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Volume 14, Issue 1 (4-2024)                   cmja 2024, 14(1): 3-12 | Back to browse issues page


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Bahrami S, Babaei N, Esmaeili Gouvarchin Ghaleh H, Mohajeri Borazjani J, Farzanehpour M. Evaluation of the Anti-inflammatory Effect of Aqueous Extract of Pistacia atlantica Gum in an Experimental Model of Ulcerative Colitis. cmja 2024; 14 (1) :3-12
URL: http://cmja.arakmu.ac.ir/article-1-968-en.html
1- Department of Cell and Molecular Biology, Bushehr Branch, Islamic Azad University, Bushehr, Iran
2- Department of Cell and Molecular Biology, Bushehr Branch, Islamic Azad University, Bushehr, Iran , nahid.babaei@iau.ac.ir
3- Applied Virology Research Center, Baqiyatullah University of Medical Sciences, Tehran, Iran
4- Department of Fisheries and Natural Resources, Bushehr Branch, Islamic Azad University, Bushehr, Iran
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INTRODUCTION
Ulcerative colitis, a chronic inflammatory condition, affects various age groups. Inflammation in colonic mucosa leads to the release of cells, causing lipid peroxidation, increased permeability, and inflammation to spread. The induction of colitis in rodents through acetic acid injection mirrors the acute phase in humans. Current treatments, such as corticosteroids and aminosalicylates, have severe side effects. Mesalazine, a frontline treatment, inhibits inflammatory mediators. Nevertheless, some patients do not respond well and have an increased risk of colorectal cancer. Research focuses on finding effective drugs with minimal side effects and exploring herbal remedies, such as Pistacia atlantica resin.

METHODS
Using 20 BALB/c mice, the enzyme myeloperoxidase activity was assessed by combining 100 microliters of tetramethyl benzidine solution (pH 5) with 10 microliters of homogenized samples and 80 microliters of 0.75 mM H2O2. Absorbance was measured at 450nm after halting the reaction with 50 microliters of 2 molar H2SO4. a Griess reagent was used to evaluate nitric oxide activity in colon tissue, A mixture of 50 microliters of Griess reagent and 50 microliters of homogenized colon tissue was prepared, and absorption at 540nm was measured after the addition of 2/1 molar hydrochloric acid. The isolation of spleen cells and evaluation using Thiazolyl Blue Tetrazolium Bromide (MTT) were conducted with 20 BALB/c mice. The cells were exposed to a PHA solution, and absorbance at 550 nanometers was measured after adding DMSO. The analysis of inflammatory cytokines, IL-1β, TNF-α, and IL-6 in spleen cells, as well as gene expression in colon tissue (COX-2, iNOS, IL-1β, IL-6, TNF-α), was performed as previously described. Statistical analysis used one-way ANOVA. All data are presented as mean±standard deviation, and statistical significance was considered for p-values less than 0.05. The analyses were conducted using SPSS software (version 24).

RESULTS
Using 20 BALB/c mice, disease activity increased significantly in untreated colitis compared to healthy mice (P<0.0001). Aqueous extract of P. atlantica gum and Mesalazine reduced disease activity, with Mesalazine displaying the most significant decrease (P<0.0001). Myeloperoxidase and nitric oxide activity increased in untreated colitis, and both P. atlantica gum extract and Mesalazine reduced these activities significantly. Spleen cell proliferation was higher in untreated colitis, reduced by P. atlantica gum extract and Mesalazine (P<0.0001). Cytokine levels (IL-1ß, IL-6, and TNF-α) increased in untreated colitis, and both interventions significantly lowered cytokine activity, with Mesalazine being the most effective (P<0.0001). Gene expression (IL-1ß, IL-6, TNF-α, iNOS, and COX-2) was significantly reduced by P. atlantica gum extract and Mesalazine compared to untreated colitis (P<0.0001).

CONCLUSION
In the untreated colitis model, the aqueous extract of P. atlantica gum and Mesalazine significantly reduced nitric oxide, managing crucial indicators of inflammation. For instance, myeloperoxidase, indicative of neutrophil density in inflamed tissue, decreased with the administration of P. atlantica gum extract and Mesalazine, signifying a reduction in inflammation in the inflamed tissue. Moreover, phenolic compounds in P. atlantica, such as alpha-pinene and beta-pinene, recognized as the main active constituents in the gum extract, contributed to the attenuation of colitis inflammatory markers, including the reduction of pro-inflammatory cytokines (IL-1ß, IL-6, and TNF-α), and the expression of COX-2 and iNOS genes.

Ethical Considerations
Compliance with ethical guidelines
All the steps of this research are in compliance with ethical principles. This study has been registered in Baqiyatullah University of Medical Sciences (code of ethics: IR.BMSU.AEC.1400.001).

Funding
There is no funding support.

Authors’ Contributions
The authors contributed equally to the conceptualization and writing of the article. All of the authors approved the content of the manuscript and agreed on all aspects of the work.

Conflict of Interest
The authors declared no conflict of interest.

Acknowledgments
The present article was extracted from a doctoral thesis submitted by Shabnam Bahrami. The authors would like to thank those who assisted us in this research project. 
Type of Study: Research | Subject: Medicinal Plants

References
1. Sandborn WJ, Ferrante M, Bhandari BR, Berliba E, Feagan BG, Hibi T, Tuttle JL, Klekotka P, Friedrich S, Durante M, Morgan-Cox M. Efficacy and safety of mirikizumab in a randomized phase 2 study of patients with ulcerative colitis. Gastroenterology. 2020;158(3):537-549. [doi:10.1053/j.gastro.2019.08.043] [pmid:31493397]
2. Lukin D, Faleck D, Xu R, Zhang Y, Weiss A, Aniwan S, Kadire S, Tran G, Rahal M, Winters A, Chablaney S. Comparative safety and effectiveness of vedolizumab to tumor necrosis factor antagonist therapy for ulcerative colitis. Clinical Gastroenterology and Hepatology. 2022;20(1):126-135. [doi:10.1016/j.cgh.2020.10.003]
3. Vaezi MF, Rustagi PK, Elson CO. Transient protein S deficiency associated with cerebral venous thrombosis in active ulcerative colitis. Am J Gastroenterol. 1995;90(2). [pmid:7847309]
4. El Mahdy RN, Nader MA, Helal MG, Abu-Risha SE, Abdelmageed ME. Eicosapentaenoic acid mitigates ulcerative colitis-induced by acetic acid through modulation of NF-κB and TGF-β/EGFR signaling pathways. Life Sci. 2023;327:121820. [doi:10.1016/j.lfs.2023.121820] [pmid:37263490]
5. Iacucci M, de Silva S, Ghosh S. Mesalazine in inflammatory bowel disease: a trendy topic once again?. Can J Gastroenterol. 2010; 24:127-133. [doi:10.1155/2010/586092] [pmid:20151072]
6. Bohm M, Xu R, Zhang Y, Varma S, Fischer M, Kochhar G, Boland B, Singh S, Hirten R, Ungaro R, Shmidt E. Comparative safety and effectiveness of vedolizumab to tumour necrosis factor antagonist therapy for Crohn's disease. Aliment Pharmacol Ther. 2020;52(4):669-681. [doi:10.1111/apt.15921] [pmid:32656800]
7. Gourine N, Yousfi M, Bombarda I, Nadjemi B, Gaydou E. Seasonal variation of chemical composition and antioxidant activity of essential oil from Pistacia atlantica Desf. leaves. Journal of the American Oil Chemists' Society. 2010; 87(2):157-166. [doi:10.1007/s11746-009-1481-5]
8. Ahmed HM. Traditional uses of Kurdish medicinal plant Pistacia atlantica subsp. kurdica Zohary in Ranya, Southern Kurdistan. Genet Resour Crop Evol . 2017; 64(6):1473-84. [doi:10.1007/s10722-017-0522-4]
9. Tahmourespour A, Aminzadeh A, Salehifard I. Anti-adherence and anti-bacterial activities of Pistacia atlantica resin extract against strongly adherent Streptococcus mutans strains. Dent Res J. 2022;19. [pmid:35669603]
10. Shakarami Z, Ghaleh HE, Motlagh BM, Sheikhian A, Kondori BJ. Evaluation of the protective and therapeutic effects of Pistacia atlantica gum aqueous extract on cellular and pathological aspects of experimental asthma in Balb/c mice. Avicenna J Phytomed. 2019 ;9(3):248. [pmid:31143692]
11. Falahi E, Delshadian Z, Ahmadvand H, Shokri Jokar S. Head space volatile constituents and antioxidant properties of five traditional Iranian wild edible plants grown in west of Iran. AIMS Agriculture and Food. 2019: 26.
12. Palla AH, Iqbal NT, Minhas K, Gilani AH. Flaxseed extract exhibits mucosal protective effect in acetic acid induced colitis in mice by modulating cytokines, antioxidant and anti-inflammatory mechanisms. Int Immunopharmacol. 2016 ;38:153-166. [doi:10.1016/j.intimp.2016.04.043] [pmid:27280586]
13. Gheibi S, Hashemi SR, Karimipour M, Motlagh BM, Ghaleh HE. Synergistic effects of hydro extract of jujube fruit in combination with Mesalazine (orally) and Asacol (intra-colonic) administration in ameliorating animal model of ulcerative colitis. Journal of Coloproctology. 2018 ;38:275-282.
14. Park YH, Kim N, Shim YK, Choi YJ, Nam RH, Choi YJ, Ham MH, Suh JH, Lee SM, Lee CM, Yoon H. Adequate dextran sodium sulfate-induced colitis model in mice and effective outcome measurement method. J Cancer Prev. 2015; 20(4):260. [doi:10.15430/jcp.2015.20.4.260] [pmid:26734588]
15. Pulli B, Ali M, Forghani R, Schob S, Hsieh KL, Wojtkiewicz G, Linnoila JJ, Chen JW. Measuring myeloperoxidase activity in biological samples. PloS one. 2013 ;8(7):e67976. [doi:10.1371/journal.pone.0067976] [pmid:23861842]
16. Mashhouri S, Froushani SM, Tehrani AA. Non-Adherent Bone Marrow-Derived Mesenchymal Stem Cells Ameliorate Clinical Manifestations and Inflammation in an Experimental Model of Ulcerative Colitis in Rats. Iran J Med Sci. 2020; 45(5):341. [doi:10.30476/ijms.2020.72514.0] [pmid:33060877]
17. Froushani SM, Zarei L, Ghaleh HE, Motlagh BM. Estragole and methyl-eugenol-free extract of Artemisia dracunculus possesses immunomodulatory effects. Avicenna J Phytomed. 2016;6(5):526. [pmid:27761422]
18. Jahantigh M, Froushani SM, Ahangaran NA. Benefits of bone marrow-derived mesenchymal stem cells primed with estradiol in alleviating collagen-induced arthritis. Iran J Basic Med Sci. 2023; 26(4):400. [doi:10.22038/ijbms.2023.68112.14882] [pmid:37009006]
19. Lü JM, Lin PH, Yao Q, Chen C. Chemical and molecular mechanisms of antioxidants: experimental approaches and model systems. J Cell Mol Med. 2010; 14(4):840-860. [doi:10.1111/j.1582-4934.2009.00897.x] [pmid:19754673]
20. Haghdoost, F., Baradaran Mahdavi, M. M., Zandifar, A., Sanei, M. H., Zolfaghari, B., & Javanmard, S. H. (2013). Pistacia atlantica resin has a dose-dependent effect on angiogenesis and skin burn wound healing in rat. Evid Based Complement Alternat Med. 2013 :893425. [doi:10.1155/2013/893425] [pmid:24285978]
21. He J, Liang J, Zhu S, Zhao W, Zhang Y, Sun W. Protective effect of taurohyodeoxycholic acid from Pulvis Fellis Suis on trinitrobenzene sulfonic acid induced ulcerative colitis in mice. Eur J Pharmacol. 2011;670(1):229-235. [doi:10.1016/j.ejphar.2011.08.036] [pmid:21925164]
22. Connelly L, Jacobs AT, Palacios-Callender M, Moncada S, Hobbs AJ. Macrophage endothelial nitric-oxide synthase autoregulates cellular activation and pro-inflammatory protein expression. J Biol Chem. 2003; 278(29):26480-7. [doi:10.1074/jbc.m302238200] [pmid:12740377]
23. He J, Liang J, Zhu S, Li J, Zhang Y, Sun W. Anti-inflammatory effects of Pulvis Fellis Suis extract in mice with ulcerative colitis. J Ethnopharmacol. 2011; 138(1):53-59. [doi:10.1016/j.jep.2011.08.019] [pmid:21872653]
24. Lopes LD, Marques RB, Fernandes HB, Pereira SD, Ayres MC, Chaves MH, Almeida FR. Mechanisms of the antinociceptive action of (−) epicatechin obtained from the hydroalcoholic fraction of Combretum leprosum Mart & Eic in rodents. J Biomed Sci. 2012;19:1-6. [doi:10.1186/1423-0127-19-68] [pmid:22830928]
25. Dudeck J, Kotrba J, Immler R, Hoffmann A, Voss M, Alexaki VI, Morton L, Jahn SR, Katsoulis-Dimitriou K, Winzer S, Kollias G. Directional mast cell degranulation of tumor necrosis factor into blood vessels primes neutrophil extravasation. Immunity. 2021;54(3):468-483. [doi:10.1016/j.immuni.2020.12.017] [pmid:33484643]
26. Ashraf K, Esmaeli E, Shahinfard N, Ansari R, Parvin N, Namjoo A, Borjian S, Shirzad H, Mansouri S, Rafieyan M. The effect of hydroalcoholic extracts of Zizipus vulgaris L. on burn healing. Journal of Shahrekord University of Medical Sciences. 2011; 12(4):78-82.
27. Bossone C, Hosseini JM, Piñeiro-Carrero V, Shea-Donohue T. Alterations in spontaneous contractions in vitro after repeated inflammation of rat distal colon. Am J Physiol Gastrointest Liver Physiol. 2001; 280(5):G949-57. [doi:10.1152/ajpgi.2001.280.5.g949] [pmid:11292604]
28. Cho EJ, Shin JS, Noh YS, Cho YW, Hong SJ, Park JH, Lee JY, Lee JY, Lee KT. Anti-inflammatory effects of methanol extract of Patrinia scabiosaefolia in mice with ulcerative colitis. J Ethnopharmacol. 2011; 136(3):428-435. doi: 10.1016/j.jep.2010.04.047 pmid: 20573566 [doi:10.1016/j.jep.2010.04.047] [pmid:20573566]
29. Gharazi P, Momtaz S, Rezaei Z, Rahimifard M, Baeeri M, Abdollahi A, Abdollahi M, Zare K, Farzaei MH. Protective effect of a formulation containing Pistacia atlantica oleo-gum-resin and honey on experimental model of acetic acid-induced colitis in rats. Research Journal of Pharmacognosy. 2021; 8(2):37-49. [doi:10.22127/rjp.2021.260288.1647]
30. Ostovan M, Fazljou SM, Khazraei H, Araj Khodaei M, Torbati M. The anti-inflammatory effect of Pistacia lentiscus in a rat model of colitis. J Inflamm Res. 2020;13: 369-376. [doi:10.2147/jir.s259035] [pmid32801830]
31. Gholami M, Ghasemi-Niri SF, Maqbool F, Baeeri M, Memariani Z, Pousti I, Abdollahi M. Experimental and Pathalogical study of Pistacia atlantica, butyrate, Lactobacillus casei and their combination on rat ulcerative colitis model. Pathol Res Pract. 2016; 212(6):500-508. [doi:10.1016/j.prp.2016.02.024] [pmid:26972417]
32. Honmore V, Kandhare A, Zanwar AA, Rojatkar S, Bodhankar S, Natu A. Artemisia pallens alleviates acetaminophen induced toxicity via modulation of endogenous biomarkers. Pharm Biol. 2015; 53(4):571-581. [doi:10.3109/13880209.2014.934382] [pmid:25339313]
33. Zhou M, He J, Shen Y, Zhang C, Wang J, Chen Y. New frontiers in genetics, gut microbiota, and immunity: a rosetta stone for the pathogenesis of inflammatory bowel disease. Biomed Res Int. 2017;2017:8201672. [doi:10.1155/2017/8201672] [pmid: 28831399]
34. Minaiyan M, Karimi F, Ghannadi A. Anti-inflammatory effect of Pistacia atlantica subsp. kurdica volatile oil and gum on acetic acid-induced acute colitis in rat. Res J Pharmacogn. 2015; 2(2):1-2.
35. Kaliora AC, Stathopoulou MG, Triantafillidis JK, Dedoussis GV, Andrikopoulos NK. Chios mastic treatment of patients with active Crohn's disease. World J Gastroenterol. 2007;13(5):748. doi: 10.3748/wjg.v13.i5.748 [doi:10.3748/wjg.v13.i5.748] [pmid: 17278198]
36. Tavakoli J, Hajpour Soq K, Yousefi A, Estakhr P, Dalvi M, Mousavi Khaneghah A. Antioxidant activity of Pistacia atlantica var mutica kernel oil and it's unsaponifiable matters. J Food Sci Technol. 2019; 56:5336-45. [doi: 10.1007/s13197-019-04004-0] [pmid: 31749481]
37. Mahjoub F, Rezayat KA, Yousefi M, Mohebbi M, Salari R. Pistacia atlantica Desf. A review of its traditional uses, phytochemicals and pharmacology. J Med Life. 2018; 11(3):180. doi: 10.25122/jml-2017-0055 pmid: 30364651 [doi:10.25122/jml-2017-0055] [pmid: 30364651]

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