Margaret R Spitz

Baylor College of Medicine, Houston, Texas, United States

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Publications (542)3375.88 Total impact

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    ABSTRACT: Analyses of genome-wide association study (GWAS) data have revealed that detectable genetic mosaicism involving large (>2 Mb) structural autosomal alterations occurs in a fraction of individuals. We present results for a set of 24,849 genotyped individuals (total GWAS set II [TGSII]) in whom 341 large autosomal abnormalities were observed in 168 (0.68%) individuals. Merging data from the new TGSII set with data from two prior reports (the Gene-Environment Association Studies and the total GWAS set I) generated a large dataset of 127,179 individuals; we then conducted a meta-analysis to investigate the patterns of detectable autosomal mosaicism (n = 1,315 events in 925 [0.73%] individuals). Restricting to events >2 Mb in size, we observed an increase in event frequency as event size decreased. The combined results underscore that the rate of detectable mosaicism increases with age (p value = 5.5 × 10(-31)) and is higher in men (p value = 0.002) but lower in participants of African ancestry (p value = 0.003). In a subset of 47 individuals from whom serial samples were collected up to 6 years apart, complex changes were noted over time and showed an overall increase in the proportion of mosaic cells as age increased. Our large combined sample allowed for a unique ability to characterize detectable genetic mosaicism involving large structural events and strengthens the emerging evidence of non-random erosion of the genome in the aging population. Copyright © 2015 The American Society of Human Genetics. Published by Elsevier Inc. All rights reserved.
    The American Journal of Human Genetics 03/2015; 96(3):487-97. DOI:10.1016/j.ajhg.2015.01.011 · 11.20 Impact Factor
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    ABSTRACT: Recently the International Agency for Research on Cancer (IARC) Programme for the Evaluation of Carcinogenic Risks to Humans has been criticized for several of its evaluations, and also the approach used to perform these evaluations. Some critics have claimed that IARC Working Groups' failures to recognize study weaknesses and biases of Working Group members have led to inappropriate classification of a number of agents as carcinogenic to humans. The authors of this paper are scientists from various disciplines relevant to the identification and hazard evaluation of human carcinogens. We have examined here criticisms of the IARC classification process to determine the validity of these concerns. We review the history of IARC evaluations and describe how the IARC evaluations are performed. We conclude that these recent criticisms are unconvincing. The procedures employed by IARC to assemble Working Groups of scientists from the various discipline and the techniques followed to review the literature and perform hazard assessment of various agents provide a balanced evaluation and an appropriate indication of the weight of the evidence. Some disagreement by individual scientists to some evaluations is not evidence of process failure. The review process has been modified over time and will undoubtedly be altered in the future to improve the process. Any process can in theory be improved, and we would support continued review and improvement of the IARC processes. This does not mean, however, that the current procedures are flawed. The IARC Monographs have made, and continue to make, major contributions to the scientific underpinning for societal actions to improve the public's health.
    Environmental Health Perspectives 02/2015; DOI:10.1289/ehp.1409149 · 7.26 Impact Factor
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    ABSTRACT: PARK2, a gene associated with Parkinson disease, is a tumor suppressor in human malignancies. Here, we show that c.823C>T (p.Arg275Trp), a germline mutation in PARK2, is present in a family with eight cases of lung cancer. The resulting amino acid change, p.Arg275Trp, is located in the highly conserved RING finger 1 domain of PARK2, which encodes an E3 ubiquitin ligase. Upon further analysis, the c.823C>T mutation was detected in three additional families affected by lung cancer. The effect size for PARK2 c.823C>T (odds ratio = 5.24) in white individuals was larger than those reported for variants from lung cancer genome-wide association studies. These data implicate this PARK2 germline mutation as a genetic susceptibility factor for lung cancer. Our results provide a rationale for further investigations of this specific mutation and gene for evaluation of the possibility of developing targeted therapies against lung cancer in individuals with PARK2 variants by compensating for the loss-of-function effect caused by the associated variation. Copyright © 2015 The American Society of Human Genetics. Published by Elsevier Inc. All rights reserved.
    The American Journal of Human Genetics 01/2015; DOI:10.1016/j.ajhg.2014.12.016 · 11.20 Impact Factor
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    ABSTRACT: Lung cancer is the leading cause of cancer death worldwide. Although several genetic variants associated with lung cancer have been identified in the past, stringent selection criteria of genome-wide association studies (GWAS) can lead to missed variants. The objective of this study was to uncover missed variants by using the known association between lung cancer and first-degree family history of lung cancer to enrich the variant prioritization for lung cancer susceptibility regions. In this two-stage GWAS study, we first selected a list of variants associated with both lung cancer and family history of lung cancer in four GWAS (3,953 cases, 4,730 controls), then replicated our findings for 30 variants in a meta-analysis of four additional studies (7,510 cases, 7,476 controls). The top ranked genetic variant rs12415204 in chr10q23.33 encoding FFAR4 in the Discovery set was validated in the Replication set with an overall OR of 1.09 (95% CI = 1.04, 1.14, P = 1.63 × 10(-4) ). When combining the two stages of the study, the strongest association was found in rs1158970 at Ch4p15.2 encoding KCNIP4 with an OR of 0.89 (95% CI = 0.85, 0.94, P = 9.64 × 10(-6) ). We performed a stratified analysis of rs12415204 and rs1158970 across all eight studies by age, gender, smoking status, and histology, and found consistent results across strata. Four of the 30 replicated variants act as expression quantitative trait loci (eQTL) sites in 1,111 nontumor lung tissues and meet the genome-wide 10% FDR threshold. © 2015 WILEY PERIODICALS, INC.
    Genetic Epidemiology 01/2015; DOI:10.1002/gepi.21882 · 2.95 Impact Factor
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    ABSTRACT: We investigated genetic variation in CYP2A6 in relation to lung cancer risk among African American smokers, a high-risk population. Previously, we found that CYP2A6, a nicotine/nitrosamine metabolism gene, was associated with lung cancer risk in European Americans, but smoking habits, lung cancer risk, and CYP2A6 gene variants differ significantly between European and African ancestry populations. Herein, African American ever-smokers, drawn from two independent lung cancer case control studies, were genotyped for reduced activity CYP2A6 alleles and grouped by predicted metabolic activity. Lung cancer risk in the Southern Community Cohort Study (n = 494) was lower among CYP2A6 reduced versus normal metabolizers, as estimated by multivariate conditional logistic regression (OR = 0.44; 95% confidence interval [CI] = 0.26 to 0.73) and by unconditional logistic regression (OR = 0.62; 95% confidence interval [CI] = 0.41 to 0.94). The association was replicated in an independent study from MD Anderson Cancer Center (n = 407) (OR = 0.64; 95% CI = 0.42 to 0.98), and pooling the studies yielded an odds ratio of 0.64 (95% CI = 0.48 to 0.86). Exploratory analyses revealed a significant interaction between CYP2A6 genotype and sex on the risk for lung cancer (Southern Community Cohort Study: P=.03; MD Anderson: P=.03; Pooled Studies: P=.003) with a CYP2A6 effect in men only. These findings support a contribution of genetic variation in CYP2A6 to lung cancer risk among African American smokers, particularly men, whereby CYP2A6 genotypes associated with reduced metabolic activity confer a lower risk of developing lung cancer. © The Author 2014. Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oup.com.
    Carcinogenesis 11/2014; 36(1). DOI:10.1093/carcin/bgu235 · 5.27 Impact Factor
  • Epidemiology (Cambridge, Mass.) 11/2014; 25(6):934-935. DOI:10.1097/EDE.0000000000000183 · 6.18 Impact Factor
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    ABSTRACT: There is expanding consensus on the need to modernize the training of cancer epidemiologists to accommodate rapidly emerging technological advancements and the digital age, which are transforming the practice of cancer epidemiology. There is also a growing imperative to extend cancer epidemiology research that is etiological to that which is applied and has the potential to affect individual and public health. Medical schools and schools of public health are recognizing the need to develop such integrated programs; however, we lack the data to estimate how many current training programs are effectively equipping epidemiology students with the knowledge and tools to design, conduct, and analyze these increasingly complex studies. There is also a need to develop new mentoring approaches to account for the transdisciplinary team-science environment that now prevails. With increased dialogue among schools of public health, medical schools, and cancer centers, revised competencies and training programs at predoctoral, doctoral, and postdoctoral levels must be developed. Continuous collection of data on the impact and outcomes of such programs is also recommended.
    American Journal of Epidemiology 09/2014; 180(10). DOI:10.1093/aje/kwu256 · 4.98 Impact Factor
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    ABSTRACT: Background:There is an urgent need to improve lung cancer outcome by identifying and validating markers of risk. We previously reported that the cytokinesis-blocked micronucleus assay (CBMN) is a strong predictor of lung cancer risk. Here we validate our findings in an independent external lung cancer population and test discriminatory power improvement of the Spitz risk prediction model upon extension with this biomarker. Methods:1,506 participants were stratified into a test set of 995 (527 cases /468 controls) from MD Anderson Cancer Center and a validation set of 511 (239 cases / 272 controls) from Massachusetts General Hospital. An epidemiologic questionnaire was administered and genetic instability was assessed using the CBMN assay. Results:Excellent concordance was observed between the two populations in levels and distribution of CBMN endpoints [binucleated-micronuclei (BN-MN), binucleated-nucleoplasmic bridges (BN-NPB)] with significantly higher mean BN-MN and BN-NPB values among cases (P<0.0001). Extension of the Spitz model led to an overall improvement in the AUC (95% CI) from 0.61 (55.5 - 65.7) with epidemiological variables to 0.92 (89.4 - 94.2) with the addition of BN-MN endpoint. The most dramatic improvement was observed with the never smokers extended model followed by the former and current smokers. Conclusions:The CBMN assay is a sensitive and specific predictor of lung cancer risk and extension of the Spitz risk prediction model led to an AUC that may prove useful in population screening programs to identify the "true" high risk individuals. Impact: Identifying high-risk subgroups that would benefit from screening surveillance has immense public health significance.
    Cancer Epidemiology Biomarkers & Prevention 08/2014; 23(11). DOI:10.1158/1055-9965.EPI-14-0462 · 4.32 Impact Factor
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    ABSTRACT: Background: Smoking experimentation in Mexican American youth is problematic. In light of the research showing that preventing smoking experimentation is a valid strategy for smoking prevention, there is a need to identify Mexican American youth at high risk for experimentation. Methods: A prospective population-based cohort of 1179 adolescents of Mexican descent was followed for 5 years starting in 2005-06. Participants completed a baseline interview at a home visit followed by three telephone interviews at intervals of approximately 6 months and additional interviews at two home visits in 2008-09 and 2010-11. The primary end point of interest in this study was smoking experimentation. Information regarding social, cultural, and behavioral factors (e.g., acculturation, susceptibility to experimentation, home characteristics, household influences) was collected at baseline using validated questionnaires. Results: Age, sex, cognitive susceptibility, household smoking behavior, peer influence, neighborhood influence, acculturation, work characteristics, positive outcome expectations, family cohesion, degree of tension, ability to concentrate, and school discipline were found to be associated with smoking experimentation. In a validation dataset, the proposed risk prediction model had an AUC of 0.719 (95% confidence interval, 0.637 to 0.801) for predicting absolute risk for smoking experimentation within 1 year. Conclusions: The proposed risk prediction model is able to quantify the risk of smoking experimentation in Mexican American adolescents. Impact: Accurately identifying Mexican American adolescents who are at higher risk for smoking experimentation who can be intervened will substantially reduce the incidence of smoking and thereby subsequent health risks.
    Cancer Epidemiology Biomarkers & Prevention 07/2014; 23(10). DOI:10.1158/1055-9965.EPI-14-0467 · 4.32 Impact Factor
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    ABSTRACT: Genome-wide association studies (GWAS) have mapped risk alleles for at least ten distinct cancers to a small region of 63,000 bp on chromosome 5p15.33. This region harbors the TERT and CLPTM1L genes; the former encodes the catalytic subunit of telomerase reverse transcriptase and the latter may play a role in apoptosis. To investigate further the genetic architecture of common susceptibility alleles in this region, we conducted an agnostic subset-based meta-analysis (ASSET) across six distinct cancers in 34,248 cases and 45,036 controls. Based on sequential conditional analysis, we identified as many as six independent risk loci marked by common single nucleotide polymorphisms (SNPs): five in the TERT gene (region 1: rs7726159, P=2.10x10-39; region 3: rs2853677, P=3.30x10-36 and PConditional=2.36x10-8; region 4: rs2736098, P=3.87x10-12 and PConditional=5.19x10-6, region 5: rs13172201, P=0.041 and PConditional=2.04x10-6; and region 6: rs10069690, P=7.49x10-15 and PConditional=5.35x10-7) and one in the neighboring CLPTM1L gene (region 2: rs451360; P=1.90x10-18 and PConditional=7.06x10-16). Between three and five cancers mapped to each independent locus with both risk-enhancing and protective effects. Allele specific effects on DNA methylation were seen for a subset of risk loci indicating that methylation and subsequent effects on gene expression may contribute to the biology of risk variants on 5p15.33. Our results provide strong support for extensive pleiotropy across this region of 5p15.33, to an extent not previously observed in other cancer susceptibility loci.
    Human Molecular Genetics 07/2014; DOI:10.1093/hmg/ddu363 · 6.68 Impact Factor
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    ABSTRACT: Wingless-type protein (Wnt)/β-catenin pathway alterations in non-small cell lung cancer (NSCLC) are associated with poor prognosis and resistance. In 598 stage III-IV NSCLC patients receiving platinum-based chemotherapy at the MD Anderson Cancer Center (MDACC), we correlated survival with 441 host single-nucleotide polymorphisms (SNPs) in 50 Wnt pathway genes. We then assessed the most significant SNPs in 240 Mayo Clinic patients receiving platinum-based chemotherapy for advanced NSCLC, 127 MDACC patients receiving platinum-based adjuvant chemotherapy and 340 early stage MDACC patients undergoing surgery alone (cohorts 2-4). In multivariate analysis, survival correlates with SNPs for AXIN2 (rs11868547 and rs4541111, of which rs11868547 was assessed in cohorts 2-4), Wnt-5B (rs12819505), CXXC4 (rs4413407) and WIF-1 (rs10878232). Median survival was 19.7, 15.6 and 10.7 months for patients with 1, 2 and 3-5 unfavorable genotypes, respectively (P=3.8 × 10(-9)). Survival tree analysis classified patients into two groups (median survival time 11.3 vs 17.3 months, P=4.7 × 10(-8)). None of the SNPs achieved significance in cohorts 2-4; however, there was a trend in the same direction as cohort 1 for 3 of the SNPs. Using online databases, we found rs10878232 displayed expression quantitative trait loci correlation with the expression of LEMD3, a neighboring gene previously associated with NSCLC survival. In conclusion, results from cohort 1 provide further evidence for an important role for Wnt in NSCLC. Investigation of Wnt inhibitors in advanced NSCLC would be reasonable. Lack of an SNP association with outcome in cohorts 2-4 could be due to low statistical power, impact of patient heterogeneity or false-positive observations in cohort 1.The Pharmacogenomics Journal advance online publication, 1 July 2014; doi:10.1038/tpj.2014.21.
    The Pharmacogenomics Journal 07/2014; DOI:10.1038/tpj.2014.21 · 5.51 Impact Factor
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    ABSTRACT: Lung cancer causes more deaths worldwide than any other cancer. In addition to cigarette smoking, dietary factors may contribute to lung carcinogenesis. Epidemiologic studies, including the environment and genetics in lung cancer etiology (EAGLE), have reported increased consumption of red/processed meats to be associated with higher risk of lung cancer. Heme-iron toxicity may link meat intake with cancer. We investigated this hypothesis in meat-related lung carcinogenesis using whole genome expression. We measured genome-wide expression (HG-U133A) in 49 tumor and 42 non-involved fresh frozen lung tissues of 64 adenocarcinoma EAGLE patients. We studied gene expression profiles by high-versus-low meat consumption, with and without adjustment by sex, age, and smoking. Threshold for significance was a false discovery rate (FDR) ≤0.15. We studied whether the identified genes played a role in heme-iron related processes by means of manually curated literature search and gene ontology-based pathway analysis. We found that gene expression of 232 annotated genes in tumor tissue significantly distinguished lung adenocarcinoma cases who consumed above/below the median intake of fresh red meats (FDR = 0.12). Sixty-three (∼28%) of the 232 identified genes (12 expected by chance, P-value < 0.001) were involved in heme binding, absorption, transport, and Wnt signaling pathway (e.g., CYPs, TPO, HPX, HFE, SLCs, and WNTs). We also identified several genes involved in lipid metabolism (e.g., NCR1, TNF, and UCP3) and oxidative stress (e.g., TPO, SGK2, and MTHFR) that may be indirectly related to heme-toxicity. The study's results provide preliminary evidence that heme-iron toxicity might be one underlying mechanism linking fresh red meat intake and lung cancer. © 2013 Wiley Periodicals, Inc.
    Molecular Carcinogenesis 07/2014; 53(7). DOI:10.1002/mc.22006 · 4.27 Impact Factor
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    ABSTRACT: Inflammation is a facilitating process for multiple cancer types. It is believed to affect cancer development and progression through several etiologic pathways including increased levels of DNA adduct formation, increased angiogenesis and altered anti-apoptotic signaling. This review highlights the application of inflammatory biomarkers in epidemiologic studies and discusses the various cellular mediators of inflammation characterizing the innate immune system response to infection and chronic insult from environmental factors. Included is a review of six classes of inflammation-related biomarkers: cytokines/chemokines, immune-related effectors, acute phase proteins, reactive oxygen and nitrogen species, prostaglandins and cyclooxygenase-related factors, and mediators such as transcription factors and growth factors. For each of these biomarkers we provide a brief overview of the etiologic role in the inflammation response and how they have been related to cancer etiology and progression within the literature. We provide a discussion of the common techniques available for quantification of each marker including strengths, weaknesses and potential pitfalls. Subsequently, we highlight a few under-studied measures to characterize the inflammatory response and their potential utility in epidemiologic studies of cancer. Finally, we suggest integrative methods for future studies to apply multi-faceted approaches to examine the relationship between inflammatory markers and their roles in cancer development.
    Cancer Epidemiology Biomarkers & Prevention 06/2014; 23(9). DOI:10.1158/1055-9965.EPI-14-0064 · 4.32 Impact Factor
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    ABSTRACT: We conducted imputation to the 1000 Genomes Project of four genome-wide association studies of lung cancer in populations of European ancestry (11,348 cases and 15,861 controls) and genotyped an additional 10,246 cases and 38,295 controls for follow-up. We identified large-effect genome-wide associations for squamous lung cancer with the rare variants BRCA2 p.Lys3326X (rs11571833, odds ratio (OR) = 2.47, P = 4.74 × 10−20) and CHEK2 p.Ile157Thr (rs17879961, OR = 0.38, P = 1.27 × 10−13). We also showed an association between common variation at 3q28 (TP63, rs13314271, OR = 1.13, P = 7.22 × 10−10) and lung adenocarcinoma that had been previously reported only in Asians. These findings provide further evidence for inherited genetic susceptibility to lung cancer and its biological basis. Additionally, our analysis demonstrates that imputation can identify rare disease-causing variants with substantive effects on cancer risk from preexisting genome-wide association study data.
    Nature Genetics 06/2014; 46(7). DOI:10.1038/ng.3002 · 29.65 Impact Factor
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    ABSTRACT: Background:accurate prognostic prediction is challenging for advanced-stage non-small cell lung cancer (NSCLC) patients.Methods:we systematically investigated genetic variants within inflammation pathway as potential prognostic markers for advanced-stage NSCLC patients treated with first-line chemotherapy. A discovery phase in 502 patients and an internal validation in 335 patients were completed at MD Anderson Cancer Center. External validation was performed in 371 patients at Harvard University.Results:a missense SNP (HLA-DOB:rs2071554) predicted to influence protein function was significantly associated with poor survival in the discovery (HR:1.46, 95% CI:1.02-2.09), internal validation (HR:1.51, 95% CI:1.02-2.25), and external validation (HR:1.52, 95% CI:1.01-2.29) populations. KLRK1:rs2900420 was associated with a reduced risk in the discovery (HR:0.76, 95% CI:0.60-0.96), internal validation (HR:0.77, 95% CI:0.61-0.99), and external validation (HR:0.80, 95% CI:0.63-1.02) populations. A strong cumulative effect was observed for these SNPs on overall survival.Conclusions:Genetic variations in inflammation-related genes could have potential to complement prediction of prognosis.Clinical Pharmacology & Therapeutics (2014); Accepted article preview online 22 April 2014; doi:10.1038/clpt.2014.89.
    Clinical Pharmacology &#38 Therapeutics 04/2014; 96(3). DOI:10.1038/clpt.2014.89 · 6.85 Impact Factor
  • Cancer Prevention Research 01/2014; 5(11_Supplement):A106-A106. DOI:10.1158/1940-6207.PREV-12-A106 · 5.27 Impact Factor
  • 01/2014; DOI:10.6000/ijipem/2014/1
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    ABSTRACT: We scanned through the genomes of 29,141 African Americans, searching for loci where the average proportion of African ancestry deviates significantly from the genome-wide average. We failed to find any genome-wide significant deviations, and conclude that any selection in African Americans since admixture is sufficiently weak that it falls below the threshold of our power to detect it using a large sample size. These results stand in contrast to the findings of a recent study of selection in African Americans. That study, which had 15 times fewer samples, reported six loci with significant deviations. We show that the discrepancy is likely due to insufficient correction for multiple hypothesis testing in the previous study. The same study reported 14 loci that showed greater population differentiation between African Americans and Nigerian Yoruba than would be expected in the absence of natural selection. Four such loci were previously shown to be genome-wide significant and likely to be affected by selection, but we show that most of the 10 additional loci are likely to be false positives. Additionally, the most parsimonious explanation for the loci that have significant evidence of unusual differentiation in frequency between Nigerians and Africans Americans is selection in Africa prior to their forced migration to the Americas.
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    ABSTRACT: Nonalcoholic fatty liver disease (NAFLD) is an emerging epidemic with high prevalence in Western countries. Genome-wide association studies had reported that a variation in the patatin-like phospholipase domain containing 3 (PNPLA3) gene is associated with high susceptibility to NAFLD. However, the relationship between this variation and hepatocellular carcinoma (HCC) has not been well established. We investigated the impact of PNPLA3 genetic variation (rs738409: C>G) on HCC risk and prognosis in the United States by conducting a case-control study that included 257 newly diagnosed and pathologically confirmed Caucasian patients with HCC (cases) and 494 healthy controls. Multivariate logistics and Cox regression models were used to control for the confounding effects of HCC risk and prognostic factors. We observed higher risk of HCC for subjects with a homozygous GG genotype than for those with CC or CG genotypes, the adjusted odds ratio (OR) was 3.21 (95% confidence interval [CI], 1.68-6.41). We observed risk modification among individuals with diabetes mellitus (OR = 19.11; 95% CI, 5.13-71.20). The PNPLA3 GG genotype was significantly associated with underlying cirrhosis in HCC patients (OR = 2.48; 95% CI, 1.05-5.87). Moreover, GG allele represents an independent risk factor for death. The adjusted hazard ratio of the GG genotype was 2.11 (95% CI, 1.26-3.52) compared with CC and CG genotypes. PNPLA3 genetic variation (rs738409: C>G) may determine individual susceptibility to HCC development and poor prognosis. Further experimental investigations are necessary for thorough assessment of the hepatocarcinogenic role of PNPLA3. © 2013 Wiley Periodicals, Inc.
    Molecular Carcinogenesis 11/2013; 52(S1). DOI:10.1002/mc.22057 · 4.27 Impact Factor

Publication Stats

21k Citations
3,375.88 Total Impact Points

Institutions

  • 2010–2015
    • Baylor College of Medicine
      • Dan L. Duncan Cancer Center
      Houston, Texas, United States
    • International Agency for Research on Cancer
      • Genetic Epidemiology Group
      Lyons, Rhône-Alpes, France
  • 1989–2014
    • University of Texas MD Anderson Cancer Center
      • Department of Epidemiology
      Houston, Texas, United States
  • 2013
    • University of Toronto
      • Department of Pharmacology and Toxicology
      Toronto, Ontario, Canada
    • Dartmouth College
      • Geisel School of Medicine
      Hanover, New Hampshire, United States
    • Molecular and Cellular Biology Program
      Seattle, Washington, United States
  • 2012
    • Harvard Medical School
      • Department of Medicine
      Boston, Massachusetts, United States
    • Karmanos Cancer Institute
      Detroit, Michigan, United States
  • 2008–2012
    • Washington University in St. Louis
      San Luis, Missouri, United States
    • Keele University
      Newcastle-under-Lyme, England, United Kingdom
  • 1998–2012
    • University of Texas Southwestern Medical Center
      • Hamon Center for Therapeutic Oncology Research
      Dallas, Texas, United States
  • 2011
    • United States Army
      Washington, West Virginia, United States
  • 2009
    • National Institutes of Health
      • Division of Cancer Epidemiology and Genetics
      Bethesda, MD, United States
  • 2007
    • University of California, San Francisco
      San Francisco, California, United States
  • 2006–2007
    • National Cancer Institute (USA)
      • Division of Cancer Epidemiology and Genetics
      Bethesda, MD, United States
  • 1989–2007
    • University of Houston
      Houston, Texas, United States
  • 2004
    • University of Pennsylvania
      Filadelfia, Pennsylvania, United States
  • 2000–2001
    • Nanjing Medical University
      • Department of Epidemiology and Biostatistics
      Nanjing, Jiangsu Sheng, China
  • 1999–2000
    • University of California, Los Angeles
      • Department of Epidemiology
      Los Angeles, CA, United States
    • Louisiana State University in Shreveport
      Shreveport, Louisiana, United States
  • 1990
    • Henry Ford Hospital
      Detroit, Michigan, United States
  • 1985
    • Icahn School of Medicine at Mount Sinai
      Manhattan, New York, United States