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Licensed Unlicensed Requires Authentication Published by De Gruyter April 17, 2020

Exposure to persistent organic pollutants during tooth formation: molecular mechanisms and clinical findings

Serena Bianchi , Sara Bernardi ORCID logo EMAIL logo , Manuel Belli , Giuseppe Varvara and Guido Macchiarelli

Abstract

Persistent organic pollutants (POPs) constitute a relevant part of environmental pollution. POPs are chemical compounds that persist for a long time in the environment, bio-accumulate in the human body and determine significant adverse consequences to human health. The characteristics of these substances are lipo-affinity, semi-volatility and resistance to the degradation processes. Results deriving from several different studies attest that exposure to the main classes of POPs results in multiple toxic effects on humans and experimental animal models. Among the various alterations caused by exposition to and bio-accumulation of POPs, there are abnormalities in tooth formation and related hard dental tissue structure, especially enamel. This review aimed to describe the close association between the exposure of these compounds during the development of the tooth germ and the occurrence of tooth structural anomalies. Indeed, structural defects of the enamel have as possible consequences higher susceptibility of the tooth to caries disease and higher fragility of the crown to the occlusal trauma.

  1. Research funding: Authors state no funding involved.

  2. Conflict of interest: Authors state no conflict of interest.

  3. Informed consent: Informed consent is not applicable.

  4. Ethical approval: The conducted research is not related to either human or animal use.

References

1. Lohmann R, Breivik K, Dachs J, Muir D. Global fate of POPs: current and future research directions. Environ Pollut 2007;150:150–65.10.1016/j.envpol.2007.06.051Search in Google Scholar PubMed

2. Snedeker SM. Pesticides and breast cancer risk: a review of DDT, DDE, and dieldrin. Environ Health Perspect 2001;109:35–47.Search in Google Scholar

3. Bajwa A, Ali U, Mahmood A, Chaudhry MJ, Syed JH, Li J, et al. Organochlorine pesticides (OCPs) in the Indus River catchment area, Pakistan: status, soil–air exchange and black carbon mediated distribution. Chemosphere 2016;152:292–300.10.1016/j.chemosphere.2016.01.024Search in Google Scholar PubMed

4. Vos JG. Health effects of hexachlorobenzene and the TEF approach. Environ Health Perspect 2000;108:A58–8.10.1289/ehp.108-a58aSearch in Google Scholar PubMed PubMed Central

5. Palmerini MG, Zhurabekova G, Balmagambetova A, Nottola SA, Miglietta S, Belli M, et al. The pesticide lindane induces dose-dependent damage to granulosa cells in an in-vitro culture. Reprod Biol 2017;17:349–56.10.1016/j.repbio.2017.09.008Search in Google Scholar PubMed

6. Palmerini MG, Belli M, Nottola SA, Miglietta S, Bianchi S, Bernardi S, et al. Mancozeb impairs the ultrastructure of mouse granulosa cells in a dose-dependent manner. J Reprod Dev 2018;64:75–82.10.1262/jrd.2017-143Search in Google Scholar PubMed PubMed Central

7. Nottola SA, Cecconi S, Bianchi S, Motta C, Rossi G, Continenza MA, et al. Ultrastructure of isolated mouse ovarian follicles cultured in vitro. Reprod Biol Endocrinol 2011;9:3.10.1186/1477-7827-9-3Search in Google Scholar PubMed PubMed Central

8. Palmerini MG, Nottola SA, Tunjung WAS, Kadowaki A, Bianchi S, Cecconi S, et al. EGF-FSH supplementation reduces apoptosis of pig granulosa cells in co-culture with cumulus-oocyte complexes. Biochem Biophys Res Commun 2016;481:159–64.10.1016/j.bbrc.2016.10.151Search in Google Scholar PubMed

9. Khalili MA, Maione M, Palmerini MG, Bianchi S, Macchiarelli G, Nottola SA. Ultrastructure of human mature oocytes after vitrification. Eur J Histochem 2012;56:e38.10.4081/ejh.2012.e38Search in Google Scholar PubMed PubMed Central

10. Bianchi S, Macchiarelli G, Micara G, Linari A, Boninsegna C, Aragona C, et al. Ultrastructural markers of quality are impaired in human metaphase II aged oocytes: a comparison between reproductive and in-vitro aging. J Assist Reprod Genet 2015;32:1343–58.10.1007/s10815-015-0552-9Search in Google Scholar PubMed PubMed Central

11. Zhurabekova G, Balmagambetova A, Bianchi S, Belli M, Bekmukhambetov Y, Macchiarelli G. The toxicity of lindane in the female reproductive system: a review on the Aral Sea. EuroMediterranean Biomed J 2018;13:104–8.Search in Google Scholar

12. Babajko S, Jedeon K, Houari S, Loiodice S, Berdal A. Disruption of steroid axis, a new paradigm for molar incisor hypomineralization (MIH). Front Physiol 2017;8:343.10.3389/fphys.2017.00343Search in Google Scholar PubMed PubMed Central

13. Guo H, Zhang L, Wei K, Zhao J, Wang Y, Jin F, et al. Exposure to a continuous low dose of tetrachlorodibenzo-p-dioxin impairs the development of the tooth root in lactational rats and alters the function of apical papilla-derived stem cells. Arch Oral Biol 2015;60:199–207.10.1016/j.archoralbio.2014.10.001Search in Google Scholar

14. Small BW, Murray JJ. Enamel opacities: prevalence, classifications and aetiological considerations. J Dent 1978;6:33–42.10.1016/0300-5712(78)90004-0Search in Google Scholar

15. Behie AM, Miszkiewicz JJ. Enamel neonatal line thickness in deciduous teeth of Australian children from known maternal health and pregnancy conditions. Early Hum Dev 2019;137:104821.10.1016/j.earlhumdev.2019.07.004Search in Google Scholar

16. Kierdorf U, Kierdorf H, Fejerskov O. Fluoride-induced developmental changes in enamel and dentine of European roe deer (Capreolus capreolus L.) as a result of environmental pollution. Arch Oral Biol 1993;38:1071–81.10.1016/0003-9969(93)90169-MSearch in Google Scholar

17. Alaluusua S, Lukinmaa P, Koskimies M, Pirinen S, Hölttä P, Kallio M, et al. Developmental dental defects associated with long breast feeding. Eur J Oral Sci 1996;104:493–7.10.1111/j.1600-0722.1996.tb00131.xSearch in Google Scholar

18. Brook AH, Fearne JM, Smith JM. Environmental causes of enamel defects. Ciba Found Symp 1997;205:212–21.10.1002/9780470515303.ch15Search in Google Scholar

19. Caruso S, Bernardi S, Pasini M, Giuca MR, Docimo R, Continenza MA, et al. The process of mineralisation in the development of human tooth. Eur J Paediatr Dent 2016;17:322–6.Search in Google Scholar

20. Bernardi S, Bianchi S, Continenza MA, Pinchi V, Macchiarelli G. Morphological study of the labial grooves’ pattern in an Italian population. Aust J Forensic Sci 2018:1–10.10.1080/00450618.2018.1541192Search in Google Scholar

21. Bernardi S, Bianchi S, Fantozzi G, Leuter C, Continenza MA, Macchiarelli G. Morphometric study on single-root premolars in a European population sample: an update on lengths and diameters. Eur J Anat 2019;23:17–25.Search in Google Scholar

22. Ashraf MA. Persistent organic pollutants (POPs): a global issue, a global challenge. Environ Sci Pollut Res 2017;24:4223–7.10.1007/s11356-015-5225-9Search in Google Scholar

23. Ahlborg UG, Brouwer A, Fingerhut MA, Jacobson JL, Jacobson SW, Kennedy SW, et al. Impact of polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls on human and environmental health, with special emphasis on application of the toxic equivalency factor concept. Eur J Pharmacol Environ Toxicol Pharmacol 1992;228:179–99.10.1016/0926-6917(92)90029-CSearch in Google Scholar

24. Ghosh S, Mitra PS, Loffredo CA, Trnovec T, Murinova L, Sovcikova E, et al. Transcriptional profiling and biological pathway analysis of human equivalence PCB exposure in vitro: indicator of disease and disorder development in humans. Environ Res 2015;138:202–16.10.1016/j.envres.2014.12.031Search in Google Scholar PubMed PubMed Central

25. Brouwer A, Ahlborg UG, Van den Berg M, Birnbaum SL, Boersma ER, Bosveld B, et al. Functional aspects of developmental toxicity of polyhalogenated aromatic hydrocarbons in experimental animals and human infants. Eur J Pharmacol Environ Toxicol Pharmacol 1995;293:1–40.10.1016/0926-6917(95)90015-2Search in Google Scholar

26. Jan J, Sovcikova E, Kočan A, Wsolova L, Trnovec T. Developmental dental defects in children exposed to PCBs in eastern Slovakia. Chemosphere 2007;67:S350–4.10.1016/j.chemosphere.2006.05.148Search in Google Scholar

27. Hashiguchi I, Akamine A, Hara Y, Maeda K, Anan H, Abe T, et al. [Effects on the hard tissue of teeth in PCB-poisoned rats]. Fukuoka Igaku Zasshi 1985;76:221–8.Search in Google Scholar

28. McNulty WP. Toxicity and fetotoxicity of TCDD, TCDF, and PCB isomers in rhesus macaques (Macaca mulatta). Environ Health Perspect 1985;60:77–88.10.1289/ehp.856077Search in Google Scholar

29. Hara I. Health status and PCBs in blood of workers exposed to PCBs and of their children. Environ Health Perspect 1985;59:85–90.10.1289/ehp.59-1568101Search in Google Scholar

30. Rogan WJ, Gladen BC, Hung KL, Koong SL, Shih LY, Taylor JS, et al. Congenital poisoning by polychlorinated biphenyls and their contaminants in Taiwan. Science 1988;241:334–6.10.1126/science.3133768Search in Google Scholar

31. Safe SH. Polychlorinated biphenyls (PCBs): environmental impact, biochemical and toxic responses, and implications for risk assessment. Crit Rev Toxicol 1994;24:87–149.10.3109/10408449409049308Search in Google Scholar

32. Masuda Y. Approach to risk assessment of chlorinated dioxins from Yusho PCB poisoning. Chemosphere 1996;32:583–94.10.1016/0045-6535(95)00314-2Search in Google Scholar

33. Long PH, Herbert RA, Nyska A. Hexachlorobenzene-induced incisor degeneration in Sprague-Dawley rats. Toxicol Pathol 2004;32:35–40.10.1080/01926230490260871Search in Google Scholar PubMed

34. Gocmen A, Peters H, Cripps D, Bryan G, Morris C. Hexachlorobenzene episode in Turkey. Biomed Env Sci 1989;2:36–43.Search in Google Scholar

35. Larigot L, Juricek L, Dairou J, Coumoul X. AhR signaling pathways and regulatory functions. Biochim Open 2018;7:1–9.10.1016/j.biopen.2018.05.001Search in Google Scholar PubMed PubMed Central

36. Mulero-Navarro S, Fernandez-Salguero PM. New trends in aryl hydrocarbon receptor biology. Front Cell Dev Biol 2016;4:45.10.3389/fcell.2016.00045Search in Google Scholar PubMed PubMed Central

37. Petrulis JR, Perdew GH. The role of chaperone proteins in the aryl hydrocarbon receptor core complex. Chem Biol Interact 2002;141:25–40.10.1016/S0009-2797(02)00064-9Search in Google Scholar

38. Robert B, Martine A, Lawrence A, Xavier C. The aryl hydrocarbon receptor system. Drug Metabol Drug Interact 2012;27:3.Search in Google Scholar

39. Varvara G, Bernardi S, Cutilli T, Bianchi S, Sinjari B, Piattelli M. Anti-inflammatory steroid use in impacted third molar surgery: a systematic review. J Biol Regul Homeost Agents 2017;31:1095–9.Search in Google Scholar

40. Alaluusua S, Calderara P, Gerthoux PM, Lukinmaa PL, Kovero O, Needham L, et al. Developmental dental aberrations after the dioxin accident in Seveso. Environ Health Perspect 2004;112:1313–8.10.1289/ehp.6920Search in Google Scholar

41. Ngoc VTN, Van Nhon B, Tan NTM, Van Thuc P, Hien VTT, Dung TM, et al. The higher prevalence of developmental defects of enamel in the dioxin-affected region than non-dioxin-affected region: result from a cross-sectional study in Vietnam. Odontology 2019;107:17–22.10.1007/s10266-018-0358-1Search in Google Scholar

42. Kattainen H, Tuukkanen J, Simanainen U, Tuomisto JT, Kovero O, Lukinmaa PL, et al. In-utero/lactational 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin exposure impairs molar tooth development in rats. Toxicol Appl Pharmacol 2001;174:216–24.10.1006/taap.2001.9216Search in Google Scholar

43. Gao Y, Sahlberg C, Kiukkonen A, Alaluusua S, Pohjanvirta R, Tuomisto J, et al. Lactational exposure of Han/Wistar rats to 2,3,7,8-tetrachlorodibenzo-p-dioxin interferes with enamel maturation and retards dentine mineralization. J Dent Res 2004;83:139–44.10.1177/154405910408300211Search in Google Scholar

44. Yilmaz B, Seyran AD, Sandal S, Aydin M, Colakoglu N, Kocer M, et al. Modulatory effects of Aroclors 1221 and 1254 on bone turnover and vertebral histology in intact and ovariectomized rats. Toxicol Lett 2006;166:276–84.10.1016/j.toxlet.2006.08.003Search in Google Scholar

45. Dobrzyński M, Kaczmarek U, Kuropka P, Reichert P, Grzech-Leśniak K, Całkosiński I. Tooth development disorders in infants of rat dams exposed to 2,3,7,8 tetrachlorodibenzo-p-dioxin and protective role of tocopherol and acetylsalicylic acid. Pol J Vet Sci 2017;20:769–78.Search in Google Scholar

46. Schlatter J, Zimmerli B, Dick R, Panizzon R, Schlatter C. Dietary intake and risk assessment of phototoxic furocoumarins in humans. Food Chem Toxicol 1991;29:523–30.10.1016/0278-6915(91)90044-8Search in Google Scholar

47. Heimler I, Trewin AL, Chaffin CL, Rawlins RG, Hutz RJ. Modulation of ovarian follicle maturation and effects on apoptotic cell death in holtzman rats exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in utero and lactationally. Reprod Toxicol 1998;12:69–73.10.1016/S0890-6238(97)00101-9Search in Google Scholar

48. Całkosiński I, Dobrzyński M, Cegielski M, Sieja A. The multifaceted effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in organisms, especially dentition changes. Postep Hig Med Dosw 2006;60:237–40.Search in Google Scholar

49. Madhukar BV, Brewster DW, Matsumura F. Effects of in-vivo–administered 2,3,7,8-tetrachlorodibenzo-p-dioxin on receptor binding of epidermal growth factor in the hepatic plasma membrane of rat, guinea pig, mouse, and hamster. Proc Natl Acad Sci USA 1984;81:7407–11.10.1073/pnas.81.23.7407Search in Google Scholar

50. Alaluusua S, Lukinmaa PL, Pohjanvirta R, Unkila M, Tuomisto J. Exposure to 2,3,7,8-tetrachlorodibenzo-para-dioxin leads to defective dentin formation and pulpal perforation in rat incisor tooth. Toxicology 1993;81:1–13.10.1016/0300-483X(93)90152-ISearch in Google Scholar

51. Romero AN, Herlin M, Finnilä M, Korkalainen M, Håkansson H, Viluksela M, et al. Skeletal and dental effects on rats following in utero/lactational exposure to the non-dioxin-like polychlorinated biphenyl PCB 180. PLoS One 2017;12:e0185241.10.1371/journal.pone.0185241Search in Google Scholar PubMed PubMed Central


Article note

The figures were realized using the infographic software MindTheGraph®


Received: 2019-11-17
Accepted: 2020-03-09
Published Online: 2020-04-17
Published in Print: 2020-11-18

©2020 Walter de Gruyter GmbH, Berlin/Boston

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