Skip to main content
Top
Published in: BMC Complementary Medicine and Therapies 1/2020

Open Access 01-12-2020 | Research article

Protective effect of Tualang honey against cadmium-induced morphological abnormalities and oxidative stress in the ovary of rats

Authors: Siti Suraya Ruslee, Siti Sarah Mohamad Zaid, Ikmal Hisyam Bakrin, Yong Meng Goh, Noordin Mohamed Mustapha

Published in: BMC Complementary Medicine and Therapies | Issue 1/2020

Login to get access

Abstract

Background

To investigate the protective effects of Tualang honey against the toxicity effects induced by cadmium (Cd) on the ovary.

Methods

A total of 32 female Sprague Dawley rats were taken and randomly divided into four groups (n = 8). Throughout the experimental period of 6 weeks, negative control-NC (vehicle deionized water), positive control-CD (Cd at 5 mg/kg), Tualang honey followed by Cd exposure-TH (Tualang honey at 200 mg/kg and Cd at 5 mg/kg) and Tualang honey control-THC (Tualang honey at 200 mg/kg) groups, were administered orally on a daily basis.

Results

Rats exposed to Cd were significantly higher in ovarian weight, number of antral and atretic follicles as compared to the NC group. The disruptive effects of Cd on ovarian follicles were associated with a disruption in gonadotropin hormones and decreases in follicular stimulating hormone (FSH) and luteinizing hormone (LH). Moreover, a significant formation of oxidative stress in ovarian Cd-exposed rats has been proven by increasing the level of lipid peroxidation products (malondialdehyde) and decreasing the levels of enzymatic antioxidant (catalase). Interestingly, a daily supplementation of high antioxidant agents such as Tualang honey in these animals, caused significant improvements in the histological changes. Additionally, less atretic follicles were observed, restoring the normal level of LH and FSH (P < 0.001), and normalizing the ovarian malondialdehyde (P < 0.05) and catalase levels in comparison with CD group (P < 0.05).

Conclusions

Tualang honey has protective effects against Cd-induced ovarian toxicity by reducing morphological abnormalities, restoring the normal levels of gonadotropin hormones and stabilizing equilibrium levels of lipid peroxidation and antioxidant enzyme in ovaries of rats.
Literature
1.
go back to reference Ciarrocca M, Capozzella A, Tomei F, Tomei G, Caciari T. Exposure to cadmium in male urban and rural workers and effects on FSH, LH and testosterone. Chemosphere. 2013;90(7):2077–84.PubMedCrossRef Ciarrocca M, Capozzella A, Tomei F, Tomei G, Caciari T. Exposure to cadmium in male urban and rural workers and effects on FSH, LH and testosterone. Chemosphere. 2013;90(7):2077–84.PubMedCrossRef
2.
go back to reference Mendiola J, Moreno JM, Roca M, Vergara-Juárez N, Martínez-García MJ, García-Sánchez A, et al. Relationships between heavy metal concentrations in three different body fluids and male reproductive parameters: a pilot study. Environ Health. 2011;10(1):6.PubMedPubMedCentralCrossRef Mendiola J, Moreno JM, Roca M, Vergara-Juárez N, Martínez-García MJ, García-Sánchez A, et al. Relationships between heavy metal concentrations in three different body fluids and male reproductive parameters: a pilot study. Environ Health. 2011;10(1):6.PubMedPubMedCentralCrossRef
3.
go back to reference Zeng X, Jin T, Buchet JP, Jiang X, Kong Q, Ye T, et al. Impact of cadmium exposure on male sex hormones: a population-based study in China. Environ Res. 2004;96(3):338–44.PubMedCrossRef Zeng X, Jin T, Buchet JP, Jiang X, Kong Q, Ye T, et al. Impact of cadmium exposure on male sex hormones: a population-based study in China. Environ Res. 2004;96(3):338–44.PubMedCrossRef
5.
go back to reference McElroy JA, Kruse RL, Guthrie J, Gangnon RE, Robertson JD. Cadmium exposure and endometrial cancer risk: a large midwestern U.S. population-based case-control study. PLoS One. 2017;12(7):e0179360.PubMedPubMedCentralCrossRef McElroy JA, Kruse RL, Guthrie J, Gangnon RE, Robertson JD. Cadmium exposure and endometrial cancer risk: a large midwestern U.S. population-based case-control study. PLoS One. 2017;12(7):e0179360.PubMedPubMedCentralCrossRef
6.
go back to reference Bhattacharya MH, Wilson AK, Rajan SS, Jonath M. Biochemical pathways in cadmium toxicity. In: Zalups RK, Koropatnick J, editors. Molecular Biology and Toxicology of Metals. London: Taylor and Francis; 2000. pp. 34–74. Bhattacharya MH, Wilson AK, Rajan SS, Jonath M. Biochemical pathways in cadmium toxicity. In: Zalups RK, Koropatnick J, editors. Molecular Biology and Toxicology of Metals. London: Taylor and Francis; 2000. pp. 34–74.
7.
go back to reference Piasek M, Blanuša M, Kostial K, Laskey JW. Placental cadmium and progesterone concentrations in cigarette smokers. Reprod Toxicol. 2001;15(6):673–81.PubMedCrossRef Piasek M, Blanuša M, Kostial K, Laskey JW. Placental cadmium and progesterone concentrations in cigarette smokers. Reprod Toxicol. 2001;15(6):673–81.PubMedCrossRef
8.
go back to reference Zadorozhnaja TD, Little RE, Mendel NA, Taylor RJ, Presley BJ, Galden BC. Concentrations of arsenic, cadmium, copper, lead, mercury and zinc in human placentas from two cities in Ukraine. J Toxicol Environ Health. 2000;61(4):255–63.CrossRef Zadorozhnaja TD, Little RE, Mendel NA, Taylor RJ, Presley BJ, Galden BC. Concentrations of arsenic, cadmium, copper, lead, mercury and zinc in human placentas from two cities in Ukraine. J Toxicol Environ Health. 2000;61(4):255–63.CrossRef
9.
go back to reference Varga B, Zsolnai B, Paksy K, Náray M, Ungváry GY. Age dependent accumulation of cadmium in the human ovary. Reprod Toxicol. 1993;7(3):225–8.PubMedCrossRef Varga B, Zsolnai B, Paksy K, Náray M, Ungváry GY. Age dependent accumulation of cadmium in the human ovary. Reprod Toxicol. 1993;7(3):225–8.PubMedCrossRef
10.
go back to reference Cuypers A, Plusquin M, Remans T, Jozefczak M, Keunen E, Gielen H, et al. Cadmium stress: an oxidative challenge. BioMetals. 2010;23(5):927–40.PubMedCrossRef Cuypers A, Plusquin M, Remans T, Jozefczak M, Keunen E, Gielen H, et al. Cadmium stress: an oxidative challenge. BioMetals. 2010;23(5):927–40.PubMedCrossRef
11.
go back to reference Nwokocha CR, Nwokocha MI, Aneto I, Obi J, Udekweleze DC, Olatunde B, et al. Comparative analysis on the effect of Lycopersicon esculentum (tomato) in reducing cadmium, mercury and lead accumulation in liver. Food Chem Toxicol. 2012;50(6):2070–3.PubMedCrossRef Nwokocha CR, Nwokocha MI, Aneto I, Obi J, Udekweleze DC, Olatunde B, et al. Comparative analysis on the effect of Lycopersicon esculentum (tomato) in reducing cadmium, mercury and lead accumulation in liver. Food Chem Toxicol. 2012;50(6):2070–3.PubMedCrossRef
12.
go back to reference Olaolu TD. Effect of cadmium on female reproduction and treatment options. Res J Obstet Gynecol. 2018;11(1):41–8.CrossRef Olaolu TD. Effect of cadmium on female reproduction and treatment options. Res J Obstet Gynecol. 2018;11(1):41–8.CrossRef
13.
go back to reference Roopha DP, Padmalatha C. Effect of herbal preparation on heavy metal (cadmium) induced antioxidant system in female Wistar rats. J Med Toxicol. 2012;8(2):101–7.CrossRef Roopha DP, Padmalatha C. Effect of herbal preparation on heavy metal (cadmium) induced antioxidant system in female Wistar rats. J Med Toxicol. 2012;8(2):101–7.CrossRef
15.
go back to reference Ali I, Damdimopoulou PPE, Mäkelä SI, Berglund M, Stenius U, Åkesson A, et al. Estrogen-like effects of cadmium in vivo do not appear to be mediated via the classical estrogen receptor transcriptional pathway. Environ Health Perspect. 2010;118(10):1389–94.PubMedPubMedCentralCrossRef Ali I, Damdimopoulou PPE, Mäkelä SI, Berglund M, Stenius U, Åkesson A, et al. Estrogen-like effects of cadmium in vivo do not appear to be mediated via the classical estrogen receptor transcriptional pathway. Environ Health Perspect. 2010;118(10):1389–94.PubMedPubMedCentralCrossRef
16.
go back to reference Höfer N, Diel P, Wittsiepe J, Wilhelm M, Degen GH. Dose and route dependent hormonal activity of the metalloestrogen cadmium in the rat uterus. Toxicol Lett. 2009;191(2–3):123–31.PubMedCrossRef Höfer N, Diel P, Wittsiepe J, Wilhelm M, Degen GH. Dose and route dependent hormonal activity of the metalloestrogen cadmium in the rat uterus. Toxicol Lett. 2009;191(2–3):123–31.PubMedCrossRef
17.
go back to reference Wang Y, Wang X, Wang Y, Fan R, Qiu C, Zhong S, et al. Effect of cadmium on cellular ultrastructure in mouse ovary. Ultrastruct Pathol. 2015;39(5):324–8.PubMedCrossRef Wang Y, Wang X, Wang Y, Fan R, Qiu C, Zhong S, et al. Effect of cadmium on cellular ultrastructure in mouse ovary. Ultrastruct Pathol. 2015;39(5):324–8.PubMedCrossRef
18.
go back to reference Rafati-Rahimzadeh M, Rafati-Rahimzadeh M, Kazemi S, Moghadamnia A. Cadmium toxicity and treatment: an update. Casp J Intern Med. 2017;8(3):135–45. Rafati-Rahimzadeh M, Rafati-Rahimzadeh M, Kazemi S, Moghadamnia A. Cadmium toxicity and treatment: an update. Casp J Intern Med. 2017;8(3):135–45.
19.
go back to reference Thompson J, Bannigan J. Cadmium: toxic effects on the reproductive system and the embryo. Reprod Toxicol. 2008;25(3):304–15.PubMedCrossRef Thompson J, Bannigan J. Cadmium: toxic effects on the reproductive system and the embryo. Reprod Toxicol. 2008;25(3):304–15.PubMedCrossRef
20.
go back to reference Zaid SSM, Othman S, Kassim NM. Protective role of Ficus deltoidea against BPA-induced impairments of the follicular development, estrous cycle, gonadotropin and sex steroid hormones level of prepubertal rats. J Ovarian Res. 2018;11(1):99.PubMedPubMedCentralCrossRef Zaid SSM, Othman S, Kassim NM. Protective role of Ficus deltoidea against BPA-induced impairments of the follicular development, estrous cycle, gonadotropin and sex steroid hormones level of prepubertal rats. J Ovarian Res. 2018;11(1):99.PubMedPubMedCentralCrossRef
21.
go back to reference Abrahim NN, Abdul-Rahman PS, Aminudin N. The antioxidant activities, cytotoxic properties, and identification of water-soluble compounds of Ficus deltoidea leaves. PeerJ. 2018;6:e5694.PubMedPubMedCentralCrossRef Abrahim NN, Abdul-Rahman PS, Aminudin N. The antioxidant activities, cytotoxic properties, and identification of water-soluble compounds of Ficus deltoidea leaves. PeerJ. 2018;6:e5694.PubMedPubMedCentralCrossRef
22.
go back to reference Khalil MI, Alam N, Moniruzzaman M, Sulaiman SA, Gan SH. Phenolic acid composition and antioxidant properties of Malaysian honeys. J Food Sci. 2011;76(6):C921–8.PubMedCrossRef Khalil MI, Alam N, Moniruzzaman M, Sulaiman SA, Gan SH. Phenolic acid composition and antioxidant properties of Malaysian honeys. J Food Sci. 2011;76(6):C921–8.PubMedCrossRef
23.
go back to reference Mohamed ZBH, Alfarisi HAH. Tualang honey: composition, physiochemical properties and clinical importance. Int Res J Pharm. 2017;8(9):1–5.CrossRef Mohamed ZBH, Alfarisi HAH. Tualang honey: composition, physiochemical properties and clinical importance. Int Res J Pharm. 2017;8(9):1–5.CrossRef
24.
go back to reference Kishore RK, Halim AS, Syazana MSN, Sirajudeen KNS. Tualang honey has higher phenolic content and greater radical scavenging activity compared with other honey sources. Nutr Res. 2011;31(4):322–5.PubMedCrossRef Kishore RK, Halim AS, Syazana MSN, Sirajudeen KNS. Tualang honey has higher phenolic content and greater radical scavenging activity compared with other honey sources. Nutr Res. 2011;31(4):322–5.PubMedCrossRef
25.
go back to reference Shafin N, Othman Z, Zakaria R, Hussain NNH. Tualang honey supplementation reduces blood oxidative stress levels/activities in postmenopausal women. ISRN Oxidative Med. 2014;2014:1–4.CrossRef Shafin N, Othman Z, Zakaria R, Hussain NNH. Tualang honey supplementation reduces blood oxidative stress levels/activities in postmenopausal women. ISRN Oxidative Med. 2014;2014:1–4.CrossRef
26.
go back to reference Zaid SSM, Sulaiman SA, Sirajudeen KNM, Othman NH. The effects of Tualang honey on female reproductive organs, tibia bone and hormonal profile in ovariectomised rats-animal model for menopause. BMC Complement Altern Med. 2010;10:82.PubMedPubMedCentralCrossRef Zaid SSM, Sulaiman SA, Sirajudeen KNM, Othman NH. The effects of Tualang honey on female reproductive organs, tibia bone and hormonal profile in ovariectomised rats-animal model for menopause. BMC Complement Altern Med. 2010;10:82.PubMedPubMedCentralCrossRef
27.
go back to reference Zaid SSM, Othman S, Kassim NM. Potential protective effect of Tualang honey on BPA-induced ovarian toxicity in prepubertal rat. BMC Complement Altern Med. 2014;14:509.PubMedPubMedCentralCrossRef Zaid SSM, Othman S, Kassim NM. Potential protective effect of Tualang honey on BPA-induced ovarian toxicity in prepubertal rat. BMC Complement Altern Med. 2014;14:509.PubMedPubMedCentralCrossRef
28.
go back to reference Zaid SSM, Sulaiman S, Othman N, Soelaiman I, Shuid A, Mohamad N, et al. Protective effects of Tualang honey on bone structure in experimental postmenopausal rats. Clinics. 2012;67(7):779–84.PubMedPubMedCentralCrossRef Zaid SSM, Sulaiman S, Othman N, Soelaiman I, Shuid A, Mohamad N, et al. Protective effects of Tualang honey on bone structure in experimental postmenopausal rats. Clinics. 2012;67(7):779–84.PubMedPubMedCentralCrossRef
29.
go back to reference Zaid SSM, Kassim NM, Othman S. Tualang honey protects against BPA-induced morphological abnormalities and disruption of ERα, ERβ, and C3 mRNA and protein expressions in the uterus of rats. Evid-Based Complement Altern Med. 2015;2015:202874.CrossRef Zaid SSM, Kassim NM, Othman S. Tualang honey protects against BPA-induced morphological abnormalities and disruption of ERα, ERβ, and C3 mRNA and protein expressions in the uterus of rats. Evid-Based Complement Altern Med. 2015;2015:202874.CrossRef
30.
go back to reference Omotayo EO, Gurtu S, Sulaiman SA, Wahab AMS, Sirajudeen KN, Salleh MS. Hypoglycemic and antioxidant effects of honey supplementation in streptozotocin-induced diabetic rats. Int J Vitam Nutr Res. 2010;80(1):74–82.PubMedCrossRef Omotayo EO, Gurtu S, Sulaiman SA, Wahab AMS, Sirajudeen KN, Salleh MS. Hypoglycemic and antioxidant effects of honey supplementation in streptozotocin-induced diabetic rats. Int J Vitam Nutr Res. 2010;80(1):74–82.PubMedCrossRef
31.
go back to reference Auger J, Eustache F, Rouiller-Fabre V, Canivenc-Lavier MC, Livera G. Integrative rodent models for assessing male reproductive toxicity of environmental endocrine active substances. Asian J Androl. 2014;16(1):60.PubMedCrossRef Auger J, Eustache F, Rouiller-Fabre V, Canivenc-Lavier MC, Livera G. Integrative rodent models for assessing male reproductive toxicity of environmental endocrine active substances. Asian J Androl. 2014;16(1):60.PubMedCrossRef
32.
go back to reference Paksy K, Varga B, Lázár P. Effect of cadmium on female fertility, pregnancy and postnatal development in the rat. Acta Physiol Hung. 1996;84(2):119–30.PubMed Paksy K, Varga B, Lázár P. Effect of cadmium on female fertility, pregnancy and postnatal development in the rat. Acta Physiol Hung. 1996;84(2):119–30.PubMed
33.
go back to reference Hatzopoulos S, Petruccelli J, Laurell G, Finesso M, Martini A. Evaluation of anesthesia effects in a rat animal model using otoacoustic emission protocols. Hear Res. 2002;170(1–2):12–21.PubMedCrossRef Hatzopoulos S, Petruccelli J, Laurell G, Finesso M, Martini A. Evaluation of anesthesia effects in a rat animal model using otoacoustic emission protocols. Hear Res. 2002;170(1–2):12–21.PubMedCrossRef
34.
go back to reference Zhuang XL, Fu YC, Xu JJ, Kong XX, Chen ZG, Luo LL. Effects of genistein on ovarian follicular development and ovarian life span in rats. Fitoterapia. 2010;81(8):998–1002.PubMedCrossRef Zhuang XL, Fu YC, Xu JJ, Kong XX, Chen ZG, Luo LL. Effects of genistein on ovarian follicular development and ovarian life span in rats. Fitoterapia. 2010;81(8):998–1002.PubMedCrossRef
35.
go back to reference Nandi A, Yan LJ, Jana CK, Das N. Role of catalase in oxidative stress and age associated degenerative diseases. Oxidative Med Cell Longev. 2019;2019:1–19.CrossRef Nandi A, Yan LJ, Jana CK, Das N. Role of catalase in oxidative stress and age associated degenerative diseases. Oxidative Med Cell Longev. 2019;2019:1–19.CrossRef
36.
go back to reference Saki G, Jasemi M, Sarkaki A, Fathollahi A. Effect of administration of vitamins C and E on fertilization capacity of rats exposed to noise stress. Noise Health. 2013;15:194.PubMedCrossRef Saki G, Jasemi M, Sarkaki A, Fathollahi A. Effect of administration of vitamins C and E on fertilization capacity of rats exposed to noise stress. Noise Health. 2013;15:194.PubMedCrossRef
37.
go back to reference Nadri F, Khavanin A, Mazaheri Z, Khajehnasiri F. The effect of noise stress on adult male rat sperm parameters and the protective effect of hydroalcoholic Cinnamomum verum extract: an experimental study. Iran Red Crescent Med J. 2018;20(12):e69779. Nadri F, Khavanin A, Mazaheri Z, Khajehnasiri F. The effect of noise stress on adult male rat sperm parameters and the protective effect of hydroalcoholic Cinnamomum verum extract: an experimental study. Iran Red Crescent Med J. 2018;20(12):e69779.
38.
go back to reference Hood RD. Developmental and reproductive toxicology: a practical approach. United States of America: CRC Press; 2005.CrossRef Hood RD. Developmental and reproductive toxicology: a practical approach. United States of America: CRC Press; 2005.CrossRef
39.
go back to reference Li Y, Zhang W, Liu J, Wang W, Li H, Zhu J, et al. Prepubertal bisphenol a exposure interferes with ovarian follicle development and its relevant gene expression. Reprod Toxicol. 2014;44:33–40.PubMedCrossRef Li Y, Zhang W, Liu J, Wang W, Li H, Zhu J, et al. Prepubertal bisphenol a exposure interferes with ovarian follicle development and its relevant gene expression. Reprod Toxicol. 2014;44:33–40.PubMedCrossRef
40.
go back to reference Schoeters G, Hond DE, Zuurbier M, Naginiene R, Hazel VDP, Stilianakis N, et al. Cadmium and children: exposure and health effects. Acta Paediatr. 2006;95:50–4.CrossRef Schoeters G, Hond DE, Zuurbier M, Naginiene R, Hazel VDP, Stilianakis N, et al. Cadmium and children: exposure and health effects. Acta Paediatr. 2006;95:50–4.CrossRef
42.
go back to reference Hood RD. Handbook of developmental toxicology. Boca Raton: CRC Press; 1996. p. 790. Hood RD. Handbook of developmental toxicology. Boca Raton: CRC Press; 1996. p. 790.
43.
go back to reference Barański B, Sitarek K. Effect of oral and inhalation exposure to cadmium on the oestrous cycle in rats. Toxicol Lett. 1987;36(3):267–73.PubMedCrossRef Barański B, Sitarek K. Effect of oral and inhalation exposure to cadmium on the oestrous cycle in rats. Toxicol Lett. 1987;36(3):267–73.PubMedCrossRef
44.
go back to reference Nasiadek M, Danilewicz M, Sitarek K, Świątkowska E, Daragó A, Stragierowicz J, et al. The effect of repeated cadmium oral exposure on the level of sex hormones, estrous cyclicity, and endometrium morphometry in female rats. Environ Sci Pollut Res. 2018;25(28):28025–38.CrossRef Nasiadek M, Danilewicz M, Sitarek K, Świątkowska E, Daragó A, Stragierowicz J, et al. The effect of repeated cadmium oral exposure on the level of sex hormones, estrous cyclicity, and endometrium morphometry in female rats. Environ Sci Pollut Res. 2018;25(28):28025–38.CrossRef
45.
go back to reference Pond WG, Walker EF. Effect of dietary Ca and cd level of pregnant rats on reproduction and on dam and progeny tissue mineral concentrations. Exp Biol Med. 1975;148(3):665–8.CrossRef Pond WG, Walker EF. Effect of dietary Ca and cd level of pregnant rats on reproduction and on dam and progeny tissue mineral concentrations. Exp Biol Med. 1975;148(3):665–8.CrossRef
46.
go back to reference Sutou S, Yamamoto K, Sendota H, Sugiyama M. Toxicity, fertility, teratogenicity, and dominant lethal tests in rats administered cadmium subchronically. Ecotoxicol Environ Saf. 1980;4(1):51–6.PubMedCrossRef Sutou S, Yamamoto K, Sendota H, Sugiyama M. Toxicity, fertility, teratogenicity, and dominant lethal tests in rats administered cadmium subchronically. Ecotoxicol Environ Saf. 1980;4(1):51–6.PubMedCrossRef
47.
go back to reference Sajjad S, Malik H, Farooq U, Rashid F, Nasim H, Tariq S, et al. Cadmium chloride toxicity revisited: effect on certain andrological, endocrinological and biochemical parameters of adult male rabbits. Physiol Res. 2014;63:8. Sajjad S, Malik H, Farooq U, Rashid F, Nasim H, Tariq S, et al. Cadmium chloride toxicity revisited: effect on certain andrological, endocrinological and biochemical parameters of adult male rabbits. Physiol Res. 2014;63:8.
48.
go back to reference Waisberg M, Joseph P, Hale B, Beyersmann D. Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology. 2003;192(2–3):95–117.PubMedCrossRef Waisberg M, Joseph P, Hale B, Beyersmann D. Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology. 2003;192(2–3):95–117.PubMedCrossRef
49.
go back to reference Jamakala O, Rani U. Amelioration effect of zinc and iron supplementation on selected oxidative stress enzymes in liver and kidney of cadmium-treated male albino rat. Toxicol Int. 2015;22(1):1.PubMedPubMedCentralCrossRef Jamakala O, Rani U. Amelioration effect of zinc and iron supplementation on selected oxidative stress enzymes in liver and kidney of cadmium-treated male albino rat. Toxicol Int. 2015;22(1):1.PubMedPubMedCentralCrossRef
50.
go back to reference Monsefi M, Fereydouni B. The effects of cadmium pollution on female rat reproductive system. J Infertil Reprod Biol. 2013;1:1–6. Monsefi M, Fereydouni B. The effects of cadmium pollution on female rat reproductive system. J Infertil Reprod Biol. 2013;1:1–6.
51.
go back to reference Liu J, Huang H, Zhang W, Li H. Cadmium-induced increase in uterine wet weight and its mechanism. Birth Defects Res B Dev Reprod Toxicol. 2010;89(2010):43–9.PubMed Liu J, Huang H, Zhang W, Li H. Cadmium-induced increase in uterine wet weight and its mechanism. Birth Defects Res B Dev Reprod Toxicol. 2010;89(2010):43–9.PubMed
52.
go back to reference Fechner P, Damdimopoulou P, Gauglitz G. Biosensors paving the way to understanding the interaction between cadmium and the estrogen receptor alpha. PLoS One. 2011;6(8):e23048.PubMedPubMedCentralCrossRef Fechner P, Damdimopoulou P, Gauglitz G. Biosensors paving the way to understanding the interaction between cadmium and the estrogen receptor alpha. PLoS One. 2011;6(8):e23048.PubMedPubMedCentralCrossRef
53.
go back to reference Iavicoli I, Fontana L, Bergamaschi A. The effects of metals as endocrine disruptors. J Toxicol Environ Health B Crit Rev. 2009;12(3):206–23.PubMedCrossRef Iavicoli I, Fontana L, Bergamaschi A. The effects of metals as endocrine disruptors. J Toxicol Environ Health B Crit Rev. 2009;12(3):206–23.PubMedCrossRef
54.
go back to reference Kluxen FM, Höfer N, Kretzschmar G, Degen GH, Diel P. Cadmium modulates expression of aryl hydrocarbon receptor-associated genes in rat uterus by interaction with the estrogen receptor. Arch Toxicol. 2012;86(4):591–601.PubMedCrossRef Kluxen FM, Höfer N, Kretzschmar G, Degen GH, Diel P. Cadmium modulates expression of aryl hydrocarbon receptor-associated genes in rat uterus by interaction with the estrogen receptor. Arch Toxicol. 2012;86(4):591–601.PubMedCrossRef
55.
go back to reference Stoica A, Katzenellenbogen BS, Martin MB. Activation of estrogen receptor-α by the heavy metal cadmium. Mol Endocrinol. 2000;14(4):545–53.PubMed Stoica A, Katzenellenbogen BS, Martin MB. Activation of estrogen receptor-α by the heavy metal cadmium. Mol Endocrinol. 2000;14(4):545–53.PubMed
56.
go back to reference Calderoni AM, Biaggio V, Acosta M, Oliveros L, Mohamed F, Giménez MS. Cadmium exposure modifies lactotrophs activity associated to genomic and morphological changes in rat pituitary anterior lobe. BioMetals. 2010;23(1):135–43.PubMedCrossRef Calderoni AM, Biaggio V, Acosta M, Oliveros L, Mohamed F, Giménez MS. Cadmium exposure modifies lactotrophs activity associated to genomic and morphological changes in rat pituitary anterior lobe. BioMetals. 2010;23(1):135–43.PubMedCrossRef
57.
go back to reference Jiménez-Ortega V, Barquilla CP, Fernández-Mateos P, Cardinali DP, Esquifino AI. Cadmium as an endocrine disruptor: correlation with anterior pituitary redox and circadian clock mechanisms and prevention by melatonin. Free Radic Biol Med. 2012;53(12):2287–97.PubMedCrossRef Jiménez-Ortega V, Barquilla CP, Fernández-Mateos P, Cardinali DP, Esquifino AI. Cadmium as an endocrine disruptor: correlation with anterior pituitary redox and circadian clock mechanisms and prevention by melatonin. Free Radic Biol Med. 2012;53(12):2287–97.PubMedCrossRef
58.
go back to reference Lafuente A, Esquifino AI. Cadmium effects on hypothalamic activity and pituitary hormone secretion in the male. Toxicol Lett. 1999;110(3):209–18.PubMedCrossRef Lafuente A, Esquifino AI. Cadmium effects on hypothalamic activity and pituitary hormone secretion in the male. Toxicol Lett. 1999;110(3):209–18.PubMedCrossRef
59.
go back to reference Miler EA, Nudler SI, Quinteros FA, Cabilla JP, Ronchetti SA, Duvilanski BH. Cadmium induced-oxidative stress in pituitary gland is reversed by removing the contamination source. Hum Exp Toxicol. 2010;29(10):873–80.PubMedCrossRef Miler EA, Nudler SI, Quinteros FA, Cabilla JP, Ronchetti SA, Duvilanski BH. Cadmium induced-oxidative stress in pituitary gland is reversed by removing the contamination source. Hum Exp Toxicol. 2010;29(10):873–80.PubMedCrossRef
60.
go back to reference Kollmer WE. Uptake and retention of cadmium-109 in the pituitary, the adrenals and the thyroid of the laboratory rat. Int J Appl Radiat Isot. 1980;31(10):607–9.PubMedCrossRef Kollmer WE. Uptake and retention of cadmium-109 in the pituitary, the adrenals and the thyroid of the laboratory rat. Int J Appl Radiat Isot. 1980;31(10):607–9.PubMedCrossRef
61.
go back to reference Pollack AZ, Ranasinghe S, Sjaarda LA, Mumford SL. Cadmium and reproductive health in women: a systematic review of the epidemiologic evidence. Curr Environ Health Rep. 2014;1(2):172–84.PubMedPubMedCentralCrossRef Pollack AZ, Ranasinghe S, Sjaarda LA, Mumford SL. Cadmium and reproductive health in women: a systematic review of the epidemiologic evidence. Curr Environ Health Rep. 2014;1(2):172–84.PubMedPubMedCentralCrossRef
62.
go back to reference Saksena SK, Salmonsen R. Effects of cadmium chloride on ovulation and on induction of sterility in the female golden hamster. Biol Reprod. 1983;29(1):249–56.PubMedCrossRef Saksena SK, Salmonsen R. Effects of cadmium chloride on ovulation and on induction of sterility in the female golden hamster. Biol Reprod. 1983;29(1):249–56.PubMedCrossRef
63.
go back to reference Panche AN, Diwan AD, Chandra SR. Flavonoids: an overview. J Nutr Sci. 2016;5(47):1–15. Panche AN, Diwan AD, Chandra SR. Flavonoids: an overview. J Nutr Sci. 2016;5(47):1–15.
64.
go back to reference Cao Y, Zhuang M, Yang Y, Xie S, Cui J, Cao L, et al. Preliminary study of Quercetin affecting the hypothalamic-pituitary-gonadal Axis on rat endometriosis model. Evid Based Complement Alternat Med. 2014;2014:1–12. Cao Y, Zhuang M, Yang Y, Xie S, Cui J, Cao L, et al. Preliminary study of Quercetin affecting the hypothalamic-pituitary-gonadal Axis on rat endometriosis model. Evid Based Complement Alternat Med. 2014;2014:1–12.
65.
go back to reference Resende FA, de Oliveira APS, de Camargo MS, Vilegas W, Varanda EA. Evaluation of Estrogenic Potential of Flavonoids Using a Recombinant Yeast Strain and MCF7/BUS Cell Proliferation Assay. Jeong J, editor. PLoS ONE. 2013;8(10):e74881.PubMedPubMedCentralCrossRef Resende FA, de Oliveira APS, de Camargo MS, Vilegas W, Varanda EA. Evaluation of Estrogenic Potential of Flavonoids Using a Recombinant Yeast Strain and MCF7/BUS Cell Proliferation Assay. Jeong J, editor. PLoS ONE. 2013;8(10):e74881.PubMedPubMedCentralCrossRef
66.
go back to reference Hassoun E. Cadmium-induced production of superoxide anion and nitric oxide, DNA single strand breaks and lactate dehydrogenase leakage in J774A.1 cell cultures. Toxicology. 1996;112(3):219–26.PubMedCrossRef Hassoun E. Cadmium-induced production of superoxide anion and nitric oxide, DNA single strand breaks and lactate dehydrogenase leakage in J774A.1 cell cultures. Toxicology. 1996;112(3):219–26.PubMedCrossRef
67.
go back to reference Liu F, Jan KY. DNA damage in arsenite- and cadmium-treated bovine aortic endothelial cells. Free Radic Biol Med. 2000;28(1):55–63.PubMedCrossRef Liu F, Jan KY. DNA damage in arsenite- and cadmium-treated bovine aortic endothelial cells. Free Radic Biol Med. 2000;28(1):55–63.PubMedCrossRef
68.
go back to reference Stohs SJ, Bagchi D, Hassoun E, Bagchi M. Oxidative mechanisms in the toxicity of chromium and cadmium ions. J Environ Pathol Toxicol Oncol. 2000;19(3):201–13.PubMed Stohs SJ, Bagchi D, Hassoun E, Bagchi M. Oxidative mechanisms in the toxicity of chromium and cadmium ions. J Environ Pathol Toxicol Oncol. 2000;19(3):201–13.PubMed
69.
go back to reference Badisa VLD, Latinwo LM, Odewumi CO, Ikediobi CO, Badisa RB, Ayuk-Takem LT, et al. Mechanism of DNA damage by cadmium and interplay of antioxidant enzymes and agents. Environ Toxicol. 2007;22(2):144–51.PubMedCrossRef Badisa VLD, Latinwo LM, Odewumi CO, Ikediobi CO, Badisa RB, Ayuk-Takem LT, et al. Mechanism of DNA damage by cadmium and interplay of antioxidant enzymes and agents. Environ Toxicol. 2007;22(2):144–51.PubMedCrossRef
70.
go back to reference Ciani F, Cocchia N, D’Angelo D, Tafuri S. Influence of ROS on ovarian functions. New Discov Embryol. 2015;3:1–34. Ciani F, Cocchia N, D’Angelo D, Tafuri S. Influence of ROS on ovarian functions. New Discov Embryol. 2015;3:1–34.
71.
go back to reference Ighodaro OM, Akinloye OA. First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): their fundamental role in the entire antioxidant defence grid. Alex J Med. 2018;54(4):287–93.CrossRef Ighodaro OM, Akinloye OA. First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): their fundamental role in the entire antioxidant defence grid. Alex J Med. 2018;54(4):287–93.CrossRef
72.
go back to reference Kohen R, Nyska A. Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicol Pathol. 2002;30(6):620–50.PubMedCrossRef Kohen R, Nyska A. Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicol Pathol. 2002;30(6):620–50.PubMedCrossRef
73.
go back to reference Ahmed S, Sulaiman SA, Baig AA, Ibrahim M, Liaqat S, Fatima S, et al. Honey as a potential natural antioxidant medicine: an insight into its molecular mechanisms of action. Oxidative Med Cell Longev. 2018;2018:1–19. Ahmed S, Sulaiman SA, Baig AA, Ibrahim M, Liaqat S, Fatima S, et al. Honey as a potential natural antioxidant medicine: an insight into its molecular mechanisms of action. Oxidative Med Cell Longev. 2018;2018:1–19.
74.
go back to reference Rice-Evans C, Miller N, Paganga G. Antioxidant properties of phenolic compounds. Trends Plant Sci. 1997;2(4):152–9.CrossRef Rice-Evans C, Miller N, Paganga G. Antioxidant properties of phenolic compounds. Trends Plant Sci. 1997;2(4):152–9.CrossRef
75.
go back to reference Silva FAM, Borges F, Guimarães C, Lima JLFC, Matos C, Reis S. Phenolic acids and derivatives: studies on the relationship among structure, radical scavenging activity, and physicochemical parameters. J Agric Food Chem. 2000;48(6):2122–6.PubMedCrossRef Silva FAM, Borges F, Guimarães C, Lima JLFC, Matos C, Reis S. Phenolic acids and derivatives: studies on the relationship among structure, radical scavenging activity, and physicochemical parameters. J Agric Food Chem. 2000;48(6):2122–6.PubMedCrossRef
76.
go back to reference Ryan MJ, Dudash HJ, Docherty M, Geronilla KB, Baker BA, Haff GG, et al. Vitamin E and C supplementation reduces oxidative stress, improves antioxidant enzymes and positive muscle work in chronically loaded muscles of aged rats. Exp Gerontol. 2010;45(11):882–95.PubMedPubMedCentralCrossRef Ryan MJ, Dudash HJ, Docherty M, Geronilla KB, Baker BA, Haff GG, et al. Vitamin E and C supplementation reduces oxidative stress, improves antioxidant enzymes and positive muscle work in chronically loaded muscles of aged rats. Exp Gerontol. 2010;45(11):882–95.PubMedPubMedCentralCrossRef
Metadata
Title
Protective effect of Tualang honey against cadmium-induced morphological abnormalities and oxidative stress in the ovary of rats
Authors
Siti Suraya Ruslee
Siti Sarah Mohamad Zaid
Ikmal Hisyam Bakrin
Yong Meng Goh
Noordin Mohamed Mustapha
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2020
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/s12906-020-02960-1

Other articles of this Issue 1/2020

BMC Complementary Medicine and Therapies 1/2020 Go to the issue