title: Effects of multiple genetic loci on age at onset in late-onset Alzheimer disease: a genome-wide association study.
abstract: OBJECTIVE
  Because APOE locus variants contribute to risk of late-onset Alzheimer disease (LOAD) and to differences in age at onset (AAO), it is important to know whether other established LOAD risk loci also affect AAO in affected participants.
  
  
  OBJECTIVE
  To investigate the effects of known Alzheimer disease risk loci in modifying AAO and to estimate their cumulative effect on AAO variation using data from genome-wide association studies in the Alzheimer Disease Genetics Consortium.
  
  
  METHODS
  The Alzheimer Disease Genetics Consortium comprises 14 case-control, prospective, and family-based data sets with data on 9162 participants of white race/ethnicity with Alzheimer disease occurring after age 60 years who also had complete AAO information, gathered between 1989 and 2011 at multiple sites by participating studies. Data on genotyped or imputed single-nucleotide polymorphisms most significantly associated with risk at 10 confirmed LOAD loci were examined in linear modeling of AAO, and individual data set results were combined using a random-effects, inverse variance-weighted meta-analysis approach to determine whether they contribute to variation in AAO. Aggregate effects of all risk loci on AAO were examined in a burden analysis using genotype scores weighted by risk effect sizes.
  
  
  METHODS
  Age at disease onset abstracted from medical records among participants with LOAD diagnosed per standard criteria.
  
  
  RESULTS
  Analysis confirmed the association of APOE with earlier AAO (P = 3.3 × 10(-96)), with associations in CR1 (rs6701713, P = 7.2 × 10(-4)), BIN1 (rs7561528, P = 4.8 × 10(-4)), and PICALM (rs561655, P = 2.2 × 10(-3)) reaching statistical significance (P < .005). Risk alleles individually reduced AAO by 3 to 6 months. Burden analyses demonstrated that APOE contributes to 3.7% of the variation in AAO (R(2) = 0.256) over baseline (R(2) = 0.221), whereas the other 9 loci together contribute to 2.2% of the variation (R(2) = 0.242).
  
  
  CONCLUSIONS
  We confirmed an association of APOE (OMIM 107741) variants with AAO among affected participants with LOAD and observed novel associations of CR1 (OMIM 120620), BIN1 (OMIM 601248), and PICALM (OMIM 603025) with AAO. In contrast to earlier hypothetical modeling, we show that the combined effects of Alzheimer disease risk variants on AAO are on the scale of, but do not exceed, the APOE effect. While the aggregate effects of risk loci on AAO may be significant, additional genetic contributions to AAO are individually likely to be small.
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authors.affiliation: Department of Neurology, University of California Irvine, Irvine.
authors.forename: Aimee
authors.initials: A
authors.lastname: Pierce
authors.affiliation: Institute for Memory Impairments and Neurological Disorders, University of California Irvine, Irvine.
authors.forename: Wayne W
authors.initials: WW
authors.lastname: Poon
authors.affiliation: USF Health Byrd Alzheimer's Institute, University of South Florida, Tampa.
authors.forename: Huntington
authors.initials: H
authors.lastname: Potter
authors.affiliation: Department of Neurology, Oregon Health & Science University, Portland.
authors.forename: Joseph F
authors.initials: JF
authors.lastname: Quinn
authors.affiliation: USF Health Byrd Alzheimer's Institute, University of South Florida, Tampa.
authors.forename: Ashok
authors.initials: A
authors.lastname: Raj
authors.affiliation: Department of Psychiatry and Behavioral Sciences, University of Washington School of Medicine, Seattle.
authors.forename: Murray
authors.initials: M
authors.lastname: Raskind
authors.affiliation: Department of Psychiatry, New York University, New York120Alzheimer's Disease Center, New York University, New York.
authors.forename: Barry
authors.initials: B
authors.lastname: Reisberg
authors.affiliation: Department of Neurology, University of California Los Angeles, Los Angeles.
authors.forename: John M
authors.initials: JM
authors.lastname: Ringman
authors.affiliation: Department of Neurology, University of Alabama at Birmingham, Birmingham.
authors.forename: Erik D
authors.initials: ED
authors.lastname: Roberson
authors.affiliation: Department of Neurology, University of California San Francisco, San Francisco.
authors.forename: Howard J
authors.initials: HJ
authors.lastname: Rosen
authors.affiliation: Department of Neurology, University of Texas Southwestern, Dallas.
authors.forename: Roger N
authors.initials: RN
authors.lastname: Rosenberg
authors.affiliation: Department of Psychiatry, Mount Sinai School of Medicine, New York, New York.
authors.forename: Mary
authors.initials: M
authors.lastname: Sano
authors.affiliation: Department of Neurology, University of Southern California, Los Angeles122Department of Psychiatry, University of Southern California, Los Angeles.
authors.forename: Lon S
authors.initials: LS
authors.lastname: Schneider
authors.affiliation: Department of Neurology, University of California San Francisco, San Francisco.
authors.forename: William W
authors.initials: WW
authors.lastname: Seeley
authors.affiliation: USF Health Byrd Alzheimer's Institute, University of South Florida, Tampa.
authors.forename: Amanda G
authors.initials: AG
authors.lastname: Smith
authors.affiliation: Department of Pathology, University of Washington, Seattle.
authors.forename: Joshua A
authors.initials: JA
authors.lastname: Sonnen
authors.affiliation: Department of Pathology and Laboratory Medicine, Indiana University, Indianapolis.
authors.forename: Salvatore
authors.initials: S
authors.lastname: Spina
authors.affiliation: Department of Neurology, Boston University, Boston, Massachusetts.
authors.forename: Robert A
authors.initials: RA
authors.lastname: Stern
authors.affiliation: Department of Neurology, Massachusetts General Hospital/Harvard Medical School, Boston.
authors.forename: Rudolph E
authors.initials: RE
authors.lastname: Tanzi
authors.affiliation: Vanderbilit Center for Human Genetics Research, Vanderbilt University, Nashville, Tennessee.
authors.forename: Tricia A
authors.initials: TA
authors.lastname: Thornton-Wells
authors.affiliation: Department of Pathology and Laboratory Medicine, University of Pennsylvania Perelman School of Medicine, Philadelphia.
authors.forename: John Q
authors.initials: JQ
authors.lastname: Trojanowski
authors.affiliation: Department of Pathology, Johns Hopkins University, Baltimore, Maryland.
authors.forename: Juan C
authors.initials: JC
authors.lastname: Troncoso
authors.affiliation: Department of Pathology and Laboratory Medicine, University of Pennsylvania Perelman School of Medicine, Philadelphia.
authors.forename: Otto
authors.initials: O
authors.lastname: Valladares
authors.affiliation: Department of Pathology and Laboratory Medicine, University of Pennsylvania Perelman School of Medicine, Philadelphia.
authors.forename: Vivianna M
authors.initials: VM
authors.lastname: Van Deerlin
authors.affiliation: Sanders-Brown Center on Aging, Department of Anatomy and Neurobiology, University of Kentucky, Lexington.
authors.forename: Linda J
authors.initials: LJ
authors.lastname: Van Eldik
authors.affiliation: Department of Neurology, Columbia University, New York, New York.
authors.forename: Badri N
authors.initials: BN
authors.lastname: Vardarajan
authors.affiliation: Department of Neurology, University of California Los Angeles, Los Angeles125Department of Pathology & Laboratory Medicine, University of California Los Angeles, Los Angeles.
authors.forename: Harry V
authors.initials: HV
authors.lastname: Vinters
authors.affiliation: Taub Institute on Alzheimer's Disease and the Aging Brain, Department of Pathology, Columbia University, New York, New York.
authors.forename: Jean Paul
authors.initials: JP
authors.lastname: Vonsattel
authors.affiliation: Cognitive Neurology and Alzheimer's Disease Center, Northwestern University, Chicago, Illinois127Department of Psychiatry, Northwestern University Feinberg School of Medicine, Chicago, Illinois.
authors.forename: Sandra
authors.initials: S
authors.lastname: Weintraub
authors.affiliation: Department of Medicine, Duke University, Durham, North Carolina128Department of Psychiatry & Behavioral Sciences, Duke University, Durham, North Carolina.
authors.forename: Kathleen A
authors.initials: KA
authors.lastname: Welsh-Bohmer
authors.affiliation: Taub Institute on Alzheimer's Disease and the Aging Brain, Department of Neurology, Columbia University, New York, New York.
authors.forename: Jennifer
authors.initials: J
authors.lastname: Williamson
authors.affiliation: John P. Hussman Institute for Human Genomics, University of Miami, Miami, Florida.
authors.forename: Sarah
authors.initials: S
authors.lastname: Wishnek
authors.affiliation: Department of Pathology, Oregon Health & Science University, Portland.
authors.forename: Randall L
authors.initials: RL
authors.lastname: Woltjer
authors.affiliation: Evelyn F. McKnight Brain Institute, Department of Neurology, Miller School of Medicine, University of Miami, Miami, Florida.
authors.forename: Clinton B
authors.initials: CB
authors.lastname: Wright
authors.affiliation: Department of Neuroscience, Mayo Clinic, Jacksonville, Florida.
authors.forename: Steven G
authors.initials: SG
authors.lastname: Younkin
authors.affiliation: Department of Medicine, University of Washington, Seattle.
authors.forename: Chang-En
authors.initials: CE
authors.lastname: Yu
authors.affiliation: Department of Neurological Sciences, Rush University Medical Center, Chicago, Illinois.
authors.forename: Lei
authors.initials: L
authors.lastname: Yu
mesh_terms: D000328:Adult; D017668:Age of Onset; D000368:Aged; D000369:Aged, 80 and over; D000544:Alzheimer Disease / Q000453:epidemiology / Q000235:genetics*; D005260:Female; D056426:Genetic Loci / Q000235:genetics*; D020022:Genetic Predisposition to Disease; D055106:Genome-Wide Association Study; D005838:Genotype; D006801:Humans; D008297:Male; D008875:Middle Aged; D020641:Polymorphism, Single Nucleotide / Q000235:genetics; D011446:Prospective Studies; D012307:Risk Factors