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Middle Ear Microbiome Differences in Indigenous Filipinos with Chronic Otitis Media Due to a Duplication in the A2ML1 Gene Regie Lyn P

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Middle Ear Microbiome Differences in Indigenous Filipinos with Chronic Otitis Media Due to a Duplication in the A2ML1 Gene Regie Lyn P Santos-Cortez et al. Infectious Diseases of Poverty (2016) 5:97 DOI 10.1186/s40249-016-0189-7 SHORT REPORT Open Access Middle ear microbiome differences in indigenous Filipinos with chronic otitis media due to a duplication in the A2ML1 gene Regie Lyn P. Santos-Cortez1,9*, Diane S. Hutchinson2, Nadim J. Ajami2, Ma. Rina T. Reyes-Quintos3,4, Ma. Leah C. Tantoco3, Patrick John Labra4, Sheryl Mae Lagrana3, Melquiadesa Pedro3,ErasmoGonzalod.V.Llanes3,4, Teresa Luisa Gloria-Cruz3,4, Abner L. Chan3,4,EvaMariaCutiongco-delaPaz5,6, John W. Belmont7,10, Tasnee Chonmaitree8, Generoso T. Abes3,4, Joseph F. Petrosino2, Suzanne M. Leal1 and Charlotte M. Chiong3,4 Abstract Background: Previously rare A2ML1 variants were identified to confer otitis media susceptibility in an indigenous Filipino community and in otitis-prone US children. The goal of this study is to describe differences in the middle ear microbiome between carriers and non-carriers of an A2ML1 duplication variant that increases risk for chronic otitis media among indigenous Filipinos with poor health care access. Methods: Ear swabs were obtained from 16 indigenous Filipino individuals with chronic otitis media, of whom 11 carry the A2ML1 duplication variant. Ear swabs were submitted for 16S rRNA gene sequencing. Results: Genotype-based differences in microbial richness, structure, and composition were identified, but were not statistically significant. Taxonomic analysis revealed that the relative abundance of the phyla Fusobacteria and Bacteroidetes, and genus Fusobacterium were nominally increased in carriers compared to non-carriers, but were non-significant after correction for multiple testing. We also detected rare bacteria including Oligella that was reported only once in the middle ear. Conclusions: These findings suggest that A2ML1-related otitis media susceptibility may be mediated by changes in the middle ear microbiome. Knowledge of middle ear microbial profiles according to genetic background can be potentially useful for therapeutic and prophylactic interventions for otitis media and can guide public health interventions towards decreasing otitis media prevalence within the indigenous Filipino community. Keywords: A2ML1, Indigenous population, Microbiome, Middle ear, Oligella,Otitismedia,Philippines Abbreviations: OTU, Operational taxonomic units; PCR, Polymerase chain reaction * Correspondence: [email protected] 1Department of Molecular and Human Genetics, Center for Statistical Genetics, Baylor College of Medicine, Houston, TX 77030, USA 9Current affiliation: Department of Otolaryngology, University of Colorado School of Medicine, Aurora, CO 80045, USA Full list of author information is available at the end of the article © 2016 The Author(s). Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Santos-Cortez et al. Infectious Diseases of Poverty (2016) 5:97 Page 2 of 9 Multilingual abstracts the middle ear microbial composition of individuals with Please see Additional file 1 for translations of the chronic otitis media, which may explain in part the abstract into the six official working languages of the pathogenic mechanism by which the A2ML1 duplication United Nations. variant confers otitis media susceptibility. This study is novel for several reasons: (A) Most microbiome studies Background for (non-chronic) otitis media used nasopharyngeal and Otitis media or middle ear infection is an important adenoid samples rather than middle ear fluid or swabs, public health problem worldwide. In developed countries and differences in microbial profiles according to sample otitis media remains the top reason for health care visits source within the head and neck is known [8, 9]. (B) and antibiotic use among children [1], while incidence Previously middle ear microbiome studies were per- and prevalence of otitis media are particularly high in formed for chronic otitis media using a single sample sub-Saharan Africa, Asia and in marginalized communi- and on 11 indigenous Australian children with effusive ties such as indigenous populations, where the burden otitis media [10, 11]. (C) Comparison of microbiome of complications due to chronic otitis media (e.g., hear- findings according to human host genotype has only ing loss) is mostly felt [2]. Due to high prevalence of been done for a few diseases (e.g., cystic fibrosis, inflam- chronic suppurative otitis media and its complications in matory bowel disease), but not otitis media [12, 13]. This developing countries, it was recently proposed for chronic study also further supports the concept that in the pres- otitis media to be classified as a neglected tropical disease ence of human or host mutation, the complexity of dis- [3]. While multiple risk factors are associated with otitis ease patterns can be partly attributed to changes in the media, there is strong evidence that a genetic basis for microbiome. otitis media susceptibility exists [4, 5]. Recently we identified rare variants in the A2ML1 Methods gene, which encodes alpha-2-macroglobulin-like 1 pro- The study was approved by the: Baylor College of Medi- tein, as a cause of otitis media susceptibility [6]. A rare cine (BCM) Institutional Review Board and Affiliated A2ML1 duplication variant c.2478_2485dupGGCTAAAT Hospitals; the National Commission on Indigenous Peo- (p.(Ser829Trpfs*9)) confers susceptibility to otitis media ples, Philippines; and the University of the Philippines in three European- or Hispanic-American children in Manila Research Ethics Board. Informed consent was Texas, USA and an indigenous Filipino population. This obtained from adult participants and parents or guard- variant co-segregated with different forms of otitis media ians of pediatric patients. Participating individuals from in a six-generation pedigree within the indigenous an indigenous Filipino community were examined by Filipino community, which is highly intermarried due to otoscopy. Previous analyses of multiple risk factors for socio-economic segregation and cultural discrimination otitis media established a homogeneous environmental and has a relatively homogeneous environmental back- background for this community [7]. Despite high preva- ground i.e., poor health care access and hygiene, lack of lence of otitis media, this community has poor access to pneumococcal vaccination, crowded households and health care including vaccinations and antibiotic treat- swimming in dirty seawater. In this population, known ments and has no surgical facilities within the island. In risk factors for otitis media including quantitative age, many cases, otitis media either spontaneously resolves gender, nutrition and tobacco exposure were not asso- with age or results in chronic eardrum perforation with ciated with otitis media status [7]. Additionally the recurrent discharge. Chronically perforated eardrums three US children who also carry the A2ML1 duplica- result in long-term exposure of the middle ear mucosa tion variant had early-onset recurrent otitis media that to the outer ear flora and the environment, e.g., during required tympanostomy tube insertion within the first bathing or swimming in the sea. six months of age. The duplication variant occurred From each individual, human genomic DNA from within a short haplotype that was common among the saliva was obtained using Oragene DNA saliva kits indigenous Filipinos and the US children, suggesting a (DNA Genotek, Ontario, Canada). DNA samples were founder variant that is estimated to be 1 800 years old Sanger-sequenced for the A2ML1 duplication variant [6]. and that may have occurred within the Filipino and US From indigenous Filipinos with perforated eardrum(s) populations through Spanish colonization [6]. due to chronic otitis media, outer ear swabs were Genetic susceptibility to otitis media has been estab- collected prior to middle ear swabs, using sterile short lished using family and association studies, however the polyester-tipped Pur-Wrap swabs (Puritan Medical, mechanisms by which genetic variants influence host- Guilford, ME, USA). The outer ear swabs were rubbed bacterial interactions in the middle ear has not been gently against outer ear canal skin, then additional swabs elucidated. Here we show suggestive evidence that car- were rubbed against middle ear mucosa and/or edges of riage of the A2ML1 duplication variant might influence eardrum perforations and soaked on discharge when Santos-Cortez et al. Infectious Diseases of Poverty (2016) 5:97 Page 3 of 9 present. Each swab specimen was placed directly in the associated with otitis media status within the indigenous collection tube from the PowerSoil DNA isolation kit Filipino community [7], no other variables were used in (MO BIO Laboratories, Carlsbad, CA, USA), the swab the analyses. stem cut with sterile scissors, and the collection tube closed, sealed and labeled. All samples were stored in a Results -20 °C freezer until shipped to BCM on dry ice. Middle and outer ear swabs were obtained from 16 indi- All collected swabs
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