Effects of Whole Grains on Coronary Heart Disease Risk
Curr Atheroscler Rep (2010) 12:368–376DOI 10.1007/s11883-010-0136-1Effects of Whole Grains on Coronary Heart Disease RiskKristina A. Harris & Penny M. Kris-EthertonPublished online: 7 September 2010# Springer Science+Business Media, LLC 2010Abstract Characterizing which types of carbohydrates, Keywords Whole grains . Coronary heart disease .including whole grains, reduce the risk for coronary heart Cardiovascular disease . Risk factors . Processing .disease (CHD) is challenging. Whole grains are characterized Nutrition . Carbohydrates . Cereal fiber . Phytochemicals .as being high in resistant carbohydrates as compared with Metabolic syndromerefined grains, meaning they typically are high in fiber,nutrients, and bound antioxidants. Whole grain intakeconsistently has been associated with improved cardiovascu- Introductionlar disease outcomes, but also with healthy lifestyles, in largeobservational studies. Intervention studies that assess the The 2005 Dietary Guidelines for Americans recommendedeffects of whole grains on biomarkers for CHD have mixed intake of whole grains, based on evidence from bothresults. Due to the varying nutrient compositions of different population and intervention studies, is at least three ounceswhole grains, each could potentially affect CHD risk via per day . The Dietary Guidelines Advisory Committeedifferent mechanisms. Whole grains high in viscous fiber (DGAC) 2010 Report emphasizes fiber-rich carbohydrate(oats, barley) decrease serum low-density lipoprotein choles- foods such as whole grains and vegetables, fruits, andterol and blood pressure and improve glucose and insulin cooked dry beans and peas. It specifically recommends thatresponses. Grains high in insoluble fiber (wheat) moderately half of the grains consumed be whole grains, hence somelower glucose and blood pressure but also have a prebiotic whole grains should replace refined grains . Recenteffect. Obesity is inversely related to whole grain intake, but evidence has shown that the beneficial effects of replacingintervention studies with whole grains have not produced saturated fat with carbohydrate depend on the type ofweight loss. Visceral fat, however, may be affected favorably. carbohydrate replaced [3, 4]. This raises important questions:Grain processing improves palatability and can have varying what carbohydrates are most beneficial for cardiovasculareffects on nutrition (e.g., the process of milling and grinding health, and where do whole grains fit into a healthy diet?flour increases glucose availability and decreases phytochem- This review examines the evidence and the complexitiesical content whereas thermal processing increases available surrounding the use of whole grains to reduce risk forantioxidants). Understanding how individual grains, in both coronary heart disease (CHD).natural and processed states, affect CHD risk can informnutrition recommendations and policies and ultimately benefitpublic health. Carbohydrate Classification: Where do Whole Grains Fit?K. A. Harris : P. M. Kris-Etherton (*) Whole grains are referred to as “complex” or “high-quality”Department of Nutritional Sciences, carbohydrates, mainly due to their dietary fiber content;The Pennsylvania State University,110 Chandlee Laboratory, however, a specific definition of “high-quality” is needed.University Park, PA 16802, USA One scheme is to differentiate carbohydrates functionallye-mail: firstname.lastname@example.org based on their ability to produce a glycemic response (i.e., a
Curr Atheroscler Rep (2010) 12:368–376 369rise in blood glucose) [5•]. “Available” carbohydrates regulated and can be confusing. Grains can be ground, e(sugars, starches) have α-1-4 and a1 À 6 glucosidic linkages cooked, parboiled, extruded, pearled, rolled, and eventhat are digested by salivary and pancreatic enzymes and are milled (Table 2) as long as the final product has all threeabsorbed readily in the small intestine, eliciting a marked parts present in the appropriate proportions.glycemic response. “Resistant” carbohydrates (fiber or non- To ensure that products labeled with a whole grain healthstarch polysaccharides, certain short chain carbohydrates, claim will provide substantive amounts of whole grains, itsugar alcohols) have different glucosidic linkages that limit must be the first ingredient listed on the ingredient label,digestion and absorption, and consequently produce little or meaning it makes up 51% of the product by weight .no glycemic response [5•]. DGAC 2010 calls for the development of criteria for Another classification scheme is the glycemic index, labeling whole grain foods to decrease confusion both forwhich compares the postprandial glucose response of researchers and consumers .carbohydrate-containing foods to that of a standard (i.e.,glucose or white bread) . However, the poor within-person reproducibility of the index brings into question Whole Grain Intake is Associated with Lower CVDhow well the index applies on a population-wide scale . Risk and Healthier LifestylesAlthough the glycemic index has been used to characterizefoods that decrease risk for chronic disease, the 2010 report Numerous prospective cohort studies of both men andof Dietary Guidelines Advisory Committee (DGAC 2010) women have reported an inverse relationship betweenreported little to no association between glycemic index and chronic intake of whole grains and CHD, such as heartweight loss, type 2 diabetes, and cancer, and an inconclu- failure , fatal and nonfatal CHD [13, 14], fatal andsive association with cardiovascular disease (CVD) . nonfatal coronary artery disease , and fatal ischemicConsequently, the overall healthfulness of a carbohydrate- heart disease . The average adjusted hazard ratios fromrich food cannot be based solely on its glycemic response these studies suggest a risk reduction of 7%–30% comparingbecause this ignores the type of fiber and the vitamins, whole grain consumers versus low or nonconsumers. Theseminerals, and bioactive non-nutrient plant compounds studies assessed whole grain intake specifically, rather than(phytochemicals) potentially present in these foods. Thus, fiber, cereal fiber, bran, or low-glycemic carbohydrates, buta chemical definition of grain and grain products yielding a not all studies used whole grain definitions that met FDAratio of available to resistant carbohydrates may be a more standards [8•]. Jacobs and Gallaher  estimated a 20%–consistent metric for classifying foods. 40% reduction in CHD risk with frequent whole grain consumption based on 17 prospective cohort studies. In a meta-analysis of 12 prospective cohort studies, Anderson etWorking Definitions of Whole Grains al.  reported a 26% reduction in CHD risk in individuals who consumed whole grains regularly.Whole grain products are derived from cereals, which are DGAC 2010 rated the evidence for the protectivedefined as the fruit of plants belonging to the Poacea (or relationship between whole grains and CVD as “moderate”Gramineae) family of grasses. These include wheat, rice, . In observational studies, causality cannot be assigned,barley, corn, rye, oats, millets, sorghum, tef, triticale, canary and it is unknown whether the whole grains are protectiveseed, Job’s tears, Fonio, and wild rice (Table 1). The term or are simply a marker of healthy lifestyles. For example,“pseudo-cereals” includes seeds from non-Gramineae whole grain intake is positively associated with vitamin usefamilies that function as cereals, such as amaranth, and negatively associated with body mass index (BMI),buckwheat, and quinoa [8•]. All grains are comprised waist circumference, and smoking status . Anotherof 1) bran—the multi-layered fibrous coat that protects challenge in observational studies is determining thethe grain from sun, pests, and diseases; 2) endosperm—the amount of whole grains consumed. Dietary intake data areenergy supply for the germ and plant; and 3) germ—the prone to misreporting and the number of new foodsembryo of the plant (Fig. 1) [9••]. containing whole grains is increasing rapidly. Earlier Because most whole grains are processed, the US Food studies counted whole grain intake from natural grains,and Drug Administration (FDA), in concert with the dark breads, and cereals with >25% whole grains byAmerican Association of Cereal Chemists, established a weight, whereas current studies count whole grain fromlabeling definition. To be considered a “whole grain,” each any food with as little as 10% whole grain . As wholeof the principal components of the grain (endosperm, germ, grains are incorporated into more processed foods, theseand bran) must be present in the same relative proportion as foods (that may not contain 51% whole grain by weight)they exist naturally in the seed . On the other hand, must be included in assessing whole grain intake. Indeed,terms such as “whole wheat” or “multi-grain” are not the relationships between whole grain intake and disease
370 Curr Atheroscler Rep (2010) 12:368–376Table 1 Summary of effects of whole grains on CHD risk factorsWhole grain Effect on CHD risk Potential MechanismWheat Improves glycemic control and Presence of bran decreases glucose absorption  insulin sensitivity SCFA from gut fermentation of resistant carbohydrates improves insulin sensitivity  Decreases inflammatory markers Bound and free antioxidant capacity equal to that of fruits and berries  High amount of vitamin E, ferulic acid, flavanoids Decreases blood pressure Via improvements in weight, insulin sensitivity, inflammatory status Associated with healthy BMI Population studies repeatedly found significant associations between healthy body weight and whole grain intake Oats Lowers LDL-C and TC Viscous fiber (β-glucan) becomes gel-like in intestine to increase bile acid excretion and Improves glycemic control and slow glucose absorption [32, 73] insulin sensitivity Decreases blood pressureBarley Lowers LDL-C and TC Viscous fiber (β-glucan) becomes gel-like in intestine to increase bile acid excretion and slow glucose absorption [25, 73] Decreases visceral fat Unknown mechanism; may be due to insulin sensitivity or increased satiety and weight loss  May improve antioxidant status High amount of vitamin E, phytochemicals Rye Improves glycemic response Starch structure in bread creates more resistant carbohydrate  May improve antioxidant status High amounts of ferulic acid Rice May lower LDL-C Lipophilic antioxidant (γ-oryzanols) in rice bran oil shown to lower LDL-C BMI body mass index; CHD coronary heart disease; LDL-C low-density lipoprotein cholesterol; SCFA short-chain fatty acid; TC total cholesterolstatus may become less clear as whole grain flour is used in may bias to the null in observational studies, suggestinglow nutrient density foods such as sugary cereals and pizza. that whole grain intake may be even more beneficial thanStill, the imprecision in determining whole grain intakes hazard ratios indicate .Fig. 1 Structures of whole grains
Curr Atheroscler Rep (2010) 12:368–376 371Table 2 Processing techniques of grains and their effects on CHD riskProcessing Definition Positive effect on CVD risk Negative effect on CVD risk ExamplestechniqueMilling Dry: separating the May increase bioavailability Loss of bran and germ Grits, meal, flour bran and germ from of vitamins and minerals due results in lower vitamin, the starchy endosperm to loss of fiber and phytates mineral, phytochemical, to be ground to flour and fiber content Wet: seeping grain in Starch, syrup, water to soften before dextrose separating componentsGrinding, Crushing or rolling grain Increases bioavailability of Increases bioavailability Flours, rolled oats rolling to decrease particle size vitamins and minerals due of glucose thus increasing to increased surface area for glycemic and insulinemic enzymes responsesThermal Exposure to heat Increases small intestine Lysine becomes unavailable Bread, pasta absorption of phytochemicals, when combined with high especially those associated heat and reducing sugars with the cell wall; may form resistant starchExtrusion Using high temperature, No change in total fiber May use flour with smaller “Puffed” breakfast pressure, and shear to content, however may be particle size to puff cereal “puff” cereal interconversion between insoluble and viscous fiberFermentation Conversion of Presence of organic acids May use low-fiber flours Sourdough bread, carbohydrate to simpler can improve glycemic alcohols, molecules using yeast or response possibly via slowed grain tempeh bacteria in anaerobic starch digestion conditionsParboiling Partial boiling or cooking Some nutrients in bran Parboiled grains often do Parboiled rice of a grain transfer to endosperm before not have bran millingNixtamalization Soaking and cooking Releases niacin from bound Corn flour is refined Corn hominy, grain in an alkaline form to be absorbed; tortillas, tamales solution then hulling improves bioavailability of calcium, iron, copper, and zincCVD cardiovascular disease(Data from Slavin et al. )Effects and Mechanisms of Whole Grains on CHD Risk ready-to-eat oat cereal confirmed this relationship, showing aFactors greater LDL-C–lowering effect than the low-fiber control cereal after 12 weeks in free-living individuals .Dyslipidemia Furthermore, barley lowered both TC and LDL-C compared with rice  and in a dose-dependent manner . DietsNumerous cross-sectional studies have reported an inverse containing whole grains low in viscous fiber typically do notassociation between whole grain intake and dyslipidemia [13, affect lipids [26••, 27••].19, 21]. Intervention trials have produced mixed results, β-glucan is a type of viscous fiber in barley and oats thatwhich reflect the type of whole grain studied. Oats and increases fecal loss of bile acids, which are derivatives ofbarley improve lipids more than wheat or brown rice, cholesterol. About 90% of the bile acids entering the smallprobably because of differences in viscous fiber content. A intestine for fat absorption are reabsorbed in the ileum.Cochrane meta-analysis evaluated ten intervention trials β-glucan reduces the reabsorption of bile acids, thereby(eight of which tested oats) to assess the effect of whole increasing bile acid excretion, lowering the bile acid levelsgrains on CVD risk factors. Oats consistently lowered in the liver, and increasing the conversion rate oftotal cholesterol (TC) (−0.20 mmol/L; 95% CI, −0.31 to cholesterol to bile acids. The liver obtains the additional−0.10) and low-density lipoprotein cholesterol (LDL-C) cholesterol by upregulating LDL receptors and increasing(−0.18 mmol/L; 95% CI, −0.28 to −0.09) compared with LDL particle uptake, thus reducing circulating LDL-C .the control diets . A recent study with a high-fiber, A viscous fiber intake of 10–25 g/d is recommended by the
372 Curr Atheroscler Rep (2010) 12:368–376National Cholesterol Education Program’s Adult Treatment do . Increased viscosity in the gut may be morePanel III as an additional diet option to decrease LDL-C. effective in lowering glucose responses due to decreasedAn intake of 5–10 g/d lowers LDL-C by about 5% . gastric emptying rates and absorption . Third, when grain is ground to produce flour, the surface area forHypertension hydrolysis of starch is increased greatly, which would increase glucose absorption . Indeed, whole kernelEvidence to support benefits of whole grains on hypertension barley or cracked wheat breads had lower glycemic indexis growing. Two large prospective cohort studies reported that values than white bread ; however, coarse, ultra-fine,about three servings (16 g per serving) of whole grain per day and white wheat flour breads all produced the sameis associated with a decreased risk of developing hypertension glycemic and insulinemic responses in healthy adults ,by 19% (95% CI, 75%–87%) in men  and by 33% (95% perhaps due to the relatively similar particle sizes of floursCI, 66%–89%) in women . Multiple types of grains and as compared intact kernels. Fourth, the presence of organicwhole grain foods can lower blood pressure in hypertensive acids (added or from sourdough fermentation) can lower[32, 33] and normotensive (yet hypercholesterolemic) glycemic response, possibly via a lower rate of starchindividuals . The hypotensive effects of whole grains digestion. Despite the lack of fiber, sourdough bread (madeare thought to be mediated by improvements in other risk with refined wheat flour) produced lower glucose andfactors such as body weight, dyslipidemia, and insulin insulin responses than white, whole wheat and whole-wheatresistance. Whole grains are emphasized in the Dietary barley breads . The research to date indicates that starchApproaches to Stop Hypertension (DASH) diet, and structure, viscosity, particle size, and the presence ofincreased intake is recommended by the Seventh Panel organic acids affect glucose availability.of the Joint National Committee on the Treatment ofHypertension [35, 36]. Obesity and Metabolic SyndromeGlycemic Control Increased whole grain intake consistently is associated with lower BMI in the United States [19, 21, 40, 49, 50] and theIn large observational studies, whole grains are inversely Netherlands ; however, this was not observed in arelated to risk of developing type 2 diabetes mellitus [37– British population . Longitudinal data from a large39] and are associated with lower serum glucose and cohort of healthy, male health professionals reported thatinsulin [19, 21, 40]. However, randomized controlled trials every 40-g/d increment of whole grains was associated with(RCTs) have reported mixed results on the effects of whole a reduction of 0.49 kg in body weight over 8 years .grains on glycemic control. Pereira et al.  conducted a Whole grains have not, however, facilitated weight loss incontrolled-feeding, crossover RCT with 11 hyperinsulinemic the few RCTs that have been conducted [26, 52].adults on either whole or refined grain diets (consisting of 12 Metabolic syndrome, arising primarily as the result of30-gram servings per day) for 6 weeks and found an excess visceral adiposity, is defined by having at least threeimprovement of insulin sensitivity after the whole grain diet. of following risk factors: increased triglycerides, glucose,Two large, free-living studies, however, did not find any blood pressure, and waist circumference and decreasedchange in insulin sensitivity in either a cross-over (112 g/d of high-density lipoprotein cholesterol (HDL-C) . Wholewhole grains for 6 weeks)  or a parallel arm (60–120 g/d grain intake of about two servings per day was associatedof whole grains for 8–16 weeks) [27••] study. with decreased prevalence of metabolic syndrome in a Studies examining the glycemic response to different cross-sectional study . In individuals with metabolicgrains (wheat, rye) and whole grain products (breads, syndrome, the effects of whole grains on glycemic controlpastas) do not provide a consistent explanation for the are mixed, as there are benefits on blood pressure anddiscrepancy between the observational and intervention weight (see previous sections) whereas there are no effectsstudies, but rather raise more questions. First, grains with a on TG and HDL-C [27••].higher percentage of amylose starch instead of amylopectin Whole grains seem to have the greatest effect on thehave lower glycemic responses . Amylose (a single visceral adipose tissue component of metabolic syndrome.strand of glucose molecules) is more resistant to digestion When visceral adipose tissue mass is reduced, there isthan amylopectin (a highly branched polymer with many significant improvement in CVD risk factors, even withsites for hydrolysis) . Second, unprocessed bran (high only modest weight loss. Whole grain (about three servingsin fiber) blocks exposure of the rapidly absorbable glucose per day) and cereal fiber (about 9 g/d) intake were inverselypolymers within the endosperm to digestive enzymes. associated with trunk fat mass (as determined by DXA)Interestingly, the presence of finely ground insoluble fiber . For every 10-g/d increment in cereal fiber intake,does not change the glycemic response while intact kernels weight was decreased by 0.77 kg/y (95% CI, −0.127 to
Curr Atheroscler Rep (2010) 12:368–376 373−0.026 kg/y) and waist circumference was decreased by may contribute to the health benefits of whole grains.0.10 cm/y (95% CI, −0.18 to 0.02 cm/year) over 6.5 years Resistant carbohydrates in whole grains fall under theof follow-up in a European adult cohort . Davis et al. broader definition of prebiotics, meaning they provide[56••] assessed fiber intake in Latino youth over the course fuel for saccharolytic bacteria such as Bifidobacteriumof 2 years and found that decreased fiber intake (average . (Probiotics, in contrast, provide bacteria to colonizedecrease of 3 g of fiber per 1,000 kcal/d) was associated the colon). It is possible that some of the effects of wholewith a 21% increase in visceral fat mass as compared with grains on metabolic risk factor are mediated by theirthose who increased fiber intake and decreased visceral fat abilities to favor the growth of certain types of gutmass by 4%. Finally, two RCTs reported significantly more flora.visceral fat loss, irrespective of total weight loss, when The majority of the bacteria in the human gut are of theparticipants consumed whole grain as compared with Bacteroidetes (48%) and Firmicutes (51%) divisions, butrefined grain diets for 12 weeks [24, 26••]. The mechanism there is great interpersonal variation in bacterial species, withby which whole grains decrease or prevent visceral fat gain some people having significant amounts of Bifidobacteriumbeyond weight loss is unknown; however, it may be due and Lactobacillus . Interestingly, animal  and humanto increased insulin sensitivity in adipose tissue, which  studies have found differences in bacterial populationsdecreases adipose lipoprotein lipase activity, thereby reducing between lean and obese individuals [64, 67]. Whether this isfatty acid uptake for storage in visceral fat stores. a cause, an effect, or unrelated to the obese state is not known. Compared with normal-weight mice, obese miceChronic Inflammation have 50% less Bacteroidetes and 50% more Firmicutes . During weight loss in humans there was an associatedChronic inflammation is central in the progression of many increase in Bacteroidetes, which correlated with weight lossdiseases. Markers of inflammation, such as C-reactive but not caloric intake .protein (CRP), tumor necrosis factor receptor 2 (TNF-R2) These observations suggest that the type of bacteria, plasminogen activator inhibitor-1 (PAI-1) , and present in the gut may affect caloric availability, whichinterleukin-6 (IL-6) , were inversely related to whole can affect weight loss (independent of decreased energygrain intake in multiple cross-sectional studies. Some of intake), and that different types of whole grains maythese relationships were attenuated in a multivariate change the character of the biota. The bacterial fermen-analysis that included insulin and obesity measures in the tation of resistant carbohydrates yields different productsmodel, meaning that the effects of whole grains on insulin depending on the type of fuel and bacteria. Fructo-resistance and excess adipose tissue could explain the oligosaccharides improve lipid metabolism, immuneassociation. In one recent intervention study (n=50), CRP status, glycemic control and vitamin and mineral absorp-was lowered on a whole grain diet compared with a refined tion, whereas other resistant carbohydrates (resistantgrain diet [26••]. Conversely, a larger study (n=316) did not starch, inulin) have more varied effects . Thefind differences in inflammatory status in participants on a products of colonic fermentation are short-chain, volatilefree-living diet who consumed whole or refined grains for fatty acids (SCFA) such as acetate, propionate, and16 weeks [27••]. butyrate. The former two enter the portal vein and are Components of whole grains, whether in their native and metabolized by the liver whereas the latter is an energyprocessed states, have a similar antioxidant capacity as do source for enterocytes . Acetate, the most abundantmany fruits and vegetables . Most of the phytochemicals product, does not stimulate insulin release, prevents freeare bound in the resistant carbohydrate fraction and are not fatty acid oxidation, and may have a hypercholesterolemicabsorbed unless released by bacteria in the large intestine. effect by entering cholesterogenic pathways . Propio-Refined grains have only about 20% of the natural nate may moderate lipid metabolism in humans byantioxidant capacity of whole grains . Some types of competing with acetate for entrance into hepatic cells,processing can actually enhance antioxidant capacity, such as thereby preventing excess cholesterol production . Anthermal treatment, which releases many of the grain increase in the ratio of propionate to acetate in the portalphytochemicals from the bound to the free state, thus vein may be responsible for the cholesterol-loweringmaintaining or increasing the antioxidant availability . effect of fermented resistant carbohydrates. An increase in total SCFA may decrease serum long-chain free fatty acid concentrations, which oppose the action ofResistant Carbohydrates: Fuel for the Gut Microbiota acetate . Nevertheless, lowering free fatty acid levels can improve the lipid profile and insulin sensitivity by increasingThe interaction between resistant carbohydrates and the insulin-mediated suppression of gluconeogenesis, decreasingmicrobiota (bacterial population) in the large intestine very-low density lipoprotein synthesis and increasing insulin
374 Curr Atheroscler Rep (2010) 12:368–376clearance . Hyperinsulinemic individuals supplemented Disclosure PM Kris-Etherton’s and KA Harris’ employer has received a grant from General Mills to conduct clinical trials assessingwith a high wheat fiber cereal (24 g/d of fiber) for 1 year had the effect of whole grains on metabolic syndrome.an increase in glucagon-like peptide-1 (a hormone related to KA Harris is supported by the Nestle PhD, RD Training Fellowship,insulin sensitivity) and SCFA production compared with the which is a competitive award funded by Nestle Research Center for alow-fiber cereal control group . SCFA levels were nutritional science graduate student pursuing both degrees at the Pennsylvania State University.increased and free fatty acid levels decreased postprandiallyin 12 healthy adults after consumption of inulin, a specificfermentable fiber . In summary, whole grains provide Referencesfuels that can change the composition of colonic bacteriaand also can increase SCFA concentrations and improve Papers of particular interest, published recently, have beenpostprandial lipid and glycemic processes. highlighted as: • Of importance •• Of major importancePros and Cons of Processing 1. United States Department of Agriculture, United States DepartmentProcessing techniques to make grains more palatable and of Health and Human Services: Dietary Guidelines for Americans,nutritious have been used for centuries. Currently, grains 6th edn. Washington, DC: Government Printing Office; 2005.are processed primarily to improve taste but also for 2. United States Department of Agriculture, United States Department of Health and Human Services: Report of the Dietary Guidelinesnutrition  (Table 2). Milling separates the bran and the Advisory Committee on the Dietary Guidelines for Americans.germ from endosperm that will be used for flour, but all Washington, DC: Government Printing Office; 2010.components can be added back into flour at the end of 3. Siri-Tarino PW, Sun Q, Hu FB, Krauss RM: Meta-analysis ofprocessing. The loss of the bran and germ decreases the prospective cohort studies evaluating the association of saturated fat with cardiovascular disease. Am J Clin Nutr 2010, 91:535–546.nutritional quality of the grain; however, the loss of 4. Jakobsen MU, Dethlefsen C, Joensen AM, et al.: Intake ofphytates and fiber increases bioavailability of certain carbohydrates compared with intake of saturated fatty acidsvitamins and minerals. Grinding increases bioavailability and risk of myocardial infarction: importance of the glycemicof all nutrients in the grain and has both a positive index. 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