Distribution of bacterial pathogens and antimicrobial resistance in cows with clinical mastitis in a dairy farm, Türkiye


Published: Oct 21, 2024
Keywords:
Antibiotic resistance Bovine mastitis Pathogens Multidrug
B Guner
https://orcid.org/0000-0001-6414-6752
B Ozturk
AA Erkan
M Erturk
N Ucan
A Keskin
Abstract

This study aimed to identify the pathogens causing clinical mastitis (CM) and their resistance levels to six common antimicrobials in a dairy farm in Turkey. A total of 973 CM milk samples were cultured and a Kirby-Bauer disc diffusion method was performed for antimicrobial susceptibility. While 64.0% (623/973) of CM samples were culture-positive, 36.0% (350/973) of CM samples yielded no growth. Escherichia coli was the most frequently isolated pathogen (36.3%), followed by coagulase-negative staphylococci (8.3%), Streptococcus dysgalactiae (7.3%), Staphylococcus aureus (3.1%), Streptococcus uberis (1.5%), Enterococcus spp. (1.4%), Mycoplasma spp. (1.4%), Streptococcus agalactiae (0.7%), and Corynebacterium spp. (0.4%). Antimicrobial resistance was higher (P > 0.01) to amoxicillin/clavulanic acid (AMC, 32.3%) than that to enrofloxacin (ENR, 23.4%), cefoperazone (CFP, 17.9%), cefquinome (CEQ, 17.7%), penicillin G (P, 15.2%), and gentamicin (CN, 3.6%) in culture-positive 642 isolates. For E. coli isolates, percentage of resistance to AMC, ENR, CFP, CEQ, P, and CN was 37.7, 30.6, 24.4, 23.2, 5.9, and 1.1%, respectively. Resistance to AMC (31.2%) and P (46.3%) was higher in CNS than Strep. dysgalactiae isolates (1.5% and 12.7%), respectively. Multidrug resistance was detected in 34 E. coli isolates (9.6%), 7 CNS isolates (8.6%), and 2 Strep. dysgalactiae (2.8%). In conclusion, the higher identification of E. coli demonstrated the higher risk of environmental microorganisms for CM in this study. Higher resistance to commonly used five of six antimicrobials showed the requirement of frequent bacteriological and antimicrobial susceptibility tests for CM. Thus, these implementations could increase treatment efficacy in cows and reduce antimicrobial resistance.

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Author Biography
B Guner, University of Balikesir

Department of Obstetrics and Gynecology

References
Abdi, R.D., Gillespie, B.E., Ivey, S., Pighetti, G.M., Almeida, R.A., Dego,
O.K. (2021). Antimicrobial resistance of major bacterial pathogens
from dairy cows with high somatic cell count and clinical mastitis.
Animals 11, 1-14.
Alanis, V.M., Tomazi, T., Santisteban, C., Nydam, D.V, Ospina, P.A.
(2022). Calculating clinical mastitis frequency in dairy cows: Incidence risk at cow level, incidence rate at cow level, and incidence rate
at quarter level. Prev. Vet. Med. 198, 105527.
Alvarez-Uria, G., Gandra, S., Mandal, S., Laxminarayan, R. (2018). Global forecast of antimicrobial resistance in invasive isolates of Escherichia coli and Klebsiella pneumoniae. Int. J. Infect. Dis. 68, 50-53.
Ardicli, O., Kahya Demirbilek, S., Carli, K.T. (2022). Pathogens isolated
from bovine clinical mastitis and their antimicrobial resistance. Med.
Awandkar, S.P., Kulkarni, M.B., & Khode, N.V. (2022). Bacteria from
bovine clinical mastitis showed multiple drug resistance. Vet. Res.
Commun. 46(1), 147-158.
Barlow, J. (2011). Mastitis therapy and antimicrobial susceptibility: A
multispecies review with a focus on antibiotic treatment of mastitis in
dairy cattle. J. Mammary Gland Biol. Neoplasia 16, 383-407.
Ben, Y., Fu, C., Hu, M., Liu, L., Wong, M.H., Zheng, C. (2019). Human
health risk assessment of antibiotic resistance associated with antibiotic residues in the environment: A review. Environ. Res. 169, 483-
Bolte, J., Zhang, Y., Wente, N., Krömker, V. (2020). In vitro susceptibility
of mastitis pathogens isolated from clinical mastitis cases on northern
german dairy farms. Vet. Sci. 7.
Bradley, A.J., Green, M.J. (2001). Aetiology of clinical mastitis in six
Somerset dairy herds. Vet. Rec. 148(22), 683-686.
Bradley, A.J., Leach, K.A., Breen, J.E., Green, L.E., Green, M.J. (2007).
Survey of the incidence and aetiology of mastitis on dairy farms in
England and Wales. Vet. Rec. 160, 253-258.
Brennecke, J., Falkenberg, U., Wente, N., Krömker, V. (2021). Are severe
mastitis cases in dairy cows associated with bacteremia? Animals 11,
-9.
Cheng, J., Qu, W., Barkema, H.W., Nobrega, D.B., Gao, J., Liu, G., De
Buck, J., Kastelic, J.P., Sun, H., Han, B. (2019). Antimicrobial resistance profiles of 5 common bovine mastitis pathogens in large Chinese dairy herds. J. Dairy Sci. 102, 2416-2426.
Cheng, W.N., Han, S.G. (2020). Bovine mastitis: Risk factors, therapeutic
strategies, and alternative treatments - A review. Asian-Australas. J.
Anim. Sci. 33, 1699-1713.
CLSI (2018). Clinical and Laboratory Standards Institute: Performance
standards for antimicrobial susceptibility testing. Twenty-ninth informational Suppl. M100-S29 32, Wayne, P.A.
de Jong, A., Garch, F.E., Simjee, S., Moyaert, H., Rose, M., Youala, M.,
Siegwart, E. (2018). Monitoring of antimicrobial susceptibility of udder pathogens recovered from cases of clinical mastitis in dairy cows
across Europe: VetPath results. Vet. Microbiol. 213, 73-81.
Doehring, C., Sundrum, A. (2019). The informative value of an overview
on antibiotic consumption, treatment efficacy and cost of clinical
mastitis at farm level. Prev. Vet. Med. 165, 63-70.
Duse, A., Persson-Waller, K., Pedersen, K. (2021). Microbial aetiology,
antibiotic susceptibility and pathogen-specific risk factors for udder
pathogens from clinical mastitis in dairy cows. Animals 11, 2113.
Dyson, R., Charman, N., Hodge, A., Rowe, S.M., Taylor, L.F. (2022). A
survey of mastitis pathogens including antimicrobial susceptibility
in southeastern Australian dairy herds. J. Dairy Sci. 105, 1504-1518.
Gao, J., Barkema, H.W., Zhang, L., Liu, G., Deng, Z., Cai, L., Shan, R.,
Zhang, S., Zou, J., Kastelic, J.P., Han, B. (2017). Incidence of clinical
mastitis and distribution of pathogens on large Chinese dairy farms.
J. Dairy Sci. 100, 4797-4806.
Guerra, S.T., Orsi, H., Joaquim, S.F., Guimarães, F.F., Lopes, B.C., Dalanezi, F.M., Leite, D.S., Langoni, H., Pantoja, J.C.F., Rall, V.L.M.,
Hernandes, R.T., Lucheis, S.B., Ribeiro, M.G. (2020). Short communication: Investigation of extra-intestinal pathogenic Escherichia coli
virulence genes, bacterial motility, and multidrug resistance pattern
of strains isolated from dairy cows with different severity scores of
clinical mastitis. J. Dairy Sci. 103, 3606-3614.
Heikkilä, A.M., Liski, E., Pyörälä, S., Taponen, S. (2018). Pathogen-specific production losses in bovine mastitis. J. Dairy Sci. 101, 9493-
Hertl, J.A., Schukken, Y.H., Bar, D., Bennett, G.J., González, R.N., Rauch,
B.J., Welcome, F.L., Tauer, L.W., Gröhn, Y.T. (2011). The effect of
recurrent episodes of clinical mastitis caused by gram-positive and
gram-negative bacteria and other organisms on mortality and culling
in Holstein dairy cows. J. Dairy Sci. 94, 4863-4877.
Jamali, H., Barkema, H.W., Jacques, M., Lavallée-Bourget, E.M., Malouin, F., Saini, V., Stryhn, H., Dufour, S. (2018). Invited review: Incidence, risk factors, and effects of clinical mastitis recurrence in dairy
cows. J. Dairy Sci. 101, 4729-4746.
Krishnamoorthy, P., Kuralayanapalya, P.S., Jayamma, K.S., Shome, B.R.,
Patil, S.S., Amachawadi, R.G. (2021). An understanding of the global
status of major bacterial pathogens of milk concerning bovine mastitis: A systematic review and meta-analysis (scientometrics). Pathogens 10, 545.
Kuehn, J.S., Gorden, P.J., Munro, D., Rong, R., Dong, Q., Plummer, P.J.,
Wang, C., Phillips, G.J. (2013). Bacterial community profiling of
milk samples as a means to understand culture-negative bovine clinical mastitis 8.
Lago, A., Godden, S.M., Bey, R., Ruegg, P.L., Leslie, K. (2011). The selective treatment of clinical mastitis based on on-farm culture results:
I. Effects on antibiotic use, milk withholding time, and short-term
clinical and bacteriological outcomes. J. Dairy Sci. 94, 4441-4456.
Lehtolainen, T., Shwimmer, A., Shpigel, N.Y., Honkanen-Buzalski, T.,
Pyörälä, S. (2003). In vitro antimicrobial susceptibility of Escherichia coli isolates from clinical bovine mastitis in Finland and Israel. J.
Dairy Sci. 86, 3927-3932.
Levison, L.J., Miller-Cushon, E.K., Tucker, A.L., Bergeron, R., Leslie,
K.E., Barkema, H.W., DeVries, T.J. (2016). Incidence rate of pathogen-specific clinical mastitis on conventional and organic Canadian
dairy farms. J. Dairy Sci. 99, 1341-1350.
Lopes, T.S., Fussieger, C., Rizzo, F.A., Silveira, S., Lunge, V.R., Streck,
A.F. (2022). Species identification and antimicrobial susceptibility
profile of bacteria associated with cow mastitis in southern Brazil.
Pesqui. Vet. Bras. 42.
Miles, A.M., Huson, H.J. (2021). Graduate Student Literature Review:
Understanding the genetic mechanisms underlying mastitis. J. Dairy
Sci. 104, 1183-1191.
NRC (2001). Nutrient requirements of dairy cattle, 7th Edition, The National Academies Press.
NMC (2017). Laboratoryhandbook on bovine mastitis, 3rd Edition, National Mastitis Council.
Oliveira, L., Hulland, C., Ruegg, P.L. (2013). Characterization of clinical
mastitis occurring in cows on 50 large dairy herds in Wisconsin. J.
Dairy Sci. 96, 7538-7549.
Oliver, S.P., Murinda, S.E. (2012). Antimicrobial resistance of mastitis
pathogens. Vet. Clin. North Am. - Food Anim. Pract. 28, 165-185.
Ozbey, G., Cambay, Z., Yilmaz, S., Aytekin, O., Zigo, F., Ozçelik, M., &
Otlu, B. (2022). Identification of bacterial species in milk by MALDI-TOF and assessment of some oxidant-antioxidant parameters
in blood and milk from cows with different health status of the udder. Pol. J. Vet. Sci. 25, 269-277.
Öztürk, D., Şahan Yapıcıer, Ö., Şabanoğlu, E., Kaya, M., Pehlivanoğlu,
F., Türütoğlu, H. (2019). The antibiotic resistance of gram negative
bacteria isolated from bovine mastitis. Van Vet J 30, 85-89.
Riekerink, R.G.M.O., Barkema, H.W., Stryhn, H. (2007). The effect of
season on somatic cell count and the incidence of clinical mastitis. J.
Dairy Sci. 90, 1704-1715.
Ruegg, P.L. (2017). A 100-Year Review: Mastitis detection, management,
and prevention. J. Dairy Sci. 100, 10381-10397.
Saini, V., McClure, J.T., Scholl, D.T., DeVries, T.J., Barkema, H.W.
(2013). Herd-level relationship between antimicrobial use and presence or absence of antimicrobial resistance in gram-negative bovine
mastitis pathogens on Canadian dairy farms. J. Dairy Sci. 96, 4965-
Santman-Berends, I.M.G.A., Lam, T.J.G.M., Keurentjes, J., van Schaik,
G. (2015). An estimation of the clinical mastitis incidence per 100
cows per year based on routinely collected herd data. J. Dairy Sci.
, 6965-6977.
Singha, S., Koop, G., Persson, Y., Hossain, D., Scanlon, L., Derks, M.,
Hoque, A., Rahman, M. (2021). Incidence, etiology, and risk factors
of clinical mastitis in dairy cows under semi-tropical circumstances
in Chattogram, Bangladesh. Animals 11, 2255.
Steeneveld, W., Hogeveen, H., Barkema, H.W., Van Den Broek, J.,
Huirne, R.B.M. (2008). The influence of cow factors on the incidence
of clinical mastitis in dairy cows. J. Dairy Sci. 91, 1391-1402.
Supré, K., Lommelen, K., De Meulemeester, L. (2014). Antimicrobial
susceptibility and distribution of inhibition zone diameters of bovine
mastitis pathogens in Flanders, Belgium. Vet. Microbiol. 171, 374-
Verbeke, J., Piepers, S., Supré, K., De Vliegher, S. (2014). Pathogen-specific incidence rate of clinical mastitis in Flemish dairy herds, severity, and association with herd hygiene. J. Dairy Sci. 97, 6926-6934.
Wente, N., Krömker, V. (2020). Streptococcus dysgalactiae-Contagious or
environmental?. Animals, 10, 2185.
Yu, Z.N., Wang, J., Ho, H., Wang, Y.T., Huang, S.N., Han, R.W. (2020).
Prevalence and antimicrobial-resistance phenotypes and genotypes of
Escherichia coli isolated from raw milk samples from mastitis cases
in four regions of China. J. Glob. Antimicrob. Resist. 22, 94-101.
Zhang, Z., Li, X.P., Yang, F., Luo, J.Y., Wang, X.R., Liu, L.H., Li, H.S.
(2016). Influences of season, parity, lactation, udder area, milk yield,
and clinical symptoms on intramammary infection in dairy cows. J.
Dairy Sci. 99, 6484-6493.
Zigo, F., Elečko, J., Farkašová, Z., Zigová, M., Vasiľ, M., Ondrašovičová,
S., Lenka, K. (2019). Preventive methods in reduction of mastitis
pathogens in dairy cows. J. Microbiol. Bioctechnol. Food Sci. 9, 121-
Zigo, F., Vasil’, M., Ondrašovičová, S., Výrostková, J., Bujok, J., Pecka-Kielb, E. (2021). Maintaining optimal mammary gland health and
prevention of mastitis. Front. Vet. Sci. 8, 607311.
Zigo, F., Farkašová, Z., Výrostková, J., Regecová, I., Ondrašovičová, S.,
Vargová, M., Sasáková, N., Pecka-Kielb, E., Bursová, S., Kiss, D.
S. (2022). Dairy cows’udder pathogens and occurrence of virulence
factors in Staphylococci. Animals, 12, 470