O R I G I N A L A R T I C L E
https://doi.org/10.1007/s10341-017-0359-1
Antimicrobial, Antioxidant, and Antimutagenic Activities of Five
Turkish Pear Cultivars
Nurcan Erbil1· Zehra Tugba Murathan2· Mehmet Arslan1· Ahmet Ilcim3· Bilge Sayin2
Received: 16 January 2017 / Accepted: 30 October 2017 / Published online: 29 November 2017 © Springer-Verlag GmbH Deutschland, ein Teil von Springer Nature 2017
Abstract The pear (Pyrus spp.) is one of the most im-portant fruits consumed in daily life. The aim of this study was to determine the total phenolic and ascorbic acid contents, as well as the antimicrobial, antioxidant, and antimutagenic activities, of various pear cultivars. The fruits of five pear (Pyrus communis L.) cultivars (‘Deveci’, ‘Kizil’, ‘Egirsah’, ‘Gugum’, and ‘Banda’) were used in this study. It was determined that the peel and pulp of the ‘Kizil’ pear had the highest total phenolic content (402.5 mg/100 g and 215.2 mg/100 g, respectively), while those of the ‘Banda’ pear had the lowest total phenolic content (326 mg/100 g and 126.1 mg/100 g, respectively). Additionally, the ‘Kizil’ pear showed the highest antioxi-dant capacity in the 2,2’-azino-bis(3-ethylbenzothiazoline-6-6-sulphonic acid) (ABTS) and ferric-reducing ability as-say (FRAP) (1.72μmol TE/g FW and 161.25 μmol Fe II/g FW, respectively) and the highest ascorbic acid content (16.02 mg/100 g). The ‘Banda’ pear showed the highest antibacterial activity against the test bacteria. However, none of the pear extracts displayed antifungal activity. While all doses of the ‘Kizil’, ‘Gugum’, and ‘Banda’ pear extracts used in this study, except 80μL/plate, exhibited antimutagenic activities, only the lowest dose (10μL/plate) of the ‘Deveci’ pear extract showed the antimutagenic activity against induced mutagenesis in the Salmonella
Nurcan Erbil
1 Health Sciences College, Department of Nursery, Ardahan University, 75000 Ardahan, Turkey
2 Faculty of Engineering, Department of Food Engineering, Ardahan University, 75000 Ardahan, Turkey
3 Faculty of Arts and Sciences, Department of Biology, Mustafa Kemal University, 31060 Hatay, Turkey
typhimurium TA 98 strain. Consequently, the five Turkish pear cultivars used in this study exhibited different levels of antimicrobial, antioxidant, and antimutagenic activities. Keywords Pear · Antimicrobial · Antioxidant ·
Antimutagenic · Total phenolic content
Antimikrobielle, antioxidative und antimutagene Eigenschaften von fünf türkischen Birnensorten Schlüsselwörter Birne · Antimikrobiell · Antioxidativ · Antimutagen · Gesamt-Phenolgehalt
Introduction
The pear (Pyrus spp.) is one of the most important fruits consumed in daily life. Pears are produced in many coun-tries worldwide. The pear production is the highest in China, followed by Italy, USA, Argentina and Spain. In 2013, the pear production was 461,826.00 thousand tons in Turkey (Faostat 2016). Pears contain dense nutrients and are low in calories, high in fiber, and rich in minerals and vitamins. The content of free sugars and organic acids in the fruit plays an important role in the nutritional value and quality of pears, contributing to the taste and regulation of chemical reactions in the body (Chen et al.2007). This fruit contains 2% of fiber, 14% of carbohydrates, 85% of water, 0.3% of protein, and 0.1% of fat. Additionally, the vitamin content of the pear includes about 3 mg/100 g Fresh Weight of ascorbic acid and trace amounts of other vitamins (Standard Tables of Food Composition2003).
When fruits and vegetables are regularly consumed in daily life, the risk of chronic diseases is dramatically
re-duced. The antioxidant constituents of fruits and vegetables consumed in daily life play an important role in the mainte-nance of health and prevention of diseases (Pérez-Jiménez and Saura-Calixto2015). The consumption of polyphenols provides significant health benefits because polyphenols possess antioxidant, inflammatory, viral, and anti-carcinogenic properties (Borges et al.2010; Catel-Ferreira et al.2015; Zhang and Tsao2016).
Antibiotic resistance of bacteria has recently become an increasing problem worldwide. In an effort to combat this problem, researchers have investigated antimicrobial prop-erties of plants. In this study, we aimed to determine the total phenolic and ascorbic acid contents, as well as antimi-crobial, antioxidant, and antimutagenic activities, of various Turkish pear cultivars.
Materials and Methods
Fruit Materials
Fruits of five pear (Pyrus communis L.) cultivars (‘Deveci’, ‘Kizil’, ‘Egirsah’, ‘Gugum’, and ‘Banda’) were used in this study. These fruits were collected in Posof/Ardahan, Turkey (Table1). While some fresh fruits were stored at +4 ºC for the analyses of antimicrobial and antimutagenic activities, some were stored at –80 ºC for the analyses of the total phenolic content (TPC) and antioxidant activities.
Preparation of Extracts
The aqueous extracts of the five pear cultivars were used in this study for antimicrobial and antimutagenic activity tests. Fruit samples (40 g) were homogenized in 200 mL of distilled water using an Ultra-Turrax disperser (WiseTis®
homogenizer, HG 15 A) and then the mixtures were shaken on a rotary shaker for 72 h at 190 rpm. The extract was centrifuged at 5000 rpm for 10 min, and the supernatant was collected. Then, the extract was concentrated using a rotary evaporator (SciLogex RE100-Pro). Filter-sterilized
Table 1 Localities and harvested dates of pear fruits (Pyrus communis L.)
Cultivars Coordinate Altitude (m) Harvested date Locality
‘Deveci’ N41º3506.600E42º49028.800 1236 17.09.2015 Around the Armutveren village, Posof/Ardahan/ Turkey
‘Kizil’ N41º34054.100E42º49026.400 1219 17.09.2015 Around the Armutveren village, Posof/Ardahan/ Turkey
‘Egirsah’ N41º34054.300E42º49020.100 1227 17.09.2015 Around the Armutveren village, Posof/Ardahan/ Turkey
‘Gugum’ N41º34053.100E42º4901000 1255 17.09.2015 Around the Armutveren village, Posof/Ardahan/ Turkey
‘Banda’ N41º33042.500E42º47052.600 1258 17.09.2015 Around the Posof city centre/Ardahan/Turkey and concentrated extracts were frozenstored at –20 °C until use.
Total Phenolic (TPC) and Ascorbic Acid Contents
TPC of the peel and pulp of pear fruits was determined us-ing the Folin-Ciocalteu method and gallic acid as a standard (Spanos and Wrolstad1992). The ascorbic acid content was determined by a spectrophotometric method ( ¸Sahin2013). Results were expressed as milligrams of ascorbic acid per 100 g of a fresh fruit sample.
Antioxidant Activity
Extraction Method for Antioxidant Activity
Pear samples (5 g) were homogenized by mixing with 50 mL of an 85% methanol solution and incubated for 24 h, 150 rpm at 30 °C. Then, the sample was centrifuged at 5000 rpm for 10 min, and the supernatant was collected.
ABTS Free Radical-Scavenging Activity
2,2’-Azino-bis(3-ethylbenzothiazoline-6-6-sulphonic acid) (ABTS) radical-scavenging activity was determined using the method of Re et al. (1999). Absorbance was measured at 734 nm using a spectrophotometer (Unico S1205), and Trolox solutions were used for calibration. The ABTS free radical-scavenging capacity of pear samples was compared with that of the Trolox standard. The antioxidant capacity was expressed as µmol Trolox equivalent (TE) per gram of fresh weight (FW) of the sample.
Ferric Reducing Ability Assay
The ferric ion reducing ability (FRAP) was measured by the method of Benzie and Strain (1996). Absorbance was mea-sured at 593 nm using a spectrophotometer (Unico S1205), and FeSO4 solutions were used for calibration. FRAP of pear fruits was calculated based on a linear calibration curve
and expressed as µmol FeSO4equivalents per gram of sam-ple.
Antimicrobial Activity
The antimicrobial activities of aqueous pear extracts were determined using an agar well diffusion method. Agar wells were prepared using a sterilized cork borer of 11 mm in di-ameter, and 150μL of each extract was added to the wells. Each microorganism (1%) from a 106–107 colony-forming units/mL suspension was added to 15 mL of sterile me-dia (Mueller-Hinton agar for bacteria, and Sabouraud 2% glucose agar for yeasts) to inoculate assay media (Collins et al.1989; Bradshaw1992). Ampicillin was used as a posi-tive control. Inhibition zones were measured using a digital caliper, and all tests were performed in triplicate.
Antimutagenic Activity
Bacterial Culture
Salmonella typhimurium strains TA 98 and TA 100 were used to test the antimutagenic activities of the five pear cul-tivars. The strains were routinely checked to confirm their genetic properties according to Maron and Ames (1983).
Antimutagenicity Test
The Ames test (Maron and Ames1983) was used to as-say the antimutagenic activities of the five pear cultivars. Four different concentrations of aqueous pear extracts (10, 20, 40, and 80μL/plate) were used in the tests with-out the metabolic activation system S9 mix using the S. typhimurium TA 98 and TA 100 strains. 4-Nitro-O-phenylenediamine (4-NPD; Product Number: 108898-5G, Sigma Aldrich, St. Louis, MO, USA) was used as a positive control for TA 98 (10μg/plate). Sodium azide (SA; Cat. No. S 2002, Sigma Aldrich) was used as a positive control for TA 100 (100μg/plate). The bacterial culture (100 μL/ plate), extract, and mutagen (4-NPD or SA) were added to 2 mL of top agar. The content of each tube was gently mixed and poured onto minimal glucose agar. The plates Table 2 Total phenolic and
ascorbic acid contents of pear cultivars
Pear cultivars Total phenolic content of peel (mg/100 g)
Total phenolic content of pulp (mg/100 g)
Ascorbic acid content (mg/100 g) Mean ± Sd ‘Gugum’ 352.3 ± 12.9c 154 ± 12.6bc 14.75 ± 3.3b ‘Banda’ 326 ± 25.2d 126.1 ± 17.4c 15.91 ± 2.1a ‘Kizil’ 402.5 ± 76.5a 215.2 ± 20.3a 16.02±1a ‘Deveci’ 396.7 ± 10.3b 175.5 ± 12.8b 10.2 ± 1.4c ‘Egirsah’ 400 ± 11.8a 200 ± 10.1a 9.03 ± 1.5d
Superscript letters indicate significant differences (p < 0.05)
Sd Standard deviation
were incubated at 37 ºC for 48–72 h. The analyses were performed in triplicate.
Statistical Analyses
The SPSS (version 16) statistical analysis package was used to analyze the results of this study. Results ob-tained from triplicate measurements are presented as the mean±standard deviation. Data were subjected to analysis of variance (ANOVA) and significant differences between the groups were determined by a multiple comparison pro-cedure according to Duncan (1955). Differences at p < 0.05 were considered significant. Antimutagenic data showed a normal distribution (Shapiro-Wilk) and were analyzed by one-way ANOVA, followed by Dunnett’s test using the SPSS software, with pÄ 0.05 significant.
Results
The TPCs and ascorbic acid contents of the pear cultivars are shown in Table2. It was observed that the peel and pulp of the ‘Kizil’ pear had the highest TPC (402.5 mg/100 g and 215.2 mg/100 g, respectively), followed by the ‘Egirsah’ pear (400 mg/100 g and 200 mg/100 g, respectively) and ‘Deveci’ pear (396.7 mg/100 g and 175.5 mg/100 g, respec-tively). The lowest TPC was observed in the peel and pulp of the ‘Banda’ pear (326 mg/100 g and 126.1 mg/100 g, respectively). TPC of the peels was approximately two times higher than that of the pulps in the pear fruits. The highest ascorbic acid content was also determined in the ‘Kizil’ pear (161.02 mg/100 g) in this study, while the low-est value was observed in the ‘Egirsah’ pear (9.03 mg/100 g).
The antioxidant activities of the pear cultivars were mea-sured as ABTS free radical-scavenging activities and FRAP values, and the results are presented in Table3. The highest ABTS and FRAP values were determined for the ‘Kizil’ pear (1.72 µmol TE/g FW and 161.25 µmol Fe (II)/g FW, respectively), while the lowest values were measured in the ‘Banda’ pear (0.81 µmol TE/g FW and 120 µmol Fe (II)/g FW, respectively).
Table 3 Antioxidant activities of pear cultivars Pear cultivars ABTS
(µmol TE/g FW) FRAP (µmol Fe II/g FW) Mean ± Sd ‘Egirsah’ 1.44 ± 0.03b 132.50 ± 10.9c ‘Gugum’ 0.89 ± 0.01d 148.75 ± 10.2b ‘Deveci’ 1.26 ± 0.0c 126.25 ± 9.9d ‘Kizil’ 1.72 ± 0.09a 161.25 ± 3.8a ‘Banda’ 0.81 ± 0.02d 120.00 ± 11.8d
Superscript letters indicate significant differences (p < 0.05)
Sd Standard deviation
The antimicrobial activity values of the pear cultivars used in this study and that of the standard antibiotic used as a positive control are presented in Table 4. Based on these results, the aqueous extracts of the pear cultivars ex-hibited different antibacterial activities against the test bac-teria, but none of the extracts displayed antifungal activ-ity against the test microorganisms used in this study. The strongest antibacterial activity was shown by the ‘Banda’ pear extract against Pseudomonas aeroginosa ATCC 9027, with the inhibition zone diameter of 20.140 mm. The low-est sensitivity was shown by Escherichia coli against the extract of the ‘Gugum’ pear, with the inhibition zone diam-eter of 12.343 mm. Additionally, it was observed that none of the extracts obtained from the pear cultivars displayed antibacterial activity against Bacillus licheniformis.
The antimutagenic activity tests were performed using the S. typhimurium TA 98 and TA 100 strains. It was de-termined that all the doses of the ‘Kizil’, ‘Gugum’, and ‘Banda’ pear extracts, except 80μL/plate, displayed the
an-Table 4 Antimicrobial activities of pear cultivars (mm) and ampicillin used as positive control
Microorganism ‘Gugum’ ‘Banda’ ‘Kizil’ ‘Deveci’ ‘Egirsah’ Ampicillin
Mean±Sd Pseudomonas aeroginosa ATCC 9027 14.483 ± 0.242 20.140 ± 0.368 19.263 ± 0.395 – 16.516 ± 0.304 14.00 ± 1.155 Bacillus subtilis 14.41 ± 0.308 18.390 ± 0.361 15.246 ± 0.072 – 16.466 ± 0.023 11.33 ± 0.333 Enterobacter aerogenes 14.546 ± 0.351 18.420 ± 0.160 15.160 ± 0.185 13.433 ± 0.067 16.203 ± 0.396 11.00 ± 0.0 Bacillus licheniformis –* – – – – 16.00 ± 1.528 Klebsiella pneumoniae 13.313 ± 0.309 17.243 ± 0.173 16.456 ± 0.146 15.240 ± 0.104 16.386 ± 0.219 10.33 ± 0.333 Staphylococcus aureus ATCC 6538 15.580 ± 0.124 16.350 ± 0.161 16.470 ± 0.311 16.273 ± 0.246 16.156 ± 0.233 10.00 ± 0.0 Bacillus megaterium DSM 32 15.193 ± 0.141 18.440 ± 0.085 15.286 ± 0.318 14.193 ± 0.148 17.270 ± 0.228 10.67 ± 0.333 Escherichia coli 12.343 ± 0.252 18.073 ± 0.167 15.286 ± 0.033 – 15.313 ± 0.215 10.33 ± 0.333 Yarrovia lipolytica – – – – – – Candida albicans – – – – – – Saccharomyces cerevisiae – – – – – –
Sd Standard deviation, *Result was not observed
timutagenic effects against induced mutagenesis in S. ty-phimurium TA 98. Only the lowest dose (10μL/plate) of the ‘Deveci’ pear extract exhibited the antimutagenic activ-ity. However, the ‘Egirsah’ pear extract did not show the antimutagenic effects at any concentration (Table5). Based on the results of the antimutagenic activity tests, no dose of any pear extract displayed antimutagenic effects against induced mutagenesis in S. typhimurium TA 100 (Table6).
Discussion
The TPC values of the pear peels and pulps ranged from 326 to 402.5 mg/100 g and from 126.1 to 215.2 mg/100 g, re-spectively, in our study. TPCs of the ‘Gugum’ and ‘Banda’ pears harvested in 2014 were previously studied by Abacı et al. (2016), and the authors determined that the TPC val-ues of the peel and pulp were 432 and 203.2 mg/100 g for the ‘Banda’ and 455 and 201 mg/100 g for the ‘Gugum’, respectively. These TPC values were higher than those of obtained in our study because the values may vary depend-ing on the harvest date. It was reported in a previous study (Li et al.2014) that TPC ranged from 263.6 to 1121.5 mg of gallic acid/100 g of dry weight—DW. The highest TPC was determined in the ’Jinqui’ pear, and the lowest TPC was observed in the ’Youran’ pear among 10 pear culti-vars. Additionally, the TPC values in the peels were found to be remarkably (approximately 6–20 times) higher than those in the flesh. The ’Radana’ pear cultivar had TPC of 894.9 mg/kg of FW (Kolniak-Ostek 2016a). Wang et al. (2015) reported that TPCs ranged in pear peels from 112.58
Table 5 Antimutagenicity of pear cultivars in Salmonella
typhimurium TA 98 strain
Pear extracts Concentration Revertant colonies Mean ± Sd ‘Banda’ Control 14.00 ± 1.15 Positive control (4-NPD) 2382 ± 328 10 µl/plate 877 ± 118b3 20 µl/plate 877 ± 180b3 40 µl/plate 480 ± 119b3 80 µl/plate 1790 ± 57.2 ‘Kizil’ Control 12.00 ± 0.577 Positive control (4-NPD) 2353 ± 274 10 µl/plate 967.3 ± 69.3b1 20 µl/plate 764.3 ± 58.0b1 40 µl/plate 946 ± 523b1 80 µl/plate 1865 ± 400 ‘Gugum’ Control 11.67 ± 1.45 Positive control (4-NPD) 2291 ± 341 10 µl/plate 599.0 ± 59.9b1 20 µl/plate 572.0 ± 14.2b1 40 µl/plate 1126 ± 128b1 80 µl/plate 1046.7 ± 43.0 ‘Egirsah’ Control 17.33 ± 8.33 Positive control (4-NPD) 1876 ± 191 10 µl/plate 854.0 ± 83.6 20 µl/plate 1015 ± 443 40 µl/plate 1420 ± 423 80 µl/plate 1791.7 ± 92.5 ‘Deveci’ Control 13.67 ± 1.20 Positive control (4-NPD) 2332 ± 377 10 µl/plate 61.0 ± 11.0b3 20 µl/plate 2194.7 ± 45.2 40 µl/plate 2649 ± 333 80 µl/plate 2585.3 ± 37.5
4-NPD 4-nitro-o-phenylenediamine; Sd Standard deviation
a: significant difference between control; b: significant difference between positive control; a1,b1: pÄ 0.05; a2,b2: pÄ 0.01; a3,b3: pÄ 0.001
to 837.73 mg of gallic acid/100 g of DW and that the pear peel had a much higher TPC than the pear pulp. Abacı et al. (2016) previously studied the ascorbic acid content of the ‘Gugum’ and ‘Banda’ pears harvested in 2014, and the authors determined that those were 10.2 and 8.8 mg/100 g, respectively. These values were lower than ours because seasonal differences may affect the contents of fruits. It was reported that the ascorbic acid contents were between 2.6 and 5.3 mg/100 g in six pear cultivars (Sanchez-Moreno
Table 6 Antimutagenicity of pear cultivars in Salmonella
typhimurium TA 100 strain
Pear extracts Concentration Revertant colonies Mean ± Sd ‘Banda’ Control 116.3 ± 21.4 Positive control (SA) 2579 ± 850 10 µl/plate 1788.7 ± 55.4 20 µl/plate 2861 ± 235 40 µl/plate 2063 ± 278 80 µl/plate 2773 ± 163 ‘Kizil’ Control 128.3 ± 14.3 Positive control (SA) 2300.0 ± 41.6 10 µl/plate 1770 ± 133 20 µl/plate 2191 ± 411 40 µl/plate 1756 ± 150 80 µl/plate 2046 ± 328 ‘Gugum’ Control 125.00 ± 9.07 Positive control (SA) 1657 ± 190 10 µl/plate 2839 ± 393 20 µl/plate 3313 ± 248 40 µl/plate 1743.3 ± 87.2 80 µl/plate 2353 ± 782 ‘Egirsah’ Control 119.00 ± 5.51 Positive control (SA) 2803 ± 515 10 µl/plate 2830 ± 408 20 µl/plate 2289 ± 179 40 µl/plate 2113 ± 350 80 µl/plate 2285 ± 430 ‘Deveci’ Control 84.33 ± 4.41 Positive control (SA) 2570 ± 241 10 µl/plate 1885 ± 124 20 µl/plate 1620 ± 167 40 µl/plate 1940 ± 555 80 µl/plate 2907 ± 215
SA Sodium azide, Sd Standard deviation
et al.2003). The ascorbic acid concentration in fruits is dif-ferent depending on growth conditions (Nagy1980).
The antioxidant activities of various pear cultivars were measured in previous studies. Kolniak-Ostek (2016b) re-ported that the 2,2-diphenil-1-1-picrylhydrazyl (DPPH) and FRAP values of the peel (1210.1 and 1981.3μmol TE/100 g of DM, respectively) were higher than those of the pear pulp (426.0 and 847.2μmol TE/100 g of DM, respectively). In another study, the strongest reducing power was found in the ’Zaosu pear’ (P. bretschnrideri Rehd.) peel (545.93 mg
of vitamin C/100 g of DW), followed by the ’Yaguang’ pear (P. ussuriensis Maxim.) peel (545.12 mg of vitamin C/100 g of DW), and the lowest reducing power was found in the ’Shuijing’ pear (P. bretschneideri Rehd.) peel (128.53 mg/100 g). The highest DPPH activities were also measured in the ’Yaguang’ pear (P. ussuriensis Maxim.) and the ’Zaosu’ pear (P. bretschnrideri Rehd.) (89.27% and 85.77%, respectively) (Wang et al.2015). Li et al. (2014) showed that the greatest reducing ability was measured in the peels extract of the ’Jinqiu’ pear among 10 pear culti-vars (813.8μg of vitamin C/100 g of DW). The ’Yaguang’ and ’Meirensu’ pears also exhibited high antioxidant ca-pacities (751.5 and 716.4 μg of vitamin C/100 g of DW, respectively). Additionally, the ’Yaguang’, ’Hongpi’, and ’Qingpi# pears showed the strongest DPPH free radical-scavenginig activities.
Antimicrobial activities of the pear cultivars used in this study have not been previously examined. There are only a few studies on antimicrobial activities of various pear cul-tivars. Güven et al. (2006) studied an ethyl acetate extract of P. communis subsp. communis and tested the extract for an-timicrobial activities. The authors showed that the extract of P. communis subsp. communis exhibited antimicrobial activities against most of the bacteria and all yeasts stud-ied but did not display any antifungal activity against the mycelial fungi tested. It was determined in another study that aqueous extracts of the tissue of young shoots of pear (Pyrus spp.) displayed high antibacterial activities against Erwinia amylovora bv. 4 (Jin and Sato2003).
The antimutagenic activities of the pear cultivars evalu-ated in this study have not been previously examined. There are only a few studies on antimutagenic effects of various pear cultivars in the literature. Antimutagenic activities of 63 kinds of fruits, including persimmon, peach, pear, ap-ple, and grape, were examined using S. typhimurium TA 98 against mutagenicity caused by 3-amino-1-1-methyl-5–5 H-pyrido[4,3-b]indole. All fruit samples showed antimuta-genic effects, but persimmon exhibited astronger effect than those of the other fruits (Shinmoto et al.2002). In another study, 13 fruit species, including pear, and 12 vegetables commonly consumed in Germany were studied and found to be antimutagenic for S. typhimurium TA 98 (Edenharder et al.1995).
Consequently, some properties and activities of the ‘De-veci’, ‘Kizil’, ‘Egirsah’, ‘Gugum’, and ‘Banda’ pear culti-vars were examined in this study. The results showed that TPCs of the peels were higher than those of the pulps. The pear cultivars used in this study possess rich total phe-nolic and ascorbic acid contents. Additionally, these pears have different levels of antioxidant, antimicrobial, and an-timutagenic properties. Because of their important roles in the maintenance of health, pears should be consumed in daily life with their peel. The ABTS and FRAP
antioxi-dant, antimicrobial, and antimutagenic activities of the five pear cultivars were examined in this study for the first time. There are very few studies in the literature on antimicro-bial and antimutagenic activities of various pear cultivars, which makes this study important.
Acknowledgements We wish to thank the Ardahan University (Turkey) Scientific Research Commission for supporting our study through Project Grants No. 2014/11.
Conflict of interest N. Erbil, Z.T. Murathan, M. Arslan, A. Ilcim and B. Sayin declare that they have no competing interests.
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