Abstract
Failure to distinguish between elemental tungsten and tungsten alloys has caused confusion, especially about their relative toxicity in shotgun ammunition. Controlled experiments indicate that the carcinogenicity of embedded tungsten–nickel–cobalt alloys derives from their nickel and cobalt content, and not the tungsten. The carcinogenicity of metallic nickel and cobalt implants in animal tissues is well-established. Studies in which pure tungsten metal is embedded in animal and human tissues indicate that there is no toxicity or carcinogenicity developed locally or systemically. The exposed tungsten corrodes slowly in the tissue fluids and is excreted from the body. Chronic studies in which pure tungsten-based shot are placed, continuously, in the foregut of ducks over 150 days indicate that there are no adverse physiological effects, nor disruption of ducks’ reproduction and development of their progeny. This type of shot is environmentally safe and non-toxic to animals. Shot containing nickel could pose health problems to animals if embedded in their tissues. The use of known toxic metals in lead-free shot should be subjected to further examination and, if warranted, regulation.
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References
Bachthaler M, Lenhart M, Paetzel M, Feuerbach S, Link J, Manke C (2004) Corrosion of tungsten coils after peripheral vascular embolization therapy: influence on outcome and tungsten load. Cathet Cardiovasc Interv 62:380–384
Bardack S, Dalgard CL, Kalinich JF, Kasper CE (2014) Genotoxic changes to rodent cells exposed in vitro to tungsten, nickel, cobalt and iron. Int J Environ Res Public Health 11:2922–2940. doi:10.3390/ijerph110302922
Barrett J, Wells I, Riordan R, Roobottom C (2000) Endovascular embolization of varicoceles: resorption of tungsten coils in the spermatic vein. Cardiovasc Intervent Radiol 23:457–459
Beyersman D (2002) Effects of carcinogenic metals on gene expression. Toxicol Lett 127:63–68
Brewer L, Fairbrother A, Clark J, Amick D (2003) Acute toxicity of lead, steel, and an iron-tungsten-nickel shot to mallard ducks (Anas platyrhynchos). J Wildl Dis 39:638–648
Butler TJ, Jackson RW, Robson JY, Owen RJT, Delves HT, Sieniawska CE, Rose JDG (2000) In vivo degradation of tungsten embolization coils. Br J Radiol 73:601–603
Cangul H, Broday L, Salnikow K, Sutherland J, Peng W, Zhang Q, Poltaratsky V, Yee H, Zoroddu MA, Costa M (2002) Molecular mechanisms of nickel carcinogenesis. Toxicol Lett 127:69–75
Centeno JA, Rogers DA, van der Voet GB, Fornero E, Zhang L, Mullick FG, Chapman GD, Olabisi AO, Wagner DJ, Stojadinovic A, Potter BK (2014) Embedded fragments from U.S. military personnel—chemical analysis and potential health implications. Int J Environ Res Public Health 11:1261–1278. doi:10.3390/ijerph110201261
Costa M, Davidson TL, Chen H, Ke Q, Zhang P, Yan Y, Huang C, Kluz T (2005) Nickel carcinogenesis: epigenetics and hypoxia signalling. Mutat Res 592:79–88. doi:10.1016/j.mrfmmm.2005.06.008
Danish Nature Agency (2013) Høringsbrev (Letter of consultation of stakeholders). https://hoeringsportalen.dk/Hearing/Details/17447 Accessed August 10, 2015
Danish Nature Agency (2014) Høringsnotat (Summary of incoming responses). https://hoeringsportalen.dk/Hearing/Details/17447 Accessed August 10, 2015
Denkhaus E, Salnikow K (2002) Nickel essentiality, toxicity, and carcinogenicity. Crit Rev Oncol/Hematol 42:35–56
De Boeck M, Kirsch-Volders M, Lison D (2003) Cobalt and antimony: genotoxicity and carcinogenicity. Mutat Res 533:135–152. doi:10.1016/j.mrfmmm.2003.07.012
Dunn CJ, Hardee MM, Gibbons AJ, Staite ND, Richard KA (1989) Local pathological responses to slow-release recombinant interleukin-1, interleukin-2 and γ-interferon in the mouse and their relevance to chronic inflammatory disease. Clin Sci 76:261–263. doi:10.1042/cs0760261
Fishcel-Ghodsian F, Brown L, Mathiowitz E, Brandenburg D, Langer R (1988) Enzymatically controlled drug delivery. Proc Natl Acad Sci U S A 85:2403–2406
Freese A, Sabel BA, Saltzman WM, During M, Langer R (1989) Controlled release of dopamine from a polymeric brain implant: in vitro characterization. Exp Neurol 103:234–238. doi:10.1016/0014-4886(89)90047-2
Gallagher SP, Beavers JB, Van Hoven R, Jaber M (1998) Tungsten Matrix shot: an oral toxicity study with the Mallard. Project No. 475-101. Wildlife International Ltd., 8598 Commerce Drive, Easton, Maryland 21601, USA
Gallagher SP, Beavers JB, Van Hoven R, Jaber M (1999) Tungsten Matrix shot. A chronic exposure study with the mallard including reproductive parameters. Project No. 475-102. Wildlife International Ltd., 8598 Commerce Drive, Easton, Maryland 21601, USA
Gero R, Borukhin L, Pikus I (2001) Some structural effects of plastic deformation on tungsten heavy metal alloys. Mater Sci Eng A302:162–167
Guillemain M, Devineau O, Lebreton J-D, Mondain-Monval J-Y, Johnson AR, Simon G (2007) Lead shot and teal (Anas crecca) in the Camargue, southern France: effects of embedded and ingested pellets on survival. Biol Conserv 137:567–576. doi:10.1016/j.biocon.2007.03.016
Hansen T, Clermont G, Alves A, Eloy R, Brochhausen C, Boutrand JP, Gatti AM, Kirkpatrick CJ (2006) Biological tolerance of different materials in bulk and nanoparticulate form in a rat model: sarcoma development by nanoparticles. J R Soc Interface 3:767–775. doi:10.1098/rsif.2006.0145
Harris RM, Williams TD, Hodges NJ, Waring RH (2011) Reactive oxygen species and oxidative DNA damage mediate the cytotoxicity of tungsten-nickel-cobalt alloys in vitro. Toxicol Appl Pharmacol 250:19–28. doi:10.1016/j.taap.2010.09.020
Heath JC, Webb M (1967) Content and intracellular distribution of the inducing metal in the primary rhabdomyosarcomata induced in the rat by cobalt, nickel and cadmium. Br J Cancer 21:768–779
Hicklin PW, Barrow WR (2004) The incidence of embedded shot in waterfowl in Atlantic Canada and Hudson Strait. Waterbirds 27:41–45
Hoots EA, Renberg WC, Patton KM, Roush JK (2007) Evaluation of local and systemic effects after intramuscular implantation of lead shot alternatives in rats. Am J Vet Res 68:446–452
Kalinich JF, Emond CA, Dalton TM, Mog SR, Coleman GD, Kordell JE, Miller AC, McClain DE (2005) Embedded weapons-grade tungsten alloy shrapnel induces metastatic high-grade rhabomyosarcomas in F344 rats. Environ Health Perspect 113:729–734. doi:10.1289/ehp.7791
Kasprzak KS, Gabryel P, Jarczewska K (1983) Carcinogenicity of nickel(II) hydroxides and nickel(II) sulfate in Wistar rats and its relation to the in vitro dissolution rates. Carcininogen 4:275–279
King L (2014) Danes to ban tungsten. Shooting times. URL: http://www.shootinguk.co.uk/news/danes-to-ban-tungsten-250 Accessed July 24, 2015
Kouketsu K, Shimizu T (1988) Storing of apheresis platelets in ethylene-vinyl acetate copolymer bags: relationship between the bag size and the number of platelets maintaining aerobic metabolism. Cryobiology 25:440–444. doi:10.1016/0011-2240(88)900-51-X
Kraabel BJ, Miller MW, Getzy DM, Ringelman JK (1996) Effects of embedded tungsten-bismuth-tin shot and steel shot on Mallards (Anas platyrhynchos). J Wildl Dis 32:1–8
Magaye R, Zhao (2012) Recent progress in studies of metallic nickel and nickel-based nanoparticles’ genotoxicity and carcinogenicity. Environ Toxicol Pharmacol 34:644–650. doi:10.1016/j.etap.2012.08.012
Magaye R, Zhao J, Bowman L, Ding M (2012) Genotoxicity and carcinogenicity of cobalt-, nickel- and copper-based nanoparticles (review). Exp Therapeut Med 4:551–561. doi:10.3892/etm.2012.656
M’Bemba-Meka P, Lemieux N, Chakrabarti SK (2005) Nickel compound-induced DNA single-strand breaks in chromosomal and nuclear chromatin in human blood lymphocytes in vitro: role of oxidative stress and intracellular calcium. Mutat Res 586:124–137. doi:10.1016/j.mrgentox.2005.06.001
Manara MC, Baldini N, Serra M, Lollini P-L, Giovanni CD, Vaccari M, Argnani A, Benini S, Maurici D, Picci P, Scotlandi K (2000) Reversal of malignant phenotype in human osteosarcoma cells transduced with the alkaline phosphatase gene. Bone 26:215–220. doi:10.1016/S8756-3282(99)00266-5
Miller AC, Mog S, McKinney L, Luo L, Allen J, Xu J, Page N (2001) Neoplastic transformation of human osteoblast cells to the tumorigenic phenotype by heavy metal-tungsten alloy particles: induction of genotoxic effects. Carcinogen 22:115–125
Miller AC, Brooks K, Smith J, Page N (2004) Effect of the military-relevant heavy metals, depleted uranium and heavy metal tungsten-alloy on gene expression in human liver carcinoma cells (HepG2). Mol Cell Biochem 255:247–256
Mitchell RR, Fitzgerald SD, Auerlich RJ, Balander RJ, Powell DC, Templeman RJ, Sickle RL, Stevens W, Bursian SJ (2001a) Health effects following chronic dosing with tungsten-iron and tungsten-polymer shot in adult game-farm mallards. J Wildl Dis 37:451–458
Mitchell RR, Fitzgerald SD, Auerlich RJ, Balander RJ, Powell DC, Templeman RJ, Cray C, Stevens W, Bursian SJ (2001b) Hematological effects and metal residue concentrations following chronic dosing with tungsten-iron and tungsten-polymer shot in adult game-farm mallards. J Wildl Dis 37:459–467
Mitchell RR, Fitzgerald SD, Auerlich RJ, Balander RJ, Powell DC, Templeman RJ, Stevens W, Bursian SJ (2001c) Reproductive effects and duckling survivability following chronic dosing with tungsten-iron and tungsten-polymer shot in game-farm mallards. J Wildl Dis 37:468–474
Muñoz A, Costa M (2012) Elucidating the mechanisms of nickel compound uptake: a review of particulate and nano-nickel endocytosis and toxicity. Toxicol Appl Pharmacol 260:1–16. doi:10.1016/j.taap.2011.12.014
Noer H, Madsen J, Hartmann P (2007) Reducing wounding of game by shotgun hunting: effects of a Danish action plan on pink-footed geese. J Appl Ecol 44:653–662. doi:10.1111/j.1365-2664.2007.01293.x
Patel E, Lynch C, Ruff V, Reynolds M (2012) Co-exposure to nickel and cobalt chloride enhances cytotoxicity and oxidative stress in human lung epithelial cells. Toxicol Appl Pharmacol 258:367–375. doi:10.1016/j.taap.2011.11.019
Peuster M, Fink C, Wohlsein P, Breugmann M, Günther A, Kaese V, Niemyer M, Haferkamp H, von Schnakenburg C (2003a) Degradation of tungsten coils implanted into the subclavian artery of New Zealand white rabbits is not associated with local or systemic toxicity. Biomaterials 24:393–399
Peuster M, Fink C, von Schnakenburg C (2003b) Biocompatibility of corroding tungsten coils: in vitro assessment of degradation kinetics and cytotoxicity on human cells. Biomaterials 24:4057–4061. doi:10.1016/S0142-961(03)00274-6
Ramsay JWA, Miller RA, Crocker PR, Ringrose BJ, Jones S, Levison DA, Whitfield HN, Wickham JEA (1986) An experimental study of hydrophilic plastics for urological use. Br J Urol 58:70–74. doi:10.1111/j.1464-410X.1986.tb05431.x
Roedel EQ, Cafasso DE, Lee KWM, Pierce LM (2012) Pulmonary toxicity after exposure to military-relevant heavy metal tungsten alloy particles. Toxicol Appl Pharmacol 259:74–86. doi:10.1016/j.taap.2011.12.008
Sanderson GC, Anderson WL, Foley GL, Havera SP, Skowron LM, Brawn JW, Taylor GD, Seets JW (1998) Effects of lead, iron, and bismuth alloy shot embedded in the breast muscles of game-farm mallards. J Wildl Dis 34:688–697. doi:10.7589/0090-3558-34.4.688
Schaumlöffel D (2012) Nickel species: analysis and toxic effects. J Trace Elem Med Biol 26:1–6. doi:10.1016/j.jtemb.2012.01.002
Schuster BE, Roszell LE, Murr LE, Ramirez DA, Demaree JD, Klotz BR, Rosencrance AB, Dennis WE, Bao W, Perkins EJ, Dillman JF, Bannon DI (2012) In vivo corrosion, tumor outcome, and microarray gene expression for two types of muscle-implanted tungsten alloys. Toxicol Appl Pharmacol 265:128–138. doi:10.1016/j.taap.2012.08.025
Scotlandi K, Serra M, Manara MC, Nanni P, Nicoletti G, Landuzzi L, Maurici D, Baldini N (1993) Human osteosarcoma cells, tumorigenic in nude mice, express β1 integrins and low levels of alkaline phosphatase activity. Int J Oncol 3:963–969. doi:10.3892/ijo.3.5.963
Simonsen LO, Harbak H, Bennekou P (2012) Cobalt metabolism and toxicology—a brief update. Sci Total Environ 432:210–215. doi:10.1016/j.scitotenv.2012.06.009
Smith AL, Cordery PM, Thompson ID (1995) Manufacture and release characteristics of Elvax polymers containing glutamate receptor antagonists. J Neurosci Methods 60:211–217. doi:10.1016/0165-0270(95)00014-L
Tavecchia G, Pradel R, Lebreton J-D, Johnson AR, Mondain-Monval J-Y (2001) The effect of lead exposure on survival of adult mallards in the Camargue, southern France. J Appl Ecol 38:1197–1207
Thomas VG (2015) Availability and use of lead-free shotgun and rifle cartridges in the UK, with reference to regulations in other jurisdictions. In: Delahay RJ, Spray CJ (eds) The Oxford Lead Symposium. Lead ammunition: understanding and minimising the risks to human and environmental health. Edward Grey Institute, Oxford, UK, pp 85–97
Thomas VG, Guitart R (2003) Evaluating non-toxic substitutes for lead shot and fishing weights: criteria and regulations. Environ Policy Law 33(3-4):150–154
Thomas VG, Roberts MJ, Harrison PTC (2009) Assessment of the environmental toxicity and carcinogenicity of tungsten-based shot. Ecotoxicol Environ Saf 72:1031–1037. doi:10.1016/j.ecoenv.2009.01.001
Thomas VG, Kanstrup N, Gremse C (2015) Key questions and responses regarding the transition to use of lead-free ammunition. In: Delahay RJ, Spray CJ (eds) The Oxford Lead Symposium. Lead ammunition: understanding and minimising the risks to human and environmental health. Edward Grey Institute, Oxford, UK, pp 125–135
USFWS (US Fish and Wildlife Service) (1986) Use of Lead Shot for Hunting Migratory Birds. Final Supplemental Environmental Impact Statement 1986. Office of Migratory Bird management, Department of the Interior. US Govt Printing Office, Washington, DC
USFWS (US Fish and Wildlife Service) (1997) Migratory bird hunting: revised test procedure for nontoxic shot approval procedure for shot and shot coatings. Fed Regist 62(320):63607–63615
USFWS (US Fish and Wildlife Service) (2006) Migratory bird hunting: approval of tungsten-iron-copper-nickel, iron-tungsten-nickel alloy, tungsten-bronze (additional information), and tungsten-tin-iron shot types as non-toxic for hunting waterfowl and coots: availability of environmental assessments. Fed Regist 71(17):4294–4297
Verma R, Xu X, Jaiswal MJ, Olsen C, Mears D, Caretti G, Galdzicki Z (2011) In vitro profiling of epigenetic modifications underlying heavy metal toxicity of tungsten-alloy and its components. Toxicol Appl Pharmacol 253:178–187. doi:10.1016/j.taap.2011.04.002
Wyszynski RE, Vahey JB, Manning L, Bruner WE, Morgan KM, Burney EN (1989) Sustained release of 5-fluorouracil from ethylene acetate copolymer. J Ocol Pharmacol Therapeut 5:141–146. doi:10.1089/jop.1989.5.141
Yang MB, Tamargo RJ, Brem H (1989) Controlled delivery of 1,3-bis(2-chloroethyl)-1-nitrosourea from ethylene-vinyl acetate copolymer. Cancer Res 49:5103–5107
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There is no potential conflict of interest. This review was prepared entirely with the personal resources of the author. He is not funded by any arms or ammunition maker, any government department, any university or any agency promoting an end to use of lead shot. The author’s travel to Denmark and the UK in 2014 to present a seminar on metal toxicity to the Danish EPA and to the UK DEFRA was supported by the company Kent Gamebore.
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Thomas, V.G. Elemental tungsten, tungsten–nickel alloys and shotgun ammunition: resolving issues of their relative toxicity. Eur J Wildl Res 62, 1–9 (2016). https://doi.org/10.1007/s10344-015-0979-4
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DOI: https://doi.org/10.1007/s10344-015-0979-4