The Effects of Cranio-Cervical Flexion on Activation of Swallowing-Related Muscles in Stroke Patients and Age-Matched Healthy Adults

Transcription

1 The Effects of Cranio-Cervical Flexion on Activation of Swallowing-Related Muscles in Stroke Patients and Age-Matched Healthy Adults Hee-Soon Woo The Graduate School Yonsei University Department of Occupational Therapy

2 The Effects of Cranio-Cervical Flexion on Activation of Swallowing-Related Muscles in Stroke Patients and Age-Matched Healthy Adults A Dissertation Submitted to the Department of Occupational Therapy and the Graduate School of Yonsei University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Hee-Soon Woo December 2012

3 This certifies that the dissertation of Hee-Soon Woo is approved. Thesis Supervisor: Soo Hyun Park Minye Jung Eunyoung Yoo Ji-Hyuk Park Jin Lee The Graduate School Yonsei University December 2012

4 Acknowledgements First of all, I thank and praise God for preparing and guidance this thesis. This thesis would not have been possible without individuals who offered their valuable assistance and strong support to prepare and complete this study. It is great pleasure to express my sincere gratitude to them in my humble acknowledgement. First and foremost I would like to convey my gratitude to my advisor, Dr. Soo Hyun Park for her excellent guidance, advice and supervision throughout this research work. She has supported me with her expertise and patiently encouraged me to bring out my best, allowing me to grow as a researcher and a scholar. The tireless passion and enthusiasm for her research was an important key which motivated me to purse my degree. Furthermore, she encouraged me not only in this work but also in my growth as an independence thinker. I gratefully acknowledge Professor Minye Jung, Professor Eunyoung Yoo, Professor Ji-Hyuk Park and Professor Jin Lee for their faith in me to be a good scholar. I also sincerely appreciate Professor Kiyeon Chang whose advice, academic experience and vast knowledge taught me a great deal. Their endless passion and commitment in occupational therapy has been driving force for me to

5 keep moving forward when frustrated. Additionally, I am indebted to professor at Woosong University for their strong support and encouragement with their best wishes. I would also like to express my deep gratitude to all members of the graduate school, Department of Occupational Therapy. Last but not the least, I would like to show my deepest gratitude to my family. This dissertation would be impossible without them. With their great care and affection, I finished my graduate course and earned doctoral degree in occupational therapy. I owe my loving thanks to my fiancé, Sunyoung. Without her understanding and persistent confidence in me, I would never finish this work. Never satisfied with my own achievement, I will continue to work to make further progress. Thank You.

6 Table of Contents List of Figures ii List of Tables iii Abstract iv Introduction 1 Materials and Methods 7 1. Participants 7 2. Pressure Biofeedback Unit Surface electromyography Procedures Statistical analysis 23 Results Activation of swallowing-related muscles in supine position Activation of swallowing-related muscles in sitting position 29 Discussion 33 Conclusion 38 References 39 Abstract in Korean 50 - i -

7 List of Figures Figure 1. Pressure Biofeedback Unit, Stabilizer 13 Figure 2. Attaching position of electrodes 15 Figure 3. Participants swallowed liquid placed in the mouth when they heard the beep sound 13 Figure 4. Two group s study diagram 17 Figure 5. Neutral position (left) and CCF (right) applied to the neck 22 Figure 6. Activation of swallowing-related muscles in the healthy group during supine position 25 Figure 7. Activation of swallowing-related muscles in the clinical group during supine position 28 Figure 8. Activation of swallowing-related muscles in the healthy group during sitting position 30 Figure 9. Activation of swallowing-related muscles in the clinical group during sitting position 32 - ii -

8 List of Tables Table 1. General characteristics of the participants 8 Table 2. FDS mean score of the clinical group 10 Table 3. Difference in muscle contraction by pressure level in the healthy group during supine position 26 - iii -

9 ABSTRACT The effects of cranio-cervical flexion on activation of swallowing-related muscles in stroke patients and agematched healthy adults Hee-Soon Woo Dept. of Occupational Therapy The Graduate School Yonsei University The cranio-cervical flexion (CCF) is a common means of postural control in the clinical setting and is equivalent to head flexion. The CCF is a low-load posture to target the deep cervical muscles, longus capitis, and longus colli. This clinical posture has been designed to assess the tonic holding abilities of the deep neck flexors. Both longus capitis and longus colli, located deeply at the posterior airway and esophagus in pairs play a vital - iv -

10 role in controlling cervical posture and maintaining stability. Weakening of these muscles decrease efficiency of muscles and leads to excessive movement of the chin and head during postural control and movement. Anatomically, swallowing-related muscles are located superficially in the same region as the SCM and anterior scalene. Based on such fact, we assumed that CCF may influence swallowing-related muscles as well as superficial neck flexors. The purpose of this study was to investigate changes in swallowing efficiency by applying CCF to stroke patients experiencing swallowing problems due to neurologic disorders in comparison with application of CCF to age-matched asymptomatic adults. Also, most of earlier studies on application of CCF investigated activation of superficial neck flexor following neck stabilization by placing subjects in the supine position. However, to associate the effects of CCF with swallowing-related muscles, investigation of the sitting position which is the actual eating position in the real world is essential. In this study, we investigated whether the effect is same by applying CCF in both the supine and sitting position. Through this study, we demonstrated that when CCF was applied, in both groups activation of swallowing-related muscles was significantly changed compared to the neutral neck position. More specifically, when CCF was applied, participants swallowed the same amount of liquid with less muscle activation in the swallowing-related muscles, and such findings were found across both the supine and sitting positions. This shows that swallowing-related muscles, located in the same area as the superficial neck flexor - v -

11 muscles, were also affected by the CCF. When it is applied to individuals with proper postural guidance and understanding of the mechanism of neck stabilization with CCF is fostered, it could be a more effective therapeutic approach for swallowing difficulties. The results of this study suggest that CCF can be recommended as a method which enhances the effectiveness of swallowing-related muscles in stroke patients with pharyngeal weakness and healthy adults in the same age range. When CCF is applied, the stability of deep flexor muscles can be secured after which superficially located muscles may better assist swallowing the same amount of liquid with less effort. As individuals with various dysphagic symptoms show decreased effectiveness of swallowing-related muscles, our results could be regarded as theoretical evidence for better safe swallowing methods. Key Words : Cranio-cervical flexion, Dysphagia, Pharyngeal weakness, Stroke patients, Swallowing-related muscle - vi -

12 Introduction Activation of swallowing-related muscles plays a pivotal role in safe swallowing. Therapeutic focus in dysphagia rehabilitation programs typically aims at improving the individual s ability to swallow by increasing the efficiency of swallowing in the clinical setting (Huckabee, Butler, Barclay, & Jit, 2005). The cranio-cervical flexion (CCF) (Jull, 2000; Jull, Barrett, Magee, & Ho, 1999) is a common means of postural control in the clinical setting and is equivalent to head flexion. The CCF was originally proposed by Jull et al. in 1998 as a method for indirect measurement of the activation of the deep neck flexors in order to direct therapeutic exercise to those stabilizing muscles where strength deficits were found (Hudswell, Mengersen, & Lucas, 2005). The CCF is a low-load posture to target the deep cervical muscles, longus capitis, and longus colli. This clinical posture has been designed to assess the tonic holding abilities of the deep neck flexors. It has been based on anatomical grounds - that is, head flexion or a head nodding movement is the action of longus capitis and colli and not the action of other superficial neck flexors such as sternocleidomastoid (SCM) and the scalene (Jull, 2000). Both longus capitis and longus colli, located deeply at the posterior airway and esophagus in pairs play a vital role in controlling cervical posture and maintaining stability (Falla, Jull, & Hodges, 2008). There is some functional specificity between superficial and deep flexors (Vasavada, Li, & Delp, 1998). Superficial muscles, SCM and - 1 -

13 anterior scalenes are major contributors to flexion torque while deep cervical flexor (DCF) muscles (longus capitis and colli) have an important role in supporting the cervical curve and segments in posture and movement (Mayoux-Benhamou, Revel, Vallee, Roudier, Barbet, & Bargy, 1994; Vasavada et al., 1998). Weakening of DCF muscles decrease efficiency of muscles and leads to excessive movement of the chin and head during postural control and movement (Jull et al., 1999; Jull, O'Leary, & Falla, 2008). Of clinical and functional relevance, reduced activation of the DCF muscles has been identified in association with increased activation of the superficial flexor muscles in studies using the CCF in patients with a variety of neck disorders (Dusunceli, Ozturk, Atamaz, Hepguler, & Durmaz, 2009; Falla, Jull, & Hodges, 2004; Sterling, Jull, Vicenzino, Kenardy, & Darnell, 2003). Head flexion, which is the same position as the CCF, has been typically investigated to judge safer swallowing by simply changing positions of anatomical structures. The chin-down or chin-tuck maneuver is a postural technique widely used in dysphagia treatment. According to Logemann (1998), the chin-down posture is helpful if patients have a delay in triggering the pharyngeal swallow, reduced tongue base retraction, and/or reduced airway entrance closure. The chin-down maneuver is a head and neck posture in the anterior direction. In biomechanics and functional anatomy, it is well known that flexion and extension movements of the cervical spine involve coordinated motions in two anatomical areas: one is the occipito-atlanto (C1)-axial (C2) complex and the other is the lower cervical (C2-C7) region (Okada et al., 2007). Therefore, in the biomechanical - 2 -

14 or functional anatomical sense of the term, there are two kinds of flexion and their combination. Movement between occipito-atlanto-axial joints can occur independent of movements below C2, but most flexion and extension in the cervical segments occur between C5 and C6 (DeLisa & Gans, 1998). Flexion of the occipito-atlanto and atlantoaxial joints can be called flexion of the head on the neck (head flexion, CCF), while flexion of the lower cervical spine is called neck flexion (Hislop & Montgomery, 2002). In both flexions, only head flexion increases efficiency of superficial neck flexors by activating deep neck flexors (Woo, Park, Jung, Yoo, & Park, 2012). Anatomically, swallowing-related muscles are located superficially in the same region as the SCM and anterior scalene. Based on such fact, we assumed that CCF may influence swallowingrelated muscles as well as neck flexors. In the previous study, we found the efficiency or effectiveness of swallowing-related muscles increased linearly when CCF was applied in normal adults (Woo et al, 2012). However, because the sample in this study consisted of young asymptomatic adults, we cannot conclude that CCF is also effective in older adults with swallowing problems or to populations who have neurologic disorders (Cagnie, Danneels, Cools, Dickx, & Cambier, 2008; Falla, Campbell, Fagan, Thompson, & Jull, 2003; Falla, Jull, & Hodges, 2004; Uthaikhup & Jull, 2009). Cerebral, cerebellar, or brain stem strokes can impair swallowing physiology. Cerebral lesions can interrupt voluntary control of mastication and bolus transport during the oral phase (Daniels, Brailey, & Foundas, 1999; Zald & Pardo, 1999). Cortical lesions involving the precentral gyrus may produce contralateral impairment in facial, lip, and - 3 -

15 tongue motor control, and contralateral compromise in pharyngeal peristalsis (Veis, & Logemann, 1985). Cerebral lesions causing impairments in cognitive function such as concentration or selective attention may also impair control of swallowing (Ertekin, Aydogdu, Tarlaci, Turman, & Kiylioglu, 2000). Brain stem strokes are less common than cortical lesions but result in the largest swallowing compromise. Brain stem lesions can affect sensation of the mouth, tongue, and cheek, timing in the trigger of the pharyngeal swallow, laryngeal elevation, glottic closure, and cricopharyngeal relaxation (Martino, Terrault, Ezerzer, Mikulis, & Diamant, 2001; Veis & Logemann, 1985). Regardless of lesion location, because stroke is more common in the elderly (Devroey, Van Casteren, & Buntinx, 2003), normal age-related swallowing difficulties could further compound stroke-related dysphagia. The elderly post-stroke patients may no longer be able to compensate for normal changes in skeletal muscle strength that reduce mastication (Jaradeh, 1994) or diminish lingual pressure (Nicosia et al., 2000). These physiologic changes affect pharyngeal phase in swallowing and lead to various swallowing problems including aspiration. Also, there is evidence to suggest that there exist differences in neuromuscular function and morphology depending on age. Changes in neuromuscular function in the back muscles have been demonstrated in elders compared to younger subjects (Brown, Mills, & Baker, 1994) and there is evidence of age-related changes in neuromuscular morphology (Akataki, Mita, Watakabe, & Ito, 2002; Faulkner, Larkin, Claflin, & Brooks, 2007; Kim, Suzuki, & Kanda, 2007; Vandervoort, 2002). The actual performance of the - 4 -

16 CCF requires accurate application and thus may also be influenced by cognitive factors, in addition to learning and motor skill acquisition in the elderly (Cabeza, Daselaar, Dolcos, Prince, Budde, & Nyberg, 2004; Mattay et al., 2002; O Sullivan, Jones, Summers, Morris, Williams, & Markus, 2001). Stroke, one of the most frequent neurologic disease, mainly occurs in older age groups and is accompanied by physical and cognitive disabilities (Hartman-Maeir, Harel, & Katz, 2009; Rogers, Coe, & Hartke, 2002; Wallenbert & Jonsson, 2005). Cognitive impairment due to stroke not only includes decrease in communication function required to express the swallowing difficulty to clinician, but also decrease in thinking skills required to understand therapeutic strategy of clinicians and apply it to oneself (Rogers et al., 2002). CCF also could be understood as a simple position that requires just making head flexion, but a certain level of cognitive function is essential to apply it distinctly from another neck flexion involving the 5 th and 6 th cervical spine. In respect to neurological impairments due to stroke, patients with upper motor neuron disease like stroke develop spastic weakness of muscles. As a result, they show slow movements in body control and decrease in range of motion. This affects swallowing function, so speed of swallowing is delayed and range of motion in swallowing-related structures is decreased (Groher & Crary, 2010). Therefore, patient groups with neurologic symptoms have a higher possibility of physiologic change of swallowing. Head flexion and neck flexion are often used indiscriminately in dysphagia treatment (Okada et al., 2007). However, the effect of each movement is different. Head flexion - 5 -

17 allows the superior laryngeal inlet to be more vertically positioned so that they could be free from aspiration. Even if there is penetration, the severity of penetration can decrease because the esophagus and pharynx are situated more perpendicularly (Bülow, Olsson, & Ekberg, 2001; Ekberg, 1986). On the other hand, neck flexion reduces the distance between the hyoid bone and larynx while widening the vallecular space so that it gives more time to control bolus in patients with delayed swallowing reflex (Bülow, 1986; Logemann, 1998). It is essential that definite separation of the two movements be made when applying such pressures for the purpose of promoting efficiency of muscles other than anatomical effects as mentioned earlier because only head flexion activates deep neck muscles in both flexions (Woo et al., 2012). The purpose of this study was to investigate changes in swallowing efficiency by applying CCF to stroke patients experiencing swallowing problems due to neurologic disorders in comparison with application of CCF to age-matched asymptomatic adults. Also, most of earlier studies on application of CCF investigated activation of superficial neck flexor following neck stabilization by placing subjects in the supine position (Hudswell et al., 2005; Jull, 2000; Jull et al., 1999). However, to associate the effects of CCF with swallowing-related muscles, investigation of the sitting position which is the actual eating position in the real world is essential. In this study, we investigated whether the effect is same by applying CCF in both the supine and sitting position

18 Materials and Methods 1. Participants For this study, two experimental groups were selected. Experimental group 1 consisted of older adults without any swallowing problems. This group was selected to investigate whether the positive effects of CCF on the efficiency of swallowing-related muscles are similar not only in young healthy adults (Woo et al., 2012) but also in older healthy adults. Experimental group 2 consisted of individuals with dysphagia experiencing pharyngeal weakness secondary to stroke to investigate whether CCF affects the swallowing-related muscles in a clinical sample of individuals with neurological disorders. A total of 25 healthy participants composed the experimental group 1 (8 men and 17 women) between the ages of 43 and 64 years (Table 1). Participants were excluded if they reported a history of orthopedic disorders affecting the neck, neurological disorders, or had participated in a neck exercise program within the past 2 months that may affect the results of the study. In addition, either participants who complained of pain during swallowing or those who were aware of problems with swallowing functions were excluded

19 Table 1. General characteristics of the participants Group 1 (healthy group, N=25) Group 2 (clinical group, N=22) Age (years) ± 5.75 a ± 9.59 a Gender (M/F) 8 / / 8 Height (cm) ± 8.21 a ± 9.97 a Weight (kg) ± 8.85 a ± a a Values are mean ± SD Twenty-two (14 men and 8 women) participants with stroke without risk of aspiration to fluid intake with plain yogurt viscosity through videofluoroscopic swallowing study (VFSS) and could understand the purpose of this study formed experimental group 2. Clinical group was selected to include those who show symptoms in more than one item in the 7 items (delayed triggering of pharyngeal swallow, reduced laryngeal elevation and epiglottic closure, nasal penetration, residue in valleculae, residue in pyriform sinuses, coating of pharyngeal wall after swallow, and delayed pharyngeal transit time) which is indicative of weakness in the pharyngeal phase in the total 11 items of the Functional Dysphagia Scale (FDS; Han, Paik, & Park, 2001). Current nutritional status of the 22 participants were as follows: Nine participants totally depended on naso-gastric tube, six participants depended on 80% nutrient supply - 8 -

20 by naso-gastric tube but they could participate in oral feeding training using thickened fluid. Seven participants were able to oral feed using thickened dysphagia diet (Table 2)

21 Table 2. Functional Dysphagia Scale (FDS) mean score of the clinical group (N=22) Factor Value Score Mean ± SD Intact 0 Lip closure Inadequate ± 1.97 None 10 Intact 0 Bolus formation Inadequate ± 1.29 None 6 None 0 Residue in oral 10% 2 cavity 10-50% ± % 6 Oral transit time 1.5sec 0 >1.5sec ± 1.28 Triggering of Normal ± 4.29 pharyngeal swallow Laryngeal elevation and epiglottic closure Nasal penetration Residue in valleculae Residue in pyriform sinuses Coating of pharyngeal wall after swallow Pharyngeal transit time Delayed 10 Normal 0 Reduced 12 None 0 10% % 8 50% 12 None 0 10% % 8 50% 12 None 0 10% % 8 50% 12 No 0 Yes sec 0 >1.0sec ± ± ± ± ± ± 2.04 Total 1.89 ±

22 Also, participants were limited to individuals who could understand the instructions of this study and follow 3-step command. All participants signed a consent form after receiving verbal and written information regarding the study

23 2. Pressure Biofeedback Unit Inflatable pressure biofeedback units (Stabilizer TM, Chattanooga Group Inc., Hixson, USA) (Figure 1) were calibrated with weights to check that they showed the same linear relationship between applied loads and pressure changes in the ranges used for this study. The pressure biofeedback unit consists of an inflatable cushion connected to a pressure gauge and an inflation device. Participants were instructed to use the visual feedback provided by the analog gauge of the pressure biofeedback unit in order to maintain the determined target pressure during CCF. The pressure biofeedback unit is reported to have a tolerance of 10 mmhg of pressure (Hudswell et al., 2005)

24 Figure 1. Pressure Biofeedback Unit. Stabilizer TM

25 3. Surface Electromyography Surface electromyographic (semg) activity was detected from the supra-hyoid muscle group (anterior belly of the digastric, mylohyoid, geniohyoid, and platysmus) and infrahyoid muscle group (omohyoid, sternohyoid, and thyrohyoid) using custom made surface bipolar Ag/AgCl electrodes (20 mm disc electrode, inter-electrode distance: 20 mm, 3M Corp, Saint Paul, MN, USA) (Figure 2). The participant s skin was first cleaned with an alcohol swab, and then two pair of electrodes were attached one above and one below the hyoid bone. The ground electrode was placed on the upper thoracic spine. The semg signal was obtained using WEMG-8 system (Laxtha Inc., Daejeon, South Korea). A WEMG system is composed of 8 electrodes, a preamplifier for initial processing, a second amplifier, an A/D converter of 16-bit resolution, a USB connection, and a WEMG-8-type cable

26 Figure 2. Attaching position of electrodes. semg activity was detected from the suprahyoid and infra-hyoid muscle group

27 The raw EMG signal was processed using Telescan 2.8 software (Laxtha Inc, Daejeon, South Korea) at a sampling frequency of 1024 Hz with 60-Hz notch filter for noise reduction associated with electrical interference arising from the usual sources including 60 Hz power lines or radio frequencies, and electric or magnetic devices. To obtain a measure of semg signal of swallowing-related muscles, peak amplitude was calculated using same software during swallowing reflex (Figure 3). For normalization, peak amplitude values per swallowing were recorded for 0.1 second period before and after the recording for a total of 0.2 second. This was converted into root mean square (RMS) to be expressed as a percentage of the reference voluntary contraction (RVC). A standard value of RVC was the capacity to contract muscles in the supine position while swallowing 20cc of plain yogurt. In addition, in order to obtain contraction power of only the swallowing-related muscles on the semg, we subtracted the neck flexors signal that had increased while applying CCF

28 Figure 3. Participants swallowed liquid placed in the mouth when they heard the beep sound. We could see that the swallowing-related muscles were activated (suprahyoid muscle group upper line; infrahyoid muscle group lower line)

29 4. Procedures Participants were asked to comfortably lie with their arms crossed over their chest, with the head supported on folded towels so that the neck assumed neutral alignment with the body. The temperature of the room was kept stable for the duration of the study. The pressure biofeedback unit was placed between the plinth and the posterior aspect of the neck just under the sub-occipital region and inflated to a baseline of 20mmHg (Chiu, Law, & Chiu, 2005). A standard approach to participant education was used before testing. The testing position consisted of a pure head nod while in the supine position, and required both care and precision for correct performance. Signs of incorrect performance, such as posterior retraction of the chin to push the neck directly back onto the sensor, were corrected by the examiner during the practice phase. The CCF posture followed the protocol described by Jull and colleagues (2008). The participants were instructed to perform and hold inner range positions of CCF while attempting to maintain the superficial flexor muscles relaxed. The participants were first taught to perform slowly and control CCF progressively. They were subsequently trained to hold increasing ranges of CCF using feedback from the air-filled pressure sensor. Each participant was reminded to relax the neck musculature and to concentrate on performing a gentle, nodding head movement. Each participant was instructed to perform the CCF movement at 3 different pressure levels (20, 30, and 40 mmhg) provided in random sequence to minimize order effect and to swallow 20cc of plain yogurt while maintaining CCF at each pressure level. The

30 activation of the each swallowing-related muscles was measured through semg. In order to improve reliability of the data, we utilized the average values which were measured three times at the same level of swallow pressure. A break of 2 minutes was allowed between each pressure level condition to minimize fatigue. In this within-participants repeated design study, the experiment proceeded with two different positions. Experiment in the sitting position was aimed to show whether similar effects can be found when the position changed from supine to sitting position, because swallowing of food usually occurs while sitting. The order of two positions was assigned randomly for each participant, and we placed a 30-minute rest period between the two position conditions. The participants sat on a chair, and they were positioned with their hip, knee, and ankle flexed at an angle of 90 degrees. Their feet were placed on the floor naturally by adjusting the seated height of the chair. We applied only two positions in the sitting condition because when applying CCF in the sitting position, not enough pressure was able to be transferred to the pressure biofeedback unit positioned in the sub-occipital region. The two positions were neutral neck and head flexion. Also, in the clinical group, application of the 3 pressure levels (20, 30 and 40mmHg) was difficult because some participants showed maximal pressure below 40mmHg when applying CCF in the supine position. As such, we applied neutral and CCF position in another format. More specifically, participants took instruction to push the stabilizer positioned behind the neck with maximal strength when applying CCF. General study flow according to group is like Figure

31 Healthy group supine sitting 20mmHg 30mmHg 40mmHg Neutral CCF Clinical group supine sitting Neutral CCF Neutral CCF Figure 4. Two group s study diagram. Each group was investigated when they received CCF effects in 2 different positions (supine, sitting)

32 The participants were encouraged to make head flexion only while not using neck flexion. We positioned a transparent 5cm section paper in front of participant to make sure whether the participant have made neck flexion. If movement of a marker attached 1cm below the ear was detected, we assumed that neck flexion had occurred. In this case, re-education was provided before the participant assumed the position again (Figure. 5). Maintaining this position, they were requested to swallow 20cc of plain yogurt. We compared semg activity obtained in this neck flexion sitting position with activity during swallowing in the neutral sitting position

33 Figure 5. Neutral position (left) and CCF (right) applied to the neck. If marker on the posterior inferior side of the ear moved, we assumed the movement as a neck flexion, not CCF

34 5. Statistical analysis In the supine position, the independent variables were the pressure of the stabilizer (20, 30, and 40 mmhg) and the dependent variables were normalized %RVC values in each muscle groups (supra-hyoid and infra-hyoid muscles). To verify the statistical significance of the dependent variables according to pressure level, one-way-repeated ANOVA was applied (p = 0.05) using SPSS v12.0 (SPSS, Inc., Chicago, IL, USA). In the sitting position, the independent variables were neutral neck position and head flexion position. The dependent variables were same as in the supine position. Paired t test was applied (p=0.05) to verify statistical significance of the dependent variables depending on neck position

35 Results 1. Activation of swallowing-related muscles in supine position The activation of swallowing-related muscles when CCF was applied in the supine position is presented in Figure 6. With increasing CCF pressure, muscle activation in the suprahyoid and infrahyoid muscle group decreased while swallowing the same amount of liquid (p <.05). In the healthy group, when the pressure level of the stabilizer escalated, there was a significant difference in activity of swallowing-related muscles compared to the baseline level

36 * * % 80 R V C mmhg 30 mmhg 40 mmhg 0 Suprahyoid muscles** Infrahyoid muscles** Muscle groups * p<.05 Figure 6. Activation of swallowing-related muscles in the healthy group during supine position

37 Post-hoc test was applied using LSD to investigate the differences of muscle contraction power according to the each muscle s pressure in supine position in the healthy group. Suprahyoid and infrahyoid muscles did not show significant difference in the 10mmHg change. However, they showed statistically significant difference in the 20mmHg change (Table 3). Table 3. Difference in muscle contraction by pressure level in the healthy group during supine position Muscle Groups Suprahyoid muscles Level (mmhg) Mean difference (% RVC) p * Infrahyoid muscles * * p<

38 In the clinical group, the activation of swallowing-related muscles when CCF was applied in the supine position is presented in Figure 7. When CCF was applied, muscle activation in the suprahyoid and infrahyoid muscle group decreased during swallowing the same amount of liquid (p <.05)

39 * * % R V C Neutral CCF 0 Suprahyoid muscles* Infrahyoid muscles** Muscle groups * p <.05 Figure 7. Activation of swallowing-related muscles in the clinical group during supine position

40 2. Activation of swallowing-related muscles in sitting position Wilcoxon sign rank test was conducted to examine the effects of CCF used as neck stabilization on activation of swallowing-related muscles in the sitting position. The activation of swallowing-related muscles when CCF was applied is presented in Figure 8. In the healthy group, there was a significant difference in activity of the swallowingrelated muscles compared to the neutral neck position when CCF was applied

41 * * % R V C Neutral CCF 0 Suprahyoid muscles* Infrahyoid muscles** Muscle groups * p<.05 Figure 8. Activation of swallowing-related muscles in the healthy group during sitting position

42 In the clinical group, there was a significant difference in activity of the swallowingrelated muscles compared to the neutral neck position when CCF was applied. This means that in both groups, we could get the effects of CCF application irrespective of neurologic symptoms (Figure 9)

43 * * % R V C Neutral CCF 0 Suprahyoid muscles* Infrahyoid muscles** Muscle groups * p <.05 Figure 9. Activation of swallowing-related muscles in the clinical group during sitting position

44 Discussion This study was conducted to examine the effects of CCF on activation of swallowingrelated muscles in stroke patients with pharyngeal weakness and healthy adults in the same age range. Through this study, we demonstrated that when CCF was applied, in both groups activation of swallowing-related muscles was significantly changed compared to the neutral neck position. More specifically, when CCF was applied, participants swallowed the same amount of liquid with less muscle activation in the swallowingrelated muscles, and such findings were found across both the supine and sitting positions. This result shows that swallowing-related muscles, located in the same area as the superficial neck flexor muscles, were also affected by the CCF regardless of pharyngeal weakness. Through this, when it is applied to individuals with proper postural guidance and understanding of the mechanism of neck stabilization with CCF is fostered, it could be a more effective therapeutic approach for swallowing difficulties. Activation of swallowing-related muscles plays a pivotal role in safe swallowing (Barofsky, 1995; Kahrilas, Logemann, Lin, & Ergun, 1992). Therefore, therapeutic focus in dysphagia rehabilitation programs typically aims at improving the individual s ability to swallow by increasing the efficiency of swallowing in the clinical setting (Huckabee et al., 2005). While there are various therapeutic strategies being applied to alleviate symptoms of dysphagia, the exercise programs are usually used in order to strengthen swallowing-related muscles over a period of 4 to 6 weeks (Ding, Larson, Logemann, &

45 Rademaker, 2002; Shaker et al., 2002). Although many studies have demonstrated its therapeutic effects, therapists have expressed a need for a therapeutic approach which could show more immediate effects (Huckabee et al., 2005). The methods which are currently being used to promptly activate swallowing-related muscles are effortful swallowing (Huckabee et al., 2005; Kahrilas et al., 1992) and biofeedback using semg (Barofsky, 1995; Crary, 1995; Huckabee & Cannito, 1999), for example. Through the results of our study, CCF may be another method that can exert an almost immediate effect on swallowing-related muscles by changing neck position. Furthermore, CCF could be applied as a method of improving muscle effectiveness in the stroke patient group showing pharyngeal weakness due to neurologic disease as well as normal healthy adults. The great significance of this study is that this study proved that CCF position could be applied as an additional method to raise effectiveness of muscles, the CCF position called head flexion, chin down which make safer swallowing by only physical changes of anatomical structures (Ekberg, 1986; Karaho, 1999; Welch et al., 1993). A number of clinicians, including this author, reported that individuals with dysphagia swallow foods with more ease when they use head flexion for the purpose of reducing risk for aspiration, and a number of studies have supported such observations. For example, Sakuma and colleagues (2010) reported that head flexion resulted in more easy swallowing in nine healthy subjects. In addition, Bülow and colleagues (1999) suggested that head forward flexion position reduced pharyngeal contraction, similar to the results of the present study. However, previous studies did not outline potential physiologically

46 based reasons for changes in swallowing ease or contraction depending on head position. The results of the present study may explain in part the reasons for such changes, namely through the association between swallowing-related muscles and CCF which is usually applied as a neck stabilization technique or for neck pain reduction. As previously mentioned, CCF secures neck stability by activating the deep neck flexor, and based on the secured stability, CCF will increase the effectiveness of swallowing-related muscles positioned in superficial neck flexor muscles. Head flexion and neck flexion are often used indiscriminately in dysphagia treatment (Okada et al., 2007). However, the purpose of each movement is different. Head flexion allows the superior laryngeal inlet to be more vertically positioned so that they could be free from aspiration. Even if there is penetration, the severity of penetration can decrease because the oesophagus and pharynx are situated more perpendicularly (Bülow, 2001; Ekberg, 1986). On the other hand, neck flexion reduces the distance between the hyoid bone and larynx while widening the vallecular space so that it gives more time to control bolus in patients with delayed swallowing reflex (Bülow, 2001; Logemann, 1998). Our study shows that only the head flexion position can lead to effectiveness of the swallowing-related muscles by applying the CCF. These results may provide a basis for a more clear distinction between the two neck positions. Also, Figure 6 and Table 3 show the linear increasing of effectiveness of swallowingrelated muscle by securing more neck stabilization although same CCF position. This means maximal muscle effectiveness could be obtained by applying most effective

47 position though understanding clear mechanism of CCF position not to simply apply CCF. The best therapeutic technique which may compensate the weakened swallowing-related muscle could be applied when swallowing induced by maximal contraction position of deep cervical muscles through maximal head flexion. The results of this CCF study indicate that for individuals demonstrating dysphagia symptoms, especially for individuals showing weakness during the pharyngeal phase, immediately increasing the efficiency of swallowing-related muscles may potentially allow such individuals to swallow more safely and with more ease. Moreover, such technique was found to be effective not only in the supine position but also in the sitting position. In stroke patients who show inadequate bolus manipulation in oral cavity, the oral intake in supine position is a contraindication because a premature bolus loss causes direct aspiration before activating airway protection mechanism (Logemann, 1998). As a result, verifying the effectiveness of CCF in the sitting position through this study is an essential process from the point of view of a clinician who guide the oral intake of patients. In conclusion, CCF may reflect the concept of proper positioning for functional eating. In other words, it aligns body position by activating deep muscles, simultaneously providing a base which enables swallowing-related muscles to move more efficiently. However, the following are the limitations of this study. First, dysphagia symptoms show different physiologic characteristics according to the brain lesion, but this study did not consider this aspect in selecting participants. Second, We only used pure water in

48 examining swallowing-related muscle activity. Further study is needed to determine the effects of CCF while swallowing different forms and density of food

49 Conclusion The results of this study suggest that CCF can be recommended as a method which enhances the effectiveness of swallowing-related muscles in stroke patients with pharyngeal weakness and healthy adults in the same age range. When CCF is applied, the stability of deep flexor muscles can be secured after which superficially located muscles may better assist swallowing the same amount of liquid with less effort. As individuals with various dysphagic symptoms show decreased effectiveness of swallowing-related muscles, our results could be regarded as theoretical evidence for better safe swallowing methods

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