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Swallowing difficulty in Parkinson's disease
Clinical Neurology and Neurosurgery ELSEVIER
Clinical Neurology and Neurosurgery 99 (1997) 106-l 12
Swallowing difficulty in Parkinson’s disease Jong-Ling Fuh a,b, Rheun-Chuan Lee ‘, Shuu-Jiun Wang a*b,Cheng-Huai Pei-Ning Wang a,b, Jen-Huey Chiang ‘, Hsiu-Chih Liu a,b,*
Lin a,b,
a The Neurological Institute, National Yang-Ming University School of Medicine, Taipei, Taiwan, R.0.C b The Neurological Institute, Veterans General Hospital, Taipei, Taiwan, R.0.C c Department of Radiology, Veterans General Hospital, Taipei, Taiwan, R.0.C
Received 12 August 1996; received in revised form 19 December 1996; accepted 9 January 1997
Abstract Dysphagia is a frequent and potentially serious complication of Parkinson’s disease (PD). We examined the oropharyngeal ability in 19 PD patients (15 men and 4 women, mean age 68.42 years, mean Hoehn and Yahr stage 1.8) using modified barium swallow before and after administering oral levodopa (in combination with benserazide). Twelve (63.2%) patients demonstrated objective evidence of swallowing abnormalities; although only six patients (31.6%) had subjective complaints. Vallecula sinus and pyriform sinus residues were the most frequent abnormalities (47.4% and 42.1%); followed by delayed swallowing reflex (26.3%). Three patients demonstrated silent aspiration. In the 12 patients with abnormal swallowing, six (50%) showed objective improvement after levodopa treatment, while the remaining six showed no change. Of the former group of six, one patient showed improvement in the oral phase, but deterioration in the pharyngeal phase. We concluded that PD patients had a high percentage of objective swallowing abnormalities which could be reduced in half of the patients through the administration of levodopa treatment. 0 1997 Elsevier Science B.V. swallowing
Keywords:
Dysphagia; Parkinson’s disease; Swallowing; Videofluoroscopy
1. Introduction Dysphagia in Parkinson’s disease (PD) was first described by James Parkinson in 1817 [l]. He described a typical PD patient with significant body weight loss, suffering greater difficulty taking solid than liquid foods, and living almost on milk alone. However, questions about the nature and origin of these swallowing disturbances have remained controversial. Early investigations reported defective esophageal peristalsis, with segmental esophageal spasms [2], de-
* Corresponding author. Tel: + 886 2 8757492; fax: + 886 2 8738696; e-mail: [email protected] 0303-8467/97/$17.00 0 1997 Elsevier Science B.V. All rights reserved. PII SO303-8467(97)00606-9
fective tongue movements [3] or hypopharyngeal neuromuscular incoordination (cricopharyngeal achalasia) [4]. More recent studies using the modified barium swallow (MBS) showed delayed swallowing reflex, vallecular and pyriform sinus residues and abnormalities which affected tongue control [5,6]. Patients with PD demonstrated mild to moderate nutritional depletion [7]. Dysphagia and aspiration in association with respiratory insufficiency are the major cause of death in PD patients. Post-levodopa improvements in swallowing function might not be consistent with clinical ratings of the same patient [S]. The purpose of this study is to determine the following: patterns of swallowing disorders in PD pabetween patient’s symptoms tients; the relationship and responses to levodopa and objective findings treatment.
J.-L. Fuh et al. /Clinical Neurology and Neurosurgery 99 (1997) 106-l 12
2. Methods 2. I. Subjects Nineteen patients, 15 men and 4 women from 35 to 86 years old (mean age 68.4 f 10.7), were chosen at random from the clinic in the Veterans General Hospital, Taipei. All patients had a clinical diagnosis of PD, that is: at least two of three cardinal symptoms (resting tremor, rigidity, bradykinesia) and levodopa responsiveness were found. None of these patients had a previous history of stroke. And patients with dementia were excluded. The five patients who had never been treated with levodopa previously, also showed responsiveness to this medication during this study. Duration of illness of individual patients ranged from 2 months to 8 years with an average of 3.2 + 2.1 years.
107
After a baseline MBS examination, patients took 200 mg levodopa (in combination with 50 mg benserazide). A second MBS examination was begun 60-90 min later. All radiological recordings were rated, using a protocol by one observer (Lee), who was blinded to the symptoms of severity of the disease, but was not blinded to the time the drugs were taken. 2.3. Statistical analysis Nonparametric, rank-order test (Mann-Whitney Utest) was used to compare grades of pooling in the pharyngeal phase in different groups. Correlation analysis was used to compare the disease severity and grade of pooling in the pharyngeal phase. The Fisher exact test was used to compare the frequency in different groups. A p value of < 0.01 was adopted for statistical significance.
2.2. Procedure Antiparkinsonian medication was stopped for all patients on the day before the beginning of the study (at least 12 h prior to the actual start). A dysphagia symptom survey was conducted in which the Unified Parkinson’s Disease Rating Scale (UPDRS) [8] was used. We graded the salivation on the following 5-point scale (O-4): (0) normal; (1) slight but definite excess of saliva in mouth with possible nighttime drooling; (2) moderately excessive saliva with minimal drooling; (3) marked excess of saliva with some drooling; and (4) marked drooling requiring constant use of tissue or handkerchief. The subjective swallowing difficulty was graded on a similar scale: (0) normal; (1) rare choking; (2) occasional choking; (3) requiring soft food; and (4) requiring nasogastric tube or gastronomic feeding. We assessed neurological examination of these PD subjects on the off-motor phase less than 1 week before the MBS examination, using the motor part of UPDRS [8]. Neurological evaluation was performed on all subjects by two neurologists (Fuh and Wang). PD severity was determined using the Hoehn and Yahr stage [9] and Schwab and England scores [lo]. Swallowing function was evaluated by MBS with videofluoroscopy and videotaped with a super VHS tape recorder which runs 30 frames/s. Each subject successively swallowed 3, 5, 7 cc thin barium, followed by 3, 5 cc barium paste and 1 cc cookie. Swallows were videotaped in the lateral upright position initially and later in the frontal position. Oral transient time for thin liquid was recorded. All recordings were analyzed frame-by-frame. The following aspects of swallow were studied: oral transient time, movement of the tongue, velopharyngeal competence, initiation of swallowing reflex, laryngeal elevation, epiglottis motility, laryngeal closure, vallecula and pyriform sinus residues and aspiration before, during and after swallowing.
3. Results 3.1. Subjects and symptoms The patients’ vital statistics and disease severity were given in Table 1. The mean stage of Hoehn and Yahr was 1.9. The mean Schwab and England score was 75.26%. Only one patient have motor fluctuation. Eight patients complained of rare salivation (grade 1) and 12 patients had no complaints (grade 0). One patient complained of occasional choking (grade 2), 5 patients complained of rare choking (grade 1) and 14 patients never had a history of choking (grade 0). 3.2. Videojhoroscopic examination Table 2 summarized the patterns of swallowing dysfunction seen in this study as well as in six other reports of dysphagia in PD. Twelve (63.2%) patients had abnormal swallows on MBS. Three (15.8%) had aspiration. Of the above-mentioned 12 patients who had abnormal swallows, six showed improvement after taking levodopa while the remaining six showed no change after levodopa treatment. One of the former group of six who showed improvement upon levodopa treatment, indicated oral phase improvement as well as a worsening in the pharyngeal phase. The abnormalities detected by videofluoroscopy were classified according to the affected phase of swallowing. Six patients displayed oral phase abnormalities. Four of them showed prolonged oral transient time; three patients, tongue elevation (i.e. elevated tongue preventing passage of bolus into pharynx [5]); one patient, reduced anterior-posterior motion of tongue; and two patients, oral tremor. Three of the six patients (50%) showed improvement after levodopa treatment; two of
J.-L. Fuh et al. /Clinical Neurology and Neurosurgery 99 (1997) 106-I 12
108
Table 1 Patient characteristics and disease severity Patient no.
Age (years)
Sex
Duration (years)
Hoehn and Yahr
Schwab and England (%)
UPDRS score
1 2 3 4 5 6 I 8 9 10 11 12 13 14 15 16 17 18 19
86 65 80 72 78 61 65 35 69 64 77 14 59 14 62 66 72 69 12
F M M F M M M F M M M M M M F M F M M
5 2 1.5 3 3 2 2 0.6 3 3 7 8 2 1 5 6 0.2 3 3
1 1 2 2 2 2 1 1 2 2 4 2 3 2 1 2 1 2 2
90 100 90 70 90 50 90 90 80 60 30 30 80 90 90 60 90 90 60
11 13 21 2s 12 I 14 I 26 9 30 17 15 16 12 21 10 11 19
them showed improvement in oral tremor. And one patient showed improvement in elevation of the tongue. Eleven patients displayed pharyngeal phase abnormalities. Fig. 1 shows the abnormalities before and after levodopa was taken. One patient’s condition worsened in the pharyngeal phase after he took levodopa. Aspiration was found in three patients. Two of them aspired after swallowing and one patient during and after swallowing. Two of these three patients revealed no post-levodopa aspiration. (Fig. 2) 3.3. Relationship to disease severity There was no statistically significant relationship between disease severity and any of the swallowing dysfunction measured by MBS.
swallowing
laryngeal
reflex
elevation
epiglottis
motility
laryngeal
vestibule
tracheal
aspiration
pyriform sinus residus
laryngeal
adductlon 0
20
30 Frequency
40 (%)
Fig. 1. The pharyngeal phase abnormalities before and after levodopa treatment. Rx: 200 mg levodopa in combination with 50 mg benserazide
3.4. Relationship to clinical symptoms We divided the patients into the tremor-predominant and the nontremor-predominant groups by UPDRS tremor score. If the patient’s tremor score was larger than two, he was included in the tremor-predominant group. If the tremor score was less than or equal to 2, the patient was classified in the nontremor-predominant group. The grades of vallecula and pyriform sinus residues neither differed between the two groups, nor between the axial involvement (posture and/or gait) group and non-involvement group (Mann-Whitney U-test). Results of abnormalities found in videofluoroscopic examinations did not correspond to or agree with the grades of salivation and swallowing complaints found in the examined patients (Fisher exact test, p > 0.20). Two patients complained of rare choking, but their MBS examinations showed no abnormalities. Six patients had no choking history, but their MBS examinations showed significant vallecula and pyriform sinus residues. Two patients who made no choking complaints even showed aspiration. Three patients complained of excess salivation, but the MBS examination did not show any abnormalities. Eight patients showed normal salivation, but their MBS examinations revealed abnormalities. Although in the patient group under study males outnumbered females-this was due to the nature of the population of the veterans hospital-no obvious difference was found in swallowing abnormalities between male and female PD patients.
6 20 24 16 22 13 20
Robbins et al., 1986 [11] Bushmann et al., 1989 [5] Stroudley et al., 1991 [6] Bird et al., 1994 [12] Wintzen et al., 1994 [13] Edwards et al., 1994 [14] Fuh et al. (Present study)
(69) (65.7) (-) (72.5) (62.7) (66.6) (68.2)
Patients numbers mean age
Reference
100 75 100 100 -38 65
Total abnormalities
Percent affected
100 40 92 --31 30
Oral phase
Table 2 Summary of swallowing studies of PD patients (modified barium swallow used)
30
32
100 50 75
Swallowing reflex
15
30
m
Laryngeal elevation
15
33 15 46 19 5
Tracheal aspiration
87 45 7.7 50
83 25
Vallecular or pyriform sinus residues
I
g~
J.-L. Fuh et al. /Clinical Neurology and Neurosurgery 99 (1997) 106-112
110
(4
(4 Fig. 2. Spot film from modified barium swallow. (a) This is a lateral view of the pharynx after swallowing 5 ml of liquid barium sulphate and before levodopa is taken. Aspiration has occurred during swallowing, but (b) normal performance of pharyngeal phase of swallowing after levodopa is taken.
4. Discussion Of the 19 patients, six experienced subjective dysphagia and 12 experienced objective dysphagia. This study, as well as past investigations [2,5,6,1 l-131, showed that patients PD patients in early stages with no symptoms of dysphagia had high percentages of objective swallowing abnormalities. Vallecula and pyriform sinus residues and delayed swallowing reflex were found more frequently than other swallowing abnormalities in
our study. The frequencies varied in the previous studies. These variations may reflect differences in age, in disease severity among the patients and in criteria and threshold levels applied in determining the abnormalities. Edwards et al. found the prevalence of gastrointestinal symptoms correlate with the duration and severity of PD, but not with diet and treatment [15]. We found that clinical staging and duration of disease did not consistently foretell radiographic abnormality. Bush-
J.-L. Fuh et al. /Clinical Neurology and Neurosurgery 99 (1997) 106-l 12
mann’s study had similar findings [5]. However, the number of patients of advanced stage PD was small in both our and Bushmann’s studies. Abnormal salivation is expressed as drooling or excess saliva in the mouth. In the past it was thought that drooling was caused by hypersecretion. Eadie attributed it to dysphagia and decreased frequency of swallowing [2]. However, we found no significant correlation between subjective complaint of drooling and the objective finding of swallowing abnormalities on MBS. We also found that a patient’s description of difficulty in swallowing and the findings on MBS correlated poorly, just as Bushmann found in her study [5]. MBS provided the basis of our understanding of the swallowing function in PD patients. Manofluorographic studies have showed that the tongue is the major driving force for pharyngeal pressure generation and probably also for pharyngeal clearance [16]. Robbins et al. suggested that rigidity and bradykinesia underlie the volitional speech abnormality as well as disordered oral and pharyngeal stages of swallowing [l 11. Johnston el al. [17] suggested that pathophysiological signs of oral phase abnormalities included tremor, rigidity and bradykinesia of lips, tongue and soft palate; and pathophysiological signs of pharyngeal phase abnormalities included delayed and uncoordinated oral delivery, rigidity and bradykinesia of striated muscle, abnormal function of hyoid musculature, reduced somatosensory stimuli and degeneration of the dorsal nucleus of the vagus nerve. Calne et al. [3] found no change in pharyngeal transient time after levodopa or placebo was taken. Bushmann et al. [5] found a clear improvement in swallowing in one third of the patients after they took an oral dose of levodopa. Our study showed that more than half of the patients experienced improved swallowing function after levodopa treatment. Bramble et al. [18] noted that after being administered intravenous atropine, PD patients showed marked disruption of coordination in swallow tests. Bramble et al. suggested that cholinergic rather than dopaminergic mechanisms are of great importance to the control of swallowing. However, the study was focused on esophageal motility. Our and Bushmann’s studies were focused on the oropharyngeal phase. Our study indicated that the post-levodopa reduction of bradykinesia and rigidity of tongue probably brought about an improvement of the swallowing function of the patients. We suggested that dopaminergic mechanism may also play a role in oropharyngeal control of swallowing. Major findings of this study may be summarized in these points: swallowing abnormalities were common in PD; vallecula and pyriform sinus residues and delayed swallowing reflex were the most frequent abnormalities; frequency of subjective complaints correlated poorly with the severity of oropharyngeal swallowing abnor-
111
malities found in MBS studies; and oropharyngeal abnormalities improved in half of the patients after levodopa treatment. Acknowledgements
This study was supported in part by grants from Chin-Lin Medical Foundation (CI-83-06) and National Science Council (NSC-83-0412-B-075-109Y and 842331-B-075-089). References [I] Parkinson, J. (1817) An essay on the shaking palsy. In: Medical Classics. Whittingham and Rowland, London, 1817.
121Eadie, M.J., Tyrer, J.H. (1965) Radiological abnormalities of the upper part of the alimentary tract in parkinsonism. Amt. Ann. Med., 14: 23-27. [31 Calne, D.B., Shaw, D.W., Spiers, A.S.D., Stern G.M. (1970) Swallowing in parkinsonism. Br. J. Radiol., 43: 456-457. 141 Palmer, E.D. (1974) Dysphagia in parkinsonism. J. Am. Med. Assoc., 229: 1349. [51 Bushmann, M., Dobmeyer, S., Leeker, L., Perlmutter J. (1989) Swallowing abnormalities and their response to treatment in Parkinson’s disease. Neurology, 39: 1309- 1314. PI Stroudley, J., Walsh, M. (1991) Radiological assessment of dysphagia in Parkinson‘s disease. Br. J. Radiol., 64: 890-893. [71 Waxman, M.J., Durfee, D., Moore, M., Morantz, R.A., Koller W. (1990) Nutritional aspects and swallowing function of patients with Parkinson’s disease. Nutrition in Clinical Practice, 1966 199. PI Fahn, S., Elton, R.L., and members of the UPDRS Development Committee (1987) Unified Parkinson’s Disease Rating Scale. In: Fahn, S., Marsden, CD., Goldstein, M., Calne, D.B., (Eds.), Recent Developments in Parkinson’s disease, Vol. 2. MacMillian, New York, pp. 153-163. [91 Hoehn, M.M., Yahr, M.D. (1967) Parkinsonism: onset, progression and mortality. Neurology, 17: 427-442. PO1 Schwab, R.S., England, A.C. (1969) Projection technique for evaluating surgery in Parkinson‘s disease. In Gillingham, F.J., Donaldson, I.M.L. (Eds.), Third Symposium on Parkinson’s Disease. Livingstone, Edinburgh, pp. l52- 157. u 11 Robbins, J.A., Logemann, J.A., Kirshner, H.S. (1986) Swallowing and speech production in Parkinson’s disease. Ann. Neurol., 283-287. u21 Bird, M.R., Woodward, MC., Gibson, E.M., Phyland, D.J., Fonda, D. (1994) Asymptomatic swallowing disorders in elderly patients with Parkinson’s disease: a description of findings on clinical examination and videofluorosocopy in sixteen patients. Age Ageing, 23: 251-254. 1131Wintzen, A.R., Badrising, U.A., Roos, R.A.C., Vielvoye, J., Liauw, L., Pauwels, E.K.J. (1994) Dysphagia in ambulant patients with Parkinson‘s disease: common, not dangerous. Can. J. Neurol. Sci., 21: 53-56. iI41 Edwards, L.L., Quigley, E.M.M., Harned, R.K., Hofman, R., Pfeiffer, R.F. (1994) Characterization of swallowing and defecation in Parkinson’s disease. Am. J. Gastroenterol., 89: 15-25. [I51 Edwards, L.L. Pfeiffer, R.F., Quigley, E.M.M., Hofman, R., BallufIf, M. (1991) Gastrointestinal symptoms. I. Parkinson’s disease. Mov. Disord., 6: 151- 156. 1161McConnel, F.M.S., Cerenko, D., Mendelsohn, M.S. (1988) Manofluoroscopic analysis of swallowing. Otolaryngeal Clin. North Am., 21: 625-635.
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112 [17] Johnston,
B.T., Li, Q., Castell, J.A., Castell, D.O. (1995) Swallowing and esophageal function in Parkinson’s disease. Am. J. Gastroenterol., 10: 1741-1746.
[18] Bramble, M.G., Cunliffe, J., Dellipiani, A.W. (1978) Evidence for a change in neurotransmitter affecting oesophageal motility in Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry, 41: 7099712.
Clinical Neurology and Neurosurgery 99 (1997) 106-l 12
Swallowing difficulty in Parkinson’s disease Jong-Ling Fuh a,b, Rheun-Chuan Lee ‘, Shuu-Jiun Wang a*b,Cheng-Huai Pei-Ning Wang a,b, Jen-Huey Chiang ‘, Hsiu-Chih Liu a,b,*
Lin a,b,
a The Neurological Institute, National Yang-Ming University School of Medicine, Taipei, Taiwan, R.0.C b The Neurological Institute, Veterans General Hospital, Taipei, Taiwan, R.0.C c Department of Radiology, Veterans General Hospital, Taipei, Taiwan, R.0.C
Received 12 August 1996; received in revised form 19 December 1996; accepted 9 January 1997
Abstract Dysphagia is a frequent and potentially serious complication of Parkinson’s disease (PD). We examined the oropharyngeal ability in 19 PD patients (15 men and 4 women, mean age 68.42 years, mean Hoehn and Yahr stage 1.8) using modified barium swallow before and after administering oral levodopa (in combination with benserazide). Twelve (63.2%) patients demonstrated objective evidence of swallowing abnormalities; although only six patients (31.6%) had subjective complaints. Vallecula sinus and pyriform sinus residues were the most frequent abnormalities (47.4% and 42.1%); followed by delayed swallowing reflex (26.3%). Three patients demonstrated silent aspiration. In the 12 patients with abnormal swallowing, six (50%) showed objective improvement after levodopa treatment, while the remaining six showed no change. Of the former group of six, one patient showed improvement in the oral phase, but deterioration in the pharyngeal phase. We concluded that PD patients had a high percentage of objective swallowing abnormalities which could be reduced in half of the patients through the administration of levodopa treatment. 0 1997 Elsevier Science B.V. swallowing
Keywords:
Dysphagia; Parkinson’s disease; Swallowing; Videofluoroscopy
1. Introduction Dysphagia in Parkinson’s disease (PD) was first described by James Parkinson in 1817 [l]. He described a typical PD patient with significant body weight loss, suffering greater difficulty taking solid than liquid foods, and living almost on milk alone. However, questions about the nature and origin of these swallowing disturbances have remained controversial. Early investigations reported defective esophageal peristalsis, with segmental esophageal spasms [2], de-
* Corresponding author. Tel: + 886 2 8757492; fax: + 886 2 8738696; e-mail: [email protected] 0303-8467/97/$17.00 0 1997 Elsevier Science B.V. All rights reserved. PII SO303-8467(97)00606-9
fective tongue movements [3] or hypopharyngeal neuromuscular incoordination (cricopharyngeal achalasia) [4]. More recent studies using the modified barium swallow (MBS) showed delayed swallowing reflex, vallecular and pyriform sinus residues and abnormalities which affected tongue control [5,6]. Patients with PD demonstrated mild to moderate nutritional depletion [7]. Dysphagia and aspiration in association with respiratory insufficiency are the major cause of death in PD patients. Post-levodopa improvements in swallowing function might not be consistent with clinical ratings of the same patient [S]. The purpose of this study is to determine the following: patterns of swallowing disorders in PD pabetween patient’s symptoms tients; the relationship and responses to levodopa and objective findings treatment.
J.-L. Fuh et al. /Clinical Neurology and Neurosurgery 99 (1997) 106-l 12
2. Methods 2. I. Subjects Nineteen patients, 15 men and 4 women from 35 to 86 years old (mean age 68.4 f 10.7), were chosen at random from the clinic in the Veterans General Hospital, Taipei. All patients had a clinical diagnosis of PD, that is: at least two of three cardinal symptoms (resting tremor, rigidity, bradykinesia) and levodopa responsiveness were found. None of these patients had a previous history of stroke. And patients with dementia were excluded. The five patients who had never been treated with levodopa previously, also showed responsiveness to this medication during this study. Duration of illness of individual patients ranged from 2 months to 8 years with an average of 3.2 + 2.1 years.
107
After a baseline MBS examination, patients took 200 mg levodopa (in combination with 50 mg benserazide). A second MBS examination was begun 60-90 min later. All radiological recordings were rated, using a protocol by one observer (Lee), who was blinded to the symptoms of severity of the disease, but was not blinded to the time the drugs were taken. 2.3. Statistical analysis Nonparametric, rank-order test (Mann-Whitney Utest) was used to compare grades of pooling in the pharyngeal phase in different groups. Correlation analysis was used to compare the disease severity and grade of pooling in the pharyngeal phase. The Fisher exact test was used to compare the frequency in different groups. A p value of < 0.01 was adopted for statistical significance.
2.2. Procedure Antiparkinsonian medication was stopped for all patients on the day before the beginning of the study (at least 12 h prior to the actual start). A dysphagia symptom survey was conducted in which the Unified Parkinson’s Disease Rating Scale (UPDRS) [8] was used. We graded the salivation on the following 5-point scale (O-4): (0) normal; (1) slight but definite excess of saliva in mouth with possible nighttime drooling; (2) moderately excessive saliva with minimal drooling; (3) marked excess of saliva with some drooling; and (4) marked drooling requiring constant use of tissue or handkerchief. The subjective swallowing difficulty was graded on a similar scale: (0) normal; (1) rare choking; (2) occasional choking; (3) requiring soft food; and (4) requiring nasogastric tube or gastronomic feeding. We assessed neurological examination of these PD subjects on the off-motor phase less than 1 week before the MBS examination, using the motor part of UPDRS [8]. Neurological evaluation was performed on all subjects by two neurologists (Fuh and Wang). PD severity was determined using the Hoehn and Yahr stage [9] and Schwab and England scores [lo]. Swallowing function was evaluated by MBS with videofluoroscopy and videotaped with a super VHS tape recorder which runs 30 frames/s. Each subject successively swallowed 3, 5, 7 cc thin barium, followed by 3, 5 cc barium paste and 1 cc cookie. Swallows were videotaped in the lateral upright position initially and later in the frontal position. Oral transient time for thin liquid was recorded. All recordings were analyzed frame-by-frame. The following aspects of swallow were studied: oral transient time, movement of the tongue, velopharyngeal competence, initiation of swallowing reflex, laryngeal elevation, epiglottis motility, laryngeal closure, vallecula and pyriform sinus residues and aspiration before, during and after swallowing.
3. Results 3.1. Subjects and symptoms The patients’ vital statistics and disease severity were given in Table 1. The mean stage of Hoehn and Yahr was 1.9. The mean Schwab and England score was 75.26%. Only one patient have motor fluctuation. Eight patients complained of rare salivation (grade 1) and 12 patients had no complaints (grade 0). One patient complained of occasional choking (grade 2), 5 patients complained of rare choking (grade 1) and 14 patients never had a history of choking (grade 0). 3.2. Videojhoroscopic examination Table 2 summarized the patterns of swallowing dysfunction seen in this study as well as in six other reports of dysphagia in PD. Twelve (63.2%) patients had abnormal swallows on MBS. Three (15.8%) had aspiration. Of the above-mentioned 12 patients who had abnormal swallows, six showed improvement after taking levodopa while the remaining six showed no change after levodopa treatment. One of the former group of six who showed improvement upon levodopa treatment, indicated oral phase improvement as well as a worsening in the pharyngeal phase. The abnormalities detected by videofluoroscopy were classified according to the affected phase of swallowing. Six patients displayed oral phase abnormalities. Four of them showed prolonged oral transient time; three patients, tongue elevation (i.e. elevated tongue preventing passage of bolus into pharynx [5]); one patient, reduced anterior-posterior motion of tongue; and two patients, oral tremor. Three of the six patients (50%) showed improvement after levodopa treatment; two of
J.-L. Fuh et al. /Clinical Neurology and Neurosurgery 99 (1997) 106-I 12
108
Table 1 Patient characteristics and disease severity Patient no.
Age (years)
Sex
Duration (years)
Hoehn and Yahr
Schwab and England (%)
UPDRS score
1 2 3 4 5 6 I 8 9 10 11 12 13 14 15 16 17 18 19
86 65 80 72 78 61 65 35 69 64 77 14 59 14 62 66 72 69 12
F M M F M M M F M M M M M M F M F M M
5 2 1.5 3 3 2 2 0.6 3 3 7 8 2 1 5 6 0.2 3 3
1 1 2 2 2 2 1 1 2 2 4 2 3 2 1 2 1 2 2
90 100 90 70 90 50 90 90 80 60 30 30 80 90 90 60 90 90 60
11 13 21 2s 12 I 14 I 26 9 30 17 15 16 12 21 10 11 19
them showed improvement in oral tremor. And one patient showed improvement in elevation of the tongue. Eleven patients displayed pharyngeal phase abnormalities. Fig. 1 shows the abnormalities before and after levodopa was taken. One patient’s condition worsened in the pharyngeal phase after he took levodopa. Aspiration was found in three patients. Two of them aspired after swallowing and one patient during and after swallowing. Two of these three patients revealed no post-levodopa aspiration. (Fig. 2) 3.3. Relationship to disease severity There was no statistically significant relationship between disease severity and any of the swallowing dysfunction measured by MBS.
swallowing
laryngeal
reflex
elevation
epiglottis
motility
laryngeal
vestibule
tracheal
aspiration
pyriform sinus residus
laryngeal
adductlon 0
20
30 Frequency
40 (%)
Fig. 1. The pharyngeal phase abnormalities before and after levodopa treatment. Rx: 200 mg levodopa in combination with 50 mg benserazide
3.4. Relationship to clinical symptoms We divided the patients into the tremor-predominant and the nontremor-predominant groups by UPDRS tremor score. If the patient’s tremor score was larger than two, he was included in the tremor-predominant group. If the tremor score was less than or equal to 2, the patient was classified in the nontremor-predominant group. The grades of vallecula and pyriform sinus residues neither differed between the two groups, nor between the axial involvement (posture and/or gait) group and non-involvement group (Mann-Whitney U-test). Results of abnormalities found in videofluoroscopic examinations did not correspond to or agree with the grades of salivation and swallowing complaints found in the examined patients (Fisher exact test, p > 0.20). Two patients complained of rare choking, but their MBS examinations showed no abnormalities. Six patients had no choking history, but their MBS examinations showed significant vallecula and pyriform sinus residues. Two patients who made no choking complaints even showed aspiration. Three patients complained of excess salivation, but the MBS examination did not show any abnormalities. Eight patients showed normal salivation, but their MBS examinations revealed abnormalities. Although in the patient group under study males outnumbered females-this was due to the nature of the population of the veterans hospital-no obvious difference was found in swallowing abnormalities between male and female PD patients.
6 20 24 16 22 13 20
Robbins et al., 1986 [11] Bushmann et al., 1989 [5] Stroudley et al., 1991 [6] Bird et al., 1994 [12] Wintzen et al., 1994 [13] Edwards et al., 1994 [14] Fuh et al. (Present study)
(69) (65.7) (-) (72.5) (62.7) (66.6) (68.2)
Patients numbers mean age
Reference
100 75 100 100 -38 65
Total abnormalities
Percent affected
100 40 92 --31 30
Oral phase
Table 2 Summary of swallowing studies of PD patients (modified barium swallow used)
30
32
100 50 75
Swallowing reflex
15
30
m
Laryngeal elevation
15
33 15 46 19 5
Tracheal aspiration
87 45 7.7 50
83 25
Vallecular or pyriform sinus residues
I
g~
J.-L. Fuh et al. /Clinical Neurology and Neurosurgery 99 (1997) 106-112
110
(4
(4 Fig. 2. Spot film from modified barium swallow. (a) This is a lateral view of the pharynx after swallowing 5 ml of liquid barium sulphate and before levodopa is taken. Aspiration has occurred during swallowing, but (b) normal performance of pharyngeal phase of swallowing after levodopa is taken.
4. Discussion Of the 19 patients, six experienced subjective dysphagia and 12 experienced objective dysphagia. This study, as well as past investigations [2,5,6,1 l-131, showed that patients PD patients in early stages with no symptoms of dysphagia had high percentages of objective swallowing abnormalities. Vallecula and pyriform sinus residues and delayed swallowing reflex were found more frequently than other swallowing abnormalities in
our study. The frequencies varied in the previous studies. These variations may reflect differences in age, in disease severity among the patients and in criteria and threshold levels applied in determining the abnormalities. Edwards et al. found the prevalence of gastrointestinal symptoms correlate with the duration and severity of PD, but not with diet and treatment [15]. We found that clinical staging and duration of disease did not consistently foretell radiographic abnormality. Bush-
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mann’s study had similar findings [5]. However, the number of patients of advanced stage PD was small in both our and Bushmann’s studies. Abnormal salivation is expressed as drooling or excess saliva in the mouth. In the past it was thought that drooling was caused by hypersecretion. Eadie attributed it to dysphagia and decreased frequency of swallowing [2]. However, we found no significant correlation between subjective complaint of drooling and the objective finding of swallowing abnormalities on MBS. We also found that a patient’s description of difficulty in swallowing and the findings on MBS correlated poorly, just as Bushmann found in her study [5]. MBS provided the basis of our understanding of the swallowing function in PD patients. Manofluorographic studies have showed that the tongue is the major driving force for pharyngeal pressure generation and probably also for pharyngeal clearance [16]. Robbins et al. suggested that rigidity and bradykinesia underlie the volitional speech abnormality as well as disordered oral and pharyngeal stages of swallowing [l 11. Johnston el al. [17] suggested that pathophysiological signs of oral phase abnormalities included tremor, rigidity and bradykinesia of lips, tongue and soft palate; and pathophysiological signs of pharyngeal phase abnormalities included delayed and uncoordinated oral delivery, rigidity and bradykinesia of striated muscle, abnormal function of hyoid musculature, reduced somatosensory stimuli and degeneration of the dorsal nucleus of the vagus nerve. Calne et al. [3] found no change in pharyngeal transient time after levodopa or placebo was taken. Bushmann et al. [5] found a clear improvement in swallowing in one third of the patients after they took an oral dose of levodopa. Our study showed that more than half of the patients experienced improved swallowing function after levodopa treatment. Bramble et al. [18] noted that after being administered intravenous atropine, PD patients showed marked disruption of coordination in swallow tests. Bramble et al. suggested that cholinergic rather than dopaminergic mechanisms are of great importance to the control of swallowing. However, the study was focused on esophageal motility. Our and Bushmann’s studies were focused on the oropharyngeal phase. Our study indicated that the post-levodopa reduction of bradykinesia and rigidity of tongue probably brought about an improvement of the swallowing function of the patients. We suggested that dopaminergic mechanism may also play a role in oropharyngeal control of swallowing. Major findings of this study may be summarized in these points: swallowing abnormalities were common in PD; vallecula and pyriform sinus residues and delayed swallowing reflex were the most frequent abnormalities; frequency of subjective complaints correlated poorly with the severity of oropharyngeal swallowing abnor-
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malities found in MBS studies; and oropharyngeal abnormalities improved in half of the patients after levodopa treatment. Acknowledgements
This study was supported in part by grants from Chin-Lin Medical Foundation (CI-83-06) and National Science Council (NSC-83-0412-B-075-109Y and 842331-B-075-089). References [I] Parkinson, J. (1817) An essay on the shaking palsy. In: Medical Classics. Whittingham and Rowland, London, 1817.
121Eadie, M.J., Tyrer, J.H. (1965) Radiological abnormalities of the upper part of the alimentary tract in parkinsonism. Amt. Ann. Med., 14: 23-27. [31 Calne, D.B., Shaw, D.W., Spiers, A.S.D., Stern G.M. (1970) Swallowing in parkinsonism. Br. J. Radiol., 43: 456-457. 141 Palmer, E.D. (1974) Dysphagia in parkinsonism. J. Am. Med. Assoc., 229: 1349. [51 Bushmann, M., Dobmeyer, S., Leeker, L., Perlmutter J. (1989) Swallowing abnormalities and their response to treatment in Parkinson’s disease. Neurology, 39: 1309- 1314. PI Stroudley, J., Walsh, M. (1991) Radiological assessment of dysphagia in Parkinson‘s disease. Br. J. Radiol., 64: 890-893. [71 Waxman, M.J., Durfee, D., Moore, M., Morantz, R.A., Koller W. (1990) Nutritional aspects and swallowing function of patients with Parkinson’s disease. Nutrition in Clinical Practice, 1966 199. PI Fahn, S., Elton, R.L., and members of the UPDRS Development Committee (1987) Unified Parkinson’s Disease Rating Scale. In: Fahn, S., Marsden, CD., Goldstein, M., Calne, D.B., (Eds.), Recent Developments in Parkinson’s disease, Vol. 2. MacMillian, New York, pp. 153-163. [91 Hoehn, M.M., Yahr, M.D. (1967) Parkinsonism: onset, progression and mortality. Neurology, 17: 427-442. PO1 Schwab, R.S., England, A.C. (1969) Projection technique for evaluating surgery in Parkinson‘s disease. In Gillingham, F.J., Donaldson, I.M.L. (Eds.), Third Symposium on Parkinson’s Disease. Livingstone, Edinburgh, pp. l52- 157. u 11 Robbins, J.A., Logemann, J.A., Kirshner, H.S. (1986) Swallowing and speech production in Parkinson’s disease. Ann. Neurol., 283-287. u21 Bird, M.R., Woodward, MC., Gibson, E.M., Phyland, D.J., Fonda, D. (1994) Asymptomatic swallowing disorders in elderly patients with Parkinson’s disease: a description of findings on clinical examination and videofluorosocopy in sixteen patients. Age Ageing, 23: 251-254. 1131Wintzen, A.R., Badrising, U.A., Roos, R.A.C., Vielvoye, J., Liauw, L., Pauwels, E.K.J. (1994) Dysphagia in ambulant patients with Parkinson‘s disease: common, not dangerous. Can. J. Neurol. Sci., 21: 53-56. iI41 Edwards, L.L., Quigley, E.M.M., Harned, R.K., Hofman, R., Pfeiffer, R.F. (1994) Characterization of swallowing and defecation in Parkinson’s disease. Am. J. Gastroenterol., 89: 15-25. [I51 Edwards, L.L. Pfeiffer, R.F., Quigley, E.M.M., Hofman, R., BallufIf, M. (1991) Gastrointestinal symptoms. I. Parkinson’s disease. Mov. Disord., 6: 151- 156. 1161McConnel, F.M.S., Cerenko, D., Mendelsohn, M.S. (1988) Manofluoroscopic analysis of swallowing. Otolaryngeal Clin. North Am., 21: 625-635.
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