Population structure, differential bias and genomic control in a large-scale, case-control association study.
paper
Cited
Public
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- Authors
- Clayton, David G; Walker, Neil M; Smyth, Deborah J; Pask, Rebecca; Cooper, Jason D; Maier, Lisa M; Smink, Luc J; Lam, Alex C; Ovington, Nigel R; Stevens, Helen E; Nutland, Sarah; Howson, Joanna M M; Faham, Malek; Moorhead, Martin; Jones, Hywel B; Falkowski, Matthew; Hardenbol, Paul; Willis, Thomas D; Todd, John A
- Year
- 2005
- Journal
- Nature genetics
- PMID
- 16228001
- DOI
- 10.1038/ng1653
The main problems in drawing causal inferences from epidemiological case-control studies are confounding by unmeasured extraneous factors, selection bias and differential misclassification of exposure. In genetics the first of these, in the form of population structure, has dominated recent debate. Population structure explained part of the significant +11.2% inflation of test statistics we observed in an analysis of 6,322 nonsynonymous SNPs in 816 cases of type 1 diabetes and 877 population-based controls from Great Britain. The remainder of the inflation resulted from differential bias in genotype scoring between case and control DNA samples, which originated from two laboratories, causing false-positive associations. To avoid excluding SNPs and losing valuable information, we extended the genomic control method by applying a variable downweighting to each SNP.
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| Finding common susceptibility variants for complex disease: past, present and future. | Panoutsopoulou K et al. | β | 2009 | β |
| Genetic regulation of adult stature. | Lettre G | β | 2009 | β |
| Genome-wide association studies--a summary for the clinical gastroenterologist. | Melum E et al. | β | 2009 | β |
| Genome-wide association studies: quality control and population-based measures. | Ziegler A | β | 2009 | β |
| Genome-wide association study identifies five susceptibility loci for glioma. | Shete S et al. | β | 2009 | β |
| Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer's disease. | Harold D et al. | β | 2009 | β |
| Genome-wide association study in humans. | Smith JG et al. | β | 2009 | β |
| Genomic copy number variation, human health, and disease. | Wain LV et al. | β | 2009 | β |
| Genotyping and inflated type I error rate in genome-wide association case/control studies. | Sampson JN et al. | β | 2009 | β |
| IFIH1-GCA-KCNH7 locus is not associated with genetic susceptibility to multiple sclerosis in French patients. | Couturier N et al. | β | 2009 | β |
| IL2RA genetic heterogeneity in multiple sclerosis and type 1 diabetes susceptibility and soluble interleukin-2 receptor production. | Maier LM et al. | β | 2009 | β |
| Impaired performance of FDR-based strategies in whole-genome association studies when SNPs are excluded prior to the analysis. | Marenne G et al. | β | 2009 | β |
| Lack of association between genetic polymorphisms in enzymes associated with folate metabolism and unexplained reduced sperm counts. | Ravel C et al. | β | 2009 | β |
| Loci on 7p12.2, 10q21.2 and 14q11.2 are associated with risk of childhood acute lymphoblastic leukemia. | Papaemmanuil E et al. | β | 2009 | β |
| Microarray analysis of multiple candidate genes and associated plasma proteins for nephropathy secondary to type 2 diabetes among Chinese individuals. | Lim SC et al. | β | 2009 | β |
| Missing call bias in high-throughput genotyping. | Fu W et al. | β | 2009 | β |
| Multi-criteria decision making approaches for quality control of genome-wide association studies. | Malovini A et al. | β | 2009 | β |
| Multiplex Paralogue Ratio Tests for accurate measurement of multiallelic CNVs. | Walker S et al. | β | 2009 | β |
| No association of multiple type 2 diabetes loci with type 1 diabetes. | Raj SM et al. | β | 2009 | β |
| Population-based genomewide genetic analysis of common clinical chemistry analytes. | Chasman DI et al. | β | 2009 | β |
| Power consequences of linkage disequilibrium variation between populations. | Teo YY et al. | β | 2009 | β |
| Recent advances of genetic ancestry testing in biomedical research and direct to consumer testing. | Via M et al. | β | 2009 | β |
| Replication of celiac disease UK genome-wide association study results in a US population. | Garner CP et al. | β | 2009 | β |
| Simultaneous genotype calling and haplotype phasing improves genotype accuracy and reduces false-positive associations for genome-wide association studies. | Browning BL et al. | β | 2009 | β |
| Strengthening the reporting of genetic association studies (STREGA): an extension of the strengthening the reporting of observational studies in epidemiology (STROBE) statement. | Little J et al. | β | 2009 | β |
| Strengthening the reporting of genetic association studies (STREGA): an extension of the STROBE statement. | Little J et al. | β | 2009 | β |
| Strengthening the reporting of genetic association studies (STREGA): an extension of the STROBE Statement. | Little J et al. | β | 2009 | β |
| STrengthening the REporting of Genetic Association studies (STREGA)--an extension of the STROBE statement. | Little J et al. | β | 2009 | β |
| STrengthening the REporting of Genetic Association studies (STREGA): an extension of the STROBE Statement. | Little J et al. | β | 2009 | β |
| STrengthening the REporting of Genetic Association Studies (STREGA)--an extension of the STROBE statement. | Little J et al. | β | 2009 | β |
| STrengthening the REporting of Genetic Association Studies (STREGA): an extension of the STROBE statement. | Little J et al. | β | 2009 | β |
| Systematic reviews of genetic association studies. Human Genome Epidemiology Network. | Sagoo GS et al. | β | 2009 | β |
| Targeted genome-wide investigation identifies novel SNPs associated with diabetic nephropathy. | McKnight AJ et al. | β | 2009 | β |
| The combined effect of SNP-marker and phenotype attributes in genome-wide association studies. | Chan EK et al. | β | 2009 | β |
| The impact of divergence time on the nature of population structure: an example from Iceland. | Price AL et al. | β | 2009 | β |
| The virtues of a deliberately mis-specified disease model in demonstrating a gene-environment interaction. | Burstyn I et al. | β | 2009 | β |
| Variants in TF and HFE explain approximately 40% of genetic variation in serum-transferrin levels. | Benyamin B et al. | β | 2009 | β |
| Variation in genetic admixture and population structure among Latinos: the Los Angeles Latino eye study (LALES). | Shtir CJ et al. | β | 2009 | β |
| Accounting for ancestry: population substructure and genome-wide association studies. | Tian C et al. | β | 2008 | β |
| A genome-wide association study identifies colorectal cancer susceptibility loci on chromosomes 10p14 and 8q23.3. | Tomlinson IP et al. | β | 2008 | β |
| Analysis and application of European genetic substructure using 300 K SNP information. | Tian C et al. | β | 2008 | β |
| Analysis of quantitative trait loci. | Falchi M | β | 2008 | β |
| Application of ancestry informative markers to association studies in European Americans. | Seldin MF et al. | β | 2008 | β |
| Appropriate data cleaning methods for genome-wide association study. | Miyagawa T et al. | β | 2008 | β |
| A robust statistical method for case-control association testing with copy number variation. | Barnes C et al. | β | 2008 | β |
| Assessment of cumulative evidence on genetic associations: interim guidelines. | Ioannidis JP et al. | β | 2008 | β |
| Association mapping and significance estimation via the coalescent. | Kimmel G et al. | β | 2008 | β |
| Association of interleukin-6 gene polymorphisms with bone mineral density in Mexican women. | MagaΓ±a JJ et al. | β | 2008 | β |
| Biostatistical aspects of genome-wide association studies. | Ziegler A et al. | β | 2008 | β |
| Common genetic variation and human disease. | Orr N et al. | β | 2008 | β |
| Common statistical issues in genome-wide association studies: a review on power, data quality control, genotype calling and population structure. | Teo YY | β | 2008 | β |
| Confounding in genetic association studies and its solutions. | Hu D et al. | β | 2008 | β |
| Copy-number analysis goes more than skin deep. | McCarroll SA | β | 2008 | β |
| Defensins and the dynamic genome: what we can learn from structural variation at human chromosome band 8p23.1. | Hollox EJ et al. | β | 2008 | β |
| Differences in prevalence and severity of coronary artery calcification between two non-Hispanic white populations with diverse lifestyles. | Bielak LF et al. | β | 2008 | β |
| Discerning the ancestry of European Americans in genetic association studies. | Price AL et al. | β | 2008 | β |
| Estimating local ancestry in admixed populations. | Sankararaman S et al. | β | 2008 | β |
| Extending genome-wide association studies to copy-number variation. | McCarroll SA | β | 2008 | β |
| Family-based methods for linkage and association analysis. | Laird NM et al. | β | 2008 | β |
| Genetic association analyses of non-synonymous single nucleotide polymorphisms in diabetic nephropathy. | Savage DA et al. | β | 2008 | β |
| Genetic mapping in human disease. | Altshuler D et al. | β | 2008 | β |
| Genome-wide analysis of single nucleotide polymorphisms uncovers population structure in Northern Europe. | Salmela E et al. | β | 2008 | β |
| Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease. | Barrett JC et al. | β | 2008 | β |
| Genome-wide association studies for complex traits: consensus, uncertainty and challenges. | McCarthy MI et al. | β | 2008 | β |
| Genome-wide association studies in psychiatry: lessons from early studies of non-psychiatric and psychiatric phenotypes. | Craddock N et al. | β | 2008 | β |
| Goldsurfer2 (Gs2): a comprehensive tool for the analysis and visualization of genome wide association studies. | Pettersson F et al. | β | 2008 | β |
| Haplotypic analysis of Wellcome Trust Case Control Consortium data. | Browning BL et al. | β | 2008 | β |
| Integrated genotype calling and association analysis of SNPs, common copy number polymorphisms and rare CNVs. | Korn JM et al. | β | 2008 | β |
| Investigation of the fine structure of European populations with applications to disease association studies. | Heath SC et al. | β | 2008 | β |
| Is MYO9B the missing link between schizophrenia and celiac disease? | Jungerius BJ et al. | β | 2008 | β |
| Linkage disequilibrium-based quality control for large-scale genetic studies. | Scheet P et al. | β | 2008 | β |
| Meta-analysis of genome-wide association study data identifies additional type 1 diabetes risk loci. | Cooper JD et al. | β | 2008 | β |
| Mitochondrial DNA haplogroups influence AIDS progression. | Hendrickson SL et al. | β | 2008 | β |
| Perturbation analysis: a simple method for filtering SNPs with erroneous genotyping in genome-wide association studies. | Teo YY et al. | β | 2008 | β |
| Population structure and inbreeding from pedigree analysis of purebred dogs. | Calboli FC et al. | β | 2008 | β |
| Population substructure in Finland and Sweden revealed by the use of spatial coordinates and a small number of unlinked autosomal SNPs. | Hannelius U et al. | β | 2008 | β |
| Power of genetic association studies in the presence of linkage disequilibrium and allelic heterogeneity. | Fisher SA et al. | β | 2008 | β |
| Practical aspects of imputation-driven meta-analysis of genome-wide association studies. | de Bakker PI et al. | β | 2008 | β |
| Psoriasis is associated with increased beta-defensin genomic copy number. | Hollox EJ et al. | β | 2008 | β |
| PTPN22 Trp620 explains the association of chromosome 1p13 with type 1 diabetes and shows a statistical interaction with HLA class II genotypes. | Smyth DJ et al. | β | 2008 | β |
| Refining genetic associations in multiple sclerosis. | International Multiple Sclerosis Genetics Consortium (IMSGC) | β | 2008 | β |
| Required sample size and nonreplicability thresholds for heterogeneous genetic associations. | Moonesinghe R et al. | β | 2008 | β |
| Scan of 977 nonsynonymous SNPs in CLL4 trial patients for the identification of genetic variants influencing prognosis. | Sellick GS et al. | β | 2008 | β |
| Sequencing-based genotyping and association analysis of the MICA and MICB genes in type 1 diabetes. | Field SF et al. | β | 2008 | β |
| Smarter clustering methods for SNP genotype calling. | Lin Y et al. | β | 2008 | β |
| Study designs for genome-wide association studies. | Kraft P et al. | β | 2008 | β |
| Susceptibility loci for intracranial aneurysm in European and Japanese populations. | Bilguvar K et al. | β | 2008 | β |
| Synthesis of genetic association studies for pertinent gene-disease associations requires appropriate methodological and statistical approaches. | Zintzaras E et al. | β | 2008 | β |
| The complex genetics of multiple sclerosis: pitfalls and prospects. | Sawcer S | β | 2008 | β |
| The positives, protocols, and perils of genome-wide association. | Neale BM et al. | β | 2008 | β |
| TNFA -308G>A in two international population-based cohorts and risk of asthma. | Castro-Giner F et al. | β | 2008 | β |
| A common variant of HMGA2 is associated with adult and childhood height in the general population. | Weedon MN et al. | β | 2007 | β |
| African Americans with asthma: genetic insights. | Barnes KC et al. | β | 2007 | β |
| A genome-wide association study identifies novel risk loci for type 2 diabetes. | Sladek R et al. | β | 2007 | β |
| A genomic background based method for association analysis in related individuals. | Amin N et al. | β | 2007 | β |
| A method to address differential bias in genotyping in large-scale association studies. | Plagnol V et al. | β | 2007 | β |
| Analysis of BTNL2 genetic polymorphisms in British and Dutch patients with sarcoidosis. | Spagnolo P et al. | β | 2007 | β |
| An Arabidopsis example of association mapping in structured samples. | Zhao K et al. | β | 2007 | β |
| An evaluation of power and type I error of single-nucleotide polymorphism transmission/disequilibrium-based statistical methods under different family structures, missing parental data, and population stratification. | Nicodemus KK et al. | β | 2007 | β |
| A new multipoint method for genome-wide association studies by imputation of genotypes. | Marchini J et al. | β | 2007 | β |
| An R package for analysis of whole-genome association studies. | Clayton D et al. | β | 2007 | β |
| A randomization test for controlling population stratification in whole-genome association studies. | Kimmel G et al. | β | 2007 | β |
| Association of the estrogen receptor alpha gene polymorphisms with osteoporosis in the Mexican population. | GΓ³mez R et al. | β | 2007 | β |
| Association of the interleukin-2 receptor alpha (IL-2Ralpha)/CD25 gene region with Graves' disease using a multilocus test and tag SNPs. | Brand OJ et al. | β | 2007 | β |
| Association of the vitamin D metabolism gene CYP27B1 with type 1 diabetes. | Bailey R et al. | β | 2007 | β |
| Association scan of 14,500 nonsynonymous SNPs in four diseases identifies autoimmunity variants. | Wellcome Trust Case Control Consortium et al. | β | 2007 | β |
| A type 1 diabetes subgroup with a female bias is characterised by failure in tolerance to thyroid peroxidase at an early age and a strong association with the cytotoxic T-lymphocyte-associated antigen-4 gene. | Howson JM et al. | β | 2007 | β |
| Bias in association studies of systemic lupus erythematosus susceptibility due to geographical variation in the frequency of a programmed cell death 1 polymorphism across Europe. | Ferreiros-Vidal I et al. | β | 2007 | β |
| Copy-number variation and association studies of human disease. | McCarroll SA et al. | β | 2007 | β |
| Endometriosis and genetic polymorphisms. | Falconer H et al. | β | 2007 | β |
| Fine mapping versus replication in whole-genome association studies. | Clarke GM et al. | β | 2007 | β |
| Genes, environment, health, and disease: facing up to complexity. | Manolio TA et al. | β | 2007 | β |
| Genome bioinformatic analysis of nonsynonymous SNPs. | Burke DF et al. | β | 2007 | β |
| Genome-wide analysis of barcoded Saccharomyces cerevisiae gene-deletion mutants in pooled cultures. | Pierce SE et al. | β | 2007 | β |
| Genome-wide association analysis identifies loci for type 2 diabetes and triglyceride levels. | Diabetes Genetics Initiative of Broad Institute of Harvard and MIT et al. | β | 2007 | β |
| Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. | Wellcome Trust Case Control Consortium | β | 2007 | β |
| Genome-wide association study of restless legs syndrome identifies common variants in three genomic regions. | Winkelmann J et al. | β | 2007 | β |
| Genomic DNA pooling for whole-genome association scans in complex disease: empirical demonstration of efficacy in rheumatoid arthritis. | Steer S et al. | β | 2007 | β |
| IL23R variation determines susceptibility but not disease phenotype in inflammatory bowel disease. | Tremelling M et al. | β | 2007 | β |
| Interaction analysis of the CBLB and CTLA4 genes in type 1 diabetes. | Payne F et al. | β | 2007 | β |
| Introduction to genetic association studies. | Tsao H et al. | β | 2007 | β |
| Lack of association between polymorphisms in the gene encoding protein tyrosine phosphatase 1B (PTPN1) and risk of Type 2 diabetes. | Wanic K et al. | β | 2007 | β |
| Large-scale genetic fine mapping and genotype-phenotype associations implicate polymorphism in the IL2RA region in type 1 diabetes. | Lowe CE et al. | β | 2007 | β |
| Linear trend tests for case-control genetic association that incorporate random phenotype and genotype misclassification error. | Gordon D et al. | β | 2007 | β |
| Localization of type 1 diabetes susceptibility to the MHC class I genes HLA-B and HLA-A. | Nejentsev S et al. | β | 2007 | β |
| Methods for linkage disequilibrium mapping in crops. | Mackay I et al. | β | 2007 | β |
| Non-replication and inconsistency in the genome-wide association setting. | Ioannidis JP | β | 2007 | β |
| One degree of freedom for dominance in indirect association studies. | Chapman J et al. | β | 2007 | β |
| On the synthesis and interpretation of consistent but weak gene-disease associations in the era of genome-wide association studies. | Khoury MJ et al. | β | 2007 | β |
| On the usage of HWE for identifying genotyping errors. | Teo YY et al. | β | 2007 | β |
| Pharmacogenomics: single genes, whole genomes and global networks. | Kennedy MA | β | 2007 | β |
| Platelet genomics and the risk of atherothrombosis. | Ouwehand WH et al. | β | 2007 | β |
| PLINK: a tool set for whole-genome association and population-based linkage analyses. | Purcell S et al. | β | 2007 | β |
| Polymorphisms of TLR4 but not CD14 are associated with a decreased risk of aggressive periodontitis. | James JA et al. | β | 2007 | β |
| Power of genome-wide association studies in the presence of interacting loci. | Pickrell J et al. | β | 2007 | β |
| Robust associations of four new chromosome regions from genome-wide analyses of type 1 diabetes. | Todd JA et al. | β | 2007 | β |
| Simultaneously correcting for population stratification and for genotyping error in case-control association studies. | Cheng KF et al. | β | 2007 | β |
| Systematic association mapping identifies NELL1 as a novel IBD disease gene. | Franke A et al. | β | 2007 | β |
| The association of a SNP upstream of INSIG2 with body mass index is reproduced in several but not all cohorts. | Lyon HN et al. | β | 2007 | β |
| The candidate genes TAF5L, TCF7, PDCD1, IL6 and ICAM1 cannot be excluded from having effects in type 1 diabetes. | Cooper JD et al. | β | 2007 | β |
| The effects of SNP genotyping errors on the power of the Cochran-Armitage linear trend test for case/control association studies. | Ahn K et al. | β | 2007 | β |
| The Framingham Heart Study 100K SNP genome-wide association study resource: overview of 17 phenotype working group reports. | Cupples LA et al. | β | 2007 | β |
| The genetics of cardiac birth defects. | Ransom J et al. | β | 2007 | β |
| The NCBI dbGaP database of genotypes and phenotypes. | Mailman MD et al. | β | 2007 | β |
| Two genome-wide association studies of aggressive prostate cancer implicate putative prostate tumor suppressor gene DAB2IP. | Duggan D et al. | β | 2007 | β |
| Two independent alleles at 6q23 associated with risk of rheumatoid arthritis. | Plenge RM et al. | β | 2007 | β |
| A fast method for computing high-significance disease association in large population-based studies. | Kimmel G et al. | β | 2006 | β |
| A genome-wide association study of nonsynonymous SNPs identifies a type 1 diabetes locus in the interferon-induced helicase (IFIH1) region. | Smyth DJ et al. | β | 2006 | β |
| Analysis of polymorphisms in 16 genes in type 1 diabetes that have been associated with other immune-mediated diseases. | Smyth DJ et al. | β | 2006 | β |
| Analysis of polymorphisms of the interleukin-18 gene in type 1 diabetes and Hardy-Weinberg equilibrium testing. | Szeszko JS et al. | β | 2006 | β |
| Application of oligonucleotide arrays to high-content genetic analysis. | Gibson NJ | β | 2006 | β |
| Are molecular haplotypes worth the time and expense? A cost-effective method for applying molecular haplotypes. | Levenstien MA et al. | β | 2006 | β |
| A tutorial on statistical methods for population association studies. | Balding DJ | β | 2006 | β |
| Beta2-adrenoceptor polymorphisms and asthma from childhood to middle age in the British 1958 birth cohort: a genetic association study. | Hall IP et al. | β | 2006 | β |
| Common genetic variants for breast cancer: 32 largely refuted candidates and larger prospects. | Ioannidis JP | β | 2006 | β |
| Common Kibra alleles are associated with human memory performance. | Papassotiropoulos A et al. | β | 2006 | β |
| Definition of novel GP6 polymorphisms and major difference in haplotype frequencies between populations by a combination of in-depth exon resequencing and genotyping with tag single nucleotide polymorphisms. | Watkins NA et al. | β | 2006 | β |
| Discovery, linkage disequilibrium and association analyses of polymorphisms of the immune complement inhibitor, decay-accelerating factor gene (DAF/CD55) in type 1 diabetes. | Taniguchi H et al. | β | 2006 | β |
| Effects of differential genotyping error rate on the type I error probability of case-control studies. | Moskvina V et al. | β | 2006 | β |
| EUDRAGENE: European collaboration to establish a case-control DNA collection for studying the genetic basis of adverse drug reactions. | Molokhia M et al. | β | 2006 | β |
| Evaluating coverage of genome-wide association studies. | Barrett JC et al. | β | 2006 | β |
| Family-based designs in the age of large-scale gene-association studies. | Laird NM et al. | β | 2006 | β |
| Family-based versus unrelated case-control designs for genetic associations. | Evangelou E et al. | β | 2006 | β |
| Genetic dissection of the common epilepsies. | Tan NC et al. | β | 2006 | β |
| Genetics. Delivering new disease genes. | Cardon LR | β | 2006 | β |
| High-volume "-omics" technologies and the future of molecular epidemiology. | Thomas DC | β | 2006 | β |
| LRTae: improving statistical power for genetic association with case/control data when phenotype and/or genotype misclassification errors are present. | Barral S et al. | β | 2006 | β |
| No evidence for association of OAS1 with type 1 diabetes in unaffected siblings or type 1 diabetic cases. | Smyth DJ et al. | β | 2006 | β |
| Optimal genotype determination in highly multiplexed SNP data. | Moorhead M et al. | β | 2006 | β |
| Overrepresentation of rare variants in a specific ethnic group may confuse interpretation of association analyses. | Keen-Kim D et al. | β | 2006 | β |
| Population structure and eigenanalysis. | Patterson N et al. | β | 2006 | β |
| Principal components analysis corrects for stratification in genome-wide association studies. | Price AL et al. | β | 2006 | β |
| Statistical false positive or true disease pathway? | Todd JA | β | 2006 | β |
| The catechol-O-methyl transferase (COMT) gene as a candidate for psychiatric phenotypes: evidence and lessons. | Craddock N et al. | β | 2006 | β |
| Unraveling the genetics of human obesity. | Mutch DM et al. | β | 2006 | β |
| Updating the East Asian mtDNA phylogeny: a prerequisite for the identification of pathogenic mutations. | Kong QP et al. | β | 2006 | β |