Evaluation of Morning Glory Syndrome with Spectral Optical Coherence Tomography and Echography Gilda Cennamo, MD,1 Giuseppe de Crecchio, MD,1 Gennarfrancesco Iaccarino, MD,2 Raimondo Forte, MD,1 Giovanni Cennamo, MD1 Purpose: To evaluate eyes affected by morning glory syndrome (MGS) with spectral-domain optical coherence tomography (SD OCT) and echography. Design: Prospective case series. Participants: Nineteen patients (22 eyes) with MGS observed at the Eye Department, University of Naples Federico II, Naples, Italy. Methods: All patients underwent a complete ophthalmologic examination that included best-correct visual acuity, fundus photography, and echography. Nine patients underwent SD OCT and high-frequency B-scan echography (20 MHz). Main Outcome Measures: Spectral-domain optical coherence tomography and echographic findings in MGS. Results: Spectral-domain optical coherence tomography revealed retinal detachment in the conus area of 5 eyes: 4 with noncontractile MGS (NCMGS) and 1 with contractile MGS (CMGS). There was evidence of a retinal break in only 2 cases. All 5 eyes had an abnormal communication between the subarachnoid space and the subretinal space. Spectral-domain optical coherence tomography did not reveal differences between CMGS and NCMGS. Echographic examination did not reveal any anatomic abnormalities of the optic nerve or orbit. Conclusions: Spectral-domain optical coherence tomography provides more information than echography about the posterior pole, whereas echographic examination is the only technique that can confirm the anatomic integrity of the optic nerve in the orbital wall. Retinal detachment in MGS generally is ascribed to abnormal communication between the subretinal and subarachnoid or vitreous compartments. These data suggest that myopialike retinal detachment without a retinal break may result from tissue stretching around the peripapillary conus. Financial Disclosure(s): The author(s) have no proprietary or commercial interest in any materials discussed in this article. Ophthalmology 2010;117:1269 –1273 © 2010 by the American Academy of Ophthalmology.
Morning glory syndrome (MGS) is a rare congenital optic disc dysplasia consisting of a conical excavation of the posterior pole including the optic disc. This excavation is filled with glial tissue, and a pigment ring slightly protrudes into the peripapillary area. The number of retinal vessels is increased, and they appear to arise from the disc margin from where they tend to run to the peripheral retina in a straighter course than usual. The peripheral retina appears normal.1 Morning glory syndrome is more frequent in women and, in the United States, less frequent in black people. It may be because of a lack of closure of the fetal fissure, and therefore may be a variant of optic nerve coloboma, or it may be a primary mesenchymal abnormality. It also may be the result of dilation of the optic nerve head caused by dysgenesis of the terminal optic stalk, which fails to close, thereby leading to persistent excavation of the optic nerve head. The central gliosis and the vascular pattern suggest primary neuroectodermal dysgenesis.2,3 Morning glory syndrome has been associated with other ocular abnormalities such as persistence of primary vitreous and different degrees of retinal detachment. Morning glory syndrome can be noncontractile (NCMGS) or, in extremely © 2010 by the American Academy of Ophthalmology Published by Elsevier Inc.
rare cases, it can be associated with contractile movements of the optic disc (CMGS).4 Morning glory syndrome can be confused with peripapillary staphyloma, which is a rare anomaly consisting of a deep excavation of the fundus surrounding the optic disc.4 This article reports the results of standardized echography of the posterior pole, the optic nerve, and tissue in the orbital cone in 16 patients (19 eyes) with NCMGS and in 3 patients (3 eyes) with CMGS. Nine of these 19 patients were reevaluated with high-frequency B-scan echography and with spectral-domain optical coherence tomography (SD OCT).
Patients and Methods The inclusion criteria for this study were clinical and echographic evidence of MGS confirmed by fundus examination by at least 3 ophthalmologists. A pregnancy and family history were obtained, and an ophthalmic examination and evaluation were carried out with standardized echography. Between 1981 and 2009, 19 patients were diagnosed with MGS at the Eye Clinic of the University of Naples Federico II, Naples, Italy, and were enrolled in this study. Informed consent was obtained from each patient. The ISSN 0161-6420/10/$–see front matter doi:10.1016/j.ophtha.2009.10.045
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Figure 1. A, B-scan echography with a 10-MHz probe of noncontractile morning glory syndrome (NCMGS) of the right eye showing the conical excavation of the posterior pole (arrow). B, A-scan echography showing a normal optic nerve in the same case of NCMGS. C, B-scan echography with 10-MHz probe of contractile morning glory syndrome (CMGS) of the left eye showing the conical excavation of the posterior pole (arrow). D, B-scan echography with a 20-MHz probe of the same CMGS patient.
ethics committee of the eye clinic approved the study, which was performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki. Eleven of these 19 patients were available for reexamination. Two patients declined re-examination because they were satisfied with their condition. Nine of the remaining 11 patients underwent high-frequency (20 MHz) B-scan echography, and OCT examination with a spectral-domain apparatus (SD OCT). These examinations and clinical evaluation, revealed NCMGS in 6 eyes and CMGS in 3 eyes. The retinal features were evaluated using SD OCT (Ophthalmic Technologies, Inc., Toronto, Canada). In SD OCT, a super luminescent diode produces a light with a wavelength of 840 nm (bandwidth, 150 nm). This provides simultaneous measurements of light echoes from different axial depths, without movement of the reference arm, thereby shortening acquisition time. In SD OCT, the inner retinal boundary used to obtain retinal thickness is the internal limiting membrane, whereas the outer boundary is the retinal pigment epithelium. Retinal features, vitreous features, and optic nerve and retrobulbar tissue were evaluated using standardized A-scan echography and B-scan ultrasonography (Cinescan S Ophthalmic Ultrasound System; Quantel Medical S.A., Clermont-Ferrand, France) with 10- and 20-MHz B-scan probes.5
Results Of the 19 patients in this cases series (22 eyes), 14 were women. The right eye was affected in 10 patients, the left eye in 6 patients, and both eyes were affected in 3 patients. The age at presentation ranged from 6 months to 30 years, with a mean age of 12 years and
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7 months. Snellen visual acuity was obtained in 11 patients and ranged between 20/20 and hand movements. Six of these 11 patients had a visual acuity of 20/200 or better. Three had a visual acuity of 20/40 or better, and the optic nerve abnormality did not impinge on the macula. Strabismus was present in 9 of 19 patients, of whom 6 had esotropia and 3 had exotropia. Refraction examination showed myopia between 1.0 and 10.0 D in 8 eyes and hypermetropia between 1.0 and 4.0 D in 3 eyes. It was not possible to determine refraction grade in 8 eyes because of partial or total retinal detachment or disease in the anterior or posterior segment. Standardized echography showed in all eyes a conical excavation of the posterior pole and normal optic nerve, whereas the orbital anatomic features were normal on ultrasound (Fig 1A–D). Several anomalies were identified in the eye ipsilateral to the eye affected by MGS. In fact, 2 eyes were microphthalmic with lens opacities and anterior hyaloid artery remnants in one of these cases. In the latter case, there was a striking persistence of primary vitreous and a posterior polar cataract and colobomas at 2 and 4 o’clock. In this patient, the ciliary body was stretched tightly toward the centre of the papillary field because of traction exerted on it by the primary vitreous, which appeared as a whitish mass.6 One of the 19 patients had simple chronic glaucoma only in the eye with MGS.7 Three patients had a contractile staphyloma (Fig 2A, B and Fig 3B-2). Excavation of the posterior pole was slight in one eye of a patient with bilateral MGS who had total retinal detachment in the other eye. In this case of total retinal detachment, B-scan echography showed a conical excavation in the posterior pole with the optic disc in the base. In 19 eyes, fundus examination showed a slightly raised pigmented ring around a staphyloma. Only 1 eye affected by CMGS was re-examined 26
Cennamo et al 䡠 Morning Glory Syndrome
Figure 2. A, Contractile morning glory syndrome (CMGS) of the right eye. B, C, Contractile movements of the peripapillary staphyloma (arrows). D, F, Retinal detachment can be associated with a break within the optic disc cup (arrow). The source of subretinal fluid may be cerebral spinal fluid. E, Spectral-domain optical coherence tomography showing the presence of glial tissue overlying the optic disc.
years after the first examination (1983–2009). Fundus photography of this patient showed that the pigmented ring had increased progressively during this time8 (Fig 3C-1, C-2). In 6 of the 9 eyes evaluated with SD OCT and B-scan ultrasonography, these procedures revealed glial tissue overlying the optic disc cup (Fig 3B-1, B-2 and Fig 2E). Five eyes were affected by retinal detachment localized in the conus area; there was no evidence of a retinal break in 3 of 5 cases. In all 5 eyes, there was an abnormal communication between the subarachnoid space and the subretinal space, which allowed cerebral spinal fluid to leak from the subarachnoid space of the optic nerve into the subretinal
space below the retina and caused detachment (Fig 2D, F and Fig 3A-1). One of these 5 eyes had NCMGS and a congenital optic disk pit in the contralateral eye (Fig 3A-1, A-2).
Discussion This article reports the clinical and echographic findings obtained in a large case series of MGS, and in the largest case series of CMGS published to date. Nine patients also
Figure 3. A-1, A-2, In a case of noncontractile morning glory syndrome (NCMGS) and an optic nerve pit in the contralateral eye, a retinal break (yellow arrow) can be seen in this spectral-domain optical coherence tomography (SD OCT) image, which may have been caused by traction from the peripapillary fibroglial tissue pulling on the retina. An abnormal communication between the subarachnoid space and the subretinal space (white arrow) may have allowed cerebrospinal fluid to leak from the subarachnoid space of the optic nerve to below the retina and to cause the detachment. B-1, Spectral-domain optical coherence tomography image showing glial tissue overlying the center of the optic disc in a CMGS patient. B-2, Contractile morning glory syndrome of the right eye. C-1, C-2, Fundus photography of the CMGS patient who was reexamined 26 years after the first examination (1983–2009) showing that the pigmented ring had increased during this time (arrows).
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underwent SD OCT and high-frequency B-scan echography. The findings are consistent with previous data showing that MGS usually is unilateral and more frequent in women. The possibility that MGS can be associated with ipsilateral and contralateral ocular abnormalities also was confirmed.3 To the authors’ knowledge, this is the first study of CMGS by SD OCT. However, neither SD OCT nor echography revealed any differences between CMGS and NCMGS. Morning glory syndrome can be confused with peripapillary staphyloma, which is a rare, usually unilateral, anomaly of the optic disc. In the latter malformation, the disc is situated at the base of the staphyloma, but unlike MGS, there are no vascular anomalies and the central glial tuft is absent. Peripapillary staphyloma and MGS seem to be pathogenetically distinct both regarding the timing of the lesion and the embryologic site of structural dysgenesis.4,9 Thus far, only 1 case of peripapillary staphyloma has been studied by SD OCT, and the procedure revealed a deeply seated right optic nerve with multiple intraretinal cystic cavities along the temporal tuft of staphyloma. Spectraldomain optical coherence tomography can measure the depth of a staphyloma.10 Staphyloma contractions in MGS can be induced by 2 mechanisms: pressure balance or muscle contraction.11 The case reported by Sugar and Beckman12 was the result of pressure balance because pulsation was related to the respiratory cycle and changes in venous pressure. However, other authors suggest that anomalous communication between the subarachnoid space and the juxtapapillary subretinal space causes changes in transient pressure gradients between the 2 compartments. Hence, staphyloma contraction in MGS could occur in relation to fluctuations in the cerebrospinal fluid pressure.13 However, contractile peripapillary staphyloma can be explained by the presence of heterotopic smooth muscle tissue in the posterior sclera.14 This smooth muscle tissue causes abnormal movements of the conical excavation.4,15 Kral and Svarc16 suggest that contractile staphyloma can be the result of an autonomic cholinergic muscular mechanism in the posterior part of the globe. The echographic evaluation of 3 pulsating cases seems to confirm the hypothesis that staphyloma contraction is associated with a cuff of smooth muscle tissue within the terminal optic nerve.4,14 Further support for this hypothesis comes from the observation that in all 3 cases, the contractile movement seemed to be induced by massage of the eyeball.8 However, the authors agree with Kral and Svrac that this phenomenon is the result of an autonomous cholinergic mechanism situated at the posterior pole of the eye because, in all the cases of CMGS, there was a latent period after 5 or 6 contractions. Echographic examination of the re-examined CMGS eye showed that the contraction of the staphyloma had not changed after 26 years. Moreover, in all 3 CMSG cases, echography of the optic nerve, orbital tissue, and posterior wall of the bulbus showed a normal optic nerve and absence of vascular malformation. Spectral-domain optical coherence tomography revealed retinal detachment of the conus area in 5 eyes (2 CMGS and 3 NCMGS). In accordance with other authors,17 the source of the serous fluid underlying the retina may be cerebrospi-
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nal fluid from the subarachnoid space. Only 2 eyes with retinal detachment had a retinal break that might have been caused by the traction from peripapillary fibroglial tissue pulling on the retina. Retinal detachment in the absence of a retinal break, as occurred in 3 of 5 eyes, may be the result of tissue stretching around the peripapillary conus. It also may be triggered by an abnormal communication between the cavity of the staphyloma and the subarachnoid space, which allowed cerebral spinal fluid to leak into the subretinal space. The presence of a retinal break resulting from traction near the coloboma would give rise to a rhegmatogenous retinal detachment. The SD OCT and echographic results, and reports by other groups, support this hypothesis.4,13,18 –20 The observation of a patient with optic nerve pits in one eye and MGS in the other supports the hypothesis that optic nerve pits and MGS may be simply points on a continuum, with the difference in appearance depending only on the degrees of excavation and abnormality.18 To the authors’ knowledge, this is the second report21 of optic nerve pits in one eye and MGS in the other, and the first case observed by SD OCT. These data suggest the possibility that the slightly raised pigmented ring observed around a staphyloma in all MGS eyes increases with age. The increased pigmentation in the peripapillary area after 26 years may be a consequence of the subretinal fluid in the staphyloma area identified by SD OCT, which results from the abnormal communication also identified by SD OCT. In conclusion, echography and SD OCT may contribute to a better understanding of MGS. In addition, the latter technique may provide information about the pathogenesis and clinical features of MGS.
References 1. Kindler P. Morning glory syndrome: unusual congenital optic disk anomaly. Am J Ophthalmol 1970;69:376 – 84. 2. Eustis HS, Sanders MR, Zimmerman T. Morning glory syndrome in children: association with endocrine and central nervous system anomalies. Arch Ophthalmol 1994;112:204 –7. 3. Harasymowycz P, Chevrette L, Décarie JC, et al. Morning glory syndrome: clinical, computerized tomographic, and ultrasonographic findings. J Pediatr Ophthalmol Strabismus 2005;42:290 –5. 4. Dutton GN. Congenital disorders of the optic nerve: excavations and hypoplasia. Eye 2004;18:1038 – 48. 5. Ossoinig KC. Standardized echography: basic principles, clinical applications, and results. Int Ophthalmol Clin 1979;19: 127–210. 6. Cennamo G, Liguori G, Pezone A, Iaccarino G. Morning glory syndrome associated with marked persistent hyperplastic primary vitreous and lens colobomas. Br J Ophthalmol 1989;73: 684 – 6. 7. Rinaldi E, De Rosa G, Severino R, Cennamo G. Morning glory syndrome with chronic simple glaucoma. Ophthalmic Paediatr Genet 1986;7:69 –72. 8. Cennamo G, Sammartino A, Fioretti F. Morning glory syndrome with contractile peripapillary staphyloma. Br J Ophthalmol 1983;67:346 – 8.
Cennamo et al 䡠 Morning Glory Syndrome 9. Pollock S. The morning glory disc anomaly: contractile movement, classification, and embryogenesis. Doc Ophthalmol 1987;65:439 – 60. 10. Woo SJ, Hwang JM. Spectral-domain optical coherence tomography of peripapillary staphyloma [letter]. Graefes Arch Clin Exp Ophthalmol 2009;247:1573– 4. 11. Vuori ML. Morning glory disc anomaly with pulsating peripapillary staphyloma. Acta Ophthalmol (Copenh) 1987;65:602– 6. 12. Sugar HS, Beckman H. Peripapillary staphyloma with respiratory pulsation. Am J Ophthalmol 1969;68:895–7. 13. Golnik KC. Cavitary anomalies of the optic disc: neurologic significance. Curr Neurol Neurosci Rep 2008;8:409 –13. 14. Manschot WA. Morning glory syndrome: a histopathological study. Br J Ophthalmol 1990;74:56 – 8. 15. Wise JB, MacLean AL, Gass JD. Contractile peripapillary staphyloma. Arch Ophthalmol 1966;75:626 –30. 16. Kral K, Svarc D. Contractile peripapillary staphyloma. Am J Ophthalmol 1971;71:1090 –2.
17. Yamakiri K, Uemura A, Sakamoto T. Retinal detachment caused by a slitlike break within the excavated disc in morning glory syndrome. Retina 2004;24:652–3. 18. Srinivasan G, Venkatesh P, Garg S. Optical coherence tomographic characteristics in morning glory disc anomaly. Can J Ophthalmol 2007;42:307–9. 19. Ho TC, Tsai PC, Chen MS, Lin LL. Optical coherence tomography in the detection of retinal break and management of retinal detachment in morning glory syndrome. Acta Ophthalmol Scand 2006;84:225–7. 20. Coll GE, Chang S, Flynn TE, Brown GC. Communication between the subretinal space and the vitreous cavity in the morning glory syndrome. Graefes Arch Clin Exp Ophthalmol 1995;233:441–3. 21. Samimi S, Antignac C, Combe C, et al. Bilateral macular detachment caused by bilateral optic nerve malformation in a papillorenal syndrome due to a new PAX2 mutation. Eur J Ophthalmol 2008;18:656 – 8.
Footnotes and Financial Disclosures Originally received: June 30, 2009. Final revision: October 9, 2009. Accepted: October 29, 2009. Available online: February 16, 2010.
Financial Disclosure(s): The author(s) have no proprietary or commercial interest in any materials discussed in this article. Manuscript no. 2009-878.
1
Eye Department, University of Naples Federico II, Naples, Italy.
2
Eye Department, Second University of Naples, Naples, Italy.
Presented at: American Academy of Ophthalmology Annual Meeting, November 2008, Atlanta, Georgia.
Correspondence: Gilda Cennamo, MD, Eye Department, University of Naples Federico II, Via Pansini 5, 80131 Napoli, Italy. E-mail:
[email protected].
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