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Oral vs. pharyngeal dysphagia: surface electromyography randomized study
© Vaiman and Nahlieli; licensee BioMed Central Ltd. 2009
Received: 02 October 2008
Accepted: 21 May 2009
Published: 21 May 2009
A clear differential diagnosis between oral and pharyngeal dysphagia remains an unsolved problem. Disorders of the oral cavity are frequently overlooked when dysphagia/odybophagia complaints are assessed. Surface electromyographic (sEMG) studies were performed on randomly assigned patients with oral and pharyngeal pathology to evaluate their dysphagia complaints for the sake of differential diagnosis.
Parameters evaluated during swallowing for patients after dental surgery (1: n = 62), oral infections (2: n = 49), acute tonsillitis (3: n = 66) and healthy controls (4: n = 50) included timing and amplitude of sEMG activity of masseter, infrahyoid and submental muscles.
The duration of swallows and drinking periods was significantly increased in dental patients and was normal in patients with tonsillitis. The electric activity of masseter was significantly lower in Groups 1 and 2 in comparison with the patients with tonsillitis and controls. The submental and infrahyoid activity was normal in dental patients but infrahyoid activity in patients with tonsillitis was high.
Dysphagia following dental surgery or oral infections does not affect pharynx and submental muscles and has clear sEMG signs: increased duration of a single swallow, longer drinking time, low activity of the masseter, and normal range of submental activity. Patients with tonsillitis present hyperactivity of infrahyoid muscles. These data could be used for evaluation of symptoms when differential dental/ENT diagnosis is needed.
For decades the investigation of dysphagia has been concentrated on evaluation of single and separate swallows of normal subjects and neurological or ENT patients [1–5]. The same tendency is traced in research activities with EMG evaluation of deglutition [6–9]. Dysphagia, or difficulty with swallowing, is defined as any defect in the intake or transport of endogenous secretions and nutriments necessary for the maintenance of life [2, 3]. Odynophagia is a painful swallowing and can occur even when "the intake or transport of endogenous secretions" is not affected [2, 3]. While dysphagia can be with or without pain, odynophagia it its turn can produce dysphagia secondary to odynophagia as patients trying to reduce pain change their normal swallowing patterns. When a general practitioner or a family doctor consults a patient who presented complaints on difficult swallowing or painful swallowing, they usually refers him/her further to a neurologist and/or otolaryngologist. Dysphagia and odynophagia, however, are common symptoms in oral medicine as well. They can appear following dental extraction , bimaxillary osteotomy , odontogenic infection , and other dental problems including oral cavity oncology . The connection between dentistry and dysphagia becomes more prominent in the elderly . In addition to that, salivary gland diseases like benign salivary gland tumours, sialolithiasis, sialadenitis, strictures and kinks, ductal polyps, etc. can start with pain or difficulties in mastication and swallowing [15, 16].
In cases of dental surgery or oral infections, odynophagia and dysphagia are usually related [17, 18]. I.e. while in cases of dysphagia of neurological origin patients do not feel pain, in cases when oral cavity is involved dysphagia frequently appears as a result of odynophagia. Thus, in fact, three conditions can be observed in patients: 1) "pure painless dysphagia" of anatomic, obstructive or neuromuscular etiology; 2) "pure odynophagia", when a patient experience pain during deglutition but the quality of swallowing itself is not affected and there are no secondary symptoms like weight loss, wheezing or pulmonary infections; 3) combined dysphagia/odynophagia when a patient feels pain during swallowing and swallowing itself is impaired.
Instrumental investigations like barium esophagram, manometry, manofluorography, bolus scintigraphy, videofluoroscopic swallowing study (VFSS) and videoendoscopic swallowing study (VESS) are essential for confirmation of dysphagia [19, 20]. These options are not specific for muscle testing and have nothing to do with cases of dysphagia of oral origin with an exception of VFSS that allows clear imaging of tongue movement. Moreover, they hardly can be called as simple noninvasive and inexpensive tests. The single swallow and continuous drinking tests usual for routine surface electromyography (sEMG) investigation of deglutition might be important not only in evaluation of dysphagia, but also in evaluation of odynophagia (for example, water drinking test after tonsillectomy) and in differential diagnosis in cases of dysphagia of unknown origin.
While it is well known and generally accepted that reduced buccal tension, poor dentition, disorders involved in muscles of mastication, reduced labial closure, reduced oral sensitivity, altered tongue contour and other similar oral/dental problems can cause dysphagia [10–13, 15], this knowledge is infrequently used for differential diagnosis when dysphagia is suspected. In addition to that, a referred pain is to be taken into account, so that pain originating in one area would be interpreted as coming from the other and produce secondary dysphagia. Thus, the need for a clear differential diagnosis between oral and pharyngeal dysphagia remains an unsolved problem. The current article focuses on sEMG description of swallowing in patients with predetermined oral and pharyngeal pathologies aimed to provide data for diagnosis and monitoring of dysphagia/odynophagia and to differentiate oral cases of dysphagia from pharyngeal cases.
Enrollment procedure and participant flow (Groups 1–3).
Randomly assessed for eligibility (n = 239)
Excluded (n = 32)
a. Not meeting inclusion criteria (had dysphagia and/or odynophagia due to reasons other than tonsillitis or dental problems; had chronic pain type syndromes requiring pain medication) (n = 19)
b. Refused to participate (n = 13)
Total allocated (n = 207)
Allocated to Group 1
(n = 71)
Group 2 (n = 60)
Group 3 (n = 76)
Lost to follow-up
(n = 9)
(n = 11)
(n = 10)
(n = 62)
(n = 49)
(n = 66)
Three muscle locations were examined in the study: (1) m. masseter, (2) the submental-submandibular muscle group that includes anterior belly of digastrics, mylohyoid, and geniohyoid, and (3) infrahyoid muscle group, all covered by platisma. These muscles were selected because they are superficial and they are thought to be involved in the oral and pharyngeal phases of the swallow.
The equipment used for the EMG recordings was a NeuroDyne Neuromuscular Sys/3 four channel computer based EMG unit with NeuroDyne Medical software, and AE-204 Active sensors attached to AE-131 electrodes. (NeuroDyne, Cambridge, MA, USA). Its specifications and sEMG techniques were described in detail in our previous articles [21–23]. The computer program indicates mean, standard deviation, minimum, maximum, range of muscle activity during each trial, and its duration. Muscle activity (EMG) is quantified in microvolt RMS.
The pain in odynophagia cases was assessed by visual analogue scale (VAS) pain score (0–10). Two tests were performed: voluntary single water swallows as normal from an open cup and continuous drinking of 100 cc of tap water from an open cup. In the Group 1 the tests were examined 24 hours after surgery following routine follow-up. The tests were described in detail in our previous articles [21, 23]. The single swallow test was performed after a mean volume of the normal swallow bolus was calculated for group of healthy volunteers (control group).
Three trials of swallowing mean volume of tap water from an open cup. The volume, calculated before the trials, was 15.5 cc per single swallow.
After that subjects performed a trial of continuous drinking of 100 cc of tap water.
The testing was repeated twice. A total of six swallows and two drinking periods were obtained per participant. Totally 954 swallows and 318 drinking periods were evaluated during this study. The graphic records were then evaluated. Twenty subjects were re-tested a day later to detect intertrial difference for the duration variable. These subjects were chosen randomly (sealed envelope method) from different group. Interjudge reliability was assessed by comparing scores obtained for each swallowing trial for each of the two tasks. Two judges blinded to group assignment were involved and the test observer agreement was good (Kappa coefficient 0.77).
We examined single swallowing and continuous drinking of 100 cc of tap water from an open cup (duration, mean electric activity of muscles, type of sEMG graphic record, and number of swallows). In the act of continuous drinking, the one gulp water intake can be measured by dividing 100 cc into the number of swallows the individual performed and this can be recorded on an sEMG system.
The data were analyzed off-line by computer. All graphic recordings were initially inspected by eye. The data were statistically evaluated by one-dimensional analysis of variance, SPSS, Standard version 10.0.5 (SPSS, Chicago, IL, 1999), and χ2 criterion using 95% confident interval. The level of significance for all analyses was set at p < 0.05. Normalization procedure was performed for electric amplitude records in order to change computer-calculated mean (raw mean) into real mean (raw mean minus the mean resting potential of an actual muscle group covered by skin). Further on in the results only real mean data is introduced. Obtained P values in multiple comparisons were then corrected using correction factor (Bonferroni method) to adjust the P value and reduce error in interpretation of statistics.
Single swallow test
Single swallow: duration of muscle activity excluding the initial oral stage (mean ± SD)
6.41 ± 0.78
4.57 ± 0.61
3.43 ± 0.49
3.35 ± 0.4 sec
p < 0.01
p < 0.05
p > 0.5
Electric activity of m. masseter, submental-submandibular and infrahyoid muscles in a single swallow test, in μV (mean* ± standard deviation).
9.115 ± 4.2
11.25 ± 5.37
28.33 ± 6.74
17.454 ± 7.55
30.750 ± 9.34
31.63 ± 8.35
34.2 ± 8.54
36.75 ± 10.34
14.765 ± 3.12
14.422 ± 4.65
36.73 ± 9.62
15.773 ± 6.95
The mean VAS scores during this test were 5.5 for Group 1, 3.6 for Group 2, and 6.2 for Group 3. Correlation between VAS data and sEMG data was insignificant for Groups 1 and 2 (p = 0.24 and p = 0.32 respectively) and significant for Group 3 (p < 0.05).
Continuous drinking test
The mean volume of liquid per swallow during continuous drinking was 14.7 cc for the control group, and only 9.4 cc for the group of operated patients (Group 1). We monitored a clear tendency for a decrease of the mean volume of liquid per swallow for the operated dental patients (p < 0.01) and patients with oral cavity infections (p < 0.05). Acute tonsillitis (Group 3) did not affect the duration of drinking.
Continuous drinking of 100 ml water – duration of muscle activity excluding the initial oral stage (mean ± SD)
Total duration (s)
17.9 ± 5.32
17.3 ± 5.3
10.8 ± 2.1
10.7 ± 2.81
Number of swallows
10.9 ± 3
9.4 ± 2.2
7.1 ± 1.4
6.9 ± 1.82
Duration of one swallow (s)
1.64 ± 0.6
1.75 ± 0.7
1.52 ± 0.3
1.51 ± 0.41
9.17 ± 2.85
10.64 ± 2.4
14.08 ± 3.1
14.5 ± 3.55
ml/swallow in %
The mean VAS scores during this test were 5.1 for Group 1, 3.3 for Group 2, and 5.4 for Group 3. Correlation between VAS data and sEMG data was insignificant for Groups 1 and 2 (p = 0.3 and p = 0.48 respectively) and significant for Group 3 (p < 0.05).
There was no statistically significant gender related difference for the duration and mean muscle activity during both tests for all groups (p = 0.12).
In the current article we want to draw attention on frequently overlooked oral cavity problems as a possible cause for dysphagia. The reason for presenting this study arose from our routine practice in the outpatient clinics of our ENT and Oral and Maxillofacial Surgery departments. We repeatedly consulted patients with dysphagia complaints referred to otolaryngology specialists by general practitioners who appeared to have oral problems. While patients with acute tonsillitis are frequently admitted to outpatient departments, the differential diagnosis between oral and pharyngeal dysphagia should be warranted. The reason for this is that patients seldom present their complaints presicely. A patient after a dental extraction, for example, can say that he/she feels "something uncomfortable" in the throat.
Surface EMG of swallowing is a simple and reliable method for evaluation of single swallowing and continuous drinking with low level of discomfort of the examination . In our departments, the sEMG is used for rapid evaluation of patients' complaints on dysphagia as well as to localize where the pain comes from. For example, in case of dysphagia and/or odynophagia caused by odontogenic infection in the submandibular space, the abnormal records will be observed at SUB location rather than at MS location. The onset of water swallow is usually seen as a mild elevation of the line and represents the final oral stage of a swallow which occurs when the tongue is moved so as to squeeze the liquid volume against the hard palate. Submental muscles and masseter support the tongue-induced pressure. At this stage the automatic reflexive gesture of swallowing is triggered. The same record taken from a patient after dental surgery indicated normal waves at submental-submandibular and infrahyoid locations and much lower wave, or almost no activity at all, at the masseter location.
This phenomenon clearly shows that the dysphagia in dental patients is of oral origin and does not affect pharyngeal stage of a swallow. In fact, this dysphagia is secondary to odynophagia. More precisely, what we might actually had been observing was compensation in patients with painful swallow. A patient tries to spare the operated site, does not clench teeth and, therefore, does not involve masseter in the acts of swallowing and drinking as it was clearly seen at the sEMG records. This condition may be called as "normal swallow modified by pain" (VAS pain scores 6.2–3.6) but terminologically we obliged to label it as dysphagia. Patients with acute tonsillitis might be suspected in having impaired submental muscular activity. In our study, however, the submental activity remained within normal range despite the fact that pharyngeal muscles are the main group of muscles involved in normal deglutition during pharyngeal phase. It seemed that during episodes of tonsillitis abnormally active infrahyoid muscles tried to "assist" the submental muscles in deglutition.
Oral alterations may occur in the occlusion of the teeth following dental surgery, and we may speculate that these might occur either as a direct involvement of the mandibular suspensory apparatus during the surgery, or as a result of compensatory muscle changes. The patients suffering from this condition appear to restore their occlusion to normal, provided that post-surgical recovery is successful. However, there seems to be a sort of break-point at about two weeks post-surgery. If the oral pain persists this long before it subsides, then the masseter seems to stay out of alignment. From the prospective of neuromuscular compensation, if there are functional connections between cervical afferents and V spinal neurons responsible for oral functions, then since most of V spinal neurons appear to be inhibitory to the jaw elevator muscles, one would expect cervical afferent stimulation to have similar effect. In fact, this exactly is seen at the sEMG records. These interactions, however, have yet to be studied.
Surface EMG appeared to be very convenient tool for assessment of patients with both the oral and the pharyngeal dysphagia/odynophagia. Its sensitivity and specificity was proven in several previous works [21–26]. Since the surface EMG monitors the summed activity of large groups of muscle fibers, surface EMG recordings are repeatable. Surface EMG is thus more valid than needle EMG for assessing and quantifying whole muscle function according to statistical criteria .
Quick reference sEMG differential diagnostic table Oral vs. Pharyngeal Dysphagia.
The duration of the reflex phase of swallows shows significant increase in patients who presented symptoms of dysphagia after lower molar surgery or oral infections. Electric activity of the oral muscles is low in these cases, while activity of submental and infrahyoid muscles remained normal. The timing of events and amplitude data can be used for diagnostic and differential diagnostic purposes, objectivization of complaints, as well as for comparison purposes in pre- and postoperative stages, monitoring of postsurgical healing, tracing postsurgical complications and in EMG monitoring during dental treatment.
Written consent was obtained from the patient shown in figure 1 for publication of their image. NO funding was involved in the study and NO funding was involved in the preparation of the manuscript.
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