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Microbiota Stratification Identifies Disease-Specific Alterations in Neuro-Behçet’S Disease and Multiple Sclerosis N

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Microbiota Stratification Identifies Disease-Specific Alterations in Neuro-Behçet’S Disease and Multiple Sclerosis N Microbiota stratification identifies disease-specific alterations in neuro-Behçet’s disease and multiple sclerosis N. Oezguen1, N. Yalçınkaya1, C.I. Kücükali2, M. Dahdouli1, E.B. Hollister3, R.A. Luna1, R. Türkoglu4, M. Kürtüncü2, M. Eraksoy5, T.C. Savidge1, E. Tüzün2 1Baylor College of Medicine, Dept. of ABSTRACT initiates in the intestines (1). Behçet’s Pathology and Immunology, and Texas Objective. Altered gut microbiota disease (BD) (2) is a distinct chronic Children’s Microbiome Center, Houston community dynamics are implicated inflammatory disorder that also targets TX, USA; 2Istanbul University, Dept. of Neuroscience, Institute for Experimental in diverse human diseases including the CNS in around 10% of cases and Medical Research, Istanbul, Turkey; inflammatory disorders such as neuro- leads predominantly to ataxia, paresis, 3Diversigen, Inc., Houston, TX, USA; Behçet’s disease (NBD) and multiple sphincter dysfunction and cognitive- 4Haydarpasa Numune Training and sclerosis (MS). Traditionally, microbio- behavioral changes. This category of Research Hospital, Dept. of Neurology, ta communities are analysed uniformly BD is named neuro-Behçet’s disease 5 Istanbul, Turkey; Istanbul University, across control and disease groups, but (NBD), which manifests mostly in Istanbul School of Medicine, Dept. of Neurology, İstanbul, Turkey. recent reports of subsample clustering the form of parenchymal lesions en- indicate a potential need for analyti- compassing brainstem, diencephalon Numan Oezguen, PhD Nazlı Yalçınkaya, MSc cal stratification. The objectives of this and basal ganglia, and occasionally Cem Ismail Kücükali, MD, PhD study are to analyse and compare fae- involves cerebral venous thrombosis Mahmoud Dahdouli, BSc cal microbiota community signatures (3). A common trigger of these disor- Emily B. Hollister, PhD of ethno-geographical, age and gender ders is believed to be due to excessive Ruth A. Luna, PhD matched adult healthy controls (HC), innate immune responses to viral and/ Recai Türkoglu, MD MS and NBD individuals. or bacterial threats (4). Experimental Murat Kürtüncü, MD Mefküre Eraksoy, MD Methods. Faecal microbiota community animal models of MS and autoimmune Tor C. Savidge, PhD compositions in adult HC (n=14), NBD encephalomyelitis provide strong Erdem Tüzün, MD patients (n=13) and MS (n=13) were causative evidence linking altered gut Please address correspondence to: analysed by 16S rRNA gene sequencing microbiota community dynamics to Dr Numan Oezguen, and standard bioinformatics pipelines. enhanced Th17-type immunity (5). Texas Children’s Microbiome Center, Bipartite networks were then used to Moreover, previous studies reported Feigin Tower, Room 955.11, identify and re-analyse dominant com- gut microbiota dysbiosis in both MS 1102 Bates Avenue, Houston, positional clusters in respective groups. (6-10) and BD (11-13) patients. How- TX 77030, USA. E-mail: [email protected] Results. We identified Prevotella and ever, no consensus of microbiota find- Received on November 25, 2018; accepted Bacteroides dominated subsample ings for BD is reported to date, and in revised form on March 28, 2019. clusters in HC, MS, and NBD cohorts. only a partial consensus was reached in Clin Exp Rheumatol 2019; 37 (Suppl. 121): Our study confirmed previous reports MS studies indicating a decrease in the S58-S66. that Prevotella is a major dysbiotic genus Prevotella. © Copyright CLINICAL AND target in these diseases. We demon- The gut microbiota colonises the new- EXPERIMENTAL RHEUMATOLOGY 2019. strate that subsample stratification is born infant with rapid expansion occur- required to identify significant disease- ring during the first years of life, until Key words: Behçet’s disease, associated microbiota community maturation around 4 years of age into multiple sclerosis, gut microbiota, shifts with increased Clostridiales evi- adulthood (14) and destabilisation in 16S ribosomal RNA, dysbiosis dent in Prevotella-stratified NBD and the aged. Several factors are reported Bacteroides-stratified MS patients. to contribute to variations in microbi- Funding: this study was supported by the Conclusion. Patient cohort stratifica- ota community composition including Research Fund of University of İstanbul, tion may be needed to facilitate identifi- host genetics, diet, age, and geographic Project no: 31110; and by the National cation of common microbiota communi- location. Different sequencing and Institute of Diabetes and Digestive and ty shifts for causation testing in disease. analytical methods also contribute to Kidney Diseases Grant UH3DK083990, variations in the interpretation of mi- the National Institute of Allergy and Infectious Diseases grants U011AI24290 Introduction crobiota community dynamics. Thus, and R01AI10091401, NIH grant P30 Multiple sclerosis (MS) is a chronic finding reproducibility in gut micro- DK56338, Texas Children’s Hospital PSO inflammatory demyelinating disorder biota community structure remains a Research Support for Texas Children’s of the central nervous system (CNS) significant challenge. Initial meta-anal- Microbiome Center. which is primarily mediated by aber- ysis (15) of the Human Microbiome Competing interests: see page S-65. rant Th17-type acquired immunity that Project (HMP) in the United States S-58 Clinical and Experimental Rheumatology 2019 Stratification prior to microbiota analysis / N. Oezguen et al. (16) and the European MetaHIT (17) Table I. Demographic and clinical features of MS and NBD patients and HC. study found subsample clusters which MS (n=13) NBD (n=13) HC (n=14) p-value were dominated by the genera Bacte- roides, Prevotella, and Ruminococ- Age 39.1 ± 11.6 42.1 ± 13.6 37.8 ± 8.6 0.642* cus, termed Enterotypes. Although the Gender (M/F) 5/8 8/5 10/4 0.209** thought that the gut microbiome could Disease duration (mean years±SD) 10.1 ± 11.0 10.6 ± 12.9 NA 0.929* EDSS (mean ± SD) 3.5 ± 1.9 3.1 ± 0.9 NA 0.731*** potentially be characterised by a lim- ited number of enterotypes, similar to BD symptoms blood types, was very appealing, it was Oral aphthous ulcers None 13 (100%) None NA Genital ulcers None 10 (77%) None NA also controversial (18, 19). A recent re- Ocular inflammation None 9 (69%) None NA analysis (20) of HMP, MetaHIT, and Skin lesions None 6 (46%) None NA a Chinese type II diabetes study (21) Positive pathergy test None 9 (69%) None NA confirmed the existence of subsample Clinical syndromes clusters. Moreover, Gupta et al. (22) Brainstem/cerebellar 4 (31%) 12 (92%) None 0.001** † reviewed gut microbiota sequencing Supratentorial 11 (85%) 2 (15%) None <0.001** data from different parts of the world Cranial MRI and concluded that the gut microbiome Typical NBD lesions†† 0 (0%) 13/13 (100%) NA <0.001** ††† in hunter-gatherer populations were Periventricular/juxtacortical 13 (100%) 0 (0%) NA <0.001** Cerebellar††† 9 (69%) 0 (0%) NA <0.001** dominated by Prevotella, Proteobac- Brainstem††† 3 (23%) 0 (0%) NA <0.001** teria, Spirochaetes, Clostridiales, and Treatment 7 (54%) 13 (100%) NA NA Ruminobacter, while urban popula- Interferon-beta Azathioprine tions were dominated by Bacteroides, 4 (31%) 9 (69%) Fingolimod Colchicine Bifidobacterium, and Firmicutes. It 2 (15%) GA was concluded that geography, ethnic/ genetic factors, and lifestyle effect in- M: male; F: female; SD: standard deviation; NA: not applicable; EDSS: expanded disability status cluding diet have a major impact on gut scale; GA: glatiramer acetate. *ANOVA; **chi-square; ***Mann-Whitney U; †include patients with hemiparesis and/or hemihypoes- microbiota composition. thesia; ††Large extensive lesions covering one or more of brainstem, diencephalon and basal ganglia Here, we sought to analyse and com- regions; †††MS-like lesions ≥5 mm with an ovoid shape. pare faecal microbiota community sig- Note that some patients displayed more than one clinical syndrome or lesion location. natures of ethno-geographical, age and gender matched adult healthy controls conducted by ANOVA and chi-square primers for the variable V3-V5 regions (HC), MS and NBD individuals. We methods, respectively (Table I). Dis- of the bacterial 16S rRNA gene (26) on further sought to test for the presence ease duration and expanded disabil- a GS-FLX platform (454 Life Sciences/ of subsample clusters in each cohort as ity status scale (EDSS) scores of MS Roche, Branford, Connecticut, USA). these could affect microbiota commu- and NBD patients were compared us- Reads of at least 200 bp of length and nity profiling. ing Mann-Whitney U test. Clinical quality score of at least 20 were further syndromes and lesion locations were processed and analysed. Materials and methods compared with chi-square. The study Patients and healthy controls was approved by the local Ethics Com- Sequence processing and analyses MS and NBD patients from the Istan- mittee of Istanbul Faculty of Medicine, Primers and barcodes were removed bul/Turkey metropolitan area were re- Istanbul University. from sequence reads conforming to the cruited and matched with HC adults length and quality criteria. Trimmed (Table I). Key inclusion criteria for MS Faecal collection, DNA extraction, reads were then de novo clustered into and NBD patients were not receiving and sequencing Operational Taxonomic Units (OTU) pulse steroid treatment within the last Faecal specimens were collected and with 97% identity cutoff using the 3 months and being in clinical remis- processed as previously described (25). UPARSE (27) clustering engine from sion. All NBD patients had to fulfill All samples
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