Bioinformatics Advance Access originally published online on August 5, 2004
Bioinformatics 2005 21(2):263-265; doi:10.1093/bioinformatics/bth457
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Bioinformatics vol. 21 issue 2 © Oxford University Press 2005; all rights reserved.
Haploview: analysis and visualization of LD and haplotype maps
1 Whitehead Institute for Biomedical Research Cambridge, MA 02142, USA
2 MIT Media Lab Cambridge, MA 02139, USA
3 Broad Institute of Harvard and MIT Cambridge, MA, USA
*To whom correspondence should be addressed.
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Abstract |
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 TOP Abstract INTRODUCTIONFEATURESIMPLEMENTATIONREFERENCES |
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Summary: Research over the last few years has revealed significant haplotype structure in the human genome. The characterization of these patterns, particularly in the context of medical genetic association studies, is becoming a routine research activity. Haploview is a software package that provides computation of linkage disequilibrium statistics and population haplotype patterns from primary genotype data in a visually appealing and interactive interface.
Availability: http://www.broad.mit.edu/mpg/haploview/
Contact: jcbarret{at}broad.mit.edu
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INTRODUCTION |
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Knowledge of local linkage disequilibrium (LD) and common haplotype patterns in disease association and positional cloning studies is becoming increasingly widespread since it has become clear (Van Eerdewegh et al., 2002; Rioux et al., 2001; Geesaman et al., 2003; Stoll et al., 2004) that intelligent use of this information has the potential to make them much more comprehensive and efficient. Early studies identifying unexpected extent of correlation and structure in haplotype patterns (Reich et al., 2001; Daly et al., 2001; Gabriel et al., 2002) have led to the initiation of the Human Haplotype Map project (HapMap) to make this information available to all medical genetics researchers (International HapMap Consortium, 2003). Given the dramatic increase in the size and number of disease association studies worldwide and the enormous amount of public genotype data from HapMap, tools for analyzing, interpreting and visualizing these data are of critical importance to researchers everywhere.
Haploview is designed to provide a comprehensive suite of tools for haplotype analysis for a wide variety of dataset sizes. Haploview generates marker quality statistics, LD information, haplotype blocks, population haplotype frequencies and single marker association statistics in a user-friendly format. All the features are customizable and all computations performed in real time, even for datasets with hundreds of individuals and hundreds of markers.
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FEATURES |
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TOPAbstractINTRODUCTIONFEATURESIMPLEMENTATIONREFERENCES |
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Haploview accepts input in a variety of formats. Pedigree data can be loaded as either partially or fully phased chromosomes or as unphased diplotypes in the standard Linkage format. The latter format also allows the user to specify family structure information as well as disease affection or case/control status. Marker information, including name and location is loaded separately. Haploview also directly accepts genotype data dumped from the Human HapMap website (http://www.hapmap.org). A graphical genome browser maintained at that site allows researchers to navigate to a particular region of the genome and dump HapMap genotype data for all genotyped markers in the selected region in a format accepted by Haploview.
Upon loading a dataset, the software presents to the user a series of marker genotyping quality metrics. These include a check for conformance with Hardy–Weinberg equilibrium, a tally of Mendelian inheritance errors and the percentage of individuals successfully genotyped for that marker. The program filters out markers which fall below a preset threshold for these tests. The user can adjust these thresholds as well as handpick markers to add or remove from the subsequent steps. At any time later in the process, the user may return to this quality control panel, add or remove additional markers, and have the changes immediately reflected in the ongoing analyses.
Haploview calculates several pairwise measures of LD, which it uses to create a graphical representation (Fig. 1). The user has the option to select one of several commonly used block definitions (Gabriel et al., 2002; Wang et al., 2002) to partition the region into segments of strong LD. Alternatively, the user may manually select groups of markers for subsequent haplotype analysis. This view also allows a number of different color schemes to represent the LD relationships. Further, the program allows the display of an ‘analysis track’ above the LD plot, to display continuous variables such as recombination rate estimates (McVean et al., 2004) (Fig. 1).
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Once groups of markers are selected (either automatically or manually), the program generates haplotypes and their population frequencies (Fig. 1). This display shows lines to indicate transitions from one block to the next with frequency corresponding to the thickness of the line and also presents Hedrick's multiallelic D', which represents the degree of LD between two blocks, treating each haplotype within a block as an ‘allele’ of that region. Again, customization is available for nearly all aspects of the display, including displaying alleles as letters, numbers or colored boxes and displaying only those haplotypes above an adjustable threshold in the population.
If affection status is included in the input file, Haploview also calculates the standard TDT statistic (for trio data) or simple 
2 (for case/control data) for each marker that can be used for association studies. Future versions will include several haplotype-tag SNP selection methods as well as haplotype-based association testing and evaluation of significance using permutation testing. These final features allow the user to go from raw genotype data through exploring genetic associations in one easy to use software package. Haploview is maintained as an open source project (http://sourceforge.net/projects/haploview/), which allows external parties to add their own methods in addition to the continuing development by the authors.
Each of these views of the data is shown on a separate tab (Fig. 1), allowing the user to move from one to the next, with interactive modifications made by the user in any panel reflected in all the others. For example, one can return at any time to the review of marker quality and manually include or exclude individual markers—these changes are instantly reflected in the LD and haplotype panels. This provides the ability to analyze the data in real-time. The information on each panel is also able to be exported to a PNG for use in presentations or publications or dumped to a text file. Additionally, the program has a fully functional command-line mode, which allows users to run all the analyses without opening the GUI on one or more files at once.
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IMPLEMENTATION |
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Haploview is written entirely in Java, which means it is usable on any platform with Java 1.3 or later installed. Running on a 1.8 GHz Pentium 4 with 1 GB of RAM, Haploview can display a dataset with 200 markers genotyped in 400 individuals and adjust parameters with no noticeable delay. The program is also able to be used (from the command line) to do the LD calculations on very large datasets in comparatively small amounts of time. Haploview was able to compute 3.3 million pairwise LD values (comparisons of all markers closer than 500 KB in a 45 500 marker dataset) in 30 min.
Haploview uses a two marker EM (ignoring missing data) to estimate the maximum-likelihood values of the four gamete frequencies, from which the D', LOD and r 2 calculations derive. Haplotype phase and population frequency are inferred using a standard EM algorithm with a partition–ligation approach for blocks with greater than 10 markers. Conformance with Hardy–Weinberg equilibrium is computed using an exact test (G.Abecasis and J.Wigginton, personal communication).
Received on June 23, 2004; revised on July 23, 2004; accepted on July 23, 2004
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REFERENCES |
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TOPAbstractINTRODUCTIONFEATURESIMPLEMENTATIONREFERENCES |
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Daly, M.J., Rioux, J.D., Schaffner, S.F., Hudson, T.J., Lander, E.S. (2001) High-resolution haplotype structure in the human genome. Nat. Genet., 29, 229–232[CrossRef][Web of Science][Medline].
Gabriel, S.B., Schaffner, S.F., Nguyen, H., Moore, J.M., Roy, J., Blumenstiel, B., Higgins, J., Defelice, M., Lochner, A., Faggart, M., et al. (2002) The structure of haplotype blocks in the human genome. Science, 296, 2225–2229
Geesaman, B.J., Benson, E., Brewster, S.J., Kunkel, L.M., Blanche, H., Thomas, G., Perls, T.T., Daly, M.J., Puca, A.A. (2003) Haplotype-based identification of a microsomal transfer protein marker associated with the human lifespan. Proc. Natl Acad. Sci., USA, 100, 14115–20
The International HapMap Consortium. (2003) The International HapMap Project. Nature, 18, 789–796.
McVean, G.A., Myers, S.R., Hunt, S., Deloukas, P., Bentley, D.R., Donnelly, P. (2004) The fine-scale structure of recombination rate variation in the human genome. Science, 304, 581–584
Reich, D.E., Cargill, M., Bolk, S., Ireland, J., Sabeti, P.C., Richter, D.J., Lavery, T., Kouyoumjian, R., Farhadian, S.F., Ward, R., Lander, E.S. (2001) Linkage disequilibrium in the human genome. Nature, 411, 199–204[CrossRef][Medline].
Rioux, J.D., Daly, M.J., Silverberg, M.S., Lindblad, K., Steinhart, H., Cohen, Z., Delmonte, T., Kocher, K., Miller, K., Guschwan, S., et al. (2001) Genetic variation in the 5q31 cytokine gene cluster confers susceptibility to Crohn disease. Nat. Genet., 29, 223–228[CrossRef][Web of Science][Medline].
Stoll, M., Corneliussen, B., Costello, C.M., Waetzig, G.H., Mellgard, B., Kroch, W.A., Rosenstiel, P., Albrecht, M., Croucher, P.J., Seegert, D., et al. (2004) Genetic variation in DLG5 is associated with inflammatory bowel disease. Nat. Genet., 36, 476–480[CrossRef][Web of Science][Medline].
Van Eerdewegh, P., Little, R.D., Dupuis, J., Del Mastro, R.G., Falls, K., Simon, J., Jorrey, D., Pandit, S., McKenny, J., Braunschweiger, K., et al. (2002) Association of the ADAM33 gene with asthma and bronchial hyperresponsiveness. Nature, 418, 426–430[CrossRef][Medline].
Wang, N., Akey, J.M., Zhang, K., Chakraborty, R., Jin, L. (2002) Distribution of recombination crossovers and the origin of haplotype blocks: the interplay of population history, recombination, and mutation. Am. J. Hum. Genet., 71, 1227–1234[CrossRef][Web of Science][Medline].
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R. Zarbock, D. Hendig, C. Szliska, K. Kleesiek, and C. Gotting Vascular endothelial growth factor gene polymorphisms as prognostic markers for ocular manifestations in pseudoxanthoma elasticum Hum. Mol. Genet., September 1, 2009; 18(17): 3344 - 3351. [Abstract] [Full Text] [PDF]
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P.-H. Liu, Y.-C. Chang, Y.-D. Jiang, W. J. Chen, T.-J. Chang, S.-S. Kuo, K.-C. Lee, P.-C. Hsiao, K. C. Chiu, and L.-M. Chuang Genetic Variants of TCF7L2 Are Associated with Insulin Resistance and Related Metabolic Phenotypes in Taiwanese Adolescents and Caucasian Young Adults J. Clin. Endocrinol. Metab., September 1, 2009; 94(9): 3575 - 3582. [Abstract] [Full Text] [PDF]
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H. Yang, Y. Zhou, Z. Zhou, J. Liu, X. Yuan, K. Matsuo, T. Takezaki, K. Tajima, and J. Cao A Novel Polymorphism rs1329149 of CYP2E1 and a Known Polymorphism rs671 of ALDH2 of Alcohol Metabolizing Enzymes Are Associated with Colorectal Cancer in a Southwestern Chinese Population Cancer Epidemiol. Biomarkers Prev., September 1, 2009; 18(9): 2522 - 2527. [Abstract] [Full Text] [PDF]
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S. SOLOVIEVA, O.-P. KAMARAINEN, A. HIRVONEN, S. HAMALAINEN, M. LAITALA, T. VEHMAS, K. LUOMA, A. NAKKI, H. RIIHIMAKI, L. ALA-KOKKO, et al. Association Between Interleukin 1 Gene Cluster Polymorphisms and Bilateral Distal Interphalangeal Osteoarthritis J Rheumatol, September 1, 2009; 36(9): 1977 - 1986. [Abstract] [Full Text] [PDF]
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Z. Lei, R.-Y. Liu, J. Zhao, Z. Liu, X. Jiang, W. You, X.-F. Chen, X. Liu, K. Zhang, B. Pasche, et al. TGFBR1 Haplotypes and Risk of Non-Small-Cell Lung Cancer Cancer Res., September 1, 2009; 69(17): 7046 - 7052. [Abstract] [Full Text] [PDF]
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N. L. Saccone, J. C. Wang, N. Breslau, E. O. Johnson, D. Hatsukami, S. F. Saccone, R. A. Grucza, L. Sun, W. Duan, J. Budde, et al. The CHRNA5-CHRNA3-CHRNB4 Nicotinic Receptor Subunit Gene Cluster Affects Risk for Nicotine Dependence in African-Americans and in European-Americans Cancer Res., September 1, 2009; 69(17): 6848 - 6856. [Abstract] [Full Text] [PDF]
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M Rossol, M Pierer, S Arnold, G Keysser, H Burkhardt, C Baerwald, and U Wagner Homozygosity for DNASE2 single nucleotide polymorphisms in the 5'-regulatory region is associated with rheumatoid arthritis Ann Rheum Dis, September 1, 2009; 68(9): 1498 - 1503. [Abstract] [Full Text] [PDF]
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M. Sikora, A. Ferrer-Admetlla, H. Laayouni, C. Menendez, A. Mayor, A. Bardaji, B. Sigauque, I. Mandomando, P. L. Alonso, J. Bertranpetit, et al. A variant in the gene FUT9 is associated with susceptibility to placental malaria infection Hum. Mol. Genet., August 15, 2009; 18(16): 3136 - 3144. [Abstract] [Full Text] [PDF]
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A. Malarstig, A. Buil, J. C. Souto, R. Clarke, F. Blanco-Vaca, J. Fontcuberta, J. Peden, M. Andersen, A. Silveira, S. Barlera, et al. Identification of ZNF366 and PTPRD as novel determinants of plasma homocysteine in a family-based genome-wide association study Blood, August 13, 2009; 114(7): 1417 - 1422. [Abstract] [Full Text] [PDF]
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A. Sabbagh, E. Pasmant, I. Laurendeau, B. Parfait, S. Barbarot, B. Guillot, P. Combemale, S. Ferkal, M. Vidaud, P. Aubourg, et al. Unravelling the genetic basis of variable clinical expression in neurofibromatosis 1 Hum. Mol. Genet., August 1, 2009; 18(15): 2768 - 2778. [Abstract] [Full Text] [PDF]
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N. Niu, V. Manickam, K. R. Kalari, I. Moon, L. L. Pelleymounter, B. W. Eckloff, E. D. Wieben, D. J. Schaid, and L. Wang Human Glucocorticoid Receptor {alpha} Gene (NR3C1) Pharmacogenomics: Gene Resequencing and Functional Genomics J. Clin. Endocrinol. Metab., August 1, 2009; 94(8): 3072 - 3084. [Abstract] [Full Text] [PDF]
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Y.-C. Cheng, W.-H. L. Kao, B. D. Mitchell, J. R. O'Connell, H. Shen, P. F. McArdle, Q. Gibson, K. A. Ryan, A. R. Shuldiner, and T. I. Pollin Genome-Wide Association Scan Identifies Variants near Matrix Metalloproteinase (MMP) Genes on Chromosome 11q21-22 Strongly Associated With Serum MMP-1 Levels Circ Cardiovasc Genet, August 1, 2009; 2(4): 329 - 337. [Abstract] [Full Text] [PDF]
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H. Ding, Y. Xu, X. Wang, Q. Wang, L. Zhang, Y. Tu, J. Yan, W. Wang, R. Hui, C.-Y. Wang, et al. 9p21 is a Shared Susceptibility Locus Strongly for Coronary Artery Disease and Weakly for Ischemic Stroke in Chinese Han Population Circ Cardiovasc Genet, August 1, 2009; 2(4): 338 - 346. [Abstract] [Full Text] [PDF]
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B Asling, J Jirholt, P Hammond, M Knutsson, A Walentinsson, G Davidson, L Agreus, A Lehmann, and M Lagerstrom-Fermer Collagen type III alpha I is a gastro-oesophageal reflux disease susceptibility gene and a male risk factor for hiatus hernia Gut, August 1, 2009; 58(8): 1063 - 1069. [Abstract] [Full Text] [PDF]
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A M Muise, T D Walters, W K Glowacka, A M Griffiths, B-Y Ngan, H Lan, W Xu, M S Silverberg, and D Rotin Polymorphisms in E-cadherin (CDH1) result in a mis-localised cytoplasmic protein that is associated with Crohn's disease Gut, August 1, 2009; 58(8): 1121 - 1127. [Abstract] [Full Text] [PDF]
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A. HELLQUIST, T. M. JARVINEN, S. KOSKENMIES, M. ZUCCHELLI, C. ORSMARK-PIETRAS, L. BERGLIND, J. PANELIUS, T. HASAN, H. JULKUNEN, M. D'AMATO, et al. Evidence for Genetic Association and Interaction Between the TYK2 and IRF5 Genes in Systemic Lupus Erythematosus J Rheumatol, August 1, 2009; 36(8): 1631 - 1638. [Abstract] [Full Text] [PDF]
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R. DIEGUEZ-GONZALEZ, S. AKAR, M. CALAZA, I. GONZALEZ-ALVARO, B. FERNANDEZ-GUTIERREZ, J. R. LAMAS, A. R. de la SERNA, R. CALIZ, F. J. BLANCO, D. PASCUAL-SALCEDO, et al. Lack of Association with Rheumatoid Arthritis of Selected Polymorphisms in 4 Candidate Genes: CFH, CD209, Eotaxin-3, and MHC2TA J Rheumatol, August 1, 2009; 36(8): 1590 - 1595. [Abstract] [Full Text] [PDF]
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X.-j. Zhou, J.-c. LV, L. Yu, Z. Cui, J. Zhao, R. Yang, J. Han, P. Hou, M.-h. Zhao, and H. Zhang FCGR2B gene polymorphism rather than FCGR2A, FCGR3A and FCGR3B is associated with anti-GBM disease in Chinese Nephrol. Dial. Transplant., July 29, 2009; (2009) gfp374v1. [Abstract] [Full Text] [PDF]
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G. Orozco, A. Hinks, S. Eyre, X. Ke, L. J. Gibbons, J. Bowes, E. Flynn, P. Martin, Wellcome Trust Case Control Consortium, YEAR consortium, et al. Combined effects of three independent SNPs greatly increase the risk estimate for RA at 6q23 Hum. Mol. Genet., July 15, 2009; 18(14): 2693 - 2699. [Abstract] [Full Text] [PDF]
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A. -M. Wills, S. Cronin, A. Slowik, D. Kasperaviciute, M. A. Van Es, J. M. Morahan, P. N. Valdmanis, V. Meininger, J. Melki, C. E. Shaw, et al. A large-scale international meta-analysis of paraoxonase gene polymorphisms in sporadic ALS Neurology, July 7, 2009; 73(1): 16 - 24. [Abstract] [Full Text] [PDF]
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N. N. Hansel, L. Gao, N. M. Rafaels, R. A. Mathias, E. R. Neptune, C. Tankersley, A. V. Grant, J. Connett, T. H. Beaty, R. A. Wise, et al. Leptin receptor polymorphisms and lung function decline in COPD Eur. Respir. J., July 1, 2009; 34(1): 103 - 110. [Abstract] [Full Text] [PDF]
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X. Yang, S.-H. Liang, D. M. Weyant, P. Lazarus, C. J. Gallagher, and C. J. Omiecinski The Expression of Human Microsomal Epoxide Hydrolase Is Predominantly Driven by a Genetically Polymorphic Far Upstream Promoter J. Pharmacol. Exp. Ther., July 1, 2009; 330(1): 23 - 30. [Abstract] [Full Text] [PDF]
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G. Wang, K. L. Spencer, B. L. Court, L. M. Olson, W. K. Scott, J. L. Haines, and M. A. Pericak-Vance Localization of Age-Related Macular Degeneration-Associated ARMS2 in Cytosol, Not Mitochondria Invest. Ophthalmol. Vis. Sci., July 1, 2009; 50(7): 3084 - 3090. [Abstract] [Full Text] [PDF]
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A. Biyasheva, R. S. Legro, A. Dunaif, and M. Urbanek Evidence for Association between Polycystic Ovary Syndrome (PCOS) and TCF7L2 and Glucose Intolerance in Women with PCOS and TCF7L2 J. Clin. Endocrinol. Metab., July 1, 2009; 94(7): 2617 - 2625. [Abstract] [Full Text] [PDF]
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M. Urbanek, G. Nampiaparampil, J. D'Souza, E. Sefton, C. Ackerman, R. S. Legro, and A. Dunaif The Role of Genetic Variation in the Lamin A/C Gene in the Etiology of Polycystic Ovary Syndrome J. Clin. Endocrinol. Metab., July 1, 2009; 94(7): 2665 - 2669. [Abstract] [Full Text] [PDF]
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H.-L. Xu, W.-H. Xu, Q. Cai, M. Feng, J. Long, W. Zheng, Y.-B. Xiang, and X.-O. Shu Polymorphisms and Haplotypes in the Caspase-3, Caspase-7, and Caspase-8 Genes and Risk for Endometrial Cancer: A Population-Based, Case-Control Study in a Chinese Population Cancer Epidemiol. Biomarkers Prev., July 1, 2009; 18(7): 2114 - 2122. [Abstract] [Full Text] [PDF]
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L. Lu, J. Sun, S. D. Isaacs, K. E. Wiley, S. Smith, K. Pruett, Y. Zhu, Z. Zhang, F. Wiklund, H. Gronberg, et al. Fine-Mapping and Family-Based Association Analyses of Prostate Cancer Risk Variants at Xp11 Cancer Epidemiol. Biomarkers Prev., July 1, 2009; 18(7): 2132 - 2136. [Abstract] [Full Text] [PDF]
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R. A. Mason, E. V. Morlock, M. R. Karagas, K. T. Kelsey, C. J. Marsit, A. R. Schned, and A. S. Andrew EGFR pathway polymorphisms and bladder cancer susceptibility and prognosis Carcinogenesis, July 1, 2009; 30(7): 1155 - 1160. [Abstract] [Full Text] [PDF]
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E. Org, S. Eyheramendy, P. Juhanson, C. Gieger, P. Lichtner, N. Klopp, G. Veldre, A. Doring, M. Viigimaa, S. Sober, et al. Genome-wide scan identifies CDH13 as a novel susceptibility locus contributing to blood pressure determination in two European populations Hum. Mol. Genet., June 15, 2009; 18(12): 2288 - 2296. [Abstract] [Full Text] [PDF]
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S. L. Zheng, V. L. Stevens, F. Wiklund, S. D. Isaacs, J. Sun, S. Smith, K. Pruett, K. E. Wiley, S.-T. Kim, Y. Zhu, et al. Two Independent Prostate Cancer Risk-Associated Loci at 11q13 Cancer Epidemiol. Biomarkers Prev., June 1, 2009; 18(6): 1815 - 1820. [Abstract] [Full Text] [PDF]
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