Download PDF
Planta Med 2020; 86(06): 405-414
DOI: 10.1055/a-1118-3918
Biological and Pharmacological Activity
Original Papers
Georg Thieme Verlag KG Stuttgart · New York

Evaluation of the Effects of Peritoneal Lavage with Rosmarinus officinalis Extract against the Prevention of Postsurgical-Induced Peritoneal Adhesion

Yasamin Roohbakhsh‡
1   Pharmacological Research Center of Medicinal Plants, Mashhad University of Medical Sciences, Mashhad, Iran
,
Vafa Baradaran Rahimi‡
1   Pharmacological Research Center of Medicinal Plants, Mashhad University of Medical Sciences, Mashhad, Iran
2   Department of Persian Medicine, School of Persian and Complementary Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
,
Samaneh Silakhori
1   Pharmacological Research Center of Medicinal Plants, Mashhad University of Medical Sciences, Mashhad, Iran
,
Hamed Rajabi
1   Pharmacological Research Center of Medicinal Plants, Mashhad University of Medical Sciences, Mashhad, Iran
,
Pouria Rahmanian-Devin
1   Pharmacological Research Center of Medicinal Plants, Mashhad University of Medical Sciences, Mashhad, Iran
3   Department of Pharmaceutics, School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran
,
Alireza Samzadeh-Kermani
4   Department of Chemistry, Faculty of Science, University of Zabol, Zabol, Iran
,
Hassan Rakhshandeh
1   Pharmacological Research Center of Medicinal Plants, Mashhad University of Medical Sciences, Mashhad, Iran
,
Maede Hasanpour
5   Biotechnology Research Center, Pharmaceutical Technology Institute, Mashhad University of Medical Sciences, Mashhad, Iran
,
Mehrdad Iranshahi
5   Biotechnology Research Center, Pharmaceutical Technology Institute, Mashhad University of Medical Sciences, Mashhad, Iran
,
Seyed Hadi Mousavi
6   Medical Toxicology Research Center, Mashhad University of Medical Sciences, Mashhad, Iran
,
Vahid Reza Askari
1   Pharmacological Research Center of Medicinal Plants, Mashhad University of Medical Sciences, Mashhad, Iran
2   Department of Persian Medicine, School of Persian and Complementary Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
› Author AffiliationsSupported by: National Institute for Medical Research Development 971206
Further Information

Publication History

received 09 October 2019
revised 21 January 2020

accepted 06 February 2020

Publication Date:
25 February 2020 (online)

    Permissions and Reprints

Abstract

Postoperative adhesions are regarded as the major complication following abdominal surgery. Rosmarinus officinalis has shown antioxidative and anti-inflammatory effects. Therefore, we aimed to assess the influence of 70% v/v hydro-ethanolic extract of the aerial parts of R. officinalis against postoperative abdominal adhesions in a rat model. Forty-eight male Wistar rats (190 ± 20 g) were divided into six groups of eight: group 1 = normal group, without any surgical procedures, group 2 = control group, group 3 = vehicle group, and groups 3, 4, and 5 = experimental groups receiving 2 mL of 4, 2, or 1% w/v R. officinalis treatment. Adhesion levels were macroscopically examined. Additionally, the levels of inflammatory cytokines (interleukin-6, interleukin-1β, and TNF-α), growth factors (transforming growth factor-β1, and vascular endothelial growth factor), oxidative (NO, nitric oxide and MDA, malondialdehyde), and antioxidative (GSH, glutathione) factors were evaluated. Our results revealed that the adhesion score, interleukin-6, interleukin-1β, TNF-α, transforming growth factor-β1, vascular endothelial growth factor, NO, and MDA levels were significantly increased in the vehicle group, while the GSH level was diminished. R. officinalis treatment notably ameliorated the adhesion score following postoperative abdominal adhesions compared with the vehicle group. Our results also revealed that R. officinalis markedly reduced inflammatory cytokines, oxidative factors, fibrosis, and angiogenesis biomarkers, whereas it increased the antioxidative factor. Therefore, R. officinalis may be a potential candidate for the management of postoperative peritoneal adhesion.

Key words

Rosmarinus officinalis - peritoneal adhesion - inflammation - antioxidant activity - TGF-β - Lamiaceae
 

  • References

  • 1 Fortin CN, Saed GM, Diamond MP. Predisposing factors to post-operative adhesion development. Hum Reprod Update 2015; 21: 536-551
    CrossrefPubMedGoogle Scholar
  • 2 Ambler DR, Fletcher NM, Diamond MP, Saed GM. Effects of hypoxia on the expression of inflammatory markers IL-6 and TNF-a in human normal peritoneal and adhesion fibroblasts. Syst Biol Reprod Med 2012; 58: 324-329
    CrossrefPubMedGoogle Scholar
  • 3 Chegini N. TGF-β system: The principal profibrotic mediator of peritoneal adhesion formation. Semin Reprod Med 2008; 26: 298-312
    Article in Thieme ConnectPubMedGoogle Scholar
  • 4 Ivarsson ML, Diamond MP, Falk P, Holmdahl L. Plasminogen activator/plasminogen activator inhibitor-1 and cytokine modulation by the PROACT™ system. Fertil Steril 2003; 79: 987-992
    CrossrefPubMedGoogle Scholar
  • 5 Shavell VI, Saed GM, Diamond MP. Cellular metabolism: contribution to postoperative adhesion development. Reprod Sci 2009; 16: 627-634
    CrossrefPubMedGoogle Scholar
  • 6 Reed KL, Heydrick SJ, Aarons CB, Prushik S, Gower AC, Stucchi AF, Becker JM. A neurokinin-1 receptor antagonist that reduces intra-abdominal adhesion formation decreases oxidative stress in the peritoneum. Am J Physiol Gastrointest Liver Physiol 2007; 293: G544-G551
    CrossrefPubMedGoogle Scholar
  • 7 Callen D. On the regulation and control of fibrinolysis. Edward Kowalski Memorial Lecture. Thromb Haemost 1980; 43: 77-89
    Article in Thieme ConnectPubMedGoogle Scholar
  • 8 Borges RS, Ortiz BLS, Pereira ACM, Keita H, Carvalho JCT. Rosmarinus officinalis essential oil: A review of its phytochemistry, anti-inflammatory activity, and mechanisms of action involved. J Ethnopharmacol 2019; 229: 29-45
    CrossrefPubMedGoogle Scholar
  • 9 Yang LT, Liu X, Cheng DY, Fang X, Mu M, Hu XB, Nie L. [Effects of diterpene phenol extract of Rosmarinus officinalis on TGFbeta1 and mRNA expressions of its signaling pathway molecules in the lung tissue of pulmonary fibrosis rats]. Zhongguo Zhong Xi Yi Jie He Za Zhi 2013; 33: 819-824
    PubMedGoogle Scholar
  • 10 Mengoni ES, Vichera G, Rigano LA, Rodriguez-Puebla ML, Galliano SR, Cafferata EE, Pivetta OH, Moreno S, Vojnov AA. Suppression of COX-2, IL-1β and TNF-α expression and leukocyte infiltration in inflamed skin by bioactive compounds from Rosmarinus officinalis L. Fitoterapia 2011; 82: 414-421
    CrossrefPubMedGoogle Scholar
  • 11 Yeo IJ, Park JH, Jang JS, Lee DY, Park JE, Choi YE, Joo JH, Song JK, Jeon HO, Hong JT. Inhibitory effect of Carnosol on UVB-induced inflammation via inhibition of STAT3. Arch Pharm Res 2019; 42: 274-283
    CrossrefPubMedGoogle Scholar
  • 12 Kamel RM. Prevention of postoperative peritoneal adhesions. Eur J Obstet Gynecol Reprod Biol 2010; 150: 111-118
    CrossrefPubMedGoogle Scholar
  • 13 Kayaoglu HA, Ozkan N, Yenidogan E, Koseoglu RD. Effect of antibiotic lavage in adhesion prevention in bacterial peritonitis. Ulus Travma Acil Cerrahi Derg 2013; 19: 189-194
    CrossrefPubMedGoogle Scholar
  • 14 Askari VR, Rahimi VB, Zamani P, Fereydouni N, Rahmanian-Devin P, Sahebkar AH, Rakhshandeh H. Evaluation of the effects of Iranian propolis on the severity of post operational-induced peritoneal adhesion in rats. Biomed Pharmacother 2018; 99: 346-353
    CrossrefPubMedGoogle Scholar
  • 15 Sahbaz A, Isik H, Aynioglu O, Gungorduk K, Gun BD. Effect of intraabdominal administration of Allium sativum (garlic) oil on postoperative peritoneal adhesion. European journal of obstetrics, gynecology, and reproductive biology 2014; 177: 44-47
    CrossrefPubMedGoogle Scholar
  • 16 Alpay Z, Saed GM, Diamond MP. Postoperative adhesions: from formation to prevention. Semin Reprod Med 2008; 26: 313-321
    Article in Thieme ConnectPubMedGoogle Scholar
  • 17 Ghasemzadeh Rahbardar M, Amin B, Mehri S, Mirnajafi-Zadeh SJ, Hosseinzadeh H. Anti-inflammatory effects of ethanolic extract of Rosmarinus officinalis L. and rosmarinic acid in a rat model of neuropathic pain. Biomed Pharmacother 2017; 86: 441-449
    CrossrefPubMedGoogle Scholar
  • 18 Grissa I, Ezzi L, Chakroun S, Mabrouk A, Saleh AB, Braham H, Haouas Z, Cheikh HB. Rosmarinus officinalis L. ameliorates titanium dioxide nanoparticles and induced some toxic effects in ratsʼ blood. Environ Sci Pollut Res Int 2017; 24: 12474-12483
    CrossrefPubMedGoogle Scholar
  • 19 Medicherla K, Ketkar A, Sahu BD, Sudhakar G, Sistla R. Rosmarinus officinalis L. extract ameliorates intestinal inflammation through MAPKs/NF-kappaB signaling in a murine model of acute experimental colitis. Food Funct 2016; 7: 3233-3243
    CrossrefPubMedGoogle Scholar
  • 20 Tsauo J, Song HY, Choi EY, Kim DK, Kim KY, Park JH, Kim MT, Yoon SH, Lim YJ. EW-7197, an oral transforming growth factor beta type I receptor kinase inhibitor, for preventing peritoneal adhesion formation in a rat model. Surgery 2018; 164: 1100-1108
    CrossrefPubMedGoogle Scholar
  • 21 Lucas PA, Warejcka DJ, Young HE, Lee BY. Formation of abdominal adhesions is inhibited by antibodies to transforming growth factor-β1. J Surg Res 1996; 65: 135-138
    CrossrefPubMedGoogle Scholar
  • 22 Domitrovic R, Skoda M, Vasiljev Marchesi V, Cvijanovic O, Pernjak Pugel E, Stefan MB. Rosmarinic acid ameliorates acute liver damage and fibrogenesis in carbon tetrachloride-intoxicated mice. Food Chem Toxicol 2013; 51: 370-378
    CrossrefPubMedGoogle Scholar
  • 23 Lin SY, Wang YY, Chen WY, Liao SL, Chou ST, Yang CP, Chen CJ. Hepatoprotective activities of rosmarinic acid against extrahepatic cholestasis in rats. Food Chem Toxicol 2017; 108: 214-223
    CrossrefPubMedGoogle Scholar
  • 24 Condon ET, Cahill RA, OʼMalley DB, Aherne NJ, Redmond HP. Evaluation of postoperative peritoneal adhesion formation following perioperative nicotine administration. J Surg Res 2007; 140: 135-138
    CrossrefPubMedGoogle Scholar
  • 25 Cahill RA, Wang JH, Soohkai S, Redmond HP. Mast cells facilitate local VEGF release as an early event in the pathogenesis of postoperative peritoneal adhesions. Surgery 2006; 140: 108-112
    CrossrefPubMedGoogle Scholar
  • 26 Cao W, Hu C, Wu L, Xu L, Jiang W. Rosmarinic acid inhibits inflammation and angiogenesis of hepatocellular carcinoma by suppression of NF-kappaB signaling in H22 tumor-bearing mice. J Pharmacol Sci 2016; 132: 131-137
    CrossrefPubMedGoogle Scholar
  • 27 Rahimi VB, Shirazinia R, Fereydouni N, Zamani P, Darroudi S, Sahebkar AH, Askari VR. Comparison of honey and dextrose solution on post-operative peritoneal adhesion in rat model. Biomed Pharmacother 2017; 92: 849-855
    CrossrefPubMedGoogle Scholar
  • 28 Amaral GP, Dobrachinski F, de Carvalho NR, Barcelos RP, da Silva MH, Lugokenski TH, Dias GRM, de Lima Portella R, Fachinetto R, Soares FAA. Multiple mechanistic action of Rosmarinus officinalis L. extract against ethanol effects in an acute model of intestinal damage. Biomed Pharmacother 2018; 98: 454-459
    CrossrefPubMedGoogle Scholar
  • 29 Amaral GP, de Carvalho NR, Barcelos RP, Dobrachinski F, Portella RdL, da Silva MH, Lugokenski TH, Dias GRM, da Luz SCA, Boligon AA, Athayde ML, Villetti MA, Antunes Soares FA, Fachinetto R. Protective action of ethanolic extract of Rosmarinus officinalis L. in gastric ulcer prevention induced by ethanol in rats. Food Chem Toxicol 2013; 55: 48-55
    CrossrefPubMedGoogle Scholar
  • 30 Bakirel T, Bakirel U, Keleş OÜ, Ülgen SG, Yardibi H. In vivo assessment of antidiabetic and antioxidant activities of rosemary (Rosmarinus officinalis) in alloxan-diabetic rabbits. J Ethnopharmacol 2008; 116: 64-73
    CrossrefPubMedGoogle Scholar
  • 31 Rahimi VB, Askari VR, Mehrdad A, Sadeghnia HR. Boswellia serrata has promising impact on glutamate and quinolinic acid-induced toxicity on oligodendroglia cells: In vitro study. Acta Pol Pharm 2017; 74: 1803-1811
    PubMedGoogle Scholar
  • 32 Nair SK, Bhat IK, Aurora AL. Role of proteolytic enzyme in the prevention of postoperative intraperitoneal adhesions. Arch Surg 1974; 108: 849-853
    CrossrefPubMedGoogle Scholar
  • 33 Askari VR, Baradaran Rahimi V, Rezaee SA, Boskabady MH. Auraptene regulates Th1/Th2/TReg balances, NF-kappaB nuclear localization and nitric oxide production in normal and Th2 provoked situations in human isolated lymphocytes. Phytomedicine 2018; 43: 1-10
    CrossrefPubMedGoogle Scholar
  • 34 Borras-Linares I, Stojanovic Z, Quirantes-Pine R, Arraez-Roman D, Svarc-Gajic J, Fernandez-Gutierrez A, Segura-Carretero A. Rosmarinus officinalis leaves as a natural source of bioactive compounds. Int J Mol Sci 2014; 15: 20585-20606
    CrossrefPubMedGoogle Scholar
  • 35 Bai N, He K, Roller M, Lai CS, Shao X, Pan MH, Ho CT. Flavonoids and phenolic compounds from Rosmarinus officinalis . J Agric Food Chem 2010; 58: 5363-5367
    CrossrefPubMedGoogle Scholar
  • 36 Mena P, Cirlini M, Tassotti M, Herrlinger KA, DallʼAsta C, Del Rio D. Phytochemical Profiling of Flavonoids, Phenolic Acids, Terpenoids, and Volatile Fraction of a Rosemary (Rosmarinus officinalis L.) Extract. Molecules 2016; 21: E1576
    CrossrefPubMedGoogle Scholar
  • 37 Kontogianni VG, Tomic G, Nikolic I, Nerantzaki AA, Sayyad N, Stosic-Grujicic S, Stojanovic I, Gerothanassis IP, Tzakos AG. Phytochemical profile of Rosmarinus officinalis and Salvia officinalis extracts and correlation to their antioxidant and anti-proliferative activity. Food Chem 2013; 136: 120-129
    CrossrefPubMedGoogle Scholar
  • 38 Romo Vaquero M, Yáñez-Gascón MJ, García-Villalba R, Larrosa M, Fromentin E, Ibarra A, Roller M, Tomás-Barberán F, Espín de Gea JC, García-Conesa MT. Inhibition of gastric lipase as a mechanism for body weight and plasma lipids reduction in Zucker rats fed a rosemary extract rich in carnosic acid. PLoS One 2012; 7: e39773
    CrossrefPubMedGoogle Scholar
  • 39 McNab H, Ferreira ESB, Hulme AN, Quye A. Negative ion ESI–MS analysis of natural yellow dye flavonoids–An isotopic labelling study. Int J Mass Spectrom 2009; 284: 57-65
    CrossrefPubMedGoogle Scholar
  • 40 Perez-Fons L, Garzon MT, Micol V. Relationship between the antioxidant capacity and effect of rosemary (Rosmarinus officinalis L.) polyphenols on membrane phospholipid order. J Agric Food Chem 2010; 58: 161-171
    CrossrefPubMedGoogle Scholar
  • 41 Romo Vaquero M, Garcia-Villalba R, Larrosa M, Yanez-Gascon MJ, Fromentin E, Flanagan J, Roller M, Tomas-Barberan FA, Espin JC, Garcia-Conesa MT. Bioavailability of the major bioactive diterpenoids in a rosemary extract: metabolic profile in the intestine, liver, plasma, and brain of Zucker rats. Mol Nutr Food Res 2013; 57: 1834-1846
    CrossrefPubMedGoogle Scholar
  • 42 Bresciani L, Calani L, Cossu M, Mena P, Sayegh M, Ray S, Del Rio D. (Poly)phenolic characterization of three food supplements containing 36 different fruits, vegetables and berries. PharmaNutrition 2015; 3: 11-19
    CrossrefPubMedGoogle Scholar
  • 43 Moharram FA, Marzouk MS, El-Shenawy SM, Gaara AH, El Kady WM. Polyphenolic profile and biological activity of Salvia splendens leaves. J Pharm Pharmacol 2012; 64: 1678-1687
    CrossrefPubMedGoogle Scholar
  • 44 Cuyckens F, Claeys M. Mass spectrometry in the structural analysis of flavonoids. J Mass Spectrom 2004; 39: 1-15
    CrossrefPubMedGoogle Scholar
  • 45 Almela L, Sanchez-Munoz B, Fernandez-Lopez JA, Roca MJ, Rabe V. Liquid chromatograpic-mass spectrometric analysis of phenolics and free radical scavenging activity of rosemary extract from different raw material. J Chromatogr A 2006; 1120: 221-229
    CrossrefPubMedGoogle Scholar