Jentashapir Journal of Health Research

Published by: Kowsar

Effect of the Ethanolic Extract of Salvia officinalis on Ovarian Angiogenesis in Mice at Preimplantation: A Morphological and Molecular Analysis

Nasim Beigi Boroujeni 1 , * and Mohammad Reza Gholami 2
Authors Information
1 Razi Herbal Medicines Research Center, Lorestan University of Medical Sciences, Khorramabad, Iran
2 Deptartment of Anatomical Sciences, Lorestan University of Medical Sciences, Khorramabad, Iran
Article information
  • Jentashapir Journal of Health Research: February 2017, 8 (1); e44386
  • Published Online: February 22, 2017
  • Article Type: Research Article
  • Received: December 26, 2016
  • Accepted: February 22, 2017
  • DOI: 10.5812/jjhr.44386

To Cite: Beigi Boroujeni N, Gholami M R. Effect of the Ethanolic Extract of Salvia officinalis on Ovarian Angiogenesis in Mice at Preimplantation: A Morphological and Molecular Analysis, Jentashapir J Health Res. 2017 ; 8(1):e44386. doi: 10.5812/jjhr.44386.

Copyright © 2017, Ahvaz Jundishapur University of Medical Sciences. This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License ( which permits copy and redistribute the material just in noncommercial usages, provided the original work is properly cited.
1. Background
2. Objectives
3. Methods
4. Results
5. Discussion
  • 1. Zihlif M, Afifi F, Abu-Dahab R, Abdul Majid AM, Somrain H, Saleh MM, et al. The antiangiogenic activities of ethanolic crude extracts of four Salvia species. BMC Complement Altern Med. 2013; 13: 358[DOI][PubMed]
  • 2. Ajonuma LC. Is vascular endothelial growth factor (VEGF) the main mediator in ovarian hyperstimulation syndrome (OHSS)? Med Hypotheses. 2008; 70(6): 1174-8[DOI][PubMed]
  • 3. Gomez R, Simon C, Remohi J, Pellicer A. Vascular endothelial growth factor receptor-2 activation induces vascular permeability in hyperstimulated rats, and this effect is prevented by receptor blockade. Endocrinology. 2002; 143(11): 4339-48[DOI][PubMed]
  • 4. Geva E, Jaffe RB. Role of vascular endothelial growth factor in ovarian physiology and pathology. Fertil Steril. 2000; 74(3): 429-38[PubMed]
  • 5. Ciesla L, Hajnos M, Staszek D, Wojtal L, Kowalska T, Waksmundzka-Hajnos M. Validated binary high-performance thin-layer chromatographic fingerprints of polyphenolics for distinguishing different Salvia species. J Chromatogr Sci. 2010; 48(6): 421-7[PubMed]
  • 6. Schwager J, Richard N, Fowler A, Seifert N, Raederstorff D. Carnosol and Related Substances Modulate Chemokine and Cytokine Production in Macrophages and Chondrocytes. Molecules. 2016; 21(4): 465[DOI][PubMed]
  • 7. Vitale DC, Piazza C, Melilli B, Drago F, Salomone S. Isoflavones: estrogenic activity, biological effect and bioavailability. Eur J Drug Metab Pharmacokinet. 2013; 38(1): 15-25[DOI][PubMed]
  • 8. Padilla-Banks E, Jefferson WN, Newbold RR. Neonatal exposure to the phytoestrogen genistein alters mammary gland growth and developmental programming of hormone receptor levels. Endocrinology. 2006; 147(10): 4871-82[DOI][PubMed]
  • 9. Rahte S, Evans R, Eugster PJ, Marcourt L, Wolfender JL, Kortenkamp A, et al. Salvia officinalis for hot flushes: towards determination of mechanism of activity and active principles. Planta Med. 2013; 79(9): 753-60[DOI][PubMed]
  • 10. Stojanovi JB, Veljkovi VB. Extraction of flavonoids from garden (Salvia officinalis L.) and glutinous (Salvia glutinosa L.) sage by ultrasonic and classical maceration. J Serb Chem Soc. 2007; 72(1): 73-80
  • 11. Denham A, Green J, Hawkey S. What's in the bottle? Prescriptions formulated by medical herbalists in a clinical trial of treatment during the menopause. J Herbal Med. 2011; 1(3): 95-101
  • 12. Limopasmanee W, Chansakaow S, Rojanasthien N, Manorot M, Sangdee C, Teekachunhatean S. Effects of the chinese herbal formulation (liu wei di huang wan) on the pharmacokinetics of isoflavones in postmenopausal women. Bio Res Inter. 2015;
  • 13. Al-Ramahi R, Jaradat N, Adawi D. Use of herbal medicines during pregnancy in a group of Palestinian women. J Ethnopharmacol. 2013; 150(1): 79-84[DOI][PubMed]
  • 14. Monsefi M, Abedian M, Azarbahram Z, Ashraf MJ. Salvia officinalis L. induces alveolar bud growing in adult female rat mammary glands. Avicenna J Phytomed. 2015; 5(6): 560-7[PubMed]
  • 15. Ososki AL, Kennelly EJ. Phytoestrogens: a review of the present state of research. Phytother Res. 2003; 17(8): 845-69[DOI][PubMed]
  • 16. Kayashima T, Matsubara K. Antiangiogenic effect of carnosic acid and carnosol, neuroprotective compounds in rosemary leaves. Biosci Biotechnol Biochem. 2012; 76(1): 115-9[DOI][PubMed]
  • 17. Kim GD, Park YS, Jin YH, Park CS. Production and applications of rosmarinic acid and structurally related compounds. Appl Microbiol Biotechnol. 2015; 99(5): 2083-92[DOI][PubMed]
  • 18. Ried K. Chinese herbal medicine for female infertility: an updated meta-analysis. Complement Ther Med. 2015; 23(1): 116-28[DOI][PubMed]
  • 19. Guo J, Li D, Liu C, Ji X, Li R, Du X. Effects of Chinese herbs combined with in vitro fertilization and embryo transplantation on infertility: a clinical randomized controlled trial. J Tradit Chin Med. 2014; 34(3): 267-73[PubMed]
  • 20. Keshavarz M, Mostafaie A, Mansouri K, Bidmeshkipour A, Motlagh HR, Parvaneh S. In vitro and ex vivo antiangiogenic activity of Salvia officinalis. Phytother Res. 2010; 24(10): 1526-31[DOI][PubMed]
  • 21. Kashyap D, Tuli HS, Sharma AK. Ursolic acid (UA): A metabolite with promising therapeutic potential. Life Sci. 2016; 146: 201-13[DOI][PubMed]
  • 22. Haas J, Ophir L, Barzilay E, Yerushalmi GM, Yung Y, Kedem A, et al. GnRH agonist vs. hCG for triggering of ovulation--differential effects on gene expression in human granulosa cells. PLoS One. 2014; 9(3): 90359[DOI][PubMed]
  • 23. Keshavarz M, Bidmeshkipour A, Mostafaie A, Mansouri K, Mohammadi-Motlagh HR. Anti tumor activity of Salvia officinalis is due to its anti-angiogenic, anti-migratory and anti-proliferative effects. Cell J. 2011; 12(4): 477-82
  • 24. Boroujeni NB, Boroujeni MB, Gholami M, Shafiei A. Ethanolic extract of Salvia officinalis alter vascular endothelial growth factor gene expression and its receptors in the mouse endometrium at preimplantation. Comparative Clin Pathol. 2016; 25(1): 125-9
  • 25. Boroujeni MB, Boroujeni NB, Gholami M. The effect of progesterone treatment after ovarian induction on endometrial VEGF gene expression and its receptors in mice at pre-implantation time. Iran J Basic Med Sci. 2016; 19(3): 252-7[PubMed]
  • 26. Albano SM, Miguel MG. Biological activities of extracts of plants grown in Portugal. Indust Crops Products. 2011; 33(2): 338-43
  • 27. Bauer J, Kuehnl S, Rollinger JM, Scherer O, Northoff H, Stuppner H, et al. Carnosol and carnosic acids from Salvia officinalis inhibit microsomal prostaglandin E2 synthase-1. J Pharmacol Exp Ther. 2012; 342(1): 169-76[DOI][PubMed]
  • 28. Baricevic D, Sosa S, Della Loggia R, Tubaro A, Simonovska B, Krasna A, et al. Topical anti-inflammatory activity of Salvia officinalis L. leaves: the relevance of ursolic acid. J Ethnopharmacol. 2001; 75(2-3): 125-32[PubMed]
  • 29. Tosun A, Khan S, Kim YS, Calin-Sanchez A, Hysenaj X, Carbonell-Barrachina A. Essential oil composition and anti-inflammatory activity of salvia officinalis l (lamiaceae) in murin macrophages. Tropical J Pharmaceutical Res. 2014; 13(6): 937-42
  • 30. Schisterman EF, Gaskins AJ, Whitcomb BW. Effects of low-dose aspirin in in-vitro fertilization. Curr Opin Obstet Gynecol. 2009; 21(3): 275-8[DOI][PubMed]
  • 31. Vardhana PA, Julius MA, Pollak SV, Lustbader EG, Trousdale RK, Lustbader JW. A unique human chorionic gonadotropin antagonist suppresses ovarian hyperstimulation syndrome in rats. Endocrinology. 2009; 150(8): 3807-14[DOI][PubMed]
  • 32. Albert C, Garrido N, Mercader A, Rao CV, Remohi J, Simon C, et al. The role of endothelial cells in the pathogenesis of ovarian hyperstimulation syndrome. Mol Hum Reprod. 2002; 8(5): 409-18[PubMed]
  • 33. Villasante A, Pacheco A, Ruiz A, Pellicer A, Garcia-Velasco JA. Vascular endothelial cadherin regulates vascular permeability: Implications for ovarian hyperstimulation syndrome. J Clin Endocrinol Metab. 2007; 92(1): 314-21[DOI][PubMed]
  • 34. Halicioglu O, Astarcioglu G, Yaprak I, Aydinlioglu H. Toxicity of Salvia officinalis in a newborn and a child: an alarming report. Pediatr Neurol. 2011; 45(4): 259-60[DOI][PubMed]
  • 35. Hazzard TM, Molskness TA, Chaffin CL, Stouffer RL. Vascular endothelial growth factor (VEGF) and angiopoietin regulation by gonadotrophin and steroids in macaque granulosa cells during the peri-ovulatory interval. Mol Hum Reprod. 1999; 5(12): 1115-21[PubMed]
  • 36. Wu L, Zhang Z, Pan X, Wang Z. Expression and contribution of the HIF‑1α/VEGF signaling pathway to luteal development and function in pregnant rats. Mol Med Rep. 2015; 12(5): 7153-9
  • 37. Berisha B, Schams D, Rodler D, Pfaffl MW. Angiogenesis in The Ovary - The Most Important Regulatory Event for Follicle and Corpus Luteum Development and Function in Cow - An Overview. Anat Histol Embryol. 2016; 45(2): 124-30[DOI][PubMed]
Creative Commons License Except where otherwise noted, this work is licensed under Creative Commons Attribution Non Commercial 4.0 International License .

Search Relations:



Create Citiation Alert
via Google Reader

Readers' Comments