Top

BMC Complementary Medicine and Therapies

Published in:

Open Access 01-12-2021 | Research

Salvia miltiorrhiza hydroalcoholic extract inhibits postoperative peritoneal adhesions in rats

Authors: Abbas Raisi, Omid Dezfoulian, Farshid Davoodi, Shayan Taheri, Soroush Afshar Ghahremani

Published in: BMC Complementary Medicine and Therapies | Issue 1/2021

Abstract

Background

One of the most prevalent postoperative complications is believed to be intra-abdominal peritoneal adhesions, which is followed by several complications. Several adhesion prevention products have been examined, yet none of them were found to be completely effective. The current research is conducted to evaluate the beneficial effects of Salvia miltiorrhiza hydroalcoholic extract in inhibiting postoperative peritoneal adhesions in rats.

Methods

Forty rats were randomly classified into five equal groups (n = 8): 1) the normal group did not undergo surgical operations, 2) the control group in which the adhesion was induced, and which did not receive any treatment, 3) distilled water group that received distilled water, and 4,5) treatment groups treated with 1 and 5% of Salvia miltiorrhiza hydroalcoholic extract. The rats were euthanized 14 days following the surgery and the macroscopic score, the microscopic score of granulomatous inflammation and granulation tissue formation, IHC markers (vimentin, CD31, IL-1β, COX-2, and iNOS), and oxidative stress biomarkers (MDA, GPx, CAT, and TAC) were assessed in the experimental groups of the study.

Results

The difference between the control group and other groups for the adhesions macroscopic score, microscopic score, IHC markers, and oxidative stress biomarkers was significant (p < 0.05). Distilled water had no protective effect on the formation of peritoneal adhesions. Salvia miltiorrhiza treatment in two different doses significantly reduced macroscopic and microscopic scores, MDA concentration, Vimentin, IL-1β, COX-2, and iNOS compared to the control group (p < 0.05). The levels of GPx, CAT, and TAC in the treatment groups increased significantly compared with the control group (p < 0.05). Our findings revealed that a higher dose of Salvia miltiorrhiza was more effective in reducing peritoneal adhesions, proinflammatory and mesenchymal cell markers, and oxidative stress.

Conclusions

Salvia miltiorrhiza extract, owing to its strong antioxidant and anti-inflammatory properties, could effectively reduce peritoneal adhesions. Therefore, Salvia miltiorrhiza is recommended to be used as an effective anti-peritoneal post-operative adhesive agent.

Catena F, Di Saverio S, Coccolini F, Ansaloni L, De Simone B, Sartelli M, et al. Adhesive small bowel adhesions obstruction: evolutions in diagnosis, management and prevention. World J Gastrointest Surg. 2016;8(3):222–31. https://doi.org/10.4240/wjgs.v8.i3.222.CrossRefPubMedPubMedCentral

Binnebösel M, Klinge U, Rosch R, Junge K, Lynen-Jansen P, Schumpelick V. Morphology, quality, and composition in mature human peritoneal adhesions. Langenbeck's Arch Surg. 2008;393(1):59–66. https://doi.org/10.1007/s00423-007-0198-x.CrossRef

Tsauo J, Song H-Y, Choi EY, Kim D-K, Kim KY, Park J-H, et al. EW-7197, an oral transforming growth factor β type I receptor kinase inhibitor, for preventing peritoneal adhesion formation in a rat model. Surgery. 2018;164(5):1100–8. https://doi.org/10.1016/j.surg.2018.07.005.CrossRefPubMed

Ten Broek RP, Issa Y, van Santbrink EJ, Bouvy ND, Kruitwagen RF, Jeekel J, et al. Burden of adhesions in abdominal and pelvic surgery: systematic review and met-analysis. Bmj. 2013;347(oct03 1):f5588. https://doi.org/10.1136/bmj.f5588.CrossRefPubMedPubMedCentral

Van Goor H. Consequences and complications of peritoneal adhesions. Color Dis. 2007;9(s2):25–34. https://doi.org/10.1111/j.1463-1318.2007.01358.x.CrossRef

Ellis H, Moran BJ, Thompson JN, Parker MC, Wilson MS, Menzies D, et al. Adhesion-related hospital readmissions after abdominal and pelvic surgery: a retrospective cohort study. Lancet. 1999;353(9163):1476–80. https://doi.org/10.1016/S0140-6736(98)09337-4.CrossRefPubMed

Lower AM, Hawthorn RJ, Emeritus HE, O'Brien F, Buchan S, Crowe AM. The impact of adhesions on hospital readmissions over ten years after 8849 open gynaecological operations: an assessment from the surgical and clinical adhesions research study. BJOG. 2000;107(7):855–62. https://doi.org/10.1111/j.1471-0528.2000.tb11083.x.CrossRefPubMed

Liakakos T, Thomakos N, Fine PM, Dervenis C, Young RL. Peritoneal adhesions: etiology, pathophysiology, and clinical significance. Dig Surg. 2001;18(4):260–73. https://doi.org/10.1159/000050149.CrossRefPubMed

Rahimi VB, Shirazinia R, Fereydouni N, Zamani P, Darroudi S, Sahebkar AH, et al. Comparison of honey and dextrose solution on post-operative peritoneal adhesion in rat model. Biomed Pharmacother. 2017;92:849–55. https://doi.org/10.1016/j.biopha.2017.05.114.CrossRefPubMed

10.

Cheong Y, Laird S, Li T, Shelton J, Ledger W, Cooke I. Peritoneal healing and adhesion formation/reformation. Hum Reprod Update. 2001;7(6):556–66. https://doi.org/10.1093/humupd/7.6.556.CrossRefPubMed

11.

Kamel RM. Prevention of postoperative peritoneal adhesions. Eur J Obstet Gynecol Reprod Biol. 2010;150(2):111–8. https://doi.org/10.1016/j.ejogrb.2010.02.003.CrossRefPubMed

12.

Abad ANA, Nouri MHK, Tavakkoli F. Effect of Salvia officinalis hydroalcoholic extract on vincristine-induced neuropathy in mice. Chin J Nat Med. 2011;9(5):354–8.

13.

Wang X-P, Wang P-F, Bai J-Q, Gao S, Wang Y-H, Quan L-N, et al. Investigating the effects and possible mechanisms of danshen-honghua herb pair on acute myocardial ischemia induced by isoproterenol in rats. Biomed Pharmacother. 2019;118:109268. https://doi.org/10.1016/j.biopha.2019.109268.CrossRefPubMed

14.

Naveed M, Wenhua L, Gang W, Mohammad IS, Abbas M, Liao X, et al. A novel ventricular restraint device (ASD) repetitively deliver Salvia miltiorrhiza to epicardium have good curative effects in heart failure management. Biomed Pharmacother. 2017;95:701–10. https://doi.org/10.1016/j.biopha.2017.07.126.CrossRefPubMed

15.

Chen G, Fu Y, Wu X. Protective effect of Salvia miltiorrhiza extract against renal ischemia-reperfusion-induced injury in rats. Molecules. 2012;17(2):1191–202. https://doi.org/10.3390/molecules17021191.CrossRefPubMedPubMedCentral

16.

Nan JX, Park EJ, Kang HC, Park PH, Kim JY, Sohn DH. Anti-fibrotic effects of a hot-water extract from Salvia miltiorrhiza roots on liver fibrosis induced by biliary obstruction in rats. J Pharm Pharmacol. 2001;53(2):197–204. https://doi.org/10.1211/0022357011775406.CrossRefPubMed

17.

Wong KK-K, Ho MT-W, Lin HQ, Lau K-F, Rudd JA, Chung RC-K, et al. Cryptotanshinone, an acetylcholinesterase inhibitor from Salvia miltiorrhiza, ameliorates scopolamine-induced amnesia in Morris water maze task. Planta Med. 2010;76(03):228–34. https://doi.org/10.1055/s-0029-1186084.CrossRefPubMed

18.

Zhang H-N, An C-N, Zhang H-N, Pu X-P. Protocatechuic acid inhibits neurotoxicity induced by MPTP in vivo. Neurosci Lett. 2010;474(2):99–103. https://doi.org/10.1016/j.neulet.2010.03.016.CrossRefPubMed

19.

Sun J, Huang SH, Tan BK-H, Whiteman M, Zhu YC, Wu YJ, et al. Effects of purified herbal extract of Salvia miltiorrhiza on ischemic rat myocardium after acute myocardial infarction. Life Sci. 2005;76(24):2849–60. https://doi.org/10.1016/j.lfs.2004.11.016.CrossRefPubMed

20.

Farahpour MR, Pirkhezr E, Ashrafian A, Sonboli A. Accelerated healing by topical administration of Salvia officinalis essential oil on Pseudomonas aeruginosa and Staphylococcus aureus infected wound model. Biomed Pharmacother. 2020;128:110120. https://doi.org/10.1016/j.biopha.2020.110120.CrossRefPubMed

21.

Liu H, Ma S, Xia H, Lou H, Zhu F, Sun L. Anti-inflammatory activities and potential mechanisms of phenolic acids isolated from Salvia miltiorrhiza F. alba roots in THP-1 macrophages. J Ethnopharmacol. 2018;222:201–7.CrossRef

22.

Ma S, Zhang D, Lou H, Sun L, Ji J. Evaluation of the anti-inflammatory activities of tanshinones isolated from Salvia miltiorrhiza var. alba roots in THP-1 macrophages. J Ethnopharmacol. 2016;188:193–9.CrossRef

23.

Peng K-Y, Gu J-F, Su S-L, Zhu Y, Guo J-M, Qian D-W, et al. Salvia miltiorrhiza stems and leaves total phenolic acids combination with tanshinone protect against DSS-induced ulcerative colitis through inhibiting TLR4/PI3K/AKT/mTOR signaling pathway in mice. J Ethnopharmacol. 2020;264:113052.CrossRef

24.

Min X, Zeng X, Zhao W, Han Z, Wang Y, Han Y, et al. Cryptotanshinone protects dextran sulfate sodium-induced experimental ulcerative colitis in mice by inhibiting intestinal inflammation. Phytother Res. 2020;34(10):2639.CrossRef

25.

Wu S, Wang Q, Wang J, Duan B, Tang Q, Sun Z, et al. Protocatechuic aldehyde from Salvia miltiorrhiza exhibits an anti-inflammatory effect through inhibiting MAPK signalling pathway. BMC Complement Med Ther. 2020;20(1):1–9.CrossRef

26.

Gao H, Sun W, Zhao J, Wu X, Lu J-J, Chen X, et al. Tanshinones and diethyl blechnics with anti-inflammatory and anti-cancer activities from Salvia miltiorrhiza Bunge (Danshen). Sci Rep. 2016;6(1):33720. https://doi.org/10.1038/srep33720.CrossRefPubMedPubMedCentral

27.

Lin T-H, Hsieh C-L. Pharmacological effects of Salvia miltiorrhiza (Danshen) on cerebral infarction. Chin Med. 2010;5(1):22. https://doi.org/10.1186/1749-8546-5-22.CrossRefPubMedPubMedCentral

28.

Yang S-A, Im N-K, Lee I-S. Effects of methanolic extract from Salvia miltiorrhiza Bunge on in vitro antithrombotic and antioxidative activities. Korean J Food Sci Technol. 2007;39(1):83–7.

29.

Davoodi F, Taheri S, Raisi A, Rajabzadeh A, Ahmadvand H, Hablolvarid MH, et al. Investigating the sperm parameters, oxidative stress and histopathological effects of salvia miltiorrhiza hydroalcoholic extract in the prevention of testicular ischemia reperfusion damage in rats. Theriogenology. 2020;144:98–106. https://doi.org/10.1016/j.theriogenology.2020.01.002.CrossRefPubMed

30.

Zhao J, Lou J, Mou Y, Li P, Wu J, Zhou L. Diterpenoid tanshinones and phenolic acids from cultured hairy roots of Salvia miltiorrhiza Bunge and their antimicrobial activities. Molecules. 2011;16(3):2259–67. https://doi.org/10.3390/molecules16032259.CrossRefPubMedPubMedCentral

31.

Kwag J-S, Baek S-H. Cytotoxicity and antimicrobial effects of extracts from Salvia miltiorrhiza. Saengyak Hakhoe Chi. 2003;34(4):293–6.

32.

Fang C-C, Chou T-H, Huang J-W, Lee C-C, Chen S-C. The small molecule inhibitor QLT-0267 decreases the production of fibrin-induced inflammatory cytokines and prevents post-surgical peritoneal adhesions. Sci Rep. 2018;8(1):1–12.

33.

Rizzo A, Spedicato M, Mutinati M, Minoia G, Angioni S, Jirillo F, et al. Peritoneal adhesions in human and veterinary medicine: from pathogenesis to therapy. Rev Immunopharmacol Immunotoxicol. 2010;32(3):481–94. https://doi.org/10.3109/08923970903524367.CrossRef

34.

Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol. 2010;8(6):e1000412. https://doi.org/10.1371/journal.pbio.1000412.CrossRefPubMedPubMedCentral

35.

Nair SK, Bhat IK, Aurora AL. Role of proteolytic enzyme in the prevention of postoperative intraperitoneal adhesions. Arch Surg. 1974;108(6):849–53. https://doi.org/10.1001/archsurg.1974.01350300081019.CrossRefPubMed

36.

Bi J, Zhang S, Du Z, Zhang J, Deng Y, Liu C, et al. Peripheral serotonin regulates postoperative intra-abdominal adhesion formation in mice. Sci Rep. 2017;7(1):1–12.CrossRef

37.

diZerega GS, Campeau JD. Peritoneal repair and post-surgical adhesion formation. Hum Reprod Update. 2001;7(6):547–55.CrossRef

38.

Askari VR, Rahimi VB, Zamani P, Fereydouni N, Rahmanian-Devin P, Sahebkar AH, et al. Evaluation of the effects of Iranian propolis on the severity of post operational-induced peritoneal adhesion in rats. Biomed Pharmacother. 2018;99:346–53. https://doi.org/10.1016/j.biopha.2018.01.068.CrossRefPubMed

39.

Fletcher NM, Jiang ZL, Diamond MP, Abu-Soud HM, Saed GM. Hypoxia-generated superoxide induces the development of the adhesion phenotype. Free Radic Biol Med. 2008;45(4):530–6. https://doi.org/10.1016/j.freeradbiomed.2008.05.002.CrossRefPubMedPubMedCentral

40.

Wu F, Liu W, Feng H, Long L, Hou L, Hou C. Application of Traditional Chinese Medicines in Postoperative Abdominal Adhesion. Evid Based Complement Alternat Med. 2020;1:2020.

41.

Oh J, Kuan KG, Tiong LU, Trochsler MI, Jay G, Schmidt TA, et al. Recombinant human lubricin for prevention of postoperative intra-abdominal adhesions in a rat model. J Surg Res. 2017;208:20–5. https://doi.org/10.1016/j.jss.2016.08.092.CrossRefPubMed

42.

Bayhan Z, Zeren S, Kocak FE, Kocak C, Akcılar R, Kargı E, et al. Antiadhesive and anti-inflammatory effects of pirfenidone in postoperative intra-abdominal adhesion in an experimental rat model. J Surg Res. 2016;201(2):348–55. https://doi.org/10.1016/j.jss.2015.11.033.CrossRefPubMed

43.

Parsaei P, Karimi M, Asadi SY, Rafieian-Kopaei M. Bioactive components and preventive effect of green tea (Camellia sinensis) extract on post-laparotomy intra-abdominal adhesion in rats. Int J Surg. 2013;11(9):811–5. https://doi.org/10.1016/j.ijsu.2013.08.014.CrossRefPubMed

44.

Karimi M, Parsaei P, Shafiei-Alavijeh S, Rafieian-Kopaei M, Asadi SY. Effect of silymarin alcoholic extract on surgery-induced intraperitoneal adhesion in rats. Surg Pract. 2016;20(1):27–33. https://doi.org/10.1111/1744-1633.12157.CrossRef

45.

Mahdy T, Mohamed G, Elhawary A. Effect of methylene blue on intra-abdominal adhesion formation in rats. Int J Surg. 2008;6(6):452–5. https://doi.org/10.1016/j.ijsu.2008.08.004.CrossRefPubMed

46.

Wei G, Wu Y, Gao Q, Shen C, Chen Z, Wang K, et al. Gallic acid attenuates postoperative intra-abdominal adhesion by inhibiting inflammatory reaction in a rat model. Med Sci Mon Int Med J Exp Clin Res. 2018;24:827.

47.

Salvemini D, Kim SF, Mollace V. Reciprocal regulation of the nitric oxide and cyclooxygenase pathway in pathophysiology: relevance and clinical implications. Am J Phys Regul Integr Comp Phys. 2013;304(7):R473–R87. https://doi.org/10.1152/ajpregu.00355.2012.CrossRef

48.

Burke SJ, Updegraff BL, Bellich RM, Goff MR, Lu D, Minkin SC Jr, et al. Regulation of iNOS gene transcription by IL-1β and IFN-γ requires a coactivator exchange mechanism. J Mol Endocrinol. 2013;27(10):1724–42. https://doi.org/10.1210/me.2013-1159.CrossRef

49.

Pata Ö, Yazıcı G, Apa DD, Tok E, Öz U, Kaplanoğlu M, et al. The effect of inducible nitric oxide synthase on postoperative adhesion formation in rats. Eur J Obstet Gynecol Reprod Biol. 2004;117(1):64–9. https://doi.org/10.1016/j.ejogrb.2003.10.034.CrossRefPubMed

50.

Lopez-Castejon G, Brough D. Understanding the mechanism of IL-1β secretion. Cytokine Growth Factor Rev. 2011;22(4):189–95. https://doi.org/10.1016/j.cytogfr.2011.10.001.CrossRefPubMedPubMedCentral

51.

Durmus AS, Yildiz H, Yaman I, Simsek H. Efficacy of vitamin E and selenium for the prevention of intra-abdominal adhesions in rats: uterine horn models. Clinics. 2011;66(7):1247–51. https://doi.org/10.1590/S1807-59322011000700021.CrossRefPubMedPubMedCentral

52.

Sogutlu G, Karabulut AB, Ara C, Cinpolat O, Isik B, Piskin T, et al. The effect of resveratrol on surgery-induced peritoneal adhesions in an experimental model. Mol Cell Biochem. 2007;25(2):217–20.

53.

Sortini D, Feo CV, Maravegias K, Carcoforo P, Pozza E, Liboni A, et al. Role of peritoneal lavage in adhesion formation and survival rate in rats: an experimental study. J Investig Surg. 2006;19(5):291–7. https://doi.org/10.1080/08941930600889409.CrossRef

Title: Salvia miltiorrhiza hydroalcoholic extract inhibits postoperative peritoneal adhesions in rats
Authors: Abbas Raisi
Omid Dezfoulian
Farshid Davoodi
Shayan Taheri
Soroush Afshar Ghahremani
Publication date: 01-12-2021
Publisher: BioMed Central
Published in: BMC Complementary Medicine and Therapies / Issue 1/2021
Electronic ISSN: 2662-7671
DOI: https://doi.org/10.1186/s12906-021-03300-7

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Salvia miltiorrhiza hydroalcoholic extract inhibits postoperative peritoneal adhesions in rats

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2021

Use of complementary and alternative therapies by patients with eye diseases: a hospital-based cross-sectional study from Palestine

Berberine ameliorates testosterone-induced benign prostate hyperplasia in rats

A review of pears (Pyrus spp.), ancient functional food for modern times

Vincetoxicum arnottianum modulates motility features and metastatic marker expression in pediatric rhabdomyosarcoma by stabilizing the actin cytoskeleton

Alkaloid and benzopyran compounds of Melicope latifolia fruit exhibit anti-hepatitis C virus activities

Protective effects of exosomes derived from lyophilized porcine liver against acetaminophen damage on HepG2 cells