Comparison of the Skin Microbiota in the Periocular Region between Patients with Inflammatory Skin Diseases and Healthy Participants: A Preliminary Study

(1) Background: Periocular or periorbital dermatitis is a common term for all inflammatory skin diseases affecting the area of skin around the eyes. The clear etiopathogenesis of periocular dermatitis is still not fully understood. Advances in molecular techniques for studying microorganisms living in and on our bodies have highlighted the microbiome as a possible contributor to disease, as well as a promising diagnostic marker and target for innovative treatments. The aim of this study was to compare the composition and diversity of the skin microbiota in the periocular region between healthy individuals and individuals affected by the specific entity of periocular dermatitis. (2) Methods: A total of 35 patients with periocular dermatitis and 39 healthy controls were enrolled in the study. After a skin swab from the periocular region was taken from all participants, DNA extraction and 16S rRNA gene amplicon sequencing using Illumina NovaSeq technology were performed. (3) Results: Staphylococcus and Corynebacterium were the most abundant bacterial genera in the microbiota of healthy skin. Analysis of alpha diversity revealed a statistically significant change (p < 0.05) in biodiversity based on the Faith’s PD index between patients and healthy individuals. We did not observe changes in beta diversity. The linear discriminant analysis effect size (LEfSe) revealed that Rothia, Corynebacterium, Bartonella, and Paracoccus were enriched in patients, and Anaerococcus, Bacteroides, Porphyromonas, and Enhydrobacter were enriched in healthy controls. (4) Conclusions: According to the results obtained, we assume that the observed changes in the bacterial microbiota on the skin, particularly Gram-positive anaerobic cocci and skin commensals of the genus Corynebacterium, could be one of the factors in the pathogenesis of the investigated inflammatory diseases. The identified differences in the microbiota between healthy individuals and patients with periocular dermatitis should be further investigated.

[1]  J. van Griensven,et al.  Bartonella quintana detection among arthropods and their hosts: a systematic review and meta-analysis , 2024, Parasites & vectors.

[2]  M. Gonçalo,et al.  Differential diagnosis of contact dermatitis: A practical-approach review by the EADV Task Force on contact dermatitis. , 2024, Journal of the European Academy of Dermatology and Venereology : JEADV.

[3]  Xue-Er Zhang,et al.  Microbiome: Role in Inflammatory Skin Diseases , 2024, Journal of inflammation research.

[4]  J. Bouwstra,et al.  Treatment with the Topical Antimicrobial Peptide Omiganan in Mild-to-Moderate Facial Seborrheic Dermatitis versus Ketoconazole and Placebo: Results of a Randomized Controlled Proof-of-Concept Trial , 2023, International journal of molecular sciences.

[5]  A. Di Nardo,et al.  S. epidermidis Rescues Allergic Contact Dermatitis in Sphingosine 1-Phosphate Receptor 2-Deficient Skin , 2023, International journal of molecular sciences.

[6]  B. Closs,et al.  Commensal Cutibacterium acnes induce epidermal lipid synthesis important for skin barrier function , 2023, Science advances.

[7]  Anna Dragoš,et al.  New Phage-Derived Antibacterial Enzyme PolaR Targeting Rothia spp. , 2023, Cells.

[8]  M. Buljan,et al.  Association of Gut Lachnospiraceae and Chronic Spontaneous Urticaria , 2023, Life.

[9]  A. Żaczek,et al.  Skin Microbiome in Prurigo Nodularis , 2023, International journal of molecular sciences.

[10]  J. Schalkwijk,et al.  Gram-positive anaerobic cocci guard skin homeostasis by regulating host-defense mechanisms. , 2023, iScience.

[11]  Luokai Wang,et al.  The role of short-chain fatty acids in inflammatory skin diseases , 2023, Frontiers in Microbiology.

[12]  Paisleigh Smythe,et al.  The Skin Microbiome: Current Landscape and Future Opportunities , 2023, International journal of molecular sciences.

[13]  D. Zillikens,et al.  Unmet Medical Needs in Chronic, Non-communicable Inflammatory Skin Diseases , 2022, Frontiers in Medicine.

[14]  B. Chung,et al.  Aryl Hydrocarbon Receptors: Evidence of Therapeutic Targets in Chronic Inflammatory Skin Diseases , 2022, Biomedicines.

[15]  Z. Wan,et al.  Ketoconazole 2% cream alters the skin fungal microbiome in seborrhoeic dermatitis: a cohort study , 2022, Clinical and experimental dermatology.

[16]  Xiang Chen,et al.  Biomarkers of Gut Microbiota in Chronic Spontaneous Urticaria and Symptomatic Dermographism , 2021, Frontiers in Cellular and Infection Microbiology.

[17]  H. Gunawan,et al.  A Pilot Study: Composition and Diversity of 16S rRNA Based Skin Bacterial Microbiome in Indonesian Atopic Dermatitis Population , 2021, Clinical, cosmetic and investigational dermatology.

[18]  A. Pallejà,et al.  Skin dysbiosis in the microbiome in atopic dermatitis is site-specific and involves bacteria, fungus and virus , 2021, BMC Microbiology.

[19]  Myung-Kyung Kim,et al.  Risk factors for periorbital dermatitis in patients using dorzolamide/timolol eye drops , 2021, Scientific Reports.

[20]  M. Mravak-Stipetić,et al.  Features of the Skin Microbiota in Common Inflammatory Skin Diseases , 2021, Life.

[21]  C. Clavaud,et al.  Continuous clinical improvement of mild‐to‐moderate seborrheic dermatitis and rebalancing of the scalp microbiome using a selenium disulfide–based shampoo after an initial treatment with ketoconazole , 2021, Journal of cosmetic dermatology.

[22]  Ruoyu Li,et al.  Skin microbiome alterations in seborrheic dermatitis and dandruff: A systematic review , 2021, Experimental dermatology.

[23]  L. Pardo,et al.  Composition of cutaneous bacterial microbiome in seborrheic dermatitis patients: A cross-sectional study , 2021, PloS one.

[24]  N. Kiss,et al.  Psoriasis and Gut Microbiome—Current State of Art , 2021, International journal of molecular sciences.

[25]  M. Shariati,et al.  Recent advances in the therapeutic application of short-chain fatty acids (SCFAs): An updated review , 2021, Critical reviews in food science and nutrition.

[26]  T. Agner,et al.  Staphylococcal Communities on Skin Are Associated with Atopic Dermatitis and Disease Severity , 2021, Microorganisms.

[27]  A. Di Nardo,et al.  Sphingosine 1-phosphate receptor 2 is central to maintaining epidermal barrier homeostasis. , 2020, The Journal of investigative dermatology.

[28]  F. Forton The Pathogenic Role of Demodex Mites in Rosacea: A Potential Therapeutic Target Already in Erythematotelangiectatic Rosacea? , 2020, Dermatology and Therapy.

[29]  E. Breitschwerdt,et al.  Imaging analysis of Bartonella species in the skin using single‐photon and multi‐photon (second harmonic generation) laser scanning microscopy , 2020, Clinical case reports.

[30]  E. Warshaw,et al.  Eyelid Dermatitis in Patients Referred for Patch Testing: Retrospective Analysis of North American Contact Dermatitis Group Data, 1994 - 2016. , 2020, Journal of the American Academy of Dermatology.

[31]  H. Hackl,et al.  First evidences of distinguishable bacterial and fungal dysbiosis in the skin of patients with Atopic Dermatitis or Netherton Syndrome. , 2020, The Journal of investigative dermatology.

[32]  M. Farhat,et al.  Bacterial and fungal microbiome characterization in patients with rosacea and healthy controls , 2020, The British journal of dermatology.

[33]  C. Antonescu,et al.  Comparison of the skin microbiota in acne and rosacea , 2020, Experimental dermatology.

[34]  Hongwei Zhou,et al.  Malassezia and Staphylococcus dominate scalp microbiome for seborrheic dermatitis , 2020, Bioprocess and Biosystems Engineering.

[35]  K. Shirahige,et al.  The Microbiome of the Meibum and Ocular Surface in Healthy Subjects , 2020, Investigative ophthalmology & visual science.

[36]  Hei Sung Kim,et al.  Characterization and Analysis of the Skin Microbiota in Rosacea: Impact of Systemic Antibiotics , 2020, Journal of clinical medicine.

[37]  A. M. Smith,et al.  The diversity and abundance of fungi and bacteria on the healthy and dandruff affected human scalp , 2019, PloS one.

[38]  L. French,et al.  Corynebacterium kroppenstedtii subsp. demodicis is the endobacterium of Demodex folliculorum , 2019, Journal of the European Academy of Dermatology and Venereology : JEADV.

[39]  J. Kere,et al.  Microbe-host interplay in atopic dermatitis and psoriasis , 2019, Nature Communications.

[40]  C. Antonescu,et al.  Characterization and Analysis of the Skin Microbiota in Rosacea: A Case–Control Study , 2019, American Journal of Clinical Dermatology.

[41]  N. Shental,et al.  Skin Microbiome Compositional Changes in Atopic Dermatitis Accompany Dead Sea Climatotherapy , 2019, Photochemistry and photobiology.

[42]  G. Gerber,et al.  Microbiota Therapy Acts Via a Regulatory T Cell MyD88/RORγt Pathway to Suppress Food Allergy , 2019, Nature Medicine.

[43]  H. Kong,et al.  The microbiome in patients with atopic dermatitis , 2018, The Journal of allergy and clinical immunology.

[44]  Vineet K. Sharma,et al.  Comparison of Healthy and Dandruff Scalp Microbiome Reveals the Role of Commensals in Scalp Health , 2018, Front. Cell. Infect. Microbiol..

[45]  A. Galor,et al.  Effect of clinical parameters on the ocular surface microbiome in children and adults , 2018, Clinical ophthalmology.

[46]  Jose U. Scher,et al.  The Microbiome in Psoriasis and Psoriatic Arthritis: Joints , 2018, The Journal of Rheumatology. Supplement.

[47]  J. Knobloch,et al.  The role of the microbiome in psoriasis: moving from disease description to treatment selection? , 2018, The British journal of dermatology.

[48]  Jia Gu,et al.  fastp: an ultra-fast all-in-one FASTQ preprocessor , 2018, bioRxiv.

[49]  Daniel L. Popkin,et al.  Characterization of the facial microbiome in twins discordant for rosacea , 2018, Experimental dermatology.

[50]  Carolyn M. Ziemer,et al.  Trends in Eyelid Dermatitis. , 2018, Dermatitis : contact, atopic, occupational, drug.

[51]  E. Mongodin,et al.  427 Finegoldia magna and Corynebacterium kroppenstedtii are significantly enriched in rosacea independent of rosacea subtype: Results of a case-control study , 2017 .

[52]  P. Chang,et al.  Periocular dermatoses , 2017, International journal of women's dermatology.

[53]  Mina Rho,et al.  A Metagenomic Analysis Provides a Culture-Independent Pathogen Detection for Atopic Dermatitis , 2017, Allergy, asthma & immunology research.

[54]  M. Kleerebezem,et al.  Gram-positive anaerobe cocci are underrepresented in the microbiome of filaggrin-deficient human skin. , 2017, The Journal of allergy and clinical immunology.

[55]  C. Yuan,et al.  Dandruff is associated with the conjoined interactions between host and microorganisms , 2016, Scientific Reports.

[56]  D. Raoult,et al.  Bartonella quintana detection in Demodex from erythematotelangiectatic rosacea patients. , 2014, International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases.

[57]  J. Latgé,et al.  Correction: Dandruff Is Associated with Disequilibrium in the Proportion of the Major Bacterial and Fungal Populations Colonizing the Scalp , 2013, PLoS ONE.

[58]  Robert C. Edgar,et al.  UPARSE: highly accurate OTU sequences from microbial amplicon reads , 2013, Nature Methods.

[59]  J. Latgé,et al.  Dandruff Is Associated with Disequilibrium in the Proportion of the Major Bacterial and Fungal Populations Colonizing the Scalp , 2013, PloS one.

[60]  Pelin Yilmaz,et al.  The SILVA ribosomal RNA gene database project: improved data processing and web-based tools , 2012, Nucleic Acids Res..

[61]  Julia Oh,et al.  Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis , 2012, Genome research.

[62]  Tanja Magoc,et al.  FLASH: fast length adjustment of short reads to improve genome assemblies , 2011, Bioinform..

[63]  C. Huttenhower,et al.  Metagenomic biomarker discovery and explanation , 2011, Genome Biology.

[64]  Marcel Martin Cutadapt removes adapter sequences from high-throughput sequencing reads , 2011 .

[65]  J. Segre,et al.  The skin microbiome , 2011, Nature Reviews Microbiology.

[66]  L. Landeck,et al.  Periorbital contact sensitization. , 2010, American journal of ophthalmology.

[67]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[68]  S. Kežić,et al.  Natural moisturizing factor components in the stratum corneum as biomarkers of filaggrin genotype: evaluation of minimally invasive methods , 2009, The British journal of dermatology.

[69]  J. Hercogova Department of Dermatology and Venerology , 2009 .

[70]  V. Mahler,et al.  Periorbital dermatitis—a recalcitrant disease: causes and differential diagnoses , 2008, The British journal of dermatology.

[71]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[72]  G. Fabbrocini,et al.  Eyelid dermatitis: an evaluation of 447 patients. , 2003, American journal of contact dermatitis : official journal of the American Contact Dermatitis Society.

[73]  J. Guin Eyelid dermatitis: experience in 203 cases. , 2002, Journal of the American Academy of Dermatology.

[74]  R. Paus,et al.  Corticotropin releasing hormone and proopiomelanocortin involvement in the cutaneous response to stress. , 2000, Physiological reviews.

[75]  D. Murdoch Gram-Positive Anaerobic Cocci , 1998, Clinical Microbiology Reviews.

[76]  D. Tayloe,et al.  Pediatrics , 1927, The Indian Medical Gazette.

[77]  R. Wolf,et al.  Periorbital (eyelid) dermatides. , 2014, Clinics in dermatology.

[78]  Ben Nichols,et al.  Distributed under Creative Commons Cc-by 4.0 Vsearch: a Versatile Open Source Tool for Metagenomics , 2022 .