INTRODUCTION
Dysphagia is clinically important in patients diagnosed with lateral medullary syndrome (LMS), because it is associated with several complications, including aspiration pneumonitis, malnutrition, and increased mortality, as well as decreased quality of life.1) During normal swallowing, the pharynx contracts, the upper esophageal sphincter (UES) opens, and the bolus passes from the pharynx to the upper esophagus. In patients with LMS and bulbar dysphagia, lesions affecting the nucleus ambiguus result in pharyngeal contraction weakness and impaired UES relaxation.2,3) Furthermore, the UES closes strongly during swallowing in patients with severe dysphagia.4) A bolus residue in the pyriform sinus after swallowing can lead to aspiration. Balloon dilatation,5) rehabilitation training including Shaker exercise,6) forehead exercise for suprahyoid muscles,7) botulinum toxin type A injection (not covered by insurance in Japan),8) and cricopharyngeal myotomy9) have been beneficial for patients with poor or absent UES relaxation.
Vacuum swallowing is a unique swallowing method that improves pharyngeal bolus passage by creating negative intraesophageal pressure in patients with dysphagia caused by LMS and neuromuscular diseases.1,10,11,12,13) Videofluoroscopic examination of swallowing (VF) revealed that a bolus is sucked from the pharynx into the esophagus because of a voluntarily created pressure gradient despite extremely weak pharyngeal contraction.10,13) The negative pressure in the esophagus during swallowing is created by the voluntary contraction of inspiratory muscles. Vacuum swallowing is an alternative maneuver for patients with weak pharyngeal contractility and impaired UES opening. Furthermore, normal participants can create a strong negative pressure in the esophagus during swallowing.14,15) To enable vacuum swallowing, it is important to provide instructions on how to generate negative pressure in the thoracic cavity and achieve the optimal inspiratory effort and swallowing time.15)
High-resolution manometry (HRM) has been used to evaluate swallowing function.16,17) A specific pattern of esophageal pressure characteristics has been observed during vacuum swallowing.10,12,13,14,15) HRM revealed that strong negative pressure was generated in the esophagus during vacuum swallowing, and the lower esophageal sphincter (LES) muscle zone had a forceful constriction. The increase in LES pressure was reflected by the contraction of the diaphragm, which is one of the main inspiratory muscles. Furthermore, the sternocleidomastoid muscle and clavicle are prominent during vacuum swallowing, reflecting negative pressure in the thoracic cavity.10,14,15)
We previously reported that patients with dysphagia caused by LMS independently acquired the technique of vacuum swallowing.10,12) The first reported patient with dysphagia caused by LMS was able to rapidly resume oral intake by spontaneously mastering vacuum swallowing.10) Furthermore, normal individuals and a patient with spinal muscular atrophy were able to master this swallowing technique with instructions.14,15) However, it remains unclear whether this swallowing method can be consistently reproduced and mastered through instructional training in other patients with dysphagia caused by LMS and effectively taught for therapeutic purposes.10)
If patients with dysphagia caused by LMS can reproduce and master vacuum swallowing through instruction, this technique could serve as a valuable alternative swallowing method. However, the risk of bolus aspiration should be evaluated because of the inspiratory effort involved while swallowing. We previously reported that expiration before and after vacuum swallowing is crucial to prevent aspiration of hypopharyngeal residues, as demonstrated using a swallowing and breathing monitoring system (SBMS).15)
In this study, we provided instructions on vacuum swallowing to two patients with dysphagia and poor pharyngeal passage because of LMS, the same pathophysiology reported previously.10) We aimed to (1) determine whether patients with dysphagia could reproduce and master vacuum swallowing through instructional training, as verified by VF and HRM and (2) demonstrate the safety of vacuum swallowing using an SBMS.18,19)
CASES
ParticipantsTwo patients with dysphagia caused by LMS, who had undergone swallowing rehabilitation but exhibited insufficient pharyngeal passage and required an alternative method, were included in this study after receiving education concerning vacuum swallowing. This study was conducted in accordance with the principles embodied in the 1975 Declaration of Helsinki, as revised in 1983, and was approved by the Ethics Committee of the Hamamatsu City Rehabilitation Hospital (#21-67). Written informed consent was obtained from both patients.
Patient 1A 41‐year‐old man presented with left-side LMS caused by infarction. His neurological deficits were mostly reversed, except for severe dysphagia. The patient exhibited no cognitive impairments, and his respiratory condition remained stable. The patient underwent percutaneous endoscopic gastrostomy (PEG). He exhibited severe dysphagia, which was classified as level 2 on the Food Intake LEVEL Scale (FILS) (level 2: swallowing training is performed without using food).18) His Barthel Index score was 90. At 15 months after dysphagia onset, he was admitted to our rehabilitation hospital for treatment of severe dysphagia. VF was conducted shortly after admission and revealed weak pharyngeal contractility and impaired UES relaxation. Even sliced jelly with low adhesiveness could not pass through the pharynx and instead pooled in the pyriform sinus despite swallowing rehabilitation with balloon catheter dilatation, Shaker exercise, forehead exercise for suprahyoid muscles, respiratory training, and direct feeding therapy. The passage of thickened liquid through the pharynx exhibited complications. Conventional swallowing rehabilitation showed limited improvement in bolus passage through the pharynx. Vacuum swallowing was introduced to facilitate the clearance of residues in the pyriform sinus into the esophagus.
Patient 2A 44-year-old man presented with right-side LMS secondary to dissection of the right vertebral artery. The patient exhibited severe dysphagia and was fed through a feeding tube. He had no cognitive impairments, and his respiratory status was stable. He had mild sensory impairments in the left upper and lower limbs but showed minimal ataxia. The patient was able to walk independently (with a full Functional Independence Measure score). One month after onset, he was transferred to our rehabilitation hospital for swallowing rehabilitation. The initial VF, performed on the day following his transfer, revealed weak pharyngeal contraction and impaired opening of the UES. The patient underwent dysphagia rehabilitation including balloon catheter dilatation, Shaker exercise, forehead exercise for suprahyoid muscles, and respiratory training. Three months after onset, his swallowing function improved to FILS level 8 (patient can eat three meals per day by avoiding food that is difficult to swallow). Nonetheless, VF revealed that the bolus did not pass completely through the pharynx and remained partially in the pyriform sinus after swallowing. Swallowing maneuvers, including dry swallowing, head rotation, and alternating swallowing, were performed to remove pyriform sinus residue; however, the effectiveness of these measures remained inadequate.
Intervention and ProcedureA physiatrist and a speech–language pathologist provided instructions on the need for and the method of vacuum swallowing to the two patients for 20–30 min each day over the course of approximately 2–3 days. VF was conducted once after instructing patients regarding vacuum swallowing to assess whether they were able to successfully perform the maneuver. It was also used to provide visual feedback. As described in previous reports,14,15) the instructor explained the indications and the mechanism of vacuum swallowing.
First, the patients were instructed to create strong negative pressure in the thoracic cavity by inhaling with the glottis closed (inspiratory effort). The instructor confirmed that, when successfully performed, the contraction of the inspiratory muscles generates strong negative pressure in the thoracic cavity, accompanied by anterior cervical depression, as observed in previous studies. Given that the prominence of the sternocleidomastoid muscle and clavicle reflects the negative pressure in the thoracic cavity, the patients were able to observe these cervical signs using a mirror (Fig. 1).
Next, the patients practiced coordinating the timing of swallowing and inspiratory effort. They were instructed to exhale and hold their breath before attempting vacuum swallowing. Immediately after the larynx was elevated (with the glottis closed) during swallowing, they attempted the inspiratory effort, as described above. The patients were also educated on strategies to prevent aspiration during vacuum swallowing. They were instructed to hold their breath before performing vacuum swallowing and to exhale afterward.
The patients practiced vacuum swallowing for approximately 1–2 weeks to acquire the technique. The training was provided as part of swallowing rehabilitation by speech–language pathologists. Each rehabilitation session lasted approximately 40 min and was typically conducted five times per week. During these sessions, the patients used a mirror to observe the depression in the neck, which reflects the generation of negative intrathoracic pressure.15) This visual feedback helped them confirm the generation of negative pressure in the thoracic cavity. In addition to therapist-led training, the patients also performed self-training using similar visual feedback with a mirror.
Videofluoroscopic examination of swallowingVF of the pharyngeal stage was performed to evaluate the improvement in pharyngeal bolus passage through vacuum swallowing. Pharyngeal bolus passage was compared with that during non-vacuum swallowing. VF images in the lateral or frontal view were captured, and the data were recorded using a video recorder. The capture rate was 30 frames/s. VF was performed using the following boluses: Patient 1 was evaluated using sliced jelly, Patient 2 was evaluated using extremely thickened liquid. The boluses were administered by the examiner using a spoon (approximately 2–3 mL). During VF examination, visual feedback was obtained with the VF images to confirm whether the bolus passed through the pharynx during vacuum swallowing.
Manometric StudyA solid-state HRM catheter (Unisensor, Attikon, Switzerland) with an outer diameter of 4.2 mm and 36 circumferential pressure sensors spaced 1 cm apart was used for the measurement. Before starting the examination, the catheter was lubricated with 2% lidocaine jelly to ease the passage through the nasal cavity. The manometric catheter was positioned to record movement from the velopharynx to the UES. Then, the HRM catheter was fixed to the nasal wing using tape. The catheter was calibrated and zeroed to atmospheric pressure. After the pharyngeal manometric study, the device was inserted until at least a few sensors were in the stomach. The catheter was secured by taping it to the nose, and the pressure was recorded from the hypopharynx to the stomach.
Pressure and timing data were extracted using ManoScan software (Star Medical, Tokyo, Japan). The patients performed non-vacuum and vacuum swallowing, according to the instructions. Successful vacuum swallowing was accomplished when the HRM topography showed the simultaneous generation of strong negative esophageal pressure with swallowing. In Patient 1, the pharyngeal parameters of HRM were detected for three vacuum swallows with sliced jelly, and esophageal parameters were noted for three vacuum swallows with dry swallows to avoid aspiration. In Patient 2, all HRM parameters were assessed for three swallows with sliced jelly. The vacuum swallows of both patients were compared with three non-vacuum swallows. Several parameters, such as the pharyngeal maximum pressure (Pmax), UES relaxation duration, UES nadir pressure, esophageal minimum pressure (Pmin), and LES Pmax, were recorded during non-vacuum and vacuum swallowing (Fig. 2). The mean and standard deviation (SD) values of each HRM parameter were calculated.
A non-invasive SBMS that records respiratory flow, laryngeal motion, and swallowing sounds was used.15,19,20) A prototype SBMS (iSwallow monitor®, EuSense Medical, Japan) was used in this study. It consisted of a nasal cannula-type flow sensor, a film-type piezoelectric sensor, and signal processing units. Swallows were detected by laryngeal motion and the absence of respiratory flow. Based on data for respiratory flow, laryngeal motion, and sound, the wide dynamic range (0–4 kHz) of the piezoelectric sensor ensured the capture of both laryngeal motion and sound. Swallowing periods were extracted semi-automatically with an algorithm using the respiratory flow, swallowing sound, and laryngeal motion. Breathing–swallowing coordination and apnea duration during swallowing were evaluated using a series of respiratory flow, laryngeal motion, and sound data (Fig. 3). The expiration–swallow and swallow–expiration (E-SW and SW-E, respectively) patterns are considered typical swallowing–breathing coordination patterns. Although inspiration–swallow and swallow–inspiration (I-SW and SW-I, respectively) patterns are unusual, they may occur even in healthy participants. The occurrence of these two unusual patterns (I-SW and/or SW-I) may indicate breathing–swallowing discoordination.18,19) The occurrence of I-SW and SW-I patterns tends to rise with age in patients with stroke, Parkinson’s disease, chronic obstructive pulmonary disease, and after treatment in head-neck cancer patients.15) Although these patterns are found even in healthy individuals, identifying a high I-SW/SW-I ratio and implementing suitable interventions for addressing it may help prevent aspiration pneumonia.
The evaluation of Patient 1 used dry swallowing to prevent aspiration because of severe dysphagia. Five dry swallows were evaluated during both non-vacuum and vacuum swallowing. Patient 2 swallowed approximately 3 mL of thickened liquid three times each during non-vacuum and vacuum swallowing.
Statistical AnalysisThe mean results for non-vacuum and vacuum swallowing were compared using an unpaired t-test. The critical value for rejecting the null hypothesis was set at P <0.05. All statistical analysis was performed using SPSS Statistics software version 22.0 (IBM, Tokyo, Japan).
This article was previously posted to the Research Square preprint server (https://doi.org/10.21203/rs.3.rs-2272803/v1) on 18 Nov, 2022.21) This work is licensed under a CC BY 4.0 License.
ResultsVideofluoroscopic examination of swallowingIn Patient 1, the bolus remained in the pyriform sinus and did not pass through the pharynx after several non-vacuum swallows. With vacuum swallowing, the timing of respiratory muscle contraction and swallowing was synchronized with visual feedback, and the bolus flowed into the upper esophagus (Fig. 4A).
In Patient 2, the bolus passed through the pharynx upon UES relaxation; however, part of the bolus remained in the pyriform sinus. Pharyngeal residues in the pyriform sinus were not cleared during non-vacuum swallowing. Conversely, the bolus flowed into the upper esophagus with vacuum swallowing (Fig. 4B). In both patients, no aspiration was observed during non-vacuum or vacuum swallowing.
Manometric MeasurementsA summary of the data obtained during non-vacuum and vacuum swallowing using HRM is presented in Table 1. The mean and SD values of each HRM parameter were calculated.
Table 1. Comparison of non-vacuum and vacuum swallowing by high-resolution manometry
| Measurement | Patient 1 | P value | Patient 2 | P value |
| Non-vacuum swallowing | Vacuum
swallowing | Non-vacuum swallowing | Vacuum
swallowing |
| Pharynx | | | | | | |
| Pharyngeal Pmax (mmHg) | 55.2 ± 17.2 | 36.9 ± 21.5 | 0.316 | 102.6 ± 9.1 | 95.4 ± 0.5 | 0.238 |
| UES nadir pressure (mmHg) | −1.1 ± 1.2 | −15.5 ± 4.4 | 0.006 | 12.0 ± 1.2 | −34.5 ± 4.5 | 0.001 |
| UES relaxation duration (ms) | 616.7 ± 76.4 | 733.3 ± 232.9 | 0.456 | 933.3 ± 28.9 | 926.7 ± 25.2 | 0.778 |
| Esophagus | | | | | | |
| Esophageal Pmin (mmHg) | −6.4 ± 1.4 | −27.9 ± 0.7 | <0.001 | −24.3 ± 3.1 | −72.1 ± 8.0 | <0.001 |
| LES Pmax (mmHg) | 42.7 ± 3.6 | 54.4 ± 11.1 | 0.157 | 42.4 ± 11.0 | 290.0 ± 18.2 | <0.001 |
LES, lower esophageal sphincter; Pmax, maximum pressure; Pmin, minimum pressure; UES, upper esophageal sphincter.
The UES nadir pressure and esophageal Pmin were significantly lower during vacuum swallowing than during non-vacuum swallowing in both patients. The LES Pmax was significantly higher in Patient 2. In Patient 1, no statistically significant difference was observed in the LES Pmax between vacuum and non-vacuum swallowing.
SBMS and AnalysisA summary of the data obtained during thickened liquid swallowing using SBMS is presented in Table 2. In Patient 1, I-SW patterns were not observed. Two out of the five vacuum swallows (40%) showed SW-I patterns; however, choking caused by saliva aspiration was not observed. In Patient 2, I-SW and SW-I patterns were not observed. These two patients experienced deglutition apnea during non-vacuum and vacuum swallowing.
Table 2. Comparison of normal and vacuum swallowing using swallowing and breathing monitoring system
| Breathing pattern | Patient 1 | Patient 2 |
Non-vacuum
swallowing | Vacuum
swallowing | Non-vacuum
swallowing | Vacuum
swallowing |
| SW-I | 0% | 0% | 0% | 0% |
| I-SW | 0% | 40% | 0% | 0% |
| Breathing during swallowing | Apnea | Apnea | Apnea | Apnea |
SW-I, swallowing immediately followed by inspiration; I-SW, swallowing during inspiration.
The vacuum swallowing method was introduced during swallowing rehabilitation to improve bolus passage through the pharynx. This new swallowing maneuver improved the patient’s motivation for oral intake training. For the approximate 1-month period prior to discharge, the patient underwent feeding training with vacuum swallowing during swallowing rehabilitation conducted by a speech–language pathologist, which was provided five times a week for 40 min per session. The FILS score improved to level 3 (swallowing training is performed using a small quantity of food). On day 42 after admission, the patient was discharged. He continued swallowing rehabilitation, including balloon dilatation therapy and nutritional management. He was able to maintain oral intake using vacuum swallowing at an enjoyment level. One year later, the patient was able to sustain oral intake by combining conventional and vacuum swallowing. He continued oral intake, performing vacuum swallowing as needed during meals to clear any residue in the pyriform sinus. The FILS score improved to level 5 (easy-to-swallow food is orally ingested in one to two meals, but alternative nutrition is also given).
Clinical Course after Acquisition of Vacuum Swallowing: Patient 2The patient occasionally performed vacuum swallowing during meals when feeling a sensation of pharyngeal residue despite employing other maneuvers to clear pharyngeal residues in the pyriform sinus, such as cyclic ingestion with thickened liquid and head rotation. He continued swallowing rehabilitation, and his swallowing function gradually improved. Consequently, the frequency of vacuum swallowing gradually decreased with the improvement in his swallowing function. Approximately 4 months after the onset of stroke, he was able to ingest food orally without vacuum swallowing. The FILS score improved to level 9 (no dietary restriction, the patient ingests three meals orally, but medical considerations are given).
DISCUSSION
To the best of our knowledge, this is the first report to confirm that patients with dysphagia caused by LMS can reproduce vacuum swallowing with instructional training. Furthermore, the safety of vacuum swallowing was demonstrated using an SBMS by assessing the risk of aspiration associated with the technique, as described in our previous report.15)
This study had two major findings. First, patients with dysphagia caused by LMS were able to master vacuum swallowing with instructional training, generating negative pressure in the esophagus. The two patients could improve pharyngeal bolus passage during vacuum swallowing. This swallowing method may be an effective maneuver to clear pharyngeal residues from the pyriform sinus. It was considered unlikely to be suitable for clearing residues in the vallecular. In a previously reported patient who acquired vacuum swallowing spontaneously, the bolus rapidly flowed from the pharynx into the esophagus. However, when providing instructions to patients, it is recommended that clinicians focus on residue removal from the pyriform sinus to reduce the risk of aspiration. A better indication for vacuum swallowing is bulbar dysphagia with weakened pharyngeal contractility and impaired UES dysfunction, as observed in the aforementioned patients. Apart from the acquisition of LMS, there is a single case report of spinal muscular atrophy acquiring vacuum swallowing; however, further investigation is needed to determine whether it can be adapted in patients with other conditions, such as neuromuscular diseases or head and neck cancer. Even if UES function is severely impaired, creating negative pressure in the esophagus during swallowing may be the driving force behind the influx of the bolus from the pharynx into the esophagus. Vacuum swallowing, as demonstrated in Patient 1, could serve as a trigger for resuming oral intake in patients with severe dysphagia in the chronic phase of LMS. For Patient 1, who had severe dysphagia, the acquisition of the novel swallowing maneuver contributed toward improving his motivation for feeding training. It is essential that conventional swallowing rehabilitation is carried out properly when introducing vacuum swallowing.
Second, the previously reported teaching method of vacuum swallowing was shown to be useful for patients with dysphagia caused by LMS. A combination of ideal timing for swallowing and inspiratory effort was needed to create negative pressure in the esophagus. In the HRM findings, the creation of strong negative pressure in the esophagus and LES contraction during vacuum swallowing were similar to a previously reported case, as shown in Fig. 2. Obstruction of the airway, which is caused by a closed glottis, contracted pharynx, and attachment of the tongue to the palate during swallowing, contributes to creating a strong negative pressure in the thoracic cavity through inspiratory effort. Intrathoracic pressure may decrease, ranging from −50 to −100 cmH2O, when inspiration is attempted against a closed glottis.22) Changes in respiratory function, such as a decrease in vital capacity, unstable respiratory conditions, or respiratory diseases, may make inspiratory effort difficult and affect the formation of negative intrathoracic pressure. Further research is needed to investigate the potential impact of respiratory function on vacuum swallowing.
Notably, this study clarified the relationship between the respiratory pattern and vacuum swallowing, demonstrated the safety and mechanism of vacuum swallowing using the SBMS, and contributed to the establishment of safe practices and effective instructional methods. As in the previous study, respiratory patterns both preceding and following vacuum swallowing play a crucial role in protecting the airway.15) Furthermore, exhalation before and after vacuum swallowing is important to minimize the risk of aspirating hypopharyngeal residues. I-SW and SW-I patterns should be avoided to prevent aspiration of the hypopharyngeal residues. In this study, patients were advised to exhale prior to vacuum swallowing. They exhibited a minimal risk of aspiration from inspiration. The SW-I pattern was observed in Patient 1. VF revealed no aspiration during vacuum swallowing in these patients. However, it is important to teach the expiration–vacuum swallowing–expiration pattern to protect the airway, which is typically observed in healthy individuals before and after swallowing. In particular, exhalation after vacuum swallowing is important to prevent aspiration. Supraglottic swallowing protects the airway from bolus aspiration by closing the glottis before swallowing.23) Vacuum swallowing after holding one’s breath during expiration may be helpful in preventing respiratory complications.15) Additionally, deglutition apnea was observed in all vacuum swallowing episodes in both patients in the SBMS study. This demonstrated that the bolus did not flow into the airway because of the inspiratory effort during vacuum swallowing, as in the previous report.14,15)
Establishing effective instructional strategies to support patients in acquiring vacuum swallowing is crucial. As reported in a previous study,15) visual feedback provided during VF helps patients synchronize the timing of swallowing and inspiratory effort. Videoendoscopic examination of swallowing and VF would be valuable for confirming whether vacuum swallowing improves pharyngeal bolus passage, and the topography of HRM could also offer useful visual feedback. The Mendelsohn maneuver, which involves holding the tongue forcefully and maintaining laryngeal elevation during swallowing, might be effective for teaching vacuum swallowing in a clear and safe manner.24,25) Combining the prolonged laryngeal elevation of the Mendelsohn maneuver with inspiratory effort could be recommended as an easily understandable instructional approach. However, appropriate cognitive function is essential to grasp the instructions for vacuum swallowing. Although the motor dysfunction of the present patients was mild, vacuum swallowing could be acquired even in cases with severe motor impairment. Further studies are required to validate this point.
This study had several limitations. First, only two patients were included, which limits the generalizability of the findings. The indications for vacuum swallowing are: 1) dysphagia with a bulbar palsy pattern characterized by weak pharyngeal contraction and impaired UES opening, and 2) sufficient cognitive function to comprehend the instructional methods. Although the method can be instructed to help clear pharyngeal residues in the pyriform sinus, further studies are necessary to evaluate its effectiveness in a broader range of patients with weak pharyngeal contraction and impaired UES opening. Second, the teaching method has not been fully optimized; it is arguably complex, and developing a clearer method, such as through video demonstrations, is essential.
