Patient characteristics in the first experiment. F: female, M: male.
1. Introduction
Patients with dysphasia have a variety of motor deficits in orofacial and pharyngeal movements. Disorders in the orofacial region, such as dysphasia developed, may be induced by cerebral vessel disease, cancer in the orofacial and neck region, and other conditions. Functional assessment of mastication and the deglutition is most likely to be performed using videoendoscopy (VE) and videofluoroscopy (VF), although electromyography (EMG), ultrasonography (US), and other modalities are also used. Although VE is the primary method for examination of swallowing, projection of VE during instantaneous variations in swallowing cannot be observed because of whiteout. On the other hand, although VF is the best choice for functional assessment of eating and swallowing, we cannot avoid a bombing experience. Therefore, we devised a new method to reduce the reliance on VF examination.
Electrical thresholds of the sensation of structures with primary disease in the orofacial region of patients with stroke, head and neck tumor, external injuries, and other conditions following orofacial treatments were examined. The results suggested a close relationship between the electrical threshold of sensation and the recovery process, because patients with various orofacial and neck diseases showed a lower threshold of electrical sensation associated with treatment. Thus, changes in the oral and pharyngeal phases using VF in patients with brain tumors, stroke, external injuries, amyotrophic lateral sclerosis and myasthenia gravis were investigated.
Many researchers have evaluated VF results based on the Videofluorographic Examination of Swallowing Worksheet developed by Logemann [8]. However, because the inspection items on this worksheet comprise many measurement items, numerous hospitals conduct their own modified VF assessments [2, 3, 5-7, 14]. Based on experiences in other hospitals, 11 key events were identified for the assessment of VF: bolus formation, tongue-to-palate contact, premature bolus loss, residue in the oral cavity, and oral transit time in the oral phase; and lift in the soft palate, triggering of the pharyngeal swallow, vallecula residue, pyriform sinus residue, pharyngeal transit time, and aspiration in the pharyngeal phase. Furthermore, these items were classified into three levels: grade 0 as normal, grade 1 as inadequate, and grade 2 as a true abnormality. The total scores for all items in the oral and pharyngeal phases separately are calculated and a higher sum in each phase represented a more serious condition is presumed. Electrical thresholds of sensation on the soft palate during the hospital visit were measured, too. Guidance regarding an accepted way of stretch training fitting various disorder parts, such as gum rubbing, the Mendelsohn maneuver, thermal tactile stimulation, the head lift exercise (Shaler exercise), the tongue holding maneuver and Sylvester maneuver. Trainings involved procedures suitable for each patient after obtaining first-person informed consent. For example, patients with the deglutition disorder were performed by thermal tactile stimulation during the hospital visit and Shaker exercise in the residence. Patients performed the training method best suited to their disease twice daily.
Finally, we examined the relationship between the total scores for all items in the oral and pharyngeal phases and the threshold of electrical sensation on the soft palate. We hypothesized that if electrical threshold measurement can be substituted for VF assessments, radiation exposure to patients can be reduced. Furthermore, electrical threshold stimuli on the soft palate and other areas are produced by an appeal of a loose press feeling in the stimulus area of subjects, not painful sensation.
2. Material and method
We aimed to elucidate the relationship between changes in the electrical threshold of sensations associated with various orofacial symptoms and the recovery processes of areas affected by orofacial disorders depending on the oral rehabilitation technique. Thus, we investigated the relationship between modified VF assessments and sensory electrical threshold evoked on the soft palate. In particular, electrical stimuli are appealed by a loose press feeling in the stimulus area of subjects, not painful sensation.
2.1. Subjects
We utilized the total scores for all items in the oral and pharyngeal phases separately. In particular, we considered that a higher sum in each phase might indicate a more serious condition. All procedures were approved by the ethic committee at Nihon University School of Dentistry.
2.2. Threshold of electrical sensations
2.3. Modified VF worksheet
Although the VF worksheet proposed in Logemann’s study [8] is used by many dentists and otolaryngologists, many medical institutions use a more concise version. We divided the dysphasia scale into the oral phase and pharyngeal phase. In the oral phase, we examined the bolus formation, tongue-to palate contact, premature bolus loss, residue in the oral cavity, and oral transit time. In the pharyngeal phase, we examined the lift in the soft palate, triggering of pharyngeal swallow, epiglottic vallecula, pyriform sinus residue, pharyngeal transit time, and aspiration.
For both the oral and pharyngeal phases, the bolus formation, tongue-to-palate contact, premature bolus loss, residue in the oral cavity, oral transit time, lift in the soft palate, and triggering of the pharyngeal swallow were categorized into three levels: grade 0 as normal, grade 1 as inadequate, and grade 2 as a true abnormality (Table 3). In particular, the amount of premature bolus loss, residue in the oral cavity, and epiglottic vallecula and pyriform sinus residue were divided into three levels: grade 0 indicated no residue, grade 1 indicated residue in <50% of the bolus, and grade 2 indicated residue in >50% of the bolus. Furthermore, aspiration was divided into three levels: grade 0 indicated no aspiration, grade 1 indicated supraglottic penetration and grade 2 indicated subglottic aspiration.
All oral and pharyngeal phase criteria were categorized into three levels, 0, 1 and 2. Based on the assortment of the three levels according to the standardized definition, wthat a more serious condition in the oral or pharyngeal phase would be indicated by a higher total for each criterion, as shown in the totals for the oral and pharyngeal phases in Table 3. We considered that assessments performed using these three simplified levels would provide consistency with respect to the criteria used during long-term evaluation (>2 months after symptom onset). The criterion for each phase (oral and pharyngeal) was employed by the total.
3. Results
All criteria of the oral and pharyngeal phases were categorized into three levels: 0, 1 and 2 (Table 2). We investigated the relationship between the threshold of sensation and each value in the VF assessment of each patient’s disease condition. These values were grouped into classes according to the data shown in Table 3. The total score of the VF assessments in the oral and pharyngeal phases and the threshold of sensation in each patient are shown in Figures 3Aa, 3Ab and 3B; the averages and standard deviations in each figure are indicated in Figures 3C and 3D. Almost all data showed a recovery trend (negative “gradient” of the regression curve) with the exception of amyotrophia lateral sclerosis and myasthenia gravis. Thus, amyotrophic lateral sclerosis and myasthenia gravis did not exert a curative influence on our treatment, because suggesting based on the VF and threshold that sensation did not recover (Figure 3: black lines, amyotrophic lateral sclerosis; red lines, myasthenia gravis). These results may suggest that such muscle diseases do not recovery with the type of training performed in this study. Although the average scores of the VF assessments and threshold electrical stimulation indicated a recovery trend for all diseases, separate analysis for each disease was importance to obtain more detailed data. Based on these findings, we believe that the electrical threshold of sensation on the soft plate may reflect the recovery process of swallowing reflex disorders.
4. Discussion
4.1. Total of VF assessments in the oral and pharyngeal phases and the threshold of electrical sensation
It was investigated that the relationship between the threshold of sensation and each value in the disease history of each patient. The relationship between the total in the oral phase and the threshold of sensation differed significantly (paired t-test, P<0.05). Furthermore, the relationship between the total in the pharyngeal phase and the threshold of sensation were statistically significant at P<0.01. The regression curves of each relationship were examined, too. The total scores of the VF assessments in the pharyngeal phase and the threshold of electrical sensation were strongly associated (r2=0.75). However, the total score of the VF assessments in the oral phase and the threshold of electrical sensation were not strongly associated (r2=0.13) (Figures 4A and 4B).
Because the total scores in the pharyngeal phase and the threshold of sensation showed a strong correlation, the decrease in electrical sensation might be related to recovery of the pharyngeal phase.
4.2. Relationship between VF assessments and electrical stimulations on the soft palate
We considered the presence of a relationship between the recovery process and electrical threshold of sensation, as shown in the first experiment. The results were assumed by a close relationship between the two. Why is there a relationship between a decrease in the threshold of electrical sensation and the recovery process? The well-known phenomenon of “active touch” or “haptic perception” is characterized by object perception through touch. It has been believed that sensory organs function by passive touch. However, Asanuma and Arissian [1] reported the functional role of peripheral input to the motor cortex during voluntary movements in the monkey. Specifically, they proposed that voluntary movements are induced by peripheral sensory inputs. Thus, we believe that measurements of the threshold of electrical sensation are necessary to measure recovery of voluntary movements.
Furthermore, our hypothesis involves the relationship between VF assessment parameters and electrical stimulation in patients with various disorders. VF assessments were divided into the oral and pharyngeal phases because the former is controlled by the first motor cortex of cerebral cortex (M1) and the latter is controlled by the brain stem. In particular, VF assessments of the oral phase are related to voluntary masticatory movements, while VF assessments of the pharyngeal phase are related to the swallowing reflex. We evaluated the relationship between VF assessment parameters and electrical stimulation in patients with various disorders using the swallowing worksheet proposed by Longemann [8], because we utilized measurements in the oral phase (related to masticatory processes) and pharyngeal phase (related to the swallowing reflex). In oral phase, we measured (1) bolus formation, (2) tongue-to-palate contact, (3) premature bolus loss, (4) residue in oral cavity, and (5) oral transit time. On the other hand, measurements in the pharyngeal phase included (1) lift in the soft palate, (2) triggering of pharyngeal swallow, (3) epiglottic vallecula residue, (4) pyriform sinus residue, (5) pharyngeal transit time, and (6) aspiration. The relationship between total VF assessments in the oral phase and the threshold of electrical sensation showed a weak association with cerebral hemorrhage, cerebral contusion, amyotrophic lateral sclerosis and myasthenia gravis (Figure 4A). However, the relationship between total VF assessments in the pharyngeal phase and the threshold of electrical sensation had a strong association with these disorders (Figure 3B). On the other hand, a decrease in the electrical threshold of sensations following the treatment process was not observed in patients with amyotrophic lateral sclerosis or myasthenia gravis (black and red lines of Figures Aa, Ab and B).
In summary, the criteria for evaluating recovery of the swallowing reflex may be covered by the electrical threshold of sensation on the soft palate, and acceptance of the electrical stimulation will produce a reduction in the bombing experience. Why dose the threshold of electrical sensation reflect recovery of the swallowing reflex? The reflex arc progresses as follows: receptor organ, afferent fiber, central nerve for the reflex, efferent fiber and effector organ. In particular, initiation of the swallowing reflex starts from the regions that induce swallowing (primarily the soft palate, posterior part of tongue, and posterior wall of the pharynx). VF assessments of the pharyngeal phase exhibited the swallowing reflex, and this reflex was initiated by stimulation of the regions that induce swallowing. We consider that the stimulation of these regions involves perception by sensory organs, and the swallowing reflex is then evoked by the sensory stimulation.
4.3. Relationship between electrical sensation and voluntary movement or reflex
When we execute hand movements (especially during search behavior), we take notice of a keen sense in the fingers. Namely, our cutaneous sensation is excited before the execution of movements. This helps us to understand the inaccuracy and inadequacy of movements in patients with sensation disorders. In particular, when the patients with unilateral lingual nerve disease (e.g., secondary to sensory nerve damage during wisdom teeth extraction) are promoted to perform tongue protrusion, the tongue bends toward the diseased side. Furthermore, monkeys with tactile agnosia after blocking of the first somatosensory cortex (SI) exhibit poor performance in gripping an object (Hikosaka et al.) [4]. Nelson [9] reported somatosensory neuronal activity in the SI prior to movement. These results indicate that sensory information in the SI is necessary for the initiation and preparatory of the start of movements. Based on these findings, it is understandable that the somatosensory information obtained prior to movement excites the facial, intraoral, and pharyngeal regions. Sessle et al. [10]. Sessle [11], Stohr and Petruch [12] and Stohr et al. [13] reported that a close relationship between the facial motor and sensory cortices is needed during facial and tongue movements. We assumed the presence of a relationship between electrical sensation and the recovery process based on our findings in the orofacial region. However, two patients in the present study (nos. 7 and 8, Table 2) exhibited no change with electrical stimulation treatment. Both of these patients had muscular atrophy, a degenerative disease. These results may suggest that progressive deterioration of the muscle and spinal cord make reconstruction difficult. On the other hand, although a close relationship between VF assessment of the pharyngeal phase and electrical stimulation on the soft palate was observed (cumulating tendency), there was a week relationship between VF assessment of the oral phase and electrical stimulation on the soft palate (scattering tendency) (Figures 4A and 4B). VF assessments of the oral phase involved stimulation of various regions of masticatory movements controlled by the M1. Because disorders of these regions become diffuse around the orofacial region, the electrical sensation of the soft palate cannot cover the entire disease region. However, VF assessments of the pharyngeal phase showed that the swallowing reflex was initiated by stimulation of the regions involved in induction of swallowing (primarily the soft palate, root of tongue, and posterior portion of wall of pharynx). We believe that this conclusion can be drawn from our experimental data: measurement of the electrical threshold can be performed as a substitute for VF assessment in the pharyngeal phase, and patients can undergo less radiation. Namely, the swallowing reflex, nasopharyngeal closure, elevation of hyoid bone and pharynx (laryngeal elevation), laryngeal closure (downward movement of the epiglottis), and esophageal sphincter relaxation are accomplished by serial processing after the initiation of sensory stimulation in the induced regions. We arrived at this conclusion from our experimental data.
Measurement of the electrical threshold can be performed as a substitute for VF assessment in the pharyngeal phase, and patients can undergo less radiation as a consequence.
5. Conclusion
Although VF (videofluoroscopic examination of swallowing) is the best choice for the functional assessment of eating (mastication) and swallowing, we cannot avoid a bombing experience. Therefore, we devised at new method to reduce the need for VF examination. The electrical threshold of sensation in centrally diseased sites of the orofacial region has long been examined in patients with stroke, head and neck tumor, external injury and other disorders following on the orofacial treatments. The results suggest a close relationship between the electrical threshold of sensation and the recovery process. Many researchers have evaluated the results of VF assessments based on the Videofluorographic Examination of Swallowing Worksheet developed by Logemann (1993). We selected 11 applicable items used by many hospitals: bolus formation, tongue-to-palate contact, premature bolus loss, residue in oral cavity, and oral transit time in the oral phase; and lift in the soft palate, triggering of pharyngeal swallow, vallecular residue, pyriform sinus residue, pharyngeal transit time, and aspiration in pharyngeal phase. In particular, we considered that a higher sum in each phase might indicate a more serious condition. We also measured the electrical threshold of sensation on the soft palate when patients visited the hospital. Why is the threshold of electrical sensation reflected by recovery of the swallowing reflex?
In particular, VF assessments in the oral phase are related to voluntary masticatory movement, while those in the pharyngeal phase are related to the swallowing reflex. Initiation of swallowing reflex starts from the regions that induce swallowing (primarily the soft palate, posterior part of tongue, and posterior wall of the pharynx). We propose that electrical thresholds in the soft plate can be assessable as the function of swallowing reflex.
Nomenclature
VE: videoendoscopic evaluation of swallowing. VF: videofluoroscopic examination of swallowing. SI: first somatosensory cortex. M1: first motor cortex.
Acknowledgments
This work was supported by Sato research grand and Sogoshigaku research grant of Nihon University School of Dentistry, by Grants-in-Aid for Scientific Research (21592539) and by a grant from the Ministry of Education, Culture, Sports, Science, and Technology to promote multi-disciplinary research projects.
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