Only 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.
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 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 neuro-opthalmologic 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 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.
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 increased knowledge of the spectrum of neuro-ophthalmic disease among the general ophthalmologists at secondary-level 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 neuro-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.
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 neuro-ophthalmic disease be made available at a secondary eye care level. In addition, we must increase the number and expertise of those practicing this subspecialty in our country.
1. Census of India 2011. Ministry of Home Affairs, Government of India. Age Structure and Marital Status. Table of Population Indifferent Age Groups and Their Proportion of Total Age Group, 2011. Available at: censusindia.gov.in/Census_And_You/age_structure_and_marital_status.aspx
. Accessed October 10, 2017.
2. Nair AG, Gandhi RA. Neuro-ophthalmology in India: the way forward. Indian J Ophthalmol. 2014;62:980–981.
3. Lee V, Ford RL, Xing W, Bunce C, Foot B. Surveillance of traumatic optic neuropathy in the UK. Eye. 2010;24:240–250.
4. Levin LA, Beck RW, Joseph MP, Seiff S, Kraker R. The treatment of traumatic optic neuropathy: the International Optic Nerve Trauma Study. Ophthalmology. 1999;106:1268–1277.
5. Mahapatra AK, Tandon DA. Traumatic optic neuropathy in children: a prospective study. Pediatr Neurosurg. 1993;19:34–39.
6. Cockerham GC, Goodrich GL, Weichel ED, Orcutt JC, Rizzo JF, Bower KS, Schuchard RA. Eye and visual function in traumatic brain injury. J Rehabil Res Dev. 2009;46:811–818.
7. Edmund J, Godtfredson E. Unilateral optic atrophy following head injury. Acta Ophthalmol (Copenh). 1963;41:693–697.
8. Nau HE, Gerhad L, Focrster M, Nahser HC, Reinhardt V, Joka T. Optic nerve trauma: clinical, electrophysiological and histological remarks. Acta Neurochir (Wien). 1989;89:16–27.
9. Pirouzmand F. Epidemiological trends of traumatic optic nerve injuries in the largest Canadian adult trauma center. J Craniofac Surg. 2012;23:516–520.
10. Sharma B, Gupta R, Anand R, Ingle R. Ocular manifestations of head injury and incidence of post-traumatic ocular motor nerve involvement in cases of head injury: a clinical review. Int Ophthalmol. 2014;34:893–900.
11. Global Tuberculosis Report. Annex 2: Country Profiles, 2015. Available at: http://www.who.int/tb/publications/global_reports/en/
. Accessed October 10, 2017.