Objective: to investigate visual function pre- and post surgery in children with single-suture non-syndromic craniosynostosis
Design: Twenty-nine infants (12 with sagittal synostosis, 10 with trigonocephaly and 7 with anterior plagiocephaly) were longitudinally evaluated using a battery of tests assessing various aspects of visual function, including ocular behaviour, acuity, visual fields and fixation shift. All infants were assessed before surgery and 2, 6 and 12 months after surgery.
Results: Before surgery only 16% of infants had completely normal visual function, while on the assessment performed 12 months after surgery, the number with normal results on all the tests increased to 65%. The only abnormalities found 12 months after surgical correction were mainly found on abnormal oculomotor behaviour in infants with plagiocephaly.
Conclusion: Abnormalities of visual function were not frequent in infants with non-syndromic craniosynostosis who underwent surgical correction. Approximately half of the patients had some visual abnormalities before surgery, which subsequently improved, showing a delayed visual maturation rather than persistent abnormalities.
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In the last two decades a few papers have reported visual impairment in infants with craniosynostosis.1–12 While most of the early studies did not provide detailed information on their inclusion criteria,1–6 more recent studies have focused either on syndromic8–11 or, in a few cases, on non-syndromic craniosynostosis.7 12 In the non-syndromic forms visual function was evaluated by assessing ophthalmological findings,7 but we have recently reported that more behavioural aspects of visual function can also be affected.12 Using an age-specific battery of tests assessing various aspects of visual function, we found that abnormal eye movements were present in 22% of the whole cohort, and were more common in infants with plagiocephaly, who also had frequent visual field abnormalities. In contrast, infants with sagittal synostosis mainly showed abnormal visual attention, tested by means of fixation shift test. In our previous study all infants were only assessed before surgical correction.
The aim of the present study has been to follow longitudinally, various aspects of visual function before and after surgical correction in children with single-suture non-syndromic craniosynostosis.
All patients included in the study had been referred to the Paediatric Neurosurgery Unit of the Catholic University Medical School and Bambino Gesù Children’s Hospital, Rome, between November 2003 and February 2006. The diagnosis was made by clinical examination and the involved suture was identified and generally confirmed by computerised tomography (CT) scans with three-dimensional reconstruction. Patients were included in this study according to the following inclusion criteria: i) single-suture non-syndromic craniosynostosis; ii) surgical correction performed in one of the two units; and iii) visual assessments performed pre surgery and 2, 6 and 12 months after surgical correction.
All patients were assessed for visual function in the Department of Ophthalmology and in the Unit of Child Neurology and Psychiatry of the Catholic University, Rome.
A complete ophthalmological examination (slit lamp, cycloplegic refraction and funduscopy) was performed. Myopia was defined as cycloplegic refraction ⩽−0.5 diopter (D), hyperopia as ⩾+2.50 D,13 asthigmatism was considered if <0.75 D.
Because of the young age of the patients, orthoptic evaluation was performed by means of Krimsky test14 (and, when possible, cover-uncover test) for far and near-distance and eye motility examination in the nine gaze positions. Presence or absence of horizontal and/or vertical deviations was noticed as well as anomalous head posture.
Behavioural assessment of visual function
The assessment of visual function also included other aspects, outlined below:
Ability to fix and follow was tested by observing the ability of the infant to fix a target with black and white concentric circles with a diameter of 10 cm, on a card of 15 cm × 15 cm at a distance of 30–50 cm and to follow it horizontally, vertically and in a full circle, looking for quality of pursuit.
Acuity was assessed binocularly by means of the Teller acuity card procedure.15–17 This method is based on an inborn preference for a pattern (black and white gratings of different stripe widths) over a uniform field, depicted on cards with decreasing stripe widths. The location of the left/right position of the test stimulus varies randomly. An observer judges the infant’s reaction to the location of the test stimulus on the basis of eye and head movement. The threshold of acuity is taken as the minimum stripe width to which the subject consistently responds correctly. Acuity values were expressed in minutes of arc (or cycles per degree) and were compared to age-specific normative data reported in the literature.18 19
Binocular visual fields were assessed using kinetic perimetry, according to the technique described in detail by van Hof-van Duin.18 The apparatus consisted of two 4 cm-wide black metal strips, mounted perpendicularly to each other and bent to form two arcs, each with a radius of 40 cm. The perimeter was placed in front of a black curtain, concealing the observer, who could watch the infant’s eye and head movements through a peep-hole. The patient was held in the centre of the arc perimeter, with the chin supported. During central fixation of a 6° diameter white ball, an identical target was moved from the periphery towards the fixation point, along one of the arcs of the perimeter, at a velocity of about 3°/s. Eye and head movements towards the peripheral ball were used to estimate the outline of the visual fields. Age-specific normative data for full-term and pre-term infants are available.18
Fixation shift test assesses visual attention by evaluating the direction and the latency of saccadic eye movements in response to a peripheral target (alternating black and white stripes) in the lateral field. Using a 28-inch monitor, a central target was used as a fixation stimulus before the appearance of the peripheral target. While in some trials the central target disappeared simultaneously with the appearance of the peripheral target (non-competition), in others the central target remained visible and created a situation of competition between the two stimuli. Details of the methodology have been previously described.20 21
Normal children can reliably shift their attention in a situation of non-competition during the first weeks of life, but brisk refixations in a situation of competition is only found after 6–8 weeks and reliably by 12–18 weeks of age. Absent or delayed (a latency of more than 1.2 s) refixation after 5 months of age is considered abnormal. All the tests were performed by the same examiner.
All the infants were assessed at 12 months after surgical correction, using the Griffith’s neurodevelopmental assessment.22 Neurodevelopment outcome was classified as normal when the developmental quotient (DQ) was above 85.
Twenty-nine children were included in the study. Twelve of the 29 had sagittal synostosis, 10 had trigonocephaly and 7 had anterior plagiocephaly. None of the children had signs of increased intracranial pressure, before or after surgical correction. Mean age at surgery was 7 months, ranging from 4.5 to 15 months.
Pre- and post-surgical ophthalmological examination
Individual details are shown in table 1.
In the plagiocephaly group five of the seven infants had strabismus before and after surgical correction (esotropia in three and vertical strabismus in the other two).
In the trigonocephaly group only one of the 10 infants had a slight underaction of inferior obliques before and after surgical correction, but no detectable strabismus in the primary position. Another child showed horizontal strabismus (esotropia) on the assessment performed 12 months after surgical correction.
In the sagittal synostosis group only one child had a unilateral deficit of elevation associated with ipsilateral ptosis before and after surgical correction. Another child had vertical strabismus on the assessment performed 12 months after surgical correction.
The anterior and posterior segment examination was always normal.
No change in refractive power was observed during the examinations performed before and after surgical correction.
Pre- and post-surgical behavioural assessment of visual function
Ability to fix and follow
In the plagiocephaly group the ability to fix and follow was abnormal in four of the seven infants assessed before surgical correction (57%), but it progressively improved, with normal results on all the assessments performed 12 months after surgical correction.
In the trigonocephaly group the ability to fix and follow was asymmetric in eight of the 10 infants assessed before surgical correction (80%), but it progressively improved, with normal results by 6 months after surgical correction.
In the sagittal synostosis group only one patient, who also had ptosis, had abnormal ability to fix and follow before surgical correction, and this remained abnormal on all the assessments.
Age equivalent acuity was normal in 25 of the 29 children assessed before the surgical correction, and it was normal in all 29 children by 2 months after surgical correction, irrespective of the type of craniosynostosis.
In the plagiocephaly group visual field was asymmetric in four of the seven infants assessed before surgical correction (57%) but all seven had symmetric visual fields at 12 months follow-up.
In the trigonocephaly group visual fields were abnormal in two of the 10 infants assessed before surgical correction (20%) but all 10 infants had normal visual fields at 12 months follow-up.
In the sagittal synostosis group visual fields were asymmetric in two of the 12 patients assessed before surgical correction (17%). One of the two children had normal fields by 2 months after surgical correction, while the other child, who also had an ipsilateral ptosis, still had asymmetric fields at 12 months follow-up.
Fixation shift test
In the plagiocephaly group fixation shift test was abnormal in one of the seven infants before surgical correction (14%), but all seven infants had normal results at 12 months follow-up.
In the trigonocephaly group fixation shift test was abnormal in three of the 10 infants before surgical correction (30%), but all 10 infants had normal results at 12 months follow-up.
In the sagittal synostosis group fixation shift test was abnormal in 10 of the 12 infants before surgical correction (83%), with a progressive improvement. At 6 and 12 months follow-up only one infant, who also had unilateral ptosis, still had abnormal results.
All the infants had a DQ within the normal range (mean 104; range 85–120).
Several studies have reported visual impairment in infants with craniosynostosis, mainly focusing on ophthalmological aspects and, more rarely, electrophysiological findings.1–11 23 We recently reported our observation on visual function in a cohort of infants with non-syndromic craniosynostosis assessed before surgery, using a battery of tests assessing oculomotor behaviour and various behavioural aspects of visual function such as acuity, visual fields and fixations shift.12 In that study we found that abnormalities of visual function were frequent and that the patterns of visual abnormalities were different in the various forms of craniosynostosis. In the present study we followed the same children longitudinally for at least 12 months after surgical correction. While only 16% of children had normal visual abilities before surgical correction, on the assessment performed 12 months after surgery, the number of children with normal results on all the visual tests performed increased to 65%. The remaining 35% only had oculomotor abnormalities, with the exception of one infant, who had abnormal results on acuity, fields and fixation shift and also had a unilateral ptosis.
It is of interest that oculomotor abnormalities did not significantly improve after surgery. This may be partly explained by the complex relationship between the possible effect of changes in orbital dimensions and volume on ocular movements. Several studies have recently highlighted new concepts regarding specific aspects of ocular motility that are not only related to mechanisms of innervation but can also be mechanically determined by extraocular muscles and their associated connective tissue pulleys.24
These were most frequent in patients with plagiocephaly, in keeping with previous studies also reporting frequent oculomotor problems in plagiocephaly.1–4 6 7 25 In this group abnormalities of fix and follow and of visual fields, in contrast, progressively improved after surgery.
Two of the infants with plagiocephaly had a marked torticollis, which was still obvious 12 months after surgery, at the time when strabismus was still present but visual function had improved. This suggests that torticollis may not significantly affect the behavioural aspects of visual performance.
A different pattern of visual impairment was found in the other forms of craniosynostosis. Oculomotor abnormalities were less frequent in the infants with trigonocephaly, and ability to fix and follow, abnormal in 80% of the infants before surgical correction, normalised in all by 6 months after surgery, with most infants having normal results within 2 months.
The sagittal synostosis group showed yet a different profile, with 83% of abnormal responses on fixation shift test before surgical correction. This test explores the ability to shift the attention from a central target to a peripheral one in situations of both competition and non-competition, and allows a measure of attention, which is known to be mediated by the parietal lobe.20 Our hypothesis that the potential compression on the parietal lobes, due to the anteroposterior lengthening of the skull, might be responsible for the deficit of shift of visual attention, appears to be supported by the post-surgical results, showing a complete recovery at 12 months after surgical correction in nine of the 10 infants with early abnormalities.
It is of interest that at variance, with several previous studies reporting abnormal visual acuity,8–11 in our cohort this was normal in all patients after surgery and in only four of the 29 before surgery. The difference is certainly related to the different inclusion criteria, as previous studies such as Apert, Crouzon, Pfeiffer, and Saethre-Chotzen, also included syndromic craniosynostosis, which is at higher risk of optic neuropathy with subsequent visual impairment.
What is already known on this topic
Previous studies in infants with craniosynostosis mainly assessed ophthalmological findings in children with both syndromic and non-syndromic craniosynostosis, reporting a high incidence of ocular abnormalities and of visual impairment.
What this study adds
Our study provides evidence that abnormalities of visual function are not frequent in infants with non-syndromic craniosynostosis who undergo surgical correction.
About half of the infants had some visual abnormalities before surgery, which were different in the different forms of craniosynostosis, but they subsequently improved, therefore showing a delayed visual maturation rather than persistent abnormalities.
The early visual abnormalities observed in our cohort did not appear to affect early neurocognitive development, as all the infants had normal global DQs with normal scores on all the subscales, including eye–hand coordination and performance.
In conclusion our study provides evidence that abnormalities of visual function are not frequent in infants with non-syndromic craniosynostosis who undergo surgery. Approximately 85% of the patients had visual abnormalities before surgery, but only 31% were still abnormal 1 year after. The improvement noticed in our cohort cannot be explained by scarce sensitivity of the tests, as these have age-specific normative data, or by any specific rehabilitative treatment, as only three patients with plagiocephaly, who had the most severe and persistent abnormalities, had regular treatment and their visual outcome is not normal. These results would therefore suggest that surgery may play a role in this improvement, but this statement could only be proved by large randomised studies using a control group of infants with similar craniosynostosis who do not undergo surgery.
Competing interests: None.
Ethics approval: The study was approved by the Research Ethical Committee of the Catholic University, Rome, Italy.