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Validation of the Preverbal Visual Assessment (PreViAs) questionnaire
Early Human Development 90 (2014) 635–638
Contents lists available at ScienceDirect
Early Human Development journal homepage: www.elsevier.com/locate/earlhumdev
Validation of the Preverbal Visual Assessment (PreViAs) questionnaire Inés García-Ormaechea a, Inmaculada González b,c, María Duplá d, Eva Andres e, Victoria Pueyo b,⁎ a
Ophthalmology Department, Asociación Telefónica Asistencia Minusválidos (ATAM), Madrid, Spain Ophthalmology Department, Hospital Universitario Miguel Servet, Zaragoza, Spain c Aragon Health Sciences Institute (IACS), Zaragoza, Spain d Pediatric Department, Centro de Salud San Pablo, Zaragoza, Spain e Instituto de Investigación Hospital 12 de Octubre, Madrid, Spain b
a r t i c l e
i n f o
Article history: Received 11 June 2014 Received in revised form 1 August 2014 Accepted 4 August 2014 Available online xxxx Keywords: Cerebral visual impairment Delayed visual maturation Questionnaire Visual development Visual cognitive functions
a b s t r a c t Background: Visual cognitive integrative functions need to be evaluated by a behavioral assessment, which requires an experienced evaluator. The Preverbal Visual Assessment (PreViAs) questionnaire was designed to evaluate these functions, both in general pediatric population or in children with high risk of visual cognitive problems, through primary caregivers' answers. Aim: We aimed to validate the PreViAs questionnaire by comparing caregiver reports with results from a comprehensive clinical protocol. Study design: A total of 220 infants (b 2 years old) were divided into two groups according to visual development, as determined by the clinical protocol. Their primary caregivers completed the PreViAs questionnaire, which consists of 30 questions related to one or more visual domains: visual attention, visual communication, visual–motor coordination, and visual processing. Questionnaire answers were compared with results of behavioral assessments performed by three pediatric ophthalmologists. Results: Results of the clinical protocol classified 128 infants as having normal visual maturation, and 92 as having abnormal visual maturation. The specificity of PreViAs questionnaire was N 80%, and sensitivity was 64%–79%. More than 80% of the infants were correctly classified, and test–retest reliability exceeded 0.9 for all domains. Conclusions: The PreViAs questionnaire is useful to detect abnormal visual maturation in infants from birth to 24 months of age. It improves the anamnesis process in infants at risk of visual dysfunctions. © 2014 Published by Elsevier Ireland Ltd.
1. Introduction The level of visual development in a baby (i.e., the way vision integrates with other higher order cognitive functions) cannot be evaluated by means of clinical history taking or conventional ophthalmologic examination. Early detection of abnormal visual maturation, from any cause, allows us to establish close follow-up care and initiate visual stimulation strategies. To optimize higher integrative functions, which depend on ventral and dorsal efferent streams, detection and management of delayed maturation must begin before 2 years of age. Current clinical protocols for young children include electrophysiological and neuroradiologic exams. However, these tests do not clarify the integrity of the ventral and dorsal streams [1]. Symptoms may be confusing for pediatricians and ophthalmologists inexperienced in assessing preverbal infants at neurologic risk, because the abnormality is not present in ocular structures but in visual behaviors. Therefore, a structured clinical history including a behavioral visual assessment facilitates the diagnostic process [2–4]. ⁎ Corresponding author at: Pso. Isabel la Católica 3, Ophthalmology Department, Hospital Universitario Miguel Servet, 50009 Zaragoza, Spain. E-mail address: [email protected] (V. Pueyo).
http://dx.doi.org/10.1016/j.earlhumdev.2014.08.002 0378-3782/© 2014 Published by Elsevier Ireland Ltd.
Since 1980, several questionnaires have been available for completion by parents or primary caregivers. These questionnaires consist of simple questions about activities of daily living that require fast and spontaneous answers. After revising the existing questionnaires, we developed the Preverbal Visual Assessment (PreViAs) questionnaire for infants younger than 24 months [5]. It was designed to evaluate the way the infant integrates vision with other neurological functions, assessing four visual domains: visual attention, visual communication, visual–motor coordination, and visual processing. The PreViAs questionnaire has proven to be a useful scale that is easy to complete by primary caregivers [5]. The aim of this study is to evaluate the validity and reliability of the PreViAs questionnaire for use in clinical practice. 2. Methods 2.1. Questionnaire The PreViAs questionnaire consists of 30 simple yes/no questions regarding visual development in infants (Appendix A) [5]. Each question is related to at least one of the selected four cognitive domains. The score for each domain is the sum of all positive answers to the questions
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included in its assessment. The father, mother, or other primary caregiver of the infant completed the questionnaire at the beginning of the clinical visit, before the clinical evaluation. In 25% of the cases, the questionnaire was administered again within 7 days for the test–retest analysis. Although parents had received the information about the visual function of their infants, they did not know specific information about their performance on every evaluated item. The clinical protocol was performed by one of three pediatric ophthalmologists (IGO, IG and VP), who were masked to the results of the questionnaire. Visual acuity was assessed using LEA grating paddles and scored from 0 to 16 cycles per degree. The visual assessment included ocular motility, cycloplegic refraction, fundoscopy, and visual behavioral assessment. Because no standard behavioral protocol exists for the visual assessment of infants (b 24 months of age), we designed a test battery based on the VAP–CAP assessment [6]. It is a visual assessment procedure (VAP) which evaluates capacity, attention and processing (CAP) of infants. It was designed to evaluate children with visual impairments. Our clinical battery consists of 51 items that sample the same four cognitive visual abilities measured by the questionnaire: visual attention, visual communication, visual–motor coordination, and visual processing. This examination classifies visual domain scores as appropriate or not appropriate for the infant's age. Infants with at least one domain scored as not appropriate for their age were diagnosed with abnormal visual maturation (AVM), whereas infants for whom all four domains were scored as appropriate for their age, were considered to have normal visual maturation (NVM). 2.2. Patients All infants younger than 24 months of age who visited the clinic for any concern (i.e., strabismus, retinopathy of prematurity, refractive error, …) were included in the study, until all age groups reached the minimum number of children. The infants were divided into 10 groups according to age: birth to 2 months (group 1), 2 to 4 months (group 2), 4 to 6 months (group 3), 6 to 8 months (group 4), 8 to 10 months (group 5), 10 to 12 months (group 6), 12 to 15 months (group 7), 15 to 18 months (group 8), 18 to 21 months (group 9), and 21 to 24 months (group 10). The ages of preterm infants were corrected according to their gestational age at birth. 2.3. Statistical analysis Given the low prevalence of visual integrative disorders in the pediatric population, and assuming a confidence level of 95% and a test power of 80%, we required a sample size of at least 74 children. Assuming a 5% loss, the necessary sample size was calculated as ≥78 children per study group (AVM and NVM). Questionnaire domain scores were compared with the results of clinical behavioral assessments for the same four domains using ranked comparisons (Kendall's coefficient of concordance, tau). We selected cut-off points with the best balance between sensitivity and specificity for every age group. Sensitivity, specificity, and positive and negative predictive values were calculated globally and for every age group in each domain. Test–retest reliability was determined by the Spearman test, which evaluated the similarity between results of two questionnaires completed by the same person within 7 days. All procedures adhered to the tenets of the Declaration of Helsinki, and the local ethics committee (CEICA, Comité Ético de Investigación Clínica de Aragón) approved the experimental protocol. Written informed consent for participation and publication has been obtained. 3. Results A total of 220 infants were included in the study; 128 were classified as having NVM, and 92 as having AVM, according to the behavioral assessment. The diagnosis of DVM was homogeneously distributed
Table 1 Clinical and neurologic diagnoses of infants classified according to visual maturation. Diagnosis
NVM group
AVM group
Premature, n (%) Intrauterine growth restriction, n (%) Hydrocephalus, n (%) Meningitis, n (%) Neonatal seizures, n (%) Genetic or chromosomal disorder, n (%) Ocular congenital malformation, n (%) Hypoxic–ischemic encephalopathy, n (%) Motor disability (n, %) N
21 (16.41%) 15 (11.72%) 9 (7.03%) 0 (0%) 3 (2.34%) 5 (3.91%) 2 (1.56%) 2 (1.56%) 2 (1.56%) 128
25 (27.17%) 14 (15.22%) 10 (10.87%) 4 (4.35%) 5 (5.44%) 3 (3.26%) 2 (2.17%) 12 (13.04%) 6 (6.52%) 92
Abbreviations: NVM, normal visual maturation; AVM, abnormal visual maturation.
among the 10 age groups, each of which consisted of at least eight infants with NVM, and eight with AVM. Mean age was 10.60 months (standard deviation [SD] 6.79) in the NVM group, and 11.20 months (SD 7.22) in the AVM group. The male to female ratio was similar in both groups (NVM 53.5% males, AVM 56.5% males). Gestational age at birth was 38.30 weeks in the NVM group, and 37.45 weeks in the AVM group (p = 0.089). Weight at birth was higher in the NVM group, but this difference was not significant (NVM 2940 g, AVM 2714 g; p = 0.079). Table 1 shows the clinical and neurological diagnoses, and Table 2 shows the visual characteristics of the infants. Cut-off points were selected for each visual domain and each age group. With the selected cut-off points, the specificity of the PreViAs questionnaire exceeded 80%, with sensitivity ranged from 64% to 79% (Table 3). More than 80% of the infants were correctly classified by the questionnaire. Test accuracy was good for all domains, and the area under the receiver operating characteristic ranged from 0.744 to 0.829. Test–retest reliability was very high, exceeding 0.9 for all domains (0.97 for visual attention, 0.94 for visual communication, 0.98 for visual–motor coordination, and 0.98 for visual processing). 4. Discussion Early or congenital visual dysfunctions impair neurocognitive development in infants and interfere with related functions such as attention, sequential memory, motor development, communication, and learning [7,8]. Accurate diagnosis allows the initiation of structured habilitative strategies, which are crucial to minimize the consequences of AVM on future visual function and global development. Quality instruments facilitate developmental surveillance, especially in children at risk [9]. In children with neuro-ophthalmologic disorders, questionnaires focusing on visual behaviors improve the process of history taking, and parents or other primary caregivers are important sources of information about the acquisition of certain visual behaviors [10–12]. Visual development questionnaires can be used to assess the Table 2 Results of visual assessment for infants classified according to visual maturation. Results
NVM group
AVM group
Best corrected visual acuity (cpd), mean (SD) Abnormal fixation, n (%) Abnormal pursuit, n (%) Abnormal saccades, n (%) Spherical equivalent refractive error, mean (SD) Strabismus, n (%) Oculomotor apraxia, n (%) Nystagmus, n (%) Fundoscopy findings, n (%) Optic nerve pallor Retinal anomalies N
5.80 (3.11) 8 (6.25%) 13 (10.16%) 19 (14.84%) 1.61 (5.57) 19 (14.84%) 3 (2.34%) 3 (2.34%)
3.54 (4.29) 34 (37.02%) 50 (54.35%) 52 (56.52%) 3.02 (8.49) 38 (41.30%) 15 (16.30%) 1 (1.09%)
5 (3.91%) 2 (1.56%) 128
21 (22.83%) 5 (5.43%) 92
Abbreviations: NVM, normal visual maturation; AVM, abnormal visual maturation, cpd, cycles per degree.
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Table 3 Accuracy indices for the four domains of the PreViAs questionnaire. Domain
Sensitivity
Specificity
PPV
NPV
AUC
Visual attention Visual communication Visual–motor coordination Visual processing
79.2% 64.2% 77.9% 67.5%
86.5% 89.5% 81.5% 81.3%
62.3% 72.9% 65.4% 67.5%
93.7% 85.0% 89.1% 81.3%
0.829 (0.756–0.902) 0.768 (0.693–0.843) 0.797 (0.730–0.864) 0.744 (0.673–0.815)
Abbreviations: AUC, area under the curve; NPV, negative predictive value; PPV, positive predictive value.
performance of the afferent visual pathways, [8,13] or evaluate the function of the dorsal and ventral efferent visual streams [6,14]. The increasing number of available questionnaires is due to changes in the epidemiology of severe visual impairment that have occurred during the last three decades. Cerebral visual impairment is now the leading cause of severe visual impairment, [15] requiring questions that focus on visual behavior to improve clinical history taking. In addition, some questionnaires are used to evaluate visual development in children with associated impairments such as cerebral palsy, syndromes, or malformative encephalopathy [6,14]. For this purpose, the VAP–CAP Handbook by Blanksby organizes behaviors related to four visual domains (visual attention, visual communication, visual–motor coordination, and visual processing) according to chronological age [6]. Other questionnaires include specific items that are able to detect cerebral visual impairment in children with normal afferent pathways and good visual acuity [7,14,16,17]; however, none of these questionnaires takes the child's age into account when interpreting the answers. Although questionnaires have been designed to detect visual– perceptive disorders in school-age children, [4,16] we identified a need for a questionnaire to assess visual cognitive functions in very young children. We designed the PreViAs questionnaire to provide a useful tool for the complex process of detecting visual impairment and identifying the specific cognitive dysfunction. To optimize validity, a questionnaire should be written in the primary language of the individuals who will complete it. The PreViAs questionnaire was therefore written in Spanish and validated in a Spanish-speaking population. To use the scale in another language, it would be most appropriate to first adapt and validate its use in the other language. Nearly half of the infants with AVM in our study exhibited normal fixation, tracking, and saccadic movements, and only 28% had any sign of pathology in the fundoscopic examination. Cognitive visual problems frequently remain undiagnosed until the child is older and begins to have difficulties carrying out activities of daily living [18]. These unrecognized visual dysfunctions can mimic intellectual or social disorders [19]; therefore, transdisciplinary assessment is needed to identify the existing deficits. Accurate information about visual functioning and cognitive visual abilities should be given to all physicians, pediatricians, neurologists, and therapists working with the infant. The PreViAs questionnaire was designed to help with the process of history taking and to discriminate the infants requiring further cognitive visual examinations. Desirable characteristics of developmental screening questionnaires are standardization, reliability, validity, and criterion-related reliability (i.e., sensitivity, specificity, and positive and negative predictive value) [20]. Standardization and internal consistency of the PreViAs questionnaire has already been demonstrated in a sample of 298 children recruited from patients attending a primary care center for routine visits [5]. Concurrent validation was performed with a test battery that samples the same visual domains in the same age ranges as the questionnaire. As previously reported, the validity of the PreViAs questionnaire is good in infants from birth to 24 months of age. The questionnaire accurately identifies children with AVM, as shown by the criterion-related validity. Although the sensitivity and specificity of a questionnaire should be greater than 70%, the sensitivity of our questionnaire is slightly lower than 70% for two domains. The lowest value of sensitivity was found in the youngest infants (from 0 to 2 months of age). When this age group was excluded from the
analysis, sensitivity was greater than 70% for all the domains in the remaining infants. However, specificity exceeds 80% for all four domains, which is desirable because there are many more children with normal visual development than there are children with AVM in the global pediatric population. With the selected cut-off points the negative predictive values are high, but the positive predictive values are slightly low. The consequences of cognitive visual problems remaining undiagnosed may be important for the infant's development. For this reason, our questionnaire provides two different cut-off levels: the first one, as previously reported, has a good sensitivity–specificity balance, and a second one, provides sensitivity levels higher than 95% for every age group and domain. When results are between these two cut-off points we recommend repeating the questionnaire in one month. The main limitations of the study derive from the early age of the infants and the concomitant disabilities. Motor or hearing problems may hinder the assessment of visual cognitive function in young infants and they may thus interfere with some of the asked behaviors. To minimize this influence we inform parents to answer the questions trying to take into account only the visual function of their children. Abnormal results found in infants younger than 2 months of age should be taken with caution since predictive values are low in this group. Our findings demonstrate that the PreViAs questionnaire is a useful tool for the early detection of AVM. In addition, it may be useful to assess the follow-up care of infants with AVM. However, additional studies are needed to determine the accuracy of the PreViAs questionnaire in certain groups of children at risk (such as those with hypoxic–ischemic encephalopathy) and in the prediction of long-term cognitive visual difficulties. Conflict of interest statement None of the authors has any conflict of interest. Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.earlhumdev.2014.08.002. References [1] Braddick O, Atkinson J. Development of human visual function. Vis Res 2011;51: 1588–609. [2] Lheman SS. Cortical visual impairment in children: identification, evaluation and diagnosis. Curr Opin Ophthalmol 2012;23:384–7. [3] Dutton G. Cognitive vision, its disorders and diagnosis in adults and children: knowing were and what things are. Eye 2003;17:289–304. [4] Van Genderen M, Dekker M, Pilon F, Bals I. Diagnosing cerebral visual impairment in children with good visual acuity. Strabismus 2012;20:78–83. [5] Pueyo V, García-Ormaechea I, Gonzalez I, Ferrer C, de la Mata G, Duplá M, et al. Development of the Preverbal Visual Assesment (PreViAs) questionnaire. Early Hum Dev 2014;90:165–8. [6] Blanksby DC. Visual assessment and programming: The VAP-CAP handbook. Australia: Royal Institute for the Blind; 1993. [7] Ahmed M, Dutton GN. The cognitive visual dysfunction in a child with cerebral damage. Dev Med Child Neurol 1996;38:736–43. [8] Cass HD, Sonksen PM, McConachie HR. Developmental setback in severe visual impairment. In: Sonksen PM, Silver J, editors. The Sonksen-Silver Acuity Sistem. Keeler Ltd.; 1988 [9] Glascoe FP. Screening for developmental and behavioral problems. Ment Retard Dev Disabil Res Rev 2005;11:173–9.
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[10] Diamond K, Squires J. The role of parental report in the screening and assessment of young children. J Early Interv 1993;17:107–15. [11] Glascoe FP, Dworkin PH. The role of parents in the detection of developmental and behavioral problems. Pediatrics 1995;95:829–35. [12] Squires J, Nickel R, Bricker D. Use of parent-completed developmental questionnaires for child-find and screening. Infant Young Child 1990;3:46–57. [13] Atkinson J, Anker S, Rae S, Hughes C, Braddick O. A test battery of child development for examining functional vision (ABCDEFV). Strabismus 2002;10:245–69. [14] Mc Culloch DL, Mackie RT, Dutton G, Bradnam MS, Day RE, McDaid GJ, et al. A visual skils inventory for children with neurological impairments. Dev Med Child Neurol 2007;49:757–63. [15] Jan JE. Changing patterns of visual impairment. Dev Med Child Neurol 2001;43:219.
[16] Roman-Lanzy C. Cortical Visual Impairment. An approach to assessment and intervention. American Foundation for the Blind. ABC Press; 2008. [17] Ferzinger NB, Nemet P, Brezner A, Feldman R, Galili G, Zovotofsky AZ. Visual assessment in children with cerebral palsy: implementation of a functional questionnaire. Dev Med Child Neurol 2011;53:422–8. [18] Fazzi E, Signorini G, Bova SM, La Piana R, Ondei P, Bertone C, et al. Spectrum of visual disorders in children with cerebral visual impairment. J Child Neurol 2007;22: 294–301. [19] Dale N, Sonksen P. Development outcome, including setback, in young children with severe visual impairment. Dev Med Child Neurol 2002;44:613–22. [20] Glascoe FP. Standards for screening test construction. Available at: www.dbpeds.org.
Contents lists available at ScienceDirect
Early Human Development journal homepage: www.elsevier.com/locate/earlhumdev
Validation of the Preverbal Visual Assessment (PreViAs) questionnaire Inés García-Ormaechea a, Inmaculada González b,c, María Duplá d, Eva Andres e, Victoria Pueyo b,⁎ a
Ophthalmology Department, Asociación Telefónica Asistencia Minusválidos (ATAM), Madrid, Spain Ophthalmology Department, Hospital Universitario Miguel Servet, Zaragoza, Spain c Aragon Health Sciences Institute (IACS), Zaragoza, Spain d Pediatric Department, Centro de Salud San Pablo, Zaragoza, Spain e Instituto de Investigación Hospital 12 de Octubre, Madrid, Spain b
a r t i c l e
i n f o
Article history: Received 11 June 2014 Received in revised form 1 August 2014 Accepted 4 August 2014 Available online xxxx Keywords: Cerebral visual impairment Delayed visual maturation Questionnaire Visual development Visual cognitive functions
a b s t r a c t Background: Visual cognitive integrative functions need to be evaluated by a behavioral assessment, which requires an experienced evaluator. The Preverbal Visual Assessment (PreViAs) questionnaire was designed to evaluate these functions, both in general pediatric population or in children with high risk of visual cognitive problems, through primary caregivers' answers. Aim: We aimed to validate the PreViAs questionnaire by comparing caregiver reports with results from a comprehensive clinical protocol. Study design: A total of 220 infants (b 2 years old) were divided into two groups according to visual development, as determined by the clinical protocol. Their primary caregivers completed the PreViAs questionnaire, which consists of 30 questions related to one or more visual domains: visual attention, visual communication, visual–motor coordination, and visual processing. Questionnaire answers were compared with results of behavioral assessments performed by three pediatric ophthalmologists. Results: Results of the clinical protocol classified 128 infants as having normal visual maturation, and 92 as having abnormal visual maturation. The specificity of PreViAs questionnaire was N 80%, and sensitivity was 64%–79%. More than 80% of the infants were correctly classified, and test–retest reliability exceeded 0.9 for all domains. Conclusions: The PreViAs questionnaire is useful to detect abnormal visual maturation in infants from birth to 24 months of age. It improves the anamnesis process in infants at risk of visual dysfunctions. © 2014 Published by Elsevier Ireland Ltd.
1. Introduction The level of visual development in a baby (i.e., the way vision integrates with other higher order cognitive functions) cannot be evaluated by means of clinical history taking or conventional ophthalmologic examination. Early detection of abnormal visual maturation, from any cause, allows us to establish close follow-up care and initiate visual stimulation strategies. To optimize higher integrative functions, which depend on ventral and dorsal efferent streams, detection and management of delayed maturation must begin before 2 years of age. Current clinical protocols for young children include electrophysiological and neuroradiologic exams. However, these tests do not clarify the integrity of the ventral and dorsal streams [1]. Symptoms may be confusing for pediatricians and ophthalmologists inexperienced in assessing preverbal infants at neurologic risk, because the abnormality is not present in ocular structures but in visual behaviors. Therefore, a structured clinical history including a behavioral visual assessment facilitates the diagnostic process [2–4]. ⁎ Corresponding author at: Pso. Isabel la Católica 3, Ophthalmology Department, Hospital Universitario Miguel Servet, 50009 Zaragoza, Spain. E-mail address: [email protected] (V. Pueyo).
http://dx.doi.org/10.1016/j.earlhumdev.2014.08.002 0378-3782/© 2014 Published by Elsevier Ireland Ltd.
Since 1980, several questionnaires have been available for completion by parents or primary caregivers. These questionnaires consist of simple questions about activities of daily living that require fast and spontaneous answers. After revising the existing questionnaires, we developed the Preverbal Visual Assessment (PreViAs) questionnaire for infants younger than 24 months [5]. It was designed to evaluate the way the infant integrates vision with other neurological functions, assessing four visual domains: visual attention, visual communication, visual–motor coordination, and visual processing. The PreViAs questionnaire has proven to be a useful scale that is easy to complete by primary caregivers [5]. The aim of this study is to evaluate the validity and reliability of the PreViAs questionnaire for use in clinical practice. 2. Methods 2.1. Questionnaire The PreViAs questionnaire consists of 30 simple yes/no questions regarding visual development in infants (Appendix A) [5]. Each question is related to at least one of the selected four cognitive domains. The score for each domain is the sum of all positive answers to the questions
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included in its assessment. The father, mother, or other primary caregiver of the infant completed the questionnaire at the beginning of the clinical visit, before the clinical evaluation. In 25% of the cases, the questionnaire was administered again within 7 days for the test–retest analysis. Although parents had received the information about the visual function of their infants, they did not know specific information about their performance on every evaluated item. The clinical protocol was performed by one of three pediatric ophthalmologists (IGO, IG and VP), who were masked to the results of the questionnaire. Visual acuity was assessed using LEA grating paddles and scored from 0 to 16 cycles per degree. The visual assessment included ocular motility, cycloplegic refraction, fundoscopy, and visual behavioral assessment. Because no standard behavioral protocol exists for the visual assessment of infants (b 24 months of age), we designed a test battery based on the VAP–CAP assessment [6]. It is a visual assessment procedure (VAP) which evaluates capacity, attention and processing (CAP) of infants. It was designed to evaluate children with visual impairments. Our clinical battery consists of 51 items that sample the same four cognitive visual abilities measured by the questionnaire: visual attention, visual communication, visual–motor coordination, and visual processing. This examination classifies visual domain scores as appropriate or not appropriate for the infant's age. Infants with at least one domain scored as not appropriate for their age were diagnosed with abnormal visual maturation (AVM), whereas infants for whom all four domains were scored as appropriate for their age, were considered to have normal visual maturation (NVM). 2.2. Patients All infants younger than 24 months of age who visited the clinic for any concern (i.e., strabismus, retinopathy of prematurity, refractive error, …) were included in the study, until all age groups reached the minimum number of children. The infants were divided into 10 groups according to age: birth to 2 months (group 1), 2 to 4 months (group 2), 4 to 6 months (group 3), 6 to 8 months (group 4), 8 to 10 months (group 5), 10 to 12 months (group 6), 12 to 15 months (group 7), 15 to 18 months (group 8), 18 to 21 months (group 9), and 21 to 24 months (group 10). The ages of preterm infants were corrected according to their gestational age at birth. 2.3. Statistical analysis Given the low prevalence of visual integrative disorders in the pediatric population, and assuming a confidence level of 95% and a test power of 80%, we required a sample size of at least 74 children. Assuming a 5% loss, the necessary sample size was calculated as ≥78 children per study group (AVM and NVM). Questionnaire domain scores were compared with the results of clinical behavioral assessments for the same four domains using ranked comparisons (Kendall's coefficient of concordance, tau). We selected cut-off points with the best balance between sensitivity and specificity for every age group. Sensitivity, specificity, and positive and negative predictive values were calculated globally and for every age group in each domain. Test–retest reliability was determined by the Spearman test, which evaluated the similarity between results of two questionnaires completed by the same person within 7 days. All procedures adhered to the tenets of the Declaration of Helsinki, and the local ethics committee (CEICA, Comité Ético de Investigación Clínica de Aragón) approved the experimental protocol. Written informed consent for participation and publication has been obtained. 3. Results A total of 220 infants were included in the study; 128 were classified as having NVM, and 92 as having AVM, according to the behavioral assessment. The diagnosis of DVM was homogeneously distributed
Table 1 Clinical and neurologic diagnoses of infants classified according to visual maturation. Diagnosis
NVM group
AVM group
Premature, n (%) Intrauterine growth restriction, n (%) Hydrocephalus, n (%) Meningitis, n (%) Neonatal seizures, n (%) Genetic or chromosomal disorder, n (%) Ocular congenital malformation, n (%) Hypoxic–ischemic encephalopathy, n (%) Motor disability (n, %) N
21 (16.41%) 15 (11.72%) 9 (7.03%) 0 (0%) 3 (2.34%) 5 (3.91%) 2 (1.56%) 2 (1.56%) 2 (1.56%) 128
25 (27.17%) 14 (15.22%) 10 (10.87%) 4 (4.35%) 5 (5.44%) 3 (3.26%) 2 (2.17%) 12 (13.04%) 6 (6.52%) 92
Abbreviations: NVM, normal visual maturation; AVM, abnormal visual maturation.
among the 10 age groups, each of which consisted of at least eight infants with NVM, and eight with AVM. Mean age was 10.60 months (standard deviation [SD] 6.79) in the NVM group, and 11.20 months (SD 7.22) in the AVM group. The male to female ratio was similar in both groups (NVM 53.5% males, AVM 56.5% males). Gestational age at birth was 38.30 weeks in the NVM group, and 37.45 weeks in the AVM group (p = 0.089). Weight at birth was higher in the NVM group, but this difference was not significant (NVM 2940 g, AVM 2714 g; p = 0.079). Table 1 shows the clinical and neurological diagnoses, and Table 2 shows the visual characteristics of the infants. Cut-off points were selected for each visual domain and each age group. With the selected cut-off points, the specificity of the PreViAs questionnaire exceeded 80%, with sensitivity ranged from 64% to 79% (Table 3). More than 80% of the infants were correctly classified by the questionnaire. Test accuracy was good for all domains, and the area under the receiver operating characteristic ranged from 0.744 to 0.829. Test–retest reliability was very high, exceeding 0.9 for all domains (0.97 for visual attention, 0.94 for visual communication, 0.98 for visual–motor coordination, and 0.98 for visual processing). 4. Discussion Early or congenital visual dysfunctions impair neurocognitive development in infants and interfere with related functions such as attention, sequential memory, motor development, communication, and learning [7,8]. Accurate diagnosis allows the initiation of structured habilitative strategies, which are crucial to minimize the consequences of AVM on future visual function and global development. Quality instruments facilitate developmental surveillance, especially in children at risk [9]. In children with neuro-ophthalmologic disorders, questionnaires focusing on visual behaviors improve the process of history taking, and parents or other primary caregivers are important sources of information about the acquisition of certain visual behaviors [10–12]. Visual development questionnaires can be used to assess the Table 2 Results of visual assessment for infants classified according to visual maturation. Results
NVM group
AVM group
Best corrected visual acuity (cpd), mean (SD) Abnormal fixation, n (%) Abnormal pursuit, n (%) Abnormal saccades, n (%) Spherical equivalent refractive error, mean (SD) Strabismus, n (%) Oculomotor apraxia, n (%) Nystagmus, n (%) Fundoscopy findings, n (%) Optic nerve pallor Retinal anomalies N
5.80 (3.11) 8 (6.25%) 13 (10.16%) 19 (14.84%) 1.61 (5.57) 19 (14.84%) 3 (2.34%) 3 (2.34%)
3.54 (4.29) 34 (37.02%) 50 (54.35%) 52 (56.52%) 3.02 (8.49) 38 (41.30%) 15 (16.30%) 1 (1.09%)
5 (3.91%) 2 (1.56%) 128
21 (22.83%) 5 (5.43%) 92
Abbreviations: NVM, normal visual maturation; AVM, abnormal visual maturation, cpd, cycles per degree.
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Table 3 Accuracy indices for the four domains of the PreViAs questionnaire. Domain
Sensitivity
Specificity
PPV
NPV
AUC
Visual attention Visual communication Visual–motor coordination Visual processing
79.2% 64.2% 77.9% 67.5%
86.5% 89.5% 81.5% 81.3%
62.3% 72.9% 65.4% 67.5%
93.7% 85.0% 89.1% 81.3%
0.829 (0.756–0.902) 0.768 (0.693–0.843) 0.797 (0.730–0.864) 0.744 (0.673–0.815)
Abbreviations: AUC, area under the curve; NPV, negative predictive value; PPV, positive predictive value.
performance of the afferent visual pathways, [8,13] or evaluate the function of the dorsal and ventral efferent visual streams [6,14]. The increasing number of available questionnaires is due to changes in the epidemiology of severe visual impairment that have occurred during the last three decades. Cerebral visual impairment is now the leading cause of severe visual impairment, [15] requiring questions that focus on visual behavior to improve clinical history taking. In addition, some questionnaires are used to evaluate visual development in children with associated impairments such as cerebral palsy, syndromes, or malformative encephalopathy [6,14]. For this purpose, the VAP–CAP Handbook by Blanksby organizes behaviors related to four visual domains (visual attention, visual communication, visual–motor coordination, and visual processing) according to chronological age [6]. Other questionnaires include specific items that are able to detect cerebral visual impairment in children with normal afferent pathways and good visual acuity [7,14,16,17]; however, none of these questionnaires takes the child's age into account when interpreting the answers. Although questionnaires have been designed to detect visual– perceptive disorders in school-age children, [4,16] we identified a need for a questionnaire to assess visual cognitive functions in very young children. We designed the PreViAs questionnaire to provide a useful tool for the complex process of detecting visual impairment and identifying the specific cognitive dysfunction. To optimize validity, a questionnaire should be written in the primary language of the individuals who will complete it. The PreViAs questionnaire was therefore written in Spanish and validated in a Spanish-speaking population. To use the scale in another language, it would be most appropriate to first adapt and validate its use in the other language. Nearly half of the infants with AVM in our study exhibited normal fixation, tracking, and saccadic movements, and only 28% had any sign of pathology in the fundoscopic examination. Cognitive visual problems frequently remain undiagnosed until the child is older and begins to have difficulties carrying out activities of daily living [18]. These unrecognized visual dysfunctions can mimic intellectual or social disorders [19]; therefore, transdisciplinary assessment is needed to identify the existing deficits. Accurate information about visual functioning and cognitive visual abilities should be given to all physicians, pediatricians, neurologists, and therapists working with the infant. The PreViAs questionnaire was designed to help with the process of history taking and to discriminate the infants requiring further cognitive visual examinations. Desirable characteristics of developmental screening questionnaires are standardization, reliability, validity, and criterion-related reliability (i.e., sensitivity, specificity, and positive and negative predictive value) [20]. Standardization and internal consistency of the PreViAs questionnaire has already been demonstrated in a sample of 298 children recruited from patients attending a primary care center for routine visits [5]. Concurrent validation was performed with a test battery that samples the same visual domains in the same age ranges as the questionnaire. As previously reported, the validity of the PreViAs questionnaire is good in infants from birth to 24 months of age. The questionnaire accurately identifies children with AVM, as shown by the criterion-related validity. Although the sensitivity and specificity of a questionnaire should be greater than 70%, the sensitivity of our questionnaire is slightly lower than 70% for two domains. The lowest value of sensitivity was found in the youngest infants (from 0 to 2 months of age). When this age group was excluded from the
analysis, sensitivity was greater than 70% for all the domains in the remaining infants. However, specificity exceeds 80% for all four domains, which is desirable because there are many more children with normal visual development than there are children with AVM in the global pediatric population. With the selected cut-off points the negative predictive values are high, but the positive predictive values are slightly low. The consequences of cognitive visual problems remaining undiagnosed may be important for the infant's development. For this reason, our questionnaire provides two different cut-off levels: the first one, as previously reported, has a good sensitivity–specificity balance, and a second one, provides sensitivity levels higher than 95% for every age group and domain. When results are between these two cut-off points we recommend repeating the questionnaire in one month. The main limitations of the study derive from the early age of the infants and the concomitant disabilities. Motor or hearing problems may hinder the assessment of visual cognitive function in young infants and they may thus interfere with some of the asked behaviors. To minimize this influence we inform parents to answer the questions trying to take into account only the visual function of their children. Abnormal results found in infants younger than 2 months of age should be taken with caution since predictive values are low in this group. Our findings demonstrate that the PreViAs questionnaire is a useful tool for the early detection of AVM. In addition, it may be useful to assess the follow-up care of infants with AVM. However, additional studies are needed to determine the accuracy of the PreViAs questionnaire in certain groups of children at risk (such as those with hypoxic–ischemic encephalopathy) and in the prediction of long-term cognitive visual difficulties. Conflict of interest statement None of the authors has any conflict of interest. Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.earlhumdev.2014.08.002. References [1] Braddick O, Atkinson J. Development of human visual function. Vis Res 2011;51: 1588–609. [2] Lheman SS. Cortical visual impairment in children: identification, evaluation and diagnosis. Curr Opin Ophthalmol 2012;23:384–7. [3] Dutton G. Cognitive vision, its disorders and diagnosis in adults and children: knowing were and what things are. Eye 2003;17:289–304. [4] Van Genderen M, Dekker M, Pilon F, Bals I. Diagnosing cerebral visual impairment in children with good visual acuity. Strabismus 2012;20:78–83. [5] Pueyo V, García-Ormaechea I, Gonzalez I, Ferrer C, de la Mata G, Duplá M, et al. Development of the Preverbal Visual Assesment (PreViAs) questionnaire. Early Hum Dev 2014;90:165–8. [6] Blanksby DC. Visual assessment and programming: The VAP-CAP handbook. Australia: Royal Institute for the Blind; 1993. [7] Ahmed M, Dutton GN. The cognitive visual dysfunction in a child with cerebral damage. Dev Med Child Neurol 1996;38:736–43. [8] Cass HD, Sonksen PM, McConachie HR. Developmental setback in severe visual impairment. In: Sonksen PM, Silver J, editors. The Sonksen-Silver Acuity Sistem. Keeler Ltd.; 1988 [9] Glascoe FP. Screening for developmental and behavioral problems. Ment Retard Dev Disabil Res Rev 2005;11:173–9.
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