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Accepted Manuscript Disclaimer and Additional Information DNA methylation profiling and genomic analysis in 20 children with short stature who were born small-for-gestational age 1 2 3 1 Silke Peeters, MSc , Ken Declerck, PhD , Muriel Thomas, MD , Eveline Boudin, PhD , Dominique Downloaded from https://academic.oup.com/jcem/article-abstract/doi/10.1210/clinem/dgaa465/5873625 by KU Leuven Libraries user on 24 July 2020 Beckers, MD4, Olimpia Chivu, MD5, Claudine Heinrichs, MD, PhD6, Koenraad Devriendt, MD, PhD7, Francis de Zegher, MD, PhD8, Wim Van Hul, PhD1, Wim Vanden Berghe, PhD2, Jean De Schepper, MD9, Raoul Rooman, MD, PhD10, Geert Mortier, MD, PhD1 on behalf of the WES-BESPEED study group°. 1Department of Medical Genetics, University of Antwerp and Antwerp University Hospital, Antwerp, Belgium 2Laboratory of Protein Chemistry, Proteomics and Epigenetic Signalling (PPES), Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium 3Belgian Society for Pediatric Endocrinology and Diabetology, Brussels, Belgium 4Unité d'Endocrinologie Pédiatrique, CHU NAMUR, Université catholique de Louvain, 5530 Yvoir, Belgium and Department of Pediatrics, University Hospital Gasthuisberg, 3000, Leuven, Belgium 5Department of Pediatrics, Clinique de l'Espérance, Saint-Nicolas, Belgium 6Paediatric Endocrinology Unit, Hôpital Universitaire des Enfants Reine Fabiola (HUDERF), Brussels, Belgium 7Center for Human Genetics, University hospital Leuven, University of Leuven, Leuven, Belgium 8Department of Development & Regeneration, University of Leuven, Leuven, Belgium 9Department of Pediatrics, Vrije Universiteit Brussel, Universitair Ziekenhuis Brussel, Brussels, Belgium and DepaAcceptedrtment of Pediatrics, Universitair Ziek enhManuscriptuis Gent, Ghent, Belgium 10PendoCon bvba, Putte, Belgium °Additional collaborators of the WES-BESPEED study group include Dotremont Hilde, MD, Department of Pediatrics, Antwerp University Hospital, Antwerp Belgium; Craen Margareta, MD, Department of Pediatrics, University of Ghent, Ghent, Belgium; Gies Inge, MD/PhD, Department of Pediatrics, UZ © Endocrine Society 2020. All rights reserved. For permissions, please e-mail: [email protected]. jc.2020-00271. See https://academic.oup.com/endocrinesociety/pages/Author_Guidelines for Accepted Manuscript disclaimer and additional information. Brussel, Brussels Belgium; Lebrethon, Marie-Christine, MD, Department of Pediatrics, University of Liège, Liège, Belgium. Corresponding author: Name: Mortier Geert Downloaded from https://academic.oup.com/jcem/article-abstract/doi/10.1210/clinem/dgaa465/5873625 by KU Leuven Libraries user on 24 July 2020 Address: Department of Medical Genetics Prins Boudewijnlaan 43 2650 Edegem Belgium TEL: +32 3275 9774 E-mail address: [email protected] Grant support Supported by an unrestricted grant (53232139) from Pfizer, the Research Fund of the University of Antwerp (Methusalem-OEC grant – “GENOMED”; FFB190208), a predoctoral grant from the University of Antwerp (to S Peeters) and a postdoctoral grant from the Research Foundation-Flanders (12A3814N) (to E Boudin). Disclosure Statement RR has received consulting fees or grant support from Pfizer, Ferring, Sandoz and Ipsen. JDS has received consulting fees or grant support from Novo-Nordisk, Pfizer, Eli-Lilly, Ferring, Sandoz and Ipsen. DB receivedAccepted travel fees from Novo Nordisk, Pfizer Manuscript and Ferring and conference fees from Merck. All other authors declare no conflict of interest. Although part of the study was supported by a grant from Pfizer, decisions about the design of the study, collection and analysis of data or decision to publish were made independently. 2 Abstract Purpose: In a significant proportion of children born small-for-gestational age (SGA) with failure of catch-up growth, the etiology of short stature remains unclear after routine diagnostic work-up. We Downloaded from https://academic.oup.com/jcem/article-abstract/doi/10.1210/clinem/dgaa465/5873625 by KU Leuven Libraries user on 24 July 2020 wanted to investigate if extensive analysis of the (epi)genome can unravel the cause of growth failure in a significant portion of these children. Patients and Methods: Twenty SGA children treated with growth hormone (GH) because of short stature were selected from the BELGROW database of the Belgian Society for Pediatric Endocrinology and Diabetology for exome sequencing, SNP array and genome-wide methylation analysis to identify the (epi)genetic cause. First year response to GH was compared to the response of SGA patients in the KIGS database. Results: We identified (likely) pathogenic variants in 4 children (from 3 families) using exome sequencing and found pathogenic CNV in 2 probands using SNP array. In a child harboring a NSD1- containing microduplication, we identified a DNA methylation signature that is opposite to the genome-wide DNA methylation signature of Sotos syndrome. Moreover, we observed multi-locus imprinting disturbances in two children in whom no other genomic alteration could be identified. Five out of 6 children with a genetic diagnosis had an "above average" response to GH. Conclusions: The study indicates that a more advanced approach with deep genotyping can unravel unexpected (epi)genomic alterations in SGA children with persistent growth failure. Most SGA children with a Acceptedgenetic diagnosis had a good response to GHManuscript treatment. Key words: small for gestational age; short stature; growth hormone; DNA methylation; NSD1 3 Introduction About 20% of children with short stature are born small for gestational age (SGA)1. SGA can be defined as a birth weight and/or birth length equal or less than -2 SD for sex and gestational age2. Most of the Downloaded from https://academic.oup.com/jcem/article-abstract/doi/10.1210/clinem/dgaa465/5873625 by KU Leuven Libraries user on 24 July 2020 SGA children catch up on weight and height during the first two years of their life3. However, approximately 10% of the children fail to catch up on growth and remain short in adult life1. Genetic association studies with candidate genes identified several common single nucleotide polymorphisms (SNP) associated with persistent short stature in SGA children4. Moreover, also rare single nucleotide variants (SNV), copy number variants (CNV) and larger chromosomal abnormalities have been shown to cause prenatal onset (syndromic) short stature5-7. Other causes of growth deficits are related to genomic imprinting8. Epigenetic mechanisms, including DNA methylation, control imprinting and, if disturbed, may result in imprinting associated disorders. These disorders usually affect fetal growth, metabolism and development. Although several genetic and epigenetic factors have been identified, the etiology of short stature remains unclear in a significant proportion of children born SGA5,9,10. The multitude of different disorders with sometimes variable, complex and overlapping phenotypes often complicates a rapid and accurate genetic diagnosis11,12. Nevertheless, the elucidation of the exact cause of growth failure is important for proper treatment, management and eventually genetic counseling11. In this study, we investigated a well-defined group of 20 SGA children with persistent short stature by applying an advanced (epi)genetic approach to unravel the underlying cause. MaterialAccepteds and methods Manuscript Patient recruitment BELGROW, the Belgian database of children treated with growth hormone (GH), was searched for children born SGA and with short stature at the start of GH treatment. Other inclusion criteria were: (1) both biological parents are alive (2) bone age at the start of GH treatment is within 1.5 year of the 4 calendar age; (3) Height SDS at the start of GH treatment is at least 1.5 SD below the height SDS of each parent; (4) Still prepubertal during the first year of GH treatment to allow a reliable assessment of the first year growth response to GH administration. Exclusion criteria were: (1) a known bone dysplasia or sitting height/total height > 2SDS; (2) evidence for fetotoxic factors that explained the Downloaded from https://academic.oup.com/jcem/article-abstract/doi/10.1210/clinem/dgaa465/5873625 by KU Leuven Libraries user on 24 July 2020 intra-uterine growth retardation (e.g. tobacco or alcohol abuse) or another known factor that explained the growth deficit or that modulated the response to GH therapy such as a chronic disease or chronic medication. Birth weight and length were calculated using the Niklasson references13. Height and weight SDS were calculated using the 2004 Flemish growth references14. Out of 65 eligible patients, 20 participated in the study. Reasons for non-participation included: one parent not available (died, in prison, moved to another country, …), patient had moved and address was unknown, incorrect registry data that when corrected turned the patient no longer eligible, genetic diagnosis reached but not available in the registry, refusal to participate, patient did not start treatment, patient was not invited for the study. Ethical and regulatory aspects The study was approved by the Academic Ethical Committee of the Brussels Alliance for Research and Higher Education (B200-2014-043). Both parents gave their informed consent and each child received an age-appropriate study information document and signed an assent form. It was stipulated in the study information document that secondary findings would not be communicated to the parents unless the genetic finding was featured on the list of the American College of Genetics and
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