Clinical manifestations

Presentation and course

	• Dysphagia or swallowing difficulty may be associated with other symptoms such as tracheobronchial aspiration.
	• Prognosis of dysphagia depends on the cause or the primary disease.
	• Dysphagia is frequent in neurodegenerative disorders such as Parkinson disease.
	• The clinical and videofluoroscopic features of dysphagia due to stroke at presentation are important predictors of recovery of swallowing.

Dysphagia usually manifests as a sensation of "stickiness" or difficulty in swallowing food. In upper oropharyngeal dysphagia, there is difficulty in initiating the act of swallowing, but once initiated, swallowing is completed normally. In esophageal dysphagia, the swallowed food may eventually navigate the esophagus or may be regurgitated or vomited if the obstruction is severe. An associated symptom is tracheobronchial aspiration if there is pharyngeal paralysis. Other associated symptoms include hiccups and hoarseness, the latter implying lesions affecting both the pharynx and the larynx. Laryngitis may also occur in patients with gastroesophageal reflux. Chest pain with dysphagia occurs due to esophageal spasm or obstruction due to a large bolus. Patients with chronic dysphagia may present with weight loss and malnutrition due to inadequate food intake; the weight loss may also be due to a malignant lesion responsible for dysphagia.

Because of the large number of disorders associated with dysphagia, there are several other manifestations of the primary pathology. Several symptoms that are related to dysphagia, but need to be considered as separate entities, include:

	• Aphagia: the inability to swallow due to complete obstruction of the esophagus.
	• Odynophagia: painful swallowing.
	• Globus pharyngeus: the sensation of a lump in the throat without any difficulty in swallowing.
	• Phagophobia: fear of swallowing.
	• Presbyphagia: difficulty in swallowing with aging; without any disease in case of primary presbyphagia, but secondary presbyphagia could be a manifestation of disorders that are more common in the elderly. If difficulty in swallowing is so severe that it cannot be compensated for, the term presbydysphagia is used.
	• A prospective cross-sectional study using M-mode ultrasonography showed that stroke patients with dysphagia have decreased diaphragm excursion and compromised respiratory function during voluntary coughing (30).

Prognosis and complications

Prognosis of dysphagia depends on the cause. Dysphagia can be relieved if there is a benign obstructive lesion that can be removed. Prognosis is poor if obstruction is due to a malignant lesion. In cases of dysphagia due to neurologic disorders, the prognosis depends on the primary disease, the degree of advancement of the disease, and the stage of dysphagia.

The clinical and videofluoroscopic features of dysphagia due to stroke at presentation are important predictors of subsequent swallowing abnormalities. The prognosis is guarded and depends on the location of the infarction and the extent of neurologic deficit. Indicators of poor outcome include medullary lesions as well as a delay or absence of the swallowing reflex. Dysphagia in stroke is related to the involvement of the hemisphere with the dominant swallowing projection, and clinical recovery can be correlated with compensatory changes in the previously nondominant, unaffected hemisphere. Signs of aspiration in the first 72 hours of acute stroke can predict severe swallowing problems after 3 months (17). Screening for dysphagia has been recommended for identification of patients at risk for aspiration. A review of the few available randomized controlled trials on this topic concluded that there were insufficient data to determine the effect of dysphagia screening protocols on reducing the rates of pneumonia, death, or dependency after stroke (39).

More than half of patients with Parkinson disease suffer from dysphagia, and aspiration pneumonia is one of the major causes of mortality in these patients. Penetration-aspiration is the most severe sign of dysphagia, with aspiration pneumonia as one of its complications. Logistic regression of data from a retrospective study that analyzed videofluoroscopic studies of swallowing in patients with Parkinson disease showed that a delayed initiation of the pharyngeal swallow and a reduced hyolaryngeal excursion were predictors of penetration-aspiration (11). The prognosis regarding dysphagia in a patient with Parkinson disease improves with the effective management of the primary disease. In a patient with advanced Parkinson disease or amyotrophic lateral sclerosis and stage 5 dysphagia, the prognosis is poor.

Dysphagia is a prevalent motor symptom of Huntington disease and increases morbidity and mortality of the affected persons. In a study of clinical evaluation of Huntington disease, Bedside Swallowing Assessment Scale (BSAS) was used and Dysphagia Outcome and Severity Scale was applied for a preliminary classification of swallowing difficulties (09). The BSAS scores indicated that in this Huntington disease cohort, 32.4% presented with relevant or severe dysphagia.

Dysphagia in frontotemporal lobar dementia indicates deficits in cortical and subcortical pathways connecting with the brainstem swallowing center and indicates progression of lesions to brainstem systems.

Risk factors for dysphagia following anterior cervical spinal surgery include the use of anterior cervical plate, more than 1 surgical level, the upper surgical level at C3/4, and the use of bone morphogenetic protein-2 (23). Apart from trauma to the esophagus during anterior spinal surgery, dysphagia is a complication of other neurosurgical procedures, for example, manipulation of the brainstem during posterior fossa surgery. Dysphagia is reported in 15% to 17% of cases after removal of tumors of the posterior cranial fossa and may cause postoperative complications such as bronchopulmonary aspiration (13).

Dysphagia is common in multiple sclerosis and usually involves oral and pharyngeal phases of swallowing, although upper esophageal sphincter dysfunction can also occur. Early detection of dysphagia is important to prevent aspiration in these patients.

A follow-up of patients with severe traumatic brain injury showed that swallowing improved and the number of aspirations decreased between 3 and 6 months after injury (42). Prognostic factors for persisting aspiration included neurologic impairment, alteration in tongue control, and loss of oropharyngeal reflex.

Complications of dysphagia are dehydration, weight loss, airway obstruction, and aspiration pneumonia, the latter being the most serious. Among stroke survivors in the United States, approximately 100,000 individuals per year develop aspiration due to dysphagia.

Aspiration pneumonia. Aspiration occurs secondary to dysphagia and is defined as penetration or inhalation of either food or oropharyngeal contents below the level of the vocal cords. It may occur soon after the food is placed in the oral cavity or during the act of swallowing; it may be an event unrelated to swallowing such as aspiration of vomited or regurgitated material. Occasionally, ingested food is retained in pharyngeal recesses or "pockets" and is aspirated into the pulmonary tree when respiration is resumed after completion of the act of swallowing. Chronic aspiration is common in patients with some neurologic conditions and in chronically intubated patients. Macroaspiration occurs when large amounts of foreign material are inhaled, and microaspiration occurs when minute amounts are inhaled. Chronic aspiration is most often secondary to microaspiration.

Aspiration pneumonia is a significant cause of morbidity and mortality in neurologic patients with dysphagia. Although there are many predisposing factors for developing aspiration pneumonia, there is a strong association between dysphagia and the development of aspiration pneumonia.

Biological basis

	• Swallowing involves a larger neural network that includes the anterior insula and cerebellum.
	• Dysphagia can be due to mechanical or neuromuscular causes, and the latter is more relevant to neurologic disorders.

Anatomic localization

Swallowing is a sequential, semiautomatic contraction and relaxation of the 55 muscles of the oropharyngeal, laryngeal, and esophageal regions, which are innervated by 6 cranial nerves and 2 cervical nerve roots. Although numerous processes, both voluntary and reflex, are required for normal swallowing, conventional models of the central control of swallowing only describe the involvement of the bulbar swallowing center in the brainstem and the inferior precentral gyrus. This concept does not explain why neurologic disorders involving other brain regions also cause dysphagia. To determine the brain regions participating in voluntary swallowing, regional cerebral blood flow studies with positron emission tomography have been conducted during swallowing in healthy human subjects. The findings indicate that swallowing involves a larger neural network that includes the anterior insula and cerebellum. The anterior insula has connections with the primary and supplementary motor cortices, the ventroposterior medial nucleus of the thalamus, and the nucleus tractus solitarius; all of these are involved in oropharyngeal swallowing. Therefore, lesions of the anterior insula may disrupt these connections and produce dysphagia. Invasive electroencephalographic monitoring and stimulation in a patient with intractable seizures showed that the right posterior insular cortex is involved in the neural circuitry underlying the control of swallowing (40). Magnetoencephalography shows that the posterior parietal cortex is involved in the central coordination of swallowing, and there is strong bilateral reduction of cortical activation on dysphagic patients with hemispheric stroke as compared to nondysphagic patients. However, there is right hemispheric lateralization of activation in brainstem stroke, which has been interpreted as cortical compensation of subcortically caused dysphagia in the early subacute phase (41).

Vagal afferent sensory endings from the distal esophagus terminate in the nucleus tractus solitarius. The preganglionic motor innervation of the lower esophagus arises from the dorsal motor nucleus of the vagus. Together these nuclei comprise the dorsal vagal complex, wherein there is a neural network coordinating reflex control of the sphincter at the lower end of the esophagus. Vagal efferent preganglionic neurons to the gastrointestinal tract have a viscerotopographic representation in the dorsal motor nucleus of the vagus. Stimulation of the dorsal motor nucleus of the vagus caudal to the opening of the fourth ventricle results in relaxation, whereas stimulation in the rostral portion of the nucleus evokes contractions of the lower esophageal sphincter. The motor vagal preganglionic output is primarily cholinergic, which ultimately stimulates excitatory or inhibitory motor neurons that control the smooth muscle tone. Excitatory neurons evoke muscarinic receptor-mediated muscle contraction. Inhibitory neurons evoke nitric oxide or vasoactive intestinal polypeptide-mediated relaxation of the lower esophageal sphincter. However, other neurotransmitters are found in vagal preganglionic neurons, including norepinephrine, dopamine, and nitric oxide. A subpopulation of nitric oxide synthase-containing vagal preganglionic neurons innervates the upper gastrointestinal tract and mediates relaxation.

Involvement of the excitatory and inhibitory corticobulbar fiber systems linked with the bulbar swallowing center is mainly responsible for the triggering difficulties of the swallowing reflex and for the hyperreflexic or incoordinated nature of the cricopharyngeal sphincter.

Pathophysiology

To describe the pathophysiology, dysphagia can be divided into mechanical and neuromuscular causes, as shown in Tables 1 and 2. Neuromuscular dysphagia is more relevant to neurology.

Neuromuscular dysphagia. Neuromuscular dysphagia is also called motor dysphagia. It results from the difficulty of swallowing or from abnormalities of propulsion of the bolus due to diseases of the muscles of the pharynx and the esophagus. Peristalsis in the striated muscle segment of the esophagus, innervated by the somatic component of the vagus with cell bodies of the lower motor neurons located in the nucleus ambiguus, is due to coordinated activation of muscles at different levels along the esophagus. Neuromuscular disorders due to motor neuron lesions can cause muscle paralysis, simultaneous nonperistaltic contraction, and failure of the opening of the upper esophageal sphincter.

Disorders of the smooth muscle, innervated by the parasympathetic component of the vagus with postganglionic neurons in the myenteric plexus, involve the lower esophagus and the lower esophageal sphincter. A defect in the inhibitory vagal innervation may result in a dearth of this segment and impaired relaxation of the lower sphincter, resulting in dysphagia.

Transgenic mouse models of amyotrophic lateral sclerosis are useful for understanding the pathomechanisms of dysphagia. The findings indicate that pharyngeal dysphagia may be attributed to both motor and sensory pathologies, suggesting that sensory stimulation approaches may facilitate swallowing function.

Table 1. Mechanical Causes of Dysphagia

Intrinsic obstructions of the oropharynx and esophagus
Inflammatory conditions
	• Pharyngitis • Esophagitis
		- Infections - Eosinophilic esophagitis - Chemical and thermal injury
Esophageal strictures
		- Congenital lesions - Secondary to inflammatory lesions - Secondary to peptic ulceration - Postoperative - Postintubation - Postirradiation
Lower esophageal contractile muscular ring Esophageal tumors
Extrinsic compression of the esophagus
Osteophytes in cervical spondylosis Diffuse idiopathic skeletal hyperostosis Retropharyngeal abscess Enlarged thyroid gland Extracranial carotid artery aneurysms Posterior mediastinal masses Head and neck cancer Tortuous common carotid artery Atherosclerotic dilated aortic diverticulum in a mirror-image right aortic arch
Narrowing of the oropharyngeal space from extrinsic compression
Decrease of the occipito-cervical angle by hyperflexion of the upper cervical spine following occipito-cervical fusion operation (15).

Table 2. Causes of Neuromuscular Dysphagia

Difficulty in initiating swallowing
	• Lesions of the swallowing center • Lesions of the brainstem involving nuclei of lower cranial nerves
		- Basilar artery aneurysms - Brainstem neoplasms - Brainstem injuries - Brainstem dysfunction associated with Chiari malformation - Ischemic syndromes involving the brainstem, eg, Avellis syndrome (ischemia of lateral medulla oblongata), pontine infarction
Cranial nerve lesions
	• Lesions of the sensory components of vagal and glossopharyngeal nerves • Lesion of the motor component of glossopharyngeal nerve: paralysis of the tongue • Ramsay Hunt syndrome (07) • Multiple cranial nerve palsies
Degenerative neurologic disorders
	• Alexander disease • Amyotrophic lateral sclerosis • Cortical-basal ganglionic degeneration • Frontotemporal lobar dementia • Huntington disease (14) • Machado-Joseph disease • Multiple sclerosis • Parkinson disease • Wilson disease
CNS trauma
	• Traumatic brain injury • Cervical spine injury
Lower motor neuron lesions: poliomyelitis Upper motor neuron lesions: pseudobulbar paralysis Disorders of the autonomic nervous system: pandysautonomia Peripheral neuropathies
	• Inflammatory systemic neuropathies • Diabetic neuropathy
Neuromuscular disorders: myasthenia gravis (03) Muscle disorders
	• Inclusion body myositis • Myopathies • Myotonic dystrophy • Oculopharyngeal muscular dystrophy • Facioscapulohumeral muscular dystrophy
Movement disorders
	• Oromandibular dystonia
Miscellaneous neurologic disorders
	• Ataxia telangiectasia • Cerebral palsy • Critical illness neuropathy • Gaucher disease Type 2 • Hyperventilation syndrome • Intellectual disability • Niemann-Pick disease • Paraneoplastic sensory neuronopathy • Rabies • Subacute spongiform encephalopathy • Subacute necrotizing encephalomyelopathy
Local anesthetic application in oropharynx Complications of surgical procedures
	• Cervical spine surgery by anterior approach • Posterior fossa surgery (46) • Hemispherectomy for epilepsy • Palatoplasty • Vagotomy and pyloroplasty
Drug-induced neurologic disorders with dysphagia
	• Botulinum toxin therapy • Phenytoin toxicity • Neuroleptic malignant syndrome • Antipsychotic-induced movement disorders: tardive dyskinesia
Disorders of esophageal muscles
	• Intestinal pseudo-obstruction syndrome • Malignant disease • Chagas disease • Muscle disorders induced by toxins and drugs

Disruption of cortical control of swallowing. Transient dysphagia due to impairment of cortical control of swallowing is a frequent complication of hemispherectomy for intractable epilepsy in pediatric patients (05).

Dysphagia as a complication of cervical spine surgery by anterior approach. In a prospective study, the incidence of dysphagia was 22% within 12 months after anterior cervical discectomy and interbody fusion (28). None of these was severe.

Postintubation dysphagia. Postextubation dysphagia is a burden on patients in intensive care units. Over half a million patients in the United States survive mechanical ventilation during critical care annually. A major concern is aspiration leading to the development of aspiration pneumonia when patients resume oral feeding (04). Screening for aspiration with a water swallow test has been reported to be positive for 12% of patients in the intensive care unit after extubation.

Critical illness neuropathy. Dysphagia diagnosed by fiberoptic endoscopy is common and transient in critical illness polyneuropathy (32).

Epidemiology

	• Dysphagia occurs frequently in the elderly in nursing homes, particularly those with stroke and Parkinson disease.
	• Dysphagia is the main causes of pneumonia in the elderly.

It is estimated that 400,000 to 800,000 individuals worldwide develop neurogenic dysphagia per year. The prevalence of dysphagia in the otherwise healthy general population is difficult to determine, but it occurs in 44% to 50% of persons in nursing homes, and it is 1 of the main causes of pneumonia in the elderly. Dysphagia occurs in more than 30% of elderly stroke patients, 52% to 82% of those with Parkinson disease, 60% following treatment of head and neck cancer, and 84% of patients with Alzheimer disease (36). The prevalence of dysphagia is reported to be 30% to 100% of individuals depending on the type of motor neuron disease and the stage of disease and affects all individuals in the later stages of the disease. A systematic review of prevalence of dysphagia in persons with intellectual disability showed it to be associated with more severe levels of intellectual disability, comorbid cerebral palsy, and motor impairments (35). Further studies are needed for precise prevalence figures.

Differential diagnosis

The first step in differential diagnosis is the distinction between mechanical and motor dysphagia. Historical findings of the physical examination and diagnostic procedures usually provide enough information to make this distinction. From a neurologic point of view, the differential diagnosis is among various causes of neuromuscular dysfunction leading to swallowing initiation difficulties. Most of the diseases listed have distinct neurologic features. If neurologic disorders have been ruled out, the following 2 conditions should be considered in the differential diagnosis:

Globus pharyngeus. Globus pharyngeus is the sensation of a lump or tightness in the throat. The symptom is considered functional if no organic explanation is detected. The diagnostic criteria are the persistence of the sensation of a lump for at least 12 weeks during the preceding 12 months, occurrence of sensation between meals, absence of dysphagia or odynophagia, and absence of a motility disorder of the upper gastrointestinal tract.

Phagophobia. Patients present with either acute or chronic dysphagia secondary to fear of swallowing. Head and neck examination, standard barium swallow study, and oropharyngeal swallowing videofluoroscopy do not reveal any abnormality.

Associated or underlying disorders

These are described as causes of dysphagia in previous sections.

Diagnostic workup

	• Basic laboratory studies and chest x-rays for detection of aspiration pneumonia.
	• Toronto Bedside Swallowing Screening Test
	• Barium swallow and esophageal motility studies for mechanical dysphagia
	• Pharyngoesophageal manometry
	• Endoscopy
	• Laryngeal electromyography
	• Brain imaging

All patients with dysphagia should be thoroughly investigated to find the cause, because the treatment depends on the cause. Basic studies include blood counts and chemistry. Plain x-rays of the head, neck, and chest can provide useful information, such as evidence of aspiration pneumonia.

A typical clinical assessment starts with swallowing sips of water; observations include timing of swallow, laryngeal elevation, and signs of aspiration before, during, or after swallowing. For further testing, 100 ml of water is offered to assess continuous swallowing and the same observations are made together with the rate and total volume managed and the unswallowed residual. The water swallow item alone does not identify all patients with dysphagia. For a water swallow to accurately identify dysphagia, it is critical to administer 10 teaspoons according to the protocol of TOR-BSST (Toronto Bedside Swallowing Screening Test), with the result that the screening score becomes more accurate and reliable (24). Bedside tests for dysphagia in conditions such as stroke are easy to perform but have variable sensitivity, specificity, and interrater reliability. They are poor at detecting silent aspiration.

If mechanical dysphagia is suspected from the history and physical examination, the special diagnostic procedures of choice are barium swallow, esophagogastroscopy, and endoscopic biopsy. Barium swallow and esophageal motility studies are indicated for motor dysphagia. Brief comments on the use of these procedures are:

Videofluoroscope of barium swallow. A liquid barium swallowing study is a standard diagnostic procedure. This can be supplemented with soft and chewable boluses mixed with barium. This helps to determine whether the patient can best tolerate liquids, soft foods, solid chewable boluses, or none of these. Dynamic videofluoroscopic swallow studies enable fast and accurate recording of deglutition events. Videofluoroscopy helps in the classification of the degree of dysphagia that guides the dietary management of each neurologically compromised patient. A functional dysphagia scale, based on a videofluoroscopic swallowing study in stroke patients, is a sensitive and specific method for quantifying the severity of dysphagia in stroke patients.

Pharyngoesophageal manometry. Pharyngoesophageal manometry involves placing a small diameter flexible tube into the patient's pharynx and esophagus through the nose or the mouth under local anesthesia. Contraction pressures are measured through the manometry tube while the patient is asked to perform dry as well as wet swallowing. It is possible to determine the primary pathology that is causing the patient's dysphagia by analyzing the manometry results. Manometric studies have shown that presence of aperistalsis or multiple simultaneous contractions in the esophagus does correlate with dysphagia and is independent of Parkinson disease severity or duration. This may reflect selective involvement of either the dorsal motor nucleus of the vagus or the esophageal myenteric plexus.

Endoscopy. Flexible fiberoptic endoscopes are used for evaluation of swallowing both fluids and solids and can explore the pharynx, esophagus, and the stomach. These can be combined with sensory testing of oropharynx by using a technique that determines the sensory discrimination thresholds by endoscopically delivering air-pulse stimuli to the mucosa innervated by the superior laryngeal nerve. Biopsy may be done through the endoscope if required.

Because clinical screening alone is not sufficient to identify patients at risk for aspiration pneumonia, flexible endoscopic evaluation of swallowing should be used at a low threshold in cases of severe stroke and other symptoms, especially isolated dysarthria and cough after swallowing water (22).

Electrophysiological studies. Laryngeal electromyography can be used to investigate disorders of the pharyngeal phase of swallowing. The responses from the thyroarytenoid muscles, the cricothyroid muscles, and the cricopharyngeus muscle can provide useful information for the diagnosis, prognosis, and treatment of dysphagia. Other useful information includes the records and measures of the oropharyngeal swallowing patterns: triggers of voluntarily initiated swallows, duration of laryngeal relocation time, and total duration of oropharyngeal swallowing.

Mylohyoideus muscle contraction is an important component of the initial step in swallowing. Electromyographic recording of mylohyoideus muscle activity can reveal the number of asynchronisms. The occurrence of 1 or more long-lasting asynchronisms or of at least 6 asynchronisms during a sequence of 10 successive swallows should be considered abnormal. Surface electromyography may be used as a screening method for optimal patient management but not for proper investigation of neurogenic dysphagia (44). Bulbar electromyography is used for assessment of neurogenic dysphagia (33).

Brain imaging. Brain imaging is important in some situations. A study has shown that real-time MRI as well as videofluoroscopy can identify the cause of dysphagia in inclusion body myositis with the advantages of better visualization of soft tissue (27).

Precise infarct localization by diffusion-weighted MRI has shown that ischemic stroke in the pons, eg, in the upper part of the pons and in the anterolateral vascular territory occurred more often in the patients who developed dysphagia (21).

Staging of dysphagia. A functional outcome swallowing scale, which is still in use, was devised for patients with oropharyngeal dysphagia to determine the severity of the disorder and the effectiveness of therapy or outcome (37). The following are various stages of this scale:

• Stage 0: normal function and asymptomatic. • Stage 1: normal function but symptomatic. • Stage 2: compensated abnormal function manifested. • Stage 3: decompensated abnormal function with weight loss of up to 10% or aspiration. • Stage 4: severely decompensated function with weight loss of more than 10% or severe aspiration with bronchopulmonary complications. • Stage 5: dysphagia severe enough to require nonoral feeding.

The O'Neil severity graduation scale correlates imaging and patients' symptoms, and a preliminary assessment according to this scale is used to plan treatment of mild, moderate, and severe dysphagia associated with multiple sclerosis (12).

Management

	• Management of dysphagia is considered according to the cause.
	• If primary cause can be corrected or has a good prognosis for recovery, supportive care may be required until the patient can swallow normally.
	• Other options for persistent dysphagia include nutritional support, medical treatment, surgery, or rehabilitation.

Most dysphagia cases due to mechanical causes are treated by gastroenterologists and surgeons. Management decisions for dysphagia in neurologic patients are influenced by several factors, eg, whether the primary condition of the patient has any possibility of improving or if the management should take the form of nutritional support, medical treatments, surgery, or rehabilitation.

Treatment of drug-induced dysphagia. This is usually relieved by discontinuation of the offending drug. A case of phenytoin-induced dysphagia with lack of velopharyngeal coordination and nasopharyngeal reflux combined with massive palatine tonsillar hypertrophy was relieved by discontinuation of phenytoin (16). However, sufficient time should be allowed for lymphoid hypertrophy to resolve resolution before considering surgery.

Compensatory measures for nutrition. It should be determined whether the food can be given safely by mouth or needs to be given via enteral or parenteral routes. The decision regarding oral feeding is influenced by episodes of aspiration during eating and development of pneumonia. If a patient has only infrequent episodes of aspiration and is able to maintain weight, oral feeding may be continued. If oral intake is inadequate, compensatory strategies may be used. These include postural adjustment during feeding and use of liquid diet if there is difficulty in swallowing solids.

A nasogastric tube is commonly used for parenteral nutrition. Nasogastric tubes offer only limited protection against aspiration pneumonia in patients with dysphagia from acute stroke. Improperly placed nasogastric tubes can interfere with normal swallowing, but a correctly placed nasogastric tube does not cause worsening of stroke-related dysphagia (10). Based on this observation, limited and supervised oral feeding may be started in stroke patients with a nasogastric tube in place. In severe cases, parenteral nutritional support using percutaneous endoscopic gastrostomy may be required if the patient is unable to swallow. For dysphagic stroke patients, feeding by percutaneous endoscopic gastrostomy may improve outcome and nutrition as compared to nasogastric tube. It is difficult to compare results of clinical trials in this area as methodology and endpoints are not uniform. In addition to management of dysphagia, the nutritional status of stroke patients should be assessed, and adequate food as well as fluid intakes should be maintained.

Medical treatments. Pharmacological treatment of dysphagia associated with neurologic disorders is limited. Benzodiazepines, antidepressants, and spasmolytic agents have been tried without success in patients with dysphagia following brainstem stroke, but nitroglycerin may be helpful. Improvement can occur if the underlying cause can be treated. Dysphagia associated with tardive dyskinesia can be improved by using pharmacological agents to treat dyskinesia or by discontinuing the offending drug responsible for dyskinesia.

Imidapril, an angiotensin-converting enzyme inhibitor, has been shown to improve dysphagia and prevent aspiration pneumonia in the elderly patients. Nicergoline may improve dysphagia by upregulating substance P as impaired substance P secretion is associated with dysphagia (25).

A systematic review of randomized clinical trials showed that there is insufficient and low-quality evidence to determine the effect of interventions for dysphagia in long-term, progressive muscle disease (19). Clinically relevant effects of intravenous immunoglobulin for dysphagia in inclusion body myositis can neither be confirmed nor excluded using the evidence presented in this review.

Botulinum toxin therapy may be useful for cricopharyngeal dysphagia. It should be noted that dysphagia is also a complication of botulinum therapy applied to jaw muscles. A study has shown that botulinum toxin A is effective in improving dysphagia in patients with amyotrophic lateral sclerosis with upper esophageal sphincter hyperactivity without lower motor neuron involvement (34). Botulinum toxin has also been reported to be beneficial for treatment of dysphagia in oculopharyngeal muscular dystrophy, but there is a dose-related risk of dysphonia following injection of the cricopharyngeus muscle (49).

Surgery. Several surgical procedures have been used to improve swallowing in selected patients with neuromuscular dysphagia: vocal fold augmentation or medialization, cricopharyngeal myotomy, laryngeal suspension, intrahyoid myotomy, lateral thyrolaminectomy, and tracheoesophageal separation procedures. The best known of these is cricopharyngeal myotomy, which involves cutting the cricopharyngeal muscle to relax the upper esophageal sphincter permanently. It has been reported to be successful for patients with dysphagia due to inclusion body myositis. Dysphagia due to anterior cervical osteophytes is relieved after resection of the osteophytes via an anterolateral, extrapharyngeal approach. Dysphagia as a complication of anterior cervical interbody fusion with implantation of devices, such as anterior cervical plates, improves following removal of these devices.

Brain stimulation. Deep brain stimulation of the subthalamic nucleus may improve swallowing in Parkinson disease. Noninvasive brain stimulation, eg, transcranial magnetic stimulation and transcranial direct-current stimulation (tDCS), have been applied experimentally for the treatment of poststroke dysphagia. Although significant results were achieved in most studies in swallowing rehabilitation, it is still difficult to draw conclusions for the efficacy of these neurostimulation techniques, considering the great disparities between studies (48).

Neuromuscular stimulation for management of dysphagia. Several devices are available commercially:

	• VitalStim® Therapy System is an adjunctive to traditional exercises and combines electrical stimulation with the benefits of swallowing exercises.
	• Device for Neuromuscular Electrical Stimulation is an FDA-approved therapy for the treatment of dysphagia featuring 2 channels of stimulation and a wide range of stimulation intensities.
	• Effective Swallowing Protocol, an FDA-approved device, is based on most effective electrical stimulation parameters. It includes a portable powered muscle stimulator with easily adjustable parameters.

A systematic review of randomized controlled trials found that neuromuscular electrical stimulation coupled with traditional swallowing therapy could be an optional intervention to improve swallowing function after stroke in a rehabilitation department (01).

Rehabilitation. During the last decade, speech language pathologists have started to take an interest in the management of services for patients with oropharyngeal dysphagia. Rehabilitation is considered for patients who have a potential for improvement and should be conducted under the supervision of a speech therapist or swallowing therapist. Various rehabilitation measures include the following:

	• Normal swallowing, which can be achieved by simple coaching even with complete anesthesia of the pharyngeal mucosa.
	• Rehabilitation focuses on partial or complete restitution of disturbed functions, and the combination of mechanical, thermal, and gustatory stimuli seems to be more efficient (29). For example, effortful swallowing exercise is indicated for patients with an impaired tongue base retraction or reduced pharyngeal propulsion, and stimulating the anterior faucial pillars effectively triggers the swallowing reflex.
	• Oromotor exercises.
	• Facio-oral tract therapy has been shown to produce a significant increase in alertness and swallowing ability.
	• Vocal cord adduction exercises for patients who are prone to aspirate.
	• Thermal sensitization therapy that is designed to sensitize the posterior pharynx to cold stimulation and trigger the pharyngeal phase of swallowing.
	• The ability to slow and reduce the volume taken per swallow may be advantageous in patients with dysphagia where inappropriately judged intake might be a factor in the development of aspiration.
	• Suprahyoid muscle strengthening exercises are effective in restoring oral feeding in some patients with failure of deglutition because of abnormal upper esophageal sphincter opening.
	• Submental transcutaneous electrical stimulation applied during swallowing has been shown to improve swallowing function in patients with chronic neurologic disorders (45).
	• Stimulation of the external auditory canal with ointment containing capsaicin improves swallowing function in elderly patients with nonobstructive dysphagia by inducing cough reflex, which has been shown to prevent aspiration pneumonia (20).

Several methods have been used in managing dysphagia during the rehabilitation of stroke patients. Biofeedback may be effective, but it is time and labor-intensive. Short-term sensory stimulation of the pharynx, which induces long-term reorganization in human motor cortex, has also been shown to improve poststroke swallowing. Pharyngeal electrical stimulation reverses swallow disability caused by stroke-induced lesions in the motor cortex. However, there is no evidence that plasticity is facilitated by this technique. Results of a study confirm that laryngopharyngeal neuromuscular electrical stimulation in poststroke patients with dysphagia improves outcome of the conventional dysphagia training (38).

Most patients with chronic progressive neurodegenerative diseases are unlikely to respond to pharyngeal electrical stimulation. Changing the form of foods and training in rehabilitation techniques such as the chin down posture, supraglottic swallowing, and ice massage of the oral region may be effective for dysphagia in patients with Parkinson disease. A systematic review of effects of therapy for dysphagia in Parkinson disease is inconclusive because most studies cannot be compared with one another due to heterogeneous methods of treatment and outcome measures (02).

Future of dysphagia management. There is need for improvement in rehabilitation of patients with dysphagia due to neurologic disorders. Effective management of dysphagia requires a multidisciplinary approach. Efforts are being made to translate concepts of neural plasticity into the clinical science of rehabilitation for oropharyngeal swallowing disorders. Novel treatment paradigms have leveraged poststroke neuroplastic improvements using neurostimulation and biofeedback techniques (18). Initial promising results of experimental studies show potential for the use of stem cell-based regenerative therapies to treat oropharyngeal dysphagia and warrant further research (43). Future advances will be based on swallowing physiology and continuous refinement of treatments, particularly in the acute stage.