Effects of Electronic Cigarette Use on the Human Lung
Little is known about the potential benefits of e-cigs for fostering smoking cessation and the numerous types of harm that they could cause, both on an individual level and a population basis. The Food and Drug Administration (FDA) Center for Tobacco Products current research priorities include the study of e-cigs use and toxicity. To make sound policy about e-cigs, regulators need data about toxicity in humans, as well as use in youth, former smokers and others.
The aims of this study are:
- To conduct a pilot cross-sectional study of e-cig users, never smokers, former smokers and smokers to better determine the influence of e-cig and smoking use between never smokers and e-cig users, and to compare former smokers with e-cig use and assessing use patterns and biomarkers by bronchoscopies using bronchioalveolar lavage and bronchial brushings
- To conduct a supplemental contamination study to measure if bacteria from oral cavity, nasal cavity or oropharynx may contaminate BAL fluid recovered during the bronchoscopy
- To conduct a four-week pilot clinical trial of nicotine-free and flavor-free e-cig use in never-smokers and assess biomarkers as in Aim 1 by bronchoscopy at baseline and at four weeks while on product (week five of trial)
Selected Publications
1. Accelerated epigenetic age, inflammation, and gene expression in lung: comparisons of smokers and vapers with non-smokers. Song MA, Mori KM, McElroy JP, Freudenheim JL, Weng DY, Reisinger SA, Brasky TM, Wewers MD, Shields PG. Clin Epigenetics. 2023 Oct 11;15(1):160. doi: 10.1186/s13148-023-01577-8. PMID: 37821974
2. Sex-specific lung inflammation and mitochondrial damage in a model of electronic cigarette exposure in asthma. Song MA, Kim JY, Gorr MW, Miller RA, Karpurapu M, Nguyen J, Patel D, Archer KJ, Pabla N, Shields PG, Wold LE, Christman JW, Chung S. Am J Physiol Lung Cell Mol Physiol. 2023 Nov 1;325(5):L568-L579. doi: 10.1152/ajplung.00033.2023. Epub 2023 Sep 12. PMID: 37697923
3. A Pilot Cross-Sectional Study of Immunological and Microbiome Profiling Reveals Distinct Inflammatory Profiles for Smokers, Electronic Cigarette Users, and Never-Smokers. Shields PG, Ying KL, Brasky TM, Freudenheim JL, Li Z, McElroy JP, Reisinger SA, Song MA, Weng DY, Wewers MD, Whiteman NB, Yang Y, Mathé EA. Microorganisms. 2023 May 26;11(6):1405. doi: 10.3390/microorganisms11061405. PMID: 37374908
4. Long-Term Impact of Daily E-cigarette Exposure on the Lungs of Asthmatic Mice. Song MA, Wold LE, Aslaner DM, Archer KJ, Patel D, Jeon H, Chung D, Shields PG, Christman JW, Chung S. Nicotine Tob Res. 2023 Nov 22;25(12):1904-1908. doi: 10.1093/ntr/ntad100. PMID: 37349133
5. Lung mitochondrial DNA copy number, inflammatory biomarkers, gene transcription and gene methylation in vapers and smokers. Mori KM, McElroy JP, Weng DY, Chung S, Fadda P, Reisinger SA, Ying KL, Brasky TM, Wewers MD, Freudenheim JL, Shields PG, Song MA. EBioMedicine. 2022 Nov;85:104301. doi: 10.1016/j.ebiom.2022.104301. Epub 2022 Oct 7. PMID: 36215783
6. Saliva and Lung Microbiome Associations with Electronic Cigarette Use and Smoking. Ying KL, Brasky TM, Freudenheim JL, McElroy JP, Nickerson QA, Song MA, Weng DY, Wewers MD, Whiteman NB, Mathe EA, Shields PG. Cancer Prev Res (Phila). 2022 Jul 5;15(7):435-446. doi: 10.1158/1940-6207.CAPR-21-0601. PMID: 35667088
7. Lipid-Laden Macrophages and Electronic Cigarettes in Healthy Adults. Shields PG, Song MA, Freudenheim JL, Brasky TM, McElroy JP, Reisinger SA, Weng DY, Ren R, Eissenberg T, Wewers MD, Shilo K. EBioMedicine. 2020; DOI:10.1016/j.ebiom.2020.102982.
8. Vitamin E Acetate in Bronchoalveolar-Lavage Fluid Associated With EVALI. Blount BC, Karwowski MP, Shields PG, Morel-Espinosa M, Valentin-Blasini L, Gardner M, Braselton M, Brosius CR, Caron KT, Chambers D, Corstvet J, Cowan E, De Jesús VR, Espinosa P, Fernandez C, Holder C, Kuklenyik Z, Kusovschi JD, Newman C, Reis GB, Rees J, Reese C, Silva L, Seyler T, Song MA, Sosnoff C, Spitzer CR, Tevis D, Wang L, Watson C, Wewers MD, Xia B, Heitkemper DT, Ghinai I, Layden J, Briss P, King BA, Delaney LJ, Jones CM, Baldwin GT, Patel A, Meaney-Delman D, Rose D, Krishnasamy V, Barr JR, Thomas J, Pirkle JL. The New England Journal of Medicine. 2020; 382(8):697-705; DOI: 10.1056/NEJMoa1916433.
9. Biomarkers of Exposure and Effect in the Lungs of Smokers, Nonsmokers, and Electronic Cigarette Users. Song MA, Freudenheim JL, Brasky TM, Mathe EA, McElroy JP, Nickerson QA, Reisinger SA, Smiraglia DJ, Weng DY, Ying KL, Wewers MD, Shields PG. Cancer Epidemiol Biomarkers Prev. 2020; 29(2) 443-451; DOI: 10.1158/1055-9965.EPI-19-1245
10. Effects of Electronic Cigarette Constituents on the Human Lung: A Pilot Clinical Trial. Song MA, Reisinger SA, Freudenheim JL, Brasky TM, Mathé EA, McElroy JP, Nickerson QA, Weng DY, Wewers MD, Shields PG. Cancer Prevention Research. 2020; 13(2):145-152; DOI: 10.1158/1940-6207.CAPR-19-0400
11. Electronic versus Combustible Cigarette Effects on Inflammasome Component Release into Human Lung. Tsai M, Song MA, McAndrew C, Brasky TM, Freudenheim JL, Mathé E, McElroy JP, Reisinger SA, Shields PG, Wewers MD. Am J Respir Crit Care Med. 2019; 199:922-925.
12. Electronic Cigarettes and the Lung Proteome. Shields PG, Song MA, Freudenheim JL, Brasky TM, Mathe E, McElroy JP, Hummon AB, Wewers MD. Am J Respir Crit Care Med. 2018; 198:1350-1351.
13. Sex-related DNA methylation is associated with inflammation and gene expression in the lungs of healthy individuals. Patel D, McElroy JP, Weng DY, Sahar K, Reisinger SA, Freudenheim JL, Wewers MD, Shields PG, Song MA. Sci Rep. 2024 Jun 20;14(1):14280. doi: 10.1038/s41598-024-65027-y. PMID: 38902313
The Effects of a Standardized Research E-Cigarette on the Human Lung: A Clinical Trial With Bronchoscopic Biomarkers
The use of electronic cigarettes (e-cigs) is increasing rapidly. Yet little is known about the potential lung toxicity for inhaling e-cig aerosols relative to smoking. The Food and Drug Administration (FDA) has deemed regulatory authority over e-cigs and needs data to determine how to regulate their designs and constituents. In this project, we can take advantage of a new opportunity using the newly released National Institute on Drug Abuse (NIDA) standardized research e-cig (SREC) because this is a product that will likely not change over time subject to marketing and manufacturing influences, and allows for comparisons across studies. The primary aim of this study is to assess pulmonary effects of e-cig use in a randomized clinical trial of 160 smokers, some of whom will be provided the SREC for 10 weeks assessing biomarkers obtained by bronchoscopy (bronchoalveolar lavage [BAL] and lung brushings).
Consortium on Methods Evaluating Tobacco (COMET): Filter Ventilation and Product Standards
To date, no systematic and comprehensive study has been conducted to determine the effects of switching smokers from ventilated to unventilated cigarettes on a broad range of biomarkers of tobacco-related exposure and harm and on toxicity, appeal and abuse liability. The primary aim of this project is to examine the effects of ventilated vs. unventilated cigarettes on biomarkers of exposure and harm and smoking behaviors in the context of no availability of ANDS vs. availability of non-combusted ANDS using an experimental marketplace. A secondary aim includes determining predictors of amount of study cigarettes that are smoked and levels of exposure biomarkers. These predictors include type of cigarettes, health risk and subjective responses to the cigarette, the availability and amount of use of alternative products as well as smoking history and demographic variables. Another secondary aim includes examining the characteristics of ANDS chosen (e.g. type of product, flavors and nicotine dose) among smokers assigned to the experimental marketplace with ANDS and subjective responses and pattern of use of these products.
The bronchoscopy study includes a subgroup of smokers who undergo bronchoscopy. This study will focus on biomarkers measured in the lung by bronchoscopy and are markers of effect, allowing us to consider exposures at the target organ level.
Selected Publications
1. Cigarette Filter Ventilation and its Relationship to Increasing Rates of Lung Adenocarcinoma.
2. Song MA, Benowitz NL, Berman M, Brasky TM, Cummings KM, Hatsukami DK, Marian C, O'Connor R, Rees VW, Woroszylo C, Shields PG. J Natl Cancer Inst. 2017 Dec 1;109(12):djx075. doi: 10.1093/jnci/djx075. PMID: 28525914
3. Impact of Cigarette Filter Ventilation on U.S. Smokers' Perceptions and Biomarkers of Exposure and Potential Harm. Carroll DM, Stepanov I, O'Connor R, Luo X, Cummings KM, Rees VW, Bickel WK, Berman ML, Ashley DL, Bansal-Travers M, Shields PG, Hatsukami DK. Cancer Epidemiol Biomarkers Prev. 2021 Jan;30(1):38-44. doi: 10.1158/1055-9965.EPI-20-0852. Epub 2020 Oct 22. PMID: 33093163
4. Is perception reality? Associations among "light" cigarettes and number of cigarettes smoked per day. Freitas-Lemos R, Tegge AN, Athamneh LN, Yeh YH, Craft WH, Stein JS, Smith TT, Stepanov I, Rees VW, Cummings KM, O'Connor RJ, Shields PG, Hatsukami DK, Bickel WK. Drug Alcohol Depend. 2023 Mar 1;244:109709. doi: 10.1016/j.drugalcdep.2022.109709. Epub 2023 Jan 13. PMID: 36642000
5. The experimental tobacco marketplace: Effects of low-ventilated cigarette exposure. Freitas-Lemos R, Tegge AN, Stein JS, DeHart WB, Reisinger SA, Shields PG, Hatsukami DK, Bickel WK. Addict Behav. 2022 Feb;125:107160. doi: 10.1016/j.addbeh.2021.107160. Epub 2021 Oct 19. PMID: 34710841
6. Risk perceptions and continued smoking as a function of cigarette filter ventilation level among US youth and young adults who smoke. Carroll DM, Tessier KM, Cummings KM, O'Connor RJ, Reisinger S, Shields PG, Stepanov IS, Luo X, Hatsukami DK, Rees VW. Tob Control. 2023 Jul;32(4):473-479. doi: 10.1136/tobaccocontrol-2021-056833. Epub 2021 Dec 2. PMID: 34857645
7. Switching to cigarette brand variants with different filter ventilation levels: a descriptive analysis. Carroll DM, Tessier K, Luo X, Stepanov IS, Shields PG, O'Connor R, Rees VW, Cummings M, Bickel W, Hatsukami D. Tob Control. 2023 Jan 23:tobaccocontrol-2022-057571. doi: 10.1136/tc-2022-057571. PMID: 36690447
8. Illegal product purchasing in the experimental tobacco marketplace: Effects of menthol cigarette and cigarette ventilation ban. Freitas-Lemos R, Tegge AN, Tomlinson DC, Yeh YH, Stein JS, Michael Cummings K, Fong GT, Shields PG, Hatsukami DK, Bickel WK. Drug Alcohol Depend. 2023 Dec 1;253:111015. doi: 10.1016/j.drugalcdep.2023.111015. Epub 2023 Oct 31. PMID: 37951005 Clinical Trial.
9. Estimating the causal effect of filter ventilation levels in cigarettes on past 30-day smoking. Eaton AA, Hatsukami DK, Stepanov I, Shields PG, Carroll DM. Nicotine Tob Res. 2024 Aug 3:ntae191. doi: 10.1093/ntr/ntae191. Online ahead of print. PMID: 39096265
Beating Lung Cancer in Ohio (BLCIO)
Beating Lung Cancer in Ohio is a statewide clinical trial funded by Pelotonia and the Ohio State University Comprehensive Cancer Center aimed at giving more advanced-stage lung cancer patients access to advanced genomic and immunotherapy testing (AGIT) that can guide treatment decisions. Information provided by the AGIT may inform treatment decisions and identify potential new treatments available that target specific cancer-causing genetic mutations that do a better job at controlling the cancer with fewer side effects. The study also connects patients and their household members with smoking cessation support services. The OSUCCC – James has partnered with more than 50 community hospitals with the end goal of ensuring that all newly diagnosed, stage IV lung cancer patients in the state of Ohio get baseline AGIT so that they can get the treatment most likely to control their specific cancer – whether that be a targeted drug therapy, a new clinical trial treatment or a more standard chemotherapy drug. This initiative also examines the impact on survival and quality of life for smokers and recent quitters receiving centralized cessation counseling by telephone.
Pelotonia provides critical funding for many research projects at the OSUCCC. For more information on Pelotonia and how it is changing the world through mobilizing communities and accelerating funding for innovative cancer research, visit https://pelotonia.org.
Selected Publications
1. Anxiety and Depressive Symptoms in Patients with Advanced Lung Cancer. Blevins TR, Lo SB, Coker CA, Arrato NA, Reisinger SA, Shields PG, Andersen BL. COVID-19 or Cancer Stress? Int J Behav Med. 2024 Apr;31(2):325-330. doi: 10.1007/s12529-023-10206-w. Epub 2023 Aug 18. PMID: 37594667.
2. Depression in association with neutrophil-to-lymphocyte, platelet-to-lymphocyte, and advanced lung cancer inflammation index biomarkers predicting lung cancer survival. Andersen BL, Myers J, Blevins T, Park KR, Smith RM, Reisinger S, Carbone DP, Presley CJ, Shields PG, Carson WE. (2023) PLoS One. 2023 Feb 24;18(2):e0282206. doi: 10.1371/journal.pone.0282206. PMID: 36827396; PMCID: PMC9956881.
3. Evaluating the implications of allostatic load on overall mortality among patients with metastatic non-small cell lung cancer. Obeng-Gyasi, S., Reisinger, S., Li, Y., Carson, W.E., Presley, C.J., Shields, P.G., Carbone, D.P., Ceppa, D.P., Carlos, R.C., Andersen, B.L. (2022). JAMA Network Open. 5(7):e2221626. doi:10.1001/jamanetworkopen.2022.21626
4. Tense and release: Improving standard of care with Progressive Muscle Relaxation for patients with advanced lung cancer. Arrato, N.A., Lo, S.B., Grogan, M.M., Andersen, B.L., & Presley, C.J. (2022). Journal of Cancer Rehabilitation, 5, 69-76. doi: 10.48252/JCR65
5. Cancer Treatment During COVID-19: Resilience of Individuals with Advanced Non-small Cell Lung Cancer versus Community Controls. Arrato, N.A., Lo, S.B., Coker, C.A., Covarrubias, J.J., Blevins, T.R., Reisinger, S.A., Presley, C.J., Shields, P.G., & Andersen, B.A. (2022). JNCCN, 20(2): 118-125. doi: 10.6004/jnccn.2021.7076
6. Illness perception profiles and psychological and physical symptoms in newly diagnosed advanced non-small cell lung cancer. Valentine TR, Presley CJ, Carbone DP, Shields PG, Andersen BL (2022). Health Psychol. 2022 Jun;41(6):379-388. doi: 10.1037/hea0001192. PMID: 35604701. doi: 10.1037/hea0001192
7. Psychological Symptom Trajectories and Non-Small Cell Lung Cancer Survival: A Joint Model Analysis. Andersen, B.L., McElroy, J., Carbone, D.P., Presley, C.J., Shields, P.G., & Brock, G.N. (2022). Psychosom Med, 84(2): 215-223. doi: 10.1097/PSY.0000000000001027
8. Checkpoint inhibitor immunotherapy toxicity and overall survival among older adults with advanced cancer. Johns, A., Wei, L., Grogan, M., Hoyd, R., Bridges, J., Patel, S., Li, M., Husain, M., Kendra, K., Otterson, G., Burkart, J., Rosko, A., Andersen, B.L, Carbone, D., Owen, D., Spakowicz, D., & Presley, C.J. (2021). Journal of Geriatric Oncology, 12(5), 813-819. doi: 10.1016/j.jgo.2021.02.002
9. Functional Trajectories and Resilience Among Adults With Advanced Lung Cancer. Presley CJ, Arrato NA, Shields PG, Carbone DP, Wong ML, Benedict J, Reisinger SA, Han L, Gill TM, Allore H, Andersen BL, Janse S. (2021) JTO Clin Res Rep. 2022 May 17;3(6):100334. doi: 10.1016/j.jtocrr.2022.100334.
10. Functional Disability among Older vs Younger Adults with Advanced Non-Small Cell Lung Cancer. Presley, C.J., Arrato, N.A., Janse, S., Shields, P.G., Carbone, D.P., Wong, M.L., Han, L., Gill, T.M., Allore, H., & Andersen, B.L. (2021). Journal of Oncology Practice, e848-e858. doi: 10.1200/OP.20.01004
11. Newly diagnosed patients with advanced non-small cell lung cancer: A clinical description of those with moderate to severe depressive symptoms. Andersen, B.L., Valentine, T.R., Lo, S.B., Carbone, D.P., Presley, C.J., Shields, P.G. (2020). Lung Cancer, 145: 195-204. doi: 10.1016/j.lungcan.2019.11.015
Ohio State University Center of Excellence in Regulatory Tobacco Science (OSU-CERTS)
At Ohio State, Dr. Shields and Dr. Mary Ellen Wewers (College of Public Health) co-led the Tobacco Center of Regulatory Science, a five-year, 18 million dollar co-lead grant from the National Cancer Institute. This grant established the OSU-CERTS, which was one of 14 Centers of Regulatory Science (TCORS) established as part of an NIH/FDA collaboration designed to generate research regarding the regulation of tobacco products, protect public health and train the next generation of tobacco regulatory scientists.
Along with serving as co-PI of the grant, Dr. Shields’ project, closely linked with another project directed by Dr. Amy Ferketich (College of Public Health), focuses on the dual use of cigarette smoking and smokeless tobacco among adolescent males in Ohio. Researchers studied tobacco use, the way these affect how quickly adolescents and young adults develop addictions, what their toxic exposures are and the genetics that make them more susceptible to addiction. Information from this large study will help FDA decision-making about what restrictions, if any, to place on the marketing of tobacco products in the context of youth initiation and dual use. It assists with the regulation of tobacco marketing and promotion, with the decision to target health-related communications to adolescents susceptible to dual use, the development of product standards related to exposures and flavorings and the development of better tests to identify tobacco-related health risks.
Selected Publications
1. Untargeted Metabolomics and Body Mass in Adolescents: A Cross-Sectional and Longitudinal Analysis. Singh A, Kinnebrew G, Hsu PC, Weng DY, Song MA, Reisinger SA, McElroy JP, Keller-Hamilton B, Ferketich AK, Freudenheim JL, Shields PG. Metabolites. 2023 Jul 30;13(8):899. doi: 10.3390/metabo13080899. PMID: 37623843
2. Characteristics of the Tobacco User Adult Cohort in Urban and Rural Ohio. Brasky TM, Hinton A, Doogan NJ, Cooper SE, Nagaraja HN, Xi W, Shields PG, Wewers ME.Tob Regul Sci. 2018 Jan;4(1):614-630. doi: 10.18001/TRS.4.1.8. Epub 2018 Jan 1.PMID: 29862311
Discovery of Biomarkers for Breast Cancer Risk Using Genome-Wide Approaches
Dr. Shields' research focuses on gene-environment interactions for breast cancer risk, with an emphasis on toxicology and carcinogenesis. The researchers study the effects of nutrition, alcohol drinking and other lifestyle factors in the breast using various biomarkers such as nutrients, hormone-like adipokines and IGFs, markers of differentiation and proliferation, and Omics technologies including gene expression, microRNA expression and DNA methylation.
Selected Publications
1. Basree MM, Shinde N, Koivisto C, Cuitino M, Kladney R, Zhang J, Stephens J, Palettas M, Zhang A, Kim HK, Acero-Bedoya S, Trimboli A, Stover DG, Ludwig T, Ganju R, Weng DY, Shields PG, Freudenheim J, Leone GW, Sizemore GM, Majumder S, Ramaswamy B. Abrupt Involution Induces Inflammation, Estrogenic Signaling and Hyperplasia Linking Lack of Breastfeeding With Increased Risk of Breast Cancer. Breast Cancer Res. 2019; 21:80
2. Taslim C, Weng DY, Brasky TM, Dumitrescu RG, Huang K, Kallakury BV, Krishnan S, Llanos AA, Marian C, McElroy J, Schneider SS, Spear SL, Troester MA, Freudenheim JL, Geyer S, Shields PG. Discovery and Replication of microRNAs for Breast Cancer Risk Using Genome-Wide Profiling. Oncotarget. 2016; 7:86457-86468.
3. Song MA, Brasky TM, Marian C, Weng DY, Taslim C, Llanos AA, Dumitrescu RG, Liu Z, Mason JB, Spear SL, Kallakury BV, Freudenheim JL, Shields PG. Genetic Variation in One-Carbon Metabolism in Relation to Genome-Wide DNA Methylation in Breast Tissue From Heathy Women. Carcinogenesis. 2016; 37:471-480.
4. Song MA, Brasky TM, Marian C, Weng DY, Taslim C, Dumitrescu RG, Llanos AA, Freudenheim JL, Shields PG. Racial Differences in Genome-Wide Methylation Profiling and Gene Expression in Breast Tissues From Healthy Women. Epigenetics. 2015; 10:1177-1187.
5. Roy S, Brasky TM, Belury MA, Krishnan S, Cole RM, Marian C, Yee LD, Llanos AA, Freudenheim JL, Shields PG. Associations of Erythrocyte ω-3 Fatty Acids With Biomarkers of ω-3 Fatty Acids and Inflammation in Breast Tissue. Int J Cancer. 2015; 137:2934-2946.
6. Llanos AA, Marian C, Brasky TM, Dumitrescu RG, Liu Z, Mason JB, Makambi KH, Spear SL, Kallakury BV, Freudenheim JL, Shields PG. Associations Between Genetic Variation in One-Carbon Metabolism and LINE-1 DNA Methylation in Histologically Normal Breast Tissues. Epigenetics. 2015; 10:727-735.
7. Llanos AA, Dumitrescu RG, Brasky TM, Liu Z, Mason JB, Marian C, Makambi KH, Spear SL, Kallakury BV, Freudenheim JL, Shields PG. Relationships Among Folate, Alcohol Consumption, Gene Variants in One-Carbon Metabolism and p16INK4a Methylation and Expression in Healthy Breast Tissues. Carcinogenesis. 2015; 36:60-67.
Lifestyle, Genetics and Other Exposures Associated With Breast Cancer Risk
Dr. Shields' work includes major collaborations with Dr. Jo Freudenheim at the University of Buffalo and the Roswell Park Cancer Institute, Dr. Christine Ambrosone at Roswell Park Cancer Institute and Dr. Catalin Marian at the University of Medicine and Pharmacy of Timisoara in the Western New York Exposures and Breast Cancer Study, which have yielded over 40 publications discovering the causes of breast cancer and those with increased risk due to lifestyle and other causes like genetics.
Selected Publications
1. Callahan CL, Bonner MR, Nie J, Wang Y, Tao MH, Shields PG, Marian C, Eng KH, Trevisan M, Freudenheim JL. Active and Secondhand Smoke Exposure Throughout Life and DNA Methylation in Breast Tumors. Cancer Causes Control. 2019; 30:53-62.
2. Vaughn CB, Freudenheim JL, Nie J, Sucheston-Campbell L, Wactawski-Wende J, Marian C, Shields PG, Kallakury BV, Trevisan M, Ochs-Balcom HM. Sleep and Breast Cancer in the Western New York Exposures and Breast Cancer (WEB) Study. J Clin Sleep Med. 2018; 14:81-86.
3. Callahan CL, Bonner MR, Nie J, Han D, Wang Y, Tao MH, Shields PG, Marian C, Eng KH, Trevisan M, Beyea J, Freudenheim JL. Lifetime exposure to Ambient Air Pollution and Methylation of Tumor Suppressor Genes in Breast Tumors. Environ Res. 2018; 161:418-424.
4. Callahan CL, Wang Y, Marian C, Weng DY, Eng KH, Tao MH, Ambrosone CB, Nie J, Trevisan M, Smiraglia D, Edge SB, Shields PG, Freudenheim JL. DNA Methylation and Breast Tumor Clinicopathological Features: The Western New York Exposures and Breast Cancer (WEB) Study. Epigenetics. 2016; 11:643-652.