Superfund Research Program

Project 1: Biomarkers of Chemical Exposure and Leukemia Risk

• Section Navigation:
• Summary
• News
• Events
• Project Update
• Publications

Summary

This project builds upon the existing Northern California Childhood Leukemia Study (NCCLS), a large case-control study with over 1,000 cases. Its overall goal is to determine the role exposure to environmental chemicals plays in the etiology of childhood leukemia. Project investigators are examining the potential role benzene, polycyclic aromatic hydrocarbons (PAH) and other selected Superfund chemicals, such as trichloroethylene (TCE), play in the etiology of childhood leukemia in California. They are using state-of-the-art exposure assessment techniques to accomplish this goal. They are further using gene expression profiling and proteomics to develop new biomarkers that aid in the classification of etiologic subtypes of this disease and help find its cause(s). The hypothesis is that certain subtypes of leukemia will have specific environmental causes. Specifically, Drs. Buffler and Smith are: 1) Extending case ascertainment through 2009, such that biological samples will be available from over 1000 cases; 2) characterizing the childhood leukemia cases by proteomics and gene expression profiling; 3) collaborating with the CDC to measure more than 30 volatile hydrocarbons in the blood of mothers of children with leukemia and control mothers (they are comparing these measures with results from concomitant home air and water sampling and with surrogate markers of past exposures to VOCs using self-reported exposure to tobacco smoke and estimated traffic density); 4) measuring protein adducts of benzene and naphthalene (a representative PAH) in serum from mothers of cases and controls in collaboration with Dr. Rappaport of the University of North Carolina SBRP; and, 5) measuring protein adducts of benzene and naphthalene in the plasma of children with different forms of leukemia and correlate these measurements with the chemical exposure analysis conducted with household samples. The strengths of the study are: a) Large sample size; b) extensive residential exposure assessment; c) measures of current and cumulative exposure to Superfund chemicals in both case and control mothers and children; d) ability to compare exposures to national NHANES data; e) availability of carefully processed biological samples; and, f) application of sophisticated -omic technologies to case characterization. These studies should provide new insights into the role of chemical exposure in the etiology of childhood leukemia and produce new biomarkers of exposure and disease status that can be used in future studies.

News

Events

No events at this time.

Project Update

Childhood leukemia is the most common form of childhood cancer affecting 3,000 children annually in the U.S. and many more worldwide. The causes are essentially unknown. The major form of childhood leukemia is ALL (acute lymphoblastic leukemia) and the other is AML (acute myeloid leukemia).

Overall goals
The goal of Project 1 is to determine the role chemical exposures play in the development of childhood leukemia. In one of the largest studies of its kind in the world, bone marrow and/or peripheral blood was obtained on 961 cases of childhood leukemia and peripheral blood and urine obtained from many of the mothers. These have been analyzed with the latest technologies.

Important discoveries so far

1. Project 1 investigators examined whether the use of paint and petroleum solvents at home before birth and in early childhood influenced the risk of leukemia in children. They found that ALL risk was significantly associated with paint exposure, with a higher risk observed when paint was used post-natally, by an adult other than the mother, or frequently. They found no significant association between solvent use and ALL risk overall, but a significant association with AML risk was observed.
2. The investigators measured blood levels of selected Superfund chemicals in the blood of mothers of children with leukemia and control mothers, including 33 volatile organic compounds (VOCs), and urine levels for 10 cancer-causing polycyclic aromatic hydrocarbons (PAHs) and cotinine (a biomarker of smoking). House dust was collected simultaneously and a significant positive correlation between levels of nicotine in house dust and those of serum cotinine (a nicotine metabolite) in maternal blood samples was found, showing that nicotine in house dust is a good surrogate marker of adult smoking in the home. House dust was also used as an exposure indicator to examine the risk of childhood leukemia in relation to residential exposure to persistent organochlorine chemicals, such as polychlorinated biphenyls (PCB). Detection of any PCB congener in the dust conferred a 2-fold increased risk of ALL.
3. Earlier studies had shown that most causal genetic changes found in the children’s leukemia were present before they were born. Recent studies have shown that secondary changes, including those in a cancer gene called RAS, occur post-natally after the child is born.

What we plan to do next
The project has now become part of a new NIEHS/EPA Children’s Environmental Health Center, called the Center for Interdisciplinary Research on Childhood Leukemia and the Environment (CIRCLE) lead by Dr. Buffler.

» Project Update Archive

Selected Publications

2013

• Rappaport SM, Kim S, Thomas R, Johnson BA, Bois FY, Kupper LL (2013) Low-dose metabolism of benzene in humans: science and obfuscation. Carcinogenesis. Jan;34(1):2-9. PMID: 23222815. (PMC Journal – In Process). [PDF]
  
• Ren X, Ji Z, Yuh J, Tang M, Bersonda J, Smith MT, Zhang L (2013) The impact of FANCD2 deficiency on formaldehyde-induced toxicity in human lymphoblastoid cell lines. Arch Toxicol. Jan;87(1):189-196. PMID: 22872141. NIHMS399462. [PDF]
  
• Zhang L, Bassig BA, Mora JL, Vermeulen R, Ge Y, Curry JD, Hu W, Shen M, Qiu C, Ji Z, Reiss B, McHale CM, Liu S, Guo W, Purdue MP, Yue F, Li L, Smith MT, Huang H, Tang X, Rothman N, Lan Q (2013) Alterations in serum immunoglobulin levels in workers occupationally exposed to trichloroethylene. Carcinogenesis. Jan16. [Epub ahead of print]. PMID: 23276795. (PMC Journal- In Progress). [PDF]

2012

• Zhang L, Lan Q, Ji Z, Li G, Shen M, Vermeulen R, Guo W, Hubbard A, McHale CM, Rappaport SM, Hayes RB, Linet B, Yin S, Fraumeni JF, Rothman N, Smith MT (2012). Leukemia-related chromosomal loss detected in hematopoietic progenitor cells of benzene-exposed workers. Leukemia. Dec;26(12):2494-2498. PMCID: PMC3472034. [PDF]
• O’Connor ST, Lan J, North M, Loguinov A, Zhang L, Smith MT, Gu A, Vulpe C (2012) Genome-wide functional and stress response profiling reveals toxic mechanism and genes required for tolerance to benzo[a]pyrene in S. cerevisiae. Front in Toxicogenomics. Dec;doi: 10.3389/fgene.2012.00316. (PMC Journal – In Process). [PDF]
• Vermeulen R, Zhang L, Spirenburg A, Tang X, Bonventre JV, Reiss B, Shen M, Smith MT, Qui C, Ge Y, Ji Z, Xiong J, He J, Hao Z, Liu S, Xie Y, Yue F, Guo W, Purdue M, Beane-Freeman LE, Sabbisetti V, Li L, Huang H, Rothman N, Lan Q (2012) Kidney toxicity in Chinese factory workers exposed to trichloroethylene. Carcinogenesis. Aug;33(8):1538-41. PMID: 22730190. [PDF]
• Ji Z, Weldon RH, Marchetti F, Chen H, Li G, Xing C, Kurtovich E, Young S, Schmid TE, Waidyanatha S, Rappaport SM, Zhang L, Eskenazi B (2012) Comparison of aneuploidies of chromosomes 21, X, and Y in the blood lymphocytes and sperm cells among workers exposed to benzene. Environ Mol Mutagen. Apr;53(3):218-26. PMID: 22351378. (PMC Journal – In Process). [PDF]
• Marchetti F, Eskenazi B, Weldon RH, Li G, Zhang L, Rappaport SM, Schmid TE, Xing C, Kurtovich E, Wyrobek AJ (2012) Occupational exposure to benzene and chromosomal structural aberrations in the sperm of Chinese men. Environ Health Perspect. Feb;120(2):229-34. PMCID: PMC3279447. [PDF]
• Godderis L, Thomas R, Hubbard AE, Tabish AM, Hoet P, Zhang L, Smith MT, Veulemans H,  McHale CM (2012) Effect of Chemical Mutagens and Carcinogens on Gene Expression Profiles in Human TK6 Cells. PLoS One. 7(6):e39205. PMCID: PMC3377624. [PDF]

2011

• Hosgood HD, Zhang L, Tang X, Vermeulen R, Shen M, Smith MT, Blair A, Qui C, Ge Y, Ji Z, Xiong J, He J, Reiss B, Liu S, Xie Y, Guo W, Galvan N, Li L, Hao Z, Rothman N, Huang H, Lan Q (2011) Decreased numbers of CD4+ naive and effector memory T cells, and CD8+ naïve T cells, are associated with trichloroethylene exposure. Front Oncol. 1:53. PMCID: PMC3355872. [PDF]
• Chang JS, Zhou M, Buffler PA, Chokkalingam AP, Metayer C, Wiemels JL (2011) Profound Deficit of IL10 at Birth in Children Who Develop Childhood Acute Lymphoblastic Leukemia. Cancer Epidemiol Biomarkers Prev. Aug;20(8):1736-40. PMID: 21653647. [PDF]
• Smith MT, Zhang L, McHale CM, Skibola CF, Rappaport SM (2011) Benzene, the exposome and future investigations of leukemia etiology. Chem Biol Interact. Jun 30;192(1-2):155-9. PMID: 21333640. [PDF]
• Shen M, Zhang L, Lee KM, Vermeulen R, Hosgood HD, Li G, Yin S, Rothman N, Chanock S, Smith MT, Lan Q (2011) Polymorphisms in genes involved in innate immunity and susceptibility to benzene-induced hematotoxicity. Exp mol Med. Jun 30;43(6):374-8. PMCID: PMC3128916. [PDF]
• Ren X, Aleshin M, Jo WJ, Dills R, Kalman DA, Vulpe CD, Smith MT, Zhang L (2011) Involvement of N-6 Adenine-Specific DNA Methyltransferase 1 (N6AMT1) in Arsenic Biomethylation and Its Role in Arsenic-Induced Toxicity. Environ Health Perspect. Jun;119(6):771-7. PMCID: PMC3114810. [PDF]
• McHale CM, Zhang L, Lan Q, Vermeulen R, Li G, Hubbard AE, Porter KE, Thomas R, Portier CJ, Shen M, Rappaport SM, Yin S, Smith MT, Rothman N (2011) Global Gene Expression Profiling of a Population Exposed to a Range of Benzene Levels. Environ Health Perspect. May;119(5):628-34. PMCID: PMC3094412. [PDF]
• Zhang L, Lan Q, Guo W, Hubbard AE, Li G, Rappaport SM, McHale CM, Shen M, Ji Z, Vermeulen R, Yin S, Rothman N, Smith MT (2011) Chromosome-Wide Aneuploidy Study (CWAS) in Workers Exposed to an Established Leukemogen, Benzene. Carcinogenesis. Apr;32(4):605-12. PMCID: PMC3066415. [PDF]
• Urayama KY, Ma X, Selvin S, Metayer C, Chokkalingam AP, Wiemels JL, Does M, Chang J, Wong A, Trachthenberg E, Buffler PA (2011) Early Life exposure to infections and risk of childhood acute lymphoblastic leukemia. Int J Cancer. Apr 1;128(7):1632-43. PMID: 21280034.  [PDF]
• Does M, Scélo G, Metayer C, Selvin S, Kavet R, Buffler PA (2011) Exposure to electrical contact currents and the risk of childhood leukemia. Radiat Res. Mar;175(3):390-6. PMID: 21388283. [PDF]
• Metayer C, Scélo G, Chokkalingam AP, Barcellos LF, Aldrich MC, Chang JS, Guha N, Urayama KY, Hansen HM, Block G, Kiley V, Wiencke JK, Wiemels JL, Buffler PA (2011) Genetic variants in the folate pathway and risk of childhood acute lymphoblastic leukemia. Cancer Causes Control. Sep;22(9):1243-58. PMID: 21748308. [PDF]
• Ren X, Lim S, Ji Z, Yuh J, Peng V, Smith MT, Zhang L (2011) Comparison of Proliferation and Genomic Instability Responses to WRN Silencing in Hematopoietic HL60 and TK6 Cells. PLoS One. Jan 18;6(1):e14546. PMCID: PMC3022623. [PDF]
• Novak R, Zeng Y, Shuga J, Venugopalan G, Fletcher DA, Smith MT, Mathies RA (2011) Single cell multiplex gene detection and sequencing with microfluidically generated agarose emulsions. Angew Chem Int Ed Engl. Jan 10;50(2):390-5. PMCID: PMC3027204. [PDF]

2010

• Bartley K, Metayer C, Selvin S, Ducore J, Buffler PA (2010) Diagnostic X-rays and risk of childhood leukemia. Int J Epidemiol. Dec;39(6):1628-37. PMID: 20889538. [PDF]
• Rappaport SM, Smith MT (2010) Environment and disease risks. Science, Oct 22. 330(6003):460-1. PMID: 20966241. [PDF]
• Rappaport SM, Smith MT (2010) Environment and disease risks. Science. Oct 22. In Press. [PDF]
• Wiemels JL, Kang M, Chang JS, Zheng L, Kouyoumji C, Zhang L, Smith MT, Scelo G, Metayer C, Buffler P, Wiencke JK (2010) Backtracking RAS mutations in high hyperdiploid childhood acute lymphoblastic leukemia. Blood Cells Mol Dis. Oct 15;45(3):186-91. PMCID: PMC2943008. [PDF]
• Ward EM, Schulte PA, Straif K, Hopf NB, Caldwell JC, Carreón T, Demarini DM, Fowler BA, Goldstein BD, Hemminki K, Hines CJ, Pursiainen KH, Kuempel E, Lewtas J, Lunn RM, Lynge E, McElvenny DM, Muhle H, Nakajima T, Robertson LW, Rothman N, Ruder AM, Schubauer-Berigan MK, Siemiatycki J, Silverman D, Smith MT, Sorahan T, Steenland K, Stevens RG, Vineis P, Zahm SH, Zeise L, Cogliano VJ (2010) Research recommendations for selected IARC-classified agents. Environ Health Perspect. Oct;118(10):1355-62. PMCID: PMC2957912. [PDF]
• McHale, CM, Zhang L, Hubbard AE, Smith MT (2010) Toxicogenomic profiling of chemically exposed humans in risk assessment. Mutat Res. Apr 9. [Epub ahead of print]. PMCID: PMC2928857. [PDF]
• Rappaport SM, Kim S, Lan Q, Li G, Vermeulen R, Waidyanatha S, Zhang L, Yin S, Smith MT and Rothman N (2010) Human benzene metabolism following occupational and environmental exposures. Chem Biol Interact, 184(1-2):189-95. PMID: 20026321 [PDF]
• Smith MT (2010) Advances in understanding benzene health effects and susceptibility. Annu Rev Public Health. Apr 21; 31:133-48. PMID: 20070208. [PDF]
• Zhang L, McHale CM, Rothman N, Li G, Ji Z, Vermeulen R, Hubbard AE, Ren X, Shen M, Rappaport SM, North M, Skibola CF, Yin S, Vulpe C, Chanock SJ, Smith MT, Lan Q (2010) Systems biology of human benzene exposure. Chem Biol Interact. Mar 19;184(1-2):86-93. PMID: 20026094. PMCID: PMC2846187. [PDF]
• Lightfoot TJ, Roman E, Smith MT, Skibola CF (2010) Acute lymphoblastic leukaemia in children – is there a role for MTHFR? Br J Haematol. Feb 8 [Epub ahead of print]. PMID: 20148884. [PDF]
• Vlaanderen J, Moore LE, Smith MT, Lan Q, Zhang L, Skibola CF, Rothman N, Vermeulen R (2010) Application of OMICS technologies in occupational and environmental health research; current status and projections. Occup Environ Med. Feb; 67(2):136-43. PMID: 19933307. [PDF]
• Lightfoot TJ, Johnston WT, Painter D, Simpson J, Roman E, Skibola CF, Smith MT, Allan JM, Taylor GM (2010) Genetic variation in the folate metabolic pathway and risk of childhood leukemia. Blood. Jan 25; PMID: 20101025. [PDF]

2009

• Whitehead T, Metayer C, Gunier RB, Ward MH, Nishioka MG, Buffler P, Rappaport SM (2009) Determinants of polycyclic aromatic hydrocarbon levels in house dust. J Expo Sci Environ Epidemiol. Dec 30. [Epub ahead of print] doi:10.1038/jes.2009.68. PMID: 20040932. [PDF]
• Chang JS, Buffler PA, Metayer C, Chokkalingam AP, Patoka J, Kronish D, Wiemels JL (2009) Maternal immunoglobulin E and childhood leukemia. Cancer Epidemiol Biomarkers Prev. Aug; 18(8):2221-7. PMID: 19622720. [PDF]
• Urayama KY, Von Behren J, Reynolds P, Hertz A, Does M, Buffler PA (2009) Factors associated with residential mobility in children with leukemia: implications for assigning exposures. Ann Epidemiol. Nov; 19(11):834-40. PMID: 19364662. PMCID: PMC2761989. [PDF]
• Ward MH, Colt JS, Metayer C, Gunier RB, Lubin J, Crouse V, Nishioka MG, Reynolds P, Buffler PA (2009) Residential exposure to polychlorinated biphenyls and organochlorine pesticides and risk of childhood leukemia. Environ Health Perspect. Jun; 117(6):1007-13. PMID: 19590698. PMCID: PMC2702395. [PDF]
• Whitehead T, Metayer C, Ward MH, Nishioka MG, Gunier R, Colt JS, Reynolds P, Selvin S, Buffler P, Rappaport SM (2009) Is house-dust nicotine a good surrogate for household smoking? Am J Epidemiol. May 1; 169(9):1113-23. PMID: 19299402. PMCID: PMC2727236. [PDF]
• Scelo G, Metayer C, Zhang L, Wiemels JL, Aldrich MC, Selvin S, Month S, Smith MT, Buffler PA (2009) Household exposure to paint and petroleum solvents, chromosomal translocations, and the risk of childhood leukemia. Environ Health Perspect. Jan; 117(1):133-9. PMID: 19165400. PMCID: PMC2627857. [PDF]

2008

• Guha N, Chang JS, Chokkalingam AP, Wiemels JL, Smith MT, Buffler PA (2008) NQO1 polymorphisms and de novo childhood leukemia: a HuGE review and meta-analysis. Am J Epidemiol. Dec 1; 168(11):1221-32. PMID: 18945694. PMCID: PMC2727266. [PDF]
• Wiemels JL, Hofmann J, Kang M, Selzer R, Green R, Zhou M, Zhong S, Zhang L, Smith MT, Marsit C, Loh M, Buffler P, Yeh RF (2008) Chromosome 12p deletions in TEL-AML1 childhood acute lymphoblastic leukemia are associated with retrotransposon elements and occur postnatally. Cancer Res. Dec 1; 68(23):9935-44. PMID: 19047175. PMCID: PMC2597307. [PDF]
• Vasconcelos GM, Kang M, Pombo-de-Oliveira MS, Schiffman JD, Lorey F, Buffler P, Wiemels JL (2008) Adenovirus detection in Guthrie cards from paediatric leukaemia cases and controls. Br J Cancer. Nov 18; 99(10):1668-72. PMID: 19002185. PMCID: PMC2584954. [PDF]
• Rollison DE, Howlader N, Smith MT, Strom SS, Merritt WD, Ries LA, Edwards BK, List AF (2008) Epidemiology of myelodysplastic syndromes and chronic myeloproliferative disorders in the United States, 2001-2004, using data from the NAACCR and SEER programs. Blood. Jul 1; 112(1):45-52. PMID: 18443215. [PDF]
• Metayer C, Buffler PA (2008) Residential exposures to pesticides and childhood leukaemia. Radiat Prot Dosimetry. 132(2):212-9. PMID: 18940823. [PDF]
• Colt JS, Gunier RB, Metayer C, Nishioka MG, Bell EM, Reynolds P, Buffler PA, Ward MH (2008) Household vacuum cleaners vs. the high-volume surface sampler for collection of carpet dust samples in epidemiologic studies of children. Environ Health. 7:6. PMID: 18291036. PMCID: PMC2265689. [PDF]

2007

• Chang JS, Metayer C, Fear NT, Reinier K, Yin X, Urayama K, Russo C, Jolly KW, Buffler PA (2007) Parental social contact in the work place and the risk of childhood acute lymphoblastic leukaemia. Br J Cancer. Nov 5; 97(9):1315-21. PMID: 17923868. PMCID: PMC2360459: [PDF]
• Escobar PA, Smith MT, Vasishta A, Hubbard AE, Zhang L (2007) Leukaemia-specific chromosome damage detected by comet with fluorescence in situ hybridization (comet-FISH). Mutagenesis. Sep; 22(5):321-7. PMID: 17575318. [PDF]
• Zhang L, Rothman N, Li G, Guo W, Yang W, Hubbard AE, Hayes RB, Yin S, Lu W, Smith MT (2007) Aberrations in chromosomes associated with lymphoma and therapy-related leukemia in benzene-exposed workers. Environ Mol Mutagen. Jul; 48(6):467-74. PMID: 17584886. [PDF]
• Urayama KY, Wiencke JK, Buffler PA, Chokkalingam AP, Metayer C, Wiemels JL (2007) MDR1 gene variants, indoor insecticide exposure, and the risk of childhood acute lymphoblastic leukemia. Cancer Epidemiol Biomarkers Prev. Jun; 16(6):1172-7. PMID: 17548681. [PDF]
• Hegedus CM, Skibola CF, Bracci P, Holly EA, Smith MT (2007) Screening the human serum proteome for genotype-phenotype associations: An analysis of the IL6 -174G>C polymorphism. Proteomics. Feb;7(4):548-57. PMID: 17309100. [PDF]
• Kwan ML, Metayer C, Crouse V, Buffler PA (2007) Maternal illness and drug/medication use during the period surrounding pregnancy and risk of childhood leukemia among offspring. Am J Epidemiol. Jan 1; 165(1):27-35. PMID: 17035343. [PDF]
• Lin YS, Vermeulen R, Tsai CH, Waidyanatha S, Lan Q, Rothman N, Smith MT, Zhang L, Shen M, Li G, Yin S, Kim S, Rappaport SM (2007) Albumin adducts of electrophilic benzene metabolites in benzene-exposed and control workers. Environ Health Perspect. Jan; 115(1):28-34. PMID: 17366815. PMCID: PMC1797829. [PDF]
• Chen J, van der Laan MJ, Smith MT, Hubbard AE (2007) A comparison of methods to control type I errors in microarray studies. Stat Appl Genet Mol Biol. 6:Article28. PMID: 18052911. [PDF]

2006

• Paynter RA, Skibola DR, Skibola CF, Buffler PA, Wiemels JL, Smith MT (2006) Accuracy of multiplexed Illumina platform-based single-nucleotide polymorphism genotyping compared between genomic and whole genome amplified DNA collected from multiple sources. Cancer Epidemiol Biomarkers Prev. Dec; 15(12):2533-6. PMID: 17164381. [PDF]
• Chang JS, Selvin S, Metayer C, Crouse V, Golembesky A, Buffler PA (2006) Parental smoking and the risk of childhood leukemia. Am J Epidemiol. Jun 15; 163(12):1091-100. PMID: 16597704. [PDF]
• Aldrich MC, Zhang L, Wiemels JL, Ma X, Loh ML, Metayer C, Selvin S, Feusner J, Smith MT, Buffler PA (2006) Cytogenetics of Hispanic and White children with acute lymphoblastic leukemia in California. Cancer Epidemiol Biomarkers Prev. Mar; 15(3):578-81. PMID: 16537719. [PDF]
• Birkner MD, Hubbard AE, van der Laan MJ, Skibola CF, Hegedus CM, Smith MT (2006) Issues of processing and multiple testing of SELDI-TOF MS proteomic data. Stat Appl Genet Mol Biol. 5:Article11. PMID: 16646865. [PDF]

2005

• Hegedus CM, Gunn L, Skibola CF, Zhang L, Shiao R, Fu S, Dalmasso EA, Metayer C, Dahl GV, Buffler PA, Smith MT (2005) Proteomic analysis of childhood leukemia. Leukemia. Oct; 19(10):1713-8. PMID: 16136170. [PDF]
• Smith MT, McHale CM, Wiemels JL, Zhang L, Wiencke JK, Zheng S, Gunn L, Skibola CF, Ma X, Buffler PA (2005) Molecular biomarkers for the study of childhood leukemia. Toxicol Appl Pharmacol. Aug 7; 206(2):237-45. PMID: 15967214. [PDF]
• Rappaport SM, Waidyanatha S, Yeowell-O’Connell K, Rothman N, Smith MT, Zhang L, Qu Q, Shore R, Li G, Yin S (2005) Protein adducts as biomarkers of human benzene metabolism. Chem Biol Interact. May 30; 153-154(103-9. PMID: 15935805. [PDF]
• Zhang L, Yang W, Hubbard AE, Smith MT (2005) Nonrandom aneuploidy of chromosomes 1, 5, 6, 7, 8, 9, 11, 12, and 21 induced by the benzene metabolites hydroquinone and benzenetriol. Environ Mol Mutagen. May; 45(4):388-96. PMID: 15662717. [PDF]
• Wiemels JL, Zhang Y, Chang J, Zheng S, Metayer C, Zhang L, Smith MT, Ma X, Selvin S, Buffler PA, Wiencke JK (2005) RAS mutation is associated with hyperdiploidy and parental characteristics in pediatric acute lymphoblastic leukemia. Leukemia. Mar; 19(3):415-9. PMID: 15674422. [PDF]
• Buffler PA, Kwan ML, Reynolds P, Urayama KY (2005) Environmental and genetic risk factors for childhood leukemia: appraising the evidence. Cancer Invest. 23(1):60-75. PMID: 15779869. [PDF]

Book Chapters

• Gunn L, Zhang L, Smith MT (2005) Novel biomarkers: New methods for assessing acquired DNA damage in humans without cancer. Cancer Risk Assessment, edited by Shields PG. Chapter 5, pp77-97.

» Publications Archive