Ctrl-X, Ctrl-C and Ctrl-V in Veterinary Dermatology: Skin microbiota transplantation as a promising approach for dogs with cutaneous adverse food reactions

Authors

DOI:

https://doi.org/10.24215/15142590e080

Keywords:

atopic dermatitis, food intolerance, microbiota, skin, transfer

Abstract

The probability of influencing the skin microbiome for addressing skin disorders opens a novel aisle of therapy. This study aimed to evaluate the efficacy of skin microbiota transplantation (sMt) for cutaneous adverse food reactions (caFr) in dogs. Ten client-owned dogs with caFr were included in the study. Unenriched heterologous sMt was performed using Nivea Skin Refining Clear-Up Strips (N-cUs). The bacterial microbiota of skin samples was analysed by next-generation sequencing of the 16S rRNA gene. Other relevant biomarkers were involved in VAS (visual analogue scale of pruritus score), CADESI-04 (canine atopic dermatitis extent and severity index) and epidermal corneometric analysis. Increased Faecalibacterium (0 to 1.9 %), Peptoclostridium (5.49 % to 9.11 %) and Collinsella (0.65 % to 8.91 %), and decreased Fusobacterium (19.16 % to 9.06 %), Porphyromona (8.75 % to 0.13 %), Streptococcus (1.63 % to 0.14 %) and Staphylococcus (1.09 % to 0.49 %) was evidenced before and after sMt, respectively. Treatment with sMt effectively controlled clinical signs and drastically reduced median VAS pruritus (6.5 vs. 2) and CADESI-04 scores (74.50±22.62 to 19.30±11.30) (p<0,001). In addition, skin pH and hydration values were improved (p<0,001) after sMt. The heterologous and unenriched sMt with N-cUs could be responsible for the clinical recovery observed in this study.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

References

Bay L, Barnes CJ, Fritz BG, Thorsen J, Restrup MEM, Rasmussen L, Sørensen JK, Hesselvig AB, Odgaard A, Hansen AJ, Bjarnsholt T. 2020. Universal dermal microbiome in human skin. MBio. 11(1):e02945-19. https://doi.org/10.1128/mbio.02945-19

Callewaert C, Knödlseder N, Karoglan A, Güell M, Paetzold B. 2021. Skin microbiome transplantation and manipulation: Current state of the art. Computational and Structural Biotechnology Journal. 19:624-31. https://doi.org/10.1016/j.csbj.2021.01.001

Cho SS, Finocchiaro ET. 2010. Handbook of prebiotics and probiotics ingredients. U. S. A, CRC Press. Retrieved.

Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. 2009. Bacterial community variation in human body habitats across space and time. Science. 326:1694-7. https://doi.org/10.1126/science.1177486

D’hoe K, Vet S, Faust K, Moens F, Falony G, Gonze D, Lloréns-Rico V, Gelens L, Danckaert J, De Vuyst L, Raes J. 2018. Integrated culturing, modeling and transcriptomics uncovers complex interactions and emergent behavior in a three-species synthetic gut community. Elife. 7:e37090. https://doi.org/10.7554/eLife.37090

Dréno B, Araviiskaia E, Berardesca E, Gontijo G, Sanchez Viera M, Xiang LF, Martin R, Bieber T.2016. Microbiome in healthy skin, update for dermatologists. Journal of the European Academy of Dermatology and Venereology. 30(12):2038-47. https://doi.org/10.1111/jdv.13965

Esteban J, Nieto E, Calvo R, Fernández-Robals R, Valero-Guillén PL, Soriano F. 1999. Microbiological characterization and clinical significance of Corynebacteriumamycolatum strains. European Journal of Clinical Microbiology & Infectious Diseases. 18(7):518-21. https://doi.org/10.1007/s100960050336

Grice EA, Kong HH, Conlan S, Deming CB, Davis J, YoungAC, NISC Comparative Sequencing Program, Bouffard GG, Blakesley RW, Murray PR, Green ED, Turner ML, Segre JA. 2009. Topographical and temporal diversity of the human skin microbiome. Science. 324(5931):1190-2. https://doi.org/10.1126/science.1171700

Grice EA, Kong HH, Renaud G, Young AC, NISC Comparative Sequencing Program, Bouffard GG, Blakesley RW, Wolfsberg TG, Turner ML, Segre JA. 2008. A diversity profile of the human skin microbiota. Genome Research. 18(7):1043-50. https://doi.org/10.1101/gr.075549.107

Grice EA, Segre JA. 2011. The skin microbiome. Nature Reviews Microbiology. 9:244-53. https://doi.org/10.1038/nrmicro2537

Gunal M, Yayli G, Kaya O, Karahan N, Sulak O. 2006. The effects of antibiotic growth promoter, probiotic or organic acid supplementation on performance, intestinal microflora and tissue of broilers. International Journal of Poultry Science. 5:149-55. https://doi.org/10.9323/ijps.2006.149.155

Hammond AM, Monir RL, Schoch JJ. 2021. The role of the pediatric cutaneous and gut microbiomes in childhood disease: A review. Seminars in Perinatology. 45(6):151452. https://doi.org/10.1016/j.semperi.2021.151452

Hoek M. v, Merks RMH. 2017. Emergence of microbial diversity due to cross-feeding interactions in a spatial model of gut microbial metabolism. BMC Systems Biology. 11(1):1-18. https://doi.org/10.1186/s12918-017-0430-4

Inoue H, Someno T, Kawada M, Ikeda D. 2010. Citric acid inhibits a bacterial ceramidase and alleviates atopic dermatitis in an animal model. The Journal of Antibiotics. 63(10):611-13. https://doi.org/10.1038/ja.2010.91

Liang X, Ou C, Zhuang J, Li J, Zhang F, Zhong Y, Chen Y. 2021. Interplay Between Skin Microbiota Dysbiosis and the Host Immune System in Psoriasis: Potential Pathogenesis. Frontiers in Immunology. 12:764384. https://doi.org/10.3389/fimmu.2021.764384

Louis P, Flint HJ. 2017. Formation of propionate and butyrate by the human colonic microbiota. Environmental Microbiology. 19(1):29-41. https://doi.org/10.1111/1462-2920.13589

Martín A, Sierra MP, González JL, Arévalo MÁ. 2004. Identification of allergens responsible for canine cutaneous adverse food reactions to lamb, beef and cow's milk. Veterinary Dermatology. 15(6):349-56. https://doi.org/10.1111/j.1365-3164.2004.00404.x

Morris BE, Henneberger R, Huber H, Moissl-Eichinger C. 2013. Microbial syntrophy: interaction for the common good. FEMS Microbiology Reviews. 37(3):384-406. https://doi.org/10.1111/1574-6976.12019

Nakatsuji T, Chiang HI, Jiang SB, Nagarajan H, Zengler K, Gallo RL. 2013. The microbiome extends to subepidermal compartments of normal skin. Nature Communications. 4:1431. https://doi.org/10.1038/ncomms2441

Ogai K, Nagase S, Mukai K, Iuchi T, Mori Y, Matsue M, Sugitani K, Sugama J, Okomoto S. 2018. A comparison of techniques for collecting skin microbiome samples: swabbing versus tape-stripping. Frontiers in Microbiology. 9:2362. https://doi.org/10.3389/fmicb.2018.02362

Olivry T, Mueller RS. 2019.Critically appraised topic on adverse food reactions of companion animals (7): signalment and cutaneous manifestations of dogs and cats with adverse food reactions. BMC Veterinary Research. 15(1):140. https://doi.org/10.1186/s12917-019-1880-2

Olivry T, Saridomichelakis M, Nuttall T, Bensignor E, Griffin CE, Hill PB, International Committee on Allergic Diseases of Animals (ICADA).2014. Validation of the Canine Atopic Dermatitis Extent and Severity Index (CADESI)-4, a simplified severity scale for assessing skin lesions of atopic dermatitis in dogs. Veterinary Dermatology. 25(2):77-e25. https://doi.org/10.1111/vde.12107

Perin B, Addetia A, Qin X. 2019. Transfer of skin microbiota between two dissimilar autologous microenvironments: A pilot study. PLoS One. 14(12):e0226857. https://doi.org/10.1371/journal.pone.0226857

Rodrigues Hoffmann A, Patterson AP, Diesel A, Lawhon SD, Ly HJ, Elkins Stephenson C, Mansell J, Steiner JM, Dowd SE, Olivry T, Suchodolski JS. 2014. The skin microbiome in healthy and allergic dogs. PloS One. 9(1):e83197. https://doi.org/10.1371/journal.pone.0083197

Rondelli MCH, Oliveira MCdeC, daSilva FL, Palacios Junior RJG, Peixoto MC, Carciofi AC, Tinucci-Costa M.2015.A retrospective study of canine cutaneous food allergy at a Veterinary Teaching Hospital from Jaboticabal, São Paulo, Brazil. Ciência Rural. 45(10):1819-25. https://doi.org/10.1590/0103-8478cr20140440

Rungjang A, Meephansan J, Payungporn S, Sawaswong V, Chanchaem P, Pureesrisak P, Wongpiyabovorn J, Thio HB. 2022. Skin Microbiota Profiles from Tape Stripping and Skin Biopsy Samples of Patients with Psoriasis Treated with Narrowband Ultraviolet B. Clinical, Cosmetic and Investigational Dermatology. 15:1767-1778. https://doi.org/10.2147/CCID.S374871

Russel JB, Diez-Gonzalez F. 1998. The effect of fermentation acids on bacterial growth. Advances in Microbial Physiology. 39:205-34. https://doi.org/10.1016/S0065-2911(08)60017-X

Rybníček J, Lau‐Gillard PJ, Harvey R, Hill PB. 2009. Further validation of a pruritus severity scale for use in dogs. Veterinary Dermatology. 20(2):115-22. https://doi.org/10.1111/j.1365-3164.2008.00728.x

Schaub B, Lauener R, von Mutius E. 2006. The many faces of the hygiene hypothesis. Journal of Allergy and Clinical Immunology. 117(5):969-78. https://doi.org/10.1016/j.jaci.2006.03.003

Su LC, Xie Z, Zhang Y, Nguyen KT, Yang J. 2014. Study on the antimicrobial properties of citrate-based biodegradable polymers. Frontiers in Bioengineering and Biotechnology. 2:23. https://doi.org/10.3389/fbioe.2014.00023

Tang S, Prem A, Tjokrosurjo J, Sary M, Van Bel MA, Rodrigues-Hoffmann A, Kavanagh M, Wu G, Van Eden ME, Kurumbeck JA. 2020. The canine skin and ear microbiome: A comprehensive survey of pathogens implicated in canine skin and ear infections using a novel next-generation-sequencing-based assay. Veterinary Microbiology. 247:108764. https://doi.org/10.1016/j.vetmic.2020.108764

Tizard IR, Jones SW. 2018. The microbiota regulates immunity and immunologic diseases in dogs and cats. The Veterinary Clinics of North America: Small Animal Practice. 48(2):307-22. https://doi.org/10.1016/j.cvsm.2017.10.008

Ural K, Erdoğan H, Erdoğan S. 2022. Heterologue skin microbiota transplantation for treatment of sarcoptic mange in two dogs with zoonotic transmission. Bozok Veterinary Sciences. 3(2):52-6. https://doi.org/10.58833/bozokvetsci.1207900

Ural K, Erdoğan H, Erdoğan S. 2023. Skin microbiota transplantation by Nivea Refining Clear-Up Strips could reverse erythema scores in dogs with atopic dermatitis: Novel strategy for skin microbiome manipulation. Turkiye Klinikleri Journal of Veterinary Sciences.14(1):11-7. https://doi.org/10.5336/vetsci.2022-93888

Zeeuwen PL, Boekhorst J, van den Bogaard EH, de Koning HD, van de Kerkhof PM, Saulnier DM, van Swam II, van Hijum SA, Kleerebezem M, Schalkwijk J, Timmerman HM. 2012. Microbiome dynamics of human epidermis following skin barrier disruption. Genome Biology. 13:R101. https://doi.org/10.1186/gb-2012-13-11-r101

Published

2024-04-16

How to Cite

Ural, K., Erdoğan, H., & Erdoğan, S. (2024). Ctrl-X, Ctrl-C and Ctrl-V in Veterinary Dermatology: Skin microbiota transplantation as a promising approach for dogs with cutaneous adverse food reactions. Analecta Veterinary, 44, 080. https://doi.org/10.24215/15142590e080

Issue

Section

Research Articles