Skip to main content

Advertisement

Log in

Alternations of Fertility Parameters by Graded Dose of Inorganic Arsenic in Adult Male White Pekin Ducks

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

Abstract

A significant health issue, reproductive toxicity is mostly linked to exposure to various environmental heavy metals. A pervasive toxin that occurs naturally in the environment is arsenic (As). This research was done to determine the effects of various doses of inorganic As supplements on the reproductive organs of adult male white Pekin ducks. A total of 240 numbers of 14-days-old male white Pekin ducks were weighed and randomly assigned into 4 experimental groups with six replicates (10 ducklings in each replicate). The experimental groups were as follows: (T-1) basal diet along with normal drinking water (control group); (T-2 to T-4) basal diet along with As in the form of sodium-meta-arsenite at 7, 14, and 28 ppm of drinking water respectively. The results showed reduction in body weight and testicular weight, disruption of spermatogenesis, reduction in follicular-stimulating hormone (FSH), leutinizing hormone (LH), and testosterone levels and histopathological alterations as compared to control. Additionally, there was not only a significant decrease in various antioxidant parameters in testis tissue, like catalase (CAT), reduced glutathione (GSH), super oxide dismutase (SOD), and ferric-reducing antioxidant power (FRAP), but also a significant increase in oxidative parameters of testis like lipid peroxidation (LPO), myloperoxidase (MPO), nitric oxide (NO), and super oxide anion radical (O2) in As-treated groups, in comparison with T-1. A significantly higher level of As content in testis was observed in all the 3 As-treated groups, with highest level recorded in T-4 birds. Besides that, there was upregulation of nuclear factor kappa B (NF-κB), heat shock proteins (Hsps) and pro-inflammatory cytokines like interlukin (IL) series, i.e., IL-2, IL-6, IL-18, IL-1β and tumor necrosis factor- α (TNF-α) levels, whereas anti-inflammatory parameters like IL-4 and IL-10 levels showed downregulation in testis of As-treated groups. Together, these findings provide deeper understandings of the roles played by oxidative stress, NF-κB and Hsps in the progression of testicular injury, which may help to explain how the As induced male sterility, in ducks, due to exposure.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Chart 1
Chart 2
Chart 3
Chart 4
Fig. 1
Fig. 2
Fig. 3
Fig. 4
Chart 5

Similar content being viewed by others

Data Availability

The data used to support the findings are all included in the article.

References

  1. Flora SJS, Bhadauria S, Pant SC, Dhaked RK (2005) Arsenic induced blood and brain oxidative stress and its response to some thiol chelators in rats. Life Sci 77(18):2324–2337. https://doi.org/10.1016/j.lfs.2005.04.016

    Article  CAS  PubMed  Google Scholar 

  2. Martinez VD, Vucic EA, Becker-Santos DD, Gil L, Lam WL (2011) Arsenic exposure and the induction of human cancers. J Toxicol 2011:431287. https://doi.org/10.1155/2011/431287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Brandon EF, Janssen PJ, de Wit-Bos L (2014) Arsenic: bioaccessibility from seaweed and rice, dietary exposure calculations and risk assessment. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 31(12):1993–2003. https://doi.org/10.1080/19440049.2014.974687

    Article  CAS  PubMed  Google Scholar 

  4. Bissen MF, Frimmel FH (2003) Arsenic a review, part 1: occurrence, toxicity, speciation, mobility. Acta Hydrochim Hydrobiol 31(1):9–18. https://doi.org/10.1002/aheh.200390025

    Article  CAS  Google Scholar 

  5. Anwar HM, Akai J, Mustafa KM, Saifullah S, Tareq SM (2002) Arsenic poisoning in groundwater: health risk and geochemical sources in Bangladesh. Environ Int 27(7):597–604. https://doi.org/10.1016/S0160-4120(01)00116-7

    Article  Google Scholar 

  6. Hopenhayn-Rich C, Hertz-Picciotto I, Browning S, Ferreccio C, Peralta C (1999) Reproductive and developmental effects associated with chronic arsenic exposure. Ars Expos Hlth Eff 3:151–164. https://doi.org/10.1016/B978-008043648-7/50019-4

    Article  Google Scholar 

  7. Marettová E, Maretta M, Legáth J (2015) Toxic effects of cadmium on testis of birds and mammals: a review. Anim Reprod Sci 155:1–10. https://doi.org/10.1016/j.anireprosci.2015.01.007

    Article  CAS  Google Scholar 

  8. Gaballa A, Newton GL, Antelmann H, Parsonage D, Upton H, Rawat M, Claiborne A, Fahey RC, Helmann JD (2010) Biosynthesis and functions of bacillithiol, a major low-molecular-weight thiol in Bacilli. Proc Natl Acad Sci USA 107(14):6482–6486. https://doi.org/10.1073/pnas.1000928107

    Article  PubMed  PubMed Central  Google Scholar 

  9. White CC, Viernes H, Krejsa CM, Botta D, Kavanagh TJ (2003) Fluorescence-based microtiter plate assay for glutamate-cysteine ligase activity. Anal Biochem 318(2):175–180. https://doi.org/10.1016/s0003-2697(03)00143-x

    Article  CAS  PubMed  Google Scholar 

  10. Gao S, Duan X, Wang X, Dong D, Liu D, Li X, Sun G, Li B (2013) Curcumin attenuates arsenic-induced hepatic injuries and oxidative stress in experimental mice through activation of Nrf2 pathway, promotion of arsenic methylation and urinary excretion. Food Chem Toxicol 59:739–747. https://doi.org/10.1016/j.fct.2013.07.032

    Article  CAS  PubMed  Google Scholar 

  11. Mena S, Ortega A, Estrela JM (2009) Oxidative stress in environmental-induced carcinogenesis. Mutat Res 674(1–2):36–44. https://doi.org/10.1016/j.mrgentox.2008.09.017

    Article  CAS  PubMed  Google Scholar 

  12. Zhao P, Guo Y, Zhang W, Chai H, Xing H, Xing M (2017) Neurotoxicity induced by arsenic in Gallus Gallus: Regulation of oxidative stress and heat shock protein response. Chemosphere 166:238–245. https://doi.org/10.1016/j.chemosphere.2016.09.060

    Article  CAS  PubMed  Google Scholar 

  13. Samuel S, Kathirvel R, Jayavelu T, Chinnakkannu P (2005) Protein oxidative damage in arsenic induced rat brain: influence of DL-alpha-lipoic acid. Toxicol Lett 155(1):27–34. https://doi.org/10.1016/j.toxlet.2004.08.001

    Article  CAS  PubMed  Google Scholar 

  14. Phillips B, Abravaya K, Morimoto RI (1991) Analysis of the specificity and mechanism of transcriptional activation of the human hsp70 gene during infection by DNA viruses. J Virol 65(11):5680–5692. https://doi.org/10.1128/jvi.65.11.5680-5692.1991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Hunt C, Morimoto RI (1985) Conserved features of eukaryotic hsp70 genes revealed by comparison with the nucleotide sequence of human hsp70. Proc Natl Acad Sci USA 82(19):6455–6459. https://doi.org/10.1073/pnas.82.19.6455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Kang PJ, Ostermann J, Shilling J, Neupert W, Craig EA, Pfanner N (1990) Requirement for hsp70 in the mitochondrial matrix for translocation and folding of precursor proteins. Nature 348(6297):137–143. https://doi.org/10.1038/348137a0

    Article  CAS  PubMed  Google Scholar 

  17. Neckers L, Ivy SP (2003) Heat shock protein 90. Curr Opin Oncol 15(6):419–424. https://doi.org/10.1097/00001622-200311000-00003

    Article  CAS  PubMed  Google Scholar 

  18. Mehlen P, Schulze-Osthoff K, Arrigo AP (1996) Small stress proteins as novel regulators of apoptosis Heat shock protein 27 blocks Fas/APO-1- and staurosporine-induced cell death. J Biol Chem 271(28):16510–16514. https://doi.org/10.1074/jbc.271.28.16510

    Article  CAS  PubMed  Google Scholar 

  19. Ercal N, Gurer-Orhan H, Aykin-Burns N (2001) Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage. Curr Top Med Chem 1(6):529–539. https://doi.org/10.2174/1568026013394831

    Article  CAS  PubMed  Google Scholar 

  20. Jana K, Jana S, Samanta PK (2006) Effect of chronic exposure to sodium arsenite on hypothalamopituitary- testicular activities in adult rats: possible an estrogenic mode of action. Reprod Biol Endocrinol 4:91–96. https://doi.org/10.1186/2F1477-7827-4-9

    Article  Google Scholar 

  21. Mukherjee S, Mukhopadhyay PK (2009) Studies on arsenic toxicity in male rat gonads and its protection by high dietary protein supplementation. Al Ameen J Med Sci 2:73–77

    CAS  Google Scholar 

  22. Sarkar S, Hazra J, Upadhyay SN, Singh RK, Amal RC (2008) Arsenic induced toxicity on testicular tissue of mice. Indian J Physiol Pharmacol 52(1):84–90

    CAS  Google Scholar 

  23. Rosenblatt AE, Burnstein KL (2009) Inhibition of androgen receptor transcriptional activity as a novel mechanism of action of arsenic. Mol Endocrinol 23(3):412–421. https://doi.org/10.1210/me.2008-0235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Shao YZ, Zhao HJ, Wang Y, Liu JJ, Li JL, Luo LY, Xing MW (2018) The apoptosis in arsenic-induced oxidative stress is associated with autophagy in the testis tissues of chicken. Poult Sci 97(9):3248–3257. https://doi.org/10.3382/ps/pey156

    Article  CAS  PubMed  Google Scholar 

  25. Lin CC, Huang CC, Chen MC, Huang AJF, Chiou HY (2002) Arsenic toxicity on duck spermatozoa and the ameliorating effect of L-ascorbic acid. Asian Australas J Anim Sci 15:19–25

    Article  CAS  Google Scholar 

  26. BIS (2007) Bureau of Indian Standards, Poultry Feeds Specification (5th Revision), Manak Bhavan, 9 Bahadur Shah Zafar Marg, New Deli-110002

  27. Kamar GA (1962) Semen characteristics of various breeds of drakes in the subtropics. J Reprod Fertil 3:405–409. https://doi.org/10.1530/jrf.0.0030405

    Article  CAS  PubMed  Google Scholar 

  28. Taneja GS, Gowe RS (1961) Spermatozoa concentration in the semen of two breeds of fowl estimated by three different methods. Poult Sci 40(3):608–615. https://doi.org/10.3382/ps.0400608

    Article  Google Scholar 

  29. Mamun AM, Bhuiyan MMU, Ferdousy RN, Juyena NS (2013) Evaluation of semen quality among four chicken lines. IOSR-JAVS 6(5):7–13. https://doi.org/10.9790/2380-0650713

    Article  Google Scholar 

  30. Rehman SU (1984) Lead-induced regional lipid peroxidation in brain. Toxicol Lett 21(3):333–337. https://doi.org/10.1016/0378-4274(84)90093-6

    Article  Google Scholar 

  31. Sedlak J, Lindsay RH (1968) Estimation of total, protein bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25:192–205. https://doi.org/10.1016/0003-2697(68)90092-4

    Article  CAS  PubMed  Google Scholar 

  32. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3

    Article  CAS  PubMed  Google Scholar 

  33. Madesh M, Balasubramanian KA (1993) Microtiter plate assay for superoxide dismutase using MTT reduction by superoxide. Indian J Biochem Biophys 35(3):184–188

    Google Scholar 

  34. Grisham MB, Specian RD, Zimmerman TE (1994) Effects of nitric oxide synthase inhibition on the pathophysiology observed in a model of chronic granulomatous colitis. J Pharmacol Exp Ther 271(2):1114–1121

    CAS  PubMed  Google Scholar 

  35. Patriarca P, Dri P, Snidero M (1997) Interference of myeloperoxidase with the estimation of superoxide dismutase activity. J Lab Clin Med 90(2):289–294

    Google Scholar 

  36. Wang HD, Pagano PJ, Du Y, Cayatte AJ, Quinn MT, Brecher P, Cohen RA (1998) Superoxide anion from the adventitia of the rat thoracic aorta inactivates nitric oxide. Circ Res 82(7):810–818. https://doi.org/10.1161/01.RES.82.7.810

    Article  CAS  Google Scholar 

  37. Sastry KV, Moudgal RP, Mohan J, Tyagi JS, Rao GS (2002) Spectrophotometric determination of serum nitrite and nitrate by copper-cadmium alloy. Anal Biochem 306(1):79–82. https://doi.org/10.1006/abio.2002.5676

    Article  CAS  PubMed  Google Scholar 

  38. Hershey JW, Oostdyk TS, Keliher PN (1988) Determination of arsenic and selenium in environmental and agricultural samples by hydride generation atomic absorption spectrophotometry. J Assoc Off Anal Chem 71(6):1090–1093

    CAS  PubMed  Google Scholar 

  39. Dos Passos AS, Neri TS, Maciel MV, da Silva Roma~o IL, Lemos VA (2012) Determination of arsenic in chicken feed by hydride generation atomic absorption spectrometry after preconcentration with polyurethane foam Food Addit Contam. Part A Chem Anal Control Expo Risk Assess 29(11):1689–1695. https://doi.org/10.1080/19440049.2012.706833

    Article  CAS  Google Scholar 

  40. Kalavathi S, Anand KA, Gopala RA, Srilatha Ch, Rajasekhar RA (2011) Sodium arsenite toxicity in broiler chicks and its amelioration: haemato-biochemical and pathological studies. Indian J Vet Pathol 35(2):171–176

    Google Scholar 

  41. Bancroft JD, Gamble M (2007) Theory and practice of histological techniques, 6th edition. Churchill Livingstone, London, UK pp 125–138

  42. Sikandar A, Cheema AH, Younus M, Aslam A, Zaman MA, Rehman T (2012) Histopathological and serological studies on paratuberculosis in cattle and buffaloes. Pak Vet J 32(4):547–551

    Google Scholar 

  43. Panda SK, Kumar D, Jena GR, Sethy K, Mishra SK, Swain BK, Naik PK, Beura CK, Elmorsy MAM (2021) Efficacy of ginger on male reproductive traits and oxidative stress indices in White Pekin ducks intoxicated with arsenic. Anim Nutr Feed Technol 21(3):559–569. https://doi.org/10.5958/0974-181X.2021.00046.9

    Article  Google Scholar 

  44. Panda SK, Kumar D, Jena GR, Patra RC, Panda SK, Sethy K, Mishra SK, Swain BK, Naik PK, Beura CK (2021) Panda S (2021) Ameliorative property of ginger (Zingiber officinale) in minimising immunosuppression induced by arsenic in White Pekin ducks (Anas platyrhynchos). Indian J Poult Sci 56(3):277–285. https://doi.org/10.5958/0974-8180.2021.00037.4

    Article  Google Scholar 

  45. Panda SK, Kumar D, Jena GR, Patra RC, Panda SK, Sethy K, Mishra SK, Swain BK, Naik PK, Beura CK, Panda B (2022) Hepatorenal toxicity of inorganic arsenic in White Pekin ducks and its amelioration by using ginger. Biol Trace Elem Res. https://doi.org/10.1007/s12011-022-03317-0

    Article  PubMed  Google Scholar 

  46. Aman RP (1981) A critical review of methods for evaluation of spermatogenesis from seminal characteristics. J Androl 2(1):37–38. https://doi.org/10.1002/j.1939-4640.1981.tb00595.x

    Article  Google Scholar 

  47. Sarkar M, Chaudhuri GR, Chattopadhyay A, Biswas NM (2003) Effect of sodium arsenite on spermatogenesis, plasma gonadotrophins and testosterone in rats. Asian J Androl 5(1):27–31

    CAS  PubMed  Google Scholar 

  48. Morakinyo AO, Adeniyi OS, Arikawe AP (2008) Effects of Zingiber officinale on reproductive functions in male rats. Afr J Biomed Res 11:329–333

    Google Scholar 

  49. Iwasaki A, Gagnon CF (1992) Formation of reactive oxygen species in spermatozoa of infertile patients. Fertil Steril 57(2):409–416. https://doi.org/10.1016/s0015-0282(16)54855-9

    Article  CAS  PubMed  Google Scholar 

  50. Aitken RJ, Buckinhham D, Harkiss D (1993) Use of xanthine oxidase free radical generating system to investigate the cytotoxic effects of reactive oxygen species on human spermatozoa. J Reprod Fertil 97(2):441–450. https://doi.org/10.1530/jrf.0.0970441

    Article  CAS  Google Scholar 

  51. Ogedengbe OO, Naidu ECS, Akang EN, Offor U, Onanuga IO, Peter AI, Jegede AI, Azu OO (2018) Virgin coconut oil extract mitigates testicular-induced toxicity of alcohol use in antiretroviral therapy. Andrology 6(4):616–626. https://doi.org/10.1111/andr.12490

    Article  CAS  PubMed  Google Scholar 

  52. Ogunlade B, Adelakun SA, Ukwenya VO, Elemosol TT (2021) Potentiating response of D- Ribose-L-Cysteine on Sodium arsenate-induced hormonal imbalance, spermatogenesis impairments and histomorphometric alterations in adult male Wistar rat. JBRA Assist Reprod 25(3):358–367. https://doi.org/10.5935/1518-0557.20200109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Sharpe RM, Donachie K, Cooper I (1988) Reevaluation of the intratesticular level of testosterone required for quantitative maintenance of spermatogenesis in the rat. J Endocrinol 117(1):19–26. https://doi.org/10.1677/joe.0.1170019

    Article  CAS  PubMed  Google Scholar 

  54. Sharpe RM, Maddocks S, Millar M, Saunders PTK, Kerr JB, Mckinnell C (1992) Testosterone and spermatogenesis: identification of stage dependent, androgen regulated proteins secreted by adult rat seminiferous tubules. J Androl 13(2):172–184

    CAS  PubMed  Google Scholar 

  55. Penfold LM, Wildt DE, Herzog TL, Lynch W, Ware L, Derrickson SE, Monfort SL (2000) Seasonal patterns of LH, testosterone and semen quality in the Northern pintail duck (Anas acuta). Reprod Fértil Dev 12(3–4):229–235. https://doi.org/10.1071/rd00093

    Article  CAS  PubMed  Google Scholar 

  56. Wang TS, Huang H (1994) Active oxygen species are involved in the induction of micronuclei by arsenic in XRS-5 cells. Mutagenesis 9(3):253–257. https://doi.org/10.1093/mutage/9.3.253

    Article  CAS  PubMed  Google Scholar 

  57. Lee TC, Ho IC (1995) Modulation of cellular antioxidant defense activities by sodium arsenite in human fibroblasts. Arch Toxicol 69(7):498–504. https://doi.org/10.1007/s002040050204

    Article  CAS  PubMed  Google Scholar 

  58. Matés JM (2000) Effects of antioxidant enzymes in the molecular control of reactive oxygen species toxicology. Toxicology 153(1–3):83–104. https://doi.org/10.1016/s0300-483x(00)00306-1

    Article  PubMed  Google Scholar 

  59. Barchowsky A, Klei LR, Dudek EJ, Swartz HM, James PE (1999) Stimulation of reactive oxygen, but not reactive nitrogen species, in vascular endothelial cells exposed to low levels of arsenite. Free Radic Biol Med 27(11–12):1405–1412. https://doi.org/10.1016/s0891-5849(99)00186-0

    Article  CAS  PubMed  Google Scholar 

  60. Banerjee M, Banerjee N, Ghosh P, Das JK, Basu S, Sarkar AK, States JC, Giri AK (2010) Evaluation of the serum catalase and myeloperoxidase activity in the chronic arsenic exposed individuals and concomitant cytogenetic damage. Toxicol Appl Pharmacol 249(1):47–54. https://doi.org/10.1016/j.taap.2010.08.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Rio DD, Stewart AJ, Pellegrini N (2005) A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr Metab Cardiovasc Dis 15(4):316–328. https://doi.org/10.1016/j.numecd.2005.05.003

    Article  PubMed  Google Scholar 

  62. Sikka SC (2004) Role of oxidative stress and antioxidants in andrology and assisted reproductive technology. J Androl 25(1):5–18. https://doi.org/10.1002/j.1939-4640.2004.tb02751.x

    Article  CAS  PubMed  Google Scholar 

  63. Wafa T, Amel N, Issam C, Imed C, Abdelhedi M, Mohamed H (2011) Subacute effects of 2,4-dichlorophenoxyacetic herbicide on antioxidant defense system and lipid peroxidation in rat erythrocytes. Pestic Biochem Physiol 99(3):256–264. https://doi.org/10.1016/j.pestbp.2011.01.004

    Article  CAS  Google Scholar 

  64. Adeyemi JA, da Cunha M-J, Barbosa F Jr (2015) Teratogenicity, genotoxicity and oxidative stress in zebrafish embryos (Danio rerio) co-exposed to arsenic and atrazine. Comp Biochem Physiol C Toxicol Pharmacol 172–173:7–12. https://doi.org/10.1016/j.cbpc.2015.04.001

    Article  CAS  PubMed  Google Scholar 

  65. Hellou J, Ross NW, Moon TW (2012) Glutathione, glutathione S-transferase, and glutathione conjugates, complementary markers of oxidative stress in aquatic biota. Environ Sci Pollut Res Int 19(6):2007–2023. https://doi.org/10.1007/s11356-012-0909-x

    Article  CAS  Google Scholar 

  66. Sun X, Li S, He Y, Zhao H, Wang Y, Zeng X, Xing M (2017) Arsenic-induced testicular toxicity in Gallus gallus: expressions of inflammatory cytokines and heat shock proteins. Poult Sci 96(9):3399–3406. https://doi.org/10.3382/ps/pex073

    Article  CAS  PubMed  Google Scholar 

  67. Zhao FQ, Zhang ZW, Wang C, Zhang B, Yao HD, Li S, Xu SW (2013) The role of heat shock proteins in inflammatory injury induced by cold stress in chicken hearts. Cell Stress Chaperon 18(6):773–783. https://doi.org/10.1007/2Fs12192-013-0429-8

    Article  CAS  Google Scholar 

  68. Xing M, Zhao P, Guo G, Guo Y, Zhang K, Tian L, He Y, Chai H, Zhang W (2015) Inflammatory factor alterations in the gastrointestinal tract of cocks overexposed to arsenic trioxide. Biol Trace Elem Res 167(2):288–299. https://doi.org/10.1007/s12011-015-0305-8

    Article  CAS  PubMed  Google Scholar 

  69. Rajeshkumar S, Munuswamy N (2011) Impact of metals on histopathology and expression of HSP 70 in different tissues of Milk fish (Chanos chanos) of Kaattuppalli Island, South East Coast. India Chemosphere 83(4):415–421. https://doi.org/10.1016/j.chemosphere.2010.12.086

    Article  CAS  PubMed  Google Scholar 

  70. Lindquist S, Craig EA (1988) The heat-shock proteins. Annu Rev Genet 22:631–677. https://doi.org/10.1146/annurev.ge.22.120188.003215

    Article  CAS  PubMed  Google Scholar 

  71. Yao HD, Wu Q, Zhang ZW, Li S, Wang XL, Lei XG (1830) Xu SW (2013) Selenoprotein W serves as an antioxidant in chicken myoblasts. Biochim Biophys Act 4:3112–3120. https://doi.org/10.1016/j.bbagen.2013.01.007

    Article  CAS  Google Scholar 

  72. Yao HD, Wu Q, Zhang ZW, Zhang JL, Li S, Huang JQ, Ren FZ, Xu SW, Wang XL, Lei XG (2013) Gene expression of endoplasmic reticulum resident selenoproteins correlates with apoptosis in various muscles of Se-Deficient Chicks. J Nutr 143(5):613–619. https://doi.org/10.3945/jn.112.172395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Suzuki CK, Bonifacino JS, Lin AY, Davis MM, Klausner RD (1991) Regulating the retention of T-cell receptor alpha chain variants within the endoplasmic reticulum: Ca(2+)- dependent association with BiP. J Cell Biol 114(2):189–205. https://doi.org/10.1083/jcb.114.2.189

    Article  CAS  PubMed  Google Scholar 

  74. Grosvik BE, Goksoyr A (1996) Biomarker protein expression in primary cultures of salmon (Salmo salar L.) hepatocytes exposed to environmental pollutants. Biomarkers 1(1):45–53. https://doi.org/10.3109/13547509609079346

    Article  CAS  PubMed  Google Scholar 

  75. Cao H, Gao F, Xia B, Zhang M, Liao Y, Yang Z, Hu G, Zhang C (2016) Alterations in trace element levels and mRNA expression of Hsps and inflammatory cytokines in livers of duck exposed to molybdenum or/and cadmium. Ecotox Environ Safe 125:93–101. https://doi.org/10.1016/j.ecoenv.2015.12.003

    Article  CAS  Google Scholar 

  76. Parizek J, Zahor Z (1956) Effect of cadmium salts on testicular tissue. Nature 177:1036. https://doi.org/10.1038/1771036a0

    Article  CAS  PubMed  Google Scholar 

  77. Paksoy Z, Kandemir FM, Gokhan N, Ozkaraca M (2018) The effects of 4-vinylcyclohexene diepoxide on the testes of dogs. Vet Arh 88(6):807–822. https://doi.org/10.24099/vet.arhiv.0101

    Article  CAS  Google Scholar 

  78. Chapin RE, Lamb JC (1984) Effect of ethylene glycol monoethyl ether on various parameters of testicular function in the F344 rats. Environ Health Perspect 57:219–224. https://doi.org/10.1289/ehp.8457219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors all wish to acknowledge the Directors of Central Avian Research Institute (Bhubaneswar, India) and Directorate on Poultry Research, Hyderabad (India), for providing the funding and all logistics, besides ensuring progress of scientific experiments smoothly. We also acknowledge the College of Veterinary Science and Animal Husbandry, Odisha University of Agriculture and Technology (Bhubaneswar, India), for experimental material assistance.

Funding

CARI & DPR together funded this experiment under project number P-1/2017/1-IAV/L34/6200.

Author information

Authors and Affiliations

Authors

Contributions

Dhirendra Kumar, Prafulla Kumar Naik, Bijaya Kumar Swain, and Suryakanta Mishra designed the experiment. Geeta Rani Jena and Santosh Kumar Panda provided helpful suggestions; Statiscal analysis of all data were completed by Kamdev Sethy and Rajalaxmi Behera. Experiment was conducted by Dhirendra Kumar, Prafulla Kumar Naik, Santosh Kumar Panda, Chandra Kant Beura and Geeta Rani Jena. The Manuscript was finally written and modified by Dhirendra kumar, Santosh Kumar Panda, and Suryakanta Mishra.

Corresponding author

Correspondence to Dhirendra Kumar.

Additional information

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumar, D., Panda, S.K., Jena, G.R. et al. Alternations of Fertility Parameters by Graded Dose of Inorganic Arsenic in Adult Male White Pekin Ducks. Biol Trace Elem Res 201, 5358–5367 (2023). https://doi.org/10.1007/s12011-023-03580-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-023-03580-9

Keywords

Navigation