Neurol Sci DOI 10.1007/s10072-014-1930-2

ORIGINAL ARTICLE

Visual dysfunction in patients with Parkinson’s disease and essential tremor Ivanka Sˇtenc Bradvica • Mario Bradvica Suzana Matic´ • Patricia Reisz-Majic´



Received: 25 April 2014 / Accepted: 18 August 2014 Ó Springer-Verlag Italia 2014

Abstract The aim of this study was to determine the specificity and sensitivity of the Pelli-Robson and Ishihara diagnostic methods in differing Parkinson’s disease from essential tremor compared to DaTSCAN (dopamine transporter scan) findings. The intention was to investigate whether visual dysfunction appears in the early state of Parkinson’s disease. Therefore, we included patients with the symptomatology of parkinsonism lasting between 6 and 12 months. The study included 164 patients of which 59 (36.0 %) suffered from Parkinson’s disease, 51 (31.1 %) from essential tremor, and 54 (32.9 %) healthy patients which presented the control group. The specificity of PelliRobson test in confirming Parkinson’s disease was 53 % and the sensitivity 81.4 %. The specificity of Ishihara test in confirming Parkinson’s disease was 88.2 %, and sensitivity 55.9 %. We found that the colour and contrast dysfunction are present as the earliest symptoms of Parkinson’s disease. In this study the Pelli-Robson test is highly sensitive and the Ishihara tables are highly specific in the differential diagnosis between Parkinson’s disease and essential tremor, but neither of these methods fulfils the criteria for the validity of a test. We suggest performing both of these methods to evaluate which patients are indicated for DaTSCAN. Keywords Pelli-Robson test  Ishihara test  Contrast sensitivity  Colour dysfunction  Parkinson’s disease I. Sˇtenc Bradvica (&) Department for Neurology, Osijek University Hospital Center, Osijek, Croatia e-mail: [email protected] M. Bradvica  S. Matic´  P. Reisz-Majic´ Department for Ophthalmology, Osijek University Hospital Center, Osijek, Croatia

Introduction The presence of different non-motor symptoms in patients with Parkinson’s disease are intensively investigated lately [1, 2]. As the Parkinson’s disease progresses, the neurodegeneration diffusely involves the central nervous system which correlates with the appearance of the visual and other non-motor disturbances in Parkinson’s disease [3, 4]. The most of Parkinson’s disease patients suffer from the tremor dominant type of the disease which symptoms mostly overlap with essential tremor [4]. In patients with essential tremor, the tremor may be asymmetric and may be associated with bradykinesis and rigidity. On the other side, some patient with Parkinson’s disease may have postural and hyperkinetic tremor, so the differential diagnosis between these two illnesses is difficult in some cases [5]. The most adequate technique in differing these two states is the single photon emission computed tomography also called DaTSCAN, which is normal in patients with essential tremor and affected in patients with Parkinson’s disease [6–8]. Recent studies confirm that visual contrast dysfunction and the colour detection are the earliest signs of Parkinson’s disease. These disorders are caused by the damage of dopaminergic system of the retina which in consequence leads to a reduction of dopamine in amacrine and plexiform retinal cells [9–13]. This study is based on the assumption that people who suffer from Parkinson’s disease may significantly have a greater contrast and colour vision dysfunction. Therefore, in this study we determined the sensitivity and specificity of colour and contrast vision tests in patients with Parkinson’s disease. All results were compared with the DaTSCAN findings, which in this study is taken as a gold standard.

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The aim of this study was to indicate the necessity of implementing non-invasive and easy to perform colour and contrast vision tests in the early stages of parkinsonism to determine the differential diagnosis as early as possible and to determine which patients need to be investigated by DaTSCAN. The ability to discern contrast is essential in recognizing faces, reading, working at a computer, as well as in performing other daily activities [14]. In a healthy population the values of Pelli-Robson vary depending on age. At the age of 30–39 years the values are 1.99, while in the population from 40 to 49 years they are about 1.73 and in the age above 60 years they are 1.68 or even less [15]. Result 1.0 is a tenfold loss of contrast sensitivity, which means that people with this impairment need ten times greater contrast to see anything in comparison with a person with normal contrast sensitivity. A great loss of contrast vision significantly disables person in everyday life because it affects the visuoperceptual and visuomotor functions [16]. Qualitative impairment of colour vision is determined using Ishihara tables [17]. In the general population, the colour blindness occurs in 5–8 % of men and 0.5 % of women. So far, no data suggest about the specificity and sensitivity of the Ishihara test in patients with Parkinson’s disease [18].

Patients and methods We included 110 patients with clinical signs of parkinsonism lasting between 6 months and a year divided into two groups, and the third group of 54 healthy patients. The first group consisted patients whose findings were positive on DaTSCAN, which confirmed Parkinson’s disease, and the second group was patients with negative findings which indicated the presence of essential tremor. All patients were on therapy regarding their medical state. Third group consists of healthy patients, age matched to the first two groups. The contrast vision dysfunction was determined by PelliRobson test while the colour vision dysfunction by Ishihara tables. The tests were performed by a trained medical technician who was not aware about patients’ medical status. DaTSCAN is an analogue of cocaine, which binds with high selectivity for the dopamine transport proteins on presynaptic nigrostriate dendrites [8]. DaTSCAN is used as a biological marker which is convertible in vivo to show graphically the density of dopaminergic neurons in the striatum, and consequently, their preservation and function. In healthy people as well as in people with essential tremor, nigrostriate routes are fully preserved.

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In people who are suffering from Parkinson’s disease, corticobasal degeneration, multiple system atrophy, progressive supranuclear palsy, or dementia with Lewy bodies, DaTSCAN shows a marked deficit of striatal dopaminergic neurons, which is usually expressed on both sides, and sometimes it is asymmetric with stronger expression on the side where the disease started, so, therefore, these patients were excluded from this study. The study is based on the assumption that people who suffer from Parkinson’s disease are significantly more likely to have damage of contrast and colour vision. Therefore, in this study we determined the sensitivity and specificity of diagnostic tests for colour and contrast vision dysfunction in patients with Parkinson’s disease and essential tremor and compared the results to DaTSCAN findings, which in this study presented the golden standard for the differential diagnosis between Parkinson’s disease and essential tremor. Depending on the DaTSCAN findings, two groups of patients were formed: the first group whose findings were positive, which confirmed Parkinson’s disease, and second group with negative findings which indicated the presence of essential tremor. The study involved patients who had presented extrapyramidal symptomatology lasting between 6 months and 1 year. All respondents who have had any secondary or familial forms of parkinsonism were excluded from the study, which was determined on the basis of anamnesis, clinical examination and computed brain tomography. All patients who had head trauma, who had taken some of the drugs that could cause parkinsonism, those who were in contact with toxins, as well as those who had previously suffered a possible infection of the central nervous system were also excluded from the study. All patients with some clinical signs that could refer to multiple system atrophy or corticobasal degeneration were excluded from the study. The first group consisted of subjects who were suffering from idiopathic Parkinson’s disease according to the clinical history, which was confirmed with positive finding DaTSCANs. The second group included the patients who had a clinical picture of essential tremor, which was confirmed by the finding of normal DaTSCANs. The third group of healthy one which was taken as a control group did not undergo a DaTSCAN. Pelli-Robson test is designed to examine each eye separately first, and then the binocular contrast recognition. Pelli-Robson test measures contrast sensitivity by individual capital letters. Each line contains six letters, grouped into three letters of the same contrast intensity. In groups, contrast varies from stronger to weaker. Respondents read letters from stronger to weaker contrast until they are able to read two or even all three letters in each group and the result is recorded.

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The result is a measure of the logarithm of the subject’s contrast sensitivity. So the result of 2.0 means that the respondent is able to read at least two of three letters with a contrast ratio of 1 % and then contrast sensitivity is hundred percent, or log 2.0. The result, therefore, suggests normal contrast sensitivity. The result less than 2.0 indicates lower contrast sensitivity, the result less than 1.5 indicates visual impairment, and the result less than 1.0 indicates complete visual contrast impairment. Result 1.0 is a tenfold loss of contrast sensitivity, which means that people with these impairments need ten times greater contrast to see anything in comparison with a person with normal contrast sensitivity. Ishihara tables were designed by Shinobu Ishihara in 1917, to detect disorders of colour perception. This disorder can be inherited or acquired. The test consists of 24 different templates made of coloured dotted pattern forming a figure, or a curve, that healthy individuals very easily distinguish within a few seconds, while people with colour vision impairment hardly recognize displayed number, or do not even notice it. If a patient does not recognize one or more templates, the test is considered positive and indicates the presence of colour vision disorder. Patients with eye diseases that might cause contrast or colour vision dysfunction, namely those with glaucoma,

cataracts, complicated and advanced diabetic retinopathy were also excluded from the study.

Table 1 Mean values and distribution of the level of contrast sensitivity

Sv (SD)a

Parameters

N

Statistical methods To determine the difference in the measured parameters between groups of patients with Parkinson’s disease and essential tremor, Student’s t test for parametric and Mann– Whitney U test for nonparametric analysis were used. To determine the difference in proportion between two independent samples, v2 test and Fisher’s exact test were used. For three independent samples Kruskal–Wallis test was used. For the statistical evaluation of the classification procedures sensitivity (measured accuracy in positive examples) and specificity (a measure of the accuracy of the negative examples) measurements were applied. For the assessment of the significance of the results, significance level a = 0.05 was chosen. Statistical analysis with SAS Software System for Windows (version 8.2, SAS Institute Inc., Cary, NC, USA) was performed.

Results The group of patients with essential tremor included 51 patients, the group with Parkinson’s disease 59 and the Min–max

Median

25–75 %

pb

\0.001

Contrast sensitivity—Pelli-Robson (right eye) Essential tremor

51

1.51 (0.18)

1.2–1.95

1.50

1.35–1.65

Parkinson’s disease

59

1.37 (0.21)

0.9–1.95

1.35

1.20–1.50

54

1.52 (0.07)

1.35–1.65

1.50

1.50–1.50

164

1.43 (0.21)

0.9–1.95

1.35

1.35–1.65

1.52 (0.17) 1.37 (0.2)

1.2–1.95 0.9–1.95

1.65 1.35

1.35–1.65 1.20–1.50

54

1.52 (0.07)

1.35–1.65

1.50

1.50–1.50

164

1.44 (0.2)

0.9–1.95

1.35

1.35–1.65

Control group Total

Contrast sensitivity—Pelli-Robson (left eye) Essential tremor Parkinson’s disease Control group Total

51 59

\0.001

Contrast sensitivity—Pelli-Robson (bilaterally)

a

Mean value (standard deviation)

b

Kruskal–Wallis test

Table 2 Distribution of patients according to the results of the Ishihara test

Essential tremor

51

1.53 (0.18)

1.2–1.95

1.65

1.35–1.65

Parkinson’s disease

59

1.39 (1.99)

0.9–1.95

1.35

1.35–1.50

Control group Total

Ishihara test results

Do not recognize colours Kruskal–Wallis test

1.55 (0.11)

1.00–1.65

1.50

1.50–1.65

1.46 (0.19)

1.05–1.95

1.35

1.35–1.65

Total

pa

Respondents Essential tremor

Recognize colours

a

54 164

\0.001

Parkinson’s disease

Control group

Total 125 (77)

45 (88.2)

26 (44.1)

54 (100)

6 (11.8)

33 (55.9)

0

51 (100)

59 (100)

54 (100)

\0.001

39 (23) 164 (100)

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control group 54 patients. With regard to gender, 80 (48.8 %) of patients were male and 84 (51.2 %) were female (Fischer exact test p = 0.021). There were significantly more women in the group with essential tremor, and men in the group of patients with Parkinson’s disease. In the control group they were equally divided. Bilateral contrast sensitivity gives significantly higher mean values in the group of patients with essential tremor and the control group. The result was 1.53 (±0.18) and 1.55 (±0.11), respectively, while in patients suffering from Parkinson’s disease it was 1.39 (±0.18) (Kruskal–Wallis test, p \ 0.001). Mean values of contrast sensitivity suggest that the group of patients with essential tremor belongs to the group of those with a lower contrast sensitivity, while in the group of patients with Parkinson’s disease, the contrast sensitivity was classified to the group of those with visual impairments. Significant differences were proven between the groups, Table 1. According to the Ishihara tables, a total of 39 patients from both groups do not recognize colours. This test determined a high proportion of patients with Parkinson’s disease which does recognize colours (44.1 %) and thus gave us a low sensitivity of this test in the confirmation of Parkinson’s disease. Significantly more patients suffering from Parkinson’s disease did not recognize colours, 33 (55.9 %) compared to 6 (11.8 %) patients with essential tremor (Kruskal–Wallis test, p \ 0.001), Table 2. In confirmation of Parkinson’s disease the specificity of Ishihara test was 88.2 % and the sensitivity 55.9 %. All patients from the control group recognized colours.

Discussion The main features of Parkinson’s disease, particularly akinesia and rigidity occur only at a level of 70–80 % loss of dopaminergic cells in the substantia nigra [19]. This stage precedes prolonged latent period of lack of striatal dopamine, which is inconspicuous due to compensatory increase in the activity of the remaining neurons and hypersensitivity of the postsynaptic dopamine receptors [3, 4, 9]. In this asymptomatic period blurred vision, decreased contrast sensitivity and reduced chromatic vision appears. It is believed that the basis of these disturbances is in the dopaminergic retinal system damage [20]. In patients with essential tremor disturbances of colour, or contrast vision were not found [10, 21, 22]. For the diagnosis of essential tremor there are still any standardized tests or biological markers [23, 24]. The diagnosis of essential tremor in most cases is based on clinical observation, medical history and clinical status, while the extremely doubtful cases have indication for DaTSCAN

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[25]. In the classical essential tremor there is a bilateral, symmetrical postural and/or kinetic tremor affecting the hands and it is constantly present [26]. Essential tremor is excluded if it is present with signs of dystonia, drug exposure to tremor inducing drugs, in an isolated voice tremor, isolated tongue and legs tremor, tremors in particular specific position, or a clear psychological substrate rapidly forthcoming tremors [27]. In patients suffering from Parkinson’s disease, DaTSCAN shows a deficit of dopaminergic system in the striatum area. DaTSCAN is a very reliable, but invasive screening method because of a contrast agent and the radiation exposure. In patients with essential tremor nigrostriatal system is fully intact due to a different pathophysiological basis of this type of tremor [7]. Results of some studies suggest a pathophysiological disorder in the olivocerebellar rhytmicity [24]. It is, therefore, considered that people with essential tremor may be similar to the control group of healthy one. DaTSCAN has a high sensitivity of 97.5 % and a specificity of 100 % in the confirmation of Parkinson’s disease [28]. For these reasons, in this study, on the basis of the clinical examination, computed tomography of the brain and using all inclusive and exclusionary criteria, we excluded all potential patients who might possibly suffer from any other form of parkinsonism, so called any secondary or Parkinson plus syndrome. Lately researches are focused on the early detection of the signs of Parkinson’s disease using non-invasive functional tests of vision, smell, sleep disorders, depression, autonomic and other disorders [9]. Most of these methods with the aim of early differential diagnosis of parkinsonism seem that they are still not carried out routinely in clinical practice Visual dysfunction in patients with Parkinson’s disease are not considered cardinal, although numerous studies have indicated that these patients often have blurred vision, photophobia, tired eyes, reduced vision as well as difficulties in reading [29, 30]. Patients with Parkinson’s disease do not lead to a loss of visual acuity, but they have a subclinical colour dysfunction, especially in the blue-green axis and contrast vision defects [22]. In amacrine cells of the retina, the main neurotransmitter is dopamine [31]. Vesela and colleagues [32] in their study did not determine that the colour vision dysfunction is a reliable early sign of Parkinson’s disease. Comparing the results of the Farnsworth–Munssel test and Lanthony test for colour, Tabassi in his research confirmed the dysfunction of colour vision with both tests in patients with Parkinson’s disease [10]. Oh, in his research found significantly greater damage of colour vision in patients with Parkinson’s disease compared with the findings in patients with essential tremor [21]. All authors pointed to the need for further and more detailed investigations of colour vision defects in patients with Parkinson’s disease. All those authors used

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the Farnsworth–Munsell test in their study, while Ishihara tables in detecting colour vision defects in patients with Parkinson’s disease have not been used. The first studies that indicate impairment of contrast vision in patients with Parkinson’s disease started in 1987, when Mr. Bodis-Wollner and colleagues [33] found contrast vision dysfunction in these individuals. Further studies confirm that disorder and so Pieri et al., Haug et al., Jones et al., as well as Diederich et al. also found contrast vision dysfunction in patients with Parkinson’s disease, suggesting a deficiency of dopamine in the visual system [11, 16, 17, 22]. Proven lack of dopamine in the retina of patients could be responsible for both the reduction of visual acuity and colour vision damage. Contrast sensitivity dysfunction becomes most evident in the conditions of reduced brightness as it is at dawn or at dusk. This contributes to a significant appearance of visual hallucination and impossibility of starting the movement of people with Parkinson’s disease [34]. People with Parkinson’s disease often notice blurred vision despite good visual acuity. They often suffer of ‘‘fatigue in their eyes’’, blurred vision when reading, and this interference can be confirmed only with detailed examination. Very subtle changes in visual acuity in patients with Parkinson’s disease correlate with the stage of the disease. We found no available data of possible colour and contrast dysfunction in patients with essential tremor, as well as no data about the specificity and sensitivity of this tests. In this study contrast vision impairment was found in all groups, but in patients with essential tremor and the control group the dysfunction was at the level of lower contrast sensitivity, whereas in the group of patients with Parkinson’s disease contrast sensitivity was mostly present at the level of visual impairment (Table 1). The specificity of Pelli-Robson test in confirming Parkinson’s disease in this study is 53 %, and the sensitivity 81.4 %. According to these results, the sensitivity of Pelli-Robson test is acceptable, but the relatively low specificity of this test indicates that a small proportion of truly healthy people out of the total number of healthy individuals may be detected with this test. Numerous works show an impairment of colour vision or inability of adequate colour vision recognition in patients with Parkinson’s disease [10, 21, 22]. In these studies the Farnsworth–Munsell test was used. Ishihara tables are much easier to use in everyday clinical practice, but for now they are mainly used in the assessment of visual impairment in patients with dementia [18, 35]. In this study, significantly more patients suffering from Parkinson’s disease did not recognize colours (Table 2).

The specificity of Ishihara test was 88.2 % and the sensitivity 55.9 % in confirming of Parkinson’s disease. Results of this study confirmed a statistically significant difference in impairment of colour and contrast vision in patients with Parkinson’s disease compared to patients with essential tremor. In this study, Pelli-Robson contrast sensitivity test is due to its high sensitivity useful in confirming the sick person as truly sick, unlike Ishihara tables in colour vision testing that showed low sensitivity. Inversely, Ishihara tables according to the results of this study have confirmed the high specificity for Parkinson’s disease, and the PelliRobson test has low specificity. If we would use those tests in clinical practice, both criteria must be met as a condition, must have high enough sensitivity, and specificity, otherwise the tests would confirm a small number of truly healthy as healthy (the specificity of the test), and the sick persons would not be recognized as sick (sensitivity of the test). In this study Ishihara tables and Pelli-Robson test were not confirmed as accurate methods in the differential diagnosis between Parkinson’s disease and essential tremor, but they can confirm the visual dysfunction in this group of patients in comparison to healthy one. The implementation of these methods for contrast and colour vision impairment detection is important for evaluating these dysfunctions in the early stages of the diseases, but they are of minor validity for the differential diagnosis between Parkinson’s disease in relation to essential tremor. For the final differentiation DaTSCAN should be performed.

Conclusions It is advisable to conduct this tests for colour and contrast vision dysfunction, although the results of this study indicate that the Pelli-Robson test has a slightly lower specificity and Ishihara tables a lower sensibility in the differential diagnosis of Parkinson’s disease and essential tremor. We conclude that these tests should be implemented as a basis for a better selection of patients before referring to DaTSCAN. Conflict of interest of interest.

The authors declare that they have no conflict

Ethical standard statement This study has been approved by Ethical committee of University Hospital Center in Osijek and has, therefore, been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. Informed consent statement All patients gave their informed consent prior to their inclusion in the study.

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Visual dysfunction in patients with Parkinson's disease and essential tremor.

The aim of this study was to determine the specificity and sensitivity of the Pelli-Robson and Ishihara diagnostic methods in differing Parkinson's di...
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