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Reanlatorv Mechanisms
in Biosysiems
Regulatory Mechanisms
in Biosystems
ISSN 2519-8521 (Print) ISSN 2520-2588 (Online) Regul. Mech. Biosyst., 2020, 11(2), 305-309 doi: 10.15421/022046
Antibacterial and fungicidal activities of ethanol extracts
from Cotinus coggygria, Rhus typhina, R. trilobata, Toxicodendron orientale,
Hedera helix, Aralia elata, Leptopus chinensis and Mahonia aquifolium
V. V. Zazharskyi*, P. O. Davydenko*, O. M. Kulishenko*, I. V. Borovik*, V. V. Brygadyrenko**
Zazharskyi, V. V., Davydenko, P. O., Kulishenko, O. M, Borovik, I V., & Brygadyrenko, V. V. (2020). Antibacterial andfungicidal activities of ethanol extracts from Cotinus coggygria, Rhus typhina, R trilobata, Toxicodendron Orientale, Hedera helix, Aralia elata, Leptopus chinensis and Mahonia aquifolium. Regulatory Mechanisms in Biosystems, 11(2), 305-309. doi:10.15421/022046
The search for promising plants with bactericidal and fungicidal activity is of great interest for practical and veterinary medicine, This article reveals the high antibacterial effect of the use of ethanol extracts from 8 species of plants of the families Anacardiaceae (Cotinus coggygria Scop., Rhus typhina L., Rhus trilobata Nutt. and Toxicodendron Orientale Greene), Araliaceae (Hedera helix Linnaeus and Aralia elata (Miq.) Seem.), Phyllanthaceae (Leptopus chinensis (Bunge) Pojark.), Berberidaceae (Mahonia aquifolium (Pursh) Nutt.) against 23 strains of bacteria and one strain of fungi. The in vitro experiment revealed the zone of inhibition of growth of colonies exceeding 8 mm during the application of ethanol extracts of C. coggygria against twelve species of microorganisms (Entero-coccus faecalis, Escherichia coli, Staphylococcus aureus, S. epidermidLs, Bacillus cereus, Listeria ivanovi, Corynebacterium xerosis, Rhodococcus equi, Proteus vulgaris, P. mirabilis, Serratia marcescens and Candida albicans), Rhus typhina - against twelve species (E. faecalis, E. coli, S. aureus, S. epidermidis, L. ivanovi, C. xerosis, Rh. equi, P. vulgaris, Salmonella typhimurium, S. adobraco, S. marcescens and C. albicans), Rhus trilobata - against fourteen (E. faecalis, E. coli, S. aureus, S. epidermidis, B. subtilis, B. cereus, L. ivanovi, C. xerosis, Rh. equi, P. vulgaris, P. mirabilis, Pseudomonas aeruginosa, Yersinia enterocolitica and C. albicans), Toxicodendron orientale - against eleven (E. faecalis, S. aureus, L. innocua, C. xerosis, Campylobacter jejuni, Rh. equi, P. vulgaris, P. mirabilis, P. aeruginosa and C. albicans), Hedera helix - against seven (S. aureus, S. epidermidis, L. monocytogenes, C. jejuni, Rh. equi, P. vulgaris and C. albicans), Aralia elata - against nine (E. coli, S. aureus, B. cereus, C. xerosis, P. vulgaris, P. mirabilis, S. typhimurium, S. marcescens and C. albicans), Leptopus chinensis - only against four (E. coli, S. epidermidis, B. cereus and P. mirabilis) and Mahonia aquifolium - against only three species (S. epidermidis, C.jejuni and P. vulgaris). As a result of the research, the most promising for studying in future regarding in vivo antibacterial activity were determined to be C. coggygria, Rhus typhina, R trilobata, Toxicodendron orientale and Aralia elata.
Keywords: growth inhibition zone; bacterial colonies; poly-resistant strain; candidiasis.
*Dnipro State Agrarian and Economic University, Dnipro, Ukraine **Oles Honchar Dnipro National University, Dnipro, Ukraine
Article info
Received 20.03.2020 Received in revisedform
14.04.2020 Accepted 16.04.2020
Dnipro State Agrarian and Economic University, Sergiy Efremov st., 25, Dnipro, 49000, Ukraine. Tel.: +38-056-713-51-74. E-mail:
zazharskiyv@gmail. com
Oles Honchar Dnipro National University, Gagarin av., 72, Dnipro, 49010, Ukraine. Tel.: +38-050-93-90-788. E-mail: brigad@ua.fm
Introduction
Recently, reports have appeared with increasing frequency about the potential possibilities of the search for effective antibacterial substances in plant extracts in the context of the spread of antibiotic poly-resistant strains which aie hard to treat (Zazharskyi et al., 2019a; Palchykov et al., 2020). Natural products produced by Embryophyta as secondary metabolites were found to be a rich source of biologically active compounds which may be the basis for the development of novel chemical substances for pharmaceutical preparations (Boyko & Brygadyrenko, 2016; Zazharskyi et al., 2019b; Palchykov et al., 2019). Plants contain a diverse group of very valuable and available resources of secondary metabolites, such as tannins, terpenoids, alkaloids and flavonoids with important pharmacological properties (Georgiev et al., 2014; Jeruto et al., 2017; Hussein & El-Anssary, 2019; Zazharskyi et al., 2019c). In general, herbal essential oils and extracts of many species of plants are considered as non-phytotoxic compounds and until now were surveyed only for presence of different types of biological activity, and their antimicrobial, anti-inflammatory, an-tioxidant, antimutagenic and anticancer effect have been partly described (Giriiaju & Yunus, 2013; Matic et al., 2013; Kchaou et al., 2014).
Cotinus coggygria Scop., also known as smoke tree, is one of two species which compose a small genus of the Anacardiaceae family. It has
a wide range extending from Southern Europe, the Mediterranean, Moldova and the Caucasus to Central China and the Himalayas (Novakovic et al., 2007). This plant is usually considered a large bush or small tree. The leaves are glaucous, simple, ovoid, 3-8 cm long. The flowers are pentagonal, pale yellow or yellow-green, hermaphrodite, or some of them are abortive, with long pedicels, in indeterminate inflorescences.
Plants of the Anacardiaceae family are well-known for their cultivated edible fruits and seeds, dermatitis-causing taxa (for example, Comoc-ladia, Metopium, Semecarpus, Toxicodendron), medical compounds, valuable timber and varnish-bearing plants (Toxicodendron and Gluta). Many species of Anacardiaceae are also valuable for their attractiveness in gardens. Specimens of Rhus, Schinus, Searsia, Pistacia chinensis Bunge, P. mexicana Kunth, Smodingium and Toxicodendron are attractive because of their beautiful inflorescences, evergreen or bright-coluored autumn leaves. Some products of the species of the Anacardiaceae family, including mango (Mangifera indica L. and other species), pistachio (Pistacia vera L.), cashew (Anacardium occidentale L.) and rose pepper (Schinus terebinthifolius L.) are used in food all around the globe.
Rhus typhina L. is a fast-growing species which reproduces by rhizomes and seeds. Due to its biological advantages, this deciduous species of the Anacardiaceae family has been brought to urbanized landscapes of Ukraine from native areas in the East of North America. Dzhygan et al.
(2018) analyzed the changes in morphometric and physiological parameters of 12-year old plants of this species in artificial phytocenoses near the roads in Pavlohrad (Ukraine). Compared with plants in relatively clean zone, the greatest decrease in the length of annual shoots of the trees was observed in those at the distance of25-40 m from the highway. Leaves of R. typhina contain several galloyltransferases which catalyze P-glucogal-lin-dependent transformation of 1,2,3,4,6-pentagalloylglucose to gallotan-nins, have excellent thermostability and high tolerance to cold (Niemetz & Gross, 2001). Allelopathy plays a role in the formation of resistance of R typhina to invasion (Wei et al., 2017). Wang & Zhu (2017) suggest using R typhina as an antioxidant in food, nutraceutical and cosmetic industries.
Methanol extract of leaves of C. coggygria was tested against seven strains of bacteria (B. subtilis, S. aureus, E. coli, E. aerogenes, K. pneumoniae, P. vulgaris and P. aeruginosa) using the method of disk diffusion. Extract from C. coggygria in the concentration of 10, 20 ^ig/mL and 1 mg/mL displayed moderate effect on all the named strains of bacteria (Singh et al., 2012).
Method of diffusion in agar was used to assess the activity of hexane, ethanolic and aqueous extracts from C. coggygria in the concentrations of 12.5, 25 and 50 mg/mL towards Streptococcus mutans, S. sobrinus, Lactobacillus casei and Actinomyces viscosus. Water and ethanolic extracts of C. coggygria demonstrated significant activity against all four indicated bacteria in all of the tested concentrations (F errazzano et al., 2013).
Essential oils from leaves with young shoots of C. coggygria in Serbia were tested for antibacterial and antifungal activities (Novakovic et al., 2007). Essential oil produced inhibition zones measuring 6-23 mm. The largest inhibition zones were observed against species of Staphylococcus and Micrococcus genera, while the smallest were observed against Proteus mirabilis. Essential oil exerted higher antibacterial activity than streptomycin, which was used as positive control, except in the case of P. mirabilis. Bacteriostatic activity of the oil ranged within the concentrations of 2.5-5.0 ^iL/mL, while its bactericidal concentration - 2.510.0 |iL/mL.
There are two major ways of action of antiviral agents: the first one is inhibiting infection, and the other is inhibition of replication of virus. The activity of the extract from C. coggygria against infection and replication was determined using the methods of local effect and disk method (Jing et al., 2012). Ethanol extract from leaves of C. coggygria exhibited especially strong inhibiting activity towards the infection with Tobacco mosaic virus (TMV - 93.5%), and significantly inhibited the replication of this virus (38.2%).
Ilczuk & Jacygrad (2016) assessed the efficiency of aqueous extract from C. coggygria in an in vitro experiment against the tissue factor in the samples of saliva obtained from clinically healthy people. Extract from C. coggygria caused increase in the buffer ability of the saliva, decrease in the number of bacteria and prevented the aggregation of bacteria.
Rendekova et al. (2015) determined the anti-biofilm activity of extract from C. coggygria against two strains from the collection and ten clinical strains of S. aureus. The tested extract exerted bactericidal activity against all strains of S. aureus, particularly strains sensitive to meticyllin (in the concentrations of 0.313-0.625 mg/mL) The concentrations of extract from C. coggygria which inhibited the formation of biofilm were 10-100 times higher (up to 32 mg/mL). Phytochemical analysis of C. coggygria detected quercetin, rhamnoside, methyl gallate and methyl trigallate as the
main constituents of the extract. The results of the research revealed that C. coggygria is rich in tannins and flavonoids and is a promising local antibacterial preparation with anti-biofilm activity (Rendekova et al., 2015). C. coggygria is a commercial decorative plant with broad range of medical use. It is one of the most important species of trees used in ecological and landscape plantations in China, the main component ofthe landscape formed of red leaves in Beijing region in autumn (Wang et al., 2012; Fraternale & Ricci, 2018).
Species of the Hedera genus are widely used in greening. Researchers from Dresden University of Applied Sciences (Germany) are undertaking surveys on hydroponic facing of facades using Hedera (Koleva, 2015), as well as possibility of future optimization of these new ecosystems.
Hu & Wang (2008) demonstrated that arasolide A obtained from the seeds of Aralia elata (Miq.) Seem.) has anti-inflammatory activity which inhibits the production ofNO and anti-cancer activity against SNU, cancer cells of AGS and cancer cells of melanoma, despite its low antioxidant activity. Hu & Wang (2008) presume that triterpene saponins from A. elata can play important role in displaying antibacterial and neuropro-tective properties of tinctures ofthe plant.
Fadiloglu & Qoban (2019) state that alcohol extract of Rhus trilobata Nutt. may be used as a natural antioxidant, antibacterial agent and glaze material for slowing of the oxidation of lipids and inhibition of loss of quality of frozen fish.
Zhang & Shi (2020) presume that correct addition of Leptopus chi-nensis (Bunge) Pojark. could be one of the strategies of feeding which improve the digestion and digestion of dietary fibre and potentially reduce deficiency in quality feed for ruminant animals, modeling the microbial community of scar.
Therefore, the species of plants we analyze in this paper remain unstudied regarding their antimicrobial activity and could have a significant potential for human and veterinary medicine. The objective of this article was determining the antibacterial effect of ethanol extracts from Cotinus coggygria, Rhus typhina, R trilobata, Toxicodendron orientale, Hedera helix, Aralia elata, Leptopus chinensis and Mahonia aquifolium on separate species of microorganisms in in vitro experiments.
Materials and methods
The leaves and shoots of eight species of plants (Table 1) were collected in the territory ofthe Botanical Garden of Oles Honchar Dnipro National University (Khromykh et al., 2018; Boyko & Brygadyrenko, 2019), dried at room temperature, fragmented, weighed and maintained for 10 days in 70% ethyl alcohol, and filtered.
Antibacterial activity of the plant tinctures were determined using disk diffusion in agar. From daily culture of ethanol strains of microorganisms, we prepared weighed amounts according to the standard of opacity of bacterial suspension equaling 0.5 units of density according to McFarland (McF) 1.5 x 108 CFU (colony-forming units), which was determined using a densitometer (Densimeter II).
The obtained weighed amount was inoculated to Muller-Hinton agar (Himedia) with subsequent cultivation in TC0-80/1 thermostat for 24 h at the temperature of 37 °C. On top ofthe inoculations, we put disks saturated with the tinctures of the extracted ethanol tinctures of four species of plants (Table 1).
Table 1
Used part of four species ofplants and the most important information on their antibacterial activity
Family
Species
Used part of 1he plant
Literature sources about Hie action of plants on bacteria
Cotinus coggygria Scop. shoots Novakovic et al. (2007)
Anacardiaceae Rhus trilobata Nutt. shoots Pfeiffer & Drinnenberg (2010)
R typhina L. leaves Kossah et al. (2011), Zhu et al. (2020)
Toxicodendron orientale Greene leaves Zhao & Zhu (2014), Kruger (2017)
Araliaceae Hedera helix Linnaeus leaves Pane et al. (2007), Pollet et al. (2009), Strelau et al. (2018)
Aralia elata (Miq.) Seem. leaves Zhang et al. (2018)
Phyllanthaceae Leptopus chinensis (Bunge) Pojark. leaves Zhang & Shi (2020)
Berberidaceae Mahonia aquifolium (Pursh) Nutt. shoots Sochorova R. (1998)
As positive control, we used disks with 15.0 ^g of azithromycin - also used as a second control against C. albicans (Valle et al., 2015). After 9-deoxo-9a-aza-9a-methyl-9a-homoerythromycin A - macrolide antibio- 24 h, the growth of the culture was assessed using antibiotic zone scale for tic of broad spectrum of action. Discs with 15.0 ^g amphotericinin were measuring the growth inhibition zones of microorganisms (Antibiotic
Zone Scale-C, model PW297, India) and software TpsDig2 (F. James Rohlf, 2016). The data in tables are presented as x ± SD (standard deviation).
Results
Prevention of growth of separate strains of microorganisms was seen under the influence of ethanol extracts from the studied plants (Table 2, 3).
C. coggygria exhibited the highest inhibiting activity, slowing the growth of E. faecalis (10.2 mm, hereafter the average radius of growth inhibition zone is indicated in mm), two strains ofE. coli (F50 and 055 -16.4 and 12.4 mm respectively), Proteus vulgaris (10.7), P. mirabilis (12.4), S. marcescens (13.7) during moderate slowing of growth for
Table 2
The width of zone of growth inhibition (mm) for the ethanol extracts ofAnacardiaceae families against 24 strains of microorganisms (n = 8)
Y. enterocolitica (5.7). The extract from Rhus typhina competed with C. coggygria for influence on E. faecalis (11.3), E. coli F50 (12.5), S. aureus and S. epidermidis (8.3 and 10.7), L. ivanovi (9.7), C. xerosis (11.7), Rh. equi (10.3), P. vulgaris (9.6), S. typhimurium and S. adobraco (10.2 and 10.6), S. marcescens (12.3) and C. albicans (9.3), and at the same time moderately slowed the growth ofB. subtilis (3.5), P. mirabilis (7.8), P. aeruginosa ATCC 2799 (6.3) and Y. enterocolitica (4.5). Antibacterial effectiveness was determined for alcohol extract of R trilobata against E. faecalis (10.4), E. coli 055 (11.4), P. vulgaris and P. mirabilis (11.7 and 20.7), Y. enterocolitica (11.3), it also moderately slowed the growth of P. aeruginosa (4.2). Extract of T. orientale had notable inhibiting activity towards E. faecalis (12.7), P. vulgaris (10.5), moderate activity towards E. coli 055 (6.8) and P. mirabilis (8.7).
Strains of microorganisms Cotinus coggygria Rhus typhina Rhus trilobata Toxicodendron orientale Control*
Enterococcus faecalis ATCC 19433 10.2 ± 1.32 11.3 ± 1.13 10.4 ± 0.78 12.7 ± 1.34 23.9 ± 2.45
Enterobacter aegorenes ATCC 10006 2.7 ± 0.19 1.6 ± 0.14 4.2 ± 0.42 2.6 ± 0.41 15.9 ± 1.67
Escherichia coli F50 16.4 ± 1.56 12.5 ± 1.24 0 ± 0 1.5 ± 0.16 17.8 ± 1.87
E. coli 055 12.4 ± 1.34 0 ± 0 11.4 ± 1.43 6.8 ± 0.55 15.6 ± 1.62
Staphylococcus aureus ATCC 25923 13.3 ± 1.12 8.3 ± 0.46 15.8 ± 1.29 10.8 ± 0.87 21.6 ± 2.45
S. epidermidis ATCC 14990 11.9 ± 1.54 10.7 ± 1.22 14.4 ± 0.78 0 ± 0 10.3 ± 1.34
Bacillus subtilis ATCC 6633 0 ± 0 3.5 ± 0.86 12.8 ± 1.45 4.5 ± 0.77 30.3 ± 3.05
B. cereus ATCC 10702 12.6 ± 1.43 2.3 ± 0.89 9.5 ± 1.76 4.2 ± 0.92 16.8 ± 1.86
Listeria ivanovi 9.8 ± 0.7 9.7 ± 0.87 9.9 ± 0.77 4.3 ± 0.32 14.7 ± 1.21
L. innocua ATCC 33090 0 ± 0 0 ± 0 0 ± 0 10.7 ± 1.41 25.1 ± 1.98
L. monocytogenes ATCC 19112 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0
Corynebacterium xerosis 1911 15.8 ± 1.45 11.7 ± 1.23 11.5 ± 0.78 11.7 ± 0.79 9.3 ± 1.34
Campylobacter jejuni ATCC 11322 0 ± 0 0 ± 0 0 ± 0 12.7 ± 1.43 0 ± 0
Rhodococcus equi ATCC 6939 11.7 ± 0.83 10.3 ± 0.12 12.6 ± 1.36 10.2 ± 0.89 19.1 ± 1.98
Proteus vulgaris ATCC 13315 10.7 ± 1.22 9.6 ± 0.86 11.7 ± 1.28 10.5 ± 1.12 0 ± 0
P. mirabilis ATCC 14153 12.4 ± 1.21 7.8 ± 0.88 20.7 ± 2.24 8.7 ± 0.67 0 ± 0
Salmonella typhimurium ATCC 14028 0 ± 0 10.2 ± 0.96 0 ± 0 1.7 ± 0.33 20.3 ± 1.54
S. adobraco 1 0 ± 0 10.6 ± 0.89 0 ± 0 0 ± 0 26.3 ± 2.76
Pseudomonas aeruginosa ATCC 2353 0 ± 0 0 ± 0 10.1 ± 0.88 17.4 ± 1.54 0 ± 0
P. aeruginosa ATCC 2799 0 ± 0 6.3 ± 0.41 6.5 ± 0.65 6.3 ± 0.67 0 ± 0
Klebsiella pneumoniae ATCC 13883 0 ± 0 1.3 ± 0.14 0 ± 0 1.3 ± 0.13 0 ± 0
Yersinia enterocolitica ATCC 9610 5.7 ± 0.45 4.5 ± 0.25 11.3 ± 0.94 2.3 ± 0.35 12.8 ± 1.27
Serratia marcescens ATCC 8100 13.7 ± 1.45 12.3 ± 1.09 0 ± 0 2.8 ± 0.25 0 ± 0
Candida albicans ATCC 2091 11.2 ± 1.38 9.3 ± 0.89 16.8 ± 1.78 17.8 ± 1.78 0 ± 0* / 2.4 ± 0.21**
Note: * - discs with 15.0 ^g of azithromycin were used for all bacteria as positive control; ** - discs with 15.0 |jg amphotericinin were used as positive control for C. albicans.
Table 3
Width of growth inhibition zone (mm) produced by ethanol extracts of Hedera helix, Aralia elata, Leptopus chinensis and Mahonia aquifolium against 24 strains of microorganisms (n = 8)
Strains of microorganisms Hedera helix Aralia elata Leptopus chinensis Mahonia aquifolium Control*
Enterococcus faecalis ATCC 19433 0 ± 0 0 ± 0 0 ± 0 3.2 ± 0.65 23.9 ± 2.45
Enterobacter aegorenes ATCC 10006 0 ± 0 1.3 ± 0.17 0 ± 0 1.3 ± 0.14 15.9 ± 1.67
Escherichia coli F50 3.8 ± 0.34 11.9 ± 1.16 11.5 ± 0.78 1,5±0,12 17.8 ± 1.87
E. coli 055 0 ± 0 10.6 ± 0.98 3,6 ± 0.32 2,7±0,43 15.6 ± 1.62
Staphylococcus aureus ATCC 25923 23.5 ± 2.78 9.7 ± 0.78 2.6 ± 0.21 2.8 ± 0.19 21.6 ± 2.45
S. epidermidis ATCC 14990 26.3 ± 2.15 0 ± 0 18.7 ± 1.78 21.6 ± 2.34 10.3 ± 1.34
Bacillus subtilis ATCC 6633 0 ± 0 0 ± 0 0 ± 0 2.2 ± 0.67 30.3 ± 3.05
B. cereus ATCC 10702 0 ± 0 15.8 ± 2.34 10.8 ± 0.98 4.7 ± 1.21 16.8 ± 1.86
Listeria ivanovi 0 ± 0 0 ± 0 1.6 ± 0.19 0 ± 0 14.7 ± 1.21
L. innocua ATCC 33090 0 ± 0 0 ± 0 0 ± 0 0 ± 0 25.1 ± 1.98
L. monocytogenes ATCC 19112 9.3 ± 1.22 0 ± 0 0 ± 0 2.1 ± 0.34 0 ± 0
Corynebacterium xerosis 1911 4.4 ± 0.19 8.4 ± 0.89 0 ± 0 3.6 ± 0.21 9.3 ± 1.34
Campylobacter jejuni ATCC 11322 12.4 ± 1.26 0 ± 0 2.4 ± 0.32 17.5 ± 1.43 0 ± 0
Rhodococcus equi ATCC 6939 11.8 ± 0.77 2.2 ± 0.18 1.3 ± 0.13 1.6 ± 0.21 19.1 ± 1.98
Proteus vulgaris ATCC 13315 10.8 ± 1.21 9.3 ± 1.11 4.2 ± 0.77 9.4 ± 0.97 0 ± 0
P. mirabilis ATCC 14153 1.5 ± 0.14 14.7 ± 1.34 10.6 ± 0.68 4.3 ± 0.43 0 ± 0
Salmonella typhimurium ATCC 14028 5.4 ± 0.77 9.7 ± 0.76 0 ± 0 1.4 ± 0.18 20.3 ± 1.54
S. adobraco 1 0 ± 0 4.4 ± 0.57 2.3 ± 0.22 7.2 ± 0.76 26.3 ± 2.76
Pseudomonas aeruginosa ATCC 2353 2.8 ± 0.54 0 ± 0 0 ± 0 0 ± 0 0 ± 0
P. aeruginosa ATCC 2799 2.3 ± 0.45 0 ± 0 0 ± 0 2.2 ± 0.34 0 ± 0
Klebsiella pneumoniae ATCC 13883 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0
Yersinia enterocolitica ATCC 9610 4.6 ± 0.32 0 ± 0 0 ± 0 0 ± 0 12.8 ± 1.27
Serratia marcescens ATCC 8100 2.8 ± 0.35 8.2 ± 0.78 3.5 ± 0.34 1.1 ± 0.16 0 ± 0
Candida albicans ATCC 2091 10.7 ± 1.03 13.6 ± 1.45 2.6 ± 0.32 5.7 ± 0.45 0 ± 0* / 2.4 ± 0.21**
Note: see Table 2.
Antibacterial effect was determined for the extracts ofR trilobata and (growth inhibition zone of 0 mm). Also, significant inhibiting effect of the T. orientale on P. aeruginosa (10.1 and 17.4); T. orientale - against tested alcohol extracts should be noted against S. aureus (15.8 and C. jejuni (12.7), both of which had antibiotic resistance to azithromycin 10.8 mm, respectively). During the study on the influence of the extracts
on the microorganisms of the Bacillaceae family, notable impact was observed for C. coggygria on B. cereus (12.6) and R trilobata on B. subti-lis and B. cereus (12.8 and 9.5). Moderate and high inhibitory effects on the microorganisms of the Listeriaaceae family: C. coggygria slowed the growth of L. ivanovi (9.8), T. orientale - L. innocua (10.7). Azitromycin was not effective against L monocytogenes (0 mm). There was seen high inhibiting effect of the extracts from C. coggygria, R trilobata and T. orientale against C. xerosis (15.8, 11.5, 11.7), Rh. equi (11.7, 12.6, 10.2) and C. albicans (11.2, 16.8 and 17.8 mm, respectively). At the same time, the radius of the zone of inhibition of growth produced by amphoterici-num equaled only 2.4 mm.
Against the background of effective inhibition of microorganisms E. faecalis, E. coli 055 (except Rhus typhina), S. aureus, S. epidermidis (except T. orientale), L. ivanovi, C. xerosis, Rh. equi, P. vulgaris, P. mirabilis and C. albicans by ethanol extracts of plants of the Anacardiaceae family, we should note antibiotic-resistance of P. vulgaris, P. mirabilis, K. pneumoniae, S. marcescens to azithromycin (0 mm).
Extracts from H. helix, L. chinensis and M aquifolium have high inhibitory effect on S. epidermidis (26.3, 18.7 and 21.6 mm), at the same time the growth inhibition zone exceeded the control by 16.0, 8.4 and 11.3 mm; H. helix and A. elata showed impact against S. aureus (23.5 and 9.7 mm), C. albicans (10.7 and 13.6 mm), H. helix, A. elata and M. aquifolium against P. vulgaris (10.8, 9.3 and 9.4 mm), A. elata and L. chinensis - E. coli F50 (11.9 and 11.5 mm), B. cereus (15.8 and 10.8 mm), P. mirabilis (14.7 and 10.6 mm), H. helix andM. aquifolium -C. jejuni (12.4 and 17.5 mm).
Furthermore, high antibacterial effect of H. helix was displayed against L. monocytogenes (9.3), A. elata - E. coli 055 (10.6), S. typhimurium (9.7), while M. aquifolium moderately inhibited S. adobraco and C. albicans (7.2 and 5.7 mm). Antibiotic resistance was determined for L. monocytogenes, C. jejuni, P. vulgaris, P. mirabilis, P. aeruginosa, K. pneumoniae, S. marcescens to the control group (azithromycin 0) and C. albicans to amphotericinin (2.4).
Discussion
Antimicrobial activity of ethanol extract of C. coggygria was surveyed by Milosevic et al. (2008). Extracts from leaves of C. coggygria inhibited S. aureus and P. aeruginosa, producing growth inhibition zones of 13 and 10 mm. Despite the fact that C. albicans and E. coli were included in this study, Milosevic et al. (2008) did not report about inhibition of these microorganisms.
Antibacterial activity of extracts from leaves of C. coggygria growing mostly naturally in Turkey (Han et al., 2009), prepared using different solvents, was determined using disk diffusion method. The extract was found to be most efficient against E. faecalis (diameter of the inhibition zone of 20 mm) in distilled water, and methanol extract was most effective against S. aureus, S. epidermidis and E. faecalis (Han et al., 2009). Antimicrobial activity expressed as minimum inhibitory concentration (MIC) of acetone extract and fractions obtained from young shoots of C. coggygria ranged 3-200 mg/mL (MarcetiC et al., 2012). Acetone extract inhibited the growth of Gram-positive bacteria S. epidermidis (MIC = 25 mg/mL) and S. aureus (MIC = 25 mg/mL), whereas the ethyl acetate fraction was active against B. subtilis (MIC = 25 mg/mL), K. pneumoniae (MIC = 50 mg/mL) and E. coli (MIC = 50 mg/mL). The greatest activity with chloroform fraction was seen towards C. albicans yeasts (MIC = 3.1 mg/mL), more efficiently than with the control antifungal preparation - nystatin (6.2 mg/mL).
Hooshyar et al. (2014) recommend further research on the use of the main constituents of H. helix, especially hederasaponin (saponin K10), to study the antileishmanial activity towards L. major. Shckorbatov (2017) recommends using H. helix in the sphere of food chemistry, food technologies and nutraceutical studies (for diet-therapy and cosmetics).
García-Ramírez et al. (2016) studied in vitro anti-amoebic activity of extracts from fruits and stems ofRhus trilobata towards Entamoeba histolytica. Also, Varela-Rodríguez et al. (2019) report that flavonoids, phenolic and fatty acids, and also quercetin, methyl gallate, epigallocatechin 3-cinnamate, fisetin and margaric acid, included in the content ofR trilobata, can have anti-cancer properties.
Aschenbeck & Hylwa (2017) consider that Toxicodendron orientale has local antibacterial effect.
Ethanolic tincture of Aralia elata (Brygadyrenko et al., 2019) exerted low immunosuppressive action, in the conditions of high fat diet, leading to increase in the quantity of typical Escherichia coli, decrease in Enterococcus spp. and Enterobacter spp. High concentrations of it (0.1% ethanolic tincture of A. elata) killed bacteria of Clostridium and Klebsiella genera and various yeast fungi in the intestine. Male rats on a diet with excess of fat were observed to have no serious changes in the composition of the normal gut microbiota (Bifidobacterium spp., Lactobacillus spp., Proteus spp., Staphylococcus spp., Candida spp.), and no lactose-negative enterobacteria (Citrobacter genus) were detected.
R. typhina decreases the diversity of the soil bacterial community compared with other species of plants: soil was characterized by higher number of Actinobacteria and lower Proteobacteria and Acidobacteria (Zhu et al., 2020). A difference was found in the relative amount of No-cardioides and Streptomyces, which may be useful for the growth of R. typhina. Concentration of total carbon, potassium and nitrates are the main soil factors which affect the relative number of soil bacteria. Extract from R. typhina exhibited strong antimicrobial activity depending on the concentration and broad spectrum towards the tested bacteria of Bacillus cereus and Helicobacter pylori with MIC equaling 0.10%. Yeasts displayed lower susceptibility with MIC of0.60-0.75%. Furthermore, Zhang et al. (2018) surveyed the antioxidant activity of the extract, including the absorbing activity of radicals 2,2-diphenyl-1 picrylhydrazyl (DPPH, MIC = 0.016 mg/mL) (Kossah et al., 2011). Extract of Mahonia aquifolium is recommended for the treatment of psoriasis in humans (Sochorova, 1998; Na, 2006).
Conclusion
Thus, all the 8 surveyed species of plants have no notable antibacterial effect against multi-resistant strains Enterobacter aegorenes, Listeria innocua, P. aeruginosa ATCC 2799, K. pneumoniae. High inhibitory effect was determined for ethanol extracts from Cotinus coggygria against 13 strains of microorganisms, Rhus typhina - against 12, Rhus trilobata -14, Toxicodendron orientale - 10, Hedera helix -7, Aralia elata -10, Leptopus chinensis -4 and Mahonia aquifolium - 3 of 24 surveyed poly-resistant strains of bacteria and fungi. We think that it is possible to recommend the extracts from C. coggygria, R. typhina, R. trilobata, T. orientale, H. helix, A. elata, L. chinensis and M aquifolium or individual compounds they contain for further study of methods against poly-resistant strains of the abovementioned microorganisms.
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