|Year : 2017 | Volume
| Issue : 1 | Page : 32-36
Role of spectral domain optical coherence tomography in assessment of macular morphological abnormalities in patients with retinitis pigmentosa
Walid Ibrahim, Zeiad Eldaly
Department of Ophthalmology, Assiut University Hospital, Assiut, Egypt
|Date of Submission||30-Jul-2016|
|Date of Acceptance||10-Sep-2016|
|Date of Web Publication||6-Mar-2017|
Department of Ophthalmology, Assiut University Hospital, Assiut, 71516
Source of Support: None, Conflict of Interest: None
Objectives To evaluate macular morphological changes in patients with retinitis pigmentosa (RP) by spectral domain optical coherence tomography (SD-OCT) and to assess their correlation with visual acuity.
Setting and design A prospective observational comparative study was conducted in Tiba Eye Center (T. E. C.), Assiut, Egypt, from August 2013 to July 2014.
Patients and methods A total of 13 consecutive patients experiencing RP (26 eyes) were recruited. An age-matched control group of 13 healthy volunteers was also recruited. All patients and volunteers underwent SD-OCT evaluation by SPECTRALIS OCT.
Results Overall, 26 (13 patients) eyes in the RP group and 26 (13 volunteers) eyes in the control group were included. In RP group, the mean central macular thickness (CMT) at 1 mm was 180.6±22.18 µm, whereas the mean best-corrected visual acuity (BCVA) was 0.11±0.08. In the control group, the mean CMT was 222.6±10.9 µm, whereas the mean BCVA was 0.9±0.11. By SD-OCT, foveal atrophy was found in 14 (53.8%) eyes, cystoid macular edema in five (19.2%) eyes, epiretinal membrane in six (23.1%) eyes, and lamellar macular hole in one (3.8%) eye in patients with RP. In nine (34.6%) eyes, there was interruption of the inner segment-outer segment junction and the external limiting membrane in the subfoveal region. There was a statistically significant positive correlation between CMT and BCVA among the RP group (r=0.813, P=0.000). BCVA categories among RP group were significantly associated with foveal atrophy (P=0.003) and inner segment-outer segment junction interruption (P=0.000).
Conclusion SD-OCT is an important tool in the evaluation of macular morphological changes in patients with RP.
Keywords: cystic spaces, foveal atrophy, photoreceptor dystrophy, retinal degeneration, retinal imaging
|How to cite this article:|
Ibrahim W, Eldaly Z. Role of spectral domain optical coherence tomography in assessment of macular morphological abnormalities in patients with retinitis pigmentosa. Delta J Ophthalmol 2017;18:32-6
|How to cite this URL:|
Ibrahim W, Eldaly Z. Role of spectral domain optical coherence tomography in assessment of macular morphological abnormalities in patients with retinitis pigmentosa. Delta J Ophthalmol [serial online] 2017 [cited 2017 Dec 12];18:32-6. Available from: http://www.djo.eg.net/text.asp?2017/18/1/32/201620
| Introduction|| |
Retinitis pigmentosa (RP) is a genetically heterogeneous disorder with an incidence of ∼1 in 3500 individuals. Affected individuals experience progressive degeneration of the photoreceptors, eventually resulting in night blindness and severe visual impairment. The disease is characterized by midperipheral pigmentary deposits and rod-cone dystrophy manifested as impaired rod-driven scotopic electroretinogram (ERG) response than cone-mediated responses. The initial degenerative changes occur in the photoreceptors, especially in the midperipheral retina where rod photoreceptor density is maximal. Cone cell death is probably consequent on rod photoreceptor death ,.
As the disease progresses, the macula may or may not become involved. The structure of the macula can be assessed objectively using optical coherence tomography (OCT). As early as 2003, adding ERG and time-domain OCT (TD-OCT) to clinical examinations was proposed for a more refined evaluation of visual function in patients with RP ,.
The limited histopathological literature on RP describes photoreceptor damage with the earliest histologic change in all forms of RP being shortening of the rod outer segments, in keeping with diminished rod outer segment renewal. Consequently, cellular degeneration proceeds with predominant involvement of the photoreceptors ,,,,.
Evaluation of the early pathologic events was difficult before the advent of OCT technology. Spectral domain (SD)-OCT provides in vivo cross-sectional evaluation of the retinal ultrastructure. There are many computer-based algorithms nowadays to provide OCT-based quantitative information about the retinal architecture ,
The objective of the current study was to evaluate macular morphological changes in patients with RP by SD-OCT and to assess their correlation with visual acuity.
| Patients and methods|| |
A prospective observational comparative study was conducted in T. E. C. (private practice), Assiut, Egypt, from August 2013 till July 2014. The study included 26 eyes of 13 (six males and seven females) patients experiencing RP. An age-matched control group of volunteers was also recruited. Approval of the ethical committee of the faculty of Medicine, Assiut University was obtained. All the study procedures were under the tenets of the Declaration of Helsinki. All patients and volunteers underwent detailed history taking and complete ophthalmic examination [including best-corrected visual acuity (BCVA) by Landolt C chart, Goldmann applanation tonometry (Haag-Streit, Germany), slit lamp biomicroscopy, and a detailed fundus examination]. In the RP group, the rod-cone dystrophy characterizing RP was documented by full-field ERG. Full-field ERG was conducted under international standards and guidelines of the International Society of Clinical Electrophysiology of Vision . Patients with diabetes mellitus, ocular inflammatory diseases, primary retinal vascular diseases, previous ocular trauma, or previous intraocular surgery were excluded. Patients younger than 18 years or those with RP with systemic associations were also excluded.
In both RP and control groups, OCT was done by SPECTRALIS SD-OCT (Heidelberg Engineering GmbH, Heidelberg, Germany). Using a line scan averaged to 100 frames, macular morphological changes were evaluated. In macular thickness map evaluation, a 30×30° rectangle encompassing the macula was obtained, averaged to 40 frames and included 31 horizontal line scans. OCT images were converted to gray scale for better contrast of the individual layers. Meticulous evaluation of vitreomacular interface, outer retinal layers, inner segment-outer segment (IS-OS) junction, and retinal pigment epithelium (RPE) was carried out to reveal subtle changes by two independent observers (W.I. and Z.E.). In the control group, SD-OCT was done to measure the central macular thickness (CMT) at 1-mm circle.
Foveal atrophy was defined as CMT at 1-mm Early Treatment Diabetic Retinopathy Study circle less than or equal to180 µm. Cystoid macular edema (CME) was defined by the presence of low reflective intra-retinal cystic spaces in the foveal region. Epiretinal membrane (ERM) was defined as a highly reflective linear structure overlying the inner retinal surface and the internal limiting membrane and was distinguished from the posterior hyaloid by differential reflectivity and attachment. Lamellar macular hole was defined by partial loss of inner retinal layers with undermined edges and residual outer retinal tissue in the presence or absence of ERM. For the sake of correlation between different macular morphological abnormalities, the BCVA in the RP group was categorized into three categories: category 1 included BCVA equal to or better than 0.25, category 2 included BCVA equal to or worse than 0.2 and better than or equal to 0.1, and category 3 included BCVA worse than 0.1.
Clinical information including clinical findings and SD-OCT findings as entered into the database. A format was devised using Microsoft Excel (Microsoft Corp., Redmond, Washington, USA) to collect and analyze the clinical information from the patients’ records. The statistical analysis was done by SPSS software, version 16.0 (SPSS Inc., Chicago, Illinois, USA). Descriptive statistics were evaluated to compare patients’ characteristics between control and RP groups. Student’s t-test was used to compare means among groups. Pearson’s correlation coefficient was used for correlation between BCVA and CMT. χ2-Test was used to evaluate the correlation between BCVA categories and the different macular morphological abnormalities. P less than 0.05 was considered significant.
| Results|| |
Among the RP group, there were seven females and six males. The mean age of participants at the time of evaluation was 33.4±9.2 (range: 19–54) years. The mean CMT at 1 mm was 180.6±22.18 µm, whereas mean BCVA was 0.11±0.08 (range: 0.01–0.3).
Among the control group, there were six females and seven males. The mean age of volunteers at the time of evaluation was 29.4±8.1 (range: 20–41) years. The mean CMT at 1 mm was 222.6±10.9 µm, whereas the mean BCVA was 0.9±0.11 (range: 0.7–1.0).
According to prespecified categories of BCVA, five (19.2%) eyes were classified into category 1 (BCVA≥0.25), 12 (46.2%) eyes into category 2 (BCVA ≤0.2 and ≥0.1), and nine (34.6%) eyes into category 3 (BCVA<0.1).
There was a statistically significant difference in CMT among the RP and the control groups (P<0.001). Foveal atrophy was found in 14 (53.8%) eyes ([Figure 1]). SD-OCT identified CME in five (19.2%) eyes ([Figure 2]). ERM was detected in six (23.1%) eyes ([Figure 3]). Lamellar macular hole was detected in one (3.8%) eyes ([Figure 4]). In nine (34.6%) eyes, there was interruption of the IS-OS junction and the external limiting membrane in the subfoveal region.
|Figure 1 RP with foveal atrophy. SD-OCT shows exaggerated foveal depression, diffuse foveal thinning, and disruption of IS-OS junction. IS-OS, inner segment-outer segment; RP, retinitis pigmentosa; SD-OCT, spectral domain optical coherence tomography.|
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|Figure 2 RP with cystoid macular edema (CME). A 35-year-old male patient with bilateral CME. Multiple low reflective cystic spaces could be detected by SD-OCT. Fundus autofluorescence also revealed faint hyperautofluorescent cysts obliterating central foveal hypoautofluorescence. RP, retinitis pigmentosa; SD-OCT, spectral domain optical coherence tomography.|
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|Figure 3 RP with both CME and ERM. A 29-year-old female patient with multiple low reflective cystic spaces (CME) and a highly reflective ERM and irregular macular contour. CME, cystoid macular edema; ERM, epiretinal membrane; RP, retinitis pigmentosa.|
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BCVA categories among the RP group were significantly associated with the presence of foveal atrophy (Pearson’s χ2-test, P=0.003) and IS-OS junction interruption (Pearson’s χ2-test, P=0.000). On the contrary, ERM, CME, and lamellar macular hole did not show any significant association with any BCVA categories (Pearson’s χ2-test, P=0.839, 0.583 and 0.492, respectively) ([Table 1]).There was a statistically significant strong correlation between BCVA and CMT at 1 mm (Pearson’s correlation coefficient=0.784; P=0.000).
|Table 1 Association between SD-OCT findings and different categories of BCVA among patients with retinitis pigmentosa|
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| Discussion|| |
Histopathologic studies have been used to understand the anatomic changes of the retina and RPE that occur initially and over time in RP and related diseases ,. SD-OCT allows the visualization and measurement of the RPE and photoreceptors in great detail, permitting in vivo assessment of small anatomic abnormalities in diseases known to specifically affect these layers ,. Witkin et al.  described that the macula in patients with RP showed macular volume reduction and decreased central foveal thickness with enlargement of the central foveal depression. Ultrahigh resolution OCT demonstrated macular photoreceptor thinning in all patients with RP . Extrafoveal photoreceptor loss was also visible in ultrahigh resolution OCT images in all patients .
Foveal outer segment/pigment epithelium thickness was statistically thinner in patients with RP and related diseases than in normal eyes and showed correlation with logMAR visual acuity. Foveal outer segment/pigment epithelium thickness appears to be a probable predictor of visual acuity in RP. In the current study, there was a statistically significant correlation between CMT and BCVA (Snellen chart); however, Witkin et al.  found a fair nonsignificant correlation between CMT and BCVA (logMAR).
Prevalence of CME in patients with RP is variable. Sandberg et al.  found that 15% of patients with RP included in their study had CME. Triolo et al.  detected CME in 12.5% of studied eyes. Hajali et al.  found variable prevalence of CME according to the mode of inheritance of RP. The prevalence of CME in at least one eye for autosomal dominant patients with RP was 52%, for autosomal recessive 39%, isolated RP 39%, Usher II 35%, and none in the x-linked recessive patients with RP . Subfoveal cystic spaces were found in 19.2% of eyes included in the present study.
Triolo et al.  detected ERM in 27.3% of studied eyes. By SD-OCT, ERM was detected in 23.1% of eyes in the RP group, in the present study. In addition, there was a single case of lamellar macular hole found in the RP group. Macular hole was found in 4.5% of eyes in the current study .
No choroidal neovascular membrane (CNVM) was detected in any patient with RP. On the contrary, Malik et al.  and Battaglia et al.  detected CNVM in patients with RP treated successfully with intravitreal bevacizumab injection. Triolo et al.  found CNVM in 1.7% of patients with RP.
By analyzing the association between BCVA categories in the RP group and macular morphological abnormalities, foveal atrophy, and interruption of IS-OS junction in the subfoveal region seem to be the macular pathology that could jeopardize patient’s visual acuity greater than other macular abnormalities. Kim et al.  concluded also that the IS-OS disruption correlates with a worse visual acuity. Aizawa et al.  concluded that the absence of an IS-OS junction line may reflect a foveal dysfunction in patients with RP and the more affection of IS-OS junction line is associated with worse visual acuity.
Limitations of the current study were a small number of patients and categorization of RP according to mode of inheritance. Further studies are needed to confirm the correlation between macular thickness, macular morphological changes, and patient’s visual acuity.
| Conclusion|| |
OCT is a very useful tool to define the pathological changes in cases of RP. Macular thickness reduction was noticed with other inner and outer retinal changes. Not all macular morphological changes could jeopardize patient’s visual acuity. Foveal atrophy and IS-OS junction disruption carry the most guarded prognosis.
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Conflicts of interest
There are no conflicts of interest.
| References|| |
Berson EL. Retinitis pigmentosa. Invest Ophthalmol Vis Sci 1993; 34:1659–1676.
Pagon RA. Retinitis pigmentosa. Surv Ophthalmol 1988; 33:137–177.
Hirakawa H, Iijima H, Gohdo T, Tsukahara S. Optical coherence tomography of cystoid macular edema associated with retinitis pigmentosa. Am J Ophthalmol 1999; 128:185–191.
Hamada S, Yoshida K, Chihara E. Optical coherence tomography images of retinitis pigmentosa. Ophthalmic Surg Lasers 2000; 31:253–256.
Van Soest S, Westerveld A, de Jong PT, Bleeker-Wagemakers EM, Bergen AA. Retinitis pigmentosa: defined from a molecular point of view. Surv Ophthalmol 1999; 43:321–334.
Milam AH, Li ZY, Fariss RN. Histopathology of human retina in retinitis pigmentosa. Prog Retin Eye Res 1998; 17:175–205.
Stone JL, Barlow WE, Humayun MS, de Juan E Jr, Milam AH. Morphometric analysis of macular photoreceptors and ganglion cells in retinas with retinitis pigmentosa. Arch Ophthalmol 1992; 110:1634–1639.
Li ZY, Possin DE, Milam AH. Histopathology of bone spicule pigmentation in retinitis pigmentosa. Ophthalmology 1995; 102:805–816.
Rodrigues MM, Wiggert B, Hackett J, Lee L, Fletcher RT, Chader GJ. Dominantly inherited retinitis pigmentosa. Ultrastructure and biochemical analysis. Ophthalmology 1985; 92:1165–1172.
Apushkin MA, Fishman GA, Janowicz MJ. Monitoring cystoid macular edema by optical coherence tomography in patients with retinitis pigmentosa. Ophthalmology 2004; 11:1899–1904.
Catier A, Tadayoni R, Paques M, Erginay A, Haouchine B, Gaudric A et al.
Characterization Of macular edema from various etiologies by optical coherence tomography. Am J Ophthalmol 2005; 140:200–206.
McCulloch DL, Marmor MF, Brigell MG, Hamilton R, Holder GE, Tzekov R et al.
ISCEV standard for full-field clinical electroretinography (2015 update). Doc Ophthalmol 2015; 130:1–12.
Witkin AJ, Ko TH, Fujimoto JG, Chan A, Drexler W, Schuman JS et al.
Ultra-high resolution optical coherence tomography assessment of photoreceptors in retinitis pigmentosa and related diseases. Am J Ophthalmol 2006; 142:945–952.
Sandberg MA, Brockhurst RJ, Gaudio AR, Berson EL. The association between visual acuity and central retinal thickness in retinitis pigmentosa. Invst Ophthalmol Vis Sci 2005; 46:3349–3354.
Triolo G, Pierro L, Parodi MB, De Benedetto U, Gagliardi M, Manitto MP et al.
Spectral domain optical coherence tomography findings in patients with retinitis pigmentosa. Ophthalmic Res 2013; 50:160–164.
Hajali M, Fishman GA, Anderson RJ. The prevalence of cystoid macular oedema in retinitis pigmentosa patients determined by optical coherence tomography. Br J Ophthalmol 2008; 92:1065–1068.
Malik A, Sood S, Narang S. Successful treatment of choroidal neovascular membrane in retinitis pigmentosa with intravitreal bevacizumab. Int Ophthalmol 2010; 30:425–428.
Battaglia Parodi M, De Benedetto U, Knutsson KA, Scotti F, Librando A et al.
Juxtafoveal choroidal neovascularization associated with retinitis pigmentosa treated with intravitreal bevacizumab. J Ocul Pharmacol Ther 2012; 28:202–204.
Kim YJ, Joe SG, Lee DH, Lee JY, Kim JG, Yoon YH. Correlations between spectral domain OCT measurements and visual acuity in cystoid macular edema associated with retinitis pigmentosa. Invest Ophthalmol Vis Sci 2013; 54:1303–1309.
Aizawa S, Mitamura Y, Baba T, Hagiwara A, Ogata K, Yamamoto S. Correlation between visual function and photoreceptor inner/outer segment junction in patients with retinitis pigmentosa. Eye 2009; 23:304–308.
[Figure 1], [Figure 2], [Figure 3], [Figure 4]