Black chokeberry (Aronia melanocarpa) extracts in terms of geroprotector criteria
Introduction
Natural products, such as plant extracts or isolated plant compounds, have been used increasingly to prevent and treat diseases and maintain healthy longevity (Fontana & Partridge, 2015). Numerous studies have confirmed that a diet rich in plant foods (berries, fruits, and vegetables) provides functional benefits for human health and protects against cancer, cardiovascular diseases, diabetes, osteoporosis, and neurodegenerative diseases (Borowska & Brzóska, 2016; Kahleova, Levin, & Barnard, 2020; Lee et al., 2017; Nile & Park, 2014; Olas, 2018; Szajdek & Borowska, 2008). Therefore, studies of new biologically active molecules and their sources have attracted considerable interest, particularly in the food industry, which has introduced various natural components in food products to improve their functionality (Arruda, Neri-Numa, Kido, Maróstica Júnior, & Pastore, 2020; Tolun & Altintas, 2019, pp. 235–284).
Black chokeberry Aronia melanocarpa (Michx.) Elliot is a valuable fruit crop that belongs to the Rose family (Rosaceae) and Apple subfamily (Pomodieae) (Kokotkiewicz, Jaremicz, & Luczkiewicz, 2010). Black chokeberry originates from North America (Jurikova et al., 2017; Kokotkiewicz et al., 2010; Rugină et al., 2012). Staszowska-Karkut and Materska (2020) reported that American Indians used infusion of Aronia leaves as an elixir of youth. Aronia was also used as a cure for colds, to heal wounds and bones, and by pregnant women to promote strength development (Costea, Lupu, Vlase, Nencu, & Gird, 2016; Staszowska-Karkut & Materska, 2020). Chokeberry leaf extracts were used as an anti-cold and anti-inflammatory remedy (Costea et al., 2016; Ferlemi & Lamari, 2016; Staszowska-Karkut & Materska, 2020). Chokeberry was first mentioned in Northern (Finland, Sweden, and Norway), Eastern (Poland) and Central (Germany) Europe at the beginning of the 20th century. In Russia, the distribution of chokeberry occurred initially in the Northern regions in the middle of the 20th century and then became widespread throughout the country (Chrubasik, Li, & Chrubasik, 2010; Denev, Kratchanov, Ciz, Lojek, & Kratchanova, 2012; Janick & Paull, 2008; Jurikova et al., 2017; Kulling & Rawel, 2008). Nowadays Aronia is cultivated all over the world, but as a commercial berry crop, it has gained the highest popularity in the Northern (Denmark, Estonia, Latvia, Lithuania, Sweden), Eastern (Bulgaria, Poland, Serbia), and Central (Czech Republic, Germany) European countries (Borowska & Brzóska, 2016; Kulling & Rawel, 2008; Sueiro et al., 2006). Poland is the world's largest producer of chokeberries, accounting for almost 90% of global production (Engels & Brinckmann, 2014). According to Poland's Agricultural Market Agency, between 2004 and 2013 chokeberry fields in Poland increased from a total of 5000 ha to 8000 ha in size and the yield from 38,000 to 58,000 metric tons. However, the larger 2013 crop caused oversupply and depressed the chokeberry market (Engels & Brinckmann, 2014). The most common cultivated varieties of black chokeberry are Finnish “Viking”, Czech “Nero”, Danish “Aron”, Polish “Galichanka”, Swedish “Hugin”, Russian “Rubina” and Hungarian "Fertödi" (Janick & Paull, 2008; Jurikova et al., 2017). Currently, chokeberry is distributed widely all over the world and is used as a food (juices, jams, wine, and desserts), a source of natural food colorant, and a rich source of phytonutrients with a wide spectrum of beneficial actions (Cvetanovic et al., 2018; Ferlemi & Lamari, 2016; Jurikova et al., 2017; Kokotkiewicz et al., 2010; Kulling & Rawel, 2008; Staszowska-Karkut & Materska, 2020).
Aronia has positive effects on chronic diseases, including cardiovascular diseases (Duchnowicz, Nowicka, Koter-Michalak, & Broncel, 2012; Naruszewicz, Laniewska, Millo, & Dłuzniewski, 2007), neurodegenerative disorders (Daskalova et al., 2019; Islam, 2017; Lee et al., 2016, 2017), and type 1 diabetes (Badescu, Badulescu, Badescu, & Ciocoiu, 2015; Jeon et al., 2018). Experimental studies have shown that the health-promoting properties of black chokeberry products (such as extracts from berries, leaves, and stems) may be associated with their strong antioxidant activity (Cvetanovic et al., 2018; Jurikova et al., 2017; Kim, Ku, et al., 2013; Thi & Hwang, 2016), antitumor activity (Rugină et al., 2012; Skupień, Kostrzewa-Nowak, Oszmiański, & Tarasiuk, 2008; Staszowska-Karkut & Materska, 2020), anti-inflammatory activity (Lee et al., 2018; Ohgami et al., 2005; Zapolska-Downar, Bryk, Małecki, Hajdukiewicz, & Sitkiewicz, 2012), gastroprotective effects (Matsumoto, Hara, Chiji, & Kasai, 2004; Paulrayer et al., 2017) and improvement of lipid metabolism (Bakuradze et al., 2019; Jakovljevic et al., 2018; Park et al., 2017).
This review summarizes and evaluates the relevant literature on the effects of chokeberry extracts on various model organisms (fruit fly, mouse, rat) and intracellular processes to identify its potential geroprotective (anti-aging) properties. The geroprotective properties were estimated based on the criteria proposed previously (Moskalev et al., 2016), which include the following effects: (1) lifespan extension in model organisms, (2) amelioration of the biomarkers of aging, (3) low toxicity, (4) minimal risk for adverse events, (5) improvement of the quality of life, (6) evolutionarily conserved mechanisms, (7) reproducibility on different models, (8) prevention of age-associated diseases, and (9) increased resistance to environmental stress factors.
Section snippets
Content of biologically active compounds
Black chokeberry fruit contains a range of complex biologically active substances. Their most important constituents are phenolic acids and flavonoids, such as anthocyanins and proanthocyanidins (Borowska & Brzóska, 2016; Denev et al., 2012; Hudec et al., 2006; Kulling & Rawel, 2008). Proanthocyanidins (condensed tannins) are oligomeric and polymer catechins, consisting of (−)-epicatechin, which is responsible for the astringent taste of black chokeberry. Proanthocyanidins form complexes with
Lifespan extension
A number of biologically active substances, which are contained in black chokeberries such as flavonoids (quercetin, quercetin-3-O-glucoside) and phenolic acids (caffeic acid), have been reported to increase the lifespan of model organisms, that is one of the main characteristics of geroprotector (Moskalev et al., 2015). For example, constant supplementation of the nematode growth medium with 0.1 and 0.2 mM quercetin for several generations has increased the average lifespan of Caenorhabditis
Hormesis
Hormesis refers to the biphasic dose-response relationship for effects of some environmental factors with low dose stimulatory/beneficial outcomes and high dose inhibitory/toxic outcomes (Calabrese, 2013; Mattson, 2008; Rattan, 2008). Hormesis leads to stress-induced stimulation of protective mechanisms that can contribute to healthy longevity due to preserving cellular and organismal homeostasis during stressful conditions and the aging process (Calabrese et al., 2012; Rattan, 2008).
Antimicrobial activity
A virucidal test was performed to evaluate the effectiveness of A. melanocarpa fruit against various seasonal influenza strains (H1/K09, H3/PE16 and H1/K2785) and to test its efficiency to induce resistance to the influenza B virus. The alcoholic chokeberry extract powder at low concentrations (from 0.0625 to 1 mg/ml) inhibited approximately 70% of the viral plaques of the H1 and H3 viruses including the oseltamivir-resistant H1/K2785 strain (Park et al., 2013). These effects were attributed to
Toxicity and side effects
Berry fruits are considered important nutritional sources that are rich in minerals, vitamins, and beneficial bioactive molecules with minimal harmful or toxic effects on the body (Nile & Park, 2014; Paredes-López et al., 2010). Most adverse health effects reported for berries may be manifested in the form of allergic reactions in children and adults (Fernández-Rivas, 2015). Allergy to berry fruits of the Rosaceae family plants, which can cross-react with birch and grass pollen, is a severe
Conclusions
In recent years, there is a growing interest in foods and dietary supplements that can provide functional benefits for human health and slow down the aging process. A. melanocarpa is a rich source of polyphenolic compounds with many health benefits, including induction of anti-proliferative effects, improvement of glucose and lipid metabolism, amelioration of neurodegenerative disorders, antiviral and antibacterial activity, protection of the gastrointestinal system. In addition,
Author contributions
Conceptualization, EYP, MVS, AM, KJM; Writing – Original Draft Preparation, EYP, HYL, JHL; Writing – Review & Editing, MVS, KJM, AM; Supervision, MVS, KJM, AM; Project Administration, EYP, KJM, AM; Funding Acquisition, AM, KJM.
Funding
This study was funded by the joint grant of the Russian Foundation for Basic Research (№ 19-515-51001) and the National Research Foundation of Korea (N 2019K2A9A1A06098657).
Declaration of competing interest
None.
Acknowledgments
Figures were made using BioRender.
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