Moro (2021)
Moro (2021)
Moro (2021)
Review
A R T I C L E I N F O A B S T R A C T
Keywords: The roots and tubers of the Asteraceae family are known as a source of various oligosaccharides, and chicory roots
High fiber roots and Jerusalem artichoke have stood out for its commercial viability. However burdock root (Arctium lappa L.),
Fructans which is adapted to temperate climate, moist, and sandy soil, is still unknown as health food in the western
Oligofructose
world. This review showed the potential of burdock roots as a source of prebiotic fibers, chlorogenic acids,
Caffeoylquinic acid
cinnarine, lignans, and quercetin. The extraction methods of burdock functional compounds are made with
Biological activity
water, temperature and time variations only. Biological assays showed antioxidant activity, anti-inflammatory,
Chemical compounds studied in this article:
Fructose (PubChem CID: 2723872)
and hypolipidemic properties, and gastric mucosal defense mechanisms, among others. Therefore, the use of
Glucose (PubChem CID: 5796) burdock roots as functional food should be encouraged in countries that have imported products derived from
Sucrose (PubChem CID: 5988) other roots of the same family for health benefits.
1-Kestose (PubChem CID: 440080)
1-Nystose (PubChem CID: 166775)
Fructofuranosylnystose (PubChem CID:
3085157)
Inulobiose (PubChem CID: 439552)
5-O-Caffeoylquinic acid (PubChem CID:
5280633)
1,5-Dicaffeoylquinic acid (PubChem CID:
6474640)
Caffeic acid (PubChem CID: 689043)
1. Introduction esculenta) and potatoes (Solanum tuberosum) are sources of energy and
subjected to industrial processes (Eliasson, 2004). In contrast, other
The World Health Organization (WHO) has published that more than tubers present processing challenges, especially non-starchy tubers, as
1.9 billion adults were overweight and obese in 2016, which represents they have been neglected for a long time due to low consumption, with
almost 40% of the world’s population. This prevalence has also no data about its cultivation worldwide. This scenario has been changed
increased among children and adolescents, with a population of after several studies have shown the importance of prebiotic fibers in
approximately 400 million individuals aged 0–18 years (Who, 2018). In food, and tubers such as Jerusalem artichoke (Kocsis, Liebhard, &
addition, in the face of the current world reality on the coronavirus Praznik, 2007) and chicory (Pilon, Oetterer, Gallo, & Spoto, 2006) have
pandemic, in which people with chronic non-communicable diseases are gained some economic importance.
risk group for COVID-19 (Stefan, Birkenfeld, Schulze, & Ludwig, 2020), Non-starchy roots and tubers belonging to the family Asteraceae are
the dissemination and investment in foods that promote health and known to have the oligofructose and inulin as reserve carbohydrates,
satiety, and easily accessible by low-income population are needed with prebiotic activity (Flamm, Glinsmann, Kritchevsky, Prosky, &
(Hobbs, 2020). Starchy roots and tubers, such as cassava (Manihot Roberfroid, 2001). Although some of them have been widely studied,
* Corresponding author.
E-mail address: mclerici@unicamp.br (M. T.P.S. Clerici).
https://doi.org/10.1016/j.foodres.2020.109889
Received 15 January 2020; Received in revised form 6 September 2020; Accepted 4 November 2020
Available online 10 November 2020
0963-9969/© 2020 Elsevier Ltd. This article is made available under the Elsevier license (http://www.elsevier.com/open-access/userlicense/1.0/).
T.M.A. Moro and M. T.P.S. Clerici Food Research International 141 (2021) 109889
such as chicory root (Cichorium intybus L) (Moser, Agemans, & Caers, Mediterranean climate. Humid, low light, and sandy soils are indicated
2014) and Jerusalem artichoke (Helianthus tuberosus L) (Rubel, Pérez, to facilitate harvesting and allow root growth without fibrousness and
Genovese, & Manrique, 2014), others have more restricted consumption deformation. After sowing, the harvest period varies between 120 and
such as yacon (Smallanthus sonchifolius L) in Peru (Zhu et al., 2012), 180 days, with an average harvest at 150 days (Munarin et al., 2010).
agave (Agave angustifolia L) in Mexico (Ávila-Fernández, Galicia- In Brazil, it is cultivated from March to September, at milder tem
Lagunas, Rodríguez-Alegría, Olvera, & López-Munguía, 2011) and peratures and drier climate (Munarin et al., 2010). Although there is no
burdock root (Arctium lappa L), which can be cultivated in several cli robust scientific data, the burdock production in Japan is estimated at
mates (Munarin, Herediazárate, Vieira, Rosa, & Rodrigues, 2010), with 161.3 tons per year (Statista, 2016). The productivity of this species
a higher potential for food application. Burdock root has limited use in varies according to the cultivars used; for example in New Zealand, the
folk medicine, being consumed as food in countries in Asia and Europe. production yields vary between 8 and 40 tons per hectare of planting
Some studies have focused on the use of burdock root as an ingredient in (Douglas, Burgmans, Burton, & Smallfield, 1992). In Brazil and other
bread (Tae, Kim, & Yook, 2015), and cookies (Moro et al., 2018), which cultivating countries, such as China, Japan, and South Korea, planting is
was studied by our research group. carried out by family farming, and there is a lack of data on burdock
Chan et al. (2011) reported in a review the main therapeutic appli cultivation, value, and marketing volume.
cations of the components of burdock roots, with emphasis on the
identification of lignans, tepenoids, polyphenols, fructose, and sterols 3. Chemical composition of burdock roots
and their respective effects. However, there is no information on the
functional properties and dietary applications of the roots alone. According to the United States Department of Agriculture (USDA,
Therefore, this study aimed to present the potential of burdock root as a 2015) composition table, the burdock root contains 80% moisture, 1.5%
novel food and ingredient, which can promote satiety as a source of protein, 0.9% ash, and 0.1% lipids, and the total carbohydrates (calcu
fiber, with cultivation and consumption by family farming. lated by difference) correspond to 17.5%, which are the most prominent
nutrients. Burdock root also presents antioxidant compounds with
2. Taxonomy and botanical characteristics of burdock (Arctium health benefits, such as caffeine, flavonoids, and lignans (Predes, Ruiz,
lappa L) Carvalho, Foglio, & Dolder, 2011), which will be discussed further in
this review.
2.1. Taxonomy
3.1. Burdock root carbohydrates
The scientific classification of Arctium lappa L taken from the USDA
Plant Database (USDA, 2020) is kingdom: Plantae; subkingdom: Tra According to the Gibson and Roberfroid (1995) criteria for classifi
cheobionta; super division: Spermatophyta; division: Magnoliophyta; class: cation of inulin-type fructans, oligofructoses are characterized by chains
Magnoliopsida; subclass: Asteridae; order: Asterales; family: Asteraceae ⁄ with 2 to 9 fructose units, while inulin consists of fructose chain that
Compositae; genus: Arctium L.; and species Arctium lappa L. contains more than 10 fructose units. Both are considered prebiotics, a
substrate that is selectively used by host microorganisms conferring a
health benefit, mainly in the digestive system, but also in the circulatory,
2.2. Botanical characteristics of burdock nervous and locomotor systems (Gibson et al., 2017). As reported by
Hao, Chen, Zhong, Chen, and Li (2005), burdock presents inulin-type
Burdock is a species belonging to the Asteraceae family and Cardueae fructans, in addition to the monosaccharides fructose, glucose, and
tribe. It is a shrub that grows up to about one meter high, and has a
branched and shirred stem with a diameter of 1 to 2 cm. It has major root
development, with few branches, and reaches 45–50 cm depth, a 3–6 cm
in diameter, and 100–250 g (Munarin et al., 2010).
Small cavities are located at the center of the root, formed by the
resorption of tissues, especially in plants aged one year or more
(Munarin et al., 2010). Fig. 1a shows a sectional cut of burdock root with
a white to yellow coloring heart; Fig. 1b shows fresh burdock roots, and
Fig. 1c shows a sectional cut representation with a description of the
main root components.
Burdock is cultivated at temperatures between 10 and 25 ◦ C, with
better development between 16 and 22 ◦ C. The temperate climate is
considered adequate with adaptation in places with a subtropical and
Fig. 1. Images and structures of burdock root (Arctium lappa L). Sectional cut of
the root (a) fresh roots (b), and (c) representation with a description of the Fig. 2. Carbohydrate structures of burdock roots (Li et al., 2013; Ishiguro
tissues. Author’s collection. et al., 2011).
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T.M.A. Moro and M. T.P.S. Clerici Food Research International 141 (2021) 109889
sucrose, as can be seen in Fig. 2. storage conditions for burdock roots in polyethylene packages: cooling
The inulin-type fructans found in burdock roots are linear chains (2 ◦ C), refrigeration (8 ◦ C) and ambient temperature (20 ◦ C) for 30 days.
(Fig. 2) of fructose molecules bound together by β-bond (2,1) and a Although lower inulin-type fructans contents were observed in the first
glucose molecule attached to the free end of the chain by α (1,2) and its 10 days for all conditions studied, there were no subsequent changes in
size can be represented by acronym GFn, where n represents the number the roots stored at 2 ◦ C, i.e., the inulin content was preserved from day
of fructoses in β binding (Li et al., 2013; Ishiguro, Ueno, Onodera, 10 to day 30 of storage, indicating that cooling temperature was the
Benkeblia, & Shiomi, 2011). most adequate for the storage of fresh roots.
Hao et al. (2005) and Fu (2009) studied the average size of inulin- Imahori et al. (2010) studied fresh burdock roots stored in poly
type fructans chains from burdock roots, and reported fructose: ethylene packs at 1 ◦ C for 12 weeks, to evaluate the enzymatic activity
glucose ratios of 12: 1 and 14: 1, respectively. These inulin-type fructans and the changes in carbohydrate fraction. The authors found no signif
are formed during the development and growth of burdock, for use as icant changes in the performance of the fructan-exohydrolase enzyme,
energy storage, remaining accessible to the plant when necessary. The while the inulin synthesizing enzymes had random variations during the
chains originate from two sucrose molecules hydrolyzed by the enzyme 12 weeks, leading to an increase in the content of sucrose and oligo
sucrose: sucrose 1-fructosyltransferase (1-SST), on the binding site be fructoses GF2, GF3, and GF4. The authors concluded that the tempera
tween fructose units from α to β. After the formation of the structure ture of storage was sufficient to preserve the inulin content during the
(two units of fructose and one molecule of glucose), there is the release period evaluated, once the activity of the hydrolyzing enzyme remained
of a glucose unit and addition of new fructose units, joined by the free stable.
end of the new molecule, through the enzyme fructan: fructan 1-fructo The inulin contents of burdock roots can reduce after the first flow
syltransferase (1-SST), which increases the chain size (polymerization) ering, thus harvesting should occur until this period to obtain roots with
(Ueno, Ishiguro, Yoshida, Onodera, & Shiomi, 2011). a high content of inulin-type fructan. After harvest, the adequate storage
The concentration of inulin-type fructans depends on the age of the of the roots (1–2 ◦ C) can reach up to 30 days.
root, and Fig. 3 shows a scheme of the carbohydrates metabolism and In addition to the enzymes that act on the metabolism of carbohy
the enzymes that act during the life cycle of the plant and after harvest of drates, the polyphenol oxidase (PPO) present in the root acts on the
the roots (Ueno et al., 2011). phenolic compounds. This enzyme alters the sensory characteristics of
During the first year of plant growth, there is a predominance of the the pre-processed root (after cutting and peeling processes) which may
enzymes SST and FFT, which are inulin-type fructans synthesizers. From limit possible applications. Salt treatment, physical bleaching, and
the first flowering and fruit formation, the levels of inulin-type fructans drying processes should be used for the industrial applications, domestic
are reduced by the enzyme fructan-exohydrolase, which releases fruc processing, and carbohydrate extraction (Murao, Oyama, Nomura,
tose molecules in the root tissue leaving a molecule of sucrose and free Tono, & Shin, 1993). Besides the changes in the sensory characteristics,
fructose. The released fructose and sucrose molecules are used by the PPO reduces the antioxidant capacity of the roots, due to the reduction
plant as an energy source, and also act on the osmotic balance of the of the phenolic contents (Lee-Kim, Hwang, & Kim, 1997). Additional
root, along with smaller chain size oligosaccharides (GF2, GF3, and GF4) information about the phenolic compounds of the roots will be further
(Ueno et al., 2011). discussed.
After harvesting the roots, the inulin-type fructans are the only en In addition to inulin-type fructans carbohydrates, burdock roots also
ergy source of the burdock, which contains fructose to be released contain inulooligosaccharides formed by fructose unit chains, described
gradually through the action of 1-FEH, leading to an increase in osmo by FFn, where n represents the number of fructose molecules bound by β
larity that influences the shelf life of the roots (Ishiguro et al., 2011). 2,1-bond (Ronkart et al., 2007). This type of oligosaccharide was
Some studies on the adequate temperature and storage time of burdock quantified by Ishiguro et al. (2011) in burdock roots, with values of
roots are presented below. approximately 9 g/100 g (dry weight). Those authors also evaluated the
Ishimaru, Kagoroku, Chachin, Imahori, and Ueda (2004) investi changes in inuloligosaccharides (Fig. 2) with low degree of polymeri
gated the post-harvest enzymatic activity of burdock roots and the zation during 42 days of storage at 0, 15, and 20 ◦ C. The formation of
inulin-type fructan content during storage. The authors studied three this type of oligosaccharide is possible due to the high free fructose
Fig. 3. Carbohydrate metabolism of burdock root and enzymes: 1- Sucrose: Sucrose fructosyltransferase (1-SST), 1-Fructan: fructan fructosyl-transferase (1-FFT) and
1-Fructan exohydrolase (1-FEH) increase (+) or decrease (-) of its activities in the life cycle of the plant and after harvesting the roots (Imahori et al., 2010).
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T.M.A. Moro and M. T.P.S. Clerici Food Research International 141 (2021) 109889
contents in the plant tissue, once fructose is the receptor of the 1-FFT technologies have been used by other authors, including Milani, Koo
enzyme. A behavior similar to the inulin-type fructans was observed, cheki, and Golimovahhed (2011), who compared the use of ultrasound
with the reduction of the chain size and consequent increase in these with direct heating, and also observed an increase in the process yield of
carbohydrates with a lower degree of polymerization after 42 days of burdock root extract from 12 to 24%.
storage of the roots at 0 ◦ C.
Table 1
Methods of extraction of burdock root carbohydrates (Arctium lappa L) from studies published from 1930 to 2018.
Fresh/ Extraction method Temperature Time Raw material (g): Extraction Separation Yield Reference
dried (◦ C) solvent (water, mL) number process (%)
Dried Conventional Boiling n.p. 1:10 1 Ethanol n.p.* Krantz and Carr (1930)
Dried Conventional Cold water 24 h 1:60 1 Ethanol 5.2 Kardošová et al. (2003)
Dried Conventional 75 ◦ C 45 1:8 2 Ethanol 7.5 Turdumambetov, Bakirov, and
min. Rakhimov (2004)
Dried Conventional 70 ◦ C 90 1:10 2 Ethanol n.p. Hao et al. (2005)
min.
Dried Conventional 80 ◦ C 2h 1:5 3 Ethanol n.p. Fu (2009)
Fresh Conventional 50 ◦ C 15 1: 15 1 No separation n.p. Lou et al. (2009)
min. process
Fresh Microwave: 50 W/ 50 ◦ C 1 1: 15 1 n.p.
Ultrasound: 40 kHz min.
Fresh Reflux Soxhlet 85 ◦ C 3h 1: 20 1 Freeze-drying 9.9 Lee, Lee, and Jo (2010)
70% ethanol 25 ◦ C 72 h 1 8.2
Dried Conventional 65 ◦ C 40 1:15 1 Centrifugation 12.3 Milani et al. (2011)
min.
Ultrasound probe: 21 40 C
◦
25 1:15 1 24.3
kHz min.
Dried Reflux Soxhlet 100 ◦ C 1h 1:20 3 Acetone 14.2 Olennikov and Tankhaev (2011)
Dried Microwave: 800 W 80 ◦ C 10 1:20 1 Centrifugation 42.2 Li et al. (2013)
min.
Dried Microwave: 500 W 100 ◦ C 10 1:20 1 Freeze-drying n.p. Li, Liu, Zhou, Zhao, and Li (2013)
min.
Dried Ultrasound: 35 kHz 80 C
◦
30 1:50 3 Ethanol 8.5 D’yakova, Samylina, Slivkin,
min. Gaponov, and Myndra (2015)
Dried Conventional 90 ◦ C 15 1:20 1 Ethanol n.p. Cao et al. (2018)
min.
*
n.p.: not published.
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T.M.A. Moro and M. T.P.S. Clerici Food Research International 141 (2021) 109889
compounds were more effective than the three standards, probably due between the cultivated burdock root (BC) and wild root, which grows
to the higher number of caffeine residues. freely in nature (BS). The authors used HPLC and Ultra Performance
Der Duh (1998) investigated the antioxidant activity of dried Liquid Chromatography (UPLC) to identify and quantify the phenolic
burdock root extracts at 25 ◦ C using water, methanol, ethanol, chloro compounds of the chlorogenic class. The total phenolics content was also
form, and hexane as solvents, and an extract in hot water. The water determined using chlorogenic acid standard (5-CQA) as equivalent. The
extracts, especially those obtained in hot water had a higher yield in cultivated burdock root presented 5-CQA (chlorogenic) and 1,5-DCQA
weight and more intense antioxidant capacity among all solvents used. (cinnarine) levels around 50% higher. A similar increase was observed
The authors suggested that burdock root infusion beverages, widely for the total phenolic content of the cultivated root, probably due to
consumed by the Chinese population, provide antioxidant properties differences in the genetic load, environment, growing conditions, and
and may be considered nutritionally healthy. root culture time.
Lin and Harnly (2008) identified 24 hydroxycinnamic acids in Although those studies followed a chronological sequence, with a
freeze-dried burdock root powder using High-Performance Liquid deepening of the investigation over the years (from 1995 to 2018) to
Chromatography (HPLC) coupled with a mass spectrometer. The ma identify the compounds present in the root, no studies have assessed the
jority was caffeoylquinic acids, of which four were monocafeoilquinic metabolism of these compounds during the plant growth and after
acids, six dicafeoilquinic acids, and two tricafeoilquinic acids. The au harvesting. In addition, whereas the root is not usually consumed in its
thors confirmed the chlorogenic acids as the phenolic compounds with raw form, deep studies are needed to identify the effect of cooking and
the highest nutritional value in the burdock roots. preservation processes on these compounds, which are more sensitive
Ferracane, Graziani, Gallo, Fogliano, and Ritieni (2010) identified when compared with carbohydrates, thus more susceptible to the pro
other classes of phenolic compounds in the burdock root, including cessing conditions.
flavonoids, which are the most abundant phenolics in nature, composed As with many plants used in folk medicine, burdock has also been
of two phenylpropanes, two aromatic rings bound by three carbon investigated not only for the presence of compounds with biological
molecules, and lignans, consisting of two phenylpropanoids linked by activity but also for its possible performance in biological trials, as
the β-carbon of their side chains, forming diphenolic compounds. For the presented below.
first time, flavonol quercetin in its free and glycosylated form, quercetin,
and lignan arctiinin have been described. Another flavonoid from the 4. Biological activities of the compounds from burdock roots
flavone class, luteolin, was identified using HPLC-MS, in addition to
chlorogenic, caffeic and dicafeoilquinic acids (called kinarin). Carbohydrates are the most abundant nutrients in the burdock roots,
In a recent study, Jiang et al. (2016) evaluated the antioxidant ca thus the possible health benefits of this fraction have been studied.
pacity of mono-, di and tri-CQA (one to three units of quinidine-linked Table 2 shows possible compounds that promote biological activities of
caffeoyl, respectively), isolated from burdock root alcoholic extract, burdock, as reported by several authors.
using the DPPH (2,2-diphenyl − 1-picrylhydrazyl), ABTS (2,2′ -azino-bis The studies showed positive results for various biological activities,
(3-ethylbenzothiazoline-6-sulphonic acid)), and FRAP (Ferric Reducing including prebiotic activity, hypoglycemic activity, hepatoprotective
Antioxidant Power) assays. An increase in the antioxidant capacity was effect, among others. However, there are still challenges to be overcome,
observed with the increase in the number of caffeoyl units, and the concerning the compounds that in fact had such action and the existence
greater the number of these units in the chlorogenic acid molecule, the of synergy between the antioxidant compounds and the prebiotic fibers.
greater its antioxidant capacity, which corroborates with the study by Therefore, further research is required, once no studies have assessed the
Maruta et al. (1995). isolated and purified compounds and their mechanisms of action.
So far, in vitro and in vivo studies of the prebiotic activity of burdock
3.2.2. Identification and quantification of compounds root have been carried out by Li, Kim, Jin, and Zhou (2008) (Table 2).
The first study on the quantification of lignans in the burdock root The authors performed an in vitro test to evaluate the growth of Bifido
was carried out by Liu et al. (2012), who used freeze-dried roots and peel bacterium adolescentis in MRS (Man-Ragosa-Sharp) medium containing
of six different genotypes of Chinese origin. The arctiinin concentration inulin from burdock at different concentrations (0, 0.5, 1, 2, 3, and 4%)
in the dried root and root peel ranged from 20 to 40 mg/100 g and 130 to for 24 h. After this period, a higher bacterial growth (P < 0.05) was
210 mg/100 g, respectively. observed in the tubes with concentrations between 1 and 4% when
Chen, Wu, and Chen (2004) studied the effect of peel removal and compared to tubes with glucose (0%) and 0.5% inulin. Concerning the
thermal processing on the antioxidant properties of burdock roots. For tests in vivo, 5% of the carbohydrates (pregelatinized maize starch, 61.4
that, raw, filtered juice was extracted from both the root with and g/100 g), corresponding to 3.2 g/100 g, was replaced by burdock inulin
without peel, which was packed and submitted to heat treatment (98 ◦ C) in the diet of adult female mice, and with no changes in weight or
for 10 min. All samples were freeze-dried and evaluated for their anti amount of animal feed ingested. Fecal analysis performed after 27 days
oxidant capacity and bioactive compounds, and quantification of of feeding showed a significant stimulus for the proliferation of the
chlorogenic and caffeic acids. The antioxidant capacity decreased with genera bifidobacteria and lactobacilli, both probiotics.
the peel removal, which was also observed in the quantification of acids Other studies investigated different therapeutic activities, once
by HPLC analyses, with a 40% decrease in chlorogenic acid content, burdock has been consumed in the form of medicinal tea. Although some
indicating that most of these compounds are located in the peel, except authors have reported the importance of fructooligosaccharides as a
for caffeic acid. According to the authors, the preservation of this part of bioactive compound, in-depth studies on prebiotics and probiotics have
the root is important for the maintenance of the content of chlorogenic shown many benefits rather than improvements in the functioning of the
acids in burdock roots. In addition, the heat treatment negatively digestive system (DS), such as improving the immune system in the face
affected the chlorogenic acid content, which was expected due to the of respiratory viral diseases (Antunes et al., 2019). Those authors stud
heat sensitivity of this compound. ied the mechanism of action of the acetate, as a product of metabolism of
Predes et al. (2011) used mass spectrometry with high-resolution prebiotic fibers in DS, showing their importance to stimulate the im
electrospray ionization (HRESI-MS) to determine the presence of quer mune system.
cetin and arctigenin in the burdock root hydroethanolic extract. The Inulin and its industrial products obtained from chicory roots (Pilon
phenolics concentration was estimated at 1.27, 2.18, 0.68, and 1.82 mg/ et al., 2006) have been studied for its ability to stimulate the growth of
100 g for arctigenin, caffeic acid, chlorogenic acid, and quercetin, different types of probiotic microorganisms, and their possible beneficial
respectively. effects on health of the host. Studies carried out with this prebiotics
Haghi, Hatami, and Mehran (2013) investigated possible differences reported an increase in calcium and magnesium absorption (Holloway
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T.M.A. Moro and M. T.P.S. Clerici Food Research International 141 (2021) 109889
Table 2
Positive biological activity of burdock root extracts (Arctium lappa L) in assays in vivo and in vitro.
Reference Extraction Study Animal type Administration Dose Duration of Biological Compounds with
method type (body weight)/ treatment activity possible health claims
cells culture
Kardošová Cold water, 24 h in vivo Adult cats both Orally 50 mg/kg 0, 0.5, 1, 2, 3 and 5 Antitussive Fructooligosaccharide
et al. sexes ha
(2003) (1500–2500 g)
Cavalli et al. Reflux, water in vivo Adult male Wistar Orally 500 mg/kg 21 days Hypoglycemic n.p.b
(2007) rats
(250–330 g)
Li et al. Cold water, 24 h in vitro Bifidobacterium in vitro 0.3 g/10 24 h (incubation) Prebiotic activity Fructooligosaccharide
(2008) adolescens ml
Li et al. Cold water, 24 h in vivo Adult female Orally 3.2 g/100 g 14 days Prebiotic activity Fructooligosaccharide
(2008) cumming mice of diet
(20 ± 1 g)
Dos Santos Chloroform in vivo Adult female Orally 30, 100, 7 days Gastroprotective Radical-scavenging and
et al. (room Wistar rats 300 and antioxidant activities
(2008) temperature, 24 (180–200 g) 600 mg/kg
h)
JianFeng Water (80 ◦ C, in vivo Adult male Orally 600 and 15 days Male sexual Flavonoids, saponins,
et al. 1.5 h) Sprague-Dawley 1200 mg/ behavior lignans, and alkaloids
(2012) rats (230–260 g)c kg
Kuo et al. Reflux (water in vivo Adult male Orally 500 and 28 days Body weight α-linolenic acid, methyl a-
(2012) and ethanol) 3 h Sprague-Dawley 1000 mg/ management linoleate, and methyl
rats (150–200 g) kg oleate
da Silva et al. Ethanol (96%, in vivo Adult female Orally 10 and 30 7 days Gastroprotective Chlorogenic acid series
(2013) 25 ◦ C, 4 h) Wistar rats mg/kg and other polar
(180–200 g) phytochemical
compounds
Liu et al. Water (60 ◦ C, 3 in vivo Adult ICR female Orally 100–400 63 days Antioxidant Fructooligosaccharide
(2014) h) mice mg/kg activity
(18–22 g)d
Tousch et al. Ethanol 70% in vivo Adult male Wistar Orally and 0.75 to 3 4 days Hypoglycemic Caffeoylquinic acids
(2014) (room rats Intraperoneal and 3 to 15
temperature for (280–320 g) mg/kg
48 h)
Predes et al. Reflux (ethanol in vivo Adult male Wistar Orally and 300 mg/kg 7 or 56 days Hepatoprotective Quercetin, arctigenin,
(2014) 70%, 6 h, 3x) rats Intraperitoneal chlorogenic acid, and
(380–460 g) caffeic acid
El-Kott and Water (boiled, in vivo Adult male Orally 300 mg/kg Single dose 12 h Hepatoprotective Radical-scavenging and
Bin- 60 min.) Sprague-Dawley before antioxidant activities
Meferij rats (200–250 g) acetaminophen
(2015) injection
Tian et al. Ethanol 55% in vitro Human in vitro 20, 40, and Exposure for 12 h Neuroprotective Radical-scavenging and
(2015) (room neuroblastoma 80 μg/mL antioxidant activities
temperature, 30 SH-SY5Y cells
min.
Wang et al. Water, in vivo Adult male quails Orally 100 to 70 days Hypolipidemic Radical-scavenging and
(2016) chloroform and (±100 g)e 3000 mg/ antioxidant activities
ethanol extracts kg
Yang et al. Ethanol 50% in vivo Adult male Orally 25, 50, and 1 h before allergy Antiallergenic Oleamide
(2016) Sprague-Dawley 100 mg/kg induction
rats (200–230 g)f
b
After cough stimulation. an.p.: not published. cFour months old. dSix to eight weeks old. eThree weeks old. fSix weeks old.
et al., 2007) due to the presence of SCFA (short-chain fatty acids), and The effect of burdock on diabetes control has been previously
control of total cholesterol, LDL-c (low density cholesterol) and tri mentioned in folk medicine. Teske and Trentini (1995) and Cavalli et al.
glycerides (Beserra et al., 2015) The studies on burdock carbohydrates (2007) studied the metabolic effect of the burdock root extract in the
described in Table 2 will be discussed in more detail, aiming to show the treatment of diabetes in adult diabetic rats. The animals that ingested
great potential of using burdock for health promotion. the burdock extract showed a 35% reduction in fasting glycemia when
Kardošová et al. (2003) observed a significant increase in the anti compared to the control treatment. In addition, the consumption of
tussive effects when compared with the control (negative), when the burdock extract helped to preserve lean mass, and weight maintenance
aqueous extract of burdock root (single dose: 50 mg/kg of weight) was observed in the animals fed with the extract.
administered by gavage in adult cats of both sexes. Tousch et al. (2014) tested glucose tolerance under oral and intra
The in vivo antioxidant capacity of the carbohydrates from burdock peritoneal administration of burdock root extract in healthy male rats,
roots was evaluated by Liu et al. (2014) in aged female mice (via with a significant reduction of glucose and insulinemia after 10 and 60
galactose). The animals receiving by gavage 400 mg/kg of purified min for the intraperitoneal trial, and 15, 30, and 120 min when
extract (phenolics free) from burdock roots had an increase in all en administered by the oral route. The authors suggested that the anti
zymes related to free radicals and a reduction of malondialdehyde, hyperglycemic effect of the extract (containing 86% chlorogenic acid)
indicating a significant antioxidant capacity of this extract. corroborated with the glycemia modulation effect of the phenolic
The biological activities that are related to other components rather compounds.
than inulin-type fructans are presented in Section 3 and the most Some authors have reported the effect of the consumption of burdock
important are discussed as follow. roots on lipid metabolism. Kuo et al. (2012) studied the effect of the
6
T.M.A. Moro and M. T.P.S. Clerici Food Research International 141 (2021) 109889
consumption of aqueous and ethanolic extracts on weight reduction of investigating the possible interferences of other compounds in human
male rats. In vitro tests revealed the inhibition of lipogenesis and stim and animal feeding should be studied, concerning the biological activity
ulation of catabolism as the main key mechanisms for the performance of the whole roots.
of burdock extracts for weight reduction. Subsequently, Wang et al.
(2016) administered a high lipid diet (14% pork fat, 1% cholesterol) and 5. Food and non-food applications
different burdock root extracts in male quail. Regardless of the extrac
tion method, all extracts presented anti-atherosclerosis, hypolipidemic The burdock root is part of the eating habits of Asian populations,
activity, or attenuation of the oxidative stress of the arteries. The inhi who consume fresh roots in tea, salads, and soups after domestic pre-
bition of lipogenesis and hypolipidemia observed in both studies indi processing. The dried root is also found in the market for making tea
cate that other mechanisms rather than the root fibers may contribute to (Der Duh, 1998). In recent years, studies on burdock roots as an ingre
the maintenance of weight and consumers health. dient of food products have been performed due to the presence of
The gastroprotective activity of burdock root extracts was investi bioactive compounds and biological activity, with two studies on the use
gated by Dos Santos et al. (2008) and da Silva et al. (2013) using of flour in pan bread and cookies.
chloroform extract (100 mg/kg) and ethanolic extract (3, 10, and 30 Tae et al. (2015) investigated burdock root flour to replace wheat
mg/kg), respectively. In the both articles, an anti-secretory effect was flour in pan bread, in the proportions of 0, 5, 10, and 15%, and observed
observed with the reduction of gastric acid secretion and the lesion of a reduction of dough density with the increase in burdock flour. Bread
the stomach, both related to the antioxidant capacity of the extracts. presented lower luminosity and higher green-yellow color of the crumb
Although the authors of the first study used extraction methods and with the increase in burdock flour concentration. In addition, there was
dosages different from those reported by da Silva et al. (2013), similar an increase in hardness and antioxidant activity of bread made with 5,
results were observed between both studies. 10, and 15% of burdock flour when compared to the control. The sen
The hepatoprotective effect of burdock roots was reported in two sory evaluation showed no significant difference between the samples,
studies, both with similar dosage (300 mg/kg of weight) using different with all scores above 4 (indifferent), indicating acceptance of this novel
extracts. Predes et al. (2014) studied an ethanolic extract, and reported a product by the assessors.
complete reestablishment of the biochemical functions generated by the To reduce postharvest losses, which is a problem characteristic of
administration of cadmium (hepatotoxic), although a morphological countries with a tropical climate, and to increase the use of burdock, our
change in the tissue was also observed. El-Kott and Bin-Meferij (2015) research group produced burdock flour to be used in cookies (Moro
induced liver damage with paracetamol (800 mg/kg) in rats previously et al., 2018). Wheat flour was replaced by burdock flour in the pro
administered burdock extract 12 h before the trials. After 30 days, duction of cookies, in the concentrations of 0, 5, and 10%. The authors
normalization of hepatic function in rats was observed, except for the found a significant increase in the concentration of oligosaccharides
histopathological evaluation, which evidenced an incomplete reduction with the increase in burdock flour. In addition, the cookies made with
of necrosis. Both results, even with different extracts and duration of the 10% burdock flour had higher prebiotic activity in vitro when compared
treatment, indicated that the burdock roots contributed with the re to both the control (0%) and the cookies made with 5% burdock flour.
covery of hepatic function when compared to the control, probably due All cookies were well accepted by the assessors corresponding to the
to the antioxidant capacity of the extracts. majority of Latin American individuals, with scores above the neutrality,
Tian et al. (2015) investigated the possible neuroprotective activity indicating that cookies can be a good vehicle for burdock roots. Burdock
of burdock root extract in human neuroblastoma injured with hydrogen root has a slightly earthy flavor, and does not belong to the eating habits
peroxide. An increase in cell viability was observed with the extract of Latin American people, despite being quite pleasant for Asians who
consumption, and an improvement of all parameters evaluated was have a habit of consuming the roots.
observed for the concentrations of 40 and 80 μg/mL. The antioxidant The non-food application of burdock root was studied by Cao, Yang,
capacity and the antiapoptotic activity of the extract were associated and Song (2018), who used a root extract (obtained by conventional
with the neuroprotective effects. method at 90 ◦ C for 15 min) in chitosan-sorbitol-edible films. Burdock
The aphrodisiac activity of burdock roots on the sexual behavior of root extract increased the opacity and the yellow color of the films and
male rats was suggested by JianFeng et al. (2012) with improvements in reduced the water permeability. In relation to the mechanical proper
the testosterone level, which was significantly higher for the groups that ties, there was an increase in deformation at rupture. The authors re
ingested 600 and 1200 mg/kg of extract. Although the compounds that ported compatibility of the extract with the other ingredients, due to the
affected the behavior of the rats have not been elucidated, this effect homogeneity of the films, which points to a new possibility of use of the
may have been due to the combined effect of the bioactive compounds. burdock roots.
Yang et al. (2016) identified oleamide as the bioactive compound
responsible for the antiallergic activity of burdock roots, and reported an 6. Future perspectives
isolated effect on attenuating the histamine secretion, the production of
tumor necrosis factor (TNF) -α and interleukins in a study in vivo. The This study showed various possible applications of burdock root,
authors concluded that the identification of this compound can thus an increase in its agronomic importance in the world root pro
contribute to further research to reduce the allergic response under duction is expected in the coming years, which will lead to further
burdock root administration. studies on the viability of cultivars, yield per hectare, and the dissemi
This section presented few studies to elucidate the pharmacological nation of the annual harvest data from producing countries.
importance of this root, which has a well-established therapeutic Unlike other roots of the same family that are investigated for their
application in popular medicine. Possible therapeutic effects of burdock content of inulin and oligofructoses (yacon, Jerusalem artichoke, and
roots have also been reported by Fierascu et al. (2018), Gao et al. (2020), agave, for example), burdock has potential as a source of prebiotic fibers
Jiang et al. (2019), and Maghsoumi-Norouzabad et al. (2016). and antioxidant compounds, and can be used to replace starch (digest
All authors cited in this review used different burdock root extracts ible carbohydrates) in various food products. With the increased de
to study the compounds with specific or systemic biological activities mand for the use of burdock roots, further studies in vivo and in vitro
with health benefits. Those studies evidenced the effect of burdock root about the interaction between its prebiotic carbohydrates and gut bac
extracts when ingested by the animals, showing a functional food appeal teria and the production of short chain fatty acids should be encouraged.
in western and eastern diets, but they did not address the use of whole The probiotic effects of the fermentation of burdock carbohydrates when
roots for dietary and medicinal application, which is the most consumed compared to other probiotic ingredients should also be studied.
form. The fresh or dried roots can be used as an alternative to As previously reported, the burdock root has high enzymatic activity
7
T.M.A. Moro and M. T.P.S. Clerici Food Research International 141 (2021) 109889
and moisture content, thus the preservation of fresh roots depends on Ferracane, R., Graziani, G., Gallo, M., Fogliano, V., & Ritieni, A. (2010). Metabolic profile
of the bioactive compounds of burdock (Arctium lappa) seeds, roots and leaves.
cooling and drying processes to preserve the roots in the form of flour,
Journal of Pharmaceutical and Biomedical Analysis, 51(2), 399–404. https://doi.org/
allowing expanding the commerce in long-distance markets. Therefore, 10.1016/j.jpba.2009.03.018.
the use of preservation methods can improve the market of burdock Fierascu, R. C., Georgiev, M. I., Fierascu, I., Ungureanu, C., Avramescu, S. M., Ortan, A.,
roots, besides contributing to the creation of healthier eating habits. … Anuta, V. (2018). Mitodepressive, antioxidant, antifungal and anti-inflammatory
effects of wild-growing Romanian native Arctium lappa L. (Asteraceae) and Veronica
persica Poiret (Plantaginaceae). Food and Chemical Toxicology, 111, 44–52. https://
Declaration of Competing Interest doi.org/10.1016/j.fct.2017.11.008.
Flamm, G., Glinsmann, W., Kritchevsky, D., Prosky, L., & Roberfroid, M. (2001). Inulin
and oligofructose as dietary fiber: A review of the evidence. Critical Reviews in Food
The authors declare that they have no known competing financial Science and Nutrition, 41, 353–362. https://doi.org/10.1080/20014091091841.
interests or personal relationships that could have appeared to influence Fu, Y. L. (2009). Isolation, purification, and structural elucidation of a fructan from
the work reported in this paper. Arctium lappa L. In Journal of Medicinal Plants Research, Vol. 3(3), 171-173,
Retrieved from: https://www.academicjournals.org/JMPR.
Gao, H., Jiang, X. W., Yang, Y., Liu, W. W., Xu, Z. H., & Zhao, Q. C. (2020). Isolation,
Acknowledgment structure elucidation and neuroprotective effects of caffeoylquinic acid derivatives
from the roots of Arctium lappa L. Phytochemistry, 177, Article 112432. https://doi.
org/10.1016/j.phytochem.2020.112432.
The authors are grateful to the Coordenação de Aperfeiçoamento de Gibson, G. R., Hutkins, R., Sanders, M. E., Prescott, S. L., Reimer, R. A., Salminen, S. J., …
Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001, and Reid, G. (2017). Expert consensus document: The International Scientific Association
doctorate scholarship for Thaisa Moro, and FAEPEX-Unicamp (519292- for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and
scope of prebiotics. Nature Reviews Gastroenterology & Hepatology, 14(8), 491–502.
2425/16) for the financial support in part of this study. https://doi.org/10.1038/nrgastro.2017.75.
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