Heated Vs Unheated Roast Beef Nutrition

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J Am Diet Assoc. Author manuscript; available in PMC 2013 Jul 8.

Published in final edited form as:

PMCID: PMC3704564

NIHMSID: NIHMS482555

Advanced Glycation End Products in Foods and a Practical Guide to Their Reduction in the Diet

JAIME URIBARRI, MD, SANDRA WOODRUFF, RD, SUSAN GOODMAN, RD, WEIJING CAI, MD, XUE CHEN, MD, RENATA PYZIK, MA, MS, ANGIE YONG, MPH, GARY E. STRIKER, MD, and HELEN VLASSARA, MD

Abstract

Modern diets are largely heat-processed and as a result contain high levels of advanced glycation end products (AGEs). Dietary advanced glycation end products (dAGEs) are known to contribute to increased oxidant stress and inflammation, which are linked to the recent epidemics of diabetes and cardiovascular disease. This report significantly expands the available dAGE database, validates the dAGE testing methodology, compares cooking procedures and inhibitory agents on new dAGE formation, and introduces practical approaches for reducing dAGE consumption in daily life. Based on the findings, dry heat promotes new dAGE formation by >10- to 100-fold above the uncooked state across food categories. Animal-derived foods that are high in fat and protein are generally AGE-rich and prone to new AGE formation during cooking. In contrast, carbohydrate-rich foods such as vegetables, fruits, whole grains, and milk contain relatively few AGEs, even after cooking. The formation of new dAGEs during cooking was prevented by the AGE inhibitory compound aminoguanidine and significantly reduced by cooking with moist heat, using shorter cooking times, cooking at lower temperatures, and by use of acidic ingredients such as lemon juice or vinegar. The new dAGE database provides a valuable instrument for estimating dAGE intake and for guiding food choices to reduce dAGE intake.

Advanced glycation end products (AGEs), also known as glycotoxins, are a diverse group of highly oxidant compounds with pathogenic significance in diabetes and in several other chronic diseases (1–6). AGEs are created through a nonenzymatic reaction between reducing sugars and free amino groups of proteins, lipids, or nucleic acids. This reaction is also known as the Maillard or browning reaction (7). The formation of AGEs is a part of normal metabolism, but if excessively high levels of AGEs are reached in tissues and the circulation they can become pathogenic (2). The pathologic effects of AGEs are related to their ability to promote oxidative stress and inflammation by binding with cell surface receptors or cross-linking with body proteins, altering their structure and function (8–10). Among the better-studied AGEs are the stable and relatively inert N ε -carboxymethyllysine (CML) and the highly reactive derivatives of methyl-glyoxal (MG). Both these AGEs can be derived from protein and lipid glycoxidation (11,12).

In addition to AGEs that form within the body, AGEs also exist in foods. AGEs are naturally present in uncooked animal-derived foods, and cooking results in the formation of new AGEs within these foods. In particular, grilling, broiling, roasting, searing, and frying propagate and accelerate new AGE formation (7,13). A wide variety of foods in modern diets are exposed to cooking or thermal processing for reasons of safety and convenience as well as to enhance flavor, color, and appearance. The fact that the modern diet is a large source of AGEs is now well-documented (3,7,13). Because it had previously been assumed that dietary AGEs (dAGEs) are poorly absorbed, their potential role in human health and disease was largely ignored. However, recent studies with the oral administration of a single AGE-rich meal to human beings as well as labeled single protein-AGEs or diets enriched with specific AGEs such as MG to mice clearly show that dAGEs are absorbed and contribute significantly to the body's AGE pool (14–16).

Consumption of AGE-rich diets by mice is associated with elevated circulating and tissue AGEs and conditions such as atherosclerosis (17) and kidney disease (18). On the other hand, restriction of dAGEs prevents vascular and kidney dysfunction (18,19), diabetes type 1 or type 2 (20), improves insulin sensitivity (21,22), and accelerates wound healing (23). Low dAGE intake has also been shown to lengthen lifespan to the same extent as does energy restriction in mice (16). Studies in healthy human beings show that dAGEs directly correlate with circulating AGEs, such as CML and MG, as well as with markers of oxidative stress (24). Moreover, restriction of dAGEs in patients with diabetes (25) or kidney disease (26,27) as well as in healthy subjects (28) also reduces markers of oxidative stress and inflammation. Together, the findings from animal and human studies suggest that avoidance of dAGEs in food helps delay chronic diseases and aging in animals and possibly in human beings (3).

From a practical perspective, aside from a few reports, which include an initial dAGE database on 249 foods (13), this area is void of relevant information and guidance for professionals. The purpose of this report is to expand the existing dAGE database by more than twofold, validate the methods used to test AGEs in food, examine different procedures and reagents on new dAGE formed, and introduce practical methods to reduce the consumption of dAGEs in daily life.

METHODS

AGE Content of Foods

The AGE content of food samples was analyzed during the period 2003–2008. Foods were selected on the basis of their frequency on 3-day food records collected from healthy subjects in a catchment population in the Upper East Side and East Harlem in Manhattan, New York, NY. Therefore, these foods represent foods and culinary techniques typical of a Northeastern American multiethnic urban population. Foods were obtained from the cafeteria of The Mount Sinai Hospital, from local restaurants or supermarkets, or were prepared in the General Clinical Research Center at the Mount Sinai School of Medicine. Foods were subjected to standard cooking methods such as boiling (100°C), broiling (225°C), deep-frying (180°C), oven-frying (230°C), and roasting (177°C), unless otherwise stated in the database (see Table 1 available online at www.adajournal.org). The time of cooking varied as described in the database. Test procedures such as marinating, application of differing heating conditions, or cooking foods in differing fats or oils are also described in the database.

Table 1

The advanced glycation end product (AGE) content of 549 foods, based on carboxymethyllysine content

AGE Content
Food item AGEa kU/100g Serving size (g) AGE kU/serving
Fats
Almonds, blanched slivered (Bazzini's Nut Club, Bronx, NY) 5,473 30 1,642
Almonds, roasted 6,650 30 1,995
Avocado 1,577 30 473
Butter, whippedb 26,480 5 1,324
Butter, sweet cream, unsalted, whipped (Land O'Lakes, St Paul, MN) 23,340 5 1,167
Cashews, raw (Bazzini's Nut Club) 6,730 30 2,019
Cashews, roasted 9,807 30 2,942
Chestnut, raw 2,723 30 817
Chestnut, roasted, in toaster oven 350°F for 27 min 5,353 30 1,606
Cream cheese, Philadelphia soft, (Kraft, Northfield, IL) 10,883 30 3,265
Cream cheese, Philadelphia original (Kraft) 8,720 30 2,616
Margarine, tub 17,520 5 876
Margarine, tub, I Can't Believe it's Not Butter (Unilever, Rotterdam, The Netherlands) 9,920 5 496
Margarine, tub, Smart Balance (CFA Brands, Heart Beat Foods, Paramus, NJ) 6,220 5 311
Margarine, tub, Take Control (Unilever Best Foods) 4,000 5 200
Mayonnaise 9,400 5 470
Mayonnaise, imitation (Diet Source, Novartis Nutriton Group, East Hanover, NJ) 200 5 10
Mayonnaise, low fat (Hellman's, Unilever Best Foods) 2,200 5 110
Olive, ripe, large (5 g) 1,670 30 501
Peanut butter, smooth, Skippy (Unilever) 7,517 30 2,255
Peanuts, cocktail (Planters, Kraft) 8,333 30 2,500
Peanuts, dry roasted, unsalted (Planters, Kraft) 6,447 30 1,934
Peanuts, roasted in shell, salted (Frito-Lay, Plano, TX) 3,440 30 1,032
Pine nuts (pignolias), raw (Bazzini's Nut Club) 11,210 30 3,363
Pistachios, salted (Frito Lay) 380 30 114
Pumpkin seeds, raw, hulled (House of Bazzini, Bronx, NY) 1,853 30 556
Soybeans, roasted and salted (House of Bazzini) 1,670 30 501
Sunflower seeds, raw, hulled (House of Bazzini) 2,510 30 753
Sunflower seeds, roasted and salted (House of Bazzini) 4,693 30 1,408
Tartar Sauce, creamy (Kraft) 247 15 37
Walnuts, roasted 7,887 30 2,366
AGE kU/100 mL Serving size (mL) AGE kU/serving

Fat, liquid
Cream, heavy, ultra-pasteurized (Farmland Dairies, Fairlawn, NJ) 2,167 15 325
Oil, canola 9,020 5 451
Oil, corn 2,400 5 120
Oil, cottonseed (The B Manischewitz Company, Cincinnati, OH) 8,520 5 426
Oil, diaglycerol, Enova (ADM Kao LLC, Decatur, IL) 10,420 5 521
Oil, olive 11,900 5 595
Oil, olive, extra virgin, first cold pressed (Colavita, Linden, NJ) 10,040 5 502
Oil, peanut (Planters) 11,440 5 572
Oil, safflower (The Hain Celestial Group, Inc, Melville, NY) 3,020 5 151
Oil, sesame (Asian Gourmet) 21,680 5 1084
Oil, sunflower (The Hain Celestial Group, Inc) 3,940 5 197
Salad dressing, blue cheese (Kraft) 273 15 41
Salad dressing, caesar (Kraft) 740 15 111
Salad dressing, French (H. J. Heinz Co, Pittsburgh, PA) 113 15 17
Salad dressing, French, lite, (Diet Source, Novartis Nutr Corp) 0 15 0
Salad dressing, Italian (Heinz) 273 15 41
Salad dressing, Italian, lite (Diet Source, Novartis Nutr Corp) 0 15 0
Salad dressing, thousand island (Kraft) 187 15 28
AGE Content
Meats and meat substitutes AGE kU/100 g Serving size (g) AGE kU/serving
Beef
Beef, bologna 1,631 90 1,468
Beef, corned brisket, deli meat (Boar's Head, Sarasota, FL) 199 90 179
Beef, frankfurter, boiled in water, 212° F, 7 min 7,484 90 6,736
Beef, frankfurter, broiled 450°F, 5 min 11,270 90 10,143
Beef, ground, boiled, marinated 10 min w/lemon juice 1,538 90 1,384
Beef, ground, pan browned, marinated 10 min w/lemon juice 3,833 90 3,450
Beef, ground, 20% fat, pan browned 4,928 90 4,435
Beef, ground, 20% fat, pan/cover 5,527 90 4,974
Beef, hamburger (McDonald's Corpd, Oak Brook, IL) 5,418 90 4,876
Beef, hamburger patty, olive oil 180°F, 6 min 2,639 90 2,375
Beef, meatball, potted (cooked in liquid), 1 hc 4,300 90 3,870
Beef, meatball, w/saucec 2,852 90 2,567
Beef, meatloaf, crust off, 45 min 1,862 90 1,676
Beef, raw 707 90 636
Beef, roastb 6,071 90 5,464
Beef, salami, kosher (Hebrew National, ConAgra Foods, Omaha, NE) 628 90 565
Beef, steak, broiledc 7,479 90 6,731
Beef, steak, grilled 4 min, George Foreman grill (Salton Inc, Lake Forest, IL) 7,416 90 6,674
Beef, steak, microwaved, 6 min 2,687 90 2,418
Beef, steak, pan fried w/olive oil 10,058 90 9,052
Beef, steak, raw 800 90 720
Beef, steak, strips, 450°F, 15 minc 6,851 90 6,166
Beef, steak, strips, stir fried with 1 T canola oil, 15 min 9,522 90 8,570
Beef, steak, strips, stir fried without oil, 7 min 6,973 90 6,276
Beef, stewed, shoulder cutc 2,230 90 2,007
Beef, stewedb 2,657 90 2,391
Beef, stewed, (mean) 2,443 90 2,199
Poultry
Chicken, back or thigh, roasted then BBQb 8,802 90 7,922
Chicken, boiled in water, 1 h 1,123 90 1,011
Chicken, boiled with lemon 957 90 861
Chicken, breast, skinless, roasted with BBQ saucec 4,768 90 4,291
Chicken, breast, skinless, breadedb 4,558 90 4,102
Chicken, breast, skinless, breaded, reheated 1 minb 5,730 90 5,157
Chicken, breast, boiled in waterc 1,210 90 1,089
Chicken, breast, breaded, deep fried, 20 min 9,722 90 8,750
Chicken, breast, breaded, oven fried, 25 min, with skinc 9,961 90 8,965
Chicken, breast, breaded/pan friedc 7,430 90 6,687
Chicken, breast, grilled/George Foreman grill (Salton Inc) 4,849 90 4,364
Chicken, breast, pan fried, 13 min, highc 4,938 90 4,444
Chicken, breast, pan fried, 13 min high/microwave 12.5 secc 5,417 90 4,875
Chicken, breast, poached, 7 min, medium heatc 1,101 90 991
Chicken, breast, potted (cooked in liquid), 10 min medium heatc 2,480 90 2,232
Chicken, breast, roasted, 45 min with skinc 6,639 90 5,975
Chicken, breast, skinless, microwave, 5 min 1,524 90 1,372
Chicken, breast, skinless, poached, 15 min 1,076 90 968
Chicken, breast, skinless, raw 769 90 692
Chicken, breast, steamed in foil, 15 min, medium heatc 1,058 90 952
Chicken, breast, strips, stir fried with canola oil, 7 min 4,140 90 3,726
Chicken, breast, strips, stir fried without oil, 7 min 3,554 90 3,199
Chicken, breast, with skin, 450°F, 45 minc 8,244 90 7,420
Chicken, breast, skinless, broiled, 450°F, 15 min 5,828 90 5,245
Chicken, crispy (McDonald'sd) 7,722 90 6,950
Chicken, curry, cube skinless breast, panfry10 min, broiled 12 minc 6,340 90 5,706
Chicken, curry, cube skinless breast, steam 10 min, broiled 12 minc 5,634 90 5,071
Chicken, dark meat, broiled, inside, 450°F, 15 min 8,299 90 7,469
Chicken, fried, in olive oil, 8 min 7,390 90 6,651
Chicken, ground, dark meat with skin, rawc 1,223 90 1,101
Chicken, ground, dark w/skin, pan fried, w/canola oil, 2.5 min, high heatc 3,001 90 2,701
Chicken, ground, white meat, pan fried, no added fat, 5 min, high heatc 1,808 90 1,627
Chicken, ground, white meat, pan fried, with oil 1,647 90 1,482
Chicken, ground, white meat, raw 877 90 789
Chicken, kebab, cubed skinless breast, pan fried, 15 minc 6,122 90 5,510
Chicken, leg, roastedb 4,650 90 4,185
Chicken, loaf, roastedc 3,946 90 3,551
Chicken, loaf, roasted, crust offc 1,420 90 1,278
Chicken, meat ball, potted (cooked in liquid), 1 h 1,501 90 1,351
Chicken, nuggets, fast food (McDonald'sd) 8,627 90 7,764
Chicken, potted (cooked in liquid) with onion and water 3,329 90 2,996
Chicken, roastedc 6,020 90 5,418
Chicken, selects (McDonald's) 9,257 90 8,331
Chicken, skin, back or thigh, roasted then BBQb 18,520 90 16,668
Chicken, skin, leg, roastedb 10,997 90 9,897
Chicken, skin, thigh, roastedb 11,149 90 10,034
Chicken, thigh, roastedb 5,146 90 4,631
Turkey, burger, pan fried with cooking spray, 5 min, high heatc 7,968 90 7,171
Turkey, burger, pan fried with cooking spray, 5 min, high heat, microwaved 13.5 sec, high heatc 8,938 90 8,044
Turkey, burger, pan fried with 5 mL canola oil, 3.5 min, high heatc 8,251 90 7,426
Turkey, ground, grilled, crust 6,351 90 5,716
Turkey, ground, grilled, interior 5,977 90 5,379
Turkey, ground, raw 4,957 90 4,461
Turkey, burger, broiled 5,366 90 4,829
Turkey, breast, roasted 4,669 90 4,202
Turkey, breast, smoked, searedc 6,013 90 5,412
Turkey, breast, steak, skinless, marinated w/orange juice, broiledc 4,388 90 3,949
Pork
Bacon, fried 5 min no added oil 91,577 13 11,905
Bacon, microwaved, 2 slices, 3 min 9,023 13 1,173
Ham, deli, smoked 2,349 90 2,114
Liverwurst (Boar's Head) 633 90 570
Pork, chop, marinated w/balsamic vinegar, BBQb 3,334 90 3,001
Pork, chop, raw, marinated w/balsamic vinegarb 1,188 90 1,069
Pork, chop, pan fried, 7 min 4,752 90 4,277
Pork, ribs, roasted, Chinese take out 4,430 90 3,987
Pork, roast, Chinese take out 3,544 90 3,190
Sausage, beef and pork links, pan fried 5,426 90 4,883
Sausage, Italian, rawb 1,861 90 1,675
Sausage, Italian, BBQb 4,839 90 4,355
Sausage, pork links, microwaved, 1 min 5,943 90 5,349
Lamb
Lamb, leg, boiled, 30 min 1,218 90 1,096
Lamb, leg, broiled, 450°F, 30 min 2,431 90 2,188
Lamb, leg, microwave, 5 min 1,029 90 926
Lamb, leg, raw 826 90 743
Veal
Veal, stewed 2,858 90 2,572
Fish/seafood
Crabmeat, fried, breaded (take out) 3,364 90 3,028
Fish, loaf (gefilte), boiled 90 min 761 90 685
Salmon, Atlantic, farmed, prev. frozen, microwaved, 1 min, high heatc 954 90 859
Salmon, Atlantic, farmed, prev. frozen, poached, 7 min, medium heatc 1,801 90 1,621
Salmon, Atlantic, farmed, prev. frozen, steamed, 10 min, medium heatc 1,212 90 1,091
Salmon, Atlantic, farmed, prev. frozen, steamed in foil, 8 min, medium heatc 1,000 90 900
Salmon, breaded, broiled 10 min 1,498 90 1,348
Salmon, broiled with olive oil 4,334 90 3,901
Salmon, canned pink (Rubenstein, Trident Seafoods, Seattle, WA) 917 90 825
Salmon, fillet, boiled, submerged, 18 min 1,082 90 974
Salmon, fillet, broiled 3,347 90 3,012
Salmon, fillet, microwaved 912 90 821
Salmon, fillet, poached 2,292 90 2,063
Salmon, pan fried in olive oil 3,083 90 2,775
Salmon, raw, previously frozen 517 90 465
Salmon, raw 528 90 475
Salmon, smoked 572 90 515
Scrod, broiled 450°F, 30 min 471 90 424
Shrimp frozen dinner, microwaved 4.5 min 4,399 90 3,959
Shrimp, fried, breaded (take out) 4,328 90 3,895
Shrimp, marinated rawb 1,003 90 903
Shrimp, marinated, grilled on BBQb 2,089 90 1,880
Trout, baked, 25 min 2,138 90 1,924
Trout, raw 783 90 705
Tuna, patty, chunk light, broiled, 450°F, 30 min 747 90 672
Tuna, broiled, with soy, 10 min 5,113 90 4,602
Tuna, broiled, with vinegar dressing 5,150 90 4,635
Tuna, fresh, baked, 25 min 919 90 827
Tuna, loaf (chunk light in recipe), baked 40 min 590 90 531
Tuna, canned, chunk light, w/water 452 90 407
Tuna, canned, white, albacore, w/oil 1,740 90 1,566
Whiting, breaded, oven fried, 25 minc 8,774 90 7,897
Cheese
Cheese, American, low fat (Kraft) 4,040 30 1,212
Cheese, American, white, processed 8,677 30 2,603
Cheese, brie 5,597 30 1,679
Cheese, cheddar 5,523 30 1,657
Cheese, cheddar, extra sharp, made with 2% milk (Cracker Barrel, Kraft) 2,457 30 737
Cheese, cottage, 1% fat (Light & Lively, Kraft) 1,453 30 436
Cheese, feta, Greek, soft 8,423 30 2,527
Cheese, mozzarella, reduced fat 1,677 30 503
Cheese, parmesan, grated (Kraft) 16,900 15 2,535
Cheese, Swiss, processedb 4,470 30 1,341
Cheese, Swiss, reduced fat (Alpine Lace, Alpine Lace Brands, Inc, Maplewood, NJ) 4,743 30 1,423
Soy
Bacon bits, imitation, Bacos (Betty Crocker, General Mills, Minneapolis, MN) 1,247 15 187
Meatless jerky, Primal Strips (Primal Spirit Inc, Moundsville, WV) 1,398 90 1,258
Soy burger, Boca Burger, 400°F, 8 min-4 each sidec (BOCA Foods Co, Mandison, WI) 130 30 39
Soy burger, Boca Burger, microwaved, 1.5 minc (BOCA Foods Co) 67 30 20
Soy burger, Boca Burger, skillet, cook spray, 5 minc (BOCA Foods Co) 100 30 30
Soy burger, Boca Burger, skillet, w/1 tsp olive oil, 5 minc (BOCA Foods Co) 437 30 131
Soy burger, Boca Burger (BOCA Foods Co) (mean) 183 30 55
Tofu, broiled 4,107 90 3,696
Tofu, raw 788 90 709
Tofu, soft, raw 488 90 439
Tofu, sautéed, inside 3,569 90 3,212
Tofu, sautéed, outside 5,877 90 5,289
Tofu, sautéed (mean) 4,723 90 4,251
Tofu, soft, boiled 5 min, +2 min to return to boilc 628 90 565
Tofu, soft, boiled 5 min, +2 min,+ soy sauce, sesame oilc 796 90 716
Eggs
Egg, fried, one large 2,749 45 1,237
Egg white powder (Deb-El Products, Elizabeth, NJ) 1,040 10 104
Egg white, large, 10 min 43 30 13
Egg white, large, 12 min 63 30 19
Egg yolk, large, 10 min 1,193 15 179
Egg yolk, large, 12 min 1,680 15 252
Egg, omelet, pan, low heat, cooking spray, 11 minc 90 30 27
Egg, omelet, pan, low heat, corn oil, 12 minc 223 30 67
Egg, omelet, pan, low heat, margarine, 8 minc 163 30 49
Egg, omelet, pan, low, butter, 13 minc 507 30 152
Egg, omelet, pan, low, olive oil, 12 minc 337 30 101
Egg, poached, below simmer, 5 minc 90 30 27
Egg, scrambled, pan, high, butter, 45 secc 337 30 101
Egg, scrambled, pan, high, cooking spray, 1 minc 117 30 35
Egg, scrambled, pan, high, corn oil, 1 minc 173 30 52
Egg, scrambled, pan, high, margarine, 1 minc 123 30 37
Egg, scrambled, pan, high, olive oil, 1minc 243 30 73
Egg, scrambled, pan, med-low, butter, 2 minc 167 30 50
Egg, scrambled, pan, med-low, cooking spray, 2 minc 67 30 20
Egg, scrambled, pan, med-low, corn oil, 1.5 minc 123 30 37
Egg, scrambled pan, med-low, margarine, 2 minc 63 30 19
Egg, scrambled, pan, med-low, olive oil, 2 minc 97 30 29
AGE Content
Carbohydrates AGE kU/100 g Serving size (g) AGE kU/serving
Bread
Bagel, small, Lender'sb 133 30 40
Bagel, largeb 107 30 32
Bagel, toastedb 167 30 50
Biscuit (Mc Donald'sd) 1,470 30 441
Biscuit, refrigerator, baked-oven, 350°F, 17 min (Pillsbury Grands, General Mills) 1,343 30 403
Biscuit, refrigerator, uncooked (Pillsbury Grands, General Mills) 823 30 247
Bread, 100% whole wheat, center, toasted (Wonder, Interstate Bakeries, Inc, Irving, TX) 83 30 25
Bread, 100% whole wheat, center (Wonder) 53 30 16
Bread, 100% whole wheat, top crust (Wonder) 73 30 22
Bread, 100% whole wheat, top crust, toasted (Wonder) 120 30 36
Bread, Greek, hard 150 30 45
Bread, Greek, hard, toasted 607 30 182
Bread, Greek, soft 110 30 33
Bread, pita 53 30 16
Bread, white, Italian, center (Freihoffer's, Bimbo Bakeries, Horsham, PA) 23 30 7
Bread, white, Italian, center, toasted (Freihoffer's) 83 30 25
Bread, white, Italian, crust (Freihoffer's) 37 30 11
Bread, white, Italian, top crust, toasted (Freihoffer's) 120 30 36
Bread, white, slice (Rockland Bakery, Nanuet, NY) 83 30 25
Bread, white, slice, toasted (Rockland Bakery) 107 30 32
Bread, whole wheat, slice (Rockland Bakery) 103 30 31
Bread, whole wheat, slice, toasted, slice, (Rockland Bakery) 137 30 41
Croissant, butter (Starbucks, Seattle, WA) 1,113 30 334
Roll, dinner, inside 23 30 7
Roll, dinner, outside 77 30 23
Breakfast cereals
Bran flakes, from raisin bran (Post, Kellogg Co, Battle Creak, MI) 33 30 10
Cinnamon Toast Crunch (General Mills) 1,100 30 330
Corn Flakes (Kellogg's) 233 30 70
Corn Flakes, Honey Nut (Kellogg Co) 320 30 96
Corn Flakes, Sugar Frosted (Kellogg Co) 427 30 128
Corn Pops (Kellogg's) 1,243 30 373
Cream of Wheat, instant, prepared (Nabisco, East Hanover, NJ) 108 175 189
Cream of Wheat, instant, prepared with honey (Nabisco) 189 175 331
Fiber One (General Mills) 1,403 30 421
Froot Loops (Kellogg Co) 67 30 20
Frosted Mini Wheats (Kellogg Co) 210 30 63
Granola, Organic Oats & Honey (Cascadian Farms, Small Planet Foods, Minneapolis, MN) 427 30 128
Life, mean (Quaker Oats, Chicago, IL) 1,313 30 394
Puffed Corn Cereal (Arrowhead Mills, The Hain Celestial Group, Inc) 100 30 30
Puffed Wheat 17 30 5
Rice Krispies (Kellogg Co) 2,000 30 600
Total, Wheat and Brown Rice (General Mills) 233 30 70
Oatmeal, instant, dry (Quaker Oats) 13 30 4
Oatmeal, instant, prepared (Quaker Oats) 14 175 25
Oatmeal, instant, prepared with honey (Quaker Oats) 18 175 31
Breakfast foods
French toast, Aunt Jemima, frozen, microwaved 1 min (Pinnacle Foods) 603 30 181
French toast, Aunt Jemima, frozen,10 min @ 400°F (Pinnacle Foods Corp) 850 30 255
French toast, Aunt Jemima, frozen, not heated (Pinnacle Foods Corp, Cherry Hill, NJ) 263 30 79
French toast, Aunt Jemima frozen, toaster medium-1 cycle (Pinnacle Foods) 613 30 184
Hot Cakes (McDonald'sd) 243 30 73
Pancake, from mix 823 30 247
Pancake, frozen, toasted (General Mills) 2,263 30 679
Pancake, homemade 973 30 292
Waffle, frozen, toasted (Kellogg Co) 2,870 30 861
Grains/legumes
Beans, red kidney, raw 116 100 116
Beans, red kidney, canned 191 100 191
Beans, red kidney, cooked 1 h 298 100 298
Pasta, cooked 8 min 112 100 112
Pasta, cooked 12 min 242 100 242
Pasta, spiralb 245 100 245
Rice, white, quick cooking, 10 min 9 100 9
Rice, Uncle Ben's white, cooked, 35 min (Mars, Inc, Houston, TX) 9 100 9
Rice, white, pan toasted 10 min, cooked 30 min 32 100 32
Starchy vegetables
Corn, canned 20 100 20
Potato, sweet, roasted 1 h 72 100 72
Potato, white, boiled 25 min 17 100 17
Potato, white, roasted 45 min, with 5 mL oil/servingc 218 100 218
Potato, white, french fries (McDonald'sd) 1,522 100 1,522
Potato, white, french fries, homemade 694 100 694
Potato, white, french fries, in corn oil, held under heat lampb 843 100 843
Potato, white, hash browns (McDonald'sd) 129 100 129
Crackers/snacks
Breadsticks, Stella D'oro hard (Brynwood Partners, Greenwich, CT) 127 30 38
Cheez Doodles, crunchy (Wise Foods Inc, Berwick, PA) 3,217 30 965
Chex mix, traditonal (General Mills, Inc) 1,173 30 352
Chips, corn, Doritos (Frito Lay) 503 30 151
Chips, corn, Harvest Cheddar Sun Chips (Frito-Lay) 1,270 30 381
Chips, Platanitos, plantain (Plantain Products Co, Tampa, FL) 370 30 111
Chips, potato (Frito Lay) 2,883 30 865
Chips, potato, baked original potato crisps (Frito Lay) 450 30 135
Combos, nacho cheese pretzel (M & M Mars, McLean, VA) 1,680 30 504
Cracker, chocolate Teddy graham (Nabisco) 1,647 30 494
Cracker, Pepperidge Farms Goldfish, cheddar (Campbell Soup Co, Camden, NJ) 2,177 30 653
Cracker, Keebler honey graham (Kellogg Co) 1,220 30 366
Cracker, Old London melba toast (Nonni's Food Co, Tulsa, OK) 903 30 271
Cracker, oyster 1,710 30 513
Cracker, rice cake, corn (Taanug) 137 30 41
Cracker, saltine, hospital (Alliant) 937 30 281
Cracker, Keebler sandwich, club+cheddar, (Kellogg Co) 1,830 30 549
Cracker, toasted wheat 917 30 275
Cracker, wheat, round 857 30 257
Cracker, KA-ME rice crunch, plain (Liberty Richter, Bloomfield, NJ) 917 30 275
Popcorn, air popped, with butter 133 30 40
Popcorn, Pop Secret microwaved, fat free, no added fat (General Mills) 33 30 10
Pretzel, minis (Snyder's of Hanover, Hanover, NJ) 1,790 30 537
Pretzel, Q rolled 1,883 30 565
Pretzel, stick 1,600 30 480
Pretzel (mean) 1,757 30 527
Veggie Booty (Robert's American Gourmet, Seacliff, NY) 983 30 295
Cookies, cakes, pies, pastries
Bar, granola, chocolate chunk, soft (Quaker) 507 30 152
Bar, Nutrigrain, apple cinnamon (Kellogg's) 2,143 30 643
Bar, Rice Krispies Treat (Kelloggs) 1,920 30 576
Bar,Granola, peanut butter & choc chunk, hard (Quaker) 3,177 30 953
Cake, angel food, Danish Kitchen (Sam's Club, Bentonville, AR) 27 30 8
Cookie, biscotti, vanilla almond (Starbucks) 3,220 30 966
Cookie, chocolate chip, Chips Ahoy (Nabisco) 1,683 30 505
Cookie, Golden Bowl fortune (Wonton Food, Inc, Brooklyn, NY) 90 30 27
Cookie, Greek wedding, nut cookie 960 30 288
Cookie, meringue, homemade 797 30 239
Cookie, Keebler oatmeal raisin (Kellogg Co) 1,370 30 411
Cookie, Oreo (Nabisco) 1,770 30 531
Cookie, Nilla vanilla wafer (Nabisco) 493 30 148
Croissant, chocolate (Au Bon Pain, Boston, MA) 493 30 148
Danish, cheese (Au Bon Pain) 857 30 257
Donut, glazed devil's food cake (Krispy Kreme, Winston-Salem, NC) 1,407 30 422
Donut, chocolate iced, crème filled (Krispy Kreme) 1,803 30 541
Fruit pop, frozen (Dole, Westlake Village, CA) 18 60 11
Fruit roll up, sizzlin' red (General Mills) 980 30 294
Gelatin, Dole strawberry (Nestle, Minneapolis, MN) 2 125 2
Gelatin, Dole strawberry, sugar free (Nestle) 1 125 1
Ice cream cone, cake (Haagen Dazs, Oakland, CA) 147 30 44
Ice cream cone, sugar (Haagen Dazs) 153 30 46
Muffin, bran (Au Bon Pain) 340 30 102
Pie, apple, individual, baked (McDonald'sd) 637 30 191
Pie, crust, frozen, baked per pkg, mean Mrs. Smith's Dutch Apple Crumb and Pumpkin Custard (Kellogg Co) 1,390 30 417
Pie, Mrs. Smith's Dutch apple crumb, deep dish, apple filling (Kellogg Co) 340 30 102
Pie, Mrs. Smith's Dutch apple crumb, deep dish, crumbs (Kellogg Co) 1,030 30 309
Pie, Mrs. Smith's Dutch apple crumb, deep dish, crust (Kellogg Co) 1,410 30 423
Pie, Mrs. Smith's Dutch apple crumb, deep dish, pie (Kellogg Co) 893 30 268
Pie, Mrs. Smith's pumpkin custard, bake it fresh, original recipe, crust (Kellogg Co) 1,373 30 412
Pie, Mrs. Smith's pumpkin custard, bake it fresh, original recipe, custard (Kellogg Co) 617 30 185
Pie, Mrs. Smith's pumpkin custard, bake it fresh, original recipe, pie (Kellogg Co) 880 30 264
Pop tart, microwave-3 sec high power (Kellogg Co) 243 30 73
Pop tart, microwave-6 se medium high power (Kellogg's) 210 30 63
Pop tart, not heated (Kellogg Co) 133 30 40
Pop tart, toaster-low, 1 cycle (Kellogg Co) 260 30 78
Scone, cinnamon (Starbucks) 790 30 237
Sorbet, Edy's strawberry (Dryer's, Oakland, CA) 2 125 3
Sweet roll, cinnamon swirl roll (Starbucks) 907 30 272
Fruits
Apple, baked 45 100 45
Apple, Macintosh 13 100 13
Banana 9 100 9
Cantaloupe 20 100 20
Coconut cream, Coco Goya cream of coconut (Goya, Secaucus, NJ) 933 15 140
Coconut milk, leche de coco, (Goya) 307 15 46
Coconut, Baker's Angel Flake, sweetened (Kraft) 590 30 177
Dates, Sun-Maid California chopped (Sun-Maid, Kingsburg, CA) 60 30 18
Fig, dried 2,663 30 799
Plums, Sun-Maid dried pitted prunes (Sun-Maid) 167 30 50
Raisin, from Post Raisin Bran (Kellogg Co) 120 30 36
Vegetables (raw unless specified otherwise)
Carrots, canned 10 100 10
Celery 43 100 43
Cucumber 31 100 31
Eggplant, grilled, marinated with balsamic vinegarb 256 100 256
Eggplant, raw, marinated with balsamic vinegarb 116 100 116
Green beans, canned 18 100 18
Portabella mushroom, raw, marinated with balsamic vinegarb 129 100 129
Onion 36 100 36
Tomato 23 100 23
Tomato sauce (Del Monte Foods, San Francisco, CA) 11 100 11
Vegetables, grilled (broccoli, carrots, celery) 226 100 226
Vegetables, grilled (pepper, mushrooms) 261 100 261
Other carbohydrates
Sugar, white 0 5 0
Sugar substitute, aspartame as Canderel (Merisant, Chicago, IL) 0 5 0
AGE Content
Liquids AGE kU/100 mL Serving size (mL) AGE kU/serving
Milk and milk products
Cocoa packet, Swiss Miss, prepared (ConAgra Foods) 262 250 656
Cocoa packet, Swiss Miss sugar-free, prepared (ConAgra Foods) 204 250 511
Ice cream, America's Choice vanilla (The Great Atlantic and Pacific Tea Co, Montvale, NJ) 34 250 84
Milk, fat-free (hospital) 1 250 2
Milk, Lactaid fat free (McNeil Nutritionals, Fort Washington, PA) 10 250 26
Milk, fat free (Tuscan Dairy Farms, Burlington, NJ) 2 250 4
Milk, fat free, with A and D 0 250 1
Milk, fat free, with A and D (microwaved,1 min) 2 250 5
Milk, fat free, with A and D (microwaved, 2 min) 8 250 19
Milk, fat free, with A and D (microwaved, 3 min) 34 250 86
Milk, soy (Imagine Foods, The Hain Celestial Group) 31 250 77
Milk, whole (4% fat) 5 250 12
Pudding, instant chocolate, fat-free, sugar-free, prepared 1 120 1
Pudding, instant chocolate, skim milk 1 120 1
Pudding, Hunt Wesson snack pack, chocolate (ConAgra Foods) 17 120 20
Pudding, Hunt Wesson snack pack, vanilla (ConAgra Foods) 13 120 16
Yogurt, cherry, (Dannon, White Plains, NY) 4 250 10
Yogurt, vanilla, (Dannon) 3 250 8
Fruit juice
Juice, apple 2 250 5
Juice, cranberry 3 250 8
Juice, orange 6 250 14
Juice, orange, from fresh fruit 0 250 1
Juice, orange, with calcium 3 250 8
Vegetable juice
Vegetable juice, V8 (Campbell Soup Co) 2 250 5
Other carbohydrate liquids
Fruit pop, frozen (Dole) 18 60 11
Honey 7 15 1
Sorbet, strawberry (Edy's) 2 125 3
Syrup, caramel, sugar free 0 15 0
Syrup, dark corn 0 15 0
Syrup, pancake, lite 0 15 0
AGE Content
Combination foods and solid condiments AGE kU/100 g Serving size (g) AGE kU/serving
Combination foods
Bacon Egg Cheese Biscuit (McDonald'sd) 2,289 100 2,289
Bacon, Egg and Cheese McGriddles (McDonald'sd) 858 100 858
Big Mac (McDonald'sd) 7,801 100 7,801
Casserole, tuna 233 100 233
Cheeseburger (McDonald'sd) 3,402 100 3,402
Chicken McGrill (McDonald'sd) 5,171 100 5,171
Corned beef hash, canned, microwaved 2 min, high power (Broadcast) 1,691 100 1,691
Corned beef hash, canned, stove top, medium heat, 12 min (Broadcast) 2,175 100 2,175
Corned beef hash, canned, unheated (Broadcast) 1,063 100 1,063
Double Quarter Pounder With Cheese (McDonald'sd) 6,283 100 6,283
Filet-O-Fish (McDonald'sd) 6,027 100 6,027
Gnocchi, potato/flour/Parmesan cheese, 3 min 535 100 535
Gnocchi, potato/flour/Parmesan cheese, 4.5 min 2,074 100 2,074
Hot Pocket, bacon, egg, cheese, oven, 350°F, 20 min (Nestle) 1,695 100 1,695
Hot Pocket-bacon, egg, cheese, microwaved 1 min (Nestle) 846 100 846
Hot Pocket-bacon, egg, cheese, frozen-not heated (Nestle) 558 100 558
Hummus, commercial 733 100 733
Hummus, with garlic and scallions 884 100 884
Hummus, with vegetables 487 100 487
Hummus (mean) 701 100 701
Macaroni and cheeseb 2,728 100 2,728
Macaroni and cheese, bakedc 4,070 100 4,070
Pasta primavera 959 100 959
Pesto, with basil (Buitoni, Nestle) 150 100 150
Pizza, thin crust 6,825 100 6,825
Salad, Italian pastac 935 100 935
Salad, lentil potatoc 123 100 123
Salad, tuna pastac 218 100 218
Sandwich, cheese melt, open facedc 5,679 100 5,679
Sandwich, toasted cheese 4,333 100 4,333
Soufflé, spinachc 598 100 598
Timbale, broccolic 122 100 122
Taramosalata (Greek style caviar spread) 678 100 678
Veggie burger, California burger, 400°F, 8 min-4 each side (Amy's Kitchen, Petaluma, CA) 198 100 198
Veggie burger, California burger, skillet, with spray, 5 min (Amy's) 149 100 149
Veggie burger, California burger, skillet, with 1 tsp olive oil, 5 min (Amy's) 374 100 374
Veggie burger, California burger, microwave, 1 min (Amy's) 68 100 68
Won ton, pork, fried (take out) 2,109 100 2,109
Ziti, baked 2,795 100 2,795
Condiments
Ginger, crystallized 490 10 49
Candy, Hershey Special Dark Chocolate (The Hershey Co, Hershey, PA) 1,777 30 533
Candy, M & M's, milk chocolate (Mars) 1,500 30 450
Candy, Reese's Peanut Butter Cup (The Hershey Co) 3,440 30 1,032
Candy, Raisinets (Nestle) 197 30 59
Candy, Snickers (Nestle) 263 30 79
Pickle, bread and butter 10 30 3
AGE Content
Soups, liquid condiments, and miscellaneous liquids AGE kU/100 mL Serving size (mL) AGE kU/serving
Soups
Soup, beef bouillon 0.40 250 1
Soup, chicken bouillon 1.20 250 3
Soup, College Inn chicken broth, (Del Monte) 0.80 250 2
Soup, chicken noodle, (Campbell Soup Company) 1.60 250 4
Soup, couscous and lentil (Fantastic World Foods, Edison, NJ) 3.60 250 9
Soup, Knorr vegetable broth, (Unilever) 1.60 250 4
Soup, summer vegetablec 1.20 250 3
Condiments
Ketchup 13.33 15 2
Mustard 0.00 15 0
Pectin 80.00 15 12
Soy sauce 60.00 15 9
Vinegar, balsamic 33.33 15 5
Vinegar, white 40.00 15 6
Miscellaneous
SoBe Adrenaline Rush (South Beach Beverage Co, Norwalk, CT) 0.40 250 1
Budwiser Beer (Anheuser-Busch, St Louis, MO) 1.20 250 3
Breast milk, fresh 6.67 30 2
Breast milk, frozen 10.00 30 3
Coca Cola, classic (The Coca-Cola Co, Atlanta, GA) 2.80 250 7
Coffee, with milk and sugar 2.40 250 6
Coffee, drip method 1.60 250 4
Coffee, heating plate >1 h 13.60 250 34
Coffee, Taster's Choice instant (Nestle) 4.80 250 12
Coffee, instant, decaf (mean Sanka [Kraft] and Taster's Choice) 5.20 250 13
Coffee, Spanish 4.80 250 12
Coffee, with milk 6.80 250 17
Coffee, with sugar 7.60 250 19
Coke 6.40 250 16
Coke, Diet (The Coca-Cola Company) 1.20 250 3
Coke, Diet 2008 (The Coca-Cola Company) 4.00 250 10
Coke, Diet plus (The Coca-Cola Company) 1.60 250 4
Enfamil, old (Mead Johnson Nutritonal, Glenview, IL) 486.67 30 146
Ensure plus 12.80 250 32
Gelatin, Dole strawberry (Nestle) 1.60 125 2
Gelatin, Dole strawberry, sugar free (Nestle) 0.80 125 1
Glucerna (Abbott Nutrition, Columbus, OH) 70.00 250 175
Malta (Goya) 1.20 250 3
NOFEAR Super Energy Supplement (Pepsico, Purchase, NY) 0.40 250 1
Pepsi, diet (Pepsico) 2.80 250 7
Pepsi, diet MAX (Pepsico) 3.20 250 8
Pepsi, diet, caffeine free (Pepsico) 2.40 250 6
Pepsi, regular (Pepsico) 2.40 250 6
Resource (Nestle) 72.00 250 180
Rum, Bacardi Superior, 80 proof (Miami, FL) 0.00 250 0
Sprite (The Coca-Cola Company) 1.60 250 4
Sprite, diet (The Coca-Cola Company) 0.40 250 1
Tea, apple (RC Bigelow, Inc, Fairfield, CT) 0.40 250 1
Tea, Lipton Tea bag (Unilever) 2.00 250 5
Tea, Lipton Tea bag, decaf (Unilever) 1.20 250 3
Vodka, Smirnoff, 80 proof (Diageo, London, UK) 0.00 250 0
Whiskey, Dewar's White Label (Dewar's, Perthsire, UK) 0.40 250 1
Wine, pinot grigio (Cavit Collection, Port Washington, NY) 32.80 250 82
Wine, pinot noir (Cavit Collection) 11.20 250 28

Preparation of food samples for AGE measurement was performed as previously described (13). Briefly, food samples were homogenized and dissolved in phosphate buffer saline and the supernatants tested for AGEs with enzyme-linked immunosorbent assay based on a monoclonal anti-CML antibody (4G9) (29,30). The AGE content of each food item was based on the mean value of at least three measurements per sample and expressed as AGE kilounits/100 g food.

Selected items from different food categories were tested by a second enzyme-linked immunosorbent assay for content of MG-derivatives using an anti-MG monoclonal antibody (3D11 mAb) (29) and the results were expressed as nmol/100 g or nmol/100 mL food. The test sensitivity for CML and MG was 0.1 U/mL and 0.004 nmol/mL, respectively; the intra-assay variation was ±2.6% (CML) and ±2.8% (MG) and the inter-assay variation was ±4.1% (CML) and ±5.2% (MG).

AGE Inhibitory Agents

Because a low or acidic pH arrests AGE development, new AGE formation in cooked meat was tested following exposure to acidic solutions (marinades) of lemon juice and vinegar. Samples from lean beef were marinated in acidic solutions of either lemon or vinegar for 1 hour before cooking (see the Figure). In addition, the effect of a prototypic AGE inhibitor (aminoguanidine, 200 μmol/L) was compared to that of a lipid antioxidant (butylated hydroxytoluene [BHT], 100 μmol/L) on new AGE formation during heating by assessing CML content in oil (extra virgin olive oil, Colavita, Linden, NJ) samples, heated at 100°C for 5 minutes.

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Effect of acidic environment on the advanced glycation end product (AGE) content of beef. Beef (25 g) was roasted for 15 minutes at 150°C with or without premarinating in 10 mL vinegar (A) or lemon juice (B) for 1 hour. Samples were homogenized and AGE (N ε -carboxy-methyl-lysine) content was assessed by enzyme-linked immunosorbent assay as described in the Methods section. Data are shown as % change from raw state. White bars represent raw state, hatched bars roasted without marinating and black bars marinated samples. *Significant changes compared to the raw state (P<0.05). #Significant changes compared to cooked without marinating samples. 1=raw beef. 2=roasted beef with no vinegar or lemon. 3=roasted beef after marinating with either vinegar or lemon for 1 hour.

Statistical Analysis

Data in the Table 1 (available online at www.adajournal.org), Table 2, and the Figure are presented as mean±standard error of the mean. Differences of mean values between groups were tested by unpaired Student t test or analysis of variance (followed by Bonferroni correction for multiple comparisons), depending on the number of groups. For nonparametric values, the Mann-Whitney U unpaired test or the Kruskal-Wallis analysis of ranks was used, depending on the number of groups. Correlation analyses were evaluated by Pearson's correlation coefficient. Significant differences were defined as a P value <0.05 and are based on two-sided tests. Data were analyzed using the SPSS statistical program (version 15.0 for Windows, 2005, SPSS Inc, Chicago, IL). For data presentation, food groups were based on the American Diabetes Association and the American Dietetic Association exchange lists for diabetes (31).

Table 2

Database of combined methylyglyoxal (MG) and carboxymetyllysine (CML) content of selected foods

Advanced Glycation End Product Content
Food item Total MG nmol/100 g Total CML kU/100 g
Solid foods (per 100 g food)
Bread, white 3,630 8.3
Bread, wheat 4,840 105
Cereal, Life (Quaker Oats, Chicago, IL) 9,000 1,452
Cheese, American 16,790 8,677
Cheese, Brie 5,670 5,598
Chicken, grilled 14,440 4,848
Chicken, microwaved (5 min) 8,350 1,524
Chicken, raw 4,170 769
Crackers, Pepperidge Farms Goldfish (Campbell Soup Co, Camden, NJ) 4,170 2,176
Egg, fried 13,670 2,749
French fries 13,130 843
Margarine, Smart Balance (CFA Brands, Heart Beat Foods, Paramus, NJ) 10,790 6,229
Salmon, broiled with olive oil 14,950 4,334
Salmon, broiled, plain 9,350 3,347
Salmon, pan fried in olive oil 9,090 3,083
Salmon, raw 6,820 527
Salmon, raw, previously frozen 6,190 517
Steak, broiled, plain 17,670 7,478
Steak, pan fried in olive oil 18,150 10,058
Steak, raw 5,860 800
Tuna, solid white packed in water 4,060 452
Total MG nmol/100 mL Total CML kU/100 mL

Liquids (per 100 mL food)
Ice cream, vanilla 620 352
Milk, whole 620 4.9
Olive oil, fresh (Colavita, Linden, NJ) 7,700 5,852
Olive oil, heated at 100°C for 5 min (Colavita, Linden, NJ) 9,700 6,295
Olive oil, heated at 100°C for 5 min + butylated hydroxytoluene (Colavita, Linden, NJ) 8,200 6,682
Olive oil, heated at 100°C for 5 min + aminoguanidine (Colavita, Linden, NJ) 7,900 5,763
Pudding, chocolate 160 16
Pudding, vanilla 110 13
Yogurt, Dannon (White Plains, NY) 830 3
Coke, diet (Coca-Cola Co, Atlanta, GA) 334 4
Coke, Diet Plus (Coca-Cola Co, Atlanta, GA) 422 2
Coca Cola Classic (Coca-Cola Co, Atlanta, GA) 13 3
Pepsi, diet (PepsiCo, Purchase, NY) 33 3
Pepsi, regular (PepsiCo, Purchase, NY) 325 2
Pepsi, diet, caffeine free (PepsiCo, Purchase, NY) 201 2.6
Pepsi Max, diet (PepsiCo, Purchase, NY) 202 3.3
SoBe Adrenaline Rush (South Beach Beverage Co, Norwalk, CT) 821 0.4
SoBe NO FEAR Super Energy (South Beach Beverage Co, Norwalk, CT) 339 0.06

RESULTS AND DISCUSSION

AGE Content of Foods as Determined by CML Levels

The AGE content in 549 foods, based on CML, is presented in Table 1 (available online at www.adajournal.org).

The new database contains more than twice the number of food items than the previously reported database (13) and shows that, based on standard serving sizes, the meat group contained the highest levels of AGEs. Although fats tend to contain more dAGE per gram of weight, meats will likely contribute more to overall dAGE intake because meats are served in larger portions than are fats. When items in the meat category prepared by similar methods were compared, the highest dAGE levels were observed in beef and cheeses followed by poultry, pork, fish, and eggs. Lamb ranked relatively low in dAGEs compared to other meats (Table 1 available online at www.adajournal.org). It is noteworthy that even lean red meats and poultry contain high levels of dAGEs when cooked under dry heat. This is attributable to the fact that among the intracellular components of lean muscle there exist highly reactive amino-lipids, as well as reducing sugars, such as fructose or glucose-6-phosphate, the combination of which in the presence of heat rapidly accelerates new dAGE formation (30,32).

Higher-fat and aged cheeses, such as full-fat American and Parmesan, contained more dAGEs than lower-fat cheeses, such as reduced-fat mozzarella, 2% milk cheddar, and cottage cheese. Whereas cooking is known to drive the generation of new AGEs in foods, it is interesting to note that even uncooked, animal-derived foods such as cheeses can contain large amounts of dAGEs. This is likely due to pasteurization and/or holding times at ambient room temperatures (eg, as in curing or aging processes) (33). Glycation-oxidation reactions, although at a slower rate, continue to occur over time even at cool temperatures, resulting in large accumulation of dAGEs in the long term.

High-fat spreads, including butter, cream cheese, margarine, and mayonnaise, were also among the foods highest in dAGEs, followed by oils and nuts. As with certain cheeses, butter and different types of oils are AGE-rich, even in their uncooked forms. This may be due to various extraction and purification procedures involving heat, in combination with air and dry conditions, however mild they are.

Of note, with heat kept constant, the type of cooking fat used led to different amounts of dAGEs. For instance, scrambled eggs prepared with a cooking spray, margarine, or oil had ~50% to 75% less dAGEs than if cooked with butter (Table 1 available online at www.adajournal.org).

In comparison to the meat and fat groups, the carbohydrate group generally contained lower amounts of AGEs (Table 1 available online at www.adajournal.org). This may be due to the often higher water content or higher level of antioxidants and vitamins in these foods, which may diminish new AGE formation. Furthermore, in this food category, most polysaccharides consist of non-reducing sugars, less likely to give rise to AGEs. The highest dAGE level per gram of food in this category was found in dry-heat processed foods such as crackers, chips, and cookies. This is likely due to the addition of ingredients such as butter, oil, cheese, eggs, and nuts, which during dry-heat processing substantially accelerate dAGE generation. Although AGEs in these snack types of food remain far below those present in meats, they may represent an important health hazard for people who consume multiple snacks during the day or as fast meals (34).

Grains, legumes, breads, vegetables, fruits, and milk were among the lowest items in dAGE, unless prepared with added fats. For instance, biscuits had more than 10 times the amount of dAGEs found in low-fat breads, rolls, or bagels.

Nonfat milk had significantly lower dAGEs than whole milk. Whereas heating increased the dAGE content of milk, the values were modest and remained low relative to those of cheeses (Table 1 available online at www.adajournal.org). Likewise, milk-related products with a high moisture index such as yogurt, pudding, and ice cream were also relatively low in AGEs. However, hot cocoa made from a dehydrated concentrate contained significantly higher amounts of AGEs.

AGE Content of Foods as Determined by MG Levels

Selected common foods were simultaneously analyzed for MG derivatives to determine whether food AGEs other than CML followed the same pattern (Table 2). A highly significant linear correlation (r=0.8, P=0.0001) was observed between the CML and MG content of foods prepared by different cooking techniques. As with CML, foods high in protein and fat contained higher amounts of MG than did carbohydrate-rich foods. Noncooked butter and oil contained low amounts of MG, but in dry-heated fat, as in french fries, MG content was significantly higher (Table 2). The highly significant internal correlation between two chemically distinct AGEs (CML and MG) in a variety of foods prepared by different methods validates the methodology applied and supports the choice of CML levels as a useful marker of dAGE content.

Effect of Cooking Procedures on AGE Formation in Foods

Preparation of common foods under varying conditions of water and heat had a different effect on dAGE content. For example, scrambled eggs prepared in an open pan over medium-low heat had about one half the dAGEs of eggs prepared in the same way but over high heat. Poached or steamed chicken had less than one fourth the dAGEs of roasted or broiled chicken. In all food categories, exposure to higher temperatures and lower moisture levels coincided with higher dAGE levels for equal weight of food as compared to foods prepared at lower temperatures or with more moisture. Thus, frying, broiling, grilling, and roasting yielded more dAGEs compared to boiling, poaching, stewing, and steaming. Microwaving did not raise dAGE content to the same extent as other dry heat cooking methods for the relatively short cooking times (6 minutes or less) that were tested.

Effect of AGE Inhibitors on New AGE Formation in Foods

The heat-induced new AGE formation in olive oil was completely prevented in the presence of the AGE inhibitor, aminoguanidine, but only partly blocked by the anti-oxidant BHT (Table 2). The amelioration of new AGE formation by the AGE inhibitor aminoguanidine compared to the anti-oxidant BHT suggests that the process seems to be driven by glycation rather than oxidation.

New AGE formation in cooked meat was also inhibited following exposure to acidic solutions (marinades) of lemon juice and vinegar. Beef that was marinated for 1 hour in these solutions formed less than half the amount of AGEs during cooking than the untreated samples (Figure).

Implications for Practice

Currently, there are limited data on dAGE intakes in the general population. The average dAGE intake in a cohort of healthy adults from the New York City area was recently found to be 14,700±680 AGE kU/day (24). These data could tentatively be used to define a high- or low-AGE diet, depending on whether the estimated daily AGE intake is significantly greater or less than 15,000 kU AGE. From the data presented in Table 1 (available online at www.adajournal.org), it is easy to see how people who consume a diet rich in grilled or roasted meats, fats, and highly processed foods could achieve a dAGE intake in excess of 20,000 kU/day. Conversely, people who regularly consume lower-meat meals prepared with moist heat (such as soups and stews) as part of a diet rich in plant foods could realistically consume half the daily intake seen in this cohort. A safe and optimal dAGE intake for the purposes of disease prevention has yet to be established. However, in animal studies, a reduction of dAGE by 50% of usual intake is associated with reduced levels of oxidative stress, less deterioration of insulin sensitivity and kidney function with age, and longer life span (16).

Reducing dAGE may be especially important for people with diabetes, who generate more endogenous AGEs than those without diabetes (5) and for those with renal disease, who have impaired AGE clearance from the body (14). Recently there has been heightened interest in therapeutic diets that are higher in protein and fat and lower in carbohydrate for weight loss, diabetes, and cardiovascular disease (35–41). This type of dietary pattern may substantially raise dAGE intake and thus contribute to health problems over the long term.

CONCLUSIONS

AGEs in the diet represent pathogenic compounds that have been linked to the induction and progression of many chronic diseases. This report reinforces previous observations that high temperature and low moisture consistently and strongly drive AGE formation in foods, whereas comparatively brief heating time, low temperatures, high moisture, and/or pre-exposure to an acidified environment are effective strategies to limit new AGE formation in food (13). The potentially negative effects of traditional forms of cooking and food processing have typically remained outside the realm of health considerations. However, accumulation of AGEs due to the systematic heating and processing of foods offers a new explanation for the adverse health effects associated with the Western diet, reaching beyond the question of over-nutrition.

The current dAGE database demonstrates that a significantly reduced intake of dAGEs can be achieved by increasing the consumption of fish, legumes, low-fat milk products, vegetables, fruits, and whole grains and by reducing intake of solid fats, fatty meats, full-fat dairy products, and highly processed foods. These guidelines are consistent with recommendations by organizations such as the American Heart Association (42), the American Institute for Cancer Research (43), and the American Diabetes Association (44). It should, therefore, be possible to integrate this new evidence into established guidelines for disease prevention as well as medical nutrition therapy for a wide variety of conditions.

Equally important, consumers can be educated about low-AGE–generating cooking methods such as poaching, steaming, stewing, and boiling. For example, the high AGE content of broiled chicken (5,828 kU/100 g) and broiled beef (5,963 kU/100 g) can be significantly reduced (1,124 kU/100 g and 2,230 kU/100 g, respectively) when the same piece of meat is either boiled or stewed. The use of acidic marinades, such as lemon juice and vinegar, before cooking can also be encouraged to limit dAGE generation. These culinary techniques have long been featured in Mediterranean, Asian, and other cuisines throughout the world to create palatable, easily prepared dishes.

The new database may have limitations, including the fact that foods were selected from diets common in a northeastern metropolitan US area, and may thus not represent the national average. Another limitation is that only two of many AGEs have been measured. However, the fact that both are associated with markers of disease in healthy subjects and are elevated in patients with diabetes and kidney disease lends credibility to their role as pathogens in foods consumed by the general public and persons with certain chronic diseases.

Ongoing studies are needed to further expand the dAGE database and investigate additional methods for reducing AGE generation during home cooking and food processing. Future studies should continue to investigate the health effects of AGEs and refine recommendations for safe dietary intakes. However, current data support the need for a paradigm shift that acknowledges that how we prepare and process food may be equally important as nutrient composition.

Acknowledgments

FUNDING/SUPPORT: This work was supported by the National Institute on Aging (MERIT AG-23188 and AG-09453) and by the National Institute of Research Resources, MO1-RR-00071, awarded to the General Clinical Research Center at Mount Sinai School of Medicine.

Footnotes

STATEMENT OF POTENTIAL CONFLICT OF INTEREST: No potential conflict of interest was reported by the authors.

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