The Influence of Probiotic Lactobacillus casei in Combination with Prebiotic Inulin on the Antioxidant Capacity of Human Plasma

Oxidative Medicine and Cellular Longevity

Volumn 2016, Issue , 2016, Pages

  Kleniewska, Paulina ^a   Hoffmann, Arkadiusz ^a   Pniewska, Ewa ^a   Pawliczak, Rafal ^a  

^a MEDICAL UNIVERSITY OF LODZ   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANTS; ENZYMES; OXYGEN; PLASMA (HUMAN);

ANTIOXIDANT CAPACITY; ANTIOXIDANT PROPERTIES; FERRIC REDUCING ABILITY OF PLASMAS; GLUTATHIONE PEROXIDASE; LACTOBACILLUS CASEI; PROBIOTIC BACTERIA; PROBIOTIC LACTOBACILLI; SUPEROXIDE DISMUTASES;

POLYSACCHARIDES;

CATALASE; GLUTATHIONE PEROXIDASE; INULIN; LACTOBACILLUS CASEI EXTRACT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SUPEROXIDE DISMUTASE; ANTIOXIDANT; FERRIC ION; PREBIOTIC AGENT; PROBIOTIC AGENT; SYNBIOTIC AGENT;

ANTIOXIDANT ACTIVITY; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DIET SUPPLEMENTATION; ENZYME ACTIVITY; FEMALE; HUMAN; LACTOBACILLUS CASEI; MALE; NONHUMAN; OXIDATION; PLASMA; RANDOMIZED CONTROLLED TRIAL; ADULT; BLOOD; CHEMISTRY; CONTROLLED CLINICAL TRIAL; DIETARY SUPPLEMENT; METABOLISM; PHYSIOLOGY; UPREGULATION;

ADULT; ANTIOXIDANTS; CATALASE; DIETARY SUPPLEMENTS; FEMALE; FERRIC COMPOUNDS; GLUTATHIONE PEROXIDASE; HUMANS; INULIN; LACTOBACILLUS CASEI; MALE; PREBIOTICS; PROBIOTICS; SUPEROXIDE DISMUTASE; SYNBIOTICS; UP-REGULATION;

EID: 84962815630     PISSN: 19420900     EISSN: 19420994     Source Type: Journal    
DOI: 10.1155/2016/1340903     Document Type: Article

References (86)

1. P. D. Ray, B.-W. Huang, and Y. Tsuji, "Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling, " Cellular Signalling, vol. 24, no. 5, pp. 981-990, 2012.
2. J. E. Klaunig, Z. Wang, X. Pu, and S. Zhou, "Oxidative stress and oxidative damage in chemical carcinogenesis, " Toxicology and Applied Pharmacology, vol. 254, no. 2, pp. 86-99, 2011.
3. M. Valko, C. J. Rhodes, J. Moncol, M. Izakovic, and M. Mazur, "Free radicals, metals and antioxidants in oxidative stressinduced cancer, " Chemico-Biological Interactions, vol. 160, no. 1, pp. 1-40, 2006.
4. P. Song and M. H. Zou, "Roles of reactive oxygen species in physiology and pathology, " in Atherosclerosis: Risks, Mechanisms, andTherapies, H. Wang and C. Patterson, Eds., pp. 379-392, JohnWiley & Sons, Hoboken, NJ, USA, 2015.
5. K. Apel and H. Hirt, "Reactive oxygen species: metabolism, oxidative stress, and signal transduction, " Annual Review of Plant Biology, vol. 55, pp. 373-399, 2004.
6. T. Fukai and M. Ushio-Fukai, "Superoxide dismutases: role in redox signaling, vascular function, and diseases, " Antioxidants and Redox Signaling, vol. 15, no. 6, pp. 1583-1606, 2011.
7. I. N. Zelko, T. J. Mariani, and R. J. Folz, "Superoxide dismutase multigene family: a comparison of theCuZn-SOD(SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression, " Free Radical Biology and Medicine, vol. 33, no. 3, pp. 337-349, 2002.
8. S. Chen, P. Sayana, X. Zhang, and W. Le, "Genetics of amyotrophic lateral sclerosis: an update, "Molecular Neurodegeneration, vol. 28, no. 8, pp. 1-15, 2013.
9. S. Miriyala, I. Spasojevic, A. Tovmasyan et al., "Manganese superoxide dismutase, MnSOD and its mimics, " Biochimica et Biophysica Acta (BBA)-Molecular Basis of Disease, vol. 1822, no. 5, pp. 794-814, 2012.
10. C. D. Putnam, A. S. Arvai, Y. Bourne, and J. A. Tainer, "Active and inhibited human catalase structures: ligand and NADPH binding and catalyticmechanism, " Journal ofMolecular Biology, vol. 296, no. 1, pp. 295-309, 2000.
11. P. Chelikani, I. Fita, and P. C. Loewen, "Diversity of structures and properties among catalases, " Cellular and Molecular Life Sciences, vol. 61, no. 2, pp. 192-208, 2004.
12. R. Francik, M. Krósniak, I. Sanocka, H. Bartón, T. Hebda, and S. Francik, "Aronia melanocarpa treatment and antioxidant status in selected tissues inwistar rats, " BioMed Research International, vol. 2014, Article ID457085, 9 pages, 2014.
13. E. Lubos, J. Loscalzo, andD. E. Handy, "Glutathioneperoxidase-1 in health and disease: from molecular mechanisms to therapeutic opportunities, " Antioxidants and Redox Signaling, vol. 15, no. 7, pp. 1957-1997, 2011.
14. G. R. Gibson and M. B. Roberfroid, "Dietary modulation of the human colonic microbiota. Introducing the concept of prebiotics, " Journal of Nutrition, vol. 125, no. 6, pp. 1401-1412, 1995.
15. B. Poljsak, "Strategies for reducing or preventing the generation of oxidative stress, " Oxidative Medicine and Cellular Longevity, vol. 2011, Article ID 194586, 15 pages, 2011.
16. B. M. Hybertson, B. Gao, S. K. Bose, and J. M. McCord, "Oxidative stress in health and disease: the therapeutic potential ofNrf2 activation, "Molecular Aspects ofMedicine, vol. 32, no. 4-6, pp. 234-246, 2011.
17. I. F. F. Benzie and J. J. Strain, "The ferric reducing ability of plasma (FRAP) as a measure of 'antioxidant power': the FRAP assay, " Analytical Biochemistry, vol. 239, no. 1, pp. 70-76, 1996.
18. https://www.caymanchem.com/pdfs/707002.pdf.
19. https://www.caymanchem.com/pdfs/706002.pdf.
20. https://www.caymanchem.com/pdfs/703102.pdf.
21. D. Martarelli, M. C. Verdenelli, S. Scuri et al., "Effect of a probiotic intake on oxidant and antioxidant parameters in plasma of athletes during intense exercise training, " Current Microbiology, vol. 62, no. 6, pp. 1689-1696, 2011.
22. H. An, H. Zhou, Y. Huang et al., "High-level expression of heme-dependent catalase gene katA from Lactobacillus sakei protects Lactobacillus rhamnosus from oxidative stress, " Molecular Biotechnology, vol. 45, no. 2, pp. 155-160, 2010.
23. P. Hütt, H.,reson, T. Kullisaar et al., "Effects of a synbiotic product on blood antioxidative activity in subjects colonized with Helicobacter pylori, " Letters in Applied Microbiology, vol. 48, no. 6, pp. 797-800, 2009.
24. T. Kullisaar, E. Songisepp, M. Mikelsaar, K. Zilmer, T. Vihalemm, and M. Zilmer, "Antioxidative probiotic fermented goats' milk decreases oxidative stress-mediated atherogenicity in human subjects, " British Journal of Nutrition, vol. 90, no. 2, pp. 449-456, 2003.
25. M. Mikelsaar and M. Zilmer, "Lactobacillus fermentum ME-3-an antimicrobial and antioxidative probiotic, " Microbial Ecology in Health and Disease, vol. 21, no. 1, pp. 1-27, 2009.
26. E. Songisepp, J. Kals, T. Kullisaar et al., "Evaluation of the functional efficacy of an antioxidative probiotic in healthy volunteers, " Nutrition Journal, vol. 4, article 22, 2005.
27. M. A. Uskova and L. V. Kravchenko, "Antioxidant properties of lactic acid bacteria-probiotic and yogurt strains, " Voprosy Pitaniia, vol. 78, no. 2, pp. 18-23, 2009.
28. A. Amaretti, M. di Nunzio, A. Pompei, S. Raimondi, M. Rossi, andA. Bordoni, "Antioxidant properties of potentially probiotic bacteria: in vitro and in vivo activities, " Applied Microbiology and Biotechnology, vol. 97, no. 2, pp. 809-817, 2013.
29. A. S. Hathout, S. R. Mohamed, A. A. El-Nekeety, N. S. Hassan, S. E. Aly, andM. A. Abdel-Wahhab, "Ability of Lactobacillus casei and Lactobacillus reuteri to protect against oxidative stress in rats fed aflatoxins-contaminated diet, " Toxicon, vol. 58, no. 2, pp. 179-186, 2011.
30. M. Gagnon, P. Savard, A. Rivière, G. Lapointe, and D. Roy, "Bioaccessible antioxidants in milk fermented by Bifidobacterium longum subsp. longum strains, " BioMed Research International, vol. 2015, Article ID 169381, 12 pages, 2015.
31. Q. Shen, N. Shang, and P. Li, "In vitro and in vivo antioxidant activity of bifidobacterium animalis 01 isolated from centenarians, " Current Microbiology, vol. 62, no. 4, pp. 1097-1103, 2011.
32. M. Chamari, A. Djazayery, M. Jalali, H. Sadrzadeh Yeganeh, S. Hosseini, and R. Heshmat, "The effect of daily consumption of probiotic and conventional yogurt on some oxidative stress factors in plasma of young healthy women, " ARYA Atherosclerosis Journal, vol. 4, no. 4, pp. 175-179, 2008.
33. X. Shen, D. Yi, X. Ni et al., "Effects of lactobacillus plantarumon production performance, immune characteristics, antioxidant status, and intestinal microflora of bursin-immunized broilers, " Canadian Journal of Microbiology, vol. 60, no. 4, pp. 193-202, 2014.
34. H. Yadav, S. Jain, and P. R. Sinha, "Oral administration of dahi containing probiotic Lactobacillus acidophilus and Lactobacillus casei delayed the progression of streptozotocin-induced diabetes in rats, " Journal of Dairy Research, vol. 75, no. 2, pp. 189-195, 2008.
35. S. Rajpal and V. K. Kansal, "Probiotic Dahi containing Lactobacillus acidophilus and Bifidobacterium bifidum stimulates antioxidant enzyme pathways in rats, " Milchwissenschaft, vol. 64, no. 3, pp. 287-290, 2009.
36. T. Balog, S. Sobocanec, V. Sverko et al., "The influence of season on oxidant-antioxidant status in trained and sedentary subjects, " Life Sciences, vol. 78, no. 13, pp. 1441-1447, 2006.
37. J. Kodydková, L. Vávrová, M. Koćk, and A. Z ák, "Human catalase, its polymorphisms regulation and changes of its activity in different diseases, " Folia Biologica, vol. 60, no. 4, pp. 153-167, 2014.
38. L. Rönnberg, A. Kauppila, J. Leppäluoto, H. Martikainen, and O. Vakkuri, "Circadian and seasonal variation in human preovulatory follicular fluid melatonin concentration, " Journal of Clinical Endocrinology andMetabolism, vol. 71, no. 2, pp. 493-496, 1990.
39. Y. Ito, T. Iida, Y. Yamamura et al., "Relationships between salivary melatonin levels, quality of sleep, and stress in young Japanese females, " International Journal of Tryptophan Research, vol. 6, supplement 1, pp. 75-85, 2013.
40. J. Schröder, M. Dören, B. Schneider, and M. Oettel, "Are the antioxidative effects of 17-estradiol modified by concomitant administration of a progestin" Maturitas, vol. 25, no. 2, pp. 133-139, 1996.
41. L. Góth, Lenkey A, andW. N. Bigler, "Blood catalase deficiency and diabetes in Hungary, " Diabetes Care, vol. 24, no. 10, pp. 1839-1840, 2001.
42. N. Niikawa, Y. Fukushima, N. Taniguchi, S. Iizuka, and T. Kajii, "Chromosome abnormalities involving 11p13 and low erythrocyte catalase activity, " Human Genetics, vol. 60, no. 4, pp. 373-375, 1982.
43. R. A. Omar, Y.-J. Chyan, A. C.,orn, B. Poeggeler, N. K. Robakis, andM. A. Pappolla, "Increased expression but reduced activity of antioxidant enzymes in Alzheimer's disease, " Journal of Alzheimer's Disease, vol. 1, no. 3, pp. 139-145, 1999.
44. D. Gao, Z. Gao, andG. Zhu, "Antioxidant effects of Lactobacillus plantarum via activation of transcription factor Nrf2, " Food and Function, vol. 4, no. 6, pp. 982-989, 2013.
45. A. N. Wang, X. W. Yi, H. F. Yu, B. Dong, and S. Y. Qiao, "Free radical scavenging activity of Lactobacillus fermentum in vitro and its antioxidative effect on growing-finishing pigs, " Journal of Applied Microbiology, vol. 107, no. 4, pp. 1140-1148, 2009.
46. H. S. Ejtahed, J. Mohtadi-Nia, A. Homayouni-Rad, M. Niafar, M. Asghari-Jafarabadi, and V. Mofid, "Probiotic yogurt improves antioxidant status in type 2 diabetic patients, " Nutrition, vol. 28, no. 5, pp. 539-543, 2012.
47. F. Gan, X. Chen, S. F. Liao et al., "Selenium-enriched probiotics improve antioxidant status, immune function, and selenoprotein gene expression of piglets raised under high ambient temperature, " Journal of Agricultural and Food Chemistry, vol. 62, no. 20, pp. 4502-4508, 2014.
48. S. Pandey, A. Singh, P. Kumar, A. Chaudhari, andG. Nareshkumar, "Probiotic Escherichia coli CFR 16 producing pyrroloquinoline quinone (PQQ) ameliorates 1, 2-dimethylhydrazineinduced oxidative damage in colon and liver of rats, " Applied Biochemistry and Biotechnology, vol. 173, no. 3, pp. 775-786, 2014.
49. M. A. Ghoneim and S. S. Moselhy, "Antioxidant status and hormonal profile reflected by experimental feeding of probiotics, " Toxicology and Industrial Health, 2013.
50. S. Kapila, R. Kapila, S. Reddi, and P. R. Sinha, "Oral administration of probiotic Lactobacillus casei spp. casei ameliorates oxidative stress in rats, " International Journal of CurrentMicrobiology and Applied Sciences, vol. 3, no. 9, pp. 670-684, 2014.
51. E. Fabian and I. Elmadfa, "The effect of daily consumption of probiotic and conventional yoghurt on oxidant and antioxidant parameters in plasma of young healthy women, " International Journal for Vitamin and Nutrition Research, vol. 77, no. 2, pp. 79-88, 2007.
52. E. Vaghef-Mehrabany, A. Homayouni-Rad, B. Alipour, S. K. Sharif, L. Vaghef-Mehrabany, and S. Alipour-Ajiry, "Effects of probiotic supplementation on oxidative stress indices inwomen with rheumatoid arthritis: a randomized double-blind clinical trial, " Journal of the American College of Nutrition, 2015.
53. M. L. Stecchini, M. Del Torre, and M. Munari, "Determination of peroxy radical-scavenging of lactic acid bacteria, " International Journal of FoodMicrobiology, vol. 64, no. 1-2, pp. 183-188, 2001.
54. R. Chauhan, A. S. Vasanthakumari, H. Panwar et al., "Amelioration of colitis in mouse model by exploring antioxidative potentials of an indigenous probiotic strain of Lactobacillus fermentum Lf1, " BioMed Research International, vol. 2014, Article ID206732, 12 pages, 2014.
55. T. Cecchi, M. Savini, S. Silvi, M. C. Verdenelli, and A. Cresci, "Optimisation of the measurement of the antioxidant activity of probiotics and pathogens: a crucial step towards evidencebased assessment of health claims and production of effective functional foods, " FoodAnalyticalMethods, vol. 8, no. 2, pp. 312-320, 2014.
56. Y. Ishii, S. Sugimoto, N. Izawa, T. Sone, K. Chiba, and K. Miyazaki, "Oral administration of Bifidobacterium breve attenuates UV-induced barrier perturbation and oxidative stress in hairless mice skin, " Archives of Dermatological Research, vol. 306, no. 5, pp. 467-473, 2014.
57. K. H. S. Farvin, C. P. Baron, N. S. Nielsen, and C. Jacobsen, "Antioxidant activity of yoghurt peptides: part 1-in vitro assays and evaluation in-3 enriched milk, " Food Chemistry, vol. 123, no. 4, pp. 1081-1089, 2010.
58. K. H. S. Farvin, C. P. Baron, N. S. Nielsen, J. Otte, and C. Jacobsen, "Antioxidant activity of yoghurt peptides: part 2-characterisation of peptide fractions, " Food Chemistry, vol. 123, no. 4, pp. 1090-1097, 2010.
59. H. Korhonen and A. Pihlanto, "Bioactive peptides: production and functionality, " International Dairy Journal, vol. 16, no. 9, pp. 945-960, 2006.
60. M. Hayes, C. Stanton, G. F. Fitzgerald, and R. P. Ross, "Putting microbes to work: diary fermentation, cell factories and bioactive peptides. Part II: bioactive peptide functions, " Biotechnology Journal, vol. 2, no. 4, pp. 435-449, 2007.
61. M.-Y. Lin and F.-J. Chang, "Antioxidative effect of intestinal bacteria Bifidobacterium longum ATCC 15708 and Lactobacillus acidophilus ATCC 4356, " DigestiveDiseases and Sciences, vol. 45, no. 8, pp. 1617-1622, 2000.
62. V. J. Koller, B. Marian, R. Stidl et al., "Impact of lactic acid bacteria on oxidative DNA damage in human derived colon cells, " Food and Chemical Toxicology, vol. 46, no. 4, pp. 1221-1229, 2008.
63. S. S. Choi, Y. Kim, K. S. Han, S. You, S. Oh, and S. H. Kim, "Effects of Lactobacillus strains on cancer cell proliferation and oxidative stress in vitro, " Letters in AppliedMicrobiology, vol. 42, no. 5, pp. 452-458, 2006.
64. D. G. Duman, Z. N. O. Kumral, F. Ercan, M. Deniz, G. Can, and B. Cąglayan Yegen, "Saccharomyces boulardii ameliorates clarithromycin-and methotrexate-induced intestinal and hepatic injury in rats, " British Journal of Nutrition, vol. 110, no. 3, pp. 493-499, 2013.
65. T. Sąhin, S. Aydin, O. Yüksel et al., "Effects of the probiotic agent Saccharomyces boulardii on the DNA damage in acute necrotizing pancreatitis induced rats, " Human and Experimental Toxicology, vol. 26, no. 8, pp. 653-661, 2007.
66. A. Suryavanshi, A. Agarwal, A. Kaler et al., "Comparative studies on the antioxidant potential of vanillin-producing Saccharomyces boulardii extracts, " Oxidants and Antioxidants in Medical Science, vol. 2, no. 3, pp. 201-209, 2013.
67. H. Annuk, J. Shchepetova, T. Kullisaar, E. Songisepp, M. Zilmer, and M. Mikelsaar, "Characterization of intestinal lactobacilli as putative probiotic candidates, " Journal of Applied Microbiology, vol. 94, no. 3, pp. 403-412, 2003.
68. M. Kumar, A. Kumar, R. Nagpal et al., "Cancer-preventing attributes of probiotics: an update, " International Journal of Food Sciences and Nutrition, vol. 61, no. 5, pp. 473-496, 2010.
69. D. Najgebauer-Lejko, "Effect of green tea supplementation on the microbiological, antioxidant, and sensory properties of probiotic milks, " Dairy Science and Technology, vol. 94, no. 4, pp. 327-339, 2014.
70. G. Grompone, P. Martorell, S. Llopis et al., "Anti-inflammatory Lactobacillus rhamnosus CNCM I-3690 strain protects against oxidative stress and increases lifespan in Caenorhabditis elegans, " PLoS ONE, vol. 7, no. 12, Article IDe52493, 2012.
71. S. Kapila, Vibha, and P. Sinha, "Antioxidative and hypocholesterolemic effect of Lactobacillus casei ssp casei (biodefensive properties of lactobacilli), " Indian Journal of Medical Sciences, vol. 60, no. 9, pp. 361-370, 2006.
72. B. G. Spyropoulos, E. P. Misiakos, C. Fotiadis, and C. N. Stoidis, "Antioxidant properties of probiotics and their protective effects in the pathogenesis of radiation-induced enteritis and colitis, " Digestive Diseases and Sciences, vol. 56, no. 2, pp. 285-294, 2011.
73. J. Lee, K.-T. Hwang, M.-Y. Chung, D.-H. Cho, and C.-S. Park, "Resistance of Lactobacillus casei KCTC 3260 to reactive oxygen species (ROS): role for a metal ion chelating effect, " Journal of Food Science, vol. 70, no. 8, pp. M388-M391, 2005.
74. J. Sun, X.-L. Hu, G.-W. Le, and Y.-H. Shi, "Lactobacilli prevent hydroxy radical production and inhibit Escherichia coli and Enterococcus growth in system mimicking colon fermentation, " Letters in AppliedMicrobiology, vol. 50, no. 3, pp. 264-269, 2010.
75. Y.-C. Wang, R.-C. Yu, and C.-C. Chou, "Antioxidative activities of soymilk fermented with lactic acid bacteria and bifidobacteria, " Food Microbiology, vol. 23, no. 2, pp. 128-135, 2006.
76. V. P. Kodali and R. Sen, "Antioxidant and free radical scavenging activities of an exopolysaccharide from a probiotic bacterium, " Biotechnology Journal, vol. 3, no. 2, pp. 245-251, 2008.
77. N. Sengül, B. Aslm, G. Ucar et al., "Effects of exopolysaccharide-producing probiotic strains on experimental colitis in rats, " Diseases of the Colon and Rectum, vol. 49, no. 2, pp. 250-258, 2006.
78. W. Han, A. Mercenier, A. Ait-Belgnaoui et al., "Improvement of an experimental colitis in rats by lactic acid bacteria producing superoxide dismutase, " Inflammatory BowelDiseases, vol. 12, no. 11, pp. 1044-1052, 2006.
79. I. M. Carroll, J. M.,rus, J. M. Bruno-Bárcena, T. R. Klaenhammer, H. M. Hassan, and D. S. Threadgill, "Anti-inflammatory properties of Lactobacillus gasseri expressing manganese superoxide dismutase using the interleukin 10-deficient mouse model of colitis, " The American Journal of Physiology-Gastrointestinal and Liver Physiology, vol. 293, no. 4, pp. G729-G738, 2007.
80. T. Kullisaar, M. Zilmer, M. Mikelsaar et al., "Two antioxidative lactobacilli strains as promising probiotics, " International Journal of Food Microbiology, vol. 72, no. 3, pp. 215-224, 2002.
81. S. K. Chang and H. M. Hassan, "Characterization of superoxide dismutase in Streptococcus thermophilus, " Applied and Environmental Microbiology, vol. 63, no. 9, pp. 3732-3735, 1997.
82. A. deMoreno de LeBlanc, J. G. LeBlanc, G. Perdigón et al., "Oral administration of a catalase-producing Lactococcus lactis can prevent a chemically induced colon cancer in mice, " Journal of Medical Microbiology, vol. 57, no. 1, pp. 100-105, 2008.
83. H. An, Z. Zhai, S. Yin, Y. Luo, B. Han, andY. Hao, "Coexpression of the superoxide dismutase and the catalase provides remarkable oxidative stress resistance in lactobacillus rhamnosus, " Journal of Agricultural and Food Chemistry, vol. 59, no. 8, pp. 3851-3856, 2011.
84. L.-X. Wang, K. Liu, D.-W. Gao, and J.-K. Hao, "Protective effects of two Lactobacillus plantarum strains in hyperlipidemic mice, " World Journal of Gastroenterology, vol. 19, no. 20, pp. 3150-3156, 2013.
85. F. Lutgendorff, R. M. Nijmeijer, P. A. Sandström et al., "Probiotics prevent intestinal barrier dysfunction in acute pancreatitis in rats via induction of ileal mucosal glutathione biosynthesis, " PLoS ONE, vol. 4, no. 2, Article ID e4512, 2009.
86. L. P. van Minnen, H. M. Timmerman, F. Lutgendorff et al., "Modification of intestinal flora with multispecies probiotics reduces bacterial translocation and improves clinical course in a rat model of acute pancreatitis, " Surgery, vol. 141, no. 4, pp. 470-480, 2007.