Elsevier

Nutrition

Volume 23, Issue 2, February 2007, Pages 172-178
Nutrition

Basic nutritional investigation
Liver-protecting effects of table beet (Beta vulgaris var. rubra) during ischemia-reperfusion

https://doi.org/10.1016/j.nut.2006.11.004Get rights and content

Abstract

Objective

Table beet (Beta vulgaris var. rubra) contains important bioactive agents (betaine and polyphenols), which have a wide range of physiologic effects. Because nutritive antioxidants may reduce the occurrence of complications and postoperative mortality, dietary intake of polyphenols and vitamins before surgery may greatly contribute to the survival of patients. Our aim was to determine the liver-protecting properties of bioactive substances of table beet in a model of ischemia-reperfusion injury of the rat.

Methods

Wistar rats were divided into two groups: non-treated (n = 24) and fed with table beet (n = 8). For 10 days the second group was treated with lyophilized table beet (2 g/kg body weight daily) mixed into the rat chow. Hepatic ischemia was maintained for 45 min, followed by 15 min of reperfusion. Ischemia-reperfusion was carried out on animals from both groups. Chemiluminescent intensity, H-donating ability, reducing power, free SH group concentration, Randox-total antioxidant status, glutathione peroxidase, and superoxide dismutase activities were determined by luminometry and spectrophotometry. Fatty acid (Shimadzu GC) and metal ion (inductively coupled plasma optical emission spectrometry) concentrations were observed in the liver.

Results

As a result of feeding, global parameters (H-donating ability, reducing power, free SH group concentration) and enzymatic antioxidants (glutathione peroxidase and superoxide dismutase) of the liver were found to increase significantly, which indicated that the treatment had a positive effect on its redox state. The increase found in zinc and copper content may protect the hepatocytes against oxidative stress because these elements are required for the function of superoxide dismutase enzymes. In the table beet group the concentration of short-chain fatty acids decreased, whereas that of long-chain fatty acids increased. The changes in metal element and fatty acid concentrations confirmed that these elements have an essential function in cellular pathways.

Conclusion

It may be stated that a natural antioxidant-rich diet has a positive effect on redox homeostasis during hepatic ischemia-reperfusion.

Introduction

Ischemia-reperfusion during hepatic surgery and transplantation is associated with oxidative stress, which alters the main cellular functions and causes damage to the hepatocytes [1].

Kupffer cells and stellate cells are also activated by oxidative stress and are responsible for most of the ensuing liver damage [2]. During the respiratory burst, Kupffer cells generate an enormous amount of free radicals. In addition, cytokines (e.g., tumor necrosis factor-α) and prostaglandins are generated, transcriptional factors (nuclear factor-κB, nuclear factor E2-related factor-2) are induced; therefore, hepatic injury may be prevented by altering these molecular pathways [3], [4], [5].

In addition to damaging DNA and proteins, oxidative stress causes lipid peroxidation, which has a lethal effect on the liver cells by changing the cellular homeostasis due to the insufficiency of the membranes [6].

Through the generation of prostaglandins, inflammation is also associated with oxidative damage. It has been assumed that Kupffer cells and T cells mediate the activation of neutrophil inflammatory responses [7].

Owing to the low risk of possible side effects, the administration of natural food constituents before surgery seems to be a promising treatment option.

The consumption of table beet (Beta vulgaris var. rubra) has numerous beneficial physiologic effects, some of which may be appropriate for the protection of the liver of presurgical patients. Because table beet contains a great number of different components, it may be able to modulate various cellular pathways. The beneficial medical effect is due to bioactive components, such as betaine, betanin, betaxanthins, flavonoids, polyphenols, vitamins (thiamine, riboflavine, pyridoxine, ascorbic acid), folic acid, and biotin, and soluble fiber and pectin. Mainly betanin (the natural coloring agent of beetroot), flavonoids (e.g., quercetin), and other polyphenols have extremely effective antioxidant properties [8], [9], [10].

The results measured in cell culture experiments are difficult to compare with real pathologic states of the living organism; therefore, it may be presumed that studying the consumption of bioactive molecules in their natural form may provide more relevant information.

Our aim was to determine whether hepatic tissue damage during ischemia-reperfusion can be prevented by pretreatment with a table beet-rich diet. The wide range of physiological effects may include possible protection against oxidative stress. It has been assumed that metal element content of the liver has an essential role in determining the survival of hepatocytes by modification of the antioxidant enzyme activity [11], [12], [13], [14]. The metal element content of table beet may prevent the decrease of copper/zinc superoxide dismutase (SOD) activity in the liver. Although table beet may restore the normal function of fatty acid metabolism, these essential cellular pathways have not been thoroughly studied thus far. Because betaine is a potent methyl donor, study of the effect of transmethylation may provide new perspectives for liver protection during surgery.

Section snippets

Materials and methods

Luminol, microperoxidase, hydrogen peroxide, and the 1,1-diphenyl-2-picryl-hydrasyl radical were obtained from Sigma (St. Louis, MO, USA), and total antioxidant status (NX2332), SOD (SD 125) and glutathione peroxidase (GSHPx; RS 506) kits were bought from Randox (Crumlin, UK). The standard solution for inductively coupled plasma measurements was made from Merck inductively coupled plasma standards (Merck, Darmstadt, Germany). Other chemical reagents were purchased from Reanal Chemical Co.

Statistical analysis

The differences between two groups was examined by Student’s t probe using Statistica 6.0 software (Statsoft, Tulsa, OK, USA). One-way analysis of variance was also applied to evaluate the significance across the different groups. Significance levels were determined at P < 0.05.

Changes in the blood

Lyophilized table beet reduced the chemiluminescent intensity of the plasma significantly after ischemia-reperfusion (Fig. 1).

Antioxidant parameters of the plasma were higher in rats fed the beetroot diet (Table 2).

Changes in the liver

Beetroot significantly reduced the diene conjugate concentration of liver during ischemia-reperfusion. H-donor ability and the reducing power of the liver tissue were significantly increased as a result of feeding, whereas the concentration of free SH groups showed no significant

Discussion

The most important physiologic role of betaine is that it may serve as an osmolyte and methyl donor [26]. In addition, betaine treatment has a restoring effect on the alterations in the level of triacylglycerol, lipid peroxide, and GSH under pathologic conditions [27].

Polyphenols have antioxidative, anti-inflammatory, and antiviral effects. Polyphenols may reduce the severity of liver injury in association with lower concentrations of lipid peroxides and proinflammatory nitric oxide–generated

Acknowledgments

The authors thank Sarolta Bárkovits and Edina Pintér for great technical assistance. This work was supported by Zsolt Pallai, head of Diachem Ltd., and Timea Kurucz, chemical engineer (Diachem Ltd., Hungary).

References (42)

  • J. Balkan et al.

    The effect of betaine treatment on triglyceride levels and oxidative stress in the liver of ethanol-treated guinea pigs

    Exp Toxicol Pathol

    (2004)
  • Z. Zhong et al.

    Polyphenols from Camellia sinenesis prevent primary graft failure after transplantation of ethanol-induced fatty livers from rats

    Free Radic Biol Med

    (2004)
  • J.D. Lambert et al.

    Mechanisms of cancer prevention by tea constituents

    J Nutr

    (2003)
  • Z. Gao et al.

    Antioxidant status and mineral contents in tissues of rutin and baicalin fed rats

    Life Sci

    (2003)
  • Y.O. Son et al.

    Selective antiproliferative and apoptotic effects of flavonoids purified from Rhus verniciflua Stokes on normal versus transformed hepatic cell lines

    Toxicol Lett

    (2005)
  • C.H. Kim et al.

    Zinc-induced NF-kappaB inhibition can be modulated by changes in the intracellular metallothionein level

    Toxicol Appl Pharmacol

    (2003)
  • S.D. Finkelstein et al.

    Alterations in the metabolism of lipids in ischemia of the liver and kidney

    J Lipid Res

    (1985)
  • J.C. Cutrin et al.

    Primary role of Kupffer cell-hepatocyte communication in the expression of oxidative stress in the post-ischaemic liver

    Cell Biochem Funct

    (1998)
  • T. Akita et al.

    New medium composition for high betacyanin production by a cell suspension culture of table beet (Beta vulgaris L.)

    Biosci Biotech Biochem

    (2002)
  • R. Lichtenthaler et al.

    Total oxidant scavenging capacities of common European fruit and vegetable juices

    J Agr Food Chem

    (2005)
  • T.S. Kujala et al.

    Phenolics and betacyanins in red table beet (Beta vulgaris) root: distribution and effect of cold storage on the content of total phenolics and three individual compounds

    J Agr Food Chem

    (2000)
  • Cited by (70)

    • Inhibition of NF-κB and the oxidative stress -dependent caspase-3 apoptotic pathway by betaine supplementation attenuates hepatic injury mediated by cisplatin in rats

      2019, Pharmacological Reports
      Citation Excerpt :

      In previous studies, betaine administration exhibited protective effects against oxidative injury in liver [13], and other organs as heart [39], and kidney [17]. Betaine accentuates oxidative hepatic injury induced by ischemia/reperfusion [40], and by hepatotoxicants such as ethanol [41], chloroform [13], lipopolysaccharide [35,15], dimethylnitrosoamine [14], and α-naphthylisothiocyanate [13]. Betaine was also protective in alcoholic and non-alcoholic fatty liver disease [8,9,42,43]

    View all citing articles on Scopus

    This study was supported by the Ph.D. Programme of the Semmelweis University No. 2/1, ETT 012/2006 Project, NKFP 1A 005/2004, and NKFP1B 047/2004 Projects.

    View full text