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Oral Bacteriome of HIV‐1‐Infected Children from Rio De PROF. LUCIO SOUZA GONÇALVES (Orcid ID : 0000-0002-4388-6310) Article type : Original Article Clinical Periodontology Oral bacteriome of HIV-1-infected children from Rio de Janeiro – Brazil: Next- generation DNA sequencing analysis Running title: Oral bacteriome of HIV-infected children 1 Lucio Souza Gonçalves, DDS, MSc, PhD 1,2 Dennis de Carvalho Ferreira, DDS, MSc, PhD 7 Nicholas C. K. Heng, BSc, PhD 1 Fabio Vidal, DDS, MSc, PhD 3 Henrique Fragoso dos Santos, DDS, MSc, PhD 7 Diogo Godoy Zanicott, BDS, MClinDent, PhD 4 Mariana Vasconcellos, DDS, MSc 2 Mayra Stambovsky, DDS, MSc 8 Blair Lawley, PhD 6 Norma de Paula Motta Rubini, PhD 5 Katia Regina Netto dos Santos, MSc, PhD 9 Gregory J Seymour, BDS, MDSc, PhD 1Programa de Pós-Graduação em Odontologia, Universidade Estácio de Sá, Rio de Janeiro, Brazil. Author Manuscript This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/JCPE.13176 This article is protected by copyright. All rights reserved 2 Universidade Veiga de Almeida, Rio de Janeiro, Brazil. 3Universidade Federal Fluminense, RJ, Brazil. 4 Universidade Federal do Rio de Janeiro, Rio de janeiro, Brazil. 5Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil. 6Departmento de Imunologia, Universidade Federal do Estado do Rio de Janeiro, Rio de Janeiro, Brazil. 7Sir John Walsh Research Institute, University of Otago, Dunedin, New Zealand 8Department of Microbiology and Immunology, University of Otago, Dunedin, New Zealand 9School of Dentistry, The University of Queensland, Brisbane, Australia Conflict of interest: The authors declare that they have no competing interests. Acknowledgements This work was supported by National Council for Scientific and Technological Development (CNPq) (Project: 211309/2013-3) and Foundation for Research Financial Support in the State of Rio de Janeiro (FAPERJ), Rio de Janeiro, Brazil (Project: E26/103.001/2012). Correspondence and reprints should be sent to: Lucio Souza Gonçalves, Estácio de Sá University, Rio de Janeiro, Brazil Address: Av. Alfredo Baltazar da Silveira, 580 – cobertura, Recreio dos Bandeirantes, Rio de Janeiro, RJ, Brazil. Postal code: 22790-710Author Manuscript Telephone number: +5521994550040 Email: [email protected] This article is protected by copyright. All rights reserved Author Manuscript This article is protected by copyright. All rights reserved ABSTRACT Background & Aim: This study compared the oral bacteriome between HIV-1-infected and non-HIV-1-infected Brazilian children/teenagers. Methods: Whole saliva, biofilm from the dorsal surface of the tongue, and biofilm from supragingival and subgingival sites were collected from 27 HIV-1-infected and 30 non- HIV-1-infected individuals. Bacterial genomic DNA was extracted and 16S rRNA genes were sequenced using next-generation sequencing technology (Ion Torrent). Results: In the supragingival biofilm, the phylum Firmicutes and genus Streptococcus sp. were more frequent in HIV-1-infected (95% and 78%, respectively) than in non- HIV-1-infected individuals (40% and 24%, respectively). In the subgingival biofilm of HIV-infected participants, the relative abundance of the Veillonella sp. and Prevotella sp. genera were higher than in non-HIV-1-infected participants. On the tongue, the genera with greater relative abundance in HIV-1-infected individuals were Neisseria sp. (21%). In saliva, the difference of the genus Prevotella sp. between non-HIV-1-infected and HIV-1-infected individuals was 15% and 7%, respectively. The Chao index revealed an increase in the richness of both sub- and supragingival biofilms in the HIV- 1-infected samples compared with non-HIV-1-infected samples. Conclusion: HIV-1-infected children/teenagers have a higher frequency of the phyla Firmicutes and genus Streptococcus, and their oral microbiome shows more complexity than that of non-HIV-1-infected children/teenagers. CLINICAL RELEVANCE Scientific rationaleAuthor Manuscript for study Only two papers have been published regarding the oral microbiome of HIV-1-infected children. This article is protected by copyright. All rights reserved Principal findings The samples of supragingival dental biofilm of HIV-1-infected subjects were almost entirely dominated by Firmicutes (~95%). Neisseria sp., Leptotrichia sp. and Fusobacterium sp. with relative abundance of approximately 13%. 15% and 8% in non- HIV-1-infected individuals respectively, were not found in HIV-1-infected children/teenagers. Practical implications Oral bacterial community shifts or dysbiosis are relevant factors associated with oral diseases, such as caries and periodontal disease, as well as with systemic events in HIV- 1-infected children/teenagers. INTRODUCTION The human immunodeficiency virus-1 (HIV-1) epidemic has been so dramatic and devastating that it has been described as the “epidemic of our century” (Merchant et al. 2001). It is estimated that approximately 36.7 million people, (2.1 million children younger than 15 years old) are currently living with HIV-1. (UNAIDS/WHO – Global HIV epidemic, 2017). Several studies have assessed the periodontal microbiota of HIV-1-infected patients (Zambon et al. 1990, Murray et al. 1991, Luch et al. 1991, Rams et al. 1991, Moore et al. 1993, Cross & Smith 1995, Brady et al. 1996, Tenenbaum et al. 1997, Scully et al. 1999, Jabra Risk et al. 2001, Tsang & Samaranayake 2001, Patel et al. 2003, Gonçalves et al. 2004, Gonçalves et al. 2007, Aas et al. 2007, Gonçalves et al. 2009, Ramos et al. 2012). Nevertheless, the findings of these studies are still controversial. Studies have detected a greater prevalence of periodontal pathogens such as Aggregatibacter actinomycetemcomitans, Fusobacterium nucleatum, Porphyromonas gingivalis, Prevotella intermedia, Tannerella forsythia, and Treponema denticola, as well as a combinationAuthor Manuscript of these species in HIV-1-infected patients compared with non- HIV-1-infected individuals (Cross & Smith 1995, Tenenbaum et al. 1997, Scully et al. 1999, Patel et al. 2003). Microorganisms usually not considered as members of the periodontal microbiota have also been identified in HIV-1-infected individuals, such as This article is protected by copyright. All rights reserved Staphylococcus epidermidis, Candida albicans (Zambon et al. 1990, Odden et al. 1994, Chattin et al. 1999), Enterococcus faecalis, Clostridium clostridiiforme, Clostridium difficile, Mycoplasma salivarium (Zambon et al. 1990, Moore et al. 1993, Gonçalves et al. 2004, Gonçalves et al. 2007), Acinetobacter baumannii and Pseudomonas aeruginosa (Gonçalves et al. 2007). Very few studies regarding the oral microbiota of HIV-1-infected children have been reported and most of them are usually restricted to Candida species (Brown et al. 2000, Munro & Hube 2002, Bosco et al. 2003, Pongsiriwet et al. 2004, Portela et al. 2004). Differences in the distribution of cariogenic microorganisms, such as Streptococcus mutans, Streptococcus sobrinus, and Lactobacillus acidophilus, have not been observed between HIV-1 and non-HIV-1-infected children (Castro et al. 2004). However, Silva-Boghossian et al. (2007) have shown higher frequencies and levels of beneficial species of oral streptococci, together with Actinomyces sp., and Veilonella parvula, potential oral pathogens (Eubacterium nodatum, F. nucleatum, Parvimona micra, P. intermedia, Selenomonas noxia, T. forsythia, T. denticola) and species not usually detected in the oral cavity (Bacillus cereus, Corynebacterium diphteriae, E. faecalis, Klebsiella pneumoniae, P. aeruginosa, and Staphylococcus aureus) in the salivary microbiota of non-HIV-1 than HIV-1-infected children. A number of authors have studied the oral microbiota of HIV-1-infected individuals using gene amplicon sequencing (Dang et al. 2012, Li et al. 2014, Beck et al. 2015, Kistler et al. 2015, Noguera-Julian et al. 2017, Presti et al. 2018, Goldberg et al. 2015, Starr et al. 2018), however only two papers have been published regarding the oral microbiome of HIV-1-infected children (Goldberg et al. 2015, Starr et al. 2018). These studies were carried out with HIV-1-infected children from the USA, by the use of 454 pyrosequencing (Goldberg et al. 2015) or Illumina platform on a MiSeq (Starr et al. 2018). The relationship between the oral microbiome and oral disease in HIV-1- infected patients is still poorly understood, especially in children (Goldberg et al. 2015, Starr et al. 2018).Author Manuscript It has been proposed that HIV-1-infection is associated with alterations in the gut microbiome. These occur early in the course of infection, as a consequence of the depletion of CD4+ T cells in the intestinal mucosa and are not fully restored with antiretroviral therapy (Brenchley et al. 2006, Zevin et al. 2016, Saxena This article is protected by copyright. All rights reserved et al. 2016, Heron & Elahi 2017). Whether similar changes occur in the oral microbiome are, as yet, unknown. The aim of the current study therefore was to compare the oral bacteriome between non-HIV-1 and HIV-1-infected Brazilian children/teenagers using Ion Torrent 16S rRNA gene amplicon sequencing. MATERIAL AND METHODS Subject selection Twenty-seven patients were selected from a group of the HIV-1-infected children/teenagers between 2 and 18 years old who were
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