Impressions of Esophageal Clearance Under Two Conditions During the Modified Barium Swallow Study: A Pilot Study

Abstract

Background:

Esophageal visualization is an important aspect of the Modified Barium Swallow Study (MBSS). Sequential swallows have an impact on esophageal clearance; however, standard cueing for esophageal clearance does not limit the number of times a patient swallows. We aimed to determine the potential impact of providing additional verbal cues related to the number of times to swallow on impressions of esophageal clearance during the MBSS.

Methods:

Standard of care MBSS were performed using the Modified Barium Swallow Impairment Profile (MBSImP). In the standard MBSImP condition, participants were instructed to “swallow when you’re ready.” Whereas, in the experimental condition, participants were instructed to “only swallow one time.” We report a combination of MBSImP component 17 scores (esophageal clearance) for both conditions. We performed tests of association and determine if statistically significant associations exist between MBSImP component 17 scores under two conditions.

Results:

Thirty-six participants qualified for this study. Esophageal clearance scores changed in 14 (38.9%) of participants when comparing between the two conditions. For participants with score change, 57.1% had an increase (more altered clearance) and 42.9% had a decrease (more typical clearance) in scores. A significant association was identified for esophageal clearance (component 17) scores in the standard versus experimental conditions (P < 0.0001).

Conclusion:

Impressions of esophageal clearance (component 17) changed in 38.9% of participants in the experimental condition, with over half of those whose score changed indicating more atypical esophageal clearance. Our results illuminate the need for further study into the contexts in which impressions of esophageal clearance during the MBSS are made.

Visual Abstract

Keywords

deglutition disorder swallowing fluoroscopy esophagus

Introduction

The Modified Barium Swallow (MBSS) study is an important exam for the assessment of swallow function. The MBSS study traditionally involves examination of the swallowing continuum (eg, oral cavity, pharynx, and esophagus) with various liquid viscosities and food textures with the patient seated or standing unless positioning techniques are being trialed.¹

Historic expert opinion and early work identified interrelationships between aspects of the swallowing continuum, oropharyngeal and esophageal, as early as 1985.^2
-4 More recently, the scientific evidence which supports incorporating esophageal visualization into standard MBSS practice continues to grow.^5
-11 However, practices relating to the fluoroscopic imaging of the oropharynx/pharynx and esophagus vary significantly in the literature.^{2
-4,6,10
-21}

Non-diagnostic visualization of the esophagus falls within the scope of practice for speech-language pathologists (SLP) according to the American Speech-Language Hearing Association (ASHA).^22
-24 The American College of Radiology (ACR) states that the assessment of esophageal clearance falls within the scope of the MBSS, whereas diagnostic assessment of the esophagus falls to other radiographic studies (eg, esophagram).²⁵ Both Watts et al¹¹ and Miles et al¹⁹ demonstrated that SLPs are capable of learning esophageal physiology and demonstrated their ability to identify abnormal esophageal bolus transit and need for further assessment (eg, Gastroenterology [GI] referral).^11,19 Non-diagnostic esophageal visualization during an MBSS is well-supported.^{5,8
-11,16
-18,20,26,27} While several standardized MBSS protocols exist, currently, the MBSImP is the only standardized, validated, and reliable protocol and scoring system that assess the physiology of swallowing components across all domains (oral, pharyngeal) for the MBSS and includes an esophageal visualization component.¹⁸ The MBSImP identifies the 17 physiologic components of swallowing, including the determination of esophageal clearance (component 17) in the upright position.¹⁸ For the judgement of esophageal clearance, the MBSImP protocol includes two swallows in the anterior-posterior plane with 5 mL of nectar-thick Varibar^® (barium sulfate) and 5 mL pudding Varibar. Per the standard MBSImP protocol, the patient is instructed to perform an oral bolus hold and then to “swallow when you’re ready.”²⁸ The bolus is then followed through the esophagogastric junction (EGJ) and bolus clearance though the esophageal body is judged. MBSImP component 17 (esophageal clearance) score has five possible scores: 0, or “complete clearance; esophageal coating,” 1, or “esophageal retention,” 2, or “esophageal retention without retrograde flow through the pharyngoesophageal segment (PES),” 3, or “esophageal retention with retrograde flow through [the] PES,” and 4, “minimal to no esophageal clearance.” Though esophageal visualization is non-diagnostic, scores are considered hierarchical. In the MBSImP protocol, the patient receives no other instruction other than to hold the bolus in the oral cavity until directed to “swallow when ready.”^29
-35

During swallowing, a bolus is propelled through the oropharynx and into the esophagus. Once in the esophageal body, the swallowed bolus is propelled by primary peristalsis where pressure is applied to the tail of the bolus as it moves through the length of the cervical and thoracic esophagus.³² Once the bolus is in the most distal esophagus it moves through the open LES through the esophagogastric junction (EGJ) and into the gastric cardia. Primary peristalsis is only initiated with a bolus that passes through the upper esophageal sphincter (UES). If this first wave is ineffective at clearing the bolus, a secondary peristaltic wave should be initiated to help clear the bolus through the EGJ. Non-propulsatile contractions of the esophagus are referred to as “tertiary contractions” if seen radiographically. These incomplete contractions may be consistent with ineffective esophageal motility (IEM) if certain manometric thresholds are met.³⁶ Though, weak, or failed swallows can occur in healthy normal patients. Per the Chicago Classification v4.0 for high-resolution esophageal manometry (HRM), it is normal to have up to 30% of swallows that are weak or “failed.”³⁶ However, there is some evidence to suggest that this is much higher in some healthy normal adults.^37,38 Deglutitive inhibition is a normal phenomenon resulting in the cessation or alteration of peristalsis in the case of “dry” swallows or rapid drinking.^29
-35 Meyer et al³³ identified 20 to 30 seconds as the time that it takes for the distal esophagus to “recover.” Importantly, not all swallows which follow less than 20 to 30 seconds after an initial swallow will result in inhibition, but rather an attenuation.^33
-35 If only two oropharyngeal swallows occur, there may be no significant esophageal consequence (inhibition or alteration of peristalsis) in healthy adults.³⁸

Patients with dysphagia, particularly if oropharyngeal in nature, may elicit multiple swallows for a single bolus.^39
-42 Patients without identifiable oropharyngeal pathophysiology who report oropharyngeal symptoms (eg, globus) may also elicit multiple swallows per bolus. Because oropharyngeal and esophageal physiology swallowing are interrelated—primary peristalsis can only be initiated by a bolus that passes the esophageal sphincter (eg, a swallow originated in the mouth); thus, the influence of multiple swallows on impressions of esophageal clearance is unknown. Therefore, we sought to investigate the influence of a cueing for single swallows on impressions of upright esophageal clearance during the MBSS. We hypothesized specific cueing, to swallow only once, would eliminate multiple swallows, and thus would result in a different determination of esophageal clearance compared to an un-cued condition for participants who swallow more than once per bolus.

Methods

Study Design

Between April 1, 2021 and July 15, 2021, participants were recruited from the Medical University of South Carolina (MUSC) speech-language pathology (SLP) clinics where MBSS are performed. Informed consent procedures were completed within all ethical standards and written consent was obtained prior to participation in study procedures. This study was approved by the MUSC Institutional Review Board (IRB) (Pro 00106650).

Inclusion and Exclusion Criteria

Inclusion criteria were established to include adults (18+ years) who were referred for an outpatient MBSS for an assessment of swallowing function as a standard of care. Those participants with any past medical history for altered oral, pharyngeal, and/or esophageal anatomy (eg, tongue resection, laryngectomy, or fundoplication) were excluded. Participants who were unable to follow or execute the instructions for the experimental (cued) condition were excluded.

All eligible participants had a Modified Barium Swallow Study (MBSS) using the MBS Impairment Profile (MBSImP™©) protocol and scoring system.¹⁸ Participants whose MBSS reports did not include any MBSImP scores or lacked an MBSImP component 17 (esophageal clearance) score under both conditions were excluded.

Modified Barium Swallow Study

All participants were referred for an MBSS as part of the standard of care for patients with complaints of, or concerns for, dysphagia. MBSS were performed at 30 pulses per second (pps) and were recorded at 30 frames per second (fps) according to best practices.^43,44 All MBSS were conducted using the Modified Barium Swallow Impairment Profile (MBSImP™©)¹⁸ protocol and scoring metric which measures 17 distinct physiologic components of swallowing. The core protocol uses 12 swallows across varying liquid and solid consistencies, the initial 10 in the lateral view, the last 2 in the anterior-posterior view. The standard MBSImP component 17, our outcome measure, is determined by the esophageal bolus clearance patterns through the esophageal body and lower esophageal sphincter (LES) in the A-P view with 5 mL nectar and 5 mL pudding contrast Varibar^® (Bracco Diagnostics Inc.). Per the standard MBSImP protocol, the patient is instructed to “Hold this in your mouth until I ask you to swallow,” and then, to “swallow when you’re ready.”²⁸ In the experimental condition, the participant was prompted by the clinician saying, “For these next two swallows I want you to swallow only one time.” For each bolus provision the participant was instructed to hold the bolus in their mouths until directed to “swallow once and only once, then keep your mouth open and focus on your breathing and don’t swallow again.” A period of 30 seconds was provided between the 5 mL nectar and 5 mL pudding boluses in the experimental condition. The standardized score was recorded in the MBSImP database and in the electronic health record (EHR), and the experimental score was recorded only in the MBSS EHR documentation and separately from other MBSImP scores. One-third of the studies were re-rated by the first and senior authors for reliability. Any discrepancies in scoring were rated by consensus between these two authors. If unable to reach a consensus, a third author was tasked with rating the swallow.

Statistical Analysis

Analysis was performed using SAS (v9.4, Cary, NC). Summary statistics were calculated for all variables collected (mean, median, the standard deviation for continuous variables and frequency, median, and mode for categorical variables). Our statistical hypothesis (H₀) was that there would be no statistically significant differences in MBSImP component 17 (esophageal clearance) scores in un-cued (standard MBSImP) versus cued (experimental) conditions. Fisher’s exact tests were used to describe categorical variables (eg, MBSImP component 17 scores) and determine if associations exist between scores in the two conditions (standard versus experimental). Our hypothesis was that there were no statistically significant associations. Mann-Whitney U/Wilcoxon Rank Sum tests were used to describe continuous variables (eg, age) Chi-Square or Fisher’s Exact tests were used to describe categorical variables. Findings reflect the overall statistical significance and for all statistical analyses, the alpha was set at 0.05 with P values of ≤0.05 indicating statistical significance.

Results

Participants

A total of 36 participants met study inclusion criteria. The average age of participants was 64 years (range 33-94). The majority (55.6%) of participants were female. Most participants were white (83.3%), and none identified as Hispanic. Most of the participants were referred by Laryngology (52.9%), followed by Primary Care (17.7%). While only 27.8% of participants’ medical records included a diagnosis of gastroesophageal reflux disease (GERD), 61.1% of participants were on a proton pump inhibitor (PPI) (eg, omeprazole) and 33.3% were on an H2-receptor antagonist (eg, famotidine). Of these patients, 9/25 (36%) were on both a PPI and an H2-receptor antagonist. Only 11/36 (30.6%) participants were not prescribed either medication. The most common participant-reported symptom was dysphagia to solids (55.6%), followed by coughing with eating (44.4%), dysphagia to pills (36.1%), and globus (27.8%). See Table 1 for further detail. Appendix A reports all MBSImP scores for this cohort.

Table 1.

Participant Demographics, Characteristics, and Baseline Data by Influence of Cueing on MBSImP Component 17 (Esophageal Clearance) Score.

Participant variables	Total n = 36 n (%)	No change in clearance n = 22 n (%)	Change in clearance n = 14 n (%)	P-value*
Age, mean, SD (95% CI)	64.1 ± 14.1 (60.1 69.6)	65.4 ± 15.6 (58.5, 72.3)	63.9 ± 11.7 (57.1, 70.6)	0.6490
Sex				0.8785
Female	20 (55.6)	12 (54.6)	8 (57.1)
Male	16 (44.4)	10 (45.5)	6 (42.9)
Race				0.3266
White	30 (83.3)	18 (81.8)	12 (85.7)
Black	5 (13.9)	4 (18.2)	1 (7.1)
Other	1 (2.8)	0 (0)	1 (7.1)
Ethnicity
Non-Hispanic	37 (100)	22 (100)	14 (100)
Past medical history
Pulmonary disease	9 (25)	6 (27.3)	3 (21.4)	1.000
Diabetes	8 (21.6)	6 (27.3)	3 (21.4)	0.2677
Thyroid disease	9 (25)	5 (22.7)	4 (28.6)	0.7115
Gastroesophageal reflux disease	10 (27.8)	9 (40.9)	1 (7.1)	0.0536
Other GI disorder, not esophageal	11 (30.6)	9 (40.9)	2 (14.3)	0.1419
Stroke	3 (8.3)	2 (9.1)	1 (7.1)	1.000
Neurodegenerative disease	3 (8.3)	1 (4.55)	2 (14.3)	0.5471
Seizure disorder or seizure history	2 (5.6)	1 (0)	1 (14.3)	0.1444
Migraine	5 (14.3)	3 (13.6)	2 (15.4)	1.000
Psychiatric disorder	6 (16.7)	3 (13.6)	3 (21.4)	1.000
Autoimmune disorder	5 (13.9)	3 (13.6)	2 (14.3)	0.3566
Medications
Proton pump inhibitor (PPI)	22 (61.1)	15 (68.2)	7 (50)	0.3142
H2-receptor antagonist	12 (33.3)	8 (36.4)	4 (28.6)	1.000
H1-receptor antagonist	6 (16.7)	4 (18.2)	2 (14.3)	0.6582
Gabapentin (neurontin)	11 (30.6)	7 (31.8)	4 (28.6)	1.000
Opioid	8 (22.2)	6 (27.3)	2 (14.3)	0.3609
Vitamin D	16 (44.4)	12 (54.4)	4 (28.6)	0.1263
Referral source				0.5106
Primary care	6 (17.7)	5 (35)	1 (7.1)
Laryngology	18 (52.9)	9 (45)	9 (62.3)
General ENT	5 (4.7)	1 (5)	4 (28.6)
Gastroenterology	1 (2.9)	1 (5)	0 (0)
Neurology	1 (2.9)	0 (0)	1 (7.1)
Report of symptoms
Dysphagia to liquids	15 (41.7)	10 (45.5)	5 (35.7)	0.5633
Dysphagia to solids	20 (55.6)	12 (54.6)	8 (57.1)	0.8785
Dysphagia to pills	13 (36.1)	8 (36.4)	5 (35.7)	0.9685
Coughing with eating/drinking	16 (44.4)	9 (40.9)	7 (50)	0.5926
Globus sensation	10 (27.8)	6 (27.3)	4 (28.6)	0.9324
Odynophagia	5 (13.9)	2 (9.1)	3 (21.4)	0.2967
Eructation	2 (5.4)	1 (4.6)	1 (7.1)	0.7401
Gagging	2 (5.6)	1 (4.6)	1 (7.1)	0.7401
Regurgitation/vomiting	2 (5.6)	1 (4.6)	1 (7.1)	0.7401
EAT-10 scores⁺ mean, SD (95% CI)	15.5 ± 11.2 (10.1, 20.9)	13.9 ± 9.6 (8.4, 19.4)	19.8 ± 15.3 (0.8, 38.8)	0.2432

Chi-Square or Fisher’s exact for categorical variables, Wilcoxon Rank-Sum for continuous variables. Alpha set at 0.05 to determine statistical significance.

Data not available for all participants.

Impressions of Esophageal Clearance Under Two Conditions

Component 17 (esophageal clearance) scores under the standard MBSImP protocol (un-cued) ranged from 0 to 4. Component 17 (esophageal clearance) scores changed between the standard and experimental conditions in 38.9% (14/36) of participants. For those with a change in component 17 scores, 42.9% (6/14) had a decrease (improvement in clearance) and 57.1% (8/14) had an increase (decline in clearance) in scores. A statistically significant association was identified for esophageal clearance (component 17) scores in the standard versus experimental condition (P < 0.0001). See Table 2.

Table 2.

Impressions of Esophageal Clearance (MBSImP Component 17) Scores Under Two Conditions.

Esophageal clearance scores	Standard condition n (%)	Experimental condition n (%)
0—Complete clearance, esophageal coating	6 (16.7)	5 (13.9%)
1—Esophageal retention	16 (44.4%)	20 (55.6)
2—Esophageal retention with retrograde flow below the PES	9 (25%)	6 (16.7)
3—Esophageal retention with retrograde flow through the PES	0 (0)	0 (0)
4—Minimal to no esophageal clearance	5 (13.9%)	9 (25)

Sub-Group Analysis of Participants with a Change in Component 17 (Esophageal Clearance) Scores Given Cueing

Fourteen participants were identified as having a change in component 17 scores in the cued (experimental) versus un-cued (standard) condition. The mean age for participants with a change in scores was 63.9 years (range 36-76, standard deviation ± 11.7). Most participants with a score change were female (57.1%) and almost all (85.7%) were white.

No statistically significant differences were seen between any of the other MBSImP components or swallowing outcome measures. However, results from comparisons with component 12 (pharyngeal stripping wave) might indicate a trend toward significance (P = 0.0609).

Decrease in Esophageal Clearance Scores

Six participants (6/14, 42.9%) were found to have a decrease in component 17 scores in our two study conditions indicating an impression for more typical esophageal clearance in the experimental (cued) condition. The mean age for participants who were found to have a decrease in component 17 scores was 64.8 years (range 53-74, standard deviation ± 9.5). Most, 5/7, (83.3%) participants in this subgroup of decreased scores were female and all were white.

Two (2/6, 33.3%) participants went from a score of 1 to a score of 0, thereby changing binary classifications from “atypical” to “typical” scores when comparing standard to experimental (cued) conditions. The remaining four participants (4/6, 66.7%) went from a score of 2 to a score of 1. This last change type represents a change in bolus retention patterns within the esophagus where patients in the cued condition no longer demonstrated retrograde flow.

Increase in Esophageal Clearance Scores

Eight participants (8/14, 57.1%) were found to have an increase in component 17 scores between the standard and experimental conditions indicating a more atypical impression of esophageal clearance in the experimental (cued) condition. The mean age for participants with an increase in component 17 scores was 63.1 years (range 36-76, standard deviation ± 13.7). Slightly fewer participants (3/7, 37.5%), in this subgroup of participants with an increase in scores, were female and almost all (6/7, 75%) were white.

A change from 0 to 1 was seen in 3 (3/8, 37.5%) participants, representing a change in binary classification from “typical” to “atypical” clearance when comparing the standard to the experimental conditions. One participants (1/8, 12.5%) demonstrated a change from a score of 1 to a score of 2. And three participants (3/8, 37.5%) changed from a score of 2 to a score of 4. This last change type representing the most “dramatic” of score changes (eg, largest score changes range) of this subgroup indicating that patients who had retention with retrograde flow within the esophageal body in the standard condition had minimal to no clearance in the experimental condition.

Discussion

When participants were provided a specific cue to swallow only once, impressions of esophageal clearance (component 17) changed in 38.9% of participants. In this small sample, providing an additional cue to swallow only one time resulted in more atypical clearance in the majority (57.1%) of our participants which contradicted our pre-study hypothesis that cueing would result in a reduction (improvement) in clearance. Our results, therefore, highlight the need for further study into the conditions under which impressions of esophageal clearance in the upright position are made during the MBSS.

Our cohort had very mild to no identifiable oropharyngeal swallowing impairments which likely influenced our findings of esophageal clearance. Most participants were classified with MBSImP oral total scores that indicated a mild/functional impairment and all participants had pharyngeal scores that were classified as mild/functional. Therefore, our cohort of participants with relatively “normal” oropharyngeal swallow function may not demonstrate meaningful relationships between oropharyngeal measures and impressions of esophageal clearance (component 17 scores) in our two conditions. Significant findings may be identified in a more heterogeneous sample representing a wider range of swallowing impairments from multiple primary etiologies (eg, stroke, neurodegenerative disease, head and neck cancer).

The evidence for co-occurring esophageal abnormalities identified during MBSSs is mounting.

Reported esophageal abnormality identified during the MBSS ranges from 26% to 100% in the literature.^11,12 In our systematic review, we identified that when esophageal visualization was completed during the MBSS, 48.7% of participants had some type of esophageal abnormality.⁹ Studies that report MBSImP scores demonstrated that populations whose acute impairment is traditionally thought to be for solely for oropharyngeal have evidence for abnormal esophageal clearance (component 17). Our work in stroke identified abnormal esophageal clearance in 57.9% of patients.²⁷ The majority of patients pre- and post-lung transplant have been identified with abnormal esophageal clearance.^45,46 Similarly high prevalence for abnormal esophageal clearance was reported by Fong and colleagues in patients post-nonsurgical nasopharyngeal cancer treatment.⁴⁷ In the current study, abnormal esophageal clearance was identified in both standard MBSImP and experimental conditions (80.6% and 86.1%, respectively). The high proportion of esophageal findings may reflect that many patients referred for an MBSS, particularly outpatients, may have a primary esophageal etiology for their complaints of dysphagia but be referred first for an MBSS, likely due to ordering provider concern for potential aspiration or a lack of awareness in how to stratify risk for oropharyngeal versus esophageal disorders. It should be acknowledged that the participant-reported symptoms in our cohort could indicate a primary esophageal etiology, particularly as most of our cohort had no documented etiology that would predispose them to oropharyngeal dysphagia. Most participants reported dysphagia to solids (55.6%), followed by coughing with eating (44.4%), dysphagia to pills (36.1%), and globus sensation (27.8%). Studies attempting to study patient localization of dysphagia symptoms, specifically globus and a “sticking” sensation, have found poor correlation. Madhavan and colleagues identified esophageal abnormality in 69.5% of their participants presenting with globus sensation.¹⁷ Ortiz and colleagues found that in 90% of their participants with globus had retained contrast in the esophageal body.²⁰ Though when patient symptoms were grouped into above the thyroid notch to below the thyroid notch, there was poor correlation to fluoroscopic findings. However, Ashraf et al⁴⁸ reported that the exact nature of anatomic abnormality or physiologic impairment influenced localization. For example, participants with an obstructive pathology in the proximal esophagus were the most accurate (81.7%) at identifying the level of their dysphagia. Overall, participants were determined to have an accuracy of 48.2% in identifying the level of their dysphagia.

There are many different factors that may influence esophageal visualization during the MBSS including positioning, protocol (eg, order of presentation, types of barium stimuli used, and under what conditions). Deglutitive inhibition, the alteration or cessation of peristalsis with swallows that occur quickly together, is relatively unexplored in visualization protocols and its influence is unknown in our sample owing to not counting the number of swallows in the standard (un-cued) condition. Both of Miles et al’s^6,7 studies on esophageal bolus transit time report a patient directive to swallow a 20 mL bolus “all in one go,” potentially to address deglutitive inhibition. Miles et al⁶ protocol specified a cue of “try hard not to swallow a second time,” and Watts et al¹¹ protocol included a cue to “only swallow one time.” Though cueing was included, the patient’s ability to adhere to the protocol was not recorded. To our knowledge, our study is the first of its kind investigating the potential influence of swallowing only once on impressions of esophageal clearance during the MBSS.

There is limited research that compares esophageal visualization during the MBSS to the standards of dedicated esophageal testing (eg, barium esophagram, high-resolution esophageal manometry). In their study comparing an esophageal screening protocol to a barium esophagram, Allen et al⁵ reported a 62.8% specificity, 100% sensitivity, though both reported 95% confidence intervals had a range greater than 20%. Gullung et al¹⁶ identified abnormal component 17 (esophageal clearance) MBSImP scores in 63.4% of their participants which correlated to a 78% sensitivity for detecting abnormality when compared to HRM-MII. No confidence intervals were reported for reference. Watts et al¹⁰ reported a 100% agreement of abnormality identified during esophageal visualization when compared to dedicated esophageal testing (HRM, timed barium esophagram, esophagogastroduodenoscopy [EGD]), though only for a subset (52.5%) of their participants. More recently, Watts et al¹¹ reported a sensitivity of 83.7% and specificity of 73.7% when their Robust Esophageal Screening Test (REST) was compared against HRM or a timed barium esophagram; Though the 95% confidence intervals reported were greater than 20% sensitivity and greater than 30% for specificity.

While the esophageal visualization portion of the MBSImP is non-diagnostic, it provides relevant information to be correlated clinically to help determine those patients who would benefit from dedicated esophageal testing. It is important to acknowledge that an abnormal esophageal clearance in the upright position may not be indicative of a disorder. Only Gullung et al¹⁶ has compared MBSImP findings against a gold-standard for esophageal assessment (HRM-MII). However, the study did not focus on this finding alone and did not further investigate findings by score, rather, by a dichotomized normal versus abnormal esophageal clearance (component 17) score. It is important to note that the MBSImP differs from other standardized assessments of esophageal visualization in its strict parameters for judging only esophageal clearance, whereas other protocols have been designed as an adjunct to a standard MBSS and is intended to assess esophageal function and/or anatomy.

What can be translated from this work is the nuances of assessing patients with symptoms of dysphagia. Given the interconnections between the oropharynx, esophagus, and the broader respiratory and digestive (aerodigestive) system; a multidisciplinary or transdisciplinary approach is ideal for ensuring proper work-up. Gregor and colleagues recently published their systematic approach to multidisciplinary care (SLP, ENT, GI) for patients with swallowing disorders and highlight the importance of contributions from many different specialties to enhance patient care and outcomes.⁴⁹ Every perspective is critical to acknowledge as each of us view the patient through our own discipline-specific lens.

Future Considerations

Future research into the parameters for judging esophageal clearance during the MBSS should consider patient factors and refine the assessment of swallowing. Standardized cognitive screening tests such as the Mini Mental Status Exam (MMSE)⁵⁰ should be considered in protocols where cognition may influence outcome. The process of counting swallows should be refined, such as by including sEMG which would register submental and laryngeal activity related to oropharyngeal swallowing. Additional metrics such as temporal and kinematic measures would help better describe the impact of different conditions on judgements of esophageal clearance during the MBSS. Future work using simultaneous manometry and fluoroscopy that examines different conditions on esophageal function is planned. Ultimately, our findings compel further research into the conditions in a more rigorous manner.

Limitations

This study has several limitations. First, as a pilot study no threshold was set for participant recruitment, and we only achieved a small sample size for this cohort. We did not address cognition as a potential influence on the participants’ ability to follow directions. The number of swallows in the standard (un-cued) MBSImP condition was not counted and, therefore, we were unable to compare if multiple swallows occurred in the un-cued condition; and if more than one swallow did occur, the time between swallows was not measured.

Conclusion

This study contributes to our knowledge about esophageal visualization and determinations of clearance during the MBSS. This study found that 38.9% of participants had a change in scores when provided a verbal cue to swallow only one time to account for deglutitive inhibition. Most of those with a change in scores demonstrated an increase indicating that impressions of esophageal clearance were more atypical in our experimental condition, which given the sample size and limitations should be interpreted with caution. Our findings highlight the importance of future work investigating the influence of cueing to account for the effect of deglutitive inhibition on impressions of esophageal clearance.

Footnotes

Appendix

Appendix A.

Comparison of Swallowing Impairment and Outcome Measures in Unchanged Versus Changed MBSImP Component 17 (Esophageal Clearance) Scores Under Two Conditions.

Swallowing impairment and outcome measures	Total n = 36 (%)	No change clearance n = 22 n (%)	Change in clearance n = 14 n (%)	P-value*
MBSImP component 1 (lip closure)				0.6287
C1 ≤ 1	32 (88.9)	20 (90.9)	12 (85.1)
C1 ≥ 2	4 (10.8)	2 (9.1)	2 (14.3)
MBSImP component 2 (tongue control during bolus hold)				0.6287
C2 = 0	24 (66.7)	14 (63.6)	10 (71.4)
C2 ≥ 1	12 (33.3)	8 (36.4)	4 (28.6)
MBSImP component 3 (bolus prep/mastication)				0.6549
C3 = 0	25 (73.5)	16 (76.2)	9 (69.2)
C3 ≥ 1	9 (26.5)	5 (23.8)	24(30.8)
MBSImP component 4 (bolus transport/lingual motion)				0.1203
C4 = 0	28 (77.8)	19 (86.4)	9 (64.3)
C4 ≥ 1	8 (22.2)	3 (13.6)	5 (35.7)
MBSImP component 5 (oral residue) to component 17
C5 ≤ 1	17 (47.2)	11 (50)	6 (42.9)	0.6756
C5 ≥ 2	19 (52.8)	11 (50)	8 (57.1)
MBSImP component 6 (initiation of pharyngeal swallow)				0.1161
C6 = 0	4 (11.1)	1 (4.5)	3 (21.4)
C6 ≥ 1	32 (88.9)	21 (95.5)	11 (78.6)
MBSImP component 7 (velar elevation)				—
C7 = 0	35 (100)	21 (100)	14 (100)
C7 ≥ 1	0 (0)	0 (0)	0 (0)
MBSImP component 8 (laryngeal elevation)				0.7662
C8 = 0	24 (68.6)	14 (66.7)	10 (71.4)
C8 ≥ 1	11 (31.4)	7 (33.3)	4 (28.6)
MBSImP component 9 (anterior hyoid excursion)				0.5549
C9 = 0	27 (79.4)	16 (76.2)	11 (84.6)
C9 ≥ 1	7 (20.6)	5 (23.8)	2 (15.4)
MBSImP component 10 (epiglottic movement)				0.3964
C10 = 0	26 (72.2)	17 (77.3)	9 (64.3)
C10 ≥ 1	10 (27.8)	5 (22.7)	5 (35.7)
MBSImP component 11 (laryngeal vestibule closure)				0.8695
C11 = 0	27 (77.1)	16 (76.2)	11 (78.6)
C11 ≥ 1	8 (22.9)	5 (23.8)	3 (21.4)
MBSImP component 12 (pharyngeal stripping wave)				0.0609
C12 = 0	23 (65.7)	17 (77.3)	6 (46.2)
C12 ≥ 1	12 (34.3)	5 (22.7)	7 (53.8)
MBSImP component 13 (pharyngeal contraction)				0.9324
C13 = 0	26 (72.2)	16 (72.7)	10 (71.4)
C13 ≥ 1	10 (27.8)	6 (27.2)	4 (28.6)
MBSImP component 14 (pharyngoesophageal segment opening)				0.7242
C14 = 0	17 (50)	11 (52.4)	6 (46.2)
C14 ≥ 1	17 (50)	10 (47.6)	7 (53.8)
MBSImP component 15 (tongue base retraction)				0.0738
C15 ≤ 1	17 (47.2)	13 (59.1)	4 (28.6)
C15 ≥ 1	19 (52.8)	9 (40.9)	10 (71.4)
MBSImP component 16 (pharyngeal residue)				0.3111
C16 ≤ 1	14 (38.8)	10 (45.5)	4 (28.6)
C16 ≥ 1	22 (61.1)	12 (54.5)	10 (71.4)
Penetration-aspiration scale (PAS) score				1.000
PAS ≤ 3	32 (88.9)	19 (86.4)	13 (92.9)
PAS ≥ 4	4 (11.1)	3 (13.6)	1 (7.1)
Presence of aspiration	4 (11.1)	3 (13.6)	1 (7.1)	0.5456
Functional oral intake scale (FOIS) score				0.4185
FOIS 6-7	35 (97.2)	21 (95.5)	14 (100)
FOIS 5-3	1 (2.8)	1 (4.5)	0 (0)
FOIS 1-2	0 (0)	0 (0)	0 (0)
International dysphagia diet (IDDSI) liquid score				—
IDDSI liquids = 0	34 (100)	21 (100)	13 (100)
IDDSI liquids 2-3	0 (0)	0 (0)	0 (0)
International dysphagia diet (IDDSI) solid score
IDDSI solids = 7	33 (91.7)	21 (95.5)	12 (85.7)	0.3026
IDDSI solids 4-6	3 (8.33)	1 (4.5)	2 (14.3)

Chi square or Fisher’s exact tests, P-value < 0.05.

Acknowledgements

The authors would like to acknowledge the MUSC Health and Rehabilitation Sciences department for PhD funding. A special thanks to the Speech-Language Pathologists who contributed to this study: Melissa Cooke, Kate Davidson, Olivia Bupp, and Mary-Chase Godwin. Further, the authors would like to acknowledge the MUSC Speech Language Pathology department, MUSC Laryngology department, and MUSC Gastroenterology Manometry Lab for their immense support of this work.

Author Contributions

Study design, data acquisition, and drafting of the original manuscript were performed by first author, E.L.R. Both E.L.R. and A.N.S. completed data analysis and contributed to the interpretation of this work. A.K.O and senior author, H.S.B., contributed substantially to study conceptualization and edition of earlier versions of the manuscript. All authors read and approved of the final manuscript.

Use of Artificial Intelligence

No artificial intelligence (AI) was used in the preparation of this manuscript.

Data Availability

Reasonable requests for data can be made to corresponding author.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Funding was provided for first-author’s doctoral studies through the Health and Rehabilitation Sciences Department in the Collage of Health Professions at the Medical University of South Carolina.

Ethical Approval

All ethical standards for research were maintained throughout this study. Written informed consent was obtained from all participants. Approval from the Medical University of South Carolina’s Institutional Review Board was received.

ORCID iD

Erin L. Reedy

References

Martin-Harris

Canon

Bonilha

Murray

Davidson

Lefton-Greif

MA.

Best practices in modified barium swallow studies. Am J Speech Lang Pathol. 2020;29(2S):1078-1093. doi:10.1044/2020_AJSLP-19-00189

Jones

Donner

Rubesin

Ravich

Hendrix

TR.

Pharyngeal findings in 21 patients with achalasia of the esophagus. Dysphagia. 1987;2(2):87-92. doi:10.1007/BF02408139

Jones

Ravich

Donner

Kramer

Hendrix

TR.

Pharyngoesophageal interrelationships: observations and working concepts. Gastrointest Radiol. 1985;10(3):225-233. doi:10.1007/BF01893105

Triadafilopoulos

Hallstone

Nelson-Abbott

Bedinger

Oropharyngeal and esophageal interrelationships in patients with nonobstructive dysphagia. Dig Dis Sci. 1992;37(4):551-557. doi:10.1007/BF01307579

Allen

White

Leonard

Belafsky

PC.

Comparison of esophageal screen findings on videofluoroscopy with full esophagram results. Head Neck. 2012;34(2):264-269. doi:10.1002/hed.21727

Miles

Bennett

Allen

Esophageal transit times vary with underlying comorbid disease. Otolaryngol Head Neck Surg. 2019;161(5):829-834. doi:10.1177/0194599819874342

Miles

Clark

Jardine

Allen

Esophageal swallowing timing measures in healthy adults during videofluoroscopy. Ann Otol Rhinol Laryngol. 2016;125(9):764-769. doi:10.1177/0003489416653410

Miles

McMillan

Ward

Allen

Esophageal visualization as an adjunct to the videofluoroscopic study of swallowing. Otolaryngol Head Neck Surg. 2015;152(3):488-493. doi:10.1177/0194599814565599

Reedy

Herbert

Bonilha

HS.

Visualizing the esophagus during modified barium swallow studies: a systematic review. Am J Speech Lang Pathol. 2021;30(2):761-771. doi:10.1044/2020_AJSLP-20-00255

10.

Watts

Gaziano

Jacobs

Richter

Improving the diagnostic capability of the modified barium swallow study through standardization of an esophageal sweep protocol. Dysphagia. 2019;34(1):34-42. doi:10.1007/s00455-018-09966-5

11.

Watts

Gaziano

Kumar

Richter

Diagnostic accuracy of an esophageal screening protocol interpreted by the speech-language pathologist. Dysphagia. 2021;36(6):1063-1071. doi:10.1007/s00455-020-10239-3

12.

Belafsky

Rees

Rodriguez

Pryor

Katz

PO.

Esophagopharyngeal reflux. Otolaryngol Head Neck Surg. 2008;138(1):57-61. doi:10.1016/j.otohns.2007.09.006

13.

Borgström

Birch-Iensen

Ekberg

Radiology of the pharynx and oesophagus in young adults. Br J Radiol. 1988;61(730):909-913. doi:10.1259/0007-1285-61-730-909

14.

Ekberg

Feinberg

MJ.

Altered swallowing function in elderly patients without dysphagia: radiologic findings in 56 cases. AJR Am J Roentgenol. 1991;156(6):1181-1184. doi:10.2214/ajr.156.6.2028863

15.

Feinberg

Ekberg

Videofluoroscopy in elderly patients with aspiration: importance of evaluating both oral and pharyngeal stages of deglutition. AJR Am J Roentgenol. 1991;156(2):293-296. doi:10.2214/ajr.156.2.1898801

16.

Gullung

Hill

Castell

Martin-Harris

Oropharyngeal and esophageal swallowing impairments: their association and the predictive value of the modified barium swallow impairment profile and combined multichannel intraluminal impedance-esophageal manometry. Ann Otol Rhinol Laryngol. 2012;121(11):738-745. doi:10.1177/000348941212101107

17.

Madhavan

Carnaby

Crary

MA.

‘Food sticking in my throat’: videofluoroscopic evaluation of a common symptom. Dysphagia. 2015;30(3):343-348. doi:10.1007/s00455-015-9605-6

18.

Martin-Harris

Brodsky

Michel

, et al. MBS measurement tool for swallow impairment—MBSImp: establishing a standard. Dysphagia. 2008;23(4):392-405. doi:10.1007/s00455-008-9185-9

19.

Miles

Inter-rater reliability for speech-language therapists’ judgement of oesophageal abnormality during oesophageal visualization. Int J Lang Commun Disord. 2017;52(4):450-455. doi:10.1111/1460-6984.12283

20.

Ortiz

Lawton

Rives

Gutierrez

Dion

GR.

Correlating videofluoroscopic swallow study findings with subjective globus location. Laryngoscope. 2019;129(2):335-338. doi:10.1002/lary.27536

21.

Scharitzer

Lenglinger

Schima

Weber

Ringhofer

Pokieser

Comparison of videofluoroscopy and impedance planimetry for the evaluation of oesophageal stenosis: a retrospective study. Eur Radiol. 2017;27(4):1760-1767. doi:10.1007/s00330-016-4516-y

22.

American Speech-Language Hearing Association. Knowledge and Skills Needed by Speech-Language Pathologists Performing Videofluoroscopic Swallowing Studies. New York, NY: ASHA, 2004. www.asha.org/policy

23.

American Speech-Language Hearing Association. Preferred Practice Patterns for the Profession of Speech-Language Pathology. New York, NY: ASHA, 2004. www.asha.org/policy

24.

American Speech-Language-Hearing Association. Guidelines for speech-language pathologists performing videofluoroscopic swallowing studies. ASHA Suppl. 2004;24:77-92.

25.

American College of Radiology. ACR-SPR Practice Parameter for the Performance of the Modified Barium Swallow. Richmond, VA: ACR, 2023. https://www.acr.org/-/media/ACR/Files/Practice-Parameters/Modified-Ba-Swallow.pdf

26.

Dhar

Nativ-Zeltzer

Starmer

, et al. The American Broncho-Esophagological Association position statement on swallowing fluoroscopy. Laryngoscope. 2023;133(2):255-268. doi:10.1002/lary.30177

27.

Reedy

Simpson

O’Rourke

Bonilha

HS.

Abnormal esophageal clearance identified during modified barium swallow study in an acute poststroke cohort. Am J Speech Lang Pathol. 2022;31(6):2643-2662. doi:10.1044/2022_AJSLP-22-00029

28.

Martin-Harris

Standardized Training in Swallow Physiology – Evidence-Based Assessment Using the Modified Barium Swallow Impairment Profile (MBSImP) Approach. Gaylord, MI: Northern Speech Services, 2015.

29.

Hightower

NC.

Esophageal motility in health and disease. Dis Chest. 1955;28(2):150-169. doi:10.1378/chest.28.2.150

30.

Tutuian

Jalil

Katz

Castell

DO.

Effect of interval between swallows on oesophageal pressures and bolus movement in normal subjects—studies with combined multichannel intraluminal impedance and oesophageal manometry. Neurogastroenterol Motil. 2004;16(1):23-29. doi:10.1046/j.1365-2982.2003.00460.x

31.

Sifrim

Jafari

Deglutitive inhibition, latency between swallow and esophageal contractions and primary esophageal motor disorders. J Neurogastroenterol Motil. 2012;18(1):6-12. doi:10.5056/jnm.2012.18.1.6

32.

Goyal

Chaudhury

Physiology of normal esophageal motility. J Clin Gastroenterol. 2008;42(5):610-619. doi:10.1097/MCG.0b013e31816b444d

33.

Meyer

Gerhardt

Castell

DO.

Human esophageal response to rapid swallowing: muscle refractory period or neural inhibition?

Am J Physiol. 1981;241(2):G129-G136. doi:10.1152/ajpgi.1981.241.2.G129

34.

Pandolfino

Shi

Zhang

Kahrilas

PJ.

Absence of a deglutitive inhibition equivalent with secondary peristalsis. Am J Physiol Gastrointest Liver Physiol. 2005;288(4):G671-G676. doi:10.1152/ajpgi.00388.2004

35.

Shi

Pandolfino

Zhang

Hirano

Joehl

Kahrilas

PJ.

Deglutitive inhibition affects both esophageal peristaltic amplitude and shortening. Am J Physiol Gastrointest Liver Physiol. 2003;284(4):G575-G582. doi:10.1152/ajpgi.00311.2002

36.

Yadlapati

Kahrilas

Fox

, et al. Esophageal motility disorders on high-resolution manometry: Chicago classification version 4.0^© [published correction appears in Neurogastroenterol Motil. 2024;36(2):e14179. doi:10.1111/nmo.14179]. Neurogastroenterol Motil. 2021;33(1):e14058. doi:10.1111/nmo.14058

37.

Fox

Sweis

Yadlapati

, et al. Chicago classification version 4.0^© technical review: update on standard high-resolution manometry protocol for the assessment of esophageal motility. Neurogastroenterol Motil. 2021;33(4):e14120. doi:10.1111/nmo.14120

38.

Hollenstein

Thwaites

Bütikofer

, et al. Pharyngeal swallowing and oesophageal motility during a solid meal test: a prospective study in healthy volunteers and patients with major motility disorders. Lancet Gastroenterol Hepatol. 2017;2(9):644-653. doi:10.1016/S2468-1253(17)30151-6

39.

Donohue

Robison

Steele

Wymer

Plowman

EK.

Profiling number of swallows per bolus and residue in individuals with amyotrophic lateral sclerosis. J Speech Lang Hear Res. 2023;66(10):3763-3772. doi:10.1044/2023_JSLHR-23-00209

40.

Jardine

Miles

Allen

A systematic review of physiological changes in swallowing in the oldest old. Dysphagia. 2020;35(3):509-532. doi:10.1007/s00455-019-10056-3

41.

Steele

Peladeau-Pigeon

Barrett

Wolkin

TS.

The risk of penetration-aspiration related to residue in the pharynx. Am J Speech Lang Pathol, 2020;29(3):1608-1617. doi:10.1044/2020_AJSLP-20-00042

42.

Steele

Peladeau-Pigeon

Nagy

Waito

AA.

Measurement of pharyngeal residue from lateral view videofluoroscopic images. J Speech Lang Hear Res. 2020;63(5):1404-1415. doi:10.1044/2020_JSLHR-19-00314

43.

Bonilha

Blair

Carnes

, et al. Preliminary investigation of the effect of pulse rate on judgments of swallowing impairment and treatment recommendations. Dysphagia. 2013;28(4):528-538. doi:10.1007/s00455-013-9463-z

44.

Bonilha

Reedy

Wilmskoetter

Nietert

Martin-Harris

Impact of reducing fluoroscopy pulse rate on adult modified barium swallow studies. Dysphagia. 2024;39(4):632-641. doi:10.1007/s00455-023-10643-5

45.

Graham

Reedy

Lee

, et al. Respiratory-swallow patterning and oropharyngeal swallowing impairment in patients undergoing evaluation for lung transplant. Neurogastroenterol Motil. 2024;36(11):e14912. doi:10.1111/nmo.14912

46.

Reedy

Simpson

O’Rourke

Bonilha

HS.

Characterizing swallowing impairment in a post-lung transplant population. Am J Speech Lang Pathol. 2023;32(3):1236-1251. doi:10.1044/2023_AJSLP-22-00266

47.

Fong

Rumbach

Ward

EC.

Prevalence and associated impacts of cervical esophageal clearance issues post chemoradiotherapy for nasopharyngeal carcinoma (NPC). Dysphagia. 2020;35(1):99-109. doi:10.1007/s00455-019-10007-y

48.

Ashraf

Palmer

Dalton

, et al. Can patients determine the level of their dysphagia? World J Gastroenterol. 2017;23(6):1038-1043. doi:10.3748/wjg.v23.i6.1038

49.

Gregor

Lott

Kahn

Comprehensive multidisciplinary evaluation of dysphagia. Clin Gastroenterol Hepatol. 2025;23(5):707-710. doi:10.1016/j.cgh.2024.12.002

50.

Folstein

McHugh

PR.

“Mini-mental state.” A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12(3):189-198. doi:10.1016/0022-3956(75)90026-6