The Maillard Reaction in Foods and Nutrition - ACS Publications

25

Downloaded by UNIV OF MASSACHUSETTS AMHERST on May 29, 2018 | https://pubs.acs.org Publication Date: April 29, 1983 | doi: 10.1021/bk-1983-0215.ch025

Nutritional and Toxicological Effects of Maillard Browned Protein Ingestion in the Rat 1

STEPHEN J. PINTAURO , TUNG-CHING LEE, and CLINTON O. CHICHESTER University of Rhode Island, Department of Food Science and Technology, Nutrition, and Dietetics, Kingston, RI 02881

The Maillard, or nonenzymatic "browning, reaction between reducing sugars and proteins is known to cause serious deterioration of the nutritional quality of foods during processing and storage (1-7). Recently, considerable attention has focused on the physiological effects of the ingestion of Maillard browned compounds beyond those that can be attributed to nutritionally related causes (7,8,9). In addition, the food industry often employs the reaction to produce desirable aromas, colors, and flavors. Thus, if there is indeed a food safety risk associated with Maillard browning, priorities in the food industry may have to be redirected to minimize and control the reaction, rather than promote i t . The purpose of this study was to separate the nutritionally related effects of the long-term feeding of Maillard browned protein, from the toxicological effects. This was done by eliminating, wherever possible, variables that might lead to nutritional problems secondary to the effects of feeding the Maillard proteins. The diets were not only of equal protein quantity, but also of equal and high protein quality. PROCEDURE Maillard Browned Proteins Three types of browned proteins were used in the long-term feeding study; egg albumin, hydrolyzed egg albumin, and a commercial, casein-based, instant breakfast product. The hydrolyzed egg albumin was chosen to examine the effects of feeding severely browned hydrolyzed proteins, such as are commonly used in a variety of processed foods to produce characteristic flavors and colors. The instant breakfast product was included in the feeding study as a representative, commercial food product which may undergo some degree of browning due to the processing or storage. The hydrolyzed egg albumin was prepared by d i s s o l v i n g 5 0 0 g of egg albumin (ICN N u t r i t i o n a l Biochemicals, Cleveland, Ohio) i n 1

Current address : University of Vermont, Department of Human Nutrition & Foods, Burlington, V T 05405

0097-6156/83/0215-0467$06.00/0 © 1983 American Chemical Society Waller and Feather; The Maillard Reaction in Foods and Nutrition ACS Symposium Series; American Chemical Society: Washington, DC, 1983.


468

MAILLARD

REACTIONS

3 1 of d i s t i l l e d water. The s o l u t i o n was adjusted t o pH 1.5 with IN HC1 and 1 g of pepsin (1:10,000, Sigma Chemical Co., St. L o u i s , MO) was added t o the s o l u t i o n . The mixture was allowed t o incubate at 3T°C with mixing f o r 2k h. Following i n c u b a t i o n , the s o l u t i o n was adjusted t o pH 7-0 with IN NaOH and f r e e z e - d r i e d . The egg albumin and hydrolyzed egg albumin samples were prepared f o r browning by mixing 3 parts of the p r o t e i n with 2 p a r t s D-(+)-glucose (ICN N u t r i t i o n a l Biochemicals, Cleveland, Ohio) and a d j u s t i n g the moisture content t o 15$. The i n s t a n t breakfast product (Carnation Company, Waverly, Iowa) was prepared f o r browning by simply a d j u s t i n g the moisture content t o 9%· A l l samples were browned by storage at 37°C i n a sealed g l a s s chamber. The humidi t y was maintained at 68% by p l a c i n g a small beaker of h0% s u l f u r i c a c i d i n the chamber. A f t e r storage f o r hO days, the samples were f r e e z e - d r i e d and m i l l e d f o r i n c o r p o r a t i o n i n t o the d i e t s . Control samples f o r a l l p r o t e i n s were prepared i d e n t i c a l l y t o the browned samples, but immediately f r e e z e - d r i e d r a t h e r than s t o r e d as described above. Determination of P r o t e i n Q u a l i t y The P r o t e i n E f f i c i e n c y Ratio (PER) method was used f o r determining the p r o t e i n q u a l i t y of the treatment d i e t s (10). I t was the purpose of t h i s study t o e l i m i n a t e , as much as p o s s i b l e , n u t r i t i o n a l f a c t o r s from the treatment d i e t s . I t was necessary, t h e r e f o r e , to design the d i e t s so as t o contain s u f f i c ient l e v e l s of brown p r o t e i n , yet at the same time keep the prot e i n q u a l i t y r e l a t i v e l y high. P r o t e i n E f f i c i e n c y Ratios were determined f o r the three types of p r o t e i n at i n t e r v a l s from 0 to ho days of browning under the c o n d i t i o n s described e a r l i e r . PER s were then run on various combinations of the U0-day browned prot e i n s and non-browned p r o t e i n . I t was determined that a d i e t could be formulated that would contain no l e s s than 3% U0-day browned p r o t e i n and s t i l l r e s u l t i n a PER of no lower than 2.0. The PER of the c o n t r o l d i e t s were adjusted t o match the p r o t e i n q u a l i t y o f the experimental (browned) d i e t s by s u b s t i t u t i n g app r o p r i a t e l e v e l s of g e l a t i n as a p r o t e i n source. The r e s u l t i n g p r o t e i n compositions f o r the long-term feeding experiment and t h e i r r e s p e c t i v e P r o t e i n E f f i c i e n c y Ratios are given i n Table I. Diets A l l d i e t s were designed t o contain e x a c t l y 10% p r o t e i n , as measured by the Kjeldahl n i t r o g e n determination method (10). The composition of the remainder of the d i e t i s described i n Table I I . Animals Male, Sprague-Dawley r a t s (COBS-CD s t r a i n ) were purchased at f i v e weeks of age from Charles R i v e r Breeding L a b o r a t o r i e s , Wilmington, MA. The animals were maintained f o r two weeks on Rat Chow (Purina Lab Chow, Ralston Purina Company, St. L o u i s , M0). Following the two-week pretreatment, the animals were weighed and d i s t r i b u t e d i n t o treatment groups as described i n Table I. Animals i n the c o n t r o l groups were p a i r - f e d t o t h e i r c o r r e s ponding browned d i e t treatment animals t o insure equal p r o t e i n i n take i n both groups. Water was s u p p l i e d ad l i b i t u m and weight gain was monitored throughout the study. F i v e animals from each group were s a c r i f i c e d at the end of s i x 1

Waller and Feather; The Maillard Reaction in Foods and Nutrition ACS Symposium Series; American Chemical Society: Washington, DC, 1983.


1% 0-Day Egg Albumin 3% 3% U0-Day Browned Egg Albumin 1% 0-Day Egg Albumin 3% 0-Day Hydrolyzed Egg Albumin 3% Egg Albumin

20

20

20

20

EA-C

EA-B

HEA-C

HEA-B

Cleveland, Ohio

'Carnation Company, Waverly, Iowa

*ICN N u t r i t i o n a l Biochemicals,

Gelatin

2.10 + .39

2.U8 + .23

2.3h + .20

1.9h + .11

2.01 + .07

PER

(Mean + S. D. )

3% U0-Day Browned, Hydrolyzed Egg Albumin 2.28 + .29 1% Egg Albumin

k%

Gelatin

. b

10% U0-Day Browned Instant Breakfast

20

8,

IB-B

1% 0-Day Instant B r e a k f a s t 3% G e l a t i n

P r o t e i n Composition o f D i e t s

20

Number of Rats

IB-C

Group

Composition and P r o t e i n Q u a l i t y o f Proteins Used i n l8-Month Feeding Study-

TABLE I


470

MAILLARD

REACTIONS

TABLE II


Composition of Diets f o r l8-Month Feeding Study

3,

1056

Corn O i l

10%

Protein

Cellulose

5%

Vitamin M±x° Salt Mix

1.2%

h%

0

Dextrose^"

11

M%

Dextrin

11

M%

Sucrose

H

M%

Corn Starch

ilM%

f e r t o Table I f o r composition of p r o t e i n p o r t i o n of d i e t . ^Vitamin d i e t f o r t i f i c a t i o n mixture, ICN N u t r i t i o n a l B i o chemicals, Cleveland, Ohio. °Mineral mixture, ICN N u t r i t i o n a l Biochemicals, Cleveland, Ohio. ^Dextrose content of d i e t was preparing browned p r o t e i n s .

corrected f o r dextrose added i n



25.

PINTAURO

E TA L .

Effects of Browned

Protein

Ingestion

All

and twelve months o f feeding. The remainder were s a c r i f i c e d at the end o f 18 months. A l l animals were f a s t e d f o r 18 hours p r i o r to being s a c r i f i c e d . Serum Preparation Whole blood was c o l l e c t e d a f t e r d e c a p i t a t i o n of the animal and allowed t o c l o t at room temperature f o r 30 min. The serum was then separated from t h e c l o t by c e n t r i f u g a t i o n at 5000 rpm at h°C. A l i q u o t s o f the serum were immediately taken and r e f r i g e r a t e d f o r the determination o f glutamic-pyruvic t r a n s aminase and l a c t i c dehydrogenase. An a d d i t i o n a l 0.5 ml o f serum from each animal was t r e a t e d with a few m i l l i g r a m s o f sodium f l u oride and r e f r i g e r a t e d f o r l a t e r glucose determinations. The r e s t o f the serum was frozen f o r the remainder o f the c l i n i c a l chemistry determinations. Samples o f whole blood were obtained by heart puncture using and EDTA-treated s y r i n g e . The whole blood was immediately assayed f o r hematocrit (percent packed c e l l volume) and hemoglobin by the method o f Drabkin and A u s t i n ( l l ) . Tissue Preparation Following d e c a p i t a t i o n and exsanguination, the l i v e r , kidneys, h e a r t , lungs, spleen, t e s t e s , stomach, and proximal t h i r d o f the small i n t e s t i n e were removed, freed o f f a t , b l o t t e d , and weighed. In a d d i t i o n , t h e cecum was removed, c l e a n ed and r i n s e d i n s a l i n e , b l o t t e d , and weighed. Small samples o f the l i v e r , kidney, spleen, lung, h e a r t , small i n t e s t i n e , and b r a i n were f i x e d i n 10% b u f f e r e d f o r m a l i n f o r h i s t o p a t h o l o g i c a l examination. The remainder o f the t i s s u e was kept i n 0.25M sucrose and frozen i n l i q u i d n i t r o g e n . C l i n i c a l Biochemical Determinations o f t h e Serum Serum l a c t i c dehydrogenase (LDH) and glutamic-pyruvic transaminase (GPT) a c t i v i t i e s were measured on f r e s h , r e f r i g e r a t e d serum w i t h i n U8 h o f s a c r i f i c i n g the animal. L a c t i c dehydrogenase was measured according t o the method o f Amador, Dorfman, and Wacker (12). Serum GPT a c t i v i t y was measured according t o the method o f Wroblewski and LaDue (13). Serum g l u t a m i c - o x a l a c e t i c transaminase (GOT) a c t i v i t y was measured according t o the method o f Karmen ( l k ) serum albumin by the bromocresol green method o f Doumas and Biggs (15), a l k a l i n e phosphatase by the method o f Young, Pestaner, and Gibberman ( l 6 ) , urea n i t r o g e n by the method o f Crocker (17) , t o t a l i r o n and t o t a l i r o n b i n d i n g c a p a c i t y by the method o f P e r s i j n , Van Der S t i k , and R i e t h o r s t ( l 8 ) , t r i g l y c e r i d e s by the method o f Bercolo and David (19), and c h o l e s t e r o l by the method o f Wybenga, et_ a l . (20). Glucose was determined i n serum on a Model 23A, YSI Glucose Analyzer. Determination o f Small I n t e s t i n e Disaccharidases The proximal t h i r d o f the small i n t e s t i n e from r a t s f e d treatment d i e t s f o r l8 months was r i n s e d i n i c e - c o l d 0.25M sucrose, cut open, and the mucosa scraped o f f with a g l a s s s l i d e . The mucosa were then homogenized i n c o l d 0.25M sucrose and c e n t r i f u g e d at 5000 rpm f o r 10 min. The method o f Dahlqvist (21) was used f o r determination o f maltase and sucrase a c t i v i t y . Determination o f L i v e r Glutamic-Oxalacetic Transaminase A sam5


472 pie

MAILLARD

REACTIONS

o f l i v e r (approximately one g) was homogenized i n i c e c o l d

0.25M sucrose and c e n t r i f u g e d at 5000 rpm f o r 10 min t o remove


n u c l e i and c e l l d e b r i s . The method o f Reitman and F r a n k e l (22) was used f o r determination o f g l u t a m i c - o x a l a c e t i c transaminase activity. P r o t e i n Determinations The b i u r e t assay (23) was employed f o r determining p r o t e i n i n t i s s u e samples. S t a t i s t i c a l Analysis A l l data were analyzed f o r s i g n i f i c a n c e between treatment groups u s i n g the Student's t_ t e s t . RESULTS Weight Gain No s i g n i f i c a n t d i f f e r e n c e i n weight gain was d e t e c t ed between browned and c o n t r o l i n s t a n t breakfast product, egg a l bumin, and hydrolyzed egg albumin f e d animals, through 18 months. R e l a t i v e Organ Weights The r e s u l t s f o r the r e l a t i v e organ weights of r a t s f e d the three browned p r o t e i n s or t h e i r c o n t r o l s are l i s t e d i n Table I I I . The browned i n s t a n t b r e a k f a s t product r e s u l t e d i n a s i g n i f i c a n t l y enlarged l i v e r a f t e r s i x months, and a s i g n i f i c a n t l y smaller l i v e r a f t e r 18 months. A f t e r 12 months o f feeding the browned i n s t a n t breakfast product, a s i g n i f i c a n t enlargement of the lung and heart was noted. The browned egg albumin d i e t s r e s u l t e d i n a s i g n i f i c a n t enlargement o f a l l t i s s u e s a f t e r 12 months o f f e e d i n g . The r e l a t i v e weight o f the cecum was n e a r l y double that of the c o n t r o l group. It should be noted, however, that with the p o s s i b l e exception o f the cecum, a l l o f these organ weights f a l l w i t h i n the normal ranges f o r a r a t ( 2U ,25 ). The r e s u l t s f o r the r e l a t i v e organ weights o f r a t s f e d the hydrolyzed egg albumin show few s i g n i f i c a n t changes. Again, the cecum i s enlarged a f t e r s i x and eighteen months of f e e d i n g , and there i s a s l i g h t enlargement of the kidney i n the browned p r o t e i n fed r a t s a f t e r s i x months. Although we observed an i n c r e a s e i n the r e l a t i v e weight of the cecum o f r a t s f e d browned p r o t e i n s , the i n c r e a s e i s much l e s s dramatic than p r e v i o u s l y r e p o r t e d (7 »9 >26)· T h i s appears t o be due t o the f a c t that we cleaned and r i n s e d the cecum before weighing. E a r l i e r i n v e s t i g a t o r s weighed the cecum plus i t s contents. Nevertheless, the enlargement of the cecum i s s t i l l the most d e f i n i t i v e and c o n s i s t e n t organ weight change a s s o c i a t e d with the feeding of M a i l l a r d browned p r o t e i n s . Hemoglobin and Hematocrit The values f o r hemoglobin and hematoc r i t f o r a l l treatment d i e t s through 18 months o f feeding are l i s t ed i n Table IV. The r a t s f e d browned, hydrolyzed egg albumin demonstrated s i g n i f i c a n t l y depressed hemoglobin l e v e l s at s i x months, and s i g n i f i c a n t l y e l e v a t e d hematocrit values at 12 months. The browned-instant b r e a k f a s t - f e d r a t s showed depressed hemoglobin l e v e l s a f t e r 12 months of f e e d i n g . Again, however, a l l values f o r both hemoglobin and hematocrit are w i t h i n the normal ranges f o r r a t s (27,28). I t i s l i k e l y , t h e r e f o r e , that any apparent d i f f e r ence between brown and c o n t r o l groups has l i t t l e c l i n i c a l s i g n i f i cance .



558 6U7 628 553 687 6U7

18 M o n t h s IB-C IB-? EA-C EA-B HEA-C. HEA-B

c

k9-9 2Q.k U9.8 129.7 13k. 2 87.3

2 3 . .6 2 2 . .1 30, .3 77. ,k 7 7 , .5 20, .9

+ S.D.

+ + + + + +

+ + + + + +

2. ,09 1, .89 2. .03 2. .Ik 2, .08 2. .31

2, .17 2, .27 2, .05 2, .29 2. ,U8 2, .36

+ + + + + +

+ + + + + +

.21 .12 .16 .32 .22

.10 .19 .18

.18 .03

2 2

b

b

a

b

Liver 2, .8U + * h 3. .13 + . l l 2. .23 + . 1 2 2. .09 + . o 8 2. .33 + .32 2 . .37 + . 0 8

0. • 5U 0 .Λ 8 0..52 0..58 0, .51 0..5U

0. ,63 0..66 0..62 0..73 0.. 7 3 0,.61

+ + + + + +

+ + + + + +

.06 .05 .OU .11 -13 .08

.08 .ok .03 .io .13 .05

Kidney 0,.57 + .03 0..61 + .03 0..57 + .03 0..56 + . 0 5 0. ,53 + .03 0.,58 + . 0 5

b

a

a

0..27 0..28 0.,2k 0..3k 0,.27 0..3U

0. ,56 0.,59 0 . ,35 0. ,6k 0..55 0. • 51 .07 .08 .06 .l8 .18 .07

+ .07 .07 + .06 + .12 + .09 + .05

+ + + + + +

a

a

b

Cecum 0..UU + . 0 9 0..U6 + . 1 0 0,.33 + . 0 9 0..Uo + .03 0..32 + . 0 2 0..U6 + . 0 7 °

0 . ,12 0..12 0. .11 0.,1k 0..12 0,.1U

0..18 0..20 0,.13 0..19 0,.15 0,.11

+ + + + +

+ + + + + +

.02 .OU .02 .02 .02 .02

a

.03 .02 .03 .02° .05 .02

Spleen 0.13 + . 0 1 0.13 + . 0 1 0.13 + '. 0 1 0.13 + . 0 1 0.13 + . 0 2 O.lU + . 0 2

S i g n i f i c a n t l y d i f f e r e n t from c o n t r o l : a , a t p

2

4^


25.

PINTAURO

E TA L .

Effects of Browned

Protein

Ingestion

475

C l i n i c a l Biochemistry The r e s u l t s o f the c l i n i c a l "biochemical a n a l y s i s o f the serum from r a t s fed treatment d i e t s f o r up t o 18 months are l i s t e d i n Table V. Rats fed browned i n s t a n t breakfast product f o r 12 months e x h i b i t e d s i g n i f i c a n t l y elevated blood urea nitrogen l e v e l s over c o n t r o l r a t s . A f t e r 18 months o f feeding, serum g l o b u l i n and albumin were c l e a r l y lower than i n c o n t r o l s . The r e s u l t s f o r r a t s fed browned or c o n t r o l egg albumin are also l i s t e d i n Table V. The only s i g n i f i c a n t change evident was a depressed serum glutamic-oxalacetic transaminase a c t i v i t y i n the browned fed r a t s a f t e r s i x months. The only s i g n i f i c a n t changes observed i n r a t s fed browned hydrolyzed egg albumin were a s l i g h t l y elevated serum glutamic-pyr u v i c transaminase a c t i v i t y a f t e r 6 months, and a s l i g h t l y e l e v a t ed serum g l o b u l i n l e v e l a f t e r 12 months. A l l values f o r a l l serum assays i n t h i s s e c t i o n f a l l w i t h i n the normal ranges f o r r a t s , reported i n the l i t e r a t u r e (25,27)» No p a t t e r n i n the c l i n i c a l biochemistry p r o f i l e a s s o c i a t e d with the feeding o f M a i l l a r d browned proteins i s apparent. The few assays that d i d show s i g n i f i c a n t d i f f e r e n c e s between browned and c o n t r o l groups are s t i l l w i t h i n the normal ranges and, t h e r e f o r e , probably have no c l i n i c a l s i g n i f i c a n c e . Serum, C h o l e s t e r o l and T r i g l y c e r i d e Serum t r i g l y c e r i d e and chol e s t e r o l l e v e l s were measured i n r a t s fed M a i l l a r d browned prot e i n s o r c o n t r o l d i e t s f o r 18 months. The r e s u l t s are given i n Table VI. The feeding o f M a i l l a r d browned egg albumin r e s u l t e d i n a s i g n i f i c a n t l y lower l e v e l o f both c h o l e s t e r o l and t r i g l y c e r ides over animals fed the c o n t r o l egg albumin d i e t . S i m i l a r r e s u l t s o f serum c h o l e s t e r o l values were observed by Gomyo (2£). He suggested that the e f f e c t may be due t o an i n t e r f e r e n c e i n enterohepatic c i r c u l a t i o n and/or an i n h i b i t i o n o f the absorption of d i e t a r y c h o l e s t e r o l . The l a t t e r hypothesis i s l i k e l y the more accurate explanation, as we found no other evidence o f an i n t e r ference i n enterohepatic c i r c u l a t i o n , such as changes i n serum bilirubin levels. Serum T o t a l Iron and T o t a l Iron Binding Capacity The r e s u l t s f o r the determination o f serum t o t a l i r o n and t o t a l i r o n - b i n d i n g c a p a c i t y o f r a t s fed treatment d i e t s f o r 18 months are a l s o l i s t e d i n Table VI. A s i g n i f i c a n t increase i n serum t o t a l i r o n was det e c t e d i n r a t s fed the M a i l l a r d browned egg albumin over t h e i r c o n t r o l group. Increased serum t o t a l i r o n with normal t o t a l i r o n binding capacity i s a s s o c i a t e d with hemolytic anemia, hemochromat o s i s , hemosiderosis, and h e p a t i t i s (30). On the b a s i s o f other c l i n i c a l and h i s t o p a t h o l o g i c a l data, however, none o f these causes are l i k e l y . I n t e s t i n a l Disaccharidase A c t i v i t y The r e s u l t s o f the determinat i o n o f small i n t e s t i n e mucosal maltase and suerase a c t i v i t y f o r a l l animals fed treatment d i e t s f o r 18 months are given i n Table VII. No d i f f e r e n c e was detected i n the a c t i v i t i e s o f these enzymes from the animals fed the i n s t a n t breakfast product or the hydrolyzed egg albumin. The animals fed the browned egg albumin,



1

b

(mg %)

1 2 ..7 9-.8 7-.8 1 7 .,1+ 1 1 .,2 Ik.,6

+ 9. 6 + 17. 9 + 10. 6 + 9- 3 + 17. 8 + Ik. 1

+ + + + + +

(Mean + S.D.)

81 76 78 87 73 73

73 82 78 67 75 79

ND 10k + 1 1 ,• 7 8 0 + 1 2 , .1 6 7 + 1 2 , .8 58 + 1 6 ..3 63 + 6..7

Glucose

2.1 1.5 2.1+ 2.1+ 2.1 2.1

3.5 3.1 3.9 3.8 3.k 1+.0

2.5 2.7 2.5 2.6 2Λ

+ + + + + +

+ + + + + +

ND + + + + +

0.30 0.1+6 0.25 0.3k 0.33 0.25

0.15 0.37 0.5U 0.7k 0.39 0.38

e

c

( g %)

0.30 O.3U 0.33 0.53 0.25

Globulin

3 . .8 3 . .2 1+..0 1+. 0 k.,0 3. 9

2, .1+ 2. .3 2. .5 2. .1+ 2. .1+ 2 . •3

2,. 0 3,.2 3,.2 3,.7 3, .1+ 1.1 0.1+9 0.23 0.28 0.19

+ + + + + +

0.1+0 0.52 0.25 2.6 0.33 0.21+ d

( g %)1

0.10 0.3k 0.18 0.36 0.23 ± 0.2k

+ + + + +

ND + + + + +

Albumin

Significantly different

(units/ml)

from c o n t r o l :

Serum a l k a l i n e phosphatase

+ + + + + +

+ + + + + +

+ + + + + +

3.0 2.3 2.3 1.6 1.9 1.5

e

3.1 1.8 3.2 1.2 Ο.76 1.58

6.6 1.6 0.72 1.7 0.68 0.91

(mg %)

transaminase

8.8 8.6 11.5 10.7 10.7 10.9

8.8 12.3 8.9 12.1+ 11.9 12.1

6.0 6.0 7.1 5Λ 5.2 5.7

B . U. N . .

Λ

+ + + + + +

+ + + + + +

27.,3 1+6..8 58. ,1+ 38. .1+ 9 1 . .6 U9.9

17, .2 2 1 . .5 2 8 . .2 k3. .1 16. .0 1 6 . .2

d

+ 1 1 . .2 + 9..9 + 5,. 5 + 8,.k + 9,.1+ + 3. .8

(units/ml)

179 175 225 231 21+3 21+8

92 100 103 9k 100 101+

kl 53 5U 1+1 53 53

a

Proteins

SG0T

c , a t p < 0 . 0 5 ; d , a t p < 0 . 0 2 5 ; e, a t p

The Maillard Reaction in Foods and Nutrition - ACS Publications

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