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Mediation of mitochondrial DNA copy number and oxidative stress in fluoride-related bone mineral density alteration in Chinese farmers

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Abstract

Excessive fluoride can adversely affect bone mineral density (BMD). Oxidative stress and mitochondrial dysfunction are crucial mechanisms of health damage induced by fluoride. Here, a cross-sectional survey involving 907 Chinese farmers (aged 18–60) was carried out in Tongxu County in 2017, aiming to investigate the significance of mitochondrial DNA copy number (mtDNAcn) and oxidative stress in fluoride-related BMD change. Concentrations of urinary fluoride (UF), serum oxidative stress biomarkers, including total antioxidant capacity (T-AOC), total superoxide dismutase (T-SOD), glutathione peroxidase (GSH-Px), and malondialdehyde (MDA), as well as relative mtDNAcn in peripheral blood were determined. The multivariable linear model and mediation analysis were performed to assess associations between UF, oxidative stress, and relative mtDNAcn with BMD. Results showed that GSH-Px levels increased by 6.98 U/mL [95% confidence interval (CI) 3.41–10.56)] with each 1.0 mg/L increment of UF. After stratification, the T-AOC, relative mtDNAcn, and BMD decreased by 0.04 mmol/L (–0.08 ~ –0.01), 0.29-unit (–0.55 ~ –0.04), and 0.18-unit (–0.33 ~ –0.03) with every 1.0 mg/L elevation of UF in the excessive fluoride group (EFG, adults with UF > 1.6 mg/L), respectively. Furthermore, T-AOC and relative mtDNAcn were favorably related to the BMD in the EFG (β = 0.82, 95%CI 0.16–1.48 for T-AOC; β = 0.11, 95%CI 0.02–0.19 for relative mtDNAcn). Mediation analysis showed that relative mtDNAcn and T-AOC mediated 15.4% and 17.1% of the connection between excessive fluoride and reduced BMD, respectively. Findings suggested that excessive fluoride was related to lower BMD in adults, and the decrement of T-AOC and relative mtDNAcn partially mediate this relationship.

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References

  • Abduweli Uyghurturk, D., Goin, D. E., Martinez-Mier, E. A., Woodruff, T. J., & DenBesten, P. K. (2020). Maternal and fetal exposures to fluoride during mid-gestation among pregnant women in northern California. Environmental Health, 19(1), 38. https://doi.org/10.1186/s12940-020-00581-2

    Article  CAS  Google Scholar 

  • Arican, O., Kurutas, E. B., & Sasmaz, S. (2005). Oxidative stress in patients with acne vulgaris. Mediators of Inflammation, 6, 380–384. https://doi.org/10.1155/Mi.2005.380

    Article  Google Scholar 

  • Cagalova, A., Ticha, L., Gaal Kovalcikova, A., Sebekova, K., & Podracka, L. (2021). Bone mineral density and oxidative stress in adolescent girls with anorexia nervosa. European Journal of Pediatrics, 181(1), 311–321. https://doi.org/10.1007/s00431-021-04199-5

    Article  CAS  Google Scholar 

  • Ciccone, S., Maiani, E., Bellusci, G., Diederich, M., & Gonfloni, S. (2013). Parkinson’s disease: A complex interplay of mitochondrial DNA alterations and oxidative stress. International Journal of Molecular Sciences, 14(2), 2388–2409. https://doi.org/10.3390/ijms14022388

    Article  CAS  Google Scholar 

  • Dec, K., Lukomska, A., Skonieczna-Zydecka, K., Jakubczyk, K., Tarnowski, M., Lubkowska, A., Baranowska-Bosiacka, I., Styburski, D., Skorka-Majewicz, M., Maciejewska, D., & Gutowska, I. (2020). Chronic exposure to fluoride affects GSH level and NOX4 expression in rat model of this element of neurotoxicity. Biomolecules, 10(3), 422. https://doi.org/10.3390/biom10030422

    Article  CAS  Google Scholar 

  • Dey Bhowmik, A., Das, T., & Chattopadhyay, A. (2023). Chronic exposure to environmentally relevant concentration of fluoride impairs osteoblast’s collagen synthesis and matrix mineralization: Involvement of epigenetic regulation in skeletal fluorosis. Environmental Research, 236(Pt 2), 116845. https://doi.org/10.1016/j.envres.2023.116845

    Article  CAS  Google Scholar 

  • Di, D., Zhang, R., Zhou, H., Wei, M., Cui, Y., Zhang, J., Yuan, T., Liu, Q., Zhou, T., & Wang, Q. (2023). Joint effects of phenol, chlorophenol pesticide, phthalate, and polycyclic aromatic hydrocarbon on bone mineral density: Comparison of four statistical models. Environmental Science and Pollution Research International, 30(33), 80001–80013. https://doi.org/10.1007/s11356-023-28065-z

    Article  CAS  Google Scholar 

  • Ding, H., Yin, C., Yang, M., Zhou, R., Wang, X., & Pan, X. (2023). Screening of differentially methylated genes in skeletal fluorosis of rats with different types and involvement of aberrant methylation of Cthrc1. Environmental Pollution, 332, 121931. https://doi.org/10.1016/j.envpol.2023.121931

    Article  CAS  Google Scholar 

  • Emperador, S., Garrido-Perez, N., Amezcua-Gil, J., Gaudo, P., Andres-Sanz, J. A., Yubero, D., Fernandez-Marmiesse, A., O’Callaghan, M. M., Ortigoza-Escobar, J. D., Iriondo, M., Ruiz-Pesini, E., Garcia-Cazorla, A., Gil-Campos, M., Artuch, R., Montoya, J., & Bayona-Bafaluy, M. P. (2019). Molecular characterization of New FBXL4 mutations in patients with mtDNA depletion syndrome. Frontiers in Genetics, 10, 1300. https://doi.org/10.3389/fgene.2019.01300

    Article  CAS  Google Scholar 

  • Gao, M., Sun, L., Xu, K., Zhang, L., Zhang, Y., He, T., Sun, R., Huang, H., Zhu, J., Zhang, Y., Zhou, G., & Ba, Y. (2020). Association between low-to-moderate fluoride exposure and bone mineral density in Chinese adults: Non-negligible role of RUNX2 promoter methylation. Ecotoxicology and Environmental Safety, 203, 111031. https://doi.org/10.1016/j.ecoenv.2020.111031

    Article  CAS  Google Scholar 

  • Helte, E., Donat Vargas, C., Kippler, M., Wolk, A., Michaelsson, K., & Akesson, A. (2021). Fluoride in drinking water, diet, and urine in relation to bone mineral density and fracture incidence in postmenopausal women. Environmental Health Perspectives, 129(4), 47005. https://doi.org/10.1289/EHP7404

    Article  CAS  Google Scholar 

  • Hung, M., Hon, E. S., Mohajeri, A., Moparthi, H., Vu, T., Jeon, J., & Lipsky, M. S. (2023). A national study exploring the association between fluoride levels and dental fluorosis. JAMA Network Open, 6(6), e2318406. https://doi.org/10.1001/jamanetworkopen.2023.18406

    Article  Google Scholar 

  • Janssen, B. G., Munters, E., Pieters, N., Smeets, K., Cox, B., Cuypers, A., Fierens, F., Penders, J., Vangronsveld, J., Gyselaers, W., & Nawrot, T. S. (2012). Placental mitochondrial DNA content and particulate air pollution during in utero life. Environmental Health Perspectives, 120(9), 1346–1352. https://doi.org/10.1289/ehp.1104458

    Article  CAS  Google Scholar 

  • Jin, Y., Zhou, B. H., Zhao, J., Ommati, M. M., Wang, S., & Wang, H. W. (2023). Fluoride-induced osteoporosis via interfering with the RANKL/RANK/OPG pathway in ovariectomized rats: Oophorectomy shifted skeletal fluorosis from osteosclerosis to osteoporosis. Environmental Pollution, 336, 122407. https://doi.org/10.1016/j.envpol.2023.122407

    Article  CAS  Google Scholar 

  • Kluska, M., Juszczak, M., Zuchowski, J., Stochmal, A., & Wozniak, K. (2022). Effect of Kaempferol and Its glycoside derivatives on antioxidant status of HL-60 Cells treated with etoposide. Molecules, 27(2), 333. https://doi.org/10.3390/molecules27020333

    Article  CAS  Google Scholar 

  • Kosmider, B., Lin, C. R., Karim, L., Tomar, D., Vlasenko, L., Marchetti, N., Bolla, S., Madesh, M., Criner, G. J., & Bahmed, K. (2019). Mitochondrial dysfunction in human primary alveolar type II cells in emphysema. eBioMedicine, 46, 305–316. https://doi.org/10.1016/j.ebiom.2019.07.063

    Article  Google Scholar 

  • Li, J., Cai, D., Yao, X., Zhang, Y., Chen, L., Jing, P., Wang, L., & Wang, Y. (2016). Protective effect of ginsenoside Rg1 on hematopoietic stem/progenitor cells through attenuating oxidative stress and the Wnt/beta-catenin signaling pathway in a mouse model of d-galactose-induced aging. International Journal of Molecular Sciences, 17(6), 849. https://doi.org/10.3390/ijms17060849

    Article  CAS  Google Scholar 

  • Lin, M. T., & Beal, M. F. (2006). Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature, 443(7113), 787–795. https://doi.org/10.1038/nature05292

    Article  CAS  Google Scholar 

  • Liu, F., Yuan, L., Li, L., Yang, J., Liu, J., Chen, Y., Zhang, J., Lu, Y., Yuan, Y., & Cheng, J. (2023). S-sulfhydration of SIRT3 combats BMSC senescence and ameliorates osteoporosis via stabilizing heterochromatic and mitochondrial homeostasis. Pharmacological Research, 192, 106788. https://doi.org/10.1016/j.phrs.2023.106788

    Article  CAS  Google Scholar 

  • Lv, Y. G., Kang, L., & Wu, G. (2016). Fluorosis increases the risk of postmenopausal osteoporosis by stimulating interferon gamma. Biochemical and Biophysical Research Communications, 479(2), 372–379. https://doi.org/10.1016/j.bbrc.2016.09.083

    Article  CAS  Google Scholar 

  • Medikayala, S., Piteo, B., Zhao, X., & Edwards, J. G. (2011). Chronically elevated glucose compromises myocardial mitochondrial DNA integrity by alteration of mitochondrial topoisomerase function. American Journal of Physiology. Cell Physiology, 300(2), C338-348. https://doi.org/10.1152/ajpcell.00248.2010

    Article  CAS  Google Scholar 

  • Melekoglu, R., Ciftci, O., Eraslan, S., Cetin, A., & Basak, N. (2018). Beneficial effects of curcumin and capsaicin on cyclophosphamide-induced premature ovarian failure in a rat model. J Ovarian Res., 11(1), 33. https://doi.org/10.1186/s13048-018-0409-9

    Article  CAS  Google Scholar 

  • Melkonian, S. C., Wang, X., Gu, J., Matin, S. F., Tannir, N. M., Wood, C. G., & Wu, X. (2015). Mitochondrial DNA copy number in peripheral blood leukocytes and the risk of clear cell renal cell carcinoma. Carcinogenesis, 36(2), 249–255. https://doi.org/10.1093/carcin/bgu248

    Article  CAS  Google Scholar 

  • Meng, X., Wang, J., Liu, Y., Li, M., Guan, Z., Sowanoua, A., Yang, D., Pei, J., & Gao, Y. (2023). Relatively low fluoride in drinking water increases risk of knee osteoarthritis (KOA): A population-based cross-sectional study in China. Environmental Geochemistry and Health, 45(11), 8735–8747. https://doi.org/10.1007/s10653-023-01742-1

    Article  CAS  Google Scholar 

  • Mondal, D., Dutta, G., & Gupta, S. (2016). Inferring the fluoride hydrogeochemistry and effect of consuming fluoride-contaminated drinking water on human health in some endemic areas of Birbhum district, West Bengal. Environmental Geochemistry Health, 38(2), 557–576. https://doi.org/10.1007/s10653-015-9743-7

    Article  CAS  Google Scholar 

  • Mou, Y., Qu, T., Wang, R., Zhang, Y., He, Z., & Gu, S. (2023). The association of high-fluoride and high-iodine combined exposure with dental fluorosis and goiter: A meta-analysis. Environmental Geochemistry and Health, 45(6), 3143–3153. https://doi.org/10.1007/s10653-022-01396-5

    Article  CAS  Google Scholar 

  • Ozgocmen, S., Kaya, H., Fadillioglu, E., & Yilmaz, Z. (2007). Effects of calcitonin, risedronate, and raloxifene on erythrocyte antioxidant enzyme activity, lipid peroxidation, and nitric oxide in postmenopausal osteoporosis. Archives of Medical Research, 38(2), 196–205. https://doi.org/10.1016/j.arcmed.2006.09.010

    Article  CAS  Google Scholar 

  • Phipps, K. R., Orwoll, E. S., & Bevan, L. (1998). The association between water-borne fluoride and bone mineral density in older adults. Journal of Dental Research, 77(9), 1739–1748. https://doi.org/10.1177/00220345980770091001

    Article  CAS  Google Scholar 

  • Pramanik, S., & Saha, D. (2017). The genetic influence in fluorosis. Environmental Toxicology and Pharmacology, 56, 157–162. https://doi.org/10.1016/j.etap.2017.09.008

    Article  CAS  Google Scholar 

  • Qi, J. Y., Yang, Y. K., Jiang, C., Zhao, Y., Wu, Y. C., Han, X., Jing, X., Wu, Z. L., & Chu, L. (2022). Exploring the Mechanism of Danshensu in the treatment of doxorubicin-induced cardiotoxicity based on network pharmacology and experimental evaluation. Front Cardiovasc Med., 9, 827975. https://doi.org/10.3389/fcvm.2022.827975

    Article  CAS  Google Scholar 

  • Qian, H., Li, G., He, Q., Zhang, H., & Xu, A. (2016). Analysis of differentially expressed genes between fluoride-sensitive and fluoride-endurable individuals in midgut of silkworm. Bombyx Mori. Gene., 588(1), 47–53. https://doi.org/10.1016/j.gene.2016.04.033

    Article  CAS  Google Scholar 

  • Qiao, L., Liu, X., He, Y., Zhang, J., Huang, H., Bian, W., Chilufya, M. M., Zhao, Y., & Han, J. (2021). Progress of signaling pathways, stress pathways and epigenetics in the pathogenesis of skeletal fluorosis. International Journal of Molecular Sciences, 22(21), 11932. https://doi.org/10.3390/ijms222111932

    Article  CAS  Google Scholar 

  • Qin, M., Gao, Y., Zhang, M., Wu, J., Liu, Y., Jiang, Y., Zhang, X., Wang, X., Yang, Y., & Gao, Y. (2023). Association between ADAMTS14_rs4747096 gene polymorphism and bone mineral density of Chinese Han population residing in fluorine exposed areas in ShanXi Province, China. Environmental Science and Pollution Research, 30(48), 106059–106067. https://doi.org/10.1007/s11356-023-29698-w

    Article  CAS  Google Scholar 

  • Richter, C., Park, J. W., & Ames, B. N. (1988). Normal oxidative damage to mitochondrial and nuclear-DNA is extensive. Proceedings of the National Academy of Sciences of the United States of America., 85(17), 6465–6467. https://doi.org/10.1073/pnas.85.17.6465

    Article  CAS  Google Scholar 

  • Shahriarpour, Z., Nasrabadi, B., Hejri-Zarifi, S., Shariati-Bafghi, S. E., Yousefian-Sanny, M., Karamati, M., & Rashidkhani, B. (2021). Oxidative balance score and risk of osteoporosis among postmenopausal Iranian women. Archives of Osteoporosis, 16(1), 43. https://doi.org/10.1007/s11657-021-00886-w

    Article  Google Scholar 

  • Solanki, Y. S., Agarwal, M., Gupta, A. B., Gupta, S., & Shukla, P. (2022). Fluoride occurrences, health problems, detection, and remediation methods for drinking water: A comprehensive review. Science of the Total Environment, 807(Pt 1), 150601. https://doi.org/10.1016/j.scitotenv.2021.150601

    Article  CAS  Google Scholar 

  • Stewart, J. B., & Chinnery, P. F. (2015). The dynamics of mitochondrial DNA heteroplasmy: Implications for human health and disease. Nature Reviews Genetics, 16(9), 530–542. https://doi.org/10.1038/nrg3966

    Article  CAS  Google Scholar 

  • Sun, Z., Li, S., Yu, Y., Chen, H., Ommati, M. M., Manthari, R. K., Niu, R., & Wang, J. (2018). Alterations in epididymal proteomics and antioxidant activity of mice exposed to fluoride. Archives of Toxicology, 92(1), 169–180. https://doi.org/10.1007/s00204-017-2054-2

    Article  CAS  Google Scholar 

  • Tang, P., Liao, Q., Huang, H., Chen, Q., Liang, J., Tang, Y., Zhou, Y., Zeng, X., & Qiu, X. (2023). Effects of urinary barium exposure on bone mineral density in general population. Environmental Science and Pollution Research International, 30(48), 106038–106046. https://doi.org/10.1007/s11356-023-29791-0

    Article  CAS  Google Scholar 

  • Tian, Z. Y., Chen, J. W., Zhou, G. Y., Li, P., Zhao, Q., Luo, C., Zhang, S., & Wang, A. G. (2018). The effects of resveratrol on mitochondrial biogenesis dysfunction induced by fluoride in human neuroblastoma SH-SY5Y cells. Zhonghua Lao Dong Wei Sheng Zhi Ye Bing Za Zhi, 36(10), 721–727. https://doi.org/10.3760/cma.j.issn.1001-9391.2018.10.001

    Article  CAS  Google Scholar 

  • Wallace, D. C. (2005). The mitochondrial genome in human adaptive radiation and disease: On the road to therapeutics and performance enhancement. Gene, 354, 169–180. https://doi.org/10.1016/j.gene.2005.05.001

    Article  CAS  Google Scholar 

  • Wang, H., Chen, H., Han, S., Fu, Y., Tian, Y., Liu, Y., Wang, A., Hou, H., & Hu, Q. (2021). Decreased mitochondrial DNA copy number in nerve cells and the hippocampus during nicotine exposure is mediated by autophagy. Ecotoxicology and Environmental Safety, 226, 112831. https://doi.org/10.1016/j.ecoenv.2021.112831

    Article  CAS  Google Scholar 

  • Wang, H., Fu, M., Ma, Y., Liu, C., Wu, M., & Nie, J. (2022a). Tobacco smoke exposure and mitochondrial DNA copy number on neurobehavioural performance: A community study. Environmental Science and Pollution Research International, 29(56), 84180–84190. https://doi.org/10.1007/s11356-022-20921-8

    Article  CAS  Google Scholar 

  • Wang, J., Yang, J., Cheng, X., Xiao, R., Zhao, Y., Xu, H., Zhu, Y., Yan, Z., Ommati, M. M., Manthari, R. K., & Wang, J. (2019). Calcium alleviates fluoride-induced bone damage by inhibiting endoplasmic reticulum stress and mitochondrial dysfunction. Journal of Agriculture and Food Chemistry, 67(39), 10832–10843. https://doi.org/10.1021/acs.jafc.9b04295

    Article  CAS  Google Scholar 

  • Wang, M., Wang, X., Cui, W., Zhu, G., Liang, Y., Chen, X., & Jin, T. (2022b). The association between hemoglobin level and osteoporosis in a Chinese population with environmental lead and cadmium exposure. Environmental Geochemistry and Health, 44(6), 1673–1682. https://doi.org/10.1007/s10653-021-01129-0

    Article  CAS  Google Scholar 

  • Wang, Y. W., Yang, K., Tang, H., Chen, D., & Bai, Y. L. (2014). Toxicity assessment of repeated intravenous injections of arginine-glycine-aspartic acid peptide conjugated CdSeTe/ZnS quantum dots in mice. International Journal of Nanomedicine, 9, 4809–4817. https://doi.org/10.2147/IJN.S70092

    Article  CAS  Google Scholar 

  • Wang, Y., Yin, Y., Gilula, L. A., & Wilson, A. J. (1994). Endemic fluorosis of the skeleton: Radiographic features in 127 patients. AJR American Journal of Roentgenology, 162(1), 93–98. https://doi.org/10.2214/ajr.162.1.8273699

    Article  CAS  Google Scholar 

  • Wongchitrat, P., Shukla, M., Sharma, R., Govitrapong, P., & Reiter, R. J. (2021). Role of melatonin on virus-induced neuropathogenesis-a concomitant therapeutic strategy to understand SARS-CoV-2 infection. Antioxidants (basel), 10(1), 47. https://doi.org/10.3390/antiox10010047

    Article  CAS  Google Scholar 

  • Xin, J., Zhu, B., Wang, H., Zhang, Y., Sun, N., Cao, X., Zheng, L., Zhou, Y., Fang, J., Jing, B., Pan, K., Zeng, Y., Zeng, D., Li, F., Xia, Y., Xu, P., & Ni, X. (2023). Prolonged fluoride exposure induces spatial-memory deficit and hippocampal dysfunction by inhibiting small heat shock protein 22 in mice. Journal of Hazardous Materials, 456, 131595. https://doi.org/10.1016/j.jhazmat.2023.131595

    Article  CAS  Google Scholar 

  • Xue, S., Kemal, O., Lu, M., Lix, L. M., Leslie, W. D., & Yang, S. (2020). Age at attainment of peak bone mineral density and its associated factors: The national health and nutrition examination survey 2005–2014. Bone, 131, 115163. https://doi.org/10.1016/j.bone.2019.115163

    Article  Google Scholar 

  • Yang, J., Zhu, Y., Zhang, D., Yan, Z., Zhao, Y., Manthari, R. K., Cheng, X., Wang, J., & Wang, J. (2021). Effects of different doses of calcium on the mitochondrial apoptotic pathway and Rho/ROCK signaling pathway in the bone of fluorosis rats. Biological Trace Element Research, 199(5), 1919–1928. https://doi.org/10.1007/s12011-020-02305-6

    Article  CAS  Google Scholar 

  • Yu, F. F., Zuo, J., Fu, X., Gao, M. H., Sun, L., Yu, S. Y., Li, Z., Zhou, G. Y., & Ba, Y. (2021). Role of the hippo signaling pathway in the extracellular matrix degradation of chondrocytes induced by fluoride exposure. Ecotoxicology and Environmental Safety, 225, 112796. https://doi.org/10.1016/j.ecoenv.2021.112796

    Article  CAS  Google Scholar 

  • Yuan, S., Yang, Y., Li, J., Tan, X., Cao, Y., Li, S., Hong, H. D., Liu, L., & Zhang, Q. (2020). Ganoderma lucidum Rhodiola compound preparation prevent D-galactose-induced immune impairment and oxidative stress in aging rat model. Science and Reports, 10(1), 19244. https://doi.org/10.1038/s41598-020-76249-1

    Article  CAS  Google Scholar 

  • Zhang, C., Li, H., Li, J., Hu, J., Yang, K., & Tao, L. (2023a). Oxidative stress: A common pathological state in a high-risk population for osteoporosis. Biomedicine & Pharmacotherapy, 163, 114834. https://doi.org/10.1016/j.biopha.2023.114834

    Article  CAS  Google Scholar 

  • Zhang, Y., Dong, F., Wang, Z., Xu, B., Zhang, T., Wang, Q., & Lin, Q. (2023b). Fluoride exposure provokes mitochondria-mediated apoptosis and increases mitophagy in osteocytes via increasing ROS production. Biological Trace Element Research, 201(8), 3994–4007. https://doi.org/10.1007/s12011-022-03450-w

    Article  CAS  Google Scholar 

  • Zhang, Y., Liu, Y., Hou, M., Xia, X., Liu, J., Xu, Y., Shi, Q., Zhang, Z., Wang, L., Shen, Y., Yang, H., He, F., & Zhu, X. (2023c). Reprogramming of mitochondrial respiratory chain complex by targeting SIRT3-COX4I2 axis attenuates osteoarthritis progression. Adv Sci (weinh)., 10(10), e2206144. https://doi.org/10.1002/advs.202206144

    Article  CAS  Google Scholar 

  • Zhou, G., Yang, L., Luo, C., Liu, H., Li, P., Cui, Y., Liu, L., Yu, X., Zeng, Q., Chen, J., Zhao, Q., Dong, L., Niu, Q., Zhang, S., & Wang, A. (2019). Low-to-moderate fluoride exposure, relative mitochondrial DNA levels, and dental fluorosis in Chinese children. Environment International, 127, 70–77. https://doi.org/10.1016/j.envint.2019.03.033

    Article  CAS  Google Scholar 

  • Zhou, G., Zhao, Q., Luo, C., Liu, H., Li, P., Cui, Y., Yu, X., Chen, J., Liu, L., Zhang, S., & Wang, A. (2021). Low-moderate fluoride exposure and intelligence among Chinese school-aged children: Role of circulating mtDNA content. Science of the Total Environment. https://doi.org/10.1016/j.scitotenv.2021.147330

    Article  Google Scholar 

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Acknowledgements

We thank all the staff and volunteers involved in this study.

Funding

This study was supported by the National Natural Science Foundation of China (81972981, 82003401).

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Authors and Affiliations

  1. Department of Occupational and Environmental Health, School of Public Health, Zhengzhou University, Zhengzhou, 450001, Henan, China

    Yue Ba, Zichen Feng, Yuhui Du, Xiaoxue Liu, Hui Huang, Fangfang Yu & Guoyu Zhou

  2. Yellow River Institute for Ecological Protection & Regional Coordinated Development, Zhengzhou University, Zhengzhou, 450001, Henan, China

    Yue Ba, Fangfang Yu & Guoyu Zhou

  3. Department of Health Management, School of Public Health, Zhengzhou University, Zhengzhou, 450001, Henan, China

    Xiaoli Fu

  4. Department of Epidemiology, Jinshui District Center for Disease Control and Prevention, Zhengzhou, 450053, Henan, China

    Ruiqin Chen

  5. Department of Epidemic Prevention and Control, Puyang Center for Disease Control and Prevention, Puyang, 457001, Henan, China

    Xuecheng Jiao

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  1. Yue Ba
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Contributions

All authors contributed to the study conception and design. YB and GZ collected data, reviewed the manuscript, and provided the funding. ZF analyzed the data and was a major contributor in writing the manuscript. XF, RC, XJ, and XL were responsible for validation and manuscript review. YD, HH, and FY provided software or experimental support. All authors read and approved the final manuscript.

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Correspondence to Guoyu Zhou.

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Ba, Y., Feng, Z., Fu, X. et al. Mediation of mitochondrial DNA copy number and oxidative stress in fluoride-related bone mineral density alteration in Chinese farmers. Environ Geochem Health 46, 184 (2024). https://doi.org/10.1007/s10653-024-01970-z

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  • DOI: https://doi.org/10.1007/s10653-024-01970-z

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