Home LiteratureArticle Details
PMID: 21769936 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Comparison of statistical tests for disease association with rare variants.

Genetic epidemiology ·Vol. 35 ·No. 7 ·2011-11-00 ·Pages 606-19

Basu S, Pan W

Abstract

In anticipation of the availability of next-generation sequencing data, there is increasing interest in investigating association between complex traits and rare variants (RVs). In contrast to association studies for common variants (CVs), due to the low frequencies of RVs, common wisdom suggests that existing statistical tests for CVs might not work, motivating the recent development of several new tests for analyzing RVs, most of which are based on the idea of pooling/collapsing RVs. However, there is a lack of evaluations of, and thus guidance on the use of, existing tests. Here we provide a comprehensive comparison of various statistical tests using simulated data. We consider both independent and correlated rare mutations, and representative tests for both CVs and RVs. As expected, if there are no or few non-causal (i.e. neutral or non-associated) RVs in a locus of interest while the effects of causal RVs on the trait are all (or mostly) in the same direction (i.e. either protective or deleterious, but not both), then the simple pooled association tests (without selecting RVs and their association directions) and a new test called kernel-based adaptive clustering (KBAC) perform similarly and are most powerful; KBAC is more robust than simple pooled association tests in the presence of non-causal RVs; however, as the number of non-causal CVs increases and/or in the presence of opposite association directions, the winners are two methods originally proposed for CVs and a new test called C-alpha test proposed for RVs, each of which can be regarded as testing on a variance component in a random-effects model. Interestingly, several methods based on sequential model selection (i.e. selecting causal RVs and their association directions), including two new methods proposed here, perform robustly and often have statistical power between those of the above two classes.

MeSH Terms
Data Interpretation, Statistical Genetic Predisposition to Disease/genetics Genetic Variation Humans Models, Genetic Models, Statistical Regression Analysis
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Basu Saonli
Division of Biostatistics, School of Public Health, University of Minnesota, Minneapolis, Minnesota 55455-0392, USA.
Pan Wei
References (51)
51 references, click to expand
  1. A likelihood-based trait-model-free approach for linkage detection of binary trait.
    Biometrics. 2010 Mar;66(1):205-13 PMID: 19459835
  2. Pooled association tests for rare variants in exon-resequencing studies.
    Am J Hum Genet. 2010 Jun 11;86(6):832-8 PMID: 20471002
  3. Power comparisons between similarity-based multilocus association methods, logistic regression, and score tests for haplotypes.
    Genet Epidemiol. 2009 Apr;33(3):183-97 PMID: 18814307
  4. Rare independent mutations in renal salt handling genes contribute to blood pressure variation.
    Nat Genet. 2008 May;40(5):592-599 PMID: 18391953
  5. Generalized genomic distance-based regression methodology for multilocus association analysis.
    Am J Hum Genet. 2006 Nov;79(5):792-806 PMID: 17033957
  6. Rare variant association analysis methods for complex traits.
    Annu Rev Genet. 2010;44:293-308 PMID: 21047260
  7. Multiple rare nonsynonymous variants in the adenomatous polyposis coli gene predispose to colorectal adenomas.
    Cancer Res. 2008 Jan 15;68(2):358-63 PMID: 18199528
  8. A spectrum of PCSK9 alleles contributes to plasma levels of low-density lipoprotein cholesterol.
    Am J Hum Genet. 2006 Mar;78(3):410-22 PMID: 16465619
  9. Are rare variants responsible for susceptibility to complex diseases?
    Am J Hum Genet. 2001 Jul;69(1):124-37 PMID: 11404818
  10. Sequence analysis using logic regression.
    Genet Epidemiol. 2001;21 Suppl 1:S626-31 PMID: 11793751
  11. Genome-wide searching of rare genetic variants in WTCCC data.
    Hum Genet. 2010 Sep;128(3):269-80 PMID: 20549515
  12. Generalized T2 test for genome association studies.
    Am J Hum Genet. 2002 May;70(5):1257-68 PMID: 11923914
  13. Genome association studies of complex diseases by case-control designs.
    Am J Hum Genet. 2003 Apr;72(4):850-68 PMID: 12647259
  14. A covering method for detecting genetic associations between rare variants and common phenotypes.
    PLoS Comput Biol. 2010 Oct 14;6(10):e1000954 PMID: 20976246
  15. Methods for detecting associations with rare variants for common diseases: application to analysis of sequence data.
    Am J Hum Genet. 2008 Sep;83(3):311-21 PMID: 18691683
  16. Comprehensive approach to analyzing rare genetic variants.
    PLoS One. 2010 Nov 03;5(11):e13584 PMID: 21072163
  17. Common vs. rare allele hypotheses for complex diseases.
    Curr Opin Genet Dev. 2009 Jun;19(3):212-9 PMID: 19481926
  18. Genomic similarity and kernel methods I: advancements by building on mathematical and statistical foundations.
    Hum Hered. 2010;70(2):109-31 PMID: 20610906
  19. Detecting rare variants for complex traits using family and unrelated data.
    Genet Epidemiol. 2010 Feb;34(2):171-87 PMID: 19847924
  20. A powerful and flexible multilocus association test for quantitative traits.
    Am J Hum Genet. 2008 Feb;82(2):386-97 PMID: 18252219
  21. Sequencing the IL4 locus in African Americans implicates rare noncoding variants in asthma susceptibility.
    J Allergy Clin Immunol. 2009 Dec;124(6):1204-9.e9 PMID: 19910025
  22. A new testing strategy to identify rare variants with either risk or protective effect on disease.
    PLoS Genet. 2011 Feb 03;7(2):e1001289 PMID: 21304886
  23. Statistical analysis strategies for association studies involving rare variants.
    Nat Rev Genet. 2010 Nov;11(11):773-85 PMID: 20940738
  24. Shifting paradigm of association studies: value of rare single-nucleotide polymorphisms.
    Am J Hum Genet. 2008 Jan;82(1):100-12 PMID: 18179889
  25. The allelic architecture of human disease genes: common disease-common variant...or not?
    Hum Mol Genet. 2002 Oct 1;11(20):2417-23 PMID: 12351577
  26. A strategy to discover genes that carry multi-allelic or mono-allelic risk for common diseases: a cohort allelic sums test (CAST).
    Mutat Res. 2007 Feb 3;615(1-2):28-56 PMID: 17101154
  27. Adaptive tests for association analysis of rare variants.
    Genet Epidemiol. 2011 Jul;35(5):381-8 PMID: 21520272
  28. Estimation and testing for the effect of a genetic pathway on a disease outcome using logistic kernel machine regression via logistic mixed models.
    BMC Bioinformatics. 2008 Jun 24;9:292 PMID: 18577223
  29. A groupwise association test for rare mutations using a weighted sum statistic.
    PLoS Genet. 2009 Feb;5(2):e1000384 PMID: 19214210
  30. Common and rare variants in multifactorial susceptibility to common diseases.
    Nat Genet. 2008 Jun;40(6):695-701 PMID: 18509313
  31. Relationship between genomic distance-based regression and kernel machine regression for multi-marker association testing.
    Genet Epidemiol. 2011 May;35(4):211-6 PMID: 21308765
  32. Asymptotic tests of association with multiple SNPs in linkage disequilibrium.
    Genet Epidemiol. 2009 Sep;33(6):497-507 PMID: 19170135
  33. Testing for an unusual distribution of rare variants.
    PLoS Genet. 2011 Mar;7(3):e1001322 PMID: 21408211
  34. Powerful multi-marker association tests: unifying genomic distance-based regression and logistic regression.
    Genet Epidemiol. 2010 Nov;34(7):680-8 PMID: 20976795
  35. Genomic similarity and kernel methods II: methods for genomic information.
    Hum Hered. 2010;70(2):132-40 PMID: 20606458
  36. To identify associations with rare variants, just WHaIT: Weighted haplotype and imputation-based tests.
    Am J Hum Genet. 2010 Nov 12;87(5):728-35 PMID: 21055717
  37. An evaluation of statistical approaches to rare variant analysis in genetic association studies.
    Genet Epidemiol. 2010 Feb;34(2):188-93 PMID: 19810025
  38. Analysis of multiple SNPs in a candidate gene or region.
    Genet Epidemiol. 2008 Sep;32(6):560-6 PMID: 18428428
  39. Pair-wise multifactor dimensionality reduction method to detect gene-gene interactions in a case-control study.
    Hum Hered. 2010;69(1):60-70 PMID: 19797910
  40. A global test for groups of genes: testing association with a clinical outcome.
    Bioinformatics. 2004 Jan 1;20(1):93-9 PMID: 14693814
  41. A novel adaptive method for the analysis of next-generation sequencing data to detect complex trait associations with rare variants due to gene main effects and interactions.
    PLoS Genet. 2010 Oct 14;6(10):e1001156 PMID: 20976247
  42. Improved power by use of a weighted score test for linkage disequilibrium mapping.
    Am J Hum Genet. 2007 Feb;80(2):353-60 PMID: 17236140
  43. Efficient utilization of rare variants for detection of disease-related genomic regions.
    PLoS One. 2010 Dec 10;5(12):e14288 PMID: 21170328
  44. Personal genomes: The case of the missing heritability.
    Nature. 2008 Nov 6;456(7218):18-21 PMID: 18987709
  45. A data-adaptive sum test for disease association with multiple common or rare variants.
    Hum Hered. 2010;70(1):42-54 PMID: 20413981
  46. Bayesian analysis of rare variants in genetic association studies.
    Genet Epidemiol. 2011 Jan;35(1):57-69 PMID: 21181897
  47. So many correlated tests, so little time! Rapid adjustment of P values for multiple correlated tests.
    Am J Hum Genet. 2007 Dec;81(6):1158-68 PMID: 17966093
  48. Use of unphased multilocus genotype data in indirect association studies.
    Genet Epidemiol. 2004 Dec;27(4):415-28 PMID: 15481099
  49. Powerful SNP-set analysis for case-control genome-wide association studies.
    Am J Hum Genet. 2010 Jun 11;86(6):929-42 PMID: 20560208
  50. Accommodating linkage disequilibrium in genetic-association analyses via ridge regression.
    Am J Hum Genet. 2008 Feb;82(2):375-85 PMID: 18252218
  51. Association screening of common and rare genetic variants by penalized regression.
    Bioinformatics. 2010 Oct 1;26(19):2375-82 PMID: 20693321
Article Info
Journal
Genetic epidemiology
Abbr.
Genet Epidemiol
ISSN
1098-2272
Published
2011-11-00
Epub
2011-00-18
Pages
606-19
Language
English
Region
United States
NLM ID
8411723
PMCID
PMC3197766
Subset
IM
Grants
NHLBI NIH HHS · R01 HL105397-01 · United States
NHLBI NIH HHS · R01 HL105397 · United States
NIDDK NIH HHS · R21 DK089351 · United States
NHLBI NIH HHS · R01HL105397 · United States
NHLBI NIH HHS · R01HL65462 · United States
NHLBI NIH HHS · R01 HL065462-08 · United States
NIDDK NIH HHS · R21 DK089351-01 · United States
NHLBI NIH HHS · R01 HL065462 · United States
NIDDK NIH HHS · R21DK089351 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]