Effects of Lactofermented Beetroot Juice Alone or with N-nitroso-N-methylurea on Selected Metabolic Parameters, Composition of the Microbiota Adhering to the Gut Epithelium and Antioxidant Status of Rats
Abstract
:1. Introduction
2. Experimental Section
2.1. Plant Material
2.2. Microorganisms and Lactic Fermentation
2.3. Animals, Chemicals and Diets
2.4. Antioxidant Capacity of Blood Serum
2.5. Enzymatic Analysis
2.6. The Ammonia Content and pH of Intestinal Digesta
2.7. Sample Preparation and Analysis by Fluorescent in Situ Hybridization (FISH)
2.8. Statistic Analysis
3. Results
3.1. Cecum Parameters
Index | C | CJ | M | MJ | SEM | Diet | Juice | D × J | ||
---|---|---|---|---|---|---|---|---|---|---|
C | M | 0 | + | P | ||||||
Tissue mass 1 | 2.09 | 2.88 | 2.90 | 3.02 | 0.004 | 2.89 | 2.96 | 2.93 | 2.95 | 0.682 |
Digesta mass 1 | 10.25 | 10.14 | 9.85 | 9.37 | 0.028 | 10.20 | 9.61 | 10.05 | 9.76 | 0.947 |
NH3 2 | 0.260 a | 0.209 b | 0.272 a | 0.226 c | 0.694 | 0.234 | 0.249 | 0.266 a | 0.217 b | <0.05 |
pH of digesta | 6.77 | 6.94 | 6.70 | 6.76 | 0.029 | 6.82 | 6.74 | 6.73 | 6.85 | 0.263 |
3.2. Intestinal Enzymes Activity
Enzyme | Dietary Group | |||
---|---|---|---|---|
C | CJ | M | MJ | |
Small Intestine—Mucosal Disaccharide Activity 1 | ||||
Sucrase | 31.1 (0.388) a | 29.3 (0.318) ab | 26.8 (0.848) b | 26.3 (0.709) b |
Maltase | 98.4 (1.131) a | 85.3 (0.742) a | 78.7 (1.343) b | 76,7 (1.631) b |
Lactase | 3.9 (0.318) | 4.2 (0.353) | 3.9 (0.141) | 3.4 (0.176) |
Cecum—Microbial Glycolytic Activity 2 | ||||
β-glucuronidase | 11.8 (0.671) b | 9.5 (0.318) b | 23.0 (0.742) a | 11.0 (0.919) b |
β-glucosidase | 12.0 (0,636) | 12.6 (0.707) | 15.5 (0.671) | 14.4 (0.636) |
α-galactosidase | 18.1 (0.318) a | 25.8 (0.884) a | 21.7 (0.990) a | 46.2 (1.519) b |
β-galactosidase | 53.4 (2.227) | 51.5 (1.025) | 56.7 (1.343) | 55.9 (1.025) |
3.3. Microorganisms Adhering to Intestinal Epithelium
3.4. Antioxidant Status of Serum, Liver and Kidney of Rats
Probe | Dietary Group | |||
---|---|---|---|---|
C | CJ | M | MJ | |
Lab 158 | 7.02 (0.053) a | 7.56 (0.038) b | 6.64 (0.063) c | 6.63 (0.042) c |
Bac 303 | 7.47 (0.042) a | 8.17 (0.226) b | 6.89 (0.265) a | 7.12 (0.038) a |
Eub 338 | 7.47 (0.099) a | 7.19 (0.109) a | 6.71 (0.137) b | 6,76 (0.201) b |
Erec 484 | 6.58 (0.155) a | 5.57 (0.180) b | 6.79 (0.109) a | 6.37 (0.099) a |
Enter 1432 | 6.02 (0.060) a | 5.95 (0.113) a | 7.25 (0.042) b | 6.36 (0.162) c |
Bif 164 | 5.44 (0.127) a | 5.73 (0.109) a | 5.67 (0.131) a | 5.86 (0.053) a |
Index | C | CJ | M | MJ | SEM | Diet | Juice | D × J | ||
---|---|---|---|---|---|---|---|---|---|---|
C | M | 0 | + | P | ||||||
Hydrophilic antioxidants 1 | 0.043a | 0.043 a | 0.023 b | 0.039 a | 0.002 | 0.043 a | 0.031 b | 0.033 b | 0.041 a | <0.05 |
Lipophilic antioxidants 2 | 0.061a | 0.066 a | 0.048 b | 0.048b | 0.002 | 0.063 a | 0.048 b | 0.054 b | 0.057 b | <0.05 |
Liver 3 | 36.88 | 35.59 | 36.41 | 37.13 | 0.040 | 36.24 | 36.77 | 36.64 | 36.36 | 0.414 |
MDA 4 | 30.15 | 29.84 | 29.43 | 30.87 | 0.854 | 30.00 | 30.15 | 27.79 | 30.36 | 0.530 |
Kidneys 3 | 5.99 | 5.88 | 6.22 | 6.33 | 0.008 | 5.93 | 6.28 | 6.11 | 6.11 | 0.837 |
MDA 4 | 85.84 | 86.18 | 84.08 | 86.08 | 2.250 | 86.01 | 85.17 | 84.96 | 86.13 | 0.550 |
4. Discussion
5. Conclusions
Acknowledgments
Author Contributions
Conflicts of Interest
References
- Herbach, K.M.; Stintzing, F.C.; Carle, R. Thermal degradation of betacyanins in juices from purple pitaya [Hylocereus polrhizus (Weber) Britton & Rose] monitored by high-performance liquid chromatography-tandem mass spectrometric analyses. Eur. Food Res. Technol. 2004, 219, 377–385. [Google Scholar]
- Stintzing, F.C.; Schieber, A.; Carle, R. Evaluation of colour properties and chemical quality parameters of cactus juices. Eur. Food Res. Technol. 2003, 216, 303–311. [Google Scholar]
- Czyżowska, A.; Klewicka, E.; Libudzisz, Z. The influence the lactic acid fermentation process of red beet juice on the stability of biologically active colorants. Eur. Food Res. Technol. 2006, 223, 110–116. [Google Scholar] [CrossRef]
- Klewicka, E.; Zduńczyk, Z.; Juśkiewicz, J. Effect of lactobacillus fermented beetroot juice on composition and activity of cecal microflora of rats. Eur. Food Res. Technol. 2009, 229, 153–157. [Google Scholar] [CrossRef]
- Klewicka, E.; Nowak, A.; Zduńczyk, Z.; Cukrowska, B.; Błasiak, J. Protective effect of lactofermented beetroot juice against aberrant crypt foci formation and genotoxicity of fecal water in rats. Exp. Toxicol. Pathol. 2012, 64, 599–604. [Google Scholar] [CrossRef] [PubMed]
- Reeves, P.G. Components of the AIN-93 diets as improvements in the AIN-76A. J. Nutr. 1997, 127, S838–S841. [Google Scholar]
- Ohkawa, H.; Ohishi, N.; Yagi, K. Assay for lipid peroxides in animal tissue by thiobarbituric acid reaction. Anal. Biochem. 1979, 95, 351–358. [Google Scholar] [CrossRef]
- Dahlqvist, A. Method for assay of intestinal disaccharidases. Anal. Biochem. 1964, 7, 18–25. [Google Scholar] [CrossRef]
- Juśkiewicz, J.; Zduńczyk, Z. Lactulose-induced diarrhoea in rats: Effects on caecal development and activities of microbial enzymes. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 2002, 133, 411–417. [Google Scholar] [CrossRef]
- Hofirek, B.; Hass, D. Comparative studies of ruminal fluid collected by oral tube or puncture of the caudorental ruminal sac. Acta Vet. Brno. 2001, 70, 27–33. [Google Scholar] [CrossRef]
- Klewicka, E.; Nowak, A.; Zduńczyk, Z.; Juśkiewicz, J.; Cukrowska, B. Protective effect of lactofermented red beetroot juice against aberrant crypt foci formation, genotoxicity of fecal water and oxidative stress induced by 2-amino-l-methyl-6-phenylimidazo[4,5-b] pyridine in rats model. Environ. Toxicol. Pharmacol. 2012, 31, 895–904. [Google Scholar] [CrossRef] [PubMed]
- Kapadia, G.J.; Azuine, M.A.; Sridhar, R.; Okuda, Y.; Tsuruta, A.; Ichiishi, E.; Mukainake, T.; Takasaki, M.; Konoshima, T.; Nishino, H.; et al. Chemoprevention of DMBA-induced UV-B promoted, NOR 1-induced TPA promoted skin carcinogenesis, and DEN-induced phenobarbital promoted liver tumors in mice by extract of beetroot. Pharmacol. Res. 2003, 47, 141–148. [Google Scholar] [CrossRef]
- Sreekanth, D.; Arunasree, M.K.; Roy, K.R.; Reddy, T.C.; Reddanna, P. Betanin a betacyanin pigment purified from fruits of Opuntia ficus-indica induces apoptosis in human chronic leukemia cell line K562. Phytomedicine 2007, 14, 739–46. [Google Scholar] [CrossRef] [PubMed]
- Gandia-Herrero, F.; Escribano, J.; Garcia-Carmona, F. Structural implications on color, fluorescence, and activity in betalains. Planta 2010, 232, 449–460. [Google Scholar] [CrossRef] [PubMed]
- Tesoriere, L.; Butera, D.; d’Arpa, D.; di Guadio, F.; Allegra, M.; Gentile, C.; Livera, M.A. Increased resistance to oxidation of betalain-enriched human low density lipoproteins. Free Radic. Res. 2003, 37, 689–696. [Google Scholar] [CrossRef] [PubMed]
- Reynoso, R.C.; Giner, T.V.; Gonzalez de Mejia, E. Safety of filtrate of fermented garambullo fruit: Biotransformation and toxicity studies. Food Chem. Toxicol. 1999, 37, 825–830. [Google Scholar] [CrossRef]
- Klewicka, E. Betacyanins-bioavailability and biological activity. Żywnosć. Nauka. Technologia. Jakość 2012, 2, 5–21. [Google Scholar] [CrossRef]
- Lin, H.C.; Visek, W.J. Large intestinal pH and ammonium in rats: Dietary fat and protein interaction. J. Nutr. 1991, 121, 832–843. [Google Scholar] [PubMed]
- Katayama, K. Ammonia metabolism and hepatic encephalopathy. Hepatol. Res. 2004, 30, S73–S80. [Google Scholar] [CrossRef] [PubMed]
- Wrzosek, L.; Miquel, S.; Noordine, M.L.; Bouet, S.; CHevalier-Curt, M.J.; Robert, V.; Philippe, C.; Bridonneau, C.; Cherbuy, C.; Robbe-Masselot, C.; et al. Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii influence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent. BMC Biol. 2013, 11, 61–74. [Google Scholar] [CrossRef] [PubMed]
- Nowak, A.; Libudzisz, Z. Ability of intestinal lactic bacteria to bind or/and metabolise phenol and p-cresol. Ann. Microbiol. 2007, 57, 329–335. [Google Scholar] [CrossRef]
- Nowak, A.; Libudzisz, Z. Ability of probiotic Lactobacillus casei DN 114001 to bind or/and metabolise heterocyclic aromatic amines in vitro. Eur. J. Nutr. 2009, 48, 419–427. [Google Scholar] [CrossRef] [PubMed]
- Piotrowska, M. The Adsorption of Ochratoxin A by Lactobacillus Species. Toxins 2014, 6, 2826–2839. [Google Scholar] [CrossRef] [PubMed]
- Wollowski, I.; Rechkemmer, G.; Pool-Zobel, B.L. Protective role of probiotics and prebiotics in colon cancer. Am. J. Clin. Nutr. 2001, 73S, 451S–455S. [Google Scholar] [PubMed]
- Zenser, T.V.; Lakshmi, V.M.; Davis, B.B. Human and Escherichia coli β-glucuronidase hydrolysis of glucuronide conjugates of benzidine and 4-aminobiphenyl, and their hydroxy metabolites. Drug Metab. Dispos. 1999, 27, 1064–1067. [Google Scholar] [PubMed]
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Klewicka, E.; Zduńczyk, Z.; Juśkiewicz, J.; Klewicki, R. Effects of Lactofermented Beetroot Juice Alone or with N-nitroso-N-methylurea on Selected Metabolic Parameters, Composition of the Microbiota Adhering to the Gut Epithelium and Antioxidant Status of Rats. Nutrients 2015, 7, 5905-5915. https://doi.org/10.3390/nu7075260
Klewicka E, Zduńczyk Z, Juśkiewicz J, Klewicki R. Effects of Lactofermented Beetroot Juice Alone or with N-nitroso-N-methylurea on Selected Metabolic Parameters, Composition of the Microbiota Adhering to the Gut Epithelium and Antioxidant Status of Rats. Nutrients. 2015; 7(7):5905-5915. https://doi.org/10.3390/nu7075260
Chicago/Turabian StyleKlewicka, Elżbieta, Zenon Zduńczyk, Jerzy Juśkiewicz, and Robert Klewicki. 2015. "Effects of Lactofermented Beetroot Juice Alone or with N-nitroso-N-methylurea on Selected Metabolic Parameters, Composition of the Microbiota Adhering to the Gut Epithelium and Antioxidant Status of Rats" Nutrients 7, no. 7: 5905-5915. https://doi.org/10.3390/nu7075260