The Role of the Insular Cortex in Dysphagia - Springer Link

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In the oral stage these features were anterior bolus loss, delayed ini- tiation of movement, and uncoordinated initiation of oral transfer. An- terior bolus loss was ...
Dysphagia 12:146–156 (1997)

© Springer-Verlag New York Inc. 1997

The Role of the Insular Cortex in Dysphagia Stephanie K. Daniels, MS, CCC1 and Anne L. Foundas, MD2 1

Audiology/Speech Pathology Service,2Neurology Service, Veteran’s Affairs Medical Center, New Orleans, Louisiana, USA and Psychiatry and Neurology, Tulane University School of Medicine, New Orleans, Louisiana, USA

Abstract. Recent data indicate that dysphagia may occur following unilateral cortical stroke; however, the elucidation of specific cytoarchitectonic sites that produce deglutition disorders remains unclear. In a previous study of unilateral cortical stroke patients with dysphagia, Daniels et al. [8] proposed that the insula may be important in swallowing as it was the most common lesion site in the patients studied. Therefore, 4 unilateral stroke patients with discrete lesions of the insular cortex were studied to further facilitate understanding of the role of the insula in swallowing. Dysphagia, as confirmed by videofluoroscopy, was evident in 3 of the 4 patients; all had lesions that involved the anterior insula, whereas the only patient without dysphagia had a lesion restricted to the posterior insula. These data suggest that the anterior insula may be an important cortical substrate in swallowing. The anterior insula has connections to the primary and supplementary motor cortices, the ventroposterior medial nucleus of the thalamus, and to the nucleus tractus solitarius, all of which are important regions in the mediation of oropharyngeal swallowing. Therefore, discrete lesions of the anterior insula may disrupt these connections and, thereby, produce dysphagia. Key words: Stroke — Insula — Videofluoroscopy — Deglutition — Deglutition disorders.

Traditionally, dysphagia has been associated with brainstem or bilateral cortical lesions [1], and deglutition disorders resulting from these lesions have been well documented [2–7]. Although recent studies have demonstrated that dysphagia may also occur following unilat-

Correspondence to: Stephanie K. Daniels, M.S., CCC, Speech Pathology Service (126), VA Medical Center, 1601 Perdido Street, New Orleans, LA 70146, USA

1,2

Department of

eral cortical stroke [1,8–16], the specific cortical lesions that may produce dysphagia remain unknown [8–10,16– 19]. To date, most studies of unilateral stroke and dysphagia have focused upon differences in patterns of dysphagia in left vs. right hemispheric stroke [9,10,16–19]. To our knowledge, only one study attempted to document the precise neuroanatomical location of strokes that produce dysphagia [8]. In that study, Daniels et al. [8] studied dysphagia following unilateral stroke in 8 patients with left hemispheric damage (LHD) and 8 with right hemispheric damage (RHD). The insular cortex was the most common site of involvement, as it was lesioned in 11 of the 16 unilateral stroke patients with dysphagia. This finding was unexpected as lesions to the insula had not previously been associated with dysphagia. Therefore, Daniels et al. postulated that the insula may be important in swallowing because of its connectivity to crucial cortical, subcortical, and brainstem sites known to be important in swallowing. As the insula has been associated with related swallowing and nutritional properties such as coordinated interaction of oral musculature, gustation, and autonomic functions, through connectivity or inherent properties of its own [20–27], it was hypothesized that the insula, particularly the anterior insula, may contribute to oral and pharyngeal motility. To further elucidate the possible role of the insula in deglutition, 4 cases of unilateral stroke patients with discrete lesions of the insula were investigated. Neuroimaging studies, neurological examination, videofluoroscopy, bedside swallowing evaluation, and clinical oropharyngeal examination were performed on all patients. The clinical findings and the extent of the insular lesions in these 4 patients demonstrate the probable importance of the anterior insula in the mediation of swallowing. Subjects and Methods Subjects were selected from a sample of patients (n 4 39) enrolled in a prospective dysphagia study consisting of consecutive unilateral

S.K. Daniels and A.L. Foundas: Insular Cortex in Dysphagia stroke patients with new neurological deficits admitted to the Veterans Affairs Medical Center in New Orleans. The participants had no prior history of dysphagia, dementia, or neurodegenerative disorders. They consisted of 4 males, ages 50–63 years (mean age 55.5 years) who had sustained a unilateral cortical stroke with the lesion isolated to the insular cortex, as documented on computed tomography (CT) scan of the head. Four additional patients in the larger stroke sample had lesions that included portions of the insula and adjacent cortical regions. Three of these 4 had dysphagia. However, given that the lesions in these additional 4 patients extended beyond the insular cortex, they were not included in further analysis.

Procedures A neurological examination was completed upon hospital admission. Speech-language testing, oromotor examination, and bedside swallowing assessment were conducted within the first week of hospitalization, except for Case 2, who was referred for evaluation 4 months after the stroke. Each patient underwent a CT scan and videofluoroscopic swallow study (VSS) within 1 week of stroke onset, except for Case 2 who underwent the VSS 4 months after the stroke.

Neurological Examination The neurological evaluation included mental status examination and an elemental neurological assessment (Appendix 1). The mental status examination included tests of memory, intention, attention, language and related functions, neglect, and visuospatial abilities. The elemental neurological assessment included cranial nerve examination, sensory (pain, temperature, proprioception, and vibration), motor (bulk, tone, strength, movement disorders), cerebellar, gait and station, deep tendon reflexes, and pathological reflexes (Babinski response and frontal release signs).

Speech-Language Assessment Speech assessment included evaluation of articulatory precision and agility, fluency, resonance, and intelligibility. Language assessment consisted of evaluation of auditory comprehension, verbal fluency, naming, repetition, reading comprehension, and writing. Standardized testing in all areas was completed, as warranted, and consisted of the Western Aphasia Battery [28] and the Boston Naming Test [29].

Oromotor Examination Assessment of oral musculature symmetry, strength, agility and sensation was completed (Appendix 2). Features of the oromotor examination included measurements of isolated movement as well as continual speech and nonspeech movements of the mandible, lips, tongue, velum, and larynx. Light touch of the face was examined as well as the presence of gag and volitional cough. Identification of dysphonic voice quality was made and classified as wet-hoarseness, strained, breathy, or nonspecific hoarseness.

Bedside Swallowing Examination The clinical swallowing assessment consisted of administration of liquid, semisolid, and solid consistencies at varying calibrated volumes with assessment of oral transition, oral retention, initiation of laryngeal elevation, laryngeal excursion, voice quality after swallow, and spontaneous cough. Assessments were initiated with a 3-ml liquid bolus and progressed with increasing volumes as tolerated by the patient. Semisolid and solid volumes were initiated at half teaspoon volumes and progressed to continuous ingestion. Administration of a consistency was terminated if a patient demonstrated, on two swallows, either a cough or voice changes after the swallow.

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Fluoroscopic Examination The VSS was performed by speech pathology in conjunction with radiology. VSS samples were recorded using a Super-VHS videocassette recorder which was coupled to a counter timer that encoded digital time in hundredths of a second on each video frame. A video recording of the oral cavity (anterior to the lips) and the pharynx (inferior to the upper esophageal sphincter) was obtained in the lateral plane, as the patient swallowed liquid barium at volumes of 3, 5, 10, and 20 ml, and 1⁄2 teaspoon barium paste, twice each. Eight features of oropharyngeal dysmotility were evaluated. In the oral stage these features were anterior bolus loss, delayed initiation of movement, and uncoordinated initiation of oral transfer. Anterior bolus loss was identified as spillage from the lips. Delayed initiation of movement was identified as inability to begin oral transfer upon command to swallow. Uncoordinated initiation of oral transfer was defined as groping and effortful labial, lingual, and mandibular movements. The pharyngeal stage dysmotility patterns evaluated were delayed pharyngeal swallow, reduced laryngeal excursion, penetration into the laryngeal vestibule, aspiration, and stasis. Delayed pharyngeal swallow was measured from the time the bolus head reached the point where the ramus of the mandible bisects the base of the tongue until the onset of laryngeal excursion [30]. The delay was rated as mild (0.45–2 sec delay), moderate (3–5 sec delay), and severe (6 sec or greater delay). Patients with delay times