Skip to main content
Log in

Genotyping and antimicrobial resistance of Staphylococcus aureus isolates from dairy ruminants: differences in the distribution of clonal types between cattle and small ruminants

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Staphylococcus aureus is part of the normal flora of animals, and represents one of the leading causes of contagious mastitis in dairy herds worldwide. Sixty-seven epidemiologically unrelated S. aureus isolates from nasal and mastitis milk samples of dairy-producing animals (32 cows, 25 sheep, and 10 goats) were characterized by antimicrobial susceptibility testing and spa typing followed by multilocus sequence typing (MLST) on representative isolates and SCCmec-typing on methicillin-resistant S. aureus (MRSA) isolates. The highest resistance was observed to penicillin (64.2%, 43/67), followed by tetracycline (23.9%, 16/67), erythromycin (22.4%, 15/67), and streptomycin (17.9%, 12/67). In general, 18 spa types (including newly identified t16958) and 13 sequence types (STs) belonging to 8 clonal complexes (CCs) were detected. The cow-associated isolates were mainly assigned to CC5 (n = 18, related to t267-ST97, t521-ST352, t527-ST97, t304-ST6, and t084-ST15), followed by CC398 (n = 6, t937-ST291), CC45 (n = 3, t230-ST45), CC88 (n = 2, t2526-ST88), CC22 (n = 2, t3680-ST22), and CC522 (n = 1, t3576-ST522). Small ruminant isolates were mostly clustered into CC522 (n = 29, related to t3576, t1534, t16958, t7308, t7311, t7305 [ST522], t1534-ST2057, and t5428-ST2079). Two isolates from cows with mastitis were found to be MRSA, exhibited a composite profile of t937-ST291-SCCmecIV. No isolates carried the PVL and mecC genes. A significant difference in clonal types of S. aureus isolates from cows in comparison with those from small ruminants was found. This study demonstrated the circulation of diverse clones of S. aureus among dairy animals in Iran, with a different clonal composition between cows and small ruminants. The current study also reports MRSA-related mastitis in dairy cows, emphasizing the need for comprehensive surveillance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aalipour F, Mirlohi M, Jalali M (2014) Determination of antibiotic consumption index for animal originated foods produced in animal husbandry in Iran, 2010. J Environ Health Sci Eng 12:42

    PubMed  PubMed Central  Google Scholar 

  • Agabou A, Ouchenane Z, Ngba Essebe C, Khemissi S, Chehboub MTE, Chehboub IB, Sotto A, Dunyach-Remy C, Lavigne JP (2017) Emergence of nasal carriage of ST80 and ST152 PVL+ Staphylococcus aureus isolates from livestock in Algeria. Toxins 9:303–314

    PubMed Central  Google Scholar 

  • Aires-de-Sousa M, Parente CE, Vieira-da-Motta O, Bonna IC, Silva DA, de Lencastre H (2007) Characterization of Staphylococcus aureus isolates from buffalo, bovine, ovine, and caprine milk samples collected in Rio de Janeiro State, Brazil. Appl Environ Microbiol 73:3845–3849

    CAS  PubMed  PubMed Central  Google Scholar 

  • Asadollahi P, Farahani NN, Mirzaii M, Khoramrooz SS, van Belkum A, Asadollahi K, Dadashi M, Darban-Sarokhalil D (2018) Distribution of the most prevalent spa types among clinical isolates of methicillin-resistant and—susceptible Staphylococcus aureus around the world: a review. Front Microbiol 9:163

    PubMed  PubMed Central  Google Scholar 

  • Bardiau M, Yamazaki K, Duprez JN, Taminiau B, Mainil JG, Ote I (2013) Genotypic and phenotypic characterization of methicillin-resistant Staphylococcus aureus (MRSA) isolated from milk of bovine mastitis. Lett Appl Microbiol 57:181–186

    CAS  PubMed  Google Scholar 

  • Bar-Gal GK, Blum SE, Hadas L, Ehricht R, Monecke S, Leitner G (2015) Host-specificity of Staphylococcus aureus causing intramammary infections in dairy animals assessed by genotyping and virulence genes. Vet Microbiol 176:143–154

    CAS  PubMed  Google Scholar 

  • Ben Said M, Abbassi MS, Gomez P, Ruiz-Ripa L, Sghaier S, El Fekih O, Hassen A, Torres C (2017) Genetic characterization of Staphylococcus aureus isolated from nasal samples of healthy ewes in Tunisia. High prevalence of CC130 and CC522 lineages. Comp Immunol Microbiol Infect Dis 51:37–40

    PubMed  Google Scholar 

  • Ben Zakour NL, Sturdevant DE, Even S, Guinane CM, Barbey C, Alves PD, Cochet MF, Gautier M, Otto M, Fitzgerald JR, Le Loir Y (2008) Genome-wide analysis of ruminant Staphylococcus aureus reveals diversification of the core genome. J Bacteriol 190:6302–6317

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bonsaglia ECR, Silva NCC, Rossi BF, Camargo CH, Dantas STA, Langoni H, Guimaraes FF, Lima FS, Fitzgerald JR, Fernandes AJ, Rall VLM (2018) Molecular epidemiology of methicillin-susceptible Staphylococcus aureus (MSSA) isolated from milk of cows with subclinical mastitis. Microb Pathog 124:130–135

    CAS  PubMed  Google Scholar 

  • Boss R, Cosandey A, Luini M, Artursson K, Bardiau M, Breitenwieser F, Hehenberger E, Lam T, Mansfeld M, Michel A, Mosslacher G, Naskova J, Nelson S, Podpecan O, Raemy A, Ryan E, Salat O, Zangerl P, Steiner A, Graber HU (2016) Bovine Staphylococcus aureus: Subtyping, evolution, and zoonotic transfer. J Dairy Sci 99:515–528

    CAS  PubMed  Google Scholar 

  • Boye K, Bartels MD, Andersen IS, Moller JA, Westh H (2007) A new multiplex PCR for easy screening of methicillin-resistant Staphylococcus aureus SCCmec types I-V. Clin Microbiol Infect 13:725–727

    CAS  PubMed  Google Scholar 

  • Brakstad OG, Aasbakk K, Maeland JA (1992) Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene. J Clin Microbiol 30:1654–1660

    CAS  PubMed  PubMed Central  Google Scholar 

  • CLSI (2015) Performance standards for antimicrobial susceptibility testing; Twenty-fifth information supplement M100–S25 Wayne. Clinical Laboratory Standards Institute, Washington

    Google Scholar 

  • Cuny C, Friedrich A, Kozytska S, Layer F, Nubel U, Ohlsen K, Strommenger B, Walther B, Wieler L, Witte W (2010) Emergence of methicillin-resistant Staphylococcus aureus (MRSA) in different animal species. Int J Med Microbiol 300:109–117

    PubMed  Google Scholar 

  • Dadashi M, Nasiri MJ, Fallah F, Owlia P, Hajikhani B, Emaneini M, Mirpour M (2018) Methicillin-resistant Staphylococcus aureus (MRSA) in Iran: a systematic review and meta-analysis. J Glob Antimicrob Resist 12:96–103

    PubMed  Google Scholar 

  • Darban-Sarokhalil D, Khoramrooz SS, Marashifard M, Malek Hosseini SA, Parhizgari N, Yazdanpanah M, Gharibpour F, Mirzaii M, Sharifi B, Haeili M (2016) Molecular characterization of Staphylococcus aureus isolates from southwest of Iran using spa and SCCmec typing methods. Microb Pathog 98:88–92

    CAS  PubMed  Google Scholar 

  • Delgado S, Garcia P, Fernandez L, Jimenez E, Rodriguez-Banos M, Del Campo R, Rodriguez JM (2011) Characterization of Staphylococcus aureus strains involved in human and bovine mastitis. FEMS Immunol Med Microbiol 62:225–235

    CAS  PubMed  Google Scholar 

  • Diaz R, Ramalheira E, Afreixo V, Gago B (2016) Methicillin-resistant Staphylococcus aureus carrying the new mecC gene-a meta-analysis. Diagn Microbiol Infect Dis 84:135–140

    CAS  PubMed  Google Scholar 

  • El-Ashker M, Gwida M, Tomaso H, Monecke S, Ehricht R, El-Gohary F, Hotzel H (2015) Staphylococci in cattle and buffaloes with mastitis in Dakahlia Governorate. Egypt J Dairy Sci 98:7450–7459

    CAS  PubMed  Google Scholar 

  • Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG (2000) Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 38:1008–1015

    CAS  PubMed  PubMed Central  Google Scholar 

  • Enright MC, Robinson DA, Randle G, Feil EJ, Grundmann H, Spratt BG (2002) The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc Natl Acad Sci USA 99:7687–7692

    CAS  PubMed  Google Scholar 

  • Eriksson J, Espinosa-Gongora C, Stamphoj I, Larsen AR, Guardabassi L (2013) Carriage frequency, diversity and methicillin resistance of Staphylococcus aureus in Danish small ruminants. Vet Microbiol 163:110–115

    CAS  PubMed  Google Scholar 

  • Gharsa H, Ben Slama K, Gomez-Sanz E, Lozano C, Zarazaga M, Messadi L, Boudabous A, Torres C (2015) Molecular characterization of Staphylococcus aureus from nasal samples of healthy farm animals and pets in Tunisia. Vector Borne Zoonotic Dis 15:109–115

    PubMed  Google Scholar 

  • Giacinti G, Carfora V, Caprioli A, Sagrafoli D, Marri N, Giangolini G, Amoruso R, Iurescia M, Stravino F, Dottarelli S, Feltrin F, Franco A, Amatiste S, Battisti A (2017) Prevalence and characterization of methicillin-resistant Staphylococcus aureus carrying mecA or mecC and methicillin-susceptible Staphylococcus aureus in dairy sheep farms in central Italy. J Dairy Sci 100:7857–7863

    CAS  PubMed  Google Scholar 

  • Gopal S, Divya KC (2017) Can methicillin-resistant Staphylococcus aureus prevalence from dairy cows in India act as potential risk for community-associated infections?: a review. Vet World 10:311–318

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goudarzi M, Fazeli M, Goudarzi H, Azad M, Seyedjavadi SS (2016a) Spa typing of Staphylococcus aureus strains isolated from clinical specimens of patients with nosocomial infections in Tehran. Iran Jundishapur J Microbiol 9:e35685

    PubMed  Google Scholar 

  • Goudarzi M, Goudarzi H, Sa Figueiredo AM, Udo EE, Fazeli M, Asadzadeh M, Seyedjavadi SS (2016b) Molecular characterization of methicillin resistant Staphylococcus aureus strains isolated from intensive care units in Iran: ST22-SCCmec IV/t790 Emerges as the Major Clone. PLoS ONE 11:e0155529

    PubMed  PubMed Central  Google Scholar 

  • Goudarzi M, Navidinia M, Beiranvand E, Goudarzi H (2018) Phenotypic and molecular characterization of methicillin-resistant Staphylococcus aureus clones carrying the Panton-Valentine leukocidin genes disseminating in Iranian hospitals. Microb Drug Resist. https://doi.org/10.1089/mdr.2018.0033

    Article  PubMed  Google Scholar 

  • Haenni M, Chatre P, Tasse J, Nowak N, Bes M, Madec JY, Laurent F (2014) Geographical clustering of mecC-positive Staphylococcus aureus from bovine mastitis in France. J Antimicrob Chemother 69:2292–2293

    CAS  PubMed  Google Scholar 

  • Harastani HH, Araj GF, Tokajian ST (2014) Molecular characteristics of Staphylococcus aureus isolated from a major hospital in Lebanon. Int J Infect Dis 19:33–38

    CAS  PubMed  Google Scholar 

  • Hata E, Katsuda K, Kobayashi H, Uchida I, Tanaka K, Eguchi M (2010) Genetic variation among Staphylococcus aureus strains from bovine milk and their relevance to methicillin-resistant isolates from humans. J Clin Microbiol 48:2130–2139

    CAS  PubMed  PubMed Central  Google Scholar 

  • Havaei SA, Azimian A, Fazeli H, Naderi M, Ghazvini K, Samiee SM, Soleimani M (2013) Isolation of Asian endemic and livestock associated clones of methicillin resistant Staphylococcus aureus from ocular samples in Northeastern Iran. Iran J Microbiol 5:227–232

    PubMed  PubMed Central  Google Scholar 

  • Jamali H, Radmehr B, Ismail S (2014) Short communication: prevalence and antibiotic resistance of Staphylococcus aureus isolated from bovine clinical mastitis. J Dairy Sci 97:2226–2230

    CAS  PubMed  Google Scholar 

  • Jorgensen HJ, Mork T, Caugant DA, Kearns A, Rorvik LM (2005) Genetic variation among Staphylococcus aureus strains from Norwegian bulk milk. Appl Environ Microbiol 71:8352–8361

    CAS  PubMed  PubMed Central  Google Scholar 

  • Khademi F, Ghanbari F, Mellmann A, Najafzadeh MJ, Khaledi A (2016) Phylogenetic relationships among Staphylococcus aureus isolated from clinical samples in Mashhad. Iran J Infect Public Health 9:639–644

    PubMed  Google Scholar 

  • Klibi A, Jouini A, Gomez P, Slimene K, Ceballos S, Torres C, Maaroufi A (2018) Molecular characterization and clonal diversity of methicillin-resistant and -susceptible Staphylococcus aureus isolates of milk of cows with clinical mastitis in Tunisia. Microb Drug Resist 24:1210–1216

    CAS  PubMed  Google Scholar 

  • Lakhundi S, Zhang K (2018) Methicillin-resistant Staphylococcus aureus: molecular characterization, evolution, and epidemiology. Clin Microbiol Rev 31:e00020–e118

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lina G, Piemont Y, Godail-Gamot F, Bes M, Peter MO, Gauduchon V, Vandenesch F, Etienne J (1999) Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 29:1128–1132

    CAS  PubMed  Google Scholar 

  • Loncaric I, Kubber-Heiss A, Posautz A, Stalder GL, Hoffmann D, Rosengarten R, Walzer C (2014) mecC- and mecA-positive meticillin-resistant Staphylococcus aureus (MRSA) isolated from livestock sharing habitat with wildlife previously tested positive for mecC-positive MRSA. Vet Dermatol 25:147–148

    PubMed  Google Scholar 

  • Lozano C, Gharsa H, Ben Slama K, Zarazaga M, Torres C (2016) Staphylococcus aureus in animals and food: methicillin resistance, prevalence and population structure. A review in the African continent. Microorganisms 4:12–30

    PubMed Central  Google Scholar 

  • Martins KB, Faccioli-Martins PY, Riboli DF, Pereira VC, Fernandes S, Oliveira AA, Dantas A, Zafalon LF, da Cunha Mde L (2015) Clonal profile, virulence and resistance of Staphylococcus aureus isolated from sheep milk. Braz J Microbiol 46:535–543

    PubMed  PubMed Central  Google Scholar 

  • Merz A, Stephan R, Johler S (2016) Staphylococcus aureus isolates from goat and sheep milk seem to be closely related and differ from isolates detected from bovine milk. Front Microbiol 7:319

    PubMed  PubMed Central  Google Scholar 

  • Mistry H, Sharma P, Mahato S, Saravanan R, Kumar PA, Bhandari V (2016) Prevalence and characterization of oxacillin susceptible mecA-positive clinical isolates of Staphylococcus aureus causing bovine mastitis in India. PLoS ONE 11:e0162256

    PubMed  PubMed Central  Google Scholar 

  • Monecke S, Coombs G, Shore AC, Coleman DC, Akpaka P, Borg M, Chow H, Ip M, Jatzwauk L, Jonas D, Kadlec K, Kearns A, Laurent F, O'Brien FG, Pearson J, Ruppelt A, Schwarz S, Scicluna E, Slickers P, Tan HL, Weber S, Ehricht R (2011) A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS ONE 6:e17936

    CAS  PubMed  PubMed Central  Google Scholar 

  • Monistero V, Graber HU, Pollera C, Cremonesi P, Castiglioni B, Bottini E, Ceballos-Marquez A, Lasso-Rojas L, Kroemker V, Wente N, Petzer IM, Santisteban C, Runyan J, Veiga Dos Santos M, Alves BG, Piccinini R, Bronzo V, Abbassi MS, Said MB, Moroni P (2018) Staphylococcus aureus isolates from bovine mastitis in eight countries: genotypes, detection of genes encoding different toxins and other virulence genes. Toxins 10:247–268

    PubMed Central  Google Scholar 

  • Mork T, Tollersrud T, Kvitle B, Jorgensen HJ, Waage S (2005) Comparison of Staphylococcus aureus genotypes recovered from cases of bovine, ovine, and caprine mastitis. J Clin Microbiol 43:3979–3984

    CAS  PubMed  PubMed Central  Google Scholar 

  • Murakami K, Minamide W, Wada K, Nakamura E, Teraoka H, Watanabe S (1991) Identification of methicillin-resistant strains of Staphylococci by polymerase chain reaction. J Clin Microbiol 29:2240–2244

    CAS  PubMed  PubMed Central  Google Scholar 

  • Narenji Sani R, Mahdavi A, Moezifar M (2015) Prevalence and etiology of subclinical mastitis in dairy ewes in two seasons in Semnan province. Iran Trop Anim Health Prod 47:1249–1254

    PubMed  Google Scholar 

  • Obaidat MM, Bani Salman AE, Roess AA (2018) High prevalence and antimicrobial resistance of mecA Staphylococcus aureus in dairy cattle, sheep, and goat bulk tank milk in Jordan. Trop Anim Health Prod 50:405–412

    PubMed  Google Scholar 

  • Ohadian SM, Pourmand MR, Mahmoudi M, Sadighian H (2015) Molecular characterization of methicillin-resistant Staphylococcus aureus: characterization of major clones and emergence of epidemic clones of sequence type (ST) 36 and ST 121 in Tehran, Iran. FEMS Microbiol Lett 362:fnv043

    Google Scholar 

  • O'Hara FP, Suaya JA, Ray GT, Baxter R, Brown ML, Mera RM, Close NM, Thomas E, Amrine-Madsen H (2016) spa typing and multilocus sequence typing show comparable performance in a macroepidemiologic study of Staphylococcus aureus in the United States. Microb Drug Resist 22:88–96

    CAS  PubMed  PubMed Central  Google Scholar 

  • Panahi M, Saei HD (2019) Genetic diversity and methicillin resistance of Staphylococcus aureus originating from buffaloes with mastitis in Iran. Comp Immunol Microbiol Infect Dis 62:19–24

    PubMed  Google Scholar 

  • Papadopoulos P, Papadopoulos T, Angelidis AS, Kotzamanidis C, Zdragas A, Papa A, Filioussis G, Sergelidis D (2018) Prevalence, antimicrobial susceptibility and characterization of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus isolated from dairy industries in north-central and north-eastern Greece. Int J Food Microbiol 291:35–41

    PubMed  Google Scholar 

  • Papadopoulos P, Angelidis AS, Papadopoulos T, Kotzamanidis C, Zdragas A, Papa A, Filioussis G, Sergelidis D (2019) Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) in bulk tank milk, livestock and dairy-farm personnel in north-central and north-eastern Greece: prevalence, characterization and genetic relatedness. Food Microbiol. https://doi.org/10.1016/j.fm.2019.103249

    Article  PubMed  Google Scholar 

  • Porrero MC, Hasman H, Vela AI, Fernandez-Garayzabal JF, Dominguez L, Aarestrup FM (2012) Clonal diversity of Staphylococcus aureus originating from the small ruminants goats and sheep. Vet Microbiol 156:157–161

    PubMed  Google Scholar 

  • Rao Q, Shang W, Hu X, Rao X (2015) Staphylococcus aureus ST121: a globally disseminated hypervirulent clone. J Med Microbiol 64:1462–1473

    CAS  PubMed  Google Scholar 

  • Sarkar A, Raji A, Garaween G, Soge O, Rey-Ladino J, Al-Kattan W, Shibl A, Senok A (2016) Antimicrobial resistance and virulence markers in methicillin sensitive Staphylococcus aureus isolates associated with nasal colonization. Microb Pathog 93:8–12

    CAS  PubMed  Google Scholar 

  • Schauer B, Krametter-Frotscher R, Knauer F, Ehricht R, Monecke S, Fessler AT, Schwarz S, Grunert T, Spergser J, Loncaric I (2018) Diversity of methicillin-resistant Staphylococcus aureus (MRSA) isolated from Austrian ruminants and New World camelids. Vet Microbiol 215:77–82

    CAS  PubMed  Google Scholar 

  • Schaumburg F, Pauly M, Anoh E, Mossoun A, Wiersma L, Schubert G, Flammen A, Alabi AS, Muyembe-Tamfum JJ, Grobusch MP, Karhemere S, Akoua-Koffi C, Couacy-Hymann E, Kremsner PG, Mellmann A, Becker K, Leendertz FH, Peters G (2015) Staphylococcus aureus complex from animals and humans in three remote African regions. Clin Microbiol Infect 21(345):e341–348

    Google Scholar 

  • Schmidt T, Kock MM, Ehlers MM (2017) Molecular characterization of Staphylococcus aureus isolated from bovine mastitis and close human contacts in south African dairy herds: genetic diversity and inter-species host transmission. Front Microbiol 8:511

    PubMed  PubMed Central  Google Scholar 

  • Seyffert N, Le Marechal C, Jardin J, McCulloch JA, Rosado FR, Miyoshi A, Even S, Jan G, Berkova N, Vautor E, Thiery R, Azevedo V, Le Loir Y (2012) Staphylococcus aureus proteins differentially recognized by the ovine immune response in mastitis or nasal carriage. Vet Microbiol 157:439–447

    CAS  PubMed  Google Scholar 

  • Seyoum B, Kefyalew H, Abera B, Abdela N (2018) Prevalence, risk factors and antimicrobial susceptibility test of Staphylococcus aureus in Bovine cross breed mastitic milk in and around Asella town, Oromia regional state, southern Ethiopia. Acta Trop 177:32–36

    CAS  PubMed  Google Scholar 

  • Shah MS, Qureshi S, Kashoo Z, Farooq S, Wani SA, Hussain MI, Banday MS, Khan AA, Gull B, Habib A, Khan SM, Dar BA (2019) Methicillin resistance genes and in vitro biofilm formation among Staphylococcus aureus isolates from bovine mastitis in India. Comp Immunol Microbiol Infect Dis 64:117–124

    PubMed  Google Scholar 

  • Shakeri F, Shojai A, Golalipour M, Rahimi Alang S, Vaez H, Ghaemi EA (2010) Spa diversity among MRSA and MSSA strains of Staphylococcus aureus in North of Iran. Int J Microbiol 2010:351397. https://doi.org/10.1155/2010/351397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shettigar K, Jain S, Bhat DV, Acharya R, Ramachandra L, Satyamoorthy K, Murali TS (2016) Virulence determinants in clinical Staphylococcus aureus from monomicrobial and polymicrobial infections of diabetic foot ulcers. J Med Microbiol 65:1392–1404

    CAS  PubMed  Google Scholar 

  • Smith EM, Needs PF, Manley G, Green LE (2014) Global distribution and diversity of ovine-associated Staphylococcus aureus. Infect Genet Evol 22:208–215

    PubMed  PubMed Central  Google Scholar 

  • Sotto A, Richard JL, Messad N, Molinari N, Jourdan N, Schuldiner S, Sultan A, Carriere C, Canivet B, Landraud L, Lina G, Lavigne JP (2012) Distinguishing colonization from infection with Staphylococcus aureus in diabetic foot ulcers with miniaturized oligonucleotide arrays: a French multicenter study. Diabetes Care 35:617–623

    CAS  PubMed  PubMed Central  Google Scholar 

  • Srednik ME, Crespi E, Testorelli MF, Puigdevall T, Pereyra AMD, Rumi MV, Caggiano N, Gulone L, Mollerach M, Gentilini ER (2019) First isolation of a methicillin-resistant Staphylococcus aureus from bovine mastitis in Argentina. Vet Anim Sci 7:100043

    Google Scholar 

  • Stegger M, Andersen PS, Kearns A, Pichon B, Holmes MA, Edwards G, Laurent F, Teale C, Skov R, Larsen AR (2012) Rapid detection, differentiation and typing of methicillin-resistant Staphylococcus aureus harbouring either mecA or the new mecA homologue mecA(LGA251). Clin Microbiol Infect 18:395–400

    CAS  PubMed  Google Scholar 

  • Sung JM, Lloyd DH, Lindsay JA (2008) Staphylococcus aureus host specificity: comparative genomics of human versus animal isolates by multi-strain microarray. Microbiology 154:1949–1959

    CAS  PubMed  Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    CAS  PubMed  Google Scholar 

  • Unal N, Askar S, Macun HC, Sakarya F, Altun B, Yildirim M (2012) Panton-Valentine leukocidin and some exotoxins of Staphylococcus aureus and antimicrobial susceptibility profiles of staphylococci isolated from milks of small ruminants. Trop Anim Health Prod 44:573–579

    PubMed  Google Scholar 

  • Unnerstad HE, Bengtsson B, Rantzien HM, Borjesson S (2013) Methicillin-resistant Staphylococcus aureus containing mecC in Swedish dairy cows. Acta Vet Scand 55:6

    PubMed  PubMed Central  Google Scholar 

  • van Leeuwen WB, Melles DC, Alaidan A, Al-Ahdal M, Boelens HA, Snijders SV, Wertheim H, van Duijkeren E, Peeters JK, van der Spek PJ, Gorkink R, Simons G, Verbrugh HA, van Belkum A (2005) Host- and tissue-specific pathogenic traits of Staphylococcus aureus. J Bacteriol 187:4584–4591

    PubMed  PubMed Central  Google Scholar 

  • Wang D, Wang Z, Yan Z, Wu J, Ali T, Li J, Lv Y, Han B (2015) Bovine mastitis Staphylococcus aureus: antibiotic susceptibility profile, resistance genes and molecular typing of methicillin-resistant and methicillin-sensitive strains in China. Infect Genet Evol 31:9–16

    PubMed  Google Scholar 

  • Wang W, Lin X, Jiang T, Peng Z, Xu J, Yi L, Li F, Fanning S, Baloch Z (2018) Prevalence and characterization of Staphylococcus aureus cultured from raw milk taken from dairy cows with mastitis in Beijing. China Front Microbiol 9:1123

    PubMed  Google Scholar 

  • Yi Y, Su L, Li B, Li S, Zhang B, Su Y (2018) Analysis of the Genetic Diversity in Methicillin-resistant Staphylococcus aureus isolates from bovine subclinical mastitis case in Xinjiang, China. Foodborne Pathog Dis 15:568–575

    CAS  PubMed  Google Scholar 

  • Zhang L, Gao J, Barkema HW, Ali T, Liu G, Deng Y, Naushad S, Kastelic JP, Han B (2018) Virulence gene profiles: alpha-hemolysin and clonal diversity in Staphylococcus aureus isolates from bovine clinical mastitis in China. BMC Vet Res 14:63

    PubMed  PubMed Central  Google Scholar 

  • Zhou Z, Zhang M, Li H, Yang H, Li X, Song X, Wang Z (2017) Prevalence and molecular characterization of Staphylococcus aureus isolated from goats in Chongqing. China BMC Vet Res 13:352

    PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Dean for Research of Urmia University for the financial support of the current investigation. The authors are very grateful to Professor Alexander Mellmann from University of Münster, Institute of Hygiene, Germany, for conducting the BURP analysis. We are also thankful to Dr. Somayeh Hoseinzadeh, Mr. Heidar Rahimi, and Mr. Hamed Salami Pargoo for their help in sample collection.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Habib Dastmalchi Saei.

Additional information

Communicated by Dennis Linton.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dastmalchi Saei, H., Panahi, M. Genotyping and antimicrobial resistance of Staphylococcus aureus isolates from dairy ruminants: differences in the distribution of clonal types between cattle and small ruminants. Arch Microbiol 202, 115–125 (2020). https://doi.org/10.1007/s00203-019-01722-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-019-01722-z

Keywords

Navigation