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Garlic and its potential for prevention of colorectal cancer and other conditions

Alpers, David H

Current Opinion in Gastroenterology: March 2009 - Volume 25 - Issue 2 - p 116–121
doi: 10.1097/MOG.0b013e32831ef221
Nutrition: Edited by David H. Alpers and William F. Stenson
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Introduction

Garlic (Allium sativum) has been used medicinally for over 5000 years, but in the last 30 years, a considerable body of evidence has sought to link extracts of the vegetable or its active ingredients to physiological processes and to a role in the prevention or management of human disease. Claims have been and are being made for a role of garlic in antibacterial, antiviral, anti-inflammatory, and antineoplastic activities. Moreover, some evidence exists that it may prevent colorectal tumor formation, reduce cholesterol, reduce blood pressure (BP), provide anticoagulation, and provide broad antioxidant activity to limit free radical damage.

Two meta-analyses in 2000 provided the framework for the last 8 years of work, in that authors suggested the possibility of an effect on prevention of gastrointestinal cancers and on lowering serum cholesterol. Eighteen studies were included in an analysis [1] of the epidemiologic literature on the association between garlic intake and risk of cancers. The relative risk (RR) estimate of colorectal cancer (CRC) in individuals eating food-related garlic (raw or cooked garlic) was 0.69 [95% confidence interval (CI) 0.55–0.89], and for gastric cancer the RR was 0.53 (95% CI 0.31–0.92). However, because of the extreme heterogeneity of the effect and dose estimates, no firm recommendation could be made. The meta-analysis [2] for lowering cholesterol was based on 13 double-blind, placebo-controlled trials. A modest lowering effect [−15.7 mg/dl (95% CI −25.6 to −5.7 mg/dl)] was found, but using the six studies with the highest methodological quality, the difference was only −4.3 mg/dl (95% CI −11.7 to −3.1 mg/dl). The authors concluded that the effect was probably real, but that the effect size was small, and the robustness of the effect was in question, because of study heterogeneity.

As is the case with many food substances, the in-vitro work is substantial in supporting mechanisms of action, but the clinical data are sparse or nonsupporting. Some of these data will be reviewed below, focusing on the last few years. In addition, there are various forms of food garlic and garlic supplements, containing different amounts of the presumed active substances, making it difficult to compare preparations and studies.

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Varieties of ingested garlic and presumed active ingredients

Garlic (A. sativum) is a member of the lily family, in the same plant group as onions. Many individual cloves comprise a bulb. Each clove contains approximately 1.5–3.0 g of raw garlic, containing mostly fructose-rich carbohydrates, sulfur compounds, and proteins. Alliin (S-allyl-cysteine sulfoxide) is converted to allicin (allyl-2-propenethiosulfinate) by alliinase, an enzyme activated when garlic is cut or crushed. Allicin is responsible for the pungent odor of garlic and has antibiotic activity, but is very unstable and decomposes at room temperature within a few hours. The resulting sulfides are thought to provide the active ingredients, including diallyl sulfide (DAS), diallyl disulfide (DADS), diallyl trisulfide (DATS), and ajoene [3••,4••]. These compounds are metabolized to allyl methyl sulfide (AMS) that stimulates production of acetone in breath and can be used to assess the bioavailability of allicin [5]. The organosulfur content of garlic cloves is dependent upon the conditions of cultivation. Garlic cloves contain free amino acids (glutamine is most abundant), vitamins A, C, E, and B-complex (especially riboflavin), and fiber (2% by weight). Thus, there are many potential sources of biological activity.

There are five major garlic preparations available: fresh garlic, garlic oil, garlic powder, aged, and pickled garlic [3••]. Fresh garlic is the form most often cited in epidemiologic studies, but its active ingredients are not standardized. Garlic can apparently be blanched, boiled, fried, and microwaved for various times without significantly changing the content of bioactive compounds and free antioxidant activity [6]. Garlic oil is produced by steam distillation of crushed raw garlic, followed by dilution about 200-fold with vegetable oil to reduce the odor. It contains sulfides (especially diallyl and allyl methyl derivatives) but no water-soluble sulfides and no nonvolatile components. Garlic powder is prepared from frozen lyophilized raw garlic. About 250 g of powdered garlic is derived from 1 kg of raw garlic. The yield of active sulfides depends upon the activity of alliinase. If the garlic was dried at temperatures above 70°C, the enzyme is inactivated and allicin is not produced. If dried at suitable temperatures, the tablets must be enteric coated to prevent inactivation of alliinase at low pH in the stomach. Thus, the content of active sulfides can be quite variable. Moreover, antioxidant activity may vary greatly. One report [7] studied Kwai-coated tablets with fresh garlic extract standardized to 1–1.4% alliin (Lichtwer Pharma, Cologne, Germany), and was unable to show antioxidant activity. Aged garlic extract is made from sliced raw garlic stored without heating for 20 months in 15–20% ethanol. The preparation is odor free because it is very low in allicin, and produces water-soluble compounds, for example, S-allylcysteine (SAC) and S-allylmercaptocysteine. This preparation contains the highest concentration of antioxidant activity, and is standardized by the SAC content. Finally, pickled garlic results in a quite different bioactive spectrum. It contains salt, of course, and is sometimes fermented. The fermented product contains more riboflavin and α-tocopherol but has lower thiamin content, and ascorbic acid is absent [8]. Recommended doses of raw garlic are usually one whole clove daily, or 900 mg of garlic equivalent, standardized to 1.3% of alliin. The commercial preparations may or may not be standardized to the dominant allyl derivative.

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Evidence for a role in colorectal cancer prevention: preclinical data

Organosulfur compounds from garlic have been tested in many isolated cell systems targeting outcomes related to the prevention and treatment of cancer in humans. These preparations have shown some effect in modulation of carcinogen metabolism, inhibition of cell cycle progression, induction of apoptosis, histone modification, and inhibition of angiogenesis [4••]. Most of these effects involve neoplastic cells, but no effect is seen in normal cells for most functions (e.g. apoptosis). Multiple tumor cell lines, colonic [9] and noncolonic [10•] have been inhibited by DAS or DADS. The mechanism of these effects is not clear. In most experiments, high levels of organosulfur compounds were used (50–100 μmol/l). Allyl sulfides have been used to inhibit inflammation in vitro, using quite heroic concentrations up to 20 mmol/l [11•].

Garlic extracts/compounds have been used in vivo in animals for cancer prevention. DAS inhibited the colon cancer produced by 1,2-dimethylhydrazine in mice, and DADS inhibited invasive colon cancer induced by azoxymethane in rats. DADS and DATS have inhibited tumor growth in xenograft mouse models [4••]. Similar results have been reported using animal models of chemically induced mammary, prostatic, or uterine cancers [12•]. A systematic review [13••] of animal studies of carcinogen-induced colonic tumor production revealed a significant effect of garlic, its allyl sulfur components, or both. Most common foods contain some selenium, another antioxidant-related factor and exchangeable in organic compounds with sulfur. Natural garlic contains small amounts of selenium. Organoselenium compounds have been found to be superior to their corresponding sulfur analogues in cancer chemoprevention [14]. This finding points again to the need for identifying the active components of garlic in producing chemoprevention in animals. Until that is achieved, and the compound can be provided in sufficient dose, it seems likely that clinical trials using garlic preparations will not progress.

Another major question in interpreting the preclinical in-vivo studies is whether the high micromolar concentrations of active compounds needed to suppress growth and apoptosis of cancer line cells is achievable in vivo. There are insufficient pharmacokinetic data in animals to answer this question. The problem is that the major metabolites of allicin are very unstable, and methods for their analysis have not been available until recently. DATS can be measured by gas chromatography–mass spectrometry, and in rats, an intravenous dose of 10 mg produces a serum concentration of approximately 30 μmol/l [15]. No studies have been done using oral administration. The bioavailability of water-soluble allicin metabolites is high in rats, more than 85% [16]. However, there was a very significant first pass effect, and feeding 9–27 mg of stable DATS metabolites to rats produced serum levels of only about 7 μmol/l [17]. Concentrations in other tissues of the body were lower than in the serum. No pharmacokinetic studies of any allicin metabolite have been reported in humans. Thus, it is not yet clear whether adequate concentrations of allicin metabolites can achieve concentrations in rats (or humans) comparable with what has been used to demonstrate mechanistic effects in cell culture.

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Clinical data

Epidemiologic studies provide the bulk of the evidence suggesting that dietary intake of garlic might be protective against colorectal and gastric cancers [1]. The level of intake associated with lower risk in case–control studies is more than 10 g/day of garlic compared with low intake (<2.2 g/day) [12•]. One clove of garlic averages approximately 3–4 g, so high intake is equivalent to more than three cloves per day or their equivalent, assuming that all bioactive compounds are not degraded. One more recent study [18•] examined fruit and vegetable intake associated with the prevalence of colorectal adenomas. The highest two quintiles of garlic intake showed an adjusted odds ratio (OR) of 0.86 (95% CI 0.76–0.99), but it is not clear whether the effect of garlic intake would have persisted in isolation from the other fruits and vegetables. Similar data have been obtained with prevalence of cancers from other organs, including esophageal and prostatic [19•].

As so commonly occurs, results of intervention studies are neither so available nor clear. A single study [20] has been performed using high (2.4 ml equivalent) and low (0.16 ml equivalent) doses of aged garlic extract (Wakunaga Pharmaceutical Co., Mission Viejo, California, USA) to detect the effect on patients with known colorectal adenomas. At 12 months, a difference in polyp number and size was noted using the high dose of extract, but 12 out of 51 patients had dropped out by 6 months. The study is suggestive, but has not been repeated. A possible caution can be drawn from the experience with gastric cancer. The first double-blind study [21] of DATS (200 mg/day for 1 month in 2526 patients vs. 2507 controls) showed a 47% decrease in the incidence of gastric cancer over 5 years, but a subsequent study [22] using a blend of aged garlic extract and steam-distilled garlic oil showed no effect, even over 7 years. This study also included a positive control arm of amoxicillin and omeprazole for treatment of Helicobacter pylori infection. The review by Ngo et al. [13••] of animal studies also identified 10 case–control and cohort studies, and concluded that a consistent inverse association between a high-garlic intake and CRC had been shown. Another systematic review [23••] of human studies using the US Food and Drug Administration (FDA)'s evidence-based review system for the scientific evaluation of health claims identified 19 studies, 10 of which included colon cancer. Seven studies were the same in the reviews by Ngo et al. [13••] and Kim and Kwon [23••], but two other studies were included in the latter review. These authors concluded, unlike Ngo et al. [13••], that very limited evidence could support a relationship between garlic consumption and reduced risk of any of the cancers (colon, prostate, esophageal, larynx, oral, ovary, or renal) [23••]. Because larger studies often do not support the findings of small preliminary studies, the role of garlic in prevention of colorectal adenomas must be considered unproven at the present time.

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Treatment of hypercholesterolemia

DADS, DATS, and allyl mercaptan (but not other allicin metabolites) inhibited cholesterol synthesis in animals, and the effect was dose dependent [3••]. The largest body of evidence for a role of garlic in prevention of human disease has come from intervention studies in lowering serum cholesterol. The meta-analysis of Stevinson et al. [2] suggested a possible effect, but the data were not very robust, and there was great heterogeneity and bias in the studies. Since then, a few additional studies have appeared with conflicting results. One small study (n = 22/arm) used enteric-coated garlic tablets containing 9.6 mg of allicin equivalent (∼seven cloves) in addition to a low-fat diet in hypercholesterolemic patients [24]. A small but significant change in cholesterol was found (−0.36 mmol/l). A somewhat larger study (48/arm) examined the effect of raw garlic and of two garlic tablets on plasma lipid concentrations in patients with moderate hypercholesterolemia [25••]. This study is unique in that it attempted to equate the allicin content of the three forms of garlic, providing 4 g/day of blended raw garlic, four Garlicin tablets (Nature's Way Products, Inc., Springville, Utah, USA), twice the recommended dose, and six Kyolic tablets (Wakunaga Pharmaceutical Co.), 1½–3 times the recommended dose. There was no effect of any form of garlic on serum cholesterol levels, either total, LDL-cholesterol (LDL-C), or HDL-cholesterol (HDL-C). A prospective but uncontrolled trial [26•] used six capsules per day of oily garlic extract (1.62 mg of allicin equivalents) for 30 days in 70 patients with hypertension. Total cholesterol and LDL levels fell, but BP was not affected, and serum vitamin E rose by more than 50%. It is not clear whether vitamin E improves hyperlipidemia in humans, but a small study [27] in diabetic patients suggests that it might do so. Thus, the role of garlic in treatment of hyperlipidemia is still unproven.

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Management of diabetes mellitus

Allicin had no effect on fasting blood sugar (FBS) in normal rats but lowered FBS in alloxan-treated diabetic rats, perhaps by stimulating β cells. [28•]. Moreover, major metabolites, including a precursor of SAC and DATS, themselves also have hypoglycemic effect in diabetic rats. It has been suggested that allicin works as a sulfhydryl donor to prevent degradation of insulin, but no direct evidence has been produced concerning this hypothesis. There is evidence, however, of a direct effect of garlic preparations on the rate of insulin secretion [28•]. One double-blind placebo-controlled clinical trial [29•] has been performed in 60 type 2 diabetic patients, using 300 mg of garlic powder per day in the form of Allicor (INAT-Farma, Moscow, Russia). Allicor proved superior to placebo (no treatment) over 4 weeks, dropping FBS from 138 to 113 mg/dl. Serum triglycerides fell modestly as well. However, a review [30] of 12 trials examining the effect of garlic on serum glucose levels found only one study in nondiabetic persons to report a statistically significant reduction in glucose. It is not clear whether garlic preparations would add benefit to the management of diabetes mellitus at this time.

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Possible protective role in atherosclerotic heart disease and hypertension

In addition to its possible effect in lowering serum cholesterol levels, garlic preparations have shown anti-inflammatory and antioxidant activity in vitro. On the basis of antioxidant potential in relationship to other vegetables, red pepper ≥ green pepper = garlic = onion ≥white cabbage [3••]. A number of animal models of ischemia–reperfusion injury have been examined using aqueous garlic preparations, and inhibition of lipid peroxidation was found, as well as prevention of glutathione depletion [31•]. Seven studies in humans to test the antioxidant theory were reviewed [32]. Four of these studies used aged garlic extract and showed a decrease in measures of the oxidative state, including superoxide dismutase, xanthine oxidase, and glutathione peroxidase activities. Two trials using garlic tablets showed no changes. A further study of elderly individuals ingesting fresh garlic (0.1 g/kg body weight) for 1 month also showed decreased oxidation reactions and increased protective enzyme activity [33•]. However, none of these studies measured the content of vitamin E or of other antioxidant vitamins of the garlic preparations, or controlled for such content. None measured clinically relevant outcomes. In fact, the scientific basis for the value of food antioxidants has been seriously questioned. There are more than 40 methods for evaluating the antioxidant activity of food, but most rely on test tube reactions and not how the relevant chemical functions in the body. As a result, none of these methods are endorsed by the US Food and Drug Administration. Polyphenols are examples of foodstuff-associated compounds with antioxidant properties, but they are absorbed to various degrees in the intestine, but little is known about their in-vivo antioxidant activity, the interaction with other antioxidants, and the importance of the many metabolites that are produced [34••]. Furthermore, absorption of antioxidants from green tea and wine is dependent on the contents of other food components in the intestinal lumen [35•]. Thus, claims based on in-vitro methods of antioxidant activity must be viewed with great skepticism.

One randomized controlled trial [36] of 78 patients with peripheral arterial disease treated with a garlic extract showed no clinical benefit. A meta-analysis [37••] of three studies using garlic-only preparations to treat hypertension found a mean decrease of 8.4 ± 2.8 mmHg for systolic BP and 7.3 ± 1.5 mmHg for diastolic BP compared with placebo. A review [30] of the effects of garlic on several cardiovascular risk factors confirms a small reduction in total cholesterol at 1 and 3 months, but not at 6 months, changes in lipoproteins and triglycerides that were not statistically significant, mixed effects on BP outcomes, and significant reductions in platelet aggregation. Further studies with standardized garlic preparations are needed in patients with atherosclerosis or hypertension.

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Effect on platelet function

Increased platelet aggregation is a risk factor in the pathogenesis of atherosclerotic heart disease, and the antithrombotic effect of garlic consumption has been well studied in vitro. Garlic preparations inhibit cyclooxygenase activity and thromboxane A2 formation [38•]. The mechanism of this inhibition is due to multiple steps in platelet aggregation. Garlic suppresses intracellular calcium mobilization, increases intracellular levels of cyclic AMP and cyclic GMP, activates nitric oxide synthase and thus increases nitric oxide derived from platelets, and interacts with glycoprotein (GP)IIb/IIIa receptors, inhibiting platelet binding to fibrinogen. The activity in garlic that leads to antiplatelet activity survives heating by microwave, and boiling or heating at 200°C for 3 min, but not longer [39•]. Nine of 12 studies in humans have shown that consumption of garlic preparations led to inhibition of platelet aggregation [38•]. The range of garlic preparations included aged garlic extract, garlic powder, ethyl acetate extract, and oil extract. However, no comparison can be made because the garlic preparations were not all standardized and the trials were of different length. Some were in healthy volunteers and some with hyperlipidemia or hypertension. None of the studies measured clinical outcomes. When a garlic preparation was used for 2 weeks to test the effect on collagen-stimulated platelet function, no effect was found [40•]. Thus, the effect on platelet aggregation may be the best documented effect of garlic preparations in humans, but it has not yet been shown to have a clinically significant effect, either in causing bleeding, preventing thrombotic sequelae, or leading to alteration of doses of anticoagulant medication.

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Adverse events

The most common adverse events from ingestion of garlic preparations are malodorous breath and body odor [30]. Contact dermatitis does occur but only in atopic individuals, and is not so commonly seen as with many excipients in skin preparations [41•]. Gastrointestinal symptoms occur, but there is no evidence that they are specific.

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Conclusion

Data from in-vitro experiments in animals and with human tissue, and from in-vivo animal studies provide intriguing suggestions that there are active ingredients in natural garlic that might have medicinal use. However, the active ingredients of garlic are not known with certainty. There are many possible candidates, and it is possible that they interact with each other or other components of garlic, either positively or negatively. Moreover, garlic contains other components such as vitamin E that might account for some of the activity seen. There are almost no dose-equivalence studies to relate the in-vitro and animal studies to concentrations that might produce effects in humans, nor have the many available commercial garlic preparations been compared within studies except in a few reports. Finally, there are no studies demonstrating a meaningful clinical benefit for garlic. The effects that have been noted (lowering cholesterol and inhibiting platelet aggregation) are quite modest, and not all studies agree on the effect. We should watch with interest to see what developments occur in future, but until there is agreement on the active ingredient(s) and proper dose responses can be demonstrated for the potential effects, the use of garlic will continue in the realm of folk medicine.

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References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

• of special interest

•• of outstanding interest

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3•• Gorinstein S, Jastrzebski Z, Namiesnik J, et al. The atherosclerotic heart disease and protecting effects of garlic: contemporary data. Mol Nutr Food Res 2007; 51:1365–1381. A review of the active chemical ingredients of garlic, along with a general review of studies using garlic to prevent heart disease.
4•• Powolny AA, Singh SV. Multitargeted prevention and therapy of cancer by diallyl trisulfide and related Allium vegetable-derived organosulfur compounds. Cancer Lett 2008; 269:305–314. A review of the role of garlic in prevention of cancers.
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9 Jo HJ, Song JD, Kim KM, et al. Diallyl sulfide induces reversible G2/M phase arrest on a p53-independent mechanism in human colon cancer HCT-116 cells. Oncol Rep 2008; 19:275–280.
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18• Millen AE, Sabar AF, Graubard BI, et al. Fruit and vegetable intake and prevalence of colorectal adenoma in a cancer screening trial. Am J Clin Nutr 2007; 86:1754–1764. The effect of garlic could not be distinguished from other ingested fruits and vegetables.
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20 Tanaka S, Haruma K, Yoshihara M, et al. Aged garlic extract has potential suppressive effect on colorectal adenomas in humans. J Nutr 2006; 136:821S–826S.
21 Li H, Li HQ, Wang Y, et al. An intervention study to prevent gastric cancer by micro-selenium and large dose of allitridum. Chin Med J (Engl) 2004; 117:1155–1160.
22 You WC, Brown LM, Zhang JY, et al. Randomized double-blind factorial trial of three treatments to reduce the prevalence of precancerous gastric lesions. J Natl Cancer Inst 2006; 98:974–983.
23•• Kim JY, Kwon O. Evidence-based review of the garlic intake and cancer risk for food labeling. Am J Clin Nutr 2009; 89:257–264. A review of clinical studies in CRC, finding no compelling data to support a role for garlic supplements.
24 Kannar D, Wattanapenpaiboon N, Saige GS, Wahlqvist ML. Hypercholesterolemic effect of an enteric-coated garlic supplement. J Am Coll Nutr 2001; 20:225–231.
25•• Gardner CD, Lawson LD, Block E, et al. Effect of raw garlic vs commercial garlic supplements on plasma lipid concentrations in adults with moderate hypercholesterolemia. Arch Intern Med 2007; 167:346–353. A study that compares roughly equivalent potency of three different preparations of garlic.
26• Duda G, Suliburska J, Pupek-Musialik D. Effects of short-term garlic supplementation on lipid metabolism and antioxidant status in hypertensive adults. Pharmacol Rep 2008; 60:163–170. A prospective but uncontrolled study.
27 Baliarsingh S, Beg ZH, Ahmad J. The therapeutic impacts of tocotrienols in type 2 diabetic patients with hyperlipidemia. Atherosclerosis 2005; 182:367–374.
28• Liu CT, Sheen LY, Lii CK. Does garlic have a role as an antidiabetic agent? Mol Nutr Food Res 2007; 51:1353–1364. Blood sugar was lowered in alloxan rats, perhaps by increasing insulin secretion.
29• Sobenin IA, Nedosugova LV, Filatova LV, et al. Metabolic effects of time-released garlic powder tablets in type 2 diabetes mellitus: the results of double-blinded placebo-controlled study. Acta Diabetol 2008; 45:1–6. One of the few prospective double-blind studies using garlic preparations in humans.
30 Ackermann RT, Mulrow CD, Ramirez G, et al. Garlic shows promise for improving some cardiovascular risk factors. Arch Intern Med 2001; 161:813–824.
31• Sener G, Sakarcan A, Yegen BC. Role of garlic in the prevention of ischemia-reperfusion injury. Mol Nutr Food Res 2007; 51:1345–1352. Decreased lipid peroxidation was noted, but no ‘clinical’ endpoints were reported in these animal experiments.
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33• Avci A, Atli T, Erguder IB, et al. Effects of garlic consumption on plasma and erythrocyte antioxidant parameters in elderly subjects. Gerontology 2008; 54:173–176. Garlic (0.1 g/kg) improved ex-vivo oxidation reactions, with no clinical endpoint data.
34•• Frankel EN, Finley JW. How to standardize the multiplicity of methods to evaluate natural antioxidants. J Agric Food Chem 2008; 56:4901–4908. A review of the various methods to determine antioxidant properties of foods.
35• Scholz S, Williamson G. Interactions affecting the bioavailability of dietary polyphenols in vivo. Int J Vitam Nutr Res 2007; 77:224–235. Absorption of antioxidants is modified by the presence of other foods.
36 Meher S, Duley L. Garlic for preventing preeclampsia and its complications. Cochrane Database Syst Rev 2006:CD006065.
37•• Reid K, Frank OR, Stocks NP, et al. Effect of garlic on blood pressure: a systematic review and meta-analysis. BMC Cardiovascular Disorders 2008; 8:13. A small effect on blood pressure was found, but the analysis was derived from only three studies.
38• Rahman K. Effects of garlic on platelet biochemistry and physiology. Mol Nutr Food Res 2007; 51:1335–1344. Nine out of 12 studies with human platelets showed a decrease in aggregation
39• Cavagnaro PF, Camargo A, Galmarini CR, Simon PW. Effect of cooking on garlic (Allium sativum L.) antiplatelet activity and thiosulfinates content. J Agric Food Chem 2007; 55:1280–1288. Activity of garlic preparations can survive, mild or short heating times.
40• Beckert BW, Concannon MJ, Henry SL, et al. The effect of herbal medicines on platelet function: an in vivo experiment and review of the literature. Plast Reconstr Surg 2007; 120:2044–2050. No effect on collagen-stimulated platelet function was found.
41• McFadden JP, White JML, Basketter DA, Kimber I. Reduced allergy rates in atopic eczema to contact allergens used in both skin products and foods: atopy and the ‘hapten-atopy hypothesis’. Contact Dermatitis 2008; 58:156–158. Contact dermatitis with garlic preparations was seen only in atopic individuals.
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