Morphological Changes Associated with the Antibacterial Action of Silver Ions against Bovine Mastitis Pathogens

은 이온의 항균효과에 대한 소 유방염 원인균의 형태학적 변화

  • Kang, Seog-Jin (National Institute of Animal Science, Rural Development Administration) ;
  • Seol, Jae-Won (Center for Healthcare Technology Development, Bio-Safety Research Institute, College of Veterinary Medicine, Chonbuk National University) ;
  • Hur, Tai-Young (National Institute of Animal Science, Rural Development Administration) ;
  • Jung, Young-Hun (National Institute of Animal Science, Rural Development Administration) ;
  • Choe, Chang-Yong (National Institute of Animal Science, Rural Development Administration) ;
  • Park, Sang-Youel (Center for Healthcare Technology Development, Bio-Safety Research Institute, College of Veterinary Medicine, Chonbuk National University)
  • 강석진 (농촌진흥청 국립축산과학원) ;
  • 설재원 (헬스케어 기술개발 사업단, 전북대학교 수의과대학 생체안전성 연구소) ;
  • 허태영 (농촌진흥청 국립축산과학원) ;
  • 정영훈 (농촌진흥청 국립축산과학원) ;
  • 최창용 (농촌진흥청 국립축산과학원) ;
  • 박상열 (헬스케어 기술개발 사업단, 전북대학교 수의과대학 생체안전성 연구소)
  • Accepted : 2011.12.15
  • Published : 2011.12.31

Abstract

Silver has potent antibacterial activity against a variety of bacteria while maintaining low toxicity in mammalian cells. This study was conducted to investigate the possible mechanism underlying the bactericidal effects of silver ions against bovine mastitis pathogens using electron microscopy. We used two different bacterial strains, Escherichia coli and Staphylococcus aureus, which are primarily responsible for the majority of bovine mastitis cases. Interaction between the bacteria and silver ions (50 ${\mu}g/mL$, 2 hours) were studied using energy-filtering transmission electron microscopy (EFTEM). EFTEM images showed that E. coli and S. aureus cells treated with the silver ions had distorted plasma membranes, silver ions attached to the outer membranes, scattered electron-light material, and leakage of cell contents from disrupted cell membranes.

은 이온(silver ion)은 동물세포에 낮은 독성을 가지면서도 다양한 종류의 세균들에 대해 강력한 항균력을 가지고 있다. 본 연구에서는 젖소 유방염 원인균들에 대한 은 이온의 항균효과를 전자현미경(TEM)을 통해 조사하였다. 본 실험에 사용된 균주는, 젖소 유방염의 주요 원인균인 Escherichia coli 와 Staphylococcus aureus를 사용하였다. 유방염 원인균에 대한 은 이온의 항균효과를 관찰하기 위해 50 ${\mu}g/mL$의 은 이온을 2시간 동안 세균에 노출시킨 후 전자현미경(Energy-Filtering Transmission Electron Microscopy, EFTEM) 을 이용하여 은 이온에 의한 세균의 형태 변화를 확인하였다. 은 이온 처리 후 전자현미경 촬영 결과 E. coli 와 S. aureus의 세포막이 변형되고, 세포 외부에 침착된 은 이온과, electron-light 모습으로 세포내 분산된 은 이온을 관찰 할 수 있었으며, 결과적으로 E. coli 와 S. aureus의 세포막이 파괴되어, 세포내용물이 외부에 누출됨으로써 세균이 사멸되는 것을 확인하였다.

Keywords

References

  1. Bechert T, Steinrucke P, Guggenbichler JP. A new method for screening anti-infective biomaterials. Nature Med 2000; 6: 1053-1056. https://doi.org/10.1038/79568
  2. Bennett RM, Christiansen K, Clifton-Hadley RS. Estimating the costs associated with endemic diseases of dairy cattle. J Dairy Res 1999; 66: 455-459. https://doi.org/10.1017/S0022029999003684
  3. Berger TJ, Spadaro JA, Bierman R, Chapin SE, Becker RO. Antifungal properties of electrically generated metallic ions. Antimicrob Agents Chemother 1976; 10: 856-860. https://doi.org/10.1128/AAC.10.5.856
  4. Berger TJ, Spadaro JA, Chapin SE, Becker RO. Electrically generated silver ions: quantitative effects on bacterial and mammalian cells. Antimicrob Agents Chemother 1976; 357-358.
  5. Bramley AJ, Foster R. Effects of lysostaphin on staphylococcus aureus infections of the mouse mammary gland. Res Vet Sci 1990; 49: 120-121.
  6. Coward JE, Carr HS, Rosenkranz HS. Silver sulfadiazine: effect on the ultrastructure of Pseudomonas aeruginosa. Antimicrob Agents Chemother 1973; 3: 621-624. https://doi.org/10.1128/AAC.3.5.621
  7. Dibrov P, Dzioba J, Gosink KK, Hase CC. Chemiosmotic mechanism of antimicrobial activity of Ag(+) in Vibrio cholerae. Antimicrob Agents Chemother 2002; 46: 2668-2670. https://doi.org/10.1128/AAC.46.8.2668-2670.2002
  8. Feng QL, Wu J, Chen GQ, Cui FZ, Kim TN, Kim JO. A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus. J Biomed Mater Res 2000; 52: 662-668. https://doi.org/10.1002/1097-4636(20001215)52:4<662::AID-JBM10>3.0.CO;2-3
  9. Fox CL. Silver sulphadiazine: a new topical therapy for Pseudomonas aeruginosa in burns. Arch Surg 1968; 96: 184-188. https://doi.org/10.1001/archsurg.1968.01330200022004
  10. Furr JR, Russell AD, Turner TD, Andrews A. Antimicrobial activity of Actisorb Plus, Actisorb and silver nitrate. J Hosp Infect 1994; 27: 201-208. https://doi.org/10.1016/0195-6701(94)90128-7
  11. Holt KB, Bard AJ. Interaction of silver(I) ions with the respiratory chain of Escherichia coli: an electrochemical and scanning electrochemical microscopy study of the antimicrobial mechanism of micromolar Ag+. Biochemistry 2005; 44: 13214-13223. https://doi.org/10.1021/bi0508542
  12. Hotta M, Nakajima H, Yamamoto K, Aono M. Antibacterial temporary filling materials: the effect of adding various ratios of Ag-Zn-zeolite. J Oral Rehabil 1998; 25: 485-489. https://doi.org/10.1046/j.1365-2842.1998.00265.x
  13. Hu S, Concha C, Johannisson A, Meglia G, Waller KP. Effect of subcutaneous injection of ginseng on cows with subclinical Staphylococcus aureus mastitis. J Vet Med B Infect Dis Vet Public Health 2001; 48: 519-528. https://doi.org/10.1046/j.1439-0450.2001.00470.x
  14. Kai K, Komine K, Asai K, Kuroishi T et al. Antiinflammatory effects of intramammary infusions of glycyrrhizin in lactating cows with mastitis caused by coagulase-negative staphylococci. Am J Vet Res 2003; 64: 1213-1220. https://doi.org/10.2460/ajvr.2003.64.1213
  15. Kawai K, Nagahata H, Lee NY, Anri A, Shimazaki K. Effect of infusing lactoferrin hydrolysate into bovine mammary glands with subclinical mastitis. Vet Res Commun 2003; 27: 539-548 https://doi.org/10.1023/A:1026039522286
  16. Klabunde KJ, Koper OB, Klabunde JS et al. Nanoscale powders and formulations with biocidal activity toward spores and vegetative cells of bacillus species, viruses, and toxins. Curr Microbiol 2002; 44: 49-55. https://doi.org/10.1007/s00284-001-0073-x
  17. Kumar R, Munstedt H. Silver ion release from antimicrobial polyamide/silver composites. Biomaterials 2005; 26: 2081-2088. https://doi.org/10.1016/j.biomaterials.2004.05.030
  18. Lansdown AB. Silver. I: its antibacterial properties and mechanism of action. J Wound Care 2002; 11: 125-130. https://doi.org/10.12968/jowc.2002.11.4.26389
  19. Liau SY, Read DC, Pugh WJ, Furr JR, Russell AD. Interaction of silver nitrate with readily identifiable groups: relationship to the antibacterial action of silver ions. Lett Appl Microbiol 1997; 25: 279-283. https://doi.org/10.1046/j.1472-765X.1997.00219.x
  20. Lok CN, Ho CM, Chen R et al. Proteomic analysis of the mode of antibacterial action of silver nanoparticles. J Proteome Res 2006; 5: 916-924. https://doi.org/10.1021/pr0504079
  21. Mermel LA, Stolz SM, Maki DG. Surface antimicrobial activity of heparin-bonded and antiseptic-impregnated vascular catheters. J Infect Dis 1993; 167: 920-924. https://doi.org/10.1093/infdis/167.4.920
  22. Modak SM, Fox CL. Binding of silver sulfadiazine to the cellular components of Pseudomonas aeruginosa. Biochem Pharm 1973; 22: 2391-2404. https://doi.org/10.1016/0006-2952(73)90341-9
  23. Nover L, Scharf KD, Neumann D. Formation of cytoplasmic heat shock granules in tomato cell cultures and leaves. Mol Cell Biol 1983; 3: 1648-1655. https://doi.org/10.1128/MCB.3.9.1648
  24. Ovington LG Battling bacteria in wound care. Home Health Nurse 2001; 19: 622-630. https://doi.org/10.1097/00004045-200110000-00013
  25. Russell AD, Hugo WB. Antimicrobial activity and action of silver. Prog Med Chem 1994; 31: 351-370.
  26. Seol JW, Kang SJ, Park SY. Silver ion treatment of primary cultured bovine mammary gland epithelial cell (BMEC) damage from Staphylococcus aureus-derived $\alpha$-toxin. Vet Res Commun 2010; 34: 33-42.
  27. Seol JW, Hur TY, Jung YH, Kang SJ, Park SY. Application of Silver Ion for Clinical Mastitis in Holstein Cows. J Vet Clin 2010; 27: 246-251.
  28. Seol JW, Hur TY, Jung YH, Kang SJ, Park SY. Evaluation of Bactericidal Capacity of Silver Ion against Bovine Mastitis Pathogens. J Vet Clin 2010; 27:252-256.
  29. Shin HS, Yang HJ, Kim SB, Lee MS. Mechanism of growth of colloidal silver nanoparticles stabilized by polyvinyl pyrrolidone in $\gamma$-irradiated silver nitrate solution. J Collo Interf Sci 2004; 274: 89-94 https://doi.org/10.1016/j.jcis.2004.02.084
  30. Slawson RM, Lee H, Trevors JT. Bacterial interactions with silver. Biol Metals 1990; 3: 151-154. https://doi.org/10.1007/BF01140573
  31. Wadu-Mesthrige K, Amro NA, Liu GY. Immobilization of proteins on self-assembled monolayers. Scanning 2000; 22: 380-388.
  32. Watts DH, Eschenbach DA. Treatment of Chlamydia, Mycoplasma, and group B streptococcal infections. Clin Obstet Gynecol 1988; 31: 435-452. https://doi.org/10.1097/00003081-198806000-00018
  33. Wright JB, Lam K, Hansen D, Burrell RE. Efficacy of topical silver against fungal burn wound pathogens. Am J Infect Cont. 1999; 27: 344-350. https://doi.org/10.1016/S0196-6553(99)70055-6
  34. Zhanel GG, Karlowsky JA, Davidson RJ, Hoban DJ. Effect of pooled human cerebrospinal fluid on the postantibiotic effects of cefotaxime, ciprofloxacin, and gentamicin against Escherichia coli. Antimicrob Agents Chemother 1992; 36: 1136-1139. https://doi.org/10.1128/AAC.36.5.1136