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Assessing strabismus in children
SYMPOSIUM: EYES AND ENT
Assessing strabismus in children
neurodevelopmental or neurological disorders) are maternal smoking beyond the first trimester, low birth weight for gestational age and sex, maternal ill health during pregnancy and perinatal and neonatal illnesses. In children with strabismus, convergent squints (esotropia, occur in 60.1%) are more common than divergent squints (exotropia, occur in 32.7%), with fully accommodative esotropias occurring the most frequently.
Tejaswi Bommireddy Kate Taylor Michael Patrick Clarke
Causes of strabismus
Abstract
Some of the primary and secondary causes of strabismus are outlined in Table 1. Primary strabismus may be idiopathic or congenital, however there known factors that can increase the likelihood of developing strabismus. Strabismus can be secondary to various pathologies. One important secondary cause which leads to sensory strabismus is poor visual acuity (unilateral or bilateral). This results in amblyopia and subsequent ocular deviation of the affected eye. Strabismus can itself cause amblyopia of the deviated eye. Other secondary causes of strabismus include children with pre-existing neurodevelopmental disorders, craniofacial syndromes, congenital abnormalities in extra-ocular muscles or their innervation and disorders affecting extra-ocular muscles or their innervation. Intracranial pathologies can cause cranial nerve III, IV and VI palsies; these present with reduced ocular motility and incomitant squints.
Strabismus, also known as a squint, is an ocular misalignment. In the UK the prevalence of strabismus in children is 2.1%. There are multiple causes of strabismus in children; some of which can be sinister and are potentially eye or life threatening. Therefore it is essential that strabismus is identified and managed appropriately and in a timely manner. Amblyopia is frequently associated with strabismus, and can be a cause or a complication of strabismus, it needs to be recognized and treated early to prevent a permanent reduction in visual acuity. This article explains how to correctly assess strabismus in children. A detailed history should be taken, and an ocular examination should be performed using the correct techniques and ocular motility tests. The important red flag features of strabismus in children are also outlined in this article.
Keywords amblyopia; child; eye; eye movements; ophthalmology; strabismus; visual acuity
What is strabismus?
Summary of the causes of strabismus in children2
Strabismus, more commonly known as a squint, occurs when there is a misalignment of the eyes. Pseudostrabismus, or pseudosquint, can also present giving the impression that the eyes are misaligned, however no true strabismus is present. Pseudostrabismus occurs more commonly in children with a broad nasal bridge and prominent nasal epicanthic folds, close set eyes, and eyelid asymmetry.
Causes of strabismus
Examples
Primary cause
Idiopathic Congenital Refractive error Amblyopia Cataract Retinoblastoma Optic neuropathy Optic nerve tumours such as gliomas Cerebral palsy Downs syndrome Foetal alcohol syndrome Developmental delay Craniosynostosis Crouzon’s syndrome Apert’s syndrome Brown’s syndrome Duane’s syndrome Cranial nerve III, IV, VI palsies Intracranial tumours Hydrocephalus Head trauma Myaesthenia gravis Thyroid eye disease
Poor visual acuity (unilateral or bilateral)
Epidemiology of strabismus The onset of strabismus is mostly before the age of 5 years. In the UK the prevalence of childhood strabismus in children is 2.1%, of which 90% have an isolated strabismus. Various factors such as prematurity, low birth weight, intrapartum complications, assisted or caesarean delivery and neonatal ill health in the first week of life increase the risk of isolated strabismus. The risk factors for neurodevelopmental strabismus (associated with
Neurodevelopmental disorders
Craniofacial syndromes
Abnormalities in extra-ocular muscles or their innervation Disorders affecting extra-ocular muscles or their innervation
Tejaswi Bommireddy MBChB, Ophthalmology Specialist Trainee, Newcastle Eye Centre, Royal Victoria Infirmary, Newcastle, UK. Conflicts of interest: none declared. Kate Taylor BSc, Deputy Head Orthoptist, Newcastle Eye Centre, Royal Victoria Infirmary, Newcastle, UK. Conflicts of interest: none declared. Michael Patrick Clarke MA MB BChir DO FRCS FRCOphth PhD, Consultant Ophthalmologist, Newcastle Eye Centre, Royal Victoria Infirmary, Newcastle, UK. Conflicts of interest: none declared.
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Table 1
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Please cite this article as: Bommireddy T et al., Assessing strabismus in children, Paediatrics and Child Health, https://doi.org/10.1016/ j.paed.2019.10.003
SYMPOSIUM: EYES AND ENT
Onset of strabismus-age of onset (congenital or acquired) and nature of onset (sudden or gradual). Symptoms-enquire about associated symptoms such as headache, vomiting, diplopia (more common in adults than children as suppression is present in children), the variability of strabismus and the psychosocial impact of strabismus. Past medical history including birth history-neurodevelopmental, neurological and systemic conditions can cause secondary strabismus. A birth history can identify risk factors for developing strabismus such as intrapartum problems, prematurity, birth weight, health during the neonatal period and trauma during birth. Past ocular history-enquire about the presence of a refractive error and whether glasses are worn. It is also important to note any previous ocular surgery such as squint surgery or previous treatment for amblyopia. Family history-there is a strong familial association with strabismus and around 30% have other family members with strabismus.1 Family members should be asked if they had any previous treatment or surgery to correct strabismus.
Classifying strabismus Strabismus is classified using various terms. Classifications include the age of onset of the strabismus (congenital or acquired), the fusional status (manifest or latent), when present (intermittent or constant), the laterality (unilateral or alternating), variation with gaze position (comitant or incomitant), the direction of the deviation (horizontal, vertical or cyclotortional), and the relation to accommodation (accommodative or non-accommodative). Table 2 defines the terminology.
History taking History taking is important in the assessment of strabismus as it helps to formulate the differential diagnoses and identify any red flags. These are some key areas that should be identified:
The classification of strabismus2,3 Classification
Definition
Congenital/infantile Acquired
Onset of strabismus less than 6 month of age Onset of strabismus greater than 6 months of age Manifest A tropia is seen when no fusional control is present. There is a deviation of one eye whilst the other eye takes up fixation Latent Fusional control is present with normal ocular alignment, but a phoria is seen when the binocularity of vision is interrupted Constant An ocular misalignment present all the time Intermittent Fluctuation in the presence of an ocular misaligment, can be worse towards the end of the day or with fatigue Unilateral Strabismus present in one eye Alternating Either eye can take up fixation and the laterality of the strabismus can vary Comitant The ocular deviation can be seen in all directions of gaze by an equal amount Incomitant The ocular deviation varies depending on the direction of gaze, a limitation or restriction in ocular movement may be present indicating a neurological, orbital or extra-ocular muscle pathology Horizontal Convergent (eso deviation nasally) or divergent (exo deviation temporally) strabismus relative to the fixing eye Vertical Hyper deviation upwards or hypo deviation downwards relative to the fixing eye Cyclotortional Incyclotorsion or excyclotorsion Accommodative Associated with hypermetropia and the strabismus is more noticeable with accommodative effort. Strabismus can be improved or reduced with the use of glasses to correct the refractive error Non-accommodative Significant hypermetropia may not be present, or correcting the refractive error does not improve the angle of strabismus
Examination of strabismus There are various elements that should be examined or tested when assessing strabismus in a child. General inspection The starting point for examination should begin with a general inspection of the child’s eyes. Features to look for on examination include the presence of a ptosis, pupil abnormalities or asymmetry, and a manifest strabismus. The presence of a head tilt should be noted; this can indicate a cranial nerve IV palsy or congenital abnormality of the superior oblique muscle if the head is in a chin down position and tilted to the opposite side. Visual assessment Visual function can be assessed and a visual acuity can be obtained using an age appropriate method. In very young or nonverbal children visual behaviour can be observed, for example assessing if the child can fix and follow to targets, and comparing both eyes by occluding one at a time to see if the child has an imbalanced visual preference (the child may resist occlusion of the eye with better vision). A quantitative visual acuity can be ascertained by using various tests: forced choice preferential looking grating is used for children aged up to 1 year, Cardiff cards for children aged up to 2 years, 3 m uncrowded Kay pictures between 18 months and 3 years, 3 m crowded Kay pictures for children aged between 2 and 4 years, and 3 m crowded logMAR letters above 3 years. Crowded tests are preferred for the detection of amblyopia as they are more accurate, and children should be encouraged to perform these as soon as they are able to. Visual acuity should be obtained for each eye separately, in young children this may be difficult to perform, therefore a binocular visual acuity can be obtained. When testing visual acuity, refractive error if present should be corrected (with glasses or contact lenses), subsequently a pin hole can be used to identify any further visual improvement.
Table 2
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Please cite this article as: Bommireddy T et al., Assessing strabismus in children, Paediatrics and Child Health, https://doi.org/10.1016/ j.paed.2019.10.003
SYMPOSIUM: EYES AND ENT
deviation. Prisms of varying strength are placed over the fixating eye and the end point is reached when the corneal light reflexes are positioned symmetrically in both eyes.
Stereoacuity Stereopsis or depth perception relates to the binocular disparity between the images perceived by both eyes. Stereoacuity is the measure of the level of depth perception. A reduction in stereoacuity can be caused by various factors such as the presence of strabismus, refractive error or amblyopia. There are various measures of stereoacuity such as the TNO random dot test, Frisby test, Titmus test and the Lang stereotest to name a few.
Cover testing The cover test is useful for the detection of manifest strabismus, however it requires cooperation from the child and hence may be difficult to perform in young children. The child is directed to look towards a target straight ahead and then one eye is covered, simultaneously the movement of the fellow eye must be observed. This procedure is then repeated on the other eye. If a manifest strabismus is present, corrective movement of the deviated eye will be seen in the opposite direction from the deviation when the fellow fixating eye is covered (see Figure 2), so long as the deviated eye has some vision. The cover test should be performed for near and distance targets, and with and without glasses if the child has a refractive error. A light can be used as a target in the first instance but an accommodative target should also be used.
Corneal light reflex The corneal light reflex test, also known as the Hirschberg test, is used to detect manifest strabismus. It is performed by shining a pen torch around 50cm from the child’s eyes, the child is then directed to look towards the light. The light reflexes on both corneas should be observed and if normal ocular alignment is present the reflexes will be symmetrical (see Figure 1A). A decentred light reflex indicates a deviation of that eye in the opposite direction to the deflection. For example, a corneal light reflex observed towards the temporal aspect of the cornea of one eye suggests an esotropia of that eye (see Figure 1B). Contrastingly, a corneal light reflex observed towards the nasal aspect of the cornea of one eye suggests an exotropia of that eye (see Figure 1C). The angle of manifest strabismus can be roughly calculated using this test; 1mm of displacement of the light reflex from the centre of the pupil equates to around 15 prism dioptres of deviation. This is a useful test in uncooperative children, if fixation is poor in the deviated eye and also when assessing pseudostrabismus.
Simultaneous prism cover test The simultaneous prism cover test is used to measure the angle of manifest strabismus if it is found on cover testing. A prism is placed in front of the misaligned eye and the fellow fixing eye is occluded, simultaneously movement of the uncovered eye should be observed (see Figure 3). The strength of the prism used is varied and the angle of strabismus can be noted at the point when it is neutralised by the prism and no recovery movement of the deviated eye is seen.
Krimsky test If a manifest ocular deviation is found on the Hirschberg testing, then the Krimsky test is undertaken to measure angle of this
Figure 1 Corneal light reflex test. (a) Symmetrical corneal light reflexes: no ocular deviation present; (b) asymmetrical corneal light reflexes: left esotropia seen; (c) asymmetrical corneal light reflexes: right exotropia seen.
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Figure 2 Cover testing. (a) Right esotropia; (b) corrective movement of the right eye temporally on covering the left fixating eye; (c) no movement of the left fixating eye is seen when covering the fellow eye with the manifest strabismus.
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SYMPOSIUM: EYES AND ENT
Red reflex The red reflex test is performed using the direct ophthalmoscope. The child’s pupillary red reflexes (see Figure 4) are viewed through a direct ophthalmoscope at a distance of around 50 cm from the child. Asymmetrical reflexes (size, shape or colour) should be identified. An absent red reflex (unilateral or bilateral) may indicate serious pathology. Cycloplegic retinoscopy or refraction A significant refractive error is present in 6% of 1 year old children. Strabismus can be secondary to refractive errors, astigmatism or anisometropia. Therefore cycloplegic (with the use of drops which paralyse accommodation and dilate the pupil) retinoscopy in young children, or non-cycloplegic refraction in older children should be performed in children with strabismus to help identify the cause. Appropriate correction of the refractive error can improve the strabismus in certain types of strabismus.
Figure 3 Simultaneous prism cover test using a prism bar.
Uncover test The uncover test is used to detect latent strabismus. The child is directed to look straight towards a target and then one eye is covered for 3 seconds. The cover is then removed and the movement of that eye is observed closely. If a latent strabismus is present, the eye deviates when covered, consequently a re-fixation movement of this eye will be seen in the opposite direction to the latent deviation when the cover is removed. This test should be performed with near and distance targets.
Fundus examination A fundal examination is an essential part of assessing a child with strabismus as intraocular causes need to be excluded, and the optic nerve examined for any abnormalities such as optic nerve swelling or optic nerve atrophy. General examination A general examination of the child can be performed to detect any other abnormalities, and identify any associated syndromes or systemic conditions. Additionally an appropriate neurological examination should be performed with a focus on the cranial nerves.
Alternate cover test After the cover and uncover tests the alternate cover test can be performed. This test induces a dissociation in the binocularity of vision and identifies the total angle of strabismus (manifest plus latent components). Each eye is occluded for a few seconds consecutively in order to disrupt fusion, and the eyes observed for re-fixation movements indicating the direction of strabismus. This test should be performed with near and distance targets.
Investigations and red flags There are various causes of strabismus as outlined in Table 1, therefore the investigations performed should be guided by the examination findings. Investigations can include appropriate blood tests for example if thyroid eye disease or myasthenia gravis is suspected. Neuro-imaging may need to be performed if there are any red flags on assessment. Some red flag features that require urgent investigation or referral to the appropriate teams include the presence of headaches, vomiting, diplopia, absent red reflex, incomitant strabismus, cranial nerve palsies, abnormal head posture, afferent pupillary defect, optic nerve pathologies, neurological abnormalities, an unexplained reduction in vision, and sudden or late onset strabismus (over 3e4 years of age).
Alternate prism cover test The alternate prism cover test measures the cumulative angle of the manifest and latent strabismus. Prisms are placed in front of one eye and the alternate cover test is performed. The strength of the prism is increased until no re-fixation movement can be seen, this neutralisation point indicates the total angle of deviation, and strength of prism used to achieve this can be documented.
Complications of strabismus
Ocular motility Eye movement testing should be performed in children with strabismus to identify if the strabismus is comitant or incomitant e that is whether the size of the strabismus is constant in different positions of gaze (comitant) or varies with gaze position (incomitant). Important causes of incomitant strabismus are cranial nerve III, IV and VI palsies. An attempt to assess all nine positions of gaze should be made although it may be difficult in young children. Testing of the versions movement (binocular eye movements) of the eyes should be performed, however if any limitation or restriction in eye movement is found then ductions testing (unilateral eye movements) should be done by occluding one eye and observing the fellow eye movement.
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Amblyopia can occur as a result of strabismus. Therefore children found to have strabismus are regularly monitored for changes in vision along with orthoptic assessment. Children who have not developed visual maturity are at risk of developing amblyopia and it most commonly occurs in children less than 7 years of age, although amblyopia can occur in children older than this if they have not reached visual maturity. If a child is found to have a reduced visual acuity, then amblyopia treatment (occlusion or atropine eye drop therapy to the fellow eye) can be commenced in a timely manner, in an attempt to improve the vision and prevent a permanent reduction in vision.
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SYMPOSIUM: EYES AND ENT
referred directly to community or hospital ophthalmology services for a full assessment. Programmes vary, but generally children are referred for further ophthalmological and orthoptic assessment in secondary care if they have very poor vision (Snellen visual acuity less than 6/18) or poor vision which does not improve with glasses. A REFERENCES 1 Bowling B. Kanski’s clinical ophthalmology: a systematic approach. 8th edn. China: Elsevier, 2016. 2 National Institute for Health and Care Excellence (NICE). Clinical knowledge summaries: squint in children. 2016. National Institute for Health and Care Excellence. Available from: https://cks.nice. org.uk/squint-in-children (accessed 16 June 2019). 3 Salchow DJ. Strabismus. British medical journal best practice. 2017. Available from: https://bestpractice.bmj.com/topics/en-gb/ 689 (accessed 16 June 2019). FURTHER READING O’Dowd C. Evaluating squints in children. Aust Fam Phys 2013; 42: 872e4. Pathai S, Cumberland PM, Rahi JS. Prevalence of and early-life influences on childhood strabismus: findings from the Millennium Cohort Study. Arch Pediatr Adolesc Med 2010; 164: 250e7. Sawers N, Jewsbury H, Ali N. Diagnosis and management of childhood squints: investigation and examination with reference to red flags and referral letters. Br J Gen Pract 2017; 67: 42e3. Taylor RH. Guidelines for the management of strabismus in childhood. 2012. Royal College of Ophthalmologists. Available from: https:// www.rcophth.ac.uk/wp-content/uploads/2014/12/2012-SCI-250Guidelines-for-Management-of-Strabismus-in-Childhood-2012.pdf (accessed 16 June 2019). Yeung J. Management of strabismus. Hong Kong Med Diary 2010; 15: 14e7.
Figure 4 Normal red reflex.
Other adverse consequences of strabismus can include a reduced stereoacuity, an abnormal head posture, reduced eye contact which affects the ability of pre-verbal children to communicate effectively, psychological and social issues due to the stigma of strabismus and a reduced self-esteem, and strabismus can also have an impact on certain career prospects.
Management of strabismus The management of strabismus depends on the cause. The treatment options for benign strabismus include the use of glasses, patching therapy or atropine eye drops to blur the vision in the eye without strabismus or amblyopia, and squint surgery. Following squint surgery the operated eye can appear red and can be uncomfortable; post-operative eye drops are given for a few weeks routinely. Children take a few weeks to recover fully and are advised to avoid swimming during this period, however they can usually re-attend school within a few days.
Practice points C
C
Screening A newborn examination, part of the NHS Newborn and Infant Physical Examination (NIPE) programme, is performed within 72 hours of birth and again when the child is 6e8 weeks of age in the UK. This newborn screen helps to detect any congenital abnormalities or cataracts on ocular examination, and consists of an external eye exam, red reflex check and identification of visual fixation. Furthermore in the UK, additional screening is offered to all children aged 4e5 years. This screening is orthoptist-led with the main aim of detecting reduced vision which can be a sign of refractive error, amblyopia or strabismic amblyopia. Children who are not suitable for screening are
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C
C
C
C
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Take a good history in a patient with strabismus to help identify the cause and any red flag features. Examination should include a check of the visual acuity, presence of manifest or latent strabismus, red reflex check, oculomotility testing and a fundal check. A neurological examination should be performed as necessary. Timely identification and investigation of strabismus is necessary as it can be secondary to serious underlying pathology intracranially, intraorbitally or intraocularly. It is important to detect and treat amblyopia if it is present to prevent a permanent reduction in vision. An appropriate referral to the ophthalmology team for a full assessment of the strabismus should be made.
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Please cite this article as: Bommireddy T et al., Assessing strabismus in children, Paediatrics and Child Health, https://doi.org/10.1016/ j.paed.2019.10.003
Assessing strabismus in children
neurodevelopmental or neurological disorders) are maternal smoking beyond the first trimester, low birth weight for gestational age and sex, maternal ill health during pregnancy and perinatal and neonatal illnesses. In children with strabismus, convergent squints (esotropia, occur in 60.1%) are more common than divergent squints (exotropia, occur in 32.7%), with fully accommodative esotropias occurring the most frequently.
Tejaswi Bommireddy Kate Taylor Michael Patrick Clarke
Causes of strabismus
Abstract
Some of the primary and secondary causes of strabismus are outlined in Table 1. Primary strabismus may be idiopathic or congenital, however there known factors that can increase the likelihood of developing strabismus. Strabismus can be secondary to various pathologies. One important secondary cause which leads to sensory strabismus is poor visual acuity (unilateral or bilateral). This results in amblyopia and subsequent ocular deviation of the affected eye. Strabismus can itself cause amblyopia of the deviated eye. Other secondary causes of strabismus include children with pre-existing neurodevelopmental disorders, craniofacial syndromes, congenital abnormalities in extra-ocular muscles or their innervation and disorders affecting extra-ocular muscles or their innervation. Intracranial pathologies can cause cranial nerve III, IV and VI palsies; these present with reduced ocular motility and incomitant squints.
Strabismus, also known as a squint, is an ocular misalignment. In the UK the prevalence of strabismus in children is 2.1%. There are multiple causes of strabismus in children; some of which can be sinister and are potentially eye or life threatening. Therefore it is essential that strabismus is identified and managed appropriately and in a timely manner. Amblyopia is frequently associated with strabismus, and can be a cause or a complication of strabismus, it needs to be recognized and treated early to prevent a permanent reduction in visual acuity. This article explains how to correctly assess strabismus in children. A detailed history should be taken, and an ocular examination should be performed using the correct techniques and ocular motility tests. The important red flag features of strabismus in children are also outlined in this article.
Keywords amblyopia; child; eye; eye movements; ophthalmology; strabismus; visual acuity
What is strabismus?
Summary of the causes of strabismus in children2
Strabismus, more commonly known as a squint, occurs when there is a misalignment of the eyes. Pseudostrabismus, or pseudosquint, can also present giving the impression that the eyes are misaligned, however no true strabismus is present. Pseudostrabismus occurs more commonly in children with a broad nasal bridge and prominent nasal epicanthic folds, close set eyes, and eyelid asymmetry.
Causes of strabismus
Examples
Primary cause
Idiopathic Congenital Refractive error Amblyopia Cataract Retinoblastoma Optic neuropathy Optic nerve tumours such as gliomas Cerebral palsy Downs syndrome Foetal alcohol syndrome Developmental delay Craniosynostosis Crouzon’s syndrome Apert’s syndrome Brown’s syndrome Duane’s syndrome Cranial nerve III, IV, VI palsies Intracranial tumours Hydrocephalus Head trauma Myaesthenia gravis Thyroid eye disease
Poor visual acuity (unilateral or bilateral)
Epidemiology of strabismus The onset of strabismus is mostly before the age of 5 years. In the UK the prevalence of childhood strabismus in children is 2.1%, of which 90% have an isolated strabismus. Various factors such as prematurity, low birth weight, intrapartum complications, assisted or caesarean delivery and neonatal ill health in the first week of life increase the risk of isolated strabismus. The risk factors for neurodevelopmental strabismus (associated with
Neurodevelopmental disorders
Craniofacial syndromes
Abnormalities in extra-ocular muscles or their innervation Disorders affecting extra-ocular muscles or their innervation
Tejaswi Bommireddy MBChB, Ophthalmology Specialist Trainee, Newcastle Eye Centre, Royal Victoria Infirmary, Newcastle, UK. Conflicts of interest: none declared. Kate Taylor BSc, Deputy Head Orthoptist, Newcastle Eye Centre, Royal Victoria Infirmary, Newcastle, UK. Conflicts of interest: none declared. Michael Patrick Clarke MA MB BChir DO FRCS FRCOphth PhD, Consultant Ophthalmologist, Newcastle Eye Centre, Royal Victoria Infirmary, Newcastle, UK. Conflicts of interest: none declared.
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Table 1
1
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SYMPOSIUM: EYES AND ENT
Onset of strabismus-age of onset (congenital or acquired) and nature of onset (sudden or gradual). Symptoms-enquire about associated symptoms such as headache, vomiting, diplopia (more common in adults than children as suppression is present in children), the variability of strabismus and the psychosocial impact of strabismus. Past medical history including birth history-neurodevelopmental, neurological and systemic conditions can cause secondary strabismus. A birth history can identify risk factors for developing strabismus such as intrapartum problems, prematurity, birth weight, health during the neonatal period and trauma during birth. Past ocular history-enquire about the presence of a refractive error and whether glasses are worn. It is also important to note any previous ocular surgery such as squint surgery or previous treatment for amblyopia. Family history-there is a strong familial association with strabismus and around 30% have other family members with strabismus.1 Family members should be asked if they had any previous treatment or surgery to correct strabismus.
Classifying strabismus Strabismus is classified using various terms. Classifications include the age of onset of the strabismus (congenital or acquired), the fusional status (manifest or latent), when present (intermittent or constant), the laterality (unilateral or alternating), variation with gaze position (comitant or incomitant), the direction of the deviation (horizontal, vertical or cyclotortional), and the relation to accommodation (accommodative or non-accommodative). Table 2 defines the terminology.
History taking History taking is important in the assessment of strabismus as it helps to formulate the differential diagnoses and identify any red flags. These are some key areas that should be identified:
The classification of strabismus2,3 Classification
Definition
Congenital/infantile Acquired
Onset of strabismus less than 6 month of age Onset of strabismus greater than 6 months of age Manifest A tropia is seen when no fusional control is present. There is a deviation of one eye whilst the other eye takes up fixation Latent Fusional control is present with normal ocular alignment, but a phoria is seen when the binocularity of vision is interrupted Constant An ocular misalignment present all the time Intermittent Fluctuation in the presence of an ocular misaligment, can be worse towards the end of the day or with fatigue Unilateral Strabismus present in one eye Alternating Either eye can take up fixation and the laterality of the strabismus can vary Comitant The ocular deviation can be seen in all directions of gaze by an equal amount Incomitant The ocular deviation varies depending on the direction of gaze, a limitation or restriction in ocular movement may be present indicating a neurological, orbital or extra-ocular muscle pathology Horizontal Convergent (eso deviation nasally) or divergent (exo deviation temporally) strabismus relative to the fixing eye Vertical Hyper deviation upwards or hypo deviation downwards relative to the fixing eye Cyclotortional Incyclotorsion or excyclotorsion Accommodative Associated with hypermetropia and the strabismus is more noticeable with accommodative effort. Strabismus can be improved or reduced with the use of glasses to correct the refractive error Non-accommodative Significant hypermetropia may not be present, or correcting the refractive error does not improve the angle of strabismus
Examination of strabismus There are various elements that should be examined or tested when assessing strabismus in a child. General inspection The starting point for examination should begin with a general inspection of the child’s eyes. Features to look for on examination include the presence of a ptosis, pupil abnormalities or asymmetry, and a manifest strabismus. The presence of a head tilt should be noted; this can indicate a cranial nerve IV palsy or congenital abnormality of the superior oblique muscle if the head is in a chin down position and tilted to the opposite side. Visual assessment Visual function can be assessed and a visual acuity can be obtained using an age appropriate method. In very young or nonverbal children visual behaviour can be observed, for example assessing if the child can fix and follow to targets, and comparing both eyes by occluding one at a time to see if the child has an imbalanced visual preference (the child may resist occlusion of the eye with better vision). A quantitative visual acuity can be ascertained by using various tests: forced choice preferential looking grating is used for children aged up to 1 year, Cardiff cards for children aged up to 2 years, 3 m uncrowded Kay pictures between 18 months and 3 years, 3 m crowded Kay pictures for children aged between 2 and 4 years, and 3 m crowded logMAR letters above 3 years. Crowded tests are preferred for the detection of amblyopia as they are more accurate, and children should be encouraged to perform these as soon as they are able to. Visual acuity should be obtained for each eye separately, in young children this may be difficult to perform, therefore a binocular visual acuity can be obtained. When testing visual acuity, refractive error if present should be corrected (with glasses or contact lenses), subsequently a pin hole can be used to identify any further visual improvement.
Table 2
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2
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Please cite this article as: Bommireddy T et al., Assessing strabismus in children, Paediatrics and Child Health, https://doi.org/10.1016/ j.paed.2019.10.003
SYMPOSIUM: EYES AND ENT
deviation. Prisms of varying strength are placed over the fixating eye and the end point is reached when the corneal light reflexes are positioned symmetrically in both eyes.
Stereoacuity Stereopsis or depth perception relates to the binocular disparity between the images perceived by both eyes. Stereoacuity is the measure of the level of depth perception. A reduction in stereoacuity can be caused by various factors such as the presence of strabismus, refractive error or amblyopia. There are various measures of stereoacuity such as the TNO random dot test, Frisby test, Titmus test and the Lang stereotest to name a few.
Cover testing The cover test is useful for the detection of manifest strabismus, however it requires cooperation from the child and hence may be difficult to perform in young children. The child is directed to look towards a target straight ahead and then one eye is covered, simultaneously the movement of the fellow eye must be observed. This procedure is then repeated on the other eye. If a manifest strabismus is present, corrective movement of the deviated eye will be seen in the opposite direction from the deviation when the fellow fixating eye is covered (see Figure 2), so long as the deviated eye has some vision. The cover test should be performed for near and distance targets, and with and without glasses if the child has a refractive error. A light can be used as a target in the first instance but an accommodative target should also be used.
Corneal light reflex The corneal light reflex test, also known as the Hirschberg test, is used to detect manifest strabismus. It is performed by shining a pen torch around 50cm from the child’s eyes, the child is then directed to look towards the light. The light reflexes on both corneas should be observed and if normal ocular alignment is present the reflexes will be symmetrical (see Figure 1A). A decentred light reflex indicates a deviation of that eye in the opposite direction to the deflection. For example, a corneal light reflex observed towards the temporal aspect of the cornea of one eye suggests an esotropia of that eye (see Figure 1B). Contrastingly, a corneal light reflex observed towards the nasal aspect of the cornea of one eye suggests an exotropia of that eye (see Figure 1C). The angle of manifest strabismus can be roughly calculated using this test; 1mm of displacement of the light reflex from the centre of the pupil equates to around 15 prism dioptres of deviation. This is a useful test in uncooperative children, if fixation is poor in the deviated eye and also when assessing pseudostrabismus.
Simultaneous prism cover test The simultaneous prism cover test is used to measure the angle of manifest strabismus if it is found on cover testing. A prism is placed in front of the misaligned eye and the fellow fixing eye is occluded, simultaneously movement of the uncovered eye should be observed (see Figure 3). The strength of the prism used is varied and the angle of strabismus can be noted at the point when it is neutralised by the prism and no recovery movement of the deviated eye is seen.
Krimsky test If a manifest ocular deviation is found on the Hirschberg testing, then the Krimsky test is undertaken to measure angle of this
Figure 1 Corneal light reflex test. (a) Symmetrical corneal light reflexes: no ocular deviation present; (b) asymmetrical corneal light reflexes: left esotropia seen; (c) asymmetrical corneal light reflexes: right exotropia seen.
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Figure 2 Cover testing. (a) Right esotropia; (b) corrective movement of the right eye temporally on covering the left fixating eye; (c) no movement of the left fixating eye is seen when covering the fellow eye with the manifest strabismus.
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SYMPOSIUM: EYES AND ENT
Red reflex The red reflex test is performed using the direct ophthalmoscope. The child’s pupillary red reflexes (see Figure 4) are viewed through a direct ophthalmoscope at a distance of around 50 cm from the child. Asymmetrical reflexes (size, shape or colour) should be identified. An absent red reflex (unilateral or bilateral) may indicate serious pathology. Cycloplegic retinoscopy or refraction A significant refractive error is present in 6% of 1 year old children. Strabismus can be secondary to refractive errors, astigmatism or anisometropia. Therefore cycloplegic (with the use of drops which paralyse accommodation and dilate the pupil) retinoscopy in young children, or non-cycloplegic refraction in older children should be performed in children with strabismus to help identify the cause. Appropriate correction of the refractive error can improve the strabismus in certain types of strabismus.
Figure 3 Simultaneous prism cover test using a prism bar.
Uncover test The uncover test is used to detect latent strabismus. The child is directed to look straight towards a target and then one eye is covered for 3 seconds. The cover is then removed and the movement of that eye is observed closely. If a latent strabismus is present, the eye deviates when covered, consequently a re-fixation movement of this eye will be seen in the opposite direction to the latent deviation when the cover is removed. This test should be performed with near and distance targets.
Fundus examination A fundal examination is an essential part of assessing a child with strabismus as intraocular causes need to be excluded, and the optic nerve examined for any abnormalities such as optic nerve swelling or optic nerve atrophy. General examination A general examination of the child can be performed to detect any other abnormalities, and identify any associated syndromes or systemic conditions. Additionally an appropriate neurological examination should be performed with a focus on the cranial nerves.
Alternate cover test After the cover and uncover tests the alternate cover test can be performed. This test induces a dissociation in the binocularity of vision and identifies the total angle of strabismus (manifest plus latent components). Each eye is occluded for a few seconds consecutively in order to disrupt fusion, and the eyes observed for re-fixation movements indicating the direction of strabismus. This test should be performed with near and distance targets.
Investigations and red flags There are various causes of strabismus as outlined in Table 1, therefore the investigations performed should be guided by the examination findings. Investigations can include appropriate blood tests for example if thyroid eye disease or myasthenia gravis is suspected. Neuro-imaging may need to be performed if there are any red flags on assessment. Some red flag features that require urgent investigation or referral to the appropriate teams include the presence of headaches, vomiting, diplopia, absent red reflex, incomitant strabismus, cranial nerve palsies, abnormal head posture, afferent pupillary defect, optic nerve pathologies, neurological abnormalities, an unexplained reduction in vision, and sudden or late onset strabismus (over 3e4 years of age).
Alternate prism cover test The alternate prism cover test measures the cumulative angle of the manifest and latent strabismus. Prisms are placed in front of one eye and the alternate cover test is performed. The strength of the prism is increased until no re-fixation movement can be seen, this neutralisation point indicates the total angle of deviation, and strength of prism used to achieve this can be documented.
Complications of strabismus
Ocular motility Eye movement testing should be performed in children with strabismus to identify if the strabismus is comitant or incomitant e that is whether the size of the strabismus is constant in different positions of gaze (comitant) or varies with gaze position (incomitant). Important causes of incomitant strabismus are cranial nerve III, IV and VI palsies. An attempt to assess all nine positions of gaze should be made although it may be difficult in young children. Testing of the versions movement (binocular eye movements) of the eyes should be performed, however if any limitation or restriction in eye movement is found then ductions testing (unilateral eye movements) should be done by occluding one eye and observing the fellow eye movement.
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Amblyopia can occur as a result of strabismus. Therefore children found to have strabismus are regularly monitored for changes in vision along with orthoptic assessment. Children who have not developed visual maturity are at risk of developing amblyopia and it most commonly occurs in children less than 7 years of age, although amblyopia can occur in children older than this if they have not reached visual maturity. If a child is found to have a reduced visual acuity, then amblyopia treatment (occlusion or atropine eye drop therapy to the fellow eye) can be commenced in a timely manner, in an attempt to improve the vision and prevent a permanent reduction in vision.
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SYMPOSIUM: EYES AND ENT
referred directly to community or hospital ophthalmology services for a full assessment. Programmes vary, but generally children are referred for further ophthalmological and orthoptic assessment in secondary care if they have very poor vision (Snellen visual acuity less than 6/18) or poor vision which does not improve with glasses. A REFERENCES 1 Bowling B. Kanski’s clinical ophthalmology: a systematic approach. 8th edn. China: Elsevier, 2016. 2 National Institute for Health and Care Excellence (NICE). Clinical knowledge summaries: squint in children. 2016. National Institute for Health and Care Excellence. Available from: https://cks.nice. org.uk/squint-in-children (accessed 16 June 2019). 3 Salchow DJ. Strabismus. British medical journal best practice. 2017. Available from: https://bestpractice.bmj.com/topics/en-gb/ 689 (accessed 16 June 2019). FURTHER READING O’Dowd C. Evaluating squints in children. Aust Fam Phys 2013; 42: 872e4. Pathai S, Cumberland PM, Rahi JS. Prevalence of and early-life influences on childhood strabismus: findings from the Millennium Cohort Study. Arch Pediatr Adolesc Med 2010; 164: 250e7. Sawers N, Jewsbury H, Ali N. Diagnosis and management of childhood squints: investigation and examination with reference to red flags and referral letters. Br J Gen Pract 2017; 67: 42e3. Taylor RH. Guidelines for the management of strabismus in childhood. 2012. Royal College of Ophthalmologists. Available from: https:// www.rcophth.ac.uk/wp-content/uploads/2014/12/2012-SCI-250Guidelines-for-Management-of-Strabismus-in-Childhood-2012.pdf (accessed 16 June 2019). Yeung J. Management of strabismus. Hong Kong Med Diary 2010; 15: 14e7.
Figure 4 Normal red reflex.
Other adverse consequences of strabismus can include a reduced stereoacuity, an abnormal head posture, reduced eye contact which affects the ability of pre-verbal children to communicate effectively, psychological and social issues due to the stigma of strabismus and a reduced self-esteem, and strabismus can also have an impact on certain career prospects.
Management of strabismus The management of strabismus depends on the cause. The treatment options for benign strabismus include the use of glasses, patching therapy or atropine eye drops to blur the vision in the eye without strabismus or amblyopia, and squint surgery. Following squint surgery the operated eye can appear red and can be uncomfortable; post-operative eye drops are given for a few weeks routinely. Children take a few weeks to recover fully and are advised to avoid swimming during this period, however they can usually re-attend school within a few days.
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Screening A newborn examination, part of the NHS Newborn and Infant Physical Examination (NIPE) programme, is performed within 72 hours of birth and again when the child is 6e8 weeks of age in the UK. This newborn screen helps to detect any congenital abnormalities or cataracts on ocular examination, and consists of an external eye exam, red reflex check and identification of visual fixation. Furthermore in the UK, additional screening is offered to all children aged 4e5 years. This screening is orthoptist-led with the main aim of detecting reduced vision which can be a sign of refractive error, amblyopia or strabismic amblyopia. Children who are not suitable for screening are
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Take a good history in a patient with strabismus to help identify the cause and any red flag features. Examination should include a check of the visual acuity, presence of manifest or latent strabismus, red reflex check, oculomotility testing and a fundal check. A neurological examination should be performed as necessary. Timely identification and investigation of strabismus is necessary as it can be secondary to serious underlying pathology intracranially, intraorbitally or intraocularly. It is important to detect and treat amblyopia if it is present to prevent a permanent reduction in vision. An appropriate referral to the ophthalmology team for a full assessment of the strabismus should be made.
Ó 2019 Elsevier Ltd. All rights reserved.
Please cite this article as: Bommireddy T et al., Assessing strabismus in children, Paediatrics and Child Health, https://doi.org/10.1016/ j.paed.2019.10.003