Surface electromyography for diagnosing dysphagia in patients with cerebral palsy

Table 1 Demographic characteristics of participants in the oropharyngeal dysphagia and control groups n (%)

Characteristic	OPD group1(n = 20)	Control group2(n = 60)	P value
Sex
Male	14 (70.0)	42 (70.0)	1.0003
Female	6 (30.0)	18 (30.0)
Age (yr)	14.5 ± 6.2	14.5 ± 6.1	0.9984
Height (cm)	128.1 ± 19.2	153.4 ± 20.1	< 0.0014
Weight (kg)	25.4 ± 12.7	47.7 ± 17.6	< 0.0014
BMI (kg/m2)	14.6 ± 3.4	19.5 ± 3.5	< 0.0014
DOSS6
Level 1	8 (42.1)	0 (0.0)	< 0.0015
Level 2	0 (0.0)	0 (0.0)
Level 3	1 (5.3)	0 (0.0)
Level 4	4 (21.1)	0 (0.0)
Level 5	3 (15.8)	0 (0.0)
Level 6	3 (15.8)	0 (0.0)
Level 7	0 (0.0)	60 (100.0)

Data are presented as mean ± SD.

¹Participants in the dysphagia group had cerebral palsy;

²Participants in the control group did not have cerebral palsy and were healthy;

³Determined by χ² test;

⁴Determined by independent samples t-test;

⁵Determined by Fisher’s exact test;

⁶Dysphagia outcome and severity scale (DOSS) score was missing for one oropharyngeal dysphagia (OPD) patient. BMI: Body mass index. Level 7 = normal; Level 6 = within functional limits; Level 5 = mild dysphagia; Level 4 = mild to moderate dysphagia; Level 3 = moderate dysphagia; Level 2 = moderate to severe dysphagia; Level 1 = severe dysphagia.

Table 2 Surface electromyographic findings for participants in the oropharyngeal dysphagia and control groups after adjusting for body mass index

Characteristic	OPD group(n = 20)	Control group (n = 60)	β1 (SE)	P value
MSV (mL)	3.70 ± 3.01	54.50 ± 24.47	-33.87 (5.32)	< 0.001
At 3 mL swallowing volume
SMGMA (μV)	80.77 ± 65.00	35.02 ± 13.02	38.30 (10.21)	< 0.001
IMGMA (μV)	88.89 ± 78.52	30.23 ± 10.55	44.09 (11.68)	< 0.001
TDBMG (s)	0.35 ± 0.35	0.13 ± 0.12	0.22 (0.06)	< 0.001
ADBMG (μV)	60.59 ± 71.50	10.18 ± 11.49	38.55 (10.84)	< 0.001
At MSV
SMGMA (μV)	100.24 ± 96.96	52.78 ± 28.05	34.90 (16.10)	0.033
IMGMA (μV)	98.28 ± 89.75	51.32 ± 21.78	30.59 (14.20)	0.034
TDBMG (s)	0.35 ± 0.35	0.15 ± 0.15	0.20 (0.07)	0.004
ADBMG (μV)	62.87 ± 73.05	18.75 ± 22.00	33.92 (12.20)	0.007

Data are presented as mean ± SD unless otherwise indicated.

¹Mean difference between experimental and control group adjusted for body mass index (BMI). MSV: Maximum swallowing volume; SMGMA: Submental muscle group maximum amplitude; IMGMA: Infrahyoid muscle group maximum amplitude; TDBMG: Time difference between 2 muscle groups; ADBMG: Amplitude difference between 2 muscle groups; OPD: Oropharyngeal dysphagia.

Table 3 Spearman’s partial correlations between Dysphagia Outcome and Severity Scale score and surface electromyographic findings after adjusting for body mass index (n = 79¹)

Characteristic	Correlation coefficient	P value
At 3 mL swallowing volume
SMGMA (μV)	-0.329	0.003
IMGMA (μV)	-0.389	< 0.001
TDBMG (s)	-0.153	0.182
ADBMG (μV)	-0.353	0.002
At MSV
SMGMA (μV)	-0.117	0.309
IMGMA (μV)	-0.056	0.626
TDBMG (s)	-0.168	0.140
ADBMG (μV)	-0.193	0.091

¹One patient with a missing Dysphagia Outcome and Severity Scale score value was omitted from this analysis. MSV: Maximum swallowing volume; SMGMA: Submental muscle group maximum amplitude; IMGMA: Infrahyoid muscle group maximum amplitude; TDBMG: Time difference between 2 muscle groups; ADBMG: Amplitude difference between 2 muscle groups.

Table 4 Diagnostic performance of difference surface electromyographic parameters for detecting oropharyngeal dysphagia

Characteristic	AUC (95%CI)	P value	Optimal cutoff value	Sensitivity (%)	Specificity (%)	PPV (%)	NPV (%)	Accuracy (%)
At 3 mL swallowing volume
SMGMA (μV)	0.80 (0.68-0.92)1	< 0.001	39.27	80.0	73.3	50.0	91.7	75.0
IMGMA (μV)	0.88 (0.78-0.98)123	< 0.001	37.30	85.0	90.0	73.9	94.7	88.8
TDBMG (s)	0.72 (0.59-0.86)	< 0.001	0.19	70.0	70.0	43.8	87.5	70.0
ADBMG (μV)	0.82 (0.71-0.93)123	< 0.001	12.02	75.0	76.7	51.7	90.2	76.3
At MSV
SMGMA (μV)	0.63 (0.48-0.79)	0.091	110.00	40.0	98.3	88.9	83.1	83.8
IMGMA (μV)	0.64 (0.48-0.81)	0.097	79.55	45.0	90.0	60.0	83.1	78.8
TDBMG (s)	0.72 (0.59-0.84)	< 0.001	0.19	70.0	70.0	43.8	87.5	70.0
ADBMG (μV)	0.70 (0.56-0.84)	0.005	35.69	50.0	90.0	62.5	84.4	80.0

¹Area under receiver operating characteristic curve (AUC) significantly higher compared with submental muscle group maximum amplitude (SMGMA) at maximum swallowing volume (MSV) (P < 0.01, vs SMGMA at MSV);

²AUC significantly higher compared with infrahyoid muscle group maximum amplitude (IMGMA) at MSV (P < 0.05, vs IMGMA at MSV);

³AUC significantly higher compared with amplitude difference between 2 muscle groups (ADBMG) at MSV (P < 0.01, vs ADBMG at MSV). PPV: Positive predictive value; NA: Not applicable; NPV: Negative predictive value; TDBMG: Time difference between 2 muscle groups.

Table 5 Diagnostic performance of combinations of surface electromyography parameters at the 3 mL swallowing volume for detecting oropharyngeal dysphagia

sEMG parameters at the 3 mL swallowing volume	Sensitivity (%)	Specificity (%)	PPV (%)	NPV (%)	Accuracy (%)
Of 4 parameters
≥ 2 parameters met diagnostic criteria1	100	71.7	54.1	100	78.8
≥ 3 parameters met diagnostic criteria1	85.0	93.3	81.0	94.9	91.3
Of 3 parameters other than TDBMG
≥ 2 parameters met diagnostic criteria1	95.0	75.0	55.9	97.8	80.0

¹Diagnostic criteria of each surface electromyography (sEMG) parameter at the 3 mL are as follows: submental muscle group maximum amplitude (SMGMA) ≥ 39.27 μV; infrahyoid muscle group maximum amplitude (IMGMA) ≥ 37.30 μV; time difference between 2 muscle groups (TDBMG) ≥ 0.19 s; amplitude difference between 2 muscle groups (ADBMG) ≥ 12.02 μV. AUC: Area under receiver operating characteristic curve; PPV: Positive predictive value; NA: Not applicable; NPV: Negative predictive value; MSV: Maximum swallowing volume.

Table 6 Summary of studies of non-invasive screening methods for oropharyngeal dysphagia

Ref.	Test	No. of participants	Sensitivity (%)	Specificity (%)	PPV (%)	NPV (%)
DePippo et al[24]	Burke Dysphagia Screening Test	44	76	59	-	-
Gottlieb et al[25]	50 mL Drinking Test	180	80	86	-	-
Ellul et al[26]	Standardized Swallowing Assessment	136	68	86	50	88
Smithard et al[27]	Bedside Swallowing Assessment	83	70	66	50	85
Hinds et al[28]	Timed Test	115	73	67	-	-
Mari et al[29]	3oz Water Swallow Test	93	74	74	71	77
Smith et al[30]	Pulse Oximetry	53	86	-	69
Martino et al[31]	Toronto Bedside Swallowing Screening Test	115	82	39	24	90
Kopey et al[32]	3-Sp Test	223	21	99	88	72
Antonios et al[33]	Modified Mann Assessment of Swallowing Ability	150	93	86	79	95

PPV: Positive predictive value; NPV: Negative predictive value.