EFFECTS OF BOLUS CONSISTENCY ON TIMING AND SAFETY OF SWALLOW

IN PARKINSON’S DISEASE

By

MICHELLE S. TROCHE

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

2006

Copyright 2005

by

Michelle S. Troche

iii

ACKNOWLEDGMENTS

There are so many people who have provided me with support and encouragement

throughout my journey thus far. I am abundantly grateful to God for placing each of

those people in my path.

I would especially like to thank my parents who have supported me in everything I

have done until now. It is their love, guidance, and wisdom that have molded me into the

person I am today. I must also thank my brother, Joshua, who not only provided his

expert trajectory measurement skills to this project, but also keeps me grounded and sane

on a daily basis.

It is with much gratitude that I also thank my committee for their mentorship and

guidance throughout this experience. I thank Dr. Christine Sapienza for providing me

with so many amazing professional and educationally enriching opportunities throughout

the four years I have been under her mentorship. Under her guidance, I have not only

grown as a researcher, student, and clinician, but also as an individual. I thank Dr.

Rosenbek whose undying passion for all aspects of speech-language pathology (i.e.,

patient care, education, research) is truly inspirational. His example of using just the

right amount of “brains” and just the right amount of “heart” in the care of patients is one

I hope to follow.

Lastly, I would like to thank my classmates, labmates, and friends, especially

Christina del Toro, whose enthusiasm and motivation were essential for the completion

iv

of this project and Karen Wheeler, who always made herself available to help, be it with

statistics, answering questions, or just listening to my theories. Many thanks to all.

v

TABLE OF CONTENTS page

ACKNOWLEDGMENTS ................................................................................................. iii

LIST OF TABLES............................................................................................................ vii

LIST OF FIGURES ......................................................................................................... viii

ABSTRACT.........................................................................................................................x

CHAPTER

1 INTRODUCTION ........................................................................................................1

Background...................................................................................................................1 Significance and Hypotheses......................................................................................12

2 METHODS.................................................................................................................14

Participants .................................................................................................................14 Clinical Assessment of Parkinson’s Disease Severity................................................15 Videoradiography .......................................................................................................16 Data Analysis..............................................................................................................18

Measurements Related to Swallow Timing.........................................................18 Measurements Related to Penetration/Aspiration ...............................................19 Measurements of Hyoid Motion..........................................................................20 Measures of Quality of Life ................................................................................21

Statistics......................................................................................................................22 Primary Aim ........................................................................................................22 Exploratory Study................................................................................................22

3 RESULTS...................................................................................................................23

Primary Aim ...............................................................................................................23 Reliability ............................................................................................................24 Statistical Analysis ..............................................................................................24

Exploratory Study: Hyoid Trajectory Measurements.................................................28 Reliability ............................................................................................................28 Statistical Analysis ..............................................................................................28 Case Studies.........................................................................................................30

vi

4 DISCUSSION.............................................................................................................39

Primary Aim ...............................................................................................................39 Measures of Bolus Transit...................................................................................39 Measures of Penetration/Aspiration ....................................................................42 Quality of Life .....................................................................................................43

Exploratory Study.......................................................................................................44 Limitations and Strengths ...........................................................................................47 Implications for Future Research................................................................................48 Implications for Swallow Intervention .......................................................................48

APPENDIX

A UNIFIED PARKINSON’S DISEASE RATING SCALE (UPDRS) .........................50

B THE SWAL-QOL SURVEY......................................................................................56

BIOGRAPHICAL SKETCH .............................................................................................74

vii

LIST OF TABLES

Table page 2-1 Participant Demographics ........................................................................................15

2-2 Hoehn and Yahr Scale..............................................................................................16

2-3 Tags of bolus oral and pharyngeal transit times.......................................................18

2-4 Penetration-Aspiration Scale....................................................................................19

3-1 Mean values for the dependent variables. ................................................................23

3-2 Pearson r correlation results for inter-rater reliability. .............................................24

3-3 Results of the MANOVA.........................................................................................25

3-4 Results of the one-way analysis of variance (ANOVA). .........................................25

3-5 Means and standard deviations for dependent variables as a function of bolus consistency. ..............................................................................................................26

3-6 Results of Pearson r correlations within the thin consistency. .................................27

3-7 Results of Pearson r correlations within the thick consistency. ...............................27

3-8. Intra-rater reliability for trajectory measurements....................................................28

3-9 Inter-rater reliability for trajectory measurements ...................................................28

3-10 Means and standard deviations of dependent measures as a function of bolus consistency. ..............................................................................................................28

3-11 Order of swallow events and hyoid trajectory measurements for “safe swallow”...30

3-12 Order of swallow events and hyoid trajectory measurements for “unsafe swallow”...................................................................................................................31

3-13 Order of swallow events and hyoid trajectory measurements for shorter swallow..34

3-14 Order of swallow events and hyoid trajectory measurements for longer swallow. .35

viii

LIST OF FIGURES

Figure page 2-1 Example of fluoroscopic image from where the measurements were completed....17

2-2 Figure depicting the reference line drawn from C3 to the hyoid prominence in frame one and a second line from a later frame .......................................................21

3-1 Figure depicting the change in average and max angle as a function of bolus consistency. ..............................................................................................................29

3-2 Figure depicting the change in average and max displacement as a function of bolus consistency......................................................................................................29

3-3 Figure depicting the change in average and max velocity as a function of bolus consistency. ..............................................................................................................30

3-4 Figure depicting the angle of the hyoid in degrees and the relationship to the defined swallow events in the “safe swallow”. ........................................................31

3-5 Figure depicting the angle of the hyoid in degrees and the relationship to the defined swallow events in the “unsafe swallow” .....................................................32

3-6 Figure depicting the displacement of the hyoid in millimeters and the relationship to the defined swallow events in the “safe swallow” ...........................32

3-7 Figure depicting the displacement of the hyoid in millimeters and the relationship to the defined swallow events in the “unsafe swallow” .......................33

3-8 Figure depicting the hyoid trajectory in the “safe swallow”. ...................................33

3-9 Figure depicting the hyoid trajectory in the “unsafe swallow”. ...............................34

3-10 Figure depicting the angle of the hyoid movement and the relationship to the defined swallow events in the shorter swallow. .......................................................35

3-11 Figure depicting the angle of the hyoid movement and the relationship to the defined swallow events in the longer swallow.........................................................36

3-12 Figure depicting the displacement of the hyoid in millimeters and the relationship to the defined swallow events in the shorter swallow ..........................36

ix

3-13 Figure depicting the displacement of the hyoid in millimeters and the relationship to the defined swallow events in the longer swallow...........................37

3-14 Figure depicting the hyoid trajectory in the shorter swallow...................................37

3-15 Figure depicting the hyoid trajectory in the longer swallow....................................38

x

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

EFFECTS OF BOLUS CONSISTENCY ON TIMING AND SAFETY OF SWALLOW IN PARKINSON’S DISEASE

By

Michelle S. Troche

May 2006

Chair: Christine Sapienza Major Department: Communication Sciences and Disorders

Safety and timing of swallow are essential for health and quality of life. The study

of swallow in Parkinson’s disease (PD) is especially important, in that aspiration

pneumonia is the leading cause of death in this population. One of the therapeutic

strategies employed in the treatment of swallowing problems is diet modification. The

primary aim of this study was to investigate the effects of bolus consistency on P-A score

and timing of the oral-pharyngeal swallow of persons with PD. The secondary goal was

to explore the relationship between various quantifiable components of hyoid movement

and measures of swallow timing and penetration/aspiration. The videoradiographic

images of ten participants with PD swallowing six thin, and six pudding thick boluses

were measured. The results demonstrated various significant differences and

relationships among the dependent variables (i.e., oral transit time, pharyngeal transit

time, number of tongue pumps, P-A score, and SWAL-QOL measures). The implications

for further research and clinical practice are discussed.

1

CHAPTER 1 INTRODUCTION

Background

Parkinson’s disease (PD) is a neurologic condition characterized by impairment of

the basal ganglia with death of dopaminergic neurons primarily in the substantia nigra

pars compacta (Brodal 1998; Marsden, 1984). Cardinal symptoms include skeletal

muscle rigidity, akinesia (inability to initiate movement), hypokinesia (reduced range of

movement with consequent target undershooting), bradykinesia (slowness of movements

once initiated), and resting tremor (Brodal, 1998; Hoehn & Yahr, 1967; Marsden, 1989).

The above mentioned physiological changes affect the various muscle systems and cause

changes at different levels of function. Of particular importance to this study, is the

presence of changes in the bulbar system.

One of the primary bulbar changes reported by patients with PD is speech

impairment. The speech of persons with PD, termed hypokinetic dysarthria, has been

studied to great extent (i.e., Darley, Aronson, & Brown, 1969a; 1969b; Canter, 1963,

1965a, b). Although persons with hypokinetic dysarthria do not comprise a homogenous

group, there are several predominant features affecting many domains of speech

including respiration, phonation, articulation, resonance, and prosody (Darley et al.,

1969a; 1969b). More specifically, speech associated with PD has been described as

slurred (Doshay, 1960) and has been characterized by monopitch, reduced stress,

monoloudness, imprecise consonants, variable rate, inappropriate pauses, short rushes,

and a harsh, breathy voice (Darley et al., 1969a, b; Canter, 1963, 1965a, b).

2

Along with these predominant speech characteristics, James Parkinson (1817) also

reported changes in swallow function associated with the disease. In his first published

description of PD, An Essay on the Shaking Palsy, he reported prepharyngeal

abnormalities of ingestion, including difficulty initiating the swallow, maintaining self-

feeding, impaired oral containment of both saliva and food, and labored lingual

movements. His observations have proven quite accurate, but since Parkinson’s essay,

much more research has been conducted in the area of normal swallowing function and

swallowing dysfunction in various populations, including PD (i.e., Ardran & Kemp,

1951; 1956; 1967; Blonsky, Logemann, Boshes, & Fisher, 1975, Bosma, 1957;

Logemann, 1983).

Swallowing is a complex process consisting of various pressure changes which

successfully transport a bolus from the oral cavity to the esophagus and into the stomach.

The healthy swallow consists of four main phases: (1) the oral-preparatory phase, in

which food is manipulated in the oral cavity; (2) the oral phase, at which time the tongue

propels the bolus to the posterior aspect of the mouth and the swallow is triggered; (3) the

pharyngeal phase, where the swallow is triggered and the bolus is transported through the

pharynx, and (4) the esophageal phase at which time peristalsis transports the bolus

through the esophagus and into the stomach (Logemann, 1983).

The different phases of swallow are controlled by various neural substrates. The

oral-preparatory phase, which is considered to be volitionally controlled, is mediated by

such cerebral structures as the cingulated cortex, insula, inferior frontal gyrus,

supplementary motor area, sensorimotor cortex, supplementary sensory area, premotor

cortex, antereolateral and posterior parietal cortex, basal ganglia, thalamus, and

3

cerebellum (Hamdy et al., 1996; Hamdy, Mikulis, Crawley, et al., 1999; Hamdy,

Rothwell, Brooks, et al., 1999; Hamdy, Xue, Valdez, & Diamant, 2001; Martin,

Goodyear, Gati, & Menon, 2001; Martin & Sessle, 1993; Mosier et al., 1999; Zald &

Pardo, 1999). Alternatively, it has been suggested that the pharyngeal phase of swallow,

which is mainly considered reflexive, is cortically controlled by indirect pathways

between extrapyramidal cortical motor planning regions and lower motor neurons

(Huckabee, Deecke, Cannito, Gould, & Mayr, 2003).

Persons with PD may experience changes in all the phases of swallow. It is

uncertain which phase of the swallow is most impaired with the disease and what

mechanisms are largely responsible for aspiration. Ali et al. (1996) stated that the

majority of patients with PD have dysphagia related to the oral-pharyngeal phase of

swallow, calling pharyngeal bolus transfer a “major determinant” of dysphagia in this

population. Bassotti, Germani, Pagliaricci, Plesa, & Giuletti (1998), on the other hand,

reported that esophageal motility was the most affected of the swallowing functions.

Interestingly, the vast majority of these studies have been conducted utilizing only one

consistency of bolus, which is difficult to generalize to the patients’ routine eating habits.

More specifically, the study of swallow function in those with PD indicates

changes to the oral phase of swallow relating to bolus preparation and also indicate the

presence of labial bolus leakage, deficient or hesitant mastication, impaired lingual

motility, lingual tremor, and slowed and limited mandibular excursion, all of which affect

the overall formation of the bolus (Ertekin et al., 2002: Leopold & Kagel, 1996). Oral

transit time is also often slowed in PD with changes including slow, repetitive lingual

pumping, inability to properly propel the bolus posteriorly, prolonged lingual elevation,

4

hesitancy in initiating the swallow, preswallow spill, and piecemeal deglutition (Blonsky

et al., 1975; Born, Harned, Rikkers, Pfeiffer, & Quigley, 1996; Coates& Bakheit, 1997;

Ertekin et al., 2002: Leopold & Kagel, 1996). Consequently, post swallow residue in the

oral cavity is often observed (Ali et al., 1996; Nagaya, Kachi, Yamada, & Igata, 1998;

Stroudley & Walsh, 1991).

Many changes also occur in the pharyngeal phase of swallow. Pharyngeal transit

time is reported to be slow due to various symptoms causing dysfunction in the

pharyngeal phase. Some of these changes include abnormal or delayed contraction of the

pharyngeal wall with subsequent coating of the walls (Ali et al., 1996), deficient

epiglottic positioning, decreased epiglottic range of motion, stasis in the valleculae and/or

pyriform sinuses (Blonsky et al., 1975; Ertekin et al., 2002; Leopold & Kagel, 1997),

slow laryngeal elevation and excursion, aspiration, UES incoordination, as well as

cricopharyngeal dysfunction (Ali et al., 1996; Born et al., 1996; Bushmann, Dobmeyer,

Leeker, & Perlmutter, 1989; Coates & Bakheit, 1997; Eadie & Tyrer, 1964).

Finally, changes in esophageal function which lead to prolonged transit times

include decreased peristaltic motion, especially in the inferior third of the esophagus

(Blonsky et al., 1975; Born et al., 1996), and delayed opening of the LES leading to

gastro-esophageal reflux disease (Castell et al., 2001; Leopold & Kagel, 1997; Nagaya et

al., 1998; Stroudley & Walsh, 1991).

The swallow mechanism as a whole is itself composed of many structures; the

muscles of which are both of the striated and smooth type. The smooth muscle is

controlled by the autonomic nervous system and may cause changes in esophageal and

pharyngeal transit times due to motility changes evidenced by decreased peristalsis

5

(Athlin, Norberg, Axelsson, Moller, & Nordstrom, 1989; Lieberman et al., 1980).

Changes due to the cardinal symptoms of PD are also observed in the swallow system

with decline in motoric abilities due to rigidity, hypokinesia, and tremor; processes

controlled by dopaminergic pathways (Lieberman et al., 1980). Specifically, rigidity and

bradykinesia are likely responsible for difficulty chewing and drooling of saliva. Eadier

& Tyrer (1965) and Ertekin et al. (2002) hypothesized that the hypokinetic, reduced rate

of spontaneous swallowing movements, and the “slowness of segmented but coordinated

sequential movements” a problem seen in other motor systems in PD, may be the most

significant cause of swallow dysfunction in PD. It is interesting to note, that often times

patients with PD demonstrate greater impairment of voluntary tasks versus involuntary

tasks (Yamaguchi & Kabayashi, 1998). This is important to the understanding of

swallow dysfunction in PD due to the voluntary nature of the oral phase of swallow, and

the involuntary nature of the pharyngeal phase of swallow. In addition to the above-

mentioned mechanistic impairments, it has been reported that swallow dysfunction in PD

may be secondary to impairment of other mechanisms including autonomic processes,

perception, cognition, and emotion (Athlin et al., 1989).

Severity and degree of motor involvement in PD do not necessarily correlate with

severity of swallow dysfunction, making the timeline of swallow changes difficult to

predict (Ali et al., 1996). Similarly, clinical staging does not predict swallow difficulty

(Bushmann et al., 1989). For instance, the literature suggests that the Unified Parkinson

Disease Rating Scale (UPDRS; Fahn, Marsden, Calne, & Goldstein, 1987), which is used

to assess severity of the disease, does not predict swallowing dysfunction. In fact, Ali et

al. (1996) found no relation between limb tremor and lingual tremor and no relation

6

between muscular rigidity and dysmotility of the pharyngeal wall. The poor correlation

between swallowing dysfunction and disease severity rating, along with patient

complaints of swallow problems and findings on videofluoroscopic examinations makes

swallow assessment and subsequent treatment in PD a difficult task (Bushmann et al.,

1989).

Currently the primary treatment for PD is Levodopa (L-Dopa). L-Dopa has been

found to be efficacious for the treatment of the primary clinical features of the PD

syndrome (Calne, Shaw, Spiers, & Stern, 1970). The same results have not been

observed consistently in the treatment of dysphagia in PD (Born et al., 1996; Hunter,

Crameri, Austin, Woodward, & Hughes, 1997; Leopold & Kagel, 1997). Nilson,

Ekberg, Olsson, & Hindfelt (1996) assert that oral and pharyngeal function in PD are not

the result of reduced dopamine levels, therefore L-Dopa is ineffective. On the other

hand, Bushmann et al. (1989) found less vallecular residue and decreased coating of the

pharyngeal walls post treatment with L-dopa. The strongest theory as to the

ineffectiveness of dopaminergic medications in PD swallow is the dual involvement of

muscle tissue described previously. Therefore treatment for swallow dysfunction in PD

cannot be treated solely with medical interventions, but instead by compensatory

strategies and dietary modifications.

Dysfunction in swallow, also called dysphagia, can lead to many life-threatening

problems such as dehydration, malnutrition, weight loss, aspiration of solids and liquids,

and pneumonia (Bushmann et al., 1989; Raut, McKee, & Johnston, 2001). A timely and

safe swallow, is essential to health and quality of life. Assessment of swallow safety and

treatment of swallowing disorders is an integral part of a speech-language pathologist’s

7

scope of practice. Unfortunately, there are no clear cut guidelines regarding the amount

of aspiration which can occur in a specific patient before the patient is at severe risk for

pneumonia. Actually, physicians show variance in their tolerance for aspiration in

patients, with some tolerating only small amounts of aspiration, and others more. In

addition, of concern is whether or not the patient is healthy enough to combat a severe

infection like pneumonia; therefore, aspiration is kept to a minimum in order to avoid any

complications. Logemann (1983) suggests that health, mobility, cognition, frequency of

aspiration, and type of material aspirated all influence the body’s response to aspiration

and penetration. Rosenbek, Robbins, Roecker, Coyle, & Wood (1996) suggest that the

amount of aspiration, the extent to which the material passes into the airway, and the

ability of the person to expel the material are also crucial. Logemann (1983)

recommends that any patient who aspirates at least 10% of boluses of a specific

consistency, even following use of maneuvers and compensatory strategies, should

eliminate or restrict their oral consumption of boluses of said consistency.

Currently, the most effective method of determining presence and degree of

aspiration is videoradiographic evaluation; unfortunately though, this method cannot

elucidate the amount of aspiration a person can tolerate before pneumonia develops and

possible death ensues. There are few scales which actually quantify the swallow

impairment. The Penetration-Aspiration Scale (P-A Scale; Rosenbek et al., 1996) is

currently the most reliable measure. This ordinal measurement describes whether or not

the bolus has entered the airway, the degree to which it has entered the airway, whether

there is any residue, and whether the person tried to expel the material or not.

8

Although it has often been considered a feature of late stage PD (Lieberman et al.,

1980), dysphagia has also been reported in early stages of PD (Ali et al., 1996; Coates &

Bakheit, 1997; Stroudley & Walsh, 1991) and as a presenting symptom of the disease

(Croxson & Pye, 1988). These changes are of marked concern due to its association with

considerable morbidity from nutritional and pulmonary compromise (Ali et al., 1996;

Bassotti et al., 1998; Coates & Bakheit, 1997), as well as the possibility of death

(Kirshner, 1997; Stroudley & Walsh, 1991). In fact, aspiration pneumonia is the leading

cause of death in PD (Fernandez & Lapane, 2002; Gorell, Johnson, & Rybicki, 1994;

Hoehn & Yahr, 1967; Schiermier, Schafer, Schafer, Greulich, & Schlafke, 2001; Shill &

Stacy, 1998; Singer, 1992).

The incidence of dysphagia in persons with PD is hard to define, with evidence of

swallow dysfunction reported between 18.5% to 100% of the patients studied (Ali et al.,

1996; Bassotti et al., 1998; Coates & Bakheit, 1997; Hunter et al., 1997; Logemann,

Blonsky, & Boshes, 1975; Stroudley & Walsh, 1991), depending on the criteria and

instrumentation used to diagnose dysphagia and the participant population selected. In

comparison, studies assessing patients’ awareness of dysphagia have found only 15-50%

of these patients demonstrating signs of swallow dysfunction complain of dysphagia,

compared to 6-12% in age matched adults (Born et al., 1996; Logemann et al., 1975).

Therefore, many patients with PD are unaware of their swallowing dysfunction. In

addition, studies have found that as many as 15% of patients with PD who do not

complain of dysphagia do not recognize they are aspirating, termed silent aspiration (Ali

et al., 1996). It is this aspiration, in conjunction with a decreased cough strength and

9

delayed cough reflex, which places patients with PD at significant risk for complications

related to swallow dysfunction (Ertekin et al., 2002; Hunter et al., 1997).

Swallow timing, although less critical to health than swallow safety, has significant

implications for quality of life. As described above, persons with PD often develop

dysphagia early on in the disease process with tongue pumping arising as one of the first

symptoms. This tongue pump can cause increased oral transit times and therefore

increased eating time for the patient. These changes may have social or personal

repercussions which affect the person’s quality of life.

In order to aid the swallow function in patient populations, swallow therapy

strategies have been developed by clinicians. Swallowing maneuvers and other similar

compensatory strategies, although valuable in many populations, may be less beneficial

in the PD population which often has difficulties with cognition, including an inability to

maintain and shift sets, and problems with the coordination of complex tasks (i.e., Bayles,

1990; Cooper et al., 1991). This is significant because many compensatory strategies

used for swallow are often multi-step, complex motor movements. Such maneuvers

include the supraglottic swallow in which the patient is instructed to take a breath and

hold it while swallowing and then cough after the swallow, and the super-supraglottic

swallow, the instructions of which are the same as above, but the patient is instructed to

bear down while holding their breath (Martin, Logemann, Shaker, & Dodds, 1993;

Mendelsohn, & Martin, 1993; Ohmae, Logemann, Kaiser, Hanson, & Kahrilas, 1995;

Ohmae, Logemann, Kaiser, Hanson, & Kahrilas, 1996). Others include maneuvers such

as the Mendelssohn (Jacob, Kahrilas, Logemann, Shah, & Ha, 1989; Kahrilas, Dodds,

Dent, Logemann, & Shaker, 1988; Kahrilas, Logemann, Krugler, & Flanagan, 1991;

10

Lazarus, Logemann, & Gibbons, 1993; Logemann & Kahrilas, 1990) and Effortful

swallow (Bulow, Olsson, & Ekberg, 1999; Hind, Nicosia, Roeker, Carnes, & Robbins,

2001; Lazarus, Logemann, Song, Rademaker, & Kahrilas, 2002; Pouderoux & Kahrilas,

1995), where patients are asked to keep the larynx elevated for several seconds after the

swallow, and to swallow hard tightening the throat and neck muscles, respectively

(Logemann, 1983). The complex nature of these tasks, in conjunction with the cognitive

and working memory impairments often present, leave few options for the treatment of

swallowing disorders in persons with PD. This is of particular concern in that swallow

dysfunction can initiate in the early stages of PD, as can cognitive changes. Dietary

modifications may be most beneficial in this population.

Generalization and maintenance of maneuver and compensatory strategy use

outside of the clinic may be compromised by possible anosognosia, or unawareness of

deficits associated with illness, in patients with PD. Although little research has been

conducted in the area of anosgnosia in PD, Starkstein et al. (1996) and Seltzer,

Vasterling, Mathias, & Brennan (2001) found that patients with PD did demonstrate

some anosognosic symptoms, although not as severe as those observed in Alzheimer’s

disease. Clinically, it seems that the symptoms observed in patients with PD can more

accurately be described as a problem of “insight.” Often times patients with PD require

much more cueing during and before tasks in order for the tasks to be completed

accurately and appropriately, this may be a function of both working memory

dysfunction and “insight” deficits, impeding the patient from completing the tasks to their

maximum performance. It is these problems of generalization and maintenance, coupled

11

with the challenge of learning the often complex maneuvers, that may make this type of

swallow therapy a real challenge in this population.

Dietary modifications as a treatment strategy for oral-pharyngeal dysphagia

normally consist of thickening liquids or recommending puree consistency foods (Raut et

al., 2001). Although there is research investigating the effects of consistency on swallow

in healthy adults, healthy older adults, and persons with dysphagia caused by stroke and

other neurological conditions, consistency differences related to swallow function in PD

has not been adequately studied.

In terms of diet modification, thicker liquids have been used based on the theory

that perhaps the thickened liquid stimulates the pharynx to contract harder and longer in

order to protect the airway more adequately (Raut et al., 2001). Research involving

healthy ageing persons and others with dysphagia secondary to stroke reports results

demonstrating that as a liquid becomes more viscous duration of tongue base posterior

pharyngeal wall contact increases, oral-pharyngeal transit time increases, pharyngeal

delay times decrease, duration of peristaltic waves are longer, and average EMG activity

is increased (Ding, Logemann, Larson, & Rademaker, 2003; Kendall, Leonard, &

McKenzie, 2001; Kuhlemeier, Palmer, & Rosenberg, 2001). Increases in oral-pharyngeal

pressures and velocities are needed in order to propel the bolus into the pharynx (Hiss,

Strauss, Treole, Stuart, & Boutilier, 2004).

Research has also focused greatly on the movement of the hyoid bone during

swallowing of differing consistencies in healthy normal controls and persons with

neurological impairment (not including PD), with some controversy. Some of the

literature shows that thicker boluses can lead to greater hyoid displacements and

12

subsequently higher magnitudes of laryngeal movement, but shorter laryngeal elevation

durations (Dantas & Dodds, 1990; Dantas, Dodds, Massey, & Kern, 1989; Ertekin et al.,

1997), yet other researchers have found just the opposite (Bisch, Logemann, Rademaker,

Kahrilias, & Lazarus, 1994; Ekberg, Liedberg, Owall, 1986; Perlman, Vandaele, &

Otterbacker, 1995). Nonetheless, research using EMG has consistently found a positive

relationship between bolus viscosity and activation magnitude and duration of the

suprahyoid and infrahyoid muscles (Dantas & Dodds, 1990; Palmer, Luschei, Jaffe, &

McCulloch, 1999).

Significance and Hypotheses

There are many unanswered questions related to the effects of bolus consistency on

the oral and pharyngeal phases of swallow in PD. Of more concern, is the fact that these

variables have not been described in relationship to the swallow timing and

penetration/aspiration, which are both factors essential to health and quality of life in this

population which has a high incidence of dysphagia and aspiration pneumonia (often

resulting in death). To the researcher’s knowledge, no well-controlled study has ever

looked at both the oral and pharyngeal phases of swallow as related to bolus consistency

in the same group of participants with PD, with special attention to swallow timing and

penetration/aspiration; a topic of great clinical significance. The primary aim of this

study is to investigate the effects of bolus consistency on the P-A score and timing of the

oral-pharyngeal swallow of persons with PD. The secondary goal of this study is to

explore the relationship between the various quantifiable components of hyoid movement

and measures of swallow timing and penetration/aspiration.

The following questions and hypotheses were developed for study:

13

1. What are the effects of bolus consistency on the timing of swallow in persons with PD as measured by oral and pharyngeal transit times and number of tongue pumps? It was hypothesized that both oral and pharyngeal transit times would increase with thicker consistencies versus thinner consistencies. It was also hypothesized that oral transit time would be increased to a greater degree across the consistency condition and that the number of tongue pumps would increase significantly with thicker consistencies.

2. What are the effects of bolus consistency on Penetration-Aspiration Scale in persons with PD? It was hypothesized that P-A scale values would decrease with thicker consistencies, than thinner consistencies, indicating increased safety of swallow.

3. Is there a relationship between timing and penetration/aspiration within the thick and thin consistency conditions? It was hypothesized that there would be a significant negative correlation between oral and pharyngeal transit times and P-A scale values for the thick and thin consistencies.

4. Do the distinct changes evidenced in the swallow of persons with PD translate to changes in quality of life as measured by the SWAL-QOL? It was hypothesized that persons with more impaired oral stages of swallow would report more impaired quality of life.

14

CHAPTER 2 METHODS

Participants

Ten (5 male; 5 female; mean age 68.5 years; Table 2-1) participants with idiopathic

Parkinson’s disease (PD) were recruited from the University of Florida (UF) and Malcom

Randall Veterans Affairs (VA) Medical Center Movement Disorders Clinics in

Gainesville, Florida. All participants were on one or more anti-Parkinsonian

medications (i.e., Levodopa/Carbidopa, Selegeline, Amantadine etc).

Inclusionary criteria included: 1) age between 35-80 years; 2) diagnosis of

idiopathic Parkinson’s disease by a movement disorders neurologist; 3) moderate clinical

disability level (II-III; Hoehn & Yahr, 1967); and 4) score of at least 24 on the Mini-

Mental State Examination (Folstein, Folstein, & McHugh, 1975).

Exclusionary criteria included: 1) other neurological disorders; 2) gastrointestinal

disease; 3) gastro-esophageal surgery; 4) head and neck cancer; 5) history of breathing

disorders or diseases; 6) untreated hypertension; 7) heart disease; 8) history of smoking in

the last five years; 9) failing the screening test of pulmonary functions; and 10) difficulty

complying due to neuropsychological dysfunction (i.e., severe depression).

Once patients were screened for inclusionary and exclusionary criteria, participants

gave written consent and were subsequently enrolled in the study. The study was

approved by the UF and VA Institutional Review Boards (154-2003). Participants were

all “on” PD medications when the testing was conducted. They were tested one-hour

after medications were taken in order to help ensure measures were completed at optimal

15

medication activity (Nutt, 1987). In addition, all participants reported feeling “on” their

medications, and none of the patients showed signs of dyskinesias.

Table 2-1. Participant Demographics Participant

No. Gender Age H & Y

1 F 56 2 2 F 74 2 3 M 71 2 4 M 73 2 5 M 76 2 6 M 77 2 7 M 56 2 8 F 76 3 9 F 63 2 10 F 63 2

Clinical Assessment of Parkinson’s Disease Severity

Each patient underwent a clinical assessment of Parkinson’s disease severity. This

assessment was completed by a UF Movement Disorders neurologist. Severity was

measured using the Unified Parkinson’s Disease Rating Scale (UPDRS; Fahn et al., 1987;

Appendix A) and Hoehn & Yahr Scale (1967; Table 2-2). The UPDRS quantifies the

primary and secondary motor symptoms of a person with PD by assessing cognition,

ability to perform activities, mentation, activities of daily living, and neurological

examination. For the purposes of this clinical assessment, only the motor exam portion

(III) of the UPDRS was utilized. The Hoehn & Yahr scale is based on five stages, and is

an objective measure used to grade presence of tremor, rigidity, bradykinesia, and

postural instability.

16

Table 2-2. Hoehn and Yahr Scale (1967) Stage Characteristics 1 Signs and symptoms on one side only

Symptoms mild Symptoms inconvenient, but not disabling Usually present with tremor of one limb Friends have noticed changes in posture, locomotion, and facial expression

2 Symptoms are bilateral Minimal disability Posture and gait affected

3 Significant slowing of body movements Early impairment of equilibrium on walking or standing Generalized dysfunction that is moderately severe

4 Severe symptoms Can still walk to a limited extent Rigidity and bradykinesia No longer able to live alone Tremor may be less than earlier stages

5 Chachectic stage Invalidism complete Cannot stand or walk Requires constant nursing care

Videoradiography

Swallowing function was visualized and studied using videofluoroscopy. Patients

were seated upright and images of barium swallows were recorded in the lateral view. A

penny was placed behind the ear in order to have a referent of known length for later

displacement measurements. In addition, a headband with a hanging copper-lined

triangle (i.e., Chi-Fishman & Sonies, 2000) was in place controlling for head posture

changes and facilitating later displacement measures (Figure 2-1). A properly collimated

Phillips Radiographic/Fluoroscopic unit that provides a 63-kV, 1.2-m-A type output for

full field of view mode was used. Fluoroscopic images were recorded to a Kay

Elemetrics Swallowing Signals Lab (Kay Elemetrics, Lincoln Park, NJ) using a digital

scan converter and were electronically recorded at 30 frames per second.

17

Included in the field of view, at the very least, were the lips and teeth anteriorly,

nasal spine superiorly, cervical spine posteriorly, and upper esophageal sphincter

inferiorly, allowing for a complete visualization of the oral and pharyngeal structures

involved in swallow, specifically those needed for the measurements completed for this

protocol: the tongue, ramus of the mandible, hyoid bone, and upper esophageal sphincter.

Figure 2-1. Example of Fluoroscopic image from where the measurements were

completed. Note penny and copper triangle headband for measurement purposes.

Participants completed a dry swallow, six 5 cc. trials of pudding thick liquid

(Varibar Pudding-Barium Sulfate Esophageal Paste 230 mL 40% w/v, 30% w/w from E-

Z-EM) in a spoon, and six 5 cc trials of thin liquid (Liquid E-Z Paque Barium Sulfate

Suspension; 60% w/v, 41% w/w; from E-Z-EM) in a cup. Trials were presented in

random order, in order to control for fatigue and other effects related to order of bolus

presentation. In order to approximate the everyday feeding conditions of the patient, the

cup and spoon were utilized; all the patients fed themselves in the home, therefore they

18

self-fed during all trials. Patients were given the spoon or cup and prompted by the

clinical researcher to “place the liquid in your mouth and swallow when you are ready.”

Data Analysis

Measurements Related to Swallow Timing

Measurements of bolus transit were completed by analyzing the recordings of

swallow trials frame-by-frame or in slow-motion using the Kay Swallow station. The

measurements were completed by an examiner trained in the analysis of modified barium

swallow studies. The examiner was blinded to the patients’ identity. Tags were placed at

various swallow events in order to facilitate measurement. The swallow events measured

are explained in detail in Table 2-3. These measurements were selected in order to

capture the effects of bolus consistency on the timing of the swallow in persons with PD.

Using these events, measurements of oral and pharyngeal transit times were completed.

Table 2-3. Tags of bolus oral and pharyngeal transit times Onset of Oral Transit Time Onset of posterior movement by the

bolus in the oral cavity Point at which the tongue tip is raised and the bolus begins posterior movement towards the posterior aspect of the oral cavity.

Offset of Oral Transit Time Point at which the tail of the bolus passes the level of the ramus of the mandible

Onset of Pharyngeal Transit Time Point at which the leading edge of the bolus passes the level of the ramus of the mandible.

Offset of Pharyngeal Transit Time Point at which the tail of the bolus passes through the upper esophageal sphincter (UES).

Number of tongue pumps Number of times the tongue pumps (rocks) while the bolus is in the oral cavity, resulting in the posterior movement of the bolus and the initiation of the swallow reflex.

19

Measurements Related to Penetration/Aspiration

In order to assess the penetration/aspiration of swallows of different consistencies,

the Penetration-Aspiration Scale (P-A Scale; Rosenbek et al., 1996; Table 2-4) was used

to rate each swallow. The P-A Scale is used to measure whether or not material entered

the airway and if it did, whether the residue remained or was expelled. These

measurements were also completed using frame-by-frame analysis by an expert rater who

was blinded to the participant’s identity.

Table 2-4. Penetration-Aspiration Scale 1 Contrast does not enter the

airway

No Penetration/Aspiration

2 Contrast enters the airway, remains above the vocal folds

Penetration

3 Contrast remains above the vocal folds with visible residue

Penetration

4 Contrast contacts vocal folds, no residue

Penetration

5 Contrast contacts vocal folds, visible residue

Penetration

6 Contrast passes glottis, no sub-glottic residue

Aspiration

7 Contrast passes glottis, visible sub-glottic residue despite patient response

Aspiration

8 Contrast passes glottis, visible sub-glottic residue, absent of patient response

Aspiration

(Rosenbek et al., 1996)

20

Measurements of Hyoid Motion

In order to better assess the function of the hyoid bone, trajectory measurements

were completed. These measurements are used to determine the hyoid anterior and

superior pattern of excursion and depict the pattern of movement as related to the bolus

location.

The data was collected from two randomly selected swallows of six (three men,

three women) of the previous ten participants. The measurements were completed by an

expert rater with experience measuring hyoid trajectories. In order to complete these

measures, using dpsReality Video Editor, the JPG images for each frame of the

individual swallows were extracted. The images extracted were those between the point

when the bolus first began its posterior movement and the point when the bolus tail

entered the UES. These images were then imported and analyzed using a Matlab 7.0.1

routine (Wheeler, Martin-Harris, Bronsky, & Sapienza, 2006), which was developed at

the University of Florida.

The imported files were then presented in random order to the measurer. The

measurer picked two points in each frame. One point was the anterior most portion of C3

and the other the anterior portion of the hyoid bone. Once this was completed, the

program presented the frames in sequential order and the rater tagged the various

swallow events which were chosen for analysis. In this study the swallow events chosen

were: 1) onset of bolus posterior movement, 2) point when the bolus head arrived at the

level of the ramus of the mandible, 3) point when the palate first made contact with the

posterior pharyngeal wall, 4) point of maximum laryngeal elevation, 5) point at which the

bolus entered the UES, 6) point at which the UES closed, following the passing of the

bolus, and 7) point when the palate lowered from the palate. Once the analysis was

21

complete, the program provided a figure depicting the motion of the hyoid bone, a

spreadsheet with the angle and displacement measures, and figures representing

displacement and angle in pixels and millimeters. The program obtains the angle

measurements from a reference line drawn from the anterior portion of C3 to the anterior

prominence of the hyoid bone in frame one (Figure 3-2). The displacement measures are

also obtained using C3 as a referent. The use of the penny marker, allows for the

translation of pixel measurements to actual millimeters.

Figure 2-2. Figure depicting the reference line drawn from C3 to the hyoid prominence in frame one and a second line from a later frame.

Measures of Quality of Life

In addition, the patients’ quality of life as related to swallow function was

measured using a perceptual self-rating scale, Swallowing Quality of Life Questionnaire

(SWAL-QOL; McHorney, Bricker, Kramer, et al., 2000; McHorney, Bricker, Robbins, et

al., 2000; McHorney et al., 2002; Appendix B). This tool includes questions regarding

both the oral and pharyngeal phases of swallow as well as appetite, eating duration, and

other factors affecting swallow function. Completing these measures allows for the

assessment of persons’ awareness of their swallowing deficits.

C3

22

Statistics

Primary Aim

A one way analysis of variance was used to assess the effect of bolus consistency

on the dependent measures (i.e., oral transit, pharyngeal transit, number of tongue pumps,

P-A score). Pearson r correlations were used to assess the relationships of the dependent

variables within consistencies. Lastly, descriptive statistics were used to identify outliers

and questions for further study.

Exploratory Study

Due to the small sample size in this pilot project, descriptive statistics together with

scatter plots and visual analysis of output from the MATLAB program were used to

identify trends, outliers, and evidence for formulation of further research questions.

23

CHAPTER 3 RESULTS

Primary Aim

Hypotheses 1-4 were tested by completing measures of timing and

penetration/aspiration on six thin consistency and six thick consistency swallows in ten

patients (5 male, and 5 female) with PD. The mean data for each dependent variable are

presented below in Table 3-1.

Table 3-1. Mean values for the dependent variables (for consistency, 1=thin, 2=thick). Subj No. Consistency OTT PTT

Tongue Pumps

PA Scale

Swal-qol

1 1 1.527 1.561 1.000 1.333 176 1 2 4.433 2.389 6.833 1.000 2 1 0.945 0.889 0.167 3.333 208 2 2 5.533 3.139 3.667 1.333 3 1 1.374 0.823 2.000 1.667 211 3 2 2.931 1.716 4.000 1.000 4 1 0.553 0.656 0.167 2.833 207 4 2 1.079 0.959 0.667 1.000 5 1 0.729 0.998 0.167 1.167 204 5 2 1.187 0.623 0.833 1.000 6 1 0.295 0.489 0.500 1.500 138 6 2 1.254 0.470 1.000 1.167 7 1 1.193 0.642 0.167 1.333 156 7 2 1.604 0.612 0.500 1.000 8 1 1.146 0.842 0.167 1.000 193 8 2 2.261 1.269 2.333 1.000 9 1 0.361 0.762 0.000 1.000 211 9 2 2.475 0.548 3.833 1.000 10 1 1.035 0.646 0.000 4.000 212 10 2 1.182 0.642 1.833 1.167

24

Reliability

Pearson r correlations were conducted in order to assess inter-rater reliability for

measures of swallow timing and penetration/aspiration. All measures were found to be

reliable at p≤0.05 showing moderate to strong correlations between the ratings of the two

measurers (Table 3-2).

Table 3-2. Pearson r correlation results for inter-rater reliability. Dependent Variable Pearson r coefficient Alpha

Oral transit time .989** .000

Pharyngeal transit time .883** .000

No. of Tongue Pumps .759** .004

P-A Score .674* .016

*correlation is significant at the 0.05 level (two-tailed). **correlation is significant at the 0.01 level (two-tailed) Statistical Analysis

A multivariate analysis of variance (MANOVA) with covariates of gender and

consistency was completed in order to determine if there were any significant effects of

gender or interactions between gender and consistency on the dependent measures. The

MANOVA showed no significance for gender (Table 3-3). Significance level was set at

0.05.

Therefore, a one-way analysis of variance (ANOVA) was used to analyze the

results of the dependent variables (oral transit time, pharyngeal transit time, number of

tongue pumps, and P-A Scale) as a function of bolus consistency (i.e., thin vs. pudding

thick). Results of this ANOVA (presented in Table 3-4) revealed significant differences

(p≤0.02) between oral transit time (p=0.008), number of tongue pumps (p=0.005), and P-

25

A scale (p=0.023) with bolus consistency. No significant difference was found for

pharyngeal transit time (p=0.196) as a function of bolus consistency

Table 3-3. Results of the MANOVA.

Multivariate Testsb

.894 27.360a 4.000 13.000 .000

.106 27.360a 4.000 13.000 .0008.419 27.360a 4.000 13.000 .0008.419 27.360a 4.000 13.000 .000

.221 .922a 4.000 13.000 .481

.779 .922a 4.000 13.000 .481

.284 .922a 4.000 13.000 .481

.284 .922a 4.000 13.000 .481

.688 7.160a 4.000 13.000 .003

.312 7.160a 4.000 13.000 .0032.203 7.160a 4.000 13.000 .0032.203 7.160a 4.000 13.000 .003

.291 1.332a 4.000 13.000 .310

.709 1.332a 4.000 13.000 .310

.410 1.332a 4.000 13.000 .310

.410 1.332a 4.000 13.000 .310

Pillai's TraceWilks' LambdaHotelling's TraceRoy's Largest RootPillai's TraceWilks' LambdaHotelling's TraceRoy's Largest RootPillai's TraceWilks' LambdaHotelling's TraceRoy's Largest RootPillai's TraceWilks' LambdaHotelling's TraceRoy's Largest Root

EffectIntercept

GENDER

CONSIST

GENDER * CONSIST

Value F Hypothesis df Error df Sig.

Exact statistica.

Design: Intercept+GENDER+CONSIST+GENDER * CONSISTb.

Table 3-4. Results of the one-way analysis of variance (ANOVA). ANOVA

10.924 1 10.924 8.743 .00822.490 18 1.24933.414 19

.824 1 .824 1.803 .1968.224 18 .4579.048 19

22.396 1 22.396 9.951 .00540.511 18 2.25162.906 19

3.612 1 3.612 6.210 .02310.468 18 .58214.080 19

Between GroupsWithin GroupsTotalBetween GroupsWithin GroupsTotalBetween GroupsWithin GroupsTotalBetween GroupsWithin GroupsTotal

Oral Transit Time

Pharyngeal Transit Time

Tongue Pumps

PA Scale

Sum ofSquares df Mean Square F Sig.

Table 3-5 presents the mean data for each of the dependent variables for the thin

and thick consistencies. Oral transit time was longer with the pudding thick consistency

than the thin consistency. The number of tongue pumps increased with the pudding thick

26

consistency, than the thin consistency. P-A score was lower with the pudding thick

consistency than the thin consistency.

Table 3-5. Means and standard deviations for dependent variables as a function of bolus consistency.

Thin Thick Dependent Variable Mean St Dev Mean St Dev Oral Transit Time 0.916 0.420 2.394 1.524 Pharyngeal Transit Time 0.831 0.296 1.237 0.909 Number of Tongue Pumps 0.433 0.625 2.550 2.028 P-A Scale 1.917 1.072 1.067 0.117

The third hypothesis was that there would be a significant negative correlation

between oral and pharyngeal transit times and P-A scale values for the thick and thin

consistencies. The fourth hypothesis was that persons with more impaired oral stages of

swallow would report more impaired quality of life. A Pearson r correlation was

conducted in order to assess the relationship between the various dependent measures

within each bolus consistency. Results of the Pearson r correlation are presented in

Tables 3-6 and 3-7. There were no significant correlations between the dependent

measures within the thin consistency.

Various significant relationships were identified within the thick consistency

boluses. For the thick consistency, significant positive relationships (p< 0.05) were

found between oral transit and pharyngeal transit times (p=.000, r=.939), number of

tongue pumps and oral transit (p=.007, r=.789), and tongue pumps and pharyngeal transit

time (p=.029, r=.683). No significant relationship was found between any of the

dependent measures and swallow quality of life or P-A score in either of the

consistencies.

27

Table 3-6. Results of Pearson r correlations within the thin consistency.

Correlations

1 .586 .515 .005 .074. .075 .128 .989 .840

10 10 10 10 10.586 1 .314 -.248 .125.075 . .376 .490 .731

10 10 10 10 10.515 .314 1 -.212 -.013.128 .376 . .557 .971

10 10 10 10 10.005 -.248 -.212 1 .390.989 .490 .557 . .265

10 10 10 10 10.074 .125 -.013 .390 1.840 .731 .971 .265 .

10 10 10 10 10

Pearson CorrelationSig. (2-tailed)NPearson CorrelationSig. (2-tailed)NPearson CorrelationSig. (2-tailed)NPearson CorrelationSig. (2-tailed)NPearson CorrelationSig. (2-tailed)N

Oral Transit Time

Pharyngeal Transit Time

Tongue Pumps

PA Scale

Swal-qol

Oral TransitTime

PharyngealTransit Time

TonguePumps PA Scale Swal-qol

Table 3-7. Results of Pearson r correlations within the thick consistency. Correlations

1 .939** .789** .408 .169. .000 .007 .241 .642

10 10 10 10 10.939** 1 .683* .426 .226.000 . .029 .220 .531

10 10 10 10 10.789** .683* 1 -.003 .199.007 .029 . .993 .582

10 10 10 10 10.408 .426 -.003 1 -.003.241 .220 .993 . .993

10 10 10 10 10.169 .226 .199 -.003 1.642 .531 .582 .993 .

10 10 10 10 10

Pearson CorrelationSig. (2-tailed)NPearson CorrelationSig. (2-tailed)NPearson CorrelationSig. (2-tailed)NPearson CorrelationSig. (2-tailed)NPearson CorrelationSig. (2-tailed)N

Oral Transit Time

Pharyngeal Transit Time

Tongue Pumps

PA Scale

Swal-qol

Oral TransitTime

PharyngealTransit Time

TonguePumps PA Scale Swal-qol

Correlation is significant at the 0.01 level (2-tailed).**.

Correlation is significant at the 0.05 level (2-tailed).*.

28

Exploratory Study: Hyoid Trajectory Measurements

Reliability

Recent investigations have found that the University of Florida hyoid trajectory

program measurements are highly reliable. A recent study by Wheeler et al. (2006),

found both intra and inter-rater reliability to be high (Tables 3-8 & 3-9).

Table 3-8. Intra-rater reliability for trajectory measurements Dependent Variable

Pearson r coefficient

Alpha value

Average Angle .942 .000 Average Displ .823 .001 Max Angle .945 .000 Max Displacement .872 .000 Table 3-9. Inter-rater reliability for trajectory measurements Dependent Variable

Pearson r coefficient

Alpha value

Average Angle .975 .000 Average Displ .895 .003 Max Angle .966 .000 Max Displacement .793 .019

Statistical Analysis

Due to the nature of this pilot work, (i.e., small n, no data norms) mainly

descriptive statistics (Table 3-10) were used in order to identify any possible preliminary

effects.

Table 3-10. Means and standard deviations of dependent measures as a function of bolus consistency.

Thin Thick Dependent Variables Mean St Dev Mean St Dev Average Angle 4.64 1.67 6.19 3.50 Max Angle 10.95 3.50 15.17 4.85 Average Displacement 3.41 2.58 3.11 2.26 Max Displacement 11.53 3.92 13.60 3.52 Average Velocity 43.56 11.06 46.33 15.99 Max Velocity 154.00 45.99 161.20 47.28

29

The means of all, except one of the dependent measures were higher with the

thicker consistency (Figure 3-1 –3-3). The only dependent measure where this trend was

not observed was average displacement (Figure 3-2).

0.0000

2.0000

4.0000

6.0000

8.0000

10.0000

12.0000

14.0000

16.0000

Thin Thick

Ang

le (d

egre

es)

Average AngleMax Angle

Figure 3-1. Figure depicting the change in average and max angle as a function of bolus

consistency.

0.0000

2.0000

4.0000

6.0000

8.0000

10.0000

12.0000

14.0000

16.0000

Thin Thick

Dis

plac

emen

t (m

m)

Average DisplacementMax Displacement

Figure 3-2. Figure depicting the change in average and max displacement as a function

of bolus consistency.

30

0.0000

20.0000

40.0000

60.0000

80.0000

100.0000

120.0000

140.0000

160.0000

180.0000

Thin Thick

Velo

city

(Dis

plac

emen

t/Tim

e)

Average VelocityMax Velocity

Figure 3-3. Figure depicting the change in average and max velocity as a function of

bolus consistency.

Case Studies

Below the data output from the MATLAB hyoid trajectory program is provided for

a single subject with both a safe (P-A=1) and unsafe (P-A=8) swallow.

Table 3-11. Order of swallow events and hyoid trajectory measurements for “safe swallow”.

Swallow Event Frame No. Angle Displacement Velocity Onset Bolus Transit 1 0.157 1.279 42.641 Palatal onset 11 2.45 -0.154 34.900 Bolus at ramus 12 2.059 -0.609 15.144 UES opening 17 2.741 1.288 14.484 Max Laryngeal Closure 20 1.549 2.258 71.923 UES closing 27 0.220 5.028 17.711 Palatal offset 34 7.788 -2.136 32.096

Following are the figures depicting the trajectory of the hyoid in terms of angle and

in terms of displacement (Figures 3-4 through 3-9). Although the pattern of movement

is similar, in the “safe and “unsafe” swallows, in the “unsafe” swallow the first three

events (onset bolus transfer, palatal onset, and bolus head at ramus) have occurred within

31

the first four frames, whereas in the “safe” swallow the bolus doesn’t arrive at the ramus

until the twelfth frame.

Table 3-12. Order of swallow events and hyoid trajectory measurements for “unsafe swallow”.

Swallow Event Frame No. Angle Displacement Velocity Onset Bolus Transit 1 0.306 2.165 72.177 Palatal onset 2 1.586 -0.252 80.583 Bolus head at ramus 4 0.790 -1.630 34.430 UES opening 11 4.772 2.721 105.261 Max Laryngeal Closure 18 7.567 6.332 18.484 UES closing 23 5.487 5.425 31.386 Palatal offset 26 7.500 0.923 44.175

Figure 3-4. Figure depicting the angle of the hyoid in degrees and the relationship to the

defined swallow events in the “safe swallow”. Swallow events are labeled with asterisks.

32

Figure 3-5. Figure depicting the angle of the hyoid in degrees and the relationship to the

defined swallow events in the “unsafe swallow”. Swallow events are labeled with asterisks.

Figure 3-6. Figure depicting the displacement of the hyoid in millimeters and the

relationship to the defined swallow events in the “safe swallow”. Swallow events are labeled with asterisks.

33

Figure 3-7. Figure depicting the displacement of the hyoid in millimeters and the

relationship to the defined swallow events in the “unsafe swallow”. Swallow events are labeled with asterisks.

Figure 3-8. Figure depicting the hyoid trajectory in the “safe swallow”.

34

Figure 3-9. Figure depicting the hyoid trajectory in the “unsafe swallow”.

Below the data output from the MATLAB hyoid trajectory program is provided for

a participant with a shorter oral transit time because of little tongue pumping (TP=1) and

another with a much larger amount of tongue pumping and an increased oral transit time

(TP=7). P-A score was 1 for both swallows.

Table 3-13. Order of swallow events and hyoid trajectory measurements for shorter

swallow. Swallow Event Frame No. Angle Displacement Velocity Onset Bolus Transit 1 1.328 -1.028 34.262 Bolus head ramus 10 4.5023 -3.100 15.206 Palatal onset 45 0.808 3.632 3.141 Max Laryngeal Closure 50 4.280 5.223 6.767 UES opening 51 3.569 6.479 41.869 UES closing 58 3.234 8.438 26.700 Palatal offset 65 4.986 1.314 26.966

35

Table 3-14. Order of swallow events and hyoid trajectory measurements for longer swallow.

Swallow Event Frame No. Angle Displacement Velocity Onset Bolus Transit 1 2.173 0.811 27.029 Bolus head at ramus 71 2.460 1.851 42.338 Palatal onset 145 10.920 7.282 61.012 Max laryngeal Closure 147 15.765 7.719 13.113 UES opening 149 17.825 9.339 41.617 UES closing 156 17.154 7.485 51.887 Palatal Offset 165 8.851 8.856 22.010

Following are the figures depicting the trajectory of the hyoid in terms of angle and

in terms of displacement (Figures 3-10-3-15). There are great differences in the amount

of movement of the hyoid, with much more extraneous movement of the hyoid observed

in the swallow containing more tongue pumping. The order of the swallow events is the

same in both swallows, but the distribution of the events throughout the length of time is

quite different.

Figure 3-10. Figure depicting the angle of the hyoid movement and the relationship to

the defined swallow events in the shorter swallow. Swallow events are labeled with asterisks.

36

Figure 3-11. Figure depicting the angle of the hyoid movement and the relationship to

the defined swallow events in the longer swallow. Swallow events are labeled with asterisks.

Figure 3-12. Figure depicting the displacement of the hyoid in millimeters and the

relationship to the defined swallow events in the shorter swallow. Swallow events are labeled with asterisks.

37

Figure 3-13. Figure depicting the displacement of the hyoid in millimeters and the

relationship to the defined swallow events in the longer swallow. Swallow events are labeled with asterisks.

Figure 3-14. Figure depicting the hyoid trajectory in the shorter swallow.

38

Figure 3-15. Figure depicting the hyoid trajectory in the longer swallow.

39

CHAPTER 4 DISCUSSION

The current study assessed the effects of bolus consistency on swallow timing and

P-A score in persons with PD. The findings were mainly consistent with the hypotheses

set forth, with the exception of some minor differences that will be discussed in greater

detail below. The current study also presents exploratory data quantifying the motion of

the hyoid bone in relation to measures of bolus transit and penetration/aspiration. These

measures were obtained utilizing an innovative MATLAB program which provides

information about angle, displacement, and the order of events relative to hyoid motion.

The following discusses the research findings and their clinical importance.

Primary Aim

Measures of Bolus Transit

When measuring bolus transit, the primary dependent variables included oral transit

time, pharyngeal transit time, and number of tongue pumps. Both oral and pharyngeal

transit time have been used to address bolus transit in varying populations (i.e., De

Vincentiis et al., 2004; Han, Paik, & Park, 2001; Monte, da Silva-Junior, Braga-Neto,

Nobre e Souza, & Sales de Bruin, 2005; Nagaya et al., 1998; Robbins, Levine, Maser,

Rosenbek, & Kempster, 1993). In the current study, a significant difference was found in

oral transit time as a function of the thickness of the bolus, with oral transit time

increasing with thicker boluses. These findings are not surprising. Past research has

found that thicker consistencies lead to greater oral transit times (Dantas et al., 1990), but

40

this relationship had not been identified in the PD population, nor has the cause of the

increased oral transit time been discussed.

Increased oral transit times can be caused by various factors, many of which are

related to the motion of the tongue. The presence of tongue pumping in persons with PD

may not only affect the bolus movement from the anterior portion of the oral cavity to the

posterior portion, but may also affect the strength with which the bolus is propelled into

the pharynx. Although the presence of tongue pumping, also referred to as festination of

the tongue or lingual rocking, has been identified in persons with PD (i.e., Hunter et al.,

1997; Leopold et al., 1996; Nagaya et al., 1998), quantifying the number of tongue

pumps has never been completed to the researcher’s knowledge. This measure was

selected as the most obvious characteristic of the oral phase of swallow in persons with

PD, which was associated with an increase in oral transit time.

Results identified not only the effect of the differing consistencies on oral transit

time, but number of tongue pumps as a predictor of increased oral transit, with a

significant positive correlation found between number of tongue pumps and oral transit

time. This significantly positive relationship was only identified in the pudding thick

consistency. There was also a significant difference between the number of tongue

pumps in the thin versus the pudding thick consistencies. The literature discussing the

festinating tongue phenomenon states that this process is caused by bradykinesia and

rigidity of the tongue (Bushmann et al., 1989; Edwards, Quigley, & Pfeiffer, 1982).

There is little explanation as to why the tongue pumping does not occur as frequently in

thinner consistencies, or why there is no relationship between oral transit time and tongue

pumping in thinner consistencies.

41

It can be hypothesized that the thinner boluses lack of resistance to flow may

reduce the need for oral manipulation, thus causing spillage into the posterior portion of

the oral cavity, and possibly the pharynx. Since those with PD have difficulty

coordinating movements, as well as slowness and weakness of the oral musculature, it is

possible that the bolus moves to the posterior portion of the oral cavity before the

structures are prepared to receive the bolus and trigger the pharyngeal swallow. It is for

this reason that the relationship between tongue pumping, pharyngeal transit time, and P-

A score was addressed.

A significant relationship between tongue pumping and pharyngeal transit time was

identified through Pearson r correlations, with pharyngeal transit time increasing as

number of tongue pumps increased. This relationship provides insight into the

relationship between the oral phase of swallow and the pharyngeal phase. Even with this

defined relationship, a significant difference in pharyngeal transit time between the two

consistencies was not found. The fact that pharyngeal transit time did not change

significantly as a function of consistency may be due to limitations of the study like small

sample size and small bolus size, or may be due to the reflexive nature of the pharyngeal

phase in comparison to the more voluntary nature of the oral phase of swallow; especially

in this population who often exhibit more impairment in voluntary than involuntary

behaviors (Yamaguchi & Kabayashi, 1998). However, this does not explain the

relationship between tongue pumping and pharyngeal transit time. The fact that tongue

pumping was associated with increased pharyngeal transit time in the pudding thick

consistency, provides further support for the consideration of the swallow mechanism as

a more cohesive unit versus a mechanism consisting of separate phases which in the end

42

add up to a swallow. In addition, this data supports the case that the pharyngeal phase of

swallow, although reflexive by nature (i.e., Huckabee et al., 2003; Martin et al., 2001;

Martin & Sessle, 1993; Mosier et al., 1999), is also controlled or influenced somewhat by

voluntary mechanisms (Wheeler & Sapienza, 2006). In the case of this participant pool,

it can be hypothesized that the dysfunction of the base of tongue may have reduced the

pressure with which the bolus was propelled down the pharyngeal cavity, which could in

turn have had repercussions on pharyngeal transit times.

In summary, the data supported the hypotheses set forth by the investigators. It

was hypothesized that both oral and pharyngeal transit times would increase with thicker

consistencies versus thinner consistencies. Although the means were greater for both oral

and pharyngeal transit as a function of bolus consistency, pharyngeal transit did not

demonstrate significance. This finding also supported the hypothesis that oral transit

time would be increased to a greater degree across the consistency condition. Lastly, it

was hypothesized that the number of tongue pumps would increase significantly with

thicker consistencies, as was found in the data.

Measures of Penetration/Aspiration

Past research has found that thicker consistencies are safer for persons to ingest

than thinner consistencies because they reduce the possibilities of penetration and

aspiration (Bulow, Olsson, & Ekberg, 2003; Kuhlemeier et al., 2001). It is on this

premise that diet modification recommendations (i.e., thickner for thin liquids, or

modification to puree consistencies) have been based. A significant difference was found

between P-A score as a function of consistency, with P-A score being higher (less safe)

for thinner consistencies, supporting one of the hypotheses set forth. Interestingly, the

hypothesis that there would be a significant negative correlation between oral and

43

pharyngeal transit times and P-A scale values for the thick and thin consistencies was not

supported by the data in this study. Pearson r correlations did not show significant

relationships between oral transit time, pharyngeal transit time, and/or tongue pumps with

P-A score. This is somewhat surprising given the strong relationship identified in this

study between consistency, increased oral transit and the number of tongue pumps, as

well as the strong relationship identified in prior research between thicker consistencies

and penetration/aspiration of the bolus. Further discussion on the variables which could

have possibly contributed to this result are to follow in the discussion of the study’s

limitations.

Quality of Life

It was hypothesized that persons with more impaired oral stages of swallow would

report more impaired quality of life, but no significant relationships were found between

swallowing quality of life and other dependent measures, including

penetration/aspiration. This may be explained by the “anosognosic” nature of persons

with PD. This population is often considered to have decreased insight into their own

behaviors and medical severity (Starkstein et al., 1996, Seltzer et al., 2001).

Interestingly, the oldest participant reported the best swallowing quality of life, although

both the oral and pharyngeal phases of this participant’s swallow were no more or less

impaired than most of the other participants. This apparent reduced reliability of patients

with PD to recognize or quantify swallow impairment is important to note clinically.

This lack of insight may prove detrimental to health and safety in later stages of

dysphagia. It is therefore the responsibility of the clinician to judge a patient’s insight

into their own disorder, be it through interview or more extensive neuropsychological

testing, in order to make wise decisions involving management of dysphagia. These

44

issues can have negative implications for compliance of dietary modifications or use of

compensatory strategies, and/or may negatively influence therapy outcomes.

Exploratory Study

The hyoid bone is an essential member of the swallow mechanism. Together with

the suprahyoid muscles, this bone moves superiorly and anteriorly raising the larynx

which ultimately protects the airway during swallowing. Before the UF hyoid trajectory

program was developed, there had been no way to quantify the movements of the hyoid

and relate them to various swallow events, in an automated, time efficient manner. With

this program, investigators are able to quantify the angle and displacements of hyoid

motion during swallow. In the current exploratory study, these measures were obtained

and then compared to timing and penetration/aspiration measures in order to identify any

preliminary relationships between the hyoid motion and factors relating to swallow

timing and penetration/aspiration. In addition, various swallow events were overlayed on

the hyoid trajectory measurements in order to better identify and describe the factors

contributing to a safe or unsafe swallow. Also, the pilot data that was presented in the

results section was obtained and compared to the preliminary data of healthy adults.

These comparisons were made in order to identify differences in the motion of the hyoid

bone as a function of disease process, and thus describe factors which may be influencing

swallow safety and timing in patients with PD compared to healthy adults.

Comparison of the means of the various dependent measures acquired from the

MATLAB program (i.e., average and max angle, average and max displacement, and

average and max velocity) as a function of consistency showed increases in all the

measures related to hyoid movement with increased bolus thickness, except average

hyoid displacement. This is consistent with past research which has shown that with

45

increased bolus thickness there is a greater activation of the suprahyoid muscles as

measured by sEMG (Dantas & Dodds, 1990; Ding et al., 2003).

Preliminarily, it seems that there is a relationship between angle size and

penetration/aspiration of the bolus, but not a relationship between displacement and

penetration/aspiration of the bolus. Within the thin consistencies, the participant with the

largest average angle presented with a very safe swallow, and the person with the

smallest angle was among those with the least safe swallow. In addition, the latter

participant presented with the smallest maximum angle size. This is especially

interesting in light of data from healthy controls (Wheeler et al., 2006) which found that

angle was the only measure (of the dependents described above) which was not

significantly different from person to person. In other words it was the most consistent of

the measures within healthy controls, yet in this population of persons with PD there

seems to be great variability in the degree of angle produced with each swallow. This

increased variability may be consistent with decreased coordination of swallow and

subsequent differences in swallow safety, specifically penetration/aspiration.

A case study presenting evidence of decreased coordination of the oral-pharyngeal

phases of swallow resulting in an unsafe swallow was introduced in the results section.

In this case, one safe (P-A=1) and one unsafe (P-A=8) swallow, within the same patient,

was analyzed in order to compare hyoid trajectory measures. It was observed that

although the trajectory pattern itself was not much different between the two swallows

and the order of the swallow events was no different, the speed with which the swallow

events occurred was quite different. In the “unsafe” swallow, the bolus arrived at the

ramus of the mandible by the fourth frame, whereas in the “safe” swallow the bolus

46

arrived at the mandible in the twelfth frame. One could hypothesize that in this

population, faster is not better, in terms of swallowing function. In this single case, it

seems that the discoordination of the swallow mechanism may have led to a rushing of

the swallow events, and subsequent aspiration. The relationship among increased speed

of bolus events, together with discoordination of the swallow mechanism, and

penetration/aspiration is disconcerting in this population which often presents with

decreased cough strength (Ertekin et al., 2002; Hunter et al., 1997) and limited insight

into their condition (Starkstein et al., 1996, Seltzer et al., 2001; Kleinow et al., 2001).

Also interesting, was the absence of any recognizable trend between displacement

and angle measurement or displacement and penetration/aspiration of the bolus. These

findings challenge past research which has defined both the superior and anterior

excursion of the hyoid bone essential for swallow (i.e., Logemann, 1983). The current

pilot data would suggest that perhaps the angle of the hyoid motion is more important for

a safe swallow than the hyoid displacement in the anterior or superior direction alone

In terms of the thick consistencies, much variability is present in hyoid motion due

to the increased amount of extraneous tongue movement associated with tongue

pumping. Because the tongue and hyoid bone are attached, it makes sense that tongue

movements would result in movements of the hyoid bone as well. The importance of

these movements and their effect on subsequent motion of the hyoid related to the

pharyngeal swallow are yet to be identified. It is challenging to discuss these data as

there is no obvious trend to the tongue movement, but it is interesting to note the close

relationship between these two structures which are essential components of the swallow

mechanism.

47

Limitations and Strengths

There are several limitations to the current study. Primarily, the present is a small n

study whose goal is to identify areas for further research and identify differences which

are present in the oral and pharyngeal phases of swallow as a function of consistency in

patients with PD. The nature of this small n study limits the generalizability of the

study’s results. Also, the population which was recruited for this study, although

homogeneous in their clinical severity, may have been too mildly impaired to show true

effects of the dependent variables on P-A score. The lack of pharyngeal dysphagia in this

current participant pool, may have acted as a ceiling effect due to the fact that many of

the patients presented with relatively “safe” swallows, and most did not aspirate.

Although this is true, the trends which were observed are useful for predicting changes

which may occur in patients with PD who exhibit more severe dysphagia. A ceiling

effect may also have been caused by the size of the bolus. The five cc. bolus may have

been too small to truly tax the system and show changes which are representative of real

life swallow challenges.

This being said, the current study is the first of its kind, studying timing and P-A

score as a function of consistency, in a well controlled population, while concurrently

obtaining data which greater specifies hyoid function relative to these variables. The

current study controlled for medication state, with testing one hour after medication

dosage, and controlling also for clinical severity of symptoms. Also, randomization of

the bolus presentation controlled for the possible effects of fatigue. The presentation of

these randomized boluses using cup and spoon, versus syringe, made for a closer

simulation of the participants’ daily eating routines. Lastly, the researchers controlled for

other medical diagnoses, which could have affected swallow function, these included

48

dementia (i.e., Amella, 2004; Dahlin, 2004; Kalia, 2003), other neurological conditions

(i.e., Logemann, 1983), head and neck cancer (i.e., Pauloski et al., 2002), and certain

respiratory conditions, including COPD and asthma (i.e., Good-Fratturelli, Curlee, &

Holle, 2002).

Implications for Future Research

In terms of the primary aim of this study, there are many more questions to be

answered relative to the changes which occur in the oral-pharyngeal phases of swallow as

a function of consistency differences in persons with PD. Now that a possible difference

has been determined between consistency and penetration/aspiration in PD, and a

preliminary relationship between tongue pumping on bolus transit times has been

identified, research should focus on more specifically defining the changes which are

taking place. Manometry would help assess the pressure changes which may be

occurring at the base of tongue, causing subsequent changes in the pharyngeal and

possibly the oral phases of swallow. The effects of bolus consistency on the relationship

between swallowing and breathing in patients with PD is also an interesting question,

especially due to the respiratory changes which often occur in this population, and the

presence of dysphagia which had been described in populations who exhibit respiratory

compromise (i.e., Good-Fratturelli et al., 2002). Lastly, including participants with PD

who exhibit more impairment of the pharyngeal swallow, coupled with the use of a larger

bolus may help assess more specifically the safety issues, particularly P-A score, of this

population with high risk of death secondary to aspiration pneumonia.

Implications for Swallow Intervention

There are more questions than there are answers concerning swallow intervention.

Even today, clinicians will limit patients PO intake or modify their diets long before it is

49

necessary. This is driven mainly by a paucity of literature describing the physiology of

swallow secondary to variables like consistency and compensation strategies, in addition

to questions related to aspiration; its effects and repercussions. It is the hope of the

investigator that through this and future research, the many remaining questions may be

slowly addressed, and the quality and length of life in persons with PD and other similar

disorders may be enhanced due to better management of alimentary issues.

APPENDIX A UNIFIED PARKINSON’S DISEASE RATING SCALE (UPDRS)

51

52

53

54

55

APPENDIX B THE SWAL-QOL SURVEY

57

58

59

60

61

62

63

64

65

66

LIST OF REFERENCES

Ardran, G.M., & Kemp, F.H. (1951). The mechanism of swallowing. Proceedings of the Royal Society of Medicine, 44, 1038-1040.

Ardran, G.M., & Kemp, F.H. (1956). Radiologic investigation of pharyngeal and laryngeal palsy. Acta Radiologica, 46, 446-55.

Ardran, G.M., & Kemp, F.H. (1967). The mechanism of the larynx. II. The epiglottis and closure of the larynx. British Journal of Radiology, 40, 372-89.

Ali, G.N., Wallace, K.L., Schwartz, R., DeCarle, D.J., Zagami, A.S., & Cook, I.J. (1996). Mechanisms of oral-pharyngeal dysphagia in patients with Parkinson’s disease. Gastroenterology, 110, 383-392.

Amella, E,J. (2004). Feeding and hydration issues for older adults with dementia. The Nursing Clinics of North America, 39, 607-23.

Athlin, E., Norberg, A., Axelsson, K., Moller, A., & Nordstrom, G. (1989). Aberrant eating behavior in elderly Parkinsonian patients with and without dementia: analysis of videorecorded meals. Research in Nursing & Health, 12, 41-51.

Bassotti, G., Germani, U., Pagliaricci, S., Plesa, A., & Giuletti, O. (1998). Esophageal manometric abnormalities in Parkinson’s disease. Dysphagia, 13, 28-31.

Bayles, K. (1990). Language and Parkinson’s disease. Alzheimer Disease and Associated Disorders, 4, 171-180.

Bisch, E.M., Logemann, J.A., Rademaker, A.W., Kahrilas, P.J., & Lazarus, C.L. (1994). Pharyngeal effect of bolus volume, viscosity, and temperature in patients with dysphagia resulting from neurologic impairment and in normal subjects. Journal of Speech and Hearing Research, 37, 1041-1049.

Blonsky, E.R., Logemann, J.A., Boshes, B., & Fisher, H.B. (1975). Comparison of speech and swallowing function in patients with tremor disorders and in normal geriatric patients: a cinefluorographic study. Journal of Gerontology, 30 (3), 299-303.

Born, L.J., Harned, R.H., Rikkers, L.F., Pfeiffer, R.F., & Quigley, E.M. (1996). Cricopharyngeal dysfunction in Parkinson’s disease: Role in dysphagia and response to myotomy. Movement Disorders, 11 (1), 53-58.

67

Bosma, J.F. (1957). Deglutition: Pharyngeal Phase. Physiological Reviews, 37, 275-300.

Brodal, P. (1998). The central nervous system: Structure and function (2nd ed.). New York: Oxford University Press.

Bulow, M., Olsson, R., & Ekberg, O. (1999). Videomanometric analysis of supraglottic swallow, effortful swallow, and chin tuck in healthy volunteers. Dysphagia, 14, 67-72.

Bulow, M., Olsson, R., & Ekberg, O. (2003). Videoradiographic analysis of how carbonated thing liquids and thickened liquids affect the physiology of swallowing in subjects with aspiration on thin liquids. Acta Radiologica, 44, 366-372.

Bushmann, M., Dobmeyer, S.M., Leeker, L., & Perlmutter, S. (1989). Swallowing abnormalities and their response to treatment in Parkinson’s disease. Neurology, 39, 1309-1314.

Calne, D.B., Shaw, D.G., Spiers, A.S.D., & Stern, G.M. (1970). Swallowing in Parkinsonism. British Journal of Radiology, 43, 456-457.

Canter, G. (1963). Speech characteristics of patients with Parkinson’s disease I: Intensity, pitch, & duration. Journal of Speech and Hearing Disorders, 28, 221-229.

Canter, G. (1965a). Speech characteristics of patients with Parkinson’s disease II: Physiological support for speech. Journal of Speech and Hearing Disorders, 30, 44-49.

Canter, G. (1965b). Speech characteristics of patients with Parkinson’s disease III: Articulation, diadochokinesis, and overall speech accuracy. Journal of Speech and Hearing Disorders, 30, 217-224.

Castell, J.A., Johnston, B.T., Colcher, A., Li, Q., Gideon, R.M., & Castell, D.O. (2001). Manometric abnormalities of the oesophagus in patients with Parkinson’s disease. Neurogastroenterology, 13, 361-364.

Chi-Fishman, G., & Sonnies, B.C. (2000). Motor strategy in rapid sequential swallowing: new insights. Journal of Speech Language & Hearing Research, 43, 1481-1492.

Coates, C. & Bakheit, A.M.O. (1997). Dysphagia in Parkinson’s disease. European Neurology, 38, 49-52.

Cooper, J.A. Sagar, H.J., Doherty, S.M., Jordan, N., Tidswell, P., & Sullivan, E.V. (1992). Different effects of dopaminergic and anticholinergic therapies on cognitive and motor function in Parkinson’s disease. Brain, 115, 1701-1725.

68

Croxson, S.C.M., & Pye, I. (1988). Dysphagia as the presenting feature of Parkinson’s disease. Geriatric Medicine, August 16, 1988.

Dahlin C. (2004). Oral complications at the end of life. American Journal of Nursing, 104, 40-7.

Dantas, R.O., & Dodds, W.J. (1990). Effects of bolus volume and consistency on swallow-induced submental and infrahyoid electromyographic activity. Brazilian Journal of Medical and Biological Research, 23, 37-44.

Dantas, R.O., Dodds, W.J., Massey, B.T., & Kern, M.K. (1989). The effect of high- vs low-density barium preparations on the quantitative features of swallowing. American Journal of Roentgenolgy, 153, 1191-1195.

Dantas, R.O., Kern, M.K., Massey, B.T., Dodds, W.J., Kahrilas, P.J., Brasseur, J.G., et al. (1990). Effects of swallowed bolus variables on oral and pharyngeal phases of swallowing. American Journal of Physiology, 258, G675-81.

Darley, F., Aronson, A., & Brown, J. (1969a). Differential diagnosis patterns of dysarthria. Journal of Speech and Hearing Research, 12, 246-269.

Darley, F., Aronson, A., & Brown, J. (1969b). Clusters of deviant speech dimensions in the dysarthrias. Journal of Speech and Hearing Research, 12, 462-496.

De Vincentiis, M.I., Calcagno, P., Di Cello, P., Mastronicola, R., Simonelli, M., Ruoppolo, G., et al. (2004). Transit time of swallowing after subtotal laryngectomy. Review of Laryngology, Otology, & Rhinology, 125, 223-7.

Ding, R., Logemann, J.A., Larson, C.R., & Rademaker, A.W. (2003). The effects of taste and consistency on swallow physiology in younger and older healthy individuals: a surface electromyographic study. Journal of Speech, Language, and Hearing Research, 46, 977-989.

Doshay, L.J. (1960) Parkinson’s disease: its meaning and management. Journal of the American Medical Academy, 174, 1962-1965.

Eadie, M.J., & Tyrer, J.H. (1964). Radiological abnormalities of the upper part of the alimentary tract in Parkinsonism. Australasian Annals of Medicine, 14, 23-27.

Eadie, M.J., & Tyrer, J.H. (1965). Alimentary Disorder in Parkinsonism. Australasian Annals of Medicine, 14, 13-22.

Edwards, L.L., Quigley, E.M.M., & Pfeiffer, R.F. (1992). Gastrointestinal dysfunction in Parkinson’s disease: frequency and pathophysiology. Neurology, 42, 726-732.

Ekberg, O., Liedberg, B., & Owall, B. (1986). Barium and meat. A comparison between pharyngeal swallow of fluid and solid boluses. Acta Radiologica. Diagnosis, 27, 701-4.

69

Ertekin, C., Aydogdu, I., Yuceyar, N., Pehlivan, M., Ertas, M., Uludag, B., et al. (1997). Effects of bolus volume on oropharyngeal swallowing: an electrophysiologic study in man. American Journal of Gastroenterology, 92, 2049-2053.

Ertekin, C., Tarlaci, S., Ayodogdu, I., Kiylioglu, N., yuceyar, N., Turman, A.B., et al. (2002). Electrophysiological evaluation of pharyngeal phase of swallowing in patients with Parkinson’s disease. Movement Disorders, 17 (5), 942-949.

Fahn, S., Marsden, C.D., Calne, D.B., & Goldstein, M. (Eds.). (1987). Recent Developments in Parkinson's Disease, (Vol 2). Florham Park, NJ: Macmillan Health Care Information.

Fernandez, H.H., & LaPane, K.L. (2002). Predictors of mortality among nursing home residents with a diagnosis of Parkinson's disease. Medical Science Monitor, 8(4), 241-246.

Folstein, M.F., Folstein, S.E., & McHugh, P.R. (1975). "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatry Research, 12, 189-198.

Good-Fratturelli, M.D., Curlee, R.F., & Holle, J.L. (2000). Prevalence and nature of dysphagia in VA patients with COPD referred for videofluoroscopic swallow examination. Journal of Communication Disorders, 33(2), 93-110.

Gorell, J.M., Johnson, C.C., & Rybicki, B.A. (1994). Parkinson’s disease and its comorbid disorders: an analysis of Michigan mortality data, 1970 to 1990. Neurology, 44 (10), 1856-1858.

Hamdy, S., Aziz, Q., Rothwell, J. C., Singh, K. D., Barlow, J., Hughes, D. G., et al. (1996). The cortical topography of human swallowing musculature in health and disease. Nature Medicine, 2(11), 1217-1224.

Hamdy, S., Mikulis, D. J., Crawley, A., Xue, S., Lau, H., Henry, S., et al. (1999). Cortical activation during human volitional swallowing: an event-related fMRI study. American Journal of Physiology, 277, G219-225.

Hamdy, S., Rothwell, J. C., Brooks, D. J., Bailey, D., Aziz, Q., & Thompson, D. G. (1999). Identification of the cerebral loci processing human swallowing with H2(15)O PET activation. Journal of Neurophysiology, 81, 1917-1926.

Hamdy, S., Xue, S., Valdez, D., & Diamant, N. E. (2001). Induction of cortical swallowing activity by transcranial magnetic stimulation in the anaesthetized cat. Neurogastroenterology and Motility, 13, 65-72.

Han, T.R., Paik, N.J., & Park, J.W. (2001). Quantifying swallowing function after stroke: A functional dysphagia scale based on videofluoroscopic studies. Archives of Physical Medicine and Rehabilitation, 82, 677-682.

70

Hind, J.A., Nicosia, M.A., Roecker, E.B., Carnes, M.L., & Robbins, J. (2001). Comparison of effortful and noneffortful swallows in healthy middle-aged and older adults. Archives of Physical Medicine and Rehabilitation, 82, 1661-5.

Hiss, S.G., Strauss, M., Treole, K., Stuart, A., & Boutilier, S. (2004). Effects of age, gender, bolus volume, bolus viscosity, and gestation on swallowing apnea onset relative to lingual bolus propulsion onset in normal adults. Journal of Speech, Language and Hearing Research, 47, 572-583.

Hoehn, M. & Yahr, M. (1967). Parkinsonism: onset, progression, and mortality. Neurology, 17, 427-442.

Huckabee, M. L., Deecke, L., Cannito, M. P., Gould, H. J., & Mayr, W. (2003). Cortical control mechanisms in volitional swallowing: the Bereitschaftspotential. Brain Topography, 16, 3-17.

Hunter, P.C., Crameri, J., Austin, S., Woodward, M.C., & Hughes, A.J. (1997). Response of parkinsonian swallowing dysfunction to dopaminergic stimulation. Journal of Neurology, Neurosurgery, & Psychiatry, 63, 579-583.

Jacob, P., Kahrilas, P.J., Logemann, J.A., Shah, V., & Ha, T. (1989). Upper esophageal sphincter opening and modulation during swallowing. Gastroenterology, 97, 1469-78.

Kahrilas, P.J., Dodds, W.J., Dent, J., Logemann, J.A., & Shaker, R. (1988). Upper esophageal sphincter function during deglutition. Gastroenterology, 95, 52-62.

Kahrilas, P.J., Logemann, J.A., Krugler, C., & Flanagan, E. Volitional augmentation of upper esophageal sphincter opening during swallowing. American Journal of Physiology, 260, G450-6.

Kalia, M. (2003). Dysphagia and aspiration pneumonia in patients with Alzheimer's disease. Metabolism, 52, 36-8.

Kendall, K.A., Leonard, R.J., & McKenzie, S.W. (2001). Accommodation to changes in bolus viscosity in normal deglutition: a videofluoroscopic study. Annals of Otology, Rhinology, and Laryngology, 110, 1059-1065.

Kirshner, H.S. (1997). Disorders of the pharyngeal and esophageal stages of swallowing in Parkinson’s disease. Dysphagia, 12, 19-20.

Kuhlemeier, K.V., Palmer, J.B., & Rosenberg, D. (2001). Effect of liquid bolus consistency and delivery method on aspiration and pharyngeal retention in dysphagia patients. Dysphagia, 16, 119-122.

Lazarus, C., Logemann, J.A., & Gibbons, P. (1993). Effects of maneuvers on swallowing function in a dysphagic oral cancer patient. Head Neck, 15, 419-24.

71

Lazarus, C., Logemann, J.A., Song, C.W., Rademaker, A.W., & Kahrilas, P.J. (2002). Effects of voluntary maneuvers on tongue base function for swallowing. Folia Phoniatrica et Logopaedica, 54, 171-6.

Leopold, N.A. & Kagel, M.C. (1996). Prepharyngeal dysphagia in Parkinson’s disease. Dysphagia, 11, 14-22.

Leopold, N.A., & Kagel, M.C. (1997). Pharyngo-esophageal dysphagia in Parkinson’s disease. Dysphagia, 12, 11-18.

Lieberman, A.N., Horowitz, L., Redmond, P., Pachter, L., Lieberman, I., & Leibowitz, M. (1980). Dysphagia in Parkinson’s disease. American Journal of Gastroenterology, 74, 157-160.

Logemann, J.A. (1983). Evaluation and Treatment of Swallowing Disorders. Austin, TX: Pro-ed.

Logemann, J.A., Blonsky, E.R., & Boshes, B. (1975). Dysphagia in Parkinsonism. Journal of the American Medical Academy, 231, 69-70.

Logemann, J.A., & Kahrilas, P.J. (1990). Relearning to swallow after stroke--application of maneuvers and indirect biofeedback: a case study. Neurology, 40, 1136-8.

Marsden, C.D. (1984). The pathophysiology of movement disorders. Neurologic Clinics, 2, 435-459.

Marsden, C.D. (1989). Slowness of movement in Parkinson's disease. Movement Disorders, 4 Suppl 1, S26-37.

Martin, B.J., Logemann, J.A., Shaker, R., & Dodds, W.J. (1993). Normal laryngeal valving patterns during three breath-hold maneuvers: a pilot investigation. Dysphagia, 8, 11-20.

Martin, R. E., Goodyear, B. G., Gati, J. S., & Menon, R. S. (2001). Cerebral cortical representation of automatic and volitional swallowing in humans. Journal of Neurophysiology, 85, 938-950.

Martin, R. E., & Sessle, B. J. (1993). The role of the cerebral cortex in swallowing. Dysphagia, 8(3), 195-202.

McHorney, C.A., Bricker, D.E., Kramer, A.E., Rosenbek, J.C., Robbins, J., Chignell, K.A., et al. (2000). The SWAL-QOL outcomes tool for oropharyngeal dysphagia in adults: I. Conceptual foundation and item development. Dysphagia, 15, 115-21.

McHorney, C.A., Bricker, D.E., Robbins, J., Kramer, A.E., Rosenbek, J.C., & Chignell, K.A. (2000). The SWAL-QOL outcomes tool for oropharyngeal dysphagia in adults: II. Item reduction and preliminary scaling. Dysphagia, 15, 122-33.

72

McHorney, C.A., Robbins, J., Lomax, K., Rosenbek, J.C., Chignell, K., Kramer, A.E., et al. (2002). The SWAL-QOL and SWAL-CARE outcomes tool for oropharyngeal dysphagia in adults: III. Documentation of reliability and validity. Dysphagia, 17(2), 97-114.

Mendelsohn, M.S., & Martin, R.E. (1993). Airway protection during breath-holding. Annals of Otology, Rhinology, & Laryngology, 102, 941-944.

Monte, F.S., da Silva-Junior, F.P., Braga-Neto, P., Nobre e Souza, M.A., & Sales de Bruin, V.M. (2005). Swallowing abnormalities and dyskinesia in Parkinson's disease. Movement Disorders, 20, 457-62.

Mosier, K., Patel, R., Liu, W. C., Kalnin, A., Maldjian, J., & Baredes, S. (1999). Cortical representation of swallowing in normal adults: functional implications. Laryngoscope, 109, 1417-1423.

Nagaya, M., Kachi, T., Yamada, T., & Igata, A. (1998). Videofluorographic study of swallowing in Parkinson’s disease. Dysphagia, 13, 95-100.

Nilson, H., Ekberg, O., Olsson, R., & Hindfelt, B. (1996). Quantitative assessment of oral and pharyngeal function in Parkinson’s disease. Dysphagia, 11, 144-150.

Nutt, J.G. (1987). On-off phenomenon: relation to levodopa pharmacokinetics and pharmacodynamics. Annals of Neurology, 22, 535-540.

Ohmae, Y., Logemann, J.A., Kaiser, P., Hanson, D.G., & Kahrilas, P.J. (1995). Timing of glottic closure during normal swallow. Head Neck, 17, 394-402.

Ohmae, Y., Logemann, J.A., Kaiser, P., Hanson, D.G., & Kahrilas, P.J. (1996). Effects of two breath-holding maneuvers on oropharyngeal swallow. Annals of Otology, Rhinology, & Laryngology, 105, 123-31.

Palmer, P.M., Luschei, E.S., Jaffe, D., & McCulloch, T.M. (1999). Contributions of individual muscles to the submental surface electromyogram during swallowing. Journal of Speech, Language, & Hearing Research, 42, 1378-91

Pauloski, B.R., Rademaker, A.W., Logemann, J.A., Lazarus, C.L., Newman, L., Hamner, A., et al. (2002). Swallow function and perception of dysphagia in patients with head and neck cancer. Head Neck, 24, 555-65.

Parkinson, J. (1817). An essay on the shaky palsy. London, Whittingham and Bowland.

Perlman, A.L., VanDaele, D.J., Otterbacher, M.S. (1995). Quantitative assessment of hyoid bone displacement from video images during swallowing. Journal of Speech & Hearing Research,38, 579-85.

Pouderoux, P., & Kahrilas, P.J. (1995). Deglutitive tongue force modulation by volition, volume, and viscosity in humans. Gastroenterology, 108, 1418-26.

73

Raut, V.V., McKee, G.J., & Johnston, B.T. (2001). Effect of bolus consistency on swallowing-does altering consistency help? European Archives of Otorhinolaryngology, 258, 49-53.

Robbins, J., Levine, R.L., Maser, A., Rosenbek, J.C., & Kempster, G.B. (1993). Swallowing after unilateral stroke of the cerebral cortex. Archives of Physical Medicine & Rehabilitation, 74, 1295-300.

Rosenbek, J.C., Robbins, J.A. Roecker, E.B., Coyle, J.L. & Wood, J.L. (1996). A penetration-aspiration scale. Dysphagia, 11(2), 93-98.

Seltzer, B., Vasterling, J.J., Mathias, C.W., & Brennan, A. (2001). Clinical and neuropsychological correlates of impaired awareness of deficits in Alzheimer disease and Parkinson disease: a comparative study. Neuropsychiatry Neuropsychology & Behavioral Neurology, 14, 122-9.

Schiermier, S., Schafer, D., Schafer, T., Greulich, W., & Schlafke, M.E. (2001).Breathing and locomotion in patients with Parkinson’s disease. Pflugers ArchivesEuropean Journal of Physiology, 443, 67-71.

Shill, H. & Stacy, M. (1998). Respiratory function in Parkinson’s disease. Clinical Neuroscience of New York, 5, 131-135.

Singer, R.B. (1992). Mortality in patients with Parkinson’s disease treated with dopa. Journal of Insurance Medicine, 24, 126-127.

Starkstein, S.E., Sabe, L., Petracca, G., Chemerinski, E., Kuzis, G., Merello, M., et al. (1996). Neuropsychological and psychiatric differences between Alzheimer's disease and Parkinson's disease with dementia. Journal of Neurology, Neurosurgergy, & Psychiatry, 61, 381-7.

Stroudley, J., & Walsh, M. (1991). Radiological assessment of dysphagia in Parkinson’s disease. The British Journal of Radiology, 64, 890-893.

Wheeler, K., Martin-Harris, B., Bronsky, M., & Sapienza, C.M. (2006). Development of a measurement scheme for documenting hyoid motion. Presented at Dysphagia Research Symposium (DRS) March 2006.

Wheeler, K., & Sapienza, C.M. (2006). Swallowing and respiration: shared neural substrates. Submitted.

Yamaguchi, S., & Kabayashi, S. (1998). Contributions of the dopaminergic system to voluntary and automatic orienting of visuospatial attention. Journal of Neuroscience, 18, 1869-1878.

Zald, D. H., & Pardo, J. V. (1999). The functional neuroanatomy of voluntary swallowing. Annals of Neurology, 46, 281-286.

74

BIOGRAPHICAL SKETCH

Michelle Troche graduated with her Bachelor of Arts degree in communication

sciences and disorders and linguistics from the University of Florida in 2004. She

graduated summa cum laude and also received minors in teaching English as a second

language (TESL) and gerontology. She will complete the requirements for the Master of

Arts degree in speech pathology at the University of Florida as well. After graduation,

Michelle plans on pursuing a doctoral degree in speech pathology under the mentorship

of Christine Sapienza, specializing in motor speech disorders.