Journal of Cereal Science 84 (2018) 112–124

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Journal of Cereal Science

journal homepage: www.elsevier.com/locate/jcs

Sorghum polyphenols and other bioactive components as functional and T

health promoting food ingredients
Audrey L. Girard, Joseph M. Awika∗
Texas A&M University, Soil & Crop Sciences Department, Nutrition & Food Science Department, 2474 TAMU, College Station, TX, 77843, USA

A R T I C LE I N FO A B S T R A C T

Keywords: Sorghum is a versatile, drought and heat tolerant crop that fits well in sustainable production systems. Sorghum
Sorghum grain has attractive attributes highly relevant to modern food use, especially in relation to chronic disease
Polyphenols prevention. The sorghum endosperm generally has a slower digesting starch profile than other cereal grains,
Bioactive compounds which contributes to slowed gastric emptying and may thus benefit satiety and weight management. In addition,
Functional ingredients
the diversity of phytochemicals in sorghum, especially the polyphenols, have been linked to various benefits,
Human health
including improvements in glucose metabolism and insulin sensitivity, and lipid metabolism, as well as reduced
fat accumulation, and markers of oxidative stress and inflammation in recent human trials. Despite the health
benefits, the use of sorghum as a food ingredient severely lags its potential. The review focuses primarily on
highlighting some of the challenges facing sorghum as a modern food ingredient, and discusses how the unique
chemistry and properties of sorghum polyphenols can be exploited to improve food quality, while providing
enhanced bioactive functionality.

1. Introduction remains fairly modest.

Sorghum is a versatile, drought-tolerant crop that is commonly
produced in semi-arid regions of Africa, Asia, Australia, and North and
South America. As a C4 photosynthetic plant, sorghum is highly effi-
cient at assimilating carbon and accumulating biomass at elevated
temperatures, in contrast to the C3 cereal plants like rice and wheat
(Paterson et al., 2009). Thus, sorghum is well adapted for superior
productivity in a warming climate and growing scarcity of fresh water.
In addition to being grown primarily for grain, sorghum is also grown
for forage, sugar (sweet stalk) and, potentially, for cellulosic biomass
for biofuel production.
Despite the outstanding agronomic attributes of sorghum, its use
around the world, especially for food, is limited relative to its potential.
Sorghum grain is mainly used as a staple food in semi-arid regions of
Africa, and to a much more limited extent in parts of India and Central
America. In other parts of the world where significant amount of sor-
ghum grain is used, e.g., USA, Mexico, and China, it mostly serves as a
feed crop. However, a surge of interest in dietary diversification,
healthy eating, and alternative food ingredients like “ancient grains”
has resulted in a growing interest in, and use of, sorghum in different
products in the US and parts of Europe (Awika, 2017). Nevertheless,
overall use of sorghum as a food ingredient in these parts of the world
Besides its agronomic advantages, sorghum has attractive attributes
highly relevant to modern food use; especially given chronic diseases
linked to excess calorie intake and poor diet are a growing concern
globally. Sorghum is unique among major cereal grains in that it has
high levels of a diverse array of bioactive components not common to
other cereals, with demonstrated potential to benefit human health
(Althwab et al., 2015; Awika et al., 2018; de Morais Cardoso et al.,
2017). The most prominent group of beneficial sorghum bioactive
components are the polyphenols, especially the flavonoids (Awika
et al., 2018). In addition, sorghum is uniquely high in bioactive lipids
(especially policosanols and phytosterols), primarily as components of
waxes located on the grain pericarp (Awika and Rooney, 2004; Hwang
et al., 2005). Besides the bioactive compounds, sorghum endosperm
also generally has a slower starch digesting profile compared to other
cereal grains, a property that has been demonstrated to modulate
postprandial blood glucose response in humans (Simnadis et al., 2016).
The apparent superior agronomic and health beneficial attributes of
sorghum obviously beg the question of why it does not play a more
prominent role in human diet. Even though interest in sorghum as a
food ingredient is growing, significant bottlenecks stand in the way of
the crop realizing its potential. Among the key issues that limit broad
sorghum food use include;

∗
Corresponding author.
E-mail address: awika@tamu.edu (J.M. Awika).

https://doi.org/10.1016/j.jcs.2018.10.009
Received 14 September 2018; Received in revised form 17 October 2018; Accepted 17 October 2018
Available online 22 October 2018
0733-5210/ © 2018 Elsevier Ltd. All rights reserved.
A.L. Girard, J.M. Awika
i) challenges related to sorghum endosperm functionality;
ii) relatively limited clinical evidence documenting the (unique)
health benefits of sorghum components as they directly impact
specific disease outcomes;
iii) abundantly available alternative grains with familiar sensory pro-
files;
iv) lack of optimal processing technologies, and;
v) a relatively underdeveloped food sorghum value chain.
A significant part of the review discusses some of these challenges as
they relate to sorghum use as a food ingredient in modern food value
chain, along with opportunities and technologies that must be exploited
to derive maximum benefits from the unique bioactive compounds in
sorghum.
2. Bioactive compounds in sorghum
Most bioactive compounds in cereal grains are secondary metabo-
lites produced by plants as defense or signaling molecules, or as
structural molecules; the vast majority of these compounds are struc-
turally categorized as polyphenols or lipids. The polyphenols (the pri-
mary focus of the review) include mainly phenolic acid and flavonoid
derivatives, whereas lipids include mainly esters of phytosterols/stanols
and policosanols. Occasionally, the lipids are found esterified to phe-
nolic compounds, especially phenolic acids (Awika and Rooney, 2004).
In sorghum, like other cereal grains, the bioactive compounds are
mainly located in the bran fraction (pericarp, testa and aleurone tis-
sues). The compounds co-exist with the abundant cell wall poly-
saccharides in cereal bran and contribute significantly to the health
benefits attributed to whole grain intake (Awika et al., 2018; Vitaglione
et al., 2015). Consequently, food processing methods that remove the
bran will severely diminish the health benefits derived from cereal
grains. Sorghum has a more diverse and/or higher levels of both
polyphenols and bioactive lipids than most other cereal grains. Recent
reviews and/or book chapters have discussed the components and their
broader contribution to health in depth (Althwab et al., 2015; Awika
et al., 2019; Awika, 2017; de Morais Cardoso et al., 2017). The present
review will thus mainly focus on how the bioactive and other functional
properties of the bioactive compounds can be exploited to enhance food
quality and health benefits.
3. Polyphenols in sorghum
Polyphenols are common to most plants and have been widely in-
vestigated for their health benefits related to their ability to scavenge
free radicals and modulate various signaling pathways relevant to dis-
ease prevention. The dominant polyphenols in sorghum are structurally
classified as phenolic acid or flavonoid derivatives (Fig. 1). The poly-
phenols serve an important role in natural plant defense against pa-
thogens and pests; for example, presence of condensed tannins in sor-
ghum increases tolerance to bird predation (Awika, 2017). Among
cereal grains, sorghum is the most diverse in terms of the types and
amounts of the major polyphenols (Table 1) (Awika et al., 2018), thus
presents an intriguing opportunity to expand the role of cereal-derived
polyphenols in human health. The diversity of polyphenols is re-
sponsible for a wide array of pericarp colors in sorghum, ranging from
cream white to red, lemon yellow and black, and could thus also pro-
vide a natural means to diversify food visual sensory appeal.
3.1. Phenolic acids
Phenolic acids are the most prominent and well-characterized
phenolic compounds in cereal grains. Both cinnamic and benzoic de-
rivatives (Fig. 1) are found in cereals, although cinnamic acid deriva-
tives are far more abundant. The phenolic acids form major components
of the cell wall structure of cereals and are most commonly esterified to
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Journal of Cereal Science 84 (2018) 112–124
hemicelluloses. In sorghum, like other cereal grains, 70–95% of the
phenolic acids are covalently linked to cell wall polysaccharides,
commonly referred to as ‘bound’ (Table 1) (Awika et al., 2018;
Chiremba et al., 2012). The phenolic acids not covalently bound to cell
wall polysaccharides mostly exist as conjugates of carbohydrate
monomers, especially glycerol (Svensson et al., 2010; Yang et al.,
2012), and rarely as unconjugated free acids. Similar to other cereal
grains, ferulic acid derivatives are by far the most abundant group,
constituting about 90% of the bound phenolic acids in sorghum (Awika,
2017; Chiremba et al., 2012; Yang et al., 2012). Because of their ex-
tensive covalent linkage to the cell wall polysaccharides, the phenolic
acids in cereal grains contribute uniquely to the beneficial biological
effects of whole grain components in human diets; their unbound forms
can be directly absorbed in upper gastrointestinal (GI) tract, while
colon metabolism of cell wall polysaccharides can release the cova-
lently bound forms, to provide a ‘sustained’ systemic circulation of the
compounds (Neacsu et al., 2017; Vitaglione et al., 2015). In contrast,
the phenolic acids found in fruits and vegetables, and other dicot plant
foods like legumes that mostly exist in unbound form (Awika and
Duodu, 2017; Awika et al., 2018), and are thus likely to be metabolized
differently. How the covalently bound phenolic acids influence gut
microbiota population and function is still largely unknown and de-
serves to be investigated.
3.2. Flavonoids
Even though flavonoids are the most abundant forms of phenolics
compounds in plant foods, in cereal grains commonly consumed, the
flavonoids are found in relatively small amounts (Zamora-Ros et al.,
2016), and have thus not been much scrutinized for their contribution
to beneficial effects of whole grain intake. Nevertheless, a group of
flavonoids found in cereals as the major dietary source, the flavones
(Fig. 1), have been associated with strong bioactive properties related
to anti-inflammatory and chemoprotective function at low levels (Agah
et al., 2017; Lim et al., 2013; Yang et al., 2014), and thus may have
important dietary benefits. Flavonoids are especially important not only
because of their distinct biological properties, but also due to their
impact on sensory properties of foods, including color, flavor (e.g.,
bitterness) and astringency. Furthermore, the polymeric flavonoids,
condensed tannins, can also significantly impact macronutrient di-
gestibility or bioavailability (Amoako and Awika, 2016a; Mitaru et al.,
1984; Pan et al., 2018).
Unlike other cereals, sorghum, and some minor millets like teff and
pearl millet, have significant levels of monomeric and/or polymeric
flavonoids (Table 1) (Dykes et al., 2009, 2011; Gaitan et al., 1989;
Ravisankar et al., 2018). For example, teff was recently reported to
contain flavones in the range of 1400 to > 2000 μg/g (Ravisankar et al.,
2018), compared to other cereals that typically contain less than
400 μg/g of the flavones (Awika et al., 2018). Likewise, some sorghum
varieties contain polymeric tannin levels as high as 33 mg/g sorghum
(Awika et al., 2003), which can co-exist with high levels of monomeric
flavonoids, like 3-deoxyanthocyanins. Therefore, in such grains, the
flavonoids likely play a major role in their health promoting properties,
as well as other attributes relevant to food quality, like seed pericarp
color.
An important feature of sorghum flavonoids is that, with the ex-
ception of the condensed tannins, they are typically unsubstituted at the
C-3 position (Fig. 1), i.e., are 3-deoxyflavonoids. The unsubstituted C-3
generally makes flavonoids more stable, and is shared with other cereal
grains to some extent, because the dominant monomeric flavonoid in
most common cereals are the flavones (Fig. 1) (Awika et al., 2018).
However, sorghum additionally contains a unique set of pigments
known as 3-deoxyanthocyanins, in contrast to other pigmented grains
like purple maize, purple wheat or red rice, that contain the C-3 sub-
stituted anthocyanins as the primary pigments.
The vast majority of monomeric sorghum flavonoids either have a
A.L. Girard, J.M. Awika
O OH
R3 R1
R2
Major benzoic acids in sorghum;
Gallic acid, R1 = R2 = R3 = OH
Protocatechuic acid, R1 = R2 = OH, R3 = H
Vanillic acid, R1 = OCH3, R2 = OH, R3 = H
p-Hydroxybenzoic acid, R1 = R3 = H, R2 = OH
O and/or OCH3
R3
R2
R1
Major cinnamic acids in sorghum;
Ferulic acid, R1 = OCH3, R2 = OH, R3 = H
Caffeic acid, R1 = R2 = OH, R3 = H
Sinapinic acid, R1 = R3 = OCH3, R2 = OH
p-Coumaric acid, R1 = R3 = H, R2 = OH
3'
2'
1 R4
8 1' B
7 8a O 2
A C 6'
6 3
4a
5 4
Basic flavonoid structure
R2 O
R1
Sorghum 3-deoxyanthocyanin structure;
Apigeninidin derivatives, R3 = OH, R4 = H
Luteolinidin derivatives, R3 = R4 = OH
R1 & R2 are usually OH, O-glycosides, and/or OCH3
Fig. 1. Structure of the major phenolic acids and flavonoids in sorghum.
phenol or catechol group on the B-ring, thus are derivatives of nar-
ingenin (apigenin and apigeninidin, and proapigeninidin derivatives) or
eriodictyol (luteolin or luteolinidin, proluteolinidin and procyanidin
derivatives) in the phenylpropanoid pathway (Fig. 1). Flavonoids with
galloyl groups, which are found in some cereals and common in other
plant commodities, have not been credibly identified in sorghum.
4. Health benefits of bioactive compounds in sorghum
As already mentioned, evidence on specific health benefits asso-
ciated with sorghum and sorghum components has been the subject of
several reviews and/or book chapters in the recent past (Awika et al.,
2019; Awika, 2017; de Morais Cardoso et al., 2017; Simnadis et al.,
2016). Therefore, to avoid being repetitive and redundant, we avoid in-
depth discussion of the specific evidence and associated mechanisms.
Instead, we provide a summary of updated key evidence available,
especially in the past 3–5 years, in Table 2. Broadly, the evidence on
sorghum in relation to chronic disease prevention have mainly focused
on the impact of the sorghum polyphenols, as well as the apparent slow
digestibility of sorghum endosperm. Specific beneficial effects have
been found in relation to mechanisms that reduce oxidative stress and
chronic inflammation, prevent some types of cancer, improve glucose
metabolism and reduce insulin resistance, improve lipid metabolism
Journal of Cereal Science 84 (2018) 112–124
R3
R2 O
R4
R1 O
Sorghum flavone structure;
Apigenin derivatives, R3 = OH, R4 = H
Luteolin derivatives, R3 = R4 = OH
R1 & R2 are usually OH, O-glycosides,
R3
OH
R2 O
R4
R1 O
Sorghum flavanone structure;
Naringenin derivatives,R3 = OH, R4 = H
Eriodictyol derivatives, R3 = R4 = OH
R1 & R2 are usually OH and/or O-glycoside
4'
5'
R3 O
R5
R1
R2
R3
Sorghum proanthocyanidin unit structure;
R4 Proapigeninidin , R1 = R5 = H, R4 = OH
Proluteolinidin, R1 = H, R4 = R5 = OH
Procyanidin, R1 = R4 = R5 = OH
R1 & R2 are usually OH, but can rarely
have OCH3
and suppress fat accumulation, and alter gut microbiota to improve
colon health. It is encouraging to note that human intervention studies
focusing on effects of sorghum and its components to health are be-
ginning to appear more frequently in literature (Table 2). This has been
a critical missing piece of the puzzle in linking the unique properties of
sorghum observed in chemical and in vitro assays to actual benefits to
humans. Hopefully, the emerging evidence will encourage more re-
search investment aimed at uncovering the health benefits and food
application potential of the unique and intriguing crop.
5. Sorghum flavonoids as bioactive, functional ingredients
5.1. 3-Deoxyanthocyanins
5.1.1. Unique functional and bioactive properties of 3-deoxyanthocyanins
An interesting unique aspect of sorghum is that unlike other food
plants, the mature grain and other plant tissues only contain the 3-
deoxyanthocyanins as the dominant secondary plant pigments, pri-
marily as apigeninidin or luteolinidin and their O-methylated and
conjugated derivatives (Awika et al., 2005a,b; Geera et al., 2012;
Kayodé et al., 2011; Petti et al., 2014). Other rare forms, including
dimers and fused-ring (pyrano-) structures have also been identified
(Geera et al., 2012; Khalil et al., 2010). The 3-deoxyanthocyanins are
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A.L. Girard, J.M. Awika Journal of Cereal Science 84 (2018) 112–124

Table 1
Phenolic compounds in sorghum relative to the major cereal grains.
Phenolic Compound Commodity Content (μg/g) Comment Reference

Phenolic acids
Extractable phenolic acids
Sorghum 15–1650 Mostly caffeoyl glycerides; some feruloyl and coumaroyl esters, too (Awika and Rooney, 2004; Chiremba
et al., 2012)
Wheat 3–420 Mostly ferulic acid derivatives (Li et al., 2008; Mattila et al., 2005)
Maize 20–25 Mostly ferulic acid derivatives (Mattila et al., 2005)
Rice 40–300 Mostly ferulic acid derivatives; followed by p-coumaric acid derivatives (Mattila et al., 2005; Zhou et al., 2004)
Bound phenolic acids
Sorghum 430–1200 Mostly ferulic acid derivatives (Awika and Rooney, 2004; Chiremba
et al., 2012)
Wheat 200–1000 Mostly ferulic acid derivatives (Li et al., 2008; Mattila et al., 2005)
Maize 315–350 Mostly ferulic acid derivatives (Mattila et al., 2005; Chiremba et al.,
2012)
Rice 170–500 Mostly ferulic acid derivatives; followed by p-coumaric acid derivatives (Mattila et al., 2005; Zhou et al., 2004)
Flavonoids
(3-Deoxy) Anthocyanins
Sorghum 200–4500 Exclusively 3-deoxyanthocyanins (Awika et al., 2004)
Wheat 0–500
Maize 0–3000 Primarily cyanidin glucosides (in pigmented maize hybrids) (Collison et al., 2015; Salinas Moreno
et al., 2005)
Rice 0–3500 Mostly cyanidin and peonidin glucosides in pigmented varieties (Goufo and Trindade, 2014)
Flavones
Sorghum 20–390 Apigenin, luteolin, and their glycosides (Dykes et al., 2011; Yang et al., 2015)
Wheat 190–365 Apigenin C-glycosides (Hernández et al., 2011)
Maize 0–360 Apigenin C-glycosides; presence only significant in pigmented maize (Casas et al., 2014)
Rice 0–20 Mostly apigenin C-glycosides, some luteolin derivatives (Goufo and Trindade, 2014)
Flavanones
Sorghum 0–2000 Naringenin, eriodictyol, and their O-glycosides in white, red, and lemon-yellow (Dykes et al., 2009, 2011; Yang et al.,
varieties 2015)
Wheat nd
Maize nd
Rice nd
Flavan-3-ols
Sorghum 0-33,000 Present in some varieties, primarily B-type linkages, highly polymerized (mDP (Awika et al., 2003; Girard et al., 2018)
20)
Wheat unknown B-type procyanidin, prodelphinidin & propelargonidin in red wheat; difficult to McCallum and Walker (1990)
extract in mature kernels
Maize nd
Rice 0–325 Present in some pigmented varieties, A- and B-type linkages, mostly oligomers (Goufo and Trindade, 2014; Min et al.,
(DP 5–8) 2012)

Nd - no data.

unique in various ways. For example, they are among the rare group of
flavonoids that primarily exist in plant tissue as aglycones (not con-
jugated to other molecules); their anthocyanin analogs are essentially
exclusively conjugated in nature.
The 3-deoxyanthoxyanins are a lot more stable than anthocyanins to
degradative environments encountered during food processing, like
elevated temperature, pH, among others (Ojwang and Awika, 2008,
2010; Yang et al., 2014). The stability is due to the reduced suscept-
ibility of the 3-deoxyanthocyanin molecule to nucleophilic attack and
hydration (Awika, 2008; Brouillard et al., 1982), the primary me-
chanism by which anthocyanin structure transforms into colorless
forms in solution (Yang et al., 2014). The 3-deoxyanthocyanins also
give color hues that do not vary as widely with changing pH as the
anthocyanins (Awika, 2017), and thus can provide more predictable
color properties under various conditions. The rare pyrano and dimeric
forms of the 3-deoxyanthocyanins are even more stable and resistant to
color degradation relative to the conventional 3-deoxyanthocyanins,
and could thus provide enhanced food application opportunities (Geera
et al., 2012; Khalil et al., 2010; Ojwang and Awika, 2008).
Due to their better overall stability to food processing and handling
conditions relative to the more common anthocyanins, there is con-
siderable interest in using the 3-deoxyanthocyanins as natural food
colorants (Akogou et al., 2018a,b; Awika, 2017). It is actually some-
what surprising that these compounds have not found their way into
mainstream commercial use despite the fact that their economic po-
tential has been known for a long time, with at least one patent for their
synthesis being issued to Coca Cola Company in 1970s (Iacobucci and
Sweeny, 1978). A possible reason may be related to market timing, i.e.,
with the availability of highly functional and low-cost synthetic color-
ants, a compelling market need for the 3-deoxyanthocyanins was
probably lacking. However, the growing demand for natural in-
gredients by consumers has forced major food companies to seek nat-
ural colorants, with several pledging to remove artificial colors from
their product portfolios (Awika et al., 2019). The trend, therefore,
presents a renewed opportunity to exploit the highly functional sor-
ghum 3-deoxyanthocyanin pigments.
Data on bioactive properties of 3-deoxyanthocyanins is relatively
limited and has been recently summarized (Awika, 2017) (Table 2).
However, the more interesting perspective is that the 3-deox-
yanthocyanins seem to have unique bioactive properties relative to
their anthocyanin analogs, which suggests their unique structure im-
proves their affinity for cellular target relevant to disease prevention.
For example, 3-deoxyanthocyanidins with at least one O-methyl sub-
stitution, and sorghum extracts containing these compounds, were
shown to be strong phase II enzyme inducers (Awika et al., 2009; Yang
et al., 2009), a property that has not been reported for anthocyanins.
Luteolinidin was also reported to be more cytotoxic to cancer cells than
its anthocyanidin analog, cyanidin (Shih et al., 2007). More recently, a
patent application was submitted for use of 3-deoxyanthocyanidins as
agents for treating ocular diseases (Fontaine et al., 2018). The patent
applicants demonstrated that various 3-deoxyanthocyanidin molecules
were considerably superior to their anthocyanidin analogs at protecting

115
 Table 2
Summary of key recent data on health effects of sorghum and sorghum components published since 2013.
Potential Health Benefit
In vitro data
Improve glycemic response
Reduced caloric impact; Improved
glycemic response
Improve glycemic response
Improve glycemic response
Improve glycemic response
Improve glycemic response
Improve glycemic response
Anti-inflammatory
Cancer prevention
Cancer prevention
Cancer prevention
116
Cancer prevention
In vivo data
Improve glycemic response
Improve glycemic response
Antiinflammatory
Reduced fatty liver deposits
Cancer prevention
Alter gut microbiota
Alter gut microbiota
Human trials
Slow gastric emptying; improve
glycemic response
Improve glycemic response
Bioactive component
Proanthocyanidins (tannins)
Tannins
Tannins
Tannins
Sorghum endosperm
Sorghum endosperm
Sorghum endosperm
Flavones
Flavones and flavanones
3-Deoxyanthocyanins
3-Deoxyanthocyanins
Flavones, flavanones, 3-
deoxyanthocyanins
Tannins
Tannins and 3-deoxyanthocyanins
Tannins and 3-deoxyanthocyanins
Flavones
Tannins and 3-deoxyanthocyanins
Tannins and 3-deoxyanthocyanins
Decorticated sorghum
Whole grain sorghum
Matrix
Sorghum flour
PA-starch complexes
Tannin sorghum bran in wheat flour
tortillas
PA encapsulated in kafirins
Pasta made with sorghum flour
substituted for part of durum wheat
semolina
Composite extrudate of sorghum and
maize
Gluten-free bread
White sorghum extract
Lemon yellow, red, and white sorghum
extracts
Purified, and in sorghum stalk phenolic
extract
Purified sorghum phenolic extract
Sorghum phenolic extract
Encapsulated in sorghum kafirins in rat
diet
Replaced cellulose/starch with extruded
sorghum flour in diet of obese rats
Replaced cellulose/starch with extruded
sorghum flour in diet of obese rats
White and black sorghum phenolic
extract in ovariectomized mice
In diet of rats with colitis
In diet of rats with colitis
Porridge (N = 14)
Wheat flour replacer in muffin (N = 10)
Main Effect(s) Source
Increased resistant starch content (Mkandawire et al., 2013)
A.L. Girard, J.M. Awika
High MW tannins complexed with amylose and increased slow digesting and Barros et al., 2014; Amoako
resistant starch content and Awika, 2016a
Increased slowly digestible starch and decreased rapidly digestible starch (Dunn et al., 2015)
Retained inhibitory activity against α-glucosidase and α-amylase during (Links et al., 2015)
simulated digestion
Increased resistant starch content (Khan et al., 2015)
Increased slowly digestible starch in extrudates with increased sorghum (Licata, 2014)
substitution
Sorghum predicted glycemic index = 72 vs wheat (100), quinoa (95), (Wolter et al., 2014)
buckwheat (80)
Exhibited anti-inflammatory response in LPS-stimulated non-malignant (Agah et al., 2017)
colonocytes (CCD18Co); Synergistic effect with cowpea flavonols –
downregulated NF-kB and cytokine (TNF-α, IL-6, IL-8) gene and protein
expression
Apigenin and naringenin reduced young adult mouse colonocytes growth (Yang et al., 2015)
when used individually; greater effect when used in combination. Effect
shown to be due to ER-β activation.
Showed antiproliferative and proapoptotic activity in colon cancer stem cells (Massey et al., 2014)
Inhibited proliferation of human breast cancer cells (MCF-7) by 84%; Induced (Suganyadevi et al., 2013)
apoptosis by down regulating Bcl-2 gene and stimulating P53 gene
Inhibited proliferation of ovarian cancer cells (A27801AP and PTX-10); (Dia et al., 2016)
Increased chemosensitivity of these cells to paclitaxel (common
chemotherapy)
Survived digestion to small intestine, modulated blood glucose level (Links et al., 2016)
Reduced fat accumulation and markers of inflammation (TNF-α, blood glucose (Arbex et al., 2018)
level)
Increased anti-inflammatory markers (peroxisome proliferator activated
receptor-γ gene expression and IL-10)
Reduced body mass index and liver weight; (de Sousa et al., 2018)
Increased expression of lipid metabolism regulator genes (adiponectin 2
receptor and peroxisome proliferator-activated receptor α); Reduced
expression of fatty acid synthesis regulator (sterol regulatory element-binding
transcription factor 1)
Reduced aberrant crypt foci formation in distal colon of ovariectomized mice. (Yang et al., 2014)
Increased richness of colonic bacteria; (Ritchie, 2015)
Prevented dysbiosis of Firmicutes/Bacteroidetes
Upregulated repair mechanisms and SCFA transporter expression (Ritchie et al., 2017)
Traditional African foods (i.e., sorghum and millet thick porridges, millet (Cisse et al., 2018)
couscous) exhibited gastric emptying rate about 2X longer than urban starchy
foods (i.e., rice, potato, pasta)
Plasma glucose mean area under curve reduced 35% in men fed whole (Poquette et al., 2014)
sorghum vs whole wheat muffins after fasting. Insulin response decreased 55%
with sorghum muffin; attributed to measured higher slowly digestible and
resistant starches in sorghum vs wheat.
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retinal pigment epithelial (RPE) cells against N-retinyl-N-retinylidene

ethanolamine (A2E) induced apoptosis and death, both in vitro and in
(Stefoska-Needham et al.,

(Stefoska-Needham et al.,

(Anunciação et al., 2018)

an in vivo model. The A2E is a lipofuscin component whose accumu-
lation in the PRE cells has been linked to age-related macular degen-

(Lopes et al., 2018)

(Khan et al., 2015)
eration, among other visual impairment related diseases (Suter et al.,
2000). The evidence obviously suggests potential unique applications of
the 3-deoxyanthocyanins in health and disease prevention.
Source

2016)

2017)

5.1.2. Opportunities for 3-deoxyanthocyanins as functional food ingredients

For the unique 3-deoxyanthocyanins to find broad application as
Sorghum increased postprandial glucose response, but did not reduce caloric

Increased plasma polyphenols, antioxidant capacity, and SOD activity, while

glucose, fasting insulin, lipids, and inflammatory markers; similar effects for
All subjects lost weight, reduced waist circumference, and improved fasting

Decreased spike in postprandial blood glucose (all sorghums decreased, but

food colorants, the pigments must be commercially competitive.

Reduced markers of inflammation in persons with chronic kidney disease
Sorghum (white, red, brown/condensed tannin) had higher satiety than

Conventional genetic tools present one of the most exciting opportu-

nities to enhance commercial potential of the 3-deoxyanthocyanins. A
(decreased C-reactive protein and malondialdehyde serum levels)

key area that has been targeted is enhancing yield of the pigments in
protein carbonyl level (marker of oxidative stress) decreased

plant tissue, both in the grain pericarp (Pfeiffer and Rooney, 2016) or
non-grain tissue (Petti et al., 2014), and both have been accomplished
to remarkable degrees (Table 1). In grain pericarp, an additional im-
portant consideration is the crop (grain) yield which dictates overall
tannin sorghum treatment was most significant)

competitiveness of any sorghum variety. Farmers are unlikely to be

persuaded to grow a variety with too much yield drag unless the in-
centive is exceedingly strong. Important advances have been made in
making the high 3-deoxyanthocyanin black sorghums agronomically
sorghum vs whole wheat biscuit.

competitive (Rooney et al., 2013).

intake at subsequent meal.

Because the bran where the grain pigments are located is largely a
waste product of sorghum processing (milling, alcohol production), the
additional value added by its valorization would significantly enhance
sorghum competitiveness. When non-grain biomass is targeted for
Main Effect(s)

pigment accumulation, there should also be significant value attached

to the rest of the plant, e.g., grain, sugar, or cellulosic biomass pro-
wheat.

duction, to ensure competitiveness of the strategy. Nevertheless, sor-

ghum grain and other tissue have a major advantage as sources of
natural food pigments related to ease of handling compared to fruit and
Sorghum extrudate in beverage (N = 10)
Whole grain red sorghum flaked biscuit

Extruded sorghum ready-to-eat cereal

vegetable sources of anthocyanins. The sorghum tissue is non-succu-

Whole grain sorghum flaked biscuit

lent, and is typically harvested at low moisture thus is easy to dry and
Sorghum flour in pasta (N = 20)

store for long periods at low cost. Fruits and vegetables, on the other
hand, are high in moisture and enzyme activity, thus are relatively
expensive to store and process. Furthermore, levels of pigments derived
from sorghum at the moment compete favorably with anthocyanin
content in commercial pigment sources (Petti et al., 2014).
Another genetic strategy could target the composition of the 3-
(N = 40)

(N = 60)

(N = 58)

deoxyanthocyanins and their copigments in the plant tissue, because

Matrix

such attributes impact color properties and stability (Awika, 2008). In

altering 3-deoxyanthocyanin composition, the most obvious strategy
would be to identify genes responsible for synthesis of the dimeric and
Whole grain tannin sorghum with 3-

pyrano-3-deoxyanthocyanins and determine how the plant can be ma-

nipulated to increase the content of the highly stable forms of the
Whole grain tannin sorghum

pigments. Additionally, copigment polyphenols produced in conjunc-

Whole grain red sorghum

Whole grain red sorghum

tion with the 3-deoxyanthocyanins can have significant impact on

Whole grain sorghum
Bioactive component

overall color properties and stability of the pigments; phenolic com-

deoxyanthocyanins

pounds common in sorghum, like tannins and ferulic acid can sig-
nificantly increase aqueous stability of the 3-deoxyanthocyanins
(Awika, 2008). Recently, agronomically competitive sorghums that
accumulate high levels of the 3-deoxyanthocyanins along with con-
densed tannins have been developed (Hayes and Rooney, 2014), and
some have found commercial application in foods (Awika, 2017).
Biotechnology also presents an attractive avenue to enhance the
functionality of sorghum 3-deoxyanthocyanins, e.g., through microbial
transformation. For example, Bai et al. (2014) recently reported that
Improve glycemic response

Improve glycemic response

Improve glycemic response

sourdough fermentation of sorghum containing 3-deoxyanthocyanidins

Potential Health Benefit

using Lactobacillus plantarum resulted in the production of corre-

Table 2 (continued)

Anti-inflammatory

sponding pyrano and vinyl-phenol adducts of 3-deoxyanthocyanidins.

Antioxidant

The authors further demonstrated that the 3-deoxyanthocyanidin de-

Antioxidant

rivatives were the result of microbial decarboxylation of hydro-

xycinnamic acids into products that reacted with the 3-deox-
yanthocyanidins. The evidence suggests that under the right conditions,
the 3-deoxyanthocyanidins could be transformed into exceptionally

117
A.L. Girard, J.M. Awika
stable derivatives through fermentation thus further expanding com-
mercial application of the sorghum pigments.
Lastly, processing technologies that optimally extract and process
the pigments, and utilize them in appropriate food systems to ensure
maximum impact on food quality at attractive cost will go a long way in
ensuring sustainable application of the 3-deoxyanthocyanins. For ex-
ample, due to their thermal stability (Yang et al., 2014), microwave
assisted extraction can potentially enhance efficiency of extraction of
the 3-deoxyanthocyanins from sorghum grain tissue. Also, alkaline
conditions were recently shown to enhance extraction efficiency of
apigeninidin pigments from sorghum leaf sheath (Akogou et al.,
2018a,b). Beyond improved extraction methods, mechanisms to stabi-
lize the 3-deoxyanthocyanins in aqueous systems are also essential due
to their increased hydrophobicity and tendency to self-associate in
aqueous environment (Awika, 2017). For example, encapsulation
technologies could be used to stabilize the pigments in water-based
products such as soft drink-type beverages.
Another area with significant potential is in the use of whole grain
and/or bran fractions directly in foods to impart desirable natural color
while adding other benefits related to dietary fiber and slow digesting
starch, (Dunn et al., 2015; Stefoska-Needham et al., 2016). While such
strategy is relatively economical compared to pigment extraction, it
provides limited flexibility due to the propensity of the bran tissue to
interfere with/impact functionality of other ingredients, thus affect
food quality is used beyond certain levels.
An interesting potential use of the pigments as caramel color al-
ternatives was recently proposed; a patent application demonstrated
the 3-deoxyanthocyanins form stable brown color upon prolonged
thermal treatment at alkaline pH (Pietsch et al., 2018), likely through
alkali-induced oxidative condensation of the pigments. Caramel color
replacement would be an intriguing opportunity, given on-going con-
cerns about safety of some types of caramel colors processed using
ammonia compounds (class III and IV caramel) due to formation of the
potential carcinogen, 4-methylimidazole (Moon and Shibamoto, 2011).
Caramel is the most widely used food colorant, thus the application
could be significant.
5.2. Sorghum flavones and flavanones
Apart from the 3-deoxyanthocyanins, flavones and flavanones are
the other major monomeric flavonoids in sorghum (Dykes et al., 2009,
2011). The flavones and flavanones share the 4-quinone structure
(Fig. 1). The primary difference in the structure of the two flavonoid
groups is that the flavones have a C2=C3 double bond, thus are con-
jugated and relatively planar. The flavanones, on the other hand, are
chiral at C2 due to the saturated C2–C3 structure, which twists the B-
ring almost 90° relative to the chromone (A-C) ring (Awika et al., 2018).
The structural difference is highly relevant because there is a good body
of evidence that indicates the C2=C3 structure is a major determinant
of the bioactive potency of the flavonoids against various disease tar-
gets (Kim et al., 2004; Wang et al., 2018; Yang et al., 2015).
5.2.1. Sorghum flavones
Of all the phenolic compounds present in cereal grains, the flavones
may be the most biologically ‘valuable’ to human diet, because most
commonly consumed food plants (fruits, vegetables, legumes, and tu-
bers) lack meaningful levels of the flavones (Zamora-Ros et al., 2016).
Interestingly, most cereal grains contain flavones (mainly as C-glyco-
sides of apigenin, and luteolin) as the primary or major component of
their flavonoids (Awika et al., 2018). However, levels of flavones in
most cereal grains is modest, with the exception of some millets like
pearl millet, fonio, and teff that can contain > 1000 μg/g (Ravisankar
et al., 2018; Sartelet et al., 1996). Nevertheless, cereal grains remain
the most important dietary source of the flavones due to their dominant
role in the human diet (Awika et al., 2018; Zamora-Ros et al., 2016).
The levels of flavones in sorghum is similar to wheat, the major
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Journal of Cereal Science 84 (2018) 112–124
cereal grain with the highest levels of the compounds, and thus the
currently most important dietary source (Table 1) (Awika et al., 2018).
In contrast to the 3-deoxyanthocyanins, significant proportions of the
sorghum flavones exist as glycosides; interestingly, luteolin derivatives
of sorghum are dominated by glycosides, whereas apigenin derivatives
are mostly present as aglycones (Yang et al., 2012, 2015). Key struc-
tural differences that are biologically relevant exist between sorghum
flavones and those found in other cereals. The sorghum flavones are
mostly O-glycosides or aglycones, whereas other cereal grains contain
primarily C-glycosides (Hernández et al., 2011; Ravisankar et al., 2018;
Yang et al., 2015). In addition, both luteolin and apigenin derivatives
are often present in significant quantities in the same sorghum variety
(Dykes et al., 2009, 2011); by contrast most other cereal grains contain
mainly apigenin glycosides (Hernández et al., 2011; Martínez et al.,
2018).
The structural differences of sorghum vs other cereal flavones are
important because, for one, the O-glycosides are readily hydrolysable in
acidic pH (stomach conditions) (Yang et al., 2015) and by lactic acid
bacteria, thus are likely to provide more bioaccessible flavone agly-
cones in the upper gastrointestinal tract. Improved potential bioavail-
ability of flavones is particularly important because, as previously
noted, flavones appear to be among the least consumed dietary poly-
phenols (Zamora-Ros et al., 2016). On the other hand, the C-glycosides
are acid-stable and are also poorly bioavailable in the upper gastro-
intestinal tract, thus may require specialized metabolism by colon mi-
crobiota to improve their bioavailability (Xiao et al., 2016). Ad-
ditionally, luteolin derivatives contain the catechol group on the B-ring,
which may influence their bioactivity relative to the apigenin deriva-
tives without the catechol group (Wang et al., 2018).
5.2.2. Sorghum flavanones
Unlike flavones, flavanones are generally rare in cereal grains, at
least in meaningful quantities. The limited literature we found men-
tioning flavanones in some cereal grains in general did not provide
strong enough evidence on compounds identification to be deemed
credible. Sorghum appears to be an exception among cereals, with
among the highest levels of flavanones of food plants (up to 1800 μg/g)
identified in specific phenotypes with a lemon-yellow pericarp color
(Dykes et al., 2011; Yang et al., 2015). However, even in sorghum, the
flavanones are only found in specific phenotypes (Awika et al., 2018),
indicating a strong genetic component in their accumulation. The ap-
parent limited distribution of flavanones in cereal grains in general is
somewhat surprising, given naringenin, the most common flavanone, is
a common intermediate in the biosynthetic pathway of all other fla-
vonoids. The sorghum flavanones mostly exist as O-glycosides, and
their aglycones are relatively limited (Yang et al., 2012, 2015). The
flavanone O-glycosides are especially sensitive to acidic pH, and readily
hydrolyze into their aglycones (Yang et al., 2015), indicating they are
also likely to be readily accessible in the upper GI tract.
5.3. Sorghum flavones and flavanones as bioactive food ingredients
The contribution of the monomeric flavonoids to health benefits of
whole grain intake has not been the subject of much investigation. This
is primarily because, as previously mentioned, the flavonoids are rela-
tively minor components of cereal grain phenolics compared to the
phenolic acids. However, it is well known that the structure of the
phenolic compounds has a major impact on their bioactivity (Awika
et al., 2018). This implies that more attention should be paid to the
composition of specific compounds, and not just the phenolic content
when assessing potential impact of a commodity on human health, as
has been common practice.
Based on documented structure-activity relationships, flavonoids
with a planar structure, i.e., C2=C3 double bond, are more bioactive
against numerous disease targets compared to those with a saturated
C2–C3 structure (Gonzales et al., 2015; Wang et al., 2018). For
A.L. Girard, J.M. Awika
example, apigenin has been shown to be more effective than naringenin
in preventing estrogen-beta (ER-β) receptor dependent colon carcino-
genesis, as well as modulating various inflammatory pathways (Lim
et al., 2013; Yang et al., 2015). Furthermore, sorghum extract higher in
apigenin (but low in total polyphenols) was found to protect ovar-
iectomized mice against azoxymethane-induced aberrant crypt foci
formation in mice colon better than a higher total polyphenol extract
lower in flavones (Yang et al., 2014). The enhanced activity was at-
tributed to better ER-β activation by the flavone, apigenin, relative to
the other phenolic compounds in sorghum (Yang et al., 2015). Similar
superior potency has been reported for the planar flavonol (3-hydro-
xyflavone), quercetin, relative to its chiral 3-hydroxyflavanone (flava-
nonol) analog, taxifolin, in activating aryl hydrocarbon receptor (AhR)
and inducing CYP1A1 gene expression in HepG2 cells (Vrba et al.,
2012). The planar configuration likely favors better flavonoid interac-
tion with specific cellular receptors (Agah et al., 2017; Wang et al.,
2018).
It, therefore, appears that despite their relatively low content in
sorghum compared to other flavonoids, the flavones may be more re-
levant to disease prevention than presumed. The unique role of flavones
in the health benefits reported for whole grain intake thus deserves
scrutiny. The bioactive properties of the flavones indicate that low
polyphenol grains with specific composition of structurally desirable
bioactive compounds can prove more beneficial to disease prevention
that the high polyphenols grains commonly presumed to be better.
Because, in the most part, higher polyphenol sorghum grains tend to be
less preferred by consumers due to undesirable impact of the com-
pounds on sensory appeal (Awika, 2017), enhancing flavone content in
sorghum may be an excellent strategy to expand intake and benefits of
whole grain sorghum. This is because low polyphenol grains with high
sensory appeal that are also high in bioactive properties could be fea-
sible. In fact, in the study using the ovariectomized mice described
previously (Yang et al., 2014), the more functional extract was from a
traditional food-type white sorghum, while the less functional one was
from a high polyphenol black sorghum.
A practical strategy that could significantly increase the health
benefits derived from the sorghum flavones is through strategic com-
bination of high flavone sorghums with other grains or foods that
contain flavonoids that enhance the action of the flavones through sy-
nergistic interactions (Agah et al., 2017; Awika et al., 2018; Yang et al.,
2015). For example, we recently found that the sorghum flavanones
were able to significantly enhance ability of sorghum flavones (by a
factor of at least 10 X) to activate ER-β receptor in non-malignant co-
lonocytes, and thus potentially contribute to enhanced colon cancer
prevention (Yang et al., 2015). The positive interaction indicates that
sorghums that contain both groups of compounds, e.g., some red and
lemon-yellow varieties, could be important targets for health food ap-
plications. Furthermore, sorghums containing flavones could be used
with other ingredients high in flavanones (e.g., certain fruits and ve-
getables) to produce novel foods with improved bioactive functionality.
Another recent study found that the sorghum flavones were strongly
synergistic with flavonols derived from the legume, cowpea, at redu-
cing LPS-induced NFκ-B and downstream inflammatory cytokines in
intestinal myofibroblasts (Agah et al., 2017). The finding is highly re-
levant to everyday diet because many cultures around the world con-
sume cereals and pulses/legumes together as staples (Awika et al.,
2018). Furthermore, flavonols are the most widely distributed flavo-
noids in various pulses including common beans (Awika and Duodu,
2017; Awika et al., 2018; Beninger et al., 1999; Ojwang et al., 2012;
Wang et al., 2010). Thus processing technologies that creatively in-
corporate whole grain sorghum with pulses into products that meet
modern consumer needs would be highly beneficial. The increased in-
corporation of pulses in traditionally cereal-based foods, like snack
chips and breakfast cereals (Awika, 2017) is a strategy that can be
exploited.
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Journal of Cereal Science 84 (2018) 112–124
5.4. Sorghum proanthocyanidins (condensed tannins)
Proanthocyanidins, or condensed tannins, in sorghum have been the
subject of long-term investigations mainly due to their documented
negative consequences on sorghum feed value, particularly for poultry
and monogastric mammals (Awika and Rooney, 2004; Mitaru et al.,
1984), which has been confirmed by more recent studies (Pan et al.,
2018). Tannins bind readily to proteins, forming complexes that can
resist protease enzyme hydrolysis. The tannin-protein interaction can
also denature enzymes and thus lead to direct digestive enzyme in-
hibition, especially when the tannins are present in a form that can be
readily released from a food matrix. The combined effect may reduce
protein digestibility by as much as 70% (Mitaru et al., 1984). In gen-
eral, however, animals have adaptive responses to negate the undesir-
able effects of tannins to some extent; part of the adaptation is believed
to be via binding of the tannins by salivary proline-rich proteins thus
reducing their impact in the digestive tract. Consequently, the effects of
sorghum tannins on protein digestibility is strongly dependent on the
content of tannins in the grain or food matrix (Awika and Rooney,
2004; Mitaru et al., 1984).
Condensed tannins are not unique to sorghum; other cereal grains
contain these compounds, including red wheat, barley, some millets,
and pigmented rice (Chandrasekara and Shahidi, 2011; McCallum and
Walker, 1990; Pereira-Caro et al., 2013; Ravisankar et al., 2018;
Verardo et al., 2015). However, negative nutritional impact of the
tannins in the other cereal grains has not been reported. This is likely
due to the fact that the levels of tannins in the other cereal grains is
relatively low compared to sorghum varieties known to have reduced
nutritional value, the type III tannin sorghums. The type III sorghums
can have tannin levels that are more than 10-fold higher than reported
for other cereal grains (Table 1). The adaptive animal response may
readily overcome the low tannin levels in the other cereal grains. Be-
sides content, sorghum tannins also have higher average MW than other
cereal grain tannins, with mean DP of approx. 20 compared to other
grains containing mainly oligomeric proanthocyanidins (DP 3–10)
(Girard et al., 2018; Martínez et al., 2018; Pereira-Caro et al., 2013).
Higher MW tannins are known to have higher affinity for proteins
(Girard et al., 2018), thus are more likely to impact protein digest-
ibility.
However, it is important to point out that only a very small sub-
fraction of commercially produced sorghum varieties, especially in N.
America, contain tannins. Because the genetics that control tannin
synthesis in sorghum is well known, breeding efforts to remove the
tannins from commercial sorghum production have been very suc-
cessful. Such efforts have been motivated primarily by the negative
impact of tannins on feed nutritive value of sorghum. At present, tannin
sorghums are mainly commercially produced in some regions of Eastern
and Southern Africa and South America, as a matter of necessity. An
important practical benefit of tannins is that they can significantly re-
duce bird pest predation of sorghum grain in the field, and regions that
produce tannin sorghums usually have high bird pressure (Awika,
2017). Nevertheless, non-tannin sorghum producing regions, like the
US, are beginning to see some interest in contract production of tannin
sorghums due to a growing interest in health food applications (Awika,
2017).
5.5. Sorghum proanthocyanidins as bioactive food ingredients
An immediate concern when considering tannin sorghums as func-
tional food ingredients is the potential impact of tannin on product
sensory attributes. Tannins are known to have astringency and some
bitterness associated with them. However, importantly, these attributes
normally require that the tannins be chemically available to interact
with salivary proteins and taste receptors on the tongue. Therefore,
tannins in products like red wine that are mostly free in solution pro-
duce an easily perceptible sensation. On the other hand, due to their
A.L. Girard, J.M. Awika
affinity for proteins and other macronutrients, we believe the sorghum
tannins are not likely to produce such sensory attributes in most foods,
because they will be chemically bound during processing, and thus
become largely unavailable to interact with salivary proteins and taste
receptors in the mouth. The hypothesis is, perhaps, strengthened by a
recent study that found consumers actually preferred the flavor and
overall quality of a powdered drink made using tannin sorghum com-
pared to a non-tannin sorghum (Queiroz et al., 2018). A previous study
also reported similar astringency and bitterness scores for a tannin vs a
non-tannin sorghum (Kobue-Lekalake et al., 2007). Thus, evidence in-
dicates that sorghum tannins are not likely to negatively impact sensory
properties in food products.
Owing to their polymeric structure, the sorghum tannins can impact
human health via multiple ways, including interaction with macro-
nutrients, direct bioactive action, and interactions with gut microbiota.
In this regard, perhaps one of the biggest potential applications of
tannin sorghums to impact human health is in the calorie reduction
area. Excess calorie intake is the dominant global nutritional problem at
present, and is associated with a host of chronic diseases in both the
developed and, increasingly, in the developing world (Awika, 2011,
2017).
As previously stated, the ability of sorghum tannins to bind proteins
also results in their ability to inhibit digestive enzymes as well as
membrane transporters involved in nutrient transport. For example,
Anunciação et al. (2018) recently showed that when humans consumed
a tannin sorghum-based drink 30 min prior to a 25 g glucose solution, a
reduced glycemic response was observed compared to non-tannin sor-
ghum drinks or control. The reduced glycemic response suggests that
the sorghum tannins partially inhibited the action of membrane glucose
transporters. Another study in which sorghum tannins were delivered
to the rat small intestine in free form (via encapsulation) reported
significant reduction in postprandial glucose response from starch
feeding (Links et al., 2016), which could be via a combination of
amylase enzyme and glucose membrane transporter inhibition. These
properties would benefit diabetes control as well as potentially im-
proving satiety.
Besides binding to proteins, tannins from sorghum have recently
been found to directly complex starch, especially amylose, and lead to
formation of slow digesting and resistant starch (Amoako and Awika,
2016a; b; Barros et al., 2012). Starch binding is particularly relevant
because starch is the major source of calories from cereal grains, and in
human diets in general. Besides potentially reducing caloric load of
starchy foods through resistant starch formation, the tannins could also
benefit diabetics by slowing postprandial blood glucose release from
starch-based foods, via increased slow digesting starch content. Sor-
ghum tannins could be useful as a tool to produce naturally modified
starch ingredients with improved nutritional profile. Additionally, even
in a matrix that includes proteins, like whole grain or wheat gluten
containing food system, the sorghum tannins were still effective at
slowing the rate of starch digestion (Austin et al., 2012; Dunn et al.,
2015; Mkandawire et al., 2013), indicating potential to provide func-
tional benefits during normal food processing.
Sorghum tannins can also indirectly contribute to reducing un-
desirable consequences of excess calorie intake through various other
mechanisms, e.g., antiinflammatory function and inhibition of lipo-
genesis (Table 2). For example, Arbex et al. (2018) recently reported
significant reduction in lipogenesis and epididymal adipose tissue in
high fat diet fed obese rats when extrudes tannin sorghum replaced
starch and cellulose fiber. Furthermore, the authors reported that the
proinflammatory cytokine TNF-α was significantly decreased, whereas
the anti-inflammatory cytokine IL-10 was significantly increased in the
sorghum fed rats (Arbex et al., 2018). Tannin sorghum also reduced
liver weight of obese rats, along with expression of genes which lead to
hepatic lipogenesis (de Sousa et al., 2018). Thus, sorghum tannins de-
rived from whole grain sorghum, sorghum bran, or in extracted form,
can provide flexible opportunities to formulate products that benefit
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Journal of Cereal Science 84 (2018) 112–124
efforts to reduce diet-induced weight gain.
One of the more well-known properties of tannins is their powerful
antioxidant activity. However, because the high MW tannins are not
directly bioavailable, there has been a question as to whether the an-
tioxidant property can translate into meaningful biological benefit.
Because tannins were found to retain significant antioxidant activity
even when complexed to proteins, Riedl and Hagerman (2001) pro-
posed that the sorghum tannins could function as biological free radical
sinks in the GI tract, thus sparing other dietary antioxidants. Evidence
also indicates that the tannins undergo extensive metabolism in the
colon to produce phenolic metabolites that enter systemic circulation
(Gu et al., 2007) and may thus provide additional benefits against
oxidative stress, colon health, among others.
An industrial application that exploits the antioxidant property of
the tannins could be in food preservation. Because of their relative
hydrophobicity, the sorghum tannins could be valuable additives to
slow lipid oxidation in products like sausages, or high fat baked goods.
For example, sorghum tannins were reported to reduce lipid oxidation
in precooked pork and turkey patties to levels similar to or better than
the standard chemical antioxidants BHA/BHT, without any adverse
effects on flavor (Luckemeyer et al., 2015). Interestingly, the authors
used the bran, and not extracted tannins, which suggests tannin sor-
ghum could serve as an economical source of natural food preservative.
Sorghum derived tannins could also find new uses as high value
ingredients to naturally modify and expand protein functionality. The
ability of tannins to complex proteins has been long used industrially to
denature hide proteins to produce leather, or to clarify beer. The
property can also potentially be used to enhance protein film integrity
(Taylor et al., 2007). New evidence indicates that the polymeric sor-
ghum tannins can dramatically alter gluten rheological behavior (Dunn
et al., 2015; Girard et al., 2016, 2018). For example, despite being
strong antioxidants, a property known to weaken gluten by breaking
disulfide linkages, the sorghum derived tannins were found to drama-
tically increase gluten strength and mixing tolerance, much more so
than grapeseed tannins (Girard et al., 2016). The effect was primarily
attributed to the high MW sorghum tannins complexing high MW
glutenin subunits of gluten proteins, thus increasing protein polymer
size (Girard et al., 2018). Strengthening effect of sorghum tannins on
gluten provides a good opportunity to naturally improve gluten quality,
an important attribute considering the growing consumer concern, as
well as regulatory pressure, about artificial flour additives. The func-
tional attribute of sorghum tannins could also enhance ability of gluten
to function as a biofilm, encapsulating agent, texturizer, and related
applications.
Sorghum tannins can thus find broad applications due to their di-
verse functional properties that encompass food quality improvement,
expanding ingredient functionality, extending food shelf life, and pro-
moting human health, especially in reducing caloric impact of food and
associated negative consequences. Their high molecular weight profile
appears to significantly enhance the functional attributes of sorghum
tannins relative to tannins from other common food sources. The evi-
dence that indicates the tannins do not negatively impact sensory at-
tributes of foods when complexed with other food macromolecules
should help motivate product innovations utilizing the highly func-
tional sorghum tannins. Human intervention studies that demonstrate
the long-term benefits of the sorghum tannins against weight gain and
key disease targets are highly needed to motivate their use in foods.
With obesity becoming the dominant global health issue, such studies
are critically needed.
6. Whole grain sorghum and its endosperm in satiety and reduced
glycemia
Human studies linking sorghum intake to specific health outcomes
are limited. However, of the available evidence, the most consistent
thus far appears to be the ability of sorghum to reduce glycemic
A.L. Girard, J.M. Awika
response relative to other grains (reviewed by Simnadis et al., 2016).
The reduced glycemic response from sorghum consumption has been
observed independent of phenolic profile of the grain, indicating the
effect is largely due to the sorghum endosperm (Table 2). Various
mechanisms could contribute to this property, but they may be linked
to the ability of the sorghum proteins to cross-link and interact with
starch during hydrothermal food processing.
A related recent study comparing typical rural West African starchy
foods (e.g., sorghum and pearl millet thick porridges, millet couscous)
to urban starchy foods (e.g., rice, potato, pasta) found that the tradi-
tional sorghum and millet foods had a gastric emptying rate about 2X
longer than the urban foods (Cisse et al., 2018). The was true with both
thick porridges and non-viscous couscous, indicating the sorghum and
millets foods in different forms can potentially contribute to reduced
glycemic response and improved satiety compared to other starchy
foods. The factors that contribute to the slowed gastric emptying phe-
nomenon on sorghum and pearl millet need investigating, but may be
partly be related to the propensity for sorghum and some millet proteins
to extensively cross-link during hydrothermal processing to become less
digestible (Gulati et al., 2017; Hamaker et al., 1987).
Beyond the slower gastric emptying rate, slowed starch digestion
and beneficial effects on satiety have also been observed for sorghum.
For example, a study that fed men muffins made with whole sorghum
flour compared to whole wheat flour found that the sorghum muffins
produced a reduced insulin and glucose responses; the mean incre-
mental area under curve (iAUC) for plasma glucose was reduced an
average of 35% with sorghum, and the insulin responses reduced by
55% (Poquette et al., 2014). In a related randomized crossover study
(N = 40), participants consumed whole grain biscuit and their sub-
jective satiety and biomarkers measured (Stefoska-Needham et al.,
2016). All varieties of sorghum tested (white, red, brown/tannin)
yielded higher satiety than whole wheat biscuit, and resulted in higher
postprandial glucagon-like peptide-1 (GLP-1) and glucose-dependent
insulinotropic polypeptide (GIP) levels (Stefoska-Needham et al.,
2016). Again, the evidence indicates that sorghum endosperm con-
tributes to the beneficial effects on glucose metabolism.
Another study by the same group reported significant improvement
in weight loss and secondary outcomes (i.e., fasting glucose, insulin,
cholesterol, and key inflammatory biomarkers) from baseline for sub-
jects consuming whole red sorghum flaked biscuits for 12 weeks
(Stefoska-Needham et al., 2017). However, the effects were similar to a
group that consumed whole wheat biscuits, indicating additional stu-
dies are essential to understand to what extent the sorghum endosperm
specifically influences glucose metabolism. Nevertheless, the study
highlights the fact that significant health benefits that can be derived
from whole grain sorghum consumption.
In general, the emerging evidence from human studies appears to
back up the satiating effect of sorghum that has thus far been largely
anecdotal. Furthermore, it appears to provide a rational basis for some
traditional uses of sorghum-based foods to help with various conditions,
like diabetes (Awika, 2017). More important, the human studies con-
firm that some of the unique properties of sorghum observed in the
laboratory are indeed relevant to human health. Such studies need to be
expanded to provide a more complete picture on the mechanisms and
impact of whole grain sorghum on human health. The interactive ef-
fects of the various sorghum polyphenol profiles with the sorghum
endosperm on the physiological properties of whole grain sorghum
should be investigated.
7. Sorghum as a uniquely functional food ingredient; challenges
and opportunities
7.1. Challenges
Despite its obvious advantages, sorghum faces numerous challenges
as a competitive ingredient in modern food processing. Cereal grains
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Journal of Cereal Science 84 (2018) 112–124
are primarily produced for their endosperm which is the most eco-
nomically valuable part of the seed. Therefore, sorghum endosperm
functionality is often judged relative to the more abundantly available
alternatives, especially rice and maize, and to a lesser extent, wheat.
This has essentially, created a no-win ‘me too’ competitive position for
sorghum. For one, the industrial milling technologies developed for
maize or rice are not ideal for sorghum, and there are generally no
sophisticated milling systems developed uniquely for sorghum.
Consequently, sorghum enters the food processing chain as a largely
disadvantaged ingredient due to sub-optimal milled product quality.
Beyond milling, technologies to optimally process sorghum in var-
ious applications are largely lacking. This is especially relevant, because
sorghum endosperm has some unique properties that may require dif-
ferent processing conditions from those designed for maize or rice to
obtain optimal product quality. The starch granules in the sorghum
corneous endosperm are surrounded by a matrix of hydrophobic kafirin
protein bodies, which reduces the extent of granule swelling during
hydrothermal treatment and can thus impact ability of starch to interact
with other ingredients during processing to produce desirable food
texture (reviewed by Taylor and Emmambux, 2010). In addition, during
cooking, the sorghum β- and γ-kafirins at the periphery of the protein
bodies, extensively cross-link, further inhibiting the ability of starch to
swell (Hamaker et al., 1987). Therefore, when sorghum is processed
using conditions designed for other grains, undesirable quality attri-
butes, like sandy/gritty or crumbly texture may be apparent. Ironically,
the sorghum kafirin cross-linking may also contribute to the reduced
glycemic properties of sorghum endosperm relative to other cereal
grains.
For above reasons, it is obvious that trying to fit sorghum into an-
other maize or rice alternative (e.g., in breakfast cereal or snacks) is not
likely to make sorghum a very successful mainstream food ingredient.
Sorghum must find its own niche and be marketed as a unique in-
gredient with compelling benefits that can spur sustainable demand
among consumers. From preceding discussions, it is obvious that health
benefits of the sorghum polyphenols and other components could be a
powerful driver for consumer demand. However, unfortunately, there is
very limited data documenting these benefits in large human inter-
vention studies. Because such studies are required to influence policy,
drive product marketing, as well as shape consumer perception, it is our
opinion that this is the most pressing critical challenge/need facing
sorghum as a food ingredient.
7.2. Opportunities
Even though attempts to introduce sorghum into modern food
processing systems have been on-going for a while, there has been no
better time to exploit the advantages of sorghum than today. A com-
bination of consumer interest in healthy eating, natural ingredients,
dietary diversification, environmental sustainability, and a host of other
emerging long-term trends seem poised to benefit sorghum utilization
in modern food systems in major ways. A diversity of products that
incorporate sorghum as a major ingredient are increasingly appearing
on grocery shelves (Awika, 2017). However, for sorghum to success-
fully compete, the limitations of sorghum and sorghum components as
food ingredients must be competently addressed. Furthermore, the
uniqueness of sorghum and its components must be emphasized and
innovatively exploited, beyond simply imitating other grains, to pro-
duce new products that excite consumers and sustain their interest.
Some of the key opportunities are highlighted below.
7.2.1. Sorghum as a whole grain ingredient
As a whole grain ingredient, sorghum can readily fit into various
food applications and blend well with other ingredients due to its mild
flavor. Because there is such diversity in sorghum pericarp color, the
grain provides opportunity to naturally produce different colors in
products that excite consumers and create different sensory
A.L. Girard, J.M. Awika
connotations. Furthermore, the fact that the sorghum pigments are
highly stable to various food processing conditions (Ojwang and Awika,
2008; Yang et al., 2014) imply that they are likely to provide stable and
predictable colors in products. Also, the fact that the different pericarp
colors are associated with different phenolic profiles with potentially
different health properties suggests that in future, as more data on
specific physiological benefits of the compounds become available,
sorghum-based products could be ‘color-coded’ for targeted benefits
against specific chronic conditions.
However, the key challenge of reduced sorghum endosperm func-
tionality must be effectively overcome to enable sorghum to fit better
into modern food processes and produce products with competitive
sensory appeal. It is worth noting that significant research effort is on-
going aimed at genetically developing sorghums with a more functional
endosperm protein matrix (Elhassan et al., 2015; Jampala et al., 2012;
Mezgebe et al., 2018; Teferra et al., 2019). The research is mostly
taking advantage of sorghum protein body mutation that was dis-
covered by Purdue University researchers in the 1990s (Oria et al.,
2000; Weaver et al., 1998). The mutant sorghums have irregularly
shaped protein bodies with prominent invaginations and increased
exposure of the hydrophilic α-kafirins (Oria et al., 2000).
The mutant protein body trait appears to make sorghum endosperm
more functional by improving the ability of sorghum proteins to absorb
water and interact with starch to produce desired viscosity during hy-
drothermal processing (Elhassan et al., 2015; Teferra et al., 2019). The
protein body mutation also improves nutritional quality of sorghum
protein by increasing its digestibility and lysine content (Teferra et al.,
2019; Tesso et al., 2006); a property that is especially relevant for po-
pulations that consume sorghum as staple. In all, the protein body
mutation has the potential to significantly expand sorghum food use by
making the grain easier to process into products with superior sensory
quality, using existing technology.
Transgenic approach has also been shown to alter functionality of
sorghum endosperm in a way that is beneficial to food processing and
quality. For example, transgenic sorghums with increased lysine con-
tent and protein digestibility produced by suppressing the synthesis of
mainly the cysteine-rich hydrophobic γ-kafirin, were shown to have
improved sorghum flour dough functionality and protein-starch inter-
actions during processing to produce higher pasting viscosity (Elhassan
et al., 2017). However, the potential acceptability of transgenic sor-
ghum in human food system brings its own set of challenges.
7.2.2. Sorghum components as high value functional ingredients
Besides whole grain, sorghum components can be used as a rich
source of specific bioactive components for a broader and more flexible
product application. Sorghum bran and spent brewers/distillers’ grain
are among the most prominent byproducts that are especially high in
the bioactive polyphenols (approx. 5 times higher than whole grain)
and other beneficial components like dietary fiber and bioactive lipids
(Althwab et al., 2015; Awika et al., 2005a,b). The advantage of using
the byproducts is that intended functionality/beneficial effects can be
achieved at low level of use, thus reducing the need to extensively
adjust formulations and processing conditions. For example, depending
on phenolic profile, the sorghum byproducts can find uses that vary
from serving as natural colorants, to helping reduce starch digestibility
(Dunn et al., 2015), and acting as natural antioxidant preservatives
(Luckemeyer et al., 2015).
Industrial use of isolated sorghum components is another promising
means to add value to sorghum by-products, as well as maximize the
flexibility of their applications. For example, as discussed in Section 5.1,
specific sorghums are rich in the unique and stable 3-deoxyanthocyanin
pigments that can potentially be economically extracted for use as
natural food colorants (Awika, 2017; Awika et al., 2005a,b; Geera et al.,
2012; Petti et al., 2014). The extraction approach can allow the pig-
ments to find widest application in products, including beverages,
dairy, baked goods, snacks, candy, etc. The sorghum tannins could find
122
Journal of Cereal Science 84 (2018) 112–124
broad uses as natural antioxidants to retard oxidative rancidity, or as
natural gluten strength improvers (Girard et al., 2016), as well as
provide a means to modify functionality of cereal proteins for biofilm or
biodegradable packaging applications (Girard et al., 2018; Taylor et al.,
2007). The tannins could also be used to produce novel naturally
modified starches with reduced digestibility for health food applica-
tions (Amoako and Awika, 2016a; b). Furthermore, the isolated sor-
ghum polyphenols could also find use as dietary supplements that
target specific chronic conditions.
8. Summary and future prospects
Sorghum has immense potential as a food ingredient to benefit
human health due to its versatility and composition. Its unique phyto-
chemical profile, coupled with the relatively slow digesting nature of its
endosperm, have been demonstrated to contribute to superior benefits
against various chronic disease targets compared to other cereal grains.
Even though data on human intervention is limited, the emerging evi-
dence indicates whole grain sorghum and its components can improve
glucose metabolism and insulin sensitivity, enhance lipid metabolism,
reduce low-grade chronic inflammation, and promote satiety through
slowed gastric emptying. However, there is limited data on how the
various bioactive components in sorghum interact to produce the
beneficial effects, as well as the mechanisms involved. Such data is an
especially critical piece of the puzzle, considering sorghum has a highly
diverse phenolic profile. The available in vivo and in vitro data suggest
that the phenolic profile of sorghum has a major impact on the specific
physiological responses relevant to disease prevention, indicating sor-
ghum phenolic composition must be factored into future studies aimed
at documenting effects of sorghum intake on chronic disease preven-
tion.
Significant headway has been made in overcoming the key chal-
lenges that have traditionally hampered sorghum use as a food in-
gredient. For example, the new sorghums with improved endosperm
functionality through altered protein body structure, currently under
genetic development, have the potential to dramatically enhance sor-
ghum application in existing food processing systems. The new dis-
coveries on unique functional properties of sorghum components, like
the proanthocyanidins and the 3-deoxyanthocyanins, will likely lead to
isolation and use of such components as high value ingredients to en-
hance food quality and health attributes, as well as use as therapeutic
agents. Application of biotechnology, e.g., through microbial structural
modification, appears poised to further enhance the functionality and
value of the sorghum components.
Conflicts of interest
None declared.
Funding
This work did not receive any specific grant from funding agencies
in the public, commercial, or not-for-profit sectors.
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