Bread enriched with flour from cinereous cockroach (Nauphoeta cinerea)

ABSTRACT

Animals and insects are the main sources of protein. The objective of the present study was to
produce a flour from cinereous cockroach (Nauphoeta cinerea) for protein enrichment of wheat
bread. To prepare the flour, the dehydrated insects were crushed and sieved to reduce the
granulometry to a particle size of 1.18 mm. The flour was analyzed microbiologically and then added
in amounts of 5, 10, and 15% (based on wheat flour) in a bread formulation that was analyzed for
chemical composition and color, firmness, and specific volume and compared to white wheat bread
and whole wheat bread. Sensorial evaluation was carried out on bread enriched with 10% roasted
flour as the one that presented the best nutritional characteristics, differing little from the white and
whole wheat bread. It is concluded that the use of cinereous cockroach (Nauphoeta cinerea) flour is
an efficient way to enrich wheat bread without alterations in sensorial quality.

1. Introduction

A report released by the United Nations (UN) discloses that the world population is expected o
reach> 9.2 billion by 2050. This represents a great challenge to the availability of resources to meet
the needs of this enormous population. Increased productivity, new and more efficient and
sustainable technical proposals to combat crop pests, and more appropriate product handling to
minimize losses to marketing, among other factors, will be needed so that the world food
production meets the growing demand for decades to come (Zuben,

2012). Wild animals and insects are often the main sources of protein in forest areas, while leaves,
seeds, mushrooms, honey, and fruits provide minerals and vitamins that ensure a nutritious diet.
The forecast of the UN Food and Agriculture Organization (FAO) says that the land area intended for
breeding will have to grow by 70% to feed the planet's population by 2050, which is expected to
reach 9 billion people, and even with the small amount of insects that can be consumed by humans
(only 1600 edible types in 1.5 million species cataloged), the frenetic pace at which insects
reproduce makes their “meat” an abundant source of food. They are rich in protein, vitamins
(especially vitamin B), and minerals, such as iron and calcium. In addition, they are rich in lipids and
essential fatty acids .

University of California in the United States, besides being more nutritious than other types of meat,
it is cheaper to raise insects than cattle. Since insects are cold-blooded, have more complex
metabolisms than warm-blooded animals, and can adapt to different temperature levels, they need
less food and a simpler and cheaper feed. In addition, insects take up less space and reproduce
faster than other animals commonly seen in pastures. And at the end of the process, they are

better leveraged by the fact that many parts of cattle, for example, are not used for human
consumption, such as the hooves, teeth, bones, and skin, which are commonly used in the
manufacture of animal feed. The FAO lists the benefits of large-scale insect production: 2 kg of feed
is required to produce 1 kg of insects, whereas cattle require 8 kg of feed to produce 1 kg of meat.
The insect feed is simple because it can be made from agricultural residues. Insects are extremely
ecological; they use much less water and produce less greenhouse gases than cattle (Durst, Johnson,
Leslie, & Shono, 2006). Several groups of insects can be found in abundance in different
environments; one can therefore infer that a large amount of biomass is not utilized as a food source
for humans. And since in the future the greatest challenge for humanity will be growing food in
increasingly greater quantity, insects are likely to be an important food source (MacEvilly, 2000;
Zuben, 2012). Worldwide, the base of the food pyramid is made up of carbohydrates.

Because of this, bread has high consumption because it is high in this energy source, and it is not an
expensive food. It can be consumed by all social classes, from a food supplement, as seen in
families with greater purchasing power, or even as one of the few sources of food, as seen
in low-income families. Bread can be purchased in high-end establishments or produced at
home in a more artisanal way. Therefore, aiming at the protein enrichment of bread, this
study set out to modify a product very popular in Brazil using a type of insect, the cinereous

cockroach (Nauphoeta cinerea).

2. Materials and methods

2.1. Raw materials

Wheat flour was purchased in the local market of Rio Grande, RS, and flour based on the
cinereous cockroach (Nauphoeta cinerea) was provided by Nutrinsecta, a company that
develops ingredients for animal feed that is certified by the Ministry of Agriculture,
Livestock and Supply. Insects were reared obeying strict environmental and health
standards. They were fed with fruit and vegetable remains, slaughtered in boiling water, and
dried in an oven and packaged. The ingredients used for the production of bread, such as
hydrogenated vegetable oil (Primor), sodium chloride (Synth), and sucrose (União), were
purchased from the local shops. Additives such as ascorbic acid PA (Synth), manufacturing
aids, and fresh yeast (Fleischmann) were also used.

2.2. Methods

2.2.1. Obtaining the insect flour

To obtain the flour, cinereous cockroaches, received dehydrated, were ground in a ball mill
for 3 h. Subsequently, the flour obtained was sieved through a 14 mesh and then packaged
in glass jars and kept refrigerated at 4 °C until testing.

2.2.2. Assessment of cinereous cockroach flour

2.2.2.1. Chemical composition of the insect flour. The following chemical analysis was
conducted on the cockroach flour:

a) Humidity: determined according to AACC (2000), Method No. 44-15ª;

b) Ash: determined according to AACC (2000), Method No. 08-01;

c) Protein: determined according to the Kjeldahl method, AACC(2000), Method No. 46-13;
d) Total lipids: the fat content was determined by the Soxhlet method,AACC (2000), Method
No. 30-20;

e) Fibers: determined by the Adolfo Lutz Institute (Zenebon & Pascuet,2008);

f) Amino acid profile: determined by high-performance liquid chromatography(HPLC) in CBO

laboratory, Campinas São Paulo/Brazil;

g) Fatty acids: determined by gas chromatography in CBO laboratory,Campinas São

Paulo/Brazil.

2.2.2.2. Microbiological evaluation of cockroach flour.

In themicrobiological evaluation, analyses were carried out to determine thermo-tolerant

coliforms at 45 °C and mold and yeast counts. These analyses were performed following the
procedures described by the American Public Health Association (APHA, 2001). To verify the
sanitary conditions, the sample was subjected to Salmonella analysis according to NBR
12124 - MB 3465/1991 (Salmonella – Determination in Food) and positive Staphylococcus
coagulase following the procedures described by the APHA (2001).

2.2.3. Formulation of standard and insect flour-added breads

The straight dough method was used for the preparation of the bread. Three formulations
(Table 1) with different quantities (5%, 10%, and 15% of cockroach flour in wheat flour
basis) were evaluated and compared to the standard bread to verify the influence on the
specific volume (SV), hardness, color, protein content, and sensory quality.

2.2.3.1. Elaboration of standard and cockroach flour-enriched bread.

First, the dry ingredients were blended into a planetary mixer (Kitchen-Aid) followed by the
addition of vegetable fat, water, and dissolved yeast. The mixture was done at full speed for
10 min until the gluten was developed. The dough was weighed, divided into 80-g pieces,
rounded in a spherical shape by hand, modeled with a roll of pasta and placed with roll and
put into greased individual metal pans (3 × 5× 11.5 cm). The fermentation step was carried
out in an oven (Q317M-Quimis) at 30 °C for 95 min, with controlled temperature and
relative humidity. Baking occurred at 200 °C for 20 min in an electric oven (Diplomata-
Fischer). The resulting breads were cooled to ambient temperature and examined after 1 h
of rest.
2.2.4. Evaluation of bread quality
The evaluation of bread quality was performed by determining the external and internal
characteristics, aroma, and taste according to El Dash, Diaz, and Camargo (1982)
spreadsheet. The parameters analyzed as external characteristics were crust color, breaking,
symmetry, and SV (mL/g), which was obtained by the ratio between the apparent volume
(mL) carried by millet seed displacement according to Pizzinatto, Magno, Campagnollli, Vitti,
and Leitao (1993) and the mass (g). Crust characteristics, crumb color, crumb cell structure,
and crumb texture were analyzed as internal characteristics. Subsequently, the aroma and
taste were analyzed.
2.2.4.1. Crumb hardness.
The hardness of the bread crumb was measured on fresh bread after 1 h of baking and held
in a texturometer TA-XT2 (Stable Micro Systems, UK). The test was performed according to
AACC method 2000 (74-09.01), which consists of compressing two slices of 25 mm thickness
in the texturometer platform center with a cylindrical probe of 36 mm diameter under the
following working conditions: pre-test speed of 1.0 mm/s, test speed of 1.7 mm/s, post-test
speed of 10.0 mm/s, 40% compression, and trigger force of 5 g.
2.2.4.2. Crumb color. The analysis of the bread crumb and crust was
done in a Minolta® CR400 colorimeter (Minolta, 1993). The experiment followed the color
system in the L* a* b* (or CIE L*a*b*) space defined by the CIE (International Commission
on Illumination) in 1976, evaluating the L* values (brightness) and a* and b * (chromaticity
coordinates). The value of chroma or C* and hue angle or hab was also calculated, referred
to as the CIELCh color system according to Minolta (1993) (Eqs. (1) and (2)).

3.1. Chemical composition of cockroach flour

The results of the analysis of the proximal composition of cockroach flour are shown in
Table 2. One can observe a slight variation in the proximal composition values performed in
the laboratory when compared to the figures provided for Nutrinsecta. This variation may
be due to the fact that the dehydrated insects were ground and sieved to obtain the flour
that was used in the enrichment of breads. We can highlight a reduction of fibers
and an increase in the concentration of protein, demonstrating that the insect exoskeleton,
which has a considerable amount of fibers and minerals, was retained in the fraction that
was discharged. The protein content of the cockroach flour (63.22) was similar to that
presented by Ramos-Elorduy (1998) for Periplaneta americana L (65.60) and Periplaneta
australasiae (62.40), showing a high content of the component that is desired to elevate in
tested breads.
3.2. Microbiological evaluation of cockroach flour (Nauphoeta cinerea)
The results obtained in the microbiological analyses of cockroach flour are shown in Table 3.
The insect flour presented satisfactory sanitary conditions, since the analytical results are
within the range of established values as specified in the regulation, thus enabling the
follow-up study.

3.3. Evaluation of standard bread and flour-enriched breads with cinereous cockroach
(Nauphoeta cinerea)
Table 4 shows the results of the SV and hardness an hour after removal from the oven. It is
possible to observe from the data that there were significant differences in the volumes of
all the trials, and with the increase of the insect flour concentration, the SV reduced.
Additionally, the values of hardness found for standard bread and for 5% enriched bread did
not present a significant difference, nor did the 10% bread differ significantly from the
whole wheat bread. The higher the concentration of insect meal added, the greater the
change in the formation of the gluten network, due to the type and nature of the proteins
present. This made the mass less viscoelastic, making it difficult to expand the gas cells, or
SV whole wheat flour has a higher amount of fiber than wheat flour, and this also prevents
the formation of gluten, a reason that justifies the similarity statistic with bread enriched
with 10% of the flour of cinerea cheap.
As reported by Moore, Heinbockel, Dockery, Ulmer, and Arendt (2006) and Mezaize,
Chevallier, Le Bail, and De Lamballerie (2009), there is a strong negative correlation between
SV and the hardness of the breads justified by the greater compression of the gas cells in the
breads of lower volume, resulting in increased crumb hardness by increasing the resistance
to deformation of the product in the mouth. Figueira, Crizel, Silva, and Salas-Mellado (2011)
added concentrations of 2, 3, 4, and 5% of Spirulina platensis in breads prepared with rice
flour and found that up to a concentration of 4%, there were no significant differences in
the SV and hardness of the breads; however, from this concentration, the bread started to
show significant differences. The insect flour used for enrichment at a concentration of 5%
showed no significant difference in hardness compared to standard wheat bread, but the
crumb hardness increased for additions beyond this concentration. Fig. 1 shows the breads
made with cockroach flour at different concentrations.
3.4. Color of the crumb and crust of standard and insect-added flour breads
Table 5 shows the color parameters evaluated in the crumb and crust of standard bread and
breads from insect-added flour. We observed that the resulting breads presented crust and
crumb color parameters similar to whole wheat bread. Fig. 1 presents the color parameters
of the crumb and crust of the standard bread and breads from cinereous cockroach
(Nauphoeta cinerea) flour. The lightness in the crust ranged from 64.62 to 59.40, showing
that the samples of 10 and 15% had no significant difference between them. Regarding the
crust, the samples of 5, 10, and 15% did not have significant differences among them, and
the whole wheat bread did not present a significant difference from the bread crust with 5
and 10% enriched bread. The addition of cinereous cockroach (Nauphoeta cinerea) flour
meal at all concentrations showed that the higher the concentration, the lower the hue
(hab) angle in the crumb and crust, resulting in a distancing of the desired value (close to
90°), which should tend to yellow to obtain a product similar to wheat bread.
3.5. Bread quality evaluation by spreadsheet (El Dash et al., 1982)
The total scores obtained for standard bread and breads made from cockroach flour are
presented in Table 6. According to Dutcosky (1996), bread with a score of 81–100 points
can be classified as a good-quality bread, 61–80 as regular bread, and 31–60 as a bad-quality
bread. The values of the total score of the bread varied from 72.4 to 85.17. According to this
classification, both standard bread and the 5% modified bread showed good quality, and
breads enriched with 10% and 15% cockroach flour showed regular quality, but 10%
enriched bread reached a value of 81, becoming a better classification than 15% enriched
bread.
The following characteristics evaluated in the worksheet decreased in value with the
increase in insect flour addition: crumb color, due to the fact that the bread gets darker,
similarly to the whole grain; crumb texture, where increased cockroach flour presented
higher crumb compression values resulting from the alteration of the protein network in the
formation of gluten, which was also observed in bread made with whole wheat flour; and
aroma and taste, as a slight odor and taste change could be observed with an increasing
concentration of cockroach flour compared to wheat flour.
3.6. Physicochemical analysis of the breads
3.6.1. Protein content in bread with cockroach flour
With respect to the percentage of proteins, bread with 5% cinereous cockroach flour
obtained 7.88% protein, 10% obtained 12.53% protein, and 15% obtained 14.67% protein.
Bread with 10% cinereous cockroach flour obtained an increase of 49.16% of protein
compared to standard bread. Besides high protein, the 10% enriched bread showed a
good total quality score and low crumb hardness values.
3.6.2. Chemical composition of the standard bread and bread with 10% cockroach flour
Table 7 presents the results of chemical analyses performed in standard breads and breads
enriched with 10% cockroach flour. According to Table 7, the bread enriched with cockroach
flour obtained a much higher protein content than standard bread and also presented a
lower percentage of carbohydrates. Regarding the percentage of lipids, there were no
significant differences in all samples; the bread enriched with cockroach flour presents an
advantage in the type of fat present, with a large percentage being unsaturated fatty acids
rich in ω6 and ω9.
3.7. Amino acid profile of cockroach flour
Fig. 2 shows the data obtained in amino acid profile analysis of cockroach flour. According to
Blanco and Bressani (1991), the protein quality refers to its ability to meet the nutritional
requirements of humans for essential amino acids and non-essential nitrogen for protein
synthesis purposes. Considering the average contents of the different orders of insect, the
main components of insects are protein and fat, followed by fiber, nitrogen-free extract,
and ash.
Based on the amino acid composition in the cockroach flour, it can be seen that those
classified as essentials are present in large quantities, and among them, leucine with 3.51%,
lysine with 3.37%, and valine with 2.61% are worth mentioning, since these are of great
importance due to their daily intake necessity for humans. Comparing the amino acid
requirements for adults published by the World Health Organization (WHO, 2007) with the
amino acid profile of the cockroach flour produced in this study, it can be observed that the
flour meets the amino acid requirements of adults, showing that bread enriched with the
insect flour would have improved nutritive value compared to standard bread. When
comparing these values to those of meat and pig bone flours (Pozza et al., 2004), values for
the same amino acids (leucine, valine, and lysine) are in higher quantity in cockroach flour.
Meat flour presented 1.48% for leucine, 1.10% for valine, and 1.41% for lysine, whereas
bone flour presented values of 2.00% for leucine, 1.44% for valine, and 1.99% for lysine.
Compared to shrimp head silage flour (Guilherme, Cavalheiro, & Souza, 2007), insect flour
obtained a higher value only for leucine, whereas the study indicates a lysine value of
3.67%, a valine value of 3.41%, and a leucine value of 2.73%. 3.8. Fatty acid profile of
cockroach (Nauphoeta cinéria) flour Fig. 3 shows the fatty acid profile of cinereous
cockroach flour. Regarding the composition of unsaturated fatty acids of the cockroach
flour, of the 18.45% total fat present in flour, 10.94% is unsaturated fat. Oleic acid (ω9) with
9.52% and the essential fatty acid linoleic acid (ω6) with 1.42% are included in this
percentage. The omega-9 (ω9) fatty acid showed a good concentration in cockroach flour of
approximately 49.7% total fatty acids compared with beef, which, according to Domene
(2002), has about 40% total fatty acids.
This high concentration is a positive factor, since the ω9 has a hypocholesterolemic effect.
These results are similar to those presented by Thompson (1973), showing that the principal
fatty acids of the cockroaches are oleic acid and monounsaturated fatty acids, groups that
present a healthy performance in humans.
According to Hautrive, Marques, and Kubota (2012), the saturated fatty acid content
present in ostrich meat is 27.34%, similar to that of pork (ham), which is 28.02%, beef
(rump) percentage of and chicken (thigh and drumstick) is the one with the least percentage
at 19.73%.When comparing these data with those found in cockroach flour, we can see the
low percentage of saturated fat, which reaches less than half the value obtained for the
chicken, and thus the insect flour showed the lowest percentage compared to other meats.
Saturated fat can contribute in the medium and long term to the onset of obesity and
cardiovascular disease, which therefore makes the low percentage in the cockroach flour a
positive point. According to Grundy and Denke (1990), saturated fatty acids are considered
hypercholesterolemic, and more worrying in this regard are myristic (C14:0), lauric (C12:00),
and palmitic (C16:0) acids. Stearic acid (C18: 0) has a neutral function, because the body
immediately turns it into oleic acid (C18:1). The saturated fatty acids increase the level of
cholesterol in the blood by reducing LDL-cholesterol receptor activity and the clearance
of LDL in the bloodstream.
3.9. Sensory evaluation of bread with cockroach flour
Table 8 shows the results obtained in the sensorial analysis of breads made from cockroach
flour. Regarding the acceptance index (AI), a value> 75% was obtained in all parameters
analyzed. According to Spehar and Santos (2002), for a product to be considered as
accepted in terms of its sensory properties, it is necessary to obtain an AI of at least 70%.
The flavor parameter was the lowest. It is believed this occurred because the judges knew
about the addition of the cockroach flour in the bread, and the evaluation may have been
influenced because entomophagy is not a local custom, in addition to the disgust of some
people for insects. On the other hand, the taste of the product obtained a 76% acceptance
rate, showing good sensory acceptance. Fig. 4 shows the results for purchase intention of
the loaves developed with cinereous cockroach flour.
Regarding the purchase intention (Fig. 4), the sample of bread with cinereous cockroach
flour added received a positive attitude of purchase, with 22% of the judges stating that
they would certainly buy and 41% possibly buy, totaling a 63% positive response. Since
bread enriched with cockroach flour is an unknown product by consumers,
being new with respect to the culture of the judges, an acceptance of possible purchase of
63% is considered a good result.
4. Conclusion
Through this study, the feasibility of producing an insect-based flour for bread enrichment
was verified. The flour produced presented satisfactory sanitary conditions and can
therefore be used in human food with a proper chemical composition, showing a good
nutritional profile due to the amino acid and fatty acid contents. The addition of cockroach
flour to bread formulations did not alter the technical characteristics in a negative way, and
the choice of the bread enriched at 10% was due to the increase of 49.16% in protein
compared to standard bread. In the sensorial analysis, the judges moderately liked the 10%
enriched bread. Regarding the acceptance index, a value> 75% was obtained in all
parameters analyzed, and for the purchase intent, the bread with cinereous cockroach flour
added obtained a positive attitude of purchase, with 22% of the judges stating that they
would certainly buy and 41% stating that they would possibly buy.