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Öztürk / Eur Food Sci Eng 2023, 4 (1), 15-25
15
A waste material rich in bioactive compounds: Hazelnut waste
Göktürk Öztürk
Food Technology Programme, Kaman Vocational High School, Kırşehir Ahi Evran University, 40300, Kırşehir, Turkey
ARTICLE INFO
ABSTRACT
Review Article
Nowadays, increasing sensitivity to the environment has led to the development of
sustainable agricultural policies. In this respect, it has become important to transform
agricultural waste products into value-added products. Hazelnut, which has a
significant trade volume worldwide, is processed into products, and some waste
materials can be emerge. These waste products could transform into high added-value
to food, cosmetics, and pharmaceutical industries due to possessing the bioactive
compounds such as phenolics, bioactive peptide and, dietary fibre in them. This review
represents the research on the bioactive compounds from the hazelnut waste, especially
conducted in recently, and concentrates on its tree leaf, husk, and oil meal.
Article History:
Received: 29 April 2023
Accepted: 6 June 2023
Available Online: 8 June 2023
Keywords:
Hazelnut
Waste
Leaf
Husk
Oil meal
1. Introduction
Today, the energy crisis in the world and the increasing
concerns on the environment have accelerated the research on
the search for the alternative energy sources to fossil fuels
(Havrysh et al., 2021; Tsekos et al., 2021). One of them is
waste. According to Directive 2008/98/CE, ‘waste means any
substance or object which the holder discards or intends or is
required to discard’ (Anonymous, 2008). Based on this
definition, waste can be classified as follows; state (solid,
liquid, gaseous), source (agricultural, commercial, industrial,
municipal), and degradability (biodegradable, non-
biodegradable) (Dey et al., 2021; Koul et al., 2022). A
considerable amount of waste is generated in the world, for
example, only the European Union generated about 2.2
billion tons of waste in 2020 (Anonymous, 2020). On the other
hand, in terms of solid waste, 2.02 billion tons of it was
produced in the world in 2016, and it is estimated that this
number will increase to 2.59 billion tons and, 3.4 billion tons in
2030 and 2050, respectively (Kaza, 2018). If the waste cannot
be controlled, that is, if zero waste management is not
implemented, the world may inevitably face serious problems.
It might affect on both environmental safety by causing air
pollution, water pollution, soil contamination and increasing
greenhouse gases, and human health (Anonymous, 2016). Due
to these adverse effects, the principles of zero waste
management have been focused all over the world in recent
years, comprising prevention, reduction, recycle, recovery, and
disposal (Anonymous, 2008). Therefore, for the
implementation of zero waste management, recently, there has
been conducted a lot of research on the reusing of the waste
from applied as the fertilizer and animal feed (Chew et al.,
2018) to manufacturing bio-based films for food packaging
(Bastante et al., 2021) and producing biogas (Havrysh et al.,
2021), and biodegradable polymers (Maraveas, 2020).
Probably, it can seem like that recovering biochemicals,
producing energy or value-added products from waste rather
than their disposal will be an important philosophy of this
century.
Agriculture provides an important source of raw materials
for the food industry and human need, and eventually a large
amount of agricultural waste is occurred as a result of
agricultural and agro-industrial activity (Sharma et al., 2022).
Agriculture waste is made up field residues (i.e stems, seeds,
husk, shell and so on), industrial processing waste (i.e pomace,
sugarcane bagasse, hazelnut cake etc.), livestock waste
(bedding/litter, wastewater in the slaughterhouse, animal
carcasses etc.), and chemical waste (pesticides, insecticides,
and herbicides etc.) (Dey et al., 2021). They can comprise a
number of bioactive chemicals such as polyphenols, and dietary
fiber, especially in field residues and industrial processing
waste (Balasundram et al., 2006; Beutinger et al., 2020;
Castrica et al., 2019; Dey et al., 2021). The former has
antioxidant, antimicrobial, anticancer, and antiproliferative
activity (Beutinger et al., 2020; Castrica et al., 2019; Dey et al.,
2021). The latter, which is an essential part of the plant cell
wall, may be divided into two subgroups; soluble and insoluble
in water (Gill et al., 2021). They have a favorable impact on
human health, regulating the bile salts, improving the fecal
volume by holding the water, influencing the microbial
spectrum to beneficial ones, taking part in the production of
short-chain fatty acids (propionate, butyrate, and acetate) in the
gastrointestinal tract, which have an important role in both
energy metabolism, host immunity and inflammation, and in
inhibiting colon cancer cell proliferation (Capuano, 2017;
European Food Science and Engineering
Eur Food Sci Eng 2023, 4 (1), 15-25
doi: 10.55147/efse.1289656
https://dergipark.org.tr/tr/pub/efse
*Corresponding author
E-mail address: gozturk@ahievran.edu.tr
Öztürk / Eur Food Sci Eng 2023, 4 (1), 15-25
16
Holscher, 2017; Morrison & Preston, 2016; Yao et al., 2022).
Because of these positive effects on human health, today, it is
recommended to consume 14 grams of dietary fiber per 1000
kcal daily (Anderson et al., 2009). Dietary fiber has been
isolated and characterized from various agricultural wastes, for
instance, cellulose from waste of wheat straw (Bian et al.,
2019), rice husk (Ragab et al., 2018), onion and garlic (Reddy
& Rhim, 2018); hemicellulose from rice straw and its husk
(Ragab et al., 2018), pineapple peel (Banerjee et al., 2019);
lignin from hazelnut and walnut shell (Gordobil et al., 2020);
and glucans and pectin from walnut green husk (La Torre et al.,
2021).
Hazelnut is one of the nuts, derived from the tree, a genus
(Corylus) belonging to the Betuliaceae family. It was produced
approximately 963 million tons in between 2016-2020
(Anonymous, 2023). Turkey is an important producer, which
met about 63% of the world hazelnut production in between
2016-2020, followed by Italy, Azerbaijan, and others
(Anonymous, 2023). It is a product with a significant
commercial value in the world, mainly for Turkey. The world
export value of hazelnut was about 2.2 billion dollars, which of
Turkey was 1.3 billion dollars in 2021 (Anonymous, 2023). In
addition to its economic value, it can be added to baklava,
cakes, ice cream, chocolate, confectionery, cacoa-hazelnut
cream (Baycar et al., 2021; Dervisoglu, 2006; Ermis & Ozkan,
2021; Gonzalez-Estanol et al., 2022; Guiné & Correia, 2020),
its milk (Gul et al., 2017) and fermented their products (Atalar,
2019; Ermiş et al., 2018) to the alternative commodity to milk,
and thus both contributing taste-aroma to the products to which
it is added and enriching them in terms of nutrients such as
protein (Muller et al., 2020), lipids (Granata et al., 2017),
vitamins (Stuetz et al., 2017), minerals (Muller et al., 2020),
dietary fibers (Tuncil, 2020) and bioactive compounds
(Gültekin-Özgüven et al., 2015; Taş & Gökmen, 2015).
After the hazelnut with green husk is harvested, it is dried
in the sun to certain moisture content, and then hazelnut in shell
is separated from the green husk by a hazelnut threshing
machine. Besides, during this process, rotten and damaged
hazelnuts are relatively removed from the healthy hazelnuts
with the help of ventilation. Then, the hazelnuts are sent to the
factory to be processed into products such as natural hazelnut
kernel, roasted hazelnut kernel, chopped hazelnut kernel,
hazelnut puree, and hazelnut oil. In the view of the process from
harvesting to consumption, there are five hazelnut by-products
including hazelnut tree leaf, green leafy husk, shell, skin, and
oil meal (Figure 1). This review focused on hazelnut tree leaf,
husk and oil meal, but not its shell and skin and it has been
recommended for further reading on them as follows; Fuso et
al. (2021), Alalwan et al. (2022).
2. Hazelnut Tree Leaf
After harvesting, the hazelnut leaves fall off and may
become a natural source of fertilizer for the soil owing to its
mineral and organic matter content (Öztürk & Tarakçıoğlu,
2016; Wang et al., 2018). Additionally, it possesses the
bioactive compounds such as phenolics (Shahidi et al., 2007),
diarylheptanoids (Masullo et al., 2015a; Masullo et al., 2015b),
taxanes (Ottaggio et al., 2008), essential oils (Najda & Gantner,
2012) and α-tocopherol (Sivakumar & Bacchetta, 2005).
Figure 1. Hazelnut waste
Öztürk / Eur Food Sci Eng 2023, 4 (1), 15-25
17
The leaves of the plant may be often used in traditional
medicine to treat the swelling, rash, phlebitis, varicose veins,
and hemorrhoidal symptoms (Riethmuller et al., 2016). This
effect may be probably due to its bioactive compounds. In a
study by Amaral et al. (2005) in which the effect of hazelnut
tree leaves (Corylus avellana L.) from different subspecies on
its phenolic composition was investigated, eight phenolic
compounds were detected in hazelnut tree leaves, as follows; 3-
caffeoylquinic acid, 5-caffeoylquinic acid, caffeoyltartaric
acid, ρ-coumaroyltartaric acid, myricetin 3-hexoside, myricetin
3-rhamnoside, quercetin 3-hexoside, quercetin 3-rhamnoside,
kaempferol 3-rhamnoside and among these phenolics,
myricetin 3-rhamnoside (10.60-18.24 g/kg, dry basis) and
quercetin 3-rhamnoside (1.57-4.68 g/kg, dry basis) were found
to be dominant phenolics (Amaral et al., 2005). The same
phenolics, plus 3-caffeoylquinic, and caffeoyltartaric acids
were reported in Corylus avellana (Fertille Coutard, Daviana,
and M. Bollwiller cultivars) by Oliveira et al. (2007). The
researchers also examined the antioxidant and antimicrobial
activities of hazelnut tree leaves. It was found that they
inhibited more than 93.1% of DPPH at 0.5 mg/ml concentration
compared to BHA (96% at 3.6 mg/ml) and α-tocopherol (95%
at 8.6 mg/ml). It has an antimicrobial effect against Bacillus
cereus, Bacillus subtilis, Staphylococcus aureus, Escherichia
coli, Pseudomonas aeruginosa, and Klebsiella pneumoniae, but
not toward Candida albicans and, Cryptococcus neoformans
(only cultivar M. Bollwiller was effective at 100 ml/mg)
(Oliveira et al., 2007). Riethmuller et al. (2013) evaluated the
effect of methanol and ethyl acetate solvents on their bioactive
compounds the leaves of C. avellana L. Among their bioactive
compounds, six flavonoid glycosides (myricetin-3-O-hexoside,
myricetin-3-O-rhamnoside, quercetin-3-O- hexoside,
quercetin-3-O-rhamnoside, kaempferol-3-O-rhamnoside,
kaempferol-di(desoxyhexoside), rosmarinic acid, and a
caffeoyl-hexoside derivative were characterized in the
methanolic extract while five flavonoids (only not myricetin-3-
O-hexoside), and rosmarinic acid were identified in the ethyl
acetate extract. Myricetin-3-O-rhamnoside was the
predominant flavonoid in both solvents (37.7 µg/mg for
methanol, 72.64 µg/mg for ethyl acetate). The research also
pointed out that the most suitable solvent is ethyl acetate in
terms of the amount of flavonoid compounds (Riethmuller et
al., 2013).
In a study by Shahidi et al. (2007), in which the extraction
process was carried out in a water bath at 80 °C with 80%
ethanol, the amounts of gallic acid, caffeic acid, coumaric acid,
ferulic acid and sinapic acid in hazelnut leaves (Corylus
avellana L.) were found to be 157 mg CE (catechin
equivalent)/g, 362 mg CE/g, 884 mg CE/g, 237 mg CE/g, and
247 mg CE/g, respectively. It has been found that it might
inhibit the oxidation of LDL cholesterol by 61% at 50 ppm
while do catechin 53% and can prevent DNA damage by
scavenging the hydroxyl radical up to 50 ppm (Shahidi et al.,
2007).
Corylus colorna L., known as Turkish hazel, is rich in
flavonoids (Benov & Georgiev, 1994). Riethmuller et al. (2014)
investigated the antioxidant activity in different parts, including
leaves, bark, catkins, and involucre. They found that the total
phenolic, tannin, and flavonoid content in the leaves were 0.94
g/100 g, 0.38 g/100 g, 0.49 g/100 g, respectively. In their study,
the derivatives of quinic acid, myricetin, quercetin, and
kaempferol were identified and characterized in the extracts
from the leaves with methanol and ethyl acetate solvent. The
research showed that there was a correlation between the
phenolic content of the extracts observed in the research and
their antiradical activity (Riethmuller et al., 2014).
Another species of Corylus is Corylus maxima, a type of
hazelnut tree common in the Balkans, Southeast Europe, and
Southwest Asia. Riethmuller et al. (2015) conducted research
to characterize the bioactive compounds in Corylus maxima
(leaves and bark). The authors found that the total phenolic,
tannin, and flavonoid content in the leaves were 2.43 g/100 g,
0.10 g/100 g, 0.96 g/100 g, respectively. Catechin/epicatechin,
myricetin-3-O-rhamnoside, myricetin-3-O-hexoside,
kaempferol-glucuronide, quercetin-3-O-rhamnoside,
kaempferol, kaempferol-3-O-rhamnoside, and kaempferol-
(di)desoxyhexoside were determined in the extract of the leaves
and bark with methanol and ethyl acetate and found that the
major phenolic compounds are quercetin-3-O-rhamnoside and
myricetin-3-O-rhamnoside in both solvents. In the study, the
amount of 3-O-rhamnoside in the methanolic extract was 30.01
µg/mg while for the ethyl acetate was 16.9 µg/mg and also a
higher amount of quercetin-3-O-rhamnoside (19.8 µg/mg) was
obtained by the methanolic extract than by the ethyl acetate (8.2
µg/mg) (Riethmuller et al., 2015).
Cerulli et al. (2018) investigated the metabolomic
fingerprinting of the leaves of Corylus avellana L. (Tonda di
Giffoni, Italian cultivars) by applying the technique of
maceration, infusion, and SLDE-Naviglio extraction (Naviglio
et al., 2019), which is an eco-friendly solid-liquid extraction
technique, allowing us to apply different pressure at different
times within a short time compared to maceration and infusion.
The extracts with the highest phenolic content were evaluated
at optimum extraction conditions, which are 50% ethanol, 1:30
(solid:solvent ratio), 10 h for the maceration; 10:100 for the
infusion, and 8 min for the SLDE-Naviglio extraction, and it
was found that the phenolic content in each extract was 608.10
mg GAE (gallic acid equivalent) /g extract, 170.57 mg GAE/g
extract, 471.80 mg GAE/g extract, respectively. Although the
highest phenolic content was in the maceration process, the
highest radical scavenging activity (100.33 µg/mL EC50 for
DPPH, 1.62 mg/mL for TEAC value) was observed in the
extract with SLDE-Naviglio extractor as compared to the
maceration, the infusion, and quercetin 3-O-rhamnopyranoside.
The amount in which it did not show the cytotoxic effect, at 5
µg/mL, 42% inhibition was achieved on pyocyanin, which
triggers reactive oxygen species and inflammation.
In addition to flavonoid glycosides (kaempferol 3-O-
rhamnopyranoside, quercetin 3-O-rhamnopyranoside,
myricetin 3-O-rhamnpyranoside, kaempferol 3-O-
rhamnopyranoside), Giffonin A-T, known as diarylheptanoids,
were detected in the leaves (Cerulli et al., 2018).
Diarylheptanoids, secondary metabolites in plants, are another
bioactive compounds contributing to the antioxidant activity of
hazelnut tree leaves. They are composed of a 1,7-
diphenylheptane skeleton and can be classified into subgroups;
linear and macrocyclic, depending on their chemical structure
(Figure 2) (Vanucci-Bacqué & Bedos-Belval, 2021). They have
been proven to exhibit many biological activities such as anti-
inflammatory, anti-carcinogenic, anti-oxidant, anti-microbial
(Ganapathy et al., 2019).
Diarylheptanoids were identified and characterized in the
leaves of Corylus avellana, Corylus maxima, Corylus colorna
(Cerulli et al., 2018; Masullo et al., 2015a; Masullo et al.,
2015b; Riethmuller et al., 2013; Riethmuller et al., 2014;
Riethmuller et al., 2015). Riethmuller et al. (2013) compared
the amount of hirsutenone observed in the extract from the
leaves of Corylus avellana L. with methanol (0.33 µg/mg
extract) and ethyl acetate (2.08 µg/mg), and their results
indicated that the most suitable solvent to obtain a high amount
of hirsutenone (for other diarylheptanoids detected in the study)
was ethyl acetate (Riethmuller et al., 2013). The same result for
Öztürk / Eur Food Sci Eng 2023, 4 (1), 15-25
18
Figure 2. Chemical structure of diarylheptanoids; a: linear skeleton; b, c: macrocyclic skeleton (Vanucci-Bacqué & Bedos-Belval,
2021)
the leaves of Corylus maxima was reported by Riethmuller et
al. (2015), that is, the content of oregonin (3.40 µg/mg) and
hirsutenone (8.39 µg/mg) obtained the extract with ethyl acetate
were higher than the methanolic extract (2.21 µg/mg, 0.59
µg/mg, respectively) (Riethmuller et al., 2015).
Giffonin A-I, Giffonin J-P, and Giffonin W-X were isolated
and characterized from the leaves of Corylus avellana (Tonda
di Giffoni, Italian cultivars) and methanolic extract of which
tested on plasma lipid peroxidation caused by both H2O2 and
H2O2/Fe+2 as well as against oxidation of thiol groups in plasma
proteins and human cancer cells (U2Os and SAOs cells). With
no cytotoxic on the cancer cells, all the extracts (except for
oregonin, and giffonin V only in H2O2) exhibited an inhibitory
effect on lipid oxidation (H2O2 and H2O2/Fe+2), which ranged
between 2.2-64.3%, 4.0-63.2%, respectively. While the lowest
inhibition was found in Giffonin B and J in H2O2- or H2O2/Fe+2-
induced lipid oxidation, the highest inhibition was observed
from Giffonin D in both assays compared to curcumin, the most
studied diarylheptanoid today (Masullo et al., 2015a; Masullo
et al., 2015b; Masullo et al., 2021). Moreover, giffonins
decreased protein carbonylation induced H2O2 and H2O2/Fe+2
by inhibiting the oxidation of thiol groups in the protein
(Masullo et al., 2021).
Taxane refers to a group of diterpenoid skeletal compounds,
which was first isolated from yew-Taxus species, by far more
than five hundred compounds have been characterized based on
eleven different taxane skeletal structures (Nižnanský et al.,
2022; Wang et al., 2011) (Figure 3). One of the widely studied
taxane types today, paclitaxel (Taxol is tradename, an anti-
cancer chemotherapy drug) is used for treating many types of
cancer such as breast, lung, prostate, and ovarian. With
obtaining in very low amounts from natural sources, it is also
possible to produce paclitaxel by semi-synthetic or cell culture
methods (Gallego et al., 2017). Paclitaxel, 10-deacetylbaccatin
III, baccatin III, 10-deacetyl-7-xylosylcephalomannine, 10-
deacetyl-7-xylosylpaclitaxel, 10-deacetyl-7-xylosylpaclitaxel
C, 10-deacetylpaclitaxel, 7-xylosylpaclitaxel, cephalomannine,
10-deacetyl-7-epipaclitaxel, paclitaxel C, 7-epipaclitaxel, and
taxinine M have been detected in hazelnut tree leaves (Ottaggio
et al., 2008). In the defatted-samples, the amount of paclitaxel,
10-deacetylbaccatin III, and cephalomannine were found to be
0.08-0.74 µg/g, 1.48-7.71 µg/g, 0.01-0.16 µg/g, respectively
(Hoffman & Shahidi, 2009). The amount of taxane-derived
compounds in the leaves is higher than in its shell (Ottaggio et
al., 2008).
Another of the bioactive compounds found in hazelnut
leaves is alpha tocopherol, which is a type of vitamin E. The
amount of alpha tocopherol in hazelnut leaves can vary between
34.6-237.4 µg/g, the highest amount was found in the Moro
variety grown in the Saldinia region, in Italy (Sivakumar &
Bacchetta, 2005).
Figure 3. Chemical structure of some taxanes (Nižnanský et al.,
2022; Wang et al., 2011)
3. Hazelnut Husk
Hazelnut husk is the plant tissue that surrounds the shelled
hazelnut from the outside, is also called as green leafy cover
(Alasalvar et al., 2006b), green shell cover (Hoffman &
Shahidi, 2009), hazelnut involucre (Rusu et al., 2019), and
green outer nut husk (Oguzkan et al., 2018). After the harvest
of hazelnut, the hazelnut is separated from the husk by the
hazelnut threshing machine in the drying place, and then either
may be left in the area where it is dried or burned (Sayar et al.,
2019) or used as fertilizer for the hazelnut orchards (Kizilkaya,
2016), plant growing (Özenç, 2006) and used to improve soil
quality (Zeytin & Baran, 2003). Furthermore, it can be
considered as a raw material, known as biomass, in bioethanol
production (Sayar et al., 2019) and may be used as potentially
a raw material in value-added biochemical production such as
levulinic acid (Sajid et al., 2021), lactic acid (Dusselier et al.,
2013), and hydroxymethylfurfural (Van Putten et al., 2013)
because of being rich in its lignocellulosic content which is
made up of holocellulose (55.1%), α-cellulose (34.5%), and
lignin (35.1%) (Çöpür et al., 2007). Monosaccharides such as
glucose and, fructose are firstly obtained from lignocellulosic
biomass in the presence of acids, alkaline reagents, organic
solvents, ionic liquids, deep eutectic solvents, enzymes, and
Öztürk / Eur Food Sci Eng 2023, 4 (1), 15-25
19
microorganisms and then these sugars are converted into the
value-added chemicals (Ashokkumar et al., 2022). Hazelnut
husk might be a potentially important raw material source due
to its lignocellulosic content, being cheap and widespread
availability; it emerged at the rate of one-third of the shelled
hazelnut, so it is estimated that approximately 200 thousand
tons of it is released annually in Turkey alone (Tufan et al.,
2015).
In a study by Alasalvar et al. (2006b), the antiradical and
antioxidant activity of hazelnut husk was evaluated, in which
50% ethanol and 50% acetone solvents were used to extract its
phenolic acids. According to the results of the study, total
phenolic (201 mg CE/g), condensed tannin (542 mg CE/g), total
antioxidant activity (1.29 mmol TE/g), and IC50 (0.065 mg)
obtained from the extract of 50% acetone were higher than
those of 50% ethanol extract (156 mg CE/g, 385 mg CE/g, 1.14
mmol TE/g, 0.074 mg, respectively). Moreover, hydrolysis was
applied to the hazelnut husk with HCl, and gallic acid was
found to be the dominant phenolic acids among free (269 µg/g)
and esterified ones (1450 µg/g) (Alasalvar et al., 2006b).
Shahidi et al. (2007), determined the antioxidant
phytochemicals in by-product of the hazelnut and gallic,
caffeic, ρ-coumaric, ferulic, and sinapic acid from the hazelnut
husk extract with 80% ethanol were found to be 892 µg/g, 158
µg/g, 1662 µg/g, 327 µg/g, 64 µg/g (both free and esterified)
(Shahidi et al., 2007). The highest antiradical activity was
observed at 200 ppm for hydrogen peroxide (97%), superoxide
radical (99%), and DPPH radical (99.5%). Hydroxyl radical
activity, an index of DNA damage, was tested at different
concentrations ranging from 5 ppm to 50 ppm, and it was
determined that the inhibition increased as the concentration
increased, so the highest inhibition against the hydroxyl radical
was achieved at 50 ppm (89.9%) (Shahidi et al., 2007). In
another study investigating the antimicrobial and antioxidant
activity of the hazelnut husk was conducted by Cerulli et al.
(2017) and they isolated and characterized the first giffonin T,
U as well as giffonin I, citric acid, 1-methylcitrate,
trimethylcitrate, kaempferol 3-O-rhamnopyranoside, 3,5-
dicaffeoylquinic acid, myricetin 3-O-rhamnopyranoside, and
kaempferol 3-O-(4″-trans-pcoumaroyl) rhamnopyranoside
from the methanolic extract of the hazelnut husk. The highest
and lowest inhibition in the antioxidant activity against lipid
peroxidation induced by H2O2 and H2O2/Fe+2 of the isolated
compounds was recorded for myricetin 3-O-rhamnopyranoside
(44.4%), kaempferol 3-O-rhamnopyranoside (5.7%), and
kaempferol 3-O-(4″-trans-pcoumaroyl) rhamnopyranoside
(39.7%), myricetin 3-O-rhamnopyranoside (34.1%),
respectively. They found that carpinontriol B and giffonin U in
the methanolic extract of hazelnut husk were the most effective
compounds against Bacillus cereus, Escherichia coli,
Pseudomonas aeruginosa, and Staphylococcus aureus (Cerulli
et al., 2017). Rusu et al. (2019) investigated the bioactive
content from the hazelnut involucre, including phenolics and
sterolic compounds with D-optimal design. The optimum
extraction point for the content of total phenolic, total
flavonoid, condensed tannin and antioxidant activity was found
to be mixing time 3 min, pH 3 and 50% acetone, as 377.43 mg
GAE/g, 43.10 mg QE-quercetin equivalent/g, 280.69 mg CE/g,
1296.51 mg TE/g (TEAC), 292.23 mg TE/g (DPPH), 350.52
mg TE/g (FRAP), respectively. Considering the results of the
study, different amounts of individual phenolics and
phytosterols were obtained under the different extraction
conditions used in the study. The highest amount of
epicatechin, catechin, syringic acid, gallic acid, protocatechuic
acid, vanillic acid, p-coumaric, ferulic acids, hyperoside,
quercitrin, and isoquercitrin were determined to be 3.73,
243.02, 5.53, 91.93, 227.37, 25.41, 6.58, 3.97, 51.72, 17.74, and
114.26 µg/g, respectively. In the case of phytosterol, the
optimum extraction conditions for stigmasterol (197.31 µg/g),
and β-sitosterol (5305.01 µg/g) were stirring time 2, pH 5, and
25% acetone while those for campesterol (45.04 µg/g) was
stirring time 3, pH 5, and 25% acetone. Additionally, the extract
from hazelnut involucre at the optimum extraction condition
was evaluated for enzyme (tyrosinase inhibitory activity and α-
glucosidase inhibitory activity) and anticancer activity (A549-
human lung adenocarcinoma and T47D-KBluc-human breast
cancer). IC50 of hazelnut involucre extract for tyrosinase
inhibitory activity was 165.17 mg KAE/g whereas those for α-
glucosidase inhibitory activity was 0.1 mg/g. Without the
cytotoxic effects on human gingival fibroblasts up to very high
doses (>300 µg/mL), the hazelnut involucre extract was found
to be effective on two cancer cells- A549, T47D-KBluc at 50
and 75 µg/mL (Rusu et al., 2019).
This effect of hazelnut husk on cancer cells may be due to
the anticancer compounds it contains. Taxane class compounds
such as baccatin III-precursor for the semi-production of
paclitaxel have been detected in hazelnut husk as do in the
hazelnut leaf. Hoffman & Shahidi, (2009) found the quantities
of baccatin III in the ethanolic extract obtained from hazelnut
husk of Tombul cultivar, grown in Giresun (in Turkey) after
defatting with hexane ranged from 1.10 to 67.77 µg/g (Hoffman
& Shahidi, 2009), but not detected the other taxanes containing
10-deacetyl baccatin, 10-deacetyl taxol, cephalomannine, 7-
epi-10-deacetyl taxol, and paclitaxel. A similar result was also
reported by Oguzkan et al. (2018) and they investigated taxanes
in the extract with acetone (at 1:10 g/mL), depending on
altitudes and regions in Turkey. They determined that the
amount of baccatin III varied from 166.12 µg/kg to 923.64
µg/kg, and the highest quantities were obtained from the extract
up to 250 m altitude in Vakfıkebir, in Turkey (Oguzkan et al.,
2018).
Cabo et al. (2021) have conducted on the phenolic
composition and antioxidant activity of the hazelnut husk of
different cultivars (Butler, Grada de Viseu, Lansing and Morell
in Portugal) by using different solvents including methanol,
water, acetone, hexane, and ethyl acetate. They determined and
quantified the phenolics (gallic acid, protocatechuic acid, (−)-
epicatechin, quercetin-3-o-rutinoside, ellagic acid, luteolin-7-
o-rutinoside, vanillic acid, kaempferol-3,7-odiglucoside,
kaempferol-3-o-[6-acetylglucoside]-7-oglucoside, kaempferol-
3-o-[6-acetylglucoside]-7-orhamnoside), chlorophyl a-b, and
total carotenoids from the hazelnut husk. The total amount of
phenolics, flavonoids and total carotenoid obtained with
methanol was higher than those with water, acetone, ethyl
acetate and hexane whereas the highest chlorophyl content was
achieved with acetone. It was emphasized that the hazelnut
cultivar and the type of solvent used in the study were effective
on the amount of bioactive components from the hazelnut husk
(Cabo et al., 2021).
4. Hazelnut Oil Meal
Oil from oilseeds can be obtained using various methods,
which can be classified as chemical, high pressure, distillation,
and mechanical systems (Ionesu et al., 2016). Hazelnut is an
important source of oil raw material and it contains 60% of oil
on average, and the main component of its oil is triacylglycerol
(Celenk et al., 2020). The triacylglycerol is composed of high
levels of oleic acid and, linoleic acid, followed by palmitic and
stearic acid (Venkatachalam & Sathe, 2006). In addition to this,
it also possesses important food components such as phenolic
Öztürk / Eur Food Sci Eng 2023, 4 (1), 15-25
20
compounds, B1, B2, B6, β-carotene, lutein/zeaxanthin,
tocopherols (α-, β-, γ-, δ-), phytosterols, essential amino acids,
serotonin, and minerals (Alasalvar et al., 2009; Alasalvar et al.,
2006a; Alasalvar et al., 2003; Celenk et al., 2018; Jiang et al.,
2021; Pelvan et al., 2018; Stuetz et al., 2017; Tas et al., 2019;
Taş & Gökmen, 2015).
After the hazelnut oil is obtained with a suitable oil
extraction technique, the cake remains, which is called as
hazelnut oil meal or hazelnut cake in the hazelnut oil industry.
The composition of the cake might change on the basis of the
extraction methods and solvents used in the extraction process
(Geow et al., 2021), in general, the hazelnut cake can include in
the range of 81.70-95.87% dry matter, 39.2-54.5% protein, 1-
17.38% lipid, 25.20-48.00 % carbohydrate, 4.97-8.64% ash and
essential amino acids content account for 17.40-33% of total
proteins in the hazelnut cake (Acan et al., 2021; Altop et al.,
2019; Aydemir et al., 2014; Gul et al., 2017; Sen & Kahveci,
2020; Xu & Hanna, 2011; Yalçin et al., 2005). Its protein
content can be increased up to 94.2% by pretreatments such as
acetone washing, alkali extraction and precipitation (Aydemir
et al., 2014), or up to 94.8% by proteolytic enzymes (Çağlar et
al., 2021b). It has been reported that the essential amino acid
content of the hazelnut cake obtained by precipitation after
alkaline extraction was up to 37% (Sen & Kahveci, 2020) and
arginine was the main dominant essential amino acid, followed
by leucine, isoleucine, and phenylalanine (Sen & Kahveci,
2020; Xu & Hanna, 2011).
Because of its high protein content, it might be generally
added to diets of animal and fish as a protein source (Karabulut
et al., 2019; Kirmizigül & Cufadar, 2019), however, recently, a
number of studies have been conducted to determine its
technological and bioactivity properties in food technology
(Gul et al., 2017; Saricaoglu et al., 2018; Tatar et al., 2015) and
to use it an ingredient in food formulations such as hazelnut
milk (Gul et al., 2017), functional kefir drink (Atalar, 2019),
functional beverage (Sen & Kahveci, 2020), chocolate spread
(Acan et al., 2021), chocolate (Bursa et al., 2021), ice cream
with the hazelnut milk (Atalar et al., 2021), hazelnut paste
(Göksu et al., 2022), and functional yogurt with hazelnut
beverage (Gul et al., 2022). What’s more it exhibits antioxidant,
antiproliferative, antidiabetic, and antihypertensive activity
owing to its phenolic compounds and peptides (Aydemir et al.,
2014; Eroglu & Aksay, 2017; Simsek, 2021).
Simsek et al. (2017) analyzed the phenolic composition of
defatted hazelnut cake obtained from seventeen hazelnut
varieties grown in Turkey and found that the total phenolic
content of the hazelnut cake varied between 5.29-10.93 mg
GAE/g. Mincane had the highest total phenolic content among
the seventeen hazelnut varieties whereas the lowest content was
found in Foşa. Concerning the phenolic composition in the
samples, (+)-catechin was the predominant phenolic, followed
by catechol, chlorogenic acid, and quercetin (Simsek et al.,
2017). They emphasized that there was a significant difference
in terms of phenolic composition and TPC between the hazelnut
cakes tested (Simsek et al., 2017). In previous studies, it pointed
out that the variety was effective on the phenolic composition
of hazelnut skin (Lelli et al., 2021).
A study by Xu & Hanna (2011), in which the extracts from
defatted meal in Nebraska was evaluated their physicochemical
and bioactivity properties and total phenolic content, tannins,
and condensed tannin were found to be 10.7 mg TA (tannic
acid)/g, 7.53 mg TA/g, 0.64 mg TA/g, respectively.
Furthermore, in the study, it has been stated that it may be an
important raw source for minerals, mainly K, P, Ca, and Mg, to
human nutrition (Xu & Hanna, 2011).
Bioactive peptides are compounds with bioactivity, which
are inactive in the parent protein, which have between 2-20
amino acid sequences with low molecular weight (<6000 kDa)
in general (Karami & Akbari-Adergani, 2019). Enzymatic
hydrolysis and microbial fermentation are used to produce the
bioactive peptides, or they can be synthesized via chemical
methods or recombinant DNA technology (Akbarian et al.,
2022). The important sources of the bioactive peptides are
animals, plants, foods, edible insects, marine organisms, and
waste, especially agri-food waste (Chai et al., 2020).
Temperature, pH, enzyme used, the length, charge,
hydrophobic/hydrophilic properties and type of the amino acid
might affect their biological features, such as antioxidants,
antimicrobial, antidiabetic, antihypertensive, antiobesity,
antithrombotic antiaging, opioid, hypocholesterolemic, and
mineral binding activity (Akbarian et al., 2022).
Researchers have reported that hazelnut cake contains
bioactive peptides released by various enzymes such as trypsin,
pepsin, chymotrypsin, or extracted after pretreatments such as
acetone washing or heating (Aydemir et al., 2014; Çağlar et al.,
2021b; Simsek, 2021). It has been reported that the combination
(86.0%) of acetone washing and heat treatment reduced the
protein content of hazelnut meal compared with those of both
individual treatment (93.3%, 94.5%) and hazelnut protein
isolate (94.2%), respectively, but the antioxidant activity of the
combination, measured TEAC and ORAC, was increased. The
combination treatment increased ACE (Angiotensin
Converting Enzyme) inhibition level by 40% compared to the
untreated sample, from 50% to 70%, with IC50 1 mg/mL and,
0.57 mg/mL, respectively (Aydemir et al., 2014).
Depending on the enzyme used in the research, different
degrees of free hydrolysis were determined in the hazelnut
meal. The degree of hydrolysis for pepsin, papain, thermolysin,
bromelain, trypsin, alcalase, chymotrypsin, protamex,
trypsin+chymotrypsin (combined) were 74.33%, 60.97%,
50.4%, 46.18%, 26.4%, 23.5%, 21.8%, 18.8%, 13.7%,
respectively (Çağlar et al., 2021a; Göksu et al., 2022; Simsek,
2021). Trypsin was used in a study by Gülseren & Çakır (2019),
at the end of 4 h incubation with the enzyme, ACE inhibition
level of the hazelnut cake increased from 7.6% to around 40%
(Gülseren & Çakır, 2019). In a study, pepsin was used to
produce bioactive peptides from the hazelnut cake at different
times (0, 30, 60 min), its isolate fraction (98.77%) was found to
be higher than their hydrolysates when their inhibition levels
(98.25%, 97.37%) against ACE were compared, respectively,
but the highest IC50 (0.22 mg protein/mL) value was observed
in the hydrolyzed fraction obtained at 60 min, in comparison to
those of the isolate fraction (1.29 mg protein/mL) (Eroglu &
Aksay, 2017). Eroglu et al. (2020) found a similar decreasing
trend in IC50 value, in which the hazelnut protein isolate and its
hydrolysates were prepared pepsin and trypsin, IC50 of them at
0, 30, 60 and 120 minutes followed the order of 1.47-0.27-0.27-
0.26 mg protein/mL; 5.51-0.61-0.56-0.54 mg protein/mL,
respectively (Eroglu et al., 2020).
Another study, incorporation of three enzymes (alcalase,
protamex, trypsin+chymotrypsin) into a mixture prepared with
the hazelnut meal, was performed and their inhibition activity
for ACE, DPP‑IV (Dipeptidyl peptidase), and α‑glucosidase
were investigated. It was found that hydrolysates with a 5-20
kDa had higher ACE inhibition value while those with lower
than 5 kDa showed higher DPP‑IV and α-glucosidase activity
(Simsek, 2021). IC50 of the peptides with 5 kDa-20 kDa in the
study, which were released by alcalase and
trypsin+chymotrypsin except for protamex, ranged from 0.10
to 0.18 mg/mL, 0.37 to 1.28 mg/mL, 0-4.76 mg/mL for ACE,
DPP-IV, and α‑glucosidase, respectively (Simsek, 2021).
Öztürk / Eur Food Sci Eng 2023, 4 (1), 15-25
21
Mundi & Aluko (2014) found that <1 kDa to >5 kDa peptide
fractions obtained from kidney bean showed better ACE
inhibition and antioxidant activity compared to 1-3 kDa, 3-5
kDa fractions, and it was emphasized that this feature may be
due to amino acids with hydrophobic and aromatic characters
such as valine, isoleucine, leucine, and phenylalanine,
tryptophan, respectively (Mundi & Aluko, 2014). Gülseren
(2018) obtained twenty-three ribosomal proteins from hazelnut
cake, by digesting it with gastrointestinal (trypsin, pepsin,
chymotrypsin) and non-gastrointestinal enzymes (lysin, papain
and bromelain) and examined their bioactive properties
(DPP‑IV, ACE) via silico proteolysis using UniProtKB,
BIOPEP, and PeptideRanker. According to the results of the
research, the bioactivities of peptides produced with non-
gastrointestinal enzymes were higher than those of
gastrointestinal enzymes, especially papain was the dominant
enzyme in comparison of the others in terms of the potential
bioactivity, which followed the order DPP‑IV (50.68-76.34 %),
ACE (16.67-50.23 %), and antioxidative activity (Gülseren,
2018).
Çağlar et al. (2021a) produced the bioactive peptides with
ACE inhibitory activity from the hazelnut cake of Tombul
hazelnut (Giresun) obtained after the extraction oil by using the
enzymatic treatment including trypsin, chymotrypsin, and
thermolysin. They determined three peptides by means of LC-
Q-TOF/MS and in silico analyses, namely, SPLAGR (trypsin-
treated), VPHW (chymotrypsin-treated), and PGHF
(thermolysin-treated), which have sixteen, ten, and eleven sites
that can bind to the ACE molecule, respectively, compared to
VPP (eleven sites binding to ACE) which is one of the most
studied dairy-derived tripeptides (Çağlar et al., 2021a). The
authors calculated the molecular docking scores for SPLAGR,
VPHW, and PGHF through HPEPDOCK (Zhou et al., 2018),
which is a web server service used to predict potential
interaction between a protein and ligand, for example ACE and
the hazelnut protein. According to the results, the molecular
docking scores of SPLAGR (−179.023), VPHW (−202.333),
and PGHF (− 192.080) were higher VPP (−96.288), indicating
that these hydrolysates from the hazelnut cake could be
potential inhibitory against ACE (Çağlar et al., 2021a). The
research revealed that this interaction was due to amino acids
with nonpolar and aromatic rings (tryptophan and
phenylalanine) and amino acids with basic and polar character
(arginine) (Çağlar et al., 2021a). In another study, molecular
docking scores were also found to be higher for LEPTNRIEA
(−163.872) and IQVNKENKEFK (−188.424), from hazelnut
cake, than VPP (−97.004) based on PeptideRanker scores
(Göksu et al., 2022). Additionally, the hydrolysates from the
hazelnut cake, which were the fraction of bromelain, papain,
and pepsin, were incorporated into the hazelnut paste
formulation at ratio of %1, and it was observed that the fractions
were not adversely affected by the processes in the production
of hazelnut paste and thus maintained their ACE inhibition
level (94.21-94.82%) after the production compared to
captopril (95.26%) (Göksu et al., 2022).
Çağlar et al. (2021b) determined 256 hazelnut peptides from
Tombul hazelnut in Giresun by using proteases (trypsin, pepsin,
chymotrypsin, papain, thermolysin and bromelain) through LC-
Q-TOF/MS, 7 of which posed a potential high anti-DPP‑IV
activity according to the results of the silico analyses. They
suggested that the interaction between potential bioactivity
peptides from the hazelnut cake, namely, PGHF,
FMRWRDRFL, APGHF, FFFPGPNK,
LSVPNLYVWLCMFY,
NSMVGNMIFWFFFCILGQPMCVLLYYHDLMNR,
LILVSFSLCLLVLFNGCLG, and DPP‑IV could be due to the
hydrophobic properties of the amino acids in the hazelnut cake
(Çağlar et al., 2021b). Liu et al. (2018) emphasized that leucine
is an important amino acid in the inhibition of ACE by hazelnut,
as it is a common amino acid in all three bioactive biopeptides,
called as AVKVL, TLVGR, and YLVR, produced using
alcalase from hazelnut. Moreover, they suggested that cation–π
interaction which is a non-covalent bond, as well as
electrostatic force and hydrogen bonding, play a role in the
interaction between ACE and these three (AVKVL, TLVGR,
YLVR) hazelnut hydrolysates (Liu et al., 2018).
The plastein reaction is a chemical reaction whereby peptide
bonds in proteins or peptides are hydrolyzed with proteases
such as alcalase, papain, and bromelain with a high ratio (%20-
50, hydrolyzed product:enzyme), and then ultimately it results
in a mixture rich in peptides with high molecular weight
through the formation of new peptide bonds between partially
hydrolyzed peptide chains, which is known as plastein.
Structural and biological changes can occur in plastein at the
end of the reaction, which include its particle size, surface
hydrophobicity, antioxidant, and ACE inhibition activity and so
on (Udenigwe & Rajendran, 2016).
It has been reported that the plastein reaction is a suitable
method for modifying hazelnut proteins. Song et al. (2023)
modified the hydrolysates from the hazelnut with the plastein
reaction by using alcalase in their study, and they found that the
ACE inhibitory activity of the plastein (60.74%) was higher
than hydrolysates of the hazelnut (41.43%). Moreover, they
found that the ACE inhibitory activity of the mixture obtained
after the reaction (93.56%) was much higher than YLVR
(52.58%) which was used as a substrate to perform the plastein
reaction with alcalase (Song et al., 2023).
In addition to having their ACE inhibitory activity, peptides
from the hazelnut can also exhibit antioxidant activity,
especially those containing methionine, tyrosine, and
tryptophan residues at the located C-terminal (Shi et al., 2022).
Along with emphasizing the importance of amino acid
composition and sequence in a peptide, Shi et al stated that in
peptides obtained from the hazelnut hydrolysates, the C-
terminus and order of the tyrosine amino acid can affect the
functional properties of the peptide (Shi et al., 2022).
5. Conclusion
Hazelnut, which has an important commercial value around
the world, is processed into various products. During the
process, by-products such as hazelnut tree leaf, husk, skin, and
oil meal emerge, which possess the bioactive compounds such
as phenolics, dietary fibre, bioactive peptides, and fatty acids.
These substances have been proven to have the antioxidant,
antiradical, antimicrobial, and antihypertensive effects in both
vitro and silico. Therefore, bioactive compounds to be obtained
using environmentally friendly extraction methods and
solvents, such as ultrasound extraction or deep eutectic solvent,
which are the basis of the circular economy, can be used in the
food industry, pharmacy, and cosmetics industry. More
research should be conducted to test their stability in different
medium including food matrix or emulsion or exposed to
different heating and its time.
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