Chemical and biological characteristics of propolis from Apis mellifera caucasica from the Ardahan and Erzurum provinces of Turkey: a comparative study

Mehmet Arslan; Yusuf Sevgiler; Celal Güven; Zehra Tuğba Murathan; Nurcan Erbil; Deniz Yıldırım; Mehmet Büyükleyla; Şakire Karadaş; Rima Çelik; Eyyüp Rencüzoğulları

doi:10.2478/aiht-2021-72-3492

Figures & Tables

Apoptotic effects of A. m. caucasica propolis extracts from the Ardahan province of Turkey on MCF-7 cancer cells A (visualised with TUNEL, 20x magnification); B Apoptotic cell count (mean±standard error) (minimum 10, maximum 35 regions were photographed and scanned for their cell number). Columns marked with different letters denote significant difference (P<0.05). MMC – mitomycin C

Apoptotic effects of A. m. caucasica propolis extracts from the Erzurum province of Turkey on MCF-7 cancer cells A (visualised with TUNEL, 20x magnification); B Apoptotic cell count (mean±standard error) (Minimum 10, maximum 35 regions were photographed and scanned for their cell number). Columns marked with different letters denote significant difference (P<0.05). MMC – mitomycin C

Alkaloid, organic acid, and flavonoid content in ethanolic extracts of A_ m_ caucasica propolis obtained from the Ardahan and Erzurum provinces of Turkey

Peak	Retention Time (min)	Quantity in the sample (%)	Name ARDAHAN	Retention Time (min.)	Quantity in the sample (%)	Name ERZURUM
1	7.41	0.70	Benzyl alcohol	8.43	1.59	2-Phenylethanol (Benzeneethanol)
2	8.13	1.18	Guaiacol	9.28	1.35	1,2-dihydroxybenzene (pyrocatechol)
3	9.02	3.85	Benzoic acid	9.52	0.62	2,3-dihydrobenzofuran (coumaran)
4	9.53	7.64	2, 3-dihydrobenzofuran (coumaran)	15.61	0.73	5-phenylpenta-2,4-dienoic acid (cinnamylidene acetic acid)
5	10.71	19.15	4-hydroxy-3-methoxystyrene (p-vinylguaiacol)	18.35	2.71	3-hydroxy-4-methoxycinnamic acid (isoferulic acid)
6	11.64	0.61	Iso-vanillin or vanillin	18.89	0.74	Palmitic acid
7	15.91	0.60	β-caryophyllene	20.41	1.02	2-nonadecanone
8	16.77	2.25	Benzylbenzoate	20.73	1.03	Elaidic acid
9	17.39	1.11	[1S,3S,(+)]-l-methyl-3-isopropenyl-4- cyclohexene	21.95	1.48	Methyl 4-hydroxycinnamate (p-coumaric acid methyl ester)
10	20.54	13.22	Benzyl cinnamate	22.08	0.82	4-hydroxy-3- methoxycinnamic acid (ferulic acid)
11	22.19	1.70	Tricosane or eicosane	22.19	2.14	Tricosane or eicosane or n-hexadecane
12	23.34	0.59	Corydaldme	23.11	2.89	5-methylisophthalic acid
13	23.57	0.79	6-methoxy-1,3-benzodioxole-5-carbaldehyde (6-metlioxy piperonal)	23.62	1.73	1,2-dimethylcyclopropene
14	23.78	1.42	(E)-l-(2,6-dihydroxy-4-methoxyphenyl)-3- phenylprop-2-en-l-on (pinostrobin chalcone)	23.82	9.64	(E)-l-(2,6-dihydroxy-4-methoxyphenyl)-3-phenylprop-2-en-1-one (pinostrobin chalcone)
15	24.26	3.06	Pentacosane or eicosane	24.27	2.14	Pentacosane
16	24.43	5.29	Benzyl 4-acetylbenzoate	24.79	20.74	Pinocembrin
17	24.75	9.42	Pinocembrin	26.45	5.31	5-hydroxy-7-methoxyflavone (tectochrysin)
18	25.83	9.52	2,5-bis dimethylanino-3,9-dimethyl-3H-1,3,4,6-tetrasacyclopentazulene	27.02	3.38	Eicosane
19	26.40	0.72	5-hydroxy-7-methoxyflavone (tectochrysin)	27.34	10.02	Naringenin or chrysophanic acid
20	27.01	4.94	Eicosane or heptacosane	27.85	11.98	Chrysin
21	27.27	1.23	Naringenin or chrysophanic acid	28.44	0.93	4',5-dihydroxy-7-methoxyflavone (an apigenin derivative)
22	27.74	2.68	Chrysin	28.76	6.92	Galangin
23	28.67	0.77	Galangin	29.20	0.94	Sakuranetin
24	29.18	1.11	Sakuranetin
25	31.03	0.94	Nonacosane
26	33.64	0.83	7,3',4'-trmethoxyflavone

Total flavonoid and phenolic content and antioxidant capacity of A_ m_ caucasica propolis samples obtained from the Ardahan and Erzurum provinces of Turkey

	Ardahan	Erzurum
Total flavonoid content (μg quercetin equivalent of total flavonoids/g)	591.5±26.2^a	271.7±2.9^b
Total phenolic content (mg gallic acid equivalent/g)	235.5±5.3^a	131.3±3.1^b
DPPH (% of control)	94.9±0.3^a	94.6±0.7^a
FRAP (μM FeSO₄ equivalent/g)	4017.7±16.4^a	3813.2±3.6^b

Comparison of mineral composition of A_ m_ caucasica propolis samples collected from the Ardahan and Erzurum provinces of Turkey

Element	Ardahan (mg/kg)	Erzurum (mg/kg)
Co	0.14±0.04^a	0.25±0.06^b
Se	0.038±0.016	0.025±0.006
Li	0.20±0.04	0.22±0.04
Cd	0.005±0.006	0.004±0.004
As	0.13±0.02^a	0.22±0.049^b
Cr	0.98±0.22^a	1.39±0.18^b
Ni	1.08±0.23	1.53±0.34
Pb	0.83±0.19	0.97±0.19
Cu	2.45±0.16	2.01±0.79
Ca	269.42±51.83^a	428.97±76.28^b
Mg	376.17±85.91	560.21±171.45
K	1156.06±278.58	2607.36±1468.87
Mn	5.297±0.71	7.47±3.27
Na	193.19±15.34	203.47±9.58
Zn	30.05±7.30	41.77±19.65
Fe	428.51±77.75	507.62±287.13
Al	408.46±88.17	406.86±202.20
	% of total mass	% of total mass
N	0.42±0.09	0.35±0.02
C	66.84±1.38	64.06±6.38
S	ND	ND

Comparison of vitamin C and carbohydrate content in A_ m_ caucasica propolis samples collected from the Ardahan and Erzurum provinces of Turkey

	Ardahan (μg/g dry weight)	Erzurum (μg/g dry weight)
Vitamin C	40.31±2.97^a	16.18±1.48^b
Fructose	1.58±0.30^a	0.86±0.18^b
Glucose	0.98±0.20^a	0.39±0.05^b
Sucrose	0.15±0.04^a	0.69±0.19^b

Comparison of fatty acid content in A_ m_ caucasica propolis samples collected from the Ardahan and Erzurum provinces of Turkey

Fatty Acid	Retention time (min)	Ardahan (%)	Erzurum (%)
Saturated
Caproic acid	6.54	–	8.85
Caprylic acid	9.24	0.26	–
Decanoic acid (capric acid)	13.85	1.14–1.47	0.08
Undecanoic acid	17.80	0.67	–
Dodecanoic acid (lauric acid)	21.53	24.39–36.95	49.62–54.27
Tridecanoic acid	25.38	5.00–6.59	6.29–8.10
Tetradecanoic acid (myristic acid)	30.81	4.68–5.86	8.66
Pentadecanoic acid	34.13	6.97–8.85	–
Hexadecanoic acid (palmitic acid)	36.89	0.84–0.89	1.53
Heptadecanoic acid (margaric acid)	41.10	1.03–1.64	0.54–1.12
Octadecanoic acid (stearic acid)	44.19	1.86	1.48–2.12
Eicosanoic acid (arachidic acid)	49.47	–	3.13–4.43
Heneicosanoic acid	54.98	1.21	1.57–2.05
Docosanoic acid (behenic acid)	56.66	0.54	0.78–1.35
Tricosanoic acid	59.78	0.31–2.44	0.26
Lignoceric acid	62.16	0.45–0.57	0.22–0.45
TOTAL		49.4–69.8	83.0–93.3
Monounsaturated
9-tetradecenoic acid (myristoleic acid)	32.80	–	0.49
cis-10-pentadecenoic acid	36.57	3.36–4.70	0.88–1.69
cis-9-hexadecenoic acid (palmitoleic acid)	39.52	1.48–2.61	0.32–2.83
cis-10-heptadecenoic acid	42.58	3.18–3.35	–
trans-9-octadecenoic acid (elaidic acid)	45.97	–	0.59–1.73
cis-9-octadecenoic acid (oleic acid)	46.98	1.75–1.92	0.56–1.15
cis-11-eicosenoic acid (gondoic acid)	51.98	1.14	1.61–2.28
cis-13-docosenoic acid (erucic acid)	57.64	0.66	–
cis-15-tetracosenoic acid (nervonic acid)	65.02	0.54–0.79	0.16–0.26
TOTAL		12.1–15.2	4.6–10.4
Polyunsaturated
9,12-octadecadienoic acid (linolelaidic acid)	47.80	–	1.04–1.09
Linoleic acid	48.20	1.42–1.89	7.89–11.46
Gamma-linolenic acid	50.96	0.61–1.26	1.10–1.39
Linolenic acid	53.33	0.65–0.79	0.14–0.28
cis-11,14-eicosadienoic acid	55.09	1.44	0.26
cis-8,11,14-eicosatrienoic acid	57.22	16.30–22.14	0.16
cis-11,14,17-eicosatrienoic acid	58.10	2.00–2.14	1.04
all-cis-5,8,11,14-eicosatetraenoic acid (arachidonic acid)	59.28	0.94–2.69	0.66–0.92
cis-13, 16-docosadienoic acid	60.93	0.65–0.72	–
cis-5,8,11,14,17-eicosapentaenoic acid (timnodonic acid)	64.00	0.79–2.16	0.07–0.40
cis-4,7,10,13,16,19-docosahexaenoic acid (cervonic acid)	66.92	0.60–0.75	0.22–0.45
TOTAL		25.4–36.0	12.6–17.5

Minimal inhibition concentrations of the ethanolic extracts of A_ m_ caucasica propolis samples from the Ardahan and Erzurum provinces of Turkey

Microorganism	Ardahan (μg/mL)	Erzurum (μg/mL)
Klebsiella pneumoniae	30.71	43.37
Staphylococcus aureus ATCC 6538	30.71	43.37
Bacillus megaterium DSM 32	30.71	43.37

Protective effects of the Ardahan and Erzurum propolis against oxidation in MCF-7 cells exposed to mitomycin C

	TBARS (nmol/mL)
Control	0.40±0.02^a
Solvent control	0.41±0.02^a
MMC (0.74 μmol/L)	0.40±0.05^a
Propolis + MMC	Ardahan	Erzurum
32.5 μg/mL	0.03±0.02^b	0.03±0.02^b
65 μg/mL	0.10±0.02^bcd	0.05±0.01^b
125 μg/mL	0.06±0.02^bc	0.07±0.02^bcd
250 μg/mL	0.09±0.01^bcd	0.10±0.03^bcd
500 μg/mL	0.15±0.04^cd	0.16±0.04^d

Effects of different concentrations of propolis extracts obtained from Ardahan and Erzurum on the viability of human lymphocytes

	Cell viability (% of control)
	Ardahan		Erzurum
	24 h	48 h	24 h	48 h
Control	100.0±0.0^a	100.0±0.0	100.0±0.0	100.0±0.0^ab
Solvent control	97.3±1.3^bd	102.2±8.5	96.5±13.3	89.8±14.9^a
MMC (0.74 μmol/L)	97.3±2.6^be	97.7±1.2	92.4±13.4	89.1±14.0^a
Propolis extract
62.5 μg/mL	98.0±2.8^ade	102.8±11.4	99.7±13.5	93.9±13.9^a
125 μg/mL	102.9±5.7^acde	105.2±7.9	104.0±19.6	100.7±19.5^ab
250 μg/mL	107.0±1.8^c	102.9±2.1	118.1±17.8	113.3±20.3^abc
500 μg/mL	116.5±6.6^f	108.8±3.9	139.9±22.5	127.0±20.0^c
Propolis + MMC
62.5 μg/mL+MMC	99.5±3.2^ab	101.1±7.7	98.9±19.2	94.7±16.7^ab
125 μg/mL+MMC	99.6±1.9^ab	99.3±7.6	116.4±41.1	109.1±10.3^abc
250 μg/mL+MMC	100.5±6.1^abc	101.6±6.0	117.2±16.2	119.6±11.7^bc
500 μg/mL+MMC	112.5±2.8^f	113.0±5.5	138.9±23.8	133.5±19.6^c

Comparison of phenolic acid content in A_ m_ caucasica propolis samples collected from the Ardahan and Erzurum provinces of Turkey

Phenolic acids	Ardahan (mg/kg)	Erzurum (mg/kg)
3,4,5-trihydroxybenzoic acid (gallic acid)	ND	ND
4-hydroxy-3-methoxybenzoic acid (vanillic acid)	ND	ND
3,4-dihydroxycinnamic acid (caffeic acid)	0.033	0.046
4-hydroxycinnamic acid (p-coumaric acid)	0.042	0.008
4-hydroxy-3,5-dimethoxycinnamic acid (sinapic acid)	ND	ND
4-hydroxy-3-methoxycinnamic acid (trans-ferulic acid)	0.079	0.005
Quercetin	0.018	0.054
Benzoic acid	ND	ND
2,4-hexadienoic acid (sorbic acid)	ND	ND
Naringenin	ND	ND
Myricetin	ND	ND

Antimicrobial activities of the ethanolic extracts of A_ m_ caucasica propolis samples from the Ardahan and Erzurum provinces of Turkey

	Ardahan	(in millimetres)		Erzurum	(in millimetres)
Microorganism	50 μg	100 μg	150 μg	50 μg	100 Mg	150 μg	Gen	Amp	Ery	Pen
Klebsiella pneumoniae	8.07±1.22	9.00±1.29	9.38±1.28	7.94±0.36	8.52±0.47	9.56±0.97	24.25±1.20	9.22±0.67	31.64±1.56	9.62±0.36
Staphylococcus 6538 aureus ATCC	8.10±0.23	10.84±2.36	12.46±3.42	-	8.90±1.41	9.80±1.11	23.83±0.15	10.68±1.03	30.99±0.70	10.54±1.22
Bacillus megaterium DSM 32	7.52±0.49	9.44±0.59	11.96±1.22	-	7.72±0.80	9.16±1.20	24.73±1.41	10.03±0.78	31.07±1.19	10.35±0.50
Pseudomonas 9027 aeruginosa ATCC	-	-	-	-	-	-	28.02±0.11	13.92±0.68	26.83±0.79	13.92±0.94
Candida albicans	-	-	-	-	-	-	-	-	-	-
Yarrowia lipolytica	-	-	-	-	-	-	-	-	-	-

Chemical and biological characteristics of propolis from Apis mellifera caucasica from the Ardahan and Erzurum provinces of Turkey: a comparative study

Figures & Tables

Figure 1

Figure 2

Alkaloid, organic acid, and flavonoid content in ethanolic extracts of A_ m_ caucasica propolis obtained from the Ardahan and Erzurum provinces of Turkey

Total flavonoid and phenolic content and antioxidant capacity of A_ m_ caucasica propolis samples obtained from the Ardahan and Erzurum provinces of Turkey

Comparison of mineral composition of A_ m_ caucasica propolis samples collected from the Ardahan and Erzurum provinces of Turkey

Comparison of vitamin C and carbohydrate content in A_ m_ caucasica propolis samples collected from the Ardahan and Erzurum provinces of Turkey

Comparison of fatty acid content in A_ m_ caucasica propolis samples collected from the Ardahan and Erzurum provinces of Turkey

Minimal inhibition concentrations of the ethanolic extracts of A_ m_ caucasica propolis samples from the Ardahan and Erzurum provinces of Turkey

Protective effects of the Ardahan and Erzurum propolis against oxidation in MCF-7 cells exposed to mitomycin C

Effects of different concentrations of propolis extracts obtained from Ardahan and Erzurum on the viability of human lymphocytes

Comparison of phenolic acid content in A_ m_ caucasica propolis samples collected from the Ardahan and Erzurum provinces of Turkey

Antimicrobial activities of the ethanolic extracts of A_ m_ caucasica propolis samples from the Ardahan and Erzurum provinces of Turkey

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