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Journal of Cereal Science 67 (2016) 83e91

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Journal of Cereal Science


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

Gluten-free breadmaking: Improving nutritional and bioactive


compounds
Vanessa D. Capriles a, *, Fernanda G. dos Santos a, Jose
 Alfredo G. Are
^as b
a
Departamento de Bioci^ ~o Paulo, Rua Silva Jardim, 136, CEP 11015-020, Santos, SP, Brazil
encias, Campus Baixada Santista, Universidade Federal de Sa
b
Departamento de Nutriça~o, Faculdade de Saúde Pública, Universidade de Sa
~o Paulo, Avenida Doutor Arnaldo, 715, CEP 01246-904, Sa~o Paulo, SP, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: This review focuses on the contemporary approaches that are used to increase nutrient and bioactive
Received 6 June 2015 compound contents of gluten-free bread (GFB), and highlights the use of nutrient-dense alternative raw
Received in revised form materials, nutritional and functional ingredients, and their combinations. Few studies address micro-
12 August 2015
nutrient fortification in GFB, and only one study has addressed the performance of in vitro trials to
Accepted 19 August 2015
Available online 20 August 2015
examine bioaccessibility. Some studies have demonstrated the potential use of nutrient-dense raw
materials, dietary fiber enrichment and technological processes in decreasing the GFB glycemic response,
which is evaluated through in vivo trials or by using the in vitro-predicted glycemic response method. The
Keywords:
Gluten-free
reviewed studies have shown promising approaches to overcoming both the technological and nutri-
Nutrition tional challenges involved in GFB development. However, further studies on the improvement or
Glycemic response development of new nutrient-dense GFB and their evaluation using digestibility, bioaccessibility, and
Sensory acceptance bioavailability trials are required to understand or improve their efficacy as vehicles of micronutrients
and bioactive compounds. In addition, short- and long-term controlled clinical trials are needed to
evaluate their potential health benefits. Furthermore, efforts to apply some of this promising research to
commercial products should be made to make GFB with good technological, sensory and nutritional
properties available to consumers with gluten-related disorders.
© 2015 Elsevier Ltd. All rights reserved.

1. Introduction trouble finding GF products because of high prices, limited variety


and availability and poor sensory properties. These factors are
The once small GF food market has experienced increased responsible for hampering adherence to the GF diet and for general
growth in recent years and has become a trend in the food sector. dissatisfaction (do Nascimento et al., 2014).
This growth has occurred primarily because of a GF craze that has Despite the considerable advances made in understanding and
made consumers avoid gluten because they believe that GF prod- improving GF systems by evaluating different ingredients, addi-
ucts are a “healthier” option and that a GF diet is an effective way to tives, and technologies over the past two decades, the development
lose weight, although there is no scientific evidence to support of GF products remains a technological challenge due to the role of
these beliefs (Brouns et al., 2013; Pszczola, 2012). For individuals gluten in various grain-based products. The technological challenge
with CD, dermatitis herpetiformis, gluten ataxia, wheat allergies increases according to the dependency of products' properties on
and gluten sensitivity, the GF food market segment is important for gluten, which is considerable in bread and pasta making (Capriles
assisting in their adherence to a strict GF diet (Sapone et al., 2012). et al., 2015). Bread is the most studied among all GF products.
Despite the growth of the GF market, individuals with CD still have However, a GFB with a good sensory aspect remains the most
desired product by individuals with CD (do Nascimento et al., 2014).
A range of GFB formulations have been developed by using rice
Abbreviations: CD, Celiac disease; DF, Dietary fiber; fwb, flour weight basis; GF, and maize flours, which are often combined with maize, potato, or
Gluten-free; GFB, Gluten-free bread; GI, Glycemic index; GL, Glycemic load; GR, cassava starches as base flours because they are widely available,
Glycemic response; HI, Hydrolysis index; HPMC, Hydroxypropylmethylcellulose;
inexpensive ingredients that are bland in taste and flavor. However,
ITFs, Inulin-type fructans; RS, Resistant starch; RSM, Response surface
methodology. these flours and starches have minimal structure-building potential
* Corresponding author. and, thus, are frequently used along with proteins and hydrocolloid
E-mail address: vanessa.capriles@unifesp.br (V.D. Capriles).

http://dx.doi.org/10.1016/j.jcs.2015.08.005
0733-5210/© 2015 Elsevier Ltd. All rights reserved.
84 V.D. Capriles et al. / Journal of Cereal Science 67 (2016) 83e91

binding agents and with other additives to improve GFB physical aminobutyric acid and polyphenols), increasing the antioxidant
properties, acceptance and shelf-life (Capriles and Are ^as, 2014). activity and reducing the phytic acid content and in vitro enzymatic
These GF flours and starches are not generally enriched or fortified, hydrolysis of starch.
and neither are the resulting GF products, in the same way as their Studies of composite GFB formulations have shown promising
wheat-based counterparts. Therefore, GF products may lead to results regarding the physical properties of GF dough and bread
nutritional deficiencies in micronutrients, protein and DF (do when using up to 70% sorghum flour in combination with corn,
Nascimento et al., 2013; Kinsey et al., 2008; Thompson, 2000). potato, rice, or cassava starches (Onyango et al., 2011; Schober et al.,
Thus, enhancing the nutritional quality of GF products remains an 2005).
important task for research and development, which is a Some researchers have investigated the feasibility of using
concomitant challenge towards the improvement of technological pseudocereals in GF breadmaking. Alvarez-Jubete et al. (2009a,
and sensory properties. 2009b, 2010a, 2010b) replaced potato starch with amaranth,
The development of GFB is still a challenge because no single buckwheat, or quinoa flour in a control formulation with 50% rice
raw material, ingredient, or additive can currently replace gluten flour and 50% potato starch. These pseudocereals increased the
fully. Nevertheless, great research advances have been made in this protein, fiber, calcium, iron, vitamin E, and polyphenol contents and
field. Several recent studies have used food science tools to improve the in vitro antioxidant activity of GFB. The GFBs containing pseu-
the technological and sensory qualities of GFB, together with the docereals presented a softer crumb texture and darker crust and
nutritional value (Capriles and Are^as, 2014). It is not the objective of crumb colors. However, no significant differences were observed
this review to list all of these advances. between the acceptability scores of the pseudocereal breads and
The primary focus of this review is to discuss the current ap- the control GFB, which resulted in medium acceptability (scores
proaches used to improve the nutritional and bioactive compounds ranging between approximately 2 and 3 on a 6-cm scale) (Alvarez-
of GFB. This review concentrates on contemporary GFB research (as Jubete et al., 2010c).
published since 2005), with particular focus on raw materials and In the production of acceptable GFB, researchers have reported
ingredients that improve the nutritional properties of GFB, espe- good results with rice-based composite flour that was made of up
cially the sensory-accepted ones. to 50% buckwheat (Alvarez-Jubete et al., 2010c; Torbica et al., 2010)
and with corn starch-based flour composed of up to 40% buckwheat
2. Nutrient-dense alternative raw materials flour (Wronkowska et al., 2010). These levels increased the nutri-
tion and antioxidant compounds and the antioxidant capacity of
Research has shown that some nutrient-dense alternative raw GFB.
materials that are derived from non-gluten cereals, pseudocereals, Marciniak-Lukasiak and Skrzypacz (2008) reported good results
legumes, nuts, seeds and fruit- and vegetable-based ingredients when adding 10% amaranth flour to the total GFB mass, which
can be used to develop GFB with good physical and sensory prop- increased the nutrient contents and resulted in approximately 50%
erties, along with enhanced nutritional composition (Capriles and consumer acceptability. Lemos et al. (2012) also observed the best
Are^as, 2014). results in a cheese bread with a mixture containing 10% amaranth
Despite their nutritional benefits, the use of whole grain flours flour, which increased the DF and iron contents and maintained the
and other alternative raw materials presents certain technological same level of acceptance as that of the control formulation (for a
limitations because these flours can change the appearance, color, score of 6.8 on a 9-point hedonic scale). Interesting results were
texture, aroma, and taste of GFB, which can easily impair consumer also found by de la Barca et al. (2010), who prepared 100% amaranth
acceptability. Consequently, nutrient-dense alternative raw mate- GFB with different ratios of popped and raw amaranth flour. The
rials have frequently been used in combination with conventional best formulation contained 60% popped amaranth flour and 40%
GF flours and starches (rice flour and starch, maize flour and starch, raw amaranth flour, which produced breads with a homogeneous
and potato, cassava and wheat starches) in composite GFB formu- crumb and a higher volume.
lations. However, some good-quality single formulations have also Legume flours have also been investigated in GFB formulations,
been developed. and promising technological and sensory results have been ach-
Various approaches have been applied to develop and improve ieved in composite formulations with soy, chickpea, carob germ,
the physical properties of GFB based on single formulations made and vinal (Minarro et al., 2012). Further research should evaluate
with whole grain maize, oat, and rice flours. The inclusion of oats in the acceptability and compositions of these breads. Tsatsaragkou
GF products has been controversial for years because although this et al. (2012) observed that the addition of 15% carob germ to a
ingredient can improve a product's quality and diversify the GF diet, rice-based GFB formulation resulted in a product with good phys-
it may contain gluten. Therefore, the allowance of pure oat in GF ical properties that was enriched with DF (6.1%) and protein (8.4%)
products is determined by each nation's labeling regulations. and was a source of some minerals. Interesting results were re-
Interesting results were obtained by Brites et al. (2010), who ported by Shin et al. (2013), who developed a 100% soybean GFB.
developed a GF “broa” bread formulation based on whole yellow Bread made with heat-treated soy flour (steaming or roasting) was
maize flour, which presents no significant differences compared perceived to have a less beany aroma and taste than a GFB made
with the sensory characteristics of maize- and wheat-based tradi- with non-heat-treated flour (germination).
tional broa in a paired preference test. Kim and Yokoyama (2011) Other alternative flours have been investigated, and promising
developed a formulation of all-oat breads with the addition of 5% results have been achieved with seeds and nuts. Costantini et al.
HPMC (fwb). Oat-based GF bread contains 1% b-glucan and has (2014) replaced common and tartary buckwheat flour with 10%
received sensory scores ranging from 4.3 to 5.1 on a 7-point he- whole chia flour and observed an improvement in the protein,
donic scale, with no acceptability difference compared with that of lipids, DF, ash, a-linolenic acid, and phenolic compound contents,
whole wheat bread. Interesting results were recently reported by and the antioxidant capacity of the formulations. Steffolani et al.
Cornejo et al. (2015), who investigated the effects of different (2014) observed that the replacement of rice flour with 15%
germination times (0, 12, 24 and 48 h) of brown rice flour on the whole chia flour or 15% chia seeds diminished the GFB physical
nutritional quality of brown rice flour-based GFB. The results show properties but did not reduce the medium overall acceptability (for
that germination for 48 h enhances the nutritional quality of GFB by scores of approximately 5, indicating neither like nor dislike, on a 9-
increasing the protein, lipid and bioactive compound contents (c- point hedonic scale). Demirkesen et al. (2010, 2013) studied the
V.D. Capriles et al. / Journal of Cereal Science 67 (2016) 83e91 85

potential use of chestnut and tigernut flours in GFB composite chickpea and sorghum (unpublished results). However, mixing
formulations by mixing different ratios of these flours with rice those alternative flours with rice flour and/or potato starch en-
flour. Breads with good physical properties were produced with hances the product's quality and acceptance. A GFB with good
mixes of rice flour with 10 and 20% tigernut flour, and rice flour physical properties and sensory acceptance (with appearance, co-
with 30% chestnut flour. lor, aroma, texture, flavor and overall acceptability scores that are
Interesting results have been achieved by incorporating fruit- higher than 7.0 on a 10-cm hybrid hedonic scale) could be prepared
and vegetable-based ingredients, such as raisin juice (Sabanis et al., with 15e65% unripe banana flour, 55e75% buckwheat flour, up to
2008), extracts from green kiwifruit puree (Sun-Waterhouse et al., 96% sorghum flour, and up to 100% chickpea flour (fwb).
2009), and by-products, such as defatted strawberry and black Table 1 presents the sensory acceptability scores of optimized
currant seeds (Korus et al., 2012), and orange pomace (O'Shea et al., GFB formulations containing nutrient-dense alternative raw ma-
2013) into GFB formulas, resulting in acceptable products with terials, and their comparison with white GF and wheat-containing
improved nutritional compositions. Sarawong et al. (2014) added counterparts. White GFBs were prepared with 100% rice flour and
30% unripe banana flour to a blend of rice flour and wheat starch to with a 50% rice flour and 50% potato starch blend (fwb). The GFB
improve the RS content of their GFB. These authors explained the formulations differ only in the flour mixture composition. Two
importance of the water content, baking temperature and baking wheat flour bread formulations were prepared, a standard wheat
time to achieve GFB with satisfying physical properties and the bread (AACC International, 2010) and an adapted formulation
highest RS retention levels. prepared with the same ingredient proportions as the GFB, except
So far, much of this research has focused on developing single or for the GF flours and hydrocolloids, which are replaced by wheat
composite flour GFB formulas by testing different ratios and flour and the appropriate addition of water.
assessing quality parameters for dough and bread. Little work has These new GFB formulations present physical properties that
been performed on defining and optimizing the alternative raw are slightly different from those of the two white GFBs. All GFBs
material levels based on statistical approaches. This type of work present a lower specific volume and higher crumb firmness and
could help when designing GF formulas that yield GFBs with moisture than their wheat-containing counterparts (unpublished
improved nutritional quality and sensory profiles. data). In Fig. 1, it is easy to observe the influence of alternative raw
In our research group, we are using mixture design experiments materials on the GFB appearance. However, these new GFBs present
to optimize GFB formulations based on non-gluten cereals, pseu- high consumer acceptability, with no difference in acceptability
docereals, legumes and other raw materials. A simplex-centroid scores compared with white GFBs and standard wheat bread,
design for mixtures of three ingredients was used to evaluate the except for GFB prepared with 64% buckwheat flour, which present
effects of rice flour, potato starch, and nutrient-dense alternative lower acceptability scores for color. The adapted wheat bread
flour, as well as their interactions, on GFB physical properties and formulation, which includes eggs and milk, had a higher texture
sensory acceptability. The maximum level (component and global acceptance score than the standard formulation. No
proportion ¼ 100%) of each of these ingredients was 100% of the differences in the aroma and taste scores were found between GF
flour mixture, 35.8% of the dough and 41% of the baked loaf. Opti- and wheat breads. GFBs prepared with sorghum or chickpea pre-
mized formulations were defined on the basis of the RSM to achieve sent high acceptability scores, similar to those of their wheat-based
alternative flour levels that could be used in a GFB formulation with counterparts.
high consumer acceptability. These results show that it is possible to use a high proportion of
Capriles and Are ^as (2010) were the first to use a mixture design nutrient-dense alternative flour (64e75% fwb) to develop well-
to optimize a GFB formulation. The optimized GFB (formulation 1: accepted GFB that can also be expected to produce a nutritionally
33.3% rice flour, 33.3% potato starch, and 33.3% amaranth flour; and superior product comparable to conventional ones. The proximate
formulation 2: 40% rice flour, 15% potato starch, and 45% amaranth composition and shelf life of these breads are under evaluation.
flour) presented high fiber contents (23.4 and 25% db, respectively)
and were sensory-accepted (overall acceptances of 7.4 and 6.6, 3. Nutritional and functional ingredients
respectively, on a 9-point hedonic scale). Information regarding the
effects of amaranth levels on the predicted GR of GFB is provided in Ingredients such as DFs, proteins and micronutrients have been
the fourth section of this review. used in GFB to improve nutrition and bioactivity. Dietary fibers are
The results of the recent mixture design experiments showed the most widely studied nutritional and functional ingredients in
that it is possible to produce a GFB with a single formulation based GFB. In some formulas, DFs also improve the physical and sensory
on unripe banana flour, whole flours derived from buckwheat, qualities, shelf-life, and nutritional composition of bread. Notably,

Table 1
Sensory acceptability scores of optimized gluten-free bread formulations containing nutrient-dense alternative flours, and their comparison with white gluten-free and wheat-
containing counterparts.

Base flours used for bread production Acceptability scores

Appearance Color Aroma Texture Taste Overall

65% unripe banana flour þ 23% potato starch þ 12% rice flour 7.6b ± 1.9 7.6bc ± 2.0 8.0a ± 1.8 7.7ab ± 1.8 7.5a ± 2.2 7.6 b ± 2.0
64% whole buckwheat flour þ 36% potato starch 7.5 b ± 1.6 7.1c ± 1.8 7.8a ± 1.7 7.6 b ± 1.7 7.6a ± 1.9 7.6 b ± 1.7
67% whole sorghum flour þ 33% potato starch 8.3ab ± 1.5 8.2ab ± 1.5 8.7ab ± 1.4 8.3ab ± 1.6 8.4a ± 1.5 8.3ab ± 1.4
75% whole chickpea flour þ 25% potato starch 8.7a ± 1.4 8.6ab ± 1.4 8.1a ± 1.8 8.0ab ± 1.8 8.1a ± 1.7 8.2ab ± 1.4
50% rice flour þ 50% potato starch 8.5ab ± 1.9 8.2ab ± 2.0 8.2a ± 1.8 7.8ab ± 2.1 7.9a ± 2.0 7.9ab ± 1.8
100% rice flour 8.3ab ± 1.9 8.4ab ± 1.8 8.0a ± 1.8 7.6b ± 1.8 7.9a ± 1.7 7.9ab ± 1.7
100% wheat flour e standard 8.4ab ± 1.9 8.3a ± 1.8 8.0a ± 2.1 7.6b ± 2.1 8.1a ± 1.9 7.9b ± 1.8
100% wheat flour e adapted 9.0a ± 1.2 9.1a ± 1.2 8.5a ± 1.9 8.8a ± 1.5 8.6a ± 1.6 8.9a ± 1.3

Values are means ± standard deviations (n ¼ 52) of acceptability scores on a 10-cm hybrid hedonic scale.
Values followed by a different superscript in each row are significantly different (P < 0.05).
Source: Adapted from Capriles et al. (2015), with permission from Nova Science Publishers, Inc.
86 V.D. Capriles et al. / Journal of Cereal Science 67 (2016) 83e91

Fig. 1. Appearances of central slices of optimized gluten-free bread formulations containing nutrient-dense alternative flours, and their comparison with white gluten-free and
wheat-containing counterparts.

increasing the amount of water is usually required in bakery for- from 4.4 (control formulation) to 5.9e7.7 on a 10-cm scale.
mulations that are enriched with DFs because of the high water- Soluble fiber and RS enrichment can decrease the GR of GFB,
binding capacity of fibers. Increasing the amount of water allows which is highly desirable for individuals with concomitant CD and
for the adequate dough viscosity, starch gelatinization, and protein insulin-dependent diabetes. The functional soluble fibers inulin,
denaturation that are required during baking (Capriles and Are ^as, oligofructose, oat b-glucan and psyllium have been applied to
2014). improve the technological, sensory and nutritional qualities of GFB.
The addition of DFs from cereals in GFB formulations has been Table 2 presents a summary of studies that have investigated the
studied. Sabanis et al. (2009a) developed a GFB containing 3% effects of bioactive polysaccharide on the sensory evaluation and/or
maize fiber, which yielded scores for color, appearance, flavor, DF content of GFB formulations.
texture, taste, and overall acceptability ranging from 7 to 8 on a 9- Because ITFs and b-glucan are partly degraded during the
point hedonic scale. In a subsequent study, Sabanis et al. (2009b) baking process, the quantities and molecular weights of the
applied RSM to optimize the maize fiber and water levels in the remaining compounds contribute to viscosity, which is an impor-
formulation. The optimal formulation contained 6.5% maize fiber tant factor related to functional properties that must be evaluated
and 102.5% water (fwb) and resulted in breads with enhanced (Capriles and Are ^as, 2013; Hager et al., 2011; Ronda et al., 2015). A
volume and crumb softness and 5.2% DF. Phimolsiripol et al. (2012) portion of the GFB (50 g) developed by Hager et al. (2011) contains
added 10% different fractions of rice bran to rice-based GFB and 0.75 g b-glucan, and the GFB studied by Ronda et al. (2015) contains
observed improvements in the physical properties and, conse- 0.70 g b-glucan, which can cause health effects because 3 g of b-
quently, an increase in the sensory acceptance, which increased glucan is the suggested daily intake for reducing postprandial

Table 2
Summary of studies that have investigated the effects of bioactive polysaccharide on the sensory evaluation and/or dietary fiber content of gluten-free bread formulations.

Bioactive polysaccharide Effects on some gluten-free bread properties References


(best level reported)
Sensory evaluation Dietary fiber content

Inulin (5% replacing starch) Class I (the highest quality) 1.5% inulin (Korus et al., 2006)
Inulin-type fructans mixture Enhance sensory overall acceptability score from 5.4 8% ITFs, 11% total dietary fiber (Capriles and Are^as, 2013)
50% inulin þ 50% oligofructose (28% fwb) (control bread) to 7.0 on a 9-point hedonic scale
Oat b-glucan (5.6% fwb) e 1.5% b-glucan (Hager et al., 2011)
Oat b-glucan (3.9% fwb) e 1.4% b-glucan (Ronda et al., 2015)
Psyllium (3% fwb) Sensory overall acceptability score of 6.6 on a 7-point e (Zandonadi et al., 2009)
hedonic scale. 100% overall acceptability (scores 5)
by celiacs and non-celiacs.
Corn resistant starch (20% replacing starch) e 6.3% dietary fiber (Korus et al., 2009)
^as (2014), with permission from John Wiley and Sons.
Source: Adapted from Capriles and Are
V.D. Capriles et al. / Journal of Cereal Science 67 (2016) 83e91 87

serum glucose and cholesterol levels. A portion of the GFB (50 g) electrolytic iron nearly causes no adverse changes in GFB. However,
developed by Capriles and Are ^as (2013) contains 4 g of ITFs, which this iron is usually poorly absorbed.
can provide health effects similar to those of prebiotics and can Krupa-Kozak et al. (2011) obtained significant calcium supple-
enhance calcium absorption. A prebiotic effect has been observed mentation in GFB with 2% calcium citrate and 1.3% calcium
with an intake of 5e8 g of ITFs per day, whereas calcium absorption citrate þ 0.7% calcium caseinate, which increased the calcium levels
enhancement was obtained by ingesting 8 g of an ITFs mixture per from 2.2 mg/100 g in the control bread to 469 mg/100 g and
day. Information regarding the effects of ITFs on GR of GFB is pro- 315.3 mg/100 g, respectively. Calcium-fortified GFB received a
vided in the fourth section of this article. Notable results were higher overall preference score than the control bread (4.7
obtained by Zandonadi et al. (2009), who developed a fiber- compared with 3.6, on a 10-scale unit). In a subsequent study,
enriched GFB that was well-accepted by celiac and non-celiac Krupa-Kozak et al. (2012) developed a GFB formulation that was
suffers (Table 2). enriched with 3.9% inulin, substituting for a similar starch level.
Proteins have been used to improve the physical, sensory and This formulation was fortified with different organic and nonor-
nutritional properties of GFB. Proteins are primarily used to build ganic calcium sources, providing an equal elementary calcium
up a network that can mimic some of gluten's properties, content (0.6%). The best results were achieved with the addition of
improving the rheological and baking properties of the dough and calcium carbonate, which raised the overall acceptability of this
the structural, sensory, and shelf-life characteristics of GFB. The GFB from 5.7 to 7 (on a 9-point hedonic scale), and increased the
most common protein sources in use are dairy, eggs, legumes, and calcium content from 0.15 to 10.85 mg/g.
cereals. Allergy or (lactose) intolerance issues must be considered Further investigations remain required in GFB mineral fortifi-
before developing, recommending, or consuming protein-enriched cation. In addition, vitamins such as vitamin D and folate should
GF products (Capriles and Are ^as, 2014). also be evaluated. So far, DFs are the only functional ingredients
Some studies have demonstrated the potential use of DF/RS in studied in GFB. Other functional ingredients used in wheat-
combination with proteins to improve the GFB quality. containing products should also be incorporated into GFB formu-
Tsatsaragkou et al. (2014) applied an RSM to optimize the RS, lations, such as omega-3 fatty acids, probiotics, phytosterols, and
protein, carob flour and water contents that were added to a rice others (Capriles et al., 2015).
flour-based formulation. The optimum formulation for obtaining
GFB with low crumb firmness and improved porosity values was 4. Studies of digestibility, bioaccessibility and bioavailability
achieved by combining 15% carob flour, 15% RS, 10% protein and
140% water (fwb). Kittisuban et al. (2014) used RSM to define the This section discusses the importance of studies on digestibility,
optimum HPMC, yeast b-glucan, and whey protein isolate levels in bioaccessibility and bioavailability to understand or improve the
a rice-based GFB formulation, considering comparable physical efficacy of GFB as a vehicle for micronutrients and bioactive com-
properties in wheat bread. The optimal formulation contained pounds. This topic could be important for research over the next
4.35% HPMC, 1% b-glucan, and 0.37% whey protein (fwb). This few years, along with short- and long-term controlled clinical trials
product had a well-accepted color (with a score of 7.1 on a 9-point to investigate their potential health benefits.
hedonic scale), with no observed differences compared with the Different in vitro and animal and human in vivo studies have
characteristics of wheat bread (score 6.8). However, this product been developed and applied, allowing for a better understanding of
presented moderate acceptability scores for texture, taste and the effects of food component mechanisms on human health.
overall acceptability (the scores ranged from 5.3 to 5.7), which are However, although in vivo feeding methods provide the most ac-
lower than the scores for wheat bread (the scores ranged from 6.8 curate results, these methods are time-consuming, costly, and
to 7.4). related to important ethical constraints. Thus, in vitro digestion
People who are undergoing GF diet treatment could be at risk of models offer a rapid, low-cost method for studying the digestibility
mineral and vitamin deficiencies because of the low micronutrient and release of food components under simulated gastrointestinal
contents in GF products. These products are frequently made by conditions and for screening samples for further in vivo studies
using refined GF raw materials and are generally not fortified like (Carbonell-Capella et al., 2014; Hur et al., 2011).
their wheat-based counterparts, which assume a central role in In vitro methods are used to assess bioaccessibility by evaluating
many national fortification programs. Therefore, studying and a food component releases from the food matrix, its transformation
optimizing the conditions of GFB fortification are important for during digestion conditions and/or assimilation through the
defining the compounds that provide the best results while also epithelium. In vivo methods are used to study bioavailability by
considering the sensory and technological quality, bioavailability assessing gastrointestinal digestion, absorption, metabolism, tissue
and economy feasibility. distribution and bioactivity (Carbonell-Capella et al., 2014). Di-
Research has been performed to define an iron or calcium gestibility refers to the fraction of food components that is trans-
compound that can be adequately absorbed and does not impair formed by digestion into potentially accessible material through
the sensory quality of GFB. Kiskini et al. (2007) used different iron physicochemical processes that occur in the lumen, which can be
compounds to fortify amaranth-based GFB. These authors observed assessed by in vivo or in vitro methods (Carbonell-Capella et al.,
that the most acceptable products were those fortified with ferric 2014).
pyrophosphate (trained panelists gave an overall quality score of Recognizing that none of the in vitro methods will absolutely
6.3 on a 10-cm scale) and ferric pyrophosphate (overall quality predict how much of a specific nutrient or bioactive compound will
score of 5.7). These scores were higher than those of the control be absorbed and used in the human body is important because
bread (overall quality score of 5.1). Details of the in vitro-predicted metabolic responses cannot be completely mimicked and can
bioavailability assay are provided in the fourth section of this determine significant differences with in vivo procedures. Notably,
article. In a subsequent study, Kiskini et al. (2012) compared the some in vitro procedures have yet to be validated against human
effects of different iron compounds on the physical and sensory absorption data. In addition, in vitro method protocols exhibit
characteristics of iron-fortified GFB (40 mg/kg solid compound). considerable differences that result in difficult comparisons
These authors observed that the addition of ferric pyrophosphate (Carbonell-Capella et al., 2014; Hur et al., 2011). In recognizing
and NaFeEDTA caused undesirable changes in the bread, such as a these limitations, in vitro studies could be an interesting tool for
dark crust and crumb and a metallic taste. The addition of scientific research, enabling a better understanding of the
88 V.D. Capriles et al. / Journal of Cereal Science 67 (2016) 83e91

digestibility and bioavailability of GFB. and par-baking and freezing technologies could decrease the GI and
This section presents some examples of the studies that have improve the GFB quality and shelf-life.
applied nutrient-dense alternative raw materials and/or nutritional Because of the cost and the labor-intensive and time-consuming
and functional ingredients in the formulation of GFB and have procedures associated with GI evaluation in humans, in vitro
evaluated the potential health benefits of these products through methods have been developed for estimating the GR of foods. These
in vivo trials or in vitro studies that have estimated the in vivo re- methods are based on the rate of available carbohydrate digestion,
sponses. To the best of our knowledge, the only health effect of GFB which refers to the percentage of available carbohydrate that is
evaluation with human volunteers has been the GR. hydrolyzed after 90e180 min of incubation, depending on the
protocol in use. The HI was then derived from the ratio between the
4.1. Approaches to reduce the glycemic response to gluten-free area under the hydrolysis curve of the tested and the reference food
bread (wheat white bread) over the same period. A reference material
assay (reference food, analytical standard or in-house reference
Because CD is associated with a high incidence of type I (insulin- material), together with the tested food, must be performed for
dependent) diabetes mellitus, the maintenance of a good glycemic internal quality control (Capriles et al., 2015). This HI was found to
control with adherence to a strict GF diet is an important task for be a good predictor of the GR from food ingestion and was highly
individuals with concomitant CD and insulin-dependent diabetes. correlated with the GI in vivo. The predicted GI (pGI) was estimated
Nevertheless, information about the GR of GF food is scarce. by using the equation established by Gon ~ i et al. (1997) as follows:
The GI and the resulting GL have been used as tools to compare pGI ¼ 39.71 þ 0.549HI, with a reported correlation coefficient of
and classify foods according to their postprandial GR. The GI is r ¼ 0.89, P < 0.05. Researchers also use the equation described by
defined as the indexing of the GR to a fixed amount of available Granfeldt et al. (1992), which is pGI ¼ 8.198 þ 0.862HI.
carbohydrates from a test food to the same amount of available Table 4 summarizes the research on the in vitro predicted GR of
carbohydrates from a reference food (glucose or white bread) when GFB.
consumed by the same subject (Jenkins et al., 1981). The GL is Segura and Rosell (2011) observed high pGI values in commer-
calculated as the product of the amount of available carbohydrates cial GFB. Capriles and Are^as (2013) observed a high pGI following
in a specified serving size and the GI value (when considering the ingestion of control GFB, and it was similar to that of wheat
glucose as the reference food), and then divided by 100 (Atkinson white bread. These data suggest that 8% ITFs enrichment reduced
et al., 2008). In using glucose as a standard food, the GI of food the pGI by 10% and the pGL by 14%. Nevertheless, the in vivo re-
can be classified into low (55), medium (56e69), and high (70); ductions were approximately triple the expected reductions based
and the GL can be classified into low (10), medium (11e19), and on in vitro analysis (Tables 3 and 4).
high (20) (Atkinson et al., 2008). Wolter et al. (2013) evaluated the in vitro starch digestibility of
Table 3 summarizes the existing research about the effects of basic GFB formulations that were prepared with single flours, and
nutrient-dense alternative raw materials, functional ingredients all products were categorized into high GI (70) and low GL (10).
and technological approaches on the GI and GL of GFB. These authors reported that smaller starch granules resulted in a
These results demonstrated that 8% ITFs enrichment decreased higher pGI because enzymatic hydrolysis is facilitated by smaller
the GR of GFB, resulting in a low-GI and low-GL product that starch granules. These authors also explained that the presence of
combined high acceptability and a physiologically significant sup- DF and hydrocolloids might influence the in vitro starch di-
ply of prebiotic soluble DF (Capriles and Are^as, 2013). In a subse- gestibility in the commercial sample. In a subsequent study, Wolter
quent study, Capriles and Are^as (2010) incorporated 33.3% and 45% et al. (2014) investigated the potential of sourdough application to
of whole amaranth flour into the previously developed 8% ITFs- reduce the pGI of the aforementioned GFB recipes. The predicted
enriched GFB formulation, which reduced the available carbohy- GIs were reduced upon sourdough addition in wheat, sorghum and
drate content and the GL. Amaranth flour levels were defined by the teff breads compared with that of the control (no sourdough
mixture design, as explained in the second section. Novotni et al. added). By contrast, increased pGIs were found in quinoa and
(2012) investigated the influence of sourdough addition on GI buckwheat sourdough breads. In addressing sourdough-containing
and quality parameters of GFB that had been partially-baked and GFB, these authors explained that the influence of the flour and the
frozen. Sourdough was fermented with a commercial Lactobacillus type of lactic acid bacterium strain must be considered for further
fermentum starter. The addition of 15 and 22.5% sourdough to the development of low GI products.
formulation significantly reduced the GI and also increased the de la Hera et al. (2014) assessed the effects of the rice flour
volume and crumb softness and delayed crumb firming. The re- particle size (fine and coarse) and dough hydration level on the
searchers concluded that the combined application of sourdough physical properties and the pGI of GFB. The pGI values ranged from

Table 3
Approaches to reduce the glycemic response to gluten-free breads (data obtained from glycemic index trials with human volunteers).

Gluten-free bread Glycemic indexa Glycemic indexa Serve Available Glycemic References
(bread ¼ 100) (glucose ¼ 100) size (g) carbohydrates load per
(g/serving) serving

- Control bread (prepared with rice flour and potato starch blend) 100.9 70.6 50 17.7 12.5 (Capriles and Are ^as, 2013)
- Bead enriched with 8% ITFs 68.5 47.9 50 16.9 8.1 (Capriles and Are ^as, 2013)
- Bread enriched with 8% ITFs, containing 33.3% amaranth flour 78.4 54.8 50 13.6 7.5 (Capriles and Are ^as, 2010)
- Bread enriched with 8% ITFs, containing 45% amaranth flour 81.7 57.2 50 10.3 5.9 (Capriles and Are ^as, 2010)
- Control bread (enriched with inulin, partially-baked frozen bread) 97.1 68 e e e (Novotni et al., 2012)
- Bread prepared with 15% of sourdough 74.3 52 e e e (Novotni et al., 2012)
- Bread prepared with 22.5% of sourdough 77.1 54 e e e (Novotni et al., 2012)
a
The conversion factor 70/100 was used to convert from bread to the glucose scale, and 100/70 was used to convert from glucose to the bread scale according to Atkinson
et al. (2008).
Source: Capriles et al. (2015), with permission from Nova Science Publishers, Inc.
V.D. Capriles et al. / Journal of Cereal Science 67 (2016) 83e91 89

Table 4
Summary of the research on the in vitro predicted glycemic response of gluten-free bread.

Gluten-free bread (GFB) HIa pGIa,b pGIa,b pGLb per 50 g References


(bread ¼ 100) (bread ¼ 100) (glucose ¼ 100) serving

- 11 commercial GFB 87e102 83e96 58e67 e (Segura and Rosell, 2011)


- Reference sample (white wheat bread) 100 95 66 20 (Capriles and Are ^as, 2013)
- Control GFB (prepared with rice flour and potato starch blend) 97 93 65 12 (Capriles and Are ^as, 2013)
- GFB enriched with 8% ITFS 81 84 59 10 (Capriles and Are ^as, 2013)
- Reference sample (white wheat bread) e 100 70 13 (Wolter et al., 2013)
- Basic GFB prepared with buckwheat flour 73 80 56 8 (Wolter et al., 2013)
- Basic GFB prepared with oat flour 58 71 50 9 (Wolter et al., 2013)
- Basic GFB prepared with quinoa flour 100 95 66 9 (Wolter et al., 2013)
- Basic GFB prepared with sorghum flour 59 72 50 10 (Wolter et al., 2013)
- Basic GFB prepared with teff flour 62 74 52 8 (Wolter et al., 2013)
- Commercial GFB 54 69 48 7 (Wolter et al., 2013)
- Wheat bread þ sourdough with Weissella cibaria (Wc) 82 85 59 11 (Wolter et al., 2014)
- Wheat bread þ sourdough with Lactobacillus plantarum (Lp) 65 76 53 10 (Wolter et al., 2014)
- Basic GFB prepared with buckwheat flour þ sourdough with Wc 90 89 62 11 (Wolter et al., 2014)
- Basic GFB prepared with buckwheat flour þ sourdough with Lp 84 86 60 10 (Wolter et al., 2014)
- Basic GFB prepared with quinoa flour þ sourdough with Wc 121 106 74 9 (Wolter et al., 2014)
- Basic GFB prepared with quinoa flour þ sourdough with Lp 116 103 72 9 (Wolter et al., 2014)
- Basic GFB prepared with sorghum flour þ sourdough with Wc 76 81 57 12 (Wolter et al., 2014)
- Basic GFB prepared with sorghum flour þ sourdough with Lp 54 69 48 10 (Wolter et al., 2014)
- Basic GFB prepared with teff flour þ sourdough with Wc 81 84 59 9 (Wolter et al., 2014)
- Basic GFB prepared with teff flour þ sourdough with Lp 51 68 48 8 (Wolter et al., 2014)
- GFB prepared with rice flour þ 70% water (fwb) 92 87 61 e (de la Hera et al., 2014)
- GFB prepared with rice flour þ 90% water (fwb) 97 92 64 e (de la Hera et al., 2014)
- GFB prepared with rice flour þ 100% water (fwb) 98 93 65 e (de la Hera et al., 2014)
- GFB prepared with raw brown rice 60 60 42 e (Cornejo et al., 2015)
- GFB prepared with pre-germinated brown rice 57 57 40 e (Cornejo et al., 2015)
- GFB prepared with 12 h germinated brown rice 47 49 34 e (Cornejo et al., 2015)
- GFB prepared with 24 h germinated brown rice 46 48 34 e (Cornejo et al., 2015)
- GFB prepared with 48 h germinated brown rice 34 38 27 e (Cornejo et al., 2015)
a
HI ¼ hydrolysis index; pGI ¼ predicted glycemic index; pGL ¼ predicted glycemic load. Values were compiled from the references.
b
The conversion factor 70/100 was used to convert from bread to the glucose scale, and 100/70 was used to convert from glucose to the bread scale (Atkinson et al., 2008).
Source: Adapted from Capriles et al. (2015), with permission from Nova Science Publishers, Inc.

61 to 65 (medium GI), and although the particle size did not affect emulsifiers, NaFeEDTA, ferrous bis-glycinate, ferrous gluconate or
that index, the added water content did. The lowest dough hydra- ferrous sulfate presented higher ferrous dialyzable iron than breads
tion not only limited starch gelatinization and hindered in vitro fortified with electrolytic iron, ferrous lactate or ferric pyrophos-
starch digestibility but also resulted in GFB with poor physical phate. The best result, considering the highest sensory acceptability
properties. score and predicted in vitro bioavailability, was achieved with the
Cornejo et al. (2015) investigated the effects of the different fortification with ferric pyrophosphate.
germination times of brown rice flour on the nutritional quality of Another promising approach was that of Krupa-Kozak et al.
brown rice flour-based GFB. In viewing the results of the in vitro (2012), who developed a sensory-accepted GFB enriched with
starch digestibility assay, soaking (pre-germination) and germina- inulin (3.9 g/100 g) and fortified with calcium (108.5 mg/100 g)
tion can be observed to reduce the HI and pGI of GFB. This effect because ITFs could improve calcium absorption.
was more accentuated after 48 h of germination, leading to GFB
with low pGI (27). These authors explained that the reduction in 5. Conclusions and future prospects
the predicted GR might be associated with internal structural
changes in the starch granules during germination, indicating that The promising results of the reviewed studies indicate the great
germination could lead to less accessible or more RS granules. potential of GFB that is prepared with nutrient-dense alternative
Tables 3 and 4 present the promising results from different raw materials, nutritional and functional ingredients, and their
approaches to produce a GFB with a low GR due to an increase in DF combinations. Some of those products were acceptable and pre-
and protein contents, which can alter the rate of starch digestion, sented similar or better sensory attributes than control formula-
reducing the pGI and diluting the amount of available carbohy- tions, and some were even comparable to their wheat-based
drate; both factors contributed to reduce the pGL. counterparts.
Efforts should be made to apply some of these promising ap-
4.2. Approaches to improve mineral bioavailability proaches to commercial products to make GFB with good techno-
logical, sensory and nutritional properties available to consumers
The only study found in this field was that conducted by Kiskini with gluten-related disorders. These products are extremely
et al. (2007), who used different iron compounds to fortify important for assisting with individual adherence to a strict GF diet
amaranth-based GFB. These authors use a ferrous iron dialyzability treatment, increasing social inclusion, and improving the quality of
method to provide information regarding the chemical behavior of life.
the iron fortificant compounds in GFB digested in vitro. This method Furthermore, new studies should be performed to test and
was found to be a good predictor of iron bioavailability, based on optimize the nutrient-dense alternative raw materials and nutri-
correlation with iron uptake by cells and with iron absorption by tional and functional ingredient levels of GFB formulations by
humans. These authors tested a series of iron compounds and considering their nutritional, sensory and technological properties
observed that GFB fortified with ferric pyrophosphate with as well as shelf-life. Food scientists and technologists should assess
90 V.D. Capriles et al. / Journal of Cereal Science 67 (2016) 83e91

the proximal composition and the nutrient and bioactive com- Paulo Research Foundation (FAPESP). Special thanks to Camilly F.
pounds in enriched/fortified GFB formulations to evaluate whether Pereira and Denise G. Muniz for help in baking and other laboratory
the target values were achieved and to define adequate dosage tasks. Authors also thank Nova Science Publishers, Inc for permis-
levels. Studies regarding digestibility, bioaccessibility and sion to reuse parts of the book chapter Capriles et al. (2015).
bioavailability could be performed on those specially designed Innovative approaches to improve nutritional and bioactive com-
formulas, recognizing the limitations of in vitro studies discussed in pounds of grain-based gluten-free products. In: Langdon, R. (Ed.),
this review (Capriles et al., 2015). Another topic for further inves- Gluten-free diets: Food sources, role in celiac disease and health
tigation is short- and long-term controlled clinical trials to inves- benefits. Nova Science Publishers, Inc, Hauppauge, NY, pp. 67e116;
tigate or improve the efficacy of these improved GFBs as vehicles of and John Wiley and Sons for permission to adapt Table 2.
micronutrients and bioactive compounds as well as their potential
health benefits (e.g., formulations enriched with functional in-
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