Antispasmodic effects of black chokeberry ( Aronia melanocarpa (Michx.) Elliott) extracts and juice and their potential use in gastrointestinal disorders
Restricted accessResearch articleFirst published online June 1, 2020
Antispasmodic effects of black chokeberry ( Aronia melanocarpa (Michx.) Elliott) extracts and juice and their potential use in gastrointestinal disorders
Phytotherapy has an important role in the functional gastrointestinal and motility disorder prevention and treatment.
OBJECTIVE:
The aims of our study were to analyze the chemical composition and the antispasmodic activity of the dry black chokeberry ethanolic extract, waste extract and the juice in the isolated rat ileum.
METHODS:
The anthocyanins and flavonoids quantification was carried out by the spectrophotometric method using the HPLC instrument. The study examined the influence of the chokeberry preparations and cyanidin-3-O-galactoside, the main anthocyanin compound, on the spontaneous, acetylcholine and KCl-induced ileum smooth muscle contraction, as well as on the contractions induced by histamine, CaCl2 and BaCl2 and contractions in the presence of nitric oxide synthase inhibitor (L-NAME).
RESULTS:
In all the examined preparations, the most abundant compounds were anthocyanins, especially cyanidin heterosides. The highest content of polyphenols and anthocyanins was found in the chokeberry waste extract. Among the chokeberry preparations, the ethanolic extract had the highest flavonoid concentration. The chokeberry preparations and cyanidin-3-O-galactoside in a concentration dependent manner significantly relaxed the rat ileum spontaneous and induced contractions. The results demonstrated that the nitric-oxide pathway was not involved in the relaxant activity of the chokeberry extracts and juice.
CONCLUSIONS:
The study demonstrated that the chokeberry preparations were able to relax contractions in the isolated rat ileum.
Canadanovic-BrunetJ, Tumbas SaponjacV, StajcicS, CetkovicG, CanadanovicV, CebovicT, et al.Polyphenolic composition, antiradical and hepatoprotective activities of bilberry and blackberry pomace extracts. J Berry Res. 2019); Pre-press: 1–14. doi: 10.3233/JBR-180362
2.
BenvenutiS, PellatiF, MelegariM, BertelliD. Polyphenols, anthocyanins, ascorbic acid, and radical scavenging activity of Rubus, Ribes, and Aronia. J Food Sci. 2004;69(3):FCT164–FCT169. doi: 10.1111/j.1365-2621.2004.tb13352.x
3.
SlimestadR, TorskangerpollK, NatelandH, JohannessenT, GiskeN. Flavonoids from black chokeberries Aronia melanocarpa. J Food Compos Anal. 2005;18:61–8. doi: 10.1016/j.jfca.2003.12.003
4.
OszmianskiJ, SapisJC. Anthocyanins in fruits of Aronia Melanocarpa (Chokeberry). J Food Sci. 1988;53(4):1241–2. doi: 10.1111/j.1365-2621.1988.tb13577.x
5.
GasiorowskiK, SzybaK, BrokosB, KołaczynskaB, Jankowiak-WłodarczykM, OszmianskiJ. Antimutagenic activity of anthocyanins isolated from Aronia melanocarpa fruits. Cancer Lett. 1997;119:37–46. doi: 10.1016/S0304-3835(97)00248-6
6.
ĆujićN, SavikinK, MiloradovicZ, IvanovM, VajicU, KaranovicD, et al.Characterization of dried chokeberry fruit extract and its chronic effects on blood pressure and oxidative stress in spontaneously hypertensive rats. J Funct Foods. 2018;44:33–9. doi: 10.1016/j.jff.2018.02.027
7.
SteynWJ. Prevalence and functions of anthocyanins in fruits. In: GouldK, DaviesK, WinefieldC, editors. Anthocyanins, biosynthesis, functions, and aplications. New York: Springer; 2009.
8.
GalvánA, DimitrovK, VauchelP, NikovI. Kinetics of ultrasound assisted extraction of anthocyanins from Aronia melanocarpa (black chokeberry) wastes. Chem Eng Res Des. 2014;92:1818–26. doi: 10.1016/j.cherd.2013.11.020
9.
LarozeLE, Díaz-ReinosoB, MoureA, ZúñigaME, DomínguezH. Extraction of antioxidants from several berries pressing wastes using conventional and supercritical solvents. Eur Food Res Technol. 2010;231:669–77. doi: 10.1007/s00217-010-1320-9
10.
WuX, GuL, PriorRL, McKayS. Characterization of anthocyanins and proanthocyanidins in some cultivars of Ribes, Aronia, and Sambucus and their antioxidant capacity. J Agric Food Chem. 2004;52:7846–56. doi: 10.1021/jf0486850
11.
BorowskaS, BrzóskaMM. Chokeberries (Aronia melanocarpa) and their products as a possible means for the prevention and treatment of noncommunicable diseases and unfavorable health effects due to exposure to xenobiotics. Compr Rev Food Sci Food Saf. 2016;15:982–1017. doi: 10.1111/1541-4337.12221
12.
KullingSE, RawelHM. Chokeberry (Aronia melanocarpa) – A Review on the characteristic components and potential health effects. Planta Med. 2008;74:1625–34. doi: 10.1055/s-0028-1088306
13.
KokotkiewiczA, JaremiczZ, LuczkiewiczM. Aronia Plants: A review of traditional use, biological activities, and perspectives for modern medicine. J Med Food. 2010;13:255–69. doi: 10.1089/jmf.2009.0062
14.
MilutinovicM, BrankovicS, SavikinK, ZdunicG, KosticM, MiladinovicB, et al.Hypothensive and antioxidant effects induced by polyphenol rich black chokeberry (Aronia melanocarpa Elliott) juice. Acta Med Median. 2019;58(2):70–6. doi: 10.5633/amm.2019.0212
DrossmanDA, CorazziariE, TalleyJN, Grant ThompsonW, WhiteheadWE. Rome II. The functional gastrointestinal disorders, 2nd ed. McLean (VA, USA): Degnon Associates; 2000.
17.
American College of Gastroenterology Functional Gastrointestinal Disorders Task Force, BrandtLJ, CheyWD, Foxx-OrensteinAE, SchillerLR, SchoenfeldPS, SpiegelBM, et al.An evidence-based position on the management of irritable bowel syndrome in North America. Am J Gastroenterol. 2009;104:S1–S5. doi: 10.1038/ajg.2008.122
18.
Martinez-PérezFE, JuárezNZ, HernándezRL, BachH. Natural Antispasmodics: Source, Stereochemical Configuration, and Biological Activity. Biomed Res Int. 2018;3819714. doi: 10.1155/2018/3819714
19.
Gočmanac IgnjatovićM, KitićD, RadenkovicM, KostićM, MilutinovićM, Nedin RankovićG, BrankovicS. The effect of the aqueous and methanol fennel stem extracts (Foeniculum vulgare Miller) on isolated rat ileum contractility. Vojnosanit Pregl. 2017;75(8), 809–14.
20.
Yugoslav Pharmacopoeia 2000 (Ph. Jug. V) – Adjusted translation of European Pharmacopoeia 1997 (Ph. Eur. III) Pharmacopoeia (5th ed.). Kovac M, editor. Belgrade: Federal Institute for Health Protection and Improvement; 2001.
21.
CujicN, SavikinK, JankovicT, PljevljakusicD, ZdunicG, IbricS. Optimization of polyphenols extraction from dried chokeberry using maceration as traditional technique. Food Chem. 2016;194:135–42. doi: 10.1016/j.foodchem.2015.08.008
European Pharmacopoeia 6.0. Strasbourg Cedex, France: Council of Europe; 2008.
24.
LiYG, TannerG, LarkinP. The DMACA-HCl protocol and the threshold proanthocyanidin content for bloat safety in forage legumes. J Sci Food Agric. 1996;70:89–101. doi: 10.1002/(SICI)1097-0010(199601)70:13.0.CO;2-N
25.
LoizzoRM, TundisR, BonesiM, MenichiniF, MastelloneV, AvalloneL, et al.Radical scavenging, antioxidant and metal chelating activities of Annona cherimola Mill. (cherimoya) peel and pulp in relation to their total phenolic and total flavonoid contents. J Food Compos Anal. 2012;25:179–84. doi: 10.1016/j.jfca.2011.09.002
26.
BigovicD, BrankovicS, KiticD, RadenkovicM, JankovicT, SavikinK, et al.Relaxant effect of the ethanol extract of Helichrysum plicatum (Asteraceae) on isolated rat ileum contractions. Molecules. 2010;15:3391–401. doi: 10.3390/molecules15053391
27.
BrankovicS, KiticD, RadenkovicM, VeljkovicS, JankovicT, SavikinK, et al.Spasmolytic activity of the ethanol extract of Sideritis raeseri spp. raeseri Boiss. & Heldr. on the isolated rat ileum contractions. J Med Food. 2011;14:495–8. doi: 10.1089/jmf.2010.0036
28.
KostićM, ZlatkovićB, MiladinovićB, ŽivanovićS, Mihajilov-KrstevT, PavlovićD, et al.Rosmarinic acid levels, phenolic contents, antioxidant and antimicrobial activities of the extracts from Salvia verbenaca L. obtained with different solvents and procedures. J Food Biochem. 2015;39:199–208. doi: 10.1111/jfbc.12121
29.
HellstromJ, ShikovA, MakarovaM, PihlantoA, PozharitskayaO, RyhanenE, et al.Blood pressure-lowering properties of chokeberry (Aronia mitchurinii, var Viking). J Funct Foods. 2010;2(2):163–9. doi: 10.1016/j.jff.2010.04.004
30.
CiocoiuM, BadescuL, MironA, BadescuM. The involvement of a polyphenols rich extract of black chokeberry in oxidative stress on experimental arterial hypertension. Evid Based Complement Alternat Med. 2013;912769. doi: 10.1155/2013/912769
31.
BräunlichM, SlimestadR, WangensteenH, BredeC, MalterudKE, BarsettH. Extracts, Anthocyanins and Procyanidins from Aronia melanocarpa as Radical Scavengers and Enzyme Inhibitors. Nutrients. 2013;5(3):663–78. doi: 10.3390/nu5030663
FuC, YangD, PehWY, LaiS, FengX, YangH. Structure and antioxidant activities of proanthocyanidins from elephant apple (Dillenia indica Linn.). J Food Sci. 2015;80(10):C219–C2199. doi: 10.1111/1750-3841.13005
34.
ZhaoZ, WuM, ZhanY, ZhanK, ChangX, YangH, LiZ. Characterization and purification of anthocyanins from black peanut (Arachis hypogaea L.) skin by combined column chromatography. J Chromatogr A. 1519;1519:74–82. doi: 10.1016/j.chroma.2017.08.078
35.
MeliR, AutoreG, Di CarloG, CapassoF. Inhibitory action of quercetin on intestinal transit in mice. Phytother Res. 1990;4:201–2. doi: 10.1002/ptr.2650040509
36.
Di CarloG, MascoloN, IzzoA, CapassoF, AutoreG. Effects of quercetin on the gastrointestinal tract in rats and mice. Phytother Res. 1994;8:42–5. doi: 10.1002/ptr.2650080110
37.
HammadH, AbdallaS. Pharmacological effects of selected flavonoids on rat isolated ileum: Structure-activity relationship. Gen Pharmacol. 1997;28:767–71. doi: 10.1016/S0306-3623(96)00299-6
38.
RevueltaM, CantabranaB, HidalgoA. Depolarization-dependent effect of flavonoids in rat uterine smooth muscle contraction elicited by CaCl2. Gen Pharmacol. 1997;29:847–57. doi: 10.1016/S0306-3623(97)00002-5
39.
RotondoA, SerioR, MuleF. Gastric relaxation induced by apigenin and quercet: Analysis of the mechanism of action. Life Sci. 2009;85:85–90. doi: 10.1016/j.lfs.2009.04.022
40.
Santos-FagundesD, GrasaL, GonzaloS, ValeroMS, CastroM, ArrueboMP, et al.Different mechanisms of actions of genistein and quercetin on spontaneous contractions of rabbit duodenum. Rev Esp Enferm Dig. 2015;107:413–6. doi: 1130-0108/2015/107/7/413-416
41.
MoralesMA, TortorielloJ, MeckesM, PazD, LozoyaX. Calcium-antagonist effect of quercetin and its relation with the spasmolytic properties of Psidium guajava L. Arch Med Res. 1994;25, 17–21.
42.
GoyalRK, HiranoI. The enteric nervous system. N Engl J Med. 1996;334:1106–15. doi: 10.1056/NEJM199604253341707
43.
GilaniA, KhanA, RaoofM, GhayuorM, SiddiquiB, VohraW, et al.Gastrointestinal, selective airways and urinary bladder relaxant effect of Hyoscyamus niger are mediated through dual blockade of muscarinic receptors and Ca2+ channels. Fundam Clin Pharmacol. 2008;22:87–99. doi: 10.1111/j.1472-8206.2007.00561.x
44.
PavlovicRD, VeljkovicM, StojanovicMN, Gocmanac-IgnjatovicM, Mihajilov-KrstevT, BrankovicS, et al.Influence of different wild garlic (Allium ursinum) extracts on the gastrointestinal system: Spasmolytic, antimicrobial and antioxidant properties. J Pharm Pharmacol. 2017;69:1208–18. doi: 10.1111/jphp.12746
45.
BrankovićS, Gočmanac IgnjatovićM, KostićM, VeljkovićM, MiladinovićB, MilutinovićM, et al.Spasmolytic activity of the aqueous and ethanol celery leaves (Apium graveolens L.) extracts on the contraction of isolated rat ileum. Acta Med Median. 2015;54:11–6. doi: 10.5633/amm.2015.0202
46.
Gočmanac IgnjatovićM, KitićD, KostićM, MiladinovićB, MilutinovićM, VeljkovićM, et al.Spasmolytic effect of Anethum graveolens L. methanol extract on isolated rat ileum, Acta Med Median. 2015;54:5–10. doi: 10.5633/amm.2015.0201
47.
OmaraE, PavlovicI, DrobacM, RadenkovicM, BrankovicS, KovacevicN. Chemical composition and spasmolytic activity of Cymbopogon nervatus (Hochst.) Chiov. (Poaceae) essential oil. Ind Crops Prod. 2016;91:249–54. doi: 10.1016/j.indcrop.2016.07.013.
48.
PavlovicI, OmaraE, DrobacM, RadenkovicM, BrankovicS, KovacevicN. Chemical composition and spasmolytic activity of Cymbopogon schoenanthus (L.) Spreng. (Poaceae) essential oil from Sudan. Arch Biol Sci. 2017;69:409–15. doi: 10.2298/ABS160506113P
49.
PavlovićD, BrankovićS, KovačevićN, KitićD, VeljkovicS. Comparative study of spasmolytic properties, antioxidant activity and phenolic content of Arbutus unedo from Montenegro and Greece. Phytother Res. 2011;25:749–54. doi: 10.1002/ptr.3460
50.
KiticD, BrankovicS, RadenkovicM, SavikinK, ZdunicG, KocicB, et al.Hypotensive, vasorelaxant and cardiodepressant activities of the ethanol extract of Sideritis raeseri spp. raeseri boiss & heldr. J Physiol Pharmacol. 2012;63, 531–5.
51.
WalshJV, SingerJJ. Calcium action potentials in single freshly isolated smooth muscle cells. Am J Physiol. 1980;239:C162–C174. doi: 10.1152/ajpcell.1980.239.5.C162
52.
HuJ, GaoWY, GaoY, LingNS, HuangLQ, LiuCX. M3 muscarinic receptor- and Ca2+ influx-mediated muscle contractions induced by croton oil in isolated rabbit jejunum. J Ethnopharmacol. 2010;129:377–80. doi: 10.1016/j.jep.2010.04.020
53.
HuJ, GaoWY, MaL, ManSL, HuangLQ, LiuCX. Activation of M3 muscarinic receptor and Ca2 + influx by crude fraction from Crotonis fructus in isolated rabbit jejunum. J Ethnopharmacol. 2012;139:136–41. doi: 10.1016/j.jep.2011.10.041
54.
KarakiH, WiesG. Mini-review: Calcium release in smooth muscles. Life Sci. 1983;13:111–2. doi: 10.1016/0024-3205(88)90674-1
KarakiH, SatakeN, ShibataS. Mechanism of barium-induced contraction in the vascular smooth muscle of rabbit aorta. Br J Pharmacol. 1986;88, 821–6.
57.
HemmingJM, GuarraciFA, FirthTA, JenningsLJ, NelsonMT, MaweGM. Actions of histamine on muscle and ganglia of the guinea pig gallbladder. Am J Physiol Gastrointest Liver Physiol. 2000;279, G622–G630.
58.
MatsumotoT, HoriuchiM, KamataK, SeyamaY. Effects of Bidens pilosa L. var. radiata SCHERFF treated with enzyme on histamine-induced contraction of guinea pig ileum and on histamine release from mast cells. J Smooth Muscle Res. 2004;45, 75–86.
59.
AliN, AleemU, Ali ShahSW, ShahI, JunaidM, AhmedG, et al.Acute toxicity, brine shrimp cytotoxicity, anthelmintic and relaxant potentials of fruits of Rubus fruticosus Agg. BMC Complem Altern Med. 2013;13:138–49. doi: 10.1186/1472-6882-13-138
60.
MiladinovicB, BrankovicS, KosticM, MilutinovicM, KiticN, ŠavikinK, et al.Antispasmodic effect of black currant (Ribes nigrum L.) juice and its potential use as functional food in gastrointestinal disorders. Med Princ Pract. 2018;27:179–85. doi: 10.1159/000487202
