Anti-invasion activities of heat-killed lactic acid bacteria isolates against Salmonella enterica serovar Typhimurium
-
Anis Syahirah Saifor Adzuan
,
Sharifah Aminah Syed Mohamad
,
Rashidah Iberahim
,
Noor Nadia Syahira Mohd Kamal
,
Nurliana Abd Mutalib
,
Nur Intan Hasbullah
,
Muneer Alsaydi
,
Nor'aishah Hasan
,
Low Kheng Oon
,
Olaide Olawunmi Ajibola
,
Rozila Alias
,
Maimunah Mustakim
,
Azlin Sham Rambely
,
Emida Mohamed
,
Mohammad Reza Pourmand
Abstract
Background and Objectives: The most common cause of severe foodborne salmonellosis is S. Typhimurium. Its interaction with intestinal epithelial cells is little known. Lactic acid bacteria (LAB) were recognized as a prominent probiotic gastrointestinal microbiota of humans and animals that confer health-promoting and protective effects. This study aims to determine the anti-invasion and antibacterial effects of heat-killed LAB (HK-LAB) isolates against S. Typhimurium towards human intestinal cells.
Materials and Methods: 12 HK-LAB isolates from 3 sources of origin (stingless bee, plant, and food) were tested to determine the adhesion of HK-LAB to Caco-2 cells, anti-invasion and antibacterial activities against S. Typhimurium, the adhesion and invasion pattern of S. Typhimurium on intestinal epithelial cells (Caco-2) and assessing the effect of LAB on the S. Typhimurium-host cell interaction.
Results: Tairu isolates from food have the highest adhesion rate with 19 ± 1.32/10 Caco-2 cells followed by HK-LAB R-isolate from plant 17 ± 0.70/10 Caco-2 cells, which is similar to the control (Lactobacillus casei). In the anti-invasion assay, the two HK-LAB isolates that had the strongest adherence to Caco-2 cells, Tairu-isolate inhibited at 78.1 ± 3.06% and R-isolate inhibited at 64.76 ± 9.02% compared to the positive control (63.81 ± 1.15%), which led to increased suppression of S. Typhimurium accordingly. Tairu and R isolates were tested for their antibacterial ability against S. Typhimurium. Both R and Tairu isolates displayed strong inhibition zones (27 ± 0.06 mm, 23 ± 0.06 mm) respectively.
Conclusion: These findings suggest that the anti-invasion activities of HK-LAB R and Tairu may correlate to their bactericidal effects that serve to protect the host from infection.
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9. Yusof TA (2022). Jif peanut butter recalled over Salmonella fears. New Straits Times.
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14. Sharma S, Kanwar SS. Adherence potential of indigenous lactic acid bacterial isolates obtained from fermented foods of Western Himalayas to intestinal epithelial Caco-2 and HT-29 cell lines. J Food Sci Technol 2017; 54: 3504-3511.
15. Hasbullah NI, Aminah S, Syed Mohamad SA, Iberahim R, Hasan N, Ahmad N, et al. A review on in vitro cell culture model for bacterial adhesion and invasion: From simple monoculture to co-culture human intestinal epithelium model. J Pharm Res Int 2021; 33: 97-106.
16. Asadi A, Razavi S, Talebi M, Gholami M. A review on anti-adhesion therapies of bacterial diseases. Infection 2019; 47: 13-23.
17. Paula Menezes Barbosa P, Roggia Ruviaro A, Mateus Martins I, Alves Macedo J, LaPointe G, Alves Macedo G. Effect of enzymatic treatment of citrus by-products on bacterial growth, adhesion and cytokine production by Caco-2 cells. Food Funct 2020; 11: 8996-9009.
18. Birhanu BT, Lee EB, Lee SJ, Park SC. Targeting Salmonella Typhimurium invasion and intracellular survival using pyrogallol. Front Microbiol 2021; 12: 631426.
19. Mechesso AF, Quah Y, Park S-C. Ginsenoside Rg3 reduces the adhesion, invasion, and intracellular survival of Salmonella enterica serovar Typhimurium. J Ginseng Res 2021; 45: 75-85.
20. Parker P, Sando L, Pearson R, Kongsuwan K, Tellam RL, Smith S. Bovine Muc1 inhibits the binding of enteric bacteria to Caco-2 cells. Glycoconj J 2010; 27: 89-97.
21. Yang Y, Li J, Yin Y, Guo D, Jin T, Guan N, et al. Antibiofilm activity of coenzyme Q0 against Salmonella Typhimurium and its effect on adhesion-invasion and survival-replication. Appl Microbiol Biotechnol 2019; 103: 8545-8557.
22. Tian L, Zhong C, He Y, Lu Q, Wang Y, Zhao X, et al. Preventive of Lacticcaseibacillus casei WLCA02 against Salmonella Typhimurium infection via strengthening the intestinal barrier and activating the macrophages. J Funct Foods 2023; 104: 105507.
23. Ngalimat MS, Abd Rahman RNZR, Yusof MT, Amir Hamzah AS, Zawawi N, Sabri S. A review on the association of bacteria with stingless bees. Sains Malays 2020; 49: 1853-1863.
24. Jang HJ, Song MW, Lee NK, Paik HD. Antioxidant effects of live and heat-killed probiotic Lactobacillus plantarum ln1 isolated from kimchi. J Food Sci Technol 2018; 55: 3174-3180.
25. Somashekaraiah R, Shruthi B, Deepthi BV, Sreenivasa MY. Probiotic properties of lactic acid bacteria isolated from neera: A naturally fermenting coconut palm nectar. Front Microbiol 2019; 10: 1382.
26. Gupta R, Jeevaratnam K, Fatima A. Lactic acid bacteria: Probiotic characteristic, selection criteria, and its role in human health (a review). J Emerg Technol Innov Res 2018; 5: 411-424.
27. Kathiresan K, Thiruneelakandan G. Prospects of lactic acid bacteria of marine origin. Indian J Biotechnol 2008; 7: 170-177.
28. Gao Z, Daliri EB, Wang J, Liu D, Chen S, Ye X, et al. Inhibitory effect of lactic acid bacteria on foodborne pathogens: A review. J Food Prot 2019; 82: 441-453.
29. Jankowska A, Laubitz D, Antushevich H, Zabielski R, Grzesiuk E. Competition of Lactobacillus paracasei with Salmonella enterica for adhesion to Caco-2 cells. J Biomed Biotechnol 2008; 2008: 357964.
30. Katkowska M, Garbacz K, Kusiak A. Probiotics: Should all patients take them? Microorganisms 2021; 9: 2620.
31. Karbowiak M, Gałek M, Szydłowska A, Zielińska D. The influence of the degree of thermal inactivation of probiotic lactic acid bacteria and their postbiotics on aggregation and adhesion inhibition of selected pathogens. Pathogens 2022; 11: 1260.
32. Tareb R, Bernardeau M, Gueguen M, Vernoux JP. In vitro characterization of aggregation and adhesion properties of viable and heat-killed forms of two probiotic Lactobacillus strains and interaction with foodborne zoonotic bacteria, especially Campylobacter jejuni. J Med Microbiol 2013; 62: 637-649.
33. Servin AL. Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol Rev 2004; 28: 405-440.
34. Aiba Y, Ishikawa H, Tokunaga M, Komatsu Y. Anti-Helicobacter pylori activity of non-living, heat-killed form of Lactobacilli including Lactobacillus johnsonii No.1088. FEMS Microbiol Lett 2017; 364: 10.1093/femsle/fnx102.
35. Wassie M, Wassie T. Isolation and Identification of Lactic Acid Bacteria from Raw Cow Milk. Int J Adv Res Biol Sci 2016; 3: 44-49.
36. Antunes F, Andrade F, Araújo F, Ferreira D, Sarmento B. Establishment of a triple co-culture in vitro cell models to study intestinal absorption of peptide drugs. Eur J Pharm Biopharm 2013; 83: 427-435.
37. Campana R, Merli A, Verboni M, Biondo F, Favi G, Duranti A, et al. Synthesis and evaluation of saccharide-based aliphatic and aromatic esters as antimicrobial and antibiofilm agents. Pharmaceuticals (Basel) 2019; 12: 186.
38. Burkholder KM, Fletcher DH, Gileau L, Kandolo A. Lactic acid bacteria decrease Salmonella enterica Javiana virulence and modulate host inflammation during infection of an intestinal epithelial cell line. Pathog Dis 2019; 77: ftz025.
39. Dostal A, Gagnon M, Chassard C, Zimmermann MB, O’Mahony L, Lacroix C. Salmonella Adhesion, invasion and cellular immune responses are differentially affected by iron concentrations in a combined in vitro gut Fermentation-Cell model. PLoS One 2014; 9(3): e93549.
40. Gagnon M, Zihler Berner A, Chervet N, Chassard C, Lacroix C. Comparison of the Caco-2, HT-29 and the mucus-secreting HT29-MTX intestinal cell models to investigate Salmonella adhesion and invasion. J Microbiol Methods 2013; 94: 274-279.
41. Chen W-H, Luo G-F, Lei Q, Hong S, Qiu W-X, Liu L-H, et al. Overcoming the heat endurance of tumour cells by interfering with the anaerobic glycolysis metabolism for improved photothermal therapy. ACS Nano 2017; 11: 1419-1431.
42. Lin W-H, Y-u B, Lin C-K, Hwang W-Z, Tsen H-Y. Immune effect of heat-killed multistrain of Lactobacillus acidophilus against Salmonella Typhimurium invasion to mice. J Appl Microbiol 2007; 102: 22-31.
43. Vasiee A, Falah F, Behbahani BA, Tabatabaee-Yazdi F. Probiotic characterization of Pediococcus strains isolated from Iranian cereal-dairy fermented product: Interaction with pathogenic bacteria and the enteric cell line Caco-2. J Biosci Bioeng 2020; 130: 471-479.
44. Reuben RC, Roy PC, Sarkar SL, Alam RU, Jahid IK. Isolation, characterization, and assessment of lactic acid bacteria toward their selection as poultry probiotics. BMC Microbiol 2019; 19: 253.
45. Ahmad A, Yap WB, Kofli NT, Ghazali, AR. Probiotic potentials of Lactobacillus plantarum isolated from fermented durian (Tempoyak), a Malaysian traditional condiment. Food Sci Nutr 2018; 6: 1370-1377.
46. Mokoena MP, Omatola CA, Olaniran AO. Applications of lactic acid bacteria and their bacteriocins against food spoilage microorganisms and foodborne pathogens. Molecules 2021; 26: 7055.
47. Chen C-Y, Tsen H-Y, Lin C-L, Lin C-K, Chuang L-T, Chen C-S, et al. Enhancement of the immune response against Salmonella infection of mice by heat-killed multispecies combinations of lactic acid bacteria. J Med Microbiol 2013; 62: 1657-1664.
48. Feng J, Wang L, Zhou L, Yang X, Zhao X. Using in vitro immunomodulatory properties of lactic acid bacteria for selection of probiotics against Salmonella infection in broiler chicks. PLoS One 2016; 11(1): e0147630.
49. Zeng J, Jiang J, Zhu W, Chu Y. Heat-killed yogurt-containing lactic acid bacteria prevent cytokine-induced barrier disruption in human intestinal Caco-2 cells. Ann Microbiol 2016; 66: 171-178.
50. Tan W, Tian Y, Zhang Q, Miao S, Wu W, Miao X, et al. Antioxidant and antibacterial activity of Apis laboriosa honey against Salmonella enterica serovar Typhimurium. Front Nutr 2023; 10: 1181492.
51. Atta H, Gimba A, Bamgbose T. Antimicrobial activity of lactic acid bacteria isolated from garri on Escherichia coli strains isolated from clinical and environmental samples. Agric Sci Technol 2020; 12: 357-365.
52. Abdalla AK, Ayyash MM, Olaimat AN, Osaili TM, Al-Nabulsi AA, Shah NP, et al. Exopolysaccharides as antimicrobial agents: Mechanism and spectrum of activity. Front Microbiol 2021; 12: 664395.
2. Abdul-Mutalib NA, Syafinaz AN, Sakai K, Shirai Y. An overview of foodborne illness and food safety in Malaysia. Int Food Res J 2015; 22: 896-901.
3. Mohan A, Munusamy C, Tan Y-C, Muthuvelu S, Hashim R, Chien S-L, et al. Invasive Salmonella infections among children in Bintulu, Sarawak, Malaysian Borneo: A 6-year retrospective review. BMC Infect Dis 2019; 19: 330.
4. Jamaludin MH (2016). Canteen operators, food suppliers to have contracts terminated if linked to food poisoning cases. from: http://www.nst.com.my/news/2016/08/167226/canteen-operators-food-suppliers-have-contracts-terminated-if-linked-food
5. Karim BA, Latip AL, Shukor ASA, Rashid NA, Mohd WMW, Kamaludin F. A large common source outbreak of Salmonella Typhimurium Linked to Kuala Terengganu Night Markets, Malaysia, 2014. OSIR 2017; 10: 1-7. https://doi.org/10.59096/osir.v10i2.263136
6. Abdullah NBA, Ismail AA. Food poisoning outbreaks among school children in Terengganu and their associated factors. Sains Malays 2021; 50: 1027-1036.
7. Bernama (2018). Laksa poisoning is caused by Salmonella. New Straits Times. https://www.nst.com.my/news/nation/2018/10/423469/laksa-poisoning-caused-salmonella
8. Bernama (2021). Singapore recalls eggs from yet another Malaysian farm. New Straits Times.
https://www.nst.com.my/news/nation/2021/03/675438/singapore-recalls-eggs-yet-another-malaysia-farm
9. Yusof TA (2022). Jif peanut butter recalled over Salmonella fears. New Straits Times.
https://www.nst.com.my/news/nation/2022/05/800716/jif-peanut-butter-recalled-over-salmonella-fears
10. Somorin YM, Odeyemi OA, Ateba CN. Salmonella is the most common foodborne pathogen in African food exports to the European Union: Analysis of the rapid alert system for food and feed (1999–2019). Food Control 2021; 123: 107849.
11. European Centre for Disease Prevention and Control (2024). Salmonellosis outbreaks.
https://www.ecdc.europa.eu/en/infectious-diseases-and-public-health/salmonellosis/threats-and-outbreaks
12. Centers for Disease Control and Prevention CDC (2024). Salmonella Infection https://www.cdc.gov/salmonella/index.html
13. Krausova G, Hynstova I, Svejsti R, Mrvikova I, Kadlec R. Identification of synbiotics conducive to probiotics adherence to intestinal mucosa using an in vitro Caco-2 and HT29-MTX cell model. Processes 2021; 9: 569.
14. Sharma S, Kanwar SS. Adherence potential of indigenous lactic acid bacterial isolates obtained from fermented foods of Western Himalayas to intestinal epithelial Caco-2 and HT-29 cell lines. J Food Sci Technol 2017; 54: 3504-3511.
15. Hasbullah NI, Aminah S, Syed Mohamad SA, Iberahim R, Hasan N, Ahmad N, et al. A review on in vitro cell culture model for bacterial adhesion and invasion: From simple monoculture to co-culture human intestinal epithelium model. J Pharm Res Int 2021; 33: 97-106.
16. Asadi A, Razavi S, Talebi M, Gholami M. A review on anti-adhesion therapies of bacterial diseases. Infection 2019; 47: 13-23.
17. Paula Menezes Barbosa P, Roggia Ruviaro A, Mateus Martins I, Alves Macedo J, LaPointe G, Alves Macedo G. Effect of enzymatic treatment of citrus by-products on bacterial growth, adhesion and cytokine production by Caco-2 cells. Food Funct 2020; 11: 8996-9009.
18. Birhanu BT, Lee EB, Lee SJ, Park SC. Targeting Salmonella Typhimurium invasion and intracellular survival using pyrogallol. Front Microbiol 2021; 12: 631426.
19. Mechesso AF, Quah Y, Park S-C. Ginsenoside Rg3 reduces the adhesion, invasion, and intracellular survival of Salmonella enterica serovar Typhimurium. J Ginseng Res 2021; 45: 75-85.
20. Parker P, Sando L, Pearson R, Kongsuwan K, Tellam RL, Smith S. Bovine Muc1 inhibits the binding of enteric bacteria to Caco-2 cells. Glycoconj J 2010; 27: 89-97.
21. Yang Y, Li J, Yin Y, Guo D, Jin T, Guan N, et al. Antibiofilm activity of coenzyme Q0 against Salmonella Typhimurium and its effect on adhesion-invasion and survival-replication. Appl Microbiol Biotechnol 2019; 103: 8545-8557.
22. Tian L, Zhong C, He Y, Lu Q, Wang Y, Zhao X, et al. Preventive of Lacticcaseibacillus casei WLCA02 against Salmonella Typhimurium infection via strengthening the intestinal barrier and activating the macrophages. J Funct Foods 2023; 104: 105507.
23. Ngalimat MS, Abd Rahman RNZR, Yusof MT, Amir Hamzah AS, Zawawi N, Sabri S. A review on the association of bacteria with stingless bees. Sains Malays 2020; 49: 1853-1863.
24. Jang HJ, Song MW, Lee NK, Paik HD. Antioxidant effects of live and heat-killed probiotic Lactobacillus plantarum ln1 isolated from kimchi. J Food Sci Technol 2018; 55: 3174-3180.
25. Somashekaraiah R, Shruthi B, Deepthi BV, Sreenivasa MY. Probiotic properties of lactic acid bacteria isolated from neera: A naturally fermenting coconut palm nectar. Front Microbiol 2019; 10: 1382.
26. Gupta R, Jeevaratnam K, Fatima A. Lactic acid bacteria: Probiotic characteristic, selection criteria, and its role in human health (a review). J Emerg Technol Innov Res 2018; 5: 411-424.
27. Kathiresan K, Thiruneelakandan G. Prospects of lactic acid bacteria of marine origin. Indian J Biotechnol 2008; 7: 170-177.
28. Gao Z, Daliri EB, Wang J, Liu D, Chen S, Ye X, et al. Inhibitory effect of lactic acid bacteria on foodborne pathogens: A review. J Food Prot 2019; 82: 441-453.
29. Jankowska A, Laubitz D, Antushevich H, Zabielski R, Grzesiuk E. Competition of Lactobacillus paracasei with Salmonella enterica for adhesion to Caco-2 cells. J Biomed Biotechnol 2008; 2008: 357964.
30. Katkowska M, Garbacz K, Kusiak A. Probiotics: Should all patients take them? Microorganisms 2021; 9: 2620.
31. Karbowiak M, Gałek M, Szydłowska A, Zielińska D. The influence of the degree of thermal inactivation of probiotic lactic acid bacteria and their postbiotics on aggregation and adhesion inhibition of selected pathogens. Pathogens 2022; 11: 1260.
32. Tareb R, Bernardeau M, Gueguen M, Vernoux JP. In vitro characterization of aggregation and adhesion properties of viable and heat-killed forms of two probiotic Lactobacillus strains and interaction with foodborne zoonotic bacteria, especially Campylobacter jejuni. J Med Microbiol 2013; 62: 637-649.
33. Servin AL. Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol Rev 2004; 28: 405-440.
34. Aiba Y, Ishikawa H, Tokunaga M, Komatsu Y. Anti-Helicobacter pylori activity of non-living, heat-killed form of Lactobacilli including Lactobacillus johnsonii No.1088. FEMS Microbiol Lett 2017; 364: 10.1093/femsle/fnx102.
35. Wassie M, Wassie T. Isolation and Identification of Lactic Acid Bacteria from Raw Cow Milk. Int J Adv Res Biol Sci 2016; 3: 44-49.
36. Antunes F, Andrade F, Araújo F, Ferreira D, Sarmento B. Establishment of a triple co-culture in vitro cell models to study intestinal absorption of peptide drugs. Eur J Pharm Biopharm 2013; 83: 427-435.
37. Campana R, Merli A, Verboni M, Biondo F, Favi G, Duranti A, et al. Synthesis and evaluation of saccharide-based aliphatic and aromatic esters as antimicrobial and antibiofilm agents. Pharmaceuticals (Basel) 2019; 12: 186.
38. Burkholder KM, Fletcher DH, Gileau L, Kandolo A. Lactic acid bacteria decrease Salmonella enterica Javiana virulence and modulate host inflammation during infection of an intestinal epithelial cell line. Pathog Dis 2019; 77: ftz025.
39. Dostal A, Gagnon M, Chassard C, Zimmermann MB, O’Mahony L, Lacroix C. Salmonella Adhesion, invasion and cellular immune responses are differentially affected by iron concentrations in a combined in vitro gut Fermentation-Cell model. PLoS One 2014; 9(3): e93549.
40. Gagnon M, Zihler Berner A, Chervet N, Chassard C, Lacroix C. Comparison of the Caco-2, HT-29 and the mucus-secreting HT29-MTX intestinal cell models to investigate Salmonella adhesion and invasion. J Microbiol Methods 2013; 94: 274-279.
41. Chen W-H, Luo G-F, Lei Q, Hong S, Qiu W-X, Liu L-H, et al. Overcoming the heat endurance of tumour cells by interfering with the anaerobic glycolysis metabolism for improved photothermal therapy. ACS Nano 2017; 11: 1419-1431.
42. Lin W-H, Y-u B, Lin C-K, Hwang W-Z, Tsen H-Y. Immune effect of heat-killed multistrain of Lactobacillus acidophilus against Salmonella Typhimurium invasion to mice. J Appl Microbiol 2007; 102: 22-31.
43. Vasiee A, Falah F, Behbahani BA, Tabatabaee-Yazdi F. Probiotic characterization of Pediococcus strains isolated from Iranian cereal-dairy fermented product: Interaction with pathogenic bacteria and the enteric cell line Caco-2. J Biosci Bioeng 2020; 130: 471-479.
44. Reuben RC, Roy PC, Sarkar SL, Alam RU, Jahid IK. Isolation, characterization, and assessment of lactic acid bacteria toward their selection as poultry probiotics. BMC Microbiol 2019; 19: 253.
45. Ahmad A, Yap WB, Kofli NT, Ghazali, AR. Probiotic potentials of Lactobacillus plantarum isolated from fermented durian (Tempoyak), a Malaysian traditional condiment. Food Sci Nutr 2018; 6: 1370-1377.
46. Mokoena MP, Omatola CA, Olaniran AO. Applications of lactic acid bacteria and their bacteriocins against food spoilage microorganisms and foodborne pathogens. Molecules 2021; 26: 7055.
47. Chen C-Y, Tsen H-Y, Lin C-L, Lin C-K, Chuang L-T, Chen C-S, et al. Enhancement of the immune response against Salmonella infection of mice by heat-killed multispecies combinations of lactic acid bacteria. J Med Microbiol 2013; 62: 1657-1664.
48. Feng J, Wang L, Zhou L, Yang X, Zhao X. Using in vitro immunomodulatory properties of lactic acid bacteria for selection of probiotics against Salmonella infection in broiler chicks. PLoS One 2016; 11(1): e0147630.
49. Zeng J, Jiang J, Zhu W, Chu Y. Heat-killed yogurt-containing lactic acid bacteria prevent cytokine-induced barrier disruption in human intestinal Caco-2 cells. Ann Microbiol 2016; 66: 171-178.
50. Tan W, Tian Y, Zhang Q, Miao S, Wu W, Miao X, et al. Antioxidant and antibacterial activity of Apis laboriosa honey against Salmonella enterica serovar Typhimurium. Front Nutr 2023; 10: 1181492.
51. Atta H, Gimba A, Bamgbose T. Antimicrobial activity of lactic acid bacteria isolated from garri on Escherichia coli strains isolated from clinical and environmental samples. Agric Sci Technol 2020; 12: 357-365.
52. Abdalla AK, Ayyash MM, Olaimat AN, Osaili TM, Al-Nabulsi AA, Shah NP, et al. Exopolysaccharides as antimicrobial agents: Mechanism and spectrum of activity. Front Microbiol 2021; 12: 664395.
| Files | ||
| Issue | Vol 16 No 6 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v16i6.17254 | |
| Keywords | ||
| Salmonella Typhimurium; Lactic acid bacteria; Caco-2 cells; Anti-invasion | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Saifor Adzuan AS, Syed Mohamad SA, Iberahim R, Syahira Mohd Kamal NN, Abd Mutalib N, Hasbullah NI, Alsaydi M, Hasan N, Oon LK, Olawunmi Ajibola O, Alias R, Mustakim M, Rambely AS, Mohamed E, Pourmand MR. Anti-invasion activities of heat-killed lactic acid bacteria isolates against Salmonella enterica serovar Typhimurium. Iran J Microbiol. 2024;16(6):763-772.
