Jpn J Ophthalmol DOI 10.1007/s10384-014-0330-8
CLINICAL INVESTIGATION
Bilateral papillomacular retinoschisis and macular detachment accompanied by focal lamina cribrosa defect in glaucomatous eyes Tatsuya Yoshitake • Hideo Nakanishi • Yoshinao Setoguchi • Kenichi Kuroda • Kaori Amemiya • Misa Taniguchi • Atsushi Otani
Received: 14 December 2013 / Accepted: 28 April 2014 Ó Japanese Ophthalmological Society 2014
Abstract Purpose We report here a patient with bilateral papillomacular retinoschisis with an enlarged glaucomatous optic nerve head cup and a focal lamina cribrosa defect, the findings of our clinical investigations of this case, and the chosen treatment and outcome. Design This is an observational case report. Methods Clinical examinations were performed using simultaneous confocal scanning laser ophthalmoscopy and optical coherence tomography (OCT). The patient was treated by pars plana vitrectomy (PPV). Results The left eye had a macular detachment with a presumed acquired pit of the optic nerve, while the right eye did not have an obvious optic nerve pit. Enhanced depth imaging OCT showed focal lamina cribrosa defects in both eyes. PPV was performed on the left eye, which resulted in a re-attachment of the macula and improvement of the visual acuity. Conclusions Our findings suggest that the pathological changes were most likely due to focal lamina cribrosa defects in both glaucomatous eyes. This type of maculopathy can be successfully treated with PPV.
T. Yoshitake H. Nakanishi (&) Y. Setoguchi K. Kuroda K. Amemiya M. Taniguchi A. Otani Department of Ophthalmology, Japanese Red Cross Society Wakayama Medical Center, 4-20 Komatsubaradouri, Wakayama City, Wakayama 640-8558, Japan e-mail: [email protected] H. Nakanishi Department of Ophthalmology and Visual Sciences, Kyoto University Graduate School of Medicine, Kyoto, Japan
Keywords Focal lamina cribrosa defect Acquired pit of the optic nerve Enhanced depth imaging optical coherence tomography Retinoschisis Pars plana vitrectomy
Introduction Papillomacular retinoschisis with or without macular detachment is a relatively common complication of an optic nerve head pit, and papillomacular retinoschisis with a pit is called optic pit maculopathy or pit macular syndrome [1–6]. An optic nerve head pit is a congenital optic nerve anomaly [7, 8] which occurs in approximately 1 in 11,000 individuals [1]. Several studies have shown that although the maculopathy associated with an optic nerve head pit has a relatively poor visual prognosis [5, 9], it can be successfully treated by pars plana vitrectomy (PPV) [10, 11]. Retinoschisis and macular detachment without a visible optic nerve head pit has also been identified by optical coherence tomography (OCT), especially in eyes with glaucoma [12–22]. Glaucomatous eyes often have focal structural abnormalities of the optic nerve head, referred to as acquired pits of the optic nerve (APON) [23]. In early case reports, the treating physician assumed that these APON were correlated with the presence of macular retinoschisis or macular detachment [24, 25]. To date, the pathogenesis of papillomacular retinoschisis with or without macular detachment in glaucomatous eyes has not been completely determined. Early histological studies revealed the presence of lamina cribrosa defects in eyes with congenital optic pits [2] and in eyes with APON [23]. Enhanced depth imaging (EDI)-OCT was developed to improve the quality of the images of the deep posterior segment structures [26]. This imaging methods has been used
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in several studies to show focal lamina cribrosa defects in eyes with glaucoma. Some of the defects were associated with APON, but others were not [27–29]. We report here the case of a woman with bilateral papillomacular retinoschisis with enlarged glaucomatous optic nerve head cups. One of the eyes also had a macular detachment with a presumed APON, whereas the other eye did not have a visible optic nerve pit. Focal lamina cribrosa defects were detected by EDI-OCT in both eyes. PPV was performed on the left eye, which had the macular detachment, and the retina was re-attached with a subsequent improvement of visual acuity.
Methods This was a retrospective study of a case of bilateral papillomacular retinoschisis in a elderly Japanese woman. The study followed the tenets of the Declaration of Helsinki, and the ethics committee of our institute had ruled that approval was not required for such retrospective studies. The patient had a comprehensive ophthalmologic examination, including automatic objective determination of refractive errors, best-corrected visual acuity (BCVA) measurements, intraocular pressure (IOP) measurements with a Goldmann applanation tonometer, visual field testing by standard automated perimetry (Humphrey Visual Field Analyzer, the SAP, 24-2 Swedish Interactive Threshold Algorithm Standard strategy; Carl Zeiss Meditec, Dublin, CA), dilated indirect ophthalmoscopy, slitlamp biomicroscopy of the fundus, color fundus photography, confocal scanning laser ophthalmoscopy (cSLO), and spectral-domain OCT (SD-OCT; HRA-2; Heidelberg Engineering, Heidelberg, Germany). The B-scan SD-OCT images were obtained by averaging 25-50 images to reduce speckle noise. White-on-black images were used for all OCT evaluations, and the contrast and brightness were adjusted on each image to obtain the best image quality. For the EDI-OCT, a previously described method was used [26]. The evaluations of the cSLO and SD-OCT images were independently performed by two investigators (T.Y. and A.O.), who were blinded to all other ophthalmic information on each patient. When the two investigators disagreed, consensus was reached with further discussion.
Case report A 69-year-old Japanese woman who complained of blurred vision in her left eye was referred to our clinic in April 2011. At the initial visit, her decimal BCVA, determined on a Landolt chart, was 0.9 (20/22 Snellen units) in the right eye and 0.4 (20/50) in the left eye. Both eyes were
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phakic, and the refractive error (spherical equivalent) was ?1.5 D in the right eye and ?2.0 D in the left eye. The IOP was 11 mmHg in both eyes. Ophthalmoscopy, near-infrared reflectance (nIR), and red-free cSLO showed that she had an enlarged optic nerve head cup with annular peripapillary atrophy in both eyes (Fig. 1a-g). In her left eye, the nIR and red-free cSLO images showed focal hyporeflectivity of the optic disc border at the inferotemporal quadrant (Fig. 1f, g; arrows) and nerve fiber layer defects (Fig. 1g; arrowheads). The mean deviation (MD) values obtained by standard automated perimetry were ?0.73 dB in the right eye and -1.65 dB in the left eye (Fig. 1d, j). Examination of a horizontal OCT scan through the fovea showed outer retinoschisis and macular detachment in the left eye (Fig. 2a, b). Fluorescein angiography (FA) and additional EDI-OCT radial scans centered on the optic nerve head (12 B-scans at 15° intervals) were obtained for the left eye. FA showed late focal staining of the optic nerve head margin corresponding to the focal hyporeflectivity observed in the nIR cSLO images (Fig. 1h, i; arrows). No other leakage or staining was observed in either eye. Oblique EDI-OCT scans showed a thickening of the optic nerve head rim (Fig. 2e, h; arrows) corresponding to the focal hyporeflectivity in the nIR images (Fig. 2c, f; arrows). The EDIOCT images also showed a downward sloping of the peripheral anterior laminar surface toward its expected insertion point (Fig. 2e, h; yellow lines). Earlier studies had defined this localized alteration of the peripheral lamina cribrosa insertion as a type of focal lamina cribrosa defect and called it a ‘‘laminar disinsertion’’ [27–29]. One of the oblique EDI-OCT images also showed a small focal excavation of the optic nerve head in the left eye (Fig. 2h; arrowhead). An examination 1 month later showed no spontaneous improvements of the retinoschisis or macular detachment. In May 2011, we decided to treat the left eye with 25-gauge 3-port PPV combined with phacoemulsification and intraocular lens implantation. The patient was informed about the risks and benefits of the surgery, and her written informed consent was obtained before the surgery. The preoperative decimal BCVA in the left eye was 0.5 (20/40). A partial posterior vitreous detachment was present, and a thin premacular vitreous cortex was observed during the surgery. However, no unusual posterior vitreous strand connected to the optic nerve head was observed. Removal of the residual premacular vitreous cortex, internal limiting membrane peeling with indocyanine green staining, air-fluid exchange, and tamponade with nonexpansive sulfur hexafluoride (SF6) gas were performed. However, draining of the subretinal fluid and endolaser photocoagulation of the temporal margin of the optic nerve
Focal lamina cribrosa defect maculopathy
Fig. 1 Color fundus photographic, confocal scanning laser ophthalmoscopic (cSLO), and standard automated perimetric images of a patient with bilateral papillomacular retinoschisis and macular detachment accompanied by a focal lamina cribrosa defect at the initial visit. a–c Color fundus photographic (a), near-infrared (nIR) (b), and red-free (c) images of the right eye showing enlargement of the optic nerve head cup and annular peripapillary atrophy. d The mean deviation (MD) value of the Humphrey Visual Field Analyzer with the 24-2 Swedish interactive threshold algorithm standard program (d) was ?0.73 dB in the right eye. e–g Color fundus photographic (e), nIR (f), and red-free (g) images of the left eye also
showed an enlargement of the optic nerve head cup and annular peripapilllary atrophy. Additionally, nIR (f) and red-free cSLO (g) images showed focal hyporeflectivity of the optic disc border at the inferotemporal quadrant (arrows) and consecutive nerve fiber layer defects (arrowheads) in the left eye. A typical pit of the optic nerve head was not evident in either eye. h, i Fluorescein angiography at 70 s (h) and 360 s (i) showed focal staining of the optic nerve head border at the inferotemporal quadrant (arrows). No other leakage or staining was observed in either eye. The pattern deviation map of the Humphrey Visual Field Analyzer (j) showed a central relative scotoma with an MD value of -1.65 dB in the left eye
head were not performed. The patient was instructed to maintain a prone position postoperatively for 1 week. The preoperative central macular thickness (CMT) was 327 lm with the subretinal fluid. Two weeks after the surgery, the CMT was 305 lm, but the subretinal fluid remained; both the retinoschisis and the subretinal fluid slowly resolved, and the macular detachment had completely resolved 3 months after the surgery. At 6 months after the surgery, the CMT was 172 lm, and the BCVA had improved to 0.9 (20/22) in the left eye. An OCT oblique scan showed a reduction in the retinal thickness at the optic nerve head rim (Fig. 3e; arrows), although the papillomacular outer retinoschisis was still present (Fig. 3b). OCT also showed a focal defect of the peripheral lamina cribrosa, i.e., a laminar disinsertion (Fig. 3e, h; yellow lines). At this time, the focal excavation of the optic nerve head was seen more clearly than at the initial examination in the left eye, which suggested an APON (Fig. 3h; arrowhead).
At 12 months after the surgery, the patient’s decimal BCVA was 1.0 (20/20) in both eyes. The IOP was 13 mmHg in the right eye and 11 mmHg in the left eye. The CMT measured by SD-OCT was 201 lm in the right eye and 184 lm in the left eye. The macular re-attachment and further resolution of the papillomacular retinoschisis in the left eye were confirmed by SD-OCT. Although there was no visual deterioration in the right eye, the nIR SLO images showed focal hyporeflectivity of the optic disc border at the inferotemporal quadrant which had not been observed during past routine examinations of the right eye (Fig. 4a; arrow). The SD-OCT image showed peripapillary inner and outer retinoschisis in the right eye (Fig. 4b, c). Additional FA examinations revealed late focal staining in the right eye corresponding to the focal hyporeflectivity observed in the nIR SLO images (Fig. 4d, e; arrows). Late fluorescein staining was no longer evident in the left eye. At 20 months postsurgery on the left eye and 8 months after the development of the peripapillary retinoschisis in
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Fig. 2 nIR and simultaneous spectral-domain optical coherence tomography (SD-OCT) images of the left eye at the initial visit. a, b Horizontal scan across the fovea showing papillomacular outer retinal schisis and macular detachment. c, d, f, g nIR and enhanced depth imaging OCT (EDI-OCT) images obtained by oblique scan along the 12 radial scans centered on the optic nerve head. The nIR images showed focal hyporeflectivity of the optic disc border at the inferotemporal quadrant (arrows). e High magnification of the boxed portion of d, showing thickening of the optic nerve head rim (arrows). Localized alterations of the lamina cribrosa insertion, a type of focal
laminar cribrosa defect, could also be seen (yellow line anterior laminar surface, filled light-blue circle expected anterior laminar insertion point, filled blue circle edge of the laminar disinsertion [29]). h High magnification of the boxed portion of g showing a focal excavation of the optic nerve head (arrowhead), suggesting a presumed acquired pit of the optic nerve head. Localized alterations of the lamina cribrosa insertion could also be seen (yellow line anterior laminar surface, filled light-blue circle expected anterior laminar insertion point, filled dark-blue circle edge of the laminar disinsertion [29])
the right eye, her BCVA was 1.0 (20/20) in both eyes. The peripapillary retinoschisis in her right eye extended beyond the macula, but its height had been reduced (Fig. 5a, b). EDI-OCT showed localized alterations of the lamina cribrosa insertion and consecutive residual inner and outer retinoschisis in the right eye (Fig. 5c, d).
examinations showed it more clearly. The postoperative OCT image was similar to the images obtained in an earlier study, which showed the excavations to be an APON [29]. We had no evidence to indicate that these pits were truly acquired; thus, our diagnosis was that of a presumed APON. Acquired optic nerve pits have been reported to be associated with visual field defects and the presence and progression of glaucoma [23, 30–33]. However, retinoschisis or macular detachment has rarely been reported to be associated with APON [24, 25]. Thus, our results indicate the need for special attention to be paid to the macular area when patients with acquired optic nerve pits complain of reduced vision. EDI-OCT revealed localized alterations of the lamina cribrosa insertions in both eyes, which have been defined as a type of focal lamina cribrosa defect [27–29]. In earlier histological studies lamina cribrosa defects were
Discussion We report here a case of bilateral papillomacular retinoschisis with an enlarged glaucomatous optic nerve cup. Vision in the left eye was reduced due to a macular detachment. Ophthalmoscopic examination did not reveal a congenital optic pit in either eye. The preoperative EDIOCT examinations demonstrated a small focal excavation of the optic nerve head, and the postoperative OCT
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Fig. 3 nIR and simultaneous SD-OCT images of the left eye 6 months after pars plana vitrectomy (PPV). a, b Horizontal SDOCT scan across the fovea showing macular re-attachment and a flattening of the papillomacular outer retinoschisis. c, d, f, g OCT oblique scans among the 12 radial scans centered on the optic nerve head. e, h High magnification of the boxed portion of d and g,
showing an improvement of the thickening at the optic nerve head rim (arrows). Localized alterations of the lamina cribrosa insertion are still present: yellow line anterior laminar surface, filled light-blue circle expected anterior laminar insertion point, filled dark-blue circle edge of the laminar disinsertion [29], arrowhead presumed acquired pit of the optic nerve head
found to be present in eyes with congenital optic pits [2] as well as in eyes with APON [23]. Recent EDI-OCT studies have shown that focal lamina cribrosa defects are often present in glaucomatous eyes without visible acquired pits [27–29]. In our case, papillomacular retinoschisis, which is typically associated with optic nerve head pits [34, 35], was observed in both eyes, but EDIOCT demonstrated a small pit-like excavation in the optic nerve head only in the left eye. An optic nerve head pit was not detected in the right eye on either the color photographs or on the cSLO and SD-OCT images. The findings in our case suggest that the retinoschisis with or without macular detachment resulted from the focal peripheral lamina cribrosa defects. Several earlier studies have shown optic pit-like maculopathies in eyes without an optic pit [12–22], but the pathogenesis of these maculopathies was not determined. The use of EDI-OCT to investigate focal lamina cribrosa defects may be a key
examination method to determine the pathogenesis of maculopathies without obvious optic pits. FA showed late fluorescein staining of the inferotemporal border of the optic nerve head in both eyes when an optic pit-like maculopathy was observed. This finding is consistent with typical observations of the optic nerve pit in earlier studies, but the source of the late FA staining was not determined [7, 8]. To the contrary, no fluorescein staining was seen when maculopathy was not present. Optic nerve rim volume fluctuations at the inferotemporal quadrant were observed in the OCT images that corresponded with the presence or absence of late fluorescein staining. Similar to the findings in our patient, Perkins et al. reported three patients with atypical optic nerve pits that showed fluctuating appearances of the optic nerve head [16]. These authors hypothesized that such dynamic changes resulted from fluid trapped under the redundant dysplastic retinal tissue normally lining the atypical optic
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Fig. 4 nIR image, simultaneous SD-OCT, and fluorescein angiographic (FA) images of the right eye at 13 months after the initial visit. a nIR image showing focal hyporeflectivity of the optic disc border at the inferotemporal quadrant (arrow). b Horizontal SD-OCT scan across the fovea showing peripapillary outer retinoschisis.
c Another horizontal scan at the inferotemporal margin of the optic nerve head showing inner and outer retinoschisis. d, e FA (d 63 s, e 467 s) showing focal staining of the optic nerve head border at the inferotemporal quadrant (arrows)
Fig. 5 nIR and simultaneous SD-OCT images of the right eye at 21 months after the initial visit. a, b Horizontal scan across the fovea showing that the peripapillary retinoschisis extended beyond the macula, but that the height was reduced. c EDI-OCT oblique scan across the optic nerve head. d High magnification of the boxed
portion of c, showing peripapillary inner and outer retinoschisis and localized alterations of the lamina cribrosa insertion: yellow line anterior laminar surface, light-blue filled circle expected anterior laminar insertion point, dark-blue filled circle edge of the laminar disinsertion [29]
pit wall [16]. Although the source of the intraretinal/subretinal fluid was not determined, the late FA staining indicated an active pooling of the fluid, which resulted in the thickening of the optic nerve head rim and papillomacular retinoschisis. The late FA staining in our patient suggested an active phase of pathological changes, and special attention should be paid to possible progression to vision-threatening macular complications.
PPV with internal limited membrane (ILM) peeling and SF6 gas tamponade was performed to re-attach the detached macula accompanied by a presumed APON in the left eye. During the surgery, a thin premacular vitreous cortex was observed, but an unusual posterior vitreous strand connected to the optic nerve head [36] was not. Despite the gas tamponade, postoperative resolution of the retinoschisis or subretinal fluid was not observed
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immediately. We did not drain the subretinal fluid or perform endolaser photocoagulation intraoperatively, and the retinoschisis and macular detachment resolved slowly. Our case study suggests that PPV seems to be an effective method of managing the macular detachment resulting from a presumed APON or a focal lamina cribrosa defect. However, the need for ILM peeling or gas tamponade could not be assessed. The major limitation of this study is its retrospective nature. The methods we used to acquire the SD-OCT images must also be borne in mind. We used radial scans (12 B-scans at 15° intervals) centered on the optic disc and not a three-dimensional volumetric scan to evaluate optic nerve head morphology. This was done to reduce the data acquisition time and thereby also the patient’s stress. However, a small lesion may exist that was missed by the 12 radial scans. In summary, we have presented a case of bilateral optic pit-like maculopathy and an enlarged glaucomatous optic nerve head cup. However, a typical congenital optic pit was not evident in either eye. EDI-OCT showed a focal lamina cribrosa defect at the inferotemporal margin of the optic nerve head. This area corresponded to the late fluorescein staining shown in the FA examination. We suggest that the papillomacular retinoschisis was due to the focal peripheral lamina cribrosa defect. Acknowledgments The authors thank Dr. Masanori Hangai for his support in the data interpretation. Conflicts of interest T. Yoshitake, None; H. Nakanishi, None; Y. Setoguchi, None; K. Kuroda, None; K. Amemiya, None; M. Taniguchi, None; A. Otani, None.
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10. Hirakata A, Okada AA, Hida T. Long-term results of vitrectomy without laser treatment for macular detachment associated with an optic disc pit. Ophthalmology. 2005;112:1430–5. 11. Hirakata A, Inoue M, Hiraoka T, McCuen BW II. Vitrectomy without laser treatment or gas tamponade for macular detachment associated with an optic disc pit. Ophthalmology. 2012;119: 810–8. 12. Hamada S, Yoshida K, Chihara E. Pseudo-disc-pits.macular syndrome. Nihon Ganka Gakkai Zasshi. 2001;105:338–42 (in Japanese). 13. Spaide RF, Costa DL, Huang SJ. Macular schisis in a patient without an optic disk pit optical coherence tomographic findings. Retina. 2003;23:238–40. 14. Hotta K. Unsuccessful vitrectomy without gas tamponade for macular retinal detachment and retinoschisis without optic disc pit. Ophthalmic Surg Lasers Imaging. 2004;35:328–31. 15. Hollander DA, Barricks ME, Duncan JL, Irvine AR. Macular schisis detachment associated with angle-closure glaucoma. Arch Ophthalmol. 2005;123:270–2. 16. Perkins SL, Han DP, Gonder JR, Beaumont PE, Colev G. Dynamic atypical optic nerve coloboma associated with transient macular detachment. Arch Ophthalmol. 2005;123:1750–4. 17. Zumbro DS, Jampol LM, Folk JC, Olivier MM, Anderson-Nelson S. Macular schisis and detachment associated with presumed acquired enlarged optic nerve head cups. Am J Ophthalmol. 2007;144:70–4. 18. Farjad H, Besada E, Frauens BJ. Peripapillary schisis with serous detachment in advanced glaucoma. Optom Vis Sci. 2010;87: E205–17. 19. Pokroy R, Desai UR. Bilateral optic pit-like maculopathy with normal optic nerve heads. Can J Ophthalmol. 2010;45:415–6. 20. Zhao M, Li X. Macular retinoschisis associated with normal tension glaucoma. Graefes Arch Clin Exp Ophthalmol. 2011;249: 1255–8. 21. Moreno-Lopez M, Gonzalez-Lopez JJ, Jarrin E, Bertrand J. Retinoschisis and macular detachment associated with acquired enlarged optic disc cup. Clin Ophthalmol. 2012;6:433–6. 22. Hedels C, Krohn J. Enhanced depth imaging optical coherence tomography of optic disc maculopathy without a visible optic pit. Clin Experiment Ophthalmol. 2013;41:894–6. 23. Radius RL, Maumenee AE, Green WR. Pit-like changes of the optic nerve head in open-angle glaucoma. Br J Ophthalmol. 1978;62:389–93. 24. Rath EZ, Rumelt S. Acute visual loss due to serous retinal detachment from acquired optic pit may be a rare presentation of primary open-angle glaucoma. Can J Ophthalmol. 2007;42: 339–40. 25. Song IS, Shin JW, Shin YW, Uhm KB. Optic disc pit with peripapillary retinoschisis presenting as a localized retinal nerve fiber layer defect. Korean J Ophthalmol. 2011;25:455–8. 26. Spaide RF, Koizumi H, Pozzoni MC. Enhanced depth imaging spectral-domain optical coherence tomography. Am J Ophthalmol. 2008;146:496–500. 27. Kiumehr S, Park SC, Syril D, Teng CC, Tello C, Liebmann J, et al. In vivo evaluation of focal lamina cribrosa defects in glaucoma. Arch Ophthalmol. 2012;130:552–9. 28. Park SC, De Moraes CG, Teng CC, Tello C, Liebmann JM, Ritch R. Enhanced depth imaging optical coherence tomography of deep optic nerve complex structures in glaucoma. Ophthalmology. 2012;119:3–9. 29. You JY, Park SC, Su D, Teng CC, Liebmann JM, Ritch R. Focal lamina cribrosa defects associated with glaucomatous rim thinning and acquired pits. JAMA Ophthalmol. 2013;131:314–20. 30. Javitt JC, Spaeth GL, Katz LJ, Poryzees E, Addiego R. Acquired pits of the optic nerve. Increased prevalence in patients with lowtension glaucoma. Ophthalmology. 1990;97:1038–43.
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35. Roy R, Waanbah AD, Mathur G, Raman R, Sharma T. Optical coherence tomography characteristics in eyes with optic pit maculopathy. Retina. 2013;33:771–5. 36. Hirakata A, Hida T, Wakabayashi T, Fukuda M. Unusual posterior hyaloid strand in a young child with optic disc pit maculopathy: intraoperative and histopathological findings. Jpn J Ophthalmol. 2005;49:264–6.
CLINICAL INVESTIGATION
Bilateral papillomacular retinoschisis and macular detachment accompanied by focal lamina cribrosa defect in glaucomatous eyes Tatsuya Yoshitake • Hideo Nakanishi • Yoshinao Setoguchi • Kenichi Kuroda • Kaori Amemiya • Misa Taniguchi • Atsushi Otani
Received: 14 December 2013 / Accepted: 28 April 2014 Ó Japanese Ophthalmological Society 2014
Abstract Purpose We report here a patient with bilateral papillomacular retinoschisis with an enlarged glaucomatous optic nerve head cup and a focal lamina cribrosa defect, the findings of our clinical investigations of this case, and the chosen treatment and outcome. Design This is an observational case report. Methods Clinical examinations were performed using simultaneous confocal scanning laser ophthalmoscopy and optical coherence tomography (OCT). The patient was treated by pars plana vitrectomy (PPV). Results The left eye had a macular detachment with a presumed acquired pit of the optic nerve, while the right eye did not have an obvious optic nerve pit. Enhanced depth imaging OCT showed focal lamina cribrosa defects in both eyes. PPV was performed on the left eye, which resulted in a re-attachment of the macula and improvement of the visual acuity. Conclusions Our findings suggest that the pathological changes were most likely due to focal lamina cribrosa defects in both glaucomatous eyes. This type of maculopathy can be successfully treated with PPV.
T. Yoshitake H. Nakanishi (&) Y. Setoguchi K. Kuroda K. Amemiya M. Taniguchi A. Otani Department of Ophthalmology, Japanese Red Cross Society Wakayama Medical Center, 4-20 Komatsubaradouri, Wakayama City, Wakayama 640-8558, Japan e-mail: [email protected] H. Nakanishi Department of Ophthalmology and Visual Sciences, Kyoto University Graduate School of Medicine, Kyoto, Japan
Keywords Focal lamina cribrosa defect Acquired pit of the optic nerve Enhanced depth imaging optical coherence tomography Retinoschisis Pars plana vitrectomy
Introduction Papillomacular retinoschisis with or without macular detachment is a relatively common complication of an optic nerve head pit, and papillomacular retinoschisis with a pit is called optic pit maculopathy or pit macular syndrome [1–6]. An optic nerve head pit is a congenital optic nerve anomaly [7, 8] which occurs in approximately 1 in 11,000 individuals [1]. Several studies have shown that although the maculopathy associated with an optic nerve head pit has a relatively poor visual prognosis [5, 9], it can be successfully treated by pars plana vitrectomy (PPV) [10, 11]. Retinoschisis and macular detachment without a visible optic nerve head pit has also been identified by optical coherence tomography (OCT), especially in eyes with glaucoma [12–22]. Glaucomatous eyes often have focal structural abnormalities of the optic nerve head, referred to as acquired pits of the optic nerve (APON) [23]. In early case reports, the treating physician assumed that these APON were correlated with the presence of macular retinoschisis or macular detachment [24, 25]. To date, the pathogenesis of papillomacular retinoschisis with or without macular detachment in glaucomatous eyes has not been completely determined. Early histological studies revealed the presence of lamina cribrosa defects in eyes with congenital optic pits [2] and in eyes with APON [23]. Enhanced depth imaging (EDI)-OCT was developed to improve the quality of the images of the deep posterior segment structures [26]. This imaging methods has been used
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in several studies to show focal lamina cribrosa defects in eyes with glaucoma. Some of the defects were associated with APON, but others were not [27–29]. We report here the case of a woman with bilateral papillomacular retinoschisis with enlarged glaucomatous optic nerve head cups. One of the eyes also had a macular detachment with a presumed APON, whereas the other eye did not have a visible optic nerve pit. Focal lamina cribrosa defects were detected by EDI-OCT in both eyes. PPV was performed on the left eye, which had the macular detachment, and the retina was re-attached with a subsequent improvement of visual acuity.
Methods This was a retrospective study of a case of bilateral papillomacular retinoschisis in a elderly Japanese woman. The study followed the tenets of the Declaration of Helsinki, and the ethics committee of our institute had ruled that approval was not required for such retrospective studies. The patient had a comprehensive ophthalmologic examination, including automatic objective determination of refractive errors, best-corrected visual acuity (BCVA) measurements, intraocular pressure (IOP) measurements with a Goldmann applanation tonometer, visual field testing by standard automated perimetry (Humphrey Visual Field Analyzer, the SAP, 24-2 Swedish Interactive Threshold Algorithm Standard strategy; Carl Zeiss Meditec, Dublin, CA), dilated indirect ophthalmoscopy, slitlamp biomicroscopy of the fundus, color fundus photography, confocal scanning laser ophthalmoscopy (cSLO), and spectral-domain OCT (SD-OCT; HRA-2; Heidelberg Engineering, Heidelberg, Germany). The B-scan SD-OCT images were obtained by averaging 25-50 images to reduce speckle noise. White-on-black images were used for all OCT evaluations, and the contrast and brightness were adjusted on each image to obtain the best image quality. For the EDI-OCT, a previously described method was used [26]. The evaluations of the cSLO and SD-OCT images were independently performed by two investigators (T.Y. and A.O.), who were blinded to all other ophthalmic information on each patient. When the two investigators disagreed, consensus was reached with further discussion.
Case report A 69-year-old Japanese woman who complained of blurred vision in her left eye was referred to our clinic in April 2011. At the initial visit, her decimal BCVA, determined on a Landolt chart, was 0.9 (20/22 Snellen units) in the right eye and 0.4 (20/50) in the left eye. Both eyes were
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phakic, and the refractive error (spherical equivalent) was ?1.5 D in the right eye and ?2.0 D in the left eye. The IOP was 11 mmHg in both eyes. Ophthalmoscopy, near-infrared reflectance (nIR), and red-free cSLO showed that she had an enlarged optic nerve head cup with annular peripapillary atrophy in both eyes (Fig. 1a-g). In her left eye, the nIR and red-free cSLO images showed focal hyporeflectivity of the optic disc border at the inferotemporal quadrant (Fig. 1f, g; arrows) and nerve fiber layer defects (Fig. 1g; arrowheads). The mean deviation (MD) values obtained by standard automated perimetry were ?0.73 dB in the right eye and -1.65 dB in the left eye (Fig. 1d, j). Examination of a horizontal OCT scan through the fovea showed outer retinoschisis and macular detachment in the left eye (Fig. 2a, b). Fluorescein angiography (FA) and additional EDI-OCT radial scans centered on the optic nerve head (12 B-scans at 15° intervals) were obtained for the left eye. FA showed late focal staining of the optic nerve head margin corresponding to the focal hyporeflectivity observed in the nIR cSLO images (Fig. 1h, i; arrows). No other leakage or staining was observed in either eye. Oblique EDI-OCT scans showed a thickening of the optic nerve head rim (Fig. 2e, h; arrows) corresponding to the focal hyporeflectivity in the nIR images (Fig. 2c, f; arrows). The EDIOCT images also showed a downward sloping of the peripheral anterior laminar surface toward its expected insertion point (Fig. 2e, h; yellow lines). Earlier studies had defined this localized alteration of the peripheral lamina cribrosa insertion as a type of focal lamina cribrosa defect and called it a ‘‘laminar disinsertion’’ [27–29]. One of the oblique EDI-OCT images also showed a small focal excavation of the optic nerve head in the left eye (Fig. 2h; arrowhead). An examination 1 month later showed no spontaneous improvements of the retinoschisis or macular detachment. In May 2011, we decided to treat the left eye with 25-gauge 3-port PPV combined with phacoemulsification and intraocular lens implantation. The patient was informed about the risks and benefits of the surgery, and her written informed consent was obtained before the surgery. The preoperative decimal BCVA in the left eye was 0.5 (20/40). A partial posterior vitreous detachment was present, and a thin premacular vitreous cortex was observed during the surgery. However, no unusual posterior vitreous strand connected to the optic nerve head was observed. Removal of the residual premacular vitreous cortex, internal limiting membrane peeling with indocyanine green staining, air-fluid exchange, and tamponade with nonexpansive sulfur hexafluoride (SF6) gas were performed. However, draining of the subretinal fluid and endolaser photocoagulation of the temporal margin of the optic nerve
Focal lamina cribrosa defect maculopathy
Fig. 1 Color fundus photographic, confocal scanning laser ophthalmoscopic (cSLO), and standard automated perimetric images of a patient with bilateral papillomacular retinoschisis and macular detachment accompanied by a focal lamina cribrosa defect at the initial visit. a–c Color fundus photographic (a), near-infrared (nIR) (b), and red-free (c) images of the right eye showing enlargement of the optic nerve head cup and annular peripapillary atrophy. d The mean deviation (MD) value of the Humphrey Visual Field Analyzer with the 24-2 Swedish interactive threshold algorithm standard program (d) was ?0.73 dB in the right eye. e–g Color fundus photographic (e), nIR (f), and red-free (g) images of the left eye also
showed an enlargement of the optic nerve head cup and annular peripapilllary atrophy. Additionally, nIR (f) and red-free cSLO (g) images showed focal hyporeflectivity of the optic disc border at the inferotemporal quadrant (arrows) and consecutive nerve fiber layer defects (arrowheads) in the left eye. A typical pit of the optic nerve head was not evident in either eye. h, i Fluorescein angiography at 70 s (h) and 360 s (i) showed focal staining of the optic nerve head border at the inferotemporal quadrant (arrows). No other leakage or staining was observed in either eye. The pattern deviation map of the Humphrey Visual Field Analyzer (j) showed a central relative scotoma with an MD value of -1.65 dB in the left eye
head were not performed. The patient was instructed to maintain a prone position postoperatively for 1 week. The preoperative central macular thickness (CMT) was 327 lm with the subretinal fluid. Two weeks after the surgery, the CMT was 305 lm, but the subretinal fluid remained; both the retinoschisis and the subretinal fluid slowly resolved, and the macular detachment had completely resolved 3 months after the surgery. At 6 months after the surgery, the CMT was 172 lm, and the BCVA had improved to 0.9 (20/22) in the left eye. An OCT oblique scan showed a reduction in the retinal thickness at the optic nerve head rim (Fig. 3e; arrows), although the papillomacular outer retinoschisis was still present (Fig. 3b). OCT also showed a focal defect of the peripheral lamina cribrosa, i.e., a laminar disinsertion (Fig. 3e, h; yellow lines). At this time, the focal excavation of the optic nerve head was seen more clearly than at the initial examination in the left eye, which suggested an APON (Fig. 3h; arrowhead).
At 12 months after the surgery, the patient’s decimal BCVA was 1.0 (20/20) in both eyes. The IOP was 13 mmHg in the right eye and 11 mmHg in the left eye. The CMT measured by SD-OCT was 201 lm in the right eye and 184 lm in the left eye. The macular re-attachment and further resolution of the papillomacular retinoschisis in the left eye were confirmed by SD-OCT. Although there was no visual deterioration in the right eye, the nIR SLO images showed focal hyporeflectivity of the optic disc border at the inferotemporal quadrant which had not been observed during past routine examinations of the right eye (Fig. 4a; arrow). The SD-OCT image showed peripapillary inner and outer retinoschisis in the right eye (Fig. 4b, c). Additional FA examinations revealed late focal staining in the right eye corresponding to the focal hyporeflectivity observed in the nIR SLO images (Fig. 4d, e; arrows). Late fluorescein staining was no longer evident in the left eye. At 20 months postsurgery on the left eye and 8 months after the development of the peripapillary retinoschisis in
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Fig. 2 nIR and simultaneous spectral-domain optical coherence tomography (SD-OCT) images of the left eye at the initial visit. a, b Horizontal scan across the fovea showing papillomacular outer retinal schisis and macular detachment. c, d, f, g nIR and enhanced depth imaging OCT (EDI-OCT) images obtained by oblique scan along the 12 radial scans centered on the optic nerve head. The nIR images showed focal hyporeflectivity of the optic disc border at the inferotemporal quadrant (arrows). e High magnification of the boxed portion of d, showing thickening of the optic nerve head rim (arrows). Localized alterations of the lamina cribrosa insertion, a type of focal
laminar cribrosa defect, could also be seen (yellow line anterior laminar surface, filled light-blue circle expected anterior laminar insertion point, filled blue circle edge of the laminar disinsertion [29]). h High magnification of the boxed portion of g showing a focal excavation of the optic nerve head (arrowhead), suggesting a presumed acquired pit of the optic nerve head. Localized alterations of the lamina cribrosa insertion could also be seen (yellow line anterior laminar surface, filled light-blue circle expected anterior laminar insertion point, filled dark-blue circle edge of the laminar disinsertion [29])
the right eye, her BCVA was 1.0 (20/20) in both eyes. The peripapillary retinoschisis in her right eye extended beyond the macula, but its height had been reduced (Fig. 5a, b). EDI-OCT showed localized alterations of the lamina cribrosa insertion and consecutive residual inner and outer retinoschisis in the right eye (Fig. 5c, d).
examinations showed it more clearly. The postoperative OCT image was similar to the images obtained in an earlier study, which showed the excavations to be an APON [29]. We had no evidence to indicate that these pits were truly acquired; thus, our diagnosis was that of a presumed APON. Acquired optic nerve pits have been reported to be associated with visual field defects and the presence and progression of glaucoma [23, 30–33]. However, retinoschisis or macular detachment has rarely been reported to be associated with APON [24, 25]. Thus, our results indicate the need for special attention to be paid to the macular area when patients with acquired optic nerve pits complain of reduced vision. EDI-OCT revealed localized alterations of the lamina cribrosa insertions in both eyes, which have been defined as a type of focal lamina cribrosa defect [27–29]. In earlier histological studies lamina cribrosa defects were
Discussion We report here a case of bilateral papillomacular retinoschisis with an enlarged glaucomatous optic nerve cup. Vision in the left eye was reduced due to a macular detachment. Ophthalmoscopic examination did not reveal a congenital optic pit in either eye. The preoperative EDIOCT examinations demonstrated a small focal excavation of the optic nerve head, and the postoperative OCT
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Fig. 3 nIR and simultaneous SD-OCT images of the left eye 6 months after pars plana vitrectomy (PPV). a, b Horizontal SDOCT scan across the fovea showing macular re-attachment and a flattening of the papillomacular outer retinoschisis. c, d, f, g OCT oblique scans among the 12 radial scans centered on the optic nerve head. e, h High magnification of the boxed portion of d and g,
showing an improvement of the thickening at the optic nerve head rim (arrows). Localized alterations of the lamina cribrosa insertion are still present: yellow line anterior laminar surface, filled light-blue circle expected anterior laminar insertion point, filled dark-blue circle edge of the laminar disinsertion [29], arrowhead presumed acquired pit of the optic nerve head
found to be present in eyes with congenital optic pits [2] as well as in eyes with APON [23]. Recent EDI-OCT studies have shown that focal lamina cribrosa defects are often present in glaucomatous eyes without visible acquired pits [27–29]. In our case, papillomacular retinoschisis, which is typically associated with optic nerve head pits [34, 35], was observed in both eyes, but EDIOCT demonstrated a small pit-like excavation in the optic nerve head only in the left eye. An optic nerve head pit was not detected in the right eye on either the color photographs or on the cSLO and SD-OCT images. The findings in our case suggest that the retinoschisis with or without macular detachment resulted from the focal peripheral lamina cribrosa defects. Several earlier studies have shown optic pit-like maculopathies in eyes without an optic pit [12–22], but the pathogenesis of these maculopathies was not determined. The use of EDI-OCT to investigate focal lamina cribrosa defects may be a key
examination method to determine the pathogenesis of maculopathies without obvious optic pits. FA showed late fluorescein staining of the inferotemporal border of the optic nerve head in both eyes when an optic pit-like maculopathy was observed. This finding is consistent with typical observations of the optic nerve pit in earlier studies, but the source of the late FA staining was not determined [7, 8]. To the contrary, no fluorescein staining was seen when maculopathy was not present. Optic nerve rim volume fluctuations at the inferotemporal quadrant were observed in the OCT images that corresponded with the presence or absence of late fluorescein staining. Similar to the findings in our patient, Perkins et al. reported three patients with atypical optic nerve pits that showed fluctuating appearances of the optic nerve head [16]. These authors hypothesized that such dynamic changes resulted from fluid trapped under the redundant dysplastic retinal tissue normally lining the atypical optic
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Fig. 4 nIR image, simultaneous SD-OCT, and fluorescein angiographic (FA) images of the right eye at 13 months after the initial visit. a nIR image showing focal hyporeflectivity of the optic disc border at the inferotemporal quadrant (arrow). b Horizontal SD-OCT scan across the fovea showing peripapillary outer retinoschisis.
c Another horizontal scan at the inferotemporal margin of the optic nerve head showing inner and outer retinoschisis. d, e FA (d 63 s, e 467 s) showing focal staining of the optic nerve head border at the inferotemporal quadrant (arrows)
Fig. 5 nIR and simultaneous SD-OCT images of the right eye at 21 months after the initial visit. a, b Horizontal scan across the fovea showing that the peripapillary retinoschisis extended beyond the macula, but that the height was reduced. c EDI-OCT oblique scan across the optic nerve head. d High magnification of the boxed
portion of c, showing peripapillary inner and outer retinoschisis and localized alterations of the lamina cribrosa insertion: yellow line anterior laminar surface, light-blue filled circle expected anterior laminar insertion point, dark-blue filled circle edge of the laminar disinsertion [29]
pit wall [16]. Although the source of the intraretinal/subretinal fluid was not determined, the late FA staining indicated an active pooling of the fluid, which resulted in the thickening of the optic nerve head rim and papillomacular retinoschisis. The late FA staining in our patient suggested an active phase of pathological changes, and special attention should be paid to possible progression to vision-threatening macular complications.
PPV with internal limited membrane (ILM) peeling and SF6 gas tamponade was performed to re-attach the detached macula accompanied by a presumed APON in the left eye. During the surgery, a thin premacular vitreous cortex was observed, but an unusual posterior vitreous strand connected to the optic nerve head [36] was not. Despite the gas tamponade, postoperative resolution of the retinoschisis or subretinal fluid was not observed
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immediately. We did not drain the subretinal fluid or perform endolaser photocoagulation intraoperatively, and the retinoschisis and macular detachment resolved slowly. Our case study suggests that PPV seems to be an effective method of managing the macular detachment resulting from a presumed APON or a focal lamina cribrosa defect. However, the need for ILM peeling or gas tamponade could not be assessed. The major limitation of this study is its retrospective nature. The methods we used to acquire the SD-OCT images must also be borne in mind. We used radial scans (12 B-scans at 15° intervals) centered on the optic disc and not a three-dimensional volumetric scan to evaluate optic nerve head morphology. This was done to reduce the data acquisition time and thereby also the patient’s stress. However, a small lesion may exist that was missed by the 12 radial scans. In summary, we have presented a case of bilateral optic pit-like maculopathy and an enlarged glaucomatous optic nerve head cup. However, a typical congenital optic pit was not evident in either eye. EDI-OCT showed a focal lamina cribrosa defect at the inferotemporal margin of the optic nerve head. This area corresponded to the late fluorescein staining shown in the FA examination. We suggest that the papillomacular retinoschisis was due to the focal peripheral lamina cribrosa defect. Acknowledgments The authors thank Dr. Masanori Hangai for his support in the data interpretation. Conflicts of interest T. Yoshitake, None; H. Nakanishi, None; Y. Setoguchi, None; K. Kuroda, None; K. Amemiya, None; M. Taniguchi, None; A. Otani, None.
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