BLBS102-c10 BLBS102-Simpson March 21, 2012 13:7 Trim: 276mm X 219mm Printer Name: Yet to Come
10 Protein Cross-linking in Food – Structure, Applications, Implications for Health and Food Safety 211been identified, including those shown in Figure 10.2 (Ames
1992, Hill et al. 1993, Easa et al. 1996a, 1996b, Gerrard et al.
1998a, 1999, 2002a, 2003a, 2003b, Hill and Easa 1998, Fayle
et al. 2000, 2001, Mohammed et al. 2000). One of the first
protein-derived Maillard reaction products (MRPs) isolated and
characterised was the cross-link pentosidine (Sell and Monnier
1989, Dyer et al. 1991), a fluorescent moiety that is believed
to form through the condensation of a lysine residue with an
arginine residue and a reducing sugar. The exact mechanism
of formation of pentosidine remains the subject of considerable
debate (Chellan and Nagaraj 2001, Biemel et al. 2001).
Some of the earliest studies that assessed the effect of pro-
tein cross-linking on food quality examined the digestibility of a
model protein following glycation. Kato et al. (1986a) observed
that following incubation of lysozyme with a selection of dicar-
bonyl compounds for 10 days, the digestibility of lysozyme by a
pepsin-pancreatin solution was reduced to up to 30% relative to
the non-glycated sample. This trend of decreasing digestibility
was concomitant with an observed increase in cross-linking of
lysozyme. The increased resistance of cross-linked proteins to
enzymes commonly involved in the digestion of proteins in the
body is unfavourable from a nutritional standpoint. It has also
been reported that the digestion process can be inhibited by the
Maillard reaction (Friedman 1996b).AGE PROTEIN CROSS-LINKS ISOLATED
TO DATE IN FOODInformation regarding the presence of specific Maillard protein
cross-links in food is, to date, limited, with only a handful of
studies in this area (Henle et al. 1997, Schwarzenbolz et al. 2000,
Biemel et al. 2001). For example, compared with the extensive
literature on the Maillard chemistry in vivo, relatively little has
been reported on the existence of pentosidine in food. In a study
by Henle et al. (1997), the pentosidine content of a range of
foods was examined, with the highest values observed in roasted
coffee. Overall concentrations, however, were considered low,
amongst most of the commercial food products tested. It was,
therefore, concluded that pentosidine does not have a major role
in the polymerisation of food proteins. Schwarzenbolz et al.
(2000) showed that pentosidine formation in a casein-ribose
reaction is carried out under high hydrostatic pressure, which
could be relevant to some areas of food processing. Iqbal et al.
have investigated the role of pentosidine in meat tenderness in
broiler hens (Iqbal et al. 1997, Iqbal et al. 1999a, 1999b, Iqbal
et al. 2000).
Other Maillard cross-links have recently been detected in
food, and attempts have been made to quantify the levels found.
Biemel et al. (2001) examined the content of the lysine–arginine
cross-links, GODIC, MODIC, DODIC and glucosepane in food.
These cross-links were found to be present in proteins extracted
from biscuits, pretzels, salt stick and egg white in the range
of 7–151 mg/kg. The lysine–lysine imidazolium cross-links
MOLD and GOLD were also isolated but were present at a
lower concentration than MODIC and GODIC.HEALTH AND FOOD SAFETY ASPECTS
OF MRPSThe complexity of the Maillard reaction means that during any
cross-linking reaction in the food matrix, a variety of other prod-
ucts are likely to form. Over the last decade, there has been an on-
going debate over the health and safety impacts of dietary MRPs,
particularly advanced glycation end products (AGEs) generated
in the later stages of the Maillard reaction in foods, with regards
to their potential risks and/or benefits towards human health
when consumed in the diet. To date, numerous research groups
have argued that MRPs pose a risk to human health, particularly
certain heterocyclic products, when consumed in the diet (Felton
and Knize 1998, Faist and Erbersdobler 2002, Shin 2003, Shin
et al. 2003, Bordas et al. 2004, Murkovic 2004, Taylor et al.
2004, Sebekova and Somoza 2007, Garcia et al. 2009). Other
research has provided evidence to the contrary, highlighting the
potential of MRPs to act as antioxidants or have other beneficial
effects (Manzocco et al. 2000, Faist and Erbersdobler 2002, Lee
and Shibamoto 2002, Morales and Babbel 2002, Dittrich et al.
2003, Morales and Jimenez-Perez 2004, Ames 2007), with a
few groups considering both the positive and negative effects of
MRPs when consumed in the diet (Faist and Erbersdobler 2002,
Somaza 2005, Gerrard 2006, Henle 2007).
This ongoing debate was discussed by Henle (2007) in a
review paper, in which he explored whether dietary MRPs are a
risk to human health based on the arguments from two prominent
papers on the topic by Ames (2007), who provided evidence
against the MRPs being a risk to human health, and Sebekova
and Somoza (2007), who argued the opposite. Both sides of the
debate are outlined here.
Sebekova and Somoza (2007) argued that there was sufficient
evidence concerning the negative impact of dietary AGEs on
health. Their argument is based on research from both experi-
mental studies in rodents and clinical studies in humans, includ-
ing healthy people and those suffering from diseases that are
associated with AGEs, such as diabetes and cardiovascular dis-
ease. Their analysis of the current literature revealed that a high
intake of thermally processed foods in the diet may have signif-
icant nephrotoxic effects, aggravate low levels of inflammation
and exert oxidative stress. There is also significant evidence to
show that a high AGE-diet can influence the development of
complications that are associated with diabetes and have detri-
mental effects on, for example, wound healing (Peppa et al.
2003, 2009) and atherosclerois (Lin et al. 2003, Walcher and
Marx 2009). This is supported by further studies that show po-
tential negative effects of an AGE-rich diet to health. The first
of these studies was an animal study in which Wistar rats were
fed either an AGE-rich diet or an AGE-poor diet over a 6-week
period, where wheat starch was replaced by bread crusts (Se-
bekova et al. 2005, Somoza et al. 2005). The results obtained
were interesting, with the rats on the AGE-rich diet gaining
weight more rapidly than those on the AGE-poor diet, with a
trend towards higher glucose and albumin levels. There was also
noticeable weight gain in specific organs such as the heart, kid-
ney, liver and lungs, but not the spleen, intestine or brain. These
results suggest the idea that some organs are more susceptible to