Journal of Cereal Science 60 (2014) 540e548
Contents lists available at ScienceDirect
Journal of Cereal Science
journal homepage: www.elsevier.com/locate/jcs
Review
How can both the health potential and sustainability of cereal
products be improved? A French perspective
Anthony Fardet*
INRA, UMR 1019, UNH, CRNH Auvergne, F-63000 CLERMONT-FERRAND & Clermont Universit
e, Universit
e d'Auvergne, Unit
e de Nutrition Humaine,
BP 10448, F-63000 Clermont-Ferrand, France
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 21 April 2014
Received in revised form
25 July 2014
Accepted 26 July 2014
Available online 16 September 2014
A more sustainable cereal sector would preserve the environment (environmental sustainability) and
promote health (physiological sustainability) at a price that is acceptable to consumers regardless of their
social status (socio-economic sustainability). The health potential of cereal products can be improved
throughout the cereal sector via a more integrative approach based on reverse engineering. Globally,
whole-grain products that contain less sugar, fat and salt must be developed. Therefore, the first main
point is to fully understand the consumers' acceptance of such new cereal products of higher nutritional
value. Then, levers and locks at the technological, agricultural and genetic selection levels must be
identified. Recent literature reviews and Committee reports emphasised the importance of preserving
the structure of cereal foods via less drastic hydrothermic and mechanical processes and greater use of
pre-fermentation and/or germination processing. The results of more human intervention studies are
required to fill the gap between those obtained from observational and mechanistic/animal studies,
notably, in reaching a conclusion regarding the health-promoting antioxidant potential of whole-grain
cereal products. However, genetic selection faces the constraints of preserving both high yields and
high levels of protective bioactive compounds. In conventional agriculture, one important issue is the
accumulation of pesticides in the outer fractions of grains, which affects the development of whole-grain
products. Although organic agriculture does not seem to provide a significant improvement in nutritional
value, this practice is clearly more sustainable in terms of environmental protection. In conclusion, the
improvement of the nutritional value of cereal products in the framework of a sustainable development
should involve the concerted contribution of different actors of the sector.
© 2014 Elsevier Ltd. All rights reserved.
Keywords:
Cereal health potential
Sustainability
Cereals sector
1. Introduction
Certain practices affect the nutritional quality of cereal products,
including the refining and fractionation processes applied to the
raw material and the addition of sugar, salt and fat in product formulations. During refining, the components of high-nutritional
value that are contained in the bran and germ fractions, such as
fibre, micronutrients and protective phytochemicals, are stripped
from the grains; whereas the addition of salt, sugar and fat causes
public health problems, such as the increased prevalence of obesity,
type 2 diabetes, cardiovascular diseases and cancers. A typical
example is childrens' breakfast cereals, which are usually made
from refined grains (with very few protective micronutrients) that
are extruded under stringent conditions (causing a high glycaemic
* Tel.: þ33 473624704; fax: þ33 473624755.
E-mail address: [email protected].
http://dx.doi.org/10.1016/j.jcs.2014.07.013
0733-5210/© 2014 Elsevier Ltd. All rights reserved.
index) and are high in sugars and fats (risk factors for the development of overweight and obesity) (Lioger et al., 2007).
In addition to addressing problems caused by the accumulation
of contaminants (including mycotoxins and insecticidal residues) in
the outer layers of the grain, the proponents of non-refining or less
intensive refining must also address the question of the acceptability of whole-grain and partly refined flours from digestive and
taste perspectives. The challenge for the cereal sector is to maintain
the organoleptic properties and safety of cereal products while
improving their nutritional quality.
With the objective to develop sustainable diet, several questions
must be addressed at the different levels of the cereal sector, as
follows: 1) at the level of agricultural production, can we select
genetic varieties that are the richest in protective micronutrients or
use cereal varieties that are very little cultivated currently but are
rich in the nutrients of interest while maintaining a satisfactory
yield? Can we use cultivation practices that are more protective of
the environment and at the same time ensure the nutritional value
A. Fardet / Journal of Cereal Science 60 (2014) 540e548
of cereals? Are the increased yields necessary to feed a growing
population compatible with maintaining a satisfactory level of
protective micronutrients? 2) At the level of first transformation,
what degree of flour refining should be achieved to maintain both
good acceptability and good nutritional quality of cereal products?
Can we generalise the techniques for isolating the aleurone layer
(rich in lysine and protective micronutrients but also in potential
allergens) and systematise the fortification of grain products using
this fraction (Brouns et al., 2012; Hemery et al., 2007)? How can we
make better use of the germ fraction? 3) At the level of the second
transformation, can we develop “softer” technologies for formulating grain products? Can we reduce the levels of sugar, salt and fat
from a technological point of view (Poutanen et al., 2014)? 4) In
terms of consumption, are consumers' tastes likely to evolve toward cereal products that are less refined and are less rich in sugar,
salt and fat than current cereal products? In other words, a more
sustainable cereal sector must preserve the environment (environmental sustainability), human health (physiological sustainability) and cultural habits (cultural sustainability) at a price that is
acceptable to the consumer regardless of his or her socio-economic
status (socio-economic sustainability).
The main objective of this review is to discuss the possible improvements in the health potential of cereal products that could be
made throughout the entire sector, from “field to plate” by adopting
a more holistic and integrative perspective.
2. State of the art and current investigations
What is known about the health potential and health effects of
grain products? This topic has been thoroughly covered by many
€rck et al., 2012; Borneo and Leon, 2012; Fardet, 2010;
reviewers (Bjo
Frølich et al., 2013; Gibson et al., 2013; Poutanen, 2012). Based on a
recent review of the literature, the issues described below deserve
emphasis in future study.
541
vitamins (Laerke and Knudsen, 2011). The considerations for flour
refining, other than the considerable reduction of the content of
phytochemicals, involve the amount of fibre, which is contained
mainly in the outer layers, and which is also important because
numerous phytochemicals are associated with the fibre fraction,
i.e., they are “fibre co-passengers” (Fardet, 2010; Jones, 2010; Laerke
and Knudsen, 2011; Vitaglione et al., 2008). Increasing the fibre
intake is strongly encouraged as part of the recommendations of
(PNNS) (Ministe
re
the French Programme National Nutrition Sante
, 2011). Thus, there is a strong
du Travail, de l'Emploi et de la Sante
temptation to systematically enrich refined cereal products with
fibre extracts rather than using more wholemeal flours. However,
whether or not the fibre extracts are as beneficial to health as the
fibres that are natural components of the whole grain remains
largely unexplored. Adding fibres may be a solution that would
reduce the gap between the recommended intake and the actual
fibre consumption. However, fibre isolates generally lack the phytochemicals present in whole grains that can provide additional
potential health benefits (Smith and Tucker, 2011). In addition, the
health implications of the widespread use of fibre extracts are not
clear (Laerke and Knudsen, 2011).
Regarding the salt, refined fat and sugar that are added to cereal
products, the health effects are more obvious; too much salt intake
can cause hypertension, whereas the excessive intake of sugars and
fat is a risk factor for cardiovascular disease, obesity, type 2 diabetes
and certain cancers. Incidentally, the presence of rapidly bioavailable sugars in very refined and processed cereal products is also a
risk factor for the development of type 2 diabetes. However, the
addition of salts is primarily an issue for the baking industry, with
bread being one of the main sources of added salt in France (i.e.,
z25% of total daily consumed salt) (Afssa, 2002), and the addition
of fats and sugars is relevant mainly for the biscuit and breakfast
cereal industries.
2.2. The importance of the physical structure of cereal products
2.1. Health effects of whole-grain versus refined cereals and of
highly versus slightly processed cereal products
Overall, whereas the regular high consumption of more or less
whole-grain products is associated with a lower prevalence of
overweight/obesity, type 2 diabetes, cardiovascular disease and
certain gastrointestinal cancers, the reverse was observed for the
consumption of refined grain products e although there are fewer
studies of the latter e and many studies have shown only a lack of
association (Fardet and Boirie, 2014). For example, a recent metaanalysis showed a significantly higher (þ27%) prevalence of type
2 diabetes in the highest consumers of white rice (Hu et al., 2012).
The same result was obtained in a previous pooled analysis (17%),
which also showed that the prevalence of type 2 diabetes was
significantly lower among the highest consumers of unrefined
-vis
brown rice (11%) (Sun et al., 2010). The protective effect vis-a
type 2 diabetes could be more related to the bran fraction rather
than the germ fraction (Sun et al., 2010).
Concerning intervention studies, all researchers agreed that
there is a great need for more studies to identify a direct causal role
of phytochemicals in the metabolic health benefits of whole-grain
cereal and in their ability to mitigate the progression of chronic
diseases (Belobrajdic and Bird, 2013; Giacco et al., 2011; Smith and
Tucker, 2011). For example, the high antioxidant potential of cereal
products as measured in vitro has not been convincingly confirmed
in vivo in humans (Fardet et al., 2008; Price et al., 2012).
Refining grains causes considerable losses of the micronutrients,
phytochemicals and fibre fractions that are concentrated in the
bran and germ (Fardet, 2010). For example, refining wheat flour at
less than a 70% extraction rate causes the loss of 60e90% of the B
The physical structure of grain products is increasingly recognised as a parameter governing the health benefits of whole-grain
products because it affects the prolonged feeling of satiety (limiting
snacking between meals) and the gradual release of nutrients,
including that of glucose from the digestion of starch, such as in the
case of pasta (Fardet, 2010; Fardet et al., 1998, 2013). Although
cereal grain processing is indispensable for producing the final
physiological and health effects (Frølich et al., 2013), highly processed grain products generally have a less compact physical
structure and therefore are less satiating (Abou Samra et al., 2008;
Isaksson et al., 2011, 2012); for example, minimally processed lowglycaemic index (GI) muesli-type breakfast cereals are more satiating than are highly processed extruded high-GI breakfast cereals
(Brand-Miller et al., 2002). However, optimising the satiation effect
is not sufficient if acceptability and enjoyment are not achieved
(Villemejane et al., 2012, 2013).
2.3. Can behaviours be changed?
Around the issues regarding wholemeal flours and more
particularly the issue of reducing sugar, salt and fat contents, the
acceptability of products by consumers is important.
Some recent surveys provided insight into the acceptability of
less refined grain products. In the first survey, Saulnier and Micard
reported: “The criteria for consumer preference are not always
compatible with the technological innovations developed to meet
the nutritional recommendations” (page 7) (Saulnier and Micard,
2012). For example, introducing fibre to French baguette reduced
their visual acceptability, and acceptability after tasting was
542
A. Fardet / Journal of Cereal Science 60 (2014) 540e548
preserved only for certain products, e.g., French traditional baguettes. Second, as part of the HealthGrain project, a survey of the
health and hedonic expectations of consuming bread, pasta and
biscuits made from whole-grain or refined flour was conducted
among consumers in Germany, Finland, Great Britain, and Italy
(Shepherd et al., 2012). The results showed that there was a difference in perception among the consumers from different countries, for example, the health benefits of whole-grain products are
highly apparent in Finland while quite a few of them in Italy are
hardly known. Globally, women and the elderly have a more positive perception of whole grains, and modifications in bread and
pasta products are better received than are modifications in biscuits. Finally, the pleasure in consumption, the perceived health
benefits and health-based motivations are the main criteria that
appear to affect the acceptability of whole-grain-rich products
(Saulnier and Micard, 2012). In an explorative study of whole-grain
perception, the participants were generally aware of the term
‘whole grain’, but many key barriers to whole-grain consumption
were still evident. Nevertheless, in addition to educational efforts,
the agro-food industry has quite a few possibilities “to develop
novel, but affordable, food products that are able to deliver whole
grains in a wide variety of forms, including whole grains ‘in
disguise’ for those who are most resistant to change” (page 743)
(McMackin et al., 2013).
Thus, it is interesting to note that in Denmark, whole-grain
consumption increased 72% between 2011 and 2013 (The Whole
Grains Council, 2013). The Danes were already consuming 32 g of
whole grains a day in mid-2011, and now they are ingesting up to
55 g a day on average. The Danes attribute this large increase to
manufacturers providing better products and the presence of a
packaging symbol that identifies those products. The study indicated that Danes do not eat more bread and grain products than
they did previously, but that the increase is because foods like
coarse wheat bread and pasta contain more whole grains at present. Furthermore, it has become easier to choose whole-grain
products.
Beyond the sensory perception of less refined grain products
is the question of whether the consumption of products of plant
origin has tended to increase. The study of Dubuisson et al.
indicated that an evolution in the consumption of cereals by the
French population occurred between 1998e1999 (INCA1 study)
and 2006e2007 (INCA2 study); in men and women in the 18e34,
35e54 and 55e79 year age groups, a reduction in the consumption of breads and bread-derived products from 6 to 21%
was observed (depending on sex and age), with pasta consumption changing from 10% (women aged 35e54) to þ25%,
rice and wheat consumption changing from 6 (women aged
18e34) to þ44%; and breakfast cereal consumption increasing
from þ9 to þ57%; and pizza and pastry consumption changing
from 8 (women aged 35e54) to þ33% (Dubuisson et al., 2009).
Otherwise, the overall consumption of starchy foods remained
constant, with traditional starchy foods, such as bread and potatoes, partially replaced by pasta, rice and wheat (Dubuisson
et al., 2009). The stability in the rate of consumption of fish
and cereal-based foods, the increased consumption of fruit and
vegetables and the decreased consumption of meat, dairy products and sugary foods in France is similar to the trends in the
Nordic countries (Dubuisson et al., 2009). There was therefore a
tendency toward the increased consumption of grain products
(including breakfast cereals), fruits and vegetables and the
decreased consumption of products of animal origin, including
meat, milk, eggs and cheese (Dubuisson et al., 2009). If this trend
of increased consumption of grain products continues as it has
since 2007, the development of a more varied range of wholegrain products may accompany it.
Finally, although it is difficult to obtain accurate statistics on the
percentage of vegetarians and vegans in France, the change in this
population over 10 years indicates the evolution toward the
increased consumption of more or less plant-based products. The
total number of vegetarians is estimated to be approximately 2% in
France (compared with 40% in India). In the issue of 24 May 2012,
the French magazine Terra Eco noted “The number of members of
the French Vegetarian Association has doubled in three years”
(http://www.terraeco.net/). There is very little data available
regarding the vegan population.
2.4. Genetic and environmental factors
Plant breeding projects have been conducted within the
framework of European research programs to study the genetic
and agronomic variability related to the components of the
germ, the aleurone layer and other peripheral portions of grains
(Andersson et al., 2010; Fernandez-Orozco et al., 2010; Kariluoto
et al., 2010; Lampi et al., 2010; Nurmi et al., 2010a, 2010b; Oury
et al., 2006; Poutanen et al., 2010; Shewry et al., 2012, 2010a,
2010b). The levels of certain wheat micronutrients, particularly
minerals, depend on the genetic origin (magnesium), the agronomic conditions (zinc) and often, interaction between these
factors (iron) (Oury et al., 2006). However, programs for the
fortification of wheat with iron and zinc exist at the international level (CIMMYT) to overcome the nutritional deficiencies in
some of the developing countries. It was also shown that the
fibre content and fibre composition (insoluble/soluble ratio)
depend on the genetic and agro-environmental conditions
(Shewry et al., 2010a; Abecassis and Rousset, 2012). However,
the content of soluble fibre (mainly arabinoxylans in wheat) is a
highly heritable character (Charmet et al., 2012), i.e., it can be
improved by genetic means. However, if this improvement were
accompanied by a reduction in the yield or the baking properties
of traditional bread, the high-fibre varieties of bread would only
be valued in niche markets, which would not attract private
breeding companies. In the case of other micronutrients,
particularly vitamins and antioxidants, some have a range of
heritability (Shewry et al., 2010a,b) and the difficulty for the
breeder lies in the expectations of nutritionists: indeed, selecting
a particular nutrient may have no meaning in preventive nutrition because it is the totality of bioactive compounds (“cocktail”)
that is health-protective via synergistic activities (Fardet, 2010).
It therefore seems better to seek grain varieties with a good
balance of numerous protective compounds and to promote
genetic diversity e a guarantor of this balance - rather than
selecting varieties with only a few beneficial compounds. First, it
will be interesting to determine a posteriori if intensive selection
for yield caused a corresponding decrease in the overall micronutrient content, which appears to occur due to the ‘dilution’
effect (following a better ability of the grain to accumulate grain
starch) (Shewry et al., 2011).
2.5. Transformation processes
Cereal grains cannot be consumed as such by humans and
therefore grain-transformation processes are essential; however,
these processes can either improve or reduce the nutritional quality
of cereal products, depending on their intensity and nature. For
example, pasta formatting renders starch slowly digestible (Fardet
et al., 1998), which is very beneficial for health, whereas drastic
extrusion processes burst the initial structure of grains and produce
highly gelatinised starch that is rapidly digestible, as is the case for
some types of breakfast cereals made for children (Foster-Powell
and Miller, 1995).
A. Fardet / Journal of Cereal Science 60 (2014) 540e548
The nutritional value of cereal products may be increased
either through using flours that have been extracted less (i.e.,
more or less whole-grain flours) or by re-incorporating cereal
fractions with a high nutritional density, such as aleurone-layerrich fractions. For example, research to improve the dryfractionation processes for grain has led to proposals of ways
to improve the composition of flours through increasing their
content of constituents from the aleurone layer (Hemery et al.,
2007; Delcour et al., 2012). However, the question of the relative energy costs and sustainability arises when comparing dry
fractionation processes to isolate aleurone-rich fractions vs
classical milling processes to directly obtain flours of a lower
extraction level; we are currently unable to answer this question, which probably depends on the amount of wheat flour
produced. In contrast, concerning the second graintransformation processes, it has been shown that the energy
use and greenhouse-gas effects of the bread production chain
are mainly determined by baking (i.e., the baking oven) and
farming, whereas milling, transport and dough making/fermentation play a minor role (Braschkat et al., 2003).
In addition to optimising the hydro-thermo-mechanical parameters when producing cereal products, we must also
consider the growing interest in pre-germination and/or prefermentation of grains to optimise their nutrient density
(Nelson et al., 2013). Indeed, pre-fermentation may increase the
density of bioactive compounds that are beneficial for health
(Buddrick et al., 2014; Dordevic et al., 2010; Katina and
Poutanen, 2013; Lioger et al., 2006; Poutanen et al., 2009)
whereas excessive refining strongly decreases this content
(Fardet, 2010). Germination processes can also significantly increase the nutritional and bioactive content of cereals and
improve their palatability. Indeed, Nelson et al. stated that
“germination techniques may offer a practical, natural, dietary
intervention to increase the health benefits and acceptability of
whole grains, with potentially widespread effects across populations in attenuating adverse lifestyle disease outcomes”
(Nelson et al., 2013). However, the in vitro results now must be
substantiated in humans to facilitate the future development of
germinated grains (Nelson et al., 2013).
2.6. Legumes as additional ingredients in cereal products
Legumes have long been a traditional staple food. Nevertheless, legume consumption in France has decreased so that in
2006e2007 the average intake was only 9.7 g/day with a consumption rate of 29.7% (ANSES-Afssa, 2009); which represents an
insignificant decrease of 2.4% compared with the rate observed
in the INCA1 1998e1999 study (Dubuisson et al., 2009). However,
a resurgence in the consumption of legumes has occurred due to
their supplementation of the protein fraction of cereals and the
recommendations to increase fibre intake. Whereas combining
cereals and legumes has long been practiced in developing
countries, this combination is less prevalent in the industrialised
countries. Some recent work highlighted the importance of such
a combination, such as in the case of pasta (Petitot et al., 2010;
Petitot and Micard, 2010). The margin for increasing the consumption of legumes e which have a very significant nutritional
value e is large in France, and this could be accomplished via
cereal-product technology (including bread and pasta, which
constitute good vectors of pulses) to provide all of the amino
acids essential for humans, particularly if the tendency to eat
more plant products is confirmed in the coming years. A great
deal remains to be done in this area to develop new food
products.
543
3. Proposed topics for future research
From a general point of view, an important question is whether
we can develop e from a reverse engineering perspective e a cereal
sector that is more respectful of the health potential of cereals and
their derivatives.
3.1. Locks and levers
There are locks at different stages of the grain-product chain
(Fig. 1). At the agronomic level, the pesticide contamination of the
outer layers of grain that results from conventional agricultural
practice limits the use of whole grains for nutritional purposes
(Hemery et al., 2007). Will the expansion of the least restrictive
type of organic culture provide a long-term solution to this problem? Is the diversification of cereal species and/or the introduction
of new species ( i.e., ancient cereal species and/or cereal species that
are consumed in developing countries) economically viable for
farmers? There is also the difficulty of defining genetic targets (i.e.,
compounds with a clear metabolic precursor/pathway) and the
economic viability of a breeding sector, because improved nutritional value must be defined in collaboration with nutritionists, the
relative slowness of which may at first seem unattractive to industrialists who too often have a vision of short-term profits or of
new-product development based on scientific findings that are
mostly focussed on only one protective compound, e.g., enrichment
with exogenous fibre or resistant starch, when a cocktail of compounds may be health-protective. During the primary transformation stages, can we more systematically produce less-refined
flours with lower energy costs? How can we optimise the conservation of the germ fraction either without isolating it from the grain
or after extraction? Can the techniques for isolating the aleurone
layer of wheat be generalised? What are their energy costs?
Regarding the secondary transformation stages, how can lessrefined grain products that contain less salt, sugar and fat be produced? Downstream of the cereal production sector, are consumers
prepared to move toward increasing their intake of less refined and
less sugary, salty and fatty cereals?
Globally, it is now recognised that more efforts should be made
to retain the phytochemical components initially present in wholegrains throughout the cereals sector. Thus, we must use several
levers in the sector, including the agricultural conditions, the choice
of grain varieties, more or less thorough refining and less
destructive technological processes.
The levers for improving the nutritional properties of cereal
products are found at the same levels as the locks in the various
stages of the production chain. At the agronomic level, farming
practices and plant breeding can be improved; at the genetic level,
with the advent of genomic selection, one can consider nutritional
criteria in the overall index, as has been realised in the selection of
dairy cattle (e.g., fatty-acid contents of milk); at the level of the
primary transformation, less flour refining and the preservation of
the germ and aleurone fractions may be relevant levers to act upon;
at the level of the secondary transformation, the use of less drastic
processing technologies (‘minimal processing’, e.g., prefermentation and a muesli-type process) and the formulation of
less refined products with lower salt, sugar and fat contents appear
to be promising sustainable levers; downstream, consumers can be
encouraged to evolve toward accepting less-refined grain products
with less salt, sugar and fat.
Before looking for levers to improve the health potential of grain
products in the framework of a sustainable diet, the advantage to
humans of consuming more or less whole-grain products over the
long term and understanding protective mechanisms of wholegrains should be demonstrated; for example, the antioxidant
544
A. Fardet / Journal of Cereal Science 60 (2014) 540e548
Fig. 1. Sustainability of the cereal sector: the locks and levers at the agricultural, technological, health and consumer levels.
potential of whole-grain cereals compared to refined grain cereals
has never been convincingly demonstrated in humans although
researchers continue to measure the in vitro antioxidant capacities
of cereals and to propose these capacities as essential nutritional
properties of whole-grain cereals (Fardet et al., 2008).
3.2. Whole-grain cereals and health
The scientific literature has convincingly shown the lower
prevalence of various chronic diseases (type 2 diabetes, cardiovascular diseases and certain digestive cancers) among regular
consumers (or among the highest vs lowest consumers) of wholegrain products (Fardet, 2010; Fardet and Boirie, 2014).
However, careful examination of recent reviews on the health
potential of cereal products shows that more studies are needed to
provide solid arguments for conducting the necessary upstream
investigations (e.g., into breeding, the growing conditions, refining,
and technologies) using a reverse-engineering approach. We can
distinguish, in descending order, the following priorities:
1) There is a lack of intervention studies (RCTs or randomised
controlled trials) in humans over the long term to determine
causality regarding the protective effect of whole grains; the
previously conducted intervention studies did not always
confirm the results of observational studies, e.g., an improved
antioxidant status after regularly consuming whole grains
should be promptly investigated in humans.
2) Observational studies should be carried out, e.g., the association
between the consumption of whole-grain products and the
prevalence of obesity should be further studied (Fardet and
Boirie, 2014) and the association between a high intake of
refined grains (± enriched in sugar, salt and fat) (e.g., bread and
white rice or children's breakfast cereals) and the prevalence of
chronic disease has not been sufficiently explored (Fardet and
Boirie, 2014). Additionally, some recent studies and reviews
showed that the association between the consumption of
whole-grain products and the quality of bone and mental health
should be more clearly determined (Fardet, 2010; Fardet and
Boirie, 2014).
3) As to research strategies for investigating the deleterious potential of gluten, we must distinguish between allergenicity,
intolerance (celiac disease) and non-celiac gluten sensitivity to
gluten; development of cereal products for people who are
allergic, sensitive or intolerant to gluten is a good example of
research that can be conducted throughout the cereal sector;
genetic and technological levers in this area may exist.
4) The contribution of the fibre fraction to the health effects of
whole grain has not been resolved; thus, should the health
potential of whole grain products be attributed to only their
fibre fraction? According to Smith and Tucker, “the relative
benefits of fibre extracts compared to fibres directly from whole
grain products is a critical area in which additional research is
needed” (page 118) (Smith and Tucker, 2011). In addition, recent
studies clearly showed that the health potential of grain products cannot be attributed to merely the presence of fibre (Fardet,
2010; Poutanen, 2012). Indeed, many polyphenols (e.g., ferulic
and para-coumaric acids) are chemically bound with fibre and
are lost during the extraction of the fibre fraction, i.e., they are
‘fibre co-passengers’ (Jones, 2010; Laerke and Knudsen, 2011;
Vitaglione et al., 2008) that could be progressively released
throughout the digestive tract and provide digestive, cardiovascular and colonic protection (Vitaglione et al., 2008) and
positively affect the colonic bacterial population (e.g., betaglucans and arabinoxylans) (Mitsou et al., 2010; Broekaert
et al., 2011), which remains a ‘black box’ that requires further
studies.
A. Fardet / Journal of Cereal Science 60 (2014) 540e548
However, although the health potential of whole-grain products
cannot be reduced to that of the fibre fraction (Fardet, 2010; Cho
et al., 2013), whole-grain cereals are good sources of fibre for
humans and the recommended levels of dietary fibre consumption
in France are 25e35 g/day for adults. Considering that approximately 1/3 of fibre should come from cereal-based foods, i.e., 10 g/
day, based on the French nutritional database ANSES-Ciqual for
fibre contents (ANSES-Afssa, 2008), one should consume z300 g/
day of whole-grain cereal-based foods to reach the recommended
target of 30 g of fibre/day. In France, adults consume an average of
183 g/day of breads and grain-derived products, such as pasta,
breakfast cereals, rice, durum wheat and other cereals, often in
refined form (ANSES-Afssa, 2009). This finding suggests that
perhaps products should be engineered with more fibre than is
present in whole-grain wheat products. However, a more sustainable solution for French people would be to consume more fibrerich leguminous and oleaginous seeds; currently, the rate of consumption of such seed is less than 10 g/day (ANSES-Afssa, 2009).
Therefore, there is a great need for studies on combining cereals
and legumes in commonly consumed cereal vectors, such as pasta,
breads, breakfast cereals, and biscuits.
5) Another important issue is reducing the sugar, fat and salt
contents of cereal-based foods: for example, according to the
), the target
French PNNS (Programme National Nutrition Sante
salt intake should be 8 g/day for adult men and 6.5 g/day for
re du Travail, de l'Emploi et
children and adult women (Ministe
, 2011). Today, the average salt content of a French
de la Sante
baguette is greater than 1.5% and may even reach 2%, and bread
products remain the main source of salt. Reducing the intake of
salt is expected to reduce the risk of hypertension and cardiovascular diseases.
6) Deregulation of the antioxidant status is the precursor to several
hundred diseases in humans. Grains are a very significant potential source of antioxidants, notably phenolic acids; however,
few human studies have been conducted to demonstrate their
protective antioxidant effects. Moreover, it appears that we
should distinguish between the slowly vs rapidly released
phenolic acid fractions (Fardet, 2010); the phenolic acids that
are rapidly released and absorbed have antioxidant activity and
cell-signalling activities, and the phenolic acids that are gradually released in the digestive tract potentially provide antioxidant protection to the mucous membranes (e.g., protection
against digestive cancers). Much remains to be demonstrated in
this area, including the antioxidant protection of the human
colon.
7) Cereals are also a significant source of choline and betaine, two
methyl donors that can reduce the level of hepatic triglycerides
via the homocysteine cycle, i.e., lipotropes (Fardet and
Chardigny, 2013; Fardet, 2010); the bran fraction can contain
up to 0.9% betaine and 0.2% choline, yielding a total of 1% by
weight of lipotropes. The health impact of these two components of whole grains has never been studied in humans, except
for one intervention study conducted in healthy humans that
showed an increase in the plasma betaine content after the
consumption of aleurone-rich grain products (Price et al., 2010).
Moreover, we know little about the fate of the myo-inositol
fraction of phytic acid in humans, and myo-inositol is an
important lipotrope. Thus, whole-grain wheat is potentially rich
in lipotropes (choline, betaine and myo-inositol) and in micronutrients with indirect lipotropic activity, such as some of the B
vitamins, magnesium and many polyphenols) (Fardet and
Chardigny, 2013). The prevalence of hepatic steatosis in regular consumers of whole-grain products should be studied and
the findings confirmed in intervention studies. Indeed, one
545
recent caseecontrol study showed that whole-grain consumption favourably affected the clinical characteristics of patients
with non-alcoholic fatty liver disease (NAFLD) and tended to be
associated with a less severe disease (OR ¼ 0.97, 95% CI
0.94e1.00) (Georgoulis et al., 2014). Thus, considering that there
are several million people who are affected by fatty liver disease
worldwide and that this condition can lead to much more severe
liver disease (Fardet and Chardigny, 2013), the pool of lipotropes
in wheat may constitute an attractive target for breeders (lipotrope-rich varieties). Phytic acid and/or its degradation products
may also have an anticarcinogenic potential (Norhaizan et al.,
2011; Saad et al., 2013; Shamsuddin, 2002).
The antioxidant and lipotropic potentials of whole grains should
therefore be more widely studied in humans, knowing the importance of antioxidant and lipotropic status deregulations in the onset
of many chronic diseases.
8) Scientific evidence suggests that a profile of compounds with
complementary mechanisms of action rather than a single
nutrient is protective (Fardet, 2010). So, rather focussing on
studying the relationship between a component and a metabolic effect (the reductionist approach), high throughput technologies of integrative biology should be used to study the
nutritional impact of cereals as foods/complex matrices on
metabolism as a whole (Fardet et al., 2007) or on gene expression (the holistic approach) to ultimately determine the positive
metabolic and gene networks that are activated by the consumption of whole-grain products (Fardet, 2010).
3.3. Refining and new technological processes
The main issues in grain refining appear to be the following: 1)
to determine how to maintain the protective compounds of whole
grains that are contained mainly in the germ and bran fractions
while avoiding the contaminants in the outermost layers of the
grain; 2) to reduce the levels of sugars, salts and fats; and 3) to
develop new cereal products that are accepted by the consumer.
A review of the literature suggests several questions to be
addressed in research, as follows:
3.3.1. First transformation
Can we preserve the germ fraction in flour without prior isolation, stabilisation and reincorporation? Regarding the contamination of the outer layers of the grain, is this currently a real risk to
health? Further studies should be conducted to definitively answer
this question. Regarding the aleurone layer, there are now welldeveloped techniques for isolating it or maintaining it during
fractionation (while excluding the outermost layers, such as the
pericarp) (Barron et al., 2012), but can these be widely applied and
are they sustainable in the long term in terms of their energy cost?
In addition to offering complete or semi-complete flours, these
issues can be addressed by acting on the ‘formulation’ lever, i.e.,
how flour is refined and whether fibre and/or the previously isolated aleurone layer are added, with the risk, however, of losing
some of the ‘physical structure effects’ of whole grain.
3.3.2. Second transformation
At the level of the second transformation, several issues should
also be addressed. Firstly, the use of softer technologies for shaping
grain products should be further studied (“minimal processing”).
The literature suggested the following areas of research: the effects
of cereal pre-fermentation/germination on the nutrient density of
cereal products and reconsidering the hydro-thermo-mechanical
546
A. Fardet / Journal of Cereal Science 60 (2014) 540e548
parameters used during extrusion to reduce the gelatinisation of
starch and preserve the physical structure of the food matrix,
perhaps drawing on muesli-production techniques. Preserving the
physical structure of the matrix has many potential health benefits,
such as a more gradual release of nutrients, increased satiety, a
positive effect on passage through the intestine and a positive effect
on the intestinal flora (Wang et al., 2014).
Secondly, multiple grain species can be mixed to maximise the
intake of bioactive compounds.
Third, is it feasible to decrease the levels of salt, sugar and fat
from a technological point of view, and will products with lower
levels be accepted by the consumers? A suggestion is to replace the
salt (or sodium chloride) with a mixture that includes NaCl and
calcium carbonate, potassium and magnesium salts and various
me
sy et al., 2014). These saline mixtures, like
trace elements (Re
those in animal feed, could be easily incorporated in bread to give it
the status of a particularly balanced food. Research on lowering the
contents of sugar and salt while maintaining the consumer's
acceptance, e.g., in biscuits (Villemejane et al., 2012), are in
progress.
3.4. Genetic selection and agronomic conditions
Upstream, at the agronomic and genetic levels, several issues
also need to be addressed. It seems promising to attempt the
following:
1) To encourage the diversity of wheat varieties or cereal species
(ancient and/or pseudo-cereal grains) to benefit from the
greatest possible diversity of microconstituents and bioactive
compounds rather than to focus on a single grain component. Is
the introduction of new varieties and/or species (sorghum,
quinoa, millet and others) economically and agronomically
viable?
2) To screen varieties to seek those that have the best balance of
the largest number of bioactive compounds (e.g., via metabolomics (Shewry et al., 2013). For example, regarding antioxidants, focussing on only one antioxidant has little meaning
because more than 30 compounds in whole grains have antioxidant activities: their synergistic action may be effective, not
the action of a single compound (Fardet, 2010; Thompson et al.,
2006). This concept holds true for all of the other compounds
with a given physiological effect, such as lipotropes, lipidlowering compounds, anti-carcinogens, and anti-inflammatory
compounds. Thus, rather than focussing on improving the
content of a single component, genetic-selection research could
focus on ‘packages’ of compounds, such as antioxidants, lipotropes or anti-inflammatory compounds, to develop varieties
with high antioxidant or lipotropic potential,
3) To measure the impact of organic agriculture on the health
potential of grain products via a prospective cohort study
(organic vs conventional cereal products), even though this type
of study is very difficult and expensive to conduct. Notably,
however, the products of organic agriculture do not appear to
have a better nutritional composition than those produced using conventional agriculture, as was generally shown for crops
(Dangour et al., 2009, 2010) or more specifically, for maize
€ hlig and Engel, 2010) or wheat (Nitika et al., 2008) using the
(Ro
identical grinding mode (Chaurand et al., 2006), although the
level of antioxidants and some mineral compounds might be
generally higher in some plant products (Lairon, 2010). However, in vitro measurements of the levels of nutrients cannot
alone predict their nutritional effects in humans. Nevertheless,
the robustly demonstrated added value of organically grown
crops is currently fostering a greater respect for the
environment.
4) To study the impact of reducing the rate of nitrogen fertilisation.
The most significant environmental effect of the implementation of the Nitrate Directive, which was issued in 1995, is its
major contribution to decreasing the N balance (N surplus) in
soil, particularly in Denmark, Ireland, the Netherlands and the
United Kingdom (van Grinsven et al., 2012).
3.5. The more general issue of plant vs animal proteins
In the framework of a sustainable diet, the question of eating
more plant than animal products is increasingly emphasised. Nutritionists agree that we should consume a maximum of 20% animal
products and a minimum of 80% plant products; based on the
INCA2 survey, the respective proportions are estimated to be
approximately 35e40 and 60e65% in the French population
(ANSES-Afssa, 2009). In addition, the Agrimonde report (conducted
jointly by INRA and CIRAD) estimated that by 2050, to ensure
environmental sustainability, 15% of the energy intake should be
from animal products and 85% from plant products (Agrimonde,
2009).
However, encouraging the ingestion of more plant products and
therefore more vegetable proteins requires assessing the long-term
effects of the increased consumption of plant-based proteins and
thinking about what animal/plant protein ratios to achieve, with
upstream implications on crop-cultivation patterns (e.g., reducing
the input and the carbon cost (Jeuffroy and Oury, 2012)). Cereal
products could play a key role in this development, particularly in
combination with legumes, for which they are good vectors, e.g.,
biscuits, breakfast cereals, pasta and bread are among the most
consumed cereal products.
However, the distinction between plant and animal proteins
appears to be rather reductionist for several reasons, as follows: 1)
we know we can compare the value of meat protein with that of a
combination of cereals with legumes even though the average total
digestibility of the latter is a little worse; 2) the environment of the
protein and the protein-associated components matter, as well as
does the structure of the food matrices. Therefore, the issue is much
more complex than whether proteins are derived from animal- vs
plant-based products. I believe the real issue is more holistic, i.e., to
move towards more complex plant-based foods.
4. Conclusions and perspectives
Improving the health potential of cereal products requires a
reverse engineering-based approach. The health potential of cereal
products and consumer's acceptance should be prioritised before
all other considerations.
However, there are numerous outstanding issues about the
health potential of cereal-based foods that remain to be investigated. First, the relationship between cause and effect has not been
sufficiently well established to reinforce the conclusions of epidemiological studies. Second, researchers must more precisely characterise whole grains and their bioactive compounds and
determine how these factors interact to affect the metabolic and
physiological functions far beyond those of the gut. Third, more
studies are needed to confirm the role played by whole grains in the
protection against colorectal cancer via their fibre content. Fourth,
the polyphenols associated with the fibre fraction (‘fibre co-passengers’) in whole grains may play a positive role in the oxidative
and inflammation processes underlying obesity and this issue must
be addressed. Fifth, a consensus on the definition of whole-grain
cereals is a necessary pre-requisite for a common language in
A. Fardet / Journal of Cereal Science 60 (2014) 540e548
basic research and clinical and intervention studies of cereals, as
well as in the field of controlled labelling. The standardisation of
this definition and related labelling and health claims will help to
minimise the confusion of the consumer and facilitate advocating
for a healthy diet that includes whole grains (Gibson et al., 2013).
More generally, it is clear that the agro-food industry and cereal
sector must adapt to the production of grain products that are more
‘friendly’ for the environment and for health (eco-conception) at an
economically viable price. This goal can be realised only if there is a
concerted and integrated approach among all of the actors in the
sector.
Funding source
There was no funding source for this study.
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