Nasopharyngeal Microbiomes in Donkeys Shedding Streptococcus equi Subspecies equi in Comparison to Healthy Donkeys.
Abstract: subsp. equi () is the pathogen causing strangles, a highly infectious disease that can affect equids including donkeys of all ages. It can persistently colonize the upper respiratory tract of animals asymptomatically for years, which serves as a source of infection. Several strangles outbreaks have been reported in the donkey industry in China in the last few years and pose a great threat to health, production, and the welfare of donkeys. Nasopharyngeal swab samples for culture and PCR are used widely in strangles diagnosis. Additionally, microbiomes within and on the body are essential to host homoeostasis and health. Therefore, the microbiome of the equid nasopharynx may provide insights into the health of the upper respiratory tract in animals. There has been no study investigating the nasopharyngeal microbiome in healthy donkeys, nor in donkeys shedding . This study aimed to compare nasopharyngeal microbiomes in healthy and carrier donkeys using 16S rRNA gene sequencing. Nasopharyngeal samples were obtained from 16 donkeys recovered from strangles (group S) and 14 healthy donkeys with no history of strangles exposure (group H). Of those sampled, 7 donkeys were determined to be carriers with positive PCR and culture results in group S. In group H, all 14 donkeys were considered free of strangles based on the history of negative exposure, negative results of PCR and culture. Samples from these 21 donkeys were used for microbial analysis. The nasopharyngeal microbiome composition was compared between the two groups. At the phylum level, relative abundance of Proteobacteria was predominantly higher in the carrier donkeys than in healthy donkeys ( < 0.01), while Firmicutes and Actinobacteria were significantly less abundant in the carrier donkeys than in healthy donkeys ( < 0.05). At the genus level, was detected in the upper respiratory tract of donkeys for the first time and dominated in carrier donkeys. It is suspected to suppress other normal flora of URT microbiota including spp., spp., and spp. We concluded that the nasopharyngeal microbiome in carrier donkeys still exhibited microbial dysbiosis, which might predispose them to other airway diseases.
Copyright © 2021 Zhu, Chen, Yi, Holyoak, Wang, Ding and Li.
Publication Date: 2021-04-22 PubMed ID: 33969039PubMed Central: PMC8100518DOI: 10.3389/fvets.2021.645627Google Scholar: Lookup
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- Journal Article
Summary
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The research investigates the differences in nasopharyngeal microbiomes between healthy donkeys and ones that are carriers of Streptococcus equi, a pathogen that causes strangles, a severe infection affecting equids. The study indicates that carrier donkeys exhibit significant changes in their nasopharyngeal microbiomes, potentially making them more susceptible to other diseases.
Objective and Methodology
- The aim of this study was to compare the nasopharyngeal microbiomes in healthy donkeys and carrier donkeys. This was achieved through 16S rRNA gene sequencing, a technique often used to investigate microbial communities.
- Two groups of donkeys were examined in this study. Group S consisted of 16 donkeys that had recovered from strangles, among which seven were identified as carriers based on positive PCR and culture results. In contrast, Group H encompassed 14 healthy donkeys with no history of strangles, all of whom were determined to be free of the disease. The nasopharyngeal samples from a total of 21 donkeys from both groups were then used for microbial analysis.
Results
- The study found that the composition of the nasopharyngeal microbiome significantly varied between the two groups. Specifically, a higher relative abundance of Proteobacteria was observed in carrier donkeys, while the amounts of Firmicutes and Actinobacteria were noticeably lower compared to their healthy counterparts.
- At the genus level, the pathogen Streptococcus equi was spotted for the first time in the upper respiratory tract of donkeys, predominantly in those identified as carriers. Alongside this, it was noted that the presence of this bacterium might suppress other normal flora of the upper respiratory tract microbiota, including Streptococcus spp., Pasteurella spp., and Actinobacillus spp.
Conclusions
- These findings led researchers to conclude that donkeys carrying Streptococcus equi show signs of microbial dysbiosis in their nasopharyngeal microbiomes. Dysbiosis refers to an imbalance or maladjustment in the microbiomes, potentially predisposing these donkeys to other diseases affecting the airway.
Cite This Article
APA
Zhu Y, Chen S, Yi Z, Holyoak R, Wang T, Ding Z, Li J.
(2021).
Nasopharyngeal Microbiomes in Donkeys Shedding Streptococcus equi Subspecies equi in Comparison to Healthy Donkeys.
Front Vet Sci, 8, 645627.
https://doi.org/10.3389/fvets.2021.645627 Publication
Researcher Affiliations
- Equine Clinical Diagnostic Center, College of Veterinary Medicine, China Agricultural University, Beijing, China.
- Equine Clinical Diagnostic Center, College of Veterinary Medicine, China Agricultural University, Beijing, China.
- Equine Clinical Diagnostic Center, College of Veterinary Medicine, China Agricultural University, Beijing, China.
- College of Veterinary Medicine, Oklahoma State University, Stillwater, OK, United States.
- Dong-E-E-Jiao Co., Ltd., Dong-E County, China.
- Dong-E-E-Jiao Co., Ltd., Dong-E County, China.
- Equine Clinical Diagnostic Center, College of Veterinary Medicine, China Agricultural University, Beijing, China.
Conflict of Interest Statement
TW and ZD were employed by the company Dong-E-E-Jiao Co., Ltd. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
This article includes 55 references
- Newton JR, Wood JL, Dunn KA, DeBrauwere MN, Chanter N. Naturally occurring persistent and asymptomatic infection of the guttural pouches of horses with Streptococcus equi.. Vet Rec 1997 Jan 25;140(4):84-90.
- Slater JD. Strangles, bastard strangles, vives and glanders: archaeological relics in a genomic age.. Equine Vet J 2003 Mar;35(2):118-20.
- Robinson C, Waller AS, Frykberg L, Flock M, Zachrisson O, Guss B, Flock JI. Intramuscular vaccination with Strangvac is safe and induces protection against equine strangles caused by Streptococcus equi.. Vaccine 2020 Jun 26;38(31):4861-4868.
- Sweeney CR, Whitlock RH, Meirs DA, Whitehead SC, Barningham SO. Complications associated with Streptococcus equi infection on a horse farm.. J Am Vet Med Assoc 1987 Dec 1;191(11):1446-8.
- Libardoni F, Machado G, Gressler LT, Kowalski AP, Diehl GN, dos Santos LC, Corbellini LG, de Vargas AC. Prevalence of Streptococcus equi subsp. equi in horses and associated risk factors in the State of Rio Grande do Sul, Brazil.. Res Vet Sci 2016 Feb;104:53-7.
- Boyle AG, Timoney JF, Newton JR, Hines MT, Waller AS, Buchanan BR. Streptococcus equi Infections in Horses: Guidelines for Treatment, Control, and Prevention of Strangles-Revised Consensus Statement.. J Vet Intern Med 2018 Mar;32(2):633-647.
- Sweeney CR, Timoney JF, Newton JR, Hines MT. Streptococcus equi infections in horses: guidelines for treatment, control, and prevention of strangles.. J Vet Intern Med 2005 Jan-Feb;19(1):123-34.
- Whelchel DD, Arnold CE, Chaffin MK. Subscapular lymph node abscessation as a result of metastatic Streptococcus equi subspecies equi infection: an atypical presentation of bastard strangles in a mare. Equine Vet Educ (2009) 21:131–4.
- Boyle AG. Strangles and its complications. Equine Vet Educ (2017) 29:149–57.
- Swerczek TW. Exacerbation of Streptococcus equi (strangles) by overly nutritious diets in horses: a model for infectious bacterial diseases of horses and other livestock. Anim Vet Sci (2019) 7:18–23.
- George JL, Reif JS, Shideler RK, Small CJ, Ellis RP, Snyder SP, McChesney AE. Identification of carriers of Streptococcus equi in a naturally infected herd.. J Am Vet Med Assoc 1983 Jul 1;183(1):80-4.
- Chanter N, Newton JR, Wood JL, Verheyen K, Hannant D. Detection of strangles carriers.. Vet Rec 1998 May 2;142(18):496.
- Dong J, Gao N, Waller AS, Cook FR, Fan S, Yuan D, Du Y, Li F, Norimine J, Zhu W. An outbreak of strangles associated with a novel genotype of Streptococcus equi subspecies equi in donkeys in China during 2018.. Equine Vet J 2019 Nov;51(6):743-748.
- Liu Y, Gao N, He D, Waller A, Gu J, Wang T, Han W. Identification of a novel genotype of Streptococcus equi subspecies equi in a donkey suffering from strangles. Pak Vet J 39:609–11.
- Bosch AA, Biesbroek G, Trzcinski K, Sanders EA, Bogaert D. Viral and bacterial interactions in the upper respiratory tract.. PLoS Pathog 2013 Jan;9(1):e1003057.
- Man WH, de Steenhuijsen Piters WA, Bogaert D. The microbiota of the respiratory tract: gatekeeper to respiratory health.. Nat Rev Microbiol 2017 May;15(5):259-270.
- Zhao F, Jiang G, Ji C, Zhang Z, Gao W, Feng P, Li H, Li M, Liu H, Liu G, Magalhaes HB, Li J. Effects of long-distance transportation on blood constituents and composition of the nasal microbiota in healthy donkeys.. BMC Vet Res 2020 Sep 15;16(1):338.
- Niederwerder MC. Role of the microbiome in swine respiratory disease.. Vet Microbiol 2017 Sep;209:97-106.
- Allen EK, Koeppel AF, Hendley JO, Turner SD, Winther B, Sale MM. Characterization of the nasopharyngeal microbiota in health and during rhinovirus challenge.. Microbiome 2014;2:22.
- Schenck LP, Surette MG, Bowdish DM. Composition and immunological significance of the upper respiratory tract microbiota.. FEBS Lett 2016 Nov;590(21):3705-3720.
- Holman DB, McAllister TA, Topp E, Wright AD, Alexander TW. The nasopharyngeal microbiota of feedlot cattle that develop bovine respiratory disease.. Vet Microbiol 2015 Oct 22;180(1-2):90-5.
- Artiushin S, Timoney JF. PCR for detection of Streptococcus equi.. Adv Exp Med Biol 1997;418:359-61.
- Pusterla N, Mapes S, Wilson WD. Diagnostic sensitivity of nasopharyngeal and nasal swabs for the molecular detection of EHV-1.. Vet Rec 2008 Apr 19;162(16):520-1.
- Newton JR, Verheyen K, Talbot NC, Timoney JF, Wood JL, Lakhani KH, Chanter N. Control of strangles outbreaks by isolation of guttural pouch carriers identified using PCR and culture of Streptococcus equi.. Equine Vet J 2000 Nov;32(6):515-26.
- Cordoni G, Williams A, Durham A, Florio D, Zanoni RG, La Ragione RM. Rapid diagnosis of strangles (Streptococcus equi subspecies equi) using PCR.. Res Vet Sci 2015 Oct;102:162-6.
- Neefs JM, Van de Peer Y, De Rijk P, Chapelle S, De Wachter R. Compilation of small ribosomal subunit RNA structures.. Nucleic Acids Res 1993 Jul 1;21(13):3025-49.
- Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor.. Bioinformatics 2018 Sep 1;34(17):i884-i890.
- Goodrich JK, Di Rienzi SC, Poole AC, Koren O, Walters WA, Caporaso JG, Knight R, Ley RE. Conducting a microbiome study.. Cell 2014 Jul 17;158(2):250-262.
- Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads.. Nat Methods 2013 Oct;10(10):996-8.
- Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. QIIME allows analysis of high-throughput community sequencing data.. Nat Methods 2010 May;7(5):335-6.
- Taylor SD, Wilson WD. Streptococcus equi subsp. equi (strangles) infection. Clin Tech Equine Pract (2006) 5:211–17.
- Lindahl S, Båverud V, Egenvall A, Aspán A, Pringle J. Comparison of sampling sites and laboratory diagnostic tests for S. equi subsp. equi in horses from confirmed strangles outbreaks.. J Vet Intern Med 2013 May-Jun;27(3):542-7.
- Davidson A, Traub-Dargatz JL, Magnuson R, Hill A, Irwin V, Newton R, Waller A, Smith K, Callan RJ, Meehan M, Owen P, Salman M. Lack of correlation between antibody titers to fibrinogen-binding protein of Streptococcus equi and persistent carriers of strangles.. J Vet Diagn Invest 2008 Jul;20(4):457-62.
- Knowles EJ, Mair TS, Butcher N, Waller AS, Wood JL. Use of a novel serological test for exposure to Streptococcus equi subspecies equi in hospitalised horses.. Vet Rec 2010 Mar 6;166(10):294-7.
- North SE, Wakeley PR, Mayo N, Mayers J, Sawyer J. Development of a real-time PCR to detect Streptococcus equi subspecies equi.. Equine Vet J 2014 Jan;46(1):56-9.
- Pusterla N, Leutenegger CM, Barnum SM, Byrne BA. Use of quantitative real-time PCR to determine viability of Streptococcus equi subspecies equi in respiratory secretions from horses with strangles.. Equine Vet J 2018 Sep;50(5):697-700.
- Bond SL, Timsit E, Workentine M, Alexander T, Léguillette R. Upper and lower respiratory tract microbiota in horses: bacterial communities associated with health and mild asthma (inflammatory airway disease) and effects of dexamethasone.. BMC Microbiol 2017 Aug 23;17(1):184.
- Welp AL, Bomberger JM. Bacterial Community Interactions During Chronic Respiratory Disease.. Front Cell Infect Microbiol 2020;10:213.
- Lawley TD, Clare S, Walker AW, Goulding D, Stabler RA, Croucher N, Mastroeni P, Scott P, Raisen C, Mottram L, Fairweather NF, Wren BW, Parkhill J, Dougan G. Antibiotic treatment of clostridium difficile carrier mice triggers a supershedder state, spore-mediated transmission, and severe disease in immunocompromised hosts.. Infect Immun 2009 Sep;77(9):3661-9.
- Abreu NA, Nagalingam NA, Song Y, Roediger FC, Pletcher SD, Goldberg AN, Lynch SV. Sinus microbiome diversity depletion and Corynebacterium tuberculostearicum enrichment mediates rhinosinusitis.. Sci Transl Med 2012 Sep 12;4(151):151ra124.
- Hoggard M, Waldvogel-Thurlow S, Zoing M, Chang K, Radcliff FJ, Wagner Mackenzie B, Biswas K, Douglas RG, Taylor MW. Inflammatory Endotypes and Microbial Associations in Chronic Rhinosinusitis.. Front Immunol 2018;9:2065.
- Dlugaszewska J, Leszczynska M, Lenkowski M, Tatarska A, Pastusiak T, Szyfter W. The pathophysiological role of bacterial biofilms in chronic sinusitis.. Eur Arch Otorhinolaryngol 2016 Aug;273(8):1989-94.
- Stephenson MF, Mfuna L, Dowd SE, Wolcott RD, Barbeau J, Poisson M, James G, Desrosiers M. Molecular characterization of the polymicrobial flora in chronic rhinosinusitis.. J Otolaryngol Head Neck Surg 2010 Apr;39(2):182-7.
- Bogaert D, Keijser B, Huse S, Rossen J, Veenhoven R, van Gils E, Bruin J, Montijn R, Bonten M, Sanders E. Variability and diversity of nasopharyngeal microbiota in children: a metagenomic analysis.. PLoS One 2011 Feb 28;6(2):e17035.
- Weese JS, Slifierz M, Jalali M, Friendship R. Evaluation of the nasal microbiota in slaughter-age pigs and the impact on nasal methicillin-resistant Staphylococcus aureus (MRSA) carriage.. BMC Vet Res 2014 Mar 15;10:69.
- Kuhar HN, Tajudeen BA, Mahdavinia M, Heilingoetter A, Ganti A, Gattuso P, Ghai R, Batra PS. Relative abundance of nasal microbiota in chronic rhinosinusitis by structured histopathology.. Int Forum Allergy Rhinol 2018 Dec;8(12):1430-1437.
- Yang X, Li H, Ma Q, Zhang Q, Wang C. Neutrophilic Asthma Is Associated with Increased Airway Bacterial Burden and Disordered Community Composition.. Biomed Res Int 2018;2018:9230234.
- Lima SF, Teixeira AG, Higgins CH, Lima FS, Bicalho RC. The upper respiratory tract microbiome and its potential role in bovine respiratory disease and otitis media.. Sci Rep 2016 Jul 1;6:29050.
- Verheyen K, Newton JR, Talbot NC, de Brauwere MN, Chanter N. Elimination of guttural pouch infection and inflammation in asymptomatic carriers of Streptococcus equi.. Equine Vet J 2000 Nov;32(6):527-32.
- Kuhnert P, Korczak B, Falsen E, Straub R, Hoops A, Boerlin P, Frey J, Mutters R. Nicoletella semolina gen. nov., sp. nov., a new member of Pasteurellaceae isolated from horses with airway disease.. J Clin Microbiol 2004 Dec;42(12):5542-8.
- Hansson I, Johansson KE, Persson M, Riihimäki M. The clinical significance of Nicoletella semolina in horses with respiratory disorders and a screening of the bacterial flora in the airways of horses.. Vet Microbiol 2013 Mar 23;162(2-4):695-699.
- McConachie EL, Hart KA, Whelchel DD, Schroeder EL, Schott HC 2nd, Sanchez S. Pulmonary disease potentially associated with Nicoletella semolina in 3 young horses.. J Vet Intern Med 2014 May-Jun;28(3):939-43.
- Riley CB, Aldrich ED, Pemberton SL, Mirza AA. First report of pulmonary disease associated with Nicoletella semolina in a horse in New Zealand.. N Z Vet J 2021 Jan;69(1):65-69.
- Gao X, Lin H, Revanna K, Dong Q. A Bayesian taxonomic classification method for 16S rRNA gene sequences with improved species-level accuracy.. BMC Bioinformatics 2017 May 10;18(1):247.
- Manguin E, Pépin E, Boivin R, Leclere M. Tracheal microbial populations in horses with moderate asthma.. J Vet Intern Med 2020 Mar;34(2):986-995.
Citations
This article has been cited 5 times.- McLinden LA, Kemp-Symonds JG, Daly JM, Blanchard AM, Waller AS, Freeman SL. Effectiveness of a screening protocol employed at a UK rescue centre to prevent introduction of strangles. Equine Vet J 2026 Mar;58(2):466-475.
- Khan MZ, Li Y, Zhu M, Li M, Wang T, Zhang Z, Liu W, Ma Q, Wang C. Advances in Donkey Disease Surveillance and Microbiome Characterization in China. Microorganisms 2025 Mar 26;13(4).
- Huang F, Ma Z, Du X, Wang C, Liu G, Zhou M. Methionine Alters the Fecal Microbiota and Enhances the Antioxidant Capacity of Lactating Donkeys. Animals (Basel) 2025 Feb 23;15(5).
- Li L, Li S, Ma H, Akhtar MF, Tan Y, Wang T, Liu W, Khan A, Khan MZ, Wang C. An Overview of Infectious and Non-Infectious Causes of Pregnancy Losses in Equine. Animals (Basel) 2024 Jul 2;14(13).
- Cantelmi MC, Merola C, Averaimo D, Chiaverini A, Cito F, Cocco A, Di Teodoro G, De Angelis ME, Di Bernardo D, Auzino D, Petrini A. Identification of the Novel Streptococcus equi subsp. zooepidemicus Sequence Type 525 in Donkeys of Abruzzo Region, Italy. Pathogens 2023 May 23;12(6).
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