Staphylococcal species composition in the skin microbiota of domestic pigeons (Columba livia domestica)

Staphylococci are a natural component of the skin microbiota of many organisms, including humans and birds. As opportunistic pathogens, they can cause a variety of infections in humans. The close contact between domestic pigeons and their owners provide an opportunity for exchange of skin-associated bacteria. In this study, 41 healthy racing pigeons were tested. Staphylococci were detected on the skin of each bird (41/41, 100%). Isolates were identified at the species level using matrix-assisted laser desorption ionization time of flight mass spectrometry (MALDI-TOF MS). The diversity of the Staphylococcus species was relatively high and coagulase-negative staphylococci (CoNS) were predominantly isolated. In total, ten different staphylococcal species were identified. S. lentus (19/41, 46.3%) was noted most frequently. The pigeon skin was also inhabited by S. xylosus (6/41, 14.6%), S. equorum (4/41, 9.8%), S. hyicus (3/41, 7.3%), S. intermedius (2/41, 4.9%), S. sciuri (2/41, 4.9%), S. vitulinus (2/41, 4.9%), S. lugdunensis (1/41, 2.4%), S. hominis (1/41, 2.4%), and S. auricularis (1/41, 2.4%). Our results indicate that domestic pigeons may carry pathogens with zoonotic potential. All strains were susceptible to 12 antibiotics (ciprofloxacin, clindamycin chloramphenicol, erythromycin, fosfomycin, gentamicin, levofloxacin, norfloxacin, rifampicin, tobramycin, trimethoprim/sulfamethoxazole, vancomycin) representing 8 different classes. None isolate displayed a multidrug-resistant phenotype. Resistance to tetracycline (6/41, 14.6%) and to penicillin (4/41, 9.7%) was shown. The mecA gene was not detected in the examined strains and no methicillin-resistant staphylococci were found on the skin of the healthy pigeons.

[1]  A. Madsen,et al.  Airborne methicillin-resistant Staphylococcus aureus, other bacteria, fungi, endotoxin, and dust in a pigeon exhibition. , 2022, Environmental research.

[2]  C. B. Miguel,et al.  Staphylococcus aureus and Enterococcus faecium isolated from pigeon droppings (Columba livia) in the external environment close to hospitals , 2022, Revista da Sociedade Brasileira de Medicina Tropical.

[3]  W. Witte,et al.  Colonization of Dogs and Their Owners with Staphylococcus aureus and Staphylococcus pseudintermedius in Households, Veterinary Practices, and Healthcare Facilities , 2022, Microorganisms.

[4]  Amira M. El-Tahan,et al.  Investigation of many bacterial and viral infections circulating in pigeons showing nervous symptoms , 2022, Saudi journal of biological sciences.

[5]  M. Castro,et al.  Once a Known Veterinary Pathogen, Now a Forgotten Zoonosis. Case Report of An Invasive Staphylococcus intermedius Group Infection , 2021, International Journal of Infection.

[6]  J. A. Corbera,et al.  Multidrug-Resistant Phenotypes of Escherichia coli Isolates in Wild Canarian Egyptian Vultures (Neophron percnopterus majorensis) , 2021, Animals : an open access journal from MDPI.

[7]  M. Spînu,et al.  Pigeons as Carriers of Clinically Relevant Multidrug-Resistant Pathogens—A Clinical Case Report and Literature Review , 2021, Frontiers in Veterinary Science.

[8]  D. Sherris,et al.  Staphylococcus lentus Sinusitis: A New Sinonasal Pathogen , 2020, Ear, nose, & throat journal.

[9]  G. Gao,et al.  Metagenomic analysis reveals the microbiome and resistome in migratory birds , 2020, Microbiome.

[10]  D. Chrobak-Chmiel,et al.  Prevalence, antibiotic susceptibility and virulence factors of Enterococcus species in racing pigeons (Columba livia f. domestica) , 2020, BMC Veterinary Research.

[11]  M. T. Tejedor-Junco,et al.  Virulence factors in coagulase-positive staphylococci of veterinary interest other than Staphylococcus aureus , 2020, The veterinary quarterly.

[12]  T. Donovan,et al.  Vegetative Endocarditis due to Staphylococcus aureus in an Umbrella Cockatoo (Cacatua alba) , 2019, Journal of Avian Medicine and Surgery.

[13]  J. Neufeld,et al.  The skin microbiome of vertebrates , 2019, Microbiome.

[14]  A. Tichy,et al.  Prevalence of Methicillin-Resistant Staphylococcus sp. (MRS) in Different Companion Animals and Determination of Risk Factors for Colonization with MRS , 2019, Antibiotics.

[15]  Gilles Prévost,et al.  Coagulase-Negative Staphylococci Pathogenomics , 2019, International journal of molecular sciences.

[16]  M. Dominguez-Bello,et al.  Comparison of gizzard and intestinal microbiota of wild neotropical birds , 2018, PloS one.

[17]  P. Shahbazi,et al.  ANTIMICROBIAL SUSCEPTIBILITY PATTERNS OF BIOFILM FORMING STAPHYLOCOCCUS AUREUS ISOLATED FROM PIGEON EXTERNAL OCULAR INFECTIONS , 2018 .

[18]  Yasmine Belkaid,et al.  The human skin microbiome , 2018, Nature Reviews Microbiology.

[19]  František Zigo,et al.  Changes in bacterial microflora in young carrier pigeons during the race season , 2017 .

[20]  K. Bierowiec,et al.  Is the Colonisation of Staphylococcus aureus in Pets Associated with Their Close Contact with Owners? , 2016, PloS one.

[21]  R. Humphries,et al.  In Vitro Antimicrobial Susceptibility of Staphylococcus pseudintermedius Isolates of Human and Animal Origin , 2016, Journal of Clinical Microbiology.

[22]  C. Cosseau,et al.  Proteobacteria from the human skin microbiota: Species-level diversity and hypotheses , 2016, One health.

[23]  C. Miracco,et al.  Erythema nodosum associated with Staphylococcus xylosus septicemia. , 2016, Journal of microbiology, immunology, and infection = Wei mian yu gan ran za zhi.

[24]  M. Rzewuska,et al.  Genetic characterization of coagulase-positive staphylococci isolated from healthy pigeons. , 2015, Polish journal of veterinary sciences.

[25]  Georg Peters,et al.  Coagulase-Negative Staphylococci , 2005 .

[26]  C. Quereda,et al.  Staphylococcus lentus Peritonitis: A Case Report , 2014, Peritoneal Dialysis International.

[27]  M. Śmiałek,et al.  Antimicrobial resistance in bacteria isolated from pigeons in Poland. , 2014, Polish journal of veterinary sciences.

[28]  G. Gray,et al.  Reverse Zoonotic Disease Transmission (Zooanthroponosis): A Systematic Review of Seldom-Documented Human Biological Threats to Animals , 2014, PloS one.

[29]  M. Falagas,et al.  Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. , 2012, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[30]  S. Beatson,et al.  Comparative Genomics of the Staphylococcus intermedius Group of Animal Pathogens , 2012, Front. Cell. Inf. Microbio..

[31]  C. Maranta,et al.  Human infection associated with methicillin-resistant Staphylococcus pseudintermedius ST71. , 2010, The Journal of antimicrobial chemotherapy.

[32]  B. Sieger,et al.  Staphylococcus lentus: The troublemaker , 2010 .

[33]  M. Kostrzewa,et al.  Identification of a Variety of Staphylococcus Species by Matrix-Assisted Laser Desorption Ionization-Time of Flight Mass Spectrometry , 2009, Journal of Clinical Microbiology.

[34]  M. Hendrick,et al.  Methicillin-Resistant Staphylococcus aureus–Associated Dermatitis in a Congo African Grey Parrot (Psittacus erithacus erithacus) , 2008, Journal of avian medicine and surgery.

[35]  K. Futagawa-Saito,et al.  High occurrence of multi-antimicrobial resistance in Staphylococcus intermedius isolates from healthy and diseased dogs and domesticated pigeons. , 2007, Research in veterinary science.

[36]  S. Leroy,et al.  Genomic Diversity in Staphylococcus xylosus , 2007, Applied and Environmental Microbiology.

[37]  Meng Gan,et al.  A Highly Pathogenic Strain of Staphylococcus sciuri Caused Fatal Exudative Epidermitis in Piglets , 2007, PloS one.

[38]  R. Pantůček,et al.  Staphylococcus equorum and Staphylococcus succinus isolated from human clinical specimens. , 2006, Journal of medical microbiology.

[39]  Tsuguaki Fukuyasu,et al.  Prevalence of virulence factors in Staphylococcus intermedius isolates from dogs and pigeons , 2006, BMC veterinary research.

[40]  A. Vergara,et al.  Antimicrobial susceptibility of environmental Staphylococcus aureus strains isolated from a pigeon slaughterhouse in Italy. , 2005, Poultry science.

[41]  P. Ježek,et al.  Identification and Characterization of Clinical Isolates of Members of the Staphylococcus sciuri Group , 2005, Journal of Clinical Microbiology.

[42]  F. Vandenesch,et al.  Population Diversity of Staphylococcus intermedius Isolates from Various Host Species: Typing by 16S-23S Intergenic Ribosomal DNA Spacer Polymorphism Analysis , 2002, Journal of Clinical Microbiology.

[43]  Y. Wakita,et al.  Isolation and species distribution of staphylococci from animal and human skin. , 2002, The Journal of veterinary medical science.

[44]  S. Schwarz,et al.  Antibiotic Resistance in Staphylococci Isolated from Pigeons. , 1994, Veterinary dermatology.

[45]  V. Hájek Staphylococcus intermedius, a New Species Isolated from Animals , 1976 .

[46]  A. Aydin,et al.  Virulence properties of Staphylococcus delphini strains isolated from domestic pigeons , 2012 .