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Effects of Cadmium on Kidney Function of the Freshwater Turtles Mauremys reevesii

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Abstract

This research studied the effects of cadmium on kidney function of the freshwater turtles Mauremys reevesii. Turtles were injected intraperitoneally with 0, 7.5, 15, and 30 mg kg−1 cadmium separately for once. The samples were gathered to check the kidney index, the contents of TP in kidney tissue, and the levels of CRE and BUN in the plasma of the turtles. Results showed that the concentration of TP was overall decreased with the extension of cadmium exposure time and the increasing of the exposure dose of cadmium. The CRE content in the plasma of each treatment group increased with the prolongation of exposure time in a dose-dependent, and the BUN levels of all poisoned groups showed a trend of increasing. The kidney index of treated turtles increased. In summary, cadmium could induce the increase of turtle kidney index, the content of CRE and BUN in plasma, and the decrease of TP content in the kidney.

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References

  1. Theron AJ, Tintinger GR, Anderson R (2012) Harmful interactions of non-essential heavy metals with cells of the innate immune system. J Clin Toxicol S 3:005. https://doi.org/10.4172/2161-0495.S3-005

    Article  Google Scholar 

  2. Simon O, Ribeyre F, Boudou A (2000) Comparative experimental study of cadmium and methylmercury trophic transfers between the Asiatic clam Corbicula fluminea and the crayfish Astacus astacus. Arch Environ Contam Toxicol 38:317–326

    Article  CAS  PubMed  Google Scholar 

  3. Adel M, Cortés-Gómez AA, Dadar M et al (2017) A comparative study of inorganic elements in the blood of male and female Caspian pond turtles (Mauremys caspica) from the southern basin of the Caspian Sea. Environ Sci Pollut Res 24:24965–24979

    Article  CAS  Google Scholar 

  4. Lídia N, Sílvia SM, Andreia TP et al (2017) Trace elements in loggerhead turtles (Caretta caretta) stranded in mainland Portugal: bioaccumulation and tissue distribution. Chemosphere 179:120–126

    Article  Google Scholar 

  5. Malik RN, Ghaffar B, Hashmi MZ (2013) Trace metals in Ganges soft-shell turtle (Aspideretes gangeticus) from two barrage: Baloki and Rasul, Pakistan. Environ Sci Pollut Res 20:8263–8273

    Article  CAS  Google Scholar 

  6. Manuel EO, Antonio R, Pareja-Carrera J et al (2019) Tools for non-invasive sampling of metal accumulation and its effects in Mediterranean pond turtle populations inhabiting mining areas. Chemosphere 231:194–206

    Article  Google Scholar 

  7. Rodriguez CAB, de Lacerda LD, Bezerra MF et al (2020) Influence of size on total mercury (THg), methyl mercury (MeHg), and stable isotopes of N and C in green turtles (Chelonia mydas) from NE Brazil. Environ Sci Pollut Res 27:20527–20537

    Article  CAS  Google Scholar 

  8. Cortés-Gómez AA, Fuentes-Mascorro G, Romero D (2014) Metals and metalloids in whole blood and tissues of Olive Ridley turtles (Lepidochelys olivacea) from La Escobilla Beach (Oaxaca, Mexico). Mar Pollut Bull 89:367–375

    Article  PubMed  Google Scholar 

  9. Macêdo GRd, Tarantino TB, Barbosa IS et al (2015) Trace elements distribution in hawksbill turtle (Eretmochelys imbricata) and green turtle (Chelonia mydas) tissues on the northern coast of Bahia, Brazil. Mar Pollut Bull 94:284–289

    Article  PubMed  Google Scholar 

  10. Storelli MM, Barone G, Storelli A et al (2008) Total and subcellular distribution of trace elements (Cd, Cu and Zn) in the liver and kidney of green turtles (Chelonia mydas) from the Mediterranean Sea. Chemosphere 70(5):908–913

    Article  CAS  PubMed  Google Scholar 

  11. Dieter IMDC, Jana A, Stephen G, Colin RJ, John KC, Joseph RS, Karel ACDS (2014) Genome-wide transcription profiles reveal genotype-dependent responses of biological pathways and gene families in Daphnia exposed to single and mixed stressors. Environ Sci Technol 48:3513–3522

    Article  Google Scholar 

  12. Helen CP, Nadine ST, Joshua H, Kimberly C, Sarah C, Candace C, Leona S, Alexandre VL, Chris V, Mark RV (2011) Metabolomics of microliter hemolymph samples enables an improved understanding of the combined metabolic and transcriptional responses of Daphnia magna to cadmium. Environ Sci Technol 45:3710–3717

    Article  Google Scholar 

  13. Järup L, Berglund M, Elinder CG, Nordberg G, Vahter M (1998) Health effects of cadmium exposure—a review of the literature and a risk estimate. Scand J Work Environ Health 24:1–51

    PubMed  Google Scholar 

  14. Mehinto AC, Prucha MS, Colli-Dula RC, Kroll KJ, Lavelle CM, Barber DS, Vulpe CD, Denslow ND (2014) Gene networks and toxicity pathways induced by acute cadmium exposure in adult largemouth bass (Micropterus salmoides). Aquat Toxicol 152:186–194

    Article  CAS  PubMed  Google Scholar 

  15. Novelli F, Novelli E, Manzano MA, Lopes AM, Cataneo AC, Barbosa LL, Ribas BO (2000) Effect of alpha-tocopherol on superoxide radical and toxicity of cadmium exposure. Int J Environ Health Res 10:125–134

    Article  Google Scholar 

  16. Pacyna JM, Pacyna EG, Aas W (2009) Changes of emissions and atmospheric deposition of mercury, lead, and cadmium. Atmos Environ 43:117–127

    Article  CAS  Google Scholar 

  17. Pirrone N, Cinnirella S, Feng X, Finkelman RB, Friedll HR (2010) Global mercury emissions to the atmosphere from anthropogenic and natural sources. Atmos Chem Phys 10:4719–4752

    Article  Google Scholar 

  18. Han T, Wang Q, Wang L (2008) Ecological investigation of freshwater crab and river pollution in basin of Qinhe River. Sichuan J Zool 27:804–806

    Google Scholar 

  19. Zhao CD, Chen FR, Chen XR, Zhao HC, XiaWL NHF, Kong M, Liu F, Yang K (2008) A methodology of tracking sources of cadmium anomalies and their quantitative estimation in the Yangtze River basin. Earth Sci Front 15:179–193

    Article  CAS  Google Scholar 

  20. Cheng HX, Zhao CD, Zhuang GM, Xia WL, Liu YH, Yang K, Nie HF (2008) Reconstruction of the regional soil pollution history by heavy metals in Taihu lake drainage area: taking Pb and Cd as examples. Earth Sci Front 5:167–178

    Google Scholar 

  21. Fordhama DF, Georges A, Corey B (2007) Optimal conditions for egg storage, incubation and post-hatching growth for the freshwater turtle, Chelodina rugosa: science in support of an indigenous enterprise. Aquaculture 270:105–114

    Article  Google Scholar 

  22. Mutalib AHA, Fadzly N, Foo R (2013) Striking a balance between tradition and conservation: general perceptions and awareness level of local citizens regarding turtle conservation efforts based on age factors and gender. Ocean Coast Manag 78:56–63

    Article  Google Scholar 

  23. Xu CX, Xu W, Lu HL (2014) Compensatory growth responses to food restriction in the Chinese three-keeled pond turtle, Chinemys reevesii. SpringerPlus 3:687

    Article  PubMed  PubMed Central  Google Scholar 

  24. Tada N, Saka M, Ueda Y et al (2004) Comparative analyses of serum vitellogenin levels in male and female Reeves’ pond turtles (Chinemys reevesii Gray) by an immunological assay. J Comp Physiol B 174:13–20

    Article  CAS  PubMed  Google Scholar 

  25. Dayna L, Smith MJ, Cooper JM et al (2016) Body burdens of heavy metals in Lake Michigan wetland turtles. Environ Monit Assess 188:128

    Article  Google Scholar 

  26. Elodie G, Krishna D (2012) Cadmium toxicokinetics and bioaccumulation in turtles, trophic exposure of Trachemys scripta elegans. Ecotoxicology 21(1):18–26

    Article  Google Scholar 

  27. Dong AG, Huo JF, Yan JJ et al (2021) Lipid peroxidation of kidney of the turtle Mauremys reevesii caused by cadmium. Environ Sci Pollut Res 28:6811–6817

    Article  CAS  Google Scholar 

  28. Dong AG, Huo JF, Yan JJ et al (2021) Oxidative stress in liver of turtle Mauremys reevesii caused by cadmium. Environ Sci Pollut Res 28:6405–6410

    Article  CAS  Google Scholar 

  29. Huo JF, Dong AG, Niu XJ et al (2018) Effects of cadmium on oxidative stress activities in plasma of freshwater turtle Chinemys reevesii. Environ Sci Pollut Res 25:8027–8034

    Article  CAS  Google Scholar 

  30. Huo JF, Dong AG, Wang YH et al (2017) Cadmium induces histopathological injuries and ultrastructural changes in the liver of freshwater turtle (Chinemys reevesii). Chemosphere 186:459–465

    Article  CAS  PubMed  Google Scholar 

  31. Huo JF, Dong AG, Yan JJ et al (2020) Effects of cadmium on the activities of ALT and AST as well as the content of TP in plasma of freshwater turtle Mauremys reevesii. Environ Sci Pollut Res 27:18025–18028

    Article  CAS  Google Scholar 

  32. Huo JF, Dong AG, Yan JJ et al (2020) Effects of cadmium on the gene transcription of the liver in the freshwater turtle (Chinemys reevesii). Environ Sci Pollut Res 27:8431–8438

    Article  CAS  Google Scholar 

  33. Huo JF, Dong AG, Yan JJ et al (2017) Cadmium toxicokinetics in the freshwater turtle, Chinemys reevesii. Chemosphere 182:392–398

    Article  CAS  PubMed  Google Scholar 

  34. Yu S, Halbrook RS, Sparling DW (2013) Correlation between heavy metals and turtle abundance in ponds near the Paducah Gaseous Diffusion Plant, Kentucky, USA. Arch Environ Contam Toxicol 65:555–566

    Article  CAS  PubMed  Google Scholar 

  35. Wei YH, Li L, Cao YG et al (2005) Study on relationship between renal injury induced by cadmium and acute renal failure. J Environ Health 22(1):16–18

    Google Scholar 

  36. Aldulaimi (2019) Effect of aqueous extract Cyperus rotundus tubers as antioxidant on liver and kidney functions in albino males rats exposed to cadmium chloride toxic. Baghdad Sci J. https://doi.org/10.21123/bsj.16.2.0315

    Article  Google Scholar 

  37. Salam BA, Joshi H, Gururaja MP (2018) Protective effect of Ixora coccinea flowers against cadmium chloride induced nephrotoxicity model in rats. Res J Pharmacy Technol. https://doi.org/10.5958/0974-360X.2018.00901.0

    Article  Google Scholar 

  38. Lian XL, Lian WF (2000) Effect of molybdenum on renal injury in rats with subacute cadmium poisoning. Industr Health Occupat Diseases 26(3):177–178

    Google Scholar 

  39. Salama SA, AbdAllah GM, Gad HS et al (2022) Galangin attenuates cadmium-evoked nephrotoxicity: targeting nucleotide-binding domain-like receptor pyrin domain containing 3 inflammasome, nuclear factor erythroid 2-related factor 2, and nuclear factor kappa B signaling. J Biochem Mol Toxic. https://doi.org/10.1002/JBT.23059

    Article  Google Scholar 

  40. Arab HH, Ashour AM, Eid AH et al (2022) Targeting oxidative stress, apoptosis, and autophagy by galangin mitigates cadmium-induced renal damage: role of SIRT1/Nrf2 and AMPK/mTOR pathways. Life Sci. https://doi.org/10.1016/J.LFS.2021.120300

    Article  PubMed  Google Scholar 

  41. Salama SA, Mohamadin AM, Abdel-Bakky MS (2021) Arctigenin alleviates cadmium-induced nephrotoxicity: targeting endoplasmic reticulum stress, Nrf2 signaling, and the associated inflammatory response. Life Sci. https://doi.org/10.1016/J.LFS.2021.120121

    Article  PubMed  Google Scholar 

  42. Fang J, Xie SL, Chen Z et al (2021) Protective effect of vitamin E on cadmium-induced renal oxidative damage and apoptosis in rats. Biol Trace Elem Res. https://doi.org/10.1007/S12011-021-02606-4

    Article  PubMed  PubMed Central  Google Scholar 

  43. Fan RF, Li ZF, Zhang D et al (2020) Involvement of Nrf2 and mitochondrial apoptotic signaling in trehalose protection against cadmium-induced kidney injury. Metallomics. https://doi.org/10.1039/D0MT00213E

    Article  PubMed  Google Scholar 

  44. Riaz MA, Nisa ZU, Mehmood A et al (2019) Metal-induced nephrotoxicity to diabetic and non-diabetic Wistar rats. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-019-06022-z

    Article  Google Scholar 

  45. Liu QL, Zhang RQ, Wang X et al (2019) Effects of sub-chronic, low-dose cadmium exposure on kidney damage and potential mechanisms. Ann Transl Med. https://doi.org/10.21037/atm.2019.03.66

    Article  PubMed  PubMed Central  Google Scholar 

  46. Golbaghi A, Fouladi DB, Ahmadizadeh M (2019) Combined effect of cadmium and noise on rat’s kidney. J Renal Inj Prev. https://doi.org/10.15171/jrip.2019.43

    Article  Google Scholar 

  47. Mohammad H, Baby T, Elsayed FAA et al (2018) Bioremediation of cadmium induced renal toxicity in Rattus norvegicus by medicinal plant Catharanthus roseus. Saudi J Biol Sci. https://doi.org/10.1016/j.sjbs.2018.09.009

    Article  PubMed  Google Scholar 

  48. Kyeong SK, Hyun-Jung L, Jong SL et al (2018) Curcumin ameliorates cadmium-induced nephrotoxicity in Sprague-Dawley rats. Food Chem Toxicol. https://doi.org/10.1016/j.fct.2018.02.007

    Article  Google Scholar 

  49. Mohamed AOS, Elshaer SS, Anwar HM et al (2017) Relevance of cystatin-C, N-acetylglucosaminidase, and interleukin-18 with the diagnosis of acute kidney injury induced by cadmium in rats. J Biochem Mol Toxic. https://doi.org/10.1002/jbt.21968

    Article  Google Scholar 

  50. Jafarpour D, Shekarforoush SS, Ghaisari HR et al (2017) Protective effects of synbiotic diets of Bacillus coagulans, Lactobacillus plantarum and inulin against acute cadmium toxicity in rats. BMC Complement Altern Med. https://doi.org/10.1186/s12906-017-1803-3

  51. Chen JL, Du LF, Li JJ et al (2016) Epigallocatechin-3-gallate attenuates cadmium-induced chronic renal injury and fibrosis. Food Chem Toxicol. https://doi.org/10.1016/j.fct.2016.07.030

    Article  PubMed  PubMed Central  Google Scholar 

  52. Neelamegam K, Natarajan A (2014) Protective effect of bioflavonoid myricetin enhances carbohydrate metabolic enzymes and insulin signaling molecules in streptozotocin–cadmium induced diabetic nephrotoxic rats. Toxicol Appl Pharma. https://doi.org/10.1016/j.taap.2014.05.014

    Article  Google Scholar 

  53. Hanan H, Waleed AM (2014) Betaine supplementation protects against renal injury induced by cadmium intoxication in rats: role of oxidative stress and caspase-3. Environ Toxicol Phar. https://doi.org/10.1016/j.etap.2014.02.013

    Article  Google Scholar 

  54. Morshedi A, Ahmadi A (2014) Protective effects of zinc supplementation on renal toxicity in rats exposed to cadmium. Jundishapur J Health Sci. https://doi.org/10.5812/jjhs.21717

    Article  Google Scholar 

  55. Lu Q, Lei YX, He CC et al (2013) Blood translation elongation factor-1δ is a novel marker for cadmium exposure. IJMS. https://doi.org/10.3390/ijms14035182

    Article  PubMed  PubMed Central  Google Scholar 

  56. Kara H, Karatas F, Canatan H et al (2005) Effects of exogenous metallothionein on acute cadmium toxicity in rats. Biol trace elem res 104(3):223–232

    Article  CAS  PubMed  Google Scholar 

  57. Huang J, Ma XT, Xu DD et al (2021) Xianling Gubao Capsule prevents cadmium-induced kidney injury. BioMed Res Int. https://doi.org/10.1155/2021/3931750

    Article  PubMed  PubMed Central  Google Scholar 

  58. Zhu MK, Zhou WT, Bai LH et al (2019) Dietary cadmium chloride supplementation impairs renal function and bone metabolism of laying hens. Animals. https://doi.org/10.3390/ani9110998

    Article  PubMed  PubMed Central  Google Scholar 

  59. Omid K, Saeed H, Seyyed PM (2017) Histological and functional alteration in the liver and kidney and the response of antioxidants in Japanese quail exposed to dietary cadmium. Iranian J Toxic 11(3):19–26

    Article  Google Scholar 

  60. Okoroiwu HU, Uchendu IK (2020) Seed protects against cadmium-induced renal toxicity in rats. Current Chem Biol 14(2):140–149

    Article  Google Scholar 

  61. Kini RD, Arunkumar N, Shetty BS et al (2019) Potential protective role of beta carotene on cadmium induced brain and kidney damage. Indian J Public Health Res Develop. https://doi.org/10.5958/0976-5506.2019.02484.7

    Article  Google Scholar 

  62. Wang JC, Zhu HL, Zhang C et al (2019) Puerarin protects rat liver and kidney against cadmium-induced oxidative stress. Indian J Anim Sci 89:927–931

    Article  CAS  Google Scholar 

  63. Wang JC, Zhu HL, Zhang C et al (2018) Baicalein ameliorates cadmium-induced hepatic and renal oxidative damage in rats. Indian J Anim Res. https://doi.org/10.18805/IJAR.B-853

    Article  Google Scholar 

  64. Lee YK, Park EY, Kim S et al (2014) Evaluation of cadmium-induced nephrotoxicity using urinary metabolomic profiles in Sprague-Dawley male rats. J Toxicol Environ Health A. https://doi.org/10.1080/15287394.2014.951755

    Article  PubMed  Google Scholar 

  65. Zhou L, Kai SB, Xiao HC (2014) Ligustrazine attenuates elevated levels of indoxyl sulfate, kidney injury molecule-1 and clusterin in rats exposed to cadmium. Food Chem Toxicol. https://doi.org/10.1016/j.fct.2013.10.038

    Article  PubMed  Google Scholar 

  66. Yang HY, Xing RG, Liu S et al (2021) Role of fucoxanthin towards cadmium-induced renal impairment with the antioxidant and anti-lipid peroxide activities. Bioengineered. https://doi.org/10.1080/21655979.2021.1973875

    Article  PubMed  PubMed Central  Google Scholar 

  67. Chen CJ, Han X, Wang G et al (2021) Nrf2 deficiency aggravates the kidney injury induced by subacute cadmium exposure in mice. Arch Toxicol. https://doi.org/10.1007/S00204-020-02964-3

    Article  PubMed  PubMed Central  Google Scholar 

  68. Fan R, Hu PC, Wang Y et al (2018) Betulinic acid protects mice from cadmium chloride-induced toxicity by inhibiting cadmium-induced apoptosis in kidney and liver. Toxicol Lett. https://doi.org/10.1016/j.toxlet.2018.09.003

    Article  PubMed  PubMed Central  Google Scholar 

  69. Peng SX, Lu TJ, Liu YS et al (2022) Short-term exposure to fine particulate matter and its constituents may affect renal function via oxidative stress: a longitudinal panel study. Chemosphere. https://doi.org/10.1016/J.Chemosphere.2022.133570

    Article  PubMed  PubMed Central  Google Scholar 

  70. RodríguezLópez E, TamayoOrtiz M, Ariza AC et al (2020) Early-life dietary cadmium exposure and kidney function in 9-year-old children from the PROGRESS cohort. Toxics. https://doi.org/10.3390/toxics8040083

    Article  PubMed  Google Scholar 

  71. Pollack AZ, Mumford SL, Mendola P et al (2015) Kidney biomarkers associated with blood lead, mercury, and cadmium in premenopausal women: a prospective cohort study. J Toxicol Environ Health A. https://doi.org/10.1080/15287394.2014.944680

    Article  PubMed  PubMed Central  Google Scholar 

  72. Dong AG, Huo JF, Ma JF (2010) Therapeutical effect of hydrophilic polysaccharides extracted from Agaricus Blazei Murrill on mice with cadmium poisoning. J Tradit Chinese Vet Med 29(3):5–7

    CAS  Google Scholar 

  73. Xu YL, Du HY, Jin MH et al (2011) Inhibitory effects of cadmium chloride on SMMC-7721 cells in hepatocarcinoma transplanted nude mice and influence in mitochondrial enzymes. J Jilin University (Medicine Edition) 37(1):56–60

    CAS  Google Scholar 

  74. Huang F, Liu WH, Wu Y et al (2018) Chlorogenic acid attenuates cadmium-induced intestinal injury in rats. Food Sci 39(17):187–191

    Google Scholar 

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Funding

This study was funded by Science and Technology Innovation Project of Colleges and Universities in Shanxi Province (grant numbers 2020L0458, 2020L0460) and Health Commission of Shanxi Province (grant number 201601103).

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Authors and Affiliations

  1. Shanxi University of Chinese Medicine, Taiyuan, Shanxi Province, China

    Aiguo Dong, Huidong Dong, Hui He, Juanjuan Yan & Junfeng Huo

  2. Bureau of Agriculture and Rural Affairs of Qianan, Tangshan, Hebei Province, China

    Ailing Dong

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  4. Ailing Dong
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Contributions

AD and JH designed the study, performed the research, analyzed the data, and wrote the paper. HD, HH, AD, and JY were major contributors in writing the manuscript. All authors read and approved the final manuscript.

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Correspondence to Junfeng Huo.

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This study was approved by Shanxi University of Chinese Medicine (permit number: 2018LL054).

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Aiguo Dong and Junfeng Huo: joint first co-authorship. The authors contributed equally to this work.

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Dong, A., Dong, H., He, H. et al. Effects of Cadmium on Kidney Function of the Freshwater Turtles Mauremys reevesii. Biol Trace Elem Res 201, 3000–3005 (2023). https://doi.org/10.1007/s12011-022-03397-y

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