Reintroducing Dyslexia: Early Identification and Implications for Pediatric Practice Joseph Sanfilippo, MS, EdM,a,b Molly Ness, PhD,c Yaacov Petscher, PhD,d Leonard Rappaport, MD, MS,a,e Barry Zuckerman, MD,f,g Nadine Gaab, PhDa,e,h

Dyslexia is a common learning disorder that renders children susceptible to abstract poor health outcomes and many elements of socioeconomic difficulty. It is commonly undiagnosed until a child has repeatedly failed to learn to read in aDivision of Developmental Medicine, Boston Children’s elementary school; this late diagnosis not only places the child at an academic Hospital, Boston, Massachusetts; bSchool of Medicine, disadvantage but also can be a precursor to psychiatric comorbidities such as Faculty of Health Sciences, Queen’s University, Kingston, Ontario, Canada; cGraduate School of Education, Fordham anxiety and depression. Genetic and neuroimaging research have revealed University, New York, New York; dFlorida Center for Reading that dyslexia is heritable and that it is undergirded by brain differences that Research, Florida State University, Tallahassee, Florida; eDepartment of Pediatrics, Harvard Medical School, Harvard are present even before reading instruction begins. Cognitive-behavioral University, Boston, Massachusetts; fDepartment of research has revealed that there are early literacy skill deficits that represent Pediatrics, School of Medicine, Boston University, Boston, fl Massachusetts; gBoston Medical Center, Boston, red ags for dyslexia risk and can be measured at a preschool age. Altogether, Massachusetts; and hHarvard Graduate School of Education, this evidence points to dyslexia as a disorder that can be flagged by Harvard University, Cambridge, Massachusetts a pediatrician before school entry, during a period of heightened brain Drs Gaab, Rappaport, and Zuckerman conceptualized plasticity when interventions are more likely to be effective. In this review, we the review, participated in the drafting of the initial discuss the clinical implications of the most recent advances in dyslexia manuscript, and continuously reviewed and revised fi the manuscript; Mr Sanfilippo conducted the research, which converge to indicate that early identi cation and screening literature review, led in the writing and design of the are crucial to the prevention or mitigation of adverse secondary final manuscript, consolidated coauthor feedback, consequences of dyslexia. We further highlight evidence-based and practical and continuously revised the manuscript; Drs Ness strategies for the implementation of early risk identification in pediatric and Petscher contributed their respective expertise in writing significant components of the manuscript practice so that physicians can be empowered in their ability to treat, educate, and reviewed and revised the manuscript and advocate for their patients and families with dyslexia. throughout; and all authors approved the final manuscript as submitted and agree to be accountable for all aspects of the work. DOI: https://doi.org/10.1542/peds.2019-3046 The development of reading proficiency experience poverty, are more likely to Accepted for publication Jan 29, 2020 in childhood is a public health issue: find employment, and achieve higher Address correspondence to Nadine Gaab, PhD, literacy is a widely recognized average incomes as adults compared Division of Developmental Medicine, Boston determinant of health outcomes and is with children who fail to achieve Children’s Hospital, 1 Autumn St, Office 643, Boston, 3 MA, 02215. E-mail: nadine.gaab@ associated with many indices of reading proficiency. For many children childrens.harvard.edu academic, social, vocational, and with reading impairments, however, the 1 process of learning to read is rife with PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, economic success. In a recent National 1098-4275). Academy of Medicine summary, the struggle and frustration, and these children are left susceptible to adverse Copyright © 2020 by the American Academy of author highlights that duration of Pediatrics secondary outcomes, including anxiety education, which is highly dependent FINANCIAL DISCLOSURE: and depression. A neurobiologically The authors have indicated on reading proficiency, is a better they have no financial relationships relevant to this based specific learning disorder, predictor of health and long life than article to disclose. dyslexia, affects 5% to 10% of cigarette smoking or obesity.2 Children children4,5 and is a persistent barrier to skilled in reading perform better in To cite: Sanfilippo J, Ness M, Petscher Y, et al. reading acquisition. school, attain higher levels of education, Reintroducing Dyslexia: Early Identification and experience lower rates of disease, are Dyslexia (or word-level reading Implications for Pediatric Practice. Pediatrics. 2020;146(1):e20193046 less likely to be incarcerated or difficulty6) is predominantly

Downloaded from www.aappublications.org/news by guest on October 6, 2021 PEDIATRICS Volume 146, number 1, July 2020:e20193046 STATE-OF-THE-ART REVIEW ARTICLE characterized by a core deficit in of children with language disorders weaknesses. The clinical implications phonological processing (the ability have dyslexia.20 Dyslexia typically of a reluctance to use dyslexia as to recognize and manipulate speech results from a core deficit in a diagnostic label include children sounds), which results in phonological processing; however, it failing to receive an adequate impairments in decoding (“sounding is important to note that language response to early risk signs, out” words), spelling, and word deficits (eg, low vocabulary or low appropriate interventions in school, recognition.7 These impairments oral listening comprehension) can and mental health support. almost always lead to difficulties in also lead to reading problems, In this article, we provide an up-to- reading fluency and comprehension, especially problems with reading date overview of dyslexia, specifically reduced vocabulary, lower content comprehension. Importantly, speech addressing common knowledge gaps, knowledge,8 and a decline in overall and language problems commonly neurobiological underpinnings of the school performance.9 Dyslexia cannot precede problems in learning to disorder, and ways in which be explained by poor hearing or read, so children with speech and pediatricians can play an active role vision, low language enrichment, or language problems should be flagged in the early identification of lack of motivation or opportunity.10 as being at increased risk for dyslexia risk. According to the Diagnostic and dyslexia.21 Statistical Manual of Mental Disorders, There are many other developmental Fifth Edition, dyslexia falls under the THE ETIOLOGY OF DYSLEXIA and psychiatric conditions that are umbrella of a “specific learning frequently comorbid with dyslexia, The etiology of dyslexia is disorder” that “impedes the ability to further jeopardizing these children’s multifaceted, including genetic, learn or use specific academic skills health and academic outcomes. In perceptual and cognitive, (eg, reading, writing, or total, 20% to 40% of children with neurobiological, and environmental arithmetic).”11 attention-deficit/hyperactivity factors.9 Dyslexia is strongly Although there are many negative disorder have dyslexia,22 and children heritable, occurring in up to 68% of outcomes associated with dyslexia, with autism spectrum disorder are identical twins of individuals with particularly salient to the pediatrician also at increased risk of having dyslexia and up to 50% of individuals is the association between dyslexia dyslexia.23 Other behavioral who have a first-degree relative with – – and poor mental health.12,13 Children disorders, such as conduct disorder dyslexia.19,28 30 Several genes31 34 with dyslexia are more likely to suffer and oppositional defiant disorder, are have been reported to be candidates from generalized anxiety14,15 and also also associated with dyslexia.24 As for dyslexia susceptibility; it is exhibit higher rates of many as 85% of children with thought that most of these genes play depression.14,16 Because screening dyspraxia (developmental a role in early brain – for dyslexia is not routinely coordination disorder) have development.31,34 38 performed, the direction of causation dyslexia,25 and children with Furthermore, various studies have between dyslexia and comorbid mood dyscalculia (math learning revealed atypical brain characteristics disorders in each case is unclear, and disorder)26 and dysgraphia (writing in individuals with dyslexia compared this uncertainty can preclude learning disorder)27 are more likely with their peers.39 In functional MRI effective early treatment. A mood to have dyslexia than those without. studies, researchers have indicated disorder may be identified in a child Knowledge of dyslexia within that reading for typical readers takes with unidentified comorbid dyslexia pediatric practice is paramount in place predominantly in left- when it is the dyslexia that is considering the most appropriate hemispheric sites of the brain, antecedent and causative, obscuring treatments for these many coexisting including the inferior frontal, superior the primary target for intervention. disorders. temporal, temporoparietal, and In addition to mood disorders, speech Despite increasing collaboration occipitotemporal cortices.40 As and language problems are frequently among educators, physicians, a group, individuals with dyslexia comorbid with dyslexia because both neuroscientists, speech and language show hypoactivation in the left- dyslexia and developmental language pathologists (SLPs), and hemisphere reading systems.41 The disorders can be characterized by psychologists, dyslexia is often structural and functional atypicalities poor phonological awareness17–19 overlooked in the field of general in these brain regions include and other language deficits (eg, oral pediatrics, perhaps because the reduced gray matter volume,42 language comprehension).20 diagnostic label of dyslexia is not hypoactivation in response to Approximately one-half of children often used in practice, having been reading-related functional MRI identified with dyslexia have language replaced largely by education tasks,43 and weaker functional disorders, and approximately one-half language of strengths and connectivity between key areas of the

Downloaded from www.aappublications.org/news by guest on October 6, 2021 2 SANFILIPPO et al reading network.44 Importantly, The classic simple view of reading a child’s language environment. In differences in brain structure and posits that skilled reading involves this review, we focus on monolingual function characteristic of dyslexia can $2 major cognitive components: English speakers, however, and, be observed before the start of formal word recognition (including decoding among these children, these key reading instruction, indicating that and phonological awareness) and linguistic and preliteracy measures dyslexia does not result from language comprehension (eg, can be assessed in children as young a struggle to learn to read but, rather, knowledge of vocabulary and as 4 years old, and they can serve as represents a biological disposition language structures); together, these crucial markers in identifying present at the preschool age or strands coalesce to form what is children at risk for dyslexia or other – perhaps as early as infancy.45–47 classically known as the “reading reading impairments.64 66 Some of Altogether, these neuroimaging rope.”57 Although the simple view of these literacy precursors measured in findings suggest that children reading has been borne out by kindergarten have been shown to predisposed to dyslexia enter their evidence,58 its components are not predict reading comprehension in the first day of school with a brain that is single entities but are multifactorial, 10th grade.67 less equipped to learn to read. malleable, and context dependent (especially language comprehension) THE DYSLEXIA PARADOX AND THE RISKS It is worth noting that reading and cannot be captured in a single OF DELAYED DIAGNOSIS proficiency is strongly associated assessment.59 Furthermore, recent – with socioeconomic status48 50: 80% research has revealed that skilled As children progress through the of fourth grade students from low reading, especially in older children, school system, reading becomes the socioeconomic backgrounds read is contingent on knowledge of expected vehicle for content learning; below grade-level proficiency.51 In academic language and the additional thus, it is imperative that children particular, children with inadequate cognitive skills of perspective-taking with dyslexia are identified early and exposure to language are more likely and reasoning.60 receive intervention without delay. to struggle with reading.52 However, When at-risk beginning readers In the past, dyslexia was diagnosed in the diagnosis of dyslexia does not receive intensive early reading the context of a discrepancy between include socioeconomic disadvantage intervention, 56% to 92% of these reading ability and IQ, such that as a potential cause. Although these children achieve average reading reading ability had to be 1 SD below children do not necessarily meet ability.68 However, many children are cognitive abilities (IQ) for dyslexia to a diagnosis of dyslexia, children who diagnosed with dyslexia long after be diagnosed. However, this struggle with reading, regardless of they first demonstrate recognizable discrepancy model has been etiology, have been shown to suffer struggles with preliteracy disproven, and dyslexia is no longer the same adverse health and milestones.69 Currently, children are considered to be associated with IQ.61 psychosocial consequences and typically diagnosed with dyslexia at benefit from interventions that have Dyslexia is related to deficits in $1 the end of the second or beginning of been primarily developed to address strands of the reading rope and third grade (and many much later), deficits associated with dyslexia.53–55 particularly to early struggles in after they have already failed to learn phonological and/or phonemic to read over a long period of time and Although neuroimaging research has awareness.62 Other predictors include have fallen behind their peers been invaluable in establishing the struggles in letter-sound academically.70 This wait-to-fail biological basis of dyslexia and correspondence, pseudoword approach fails to capitalize on the reading impairments, neuroimaging repetition (the ability to pronounce most effective window for technology (eg, brain MRI) does not spoken nonsense words), identifying intervention, which is during an have the ability to screen or diagnose rhyming sounds, rapid automatized earlier period of heightened brain dyslexia on an individual level, nor is naming (the ability to automatically plasticity in kindergarten and first it likely that this will be the case in retrieve the names of objects, letters, grade.70,71 Referred to as the the future. At this point, or colors), and deficits in oral “dyslexia paradox,”63 the gap between neuroimaging is not able to clearly language comprehension and the earliest time at which disentangle differential receptive and expressive identification is possible and the time neurobiological effects of dyslexia vocabulary.63 These measures have at which identification and treatment versus other reading been shown to be strong predictors of typically occur can preclude effective impairments.39,56 For these reasons reading ability in the English intervention and has profound and many others, cognitive- language; in other languages, the academic and socioemotional behavioral strategies are much more precursors vary, and screening implications for the developing useful in screening. approaches should be tailored to child. Children at the 10th

Downloaded from www.aappublications.org/news by guest on October 6, 2021 PEDIATRICS Volume 146, number 1, July 2020 3 percentile of reading ability may read for risk of dyslexia is possible earlier With the recognition that early as many words in 1 year as a child at in the developmental time course literacy predictors of dyslexia can be the 90th percentile reads in a few than is diagnosis; thus, it represents identified before the start of days.72 an opportunity for expeditious early kindergarten,63,65 we can no longer intervention. afford to wait for screenings in In addition to the poor academic children’s first formal schooling outcomes associated with untreated The consideration of any screening experiences. In a 2009 position article dyslexia, diagnosing children after regimen requires that a valid and negating visual deficiencies as the a prolonged period of failure can have acceptable test be available, an origin of dyslexia, the American severe implications for children’s effective and accessible means of Academy of Pediatrics stated that mental health. Often perceived as lazy treatment be available, and the pediatricians should “be vigilant in or labeled as “stupid,” children with potential benefits of screening looking for early signs of evolving dyslexia may develop decreased self- outweigh the risks78 without an learning disabilities.”81 The esteem, which can progress to anxiety 16 undue burden to the practitioner or pediatrician’s existing role in and depression. Furthermore, patient. In the case of dyslexia, monitoring early child development children with learning disorders are screening children individually for and our understanding of the less likely to complete high school,73 risk can be accomplished quickly and importance of early support for less likely to attend programs of inexpensively through language and literacy development higher education,74 and at increased a consideration of family history and present pediatricians with the risk of entering the juvenile justice through short behavioral assessments opportunity to implement dyslexia system: 28% to 45% of incarcerated 75 of early literacy abilities. Extensive screening in well-child visits even youth and 20% to 30% of 76 evidence has revealed the benefitof before children are school-aged. incarcerated adults have a learning an early evidence-based response to disorder. Additionally, adults with Pediatricians can contribute to screening,70,79,80 and the risks of learning disorders are more likely to a collaborative effort to screen for implementing a screening process are be unemployed and, on average, earn children at risk by capitalizing on minimal to negligible. A review of annual incomes well below the their unique role in a child’s early a child’s family history of dyslexia is national average.5 Given the developmental trajectory and by a worthwhile start to the process of prognostic benefit of early diagnosis taking advantage of their network of early identification: a family history and intervention and the many health and educational resources. It is with positive results necessitates adverse consequences that can be important to note that many parents close monitoring, whereas a family avoided or mitigated, there is great desire this proactive stance from their history with negative results still value in identifying early risk for child’s health care provider: more requires a level of ongoing dyslexia in the pediatric clinic. than one-third of surveyed parents observation. indicated that they have not discussed reading with their THE ROLE OF PEDIATRICIANS AND The risk of a false-positive result is pediatrician; nearly one-half of that THEIR PROFESSIONAL ORGANIZATIONS present with any screening program, IN DYSLEXIA RISK SCREENING group believed such conversations and, in the case of dyslexia screening, would be useful.82 Pediatricians can It is important to distinguish between the risk is tantamount to further also provide referrals to outside screening for dyslexia risk and evaluation, monitoring, and experts, such as neuropsychologists diagnosing dyslexia. Screening refers educational supports. Although and SLPs, and communicate with to a brief assessment that determines through these processes, demands patients’ schools.83 the risk of having or developing are placed on the child and represent dyslexia, which can be undertaken at cost and effort on the part of Pediatricians typically rely on an early age before school entry.75,77 practitioners, the burden of failing to a developmental milestone checklist Conversely, a formal diagnosis can identify these children early is in evaluating a child’s development in only occur after reading instruction ultimately greater than the burden of various domains; however, recent has begun and requires a more providing supplemental resources to research reveals that there is great comprehensive neuropsychological a child needlessly. As discussed, variability between the many evaluation, which can be motivated although not all children who struggle available checklists, both in content by a previous screening result.76 with reading will meet the criteria for and milestone age ranges.84 Although attention to both screening a dyslexia diagnosis, most children Furthermore, although receptive and and diagnosis is vital in ensuring that who struggle with reading will expressive language is accounted for the appropriate interventions are benefit from interventions designed in these checklists, a comprehensive implemented for the child, screening to address dyslexia. inventory of key early literacy

Downloaded from www.aappublications.org/news by guest on October 6, 2021 4 SANFILIPPO et al measures that are crucial for needed. Given the high overlap beneficial in supporting emerging assessing dyslexia risk is not between dyslexia and deficits in literacy while also identifying included. speech and language, physicians children at risk for dyslexia. should consider referring children Early warning signs of dyslexia are A further possibility is the use of 63,65 who are at risk for dyslexia to an SLP visible before school entry ; thus, a standardized, brief 2- or 3-question who is trained in early literacy.21 the pediatrician may be a child’s first first-step questionnaire, the likes of Furthermore, pediatric associations health or educational professional which have already been can partner with dyslexia researchers capable of identifying these signs and demonstrated to be successful in and education specialists to create implementing a management plan. prescreening other conditions like educational resources and trainings For example, pediatricians can depression88 and attention-deficit/ that can assist pediatricians in document the extent to which a child hyperactivity disorder.89 Although no providing education and support to can recognize rhyming sounds, repeat such standardized questionnaire yet their patients and families with or at nonsense words, or report the sound exists, pediatricians can pose risk for dyslexia. that a letter makes. It is important to questions to a preschool-aged child’s note that phonological deficits can Checklists, questionnaires, and caregiver(s) pertaining to key risk present differently in different interviews can be completed in factors for dyslexia. Affirmative children, and children with dyslexia conjunction with a child’s parent to answers to these first-step questions will vary in the specific tasks with assess a child’s key risk factors. can be used to lead to a more which they show difficulty. Thus, Although these methods provide detailed, validated screening tool that screenings are used to pinpoint a quick account of a child’s risk, they can be used to identify specific particular early literacy skills that are often tools that are not deficits present. There are storybooks may require remedial attention and scientifically validated or reliable85 and tablet- and smartphone-based also identify children who may and are thus intended for gamified and self-administered eventually require a more detailed a preliminary formative assessment screening tools currently being evaluation to come to a definitive only. Commonly used questionnaires developed for the use in schools, diagnosis of dyslexia. like the Ages & Stages Questionnaires, clinics, or a child’s home. These tools for example, can be helpful as are being designed to be entertaining A MORE PROACTIVE APPROACH: a starting point but do not provide for the child and will be informative SCREENING AND ADVOCACY a detailed assessment. Rigorously to the clinician in determining the validated screeners composed of appropriate next steps and referrals There are many methods by which child-centered behavioral for further evaluation and pediatricians can work toward assessments (see ref 86 for intervention. systematic early screening of dyslexia a nonexhaustive evaluation of in their practices. Pediatricians As new screening tools continue to screening tools) are used to provide should elicit a family history of become available in the coming years, a reliable and unbiased testament of dyslexia, recognize assessments done it will be important for practitioners a child’s risk status. by schools that indicate a risk and/or to be knowledgeable about the diagnosis, and include dyslexia in the Pediatric clinics could consider characteristics of an appropriate differential diagnosis for low self- hosting “screening days” with dyslexia screener and discerning in esteem, depression, anxiety, or a literacy focus that can aim to their selection. The ideal screener has disruptive behaviors. The governing simultaneously screen for early been validated in a representative bodies of associations of pediatricians predictors of dyslexia while also sample; has strong evidence for should provide training on dyslexia facilitating a literacy-rich reliability, validity, and classification assessments and interventions as environment by making literacy accuracy; has developmentally a part of ongoing continuing materials available to families. Many appropriate content given the age or education so that pediatricians can pediatricians have already made great grade level of the child; and has the become adept at implementing strides in promoting literacy within capacity to measure both word screening processes and at their clinics. The Reach Out and Read recognition and linguistic interpreting, monitoring, and program has been effective in comprehension.77 A list of available responding efficiently to evaluations facilitating language and preliteracy dyslexia screening tools, along with and interventions performed outside skills in children through the an indication of their fulfillment of the clinic. The appropriate referral to distribution of books through characteristics like those listed above, outside consultants and primary care clinics.87 A similar is presently available for practitioners interventionists should also be program with an additional screening to consult (see ref 86). An additional involved in this training when component could be even more resource for practitioners is the What

Downloaded from www.aappublications.org/news by guest on October 6, 2021 PEDIATRICS Volume 146, number 1, July 2020 5 Works Clearinghouse, which is used instructional support (for an children at risk. Early identification to provide evidence-based overview of state legislation, see ref should start with an assessment of evaluations on literacy screening 95). Despite such recent attention, family history and should be followed products as they become available.90 there is much room for growth in with validated behavioral screening In addition to child-directed pediatric neurocognitive research tools. After a positive screen, referrals assessments, given the strong funding, which has lagged compared to diagnosticians such as SLPs or heritability of dyslexia, a crucial to adult neurocognitive disorders. neuropsychologists should be made. component of early identification is Increased funding and research must Diagnoses, when they occur, should an assessment of the reading history be used to explore etiologic models, be followed with letters to schools of the child’s parent(s) to determine examine comorbid relationships, requesting the implementation of fi fi the child’s familial risk of dyslexia. re ne tools for the early identi cation literacy intervention. Family history is both quick to elicit of children at risk for dyslexia and With time, new and innovative and informative in the global other reading impairments, formats for screening will emerge. In assessment of a child’s risk. The Adult investigate additional tools for use in acknowledging the significant effort Reading History Questionnaire is an children for whom English is not their devoted by pediatricians to screening fi inventory91 of an adult’s literacy rst language, and develop and various conditions, the future will abilities and habits and can be used to evaluate intervention strategies and require a consideration of novel fi indicate a reading impairment (see their effectiveness. A rst-order goal approaches to office visits or ref 92 for a digital version). Follow-up should be the development of increased community-based questions should be presented to screening guidelines and tools for use collaboration with preschools to a parent with a high-risk score to rule during pediatric visits for 4- and 5- accomplish screening for disorders out an environmental explanation for year-old children that can be used to that, like dyslexia, are of nontrivial reading impairment (eg, lack of identify children at risk before the prevalence and are associated with formal reading instruction). This optimal window for early available and effective interventions. distinction is particularly important interventions closes, while also Pediatricians occupy a unique role in fi to consider in communities with re ning guidelines to identify older the lives of children such that they are considerable immigrant populations, children who were not screened well positioned to recognize and who may be flagged by the Adult earlier. Finally, with the help of policy respond to risk factors for dyslexia “ ” Reading History Questionnaire as “at makers, the current failure model of even before children enter the risk” simply because they are adult dyslexia must be replaced with education system; however, the “ ” learners of the dominant language. a support model that enables delivery of dyslexia interventions is Regardless of a parent’s dyslexia school-, clinic-, and community-based and will largely continue to be status, the quality of the home early screenings and subsequent implemented outside the scope of the literacy environment is a strong evidence-based response to screening pediatrician’s practice. Thus, the predictor of reading outcome.52,93,94 through empowered and well-trained contributions of both pediatricians Thus, this parent inventory is useful teachers within the general education and other health and educational not only because it can be used to framework. Physicians can be professionals are crucial to indicate a child’s possible familial risk powerful agents of these positive optimizing the process of identifying but also because it can reveal less changes, both at the level of their and treating dyslexia. Although the literacy-rich home environments that clinical practices and as advocates in response to dyslexia screening and leave children with insufficient their communities and beyond. intervention is multifaceted and literacy materials and support, longitudinal, the trajectory of illuminating additional targets for CONCLUSIONS children’s literacy outcomes has the intervention. Our current knowledge of the potential to be improved through the fi Beyond the clinic, the medical neurobiological basis for dyslexia, its implementation of early identi cation community can be vocal advocates in reliable developmental-behavioral in pediatric practice. national conversations about dyslexia, predictors, the effectiveness of early many of which are currently intervention, and the myriad adverse ABBREVIATION happening in state legislatures; as of effects of reading failure reveal now, only a few US states lack state- a demand for a proactive, preventive SLP: speech and language level legislation focusing on early approach (instead of a deficit-driven pathologist screening, teacher training, and/or approach) to identify and treat

Downloaded from www.aappublications.org/news by guest on October 6, 2021 6 SANFILIPPO et al FUNDING: Funded by the National Institute of Child Health and Human Development (grant R01 HD065762). Funded by the National Institutes of Health (NIH). POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.

REFERENCES 1. Irwin LG, Siddiqi A, Hertzman C; World 11. Petretto DR, Masala C. Dyslexia and 22. Germanò E, Gagliano A, Curatolo P. Health Organization. Early Child specific learning disorders: new Comorbidity of ADHD and dyslexia. Dev Development: A Powerful Equalizer: Final international diagnostic criteria. JChild Neuropsychol. 2010;35(5):475–493 Report for the World Health Dev Disord. 2017;3(4):19 23. Asberg J, Kopp S, Berg-Kelly K, Gillberg C. Organization’s Commission on the Social 12. Hendren RL, Haft SL, Black JM, White NC, Reading comprehension, word decoding Determinants of Health. Vancouver, Hoeft F. Recognizing psychiatric and spelling in girls with autism Canada: Human Early Learning comorbidity with reading disorders. spectrum disorders (ASD) or attention- Partnership; 2007 Front Psychiatry. 2018;9:101 deficit/hyperactivity disorder (AD/HD): 2. Johnston RB Jr.. Poor Education Predicts performance and predictors. Int J Lang Poor Health—A Challenge Unmet by 13. Grills-Taquechel AE, Fletcher JM, Vaughn Commun Disord. 2010;45(1):61–71 SR, Stuebing KK. Anxiety and reading American Medicine. Washington, DC: difficulties in early elementary school: 24. Burke JD, Loeber R, Birmaher B. National Academy of Medicine; 2019 fi evidence for unidirectional- or bi- Oppositional de ant disorder and 3. Cree A, Kay A, Steward J. The Economic directional relations? Child Psychiatry conduct disorder: a review of the past and Social Cost of Illiteracy: A Snapshot Hum Dev. 2012;43(1):35–47 10 years, part II. JAmAcadChild of Illiteracy in a Global Context. Adolesc Psychiatry. 2002;41(11): Melbourne, Australia: World Literacy 14. Mammarella IC, Ghisi M, Bomba M, et al. 1275–1293 Anxiety and depression in children with Foundation; 2012 25. Pauc R. Comorbidity of dyslexia, nonverbal learning disabilities, reading dyspraxia, attention deficit disorder 4. Shaywitz SE. Dyslexia. N Engl J Med. disabilities, or typical development. (ADD), attention defi cit hyperactive 1998;338(5):307–312 J Learn Disabil. 2016;49(2):130–139 disorder (ADHD), obsessive compulsive 5. Cortelia C, Horowitz SH. The State of 15. Nelson JM, Harwood H. Learning disorder (OCD) and Tourette’s syndrome Learning Disabilities: Facts, Trends and disabilities and anxiety: a meta-analysis. in children: a prospective Emerging Issues, 3rd ed. New York, NY: J Learn Disabil. 2011;44(1):3–17 epidemiological study. Clin Chiropr. National Center for Learning Disabilities; 2005;8(4):189–198 2014 16. Mugnaini D, Lassi S, La Malfa G, Albertini G. Internalizing correlates of dyslexia. 26. Moll K, Landerl K, Snowling MJ, Schulte- 6. Fletcher JM, Lyon GR, Fuchs LS, Barnes World J Pediatr. 2009;5(4):255–264 Körne G. Understanding comorbidity of MA. Learning Disabilities: From learning disorders: task-dependent Identification to Intervention, 2nd ed. 17. Bishop DVM, Snowling MJ. estimates of prevalence. J Child Psychol New York, NY: Guilford Press; 2018 Developmental dyslexia and specific Psychiatry. 2019;60(3):286–294 language impairment: same or 7. Vellutino FR, Fletcher JM, Snowling MJ, different? Psychol Bull. 2004;130(6): 27. Döhla D, Heim S. Developmental dyslexia fi Scanlon DM. Speci c reading disability 858–886 and dysgraphia: what can we learn from (dyslexia): what have we learned in the one about the other? Front Psychol. past four decades? J Child Psychol 18. Gooch D, Hulme C, Nash HM, Snowling 2016;6:2045 – MJ. Comorbidities in preschool children Psychiatry. 2004;45(1):2 40 28. Finucci JM, Whitehouse CC, Isaacs SD, at risk of dyslexia: the role of language Childs B. Derivation and validation of 8. Stanovich KE. Matthew effects in ability. J Child Psychol Psychiatry.2013; a quantitative definition of specific reading: some consequences of 55(3):237–246 individual differences in the acquisition reading disability for adults. Dev Med of literacy. Read Res Q. 1986;21(4): 19. Snowling MJ, Melby-Lervåg M. Oral Child Neurol. 1984;26(2):143–153 fi 360–407 language de cits in familial dyslexia: 29. Vogler GP, DeFries JC, Decker SN. Family a meta-analysis and review. Psychol Bull. history as an indicator of risk for 9. Ozernov-Palchik O, Yu X, Wang Y, Gaab N. 2016;142(5):498–545 Lessonstobelearned:how reading disability. J Learn Disabil. 1985; a comprehensive neurobiological 20. Adlof SM, Hogan TP. Understanding 18(7):419–421 framework of atypical reading dyslexia in the context of developmental 30. Grigorenko EL. Speaking genes or genes development can inform educational language disorders. Lang Speech Hear for speaking? Deciphering the genetics practice. Curr Opin Behav Sci. 2016;10: Serv Sch. 2018;49(4):762–773 of speech and language. J Child Psychol 45–58 – – 21. Cabbage KL, Farquharson K, Iuzzini- Psychiatry. 2009;50(1 2):116 125 10. Moats LC, Dakin KE. Basic Facts About Seigel J, Zuk J, Hogan TP. Exploring the 31. Galaburda AM, LoTurco J, Ramus F, Fitch Dyslexia and Other Reading Problems. overlap between dyslexia and speech RH, Rosen GD. From genes to behavior in Baltimore, MD: The International sound production deficits. Lang Speech developmental dyslexia. Nat Neurosci. Dyslexia Association; 2007 Hear Serv Sch. 2018;49(4):774–786 2006;9(10):1213–1217

Downloaded from www.aappublications.org/news by guest on October 6, 2021 PEDIATRICS Volume 146, number 1, July 2020 7 32. Paracchini S, Scerri T, Monaco AP. The 43. Richlan F, Kronbichler M, Wimmer H. instruction? Perspect Lang Lit. 2018; genetic lexicon of dyslexia. Annu Rev Functional abnormalities in the dyslexic 44(3):25–28 Genomics Hum Genet. 2007;8:57–79 brain: a quantitative meta-analysis of 54. Eunice Kennedy Shriver National neuroimaging studies. Hum Brain Mapp. 33. Mascheretti S, Riva V, Giorda R, et al. Institute of Child Health and Human 2009;30(10):3299–3308 KIAA0319 and ROBO1: evidence on Development; National Reading Panel. association with reading and pleiotropic 44. Horwitz B, Rumsey JM, Donohue BC. Teaching children to read: an evidence- effects on language and mathematics Functional connectivity of the angular based assessment of the scientific abilities in developmental dyslexia. gyrus in normal reading and dyslexia. research literature on reading and its J Hum Genet. 2014;59(4):189–197 Proc Natl Acad Sci U S A. 1998;95(15): implications for reading instruction. 8939–8944 2000. Available at: https://www.nichd.nih. 34. Mascheretti S, De Luca A, Trezzi V, et al. gov/sites/default/files/publications/ Neurogenetics of developmental 45. Langer N, Peysakhovich B, Zuk J, et al. pubs/nrp/Documents/report.pdf. dyslexia: from genes to behavior White matter alterations in infants at Accessed May 20, 2020 through brain neuroimaging and risk for developmental dyslexia. Cereb cognitive and sensorial mechanisms. Cortex. 2017;27(2):1027–1036 55. Foorman BR, Torgesen J. Critical Transl Psychiatry. 2017;7(1):e987 elements of classroom and small-group 46. Leppänen PHT, Hämäläinen JA, Guttorm instruction promote reading success in 35. Hannula-Jouppi K, Kaminen-Ahola N, TK, et al. Infant brain responses all children. Learn Disabil Res Pract. Taipale M, et al. The axon guidance associated with reading-related skills 2001;16(4):203–212 receptor gene ROBO1 is a candidate before school and at school age. gene for developmental dyslexia. PLoS Neurophysiol Clin. 2012;42(1–2):35–41 56. Noble KG, Wolmetz ME, Ochs LG, Farah Genet. 2005;1(4):e50 MJ, McCandliss BD. Brain-behavior 47. Im K, Raschle NM, Smith SA, Ellen Grant relationships in reading acquisition are 36. Meng H, Smith SD, Hager K, et al. DCDC2 P, Gaab N. Atypical sulcal pattern in modulated by socioeconomic factors. is associated with reading disability and children with developmental dyslexia Dev Sci. 2006;9(6):642–654 modulates neuronal development in the and at-risk kindergarteners. Cereb brain. Proc Natl Acad Sci U S A. 2005; Cortex. 2016;26(3):1138–1148 57. Scarborough HS. Connecting Early 102(47):17053–17058 Language and Literacy to Later Reading 48. Peterson RL, Pennington BF. (Dis)abilities: Evidence, Theory, and 37. Paracchini S, Thomas A, Castro S, et al. Developmental dyslexia. Annu Rev Clin Practice. In: Neuman SB, Dickinson DK, The chromosome 6p22 haplotype Psychol. 2015;11:283–307 eds. Handbook of Early Literacy associated with dyslexia reduces the 49. Reardon SF. The Widening Academic Research, vol. Vol 1. New York, NY: expression of KIAA0319, a novel gene Achievement Gap between the Rich and Guilford Press; 2001:97–110 involved in neuronal migration. Hum Mol the Poor: New Evidence and Possible Genet. 2006;15(10):1659–1666 58. Lonigan CJ, Burgess SR, Schatschneider Explanations. In: Murnane RJ, Duncan C. Examining the simple view of reading 38. Skiba T, Landi N, Wagner R, Grigorenko GJ, eds. Whither Opportunity? Rising with elementary school children: still EL. In search of the perfect phenotype: Inequality, Schools, and Children’sLife simple after all these years. Remedial an analysis of linkage and association Chances. New York, NY: Russell Sage Spec Educ. 2018;39(5):260–273 studies of reading and reading-related Foundation Press; 2011:91–116 processes. Behav Genet. 2011;41(1):6–30 59. Catts HW. The simple view of reading: 50. Noble KG, McCandliss BD. Reading advancements and false impressions. 39. Richlan F, Kronbichler M, Wimmer H. development and impairment: Remedial Spec Educ. 2018;39(5):317–323 Meta-analyzing brain dysfunctions in behavioral, social, and neurobiological dyslexic children and adults. factors. J Dev Behav Pediatr. 2005;26(5): 60. Snow CE. Simple and not-so-simple Neuroimage. 2011;56(3):1735–1742 370–378 views of reading. Remedial Spec Educ. 2018;39(5):313–316 40. Martin A, Schurz M, Kronbichler M, 51. National Assessment of Educational Richlan F. Reading in the brain of Progress. Data tools: NAEP Data 61. Tanaka H, Black JM, Hulme C, et al. The children and adults: a meta-analysis of Explorer. 2017. Available at: https://nces. brain basis of the phonological deficit in 40 functional magnetic resonance ed.gov/nationsreportcard/naepdata/. dyslexia is independent of IQ. Psychol imaging studies. Hum Brain Mapp. 2015; Accessed August 1, 2019 Sci. 2011;22(11):1442–1451 36(5):1963–1981 52. Metsala JL. Lexical Reorganization and 62. Hulme C, Snowling MJ. Reading 41. Peterson RL, Pennington BF. the Emergence of Phonological disorders and dyslexia [published Developmental dyslexia. Lancet. 2012; Awareness. In: Neuman SB, Dickinson correction appears in Curr Opin Pediatr. 379(9830):1997–2007 DK, eds. Handbook of Early Literacy 2018;30(4):597]. Curr Opin Pediatr. 2016; Research, vol. Vol 3. New York, NY: 28(6):731–735 42. Linkersdörfer J, Lonnemann J, Lindberg Guilford Press; 2011:66–82 S, Hasselhorn M, Fiebach CJ. Grey 63. Ozernov-Palchik O, Gaab N. Tackling the matter alterations co-localize with 53. Kilpatrick DA. Genetics, the environment, ‘dyslexia paradox’: reading brain and functional abnormalities in and poor instruction as contributors to behavior for early markers of developmental dyslexia: an ALE meta- work-level reading difficulties: does it developmental dyslexia. Wiley Interdiscip analysis. PLoS One. 2012;7(8):e43122 matter for early identification and Rev Cogn Sci. 2016;7(2):156–176

Downloaded from www.aappublications.org/news by guest on October 6, 2021 8 SANFILIPPO et al 64. Compton DL, Fuchs D, Fuchs LS, Bryant 75. Gaab N. Identifying risk instead of DIBELS performance. Psychol Sch.2011; JD. Selecting at-risk readers in first failure. Reading impairments: moving 48(4):343–356 grade for early intervention: a two-year from a deficit-driven to a preventive 86. National Center on Intensive Intervention longitudinal study of decision rules and model. 2019. Available at: https://bold. at American Institutes for Research. procedures. J Educ Psychol. 2006;98(2): expert/identifying-risk-instead-of-failure/ Academic screening tools chart. 2019. 394–409 . Accessed August 1, 2019 Available at: https://charts. 65. Puolakanaho A, Ahonen T, Aro M, et al. 76. International Dyslexia Association. intensiveintervention.org/chart/ Very early phonological and language Dyslexia assessment: what is it and how academic-screening. Accessed January skills: estimating individual risk of can it help? 2017. Available at: https:// 11, 2020 reading disability. J Child Psychol dyslexiaida.org/dyslexia-assessment- 87. Zuckerman B. Promoting early literacy Psychiatry. 2007;48(9):923–931 what-is-it-and-how-can-it-help/. Accessed August 1, 2019 in pediatric practice: twenty years of 66. Catts HW, Fey ME, Zhang X, Tomblin JB. Reach Out and Read. Pediatrics. 2009; Estimating the risk of future reading 77. Petscher Y, Fien H, Stanley C, et al. 124(6):1660–1665 difficulties in kindergarten children: Screening for Dyslexia. Washington, DC: 88. Kroenke K, Spitzer RL, Williams JB. The a research-based model and its clinical National Center on Improving Literacy; Patient Health Questionnaire-2: validity implementation. Lang Speech Hear Serv 2019 of a two-item depression screener. Med Sch. 2001;32(1):38–50 78. Morabia A, Zhang FF. History of medical Care. 2003;41(11):1284–1292 67. Stanley CT, Petscher Y, Catts H. A screening: from concepts to action. – 89. Zimmerman M, Gorlin E, Dalrymple K, longitudinal investigation of direct and Postgrad Med J. 2004;80(946):463 469 Chelminiski I. A clinically useful screen indirect links between reading skills in 79. Lovett MW, Frijters JC, Wolf M, Steinbach for attention-deficit/hyperactivity kindergarten and reading KA, Sevcik RA, Morris RD. Early disorder in adult psychiatric comprehension in tenth grade. Read intervention for children at risk for outpatients. Ann Clin Psychiatry. 2017; Writ. 2018;31(1):133–153 reading disabilities: the impact of grade 29(3):160–166 68. Torgesen JK. Lessons Learned from at intervention and individual 90. Institute of Education Sciences. What Research on Interventions for Students differences on intervention outcomes. – Works Clearinghouse. 2019. Available at: Who Have Difficulty Learning to Read. In: J Educ Psychol. 2017;109(7):889 914 https://ies.ed.gov/ncee/wwc/. Accessed McCardle P, Chhabra V, eds. The Voice of 80. Catts HW, Nielsen DC, Bridges MS, Liu YS, August 1, 2019 Evidence in Reading Research. Bontempo DE. Early identification of Baltimore, MD: Paul H. Brookes reading disabilities within an RTI 91. Lefly DL, Pennington BF. Reliability and Publishing Co, Inc; 2004:355–382 framework. J Learn Disabil. 2015;48(3): validity of the Adult Reading History 281–297 Questionnaire. J Learn Disabil. 2000; 69. Torgesen JK. The prevention of reading 33(3):286–296 difficulties. J Sch Psychol. 2002;40(1): 81. American Academy of Pediatrics, Section 7–26 on Ophthalmology, Council on Children 92. International Dyslexia Association. with Disabilities; American Academy of Dyslexia screener for adults: Adult 70. Wanzek J, Vaughn S. Research-based Ophthalmology; American Association Reading History Questionnaire. 2019. implications from extensive early for Pediatric Ophthalmology and Available at: https://dyslexiaida.org/ reading interventions. School Psych Rev. Strabismus; American Association of screening-for-dyslexia/dyslexia- 2007;36(4):541–561 Certified Orthoptists. Joint statement-- screener-for-adults/. Accessed August 1, 71. Fox SE, Levitt P, Nelson CA III. How the learning disabilities, dyslexia, and vision. 2019 timing and quality of early experiences Pediatrics. 2009;124(2):837–844 93. Christopher ME, Hulslander J, Byrne B, influence the development of brain 82. Kuo AA, Franke TM, Regalado M, Halfon et al. Genetic and environmental architecture. Child Dev. 2010;81(1):28–40 N. Parent report of reading to young etiologies of the longitudinal relations 72. Cunningham AE, Stanovich KE. What children. Pediatrics. 2004;113(suppl 6): between prereading skills and reading. reading does for the mind. Am Educ. 1944–1951 Child Dev. 2015;86(2):342–361 1998;22(1–2):8–15 83. Schulte EE. Learning disorders: how 94. Hamilton LG, Hayiou-Thomas ME, Hulme 73. Jilmerson SR, Egeland B, Sroufe LA, pediatricians can help. Cleve Clin J Med. C, Snowling MJ. The home literacy – Carlson B. A prospective longitudinal 2015;82(11 suppl 1):S24 S28 environment as a predictor of the study of high school dropouts: 84. Wilkinson CL, Wilkinson MJ, Lucarelli J, early literacy development of examining multiple predictors across Fogler JM, Becker RE, Huntington N. children at family-risk of development. J Sch Psychol. 2000;38(6): Quantitative evaluation of content and dyslexia. Sci Stud Read. 2016;20(5): 525–549 age concordance across developmental 401–419 74. Dougherty C. Numeracy, literacy and milestone checklists. J Dev Behav 95. National Center on Improving Literacy. – earnings: evidence from the national Pediatr. 2019;40(7):511 518 State of dyslexia. 2019. Available at: longitudinal survey of youth. Econ Educ 85. Martin SD, Shapiro ES. Examining the https://improvingliteracy.org/state-of- Rev. 2003;22(5):5111–52 accuracy of teachers’ judgments of dyslexia. Accessed August 1, 2019

Downloaded from www.aappublications.org/news by guest on October 6, 2021 PEDIATRICS Volume 146, number 1, July 2020 9 Reintroducing Dyslexia: Early Identification and Implications for Pediatric Practice Joseph Sanfilippo, Molly Ness, Yaacov Petscher, Leonard Rappaport, Barry Zuckerman and Nadine Gaab Pediatrics 2020;146; DOI: 10.1542/peds.2019-3046 originally published online June 23, 2020;

Updated Information & including high resolution figures, can be found at: Services http://pediatrics.aappublications.org/content/146/1/e20193046 References This article cites 78 articles, 6 of which you can access for free at: http://pediatrics.aappublications.org/content/146/1/e20193046#BIBL Subspecialty Collections This article, along with others on similar topics, appears in the following collection(s): Developmental/Behavioral Pediatrics http://www.aappublications.org/cgi/collection/development:behavior al_issues_sub Cognition/Language/Learning Disorders http://www.aappublications.org/cgi/collection/cognition:language:lea rning_disorders_sub Permissions & Licensing Information about reproducing this article in parts (figures, tables) or in its entirety can be found online at: http://www.aappublications.org/site/misc/Permissions.xhtml Reprints Information about ordering reprints can be found online: http://www.aappublications.org/site/misc/reprints.xhtml

Downloaded from www.aappublications.org/news by guest on October 6, 2021 Reintroducing Dyslexia: Early Identification and Implications for Pediatric Practice Joseph Sanfilippo, Molly Ness, Yaacov Petscher, Leonard Rappaport, Barry Zuckerman and Nadine Gaab Pediatrics 2020;146; DOI: 10.1542/peds.2019-3046 originally published online June 23, 2020;

The online version of this article, along with updated information and services, is located on the World Wide Web at: http://pediatrics.aappublications.org/content/146/1/e20193046

Pediatrics is the official journal of the American Academy of Pediatrics. A monthly publication, it has been published continuously since 1948. Pediatrics is owned, published, and trademarked by the American Academy of Pediatrics, 345 Park Avenue, Itasca, Illinois, 60143. Copyright © 2020 by the American Academy of Pediatrics. All rights reserved. Print ISSN: 1073-0397.

Downloaded from www.aappublications.org/news by guest on October 6, 2021