DEAN GIANNOBILE AT HSDM

Nov – Dec 2020 RESEARCH BULLETIN

DEAN GIANNOBILE ESTABLISHES LAB AT HSDM

William Giannobile, DDS, MS, DMSc, dean of HSDM and professor of Oral Medicine, Infection and Immunity, has established his research laboratory on the fourth floor of the REB building.

Dean Giannobile has maintained a continuously NIH-funded research program over the past 25 years, and serves as co-principal investigator for the NIDCR-supported Michigan-Pittsburgh-Wyss Regenerative Medicine Resource Center. The goal of the Center is to translate early stage dental, oral, and craniofacial reconstructive technologies into clinical practice.

He has produced over 300 manuscripts, textbook chapters, and patents focused on periodontology, regenerative medicine, and oral health research. Dr. Giannobile recently completed a 10-year term as the Editor-in-Chief for the Journal of Dental Research, the official journal of the International Association for Dental Research. He serves as a consultant to the U.S. Food and Drug Administration for dental devices, and Associate Editor for the upcoming Surgeon General’s Report on Oral Health – 2021.

His current lab has funded projects on bone anabolic agents for rebuilding bone around teeth and dental implants, gene delivery approaches to accelerate dental implant osseointegration, and precision medicine work for patient stratification by genetic and epigenetic methods via saliva diagnostics. Much of this work involves both translational research and clinical research approaches to better diagnose and treat patients through implementation of human clinical trials.

Jim Sugai is the senior research laboratory specialist in the Giannobile Lab at the University of Michigan Department of Periodontics and Oral Medicine. Jim will provide remote oversight of the Giannobile Lab.

Shogo Maekawa, DDS, PhD, osteology research scholar and postdoctoral fellow in Oral Medicine, Infection and Immunity, will join the Lab in January 2021. Dr. Maekawa received his DDS and PhD from Tokyo Medical and Dental University (TMDU).

Prior to joining HSDM and the University of Michigan, he was a specially-appointed assistant professor in the Department of Periodontology at the TMDU, and he is currently an adjunct instructor at TMDU.

2 Research Bulletin • November – December 2020 • Harvard School of Dental Medicine

Claesen J, Spagnolo J, Ramos S, Kurita K, Byrd A, Aksenov A, Melnik A, Wong W, Wang S, Hernandez R, Donia M, Dorrestein P, Kong H, Segre J, Linington R, Fischbach M, Lemon K. A Cutibacterium acnes antibiotic modulates human skin microbiota composition in hair follicles. Science Translational Medicine 2020;12(570).

Frid P, Baraniya D, Halbig J, Rypdal V, Songstad N, Rosèn A, Berstad J, Flatø B, Alakwaa F, Gil E, Cetrelli L, Chen T, Al-Hebshi N, Nordal E, Al-Haroni M. Salivary oral microbiome of children with juvenile idiopathic arthritis: A Norwegian cross-sectional study. Frontiers in Cellular and Infection Microbiology 2020 Nov 4;10:602239.

Harris J, Hunter W, Hanna G, Treister N, Menon R. Rural patients with oral squamous cell carcinoma experience better prognosis and long-term survival. Oral Oncology 2020;111:105037.

Harshe R, Xie A, Vuerich M, Frank L, Gromova B, Zhang H, Robles R, Mukherjee S, Csizmadia E, Kokkotou E, Cheifetz A, Moss A, Kota S, Robson S, Longhi M. Endogenous antisense RNA curbs CD39 expression in Crohn’s disease. Nature Communications 2020;11(1):5894.

Lamont E, Gadkari A, Kerns K, To T, Daubert D, Kotsakis G, Bor B, He X, McLean J. Modified SHI-medium supports growth of a disease-state subgingival polymicrobial community in vitro. Molecular and Oral Microbiology 2020; Nov 11.

Machtei E, Romanos G, Kang P, Travan S, Schmidt S, Papathannasiou E, Tatarakis N, Tandlich M, LeilLiberman A, Horwitz J, Bassir S, Myneni S, Shiau H, Shapira L, Donos N, Papas A, Meyle J, Giannobile W, Papapanou P, Kim D. Repeated delivery of chlorhexidine chips for the treatment of periimplantitis: A multicenter, randomized, comparative clinical trial. Journal of Periodontology 2020; Oct 28.

Murugkar P, Collins A, Chen T, Dewhirst F. Isolation and cultivation of candidate phyla radiation Saccharibacteria (TM7) bacteria in coculture with bacterial hosts. Journal of Oral and Microbiology 2020;12(1):1814666.

Rao N, Treister N, Axtell A, Muhlbauer J, He P, Lau A, Icyda R, Heng E, Rinewalt D, McGurk S, Kennedy K, Kaneko T, Cameron D, Sroussi H. Preoperative dental screening prior to cardiac valve surgery and 90-day postoperative mortality. Journal of Cardiac Surgery 2020;35(11):2995-3003.

Rasperini G, Tavelli L, Barootchi S, McGuire M, Zucchelli G, Pagni G, Stefanini M, Wang H, Giannobile W. Interproximal attachment gain: The challenge of periodontal regeneration. Journal of Periodontology 2020; Nov 5.

PUBLICATIONSDEVELOPMENTAL BIOLOGY

Feng S, Bao L, Qiu G, Liao Z, Deng Z, Chen N, Chu Y, Luo Z, Jin Y, Li X, Yang Y, Zhao L. Observation of dendrite osteocytes of mice at different developmental stages using Ploton silver staining and phalloidin staining. Journal of Southern Medical University 2020;40(11):1656-1661.

Li X, Chen Y, Xu R, Wang Y, Jian F, Long H, Lai W. Delay in articular cartilage degeneration of the knee joint by the conditional removal of discoidin domain receptor 2 in a spontaneous mouse model of osteoarthritis. Annals of Translational Medicine 2020;8(18):1178.

Moore E, Mathews O, Yao Y, Yang Y. Prx1-expressing cells contributing to fracture repair require primary cilia for complete healing in mice. Bone 2020; Nov 11;115738.

Rai M, Brophy R, Rosen V. Molecular biology of meniscus pathology: Lessons learned from translational studies and mouse models. Journal of Orthopaedic Research 2020;38(9):1895-1904.

Schulte F, Asbeutah A, Benotti P, Wood G, Still C, Bistrian B, Hardt M, Welty F. The relationship between specialized pro-resolving lipid mediators, morbid obesity and weight loss after bariatric surgery. Science Reports 2020;10(1):20128.

Volloch V, Olsen B, Rits S. Alzheimer’s disease prevention and treatment: Case for optimism. Annals of Integrative Molecular Medicine 2020;2(1):115-130.

ORAL MEDICINE, INFECTION AND IMMUNITY

Albuquerque-Souza E, Schulte F, Chen T, Hardt M, Hasturk H, Van Dyke T, Holzhausen M, Kantarci A. Maresin-1 and Resolvin E1 promote regenerative properties of periodontal ligament stem cells under inflammatory conditions. Frontiers of Immunology 2020;11:585530.

Bensadoun R, Epstein J, Nair R, Barasch A, Raber-Durlacher J, Migliorati C, Genot-Klastersky M, Treister N, Arany P, Lodewijckx J, Robijns J. Safety and efficacy of photobiomodulation therapy in oncology: A systematic review. Cancer Medicine 2020; Oct 26.

Research Bulletin • November – December 2020 • Harvard School of Dental Medicine 3

Sung T, Huang W, Ban L, Lee H, Wang J, Su H, Jen S, Chang Y, Yang J, Higuchi A, Ye Q. Enrichment of cancer-initiating cells from colon cancer cells through porous polymeric membranes by a membrane filtration method. Journal of Material and Chemical Biology 2020; Oct 30.

Treister N, Li S, Soiffer R, Cutler C. Topical sirolimus for management of refractory oral chronic graft-versus-host disease. Oral Diseases 2020; Oct 10.

Wang Y, Hu Y, Pan K, Li H, Shang S, Wang Y, Tang G, Han X. In-vivo imaging revealed antigen-directed gingival B10 infiltration in experimental periodontitis. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease 2020; Oct 17; 165991.

Ye Q, Sung T, Yang J, Ling Q, He Y, Higuchi A. Generation of universal and hypoimmunogenic human pluripotent stem cells. Cell Proliferation 2020;e12946.

Zu T, Wang D, Xu S, Lee C, Zhen E, Yoon C, Abarzua P, Wang S, Frank N, Wu X, Lian C, Murphy G. ATF-3 expression inhibits melanoma growth by downregulating ERK and AKT pathways. Laboratory Investigation 2020; Dec 9.

ORAL AND MAXILLOFACIAL SURGERY

Drouin A, Wallbillich N, Theberge M, Liu S, Katz J, Bellovoda K, Se Yun Cheon S, Gootkind F, Bierman E, Zavras J, Berberich M, Kalocsay M, Guastaldi F, Salvadori N, Troulis M, Fusco D. Impact of Zika virus on the human type I interferon osteoimmune response. Cytokine 2021;137:155342.

Malloy S, Dronkers W, Firriolo J, Nuzzi L, Koudstaal M, Padwa B, Taghinia A, Labow B. Outcomes following microvascular mandibular reconstruction in pediatric patients and young adults.vPlastic and Reconstructive Surgery – Global Open 2020;8(11):e3243.

Patel N, Harris J, Ji Y, Odera S. A telemedicine checklist for effective communication during virtual surgical visits. Journal of Oral and Maxillofacial Surgery 2020; Oct 22.

Tannyhill R, Baron M, Troulis M. Do graduating oral-maxillofacial surgery residents feel confident in practicing the full scope of the specialty? Journal of Oral and Maxillofacial Surgery 2020; Sep 24.

Wu B, Lee K, Hsiung M, Karlis V. What are the predictors of craniomaxillofacial injuries from hoverboard accidents? Journal of Oral and Maxillofacial Surgery 2020;78(11):2027-2031.

Zhang F, Hsu G, Das S, Chen Y, August M. Independent risk factors associated with higher mortality rates and recurrence of brain abscesses from head and neck sources. Oral Surgery Oral Medicine Oral Pathology Oral Radiology 2020; Aug 29.

Zhang J, Troulis M, August M. Diagnosis and treatment of pediatric primary jaw lesions at Massachusetts General Hospital. Journal of Oral and Maxillofacial Surgery 2020; Sep 12.

RESTORATIVE DENTISTRY AND BIOMATERIALS SCIENCES

Chen E, Kristie K, Ohyama H. Distance learning in the COVID-19 era: Comparison of student and faculty perceptions. Journal of Dental Education 2020; Oct 18.

Genereux D, ..., Nweeia M, and the Zoonomia Consortium. A comparative genomics multitool for scientific discovery and conservation. Nature 2020;587(7833):240-245 (details on page 6).

Gordon D, ..., Nweeia M, et al. Comparative host-coronavirus protein interaction networks reveal pan-viral disease mechanisms. Science 2020 Dec;370(6521):eabe9403.

Ha K, Lee A, Aram A, Ohyama H. Dental student perspective on Post-graduation planning in the COVID-19 Era panel. Journal of Dental Education 2020; Nov 30.

ORAL HEALTH POLICY AND EPIDEMIOLOGY

Aldosari M, Helmi M, Kennedy E, Badamia R, Odani S, Agaku I, Vardavas C. Depression, periodontitis, caries and missing teeth in the USA, NHANES 2009-2014.Family Medicine and Community Health 2020;8(4).

Cadet T, Burke S, Nedjat-Haiem F, Bakk L, Naseh M, Grudzien A, O’Driscoll J, Alcide A. Timing of Immigration Effects Asset Change Among Hispanic Caregivers of Older Family Members. Journal of Family and Economic Issues 2020;1-12.

Choi S, Oh J, Park S, Hwang S, Lee H, Kim K, Shobugawa Y, Kawachi I, Lee J. Association of community level social trust and reciprocity with mortality: a retrospective cohort study. BMC Public Health 2020;20(1):1793.

Dolce M, Barrow J, Jivraj A, Pham D, Da Silva J.Interprofessional value-based health care: Nurse practitioner-dentist model. Journal of Public Health in Dentistry 2020;80 Suppl 2:S44-S49.

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4 Research Bulletin • November – December 2020 • Harvard School of Dental Medicine

AWARDS & RECOGNITION

Dr. Arjun Saggu, MMSc21 (periodontology), has been selected as one of the four finalists of the clinical research competition at the 2020 American Academy of Periodontology Annual Meeting. He presented his poster entitled “RMS/mOCT

Probe for Chairside Diagnosis of Periodontal Diseases.” The goal of this study is to test the validity and reliability of a combined Raman microspectrocopy and micro-optical coherence tomography instrument in assessing marginal periodontium in health and periodontitis. Dr. Saggu presented results on the probe’s ability to distinguish between healthy and diseased sites using a composite measure of DNA, collagen type I, oral epithelium and connective tissue in marginal gingiva measurements that were confirmed by histology as gold standard. This work was carried out as part of a Phase II SBIR project supported by an NIH grant under the supervision of his mentor, Dr. Corneliu Sima, assistant professor of Oral Medicine, Infection and Immunity. The study also included a collaboration with Dr. Hatice Hasturk, senior member of the staff and director of the Center for Clinical and Translational Research at the Forsyth Institute, and Dr. Nicusor Iftimia, principal research scientist at Physical Sciences Inc.

Dr. Supattriya Chutinan, instructor in Restorative Dentistry and Biomaterials Sciences, received an award from the Eleanor and Miles Shore Faculty Development Program. This program supports those members of the Faculty of Medicine at

the level of instructor and assistant professor by administering a range of awards in support of academic activities. More specifically, Dr. Chutinan received the HSDM Fellowship in honor of Aina M. Auskaps, DMD, for her project entitled “Outcome Measurement of Caries Management Decision Tree Implementation at HSDM Teaching Clinic.”

Dr. Ruiying Chen, a postdoctoral fellow in the Baron-Gori Lab in the Department of Oral Medicine, Infection and Immunity, received the American Society for Bone and Mineral Research (ASBMR) 2020 Young Investigator Award. Dr. Chen presented her research

entitled “Secreted Frizzled Receptor Protein 4 (Sfrp4) is Required to Maintain Proper Ctsk+ Periosteal Stem/Progenitor Cell Niche Function.” Dr. Chen’s project is funded by an NIH-NIDCR grant awarded to Dr. Francesca Gori, assistant professor in the Department of Oral Medicine, Infection and Immunity, Division of Bone and Mineral Research; director of pre-doctoral research; and program director for the Research Academy at HSDM and the Forsyth Institute.

Dr. Jessica Latimer, DMSc24 (periodontology), received two awards from the American Academy of Periodontology 2020 Virtual Annual Meeting, Research Forum Poster Competition. She received the Clinical Science Award (given

to one of four finalists in the clinical science division of the research competition); and the Clinical Impact Award (given to one of eight finalists in the clinical or basic science divisions of the research competition to the individual

Research Bulletin • November – December 2020 • Harvard School of Dental Medicine 5

who has the greatest potential for changing and improving periodontal health and patient care). Dr. Latimer presented her research, “Interproximal Contacts Between Implant Restorations and Adjacent Natural Teeth as a Risk Indicator for Peri-Implant Disease: A Cross-Sectional Study.” Collaborators on the study include: Dr. Amit Gharpure (University of Washington School of Dentistry), Dr. Hahngoo Kahng (University of Washington School of Dentistry), Dr. Faisal Aljofi (Imam Abdulrahman Bin Faisal University College of Dentistry), and Dr. Diane Daubert (University of Washington School of Dentistry).

Dr. Ozge Erdogan, DMSc22 (oral biology), in the Harvard Forsyth Research Academy, received a competitive research grant from the Foundation for Endodontics for her research “Exploring Host-Microbiome Interactions in Symptomatic and

Asymptomatic Irreversible Pulpitis Using Quantitative Proteomics.” Dr. Erdogan’s project is being completed under the mentorship of Dr. Jennifer Gibbs, assistant professor of Restorative Dentistry and Biomaterials Sciences and program director for the advanced graduate education program in endodontics at HSDM and Dr. Markus Hardt, assistant member of the staff at the Forsyth Institute, and lecturer on Developmental Biology at HSDM. Dr. Erdogan was also selected as the highest-scoring non-resident applicant in the Fall 2020 research grant cycle. The purpose of this project is to understand how patients’ symptoms can range from excruciating, intolerable pain to a complete lack of symptoms during dental pulp inflammation due to deep caries. More specifically, this research study aims to profile host response, as well as the functional profile of the caries microbiome at protein/peptide level by investigating pulp and caries samples from patients and using a quantitative proteomics approach with hopes of identifying novel ways to alleviate pain, as well as to improve diagnosis.

ORAL HEALTH POLICY AND EPIDEMIOLOGY (CONTINUED)

Elani H, Sommers B, Kawachi I. Changes in coverage and access to dental care five years after ACA Medicaid expansion. Health Affairs (Millwood) 2020;39(11):1900-1908.

Jafer M, Crutzen R, Halboub E, Moafa I, van den Borne B, Bajonaid A, Jafer A, Hedad I. Dentists behavioral factors influencing early detection of oral cancer: Direct clinical observational study. Journal of Cancer Education 2020; Oct 22.

Kapos F, White L, Schmidt K, Hawes S, Starr J. Risk of non-syndromic orofacial clefts by maternal rural-urban residence and race/ethnicity: A population-based case-control study in Washington State 1989-2014. Paediatric Perinatal Epidemiology 2020; Dec 1.

Odani S, Lin L, Nelson JR, Agaku I. Misuse of prescription pain relievers, stimulants, tranquilizers, and sedatives among U.S. older adults aged ≥ 50 years. American Journal of Preventive Medicine 2020;59(6):860-872.

Shukla A, McKenna M, Hayes C, Klevens R. Association of human papillomavirus vaccination with exposure to dental or medical visits. Journal of Public Health in Dentistry 2020; Oct 10.

Simon L, Karhade D, Fox K, Barrow J, Palmer N. Dental services utilization by rurality among privately insured children in the United States. Pediatric Dentistry 2020;42(5):387-391.

MULTI-DEPARTMENTAL

Alqaderi H, Al-Ozairi E, Bin-Hasan S, Tavares M, Goodson JM, Alsumait A, Abu-Farha M, Abubaker J, Devarajan S, Almuhana N, Al-Mulla F. Mediation effect of C-reactive protein in the relationship between abdominal obesity and intermediate hyperglycemia in Kuwaiti adolescents. Biomarkers in Medicine 2020; Nov 5.

Carroll S, Macias Trevino C, Li E, Kawasaki K, Myers N, Hallett S, Alhazmi N, Cotney J, Carstens RP, Liao EC. An Irf6-Esrp1/2 regulatory axis controls midface morphogenesis in vertebrates. Development 2020; 194498.

He K, Breitman L, Lee J, Van Doren E, Li A, Donoff R. How US dental schools can better prepare their students to perform operative procedures. Journal of Dental Education 2020; Nov 16.

6 Research Bulletin • November – December 2020 • Harvard School of Dental Medicine

A Publication of the Office of Research

Malcolm Whitman, PhD Associate Dean for Basic Science

Yingzi Yang, PhD Associate Dean for Translational Research

Dawn M. DeCosta Editor, Design and Layout

Heather M. Denny Editing

Lia Sgourakes Editing

Ashley SimmonsEditing

If you have questions, or comments, please contact Dawn M. DeCosta, Director of Research Operations at 617-824-0715 (or) [email protected]

The Office of Global and Community Health at Harvard School of Dental Medicine hosted a special oral health seminar featuring the U.S. Surgeon General, Vice Admiral Jerome Adams, MD, MPH. The Zoom presentation drew over 300 attendees. In his talk, Dr. Adams highlighted the importance of oral health, its social determinants, and how it is inextricably integral to general health. Jane Barrow, MS, associate dean for Global and Community Health, Oral Health Policy and Epidemiology, and William V. Giannobile, DDS, MS, DMSc, dean of HSDM and professor of Oral Medicine, Infection and Immunity were the moderators.

Martin Nweeia, DMD, DDS, lecturer in the Department of Restorative Dentistry andBiomaterials Sciences, is part of a collaboration featured in a Nature cover article entitled, “A Comparative Genomics Multitool for Scientific Discovery and Conservation.”

In this article, Dr. Elinor Karlsson, director of the Vertebrate Genomics Group at the Broad Institute of MIT and Harvard and her colleagues (including Dr. Nweeia and the Zoonomia Project) describe their analysis of 240 genomes representing more than 80% of placental mammal families, including 122 newly sequenced species. To analyze these massive data sets, both teams used new software called Progressive Cactus. The Zoonomia Project is an international collaboration to discover the genomic basis of shared and specialized traits in mammals. By prioritizing phylogenetic diversity and making data available quickly and without restriction, the Zoonomia Project aims to support biological discovery, medical research and the conservation of biodiversity.