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GenABEL: an R library for genome-wide association analysis
Abstract
Here we describe an R library for genome-wide association (GWA) analysis. It implements effective storage and handling of GWA data, fast procedures for genetic data quality control, testing of association of single nucleotide polymorphisms with binary or quantitative traits, visualization of results and also provides easy interfaces to standard statistical and graphical procedures implemented in base R and special R libraries for genetic analysis. We evaluated GenABEL using one simulated and two real data sets. We conclude that GenABEL enables the analysis of GWA data on desktop computers. Availability: http://cran.r-project.org Contact: i.aoultchenko@erasmusmc.nl
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“The genomic inflation factor lambda was computed with the GenABEL 1.8-0 R package63 and a median approach after exclusion of the APOE region (44–46 Mb on chromosome 19 in GRCh38).”
From New insights into the genetic etiology of Alzheimer’s disease and related dementias (2022) · cites this paper as [63]
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MethodShadrina, A. S., Tsepilov, Y. A., Sokolova, E. А., Smetanina, M. A., Voronina, E. N., Pakhomov, E., Sevost’ianova, K. S., Shevela, A. I., Ilyukhin, Е. А., Seliverstov, E. I., et al. (2018) · Gene · doi:10.1016/j.gene.2018.03.039 · Cited by 22
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“The association between each SNP, assuming an additive genetic model, and overall survival was examined using Cox proportional hazards models, adjusted for age, sex and one principal component, using the GenABLE package of R [123].”
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“( Yang et al., 2014) Regression coefficients and standard error estimates were generated within each study and then carried forward for meta-analysis using Metasoft(Han and Eskin, 2011) and the R MetABEL package(Aulchenko et al., 2007) for plotting of results.”
kConFab Investigators, Agarwal, D., Australian Ovarian Cancer Study Group, The GENICA Network, TNBCC, Pineda, S., Michailidou, K., Herránz, J., Pita, G., Moreno, L. T., et al. (2014) · British Journal of Cancer · doi:10.1038/bjc.2013.769 · Cited by 29
“These were converted to allele doses using the impute2mach function in the GenABEL library in R (Aulchenko et al, 2007) and analysed under a per-allele model.”
MethodA systems genetics study of swine illustrates mechanisms underlying human phenotypic traits
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“The associations between phenotypes and genome-wide SNP genotype data were analyzed with the single-marker association model in the GenABEL package [12] based on a mixed linear model implemented with the mmscore function of GenABEL in R package.”
MethodEMBRACE, Hamdi, Y., Collaborators, G. S., HEBON, KConFab Investigators, Soucy, P., Kuchenbaecker, K. B., Pastinen, T., Droit, A., Lemaçon, A., et al. (2016) · Breast Cancer Research and Treatment · doi:10.1007/s10549-016-4018-2 · Cited by 22
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“…studies have reported that ignoring 315 population stratification can result in the inflation of false positives and 316 reduce the statistical power(Aulchenko et al., 2007; Matthieu, Christophe, Page 14 of 42 https://mc06.manuscriptcentral.com/genome-pubs Genome Draft 317 Mickael, & Thomas, 2011).”
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Zhong, C., Li, X., Guan, D., Zhang, B., Wang, X., Qu, L., Zhou, H., Fang, L., Sun, C., & Yang, N. (2024) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2024.09.003 · Cited by 22
Connell, S., Meade, K. G., Allan, B. J., Lloyd, A. T., Downing, T., O’Farrelly, C., & Bradley, D. G. (2013) · G3 Genes Genomes Genetics · doi:10.1534/g3.113.006031 · Cited by 21
“Average IBS was calculated from all SNP genotypes in the R package GenABEL [38].”
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Park, M. N., Choi, J. A., Lee, K., Lee, H. J., Choi, B., Kim, H., Kim, T.-H., Cho, S., & Lee, T. (2013) · Asian-Australasian Journal of Animal Sciences · doi:10.5713/ajas.2013.13413 · Cited by 21
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Quan, J., Ding, R., Wang, X., Yang, M. J., Yang, Y., Zheng, E., Gu, T., Cai, G., Wu, Z., Liu, D., et al. (2017) · Asian-Australasian Journal of Animal Sciences · doi:10.5713/ajas.17.0356 · Cited by 21
“Generalized mixed linear model and population stratification assay Association analyses based on the generalized MLM were conducted using GenABEL in R software [15].”
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Satpathy, S., Clark, N. M., Chen, Y., Hosseini, N., Chang, Y.-H., Hsiao, Y., Lei, J. T., Petralia, F., Chen, J., Geffen, Y., et al. (2025) · Cancer Cell · doi:10.1016/j.ccell.2025.07.011 · Cited by 23
Rungroj, N., Nettuwakul, C., Sudtachat, N., Praditsap, O., Sawasdee, N., Sritippayawan, S., Chuawattana, D., & Yenchitsomanus, P. (2014) · BMC Medical Genetics · doi:10.1186/1471-2350-15-50 · Cited by 20
“05) between 101 patients and 105 normal control subjects were examined by GenABEL package with no adjustment for binary traits; the test is equivalent to the Armitage test [24].”
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Moretti, R., Soglia, D., Chessa, S., Sartore, S., Finocchiaro, R., Rasero, R., & Sacchi, P. (2021) · Animals · doi:10.3390/ani11020366 · Cited by 20
Henry, B., Volle, G., Akpovi, H., Gineau, L., Roussel, C., Ndour, P. A., Tossou, F., Suárez, F., PALSTRA, F. P., Fricot, A., et al. (2022) · EBioMedicine · doi:10.1016/j.ebiom.2022.104167 · Cited by 20
Pathak, R. K., & Kim, J. (2022) · Frontiers in Veterinary Science · doi:10.3389/fvets.2022.1008728 · Cited by 22
Johnson, E. O., Hancock, D. B., Levy, J. L., Gaddis, N., Page, G. P., Glasheen, C., Saccone, N. L., Bierut, L. J., & Kral, A. H. (2015) · Addiction Biology · doi:10.1111/adb.12286 · Cited by 18
“Discovery genome-wide association study analyses GWAS analyses were conducted in each ancestry group to test the imputed SNP and indel genotype dosages for association with drug abuse using logistic regression models in ProbABEL (Aulchenko et al. 2007).”
The Buffalo Genome and the Application of Genomics in Animal Management and Improvement
Iamartino, D., Williams, J. L., Sonstegard, T. S., Reecy, J. M., Tassell, C. P. V., Nicolazzi, E. L., Biffani, S., Biscarini, F., Schroeder, S., Oliveira, D. A. A., et al. (2013) · LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) · doi:10.13140/rg.2.2.30951.85924 · Cited by 20
Sung, Y. J., Winkler, T. W., Manning, A. K., Aschard, H., Gudnason, V. G., Harris, T. B., Smith, A. V., Boerwinkle, E., Brown, M. R., Morrison, A. C., et al. (2016) · Genetic Epidemiology · doi:10.1002/gepi.21978 · Cited by 19
“The remaining two studies used the linear mixed effect model approach with a random polygenic component (for which the covariance matrix depends on the kinship matrix) with GenABEL [Aulchenko et al., 2007] or R (supplementary Table S1).”
MethodNLRC5 polymorphism is associated with susceptibility to chronic periodontitis
Zupin, L., Navarra, C. O., Robino, A., Bevilacqua, L., Lenarda, R. D., Gasparini, P., & Crovella, S. (2017) · Immunobiology · doi:10.1016/j.imbio.2017.01.001 · Cited by 20
Garza-Hernandez, D., Mucha, S., Banos, G., Kaseja, K., Moore, K., Lambe, N. R., Yates, J., & Bünger, L. (2017) · animal · doi:10.1017/s1751731117002488 · Cited by 20
“177 Quality control (QC) was performed with the GenABEL R package by considering 178 genotypes of all rams (Aulchenko et al., 2007).”
MethodSutera, A. M., Riggio, V., Mastrangelo, S., Gerlando, R. D., Sardina, M. T., Pong‐Wong, R., Tolone, M., & Portolano, B. (2019) · Animal Genetics · doi:10.1111/age.12789 · Cited by 20
Qu, L., Shen, M., Guo, J., Wang, X., Dou, T., Hu, Y., Li, Y., Ma, M., Wang, K., & Liu, H. (2019) · Archives animal breeding/Archiv für Tierzucht · doi:10.5194/aab-62-113-2019 · Cited by 20
“The GenABEL package (Aulchenko et al., 2007) in the R project was used to calculate the genomic inflation factor resulting from the estimate of false positive signals.”
MethodHolborn, M. K., Rochus, C. M., Ang, K. P., Elliott, J. A. K., Leadbeater, S., Powell, F., & Boulding, E. G. (2019) · Aquaculture · doi:10.1016/j.aquaculture.2019.734215 · Cited by 20
Genetic architecture underlying the expression of eight α-amylase trypsin inhibitors
Hassouni, K. E., Sielaff, M., Curella, V., Neerukonda, M., Leiser, W. L., Würschum, T., Schuppan, D., Tenzer, S., & Longin, C. F. H. (2021) · Theoretical and Applied Genetics · doi:10.1007/s00122-021-03906-y · Cited by 20
Determinants of retinal microvascular features and their relationships in two European populations
Kirin, M., Nagy, R., MacGillivray, T., Polašek, O., Hayward, C., Rudan, I., Campbell, H., Wild, S. H., Wright, A. F., Wilson, J. F., et al. (2017) · Journal of Hypertension · doi:10.1097/hjh.0000000000001408 · Cited by 20
Canine NAPEPLD-associated models of human myelin disorders
Minor, K. M., Letko, A., Becker, D., Drögemüller, M., Mandigers, P. J. J., Bellekom, S., Leegwater, P. A. J., Stassen, Q. E. M., Putschbach, K., Fischer, A., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-23938-7 · Cited by 20
Correction: Common Genetic Variants and Modification of Penetrance of BRCA2-Associated Breast Cancer
Gaudet, M. M., Kirchhoff, T., Green, T. J., Vijai, J., Korn, J. M., Guiducci, C., Segrè, A. V., McGee, K., McGuffog, L., Kartsonaki, C., et al. (2010) · PLoS Genetics · doi:10.1371/annotation/b28cf02d-7196-4a16-8b36-6562a0b84f75 · Cited by 20
Wang, L., Považay, B., Chen, Y. P., Höfer, B., Drexler, W., & Guggenheim, J. A. (2011) · Experimental Eye Research · doi:10.1016/j.exer.2011.06.008 · Cited by 19
Identification of QTL on Chromosome 18 Associated with Non-Coagulating Milk in Swedish Red Cows
Duchemin, S. I., Glantz, M., de Koning, D., Paulsson, M. A., & Fikse, W. F. (2016) · Frontiers in Genetics · doi:10.3389/fgene.2016.00057 · Cited by 19
“Quality controls of the data were performed using the R-package GenAbel (Aulchenko et al., 2007), and consisted of a minimum of 95% of non-missing SNP per called genotypes (call rate) andminor allele frequency (MAF) of a minimum of 1% for a called SNP.”
MethodGenome‐wide association study for plasma very low‐density lipoprotein concentration in chicken
Zhang, H., Shen, L., Li, Y., Xu, Z., Zhang, X., Yu, J., Cao, Z., & Luan, P. (2019) · Journal of Animal Breeding and Genetics · doi:10.1111/jbg.12397 · Cited by 19
Genomic Analysis of Spontaneous Abortion in Holstein Heifers and Primiparous Cows
Oliver, K. F., Wahl, A., Dick, M., Toenges, J., Kiser, J. N., Galliou, J. M., Moraes, J. G. N., Burns, G. W., Dalton, J. C., Spencer, T. E., et al. (2019) · Genes · doi:10.3390/genes10120954 · Cited by 19
“The permuted P-value was calculated using GenABEL in R with 10,000 phenotype-based permutations for each gene-set [32].”
MethodZhu, X., Leiser, W. L., Hahn, V., & Würschum, T. (2020) · The Crop Journal · doi:10.1016/j.cj.2020.06.006 · Cited by 19
Murgiano, L., Becker, D., Spector, C., Carlin, K., Santana, E., Niggel, J. K., Jagannathan, V., Leeb, T., Pearce-Kelling, S., Aguirre, G., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-77980-5 · Cited by 16
da Cruz, A. S., Silva, D. C., Minasi, L. B., Teixeira, L. K. D. F., Rodrigues, F. M., da Silva, C. C., do Carmo, A. S., da Silva, M. V. G. B., Utsunomiya, Y. T., Garcia, J. F., et al. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2020.573344 · Cited by 19
Zemach, I., Alseekh, S., Tadmor‐Levi, R., Fisher, J., Torgeman, S., Trigerman, S., Nauen, J., Hayut, S. F., Mann, V., Rochsar, E., et al. (2023) · The Plant Journal · doi:10.1111/tpj.16268 · Cited by 19
McAuley, J. B., Servin, B., Burnett, H. A., Brekke, C., Peters, L., Hagen, I. J., Niskanen, A. K., Ringsby, T. H., Husby, A., Jensen, H., et al. (2024) · Molecular Biology and Evolution · doi:10.1093/molbev/msae179 · Cited by 19
Mangino, M., Cecelja, M., Menni, C., Tsai, P.-C., Yuan, W., Small, K. S., Bell, J. T., Mitchell, G. F., Chowienczyk, P., & Spector, T. D. (2015) · Journal of Hypertension · doi:10.1097/hjh.0000000000000732 · Cited by 19
“As per the discovery, the validation analysis was performed using GenABEL [19] to correct for family structure and zygosity on the residuals of the methylation probes adjusted for age and sex, and know sources of batch effect (methylation chip, sample position on methylation chip and blood cell count).”
MethodInfluentialLiu, F., Struchalin, M. V., van Duijn, K., Albert Hofman, D., Uitterlinden, A. G., van Duijn, C. M., Aulchenko, Y. S., & Kayser, M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028145 · Cited by 22
“GWA analysis The GWA analysis was conducted using GenABEL [35] and followed closely the methods previously described [34].”
InfluentialSelf-citationSNPpy - Database Management for SNP Data from Genome Wide Association Studies
Mitha, F., Herodotou, H., Borisov, N., Chen, J., Yoder, J., & Owzar, K. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024982 · Cited by 19
“For example, PLINK [1] and GenABEL [2] verify that for each SNP the same number of patients have been called and that the SNPs are bi-allelic.”
MethodGenetic Variation in Candidate Genes Like the HMGA2 Gene in the Extremely Tall
Hendriks, E., Brown, M. R., Boot, A. M., Oostra, B. A., Drop, S. L. S., & Parks, J. S. (2011) · Hormone Research in Paediatrics · doi:10.1159/000330764 · Cited by 19
Unravelling the basis of variability in cobalamin levels in the general population
Andrew, T., Gill, R., Gillham‐Nasenya, I., & Ahmadi, K. R. (2013) · British Journal Of Nutrition · doi:10.1017/s0007114513000974 · Cited by 19
“Tests of the genetic association between Cbl levels and each SNP were conducted using GenABEL implemented within the statistical package R((17)).”
MethodEnroth, S., Enroth, S. B., Johansson, Å., & Gyllensten, U. B. (2015) · Biomarkers · doi:10.3109/1354750x.2015.1093546 · Cited by 19
“, 2014) using the GenABEL or ProbABEL (Aulchenko et al., 2007) software suites, which have been developed to enable statistical analyses of genetic data of related individuals.”
MethodInfluentialGenomic analysis of morphometric traits in bighorn sheep using the Ovine Infinium ® HD SNP BeadChip
Miller, J. M., Festa‐Bianchet, M., & Coltman, D. W. (2018) · PeerJ · doi:10.7717/peerj.4364 · Cited by 19
“, 2016) an extension of the GenABLE package (Aulchenko et al., 2007; Karssen, Van Duijn & Aulchenko, 2016).”
BackgroundMethodInfluentialShadrina, A. S., Tsepilov, Y. A., Smetanina, M. A., Voronina, E. N., Seliverstov, E. I., Ilyukhin, Е. А., Кириенко, А. И., Zolotukhin, I. A., & Филипенко, М. Л. (2018) · Clinical Genetics · doi:10.1111/cge.13362 · Cited by 19
“org; glm function).(6) Adherence of genotype distribution to Hardy-Weinberg equi-”
MethodArmstrong, N. D., Chen, W., Brewer, M. S., Williams, S. R., Sale, M. M., Worrall, B. B., & Keene, K. L. (2018) · Frontiers in Genetics · doi:10.3389/fgene.2018.00358 · Cited by 19
“Manhattan plots were generated using qqman (Turner, 2018) and lambda values were estimated using GenABEL (Aulchenko et al., 2007).”
MethodBordbar, F., Jensen, J., Du, ., Abied, A., Guo, W., Xu, L., Gao, H., Zhang, L., & Li, J. (2020) · Cell Proliferation · doi:10.1111/cpr.12870 · Cited by 18
Moraleda, C. P., Robledo, D., Gutiérrez, A. P., Del‐Pozo, J., Yañez, J. M., & Houston, R. D. (2021) · BMC Genomics · doi:10.1186/s12864-021-07443-2 · Cited by 19
A combined GWAS approach reveals key loci for socially-affected traits in Yorkshire pigs
Wu, P., Wang, K., Zhou, J., Chen, D., Jiang, A., Jiang, Y., Zhu, L., Qiu, X., Li, X., & Tang, G. (2021) · Communications Biology · doi:10.1038/s42003-021-02416-3 · Cited by 20
Peters, L., Huisman, J., Kruuk, L. E. B., Pemberton, J. M., & Johnston, S. E. (2021) · Molecular Ecology · doi:10.1111/mec.16314 · Cited by 18
“4.2 (Aulchenko et al., 2007).”
InfluentialGenomic study of the response of chicken to highly pathogenic avian influenza virus
Sironi, L., Williams, J. L., Stella, A., Minozzi, G., Moreno, A. M., Ramelli, P., Han, J., Weigend, S., Junxing, W., Lombardi, G., et al. (2011) · BMC Proceedings · doi:10.1186/1753-6561-5-s4-s25 · Cited by 19
Li, J., Eriksson, L., Humphreys, K., Czene, K., Liu, J., Tamimi, R. M., Lindström, S., Hunter, D. J., Vachon, C. M., Couch, F. J., et al. (2010) · Breast Cancer Research · doi:10.1186/bcr2488 · Cited by 19
“For the analysis of imputed data, the ProbABEL package from the ABEL set of programs was used [29].”
Method
Metadata
- Authors
- Aulchenko, Y. S., Ripke, S., Isaacs, A., & van Duijn, C. M.
- Affiliations
- Erasmus MC (NL)
- 1 Department of Epidemiology and Biostatistics, Erasmus MC Rotterdam, Postbus 2040, 3000 CA Rotterdam, The Netherlands and 2Statistical Genetics Group, Max-Planck-Institute of Psychiatry, Kraepelinstr. 10, D-80804 Munich, Germany
- Corresponding author
- Aulchenko, Yurii S.
- Venue
- Bioinformatics
- Publisher
- Oxford University Press (OUP)
- Published
- 2007-03-23
- Volume
- 23
- Issue
- 10
- Pages
- 1294-1296
- ISSN
- 1367-4803 (ISSN-L)
- 1367-4811
- OpenAlex
- W2161245845
- Cited by
- 1,836
- References
- 4
- Citations by year
- 2026: 22 · 2025: 39 · 2024: 91 · 2023: 72 · 2022: 65 · 2021: 129 · 2020: 113 · 2019: 161 · 2018: 178 · 2017: 153 · 2016: 139 · 2015: 143 · 2014: 140 · 2013: 116 · 2012: 89
- FWCI
- 19.99
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Bioinformatics (publishedVersion)
- PubMed (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Mapping and Diversity in Plants and Animals
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and phenotypic traits in livestock
- Keywords
- genome-wide association study, R library, single nucleotide polymorphisms, association testing, binary traits, quantitative traits, statistical software
- MeSH terms
- Computer Simulation, Haplotypes, Humans, Software, Gene Library, Genome, Human, Information Storage and Retrieval, Genome, Computational Biology, Oligonucleotide Array Sequence Analysis, Polymorphism, Single Nucleotide
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