Longitudinal analysis of progression of dysphagia in amyotrophic lateral sclerosis

Auris Nasus Larynx 31 (2004) 247–254

Longitudinal analysis of progression of dysphagia in amyotrophic lateral sclerosis Ryuzaburo Higo∗ , Niro Tayama, Takaharu Nito Department of Otolaryngology, Faculty of Medicine, University of Tokyo, 3-1 Hongo 7-chome, Bunkyo-ku, Tokyo 113-8655, Japan Received 12 November 2003; received in revised form 13 April 2004; accepted 21 May 2004 Available online 4 August 2004

Abstract Objective: To investigate the progression of dysphagia in amyotrophic lateral sclerosis (ALS) using videofluoroscopy (VF), according to two different scales: the duration following bulbar symptom onset, and the ALS severity scale (ALSSS). Methods: Seventy-two VF examinations, on 50 ALS patients, were performed at various time points, and the change in VF findings in the oral and pharyngeal phases was analyzed over time following bulbar symptom onset. The change according to advancement of the ALS severity scale was also assessed. Results: Delayed bolus transport from the oral cavity to the pharynx, and bolus stasis at the pyriform sinus (PS), were seen in about half of the patients with no bulbar complaints. In contrast, upper esophageal sphincter (UES) opening was relatively well maintained in the late stage of dysphagia. The other parameters, such as bolus holding in the oral cavity, constriction of the pharynx, and elevation of the larynx, became worse over time following bulbar symptom onset. These parameters on VF examination also became worse as the ALSSS advanced; however, even patients in the group with normal eating habits showed disturbed bolus transport from the mouth to the pharynx, weak constriction of the pharynx, and bolus stasis at the PS. Generally, dysfunction had progressed dramatically, in most of the parameters, in the patients that required modification of food; however, UES opening and elevation of the larynx were relatively well maintained in advanced-ALSSS patients. Conclusion: In this study, we clearly show the progression pattern of dysphagia in ALS, and we also emphasize that VF is a useful tool to follow swallowing function in ALS patients. From our results, it would be useful to perform VF by 6 months following bulbar symptom onset, because VF can contribute to rehabilitation or appropriate diet modification; and later, around 1 year following bulbar symptom onset, VF should again be performed, since ALS patients show wide-ranging nutrition intake patterns, and they need assessment to introduce intervention, such as tube feeding, according to their varying status of dysphagia, around at this time point. © 2004 Elsevier Ireland Ltd. All rights reserved. Keywords: Amyotrophic lateral sclerosis (ALS); Videofluoroscopy; ALS severity scale; Dysphagia

1. Introduction Amyotrophic lateral sclerosis (ALS) is a progressive neurodegenerative disorder that involves, primarily, motor neurons in the cerebral cortex, brainstem, and spinal cord [1]. ALS patients show wide-ranging clinical features, since the disease affects bulbar and/or spinal systems according to the site of motor neuron involvement. As the disease progresses, both upper motor neurons (UMN) and lower motor neurons (LMN) may be affected, and various symptoms overlap [2]. Among various clinical features, bulbar impairment, such as dysarthria and/or dysphagia, generally occurs late in ∗ Corresponding author. Tel.: +81-3-5800-8665; fax: +81-3-3814-9486. E-mail address: [email protected] (R. Higo).

the course of the disease, but it is present at the onset in about one-third of cases [3]. Dysphagia is one of the most critical problems for the ALS patient. ALS patients with swallowing disturbance not only suffer from dehydration and malnutrition but also face aspiration, which may result in aspiration pneumonia and can lead to death. As such, swallowing function in ALS patients should be carefully and appropriately evaluated and followed up during the course of disease progression. Videofluoroscopy (VF) has so far been the most reliable examination to evaluate swallowing function in ALS patients [4], and many videofluoroscopic studies have been reported [4–10]. These reports well described the general patterns of swallowing disturbance in ALS, but they did not assess the progression of dysphagia in ALS patients, and it remains unclear how these dysfunctions change over time.

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Hillel and Miller found the rate of the progression of symptoms to be extremely variable [3]. The rate of progression of bulbar symptoms also varies [2]. Little research has been done to examine the progression of swallowing problems in ALS patients [2], and in particular, no study has used such an objective examination as VF to evaluate the changes of swallowing function in ALS. This report is the first detailed analysis of the progression of dysphagia in ALS patients, by VF examination, seeking to contribute to elucidation of this intractable problem in ALS.

2. Patients and methods 2.1. Patients selection Fifty patients, diagnosed as having ALS at the Department of Neurology in our institute, were referred to our swallowing and speech clinic, for evaluation of swallowing function. According to the El Escorial criteria [1], the following features were evaluated for each patient: (1) signs of LMN degeneration by clinical, electrophysiological, or neuropathologic examination, (2) signs of UMN degeneration by clinical examination, and (3) progressive spread of signs within a region or to other regions, together with the absence of (1) electrophysiological evidence of other disease processes that might explain the signs of LMN and/or UMN degeneration, and (2) neuro-imaging evidence of other disease processes that might explain the observed clinical and electrophysiological signs. The onset of bulbar symptoms (dysarthria and/or dysphagia) was reported by patients, and bulbar signs (UMN signs: spasticity, increased jaw jerk and gag reflex, etc.; LMN signs: weakness and atrophy; fasciculation of muscles of the tongue, palate, and larynx; decreased jaw jerk and gag reflex, etc.) were evaluated by the laryngologists in our swallowing and speech clinic on each visit. 2.2. Videofluoroscopy These 50 patients with ALS were investigated by videofluoroscopy (VF). VF examination was routinely done at the time of a patient’s first visit to our clinic, to assess swallowing function. VF was performed from once to several times, at various time points following bulbar symptom onset. Some patients were unable to return to the clinic after the first visit, for various reasons (e.g. rapid progress of the disease), and therefore only one examination was conducted on 33 patients, while other patients could receive VF evaluation several times (twice, 14 patients; three times, 2 patients; and five times, 1 patient) over the course of the progression of dysphagia, with the repeat examinations performed at 2- to 8-month intervals. As such, a total of 72 VF examinations were performed at various time points following bulbar symptom onset, and these data were statistically analyzed. Manometric examination was also conducted on 21 patients, the results of which were previously reported [11].

Appropriate and safe bolus textures (thin liquid or semisolid) and bolus volumes (1, 3, 5 ml, or self-regulated) were used in each patient. As contrast medium, a 140%/v barium mixture was routinely used, but a water-soluble contrast (Omnipaque 300, Daiichi Pharmaceutical Co., Ltd., Tokyo) was given when a risk of aspiration was suspected. Examination of three viewing planes (anteroposterior, lateral, and right anterior oblique positions) was basically adopted in our protocol, but since many patients in this study could not stand up, the posture of patients and the viewing plane were mainly sitting upright in a wheelchair, and the lateral position. The assessment parameters in VF are set as follows: bolus transport from the mouth to the pharynx, bolus holding in the oral cavity, constriction of the pharynx, elevation of the larynx, bolus stasis at the pyriform sinus (PS), upper esophageal sphincter (UES) opening, and aspiration. A three-point scale: 0 (normal), 1 (disturbed), and 2 (severely disturbed), was used to quantify each parameter, except for aspiration, and for statistical analysis. For aspiration, a two-point scale was used. Informed consent was obtained from each patient, and they were treated according to the Declaration of Helsinki. 2.3. Analysis To analyze the progression of dysphagia in ALS patients, two units were selected as scales in this study: One is the duration (months) following bulbar symptom onset, and the other is the functional ALS Severity Scale (ALSSS) of Hillel et al. [12]. ALSSS well expresses the condition of each patient nutrition intake, and it specifies NORMAL EATING HABITS (normal swallowing or a nominal abnormality, defined as when only the patient notices slight indications of dysphagia, such as food lodging in the recesses of the mouth or sticking in the throat; ALSSS score, 10–9), EARLY EATING PROBLEMS (minor swallowing problems, which allow an essentially regular diet, but the patients have experienced isolated choking episodes or require prolonged time to eat, and they need smaller-size bites; ALSSS score, 8–7), DIETARY CONSISTENCY CHANGES (the diet is limited to primarily soft foods, and some special meal preparation is needed, or nutrition is limited to primarily a liquefied diet; ALSSS score, 6–5), NEEDS TUBE FEEDING (oral intake alone is no longer adequate and supplemental tube feeding is needed, or primary nutrition and hydration are accomplished by tube; ALSSS score, 4–3), and NOTHING BY MOUTH (secretions managed by an aspirator and/or medications, or aspiration of secretions that cannot be managed non-invasively; ALSSS score, 2–1). Changes in each parameter on VF examination were assessed, over time (duration) following bulbar symptom onset, and over the advancing ALSSS score. Relationships between these scales and the assessment parameters on VF examination were analyzed using Spearman’s rank correlation. The relationship between the durations and the ALSSS score was also analyzed, using simple regression,

R. Higo et al. / Auris Nasus Larynx 31 (2004) 247–254 Table 1 Demographics of cases (duration following bulbar symptom onset)

and ANOVA was used for multiple compression tests. Statistical significance was defined as P < 0.05.

3. Results 3.1. Demographics of the patients The total of 72 ALS patients on VF examinations included 41 males (age range, 41–89 years; average, 62.2) and 31 females (age range, 35–84 years; average, 62.5). They were divided into six groups according to the duration following the onset of bulbar symptoms (Table 1): no bulbar complaints (Group 1), 1–6 months following bulbar symptom onset (Group 2); and 7–12 months (Group 3), 13–18 months (Group 4), 19–24 months (Group 5), and more than 24 months (Group 6) following bulbar symptom onset. They were also divided into five categories according to the ALSSS (Table 2): NORMAL EATING HABITS (Group NEH; ALSSS score, 10–9), EARLY EATING PROBLEMS (Group EEP; ALSSS score, 8–7), DIETARY CONSISTENCY CHANGES (Group DCC; ALSSS score, 6–5), NEEDS TUBE FEEDING (Group NTF; ALSSS score, 4–3), NOTHING BY MOUTH (Group NBM; ALSSS score, 2–1). 3.2. Changes in VF examination parameters over the course of disease progression Fig. 1 shows the VF findings for each group (Groups 1–6). Delayed bolus transport from the oral cavity to the pharynx, and bolus stasis at the PS, were seen in about half of all the cases, even in Group 1 (no bulbar complaints). In con-

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Table 2 Demographics of cases (ALSSS)

trast, UES opening was preserved in two-thirds of the cases in Group 6. The other parameters, such as bolus holding in the oral cavity, constriction of the pharynx, and elevation of the larynx, worsened gradually over time. Spearman’s rank correlation showed that bolus holding in the oral cavity, constriction of the pharynx, and elevation of the larynx were significantly correlated to the duration following bulbar symptom onset (P = 0.011, 0.013, and 0.031, respectively). The frequency of aspiration in patients also increased over time. However, only half of the patients showed aspiration, even in Group 6. 3.3. Changes in VF examination parameters according to the ALSSS Although the VF examination parameters became clearly worse as the ALSSS score advanced (Fig. 2), there were different patterns of changes among the parameters. Patients in Group NEH, who ate a normal diet, showed disturbed bolus transport from the mouth to the pharynx, weak constriction of the pharynx, and bolus stasis at the PS (52.4, 38.1, and 52.4%, respectively). Bolus holding in the oral cavity was not very involved in Groups NEH and EEP, but it was disturbed in 68.4% of the patients in Group DCC, who needed modification of foods (soft foods or a liquefied diet) (Fig. 2). Constriction of the pharynx was also clearly worse in Group DCC (Fig. 2). As such, severe dysfunction was apparent, in most of the parameters, when the patients required modification of foods (Group DCC). According to our results, swallowing function was disturbed in both the oral and pharyngeal phases (Fig. 2). Even in Group NEH, swallowing dysfunction was seen not only in the oral phase (bolus transport from the mouth to the pharynx) but also in the pharyngeal phase (constriction of the pharynx, and bolus stasis at the PS). However, among parameters in the pharyngeal phase, UES opening and ele-

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Fig. 1. Changes in VF findings over time following bulbar symptom onset. Group 1: no bulbar complaints; Group 2: 1–6 months following bulbar symptom onset; Group 3: 7–12 months following bulbar symptom onset; Group 4: 13–18 months following bulbar symptom onset; Group 5: 19–24 months following bulbar symptom onset; Group 6: more than 24 months following bulbar symptom onset. BT: bolus transport from the mouth to the pharynx, BH: bolus holding in the oral cavity, CP: constriction of the pharynx, EL: elevation of the larynx, UO: upper esophageal sphincter (UES) opening, SP: bolus stasis at the pyriform sinus (PS), and ASP: aspiration.

vation of the larynx had relatively well maintained function in Groups NEH, EEP, DCC, and NTF. As such, in the pharyngeal phase, some parts of swallowing function were disturbed in the early stage of dysphagia (weak constriction of the pharynx and bolus stasis at the PS), but the remainder (UES opening and elevation of the larynx) was relatively well maintained in the late stage of dysphagia; in contrast, swallowing dysfunction in the oral phase progressed more rapidly, compared with swallowing dysfunction in the pharyngeal phase. 3.4. Correlation between the ALSSS score and the duration following bulbar symptom onset The relationship between the ALSSS and the duration following bulbar symptom onset was analyzed. There was a significant correlation between the ALSSS and the duration following bulbar symptom onset (Spearman’s rank correlation: P < 0.0001). Fig. 3 shows a scattergram of the duration following bulbar symptom onset versus the ALSSS scores (N = 72). The regression line reflects a statistically significant negative correlation (r = 0.409, n = 72, P = 0.0004). Almost all of the ALS patients who had durations of less than 10 months following bulbar symptom onset showed scores

above 6, but after that period, patients had a wide-ranging dysphagic status, such as from just EARLY EATING PROBLEMS to NEEDS TUBE FEEDING (Fig. 3). Fig. 4 shows the mean ± S.D. of the duration following bulbar symptom onset for Groups NEH, EEP, DCC, NTF, and NBM. The mean ± S.D. for Group NEH is 4.3 ± 5.4 months, and that for Group NBM is 23.3 ± 8.0 months. In contrast, the means for Groups EEP, DCC, and NTF were almost the same (12.9, 13.9, and 13.7 months, respectively). Post-hoc testing revealed respective significant differences between Groups NBM and NEH, Groups DCC and NEH, and Groups EEP and NEH (P = 0.0031, 0.0034, and 0.0046, respectively). These results (Figs. 3 and 4) mean that the ALSSS score worsened with a longer duration following bulbar symptom onset, but they also suggest that the progression speed of the ALSSS varies, especially after the period of 10 months following bulbar symptom onset.

4. Discussion Progression of dysphagia in ALS has not yet been well studied. This is partly because the rate of progression of symptoms is extremely variable [2,3]. However, while the

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Fig. 2. Changes in VF findings according to ALSSS scores. Group NEH: normal eating habits (ALSSS score, 10–9); Group EEP: early eating problems (ALSSS score, 8–7); Group DCC: dietary consistency changes (ALSSS score, 6–5); Group NTF: needs tube feeding (ALSSS score, 4–3); Group NBM: nothing by mouth (ALSSS score, 2–1). BT: bolus transport from the mouth to the pharynx, BH: bolus holding in the oral cavity, CP: constriction of the pharynx, EL: elevation of the larynx, UO: upper esophageal sphincter (UES) opening, SP: bolus stasis at the pyriform sinus (PS), and ASP: aspiration.

patterns of progression of spinal ALS are unpredictable, bulbar ALS most often follows a progressive, recognizable course [3]. In addition, clinically, ALS patients with bulbar symptoms often follow a rapidly progressive course. As such, in this study, we aimed to elucidate the patterns of progression of dysphagia in ALS after bulbar symptom onset. Robbins studied swallowing function, by VF examination, in 31 ALS patients, using liquid and paste substances: 22 of the patients had bulbar symptoms; the other 9 had none [6]. For liquid swallows, the bulbar patients showed a prolonged duration of the oral phase, while all non-bulbar patients showed normal duration of the oral phase. The increased duration of the oral phase was mainly caused by a delayed initiation of the pharyngeal response. Robbins also found that increased viscosity of the bolus affects swallowing function in the oral stage in ALS. Disordered motility characteristics in the oral phase, such as piecemeal swallowing, were seen in the bulbar patients during swallows of both liquid and paste, while the non-bulbar patients showed abnormal motility patterns during swallowing of paste only. In the pharyngeal phase, the bulbar group showed reduced laryngeal elevation and aspiration, compared with normal findings in the non-bulbar patients. Bolus stasis at the valleculae, and at the pyriform sinus, was seen more in the bul-

bar patients. Robbins discussed that this bolus stasis in the pharynx might be a direct result of reduced lingual motility, which led to aspiration after swallowing. Briani et al. evaluated swallowing function of 20 patients with motor neuron disease, videofluoroscopically, and found dysphagia in 13 of them [4]. Radiological changes were found in 12 of the 13 patients with clinical dysphagia; 9 showed oral stasis of residual barium, 8 showed decreased pharyngo-esophageal motility, and incomplete opening of the upper esophageal sphincter (UES), and 6 showed piecemeal swallowing or aspiration. Briani et al. concluded that the oral phase of swallowing was the most compromised, followed by the pharyngeal phase (Robbins used the term “oral or pharyngeal stage”, while Briani adopted “pharyngeal phase”). According to Briani et al., the numbers and severity of radiological swallowing abnormalities were higher in the group of patients with severer ALSSS. Kawai et al. reported videofluoroscopic changes in early-stage dysphagia in ALS [10]. They studied swallowing function in 11 ALS patients using VF, and found that the disorders in the oral phase were either a dysfunction in bolus transport at the anterior part of the tongue, or a dysfunction in holding the bolus at the posterior part of the tongue. They suggested that, of these two factors, the latter

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Fig. 3. Scattergram of the duration following bulbar symptom onset vs. ALSSS scores for each patient (N = 72). The regression line reflects a statistically significant negative correlation (r = 0.409, n = 72, P = 0.0004).

had a greater effect on the degree of severity of dysphagia, because all 4 patients who showed disturbed holding function of the bolus at the posterior part of the tongue, had experienced aspiration. Piecemeal swallowing was present

in 9 patients, but it did not correlate with the degree of dysphagia. In contrast, swallowing function in the pharyngeal phase was maintained in early-stage dysphagia; a prolonged initiation of laryngeal elevation was observed in only one

Fig. 4. The mean ± S.D. of the duration following bulbar symptom onset for Groups NEH, EEP, DCC, NTF, and NBM.

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patient, and the larynx elevated fully in all of the patients. Based on these results, Kawai et al. insisted that the tongue function of holding the bolus in the oral cavity mainly affected severity in the early stages of dysphagia in ALS. The results in our study are consistent with those of the previous studies in some points; however, we should point out some differences. In the previous studies, dysfunction in the oral phase was considered the most compromised, followed by that in the pharyngeal phase; however, in our study, swallowing dysfunction was found to be involved in both the oral and pharyngeal phases. It is true that delayed bolus transport from the mouth to the pharynx was seen, even in non-bulbar patients (Group 1), and it seems to be a typical finding in ALS patients (Fig. 1). However, bolus stasis at the pyriform sinus was also seen in half of the patients in the non-bulbar group (Group 1). In contrast, bolus holding in the oral cavity was not very involved in the non-bulbar group (Group 1). It was also found that elevation of the larynx and UES opening were relatively well maintained in the patients who had durations of less than 1 year following bulbar symptom onset (Groups 1–3); however, these same functions were more disturbed in the patients who had durations of longer than 1 year following bulbar symptom onset (Groups 4–6) (Fig. 1). As such, to assess swallowing function in ALS, it is important to analyze the data in combination with “when (following bulbar symptom onset)”, as well as “which parameter (factor)”. The results might change among studies with different components of patients, especially in studies involving few patients. It has been reported that the time-dependent progression of dysphagia in ALS is extremely variable [2,3]; however, our results clearly showed that some VF examination parameters progress over time. Bolus holding in the oral cavity, constriction of the pharynx, and elevation of the larynx were significantly correlated to the duration following bulbar symptom onset. Aspiration also increased over time (Fig. 1). These findings worsened with a longer duration following bulbar symptom onset. In contrast, progression of insufficient UES opening or bolus stasis at the pyriform sinus was not time-dependent. The former was relatively well maintained even after a long duration following bulbar symptom onset (only 33.3% involvement of cases in Group 6), and the latter was severely disturbed before bulbar symptom onset (47.4% involvement of cases in Group 1). We reached the following conclusions: (1) some functions (bolus transport through the oral cavity and bolus stasis in the pharynx) are involved before bulbar symptom onset; (2) other functions (bolus holding in the oral cavity, constriction of the pharynx, and elevation of the larynx) gradually worsen over time following bulbar symptom onset; (3) the remaining function (UES opening) is relatively well maintained even in the late stage. Disturbed bolus transport through the oral cavity is caused by lingual dysfunction. The most common early physical findings of bulbar involvement in ALS are often associated with the tongue muscles [3,13,14]. A weakness of lingual

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muscle strength is usually associated with early difficulty with the oral transport phase of swallowing, and in particular, an inability for the tip of the tongue to reach beyond the incisors is usually associated with the need for a dietary change to very soft food or thick liquid [3]. When bolus holding is disturbed, a bolus spills into the pharynx prior to the initiation of pharyngeal swallowing. This might cause aspiration before swallowing; however, in our study, patients with disturbed bolus holding in the oral cavity did not show aspiration before swallowing. ALS patients usually maintain good ability of vocal fold adduction [3]. In our study, laryngeal endoscopy was performed on all ALS patients, before VF examination, and it was also confirmed that vocal fold paralysis was only seen in two of our patients. These facts suggest that sufficient function of vocal fold adduction protects patients from aspiration even if ALS patients show poor ability for bolus holding in the oral cavity. This also suggests that a rehabilitation technique to enforce glottic closure, such as the supraglottic swallow maneuver, is useful when ALS patients suffer from aspiration before swallowing. Spearman’s rank correlation showed that constriction of the pharynx and elevation of the larynx were significantly correlated to the duration following bulbar symptom onset (P = 0.013 and 0.031, respectively), and these were disturbed in more than 50% of the patients with longer than 1 year following bulbar symptom onset. Moreover, as we reported previously, the mean of swallowing pressure in the hypopharynx was relatively well maintained until 1 year following bulbar symptom onset, but it decreased to almost half (47.1%) of the control group in the group whose symptoms had been present for longer than 1 year [11]. From these facts, we recommend the usefulness of VF examination, performed at 1 year following bulbar symptom onset. Relationships between the ALSSS and the duration following bulbar symptom onset were previously reported in detail by Strand et al. [2]. They studied 42 ALS patients over an 80-month period, and found much inter-subject variability in the rate and overall degree of progression in dysphagia; the median score of the swallowing scale declined very little in 13% of the 42 patients, while 24% of the patients declined three or more levels. Strand et al. stated that the variability among patients pointed out that clinicians might need to provide dysphagia education and intervention to different patients at different time points during the course of their disease [2]. Our data also show variability of the dysphagic status for each patient, especially around 1 year following bulbar symptom onset; they have a wide-ranging dysphagic status, such as from just early eating problems to requiring tube feeding (Fig. 4). Although, generally speaking, the ALSSS became worse as the duration following bulbar symptom onset became longer (Fig. 3), the progression speed of the ALSSS score varies, especially around 1 year following bulbar symptom onset. The ALS patients who belonged to Group NEH (normal eating habits) had a shorter period of bulbar involve-

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ment (mean, 4.3 months), and almost all of the ALS patients who had durations of less than 10 months following bulbar symptom onset had ALSSS scores above 6 (Figs. 3 and 4). These patients may take normal diets; however, according to the result of the longitudinal time scale (Fig. 1), aspiration had already been experienced by 6 months in 21% of the patients (Group 2). Some rehabilitation techniques or appropriate modification of food according to VF findings can be introduced at that period, and may help patients take nutrition orally as long as possible. Considering these facts, we think it would also be good timing to perform VF on ALS patients at between 4 months and 10 months (preferably by 6 months) following bulbar symptom onset. In contrast, patients who would be classified as belonging to Group NBM (nothing by mouth), would not need VF examination to evaluate swallowing status, as it would not contribute to rehabilitation or improvement of QOL for patients. Only for decision-making on the indication for surgical intervention, such as a laryngectomy, would VF be useful to obtain supporting evidence for Group NBM patients.

5. Conclusion We analyzed the progression of dysphagia in ALS patients using an objective evaluation method, videofluoroscopy. VF is a useful tool to follow swallowing function in ALS patients. In early-stage dysphagia in ALS, VF will contribute to rehabilitation or introducing an appropriate form of diet; it will be useful to perform VF by 6 months following bulbar symptom onset. Later, around 1 year following bulbar symptom onset, VF should also be performed, since ALS patients show wide-ranging nutrition intake patterns, and they need assessment to introduce intervention, such as tube feeding, according to their varying status of dysphagia, around this time point.

References [1] Brooks BR. El Escorial World Federation of Neurology criteria for the diagnosis of amyotrophic lateral sclerosis. Subcommittee on Motor Neuron Diseases/Amyotrophic Lateral Sclerosis of the World Federation of Neurology Research Group on Neuromuscular Diseases and the El Escorial “Clinical limits of amyotrophic lateral sclerosis” workshop contributors. J Neurol Sci 1994;124(Suppl):96–107. [2] Strand EA, Miller RM, Yorkston KM, Hillel AD. Management of oral-pharyngeal dysphagia symptoms in amyotrophic lateral sclerosis. Dysphagia 1996;11:129–39. [3] Hillel AD, Miller R. Bulbar amyotrophic lateral sclerosis: patterns of progression and clinical management. Head Neck 1989;11:51–9. [4] Briani C, Marcon M, Ermani M, Bottin R, Iurilli V, et al. Radiological evidence of subclinical dysphagia in motor neuron disease. J Neurol 1998;245:211–6. [5] Bosma JF, Brodie DR. Disabilities of the pharynx in amyotrophic lateral sclerosis as demonstrated by cineradiography. Radiology 1969;92:97–103. [6] Robbins J. Swallowing in ALS and motor neuron disorders. Neurol Clin 1987;5:213–29. [7] Wilson PS, Bruce-Lockhart FJ, Johnson AP. Videofluoroscopy in motor neuron disease prior to cricopharyngeal myotomy. Ann R Coll Surg Engl 1990;72:375–7. [8] Leighton SE, Burton MJ, Lund WS, Cochrane GM. Swallowing in motor neurone disease. J R Soc Med 1994;87:801–5. [9] Mari F, Matei M, Ceravolo G, Pisani A, Montesi A, Provinciali L. Predictive value of clinical indices in detecting aspiration in patients with neurological disorders. J Neurol Neurosurg Psychiatry 1997;63:456–60. [10] Kawai S, Tsukuda M, Mochimatsu I, Enomoto H, Kagesato Y, Hirose H, et al. A study of the early stage of Dysphagia in amyotrophic lateral sclerosis. Dysphagia 2003;18:1–8. [11] Higo R, Tayama N, Watanabe T, Nitou T. Videomanofluorometric study in amyotrophic lateral sclerosis. Laryngoscope 2002;112:911– 7. [12] Hillel AD, Miller RM, Yorkston K, McDonald E, Norris FH, Konikow N. Amyotrophic lateral sclerosis severity scale. Neuroepidemiology 1989;8:142–50. [13] Carpenter RJ, McDonald TJ, Howard FM. The otolaryngologic presentation of amyotrophic lateral sclerosis. ORL 1978;86:479–84. [14] Dworkin JP. Tongue strength measurement in patients with amyotrophic lateral sclerosis: qualitative vs. quantitative procedures. Arch Phys Med Rehabil 1980;61:422–4.