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January2008 Vol.45 Issue:      1 Table of Contents
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Screening for Cognitive Dysfunction in Patients with Hypothyroidism

Mahmoud Allam1, Sadek Helmy1, Shereen Fathy1, Akmal Moustafa2, Ashraf M. Ginina3, Nermeen Adel Kisk1, Husam Salah1
Departments of Neurology1, Psychiatry2, Cairo University; Internal Medicine3, Beni Souif University3

ABSTRACT

Thyroid disorders had been incriminated a lot in reversible dementia at the end of the last century. Yet, the relation between myxedema per se and cognitive dysfunction has been of great concern nowadays. Our aim of work is to screen the incidence and delineate the characteristics of cognitive dysfunction that may occur in association to hypothyroidism; also to decide the best test to achieve rapid diagnosis in such a problem. Subjects & Methods: our study included 50 subjects; 30patients (20 patients with overt hypothyroidism and 10 with subclinical hypothyroidism) and 20 healthy subjects serving as control group. All were submitted to general medical and neurological examination, laboratory investigations to complete the diagnosis of hypothyroidism, MRI brain, P300 latency assessment and neuropsychological assessment (WAIS-R,WMS-R and tests for frontal executive functions). Results: A definite cognitive impairment in both hypothyroid patient`s group was noted in comparison to controls, as proved by statistically significant prolonged absolute P300 latency and positive neuropsychological tests among them. Conclusion: WAIS subtests especially: [Picture arrangement test, Block design test and Digit backward test] can be used as a premonitory test to detect cognitive dysfunction with hypothyroidism.

(Egypt J. Neurol. Psychiat. Neurosurg., 2008, 45(1): 175-184)

 




INTRODUCTION

 

Dementia is one of the diseases that are of increasing frequency nowadays forming great burden on self, family and community. Its reversible forms are solving this burden with great hope and increasing efficiency1. Thyroid hormones (TH) play a crucial role as a regulator of cellular metabolic activity, also regulate neural development; the central nervous system is particularly dependent on them for normal maturation and function. Specifically, there appears to be an extensive inter-reliance between TH and acetylcholine (Ach), nerve growth factor and hippocampal function. These associations led us to investigate the possible effects of thyroxine (L-T4) on performance of a spatial learning task, where cholinergic activity and hippocampal function are known to be important2.

Thyroid gland disorders may affect cognitive functions in specific ways3. However, in our study we focused only on hypothyroid dysfunction. The clinical presentation of hypothyroidism varies considerably and may be dominated by cognitive deficits and psychological symptoms. Hence, when diagnosing dementia it is important to rule out hypothyroidism. Hypothyroidism has also been considered a classic reversible dementia; however, the etiological association between dementia and hypothyroidism is by no means debatful3. 

Isolated increase in TSH in patients completely free of any symptoms of thyroid disorders and with normal -total and free- thyroid hormone levels is quite a frequent phenomenon which affects 3 to 7 percent of middle aged population. The frequency of such cases in the population over 60 years of age, especially in women, may be as high as 17 percent4.

Recently, it has been shown that patients formerly considered as completely symptom free, may have plenty of minimal, often non-specific subjective complaints, and those patients it is possible to prove many subtle, but objective deviations compared to euthyroid individuals5.

The aim of work is to screen the incidence of cognitive dysfunction that may occur in hypothyroidism types; to delineate the characteristics of cognitive dysfunction in these patients and to decide the best test to achieve diagnosis in such a problem.

 

SUBJECTS AND METHODS

 

The present study included 50 subjects; 30 patients having hypothyroidism (randomly selected from Endocrine Out-patient Clinic of Kasr El-Aini Hospitals) with 20 healthy volunteers matching to age, sex and educational level as control group.

 

Inclusion criteria:

A.   Hypothyroid patients diagnosed on clinical and laboratory basis. They were subdivided into 2 categories4,5:

Group 1: [Overt Hypothyroidism (OH)]; 20 patients characterized by the presence of both clinical and biochemical manifestations of thyroid hormone deficiency.

Group 2: [subclinical hypothyroidism (SCH)]: 10 patients with a state of early mild clinical syndrome of hypothyroidism in spite of normal levels of thyroid hormones (T4 and T3), but elevated levels of TSH.

B.    Mini Mental Test (MMT) more than 24 to all patients.

C.    Normal MRI brain is a must to be included in the study.

 

Exclusion criteria:

1.   Subjects with any other neurological disorders.

2.   Patients with any other psychiatric disorders as diagnosed by ICD10.

3.   Positive Family history of dementia.

4.   Patients with any other systemic diseases.

All the 50 subjects were submitted to the following battery of investigations:

§  Meticulous medical, neurological and psychiatric history and examination.

§  Laboratory investigations to exclude any other medical (metabolic) disorders and to ensure the diagnoses of hypothyroidism.

§  Neurophysiological test: Long latency evoked potentials (P300).

§  Neuropsychological assessment which included:

I.       Wechsler Adult Intelligence Scale-Revised (WAIS-R)7: We selected the following subtests in this study (An Arabic edition is used):

a.   Similarities: to assess the ability to reason from verbal concepts & also assess semantic memory.

b.   Block Design: to test the visuo-spatial abilities.

c.   Picture arrangement: to assess the ability for planning.

II.      Wechsler Memory Scale-Revised (WMS-R)8: We selected the following subtests in this study (An Arabic edition is used):

1.             Visual memory subtests:

We select a,b &c to assess the (non verbal working memory):

a.   Figural memory.

b.   Visual Paired Associates.

c.   Visual Reproduction.

d.   Digit Span: to test the attention process and working memory.

e.   Digit forward: (Normal: 6±1, Bordline or impaired: 4 & Defective: 3)

f.    Digit backward: (Normal: 5±1, Bordline or impaired: 3 & Defective: 2) 

2.      Logical Memory Subtest: to test reasoning memory.

III.     Frontal executive functions: (Initiation, Response shifting and Set shifting): through Controlled Oral Word Association Test (COWA)9: It assesses the ability to generate responses by having them produced as many words as possible in one minute related to certain category, beginning with the names of foods, then names of animals.

 

Statistical methods used:

q  Descriptive statistics for parametric data and frequency tables for categorical data.

q  Independent t-test for all parametric data when comparing between two groups.

q  Man-Whitney test for all parametric data with small group size when comparing between two groups.

q  Chi-square test for all non-parametric data when comparing between groups.

q  ANOVA test followed by Post-Hoc Duncan when comparing between three groups.

q  Pearson Correlation Coefficients when examining the strength between two parametric variables.

q  Discriminant analysis is used to identify variables that can discriminate groups from each other.

 

RESULTS

 

The present study included 50 subjects, 30 patients of hypothyroidism and 20 healthy subjects matching to age, sex and educational level were taken as control. Their ages ranged from 18 to 50 years with a mean age of 35.49±9.61 years. The study included 3 males (15%) and 17 females (85%) in the G1, 2 males (20%) and 8 females (80%) in G2. Regarding the control group the study included 4 males (20%) and 16 females (80%). The duration of hypothyroidism in (G1) ranged from 2 months till 5 years with a mean±SD of 2.31±1.40 years, while in (G2) ranged from 4 months to 4 years with a mean±SD of 1.88±1.15 years. There was no statistical difference among sex and duration between different groups proving homogenous sample.

Delayed absolute latency of P300 could unmask cognitive dysfunction only in 3 patients [15%] of (G1)  of our patients. By the same time means±SD of P300 latency was statistically significant higher in (G1) than both (G2) and control group means (Table 1) (P=0.001).

All the Neuropsychological tests were able to declare the cognitive dysfunction in our hypothyroid patients. Much important, the mean±SD of scores of WAIS, WMS subtests and COWA test showed a significant statistical reduction in both hypothyroid groups in comparison to control group (Tables 2, 3 & 4).

As regards the impact of duration of illness on the psychological subtests used for screening hypothyroid dementia; an interesting finding was noted in the form of existence of low scores of these subtests in parallel to long duration of illness denoting negative statistically significant correlation between duration of illness and such psychological subtests, mainly in (G1) (P<0.05) as shown in (Table 5). On the other hand, there were no statistically significant correlations between duration of illness and latency of P300 among different groups.

A remarkable outcome was noted in the study, that delayed P300 latency to be statistically significant correlated with low scores of Block Design in the WAIS subtests (P=0.01) and low scores of Digit Backward in the WMS subtests (P=0.02) in SCH group. This specifies cognitive dysfunction in such group. However, other subtests showed no significant correlation with P300 latency.

Alterations in thyroid hormonal levels was not reflected on P300 latency results on both groups in our study. This was proved by absence of any statistically significant correlations between FT3, FT4 and TSH levels with P300 latency among different groups (P>0.05). On the other hand, a statistically significant correlation was noted between some neuropsychological subtests and thyroid hormones variations as illustrated in table (6).

A positive correlation which was statistically significant between FT4 levels with scores of COWA in the overt group (P=0.04). Also, there was a correlation between increased scores of COWA test and low levels of TSH; such negative correlation was statistically significant (Table 7).

To analyze which of the tests used in the study has the power to screen for dementia among hypothyroid patients; Discriminate analysis (which is a multivariate test that uses many variables in the same time to discriminate between groups) was used. Table (8) shows the order of such tests. It showed that [Picture Arrangement test] which is a subtest of WAIS and exclusively attest the ability for planning is the best discriminate followed by [Block Design test] which is a subtest of WAIS and exclusively attest visuo-spatial abilities then [Digit Backward test] which is a subtest of WMS and exclusively attest visual working memory in association of attention processes. While P300 was not able to discriminate between groups.


 

Table (1): Mean±SD of P300 latency among all groups of the present study.

 

 

Group

N

NL results

%

Abn. results

%

Mean

SD

F-value

P-value

 

P300

 

G1

20

17

85

3

15

396.55

90.09

14.00

0.001**

G2

10

10

100

0

0

309.03

34.55

Control

20

20

100

0

0

302.19

18.28

**= highly significant

 

 

Fig. (1): Figure of P300 test among our patient.

Table 2. Mean±SD of WAIS subtests scores in different groups of the present study.

 

WAIS subtests

Group

No.

Mean

SD

F-value

P-value

Block Design

G1

20

5.25

0.72

80.92

0.001**

G2

10

5.4

0.70

Control

20

11.2

2.38

Similarities

G1

20

8.1

1.74

9.50

0.001**

G2

10

7.7

1.16

Control

20

10.1

1.89

Picture Arrangement

G1

20

6.35

0.75

83.73

0.001**

G2

10

7

0.82

Control

20

10.95

1.61

**= highly significant

 

Table 3. Means±SD of scores of WMS subtests among different groups of the present study.

 

WMS subtests

Group

Mean

SD

F-value

P-value

Figural Memory

 

G1

3.4

1.31

50.21

0.001**

G2

4.3

0.95

Control

6.95

1.05

Visual Paired Associate I

 

G1

4.75

1.62

64.04

0.001**

G2

6.4

2.46

Control

10.65

1.23

Visual Reproduction I

 

G1

1.65

1.18

49.88

0.001**

G2

2.2

0.92

Control

4.5

0.61

Digit Forward

G1

3.75

1.52

57.67

0.001**

G2

5.3

1.95

Control

8.3

0.66

Digit Backward

 

G1

2.25

1.33

52.29

0.001**

G2

3

1.49

Control

6

0.86

Logical Memory

G1

17.2

4.83

60.16

0.001**

G2

21.1

5.67

Control

32.3

3.25

**= highly significant

 

 

Table 4. Means±SD of scores of COWA test among different groups of the present study.

 

COWA

Group

N

Mean

SD

F-value

P-value

 

COWA

 

G1

20

12.9

2.79

13.41

0.001**

G2

10

13.8

2.62

Control

20

16.5

1.24

 **= highly significant

Table 5. Correlation between duration and WMS subtests in hypothyroid groups.

 

WMS subtests

Duration

group

r-value

p-value

Figural Memory

G1

-0.55

0.012*

G2

-0.004

0.99

Visual Paired Associate I

G1

-0.47

0.038*

G2

-0.40

0.25

Visual Reproduction I

G1

0.04

0.87

G2

-0.60

0.07

Digit Forward

G1

-0.20

0.39

G2

-0.43

0.21

Digit Backward

G1

-0.29

0.21

G2

-0.27

0.46

Logical memory

G1

-0.54

0.01*

G2

-0.49

0.15

* = significant

 

Table 6. Correlation between Thyroid hormones and WAIS subtests in hypothyroid groups.

 

WAIS subtests

FT3

FT4

TSH

G

r-value

p-value

r-value

p-value

r-value

p-value

Block design

G1

0.24

0.30

0.14

0.56

-0.11

0.64

G2

-0.27

0.46

0.44

0.21

-0.23

0.52

Similarities

G1

0.52

0.02*

0.42

0.07

-0.11

0.64

G2

-0.66

0.04*

0.31

0.39

-0.08

0.83

Picture Arrangement

G1

0.32

0.17

0.48

0.03*

-0.25

0.29

G2

0.09

0.81

0.17

0.65

-0.16

0.66

* = significant

 

Table 7. Correlation between Thyroid hormones and COWA test in hypothyroid patients groups.

 

psychometric tests

FT3

FT4

TSH

G

r-value

p-value

r-value

p-value

r-value

p-value

COWA

G1

0.39

0.09

0.46

0.04*

-0.53

0.02*

G2

-0.11

0.76

0.52

0.13

0.31

0.39

*: statistically significant.

 

Table 8. Absolute correlation between all tests in discriminating between groups.

 

Tests

Absolute correlation

Picture Arrangement

0.69*

block design

0.67*

digit backward

0.61*

P300

-0.29

*= Largest absolute correlation between each variable and any discriminant function


DISCUSSION

 

The specific defect of cognitive functions due to hypothyroidism is poorly understood10. Several studies performed in this area suggested that memory performance is especially impaired in hypothyroid patients11. Whether this memory decrement reflects a specific impairment of memory functioning per se or whether it results from deficits in more general-purpose processes that facilitate the efficient functioning of a wide array of mental operations is not known12. Although subclinical hypothyroidism(SCH)  has long been viewed as a clinically asymptomatic condition, data that SCH is associated with mild somatic symptoms that are consistent with overt hypothyroidism, as well as cognitive deficits has been an issue in the last few years to observe13.

In our present study we tried to screen the incidence of cognitive dysfunction that may occur in hypothyroidism types and we found it evident in all patient groups when attested by psychological testing. On the other hand, delayed P300 latency was present only in 15% of our patients of the overt group who had clinical and lab evidence of hypothyroidism. In line with Niedermeyer and Lopes Da Silva14.

The present study revealed delay in mean±SD absolute latency of P300 in overt and SCH groups .There is a significant statistical difference between patient groups and control group, being more delayed in the overt group. Conversely there was no significant difference between the SCH and control groups. Corresponding to Khedr et al.15 P300 mean±SD results in overt and control groups were 376±31.3 ms and 338.9±36.6 ms respectively. There is a significant difference between the results of P300 mean results between both overt and control groups being higher in the control group which supports our findings.

On the contrary Osterweil et al.16 found no significant difference between overt and control groups in the mean results of P300,that could be related to the longer duration of illness among our patients. However, on the equivalence to our study there was no significant difference between SCH and control groups in the mean results of P300 in this study. Other studies15,17, revealed a significant difference between the results of P300 means between both overt and control groups being higher in the control group which supports our findings.

In contradiction to Jensovsky et al.18, who studied the changes of event related potential in SCH and concluded that there is a significant difference between P300 latency means  results in both groups being delayed in the overt group. The difference between their study and our study is that, this study included 31 patients with average age of 52±12.5 years while our study included 10 SCH patients with average age of 36.3±9.32 years.

As regards neuropsychological testing; the selected WAIS subtests (Block design, Similarities and Picture Arrangement) showed significant difference between the mean scores of the control and both overt and SCH groups. Analogus to our study, other studies16&19, used copying a cube test to attest visuo-spatial abilities and showed a significant difference between the hypothyroid groups and healthy subjects being less in the patients groups.

Our study showed that there was significant statistical difference between patients' groups and the control group as regards the results of WMS subtests. Statistically significant higher means of the control group than those of the hypothyroid groups was shown in attesting Figural memory, Visual Paired Associate I, Visual Reproduction I and Visual Memory Span. Moreover, Digit Backward and Logical Memory test scores outcome showed that means of the control group were higher than the hypothyroid groups which denotes cognitive dysfunction. In line with researches20, who applied Bingley's memory test of immediate recognition of visual shapes to patients with overt hypothyroidism and their results were consistent with our Figural Memory results.

Osterweil et al.16, assessed memory in overt hypothyroid and SCH groups patients using Inglis-low test of weakly paired associate learning and retention. Inglis-medium test of moderately paired associate learning were impaired which is consistent with Visual Paired Associate of WMS in our study.

Baldini et al.21, Monzani et al.22, and Jensovsky et al.18, when applying the WMS test to overt and subclinical hypothyroid patients, there was an impaired results in all the tests; supporting our results. Moreover, in agreement with Del Ser Quijano et al.23, SCH patients showed significant difference in comparison with control regarding visual and verbal working memory. All insisting on the genuine cognitive dysfunction especially in SCH. On the other hand, Burmeister et al.24 showed impairment in delayed recall while other aspects were intact; However, this was not in favour of our study, which may be due to the small number of patients (which is 13 overt hypothyroid patients) used in the study while our study included 20 overt hypothyroid patients, or it may be due to patient selection who were post- thyroidectomy patients on levothyroxine and stopped treatment 5-6 weeks before the study while our patients mean duration of hypothyroidism is 2.3 years.

Our study showed that COWA score means were significantly higher in the control group than both parients` groups, along the lines of Osterweil et al.16, who was consistent with our study as the Animal Naming which is used to test for word fluency was significantly higher in the control than the overt group. Moreover, In contrast to our results COWA score test was significantly higher in the control than the SCH group. The contradiction between this study and our study may be attributed to the higher mean age±SD in their study which was 68.6±16.4 years, while in our study is 36.2±9.23 years so may be attributed to presence of Mild Cognitive Impairment or dementia in conjunction with the cognitive dysfunction in hypothyroidism. In line with Volpato et al.25, who demonstrated a higher incidence of dementia in older adults with thyroid failure and also concluded that even mild thyroid failure contributes to cognitive deficits in elderly and dementia. There was a significant positive relation between P300 and Digit Backward in SCH group but there was no other significant relation between P300 and other neuropsychological tests in patient groups. To the best of our knowledge, these relations were not mentioned in previous studies.

As regards the impact of thyroid hormone levels on neuropsychological tests; we found a significant inverse relation between FT3 levels and only Similarities test scores in the SCH group. By the same time, a significant positive relationship between FT3 and each of Figural Memory, Visual Reproduction and Similarities  was present in the OH group. Likewise, FT4 was correlated positively with all WMS subtests, Picture Arrangement, and COWA in the Overt group, but only with Visual Reproduction SCH group.  This points to capability of the used tests to unmask cognitive dysfunction with  early alteration in hormonal level in SCH, that is much important than to declare it than in the Overt group, in line with others21.

As well, a positive relation between TSH levels and COWA scores only was found in Overt group. Similar to Osterweil et al.16, who found a statistically significant correlation between a laboratory index of the severity of hypothyroidism and the Animal Naming (tests for verbal fluency and initiation).

Congruent to our results, other studies15,18,26, who found no significant correlation between thyroid hormone levels and P300 latency.

When discussing the impact of duration of hypothyroidism on neuropsychological and neurophysiological tests, it was evident by increased scores of Figural memory, Visual Paired Associate and logical Memory in the Overt group with time. So we conclude that there was no clear consistent impact of neither duration nor thyroid hormone levels on the neuropsychological and neurophysiological tests, to the best of our knowledge these relations were non-precedent results and need more evaluation in further studies.

We can conclude that patients with hypothyroidism (Overt Hypothyroidism & Subclinical Hypothyroidism) have cognitive impairment, which is most obvious in the domain of visual and verbal working memory, learning, visuo-spatial abilities, executive functions and attention. Furthermore, patient with Overt group tend to have delayed latency of P300 than the controls.

A very interesting data can be produced by this study is to validate certain tests to premonitor cognitive dysfunction in hypothyroidism. These are [Picture Arrangement test followed by Block Design then Digit Backward], who are able statistically to discriminate between groups (Overt, SCH, and control), providing valuable screening test for dementia, that is reversible at that time, saving much load on patient, family and community.

We are aiming to complete our work by attesting the effect of thyroid replacement therapy on cognitive dysfunction in hypothyroidism as regards both P300 latency and neuropsychological testing; to evaluate the cerebral changes that may occur in such condition by functional imaging as PET and SPECT, and also to verify duration of illness entity on larger number of patients in different stages.

 

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الملخــص العربـــى

 

فحص الإضطرابات المعرفية في مرضى نقصان هرمون الغدة الدرقية

 

          تضمنت الدراسة الحالية 50 فرداً: 30 مريضاً، 20 أصحاء متشابهين مع المرضى في العمر والجنس ومستوى التعليم وهم المجموعة الضابطة. وتراوحت أعمار العينة بين 18 إلى 50 سنة بمتوسط 35.49 سنة وانحراف معياري 9.16 وجميعهم غير متعلمين، وقسمت العينة إلى مجموعة من المرضى ومجموعة ضابطة.

مجموعة المرضى: شملت هذه المجموعة 30 مريضاً بمرض نقص إفراز الغدة الدرقية، وتم اختيارهم من العيادة الخارجية لأمراض الغدد بمستشفى قصر العيني، وتم تقسيم هؤلاء المرضى إلى مجموعتين فرعيتين: المجموعة الفرعية الأولى تتكون من 20 مريضاً يعانون من نقص واضح (شديد) في إفراز الغدة الدرقية، المجموعة الفرعية الثانية تضمنت عشرة مرضى لديهم نقص غير واضح (خفيف) في إفراز الغدة الدرقية، المجموعة الضابطة: تكونت من 20 فرداً من الأصحاء مشابهة لمجموعة المرضى في العمر والجنس ومستوى التعليم.

          وقد أجرى على أفراد عينة الدراسة جميعهم ما يلي: فحص طبي عام، رصد تاريخ الحالة وإجراء فحص عصبي دقيق. فحوص مختبرية لإكمال تشخيص نقص إفراز الغدة الدرقية وهي: هرمون الثيروتروبين، والثيروكسين الحر، وتراي أيودوثيرونين، رنين مغناطيسي للمخ. الجهد المثار P300. تقويم نفسي عصبي باستخدام: اختبارات فرعية من اختبار وكسلر لذكاء الكبار المعدل. اختبارات فرعية من اختبار وكسلر لقياس الذاكرة المعدل WMS-R، اختبار تداعي الكلمات الشفوي COWA.

الخلاصة : نمط القصور المعرفي لمجموعة النقص الواضح في إفراز الغدة الدرقية في المجالات التالية وخاصة الذاكرة العاملة اللفظية والمصورة والتعليم والقدرات البصرية المكانية والوظائف التنفيذية (المبادأة والتخليص والتخطيط)، والانتباه. وبالمثل فأن مجموعة النقص البسيط في إفراز الغدة الدرقية لديها نمط مشابه في القصور المعرفي. مرضى النقص الواضح في إفراز الغدة الدرقية تتسم برسم المخ البطيء عن المجموعة الضابطة. كما أنهم يتميزون بتأخر في الجهد المثار P300 عن المجموعة الضابطة. يوجد ارتباط موجب بين الجهد المثار P300 والانتباه والذاكرة العاملة البصرية لمرضى النقص البسيط في إفراز الغدة الدرقية. لا يوجد تأثير واضح ومتسق لأي من مدة المرض أو هرمون الغدة الدرقية على الاختبارات النفسية أو الفسيولوجية.

 



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