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Prebiotic effects of commercial apple juice in high-fat diet fed rat

BMC Research Notes volume 17, Article number: 249 (2024) Cite this article

Abstract

Objectives

Apples are one of the most frequently consumed fruits and are effective in preventing lifestyle-related and other diseases. However, few studies have been conducted to evaluate health benefits of processed apple products such as juice. In this study, we analyzed the health benefits of consuming apple juice, focusing on changes in the gut microbiota, which plays an important role in maintaining human health.

Results

Rats were fed apple juice ad libitum, and the relative abundances of various gut microbiota in fecal samples were analyzed. In addition, rats treated apple juice were fed with a high-fat diet, and body weight, plasma triglyceride, glucose, and cholesterol levels were measured. The relative abundance of Clostridium cluster XIV did not change with the treatment of apple juice, but the relative abundance of Clostridium cluster IV was significantly decreased. In contrast, the relative abundances of Lactobacillus and Bifidobacterium, which provide benefits to the human body, were significantly increased by 3-fold and 10-fold, respectively, with apple juice consumption. When apple juice-treated rats were fed a high-fat diet, the increase in body weight, liver fat, and blood lipid parameters were all suppressed compared to high-fat alone group.

Conculusion

This study suggests that the consumption of apple juice changes the gut microbiota, exerts a prebiotic effect, and is effective in improving lifestyle-related diseases.

Peer Review reports

Introduction

In recent years, with the westernization of diet and changes in the social environment, the number of patients with lifestyle-related diseases has steadily increased. Since lifestyle-related diseases can lead to death if left untreated, their prevention and treatment have become important issues.

At present, food is gaining attention as a means of maintaining good health. In particular, the consumption of fruit is presumed to have health benefits. Apples (Malus domestica Borkh.) are consumed in large quantities. In recent years, the health effects of apples have been scientifically verified, and it has become clear that they are effective in preventing lifestyle-related diseases. For example, polyphenols and dietary fiber in apples have been reported to have antihyperlipidemic effects [1,2,3], antidiabetic effects [4,5,6], and intestinal function regulation [7, 8]. It has also been suggested that apple polyphenols may be able to alter gut microbiota, which could be used to prevent and treat diseases [9].

On the other hand, apples have many processed products, such as juice. Since these processed products contain the components of fresh apples, they can be expected to have the same health benefits as apples, but there is little scientific evidence for this. In this study, we conducted basic research on the effect of consuming commercially available apple juice. We focused on the gut microbiota, which plays an important role in maintaining human health, and assessed changes in the gut microbiota associated with apple juice consumption. We also examined the effects of apple juice on rats fed a high-fat diet.

Materials and methods

Apple juice

In this study, we used two commercial apple juice products made from different cultivars, namely, “Malus domestica Borkh. cv Tsugaru” or “Malus domestica Borkh. cv Fuji” (Shiny Apple®; Aomoriken Ringo Juice Co. Ltd., Aomori, Japan). These are 100% apple juices that have not been heat treated or filtered during the manufacturing process. These are referred to as apple juice T (AJ-T) and apple juice F (AJ-F), respectively.

Animals

Wistar rats were purchased from Japan SLC Co., Ltd. (Shizuoka, Japan). The rats were subjected to experiments following 1 week of acclimatization. Animals were kept at 24 ± 1 °C and 55 ± 15% humidity on a 12 h light/dark cycle (lights on at 8:00 A.M.). This experiment was conducted with approval from Hoshi University (approval number: 29–103 and 29–154).

Treatments

Experiment 1; The rats (seven weeks old, male) were divided into 3 groups and given purified water, AJ-T, or AJ-F freely for 2 weeks. The animals were sacrificed under deep anesthesia with overdose isoflurane inhalation, and the white adipose tissues were removed and weighed. The feces were collected from the large intestine and frozen at -80 °C. Blood was collected using a heparinized syringe, and plasma was separated (1,000×g, 15 min, 4 °C).

Experiment 2; Three weeks old rats were divided into four groups: a control group, a high-fat diet group (HF group), AJ-T/HF, or AJ-F/HF group. The control group was given a control diet (D12450J, 10 kcal% fat, Research Diets, New Brunswick, NJ, USA) and purified water ad libitum during the experimental period. The HF group was given a control diet and purified water ad libitum for 3 weeks from the age of 3 weeks, and then given a high-fat diet (D12492, 60 kcal% fat, Research Diets) for 16 weeks. The AJ-T/HF or AJ-F/HF group was given a control diet and AJ-T or AJ-F ad libitum for 3 weeks from the age of 3 weeks, and then a high-fat diet for 16 weeks. The animals were sacrificed under deep anesthesia with overdose isoflurane inhalation, and the white adipose tissues and liver were removed and weighed. Blood was collected using a heparinized syringe, and plasma was separated.

Measurement of plasma glucose, triglyceride, and cholesterol levels

Plasma glucose, triglyceride, and cholesterol levels were measured using the Glucose C-II-Test Wako, Triglyceride E-Test Wako, and Cholesterol E-Test Wako, respectively (Wako Pure Chemical Industries, Ltd., Osaka, Japan). Each plasma concentrations were calculated based on the standard samples provided with the kit.

Glucose; A 2 µL of plasma was placed in a 96-well plate, and 200 µL of reaction reagent (included in the kit) was added. After shaking, the plate was incubated at 37 °C for 15 min, and the absorbance was measured using a microplate reader.

Triglyceride; A 2 µL of plasma was placed in a 96-well plate, and 200 µL of reaction reagent (included in the kit) was added. After shaking, the plate was incubated at 37 °C for 5 min, and the absorbance was measured using a microplate reader.

Cholesterol; A 2 µL of plasma was placed in a 96-well plate, and 200 µL of reaction reagent (included in the kit) was added. After shaking, the plate was incubated at 37 °C for 5 min, and the absorbance was measured using a microplate reader.

Analysis of the gut microbiota

Extraction of bacterial DNA from fecal samples was performed using the QIAamp DNA Stool Mini Kit (QIAGEN, Hilden, Germany). The quality of extracted DNA was analyzed by the absorbance ratio of 260 nm to 280 nm using NanoDrop spectrophotometer (Thermo Fisher Scientific, Waltham, MA, USA). A 260/280 ratio of all samples was within the range of 1.8 to 2.1. The primers shown in Table 1 were prepared, and real-time PCR was performed to detect bacteria. Briefly, SsoAdvanced Universal SYBR Green Supermix (Bio-Rad Laboratories Inc., Hercules, CA, USA), forward primer, reverse primer, and DNA solution were added to each well of the PCR plate and mixed. Fluorescence intensity during the amplification process was monitored with a CFX Connect Real-Time PCR System (Bio-Rad Laboratories Inc.). The temperature conditions were as follows: 95 °C for 30 s as the denaturation temperature, 58 °C for 30 s as the annealing temperature, and 72 °C for 60 s as the elongation temperature. Bacterial 16S rRNA gene copies were determined by real-time PCR using universal bacterial primer sequences and normalized to total DNA.

Table 1 PCR primers for the detection of bacteria
Full size table

Measurement of liver triglyceride content

A portion (100 mg) of liver tissue was homogenized in phosphate buffer saline. The homogenate was extracted with isopropyl alcohol, and the extract was analyzed using a Triglyceride E-Test Wako to determine liver triglyceride content.

Statistical analysis

Experimental values are expressed as the mean ± standard deviation (S.D.). The statistical significance of differences was evaluated by one-way analysis of variance followed by Dunnett’s test or Tukey’s test. All analyses were performed using BellCurve for Excel (Social Survey Research Information Co., Ltd., Tokyo, Japan). A p value of less than 0.05 was considered statistically significant.

Results

Effects of apple juice consumption on body weight and white adipose tissue weight

Body weight and white adipose tissue weight were measured after drinking AJ-T or AJ-F for 2 weeks (Table 2).

Table 2 Body weight and white adipose tissue weight
Full size table

The body weights of both the AJ-T-treated and AJ-F-treated groups were almost the same as those of the normal group. The epididymal white adipose tissue weight of the AJ-T-treated group was almost the same as that of the normal group. In addition, no difference was observed between the AJ-T-treated group and the normal group in the weight of retroperitoneal and perirenal white adipose tissue. Furthermore, in the AJ-F-treated group as well as in the AJ-T-treated group, there was no change in white adipose tissue weight.

These results showed that the intake of apple juice for 2 weeks had no effect on body weight or white adipose tissue weight.

Plasma glucose levels, triglyceride levels, and cholesterol levels

Plasma glucose levels, triglyceride levels, and cholesterol levels after administration of apple juice were measured (Table 3).

Table 3 Plasma glucose levels, triglyceride levels, and cholesterol levels
Full size table

The plasma glucose concentration of the AJ-T-treated group was almost the same as that of the normal group. In addition, no difference was observed between the AJ-T-treated group and the normal group in plasma triglyceride or cholesterol concentrations. Furthermore, in the AJ-F-treated group, as in the AJ-T-treated group, there was no change in the plasma glucose, triglyceride, or cholesterol concentrations.

These results showed that the intake of apple juice for 2 weeks did not affect plasma glucose, triglyceride, or cholesterol levels.

Analysis of the gut microbiota at the phylum level

The gut microbiota is classified by phylum, class, order, family, genus, and species. 99% of the gut microbiota in humans belongs to four phyla: Firmicutes, Bacteroidetes, Proteobacteria, and Actinobacteria [10]. Therefore, we analyzed how the gut microbiota of rats changed in response to apple juice consumption at the phylum level (Fig. 1).

Fig. 1
figure 1

Analysis of the gut microbiota at the phylum level. Rats were given purified water, AJ-T, or AJ-F ad libitum for 2 weeks. After treatment, DNA was extracted from fecal samples, and the phyla Bacteroidetes, Proteobacteria, Actinobacteria, and Firmicutes were analyzed by real-time PCR. The relative abundance of the gut microbiota was normalized to 16S rRNA, and the average value of the normal group was shown as 100% (mean ± S.D., n = 6, *; p < 0.05 vs. normal group)

Full size image

There was no difference between the normal group and the apple juice-treated groups in the phyla Bacteroidetes and Proteobacteria. The treatment of AJ-T or AJ-F increased the relative abundance of the phylum Actinobacteria. On the other hand, it was found that the relative abundance of the phylum Firmicutes was significantly decreased by the consumption of AJ-T and AJ-F compared to the normal group.

Analysis of Clostridium cluster IV and XIV

Apple juice treatment decreased the relative abundance of the phylum Firmicutes (Fig. 1). It is known that the genus Clostridium in the phylum Firmicutes is involved in the development of lifestyle-related diseases [11, 12]. Therefore, we investigated how the intake of apple juice changes the relative abundance of the bacterium Clostridium (Fig. 2).

Fig. 2
figure 2

Analysis of Clostridium cluster IV and XIV, Lactobacillus, and Bifidobacterium. Rats were given purified water, AJ-T, or AJ-F ad libitum for 2 weeks. After treatment, DNA was extracted from fecal samples, and Clostridium cluster IV, Clostridium cluster XIV, Lactobacillus genus, Bifidobacterium genus, L. reuteri, L. acidophilus, and L. johnsonii were analyzed by real-time PCR. The relative abundance of the gut microbiota was normalized to 16S rRNA, and the average value of the normal group was shown as 100% (mean ± S.D., n = 6, *; p < 0.05, **; p < 0.01 vs. normal group)

Full size image

The treatment of AJ-T and AJ-F to rats for 2 weeks significantly decreased the relative abundance of Clostridium cluster IV compared to the normal group (Fig. 2). On the other hand, Clostridium cluster XIV showed no change in either apple juice treatment.

Analysis of Lactobacillus and Bifidobacterium

Gut microbiota are known to provide benefits to the host. Some of these bacterial strains are used as probiotics, and representative examples include the genera Lactobacillus and Bifidobacterium [13,14,15]. Therefore, we investigated how the relative abundances of Lactobacillus and Bifidobacterium change with apple juice intake (Fig. 2).

The relative abundance of Lactobacillus genus in the AJ-T-treated group was significantly higher than that in the normal group by approximately 3 times. L. reuteri, a representative useful bacterium, was not changed by AJ-T treatment. However, the relative abundances of L. acidophilus and L. johnsonii were significantly increased by treatment of AJ-T compared to the normal group. In addition, the relative abundance of Bifidobacterium genus in the AJ-T-treated group was significantly increased by approximately 10 times compared to that in the normal group. These changes were also observed in the AJ-F-treated group.

Effects of apple juice on body weight gain in high-fat fed rats

From these results, it was clarified that the gut microbiota involved in lifestyle-related diseases were altered due to consumption apple juice. Therefore, we investigated the effects of apple juice on body weight in high-fat diet fed rats (Fig. 3).

Fig. 3
figure 3

Body weight and white adipose tissue weight. Rats were given HF diet and purified water, AJ-T, or AJ-F (A). Body weight (B) and the whole white adipose tissue (C) were measured (mean ± S.D., n = 5–6, ***; p < 0.001 vs. control group, #; p < 0.05, ###; p < 0.001 vs. HF group)

Full size image

The body weight of the rats fed with a high-fat diet for 16 weeks increased compared to the control group, and the body weight on the final day was about 1.2 times that of the control group. The white adipose tissue weight in the HF group also showed significantly higher than those in the control group. In contrast, the body weight and white adipose tissue weight in the AJ-T/HF group, which was given AJ-T before HF treatment, were all significantly lower than those in the HF group. Furthermore, the same tendency as the AJ-F/HF group was observed in the AJ-F/HF group as well.

These results indicate that pre-consumption of apple juice suppresses weight gain induced by a high-fat diet.

Effects of apple juice on liver fat accumulation and lipid metabolism in high-fat fed rats

We investigated the preventive effects of apple juice on liver fat accumulation, blood glucose, triglyceride, and cholesterol levels in rats fed a high-fat diet (Fig. 4).

Fig. 4
figure 4

Liver weight, triglyceride contents, plasma glucose, triglyceride, and cholesterol levels. Rats were given HF diet and purified water, AJ-T, or AJ-F. The liver weight (A) and triglyceride contents (B) were measured. Blood was collected, and plasma glucose (C), triglyceride (D), and cholesterol levels (E) were measured (mean ± S.D., n = 5–6, *; p < 0.05 vs. normal group, **; p < 0.01 vs. control group, #; p < 0.05 vs. HF group)

Full size image

The liver weight and liver triglyceride content in HF group showed significantly higher than those in the control group. Moreover, blood glucose levels in the HF group were higher than those in the control group. In addition, although there was no difference in blood cholesterol concentration between the HF group and the control group, the blood triglyceride concentration was significantly higher. In contrast, the liver weight, liver triglyceride content, the blood glucose, and triglyceride concentrations in the AJ-T/HF or AJ-F/HF groups were significantly lower than those in the HF group.

These results indicated that pre-consumption of apple juice suppressed fatty liver and abnormalities in lipid metabolism induced by a high-fat diet.

Discussion

In this study, to investigate the health benefits of consuming commercially available apple juice, we analyzed changes in the gut microbiota. Normal rats were given two different types of apple juice for two weeks. These are 100% apple juices that have not been heat treated or filtered during the manufacturing process.

The human gut is home to an abundant and diverse community of bacteria; each person carries approximately 100 trillion bacterial cells, representing more than 1,000 different species [10]. The abundance of gut microbiota changes depending on diet [16,17,18] and drug intake [19,20,21]. In recent years, gut microbiota have been reported to change dynamically during the onset of ulcerative colitis [22], obesity [23, 24], and diabetes [25], and the importance of gut microbiota as a factor in the onset and exacerbation of these diseases has been highlighted. In addition, the involvement of gut microbiota in the development of skin diseases such as atopic dermatitis has been reported, and the role of the gut microbiota in the maintenance of skin function is attracting attention [26, 27]. Thus, the gut microbiota plays a very important role in maintaining human health. We focused on the genus Clostridium, which has been reported to be involved in metabolic diseases [11, 12], and the genera Lactobacillus and Bifidobacterium, which are useful gut microbiota that are used as probiotics [13,14,15], and analyzed the health effects of apple juice based on changes in the abundance of these genera. When apple juice was treated to normal rats, the relative abundance of gut microbiota at the phylum level changed greatly (Fig. 1). In addition, Clostridium cluster IV was significantly decreased by the apple juice treatment. In contrast, intake of apple juice markedly increased Lactobacillus genus by approximately 3-fold and the relative abundance of Bifidobacterium genus by approximately 10-fold (Fig. 2). However, no effect was observed on body weight, white adipose tissue weight, plasma glucose, triglyceride, or cholesterol concentration in the apple juice-treated groups (Tables 2 and 3).

We speculated that the reasons why apple juice intake did not affect body weight and blood lipid levels were that the administration period was short and that the study was conducted in normal rats. Based on the result of experiment 1, we next investigated the effect of apple juice on rats fed a high-fat diet [28, 29]. The body weight, white adipose tissue weight, liver triglyceride content, blood glucose concentration, and blood triglyceride concentration in the HF group were all significantly increased compared to the control group, and obesity, fatty liver, and dyslipidemia were induced. It was shown that both were significantly decreased in rats pretreated with apple juice (Figs. 3 and 4). There was little difference in food and water intakes between the HF group and apple juice treatment groups (data not shown). From the above results, it was clarified that although apple juice does not affect normal body weight or blood lipid levels, it has the effect of improving body weight gain and abnormal blood lipid levels due to HF intake. In addition, it was considered possible that this effect was due to a prebiotic effect.

Among Lactobacillus genus, the relative abundances of L. acidophilus and L. johnsonii were significantly increased by apple juice treatment (Fig. 2). These gut microbiota are reported to have various beneficial effects, including regulating the intestinal function and improving allergic diseases [30,31,32]. Also, anti-obesity effect has been reported as a probiotic effect of Lactobacillus strain or Bifidobacterium strain [33, 34]. In the future, we plan to demonstrate the health effects of apple juice using animal models.

In summary, treatment of apple juice to normal rats significantly changed the gut microbiota. In addition, prophylactic administration of apple juice may improve liver fat accumulation and lipid metabolism through prebiotic effects. Since apple juice is a readily available food, its prebiotic effects are of great interest. In the future, we believe that the value of human consumption of apple juice will be confirmed and its active ingredient discovered.

Data availability

No datasets were generated or analysed during the current study.

References

  1. Esmael OA, Sonbul SN, Kumosani TA, Moselhy SS. Hypolipidemic effect of fruit fibers in rats fed with high dietary fat. Toxicol Ind Health. 2015;31(3):281–8.

    Article  CAS  PubMed  Google Scholar 

  2. Nagasako-Akazome Y, Kanda T, Ohtake Y, Shimasaki H, Kobayashi T. Apple polyphenols influence cholesterol metabolism in healthy subjects with relatively high body mass index. J Oleo Sci. 2007;56(8):417–28.

    Article  CAS  PubMed  Google Scholar 

  3. Osada K, Suzuki T, Kawakami Y, Senda M, Kasai A, Sami M, et al. Dose-dependent hypocholesterolemic actions of dietary apple polyphenol in rats fed cholesterol. Lipids. 2006;41(2):133–9.

    Article  CAS  PubMed  Google Scholar 

  4. Shoji T, Yamada M, Miura T, Nagashima K, Ogura K, Inagaki N, et al. Chronic administration of apple polyphenols ameliorates hyperglycaemia in high-normal and borderline subjects: a randomised, placebo-controlled trial. Diabetes Res Clin Pract. 2017;129:43–51.

    Article  CAS  PubMed  Google Scholar 

  5. Ogura K, Ogura M, Shoji T, Sato Y, Tahara Y, Yamano G, et al. Oral administration of Apple Procyanidins ameliorates insulin resistance via suppression of pro-inflammatory cytokine expression in Liver of Diabetic ob/ob mice. J Agric Food Chem. 2016;64(46):8857–65.

    Article  CAS  PubMed  Google Scholar 

  6. Gorjanovic S, Micic D, Pastor F, Tosti T, Kalusevic A, Ristic S et al. Evaluation of Apple Pomace Flour obtained industrially by dehydration as a source of biomolecules with antioxidant, antidiabetic and Antiobesity effects. Antioxid (Basel). 2020;9(5).

  7. Saito T, Miyake M, Toba M, Okamatsu H, Shimizu S, Noda M. Inhibition by apple polyphenols of ADP-ribosyltransferase activity of cholera toxin and toxin-induced fluid accumulation in mice. Microbiol Immunol. 2002;46(4):249–55.

    Article  CAS  PubMed  Google Scholar 

  8. Niwa T, Nakao M, Hoshi S, Yamada K, Inagaki K, Nishida M, et al. Effect of dietary fiber on morphine-induced constipation in rats. Biosci Biotechnol Biochem. 2002;66(6):1233–40.

    Article  CAS  PubMed  Google Scholar 

  9. Wang X, Liu F, Cui Y, Yin Y, Li S, Li X. Apple Polyphenols extracts ameliorate high Carbohydrate Diet-Induced Body Weight Gain by regulating the gut microbiota and appetite. J Agric Food Chem. 2022;70(1):196–210.

    Article  CAS  PubMed  Google Scholar 

  10. Sartor RB. Microbial influences in inflammatory bowel diseases. Gastroenterology. 2008;134(2):577–94.

    Article  CAS  PubMed  Google Scholar 

  11. Yamaguchi Y, Adachi K, Sugiyama T, Shimozato A, Ebi M, Ogasawara N, et al. Association of Intestinal Microbiota with metabolic markers and Dietary habits in patients with type 2 diabetes. Digestion. 2016;94(2):66–72.

    Article  CAS  PubMed  Google Scholar 

  12. Respondek F, Gerard P, Bossis M, Boschat L, Bruneau A, Rabot S, et al. Short-chain fructo-oligosaccharides modulate intestinal microbiota and metabolic parameters of humanized gnotobiotic diet induced obesity mice. PLoS ONE. 2013;8(8):e71026.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Steenbergen L, Sellaro R, van Hemert S, Bosch JA, Colzato LS. A randomized controlled trial to test the effect of multispecies probiotics on cognitive reactivity to sad mood. Brain Behav Immun. 2015;48:258–64.

    Article  PubMed  Google Scholar 

  14. Papizadeh M, Rohani M, Nahrevanian H, Javadi A, Pourshafie MR. Probiotic characters of Bifidobacterium and Lactobacillus are a result of the ongoing gene acquisition and genome minimization evolutionary trends. Microb Pathog. 2017;111:118–31.

    Article  CAS  PubMed  Google Scholar 

  15. Invernici MM, Salvador SL, Silva PHF, Soares MSM, Casarin R, Palioto DB, et al. Effects of Bifidobacterium probiotic on the treatment of chronic periodontitis: a randomized clinical trial. J Clin Periodontol. 2018;45(10):1198–210.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Tajima M, Ikarashi N, Igeta S, Toda T, Ishii M, Tanaka Y, et al. Different diets cause alterations in the enteric environment and trigger changes in the expression of hepatic cytochrome P450 3A, a drug-metabolizing enzyme. Biol Pharm Bull. 2013;36(4):624–34.

    Article  CAS  PubMed  Google Scholar 

  17. Ikarashi N, Ogawa S, Hirobe R, Kon R, Kusunoki Y, Yamashita M, et al. Epigallocatechin gallate induces a hepatospecific decrease in the CYP3A expression level by altering intestinal flora. Eur J Pharm Sci. 2017;100:211–8.

    Article  CAS  PubMed  Google Scholar 

  18. O’Keefe SJ, Li JV, Lahti L, Ou J, Carbonero F, Mohammed K, et al. Fat, fibre and cancer risk in African americans and rural africans. Nat Commun. 2015;6:6342.

    Article  PubMed  Google Scholar 

  19. Toda T, Ohi K, Kudo T, Yoshida T, Ikarashi N, Ito K, et al. [Antibiotics suppress Cyp3a in the mouse liver by reducing lithocholic acid-producing intestinal flora]. Yakugaku Zasshi. 2009;129(5):601–8.

    Article  CAS  PubMed  Google Scholar 

  20. Maier L, Pruteanu M, Kuhn M, Zeller G, Telzerow A, Anderson EE, et al. Extensive impact of non-antibiotic drugs on human gut bacteria. Nature. 2018;555(7698):623–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Imhann F, Bonder MJ, Vich Vila A, Fu J, Mujagic Z, Vork L, et al. Proton pump inhibitors affect the gut microbiome. Gut. 2016;65(5):740–8.

    Article  CAS  PubMed  Google Scholar 

  22. Nishida A, Inoue R, Inatomi O, Bamba S, Naito Y, Andoh A. Gut microbiota in the pathogenesis of inflammatory bowel disease. Clin J Gastroenterol. 2018;11(1):1–10.

    Article  PubMed  Google Scholar 

  23. Trikha SRJ, Lee DM, Ecton KE, Wrigley SD, Vazquez AR, Litwin NS, et al. Transplantation of an obesity-associated human gut microbiota to mice induces vascular dysfunction and glucose intolerance. Gut Microbes. 2021;13(1):1940791.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Aron-Wisnewsky J, Warmbrunn MV, Nieuwdorp M, Clement K. Metabolism and metabolic disorders and the Microbiome: the intestinal microbiota Associated with obesity, lipid metabolism, and Metabolic Health-Pathophysiology and therapeutic strategies. Gastroenterology. 2021;160(2):573–99.

    Article  CAS  PubMed  Google Scholar 

  25. Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490(7418):55–60.

    Article  CAS  PubMed  Google Scholar 

  26. Reddel S, Del Chierico F, Quagliariello A, Giancristoforo S, Vernocchi P, Russo A, et al. Gut microbiota profile in children affected by atopic dermatitis and evaluation of intestinal persistence of a probiotic mixture. Sci Rep. 2019;9(1):4996.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Ikarashi N, Fujitate N, Togashi T, Takayama N, Fukuda N, Kon R et al. Acacia Polyphenol ameliorates atopic dermatitis in Trimellitic Anhydride-Induced Model mice via changes in the gut microbiota. Foods. 2020;9(6).

  28. Molina-Tijeras JA, Diez-Echave P, Vezza T, Hidalgo-Garcia L, Ruiz-Malagon AJ, Rodriguez-Sojo MJ, et al. Lactobacillus fermentum CECT5716 ameliorates high fat diet-induced obesity in mice through modulation of gut microbiota dysbiosis. Pharmacol Res. 2021;167:105471.

    Article  CAS  PubMed  Google Scholar 

  29. Mukai K, Horike SI, Meguro-Horike M, Nakajima Y, Iswara A, Nakatani T. Topical estrogen application promotes cutaneous wound healing in db/db female mice with type 2 diabetes. PLoS ONE. 2022;17(3):e0264572.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Nakata J, Hirota T, Umemura H, Nakagawa T, Kando N, Futamura M, et al. Additive effect of Lactobacillus acidophilus L-92 on children with atopic dermatitis concomitant with food allergy. Asia Pac Allergy. 2019;9(2):e18.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Inoue R, Nishio A, Fukushima Y, Ushida K. Oral treatment with probiotic Lactobacillus johnsonii NCC533 (La1) for a specific part of the weaning period prevents the development of atopic dermatitis induced after maturation in model mice, NC/Nga. Br J Dermatol. 2007;156(3):499–509.

    Article  CAS  PubMed  Google Scholar 

  32. Hrdy J, Couturier-Maillard A, Boutillier D, Lapadatescu C, Blanc P, Prochazka J, et al. Oral supplementation with selected Lactobacillus acidophilus triggers IL-17-dependent innate defense response, activation of innate lymphoid cells type 3 and improves colitis. Sci Rep. 2022;12(1):17591.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Wu T, Sun M, Liu R, Sui W, Zhang J, Yin J, et al. Bifidobacterium longum subsp. Longum Remodeled Roseburia and phosphatidylserine levels and ameliorated intestinal disorders and liver metabolic abnormalities Induced by High-Fat Diet. J Agric Food Chem. 2020;68(16):4632–40.

    Article  CAS  PubMed  Google Scholar 

  34. Song W, Song C, Li L, Wang T, Hu J, Zhu L, et al. Lactobacillus alleviated obesity induced by high-fat diet in mice. J Food Sci. 2021;86(12):5439–51.

    Article  CAS  PubMed  Google Scholar 

  35. De Bacchetti T, Aldred N, Clare AS, Burgess JG. Improvement of phylum- and class-specific primers for real-time PCR quantification of bacterial taxa. J Microbiol Methods. 2011;86(3):351–6.

    Article  Google Scholar 

  36. Siefring S, Varma M, Atikovic E, Wymer L, Haugland RA. Improved real-time PCR assays for the detection of fecal indicator bacteria in surface waters with different instrument and reagent systems. J Water Health. 2008;6(2):225–37.

    Article  CAS  PubMed  Google Scholar 

  37. Queipo-Ortuno MI, Seoane LM, Murri M, Pardo M, Gomez-Zumaquero JM, Cardona F, et al. Gut microbiota composition in male rat models under different nutritional status and physical activity and its association with serum leptin and ghrelin levels. PLoS ONE. 2013;8(5):e65465.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Matsuki T, Watanabe K, Fujimoto J, Takada T, Tanaka R. Use of 16S rRNA gene-targeted group-specific primers for real-time PCR analysis of predominant bacteria in human feces. Appl Environ Microbiol. 2004;70(12):7220–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Matsuki T, Watanabe K, Fujimoto J, Miyamoto Y, Takada T, Matsumoto K, et al. Development of 16S rRNA-gene-targeted group-specific primers for the detection and identification of predominant bacteria in human feces. Appl Environ Microbiol. 2002;68(11):5445–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Song Y, Liu C, Finegold SM. Real-time PCR quantitation of clostridia in feces of autistic children. Appl Environ Microbiol. 2004;70(11):6459–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Penders J, Vink C, Driessen C, London N, Thijs C, Stobberingh EE. Quantification of Bifidobacterium spp., Escherichia coli and Clostridium difficile in faecal samples of breast-fed and formula-fed infants by real-time PCR. FEMS Microbiol Lett. 2005;243(1):141–7.

    Article  CAS  PubMed  Google Scholar 

  42. Byun R, Nadkarni MA, Chhour KL, Martin FE, Jacques NA, Hunter N. Quantitative analysis of diverse Lactobacillus species present in advanced dental caries. J Clin Microbiol. 2004;42(7):3128–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Song Y, Kato N, Liu C, Matsumiya Y, Kato H, Watanabe K. Rapid identification of 11 human intestinal Lactobacillus species by multiplex PCR assays using group- and species-specific primers derived from the 16S-23S rRNA intergenic spacer region and its flanking 23S rRNA. FEMS Microbiol Lett. 2000;187(2):167–73.

    CAS  PubMed  Google Scholar 

  44. Malinen E, Kassinen A, Rinttila T, Palva A. Comparison of real-time PCR with SYBR Green I or 5’-nuclease assays and dot-blot hybridization with rDNA-targeted oligonucleotide probes in quantification of selected faecal bacteria. Microbiol (Reading). 2003;149(Pt 1):269–77.

    Article  CAS  Google Scholar 

  45. Furet JP, Quenee P, Tailliez P. Molecular quantification of lactic acid bacteria in fermented milk products using real-time quantitative PCR. Int J Food Microbiol. 2004;97(2):197–207.

    Article  CAS  PubMed  Google Scholar 

  46. Mohammadi T, Pietersz RN, Vandenbroucke-Grauls CM, Savelkoul PH, Reesink HW. Detection of bacteria in platelet concentrates: comparison of broad-range real-time 16S rDNA polymerase chain reaction and automated culturing. Transfusion. 2005;45(5):731–6.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Ms. Manami Ozaki for their technical assistance.

Funding

This study was funded by the Lotte Shigemitsu Prize.

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Authors and Affiliations

  1. Department of Biomolecular Pharmacology, Hoshi University, 2-4-41 Ebara, Shinagawa-ku, Tokyo, 142-8501, Japan

    Risako Kon, Nobutomo Ikarashi, Mayumi Ohkuma, Misato Toyonaga, Rei Tomimoto, Hiroyasu Sakai & Tomoo Hosoe

  2. Juntendo Advanced Research institute for Health Science, Juntendo University, Bunkyo City, Japan

    Junzo Kamei

Authors
  1. Risako Kon
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  2. Nobutomo Ikarashi
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  3. Mayumi Ohkuma
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  6. Hiroyasu Sakai
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  7. Tomoo Hosoe
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Contributions

Data collection and analysis were performed by Risako Kon, Mayumi Ohkuma, Misato Toyonaga, and Rei Tomimoto. The first draft of the manuscript was written by Risako Kon and Nobutomo Ikarashi. The review and editing were performed by Hiroyasu Sakai, Tomoo Hosoe, and Junzo Kamei. All authors reviewed the manuscript.

Corresponding author

Correspondence to Nobutomo Ikarashi.

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The authors declare no competing interests.

Ethics approval and consent to participate

The research reported in this study involved rats. This animal experiment was conducted with approval and in accordance with the Hoshi University Guiding Principles for the Care and Use of Laboratory Animals (approval number: 29–103 and 29–154). This study is reported in accordance with ARRIVE guidelines.

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Kon, R., Ikarashi, N., Ohkuma, M. et al. Prebiotic effects of commercial apple juice in high-fat diet fed rat. BMC Res Notes 17, 249 (2024). https://doi.org/10.1186/s13104-024-06907-4

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  • DOI: https://doi.org/10.1186/s13104-024-06907-4

Keywords

BMC Research Notes

ISSN: 1756-0500

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