Temporal and Biomechanical Measurements of Upper Esophageal Sphincter (UES) Opening in Normal Swallowing

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1 Temporal and Biomechanical Measurements of Upper Esophageal Sphincter (UES) Opening in Normal Swallowing Youngsun Kim School of Hearing, Speech and Language Sciences, College of Health and Human Services, Ohio University, Athens, Ohio, USA Correspondence to Prof. Youngsun Kim, PhD, CCC-SLP School of Hearing, Speech and Language Sciences, College of Health and Human Services Ohio University, Grover Center W218 Athens, OH tel.: Background & Objectives: The purpose of this study was to examine the temporal and biomechanical differences of duration and width of the UES opening among people of different ages and genders during normal swallowing. Methods: Videotapes of videofluoroscopic swallowing examinations (VFSEs) of 69 normal subjects were analyzed. Results: Results yielded a significant effect for age between younger and older subjects for both duration of UES opening (DUESO) and maximum width of UES opening (MWUESO) (p <.01). No gender differences were observed. Discussion & Conclusion: These differences may be related to muscle weakness with aging. However, older subjects did not show aspiration. These normal data of UES opening will be used for comparisons with stroke patients who exhibit aspiration in future research. (Korean Journal of Communication Disorders 2009;14; ) Key Words: upper esophageal sphincters (UES), swallowing, temporal, biomechanical, age Ⅰ. Introduction The upper esophageal sphincter (UES), referred to as the cricopharyngeal region, is a muscle located on the superior portion of the esophagus. The UES is an area that spans 2~4cm (Logemann, 1998). It is an area of great pressure, which increases during inspiration or just before swallowing in order to form a valve into the esophagus (Cook et al., 1989a; 1989b). Its purpose is to restrict airflow into the esophagus and prevent objects from entering pharynx and larynx from the esophagus. Relaxation of UES muscle occurs as the bolus approaches the esophagus (Kahrilas et al., 1988). The UES must work in conjunction with the hyoid bone to achieve sufficient UES opening (Dodds et al., 1988). The other mechanisms that affect the UES opening are the vagus nerve (CN X), which is responsible for sending a signal for UES relaxation, and force of the bolus, which applies pressure to the UES adding force to open it (Crary & Groher, 2003). The amount of UES opening can vary greatly based on the volume of the bolus. However, once a bolus becomes larger than 10ml, the increase becomes minimal. With age comes some variability in UES opening during the swallow. Age-related changes of swallowing include a slowing of the musculature. While this alone will not cause dysphagia, it increases the risk of dysphagia (Crary & Groher, 2003). Findings indicated that individuals over age 70 have a prolonged UES opening duration (Robbins et al., 1992). In addition, residue in pyriform sinus is more often seen in older men than in younger subjects, and the UES opening is smaller in older subjects than younger subjects (Logemann et al., 2000; 2002). Some gender differences were also Received January 20, 2009 Final revision received March 10, 2009 Accepted March 14, c 2009 The Korean Academy of Speech-Language Pathology and Audiology 109

2 Korean Journal of Communication Disorders 2009;14; noted. Duration of UES opening was longer in older men than in younger women. The width of UES opening in women increased with age (Logemann et al., 2002). Aspiration in dysphagic patients may result from inhalation of pyriform sinus residue due to a poor UES opening (Kendall, Leonard & McKenzie, 2004). Reduced duration and/or limitedwidth of UES opening can also be an indicator in determining risk of aspiration. While delayed and/or reduced hyoid and laryngeal excursion and subsequent reduced in UES opening contribute to aspiration, any effects on UES function are multi-faceted and must be examined from different perspectives. There are limited reports regarding UES opening in normal swallowing, all of which assess only a small number of subjects. However, there was, to our knowledge, no comprehensive investigation using a large number of subjects to study the age and gender differences of UES opening by using both temporal and biomechanical measures. The purpose of this study was to examine the temporal and biomechanical differences in duration and width of the UES opening in different ages and genders during normal swallowing. This study will supply much needed objective and quantitative data and will provide a reliable measurement of the UES opening for evidence-based practice. Ⅱ. Method 1. Subjects Videotapes of videofluoroscopic swallowing examinations (VFSEs) were collected for a previous investigation (McCullough, Wertz & Rosenbek, 2001). In this study, VFSEs of 69 normal subjects were analyzed. Subjects were divided into two age groups based on previous studies revealing age differences (Tracy et al., 1989; Kim, McCullough & Asp, 2005). Of the individuals examined, 41 subjects were between the ages of 21 and 55, and 28 were between the ages of 65 and 87. The younger group had 20 males and 21 females, and the older group had 15 male and 13 females. Each subject passed a comprehensive questionnaire, a clinical cranial nerve examination, and an oral motor/ structural examination prior to participation in the study. Subjects with any neurological or structural abnormality affecting the head and neck were excluded. 2. Videofluoroscopic swallowing examination (VFSE) Subjects were seated upright in a stretcher chair and filmed with a mobile C-arm x-ray (OEC Diasonics, model 7600) system. The study was recorded onto a Panasonic Super VHS PV-S7670 Pro Line Multiplex videocassette recorder. The fluoroscopic tube was focused in a lateral plane on the oral cavity from the lips anteriorly to the pharyngeal wall posteriorly and from the nasopharynx superiorly to just below the UES area. Each subject firstswallowed two 5ml and then two 10ml thin liquid boluses (50/50 mixture of E-Z-HD Barium Sulfate Powder for Suspension). None of the subjects exhibited signs of dysphagia or aspiration during the VFSE. All swallows appeared to be normal for tongue and pharyngeal constriction, epiglottic closure, and UES opening. 3. Procedures for temporal and biomechanical measurement of UES opening This study focused on one temporal measurement (duration of UES opening: DUESO) and onebiomechanical measurement (maximum width 110

3 Kim / Temporal and Biomechanical Measurements of Upper Esophageal Sphincter(UES) Opening in Normal Swallowing of UES opening: MUESW) in normal swallowing. A total of 271 swallows were analyzed for this study, and 5 swallows were excluded due to poor visibility of UES zone in VFSEs. To accurately analyze UES opening, the VFSE S-VHS tapes were digitized using Adobe Premier Pro 1.5, a video editing program, and a Sony DVMC-DA1 Media Converter. Duration of UES opening (DUESO) is measured from the moment the UES opens until the moment theues closes (Robbins et al., 1992, Logemann et al., 2000, 2002). To measure DUESO, each liquid swallow wasanalyzed for the following points of incidence with the 100ms timer: (1) initial opening of UES and (2) closure of UES. For MWUESO, one picture frame showing maximum width of UES opening during the swallow was generated for each swallow. Each picture frame was then submitted to the ImageJ 1.32j program (Rashband, 2004). MWUESO was measured at the narrowest point between C4 and C6 during the swallow. The investigators had at least six months of extensive training on temporal and biomechanical analysis of swallowing before joining this investigation. To determine age and gender differences, three-way repeated measurements analyses of variance (ANOVA) were performed (p <.05) for each measurement. Independent variables were age, gender, and volume of the bolus. Ⅲ. Results 1. Reliability For intra-judge reliability, the investigator randomly selected and re-analyzed 10% of the patients VFSE clips. This included 7subjects and 28 swallows. A significant correlation between the first and second judgment was observed (r =.88, p <.01). For inter-judge reliability, a second judge analyzed 10% of the subjects video-clips. The second judge who had undergone training on VFSE biomechanical measures for another investigation re-analyzed the 7 subjects. That judge s results were compared with the results of the primary investigator. A significant correlation was observed between judges (r =.90, p <.01). 2. Age Means, standard deviations, and ranges for duration of UES opening (DUESO) and maximum width of UES opening (MWUESO) separated into age groups for the younger and older subjects are presented in Table 1. Both DUESO (F (1,263) = 13.13, p <.01) and MWUESO (F (1,263) = 9.82, p <.01) were significantly different between younger and older subjects. For both 5ml and 10ml volumes of thin liquid, younger subjects had significantly shorter DUESOs and narrower MWUESOs. For DUESO, younger Figure 1. Three VFSE framessubmitted for the measurements: a.initial opening of UES, b. closure of UES, c. maximum width of UES opening. 111

4 Korean Journal of Communication Disorders 2009;14; subjects had a mean 0.04 sec (0.03sec and 0.06sec, 5ml and 10ml, respectively) shorter duration than the older subjects. For MWUESO, younger subjects had 0.56cm wider opening (0.12cm and 1.02cm, 5ml and 10ml, respectively) than older subjects. These data are provided as a mean bar graph in Figure 2 and 3. Neither DUESO nor MWUESO exhibited volume effect and volume x age interactions. Table 1. Mean and standard deviation (SD) by age differences in duration of UES opening (DUESO) and maximum width of UES opening (MWUESO) Age Young Old Volume DUESO (sec) Mean Standard Deviation MWUESO (cm) Mean Standard Deviation 5ml ml ml ml Figure 2. Mean duration of UES opening (DUESO) by age differences Figure 3. Mean maximum width of UES opening (MWUESO) by age differences Figure 4. Mean duration of UES opening (DUESO) by gender differences Figure 5. Mean maximum width of UES opening (MWUESO) by gender differences 112

5 Kim / Temporal and Biomechanical Measurements of Upper Esophageal Sphincter(UES) Opening in Normal Swallowing 3. Gender Means and standard deviations (SD) for DUESO and MWUESO separated by gender group are presented in Table 2. There was no significant gender difference for either DUESO or MWUESO. For both volume sizes, males had slightly shorter DUESO and narrower MWUESO, but neither was significantly different. In addition, there were no volume effect and volume x gender interaction. These data are provided as a mean bar graph in Figure 4 and 5. Table 2. Mean and standard deviation (SD) by gender differences in duration of UES opening (DUESO) and Maximum width of UES opening (MWUESO) Gender Volume Male Female DUESO (sec) Mean Standard Deviation MWUESO (cm) Mean Standard Deviation 5ml ml ml ml Ⅳ. Discussion and Conclusion The results of this study reported that older populations tend to have longer duration of UES opening than younger populations. This result of duration of UES opening supported the previous investigations (Logemann et al., 2000; 2002). Older populations also exhibited a wider UES opening than younger populations. Longer duration of UES opening and wider maximum UES opening in older populations may be related to changes in motor and sensory functions (Sonies, 1991; Sonies et al., 1988). The results indicate that the initiation and execution of the oropharyngeal muscles of swallowing slow in response to bolus flow after age 75. However, we are not able to determine whether a longer and wider UES opening puts older patients at risk of aspiration. Older subjects did not show signs of aspiration despite different patterns of UES opening. It is necessary to study the difference of UES opening between normal subjects and patients with dysphagia. The desired UES opening requires proper timing and extent of UES opening to accomplish the safe swallowing (Logemann et al., 2000; 2002). The difference of UES opening in younger and older populations in this study may indicate a reduced reserve in neuro-response and muscle strength in pharyngeal swallowing due to aging. In older populations, reduced reserve putsthem into a vulnerable position concerning swallowing safety. In previous studies, Kim, McCullough & Asp (2005), Kim & Park (2007), and Kim & McCullough (2008) reported other temporal and biomechanical indicators of aging, such as delayed and reduced hyoid excursion and laryngeal closurein older populations. Hyolaryngeal excursion helps the UES open and the laryngeal vestibule close by pulling the cricopharyngeal sphincter and lowering the epiglottis (Logemann, 1998). It is necessary to consider the relationship between these pharyngeal activities as a whole in future studies. The entire synchronic sequence of hyolaryngeal excursion and UES opening will provide animportant understanding of the aging process..as people get older, the possibility of having dysphagia caused by illnesses is more likely than in a younger population. The longer duration and reduced width of the UES opening can be compromised by various etiologies including stroke and neurogenic diseases (Logemann et al., 2000). Dysphagia of the UES opening occurs when the sphincter does not open or close properly. It can result in residue above the sphincter and aspiration 113

6 Korean Journal of Communication Disorders 2009;14; (Rademaker et al., 1994). Any illness or trauma that causes muscle weakness can lead to dysphagia (Logemann et al., 2000). Illnesses such as stroke, disease, or cancer of the head and neck are all commonly associated with changes in normal deglutition and UES dysphagia. In patients with oropharyngeal cancer, the duration of the UES opening decreases, and oral and pharyngeal residue is noted to be higher than in the normal population (Rademaker et al., 1994). Despite the many problems that can hinder the opening of the UES, there are a number of treatment protocols that are used to combat UES dysphagia. Muscle exercises can be used to increase the strength of the pressure in the UES. A set of muscle strengthening activities called the Shaker exercises have been shown to significantly improve the opening of the UES during deglutition (Easterling et al., 2005; Shaker et al., 1997; 2002). Through clinical observations, these exercises have also shown to improve management of clear secretions and residue. The temporal and biomechanical data of normal populations will help us compare the progress and effects of an intervention strategy for dysphagic patients. Future research should evaluate these measures for their ability to distinguish between the stroke patients who aspirated and those who did not aspirate. REFERENCES Cook, I. J., Dodds, W. J., Dantas, R. O., Massey, B., Kern, M. K., Lang, I. M., Brasseur, J. G., & Hogan, W. J. (1989a). Opening mechanisms of the human upper esophageal sphincter. The American Journal of Physiology, 257, G Cook, I. J., Dodds, W. J., Dantes, R. O., Kern, M. K., Massey, B. T., Shaker, R., & Hogan, W. J. (1989b). Timing of videofluoroscopic, manometric events, and bolus transit during the oral and pharyngeal phases of swallowing. Dysphagia, 4, Crary, M. A., & Groher, M. E. (2003). Introduction to adult swallowing disorders. Boston, MA: Butterworth- Heinemann. Dodds, W. J., Man, K. M., Cook, I. J., Kahrilas, P. J., Stewart, E. T., & Kern, M. K. (1988). Influence of bolus volume on swallow-induced hyoid Movement in normal subjects. American Journal of Roentgenology, 150, Easterling, C., Grande, B., Kern, M., Sears, K., & Shaker, R. (2005). Attaining and maintaining isometric and isokinetic goals of the shaker exercise. Dysphagia, 20, Kahrilas, P. J., Dodds, W. J., Dent, J. A., Logemann, J. A., & Shaker, R. (1988). Upper esophageal sphincter function during deglutition. Gastroenterology, 95, Kendall, K. A., Leonard, R. J., & McKenzie, S. (2004). Airway protection: Evaluation with videofluoroscopy. Dysphagia, 19, Kim, Y., & Park, T. (2007). Age and gender differences of laryngeal closure duration in normal swallowing, Korean Journal of Communication Disorders, 12, Kim, Y., McCullough, G. H., (2008). Maximum hyoid displacement in normal swallowing. Dysphagia, 23(2), Kim, Y., McCullough, G. H., & Asp, C. W. (2005). Temporal measurements of pharyngeal swallowing in normal populations. Dysphagia, 20, Logemann, J. A. (1998). Evaluation and treatment of swallowing disorders. Austin, TX: Pro-ed. Logemann, J. A., Pauloski, B. R., Rademaker, A. W., & Kahrilas, P. J. (2002). Oropharyngeal swallow in younger and older women. Journal of Speech, Language, and Hearing Research, 45, Logemann, J. A., Pauloski, B. R., Rademaker, A. W., Colangelo, L. A., Kahrilas, P. J., & Smith, C. H. (2000). Temporal and biomechanical characteristics of oropharyngeal swallow in younger and older men. Journal of Speech, Language, and Hearing Research, 43, McCullough, G. H., Wertz, R. T., & Rosenbek, J. C. (2001). Age, gender, size, consistency effects on swallowing function in adults between 21 and 99 years of age. Proceedings of the Dysphagia Research Society 10th annual meeting, Albuquerque, NM. Rademaker, A. W., Pauloski, B. R., Logemann, J. A., & Shanahan, T. K. (1994). Oropharyngeal swallow efficiency as a representative measure of swallowing function. Journal of Speech and Hearing Research, 37, Rashband, W. (2004). Imag J 1.32j. Available from the National Institutes of Health Web site, nih.gov/ij Robbins, J., Hamilton, J. W., Lof, G. L., & Kempster, G. B. (1992). Oralpharyngeal swallowing in normal adults of different ages. Gastroenterology, 103, Shaker, R., Easterling, C., Kern, M., Nitschke, T., Massey, B., Daniels, S., Grande, B., Kazandjian, M., & Dikeman, K. (2002). Rehabilitation of swallowing by exercise in 114

7 Kim / Temporal and Biomechanical Measurements of Upper Esophageal Sphincter(UES) Opening in Normal Swallowing tube-fed patients with pharyngeal dysphagia secondary to abnormal UES opening. Gastroenterology, 122, Shaker, R., Kern, M., Bardan, E., Taylor, A., Stewart, E. T., Hoffmann, R. G., Arndorfer, R. C., Hofmann, C., & Bonnevier, J. (1997). Augmentation of deglutitive upper esophageal sphincter opening in the elderly by exercise. The American Journal of Physiology, 272, G Sonies, B. C. (1991). The aging oropharyngeal system. In D. Ripich (Eds.), Handbook of geriatric communication disorders. Austin, TX: Pro-ed. pp Sonies, B.C., Parent L. J., Morrish, K., & Baum, B. J. (1988). Durational aspects of the oral-pharyngeal phase of swallow in normal adults. Dysphagia, 3, Tracy, J. F., Logemann, J. A., Kahrilas, P. J., Jacob, P., Kobara, M., & Krugler, C. (1989). Preliminary observations on the effects of age on oropharyngeal deglutition. Dysphagia, 4,

8 언어청각장애연구 2009;14; 정상삼킴시상식도조임근열림의시간및생체역학적측정 김영선 오하이오대학교언어병리학과 교신저자김영선오하이오대학교언어병리학과교수 School of Hearing, Speech and Language Sciences College of Health and Human ServicesOhio University Grover Center W218Athens, OH tel.: 목적 : 본연구의목적은연령과성별의차이를보이는정상인의삼킴시상식도조임근열림의시간및생체역학적차이를비교하는것이다. 방법 : 69 명의정상인비디오투시조영검사자료를분석하였다. 결과 : 상식도조임근열림기간과최대넓이에서청장년층과노인층에서유의미한차이를보였다 (p <.01). 그러나성별의차이는없었다. 논의및결론 : 연령에따른상식도조임근의열림기간차이는연령증가에따른노인집단의근육약화때문으로보인다. 그러나이런증상이흡인과같은삼킴장애를일으키지는않는다. 본연구의정상인의데이타는앞으로삼킴장애환자와비교를통해서삼킴시상식도조임근열림에대한이해를돕게될것이다. 언어청각장애연구, 2009;14(1); 핵심어 : 상식도조임근, 삼킴, 시간적, 생체역학적, 연령 게재신청일 : 2009 년 1 월 20 일 최종수정일 : 2009 년 3 월 10 일 게재확정일 : 2009 년 3 월 14 일 c 2009 한국언어청각임상학회 116