In Vitro Efficacy of Silver Carbene Complexes, SCC1 and SCC22, Against Some Enteric Animal Pathogens

Main Article Content

Akhil M Alsadwi
Mohamed MA Ibrahim
Kush N Shah
Carolyn L Cannon
James A Byrd
Denise Caldwell
Bob Droleskey
Christopher A Bailey

Abstract





Silver carbene complexes (SCCs), a group of novel silver-based compounds capable of gradually ‎releasing ‎silver ions, have shown significant antimicrobial activity against a wide range of ‎bacterial pathogens mainly ‎isolated from human cases. The antimicrobial activity against ‎animal isolated pathogens has yet been done. ‎The in vitro efficacy of two SCCs with different ‎carrier molecules (SCC1 with a methylated caffeine backbone ‎and SCC22 with a ‎dichloroimidazolium backbone) was investigated against three important animal and ‎human ‎pathogen species. SCC1 and SCC22 exhibited bacteriostatic and bactericidal effects against ‎multidrug ‎resistant Salmonella Typhimurium (poultry isolate), E. coli 843 and E. coli 1568 ‎‎(swine isolates), and the ‎poultry field isolates Salmonella Heidelberg, Salmonella Enteritidis, and ‎Salmonella Montevideo with MICs ‎and MBCs ranged from 16-21 µM (6-8 µg/mL) and 16-32 µM ‎‎(6-12 µg/mL), respectively. Clostridium perfringens type A was sensitive to both SCC1 and ‎SCC22 with the MICs being 11 (4 µg/mL) and 21 µM ‎‎(8 µg/mL), respectively. These values were ‎comparable to the MICs and MBCs for silver acetate. The MBCs ‎against C. perfringens was >85 µM for ‎SCCs and >192 µM for silver acetate (>32 µg/mL for all compounds). Ten hours incubation ‎of C. perfringens with ‎‎40 µg/mL of all three products showed down regulation of virulence genes plc and netB, ‎‎suggesting viable cells and silver can modulate the virulence. Treating the C. perfringens with higher ‎concentration (100 ‎‎µg/mL) of each SCC for 10 hours inhibited more bacteria compared to the ‎untreated bacterial cells, however, no ‎differences in the ultrastructure of lysed bacteria were seen ‎and this concentration might not induce viable ‎but non-culturable (VBNC) state as suggested by ‎transmission electron microscopy findings. SCCs showed a ‎broad antimicrobial activity against ‎all bacterial species tested including multidrug resistant pathogens. Both ‎SCCs demonstrated ‎inhibitory effect against the Gram-positive anaerobic C. perfringens type A ‎which ‎could have a high accumulation capacity for silver ion. These data suggest that SCCs may ‎represent a ‎novel class of broad-spectrum antimicrobial agents, which may be used to reduce the ‎burden of pathogenic ‎bacteria in the gastrointestinal tract of poultry‎‎‎.





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In Vitro Efficacy of Silver Carbene Complexes, SCC1 and SCC22, Against Some Enteric Animal Pathogens. (2024). The Iraqi Journal of Veterinary Medicine, 48(1), 1-8. https://doi.org/10.30539/yvbbhj22
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In Vitro Efficacy of Silver Carbene Complexes, SCC1 and SCC22, Against Some Enteric Animal Pathogens. (2024). The Iraqi Journal of Veterinary Medicine, 48(1), 1-8. https://doi.org/10.30539/yvbbhj22

References

Patterson JA, Burkholder KM. Application of prebiotics and probiotics in poultry production. Poult Sci. 2003;82:627-631. 1. Patterson JA, Burkholder KM. Application of prebiotics and probiotics in poultry production. Poult Sci. 2003;82:627-631. https://doi.org/10.1093/ps/82.4.627

Castanon JIR. History of the use of antibiotic as growth promoters in european poultry feeds. Poult Sci. 2007;86:2466-2471. https://doi.org/10.3382/ps.2007-00249

Niewold TA. Intestinal genomics for evaluation of alternatives for AGP, current situation and perspectives. In: Barug D, de Jong J, Jong JD, ‎Kies AK, Verstegen MWA, editors. Antimicrobial Growth Promoters : Where Do We Go from Here? Wageningen: Wageningen ‎Academic; 2006. p. 361-368.‎ https://doi.org/10.3920/9789086865703_024

Russell AD, Hugo WB. 7 Antimicrobial Activity and Action of Silver. In: Ellis GP, Luscombe DK, editors. Progress in medicinal chemistry. ‎‎31: Elsevier; 1994. p. 351-370. https://doi.org/10.1016/S0079-6468(08)70024-9

Klasen HJ. Historical review of the use of silver in the treatment of burns. I. Early uses. Burns. 2000;26:117-130. https://doi.org/10.1016/S0305-4179(99)00108-4

Napoli M, Saturnino C, Cianciulli EI, Varcamonti M, Zanfardino A, Tommonaro G, et al. Silver(I) N-heterocyclic carbene complexes: ‎Synthesis, characterization and antibacterial activity. Organomet Chem. 2013;725:46-53. https://doi.org/10.1016/j.jorganchem.2012.10.040

Gibbs RJ. Silver Colloids: Do They Work? 1999.‎

Fox CL Jr. Silver sulfadiazine--a new topical therapy for Pseudomonas in burns. Therapy of Pseudomonas infection in burns. Arch Surg. ‎‎1968;96:184-188. 10.1001/archsurg.1968.01330200022004

Johnson NA, Southerland MR, Youngs WJ. Recent developments in the medicinal applications of silver-NHC complexes and imidazolium salts. Molecules. 2017;22:1263. https://doi.org/10.1001/archsurg.1968.01330200022004

Melaiye A, Simons RS, Milsted A, Pingitore F, Wesdemiotis C, Tessier CA, et al. Formation of water-soluble pincer silver(I)-carbene ‎complexes: a novel antimicrobial agent. J Med Chem. 2004;47:973-977. https://doi.org/10.1021/jm030262m

Kascatan-Nebioglu A, Melaiye A, Hindi K, Durmus S, Panzner MJ, Hogue LA, et al. Synthesis from caffeine of a mixed N-heterocyclic ‎carbene-silver acetate complex active against resistant respiratory pathogens. J Med Chem. 2006;49:6811-6818. https://doi.org/10.1021/jm060711t

Leid JG, Ditto AJ, Knapp A, Shah PN, Wright BD, Blust R, et al. In vitro antimicrobial studies of silver carbene complexes: activity of free ‎and nanoparticle carbene formulations against clinical isolates of pathogenic bacteria. J Antimicrob Chemother. 2012;67:138-148. https://doi.org/10.1093/jac/dkr408

Patil S, Deally A, Gleeson B, Muller-Bunz H, Paradisi F, Tacke M. Novel benzyl-substituted N-heterocyclic carbene-silver acetate ‎complexes: synthesis, cytotoxicity and antibacterial studies. Metallomics. 2011;3:74-88. https://doi.org/10.1039/C0MT00034E

Hindi KM, Siciliano TJ, Durmus S, Panzner MJ, Medvetz DA, Reddy DV, et al. Synthesis, stability, and antimicrobial studies of ‎electronically tuned silver acetate N-heterocyclic carbenes. J Med Chem. 2008;51:1577-1583.https://doi.org/10.1021/jm0708679

Hindi KM, Panzner MJ, Tessier CA, Cannon CL, Youngs WJ. The medicinal applications of imidazolium carbene-metal complexes. Chem ‎Rev. 2009;109(8):3859-3884. https://doi.org/10.1021/cr800500u

Panzner MJ, Deeraksa A, Smith A, Wright BD, Hindi KM, Kascatan-Nebioglu A, et al. Synthesis and in vitro efficacy studies of silver carbene complexes on biosafety level 3 bacteria. Eur J Inorg Chem. 2009;13:1739-1745. https://doi.org/10.1002/ejic.200801159

Panzner MJ, Hindi KM, Wright BD, Taylor JB, Han DS, Youngs WJ, et al. A theobromine derived silver N-heterocyclic carbene: synthesis, ‎characterization, and antimicrobial efficacy studies on cystic fibrosis relevant pathogens. Dalton Trans. 2009;35:7308-7313. https://doi.org/10.1039/b907726j

Cannon CL, Hogue LA, Vajravelu RK, Capps GH, Ibricevic A, Hindi KM, et al. In vitro and murine efficacy and toxicity studies of nebulized ‎SCC1, a methylated caffeine-silver(I) complex, for treatment of pulmonary infections. Antimicrob Agents Chemother. 2009;53(8):3285-‎‎32w/93. https://doi.org/10.1128/AAC.00314-09

McReynolds JL, Byrd JA, Anderson RC, Moore RW, Edrington TS, Genovese KJ, et al. Evaluation of immunosuppressants and dietary mechanisms in an experimental disease model for necrotic enteritis. Poult Sci. 2004;83(12):1948-1952. https://doi.org/10.1093/ps/83.12.1948

Swaggerty CL, McReynolds JL, Byrd JA, Pevzner IY, Duke SE, Genovese KJ, et al. Selection for pro-inflammatory mediators produces chickens more resistant to Clostridium perfringens-induced necrotic enteritis. Poult Sci. 2016;95(2):370-374. https://doi.org/10.3382/ps/pev348

Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, et al. Primer3--new capabilities and interfaces. Nucleic Acids Res. 2012;40(15):e115. https://doi.org/10.1093/nar/gks596

Mollenhauer HH. Plastic embedding mixtures for use in electron microscopy. Stain Technol. 1964;39:111-114.‎

Clement JL, Jarrett PS. Antibacterial silver. Met Based Drugs. 1994;1(5-6):467-82. https://doi.org/10.1155/MBD.1994.467

Sütterlin S, Tano E, Bergsten A, Tallberg AB, Melhus A. Effects of silver-based wound dressings on the bacterial flora in chronic leg ulcers ‎and its susceptibility in vitro to silver. Acta Derm Venereol. 2012;92(1):34-39. https://doi.org/10.2340/00015555-1170

Messner KR, Imlay JA. The identification of primary sites of superoxide and hydrogen peroxide formation in the aerobic respiratory chain ‎and sulfite reductase complex of Escherichia coli. J Biol Chem. 1999;274(15):10119-10128. https://doi.org/10.1074/jbc.274.15.10119

Lansdown AB. Silver. I: Its antibacterial properties and mechanism of action. J Wound Care. 2002;11(4):125-130. https://doi.org/10.12968/jowc.2002.11.4.26389

Hasan SM, Hall JB. The physiological function of nitrate reduction in Clostridium perfringens. J Gen Microbiol. 1975;87(1):120-128. https://doi.org/10.1099/00221287-87-1-120

Shimizu T, Ohtani K, Hirakawa H, Ohshima K, Yamashita A, Shiba T, et al. Complete genome sequence of Clostridium perfringens, an ‎anaerobic flesh-eater. Proc Natl Acad Sci U S A. 2002;99(2):996-1001. https://doi.org/10.1073/pnas.022493799

Pesakhov S, Benisty R, Sikron N, Cohen Z, Gomelsky P, Khozin-Goldberg I, et al. Effect of hydrogen peroxide production and the Fenton ‎reaction on membrane composition of Streptococcus pneumoniae. Biochim Biophys Acta. 2007;1768(3):590-597. https://doi.org/10.1016/j.bbamem.2006.12.016

Park HJ, Kim JY, Kim J, Lee JH, Hahn JS, Gu MB, et al. Silver-ion-mediated reactive oxygen species generation affecting bactericidal activity. ‎Water Res. 2009;43(4):1027-1032. https://doi.org/10.1016/j.watres.2008.12.002

Matsumura Y, Yoshikata K, Kunisaki S-i, Tsuchido T. Mode of bactericidal action of silver zeolite and its comparison with that of silver ‎nitrate. Appl Environ Microbiol. 2003;69(7):4278-4281. https://doi.org/10.1128/AEM.69.7.4278-4281.2003

Chen Z, Yang P, Yuan Z, Guo J. Aerobic condition enhances bacteriostatic effects of silver nanoparticles in aquatic environment: an ‎antimicrobial study on Pseudomonas aeruginosa. Sci Rep. 2017;7(1):7398. https://doi.org/10.1038/s41598-017-07989-w

Oliver JD. Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol Rev. 2010;34(4):415-425. https://doi.org/10.1111/j.1574-6976.2009.00200.x

Quirós C, Herrero M, García LA, Díaz M. Quantitative Approach to Determining the Contribution of Viable-but-Nonculturable ‎Subpopulations to Malolactic Fermentation Processes. Appl Environ Microbiol. 2009;75:2977. https://doi.org/10.1128/AEM.01707-08

Alifano P, Bruni CB, Carlomagno MS. Control of mRNA processing and decay in prokaryotes. Genetica. 1994;94(2-3):157-172. https://doi.org/10.1007/BF01443430

Sheridan GE, Masters CI, Shallcross JA, MacKey BM. Detection of mRNA by reverse transcription-PCR as an indicator of viability in ‎Escherichia coli cells. Appl Environ Microbiol. 1998;64(4):1313-1318. https://doi.org/10.1128/AEM.64.4.1313-1318.1998

Selby CP, Sancar A. Mechanisms of caffeine inhibition of DNA repair in E. coli. Prog Clin Biol Res. 1990;340A:179-193.‎

Osman F, McCready S. Differential effects of caffeine on DNA damage and replication cell cycle checkpoints in the fission yeast ‎Schizosaccharomyces pombe. Mol Gen Genet. 1998;260(4):319-334. https://doi.org/10.1007/s004380050901

Diekert G, Ritter M. Purification of the nickel protein carbon monoxide dehydrogenase of Clostridium thermoaceticum. FEBS Lett. ‎‎1983;151:41-44. https://doi.org/10.1016/0014-5793(83)80338-X

Percival SL, Bowler PG, Russell D. Bacterial resistance to silver in wound care. J Hosp Infect. 2005;60:1-7. https://doi.org/10.1016/j.jhin.2004.11.014

Jung WK, Koo HC, Kim KW, Shin S, Kim SH, Park YH. Antibacterial activity and mechanism of action of the silver ion in Staphylococcus aureus ‎and Escherichia coli. Appl Environ Microbiol. 2008;74(7):2171-2178. https://doi.org/10.1128/AEM.02001-07

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