Superoxide Dismutase Expression in the Ovaries of Periodontitis Animal Models Induced by Porphyromonas gingivalis and Treated with Cassava Leaves Extract


  • Agustin Wulan Suci-Dharmayanti Biomedical Department, Faculty of Dentistry, Universitas Jember
  • Ajeng Nurwahyuningtyas Anjani Faculty of Dentistry, Universitas Jember
  • Ari Tri Wanodyo Handayani Dental Public Health Department, Faculty of Dentistry, Universitas Jember
  • Zahreni Hamzah Biomedical Department, Faculty of Dentistry, Universitas Jember
  • Zahara Meilawaty Biomedical Department, Faculty of Dentistry, Universitas Jember
  • Masniari Novita Biomedical Department, Faculty of Dentistry, Universitas Jember
  • Mei Syafriadi Biomedical Department, Faculty of Dentistry, Universitas Jember
  • Amandia Dewi Permana Shita Biomedical Department, Faculty of Dentistry, Universitas Jember



The ovaries represent the female reproductive organs that determine the women's fertility status and their systemic and oral health, correlating to sex steroid hormone alteration. This study aimed to investigate the effect of cassava leaves extract treatment to SOD expression in the animal model-ovaries after Porphyromonas gingivalis injection. 15 female Sprague Dawley rats were used and divided into five groups: (1) control without cassava leaves extract treatment (C); (2) P. gingivalis without cassava leaves extract treatment (T1); (3) P. gingivalis and cassava leaves extract (T2); (4) P. gingivalis and vitamin C (T3); and (5) P. gingivalis and metronidazole (T4). Animal were euthanised at day seven after the initial treatment to collect ovaries. The ovaries sections were immunohistochemically stained to quantify SOD expression using light microscope while the Image J software was used to quantify the SOD expression. The results showed that all of the follicle types had the same intensity of SOD expression. Most of the follicles exhibited low intensity of SOD expression, except for atretic follicles. In conclusion, P. gingivalis and cassava leaves extract influenced SOD expression in the ovaries of animal models, which increased the SOD expression.


Download data is not yet available.


Ramadhani SA, Supriatna I, Karja NW, Winarto A. Pengendalian folikulogenesis ovarium dengan pemberian ekstrak biji kapas. Jurnal Sain Veteriner 2017; 35(1):71-80.

Sun H, Gong TT, Jiang YT, Zhang S, Zhao YH, Wu QJ. Global, regional, and national prevalence and disability-adjusted life-years for infertility in 195 countries and territories, 1990–2017: results from a global burden of disease study, 2017. Aging (Albany NY). 2019; 11(23):10952.

Dharmayanti AW, Kusumawardani B. Deoxypyridinoline and mineral levels in gingival crevicular fluid as disorder indicators of menopausal women with periodontal disease. Dental Journal (Majalah Kedokteran Gigi). 2017; 50(3):131-7.

Dharmayanti AW, Suhartini S, Kusumawardani B. Status kesehatan rongga mulut wanita suku osing. Medica Hospitalia: Journal of Clinical Medicine. 2019; 6(2):71-9.

Trenti A, Tedesco S, Boscaro C, Trevisi L, Bolego C, Cignarella A. Estrogen, angiogenesis, immunity and cell metabolism: solving the puzzle. Int J Mol Sci. 2018; 19(3):859.

Vieira AT, Castelo PM, Ribeiro DA, Ferreira CM. Influence of oral and gut microbiota in the health of menopausal women. Front Microbiol. 2017; 8:1884.

Udagawa S, Katagiri S, Maekawa S, Takeuchi Y, Komazaki R, Ohtsu A, Sasaki N, Shiba T, Watanabe K, Ishihara K, Sato N. Effect of Porphyromonas gingivalis infection in the placenta and umbilical cord in pregnant mice with low birth weight. Acta Odontol Scand. 2018; 76(6):433-41.

Machado V, Escalda C, Proença L, Mendes JJ, Botelho J. Is there a bidirectional association between polycystic ovarian syndrome and periodontitis? A systematic review and meta-analysis. J Clin Med. 2020; 9(6):1961.

Penoni DC, Vettore MV, Torres SR, Farias ML, Leão AT. An investigation of the bidirectional link between osteoporosis and periodontitis. Arch Osteoporos. 2019; 14(1):94.

Bellanti F, Matteo M, Rollo T, De Rosario F, Greco P, Vendemiale G, Serviddio G. Sex hormones modulate circulating antioxidant enzymes: impact of estrogen therapy. Redox Biol. 2013; 1(1):340-6.

Bullon P, Cordero MD, Quiles JL, Morillo JM, del Carmen Ramirez-Tortosa M, Battino M. Mitochondrial dysfunction promoted by Porphyromonas gingivalis lipopolysaccharide as a possible link between cardiovascular disease and periodontitis. Free Radic Biol Med. 2011; 50(10):1336-43.

Rao PS, Kalva S, Yerramilli A, Mamidi S. Free radicals and tissue damage: Role of antioxidants. Free Radicals and Antioxidants. 2011; 1(4):2-7.

Onopiuk B, Onopiuk P, Dąbrowska Z, Dąbrowska E, Pietruska M, & Car H. Effect of metronidazole on the oxidoreductive processes in the submandibular and parotid glands in experimental research. Oxid Med Cell Longev. 2018; 2018:1-6.

Meilawaty Z. Efek ekstrak daun singkong (Manihot utilissima) terhadap ekspresi COX-2 pada monosit yang dipapar LPS E. coli (The effect of Manihot utilissima extracts on COX-2 expression of monocytes induced by LPS E. coli). Dental Journal (Majalah Kedokteran Gigi). 2013; 46(4):196-201.

Meilawaty Z, Shita AD, Kuncaraningtyas PL, Dharmayanti AW, Hamzah Z. Potensi ekstrak daun singkong (Manihot esculenta Crantz) terhadap ekspresi MMP-8 fibroblas gingiva pada model tikus dengan disfungsi ovarium dan periodontitis Potential of cassava (Manihot esculenta Crantz) leaf extract on the MMP-8 expression of gingival fibroblast in rats model with ovarian dysfunction and periodontitis. Jurnal Kedokteran Gigi Universitas Padjadjaran. 2020; 32(2):105-12.

Varghese F, Bukhari AB, Malhotra R, De A. IHC Profiler: an open source plugin for the quantitative evaluation and automated scoring of immunohistochemistry images of human tissue samples. PloS One. 2014; 9(5):e96801.

Devine PJ, Perreault SD, Luderer U. Roles of reactive oxygen species and antioxidants in ovarian toxicity. Biol Reprod. 2012; 86(2):27-1.

Bhardwaj JK, Sharma RK, Saraf P. Alterations in phosphatases and antioxidant enzymes’activity in follicular fluid and granulosa cells during follicular atresia in goat (Capra hircus) ovary. J Adv Zool. 2017; 38(2):154-63.

Wang X, Li C, Wang Y, Li L, Han Z, Wang G. UFL1 Alleviates LPS-Induced Apoptosis by Regulating the NF-κB Signaling Pathway in Bovine Ovarian Granulosa Cells. Biomolecules. 2020; 10(2):260.

Da Kyung Yoo SH. Effect of lipopolysaccharide (LPS) exposure on the reproductive organs of immature female rats. Development & Reproduction. 2016; 20(2):113.

Magata F. Lipopolysaccharide-induced mechanisms of ovarian dysfunction in cows with uterine inflammatory diseases. J Reprod Dev. 2020; 66(4):311-317.

Baerwald AR, Adams GP, Pierson RA. Ovarian antral folliculogenesis during the human menstrual cycle: a review. Hum Reprod Update. 2012; 18(1):73-91.

Matsuda F, Inoue N, Manabe N, Ohkura S. Follicular growth and atresia in mammalian ovaries: regulation by survival and death of granulosa cells. J Reprod Dev. 2012; 58(1):44-50.

Combelles CM, Holick EA, Paolella LJ, Walker DC, Wu Q. Profiling of superoxide dismutase isoenzymes in compartments of the developing bovine antral follicles. Reprod. 2010; 139(5):871-81.

Zalukhu ML, Phyma AR, Pinzon RT. Proses Menua, Stres Oksidatif, dan Peran Anti Oksidan. Cermin Dunia Kedokteran. 2016; 43(10):733-6.

Zeinalivand S, Hayati Roudbari N, Parivar K. Follicular growth and atresia and morphometric alteration of uterine tissue following letrozole administration in mature NMRI mice. Int J Basic Appl Med Sci. 2019; 5(2):103-10.

Procházková D, Boušová I, Wilhelmová N. Antioxidant and prooxidant properties of flavonoids. Fitoterapia. 2011; 82(4):513-523.

Dharmayanti AW, Dubey R, Dubey NK, Deng WP. Implant surface modification strategies through antibacterial and bioactive components. In Biopolymer-Based Formulations 2020 (pp. 647-673). Elsevier.

Louis XL, Thandapilly SJ, Kalt W, Vinqvist-Tymchuk M, Aloud BM, Raj P, Yu L, Le H, Netticadan T. Blueberry polyphenols prevent cardiomyocyte death by preventing calpain activation and oxidative stress. Food Funct. 2014; 5(8):1785-94.

Sadi G, Yılmaz Ö, Güray T. Effect of vitamin C and lipoic acid on streptozotocin-induced diabetes gene expression: mRNA and protein expressions of Cu–Zn SOD and catalase. Mol Cellular Biochem. 2008; 309(1-2):109-16.

Graziano TS, Closs P, Poppi T, Franco GC, Cortelli JR, Groppo FC, Cogo K. Catecholamines promote the expression of virulence and oxidative stress genes in P orphyromonas gingivalis. J Periodontal Res. 2014; 49(5):660-9.






Original/Research Article