Next Article in Journal
Complexes of Ruthenium(II) as Promising Dual-Active Agents against Cancer and Viral Infections
Previous Article in Journal
Betanin from Beetroot (Beta vulgaris L.) Regulates Lipid Metabolism and Promotes Fat Browning in 3T3-L1 Adipocytes
Previous Article in Special Issue
In Vitro Synergistic Inhibitory Effects of Plant Extract Combinations on Bacterial Growth of Methicillin-Resistant Staphylococcus aureus
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Pharmaceuticals
Volume 16
Issue 12
10.3390/ph16121728
pharmaceuticals-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Chenopodium quinoa Willd. and Amaranthus hybridus L.: Ancestral Andean Food Security and Modern Anticancer and Antimicrobial Activity

by
Juan Carlos Romero-Benavides
1,*,
Evelyn Guaraca-Pino
1,2,
Rodrigo Duarte-Casar
3,
Marlene Rojas-Le-Fort
3 and
Natalia Bailon-Moscoso
4
1
Departamento de Química, Facultad de Ciencias Exactas y Naturales, Universidad Técnica Particular de Loja, Loja 110108, Ecuador
2
Maestría en Alimentos, Facultad de Ciencias Exactas y Naturales, Universidad Técnica Particular de Loja, Loja 110108, Ecuador
3
Tecnología Superior en Gestión Culinaria, Pontificia Universidad Católica del Ecuador—Sede Manabí, Portoviejo 130103, Ecuador
4
Facultad de Ciencias de la Salud, Universidad Técnica Particular de Loja, Loja 110108, Ecuador
*
Author to whom correspondence should be addressed.
Pharmaceuticals 2023, 16(12), 1728; https://doi.org/10.3390/ph16121728
Submission received: 10 November 2023 / Revised: 1 December 2023 / Accepted: 8 December 2023 / Published: 15 December 2023
(This article belongs to the Special Issue Plant Products as Antimicrobial and Anticancer Agents)
Browse Figures
Versions Notes

Abstract

:
The species Chenopodium quinoa Willd. and Amaranthus hybridus L. are Andean staples, part of the traditional diet and gastronomy of the people of the highlands of Colombia, Ecuador, Peru, Bolivia, northern Argentina and Chile, with several ethnopharmacological uses, among them anticancer applications. This review aims to present updated information on the nutritional composition, phytochemistry, and antimicrobial and anticancer activity of Quinoa and Amaranth. Both species contribute to food security due to their essential amino acid contents, which are higher than those of most staples. It is highlighted that the biological activity, especially the antimicrobial activity in C. quinoa, and the anticancer activity in both species is related to the presence of phytochemicals present mostly in leaves and seeds. The biological activity of both species is consistent with their phytochemical composition, with phenolic acids, flavonoids, carotenoids, alkaloids, terpenoids, saponins and peptides being the main compound families of interest. Extracts of different plant organs of both species and peptide fractions have shown in vitro and, to a lesser degree, in vivo activity against a variety of bacteria and cancer cell lines. These findings confirm the antimicrobial and anticancer activity of both species, C. quinoa having more reported activity than A. hybridus through different compounds and mechanisms.

Graphical Abstract

1. Introduction

Our perception of staples is centered around Middle Eastern cereals, often leaving aside other staples domesticated and grown elsewhere, often by cultures and civilizations later overrun by invaders, such as ancestral grains, many of which became neglected or underutilized crops.
The Amaranthaceae family provides several crops of interest: the economically relevant spinach (Spinacia oleracea L.) and sugar beet (Beta vulgaris L.) and the ancestral South American pseudocereals quinoa (Chenopodium quinoa Willd.) and amaranth (Amaranthus hybridus L.). Both species are experiencing renewed interest from alimentary and biological activity perspectives [1]. Interest in Quinoa as a hardy crop began in the first half of the twentieth century, and its popularity exploded in the 1980s [2]. Quinoa became an upper-class staple in the USA, the United Kingdom and other countries in the 2010s, which drove prices up [3]; amaranth expanded as a leaf vegetable and saw a similar price increase [4,5]. Both quinoa and amaranth are considered ‘superfoods’—“foods beyond the diet, but before the drugs” [6]. This status has increased commercial and scientific interest in both species as foods and nutraceuticals.
Antibiotic-resistant bacteria (ARB) are bacteria that are not controlled or killed by antibiotics. Of concern are multidrug-resistant (MDR) bacteria, which are a growing public health problem that needs to be solved [7]. Antimicrobial-resistant infections are predicted to cause around 10 million deaths per year and a total GDP loss of the order of USD 100 trillion by 2050 if effective actions are not implemented, particularly in developing countries where the risk is higher [8,9]. “New agents displaying innovative chemistry and modes of action are desperately needed worldwide to tackle the public health menace posed by antimicrobial resistance” [10]. There is a constant search for new drugs that relies on traditionally used plants as a starting point [11].
Cancer is a group of diseases characterized by unchecked cell growth [12]. It is the second leading cause of death in high-income countries, behind cardiovascular disease [13]. In 2020, there were 19.3 million new cancer cases and 10 million deaths due to this disease [14]. In spite of these numbers, during the last decade, an encouraging general decrease in death rates due to cancer was seen, except for liver cancer in both sexes and lung cancer in women, for which death rates have increased [15]. This general reduction can be attributed, at least in part, to the development and approval of new treatments against the disease [16]. An estimated 25% of the treatments developed in the last decade are derived from natural products, mostly of plant origin, with increasing numbers of products isolated from fungi, bacteria and other kingdoms [17]. The search for active secondary metabolites—and other products, such as proteins and peptides—is fundamental in making progress against the disease.
Infectious diseases are a risk factor for cancer: Hepatitis B and C, Epstein–Barr and human papilloma viruses, Helicobacter pylori, and Streptococcus bovii are examples. Also, molecular mechanisms of cancer and infection spread are alike and are countered as foreign invaders by the immune system. Thus, antimicrobial and anticancer activities of species, extracts and compounds may be linked, and this is why both activities are reviewed together [18,19].
Quinoa and amaranth are related food crops with interesting nutritional profiles and similar modes of consumption; both are neglected crops due to the arrival of the Spaniards in the late fifteenth century and hold great potential from alimentary and medicinal points of view, appearing together in more than 450 publications according to a Dimensions search [20]. Given this, they are reviewed together.
There is renewed interest in validating the ethnopharmacological uses of ancestral plant species, and Quinoa and Amaranth have shown promise in several medical uses—cancer prevention and treatment as well as antimicrobial activity featuring prominently. Although there are several excellent reviews on these species, we found a lack of specific anticancer and antimicrobial activity reviews. The aim of this work is to compile and summarize the research about the anticancer and antimicrobial activity of Quinoa and Amaranth to identify the most active and promising lines of work and envision future research directions (Figure 1).

2. Method

A systematic literature review was performed following the SPAR-4-SLR (Scientific Procedures and Rationales for Systematic Literature Reviews) protocol [21]. The procedure is outlined in Table 1.
Data were obtained from the Dimensions web application that queries the Crossref database, which is more comprehensive than Scopus and Web of Science [22]. The search string was (Quinoa OR Amaranth) AND (antimicrobial OR cancer) in title and abstract, without time limitations and including only articles and book chapters. The first dataset consisted of 221 documents from 166 sources and a total of 959 authors. The dataset was organized by Dimensions rank, with fields of research (ANZSRC 2020) as the secondary key [23]. The document exclusion criteria are listed in Table 2. All articles not excluded were included.

3. Background

The genus Chenopodium has worldwide distribution and 130 accepted species [24]. Chenopodium quinoa was domesticated about 7000 years ago in the area surrounding Lake Titicaca, an area currently shared by Peru and Bolivia in South America, whence it spread to diverse landscapes which correspond to modern-day Ecuador, Perú, Bolivia, Argentina and Chile [2,25]. At least two other independent domestication events are considered: Chile, 3000 BC, and Bolivia, 750 BC [26].
The cosmopolitan genus Amaranthus, with worldwide distribution, has 95 accepted species. The earliest domestication findings of Amaranthus hybridus date from 7000–8000 years ago in what is now Argentina in South America [24]. The species is native to Argentina, Belize, Bolivia, Brazil, Colombia, Costa Rica, Ecuador, El Salvador, Guatemala, Honduras, Mexico, Nicaragua, Panamá, Paraguay, Peru, Uruguay and Venezuela [27,28]. The distribution of C. quinoa and A. hybridus is shown in Figure 2.
C. quinoa is an annual, dicotyledonous plant belonging to the Amaranthaceae family. Its height varies from 30 cm to 2.20 m, and it has a taproot with a size range from 0.8 to 1.5 m. The stem that connects to the root is cylindrical, while in the area where it joins the leaves and branches, it becomes angular. Its color varies with maturity. During the flowering period, it appears green, whereas in its mature state, it has a cream or pinkish color. The leaves have two structures: the petiole and the blade. The petiole originates directly from the stem. The blade is larger in the foliage than in the inflorescence and is triangular or lanceolate in shape. The fruit is a spheroidal, lenticular or conical achene, measuring 1.5 to 3 mm. It consists of a pericarp and seed. The pericarp is attached to the seed and contains saponins, which impart a bitter taste unless rinsed, although it has been reported that monomeric saponins present an umami flavor profile and that the bitterness could correspond to phenolic compounds [29]. The seeds are composed of the perisperm, embryo and endosperm. The embryo contains two cotyledons and the radicle, both contributing up to 30% of the seed’s weight. The perisperm is the storage tissue and is primarily made up of starch granules [30]. C. quinoa is of particular interest due to its high stress resistance, which may provide food security in the face of advancing desertification [31].
A. hybridus is an annual, dicotyledonous plant also in the Amaranthaceae family. Its height can reach up to 65 cm. The root is a taproot with secondary and tertiary roots that can grow up to 40 cm in length, which helps it tolerate water scarcity. The stem is cylindrical, longitudinally grooved and glabrous and can be green, purple or reddish in color. The leaves are oval-shaped, simple, alternate or opposite, with wavy edges, glabrous, and green during the growth period, turning violet or purple with prominent veins in maturity. The inflorescences are terminal or axillary, forming a panicle, and have an intense purple color. The flowers are unisexual and pistillate with five unequal tepals. The fruit corresponds to a pyxidium, which releases the seeds when mature [32].
Both species have been used since pre-agricultural times, and have long been cultivated following ancestral, sustainable methods that enable production in conditions of high altitude, drought, salinity and frost and which hold valuable lessons for the current climate emergency [33,34,35].

4. Nutritional Properties and Food Uses

Quinoa and amaranth are staples, neglected for centuries after the Spanish conquest, that are currently experiencing a revival [4,36,37]. The protein content of both species is variable but higher than that of cereals (12–19%) and lower than that of legumes and provides all nine essential amino acids in high-quality protein [38,39]. The fat content of both species is higher than that of cereals and abundant in essential unsaturated fatty acids. A comparison of example proximal compositions of quinoa and amaranth seeds is shown in Table 3.
Quinoa protein is high in essential amino acids, with notably high levels of lysine, methionine, histidine, isoleucine and cysteine, which are important in human health [40]. Amaranth seed protein is of high quality, with all nine essential amino acids, and is particularly high in lysine and tryptophan [41]. Amaranth leaf protein is also high-quality, with 36% of its weight in essential amino acids [42].
The seed oils of both species are rich in linoleic and linolenic (18:2 and 8:3) acids, with a ω-6-to-ω-3 proportion close to the recommendation for a healthy diet [38,43]. In addition, both species contain terpenoids of interest: squalene, isoprenoids and phytosterols [44].
The seeds and leaves of both species are vitamin and mineral sources: C. quinoa provides vitamins A, B1, B2, B3, B5, B6 B9, B12, C and E [45], while A. hybridus is a source of vitamins A, B1, B2, B3, B6, C and E [46]. C. quinoa is a source of calcium, phosphorus, magnesium, potassium, sodium, copper, zinc and iron, while A. hybridus provides calcium, phosphorus, magnesium, potassium, sodium, copper, iron, manganese and zinc [47]. In general, amaranth has a higher mineral content than quinoa [4].
In 1996, the FAO declared quinoa a promising crop to address human nutrition problems due to its nutritional and beneficial properties, and 2013 was declared ‘The International Year of Quinoa’ [48]. In the Andean highlands, quinoa is used to prepare soups, refreshing beverages and salads, which are consumed as part of breakfast, lunch and dinner. It is also often combined with legumes to improve the diet quality of preschool and schoolchildren populations [49].
Seeds are the main plant organ used as food for both quinoa and amaranth. Also, tender stems and leaves are used as greens in salads, or are blanched, steamed, boiled or fried. Inflorescences are also edible: the inflorescences of quinoa are used as seasoning and those of amaranth as medicinal and coloring agents in the popular traditional Ecuadorian drinks horchata and colada morada [50,51,52].
Both quinoa and amaranth seeds are highly nutritious, are naturally gluten-free and have a low glycemic index (GI). All these properties make them desirable in modern dietary trends [53,54], and recipe books combining traditional and modern recipes have been published [55].
Modern uses of both species are varied. The main domestic uses for quinoa are stews, desserts and drinks, and for Amaranth are salads and stews and, in African countries, sauces [56,57,58]. There are currently several processed food products made from, or supplemented with, flour and protein concentrates of both species: pasta, bread, breakfast cereals, sausages, snacks, biscuits, weaning foods, plant-based milks and yogurt, often bearing functional and ethical claims [59,60,61,62]. Quinoa and, to a lesser extent, Amaranth have been included in the haute cuisine offerings of Andean countries and Mexico since the second decade of the 21st century and are offered in Michelin-starred restaurants [63,64,65]. The species are also being used both as substrates and active extracts in edible films [66,67]. Also, the consumption of sprouts is encouraged for the enhanced nutrient bioavailability and antinutrient reduction [68]. Both species are also used in animal feed supplementation in cattle and to improve egg quality in laying hens [69,70].
Among the functional and nutraceutical uses of both species, probiotic-rich drinks from red quinoa have shown potential for restoring the gut microbiota, while the modification of quinoa proteins improves their functional properties and digestibility for the development of improved plant-based foods, and their antioxidant and other activities have promoted the development of several health food products [41,71,72,73].

5. Medicinal Uses

Besides their food uses, quinoa and amaranth have been traditionally appreciated as medicinal species by the Andean plateau people [74]. Quinoa seed, stems, fruits and leaves are traditionally used for diverse medicinal purposes, as shown in Table 4.
Amaranth is a popular medicinal plant frequently found in Andean markets [76]. The whole plant is used as medicine, with specific uses for leaves and inflorescences [77]. There is evidence that A. hybridus has a beneficial effect on the gut microbiota that underlies its ethnomedical uses concerning digestive system conditions [78]. It is also worth mentioning that A. hybridus and other Amaranthus species can be poisonous to cattle, exhibiting nephrotoxicity [79]. Traditional medicinal uses for A. hybridus are shown in Table 5.
Among the several uses of both species, anti-infective, antiabscess and other uses related to antimicrobial activity, as well as anticancer and chemopreventive uses, are of interest to this work.

6. Phytochemical Composition

The composition of C. quinoa and A. hybridus is diverse. Table 6 shows the main compound families found in both species [78,83].
Twenty-nine phenolic acid derivatives have been identified in Quinoa: sixteen benzoic acid derivatives and thirteen cinnamic acid derivatives [84]. Kongdang et al. reported gallic, ellagic, chlorogenic, and caffeic acids and derivatives in A. hybridus [78].
Thirty-five flavonoid compounds have been identified in Quinoa: four flavones, twenty-one flavonols, three flavanones, three flavanols and five estrogenic isoflavonoids [85]. Six flavonols have been isolated from Amaranth, mostly from methanolic leaf extract [86,87].
Fifteen monoterpenoids have been identified in C. quinoa essential oils, as well as the sesquiterpene caryophyllene. Bitter triterpenoid saponins and their aglycones are the reason why quinoa seeds must be rinsed before preparation. Ten hederagenins; four spergulagenic acids; five serjanic acids; ten phytolaccagenic acids; two gypsogenins; two 3β, 23, 30 trihydroxy oleano 12-en-28-oic acid analogues; and eleven oleanoic acids, glycated and aglycones, have been isolated, which exhibit antifungal, anti-inflammatory and cytotoxic properties [88,89,90]. Tetra- and pentacyclic terpenoids, and also meroterpenoids, have been identified in C. quinoa [91]. The carotenoid compounds lutein and β-carotene were identified in A. hybridus leaves [92]. Ten C-27, fourteen C-28 and seven C-29 steroids with antiobesity, antiangiogenic, collagenase inhibition, antioxidant, antidiabetic and anti-inflammatory activity have been identified in C. quinoa [91].
The biologically active, nitrogen-containing betalain pigments amaranthine and isoamaranthine, amongst others, have been identified in A. hybridus and other Amaranthus species [93]. C. quinoa varieties exhibit distinctive coloring, caused in part by betaxanthins and betacyanins, such as amaranthin, betanin, dopaxanthin, miraxanthin V (4) and indicaxanthin [94].
There is much interest concerning bioactive proteins and peptides from both species. Lunasin is a 43-amino acid-residue peptide present in quinoa with various health-promoting properties, including antioxidant, anti-inflammatory, hypocholesterolemic and anticancer activities [95]. Lunasin-like peptides are present in amaranth [96]. Detailed lists of phytochemicals from C. quinoa and A. hybridus are listed in Tables S1 and S2.

7. Biological Activity

7.1. Overview

According to the literature review, C. quinoa and A. hybridus present both antibacterial and anticancer activity, with more reported results for C. quinoa than for A. hybridus. The research on the main compound families concerning their antibacterial and anticancer activity in both species is shown in Figure 3.
These results show that research on quinoa phytochemicals is more abundant than that on A. hybridus phytochemicals. The bioactivity of A. hybridus extracts has been shown, but there has been little research progression from extracts to phytochemicals. The most-studied compound classes are phenolics (39%), peptides (27%), saponins (24%), polysaccharides (7%) and terpenoids (2%). Phenolic compounds, saponins and peptides are the most-studied antimicrobials, while phenolics, peptides and saponins are the most-studied compounds with respect to their anticancer activity.

7.2. Antimicrobial Activity

The antimicrobial activity of C. quinoa is due to several compound families, mainly phenolics. Compounds present in extracts of quinoa seeds, leaves, roots and inflorescences exhibit antimicrobial activity [97,98]. Examples of such activity are shown in Table 7 and Figure 4.
Even though Amaranth pigments and other phytochemicals possess antimicrobial activity, various solvent extracts of Amaranth leaves and stems are reported to exhibit weak or no antibacterial activity on the strains tested [107,108,109,110,111]. A mouthwash containing ethyl acetate extract of A. hybridus leaves has been reported to be effective against Streptococcus mutans [112]. Other species from the genus do exhibit antibacterial and antifungal activity [113,114].

7.3. Anticancer Activity

Phenolic compounds, unsaponifiable lipids, terpenoids, peptides and polysaccharides are reported as possessing anticancer activity in both Quinoa and Amaranth [95,115,116]. Antioxidant compounds and activity are associated with cancer prevention but do not imply chemopreventive or anticancer activity and can even interfere with chemotherapeutics [117].

7.3.1. Anticancer Activity of C. quinoa

Extracts, powders and oils from quinoa seed, leaves and bran have been reported as possessing anticancer activity. Quinoa leaves have been reported as chemopreventive supplements due to their antioxidant potential and high bioavailability of active compounds [118]. Quinoa bran has been reported as a source of bioactive compounds with antioxidant, antidiabetic, anti-inflammation, antibacterial and anticancer properties [116,119].
Shen et al. evaluated the anticancer activity of the oil from the seeds of the white (WSO), red (RSO) and black (BSO) varieties in HCT116 cells (human colon carcinoma) [120]. The application of BSO was more efficient than WSO and RSO, their IC50 values being 281.9, 381.3 and 647.4 µg/mL, respectively. Based on these results, the inhibitory effects of BSO at concentrations of 0, 62, 5, 125 and 250 µg/mL were tested for 36 h, and apoptotic states at concentrations of 62.5–250 µg/mL which indicated significant inhibition were observed. In addition, a change in morphology was observed, since the cells in culture appeared fusiform and retractile and the untreated cells presented a homogeneous, polygonal shape, confirming that BSO can induce significant apoptosis in HTC 116 cells. In quinoa inflorescence extracts, several compounds with anticancer activity have been found, among them 4-hydroxy-benzaldehyde, 1H-Indole-3-carboxaldehyde, methyl hexadecanoate and ((6E,10E,14E,18E)-2,6,10,15,19,23-hexamethyltetracosa-1,6,10,14,18,22-hexaen-3-ol) [97].
Phenolics in quinoa partially account for both antimicrobial and cytotoxic activities. Stikić et al. found that the Puno cultivar has a higher phenolic content and cytotoxic activity than the Titicaca cultivar against HCT 116 human colorectal cancer cells [121]. Of note is the difference in ferulic acid content between the cultivars. Quinoa seed powder was found to possess an IC50 of 14.6 μg/mL against HEPG2 liver carcinoma cells, attributable to their phytic acid, polyunsaturated fatty acid and phenolic contents [122].
Quinoa proteins are reported as having anticancer activity. The cytotoxicity of quinoin—a Type 1 Ribosome-Inactivating Protein (RIP)—extracted from quinoa seeds was investigated in two primary glioblastoma (GBM) cell lines: NULU and ZAR, and in continuous human glioblastoma cells (U87Mg) [123]. The IC50 values of quinoin were determined at 24, 48 and 72 h at concentrations 0.001, 0.1, 1.0, 2.5 and 5.0 µM using the tetrazolium dye (MTT) assay. Additionally, the GBM, NULU and ZAR cell lines were treated with 1 µM Temozolomide plus 2.5 nM quinoin for 24, 48 and 72 h. The study showed that quinoin strongly reduced the growth of glioblastoma cells and that the IC50 of primary and continuous GBM cells does not depend on the time in contact with quinoin. Furthermore, primary cells treated with quinoin in combination with temozolomide (TMZ—a chemotherapeutic used in the treatment of glioblastoma) were more sensitive to the treatment; therefore, the authors highlight that quinoin could represent a novel tool for the therapy of glioblastoma and a possible adjuvant for the treatment of the disease in combination with TMZ. Lunasin is a protein present in quinoa that also has reported anticancer activity [95].
The anticancer activity of quinoa polysaccharide (CQP) composed of glucose and galacturonic acid units was evaluated by Hu et al. on two types of cancer (SMMC 7721 liver cancer and MCF 10 A breast cancer) using the in vitro MTT assay [124]. For the study, they used normal human liver cells (L02) and normal breast epithelial cells (MCF10A) as controls. Human liver cancer cells (SMMC 7721) and human breast cancer cells (MCF-7) were seeded on plates treated with CQP concentrations of 12.5 and 200 µg/mL and cultured at 37 °C for 24 and 48 h. MTT was added in an amount of 5 mg/mL to each well. After the incubation time, the microplates were measured in a reader at an absorbance of 570 nm. The cell viability rate was estimated in relation to the absorbance given by each well of the samples treated with CQP and the absorbance of the untreated wells. The IC50 values of CQP in SMMC 7721 cells after 24 h and 48 h were 121.4 µg/mL and 53.4 µg/mL. The IC50 values of CQP in MCF-7 cells after 24 h and 48 h were 83.48 µg/mL and 64.67 µg/mL, with no effect on normal cells. Therefore, the results are indicative that the polysaccharides of Ch. quinoa present anticancer activity. On the other hand, quinoa saponin-rich extracts and their hydrolysates were found to have no activity against human colorectal cancer cells [125].
Aqueous leachates from germinating quinoa seeds contain 20-Hydroxyecdysone, a hormonal steroid that has exhibited in vitro anticancer activity against human non-small cell lung cancer cells [126,127].

7.3.2. Anticancer Activity of A. hybridus

Amaranthus hybridus, along with other species of the genus, shows chemoprotective activity, which is supported by its phytochemical composition. Phenolics, peptides, carotenoids and other compounds have shown activity in this regard [128,129].
Adewale and Olorunju showed a hepatoprotective effect against arsenite-induced cancer in rats [130]. The effect is also evident against aflatoxin and fumonisin damage in rat hepatic cells and is attributed to antigenotoxic phytochemicals and minerals: “phenolics, carotenoids, folic-, linolenic-, linoleic and palmitic acids, as well as calcium, magnesium, iron, zinc, and selenium” [131]. This is in line with other chemoprotective effects attributable to antioxidant properties, for example, against imidacloprid [132]. Due to the selenium content of A. hybridus leaves, an aqueous extract was tested for cytotoxicity against the MDA-MB-231 cancer cell line, but no activity was detected [133].
In a study carried out by Al-Mamun et al. (2016), the anticancer activity of an aqueous extract of the stem of Amaranthus lividus (AL) and an aqueous extract of the seeds of Amaranthus hybridus (AH) was tested on Ehrlich ascites carcinoma (EAC) cells. The extracts were tested on 42 mature Swiss albino mice, to which the extracts were applied for 6 days. After the administration of the extracts in doses of 25, 50 and 100 µg/mL/d for 6 days, a count of EAC cells was performed with a hemocytometer using trypan blue, whereby it was demonstrated that the AH extract exhibited growth inhibitory activity relatively higher than that of the AL stem extract used in the same concentrations. Therefore, the study shows that Amaranthus exhibits powerful anticancer properties [108]. Antioxidant polysaccharides from A. hybridus have been isolated and characterized and shown to possess significant in vitro antioxidant activity associated with cancer prevention [134]. In vitro and in vivo studies on the anticancer activity of both species are shown in Table 8, and notable compounds are shown in Figure 5.
Limitations of the present study are the lack of information about quinoa and amaranth consumption and cancer and other disease rates where the species are traditionally used and the lack of clinical trials to further establish the activity of the studied extracts and compounds.

8. Conclusions

Chenopodium quinoa and Amaranthus hybridus are ancestral pseudocereals that have experienced a revival in the last four decades. Besides their hardiness, which is relevant to attaining food security in the climate crisis we are collectively facing, and their high nutritional content, they possess significant biological activity.
The antimicrobial activity of quinoa is stronger than that of amaranth, which exhibits weak antimicrobial activity as tested. Quinoa exhibits ample antimicrobial properties, including action against antibiotic-resistant strains, due to diverse phytochemical compound classes, mainly phenolics.
Active anticancer compounds are found in both species. Of particular interest are proteins and peptides with anticancer activity, as well as phenolics, unsaponifiable terpenoids and pigments.
The substances that garner the most interest in both species, both for their antibacterial and anticancer activity, are phenolics, peptides and saponins, and there is promising work being carried out on bioactive polysaccharides.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/ph16121728/s1, Table S1: Phytochemicals from Chenopodium quinoa Willd.; Table S2: Phytochemicals from Amaranthus hybridus L.

Author Contributions

E.G.-P.: research, draft writing. N.B.-M.: conceptualization, manuscript review. R.D.-C.: research, translation, manuscript writing, figures. M.R.-L.-F.: manuscript writing and review. J.C.R.-B.: conceptualization, manuscript review, overview. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data sharing is not applicable.

Acknowledgments

The authors are grateful to the Universidad Técnica Particular de Loja (UTPL) for supporting this research and its open-access publication.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Jaikishun, S.; Li, W.; Yang, Z.; Song, S. Quinoa: In Perspective of Global Challenges. Agronomy 2019, 9, 176. [Google Scholar] [CrossRef]
  2. Bazile, D.; Jacobsen, S.-E.; Verniau, A. The Global Expansion of Quinoa: Trends and Limits. Front. Plant Sci. 2016, 7, 622. [Google Scholar] [CrossRef] [PubMed]
  3. Bellemare, M.F.; Fajardo-Gonzalez, J.; Gitter, S.R. Foods and Fads: The Welfare Impacts of Rising Quinoa Prices in Peru. World Dev. 2018, 112, 163–179. [Google Scholar] [CrossRef]
  4. Schmidt, D.; Verruma-Bernardi, M.R.; Forti, V.A.; Borges, M.T.M.R. Quinoa and Amaranth as Functional Foods: A Review. Food Rev. Int. 2023, 39, 2277–2296. [Google Scholar] [CrossRef]
  5. Joshi, R.P.; Jain, A.K.; Malhotra, N.; Kumari, M. Chapter 4—Origin, Domestication, and Spread. In Millets and Pseudo Cereals; Singh, M., Sood, S., Eds.; Woodhead Publishing Series in Food Science, Technology and Nutrition; Woodhead Publishing: Sawston, UK, 2021; pp. 33–38. ISBN 978-0-12-820089-6. [Google Scholar]
  6. Fernández-Ríos, A.; Laso, J.; Hoehn, D.; Amo-Setién, F.J.; Abajas-Bustillo, R.; Ortego, C.; Fullana-i-Palmer, P.; Bala, A.; Batlle-Bayer, L.; Balcells, M.; et al. A Critical Review of Superfoods from a Holistic Nutritional and Environmental Approach. J. Clean. Prod. 2022, 379, 134491. [Google Scholar] [CrossRef]
  7. Serwecińska, L. Antimicrobials and Antibiotic-Resistant Bacteria: A Risk to the Environment and to Public Health. Water 2020, 12, 3313. [Google Scholar] [CrossRef]
  8. Urban-Chmiel, R.; Marek, A.; Stępień-Pyśniak, D.; Wieczorek, K.; Dec, M.; Nowaczek, A.; Osek, J. Antibiotic Resistance in Bacteria—A Review. Antibiotics 2022, 11, 1079. [Google Scholar] [CrossRef]
  9. Chokshi, A.; Sifri, Z.; Cennimo, D.; Horng, H. Global Contributors to Antibiotic Resistance. J. Glob. Infect. Dis. 2019, 11, 36. [Google Scholar] [CrossRef]
  10. Miethke, M.; Pieroni, M.; Weber, T.; Brönstrup, M.; Hammann, P.; Halby, L.; Arimondo, P.B.; Glaser, P.; Aigle, B.; Bode, H.B.; et al. Towards the Sustainable Discovery and Development of New Antibiotics. Nat. Rev. Chem. 2021, 5, 726–749. [Google Scholar] [CrossRef]
  11. Calixto, J.B. The Role of Natural Products in Modern Drug Discovery. An. Acad. Bras. Ciênc. 2019, 91, e20190105. [Google Scholar] [CrossRef]
  12. Hanahan, D. Hallmarks of Cancer: New Dimensions. Cancer Discov. 2022, 12, 31–46. [Google Scholar] [CrossRef]
  13. Siegel, R.L.; Miller, K.D.; Fuchs, H.E.; Jemal, A. Cancer Statistics, 2022. CA Cancer J. Clin. 2022, 72, 7–33. [Google Scholar] [CrossRef]
  14. Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J. Clin. 2021, 71, 209–249. [Google Scholar] [CrossRef]
  15. Hashim, D.; Boffetta, P.; La Vecchia, C.; Rota, M.; Bertuccio, P.; Malvezzi, M.; Negri, E. The Global Decrease in Cancer Mortality: Trends and Disparities. Ann. Oncol. 2016, 27, 926–933. [Google Scholar] [CrossRef]
  16. Siegel, R.L.; Miller, K.D.; Jemal, A. Cancer Statistics, 2020. CA Cancer J. Clin. 2020, 70, 7–30. [Google Scholar] [CrossRef]
  17. Huang, M.; Lu, J.-J.; Ding, J. Natural Products in Cancer Therapy: Past, Present and Future. Nat. Prod. Bioprospect. 2021, 11, 5–13. [Google Scholar] [CrossRef]
  18. Masrour-Roudsari, J.; Ebrahimpour, S. Causal Role of Infectious Agents in Cancer: An Overview. Casp. J. Intern. Med. 2017, 8, 153–158. [Google Scholar] [CrossRef]
  19. Benharroch, D.; Osyntsov, L. Infectious Diseases Are Analogous with Cancer. Hypothesis and Implications. J. Cancer 2012, 3, 117. [Google Scholar] [CrossRef]
  20. Digital Science Dimensions. Available online: https://app.dimensions.ai/ (accessed on 25 May 2022).
  21. Paul, J.; Lim, W.M.; O’Cass, A.; Hao, A.W.; Bresciani, S. Scientific Procedures and Rationales for Systematic Literature Reviews (SPAR-4-SLR). Int. J. Consum. Stud. 2021, 45, O1–O16. [Google Scholar] [CrossRef]
  22. Visser, M.; van Eck, N.J.; Waltman, L. Large-Scale Comparison of Bibliographic Data Sources: Scopus, Web of Science, Dimensions, Crossref, and Microsoft Academic. Quant. Sci. Stud. 2021, 2, 20–41. [Google Scholar] [CrossRef]
  23. Australian Bureau of Statistics Australian and New Zealand Standard Research Classification (ANZSRC). Available online: https://www.abs.gov.au/statistics/classifications/australian-and-new-zealand-standard-research-classification-anzsrc/latest-release (accessed on 24 July 2022).
  24. International Plant Names Index the International Plant Names Index and World Checklist of Vascular Plants. Available online: https://powo.science.kew.org/ (accessed on 18 October 2023).
  25. POWO Chenopodium quinoa Willd. Available online: http://powo.science.kew.org/taxon/urn:lsid:ipni.org:names:165175-1 (accessed on 28 September 2023).
  26. Fuentes, F.F.; Martinez, E.A.; Hinrichsen, P.V.; Jellen, E.N.; Maughan, P.J. Assessment of Genetic Diversity Patterns in Chilean Quinoa (Chenopodium quinoa Willd.) Germplasm Using Multiplex Fluorescent Microsatellite Markers. Conserv. Genet. 2009, 10, 369–377. [Google Scholar] [CrossRef]
  27. Joshi, D.C.; Sood, S.; Hosahatti, R.; Kant, L.; Pattanayak, A.; Kumar, A.; Yadav, D.; Stetter, M.G. From Zero to Hero: The Past, Present and Future of Grain Amaranth Breeding. Theor. Appl. Genet. 2018, 131, 1807–1823. [Google Scholar] [CrossRef]
  28. POWO. Amaranthus hybridus L. Available online: http://powo.science.kew.org/taxon/urn:lsid:ipni.org:names:10648-2 (accessed on 28 September 2023).
  29. Song, L.M.; Yu, Y.; Du, L.D.; Ji, X.Y.; Gao, H.; Cai, Y.Q.; Li, C.J.; Xue, P. Does Saponin in Quinoa Really Embody the Source of Its Bitterness? Food Chem. 2024, 437, 137872. [Google Scholar] [CrossRef]
  30. Gómez Prado, L.; Aguilar Castellanos, E. Guía de Cultivo de La Quínoa, 2nd ed.; Universidad Agraria Nacional La Molina: Lima, Perú, 2016; ISBN 978-92-5-309069-3. [Google Scholar]
  31. Toderich, K.N.; Mamadrahimov, A.A.; Khaitov, B.B.; Karimov, A.A.; Soliev, A.A.; Nanduri, K.R.; Shuyskaya, E.V. Differential Impact of Salinity Stress on Seeds Minerals, Storage Proteins, Fatty Acids, and Squalene Composition of New Quinoa Genotype, Grown in Hyper-Arid Desert Environments. Front. Plant Sci. 2020, 11, 607102. [Google Scholar] [CrossRef]
  32. Aguirre Mendoza, Z.; Jaramillo Díaz, N.; Quizhpe Coronel, W. Arvenses Asociadas a Cultivos y Pastizales del Ecuador; Universidad Nacional de Loja: Loja, Ecuador, 2019; ISBN 978-9978-355-40-4. [Google Scholar]
  33. Calizaya, F.; Gómez, L.; Zegarra, J.; Pozo, M.; Mindani, C.; Caira, C.; Calizaya, E. Unveiling Ancestral Sustainability: A Comprehensive Study of Economic, Environmental, and Social Factors in Potato and Quinoa Cultivation in the Highland Aynokas of Puno, Peru. Sustainability 2023, 15, 13163. [Google Scholar] [CrossRef]
  34. Taaime, N.; Rafik, S.; El Mejahed, K.; Oukarroum, A.; Choukr-Allah, R.; Bouabid, R.; El Gharous, M. Worldwide Development of Agronomic Management Practices for Quinoa Cultivation: A Systematic Review. Front. Agron. 2023, 5, 1215441. [Google Scholar] [CrossRef]
  35. López, M.L.; Recalde, M.A. The First Quinoa (Chenopodium quinoa Willd) Macrobotanical Remains at Sierras Del Norte (Central Argentina) and Their Implications in Pre-Hispanic Subsistence Practices. J. Archaeol. Sci. Rep. 2016, 8, 426–433. [Google Scholar] [CrossRef]
  36. Lost Crops of the Incas: Little-Known Plants of the Andes with Promise for Worldwide Cultivation; National Academies Press: Washington, DC, USA, 1989; ISBN 978-0-309-04264-2.
  37. Bermejo, J.E.H.; León, J. Neglected Crops: 1492 from a Different Perspective; FAO: Rome, Italy, 1994; ISBN 978-92-5-103217-6. [Google Scholar]
  38. Rodríguez Gómez, M.J.; Matías Prieto, J.; Cruz Sobrado, V.; Calvo Magro, P. Nutritional Characterization of Six Quinoa (Chenopodium quinoa Willd) Varieties Cultivated in Southern Europe. J. Food Compos. Anal. 2021, 99, 103876. [Google Scholar] [CrossRef]
  39. Abd El-Hakim, A.F.; Mady, E.; Abou Tahoun, A.M.; Ghaly, M.S.A.; Eissa, M.A. Seed Quality and Protein Classification of Some Quinoa Varieties. J. Ecol. Eng. 2022, 23, 24–33. [Google Scholar] [CrossRef]
  40. Shi, D.; Fidelis, M.; Ren, Y.; Stone, A.K.; Ai, Y.; Nickerson, M.T. The Functional Attributes of Peruvian (Kankolla and Blanca Juli Blend) and Northern Quinoa (NQ94PT) Flours and Protein Isolates, and Their Protein Quality. Food Res. Int. 2020, 128, 108799. [Google Scholar] [CrossRef]
  41. Baraniak, J.; Kania-Dobrowolska, M. The Dual Nature of Amaranth—Functional Food and Potential Medicine. Foods 2022, 11, 618. [Google Scholar] [CrossRef]
  42. Aja, P.M.; Ale, B.A.; Ekpono, E.U.; Nwite, I.; Aja, L.; Asouzu, N.C.; Njoku, A. Amino Acid Profiles of Solanum Aethiopicum, Amaranthus hybridus, and Telfairia Occidentalis, Common Leafy Vegetables in Nigeria. Sci. Prog. 2021, 104, 00368504211032079. [Google Scholar] [CrossRef]
  43. Tang, Y.; Tsao, R. Phytochemicals in Quinoa and Amaranth Grains and Their Antioxidant, Anti-inflammatory, and Potential Health Beneficial Effects: A Review. Mol. Nutr. Food Res. 2017, 61, 1600767. [Google Scholar] [CrossRef]
  44. Santiago-Saenz, Y.O.; Hernández-Fuentes, A.D.; López-Palestina, C.U.; Garrido-Cauich, J.H.; Alatorre-Cruz, J.M.; Monroy-Torres, R.; Santiago-Saenz, Y.O.; Hernández-Fuentes, A.D.; López-Palestina, C.U.; Garrido-Cauich, J.H.; et al. Nutritional Importance and Biological Activity of Bioactive Compounds from Quelites Consumed in Mexico. Rev. Chil. Nutr. 2019, 46, 593–605. [Google Scholar] [CrossRef]
  45. Reynaga Nava, A. Caracterización Fisica-Quimica de Trece Ecotipos de Quinua Real (Chenopodium quinoa Willd.) del Altiplano Sur de Bolivia Con Fines Agroindustriales; Reynaga Nava, Arturo Edgar: Murillo, Bolivia, 2011; ISBN 978-99954-2-124-3. [Google Scholar]
  46. Akubugwo, I.E.; Obasi, N.A.; Chinyere, G.C.; Ugbogu, A.E. Nutritional and Chemical Value of Amaranthus hybridus L. Leaves from Afikpo, Nigeria. Afr. J. Biotechnol. 2007, 6, 2833–2839. [Google Scholar] [CrossRef]
  47. Yaméogo, C.W.; Garanet, F. Minerals Composition of Solanum aethiopicum L. and Amaranthus hybridus L. Leaves from Burkina Faso. Eur. J. Nutr. Food Saf. 2023, 15, 35–41. [Google Scholar] [CrossRef]
  48. FAO. International Year of Quinoa 2013. Available online: https://www.fao.org/quinoa-2013/ (accessed on 26 October 2022).
  49. FAO. La Quinua: Cultivo Milenario Para Contribuir a la Seguridad Alimentaria Mundial; FAO: Rome, Italy, 2011; p. 66. [Google Scholar]
  50. Bailon-Moscoso, N.; Tinitana, F.; Martínez-Espinosa, R.; Jaramillo-Velez, A.; Palacio-Arpi, A.; Aguilar-Hernandez, J.; Romero-Benavides, J.C. Cytotoxic, Antioxidative, Genotoxic and Antigenotoxic Effects of Horchata, Beverage of South Ecuador. BMC Complement. Altern. Med. 2017, 17, 539. [Google Scholar] [CrossRef]
  51. Rojas-Le-Fort, M.; Valdivieso-López, I.P.; Duarte-Casar, R. Representations of Ecuadorian Cuisine in the Coast and the Highlands Regions through the Free Listing Technique. Discov. Food 2023, 3, 20. [Google Scholar] [CrossRef]
  52. de la Torre, L.; Navarrete, H.; Muriel, P.; Macía, M.; Balslev, H. Enciclopedia de Las Plantas Útiles del Ecuador; Herbario QCA de la Escuela de Ciencias Biológicas de la Pontificia Universidad Católica del Ecuador: Quito, Ecuador, 2008; ISBN 978-9978-77-135-8. [Google Scholar]
  53. Filho, A.M.M.; Pirozi, M.R.; Borges, J.T.D.S.; Pinheiro Sant’Ana, H.M.; Chaves, J.B.P.; Coimbra, J.S.D.R. Quinoa: Nutritional, Functional, and Antinutritional Aspects. Crit. Rev. Food Sci. Nutr. 2017, 57, 1618–1630. [Google Scholar] [CrossRef]
  54. Alandia, G.; Odone, A.; Rodriguez, J.P.; Bazile, D.; Condori, B. Quinoa—Evolution and Future Perspectives. In The Quinoa Genome; Schmöckel, S.M., Ed.; Compendium of Plant Genomes; Springer International Publishing: Cham, Switzerland, 2021; pp. 179–195. ISBN 978-3-030-65237-1. [Google Scholar]
  55. Salcedo, S.; Santivañez, T. Recetario Internacional de la Quinua: Tradición y Vanguardia; FAO: Rome, Iatly, 2014; ISBN 978-92-5-308058-8. [Google Scholar]
  56. Ayala Macedo, G. Consumption of Quinoa in Peru. Food Rev. Int. 2003, 19, 221–227. [Google Scholar] [CrossRef]
  57. Hançer, Ç.K.; Sevgi, E.; Altinbaşak, B.B.; Çakir, E.A.; Akkaya, M. Traditional Knowledge of Wild Edible Plants of Biga (Çanakkale), Turkey. Acta Soc. Bot. Pol. 2020, 89, 8914. [Google Scholar] [CrossRef]
  58. Hilou, A.; Ouedraogo, I.; Sombié, P.A.E.D.; Guenné, S.; Paré, D.; Compaoré, M. Leafy Amaranthus Consumption Patterns in Ouagadougou, Burkina Faso. Afr. J. Food Agric. Nutr. Dev. 2016, 16, 11248–11264. [Google Scholar] [CrossRef]
  59. Franco, A.; Arias Giraldo, S.; Anaya García, S.E.; Muñoz Quintero, D. Perspectivas tecnológicas y nutricionales de la quinua (Chenopodium quinoa): Un pseudocereal andino funcional. Rev. Española Nutr. Comunitaria = Span. J. Community Nutr. 2021, 27, 12. [Google Scholar]
  60. Melini, F.; Melini, V.; Galfo, M. A Cross-Sectional Survey of the Nutritional Quality of Quinoa Food Products Available in the Italian Market. Foods 2023, 12, 1562. [Google Scholar] [CrossRef]
  61. Balakrishnan, G.; Schneider, R.G. The Role of Amaranth, Quinoa, and Millets for the Development of Healthy, Sustainable Food Products—A Concise Review. Foods 2022, 11, 2442. [Google Scholar] [CrossRef] [PubMed]
  62. Aderibigbe, O.R.; Ezekiel, O.O.; Owolade, S.O.; Korese, J.K.; Sturm, B.; Hensel, O. Exploring the Potentials of Underutilized Grain Amaranth (Amaranthus spp.) along the Value Chain for Food and Nutrition Security: A Review. Crit. Rev. Food Sci. Nutr. 2022, 62, 656–669. [Google Scholar] [CrossRef] [PubMed]
  63. Repo-Carrasco-Valencia, R.; Basilio-Atencio, J.; Luna-Mercado, G.I.; Pilco-Quesada, S.; Vidaurre-Ruiz, J. Andean Ancient Grains: Nutritional Value and Novel Uses. Biol. Life Sci. Forum 2022, 8, 15. [Google Scholar] [CrossRef]
  64. Haros, C.M.; Martínez, M.L.; Agostini, B.V.; Muñoz, L.A. Food Uses of Selected Ancient Grains. In Latin-American Seeds; CRC Press: Boca Raton, FL, USA, 2023; ISBN 978-1-00-308842-4. [Google Scholar]
  65. Mouritsen, O.G.; Rhatigan, P.; Pérez-Lloréns, J.L. The Rise of Seaweed Gastronomy: Phycogastronomy. Bot. Mar. 2019, 62, 195–209. [Google Scholar] [CrossRef]
  66. Bakouri, H.; Ziane, A.; Guemra, K. Development of Multifunctional Packaging Films Based on Arginine-Modified Chitosan/Gelatin Matrix and Betacyanins from Weed Amaranth (A. Hybridus). Int. J. Biol. Macromol. 2023, 230, 123181. [Google Scholar] [CrossRef]
  67. Alak, G.; Guler, K.; Ucar, A.; Parlak, V.; Kocaman, E.M.; Yanık, T.; Atamanalp, M. Quinoa as Polymer in Edible Films with Essential Oil: Effects on Rainbow Trout Fillets Shelf Life. J. Food Process. Preserv. 2019, 43, e14268. [Google Scholar] [CrossRef]
  68. Sharma, A.; Alam, M.; Pant, K.; Nanda, V. Amaranth & Quinoa Sprouts. In Advances in Plant Sprouts: Phytochemistry and Biofunctionalities; Majid, I., Kehinde, B.A., Dar, B., Nanda, V., Eds.; Springer International Publishing: Cham, Switzerland, 2023; pp. 127–151. ISBN 978-3-031-40916-5. [Google Scholar]
  69. Janmohammadi, H.; Hosseintabar-Ghasemabad, B.; Oliyai, M.; Alijani, S.; Gorlov, I.F.; Slozhenkina, M.I.; Mosolov, A.A.; Suarez Ramirez, L.; Seidavi, A.; Laudadio, V.; et al. Effect of Dietary Amaranth (Amaranthus hybridus Chlorostachys) Supplemented with Enzyme Blend on Egg Quality, Serum Biochemistry and Antioxidant Status in Laying Hens. Antioxidants 2023, 12, 456. [Google Scholar] [CrossRef]
  70. Asher, A.; Galili, S.; Whitney, T.; Rubinovich, L. The Potential of Quinoa (Chenopodium quinoa) Cultivation in Israel as a Dual-Purpose Crop for Grain Production and Livestock Feed. Sci. Hortic. 2020, 272, 109534. [Google Scholar] [CrossRef]
  71. Jan, N.; Hussain, S.Z.; Naseer, B.; Bhat, T.A. Amaranth and Quinoa as Potential Nutraceuticals: A Review of Anti-Nutritional Factors, Health Benefits and Their Applications in Food, Medicinal and Cosmetic Sectors. Food Chem. X 2023, 18, 100687. [Google Scholar] [CrossRef] [PubMed]
  72. Cui, H.; Li, S.; Roy, D.; Guo, Q.; Ye, A. Modifying Quinoa Protein for Enhanced Functional Properties and Digestibility: A Review. Curr. Res. Food Sci. 2023, 7, 100604. [Google Scholar] [CrossRef] [PubMed]
  73. Cerdá-Bernad, D.; Valero-Cases, E.; Pastor, J.-J.; Frutos, M.J.; Pérez-Llamas, F. Probiotic Red Quinoa Drinks for Celiacs and Lactose Intolerant People: Study of Functional, Physicochemical and Probiotic Properties during Fermentation and Gastrointestinal Digestion. Int. J. Food Sci. Nutr. 2022, 73, 49–59. [Google Scholar] [CrossRef] [PubMed]
  74. Granda, L.; Rosero, M.; Rosero, A. Plantas Medicinales de La Región Andina Tropical. Quinoa (Chenopodium quinoa Willd.) y Coca (Erythroxylum sp.), Tesoros Milenarios Para Tratamiento Medicinal. In Etnobotánica y Fitoterapia en América; Mendel University in Brno: Brno, Czech Republic, 2015; ISBN 978-80-7509-349-3. [Google Scholar]
  75. WHO Anatomical Therapeutic Chemical (ATC) Classification. Available online: https://www.who.int/tools/atc-ddd-toolkit/atc-classification (accessed on 8 June 2021).
  76. Tinitana, F.; Rios, M.; Romero-Benavides, J.C.; de la Cruz Rot, M.; Pardo-de-Santayana, M. Medicinal Plants Sold at Traditional Markets in Southern Ecuador. J. Ethnobiol. Ethnomed. 2016, 12, 29. [Google Scholar] [CrossRef] [PubMed]
  77. Ruth, O.N.; Unathi, K.; Nomali, N.; Chinsamy, M. Underutilization Versus Nutritional-Nutraceutical Potential of the Amaranthus Food Plant: A Mini-Review. Appl. Sci. 2021, 11, 6879. [Google Scholar] [CrossRef]
  78. Kongdang, P.; Dukaew, N.; Pruksakorn, D.; Koonrungsesomboon, N. Biochemistry of Amaranthus Polyphenols and Their Potential Benefits on Gut Ecosystem: A Comprehensive Review of the Literature. J. Ethnopharmacol. 2021, 281, 114547. [Google Scholar] [CrossRef]
  79. Stigger, A.L.; Marcolongo-Pereira, C.; de Lourdes Adrien, M.; Santos, B.L.; Fiss, L.; Vargas, S.F., Jr.; Grecco, F.B.; Schild, A.L. Intoxicação espontânea por Amaranthus hybridus (Amaranthaceae) em bovinos no sul do Rio Grande do Sul. Pesq. Vet. Bras. 2013, 33, 1004–1008. [Google Scholar] [CrossRef]
  80. Rios, M.; Tinitana, F.; Jarrín-V, P.; Donoso, N.; Romero-Benavides, J.C. “Horchata” Drink in Southern Ecuador: Medicinal Plants and People’s Wellbeing. J. Ethnobiol. Ethnomed. 2017, 13, 18. [Google Scholar] [CrossRef]
  81. Peralta, I.E.; Villacrés, E.; Mazón, N.; Rivera, M.M.; Subía, G.C. El Ataco, Sangorache o Amaranto Negro (Amaranthus hybridus L.) en Ecuador; Publicación Miscelánea; INIAP: Quito, Ecuador, 2008; p. 63. [Google Scholar]
  82. Ibarra-Morales, A.; Pino, I.S.; Solís-Fernández, K.Z. El amaranto en la región maya. Ecofronteras 2021, 25, 71. [Google Scholar]
  83. Qian, G.; Li, X.; Zhang, H.; Zhang, H.; Zhou, J.; Ma, X.; Sun, W.; Yang, W.; He, R.; Wahab, A.; et al. Metabolomics Analysis Reveals the Accumulation Patterns of Flavonoids and Phenolic Acids in Quinoa (Chenopodium quinoa Willd.) Grains of Different Colors. Food Chem. X 2023, 17, 100594. [Google Scholar] [CrossRef]
  84. Tang, Y.; Zhang, B.; Li, X.; Chen, P.X.; Zhang, H.; Liu, R.; Tsao, R. Bound Phenolics of Quinoa Seeds Released by Acid, Alkaline, and Enzymatic Treatments and Their Antioxidant and α-Glucosidase and Pancreatic Lipase Inhibitory Effects. J. Agric. Food Chem. 2016, 64, 1712–1719. [Google Scholar] [CrossRef]
  85. Zhengkang, H.; Wang, G.; Yao, W.; Zhu, W. Isoflavonic Phytoestrogens—New Prebiotics for Farm Animals: A Review on Research in China. Curr. Issues Intest. Microbiol. 2006, 7, 53–60. [Google Scholar] [PubMed]
  86. Ekeke, C.; Manga, T.T.; Mensah, S.I. Comparative Phytochemical, Morphological and Anatomical Studies of Amaranthus hybridus L. and Amaranthus spinosus L. (Amaranthaceae). Res. J. Med. Plants 2019, 13, 53–63. [Google Scholar] [CrossRef]
  87. Medoua, G.N.; Oldewage-Theron, W.H. Effect of Drying and Cooking on Nutritional Value and Antioxidant Capacity of Morogo (Amaranthus hybridus) a Traditional Leafy Vegetable Grown in South Africa. J. Food Sci. Technol. 2014, 51, 736–742. [Google Scholar] [CrossRef] [PubMed]
  88. Barthomeuf, C.; Debiton, E.; Mshvildadze, V.; Kemertelidze, E.; Balansard, G. In Vitro Activity of Hederacolchisid A1 Compared with Other Saponins from Hedera Colchica Against Proliferation of Human Carcinoma and Melanoma Cells. Planta Med. 2002, 68, 672–675. [Google Scholar] [CrossRef] [PubMed]
  89. Ahumada, A.; Ortega, A.; Chito, D.; Benítez, R. Saponinas de quinua (Chenopodium quinoa Willd.): Un subproducto con alto potencial biológico. Rev. Colomb. Cienc. Químico-Farm. 2016, 45, 438–469. [Google Scholar] [CrossRef]
  90. El Hazzam, K.; Hafsa, J.; Sobeh, M.; Mhada, M.; Taourirte, M.; EL Kacimi, K.; Yasri, A. An Insight into Saponins from Quinoa (Chenopodium quinoa Willd): A Review. Molecules 2020, 25, 1059. [Google Scholar] [CrossRef]
  91. Fanali, C.; Beccaria, M.; Salivo, S.; Tranchida, P.; Tripodo, G.; Farnetti, S.; Dugo, L.; Dugo, P.; Mondello, L. Non-Polar Lipids Characterization of Quinoa (Chenopodium quinoa) Seed by Comprehensive Two-Dimensional Gas Chromatography with Flame Ionization/Mass Spectrometry Detection and Non-Aqueous Reversed-Phase Liquid Chromatography with Atmospheric Pressure Chemical Ionization Mass Spectrometry Detection. J. Sep. Sci. 2015, 38, 3151–3160. [Google Scholar] [CrossRef]
  92. Ejoh, S.I.; Wireko-Manu, F.D.; Page, D.; Renard, C.M. Traditional Green Leafy Vegetables as Underutilised Sources of Micronutrients in a Rural Farming Community in South-West Nigeria I: Estimation of Vitamin C, Carotenoids and Mineral Contents. S. Afr. J. Clin. Nutr. 2021, 34, 40–45. [Google Scholar] [CrossRef]
  93. Nana, F.W.; Hilou, A.; Millogo, J.F.; Nacoulma, O.G. Phytochemical Composition, Antioxidant and Xanthine Oxidase Inhibitory Activities of Amaranthus cruentus L. and Amaranthus hybridus L. Extracts. Pharmaceuticals 2012, 5, 613–628. [Google Scholar] [CrossRef]
  94. Escribano, J.; Cabanes, J.; Jiménez-Atiénzar, M.; Ibañez-Tremolada, M.; Gómez-Pando, L.R.; García-Carmona, F.; Gandía-Herrero, F. Characterization of Betalains, Saponins and Antioxidant Power in Differently Colored Quinoa (Chenopodium quinoa) Varieties. Food Chem. 2017, 234, 285–294. [Google Scholar] [CrossRef]
  95. Ďúranová, H.; Fialková, V.; Bilčíková, J.; Lukáč, N.; Kňažická, Z. Lunasin and Its Versatile Health-Promoting Actions. J. Microbiol. Biotechnol. Food Sci. 2019, 8, 1106–1110. [Google Scholar] [CrossRef]
  96. Maldonado-Cervantes, E.; Jeong, H.J.; León-Galván, F.; Barrera-Pacheco, A.; De León-Rodríguez, A.; de Mejia, E.G.; de Lumen, B.O.; de la Rosa, A.P.B. Amaranth Lunasin-like Peptide Internalizes into the Cell Nucleus and Inhibits Chemical Carcinogen-Induced Transformation of NIH-3T3 Cells. Peptides 2010, 31, 1635–1642. [Google Scholar] [CrossRef] [PubMed]
  97. Khan, I.H.; Javaid, A. Anticancer, Antimicrobial and Antioxidant Compounds of Quinoa Inflorescence. Adv. Life Sci. 2020, 8, 68–72. [Google Scholar]
  98. Khan, I.H.; Javaid, A. Identification of Pharmaceutically Important Constituents of Quinoa Root. Jordan J. Pharm. Sci. 2023, 16, 96–102. [Google Scholar] [CrossRef]
  99. Jy, C.; Jh, M.; Ky, S.; Kh, P. Antimicrobial Activity of 4-Hydroxybenzoic Acid and Trans 4-Hydroxycinnamic Acid Isolated and Identified from Rice Hull. Biosci. Biotechnol. Biochem. 1998, 62, 2273–2276. [Google Scholar] [CrossRef]
  100. Borges, A.; Ferreira, C.; Saavedra, M.J.; Simões, M. Antibacterial Activity and Mode of Action of Ferulic and Gallic Acids against Pathogenic Bacteria. Microb. Drug Resist. 2013, 19, 256–265. [Google Scholar] [CrossRef]
  101. Wu, M.; Tian, L.; Fu, J.; Liao, S.; Li, H.; Gai, Z.; Gong, G. Antibacterial Mechanism of Protocatechuic Acid against Yersinia Enterocolitica and Its Application in Pork. Food Control 2022, 133, 108573. [Google Scholar] [CrossRef]
  102. Ojha, D.; Patil, K.N. P-Coumaric Acid Inhibits the Listeria Monocytogenes RecA Protein Functions and SOS Response: An Antimicrobial Target. Biochem. Biophys. Res. Commun. 2019, 517, 655–661. [Google Scholar] [CrossRef] [PubMed]
  103. Jan, R.; Khan, M.; Asaf, S.; Lubna; Asif, S.; Kim, K.-M. Bioactivity and Therapeutic Potential of Kaempferol and Quercetin: New Insights for Plant and Human Health. Plants 2022, 11, 2623. [Google Scholar] [CrossRef] [PubMed]
  104. Ming, D.; Wang, D.; Cao, F.; Xiang, H.; Mu, D.; Cao, J.; Li, B.; Zhong, L.; Dong, X.; Zhong, X.; et al. Kaempferol Inhibits the Primary Attachment Phase of Biofilm Formation in Staphylococcus aureus. Front. Microbiol. 2017, 8, 2263. [Google Scholar] [CrossRef]
  105. Imran, M.; Saeed, F.; Hussain, G.; Imran, A.; Mehmood, Z.; Gondal, T.A.; El-Ghorab, A.; Ahmad, I.; Pezzani, R.; Arshad, M.U.; et al. Myricetin: A Comprehensive Review on Its Biological Potentials. Food Sci. Nutr. 2021, 9, 5854–5868. [Google Scholar] [CrossRef]
  106. Sharma, A.; Kathuria, D.; Kolita, B.; Gohain, A.; Das, A.K.; Bhardwaj, G.; Simal-Gandara, J. Greener Approach for the Isolation of Oleanolic Acid from Nepeta Leucophylla Benth. Its Derivatization and Their Molecular Docking as Antibacterial and Antiviral Agents. Heliyon 2023, 9, e18639. [Google Scholar] [CrossRef]
  107. Ndukwe, G.I.; Clark, P.D.; Jack, I.R. In Vitro Antioxidant and Antimicrobial Potentials of Three Extracts of Amaranthus hybridus L. Leaf and Their Phytochemicals. Eur. Chem. Bull. 2020, 9, 164–173. [Google Scholar] [CrossRef]
  108. Al-Mamun, M.A.; Husna, J.; Khatun, M.; Hasan, R.; Kamruzzaman, M.; Hoque, K.M.F.; Reza, M.A.; Ferdousi, Z. Assessment of Antioxidant, Anticancer and Antimicrobial Activity of Two Vegetable Species of Amaranthus in Bangladesh. BMC Complement. Altern. Med. 2016, 16, 157. [Google Scholar] [CrossRef]
  109. Maiyo, Z.C.; Ngure, R.M.; Matasyoh, J.C.; Chepkorir, R. Phytochemical Constituents and Antimicrobial Activity of Leaf Extracts of Three Amaranthus Plant Species. Afr. J. Biotechnol. 2010, 9, 3178–3182. [Google Scholar]
  110. Okoye, E.I. Qualitative and Quantitative Phytochemical Analysis and Antimicrobial Screening of Solvent Extracts of Amaranthus hybridus (Stem and Leaves). Chem. Res. J. 2018, 3, 9–13. [Google Scholar]
  111. Yong, Y.Y.; Dykes, G.; Lee, S.M.; Choo, W.S. Comparative Study of Betacyanin Profile and Antimicrobial Activity of Red Pitahaya (Hylocereus polyrhizus) and Red Spinach (Amaranthus dubius). Plant Foods Hum. Nutr. 2017, 72, 41–47. [Google Scholar] [CrossRef]
  112. Yelfi, Y.; Susilo, H.; Kurnia, N.M. Mouthwash of Amaranthus hybridus L. Leaf Extract with Ethyl Acetate as A Streptococcus Mutans Antibacterial. J. Ilm. Farm. Farmasyifa 2022, 5, 79–90. [Google Scholar] [CrossRef]
  113. Guo, L.; Wang, Y.; Bi, X.; Duo, K.; Sun, Q.; Yun, X.; Zhang, Y.; Fei, P.; Han, J. Antimicrobial Activity and Mechanism of Action of the Amaranthus tricolor Crude Extract against Staphylococcus aureus and Potential Application in Cooked Meat. Foods 2020, 9, 359. [Google Scholar] [CrossRef]
  114. Jimoh, M.O.; Afolayan, A.J.; Lewu, F.B. Toxicity and Antimicrobial Activities of Amaranthus caudatus L. (Amaranthaceae) Harvested from Formulated Soils at Different Growth Stages. J. Evid. Based Integr. Med. 2020, 25, 2515690X20971578. [Google Scholar] [CrossRef] [PubMed]
  115. Agarwal, A.; Rizwana; Tripathi, A.D.; Kumar, T.; Sharma, K.P.; Patel, S.K.S. Nutritional and Functional New Perspectives and Potential Health Benefits of Quinoa and Chia Seeds. Antioxidants 2023, 12, 1413. [Google Scholar] [CrossRef] [PubMed]
  116. Ding, M.; Zhang, X.; Shi, J.; Cui, K.; Yang, R.; Liu, F.; Shan, S.; Israr, G.; Li, Z. Terpenoids of Quinoa Bran Suppresses Colorectal Cancer by Inducing Cell Apoptosis. Food Biosci. 2023, 53, 102615. [Google Scholar] [CrossRef]
  117. Bailon-Moscoso, N.; Coronel-Hidalgo, J.; Duarte-Casar, R.; Guamán-Ortiz, L.M.; Figueroa, J.G.; Romero-Benavides, J.C. Exploring the Antioxidant Potential of Tragia volubilis L.: Mitigating Chemotherapeutic Effects of Doxorubicin on Tumor Cells. Antioxidants 2023, 12, 2003. [Google Scholar] [CrossRef] [PubMed]
  118. Gawlik-Dziki, U.; Świeca, M.; Sułkowski, M.; Dziki, D.; Baraniak, B.; Czyż, J. Antioxidant and Anticancer Activities of Chenopodium quinoa Leaves Extracts—In Vitro Study. Food Chem. Toxicol. 2013, 57, 154–160. [Google Scholar] [CrossRef] [PubMed]
  119. Yang, F.; Guo, T.; Zhou, Y.; Han, S.; Sun, S.; Luo, F. Biological Functions of Active Ingredients in Quinoa Bran: Advance and Prospective. Crit. Rev. Food Sci. Nutr. 2022, 1–15. [Google Scholar] [CrossRef]
  120. Shen, Y.; Zheng, L.; Peng, Y.; Zhu, X.; Liu, F.; Yang, X.; Li, H. Physicochemical, Antioxidant and Anticancer Characteristics of Seed Oil from Three Chenopodium quinoa Genotypes. Molecules 2022, 27, 2453. [Google Scholar] [CrossRef]
  121. Stikić, R.I.; Milinčić, D.D.; Kostić, A.Ž.; Jovanović, Z.B.; Gašić, U.M.; Tešić, Ž.L.; Djordjević, N.Z.; Savić, S.K.; Czekus, B.G.; Pešić, M.B. Polyphenolic Profiles, Antioxidant, and in Vitro Anticancer Activities of the Seeds of Puno and Titicaca Quinoa Cultivars. Cereal Chem. 2020, 97, 626–633. [Google Scholar] [CrossRef]
  122. Mohamed, D.A.; Fouda, K.A.; Mohamed, R.S. In Vitro Anticancer Activity of Quinoa and Safflower Seeds and Their Preventive Effects on Non-Alcoholic Fatty Liver. Pak. J. Biol. Sci. 2019, 22, 383–392. [Google Scholar] [CrossRef]
  123. Rotondo, R.; Ragucci, S.; Castaldo, S.; Oliva, M.A.; Landi, N.; Pedone, P.V.; Arcella, A.; Di Maro, A. Cytotoxicity Effect of Quinoin, Type 1 Ribosome-Inactivating Protein from Quinoa Seeds, on Glioblastoma Cells. Toxins 2021, 13, 684. [Google Scholar] [CrossRef]
  124. Hu, Y.; Zhang, J.; Zou, L.; Fu, C.; Li, P.; Zhao, G. Chemical Characterization, Antioxidant, Immune-Regulating and Anticancer Activities of a Novel Bioactive Polysaccharide from Chenopodium quinoa Seeds. Int. J. Biol. Macromol. 2017, 99, 622–629. [Google Scholar] [CrossRef]
  125. de Cedrón, M.G.; del Hierro, J.N.; Reguero, M.; Wagner, S.; Bouzas, A.; Quijada-Freire, A.; Reglero, G.; Martín, D.; de Molina, A.R. Saponin-Rich Extracts and Their Acid Hydrolysates Differentially Target Colorectal Cancer Metabolism in the Frame of Precision Nutrition. Cancers 2020, 12, 3399. [Google Scholar] [CrossRef]
  126. Shuvalov, O.; Kirdeeva, Y.; Fefilova, E.; Netsvetay, S.; Zorin, M.; Vlasova, Y.; Fedorova, O.; Daks, A.; Parfenyev, S.; Barlev, N. 20-Hydroxyecdysone Confers Antioxidant and Antineoplastic Properties in Human Non-Small Cell Lung Cancer Cells. Metabolites 2023, 13, 656. [Google Scholar] [CrossRef]
  127. Graf, B.L.; Poulev, A.; Kuhn, P.; Grace, M.H.; Lila, M.A.; Raskin, I. Quinoa Seeds Leach Phytoecdysteroids and other Compounds with Anti-Diabetic Properties. Food Chem. 2014, 163, 178–185. [Google Scholar] [CrossRef] [PubMed]
  128. Rodríguez-García, C.; Sánchez-Quesada, C.; Gaforio, J.J. Dietary Flavonoids as Cancer Chemopreventive Agents: An Updated Review of Human Studies. Antioxidants 2019, 8, 137. [Google Scholar] [CrossRef] [PubMed]
  129. Darendelioğlu, E. Studies of Anticancer Activity of Beta-Carotene, Alpha-Tocopherol and Ascorbic Acid in SH-SY5Y Neuroblastoma Cells. J. Inst. Sci. Technol. 2019, 9, 1657–1665. [Google Scholar] [CrossRef]
  130. Adewale, A.; Olorunju, A. Modulatory of Effect of Fresh Amaranthus Caudatus and Amaranthus hybridus Aqueous Leaf Extracts on Detoxify Enzymes and Micronuclei Formation after Exposure to Sodium Arsenite. Phcog Res 2013, 5, 300. [Google Scholar] [CrossRef] [PubMed]
  131. Ibrahim, M.I.M.; Pieters, R.; Abdel-Aziem, S.H.; van der Walt, A.M.; Bezuidenhout, C.C.; Giesy, J.P.; Abdel-Wahhab, M.A. Protective Effects of Amaranthus hybridus against Aflatoxin B1 and Fumonisin B1-Induced Genotoxicity in H4IIE-Luc Cells. Hepatoma Res. 2015, 1, 136–146. [Google Scholar] [CrossRef]
  132. Nsamou, P.C.N.; Momo, A.C.T.; Tchatat, Y.B.P.; Fozin, G.R.B.; Kemka, F.X.; Ngadjui, E.; Watcho, P. The Edible Plant Amaranthus hybridus (Amaranthaceae) Prevents the Biochemical, Histopathological and Fertility Impairments in Colibri®-Treated Female Rats. Toxicol. Rep. 2022, 9, 422–431. [Google Scholar] [CrossRef] [PubMed]
  133. Mabeyo, P.E.; Manoko, M.L.K.; Gruhonjic, A.; Fitzpatrick, P.A.; Landberg, G.; Erdélyi, M.; Nyandoro, S.S. Selenium Accumulating Leafy Vegetables Are a Potential Source of Functional Foods. Int. J. Food Sci. 2015, 2015, e549676. [Google Scholar] [CrossRef] [PubMed]
  134. Tang, Z.; Zhou, C.; Cai, Y.; Tang, Y.; Sun, W.; Yao, H.; Zheng, T.; Chen, H.; Xiao, Y.; Shan, Z.; et al. Purification, Characterization and Antioxidant Activities In Vitro of Polysaccharides from Amaranthus hybridus L. PeerJ 2020, 8, e9077. [Google Scholar] [CrossRef] [PubMed]
  135. Fan, X.; Guo, H.; Teng, C.; Zhang, B.; Blecker, C.; Ren, G. Anti-Colon Cancer Activity of Novel Peptides Isolated from In Vitro Digestion of Quinoa Protein in Caco-2 Cells. Foods 2022, 11, 194. [Google Scholar] [CrossRef]
  136. Fan, X.; Guo, H.; Teng, C.; Yang, X.; Qin, P.; Richel, A.; Zhang, L.; Blecker, C.; Ren, G. Supplementation of Quinoa Peptides Alleviates Colorectal Cancer and Restores Gut Microbiota in AOM/DSS-Treated Mice. Food Chem. 2022, 408, 135196. [Google Scholar] [CrossRef]
Pharmaceuticals 16 01728 g001
Figure 1. Review flow chart.
Figure 1. Review flow chart.
Pharmaceuticals 16 01728 g001
Pharmaceuticals 16 01728 g002
Figure 2. Distribution by country of C. quinoa (A) in green and A. hybridus (B) in purple.
Figure 2. Distribution by country of C. quinoa (A) in green and A. hybridus (B) in purple.
Pharmaceuticals 16 01728 g002
Pharmaceuticals 16 01728 g003
Figure 3. Published articles on antibacterial and anticancer activity of compound classes from C. quinoa and A. hybridus.
Figure 3. Published articles on antibacterial and anticancer activity of compound classes from C. quinoa and A. hybridus.
Pharmaceuticals 16 01728 g003
Pharmaceuticals 16 01728 g004
Figure 4. Quinoa compounds with antimicrobial activity.
Figure 4. Quinoa compounds with antimicrobial activity.
Pharmaceuticals 16 01728 g004
Pharmaceuticals 16 01728 g005
Figure 5. Representative compounds with anticancer activity present in Quinoa and A. hybridus.
Figure 5. Representative compounds with anticancer activity present in Quinoa and A. hybridus.
Pharmaceuticals 16 01728 g005
Table 1. The SPAR-4-SLR systematic review method followed.
Table 1. The SPAR-4-SLR systematic review method followed.
StageSubstage
1 Assembling1a IdentificationDomain:
Phytochemistry, phytomedicine
Research questions:
What is the current knowledge about the antimicrobial and anticancer activity of neglected Andean grains C. quinoa and A. hybridus?
Source type:
Research articles, reviews and book chapters
Source quality:
Crossref database
1b AcquisitionSearch mechanism and material acquisition:
Dimensions query, ordered by rank
Search period:
No time constraints
Search keywords:
(Quinoa OR Amaranth) AND (antimicrobial OR cancer)
Total number of articles returned from the search:
221
2 Arranging2a OrganizationOrganizing codes:
As provided in Dimensions export
2b PurificationArticle type excluded (n = 121):
Remove duplicates (n = 8); remove predatory titles; remove non-empirical, non-review articles. Remove articles not related to the topic or dealing with other Amaranthus species
Article type included (n = 100):
Triangulation with previous reviews to ensure seminal articles are included
3 Assessing3a EvaluationAnalysis method:
Content—descriptive
Agenda proposal method:
Future research directions and identification of existing gaps
3c ReportingReporting conventions:
Discussion and summaries in the form of tables and figures
Limitations:
Discussed
Sources of support:
Acknowledged
Table 2. Exclusion criteria.
Table 2. Exclusion criteria.
CriterionExcluded Articles
Duplicate article8
Unrelated topics112
Corrigenda1
Total121
Table 3. Example proximal composition of Quinoa and Amaranth grains.
Table 3. Example proximal composition of Quinoa and Amaranth grains.
SpeciesProtein
(% dew)		Carbohydrate
(% dew)		Fiber
(% dw)		Fat
(% dw)		Ash
(% dw)		Energy
(kcal/100 g)
Quinoa14.164.27.06.12.4353
Amaranth13.665.36.77.06.7365
Source: [4]. Note: dw: Dry weight.
Table 4. Ethnopharmacological uses of C. quinoa.
Table 4. Ethnopharmacological uses of C. quinoa.
Plant OrganMode of UseEffectATC
Category		Ref.
Stem
Leaves		NS“Improve the quality of blood”B[74]
LeavesPoulticeSore throat relief
Angina		A
C		[49]
LeavesDecoctionUrinary infections
Laxative
Rheumatism		G
A
M		[52]
Leaves (fresh)Soup or main courseScurvy and other avitaminosesA[49]
FruitPoultice or decoctionWound treatmentD[49]
SeedDecoctionLiver abscesses
Internal secretions
Catarrhal affections		J[49]
Bronchial disorders
Colds
Cough
Tonsillitis		R[49]
SoakedIntermittent feversJ[52]
NSColon cancer preventionA[74]
Seed, stem, leavesDecoctionEmmenagogueG[52]
LeavesPoundedHeadachesN[52]
NS: Not specified. Anatomical Therapeutical Chemical (ATC) categories are as follows. A: Alimentary tract and metabolism; B: Blood and blood-forming organs; C: Cardiovascular system; D: Dermatological; G: Genito-urinary system and sex hormones; J: Anti-infective for systemic use; M: Musculo-skeletal system; N: Nervous system; R: Respiratory system [75].
Table 5. Ethnopharmacological uses of A. hybridus.
Table 5. Ethnopharmacological uses of A. hybridus.
Plant OrganMode of UseEffectATC CategoryRef.
All organsDecoctionCalming
Antiacne
Heart conditions
Antidiarrheal
Anti-inflammatory		N
D
C
A		[52,80]
All organsNSCarminativeA[52]
LeavesDecoctionCancer preventionL[81]
Whole plantPoulticeSkin conditions
Vulnerary		D[82]
InflorescenceDecoctionNSC
R
G
V		[76]
NS: Not specified. Anatomical Therapeutical Chemical (ATC) categories are as follows. A: Alimentary tract and metabolism; C: Cardiovascular system; D: Dermatological; G: Genito-urinary system and sex hormones; L: Antineoplastic and immunomodulating agents; N: Nervous system; R: Respiratory system; V: Various [75]; STDs: Sexually transmitted diseases; Vet: Veterinary.
Table 6. Quinoa and Amaranth phytochemical composition.
Table 6. Quinoa and Amaranth phytochemical composition.
C. quinoaA. hybridus
Phenolic acids
Flavonoids
Terpenoids
Steroids
Alkaloids
Peptides		Phenolic acids
Flavonoids
Tannins
Steroids
Carotenoids
Table 7. Antimicrobial activity of compounds found in Quinoa.
Table 7. Antimicrobial activity of compounds found in Quinoa.
No.CompoundBiological Activity/ModelEffectMethodRef.
14-hydroxybenzoic acidStaphylococcus epidermidisIC50: 355 µg/mLPaper disc[99]
2Gallic acidPseudomonas aeruginosaMIC: 100 µg/mLMicrodilution[100]
3Protocatechuic acidYersinia enterocoliticaMIC: 2.5 mg/mLMicrodilution[101]
4p-coumaric acidListeria monocytogenesIC50: 373.4 μMSpot-test assay[102]
5Ferulic acidEscherichia coli
Pseudomonas aeruginosa		MIC: 100 µg/mLMicrodilution[100]
6KaempferolStaphylococcus aureusBacterial film formation inhibition: 64 μg/mL causes 80% inhibitionCrystal violet staining[103,104]
7MyricetinEscherichia coliMIC50: 142 μg/mLBroth microdilution[105]
8Oleanolic acidListeria monocytogenesMIC50: 16 μg/mLBroth microdilution[106]
Note: IC50: Half-maximal inhibitory concentration; MIC: Minimum inhibitory concentration.
Table 8. In vitro and in vivo anticancer studies of Chenopodium quinoa Willd and Amaranthus hybridus L. extracts and powders.
Table 8. In vitro and in vivo anticancer studies of Chenopodium quinoa Willd and Amaranthus hybridus L. extracts and powders.
Plant OrganExtractModelMethodEffect/MechanismRef.
In VitroIn VivoBiological Model
Chenopodium quinoa Willd
Colon
BSOn-hexanex HCT116 cellsHoechst and MTT staining647.4 µg/mL, apoptosis[120]
RSOn-hexanex HCT116 cellsHoechst and MTT staining381.3 µg/mL, apoptosis[120]
WSOn-hexanex HCT116 cellsHoechst and MTT staining281.9 µg/mL, apoptosis[120]
SeedEthanolx HCT116 cellsMTTIC50 110.68 µg/mL at 48 h[121]
SeedProteinx Caco-2HDAC1IC50 0.87–1.85 g/L[135]
SeedProtein xAOM/DSS-induced colorectal cancer in miceSymptoms/
SCFA production		Symptom mitigation/partially alleviated dysbiosis[136]
Liver
SeedPowderx HEPG2Cell lineIC50 14.6 µg/mL[122]
SeedPetroleum ether, ultrasound-assisted extractionx SMMC 7721MTT121.4 µg/mL (24 h) and 53.4 µg/mL (48 h), inhibition of cell proliferation[124]
Brain
SeedNSx U87 MgMTT50 ± 5.0 nM, cytotoxicity[123]
SeedNSx GBM NULUMTT6.6 ± 4.1 nM (24 h), 8.3 ± 1.6 (48 h), 2.3 ± 4.1 (72 h); cytotoxicity[123]
SeedNSx GBM ZARMTT3.4 ± 1.9 nM (24 h), 7.6 ± 2.7 nM (48 h), 3.3 ± 1.2 nM (72 h); cytotoxicity[123]
Breast
SeedPetroleum ether, ultrasound-assisted extractionx MCF-7MTT83.48 µg/mL (24 h) and 64.67 µg/mL (48 h), inhibition of cell proliferation[124]
Amarantus hybridus L.
LeavesAqueous xSodium arsenite-induced micronucleated polychromatic erythrocyte in Wistar albino ratsHematological tests1 mL of 0.2 g/mL for 14 days, antigenotoxicity[130]
Stem and leavesNSx Aflatoxin and fumonisin-induced genotoxicity in H4IIE-luc cellsMTT40 µg/mL, antigenotoxicity[131]
SeedMethanolic xMice treated with EAC cellsHemocytometer EAC cell count by trypan blue and DAPI staining25, 50 and 100 µg/mL/d for 6 days; inhibition of cell growth[108]
Notes: NS: Not specified; BSO: Black quinoa oil; RSO: Red quinoa oil; WSO: White quinoa oil; EAC: Ehrlich ascites carcinoma; HCT 116: Human colon cancer cell line; Caco-2: Human epithelial cancer cells; HEPG2: Human hepatoblastoma cell line; GMB: Primary glioblastoma; H4IIE-luc: Luciferase receptor rat hepatoma cell line; MCF-7: Human breast cancer cells; SMMC 7721: Human liver cancer cells; U87 Mg: Continuous glioblastoma cell line; DAPI: 4′ 6-diamidino-2-phenylindole; DMEM: Dulbecco’s Modified Eagle’s Medium; MTT: 3-(4,5-dimethyl-2-yl)-2,5-diphenyltetrazolium methyl bromide method; TMZ: Temozolomide (chemotherapeutic used in the treatment of glioblastoma); HDAC1: Histone deacetylase 1 inhibitory activity assay; AOM/DSS: Azoxymethane/dextran sulfate sodium; SCFA: Short-chain fatty acids.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Romero-Benavides, J.C.; Guaraca-Pino, E.; Duarte-Casar, R.; Rojas-Le-Fort, M.; Bailon-Moscoso, N. Chenopodium quinoa Willd. and Amaranthus hybridus L.: Ancestral Andean Food Security and Modern Anticancer and Antimicrobial Activity. Pharmaceuticals 2023, 16, 1728. https://doi.org/10.3390/ph16121728

AMA Style

Romero-Benavides JC, Guaraca-Pino E, Duarte-Casar R, Rojas-Le-Fort M, Bailon-Moscoso N. Chenopodium quinoa Willd. and Amaranthus hybridus L.: Ancestral Andean Food Security and Modern Anticancer and Antimicrobial Activity. Pharmaceuticals. 2023; 16(12):1728. https://doi.org/10.3390/ph16121728

Chicago/Turabian Style

Romero-Benavides, Juan Carlos, Evelyn Guaraca-Pino, Rodrigo Duarte-Casar, Marlene Rojas-Le-Fort, and Natalia Bailon-Moscoso. 2023. "Chenopodium quinoa Willd. and Amaranthus hybridus L.: Ancestral Andean Food Security and Modern Anticancer and Antimicrobial Activity" Pharmaceuticals 16, no. 12: 1728. https://doi.org/10.3390/ph16121728

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop