SUPPLEMENTARY MATERIAL

Supplementary material 1: Modified barium swallow study measures

Modified Barium Swallow Impairment Profile (MBSImP)

The MBSImP is a standardized and validated tool to assess oropharyngeal swallow physiology to

determine the underlying impairment. Seventeen different components are independently scored

on a 3- to 5-point ordinal scale during up to 11 different swallow tasks (e.g., teaspoon thin, cup

sip nectar, solid) (Table 1). Components 1 to 6 denote oral swallow impairments and their sum

the oral total score (min 0, max 22); components 7 to 16 denote pharyngeal swallow impairment

and their sum the pharyngeal total score (min 0, max 29). Component 17 rates esophageal

clearance in the upright position (min 0, max 4). We scored all components for each swallow

separately, and calculated an overall impression (OI) score that was the worst score across all

swallow tasks for each of the 17 swallow components. For all individual components, as well as

overall impression scores, higher scores indicate more severe impairment, and lower scores

indicate less severe impairment.

1

Table 1: Components of the Modified Barium Swallow Impairment Profile (MBSImP)

Oral Components

Component 1 – Lip Closure

Component 2 – Tongue Control During Bolus Hold

Component 3 – Bolus Preparation / Mastication

Component 4 – Bolus Transport / Lingual Motion

Component 5 – Oral Residue

Component 6 – Initiation of Pharyngeal Swallow

Pharyngeal Components

Component 7 – Soft palate elevation

Component 8 – Laryngeal elevation

Component 9 – Anterior hyoid excursion

Component 10 – Epiglottic movement

Component 11 – Laryngeal vestibular closure

Component 12 – Pharyngeal stripping wave

Component 13 – Pharyngeal contraction

Component 14 – PES opening

Component 15 – Tongue base retraction

Component 16 – Pharyngeal residue

Esophageal Component

Component 17 – Esophageal clearance in upright position

2

Penetration-Aspiration Scale (PAS)

The PAS assesses the entrance of bolus material into the lower airways. It uses a standardized,

valid and reliable 8-point ordinal scale, that determines the depth of airway entrance and the

whether the material was expectorated afterwards (Rosenbek et al., 1996). We scored the PAS

on every swallow task and calculated the worst score across tasks.

Timing Measures

Timing, distance, and speed measures are known to vary by bolus characteristics (Molfenter &

Steele, 2011, 2012), thus, we obtained those measures separately per bolus and only for the first

and second teaspoons thin liquid, teaspoon nectar thick liquid and teaspoon pudding, because

they were presented in standardized volumes (5ml bolus applications via a spoon). Additionally,

we calculated the average between the first and second teaspoons thin liquid. We obtained 17

timing measures (Table 2) for up to 5 different swallow conditions; in total, up to 85 timing

measures per patient. We used the movie player “Quick Time Player” (Version 7.6.6; Apple Inc.)

to count and identify frame numbers for events of interests. We multiplied the number of frames

3

with the duration of one frame (1000ms divided by 30 frames = 33.33ms) to calculate the time of

events in milliseconds.

Table 2: Timing measures, their definitions and references as applied to the first and second

teaspoon thin liquid, average of both teaspoon thin liquid, teaspoon nectar thick liquid and

teaspoon pudding.

Timing measure Operational definition Reference

Oral transit time Onset of posterior movement of

bolus head* in the oral cavity during

first productive tongue

movement*until bolus tail* passes

the ramus of mandible*

None

Pharyngeal transit

time

Bolus head* arrival at the ramus of

mandible* until the bolus tail*

passes through the

pharyngoesophageal segment

(Logemann et al.,

1993)

Hypopharyngeal

transit time

Arrival of the bolus head* in the

valleculae until exit of the bolus

tail* from or closure of the

pharyngoesophageal segment

(Leonard & Kendall,

1997; Kendall et al.,

2000)

Pharyngeal delay

time

Arrival of the bolus head* at ramus

of mandible until first laryngeal

(Logemann et al.,

1993)

4

elevation

Stage transition

duration

Arrival of the bolus head* at ramus

of mandible until onset of hyoid

movement*

(Daniels et al., 2009)

Laryngeal response

time

Time from bolus* head arriving in

the pyriforms until maximum

laryngeal closure

None

Modified pharyngeal

response time

Time from onset of hyoid

movement* until bolus tail* passes

through the pharyngoesophageal

segment (originally the start of the

pharyngeal response time was

defined as the first laryngeal

elevation)

Adapted from

(Logemann et al.,

1993)

Pharyngoesophageal

segment opening

duration

Onset to termination of

pharyngoesophageal segment

opening

(Logemann et al.,

1993)

Velopharyngeal

closure duration

Onset to termination of velar

contraction to the posterior

pharyngeal wall

(Logemann et al.,

1993)

Duration of soft

palate elevation

Onset soft palate elevation until

maximal soft palate elevation

(Leonard & Kendall,

1997; Kendall et al.,

2000)

5

Duration of hyoid

excursion

Onset of hyoid movement* until

maximal hyoid excursion

(Logemann et al.,

1993; Martin-Harris

et al., 2003)

Hyoid movement Onset of hyoid movement* until

hyoid is back to rest position

(Leonard & Kendall,

1997)

Laryngeal vestibule

reaction time

Onset of hyoid movement* until

maximal laryngeal closure

(Nascimento et al.,

2017)

Duration of laryngeal

elevation

Onset to termination of laryngeal

elevation

(Logemann et al.,

1993)

Duration of laryngeal

closure

Onset of laryngeal closure (first

reduction in air contrast in laryngeal

inlet) until first laryngeal re-opening

(first appearance of air contrast in

laryngeal inlet)

Martin-Harris,

Brodsky, Price,

Michel, & Walters,

2003

Duration of

maximum laryngeal

closure

Onset to termination of maximal

laryngeal closure

(Leonard & Kendall,

1997; Kendall et al.,

2000)

Time from first

cricopharyngeal

opening to first

closure of the

laryngeal vestibule

Time from first cricopharyngeal

opening to first closure of the

laryngeal vestibule

(Logemann et al.,

1993)

6

*Further explanations: bolus head = leading edge of the bolus, including small drizzles of the

bolus; bolus tail: finishing edge of the bolus or of the part of the bolus that is swallowed;

productive tongue movement = tongue movement that results into transport of at least part of the

bolus into the pharynx; ramus of mandible = lower rim of the mandible crosses the tongue base;

onset of hyoid movement = import: brisk anterior-superior hyoid movement, not just when hyoid

is jumping a little bit up and down no anticipatory movement.

Distance and Area Measures

We applied 10 distance and area measures (Table 3, supplement 1) for each of the same five

swallow conditions as the timing measures. Thus, we collected up to 50 distance and areas

measures for each patient’s MBSS. We used ImageJ software (version 1.50i, U.S. National

Institutes of Health, Bathesda, Maryland, USA) to calculate the distance and area measures. We

used the distance between the second and fourth cervical vertebrae as 1) an anatomical scalar and

2) to correct for variation in patient height (Steele et al., 2011; Thompson et al., 2014; Nagy et

al., 2015).

Table 3: Distance and area measures, their definitions and references as applied to the first and

second teaspoon thin liquid, average of both teaspoon thin liquid, teaspoon nectar thick liquid

and teaspoon pudding. See Table 4 for graphical explanations of the measures.

Distance and area

measure

Operational definition Reference

7

Hyoid excursion in

reference to the

mandible

Distance between the hyoid position

during bolus hold and at its

maximum excursion

(Thompson et al.,

2014)

Hyoid excursion in

reference to the

vertebrae

Distance between the hyoid position

during bolus hold and at its

maximum excursion

(Leonard et al.,

2000; Thompson et

al., 2014).

Laryngeal elevation Difference in distance between the

posterior larynx and the cranial base

at bolus hold compared to maximum

elevation of the larynx

(Thompson et al.,

2014)

Hyolaryngeal

approximation

Difference in distance between the

anterior hyoid bone and the anterior-

superior tracheal air column at bolus

hold compared to maximum

excursion of the hyoid and

maximum elevation of the larynx

(Leonard et al.,

2000; Thompson et

al., 2014).

Base of tongue

retraction ratio

Ratio of the distance between the

base of tongue (using the lowest

point of the valleculae) and the axis

formed by the first and fourth

cervical vertebrae at the point of

maximum base of tongue retraction

divided by the distance at bolus hold

None

8

Pharyngeal

shortening

Difference in distance between the

bottom of the pyriform sinuses

(reflecting the upper esophageal

sphincter) and the nasal spine at the

hard palate at bolus hold compared

maximum excursion of the pyriform

sinuses

(Thompson et al.,

2014)

Pharyngoesophageal

segment opening

Distance of the narrowest part of the

pharyngoesophageal segment during

maximal distension

(Leonard et al.,

2000).

Pharyngeal

constriction ratio

Ratio of the pharyngeal area during

maximum constriction divided by

the pharyngeal area during bolus

hold

(Leonard et al.,

2011)

Normalized residue

ratio scale: valleculae

Comparison of the valleculae area

that is filled with residue to the total

valleculae area

(Pearson et al.,

2013).

Normalized residue

ratio scale: pyriform

sinuses

Comparison of the or pyriform

sinuses area that is filled with

residue to the total pyriform sinuses

area

(Pearson et al.,

2013).

9

Table 4: Graphical display of calculations of distance and area measures

Measures Graphical display Calculation

Hyoid excursion

in refernce to the

mandible

(Thompson et al.,

2014)

A: bolus hold, B: maximum hyoid

excursion

b−b’C 2C 4 ×100 = hyoid excursion as % of

C2-C4 length

Hyoid excursion

in refernce to the

vertebrae

(Leonard et al.,

2000; Thompson

et al., 2014).

C: bolus hold, D: maximum hyoid

excursion

xy'-xyC 2C 4 ×100= hyoid excursion as % of

C2-C4 length

A B

DC

10

Larynegal

elevation

(Thompson et al.,

2014)

E: bolus hold, F: maximum laryngeal

excursion

C 1L−C 1 ' L ' ’C 2 C 4

 × 100= larynx elevation

as % of C2-C4 length

Base of tongue

retraction ratio

G: bolus hold, H: maximum laryngeal

excursion)

a 'a = base of tongue retraction ratio

E F

G H

11

Pharynegal

shortening

(Thompson et al.,

2014)

I: bolus hold, J: maximum pharyngeal

shortening)

HPP−H P' P'

C 2C 4  ×100= pharyngeal

shortening as % of C2-C4 length

Pharyngoesophage

al segment

opening distance

(Leonard et al.,

2000).

Distance of the narrowest part of the

pharyngoesopheal segment during

maximal distension.

I J

12

Pharyngeal

constricton ratio

(Leonard et al.,

2000; Leonard et

al., 2011)

Pharyngeal Constriction Ratio =

PCR maxPCR hold

Normalized

residue ratio scale

(Pearson et al.,

2013)

Blue dotted line: vallecuale area (VALArea),

blue filled area: valleculae residue

(VALRes)

VALResVAL Area

x (VAL ResC 2C 4

x10)

= NRRS vallecula

Yellow dotted line: pyriform area (PSArea),

yelow filled area: pyriform residue (PSRes)

13

PS ResPS Area

x(PS ResC 2 C 4

x 10)

= NRRS pyriform sinuses

C1=anterior tubercle of the 1st cervical vertebrae (atlas), C2=inferior corner of the 2nd cervical vertebrae, C4= inferior corner of the

4th cervical vertebrae, H=inferior anterior corner of the hyoid, HP=nasal spine at the hard palate, L=larynx defined as the posterior-

superior tracheal air column, M=mandible, P=pyriforms, V= base of tongue defined as lowest point in the valleculae

14

Hyoid Speed Measure

Hyoid speed reflects the distance of the hyoid travelled over time irrespective to direction (total

anterior-superior hyoid excursion) and thus, combines the hyoid excursion duration and

magnitude. We calculated hyoid excursion speed as the ratio of hyoid excursion magnitude (a) in

reference to the mandible, b) in reference to the vertebrae) divided by the excursion duration

(Barikroo et al., 2015; Nagy et al., 2015).

15

Supplementary material 2: Individual patient results for MBSImP overall impression scores

Patie

nt

Age

Les

ion

volu

me Oral components Pharyngeal components

Ora

l tot

alPh

aryn

geal

to

tal

Med

ian

PAS

C1

Left hemisphere strokes

L1 63 3.58 2 3 2 2 3 3 1 1 1 0 1 1 2 1 2 2 15 12 5 1

L2 73 120.01 1 0 2 3 1 3 0 0 1 0 0 0 0 1 1 9 2 1 1

L3 68 29.59 3 2 1 2 3 2 1 0 1 0 0 0 1 1 2 2 2 13 8 1 1

L4 85 19.00 4 2 2 2 3 3 1 1 1 0 0 0 1 1 1 1 1 16 5 2 1

L5 75 45.36 4 1 3 2 2 0 0 1 0 0 0 0 1 2 2 12 6 1 1

L6 59 57.95 2 0 3 3 3 0 1 1 1 1 1 1 2 2 11 10 6 2

L7 45 178.07 0 1 3 3 2 3 0 1 1 0 1 1 1 2 2 12 9 2 1

L8 44 174.68 4 2 0 0 2 3 0 1 0 0 0 0 0 1 2 1 0 11 4 8 1

L9 93 1.22 0 1 1 2 2 3 0 1 1 0 1 0 0 1 1 2 1 9 7 8 1

L10 69 99.60 1 1 2 0 2 1 0 1 0 0 0 0 0 1 1 1 1 6 3 2 1

16

L11 44 360.72 3 1 3 2 4 3 0 1 1 2 0 1 0 1 2 1 16 8 7 1

L12 90 1.92 2 1 0 2 2 3 1 1 1 1 1 1 2 1 3 2 1 10 14 7 3

L13 56 154.07 1 3 2 2 2 3 1 1 0 0 1 0 0 1 2 2 1 12 8 8 3

L14 78 161.36 1 1 0 2 2 3 0 0 0 0 0 0 0 1 1 1 8 1 1 1

L15 74 149.16 1 1 2 2 3 0 0 1 0 0 0 0 1 2 1 8 4 1 1

L16 58 173.57 2 1 2 2 3 3 0 0 0 0 0 0 0 1 1 1 1 13 1 1 1

L17 64 93.68 3 1 2 3 3 0 1 1 2 1 1 1 3 3 12 13 2 1

L18 62 2.17 4 2 1 0 3 3 0 0 0 0 0 0 0 1 2 1 1 13 3 1 1

L19 85 29.14 2 2 3 4 3 0 2 1 1 1 1 2 3 3 14 14 5 3

L20 87 14.34 4 1 2 3 3 1 0 0 0 1 0 1 1 2 2 14 7 1 1

L21 77 78.19 2 3 0 0 1 3 0 0 0 0 0 0 2 1 1 1 2 8 3 1 1

L22 51 186.35 4 1 2 3 4 3 0 0 0 1 0 1 2 2 2 17 8 5 1

Patie

nt

Age

Les

ion

volu

me Oral components Pharyngeal components

Ora

l tot

alPh

aryn

geal

to

tal

Med

ian

PAS

C1

17

Right hemisphere strokes

R1 61 88.19 1 1 3 2 2 3 0 1 1 1 1 0 1 2 2 11 9 7 5

R2 50 0.97 2 3 2 3 2 3 1 1 0 0 1 0 0 1 1 2 1 15 6 3 1

R3 72 20.71 1 1 2 2 2 3 1 1 0 1 1 1 1 2 2 10 10 8 2

R4 82 6.92 1 1 0 3 3 3 1 1 1 0 1 1 0 2 2 2 10 11 7 2

R5 77 93.82 2 3 3 3 3 1 2 1 2 2 1 1 3 3 14 16 8 6

R6 48 247.38 4 2 2 2 3 3 1 1 0 0 0 0 0 0 2 2 16 6 8 1

R7 72 59.46 4 2 0 3 2 3 1 1 1 1 1 1 1 1 2 2 2 14 14 3 1

R8 85 64.53 4 2 3 3 3 3 0 2 2 1 2 1 2 3 3 18 16 8 7

R9 62 0.21 1 1 2 4 0 1 1 1 2 1 1 2 3 3 7 15 8 2

R10 68 304.30 4 1 2 3 3 0 1 1 1 1 1 1 1 2 2 13 11 5 3

R11 64 1.06 1 1 1 2 2 3 1 1 1 1 1 1 1 2 2 9 11 7 1

R12 57 63.45 0 2 3 3 3 0 1 1 2 1 1 1 3 3 1 11 13 8 5

R13 87 306.53 1 2 2 2 3 0 1 1 0 1 0 0 1 2 1 9 6 5 1

R14 87 14.73 2 1 3 2 2 2 0 0 1 0 0 1 0 1 2 2 2 12 7 2 1

R15 65 8.29 4 1 2 0 2 3 0 0 1 0 0 0 0 1 2 2 2 12 6 1 1

R16 77 11.80 1 1 0 2 3 3 0 1 1 1 0 1 0 2 2 2 2 9 19 2 1

18

R17 58 97.89 4 2 2 2 4 3 0 1 1 0 1 2 1 2 2 17 11 3 1

R18 80 337.29 3 1 3 2 2 0 1 1 1 1 1 1 2 2 11 10 2 2

R19 95 41.28 2 2 1 3 4 3 0 1 1 1 1 0 0 1 3 2 15 10 3 2.5

R20 37 334.06 2 2 0 1 2 3 1 1 0 0 1 0 1 1 1 10 4 2 1

R21 51 290.46 2 1 0 1 2 3 0 1 0 0 0 0 0 1 1 2 9 4 2 1

R22 62 147.16 1 1 2 3 3 3 2 1 1 1 1 0 1 2 2 12 11 3 3

R23 28 62.48 2 1 0 2 3 0 1 0 1 1 1 0 1 1 1 8 5 5 1

R24 79 130.22 4 1 2 2 3 3 1 1 1 0 1 1 2 1 2 2 15 12 5 5

C1-C17=MBSImP components; PAS=Penetration-Aspiration Scale

Green color denotes “not impaired” and red colors denote “impaired” MBSImP components or PAS scores; empty cells denote missing data

19

Supplementary material 3: Results for timing measures

Results only for swallows where the majority of the bolus was transported from the oral into the

pharyngeal cavity

When we excluded swallows where the majority of the bolus remained in the oral cavity (scores

of >2 for the MBSImP component 5 “oral residue”), only velopharyngeal closure duration for

teaspoon nectar (p=0.03) was statistically significant with patients with right hemisphere strokes

showing longer velopharyngeal closure duration than patients with left hemisphere strokes.

Results for any swallows independently of the bolus amount remaining in the oral cavity

When we included all swallows – independent of the bolus amount transported from the oral into

the pharyngeal cavity – differences in timing measures between patients with left and right

hemispheric strokes were mostly found for one teaspoon pudding swallows, shown in Figure S1.

Pharyngeal transit time and hypopharyngeal transit time were significantly longer in patients with right

hemispheric strokes compared to patients with left hemispheric strokes (p=0.04, for both). Oral transit

time, pharyngeal delay time and stage transition duration showed a trend (p<0.01) for longer durations in

patients with right hemispheric strokes compared to patients with left hemispheric strokes. After

controlling for age, race, and lesion volume in a liner multivariable regression model, pharyngeal transit

time, hypopharyngeal transit time, pharyngeal delay time, and stage transition duration were significantly

longer (p0.05) and oral transit time showed a trend to be significantly longer (p=0.06) in patients with

right compared to left hemispheric strokes for swallowing one teaspoon of pudding.

In addition to the timing measures of one teaspoon of pudding, the following other timing measures

showed at least a trend towards significant differences between patients with left and right hemispheric

strokes: hyoid excursion duration for the first teaspoon thin swallow (p=0.01; left hemispheric stroke

patients had longer durations than right); time from first cricopharyngeal opening to first closure of the

20

laryngeal vestibule for the average of two teaspoon swallows of thin (p=0.08; right longer than left);

velopharyngeal closure duration for teaspoon nectar swallow (p=0.02; right longer than left).

Velopharyngeal closure duration for teaspoon nectar swallow remained significant after controlling for

confounders (p=0.007; right longer than left).

21

Figure S1: Timing measures for one teaspoon pudding compared between patients with left and right hemispheric strokes (two sided

Wilcoxon-rank-sum- test: * = p≤0.05, T = p≤0.1).

22

Supplementary material 4: Distance and area measures for all swallows and only swallows with majority of bolus transported from oral

into pharyngeal cavity

Table S2: Distance and area measures compared between patients with left and right hemispheric strokes. Only measures are listed

that had a p-value of ≤0.1 in either the analysis with all swallows, or the analysis excluding swallows where the majority of the bolus

remained in the oral cavity. Underlined are all measures that we interpret as worse swallow physiology by group. NS=not significant

or no trend towards significance (p-value >0.1; diff.=difference test with the two-sided Wilcoxon-rank-sum-test; adj.=adjusted p-

values based on linear multivariable regression models with age, race, and lesion volume as control variables.

All swallows Only swallows with MBSImP oral residue score < 3

Left (N=22)Mean (SD), N

Right (N=24)Mean (SD), N

p-value (diff.)

p-value (adj.)

Left (N=22)Mean (SD), N

Right (N=24)Mean (SD), N

p-value (diff.)

p-value (adj.)

1st Teaspoon ThinNormalized residue rating scale - valleculae

0.003 (0.006), 21

0.05 (0.13), 20 0.06 0.08 0.004 (0.007), 19

0.05 (0.13), 20 NS 0.08

2nd Teaspoon ThinNormalized residue rating scale - valleculae

0.06 (0.15), 17 0.08 (0.13), 20 0.08 NS 0.06 (0.15), 15 0.06 (0.11), 18 0.10 NS

Average 1st and 2nd Teaspoon Thin

Superior laryngeal movement 0.79 (0.18), 16 0.67 (0.19), 17 0.09 NS 0.29 (0.11), 14 0.32 (0.16), 15 NS NSHyolaryngeal approximation 0.37 (0.11), 16 0.29 (0.13), 17 0.09 NS 0.36 (0.12), 14 0.29 (0.14), 15 NS NS

Teaspoon NectarHyoid excursion (reference mandible)

0.32 (0.13), 21 0.25 (0.11), 20 0.04 0.09 0.32 (0.13), 20 0.26 (0.09), 19 0.07 NS

23

Hyoid excursion (reference vertebrae)

0.39 (0.10), 21 0.32 (0.11), 20 0.07 NS 0.39 (0.10), 20 0.32 (0.11), 19 0.09 NS

Hyolaryngeal approximation 0.33 (0.13), 21 0.25 (0.16), 20 NS NS 0.33 (0.13), 20 0.24 (0.16), 19 0.09 NSNormalized residue rating scale - valleculae

0.10 (0.16), 21 0.23 (0.23), 20 0.03 0.08 0.10 (0.17), 20 0.23 (0.24), 19 0.04 NS

Teaspoon PuddingHyoid excursion (reference mandible)

0.38 (0.14), 20 0.23 (0.13), 22 0.001 0.001 0.35 (0.15), 15 0.21 (0.14), 16 0.01 0.01

Hyoid excursion (reference vertebrae)

0.46 (0.16), 20 0.36 (0.15), 22 0.04 0.07 0.46 (0.14), 15 0.38 (0.16), 16 NS NS

Superior laryngeal movement 0.79 (0.19), 20 0.65 (0.21), 21 0.08 0.05 0.78 (0.18), 15 0.65 (0.24), 15 NS NSTongue base retraction ratio 0.54 (0.15), 20 0.64 (0.18), 22 0.10 0.07 0.57 (0.17), 15 0.63 (0.18), 16 NS NSNormalized residue rating scale – valleculae

0.08 (0.17), 20 0.04 (0.05), 22 0.01 NS 0.07 (0.17), 15 0.32 (0.49), 16 0.01 NS

Normalized residue rating scale – piriforms

0.05 (0.13), 20 0.04 (0.05), 22 NS NS 0.04 (0.14), 15 0.03 (0.04), 16 0.08 NS

Pharyngeal constriction ratio 0.06 (0.07), 20 0.15 (0.19), 22 0.03 NS 0.06 (0.07), 15 0.12 (0.13), 16 0.08 NS

24

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