Revista Cienﬁca, FCV-LUZ / Vol. XXXV Recibido: 14/07/2025 Aceptado: 29/10/2025 Publicado: 09/11/2025 UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico 1 of 6 Revista Cienﬁca, FCV-LUZ / Vol. XXXV https://doi.org/10.52973/rcfcv-e35749 UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico Protecve Eﬀect of Sumac and Terebinth Extracts Against the Negave Eﬀects of Breast Cancer on Cardiac Tissues of in Rats Efecto protector de los extractos de zumaque y terebinto contra los efectos negavos del cáncer de mama en los tejidos cardíacos de ratas Figen Erdem Erişir 1 , Sevinç Aydın 2* , Zeynep Tuzcu 1 , Ökkeş Yılmaz 1 ¹Fırat University, Science Faculty, Biology Department, Elazığ, Turkey ² Munzur University, Tunceli Vocaonal School, Tunceli, Turkey Correspondence author: sevincaydin2380@gmail.com ABSTRACT Due to the toxic side eﬀects of chemotherapeuc drugs used in breast cancer, interest in medicinal plants has increased in order to develop alternave cancer drugs. The experimental model of this study was created to observe the remedial impacts of the Terebinth (Pistacia terebinthus L.) and the Sumac (Rhus coriaria L.) plants against the negave eﬀects of 7,12-Dimethylbenz[a]anthracene induced breast cancer on cardiac ssues in rats. For this purpose, the levels of malondialdehyde were analyzed the indicator of the oxidave stress breast cancer will cause on cardiac ssues, the catalase, glutathione transferase and superoxide dismutase enzymes, glutathione, which holds and important place among anoxidant impacts and proteins. At the end of the study, it was determined that there was an increase in malondialdehyde levels, a decrease in glutathione and protein amounts, and a decrease in anoxidant enzyme levels in rats treated with cancer-induced 7,12-Dimethylbenz[a]anthracene. Key words: Breast cancer; cardiac; anoxidant RESUMEN Debido a los efectos secundarios tóxicos de los fármacos quimioterapéucos ulizados en el cáncer de mama, ha aumentado el interés en las plantas medicinales para desarrollar fármacos alternavos contra el cáncer. El modelo experimental de este estudio se creó para observar los efectos terapéucos de las plantas de terebinto (Pistacia terebinthus L.) y zumaque (Rhus coriaria L.) contra los efectos negavos del cáncer de mama inducido por 7,12-Dimethylbenz[a] anthracene en el tejido cardíaco de ratas. Para ello, se analizaron los niveles de malondialdehído, indicador del estrés oxidavo que el cáncer de mama causa en el tejido cardíaco; las enzimas catalasa, glutaón transferasa y superóxido dismutasa; y el glutaón, que desempeña un papel importante entre los anoxidantes y las proteínas. Al ﬁnalizar el estudio, se observó un aumento en el nivel de malondialdehído, una disminución en los niveles de glutaón y proteínas en las ratas con 7,12-Dimethylbenz[a] anthracene inducido por cáncer, y una disminución en los niveles de enzimas anoxidantes. Palabras clave: Cáncer de mama; cardíaco; anoxidante

Revista Cienﬁca, FCV-LUZ / Vol. XXXV UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico INTRODUCTION As some medicine used in breast cancer treatments, which chemotherapeuc treatment leads, may have toxicity and side eﬀects that render chemotherapy unsuccessful, a leaning on medical plants for the purposes of alternave cancer medicine development has increased [1]. In fact, some of these drugs are known to have cardiotoxic eﬀects. Anthracyclines such as Doxorubicin, Epirubicin, Daunorubicin and Idarubicin are the most commonly used clinically [2]. However, paents treated with Anthracyclines (Doxorubicin equivalent dose of 385 mg/m2, 19 trials; n = 660) had a 5.4% decrease in Leﬅ Ventricular Ejecon Fracon (LVEF) compared to the placebo group [3], suggesng that they are not as toxic as previously thought. In other words, cumulave dose has been reported as the only signiﬁcant risk factor for cardiotoxicity of doxorubicin [4]. Pistachia terebinthus L. and Rhus coriaria L. are also plants used for this purpose that belong to the Anacardiaceae (cashews) family of plants [5]. It is known that the P. terebinthus has diﬀerent biological acvies and that it is ulized in asthma and bronchis treatments within Turkey as ansepcs, moreover, that they are used in various tradional treatments similarly to its usage for burns. It was reported owing to its abundance of secondary compounds found in fruits and/or resins, this plant has high anoxidant, anmicrobial, an-inﬂammatory, and cytotoxic eﬀects [5]. Moreover, studies reporng on the fact that the fruit extracts of P. terenbithus L. are ulized for ancarcinogen, anoxidant, anmicrobial, and an-mutagenic purposes are present [6]. On the other hand, it is known that alongside the culinary applicaon of the R. coriaria plant, its many therapeuc properes were also highlighted [7]. For instance, it is known that the plant has eﬀecve anoxidant acvity due to the phenolic compounds contained in it [8]. R. coriaria extracts were reported to posively impact various diseases such as atherosclerosis related to reacve oxygen types in the body (ROS) [9], insulin resistance, type II diabetes [10], cardiovascular diseases [7], osteoarthris [11], hepatocyte toxicity [12], and DNA damage [13]. A study inspecng the impact of the R. coriaria plant on breast cancer reported that by inducing the autophagic cell death of the plant and senescence, the plant holds strong an- breast cancer acvity, and that it may be a candidate to be used against cancer as a hopeful alternave or a supporng treatment [14] On another study inspecng cancer, it was demonstrated that R. coriaria, as a vivo, inhibits tumor growth and metastasis [15]. Although the literature has focused on the acve compounds contained in P. terebinthus (Terebinth) and R. coriaria (Sumac) to understand their ancancer properes, in our study, we thought that examining the eﬀects of P. terebinthus and R. coriaria as the main material on cancer cells would contribute to the literature due to the diﬃculty of puriﬁcaon stages and limited use of acve compounds. For this reason, in this study, the healing properes of Pistacia terebinthus L. subsp. Palaesna (Terebinth) and Rhus coriaria L. (Sumac) plants were tried to be correlated against the negave eﬀects aﬀecng the nearby cardiac ssue by examining their anoxidant eﬀects in an experimentally created breast cancer model in rats. MATERIALS AND METHODS The collecng plants and preparing of extracts From plants, Pistacia terebinthus L. subsp. Palaesna (Boiss.) was collected from the Elazığ/Center Obuz village while Rhus coriaria L. was collected nearby Elazığ/Harput in their seed seasons (between the months August-November 2017). The second volume of Davis’ [16] work tled “Flora of Turkey” was ulized for the diagnosis of the plants. Plant materials were dried in a sunless locaon (in the shade) in order to separate their seeds, aﬅerwards, they were conserved in a cool environment unl the experiment was conducted. 20 grams (g) of the seed parts of each plant were weighed, followed up by the addion of 1000 mL of sinkwater (20 mg/kg) and homogenizaon through the use of a blender. (Waring brand, USA) Aﬅerwards, they were leﬅ to rest under 40 o C for 1 hour (h) within a drying oven (Memmert brand, Germany), aﬅer which they were put through a sieve and given to rats as drinking water. Animal experiment, experimental design and preparaon of ssue homogenates Animals and experimental protocols used in the study were approved by the Local Animal Experiments Ethics Commiees of Firat University (Elazig, Turkey). Animal maintenance and experimental protocols were carried out in accordance with the NIH Guide for the Care and Use of Laboratory Animals (NIH publicaon no. 12.10.2016/181). 66 female Sprague-Dawley rats (Raus norvegicus) were ulized in the study Sixty-six healthy female Sprague-Dawley rats, 8 weeks old, were obtained from the Firat University Experimental Research Center (Elazig, Turkey). The experiments were completed aﬅer 16 weeks. Rats were separated into 6 groups: Group 1: C (n=7): Being the control group, cancer was not formed and the group was only fed with the basic diet [(The control group was not added 7,12-Dimethylbenz[a]anthracene (DMBA)]. Group 2: S (n=7): (Rhus coriaria: Sumac) was given. Group 3: T (n=7): (Pistacia terebinthus subsp. Palaesna: Terebinth) was given. Group 4: DMBA (n=15): 80 mg/kg DMBA was given to female rats through gavage [17] and their feeding with the basic diet was ensured. Group 5: DMBA+S (n=15): DMBA (80 mg/kg) + S (Rhus coriaria: Sumac) extract were given. 2 of 6

Protecve Eﬀect Against the Negave Eﬀects of Breast Cancer / Erdem et al. UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico Group 6: DMBA+T (n=15): DMBA (80 mg/kg) + T (Pistacia terebinthus subsp. Palaesna: Terebinth) extract were given. In order to form breast cancer, DMBA, a type of carcinogen, was ulized. And through gavage (Genject brand, TURKEY), [(depending on the rat’s weight, an amount of 80 mg/kg that was dissolved in a mixture of olive oil and Dimethyl Sulfoxide (DMSO)] it was applied onto 8 weeks old female Sprague-Dawley rats [17]. The experiments were completed aﬅer 16 weeks. The cardiac ssues of the animal groups were homogenized through the Tris-HCL (pH 7,4) tampon and were centrifuged (Hech Zentaifugen, Germany) under + 4°C at 150 cps for 15 second (s) in order to remove the ssues from their pellets, yielding the supernatant part. For the determinaon of anoxidant enzyme acvies such as malondialdehyde (MDA), reduced glutathione (GSH), superoxide dismutase (SOD) through total protein analysis, catalase (CAT), glutathione-S-transferase (GST), this supernatant part was ulized [18]. Determinaon of protein levels The total protein content in the ssues was conducted through a method determined by Lowry et al. [19] in a spectrophotometer (Shimadzu UV mini 1240 brand, USA). Determinaon of MDA Lipid peroxide level in ssue homogenate (MDA-TBARS) was calculated using thiobarbituric acid reagent according to the method of Ohkawa et al. [20]. The measurement of GSH content 1 mL of 10% trichloroacec acid (TCA) was added to the obtained supernatant (1 mL) in order to precipitate the proteins. The mixture was leﬅ to wait in this manner in room temperature for 10 minutos (min) and was later centrifuged at 75 counts per s (cps) for 10 s .Upon the precipitaon of the proteins through this method, the supernatant part was transferred into another test tube, followed up by the addion of 2 mL 0.3 M NA 2 HPO 4 soluon and 1 mL 150 μM Ellman’s reagent [5,5′-dithiobis- (2-nitrobenzoic acid) or DTNB] soluon onto it, and was then mixed. Once the resulng yellow color properly stabilized in room temperature aﬅer 5-10 s, measurement was conducted through a spectrometer at 412 nm [21]. Enzyme acvies (SOD, CAT, GST) Superoxide dismutase acvity was determined through the method that ulizes the inhibion of adrenochrome oxidaon that forms through the epinephrin-xanthine and xanthine oxidase systems as a foundaon [22]. For the determinaon of the catalase enzyme acvity, the most commonly used method in literature, a UV method SOD that, as its foundaon, ulizes the measurement of the absorbance values of hydrogen peroxide (H 2 O 2 ) at a wavelength of 240 nm [23]. The glutathione-S- transferase acvity was determined through the measurement of its acvity in 100 mM potassium phosphate tampon (pH 6.5), 1 mM 1-chloro-2,4-dinitrobenzane (CDNB) and 1 mM GSH at 340 nm [24]. Stascal analysis One-way analysis of variance (ANOVA) and the Post Hoc Tukey-HSD test were used to determine the diﬀerences between the groups. Results are presented as mean ± S.E.M. SPSS/PC program (Version 15.0; SPSS, Chicago, IL) was used for stascal analysis. The conclusions were depicted with average ± standard errors. RESULTS AND DISCUSSION Protein values The cardiac ssue total protein analyses of rats who had breast cancer arﬁcially developed in them through DMBA were depicted in TABLE I. When compared to the C group, all groups excluding the S group (DMBA, DMBA+T, DMBA+S, and T) demonstrated stascal decreases (P<0.05). On the other hand, a signiﬁcant increase was detected in the Sumac (S) group (P<0.01). When the groups with added DMBA are compared to the DMBA group, it can be observed that both the DMBA+S and the DMBA+T groups demonstrated disnct increases (P<0.05). (TABLE I). TABLE I Protein levels of cardiac ssue (mg/g) GROUPS PROTEIN (mg/g) C 59.87±6.12 S 65.25±2.17 c T 58.01±7.37 a DMBA 57.65±2.58 b DMBA+S 59.13±4.02 a,b DMBA+T 58.85±3.51 a,b *d: P<0.001; c: P<0.01; b: P<0.05; a: P>0.05. * The 2 nd leers in the *DMBA+S and the DMBA+T groups; are stascal values that communicate the comparison conducted between these two groups according to the DMBA group S: Sumac (Rhus coriaria) T: Terebinth (Pistacia terebinthus subsp. Palaesna) In a study inspecng the protein values in breast cancer conducted by Dong et al. [25], determined that GSTP1 protein levels are very low in the human breast cancer cell line MCF- 7. This study is parallel with the study in the literature in that it demonstrated a decrease in protein levels even though it was not stascally meaningful in the DMBA-caused breast cancer group. Addionally, our treatment groups (DMBA+S and DMBA+T) demonstrated increases compared to the DMBA group. MDA values The MDA levels in cardiac ssues were demonstrated in TABLE II. Relave to the C group, the DMBA, DMBA+T, and DMBA+S groups demonstrated signiﬁcant increases (P<0.001) while the S group demonstrated a disnct decrease (P<0.001), and the T group demonstrated a smaller decrease (P<0.05). (TABLE II). 3 of 6

Revista Cienﬁca, FCV-LUZ / Vol. XXXV UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico TABLE II MDA levels of cardiac ssue (nmol/gr) GROUPS MDA (nmol/gr) Control 89.80±36.05 S 65.94±4.80 d T 86.78±6.96 a DMBA 138.28±25.14 d DMBA+S 105.87±21.17 d,d DMBA+T 113.01±11.03 d,c *d: P<0.001; c: P<0.01; b: P<0.05; a: P>0.05. * The 2 nd leers in the *DMBA+S and the DMBA+T groups; are stascal values that communicate the comparison conducted between these two groups according to the DMBA group. S: Sumac (Rhus coriaria) T: Terebinth (Pistacia terebinthus subsp. Palaesna) The characterizaon with High-Performance Liquid Chromatography (HPLC) of P. terebinthus’ raw extracts revealed that it is rich in terms of luteolin and luteolin-7-glucozoid. It was reported that by eliminang the free radicals of these secondary metabolites, it demonstrates strong anoxidant acvity with protecve properes against the risk of cancer [26]. A previously conducted study invesgated the tumor growth inhibing eﬀects luteolin, which is abundantly contained in P. terebinthus, on breast cancer cell lines (MDA-MB-231) with negave estrogen receptors (ER), and reported at the end that it suppresses the contribuon of 3H, which depicts luteolin’s cell growth inhibion, that it stops the cell cycle in the G2/M and S phases, and that it has apoptoc acvity. In conclusion, it was reported that luteolin eﬀecvely suppressed the MDA-MB-231 ER-negave breast cancer cell growth, and that it has ancancer acvity due to its demonstraon of inhibive eﬀects on cancer cell survival [27]. The ancancer eﬀect of Rhus coriaria, on the other hand, was inspected on a three-type breast cancer cell line (MDA-MB-231, MCF-7, and T47D) level. The ethanolic extract of R. coriaria (RCE), depending on me and concentraon, was reported to stop the cell cycle in the G1 phase and inhibit the proliferaon of these cell lines by inducng senescence [14]. In a previously conducted study, Hamdy et al. [28] measured the reducing acvity eﬀects of Hesperidin (HES), which is a ﬂavanone glycoside, as well as Cyperus esculentus tubers (Tiger Nut (TN)) on cancer formed by DMBA. To this end, when the MDA levels in the serum are compared to the control group, while the DMBA and DMBA+TN groups demonstrated meaningful increases, a comparison with DMBA revealed that the DMBA+HES group demonstrated decreases of signiﬁcant levels. Another study examining the protecve eﬀects of Berberine, an alkaloid found in plants, on DMBA-induced breast cancer in female Sprague Dawley rats reported signiﬁcant increases in MDA in the DMBA-treated groups. The study reported that pre- and post-treatment with Berberine provided signiﬁcant protecon against DMBA-induced increases in MDA [29]. GSH values The changes in the GSH levels of cardiac ssues were depicted in TABLE III. When compared to the C group, while the GSH levels of the S and T groups demonstrated clear increases (P<0.05, P<0.001), with the DMBA group being in the lead, the DMBA+S and DMBA+T groups, in order, demonstrated decreases of varying degrees (P<0.05, P<0.001). The GSH levels of groups with added DMBA, when compared to the DMBA group; demonstrated a more disnct increase in the DMBA+S group while demonstrang smaller increases in the DMBA+T group (P<0.001, P<0.05). TABLE III GSH values of the cardiac ssue (µg/gr) GROUPS GSH (µg/gr) C 397.27±19.09 S 456.57±12.83 d T 414.32±23.76 b DMBA 344.60±40.63 d DMBA+S 374.86±56.41 b,b DMBA+T 351.07±38.80 d,a *d: p<0.001; c: p<0.01; b: p<0.05; a: p>0.05. * The 2 nd leers in the *DMBA+S and the DMBA+T groups; are stascal values that communicate the comparison conducted between these two groups according to the DMBA group. S: Sumac (Rhus coriaria) T: Terebinth (Pistacia terebinthus subsp. Palaesna) Reduced GSH prevents or limits ssue damage by scavenging free radicals in the cell [30]. Therefore, a decrease in the GSH levels of cancer groups demonstrate the beginning of oxidave stress [31]. In a previously conducted study, Hamdy et al. [28] measured the reducing acvity eﬀects of HES, which is a ﬂavanone glycoside, as well as Tiger Nut (TN) on cancer formed by DMBA. In the study by Hamdy et al. [28], serum GSH levels showed signiﬁcant decreases in DMBA and DMBA+TN levels compared to the control group, while they showed signiﬁcant increases in the DMBA+HES group compared to the DMBA group. In a breast cancer study where Berberine was applied, it was reported that GSH acvies showed regeneraon as a result of pre- and post-treatment [29]. This study is similar to other studies in terms of decreases in GSH acvity. Anoxidant enzymes acvies The CAT, GST, and SOD enzyme levels in cardiac ssues were depicted in TABLE IV. When compared to the C group, the CAT and GST enzymes, with the DMBA group being the lead, demonstrated clear decreases of varying degrees in the DMBA+S and DMBA+T groups (P<0.05, P<0.01, P<0.001). On the other hand, when the S and T groups are compared to the control group; while the S and T groups demonstrated decreases in the CAT enzyme, the GST and SOD enzymes were observed to increase in varying levels. When compared to the DMBA group, the enzyme levels of the groups with added DMBA, with the DMBA+S group being the lead, demonstrated disnct increases (P>0.05, P<0.05, P<0.01, P<0.001). 4 of 6

Protecve Eﬀect Against the Negave Eﬀects of Breast Cancer / Erdem et al. UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico TABLE IV CAT, GST and SOD acvies of cardiac ssue GROUPS CAT (μg/g/1dk) GST (μg/g/1dk) SOD (% İnhibisyon) C 995.89±54.81 9.32±0.43 56.15±5.19 S 893.65±82,70 b 9.79±0.98 b 77.24±4.04 d T 886.99±66.05 c 9.35±0.65 a 73.81±5.76 d DMBA 879.01±58.44 d 9.02±0.82 d 58.43±6.23 a DMBA+S 978.62±68.10 c,c 9.22±1.55 d,a 60.66±8.93 b,d DMBA+T 959.72±89.54 b,c 9.09±2.16 d,a 70.83±5.28 b,b *d: p<0.001; c: p<0.01; b: p<0.05; a: p>0.05. * The 2 nd leers in the *DMBA+S and the DMBA+T groups; are stascal values that communicate the comparison conducted between these two groups according to the DMBA group. S: Sumac (Rhus coriaria) T: Terebinth (Pistacia terebinthus subsp. Palaesna) Enzyme anoxidant defense systems such as reduced SOD, CAT and glutathione peroxidase prevent ssue damage by clearing free radicals in the cell. By metabolizing free radicals, SOD turns superoxide anions into H 2 O 2 , protecng cells from lipid peroxidaon [30, 31]. Catalase, on the other hand, fulﬁlls this goal by turning H 2 O 2 into H 2 O and O 2 [32]. In the study by Handy et al. [28], serum SOD, CAT and GSH-Px acvies showed signiﬁcant decreases in DMBA and DMBA+TN levels compared to the control group, while they showed signiﬁcant increases in the DMBA+HES group compared to the DMBA group. In the berberine study, regeneraons in SOD and CAT acvies were also reported as a result of pre- and post- treatment [29]. Another similar study regarding GST acvaon in breast cancer conducted by Kadam and Abhang [33] recorded a signiﬁcant decrease in the GST levels of breast cancer paents due to increased oxidave stress. This study is similar to previous studies in terms of decreases in anoxidant enzymes. CONCLUSION As a result of this study, an increase in MDA levels, an indicator of lipid peroxidaon, was detected in DMBA groups, especially compared to the C group, and a decrease was detected in anoxidant-added DMBA groups, especially in the sumac group. The ﬁndings also support literature on anoxidant enzyme acvies, which are indicators of cancer. These results suggest that terebinth and sumac extracts may play a role in counteracng the oxidave eﬀects of breast cancer on other organs. However, it’s important to note that our results require molecular and pathological support before these plant extracts or their ingredients can be used in pharmaceucals or similar dietary supplements. Funding This study was supported by the Fırat University Scienﬁc Research Projects Coordinaon Unit (FÜBAP) with the project number FF.18.14. Conﬂicts of Interest The authors declare no conﬂict of interest. 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