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REVIEW article

Front. Pharmacol., 23 April 2020
Sec. Ethnopharmacology
This article is part of the Research Topic Ethnopharmacology of Eastern European Countries View all 14 articles

Turning Meadow Weeds Into Valuable Species for the Romanian Ethnomedicine While Complying With the Environmentally Friendly Farming Requirements of the European Union’s Common Agricultural Policy

  • “Stejarul” Research Centre for Biological Sciences, National Institute of Research and Development for Biological Sciences, Piatra Neamt, Romania

The cross-compliance mechanism of the European Union (EU)'s common agricultural policy (CAP) makes the approval of the direct payments to the European farmers subject to compliance with the requirement to maintain the land in good agricultural and environmental condition. One of the obligations of the Romanian land owners and farmers is to avoid the installation of unwanted vegetation on their land plots. This vegetation is represented by some species of herbaceous or woody plants, annual or perennial, that spontaneously invade the agricultural lands, diminishing the production capacity of the cultivated plants. Included in this category are 10 meadow weeds, without fodder value or even toxic to animals: Arctium lappa L., Carduus nutans L., Conium maculatum L., Eryngium campestre L., Euphorbia cyparissias L., Pteridium aquilinum (L.) Kuhn, Rumex acetosella L., Veratrum album L., Xanthium spinosum L., and Xanthium strumarium L. Various and multiple uses in traditional medicine of these meadow weed species have been reported for Romania and other nine neighboring East European countries, i.e. Bosnia and Herzegovina, Bulgaria, Czech Republic, Estonia, Kosovo, Russia, Turkey, Serbia, and Ukraine. For A. lappa were recorded the highest number of ethnomedicinal uses, in the largest number of East European countries, including Romania. C. maculatum and V. album are not recommended for human consumption but can be further investigated as potential sources of pharmaceutically active compounds. Once removed by landowners and farmers from their land, the raw plant material of these 10 species become readily and easily available to the Romanian local communities and the industry of herbal food supplements, while the biodiversity of the agro-ecosystems is maintained.

Introduction

The European Union (EU)'s common agricultural policy (CAP) is one of the world's largest agricultural policies and the EU's longest-prevailing one (Pe'er et al., 2019). Besides producing food and stimulating rural community development, the CAP defines one more condition that allows farmers to fulfill their functions in society—environmentally sustainable farming—to produce food while simultaneously protecting nature and safeguarding biodiversity (European Commission, 2020a). Cross-compliance is a CAP's mechanism that links direct payments to compliance by farmers with basic standards concerning the environment, food safety, animal and plant health and animal welfare, as well as the requirement of maintaining land in good agricultural and environmental condition (GAEC). Evidence has shown that agriculture is the single largest cause of biodiversity loss but already nearly one-third of the world's farms have adopted more environmentally friendly practices while continuing to be productive (Pretty et al., 2018). In Europe, since 2005, all EU farmers receiving direct payments under CAP are subject to compulsory cross-compliance which is an important tool for integrating environmental requirements into the CAP (European Commission, 2020b). The good GAECs and the statutory management requirements (SMR), refer to a set of EU standards and requirements aiming at sustainable agriculture (European Parliament, 2013). In the area “Environment, climate change, good agricultural condition of land,” when referring to the issue of “Landscape, minimum level of maintenance,” GAEC 7 requires “Retention of landscape features, including where appropriate, hedges, ponds, ditches, trees in line, in group or isolated, field margins and terraces, and including a ban on cutting hedges and trees during the bird breeding and rearing season and, as an option, measures for avoiding invasive plant species” (European Parliament, 2013). After they are defined and detailed at national or regional level, all these standards are to be respected by all the European farmers receiving direct payments or some of the rural development payments.

Methods: Literature Search Strategy

We systematically searched four databases (Web of Science, PubMed, Scopus, and ScienceDirect) for relevant, peer reviewed publications, using a combination of relevant keywords and Boolean operators which included the name of the 10 plant species and of the Eastern European countries, with no other filters applied (in July 2019). The number of retrieved abstracts was below 10, irrespective of the species searched for. This result was somehow anticipated by the guest editors of the research topic when they expected that “ethnopharmacological research in this area is quite limited, many of the existing studies being published in national or local journals, thus being less visible to the scientific community.” To expand the literature search, Google Scholar database was interrogated, and all the retrieved publication was selected based in the information provided by their abstracts and subsequently by their full text version. Only peer-reviewed articles were included in our review. To access the literature published in the Romanian language, the online catalog of the County Library “G. T. Kirileanu” Neamt was searched using the eBibliophil search engine (https://bibgtkneamt.ebibliophil.ro). All the relevant specialty books retrieved were searched for the 10 plant species and if they contain any recommended use in ethnomedicine.

Selection criteria: all the publications referring to the 10 plant species and their use in the ethnomedicine of any of the Eastern European countries (from the former communist countries in the west till Russia, Ukraine and Turkey in the east) have been included in our literature review.

Romania's Provisions for Avoiding the Installation of Unwanted Vegetation on the Farming Land

Romania covers an area of 238,391 km² of which around 61% agricultural land (14.6 million ha) (64.2% arable land, 32.9% meadows and natural grasslands and 2.7% plantations of trees and vineyard), and 28.3% forests and other forestry vegetation lands. The Rural Development Programme (RDP) is outlining Romania's priorities for using the nearly € 9.5 billion of public money that is available for the CAP 2014–2020 (European Commission, 2015).

In agreement with the EU's regulations, Romania has defined three measures to be followed in order to implement the GAEC 7, one of which imposes that farmers have to prevent unwanted vegetation to install on the farming land, including on the uncultivated one. The Agency for Payments and Intervention in Agriculture (APIA) is the national authority responsible for coordinating the control activity on the cross-compliance norms within the schemes and support measures for the Romanian farmers (Ministry of Agriculture and Rural Development, 2015).

The details regarding the application of the measures of GAEC 7 have been modified along the years but its main objective was to maintain a minimum level of maintenance of agricultural land (regardless of the category of use, including land which is no longer used for production) by avoiding the installation of unwanted vegetation. In this context, the unwanted vegetation is represented by some species of herbaceous or woody plants, annual or perennial, that spontaneously invade the agricultural lands, diminishing the production capacity of the cultivated plants. Also included in this category are some meadow plant species, without fodder value or even toxic to animals.

The legal provisions recommend that the unwanted vegetation should not dominate the culture in more than 30% of the plot area, regardless of the land use category (arable land, permanent meadow, or permanent crops). However, when the percentage of weediness exceeds the threshold of 80% of the surface of the plot, the entire plot is considered ineligible and excluded from payment. Also, the uncultivated agricultural land, one or more years, on which the unwanted vegetation was installed on more than 80% of the area, is excluded from payment. This decision is taken after on-site inspections carried out by APIA representatives (Agency for Payments and Intervention in Agriculture, 2019b).

The Unwanted Meadow Weeds in Romania

The main weed species that make up the unwanted vegetation on meadows (plants without fodder value or toxic plants) are annual, biennial or perennial plants. The APIA has listed 10 biannual or perennial weeds, all to be removed by the Romanian land owners or farmers from the meadows for which direct payments (EU subsidies) are requested: Arctium lappa L., Carduus nutans L., Conium maculatum L., Eryngium campestre L., Euphorbia cyparissias L., Pteridium aquilinum (L.) Kuhn, Rumex acetosella L., Veratrum album L., Xanthium spinosum L., and Xanthium strumarium L. (Agency for Payments and Intervention in Agriculture, 2019b). The same regulating and control body has prepared and publicly released a guide for identifying these 10 species that represent unwanted vegetation growing on the meadows (Agency for Payments and Intervention in Agriculture, 2019a). For each of the 10 species, a detailed description of the plant (roots, stem, leaves, flowers, and seeds), seed dispersal mechanism, and the general ecology of the species is provided, visually supported by four to six pictures. All these details are meant to facilitate the on-the-field identification for removal by the interested individuals.

To achieve its final goal, i.e. the removal of these 10 species from the EU-subsidized fields, APIA should simultaneously act by stopping and reversing the continuous degradation of grasslands due to overgrazing, a consequence of the larger, and increasing, number of grazing animals, also receiving a per-capita EU subsidy from the same governmental body: APIA. Overgrazing leads to the invasion of ruderal plant species, later on categorized as “unwanted” weed species by APIA. From the phytosociological point of view, two of the 10 species, i.e. E. cyparissias and R. acetosella, are natural components of most of the grasslands in the vegetation classes Festuco–Brometea (E. cyparissias) and Molinio–Arrhenatheretea (R. acetosella) (Sanda et al., 2008; Chifu, 2014), and they were erroneously categorized as unwanted vegetation in APIA's guide (Agency for Payments and Intervention in Agriculture, 2019a). Moreover, some of the other 10 species are not the most common and widespread species of their genus in Romania, e.g. Carduus acanthoides invades many more hectares of degraded grasslands than C. nutans (Sarateanu et al., 2008). All the above considered, the APIA's documents with respect to the invasive and unwanted vegetation should be critically reviewed and updated for the future post-2020 CAP.

Phytochemical Constituents and Ethnomedicinal Uses of the Meadow Weeds

All 10 species have ethnomedicinal uses which were reported around the world, including in Romania and other neighboring Eastern European countries, some of them dating back for centuries or even millennia. Their traditional use as edible and medicinal species has triggered investigations on their phytochemical composition.

A. lappa L.—Greater Burdock, Asteraceae

A. lappa has been used therapeutically in Europe, North America and Asia for hundreds of years (Wang et al., 2019). A. lappa is used in Eastern European folk medicine as an adjuvant in diabetes therapy (European Medicine Agency, 2011; Tousch et al., 2014; Tabassum et al., 2019), to treat digestive, renal, lung, and skin affections, having also depurative, diuretic, and diaphoretic properties (European Medicine Agency, 2011). Traditionally, the roots, buds, and seeds serve as blood purifier, and have been used as remedy for rheumatism, scurvy, gravel, venereal disease, and sores (Di Novella et al., 2013). An improvement of oxidative stress and inflammatory status was observed in patients with knee osteoarthritis treated with A. lappa root tea (Maghsoumi-Norouzabad et al., 2016), as well as in treating inflammatory acne (Miglani and Manchanda, 2014). In Greece, A. lappa's root is used for musculoskeletal diseases, in particular against joint pains and rheumatism (Tsioutsiou et al., 2019). In Bosnia and Herzegovina this plant is used to treat skin conditions, to strengthen the hair root, against intestinal parasites, for dissolution of kidney stone, for improved urination, against diabetes and rabies, dog's bites, to release stomach gasses, against sexually transmitted diseases (STDs), and to treat facial nerve inflammation etc. (Redzic, 2010).

The main bioactive compounds identified in all parts of A. lappa are the lignans (arctigenin, artiin, matairesinol) and polyphenolic acids (caffeic acid derivatives) (Ferracane et al., 2010; da Silva et al., 2013; Edwards et al., 2015). These two groups possess high antioxidant activity (Liu et al., 2012). Arctigenin is reducing the inflammatory process through inhibiting iNOS expression and promoting cytokines (TNF-α and IL-6) productions (Zhao et al., 2009). In vitro studies show that lignans extracted from A. lappa have anti-proliferative effect against cancerous cells, inducing apoptosis and limiting migration of metastasis (Lou et al., 2017; Wang et al., 2019).

Several studies showed that the seeds are rich in caffeic acid, chlorogenic acid and cynarin, the leaves contain high amounts of phenolic acids, quercetin, quercitrin, luteolin, sesquiterpenes, and eudesmol, while the roots are rich in carbohydrates (including inulin up to 45%–50%, mucilage, pectin and sugars), arctic acid, polyacetylenes, arctiin, luteolin, quercetin rhamnoside (Ferracane et al., 2010; European Medicine Agency, 2011; Edwards et al., 2015), and caffeoylquinic acids derivatives (Tousch et al., 2014).

In Romanian ethnomedicine A. lappa is recommended for its detoxifying (due to the high fiber composition), hepatoprotective (due to caffeic acid derivatives), cholesterol lowering (reduces the absorption of cholesterol and lipids at intestine level), diuretic, antiinflammatory, antioxidative (due to caffeic acid derivatives), hypoglycemic (due to high innulin content) (Bojor and Pop, 2010), and antibiotic effects (Stanescu et al., 2014). This plant is recommended for hepatobiliary and liver protection, hypercholesterolemia, dermatitis, eczema, skin infection, hyperglycemia, cholelithiasis, oily and seborrheic skin, hair regrowth (Bojor and Alexan, 1984; Parvu, 2000; Ardelean et al., 2008; Mohan, 2008; Bojor and Pop, 2010), intoxications, flu, high blood pressure, hemorrhages (Parvu, 2000; Mohan, 2008), muscular atrophy, gout, enterocolitis (Mohan, 2008), herpes, dandruff (Parvu, 2000; Ardelean et al., 2008), cystitis (Bojor and Alexan, 1984), burns (Bojor, 2018), hepatitis, bronchitis, scurvy (Milica et al., 2012), corns, typhoid fever, heart pain, chest pain, rheumatism, STDs, skin rashes (Stanescu et al., 2014), epilepsy, arthritis, constipation, abdominal colic, hepatitis, and insect bites (Grigore and Grigore, 2007).

C. nutans L. —Musk Thistle, Asteraceae

C. nutans is used as dietary supplement (Isik and Yucel, 2017). In Turkish folk medicine, this species has been used as tonic to stimulate liver function, detoxifying herb and to ameliorate fever (Aktay et al., 2000). In Bulgaria, C. nutans is used for its antihemorroidal, cardiotonic and diuretic properties (Zheleva-Dimitrova et al., 2011).

The main biochemical compounds of musk thistle are the flavonoids (apigenin, luteolin, kempferol and derivatives, rutin, tilianin, and isorhamnetin), sterols and triterpenes (β-sitosterol acetate, sitosterol-O-xyloside, taraxasterol acetate), polyacetylenes (vinylpentacetylene), phenolic acids, and anthocyanins (Bain and Desrochers, 1988; Abdallah and Ramadan, 1989; Jordon-Thaden and Louda, 2003; Zhelev et al., 2013). Flavonoids represents an important class of compounds known to have a positive impact in ameliorating symptoms of cancer, cardiovascular disease, and neurodegenerative disorders (Spencer et al., 2004; Salvamani et al., 2014). In the last decade, studies on apigenin use as an adjuvant in cancer treatment had shown tremendous results, this plant originated flavone acting as a chemoprotective agent, inhibiting tumor development through inducing cycle arrest and apoptosis (Banerjee and Mandal, 2015; Kashyap et al., 2018).

In Romanian traditional medicine (TM) the C. nutans's seeds are used to prevent atherosclerosis, the flowers as febrifuge, blood purifier (Daraban et al., 2013) and used for treating polyarticular ankilosis, and myalgia, while the leaves are recommended for hypertension and liver diseases (Grigore and Grigore, 2007).

C. maculatum L.—Poison Hemlock, Apiaceae

C. maculatum is one of the most poisonous plants for laboratory animals, farm animals, and human beings, due to the presence of piperidine alkaloids in all its parts (Al-Snafi, 2016). Despite its poisonous nature, C. maculatum is included in several herbals as Succus conii, described as a narcotic, sedative, analgesic, spasmolytic, anti-aphrodisiac, and anti-cancer agent (Reynolds, 2005). C. maculatum extract is used as a traditional homeopathic remedy for cervix carcinoma (Mondal et al., 2014). This species has been used in ethnomedicine as an analgesic and anti-inflammatory agent (De Landoni and Conium maculatum, 1990; Arihan et al., 2009; Al-Snafi, 2016,; Madaan and Kumar, 2012), in Turkey to treat diabetes (Paksoy et al., 2016), and in Morocco as an alternative to treat typhoid fever and sterility, and also to ease labor (Kharchoufa et al., 2018). Externally, it has been used to treat herpes and swelled joints (Bloch, 2001). Some studies highlight the antispasmodic property of C. maculatum and it was reported to have a positive impact on patients with epilepsy, asthma, angina, rheumatism, and tetanus (Mitich, 1998; Hotti and Rischer, 2017).

The chemical composition of poison hemlock has been widely studied and the main toxic alkaloids are coniine and γ-coniceine identified in all plant parts, but mostly in roots and seeds, and they are also responsible for the sedative and anti-inflammatory properties of the species (Vetter, 2004; Panter et al., 2011; Cortinovis and Caloni, 2015; Al-Snafi, 2016; Kharchoufa et al., 2018). Besides alkaloids, C. maculatum is rich in flavonoids (anti-oxidative), coumarins (anti-microbial, anti-inflammatory), polyacetylenes, vitamins, and oils (Al-Snafi, 2016).

In Romanian ethnomedicine, C. maculatum was used as sedative (Bojor, 2018) and for reducing neuralgia (Ardelean et al., 2008; Bojor, 2018).

E. campestre L.—Field Eryngo, Apiaceae

E. campestre has been used in folk medicine (Zhang et al., 2008). In the European herbal medicine this plant was used as an infusion for the treatment of whooping cough, as well as in the treatment of kidney and urinary tract inflammations (Medbouhi et al., 2018). In Eastern European TM field eryngo roots and leaves are used for their anti-inflammatory, antiscorbutic, diaphoretic, antitussive, diuretic, expectorant, appetite-stimulant, and aphrodisiac properties, and to treat hemorrhoids, rheumatism, and infertility (Küpeli et al., 2006; Belda et al., 2013; Güneş et al., 2014; Conea et al., 2015; Kikowska et al., 2016; Soumia, 2018). In Turkey is used to treat intestinal disorders, flatulence, hepatitis, digestion disorders, and muscle pain (Akgul et al., 2018) but is also used fresh for human consumption (Demirci and Özkan, 2014). A study by Hawas et al., 2013 suggests its potential application in the treatment of Alzheimer's disease.

E. campestre represents an important source of multi-target antimicrobial essential oils, with spathulenol being the main chemical compound of the species (Erdem et al., 2015). Several studies showed that E. campestre is rich in flavonoids (quercetin glycosides, isorhamnetin glycosides, and myricetin glycosides), phenolic acids, acetylenes, saponins, steroids, terpenoids, and coumarins (Abou El-Kassem et al., 2013; Marčetić et al., 2014; Matejić et al., 2018; Soumia, 2018). The flavonoids and phenolic compounds contribute to the antioxidant properties of the plant (Küpeli et al., 2006; Matejić et al., 2018; Soumia, 2018).

In Romanian ethnomedicine E. campestre is recommended for its cholagogue, diuretic, appetite-stimulant (Craciun et al., 1976; Grigore and Grigore, 2007), expectorant, antitussive, bronchial antiseptic, antispasmodic, antibiotic, hypotensive, and carminative effects (Milica et al., 2012), and is used for treating gallbladder, urinary retention, gonococcal urethritis, ascites, amenorrhea, scurvy, tuberculosis, acne, oliguria, colicky nephritis, seborrheic dermatitis, leg edema (Grigore and Grigore, 2007), amenorrhea, constipation, tooth pain, periodontitis, tooth decay (Milica et al., 2012), and nephrolithiasis (Ardelean et al., 2008). In the Romanian rural areas is used as ingredient in various dishes, especially in soups (Parvu, 2000).

E. cyparissias L.—Cypress Spurge, Euphorbiaceae

The leaves of E. cyparissias are used as anti-warts (Pieroni and Vandebroek, 2007). The flowers, stems, and leaves of cypress spurge are used in folk medicine in the treatment of dermatological diseases (psoriasis, eczema), respiratory diseases (asthma, bronchitis, chest congestion, throat spasm), hay fever, and against tumor development (Özbilgin et al., 2012; Stanković and Zlatić, 2014). Its seed oil is purgative. In the past, vapor of the chloroform extract was used as anesthetic agent. It is recommended for insomnia and ear constipation. Its condensed milky sap is one of the components of “emplastrum cantharides” (blister bug plaster) which is used principally to relieve deep-seated inflammation and to promote the absorption of effusions (Papp, 2004).

The whole plant has antioxidant properties given by the high amount of secondary metabolites, mainly isoprenoids (diterpenoids, triterpenoids, sesquiterpenoids—elemene and caryophyllene), phenolic acids, and flavonoids (Hemmer and Gülz, 1989; Özbilgin et al., 2012; Stanković and Zlatić, 2014). Two new diterpenoids have been identified in extracts of E. cyparissias (i.e., cyparissin A and B) that exhibit important activity against cancerous cell lines in in-vitro studies (Lanzotti et al., 2015).

In Romanian ethnomedicine E. cyparissias is recommended for its purging, emetic (Craciun et al., 1976), antispasmodic, sedative, antifungal, anti-rheumatic, revulsive, and febrifuge effects (Milica et al., 2012) and is used for treating warts, heir loss and sciatic neuralgia (Grigore and Grigore, 2007), gastric distress, constipation, stomach pains, intestinal worms, emphysema, pleuritis, hay fever, tuberculosis, pharyngitis, mange, eczemas, arthritis, ringworm, anthrax, impetigo, nail mycosis, tooth pain, and freckles (Milica et al., 2012).

P. aquilinum (L.) Kuhn—Bracken Fern, Polypodiaceae

Dioscorides (ca. 50 AD) in his de Materia Medica referred to several ferns, including P. aquilinum, as having medicinal values. P. aquilinum is thought to be a fern with potent anti-cancer properties. In India, decoctions from the rhizomes of P. aquilinum are drunk as an herbal tea (Baskaran et al., 2018). Dried rhizomes mixed with milk are used to relieve diabetic disorders, and tender fronds are used as vegetables (Baskaran et al., 2018). Moreover, the strong rhizomes of plant have been used directly as a food or as an ingredient of bread (by Australian, British, French, Japanese populations or by Lapp and Siberian cultures) (Vetter, 2010). It is the most common edible pteridophyte in sub-Saharan Africa, used as human food in Angola, Cameroon, DRC, Gabon, Madagascar, Nigeria, and South Africa (Maroyi, 2014).

The high concentration of phenol, flavonoid, and terpenoid compounds gives to bracken fern extracts antioxidant properties and antimicrobial activity, justifying its traditional use to treat skin diseases and gastrointestinal disorders (May, 1978; Mannan et al., 2008; Piluzza and Bullitta, 2011; Kardong et al., 2013). The presence of tannins, cardiac glycosides, anthraquinone, and cyanogenic glycosides in this species may have a negative impact on liver function (Hassan et al., 2007) and vitamin B1 metabolism (Fenwick, 1989; Vetter, 2010).

R. acetosella L.—Red Sorrel, Polygonaceae

In TM the leaves of R. acetosella are used by the native populations of North America as treatment for warts and bruises. The aerial parts contribute to amelioration of diarrhea and stomach disorders in North America and Hungary, while seeds are used to treat diarrhea and dysentery in Hungary (Chevalier, 1996; Shale et al., 1999; Foster et al., 2000; Wegiera et al., 2007; Vasas et al., 2015). An ethnobotanical survey of medicinal plants used in Turkey revealed that leaves of R. acetosella are used traditionally as an analgesic and diuretic (Cakilcioglu and Turkoglu, 2010). In Iran, R. acetosella is widely used by traditional healers for the treatment of jaundice and fever (Amiri et al., 2014). In Poland, this species is still in use today as potherb (Łuczaj and Szymański, 2007).

The main chemical compounds in the genus Rumex are antraquinones (emodin, physcion, and chrysophanol in fruits and leaves, and sennoside A in fruits and roots), nepodin, and flavanoids (quercetin-3-O-glucoside) with important antioxidant activity, while the stilbenoids demonstrated to have a positive impact in cancer therapy and inflammatory diseases (Wegiera et al., 2007; Vasas et al., 2015).

In Romanian ethnomedicine R. acetosella is recommended for its digestive, stomachic, laxative, cleansing, antidiarrheal, cholagogue, diuretic, emmenagogue, anthelmintic, astringent, appetite-stimulant, nutritious, anti-anemic, and antiscorbutic properties (Milica et al., 2012). This plant was recommended for treating paralysis (Craciun et al., 1976), hepatitis, jaundice, cholelithiasis, constipation, pulmonary illnesses, asthma, insect bites, gout, leucorrhea, nephritis, wounds, acne, boils, ringworms, cancerous ulcerations, and fever and as mineralizing treatment and for blood purification in the spring (Milica et al., 2012).

V. album L.—White Hellebore, Melanthiaceae

V. album has a long history of medicinal use, dating back as far as Hippocrates in which dilutions of the plant are prescribed to produce upward purging. Through the 1700s, preparations of V. album root and rhizomes were used medicinally in Europe primarily for their emetic properties (Chandler and McDougal, 2014). In the folk medicine V. album is used to treat rheumatism, toothache, gout, herpes, trigeminal neuralgia, and catarrh, and as an hypotensive agent (Furbee, 2009; Ujváry, 2010; Wiart, 2012; Roberts and Wink, 2013).

The medicinal, and the toxic properties of white hellebore are given by the presence of steroidal alkaloids including proveratrine, cevadine, protoveratrine, jervine, veratramine, and veratridine, the last being the most poisonous of all. Some of the symptoms of intoxication with white hellebore are hypotension, bradycardia, and paralysis (Furbee, 2009). Similar to C. maculatum, the alkaloids presence in all plant parts gives the species sedative and anti-inflammatory properties, antihypertensive activity being also described, especially linked to the presence of protoveratrine A and B (Krayer and Meilman, 1977).

In the Romanian ethnomedicine V. album is used for its neuro-sedative (Craciun et al., 1976; Parvu, 2000; Ardelean et al., 2008), hypotensive, narcotic, hypnotic, antipyretic (Parvu, 2000), anthelmintic, and insecticidal effects (Milica et al., 2012). The plant is used for treating malignant hypertension, hypertensive crisis, eclampsia, fever, eczemas, mange, itchy skin (Parvu, 2000), rheumatism, gout, eczema (Ardelean et al., 2008; Milica et al., 2012), pneumonia, whooping cough, intermittent fever, mental illnesses, psychiatric disorders, mania, mange, pruritus, psoriasis, and herpes zoster (Milica et al., 2012).

X. spinosum L.—Bathurst Burr, Asteraceae

In ethnomedicine X. spinosum is used in renal disorders, for its antibacterial, antifungal, and anthelminthic properties; calming influence; wound healing properties; and the efficacy of infusions in treating benign prostate hyperplasia (Domokos et al., 2016; Aldibekova et al., 2018). It was used against rabies, to relieve chronic fevers, to abate diabetes effects, even to stimulate saliva production for its diuretic effect (Andreani et al., 2017) and “it exhibits” noticeable antioxidant activity (Aldibekova et al., 2018). In Pakistani local communities the leaves and fruits are reported to be diaphoretic, diuretic, and sedative and used for hydrophobia while the infusion of root is emetic (Aziz et al., 2018).

The main chemical compounds are polyphenols, flavones, diterpenes, sesquiterpene lactones (xanthatin), phytosterols (Domokos et al., 2016), tannins, and essential oils (Aldibekova et al., 2018). It has been showed that xanthatin can inhibit the growth of Gram positive bacteria (Staphylococcus aureus and Bacillus cereus) and fungi (Colletotrichum gloesporoides and Trichothecium roseum) (Ginesta Peris et al., 1994). In vitro and in vivo studies showed that xanthatin and xanthinosin have chemopreventive properties, inhibiting tumor cells proliferation (Ramírez-Erosa et al., 2007; Romero et al., 2015). The therapeutic properties of xanthatin can be extended also to antiviral (herpes simplex virus, feline corona virus, influenza A H1N1 and A H3N2, influenza B, repvirus, respiratory syncytial virus etc.) and anti-angiogenic activities (Romero et al., 2015).

In Romanian ethnomedicine X. spinosum is recommended for its anti-inflammatory, diuretic, diaphoretic, and disinfectant effects (Bojor and Pop, 2010). This plant is recommended for treating polyuria, prostatitis, selective electrolyte retention (K+ and Mg2+) in the blood serum, protection of the myocardium, prostate adenoma, nephrolithiasis (Bojor and Pop, 2010), rabies, and hyperthyroidism (Ardelean et al., 2008).

X. strumarium L.—Common Cocklebur, Asteraceae

Although the fruit is the predominant part of X. strumarium used in folk medicine (Fan et al., 2019), the leaves and roots have been used for their diaphoretic, diuretic, emollient, appetite-stimulant, laxative, antirheumatic, antisyphilitic, anodyne, and sedative properties (Chopra et al., 1956). Traditionally, this species is also used as febrifuge drug and as an immunostimulant, against malaria, as well as dysentery cure, astringent, sedative, analgesic, against leucorrhea and urinary diseases, eczema and skin disease, bleeding, insect bite, to treat boils and pimples, against smallpox and stomach diseases, earache and strumous disease, leprosy, headache, and fever (Katewa, 2008; Kozuharova et al., 2019). In Yemen and Russia, X. strumarium is used as a medicine soothing illness, hemolytic, reducing temperature, skin diseases, antimicrobial, for ulcers, and antifungal (Aldibekova et al., 2018).

In common cocklebur the aerial parts' main compounds are the sesquiterpene lactones (guianolides, elemanolides, germacranolides, xanthinium, xanthumin, xanthatin) with important anti-inflammatory, antiviral, antitumor, and antimicrobial properties (Kamboj and Saluja, 2010; Fan et al., 2019).

A series of compounds with pharmacological importance have been identified in all parts of X. strumarium: glycosides (xanthostrumarin, atractyloside, carboxyatractyloside, the last being also the most toxic compound) (Kamboj and Saluja, 2010), phytosterols (xanthanol, isoxanthonol, xanthinosin, 4-oxo-bedfordia acid) (Olivaro et al., 2016), caffeoylquinic acid, thiazinodine, diacetyl xanthumin (antifungal compound), linoleic acid, and triterpenoids (botulin, betulinic acid, erythrodiol, lupeol acetate, oleanolic acid, amyrin) (Kamboj and Saluja, 2010; Yadav et al., 2015; Fan et al., 2019). In n-butanol fraction of the ethanolic extract of X. strumarium has been proven to possess the highest analgesic and anti-inflammatory activity (Han et al., 2007).

In Romanian ethnomedicine, the whole X. strumarium plant is recommended for treating diabetes (Grigore and Grigore, 2007).

Recommended Ethnomedicinal Uses of Some Meadow Weeds in Romania and Other Neighboring East European Countries

The weed species growing on the Romanian meadows, which have to be removed by land owners or farmers if public subsidies under EU's CAP are expected, have multiple and documented uses in TM. Yet, two of these species, C. maculatum and V. album are very toxic and they are not recommended for human use, but they can be potential valuable sources of pharmaceutically active compounds.

For the majority of these meadow species have been reported details of their recommended ethnomedicinal uses in Romania (Table 1). On the Romanian market many commercial herbal products that have ingredients derived from the meadow weeds are on sale, including through e-commerce (Supplementary Table 1).

TABLE 1
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Table 1 Ethnomedicinal uses of the meadow weeds in Romania.

The same meadow weeds have been used in the TM (Table 2) in many neighboring European Eastern countries (Supplementary Figure 1).

TABLE 2
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Table 2 Ethnomedicinal use of the meadow weeds in neighboring East European countries.

From all 10 species, A. lappa has recorded the highest number of ethnomedicinal recommended uses, both in Romania and neighboring East European countries. On the contrary, we were not able to find any documented use of P. aquilinum in Romanian ethnomedicine, but in Kosovo its leaves decoction is used as antibacterial and diuretic treatment (Mustafa et al., 2012).

Medicinal plants have historically proven their value as a source of molecules with therapeutic potential, and still represent an important pool for the identification of novel drug leads. Particularly relevant examples of plant-derived natural compounds that have become indispensable for modern pharmacotherapy are the anti-cancer agents, e.g., paclitaxel and its derivatives from Taxus species, vincristine and vinblastine from Catharanthus roseus (L.) G. Don, and camptothecin and its analogs initially discovered in Camptotheca acuminata Decne. (Atanasov et al., 2015). There were an estimated 18.1 million new cases of cancer and 9.6 million deaths from cancer worldwide in 2018 from which in Romania alone been registered 83,461 new cases and 50,902 deaths (Ferlay et al., 2019). As a highly relevant aspect related to human health, the reviewed peer-reviewed publications reported the use of seven out of the 10 species, i.e. A. lappa, C. maculatum, E. cyparissias, P. aquilinum, R. acetosella, X. spinosum, and X. strumarium, as treatments in ethnomedicine for different types of cancer (e.g. prostatic, pulmonary, endometrial), cancerous ulcerations and tumor development in Eastern European countries, suggesting further investigations. From all the above-mentioned species, only three of them have been reported in Romanian for treatment of cancerous ulcerations (R. acetosella) and prostate cancer (X. spinosum, and X. strumarium). At least one commercial herbal product containing both herba Xanthii and herba Xanthii spinosi is sold on the Romanian market.

The Raw Plant Material and Its Influence on the Authenticity of the Derived Herbal Products

The herbal products, sold as medicines or food supplements, represent a core part of the TM which has been has recognized by the World Health Organization (WHO) as a growing and expanding global phenomenon (World Health Organization, 2013). The rapidly expanding global market is expected to reach US$ 115 billion in 2020 (Raclariu et al., 2018) while the trade of medicinal plants will grow at the rate of 15%–25% annually and will reach US$ 5 trillion by 2050 (Booker et al., 2012). The increasing demand for herbals and the limited supply of many species that are harvested from the wild (Coghlan et al., 2015) is stimulating the economically-motivated adulteration (EMA) (Simmler et al., 2018). It was recently reported that 27% of almost 6,000 commercial herbal products sold in 37 countries were found to be adulterated, while in Europe almost half (47%) were adulterated. In Romania, 94% of the herbal products analyzed (n = 70) were reported to be adulterated, when their composition was compared with the labeled ingredient species (Ichim, 2019). The availability of new plant biomass while is removed from the Romanian meadows by its owners or farmers can become readily available to the interested users and could reduce the pressure on the existing sources of raw materials. Moreover, because only selected species have to be searched, identified and removed, a supplementary quality check is added to the plant raw material, before being further used or processed, which represents additional benefits for the quality of the herbal products and their benefits for the human health.

Conclusion

The Romanian landowners or farmers have to remove from their meadows 10 plant species without fodder value or toxic to animals as a compulsory condition to receive the public subsidies under EU's CAP. For these unwanted meadow weeds have reported many and various uses in Romanian ethnomedicine, as well as in other nine neighboring East European countries. Some of the ethnopharmacological uses are highly relevant for the modern medicine, supporting the use of the removed biomass from the meadows as additional or alternative source of pharmacologically active ingredients. The local communities and the industry of herbal food supplements can take immediate advantage from these raw plant materials, readily and easily available, while assuring their environmentally-friendly, sustainable, and supportive of local traditions and commercial use.

Author Contributions

MI conceived and supervised the research. MI and EG wrote the manuscript. MI and EG read and approved the submitted manuscript.

Funding

This work was supported by a grant of the Ministry of Research and Innovation through Program 1–Development of the National R&D System, Subprogram 1.2–Institutional Performance–Projects for Excellence Financing in RDI, contract no. 22PFE/2018. This publication was supported by the National Core Program funded by the Romanian Ministry of Research and Innovation, project number 25N/11.02.2019, BIODIVERS 19270401.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

The assistance of the personnel of the County Library “G. T. Kirileanu” Neamt is kindly acknowledged. We thank the reviewers for their careful reading of our manuscript and their insightful comments and suggestions.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fphar.2020.00529/full#supplementary-material

References

Abdallah, O., Ramadan, M. (1989). Phytochemical study of Carduus nutans L. (Asteraceae). Bull. Pharm. Sci. Assiut Univ. 18, 69–76.

Google Scholar

Abou El-Kassem, L., Hawas, U., Awad, H., Taie, H. (2013). Flavonoids from the aerial parts of Eryngium campestre L. with antioxidant and anti-Alzheimer activities. Planta Med. 79, PJ2. doi: 10.1055/s-0033-1352206

CrossRef Full Text | Google Scholar

Agency for Payments and Intervention in Agriculture (2019a). Ghid pentru identificarea principalelor specii de buruieni care alcatuiesc “vegetatia nedorita” pe pajisti [Guide to identify the main weed species which make up the “unwanted vegetation” on the meadows].

Google Scholar

Agency for Payments and Intervention in Agriculture (2019b). Ghidul fermierului privind ecoconditionalitatea [The farmer's guide regarding the cross-compliance]. Bucharest.

Google Scholar

Akgul, A., Akgul, A., Senol, S. G., Yildirim, H., Secmen, O., Dogan, Y. (2018). An ethnobotanical study in Midyat (Turkey), a city on the silk road where cultures meet. J. Ethnobiol. Ethnomed. 14, 12. doi: 10.1186/s13002-017-0201-8

PubMed Abstract | CrossRef Full Text | Google Scholar

Aktay, G., Deliorman, D., Ergun, E., Ergun, F., Yeşilada, E., Çevik, C. (2000). Hepatoprotective effects of Turkish folk remedies on experimental liver injury. J. Ethnopharmacol. 73, 121–129. doi: 10.1016/S0378-8741(00)00286-5

PubMed Abstract | CrossRef Full Text | Google Scholar

Aldibekova, D. A., Kizaibek, M., Aisijiang, M., Dyuskaliyeva, G., Taldau, A., Erkinbek, M. (2018). Morphology, anatomy, chlorogenic acid content and antioxidant capacity of Xanthium strumarium L. and Xanthium spinosum L. Online J. Biol. Sci. 18, 237–246. doi: 10.3844/ojbsci.2018.237.246

CrossRef Full Text | Google Scholar

Al-Snafi, A. E. (2016). Pharmacology and toxicology of Conium maculatum - A review. Pharmaceut. Chem. J. 3, 136–142.

Google Scholar

Altundag, E., Ozturk, M. (2011). Ethnomedicinal studies on the plant resources of east Anatolia, Turkey. Proc. Soc. Behav. Sci. 19, 756–777. doi: 10.1016/j.sbspro.2011.05.195

CrossRef Full Text | Google Scholar

Amiri, M. S., Joharchi, M. R., Taghavizadeh Yazdi, M. E. (2014). Ethno-medicinal plants used to cure jaundice by traditional healers of Mashhad, Iran. Iranian J. Pharmaceut. Res. 13, 157–162. doi: 10.22037/ijpr.2014.1445

CrossRef Full Text | Google Scholar

Andreani, S., Paolini, J., Costa, J., Muselli, A. (2017). Chemical composition of essential oils of Xanthium spinosum L., an invasive species of Corsica. Chem. Biodiversity 14, e1600148. doi: 10.1002/cbdv.201600148

CrossRef Full Text | Google Scholar

Ardelean, A., Mohan, G., Mohan, D. A. (2008). Flora medicinala a Romaniei [Romania’s medicinal flora] (Bucharest: ALL Publishing House).

Google Scholar

Arihan, O., Boz, M., Iskit, A. B., Ilhan, M. (2009). Antinociceptive activity of coniine in mice. J. Ethnopharmacol. 125, 274–278. doi: 10.1016/j.jep.2009.06.032

PubMed Abstract | CrossRef Full Text | Google Scholar

Atanasov, A. G., Waltenberger, B., Pferschy-Wenzig, E. M., Linder, T., Wawrosch, C., Uhrin, P., et al. (2015). Discovery and resupply of pharmacologically active plant-derived natural products: A review. Biotechnol. Adv. 33, 1582–1614. doi: 10.1016/j.biotechadv.2015.08.001

PubMed Abstract | CrossRef Full Text | Google Scholar

Aziz, M. A., Adnan, M., Khan, A. H., Shahat, A. A., Al-Said, M. S., Ullah, R. (2018). Traditional uses of medicinal plants practiced by the indigenous communities at Mohmand Agency, FATA, Pakistan. J. Ethnobiol. Ethnomed. 14, 2. doi: 10.1186/s13002-017-0204-5

PubMed Abstract | CrossRef Full Text | Google Scholar

Bain, J. F., Desrochers, A. M. (1988). Flavonoids of Carduus nutans and C. acanthoides. Biochem. Systematics Ecol. 16, 265–268. doi: 10.1016/0305-1978(88)90005-1

CrossRef Full Text | Google Scholar

Banerjee, K., Mandal, M. (2015). Oxidative stress triggered by naturally occurring flavone apigenin results in senescence and chemotherapeutic effect in human colorectal cancer cells. Redox Biol. 5, 153–162. doi: 10.1016/j.redox.2015.04.009

PubMed Abstract | CrossRef Full Text | Google Scholar

Baskaran, X.-R., Geo Vigila, A.-V., Zhang, S.-Z., Feng, S.-X., Liao, W-b (2018). A review of the use of pteridophytes for treating human ailments. J. Zhejiang University Sci. B 19, 85–119. doi: 10.1631/jzus.B1600344

CrossRef Full Text | Google Scholar

Belda, A., Zaragozí, B., Belda, I., Martínez, J., Seva, E. (2013). Traditional knowledge of medicinal plants in the Serra de Mariola Natural Park, South-Eastern Spain. Afr. J. Tradit. Complementary Altern. Med. 10, 299–309. doi: 10.4314/ajtcam.v10i2.15

CrossRef Full Text | Google Scholar

Bloch, E. (2001). Hemlock poisoning and the death of Socrates: Did Plato tell the truth? Plato J. 1, 255–278. doi: 10.14195/2183-4105_1_1

CrossRef Full Text | Google Scholar

Bojor, O., Alexan, M. (1984). Plantele medicinale si aromatice de la A la Z [The medicinal and aromatic plants from A to Z] (Bucharest: Recoop Publishing House).

Google Scholar

Bojor, O., Pop, M. (2010). Fitoterapia in folosul tuturor [Phytotherapy for the benefit of all] (Bucharest: Medical Publishing House).

Google Scholar

Bojor, O. (2018). Plantele medicinale si aromatice de la A la Z [The medicinal and aromatic plants from A to Z] (Bucharest: Dharana Publishing House).

Google Scholar

Booker, A., Johnston, D., Heinrich, M. (2012). Value chains of herbal medicines - Research needs and key challenges in the context of ethnopharmacology. J. Ethnopharmacol. 140, 624–633. doi: 10.1016/j.jep.2012.01.039

PubMed Abstract | CrossRef Full Text | Google Scholar

Bulut, G., Zahid Bozkurt, M., Tuzlacı, E. (2017). The preliminary ethnobotanical study of medicinal plants in Uşak (Turkey). Marmara Pharmaceut. J. 21, 305–310. doi: 10.12991/marupj.300795

CrossRef Full Text | Google Scholar

Butura, V. (1979). Enciclopedie de etnobotanica romaneasca [Romanian ethnobotany encyclopedia] (Bucharest: Scientific and Encyclopedic Publishing House).

Google Scholar

Cakilcioglu, U., Turkoglu, I. (2010). An ethnobotanical survey of medicinal plants in Sivrice (Elaziĝ-Turkey). J. Ethnopharmacol. 132, 165–175. doi: 10.1016/j.jep.2010.08.017

PubMed Abstract | CrossRef Full Text | Google Scholar

Chandler, C. M., McDougal, O. M. (2014). Medicinal history of North American Veratrum. Phytochem. Rev. 13, 671–694. doi: 10.1007/s11101-013-9328-y

PubMed Abstract | CrossRef Full Text | Google Scholar

Chevalier, A. (1996). The encyclopedia of medicinal plants (New York: DK Pub).

Google Scholar

Chifu, T. (2014). Diversitatea fitosociologica a vegetatiei Romaniei [Phytosociological diversity of Romania’s vegetation] (vol.I-III) (Iasi, Romania: Editura Institutul European Iasi).

Google Scholar

Chopra, R. N., Nayar, S. L., Chopra, I. C. (1956). Glossary of Indian medicinal plants (New Delhi: Council of Scientific and Industrial Research).

Google Scholar

Coghlan, M. L., Maker, G., Crighton, E., Haile, J., Murray, D. C., White, N. E., et al. (2015). Combined DNA, toxicological and heavy metal analyses provides an auditing toolkit to improve pharmacovigilance of traditional Chinese medicine (TCM). Sci. Rep. 5, 17475. doi: 10.1038/srep17475

PubMed Abstract | CrossRef Full Text | Google Scholar

Conea, S., Pârvu, A. E., Taulescu, M. A., Vlase, L. (2015). Effects of Eryngium planum and Eryngium campestre extracts on ligature-induced rat periodontitis. Digest J. Nanomat. Biostructures 10, 693–704.

Google Scholar

Cortinovis, C., Caloni, F. (2015). Alkaloid-containing plants poisonous to cattle and horses in Europe. Toxins 7, 5301–5307. doi: 10.3390/toxins7124884

PubMed Abstract | CrossRef Full Text | Google Scholar

Craciun, F., Bojor, O., Alexan, M. (1976). Farmacia naturii [Nature’s pharmacy] (vol. I) (Bucharest: Ceres Publishing House).

Google Scholar

da Silva, L. M., Allemand, A., Mendes, D. A. G. B., Dos Santos, A. C., André, E., de Souza, L. M., et al. (2013). Ethanolic extract of roots from Arctium lappa L. accelerates the healing of acetic acid-induced gastric ulcer in rats: Involvement of the antioxidant system. Food Chem. Toxicol. 51, 179–187. doi: 10.1016/j.fct.2012.09.026

PubMed Abstract | CrossRef Full Text | Google Scholar

Daraban, I. N., Arsene, G. G., Turcus, V., Ardelean, A. (2013). Assessment on bioeconomical potential for medicinal plants in salty meadows from the aradului plain (W. Romania). Studia Universitatis Vasile Goldis Arad Seria Stiintele Vietii 23, 71–78.

Google Scholar

De Landoni, J. H., Conium maculatum, L. (1990). (PIM 144). Available at: http://www.inchem.org/documents/pims/plant/conium.htm [Accessed March 5, 2020].

Google Scholar

Demirci, S., Özkan, E. E. (2014). Ethnobotanical studies of some Apiaceae plants in Kahramanmaras and a review of their phytochemical studies. Istanbul Ecz. Fak. Derg. 44, 241–250.

Google Scholar

Di Novella, R., Di Novella, N., De Martino, L., Mancini, E., De Feo, V. (2013). Traditional plant use in the National Park of Cilento and Vallo di Diano, Campania, Southern, Italy. J. Ethnopharmacol. 145, 328–342. doi: 10.1016/j.jep.2012.10.065

PubMed Abstract | CrossRef Full Text | Google Scholar

Domokos, E., Kursinszki, L., Kelemen, H., Varga, E. (2016). [Phytopharmacological review of bathurst burr (Xanthium spinosum L.)]. Acta Pharm. Hungarica 86, 35–40.

Google Scholar

Edwards, S. E., Rocha, I., Williamson, E. M., Heinrich, M. (2015). Phytopharmacy: An evidence-based guide to herbal medical products (Hoboken, NJ: Wiley-Blackwell).

Google Scholar

Erdem, S. A., Nabavi, S. F., Orhan, I. E., Daglia, M., Izadi, M., Nabavi, S. M. (2015). Blessings in disguise: A review of phytochemical composition and antimicrobial activity of plants belonging to the genus Eryngium. DARU J. Pharmaceut. Sci. 23, 53 doi: 10.1186/s40199-015-0136-3

CrossRef Full Text | Google Scholar

European Commission (2015). Factsheet on 2014-2020 Rural Development Programme for Romania.

Google Scholar

European Commission (2020a). Common agricultural policy.

Google Scholar

European Commission (2020b). Cross-compliance.

Google Scholar

European Medicine Agency (2011). Assessment report on Arctium lappa L., radix. London.

Google Scholar

European Parliament (2013). Regulation (EU) No 1306/2013 of the European Parliament and of the Council of 17 December 2013 on the financing, management and monitoring of the common agricultural policy.

Google Scholar

Fan, W., Fan, L., Peng, C., Zhang, Q., Wang, L., Li, L., et al. (2019). Traditional uses, botany, phytochemistry, pharmacology, pharmacokinetics and toxicology of xanthium strumarium L.: A review. Molecules 24 (2), 359. doi: 10.3390/molecules24020359

CrossRef Full Text | Google Scholar

Fenwick, G. R. (1989). Bracken (Pteridium aquilinum) - toxic effects and toxic constituents. J. Sci. Food Agric. 46, 147–173. doi: 10.1002/jsfa.2740460204

CrossRef Full Text | Google Scholar

Ferlay, J., Colombet, M., Soerjomataram, I., Mathers, C., Parkin, D. M., Piñeros, M., et al. (2019). Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. Int. J. Cancer 144, 1941–1953. doi: 10.1002/ijc.31937

PubMed Abstract | CrossRef Full Text | Google Scholar

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. J. Pharmaceut. Biomed. Anal. 51, 399–404. doi: 10.1016/j.jpba.2009.03.018

CrossRef Full Text | Google Scholar

Fierascu, R. C., Fierascu, I., Ortan, A., Avramescu, S. M., Dinu-Pirvu, C. E., Ionescu, D. (2017). “Romanian aromatic and medicinal plants: From tradition to science,” in Aromatic and Medicinal Plants - Back to Nature (London: InTech), 149–173. doi: 10.5772/66513

CrossRef Full Text | Google Scholar

Foster, S., Duke, J. A., Foster, S. (2000). A field guide to medicinal plants and herbs of eastern and central North America (Boston: Houghton Mifflin Co).

Google Scholar

Furbee, B. (2009). “Neurotoxic plants,” in Clinical Neurotoxicology: Syndromes, Substances, Environments (Elsevier Inc.), 523–542. doi: 10.1016/B978-032305260-3.50053-8

CrossRef Full Text | Google Scholar

Güneş, M. G., İşgör, B. S., İşgör, Y. G., Shomali Moghaddam, N., Geven, F., Yildirim, Ö. (2014). The effects of Eryngium campestre extracts on glutathione-S-transferase, glutathione peroxidase and catalase enzyme activities. Turk J. Pharm. Sci. 11, 339–346.

Google Scholar

Gilca, M., Tiplica, G. S., Salavastru, C. M. (2018). Traditional and ethnobotanical dermatology practices in Romania and other Eastern European countries. Clinics Dermatol. 36, 338–352. doi: 10.1016/j.clindermatol.2018.03.008

CrossRef Full Text | Google Scholar

Ginesta Peris, E., Garcia Breijo, F. J., Primo Yúfera, E. (1994). Antimicrobial activity of xanthatin from Xanthium spinosum L. Lett. Appl. Microbiol. 18, 206–208. doi: 10.1111/j.1472-765X.1994.tb00848.x

CrossRef Full Text | Google Scholar

Grigore, G., Grigore, C. (2007). Ghidul plantelor medicinale si al bolilor tratate cu plante [Guide to the medicinal plants and plant treated-diseases] (Bucharest: BIC ALL Publishing House).

Google Scholar

Han, T., Li, H. L., Zhang, Q. Y., Han, P., Zheng, H. C., Rahman, K., et al. (2007). Bioactivity-guided fractionation for anti-inflammatory and analgesic properties and constituents of Xanthium strumarium L. Phytomedicine 14, 825–829. doi: 10.1016/j.phymed.2007.01.010

PubMed Abstract | CrossRef Full Text | Google Scholar

Hassan, S. W., Umar, R. A., Dabai, Y. U., Ebbo, A. A., Faruk, U. Z. (2007). Antibacterial, phytochemical and toxicity studies of Pteridium aquilinum L. (Dennstaedtiaceae) in rabbits. J. Pharmacol. Toxicol. 2, 168–175. doi: 10.3923/jpt.2007.168.175

CrossRef Full Text | Google Scholar

Hawas, U., El-Kassem, L., Awad, H., Taie, H. (2013). Anti-Alzheimer, antioxidant activities and flavonol glycosides of Eryngium campestre L. Curr. Chem. Biol. 7, 188–195. doi: 10.2174/2212796811307020010

CrossRef Full Text | Google Scholar

Hemmer, H., Gülz, P. G. (1989). Tetra-and pentacyclic triterpenoids from epicuticular wax of Euphorbia cyparissias L., Euphorbiaceae. Z. Für Naturforschung 44c, 563–567. doi: 10.1515/znc-1989-7-804

CrossRef Full Text | Google Scholar

Hotti, H., Rischer, H. (2017). The killer of Socrates: Coniine and related alkaloids in the plant kingdom. Mol. (Basel Switzerland) 22 (11), 1962. doi: 10.3390/molecules22111962

CrossRef Full Text | Google Scholar

Ichim, M. C. (2019). The DNA-based authentication of commercial herbal products reveals their globally widespread adulteration. Front. Pharmacol. 10, 1227. doi: 10.3389/fphar.2019.01227

PubMed Abstract | CrossRef Full Text | Google Scholar

Isik, G., Yucel, E. (2017). Fatty acid composition of Carduus nutans seeds. Int. J. Agri Env. Res. 3, 19–25.

Google Scholar

Jarić, S., Kostić, O., Mataruga, Z., Pavlović, D., Pavlović, M., Mitrović, M., et al. (2018). Traditional wound-healing plants used in the Balkan region (Southeast Europe). J. Ethnopharmacol. 211, 311–328. doi: 10.1016/j.jep.2017.09.018

PubMed Abstract | CrossRef Full Text | Google Scholar

Jordon-Thaden, I. E., Louda, S. M. (2003). Chemistry of Cirsium and Carduus: A role in ecological risk assessment for biological control of weeds? Biochem. Syst. Ecol. 31, 1353–1396. doi: 10.1016/S0305-1978(03)00130-3

CrossRef Full Text | Google Scholar

Küpeli, E., Kartal, M., Aslan, S., Yesilada, E. (2006). Comparative evaluation of the anti-inflammatory and antinociceptive activity of Turkish Eryngium species. J. Ethnopharmacol. 107, 32–37. doi: 10.1016/j.jep.2006.02.005

PubMed Abstract | CrossRef Full Text | Google Scholar

Kamboj, A., Saluja, A. K. (2010). Phytopharmacological review of Xanthium strumarium L. (Cocklebur). Int. J. Green Pharm. (IJGP) 4, 129–139. doi: 10.22377/IJGP.V4I3.133

CrossRef Full Text | Google Scholar

Karakaya, S., Karakaya, S., Polat, A., Aksakal, Ö., Sümbüllü, Y. Z., İncekara, Ü. (2019). Plants used in traditional medicine and other uses in South of Erzurum (Turkey): An ethnobotanical study. Ethnobot. Res. Appl. 18, 1–18.

Google Scholar

Kardong, D., Upadhyaya, S., Saikia, L. R. (2013). Screening of phytochemicals, antioxidant and antibacterial activity of crude extract of Pteridium aquilinum Kuhn. JOPR: J. Pharm. Res. 6, 179–182. doi: 10.1016/j.jopr.2012.11.037

CrossRef Full Text | Google Scholar

Kashyap, D., Sharma, A., Tuli, H. S., Sak, K., Garg, V. K., Buttar, H. S., et al. (2018). Apigenin: A natural bioactive flavone-type molecule with promising therapeutic function. J. Funct. Foods 48, 457–471. doi: 10.1016/j.jff.2018.07.037

CrossRef Full Text | Google Scholar

Katewa, S. S. (2008). “Indigenous people and forests: Perspectives of an ethnobotanical study from Rajasthan (India),” in Herbal Drugs: Ethnomedicine to Modern Medicine. Ed. Ramawat, K. (Berlin Heidelberg: Springer), 33–56. doi: 10.1007/978-3-540-79116-4_3

CrossRef Full Text | Google Scholar

Kharchoufa, L., Merrouni, I. A., Yamani, A., Elachouri, M. (2018). Profile on medicinal plants used by the people of North Eastern Morocco: toxicity concerns. Toxicon: Off. J. Int. Soc. Toxicol. 154, 90–113. doi: 10.1016/j.toxicon.2018.09.003

CrossRef Full Text | Google Scholar

Kikowska, M., Thiem, B., Sliwinska, E., Rewers, M., Kowalczyk, M., Stochmal, A., et al. (2016). Micropropagation of Eryngium campestre L. via shoot culture provides valuable uniform plant material with enhanced content of phenolic acids and antimicrobial activity. Acta Biol. Cracoviensia Ser. Bot. 58, 43–56. doi: 10.1515/abcsb-2016-0009

CrossRef Full Text | Google Scholar

Klimakhin, G. I., Fonin, V. S., Maslyakov, V. Y., Fadeev, N. B., Semikin, V. V., Pel'gunova, L. A. (2015). Biochemical features of common Cocklebur (Xanthium strumarium L.). Pharmaceut. Chem. J. 49, 547–550. doi: 10.1007/s11094-015-1324-7

CrossRef Full Text | Google Scholar

Kozuharova, E., Ionkova, I., Spadaro, V. (2019). Xanthium strumarium-a potential cheap resource of plant substances for medicinal use. Flora Mediterr. 29, 93–102. doi: 10.7320/FlMedit29.093

CrossRef Full Text | Google Scholar

Krayer, O., Meilman, E. (1977). “Veratrum alkaloids with antihypertensive activity,” in Antihypertensive agents (Berlin Heidelberg: Springer Berlin Heidelberg), 547–570. doi: 10.1007/978-3-642-66309-3_12

CrossRef Full Text | Google Scholar

Łuczaj, Ł., Szymański, W. M. (2007). Wild vascular plants gathered for consumption in the Polish countryside: a review. J. Ethnobiol. Ethnomed. 3, 17. doi: 10.1186/1746-4269-3-17

PubMed Abstract | CrossRef Full Text | Google Scholar

Lanzotti, V., Barile, E., Scambia, G., Ferlini, C. (2015). Cyparissins A and B, jatrophane diterpenes from Euphorbia cyparissias as Pgp inhibitors and cytotoxic agents against ovarian cancer cell lines. Fitoterapia 104, 75–79. doi: 10.1016/j.fitote.2015.05.012

PubMed Abstract | CrossRef Full Text | Google Scholar

Leporatti, M. L., Ivancheva, S. (2003). Preliminary comparative analysis of medicinal plants used in the traditional medicine of Bulgaria and Italy. J. Ethnopharmacol. 87, 123–142. doi: 10.1016/S0378-8741(03)00047-3

PubMed Abstract | CrossRef Full Text | Google Scholar

Liu, J., Cai, Y. Z., Wong, R. N. S., Lee, C. K. F., Tang, S. C. W., Sze, S. C. W., et al. (2012). Comparative analysis of caffeoylquinic acids and lignans in roots and seeds among various burdock (Arctium lappa) genotypes with high antioxidant activity. J. Agric. Food Chem. 60, 4067–4075. doi: 10.1021/jf2050697

PubMed Abstract | CrossRef Full Text | Google Scholar

Lou, C., Zhu, Z., Zhao, Y., Zhu, R., Zhao, H. (2017). Arctigenin, a lignan from Arctium lappa L., inhibits metastasis of human breast cancer cells through the downregulation of MMP-2/-9 and heparanase in MDA-MB-231 cells. Oncol. Rep. 37, 179–184. doi: 10.3892/or.2016.5269

PubMed Abstract | CrossRef Full Text | Google Scholar

Madaan, R., Kumar, S. (2012). Screening of alkaloidal fraction of Conium maculatum L. aerial parts for analgesic and antiinflammatory activity. Indian J. Pharmaceut. Sci. 74, 457–460. doi: 10.4103/0250-474X.108423

CrossRef Full Text | Google Scholar

Maghsoumi-Norouzabad, L., Alipoor, B., Abed, R., Eftekhar Sadat, B., Mesgari-Abbasi, M., Asghari Jafarabadi, M. (2016). Effects of Arctium lappa L. (Burdock) root tea on inflammatory status and oxidative stress in patients with knee osteoarthritis. Int. J. Rheumatic Dis. 19, 255–261. doi: 10.1111/1756-185X.12477

CrossRef Full Text | Google Scholar

Mamedov, N., Gardner, Z., Craker, L. E. (2004). Medicinal plants used in Russia and Central Asia for the treatment of selected skin conditions. J. Herbs Spices Med. Plants 11, 191–222. doi: 10.1300/J044v11n01_07

CrossRef Full Text | Google Scholar

Mannan, M., Maridass, M., Victor, B. (2008). A review on the potential uses of ferns. Ethnobot. Leaflets 12, 281–285.

Google Scholar

Marčetić, M. D., Petrović, S. D., Milenković, M. T., Niketić, M. S. (2014). Composition, antimicrobial and antioxidant activity of the extracts of Eryngium palmatum Pančić and Vis. (Apiaceae). Cent. Eur. J. Biol. 9, 149–155. doi: 10.2478/s11535-013-0247-0

CrossRef Full Text | Google Scholar

Maroyi, A. (2014). Not just minor wild edible forest products: Consumption of pteridophytes in sub-Saharan Africa. J. Ethnobiol. Ethnomed. 10, 78. doi: 10.1186/1746-4269-10-78

CrossRef Full Text | Google Scholar

Matejić, J. S., Stojanović-Radić, Z. Z., Ristić, M. S., Veselinović, J. B., Zlatković, B. K., Marin, P. D., et al. (2018). Chemical characterization, in vitro biological activity of essential oils and extracts of three Eryngium L. species and molecular docking of selected major compounds. J. Food Sci. Technol. 55, 2910–2925. doi: 10.1007/s13197-018-3209-8

PubMed Abstract | CrossRef Full Text | Google Scholar

May, L. W. (1978). The economic uses and associated folklore of ferns and fern allies. Bot. Rev. 44, 491–528. doi: 10.1007/BF02860848

CrossRef Full Text | Google Scholar

Medbouhi, A., Tintaru, A., Beaufay, C., Naubron, J.-V., Djabou, N., Costa, J., et al. (2018). Structural elucidation and cytotoxicity of a new 17-membered ring lactone from Algerian Eryngium campestre. Molecules 23 (12), 3250. doi: 10.3390/molecules23123250

CrossRef Full Text | Google Scholar

Miglani, A., Manchanda, R. K. (2014). Observational study of Arctium lappa in the treatment of acne vulgaris. Homeopathy 103, 203–207. doi: 10.1016/j.homp.2013.12.002

PubMed Abstract | CrossRef Full Text | Google Scholar

Milica, C., Roman, C. N., Troia, D. (2012). Flora medicinala a Romaniei [Romania’s medicinal flora] (Iasi: Doxologia Publishing House).

Google Scholar

Ministry of Agriculture and Rural Development (2015). Order no. 352 of February 10, 2015 for the approval of the rules on cross compliance in the support schemes and measures for farmers in Romania (published in the Official Gazette with the number 363 of May 26, 2015).

Google Scholar

Mitich, L. W. (1998). Poison-Hemlock (Conium maculatum L.). Weed Technol. 12, 194–197. doi: 10.1017/S0890037X00042792

CrossRef Full Text | Google Scholar

Mohan, G. (2008). Tratarea bolilor cu plante medicinale [Treating diseases with medicinal plants] (Bucharest: Corint Publishing House).

Google Scholar

Mondal, J., Panigrahi, A. K., Khuda-Bukhsh, A. R. (2014). Anticancer potential of Conium maculatum extract against cancer cells in vitro: Drug-DNA interaction and its ability to induce apoptosis through ROS generation. Pharmacog. Magazine 10, S524–S533. doi: 10.4103/0973-1296.139792

CrossRef Full Text | Google Scholar

Mustafa, B., Hajdari, A., Krasniqi, F., Hoxha, E., Ademi, H., Quave, C. L., et al. (2012). Medical ethnobotany of the Albanian Alps in Kosovo. J. Ethnobiol. Ethnomed. 8, 6. doi: 10.1186/1746-4269-8-6

PubMed Abstract | CrossRef Full Text | Google Scholar

Özbilgin, S., Sal, G., Citoğlu, T. (2012). Uses of some Euphorbia species in traditional medicine in Turkey and their biological activities. Turk J. Pharmaceut. Sci. 9, 241–256.

Google Scholar

Olivaro, C., Rostan, V., Bandera, D., Moyna, G., Vazquez, A. (2016). Xanthane sesquiterpenoids from the roots and flowers of Xanthium cavanillesii. Natural Prod. Res. 30, 2238–2242. doi: 10.1080/14786419.2016.1149709

CrossRef Full Text | Google Scholar

Paksoy, M. Y., Selvi, S., Savran, A. (2016). Ethnopharmacological survey of medicinal plants in UlukIşla (Niǧde-Turkey). J. Herbal Med. 6, 42–48. doi: 10.1016/j.hermed.2015.04.003

CrossRef Full Text | Google Scholar

Panter, K. E., Welch, K. D., Gardner, D. R. (2011). “Toxic plants,” in Reproductive and Developmental Toxicology. Ed. Ramesh, C. G. (Elsevier Inc.), 689–705. doi: 10.1016/B978-0-12-382032-7.10051-7

CrossRef Full Text | Google Scholar

Papp, N., Bartha, S., Boris, G., Balogh, L. (2011). Traditional uses of medicinal plants for respiratory diseases in Transylvania. Natural Product Commun. 6, 1459–1460. doi: 10.1177/1934578x1100601012

CrossRef Full Text | Google Scholar

Papp, N., Birkás-Frendl, K., Bencsik, T., Stranczinger, S., Czégényi, D. (2014). Survey of traditional beliefs in the Hungarian Csángó and Székely ethnomedicine in Transylvania, Romania. Braz. J. Pharmacog. 24, 141–152. doi: 10.1016/j.bjp.2014.03.005

CrossRef Full Text | Google Scholar

Papp, N., Tóth, M., Dénes, T., Gyergyák, K., Filep, R., Bartha, S. G., et al. (2017). Ethnomedicinal treatment of gastrointestinal disorders in Transylvania, Romania. Acta Ethnographica Hungarica 62, 207–220. doi: 10.1556/022.2017.62.1.10

CrossRef Full Text | Google Scholar

Papp, N. (2004). Antimicrobial activity of extracts of five Hungarian Euphorbia species and some plant metabolits. Acta Bot. Hungarica 46, 363–371. doi: 10.1556/ABot.46.2004.3-4.8

CrossRef Full Text | Google Scholar

Parvu, C. (2000). Universul plantelor: Mica enciclopedie [Plants’ universe: small encyclopedia] (Bucuresti: Enciclopedica Publishing House).

Google Scholar

Pe'er, G., Zinngrebe, Y., Moreira, F., Sirami, C., Schindler, S., Müller, R., et al. (2019). A greener path for the EU Common Agricultural Policy. Science 365, 449–451. doi: 10.1126/science.aax3146

PubMed Abstract | CrossRef Full Text | Google Scholar

Pieroni, A., Vandebroek, I. (2007). Traveling cultures and plants: the ethnobiology and ethnopharmacy of migrations (New York-Oxford: Berghahn Books).

Google Scholar

Piluzza, G., Bullitta, S. (2011). Correlations between phenolic content and antioxidant properties in twenty-four plant species of traditional ethnoveterinary use in the Mediterranean area. Pharmaceut. Biol. 49, 240–247. doi: 10.3109/13880209.2010.501083

CrossRef Full Text | Google Scholar

Pretty, J., Benton, T. G., Bharucha, Z. P., Dicks, L. V., Flora, C. B., Godfray, H. C. J., et al. (2018). Global assessment of agricultural system redesign for sustainable intensification. Nat. Sustainability 1, 441–446. doi: 10.1038/s41893-018-0114-0

CrossRef Full Text | Google Scholar

Raclariu, A. C., Heinrich, M., Ichim, M. C., de Boer, H. (2018). Benefits and limitations of DNA barcoding and metabarcoding in herbal product authentication. Phytochem. Anal. 29, 123–128. doi: 10.1002/pca.2732

PubMed Abstract | CrossRef Full Text | Google Scholar

Ramírez-Erosa, I., Huang, Y., Hickie, R. A., Sutherland, R. G., Barl, B. (2007). Xanthatin and xanthinosin from the burs of Xanthium strumarium L. as potential anticancer agents. Can. J. Physiol. Pharmacol. 85, 1160–1172. doi: 10.1139/Y07-104

PubMed Abstract | CrossRef Full Text | Google Scholar

Redzic, S. (2010). Wild medicinal plants and their usage in traditional human therapy (Southern Bosnia and Herzegovina, W. Balkan). J. Med. Plants Res. 4, 1003–1027. doi: 10.5897/JMPR09.254

CrossRef Full Text | Google Scholar

Reynolds, T. (2005). Hemlock alkaloids from Socrates to poison aloes. Phytochemistry 66, 1399–1406. doi: 10.1016/j.phytochem.2005.04.039

PubMed Abstract | CrossRef Full Text | Google Scholar

Roberts, M. F., Wink, M. (2013). Alkaloids: Biochemistry, ecology, and medicinal applications. (New York: Plenum Press).

Google Scholar

Romero, M., Zanuy, M., Rosell, E., Cascante, M., Piulats, J., Font-Bardia, M., et al. (2015). Optimization of xanthatin extraction from Xanthium spinosum L. and its cytotoxic, anti-angiogenesis and antiviral properties. Eur. J. Med. Chem. 90, 491–496. doi: 10.1016/j.ejmech.2014.11.060

PubMed Abstract | CrossRef Full Text | Google Scholar

Sõukand, R., Pieroni, A. (2016). The importance of a border: Medical, veterinary, and wild food ethnobotany of the Hutsuls living on the Romanian and Ukrainian sides of Bukovina. J. Ethnopharmacol. 185, 17–40. doi: 10.1016/j.jep.2016.03.009

PubMed Abstract | CrossRef Full Text | Google Scholar

Sak, K., Jürisoo, K., Raal, A. (2014). Estonian folk traditional experiences on natural anticancer remedies: from past to the future. Pharmaceut. Biol. 52, 855–866. doi: 10.3109/13880209.2013.871641

CrossRef Full Text | Google Scholar

Salvamani, S., Gunasekaran, B., Shaharuddin, N. A., Ahmad, S. A., Shukor, M. Y. (2014). Antiartherosclerotic effects of plant flavonoids. BioMed. Res. Int. 2014, 480258. doi: 10.1155/2014/480258

PubMed Abstract | CrossRef Full Text | Google Scholar

Sanda, V., Öllerer, K., Burescu, P. (2008). Fitocenozele din Romania [The phytocenoses in Romania] (Bucharest: Ars Docendi).

Google Scholar

Sarateanu, V., Horablaga, M., Stroia, C., Butnariu, M., Bostan, C. (2008). Assessing the invasive species impact on the grasslands from Western Romania. Res. J. Agric. Sci. 40, 319–326.

Google Scholar

Segneanu, A.-E., Cepan, C., Grozescu, I., Cziple, F., Olariu, S., Ratiu, S., et al. (2019). “Therapeutic use of some Romanian medicinal plants,” in Pharmacognosy - Medicinal Plants (London: IntechOpen). doi: 10.5772/intechopen.82477

CrossRef Full Text | Google Scholar

Shale, T. L., Stirk, W. A., Van Staden, J. (1999). Screening of medicinal plants used in Lesotho for anti-bacterial and anti-inflammatory activity. J. Ethnopharmacol. 67, 347–354. doi: 10.1016/S0378-8741(99)00035-5

PubMed Abstract | CrossRef Full Text | Google Scholar

Simmler, C., Graham, J. G., Chen, S.-N., Pauli, G. F. (2018). Integrated analytical assets aid botanical authenticity and adulteration management. Fitoterapia 129, 401–414. doi: 10.1016/j.fitote.2017.11.017

PubMed Abstract | CrossRef Full Text | Google Scholar

Soumia, B. (2018). “Eryngium campestre L.: Polyphenolic and flavonoid compounds; Applications to health and disease,” in Polyphenols: Mechanisms of Action in Human Health and Disease (Elsevier), 69–79. doi: 10.1016/b978-0-12-813006-3.00007-6

CrossRef Full Text | Google Scholar

Spencer, J. P. E., Abd El Mohsen, M. M., Rice-Evans, C. (2004). Cellular uptake and metabolism of flavonoids and their metabolites: Implications for their bioactivity. Arch. Biochem. Biophysics 423, 148–161. doi: 10.1016/j.abb.2003.11.010

CrossRef Full Text | Google Scholar

Spiridonov, N. A. (2008). “Russian medicinal plants in treatment of cancer,” in Botanical medicine in clinical practice. Eds. Watson, R. R., Preedy, V. R. (Trowbridge: Cromwell Press), 421–429. doi: 10.1079/9781845934132.0421

CrossRef Full Text | Google Scholar

Stanescu, U., Hancianu, M., Cioanca, O., Aprotosoaie, A. C., Miron, A. (2014). Plante medicinale de la A la Z [Medicinal plants from A to Z] (Iasi: POLIROM Publishing House).

Google Scholar

Stanković, M. S., Zlatić, N. M. (2014). Antioxidant activity and concentration of secondary metabolites in the plant parts of Euphorbia cyparissias L. Kragujevac J. Sci. 36, 121–128. doi: 10.5937/KgJSci1436121S

CrossRef Full Text | Google Scholar

Tabassum, S., Perk, A. A., Qureshi, M. Z., Sabitaliyevich, U. Y., Tokmurziyeva, G. (2019). “Arctium lappa,” in Nonvitamin and Nonmineral Nutritional Supplements (Elsevier Inc.), 277–281. doi: 10.1016/B978-0-12-812491-8.00039-4

CrossRef Full Text | Google Scholar

Tamayo, C., Richardson, M. A., Diamond, S., Skoda, I. (2000). The chemistry and biological activity of herbs used in Flor-EssenceTM herbal tonic and Essiac. Phytother. Res. 14, 1–14. doi: 10.1002/(sici)10.1002/(SICI)1099-1573(200002)14:13.3.CO;2-F

PubMed Abstract | CrossRef Full Text | Google Scholar

Tita, I., Mogosanu, G. D., Tita, M. G. (2009). Ethnobotanical invenory of medicinal plants from the South-West of Romania. FARMACIA 57, 141–156.

Google Scholar

Tousch, D., Bidel, L. P. R., Cazals, G., Ferrare, K., Leroy, J., Faucanié, M., et al. (2014). Chemical analysis and antihyperglycemic activity of an original extract from burdock root (arctium lappa). J. Agric. Food Chem. 62, 7738–7745. doi: 10.1021/jf500926v

PubMed Abstract | CrossRef Full Text | Google Scholar

Tsioutsiou, E. E., Giordani, P., Hanlidou, E., Biagi, M., De Feo, V., Cornara, L., et al. (2019). Ethnobotanical study of medicinal plants used in Central Macedonia, Greece. Evid. Based Complementary Altern. Med. 2019, 4513792. doi: 10.1155/2019/4513792

CrossRef Full Text | Google Scholar

Ujváry, I. (2010). “Pest control agents from natural products,” in Hayes" Handbook of Pesticide Toxicology (Elsevier Inc.), 119–229. doi: 10.1016/B978-0-12-374367-1.00003-3

CrossRef Full Text | Google Scholar

Vasas, A., Orbán-Gyapai, O., Hohmann, J. (2015). The Genus Rumex: Review of traditional uses, phytochemistry and pharmacology. J. Ethnopharmacol. 175, 198–228. doi: 10.1016/j.jep.2015.09.001

PubMed Abstract | CrossRef Full Text | Google Scholar

Vetter, J. (2004). Poison hemlock (Conium maculatum L.). Food Chem. Toxicol. 42, 1373–1382. doi: 10.1016/j.fct.2004.04.009

PubMed Abstract | CrossRef Full Text | Google Scholar

Vetter, J. (2010). “Toxicological and medicinal aspects of the most frequent fern species, pteridium aquilinum (L.) kuhn,” in Working with Ferns: Issues and Applications (Springer), 361–375. doi: 10.1007/978-1-4419-7162-3_25

CrossRef Full Text | Google Scholar

Wang, D., Badarau, A. S., Swamy, M. K., Shaw, S., Maggi, F., da Silva, L. E., et al. (2019). Arctium species secondary metabolites chemodiversity and bioactivities. Front. Plant Sci. 10, 834. doi: 10.3389/fpls.2019.00834

PubMed Abstract | CrossRef Full Text | Google Scholar

Wang, P. (2012). Phytochemical constituents and pharmacological activities of Eryngium L. (Apiaceae). Pharmaceutical. Crops 3, 99–120. doi: 10.2174/2210290601203010099

CrossRef Full Text | Google Scholar

Wegiera, M., Smolarz, H. D., Wianowska, D., Dawidowicz, A. L. (2007). Anthracene derivatives in some species of Rumex L. genus. Acta Societatis Bot. Poloniae 76, 103–108. doi: 10.5586/asbp.2007.013

CrossRef Full Text | Google Scholar

Wiart, C. (2012). Lead compounds from medicinal plants for the treatment of neurodegenerative diseases (Academic Press).

Google Scholar

World Health Organization (2013). WHO traditional medicine strategy: 2014-2023 (Geneva).

Google Scholar

Yadav, S., Yadav, S. S., Ganie, S. A., Gulia, S. S., Yadav, N. (2015). Xanthium strumarium L.: An ethnomedicinal and phytochemical review. Int. J. Phytomed. 6, 471–476.

Google Scholar

Zhang, Z., Li, S., Ownby, S., Wang, P., Yuan, W., Zhang, W., et al. (2008). Phenolic compounds and rare polyhydroxylated triterpenoid saponins from Eryngium yuccifolium. Phytochemistry 69, 2070–2080. doi: 10.1016/j.phytochem.2008.03.020

PubMed Abstract | CrossRef Full Text | Google Scholar

Zhao, F., Wang, L., Liu, K. (2009). In vitro anti-inflammatory effects of arctigenin, a lignan from Arctium lappa L., through inhibition on iNOS pathway. J. Ethnopharmacol. 122, 457–462. doi: 10.1016/j.jep.2009.01.038

PubMed Abstract | CrossRef Full Text | Google Scholar

Zhelev, I., Dimitrova-Dyulgerova, I., Belkinova, D., Mladenov, R. (2013). Content of phenolic compounds in the Genus Carduus L. from Bulgaria. ECOLOGIA BALKANICA 5, 13–21.

Google Scholar

Zheleva-Dimitrova, D., Zhelev, I., Dimitrova-Dyulgerova, I. (2011). Antioxidant activity of some Carduus species growing in Bulgaria. Free Radicals Antioxid. 1, 15–20. doi: 10.5530/ax.2011.4.4

CrossRef Full Text | Google Scholar

Keywords: meadow weed, medicinal plant, ethnomedicine, Arctium lappa, Eryngium campestre, Rumex acetosella, Xanthium spinosum, Xanthium strumarium

Citation: Grosu E and Ichim MC (2020) Turning Meadow Weeds Into Valuable Species for the Romanian Ethnomedicine While Complying With the Environmentally Friendly Farming Requirements of the European Union’s Common Agricultural Policy. Front. Pharmacol. 11:529. doi: 10.3389/fphar.2020.00529

Received: 25 October 2019; Accepted: 03 April 2020;
Published: 23 April 2020.

Edited by:

Marina Sokovic, University of Belgrade, Serbia

Reviewed by:

Francesca Scotti, UCL School of Pharmacy, United Kingdom
Rainer Willi Bussmann, Saving Knowledge, Bolivia
Alexandru Sabin Badarau, Babeș-Bolyai University, Romania

Copyright © 2020 Grosu and Ichim. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Mihael Cristin Ichim, cichim@hotmail.com

Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.