Skip to main content

Advertisement

SpringerLink
Log in

Maternal Serum Levels of Zinc, Copper, and Thiols in Preeclampsia Patients: a Case-Control Study

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

Abstract

Preeclampsia is one of the leading causes of maternal mortality-morbidity, and environmental factors act as the main driving force for the development of disease in genetically lean women. Trace element levels (zinc, copper) and thiol state (total, native thiol) may affect involved risk factors and play a role in the pathogenesis. The objective of our study is to assess trace element and thiol levels in patient and control groups. A total number of 88 pregnant women (in their third trimester) included 43 preeclampsia patients and 45 normotensive pregnant women as controls. The main findings of this study were the significantly elevated copper levels and decreased thiol levels (native and total thiols) in the patient group compared to controls (p < 0.05). Disulfide levels were not statistically different between the groups (p > 0.05). In patients, the predictive cutoff value of copper was 224 μg/dL and was 1.19 for the copper/native thiol ratio. Zinc levels were not statistically different between the two groups. Correlation analysis revealed no relationship between zinc-copper and zinc-total thiol levels in patients, while a positive correlation was evident in controls (zinc-copper, p < 0.05, r = 0.425, and zinc-total thiol levels, p < 0.05, r = 0.642). Patients had marginally high ALT and AST values in the normal range, and a significant difference was found between the two groups (p < 0.05). According to these results, elevated copper levels and decreased thiol levels may have a value for early prediction. The mechanisms that may be responsible for the altered element and thiol status have been discussed here in the context of oxidative stress.

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

Similar content being viewed by others

Data Availability

Based on a request, the data supporting the current work’s findings is available from the corresponding author.

Code Availability

Based on a request, the code is available from the corresponding author.

References

  1. Bartsch E, Medcalf KE, Park AL, Ray JG (2016) Clinical risk factors for pre-eclampsia determined in early pregnancy: systematic review and meta-analysis of large cohort studies. Bmj 353:i1753

    Article  Google Scholar 

  2. August P, Sibai BM (2017) Preeclampsia: Clinical features and diagnosis. Post TW, UpToDate Waltham, MA: UpToDate

  3. Sarwar MS, Ahmed S, Ullah MS, Kabir H, Rahman GM, Hasnat A, Islam MS (2013) Comparative study of serum zinc, copper, manganese, and iron in preeclamptic pregnant women. Biol Trace Elem Res 154(1):14–20

    Article  CAS  Google Scholar 

  4. Weber D, Stuetz W, Bernhard W, Franz A, Raith M, Grune T, Breusing N (2014) Oxidative stress markers and micronutrients in maternal and cord blood in relation to neonatal outcome. Eur J Clin Nutr 68(2):215–222

    Article  CAS  Google Scholar 

  5. Mills CF (2013) Zinc in human biology. Springer Science & Business Media,

  6. Hambidge KM, Krebs NF (2007) Zinc deficiency: a special challenge. J Nutr 137(4):1101–1105

    Article  CAS  Google Scholar 

  7. Jain S, Sharma P, Kulshreshtha S, Mohan G, Singh S, Bter J (2010) The role of calcium, magnesium, and zinc in pre-eclampsia. Biol Trace Elem Res 133(2):162–170

    Article  CAS  Google Scholar 

  8. Karim N (2018) Copper and Human Health-A Review. J Bahria Univ Med Dental Coll 8(2):117–122

    Article  Google Scholar 

  9. Gambling L, Kennedy C, McArdle HJ (2011) Iron and copper in fetal development. In: Seminars in cell & developmental biology. vol 6. Elsevier, pp 637-644

  10. Bost M, Houdart S, Oberli M, Kalonji E, Huneau J-F, Margaritis I (2016) Dietary copper and human health: Current evidence and unresolved issues. J Trace Elem Med Biol 35:107–115

    Article  CAS  Google Scholar 

  11. Bawa R, Tyagi S (2017) Correlation of microelements like plasma copper and zinc concentrations with female infertility. Int J Reprod Contracept Obs Gynecol 6:2351–2353

    Article  Google Scholar 

  12. Keshavarz P, Gh BFNM, Mirhafez SR, Nematy M, Azimi-Nezhad M, Afin SA, Esmaily H, Pourali L, Hakak AM, Soukhtanloo M (2017) Alterations in lipid profile, zinc and copper levels and superoxide dismutase activities in normal pregnancy and preeclampsia. Am J Med Sci 353(6):552–558

    Article  Google Scholar 

  13. Turell L, Radi R, Alvarez B (2013) The thiol pool in human plasma: the central contribution of albumin to redox processes. Free Radic Biol Med 65:244–253

    Article  CAS  Google Scholar 

  14. Practice Bulletin No AJOG (2019) 202: gestational hypertension and preeclampsia. Obstet Gynecol 133(1):e1–e25

    Google Scholar 

  15. Erel O, Neselioglu S (2014) A novel and automated assay for thiol/disulphide homeostasis. Clin Biochem 47(18):326–332

    Article  CAS  Google Scholar 

  16. Abbassi-Ghanavati M, Greer LG, Cunningham FG (2009) Pregnancy and laboratory studies: a reference table for clinicians. Obstet Gynecol 114(6):1326–1331

    Article  CAS  Google Scholar 

  17. Akinloye O, Oyewale O, Oguntibeju OO (2010) Evaluation of trace elements in pregnant women with pre-eclampsia. Afr J Biotechnol 9(32):5196–5202

    CAS  Google Scholar 

  18. Atamer Y, Koçyigit Y, Yokus B, Atamer A, Erden AC (2005) Lipid peroxidation, antioxidant defense, status of trace metals and leptin levels in preeclampsia. Eur J Obstet Gynecol Reprod Biol 119(1):60–66

    Article  CAS  Google Scholar 

  19. Serdar Z, Gür E, Develioğlu O (2006) Serum iron and copper status and oxidative stress in severe and mild preeclampsia. Cell Biochem Funct: Cellular biochemistry and its modulation by active agents or disease 24(3):209–215

    Article  CAS  Google Scholar 

  20. Rafeeinia A, Tabandeh A, Khajeniazi S, Marjani AJ (2014) Serum copper, zinc and lipid peroxidation in pregnant women with preeclampsia in gorgan. Open Biochem J 8:83

    Article  Google Scholar 

  21. Harma M, Harma M, Kocyigit A (2005) Correlation between maternal plasma homocysteine and zinc levels in preeclamptic women. Biol Trace Elem Res 104(2):97–105

    Article  CAS  Google Scholar 

  22. Vafaei H, Dalili M, Hashemi SA (2015) Serum concentration of calcium, magnesium and zinc in normotensive versus preeclampsia pregnant women: a descriptive study in women of Kerman province of Iran. Iran J Reproduct Med 13(1):23–26

    Google Scholar 

  23. Elmugabil A, Hamdan HZ, Elsheikh AE, Rayis DA, Adam I, Gasim GI (2016) Serum calcium, magnesium, zinc and copper levels in sudanese women with preeclampsia. PLoS One 11(12):e0167495

    Article  Google Scholar 

  24. Acikgoz S, Harma M, Harma M, Mungan G, Can M, Demirtas S (2006) Comparison of angiotensin-converting enzyme, malonaldehyde, zinc, and copper levels in preeclampsia. Biol Trace Elem Res 113(1):1–8

    Article  CAS  Google Scholar 

  25. Gzhegotskyi M, Sukhodolska N (2019) Lead, cadmium, copper and zinc content in women’s blood during the third trimester of uncomplicated and complicated gestation. Exp Clin Physiol Biochem 2019:5–11. https://doi.org/10.25040/ecpb2019.03.005

    Article  Google Scholar 

  26. Kumera G, Awoke T, Melese T, Eshetie S, Mekuria G, Mekonnen F, Ewunetu T, Gedle D (2015) Prevalence of zinc deficiency and its association with dietary, serum albumin and intestinal parasitic infection among pregnant women attending antenatal care at the University of Gondar Hospital, Gondar, Northwest Ethiopia. BMC Nutr 1(1):31

    Article  Google Scholar 

  27. Gammoh NZ, Rink L (2017) Zinc in infection and inflammation. Nutrients 9(6):624

    Article  Google Scholar 

  28. Olechnowicz J, Tinkov A, Skalny A, Suliburska J (2018) Zinc status is associated with inflammation, oxidative stress, lipid, and glucose metabolism. J Physiol Sci 68(1):19–31

    Article  CAS  Google Scholar 

  29. Ota E, Mori R, Middleton P, Tobe-Gai R, Mahomed K, Miyazaki C, Bhutta ZA (2015) Zinc supplementation for improving pregnancy and infant outcome. Cochrane Database Syst Rev (2)

  30. Ulas M, Cay M (2011) Effects of 17β-estradiol and vitamin E treatments on blood trace element and antioxidant enzyme levels in ovariectomized rats. Biol Trace Elem Res 139(3):347–355

    Article  CAS  Google Scholar 

  31. Bednarek-Tupikowska G, Jodkowska A, Antonowicz-Juchniewicz J (2010) Zinc, cooper, manganese, and selenium status in pre-and postmenopausal women during sex hormone therapy Stężenia cynku, miedzi, manganu i selenu u kobiet menopauzalnych przyjmujących terapię hormonalną. Adv Clin Exp Med 19(3):337–345

    Google Scholar 

  32. Linder M (2016) Ceruloplasmin and other copper binding components of blood plasma and their functions: an update. Metallomics 8(9):887–905

    Article  CAS  Google Scholar 

  33. Cantonwine DE, McElrath TF, Trabert B, Xu X, Sampson J, Roberts JM, Hoover RN, Troisi R (2019) Estrogen metabolism pathways in preeclampsia and normal pregnancy. Steroids 144:8–14

    Article  CAS  Google Scholar 

  34. Bellos I, Papantoniou N, Pergialiotis V (2018) Serum ceruloplasmin levels in preeclampsia: a meta-analysis. J Matern Fetal Neonatal Med 31(17):2342–2348

    Article  CAS  Google Scholar 

  35. Uriu-Adams JY, Keen CL (2005) Copper, oxidative stress, and human health. Mol Asp Med 26(4-5):268–298

    Article  CAS  Google Scholar 

  36. Nikolic A, Cabarkapa V, Novakov Mikic A, Jakovljević A, Stosic Z (2016) Ceruloplasmin and antioxidative enzymes in pre-eclampsia. J Matern Fetal Neonatal Med 29(18):2987–2993

    Article  CAS  Google Scholar 

  37. Sorenson JR (2012) Inflammatory diseases and copper: the metabolic and therapeutic roles of copper and other essential metalloelements in humans, vol 2. Springer Science & Business Media,

  38. Nishito Y, Kambe T (2018) Absorption mechanisms of iron, copper, and zinc: an overview. J Nutr Sci Vitaminol 64(1):1–7

    Article  CAS  Google Scholar 

  39. Alese MO, Moodley J, Naicker T (2019) Preeclampsia and HELLP syndrome, the role of the liver. J Matern Fetal Neonatal Med 34(1):117–123 1-7

    Article  Google Scholar 

  40. Ghezzi P, Bonetto V, Fratelli M (2005) Thiol–disulfide balance: from the concept of oxidative stress to that of redox regulation. Antioxid Redox Signal 7(7-8):964–972

    Article  CAS  Google Scholar 

  41. Korkmaz V, Kurdoglu Z, Alisik M, Cetin O, Korkmaz H, Surer H, Erel O (2016) Impairment of thiol-disulfide homeostasis in preeclampsia. J Matern Fetal Neonatal Med 29(23):3848–3853

    Article  CAS  Google Scholar 

  42. Ozler S, Erel O, Oztas E, Ersoy AO, Ergin M, Sucak A, Neselioglu S, Uygur D, Danisman N (2015) Serum thiol/disulphide homeostasis in preeclampsia. Hypertens Pregnancy 34(4):474–485

    Article  CAS  Google Scholar 

  43. Cremers CM, Jakob U (2013) Oxidant sensing by reversible disulfide bond formation. J Biol Chem 288(37):26489–26496

    Article  CAS  Google Scholar 

  44. Onat T, Aydoğan Kırmızı D, Başer E, Ercan M, Demir Çaltekin M, Yalçın S, Kara M, Esinler D, Yalvaç ES (2020) The relationship between oxidative stress and preeclampsia. The serum ischemia-modified albumin levels and thiol/disulfide homeostasis. Turk J Obstet Gynecol 17(2):102–107. https://doi.org/10.4274/tjod.galenos.2020.23682

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to thank Tagı Polat for his supports.

Funding

The research was funded by Bezmialem Foundation University Scientific Research Projects Unit (Project number: 6.2016/43).

Author information

Authors and Affiliations

  1. Department of Medical Biochemistry, Faculty of Medicine, Bezmialem Vakif University, 34093, Istanbul, Turkey

    Ayse Zehra Gul, Sahabettin Selek, Ufuk Sarıkaya, Tugce Yıldız & Metin Demirel

  2. Department of Gynaecology and Obstetrics, Istanbul Education Research Hospital, 34098, Istanbul, Turkey

    Nil Atakul

  3. Department of Medical Biochemistry, Faculty of Medicine, Beykent University, 34398, Istanbul, Turkey

    Yıldız Atamer

Authors
  1. Ayse Zehra Gul
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nil Atakul
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sahabettin Selek
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yıldız Atamer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ufuk Sarıkaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tugce Yıldız
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Metin Demirel
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Ayse Zehra Gul, Nil Atakul, and Sahabettin Selek contributed to the research equally.

Corresponding author

Correspondence to Ayse Zehra Gul.

Ethics declarations

Ethics Approval

This research was conducted in accordance with the Declaration of Helsinki and approved by the clinical research ethics committee of Bezmialem Vakıf University (No. 54022451-050.05.04).

Consent to Participate

Each subject was informed about the study purpose, and a written consent was obtained from all participants.

Consent for Publication

Approvals from all authors were obtained for publication.

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gul, A.Z., Atakul, N., Selek, S. et al. Maternal Serum Levels of Zinc, Copper, and Thiols in Preeclampsia Patients: a Case-Control Study. Biol Trace Elem Res 200, 464–472 (2022). https://doi.org/10.1007/s12011-021-02660-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-021-02660-y

Keywords

Search

Navigation