Details

Title

Prevalence and antimicrobial resistance profiles of bacterial pathogens associated with subclinical mastitis and dairy farm environments

Journal title

Polish Journal of Veterinary Sciences

Yearbook

2025

Volume

vol. 28

Issue

No 4

Authors

Affiliation

Ozbey, G. : Department of Medical Services and Techniques, Vocational School of Health Services, Firat University, TR-23119 Elazig, Turkey ; Tanriverdi, E.S. : Department of Medical Microbiology, Faculty of Medicine, Inonu University, TR-44280 Battalgazi, Malatya, Turkey ; Zigo, F. : Department of Animal Nutrition and Husbandry, University of Veterinary Medicine and Pharmacy in Košice, Komenského 73, Košice, 04181, Slovakia

Keywords

one health ; Escherichia coli ; MALDI-TOF MS ; mcr genes ; mastitis ; Staphylococcus aureus

Divisions of PAS

Nauki Biologiczne i Rolnicze

Coverage

639–650

Publisher

Polish Academy of Sciences Committee of Veterinary Sciences ; University of Warmia and Mazury in Olsztyn

Bibliography

Abd El-Aziz NK, Ammar AM, El Damaty HM, Abd Elkader RA, Saad HA, El-Kazzaz W, Khalifa E (2021) Environmental Streptococcus uberis associated with clinical mastitis in dairy cows: virulence traits, antimicrobial and biocide resistance, and epidemiological typing. Animals (Basel) 11: 1849. 

Adkins PR, Middleton JR, Fox LK, Pighetti G, Petersson-Wolfe C (2017) National Mastitis Council (Estats Units d’Amèrica), Laboratory Handbook on Bovine Mastitis. National Mastitis Council, 3rd Edition, Inc., New Prague, Minnesota, 147 p. https://www.academia.edu/50651208/Laboratory_Handbook_on_Bovine_Mastitis

Algammal AM, Hetta HF, Elkelish A, Alkhalifah DH, Hozzein WN, Batiha GE, El Nahhas N, Mabrok MA (2020) Methicillin-resistant Staphylococcus aureus (MRSA): One health perspective approach to the bacterium epidemiology, virulence factors, antibiotic-resistance, and zoonotic impact. Infect Drug Resist 13: 3255-3265.

Andrade-Becerra RJ, Tarazona-Manrique LE, Vargas-Abella JC (2021) Prevalence and effect of intramammary infection due to coagulase-negative staphylococcal (CNS) species in somatic cell counts in milk from Holstein dairy cows in Boyacá, Colombia. Rev Med Vet Zoot 68: 95-104. 

Anyanwu MU, Jaja IF, Nwobi OC (2020) Occurrence and characteristics of mobile colistin resistance (mcr) gene-containing isolates from the environment: a review. Int J Environ Res Public Health 17: 1028.

Badawy B, Elafify M, Farag AMM, Moustafa SM, Sayed-Ahmed MZ, Moawad AA, Algammal AM, Ramadan H, Eltholth M (2022a) Ecological distribution of virulent multidrug-resistant Staphylococcus aureus in livestock, environment, and dairy products. Antibiotics (Basel) 11: 1651. 

Badawy B, Gwida M, Sadat A, El-Toukhy M, Sayed-Ahmed M, Alam N, Ahmad S, Ali MDS, Elafify M (2022b) Prevalence and antimicrobial resistance of virulent Listeria monocytogenes and Cronobacter sakazakii in dairy cattle, the environment, and dried milk with the in vitro application of natural alternative control. Antibiotics (Basel) 11: 1087.

Baştan A, Salar S, Cengiz M, Darbaz İ, Demirel MA, Özen D (2015) The prediction of the prevalence and risk factors for subclinical heifer mastitis in Turkish dairy farms. Turk J Vet Anim Sci 39: 682-687. 

Benjelloun Touimi G, Bennani L, Berrada S, Moussa B, Bennani B (2020) Prevalence and antibiotic resistance profiles of Staphylococcus sp. isolated from food, food contact surfaces and food handlers in a Moroccan hospital kitchen. Lett Appl Microbiol 70: 241-251.

Borowiak M, Baumann B, Fischer J, Thomas K, Deneke C, Hammerl JA, Szabo I, Malorny B (2020) Development of a novel mcr-6 to mcr-9 multiplex PCR and Assessment of mcr-1 to mcr-9 occurrence in colistin-resistant Salmonella enterica isolates from environment, feed, animals and food (2011-2018) in Germany. Front Microbiol 11: 80.

Butaye P (2013) Reports on antimicrobial resistance in commensal E. coli from poultry, pigs, cows and veal calves. (2011, 2012, 2013). https://favv-afsca.be/sites/default/files/pro/amr/rapport/coda-cerva/2011_AMR_E-coli-animals.pdf 

Dadashi M, Sameni F, Bostanshirin N, Yaslianifard S, Khosravi-Dehaghi N, Nasiri MJ, Goudarzi M, Hashemi A, Hajikhani B (2022) Global prevalence and molecular epidemiology of mcr-mediated colistin resistance in Escherichia coli clinical isolates: a systematic review. J Glob Antimicrob Resist 29: 444-461.

Dubois D, Grare M, Prere MF, Segonds C, Marty N, Oswald E (2012) Performances of the Vitek MS matrix-assisted laser desorption ionization–time of flight mass spectrometry system for rapid identification of bacteria in routine clinical microbiology. J Clin Microbiol 50: 2568-2576.

El-Diasty M, Talaat H, Atwa S, Elbaz E, Eissa M (2019) Occurrence of coagulase-negative Staphylococcal mastitis in dairy cows. Mansoura Vet Med J 20: 35-39.

Ellington MJ, Kistler J, Livermore DM, Woodford N (2007) Multiplex PCR for rapid detection of genes encoding acquired metallo-beta-lactamases. J Antimicrob Chemother 59: 321-322.

EUCAST (European Committee on Antimicrobial Susceptibility Testing) (2024) European Committee on Antimicrobial Susceptibility Testing Breakpoint tables for interpretation of MICs and zone diameters Version 14.0. http://www.
 eucast.org

Grima LY, Leliso SA, Bulto AO, Ashenafi D (2021) Isolation, identification, and antimicrobial susceptibility profiles of Staphylococcus aureus from clinical mastitis in Sebeta Town dairy farms. Vet Med Int 2021: 1772658.

Gwida M, Saad T, Elgohary A, Mohamed A (2021) Characterization of methicillin-susceptible and methicillin-resistant Staphylococcus aureus from healthy cattle and buffaloes in a linked community. Mansoura Vet Med J 22: 76-81.

Gundogan N, Avci E (2014) Occurrence and antibiotic resistance of Escherichia coli, Staphylococcus aureus and Bacillus cereus in raw milk and dairy products in Turkey. Int J Dairy Technol 67: 562-569.

Güler L, Ok U, Gündüz K, Gülcü Y, Hadimli HH (2005) Antimicrobial susceptibility and coagulase gene typing of Staphylococcus aureus isolated from bovine clinical mastitis cases in Turkey. J Dairy Sci 88: 3149-3154. 

Hammad AM, Hoffmann M, Gonzalez-Escalona N, Abbas NH, Yao K, Koenig S, Allué-Guardia A, Eppinger M (2019) Genomic features of colistin resistant Escherichia coli ST69 strain harboring mcr-1 on IncHI2 plasmid from raw milk cheese in Egypt. Infect Genet Evol 73: 126-131.

Hasman H, Mevius D, Veldman K, Olesen I, Aarestrup FM (2005) Beta-lactamases among extended-spectrum beta-lactamase (ESBL)-resistant Salmonella from poultry, poultry products and human patients in The Netherlands. J Antimicrob Chemother 56: 115-121.

Hisira V, Zigo F, Kadaši M, Klein R, Farkašová Z, Vargová M, Mudroň P (2023) Comparative analysis of methods for somatic cell counting in cow’s milk and relationship between somatic cell count and occurrence of ıntramammary bacteria. Vet Sci 10: 468.

Hmede Z, Sulaiman AA, Jaafar H, Kassem II (2019) Emergence of plasmid-borne colistin resistance gene mcr-1 in multidrug-resistant Escherichia coli isolated from irrigation water in Lebanon. Int J Antimicrob Agents 54: 102-104. 

Hogan JS, Berry E, Hillerton E (2011) Current concepts of bovine mastitis. 5th ed.; National Mastitis Council: Verona, WI, USA.

Holko I, Tančin V, Vršková M, Tvarožková K (2019) Prevalence and antimicrobial susceptibility of udder pathogens isolated from dairy cows in Slovakia. J Dairy Res 86: 436-439.

Jackson P, Cockcroft P (2002) Clinical examination of farm animals. Blackwell Science Ltd, Oxford, UK. ISBN 0-632-05706-8, pp. 154-166.

Jenkins SN, Okello E, Rossitto PV, Lehenbauer TW, Champagne J, Penedo MC, Arruda AG, Godden S, Rapnicki P, Gorden PJ, Timms LL, Aly SS (2019) Molecular epidemiology of coagulase-negative Staphylococcus species isolated at different lactation stages from dairy cattle in the United States. PeerJ 7: e6749. 

Kadariya J, Smith TC, Thapaliya D (2014) Staphylococcus aureus and staphylococcal food-borne disease: An ongoing challenge in public health. Biomed Res Int 2014: 827965.

Khairullah AR, Kurniawan SC, Sudjarwo SA, Effendi MH, Widodo A, Moses IB, Hasib A, Zahra RL, Gelolodo MA, Kurniawati DA, Riwu KH, Silaen OS, Afnani DA, Ramandinianto SC (2024) Kinship analysis of mecA gene of methicillin-resistant Staphylococcus aureus isolated from milk and risk factors from the farmers in Blitar, Indonesia. Vet World 17: 216-225.

Kou K, Cai H, Huang S, Ni Y, Luo B, Qian H, Ji H, Wang X (2021) Prevalence and characteristics of Staphylococcus aureus isolated from retail raw milk in Northern Xinjiang, China. Front Microbiol 12: 705947.

Leijon M, Atkins E, Persson Waller K, Artursson K (2021) Longitudinal study of Staphylococcus aureus genotypes isolated from bovine clinical mastitis. J Dairy Sci 104: 11945-11954.

Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, Doi Y, Tian G, Dong B, Huang X, Yu LF, Gu D, Ren H, Chen X, Lv L, He D, Zhou H, Liang Z, Liu JH, Shen J (2016) Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis 16: 161-168.

Mus TE, Cetinkaya F, Karahan H, Gurbuz IB, Degirmenci G (2019) Investigation of mecA gene, virulence traits and antibiotic resistance profiles in methicillin-resistant Staphylococcus aureus isolates from dairy products. J Food Saf 39: e12620.

Ngogang MP, Ernest T, Kariuki J, Mouiche MM, Ngogang J, Wade A, van der Sande MA (2021) Microbial contamination of chicken litter manure and antimicrobial resistance threat in an urban area setting in Cameroon. Antibiotics 10: 20. 

Noumi E, Merghni A, Alreshidi M, Del Campo R, Adnan M, Haddad O, De Feo V, Snoussi M (2020) Phenotypic and genotypic characterization with MALDI-TOF-MS based identification of Staphylococcus spp. ısolated from mobile phones with their antibiotic susceptibility, biofilm formation, and adhesion properties. Int J Environ Res Public Health 17: 3761. 

Poirel L, Walsh TR, Cuvillier V, Nordmann P (2011) Multiplex PCR for detection of acquired carbapenemase genes. Diagn Microbiol Infect Dis 70: 119-123.

Rebelo AR, Bortolaia V, Kjeldgaard JS, Pedersen SK, Leekitcharoenphon P, Hansen IM, Guerra B, Malorny B, Borowiak M, Hammerl JA, Battisti A, Franco A, Alba P, Perrin-Guyomard A, Granier SA, De Frutos Escobar C, Malhotra-Kumar S, Villa L, Carattoli A, Hendriksen RS (2018) Multiplex PCR for detection of plasmid-mediated colistin resistance determinants, mcr-1, mcr-2, mcr-3, mcr-4 and mcr-5 for surveillance purposes. Euro Surveill 23: 17-00672.

Rüegsegger F, Ruf J, Tschuor A, Sigrist Y, Rosskopf M, Hässig M (2013) Antimicrobial susceptibility of mastitis pathogens of dairy cows in Switzerland. Schweiz Arch Tierheilkd 156: 483-488. 

Sadat A, Shata RR, Farag AM, Ramadan H, Alkhedaide A, Soliman MM, Elbadawy M, Abugomaa A, Awad A (2022) Prevalence and characterization of PVL-positive Staphylococcus aureus isolated from raw cow’s milk. Toxins (Basel) 14: 97. 

Sağlam AG, Otlu S, Çoşkun MR, Çelik E, Büyük F, Şahin M (2018) Prevalence of subclinical mastitis in cows, isolation of agents and determination of their antibiotic susceptibility. Eurasian J Vet Sci 34: 92-98.

Sheikholeslami MN, Hamidipanah Y, Salehnia F, Arshian S, Hosseini M, Ganjali MR (2022) Multiplex detection of antibiotic residues in milk: application of MCR-ALS on excitation – emission matrix fluorescence (EEMF) data sets. Anal Chem 94: 6206-6215.

Slettemeas JS, Urdahl AM, Mo SS, Johannessen GS, Grave K, Norstrom M, Steinbakk M, Sunde M (2017) Imported food and feed as contributors to the introduction of plasmid-mediated colistin-resistant Enterobacteriaceae to a ‘low prevalence’ country. J Antimicrob Chemother 72: 2675-2677.

Tančin V (2013) Somatic cell counts in milk of dairy cows under practical conditions. Slovak J Anim Sci 46: 31-34.

Tartor YH, Abd El-Aziz NK, Gharieb RM, El Damaty HM, Enany S, Soliman EA, Abdellatif SS, Attia AS, Bahnass MM, El-Shazly YA, Elbediwi M, Ramadan H (2021) Whole-genome sequencing of gram-negative bacteria isolated from bovine mastitis and raw milk: the first emergence of colistin mcr-10 and fosfomycin fosA5 resistance genes in Klebsiella pneumoniae in Middle East. Front Microbiol 12: 770813.

Tel OY, Keskin O, Zonturlu KA, Kaya NBA (2009) Subclinical mastitis prevalance and determination of the antibiotics susceptibility in Sanliurfa region. Fırat Univ Health Sci Vet J 23: 101-106.

Touaitia R, Ibrahim NA, Touati A, Idres T (2025 ) Staphylococcus aureus in bovine mastitis: a narrative review of prevalence, antimicrobial resistance, and advances in detection strategies. Antibiotics (Basel) 14: 810.

Ünal N, Çinar OD (2012) Detection of staphylococcal enterotoxin, methicillin-resistant and Panton – Valentine leukocidin genes in coagulase-negative staphylococci isolated from cows and ewes with subclinical mastitis. Trop Anim Health Prod 44: 369-375.

Ünal N, İstanbulluoğlu E (2009) Phenotypic and genotypic features of Staphylococcus aureus strains isolated from cattle and humans. Ankara Univ Vet Fak Derg 56: 119-126.

Velazquez-Meza ME, Galarde-López M, Carrillo-Quiróz B, Alpuche-Aranda CM (2022) Antimicrobial resistance: one health approach. Vet World 15: 743-749.

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.

World Health Organization (2017). WHO publishes list of bacteria for which new antibiotics are urgently needed. 2017 [cited 2017 February]. http://www.who.int/mediacentre/news/releases/2017/bacteria-antibiotics-needed/en/

Zhang L, Li Y, Bao H, Wei R, Zhou Y, Zhang H, Wang R (2016) Population structure and antimicrobial profile of Staphylococcus aureus strains associated with bovine mastitis in China. Microb Pathog 97: 103-109.

Zigo F, Farkašová Z, Výrostková J, Regecová I, Ondrašovičová S, Vargová M, Sasáková N, Pecka-Kielb E, Bursová Š, Kiss DS (2022) Dairy cows’ udder pathogens and occurrence of virulence factors in staphylococci. Animals (Basel) 12: 470. 

Date

12.12.2025

Type

Article

Identifier

DOI: 10.24425/pjvs.2025.157278
×