Children born preterm

Children born preterm are at risk of brain injury, with periventricular leukomalacia (PVL), the most common brain lesion. Those who avoid major motor impairment are well known to be at risk of adverse developmental outcomes, including, for example, cognitive difficulty of variable degree, impairments in attention and executive function5 ,6. It is less commonly recognised that they are also at risk of visual or ocular abnormalities. VI in children born preterm has been reported in between 1% and 3% with causes including cerebral VI and retinopathy of prematurity (ROP).7 Refractive errors have also been found to be four times more common in those born preterm (29.6%) than those born at term (7.8%)8 (table 1). These visual disorders result from both the ‘premature exteriorisation’ of the developing visual system and from the systemic complications of preterm birth.7

Holmström et al9 recently reported from a population-based follow-up study of 411 children born at <27 weeks’ gestation, with only a minority having CP at 30 months’ corrected age. Overall, a third had some type of eye or visual problem, most frequent in children previously treated for ROP (table 2).

Although hypermetropia is the most common refractive error in childhood, myopia is more common in those born preterm, occurring both in those with and without previous ROP. In those with strabismus, esotropia and exotropia are equally common, in contrast to full-term children in whom esotropia is three times as common as exotropia.7

Difficulties with higher-order processing of visual information may also occur and some authors have particularly highlighted the occurrence of such difficulties in children with PVL. Hard et al16 reported poor visual perceptual skills in almost half of a group of 51 children born before 29 weeks’ gestation, only 6% of whom had PVL. Pagliano et al17 studied 24 children with spastic diplegia and PVL, 15 born prematurely and 9 at term. Those born preterm had poorer visual perceptual skills, suggesting that the PVL was not the key factor, but some other consequence of prematurity.

Children with CP

Premature birth and its sequelae are common precursors to CP and overlap exists between these two groups. Other causes of CP, including term hypoxic ischaemic encephalopathy, early brain malformations and congenital or postnatal infections, will also contribute to visual outcomes.

Data from UK and European CP registers indicate that up to 11% of children with CP are found to have SVI (acuity <6/60).12 ,18 A retrospective case series of 92 children with spastic quadriplegia from a single centre in Canada reported 20% with ‘blindness’19 (not further defined).

A higher incidence of visual difficulties is generally seen in those with more severe motor impairment.20–22 However, visual difficulties are neither restricted to a single neurological or aetiological subtype of CP nor to acuity loss.20 ,21 ,23

Ocular disorders including refractive error, strabismus and minor ocular abnormalities, not associated with significantly reduced acuity, also increased13 (table 2).

Very marked abnormalities of eye movement have also been found in children with CP, some of whom may have been previously described as ‘blind’.24 ,25 Lesser degrees of oculomotor difficulty affecting both smooth pursuit and saccades have been described in children with all distributions of CP26 .

Children with CP can therefore be described as showing a range of neuro-ophthalmological abnormalities (reduced acuity, refractive errors, strabismus, oculomotor abnormalities and field alterations), which may be predictable according to the distribution of the motor impairment.26

Children with PVL have also been found to have visuoperceptual difficulties that were not explained by acuity or cognitive impairments.27 ,28 These included weakness in visual object recognition, visuospatial skills, visual memory and oculomotor control.

Impairments of visual attention in children with CP have been described using a variety of terms, including ‘fixation impersistence’, ‘abnormal fixation’, ‘variable performance’ and ‘gaze dysfunction’.22 ,29 ,30 A complex relationship between visual attention, visuoperceptual difficulties and eye movements may exist. Children with very severe attentional difficulties are at risk of being misdiagnosed as ‘blind’ as they may not be able to achieve or maintain fixation during vision testing.

Visual outcomes following brain injury

Visual difficulty occurring in the context of a normal ocular exam is now generally termed cerebral (previously cortical) visual impairment (CVI). A number of different definitions of CVI exist,31 but most make reference to three criteria, namely a normal ocular examination, reduced visual acuity or subnormal visual performance and evidence of damage to the posterior visual pathways. While definitions are being clarified, it may be helpful to consider CVI as a ‘spectrum’ condition, in which not all possible consequences may manifest in each individual child or at all ages, for example, some aspects of perceptual dysfunction can only be identified in school-aged children.27 It is also important to appreciate the other non-visual factors that can affect overall visual performance especially in very young children, such as cognitive or social impairment or positioning difficulties in children with severe movement difficulty.

Some children who experience brain injury show marked abnormalities of visual performance in the first year of life, which lessen over time. While improvement in visual function has been described as a characteristic of CVI, it is possible that for some children this may simply reflect a slower than normal maturation of the visual system.

Children with learning difficulty

Several studies have reported an increased risk of VI in children with learning disability (LD).3 ,10 ,32 One of the most comprehensive population-based studies of children with borderline to profound learning difficulty, aged 4–15 years, found that the prevalence of VI was as much as 10 times higher than that described in general population-based studies10 (table 2).

The most common aetiologies of VI in studies of children with additional learning difficulties were CVI, optic atrophy, retinal dystrophies and congenital nystagmus.10 This is in line with the most common disorders described in the general population of children with VI.1

Other more minor and potentially correctable visual disorders such as refractive disorders and strabismus also occur at higher frequency in children with LD (table 2)14 ,32.

In children with LD, the prevalence of strabismus is most commonly reported to be between 21% and 27% (table 2) compared with up to 4% in typically developing children.15 Refractive errors and strabismus have also been found to be correlated with low IQ.14

Ophthalmological pathology has also been reported in 40% of patients with autism or related disorders, with 29% having significant refractive errors, 21% strabismus and 10% amblyopia.33

Down syndrome

Trisomy 21 is one of the most common genetic disorders of childhood, and children with this disorder are at high risk of additional ocular disorders including refractive errors, reduced accommodation, strabismus, blepharitis, nasolacrimal duct problems, cataracts, congenital or acquired and keratoconus.11 ,34

Maturation of acuity is often slower than in typically developing children and many children have slightly reduced visual acuity even when refractive errors are appropriately corrected.35 There is also a high prevalence of strabismus among children with Down syndrome, independent of refractive error36 (table 2).

Underaccommodation has also been found to be a substantial problem even when there is no, or a fully corrected, refractive error. This has important implications because near vision will be consistently out of focus for these children. Woodhouse has shown that children can benefit from provision of bifocal spectacles to compensate for poor accommodation.37

Children with severe hearing impairment

Congenital rubella syndrome was previously the most common cause of dual sensory impairment in UK children but is now rare. Other congenital infections due to other infectious agents may have similar consequences.38

CHARGE association, a genetic condition, is now the most common congenital cause of dual sensory impairment.38 VI arises from ocular coloboma and is variable in degree. In severe cases, the eye can be rudimentary or anophthalmic; however, involvement is often asymmetrical. Retinal coloboma will also affect the visual field and will lead to severe acuity impairment if the macula or optic disc is affected. There is also an increased risk of retinal detachment and of corneal injury if there is incomplete eye closure.

Children with dual sensory impairment of any cause should undergo very careful evaluation of each sense.

Primary visual impairment leading to disability

Vision integrates all other senses and therefore it is not surprising that SVI is known to constrain all areas of development in the early years of life. This is directly related to the level of vision loss (box 1).4

Development can be delayed by as much as 2 years in the first years of life and therefore specific developmental norms are available for children who are ‘blind’ and ‘partially sighted’.39 These delays can be overcome by the time children reach school age.

However, in children with profound VI (awareness of light or light-reflecting objects only) research has found that approximately 30% of children are at risk of stasis or regression in cognitive development during the second year of life.4 Disordered social communication is most prominent in this group and the high level of autistic spectrum disorder in children who are blind is increasingly well recognised. This outcome is found even in children who have a primary visual disorder with no other obvious risk factors for brain vulnerability. It may be that there are as yet unknown genetic factors that contribute, but it seems likely that sensory deprivation plays a significant role in this serious developmental disorder.

Approach to identification of ocular or visual difficulty

Paediatric assessment of a child with disability should always include an ocular and visual assessment. Box 2 outlines a systematic approach. Potential visual difficulties can be identified through careful history taking (table 3), observation for ocular anomalies, eye movement difficulty (squint, nystagmus) or atypical visual performance. Assessment of fixing and following and near detection can be carried out in the clinic. Acuity can also be measured if tools are available (table 1).

Assessment of the child with disability should follow the same principles as that of any child, but adaptations may be necessary to take account of the child's developmental age and capacity to cooperate with more formal assessment. Therefore, knowledge of a child's developmental level is essential.

Children with severe physical disability may require adaptations to test administration and the preceding history should elicit descriptions of their usual response methods. A child must be comfortable and adequately positioned if optimal responses are to be elicited. Multidisciplinary assessment is helpful in building up a detailed picture of the impact of non-visual factors on the child's overall visual profile. An important principle of assessment is to gather information and objective observations before considering all possible explanations, both visual and non-visual, for the information gathered.

Any identified difficulty should prompt early referral to the eye clinic for more detailed ophthalmological examination including refraction, behavioural observations and acuity measurement with electrophysiology (measuring the integrity of the retina and visual pathways) where indicated. MRI may also assist in understanding the potential structural correlates of visual function as well as the pattern of additional impairments or antecedent medical history.

If SVI is identified, a referral to the local Specialist Teaching team for children with VI should also be made. It is not necessary to wait for diagnostic confirmation if paediatric assessment indicates that severe visual difficulty is present.

History taking

Assessment always begins here and incorporates exploration of the current questions and concerns as well as detailed descriptions of the child's current visual skills. In some situations, the responses of children with additional disabilities may be interpreted according to hope, and beliefs about skills that may be based on an incomplete understanding of information received. For example, parents may previously have been told that their child's eyes are ‘normal’ leading to a belief that this guarantees normal vision. Careful enquiry as to whether the child's visual responses are predictable or variable and possibly dependent on other sensory modalities is vital, for example, is the child seeing or relying on hearing to respond to the stimulus.

Questionnaire approaches

To overcome some of the potential challenges of visual assessment in children with severe movement or other developmental difficulties, some authors have explored the usefulness of structured questionnaires. McCulloch et al41 developed a questionnaire to clarify visual skills in neurologically impaired children likely to have profound VI. Ferziger et al42 developed a questionnaire designed to document evidence of basic visual skills in children with multiple disabilities. Questionnaires to elicit possible manifestations of CVI have also been developed for use with children whose acuity is 6/60 or better.43 However, it is important to appreciate that the role of some tools is to identify children who would benefit from further detailed history taking and assessment44 and that some ‘screening’ questions may yield false positives45 since some reported responses may be explained by other aspects of the child's disability.

Service provision

To meet the visual needs of children with disability, stronger links are needed between child development and community paediatric services, ophthalmology and specialist education services for children with VI. Some districts have a team with a special interest in vision who provide joint assessments and support links between all these services. The team may comprise a paediatrician, orthoptist, ophthalmologist (or have close links with a named ophthalmologist) and a qualified teacher for children with VI.

Some tertiary centres provide specialist assessment for children with VI. They can address questions that may be more challenging for local teams such as developmental questions in children with profound VI. Clinical judgements about this rare group of children require a breadth of experience that cannot usually be gained at secondary level.

Current practice: surveillance for children with disability at increased risk of ocular and visual disorders

Hall and Elliman47 state the need for visual assessment of children with neurological impairment/CP, but in practice, assessment may be haphazard and abnormalities, which may in some children be severe, can be missed.2 ,48 ,49

Studies of children with special needs have established that there are significant unmet visual needs in a high proportion of children, with one study reporting a fifth with SVI (legal blindness) who were undiagnosed.3 Woodhouse recently reported that half of a cohort of children attending special schools had refractive errors warranting new or first-time spectacle prescription.2 These studies highlight the high level of potential unmet visual need in children with disabilities.

Although the full range of ocular and visual outcomes for children with learning difficulty, CP and other children with disability or at high risk of poor visual outcomes is well described in the literature, there are few agreed guidelines for routine assessment. School-based examination of children in specialist education has been recommended,2 but local practice varies widely in the UK. For children with Down syndrome, clear guidelines have been published recommending monitoring for the onset of significant refractive errors and for strabismus regularly throughout early childhood. However, adherence to recommendations is variable.50 ,51

How can practice be improved?

Closer working between professionals involved primarily in ocular and vision health and those working with children with disability would facilitate adherence to current guidelines and support identification of VI and potentially correctable vision difficulties in children who are known to be at high risk. In some child development teams (CDT), closer working is facilitated by an orthoptist working with the team. However, currently less than one-fifth of CDT have an orthoptist within the CDT (J Parr, personal communication, 2014).52

Guidelines need to include routine ophthalmological assessment for children with severe hearing impairment and for those with severe physical disability who are highly dependent on active use of vision to support their communication and learning.38 In addition, children with primary VI are at high risk of developing subsequent additional disability and therefore need intensive support and monitoring of development. The presence of even limited form vision appears protective, therefore visual promotion and support for families as early as possible is critical.4

Future developments

Vision is arguably the most important sensory modality underpinning child development and multiple professionals currently contribute to assessment of ocular structure and function and management of pathology. Assessment of vision itself can somehow be overlooked or at least not fully reported particularly in children with established disability. By contrast, children with suspected hearing impairment undergo dedicated and often repeated assessment of hearing by professionals whose specialism is audiology. While it may not be practical or even necessary to envisage a new speciality of ‘visuology’, the multidisciplinary team, with the paediatrician at the centre, can nevertheless work more closely together to confirm the importance of detailed visual assessment that ‘measures’ acuity and assesses other vital aspects of ocular function and visual skill, and also provides practical, tailored guidance for the individual child.