Restricted accessResearch articleFirst published online 2019-2
Environmental chromium from the tannery industry induces altered reproductive endpoints in the wild female small Indian mongoose ( Urva auropunctatus )
The populations of wild animals are declining in many parts of the world in response to man-made alterations in the environment. Environmental contamination due to heavy metals discharge from industry may contribute to the decline of wild animal populations by impacting their reproduction, growth, and development. In the leather tanning industry, chromium (Cr) is used as a basic component, but it is a potent toxicant that can affect many of the physiological functions of animals. In the current study, we investigated the reproductive toxicity of industrial Cr in female small Indian mongooses inhabiting a tannery area. Adult female specimens were live trapped from February 2015 to January 2016. Blood and other body tissues (ovaries, kidneys and liver) of the captured specimens were collected along with soil and water samples from the environment for analysis. The Cr concentrations were found significantly (p < 0.0001) increased compared to control in the environment, blood, and all body tissues of the animals. Estradiol and progesterone levels were found to be significantly decreased in comparison with control (p < 0.0001), along with reduced ovarian weights, while follicle stimulating hormone (FSH) and luteinizing hormone levels were found significantly (p < 0.0001) elevated. Light microscopy revealed significantly decreased in comparison with control ovarian follicle numbers (p < 0.0001) and diameters, vacuolization of the oocytes, and a significantly higher percentage of atretic follicles inside the ovary. We conclude that Cr discharged from the tanneries is absorbed by the exposed female small Indian mongoose, leading to ovarian dysfunction with potential impairment of reproductive function.
AdamopoulosDANicopoulouSKapollaN. (1995) Endocrine effects of testosterone undecanoate as a supplementary treatment to menopausal gonadotropins or tamoxifen citrate in idiopathic oligozoospermia. Fertility and Sterility64(4): 818–824.
2.
AhmedSAPenhaleWJ (1982) The influence of testosterone on the development of autoimmune thyroiditis in thymectomized and irradiated rats. Clinical and Experimental Immunology48(2): 367–374.
3.
AllenLH (2009) How common is vitamin B-12 deficiency?American Journal of Clinical Nutrition89(2): 693S–696S.
4.
AltafMMMasoodFMalikA (2008) Impact of long-term application of treated tannery effluents on the emergence of resistance traits in Rhizobium sp. isolated from Trifolium alexandrinum. Turkish Journal of Biology32(1): 1–8.
5.
AndleebSMahmoodTKhalidA. (2018) Hexavalent chromium induces testicular dysfunction in small Indian mongoose (Herpestes javanicus) inhabiting tanneries area of Kasur District, Pakistan. Ecotoxicology and Environmental Safety148: 1001–1009.
6.
AOAC (1990) AOAC Official Methods of Analysis (volume 1), CFR section (s): 9 CFR 318.19 (b) Association of Official Analytical Chemists (USA).
7.
BancroftJDStevenA (1990) Theory and Practice of Histological Technique. New York: Churdchill Livingstone.
8.
BanuSKSamuelJBAroshJA. (2008) Lactational exposure to hexavalent chromium delays puberty by impairing ovarian development, steroidogenesis and pituitary hormone synthesis in developing Wistar rats. Toxicology and Applied Pharmacology232(2): 180–189.
9.
BanuSKStanleyJALeeJ. (2011) Hexavalent chromium-induced apoptosis of granulosa cells involves selective sub-cellular translocation of Bcl-2 members, ERK1/2 and p53. Toxicology and Applied Pharmacology251(3): 253–266.
10.
BarcelouxDG (1999) Chromium. Journal of Toxicology: Clinical Toxicology37(2): 173–194.
11.
ColbornTClementC (1992) Chemically Induced Alterations in Sexual and Functional Development. Princeton: Princeton Scientific Publishing.
DayanADPaineAJ (2001) Mechanisms of chromium toxicity, carcinogenicity and allergenicity: review of the literature from 1985 to 2000. Human & Experimental Toxicology20(9): 439–451.
14.
De MagalhaesJPCostaJ (2009) A database of vertebrate longevity records and their relation to other life-history traits. Journal of Evolutionary Biology22(8): 1770–1774.
15.
DeFloraSCamoiranoABagnascoM. (1997) Estimates of the chromium (VI) reducing capacity in human body compartments as a mechanism for attenuating its potential toxicity and carcinogenicity. Carcinogenesis18(3): 531–537.
16.
DermentzisKChristoforidisALazaridouA. (2011) Removal of hexavalent chromium from electroplating wastewater by electrocoagulation with iron electrodes. Global NEST Journal13(4): 412–418.
17.
DesaiCJainKMadamwarD (2008) Evaluation of in vitro Cr (VI) reduction potential in cytosolic extracts of three indigenous Bacillus sp. isolated from Cr (VI) polluted industrial landfill. Bioresource Technology99(14): 6059–6069.
18.
EsmaeiliAMesdaghiniaAVazirinejadR (2005) Chromium (III) removal and recovery from tannery wastewater by precipitation process. American Journal of Applied Sciences2(10): 1471–1473.
19.
GreeneLERiedererAMMarcusM. (2010) Associations of fertility and pregnancy outcomes with leather tannery work in Mongolia: a pilot study. International Journal of Occupational and Environmental Health16(1): 60–68.
20.
HayesTB (2000) Endocrine disruption in amphibians. Pensacola: SETAC Press.
21.
HoffmannJCSoaresMJNelsonML. (1984) Seasonal reproduction in the mongoose, Herpestes auropunctatus: IV. Organ weight and hormone changes in the female. General and Comparative Endocrinology55(2): 306–314.
22.
HoyerPBSipesIG (1996) Assessment of follicle destruction in chemical-induced ovarian toxicity. Annual Review of Pharmacology and Toxicology36: 307–331.
23.
JunaidMMurthyRCSaxenaDK (1996) Embryo- and fetotoxicity of chromium in pregestationally exposed mice. Bulletin of Environmental Contamination and Toxicology57(2): 327–334.
24.
KanojiaRKJunaidMMurthyRC (1998) Embryo and fetotoxicity of hexavalent chromium: A long-term study. Toxicology Letters95(3): 165–172.
25.
KotasJStasickaZ (2000) Chromium occurrence in the environment and methods of its speciation. Environmental pollution107(3): 263–283.
26.
LiZHLiPRandakT (2011) Evaluating the toxicity of environmental concentrations of waterborne chromium (VI) to a model teleost, Oncorhynchus mykiss: A comparative study of in vivo and in vitro. Comparative Biochemistry and Physiology Part C: Pharmacology153(4): 402–407.
27.
MarquesMJSalvadorAMorales-RubioA. (2000) Chromium speciation in liquid matrices: a survey of the literature. Fresenius Journal of Analytical Chemistry367(7): 601–613.
28.
MetzeDJakubowskiNKlockowD (2005) Speciation of Chromium in Environment and Food. London: Wiley.
29.
MurthyRCSaxenaDKGuptaSK. (1991) Ultrastructural observations in testicular tissue of chromium-treated rats. Reproductive Toxicology5(5): 443–447.
30.
NellisDWEverardCOR (1983) The biology of the mongoose in the Caribbean. Studies on the fauna of Curacao and other Caribbean Islands64(1): 1–162.
31.
NTP (2008) Technical report on the Toxicity and Carcinogenesis studies of Sodium Dichromate Dihydrate (CAS No. 7789-12-0) in F344/N Rats and B6C3F1 Mice (Drinking water studies) National Toxicology Program, National Institute of Health (NIH) Islamabad, Pakistan.
32.
Pakistan Govt. (2012) District Pre-Investment Study.
33.
PocockRI (1941) The Fauna And British India Including Ceylon And Burma/mammalia. London: Taylor & Francis.
34.
QuinterosFAMachiavelliLIMilerEA. (2008) Mechanisms of chromium (VI)-induced apoptosis in anterior pituitary cells. Toxicology249(2-3): 109–115.
35.
RaoMVChawlaSLSharmaSR (2009) Protective role of vitamin E on nickel and/or chromium induced oxidative stress in the mouse ovary. Food and Chemical Toxicology47(6): 1368–1371.
36.
RobertsTJ (1997) The Mammals of Pakistan. New York: Oxford University Press.
37.
SamuelJBStanleyJARoophaDP. (2011) Lactational hexavalent chromium exposure-induced oxidative stress in rat uterus is associated with delayed puberty and impaired gonadotropin levels. Human & Experimental Toxicology30(2): 91–101.
38.
SamuelJBStanleyJAVengateshG. (2012) Ameliorative effect of vitamin C on hexavalent chromium-induced delay in sexual maturation and oxidative stress in developing Wistar rat ovary and uterus. Toxicology & Industrial Health28(8): 720–733.
39.
SaxenaDKMurthyRCJainVK. (1990) Fetoplacental maternal uptake of hexavalent chromium administered orally in rats and mice. Bulletin of Environmental Contamination and Toxicology45(3): 430–435.
40.
SipowiczMAAndersonLMUtermahlenWE. (1997) Uptake and tissue distribution of chromium (III) in mice after a single intraperitoneal or subcutaneous administration. Toxicology Letters93(1): 9–14.
41.
SoudaniNSefiMAmaraIB. (2010) Protective effects of Selenium (Se) on Chromium (VI) induced nephrotoxicity in adult rats. Ecotoxicology and Environmental Safety73(4): 671–678.
42.
StoeckerJB (2004) Chromium. In Elements and their Compounds in the Environment. Germany: Weinheim.
43.
SzulczewskiMDHelmkePABleamWF (1997) Comparison of XANES analyses and extractions to determine chromium speciation in contaminated soils. Environmental Science & Technology31: 2954–2959.
44.
TravacioMPoloJMLlesuyS (2001) Chromium (VI) induces oxidative stress in the mouse brain. Toxicology162(2): 139–148.
45.
VonBRLiuD (1993) Chromium and hexavalent chromium. Journal of Applied Toxicology13(3): 225–230.
