Assessment of oropharyngeal swallowing dysfunction in myasthenia gravis patients presenting with difficulty in swallowing

G Model

ANL-RR2517; No. of Pages 7 Auris Nasus Larynx xxx (2018) xxx–xxx Contents lists available at ScienceDirect

Auris Nasus Larynx journal homepage: www.elsevier.com/locate/anl

Assessment of oropharyngeal swallowing dysfunction in myasthenia gravis patients presenting with difficulty in swallowing$ Yoshihiko Kumai a,*, Takumi Miyamoto a, Keigo Matsubara c, Yasuhiro Samejima a, Satoshi Yamashita b, Yukio Ando b, Yorihisa Orita a a

Department of Otolaryngology Head and Neck Surgery, Kumamoto University, Graduate School of Medicine, Kumamoto, Japan Department of Neurology, Graduate School of Medical Sciences, Kumamoto University, Japan c Department of Rehabilitations, Kumamoto Health Science University, Kumamoto, Japan b

A R T I C L E I N F O

A B S T R A C T

Article history: Received 3 July 2018 Received in revised form 23 September 2018 Accepted 17 October 2018 Available online xxx

Objective: To examine the correlation between the results of a clinical neurological evaluation and swallowing dysfunction in myasthenia gravis (MG) patients who presented with difficulty in swallowing and underwent videofluorographic (VF) and fiber-optic endoscopic (FE) evaluation. Methods: The swallowing studies of 13MG patients with difficulty in swallowing seen at the Department of Neurology from June 2016 to April 2018 were reviewed. The assessment parameters on VF and FE examination were as follows: swallowing initiation, bolus stasis at the pyriform sinus (PS) and vallecula (VC), and the degree of aspiration. They were assessed using a 4 or 5-point scale. Associations between these parameters and the clinical neurological evaluation, which included the Myasthenia Gravis Foundation of America (MGFA) clinical classification, the MG Activities of Daily Living score, and a quantitative MG score, were statistically determined. Results: No patients demonstrated aspiration. However, in patients MGFA IIb/IIIb disease, the Hydo’s FEES scale and pharyngeal residue examined using VF were significantly (p < 0.05) more severe than in patients classified with MGFA IIa/IIIa disease. None of the parameters evaluated with VF and FE correlated significantly with the clinical neurological evaluation except for the grip assessment. Conclusion: While not presenting with aspiration but with swallowing difficulty alone, patients classified with MGFA IIb/IIIb disease, regardless of clinical neurological evaluation, require care addressing the reduced pharyngeal clearance. Controlling the severity of the pharyngeal residue may be the key to preventing silent aspiration, especially in patients with MGFA IIb/IIIb disease. © 2018 Elsevier B.V.. All rights reserved.

Keywords: Myasthenia gravis Swallowing dysfunction Silent aspiration Videofluorographic evaluation Fiber-optic endoscopic evaluation

$ This paper was presented as a poster at the annual meeting of the American Broncho-Esophagial Association (ABEA) at Combined Otolaryngology Spring Meeting (COSM) which was held in Washington D.C. Maryland on April 19th 2018. * Corresponding author at: Department of Otolaryngology Head and Neck Surgery, Kumamoto University Graduate School of Medicine, 860-8556, 1-1-1 Honjo, Kumamoto City, Kumamoto, Japan. E-mail address: [email protected] (Y. Kumai).

https://doi.org/10.1016/j.anl.2018.10.004 0385-8146/© 2018 Elsevier B.V.. All rights reserved.

Please cite this article in press as: Kumai Y, et al. Assessment of oropharyngeal swallowing dysfunction in myasthenia gravis patients presenting with difficulty in swallowing. Auris Nasus Larynx (2018), https://doi.org/10.1016/j.anl.2018.10.004

G Model

ANL-RR2517; No. of Pages 7 Y. Kumai et al. / Auris Nasus Larynx xxx (2018) xxx–xxx

2

1. Introduction Dysphagia is an important symptom in myasthenia gravis (MG), but the degree of swallowing dysfunction varies in MG patients. Retrospective evidence suggests that almost 70% of MG patients present with swallowing dysfunction, to some extent. However, few prospective or even retrospective studies have included a sufficient number of MG patients presenting mild dysphagia without aspiration [1,2]. Silent aspiration frequently causes myasthenic crisis and may lead to aspiration pneumonia with a poor prognosis [3,4], such that oropharyngeal weakness is regarded as one of the most serious symptoms of MG [5]. Effective management of MG therefore includes the detection of swallowing dysfunction with silent aspiration, but the best way to evaluate dysphagia or to predict the risk of aspiration in MG patients with mild dysphagia is unclear. The inability of clinical neurological examination alone to sufficiently detect and grade MG-related dysphagia has been previously reported [2,3,6]. One of the main reasons for this is that both the oral and the pharyngeal phases of swallowing are frequently and simultaneously disturbed in MG patients [2]. A more effective approach may be to evaluate swallowing using a combination of a clinical neurological assessment and swallowing examinations, including videofluoroscopy (VF) or fiber-optic endoscopy (FE) performed by board-certified otolaryngologists and speech pathologists [7,8]. The objective of this study was to examine swallowing dysfunction with VF and FE and to determine the correlation between the results of a clinical-neurological evaluation including Myasthenia Gravis Foundation of America [MGFA] clinical classification which is ultimately subjective [9], MG Activities of Daily Living [MG-ADL] score [10], and Quantitative Myasthenia Gravis [QMG] test score [11] and oropharyngeal swallowing dysfunction in MG patients presenting with difficulty in swallowing without aspiration. In cooperation with board-certified otolaryngologists, these perspectives would help for neurologists to prevent myasthenic crisis induced by silent aspiration based on the mild dysphagia presented in MG patients. 2. Materials and methods The swallowing studies of 18 MG patients with difficulty in swallowing, but without aspiration, at various disease timepoints or stages who had sought consultation at the Department of Neurology of our institution between June 2016 and April 2018, were retrospectively reviewed. Written consent was obtained from all patients. Patients agreed that we could use clinical data obtained from this study for diagnosis and for the purposes of research. Ethical approval was not necessary because this was a retrospective study and included no additional examination of the patients. The exclusion criteria in this study were as follows: with Parkinson’s disease (N = 1), VF was not performed because of discharge within one week (N = 2), and patients older than eighty years old (N = 2)were excluded from the study, therefore, 13 MG patients (mean age of 53.3 years) were enrolled in this study. Myasthenia Gravis Foundation of America [MGFA] clinical classification [9], MG

Activities of Daily Living [MG-ADL] score [10], and Quantitative Myasthenia Gravis [QMG] test score [11] were listed in Table 1a–1c. FE was performed during the initial consultation at the Department of Neurology, according to a standard procedure using a flexible fiber scope (PENTAX VNL-1190STK/EPK-i7000; HOYA Inc., Tokyo, Japan) and blue-dyed water as described elsewhere. The video clips recorded in the electronic medical records were transferred to a personal computer (dc7800MT-E6850/Windows XP; HP Inc., Palo Alto, CA, USA) via password-locked USB memory sticks. Two days after the FE examination, all patients underwent VF, conducted using radiographic equipment (collimator type R-50 model; Shimadzu Corporation Medical Systems Tokyo, Japan) according to a previously described standard procedure [12,13]. The examination was performed by a speech pathologist and two board-certified otolaryngologists subspecializing in dysphagia. The VF was conducted with the patient in the upright position such that both antero-posterior (AP) and lateral projections were obtained. A 120% barium sulfate suspension was administered as a 3- or 5-mL bolus in a cup or syringe. The patients were instructed to hold the contrast medium in their mouths until the command to swallow was given. For the purposes of this investigation, AP and lateral views were reviewed, assessments were made only for the previously described solution, and evaluations of the patient were limited to the first swallow [12]. The recorded FE images were evaluated as follows. Two speech pathologists blindly scored aspiration, penetration, delayed initiation, and pharyngeal clearance in the pyriform Table 1a MGFA clinical classification. Class I Any ocular muscle weakness; may have weakness of eye closure. All other muscle strength is normal. Class II Mild weakness affecting muscles other than ocular muscles; may also have ocular muscle weakness of any severity. Predominantly affecting limb, axial muscles, or both. May also IIa have lesser involvement of oropharyngeal muscles. IIb Predominantly affecting oropharyngeal, respiratory muscles, or both. May also have lesser or equal involvement of limb, axial muscles, or both. Class IIIModerate weakness affecting muscles other than ocular muscles; may also have ocular muscle weakness of any severity. IIIa Predominantly affecting limb, axial muscles, or both. May also have lesser involvement of oropharyngeal muscles. IIIb Predominantly affecting oropharyngeal, respiratory muscles, or both. May also have lesser or equal involvement of limb, axial muscles, or both. Class IVSevere weakness affecting muscles other than ocular muscles; may also have ocular muscle weakness of any severity. IVa Predominantly affecting limb, axial muscles, or both. May also have lesser involvement of oropharyngeal muscles. IVb Predominantly affecting oropharyngeal, respiratory muscles, or both. May also have lesser or equal involvement of limb, axial muscles, or both. Class V Defined as intubation, with or without mechanical ventilation, except when employed during routine postoperative management. The use of a feeding tube without intubation places the patient in class IVb. Jaretzki A 3rd et al., Myasthenia gravis: recommendations for clinical research standards. Task Force of the Medical Scientific Advisory Board of the Myasthenia Gravis Foundation of America. Neurology. 2000;55(1):16–23.

Please cite this article in press as: Kumai Y, et al. Assessment of oropharyngeal swallowing dysfunction in myasthenia gravis patients presenting with difficulty in swallowing. Auris Nasus Larynx (2018), https://doi.org/10.1016/j.anl.2018.10.004

G Model

ANL-RR2517; No. of Pages 7 Y. Kumai et al. / Auris Nasus Larynx xxx (2018) xxx–xxx

3

Table 1b MG Activities of Daily Living (MG-ADL). Grade

0

1

2

3

Talking

Normal

Chewing Swallowing

Normal Normal

Intermittent slurring or nasal speech Fatigue with solid food Rare episode of choking

Difficult to understand speech Gastric tube Gastric tube

Breathing

Normal

Constant slurring or nasal, but can be understood Fatigue with soft food Frequent choking necessitating changes in diet Shortness of breath at rest

Impairment of ability to brush teeth or comb hair Impairment of ability to arise from a chair Double vision Eyelid droop

None

Rest periods needed

Cannot do one of these functions

Shortness of breath with exertion Extra effort, but no rest periods needed

Score

Ventilator dependence

None

Mild, sometimes uses arms

Moderate, always uses arms

Severe requires assistance

None None

Occurs, but not daily Occurs, but not daily

Daily, but not constant Daily, but not constant

Constant Constant Total score ________

Wolfe, GI et al. Myasthenia gravis activities of daily living profile. Neurology. 1999;52:1487–1489.

sinus (PS), vallecula (VC), as determined from the recorded FE movie clips and the score was averaged. Hyodo’s FE rating scale [14,15], which assesses (1) delayed initiation based on ‘white-out’ timing and (2) pharyngeal clearance (total for original Hyodo’s version, PS and VC separately for our original version) after blue-dyed water is swallowed, was used. The 4point scale used in the original report [14] is as follows: 0 = normal swallowing, 1 = mildly impaired swallowing, 2 = moderately impaired swallowing, and 3 = severely impaired swallowing. The VF examination included assessments of: swallowing initiation, laryngeal elevation, peristaltic wave of the pharynx,

mobility of the tongue base, upper esophageal sphincter opening, aspiration, and bolus residue in the PS and VC after swallowing. All of these parameters were investigated from the lateral VF view by board-certified otolaryngologists with sufficient experience in the management of swallowing disorders. The Modified Barium Swallow Impairment Profile (MBSImP) using 4 or 5-point scale [16] was used to evaluate each parameter. Associations between the following parameters were statistically determined using Spearman’s rank-order correlation: initiation of pharyngeal swallow, pharyngeal residue, penetration aspiration scale, tongue base retraction, pharyngeal constriction, laryngeal elevation, pharyngo-esoph-

Table 1c Quantitative MG scale (QMG). Test item

None

Mild

Moderate

Severe

Score

Grade Double vision on lateral gaze right or left (circle one), seconds Ptosis (upward gaze), seconds Facial muscles

0 61

1 11–60

2 1–10

3 Spontaneous

– –

61 Normal lid closure Normal

1–10 Complete, without resistance Severe coughing/choking or nasal regurgitation Dysarthria at 10–29

Spontaneous Incomplete

– –

Cannot swallow (test not attempted) Dysarthria at 9

–

None at 50

11–60 Complete, weak, some resistance Minimal coughing or throat clearing Dysarthria at 30–49

240 240 80

90–239 90–239 65–79

10–89 10–89 50–64

0–9 0–9 <50

45 30

15–44 10–29

5–14 5–9

0–4 0–4

35 25 120 100 100

15–34 10–24 30–119 31–99 31–99

5–14 5–9 1–29 1–30 1–30

0–4 0–4 0 0 0

Swallowing 4 oz. water (1/2 cup) Speech after counting aloud from 1 to 50 (onset of dysarthria) Right arm outstretched (90 sitting), seconds Left arm outstretched (90 sitting), seconds Vital capacity, % predicted Right-hand grip, kgW Men Women Left-hand grip, kgW Men Women Head lifted (45 supine), seconds Right leg outstretched (45 supine), seconds Left leg outstretched (45 supine), seconds

– – – – – – – – – – – – Total QMG score (range, 0–39)

Barohn RJ,et al. Reliability testing of the quantitative myasthenia gravis score. Ann NY Acad Sci. 1998;841:769–772.

Please cite this article in press as: Kumai Y, et al. Assessment of oropharyngeal swallowing dysfunction in myasthenia gravis patients presenting with difficulty in swallowing. Auris Nasus Larynx (2018), https://doi.org/10.1016/j.anl.2018.10.004

G Model

ANL-RR2517; No. of Pages 7 Y. Kumai et al. / Auris Nasus Larynx xxx (2018) xxx–xxx

4

Table 2 Patients profile. Age

Gender

MGFA clinical classification

Oral intake

MG-ADL score

QMG score

54 67 65 67 54 54 56 44 52 59 49 22 50

F M M F F M M F F M F M M

IIa IIb IIb IIb IIb IIb IIb IIIa IIIa IIIa IIIa IIIb IIIb

Regular Soft diet Regular Regular Regular Regular Regular Soft diet Regular Regular Regular Regular Regular

5 – 1 10 – 7 12 16 11 3 9 7 4

7 8 9 16 5 10 16 17 17 10 12 9 7

ageal segment and clinical neurological evaluation of the MGADL and QMG scores. Also, factors specifically associated with swallowing function on both the MG-ADL (chewing and swallowing) and the QMG (water swallowing, grip, and head elevation movement) tests were statistically examined for their correlation with Hyodo’s 4-point scale, also using Spearman’s rank-order correlation. Moreover, specifically for swallowing initiation, the amount of residue in the VC and PS of MGFA IIa/ IIIa (predominantly affecting the limbs, axial muscles, or both, potentially with the lesser involvement of the oropharyngeal muscles) vs. MGFA IIb/IIIb (predominantly affecting the oropharyngeal muscles, respiratory muscles, or both, potentially with the lesser or equal involvement of the limbs, axial muscles, or both) patients was statistically analyzed using the Mann–Whitney U test. When, there was significant difference between two parameters, since sample size was relatively small (N = 13), power analysis was additionally performed to guarantee the validity of the sample size for each parameter. 3. Results All of the patients reported swallowing difficulty; none had aspiration pneumonia and fixed vocal fold. Table 2 lists the characteristics of the study patients, including age, sex, type of MG, MGFA, MG-ADL score, QMG score, and type of oral intake. The MGFA clinical classification of the 13 patients was

as follows: MGFA IIa: n = 1, IIIa: n = 4, IIb: n = 6, and IIIb: n = 2 (Table 2). Fig. 1 presents the scores of the swallowing dysfunction parameters examined in the 13 patients using FE and VF. None of the patients had signs of aspiration. Initiation of pharyngeal swallow, pharyngeal residue, tongue base retraction, and pharyngeal constriction were slightly disturbed but laryngeal elevation and pharyngo-esophageal segment were close to the normal level and scored as 0 in all patients examined by both FE and VF (Fig. 1). Fig. 2 presents the correlation of total score of four-point scale (Hyodo’s original FE scale) with MG-ADL score and QMG score. None of them have significant correlation with Hyodo’s scale. Fig. 3 presents a statistical comparison of the three parameters (delayed initiation, pharyngeal clearance in VC and PS) examined by both FE and VF and Hyodo’s four-point scale examined with FE alone in patients with MGFA IIa/IIIa and MGFA IIb/IIIb disease. The Hyodo’s four-point scale examined by FE and pharyngeal residue examined by VF were significantly (p = 0.03, power = 0.84, p = 0.04, power = 0.79, respectively) more severe in patients with MGFA IIb/IIIb disease than in those with MGFA IIa/IIIa disease, respectively. Table 3 lists the results of the correlation analysis of the MG-ADL and QMG scores and all swallowing dysfunction parameters evaluated with VF and FE. None of the parameters used to assess swallowing dysfunction correlated significantly with the MGADL and QMG scores. Table 4 presents factors specifically

Fig. 1. Scores for each parameter assessing swallowing dysfunction in the 13 patients examined with FE and VF. None of the patients had aspiration. Initiation of pharyngeal swallow, pharyngeal residue (in total for VF and in PS and VC for FE), the tongue base retraction, and pharyngeal constriction were slightly disturbed, but laryngeal elevation and pharyngo-esophageal segment were considered to be normal and thus scored as 0 in all patients.

Please cite this article in press as: Kumai Y, et al. Assessment of oropharyngeal swallowing dysfunction in myasthenia gravis patients presenting with difficulty in swallowing. Auris Nasus Larynx (2018), https://doi.org/10.1016/j.anl.2018.10.004

G Model

ANL-RR2517; No. of Pages 7 Y. Kumai et al. / Auris Nasus Larynx xxx (2018) xxx–xxx

5

Fig. 2. The correlation of total score of four-point scale (Hyodo’s original FE scale) with MG-ADL score and QMG score. None of them have significant correlation with Hyodo’s scale.

associated with swallowing function in both the MG-ADL (chewing and swallowing) and the QMG (water swallowing, grip, and head elevation movement) tests, which were statistically examined for their correlation with Hyodo’s 4point scale using Spearman’s rank-order correlation. Among these factors, high correlation with Hyodo’s 4-point scale was determined only for grip, both in males (r = 0.76) and females (r = 0.69). 4. Discussion Dysphagia is a frequent symptom in patients with MG [17,18], 6–15% of whom present with dysphagia as the first symptom of the disease [19]. Even among patients with mild to moderate MG (MGFA II or III), silent aspiration occurs in 35% [2,8]. However, few studies have focused on the clinical characteristics of MG patients with mild swallowing dysfunc-

tion, the prediction of aspiration, or the correlation between clinical neurological presentation and swallowing dysfunction in MG. The first interesting finding of this study was that even though they did not present with aspiration but only with swallowing difficulty, patients with MGFA IIb/IIIb disease had severely impaired pharyngeal muscles examined with VF. Therefore, the swallowing dysfunction in these patients, specifically the reduced pharyngeal clearance, must be managed. One concern for this interpretation is that MGFA classification is not objective but subjective clinical evaluation method. Jaretzki described that this MGFA classification is designed to identify subgroups of patients with MG who share distinct clinical features or severity of disease that may indicate different prognoses or responses to therapy. Therefore, this should not be used to measure outcome and it defers quantitative assessment of muscle weakness to the more precise Quantitative MG Score for Disease Severity [9] and

Fig. 3. Statistical comparison of the three parameters (delayed initiation, pharyngeal clearance in VC and PS) examined by both FE and VF and Hyodo’s four point scale examined with FE alone in patients with MGFA IIa/IIIa and MGFA IIb/IIIb disease were performed. Hyodo’s four point scale examined by FE and pharyngeal residue examined by VF were significantly (p = 0.03, power = 0.84, p = 0.04, power = 0.79, respectively) more severe in patients with MGFA IIb/IIIb disease than in those with MGFA IIa/IIIa disease, respectively.

Please cite this article in press as: Kumai Y, et al. Assessment of oropharyngeal swallowing dysfunction in myasthenia gravis patients presenting with difficulty in swallowing. Auris Nasus Larynx (2018), https://doi.org/10.1016/j.anl.2018.10.004

G Model

ANL-RR2517; No. of Pages 7 Y. Kumai et al. / Auris Nasus Larynx xxx (2018) xxx–xxx

6

Table 3 Correlation between clinical neurological score and parameters for swallowing dysfunction. FE

MG-ADL score QMG score

VF

IPS

VC

PS

PAS

IPS

PR

PAS

TBR

PC

LE

PES

r = 0.13 p > 0.05 r = 0.21 p > 0.05

r = 0.01 p > 0.05 r = 0.24 p > 0.05

r = 0.08 p > 0.05 r = 0.36 p > 0.05

r = 0.46 p > 0.05 r = 0.22 p > 0.05

r = 0.15 p > 0.05 r = 0.19 p > 0.05

r = 0.03 p > 0.05 r = 0.19 p > 0.05

r = 0.40 p > 0.05 r = 0.27 p > 0.05

r = 0.45 p > 0.05 r = 0.36 p > 0.05

r = 0.51 p > 0.05 r = 0.52 p > 0.05

r = 0.10 p > 0.05 r = 0.16 p > 0.05

r = 0.29 p > 0.05 r = 0.24 p > 0.05

FE, fiberoptic endoscopic evaluation of swallowing; VF, video fluoroscopic swallowing study; IPS, initiation of pharyngeal swallow; VC, pharyngeal clearance in vallecula; PS, pharyngeal clearance in pyriform sinus; PR, pharyngeal residue; PAS, penetration aspiration scale; TBR, tongue base retraction; PC, pharyngeal constriction; LE, laryngeal elevation; PES, pharyngo-esophageal segment. a Spearman rank-order correlation n = 13.

consequently, this evaluation alone without VF and FE would fail to precisely evaluate swallowing dysfunction in MG patients. Although an appropriate statistical comparison with an agematched group of non-MG patients was not performed, our VF results revealed mild impairments in swallowing initiation, tongue base mobility, and pharyngeal constriction in MG patients, all of which can be attributed to weak striated muscles, including the mandibular, lingual, velopharyngeal, and pharyngeal muscles [2]. Weaknesses in these muscles leads to impaired oral or pharyngeal phases and reduces the ability to clear pharyngeal residues, as demonstrated in the present study. Previous manometric study demonstrated that all seven MG patients in the study showed extremely low swallowing pressure at the all level of the pharynx compared with healthy men [20]. Pharyngeal residues in the PS reflect a reduced pharyngeal constriction, while abnormal pharyngeal peristalsis and the presence of pharyngeal residue in the VC are indicative of impaired tongue base retraction toward the pharyngeal wall [2]. Therefore, weakness of striated muscles at various anatomical pharyngeal regions would cause reduced pharyngeal residue as demonstrated in the present study and would cause silent aspiration. Higo et al. previously showed that despite a remarkably disturbed pharyngeal residue in the PS, the correlation of its severity with aspiration was not significant (p = 0.8). In contrast, disturbed laryngeal elevation (p = 0.001) and incomplete upper esophageal sphincter opening (p = 0.067), both of which were slightly disturbed in our patients, were previously shown to correlate with aspiration. Resolution of the discrepancy between that study and ours will require additional prospective research with a sufficient number of MG patients presenting with various degrees and locations of muscle weakness [8], and the inclusion of an age-matched control group. Our study also showed that the results of a clinical neurological assessment performed using the QMG and MG-

ADL scores did not correlate significantly with any of the parameters evaluated for oropharyngeal swallowing dysfunction, except the grip score in the QMG assessment. One possible explanation for this finding is that our MG patients had only mild to moderate swallowing dysfunction without aspiration; thus, the characteristics of swallowing dysfunction evaluated in this study may not parallel those seen clinically or described in other case reports. However, our results should alert neurologists to the risk of silent aspiration even in patients diagnosed with clinically and neurologically mild MG according to the QMG and MG-ADL scores. Koopman et al. reported that the total self-directed questionnaire score and the scores of two specific questions on the self-directed questionnaire, but not the total QMG score, correlated significantly with aspiration in 20 MG patients presenting with mild to moderate swallowing dysfunction [4]. Their pilot study revealed that simple clinical tools can predict which MG patients are at risk of aspiration, in contrast to VF observations. The latter focus only on aspiration and laryngeal penetration but not on the parameters evaluated in a detailed examination of oropharyngeal swallowing dysfunction, as in the present study. Based on these perspectives and our findings, we recommend the use of self-directed questionnaire [4] and consideration of the grip score within the QMG score, which strongly correlated with Hyodo’s 4-point scale, in screening the risk of aspiration in MG patients by neurologists, regardless of the total QMG score and the MG-ADL score. Patients identified as being at high risk of aspiration should as soon as possible undergo a detailed examination evaluating oropharyngeal dysfunction, such as VF or FE performed by a board-certified otolaryngologist. The limitations of this study were the small number of patients, the absence of an age-matched control group, and the fact that the entire spectrum of dysphagia severity with various concentration and volume of test materials was not assessed. It is therefore difficult to draw conclusions regarding precisely

Table 4 Correlation between parameters for swallowing dysfunction and factors associated with swallowing function. Factors

Chewing and swallowing (MG-ADL)

Water swallowing test (QMG)

Grip (male) (QMG)

Grip (female) (QMG)

Head elevation movement test (QMG)

Hyodo’s scale (FE)

r = 0.08 (p = 0.82)

r = 0.23 (p = 0.45)

r = 0.76 (p = 0.07)

r = 0.69 (p = 0.08)

r = 0.32 (p = 0.29)

Chewing and swallowing; based on subjective symptoms; water swallowing test, swallowing 4 oz. Water (1/2 cup); head elevation movement test, head lifted: (45%, supine) sec. a Spearman rank-order correlation n = 13 (M = 7, F = 6).

Please cite this article in press as: Kumai Y, et al. Assessment of oropharyngeal swallowing dysfunction in myasthenia gravis patients presenting with difficulty in swallowing. Auris Nasus Larynx (2018), https://doi.org/10.1016/j.anl.2018.10.004

G Model

ANL-RR2517; No. of Pages 7 Y. Kumai et al. / Auris Nasus Larynx xxx (2018) xxx–xxx

distinguished patterns of dysphagia in MG. A further prospective assessment of swallowing dysfunction with various concentration and volume of test materials in a sufficient number of MG patients presenting with swallowing difficulty without obvious aspiration and the inclusion of an age-matched control is needed. 5. Conclusion Patients with MGFA IIb/IIIb disease who present without aspiration but with swallowing difficulty alone require appropriate therapeutic management regardless of the MGADL and QMG scores (except the grip score within the QMG score). In these patients, swallowing dysfunction typically manifests as reduced pharyngeal clearance. The control of pharyngeal residue, especially in patients with MGFA IIb/IIIb disease, is essential to prevent silent aspiration. Cooperation between board-certified otolaryngologists and neurologists is indispensable for the management. Financial disclosure None. Level of evidence IV. References [1] Beekman R, Kuks JB, Oosterhuis HJ. Myasthenia gravis: diagnosis and follow-up of 100 consecutive patients. J Neurol 1997;244:112–8. [2] Colton-Hudson A, Koopman WJ, Moosa T, Smith D, Bach D, Nicolle M. A prospective assessment of the characteristics of dysphagia in myasthenia gravis. Dysphagia 2002;17:147–51. [3] Kluin KJ, Bromberg MB, Feldman EL, Simmons Z. Dysphagia in elderly men with myasthenia gravis. J Neurol Sci 1996;138:49–52. [4] Koopman WJ, Wiebe S, Colton-Hudson A, Moosa T, Smith D, Bach D, et al. Prediction of aspiration in myasthenia gravis. Muscle Nerve 2004;29:256–60. [5] Keesey JC. Clinical evaluation and management of myasthenia gravis. Muscle Nerve 2004;29:484–505.

7

[6] Khan OA, Campbell WW. Myasthenia gravis presenting as dysphagia: clinical considerations. Am J Gastroenterol 1994;89:1083–5. [7] Grob D, Arsura L, Brunner NG, Namba R. The course of myasthenia gravis and therapies affecting outcome. Ann N Y Acad Sci 1987;505:472–99. [8] Higo R, Nito T, Tayama N. Videofluoroscopic assessment of swallowing function in patients with myasthenia gravis. J Neurol Sci 2005;231:45–8. [9] Jaretzki 3rd A, Barohn RJ, Ernstoff RM, Kaminski HJ, Keesey JC, Penn AS, et al. Myasthenia gravis: recommendations for clinical research standards. Task Force of the Medical Scientific Advisory Board of the Myasthenia Gravis Foundation of America. Neurology 2000;55(1):16–23. [10] Wolfe GI, Herbelin L, Nation SP, Foster B, Bryan WW, Barohn RJ. Myasthenia gravis activities of daily living profile. Neurology 1999;52 (7):1487–9. [11] Barohn RJ, McIntire D, Herbelin L, Wolfe GI, Nations S, Bryan WW. Reliability testing of the quantitative myasthenia gravis score. Ann N Y Acad Sci 1998;13(841):769–72. [12] Kumai Y, Samejima Y, Watanabe M, Yumoto E. Videofluoroscopic evaluation of pharyngeal swallowing dysfunction after esophagectomy with three-field lymph node dissection. Eur Arch Otorhinolaryngol 2017;274:321–6. [13] Kumai Y, Samejima Y, Yumoto E. Postdeglutitive residue in vagus nerve paralysis and its association with feeding style. Eur Arch Otorhinolaryngol 2016;273:4369–75. [14] Hyodo M, Nishikubo K, Hirose K. New scoring proposed for endoscopic swallowing evaluation and clinical significance. Nihon Jibiinkoka Gakkai Kaiho 2010;113:670–8. [15] Chiba Y, Sano D, Ikui Y, Nishimura G, Yabuki K, Arai Y, et al. Predictive value of the Hyodo score in endoscopic evaluation of aspiration during swallowing. Auris Nasus Larynx 2018;45 (6):1214–20. [16] Martin-Harris B, Brodsky MB, Yvonne M, Castell DO, Schleicher M, Sandidge J, et al. MBS measurement tool for swallow impairmentMBSImp: establishing a standard. Dysphagia 2008;23(4):392–405. [17] Carpenter RC, Mc Donald TJ, Howard EM. The otolaryngologic presentation of myasthenia gravis. Laryngoscope 1979;89:922–8. [18] Huang MH, King KL, Chien KY. Esophageal manometric studies in patients with myasthenia gravis. J Thorac Cardiovasc Surg 1988;95:281–5. [19] Grob D, Arsura L, Brunner NG, Namba R. The course of myasthenia gravis and therapies affecting outcome. Ann N Y Acad Sci 1987;505:472–99. [20] Joshita Y, Yoshida M, Yoshida Y, Kimura K. Manometric study of the pharynx and pharyngoesophageal sphincter in myasthenia gravis. Rinsho Shinkeigaku 1990;30(9):944–51 [Japanese].

Please cite this article in press as: Kumai Y, et al. Assessment of oropharyngeal swallowing dysfunction in myasthenia gravis patients presenting with difficulty in swallowing. Auris Nasus Larynx (2018), https://doi.org/10.1016/j.anl.2018.10.004