Neuro-Ophthalmology at a Tertiary Eye Care Centre in India

Neuro-ophthalmology as a specialty is underdeveloped in India. The aim of our study was to determine the spectrum and profile of patients presenting to a tertiary eye care center with neuro-ophthalmic disorders. A retrospective hospital-based study was conducted, and records of all patients seen at the neuro-ophthalmology clinic of Dr. Rajendra Prasad Centre for Ophthalmic Sciences, All India Institute of Medical Sciences, New Delhi, India, over a 1-year period were retrieved and evaluated. Of a total of 30,111 patients referred to various specialty clinics in a span of 1 year, 1597 (5%) were referred for neuro-ophthalmology evaluation. The mean patient age was 30.8 ± 19.5 years, with a male dominance (M:F = 2.02:1). Among these patients, optic nerve disorders were noted in 63.8% (n = 1,020), cranial nerve palsy in 7% (n = 114), cortical visual impairment in 6.5% (n = 105), and others (eye/optic nerve hypophasia, blepharospasm, and optic disc drusen) in 6% (n = 95). Among the patients with optic nerve disorders, optic neuropathy without disc edema/(traumatic optic neuropathy, hereditary, tumor-related, retrobulbar neuritis, toxic, and idiopathic) was noted in 42.8% (n = 685) and optic neuropathy with disc edema (ischemic optic neuropathy, papilledema, post-papilledema optic atrophy, papillitis, neuroretinitis, and inflammatory optic neuropathy) in 20.9% (n = 335). Sixteen percent of patients (n = 263) were incorrect referrals. The neuro-ophthalmic clinic constitutes a significant referral unit in a tertiary eye care center in India. Traumatic and ischemic optic neuropathies are the most common diagnoses. Neuro-ophthalmology requires further development as a subspecialty in India to better serve the nation's population.

Original Contribution Neuro-Ophthalmology at a Tertiary Eye Care Centre in India Rebika Dhiman, MD, Digvijay Singh, MD, Shiva P. Gantayala, MD, Vaitheeswaran L. Ganesan, MD, Pradeep Sharma, MD, Rohit Saxena, MD, PhD Background: Neuro-ophthalmology as a specialty is underdeveloped in India. The aim of our study was to determine the spectrum and profile of patients presenting to a tertiary eye care center with neuro-ophthalmic disorders. Methods: A retrospective hospital-based study was conducted, and records of all patients seen at the neuroophthalmology clinic of Dr. Rajendra Prasad Centre for Ophthalmic Sciences, All India Institute of Medical Sciences, New Delhi, India, over a 1-year period were retrieved and evaluated. Results: Of a total of 30,111 patients referred to various specialty clinics in a span of 1 year, 1597 (5%) were referred for neuro-ophthalmology evaluation. The mean patient age was 30.8 ± 19.5 years, with a male dominance (M:F = 2.02:1). Among these patients, optic nerve disorders were noted in 63.8% (n = 1,020), cranial nerve palsy in 7% (n = 114), cortical visual impairment in 6.5% (n = 105), and others (eye/optic nerve hypophasia, blepharospasm, and optic disc drusen) in 6% (n = 95). Among the patients with optic nerve disorders, optic neuropathy without disc edema/(traumatic optic neuropathy, hereditary, tumor-related, retrobulbar neuritis, toxic, and idiopathic) was noted in 42.8% (n = 685) and optic neuropathy with disc edema (ischemic optic neuropathy, papilledema, post-papilledema optic atrophy, papillitis, neuroretinitis, and inflammatory optic neuropathy) in 20.9% (n = 335). Sixteen percent of patients (n = 263) were incorrect referrals. Conclusion: The neuro-ophthalmic clinic constitutes a significant referral unit in a tertiary eye care center in India. Traumatic and ischemic optic neuropathies are the most common diagnoses. Neuro-ophthalmology requires further development as a subspecialty in India to better serve the nation's population. Journal of Neuro-Ophthalmology 2018;38:308-311 doi: 10.1097/WNO.0000000000000586 © 2017 by North American Neuro-Ophthalmology Society Strabismus and Neuro-ophthalmology Services, Dr. R. P. Centre for Ophthalmic Sciences, All India Institute of Medical Sciences, New Delhi, India. The authors report no conflicts of interest. Address correspondence to Rohit Saxena, MD, PhD, Strabismus and Neuro-ophthalmology Services, Dr. R. P. Centre for Ophthalmic Sciences, All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110029, India; E-mail: [e-mail] 308 O nly a handful of neuro-ophthalmologists are practicing in India, a country of more than a billion people (1). There are a few institutions providing fellowship training in this field. The purpose of our study was to evaluate the clinical, demographic, and etiological profile of patients presenting to a neuro-ophthalmology clinic of a tertiary care center over a 1-year period to assess the need for enhancing this specialty in India. MATERIALS AND METHODS A retrospective hospital record-based study was conducted at Dr. Rajendra Prasad Centre for Ophthalmic Sciences, All India Institute of Medical Sciences, New Delhi, India, with a dedicated neuro-ophthalmology clinic, after prior approval from the institution's ethics committee. The diagnoses in the clinic were made by faculty trained in neuro-ophthalmology. Records of all cases seen over a 1-year period (January, 2015- December, 2015) were retrieved from the medical records section, and an excel sheet was populated. Demographic and clinical data collected included patient age, sex, presenting complaints, associated systemic illnesses, and neurological disorders. Results of ophthalmic examination were as follows: visual acuity, ocular motility, and appearance of the anterior and posterior segments. Reports of additional investigations were gathered. These included electrophysiological tests, perimetry, and neuroimaging (computed tomography and magnetic resonance imaging). Statistical analysis was performed using stata 11.0 (Stata Corp LP, College Station, TX) and missing data were excluded from the analysis. RESULTS A total of 31,111 patients were referred to various specialty clinics at our center in a span of 1 year. Of these, 1,597 (5%) were referred to the neuro-ophthalmology clinic. The mean age of presentation was 30.8 ± 19.5 years (range: 3 months-88 years). Male predominance was seen with Dhiman et al: J Neuro-Ophthalmol 2018; 38: 308-311 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution a ratio of 2.02 (1,069 vs 528). More than half of the patients (54%) were #30 years. Pediatric patients (age #16 years) constituted 27% of the entire cohort. Of 1,597 patients referred to the neuro-ophthalmology clinic, optic nerve disorders were seen in 63.8% (n = 1,020), cranial nerve palsies in 7% (n = 114), cortical visual impairment in 6.5% (n = 105), and other neuroopthalmologic abnormalities in 6% (n = 95). The last group is summarized in Table 1. Sixteen percent (n = 263) of patients were incorrect referrals including retinal dystrophy, maculopathy, cataract, and refractive error. Thus, a total of 1,334 valid neuro-ophthalmology cases were seen in our clinic in 1 year. Of the 1,020 patients with optic neuropathy, 67% (n = 635) presented without disc edema, whereas 33% (n = 335) had optic neuropathy with disc edema. Optic neuropathy without disc edema also was the commonest cause of pediatric referral to the clinic. Optic neuropathy without disc edema included traumatic optic neuropathy, hereditary optic neuropathy, tumor-related optic neuropathy, retrobulbar neuritis, toxic optic neuropathy, and optic neuropathy of unknown cause. The most common cause of optic neuropathy without disc edema was traumatic (27.7%; n = 190) (Table 2). The mean age of patients presenting with traumatic optic neuropathy was 24 ± 4.2 years (range: 1-66 years) with male:female ratio of 6.6. Various modes of trauma included road traffic accidents (n = 102), fall from height (n = 44), alleged assault (n = 15), blunt ocular trauma with a ball (n = 18), and penetrating ocular trauma (n = 11). Tumor-related optic neuropathy was most frequently caused by pituitary adenoma and meningioma (Table 3). These cases had a mean age of 30 ± 5.7 years (range: 9-67 years) with a male: female ratio of 1.34. Ethambutol toxicity while on anti-tubercular treatment (ATT) and methanol poisoning after consumption of adulterated alcohol were common forms of toxic optic neuropathy. The patients with ethambutol toxicity TABLE 1. Distribution of other neuro-ophthalmic disorders Disorder Blepharospasm/hemifacial spasm Optic disc anomalies Nystagmus Papillophlebitis Ophthalmoplegia Malingering Myasthenia gravis Neurocysticercosis Orbital apex syndrome/superior orbital fissure syndrome Unknown/ambyopia Total Dhiman et al: J Neuro-Ophthalmol 2018; 38: 308-311 No. of Patients 21 18 9 2 7 5 9 3 5 16 95 had a mean age of 56 ± 4.7 years with male: female ratio of 1.5. Methanol toxicity was seen only in male patients with a mean age group of 32 ± 5.3 years. Two pediatric patients with optic neuropathy without disc edema were associated with rare systemic conditions of Moyamoya disease and craniometaphyseal dysplasia. The child with craniometaphyseal dysplasia also had a 7th cranial nerve palsy. Optic neuropathy with disc edema included ischemic optic neuropathy, papilledema/postpapilledema optic atrophy, papillitis, neuroretinitis, and inflammatory optic neuropathy (Table 2). Of these, ischemia and papillitis were most often seen. Patients with papillitis had a younger mean age at presentation (32.5 ± 11.8 years) vs ischemic optic neuropathy where the mean age of presentation was higher (56.7 ± 13.6 years). Causes of papilledema/postpapilledema optic neuropathy included idiopathic intracranial hypertension (n = 35), intracranial tumor (n = 17), hydrocephalus (n = 14), cerebral venous sinus thrombosis (n = 7), aqueductal stenosis (n = 2), arteriovenous malformation (n = 2), and malignant hypertension (n = 1). A subanalysis was performed to evaluate eyes where early treatment or intervention could have potential benefit by preventing visual disability. These included eyes with traumatic optic neuropathy (n = 190), pituitary adenoma- associated optic neuropathy (n = 69), toxic optic neuropathy (n = 60), optic neuritis (n = 134), papilledema (n = 78), and inflammatory/infectious optic neuropathy (n = 10). This constitutes 549 eyes, which forms 54% of optic nerve disorders. The most common ocular motor cranial nerve palsy was the 6th nerve in 44% (n = 39) of patients. Other cranial nerves involved were the 3rd in 21.9% (n = 25), 4th in 20.1% (n = 23), facial nerve palsy in 14% cases (n = 16), trigeminal neuropathy in 4.4% (n = 5), and multiple cranial nerves in 5.2% cases (n = 6). Trauma (42%) and intracranial tumor (35%) were the most common causes associated with cranial nerve palsy. Out of 1,334 patients, visual fields were available in 7.8% (n = 104) and 97.6% of these showed some form of visual field defects. The most common field abnormalities were enlargement of the blind spot, hemianopia, and concentric constriction. Neuroimaging was available in 35.2% (n = 467) cases and showed some abnormality in 89.2% cases. DISCUSSION Neuro-ophthalmic disorders range from the manifestations of life-threatening intracranial or systemic disease to minor congenital anomalies. It remains the responsibility of clinicians to determine appropriate management, avoiding unnecessary investigations or treatment whenever possible. This requires reliable assessment and interpretation of clinical findings. In India, there is a need for trained neuro-ophthalmologists at tertiary eye care institutions and 309 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution TABLE 2. Distribution of optic nerve disorders in 1,020 patients Type of Optic Nerve Disorder No. of Patients (%) Optic neurotpathy without disc edema Traumatic Hereditary Tumor-related Toxic Postretrobulbar neuritis Idiopathic/unknown Optic neuropathy with disc edema Ischemic Postpapilloedema Postoptic neuritis (papillitis/neuroretinitis) Inflammatory/infectious Consecutive (postretinal/choroidal/uveal disease) Total 685 190 (27.7) 68 (9.9) 175 (25.5) 68 (9.9) 120 (17.5) 64 (9.3) 335 126 (37.6) 78 (23.2) 97 (28.9) 10 (2.9) 24 (7.2) 1,020 increased knowledge of the spectrum of neuro-ophthalmic disease among the general ophthalmologists at secondarylevel eye care clinics. With more than 50% of optic nerve diseases evaluated in our clinic being potentially treatable at an early stage to prevent vision loss, early diagnosis is of immense importance. Our study showed an incorrect referral rate of 16% as the neuro-ophthalmology clinic receives referrals from within as well as outside the Institute, made by the residents and faculty who may not be trained in neuroTABLE 3. Distribution of compressive/infiltrative causes of optic neuropathy Cause Pituitary adenoma Meningioma Craniopharyngioma Tuberculoma Others Mucocele of sphenoid sinus Aplastic anemia Hemangioblastoma CML ALL Astrocytoma NHL Thalamic glioma Glioblastoma Pheocromocytoma Cysts (sinuses and ventricles)/aneurysms Nasopharyngeal tumor CP angle epidermoid Neurofibromatosis Unknown Total No. of Patients 69 40 15 6 45 2 1 1 1 1 2 2 1 1 2 8 4 1 3 15 175 ALL, acute lymphocytic leukemia; CML, chronic myelogenous leukemia; CP, cerebellopontine; NHL, non-Hodgkin lymphoma. 310 ophthalmology. This further underscores the need to impart proper neuro-ophthalmology training at a basic level. In our study, 36% patients presented with visual acuity less than 20/200. Unfortunately, a large number of these patients reached the neuro-ophthalmology clinic late in the course of their disease and already had developed optic atrophy. This, too, is a reflection of very few neuro-ophthalmologists throughout secondary eye care institutions. Most patients referred to us were young. Although this may be related to some common problems including optic neuritis, trauma, and tumors presenting at a younger age, it also may be related to the overall younger general population, short life expecting, and difficulty of older patients to access health care at a tertiary level (2). Because of geographical, social and, economic reasons, women in India are less able to access the health care facilities. This may, in part, explain the skewed sex ratio noted in our study. Traumatic optic neuropathy was the most common cause of optic neuropathy without disc edema in our study. Road traffic accidents, especially driving a motorbike, were the most common mode of trauma. These data are in agreement with other reports (3-5). The incidence of traumatic optic neuropathy varies from 0.7% to 2.5% worldwide, with a higher incidence of 4.04% reported from India (6-10). The increase in economic growth in India coupled with the rise in population, motorization, and industrialization has contributed to a significant increase in road traffic accidents. With the enormous burden of tuberculosis in India, ethambutol toxicity was found to be the most common cause of toxic neuropathy in our study (11). Educating physicians about the potentially blinding side effect of ethambutol is essential. Also, because of the social stigma attached to tuberculosis in India, patients may not report treatment details to the ophthalmologist resulting in delay in diagnosis and irreversible vision loss. Dhiman et al: J Neuro-Ophthalmol 2018; 38: 308-311 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution In our patient cohort, neuroimaging was available in only 35% of patients with abnormalities detected in almost 90% of the studies performed. Neuroimaging is costly and with majority of our patients belonging to the lower socioeconomic strata and not covered by insurance, it is not possible to get such studies in all cases. Furthermore, the public health care system is overburdened, and only cases where neuroimaging seems essential to patient management are supported with subsidized costs. Similarly, visual fields were available in 8% of our patients. Nearly 50% of eyes reported in our study had a visual acuity worse than 20/200, and more than a fourth of the patients were pediatric. Clearly, this too is a major problem regarding patient access. In addition, we lack the electronic medical record system at our institution causing our retrospective study to have limited data with regard to visual fields. There are limitations of our report. Being retrospective, medical diagnoses occasionally were made based on the patient's history and not by strict assessment of medical data. Being a tertiary eye care center, the patients who were evaluated were subject to referral bias and may not be representative of those in the general population. In addition, the limitation is terms of availability of neuroimaging or laboratory testing, which implies that certain diagnosis could have been missed. In conclusion, the neuro-ophthalmic clinic constitutes a significant referral unit in a tertiary eye care center in India. It is essential that better education of neuroophthalmic disease be made available at a secondary eye Dhiman et al: J Neuro-Ophthalmol 2018; 38: 308-311 care level. In addition, we must increase the number and expertise of those practicing this subspecialty in our country. REFERENCES 1. Census of India 2011. Ministry of Home Affairs, Government of India. Age Structure and Marital Status. 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