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1 Oral Health Outcomes As Potential Indicators Of ORAL HEALTH OUTCOMES AS POTENTIAL INDICATORS OF CANCER EXPERIENCE by Mariana Bezamat Coutinho Lucas Doctor of Dental Surgery, Federal University of Rio de Janeiro, 2013 Submitted to the Graduate Faculty of the School of Dental Medicine in partial fulfillment of the requirements for the degree of Doctor of Philosophy University of Pittsburgh 2021 1 Committee Page UNIVERSITY OF PITTSBURGH SCHOOL OF DENTAL MEDICINE This dissertation was presented by Mariana Bezamat Coutinho Lucas It was defended on January 22, 2021 and approved by Dobrawa Napierala, PhD, Department of Oral Biology Juan Taboas, PhD, Department of Oral Biology Adriana Modesto, DDS, MS, PhD, Department of Pediatric Dentistry Thesis Advisor/Dissertation Director: Alexandre R. Vieira, DDS, MS, PhD, Department of Oral Biology ii Copyright © by Mariana Bezamat Coutinho Lucas 2021 iii ORAL HEALTH OUTCOMES AS POTENTIAL INDICATORS OF CANCER EXPERIENCE Mariana Bezamat Coutinho Lucas, DDS, PhD University of Pittsburgh, 2021 According to an estimate from the American Cancer Society in 2018, 1,735,350 people were expected to be diagnosed with cancer in the United States, with 609,640 dying from the disease. The late diagnosis of cancer has a negative impact on the health care system due to higher treatment cost and decreased chances of favorable prognosis. Due to the nature of their profession, dentists and their teams are well positioned to identify oral risk markers related to cancer, which increases the potential for early diagnosis and chances of survival. For example, tooth agenesis has been associated with increased risk for ovarian cancer. A greater awareness of oral conditions that are linked to genetic predictors of cancer susceptibility will provide dentists an opportunity to improve patient outcomes by suggesting genetic screenings for prevention. The objective of this study is to identify craniofacial conditions that might be risk markers for cancers by performing association studies and approaches such as a phenome-wide association study (PheWAS) including orofacial phenotypes. A PheWAS can determine if clinical traits (phenotypes) or specific diagnosis are associated with a given genetic variant. Hence, this study will evaluate if selected single nucleotide polymorphisms (SNPs) present in cell regulatory gene pathways are associated with orofacial conditions affecting the study population; determine whether there is an increased frequency of these conditions among individuals who have been diagnosed with cancer compared to healthy controls; and identify the range of head and neck conditions associated with the selected SNPs through a PheWAS approach. All samples were obtained through the Dental Registry and iv DNA Repository (DRDR) at the University of Pittsburgh, School of Dental Medicine. DNA was extracted from whole saliva using established protocols and genotyping data from over 3,000 individuals were generated using TaqMan chemistry. PLINK software was used to perform allele frequency tests and a logistic regression using R environment was performed taking covariates such as ethnicity and gender into account. We found several genetic associations with the phenotypes of interest that were later confirmed with the PheWAS approach. Additionally, novel associations that can potentially be markers of cancer risk were found. v Table of Contents Preface .......................................................................................................................................... 13 1.0 INTRODUCTION ............................................................................................. 14 1.1 Cancer Epidemiology and Potential Markers ........................................................... 14 1.2 The Role of Oral Health Professionals in Cancer Prevention .................................. 15 1.3 Precision Medicine and Phenome-Wide Scan Approach .......................................... 16 1.4 Oral Conditions, Systemic Diseases and Gene Pathways Involved ......................... 18 1.5 Hypotheses and Specific Aims ..................................................................................... 20 INVESTIGATING WHETHER VARIATION IN MTOR AND ER STRESS GENES ARE ASSOCIATED WITH ORAL AND BONE PHENOTYPES.......................... 23 2.1 FOREWORD ................................................................................................................ 23 2.2 SUBJECTS AND METHODS ..................................................................................... 23 Phenotypes and Sample Selection .....................................................................24 Dental Caries ......................................................................................................24 Periapical Lesions Due to Deep Carious Lesions in Dentin ...........................26 Periodontitis ........................................................................................................27 Osteoporosis ........................................................................................................27 Temporomandibular Joint Symptoms .............................................................28 Combined Phenotypes .......................................................................................29 Selection of Genes and Single Nucleotide Polymorphisms .............................31 Genotyping ..........................................................................................................32 Data Analyses ...................................................................................................32 vi 2.3 RESULTS ...................................................................................................................... 33 2.4 DISCUSSION ................................................................................................................ 37 2.5 ACKNOWLEDGEMENTS ......................................................................................... 40 PERFORMING AN ORAL PHENOME-WIDE SCAN IN CANCER DIAGNOSED INDIVIDUALS .................................................................................................. 41 3.1 FOREWORD ................................................................................................................ 41 3.2 SUBJECTS AND METHODS ..................................................................................... 41 Phenotype-to-phenotype analysis .....................................................................46 Genomic polymorphisms ...................................................................................46 DNA extraction ...................................................................................................47 Genotypic analysis ..............................................................................................48 Code conversion .................................................................................................48 PheWAS statistical methods and power calculation .......................................49 3.3 RESULTS ...................................................................................................................... 50 3.4 DISCUSSION ................................................................................................................ 61 3.5 ACKNOWLEDGEMENTS ......................................................................................... 67 CONCLUSIONS AND FUTURE DIRECTIONS .............................................................. 68 Appendix A .................................................................................................................................. 71 Bibliography ................................................................................................................................ 90 vii List of Tables Table 1. Definition of caries experience based on age and DMFT scores. The thresholds were defined based on the DMFT distribution in the studied group by age. ............................. 25 Table 2. Summary of results highlighting nominal (between 0.05 and 0.002) and statistically significant (equal or lower than 0.002, marked in bold) p-values for association analyses between periapical lesions, periodontal disease, osteoporosis, dental caries experience, and temporomandibular joint symptoms and the evaluated markers. Assuming that D is the minor allele and d is the major allele, the allelic model compares the frequencies of each allele in each group (D x d), the genotypic model is an additive two degree of freedom model that compares the frequencies of each genotype in the groups (DD x Dd x dd), the dominant model compares the two copies of the common allele versus the other combinations (dd x DD + Dd), and the recessive model compares the two copies of the rare allele frequency versus the other combinations (DD x Dd + dd). Degrees of freedom (DF). ................................................................................................................................................... 34 Table 3. Summary of all nominal (p-values between 0.05 and 0.002) and significant results from the combined analysis of patients with caries, periodontitis and periapical lesions (bold indicates statistically significant p-values under the threshold 0.002). Assuming that D is the minor allele and d is the major allele, the allelic model compares the frequencies of each allele in each group (D x d), the genotypic model is an additive two degree of freedom model that compares the frequencies of each genotype in the groups (DD
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