Auris Nasus Larynx 42 (2015) 213–217

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Auris Nasus Larynx

journal homepage: www.elsevier.com/locate/anl

Evaluation of dysphagia at the initial diagnosis of amyotrophic

lateral sclerosis
Shigeyuki Murono a,*, Tsuyoshi Hamaguchi b, Hiroshi Yoshida a, Yosuke Nakanishi a,
Akira Tsuji a, Kazuhira Endo a, Satoru Kondo a, Naohiro Wakisaka a, Masahito Yamada b,
Tomokazu Yoshizaki a
a
Department of Otolaryngology, Head and Neck Surgery, School of Medicine, Kanazawa University, Kanazawa, Japan
b
Department of Neurology, School of Medicine, Kanazawa University, Kanazawa, Japan

A R T I C L E I N F O A B S T R A C T

Article history: Objective: Dysphagia eventually occurs in amyotrophic lateral sclerosis (ALS). Swallowing in patients
Received 16 June 2014 with ALS at their initial diagnosis was evaluated using videofluoroscopy (VF).
Accepted 24 October 2014 Methods: Nineteen consecutive patients with ALS, 14 with bulbar symptoms, and 5 without them,
Available online 18 November 2014
underwent VF. Fourteen physiologic components, 6 oral and 8 pharyngeal components, were assessed
during the examination.
Keywords: Results: Significantly poorer scores were observed in three of the 6 oral components and 3 of the 8
Amyotrophic lateral sclerosis
pharyngeal components in patients with bulbar symptoms. Furthermore, bolus transport from the oral
Dysphagia
Videofluoroscopy
cavity to pharynx, pharyngeal constriction, oral residue and pharyngeal residue were impaired in
Severity scale patients even without bulbar symptoms. On the other hand, pharyngoesophageal segment opening was
preserved in patients even with bulbar symptoms. Bolus transport and initiation of pharyngeal swallow
were correlated with the swallowing category of the ALS severity scale.
Conclusion: Defining types of impairment in patients with or without bulbar symptoms is useful for
evaluating dysphagia in this disease. Although VF showed impairment of oral and pharyngeal phases of
swallowing, the oral phase affected the eating habit in ALS at the initial diagnosis.
ß 2014 Elsevier Ireland Ltd. All rights reserved.

1. Introduction pneumonia [2]. Therefore, careful follow-up of the clinical

Amyotrophic lateral sclerosis (ALS) is a progressive neurode-
generative disorder that primarily involves the motor neurons in
the cerebral cortex, brainstem, and spinal cord [1]. The degenera-
tion of upper motor neurons results in symptoms that include
increased deep tendon reflexes and a manifestation of pathologic
reflexes. Degeneration of the lower motor neurons causes
muscular atrophy, decreased muscle force, fasciculation, and
bulbar palsy. As the disease progresses, both upper and lower
motor neurons may be affected; therefore, various symptoms
overlap. Among them, dysphagia eventually occurs independent of
the time of onset [2].
Dysphagia is one of the most critical problems for ALS patients,
which leads to serious nutritional deficit and results in aspiration
condition of dysphagia is required to decide on the appropriate
timing of intervention. Furthermore, because the dysphagia of ALS
is generally progressive and symptoms vary, evaluation of the
swallowing function at the initial diagnosis is inevitable.
Videofluoroscopy has been the most reliable examination to
evaluate the swallowing function of ALS patients [3]. It facilitates
accurate analysis of the mechanisms of the oral and pharyngeal
phases of swallowing, identification of possible changes respon-
sible for symptoms, and planning of appropriate therapy. The aim
of this study was to assess the role of videofluoroscopy in
identifying swallowing abnormalities, especially from the per-
spective of oral and pharyngeal dysphagia, at the initial diagnosis
of ALS.
2. Materials and methods

* Corresponding author at: Department of Otolaryngology, Head and Neck
Surgery, School of Medicine, Kanazawa University, 13-1 Takaramachi, Kanazawa
920-8640, Japan. Tel.: +81 76 265 2413; fax: +81 76 234 4265.
E-mail address: murono@med.kanazawa-u.ac.jp (S. Murono).
2.1. Patients
Nineteen patients were diagnosed with ALS by certified
neurologists based on El Escorial criteria at the Department of

http://dx.doi.org/10.1016/j.anl.2014.10.012
0385-8146/ß 2014 Elsevier Ireland Ltd. All rights reserved.
214 S. Murono et al. / Auris Nasus Larynx 42 (2015) 213–217

Table 1 present study. Each score was obtained with the average of blind
Summary of the swallowing category of the ALS severity scale proposed by Hillel
reviews by one otolaryngologist and one speech therapist.
et al. [4].
Simultaneously, the penetration-aspiration scale (PAS), an 8-
Swallowing Rating point scale to quantify selected aspects of penetration and
Normal eating habits aspiration in order to clarify the depth of airway invasion
Normal swallowing 10 and whether or not there is material entering the airway, was
Nominal abnormality 9 defined for the brief evaluation of dysphagia (Table 3) [6].
Early eating problems
Minor swallowing problems 8
Prolonged time or small bite size 7 2.3. Statistical analysis
Dietary consistency changes
Soft diet 6 The difference in scores between patients without bulbar
Liquefied diet 5
symptoms (BS-negative) and those with symptoms (BS-positive)
Needs tube feeding
Supplemental tube feedings 4
was compared using the Mann–Whitney U-test. A correlation
Tube feeding with occasional oral nutrition 3 between two variables was analyzed using Spearman’s rank
Nothing by mouth correlation. All analyses were carried out using SPSS 19.0 software
Secretions managed with aspirator/medication 2 (SPSS Inc., Chicago, IL, USA). In all tests, p < 0.05 was considered
Aspiration of secretions 1
significant.
ALS, amyotrophic lateral sclerosis.
3. Results

Neurology in our hospital between 2004 and 2011. They were
referred to our department immediately after the diagnosis to
evaluate the swallowing function. The onset of bulbar symptoms
was reported by patients, and bulbar symptoms were evaluated by
neurologists, otolaryngologists, and speech therapists. The status
of the dietary intake was evaluated using the swallowing category
of the ALS severity scale (ALSSS) (Table 1) [4]. This study was
approved by the Ethics Committee of Kanazawa University School
of Medicine.
2.2. Videofluoroscopic assessment
Videofluoroscopy was carried out in all patients at the time of
the initial diagnosis of ALS. Three milliliters of a 140% (v/v) barium
mixture was basically used; however, other contrast agents were
also used based on the circumstances. All 15 physiologic
components except for a component of esophageal clearance,
proposed by Martin-Harris and Jones, were thoroughly evaluated
from the perspective of all six oral components and all eight
pharyngeal components [5] (Table 2). In addition, we also
evaluated the oral and pharyngeal residues. Each component
was graded from 0, which was considered normal, to 3 in the
3.1. Patients
Nineteen patients were evaluated, consisting of 12 men and
7 women. The mean and median ages of the 19 patients were
64 and 66 years old, respectively, ranging from 44 to 79 years old.
Physical examinations by a neurologist and otolaryngologist at the
initial presentation revealed 5 patients with disorder of only the
extremities, 6 patients with only bulbar disorder, and 8 patients
with a combination of both disorders. The mean duration from the
onset of symptoms to the diagnosis of ALS at our hospital was
8.0 months for bulbar symptoms and 11.1 months for other
symptoms involving the limbs, showing a significant difference
(p < 0.05).
3.2. Oral swallowing impairment on videofluoroscopy
The mean score of each oral component is shown in Table 2 and
Fig. 1. The components of Lip Closure (LipC), Lingual Elevation
(LingE), and Tongue to Palatal Seal (TPS) were preserved in both BS-
negative and BS-positive patients. However, both components of
Bolus Preparation/Mastication (BP) and Initiation of Pharyngeal
Swallow (IPS) were preserved in BS-negative patients while they

Table 2
Physiologic swallowing components.

Component Abbreviation Mean score  standard deviation p-value

Bulbar symptoms ( ) (n = 5) Bulbar symptoms (+) (n = 14)

Oral
1. Lip Closure LipC 0.00  0.00 0.21  0.42 0.27
2. Lingual Elevation LingE 0.20  0.44 0.28  0.72 0.88
3. Tongue to Palatal Seal TPS 0.20  0.44 0.28  0.72 0.88
4. Bolus Preparation/Mastication BP 0.00  0.00 0.57  0.51 0.03
5. Bolus Transport/Lingual Motion BT 0.40  0.54 1.14  0.66 0.04
6. Initiation of Pharyngeal Swallow IPS 0.00  0.00 0.93  0.73 0.01
Pharyngeal
7. Soft Palate Elevation and Retraction SPE 0.00  0.00 0.43  0.51 0.08
8. Laryngeal Elevation LaryE 0.00  0.00 0.71  0.61 0.01
9. Anterior Hyoid Excursion AHE 0.00  0.00 0.93  0.61 <0.01
10. Laryngeal Closure LaryC 0.00  0.00 0.43  0.51 0.08
11. Pharyngeal Contraction PC 0.60  0.54 1.07  0.61 0.14
12. Pharyngoesophageal Segment Opening PESO 0.00  0.00 0.21  0.42 0.27
13. Tongue Base Retraction TBR 0.20  0.44 1.00  0.55 0.01
14. Epiglottic Inversion EI 0.20  0.44 0.36  0.63 0.67
Esophageal
15. Esophageal Clearance EsoC N/D N/D N/A
Residue
Oral OR 0.80  0.44 1.36  0.63 0.08
Pharyngeal PR 1.40  0.54 1.86  1.02 0.35
 S. Murono et al. / Auris Nasus Larynx 42 (2015) 213–217
Table 3
Summary of the penetration-aspiration scale proposed by Rosenbek et al. [6].
Score Status of penetration/aspiration
1 Material does not enter the airway
2 Material enters the airway, remains above the vocal folds, and is
ejected from the airway
3 Material enters the airway, remains above the vocal folds, and is not
ejected from the airway
4 Material enters the airway, contacts the vocal folds, and is ejected
from the airway
5 Material enters the airway, contacts the vocal folds, and is not
ejected from the airway
6 Material enters the airway, passes below the vocal folds, and is
ejected into the larynx or out of the airway
7 Material enters the airway, passes below the vocal folds, and is not
ejected from the trachea despite effort
8 Material enters the airway, passes below the vocal folds, and no
effort is made to eject
were significantly impaired in BS-positive patients. On the other
hand, the components of Bolus Transport/Lingual Motion (BT)
and Oral Residue (OR) were affected in both BS-negative and BS-
positive patients, while the former showed a significantly poorer
score.
3.3. Pharyngeal swallowing impairment on videofluoroscopy
The mean score of each pharyngeal component is shown in
Table 2 and Fig. 2. Soft Palate Elevation and Retraction (SPE),
Laryngeal Elevation (LaryE), Anterior Hyoid Excursion (AHE),
Laryngeal Closure (LaryC), Pharyngoesophageal Segment Opening
(PESO), Tongue Base Retraction (TBR), and Epiglottic Inversion (EI)
were preserved in BS-negative patients. Among these components,
LaryE, AHE, and TBR were significantly affected, while SPE, LaryC,
PESO, and EI were still preserved in BS-positive patients.
Pharyngeal Contraction (PC) and, especially, Pharyngeal Residue
(PR) were affected in both BS-negative and BS-positive patients.
3.4. Correlation of oral and pharyngeal components with the
penetration-aspiration scale or ALS severity scale
Mean scores of the PAS were 1.20 and 1.50 in BS-negative
and BS-positive patients, respectively, showing no significant
LipC
OR LingE
IPS* TPS
BT* BP*
Fig. 1. Mean score of each oral component. The continuous line indicates patients
without bulbar symptoms. The dotted line indicates patients with bulbar
symptoms. A higher score means severer impairment. Abbreviations are
described in Table 2. *p < 0.05.
215
SPE
PR LaryE*
EI AHE**
TBR* LaryC
PESO PC
Fig. 2. Mean score of each pharyngeal component. The continuous line indicates
patients without bulbar symptoms. The dotted line indicates patients with bulbar
symptoms. A higher score means severer impairment. Abbreviations are described
in Table 2. *p < 0.05, **p < 0.01.
difference (p = 0.49) (Fig. 3, left panel). Among the 6 oral
components, BT showed a trend toward a correlation with PAS
(r = 0.37) (Table 4). Among the 10 pharyngeal components, PC
showed a significant correlation with PAS (r = 0.58), and PESO
showed a trend toward a correlation with PAS (r = 0.39).
Mean scores of the swallowing category of ALSSS (s-ALSSS)
were 9.20 and 7.93 in BS-negative and BS-positive patients,
respectively, showing a significant difference (p = 0.01) (Fig. 3,
right panel). Among the 6 oral components, IPS showed a
significant inverse correlation with s-ALSSS (r = 0.46) (Table 4).
In addition, BT and OR showed a trend toward an inverse
correlation with s-ALSSS (r = 0.45 and r = 0.40, respectively).
On the other hand, among the 10 pharyngeal components, TBR
showed a trend toward an inverse correlation with s-ALSSS
(r = 0.35).
4. Discussion
In the clinical management of ALS, evaluating dysphagia is
essential to decide on the necessity of gastrostomy in accordance
with the most recent European guidelines [7]. Several procedures,
including VF with or without manometry, fiberoptic examination
of swallowing, and oropharyngoesophageal scintigraphy, have
been reported to evaluate the swallowing function of patients with
ALS [8–12].
The evaluation of swallowing kinematics is one of the major
advantages of VF over other procedures. The present study
demonstrated that each component belonged to one of three
types of evaluation (Table 5). The first is a component preserved
in both BS-negative and BS-positive patients (type I), indicating
that the component is preserved despite the presence of bulbar
symptoms. The second is a component preserved in BS-negative
but impaired in BS-positive patients (type II), indicating that the
component is impaired along with the progression of bulbar
symptoms. The third is a component impaired in both BS-negative
and BS-positive patients (type III), indicating that the component is
impaired despite the absence of bulbar symptoms.
Paths of impairment of oral and pharyngeal components varied
among previous reports. The present study demonstrated that BT
and OR in the oral phase, and PSW, PC, and PR in the pharyngeal
phase, belonged to type III. This suggests that bolus transport from
the mouth to pharynx and constriction of the pharynx as well as
both oral and pharyngeal residues are observed early, despite
216 S. Murono et al. / Auris Nasus Larynx 42 (2015) 213–217

Fig. 3. Mean scores of the penetration-aspiration scale (left panel) and swallowing category of the ALS severity scale (right panel) in patients with or without bulbar
symptoms. a Penetration-aspiration scale; b swallowing category of the ALS severity scale; NS, not significant.

being free from bulbar symptoms, in ALS. In accordance, Higo et al.
also reported delayed bolus transport from the oral cavity to
pharynx as well as bolus stasis at the pyriform sinus in patients
without bulbar complaints [9]. They also showed that weak
constriction of the pharynx gradually worsened over time
following bulbar symptom onset [9]. However, this contrasts with
the present study, demonstrating the earlier impairment of PC
despite the absence of bulbar symptoms.
Interpretations of findings obtained in VF varied among
investigators. Kawai et al. reported that dysfunction in holding
the bolus at the posterior part of the tongue had a greater impact
on the severity of dysphagia than dysfunction in bolus transport at
the anterior part of the tongue [10]. This also contrasts with
the present study, showing that LingE and TPS belonged to type I
while BT belonged to type III. In addition, the present study
demonstrated that PESO belonged to type III. This suggests that
upper esophageal sphincter (UES) opening is less affected even in
the presence of bulbar symptoms in ALS. This is in accordance with
the report by Higo et al., showing a maintained UES opening in
advanced-ALSSS patients, but conflicts with the report by Briani
et al., showing incomplete opening of UES [3,9]. With respect to
laryngeal elevation, Kawai et al. demonstrated full laryngeal
elevation in all patients with early ALS, while Robbins demon-
strated reduced laryngeal elevation [10,13]. The present study
showed LaryE belonged to type II, suggesting that the laryngeal
elevation gradually worsened along with the progression of bulbar
symptoms.
The assessment parameters and grading scale in the present
study were similar to, but not the same as, the reports by Higo et al.
and Briani et al. [3,9]. Kawai et al. performed valuable, but complex,
quantitative evaluations in picture analyses, being a different
procedure from the present study as well as other studies
[10]. Therefore, subtle differences in the results may arise among
studies. Although many swallowing clinicians have attempted to
evaluate components of swallowing behavior on VF examination, a
precise review of 15 physiologic components of swallowing by
Martin-Harris and Jones may be a global standard [5]. From this
perspective, the present study, which follows the assessment

Table 4
Correlation of the physiologic swallowing components with the penetration-aspiration scale and swallowing category of the ALS severity scale.

Component Abbreviation Correlation p-value Correlation p-value

Coefficient Coefficient
for PASa for s-ALSSSb

Oral
1. Lip Closure LipC 0.29 0.22 0.12 0.60
2. Lingual Elevation LingE 0.29 0.22 0.11 0.64
3. Tongue to Palatal Seal TPS 0.29 0.22 0.11 0.64
4. Bolus Preparation/Mastication BP 0.14 0.55 0.20 0.40
5. Bolus Transport/Lingual Motion BT 0.37 0.12 0.45 0.05
6. Initiation of Pharyngeal Swallow IPS 0.01 0.97 0.46 <0.05
Pharyngeal
7. Soft Palate Elevation and Retraction SPE 0.00 1.00 0.03 0.91
8. Laryngeal Elevation LaryE 0.89 0.30 0.20
9. Anterior Hyoid Excursion AHE 0.04 0.86 0.31 0.18
10. Laryngeal Closure LaryC 0.07 0.75 0.02 0.91
11. Pharyngeal Contraction PC 0.58 <0.01 0.33 0.16
12. Pharyngoesophageal Segment Opening PESO 0.39 0.10 0.10 0.69
13. Tongue Base Retraction TBR 0.30 0.90 0.35 0.13
14. Epiglottic Inversion EI 0.21 0.37 0.13 0.59
Esophageal
15. Esophageal Clearance (upright position) EC N/D N/A N/D N/A
Residue
Oral OR 0.10 0.69 0.40 0.09
Pharyngeal PR 0.25 0.28 0.23 0.34
a
Penetration-aspiration scale.
b
Swallowing category of ALS severity scale
 S. Murono et al. / Auris Nasus Larynx 42 (2015) 213–217 217

Table 5 5. Conclusions
Impairment types of each component.

Component Abbreviation In conclusion, the present study proposed a possible standard

Impairment type I (preserved in both BS and BS+) for radiographic interpretations of dysphagia in ALS patients. Bolus
Oral transport from the oral cavity to pharynx, pharyngeal constriction,
1. Lip Closure LipC oral residue and pharyngeal residue were impaired in ALS even
2. Lingual Elevation LingE without bulbar symptoms. On the other hand, pharyngoesophageal
3. Tongue to Palatal Seal TPS
segment opening was preserved in ALS even with bulbar symptoms.
Pharyngeal
7. Soft Palate Elevation SPE The oral phase of swallowing affects eating habits in ALS.
10. Laryngeal Closure LaryC
12. Pharyngoesophageal Segment Opening PESO Conflict of interest
14. Epiglottic Inversion EI
Impairment type II (preserved in BS but impaired in BS+)
Oral The authors declare that they have no conflict of interest.
4. Bolus Preparation/Mastication BP
6. Initiation of Pharyngeal Swallow IPS References
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