Steroid-Resistant Nephrotic Syndrome Is Associated With a Unique Genetic Profile in a Highly Admixed Pediatric Population

Introduction: The profile of genetic and nongenetic factors associated with progression to kidney failure (KF) in steroid-resistant nephrotic syndrome (SRNS) is largely unknown in admixed populations. Methods: A total of 101 pediatric patients with primary SRNS were genetically assessed targeting Me...

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Main Authors: Andreia Watanabe, Precil Diego Miranda de Menezes Neves, Kelly Nunes, Antonio Marcondes Lerario, Elieser Hitoshi Watanabe, Frederico Moraes Ferreira, Denise Maria Avancini Costa Malheiros, Amanda de Moraes Narcizo, Mara Sanches Guaragna, Stanley de Almeida Araujo, Thais Medeiros Cruz, Jussara Soares Fontes, Vera Maria Santoro Belangero, Maria Helena Vaisbich, Friedhelm Hildebrandt, Matthew Gordon Sampson, Luiz Fernando Onuchic
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:Kidney International Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2468024924019235
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author Andreia Watanabe
Precil Diego Miranda de Menezes Neves
Kelly Nunes
Antonio Marcondes Lerario
Elieser Hitoshi Watanabe
Frederico Moraes Ferreira
Denise Maria Avancini Costa Malheiros
Amanda de Moraes Narcizo
Mara Sanches Guaragna
Stanley de Almeida Araujo
Thais Medeiros Cruz
Jussara Soares Fontes
Vera Maria Santoro Belangero
Maria Helena Vaisbich
Friedhelm Hildebrandt
Matthew Gordon Sampson
Luiz Fernando Onuchic
author_facet Andreia Watanabe
Precil Diego Miranda de Menezes Neves
Kelly Nunes
Antonio Marcondes Lerario
Elieser Hitoshi Watanabe
Frederico Moraes Ferreira
Denise Maria Avancini Costa Malheiros
Amanda de Moraes Narcizo
Mara Sanches Guaragna
Stanley de Almeida Araujo
Thais Medeiros Cruz
Jussara Soares Fontes
Vera Maria Santoro Belangero
Maria Helena Vaisbich
Friedhelm Hildebrandt
Matthew Gordon Sampson
Luiz Fernando Onuchic
author_sort Andreia Watanabe
collection DOAJ
description Introduction: The profile of genetic and nongenetic factors associated with progression to kidney failure (KF) in steroid-resistant nephrotic syndrome (SRNS) is largely unknown in admixed populations. Methods: A total of 101 pediatric patients with primary SRNS were genetically assessed targeting Mendelian causes and APOL1 status with a 62-NS-gene panel or whole exome sequencing, as well as genetic ancestry. Variant pathogenicity was evaluated using the American College Medical of Genetics and Genomics (ACMG) criteria. Results: Focal segmental glomerulosclerosis (FSGS) was diagnosed in 54% of patients whereas familial disease was reported by 13%. The global genetic ancestry was 65% European, 22% African, 10.5% Native American, and 2% East-Asian, while 96% of cases presented with the first 3 components. APOL1 high-risk genotypes were identified in 8% of families and causative Mendelian variants in 12%: NPHS1 = 3, NPHS2 = 3, PLCE1 = 2, WT1 = 2, COQ2 = 1, and CUBN = 1. Two novel causative variants arose in the Native American background. The percentage of African genetic ancestry did not associate with the number of APOL1 risk alleles. Forty-four percent of all patients progressed to KF. Mendelian forms and APOL1 high-risk genotypes were associated with faster progression to KF. Cox regression analyses revealed that higher non-European genetic ancestry, self-declared non-White ethnicity, age of onset <1 year or ≥9 years, and non-minimal change disease (MCD) histology associated with higher risk of KF, independently of genetic findings. Conclusion: Mendelian variants and APOL1 high-risk genotype compose a unique causative genetic profile associated with pediatric SRNS in this highly admixed population, accounting for approximately 20% of families. This ancestry pattern is consistent with the identification of APOL1 high-risk genotypes in children with low proportion of African genetic ancestry. Self-declared ethnicity, age of manifestation and histology were independently associated with the risk of KF.
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spelling doaj-art-be152faabe8b4f13a41f97462f30bb5d2025-08-20T02:33:36ZengElsevierKidney International Reports2468-02492024-12-019123501351610.1016/j.ekir.2024.09.005Steroid-Resistant Nephrotic Syndrome Is Associated With a Unique Genetic Profile in a Highly Admixed Pediatric PopulationAndreia Watanabe0Precil Diego Miranda de Menezes Neves1Kelly Nunes2Antonio Marcondes Lerario3Elieser Hitoshi Watanabe4Frederico Moraes Ferreira5Denise Maria Avancini Costa Malheiros6Amanda de Moraes Narcizo7Mara Sanches Guaragna8Stanley de Almeida Araujo9Thais Medeiros Cruz10Jussara Soares Fontes11Vera Maria Santoro Belangero12Maria Helena Vaisbich13Friedhelm Hildebrandt14Matthew Gordon Sampson15Luiz Fernando Onuchic16Department of Pediatrics, University of São Paulo School of Medicine, São Paulo, Brazil; Division of Molecular Medicine, University of São Paulo School of Medicine, São Paulo, BrazilDivision of Molecular Medicine, University of São Paulo School of Medicine, São Paulo, Brazil; Division of Nephrology, University of São Paulo School of Medicine, São Paulo, BrazilDepartment of Genetics and Evolutionary Biology, Biosciences Institute, University of São Paulo, São Paulo, BrazilDivision of Endocrinology, University of Michigan, Ann Arbor, Michigan, USADivision of Molecular Medicine, University of São Paulo School of Medicine, São Paulo, Brazil; Division of Nephrology, University of São Paulo School of Medicine, São Paulo, BrazilDepartment of Pathology, University of São Paulo School of Medicine, São Paulo, BrazilDepartment of Pathology, University of São Paulo School of Medicine, São Paulo, BrazilLaboratório de Sequenciamento em Larga Escala (SELA), University of São Paulo School of Medicine, São Paulo, BrazilCenter for Molecular Biology and Genetic Engineering, State University of Campinas, Campinas, BrazilDivision of Pathology, Federal University of Minas Gerais, Belo Horizonte, BrazilDivision of Pediatric Nephrology, Federal University of Rio Grande do Norte, Natal, BrazilFederal University of São João Del Rei, Campus Centro-Oeste Dona Lindu, Divinópolis, BrazilDepartment of Pediatrics, State University of Campinas, Campinas, BrazilDepartment of Pediatrics, University of São Paulo School of Medicine, São Paulo, BrazilDivision of Pediatric Nephrology, Boston Children’s Hospital, Boston, Massachusetts, USA; Harvard Medical School, Boston, Massachusetts, USA; Broad Institute, Cambridge, Massachusetts, USADivision of Pediatric Nephrology, Boston Children’s Hospital, Boston, Massachusetts, USA; Harvard Medical School, Boston, Massachusetts, USA; Broad Institute, Cambridge, Massachusetts, USADivision of Molecular Medicine, University of São Paulo School of Medicine, São Paulo, Brazil; Division of Nephrology, University of São Paulo School of Medicine, São Paulo, Brazil; Correspondence: Luiz F. Onuchic, Divisions of Nephrology and Molecular Medicine, University of São Paulo School of Medicine, Avenida Dr. Arnaldo, 455 - Sala 4304, São Paulo, SP, 01246-903, Brazil.Introduction: The profile of genetic and nongenetic factors associated with progression to kidney failure (KF) in steroid-resistant nephrotic syndrome (SRNS) is largely unknown in admixed populations. Methods: A total of 101 pediatric patients with primary SRNS were genetically assessed targeting Mendelian causes and APOL1 status with a 62-NS-gene panel or whole exome sequencing, as well as genetic ancestry. Variant pathogenicity was evaluated using the American College Medical of Genetics and Genomics (ACMG) criteria. Results: Focal segmental glomerulosclerosis (FSGS) was diagnosed in 54% of patients whereas familial disease was reported by 13%. The global genetic ancestry was 65% European, 22% African, 10.5% Native American, and 2% East-Asian, while 96% of cases presented with the first 3 components. APOL1 high-risk genotypes were identified in 8% of families and causative Mendelian variants in 12%: NPHS1 = 3, NPHS2 = 3, PLCE1 = 2, WT1 = 2, COQ2 = 1, and CUBN = 1. Two novel causative variants arose in the Native American background. The percentage of African genetic ancestry did not associate with the number of APOL1 risk alleles. Forty-four percent of all patients progressed to KF. Mendelian forms and APOL1 high-risk genotypes were associated with faster progression to KF. Cox regression analyses revealed that higher non-European genetic ancestry, self-declared non-White ethnicity, age of onset <1 year or ≥9 years, and non-minimal change disease (MCD) histology associated with higher risk of KF, independently of genetic findings. Conclusion: Mendelian variants and APOL1 high-risk genotype compose a unique causative genetic profile associated with pediatric SRNS in this highly admixed population, accounting for approximately 20% of families. This ancestry pattern is consistent with the identification of APOL1 high-risk genotypes in children with low proportion of African genetic ancestry. Self-declared ethnicity, age of manifestation and histology were independently associated with the risk of KF.http://www.sciencedirect.com/science/article/pii/S2468024924019235APOL1childrenfocal segmental glomerulosclerosisgenetic ancestrymonogenic chronic kidney diseasesteroid-resistant nephrotic syndrome
spellingShingle Andreia Watanabe
Precil Diego Miranda de Menezes Neves
Kelly Nunes
Antonio Marcondes Lerario
Elieser Hitoshi Watanabe
Frederico Moraes Ferreira
Denise Maria Avancini Costa Malheiros
Amanda de Moraes Narcizo
Mara Sanches Guaragna
Stanley de Almeida Araujo
Thais Medeiros Cruz
Jussara Soares Fontes
Vera Maria Santoro Belangero
Maria Helena Vaisbich
Friedhelm Hildebrandt
Matthew Gordon Sampson
Luiz Fernando Onuchic
Steroid-Resistant Nephrotic Syndrome Is Associated With a Unique Genetic Profile in a Highly Admixed Pediatric Population
Kidney International Reports
APOL1
children
focal segmental glomerulosclerosis
genetic ancestry
monogenic chronic kidney disease
steroid-resistant nephrotic syndrome
title Steroid-Resistant Nephrotic Syndrome Is Associated With a Unique Genetic Profile in a Highly Admixed Pediatric Population
title_full Steroid-Resistant Nephrotic Syndrome Is Associated With a Unique Genetic Profile in a Highly Admixed Pediatric Population
title_fullStr Steroid-Resistant Nephrotic Syndrome Is Associated With a Unique Genetic Profile in a Highly Admixed Pediatric Population
title_full_unstemmed Steroid-Resistant Nephrotic Syndrome Is Associated With a Unique Genetic Profile in a Highly Admixed Pediatric Population
title_short Steroid-Resistant Nephrotic Syndrome Is Associated With a Unique Genetic Profile in a Highly Admixed Pediatric Population
title_sort steroid resistant nephrotic syndrome is associated with a unique genetic profile in a highly admixed pediatric population
topic APOL1
children
focal segmental glomerulosclerosis
genetic ancestry
monogenic chronic kidney disease
steroid-resistant nephrotic syndrome
url http://www.sciencedirect.com/science/article/pii/S2468024924019235
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