Hypometabolism in the supplementary and anterior cingulate cortices is related to dysphagia in Parkinson's disease: a cross-sectional and 3-year longitudinal cohort study

Abstract

Objective: Dysphagia is one of the cardinal symptoms of Parkinson's disease (PD). It is closely related to the quality of life and longevity of PD patients. The aim of the study is to clarify the pathophysiological mechanisms responsible for dysphagia in PD.

Design: A cross-sectional and longitudinal comparative study.

Setting: Tohoku University Hospital.

Participants: Eight patients with dysphagia, 15 patients without dysphagia and 10 normal control subjects.

Main outcome measures: The time needed for swallowing initiation and changes in brain glucose metabolism at baseline and after a 3-year follow-up period.

Results: The time needed for swallowing initiation was significantly longer in the patients with dysphagia compared with the patients without dysphagia at baseline and after the 3-year follow-up period (p<0.05). The patients with dysphagia exhibited hypometabolism in the supplementary motor area (SMA) and the anterior cingulate cortex (ACC) compared with the 10 normal control subjects at baseline (uncorrected p<0.001). After the 3-year follow-up period, the number of brain areas showing hypometabolism increased, involving not only the SMA and the ACC but also the bilateral medial frontal lobes, middle cingulate cortex, thalamus and right superior, middle, inferior and orbital frontal gyri (uncorrected p<0.001). In contrast, the patients without dysphagia showed virtually no regional hypometabolism at baseline (uncorrected p<0.001) and only a small degree of hypometabolism in the SMA and ACC after the 3-year follow-up period (uncorrected p<0.001).

Conclusions: These results suggest that dysphagia in PD patients is mainly related to a difficulty in swallowing initiation that is based on a combination of poor movement planning due to SMA dysfunction and impaired cognitive processing due to ACC dysfunction.

Figure 1

Parkinson's disease patients and follow-up flow diagram.

Figure 2

The time needed for swallowing initiation and the 30 s swallowing frequency in Parkinson's disease (PD) patients with and without dysphagia at baseline and after a 3-year follow-up period. There were significant differences between PD patients with and without dysphagia in the time needed for swallowing initiation at baseline and after a 3-year follow-up period (p<0.05) (A). In the 30 s swallowing frequency, there was no significant difference between PD patients with and without dysphagia at baseline (p>0.05), but a significant difference between the two groups was evident after the 3-year follow-up period (p<0.05) (B).

Figure 3

Cross-sectional analyses of brain maps showing the differences between Parkinson's disease (PD) patients with dysphagia and normal control subjects at baseline (A) and after a 3-year follow-up period (B). Various areas showed differences in the standardised PET data, and areas with a height threshold of p<0.001 (uncorrected) and an extent threshold of 40 voxels are illustrated. A comparison of regional cerebral glucose metabolism values demonstrated hypometabolism in the SMA and ACC in the PD patients with dysphagia compared with normal control subjects at baseline (uncorrected p<0.001, threshold=40 voxels) (A). After a 3-year follow-up period, the areas of hypometabolism included not only the SMA and the ACC but also the bilateral medial frontal lobes, middle cingulate cortex, thalamus and right superior, middle, inferior and orbital frontal gyri (uncorrected p<0.001, threshold=40 voxels) (B).

Figure 4

Cross-sectional analyses of brain maps showing differences between PD patients without dysphagia and normal control subjects at baseline (A) and after a 3-year follow-up period (B). Various areas showed differences in the standardised PET data, and areas with a height threshold of p<0.001 (uncorrected) and an extent threshold of 40 voxels are illustrated. The PD patients without dysphagia showed virtually no hypometabolism at baseline (uncorrected p<0.001, threshold=40 voxels) (A) and only a small degree of hypometabolism in the SMA and ACC after a 3-year follow-up period (uncorrected p<0.001, threshold=40 voxels) (B) compared with normal control subjects.