The term “cerebral visual impairment” describes the loss of any visual function as a result of damage to the retrogeniculate visual pathway or the pathways of higher visual functions.1–3 Cerebral visual impairment has become the leading cause of visual impairment in developed countries, with a prevalence ranging from 16% to 45%.4,5
In India, studies report that common causes of childhood blindness are cataract, corneal opacities, refractive errors, retinal dystrophies, optic atrophy, globe anomalies, and glaucoma.6 Because the survival rate of premature infants and infants who had perinatal insult, metabolic disorders, or trauma is increasing, the number of children with cerebral visual impairment reporting to pediatric ophthalmologists is also increasing. Cerebral visual impairment is emerging as one of the most common causes of visual impairment in the country.7
The severity of cerebral visual impairment depends on the timing of the injury, the extent of the brain damage, and the underlying cause and mechanism of the damage. The assessment and treatment of children with cerebral visual impairment is challenging because their vision impairment may be associated with neurological deficits that affect their cognitive and motor abilities.3,8–10 Although numerous studies have described ophthalmic associations between cerebral palsy and developmental delay in patients with retinopathy of prematurity,11–13 few studies describe the associations in the subset of children specifically diagnosed as having cerebral visual impairment with no associated retinopathy of prematurity.
This study describes the predisposing factors and ophthalmic manifestations of children presenting with cerebral visual impairment at our tertiary eye institute. A knowledge of the etiological factors will help antenatal and perinatal health care providers plan early preventable measures during the antenatal and perinatal period. The various ophthalmic manifestations can help neurologists and rehabilitation teams understand the various types of visual impairment associated with cerebral visual impairment and plan effective treatment strategies for the neurodevelopment of the child.14
Patients and Methods
This was a retrospective cross-sectional analysis of all pediatric patients younger than 16 years diagnosed as having cerebral visual impairment from January 2014 to January 2018. Records of patients were compiled in a Microsoft Excel (Microsoft Corporation, Redmond, WA) spreadsheet. The study was approved by the institutional review board of Dr. Shroff's Charity Eye Hospital and followed protection of human rights.
Cerebral visual impairment was defined as visual impairment due to retrogeniculate visual pathway pathology determined by clinical assessment and neuroradiological evidence. Patients with significant ocular pathologies affecting their vision (ie, retinopathy of prematurity) or without neuroimaging evidence of retrogeniculate pathway pathology were excluded from the current study. A detailed history and ophthalmic examination of all patients was documented and analyzed. This included the child's presenting complaint or visual behavior, any significant antenatal history, term or preterm birth, perinatal or postnatal complications, and history of neurological deficits. Significant antenatal history was defined as any systemic abnormality occurring in the mother of the child suffering from cerebral visual impairment from the time of conception until delivery, which is known to adversely affect the fetus. The period between 28 weeks' gestational age and 7 days after birth was considered the perinatal period. Where adequate history could be attained, the etiology of cerebral visual impairment was classified into antenatal, perinatal, or acquired causes. The presence of developmental delay (ie, motor and cognitive milestones) and cerebral palsy was charted wherever mentioned. The magnetic resonance imaging (MRI) findings were noted in terms of the involved area of the brain and the type of injury to the involved area.
Data on ophthalmological evaluation included vision assessment at presentation, accommodation abnormality, ocular alignment, extraocular motility binocular status, and anterior and posterior segment evaluations. An assessment of visual acuity for distance and near was performed using methods appropriate for the developmental age of the child, with multiple and single optotypes in a line. The tests included Teller acuity cards, Lea paddles, Lea symbols, and any routine logarithm of the minimum angle of resolution acuity chart. Refractive errors were determined using cycloplegic retinoscopy and non-cycloplegic retinoscopy (Mohindras technique). Cycloplegic refraction was performed with topical atropine 1% for children younger than 5 years or children with strabismus. Topical homatropine 2% was used in children older than 5 years. To assess accommodation, dynamic retinoscopy was performed and lead or lag was documented. The monocular estimation method was used. Any value +0.75 diopters (D) in near retinoscopy (after giving full correction for distance) was recorded as a lag in accommodation. Conversely, any value greater than −0.25 D was recorded as a lead in accommodation. Torch light, slit-lamp examination (wherever performed), and fundus findings were noted to rule out unrelated ocular pathology. A detailed evaluation of strabismus and nystagmus, if noted in the files, was documented. The findings of visual field analysis were noted, irrespective of the method of evaluation (confrontation or Humphrey's visual field).
The files of 256 patients younger than 16 years with cerebral visual impairment were analyzed. Of these, 88 patients met the inclusion criteria of neuroradiological evidence of retrogeniculate pathway pathology. Fifty-eight (65.90%) patients were male. The age at presentation ranged between 1 and 180 months, with a mean and median age of 47.53 and 32 months, respectively.
Antenatal. A significant antenatal history was present in 25% of patients, and the most common was gestational hypertension (20% of patients).
Perinatal. A history of preterm delivery was present in 37.5% of patients. In the preterm group, 60.60% patients were born between 34 and 37 weeks and 3 (9%) children were born before 30 weeks' gestational age. A cesarean section was performed for 44.3% of children and 3 children were delivered by assisted forceps, where the risk of peri-natal trauma may not be ruled out. Seventy-four percent of the cesarean sections were performed due to perinatal complications, including intrauterine growth retardation, fetal distress, oligohydramnios, preeclampsia, abnormal presentation, abruptio placentae, meconium aspiration, twin delivery, and premature rupture of membranes. Ninety-one percent of patients had an eventful perinatal period, with low birth weight in 50%, delayed cry in 53.4%, neonatal intensive care unit admission for a mean duration of 16.98 days in 75%, history of oxygen therapy in 60.4%, high grade fever in 10.22%, perinatal seizures in 44.8%, sepsis in 18.2%, feeding difficulties in 31.81%, significant jaundice requiring phototherapy in 12.50%, hypoglycemia in 11.36%, hydrocephalus in 4.5%, and birth trauma (vacuum-assisted delivery or forceps delivery) in 6.8%. A positive history of the first episode of seizures after the perinatal period was present in 12.5% of patients.
Postneonatal. Infectious causes and meningitis were suspected as the cause of cerebral visual impairment in 12.5% of children. Systemic associations were present in 85.2% of patients, and the most common was global developmental delay (22.7%) followed by cerebral palsy (19.3%). Other associations included West syndrome, blood disorders, epilepsy, Angelman's syndrome, liver disorders, vasculitis, congenital heart defects, and infant respiratory distress syndrome.
Based on the risk factors, the most common underlying mechanism was perinatal hypoxia (recorded in 40.90% of patients), followed by seizure disorder (35.22%). The other etiological factors were prematurity, infections, and hypoglycemia in 27.26%, 20.45%, and 19.31% of patients, respectively (Figure 1).
The distribution of risk factors of cerebral visual impairment.
MRI Localization of Lesion
The parietal lobe was involved in 50% of patients and the posterior parietal lobe with sparing the anterior part was observed in only 2 patients. The occipital lobe was affected in 40.90%, the frontal lobe was involved in 14.77%, and the temporal lobe was involved in 7.95% of patients. The periventricular region was affected in 39.77% of patients. Thinning of the corpus callosum was noted in 18.18% of patients. The perirolandic area is the area surrounding the central sulcus. Because it is a watershed zone for vascularization, it is prone to damage in patients with perinatal hypoxia. In the current study, it was involved in 5.68% of patients. Ten patients (11.36%) had non-specific atrophic or ischemic changes, as reported by radiologists, wherein no specific region was mentioned. The type of damage was described in the MRI reports of 74 of 88 patients, so only these 74 patients were analyzed. The damage was reported as encephalomalacia in 22.97%, ischemia in 30.68%, gliotic in 20.45%, atrophic in 5.68%, demyelinating in 4.54%, and hemorrhagic in 2.27% of patients.
Visual Behavior. The parents described a variety of complaints, the most common being “poor or no eye to eye contact” (57.95%). Of these, 7 children had no visual response and 4 children had a poor attention span. The second most common complaint was “squinting of eyes” (40%). Decreased vision (31.8%) and poor hand–eye coordination (13.6%) were noted. Other presenting complaints included “keeping eyes in a particular gaze” (10.2%), “to and fro eye movements” (9.0%), “routine ophthalmic evaluation as advised by a pediatrician” (5%), “frequent falling” (3.4%), “maintaining a head posture” (2.2%), and “difficulty in focusing” (1.1%).
Visual acuity assessment was recorded for all 88 children and summarized in Figure 2. Three children (3.40%) showed no response to bright light. Fifteen children (17.04%) had normal visual acuity. Thirteen children (14.77%) showed non-specific response to light. Fixing and following of light was seen in 24 children (27.27%). Visual acuity of 20/400 or better or following unilluminated bright objects was present in 15 children (17.04%), whereas a visual acuity between 20/400 and 20/200 was recorded in 7 children (7.95%). Eleven children (12.5%) had a visual acuity between 20/200 and 20/50 (Figure 2).
The distribution of visual acuity (VA) in children with cerebral visual impairment. The x-axis represents number of children and y-axis shows the assessed visual acuity.
Refractive Error. On evaluation of cycloplegic refraction of the 196 eyes of 88 children, simple myopia was more predominant than hyperopia (54.54% myopic eyes vs 22.72% hyperopic eyes). Only 15.91% of eyes were found to be emmetropic and 4.5% of eyes had mixed astigmatism. The most common refractive error encountered was simple myopic astigmatism in 27.8% of patients (Table 1). Myopia ranged up to −9.25 diopters sphere, whereas only moderate levels of hyperopia were found with a maximum of 5.25 diopters sphere.
Frequencies of the Types of Refractive Errors in Children With CVI
Accommodation Anomalies. An assessment of accommodative anomalies (by dynamic retinoscopy, monocular estimation method) was performed in 34 children, due to poor fixation in others. It was not recorded in 28 patients where it could have been attempted. Of the 34 children, 4 showed a lag in accommodation and 2 showed a lead in accommodation.
Strabismus and Ocular Motility. Motor evaluation revealed strabismus in 59 patients (67.04%). Exotropia was observed in 34 patients (57.62%) and esotropia was observed in 29 patients (49.15%). On further assessment, the deviation was variable in 7 patients (5 patients with esotropia and 2 patients with exotropia), intermittent in 6 patients (3 patients with esotropia and 3 patients with exotropia), and constant in the remaining 46 patients. The deviation was measured in 21 patients. The mean angle of deviation was 30.05 prism diopters for esotropia and 33.33 prism diopters for exotropia. An associated manifest disassociated vertical deviation was present in 8 patients and 2 patients had latent disassociated vertical deviation. Surgery for strabismus was performed in 8 patients (5 patients with esotropia and 3 patients with exotropia).
Of 88 patients, 39 (44.31%) had nystagmus and 2 (2.27%) had non-rhythmic oscillation of the eyes. The nystagmus was manifest in 20 patients (51.28%), latent in 10 patients (25.64%), and latent manifest in 9 patients (23.09%). Records showed that visually evoked potentials were performed in 45 patients. The latency was increased in 28 patients and the amplitude was reduced in 25 patients. Extinguished visually evoked potentials were observed in one patient. Amplitude was variable in one patient.
Fundus. Disc pallor was present in 53 of 88 children (60.22%) and further categorized as temporal pallor in 28 patients (52.83%) and diffuse pallor in 25 patients (47.16%). One patient had a discrepancy in the degree of pallor between the eyes (ie, temporal pallor in the right eye and diffuse optic disc pallor in left the eye).
Visual Fields. Visual fields were not recorded in 31 children and were not possible due to poor vision in 37 children. Of the 20 children in whom visual fields were performed, they were normal in 17 children and revealed inferior field defects in 3 children.
Cerebral visual impairment is becoming a primary cause of visual impairment in the developing world, after being the leading cause of poor vision in children in the developed world.1,15,16 With the advent of better perinatal care, the etiological spectrum of cerebral visual impairment has greatly widened. Literature on cerebral visual impairment is sparse, especially in the developing world. Besides having poor visual acuity, cerebral visual impairment more commonly affects the functional vision of the child, thus interfering with the overall mental and physical development. This makes its diagnosis in early childhood prudent for better holistic growth and rehabilitation of affected children.
As previously observed, our study reinforced the fact that boys are more commonly affected than girls.1 Our study reports a similar age of presentation in comparison to other studies.7,17 Also, a remarkable association of gestational hypertension with cerebral visual impairment has been established in our study.18 Based on the risk factors, the most common underlying mechanism was perinatal hypoxia because it was recorded in 40.90% of patients, followed by seizure disorder in 35.22% of patients. The other etiological factors were prematurity, infections, and hypoglycemia in 27.26%, 20.45%, and 19.31% of patients, respectively.
Compared to other studies, the incidence of hydrocephalus, encephalitis, and meningitis (as a cause of cerebral visual impairment) was markedly less in our study.1,19–21 This could be rationalized by the assumption that, despite improvements in generalized perinatal care, early diagnosis and prompt treatment of these conditions may still not be as advanced in our country as compared to western countries. Because the optic radiations and corticospinal tract pass through the periventricular white matter, periventricular leukomalacia is closely associated with cerebral visual impairment and cerebral palsy.22 In our study, associated cerebral palsy was present in 30% of cases. Being the watershed zone, involvement of the periventricular area is the most common cause of cerebral visual impairment in preterm infants. However, in our study, periventricular leukomalacia was equally associated with term and preterm births (17% vs 18%). Pfiefer et al.22 and Hoyt and Fredrick23 stated a higher incidence of subcortical damage in preterm infants, whereas 4 of 30 preterm children in the current study showed evidence of subcortical damage and another 4 children had a combination of both cortical and subcortical brain damage.
Another observation in the current study was strabismus as the second most commonly presented complaint. This could infer that, besides children who have profoundly low vision (most common presentation), visual impairment would be grossly underdiagnosed were it not for a manifest strabismus that can be easily noticed by the parents. Children without strabismus or damaged functional vision might not report to an ophthalmologist until a later age.24
Refractive errors in children with cerebral visual impairment have not been extensively analyzed. Refractive errors and accommodative anomalies are common in cerebral visual impairment.25 Glasses should be optimally prescribed after retinoscopy and the evaluation of lead or lag in accommodation. Huo et al.8 found a significant refractive error (> 3.00 diopters of hyperopia or myopia) in their patients in only 8.24% of their cases. The incidence of refractive errors was much higher in our study, with myopia being more common. Accommodative anomalies may lead to a variable angle of deviation (7 patients in our study). Such patients should receive an optimal glasses prescription for the correction of near vision and should be evaluated multiple times before planning surgery for strabismus. The incidence of nystagmus in our study is in concurrence with other studies.8,23,26
Our study was limited by the fact that we could not analyze the contrast sensitivity, saccades, and pursuits and color vision in children with cerebral visual impairment. The lack of appropriate instrumentation and poor cooperation levels in a larger proportion of our sample restricted our study. However, we should remember that these factors could also be grossly affected in cerebral visual impairment and should not be missed during evaluation. Also, a long-term follow-up after rehabilitation for functional vision with guided therapy is required to comment on the overall prognosis of these children.
This is a descriptive study in which we emphasized the importance of the etiological factors that cause cerebral visual impairment in the antenatal and perinatal period. During assessment of any child with visual impairment or neurodevelopmental delay, these factors should be looked for. The various ophthalmic manifestations could guide the multidisciplinary team treating the child with cerebral visual impairment to understand the various types of visual impairment that affect the neurodevelopment of the child and plan rehabilitation strategies accordingly.14 However, a larger sample size and a multicentric study in the future may be a better reflection of the same.
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Frequencies of the Types of Refractive Errors in Children With CVIa
|Refractive Error||No. of Eyes||%|
|Simple myopic astigmatism||49||29.87|
|Compound myopic astigmatism||39||23.78|
|Simple hyperopic astigmatism||21||12.80|
|Compound hyperopic astigmatism||14||8.53|