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October2013 Vol.50 Issue:      4 Table of Contents
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Optical Coherence Tomography of Retinal Nerve Fiber Thickness and Hippocampal Atrophy in Multiple Sclerosis

Mervat Mostafa1, Faisal Abd Elwahab1, Husam S. Mourad1, Ihab I. Ali2, Asmaa S. Sabbah1

Departments of Neurology1, Radiodiagnosis2, Cairo University; Egypt



ABSTRACT

Background: Gray matter brain structures, including deep nuclei and the cerebral cortex, are affected significantly and early in the course of multiple sclerosis and these changes may not be directly related to demyelinating white matter lesions. Objective: Optical coherence tomography (OCT) as a noninvasive tool used for measuring tissue at micrometer resolution as a marker of neurodegeneration and axonal loss. Methods: The study included 30 MS patients, who underwent full clinical neurological assessment, EDSS, hippocampal volume measurement and the retinal nerve fiber layer thickness (RNFLT) detection of both optic discs and 20 age and sex matched normal healthy controls. Results:  The mean hippocampal volume in MS patients was markedly reduced compared to controls. (p<0.001). MS patients showed marked reduction in RNFLT of the superior and inferior quadrants on both sides and the left temporal quadrant, compared to control subjects. No significant correlation was found between mean volumes of the right and left hippocampi and mean EDSS. A statistically significant positive correlation was found between mean volume of the right hippocampus and mean RNFLT of the left nasal quadrant, (p = 0.04) and between mean volume of the left hippocampus and mean RNFLT of the left superior, left inferior and left nasal quadrants. Conclusion: MS patients showed evident reduction in hippocampal volumes and RNFLT compared to controls. RNFL thinning correlated well with hippocampal volume loss, supporting previous findings of other studies that RNFLT measured by OCT can be used as a surrogate marker of neuro-degeneration and axonal loss in MS patients. [Egypt J Neurol Psychiat Neurosurg.  2013; 50(4): 411-417]

Key Words: OCT(optical coherence tomography), MS, RNFLT, hippocampal atrophy, hippocampal volume.

Correspondence to Husam S Mourad, Cairo University, Neurology Department, Egypt.Tel.: +201001554417    e-mail: husamneuro@kasralainy.edu.eg

 






INTRODUCTION

 

Multiple sclerosis is a progressive inflammatory disease of the central nervous system. Gray matter brain structures, including deep nuclei and the cerebral cortex, are affected significantly and early in the course of multiple sclerosis and these changes may not be directly related to demyelinating white matter lesions. Accumulation of neuronal loss is now believed to underlie the development of persistent disability in multiple sclerosis.1

The retinal nerve fiber layer (RNFL) contains ganglion cell axons that give rise to the optic nerve, and represents a unique region of the central nervous system because it lacks myelin. Visible RNFL defects may arise when inflammation causes degeneration of axons within the optic nerve.2 Advances in ocular imaging with optical coherence tomography (OCT) have made it possible to quantify, in vivo, RNFL atrophy as a structural marker of axonal injury in the afferent visual pathway. Studies have shown that OCT-measured RNFL values are reduced in multiple sclerosis (MS) patients with and without a history of optic neuritis (ON), although RNFL atrophy

 

tends to be greater in ON-affected, than in non-affected eyes. Patients with progressive MS sub-types have reduced RNFL values as compared to patients with relapsing remitting MS.3

It is crucial to have non-invasive surrogate markers for observing neurodegeneration and axonal loss, to monitor effect of disease modifying and possible neuroprotective drugs. Ideally, it would be a great advantage to have a structural marker, which is non-invasive, reliable, reproducible, and correlates with other measures of visual system function. There are no reliable imaging or electro-diagnostic techniques (MRI or visual evoked potential) that can be used to quantify the effects of regenerative strategies, primarily because these techniques do not specifically distinguish between demyelinating effects from axonal damage. OCT can quantify RNFL loss in the anterior visual pathways. As a measure, this technique and other retinal imaging assessments are not substitutes for clinical, radiographic, or neuro-physiological methods, but instead can be seen as a complement to these measures.4

The Fischer study revealed a conspicuous outcome, which was the association between RNFL thickness measurements and multiple sclerosis associated disability, as documented by the expanded disability status scale score and the multiple sclerosis functional composite. RNFL thickness decreased with increasing expanded disability status scores and indicating greater degrees of axonal loss in the anterior visual pathways of patients with substantial neurological impairment. These studies provide some data to suggest that OCT is an excellent and reproducible technique for the quantification of axonal loss in optic neuritis and multiple sclerosis.5

Sicotti et al. 20081, showed early hippocampal volume loss in RRMS that is disproportionate to global brain atrophy, hippocampal atrophy worsens in SPMS.

 

Aim of Work

The aim of the study was to define optical coherence tomography (OCT) as a noninvasive tool used for measuring tissue at micrometer resolution as a marker of neurodegeneration and axonal loss and its possible correlation with hippocampal volume.

              

PATIENTS AND METHODS

 

This is a cross sectional study carried out on 30 MS patients and 20 age and sex matched normal healthy control subjects. They were recruited in the period between June, 2011 to January, 2013, from the Cairo university hospitals (Kasr Al-Ainy); Neurology outpatient clinic and Neurology department MS unit. 

Inclusion criteria: 30 MS patients, clinically definite according to revised McDonald criteria (2010), both relapsing remitting and secondary progressive. MS patients aged 20-50 years. Twenty control subjects matched with patients as regards age, gender and education. Exclusion criteria: MS patients were excluded if they had fatigue or depression assessed using the fatigue severity scale (<36) and DSM- IV-TR- criteria for major depressive episode and major depressive disorder. Patients with Devic's disease (neuromyelitis optica), vasculitis, inflammatory diseases of the nervous system and patients with other associated CNS diseases, medical illnesses; as endocrinal, metabolic or psychiatric troubles that could affect cognitive functions of the patient especially depression were excluded.

All the study participants were subjected to thorough clinical assessment, EDSS, routine labs.         

Hippocampal volumetry was done as following; MRI acquisition and analysis; aall subjects received an MR scan, obtained by using a 1.5 Tesla Philips Gyroscan machine (Philips Medical Systems, Best, the Netherlands) in diagnostic radiology department, Cairo university hospitals. Anatomic basis for hippocampal volume measurement by MRI was obtained from Watson et al. 1992.6The MRI protocol for hippocampal volumetry was done according to Maller et al. 2007.7 The total time of each subject's scanning session was approximately 20 min. Volumetric measurements; were done manually. MRI images were processed on the console of the MRI machine.  The system allows manual contouring in 2-D and 3-D, and several other functions, including manual editing of existing regions of interest. Each hippocampus was measured in approximately 20 slices and volume was measured directly for each slice. The volume of the 20 slices for each hippocampus were summed for total volume measurement.  In this study we used a manual method for hippocampal volumetry. Although the automated methods were successful in detecting hippocampal atrophy. Results indicate that manual hippocampal volumetry is still the gold standard, while automated volumetric methods need to be improved.8 OCT; The RNFLT was assessed in all patients in the Ophthalmic Diagnostic and Laser Unit (DLU) in Cairo University hospitals using combined imaging system; OCT/SLO (Ophthalmic Technologies Inc. (OTI), Toronto, Ontario, Canada). Circular OCT Scan with a diameter of 3.4mm was placed around the optic nerve while the location was observed on the confocal SLO image (topographic map of the optic nerve area using 128 longitudinal scans over a five mm area) to ensure proper positioning in relation to the optic nerve. The RNFL thickness map was displayed along with its ratio to normative RNFL thickness. The global and four-quadrant average RNFL thickness data were collected as in Figure (1).

 

Statistical Methods

SPSS computer program (version 15) was used for data analysis. Data were expressed as mean± standard deviation (SD) or percentage (%). Comparison between the numerical data of three groups was performed using ANOVA test followed by Post Hoc multiple comparisons Duncan. T-Test was used for comparison of parametric data between two groups. Pearson’s correlation coefficient was used to determine significant correlations between the different qualitative variables. P value of 0.05 or less was considered significant.

 

RESULTS

 

This study included 30 multiple sclerosis patients and 20 normal healthy control subjects age and sex matched. They were recruited in the period between June, 2011 to January, 2013 from the Cairo university hospitals (Kasr Al-Ainy); Neurology outpatient clinic and Neurology department MS unit, which were further divided into 25 RRMS and 5 SPMS. MS patients mean age was 31.43 ± 8.71 years, the RRMS patients had a mean age of 30.16±8.72 years while the SPMS patients had a mean of 37.8±5.81 years, while the mean age of control subjects was 27.5±6.1 years. Multiple sclerosis patients were twenty one females and 9 males, RRMS patients were 8 males and 17 females, SPMS patients were 4 females and 1 male, whereas control patients were 15 females and 5 males.

Duration of illness in MS patients ranged from 2 to 20 years, with a mean of 8.13±4.07 years. Duration of illness in MS subtypes was 7.52±3.61 in RRMS and 11.2±5.26 in SPMS. Clinical data in RRMS patients was as follows; sensory abnormalities and positive L’Hermitte symptom in 6 patients, hemiparesis in 5 patients, optic neuritis in 11 patients, urinary precipitancy in 2 patients, while clinical data in SPMS patients was as follows; cerebellar-pyramidal syndrome in 2 patients, sensory abnormalities in 2 patients, optic neuritis in 1 patient and urinary precipitancy in 1 patient.  MS patients had an EDSS that ranged between 2 and 7 with a mean of 4.28± 1.31. Mean EDSS in MS subtypes was 3.86±0.91 in RRMS and 6.4±0.89 in SPMS as in table (1).

Twelve MS patients had optic neuritis throughout their illness. Nine patients had optic neuritis attacks involving both optic nerves. Two patients had optic neuritis affecting the right optic nerve only. One patient had optic neuritis affecting the left optic nerve only. Eighteen MS patients did not experience optic neuritis by the time this study was carried out. MS patients were further subdivided into patients with optic neuritis and patients without optic neuritis; patients without optic neuritis 14 were RRMS and 4 were SPMS, while patients with optic neuritis 11 were RRMS and 1 was SPMS.

Volume of the right hippocampus ranged from 2.09 to 4.2 cm3 with a mean of 2.89±0.52 while volume of the left hippocampus ranged from 1.91 to 4.1 with a mean of 2.9±0.58 in MS patients. There was no significant difference between mean hippocampal volumes of both RRMS and SPMS patients as in Table (2).

A statistically very highly significant difference was found between all MS patients, MS subtypes and controls as regards the RNFLT of superior and inferior quadrants on both the right and left sides (p<0.001), being very highly significantly lower mean RNFLT in all MS and subtypes than in controls as regards superior and inferior quadrants on both sides, whereas mean of RNFLT in the right inferior quadrant was very highly significantly lower in SPMS than in both all MS patients and RRMS, in addition there was a very highly significantly lower mean RNFLT in left superior quadrant in SPMS than in RRMS. Whereas mean of RNFLT in left temporal quadrant was highly significantly lower in all MS and RRMS patients than in control as in Table (2).

Mean hippocampal volumes on both sides were very highly significantly lower in all MS and MS subtype patients than in control as in Table (2).

MS patients who had optic neuritis, showed evident reduction in mean RNFLT compared to MS patients without optic neuritis. This reduction in RNFLT occurred in all quadrants of the optic disc, on both sides except for left superior and left nasal quadrant, but was not statistically significantly different as in Table (3).

No significant correlation was found between mean volumes of both the right and left hippocampi and mean EDSS.

A statistically significant positive correlation was found between mean volume of the right hippocampus and mean RNFLT of the left nasal quadrant, (p = 0.04). A statistically highly significant positive correlation was found between mean volume of the left hippocampus and mean RNFLT of the left inferior and left nasal quadrants, and a significant positive correlation with that of the left superior quadrant as in Table (4).


 

Table 1. Descriptive results of MS patients and controls.

 

 

Multiple Sclerosis Patients

RRMS

SPMS

Control

Mean

SD

Mean

SD

Mean

SD

Mean

SD

Age

31.43

8.71

30.16

8.72

37.80

5.81

27.50

6.10

duration of illness years

8.13

4.07

7.52

3.61

11.20

5.26

--

--

EDSS

4.28

1.31

3.86

0.91

6.40

0.89

--

--

Right Superior 

102.80

27.49

104.36

29.00

95.00

18.55

152.35

31.06

Right Inferior

108.13

30.02

113.00

29.84

83.80

17.49

150.15

29.47

Right Nasal

75.50

20.58

74.52

22.19

80.40

8.96

71.35

4.07

Right Temporal

61.67

20.27

61.24

21.90

63.80

9.68

73.60

8.72

Left superior

109.60

25.39

113.52

25.10

90.00

17.89

144.85

28.30

Left inferior

103.83

25.93

107.36

26.78

86.20

10.33

141.00

30.87

Left nasal

75.27

17.69

74.56

17.18

78.80

21.88

70.10

4.93

Left temporal

60.27

15.18

59.08

15.92

66.20

9.83

73.35

7.89

Right Hippocampus

2.89

0.52

2.89

0.52

2.88

0.55

3.48

0.43

Left Hippocampus

2.90

0.58

2.90

0.60

2.9080

0.54

3.51

0.34

Table 2. Comparison between all MS patients, different types of MS and control as regards mean RNFLT and hippocampal volume.

                                                                              

 

MS

RRMS

SPMS

Control

F-value

P-value

Mean

SD

Mean

SD

Mean

SD

Mean

SD

Right Superior

102.80

27.49

104.36

29.00

95.00

18.55

152.35

31.06

15.24

<0.001*

Right Inferior

108.13

30.02

113.00

29.84

83.80

17.49

150.15

29.47

11.665

<0.001*

Right Nasal

75.50

20.58

74.52

22.19

80.40

8.96

71.35

4.07

0.41

0.75

Right Temporal

61.67

20.27

61.24

21.90

63.80

9.68

73.60

8.72

2.17

0.09

Left superior

109.60

25.39

113.52

25.10

90.00

17.89

144.85

28.30

10.54

<0.001*

Left inferior

103.83

25.93

107.36

26.78

86.20

10.33

141.00

30.87

10.36

<0.001*

Left nasal

75.27

17.69

74.56

17.18

78.80

21.88

70.10

4.93

0.65

0.59

Left temporal

60.27

15.18

59.08

15.92

66.20

9.83

73.35

7.89

4.91

0.004*

Right Hippocampus

2.89

0.52

2.89

0.52

2.88

0.55

3.48

0.43

6.951

<0.001*

Left Hippocampus

2.90

0.58

2.90

0.60

2.9080

0.54

3.51

0.34

6.309

0.001*

*Significant at p<0.01

 

Table 3. Mean RNFLT in non-optic neuritis and optic neuritis groups in different MS subtypes.

                                             

 

Non-optic neuritis

Optic neuritis

T-value

P-value

Mean

SD

Mean

SD

Right Superior 

105.94

28.26

98.08

26.80

0.76

0.45

Right Inferior

113.39

33.05

100.25

23.99

1.18

0.25

Right Nasal

80.94

20.92

67.33

17.86

1.85

0.08

Right Temporal

63.67

18.56

58.67

23.11

0.66

0.52

Left superior

108.17

24.57

111.75

27.56

-0.37

0.71

Left inferior

102.78

24.62

105.42

28.84

-0.27

0.79

Left nasal

72.94

19.23

78.75

15.21

-0.88

0.39

Left temporal

62.11

14.69

57.50

16.12

0.81

0.43

 

Table 4. Correlation between RNFLT and duration of illness, EDSS and hippocampal volume.

 

 

 

Duration of illness

EDSS

Right hippocampus

Left hippocampus

Right superior

r

0.13

-.031

-.013

0.06

p

0.50

.869

0.95

0.74

Right inferior

r

-0.23

-0.39

-.062

-0.02

p

0.22

0.03*

0.74

0.91

 Right nasal

r

-0.18

-0.16

-0.22

-0.34

p

0.34

0.39

0.25

0.07

Right temporal

r

0.02

0.07

0.19

0.29

p

0.93

0.73

0.32

0.12

Left Superior

r

0.001

-0.19

0.29

0.45

p

0.99

0.31

0.11

0.013*

Left inferior

r

0.08

-0.18

0.30

0.49

p

0.69

0.33

0.11

0.005**

Left nasal

r

0.16

0.14

0.39

0.55

p

0.39

0.48

0.04*

0.002**

Left temporal

r

0.23

0.29

0.09

0.22

p

0.22

0.12

0.64

0.24

*Significant at p<0.05 **Significant at p<0.01

 

 

Figure 1. OCT of MS patient showing borderline RNFL thickness of the superior quadrant.

 

 


DISCUSSION

 

The hippocampus is an archi-cortical structure that is critical for memory functions and is especially sensitive to multiple insults including inflammation.9 A statistically very highly significant difference was found between MS patients and controls as regards the volume of the right and left hippocampi. The mean hippocampal volume in MS patients was markedly reduced compared to controls. Our results showed no significant difference between the hippocampal volumes reduction in RRMS and SPMS. Siccote et al 20081, used high-resolution MR imaging at 3 Tesla to measure segmental hippocampal volumes in RRMS and SPMS patients and controls. They found that both groups of MS patients had hippocampal atrophy compared to controls.6

In this study, failure to demonstrate a significant difference in hippocampal volume loss between the RRMS and SPMS patients may be attributed to; small difference in the mean EDSS between both groups (RRMS patients mean EDSS was almost 4 and SPMS patients mean EDSS was almost 6), in addition to the small sample size of SPMS patients.

Multiple sclerosis is a progressive disease in which subclinical RNFL thinning may also occur, even in patients who have not been clinically diagnosed with optic neuritis. Our study showed evident RNFL thinning in MS patients who never experienced optic neuritis similar to Khanifar et al 201010, who demonstrated progressive peripapillary RNFL thinning in multiple sclerosis patients who did not manifest with overt optic neuritis, especially with increased duration of disease of more than five years. On the other hand our study failed to prove any correlation between RNFLT and duration of illness similar to Henderson et al. 200811, who did not consistently demonstrate such a relationship.  However this difference may be explained by the fact that khanifar et al 201010, used high resolution spectral domain OCT, where the Henderson et al 200811 and our study used a time domain OCT.

Expanding the value of RNFLT and its results in predicting prognosis of MS, Saidha et al. 201112, identified a unique subset of patients with multiple sclerosis with primary retinal pathology "macular thinning predominant phenotype" in whom there appears to be disproportionate thinning of the inner and outer nuclear retinal layers. Hence multiple sclerosis may primarily target the retina, independent of processes occurring in the optic nerves, constitutes a novel conceptualization further broadening of the heterogeneity of this inflammatory demyelinating white and grey matter disorder of the central nervous system.  Further, these patients appear to have a predilection toward a more accelerated rate of disability progression, signifying a potential relationship between this pathological profile and the clinical course of multiple sclerosis.

Our study showed that MS patients with and without optic neuritis showed marked reduction in RNFLT compared to control subjects. MS patients who had optic neuritis, showed evident reduction in mean RNFLT compared to MS patients without optic neuritis. These findings are consistent with Parisi et al 199913, Fischer et al 20065 and Costello et al 200814 all using the Stratus TDOCT device, demonstrated a difference in RNFL thickness between eyes with and without optic neuritis.

To the best of our knowledge no available published study, ever addressed the issue of possible correlation between RNFL and hippocampal volume in MS patients.  This study showed highly positive significant correlation between the mean hippocampal volumes in MS patients and RNFLT.

Eventually some studies used other markers for cerebral degeneration in MS and correlated them with RNFLT. Dorr et al. 201115, studied correlations between brain parenchymal fraction (BPF) on one hand and RNFLT. They concluded that in RRMS patients RNFLT reflect brain atrophy and are thus promising parameters to evaluate neuro-degeneration in MS. 

Gabilondo et al 201216, studied 55 RRMS patients and found that RNFLT correlated with visual cortex volume. They concluded that degeneration of retro-geniculate pathway correlated with retinal atrophy, supporting the presence of transynaptic degeneration as a contributor to retinal atrophy in MS. These studies and ours altogether conclude that RNFLT reflects any brain atrophy secondary to MS pathology.  

Our results showed a statistically highly significant positive correlation between mean volume of the hippocampi and mean RNFLT of the left optic disc. This may be attributed to the asymmetry of the RNFLT between the right and the left optic discs. Kurimoto et al 200017, studied the asymmetry of RNFLT in normal subjects. The mean RNFLT was significantly thicker in the right eyes than in the left eyes in the temporal quadrant.   Park et al 200518, found that the nasal and temporal RNFLTs were asymmetrical between the right and left eye in the quadrant and sector analysis. The RNFLT of the nasal and temporal quadrant was thicker in the right eye than the left eye. These asymmetries should be considered when retinal nerve fiber layer loss is evaluated during the course of a disease process.

In conclusion MS patients showed marked thinning in RNFLT and hippocampal atrophy than controls, in addition hippocampal atrophy showed a significant correlation with hippocampal atrophy, hence RNFLT can be used as a surrogate marker for neurodegeneration in MS.

Several limitations of this study have been noted; First the small sample size of the SPMS patients relative to the RRMS patients. Second the effect of use of different disease-modifying treatments in MS patients; this point was not approached and analyzed.  Third the OCT applied to patients in this study was time domain instead of spectral domain OCT.

 

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.                       

 

[Disclosure: Authors report no conflict of interest]

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الملخص العربي

 

سمك طبقة الألياف العصبية بالشبكية بالتصوير المقطعي للتماسك البصري و الضمور الحصيني

في مرض التصلب المتعدد

 

الخلفية: إن المادة الرمادية بالمخ والتي تشتمل علي الأنوية العميقة و القشرة الدماغية تتأثر كثيرا وبشكل مبكر في سياق مرض التصلب المتعدد. ولذلك فإن الحاجة إلي وجود محدد بديل لعملية التنكس العصبي لا تزال قائمة بشرط أن يكون هذا المحدد موثوقا به و غير مكلف وسهل التقييم. الهدف من الدراسة : نهدف من هذه الدراسة إلي الكشف عن نقص حجم الحصين في مرضي التصلب المتعدد . ونهدف كذلك إلي تقييم التصوير المقطعي للتماسك البصري OCT كمحدد لقياس التنكس العصبي .

الأساليب و الوسائل : اشتملت الدراسة علي 30 مريض من مرضي التصلب المتعدد من نوعي التصلب المتعدد  المنتكس المتحول و التصلب المتعدد الثانوي التدريجي  و 20 شخص طبيعي معافي كضوابط للدراسة متطابقين في السن والجنس والتعليم. وقد خضع أفراد الدراسة جميعهم المرضي والضوابط  لكل ما يلي : فحص سريري كامل للجهاز العصبي و مقياس حالة الاعاقة الموسع EDSS وذلك بالنسبة للمرضي دون الأصحاء  و قياس حجم الحصين بالمخ وذلك بالطريقة اليدوية بجهاز الرنين المغناطيسي بمستشفيات جامعة القاهرة 1.5 تسله فيليبس جيروسكان. و خضع أفراد الدراسة كذلك  لقياس سمك طبقة الألياف العصبية بالشبكية عن طريق التصوير المقطعي للتماسك البصري بوحدة الليزر بالدور التاسع بمستشفيات جامعة القاهرة.

النتائج: متوسط حجم الحصين بمرضي التصلب المتعدد بمجموعتيه التصلب المتعدد المنتكس المتحول و التصلب المتعدد الثانوي التدريجي ابدي انخفاضا ملحوظا مقارنة بالمجموعة الضابطة.

كذلك أظهر مرضي التصلب المتناثر بمجموعتيه التصلب المتعدد المنتكس المتحول والتصلب المتعدد الثانوي التدريجي انخفاضا واضحا في سمك طبقة الألياف العصبية بالشبكية في الأرباع الأعلي والادني بالقرص العصبي الأيمن والأيسرو الربع الأنفي الأيسروالربع الصدغي الأيمن مقارنة بالمجموعة الضابطة.

أظهر مرضي التصلب المتعدد بمجموعتيه التصلب المتعدد المنتكس المتحول و التصلب المتعدد الثانوي التدريجي المصابين بالتهاب في العصب البصري نقص في سمك طبقة الألياف العصبية بالشبكية مقارنة بمرضي التصلب المتعدد الذين لم يصابوا بالتهاب في العصب البصري و لكن بدون وجود دلالة احصائية.

الخلاصة: أظهر مرضي التصلب المتعدد بنوعيه التصلب المتعدد  المنتكس المتحول و التصلب المتعدد الثانوي التدريجي نقصا ملحوظا ذو دلالة احصائية واضحة في متوسط حجم الحصين وكذلك متوسط سمك طبقة الالياف العصبية بالشبكية مقارنة المجموعة الضابطة. وقد أظهر نقص سمك طبقة الألياف العصبية بالشبكية ارتباطا ايجابيا ذي دلالة احصائية واضحة بالضمور الحصيني مما يثبت دعما لنتائج الدراسات الأخري بأن التصوير المقطعي للتماسك البصري يمكن استخدامه كمؤشر بديل لقياس التنكس العصبي 



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