Seventy Years of the Maillard Reaction - American Chemical Society

1

S e v e n t y Y e a r s of t h e

Maillard

Reaction

Downloaded by 171.113.221.145 on October 13, 2015 | http://pubs.acs.org Publication Date: April 29, 1983 | doi: 10.1021/bk-1983-0215.ch001

SIN'ITIRO KAWAMURA Kagawa-ken Meizen Junior College, Kameoka 1-10, Takamatu, 760 Japan

A historical review with107 references. Life and work of Louis-Camille Maillard (Feb. 4, 1878 May 12, 1936) are described. The first use of the index term Maillard reaction in Chemical Abstracts was in 1950. German scientists with early interest in this reaction were Lintner (1912) and Ruckdeschel (1914). Several aspects of this reaction are reviewed with emphasis on the work of Japanese scientists. About the Year 1912 Ten years ago Kawamura (_1) published a brief historical review on this reaction in memory of the sixtieth anniversay of its first report by Louis-Camille Maillard (2). The first Maillard paper was presented on January 8, 1912, by Armand Emile Justin Gautier (1837-1920) in a session of the Academy of Sciences in Paris. Six weeks earlier (November 27, 1911) a remarkable study was reported by Maillard Ο ) on the condensation of amino acids by use of glycerol. The method of peptide synthesis by Emil Hermann Fischer (1835-1919) was known to him. However, Maillard searched for milder conditions. Thus he wished to condense amino acids by use of glycerol as a condensing agent. He thus obtained cycloglycylglycine and pentaglycylglycine. Maillard (2^) then used sugars instead of glycerol to investigate the formation of polypeptides by the reaction of amino acids with alcohols. It was found that the aldehyde group (of an aldose) had more intense effect on amino acids than did the hydroxyl groups. This led to the discovery of this reaction. In a later report Maillard (4) cited a paper (5) by Arthur Robert Ling (1861-1937). Ling, lecturer on brewing and malting at the Sir John Cass Institute, presented a paper on 0097-6156/83/0215-0003$06.00/0 © 1983 American Chemical Society In The Maillard Reaction in Foods and Nutrition; Waller, G., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 1983.

4

MAILLARD REACTIONS

m a l t i n g at the meeting h e l d at the C r i t e r i o n R e s t a u r a n t , P i c c a d i l l y , L o n d o n , on May 11, 1908. He n o t e d a r e m a r k a b l e e f f e c t of k i l n i n g or heat d r y i n g . "At t h e s e c o n d s t a g e o f k i l n i n g when t h e range o f t e m p e r a t u r e i s f r o m 120 t o 150°C, t h i s m e l l o w i n g by a u t o d i g e s t i o n i s continued Flavouring and c o l o u r i n g m a t t e r s a r e produced....When t h e s e amino-compounds p r o d u c e d f r o m p r o t e i n s a r e h e a t e d a t 120-140 C w i t h s u g a r s s u c h as o r d i n a r y g l u c o s e o r m a l t o s e , w h i c h a r e produced at t h i s stage of p r o c e s s , c o m b i n a t i o n o c c u r s . The p r e c i s e n a t u r e o f t h e compounds p r o d u c e d i s unknown t o me, but t h e y a r e p r o b a b l y g l u c o s a m i n e - l i k e b o d i e s . " He f u r t h e r d e s c r i b e d the r e a c t i o n of h e a t i n g g l u c o s e w i t h a s p a r a g i n e , which produced darkening i n c o l o r . C a r l Joseph Ludwig L i n t n e r (1855-1926), l e a d e r of the S c i e n t i f i c S t a t i o n f o r Brewing ( W i s s e n s c h a f t l i c h e S t a t i o n fuer B r a u e r e i ) i n M u n i c h was s t u d y i n g t h e f o r m a t i o n o f m a l t aroma. He gave a l e c t u r e ( 6 ) a t t h e 3 6 t h M e e t i n g o f t h e S t a t i o n i n November, 1912. As soon as he knew o f t h e r e p o r t o f M a i l l a r d (2^), he made some e x p e r i m e n t s by t h e p r o c e s s o f M a i l l a r d ( n a c h dem Vorgange v o n M a i l l a r d ) . He o b t a i n e d d a r k r e a c t i o n p r o d u c t s w h i c h were r e s p o n s i b l e a l s o f o r f l a v o r and aroma ( c f . 7). Ame P i c t e t (1857-1937) o f t h e U n i v e r s i t y o f Geneva r e p o r t e d t h e f o r m a t i o n o f p y r i d i n e and i s o q u i n o l i n e b a s e s f r o m a c i d h y d r o l y z a t e of c a s e i n i n the presence of formaldehyde i n 1916 ( 8 ) . M a i l l a r d ( 9 ) c l a i m e d p r i o r i t y o v e r him i n d i s c o v e r i n g t h e c o n d e n s a t i o n o f amino a c i d s w i t h a l d e h y d e s o r s u g a r s t o y i e l d p y r i d i n e b a s e s by c i t i n g h i s own p a p e r ( 1 0 ) . We s h o u l d n o t e t h a t W o r l d War I went on f r o m J u l y 1914 t o November 1918; S w i s s s c i e n t i s t s c o u l d c o n t i n u e r e s e a r c h , whereas F r e n c h ones c o u l d n o t do so e a s i l y . 1

1


q

L i f e and Work o f M a i l l a r d

(1878-1936)

L o u i s - C a m i l l e M a i l l a r d was b o r n on F e b r u a r y 4, 1878 i n P o n t - a - M o u s s o n (Meuthe e t M o s e l l e ) (48.55°N , 6.03°E). He went to Nancy, where he o b t a i n e d t h e d e g r e e s o f M. S c . i n 1897 and Dr. Med. i n 1903. T h e r e a f t e r he worked i n t h e C h e m i c a l D i v i s i o n o f t h e S c h o o l o f M e d i c i n e , U n i v e r s i t y o f Nancy. In 1914 he moved t o P a r i s and t h e young d o c t o r worked as head o f a b i o l o g i c a l group i n t h e C h e m i c a l L a b o r a t o r y , U n i v e r s i t y o f Paris (7). In 1911 h i s f i r s t r e p o r t (3») on p e p t i d e s y n t h e s i s was p r e s e n t e d and i n 1912 h i s f i r s t r e p o r t ( 2 ) on t h e s u g a r - a m i n o a c i d r e a c t i o n was p u b l i s h e d . He c o m p l e t e d a book (1_1) i n 1913. A f t e r W o r l d War I i n 1919 he was a p p o i n t e d p r o f e s s o r o f b i o l o g i c a l and m e d i c a l c h e m i s t r y a t t h e U n i v e r s i t y o f A l g i e r s . In t h e same y e a r he became a c o r r e s p o n d i n g member o f t h e D i v i s i o n o f Pharmacy, Academy of M e d i c i n e . In May 1936 he was i n v i t e d t o P a r i s f o r a l e c t u r e . On

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

1.

KAWAMURA

Seventy Years of the Maillard Reaction

May 12, 1936, he d i e d s u d d e n l y d u r i n g a m e e t i n g , where he was a judge of the c o m p e t i t i o n f o r f e l l o w s h i p ( 1 2 ) . T h e r e a r e a t l e a s t 6 p a p e r s o f M a i l l a r d (_3> 13-17) on p e p t i d e s y n t h e s i s and a t l e a s t 8 (2^, 4, 9, 10, 18-21) on t h e sugar-amino a c i d r e a c t i o n . T h i s r e a c t i o n , r e p o r t e d b r i e f l y i n 1912 (_2) , was d e s c r i b e d i n d e t a i l l a t e r ( 2 0 ) . The e v o l u t i o n o f c a r b o n d i o x i d e d u r i n g the r e a c t i o n was a t t r i b u t e d t o t h e c a r b o x y l group o f t h e amino a c i d a f t e r very c a r e f u l q u a n t i t a t i v e experiments. The m e l a n o i d i n p r e p a r e d f r o m g l u c o s e and g l y c i n e was s o l u b l e i n t h e e a r l y s t a g e and t h e n became i n s o l u b l e i n t h e l a t e r stage of h e a t i n g . The i n s o l u b l e m e l a n o i d i n he o b t a i n e d c o n t a i n e d C 58.85, H 4.92, Ν 4.35, and 0 3 1 . 8 8 % ; t h u s t h e e m p i r i c a l f o r m u l a was ^ β ΐ 5 β · He p r o c e e d e d t o c a r r y o u t t h e r e a c t i o n s o f v a r i o u s amino a c i d s w i t h g l u c o s e a t 100°C, and r e a c t i o n s o f g l y c i n e w i t h v a r i o u s s u g a r s ( a r a b i n o s e , x y l o s e , g l u c o s e , mannose, g a l a c t o s e , f r u c t o s e , m a l t o s e , l a c t o s e , and s u c r o s e ) a t 100°C. I n t h e f i r s t e x p e r i m e n t s t h e a c t i v i t y i n t h i s r e a c t i o n was i n t h e order (highest f i r s t ) : a l a n i n e , v a l i n e , g l y c i n e , glutamic a c i d , l e u c i n e , s a r c o s i n e , and t y r o s i n e . T h i s i s n e a r l y t h e same as the o r d e r g i v e n more r e c e n t l y by K a t o (22^). I n l a t e r e x p e r i m e n t s M a i l l a r d ( 2 0 ) showed t h a t s u c r o s e , a n o n r e d u c i n g s u g a r , gave no b r o w n i n g upon s h o r t h e a t i n g w i t h g l y c i n e , b u t t h e m i x t u r e showed t h e b e g i n n i n g o f a d a r k e n i n g r e a c t i o n a f t e r 3 h r o f h e a t i n g , w h i c h was a t t r i b u t e d t o h y d r o l y s i s o f s u c r o s e . P e n t o s e s , e s p e c i a l l y x y l o s e , gave h i g h e r v e l o c i t y i n t h i s r e a c t i o n than hexoses. Being a b i o c h e m i s t , M a i l l a r d (20) s t u d i e d the r e a c t i o n of g l y c i n e w i t h x y l o s e o r g l u c o s e a t 40° and t h e n a t 34°C, i n o r d e r t o know t h e p o s s i b i l i t y o f t h e change i n v i v o . The l a s t c h a p t e r o f t h e same r e p o r t ( 2 0 ) d e a l s w i t h r e a c t i o n o f g l y c y l g l y c i n e w i t h x y l o s e a t 75, 40, and 34°C, and t h r e e c o m m e r c i a l p e p t o n e p r e p a r a t i o n s w i t h x y l o s e a t 110°C. The l a t t e r c o m b i n a t i o n s d a r k e n e d a f t e r 45 t o 90 m i n . The l a s t r e p o r t o f M a i l l a r d (2_1) i s r a t h e r a r e v i e w i n n a t u r e , w i t h more t h a n 50 r e f e r e n c e s . The c h e m i c a l n a t u r e s n o t o n l y o f humus i n s o i l b u t a l s o o f m i n e r a l f u e l ( c o a l ) and b r o w n i n g i n f o o d m a t e r i a l were d i s c u s s e d , e s p e c i a l l y i n r e l a t i o n t o t h e p r e s e n c e o f n i t r o g e n i n browned p r o d u c t s , w h i c h was i n f e r r e d t o be d e r i v e d f r o m amino a c i d s ( a n d r e l a t e d n i t r o g e n o u s m a t e r i a l s ) used f o r s y n t h e t i c " m e l a n o i d i n s " . Thus M a i l l a r d w o r k e d e n e r g e t i c a l l y on t h i s r e a c t i o n f r o m 1911 t h r o u g h 1917 w i t h n o t a b l e r e s u l t s .


(

Naming t h e " M a i l l a r d

Η

Ν Ο

Reaction"

R e y n o l d s (2J3, 24) and S t r a h l m a n n (_7) have c i t e d E l l i s (1959) (2_5) and Heyns and P a u l s e n ( 1 9 6 0 ) ( 2 6 ) as t h e f i r s t t o c a l l t h i s browning the M a i l l a r d r e a c t i o n . I t i s c e r t a i n l y t r u e


5

MAILLARD REACTIONS

6

t h a t t h e y p u b l i s h e d r e v i e w a r t i c l e s w i t h t h e s e words i n t h e title. However, I wondered i f any o t h e r w o r k e r u s e d t h e t e r m Maillard reaction earlier. E x a m i n a t i o n of the s u b j e c t indexes of Chemical A b s t r a c t s (CA) r e s t r i c t e d t o t h e terms b r o w n i n g and M a i l l a r d r e a c t i o n gave t h e r e s u l t s shown i n T a b l e I . Table I .


Vols.

(Years)

" B r o w n i n g " and " M a i l l a r d r e a c t i o n " as Terms i n CA ( a ) Browning

(b)

Maillard

1-10 (1907-16) C o l o r , change o f 11-20 (1917-26) 21-30 (1927-36) D i s c o l o r a t i o n * 31-40 (1937-46) 41-50 (1947-56) ( o f f o o d s ) 18 browning 169 51-55 (1957-61) π *** 56-65 (1962-66) 66-75 (1967-71) 120 3 40 76-85 (1972-76) Browning'J U ^ U J U ^ . 1 5 1

(a) (b) * **

Index

reaction.

No

Yes

13 32 52 77 157

Number o f a b s t r a c t s u n d e r each i n d e x t e r m shown. Browning or s u b s t i t u t e index term. (See a l s o C o l o r ( s ) ; C o l o r i n g ; S t a i n i n g ; Y e l l o w i n g . ) (See a l s o " b r o w n i n g " under D i s c o l o r a t i o n . )

***Browning r e a c t i o n . See M a i l l a r d r e a c t i o n ; see " b r o w n i n g " under D i s c o l o r a t i o n . D i s c o l o r a t i o n , b r o w n i n g . — See a l s o M a i l l a r d r e a c t i o n . * * * * S t u d i e s o f b r o w n i n g o f f o o d and r e l a t e d m a t e r i a l s were indexed at t h i s heading. Thus CA a l r e a d y u s e d t h e i n d e x t e r m M a i l l a r d r e a c t i o n i n t h e 5 t h C o l l e c t i v e I n d e x ( 1 9 4 7 - 5 6 ) , p r i o r t o 1959. There was no i n d e x t e r m M a i l l a r d r e a c t i o n up t o v o l . 43 (1949) o f CA. The e a r l i e s t c i t a t i o n s by t h a t t e r m a r e t o t h e 6 p a p e r s (27-32) i n CA 44 (1950) and 46-48 ( 1 9 5 2 - 5 4 ) . J o h n B. Thompson (21) worked a t t h e T r a c e M e t a l R e s e a r c h L a b o r a t o r i e s i n C h i c a g o , w h i l e Andre P a t r o n (28) was employed a t t h e I n s t i t u t e o f C o l o n i a l F r u i t s and C i t r u s e s ( I n s t i t u t e de F r u i t s e t Agrumes C o l o n i a u x ) i n P a r i s , and p r e p a r e d a r e v i e w ( 3 3 ) c o n t a i n i n g t h e words M a i l l a r d r e a c t i o n i n t h e t i t l e . R. G e o f f r o y (29) o f t h e F r e n c h C o l l e g e o f M i l l i n g ( E c o l e Française de M e u n e r i e ) i n P a r i s a l s o p u b l i s h e d a b r i e f r e v i e w on t h e M a i l l a r d r e a c t i o n i n the c e r e a l i n d u s t r y . H. L. A. T a r r (30) o f P a c i f i c F i s h e r i e s S t a t i o n , V a n c o u v e r , B r i t i s h C o l u m b i a , as w e l l as Hans Wegner (3_2) o f t h e R e s e a r c h I n s t i t u t e o f S t a r c h F a b r i c a t i o n ( F o r s c h u n g s i n s t i t u t der S t a e r k e f a b r i k a t i o n ) i n B e r l i n , a l s o used t h i s term i n the t i t l e s of r e s e a r c h papers.



1.

KAWAMURA

Seventy Years of

the

Maillard Reaction

7

P. de Lange (31) o f t h e C e n t r a l I n s t i t u t e o f Food R e s e a r c h (Centr. I n s t . Voedingonderzoek), U t r e c h t , Netherlands reviewed t h e mechanism o f t h e M a i l l a r d r e a c t i o n , though h i s t i t l e d i d n o t show t h e t e r m . Thus, I once c o n s i d e r e d Thompson ( 1 9 5 0 ) and P a t r o n (1950) to be t h e f i r s t namers o f t h e M a i l l a r d r e a c t i o n . However, B a r n e s and Kaufman (34) o f G e n e r a l Foods C o r p o r a t i o n , Hoboken, N J , p u b l i s h e d a r e v i e w i n 1947, t h r e e y e a r s e a r l i e r , o f w h i c h t h e a b s t r a c t i n CA b e g i n s t h u s : " M a i l l a r d o r b r o w n i n g r e a c t i o n i n f o o d s t u f f s i s a t t r i b u t e d t o a r e a c t i o n between s u g a r s and p r o t e i n s o r o t h e r amino b o d i e s , " and t h e r e v i e w i t s e l f r e p e a t e d l y r e f e r s to the M a i l l a r d r e a c t i o n . L a t e r I found t h a t P a t r o n (33) c i t e d a p a p e r by S e a v e r and K e r t e s z (1946) (35) w i t h t h i s term i n the t i t l e . However, t h i s t y p e o f s e a r c h p r o v e d n o t r e l i a b l e . In r e a d i n g t h e a b s t r a c t o f a p a p e r by W i l l y R u c k d e s c h e l (36) o f the L a b o r a t o r y of Fermentation Chemistry, Royal T e c h n i c a l C o l l e g e ( K o e n i g l i c h e Technische Hochschule) at Munich I found t h e words M a i l l a r d ' s r e a c t i o n i n CA more t h a n t h r e e t i m e s . The o r i g i n a l p a p e r by R u c k d e s c h e l (1914) (36) c o n t a i n e d t h e words " d i e R e a k t i o n M a i l l a r d s " f i r s t and t h e n t h e words " d i e M a i l l a r d s c h e R e a k t i o n " f o u r t i m e s . Hence, he may be c a l l e d one of t h e f i r s t namers o f t h i s r e a c t i o n . I t i s t r u e t h a t M a i l l a r d h i m s e l f w r o t e o f t e n "my r e a c t i o n " (ma r e a c t i o n ) . I t i s a v e r y s i m p l e but c l e a r c o n c l u s i o n t h a t t h e f i r s t namer o f t h e M a i l l a r d r e a c t i o n was t h e o r i g i n a l a u t h o r M a i l l a r d h i m s e l f ! I b e l i e v e t h a t no one w o u l d p r o t e s t t h i s d e d u c t i o n . As has a l r e a d y been n o t e d , i n 1912 L i n t n e r ( 6 ) u s e d t h e p h r a s e "by t h e p r o c e s s o f M a i l l a r d " . I t i s of i n t e r e s t t o f i n d two German s c i e n t i s t s , L i n t n e r and Ruckdeschel, c o n c e r n i n g themselves w i t h a r e a c t i o n then r e c e n t l y d i s c o v e r e d by a F r e n c h s c i e n t i s t , e s p e c i a l l y s i n c e W o r l d War I began i n J u l y , 1914. Chemistry of the M a i l l a r d R e a c t i o n Among c h e m i c a l r e v i e w s (22-26, 37-42) t h e p a p e r o f Hodge ( 3 8 ) c o n t a i n i n g t h e famous scheme i s e s p e c i a l l y n o t a b l e . The scheme was c o n s i d e r e d p r a c t i c a l l y u s e f u l and e f f e c t i v e even a f t e r 25 y e a r s ( 4 2 ) . The c o n d e n s a t i o n o f an amino a c i d w i t h an a l d o s e t o f o r m a S c h i f f base was f i r s t r e c o g n i z e d by M a i l l a r d (20). The r e s u l t i n g N - s u b s t i t u t e d a l d o s y l a m i n e i s c o n v e r t e d t o a d e o x y k e t o s y l a m i n e by t h e A m a d o r i r e a r r a n g e m e n t . ( I n the r e a c t i o n o f an amino a c i d w i t h a k e t o s e a d e o x y a l d o s y l a m i n e i s formed by t h e Heyns r e a r r a n g e m e n t ( 2 4 ) ) . The t h r e e pathways o f Hodge (_38) s h o u l d be augmented t o f i v e (41 ). Condensation products of t r i o s e reductone w i t h g l y c i n e , l e u c i n e , m e t h i o n i n e , and p h e n y l a l a n i n e have been c h a r a c t e r i z e d (43). H a s h i b a , ejt a l . (44) i s o l a t e d s i x A m a d o r i compounds f r o m


MAILLARD REACTIONS

soy sauce and o t h e r brewed p r o d u c t s . Very r e c e n t l y Hashiba (45) compared t h e i n t e n s i t y o f b r o w n i n g c a u s e d by h e a t i n g s u g a r s w i t h g l y c i n e a t 120°C f o r 5 m i n . I t was i n t h e o r d e r (highest f i r s t ) : ribose, glucuronic acid, xylose, arabinose, g a l a c t u r o n i c a c i d , g a l a c t o s e , mannose, g l u c o s e , and l a c t o s e . R e d u c i n g power and t h e amount o f g l y c i n e consumed were p r o p o r t i o n a l t o t h e i n t e n s i t y of b r o w n i n g , but t h e amount o f A m a d o r i compounds a c c u m u l a t e d i n t h e r e a c t i o n m i x t u r e c o u l d n o t be c o r r e l a t e d w i t h t h e s e . The c o r r e s p o n d i n g A m a d o r i compounds were a l s o compared f o r b r o w n i n g i n t e n s i t y . A general route I


Sugar + amino a c i d

II A m a d o r i compd

brown p i g m e n t

has been p o s t u l a t e d f o r t h e M a i l l a r d r e a c t i o n by K a t o (40)· It was t h e p u r p o s e o f H a s h i b a ' s s t u d y t o f i n d w h e t h e r d i f f e r e n c e s i n b r o w n i n g a r e due t o d i f f e r e n c e s i n r e a c t i o n v e l o c i t y i n s t e p I o r I I . However, t h e r e s u l t s were not c l e a r - c u t . He c o n s i d e r e d t h a t t h e d i f f e r e n c e o f b r o w n i n g among s u g a r s depended on t h e r a t e o f s t e p I o r a c o m b i n a t i o n o f r a t e s o f b o t h s t e p s I and I I , a c c o r d i n g t o t h e s u g a r u s e d . N a m i k i and H a y a s h i (46) r e c e n t l y summarized t h e i r t h e o r y o f f o r m a t i o n o f i n t e r m e d i a t e f r e e r a d i c a l s , Ν, Ν'-disubstituted p y r a z i n e c a t i o n r a d i c a l s , i n an e a r l y s t a g e o f t h e M a i l l a r d r e a c t i o n ( c f . 47). M e l a n o i d i n s ( 3 6 , 48-50) a r e d i f f e r e n t f r o m m e l a n i n s , h u m i n s , and c a r a m e l s , but s i m i l a r t o humus (3_7 ), a c c o r d i n g t o M a i l l a r d ( 4 , 11, 1 9 - 2 1 ) . K a t o and T s u c h i d a (51) s t u d i e d the p o s s i b l e c h e m i c a l s t r u c t u r e of m e l a n o i d i n s . N u t r i t i o n a l Aspects

of the M a i l l a r d

Reaction

Some r e v i e w s ( 4 ^ , 52-54) a r e a v a i l a b l e . The p o s i t i v e a s p e c t s a r e f o u n d i n t h e p r o d u c t i o n o f d e s i r a b l e f l a v o r s and aromas. F u j i m a k i and K u r a t a (5_5) l i s t e d a l d e h y d e s and p y r a z i n e s , v o l a t i l e compounds p r o d u c e d by h e a t i n g amino a c i d s w i t h c a r b o n y l compounds, i s o v a l e r a l d e h y d e p r o d u c e d by r e a c t i o n o f l e u c i n e w i t h c a r b o n y l compounds ( a l d e h y d e s , 3 - d e o x y g l u c o s o n e , x y l o s e , and g l u c o s e ) , and v o l a t i l e compounds p r o d u c e d by r e a c t i o n o f c y s t e i n e w i t h p y r u v a l d e h y d e . A recent r e v i e w (5_6) c i t e d 127 r e f e r e n c e s i n c l u d i n g about 30 J a p a n e s e ones. To s t u d y t h e e f f e c t o f t h e M a i l l a r d r e a c t i o n on n u t r i t i v e v a l u e o f p r o t e i n , P a t t o n , e_t a l . (57) h e a t e d p u r i f i e d c a s e i n and soybean g l o b u l i n i n 5% g l u c o s e s o l u t i o n f o r 24 h r s a t 96.5°C, and f o u n d s i g n i f i c a n t l o s s e s o f l y s i n e , a r g i n i n e , t r y p t o p h a n , and h i s t i d i n e ( 5 2 ) . Kawamura, e_t a _ l . (58) r e p o r t e d t h a t t h e n o n r e d u c i n g sugar l e v e l , a v a i l a b l e l y s i n e , and w h i t e n e s s d e c r e a s e d i n p a r a l l e l w i t h h e a t i n g t i m e o f d e f a t t e d soybean f l a k e s a t 100 o r 120°C. C o n c e n t r a t i o n s of the t h r e e o l i g o s a c c h a r i d e s ( s u c r o s e ,


KAWAMURA

Seventy Years of

the

Maillard Reaction

9

r a f f i n o s e , and s t a c h y o s e ) t e n d e d t o d e c r e a s e . These n o n r e d u c i n g s u g a r s were presumed t o u n d e r g o h y d r o l y s i s upon h e a t i n g , and r e d u c i n g s u g a r s formed ( f r u c t o s e , g l u c o s e , and g a l a c t o s e ) were r e s p o n s i b l e f o r t h e M a i l l a r d r e a c t i o n . S t u d i e s w i t h N - n o n d i a l y z a b l e m e l a n o i d i n showed t h a t 76% of t h e d i e t a r y m e l a n o i d i n was e x c r e t e d i n r a t s ' f e c e s ( 5 9 ) . The o r a l a d m i n i s t r a t i o n o f M a i l l a r d r e a c t i o n p r o d u c t s c a u s e d an i n c r e a s e i n t h e g r o w t h o f b o t h a e r o b i c and a n a e r o b i c l a c t o b a c i l l i i n the m i c r o f l o r a of r a t s ( 6 0 ) . 1 5


M u t a g e n i c i t y of M a i l l a r d R e a c t i o n Products I n a d v a n c e d s t a g e s o f t h e M a i l l a r d r e a c t i o n some mutagens m i g h t be f o r m e d . F o r e x a m p l e , mutagens a p p e a r e d when g r o u n d b e e f hamburgers were c o o k e d o v e r 200°C ( c f . 41)· Reductive i n t e r m e d i a t e s i s o l a t e d from b r o w n i n g m i x t u r e s o f t r i o s e r e d u c t o n e w i t h g u a n i n e and i t s d e r i v a t i v e s a l s o showed mutagenicity (61). Japanese workers i n the N a t i o n a l Cancer Center Research I n s t i t u t e p u b l i s h e d r e v i e w s c o n c e r n i n g mutagens i n h e a t e d f o o d s (62-64). P y r o l y z a t e s o f p r o t e i n s , p e p t i d e s , and amino a c i d s , e s p e c i a l l y t r y p t o p h a n and g l u t a m i c a c i d , showed m u t a g e n i c i t y (65-69). C o f f e e p r e p a r e d i n t h e u s u a l way f o r d r i n k i n g c o n t a i n e d some m u t a g e n i c s u b s t a n c e ( s ) ( 7 0 ) . B l a c k t e a and g r e e n t e a were a l s o m u t a g e n i c . However, t h e s e f a v o r i t e b e v e r a g e s were n o t c a r c i n o g e n i c ( 6 4 ) . N i n e h e t e r o c y c l i c amines were i s o l a t e d as m u t a g e n i c compounds f r o m p y r o l y z a t e s ( 6 3 ) : two p y r i d o i n d o l e s , f o u r p y r i d o i m i d a z o l e s , two i m i d a z o q u i n o l i n e s , and 2 - a m i n o - 5 - p h e n y l p y r i d i n e . None o f them have been i s o l a t e d as p r o d u c t s o f t h e M a i l l a r d r e a c t i o n . Moreover, m u t a g e n i c i t y a p p e a r e d o n l y above 400°, and even more s t r o n g l y a t 500-600°C as t h e p y r o l y s i s t e m p e r a t u r e . L e e , e_t a _ l . (_71) c a r r i e d out l o n g - t e r m (up t o 12 months) f e e d i n g e x p e r i m e n t s o f browned egg a l b u m i n w i t h r a t s . Several changes were f o u n d , b u t no m u t a g e n i c r e s p o n s e was o b s e r v e d . The

M a i l l a r d Reaction i n Vivo

A s i m p l e s k e t c h i s g i v e n a l o n g t h e l i n e s o f two r e c e n t r e v i e w s (^2> 73_). B o r s o o k , e t a l . (74) o b s e r v e d t h e o c c u r r e n c e of A m a d o r i compounds i n v i v o , w h i c h were c o n f i r m e d by Heyns and P a u l s e n (75) t o be 1-deoxy-l-N-aminoacy1-D-fructose derivatives. F e e n e y , e t a _ l . (76) i n c u b a t e d g l u c o s e w i t h egg w h i t e a t 37°C f o r a few days and o b s e r v e d t h e d i s a p p e a r a n c e o f glucose. H o l m q u i s t and S c h r o e d e r (JJ) f i r s t showed t h a t t h e N - t e r m i n a l v a l i n e of H b - A - l - c was b l o c k e d and s u b s e q u e n t r e s e a r c h e r s showed t h e o c c u r r e n c e o f A m a d o r i r e a r r a n g e m e n t o f an a l d o s y l a m i n e , N - ( 1 - d e o x y g l u c o s y l ) v a l i n e . Rahbar (78) d i s c o v e r e d an i n c r e a s e i n t h e m i n o r h e m o g l o b i n component, Hb-A-l-c, i n the blood of d i a b e t i c p a t i e n t s .


MAILLARD REACTIONS

T a n z e r (7_9) o b s e r v e d the p r e s e n c e of t h e r e d u c e d f o r m of t h e A m a d o r i compounds formed w i t h h y d r o x y l y s i n e and reducing s u g a r s i n aged c o n n e c t i v e t i s s u e s . M e s t e r , e_t a l _ . (80) s u g g e s t e d the f o r m a t i o n of A m a d o r i compounds i n the b l o o d f r o m g l u c o s e and l y s i n e - r i c h p r o t e i n o r s e r o t o n i n e . C e r a m i , eit 3^.(81) showed t h a t i n d i a b e t e s m e l l i t u s s t r u c t u r a l p r o t e i n s of t h e l e n s m i g h t be a f f e c t e d by h i g h g l u c o s e c o n c e n t r a t i o n t o induce c a t a r a c t through Amadori-type r e a c t i o n . It is likely t h a t t h i s k i n d of s t u d y has not been made by J a p a n e s e w o r k e r s .


M a i l l a r d Reaction i n R e l a t i o n to L i p i d s L i p i d s upon a u t o x i d a t i o n p r o d u c e c a r b o n y l compounds, w h i c h r e a c t w i t h amino compounds t o f o r m brown h i g h - m o l e c u l a r products. T h i s t y p e of b r o w n i n g has r e c e n t l y been r e v i e w e d by P o k o r n y (82^). A c c o r d i n g t o him the f i r s t p a p e r on the s u b j e c t was p u b l i s h e d by S t a n s b y ( 8 3 ) . F u j i m o t o , e t a l . (84-89) s t u d i e d t h i s r e a c t i o n w i t h some f i s h and r e p o r t e d t h a t most brown p i g m e n t of f i s h m u s c l e was s o l u b l e i n b e n z e n e - m e t h a n o l . Thus i n t h i s c a s e o x i d i z e d l i p i d - p r o t e i n i n t e r a c t i o n s a r e more i m p o r t a n t t h a n the r e a c t i o n between amino a c i d s and r i b o s e . In f i s h m u s c l e the b r o w n i n g due t o o x i d i z e d l i p i d s i s a c c o m p a n i e d by the M a i l l a r d r e a c t i o n between amino a c i d s and r i b o s e . In t h i s c o n n e c t i o n i t i s i n t e r e s t i n g t o n o t e an e a r l i e r g a p e r by T a r r ( 3 0 ) , who r e p o r t e d t h a t upon h e a t i n g 1 h r a t 120 C h a l i b u t browned s l i g h t l y whereas l i n g c o d d a r k e n e d m a r k e d l y and t h a t f r e e r i b o s e was d e t e c t e d i n the l a t t e r f i s h m u s c l e . M a i l l a r d r e a c t i o n p r o d u c t s have a n t i o x i d a n t a c t i v i t y ( 9 0 , 91). F r a n z k e and I w a i n s k y (92) f i r s t r e p o r t e d t h i s a c t i v i t y of melanoidins. P a t t o n (93) n o t e d the c o n t r i b u t i o n of the M a i l l a r d r e a c t i o n i n p r e v e n t i n g d r y m i l k powder f r o m o x i d a t i o n . G r i f f i t h and J o h n s o n (94) showed t h a t the p r o d u c t s from r e a c t i o n of g l u c o s e and g l y c i n e e x h i b i t e d a n t i o x i d a t i v e p r o p e r t i e s i n model s y s t e m w i t h l a r d . The a n t i o x i d a t i v e p r o p e r t i e s were a t t r i b u t e d t o r e d u c t o n e s and t h i s was p r o v e d by E v a n s , et_ a l . ( 9 5 ) . Z i p s e r and W a t t s (£6) r e p o r t e d t h a t s t e r i l i z a t i o n o f meat p r o d u c e d a n t i o x i d a t i v e compounds by t h e Maillard reaction. Y a m a g u c h i , e_t a_l. (91) as w e l l as K i r i g a y a , e t a l . (98) made e x t e n s i v e s t u d i e s c o n c e r n i n g t h i s p r o b l e m . E i c h n e r (90) s t u d i e d i n t e r m e d i a t e r e d u c t o n e - l i k e compounds as antioxidants. Y a m a g u c h i , e t a l . (99) f r a c t i o n a t e d the r e a c t i o n p r o d u c t s o b t a i n e d by h e a t i n g D - x y l o s e and g l y c i n e and f o u n d s t r o n g a n t i o x i d a t i v e a c t i v i t y i n some m e l a n o i d i n f r a c t i o n s . Studies

on

Soy

Sauce

Soy sauce i s u s e d e v e r y day by J a p a n e s e p e o p l e . It is a f e r m e n t e d p r o d u c t made f r o m steamed s o y b e a n s , p a r c h e d w h e a t , and s a l t . I t has a s p e c i a l l y p l e a s a n t f l a v o r and a deep but attractive color. I t i s now known t h a t the c o l o r of f r e s h soy


KAWAMURA


11


sauce i s formed c h i e f l y by the ordinary M a i l l a r d r e a c t i o n , whereas the undesirable dark c o l o r of soy sauce stored i n contact with atmospheric oxygen i s produced not only by the advanced M a i l l a r d r e a c t i o n but a l s o and more pronouncedly by o x i d a t i v e browning r e a c t i o n . The pigments of soy sauce, f i r s t studied by Kurono and Katsume (100), are melanoidins, which were reported by Omata, et a l . (101) to be produced from the r e a c t i o n of sugars and amino a c i d s . Kato, e_t a_l. ( 102) found 3-deoxyglucosone as an intermediate i n browning of soy sauce ( c f . 103). Oxidative browning (104,105) was again reviewed (44) with emphasis on the browning of Amadori compounds and i n t e r a c t i o n between melanoidins and i r o n . Studies on Dried Milk

Products

One of the e a r l i e r reviews (31) concerned the M a i l l a r d r e a c t i o n i n d r i e d milk during storage. Spray-dried whey has considerable amounts of lactose and p r o t e i n r i c h i n l y s i n e . T h e o r e t i c a l treatment of the problem i n whey powder was the object of recent studies by Labuza and Saltmarch (106, 107). When the whey powders are stored at a^ (water a c t i v i t y ) 0.33, 0.44, and 0.65, p r o t e i n q u a l i t y loss and browning extent were greatest not at 0.65 but at 0.44, where amorphous lactose began to s h i f t to the alpha-monohydrate c r y s t a l l i n e form with a release of water which mobilized reactants f o r the M a i l l a r d r e a c t i o n (106). This type of research was continued with s p e c i a l reference to temperature c o n d i t i o n s . The temperatures used were f a i r l y constant at 25, 35, and 45°C or f l u c t u a t i n g between 2 5 ° and 45 °C with a l t e r n a t i n g 5-day periods at each temperature. Experiments were c a r r i e d out f o r 100-200 days. Temperature h i s t o r y , however, d i d not s i g n i f i c a n t l y change r e a c t i o n mechanisms (107). Acknowledgments Thanks are due to Prof. George R. Waller for h i s kind cooperation. Professor Hiromichi Kato of the U n i v e r s i t y of Tokyo and Professor Mitsuo Namiki of Nagoya U n i v e r s i t y provided information on many valuable references. The author i s g r a t e f u l to them and several other colleagues. Literature cited Chem. Abstr.) 1. 2.

3.

(The

titles

of

articles

are included.

CA:

Kawamura, S. S i x t y years of the M a i l l a r d Reaction. Shokuhin Kaihatsu 1972, 7 (12), 64-5. M a i l l a r d , L.-C. A c t i o n des acides amines sur l e s sucres: Formation des melanoidines par voie methodique. C. R. Hebd. Seances Acad. S c i . 1912, 154, 66-8. M a i l l a r d , L.-C. Condensation des acides amines en presence de l a g l y c e r i n e ; C y c l o g l y c y l g l y c i n e et


12

MAILLARD REACTIONS

4.

5. 6.


7.

8.

9.

10.

11.

12. 13.

14.

15.

16.

17.

18.

19.

polypeptides. C. R. Hebd. Seances Acad. S c i . 1911, 153, 1078-80. M a i l l a r d , L.-C. Formation d'humus et de combustibles mineraux sans i n t e r v e n t i o n de l'oxygene atmospherique, des microorganismes, des hautes temperatures, ou des f o r t e s p r e s s i o n s . C. R. Hebd. Seances Acad. S c i . 1912, 155, 1554-6. L i n g , A. R. M a l t i n g . J . I n s t . Brew. 1908, 14, 494-521. L i n t n e r , C. J . Ueber Farbe- und Aromabildung im Darrmalz. Z. Gesamte Brauwes. 1912, 35, 545-8, 553-6. Strahlmann, H. Louis Camille M a i l l a r d (1878-1936) und die nach ihm benannte Braeunungsreaktion. Alimenta 1978, 17 (5), 144, 146. P i c t e t , Α.; Chou, T. Q. La formation des bases pyridiques et isoquinoleiques a p a r t i r de l a caseine. C. R. Hebd. Seances Acad. S c i . 1916, 162, 127-9. M a i l l a r d , L.-C. Sur l a formation des bases pyridiques a p a r t i r des albuminoides. C. R. Hebd. Seances Acad. Sci. 1916, 162, 757-8. M a i l l a r d , L.-C. Origines des bases c y c l i q u e s du goudron de h o u i l l e . C. R. Hebd. Seances Acad. S c i . 1913, 157, 850-2. M a i l l a r d , L.-C. "Genese de Matieres Proteiques et des Matieres Humiques"; Masson et C i e : P a r i s , 1913; CA 8, 1594. Achard, Ch. Deces de M. Louis M a i l l a r d . C. R. Hebd. Soc. B i o l . 1963, 122, 347-8. M a i l l a r d , L.-C. Synthese des peptides i n f e r i e u r s par une methode nouvelle et d i r e c t e , v o i s i n e des r e a c t i o n b i o l o g i q u e . C. R. Hebd. Seances Mem. Soc. B i o l . 1911, 71, 546-9. M a i l l a r d , L.-C. Synthese des polypeptides par a c t i o n de l a g l y c e r i n e sur l e g l y c o c o l l e . Ann. Chim. ( P a r i s ) , 1914, (9) 1, 519-78. M a i l l a r d , L. C. Synthese des polypeptides par a c t i o n de l a g l y c e r i n e sur l e g l y c o c o l l e : Etude dynamique. Ann. Chim. ( P a r i s ) , 1914, (9) 2, 210-68. M a i l l a r d , L.-C. Les c y c l o - g l y c y l - g l y c i n e s : Synthese d i r e c t e par a c t i o n de l a g l y c e r i n e sur l e s acides amines. Ann. Chim. ( P a r i s ) , 1915, (9) 3, 48-120. M a i l l a r d , L.-C. Synthese des c y c l o - g l y c y 1 - g l y c i n e mixtes par a c t i o n de l a g l y c e r i n e sur l e s melanges d'acides α-amines. Ann. Chim. ( P a r i s ) , 1915, (9) 3, 225-52. M a i l l a r d , L.-C. Reaction generale des acides amines sur les sucres: Ses consequences b i o l o g i q u e s . C. R. Hebd. Seances Mem. Soc. Biol., 1912, 72, 559-601. M a i l l a r d , L.-C. Formation des matieres humiques par a c t i o n de polypeptides sur l e s sucres. C. R. Hebd. Seances Acad. S c i . 1913, 156, 1159-60.


1. KAWAMURA 20. 21. 22.


23. 24. 25. 26. 27. 28. 29. 30. 31. 32. 33. 34. 35. 36. 37.


13

Maillard, L.-C. Syntheses des matieres humiques par action des acides amines sur les sucres reducteurs. Ann. Chim. (Paris), 1916, (9) 5, 258-317. Maillard, L.-C. Identité des matieres humiques de synthese avec les matieres humiques naturelles. Ann. Chim. (Paris) 1917, (9) 7, 113-52. Kato, H. Chemistry of nonenzymatic browning phenomena. "Shokuhin no Henshoku to Sono Kagaku (Food Discoloration and Its Chemistry)"; Nakabayashi, T., Kimura, S.; and Kato, H., Eds.; Korin Shoin: Tokyo, 1967; pp. 223-89. Reynolds, T. H. Chemistry of nonenzymic browning. I. The reaction between aldoses and amines. Adv. Food Res. 1963, 12, 1-52. Reynolds, T. H. Chemistry of nonenzymic browning. II. Adv. Food Res. 1965, 14, 167-283. Ellis, G. P. The Maillard reaction. Adv. Carbohydr. Chem. 1959, 14, 63-134. Heyns, K.; Paulsen, H. Ueber die chemische Grundlagen der Maillard-Reaktion. Wiss. Veroeff. Deutsch. Ges. Ernaehr. 1960, 5, 15-42. Thompson, J . B. A browning reaction involving copper-proteins. "Symposium on Copper Metabolism;" Johns Hopkins Press, 1950, pp. 141-53; CA 47, 11269f. Patron, A. Recherches sur le brunissement nonenzymatique des fruits et des produits de fruits en conserve. Fruits Outre Mer 1950, 5, 201-7; CA 44, 10204d. Geoffrey, R. The Maillard reaction in the cereal industry. Bull. Anc. Eleves Ec. Fr. Meun. 1953, (138), 260; CA 48, 7807a. Tarr, H. L. A. Ribose and the Maillard reaction in fish muscle. Nature 1953, 171, 344-5; CA 47, 5973i. Lange, P. de. Decrease of solubility and nutritive value of milk powder during storage. Conserva 1954, 2, 322-5; CA 48, 7808a. Wegner, H. The Maillard reaction and yellowing of starch sirup. Staerke 1954, 6, 5-10; CA 48, 6150d. Patron, A. La "Reaction de Maillard" et le brunissement non-enzymatique dans les industries alimentaires. Ind. Agric. Aliment. 1951, 68, 251-6; CA 46, 4687f. Barnes, H. K.; Kaufman, C. W. Industrial aspects of browning reaction. Ind. Eng. Chem. 1947, 39, 1167-70. Seaver, J . L . ; Kertesz, Ζ. I. "Browning (Maillard) reaction" in heated solutions of uronic acids. J . Am. Chem. Soc. 1946, 68, 2178-9. Ruckdeschel, W. Ueber Melanoidine und ihr Vorkommen in Darrmalz. Z. Gesamte Brauwes. 1914, 37, 430-2, 437-40. Danehy, J . P.; Pigman, W. W. Reactions between sugars and nitrogenous compounds and their relationship to certain food problems. Adv. Food Res. 1951, 3, 241-90.


14

MAILLARD REACTIONS

38. 39. 40. 41. 42.


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Seventy Years of the Maillard Reaction - American Chemical Society

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