Surface electromyography as a screening method for evaluation of dysphagia and odynophagia
© Vaiman and Eviatar; licensee BioMed Central Ltd. 2009
Received: 26 November 2008
Accepted: 20 February 2009
Published: 20 February 2009
Patients suspected of having swallowing disorders, could highly benefit from simple diagnostic screening before being referred to specialist evaluations. The article analyzes various instrumental methods of dysphagia assessment, introduces surface electromyography (sEMG) to carry out rapid assessment of such patients, and debates proposed suggestions for sEMG screening protocol in order to identify abnormal deglutition.
Subject related books and articles from 1813 to 2007 were obtained through library search, MEDLINE (1949–2007) and EMBASE (1975–2007).
Specifics steps for establishing the protocol for applying the technique for screening purposes (e.g., evaluation of specific muscles), the requirements for diagnostic sEMG equipment, the sEMG technique itself, and defining the tests suitable for assessing deglutition (e.g., saliva, normal, and excessive swallows and uninterrupted drinking of water) are presented in detail. SEMG is compared with other techniques in terms of cost, timing, involvement of radiation, etc.
According to the published data, SEMG of swallowing is a simple and reliable method for screening and preliminary differentiation among dysphagia and odynophagia of various origins. This noninvasive radiation-free examination has a low level of discomfort, and is simple, time-saving and inexpensive to perform. The major weakness of the method seems to be inability for precise diagnostic of neurologically induced dysphagia.
With standardization of the technique and an established normative database, sEMG might serve as a reliable screening method for optimal patient management but cannot serve for proper investigation of neurogenic dysphagia.
Swallowing disorders comprise an interdisciplinary phenomenon. Practitioners in various fields of medicine, such as otorhinolaryngology, neurology, general medicine, gastroenterology, head and neck surgery, dentistry and facial surgery, pediatrics and psychiatry deal with these disorders regularly, but family doctors and emergency department personnel might well be the first physicians to evaluate these patients.
Dysphagia is a difficult or abnormal swallowing, which can include nasopharyngeal regurgitation and aspiration . It is also defined as any defect in the intake or transport of saliva, liquids and food necessary for the maintenance of life. Odynophagia is a painful swallowing. Odynophagia is not a constant pain in the throat but rather pain on swallowing (swallow-evoked pain) . It was F. Magendie who, in 1813, established the concept of three stages in the act of swallowing: oral, pharyngeal, and oesophageal [3, 4]. Since the 1980s, the act of swallowing has sometimes been described as consisting of four stages, with the oral stage being divided into oral initial (for solids – oral preparation stage) and oral final stages . In case of liquid swallowing, during the oral initial stage the water intake takes place and a labial seal occurs. The oral final stage occurs when the tongue squeezes the liquid volume against the hard palate so that it is propelled past the anterior faucial arches. At this stage the automatic reflexive gesture of swallowing is triggered, but the oral stage itself remains under complete conscious control. During the pharyngeal stage the liquid volume is transferred from the level of the faucial arches through the pharynx to the cricopharyngeal sphincter at the rostral aspect of the esophagus. This stage is often described as a reflex, i.e. a person cannot stop swallowing in the middle of the process. In the oesophageal stage of the swallow, the water volume is transferred in a continuation of the peristaltic movement from the cricopharyngeal to the gastro-oesophageal sphincter at the entrance to the stomach.
The above described combination of voluntary and involuntary stages in deglutition makes evaluation of swallowing pathophysiology a difficult and sometimes timely and expensive process. Different diagnostic techniques were proposed for it. 20 years ago, in 1988, in a general description of evaluation of swallowing pathophysiology, the list of these techniques was as follows: still X-ray, computerized axial tomography (CAT), magnetic resonance imaging (MRI), indirect laryngoscopy, pharyngeal manometry, scintigraphy, ultrasound, videofluoroscopy . Electromyography (EMG) was not in this list. 10 years ago, in 1998, the list was somewhat changed and included barium esophagram, air contrast esophagram, manometry, manofluorography, flexible endscopic evaluation of swallowing with sensory testing (FEESST), bolus scintigraphy, ultrasonography, videofluoroscopic swallowing study (VFSS), and videoendoscopic swallowing study (VESS) . Once again, EMG was not mentioned.
At that moment, disadvantages for each of the above mentioned methods were well known. In brief, they are:
barium esophagram – uses x-irradiation, needs a facility and personnel, no dynamic futures;
bolus scintigraphy – cannot see patient anatomy, uses isotopes ;
ultrasonography – segmental, cannot present panoramic anatomic detail, expensive ;
VESS – the phases of swallowing cannot be seen directly, and also aspiration that occurs during the swallow, the function of the cricopharyngeus muscle cannot be directly assessed .
VFSS – relies on x-irradiation, needs radiology equipment and personnel, expensive ;
Currently VFSS is the most commonly used tool in the assessment of oropharyngeal dysphagia, and it is considered the gold standard in the dysphagia workup. But in addition to above mentioned drawbacks, VFSS does not always identify neuromuscular abnormalities in pharyngeal or laryngeal physiology.
Comparison between swallowing studies options in respect to radiation, timing and cost
Air Contrast Esophagram
Do we need dysphagia screening?
Dysphagia occurs in approximately 14% of patients in acute care setting an up to 50% of patients in nursing homes . Its prevalence is related to the fact that dysphagia often is present in patients who have sudden-onset ENT or neurologic disorders , head and neck cancers, chronic neurodegenerative diseases, and patients with general medical problems, but in general it is indeed an interdisciplinary phenomenon. Even practitioners in the field of pediatrics [19, 20] deal with these disorders. However, more than 75% of cases of oropharyngeal dysphagia are caused by ENT problems or neuromuscular disorders . To carry out the rapid assessment of patients with dysphagia and/or odynophagia requires a simple screening diagnostic tool to be used before extensive clinical and instrumental examination will be performed by a specialist. The diagnostic tool should be
providing both qualitative and quantitative data
simple and easy to operate
In general, aim of a screening procedure is to separate patients into a "passed"- vs. "failed" group, specifically into groups with normal and abnormal deglutition. Screening so far is a filter to decide whether further clinical diagnostics or treatment is necessary. In case of dysphagia, however, the second step after normal-abnormal screening is needed. This step might answer the question to what specialist a dysphagic patient should be referred to: neurologist? ENT-physician? dentist? gastroenterologist? psychiatrist? This second screening stage is actually more practicable comparing with the first passed-failed one because initial dysphagia detection starts with a history taking.
Swallowing is a muscular process. Its mechanism, by which food is transmitted to the stomach, is a complex action involving 26 muscles and five cranial nerves . This fact suggests that surface electromyography (SEMG) might be a valuable method to be used for screening purposes and early diagnostics of dysphagia and odynophagia complaints. Indeed, surface SEMG provides information on the timing of selected muscle contraction patterns during swallowing [23–25], amplitude of electric activity of the muscles , and can be easily learned by the personnel [27, 28]. Some suggestions have been already made for using SEMG for screening purposes in neurogenic dysphagia .
Quick reference simplified set of normative data for electric activity obtained by surface EMG for masseter and submental group + platisma during various tests, in μV
18–30: 4.5 – 15.9
31–70: 5.54 – 12.1
31–70: 9.52 – 49.5
61–70: 1.97 – 27.69
51–70+: 7.4 – 44.8
20 cc excessive swallow
41–70:1.2 – 29.4
31–70+: 12.1 – 47.44
100 cc drinking
masseter mean (real)
18–70: 0.8 – 6.2
70+: 1.0 – 7.84
submental mean (real)
18–60: 3.5 – 11.5
61 – 70+: 4.25 – 16.25
Up to date, however, we face various technical approaches to SEMG usage in evaluation of swallowing process. While the normative database for SEMG assessment of deglutition has been established, the next step might be establishment of standards for this diagnostic procedure, i.e. the protocol. Large variation in examination techniques, strategies, interpretations and diagnostic criteria have been found among electromyographers and it is suggested that the value of SEMG studies of deglutition may be further improved by international standardization.
Surface EMG as a screening method
SEMG is to be clearly separated from needle electrode examination EMG . Needle electrodes should be used within the neck area with great precaution and this procedure will be neither time-saving, nor noninvasive. The needle EMG report includes tabulated nerve conduction studies, which are not needed at the screening stage of investigation.
Reliability of the method was proved in a series of research using SEMG for diagnostic purposes in oral [38, 39], pharyngeal [40–43] and esophageal  diseases. These investigations suggested that different diseases have specific SEMG patterns, both in timing and amplitude of the record. The graphic record itself has visible peculiarities specific for each disease. Filtered SEMG provides a simple EKG-looking line easy to analyze and interpret.
If a diagnostic method is offered to be used in different areas of medicine but for one purpose, the standard protocol is a must. The need for established protocols in SEMG investigations is well understood [45–48], and several attempts already have been made [49, 50]. To our knowledge, no such protocols were proposed for SEMG evaluation of dysphagia and odynophagia. SEMG evaluation of deglutition is not a new diagnostic method. Nevertheless, lack of standard requirements decrease the outcome of this investigation technique significantly. In the case of SEMG evaluation of deglutition the protocol might be based on:
protocol requirements for diagnostic equipment
normative database and standard analysis
Suggestions for protocol application
As it was mentioned above, the act of swallowing is described as consisting of four stages, as the oral stage was divided into oral initial (for solids – oral preparation stage) and oral final stages . This staging can be helpful in diagnostic evaluation of disorders providing dysphagia and odynophagia. Each of these stages can be impaired and the screening evaluation should be capable to indicate the impaired stage. Surface SEMG recording cannot trace oesophageal activity and only initial oesophageal stage can be recorded and evaluated. SEMG does not detect silent breathing.
Any other SEMG device with similar characteristics can be used but one quality has to be insured: the SEMG record has to be full-wave rectified and low-passed filtered in a way to look like a single EKG-looking line. SEMG records with numerous closely packed spikes are almost impossible to interpret rapidly. If the four-channel device is used, the investigation can be performed in 3–5 minutes in cases when we have full cooperation of a patient.
for oral phase: the orbicularis oris superior and inferior (OO),
for oral phase: the masseter (MS),
for pharyngeal phase: the submental muscle group (SUB) which includes the anterior belly of the digastric, mylohyoid, and geniohyoid, all covered by the platysma,
for pharyngeal and initial oesophageal phases: (INF), the infrahyoid group, thyrohyoid, and the laryngeal strap muscles also covered by the platysma.
Two bipolar stick-on surface electrodes are to be applied at the right or left angle of mouth, one electrode above the upper lip, and another electrode below the lower lip (OO-location);
Two electrodes are to be placed parallel to the masseter muscle fibers on the left or right side of the face, preferably on the opposite side from the OO-location (MS-location);
Two surface electrodes are to be attached to the skin beneath the chin on the right or left side of midline to record SUB myoelectrical activity over the platysma (SUB-location);
Two electrodes are to be placed on the left or right side of the thyroid cartilage to record from the laryngeal strap and infrahyoid muscles (INF-location).
when OO-location is uninformative, but some general muscular-neurologic disease is suspected, the fourth electrode can be attached above a muscle not involved in deglutition, for example, above m. trapezius (Fig. 1). The same variation is preferable in cases of psychogenic swallow or malingering, when a patient strains muscles not involved in deglutition.
The exact electrode positions for each muscle group have been known since the 19th century [54, 55], and, in addition, can be clarified following anatomical correlates . The proposed electrode locations cover all stages of a swallow. The staging of normal deglutition can be clinically important as an additional tool for establishing aetiology and localization – oral, pharyngeal, or oesophageal – of causes for dysphagia or odynophagia. Each stage has its mean normal duration and its specific graphic pattern. Each pair of electrodes has a third electrode as ground. Electrical impedance at the sites of electrode contact might be reduced since the target areas are lightly scrubbed with alcohol gauze pads. Radiates skin, edematous skin and status post neck dissection are possible counter-indications for SEMG investigation.
Three trials of "dry" swallowing. Instruction given: "Swallow your saliva".
Three trials of swallowing normal volume of tap water for a particular person. These volumes, calculated for a particular age group [31–36], are: Group 1 (age 18–40) – 16,5 cc; Group 2 (age 41–70) – 14,5 cc; Group 3 (age 70+) – 12 cc. Instruction given: "Swallow this water in one gulp".
Three trials of swallowing 20 cc of tap water to check adaptation abilities of the patients ("stress test", larger bolus volume accommodation). Instructions given: "Swallow this water in one gulp".
One trial of continuous drinking of 100 ml of tap water. Instruction given: "Drink this water as normal".
The main test is a single water swallow as normal. Saliva swallow might be very important test in case of salivary glands diseases like, for example, Sjögren syndrome. Stress test with excessive amount of water swallowed in one gulp might reveal lack of larger bolus volume accommodation abilities in cases of anatomical changes of the pharynx, neurological problems or might provoke regurgitation in patients with Zenker's diverticulum. Testing of continuous drinking is important not only in the evaluation of dysphagia but also of odynophagia and in the differential diagnosis in cases of compulsive water drinking, excessive water drinking, the malingering of dysphagia and psychogenic disorders expressed by symptoms of dysphagia. This is the test that can help in better evaluation of slight dysphagia in fast-fatigable subjects. For fast-fatigable subjects continuous non-interrupted drinking is a stress test . The amount of water for continuous drinking test was set at 100 cc, approximately one-half of a standard glass because a smaller volume, e.g., 50 cc, can be swallowed in two gulps and provide inadequate data while we had observed that 200 cc of water involves significant swallowing/ventilation interactions which can confound the validity of the obtained data.
In addition to water swallow tests, there are tests with food, involving mastication. They can be justified in cases of diseases of temporomandibular joint and some other disorders. For screening purposes, however, simple water swallow tests are sufficient.
Protocol analysis includes assessment of duration (in sec), amplitude of electric activity (mean, in μV), graphic patterns and number of swallows (in continuous drinking). To carry out the rapid assessment of patients, the SEMG record should be clear and easily understandable. A comprehensive study was recently performed in which SEMG was used for monitoring functionally distinct muscle activation during swallowing . This study supports the statement that raw SEMG records should be rectified and filtered before evaluation.
There is no visible difference between the shapes of SEMG recordings of swallows based on gender [31–36, 38–44]. Elderly patients (age 70+) showed age-induced peculiarities in the recorded swallows. In general, prevalence of dysphagia increases with age and poses particular problems in the older patient, potentially compromising nutritional status, complicating the administration of solid medications, increasing the risk of aspiration pneumonia and undermining the quality of life . For them, the muscle activity is usually longer in duration, and suggests a lack of coordination between activities of different muscles involved in deglutition both in single swallows and continuous drinking. For children, the duration of muscle activity during swallows and drinking in all tests showed decrease with the age, and this tendency is statistically significant. There is no statistically significant difference in electric amplitude measurements between children and adults .
Slow swallows and drinking are usually observed in cases of various neurological disorders affecting deglutition [60–63]. Analyzing timing one needs to remember that the times indicated by an SEMG device represent the duration of SEMG activity which lasted longer than the actual time required to pass a bolus from the oral cavity to the oesophagus.
Published studies [67, 68] on normal subjects show a very wide range of normal electric amplitudes for SEMG studies. These variations are not only due to biologic causes but are also greatly affected by such technical factors as skin/electrode impedance, depth of the muscle from the skin surface, location of the recording electrodes in relation to anatomic structures, variation in muscle size among individuals, and temperature. It is because of the wide variation in the normal values that an absolute value of the amplitude is considered less clinically useful.
The SEMG amplitude, however, remains an important aspect in the relationship between muscle force and the associated electric activity. There is, however, no simple relationship between an SEMG signal and muscle force. When all the different types of neuromuscular disorders are considered collectively, amplitudes are by far the most informative features . Some authors argue that amplitudes are the only components that have a direct relationship to clinical symptoms (muscle weakness) in neurogenic lesions .
Also, during SEMG testing, there is a certain amount of impedance noise that arises directly from the resistance of the electrodes' connection to the skin. This makes skin resistance a significant factor when working with the low-level SEMG signals typical of small muscles involved in swallowing. Wiping the skin with isopropyl alcohol in a water solution has proven to be the best form of preparation for most situations. The alcohol removes the dead skin and surface oils, and the water moistens the skin and provides improved ion flow. The SEMG sensors we used are designed so that the use of electrode gel is generally not necessary.
Quick reference simplified set of SEMG data for screening purposes.
T A S
T A S
T A S
↑ ↓ Abn
↑ ↓ Abn
↑ N N
N N N
N ↓ Abn
N ↑ N
↑ ↓ Abn
↑ N N
↑ N N
N N N
↑ N Abn
Abn Regurgitation Peaks
N N N
N N N
N N N
This study emphasizes that a surface SEMG analysis of all the muscle groups involved in swallowing process, following a proper placement of the electrodes and selection of tests, can give reliable indications of muscle activity and provide data for screening evaluation of complaints a patient came with. Further investigation might help to develop a proper combination of flexible endoscopic evaluation of swallowing (FEES) with a nasopharyngoscope (or flexible endoscopic evaluation of swallowing with sensory testing, FEESST) with SEMG to achieve complete evaluation of swallowing without exposure to radiation. Such screening might help a general practitioner to direct a patient to a neurologist, ENT physician or other proper specialist and to a specific radiographic or, perhaps, manofluorographic investigation [72–74]. Other topics for further investigation might be SEMG detecting of sensory predeglutitive oropharyngeal swallowing disorders, detecting dysphagia in patients after head and neck tumor therapy.
Dysphagia due to neurologic problems, however, might present difficulties when investigated by surface EMG. It may be possible to collect data using surface electrodes, sufficient to make conclusions with respect to patients with odynophagia or non-neurological disorders such as ENT disturbances. It is, however, difficult to nearly impossible to collect proper knowledge about neurogenic dysphagia including important and urgent etiologies such as stroke, ALS and so on. While surface kind of recording picks up not only muscle activity related with swallowing but also that of some other contiguous muscles with random or associated activity during swallowing, direct and precise neurologic assessment seems problematic. Despite that, screening assessment might be successful even in neurological cases if the record shows abnormal timing (prolongation), abnormal voltage (decreased) and abnormal shape of a signal (no peak).
In this respect it might be added that neddle EMG provides valuable data when neurologic problems are investigated. Numerous researches using needle EMG contributed significantly to our knowledge of single muscle actions during deglutition [75, 76]. Specifically these studies were important for neurologic diseases . Technically, however, needle EMG is an invasive and time-consuming investigation requiring expensive devices and being potentially dangerous in the neck area . While this type of EMG testing might be invaluable to establish precise diagnosis, this method might be hardly recommended as a screening technique.
It is estimated that 15 million patients suffered from a swallowing disorder during each year in the United States alone [81, 82]. These data make us to believe that the screening method for this disorder might be a very timely addition to our evaluation techniques.
Surface SEMG of swallowing is a simple and reliable method for screening and initial evaluation of dysphagia and odynophagia complaints of various origins. This noninvasive radiation-free examination has low level of discomfort, simple, time-saving and inexpensive. With proper standard technique and established normative database surface SEMG can serve as a reliable screening method for assessment of dysphasia of unknown origin in order to refer a patient to a neurologist or some other proper specialist and proper further investigation. The findings are the impetus for further study regarding the mechanisms of muscle activity changes in disorders affecting swallowing.
Written informed consent was obtained from the patient for publication of accompanying image. A copy of the written consent is available for review by the Editor-in-Chief of this journal.
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