Curr Ophthalmol Rep (2015) 3:225–231 DOI 10.1007/s40135-015-0084-6
PEDIATRIC OPHTHALMOLOGY (S. ROBBINS, SECTION EDITOR)
Newer Understanding of Eye Issues in Craniofacial Malformations Adela Wu1 • Megan E. Collins2
Published online: 19 October 2015 Springer Science + Business Media New York 2015
Abstract Pediatric patients with craniofacial abnormalities face unique challenges requiring early intervention and longitudinal care for their ocular and systemic problems. Non-syndromic and syndromic craniosynostoses involve asymmetric development of the cranial vault and facial bones, which frequently leads to ophthalmic manifestations, including strabismus, refractive error, and visual field losses. In recent years, ophthalmologists, craniofacial surgeons, and pediatricians involved in caring for craniosynostosis patients have found that timely surgery and monitoring, using refined devices such as spectral-domain optical coherence tomography, can lead to improved quality of life and prognosis for these patients. We review relevant literature from the past 5 years describing and managing ocular symptoms of craniosynostosis. Keywords Craniosynostosis (non-syndromic, syndromic) Strabismus Refractive error Vision loss Amblyopia Pediatric management
This article is part of the Topical collection on Pediatric Ophthalmology. & Megan E. Collins
[email protected] Adela Wu
[email protected] 1
Johns Hopkins University School of Medicine, Baltimore, MD, USA
2
Wilmer Eye Institute, Johns Hopkins University School of Medicine, 600 North Wolfe Street, Wilmer 233, Baltimore, MD 21287-9028, USA
Introduction Craniofacial abnormalities encompass a range of congenital deformities in the growth and development of the skull and facial bones and can be categorized as craniosynostoses, the premature fusion of one or more cranial sutures, or clefting syndromes, the failure of two adjacent embryonic facial processes to properly fuse [1]. Craniosynostoses have an incidence of 1 in 2500 live births. Primary craniosynostoses have a genetic etiology, most often attributed to FGFR or TWIST mutations, while secondary synostoses occur when the premature fusion is secondary to another known disorder. The synostoses are divided further into simple, which involve one suture, and complex, which can involve multiple sutures and a variety of systemic symptoms, such as midface hypoplasia and digital anomalies. The syndromic craniosynostoses include Apert, Crouzon, Pfeiffer, Muenke, Saethre-Chotzen, and Antley-Bixler syndromes. Non-syndromic craniosynostoses refer to simple single suture fusion with sequelae directly resulting from the suture fusion itself, including increased intracranial pressure, proptosis, and refractive error. Examples of non-syndromic craniosynostoses include premature fusion of the frontal (metopic), sagittal, coronal, lambdoidal, or squamous suture. Given that craniosynostoses involve the development and growth of cranial and skull bones structures, patients with craniofacial conditions often present with orbital anomalies and ophthalmic findings. The most frequent visual problems for these patients involve abnormalities of the cornea due to exposure, amblyopia, strabismus, refractive error, and optic neuropathy [2, 3]. Frequent monitoring for ocular complaints is recommended as prior studies have demonstrated approximately 40 % of patients with syndromic craniosynostosis have vision of 20/40 or worse in their better-seeing eye [4].
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The published literature describing the ocular findings in craniosynostosis varies considerably in the prevalence of strabismus, refractive error, and vision loss [2, 5, 6]. The majority of articles are retrospective case series with a small number of patients, limited follow-up, and varying quantitative and qualitative descriptions of ocular findings. Furthermore, data on ocular findings are often limited, and longitudinal follow-up of patients before and after craniofacial repair is often not reported [7]. This article provides an update on the published literature regarding ophthalmic findings in craniofacial malformations over the past 5 years. A number of case reports [8– 22] have been published, which contribute to our understanding of the clinical presentations of craniosynostosis, genetic mutations, phenotypic expression, ocular findings, and strabismus management. There have also been several large studies that have contributed to our understanding of the prevalence of eye findings in craniosynostosis. Three main topics discussed below are: (1) prevalence of ophthalmic findings and causes of vision loss in isolated craniosynostosis; (2) optic neuropathy surveillance with new imaging and testing modalities; and (3) structural orbital changes in craniosynostosis and how these relate to ophthalmic findings. Little has been reported in the literature about the longterm health outcomes and quality-of-life issues for patients with craniosynostosis. In a retrospective analysis of 167 patients with syndromic craniosynostosis, de Jong et al. noted that 61 % of patients had vision impairment and 56 % suffered from hearing loss [23]. Children with complex craniosynostosis also suffer from serious systemic symptoms, such as upper airway obstruction and obstructive sleep apnea, that severely interfere with breathing and quality of life [24] These chronic problems highlight the need for a multidisciplinary approach to manage these patients, as well as the long-term needs for hearing and vision assessments, and disability services. This article will conclude with recommendations on how to incorporate the ophthalmologist into the multidisciplinary team for the management of these complex patients.
Ocular Findings in Non-syndromic Single Suture Craniosynostosis There is extensive literature on ocular findings in syndromic craniosynostosis [4, 25, 26]. Recent literature reporting frequent ocular findings in the single suture synostosis group highlights the importance of close vision surveillance in this cohort as well. In a retrospective review of 123 patients seen between 1990 and 2009 at a single institution, over half (52 %) had non-syndromic craniosynostosis; approximately one
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quarter (23.6 %) had syndromic craniosynostosis and 16.2 % had craniofacial cleft anomalies [27]. Consistent with prior studies, both syndromic and non-syndromic craniosynostosis had ocular involvement; however, it was more common in the syndromic group (27 %) versus the non-syndromic (17 %). Chung et al. report ophthalmic findings in 88 children with non-syndromic craniosynostosis treated with expansion cranioplasty [28••]. They reported findings for patients with coronal, sagittal, lambdoidal and combined sagittal plus lambdoidal craniosynostosis and found the highest rates of strabismus and refractive error in the coronal synostosis group. For their entire cohort, 25 % of patients had a fixation preference (indicative of possible amblyopia) and 45 out of 88 patients with significant refractive error [hyperopia (27 %), myopia (5 %), astigmatism (35 %) and anisometropia (20 %)]. Twenty-six percent had exodeviation, 14 % had an esodeviation and 5 % had a vertical deviation. Nine patients (10 %) had anisoastigmatism of 1D or more, which is lower than that reported in prior studies focusing solely on unilateral coronal synostosis [29, 30]. Patients had pre- and post-operative ophthalmic exams, and the authors did not report any changes in the strabismus or refractive error following expansion cranioplasty. Interestingly, none of the children in this study had optic atrophy or disc edema. Refractive Error in Unicoronal Synostosis An increasing amount of literature is shedding light on prevalence of ophthalmic findings and amblyogenic risk factors in this subset of patients with non-syndromic single suture craniosynostosis. This is particularly so in unicoronal craniosynostosis, also referred to as anterior plagiocephaly. According to Di Rocco, anterior plagiocephaly has a reported incidence of 1/10,000 live births with unicoronal synostosis occurring four to seven times more frequently than bicoronal [31]. There is a 2:1 female predilection, right side frequency is double that of left, and it presents sporadically in approximately 2/3 of cases. In comparison to other single suture craniosynostosis, DiRocco reports that patients with anterior plagiocephaly have a higher reported incidence of ocular complications, most likely related to the sutures involved and its impact on orbital growth. An earlier study also reported more exotropia in patients with coronal craniosynostosis [32]. Patients with unilateral craniosynostosis have been found to have asymmetric refractive error due to the asymmetric development of the bony cranial vault and orbital structures. Recently, Levy et al. described a group of 39 patients with unilateral coronal synostosis demonstrating a novel finding of significant astigmatism in the eye contralateral to the synostosis [29]. Fifty-four percent
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(21/39) of the patients presented with 1.00 D or greater astigmatism in at least one of their eyes. Of these 21 patients with significant astigmatism, 76 % (16/21) had anisoastigmatism of 1.00 D or greater and fourteen of those patients (88 %) had worse astigmatism in the eye contralateral to the synostosis. In general, Levy et al. found that astigmatism as well as anisoastigmatism developed to a greater degree on the side contralateral to the synostosis, which could be attributed to the abnormal development and shape of the orbit, where the superior orbital rim has been inferiorly displaced. Another group from the Children’s Hospital Los Angeles followed 25 pediatric patients who had documented unicoronal craniosynostosis, of whom 14 (56 %) had amblyogenic anisometropia [30].As also seen in Levy’s patients, the majority of these patients (79 %) with amblyogenic anisometropia had greater refractive error in the eye contralateral to the coronal synostosis [30]. In this same study, 72 % of affected Hispanic children had amblyogenic anisometropia compared to 14 % of effected non-Hispanic children, suggesting possible increased risk in certain populations [30]. As for management of refractive issues, specifically patients who suffer from unicoronal craniosynostosis, physician-investigators from both groups have studied the effect of the timing of fronto-orbital advancement [29, 30]. Neither group found a significant relation between the timing of fronto-orbital advancement and whether amblyogenic anisometropia occurred. Refractive Error in Metopic Synostosis Much of the recent literature on refractive error in single suture non-syndromic craniosynostosis focuses on unilateral coronal synostosis. MacIntosh et al. published a retrospective analysis of 64 children with metopic synostosis and reported that 20/64 subjects (31 %) had refractive error and/or strabismus [33]. Fifty percent of those subjects had refractive error requiring glasses (9 with hypermetropia, 5 with astigmatism B1.5 D, 1 with astigmatism [1.5 D, 3 with astigmatism of unknown severity and one with myopia). This case series had the largest number of patients to date building on the experience of three earlier studies, which had a combined total of 33 subjects and reported varying incidence of ocular disorders [32, 34, 35]. Similar to the studies of refractive error in unicoronal synostosis, the MacIntosh group examined whether timing of craniofacial repair had any impact on the degree of refractive error, specifically astigmatism. Their results demonstrated that timing of craniofacial surgery did not have any impact on the ocular findings. These findings differed from an earlier study of 14 patients with metopic synostosis which reported a higher incidence of refractive error with later reconstructive surgery [34].
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Strabismus The timing for craniofacial repair and its impact on strabismus continues to be a question for craniofacial teams and ophthalmologists. Investigators are attempting to learn more about how timing of surgery impacts strabismus. In syndromic craniosynostosis, there have been reports of worsening strabismus postoperatively [36]. For example, in one report of 20 patients with Apert and Pfeiffer syndrome who underwent bipartition with monobloc distraction, 9/20 cases had worsening strabismus postoperatively. Therefore, many ophthalmologists will routinely wait for major cranio-facial surgery to be performed before performing strabismus surgery. In 2015, Samra et al. published a retrospective analysis of their 36 year institutional experience with 181 patients with single suture non-syndromic unilateral coronal synostosis treated with fronto-orbital advancement surgery (FOAS) [37••]. The authors reviewed prior studies, with a reported incidence of strabismus preoperatively in 29–99 % of patients and postoperatively in 19–91 %. In their cohort, 36.7 % of patients had strabismus prior to FOAS, and the majority of patients (96.6 %) had persistence of their strabismus following the surgical repair. Of 50 patients who had no strabismus diagnosis preoperatively, 46 % developed strabismus following FOAS. Interestingly, the authors compared strabismus subtypes in those who had strabismus preoperatively and those who developed it postoperatively and found no statistically significant difference in the types of strabismus between the two groups. Vertical strabismus was more common than horizontal strabismus in both groups. Various mechanisms for vertical strabismus have been postulated, but there is no clear explanation about the etiology of horizontal strabismus. This study, the largest to date, highlights two important points in the care of craniosynostosis patients: (1) Strabismus typically does not resolve after craniofacial repair, and (2) almost half of the patients will go on to develop strabismus after surgical repair. Regarding the high rate of postoperative strabismus, the authors argue that subperiosteal dissection of the orbit during FOAS can result in detachment of the trochlea from its anatomic insertion. Several other studies are currently investigating different rates of postoperative strabismus depending on the type of craniofacial repair performed. In 2013, MacKinnon et al. compared the ophthalmic outcomes for unilateral coronal synostosis patients treated by FOAS or endoscopic strip craniectomy (ESC) and helmet therapy [38]. This retrospective review of 43 patients (22 patients treated with FOAS and 21 treated with ESC and helmet therapy) found that patients treated with ESC and helmet therapy had less severe motility abnormalities,
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amblyopia, astigmatism, and less need for strabismus surgery. Two out of 21 patients in the ESC group required strabismus surgery as compared to 9/22 in the FOAS group. Amblyopia developed in 2/21 patients in the ESC group and 10/22 patients in the FOAS group. In general, ESC is performed at an earlier age and is less disruptive to the surrounding orbital tissue.
Optic Neuropathy Previously, the incidence of elevated ICP of single suture craniosynostosis was reported as 13 % [39]. In a recent retrospective study on the prevalence of papilledema in 205 patients with single suture craniosynostosis, papilledema was noted in 9.7 % of sagittal suture synostosis, 5.6 % in the metopic suture group and no papilledema seen in patients with coronal or lambdoidal suture synostosis [7]. This study highlights the importance of optic nerve assessments in single suture craniosynostosis. There was not a correlation seen between ventricular dilatation and papilledema, which supports the argument that hydrocephalus is not the sole causative etiology of papilledema.
Vision Loss Surveillance Patients with craniosynostosis frequently suffer from vision loss, which has been attributed to amblyopia, optic atrophy, or intracranial dysfunction inherent to visual pathway impairment. Vision loss related to optic neuropathy has historically been thought to be related to obstructive hydrocephalus and cranio-cerebral disproportion [40]. In his review, Nischal explains that patients with syndromic craniosynostosis have a high incidence of congenitally absent intracranial venous sinuses and obstructive sleep apnea, due in part to maxillary hypoplasia and narrow airways, which also contribute to elevated ICP, papilledema, and ultimately optic neuropathy [41]. Reported methods of optic nerve surveillance have included fundoscopic assessment, kinetic and static perimetry, visual evoked potentials (VEP), and optical coherence tomography (OCT). Liasis et al. used kinetic perimetry and serial pattern reversal visual evoked potentials (pVEPs) to assess visual field deficits in 16 children with syndromic craniosynostosis [42]. All cases had visual field deficits, and there was a correlation between VEP asymmetries and visual field deficits. Further, there was a range in severity of visual field loss, with Pfeiffer patients sustaining greater field
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defects than Crouzon patients. In addition, patients with Apert or Crouzon syndromes appear to have nasal visual field defects, which the authors postulate is related to mechanical compression of the visual pathways and ischemic damage to the optic nerve. Dagi et al. examined the efficacy of utilizing spectraldomain OCT to assess the thickness of the peripapillary retinal nerve fiber layer (RNFL) and severity of optic neuropathy compared to assessment through fundus examination and photos with a non-mydriatic retinal camera [43•]. The authors report that spectral-domain OCT has a 77 % sensitivity and 83 % specificity in assessing peripapillary RNFL. It is important to note that the sensitivity for detecting optic atrophy (88 %) was higher than the sensitivity for detecting papilledema (60 %). Overall, the authors report that spectral-domain OCT is a valuable tool in the longitudinal monitoring of peripapillary RNFL and care of patients with craniosynostosis at risk for vision loss. An additional study demonstrating the feasibility of using OCT to screen for papilledema in children, ages 3–8, with non-syndromic sagittal suture craniosynostosis, Crouzon or Pfeiffer syndrome, ages 3–8, was published by Driessen et al. [44]. Patients with fundoscopic evidence of disc edema or atrophy had a significantly increased RNFL thickness compared to healthy controls. Of note, the authors report increased RNFL thickness, even in optic atrophy, while Dagi et al. noted decreased RNFL thickness in this group. OCT is a less invasive surveillance modality than 24 h intracranial monitoring and the hope is that it might be used in the future to detect increased ICP before florid papilledema develops. However, this study did not find an increased RNFL thickness in patients with subtle blurring of the disc margins. Continued research efforts will help refine the use of this imaging modality, but both of these studies demonstrated its feasibility, even in a young population. Driessen et al. also reported the use ultrasound as an alternative to fundoscopy and this remains another area of investigation [45].
Structural Orbital Changes in Craniosynostosis In a 2010 systematic review on congenital craniofacial anomalies, Forbes stated that the presentations and etiologies of vision loss are changing as craniofacial surgical techniques and timing of intervention have evolved [38, 46, 47]. In addition to surgical advances, there have also been advances in skull and orbit imaging modalities and optic nerve imaging to gain a better understanding of the pathophysiology of craniosynostosis.
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Orbital Dysmorphology in Unilateral Craniosynostosis Relevant to the literature on amblyogenic anisometropia in the contralateral eye of patients with unilateral craniosynostosis, Beckett et al. published a retrospective case review of 21 patients with unilateral craniosynostosis [48]. Their findings concurred with prior reports of reduced orbital volume in craniosynostosis but importantly reported bilateral orbital dysmorphology in unicoronal synostosis [49]. Specifically, they found that the horizontal zone angle in the contralateral eye was significantly larger than in the involved ipsilateral eye as well as control orbits. The authors argued that this abnormal orbital anatomy might contribute to some of the ocular findings, such as anisometropia.
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cause of the V-pattern include excyclotorsion of each eye causing the rectus muscles to have oblique vectors, posterior displacement of the trochlea with shortening, and desagittalization of the superior oblique muscle, and instability of the muscle pulleys [15, 52].One surgical approach reported is a bilateral superior oblique tuck with infraplacement of the medial rectus for a V-pattern esotropia in order to address the excyclotorsion [16]. To gain a better understanding of the impact of muscle pulleys on V-pattern strabismus, Weiss et al. examined a cohort of 20 patients with Crouzon syndrome [53]. Eleven out of twenty patients had V-pattern exotropia with 2–7 mm displacement of the rectus muscle pulleys. Displacement of muscle pulleys on simulation software produced a V-pattern strabismus, supporting the theory that extorsion of the rectus muscle pulleys accounts for the pattern strabismus.
Orbital Volume in Craniosynostosis Imai et al. report their findings of 13 syndromic craniosynostosis patients (five Crouzon and eight Apert) who underwent preoperative CT scans prior to fronto-orbital advancement with cranial distraction [50]. In their study, both groups had smaller orbital volume when compared to the normal orbital volume expected for children of that age. However, the volume was smaller in Crouzon versus Apert, which the authors argue is correlated to a greater degree of maxillary hypoplasia in Crouzon patients. Accordingly, they found reports of ocular symptoms in 100 % of the Crouzon patients and in 62.5 % of the Apert syndrome patients. Even with surgical intervention, normal orbital volume was not restored, but less ocular complications were noted. Festa’s et al. report using 3D CT preoperatively and postoperatively corroborated the findings of increased orbital volume after Lefort III advancement in syndromic craniosynostosis [3]. In a retrospective review of 61 patients with Apert and Crouzon syndromes with proptosis, findings on cephalometric analysis suggested a different etiology for the proptosis in different syndromic conditions [51]. The authors argue that differences in the sagittal plane account for these marked differences in ocular manifestations. In Crouzon syndrome, the lateral and inferior orbit walls are more recessed causing a greater degree of ocular proptosis.
Conclusions In conclusion, the literature on ocular involvement in craniosynostosis continues to grow. Recent studies suggest the need for close ophthalmic surveillance in both syndromic and non-syndromic cases of craniosynostosis. The etiology of vision loss is multifactorial and modalities for visual monitoring continue to evolve. We have a greater understanding of the mechanical forces that contribute to orbital dysmorphology and their role in causing strabismus, amblyogenic refractive error, and optic neuropathy. Care of craniosynostosis patients should involve collaboration amongst pediatric subspecialists, rehabilitation services, and primary pediatric providers [54–56]. At our institution, we have a multidisciplinary clinic involving neurosurgery, plastics/craniofacial surgery, ophthalmology, pediatrics, and genetics. Given the high incidence of vision and hearing impairment, these children should be assessed for any vision and hearing services that can help improve their quality of life. The published literature contains varied and sometimes contradictory data on ocular findings. We recommend establishing an international registry for prospective data collection on patients with both syndromic and non-syndromic craniosynostosis. Such a registry would help expand our current knowledge and better address questions about amblyopia risk factors and timing of craniofacial and strabismus surgeries.
Orbital Wall Changes Causing Excyclotorsion Strabismus is a well-described ocular finding in both syndromic and non-syndromic craniosynostosis. V-pattern strabismus with apparent inferior oblique overaction is a well-described finding. Various theories about the
Compliance with Ethics Guidelines Disclosures declare they have no conflict of interest to disclose.
The authors
Human and Animal Rights and Informed Consent This article contains no studies with human or animal subjects performed by the author.
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