who were known to have had the nerve resected had at least two signs of dysfunction. Shoulder pain has been claimed to be a consequence of dysfunction of the accessory nerve, and although there is a significant relationship, only 51 % of the patients with shoulder pain had a dysfunctional nerve. Different tissues have been suggested to be responsible for shoulder pain, in patients with dysfunction of the spinal accessory nerve: a secondary frozen shoulder, 18 a hypertrophic sternoclavicular joint, 19 and over-stretching of the rhomboid and levator scapulae muscle. 20 As well as these tissues, damage to or cutting of cutaneous sensory nerves causing deafferentation pain, or neuromas, may also cause shoulder pain. 21 Why many patients have shoulder pain after neck dissection with a normal nerve function is unknown. Deafferentation pain, myofascial pain or neuromas may be the cause. 20 Of the patients with a dysfunctional spinal accessory nerve 9 of 29 (31%) had no shoulder pain, and 7 had no major change in abduction. These findings of dysfunction without shoulder complaints are similar to the findings of Saunders et al. 9 Patients in that study had atrophy of the trapezius, shoulder drop, and a changed position of the scapula but did not develop pain or a big reduction in the range of motion. Probably these patients managed to cope with the dysfunction, which makes them an interesting group for further investigation. After neck dissection with preservation of the nerve, neurapraxia may result in a loss of function of the trapezius muscle. Several authors have hypothesised about the causes of this: traction during the operation, microtraumata or devascularisation of the nerve during, or as a consequence of the operation. 22,23 The chance for microtraumata may be more likely because of the anatomical variations in the course of the nerve, particularly in the passage of the sternocleidomastoid muscle, which may lead to more extensive damage. 12,22 Looking into the course of the nerve, the most important levels are II and V. At level V the C3 and C4 branches can be Chapter 5 67

69 damaged by the surgeon, and preservation of level V is probably the main reason why supraomohyoid neck dissection cause less morbidity of the nerve. The prevalence of dysfunction in posterolateral neck dissections should be, according to the dissected level II and V, comparable to that in modified radical neck dissections, but in our study the incidence is considerably higher. A reason for this might be that posterolateral neck dissections are more likely to be done in combination with removal of large tumours in the larynx. In this study no extended posterolateral neck dissections, in which the trapezius muscle is partly dissected, were found. The preservation of the cervical plexus may decrease the incidence of shoulder pain in 25 %. 5 In our group all seven patients in whom the spinal accessory nerve was sacrificed lost function in the trapezius muscle. Of these seven, in one the cervical plexus was sacrificed, one was partly sacrificed, and in the others cases it was unknown. So no conclusions can be drawn about the function of the cervical plexus after neck dissection. It seems worthwhile to detect, and to preserve the branches of the cervical plexus, and to try to spare or damage these branches as little as possible. This sparing mainly consists the preparation of level V in which the branches of C3 and C4 are located. Our retrospective study was based on observations at least a year after neck dissection. Because of the long follow up (mean 3 years), recall of preoperative shoulder problems may have been biased, and missing data because of incomplete medical records resulted in little information about preservation of branches of the cervical plexus. We were interested in long term outcome and did not include patients within a year after neck dissection. In the first year after operation psychological distress and risk of recurrence of the tumour are high, and may influence perception of shoulder pain. Shoulder pain may also recover during the first postoperative year. Fourteen percent of the patients in our group had temporary shoulder complaints, mostly after modified radical neck dissection, in the first year. If shoulder complaints are the result of neurapraxia of the spinal accessory nerve, regeneration might occur even after the first postoperative year. Regeneration has mainly been described after modified radical neck dissection. 24 As well as regeneration, effective coping strategies, reducing heavy physical activities, physiotherapy, 25 and changes in psychological factors 26 may reduce pain and disability. Chapter 5 68

70 In this group nine patients (8%) had shoulder complaints on the unoperated side. According to epidemiological research in a western population this is a low percentage. 27 Based on the results of this study we conclude that shoulder pain after neck dissection can only partly (51%) be attributed to neurotmesis or neurapraxia of the spinal accessory nerve. Further investigations into the causes of shoulder pain, with and without dysfunction of the nerve, is required, and is important for postoperative rehabilitation. Chapter 5 69

71 References 1. Ewing MRMH. Disability following radical neck dissection. Cancer 1952; 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: Remmler D, Byers R, Scheetz J, et al. A prospective study of shoulder disability resulting from radical and modified neck dissections. Head Neck Surg 1986; 8: Krause HR. Reinnervation of the trapezius muscle after radical neck dissection. J Craniomaxillofac Surg 1994; 22: Krause HR. Shoulder-arm-syndrome after radical neck dissection: its relation with the innervation of the trapezius muscle. Int J Oral Maxillofac Surg 1992; 21: Stacey RJ, O'Leary ST, Hamlyn PJ. The innervation of the trapezius muscle: a cervical motor supply. J Craniomaxillofac Surg 1995; 23: Robbins KT, Medina JE, Wolfe GT, Levine PA, Sessions RB, Pruet CW. Standardizing neck dissection terminology. Official report of the Academy's Committee for Head and Neck Surgery and Oncology. Arch Otolaryngol Head Neck Surg 1991; 117: Carenfelt C, Eliasson K. Occurrence, duration and prognosis of unexpected accessory nerve paresis in radical neck dissection. Acta Otolaryngol 1980; 90: Saunders JR, Hirata RM, Jaques DA. Considering the spinal accessory nerve in head and neck surgery. Am J Surg 1985; 150: Short SO, Kaplan JN, Laramore GE, Cummings CW. Shoulder pain and function after neck dissection with or without preservation of the spinal accessory nerve. Am J Surg 1984; 148: Leipzig B, Suen JY, English JL, Barnes J, Hooper M. Functional evaluation of the spinal accessory nerve after neck dissection. Am J Surg 1983; 146: Pinsolle V, Michelet V, Majoufre C, Caix P, Siberchicot F, Pinsolle J. [Spinal accessory nerve and lymphatic neck dissection]. Rev Stomatol Chir Maxillofac 1997; 98: Plukker JT, Vermey A, Roodenburg JL, Oldhoff J. Posterolateral neck dissection: technique and results. Br J Surg 1993; 80: Chapter 5 70

72 14. Fialka V, Vinzenz K. [Physiotherapy and diagnosis of shoulder lesions after radical neck dissection]. Dtsch Z Mund Kiefer Gesichtschir 1989; 13: Sobol S, Jensen C, Sawyer W, Costiloe P, Thong N. Objective comparison of physical dysfunction after neck dissection. Am J Surg 1985; 150: Zibordi F, Baiocco F, Bascelli C, Bini A, Canepa A. Spinal accessory nerve function following neck dissection. Ann Otol Rhinol Laryngol 1988; 97: Dijkstra PU, van Wilgen PC, Buijs RP et al. Incidence of shoulder pain after neck dissection: A clinical explorative study for risk factors. Head Neck 2001; 23: Patten C, Hillel AD. The 11th nerve syndrome. Accessory nerve palsy or adhesive capsulitis? Arch Otolaryngol Head Neck Surg 1993; 119: Cantlon GE, Gluckman JL. Sternoclavicular joint hypertrophy following radical neck dissection. Head Neck Surg 1983; 5: Nori S, Soo KC, Green RF, Strong EW, Miodownik S. Utilization of intraoperative electroneurography to understand the innervation of the trapezius muscle. Muscle Nerve 1997; 20: Brown H, Burns S, Kaiser CW. The spinal accessory nerve plexus, the trapezius muscle, and shoulder stabilization after radical neck cancer surgery. Ann Surg 1988; 208: Soo KC, Guiloff RJ, Oh A, Della RG, Westbury G. Innervation of the trapezius muscle: a study in patients undergoing neck dissections. Head Neck 1990; 12: Shankar K, Means KM. Accessory nerve conduction in neck dissection subjects. Arch Phys Med Rehabil 1990; 71: Kuntz AL, Weymuller-EA J. Impact of neck dissection on quality of life. Laryngoscope 1999; 109: Herring D, King AI, Connelly M. New rehabilitation concepts in management of radical neck dissection syndrome. A clinical report. Phys Ther 1987; 67: de Graeff A, de Leeuw J, Ros WJ, Hordijk GJ, Blijham GH, Winnubst JA. A prospective study on quality of life of patients with cancer of the oral cavity or oropharynx treated with surgery with or without radiotherapy. Oral Oncol 1999; 35: Chapter 5 71

73 27. van der Windt DAWM, Croft PR. Shoulder pain. In: Crombie IK, Croft PR, Linton SJ, Leresche L, Korff von M, eds. Epidemiology of pain. Seattle: IASP Press, 1999: Chapter 5 72

74 CHAPTER 6 MORBIDITY OF THE NECK AFTER HEAD AND NECK CANCER THERAPY C. Paul van Wilgen, PT 1,2,Pieter U. Dijkstra, PhD 1,2, Berend F.A.M. van der Laan, PhD 3,John T. Plukker, PhD 4, Jan L.N. Roodenburg, PhD 1 1.Department of Oral and Maxillofacial Surgery, 2. Department of Rehabilitation, 3. Department. of Otorhinolaryngology, Head & Neck Surgery, 4. Department of Surgical Oncology. University Hospital Groningen. Accepted Head and Neck (december 2003) 73

75 Abstract Background Studies on morbidity of the neck after head and neck cancer therapy are described scarcely. Methods Patients who underwent surgery, including neck dissection, with and without radiation therapy, at least 1 year before the study were asked to participate. We assessed neck pain, loss of sensation, range of motion of the cervical spine, and shoulder pain. Results Of the 220 patients who were invited 153 (70 %) participated in the study. Neck pain was present in 33% of the patients (n=51), and shoulder pain in 37% of the patients (n=57). Neuropathic pain of the neck was present in 32% (n=49), myofascial pain was present in 46% (n=70), and joint pain in 24% (n=37). Loss of sensation of the neck was present in 65% (n=99) and was related to type of neck dissection and radiation therapy. Range of motion of the neck was significantly decreased, because of the neck dissection and or radiation therapy in lateral flexion away from the operated side. Conclusion The occurrences of morbidity of the neck after cancer therapy were considerable and consisted of neck pain, loss of sensation, and decreased range of motion. Chapter 6 74

76 Introduction Head and neck tumours account for 10 % of all new cancer diagnoses in The Netherlands. 1 The treatment of head and neck tumours consists of surgery, radiation therapy or both. During surgery, often an elective or therapeutic neck dissection is performed. As a result of head and neck cancer therapy, morbidity of neck and shoulder region may occur. This morbidity manifests itself through pain, loss of sensation, disfigurement, reduced range of motion of the shoulder, and changes in quality of life. 2,3,4,5 Morbidity of the neck itself has only been described in small number of studies. Neck tightness was reported in 71% of the cases, together with shoulder discomfort in 53% of the cases, having a substantial negative effect on quality of life. This was reported by Shah et al. 6 in a retrospective study of 51 patients after different types of neck dissection. Head and neck pain was reported by Chaplin et al. 2 in 25% of 93 patients after neck dissection, radiation therapy, or both. In a study of 25 patients with persistent neck pain after neck dissection, Sist et al. 7 described two types of neck pain: neuropathic pain (100%) and myofascial pain (72%). In contrast to these studies Talmi et al. 8 described three groups of patients (n=88) after radical and modified radical neck dissection and claimed that pain in the neck after neck dissection was uncommon. The results of previous studies regarding the presence of neck pain after head and neck cancer therapy are conflicting. It is unclear whether the type of neck dissection has any relationship with the occurrence of neck pain. The exact cause of neck pain after neck dissection was unclear. Besides neuropathic pain, other causes have been described: sternoclavicular joint pain caused by subluxation 9 or hypertrophy 10 and myofascial pain in head and neck muscles. 11 Loss of sensation after selective neck dissection related to sacrificing the sensory cervical root branches. For the analyses of loss of sensation, Saffold divided the neck in eight regions. After neck dissection in which the sensory cervical root branches were sacrificed, significantly more sensory deficits were present than in neck dissections in which the sensory cervical root branches were preserved. 12 Loss of sensation after neck dissection, including dissection of the sensory nerve branches, was reported most frequently in the regions D, E, and F (Figure 1). However, loss of sensation of the neck could Chapter 6 75

77 also be related to radiation therapy. 13 To the best of our knowledge, no other studies have evaluated the loss of sensation after neck dissection adequately. Figure 1 Regions in the neck for the assessment of loss of sensation after Saffold Region A: represents the lower half of the external ear, extending from the root of the helix to the tip of the lobule. Region B: is the midface and includes the face above a line drawn between the oral commissure and the angle of the mandibule. Region C: the lower face, extends from below this line (region b) to the inferior border of the mandible. The neck is divided into upper and lower portions based on a horizontal line at the level of the thyroid prominence. Region D: is the upper posterior neck behind the anterior border of the sternocleidomastoideus. Region E: is the upper anterolateral neck, extending from the anterior border of the sternocleidomastoideus to a vertical line drawn from the facial notch of the mandible. Region F: is the lower posterior neck behind the anterior border of the sternocleidomastoideus Haribhakti et al. described impairment of neck movement after neck dissection and additional reconstruction. They found no differences in patients with or without a pectoralis major myocutaneous flap. 14 Both Schuller et al. and Haribhakti et al. used questionnaires, without a physical examination or measuring the range of motion. Studies measuring the range of motion of the cervical spine after neck dissection were not available. The aim of our study was to analyze neck morbidity, including neck pain and loss of sensation and range of motion of the neck after head and neck cancer therapy, and to study the relationship between morbidity and type of neck dissection, number of dissected levels, radiation therapy, and shoulder pain. Materials and Methods Patients who un derwent a neck dissection with or without radiation therapy, performed by the multidisciplinary Head and Neck Oncology Group of the University Hospital Groningen in the period 1994 to 2000, were asked to participate. They were informed about the study by a personal letter, which was send 1 week before they visited the hospital for an appointment as part Chapter 6 76