Journal of Veterinary Science

The Korean Society of Veterinary Science (대한수의학회)
권호 표지
DOI QR코드

DOI QR Code

Intramammary preparation of enrofloxacin hydrochloride-dihydrate for bovine mastitis (biofilm-forming Staphylococcus aureus)

  • Diana Cordova-Gonzalez (Departamento de Fisiologia y Farmacologia, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autonoma de Mexico) ;
  • Edgar Alfonseca-Silva (Departamento de Microbiologia e Inmunologia, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autonoma de Mexico) ;
  • Lilia Gutierrez (Departamento de Fisiologia y Farmacologia, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autonoma de Mexico) ;
  • Graciela Tapia-Perez (Departamento de Genetica y Bioestadistica, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autonoma de Mexico) ;
  • Hector Sumano (Departamento de Fisiologia y Farmacologia, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autonoma de Mexico)
  • Received : 2023.10.05
  • Accepted : 2023.11.14
  • Published : 2024.01.31
Download PDF
⟨ Previous Next ⟩

Abstract

Background: Chronic bovine mastitis is linked to biofilm-producing Staphylococcus aureus (bp-Sa) or Staphylococcus coagulase-negative (bp-Scn). Objectives: Bp-Sa and bp-Scn were treated with intramammary preparations of either enrofloxacin HCl·2H2O-dimethyl-sulfoxide-chitosan (enro-C/DMSO/chitosan) or enro-C alone. Their potential to inhibit and degrade biofilm formation in vitro was also assessed. Methods: Milk samples were obtained from the affected quarters in a herd. Phenotypical and genotypical identifications as biofilm-producing Staphylococcus species were carried out. Enro-C/DMSO/chitosan and enro-C alone were assessed to determine their in vitro efficacy in interfering with biofilm formation and their bactericidal effects. A prolonged eight-day treatment with a twice-daily intramammary insertion of 10 mL of enro-C/DMSO/chitosan or enro-C alone was set to evaluate the clinical and bacteriological cures on day 10 in 15 cows per group and the biofilm-inhibiting ability. Results: Fifty-seven percent of the isolates were identified as Staphylococcus spp., of which 50% were bp-Sa, 46% bp-Scn, and 4% Staphylococcus pseudintermedius. One hundred percent of the S. aureus isolated and 77% of Staphylococcus coagulase-negative were biofilm producers. In both groups, the icaA and icaD biofilm-producing genes were identified. The experimental preparation could inhibit biofilm formation, degrade mature biofilms, and have well-defined microbicidal effects on planktonic and biofilm bacteria. The respective clinical and bacteriological cure rates were 100% and 80% for enro-C/DMSO/chitosan and 41.7% and 25% for enro-C alone. Conclusions: Enro-C/DMSO/chitosan eliminates bp-Sa and bp-Scn from cases of chronic bovine mastitis.

Keywords

Acknowledgement

This study was supported by the research program PAPIIT at UNAM No. ITT200322. Diana Cordova was awarded a CONAHCYT, Mexico graduate scholarship. A sabbatical program from the PASPA-DGAPA-Universidad Nacional Autonoma de Mexico supported Edgar Alfonseca-Silva.

References

  1. Kalinska A, Wojcik A, Slosarz J, Kruzinska B, Michalczuk M, Jaworski S, et al. Occurrence and aetiology of staphylococcal mastitis - a review. Anim Sci Pap Rep. 2018;36(3):263-273.
  2. Saeed SI, Vivian L, Zalati CW, Sani NI, Aklilu E, Mohamad M, et al. Antimicrobial activities of graphene oxide against biofilm and intracellular Staphylococcus aureus isolated from bovine mastitis. BMC Vet Res. 2023;19(1):10.
  3. Nagahata H, Kawai H, Higuchi H, Kawai K, Yayou K, Chang CJ. Altered leukocyte responsiveness in dairy cows with naturally occurring chronic Staphylococcus aureus mastitis. J Vet Med Sci. 2011;73(7):885-894. https://doi.org/10.1292/jvms.10-0379
  4. Kampa J, Sukolapong V, Chaiyotwittakun A, Rerk-u-suke S, Polpakdee A. Chronic mastitis in small dairy cattle herds in Muang Khon Kaen. Thai J Vet Med. 2010;40(3):265-272. https://doi.org/10.56808/2985-1130.2236
  5. Piessens V, De Vliegher S, Verbist B, Braem G, Van Nuffel A, De Vuyst L, et al. Characterization of coagulase-negative staphylococcus species from cows' milk and environment based on bap, icaA, and mecA genes and phenotypic susceptibility to antimicrobials and teat dips. J Dairy Sci. 2012;95(12):7027-7038. https://doi.org/10.3168/jds.2012-5400
  6. Cardozo LL, Thaler Neto A, Souza GN, Picinin LC, Felipus NC, Reche NL, et al. Risk factors for the occurrence of new and chronic cases of subclinical mastitis in dairy herds in southern Brazil. J Dairy Sci. 2015;98(11):7675-7685. https://doi.org/10.3168/jds.2014-8913
  7. Pasachova GJ, Ramirez MS, Munoz LM. Staphylococcus aureus: generalidades, mecanismos de patogenicidad y colonizacion celular. NOVA. 2019;17(32):25-38. CROSSREF https://doi.org/10.22490/24629448.3631
  8. Bohl LP, Isaac P, Breser ML, Orellano MS, Correa SG, Tolosa de Talamoni NG, et al. Interaction between bovine mammary epithelial cells and planktonic or biofilm Staphylococcus aureus: the bacterial lifestyle determines its internalization ability and the pathogen recognition. Microb Pathog. 2021;152:104604.
  9. Royster E, Wagner S. Treatment of mastitis in cattle. Vet Clin North Am Food Anim Pract. 2015;31(1):17-46. https://doi.org/10.1016/j.cvfa.2014.11.010
  10. Miranda-Calderon JE, Gutierrez L, Flores-Alamo M, Garcia-Gutierrez P, Sumano H. Enrofloxacin hydrochloride dihydrate. Acta Crystallogr Sect E Struct Rep Online. 2014;70(Pt 4):o468-o469. https://doi.org/10.1107/S1600536814006059
  11. Martinez-Cortes I, Gutierrez L, Tapia G, Ocampo L, Sumano H. Serum and milk concentrations of enrofloxacin in cows intramammarily treated with a new enrofloxacin-polymorph. Med Weter. 2016;72(11):686-692. CROSSREF https://doi.org/10.21521/mw.5587
  12. Viveros M, Lopez-Ordaz R, Gutierrez L, Miranda-Calderon JE, Sumano H. Efficacy assessment of an intramammary treatment with a new recrystallized enrofloxacin vs ceftiofur and parenteral enrofloxacin in dairy cows with nonsevere clinical mastitis. J Vet Pharmacol Ther. 2018;41(1):e1-e9. https://doi.org/10.1111/jvp.12441
  13. Alfonseca-Silva E, Cruz-Villa JC, Gutierrez L, Sumano H. Successful treatment of recurrent subclinical mastitis in cows caused by enrofloxacin resistant bacteria by means of the sequential intramammary infusion of enrofloxacin HCl-2H2O and ceftiofur HCl: a clinical trial. J Vet Sci. 2021;22(6):e78.
  14. Silva-Dias A, Palmeira-de-Oliveira A, Miranda IM, Branco J, Cobrado L, Monteiro-Soares M, et al. Anti-biofilm activity of low-molecular weight chitosan hydrogel against Candida species. Med Microbiol Immunol. 2014;203(1):25-33. https://doi.org/10.1007/s00430-013-0311-4
  15. Hebling J, Bianchi L, Basso FG, Scheffel DL, Soares DG, Carrilho MR, et al. Cytotoxicity of dimethyl sulfoxide (DMSO) in direct contact with odontoblast-like cells. Dent Mater. 2015;31(4):399-405. https://doi.org/10.1016/j.dental.2015.01.007
  16. Yahya MF, Alias Z, Karsani SA. Antibiofilm activity and mode of action of DMSO alone and its combination with afatinib against Gram-negative pathogens. Folia Microbiol (Praha). 2018;63(1):23-30. https://doi.org/10.1007/s12223-017-0532-9
  17. Deutch CE. Inhibition of urease activity in the urinary tract pathogens Staphylococcus saprophyticus and Proteus mirabilis by dimethylsulfoxide (DMSO). J Appl Microbiol. 2020;128(5):1514-1523. https://doi.org/10.1111/jam.14560
  18. Swinkels JM, Kromker V, Lam TJ. Efficacy of standard vs. extended intramammary cefquinome treatment of clinical mastitis in cows with persistent high somatic cell counts. J Dairy Res. 2014;81(4):424-433. https://doi.org/10.1017/S0022029914000442
  19. McDougall S, Clausen L, Hintukainen J, Hunnam J. Randomized, controlled, superiority study of extended duration of therapy with an intramammary antibiotic for treatment of clinical mastitis. J Dairy Sci. 2019;102(5):4376-4386. https://doi.org/10.3168/jds.2018-15141
  20. Aguilar RF, Anguiano BR, Atilano LD, Bazan ME, Castaneda RA, Castanon OL, et al. Atlas Fotografico de Laboratorio de Bacteriologia y Micologia Veterinaria. 1st ed. Mexico City: Faculty of Veterinary Medicine, National Autonomous University of Mexico; 2014.
  21. Mariana NS, Atshan S, Neela V, Sekawi Z. Evaluation of modified Congo red agar for detection of biofilm produced by clinical isolates of methicillin-resistance Staphylococcus aureus. Afr J Microbiol Res. 2009;3(6):330-338.
  22. Pena J, Uffo O. Produccion de biofilme en genotipos de Staphylococcus aureus aislados de mastitis bovina en Cuba. Rev Salud Anim. 2013;35(3):189-196.
  23. Pampariene I, Veikutis V, Oberauskas V, Zymantiene J, Zelvyte R, Stankevicius A, et al. Thermography based inflammation monitoring of udder state in dairy cows: sensitivity and diagnostic priorities comparing with routine California mastitis test. J Vibroeng. 2016;18(1):511-521.
  24. Lin JJ, Chang CH, Pal N. A revisit to contingency table and tests of independence: bootstrap is preferred to Chi-square approximations as well as Fisher's exact test. J Biopharm Stat. 2015;25(3):438-458. https://doi.org/10.1080/10543406.2014.920851
  25. Faul F, Erdfelder E, Lang AG, Buchner A. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007;39(2):175-191. https://doi.org/10.3758/BF03193146
  26. Sumano LH, Ocampo CL, Gutierrez OL. Farmacologia Veterinaria. 4th ed. Mexico City: Aranda; 2015.
  27. Khan F, Pham DT, Oloketuyi SF, Manivasagan P, Oh J, Kim YM. Chitosan and their derivatives: antibiofilm drugs against pathogenic bacteria. Colloids Surf B Biointerfaces. 2020;185:110627.
  28. Confederat LG, Tuchilus CG, Dragan M, Sha'at M, Dragostin OM. Preparation and antimicrobial activity of chitosan and its derivatives: a concise review. Molecules. 2021;26(12):3694.
  29. Hoang C, Nguyen AK, Nguyen TQ, Fang W, Han B, Hoang BX, et al. Application of dimethyl sulfoxide as a therapeutic agent and drug vehicle for eye diseases. J Ocul Pharmacol Ther. 2021;37(8):441-451. https://doi.org/10.1089/jop.2021.0043
  30. Lee JS, Bae YM, Han A, Lee SY. Development of Congo red broth method for the detection of biofilmforming or slime-producing Staphylococcus sp. Lebensm Wiss Technol. 2016;73:707-714. https://doi.org/10.1016/j.lwt.2016.03.023
  31. Idrees M, Sawant S, Karodia N, Rahman A. Staphylococcus aureus biofilm: morphology, genetics, pathogenesis and treatment strategies. Int J Environ Res Public Health. 2021;18(14):7602.
  32. Yang B, Lei Z, Zhao Y, Ahmed S, Wang C, Zhang S, et al. Combination susceptibility testing of common antimicrobials in vitro and the effects of sub-MIC of antimicrobials on Staphylococcus aureus biofilm formation. Front Microbiol. 2017;8:2125.
  33. Felipe V, Breser ML, Bohl LP, Rodrigues da Silva E, Morgante CA, Correa SG, et al. Chitosan disrupts biofilm formation and promotes biofilm eradication in Staphylococcus species isolated from bovine mastitis. Int J Biol Macromol. 2019;126:60-67. https://doi.org/10.1016/j.ijbiomac.2018.12.159
  34. Breser ML, Felipe V, Bohl LP, Orellano MS, Isaac P, Conesa A, et al. Chitosan and cloxacillin combination improve antibiotic efficacy against different lifestyle of coagulase-negative Staphylococcus isolates from chronic bovine mastitis. Sci Rep. 2018;8(1):5081.
  35. Verderosa AD, Totsika M, Fairfull-Smith KE. Bacterial biofilm eradication agents: a current review. Front Chem. 2019;7:824.
  36. Tellez-Perez AD, Alva-Murillo N, Ochoa-Zarzosa A, Lopez-Meza JE. Cholecalciferol (vitamin D) differentially regulates antimicrobial peptide expression in bovine mammary epithelial cells: implications during Staphylococcus aureus internalization. Vet Microbiol. 2012;160(1-2):91-98. https://doi.org/10.1016/j.vetmic.2012.05.007
  37. Yue Y, Hymoller L, Jensen SK, Lauridsen C, Purup S. Effects of vitamin D and its metabolites on cell viability and Staphylococcus aureus invasion into bovine mammary epithelial cells. Vet Microbiol. 2017;203:245-251. https://doi.org/10.1016/j.vetmic.2017.03.008
  38. Merriman KE, Powell JL, Santos JE, Nelson CD. Intramammary 25-hydroxyvitamin D3 treatment modulates innate immune responses to endotoxin-induced mastitis. J Dairy Sci. 2018;101(8):7593-7607. https://doi.org/10.3168/jds.2017-14143