Abstract
The interaction between toxic heavy metals and bio-elements in internal organs and femoral bones and their potential impacts on bone structural properties and renal histopathological changes in bank voles and snow voles were investigated. Our results reveal that heavy metals Hg and Pb accumulate more in femoral bones of alpine habitats than forests. In snow voles, the parameters of the primary osteons’ vascular canals (length, average perimeter and area) simultaneously decreased with an increase of Pb and Sr. Wider primary osteons’ vascular canals of snow voles contained decreased levels of K, but increased Ba. In bank voles, the number of primary osteons increased in alpine habitats along with K, Hg, and Pb accumulation. In the kidneys of bank voles, rising levels of Rb, Hg, and Zn were detected in alpine habitats. Hg increases the most in kidney tissue from alpine habitats in both vole species, and Hg levels (mean value 0.25 μg/g, max. value 0.55 μg/g) in the renal tissues of bank voles from alpine localities are similar to Hg levels from Hg-polluted industrial areas in other studies. This reflects that alpine areas of the Tatra Mountains are highly contaminated with Hg. The intensity of renal hemosiderosis relates significantly to Zn, Fe, and Cu levels in snow voles, with Fe and Zn levels in bank voles from forest habitats, and with Rb in bank voles from alpine habitats. The intensity of tubule necrosis in renal tissues of bank voles from alpine habitats was negatively related to Se content. In bank voles from forest habitats, significant positive correlations were found between the intensity of glomerular hyperplasia and amounts of Zn. The interactions of the detected element’s association with bone tissue and internal organs are discussed.
Similar content being viewed by others
References
Abd El-Aziz GS, El-Fark MM, Saleh HA (2012) The prenatal toxic effect of methylmercury on the development of the appendicular skeleton of rat fetuses and the protective role of vitamin E. Anat Rec Adv Integr Anat Evol Biol 295:939–949
Agrawal R, Chansouria JP (1991) Alterations in plasma sodium and potassium levels following chronic oral ingestion of lead, mercury and cadmium in male albino rats. Indian J Exp Biol 29:767–769
Al Sayegh Petkovšek S, Kopušar N, Kryštufek B (2014) Small mammals as biomonitors of metal pollution: a case study in Slovenia. Environ Monit Assess 186:4261–4274
Al-Tubaikh JA (2010): Hemosiderosis and hemochromatosis. In: Al-Tubaikh JA (Editor), Internal medicine: an illustrated radiological guide. Springer Berlin Heidelberg, Berlin, Heidelberg, pp. 290–292
Baker DH, Ammerman CB (1995) 7 - copper bioavailability. In: Ammerman CB, Baker DH, Lewis AJ (eds) Bioavailability of nutrients for animals. Academic Press, San Diego, pp 127–156
Ballová Z, Janiga M (2018) Lead levels in the bones of small rodents from Alpine and subalpine habitats in the Tian-Shan Mountains, Kyrgyzstan. Atmosphere 9:35
Ballová Z, Janiga M, Hančinský R (2019) Comparison of element concentrations (Ba, Mn, Pb, Sr, Zn) in the bones and teeth of wild ruminants from the West Carpathians and the Tian-Shan Mountains as indicators of air pollution. Atmosphere 10:64
Belcheva M, Metcheva R, Artinian A, Nicolova E (1998) Assessment of toxic elements in the snow vole (Chionomys nivalis) and its food from Rila mountains. Observatoire de Montagne de Moussala OM2 7:276–280
Bhoelan BS, Stevering CH, van der Boog ATJ, van der Heyden MAG (2014) Barium toxicity and the role of the potassium inward rectifier current. Clin Toxicol 52:584–593
Bligh PH, Taylor DM (1963) Comparative studies of the metabolism of strontium and barium in the rat. Biochem J 87:612–618
Bonnelye E, Chabadel A, Saltel F, Jurdic P (2008) Dual effect of strontium ranelate: stimulation of osteoblast differentiation and inhibition of osteoclast formation and resorption in vitro. Bone 42:129–138
Bridges CC, Zalups RK (2017) The aging kidney and the nephrotoxic effects of mercury. J Toxicol Environ Health B Crit Rev 20:55–80
Broussard LA, Hammett-Stabler CA, Winecker RE, Ropero-Miller JD (2002) The toxicology of mercury. Lab Med 33:614–625
Brzozowska A (1989) Interaction of iron, zinc and copper in the body of animals and humans. Rocz Panstw Zakl Hig 40:302–312
Buddhachat K, Klinhom S, Siengdee P, Brown JL, Nomsiri R, Kaewmong P, Thitaram C, Mahakkanukrauh P, Nganvongpanit K (2016) Elemental analysis of bone, teeth, horn and antler in different animal species using non-invasive handheld X-ray fluorescence. PLoS One 11
Buddhachat K, Brown JL, Thitaram C, Klinhom S, Nganvongpanit K (2017) Distinguishing real from fake ivory products by elemental analyses: a Bayesian hybrid classification method. Forensic Sci Int 272:142–149
Bull KR, Roberts RD, Inskip MJ, Goodman GT (1977) Mercury concentrations in soil, grass, earthworms and small mammals near an industrial emission source. Environ Pollut (1970) 12:135–140
Burk RF, Hill KE, Awad JA, Morrow JD, Lyons PR (1995) Liver and kidney necrosis in selenium-deficient rats depleted of glutathione. Lab Investig 72:723–730
Camacho-Cardenosa M, Camacho-Cardenosa A, Timon R, Olcina G, Tomas-Carus P, Brazo-Sayavera J (2019) Can hypoxic conditioning improve bone metabolism? A systematic review. Int J Environ Res Public Health 16
Cho GJ, Park HT, Shin JH, Hur JY, Kim SH, Lee KW, Kim T (2012) The relationship between blood mercury level and osteoporosis in postmenopausal women. Menopause (New York, N.Y.) 19:576–581
Chovancová H, Martiniaková M, Omelka R, Grosskopf B, Toman R (2011) Structural changes in femoral bone tissue of rats after intraperitoneal administration of nickel. Pol J Environ Stud 20:1147–1152
Conti MI, Terrizzi AR, Lee CM, Mandalunis PM, Bozzini C, Piñeiro AE, Martínez MP (2012) Effects of lead exposure on growth and bone biology in growing rats exposed to simulated high altitude. Bull Environ Contam Toxicol 88:1033–1037
Damek-Poprawa M, Sawicka-Kapusta K (2003) Damage to the liver, kidney, and testis with reference to burden of heavy metals in yellow-necked mice from areas around steelworks and zinc smelters in Poland. Toxicology 186:1–10
Damek-Poprawa M, Sawicka-Kapusta K (2004) Histopathological changes in the liver, kidneys, and testes of bank voles environmentally exposed to heavy metal emissions from the steelworks and zinc smelter in Poland. Environ Res 96:72–78
Dardouri K, Haouem S, Gharbi I, Sriha B, Haouas Z, El Hani A, Hammami M (2016) Combined effects of Cd and Hg on liver and kidney histology and function in Wistar rats. J Agric Chem Environ 5:159–169
Debes F, Budtz-Jorgensen E, Weihe P, White RF, Grandjean P (2006) Impact of prenatal methylmercury exposure on neurobehavioral function at age 14 years. Neurotoxicol Teratol 28:363–375
Desouza ED, Gherase MR, Fleming DE, Chettle DR, O’Meara JM, McNeill FE (2017) Performance comparison of two Olympus InnovX handheld x-ray analyzers for feasibility of measuring arsenic in skin in vivo–Alpha and Delta models. Appl Radiat Isot 123:82–93
Diamond GL, Zalups RK (1998) Understanding renal toxicity of heavy metals. Toxicol Pathol 26:92–103
Dunstan CR, Blair JM, Zhou H, Seibel MJ (2007) 6.21 - bone, mineral, connective tissue metabolism. In: Taylor JB, Triggle DJ (eds) Comprehensive medicinal chemistry II. Elsevier, Oxford, pp 495–520
Ďúranová H, Martiniaková M, Omelka R, Grosskopf B, Boboňová I, Toman R (2014) Changes in compact bone microstructure of rats subchronically exposed to cadmium. Acta Vet Scand 56:64
Ensrud KE, Barbour K, Canales MT, Danielson ME, Boudreau RM, Bauer DC, LaCroix AZ, Ishani A, Jackson RD, Robbins JA (2012) Renal function and nonvertebral fracture risk in multiethnic women: the Women’s Health Initiative (WHI). Osteoporos Int 23:887–899
Fallah A, Mohammad-Hasani A, Colagar AH (2018) Zinc is an essential element for male fertility: a review of Zn roles in men's health, germination, sperm quality, and fertilization. J Reprod Infertil 19:69–81
Fleming DE, Groves JW, Gherase MR, George GN, Pickering IJ, Ponomarenko O, Langan G, Spallholz JE, Alauddin M, Ahsan H, Ahmed S (2015) Soft tissue measurement of arsenic and selenium in an animal model using portable X-ray fluorescence. Radiat Phys Chem 116:241–247
Glendening BL, Schrenk WG, Parrish DB (1956) Effects of rubidium in purified diets fed rats. J Nutr 60:563–579
Gocha TP, Agnew AM (2016) Spatial variation in osteon population density at the human femoral midshaft: histomorphometric adaptations to habitual load environment. J Anat 228:733–745
Goyer RA, Rhyne BC (1973) Pathological effects of lead. Int Rev Exp Pathol 12:1–77
Haizhou W (2015): Certificate of certified reference material NCS ZC 71001. In: Steel CNACfIa (Hrsg.), Beijing, China
Hennig C, Thomas CDL, Clement JG, Cooper DML (2015) Does 3D orientation account for variation in osteon morphology assessed by 2D histology? J Anat 227:497–505
Hernández-Becerra E, Gutiérrez-Cortez E, Del Real A, Rojas-Molina A, Rodríguez-García M, Rubio E, Quintero-García M, Rojas-Molina I (2017) Bone mineral density, mechanical, microstructural properties and mineral content of the femur in growing rats fed with Cactus Opuntia ficus indica (L.) mill. (Cactaceae) cladodes as calcium source in diet. Nutrients 9:108
Homma-Takeda S, Terada Y, Iso H, Ishikawa T, Oikawa M, Konishi T, Imaseki H, Shimada Y (2009) Rubidium distribution in kidneys of immature rats. Int J PIXE 19:39–45
Huang X, Hu J, Qin F, Quan W, Cao R, Fan M, Wu X (2017) Heavy metal pollution and ecological assessment around the Jinsha Coal-Fired Power Plant (China). Int J Environ Res Public Health 14:1589
Hurley LS, Gowan J, Milhaud G (1969) Calcium metabolism in manganese-deficient and zinc-deficient rats. Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine (New York, N.Y.) 130:856–860
Hurta V, Buchalová Z (2019) Biogenic and metallic element accumulation in the European Perch (Perca fluviatilis) in the largest dam in Slovakia. Pol J Environ Stud 28:657–667
Isfaoun A, Bureau F, Mouly-Boudey M, Drosdowsky M, Arhan P, Bougle D (1997) Relationships between iron and zinc metabolism: predictive value of digestive absorption on tissue storage. Journal of Trace Elements in Medicine and Biology: Organ of the Society for Minerals and Trace Elements (GMS) 11:23–27
Janiga M, Haas M (2019) Alpine accentors as monitors of atmospheric long-range lead and mercury pollution in alpine environments. Environ Sci Pollut Res 26:2445–2454
Janiga M, Hrehová Z, Dimitrov K, Gerasimova C, Lovari S (2016) Lead levels in the bones of snow voles Chionomys nivalis (Martins, 1842) (Rodentia) from European mountains: a comparative study of populations from the Tatra (Slovakia), Vitosha and Rila (Bulgaria). Acta Zoologica Bulgarica 68:291–295
Janiga M, Ballová Z, Angelovičová M, Korňan J (2019) The snow vole and Tatra marmot as different rodent bioindicators of lead pollution in an alpine environment: a hibernation effect. Pol J Environ Stud 28:1–11
Jia L, Zhang L, Shao C, Song E, Sun W, Li M, Gao Y (2009) An attempt to understand kidney's protein handling function by comparing plasma and urine proteomes. PLoS One 4:e5146
Jihen EH, Imed M, Fatima H, Abdelhamid K (2008) Protective effects of selenium (Se) and zinc (Zn) on cadmium (Cd) toxicity in the liver and kidney of the rat: histology and Cd accumulation. Food Chem Toxicol 46:3522–3527
Jimi E (2017) The role of osteoclastic bone resorption on bone remodeling. Clinical Calcium 27:1689–1695
Jones TC, Hunt RD, King NW (1997) Veterinary pathology. Williams & Wilkins, London, Baltimore, Maryland
Kim YH, Shim JY, Seo MS, Yim HJ, Cho MR (2016) Relationship between blood mercury concentration and bone mineral density in Korean men in the 2008-2010 Korean National Health and nutrition examination survey. Korean J Fam Med 37:273–278
Kocić K, Spasić T, Urošević MA, Tomašević M (2014) Trees as natural barriers against heavy metal pollution and their role in the protection of cultural heritage. J Cult Herit 15:227–233
Komov VT, Ivanova ES, Poddubnaya NY, Gremyachikh VA (2017) Mercury in soil, earthworms and organs of voles Myodes glareolus and shrew Sorex araneus in the vicinity of an industrial complex in Northwest Russia (Cherepovets). Environ Monit Assess 189:104
Lambert H, Frassetto L, Moore JB, Torgerson D, Gannon R, Burckhardt P, Lanham-New S (2015) The effect of supplementation with alkaline potassium salts on bone metabolism: a meta-analysis. Osteoporosis International: a Journal Established as Result of Cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 26:1311–1318
Le Louarn H, Quéré J-P (2003) Les rongeurs de France: faunistique et biologie. Editions Quae
Lentini P, Zanoli L, Granata A, Signorelli SS, Castellino P, Dell'Aquila R (2017) Kidney and heavy metals - the role of environmental exposure (review). Mol Med Rep 15:3413–3419
MacDonald RA (1963) Hemochromatosis and Hemosiderosis. Kanzo 5:34–36
Martiniaková M, Grosskopf B, Vondráková M, Omelka R, Fabiš M (2005) Observation of the microstructure of rat cortical bone tissue. Scripta Med 78:45–50
Martiniaková M, Grosskopf B, Omelka R, Vondráková M, Bauerová M (2006) Differences among species in compact bone tissue microstructure of mammalian skeleton: use of a discriminant function analysis for species identification. J Forensic Sci 51:1235–1239
Martiniaková M, Omelka R, Grosskopf B, Sirotkin AV, Chrenek P (2008) Sex-related variation in compact bone microstructure of the femoral diaphysis in juvenile rabbits. Acta Vet Scand 50:15–15
Martiniaková M, Omelka R, Jančová A, Stawarz R, Formicki G (2011) Concentrations of selected heavy metals in bones and femoral bone structure of bank (Myodes glareolus) and common (Microtus arvalis) voles from different polluted biotopes in Slovakia. Arch Environ Contam Toxicol 60:524–532
Martiniaková M, Boboňová I, Omelka R, Grosskopf B, Stawarz R, Toman R (2013) Structural changes in femoral bone tissue of rats after subchronic peroral exposure to selenium. Acta Vet Scand 55:8
Martinková B, Janiga M, Pogányová A (2019) Mercury contamination of the snow voles (Chionomys nivalis) in the West Carpathians. Environ Sci Pollut Res 26:35988–35995. https://doi.org/10.1007/s11356-019-06714-6
Marx SK, McGowan HA (2011): Long-distance transport of urban and industrial metals and their incorporation into the environment: sources, transport pathways and historical trends. In: Zereini F , Wiseman CLS (Editors), Urban airborne particulate matter: origin, chemistry, fate and health impacts. Springer Berlin Heidelberg, Berlin, Heidelberg, pp. 103–124
Meltzer HL (1991) A pharmacokinetic analysis of long-term administration of rubidium chloride. J Clin Pharmacol 31:179–184
Mendel RR, Bittner F (2006) Cell biology of molybdenum. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research 1763:621–635. https://doi.org/10.1016/j.bbamcr.2006.03.013
Mesquita M, Pedroso TF, Oliveira CS, Oliveira VA, do Santos RF, Bizzi CA, Pereira ME (2016) Effects of zinc against mercury toxicity in female rats 12 and 48 hours after HgCl2 exposure. EXCLI J 15:256–267
Metcheva R, Teodorova S, Topashka-Ancheva M (2001) A comparative analysis of the heavy metals and toxic elements loading indicated by small mammals in different Bulgarian regions. Acta Zool Bulg 53:61–80
Metcheva R, Beltcheva M, Chassovnikarova T (2008) The snow vole (Chionomys nivalis) as an appropriate environmental bioindicator in alpine ecosystems. Sci Total Environ 391:278–283
Morton B, Harrigan-Lum J, Albagli L, Jooss T (1974) The activation of motility in quiescent hamster sperm from the epididymis by calcium and cyclic nucleotides. Biochem Biophys Res Commun 56:372–379
Nganvongpanit K, Buddhachat K, Brown JL, Klinhom S, Pitakarnnop T, Mahakkanukrauh P (2016a) Preliminary study to test the feasibility of sex identification of human (Homo sapiens) bones based on differences in elemental profiles determined by handheld X-ray fluorescence. Biol Trace Elem Res 173:21–29
Nganvongpanit K, Buddhachat K, Klinhom S, Kaewmong P, Thitaram C, Mahakkanukrauh P (2016b) Determining comparative elemental profile using handheld X-ray fluorescence in humans, elephants, dogs, and dolphins: preliminary study for species identification. Forensic Sci Int 263:101–106
Noor Z, Sumitro SB, Hidayat M, Rahim AH, Sabarudin A, Umemura T (2012) Atomic mineral characteristics of Indonesian osteoporosis by high-resolution inductively coupled plasma mass spectrometry. Sci World J 2012:6
O'Dell BL, Sunde RA (1997) Handbook of nutritionally essential mineral elements. CRC Press
Owen DH, Katz DF (2005) A review of the physical and chemical properties of human semen and the formulation of a semen simulant. J Androl 26:459–469
Pamphlett R, Kum Jew S (2019) Mercury is taken up selectively by cells involved in joint, bone, and connective tissue disorders. Frontiers in Medicine 6
Patton KT, Thibodeau GA (2014) Anatomy & Physiology - E-Book
Peixoto NC, Pereira ME (2007) Effectiveness of ZnCl2 in protecting against nephrotoxicity induced by HgCl2 in newborn rats. Ecotoxicol Environ Saf 66:441–446
Peixoto NC, Serafim MA, Flores EM, Bebianno MJ, Pereira ME (2007) Metallothionein, zinc, and mercury levels in tissues of young rats exposed to zinc and subsequently to mercury. Life Sci 81:1264–1271
Pemmer B, Roschger A, Wastl A, Hofstaetter JG, Wobrauschek P, Simon R, Thaler HW, Roschger P, Klaushofer K, Streli C (2013) Spatial distribution of the trace elements zinc, strontium and lead in human bone tissue. Bone 57:184–193
Pyszel A, Wrobel T, Szuba A, Andrzejak R (2005) Effect of metals, benzene, pesticides and ethylene oxide on the haematopoietic system. Med Pr 56:249–255
Reed WP (1992): Certificate of analysis standard reference material 1486. Bone Meal. In: Technology NIoS (Hrsg.), Gaithersburg, Maryland
Richter GW (1974) Effects of cyclic starvation-feeding and of splenectomy on the development of hemosiderosis in rat livers. Am J Pathol 74:481–506
Rodríguez J, Mandalunis PM (2018) A review of metal exposure and its effects on bone health. J Toxicol 2018:4854152–4854152
Saljooghi AS, Delavar-mendi F (2011) The effect of mercury in iron metabolism in rats. J Clin Toxicol:s3
Shao J, Shi J, Duo B, Liu C, Gao Y, Fu J, Yang R, Jiang G (2016) Mercury in alpine fish from four rivers in the Tibetan Plateau. J Environ Sci 39:22–28
Six KM, Goyer RA (1972) The influence of iron deficiency on tissue content and toxicity of ingested lead in the rat. J Lab Clin Med 79:128–136
Sontag PT, Steinberg DK, Reinfelder JR (2019) Patterns of total mercury and methylmercury bioaccumulation in Antarctic krill (Euphausia superba) along the West Antarctic Peninsula. Sci Total Environ 688:174–183
Suttle NF (1974) Recent studies of the copper-molybdenum antagonism. Proc Nutr Soc 33:299–305
Suzuki N, Yamamoto M, Watanabe K, Kambegawa A, Hattori A (2004) Both mercury and cadmium directly influence calcium homeostasis resulting from the suppression of scale bone cells: the scale is a good model for the evaluation of heavy metals in bone metabolism. J Bone Miner Metab 22:439–446
Tao H, Man Y, Shi X, Zhu J, Pan H, Qin Q, Liu S (2016) Inconceivable hypokalemia: a case report of acute severe barium chloride poisoning. Case Rep Med 2016:4
Tête N, Durfort M, Rieffel D, Scheifler R, Sanchez-Chardi A (2014) Histopathology related to cadmium and lead bioaccumulation in chronically exposed wood mice, Apodemus sylvaticus, around a former smelter. Sci Total Environ 481:167–177
Tizhe EV, Ibrahim ND-G, Fatihu MY, Onyebuchi II, George BDJ, Ambali SF, Shallangwa JM (2014) Influence of zinc supplementation on histopathological changes in the stomach, liver, kidney, brain, pancreas and spleen during subchronic exposure of Wistar rats to glyphosate. Comp Clin Pathol 23:1535–1543
Van Ryssen JB, Stielau WJ (1981) Effect of different levels of dietary molybdenum on copper and Mo metabolism in sheep fed on high levels of Cu. Br J Nutr 45:203–210
Wang W, Yun Z, Peng HZ, Yan SJ, Zhang HT, Qiu XC, Wen YH, Long H, Ma BA (2017) The hypobaric hypoxia environment impairs bone strength and quality in rats. Int J Clin Exp Med 10:9397–9406
Weaver CM (2013) Potassium and health. Adv Nutr 4:368S–377S
Weaver CM, Stone MS, Lobene AJ, Cladis DP, Hodges JK (2018) What is the evidence base for a potassium requirement? Nutr Today 53:184–195
Yamaguchi M (1998) Role of zinc in bone formation and bone resorption. J Trace Elements Exp Med 11:119–135
Yanagimachi R, Usui N (1974) Calcium dependence of the acrosome reaction and activation of guinea pig spermatozoa. Exp Cell Res 89:161–174
Yanagisawa H, Miyazaki T, Nodera M, Miyajima Y, Suzuki T, Kido T, Suka M (2014) Zinc-excess intake causes the deterioration of renal function accompanied by an elevation in systemic blood pressure primarily through superoxide radical-induced oxidative stress. Int J Toxicol 33:288–296
Zalups RK (2000) Molecular interactions with mercury in the kidney. Pharmacol Rev 52:113–143
Zechmeister HG (1995) Correlation between altitude and heavy metal deposition in the Alps. Environ Pollut 89:73–80
Zhu K, Devine A, Prince RL (2009) The effects of high potassium consumption on bone mineral density in a prospective cohort study of elderly postmenopausal women. Osteoporosis International: a Journal Established as Result of Cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 20:335–340
Acknowledgments
We are grateful to prof. Marián Janiga for valuable suggestions, consultation, and comments on the scientific and methodological aspects of the study. We would like to thank our colleagues and students for their assistance in the field, especially Zuzana Hrehová, Michal Némethy, Daniela Dúhová, and Bibiána Martinková. For English proofreading and improving, we are indebted to native English-speaking editor Amanda Clarahan.
Funding
This research was funded by European Structural Funds (ITMS: 26210120016).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible editor: Philippe Garrigues
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ballová, Z.K., Korec, F. & Pinterová, K. Relationship between heavy metal accumulation and histological alterations in voles from alpine and forest habitats of the West Carpathians. Environ Sci Pollut Res 27, 36411–36426 (2020). https://doi.org/10.1007/s11356-020-09654-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-09654-8