Neurogenic dysphagia: What is the cause when the cause … · Neurogenic Dysphagia: What Is the...

Dysphagia 9:245-255 (1994) Dyspha a �9 Springer-Veflag New York Inc. 1994

Neurogenic Dysphagia: What Is the Cause When the Cause Is Not Obvious?

David W. Buchholz, MD The Johns Hopkins University School of Medicine; Neurological Consultation Clinic, The Johns Hopkins Outpatient Center; and The Johns Hopkins Swallowing Center, Baltimore, Maryland, USA

Abstract. The potential causes of neurogenic oropharyngeal dysphagia in cases in which the underlying neurologic disorder is not readily apparent are discussed. The most common basis for unexplained neurogenic dysphagia may be cerebrovascular disease in the form of either confluent periventricular infarcts or small, discrete brainstem stroke, which may be invisible by magnetic resonance imaging. The diagnosis of occult stroke causing pharyngeal dysphagia should not be overlooked, because this diagnosis carries important treatment implica- tions. Motor neuron disease producing bulbar palsy, pseudobulbar palsy, or a combination of the two can present as gradually progressive dysphagia and dysarthria with little if any limb involvement. Myopathies, especially polymyositis, and myasthenia gravis are potentially treatable disorders that must be considered. A variety of medications may cause or exacerbate neurogenic dysphagia. Psychiatric disorders can masquerade as swallowing apraxia. The basis for unexplained neurogenic dysphagia can best be elucidated by methodical evaluation including careful history, neurologic examination, videofluoroscopy of swallowing, blood studies (CBC, chemistry panel, creatine kinase, B12, thyroid screening, and anti-acetylcholine receptor antibodies), electromyography, and magnetic resonance imaging (MRI) of the brain, plus additional procedures such as lumbar puncture and muscle biopsy as indicated. Little is known about aging and neurogenic dysphagia, specifically the relative contributions of natural age-related changes in the oropharynx and of diseases of the elderly, including periventricular MRI abnormalities, in produc-

Correspondence to: David W. Buchholz, M.D., The Johns Hopkins University School of Medicine, 601 N. Caroline St., Room 5072A, Baltimore, MD 21287-0876, USA

ing dysphagia symptoms and videofluoroscopic abnormalities in this population.

Key words: Neurogenic dysphagia - - Oropharyngeal dysfunction - - Videofluoroscopy - - Deglutition - - Deglutition disorders

Neurogenic dysphagia is difficulty swallowing as a result of neurologic disease. Although neurologic disease may adversely affect esophageal function, the symptoms and complications of neurogenic dysphagia almost always arise from sensorimotor impairment of the oral and pharyngeal phases of swallowing. Oropharyngeal dysphagia can also be caused by structural problems such as postin- tubation edema, laryngeal webs, and pharyngeal masses, but the vast majority of cases of chronic oropharyngeal dysphagia are neurogenic.

Recognizing the presence of neurogenic dysphagia is usually not too difficult in a patient with a known neurologic disorder. The typical symptoms and signs include difficulty managing oropharyngeal secretions, choke/cough episodes while eating, food sticking in the throat, nasal regurgitation, and dysphonia or dysarthria [11.

Occasionally, neurogenic dysphagia is more subtle and insidious. Compensation, both voluntary and involuntary, may enable a patient to minimize overt difficulty in swallowing [2]. Laryngeal penetration and aspiration may occur silently, without producing choke/ cough episodes, as a result of diminution of the cough reflex [3,4]. The cough reflex may be diminished because of laryngeal sensory loss related to the underlying neurologic disease. Or, there may be desensitization of the reflex in the face of chronic laryngeal stimulation (i.e., chronic aspiration). Other factors such as intuba-

246 D.W. Buchholz: Neurogenic Dysphagia

tion, tracheostomy, medications (local anesthetics and central nervous system depressants), and decreased level of consciousness may compromise the cough reflex. Ac- cordingly, the threshold for suspecting swallowing dysfunction in neurologically impaired patients should be low, lest a critical event such as aspiration pneumonia or asphyxia herald the existence of previously unrecognized neurogenic pharyngeal and laryngeal dysfunction.

Some patients with unsuspected neurologic ill- nesses have dysphagia as a primary presenting symptom, and, in these cases, the role of neurogenic oropharyngeal dysfunction in causing dysphagia may go unrecognized. Often in these cases, attention is mistakenly directed to the esophagus and to structural rather than functional impairment. In order to establish correctly the neurogenic basis for dysphagia in these patients, clinicians must recognize the clinical characteristics of oropharyngeal, as opposed to esophageal, dysphagia. Ultimately, videofluoroscopy of swallowing provides conclusive evidence of neurogenic oropharyngeal dysfunction such as nasal regurgitation, decreased pharyngeal peristalsis, pharyngeal retention, and aspiration [5-16]. Even these straightforward clues to a neurogenic problem are sometimes misin- terpreted, for example, as being attributable to cervical spine disease [17].

This paper addresses the possible causes of neurogenic dysphagia in those patients who present with oropharyngeal dysphagia yet have no obvious neurologic cause for it. The diagnostic considerations discussed are those that have become familiar to the author, a neurolo- gist, over the course of 12 years of evaluating patients referred to the Johns Hopkins Swallowing Center, including many patients who have been found to have neurogenic oropharyngeal dysphagia but who had initially presented without a preestablished neurologic diagnosis. Excluded from this review are many important neurologic causes of dysphagia, such as traumatic brain injury, overt stroke, Alzheimer's disease, Parkinson's disease, and movement disorders, because these conditions, when they cause dysphagia, are relatively clearcut diagnoses [18-21]. Instead, the issue at hand is the patient with unexplained, occult neurogenic dysphagia.

Cerebrovascular Disease

Whether it be cerebral or brainstem, ischemic or hemor- rhagic, a stroke sufficient to produce oropharyngeal dysfunction and dysphagia is usually a straightforward diagnosis because of its abrupt onset, associated neurologic findings within a definable vascular territory, presence of vascular disease risk factors, and gradual recovery of deficits [22-34]. In at least two ways, though, stroke may more obscurely cause dysphagia.

First, small vessel disease related to hypertension, diabetes mellitus, and aging often produces small "lacunar"-type infarcts deep in the brain, especially in the periventricular white matter tracts, which include the corticobulbar pathways. A very discrete infarct in this area may produce dysphagia as a sole or primary symptom by interrupting only those fibers responsible for cerebral control of swallowing [35]. The consequent dysphagia may be predominantly volitional, involving the oral phase of swallowing, because the brainstem pathways for the involuntary pharyngeal aspect of swallowing remain intact. Affected patients may therefore have difficulty initiating swallowing despite normal reflexive swallowing, and the distinction between this situation and psychogenic dysphagia can be difficult.

It is possible that a small, unilateral, periventricular lacunar infarct can cause dysphagia, although no study has yet been published in which the most sensitive imaging modality, magnetic resonance imaging (MRI), has been used to rule out bilateral disease [22,23,29,34]. Or, small periventricular infarcts may be bilateral and may accumulate in a gradually confluent fashion, in which case the history of dysphagia may be slowly progressive rather than stroke-like. In a sense, this is aforme fruste of pseudobulbar palsy, yet patients may lack the zypicaI features of that syndrome such as emotional labil- ity, exaggerated jaw jerk and gag reflex, and upper motor neuron signs in the limbs. In fact, neurologic examination is often remarkably normal in these patients, although signs such as facial weakness, dysphonia, dysarthria, or tongue weakness may be noted.

The most helpful diagnostic study is MRI of the brain [33,36]. This may show diffuse or multifocal in- creased T2 signal intensity in the periventricular white matter_ The difficulty with this MRI pattern is that it is commonly found in nondysphagic individuals who are elderly or who have a background of hypertension or diabetes [37,38]. Moreover, it is not clear that these periveutricular abnormalities represent infarction, although this is more likely when the abnormalities are confluent and when clinical findings are consistent with stroke. A report by Levine etal. [39] suggests that there is an association between the degree of periventricular white matter signal abnormality by MRI and the extent of oropharyngeal impairment, which is consistent with the hypothesis that confluent periventricular infarction causes oropharyngeal dysphagia, but further study is needed [40]. In many cases, the diagnosis of periventricular infarction causing oropharyngeal dysphagia can only be made with reasonable confidence after a thorough, negative search for other neurologic disorders and with the passage of time, over which the patient remains relatively stable or gradually improves.

The second type of stroke that can produce dys-

D.W. Buchholz: Neurogenic Dysphagia 247

phagia without the stroke being obvious is brainstem infarction that is small enough to cause little if any other dysfunction and to be nonvisualized by MR/. A group of l0 such patients has been reported by the author [41]. These patients had clinically probable brainstem strokes as evidenced by acute onset of oropharyngeal dysphagia, often accompanied by dysphonia or dysarthria, and a mixture of sufficient other brainstem signs to substantiate the diagnosis of brainstem stroke on clinical grounds, especially in the presence of risk factors for either small vessel disease, chiefly hypertension, or embolism, such as cardiac disease and aortic arch surgery. Cinepharyn- goesophagography confirmed bilateral pharyngeal motor dysfunction in all patients, yet routine brain MRI showed no intrinsic brainstem lesion in any of them.

Discrete hrainstem stroke involving either the "swallowing center" in the medulla or the nucleus ambiguus can evidently produce substantial pharyngeal dysphagia with little if any additional deficit other than dysphonia or dysarthria. This observation is contrary to the commonly held notion that brainstem stroke produces a multitude of symptoms and signs, as a result of the densely packed nuclei and tracts in the brainstem. Addi- tionally, although it is the best available imaging modality, MRI has limited resolution in the detection of very small strokes in the brainstem [42,43]. In the future, higher-resolution MRI scanners and perhaps pathologic correlation will probably help to better define this issue.

There are several reasons why it is important to recognize that otherwise-unexplained dysphagia may have been caused by stroke. First, proper management of oropharyngeal dysphagia can be instituted, such as tem- porary non-oral feeding followed by swallowing therapy. Second, unnecessary and sometimes risky diagnostic procedures such as esophagoscopy can be avoided. Third, if the stroke is recent, treatment such as blood pressure control and anticoagulation may be appropriate. Fourth, stroke risk factors can be controlled and anti- platelet or anticoagulant therapy can be administered to prevent future stroke.

Motor Neuron Disease

Motor neuron disease (MND), otherwise known as amyotrophic lateral sclerosis (ALS), causes idiopathic degeneration of upper and lower motor neurons throughout the central nervous system, including the brainstem. The disease progresses gradually over several years or more, and involvement is often initially focal. Consequently, the early stages of MND may result in isolated impairment of brainstem functions such as swallowing due to either lower motor neuron loss (bulbar palsy) or upper motor neuron degeneration (pseudobulbar palsy) [9, 44-46].

The features of bulbar palsy include lower motor neuron signs such as wasting and weakness of the involved muscles of the face, tongue, and pharynx, and decreased gag and jaw jerk reflexes. Pseudobulbar pa/sy, on the other hand, is characterized by weakness without wasting and by hyperactive brainstem reflexes. In addition to muscle weakness, there is often striking slowness and incoordination of voluntary motor functions, such as side-to-side movement of the tongue. Discrepancy between involuntary and voluntary motor functions may be blatant, with exaggerated rise of the soft palate as part of the gag reflex yet no movement during attempted phona- tion.

Pseudobulbar palsy often produces characteristic forms of speech and swallowing disturbance. Speech may be strained, slow, and "spastic." Dysphagia may predominantly relate to difficulty initiating swallowing, evidenced by both history and swallowing examination, because of impairment of volitional control with relative preservation of reflex activity. In other words, the oral preparatory and oral phases of swallowing may be selectively affected in pseudobulbar palsy, akin to swallowing apraxia, whereas the pharyngeal phase may proceed fairly normally once it is triggered. Finally, another clue to the presence of pseudobulbar palsy is emotional labil- ity (an excessive tendency to laugh and/or cry).

When MND presents predominantly as dysphagia, findings may reveal bulbar palsy, pseudobulbar palsy, or, most commonly, a mixture of the two. The diagnosis is often overlooked because specific neurologic findings may be scant in the face, tongue, and pharynx and nonexistent in the limbs. At times, even though the patient may be unaware of limb involvement, careful neurologic examination reveals subtle weakness, wasting, or reflex abnormalities. The emphasis of diagnosis should be to exclude other, treatable causes of neurogenic dysphagia, as discussed elsewhere in this paper. Positive test findings consistent with MND include mildly elevated creatine kinase (CK; a muscle enzyme that is released when muscles are denervated or damaged), electromyography (EMG) demonstrating diffuse acute and chronic denervation (especially if cranial nerve-supplied and paraspinal muscles are involved), and muscle biopsy revealing changes of denervation and rein- nervation (such as grouped atrophy and fiber type group- ing).

Treatment for MND remains supportive, although directions of clinical research include immunosuppression and inhibition of toxic-free radicals and exci- tatory neurotransmitters. Swallowing therapy is of limited benefit but may nonetheless he worth trying, and enteral tube feeding is often indicated, especially for those patients with severely impaired swallowing but relatively intact limb motor function.


Myopathy

Inflammatory Myopathies

Inflammatory myopathies such as polymyositis, dermatomyositis, and sarcoid myopathy typically produce suba- cute, diffuse proximal muscle weakness without pain, and most affected individuals are aware of limb impairment before dysphagia. Exceptions occur, and it is especially important to consider these disorders, as they are immune-mediated and can be effectively treated with immunosuppression [47-54]. Physical examination usually reveals diffuse, mainly proximal muscle weakness without wasting, reflex changes or sensory loss, and characteristic abnormal test findings include elevated sedimentation rate and CK, EMG showing irritable features, and muscle biopsy demonstrating inflammatory cell infiltrates and muscle fiber degeneration.

Muscular Dystrophies

Muscular dystrophies such as myotonic dystrophy and oculopharyngeal dystrophy cause dysphagia in middle- aged adults and in the elderly, but these diagnoses are usually straightforward because of other characteristic features and often, positive family history [10,55-61]. Mitochondrial myopathy takes many clinical forms, including gradually progressive, isolated pharyngeal weakness in adults, and potential treatment in the form of mitochondrial oxidative enzyme replacement may be possible in the future. These noninflammatory myopathies are diagnosed through a combination of measurement of CK, EMG, and muscle biopsy, the latter including electron microscopy and other special studies that can only be adequately performed by an experienced neuromuscular laboratory.

Endocrine disorders are associated with myopathy, but the underlying disorders are usually readily apparent on other grounds. Both hypo- and hyperthyroidism can cause pharyngeal muscle weakness [62]. Thyroid function tests should routinely be checked in the evaluation of neurogenic dysphagia. Steroid myopathy primarily affects proximal limb muscles but sometimes involves the pharynx and is more often due to an excess of exogenous steroids (corticosteroid therapy) than en- dogenous steroids (Cushing's disease). These endocrine myopathies are largely reversible with normalization of the hormonal imbalance.

Diseases of the Neuromuscular Junction

Myasthenia Gravis

This is an immune-mediated disorder affecting acetylcholine receptors located on muscle membranes at the

neuromuscular junction. Normally, muscle contraction is triggered when acetylcholine released from motor nerve terminals crosses the neuromuscular synapse and binds with its receptors. The muscle weakness of myasthenia gravis has a predilection for the eyes (resulting in ptosis and diplopia), pharynx, and proximal limbs, and it is often fatiguable. Accordingly, myasthenic dysphagia tends to be worse as feeding progresses and worse toward the end of the day [63,64]. Muscles of mastication may be involved, so that chewing can be difficult. The diagnosis of myasthenia gravis is secured by measurement of anti-acetylcholine receptor antibodies, a specialized form of EMG (repetitive nerve stimulation), and a positive response to anticholinesterase medication, which en- hances the action of acetylcholine at the neuromuscular junction. Myasthenia gravis is treatable not only with anticholinesterases but also immunosuppressants, such as corticosteroids, and removal of the thymus gland, which seems to be the source of the abnormal antibodies.

Eaton-Lambert Syndrome

Eaton-Lambert syndrome is clinically similar to myasthenia gravis but usually arises in the setting of an underlying malignancy, which may or may not be recognized. The malignancy stimulates production of antibodies against the sites of release of acetylcholine at the neuromuscular junction, and both treatment of the underlying malignancy and immune modulation may be effective. Electromyography (specifically, repetitive nerve stimulation) reveals a diagnostic pattern in Eaton-Lambert syndrome.

Botulism

This is a condition of acute, diffuse muscle weakness resulting from ingestion (or, less commonly, production within the body) of a neuromuscular junction toxin pro- duced by anaerobic bacteria, which most often have con- taminated improperly prepared food. Botulinum toxin has become useful as a therapeutic agent in the treatment of movement disorders, including head and neck dystonia that can cause dysphagia by virtue of either postural compromise or involvement of swallowing muscles [65- 69]. Ironically, injection of botulinum toxin into the involved muscles sometimes causes dysphagia, at least temporarily, presumably because the injected toxin spreads locally and weakens muscles such as the pharyngeal constrictors [70].

Neurodegenerative and Demyelinating Diseases

Most of the common neurodegenerative disorders that typically impair swallowing as they advance, such as


Parkinson's and Alzheimer's disease [14,71-76], are overt conditions that are unlikely to cause diagnostic confusion. Occasionally, patients with Parkinson-like disorders such as progressive supranuclear palsy develop pseudobulbar dysfunction as an early or primary feature of their illness, which is otherwise characterized by gradually progressive, idiopathic degeneration of multiple aspects of the central nervous system, including corticospi- naI tracts, cerebellar functions, and cognition [77]. Other neurodegenerative disorders that similarly affect multiple systems including the brainstem, such as olivopontocere- bellar atrophy, are uncommon and usually occur in the setting of a positive family history [8].

Multiple Sclerosis

This is an immune-mediated central nervous system disorder in which myelin, the insulating material around nerve fibers in the brain and spinal cord, is damaged. The disease follows many different patterns but often afflicts young adults in a relapsing-remitting form. It is highly unusual for multiple sclerosis to initially present as neurogenic dysphagia [78,79]. If dysphagia complicates multiple sclerosis, it almost always occurs in a patient with an established diagnosis who has had prior fluctuating sensory, motor, visual, or bladder symptoms. The diagnosis of multiple sclerosis is made based upon a combination of the characteristic fluctuating history and evidence from examination and laboratory studies of multifocal central nervous system involvement. Cere- brospinal fluid examination (looking for evidence of in- flammation and abnormal antibody production), evoked potentials (looking for slowing of conduction along central sensory pathways), and MRI (looking for multiple, often clinically silent areas of white matter involvement) are the most useful ancillary tests. Immunosuppressant treatment such as corticosteroid therapy is of limited benefit, and numerous alternative approaches are being ex- plored.

Vitamin B12 Deficiency

This causes a variety of neurologic and hematologic complications, including corticobulbar tract dysfunction leading to pseudobulbar palsy. In the evaluation of unexplained neurogenic dysphagia it is always worth checking a serum vitamin B 12 level and, if there is any doubt, a Schilling test for vitamin B 12 malabsorption.

Neoplasms

Base of Skull Tumors

Tumors such as nasopharyngeal carcinoma, clivus chor- doma, retropharyngeal lymphoma, and meningioma may

disrupt lower cranial nerves and thereby cause dysphagia. Local symptoms such as pain or abnormal nasal discharge may be present, and cranial nerve deficits are often unilateral. Otolaryngologic examination, imaging studies, and biopsy are the best ways to make the diagnosis. A combination of MRI with enhancement and com- puted tomography (CT) scanning is sometimes necessary in order to optimally visualize both soft tissue and bony changes. Treatment such as surgical debutking or radio- therapy may be effective.

Brainstem Tumors

These may selectively involve structures such as the nucleus ambiguus, nucleus tractus solitarius, or medullary "swallowing center" early in their course, thereby presenting as dysphagia [80]. Other brainstem findings are likely to develop as these lesions grow, and MRI with enhancement is the best diagnostic procedure. Non-neoplastic structural lesions of the brainstem and posterior fossa rarely present primarily with dysphagia and are similarly best detected by MRI [81-84].

Neoplastic Meningitis

This condition refers to the diffuse spread of tumor cells within the subarachnoid space, where lower cranial nerves may be consequently infiltrated and compressed. Patients usually, but not always, are known to have a primary tumor by the time neoplastic meningitis devel- ops, and the most common sources are carcinoma of the lung and breast and lymphoma. In addition to cranial nerve dysfunction, headache and depressed mental status frequently result. Diagnosis is secured by MRI with enhancement and cytopathologic examination of cerebrospinal fluid.

Infections

Chronic Meningitis

Chronic meningitis caused by infectious agents is clinically similar to neoplastic meningitis, and the comments made above apply here, although infection is more likely to also cause fever. Responsible microorganisms include fungi, mycobacteria, parasites, and others than are less common. Diagnosis is established by means of MRI with enhancement and cerebrospinal fluid studies including appropriate cultures. In recent years, infection with hu- man immunodeficiency virus (HIV) often underlies op- portunistic infections which cause chronic meningitis, and HIV may itself directly infect the brain and produce


dysphagia, but it is extremely unlikely to do so as a presenting manifestation.

Spirochetal Diseases

SpirochetaI diseases such as syphilis and Lyme disease can cause not only chronic meningitis but also infection of the central nervous system in a multitude of other forms, often years or decades after the initial illness, which may have been inapparent. Although these are uncommon causes of unexplained neurogenic dysphagia, they are worth checking with simple blood studies [fluo- rescent treponemal antibody (FrA) and Lyme disease antibodies, respectively], as antibiotic therapy can arrest if not reverse neurologic dysfunction caused by these chronic infections.

Postpolio Syndrome

This syndrome refers to gradually progressive muscle weakness, wasting, fatigue, and/or pain generally begin- ning several decades after recovery from acute poliomyelitis. It has numerous causes, including progressive post-polio muscular atrophy (PPMA), thought to be due to exhaustion of motor neurons that have been over- worked since they survived acute polio decades earlier and subsequently sprouted axons to reinnervate muscles during the recovery process [85]. Postpolio dysphagia, possibly related to progressive pharyngeal weakness, has been described [86-94]. The history of a patient with unexplained neurogenic dysphagia should include in- quiry into the possibility of polio or a polio-like illness in the distant past.

Iatrogenic Causes

Neurogenic pharyngeal dysphagia may be caused or ex- acerbated by medications or surgical procedures. The issue of medication-related oropharyngeal dysfunction is distinct from medication-induced esophagitis caused by agents such as tetracycline, potassium, iron, quinidine, and nonsteroidal antiinflammatory drugs [95,96].

The mechanisms of medications causing pharyngeal swallowing impairment include sedation, pharyngeal muscle weakness, movement disorders, sensory loss, and impaired salivation. Sedation is especially likely to result from benzodiazepines. Pharyngeal muscle weakness may result from neuromuscular blockade or myopathy. Neuromuscular blockade is associated with not only systemic medications such as aminoglycoside antibiotics and penicillamine but also local injection of botulinum toxin into neck muscles for treatment of torticollis and other focal dystonias [70]. Myopathy is asso-

ciated with many drugs including corticosteroids, colchi- cine, lipid-lowering agents, and L-tryptophan, the latter by means of the eosinophilia-myalgia syndrome [97].

Oropharyngeal sensory impairment is the inten- tion of local anesthetics used during procedures such as endoscopy, but swallowing may remain impaired post- procedure. Neuroleptics can produce movement disorders such as dyskinesias involving the mouth, tongue, and pharynx [98-102]. Finally, medications with anticholinergic properties tend to decrease salivation, which may interfere with bolus preparation [103].

Postsurgical neurogenic dysphagia has been associated with carotid endarterectomy, ventral rhizotomy for spasmodic torticollis, transhiatal esophagectomy, and anterior cervical spinal fusion [68,104--106]. The mechanisms are unclear but may involve intraoperative disrup- tion of the local neural input to pharyngeal and laryngeal muscles. If so, other operative procedures localized to the neck may have similar adverse consequences on swallowing function that have not yet been recognized.

Psychogenic Causes

Twenty-six patients with a distinct pattern of probable psychogenic oropharyngeal dysphagia have been seen at the Johns Hopkins Swallowing Center [107]. Many of these individuals were referred because prior evaluation had led to a suspicion of neurogenic dysphagia. The general characteristics of this group include (1) female gender, (2) young- to mid-adult age range, (3) com- plaints of difficulty initiating swallowing and/or food sticking in the throat, (4) absence of dysphagia complications other than weight loss, (5) absence of speech disorder and other neurologic symptoms, (6) occasionally marked fluctuation of dysphagia, (7) absence of stroke risk factors and other underlying diseases, (8) normal neurologic examination, (9) normal videofluoroscopy of swallowing other than complex, nonpropulsive tongue movements during attempted swallowing in 20 patients, and (10) normal neurologic studies including brain MRI performed in approximately one-half of the cases.

In short, these patients typically exhibited what appeared to be oral swallowing apraxia yet had intact pharyngeal function, speech, and neurologic function otherwise. This pattern can result from cortical lesions or as aformefruste of pseudobulbar palsy, but these situa- tions are rare. In the cases described, extensive evaluation yielded no evidence of neurologic disease, although various indicators of psychiatric disturbance were noted. Specific psychiatric considerations included anxiety, de- pression, hypochondriasis, somatoform disorder, con- version disorder, and eating disorder.

It should be emphasized that the diagnosis of


psychogenic dysphagia should not be made without thorough investigation. The globus symptom ("lump in the throat"), especially, is likely to have an identifiable and potentially treatable basis such as gastroesophageal reflux and/or esophageal dysmotility [108]. None- theless, the syndrome of isolated voluntary oromotor dysfunction, with intact pharyngeal performance, in a young adult without evidence of neurologic disease may indicate a treatable problem of psychogenic origin. Treatment should include psychotherapy, psychiatric medication as appropriate, and a behavioral modifica- tion program of supervised progressive feeding including desensitization of the fear of swallowing [109- 1111.

Age-Related Changes

Altered oropharyngeal function has been documented in asymptomatic elderly volunteers, although most of the available literature has evaluated abnormal individuals rather than normal elderly subjects [112-122]. These changes in oropharyngeal performance are probably due partly to normal, age-related changes in pharyngeal sup- porting tissues, muscles, and central and peripheral neural pathways.

Two points are less clear. The first is the extent to which this "normal" decline in oropharyngeal performance among elderly people is actually related to an accumulation of disease processes that are more common among the elderly, such as small vessel disease producing periventricular white matter damage evidenced by MRI signal abnormalities [39,40]. The elderly are also more likely to be affected by dental deficiencies, impaired salivation, diminished taste and smell sensation, medication side effects, and concurrent medical ill- nesses. Age-related oropharyngeai changes, even among ostensibly normal, asymptomatic volunteers, may represent a conglomeration of natural effects of aging plus disease-related factors. The potential contribution of disease must be diligently sought and, if possible, treated in elderly dysphagic patients, rather than assuming their problems to be secondary to aging.

The second unclear point is the extent to which routine age-related changes influencing the oropharynx, whether due to aging or disease (or both), can be symptomatic [123-128]. There is confusing overlap of the clinical, videofluoroscopic, and MRI findings of elderly individuals with and without overt dysphagia, with and without videofluoroscopic evidence of oropharyngeal dysfunction, and with and without periventricular MRI signal abnormalities. If we understood the interrelation- ships of these factors, we would know vastly more about neurogenic dysphagia than we do today.

Evaluation of Unexplained Neurogenic Dysphagia

As a/ways, careful history and physical examination are the most valuable diagnostic tools [129,130]. Sudden onset of oropharyngea/ dysphagia strongly suggests stroke, especially if there is subsequent, at least partial, recovery. Gradually progressive dysphagia and dysarthria over several months or more is ominously suggestive of motor neuron disease but is also compatible with other considerations such as inflammatory myopathy or base of skull tumor. Fluctuation of dysphagia over hours to days is consistent with myasthenia gravis, whereas a pattern of relapse and remission over weeks to months is compatible with multiple sclerosis. A careful medical history may reveal risk factors for stroke, clues to the presence of an underlying malignancy, or intake of medications that may be causing or contributing to pharyngeal dysfunction.

Neurologic examination should especially attend to the distinction between bulbar and pseudobulbar palsy. Other specific findings may either localize the problem, for example, to the brainstem or cranial nerves on one side, or characterize the problem by disease type, such as a stroke or a movement disorder.

Videofluoroscopy of swallowing is essential to determine the extent of oropharyngeal dysfunction and to help guide decisions regarding swallowing therapy and feeding management, including the possibility of entera/ tube feeding. Unfortunately, although videofluoroscopy is sensitive for neurogenic dysphagia, it is not very specific [5-16]; that is, videofluoroscopy is likely to reveal some combination of oral, lingual, palatal, pharyngeal, and laryngeal sensorimotor dysfunction, but usually not in a pattern characteristic of a particular neurologic disorder, with certain notable exceptions. Difficulty initiating swallowing (oral phase impairment) is suggestive of upper motor neuron problems such as bilateral infarcts and motor neuron disease. Absence of the swallowing reflex (i.e., failure of barium in the pharynx to trigger swallowing) is a sign of brainstem disease. Asymmetric pharyngeal paresis is indicative of lower motor neuron problems such as a unilateral lower cranial nerve or brainstem lesion. Findings such as "fatigue" of swallowing should be interpreted carefully, as this may occur in many conditions of muscle weakness other than myasthenia gravis, and normative data regarding pharyngeal fatigue have not been well established. Videofluoroscopy may reveal a second, treatable problem in addition to neurogenic pharyngeal dysfunction, such as esophageal dysmotility or an unsuspected obstructing lesion [131 ]. Additional gas- troenterologic or otolaryngologic evaluation may be indicated by clinical and videofluoroscopic findings.

The routine evaluation of a patient with neurogenic dysphagia of unknown origin should include blood


studies (complete blood counts, chemistry panel, CK, vitamin B 12, thyroid screening, anti-acetylcholine receptor antibodies, and perhaps, FTA and Lyme antibodies), brain MRI with enhancement, and EMG, repetitive nerve stimulation, and nerve conduction studies. Depending on the available evidence, CT of the skull base, lumbar puncture for cerebrospinal fluid examination, or muscle biopsy may also be indicated. When a specific diagnosis cannot be made, waiting and watching (and sometimes repeating studies if the patient 's condition changes) is the wisest approach. A stroke having caused dysphagia may declare itself in the course of the patient 's gradual recov-

ery over months, whereas motor neuron disease mani- fests in the opposite direction, causing an accumulation of motor symptoms and signs. In the meantime, the potential role of symptomatic treatment, such as swallowing therapy, should not be overlooked.

Conclusions

Neurogenic oropharyngeal dysphagia can develop sud- denly or gradually without a known underlying neurologic illness. Proper evaluation, including videofluoroscopy of swallowing, usually reveals evidence that the problem is, nonetheless, neurogenic. A thoughtful diagnostic approach combining careful history, neurologic examination, and appropriate ancillary studies often reveals the specific cause, which may be directly treatable or preventable.

Stroke is probably a common cause of unex-

plained neurogenic dysphagia, including infarcts conflu- ently in periventricular regions or discretely in the lower brainstem, but further study is needed. Other relatively frequent considerations include motor neuron disease, myopathy, and psychogenic dysphagia. Medications that can cause or contribute to oropharyngeal dysfunction should be eliminated, if possible. The causes and effects of age-related changes in the oropharynx remain unclear.

Acknowledgments. The author gratefully acknowledges the support and guidance of the faculty of the Johns Hopkins Swallowing Center, especially including Drs. Martin Donner, James Bosma, Bronwyn Jones, William Ravich, Thomas Hendrix, and Haskins Kashima. Thanks also to Drs. Jennifer Homer and Ross Levine for their invalu- able editorial input.

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