Clinical and molecular characterization of both methicillin-resistant andsensitive staphylococcus aureus mastitis


Keywords:
MRSA Bovine Mastitis Staphylococcus aureus
A. OREIB
H. KHALIFA
A. EID
A. AHMED
T. SHIMAMOTO
T. SHIMAMOTO
Abstract

This study targeted bovine mastitis as a possible source of livestock-associated methicillin-resistant Staphylococcus aureus (MRSA), to identify clinical signs associated with MRSA- and non-MRSA-associated mastitis. Thirty-eight mastitis cases (68 infected quarters) were investigated. Gram-positive cocci-shaped isolates were selected based on Baird Parker agar growth as well as Gram-stained bacterial smears. Molecular screening for Staphylococcus aureus (S. aureus) yielded 17 isolates, of which five (29.41%) were methicillin resistant. The five isolates were mecA positive, but mecC negative. Multilocus sequence typing (MLST) indicated that sequence type 1 (ST1) was the identified type of all isolates of MRSA. S. aureus-associated cases showed different clinical forms of mastitis, including subclinical, acute, chronic, and gangrenous. Additionally, subclinical mastitis was the only detected condition associated with MRSA, which may represent a potential hidden risk for humans. Phenotypically, isolates of MRSA showed resistance to all of the tested β-lactam antimicrobials, with marked resistance to tetracycline and gentamycin. Based on our knowledge, this is the first report to identify MRSA ST1 in Egypt. Bovine mastitis could be a source for the dissemination of MRSA to humans and other animals. Additionally, while methicillin-resistance may have no effect on the clinical outcome of mastitis, it does affect therapeutic success, particularly when β-lactam antimicrobials are used.

Article Details
  • Section
  • Research Articles
Downloads
Download data is not yet available.
References
Akineden O, Annemuller C, Hassan AA, Lammler C, Wolter W, Zschock M (2001) Toxin genes and other characteristics of Staphylococcus aureus isolates from milk of cows with mastitis. Clininical and Diagnostic Laboratory Immunology 8: 959-964.
Alba P, Feltrin F, Cordaro G, Porrero MC, Kraushaar B, Argudín MA, Nykäsenoja S, Monaco M, Stegger M, Aarestrup FM, Butaye P, Franco A, Battisti A (2015) Livestock-associated methicillin resistant and methicillin susceptible Staphylococcus aureus sequence type (CC)1 in European farmed animals: high genetic relatedness of isolates from Italian cattle herds and humans. PLoS ONE 10: e0137143.
Anderson JC (1983) Veterinary aspects of staphylococci, In: Easmon, C.S.F., Adlam, C. (Eds), Staphylococci and staphylococcal infections, vol 1: Clinical and epidemiological aspects. London, Academic Press. PP. 193-241.
Barkema HW, Schukken YH, Zadoks RN (2006) Invited Review: The role of cow, pathogen, and treatment regimen in the therapeutic success of bovine Staphylococcus aureus mastitis. Journal of Dairy Science 89: 1877-1895.
Borg MA, Kraker M, Scicluna E, Sande-Bruinsma NV, Tiemersma E, Jos Monen J et al. (2007) Prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in invasive isolates from southern and eastern Mediterranean countries. The Journal of Antimicrobial Chemotherapy 60: 1310-1315.
Clinical and Laboratory Standards Institute (2005) Performance standards for antimicrobial susceptibility testing; 19th informational supplement M100-S15. CLSI, Wayne, PA. USA.
Cuny C, Wieler LH, Witte W (2015) Livestock-associated MRSA: The impact on humans. Antibiotics 4: 521-543.
Ekkelenkamp MB, Sekkat M, Carpaij N, Troelstra A, Bonten MJ (2006) Endocarditis due to methicillin-resistant Staphylococcus aureus originating from pigs. Nederlands Tijdschrift voor Geneeskunde 150:2442-2447.
Elhaig MM, Selim A (2015) Molecular and bacteriological investigation of subclinical mastitis caused by Staphylococcus aureus and Streptococcus agalactiae in domestic bovids from Ismailia, Egypt. Tropical Animal Health and Production 47: 271-276.
Enright MC, Day NPJ, Davies CE, Peacock SJ, Spratt BG (2000) Multilocus Sequence Typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. Journal of Clinical Microbiology 38: 1008-1015.
García-Álvarez L, Holden MT, Lindsay H, Webb CR, Brown DF, Curran MD, Walpole E, Brooks K, Pickard DJ, Teale C, Parkhill J, Bentley SD, Edwards GF, Girvan EK, Kearns AM, Pichon B, Hill RL, Larsen AR, Skov RL, Peacock SJ, Maskell DJ, Holmes MA (2011) Meticillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. The Lancet Infectious Diseases 11(8): 595-603.
Graveland H, Duim B, van Duijkeren E, Heederika D, Wagenaar JA (2011) Livestock-associated methicillin-resistant Staphylococcus aureus in animals and humans. International Journal of Medical Microbiology 301: 630-634.
Hartman BJ, Tomasz A (1984) Low-affinity penicillin-binding protein associated with β-lactam resistance in Staphylococcus aureus. Journal of Bacteriology 158: 513-516.
Haveri M, Roslof A, Rantala L, Pyorala S (2007) Virulence genes of bovine Staphylococcus aureus from persistent and nonpersistent intramammary infections with different clinical characteristics. Journal of Applied Microbiology 103: 993-1000.
Houe H, Vaarst M, Enevoldsen C (2002) Clinical parameters for assessment of udder health in Danish dairy herds. Acta Veterinaria Scandinavica 43: 173-184.
Juhász-Kaszanyitzky É, Jánosi S, Somogyi P, Dán Á, Bloois LV, Duijkeren EV, Wagenaar JA (2007) MRSA transmission between cows and humans. Emerging Infectious Diseases 13: 630-632.
Kasikci G, Cetin O, Bingol EB, Gunduz MC (2012) Relations between electrical conductivity, somatic cell count, California mastitis test and some quality parameters in the diagnosis of subclinical mastitis in dairy cows. Turkish Journal of Veterinary and Animal Sciences 36: 49-55.
Lammers A, Kruijt E, van de Kuijt C, Nuijten PJM, Smith HE (2000) Identification of Staphylococcus aureus genes expressed during growth in milk: a useful model for selection of genes important in bovine mastitis?. Microbiology 146: 981-987.
Monecke S, Kuhnert P, Hotzel H, Slickers P, Ehricht R (2007) Microarray based study on virulence-associated genes and resistance determinants of Staphylococcus aureus isolates from cattle. Veterinary Microbiology125: 128-140.
Paterson GK, Larsen AR, Robb A, Edwards GE, Pennycott TW, Foster G, Mot D, Hermans K, Baert K, Peacock SJ, Parkhill J, Zadoks RN, Holmes MA (2012) The newly described mecA homologue, mecALGA251, is present in methicillin-resistant Staphylococcus aureus isolates from a diverse range of host species. The Journal of Antimicrobial Chemotherapy 67: 2809–2813.
Poutrel B (1985) Generalites sur les mammites de la vache laitiere. Processus infectieux, epidemiologie, diagnostics, methodes de controle. Revue de Médecine Vétérinaire 161: 497-511.
Quinn SG, Carter HE, Markey BK, Carter GR (1994) Clinical veterinary microbiology. 1st Ed. Mosby. Year Book Europe Limited. Sasaki T, Tsubakishita S, Tanaka Y, Sakusabe A, Ohtsuka M, Hirotaki S, Kawakami T, Fukata T, Hiramatsu k (2010) Multiplex-PCR method for species identification of coagulase-positive Staphylococci. Journal of Clinical Microbiology 48: 765-769.
Silva WP, Destro MT, Landgraf M, Franco BDGM (2000) Biochemical characteristics of typical and atypical Staphylococcus aureus in mastitic milk and environmental samples of Brazalian dairy farms. Brazilian Journal of Microbiology 31: 103-106.
Spoor LE, McAdam PR, Weinert LA, Rambaut A, Hasman H, Aarestrup FM, Kearns AM, Larsen AR, Skov RL, Fitzgerald JR (2013) Livestock origin for a human pandemicclone of community-associated methicillin-resistant Staphylococcus aureus. MBio 4: doi:10.1128/mBio.00356-13.
Stefani S, Chung DR, Lindsay JA, Friedrich AW, Kearns AM, Westh H, MacKenzie FM (2012) Methicillin-resistant Staphylococcus aureus (MRSA): global epidemiology and harmonisation of typing methods. International Journal of Antimicrobial Agents 39: 273-282.
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 mecALGA251. Clinical Microbiology and Infection 18: 395-400.
Vanderhaeghen W, Cerpentier T, Adriaensen C, Vicca J, Hermans K, Butaye P (2010) Methicillin-resistant Staphylococcus aureus (MRSA) ST398 associated with clinical and subclinical mastitis in Belgian cows. Veterinary Microbiology 144: 166-171.
Walther B, Monecke S, Ruscher C, Friedrich AW, Ehricht R, Slickers P, Soba A, Wleklinski CG, Wieler LH, Lubke-Becker A (2009) Comparative molecular analysis substantiates zoonotic potential of equine methicillin-resistant Staphylococcus aureus. Journal of Clinical Microbiology 47: 704-710.
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. Infection Genetics and Evolution 31: 9-16.
Witte W, Strommenger B, Stanek C, Cuny C (2007) Methicillin-resistant Staphylococcus aureus ST398 in humans and animals, Central Europe. Emerging Infectious Diseases 13: 255-258.
Zhang K, McClure J, Elsayed S, Louie T, Conly J (2005) Novel Multiplex PCR assay for Characterization and concomitant subtyping of Staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus. Journal of Clinical Microbiology 43: 5026-5033.
Most read articles by the same author(s)