Skip to main content
SpringerLink
Log in

Nonylphenol Exposure-Induced Oocyte Quality Deterioration Could be Reversed by Boric Acid Supplementation in Rats

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

In this study, we reported boric acid’s protective effects on the quality of nonylphenol (NP)-exposed oocytes. Female rats were classified into 4 groups: control, boric acid, NP, and NP+boric acid. Histopathological studies and immunohistochemical analysis of anti-müllerian hormone (AMH), mechanistic target of rapamycin (mTOR), Sirtuin1 (SIRT1), stem cell factor (SCF) studies were done. The comet assay technique was utilized for DNA damage. The ELISA method was used to determine the concentrations of oxidative stress indicators (SOD, CAT, and MDA), ovarian hormone (INH-B), and inflammation indicators (IL-6 and TNF-α). Boric acid significantly reduced the histopathological alterations and nearly preserved the ovarian reserve. With the restoration of AMH and SCF, boric acid significantly improved the ovarian injury. It downregulated SIRT1 and upregulated the mTOR signaling pathway. It provided DNA damage protection. Ovarian SOD, CAT levels were decreased by boric acid. Boric acid co-administration significantly reduced NP's MDA, IL-6, and TNF-activities. This results imply that boric acid has a protective role in ovarian tissue against NP-mediated infertility.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Adeogun AO, Ibor OR, Adeduntan SD et al (2016) Intersex and alter- ations in reproductive development of a cichlid, Tilapia guineensis, from a municipal domestic water supply lake (Eleyele) in Southwestern Nigeria. Sci Total Environ 541:372–382. https://doi.org/10.1016/j.scitotenv.2015.09.061

    Article  CAS  PubMed  Google Scholar 

  2. Bahamonde PA, McMaster ME, Servos MR et al (2015) Molecular pathways associated with the intersex condition in rainbow darter (Etheostoma caeruleum) following exposures to municipal wastewater in the Grand River basin, ON, Canada. Part B Aquat Toxicol 159:302–316. https://doi.org/10.1016/j.aquatox.2014.11.022

    Article  CAS  PubMed  Google Scholar 

  3. Wielogorska E, Elliott CT, Danaher M et al (2015) Endocrine disruptor activity of multiple environmental food chain contaminants. Toxicol In Vitro 29:211–220. https://doi.org/10.1016/j.tiv.2014.10.014

    Article  CAS  PubMed  Google Scholar 

  4. Nappi F, Barrea L, Di Somma C et al (2016) Endocrine aspects of environmental "obesogen" pollutants. Int J Environ Res Public Health 13:765. https://doi.org/10.3390/ijerph13080765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Jie X, JianMei L, Zheng F et al (2013) Neurotoxic effects of nonylphenol: a review. Wien Klin Wochenschr 125(3):61–70. https://doi.org/10.1007/s00508-012-0221-2

    Article  CAS  PubMed  Google Scholar 

  6. Zhao Y, Ye L, Zhang XX (2018) Emerging pollutants-Part I: occurrence, fate and transport. Water Environ Res 90:1301–1322. https://doi.org/10.2175/106143018X15289915807236

    Article  CAS  PubMed  Google Scholar 

  7. Shalaby KA, Saleh EM (2011) Ameliorative effect of honey bee propolis on the nonylphenol induced-reproductive toxicity in male Albino rats. Aus J Basic Appl Sci 5(11):918–927

    CAS  Google Scholar 

  8. Yadetie F, Arukwe A, Goksoyr A et al (1999) Induction of hepatic estrogen receptor in juvenile Atlantic salmon in vivo by the environmental estrogen, 4- nonylphenol. Sci Total Environ 233:201–210. https://doi.org/10.1016/S0048-9697(99)00226-0

    Article  CAS  PubMed  Google Scholar 

  9. Qian H, Pan X, Shi S et al (2011) Effect of nonylphenol on response of physiology and photosynthesis-related gene transcription of Chlorella vulgaris. Environ Monit Assess 182(1–4):61–69. https://doi.org/10.1007/s10661-010-1858-9

    Article  CAS  PubMed  Google Scholar 

  10. Bragadin M, Perin G, Iero A et al (1999) An in vitro study on the toxic effects of nonylphenols (NP) in mitochondria. Chemosphere 38:1997–2001. https://doi.org/10.1016/S0045-6535(98)00412-3

    Article  CAS  PubMed  Google Scholar 

  11. Uluisik I, Karakaya HC, Koc A (2018) The importance of boron in biological systems. J Trace Elem Med Biol 45:156–162. https://doi.org/10.1016/j.jtemb.2017.10.008

    Article  CAS  PubMed  Google Scholar 

  12. Sogut I, Oglakci A, Kartkaya K et al (2015) Effect of boric acid on oxidative stress in rats with fetal alcohol syndrome. Exp Ther Med 9(3):1023–1027. https://doi.org/10.3892/etm.2014.2164

    Article  CAS  PubMed  Google Scholar 

  13. Fail PA, Chapi RE, Price CJ et al (1998) General, reproductive, developmental, and endocrine toxicity of boronated compounds. Reprod Toxicol 12:1–18. https://doi.org/10.1016/S0890-6238(97)00095-6

    Article  CAS  PubMed  Google Scholar 

  14. Mehri A (2020) Trace elements in human nutrition (ii)–an update. Int J Prev Med 11(1):2. https://doi.org/10.4103/ijpvm.IJPVM_48_19

    Article  PubMed  PubMed Central  Google Scholar 

  15. Nielsen FH, Eckhert CD (2020) Boron. Adv Nutr 11(2):461–462

    Article  PubMed  Google Scholar 

  16. Ataizi ZS, Ozkoc M, Kanbak G et al (2021) Evaluation of the neuroprotective role of boric acid in preventing traumatic brain injury-mediated oxidative stress. Turk Neurosurg 31(4):493–499. https://doi.org/10.5137/1019-5149.Jtn.25692-18.4

    Article  Google Scholar 

  17. Murray FJ (1998) A comparative review of the pharmacokinetics of boric acid in rodents and humans. Biol Trace Elem Res 66:331–341. https://doi.org/10.1007/BF02783146

    Article  CAS  PubMed  Google Scholar 

  18. Hacioglu C, Kar F, Kacar S et al (2020) High concentrations of boric acid trigger concentration-dependent oxidative stress, apoptotic pathways and morphological alterations in DU-145 human prostate cancer cell line. Biol Trace Elem Res 193(2):400–409. https://doi.org/10.1007/s12011-019-01739-x

    Article  CAS  PubMed  Google Scholar 

  19. Abdelnour SA, Abd El-Hack ME, Swelum AA et al (2018) The vital roles of boron in animal health and production: A comprehensive review. J Trace Elem Med Biol 50:296–304. https://doi.org/10.1016/j.jtemb.2018.07.018

    Article  CAS  PubMed  Google Scholar 

  20. Yamada KE, Eckhert CD (2019) Boric Acid Activation of eIF2alpha and Nrf2 Is PERK dependent: A mechanism that explains how boron prevents DNA damage and enhances antioxidant status. Biol Trace Elem Res 188:2–10. https://doi.org/10.1007/s12011-018-1498-4

    Article  CAS  PubMed  Google Scholar 

  21. Çolak S, Koç K, Yıldırım S et al (2022) Effects of boric acid on ovarian tissue damage caused by experimental ischemia/reperfusion. BiotechHistochem 97(6):415–422. https://doi.org/10.1080/10520295.2021.2012823

    Article  CAS  Google Scholar 

  22. Karimkhani H, Özkoç M, Shojaolsadati P et al (2021) Protective Effect of Boric Acid and Omega-3 on Myocardial Infarction in an Experimental Rat Model. Biol Trace Elem Res 199:2612–2620. https://doi.org/10.1007/s12011-020-02360-z

    Article  CAS  PubMed  Google Scholar 

  23. Goktepe O, Balcioglu E, Baran M et al (2022) Protective effects of melatonin on female rat ovary treated with nonylphenol. Biotech Histochem 98(1):13–19. https://doi.org/10.1080/10520295.2022.2075566

    Article  CAS  PubMed  Google Scholar 

  24. Suna PA, Cengiz O, Ceyhan A et al (2021) The protective role of curcumin against toxic effect of nonylphenol on bone development. Hum Exp Toxicol 40(12):63–76

    Article  Google Scholar 

  25. Taskin MI, Yay A, Adali E et al (2015) Protective effects of sildenafil citrate administration on cisplatin-induced ovarian damage in rats. Gynecol Endocrinol 31(4):272–277. https://doi.org/10.3109/09513590.2014.984679

    Article  CAS  PubMed  Google Scholar 

  26. Oz Gergin O, Bayram A, Gergin IS et al (2019) Comparison of myotoxic effects of levobupivacaine, bupivacaine and ropivacaine: apoptotic activity and acute effect on pro-inflammatory cytokines. Biotech Histochem 94(4):252–260. https://doi.org/10.1080/10520295.2018.1548711

    Article  CAS  PubMed  Google Scholar 

  27. Baran M, Yay A, Onder GO et al (2022) Hepatotoxicity and renal toxicity induced by radiation and the protective effect of quercetin in male albino rats. Int J Radiat Biol 98(9):1473–1483. https://doi.org/10.1080/09553002.2022.2033339

    Article  CAS  PubMed  Google Scholar 

  28. Ernst O, Zor T (2012) Linearization of the Bradford Protein Assay. J Vis Exp 38:1–7

    Google Scholar 

  29. Yener NA, Sinanoglu O, Ilter E et al (2013) Effects of spirulina on cyclophosphamide-induced ovarian toxicity in rats: biochemical and histomorphometric evaluation of the ovary. Biochem Res Int:1–6. https://doi.org/10.1155/2013/764262

  30. Wang HX, Wang XY, Zhou DX et al (2013) Effects of low-dose, long-term formaldehyde exposure on the structure and functions of the ovary in rats. Toxicol Ind Health 29(7):609–615

    Article  PubMed  Google Scholar 

  31. Brehm E, Flaws JA (2019) Transgenerational effects of endocrine- disrupting chemicals on Male and female reproduction. Endocrinology 160(6):1421–1435. https://doi.org/10.1210/en.2019-00034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Bhandari G, Bagheri AR, Bhatt P et al (2021) Occurrence, potential ecological risks, and degradation of endocrine disrupter, nonylphenol, from the aqueous environment. Chemosphere 275:130013. https://doi.org/10.1016/j.chemosphere.2021.130013

    Article  CAS  PubMed  Google Scholar 

  33. Kim H, Oh S, Gye MC et al (2018) Comparative toxicological evaluation of nonylphenol and nonylphenol polyethoxylates using human keratinocytes. Drug Chem Toxicol 41:486–491. https://doi.org/10.1080/01480545.2017.1391829

    Article  CAS  PubMed  Google Scholar 

  34. Noorimotlagh Z, Kazeminezhad I, Jaafarzadeh N et al (2018) The visible-light photodegradation of nonylphenol in the presence of carbon-doped TiO2 with rutile/anatase ratio coated on GAC: effect of parameters and degradation mechanism. J Hazard Mater 350:108–120. https://doi.org/10.1016/j.jhazmat.2018.02.022

    Article  CAS  PubMed  Google Scholar 

  35. Zha J, Sun L, Spear PA et al (2008) Comparison of ethinylestradiol and nonylphenol effects on reproduction of Chinese rare minnows (Gobiocypris rarus). Ecotoxicol Environ Saf 71:390–399. https://doi.org/10.1016/j.ecoenv.2007.11.017

    Article  CAS  PubMed  Google Scholar 

  36. Khaliq H, Juming Z, Ke-Mei P (2018) The physiological role of boron on health. Biol Trace Elem Res 186(1):31–51. https://doi.org/10.1007/s12011-018-1284-3

    Article  CAS  PubMed  Google Scholar 

  37. Gautam GJ, Chaube R, Joy KP (2011) 4-Nonylphenol impairs ovarian recrudescence and induces atresia in the cat fish (Heteropneustes fossills). Indian J Sci Technol 4:9–14

    Google Scholar 

  38. Cruz MH, Leal CL, da Cruz JF et al (2014) Role of melatonin on production and preservation of gametes and embryos: a brief review. Anim Reprod Sci 145:150–160. https://doi.org/10.1016/j.anireprosci.2014.01.011

    Article  CAS  PubMed  Google Scholar 

  39. Gomez R, Schorsch M, Hahn T et al (2016) The influence of AMH on IVF success. Arch Gynecol Obstet 93:667–673. https://doi.org/10.1007/s00404-015-3901-0

    Article  CAS  Google Scholar 

  40. Josso N (2019) Anti-Müllerian hormone: a look back and ahead. Reproduction 158(6):81–89. https://doi.org/10.1530/REP-18-0602

    Article  Google Scholar 

  41. Rosen MP, Johnstone E, McCulloch CE et al (2012) A characterization of the relationship of ovarian reserve markers with age. Fertil Steril 97(1):238–243. https://doi.org/10.1016/j.fertnstert.2011.10.031

    Article  PubMed  Google Scholar 

  42. Ferraretti AP, La Marca A, Fauser BCJM et al (2011) ESHRE consensus on the definition of ’poor response’ to ovarian stimulation for in vitro fertilization: the Bologna criteria. Hum Reprod 26:1616–1624. https://doi.org/10.1093/humrep/der092

    Article  CAS  PubMed  Google Scholar 

  43. Dewailly D, Andersen CY, Balen A et al (2014) The physiology and clinical utility of anti-Mullerian hormone in women. Hum Reprod Update 20:370–385. https://doi.org/10.1093/humupd/dmt062

    Article  PubMed  Google Scholar 

  44. Choi Y, Rajkovic A (2006) Genetics of early mammalian folliculogenesis. Cell Mol Life Sci 63:579–590. https://doi.org/10.1007/s00018-005-5394-7

    Article  CAS  PubMed  Google Scholar 

  45. Klinger FG, De Felici M (2002) In vitro development of growing oocytes from fetal mouse oocytes: stage-specific regulation by stem cell factor and granulosa cells. Dev Biol 244:85–95. https://doi.org/10.1006/dbio.2002.0592

    Article  CAS  PubMed  Google Scholar 

  46. Luz VB, Chaves RN, Alves AMCV et al (2015) Role of insulin-like growth factor-I (IGF-I) and kit ligand (KL) in ovarian function. Acta Sci Vet 43:1300

    Google Scholar 

  47. Reynaud K, Cortvrindt R, Smitz J et al (2000) Effects of kit ligand and anti- kit antibody on growth of cultured mouse preantral follicles. Mol Reprod Dev 56:483–494 https://doi.org/10.1002/1098-2795(200008)56:4<483:AID-MRD6>3.0.CO;2-O

  48. Nilsson EE, Schindler R, Savenkova MI et al (2011) Inhibitory actions of Anti- Müllerian Hormone (AMH) on ovarian primordial follicle assembly. PloS One 6(5):e20087. https://doi.org/10.1371/journal.pone.0020087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Seifer DB, Merhi Z (2014) Is AMH a regulator of follicular atresia? J Assist Reprod Genet 31:1403–1407. https://doi.org/10.1007/s10815-014-0328-7

    Article  PubMed  PubMed Central  Google Scholar 

  50. Hu R, Wang FM, Yu L et al (2014) Antimüllerian hormone regulates stem cell factor expression in human granulosa cells. Fertil Steril 102:1742–1750. https://doi.org/10.1016/j.fertnstert.2014.08.012

    Article  CAS  PubMed  Google Scholar 

  51. Zhang JF, Yu CM, Yan LL et al (2018) Effect of anti-mullerian hormone on stem cell factor in serum, follicular fluid and ovarian granular cells of polycystic ovarian syndrome patients. Eur Rev Med Pharmacol Sci 22:7877–7882

    PubMed  Google Scholar 

  52. Zhang J, Fang L, Lu Z et al (2016) Are sirtuins markers of ovarian aging? Gene 575:680–686. https://doi.org/10.1016/j.gene.2015.09.043

    Article  CAS  PubMed  Google Scholar 

  53. Grabowska W, Sikora E, Bielak-Zmijewska A (2017) Sirtuins, a promising target in slowing down the ageing process. Biogerontology 18:447–476. https://doi.org/10.1007/s10522-017-9685-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Zhang M, Zhang Q, Hu Y et al (2017) miR-181a increases FoxO1 acetylation and promotes granulosa cell apoptosis via SIRT1 downregulation. Cell Death Dis 8:e3088. https://doi.org/10.1038/cddis.2017.467

    Article  PubMed  PubMed Central  Google Scholar 

  55. Long GY, Yang JY, Xu JJ et al (2019) SIRT1 knock-in mice preserve ovarian reserve resembling caloric restriction. Gene 686:194–202. https://doi.org/10.1016/j.gene.2018.10.040

    Article  CAS  PubMed  Google Scholar 

  56. Tatone C, Di Emidio G, Barbonetti A et al (2018) Sirtuins in gamete biology and reproductive physiology: emerging roles and therapeutic potential in female and male infertility. Hum Reprod Update 24:267–289. https://doi.org/10.1093/humupd/dmy003

    Article  CAS  PubMed  Google Scholar 

  57. Zhang XM, Li L, Xu JJ et al (2013) Rapamycin preserves the follicle pool reserve and prolongs the ovarian lifespan of female rats via modulating mTOR activation and sirtuin expression. Gene 523:82–87. https://doi.org/10.1016/j.gene.2013.03.039

    Article  CAS  PubMed  Google Scholar 

  58. El-Sheikh AA, Morsy MA, Hamouda AH (2016) Protective mechanisms of thymoquinone on methotrexate-induced intestinal toxicity in rats. Pharmacogn Mag 12:76–81. https://doi.org/10.4103/0973-1296.176106

    Article  CAS  Google Scholar 

  59. Roy IM, Nadar PS, Khurana S (2021) Neutral comet assay to detect and quantitate DNA double-strand breaks in hematopoietic stem cells. Bio Protoc 11(16):e4130. https://doi.org/10.21769/BioProtoc.4130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Weerachayaphorn J, Chuncharunee A, Jariyawat S et al (2010) Protection of centrilobular necrosis by Curcuma comosa Roxb. in carbon tetrachlorideinduced mice liver injury. J Ethnopharmacol 129:254–260. https://doi.org/10.1016/j.jep.2010.03.026

    Article  PubMed  Google Scholar 

  61. Kyle ME, Miccadei S, Nakae D et al (1987) Superoxide dismutase and catalase protect cultured hepatocytes from the cytotoxicity of acetominophen. Biochem Biophys Res Commun 149:889–896. https://doi.org/10.1016/0006-291X(87)90491-8

    Article  CAS  PubMed  Google Scholar 

  62. Sogut I, Paltun SO, Tuncdemir M et al (2018) The antioxidant and antiapoptotic effect of boric acid on hepatoxicity in chronic alcohol-fed rats. Can J Physiol Pharmacol 96(4):404–411. https://doi.org/10.1139/cjpp-2017-0487

    Article  CAS  PubMed  Google Scholar 

  63. Lu CJ, Hu J, Wang Z et al (2018) Discovery of boron-containing compounds as Aβ aggregation in- hibitors and antioxidants for the treatment of Alzheimer’s disease. Medchemcomm 9(11):1862–1870. https://doi.org/10.1039/C8MD00315G

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Scorei RI, Ciofrangeanu C, Ion R et al (2010) In vitro effects of calcium fructoborate upon production of inflammatory mediators by LPS-stimulated RAW 264.7 macrophages. Biol Trace Elem Res 135(1–3):334–344. https://doi.org/10.1007/s12011-009-8488-5

    Article  CAS  PubMed  Google Scholar 

  65. Knight PG, Glister C (2006) TGF-beta superfamily members and ovarian follicle development. Reproduction 132:191–206. https://doi.org/10.1530/rep.1.01074

    Article  CAS  PubMed  Google Scholar 

  66. Klein NA, Illingworth PJ, Groome NP et al (1996) Decreased inhibin B secretion is associated with the monotropic FSH rise in older, ovulatory women: a study of serum and follicular fluid levels of dimeric inhibin A and B in spontaneous menstrual cycles. J Clin Endocrinol Metab 81:2742–2745. https://doi.org/10.1210/jcem.81.7.8675606

    Article  CAS  PubMed  Google Scholar 

  67. Yazici S, Aksit H, Korkut O et al (2014) Effects of boric acid and 2-aminoethoxydiphenyl borate on necrotizing en- terocolitis. J Pediatr Gastroenterol Nutr 58(1):61–67. https://doi.org/10.1097/MPG.0b013e3182a7e02b

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Histology and Embryology, Erciyes University, Faculty of Medicine, 38039, Kayseri, Turkey

    Gozde Ozge Onder, Ozge Goktepe, Ozge Cengiz Mat, Demet Bolat, Eda Okur, Esra Balcioglu & Arzu Yay

  2. Genome and Stem Cell Center (GENKOK), Erciyes University, Kayseri, Turkey

    Gozde Ozge Onder, Ozge Goktepe, Esra Balcioglu & Arzu Yay

  3. Department of Gynecology and Obstetrics, Savur Prof Dr Aziz Sancar District State Hospital, Mardin, Turkey

    Enes Karaman

  4. Department of Gynecology and Obstetrics, Kayseri State Hospital, Kayseri, Turkey

    Erol Karakas

  5. Department of Biophysics, Erciyes University, Faculty of Medicine, 38039, Kayseri, Turkey

    Fazile Canturk Tan

  6. Department of Pharmaceutical Basic Science, Faculty of Pharmacy, Erciyes University, Kayseri, Turkey

    Munevver Baran

  7. Erciyes University, Experimental Researches and Application Center, Kayseri, Turkey

    Mustafa Ermis

Authors
  1. Gozde Ozge Onder
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ozge Goktepe
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Enes Karaman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Erol Karakas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ozge Cengiz Mat
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Demet Bolat
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Eda Okur
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Fazile Canturk Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Esra Balcioglu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Munevver Baran
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Mustafa Ermis
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Arzu Yay
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Gözde Özge Önder, Özge Göktepe, Münevver Baran, Enes Karaman, Erol Karakas, Ozge Cengiz Mat, Demet Bolat, Eda Okur, Fazile Canturk Tan, Esra Balcioglu, Munevver Baran, Mustafa Ermis and Arzu Hanım Yay. The first draft of the manuscript was written by Gözde Özge Önder, Arzu Hanım Yay and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Gozde Ozge Onder.

Ethics declarations

Ethics Approval

The Erciyes University's Animal Research Ethics Committee approved this work (No:22/164).

Conflict of Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Onder, G.O., Goktepe, O., Karaman, E. et al. Nonylphenol Exposure-Induced Oocyte Quality Deterioration Could be Reversed by Boric Acid Supplementation in Rats. Biol Trace Elem Res 201, 4518–4529 (2023). https://doi.org/10.1007/s12011-023-03657-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-023-03657-5

Keyword

Search

Navigation