AIRWAY PROTECTION DEFICITS IN MULTIPLE-SYSTEM ATROPHY: A PROSPECTIVE COMPARISON
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1 AIRWAY PROTECTION DEFICITS IN MULTIPLE-SYSTEM ATROPHY: A PROSPECTIVE COMPARISON By JESSICA E. ZIPPER A THESIS PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF ARTS UNIVERSITY OF FLORIDA 2017
2 2017 Jessica E. Zipper
3 To Him who by all things were created in heaven and on earth, visible and invisible who is before all things and in whom all things hold together.
4 ACKNOWLEDGMENTS I thank my advisor, Dr. Karen Hegland, for her seemingly limitless patience, nurturing, and expertise. She welcomed a naïve and ill-equipped undergraduate student into her lab three years ago and graciously helped transform her into a passionate lover of coughing and swallowing. More than that, she modeled for her what it means to research with a purpose, imparting to her that research without humanity is void. For that lesson alone, an acknowledgement is insufficient. My hope is that my emulation of her in my future work will provide her with more adequate gratitude. I also thank Dr. Emily Plowman, my co-mentor, whose contribution of time and knowledge helped refine this research and this paper. I am grateful to Julie Hicks, speech-language pathologist and mother duck, who provided ongoing encouragement and guidance throughout this process. The other members of the University of Florida Center for Movement Disorders and Neuroresotration, including Drs. Michael Okun and Nikolaus McFarland and radiation technologist Judy Barry, were instrumental in the development and execution of this study. Equally instrumental were the faculty and staff of the UF Department of Speech, Language, and Hearing Sciences, who provide d me with a foundational understanding of research and the resources needed to build upon that. Lastly, my partner-in-thesis-crime, Molly Bowers Emery, and our diligent co-investigator, Shannon Tatum, are deserving of special praise for their enduring support and faithful commitment. Much credit goes to them for completion of this project and preservation of my sanity. 4
5 TABLE OF CONTENTS page ACKNOWLEDGMENTS... 4 LIST OF TABLES... 6 LIST OF FIGURES... 7 ABSTRACT... 8 CHAPTER 1 INTRODUCTION Normal Swallowing Physiology Swallowing in MSA Normal Coughing Physiology Coughing in MSA METHODS Cough Sensitivity Evaluation Procedures Cough Sensitivity Outcome Measures Cough Response Evaluation Measures Cough Response Outcome Measures Swallow Evaluation Procedures Statistical Analysis RESULTS DISCUSSION LIMITATIONS AND FUTURE DIRECTIONS LIST OF REFERENCES BIOGRAPHICAL SKETCH
6 LIST OF TABLES Table page 2-1 Participant demographics Swallow event definitions Timing measure definitions Cough differences across groups Swallowing difference across groups for thin liquid Swallowing difference across groups for pudding Correlations for UtC sensitivity and swallow metrics Correlations for disease duration and swallow metrics
7 LIST OF FIGURES Figure page 2-1 Modified Borg scale for UtC The Penetration-Aspiration Scale Results of the chi-square analysis of response to fog Results of the chi-square analysis of response to capsaicin
8 Abstract of Thesis Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Master of Arts AIRWAY PROTECTION DEFICITS IN MULTIPLE-SYSTEM ATROPHY: A PROSPECTIVE COMPARISON By Jessica E. Zipper May 2017 Chair: Karen W. Hegland Major: Communication Sciences and Disorders Multiple system atrophy (MSA) is a neurodegenerative disease that affects the autonomic nervous and motor systems. As it shares many of the features of Parkinson s disease (PD), it is considered an atypical parkinsonism. Among shared features is the leading cause of death in each disease: aspiration-pneumonia. While swallowing function and deficits have been studied in both patient populations, cough as an airway protective mechanism in patients with MSA remains unexamined. The purpose of this study is to examine airway protection deficits in MSA as compared to those found in PD. A prospective study design was used and patients with MSA or PD were recruited. Demographic, swallow, and cough data were collected on seven individuals with a diagnosis of MSA, as well as patients with a diagnosis of PD and age- and sex matched healthy adults (HA). Videofluoroscopic swallow studies were performed and analyzed using swallow timing metrics and swallowing safety ratings. Urge-to-cough (UtC) sensitivity was obtained by exposing each participant to varying concentrations of capsaicin in three separate trials. Cough response to low-intensity stimuli was measured using a continuous breathing paradigm with stimuli sub-threshold capsaicin, and nebulized water (fog). Parametric and non-parametric statistics were used to test 8
9 for differences between groups. Results revealed that there was not a significant difference for UtC sensitivity between groups. There was a significant difference for cough response to sub-threshold capsaicin and fog, with the MSA cohort producing more robust responses in terms of number of coughs to both stimuli, as compared to the PD and HA cohorts. Differences in timing of swallowing events were also found, with the MSA group demonstrating delayed initiation of swallow, delayed closure of the laryngeal vestibule, and prolonged closure of the laryngeal vestibule. This study provides preliminary evidence that patients with MSA may demonstrate reduced or absent cough motor response when presented with low-intensity sensory stimuli, as compared to patients with PD. While these findings should be replicated in future studies with larger sample sizes, clinical applications may include the use of cough motor data as a diagnostic indicator in differentiating PD from MSA. 9
10 CHAPTER 1 INTRODUCTION Multiple system atrophy (MSA) is a sporadic and progressive neurodegenerative disease that affects the autonomic nervous system and motor system. It is considered an oligodendroglial alpha-synucleinopathy in that its underlying pathophysiologic mechanism is an aggregation of the protein alpha-synuclein. In this sense, it is similar to Parkinson s disease (PD) in its presentation, warranting its classification as an atypical Parkinsonism or Parkinson s plus syndrome. Because of this similar presentation, MSA is commonly misdiagnosed in its early stages as PD and accurate diagnosis is only definitively achieved upon autopsy (Fanciulli & Wenning, 2015). MSA is divided into two subtypes according to clinical features: parkinsonian subtype (MSA-P) and cerebellar subtype (MSA-C). Common to both is the hallmark feature of severe autonomic decline, which presents early in the disease process. Autonomic dysfunction most commonly manifests as impairments in the urogenital and cardiovascular mechanisms. Urinary dysfunction may include urinary urgency and frequency, incontinence, nocturia, and, to a lesser extent, incomplete bladder emptying. The predominant feature of cardiovascular dysfunction in MSA is marked orthostatic hypotension. Accompanying this orthostatic hypotension may be any of the following symptoms: recurrent syncope, weakness, light-headedness, headache, nausea, tremulousness, and pain in the neck and shoulders upon standing. Respiratory dysfunction occurs less commonly but is still characteristic of MSA, with diurnal or nocturnal inspiratory stridor seen in up to 50% of patients and sleep apnea in 40% of patients. Sexual disturbances namely, erectile dysfunction in males and genital hyposensitivity during intercourse in females may also occur. Finally, autonomic failure 10
11 may also manifest in additional features, such as constipation, pupillomotor abnormalities, and vasomotor and thermoregulatory failure (Fanciulli & Wenning, 2015). As is characteristic of any parkinsonian condition, the predominant features of MSA-P are bradykinesia, rigidity, and a tendency to fall. In contrast to the resting pillrolling tremors of Parkinson s disease, postural or action tremors are more commonly seen in MSA-P. Approximately 40% of patients may be intermittently responsive to dopaminergic medications in the early phases of the disease. However, overall poor response to such medications is essential to a diagnosis of probable MSA-P (Fanciulli & Wenning, 2015). MSA-C is primarily characterized by cerebellar ataxia with features including a wide-based gait, action tremor, uncoordinated limb movements, and downward nystagmus that can by spontaneous, gaze-evoked, or positional. Generalized hyperreflexia and Babinksi sign are seen in 30-50% of cases (Fanciulli & Wenning, 2015). Currently, there are no known causes of MSA. By and large, it is considered a sporadic disease; however, the role of genetic inheritance in certain cases cannot be dismissed. An autosomal dominant or recessive pattern of transmission has been found in a few European and Japanese lineages. Mutations in COQ2, SHC2, and SNCA have been shown to be associated with MSA in select populations; however, findings remain limited and conclusive generalizations regarding genetic links remain out of reach (Fanciulli & Wenning, 2015). What is known of MSA is its underlying neuropathology, as evidenced in postmortem examination: olivopontocerebellar atrophy and striatonigral degeneration. 11
12 These changes are consistent with the clinical phenotypes of ataxia and parkinsonism seen in MSA. Additionally, changes are also seen in the central autonomic nervous system, such as the hypothalamus, dorsal nucleus of the vagus nerve, noraderenergic and serotoninergic brainstem nuclei, nucleus ambiguus, Onuf nucleus, and intermediolateral columns of the spinal cord. In more advanced disease states, there may be atrophy of the frontal lobe (Fanciulli & Wenning, 2015). Histologically, MSA is marked by proteinaceous oligodendroglial cytoplasmic inclusions, or Papp-Lantos bodies. Distinguishing it from Parkinson s disease, dementia with Lewy bodies, and pure dysautonomia whose hallmark neuropathological feature is alpha-synuclein aggregates known as Lewy bodies MSA is characterized by inclusion of misfolded alpha-synuclein in glial cytoplasm. Still, neuronal axonal, cytoplasmic, nuclear, and oligodendroglial nuclear inclusions may occur to a lesser degree (Fanciulli & Wenning, 2015). With an approximate mean incidence of cases per 100,000 person-years, MSA is an extremely rare disease. Estimated point prevalence is cases per 100,000 population. The disease usually first presents during the sixth decade of life, underscoring the fact that estimate of point prevalence increases to 7.8 per 100,000 among people aged 40 years or older. On a whole, there are nearly twice as many cases of MSA-P as there are cases of MSA-C. There is no known gender discrepancy. Upon emergence of symptoms, mean survival is 6-10 years and survival beyond 15 years is rare. As is common in neurodegenerative diseases and more specifically, the parkinsonian syndromes--aspiration-pneumonia is the leading cause of death in patients with multiple-system atrophy (Fanciulli & Wenning, 2015). 12
13 Normal Swallowing Physiology For the purposes of distinguishing normal swallowing function in healthy adults from the atypical swallowing function often found in patients with MSA, normal swallowing physiology is described here. Swallowing can have both voluntary components, as is the case with mastication, and involuntary components, as is the case with subconscious saliva swallows (Dodds et al., 1990). The primary goals underlying swallowing physiology are airway protection and bolus efficiency. In keeping with the purpose of this paper to describe the sensorimotor deficits in airway protection associated with MSA we will predominantly focus on the airway protective goal of swallowing. In general, swallowing can be divided into four phases: 1) oral preparatory phase, 2) oral phase, 3) pharyngeal phase, and 4) esophageal phase. The preparatory phase consists of mastication and formation of a bolus with saliva via lingual manipulation. The oral phase consists of propulsion of the bolus posteriorly from the oral cavity to the pharynx. The pharyngeal phase consists of movement of the bolus from the oropharynx into the esophagus. More specifically, during the pharyngeal phase there are several mechanisms of airway protection that occur. First, retraction of the base of the tongue, and its subsequent movement superiorly and posteriorly, direct the bolus toward the pharynx. Simultaneously, the velopharynx closes, allowing for pressure accumulation in the pharynx to help direct the bolus toward the esophagus. The pharynx then elevates and the superior, middle, and inferior pharyngeal constrictors are serially activated to propel the bolus inferiorly. The suprahyoid muscles contract, enabling elevation and excursion of the hyolaryngeal complex. The true and false vocal folds adduct, closing off the glottis and preventing intrusion of aspirate material into the 13
14 airway. The epiglottis inverts over the laryngeal vestibule to direct the bolus away from the airway. The anterior-superior movement of the hyolaryngeal complex, coupled with the contraction of the inferior pharyngeal muscle, contribute to opening of the upper esophageal sphincter (UES) (Pitts et al. 2012). Finally, the esophageal phase consists of movement of the bolus from the UES to the stomach via peristaltic activity of the esophageal musculature and the work of gravity. The relaxation of the lower esophageal sphincter marks the passage of the material into the stomach and the end of the esophageal phase (Dodds et al., 1990). It should be noted that while these categories are helpful for organizing swallowing function conceptually, timing of the phases may overlap and the events noted within the phases may occur simultaneously. Thus, the phases during an actual swallow need not be so rigidly delineated. The main anatomic players responsible for neural control of swallowing include: 1) efferent motor fibers of the cranial nerves and the ansa cervicalis, 2) afferent sensory fibers of the cranial nerves, 3) fibers of the cortex, midbrain, and cerebellum that synapse in the midbrain swallowing centers, and 4) paired swallowing centers of the brainstem. The primary afferent sensory nerves responsible for initiating swallowing are IX and X, and to a lesser extent the maxillary branch (V2) of V and VII. Taste fibers on the anterior two-thirds of the lingual surface, as well as touch sensory fibers for the lips and face, are innervated by the facial nerve. The posterior larynx, base of tongue, and hypopharynx are innervated by the superior laryngeal nerve of the vagus nerve (Dodds et al., 1990). The centers responsible for swallowing are housed in the brainstem, specifically the hindbrain. While basic animal science studies have shown that only one functional 14
15 center is necessary to swallowing, the centers are not in fact distinctively defined regions. Instead, the nucleus tractus solitarius and the ventromedial reticular formation the locations at which sensory information from the cranial nerves and higher-level cerebral areas synapses form the broad areas of the swallowing centers. These centers contain a sophisticated arrangement of interneurons that receive incoming sensory signals, create a preprogrammed motor swallowing response, and then allocate the signal to cranial nerve motor nuclei and their axons. From these axons, the signal for activation of swallowing musculature is delivered (Dodds et al., 1990). Two hypotheses have been suggested to explain how control of swallowing proceeds from the swallowing centers. The first, the reflex-chain hypothesis, explains that as the bolus travels through the mouth and pharyngeal cavity, sensory receptors are activated in a sequential fashion, informing one step of the swallowing process to the next. In a sense, the reflex-chain of relay of sensory information and corresponding motor response is enacted by the pharyngeal trigger. The other hypothesis, the central pattern generator hypothesis, claims that swallowing proceeds as a stereotyped behavior once it has been initiated. The brainstem formulates a programmed plan for swallowing that is not modified by sensory information (Dodds et al., 1990). Swallowing in MSA Despite the fact that aspiration pneumonia is among the leading causes of death in all Parkinsonian syndromes, swallowing function in these populations, and in MSA particularly, is grossly understudied (Litvan et al., 1996; National Institute of Neurological Disorders and Stroke, 2004; Papapetropoulos et al., 2007; Wenning, 2003). Aside from the recognition that dysphagia is a common complication in the 15
16 atypical parkinsonisms and that early onset of dysphagia may be a prognostic indicator in terms of survival (Litvan et al., 1996; Muller et al., 2001), little is known or documented of their swallowing physiology and deficits. Higo et al. (2003, 2003, and 2005) have conducted three studies examining swallowing function in MSA, all using the same participant sample and all drawing similar conclusions: oropharyngeal swallowing deficits in MSA were generally consistent with those in PD. Oral phase deficits predominate and include delayed oral transport, inadequate bolus containment, and reduced base-of-tongue retraction. Prolonged laryngeal excursion was noted in the pharyngeal phase, as well as reduced pressure in the oropharynx and hypopharynx during deglutition. Some participants also exhibited inadequate relaxation of the UES. In this sample, there was a correlation between severity of disease and history of aspiration pneumonia and there was no correlation between patient age and disease duration. To date, Dornisch et al represents the only published effort to use validated swallowing outcome measures of timing and duration to study different aspects of the swallow in patients with Parkinsonian syndromes (i.e., MSA, CBD, and PSP) as compared to patients with PD. The Penetration-Aspiration scale (PAS) and the Modified Barium Swallow Impairment Profile (MBSImP) were used to assess components of swallowing safety and efficiency. Findings indicated that patients with MSA-P are at greatest risk across all groups for decreased swallowing safety. Additionally, consistent with established literature, the most severely impaired swallow components in patients with MSA were confined to the more volitional oral phase of swallowing, including oral residue, bolus transport/lingual motion, initiation of the 16
17 pharyngeal swallow, pharyngeal residue, and tongue base retraction. In terms of MBSImp composite score--an overall impairment measure accounting for 11 different swallowing events--msa-grouped (MSA-P and MSA-C groups combined) was the least severely impaired group, whereas MSA-P was the most severely impaired group. In terms of timing measures, MSA-P had the most severely impaired oropharyngeal timing. Furthermore, MSA-P was identified as the disease group with the most or second most severe impairments in 8 out of the 11 swallow measurements. A correlation between relative severity of swallowing impairments and severity of overall dysfunction in MSA-P could be extrapolated as that disease group consistently had the most severely impaired swallow and the highest mean UPDRS (United Parkinson s Disease Rating Scale; a measure of Parkinson s disease severity) score. Normal Coughing Physiology In partnership with the airway protective mechanisms of swallowing, cough serves as an airway protective behavior. The two acts function at opposite ends of what has been described as the airway protection continuum with effective and swallowing on one end, preventing material from invading the airway, and effective coughing on the other end, removing material when airway invasion occurs (Troche et al., 2014). Given the cooperative nature of their functions, it is expected that swallow and cough would have overlapping sensorimotor control and execution, which was described by Troche et al. in Summarized below are the sensorimotor mechanisms underlying cough. Initiation of cough, and modification of cough once initiated, is determined by peripheral sensory input, which may include irritants (i.e., capsaicin, citric acid, fog, etc.), concentration of irritants, volume and duration of irritant presentation, nasal afferent stimulation, and lung volume upon cough initiation. This sensory information is 17
18 sent to cough receptors that modulate reflexive cough production and dictate the various features of cough inspiratory flow rate, number of coughs produced, cough expiratory airflow parameters, and amplitude and duration of expiratory muscle activation during cough accordingly. The receptor types involved in reflexive cough production consist of primarily cough receptors, as well as subtypes of c-fibers, tracheabronchial rapidly adapting receptors (RARS), and intrapulmonary stretch receptors (Pitts et al, 2012). Briefly, once detected by the cough receptors, sensory information travels to the appropriate cranial nerves (CNs), where it will be directed and transmitted to corresponding destinations for motor output. The glossopharyngeal nerve and the vagus nerve, CNs IX and X respectively, are primarily involved in the initiation of cough. Specifically, the pharyngeal nerve of CN IX, which innervates the oropharynx, lateral pharyngeal wall, and pharyngeal plexus via its superior, middle, and inferior subdivisions, is directly responsible for initiating cough. Also essential to the cough initiation is the internal branch of the superior laryngeal nerve, one of the two main divisions of CN X. Cough is modified via the sensory information that is sent from the posterior third of the tongue and upper pharynx via the general, or somatic, sensory component of CN IX. This sensory input eventually reaches the sensory cortex by way of the contralateral ventral posterior nucleus of the thalamus (Pitts et al., 2012). Sensory information is then transmitted to neural networks in the brainstem known as central pattern generators (CPGs), which are responsible for initiating complex, patterned motor output, as well as modulating amount, duration, and timing of motor movements according to sensory stimuli. The nucleus tractus solitarius (NTS) is 18
19 the site at which nearly all afferent fibers involved in cough converge in the brainstem. Though not conclusively determined, the NTS and the surrounding reticular formation are thought to comprise the CPG for cough (Pitts et al., 2012). In order for a behavioral reflex to be modified, it must first be perceived. For coughing, the urge-to-cough (UtC) is critical to conscious modulation and was defined as a respiratory sensation related to a cough stimulus preceding the motor behavior by Troche et al. in It has been shown to have a log-log linear relationship with increasing concentrations of a cough-inducing stimulus, such as capsaicin for the purposes of this investigation. In other words, as intensity of capsaicin increases, subjective ratings of UTC also increase. Furthermore, as UTC increases, the associated number of cough produced increases, illustrating the role of UTC in sensorimotor integration (Troche et al., 2014). It should be noted that Yamanda et al. (2008) demonstrated that patients with a history of aspiration-pneumonia have a blunted UTC at subthreshold level of citric acid. Advancing superiorly from the brainstem, afferent fibers also synapse at the thalamus and terminate ultimate in the cortex, giving rise to the role of voluntary control in cough. The cortex exerts volitional control over cough motor output by suppressing and regulating the reflexive motor output of the brainstem. Consider, for example, the role of the cortex and volitional control when an urge-to-cough is perceived in a quiet lecture hall and one attempts to not cough or cough softer. Using both affective (i.e., features of emotional salience and experience of a stimuli) and discriminative (i.e., spatial, temporal, and intensity characteristics of a stimuli) processing, the cortex can have volitional influence over cough motor behavior (Troche et al., 2014). 19
20 With the efferent components of cough activated, the motor cough response begins with the inspiratory phase. Inspiratory airflow is enabled when the thoracic cavity expands and lung volume increases, which are caused by muscular activity of the diaphragm and laryngeal dilatation by means of activation of the posterior cricoarytenoid and the cricothyroid muscles. Next, the vocal folds rapidly adduct and the expiratory muscles (primarily the internal and external oblique muscles) contract. The compression phase, when the glottis is closing, allows for greater airflow velocities, and thus, increased cough effectiveness. High positive intrapleural/intrathoracic pressures are generated during the compression phase as a result of isometric contraction of the expiratory muscles, which allows the adequate length-tension relationship to be maintained by muscles. The vocal folds then abduct, signaling the beginning of the expiratory phase. The initial expiratory airflow and high peak flow rates are generated when the glottis rapidly opens and there is a ballistic release of expiratory air. Smooth muscles in the airway also contracts, narrowing the bronchi. This, in turn, causes a decrease in the cross-sectional area within the lungs and an increase in shear forces during the expiratory phase (Pitts et al. 2012). Coughing in MSA While there is a paucity of existing literature detailing swallowing in MSA, there is a complete void of literature detailing cough in MSA. Given the critical need for investigation of the relationship between these two airway protective mechanisms in such a susceptible population, the chasm between what is known about swallowing and what is yet to be known about cough must currently be bridged by literature about cough in PD. Because the neuropathophysiology underlying both diseases and the presenting phenotypes including shared swallow deficits, as previously noted are 20
21 related, research on cough function and dysfunction in patients with PD can serve as a foundation for pilot research on cough in MSA. It has been well established that patients with PD and dysphagia demonstrate a blunted urge-to-cough sensitivity and an associated higher cough sensory threshold. Furthermore, significantly blunted urge-to-cough has been found to be correlated with increasing levels of dysphagia severity when patients were exposed to capsaicin only (Troche et al., 2014). When comparing UtC and cough sensory threshold when both capsaicin and low-intensity stimuli (i.e., fog) were used, Hegland et al. (2016) found that all participants, inclusive of PD patients and healthy younger adults, coughed more to capsaicin as compared to fog. Additionally, there was no significant difference in the number of coughs produced in response to either stimulus between the PD group and the healthy group. However, people with PD and without dysphagia produced more coughs than people with PD and with dysphagia. When data from the PD group were categorized according to response to stimulus vs. non-response to stimulus, fog was shown to be a highly sensitive (77.8%) and specific (90.9%) indicator of whether the participants had dysphagia, whereas capsaicin showed remarkable specificity (95.9%) but poor sensitivity (20%). In summary, sensorimotor integration of cough, as well as the integration of the airway protective mechanisms of cough and swallow in patients with MSA, have yet to be explored. The purpose of this study is to establish preliminary findings of the deficits leading to uncompensated airway compromise in MSA and to compare those to airway protective deficits seen in PD and in healthy adults. To that end, the aims of this study, and corresponding hypotheses, are as follows: 21
22 Aim 1: To determine the relationship between perceptual cough sensitivity and cough motor threshold in people with Multiple System Atrophy (MSA) compared to age and sex-matched healthy adults (HA), and participants with Parkinson s disease (PD). Hypothesis 1: It is hypothesized that people with MSA will under-perceive low-intensity cough-inducing stimuli, leading to a blunted urge-to-cough (UtC) sensitivity and higher cough sensory threshold (CST) compared to the HA and PD groups. Aim 2: To determine whether there are differences in the relationship between reflex cough stimulus type (capsaicin and fog), cough response and swallowing safety and physiology in patients with MSA versus PD. Hypothesis 2a: It is hypothesized that people with MSA will under-respond to both types of low-intensity cough stimuli as compared to people with PD. Hypothesis 2b: It is hypothesized that measures of swallowing safety and physiology will correlate with the cough response to both cough-inducing stimuli. 22
23 CHAPTER 2 METHODS This prospective experimental study was comprised of three participant groups: health adults control participants (HA), participants with atypical parkinsonism (multiple systems atrophy; MSA), and participants with Parkinson s disease (PD). Once enrolled in the study, all participants underwent reflex cough testing with up to 6 different concentrations of capsaicin, varying from low-intensity (25µM) to high intensity (500µM). The PD and MSA groups also underwent continuous-inhalation cough testing to lowintensity stimuli, as well as fluoroscopic swallowing evaluation. The participant pool was obtained from patients with PD or MSA seen at our clinics at the University of Florida Center for Movement Disorders and Neurorestoration (UF CMDNR), where approximately 1500 idiopathic PD patients are currently followed prospectively in an IRB approved database. The UF CMDNR is a National Parkinson s Disease Center of Excellence and as a peer reviewed center of excellence must see a minimum of 400 unique Parkinson s disease patients a year. For patients with PD, testing was completed on dopaminergic medications. The HA group was recruited from caregivers or family members accompanying patients to the center, and via the general population of healthy adults in the community. Participants were enrolled without regard for race or ethnicity. Once enrolled, participants were screened for the following exclusionary criteria: neurological disorders other than parkinsonism (i.e., stroke), history of breathing disorders or diseases, history of smoking in the last five years, uncontrolled hypertension, difficulty complying due to neuropsychological dysfunction (i.e., severe depression), and allergy to capsaicin or hot peppers. Exclusionary criteria for the control group included the aforementioned as well as any 23
24 history of neurologic disorder including PD. Participant demographics are shown in Table 2-1. Cough Sensitivity Evaluation Procedures All participants (HA, PD, MSA) completed a capsaicin challenge with three randomized blocks of 0, 25, 50, 100, 200, and 500μM capsaicin. The capsaicin was dissolved in a vehicle solution consisting of 80% physiological saline, and 20% ethanol; the concentrations were differentiated based on the amount of saline added to the stock solution. Each concentration level was placed in an Omron MicroAir nebulizer for presentation to the participant. A single-breath inhalation method was used. Participants were given the instruction to inhale deeply 1 time, and cough if you need to. They were shown a modified Borg scale of perceptual cough sensitivity (Figure 2-1) and asked to rate their UtC immediately following. There was a minimum of one minute between each trial, and participants were provided water to drink between trials. Cough Sensitivity Outcome Measures The UtC sensitivity, CST and CMT were determined using the following definitions: UtC sensitivity is the slope calculated by plotting the UtC ratings against capsaicin concentration on a log-log scale, and fitting a linear regression line to the data (e.g. [22, 25]). Cough sensory threshold (CST) is defined as the lowest concentration of capsaicin that elicits a perceived UtC of 1 (very slight) in at least 2/3 trials, and the cough motor threshold (CMT) is defined as the lowest concentration of capsaicin that elicits at least 2 cough responses in 2/3 trials [22]. Cough Response Evaluation Measures Two low-intensity stimuli were used: aerosolized water (Fog) and a low concentration of capsaicin. The concentration of capsaicin selected was the 24
25 concentration immediately below the participant s cough sensory threshold established in the single-breath inhalation procedures. When the participant s sensory threshold was at the lowest presented concentration (25 μm), half the concentration (12.5 μm) was used. The capsaicin and fog stimuli were placed in an Omron MicroAir nebulizers for presentation to the participant. Participants were instructed to relax and breathe, both in and out, through the nebulizer for up to 60 seconds per trial. Three trials were completed. They were instructed to cough if you need to. The total number of coughs recorded per trial was recorded. Cough Response Outcome Measures The primary outcome measure is the presence of a positive or negative cough response. A positive response is defined as 2 or more coughs produced in response to 2/3 presentations of the fog and capsaicin stimuli. A negative response is less than 2 coughs produced to 2/3 presentations of the stimuli. Swallow Evaluation Procedures. Swallowing was assessed for all MSA and PD participants. Swallowing was assessed using a high resolution, dual modality videofluoroscopic (VFS) workstation with signal acquisition (digitized at 250 Hz) and digital storage for retrieval of swallowing data. Participants were seated in the lateral viewing plane. One teaspoon, one one-oz. cup sip, three 3 oz. sequential swallow challenge, all of Barium sulfate of thin-liquid consistency, was administered. Additionally, a teaspoon of Barium sulfate of pudding consistency was administered by spoon. Swallowing measures included the functional 8-point penetration-aspiration scale (PAS; Rosenbek et al., 1996) (Figure 2-2), and measures of swallow event timing. The 25
26 penetration-aspiration scale was used to assess penetration or aspiration of bolus material during each swallow trial. Statistical Analysis Descriptive statistics were used to summarize participant demographics, including age, sex, and disease duration. Inferential analyses were completed using non-parametric statistical tests because of the small number of participants in the study groups. The Kruskal-Wallis test was used to identify whether there were differences in the three participant groups (HA, MSA, PD) in terms of age, UtC sensitivity slope, sensory threshold (CST), and motor threshold (CMT). The Mann-Whitney test was used to test for differences between the MSA and PD groups for swallowing measures (PAS and timing measures). Chi square analysis was used to test for differences between PD and HOA in terms of response to low-intensity capsaicin and fog stimuli. Finally, spearman s correlations were used to determine relationship between cough sensitivity and swallowing measures in the MSA and PD groups. In all cases, the significance level was set at p <
27 Table 2-1. Participant demographics MSA Patient ID Age Sex Disease Duration 1 58 M F M F F M M 1 PD N Age (mean) Sex (mode) Disease Duration (mean) M 4.56 Table 2-2. Swallow event definitions. Event Description BE bolus escape (premature spillage) to the ramus of the mandible B1 H1 LVC LVO the first movement of the bolus from a stable or hold position that passes the posterior nasal spine first superior-anterior movement of the hyoid aryepiglottic fold elevation to the point of supraglottic closure first opening of the laryngeal vestibule UESo onset of UES opening 27
28 Table 2-3. Timing measure definitions. Calculation Measurement BE-B1 Latency between non-volitional bolus escape and onset of volitional oral transit H1-B1 LVC-B1 LVO-LVC UESo-B1 Latency between onset of oral transit and onset of superior-anterior hyoid excursion Latency between onset of oral transit and onset of superior-anterior hyoid excursion Latency between supraglottic closure and first opening of laryngeal vestibule Latency between onset of oral transit and onset of UES opening Figure 2-1. Modified Borg scale for UtC. 28
29 Figure 2-2. The Penetration-Aspiration Scale. 29
30 CHAPTER 3 RESULTS Results of the Kruskal-Wallis test revealed that the MSA group is significantly younger than the PD and HOA groups (which were not significantly different than each other.) There were no differences in terms of the UtC slope, CST, or CMT between groups (Table 3-1). Results of the Mann-Whitney test revealed significant differences between the MSA and PD groups for PAS, and several of the swallow timing variables. Specifically, for thin liquid, H1_B1 and LVO_LVC were different (Table 3-2), and for pudding, BE_B1, LVC_B1, and LVO_LVC were different. Results of the chi-square analysis revealed significant differences between PD and MSA for response to capsaicin (x 2 = 7.865, p =.005) and not for fog (x 2 = 3.85, p =.05) (Figure 3-1). Specifically, for capsaicin, 81.3% of the PD group were responders, versus 16.7% of the MSA group. In contrast, 83.3% of the MSA group did not cough to capsaicin, as compared with 18.8% of the PD group (Figure 3-2). Results of the spearman correlation analyses are in Tables 3-4 and 3-5. For the MSA group, the UtC slope did not significantly correlate with any of the swallowing variables, including PAS or timing measures. It did show a strong negative correlation with participant age (r = -.886, p =.019). In contrast, in the PD group there was a significant negative correlation between UtC sensitivity and PAS (r = -.684, p =.003), and UtC sensitivity and LVC_B1 of thin liquid (r = -.499, p =.049), but not with participant age (r = -.210, p =.436). 30
31 Table 3-1. Cough differences across groups. Age UTC Slope Sensory Threshold Motor Threshold Sig. p=.002 p=.834 p=.246 p=.658 Group Mean Rank HOA PD HOA PD Group Mean Rank PD HOA MSA HOA Group Mean Rank MSA 7.50 MSA PD MSA Table 3-2. Swallowing difference across groups for thin liquid. PAS BE-B1 H1-B1 LVC-B1 LVO-LVC UESo-B1 Sig. p=.030 p=.171 p=.004 p=.191 p=.048 p=.638 Group Mean Rank PD PD MSA PD MSA PD Group Mean Rank MSA MSA PD 9.34 MSA 9.21 PD MSA Table 3-3. Swallowing difference across groups for pudding. BE-B1 H1-B1 LVC-B1 LVO-LVC UESo-B1 Sig. p=.029 p=.893 p=.005 p=.001 p=.120 Group Mean Rank PD MSA PD MSA PD Group Mean Rank MSA 9.71 PD MSA 5.79 PD 8.43 MSA
32 Fog 100% 90% 80% 70% 60% 50% 40% 30% 20% 10% 0% PD MSA Non-Responder Responder Figure 3-1. Results of the chi-square analysis of response to fog. Figure 3-2. Results of the chi-square analysis of response to capsaicin. 32
33 Table 3-4. Correlations for UtC sensitivity and swallow metrics. Thin liquid Pudding PAS Be_B1 H1_B1 LVC_B1 LVC_LVO UESo_B1 Be_B1 H1_B1 LVC_B1 LVC_LVO UESo_B1 MSA r=.494 p=.320 r=-.131 p=.805 r=.551 p=.257 r=.696 p=.125 r=-.314 p=.544 r=.829 p=.042 r=-.034 p=.949 r=-.371 p=.468 r=.530 p=.280 r=-.203 p=.700 r=.177 p=.738 PD r=-.684 p=.003 r=-.308 p=.246 r=-.046 p=.865 r=-.499 p=.049 r=-.128 p=.637 r=-.454 p=.077 r= p= r=.396 p=.129 r=.208 p=.457 r=-.036 p=.899 r=.232 p=.287 Table 3-5. Correlations for disease duration and swallow metrics. Thin Liquid Pudding PAS Be_B1_ 1 H1_B1 _1 LVC_B1 _1 LVC_LV O_1 UESo_B 1_1 Be_B1 _4 H1_B1 _4 LVC_B1 _4 LVC_LV O_4 UESo_B 1_4 MSA r=-.029 p=.9 51 r=-.816 p=.0 25 r=-.283 p=.538 r=-.248 p=.592 r=-.055 p=.908 r=-.321 p=.483 r=-.136 p=.771 r=-.413 p=.357 r=-.574 p=.178 r=.093 p=.843 r=-.524 p=.227 PD r=.53 5 p=.0 33 r=.33 7 p=.2 02 r=.300 p=.259 r=.005 p=.985 r=-.127 p=.639 r=-.060 p=.825 r= p= r=-.468 p=.067 r=-.203 p=.468 r=-.200 p=.475 r=-.355 p=
34 CHAPTER 4 DISCUSSION This study builds upon existing literature detailing swallowing physiology and deficits in patients with MSA and also serving as a pilot investigation of sensorimotor integration of cough in this population and its relationship to swallow. To date, this is the first study to examine cough function in patients with MSA, and, more specifically, to examine the relationship between perceptual cough sensitivity and cough motor threshold in patients with MSA. Furthermore, it is the first study to examine the relationship between reflex cough stimulus type, cough response, and swallowing safety and physiology in patients with MSA. To that end, this study provides preliminary data indicating that patients with MSA may demonstrate reduced or absent cough motor response when presented with low-intensity sensory stimuli. Given that patients with MSA are at an increased risk to develop and die from aspiration-pneumonia, the enhanced understanding offered in this study of the roles of the airway protective mechanisms of cough and swallow is critical. Results of the current study indicate that the MSA group is significantly younger than the PD and HOA groups. This may be attributed to the fact that age of onset of symptoms is younger in MSA: during the sixth decade of life in MSA versus in the early seventh decade of life in PD. Additionally, the progression of MSA and likely the decline of cough and swallowing functions occurs more rapidly as compared to PD. Thus, even if a patient with MSA and a patient with PD have onset of motor symptoms at the exact same age, the patient with MSA will likely experience more pronounced impairments more quickly than the patient with PD, compelling him or her to seek 34
35 treatment earlier in the disease course and subsequently be enrolled in this study at a younger age. Findings of this study indicate that MSA is not significantly different from PD with regards to reflex cough sensitivity, as evidenced by urge-to-cough, cough sensory threshold, and cough motor threshold measures. In interpreting this lack of significant difference, at least two factors should be considered: 1) the impact of disease duration and 2) the impact of age. As disease duration was not controlled for in this study and there is a sharp contrast between the course of decline in PD and the course of decline in MSA, it is plausible that this is a confounding factor. Similarly, as mentioned above, age was not well-matched in this study across the three groups, also introducing a confounding factor that could be closely linked with disease duration. Brandimore et al. (2016; in press) reported age-related differences in cough reflex sensitivity in healthy older adults as compared to healthy younger adults, and thus it may be that if the MSA group had been matched for age with the PD group that their cough sensitivity would show differences. This important consideration should be carefully controlled for in future studies. Of note, the penetration-aspiration scores of the MSA group were not correlated to any swallowing metric examined in this study, including pre-swallow spillage or delayed swallow initiation. While established literature and the current study have demonstrated that patients with MSA do have penetration/aspiration events, none of the physiologic measures of swallowing that were analyzed in this study seem to explain such events. This lack of correlation may be linked to several factors. First, the penetration/aspiration events may be occurring on swallows that were not analyzed, 35
36 such as secondary swallows of pharyngeal residue or on the second or third swallow of the sequential swallow challenge. What can be gleaned from this phenomenon is that the swallow function of patients with MSA is marked by a substantial discoordination, and within that discoordination, there is substantial between-subject variability. As such, no one variable may consistently be responsible for airway compromise across the group as a whole. Although within-subject patterns of physiological dysfunction may be noted, such analysis is beyond the scope of this study. Additionally, as a relatively small sample size was used, a stronger correlation may have been found with a larger sample size. In contrast, in the PD group, PA score is significantly correlated to disease duration, UtC slope, and the initiation of the swallow. All of these findings are in agreement with previous findings regarding swallow and cough in PD. The correlation between UtC sensitivity and the latency between onset of oral transit and onset of UES opening may be attributable to the delayed swallow initiation found in the MSA cohort. Two physiologic events account for UES opening: traction of the hyolaryngeal complex and relaxation of the cricopharyngeus muscle. The first signifies the onset of the swallow. As swallow initiation was found to be delayed in the MSA group, delay in UES opening would be expected. Particular attention should be given to our finding that the PD group (81.3%) was a robust cough responder to capsaicin, as compared to the MSA group (16.7%). Inferences that can reasonably extrapolated from this data are that the absence of response to capsaicin stimuli is more likely to support a diagnosis of MSA. In contrast, the presence of response to capsaicin stimuli is more likely to support a diagnosis of PD. Similarly, the presence of response to fog stimuli is indicative of a PD diagnosis. 36
37 However, it cannot be inferred that the absence of response to fog argues for an MSA diagnosis, as all MSA participants were non-responders to fog. Thus, this current study provides evidence that response to capsaicin may be a more specific and sensitive indicator of PD versus MSA. The implication of these findings is that cough motor response to capsaicin stimuli may be a helpful diagnostic tool in differentiating between PD and MSA during clinical evaluation. While these results would first need be replicated in larger sample sizes before clinical potency can be established, the value of such a diagnostic indicator would be immense given the frequent misdiagnosis of MSA as PD, particularly in the early stages. 37
38 CHAPTER 5 LIMITATIONS AND FUTURE DIRECTIONS The limitations of this study were briefly mentioned above and include a small sample size, analysis of select swallows only, and lack of matching between groups in regards to disease duration and poor matching across groups in regards to age. Sample size was small in this study due to the etiology of MSA. As MSA is such a rare disease, recruiting a large sample size proved challenging and unfeasible for this study at this time. Additionally, patients with MSA, particularly those in a more advanced disease state, were sometimes not amenable to participating in the study due to high fatigue and inability to tolerate higher intensities of capsaicin. Future studies should aim to include larger sample sizes, which may capture findings that may not have been attainable in this study due to small number of participants. As only select swallows were analyzed in this study, future research should expand the number and variety of swallows analyzed in order to capture greater detail regarding differences in cough and swallow between PD and MSA and within MSA. In particular, there may be correlations between PA score and swallow metrics for which this study did not account due to the fact that not all PA scores were analyzed. Lastly, future studies should also seek to match participants with MSA with participants with PD in regards to disease duration. Similar to sample size, this may be challenging as recruitment of any patient with MSA is challenging. Additionally, there is such a discrepancy between the rate of progression of symptoms in MSA and that in PD that matching would likely be difficult. Additionally, matching between all three groups (including healthy older adults) should be improved upon in future studies in order to 38
39 ensure that the findings of this study namely, that the MSA group was significantly younger than the other groups could be reliably replicated. In summary, this study provides preliminary findings regarding the relationship between swallow and cough in patients with multiple-system atrophy and a comparison to cough and swallow in patients with Parkinson s disease, allowing for increased understanding of a population that is underrepresented in current literature. In addition, it offers a foundation for future research on the airway protective mechanisms in MSA, which is a critical area of exploration for this vulnerable patient group. 39
40 LIST OF REFERENCES Dodds, W. J., Stewart, E. T., & Logemann, J. A. (1990). Physiology and radiology of the normal oral and pharyngeal phases of swallowing. AJR. American journal of roentgenology, 154(5), Dornisch, S. (2016). Oropharyngeal swallowing in the parkinsonian syndromes: A retrospective description and comparison. Available from University of Florida Digital Collections. Faniciulli, A., & Wenning, G. K. (2015). Multiple-system atrophy. New England Journal of Medicine, 372, doi: /nejmra Hegland, K.W., Troche, M.S., Brandimore, A., Okun, M.S., & Davenport, P.W. (2016). Comparison of two methods for inducing reflex cough in patients with Parkinson s disease, with and without dysphagia. Dysphagia, 31(1), Doi: /s Higo, R., Nito, T., & Tayama, N. (2005). Swallowing function in patients with multiplesystem atrophy with a clinical predominance of cerebellar symptoms (MSA-C). European Archives of Oto-Rhino-Laryngology, 262(8), doi: /s Higo, R., Tayama, N., Nitou, T., Watanabe, T., & Ugawa, Y. (2003). Videofluoroscopic and manometric evaluation of swallowing function in patients with multiple system atrophy. Annals of Otology, Rhinology & Laryngology, 112(7), Higo, R., Tayama, N., Watanabe, T., Nitou, T., & Takeuchi, S. (2003). Vocal fold motion impairment in patients with multiple system atrophy: evaluation of its relationship with swallowing function. Journal of Neurology, Neurosurgery, and Psychiatry, 74(7), Litvan, I., Mangone, C. A., McKee, A., Verny, M., Parsa, A., Jellinger, K.,... Pearce, R. (1996). Natural history of progressive supranuclear palsy (steele-richardsonolszewski syndrome) and clinical predictors of survival: A clinicopathological study. Journal of Neurology Neurosurgery and Psychiatry, 60(6), doi: /jnnp Müller J, Wenning GK, Verny M, McKee A, Chaudhuri KR, Jellinger K, Poewe W, Litvan I (2001). Progression of Dysarthria and Dysphagia in Postmortem-Confirmed Parkinsonian Disorders. Archives of Neurology, 58(2), doi: /archneur Nagaya, M., Kachi, T., Yamada, T., & Igata, A. (1998). Videofluorographic study of swallowing in parkinson's disease. Dysphagia, 13(2), doi: /pl
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