SHORT COMMUNICATION

Prevention of Cholesterol Gallstone Formation by Lactobacillus acidophilus ATCC 43121 and Lactobacillus fermentum MF27 in Lithogenic Diet-Induced Mice

Ju Kyoung Oh1https://orcid.org/0000-0003-0132-8801, You Ra Kim1https://orcid.org/0000-0001-7464-0797, Boin Lee2https://orcid.org/0000-0001-7745-9766, Young Min Choi2,*https://orcid.org/0000-0003-2376-7784, Sae Hun Kim1,*https://orcid.org/0000-0002-0990-2268
Author Information & Copyright
1Department of Food Bioscience and Technology, Korea University, Seoul 02841, Korea
2Department of Animal Sciences and Biotechnology, Kyungpook National University, Sangju 37224, Korea
*Corresponding author : Young Min Choi, Department of Animal Sciences and Biotechnology, Kyungpook National University, Sangju 37224, Korea, Tel: +82-54-530-1232, Fax: +82-54-530-1229, E-mail: ymchoi1@knu.ac.kr
*Corresponding author : Sae Hun Kim, Department of Food Bioscience and Technology, Korea University, Seoul 02841, Korea, Tel: +82-2-3290-3055, Fax: +82-2-3290-3040, E-mail: saehkim@korea.ac.kr

© Korean Society for Food Science of Animal Resources. This is an Open-Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Received: Oct 05, 2020 ; Revised: Nov 09, 2020 ; Accepted: Nov 16, 2020

Published Online: Mar 01, 2021

Abstract

The objective of this study was to evaluate the effects of Lactobacillus acidophilus ATCC 43121 and L. fermentum MF27 on biochemical indices in the serum, cholesterol metabolism in the liver and mucin expression in the gallbladder in lithogenic diet (LD)-induced C57BL/6J mice to determine the preventive effects of lactobacilli on gallstone formation. By the end of 4 wk of the experimental period, mice fed on a LD with high-fat and high-cholesterol exhibited higher levels of total and low-density lipoprotein cholesterol in the serum compared to mice fed on control diet or LD with L. acidophilus ATCC 43121 (LD+P1; p<0.05). Cholesterol-lowering effects observed in the LD+P1 and LD with L. fermentum MF27 (LD+P2) groups were associated with reduced expression of 3-hydroxy-3-methylglutaryl coenzyme A reductase in the liver compared to the LD group (p<0.05). Furthermore, expression of the gel-forming mucin, including MUC5AB and MUC5B, was suppressed in the LD+P1 and LD+P2 groups compared to the LD group (p<0.05). Therefore, steady intake of both L. acidophilus ATCC 43121 and L. fermentum MF27 may have the ability to prevent the formation of cholesterol gallstones in LD-induced C57BL/6J mice.

Keywords: cholesterol gallstone; mucin; Lactobacillus acidophilus; Lactobacillus fermentum; lithogenic diet

Introduction

Cholesterol gallstone disease is one of the most common conditions in the gastrointestinal tract, which is caused by the complex interaction of multiple genetic and environmental factors that contribute to the gallstone formation (Chuang et al., 2012). Recently, in Asian countries, this biliary tract disease has been rapidly increasing due to changes in dietary habits and life style, although it is highly prevalent in people from Western countries compared to Asian countries (Chen et al., 2019). It is well known that cholesterol gallstone formation is mainly due to the imbalance of bile components, which is affected by hypersecretion and accumulation of cholesterol (Song et al., 2015). As cholesterol content in bile increases significantly, cholesterol is supersaturated, causing precipitation and aggregation of excess cholesterol in the gallbladder, and which can become gallstone (Purushortham et al., 2012). Additionally, the formation of cholesterol gallstones is caused by mucin protein hypersecretions associated with certain variants in MUC genes, as mucin proteins have the ability to bind to lipids and bile pigments due to hydrophobic binding sites, thus contributing mucus gel formation and gallbladder hypomotility (Bar Dayan et al., 2004; Chuang et al., 2012). Generally, patients with cholesterol gallstones exhibit a higher level of mucin proteins, especially gel-forming mucin, in gallbladder than control patients without cholesterol gallstones (Bar Dayan et al., 2004; Lee et al., 1979).

It is important to inhibit mucin overproduction in the gallbladder to prevent the gallstone formation (Chuang et al., 2012). Urosodeoxycholic acid (UDCA) can reduce the concentration of mucin proteins and the formation of cholesterol crystals in patients with gallstones (Castro-Torres et al., 2015). Thus, UDCA is commonly used as a pharmacological agent for treating cholesterol gallstone disease (Castro-Torres et al., 2015). However, this agent can cause cholestasis and cell membrane damage through inhibition of bile acid absorption and choleretic function (Guarino et al., 2013). In addition, it takes a long time for UDCA to take effect and it may cause gallstone recurrence after lithotripsy (Vidyashankar et al., 2010). Therefore, the search for a better treatment is needed for the cholesterol gallstone disease. It is important to not only treat the cholesterol gallstone disease, but also to prevent the occurrence and recurrence of gallstones (Song et al., 2015).

Lactobacilli are well-known probiotics that help improve human health and prevent various diseases (Lee et al., 2011). Previous studies have shown the health benefits of lactobacilli, including immune modulation, antimicrobial, and anticarcinogenic effects in the human intestine (Oelschlaeger, 2010). Additionally, some lactobacilli, including Lactobacillus acidophilus and L. fermentum, reduced not only lipid level, and but also total and low-density lipoprotein (LDL) cholesterol levels in the serum and liver (Kim et al., 2008; Lye et al., 2012; Park et al., 2007). Due to these hypocholesterolemic properties, we reasoned that L.acidophilus and L. fermentum may affect the mucin biosynthesis and cholesterol gallstone formation. However, research on the effects of lactobacilli on cholesterol gallstone formation is limited. Therefore, this study aimed to investigate the effects of L. acidophilus ATCC 43121 and L. fermentum MF27 supplementation on biochemical indices, including cholesterols, triglycerides, and phospholipids, in the serum of lithogenic diet (LD)-induced C57BL/6J mice. Additionally, this study also examined the effects of probiotic supplementation on expressions of genes related to cholesterol metabolism in the liver and mucin in the gallbladder to determine the preventive effects of lactobacilli on gallstone formation in LD-induced C57BL/6J mice.

Materials and Methods

Bacterial strains and growth medium

Both L. acidophilus ATCC 43121 and L. fermentum MF27 were obtained from the Food Microbiology Laboratory at the Korea University (Seoul, Korea), and the origins of these lactobacilli were pig and human intestines, respectively. One percentage inoculum of bacterial strains was cultured under the anaerobic condition (Oxoid Anaerobic Gas Generating Kit, Oxoid, Basingstoke, UK) monitored by an anaerobic indicator (Oxoid). The microorganisms were grown in sterile de Mann, Rogosa, and Sharpe (MRS) broth (Difco, Becton, NJ, USA) at 37°C for 24 h and was diluted consecutively three times in fresh MRS broth prior to use. For long-term storage, stock cultures were maintained at −80°C in MRS broth containing 15% glycerol.

Animals and diets

A total of forty inbred 6-week old male C57BL/6J mice were purchased from Samtako Bio Korea (Osan, Korea) and used in this study. After a conditioning period of 7 d, the animals were randomly divided into the following 5 groups (8 mice per group): control (standard diet with saline), LD containing 1.25% cholesterol, 16% fat (5.0% soy bean oil, 7.5% cocoa butter, and 3.5% coconut oil), and 0.5% sodium cholic acid (D12336, Research Diets, New Brunswick, NJ, USA), LD with UDCA (LD+UDCA; 20 mg/kg per day, Alfa Aesar, Ward Hill, MA, USA), LD with L. acidophilus ATCC 43121 (LD+P1; 109 CFU/mL in 500 μL per day), and LD with L. fermentum MF27 (LD+P2; 109 CFU/mL in 500 μL per day). Mice from each group were treated for 4 week, and body weight was measured weekly. Saline, UDCA, L. acidophilus ATCC 43121, and L. fermentum MF27 were orally administered to mice according to their respective groups. All mice were kept under the controlled condition of 12 h light/dark cycles with temperature 22°C to 25°C and relative humidity 56% to 60%, and water and food were allowed ad libitum. The animal experiments were approved by the Korea University Institutional Animal Care and Use Committee (KUIACUC-69). All experiments in this study were conducted in accordance with the Care and Use of Laboratory Animals (National Research Council, 2010).

Biochemical assays

Blood samples were collected by cardiac puncture after administration of Anesthetics [Zoletil 50 (Vibac Laboratories, Carros, France) 60 mL/100 g and Rompun (Bayer Korea, Seoul, Korea) 40 μL/100 g]. The blood samples were placed in heparinized sterile microfuge tubes and centrifuged at 2,000×g for 15 min at 4°C. Total cholesterol, LDL cholesterol, high-density lipoprotein (HDL) cholesterol, triglycerides, and phospholipids concentrations were enzymatically assessed by a Cobas C111 automatic analyzer (Roche, Basel, Switzerland) using assay kits from Roche (Mannhein, Germany). Ratio of cholesterol and phospholipid (C:P) was calculated from the total cholesterol level divided by phospholipids level.

RNA extraction and reverse transcription-polymerase chain reaction (RT-PCR) analysis

Total RNA was extracted from the liver and gallbladder with a GeneJET RNA Purification Kit (Thermo Scientific, Massachusetts, MA, USA) according the manufacturers’ protocol, and cDNA was prepared by reverse transcription of 2 μg total RNA using first strand cDNA synthesis kit (LeGene Biosciences, California, CA, USA). Primers used for RT-PCR and the size of the PCR products are listed in Table 1. The mRNA levels of 3-hydroxy-3-methylglutaryl coenzyme A reductase (HMG CoA R), and cholesterol 7α-hydroxylase (CYP7A1), MUC1, MUC2, MUC5AC, MUC5B, and β-actin were quantified using PCR (Eppendorf, Hamburg, Germany). RT-PCR conditions and the expression levels of relevant genes were determined using the quantification methods as described by Liu et al. (2017) and Yong et al. (2019). Expression levels of relevant genes were normalized against the expression of β-actin as housekeeping gene.

Table 1. Primer sequences of real-time PCR for gene amplification
Tissue Gene Forward (5'→3') Reverse (5'→3')
Liver HMG CoA R TCC AGT TCC AGA ACC TAC GG ACA AGG CAT TCC ACA AGA GC
CYP7A1 CAA GAA CCT GTA CAT GAG GGA C CAC TTC TTC AGA GGC TGC TTT C
Gallbladder MUC1 CCA CAG TAG TGC CTC CAT CC GCC ATG GTA GGA GAA ACA GG
MUC2 CTT CCA ACC CTC CTC CTA CC GCG TCT CTG ACC TCT TCA GG
MUC5AC TGA GAG ATG CCT GTG TGA GG AGC ATC CGT CTT CTC TCA GC
MUC5B ATC GAT GAG TGC AAC TGT GC GAG AAT GAG GCC AAA ACA GC
β-Actin CCT CTA TGC CAA CAC AGT AGC CAC CAA TCC ACA CAG

HMG CoA R, 3-hydroxy-3-methylglutaryl coenzyme A reductase; CYP7A1, cholesterol 7α-hydroxylase; MUC, mucin.

Download Excel Table
Statistical analysis

To compare the body weight, serum biochemical indices, and expressions of various genes involved in cholesterol synthesis and gallstone formation among the five groups, association analysis by the general linear model was carried out using SAS software (SAS Institute Cary, NC, USA). Significant differences among the five treatments were determined using the probability difference (PDIFF), based on a significant value of 5%. All means were presented as least square means with standard errors.

Results

Effects of lactobacilli on body weight and biochemical indices

Fig. 1 presents the effects of lactobacilli on body weight in LD-induced C57BL/6J mice. No significant difference in body weight was observed between experimental groups at each period (p>0.05). By the end of 4 wk, body weight in the control and treatment groups was significantly increased compared to that at 0 wk (p<0.05). In contrast, mice group fed on LD with L. fermentum MF27 (LD+P2) showed no significant weight gain (p>0.05).

kosfa-41-2-343-g1
Fig. 1. Comparison of body weight between the experimental groups of C57BL/6J mice. Error bars represent standard errors. Level of significance: * p<0.05, *** p<0.001. LD, lithogenic diet; UDCA, ursodeoxycholic acid; P1, Lactobacillus acidophillus ATCC 43121; P2, Lactobacillus fermentum MF27.
Download Original Figure

Serum biochemical indices by the end of 4 wk of the experimental period are shown in Table 2. Total cholesterol level was approximately 1.8 times greater in the LD group on high-fat and high-cholesterol diet compared to the control group (180.3 vs. 102.0 mg/dL, p<0.001). Additionally, the LD+P1 group showed a lower level of total cholesterol compared to the LD+P2 and LD+UDCA groups (155.6 vs. 184.8 and 186.0 mg/dL, p<0.001). No significant difference in total, LDL, and HDL cholesterol contents was observed between the LD and LD+UDCA groups (p>0.05). The LD+P1 and LD+P2 groups showed lower content of LDL cholesterol (34.4 and 54.0 mg/dL) compared to the LD and LD+UDCA groups (59.6 and 58.8 mg/dL, p<0.001), even though no difference was observed in the HDL cholesterol between the LD and LD+P2 groups (112.6 vs. 120.0 mg/dL, p>0.05). Higher level of triglycerides was observed in the LD group compared to the LD+P1 and LD+P2 groups (67.3 vs. 51.8 and 54.6 mg/dL, p<0.01), although no difference was observed between the LD and control (58.2 mg/dL) groups. The LD+P2 group showed a higher value of phospholipids compared to the control and LD+P1 groups (274.0 vs. 225.8 and 241.0 mg/dL, p<0.01). However, the control group displayed a lower ratio of C:P compared to the LD+UDCA and LD+P1 groups (0.45 vs. 0.75 and 0.65, p<0.001).

Table 2. Comparison of serum biochemical indices between the experimental groups of C57BL/6J mice
Treatments SEM Level of significance
Control LD LD+UDCA LD+P1 LD+P2
Total cholesterol (C, mg/dL) 102.0c 180.3a 186.0a 155.6b 184.8a 4.33 ***
LDL cholesterol (mg/dL) 13.6d 59.6a 58.8a 34.4c 54.0b 1.62 ***
HDL cholesterol (mg/dL) 92.8c 112.6ab 117.8ab 111.2b 120.0a 2.96 ***
Triglycerides (mg/dL) 58.2ab 67.3a 47.8c 51.8bc 54.6bc 3.40 **
Phospholipids (P, mg/dL) 225.8c 199.6d 250.0b 241.0bc 274.0a 6.27 ***
C:P ratio 0.45d 0.92a 0.75b 0.65c 0.68bc 0.03 ***

** p<0.01, *** p<0.001.

a–d Different superscript letters in the same row represent significant differences (p<0.05).

LD, lithogenic diet; UDCA, ursodeoxycholic acid; P1, Lactobacillus acidophillus ATCC 43121; P2, Lactobacillus fermentum MF27; LDL, low density lipoprotein; HDL, high density lipoprotein.

Download Excel Table
Effects of lactobacilli on cholesterol metabolism in liver and MUC gene expression in gallbladder

Expression levels of HMG CoA R and CYP7Al, two genes involved in the cholesterol and bile acid synthesis pathway in the liver, are shown in Fig. 2A. Significantly higher expression levels of HMG CoA R (1.81 vs. 1.00, p<0.05) and CYP7A1 (1.38 vs. 1.00, p<0.05) showed in the LD group compared to the control group. The LD treatment groups, including +UDCA, +P1, and +P2, had lower expression levels in HMG CoA R compared to the control group (p<0.05), although no significant difference was detected in CYP7A1 expression among the control, LD+UDCA, and LD+P1 groups (p>0.05).

kosfa-41-2-343-g2
Fig. 2. Comparison of expression levels of genes involved in cholesterol metabolism in liver (A) and gallstone formation in gallbladder (B) by quantitative real-time PCR between the experimental groups of C57BL/6J mice. Error bars indicate standard errors. a–e Different letters were considered statistically different (p<0.05). HMG CoA R, 3-hydroxy-3-methylglutaryl–coenzyme A reductase; CYP7Al, cholesterol 7α-hydroxylase; MUC, mucin; LD, lithogenic diet; UDCA, ursodeoxycholic acid; P1, Lactobacillus acidophillus ATCC 43121; P2, Lactobacillus fermentum MF27.
Download Original Figure

The results for expression levels of MUC genes in the gallbladder between the groups are shown in Fig. 2B. There was no significant difference in expression levels of MUC1 among the groups except the LD+UDCA group, which exhibited the lowest level compared to the other groups (0.60, p<0.05). Expression of gel-forming mucin genes (MUC2, MUC5AC, and MUC5B) in the LD+UDCA group was lower compared to the LD group (p<0.05). Lower expression levels of MUC5AC and MUC5B were detected in both the LD+P1 and LD+P2 groups compared to the LD group (p<0.05), although no difference was observed in MUC2 level among these groups (p>0.05).

Discussion

It is generally accepted that dietary habit, especially a long-term high-fat diet, is a major risk factor contributing to the formation of cholesterol gallstone among all known factors (Acalovschi, 2014; Castro-Torres et al., 2015). Additionally, such LD can induce changes in serum biochemical indices (Deng et al., 2015; Liu et al., 2017). Liu et al. (2017) reported that mice fed on a LD containing high-fat and high-cholesterol contents for 8 wk exhibited increased levels of total cholesterol and triglycerides in the serum compared to mice fed on a control diet, although no difference was observed in the levels of LDL and HDL cholesterol between the groups. On the other hand, many studies have reported the inhibitory effect of UDCA on formation of cholesterol crystals, whereas opinions among scientists on the hypocholesterolemic effect are divided (Dorvash et al., 2018; Shan et al., 2008; Song et al., 2015). Liu et al. (2017) suggested that UDCA treatment of mice fed with a LD reduced the total cholesterol level. However, Song et al. (2015) reported no significant difference in the total cholesterol level between mice fed on a LD and LD with UDCA, although a lower level of triglycerides was observed in the LD with UDCA group than the LD group. Numerous studies have demonstrated that L. acidophilus and L. fermentum could positively modulate the serum lipid profiles (De Rodas et al., 1996; Lye et al., 2012). These results were consistent with our findings that levels of total cholesterol, LDL cholesterol, and triglycerides were reduced in the L. acidophilus ATCC 43121 group compared to the LD group (p<0.001), although no difference was found in total cholesterol content between the L. fermentum MF27 and LD groups (p>0.05). This decrease of serum cholesterol levels was associated with reduction of C:P ratio in the lactobacilli groups compared to the LD group (p<0.001). Increased C:P ratio causes supersaturation of gallbladder bile with cholesterol (Berr et al., 1992). Therefore, our results suggested that lactobacilli, especially L. acidophilus ATCC 43121, have the cholesterol-lowering effects in LD-induced C57BL/6J mice.

It is well known that polyunsaturated fatty acids (PUFAs), especially eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), play a critical role in regulating biological functions of the human body, and could positively affect on the serum biochemical indices (Cho et al., 2015; Sugiyama et al., 2008). These cholesterol-lowering effects in the serum may occur through modulating cholesterol metabolism in the liver (Sugiyama et al., 2008), and are associated with decreased activity of HMG CoA R, which is involved in cholesterol synthesis, in the liver (Ramaprasad et al., 2006). A similar result was observed in the current study, the LD+P1 mice with a lower expression of HMG CoA R exhibited a lower total cholesterol level than the LD mice with a higher expression of HMG CoA R (p<0.05). This result suggests that the hypocholesterolemic effects of the lactobacilli treatments occurred through suppression of HMG CoA R in the liver. Additionally, higher expression of CYP7A1 led to increased conversion of cholesterol to bile salts in the body (Liu et al., 2017). In this study, suppression of CYP7A1 in the LD+P2 group could be responsible for decreased bile acid synthesis in the liver, even though no difference was observed between the LD and LD+P1 groups.

Mucins are considered the major component of gallbladder mucus that provides the specific gel properties to protect the epithelium. Mucins are secreted by the mucous and submucosal cells in the epithelium (Chuang et al., 2012). However, altered expressions of mucins in the gallbladder could promote gallstone formation by accelerating cholesterol crystal nucleation in supersaturated bile (Bar Dayan et al., 2004). Notably, the gel-forming mucins, such as MUC2, MUC5AC, and MUC5B, play an important role in enhancing the gel properties and thus affect both the nuclear formation and enlargement of gallstones (Chuang et al., 2012; Zen et al., 2002). The membrane-bound mucins, including MUC1, do not form a mucous gel, but increased expression of these proteins was also associated with increased risk of the gallstone disease in human (Chuang et al., 2012; Wang et al., 2008). Thus, overexpression of MUC1, MUC2, MUC5AC, and MUC5B can participate in the gallstone formation with different lithogenic effects (Chuang et al., 2012). UDCA as a conservative treatment has demonstrated antilithiatic effect, which is associated with expression of MUC2, MUC5AC, and MUC5B, and reduced mucin secretion, as seen in the gallbladder bile (Jüngst et al., 2012; Kim et al., 2012). Cho et al. (2015) reported that PUFAs, including DHA and EPA, have the antilithogenic effects, as they led to reduced expression of MUC2, MUC5AC, and MUC5B genes in C57BL/6J mice. In the current study, L. acidophilus ATCC 43121 and L. fermentum MF27 were found to inhibit the expression of MUC5AC and MUC5B, although no significant effect was observed on the expression of MUC1 and MUC2 compared to the LD group. Thus, mucin genes involved in the cholesterol gallstone formation were differentially expressed following probiotic treatments used in this study.

Conclusion

Both L. acidophilus ATCC 43121 and L. fermentum MF27 positively affect the biochemical indices of the serum without impairing the growth rate in LD-induced C57BL/6J mice after 4 wk of treatment. These hypocholesterolemic effects in the serum, more evidently seen from L. acidophilus ATCC 43121, were mediated by a decreased expression of HMG CoA R in the liver. Additionally, these properties may contribute to decreased expression of gel-forming mucins, including MUC5AC and MUC5B, in the gallbladder. However, no differences were detected in the expressions of mucins between two strains. Thus, both lactobacilli have the preventive effect against the formation of cholesterol gallstones in the gallbladder in LD-induced C57BL/6J mice. Therefore, a steady intake of these lactobacilli can be used clinically to prevent the formation of cholesterol gallstones.

Conflicts of Interest

The authors declare no potential conflicts of interest.

Acknowledgements

This research was supported by the Seoul Dairy Cooperative.

Author Contributions

Conceptualization: Oh JK, Kim YR, Kim SH. Data curation: Oh JK, Choi YM. Formal analysis: Oh JK, Kim YR. Methodology: Oh JK, Kim YR. Software: Lee B. Validation: Lee B, Choi YM. Investigation: Oh JK. Writing - original draft: Oh JK, Kim SH, Choi YM. Writing - review & editing: Oh JK, Kim YR, Lee B, Choi YM, Kim SH.

Ethics Approval

The animal experiments were approved by the Korea University Institutional Animal Care and Use Committee (KUIACUC-69).

References

1.

Acalovschi M. 2014; Gallstones in patients with live cirrhosis: incidence, etiology, clinical and therapeutical aspects. World J Gastroenterol. 20:7277-7285

2.

Bar Dayan Y, Vilkin A, Niv Y. 2004; Gallbladder mucin plays a role in gallstone formation. Eur J Intern Med. 15:411-414

3.

Berr F, Schreiber E, Frick U. 1992; Interrelationships of bile acid and phospholipid fatty acid species with cholesterol saturation of duodenal bile in health and gallstone disease. Hepatology. 16:71-81

4.

Castro-Torres IG, de Jesús Cárdenas-Vázquez R, Velázquez-González C, VenturaMartínez R, De la O-Arciniega M, Naranjo-Rodríguez EB, Martínez-Vázquez M. 2015; Future therapeutic targets for the treatment and prevention of cholesterol gallstones. Eur J Pharmacol. 765:366-374

5.

Chen Y, Weng Z, Liu Q, Shao W, Guo W, Chen C, Jiao L, Wang Q, Lu Q, Sun H, Gu A, Hu H, Jiang Z. 2019; FMO3 and its metabolite TMAO contribute to the formation of gallstones. Biochim Biophys Acta Mol Basis Dis. 1865:2576-2585

6.

Cho SM, Park JA, Kim NH, Kim DS, Zhang D, Yi H, Cho HJ, Kim JK, Lee DK, Kim JS, Shin HC. 2015; Effect of eicosapentaenoic acid on cholesterol gallstone formation in C57BL/6J mice. Mol Med Rep. 11:362-366

7.

Chuang SC, Hsi E, Lee KT. 2012; Mucin genes in gallstone disease. Clin Chim Acta. 413:1466-1471

8.

De Rodas BZ, Gilliland SE, Maxwell CV. 1996; Hypocholesterolemic action of Lactobacillus acidophilus ATCC 43121 and calcium in swine with hypercholesterolemia induced by diet. J Dairy Sci. 79:2121-2128

9.

Deng J, Ren M, Dai X, Qu D, Yang M, Zhnag T, Jiang B. 2015; Lysimachia christinae hence regresses preestablished cholesterol gallstone in mice. J Ethnopharmacol. 166:102-108

10.

Dorvash MR, Khoshnood MJ, Saber H, Dehghanian A, Mosaddeghi P, Firouzabadi N. 2018; Metformin treatment prevents gallstone formation but mimics porcelain gallbladder in C57Bl/6 mice. Eur J Pharmacol. 833:165-172

11.

Guarino MPL, Cocca S, Altomare A, Emerenziani S, Cicala M. 2013; Ursodeoxycholic acid therapy in gallbladder disease, a story not yet completed. World J Gastroenterol. 19:5029-5034

12.

Jüngst C, Sreejayan N, Zündt B, Müller I, Spelsberg FW, Hüttl TP, Kullak‐Ublick GA, Del Pozo R, Jüngst D, Von Ritter C. 2008; Ursodeoxycholic acid reduces lipid peroxidation and mucin secretagogue activity in gallbladder bile of patients with cholesterol gallstones. Eur J Clin Invest. 38:634-639

13.

Kim JK, Cho SM, Kang SH, Kim E, Yi H, Yun ES, Lee DG, Cho HJ, Paik YH, Choi YK, Haam SJ, Shin HC, Lee DK. 2012; N-3 polyunsaturated fatty acid attenuates cholesterol gallstones by suppressing mucin production with a high cholesterol diet in mice. Gastroenterology. 27:1745-1751

14.

Kim Y, Whang JY, Whang KY, Oh S, Kim SH. 2008; Characterization of the cholesterol-reducing activity in a cell-free supernatant of Lactobacillus acidophilus ATCC 43121. Biosci Biotech Bioch. 72:1483-1490

15.

Lee J, Yun HS, Cho KW, Oh S, Kim SH, Chun T, Kim B, Whang KY. 2011; Evaluation of probiotic characteristics of newly isolated Lactobacillus spp.: Immune modulation and longevity. Int J Food Microbiol. 148:80-86

16.

Lee SP, Lim TH, Scott AJ. 1979; Carbohydrate moieties of glycoproteins in human hepatic and gallbladder bile, gallbladder mucosa and gallstones. Clin Sci. 56:533-538

17.

Liu M, Liu C, Chen H, Huang X, Zeng X, Zhou J, Mi S. 2017; Prevention of cholesterol gallstone disease by schaftoside in lithogenic diet-induced C57BL/6 mouse model. Eur J Pharmacol. 815:1-9

18.

Lye HS, Khoo BY, Karim AA, Rusul G, Liong MT. 2012; Ultrasound enhanced growth and cholesterol removal of Lactobacillus fermentum FTDC 1311 in the parent cells but not the subsequent passages. Ultrason Sonochem. 19:901-908

19.

National Research Council. 2010 National Research Council (US) for the update of the guide for the care and use of laboratory animals. 8th edNational Academies Press. Washington, DC, USA: .

20.

Oelschlaeger TA. 2010; Mechanisms of probiotic actions: A review. Int J Med Microbiol. 300:57-62

21.

Park YH, Kim JG, Shin YW, Kim SH, Whang KY. 2007; Effect of dietary inclusion of Lactobacillus acidophilus ATCC 43121 on cholesterol metabolism in rats. J Microbiol Biotechnol. 17:655-662.

22.

Purushortham A, Xu Q, Lu J, Foley JF, Yan X, Kim DH, Kemper JK, Li X. 2012; Hepatic deletion of SIRT1 decreases hepatocyte nuclear factor 1α/farnesoid X receptor signaling and induces formation of cholesterol gallstones in mice. Mol Cell Biol. 32:1226-1236

23.

Ramaprasad TR, Srinivasan K, Baskaran V, Sambaiah K, Lokesh BR. 2006; Spray-dried milk supplemented with α-linolenic acid or eicosapentaenoic acid and docosahexaenoic acid decreases HMG Co A reductase activity and increases biliary secretion of lipids in rats. Steroids. 71:409-415

24.

Shan D, Fang Y, Ye Y, Liu J. 2008; EGCG reducing the susceptibility to cholesterol gallstone formation through the regulation of inflammation. Biomed Pharmacother. 62:677-683

25.

Song XY, Xu S, Hu JF, Tang J, Chu SF, Liu H, Han N, Li JW, Zhang DM, Li YT, Chen NH. 2015; Piperine prevents cholesterol gallstone formation in mice. Eur J Pharmacol. 751:112-117

26.

Sugiyama E, Ishikawa Y, Li Y, Kagai T, Nobayashi M, Tanaka N, Kamijo Y, Yokoyama S, Hara A, Aoyama T. 2008; Eicosapentaenoic acid lowers plasma and liver cholesterol levels in the presence of peroxisome proliferators-activated receptor alpha. Life Sci. 83:19-28

27.

Vidyashankar S, Sambaiah K, Srinivasan K. 2010; Regression of preestablished cholesterol gallstones by dietary garlic and onion in experimental mice. Metabolism. 59:1402-1412

28.

Wang HH, Portincasa P, Wang DQH. 2008; Molecular pathophysiology and physical chemistry of cholesterol gallstones. Front Biosci. 13:401-423

29.

Yong CC, Lim J, Kim BK, Park DJ, Oh S. 2019; Suppressive effect of Lactobacillus fermentum Lim2 on Clostridioides difficile 027 toxin production. Lett Appl Microbiol. 68:386-393

30.

Zen Y, Harada K, Sasaki M, Tsuneyama K, Katayanagi K, Yamamoto Y, Nakanuma Y. 2002; Lipopolysaccharide induces overexpression of MUC2 and MUC5AC in cultured biliary epithelial cells: Possible key phenomenon of hepatolithiasis. Am J Pathol. 161:1475-1484

Change of publication charge


As day of June 1, 2021 (based on date of article submission), article processing charges (APC) will be applied to papers accepted after peer review as follows:
 

Author APC Remark
Member 1,000,000 KR won First and corresponding authors should pay membership fee to Korean Society for Food Science of Animal Resources.
Non-member in Korea 1,200,000 KR won
Other countries except Korea 500 US $ Affiliation of corresponding author

I don't want to open this window for a day.

Special Issue: 67th ICoMST 2021


The 67th International Congress of Meat Science and Technology (ICoMST) is currently accepting abstracts.

The deadline for submitting abstracts has been extended to April 15th, 2021, and FSAR will apply a 50% publishing fee discount to this special issue.

For more information, please check the website below.

https://www.icomst2021.com/

 


I don't want to open this window for a day.