:: Volume 5, Issue 2 (Apr-Jun 2018) ::
Nutr Food Sci Res 2018, 5(2): 29-38 Back to browse issues page
Antagonistic Effects of Lactobacilli spp. against Ciprofloxacin-Resistant Uropathogenic Escherichia coli Strains
Mahsa Yeganeh , Hedayat Hosseini , Sedigheh Mehrabian , Elham Siasi Torbati , Seyed Morteza Zamir
Faculty of Biological Sciences, Tehran-North Branch, Islamic Azad University, Tehran, Iran
Abstract:   (499 Views)
Background and Objectives: Recently, the use of probiotics for the treatment of Urinary Tract Infections has become more popular. The use of probiotics in therapy is useful as only a few side effects such as destruction of resistant bacteria or disturbance of the intestinal microbiota have been reported. The aim of this study was to evaluate the probiotic effects of lactic acid bacteria by co-aggregation of ciprofloxacin-resistant uropathogenic Escherichia coli strains using microbial techniques.
Materials and Methods: Three strains of Lactobacillus plantarum, Lactobacillus casei and Lactobacillus acidophilus were provided. Twenty isolates of uropathogenic Escherichia coli were collected from Shahid Labbafinejad hospital, Tehran. Eight samples with resistance to ciprofloxacin were selected using the disk diffusion method for the co-aggregation test. PCR was used to evaluate the presence of qnrA and qnrS genes in ciprofloxacin-resistant isolates. To evaluate the antimicrobial activity of complete culture and supernatants of lactobacilli, modified double-layer culture method and well diffusion methods were used, respectively. Co-aggregation of lactobacilli was evaluated by the co-aggregation test and microscopy test.
Results: Results showed that the eight human isolates were resistant to ciprofloxacin among other samples. Only one strain had both qnrA and qnrS genes simultaneously. L. plantarum with the average growth inhibition zone of 42 mm and with 65% of the co-aggregation had the best probiotic effects among all lactobacilli bacteria.
Conclusions: The probiotic lactobacilli had spectacular antimicrobial effects against the ciprofloxacin-resistant uropathogenic Escherichia coli strains. Also, lactobacillus spp. were aggregated with uropathogenic Escherichia coli strains and preventing from their adhesion to specific receptors on the Urethra, thus, the subsequent invasion to the host was prevented.
Keywords: Antimicrobial, Co-aggregation, Lactobacillus acidophilus, Lactobacillus casei, Lactobacillus plantarum
Full-Text [PDF 280 kb]   (176 Downloads)    
Type of Study: Research | Subject: Special
Received: 2017/08/29 | Accepted: 2018/03/10 | Published: 2018/03/10
References
1. Price SB, Wright JC, DeGraves FJ, Castanie-Cornet MP, Foster JW. Acid resistance systems required for survival of Escherichia coli H7:O157 in the bovine gastrointestinal tract and in apple cider are different. Appl Environ Microbiol. 2004; 70: 4792–4799. DOI: 10.1128/AEM.70.8.4792-4799.2004 [DOI:10.1128/AEM.70.8.4792-4799.2004]
2. Wiles TJ, Kulesus RR, Mulvey MA. Origins and Virulence Mechanisms of Uropathogenic Escherichia coli. Exp Mol Pathol. 2008; 85(1): 11–19. DOI: 10.1016/j.yexmp.2008.03.007 [DOI:10.1016/j.yexmp.2008.03.007]
3. Kanjee U, Houry WA. Mechanisms of acid resistance in Escherichia coli. Annu Rev Microbiol. 2013; 67: 65– 81. DOI: 10.1146/annurev-micro-092412-155708. [DOI:10.1146/annurev-micro-092412-155708]
4. Azap Ö, Togan T, Yesilkaya A, Arslan H, Haberal M. Antimicrobial susceptibilities of uropathogen Escherichia coli in renal transplant recipients: dramatic increase in ciprofloxacin resistance. Transplant Proc. 2013; 45: 956-7. DOI: 10.1016/j.transproceed.2013.03.006 [DOI:10.1016/j.transproceed.2013.03.006]
5. Pakzad I, Ghafourian S, Taherikalani M, sadeghifard N, Abtahi H, Rahbar M, Mansory Jamshidi N. Qnr prevalence in extended spectrum beta-lactamases (ESBLs) and none-ESBLs producing Escherichia coli isolated from urinary tract infections in central of Iran. Iran J Basic Med Sci . 2011; 14:458-64.
6. Bonkat G, Muller G, Braissant O, Frei R, Tschudin-Suter S, Rieken M, Wyler S, Gasser TC, Bachmann A, Widmer AF. Increasing prevalence of ciprofloxacin resistance in extended-spectrum-beta-lactamase-producing Escherichia coli urinary isolates. World J Urol. 2013; 31:1427-32. DOI: 10.1007/s00345-013-1031-5. [DOI:10.1007/s00345-013-1031-5]
7. Bansal S, Tandon V. Contribution of mutations in DNA gyrase and topoisomerase IV genes to ciprofloxacin resistance in Escherichia coli clinical isolates. Int J Antimicrob Agent. 2011; 37:253-5. DOI: 10.1016/j.ijantimicag.2010.11.022. [DOI:10.1016/j.ijantimicag.2010.11.022]
8. Shin JH, Jung HJ, Lee JY, Kim HR, Lee JN, Chang CL. High rates of plasmid-mediated quinolone resistance QnrB variants among ciprofloxacin-resistant Escherichia coli and Klebsiella pneumoniae from urinary tract infections in Korea. Microb Drug Resist. 2008; 14:221-6. DOI: 10.1089/mdr.2008.0834. [DOI:10.1089/mdr.2008.0834]
9. Montasir M, Jayedul H, Nazmul Hussain N, Alimul I, Khalada Z, Bahanur R, Tanvir R. Prevalence and Molecular Detection of Quinolone-Resistant E.coli in Rectal Swab of Apparently Healthy Cattle in Bangladesh. Int J Trop Dis Health. 2017; 24(2): 1-7. DOI: 10.9734/IJTDH/2017/34404 [DOI:10.9734/IJTDH/2017/34404]
10. Yoon Sung H, Sook S, Yong Ho P, Kun Taek P. Prevalence and Mechanism of Fluoroquinolone Resistance in Escherichia coli isolated from swine Feces in Korea. Int J Food Prot. 2017; 7: 1145–1151. DOI:10.4315/0362-028X.JFP-16-502 [DOI:10.4315/0362-028X.JFP-16-502]
11. Cremet L, Caroff N, Dauvergne S, Reynaud A, Lepelletier D, Corvec S. Prevalence of plasmid-mediated quinolone resistance determinants in ESBL Enterobacteriaceae clinical isolates over a 1-year period in a French hospital. Pathologie Biologie. 2011; 59:151-6. DOI: 10.1016/j.patbio.2009.04.003 [DOI:10.1016/j.patbio.2009.04.003]
12. Corkill JE, Anson JJ, Hart CA. High prevalence of the plasmid-mediated quinolone resistance determinant qnrA in multidrug- resistant Enterobacteriaceae from blood cultures in Liverpool, UK. J Antimicrob Chemotherap. 2005; 56:1115-7. [DOI:10.1093/jac/dki388]
13. Aasen IM, Møretrø T, Katla T, Axelsson L, Storrø I. Influence of complex nutrients, temperature and pH on bacteriocin production by Lactobacillus sakei CCUG 42687. Appl Microbiol Biotechnol. 2000; 53: 159-166. [DOI:10.1007/s002530050003]
14. Suskovic J, Kos B, Goreta J, Matošić S. Role of Lactic Acid Bacteria and bifidobacteria in synbiotic effect. Food Technol Biotechnol. 2001; 39: 227-235
15. Djomne VS, Ngoufack FZ, Pierre MK, Alberto C, Florence F. Probiotic properties of lactobacilli strains isolated from raw cow milk in the western highlands of Cameroon. Innovative Rom Food Biotechnol. 2011; 9: 12-28.
16. Coeuret V, Dubernet S, Bernardeau M, Gueguen M, Vernoux J. Isolation, characterisation and identification of lactobacilli focusing mainly on cheeses and other dairy products. Lait. 2003; 83: 269–306. DOI: 10.1051/lait:2003019 [DOI:10.1051/lait:2003019]
17. Oyetayo VO, Adetuyi FC, Akinyosoye FA. Safety and protective effect of Lactobacillus acidophilus and Lactobacillus casei used as probiotic agent in vivo. Afr J Biotech. 2003; 2: 448-452. [DOI:10.5897/AJB2003.000-1090]
18. Abdelbasset M, Djamila K. Antimicrobial activity of autochthonous lactic acid bacteria isolated from Algerian traditional fermented milk Raïb. Afr J Biotechnol. 2003; 7: 2908-2914.
19. O'Horo JC, Jindai K, Kunzer B, Safdar N. Treatment of recurrent Clostridium difficile infection:a systematic review. Infect. 2014; 42(1): 43-59. [DOI:10.1007/s15010-013-0496-x]
20. Maragkoudakis PA, Zoumpopoulou G, Miaris C, Kalantzopoulos G, Pot B, Tsakalidou E. Probiotic potential of Lactobacillus strains isolated from dairy products. Int Dairy J. 2006; 16: 189-199. [DOI:10.1016/j.idairyj.2005.02.009]
21. Kos B, Susković J, Vuković S, Simpraga M, Frece J, Matosić S. Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J Appl Microbiol. 2003; 94: 981-987. DOI: 10.1046/j.1365-2672.2003.01915.x [DOI:10.1046/j.1365-2672.2003.01915.x]
22. Garcia-Cayuela T, Korany AM, Bustos I, Gomez de Cadinanos LP, Requena T, Pelaez C, Carmen Martinez-Cuesta M. Adhesion abilities of dairy Lactobacillus plantarum strains showing an aggregation phenotype. Food Res Int. 2014; 57: 44-50. [DOI:10.1016/j.foodres.2014.01.010]
23. Saira B, Yasra S, Aamir A, Mashkoor M, Muhammad Azeem S, Ayesha T, and Abdul H. multiple drug resistance patterns in various phylogenetic groups of Uropathogenic E. coli isolated from faisalabad region of Pakistan. Braz J Microbiol. 2011 Oct; 42(4):1278-83. [DOI:10.1590/S1517-83822011000400005]
24. Bukh AS, Schonheyder HC, Emmersen JM, Sogaard M,Bastholm S, Roslev P. Escherichia coli phylogenetic groups are associated with site of infection and level of antibiotic resistance in community-acquired bacteraemia: a 10 year population-based study in Denmark. J Antimicrob Chemother. 2009 Jul;64(1):163-8. [DOI:10.1093/jac/dkp156]
25. Bonkat G, Müller G, Braissant O, Frei R, Tschudin-Suter S, Rieken M, Wyler S, Gasser TC, Bachmann A, Widmer AF. Increasing prevalence of ciprofloxacin resistance in extended-spectrum-beta-lactamase-producing Escherichia coli urinary isolates. World J Urol. 2013;31:1427-32. DOI: 10.1007/s00345-013-1031-5. [DOI:10.1007/s00345-013-1031-5]
26. Corkill JE, Anson JJ, Hart CA. High prevalence of the plasmid-mediated quinolone resistance determinant qnrA in multidrug- resistant Enterobacteriaceae from blood cultures in Liverpool, UK. J Antimicrob Chemotherap. 2005;56:1115-7. [DOI:10.1093/jac/dki388]
27. Putnam SD, Sanders JW, Tribble DR, Rockabrand DR, Riddle MS, Rozmajzl PJ, Frenck RW. Posttreatment changes in Escherichia coli antimicrobial susceptibility rates among diarrheic patients treated with ciprofloxacin. Antimicrob Agent Chemotherap. 2005; 49:2571-2. [DOI:10.1128/AAC.49.6.2571-2572.2005]
28. Soleimani NA, Kermanshahi RK, Yakhchali B, Sattari TN. Antagonistic activity of probiotic lactobacilli against Staphylococcus aureus isolated from bovine mastitis. Afr J Microbiol Res. 2010; 4 (20): 2169- 2173.
29. Asahara T, Nomoto K, Watanuki M, Yokokura T. Antimicrobial activity of intraurethrally administered probiotic Lactobacillus casei in a murine model of Escherichia coli urinary tract infection. Antimicrob. Agents Chemother. 2001; 45 (6):1751- 60. [DOI:10.1128/AAC.45.6.1751-1760.2001]
30. Handley SP et al. A comparison of the adhesion, coaggregation and cellsurface hydrophobicity properties of fibrillar and fimbriate strains of Streptococcus salivarius. J Gen Microbiol. 1987; 133: 3207-3217.
31. Collado M C, Meriluoto J, and Salminen S. Adhesion and aggregation properties of probiotic and pathogen strains. Eur Food Res Technol. 2008; 22(6):1065-73. Doi:10.1007/s00217-007-0632-x [DOI:10.1007/s00217-007-0632-x]
32. Vlkova E, Rada V, Šmehilova M, Killer J. Auto-Aggregation and Co-Aggregation Ability in Bifidobacteria and Clostridia. Folia Microbiol. 2008; 53(3): 263–269 . [DOI:10.1007/s12223-008-0040-z]
33. Kolenbrander PE. Co-aggregation of human oral bacteria: potential role in the accretion of dental plaque. J. Appl. Bacteriol. 1993;74:79S–86S. [DOI:10.1111/j.1365-2672.1993.tb04344.x]
34. Akbari-Nakhjavani F, Mirsalehi A, Hamidian M, Kazemi B, Mirafshar M, Jabal Ameli F, et al. Antimicrobial susceptibility testing of Escherichia coli strains isolated from urinary tract infections to fluoroquinolones and detection of gyrA mutations in resistant strains. Daru. 2007; 15(2): 94-9.
35. Muhammad I, Uzma M, Yasmin B, Mehmood Q, Habib B. Prevalence of antimicrobial resistance and integrons in Escherichia coli from Punjab, Pakistan. Braz J Microbiol. 2011; 42(3): 462-6. [DOI:10.1590/S1517-83822011000200008]
36. Moreno E, Prats G, Sabate M, Perez T, Johnson JR, Andreu A. Quinolone, fluoroquinolone and trimethoprim/sulfamethoxazole resistance in relation to virulence determinants and phylogenetic background among uropathogenic Escherichia coli. Antimicrob Agents Chemother. 2006; 57(2): 204-11. [DOI:10.1093/jac/dki468]
37. Robicsek A, Jacoby GA, Hooper DC. The worldwide, emergence of plasmid mediated quinolone resistance. Lancet Infect Dis. 2006; 6(1):629-40. [DOI:10.1016/S1473-3099(06)70599-0]
38. Wang H, Dzink-Fox JL, Chen M, Levy SB. Genetic characterization of highly flouroquinolone resistant clinical Escherchia coli strains from china: rule of acrR mutations. Antimicrob Agents Chemother. 2001; 45(5):1515-21. [DOI:10.1128/AAC.45.5.1515-1521.2001]
39. Bouchakour M, Zerouali KH, Claude JD, Amarouch H, Mdaghri NE, Courvalian P, et al. Plasmid-mediated quinolone resistance in expanded spectrum beta-lactamase producing entrobacteriaceae in Morocco. J Infect Dev Contr. 2010; 12(4): 799-803.
40. Corkill JE, Anson JJ, Hart CA. High prevalence of the plasmid-mediated quinolone resistance determinant qnrA in multidrug-resistant Enterobacteriaceae from blood cultures in Liverpool, UK. J Antimicrob Chemother. 2005;56(3): 1115–17. [DOI:10.1093/jac/dki388]
41. Maia OB, Duarte R, Silva AM, Cara DC, Nicoli JR. Evaluation of the components of a commercial probiotic in gnotobiotic mice experimentally challenged with Salmonella enterica subsp. enterica ser. Typhimurium. Vet microb. 2001; 20;79(2):183-9.
42. Soleimani NA, Kermanshahi RK, Yakhchali B, Sattari TN. Antagonistic activity of probiotic lactobacilli against Staphylococcus aureus isolated from bovine mastitis. Afr J Microbiol Res. 2010; 4 (20): 2169- 73.
43. Anas M, Eddine HJ, Mebrouk K. Antimicrobial activity of Lactobacillus species isolated from Algerian raw goat's milk against Staphylococcus aureus. World J Dairy Food Sci. 2008;3(2):39-49.
44. Ogunbanwo ST, Sanni AL, Onilude AA. Characterization of bacteriocin produced by Lactobacillus plantarum F1 and Lactobacillus brevis OG1. Afr J Biotechnol. 2003; 2(8): 219-27 [DOI:10.5897/AJB2003.000-1045]
45. Hawaz E. Isolation and identification of lactic acid bacteria from curd and in vitro evaluation of its growth inhibition activities against pathogenic bacteria. Afr J Microbiol Res. 2014; 8:1419–1425. [DOI:10.5897/AJMR2014.6639]
46. Jose NM, Bunt CR, Hussain MA. Comparison of microbiological and probiotic characteristics of lactobacilli isolates from dairy food products and animal rumen contents. Microorganisms. 2015; 3:198–212. [DOI:10.3390/microorganisms3020198]
47. Rao KP, Chennappa G, Suraj U, Nagaraja H, Raj CAP, Sreenivasa MY. Probiotic potential of Lactobacillus strains isolated from sorghum-based traditional fermented food. Probiotics Antimicrob Proteins. 2015; 7(2):146–156. [DOI:10.1007/s12602-015-9186-6]
48. Jankovic I, Ventura M, Meylan V, Rouvet M, Elli M, Zink R. Contribution of aggregation-promoting factor to maintenance of cell shapein Lactobacillus gasseri 4B2. J Bacteriol. 2003; 185:3288–96. [DOI:10.1128/JB.185.11.3288-3296.2003]
49. Schachtsiek M, Hammes WP., Hertel C. Characterization of Lactobacillus coryniformis DSM 20001T surface protein Cpf mediating coaggregation with and aggregation among pathogens. Appl. Environ. Microbiol. 2004; 70 (12): 7078–7085. [DOI:10.1128/AEM.70.12.7078-7085.2004]
50. Cesena C, Morelli L, Alander M, Siljander T, Tuomola E, Salminen S, Mattila-Sandholm T, Vilpponen-Salmela T, Von Wright A. Lactobacillus crispatus and its nonaggregating mutant in human colonization trials. J dairy sci. 2001; 84(5):1001-10. [DOI:10.3168/jds.S0022-0302(01)74559-6]
51. Collado MC, Meriluoto J, Salminen S. Interactions between pathogens and lactic acid bacteria: aggregation and coaggregation abilities. Eur.J.Food Res.Technol. 2007; 10 (7):0632.
52. Ershadian M, Arbab Soleimani N, Ajoudanifar H, Vaezi Khakhki MR. The Antimicrobial and Co-aggregation effects of probiotic lactobacilli against some pathogenic bacteria. Iran J Med Microbiol.2015; 9(3): 14-22.
53. Vandevoorde L, Christiaens H, Verstraete W. Prevalence of co-aggregation reactions among chicken lactobacilli. J Appl Microbiol. 1992; 72: 214–9.
54. Ekmekci H, Aslim B, Ozturk S. Characterization of vaginal lactobacilli co-aggregation ability with Escherichia coli. Microbiol Immunol. 2009; 53:59–65 [DOI:10.1111/j.1348-0421.2009.00115.x]
55. Pilipcineca E, Huismanb TT, Willemsenb PTJ, Appelmelkc BJ, Graaf FK, Oudega B. Identification by Tn10 transposon mutagenesis of host factors involved in the biosynthesis of K99 fimbriae of Escherichia coli: Effect of LPS core mutations. FEMS Microbiol. Lett. 1994;123:201–206. [DOI:10.1016/0378-1097(94)90295-X]



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