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Progressive Worsening of Spatial and Chromatic Processing Deficits in Parkinson Disease
Nico J. Diederich, MD;
Rema Raman, MS;
Sue Leurgans, PhD;
Christopher G. Goetz, MD
Arch Neurol. 2002;59:1249-1252.
ABSTRACT
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Context Impairments of color discrimination (CD) and contrast sensitivity are
established signs of Parkinson disease (PD), but their temporal evolution
has not been studied.
Objective To determine whether there is progressive, longitudinal deterioration
of color discrimination (CD) and contrast sensitivity (CS) in PD.
Design A prospective study.
Setting Tertiary care center–based sample of PD patients without dementia
with normal visual acuity (Snellen fraction >0.6 in the best eye).
Main Outcome Measures With a mean ± SD interval of 19.8 ± 2.8 months, the following
tests were applied twice in 28 patients: the Lanthony D15 test and the Farnsworth
Munsell 100 Hue test as tests of CD and the monocular and binocular Pelli-Robson
test and the binocular Vistech tables as tests of CS.
Results There was deterioration of both CD (Farnsworth Munsell 100 hue test: P = .002) and CS (binocular Vistech test at a spatial frequency
of 6 cycles per degree, P<.001). Both deficits
correlated with age, and the chromatic deficit additionally correlated with
higher impairment of motor function (Unified Parkinson's Disease Rating Scale
motor section, P = .04) and activities of daily life
(Unified Parkinson's Disease Rating Scale activities of daily living section, P = .006). Patients with the highest pathologic psychiatric
rating score (Brief Psychiatric Rating Scale) performed worse on both CS (P = .02) and CD (P = .01) at the
second examination.
Conclusions Impairments of CD and CS in PD are progressive over time. Visual deficits
may influence overall motor function and lead to enhanced motor impairment.
INTRODUCTION
IN PARKINSON DISEASE (PD) visual pathways can be affected at different
levels. In autopsy studies of unmedicated PD patients, retinal dopamine concentration
is reduced.1 MPTP (1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine)
intoxication in patients and monkeys produces a pathologic electroretinogram,
implicating a role of dopamine in the center-surround organization of the
receptive field.2 Pathologic changes beyond
the retina are suggested by abnormal responses of the visual P300 waves and
by reduced cerebral metabolism in the occipital area.3
In the clinical setting, visual processing deficits have been established
in several studies. Patients with PD have reduced contrast sensitivity (CS),
with maximal deficits in horizontal gratings and medium spatial frequencies.
These changes are influenced by stage and duration of the disease and circadian
variability.4-6
The deficits of color discrimination (CD) are detected early in the disease7; the tritan axis is most affected, and dopaminergic
treatment can improve the deficits. To our knowledge, there has been no longitudinal
study of visual impairment with correlation to other parkinsonian features.
We therefore designed a study to determine whether there is deterioration
of CS and CD in PD and to monitor such changes in the context of clinical
motor function.
PATIENTS AND METHODS
Thirty-one patients with idiopathic PD who had previously participated
in visual tests volunteered for this follow-up study. Three were excluded
because of low visual acuity as defined by a Snellen fraction of less than
0.6 in the best eye (2 patients) and dementia as defined as a score of less
than 24 on the Mini-Mental State Examination (1 patient). Thus, 28 patients
were examined twice and their visual test results were compared. None of the
study subjects had florid psychosis as determined by the Brief Psychiatric
Rating Scale (BPRS), inborn color blindness as defined by the Ishihara plates,
or other coexistent neurologic disease potentially worsening visual perception.
Each patient was examined in the same way as in the first session with the
same investigator, room, and lighting conditions. The same battery of ophthalmologic
and clinical examinations was applied in the same sequence, with the patients
being "on" (mobile) and taking their usual medications. The examiner did not
have access to the individual test results from the first session. In addition
to the tests already mentioned, these examinations included the Lanthony D15
test (LD) and the Farnsworth Munsell 100 Hue test (FM) as tests of CD and
the monocular and binocular Pelli-Robson test (PR) and the binocular Vistech
tables (VT) as tests of CS. These test pairs are each time complementary:
the LD is a succinct CD screening test, and the FM is a largely accepted and
user-friendly CD test that separately explores different color axes. The PR
compares monocular vs binocular CS, whereas the VT explores different spatial
frequencies (cycles per degree [cpd]).8 All
these tests have already been applied to PD patients; they have easy instructions
and require only short spans of attention. We further applied the Unified
Parkinson's Disease Rating Scale (UPDRS), including the section of activities
of daily living (ADL), and the Schwab and England test. Both test series were
performed between 8 AM and 5 PM. All technical prerequisites were identical
and have been described in detail.9 The mean
± SD time interval between the examinations was 19.8 ± 2.8 months.
The statistical analysis used standard descriptive statistics, Wilcoxon signed
rank tests, and Spearman rank correlation coefficients. Continuous data are
summarized as means ± SDs. Statistical significance is recognized at P<.05.
RESULTS
On the follow-up examination, the mean ± SD age was 65.2 ±
12.3 years; PD duration, 13.53 ± 9.14 years; and levodopa treatment
duration, 8.57 ± 7.04 years. At the follow-up examination, patients
performed worse on all the visual tests with the exception of the LD, the
results of which showed a nonsignificant improvement. The deteriorations concerned
the total color spectrum and monocular and binocular CS, especially at the
middle spatial frequencies. Statistically significant declines were seen with
the FM, for 3 of 5 VT scores, and at the monocular PR (P = .04 to P<.001) (Table 1).
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Table 1. Performances on Contrast Sensitivity and Color Discrimination
in 28 Patients With Parkinson Disease at Baseline and Follow-up Examination*
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The comparison of the most significant visual findings (the VT score
at 6 cpd for CS and the total FM score for CD) with covariables showed that
the deterioration in CS (follow-up value minus baseline value) correlated
with age (P<.001), duration of PD (P = .02), and follow-up scores of Hoehn and Yahr stage (P = .04), UPDRS motor (P = .04), and ADL (P = .006) assessments. There was no significant correlation
with levodopa dosage or UPDRS mental score. The decline in CD (follow-up value
minus baseline value) showed only a mild correlation with age (P = .04). The comparison with psychiatric rating scores revealed that
the patients with the highest BPRS scores at the follow-up examination performed
worse on both CS (P = .02) and CD (P = .01) at this examination. However, there was no statistically significant
group decline in motor, behavioral, or global function, as tested by the UPDRS
and Schwab and England tests, and the medication remained the same (Table 2).
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Table 2. Principal Disease Variables in 28 Patients With Parkinson
Disease at Baseline and Follow-up Examination*
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COMMENT
In PD, CS and CD have been shown to be independent of each other; their
impairment is worse in PD patients than in age-matched controls.6
In contrast to prior cross-sectional studies, ours is the first longitudinal
study and documents the progressive deficits in both CD and CS. We applied
a strict study protocol to ensure that the 2 testing sessions were identical.
With the exception of the LD, the deterioration of CS and CD was evident throughout
the test battery. The most powerful changes were seen in the tests that are
also the most sensitive ones in cross-sectional studies, namely, the total
score of the FM for CD and the changes at the medium spatial frequencies for
CS.10 These changes cannot be owing to a decline
in visual acuity, because we excluded patients with low Snellen scores from
the follow-up examination. The decline of contrast vision was directly correlated
with follow-up motor function scores and age. Nevertheless, deterioration
of CS and CD cannot be seen as an exclusive aging phenomenon for several reasons:
(1) cross-sectional studies have convincingly demonstrated that, in terms
of decline of CD and CS, PD patients are "in advance" (doing worse) compared
with age-matched peers; (2) influence of visual aging of CS is most prominent
at high spatial frequencies,11 a phenomenon
not seen in this study; and (3) aging of CD acts through blue-yellow confusions,12 and again, there was no significant change of this
section of the FM in our group. Additive or overlapping effects of aging and
PD are, however, possible. It has been proposed that motion sensitivity (spatial
frequencies of 1 and 4 cpd, seen at temporal frequencies of 1 and 3 Hz) can
better discriminate than static sensitivity between PD progression and aging.10 However, motion detection is not only luminance dependent
but also color specific,13 which brings us
back to test CD; furthermore, there are no confirming longitudinal studies
for this hypothesis.
No specific item in the UPDRS focuses on visual function, so the clinical
impact of our observations cannot be fully delineated. However, the correlation
of visual deficits and UPDRS and ADL follow-up scores suggests that the progressive
character of color and contrast deficits may affect patient function. The
link with the psychiatric rating (BPRS) does not tell us which comes first,
visual impairment or psychiatric deterioration; although, in a previous study,9 we demonstrated that patients with visual impairment
are at higher risk for developing visual hallucinations. Because of the insidious
character of deterioration of contrast and color perception, the patients
may not be able to compensate in the same way as they might for a suddenly
apparent but nonprogressive visual deficit. Lack of correct visual feedback
may subjectively "rattle" the patient while walking. Errors of contrast and
color perception may raise the potential for overinterpretations or misinterpretations
of the visual input and thus cause or contribute to various clinical signs,
such as frequent falls, misperceptions of distances and contours, illusions,
and even visual hallucinations.9, 14
A larger follow-up study using multivariate techniques should clarify possible
links to these frequent signs of advanced PD.
AUTHOR INFORMATION
Accepted for publication May 7, 2002.
Author contributions: Study concept and design (Drs Diederich and Goetz); acquisition of data (Dr Diederich); analysis and interpretation of data (Drs Diederich, Leurgans, and Goetz and Ms Raman); drafting of the
manuscript (Drs Diederich and Goetz and Ms Raman);
critical revision of the manuscript for important intellectual content (Drs Diederich, Leurgans, and Goetz); statistical expertise (Drs Diederich and Leurgans and Ms Raman); obtained funding (Dr Diederich); administrative, technical, and material
support (Dr Goetz); study supervision (Dr Goetz).
This study was supported by Foundation Think, Luxembourg, and the Parkinson
Disease Foundation, New York, NY.
This study was presented as a poster at the Annual Meeting of the American
Academy of Neurology, San Diego, Calif, May 1, 2000.
Corresponding author and reprints: Nico J. Diederich, MD, Department
of Neuroscience, Centre Hospitalier de Luxembourg, 4, rue Barblé, L-1210,
Luxembourg (e-mail: diederich.nico{at}chl.lu).
From the Departments of Neurological Sciences (Drs Diederich, Leurgans,
and Goetz) and Preventive Medicine (Dr Leurgans and Ms Raman), Rush-Presbyterian-St
Luke's Medical Center, Chicago, Ill; and Department of Neuroscience, Centre
Hospitalier de Luxembourg, Luxembourg (Dr Diederich).
REFERENCES
| |
1. Harnois C, Di Paolo T. Decreased dopamine in the retinas of patients with Parkinson's disease. Invest Ophthalmol Vis Sci. 1990;31:2473-2475.
FREE FULL TEXT
2. Bodis-Wollner IG, Antal A. On the functional significance of primate retinal dopamine receptors. J Neural Transm Suppl. 1995;45:67-74. Review.
PUBMED
3. Bohnen NI, Minoshima S, Giordani B, Frey KA, Kuhl DE. Motor correlates of occipital glucose hypometabolism in Parkinson's
disease without dementia. Neurology. 1999;52:541-546.
FREE FULL TEXT
4. Hutton JT, Morris JL, Elias JW, Varma R, Poston JN. Spatial contrast sensitivity is reduced bilateral in Parkinson's disease. Neurology. 1991;41:1200-1202.
FREE FULL TEXT
5. Price MJ, Feldman RG, Adelberg D, Kaynes H. Abnormalities in color vision and contrast sensitivity in Parkinson's
disease. Neurology. 1992;42:887-890.
FREE FULL TEXT
6. Pieri V, Diederich NJ, Raman R, Goetz CG. Decreased color discrimination and contrast sensitivity in Parkinson's
disease. J Neurol Sci. 2000;172:7-11.
FULL TEXT
|
ISI
| PUBMED
7. Büttner Th, Kuhn W, Müller Th, Patzold T, Heidbrink K, Przuntek H. Distorted color discrimination in de novo Parkinsonian patients. Neurology. 1995;45:386-387.
ABSTRACT
8. Acheson JF, Sanders MD. Vision. J Neurol Neurosurg Psychiatry. 1995;59:4-15.
ISI
| PUBMED
9. Diederich NJ, Goetz CG, Raman R, Pappert EJ, Leurgans S, Piery V. Poor visual discrimination and visual hallucinations in Parkinson's
disease. Clin Neuropharmacol. 1998;21:289-295.
ISI
| PUBMED
10. Bodis-Wollner IG, Paulus W. Visual and visual cognitive dysfunction in Parkinson's disease: spatial
and chromatic dysfunction. Adv Neurol. 1999;80:383-388.
PUBMED
11. Kline DW. Aging and the spatiotemporal discrimination performance of the visual
system. Eye. 1987;1:323-329.
12. Pinckers A. Color vision and age. Ophthalmologica. 1980;181:23-30.
ISI
| PUBMED
13. Cropper SJ, Derrington AM. Rapid colour-specific detection of motion in human vision. Nature. 1996;379:72-74.
FULL TEXT
| PUBMED
14. Fénelon G, Mahieux F, Huon R, Ziegler M. Hallucinations in Parkinson's disease: prevalence, phenomenology and
risk factors. Brain. 2000;123:733-745.
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