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Antibiotic sensitivity pattern of indigenous lactobacilli isolated from curd and human milk samples

Abstract

The gut microbiota plays a vital role in host well-being and lactic acid bacteria (LAB) have gained an overwhelming attention as health promoter. This perception has evolved from traditional dairy products to a money-spinning market of probiotics. The safety of probiotics is coupled to their intended use and LAB may act as pool of antimicrobial resistance genes that could be transferred to pathogens, either in food matrix or in gastrointestinal tract, which could be detrimental to host. This study evaluated the antibiotic susceptibility patterns of LAB isolated from curd (20) and human milk (11) samples. Antibiotic susceptibility was determined against 26 common antibiotics, following reference disc diffusion assay. A varied response in terms of susceptibility and resistance towards antibiotics was recorded. Among curd isolates, D7 (Lactobacillus plantarum) was the most resistant followed by D4, D8, D10 and D25. Among human milk isolates, HM-1 (L. casei) showed the highest resistance profile. All LAB isolates displayed high susceptibility pattern towards imipenem and meropenem. In general, high resistivity was exhibited by human milk isolates. The present study showed that antibiotic resistance is widespread among different lactobacilli, which may pose a food safety concern. Therefore, antibiotic sensitivity should be considered as a vital tool for safety assessment of probiotics.

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Abbreviations

ABR:

Antibiotic resistance

ABS:

Antibiotic susceptibility

LAB:

Lactic acid bacteria

References

  1. Ammor MS, Florez AB, Mayo B (2007) Antibiotic resistance in non-enterococcal lactic acid bacteria and bifidobacteria. Food Microbiol 24:559–570

    CAS  Article  Google Scholar 

  2. Aquilanti L, Garofalo C, Osimani A, Silvestri G, Vignaroli C, Clementi F (2007) Isolation and molecular characterization of antibiotic-resistant lactic acid bacteria from poultry and swine meat products. J Food Prot 70:557–565

    CAS  Article  Google Scholar 

  3. Arioli S, Elli M, Ricci G, Mora D (2013) Assessment of the susceptibility of lactic acid bacteria to biocides. Int J Food Microbiol 163:1–5

    CAS  Article  Google Scholar 

  4. Balamurugan R, Chandragunasekaran AS, Chellappan G, Rajaram K, Ramamoorthi G, Ramakrishna BS (2014) Probiotic potential of lactic acid bacteria present in homemade curd in southern India. Indian J Med Res 140:345–355

    Google Scholar 

  5. Bauer AW, Kirby WMM, Sherris JC, Turk M (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45:493–496

    CAS  Google Scholar 

  6. Belletti N, Gatti M, Bottari B, Neviani E, Tabanelli G, Gardini F (2009) Antibiotic resistance of lactobacilli isolated from two Italian hard cheeses. J Food Prot 72:2162–2169

    CAS  Article  Google Scholar 

  7. Beyan A, Ketema T, Bacha K (2011) Antimicrobial susceptibility pattern of lactic acid bacteria isolated from ergo, a traditional ethiopian fermented milk, Jimma, South West Ethiopia. Ethiop J Educ Sci 7:9–17

    Google Scholar 

  8. Charteris WP, Kelly PM, Morelli L, Collins JK (2001) Quality control Lactobacillus isolates for use with the API50 CH and API ZYM systems at 37 1C. J Basic Microbiol 41:241–251

    CAS  Article  Google Scholar 

  9. Clinical and Laboratory Standards Institute (CLSI) (2015) Performance standards for antimicrobial susceptibility testing: twenty-second informational supplement. In: CLSI document M100-S22. Clinical Laboratory Standard Institute, Wayne

  10. Curragh HJ, Collins MA (1992) High levels of spontaneous drug resistance in Lactobacillus. J Appl Bacteriol 73:31–36

    CAS  Article  Google Scholar 

  11. Danielsen M, Wind AA (2003) Susceptibility of Lactobacillus spp. to antimicrobial agents. Int J Food Microbiol 82:1–11

    CAS  Article  Google Scholar 

  12. Delgado S, Flrez AB, Mayo B (2005) Antibiotic susceptibility of Lactobacillus and Bifidobacterium species from the human gastrointestinal tract. Curr Microbiol 50:202–207

    CAS  Article  Google Scholar 

  13. Dixit G, Samarth D, Tale V, Bhadekar R (2013) Comparative studies on potential probiotic characteristics of Lactobacillus acidophilus strains. Eurasia J Biosci 7:1–9

    Article  Google Scholar 

  14. Erdourul O, Erbulur F (2006) Isolation and characterization of Lactobacillus bulgaricus and Lactobacillus casei from various foods. Turk J Biol 30:39–44

    Google Scholar 

  15. Gfeller KY, Roth M, Meile L, Teuber M (2003) Sequence and genetic organization of the 19.3-kb erythromycin and dalfopristin-resistance plasmid pLME300 from Lactobacillus fermentum ROT1. Plasmid 50:190–201

    CAS  Article  Google Scholar 

  16. Goldberg E, Bishara J (2012) Contemporary unconventional clinical use of co-trimoxazole. Clin Microbiol Infect 18:8–17

    CAS  Article  Google Scholar 

  17. Gueimonde M, Sanchez B, de los Reyes-Gavilán CG, Margolles A (2013) Antibiotic resistance in probiotic bacteria. Front Microbiol 4:1–6

    Article  Google Scholar 

  18. Halder D, Mandal S (2015) Curd lactobacilli with probiotic potentiality. Transl Biomed 7:61–66

    Google Scholar 

  19. Hawaz E (2014) Isolation and identification of probiotic lactic acid bacteria from curd and in vitro evaluation of its growth inhibition activities against pathogenic bacteria. Afr J Microbiol Res 8:1419–1425

    Article  Google Scholar 

  20. Hoque MZ, Akter F, Hossain KM, Rahman MSM, Billah MM, Islam KMD (2010) Isolation, identification and analysis of probiotic properties of Lactobacillus sp. from selective regional yoghurts. World J Dairy Food Sci 5:39–46

    Google Scholar 

  21. Hummel AS, Hertel C, Holzapeel WH, Franz CM (2007) Antibiotic resistances of starter and probiotic strains of lactic acid bacteria. Appl Environ Microbiol 73:730–739

    CAS  Article  Google Scholar 

  22. Jiang M, Zhang F, Wan C, Ziong Y, Shah NP, Wei H, Tao X (2016) Evaluation of probiotic properties of Lactobacillus plantarum WLPL04 isolated from human breast milk. J Dairy Sci 99:1–11

    Article  Google Scholar 

  23. Jose NM, Bunt CR, Hussain MA (2015) Implications of antibiotic resistance in probiotics. Food Rev Int 31(1):52–62

    CAS  Article  Google Scholar 

  24. Karapetkov N, Georgieva R, Rumyan N, Karaivanova E (2011) Antibiotic susceptibility of different lactic acid bacteria strains. Benef Microbes 2:335–339

    CAS  Article  Google Scholar 

  25. Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI (2011) Human nutrition, the gut microbiome and the immune system. Nature 474:327–336

    CAS  Article  Google Scholar 

  26. Ketema B, Tetemke M, Mogessie A (2010) Antibiotic susceptibility patterns of LAB isolated from Wakalim, a traditional Ethiopian fermented beef sausage. J Food Safety 30:213–223

    Article  Google Scholar 

  27. Klare I, Konstabel C, Muller-Bertling S, Reissbrodt R, Huys G, Vancanneyt M, Swings J, Goossens H, Witte W (2005) Evaluation of new broth media for microdilution antibiotic susceptibility testing of lactobacilli, pediococci, lactococci, and bifidobacteria. Appl Environ Microbiol 71:8982–8986

    CAS  Article  Google Scholar 

  28. Klare I, Konstabel C, Werner G, Huys G, Vankerckhoven V, Kahlmeter G, Hildebrandt B, Müller-Bertling S, Witte W, Goossens H (2007) Antimicrobial susceptibilities of Lactobacillus, Pediococcus and Lactococcus human isolates and cultures intended for probiotic or nutritional use. J Antimicrob Chemother 59:900–912

    CAS  Article  Google Scholar 

  29. Malek R, Hamdan S, Enshasy HAE, Othman NZ, Zainol NA, Sarmidi MR, Aziz RA (2010) Production of Lactobacillus salivarius, a new probiotic strain isolated from human breast milk, in semi industrial scale and studies on its functional characterization. In: Médez-Vilas A (ed) Current research, technology and education topics in applied microbiology and microbial biotechnology, pp 1196–1204

  30. Manzoor A, Ul-Haq I, Baig S, Qazi JI, Seratlic S (2016) Efficacy of locally isolated lactic acid bacteria against antibiotic-resistant uropathogens. Jundishapur J Microbiol 9:e18952

    Article  Google Scholar 

  31. Martin R, Olivares M, Marín ML, Fernandez L, Xaus J, Rodriguez JM (2005) Probiotic potential of 3 lactobacilli strains isolated from breast milk. J Hum Lact 21:8–17

    Article  Google Scholar 

  32. Maukonen J, Saarela M (2015) Human gut microbiota: does diet matter? Proc Nutr Soc 74:23–36

    CAS  Article  Google Scholar 

  33. Nawaz M, Wang J, Zhou A, Ma C, Wu X, Moore JE, Miller BC, Xu J (2011) Characterization and transfer of antibiotic resistance in lactic acid bacteria from fermented food products. Curr Microbiol 62:1081–1089

    CAS  Article  Google Scholar 

  34. Ocana V, Silva C, Nader-Macias ME (2006) Antibiotic susceptibility of potentially probiotic vaginal lactobacilli. Infect Dis Obstet Gynecol 18182:1–6

    Article  Google Scholar 

  35. Panwar H, Calderwood D, Grant IR, Grover S, Green BD (2014) Lactobacillus strains isolated from infant faeces possess potent inhibitory activity against intestinal alpha- and beta-glucosidases suggesting anti-diabetic potential. Eur J Nutr 53:1465–1474

    CAS  Article  Google Scholar 

  36. Panwar H, Calderwood D, Gillespie AL, Wylie AR, Graham SF, Grant IR, Grover S, Green BD (2016) Identification of lactic acid bacteria strains modulating incretin hormone secretion and gene expression in enteroendocrine cells. J Funct Foods 23:348–358

    CAS  Article  Google Scholar 

  37. Pfeifer Y, Cullik A, Witte W (2010) Resistance to cephalosporins and carbapenems in Gram-negative bacterial pathogens. Int J Med Microbiol 300:371–379

    CAS  Article  Google Scholar 

  38. Quercia S, Candela M, Giuliani C, Turroni S, Luiselli D, Rampelli S, Brigidi P, Franceschi C, Bacalini MG, Garagnani P, Pirazzini C (2014) From lifetime to evolution: timescales of human gut microbiota adaptation. Front Microbiol 5:1–9

    Article  Google Scholar 

  39. Rosenbaum M, Knight R, Leibel RL (2015) The gut microbiota in human energy homeostasis and obesity. Trends Endocrinol Metab 26:493–501

    CAS  Article  Google Scholar 

  40. Sharma J, Goyal A (2015) A study on the drug resistance of probiotic strains isolated from commercial probotic products available in the local market of Agra. Eur J Exp Biol 5:33–36

    CAS  Google Scholar 

  41. Sharma P, Tomar SK, Sangwan V, Goswami P, Singh R (2015) Antibiotic resistance of Lactobacillus sp. isolated from commercial probiotic preparations. J Food Saf 36:38–51

    Article  Google Scholar 

  42. Sharma C, Singh BP, Thakur N, Gulati S, Gupta S, Mishra SK, Panwar H (2017) Antibacterial effects of Lactobacillus isolates of curd and human milk origin against food-borne and human pathogens. 3 Biotech 7:1–9

    Google Scholar 

  43. Sukmarini L, Mustopa AZ, Normawati M, Muzdalifah I (2014) Identification of antibiotic resistance genes from lactic acid bacteria in Indonesian fermented foods. Hayati J Biosci 21:144–150

    Article  Google Scholar 

  44. Udhayashree N, Senbagam D, Senthilkumar B, Nithya K, Gurusamy R (2012) Production of bacteriocin and their application in food products. Asian Pac J Trop Biomed 2:S406–S410

    Article  Google Scholar 

  45. Zhou Q, Li M, Wang X, Li Q, Wang T, Zhu Q, Zhou X, Gao X, Li X (2012) Immune-related micro RNAs are abundant in breast milk exosomes. Int J Biol Sci 8:118–123

    CAS  Article  Google Scholar 

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Acknowledgements

The authors would like to acknowledge the financial support from SERB-MoFPI (SERB/MoFPI/026/2015) and SERB-DST (SB/YS/LS-131/2014), Government of India for carrying out the research work.

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Correspondence to Harsh Panwar.

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Sharma, C., Gulati, S., Thakur, N. et al. Antibiotic sensitivity pattern of indigenous lactobacilli isolated from curd and human milk samples. 3 Biotech 7, 53 (2017). https://doi.org/10.1007/s13205-017-0682-0

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Keywords

  • Antibiotic resistance
  • Susceptibility
  • Lactic acid bacteria
  • Lactobacillus
  • Probiotics