Aspergillosis; Chronic idiopathic rhinitis; Dog; Fungal rhinitis; Microbiota; Mycotic rhinitis; Nasal; Nasal cavity; Dogs; Animals; Nose; Rhinitis/veterinary; Rhinitis/diagnosis; Rhinitis/microbiology; Dog Diseases/drug therapy; Nose Neoplasms/diagnosis; Nose Neoplasms/veterinary; Dog Diseases; Nose Neoplasms; Rhinitis; Microbiology; Microbiology (medical)
Abstract :
[en] [en] BACKGROUND: Pathogenesis of canine fungal rhinitis is still not fully understood. Treatment remains challenging, after cure turbinate destruction may be associated with persistent clinical signs and recurrence of fungal rhinitis can occur. Alterations of the nasal microbiota have been demonstrated in dogs with chronic idiopathic rhinitis and nasal neoplasia, although whether they play a role in the pathogenesis or are a consequence of the disease is still unknown. The objectives of the present study were (1) to describe nasal microbiota alterations associated with fungal rhinitis in dogs, compared with chronic idiopathic rhinitis and controls, (2) to characterize the nasal microbiota modifications associated with successful treatment of fungal rhinitis. Forty dogs diagnosed with fungal rhinitis, 14 dogs with chronic idiopathic rhinitis and 29 healthy control dogs were included. Nine of the fungal rhinitis dogs were resampled after successful treatment with enilconazole infusion.
RESULTS: Only disease status contributed significantly to the variability of the microbiota. The relative abundance of the genus Moraxella was decreased in the fungal rhinitis (5.4 ± 18%) and chronic idiopathic rhinitis (4.6 ± 8.7%) groups compared to controls (51.8 ± 39.7%). Fungal rhinitis and chronic idiopathic rhinitis groups also showed an increased richness and α-diversity at species level compared with controls. Increase in unique families were associated with fungal rhinitis (Staphyloccaceae, Porphyromonadaceae, Enterobacteriaceae and Neisseriaceae) and chronic idiopathic rhinitis (Pasteurellaceae and Lactobacillaceae). In dogs with fungal rhinitis at cure, only 1 dog recovered a high relative abundance of Moraxellaceae.
CONCLUSIONS: Results confirm major alterations of the nasal microbiota in dogs affected with fungal rhinitis and chronic idiopathic rhinitis, consisting mainly in a decrease of Moraxella. Besides, a specific dysbiotic profile further differentiated fungal rhinitis from chronic idiopathic rhinitis. In dogs with fungal rhinitis, whether the NM returns to its pre-infection state or progresses toward chronic idiopathic rhinitis or fungal rhinitis recurrence warrants further investigation.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Vangrinsven, Emilie ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Médecine vétérinaire comparée
Fastrès, Aline ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Médecine vétérinaire comparée
Taminiau, Bernard ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Billen, Frédéric ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Médecine vétérinaire comparée
Daube, Georges ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Clercx, Cécile ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Médecine vétérinaire comparée
Language :
English
Title :
Assessment of the nasal microbiota in dogs with fungal rhinitis before and after cure and in dogs with chronic idiopathic rhinitis.
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Bibliography
Bassis CM, Tang AL, Young VB, Pynnonen MA. The nasal cavity microbiota of healthy adults. Microbiome. 2014;2:27. 10.1186/2049-2618-2-27. DOI: 10.1186/2049-2618-2-27
Lal D, Keim P, Delisle J, et al. Mapping and comparing bacterial microbiota in the sinonasal cavity of healthy, allergic rhinitis, and chronic rhinosinusitis subjects. Int Forum Allergy Rhinol. 2017;7(6):561–9. 10.1002/alr.21934. DOI: 10.1002/alr.21934
Salzano FA, Marino L, Salzano G, et al. Microbiota composition and the integration of exogenous and endogenous signals in reactive nasal inflammation. J Immunol Res. 2018;2018:2724951. 10.1155/2018/2724951. DOI: 10.1155/2018/2724951
Kumpitsch C, Koskinen K, Schöpf V, Moissl-Eichinger C. The microbiome of the upper respiratory tract in health and disease. BMC Biol. 2019;17(1):87. 10.1186/s12915-019-0703-z. DOI: 10.1186/s12915-019-0703-z
Elgamal Z, Singh P, Geraghty P. The upper airway microbiota, environmental exposures, inflammation, and disease. Medicina (Kaunas). 2021;57(8):823. 10.3390/medicina57080823. DOI: 10.3390/medicina57080823
Gan W, Yang F, Meng J, Liu F, Liu S, Xian J. Comparing the nasal bacterial microbiome diversity of allergic rhinitis, chronic rhinosinusitis and control subjects. Eur Arch Otorhinolaryngol. 2021;278(3):711–8. 10.1007/s00405-020-06311-1. DOI: 10.1007/s00405-020-06311-1
Banks KC, Giuliano EA, Busi SB, Reinero CR, Ericsson AC. Evaluation of healthy canine conjunctival, periocular haired skin, and nasal microbiota compared to conjunctival Culture. Front Vet Sci. 2020;7:558. 10.3389/fvets.2020.00558. DOI: 10.3389/fvets.2020.00558
Ericsson AC, Personett AR, Grobman ME, Rindt H, Reinero CR. Composition and predicted metabolic capacity of upper and lower airway microbiota of healthy dogs in relation to the fecal microbiota. PLoS One. 2016;11(5):e0154646. 10.1371/journal.pone.0154646. DOI: 10.1371/journal.pone.0154646
Isaiah A, Hoffmann AR, Kelley R, Mundell P, Steiner JM, Suchodolski JS. Characterization of the nasal and oral microbiota of detection dogs. PLoS One. 2017;12(9):e0184899. 10.1371/journal.pone.0184899. DOI: 10.1371/journal.pone.0184899
Tress B, Dorn ES, Suchodolski JS, et al. Bacterial microbiome of the nose of healthy dogs and dogs with nasal disease. PLoS One. 2017;12(5):e0176736. 10.1371/journal.pone.0176736. DOI: 10.1371/journal.pone.0176736
Rodriguez C, Taminiau B, Bouchafa L, et al. Clostridium difficile beyond stools: dog nasal discharge as a possible new vector of bacterial transmission [published correction appears in. Heliyon. 2019;5(6):e01890. 10.1016/j.heliyon.2019.e01629. DOI: 10.1016/j.heliyon.2019.e01629
Vangrinsven E, Fastrès A, Taminiau B, Frédéric B, Daube G, Clercx C. Variations in facial conformation are associated with differences in nasal microbiota in healthy dogs [published correction appears in BMC. Vet Res. 2022;18(1):100. 10.1186/s12917-021-03055-w. DOI: 10.1186/s12917-021-03055-w
Peeters D, Clercx C. Update on canine sinonasal aspergillosis. Vet Clin North Am Small Anim Pract. 2007;37(5):901. 10.1016/j.cvsm.2007.05.005. DOI: 10.1016/j.cvsm.2007.05.005
Vanherberghen M, Bureau F, Peters IR, Day MJ, Clercx C, Peeters D. Analysis of gene expression in canine sino-nasal aspergillosis and idiopathic lymphoplasmacytic rhinitis: a transcriptomic analysis. Vet Microbiol. 2012;157(1–2):143–51. 10.1016/j.vetmic.2011.12.009. DOI: 10.1016/j.vetmic.2011.12.009
Valdes ID, der Hart Ruijter ABP, Torres CJ, Breuker JCA, Wösten HAB, de Cock H. The sino-nasal warzone: transcriptomic and genomic studies on sino-nasal aspergillosis in dogs. NPJ Biofilms Microbiomes. 2020;6(1):51. DOI: 10.1038/s41522-020-00163-7
Peeters D, Peters IR, Clercx C, Day MJ. Quantification of mRNA encoding cytokines and chemokines in nasal biopsies from dogs with sino-nasal aspergillosis. Vet Microbiol. 2006;114(3–4):318–26. 10.1016/j.vetmic.2005.11.065. DOI: 10.1016/j.vetmic.2005.11.065
Peeters D, Peters IR, Helps CR, Gabriel A, Day MJ, Clercx C. Distinct tissue cytokine and chemokine mRNA expression in canine sino-nasal aspergillosis and idiopathic lymphoplasmacytic rhinitis. Vet Immunol Immunopathol. 2007;117(1–2):95–105. 10.1016/j.vetimm.2007.01.018. DOI: 10.1016/j.vetimm.2007.01.018
Valdes ID, van den Berg J, Haagsman A, et al. Comparative genotyping and phenotyping of Aspergillus fumigatus isolates from humans, dogs and the environment. BMC Microbiol. 2018;18(1):118. 10.1186/s12866-018-1244-2. DOI: 10.1186/s12866-018-1244-2
Romani L, Zelante T, Palmieri M, et al. The cross-talk between opportunistic fungi and the mammalian host via microbiota’s metabolism. Semin Immunopathol. 2015;37(2):163–71. 10.1007/s00281-014-0464-2. DOI: 10.1007/s00281-014-0464-2
Gonçalves SM, Lagrou K, Duarte-Oliveira C, Maertens JA, Cunha C, Carvalho A. The microbiome-metabolome crosstalk in the pathogenesis of respiratory fungal diseases. Virulence. 2017;8(6):673–84. 10.1080/21505594.2016.1257458. DOI: 10.1080/21505594.2016.1257458
Libertucci J, Young VB. The role of the microbiota in infectious diseases. Nat Microbiol. 2019;4(1):35–45. 10.1038/s41564-018-0278-4. DOI: 10.1038/s41564-018-0278-4
Man WH, de SteenhuijsenPiters WA, Bogaert D. The microbiota of the respiratory tract: gatekeeper to respiratory health. Nat Rev Microbiol. 2017;15(5):259–70. 10.1038/nrmicro.2017.14. DOI: 10.1038/nrmicro.2017.14
De Rudder C, Calatayud Arroyo M, Lebeer S, Van de Wiele T. Modelling upper respiratory tract diseases: getting grips on host-microbe interactions in chronic rhinosinusitis using in vitro technologies. Microbiome. 2018;6(1):75. 10.1186/s40168-018-0462-z. DOI: 10.1186/s40168-018-0462-z
Lee K, Pletcher SD, Lynch SV, Goldberg AN, Cope EK. Heterogeneity of microbiota dysbiosis in chronic rhinosinusitis: potential clinical implications and microbial community mechanisms contributing to sinonasal inflammation. Front Cell Infect Microbiol. 2018;8:168. 10.3389/fcimb.2018.00168. DOI: 10.3389/fcimb.2018.00168
Kolwijck E, van de Veerdonk FL. The potential impact of the pulmonary microbiome on immunopathogenesis of Aspergillus-related lung disease. Eur J Immunol. 2014;44(11):3156–65. 10.1002/eji.201344404. DOI: 10.1002/eji.201344404
Boase S, Jervis-Bardy J, Cleland E, Pant H, Tan L, Wormald PJ. Bacterial-induced epithelial damage promotes fungal biofilm formation in a sheep model of sinusitis. Int Forum Allergy Rhinol. 2013;3(5):341–8. 10.1002/alr.21138. DOI: 10.1002/alr.21138
Briard B, Heddergott C, Latgé JP. Volatile compounds emitted by pseudomonas aeruginosa stimulate growth of the fungal pathogen aspergillus fumigatus. mBio. 2016;7(2):00219. DOI: 10.1128/mBio.00219-16
Windsor RC, Johnson LR. Canine chronic inflammatory rhinitis. Clin Tech Small Anim Pract. 2006;21(2):76–81. 10.1053/j.ctsap.2005.12.014. DOI: 10.1053/j.ctsap.2005.12.014
Abreu NA, Nagalingam NA, Song Y, et al. Sinus microbiome diversity depletion and Corynebacterium tuberculostearicum enrichment mediates rhinosinusitis. Sci Transl Med. 2012;4(151):151ra124. 10.1126/scitranslmed.3003783. DOI: 10.1126/scitranslmed.3003783
Hoggard M, Biswas K, Zoing M, Wagner Mackenzie B, Taylor MW, Douglas RG. Evidence of microbiota dysbiosis in chronic rhinosinusitis. Int Forum Allergy Rhinol. 2017;7(3):230–9. 10.1002/alr.21871. DOI: 10.1002/alr.21871
Copeland E, Leonard K, Carney R, et al. Chronic rhinosinusitis: potential role of microbial dysbiosis and recommendations for sampling sites. Front Cell Infect Microbiol. 2018;8:57. 10.3389/fcimb.2018.00057. DOI: 10.3389/fcimb.2018.00057
Cho DY, Hunter RC, Ramakrishnan VR. The microbiome and chronic rhinosinusitis. Immunol Allergy Clin North Am. 2020;40(2):251–63. 10.1016/j.iac.2019.12.009. DOI: 10.1016/j.iac.2019.12.009
Galli J, Calò L, Ardito F, et al. Damage to ciliated epithelium in chronic rhinosinusitis: what is the role of bacterial biofilms? Ann Otol Rhinol Laryngol. 2008;117(12):902–8. 10.1177/000348940811701207. DOI: 10.1177/000348940811701207
Sharman M, Paul A, Davies D, et al. Multi-centre assessment of mycotic rhinosinusitis in dogs: a retrospective study of initial treatment success (1998 to 2008). J Small Anim Pract. 2010;51(8):423–7. 10.1111/j.1748-5827.2010.00957.x. DOI: 10.1111/j.1748-5827.2010.00957.x
Billen F, Peeters D. Aspergillosis - canine. In: Ettinger SJ, Feldman EC, Côté E, editors. Textbook of Veterinary Internal Medicine. 8th ed. St Louis: Elsevier; 2017. p. 1035–9.
Vangrinsven E, Taminiau B, Roels E, Fastrès F, Auquier C, Billen F, Daube G, Clercx C. Investigation of the nasal microbiota in healthy dolichocephalic dogs and dogs with sinonasal aspergillosis. Poster session presented at: 27th Congress of the European college of veterinary internal medicine - companion animals; 2017 September 14–16, St. Julian's, Malta.
Rodrigues Hoffmann A, Patterson AP, Diesel A, et al. The skin microbiome in healthy and allergic dogs. PLoS One. 2014;9(1):e83197. Published 2014 Jan 8. 10.1371/journal.pone.0083197. DOI: 10.1371/journal.pone.0083197
Biesbroek G, Tsivtsivadze E, Sanders EA, et al. Early respiratory microbiota composition determines bacterial succession patterns and respiratory health in children. Am J Respir Crit Care Med. 2014;190(11):1283–92. 10.1164/rccm.201407-1240OC. DOI: 10.1164/rccm.201407-1240OC
Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. Bacterial community variation in human body habitats across space and time. Science. 2009;326(5960):1694–7. 10.1126/science.1177486. DOI: 10.1126/science.1177486
Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207–14. 10.1038/nature11234. DOI: 10.1038/nature11234
Jain R, Hoggard M, Zoing M, et al. The effect of medical treatments on the bacterial microbiome in patients with chronic rhinosinusitis: a pilot study [published online ahead of print, 2018 Mar 8]. Int Forum Allergy Rhinol. 2018; https://doi.org/10.1002/alr.22110.
Wang JH, Lee BJ, Jang YJ. Bacterial coinfection and antimicrobial resistance in patients with paranasal sinus fungus balls. Ann Otol Rhinol Laryngol. 2010;119(6):406–11. 10.1177/000348941011900608.
Brook I. Recovery of aerobic and anaerobic bacteria in sinus fungal ball. Otolaryngol Head Neck Surg. 2011;145(5):851–2. 10.1177/0194599811417066. DOI: 10.1177/0194599811417066
Hauser LJ, Ir D, Kingdom TT, Robertson CE, Frank DN, Ramakrishnan VR. Investigation of bacterial repopulation after sinus surgery and perioperative antibiotics. Int Forum Allergy Rhinol. 2016;6(1):34–40. 10.1002/alr.21630. DOI: 10.1002/alr.21630
Horiguchi Y. Swine atrophic rhinitis caused by pasteurella multocida toxin and bordetella dermonecrotic toxin. Curr Top Microbiol Immunol. 2012;361:113–29. 10.1007/82_2012_206. DOI: 10.1007/82_2012_206
Kim SY, Adachi Y. Biological and genetic classification of canine intestinal lactic acid bacteria and bifidobacteria. Microbiol Immunol. 2007;51(10):919–28. 10.1111/j.1348-0421.2007.tb03983.x. DOI: 10.1111/j.1348-0421.2007.tb03983.x
Delucchi L, Fraga M, Perelmuter K, Cidade E, Zunino P. Vaginal lactic acid bacteria in healthy and ill bitches and evaluation of in vitro probiotic activity of selected isolates. Can Vet J. 2008;49(10):991–4.
Coman MM, Verdenelli MC, Cecchini C, et al. Probiotic characterization of Lactobacillus isolates from canine faeces. J Appl Microbiol. 2019;126(4):1245–56. 10.1111/jam.14197. DOI: 10.1111/jam.14197
Fernández L, Martínez R, Pérez M, Arroyo R, Rodríguez JM. Characterization of Lactobacillus rhamnosus MP01 and Lactobacillus plantarum MP02 and assessment of their potential for the prevention of gastrointestinal infections in an experimental canine model. Front Microbiol. 2019;10:1117. 10.3389/fmicb.2019.01117. DOI: 10.3389/fmicb.2019.01117
EFSA Panel on Additives and Products or Substances used in Animal Feed (FEEDAP), Rychen G, Aquilina G, et al. Safety and efficacy of Lactobacillus acidophilus D2/CSL Lactobacillus acidophilus CECT 4529 as a feed additive for cats and dogs. EFSA J. 2018;16(5):05278.
EFSA Panel on Additives and Products or Substances used in Animal Feed (FEEDAP), Bampidis V, Azimonti G, et al. Safety and efficacy of Lactobacillus reuteri NBF-1 (DSM 32203) as a feed additive for dogs. EFSA J. 2019;17(1):e05524. Published 2019 Jan 11. https://doi.org/10.2903/j.efsa.2019.5524.
Antoun M, Hattab Y, Akhrass FA, Hamilton LD. Uncommon Pathogen, Lactobacillus, Causing Infective Endocarditis: Case Report and Review. Case Rep Infect Dis. 2020;2020:8833948. Published 2020 Nov 5. https://doi.org/10.1155/2020/8833948.
Liu CM, Soldanova K, Nordstrom L, et al. Medical therapy reduces microbiota diversity and evenness in surgically recalcitrant chronic rhinosinusitis. Int Forum Allergy Rhinol. 2013;3(10):775–81. 10.1002/alr.21195. DOI: 10.1002/alr.21195
Merkley MA, Bice TC, Grier A, Strohl AM, Man LX, Gill SR. The effect of antibiotics on the microbiome in acute exacerbations of chronic rhinosinusitis. Int Forum Allergy Rhinol. 2015;5(10):884–93. 10.1002/alr.21591. DOI: 10.1002/alr.21591
Cherian LM, Bassiouni A, Cooksley CM, Vreugde S, Wormald PJ, Psaltis AJ. The clinical outcomes of medical therapies in chronic rhinosinusitis are independent of microbiomic outcomes: a double-blinded, randomised placebo-controlled trial. Rhinology. 2020;58(6):559–67. 10.4193/Rhin20.055. DOI: 10.4193/Rhin20.055
Vangrinsven E, Girod M, Goossens D, Desquilbet L, Clercx C, Billen F. Comparison of two minimally invasive enilconazole perendoscopic infusion protocols for the treatment of canine sinonasal aspergillosis. J Small Anim Pract. 2018;59(12):777–82. 10.1111/jsap.12933.
Fastrès A, Taminiau B, Vangrinsven E, et al. Effect of an antimicrobial drug on lung microbiota in healthy dogs. Heliyon. 2019;5(11):e02802. Published 2019 Nov 14. https://doi.org/10.1016/j.heliyon.2019.e02802.
Rognes T, Flouri T, Nichols B, Quince C, Mahé F. VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016;4:e2584. 10.7717/peerj.2584. DOI: 10.7717/peerj.2584
Oksanen J, Blanchet G, et al. vegan: Community Ecology Package. R package version 2.5–2. https://CRAN.R-project.org/package=vegan (2018). Accessed 28 nov 2020.
Segata N, Izard J, Waldron L, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12(6):R60. 10.1186/gb-2011-12-6-r60. DOI: 10.1186/gb-2011-12-6-r60
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