Research Article
Antimicrobial effects of inulin and Lactobacillus acidophilus La-5 on Escherichia coli O157, Staphylococcus aureus and Enterococcus faecalis in fermented milk
Abstract
One of the methods used to reduce antimicrobial resistance in microorganisms is the use of probiotics and prebiotics. This study aimed to investigate the interaction between pathogenic microorganisms that commonly cause foodborne infections and probiotics and prebiotics, specifically in fermented milk. In this context, L. acidophilus La-5 and inulin were included in the study. Pathogenic microorganisms evaluated in the study include E. coli O157:H7, E. faecalis and Methicillin-resistant S. aureus strains, which are frequently associated with foodborne infections. At the end of fermentation, it was determined that the increase in S. aureus numbers at the 3rd, 6th and 9th hours in all sample groups was statistically lower than the increase in E. coli O157:H7 and E. faecalis. This suggested that E. coli O157:H7 and E. faecalis may be more competitive than S. aureus. The study results show that the addition of probiotics and inulin does not provide a statistical inhibition effect against the pathogens evaluated within the scope of the study.
References
- Kaynaklar Anonim. (2019) Centers for Disease Control and Prevention. Antibiotic resistance threats in the United States, Atlanta, GA: U.S. Department of Health and Human Services. Erişim adresi: https://www.cdc.gov/drugresistance/biggest-threats.html, Erişim tarihi: 10.07.2024
- Anonim. (2022) World Health Organization. Food safety. Key facts. Erişim adresi: https://www.who.int/news-room/fact-sheets/detail/food-safety, Erişim tarihi: 10.07.2024
- Anonim. (2024) Centers for Disease Control and Prevention. E. coli Infection (Escherichia coli). Technical Information. Erişim adresi: https://www.cdc.gov/ecoli/php/technical-info/index.html, Erişim tarihi: 05.11.2024
- Balasubramanian D, Harper L, Shopsin B, Torres VJ. (2017) Staphylococcus aureus pathogenesis in diverse host environments. Pathog Dis. 75(1), ftx005. doi: 10.1093/femspd/ftx005
- Bedani R, Rossi EA, Saad SMI. (2013) Impact of inulin and okara on Lactobacillus acidophilus La-5 and Bifidobacterium animalis Bb-12 viability in a fermented soy product and probiotic survival under in vitro simulated gastrointestinal conditions. Food Microbiol. 34(2), 382-389. doi: 10.1016/j.fm.2013.01.012
- Charlier C, Cretenet M, Even S, Le Loir Y. (2009) Interactions between Staphylococcus aureus and lactic acid bacteria: an old story with new perspectives. Int J Food Microbiol. 131(1), 30-39. doi: 10.1016/j.ijfoodmicro.2008.06.032
- Donkor, L., Affrifah, N. S., Kunadu, A. P. H., Kwofie, S., Yeboah, S., Kuditchar, B. (2023) Modelling the survival of acid‐adapted and nonadapted Escherichia coli O157: H7 in Burkina: A Western African traditional fermented milk product. Int J Food Sci. 2023(1), 1011319. doi: 10.1155/2023/1011319
- Farag MA, El Hawary EA, Elmassry MM. (2020) Rediscovering acidophilus milk, its quality characteristics, manufacturing methods, flavor chemistry and nutritional value. Critical Rev in Food Sci Nutr. 60(18), 3024-3041. doi: 10.1080/10408398.2019.1675584
- Ghali ENHK, Chauhan SC, Yallapu MM. (2024) Inulin-based formulations as an emerging therapeutic strategy for cancer: A comprehensive review. Int J Biol Macromol. 129216. doi: 10.1016/j.ijbiomac.2024.129216
- Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD, Verbeke K, Reid, G. (2017) Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol. 14(8), 491-502. doi: 10.1038/nrgastro.2017.75
- Guarner F, Sanders ME, Szajewska H, Cohen H, Eliakim R, Herrera-deGuise C, Tarkan K, Dan M, Alejandro P, Balakrishnan R, Seppo S, Melberg J. (2024) World Gastroenterology Organisation Global Guidelines: Probiotics and prebiotics. J Clin Gastroenterol. 58(6), 533-553. doi: 10.1097/MCG.0000000000002002
- Gürbüz F, Baspinar E, Çamdeviren, H., Keskin S. (2003) Tekrarlanan Ölçümlü Deneme Düzenlerinin Analizi. 2. Baskı. Van: Yüzüncü Yıl Üniversitesi Matbaası.
- Helmy YA, Taha-Abdelaziz K, Hawwas HAEH, Ghosh S, AlKafaas SS, Moawad MM, Saied EM, Kassem II, Mawad AM. (2023) Antimicrobial resistance and recent alternatives to antibiotics for the control of bacterial pathogens with an emphasis on foodborne pathogens. Antibiot, 12(2), 274. doi: 10.3390/antibiotics12020274
- Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, Calder PC, Sanders ME. (2014) Expert consensus document: The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 11, 506-514. doi: 10.1038/nrgastro.2014.66
- Huang IF, Lin IC, Liu PF, Cheng MF, Liu YC, Hsieh YD, Chen JJ, Chen CL, Chang HW, Shu CW. (2015) Lactobacillus acidophilus attenuates Salmonella-induced intestinal inflammation via TGF-β signaling. BMC Microbiol. 15, 1-9. doi: 10.1186/s12866-015-0546-x
- Iraporda C, Rubel IA, Managó N, Manrique GD, Garrote GL, Abraham AG. (2022) Inulin addition improved probiotic survival in soy-based fermented beverage. World J Microbiol Biotechnol. 38(8), 133. doi: 10.1007/s11274-022-03322-4
- Li S, Ma C, Gong G, Liu Z, Chang C, Xu Z. (2016) The impact of onion juice on milk fermentation by Lactobacillus acidophilus. LWT-Food Sci Technol. 65, 543-548. doi: 10.1016/j.lwt.2015.08.042.
- Liu X, Wang M, Hu T, Lin X, Liang H, Li W, Zhao S, Zhong Y, Zhang H, Ge L, Jin X, Xiao L, Zou Y. (2024) Safety assessment of potential probiotic Lactobacillus acidophilus AM13-1 with high cholesterol-lowering capability isolated from human gut. Lett Appl Microbiol. 77(1), ovad143. doi: 10.1093/lambio/ovad143
- Ma Y, Lan G, Li C, Cambaza EM, Liu D, Ye X, Chen S, Ding T. (2019) Stress tolerance of Staphylococcus aureus with different antibiotic resistance profiles. Microb Pathogen. 133, 103549. doi: 10.1016/j.micpath.2019.103549
- Menezes MUFO, Bevilaqua GC, da Silva Nascimento IR, da Cruz Ximenes GN, Andrade SAC, dos Santos Cortez Barbosa NM. (2023) Antagonist action of Lactobacillus acidophilus against pathogenic strains in goat milk yogurt. J Food Sci Technol. 60(1), 353-360. doi: 10.1007/s13197-022-05622-x
- Nakajo K, Komori R, Ishikawa S, Ueno T, Suzuki Y, Iwami Y, Takahashi N. (2006) Resistance to acidic and alkaline environments in the endodontic pathogen Enterococcus faecalis. Oral microbiol Immunol. 21(5), 283-288. doi: 10.1111/j.1399-302X.2006.00289.x
- Nyathi N, Ndhlovu D, Rabvukwa E, Ndudzo A. (2024) Improving antimicrobial stewardship in human health using probiotics and their derivatives. Ghulam M. eds. Antimicrobial Stewardship - New Insights. doi: 10.5772/intechopen.112497
- Oliveira RPDS, Perego P, De Oliveira MN, Converti A. (2011) Effect of inulin as a prebiotic to improve growth and counts of a probiotic cocktail in fermented skim milk. LWT-Food Sci Technol. 44(2), 520-523. doi: 10.1016/j.lwt.2010.08.024
- Oliveira, RPDS, Perego, P., Converti, A., De Oliveira, M. N. (2009). The effect of inulin as a prebiotic on the production of probiotic fibre‐enriched fermented milk. Int J Dairy Technol. 62(2), 195-203. doi: 10.1111/j.1471-0307.2009.00471.x
- Onaran Acar B, Gülendağ E. (2023). Comparison of Antimicrobial Activities of Ethanol-and Water-Based Propolis Extracts on Various Foodborne Pathogens by Agar-Well Diffusion Method. Res Agri Sci, 54(3), 130-136.
- Sadler GD. (2017) Chapter 22: pH and Titratable acidity. Nielsen SS. ed. Food Analysis, Food Science Text Series, 389. Springer International Publishing, USA. p. 396-399. doi: 10.1007/978-3-319-45776-5
- Singha S, Thomas R, Viswakarma JN, Gupta VK. (2023) Foodborne Illnesses of Escherichia coli O157 origin and Its Control Measures. J Food Sci Technol. 60, 1274–1283. doi: 10.1007/s13197-022-05381-9ef
- Solval KM, Chouljenko A, Chotiko A, Sathivel S. (2019) Growth kinetics and lactic acid production of Lactobacillus plantarum NRRL B-4496, L. acidophilus NRRL B-4495, and L. reuteri B-14171 in media containing egg white hydrolysates. LWT 105, 393-399. doi: 10.1016/j.lwt.2019.01.058
- Urrutia-Baca VH, Hernandez-Hernandez SN, Martinez LM, Davila-Vega JP, Chuck-Hernández C. (2024) The role of probiotics in dairy foods and strategies to evaluate their functional modifications. Food Rev Int. 40(1), 434-456. doi: 10.1080/87559129.2023.2172426
- Varga L, Szigeti J, Gyenis B. (2006) Influence of chicory inulin on the survival of microbiota of a probiotic fermented milk during refrigerated storage. Ann Microbiol. 56, 139-141. doi: 10.1007/BF03174995
- Walsh LH, Walsh AM, Garcia-Perez I, Crispie F, Costabile A, Ellis R, Finlayson J, Finnegan LA, Claesson MJ, Holmes E, Cotter, PD. (2023) Comparison of the relative impacts of acute consumption of an inulin-enriched diet, milk kefir or a commercial probiotic product on the human gut microbiome and metabolome. npj Sci Food. 7(1), 41. doi: 10.1038/s41538-023-00216-z
Fermente sütte inülin ve Lactobacillus acidophilus La-5'in Escherichia coli O157, Staphylococcus aureus ve Enterococcus faecalis üzerindeki antimikrobiyal etkileri
Abstract
Mikroorganizmalarda antimikrobiyal direncini azaltmak için kullanılan yöntemlerden biri de probiyotik ve prebiyotiklerin kullanımıdır. Bu çalışma, yaygın olarak gıda kaynaklı enfeksiyonlara neden olan patojen mikroorganizmalar ile probiyotikler ve prebiyotikler arasındaki etkileşimin fermente süt özelinde araştırılmasını amaçlamıştır. Bu bağlamda, L. acidophilus La-5 ve inülin çalışmaya dahil edilmiştir. Çalışmada değerlendirilen patojen mikroorganizmalar arasında sıklıkla gıda kaynaklı enfeksiyonlarla ilişkilendirilen E. coli O157:H7, E. faecalis ve Metisiline dirençli S. aureus suşları bulunmaktadır. Fermentasyon sonunda tüm numune gruplarında 3., 6. ve 9. saatlerdeki S. aureus sayılarındaki artışın, E. coli O157:H7 ve E. faecalis artışına göre istatistiksel olarak daha düşük olduğu belirlenmiştir. Bu durum, E. coli O157:H7 ve E. faecalis’in S. aureus’a göre daha rekabetçi olabileceğini düşündürmüştür. Çalışma sonuçları probiyotik ve inülin ilavesinin çalışma kapsamında değerlendirilen patojenlere karşı istatistiksel olarak bir inhibisyon etkisi sağlamadığını göstermektedir.
References
- Kaynaklar Anonim. (2019) Centers for Disease Control and Prevention. Antibiotic resistance threats in the United States, Atlanta, GA: U.S. Department of Health and Human Services. Erişim adresi: https://www.cdc.gov/drugresistance/biggest-threats.html, Erişim tarihi: 10.07.2024
- Anonim. (2022) World Health Organization. Food safety. Key facts. Erişim adresi: https://www.who.int/news-room/fact-sheets/detail/food-safety, Erişim tarihi: 10.07.2024
- Anonim. (2024) Centers for Disease Control and Prevention. E. coli Infection (Escherichia coli). Technical Information. Erişim adresi: https://www.cdc.gov/ecoli/php/technical-info/index.html, Erişim tarihi: 05.11.2024
- Balasubramanian D, Harper L, Shopsin B, Torres VJ. (2017) Staphylococcus aureus pathogenesis in diverse host environments. Pathog Dis. 75(1), ftx005. doi: 10.1093/femspd/ftx005
- Bedani R, Rossi EA, Saad SMI. (2013) Impact of inulin and okara on Lactobacillus acidophilus La-5 and Bifidobacterium animalis Bb-12 viability in a fermented soy product and probiotic survival under in vitro simulated gastrointestinal conditions. Food Microbiol. 34(2), 382-389. doi: 10.1016/j.fm.2013.01.012
- Charlier C, Cretenet M, Even S, Le Loir Y. (2009) Interactions between Staphylococcus aureus and lactic acid bacteria: an old story with new perspectives. Int J Food Microbiol. 131(1), 30-39. doi: 10.1016/j.ijfoodmicro.2008.06.032
- Donkor, L., Affrifah, N. S., Kunadu, A. P. H., Kwofie, S., Yeboah, S., Kuditchar, B. (2023) Modelling the survival of acid‐adapted and nonadapted Escherichia coli O157: H7 in Burkina: A Western African traditional fermented milk product. Int J Food Sci. 2023(1), 1011319. doi: 10.1155/2023/1011319
- Farag MA, El Hawary EA, Elmassry MM. (2020) Rediscovering acidophilus milk, its quality characteristics, manufacturing methods, flavor chemistry and nutritional value. Critical Rev in Food Sci Nutr. 60(18), 3024-3041. doi: 10.1080/10408398.2019.1675584
- Ghali ENHK, Chauhan SC, Yallapu MM. (2024) Inulin-based formulations as an emerging therapeutic strategy for cancer: A comprehensive review. Int J Biol Macromol. 129216. doi: 10.1016/j.ijbiomac.2024.129216
- Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD, Verbeke K, Reid, G. (2017) Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol. 14(8), 491-502. doi: 10.1038/nrgastro.2017.75
- Guarner F, Sanders ME, Szajewska H, Cohen H, Eliakim R, Herrera-deGuise C, Tarkan K, Dan M, Alejandro P, Balakrishnan R, Seppo S, Melberg J. (2024) World Gastroenterology Organisation Global Guidelines: Probiotics and prebiotics. J Clin Gastroenterol. 58(6), 533-553. doi: 10.1097/MCG.0000000000002002
- Gürbüz F, Baspinar E, Çamdeviren, H., Keskin S. (2003) Tekrarlanan Ölçümlü Deneme Düzenlerinin Analizi. 2. Baskı. Van: Yüzüncü Yıl Üniversitesi Matbaası.
- Helmy YA, Taha-Abdelaziz K, Hawwas HAEH, Ghosh S, AlKafaas SS, Moawad MM, Saied EM, Kassem II, Mawad AM. (2023) Antimicrobial resistance and recent alternatives to antibiotics for the control of bacterial pathogens with an emphasis on foodborne pathogens. Antibiot, 12(2), 274. doi: 10.3390/antibiotics12020274
- Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, Calder PC, Sanders ME. (2014) Expert consensus document: The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 11, 506-514. doi: 10.1038/nrgastro.2014.66
- Huang IF, Lin IC, Liu PF, Cheng MF, Liu YC, Hsieh YD, Chen JJ, Chen CL, Chang HW, Shu CW. (2015) Lactobacillus acidophilus attenuates Salmonella-induced intestinal inflammation via TGF-β signaling. BMC Microbiol. 15, 1-9. doi: 10.1186/s12866-015-0546-x
- Iraporda C, Rubel IA, Managó N, Manrique GD, Garrote GL, Abraham AG. (2022) Inulin addition improved probiotic survival in soy-based fermented beverage. World J Microbiol Biotechnol. 38(8), 133. doi: 10.1007/s11274-022-03322-4
- Li S, Ma C, Gong G, Liu Z, Chang C, Xu Z. (2016) The impact of onion juice on milk fermentation by Lactobacillus acidophilus. LWT-Food Sci Technol. 65, 543-548. doi: 10.1016/j.lwt.2015.08.042.
- Liu X, Wang M, Hu T, Lin X, Liang H, Li W, Zhao S, Zhong Y, Zhang H, Ge L, Jin X, Xiao L, Zou Y. (2024) Safety assessment of potential probiotic Lactobacillus acidophilus AM13-1 with high cholesterol-lowering capability isolated from human gut. Lett Appl Microbiol. 77(1), ovad143. doi: 10.1093/lambio/ovad143
- Ma Y, Lan G, Li C, Cambaza EM, Liu D, Ye X, Chen S, Ding T. (2019) Stress tolerance of Staphylococcus aureus with different antibiotic resistance profiles. Microb Pathogen. 133, 103549. doi: 10.1016/j.micpath.2019.103549
- Menezes MUFO, Bevilaqua GC, da Silva Nascimento IR, da Cruz Ximenes GN, Andrade SAC, dos Santos Cortez Barbosa NM. (2023) Antagonist action of Lactobacillus acidophilus against pathogenic strains in goat milk yogurt. J Food Sci Technol. 60(1), 353-360. doi: 10.1007/s13197-022-05622-x
- Nakajo K, Komori R, Ishikawa S, Ueno T, Suzuki Y, Iwami Y, Takahashi N. (2006) Resistance to acidic and alkaline environments in the endodontic pathogen Enterococcus faecalis. Oral microbiol Immunol. 21(5), 283-288. doi: 10.1111/j.1399-302X.2006.00289.x
- Nyathi N, Ndhlovu D, Rabvukwa E, Ndudzo A. (2024) Improving antimicrobial stewardship in human health using probiotics and their derivatives. Ghulam M. eds. Antimicrobial Stewardship - New Insights. doi: 10.5772/intechopen.112497
- Oliveira RPDS, Perego P, De Oliveira MN, Converti A. (2011) Effect of inulin as a prebiotic to improve growth and counts of a probiotic cocktail in fermented skim milk. LWT-Food Sci Technol. 44(2), 520-523. doi: 10.1016/j.lwt.2010.08.024
- Oliveira, RPDS, Perego, P., Converti, A., De Oliveira, M. N. (2009). The effect of inulin as a prebiotic on the production of probiotic fibre‐enriched fermented milk. Int J Dairy Technol. 62(2), 195-203. doi: 10.1111/j.1471-0307.2009.00471.x
- Onaran Acar B, Gülendağ E. (2023). Comparison of Antimicrobial Activities of Ethanol-and Water-Based Propolis Extracts on Various Foodborne Pathogens by Agar-Well Diffusion Method. Res Agri Sci, 54(3), 130-136.
- Sadler GD. (2017) Chapter 22: pH and Titratable acidity. Nielsen SS. ed. Food Analysis, Food Science Text Series, 389. Springer International Publishing, USA. p. 396-399. doi: 10.1007/978-3-319-45776-5
- Singha S, Thomas R, Viswakarma JN, Gupta VK. (2023) Foodborne Illnesses of Escherichia coli O157 origin and Its Control Measures. J Food Sci Technol. 60, 1274–1283. doi: 10.1007/s13197-022-05381-9ef
- Solval KM, Chouljenko A, Chotiko A, Sathivel S. (2019) Growth kinetics and lactic acid production of Lactobacillus plantarum NRRL B-4496, L. acidophilus NRRL B-4495, and L. reuteri B-14171 in media containing egg white hydrolysates. LWT 105, 393-399. doi: 10.1016/j.lwt.2019.01.058
- Urrutia-Baca VH, Hernandez-Hernandez SN, Martinez LM, Davila-Vega JP, Chuck-Hernández C. (2024) The role of probiotics in dairy foods and strategies to evaluate their functional modifications. Food Rev Int. 40(1), 434-456. doi: 10.1080/87559129.2023.2172426
- Varga L, Szigeti J, Gyenis B. (2006) Influence of chicory inulin on the survival of microbiota of a probiotic fermented milk during refrigerated storage. Ann Microbiol. 56, 139-141. doi: 10.1007/BF03174995
- Walsh LH, Walsh AM, Garcia-Perez I, Crispie F, Costabile A, Ellis R, Finlayson J, Finnegan LA, Claesson MJ, Holmes E, Cotter, PD. (2023) Comparison of the relative impacts of acute consumption of an inulin-enriched diet, milk kefir or a commercial probiotic product on the human gut microbiome and metabolome. npj Sci Food. 7(1), 41. doi: 10.1038/s41538-023-00216-z
There are 31 citations in total.
Details
| Primary Language | Turkish |
|---|---|
| Subjects | Food Microbiology, Dairy Technology |
| Journal Section | Original Article |
| Authors | |
| Publication Date | July 24, 2025 |
| Submission Date | August 27, 2024 |
| Acceptance Date | January 16, 2025 |
| Published in Issue | Year 2025 Volume: 36 Issue: 1 |
