Diagnosing Cerebral Visual Impairment in Children with Good Visual Acuity

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1 Strabismus, 20(2), 78 83, 2012 ISSN: print/ online DOI: / Original Article Diagnosing Cerebral Visual Impairment in Children with Good Visual Acuity Maria van Genderen 1, Marjoke Dekker 1, Florine Pilon 1, and Irmgard Bals 2 1 Department of Ophthalmology, Bartiméus Institute for the Visually Impaired and 2 Department of Psychology, Bartiméus institute for the Visually Impaired ABSTRACT Purpose: To identify elements that could facilitate the diagnosis of cerebral visual impairment (CVI) in children with good visual acuity in the general ophthalmic clinic. Methods: We retrospectively investigated the clinical characteristics of 30 children with good visual acuity and CVI and compared them with those of 23 children who were referred with a suspicion of CVI, but proved to have a different diagnosis. Clinical characteristics included medical history, MRI findings, visual acuity, crowding ratio (CR), visual field assessment, and the results of ophthalmologic and orthoptic examination. We also evaluated the additional value of a short CVI questionnaire. Results: Eighty-three percent of the children with an abnormal medical history (mainly prematurity and perinatal hypoxia) had CVI, in contrast with none of the children with a normal medical history. Cerebral palsy, visual field defects, and partial optic atrophy only occurred in the CVI group. 41% of the children with CVI had a CR 2.0, which may be related to dorsal stream dysfunction. All children with CVI, but also 91% of the children without CVI gave 3 affirmative answers on the CVI questionnaire. Conclusion: An abnormal pre- or perinatal medical history is the most important risk factor for CVI in children, and therefore in deciding which children should be referred for further multidisciplinary assessment. Additional symptoms of cerebral damage, i.e., cerebral palsy, visual field defects, partial optic atrophy, and a CR 2 may support the diagnosis. CVI questionnaires should not be used for screening purposes as they yield too many false positives. KEYWORDS: Cerebral visual impairment, crowding, CVI questionnaire, visual acuity INTRODUCTION Cerebral visual impairment (CVI) is considered the most important cause of visual dysfunction in children in developed countries. The spectrum of CVI includes neurophthalmological abnormalities such as decreased visual acuity, visual field defects, and oculomotor problems, in combination with cognitive visual dysfunction. Two functional visual pathways responsible for cognitive visual function have been described (Goodale & Milner, 1992). The dorsal stream runs to the posterior parietal cortex and is concerned with visual-spatial abilities, for instance, extracting information from a crowded visual scene, and visually guided movement (Dutton et al., 2004). The ventral stream runs to the inferior temporal cortex and is concerned with visual object recognition and route finding. Diagnosing CVI in the general ophthalmic clinic may be difficult due to time constraints, the poor attention span of children, and the variability of the symptoms. For that reason, ophthalmologists and orthoptists in the Netherlands refer children to specialized institutes for the visually impaired, e.g., Bartiméus and Royal Visio, for multidisciplinary assessment. However, they generally use the WHO (ICD-9-CM) criteria on low vision, e.g., a visual acuity below 20/60 or a visual field of 20 degrees or less, for referral to these institutes. Although the majority of children with CVI have low vision, cognitive visual impairment may occur despite normal or near normal visual acuity (Fazzi et al., 2009; Saidkasimova et al., 2007). Consequently, there may be under-referral of children with CVI who have good visual acuity, because they are not recognized as having a visual impairment. Received 16 September 2011; revised 20 January 2012; accepted 26 February 2012 Address for Correspondence: Maria M. van Genderen, P.O. Box 1003, 3700 BA Zeist, The Netherlands. mvgenderen@bartimeus.nl 78

2 CVI in Children with Good Visual Acuity 79 The purpose of this study was to identify elements that, in the general ophthalmic clinic, could facilitate the diagnosis of CVI in children with good visual acuity, and thus aid in deciding which children should be referred to specialized institutes for multidisciplinary assessment. The diagnostic methods should require only a limited period of time and make use of commonly available investigative tools. We therefore retrospectively investigated the clinical characteristics of 30 children with good visual acuity and CVI, and compared them with those of 23 children that proved to have a different diagnosis. PATIENTS AND METHODS Over a period of 2 years, 53 school-going children with good binocular visual acuity, mean age 8 years, range 5-16 years, were referred to our institute with a suspicion of CVI. As part of the standard procedure, all children had a detailed visual assessment and full ophthalmologic and orthoptic examination. Subsequently the children were examined by experienced child psychologists with a (neuro)psychological test battery, with special attention to visual perception and visual cognitive functions. The performance was established in comparison to nonverbal intelligence subtests appropriate for the child s age and cognitive abilities (Wechsler Intelligence Scales) This way, the psychologists established CVI in 30 children, while 23 children proved to have a different diagnosis, for instance attention deficit disorder, developmental coordination disorder, and/or learning problems. We then retrospectively investigated the clinical characteristics of both groups. Clinical characteristics included medical history, MRI findings, visual acuity, crowding ratio (CR), visual field assessment, and the results of ophthalmologic and orthoptic examination. We calculated the CR by dividing the single (binocular) optotype acuity by the linear acuity (Atkinson et al., 1988; Rydberg et al., 1999). A CR 2.0 is considered abnormal regardless of age (Pike et al., 1994). In children with abnormal crowding, dynamic retinoscopy was performed to exclude a possible influence of impaired accommodation. The visual fields were mainly evaluated by confrontation techniques; some older children underwent Goldmann perimetry. We measured cycloplegic refraction in all children; significant refractive errors were defined as myopia >-1.0, hyperopia 2.0, or astigmatism >1.0 diopters. We also evaluated the additional value of a short CVI questionnaire, consisting of 7 questions on dorsal stream dysfunction and 5 on ventral stream dysfunction (see Appendix). We developed this questionnaire some years ago to quickly investigate possible CVI-related symptoms in the ophthalmic clinic. We selected the questions from the much more extensive Structured History Taking (Houliston et al., 1999); the selection was based on problems that were most frequently reported in children with CVI. The study adhered to the Declaration of Helsinki. RESULTS Children With CVI, N = 30 (Table 1) All 30 children had an abnormal medical history: 21 were born prematurely before 35 weeks of gestation, 7 suffered perinatal asphyxia, and 2 had a developmental brain abnormality. Twenty children had mild to moderate cerebral palsy, 8 children had epilepsy. Eighty-six percent of the children (24/28) had MRI abnormalities; prematurely born children mainly had periventricular leucomalacia (PVL), while perinatal hypoxic-ischaemic events in term-born children mostly resulted in cerebral infarction. MRI findings were considered normal in 4 children; in 2 children no MRI had been made. All children had a single optotype acuity of more than 20/40 (less than 0.3 LogMAR), 6 children had a visual acuity of 20/20 (0.0 LogMAR); 41% (12/29) had a crowding ratio 2.0. Visual field defects were found in 53% (16/30) of the children. Ophthalmic examination showed partial optic atrophy in 5 children and significant refractive error in 3 (2 hyperopia, 1 myopia); 10 children had nystagmus. The CVI questionnaire showed 3 or more affirmative answers in all children; dorsal stream problems were reported more frequently than ventral stream problems. Children Without CVI, N = 23 (Table 2) Six children (26%) had an abnormal medical history: 4 were born prematurely; 1 had hydrocephalus, and 1 child had epilepsy. MRI was performed in 6 children, only 1 (16%, 1/6) was abnormal. None of these children had cerebral palsy. All children had a single optotype acuity of more than 20/30 (0.18 LogMAR); 14 children had acuity of 20/20 (0.0 LogMAR). Only one child had a crowding ratio of 2.0. All children had full visual fields. Ophthalmic examination showed significant hyperopia in 9 children and myopia in 1. One child had nystagmus; funduscopy was normal in all children. The CVI questionnaire showed 3 or more affirmative answers in 91% (21/23). Figure 1 shows the frequency of the clinical characteristics in both groups. DISCUSSION We retrospectively evaluated the clinical characteristics of 30 children with CVI and 23 children without CVI, all with normal or near normal visual acuity. Our study shows that an uneventful medical history makes CVI very unlikely. Out of 53 children,

3 80 M. van Genderen et al. TABLE 1 Details of clinical characteristics of 30 children with CVI Case No Medical history MRI cp BNVA CR V/F quest ophthal nys 1 peri infarction lower 6d N 2 pre PVL N 6d refr 3 pre N N 4d refr + 4 pre hydroc N 5d N 5 pre N N 4d N + 6 pre PVL hemi 3d, 2v N 7 pre infarction quadr 5d N 8 peri np N 4d, 2v N 9 pre hydroc hemi 5d, 1v N 10 pre PVL lower 3d p opt atr 11 peri, epilepsy infarction N 2v N 12 peri, epilepsy infarction lower 5d p opt atr + 13 pre, epilepsy PVL, hydroc N 4d N 14 peri, epilepsy infarction N 4d p opt atr + 15 pre PVL narrow 3d N 16 pre np N 3d N 17 pre, epilepsy PVL narrow 3d, 3v p opt atr 18 pre PVL hemi 3d N 19 pre N N 5d, 3v p opt atr + 20 peri infarction, cyst N 3d p opt atr + 21 pre PVL upper 4d, 1v N 22 pre PVL lower 2d, 1v N 23 pre, epilepsy PVL np narrow 6d N + 24 pre PVL N 2d, 1v N 25 pre PVL lower 5d N + 26 pre PVL N 5d N + 27 pre PVL lower 4d N 28 peri, epilepsy N hemi 3d, 4v N 29 brain dev abn dev abn N 5d, 1v refr 30 brain dev abn, epilepsy dev abn narrow 5d, 1v N Pre = prematurity; peri = perinatal hypoxic ischemic event; N = normal; np = not performed; dev abn = developmental abnormalities; hydroc = hydrocephalus; cp = cerebral palsy; BNVA = binocular visual acuity; CR = crowding ratio; V/F = visual fields; hemi = homonymous hemianopia, quadr = quadrantanopia; quest = number of affirmative answers on the CVI questionnaire; 4d,2v = four affirmative answers on dorsal stream dysfunction, two on ventral stream dysfunction; ophthal = ophthalmological and orthoptic examination; p opt atr = partial optic atrophy (temporal pallor and/or large cupping); refr = significant refractive error; nys = nystagmus. 16 (30%) had a normal perinatal history and were otherwise healthy; none of them proved to have CVI. In contrast, CVI was established in 83% (30/36) of the children with a medical diagnosis (mainly prematurity and perinatal hypoxia). Not surprisingly, MRI abnormalities and medical history were closely related, as can be seen in Figure 1. Four children with CVI had normal MRIs; of these, patients 3, 19, and 28 had neonatal abnormal brain ultrasonography (USG), and patient 28 still has mild cerebral palsy. These findings indicate that abnormal processing of information will not necessarily be apparent from structural brain imaging (Fazzi et al., 2009), as has also previously been reported (Ortibus et al., 2009). Homonymous visual field defects and partial optic atrophy are sequels of damage to the posterior visual pathways (Fazzi et al., 2007; Jacobson et al., 2003); these symptoms occurred exclusively in children with CVI. The 53% field loss in our series is comparable to the 57% field loss described in a previous study on 7 normally sighted children with CVI (Saidkasimova et al., 2007). Lower visual field involvement is common in PVL (Dutton et al., 2004; Jacobson et al., 2006); in some patients we also found hemianopia and narrowed fields. In some patients, notably patient 21, inattention appeared a contributing factor to the constricted field. Earlier studies reported a high prevalence of nystagmus in children with CVI (Jacobson et al., 2002, Salati et al., 2002); in our study 30% of the CVI children had nystagmus compared with only 1 child in the non-cvi group. More than 40% of the CVI children had a crowding ratio 2.0, compared with only 1 child in the non-cvi group. Crowding is related to dorsal stream dysfunction, which may lead to problems with complex visual scenes and extracting visual information (Dutton et al., 2004). We noticed that in our series abnormal crowding occurred more frequently in prematurely born children with PVL (50%, 10/20) than in term children with cerebral infarction (14%, 1/7). These findings appear to be corroborated by the literature: several Strabismus

4 CVI in Children with Good Visual Acuity 81 TABLE 2 Details of clinical characteristics of 23 children without CVI Case No history MRI cp BNVA CR V/F quest ophthal nys Psych ass 31 N np N 4d refr autism 32 pre np N 1d N cogn imp 33 N N N 3d N cogn imp 34 N np N 2d, 2v N DCD 35 N N N 6d refr DCD 36 N np N 2d, 1v N PDD NOS 37 N np N 2d N DCD 38 N np N 5d N DCD 39 N np N 4d refr DCD 40 N np N 3d, 1v refr + att dis 41 N np N 4d, 1v refr cogn imp 42 N np N 5d refr cogn imp 43 N np N 3d refr cogn imp 44 pre np N 6d refr DCD 45 N N N 4d N mot imp 46 N np N 1d, 1v N DCD 47 N np N 3d N mot imp 48 pre np N 4d, 1v refr att dis 49 N np N 4d N mot imp 50 epilepsy N N 3d N mot imp 51 hydr hydr N 3d refr mot imp 52 pre N N 6d N att dis 53 N np N 4d, 3v N att dis pre = prematurity; N = normal; np = not performed; hydr = hydrocephalus; cp = cerebral palsy; BNVA = binocular visual acuity; CR = crowding ratio; V/F = visual fields; hemi = homonymous hemianopia; quadr = quadrantanopia; quest = number of affirmative answers on the CVI questionnaire; 4d, 2v = four affirmative answers on dorsal stream dysfunction, two on ventral stream dysfunction; ophthal = ophthalmological and orthoptic examination; refr = significant refractive error; nys = nystagmus; cogn imp = cognitive impairment; psych ass = psychological assessment; DCD = developmental coordination disorder; att dis = attention deficit disorder; mot imp = motor impairment. FIGURE 1 Clinical characteristics of children with CVI (N = 30) and children without CVI (N = 23). authors described a high CR in children born preterm (Jacobson et al., 1996; Pike et al., 1994); in contrast, Mercuri reported increased crowding in only 12% of term-born children with cerebral infarction (Mercuri et al., 2003). The CVI questionnaire showed 3 positive answers not only in the CVI group, but also in the majority of children with behavioral abnormalities or learning disorders. Subsequent more extensive structured history-taking also yielded many positive answers

5 82 M. van Genderen et al. in the non-cvi group, mostly on problems related to dorsal stream dysfunction. Neuropsychological assessment revealed that several of these problems could be explained by factors other than CVI. For instance, some children who had problems walking over uneven surfaces, frequently stumbling, etc., proved to have motor problems or coordination disorders. Children with attention deficit disorder showed not only symptoms of impaired visual attention, but also of impaired attention in other fields. One of the reasons for the high number of reported problems in both groups may lie in the selection of referred patients: several orthoptists in general practice use the short questionnaire to screen for possible symptoms of CVI. The subsequently referred children may therefore constitute a biased population. Another explanation may lie in the higher number of children with hyperopia in the non-cvi group, compared with the children with CVI (39% and 7%, respectively). A study by Atkinson et al. (2002) reported that children with high hyperopia may manifest mild deficits on visuocognitive and visuomotor testing. In conclusion, our retrospective study showed that CVI in children remains primarily a clinical diagnosis that should be based on the presence of the known causes of CVI in the medical history, as this proved to be the most important risk factor. Additional symptoms of cerebral damage, e.g., cerebral palsy, visual field defects, partial optic atrophy, and/or nystagmus, may further support the diagnosis, especially when the medical history is unknown or unclear. A crowding ratio 2 may be an indication of dorsal stream dysfunction. CVI questionnaires may be useful for identifying the various symptoms of CVI in children with a suspect medical history; however, they should not be used for screening purposes as they yield too many false positives. Declaration of interest: The authors report no conflicts of interest. 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6 Appendix: short CVI questionnaire CVI in Children with Good Visual Acuity 83 dorsal stream Are there problems in Seeing an object on patterned background no/yes/sometimes Seeing something in the distance, from a car window no/yes/sometimes Finding parents or friends in a crowd no/yes/sometimes Stumbling, looking at one s feet no/yes/sometimes Judging distances when walking on different surfaces no/yes/sometimes Thresholds, staircases no/yes/sometimes Reading crowded text no/yes/sometimes ventral stream Are there problems in Recognizing faces, i.e. parents among other people no/yes/sometimes Recognizing objects no/yes/sometimes Recognizing and naming pictures no/yes/sometimes Finding the way no/yes/sometimes Reading no/yes/sometimes