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Effect of cocoa powder on the modulation of inflammatory biomarkers in patients at high risk of cardiovascular disease
Open accessAbstract
Background Epidemiologic studies have suggested that flavonoid intake plays a critical role in the prevention of coronary heart disease. Because atherosclerosis is considered a low-grade inflammatory disease, some feeding trials have analyzed the effects of cocoa (an important source of flavonoids) on inflammatory biomarkers, but the results have been controversial.Objective The objective was to evaluate the effects of chronic cocoa consumption on cellular and serum biomarkers related to atherosclerosis in high-risk patients.Design Forty-two high-risk volunteers (19 men and 23 women; mean +/- SD age: 69.7 +/- 11.5 y) were included in a randomized crossover feeding trial. All subjects received 40 g cocoa powder with 500 mL skim milk/d (C+M) or only 500 mL skim milk/d (M) for 4 wk. Before and after each intervention period, cellular and serum inflammatory biomarkers related to atherosclerosis were evaluated.Results Adherence to the dietary protocol was excellent. No significant changes in the expression of adhesion molecules on T lymphocyte surfaces were found between the C+M and M groups. However, in monocytes, the expression of VLA-4, CD40, and CD36 was significantly lower (P = 0.005, 0.028, and 0.001, respectively) after C+M intake than after M intake. In addition, serum concentrations of the soluble endothelium-derived adhesion molecules P-selectin and intercellular adhesion molecule-1 were significantly lower (both P = 0.007) after C+M intake than after M intake.Conclusions These results suggest that the intake of cocoa polyphenols may modulate inflammatory mediators in patients at high risk of cardiovascular disease. These antiinflammatory effects may contribute to the overall benefits of cocoa consumption against atherosclerosis. This trial was registered in the Current Controlled Trials at London, International Standard Randomized Controlled Trial Number, at controlled-trials.com as ISRCTN75176807.
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“This treatment also lowered circulating levels of the inflammatory markers P-selectin and ICAM-1, compared with monocytes from the control group (only skimmed milk) (143).”
From Immunosenescence and Its Hallmarks: How to Oppose Aging Strategically? A Review of Potential Options for Therapeutic Intervention (2019) · cites this paper as [143]
In the citing paper
“Consumption of cocoa polyphenols rich in flavonoids (40 g/day) with 500 ml of skimmed milk, by participants at high cardiovascular disease risk (≥55 years), significantly reduced the expression of cell adhesion molecule very late antigen-4, CD40, and CD36 on monocytes.”
From Immunosenescence and Its Hallmarks: How to Oppose Aging Strategically? A Review of Potential Options for Therapeutic Intervention (2019) · cites this paper as [143]
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Nutrition and Cardiovascular Health
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Effect of cocoa on blood pressure
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BackgroundCocoa Polyphenols and Their Potential Benefits for Human Health
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“It has also been reported that the chronic consumption of a high flavanol diet can result in a reduction in select pro-inflammatory markers.(72) While space constraints do not allow for an in-depth review of this literature, these observations support the concept that dietary flavanols have positive vascular effects t…”
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InfluentialDoes chocolate reduce blood pressure? A meta-analysis
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BackgroundMethodResultInfluentialFlavonoids and Immune Function in Human: A Systematic Review
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BackgroundInfluentialLos polifenoles, compuestos de origen natural con efectos saludables sobre el sistema cardiovascular
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“Likewise, in a study on high-risk cardiovascular subjects [82], ICAM-1 levels were significantly decreased after consuming 40 g of cocoa powder with milk (495 mg of total polyphenols).”
BackgroundPotential for preventive effects of cocoa and cocoa polyphenols in cancer
Martín, M. Á., Goya, L., & Ramos, S. (2013) · Food and Chemical Toxicology · doi:10.1016/j.fct.2013.02.020 · Cited by 122
“, 2011), but biomarkers of inflammation, including IL-6, were unaffected in patients at high risk of cardiovascular disease consuming cocoa powder (Monagas et al., 2009).”
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Dietary cocoa ameliorates obesity-related inflammation in high fat-fed mice
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“5 years) ↑HDL cholesterol; ↓expression of adhesion molecules on the surface of monocytes and concentration of circulating soluble adhesion molecules (60, 76)”
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Mitigation of Inflammation with Foods
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Tresserra‐Rimbau, A., Medina‐Remón, A., Lamuela-Raventós, R. M., Bulló, M., Salas‐Salvadó, J., Corella, D., Fitó, M., Gea, A., Gómez‐Gracia, E., Lapetra, J., et al. (2015) · British Journal Of Nutrition · doi:10.1017/s0007114514003262 · Cited by 99
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MethodFlavan‐3‐ols, anthocyanins, and inflammation
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“Soluble forms of P-selectin and intercellular adhesion molecule (ICAM) were reduced after cocoa intake (60).”
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Marhuenda‐Muñoz, M., Santos, E. P. L., Tresserra‐Rimbau, A., Lamuela-Raventós, R. M., Martínez‐Huélamo, M., & Vallverdú‐Queralt, A. (2019) · Nutrients · doi:10.3390/nu11112725 · Cited by 99
“Recent clinical trials have reported beneficial effects of cocoa polyphenols on cardiovascular health [40,41].”
BackgroundThe impact of chocolate on cardiovascular health
Fernández-Murga, M. L., Tarín, J. J., García‐Pérez, M. Á., & Cano, A. (2011) · Maturitas · doi:10.1016/j.maturitas.2011.05.011 · Cited by 94
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“This anti-inflammatory effect may contribute to the overall benefits against atherosclerosis as an inflammatory disorder [10].”
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Ali, F., Ismail, A., & Kersten, S. (2013) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201300277 · Cited by 95
“Furthermore, randomized clinical trials with proanthocyanidine-rich cocoa powder (40 g cocoa powder in 500 mL skim milk/day for 4 wk) [125] and flavonol-rich bilberry juice (330 mL/day for 4 wk) [126] caused reduced plasma markers of inflammation in adults with high CVD risk who consumed products rich in polyphenols.”
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“levels remained similar in contrast to that observed in a previous study((60)) in high-risk CVD subjects in whom ICAM-1”
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“on monocytes and lower circulating levels of the inflammatory markers P-selectin and ICAM-1 (Monagas et al., 2009).”
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“Abbreviations CVDs Cardiovascular diseases DHPV 5-(3′,4′-dihydroxyphenyl)-γ-valerolactone DHPA 3-(3′,4′-dihydroxyphenyl)-propionic acid DHAA 3,4-dihydroxyphenyl-acetic acid Pro Procyanidin Int.”
BackgroundInfluentialRacial disparities in cardiovascular disease risk: mechanisms of vascular dysfunction
Brothers, R. M., Fadel, P. J., & Keller, D. M. (2019) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00126.2019 · Cited by 82
“Laboratory-based studies, utilizing both acute and chronic dietary flavanol interventions, in various healthy and diseased populations, have indicated improvements in numerous physiological variables including reductions in arterial blood pressure and improved lipid profile, glucose tolerance, and vascular endothelial…”
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“Studies are listed in [25–134].”
BackgroundEffect of cocoa on blood pressure
Ried, K., Sullivan, T. R., Fakler, P., Frank, O. R., & Stocks, N. P. (2012) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd008893.pub2 · Cited by 150
Cocoa Agronomy, Quality, Nutritional, and Health Aspects
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“In 42 volunteers with high cardiovascular risk factors, cocoa powder (40 g/day for 4 weeks) decreased serum P-selectin and intercellular adhesion molecule-1, and also the expression of VLA-4, CD40 and CD36 in monocytes [31].”
BackgroundKuntz, S., Asseburg, H., Dold, S., Römpp, A., Fröhling, B., Kunz, C., & Rudloff, S. (2015) · Food & Function · doi:10.1039/c4fo00755g · Cited by 70
Cocoa consumption reduces NF-κB activation in peripheral blood mononuclear cells in humans
Vázquez-Agell, M., Urpí-Sardà, M., Sacanella, E., Camino-López, S., Chiva‐Blanch, G., Llorente‐Cortés, V., Tobías, E., Roura, E., Andrés‐Lacueva, C., Lamuela-Raventós, R. M., et al. (2011) · Nutrition Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2011.03.015 · Cited by 70
“A human clinical trial recently showed that regular cocoa consumption significantly decreased the expression of VLA-4 (very late antigen-4), CD40 and CD36 on monocyte surface and also decreased serum concentrations of endothelium-derived adhesion molecules such as P-selectin and ICAM-1 (intercellular adhesion molecule…”
BackgroundThe Impact of Epicatechin on Human Cognition: The Role of Cerebral Blood Flow
Haskell‐Ramsay, C. F., Schmitt, J. A. J., & Actis‐Goretta, L. (2018) · Nutrients · doi:10.3390/nu10080986 · Cited by 71
Dugo, L., Belluomo, M. G., Fanali, C., Russo, M., Cacciola, F., Maccarrone, M., & Sardanelli, A. M. (2017) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2017/6293740 · Cited by 67
“In a healthy population of Southern Italy, regular intake of dark chocolate was inversely associated to serum C-reactive protein level [26, 27].”
BackgroundDietary Agents and Phytochemicals in the Prevention and Treatment of Experimental Ulcerative Colitis
Saxena, A., Kaur, K., Hegde, S., Kalekhan, F. M., Baliga, M. S., & Fayad, R. (2014) · Journal of Traditional and Complementary Medicine · doi:10.4103/2225-4110.139111 · Cited by 65
“[40] concluded that cocoa polyphenol intake modulated inflammatory mediators in patients with a high risk of cardiovascular disease and could be beneficial against atherosclerosis.[40] These antiinflammatory effects may contribute to the overall benefits of cocoa consumption against atherosclerosis.”
González‐Sarrías, A., Combet, E., Pinto, P., Mena, P. R., Dall’Asta, M., Garcia‐Aloy, M., Rodriguez‐Mateos, A., Gibney, E. R., Dumont, J., Massaro, M., et al. (2017) · Nutrients · doi:10.3390/nu9070746 · Cited by 64
Esser, D., Mars, M., Oosterink, E., Stalmach, A., Müller, M. M., & Afinan, L. A. (2013) · The FASEB Journal · doi:10.1096/fj.13-239384 · Cited by 63
“Second, dark chocolate consumption decreased protein expression of lymphocyte CD62L and CD11b, monocyte CD62L, and neutrophil CD66b and CD11c.”
BackgroundInfluentialBoronat, A., Mateus, J., Soldevila‐Domenech, N., Guerra, M., Rodríguez-Morató, J., Varon, C., Muñoz, D., Barbosa, F., Morales, J. C., Gaedigk, A., et al. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.08.032 · Cited by 65
“Similar decreases occurred after wine and cocoa flavonoid intake [50,51].”
BackgroundAjibola, C. F., Oyerinde, O. V., & Adeniyan, O. (2015) · Journal of Scientific Research and Reports · doi:10.9734/jsrr/2015/18070 · Cited by 61
“The health benefits associated with cocoa consumption have been related to their capacity to improve the lipid profile and insulin sensitivity, diminish blood pressure, reduce platelet activity and function, ameliorate endothelial dysfunction and act as antioxidants [13-16].”
BackgroundStudy of the factors influencing the bioaccessibility of 10 elements from chocolate drink powder
Peixoto, R. R. A., Devesa, V., Vélez, D., Cervera, M. L., & Cadore, S. (2016) · Journal of Food Composition and Analysis · doi:10.1016/j.jfca.2016.02.002 · Cited by 56
Zeng, H., Locatelli, M., Bardelli, C., Amoruso, A., Coïsson, J. D., Travaglia, F., Arlorio, M., & Brunelleschi, S. (2011) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf2005386 · Cited by 54
The effects of cocoa on the immune system
Pérez-Cano, F. J., Massot‐Cladera, M., Franch, À., Castellote, C., & Castell, M. (2013) · Frontiers in Pharmacology · doi:10.3389/fphar.2013.00071 · Cited by 56
“In addition, cocoa consumption for 4 weeks decreased some adhesion molecules involved in the recruitment of inflammatory cells (Monagas et al., 2009).”
BackgroundKennedy, D. O. (2019) · Sports Medicine · doi:10.1007/s40279-018-1007-0 · Cited by 60
Dietary Polyphenols and Their Effects on Cell Biochemistry and Pathophysiology 2013
Maraldi, T., Vauzour, D., & Angeloni, C. (2014) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2014/576363 · Cited by 55
[The polyphenols, naturally occurring compounds with beneficial effects on cardiovascular disease].
Quiñones, M., Miguel, M., & Aleixandre, A. (2012) · PubMed · doi:10.1590/s0212-16112012000100009 · Cited by 202
McGhie, T. K., & Rowan, D. D. (2011) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201100545 · Cited by 50
“Although the measurement of protein biomarkers supported an anti-inflammatory effect of cocoa [66], no evidence for metabolic effects relevant to health outcomes of the human subjects appears to have been reported.”
BackgroundMental Performance and Sport: Caffeine and Co-Consumed Bioactive Ingredients
Kennedy, D. O., & Wightman, E. L. (2022) · Sports Medicine · doi:10.1007/s40279-022-01796-8 · Cited by 50
Metabolomic fingerprint in patients at high risk of cardiovascular disease by cocoa intervention
Llorach, R., Urpí-Sardà, M., Tulipani, S., Garcia‐Aloy, M., Monagas, M., & Andrés‐Lacueva, C. (2013) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201200736 · Cited by 51
Nogueira, L. D. P., Knibel, M. P., Klein, M. R. S. T., Neto, J. F. N., & Sanjuliani, A. F. (2012) · International Journal of Hypertension · doi:10.1155/2012/147321 · Cited by 49
“Recent studies have also demonstrated beneficial effects of dark chocolate or cocoa on insulin resistance [9, 18–20], lipid profile [21, 22], and inflammatory status [23].”
BackgroundMartínez‐López, S., Sarriá, B., Sierra-Cinos, J. L., Goya, L., Mateos, R., & Bravo, L. (2013) · Food & Function · doi:10.1039/c3fo60352k · Cited by 49
Navarro, S. L., Schwarz, Y., Song, X., Wang, C., Chen, C., Trudo, S. P., Kristal, A. R., Kratz, M., Eaton, D. L., & Lampe, J. W. (2014) · Journal of Nutrition · doi:10.3945/jn.114.197434 · Cited by 49
Preventive Effects of Cocoa and Cocoa Antioxidants in Colon Cancer
Martín, M. Á., Goya, L., & Ramos, S. (2016) · Diseases · doi:10.3390/diseases4010006 · Cited by 49
“Consequently, cocoa consumption reduced NF-κB activation in peripheral blood mononuclear cells in healthy voluntaries [54], but biomarkers of inflammation, such as IL-6, were unaltered in patients at high risk of cardiovascular disease consuming cocoa powder [55].”
BackgroundDicks, L., Kirch, N., Gronwald, D., Wernken, K., Zimmermann, B., Helfrich, H., & Ellinger, S. (2018) · Nutrients · doi:10.3390/nu10101435 · Cited by 44
“Results in HDL-C were different between the studies [4–9], but HDL-C is affected by lifestyle (e.g., physical exercise, changes in weight, and diet [30]) which was not sufficiently controlled in most RCTs.”
BackgroundResultInfluentialPheidippides Redux: Reducing Risk for Acute Cardiac Events During Marathon Running
Siegel, A. J. (2012) · The American Journal of Medicine · doi:10.1016/j.amjmed.2011.11.008 · Cited by 48
Ellinger, S., & Stehle, P. (2016) · Nutrients · doi:10.3390/nu8060321 · Cited by 48
“In contrast to healthy subjects, most regular consumption trials with patients suffering from type 2 diabetes or impaired glucose tolerance found lower concentrations of ICAM-1 [64,66] and P-selectin in serum or plasma [64] and a reduced expression of VLA-4, CD36, and CD40 on monocytes [64].”
BackgroundResultInfluentialThe Impact of Cocoa Flavanols on Cardiovascular Health
Vlachojannis, J., Erne, P., Zimmermann, B., & Chrubasik-Hausmann, S. (2016) · Phytotherapy Research · doi:10.1002/ptr.5665 · Cited by 40
Modulation of metabolic syndrome‐related inflammation by cocoa
Gu, Y., & Lambert, J. D. (2013) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201200837 · Cited by 47
Davinelli, S., Corbi, G., Righetti, S., Sears, B., Olarte, H. H., Grassi, D., & Scapagnini, G. (2018) · Journal of Medicinal Food · doi:10.1089/jmf.2018.0002 · Cited by 48
“However, even though little clinical evidence exists that consumption of CPs may reduce inflammation, a randomized clinical trial with proanthocyanidine-rich cocoa powder demonstrated a reduction in plasma markers of inflammation in adults with high CVD risk.(56) Some studies suggest that cocoa flavonoids may inhibit…”
BackgroundCan chocolate consumption reduce cardio-cerebrovascular risk? A systematic review and meta-analysis
Gianfredi, V., Salvatori, T., Nucci, D., Villarini, M., & Moretti, M. (2017) · Nutrition · doi:10.1016/j.nut.2017.09.006 · Cited by 45
Kord‐Varkaneh, H., Ghaedi, E., Nazary-Vannani, A., Mohammadi, H., & Shab‐Bidar, S. (2018) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2018.1451820 · Cited by 49
“…and cocoa powder (from 1.4 to 40 g/day) (Murphy et al., 2003, Baba et al., 2007, Balzer et al., 2008, Davison et al., 2008, Muniyappa et al., 2008, Monagas et al., 2009, Sathyapalan et al., 2010, Njike et al., 2011, Tzounis et al., 2011, Desideri et al., 2012, Neufingerl et al., 2013,…”
BackgroundInfluentialProcyanidins attenuate neuropathic pain by suppressing matrix metalloproteinase-9/2
Pan, C., Wang, C., Zhang, L., Song, L., Chen, Y., Liu, B., Liu, W., Hu, L., & Pan, Y. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1182-9 · Cited by 46
“Epidemiological studies indicated that populations consuming procyanidin-rich foods had lower incidences of inflammatory diseases, including metabolic syndrome and atherosclerosis [17, 18].”
Giacco, R., Costabile, G., Fatati, G., Frittitta, L., Maiorino, M. I., Marelli, G., Parillo, M., Pistis, D., Tubili, C., Vetrani, C., et al. (2019) · Nutrition Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2019.11.015 · Cited by 47
Gligorijević, N., Stanić-Vučinić, D., Radomirović, M., Stojadinović, M., Olgica, N., Khulal, U., & Veličković, T. Ć. (2021) · Molecules · doi:10.3390/molecules26102834 · Cited by 48
“production of soluble adhesion molecules sICAM-1 and sE-selectin [153].”
BackgroundInfluence of Bioactive Nutrients on the Atherosclerotic Process: A Review
Casas, R. M., Estruch, R., & Sacanella, E. (2018) · Nutrients · doi:10.3390/nu10111630 · Cited by 45
“[84] 4-weeks of intervention of: 40 g cocoa powder with 500 mL skim milk/d (C + M) or only 500 mL skim milk/d (M).”
BackgroundMethodChocolate and Coronary Heart Disease: A Systematic Review
Khawaja, O. A., Gaziano, J. M., & Djoussé, L. (2011) · Current Atherosclerosis Reports · doi:10.1007/s11883-011-0203-2 · Cited by 41
Cocoa, Blood Pressure, and Cardiovascular Health
Ferri, C., Desideri, G., Ferri, L., Proietti, I., Agostino, S., Martella, L., Mai, F., Giosia, P. D., & Grassi, D. (2015) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.5b01064 · Cited by 42
Giacometti, J., Muhvić, D., Pavletić, A., & Đudarić, L. (2016) · Journal of Functional Foods · doi:10.1016/j.jff.2016.02.036 · Cited by 40
Nutrition epidemiology of flavan-3-ols: The known unknowns
Kuhnle, G. (2017) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2017.10.003 · Cited by 42
Anti‐influenza virus effects of cocoa
Kamei, M., Nishimura, H., Takahashi, T., Takahashi, N., Inokuchi, K., Mato, T. K., & Takahashi, K. (2015) · Journal of the Science of Food and Agriculture · doi:10.1002/jsfa.7197 · Cited by 39
Effect of Plant Polyphenols on Adipokine Secretion from Human SGBS Adipocytes
Derdemezis, C. S., Kiortsis, D. N., Tsimihodimos, V., Petraki, M. P., Vezyraki, P., Elisaf, M., & Tselepis, A. D. (2011) · Biochemistry Research International · doi:10.1155/2011/285618 · Cited by 38
Metadata
- Authors
- Monagas, M., Khan, N., Andres-Lacueva, C., Casas, R., Urpí-Sardà, M., Llorach, R., Lamuela-Raventós, R. M., & Estruch, R.
- Affiliations
- Instituto de Salud Carlos III (ES)
- Corresponding author
- Estruch, Ramón
- Venue
- The American Journal of Clinical Nutrition
- Publisher
- Elsevier BV
- Published
- 2009-11
- Volume
- 90
- Issue
- 5
- Pages
- 1144-1150
- ISSN
- 0002-9165 (ISSN-L)
- OpenAlex
- W1964861389
- Cited by
- 209
- References
- 41
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 5 · 2023: 4 · 2022: 7 · 2021: 7 · 2020: 10 · 2019: 13 · 2018: 11 · 2017: 15 · 2016: 22 · 2015: 14 · 2014: 14 · 2013: 31 · 2012: 24
- FWCI
- 10.46
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- American Journal of Clinical Nutrition (publishedVersion)
- PubMed (publishedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (acceptedVersion, other-oa)
- Dipòsit Digital de la Universitat de Barcelona (Universitat de Barcelona) (submittedVersion, public-domain)
- RECERCAT (Consorci de Serveis Universitaris de Catalunya) (submittedVersion)
- Topics
- Health Sciences › Medicine › Biochemistry (medical) › Phytochemicals and Antioxidant Activities
- Life Sciences › Agricultural and Biological Sciences › Food Science › Food Chemistry and Fat Analysis
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
- Keywords
- cocoa powder, cocoa polyphenols, flavonoids, atherosclerosis, inflammation, inflammatory markers, cardiovascular risk, monocytes, adhesion molecules, VLA-4, CD40, CD36, P-selectin, ICAM-1, T cells, dietary intervention
- MeSH terms
- Aged, Aged, 80 and over, Blood Pressure, Body Weight, Cacao, Cardiovascular Diseases, Coronary Disease, Female, Flavonoids, Humans, Inflammation, Leukocytes, Mononuclear, Male, Middle Aged, Monocytes, Obesity, Risk Factors, Smoking, T-Lymphocytes, Immunophenotyping, Patient Selection, Cross-Over Studies
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