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

Mehmet Arslan
Mehmet Arslan
, 
Yusuf Sevgiler
Yusuf Sevgiler
, 
Celal Güven
Celal Güven
, 
Zehra Tuğba Murathan
Zehra Tuğba Murathan
, 
Nurcan Erbil
Nurcan Erbil
, 
Deniz Yıldırım
Deniz Yıldırım
, 
Mehmet Büyükleyla
Mehmet Büyükleyla
, 
Şakire Karadaş
Şakire Karadaş
, 
Rima Çelik
Rima Çelik
 e 
Eyyüp Rencüzoğulları
Eyyüp Rencüzoğulları
   | 30 mar 2021
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Article Category: Original article
Pubblicato online: 30 mar 2021
Pagine: 53 - 69
Ricevuto: 01 set 2020
Accettato: 01 mar 2021
DOI: https://doi.org/10.2478/aiht-2021-72-3492
© 2021 Mehmet Arslan, Yusuf Sevgiler, Celal Güven, Zehra Tuğba Murathan, Nurcan Erbil, Deniz Yıldırım, Mehmet Büyükleyla, Şakire Karadaş, Rima Çelik, and Eyyüp Rencüzoğulları, published by Sciendo
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Figure 1

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 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

Figure 2

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
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 ج
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±26.2a 271.7±2.9b
Total phenolic content (mg gallic acid equivalent/g) 235.5±5.3a 131.3±3.1b
DPPH (% of control) 94.9±0.3a 94.6±0.7a
FRAP (μM FeSO4 equivalent/g) 4017.7±16.4a 3813.2±3.6b

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±0.04a 0.25±0.06b
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±0.02a 0.22±0.049b
Cr 0.98±0.22a 1.39±0.18b
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±51.83a 428.97±76.28b
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±2.97a 16.18±1.48b
Fructose 1.58±0.30a 0.86±0.18b
Glucose 0.98±0.20a 0.39±0.05b
Sucrose 0.15±0.04a 0.69±0.19b

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

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

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 - - - - - - - - - -
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Medicine, Basic Medical Science, other
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