with the collaboration of Iranian Food Science and Technology Association (IFSTA)

Document Type : Research Article

Authors

1 Department of Food Science, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran

2 Faculty of Science, University of Copenhagen, Denmark

Abstract

Introduction
Cronobacter sakazakii is an opportunistic pathogen, which has been linked to the contamination of powdered infant formula, and associated with outbreaks leading to fatalities in neonatal intensive care units. Few studies have explored the direct interaction between probiotics and C. sakazakii. In this study, the effect of a Lactiplantibacillus plantarum strain (M17) along with the standard strain Lactobacillus plantarum (ATCC 8014) and the well-characterized probiotic strain Lactobacillus rhamnosus GG on the adhesion of C. sakazakii to intestinal epithelial cells was analyzed.
 
Materials and Methods
Acid and bile tolerance of M17 was evaluated in the presence of pepsin and pancreatin. L-arginine hydrolysis was investigated using an arginine-including medium. Auto-aggregation and co-aggregation assays were performed by absorbance measurement. Minimum inhibitory concentrations of the antimicrobials recommended by the European Food Safety Authority were established. Total lactic acid and the ratio of D/L lactate isomers were determined with a Megazyme enzymatic kit. The ability of the isolate to produce biogenic amines was tested by qualitative and quantitative monitoring. Hemolysis was assessed phenotypically on MRS agar enriched with sheep blood. The strain was tested for its capability to adhere to mucin and Caco-2 cells. The antagonistic effects of the strain against C. sakazakii were further evaluated in vitro on mucin and cultured Caco-2 cells. The LAB strain was added simultaneously with, before, and after C. sakazakii to Caco-2 cells for competition, exclusion and displacement assays, respectively. Data analysis was performed in R using one-way analysis of variance, and the experimental groups were compared with the controls using Tukey’s test. P values <0.05 were considered statistically significant.
 
Results and Discussion
There was no significant difference in the survival rate of M17 and L. plantarum ATCC 8014 at pH = 4. After 2 h of incubation at pH = 2.5, the survival rate of L. plantarum ATCC 8014 was estimated to be higher than strain M17, but this difference was not significant. After 4 hours of incubation at pH = 8, M17 showed a higher survival rate than L. plantarum ATCC 8014, and this difference was significant after transfer from pH = 4. These results confirm the appropriate viability of M17 in the gastrointestinal tract. Both M17 and L. plantarum ATCC 8014 developed the color yellow in the L-arginine hydrolysis assay, which confirms the safety of these strains. The percentage of auto-aggregation for M17, L. plantarum ATCC 8014, and Lactobacillus rhamnosus LGG was estimated at 24.38, 25.28, and 32 after 6 hours, respectively, and no statistically significant difference between the two isolates were noticed. Given the auto-aggregation and co-aggregation parameters of M17, this strain may constitute a defense mechanism against C. sakazakii. Strain M17 showed resistance to kanamycin and clindamycin antibiotics. With intrinsic resistance, the risk of transferring resistance genes is not only speculative, but practically impossible. Intrinsic resistance of lactic acid bacteria may be considered desirable because it ensures their survival when the host is treated with antibiotics. Both D and L isomers of lactic acid were produced by the studied strains. In humans, D(-)-lactic acidosis is a rare metabolic complication that has only been reported in individuals with short bowel syndrome). Clinical studies have shown that the consumption of probiotic bacteria producing D(-)-lactic acid is safe for children and does not cause a long-term increase in blood D(-)-lactic acid. The reference L. plantarum strain and M17 did not produce biogenic amine precursors, and had no ß-hemolytic activity. Mucin adhesion assay exhibited that M17 has less adhesion (12.10 ± 1.14 %) than L. plantarum ATCC 8014 (13.33 ± 2.30 %) and LGG (15.93 ± 2.06 %) although these differences were not statistically significant. However, the amount of adhesion for the positive control sample Escherichia coli K12 (25.19 ± 4.40 %) was significantly higher than those of the other strains. Compared to the positive control, M17 had a significantly lower adhesion rate (6.8 ± 1.41) to CaCo-2 cells. This value was estimated at 13.77 ± 3.53 % for the reference strain and 21.6 ± 7.54 % for Lactobacillus fermentum PCC (positive control). In antagonistic assays, M17 was able to reduce the adhesion of C. sakazakii to mucin and CaCo-2 cells in all three methods of exclusion/inhibition, competition and displacement. Statistical analysis of the results does not show a significant difference between M17 and LGG. Therefore, the performance of M17 is similar to that of the standard probiotic LGG.
 
Conclusion
Lactic acid bacteria with acceptable ability to adhere to epithelial cells can be suitable for colonization in the intestine. They can act as a barrier to fight pathogens through various competitive mechanisms, such as co-aggregation with pathogens and adhesion. The M17 strain has an acceptable immune profile and probiotic properties because it shows an acceptable antagonistic activity against C. sakazakii invasion.
 
Acknowledgement
This study was supported by Ferdowsi University of Mashhad (Research affairs) [project No.:46718] and the research infrastructure at the University of Copenhagen.

Keywords

Main Subjects

©2023 The author(s). This is an open access article distributed under Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source.

  1. Abushelaibi, A., Al-Mahadin, S., El-Tarabily, K., Shah, N.P., & Ayyash, M. (2017). Characterization of potential probiotic lactic acid bacteria isolated from camel milk. LWT—Food Science and Technology, 79, 316–325. http://dx.doi.org/10.1016%2Fj.lwt.2017.01.041
  2. Agostoni, C., Axelsson, I., Goulet, O., Koletzko, B., Michaelsen, K.F., Puntis, J.W.L., Rigo, J., Shamir, R., Szajewska, H., Turck, D., Vandenplas, Y., & Weaver, L.T. (2004). Preparation and handling of powdered infant formula: a commentary by the ESPGHAN committee on nutrition. Journal of Pediatric Gastroenterology and Nutrition, 39, 320–322. https://doi.org/10.1097/00005176-200410000-00002
  3. Arboleya, S., González, S., Salazar, N., Ruas-Madiedo, P., de los Reyes-Gavilán, C.G., & Gueimonde, M. (2012). Development of probiotic products for nutritional requirements of specific human populations. Engineering in Life Sciences, 12, 368–376. https://doi.org/10.1002%2Felsc.201100129
  4. Aristoy, M.C., & Toldrá, F. (2012). Essential Amino Acids. Handbook of analysis of active compounds in functional foods. Boca Raton: CRC press.
  5. Azizi, F., Habibi Najafi, M.B., & Edalatian Dovom, M.R. (2017). The biodiversity of Lactobacillus from Iranian raw milk Motal cheese and antibacterial evaluation based on bacteriocin-encoding genes. AMB Expr, 7, 176. https://doi.org/10.1186/s13568-017-0474-2
  6. Bacha, K., Mehari, T., & Ashenafi, M. (2010). Antimicrobial susceptibility patterns of LAB isolated from Wakalim, a traditional Ethiopian fermented sausage. Journal of Food Safety, 30, 213–223. http://dx.doi.org/10.1111/j.1745-4565.2009.00201.x
  7. Barrett, K.E., Barman, S.M., Boitano, S., & Brooks, H.L. (Eds.).(2018). Ganong’s Review of Medical Physiology, 25e. McGraw Hill.
  8. Bassyouni, R.H., Abdel-All, W. S., Fadl, M.G., Abdel-All, S., & Kamel, Z. (2012). Characterization of lactic acid bacteria isolated from dairy products in Egypt as a probiotic. Life Science Journal, 9, 2924–2933.
  9. Bengoa, A.A., Zavala, L., Carasi, P., Trejo, S.A., Bronsoms, S., Serradell, M.L.Á., Garrote, G.L., & Abraham, A.G. (2018). Simulated gastrointestinal conditions increase adhesion ability of Lactobacillus paracasei strains isolated from kefir to Caco-2 cells and mucin. Food Research International, 103, 462-467. https://doi.org/10.1016/j.foodres.2017.09.093
  10. Blackburn, S. (2016). Maternal, Fetal, & Neonatal Physiology: A Clinical Perspective. Saunders Elsevier.
  11. Botes, M., Van Reenen, C.A., L. & Dicks, M.T. (2008). Evaluation of Enterococcus mundtii ST4SA and Lactobacillus plantarum 423 as probiotics by using a gastrointestinal model with infant milk formulations as substrate. International Journal of Food Microbiology, 128, 362–370. https://doi.org/10.1016/j.ijfoodmicro.2008.09.016
  12. Bover-Cid, S., & Holzapfel, W.H. (1999). Improved screening procedure for biogenic amine production by lactic acid bacteria. International Journal of Food Microbiology, 53, 33–41. https://doi.org/10.1016/s0168-1605(99)00152-x
  13. Bowen, A.B., & Braden, C.R. (2006). Invasive Enterobacter sakazakii disease in infants. Emerging Infectious Diseases, 12, 1185-1189. http://dx.doi.org/10.3201/eid1208.051509
  14. Briske-Anderson, M.J., Finley, J.W., & Newman, S.M. (1997). The influence of culture time and passage number on the morphological and physiological development of Caco-2 cells. Society for Experimental Biology and Medicine, 214(3). https://doi.org/10.3181/00379727-214-44093
  15. Byakika, S., Mukisa, I.M., Byenkya, Y., & Muyanja, C. (2020). Probiotic potential of lactic acid starter cultures isolated from a traditional fermented sorghum-millet beverage. International Journal of Microbiology, https://doi.org/10.1155/2020/7825943
  16. Caballero-Franco, C., Keller, K., De Simone, C., & Chadee K. (2007). The VSL#3 probiotic formula induces mucin gene expression and secretion in colonic epithelial cells. American Journal of Physiology-Gastrointestinal and Liver Physiology, 292, 315–322. https://doi.org/10.1152/ajpgi.00265.2006
  17. Campana, R., van Hemert, S., & Baffone, W. (2017). Strain‑specific probiotic properties of lactic acid bacteria and their interference with human intestinal pathogens invasion. Gut Pathogens, 9, 12. https://doi.org/10.1186/s13099-017-0162-4
  18. Cekola, P.L., Czerkies, L.A., Storm, H.M., Wang, M.H., Roberts, J., & Saavedra, J.M. (2015). Growth and tolerance of term infants fed formula with probiotic Lactobacillus reuteri. Clinical Pediatrics, 54(12), 1175-84. https://doi.org/10.1177/0009922815574076
  19. Charchoghlyan, H., Kwon, H., Hwang, D.J., Lee, J.S., Lee, J., & Kim, M. (2016). Inhibition of Cronobacter sakazakii by Lactobacillus acidophilusv. Er2 317/402. Korean Journal for Food Science of Animal Resources, 36(5), 635-640. https://doi.org/10.5851%2Fkosfa.2016.36.5.635
  20. Chou L.S., & Weimer, B. (1999). Isolation and characterization of acid- and bile-tolerant isolates from strains of Lactobacillus acidophilus. Journal of Dairy Science, 82, 23–31. https://doi.org/10.3168/jds.s0022-0302(99)75204-5
  21. CODEX Alimentarius Commission. (2008). Cac/rcp 66-2008 Code of Hygienic Practice for Powdered Infant Formula for Infants and Young Children. Joint FAO/WHO food standards programme. Food and Agriculture Organization of the United Nations, Rome, Italy.
  22. Collado, M.C., Isolauri, E., & Salminen, S. (2008a). Specific probiotic strains and their combinations counteract adhesion of Enterobacter sakazakii to intestinal mucus. FEMS Microbiology Letters, 285, 58–64. https://doi.org/10.1111/j.1574-6968.2008.01211.x
  23. Collado, M.C., Meriluoto, J., & Salminen, S. (2007). Role of commercial probiotic strains against human pathogen adhesion to intestinal mucus. Letters in Applied Microbiology, 45(4), 454-60. https://doi.org/10.1111/j.1472-765x.2007.02212.x
  24. Collado, M.C., Meriluoto, J., & Salminen, S. (2008b). Adhesion and aggregation properties of probiotic and pathogen strains. European Food Researchand Technology, 226, 1065–1073. https://doi.org/10.1007/s00217-007-0632-x
  25. de Carvalho, K.G., Kruger, M.F., Furtado, D.N., Todorov, S.D., & de Melo Franco, B.D.G. (2009). Evaluation of the role of environmental factors in the human gastrointestinal tract on the behaviour of probiotic cultures of Lactobacillus casei Shirota and Lactobacillus casei LC01 by the use of a semi-dynamic in vitro Annals of Microbiology, 59(3), 439-445. https://doi.org/10.1007/BF03175128
  26. Del Re, B., Sgorbati, B., Miglioli, M., & Palenzona, D. (2000). Adhesion, autoaggregation and hydrophobicity of 13 strains of Bifidobacterium longum. Letters in Applied Microbiology, 31, 438-442. https://doi.org/10.1046/j.1365-2672.2000.00845.x
  27. Drudy, D., Mullane, N.R., Quinn, T., Wall, P.G., & Fanning, S. (2006). Enterobacter sakazakii: An emerging Pathogen in Powdered Infant Formula. Clinical Infectious Diseases, 42, 996–1002. https://doi.org/10.1086/501019
  28. Erickson, T., Ahrens, W.R., Aks, S., Baum, C., & Ling, L. (2005). Pediatric Toxicology: Diagnosis and Management of the Poisoned Child. New York: McGraw-Hill.
  29. Erkkilä, S., Petäjä, E., Eerola, S., Lilleberg, L., Mattila-Sandholm, T., & Suihko, M.L. (2001). Flavour profiles of dry sausages fermented by selected novel meat starter cultures. Meat Science, 58, 111–116. https://doi.org/10.1016/s0309-1740(00)00135-2
  30. European Food Safety Authority. (2008). Technical guidance prepared by the panel on additives and products or substances used in animal feed (FEEDAP) on the update of the criteria used in the assessment of bacterial resistance to antimicrobials of human or veterinary importance. EFSA Journal, 732, 1–15. https://doi.org/10.2903/j.efsa.2008.732
  31. Ewaschuk, J.B., Naylor, J.M., & Zello, G.A. (2005). D-lactate in human and ruminant metabolism. The Journal of Nutrition, 135(7), 1619-25. https://doi.org/10.1093/jn/135.7.1619
  32. (2007). Enterobacter sakazakii and other microorganisms in powdered infant formula. Food and Agriculture Organization of the United Nations, Rome, Italy.
  33. FAO/WHO. (2001). Evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Report on joint FAO/WHO expert consultation, Córdoba, Argentina.
    http://www.who.int/foodsafety/publications/fs_management/en/probiotics.pdf?ua=1
  34. FAO/WHO. (2006a). Expert meeting on Enterobacter sakazakii and Salmonella in powdered infant Food and agriculture organization of the United Nations, Rome, Italy.
  35. FAO/WHO. (2006b). Probiotics in food; Health and nutritional properties and guidelines for evaluation. Rome, Italy.
  36. Farmer, J.J., Asbury, M.A., Hickman, F.W., & Brenner, D.J. (1980). The Enterobacteriaceae study group Enterobacter sakazakii: A New Species of “Enterobacteriaceae” Isolated from Clinical Specimens. International Journal of Systematic Bacteriology, 30, 569-584. https://doi.org/10.1099/00207713-30-3-569
  37. Fontana, L., Bermudez-Brito, M., Plaza-Diaz, J., Muñoz-Quezada, S., & Gil, A. (2013). Sources, isolation, characterisation and evaluation of probiotics. British Journal of Nutrition, 109, 35–50. https://doi.org/10.1017/s0007114512004011
  38. Food Safety Authority of Ireland. (2011). Guidance Note No. 18: Validation of Product Shelf-Life (Revision 1); Dublin, Ireland.
  39. Grady Jr, C.L., Daigger, G.T., Love, N.G., & Filipe, C.D. (2011). Biological Wastewater Treatment, CRC Press, Boca Raton, FL, USA. https://doi.org/10.1201/b13775
  40. Grodner, M., Escott-Stump, S., & Dorner, S. (2021). Nutritional Foundations and Clinical Applications A Nursing Approach.
  41. Guarner, F., & Schaafsma, G.J. (1998). Probiotics. International Journal of Food Microbiology, 39, 237-238. https://doi.org/10.1016/s0168-1605(97)00136-0
  42. Gurtler, J.B., Kornacki, J.L., & Beuchat, L.R. (2005). Enterobacter sakazakii: A coliform of increased concern to infant health. International Journal of Food Microbiology, 104, 1–34. https://doi.org/10.1016/j.ijfoodmicro.2005.02.013
  43. Holý, O., & Forsythe, S. (2014). Cronobacter as emerging causes of healthcare-associated infection. Journal of Hospital Infection, 86, 169-177. https://doi.org/10.1016/j.jhin.2013.09.011
  44. Hummel, A.S., Hertel, C., Holzapfel, W.H., & Franz, C.M.A.P. (2007). Antibiotic resistances of starter and probiotic strains of lactic acid bacteria. Applied and Environmental Microbiology, 73, 730–739. https://doi.org/10.1128/aem.02105-06
  45. Hunter, C.J., Williams, M., Petrosyan, M., Guner, Y., Mittal, R., Mock, D., Upperman, J.S., Ford, H.R., & Prasadarao, N.V. (2009). Lactobacillus bulgaricus prevents intestinal epithelial cell injury caused by Enterobacter sakazakii-induced nitric oxide both in vitro and in the newborn rat model of necrotizing enterocolitis. Infection and Immunity, 77(3), 1031-1043. https://doi.org/10.1128/iai.01192-08
  46. Iranian National Standard No. 19459. (2014). Probiotic microorganisms specifications and test methods. Iranian Standards and Industrial Research Institute, Tehran.
  47. Jose, N., Bunt, C., & Hussain, M. (2015). Comparison of microbiological and probiotic characteristics of lactobacilli isolates from dairy food products and animal rumen contents. Microorganisms, 3, 198–212. https://doi.org/10.3390/microorganisms3020198
  48. Kaktcham, N.F., Zambou, F.M., El-Soda, T.M., & Choudhary, M.I. (2012). Antimicrobial and safety properties of lactobacilli isolated from two Cameroonian traditional fermented foods. Scientia Pharmaceutica, 80, 189–203. https://doi.org/10.3797/scipharm.1107-12
  49. Kent, R.M., Fitzgerald, G.F., Hill, C., Stanton, C., & Ross, R.P. (2015). Novel approaches to improve the intrinsic microbiological safety of powdered infant milk formula. Nutrients, 7, 1217-1244. https://doi.org/10.3390%2Fnu7021217
  50. Kos, B., Suskovic, J., Goreta, J., & Matosic, S. (2000). Effect of protectors on the viability of Lactobacillus acidophilus M92 in simulated gastrointestinal conditions. Food Technologyand Biotechnology, 38, 121-127.
  51. Lai, K.K. (2001). Enterobacter sakazakii infections among neonates, infants, children and adults. Medicine, 80, 113-122. https://doi.org/10.1097/00005792-200103000-00004
  52. Lee, Y.K., & Puong, K.Y. (2002). Competition for adhesion between probiotics and human gastrointestinal pathogens in presence of carbohydrate. British Journal of Nutrition, 88, 101–108. https://doi.org/10.1079/bjn2002635
  53. Li, Q., Liu, X., Dong, M., Zhou, J., & Wang, Y. (2015). Aggregation and adhesion abilities of 18 lactic acid bacteria strains isolated from traditional fermented food. International Journal of Agricultural Policy and Research, 3, 84–92.
  54. Liong, M.T., & Shah N.P. (2005). Acid and bile tolerance and cholesterol removal ability of lactobacilli strains. Journal of Dairy Science, 88, 55–66. https://doi.org/10.3168/jds.s0022-0302(05)72662-x
  55. Liu, W., Chen, M., & Duo, L. (2020). Characterization of potentially probiotic lactic acid bacteria and bifidobacteria isolated from human colostrum. Journal of Dairy Science, 103, 4013–4025. https://doi.org/10.3168/jds.2019-17602
  56. Mathara, J., Schillinger, U., & Guigas, C. (2008). Functional characteristics of Lactobacillus from traditional Maasai fermented milk products in Kenya. International Journal of Food Microbiology, 126, 57–64. https://doi.org/10.1016/j.ijfoodmicro.2008.04.027
  57. Mathur, S., & Singh, R. (2005). Antibiotic resistance in food lactic acid bacteria-a review. International Journal of Food Microbiology, 105, 281–295. https://doi.org/10.1016/j.ijfoodmicro.2005.03.008
  58. Mohan Nair, M.K., Venkitanarayanan, K., Silbart, L.K., & Kim, K.S. (2009). Outer Membrane Protein A (OmpA) of Cronobacter sakazakii Binds Fibronectin and Contributes to Invasion of Human Brain Microvascular Endothelial Cells. Foodborne Pathogens and Disease, 6(4), 495-501. https://doi.org/10.1089/fpd.2008.0228
  59. Møller, C.O.A., Ücok, E.F., & Rattray, F.P. (2020). Histamine forming behaviour of bacterial isolates from aged cheese. Food Research International128, 108719. https://doi.org/10.1016/j.foodres.2019.108719
  60. Muñoz-Quezada, S., Chenoll, E., Vieites, J.M., Genovés, S., Maldonado, J., Bermúdez-Brito, M., Gomez-Llorente, C., Matencio, E., Bernal, M.J., Romero, F., Suárez, A., Ramón, D., & Gil, A. (2013). Isolation, identification and characterisation of three novel probiotic strains (Lactobacillus paracasei CNCM I-4034, Bifidobacterium breve CNCM I-4035 and Lactobacillus rhamnosus CNCM I-4036) from the faeces of exclusively breast-fed infants. British Journal of Nutrition, 109, S51–S62. https://doi.org/10.1017/s0007114512005211
  61. Nazarowec-White, M., & Farber, J.M. (1997). Enterobacter sakazakii: A review. International Journal of Food Microbiology, 34, 103-113. https://doi.org/10.1016/s0168-1605(96)01172-5
  62. Olasupo, N.A., Schillinger, U., & Holzapfel, W.H. (2001). Studies on some technological properties of predominant lactic acid bacteria isolated from Nigerian fermented foods. Food Biotechnology, 15(3), 157-167. http://dx.doi.org/10.1081/FBT-100107627
  63. Özogul, F., & Özogul, Y. (2007). The ability of biogenic amines and ammonia production by single bacterial cultures. European Food Research and Technology, 225, 385-394. http://dx.doi.org/10.1007/s00217-006-0429-3
  64. Pagotto, F.J., & Farber, J.M. (2009). Cronobacter (Enterobacter sakazakii): Advice, policy and research in Canada. International Journal of Food Microbiology, 136, 238-245. https://doi.org/10.1016/j.ijfoodmicro.2009.05.010
  65. Papagaroufalis, K., Fotiou, A., Egli, D., Tran, L.A., & Steenhout, P. (2014). A randomized double blind controlled safety trial evaluating D-lactic acid production in healthy infants fed a Lactobacillus reuteri-containing formula. Nutrition and Metabolic Insights, 7, 19-27. https://doi.org/10.4137/nmi.s14113
  66. Papamanoli, E., Tzanetakis, N., Litopoulou-Tzanetaki, E., & Kotzekidou, P. (2003). Characterization of lactic acid bacteria isolated from a Greek dry-fermented sausage in respect of their technological and probiotic properties. Meat Science, 65, 859–867. https://doi.org/10.1016/s0309-1740(02)00292-9
  67. Pereira, C.I., Barreto Crespo, M.T. & San Romao, M.V. (2001). Evidence for proteolytic activity and biogenic amines production in Lactobacillus curvatus and homohiochii. International Journal of Food Microbiology, 68, 211–216. https://doi.org/10.1016/s0168-1605(01)00534-7
  68. Pérez Martínez, G., Bäuerl, C., & Amores, M.C.C. (2012). Selection and evaluation of probiotics. In L. M. L. Nollet and F. Toldrá eds. Handbook of analysis of active compounds in functional foods. CRC Press; Taylor & Francis Group.
  69. Pesavento, G., Calonico, C., Ducci, B., Magnanini, A., & Lo Nostro, A. (2014). Prevalence and antibiotic resistance of Enterococcus isolated from retail cheese, ready-to-eat salads, ham, and raw meat. Food Microbiology, 41, 1-7. https://doi.org/10.1016/j.fm.2014.01.008
  70. Pianpumepong, P. & Noomhorm, A. (2010). Isolation of probiotic bacteria from turmeric (Curcuma longa) and its application in enriched beverages. International Journal of Food Science and Technology, 45, 2456–2462. http://dx.doi.org/10.1111/j.1365-2621.2010.02337.x
  71. Połka, J., Morelli, L., & Patrone, V. (2016). Microbiological cutoff values: A critical issue in phenotypic antibiotic resistance assessment of Lactobacilli and Bifidobacteria. Microbial Drug Resistance, 24, 345-370. https://doi.org/10.1089/mdr.2015.0328
  72. Priyadarshani, W.M.D., & Rakshit, S.K. (2011). Screening selected strains of probiotic lactic acid bacteria for their ability to produce biogenic amines (histamine and tyramine). International Journal of Food Science & Technology, 46, 2062–2069. http://dx.doi.org/10.1111/j.1365-2621.2011.02717.x
  73. Radulović, Z., Petrović, T., & Bulajić, S. (2012). Antibiotic susceptibility of probiotic bacteria. http://cdn.intechopen.com/pdfs/34710/InTechAntibiotic_susceptibility_of_probiotic_bacteria.pdf
  74. Redruello, B., Ladero, V., Cuesta, I., Álvarez-Buylla, J.R., Martín, M.C., Fernández, M., & Alvarez, M.A. (2013). A fast, reliable, ultra high performance liquid chromatography method for the simultaneous determination of amino acids, biogenic amines and ammonium ions in cheese, using diethyl ethoxymethylenemalonate as a derivatising agent. Food Chemistry, 139(1-4), 1029-35. https://doi.org/10.1016/j.foodchem.2013.01.071
  75. Reid, G., McGroarty, J.A., Angotti, R., & Cook, R.L. (1988). Lactobacillus inhibitor production against Escherichia coli and coaggregation ability with uropathogens. Canadian Journal of Microbiology, 34, 344–351. https://doi.org/10.1139/m88-063
  76. Ruiz-Moyano, S., Martín, A., Benito, M.J., Casquete, R., Serradilla, M.J., & Córdoba, M.d.G. (2009). Safety and functional aspects of pre-selected lactobacilli for probiotic use in Iberian dry-fermented sausages. Meat Science, 83, 460–467. https://doi.org/10.1016/j.meatsci.2009.06.027
  77. Sherman, P.M., Johnson-Henry, K.C., Yeung, H.P., Ngo, P.S.C., Goulet, J., & Tompkins, T.A. (2005). Probiotics reduce enterohemorrhagic Escherichia coli O157:H7- and enteropathogenic E. coli O127:H6-induced changes in polarized T84 epithelial cell monolayers by reducing bacterial adhesion and cytoskeletal rearrangements. Infection and Immunity, 73, 5183–5188. https://doi.org/10.1128/iai.73.8.5183-5188.2005
  78. Singhal, K., Joshi, H., & Chaudhary B.L. (2010). Bile and acid tolerance ability of probiotic Lactobacillus Journal of Global Pharma Technology, 2, 17–25.
  79. Srimahaeak, T., Bianchi, F., Chlumsky, O., Larsen, N., & Jespersen, L. (2021). In-vitro study of Limosilactobacillus fermentum PCC adhesion to and integrity of the Caco-2 cell monolayers as affected by pectins. Journal of Functional Foods, 79. https://doi.org/104395.10.1016/j.jff.2021.104395
  80. Tomás, M.S.J., Wiese, B., & Nader-Macías, M.E. (2005). Effects of culture conditions on the growth and auto-aggregation ability of vaginal Lactobacillus johnsonii CRL 1294. Journal of Applied Microbiology, 99, 1383–1391. https://doi.org/10.1111/j.1365-2672.2005.02726.x
  81. Tomáška, M., Drončovský, M., Klapáčová, L., Slottová, A., & Kološta, M. (2015). Potential probiotic properties of Lactobacilli isolated from goat´s milk.Potravinarstvo Slovak Journal of Food Sciences9(1), 66–71. https://doi.org/10.5219/434
  82. Veerappan, G.R., Betteridge, J., & Young, P.E. (2012). Probiotics for the treatment of inflammatory bowel disease. Current Gastroenterology Reports, 14, 324–333. https://doi.org/10.1007/s11894-012-0265-5

Vitetta, L., Coulson, S., Thomsen, M., Nguyen, T., & Hall, S. (2017). Probiotics, D-Lactic acidosis, oxidative stress and strain specificity. Gut Microbes, 4, 311-322. https://doi.org/10.1080/19490976.2017.1279379

CAPTCHA Image