Apples and Cardiovascular Health—Is the Gut Microbiota a Core Consideration?
Abstract
:1. Introduction
2. Apple Components
Components | Value per 100 g |
---|---|
Energy (kcal) | 52 |
Energy (kJ) | 218 |
Water (g) | 85.56 |
Total carbohydrates (g) | 13.81 |
§ Total dietary fiber (g) | 2.21 |
§ Insoluble fiber (g) | 1.54 |
§ Soluble fiber (g) | 0.67 |
Total sugars (g) | 10.39 |
Fructose (g) | 5.9 |
Glucose (dextrose) (g) | 2.43 |
Sucrose (g) | 2.07 |
Starch (g) | 0.05 |
Protein (g) | 0.26 |
Total lipid (fat) (g) | 0.17 |
Fatty acids, total polyunsaturated (g) | 0.051 |
Fatty acids, total monounsaturated (g) | 0.007 |
Fatty acids, total saturated (g) | 0.028 |
Vitamin C, total ascorbic acid (mg) | 4.6 |
Thiamin (mg) | 0.017 |
Riboflavin (mg) | 0.026 |
Niacin (mg) | 0.091 |
Vitamin B-6 (mg) | 0.041 |
Folate, DFE (μg) | 3 |
Vitamin A, RAE (μg) | 3 |
Vitamin A, IU (IU) | 54 |
Vitamin E (alpha-tocopherol) (mg) | 0.18 |
Vitamin K (phylloquinone) (μg) | 2.2 |
Calcium, Ca (mg) | 6 |
Iron, Fe (mg) | 0.12 |
Magnesium, Mg (mg) | 5 |
Phosphorus, P (mg) | 11 |
Potassium, K (mg) | 107 |
Sodium, Na (mg) | 1 |
Zinc, Zn (mg) | 0.04 |
* Total polyphenols (mg) | 110.20 |
* Flavanols (mg) | 96.33 |
* Hydroxycinnamates (mg) | 14.21 |
* Flavonols (mg) | 5.66 |
* Dihydrochalcones (mg) | 4.17 |
# Anthocyanins (mg) | 1.62 |
2.1. Apple Fiber
2.2. Apple Polyphenols
2.2.1. Absorption and Bioavailability of Apple Polyphenols
3. The Human Gut Microbiota—Effects of Fiber and Polyphenols
3.1. Impact of Apple Components on the Gut Microbiota Composition
3.1.1. In vitro Studies
3.1.2. Animal Studies
3.1.3. Human Studies
Type of Study | Duration-Diets-Daily Dose | Techniques Used | Results | Author |
---|---|---|---|---|
Animal (Wistar rats) | 6 weeks, 10 rats for each group: Control diet or 5% apple pomace (AP) 1B-juice colloids extract (54.3% soluble and 2.6% insoluble fiber) or 5% AP 4B-juice colloids extract, rich in soluble fiber (78.3% soluble and 1.8% insoluble) or 5% alcohol AP extract, rich in insoluble fiber (22.9% soluble and 73.3% insoluble) | FISH (caecal) Plate count (feaces) | B-juice AP extracts: Total SCFA, acetate and propionate: ↑, pH: ↓ Bacteroidaceae: ↑ (faeces) Alcohol AP extract: Total SCFA and butyrate: ↑, pH: ↓ Bacteroidaceae: ↑ (faeces) Eubacterium rectale: ↑ (caecal) | Sembries et al. (2003) [24] |
Animal (Wistar rats) | 4 weeks, 12 rats for each group: Control diet or Extraction juice from apple pomace | Plate count | Total SCFA and acetate: ↑, pH: ↓ Lactobacillus: ↑ , Bifidobacterium: ↑ Primary bile acids and neutral sterols: ↑ Secondary bile acids: ↓ | Sembries et al., 2006 [25] |
Animal (Fischer rats) | 4 weeks, 8 rats for each group: Control diet or 10 g apple or 7% apple pectin | qPCR | Apple: Butyrate: ↑, pH: ↓, Bacteroides spp: ↓ Apple pectin: Butyrate:↑, pH: ↓, Bacteroides spp: ↓, Clostridium coccoides:↑ | Licht et al., 2010 [26] |
Animal ex vivo (mice) | Granny Smith apple fermented in vitro from faeces from diet induced lean (control) and obese mice. | qPCR | Firmicutes, Bacteroidetes, Enterococcus, Enterobacteriaceae, Escherichia coli and Bifidobacterium abundances from obese mice tended to be similar to lean mice after apple fermentation. | Condezo-Hoyos et al., 2014 [118] |
Human | 2 weeks, 8 subjects: 2 apples | Plate count | Bifidobacteria: ↑ Clostridia: ↓, Enterobacteriaceae: ↓ | Shinohara et al., 2010 [27] |
Human Randomized, single blinded, controlled, crossover | 4 weeks, 23 subjects: Control: period of restricted diet or 550 g whole apples or 22 g apple pomace or 500 ml clear apple juice or 500 ml cloudy apple juice | qPCR | No changes in bacteria composition. pH: ↓ | Ravn-Haren et al., 2012 [15] |
3.2. Impact of the Gut Microbiota on Apple Components—Focus on Polyphenols
3.2.1. In vitro
3.2.2. In Vivo—Animal and Human Studies
4. Cardiovascular Disease Risk
4.1. Lipid Metabolism
4.1.1. Animal Studies
4.1.2. Human Studies
Animal Type- Number (n)- Study Duration-Design | Diets-Daily Dose | Results | Author |
---|---|---|---|
Wistar rats n = 12 each group 3 weeks/parallel | Control diet or 15% lyophilized apple | TC: ↓ 9.3% Faecal TS excretion: ↑ Faecal TC excretion: ↑ | Aprikian et al., 2001 [145] |
Wistar rats n = 10 each group 40 days/parallel | Control cholesterol (3g/kg) diet or 10% apple pomace fiber | TC: ↓ 18.4% LDL-C: ↓ 31.2% HDL phospholipids: ↑ 19% TAG: ↓ 14.8% Liver TC: ↓ 26.3% | Leontowicz et al., 2001[138] |
Lean (Fa/-) and obese (fa/fa) Zucker rats n = 8 each group 3 weeks/parallel | Control diet or 20% lyophilized apple | TC: ↓ 22% (Obese group) LDL-C: ↓ 70% (Obese group) HDL-C: ↓ 26% (Obese group) Liver and heart TAG: ↓ (Obese group) Faecal BA excretion: ↑ (Lean group) | Aprikian et al., 2002 [147] |
Wistar rats n = 8 each group 4 weeks/parallel | Control cholesterol (1%) diet or 10% whole dry apples | TC: ↓ 20% LDL-C: ↓ 32.6% TAG: ↓ 17% Liver TC: ↓ 29.6% | Leontowicz et al., 2002[146] |
Wistar mild hypercholesteolemic rats n = 10 each group 3 weeks/parallel | Control diet or Freeze dried pectin, 5% (PEC) or High polyphenol cider apple extract, 10% (PL) or Mixed diet: PEC + PL | TC: ↓ 24% (PEC + PL) TAG: ↓ 29% (PL) ↓ 35% (PEC + PL) Liver TC and TAG: ↓ (PEC and PEC + PL) Faecal BA excretion: ↓ (PEC and PEC + PL) Faecal NS excretion: ↑ (PEC and PEC + PL) | Aprikian et al., 2003 [115] |
Wistar rats n = 8 each group 4 weeks/parallel | Control cholesterol (1%) diet or apple peel, 10% (Apeel) or apple pulp, 10% (Apulp) | TC: ↓ 21.6% (Apeel), ↓ 19.4% (Apulp) LDL-C: ↓ 35.3% (Apeel), ↓ 33.3% (Apulp) TAG: ↓ 18% (Apeel), ↓ 14.6% (Apulp) Liver TC: ↓ 31.6% (Apeel), ↓ 27% (Apulp) | Leontowicz et al., 2003[150] |
Sprague-Dawley rats n = 8 or 9 each group 30 days/parallel | Control cholesterol (0.5%) diet or 0.2% apple polyphenols rich in oligomeric procyanidins (AP) or 0.5% AP or1% AP | TC: ↓ (all treatments) HDL-C: ↑ (1% AP), ↓ (0.2% AP) HDL-C/TC: ↑ (0.5% and 1% AP) Liver TC: ↓ (0.5% and 1% AP) Atherogenic indices: ↓ (0.5% and 1% AP) Faecal acidic and neutral steroid excretion: ↑ (0.5% and 1% AP) | Osada et al., 2006 [139] |
ApoE deficient mice (apoE-KO) n = 16 each group 4 months/parallel | Control diet or apple polyphenols (AP), equivalent to 1.6 g/day for humans orapple fiber (AF), equivalent to 50 g/day for humans or Mixed diet: AP + AF | Liver TC: ↓ 22% (AP + AF) Atherosclerotic lesions: ↓ (all treatments) | Auclair et al., 2008 [144] |
Hypercholesterolemic hamsters n = 8 each group 12 weeks/parallel | Control atherogenic diet orapple (A) or apple juice (AJ) Equivalent to daily consumption of 600 g apples or 500 ml of juice for humans | TC: ↓ 11% (A) ↓ 24% (AJ) Non HDL-C: ↓ 30% (A) ↓ 55% (AJ) TC/HDL-C: ↓ 25% (A) ↓ 38% (AJ) Aortic fatty streak area: ↓ 48% (A) and 60% (AJ) | Decorde et al., 2008 [142] |
Golden Syrian hamsters n = 13 each group 6 weeks/parallel | Control atherogenic diet, 0.1% cholesterol or 0.3% apple polyphenols (AP) or 0.6% AP | HDL-C: ↑14.7% (0.3% AP) ↑16.5% (0.6% AP) Non HDL-C: ↓ 20% (0.3% AP) ↓ 36.7% (0.6% AP) TAG: ↓ 31.9% (0.6% AP) Faecal BA excretion: ↑ (0.3% and 0.6% AP) Faecal NS excretion: ↓ (0.3% and 0.6% AP) | Lam et al., 2008 [143] |
Zucker fatty rats n = 10 each group 15 weeks/parallel | Control diet or High methoxylated apple pectin, 10% (HMAP) or β-glucan, 10% | TC: ↓ (HMAP and β-glucan) HDL-C: ↑ (HMAP) Non HDL-C: ↓ (HMAP and β-glucan) TAG: ↓ (HMAP and β-glucan, higher effect for HMAP) | Sanchez et al., 2008 [35] |
Rabbits n = 8 each group 2 months/parallel | Control cholesterol (1%) diet or 5 ml apple juice (low dose, LD) or 10 ml apple juice (high dose, HD) | TC: ↓ 75% (LD), ↓ 77% (HD) LDL-C: ↓ 70% (HD) HDL-C: ↑ 86% (HD) TAG: ↓ 61% (LD), ↓ 59% (HD) Atherosclerotic lesions: ↓ (LD and HD) | Setorki et al., 2009 [20] |
Wistar rats n = 8 each group 4 weeks/parallel | Control diet or 5% AP: apple pomace (61% dietary fiber (DF), 0.23% polyphenols (PP)) or 5% APE: ethanol extracted apple pomace (66% DF, 0.1% PP) or 5% APA: ethanol/acetone extracted apple pomace (67% DF, 0.01% PP) | TC: ↓ 19% (AP and APA) TAG: ↓ 26% (APA) ↓ 38% (AP) Atherogenic index, log TAG/HDL-C: ↓ (AP) | Kosmala et al., 2011 [117] |
Wistar hypercholesterolemic rats n = 8 each group 30 days/parallel | Control cholesterol (2%) diet 20% apples from 3 different varieties:
| TC: ↓ 21% (BE) LDL-C: ↓ 20.4% (BE) TAG: ↓ 27.2% (BE) | Serra et al., 2012 [140] |
Sprague–Dawley rats n = 8 each group 5 weeks/parallel | Control high fat diet or 10% apple pomace (AP) or 10% apple juice concentrate (AC) | TC: ↓ 23% (AP), ↓ 22% (AC) LDL-C: ↓ 34% (AP), ↓ 32% (AC) HDL-C: ↑ 12% (AP) HDL-C/TC: ↑ (AP and AC) TAG: ↓ 30% (AP), ↓ 27% (AC) Liver TC: ↓19% (AP) Liver TAG: ↓ 21% (AP), ↓ 10% (AC) Atherogenic index: ↓ (AP and AC) | Cho et al., 2013 [148] |
4.1.3. Potential Lipid-Lowering Mechanisms
Modulation of Bile Acid Enterohepatic Circulation
Subjects-Study Duration-Design | Diets-Daily Dose | Results | Author |
---|---|---|---|
25 healthy men/women 6 weeks Randomized, crossover | 340 g apple or 375 ml apple juice | No changes: TC, LDL-C, HDL-C and TAG | Hyson et al., 2000 [155] |
49 hypercholesterolemic, overweight women 12 weeks (35 women) Randomized, parallel | 300 g apple or 300 g pear or 60 g oat cookies | TC: ↓ (oat group) TAG: ↑ (fruit group) | de Oliveira et al., 2003[16] |
48 hypercholesterolemic men/women 4 weeks Randomized, double-blinded, placebo-controlled, parallel | Control: supplement without polyphenols or Low dose: 300 mg apple polyphenols (AP) or Medium dose: 600 mg AP or High dose: 1500 mg AP | TC: ↓ 4.5% (from baseline for High dose) LDL-C: ↓ 7.8% (from baseline for High dose) No changes: HDL-C and TAG | Nagasako-Akazome et al., 2005 [11] |
15 elderly 4 weeks | Fresh apples (2 g/kg body weight, approximately 1 apple) | No changes: TC, LDL-C, HDL-C and TAG | Avci et al., 2007 [156] |
48 moderately obese men/women 12 weeks Randomized, double-blinded, placebo-controlled, parallel | Control: capsules without polyphenols or 600 mg apple polyphenols capsules | TC: ↓ (from baseline and control group) LDL-C: ↓ (from baseline) No changes: HDL-C and TAG VFA: ↓ (from control group) Adiponectin: ↑ (from control group) | Nagasako-Akazome et al., 2007 [12] |
46 overweight, hyperlipidemic men 8 weeks Randomized, controlled, parallel | Control: no apple intake or 300 g apple | No changes: TC, LDL-C and HDL-C TAG: ↓ (in control group compared with the apple group) VLDL-C: ↓ (in control group compared with the apple group) | Vafa et al., 2011 [157] |
68 overweight men 4 weeks Randomized, blinded, placebo-controlled, parallel | Control: beverage without polyphenols or 750 ml cloudy apple juice | No changes: TC, LDL-C, HDL-C and TAG % total body fat: ↓ (from control group) Body fat mass: ↓ (only in IL-6-174 C/C variant compared with G-allele carriers). | Barth et al., 2012 [13] |
160 postmenopausal women 1 year Randomized, single blinded, controlled, parallel | Dried plum (comparative control) or 75 g dried apples | TC: ↓ (from control group) TC: ↓ 13% (from baseline) LDL-C: ↓ 24% (from baseline) TC:HDL-C: ↓ (from baseline) LDL:HDL-C: ↓ (from baseline) No changes: HDL-C and TAG | Chai et al., 2012 [14] |
23 healthy men/women 4 weeks Randomised, single blinded, controlled, crossover | Control: period of restricted diet or 550 g whole apples (WA) or 22 g apple pomace (AP) or 500 ml clear apple juice (AJ) or 500 ml cloudy AJ | Treatment resulted in significant effects in TC and LDL-C. Clear AJ: ↑ 5% TC, ↑ 6.9% LDL-C (compared with WA and AP) No changes: HDL-C and TAG | Ravn-Haren et al, 2012 [15] |
20 healthy young men/women 4 weeks Randomized, crossover | 500 ml of two cloudy apple juices: 510 mg/L catechin equivalent and 60 mg/L vitamin C (VCR) or 993 mg/L catechin equivalent and 22 mg/L vitamin C (PR) | TC: ↓ 4% (VCR) No changes: LDL-C, HDL-C and TAG | Soriano-Maldonado et al., 2014 [162] |
Modification of Lipid Metabolism
4.2. Vascular Function and Blood Pressure
4.3. Inflammation
5. Conclusions
Author Contributions
Conflicts of Interest
References
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Koutsos, A.; Tuohy, K.M.; Lovegrove, J.A. Apples and Cardiovascular Health—Is the Gut Microbiota a Core Consideration? Nutrients 2015, 7, 3959-3998. https://doi.org/10.3390/nu7063959
Koutsos A, Tuohy KM, Lovegrove JA. Apples and Cardiovascular Health—Is the Gut Microbiota a Core Consideration? Nutrients. 2015; 7(6):3959-3998. https://doi.org/10.3390/nu7063959
Chicago/Turabian StyleKoutsos, Athanasios, Kieran M. Tuohy, and Julie A. Lovegrove. 2015. "Apples and Cardiovascular Health—Is the Gut Microbiota a Core Consideration?" Nutrients 7, no. 6: 3959-3998. https://doi.org/10.3390/nu7063959