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Aggressive Periodontitis Subjects in Moroccan Population

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Aggressive Periodontitis Subjects in Moroccan Population MICROBIOME ANALYSIS OF AGGREGATIBACTER ACTINOMYCETEMCOMITANS JP2 CLONE AND NON – AGGRESSIVE PERIODONTITIS SUBJECTS IN MOROCCAN POPULATION A Thesis Submitted to Temple University Graduate Board in Partial Fulfillment of the Requirements for the Degree MASTER OF SCIENCE IN ORAL HEALTH SCIENCES by Vijaya Lakshmi Pavani Molli, BDS May, 2021 Thesis Committee: Jasim M. Albandar, DMD, PhD, Committee Chair Department of Periodontology and Oral Implantology Nezar N. Al-Hebshi, BDS, PhD, Committee Member Department of Oral Health Sciences Sumant Puri, PHD, Committee Member Department of Oral Health Sciences ABSTRACT Objectives: Earlier reports suggested that aggressive periodontitis is common in certain African populations and is associated with the JP2 clone of Aggregatibacter actinomycetemcomitans (Aa). There are few studies that investigated the type of microorganisms that colonize the subgingival sites in young subjects inflicted with a subcategory of aggressive periodontitis that is associated with the Aa-JP2 clone. Hence, the objective of this study was to characterize the subgingival microbiome of JP2 clone-associated aggressive periodontitis. Methods: The study subjects were drawn from a large survey among 14-18 years old schoolchildren in Morocco. The sample included 7 JP2-positive aggressive periodontitis subjects and 14 JP2-negative controls. The controls were selected to be either JP2-positive, JP2-negative (but Aa positive), or Aa- negative. Subgingival samples from these subjects were sequenced for the V1- V3 region (16S rRNA gene) on a Miseq platform. High-quality, non-chimeric merged reads were classified with our previously reported BLASTn-algorithm. Downstream analysis was performed with QIIME and LEfSe. Results: There were no significant differences between the groups in species richness. However, aggressive periodontitis subjects showed significantly lower alpha diversity. The microbiomes of aggressive periodontitis clustered distinctively from the controls. However, there was no significant separation between the subgroups of the control group. Species associated with health ii included Streptococcus spp., Haemophilus spp., Neisseria spp., Gemella spp., Rothia spp., Fusobacterium nucleatum subsp. polymorphum, Porphyromonas oral taxon 279, Veillonella parvula, Granulicatella adiacens and Lautropia mirabilis. Important periodontal pathogens, including Treponema spp., Fretibacterium spp. P. gingivalis and Tannerella forsythia were significantly enriched in aggressive periodontitis subjects. However, the taxa detected in high abundance and showed strongest association with aggressive periodontitis but not the controls were Pseudomonas oral taxon C61 and Enterobacter cloacae. Conclusions: The results suggest that several periodontal pathogens involved in chronic periodontitis also play a role in aggressive periodontitis. Future studies should investigate the role of Pseudomonas and Enterobacter spp. in the pathogenesis of aggressive periodontitis. iii ACKNOWLEDGEMENTS: First, I take this opportunity to thank my mentor Dr. Jasim M. Albandar for accepting me as one of his students. It was indeed a dream come true and I learnt a lot through this journey. I will always be indebted to him for this opportunity. Second, I also want to thank Dr. Nezar Al-Hebshi for providing me with a working space in in his research lab and for his constant encouragement, support, help and guidance for my thesis. Third, I also thank Dr. Sumant Puri for reviewing my thesis and sharing his thoughts about my work. I want to thank my dear friend Dr. Divyasri Baraniya for her help all through my master’s thesis project. I also want to thank my husband, my parents, and my in-laws for their constant support throughout my journey. I want to thank Dr. Dimaira, Dr. Chialastri, and all faculty at the Department of Periodontology and Oral Implantology, Temple University School of Dentistry for their support towards my thesis. Last but not the least, I want to thank my co residents for their encouragement. iv TABLE OF CONTENTS Page ABSTRACT… ...................................................... ……………………………………ii ACKNOWLEDGEMENTS……………………………………………………...………iv LIST OF TABLES………………………………………………………………………vii LIST OF FIGURES ……….…………… ........................ ……………………….…. viii 1.INTRODUCTION…………………………………………………….………….…….1 Objectives………………………………………………………………………..4 2. MATERIALS AND METHODS ……….…………… ...... ……………………….….5 Study Population………………………………………………………………...5 Plaque Sample Collection. ...................................................................... …6 Bacterial DNA extraction……………………………………………………….6 Quantitative Real-Time Polymerase Chain Reaction……………………….8 Microbiome Analysis ………………………………………………………….8 Data Statistical Analysis……………………………………………………….9 3. RESULTS ................. ………………………………………………………………12 4. DISCUSSION…………………… ........... ……………………….. ………. …… .20 5. CONCLUSIONS………………………… .... ………………………………………25 v 6.LIMITATIONS……………………………………………………………………….26 7.FUTURE DIRECTION......................................................................................27 REFERENCES CITED……………………………………………………...………..28 8. APPENDIX…………………………………………………………………………..36 ADDITIONAL FIGURES………………………………………………………..36 vi LIST OF TABLES Table Page 1. Periodontal status of study subjects……………………………………………13 2. PCR analysis of the samples based on the gel image……………………….15 vii LIST OF FIGURES Figure Page 1. PCR Analysis…………………………………………………………………………14 2. Bacteriome profile: Stacked bar plots showing the distribution of microbial phyla that were detected in the 3 study groups………………………………… ……….36 3. Bacteriome profile: Stacked bar plots showing the distribution of the top 15 genera that were detected in the 3 study groups………………………………….37 4. Bacteriome profile: Stacked bar plots showing the distribution of top 15 microbial species that were detected in the 3 study groups…………………………………38 5. (A) Alpha diversity indices and (B) Principal component analysis (PCOA) for shallow, deeper pocket group and control group. * P ≤ 0.05……………………..39 6. Results of the linear discriminant analysis effect size (LEfSe) showing the differentially abundant taxa (LDA threshold score ≥3) for bacterial phyla (A), genera (B), and species (C) for the cases and controls…………………………..40 7. Relative abundance of Enterobacter cloacae in the study groups……………….41 8. Relative abundance of Pseudomonas _sp_ Oral _ Taxon _ C61 in the study groups…………………………………………………………………………………..42 9. Relative abundance of Treponema denticola in the study groups……………….43 10. Relative abundance of Tannerella forsythia in the study groups…………………44 11. Relative abundance of Porphyromonas gingivalis in the study groups………….45 12. Heat map analysis showing clustering of study subjects based on species that maintained significant association after adjustment for multiple comparisons….46 viii CHAPTER 1 INTRODUCTION Periodontitis encompasses a group of infectious diseases characterized by an inflammatory condition that leads to destruction of the periodontal supporting tissues, and eventually may cause loss of the teeth (Van Dyke & Serhan, 2003). Aggressive periodontitis is one type of these diseases and is characterized by disease onset at an early age. A localized form of aggressive periodontitis affects especially the molars and incisors, whereas a generalized form affects most or all teeth (Albandar, 2014). In an early report, Gottileb (Gottlieb, 1923) used the term “diffuse atrophy of the alveolar bone” to describe the disease. Gottlieb hypothesized that the disease is caused by a lack of an effective cementum barrier, which he referred to as “cementopathia”, that may lead to gingival recession, alveolar bone loss, and pathological pocket formation (Gottlieb, 1923). Orban & Weinmann later introduced the term “periodontosis” to describe severe loss of periodontal tissue in young individuals (Orban & Weinmann, 1942), and Butler introduced the term “juvenile periodontitis” (Butler, 1969). In 1989 the American Academy of Periodontology (AAP) used the term “early onset periodontitis” (American Academy of Periodontology, 1989), and in the 1999 International Workshop for a Classification of Periodontal Diseases and Conditions, a consensus report introduced the term “aggressive periodontitis” (Armitage, 1999). In the rest of this document the latter term will be used to refer to this disease. 1 The etiology of aggressive periodontitis is not well understood. Microorganisms play an important role in the initiation of the local inflammatory process which, in susceptible persons, may lead to loss of periodontal fibers and alveolar bone (Henderson & Kaiser, 2018). However, the host immune response (Ebersole et al., 2017) as well as other etiologic and risk factors (Albandar & Rams, 2002) also are important in the development and progression of this disease. The subgingival microbial flora of the pathological pocket is complex and comprises more than 400 bacterial species (Bosshardt, 2018; Faveri et al., 2008; Paster et al., 2001; Paster, Olsen, Aas, & Dewhirst, 2006). It has been hypothesized that the pathogenesis of periodontitis involves an imbalance in subgingival microbial community’s composition and function (dysbiosis) (Kilian et al., 2016) and where certain periodontal pathogens subvert the leukocytes and break microbial hemostasis (normobiosis), thereby inducing a dysbiotic community that may elicit the destructive immunologic reaction observed in periodontitis (Hajishengallis & Lamont, 2012). Among the diverse microbiota of the subgingival dental
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