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Impacts of PAH accumulation on reproductive hormones, indices of oxidative stress and BPDE-albumin adduct in women with recurrent pregnancy loss

  • Amany El-Sikaily (National Institute of Oceanography and Fisheries (NIOF)) ;
  • Mohamed Helal (National Institute of Oceanography and Fisheries (NIOF)) ;
  • Augusta Chinyere Nsonwu-Anyanwu (Department of Clinical Chemistry and Immunology, University of Calabar) ;
  • Hossam Azab (Obstetrics and Gynecology Department, Faculty of Medicine, Alexandria University) ;
  • Neveen Abd ElMoneim (Applied Medical Chemistry, Medical Research Institute, Alexandria University) ;
  • Eman Othman Salem Farahat (Applied Medical Chemistry, Medical Research Institute, Alexandria University) ;
  • Aziza Saad (Applied Medical Chemistry, Medical Research Institute, Alexandria University)
  • Received : 2022.12.09
  • Accepted : 2023.04.05
  • Published : 2023.07.15

Abstract

Chronic exposure to Poly aromatic hydrocarbons (PAHs) may be associated with adverse pregnancy outcomes. Disruption of hormonal and redox balance by toxic PAH metabolites may interfere with successful pregnancy leading to miscarriage. The association of exposure to PAH contaminated mussel via the dietary route with perturbations in reproductive hormones, biomarkers of oxidative stress, and PAH metabolites were assessed in women with recurrent pregnancy loss (RPL). Furthermore, an analysis of the concentration of PAHs in environmentally relevant bivalve animals was performed to preliminary get insights into the levels of these pollutants in the environment. Seventy-six women (20-35 years) were categorized into 18 fertile women without RPL (control), and Groups I, II, and III comprising 24, 18, and 16 women with RPL (2, 3, and>3 abortions respectively) were studied. Whole blood samples were collected for the estimation of malondialdehyde (MDA), catalase, reduced glutathione (GSH), glutathione-S-transferase (GST), progesterone (P4), follicle-stimulating hormone (FSH), benzo[a]pyren-7,8-dihydrodiol-9,10-epoxide-albumin adduct (BPDE-albumin) and urine for α-naphthol and β-naphthol. Two species of mussel Donax trunculus and Andar aduloii samples were collected for the estimation of 16 priority PAHs. The concentration of PAHs exceeding the maximum limits was observed in the two species of mussels studied. Higher levels of BPDE-albumin, MDA, GST, α and β-naphthol and lower GSH, catalase, FSH, and P4 were observed in women with RPL (Groups I-III) compared to controls (p= <0.001). Negative associations were observed between BPDE-albumin and catalase (r=- 0.276, p=0.036), and GSH (r=- 0.331, p=- 0.011) only in women with RPL. Collectively, our findings indicate a possible association of chronic PAH accumulation with recurrent pregnancy loss in women.

Keywords

References

  1. Ramesh A et al (2004) Bioavailability and risk assessment of orally ingested polycyclic aromatic hydrocarbons. Int J Toxicol 23:301-333. https://doi.org/10.1080/10915810490517063
  2. Dobraca D et al (2020) Urinary polycyclic aromatic hydrocarbons in relation to anthropometric measures and pubertal development in a cohort of Northern California girls. Environ Epidemiol 4:e0102. https://doi.org/10.1097/EE9.0000000000000102
  3. Grigoriou C et al (2021) Monitoring of polycyclic aromatic hydrocarbon Levels in Mussels (Mytilus galloprovincialis) from aquaculture farms in central macedonia region, greece, using gas chromatography-tandem Mass spectrometry method. Molecules 26:5953. https://doi.org/10.3390/molecules26195953
  4. Tornero V, Ribera d'Alcala M (2014) Contamination by hazardous substances in the Gulf of Naples and nearby coastal areas: a review of sources, environmental levels and potential impacts in the MSFD perspective. Sci Total Environ 466-467:820-840. https://doi.org/10.1016/j.scitotenv.2013.06.106
  5. EU (2011) Commission Regulation (EC) No 835/2011 amending regulation (EC) No 1881/2006 as regards maximum levels for polycyclic aromatic hydrocarbons in foodstufs. Of J Eur Union L215:4-8
  6. Yang L et al (2020) The association between prenatal exposure to polycyclic aromatic hydrocarbons and birth weight: a meta-analysis. PLoS One 15:e0236708. https://doi.org/10.1371/journal.pone.0236708
  7. Agarwal P et al (2018) Association between placental polycyclic aromatic hydrocarbons (PAHS), oxidative stress, and preterm delivery: a case-control study. Arch Environ Contam Toxicol 74:218-227. https://doi.org/10.1007/s00244-017-0455-0
  8. Nsonwu-Anyanwu AC et al (2022) Assessment of Essential and Non-essential Elements as Risk 534 Evaluation Indices in Men with Prostate Cancer in Calabar South-South Nigeria. Middle East J Cancer 13:285-292. https://doi.org/10.30476/mejc.2021.86638.1361
  9. Bukowska B, Duchnowicz P (2022) Molecular Mechanisms of Action of Selected Substances Involved in the Reduction of Benzo[a]pyrene-Induced Oxidative Stress. Molecules 27:1379. https://doi.org/10.3390/molecules27041379
  10. Bukowska B, Mokra K, Michalowicz J (2022) Benzo [a]pyrene-environmental occurrence human exposure and mechanisms of toxicity. Int J Mol Sci 23:6348. https://doi.org/10.3390/ijms23116348
  11. Ye X et al (2020) Exposure to polycyclic aromatic hydrocarbons and risk for premature ovarian failure and reproductive hormones imbalance. J Environ Sci 91:1-9. https://doi.org/10.1016/j.jes.2019.12.015
  12. Ye Y et al (2020) Environmental pollutant benzo[a]pyrene induces recurrent pregnancy loss through promoting apoptosis and suppressing migration of extravillous trophoblast. Biomed Res Int 2020:8983494. https://doi.org/10.1155/2020/8983494
  13. Yin S et al (2017) Environmental exposure to polycyclic aromatic hydrocarbons (PAHs): the correlation with and impact on reproductive hormones in umbilical cord serum. Environ Pollut 220:1429-1437. https://doi.org/10.1016/j.envpol.2016.10.090
  14. Cathey AL et al (2020) Polycyclic aromatic hydrocarbon exposure results in altered CRH, reproductive, and thyroid hormone concentrations during human pregnancy. Sci Total Environ 749:141581. https://doi.org/10.1016/j.scitotenv.2020.141581
  15. Das DN, Ravi N (2022) Influences of polycyclic aromatic hydrocarbon on the epigenome toxicity and its applicability in human health risk assessment. Environm Res 213:113677. https://doi.org/10.1016/j.envres.2022.113677
  16. Cathey A et al (2018) Distribution and predictors of urinary polycyclic aromatic hydrocarbon metabolites in two pregnancy cohort studies. Environ Pollut 232:556-562. https://doi.org/10.1016/j.envpol.2017.09.087
  17. Langlois PH et al (2014) Maternal occupational exposure to polycyclic aromatic hydrocarbons and small for gestational age offspring. Occup Environ Med 71:529-535. https://doi.org/10.1136/oemed-2013-101833
  18. Sampaio GR et al (2021) Polycyclic aromatic hydrocarbons in foods: biological Effects, legislation, occurrence, analytical methods, and strategies to reduce their formation. Int J Mol Sci 22:6010. https://doi.org/10.3390/ijms22116010
  19. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121-126. https://doi.org/10.1016/s0076-6879(84)05016-3
  20. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130-7139. https://pubmed.ncbi.nlm.nih.gov/4436300/ https://doi.org/10.1016/S0021-9258(19)42083-8
  21. Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol 186:421-431. https://doi.org/10.1016/0076-6879(90)86135-i
  22. Beutler E, Duron O, Kelly BM (1963) Improved method for the determination of blood glutathione. J Lab Clin Med 61:882-888. https://pubmed.ncbi.nlm.nih.gov/13967893/
  23. Webster RP, Roberts VH, Myatt L (2008) Protein nitration in placenta - functional significance. Placenta 29:985-994. https://doi.org/10.1016/j.placenta.2008.09.003
  24. Rose MP, Gaines Das RE, Balen AH (2000) Definition and measurement of follicle stimulating hormone. Endocr Rev 21:5-22. https://doi.org/10.1210/edrv.21.1.0388
  25. Lodovici M, Bigagli E (2009) Biomarkers of induced active and passive smoking damage. Int J Environ Res Public Health 6:874-888. https://doi.org/10.3390/ijerph6030874
  26. Spencer K (1986) Analytical reviews in clinical biochemistry: the estimation of creatinine. Ann Clin Biochem 23:1-25. https://doi.org/10.1177/000456328602300101
  27. Zidi-Jrah I et al (2016) Relationship between sperm aneuploidy, sperm DNA integrity, chromatin packaging, traditional semen parameters, and recurrent pregnancy loss. Fertil Steril 105:58-64. https://doi.org/10.1016/j.fertnstert.2015.09.041
  28. Ahmed OE, El Nady MM, Mahmoud SA (2018) Assessment of polycyclic aromatic hydrocarbons of organic richness in seawater from some coastal area around Alexandria city Egypt. Pet Sci Technol 36:682-687. https://doi.org/10.1080/10916466.2018.1442856
  29. El Nemr A et al (2004) Determination of Hydrocarbons in mussels from the Egyptian Red sea coast. Environ Monit Assess 96:251-261. https://doi.org/10.1023/B:EMAS.0000031731.88863.25
  30. Haiba NS, Hassan IA (2018) Monitoring and assessment of polycyclic Aromatic hydrocarbons (PAHs) in the atmosphere of Alexandria City, Egypt. Polycyclic Aromat Compd 38:219-230. https://doi.org/10.1080/10406638.2016.1200102
  31. Hassanien MA et al (2001) Seasonal and annual variations in air concentrations of Pb, Cd and PAHs in Cairo Egypt. Inter J Environ Health Res 11:13-27. https://doi.org/10.1080/0960312002001528
  32. Abdel-Shafy HI, Mansour MSM (2016) A review on polycyclic aromatic hydrocarbons: Source environmental impact effect on human health and remediation. Egypt J Pet 25:107-123. https://doi.org/10.1016/j.ejpe.2015.03.011
  33. Abdallah MA-E, Atia NN (2014) Atmospheric concentrations, gaseous-particulate distribution, and carcinogenic potential of polycyclic aromatic hydrocarbons in Assiut. Egypt Environ Sci Pollution Res 21:8059-8069. https://doi.org/10.1007/s11356-014-2746-6
  34. Baumard P, Budzinski H, Garrigues P (1998) Polycyclic aromatic hydrocarbons in sediments and mussels of the western Mediterranean sea. Enviro Toxicol Chem 17:765-776. https://doi.org/10.1002/etc.5620170501
  35. Yusof AM, Yanta NF, Wood AKH (2004) The use of bivalves as bio-indicators in the assessment of marine pollution along a coastal area. J Radioanal Nucl Chem 259:119-127. https://doi.org/10.1023/B:JRNC.0000015816.16869.6f
  36. Abootalebi Jahromi F et al (2020) Bisphenol A (BPA) and polycyclic aromatic hydrocarbons (PAHs) in the surface sediment and bivalves from Hormozgan Province coastline in the Northern persian gulf: A focus on source apportionment. Mar Pollut Bull 152:110941. https://doi.org/10.1016/j.marpolbul.2020.110941
  37. Moslen M, Miebaka CA, Boisa N (2019) Bioaccumulation of Polycyclic Aromatic Hydrocarbon (PAH) in a bivalve (Arca senilis- blood cockles) and health risk assessment. Toxicol Rep 6:990-997. https://doi.org/10.1016/j.toxrep.2019.09.006
  38. Jeng HA et al (2011) Repeated measurements for assessment of urinary 2-naphthol levels in individuals exposed to polycyclic aromatic hydrocarbons. J Environ Sci Health A Tox Hazard Subst Environ Eng 46:865-873. https://doi.org/10.1080/10934529.2011.580197
  39. Jeng HA et al (2011) Polycyclic aromatic hydrocarbon-induced oxidative stress and lipid peroxidation in relation to immunological alteration. Occup Environ Med 68:653-658. https://doi.org/10.1136/oem.2010.055020
  40. Giusti GV, Moneta E (1973) A case of abortion using parsley extract and naphthalene. Arch Kriminol 152:161-164. https://pubmed.ncbi.nlm.nih.gov/4766923/
  41. Saad AA et al (2019) Effect of polycyclic aromatic hydrocarbons exposure on sperm DNA in idiopathic male infertility. J Health Pollut 9:190309. https://doi.org/10.5696/2156-9614-9.21.190309
  42. Boynukalin FK, Baykal C (2014) Prenatal diagnosis of multiple fetal anomalies in naphthalene-addicted pregnant women: a case report. Clin Exp Obstet Gynecol 41:217-218 https://doi.org/10.12891/ceog16602014
  43. Shafer G, Arunachalam A, Lohmann P (2020) Newborn with perinatal naphthalene toxicity after maternal ingestion of mothballs during pregnancy. Neonatology 117:127-130. https://doi.org/10.1159/000504345
  44. Li P et al (2020) Polycyclic aromatic hydrocarbons exposure and early miscarriage in women undergoing in vitro fertilization-embryo transfer. Hum Fertil (Camb) 23:17-22. https://doi.org/10.1080/14647273.2018.1479888
  45. Han Y et al (2010) Reproductive hormones in relation to polycyclic aromatic hydrocarbon (PAH) metabolites among non-occupational exposure of males. Sci Total Environ 408:768-773. https://doi.org/10.1016/j.scitotenv.2009.11.021
  46. Ada AO, Yilmazer M, Suzen S, Demiroglu C, Demirbag AE, Efe S, Alemdar Y, Burgaz S, Iscan M (2007) Cytochrome P450 (CYP) and glutathione S-transferases (GST) polymorphisms (CYP1A1, CYP1B1, GSTM1, GSTP1 and GSTT1) and urinary levels of 1-hydroxypyrene in Turkish coke oven workers. Genet Mol Biol 30:511-519. https://doi.org/10.1590/S1415-47572007000400002
  47. Susanto AN, Zaini J, Nuwidya F (2021) Comparison of Serum benzo(a)pyrene diol epoxide-protein adducts level between kretek cigarette smokers and nonsmokers and the related factors. J Nat Sci Bio Med 12:4. https://doi.org/10.4103/jnsbm.JNSBM_100_20
  48. Jo YS et al (2022) Effects of polycyclic aromatic hydrocarbons on the proliferation and differentiation of placental cells. Reprod Biol Endocrinol 20:47. https://doi.org/10.1186/s12958-022-00920-7
  49. Kukrer S, Arlier S, Karaman S (2020) Ovarian reserve testing in the prediction of recurrent pregnancy loss. J Surg Med 4:25-28. https://doi.org/10.2882/josam.670091
  50. Kaur R, Gupta K (2016) Endocrine dysfunction and recurrent spontaneous abortion: an overview. Int J Appl Basic Med Res 6:79-83. https://doi.org/10.4103/2229-516X.179024
  51. Archibong AE et al (2002) Alteration of pregnancy related hormones and fetal survival in F-344 rats exposed by inhalation to benzo(a)pyrene. Reprod Toxicol 16:801-808. https://doi.org/10.1016/s0890-6238(02)00058-8
  52. Zajda K, Gregoraszczuk EL (2020) Environmental polycyclic aromatic hydrocarbons mixture, in human blood levels, decreased oestradiol secretion by granulosa cells via ESR1 and GPER1 but not ESR2 receptor. Hum Exp Toxicol 39:276-289. https://doi.org/10.1177/0960327119886027
  53. Ghneim HK, Alshebly MM (2016) Biochemical markers of oxidative stress in Saudi women with recurrent miscarriage. J Korean Med Sci 31:98-105. https://doi.org/10.3346/jkms.2016.31.1.98
  54. Abdul-Barry J, Qasim RS (2011) Study of oxidant-antioxidant status in recurrent spontaneous abortion. Thi-Qar Medical 5:35-46. https://jmed.utq.edu.iq/index.php/main/article/view/231
  55. Gharesi-Fard B, Zolghadri J, Kamali-Sarvestani E (2014) Alteration in the expression of proteins in unexplained recurrent pregnancy loss compared with in the normal placenta. J Reprod Dev 60:261-267. https://doi.org/10.1262/jrd.2013-096
  56. Prokopenko VM et al (2002) Glutathione-dependent system of antioxidant defense in the placenta in preterm delivery. Bull Exp Biol Med 133:442-443. https://doi.org/10.1023/a:1019845217485
  57. Shimada T, Fujii-Kuriyama Y (2004) Metabolic activation of polycyclic aromatic hydrocarbons to carcinogens by cytochromes P450 1A1 and 1B1. Cancer Sci 95:1-6. https://doi.org/10.1111/j.1349-7006.2004.tb03162.x
  58. Ferguson KK et al (2017) Urinary polycyclic aromatic hydrocarbon metabolite associations with biomarkers of inflammation, angiogenesis, and oxidative stress in pregnant women. Environ Sci Technol 51:4652-4660. https://doi.org/10.1021/acs.est.7b01252
  59. Welch BM et al (2022) Inflammation and oxidative stress as mediators of the impacts of environmental exposures on human pregnancy: Evidence from oxylipins. Pharmacol Ther 239:108181. https://doi.org/10.1016/j.pharmthera.2022.108181
  60. Rahmani Z et al (2021) Effect of prenatal exposure to Benzo[a] pyrene on ovarian toxicity and reproductive dysfunction: Protective effect of atorvastatin in the embryonic period. Environ Toxicol 36:1683-1693. https://doi.org/10.1002/tox.23164
  61. Zejnullahu VA, Zejnullahu VA, Kosumi E (2021) The role of oxidative stress in patients with recurrent pregnancy loss: a review. Reprod Health 18:207. https://doi.org/10.1186/s12978-021-01257-x