Pets as Sentinels of Human Exposure to Neurotoxic Metals
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Abstract
The idea that animals may be used as sentinels of environmental hazards pending over humans and the associated public health implications is not a new one. Nowadays pets are being used as bioindicators for the effects of environmental contaminants in human populations. This is of paramount importance due to the large increase in the worldwide distribution of synthetic chemicals, particularly in the built environment. Companion animals share the habitat with humans being simultaneously exposed to and suffering the same disease spectrum as their masters. Moreover, their shorter latency periods (due to briefer lifespans) enable them to act as early warning systems, allowing timely public health interventions. The rise on ethical constraints on the use of animals and, consequently, on the sampling they can be subjected to has led to the preferential use of noninvasive matrices, and in this case we are looking into hair. This chapter focuses in three non-essential metals: mercury, lead, and cadmium, due to their ubiquitous presence in the built environment and their ability of affecting the mammal nervous system. There is a fairly short amount of studies reporting the concentrations of these metals in pets’ hair, particularly for cats. These studies are characterized, and the metal concentrations corresponding to different parameters (e.g., age, sex, diet, rearing) are described in order to provide the reader with a general vision on the use of this noninvasive matrix on the studies conducted since the last two decades of the twentieth century.
Keywords
Surrogacy Early warning Latency Cadmium Lead MercuryNotes
Acknowledgments
This work was supported by funds from the Health Sciences Research Center (CICS-UBI) through National Funds by FCT – Foundation for Science and Technology (UID/Multi/00709/2019) – and developed under the scope of the project CICECO-Aveiro Institute of Materials, FCT Ref. UID/CTM/50011/2019. Additional funding was provided by project ICON “Interdisciplinary Challenges on Neurodegeneration” (Ref. CENTRO-01-0145-FEDER-000013, project funded by FEDER funds through POCI-COMPETE 2020) and La Mer Project funded by the Japanese Ministry of Education, Culture, Sports, Science, and Technology (MEXT). Ana Catarina Sousa acknowledges the University of Aveiro, for funding in the scope of the framework contract foreseen in the numbers 4, 5, and 6 of the article 23 of the Decree-Law 57/2016 of August 29, changed by Law 57/2017, of July 19. We also thank Rita Teles for the picture of her dog Barney.
References
- Ambrosini YM, Borcherding D, Kanthasamy A, Kim HJ, Willette AA, Jergens A, Allenspach K, Mochel JP (2019) The gut-brain axis in neurodegenerative diseases and relevance of the canine model: a review. Front Aging Neurosci 11:130. https://doi.org/10.3389/fnagi.2019.00130CrossRefGoogle Scholar
- Aronson SM (2005) The dancing cats of Minamata Bay. Med Health R I 88(7):209Google Scholar
- Atanaskova E, Nikolovski G, Ulčar I, Enimiteva V (2011) Examination of the content of heavy metals using hair samples in dogs of urban areas of Macedonia. Vet World 4(8):368–370. https://doi.org/10.5455/vetworld.2011.368-370CrossRefGoogle Scholar
- AVMA (2012) US pet ownership & demographics sourcebook. AVMA –American Veterinary Medical Association, SchaumburgGoogle Scholar
- Badea E, Goran GV, Matei E, Rotaru E, Crivineanu V (2016) Heavy metal and mineral content in the coat of cats in relationship with renal failure. Lucrari Stiintifice – Universitatea de Stiinte Agricole a Banatului Timisoara, Medicina Veterinara 49(1):17–28Google Scholar
- Badea E, Goran G, Țoca C, Crivineanu V (2018) Assessment of heavy metal and mineral levels in hair samples from dogs with mammary neoplasms. Bull UASVM Food Sci Technol 75(1). https://doi.org/10.15835/buasvmcn-fst:0007CrossRefGoogle Scholar
- Bernhardt ES, Rosi EJ, Gessner MO (2017) Synthetic chemicals as agents of global change. Front Ecol Environ 15(2):84–90. https://doi.org/10.1002/fee.1450CrossRefGoogle Scholar
- Berny PJ, Côté LM, Buck WB (1995) Can household pets be used as reliable monitors of lead exposure to humans? Sci Total Environ 172(2):163–173. https://doi.org/10.1016/0048-9697(95)04787-5CrossRefGoogle Scholar
- Bischoff K, Priest H, Mount-Long A (2010) Animals as sentinels for human lead exposure: a case report. J Med Toxicol 6(2):185–189. https://doi.org/10.1007/s13181-010-0014-9CrossRefGoogle Scholar
- Bukowski JA, Wartenberg D (1997) An alternative approach for investigating the carcinogenicity of indoor air pollution: pets as sentinels of environmental cancer risk. Environ Health Perspect 105(12):1312–1319. https://doi.org/10.1289/ehp.971051312CrossRefGoogle Scholar
- Caserta D, Graziano A, Monte GL, Bordi G, Moscarini M (2013) Heavy metals and placental fetal-maternal barrier: a mini-review on the major concerns. Eur Rev Med Pharmacol Sci 17(16):2198–2206Google Scholar
- Chen P, Miah MR, Aschner M (2016) Metals and neurodegeneration. F1000Research 5:F1000. Faculty Rev-1366. https://doi.org/10.12688/f1000research.7431.1CrossRefGoogle Scholar
- Cicek A, Koparal AS, Aslan A, Yazici K (2007) Accumulation of heavy metals from motor vehicles in transplanted lichens in an urban area. Commun Soil Sci Plan 39(1–2):168–176. https://doi.org/10.1080/00103620701759111CrossRefGoogle Scholar
- Clarkson TW, Magos L (2006) The toxicology of mercury and its chemical compounds. Crit Rev Toxicol 36(8):609–662. https://doi.org/10.1080/10408440600845619CrossRefGoogle Scholar
- D’Havé H, Covaci A, Scheirs J, Schepens P, Verhagen R, De Coen W (2005) Hair as an indicator of endogenous tissue levels of brominated flame retardants in mammals. Environ Sci Technol 39(16):6016–6020. https://doi.org/10.1021/es0507259CrossRefGoogle Scholar
- Doi R, Nakaya K, Ohno H, Yamashita K, Kobayashi T, Kasai S (1986) Metal content in the fur of domestic and experimental animals. Bull Environ Contam Toxicol 37(1):213–218. https://doi.org/10.1007/bf01607752CrossRefGoogle Scholar
- Druyan ME, Bass D, Puchyr R, Urek K, Quig D, Harmon E, Marquardt W (1998) Determination of reference ranges for elements in human scalp hair. Biol Trace Elem Res 62(3):183–197. https://doi.org/10.1007/bf02783970CrossRefGoogle Scholar
- Dunlap KL, Reynolds AJ, Bowers PM, Duffy LK (2007) Hair analysis in sled dogs (Canis lupus familiaris) illustrates a linkage of mercury exposure along the Yukon River with human subsistence food systems. Sci Total Environ 385(1):80–85. https://doi.org/10.1016/j.scitotenv.2007.07.002CrossRefGoogle Scholar
- Dwivedi SK, Swarup D, Dey S, Patra RC (2001) Lead poisoning in cattle and buffalo near primary lead-zinc smelter in India. Vet Hum Toxicol 43(2):93–94Google Scholar
- Ferrari CKB (2012) Effects of xenobiotics on total antioxidant capacity. Interdiscip Toxicol 5(3):117–122. https://doi.org/10.2478/v10102-012-0019-0CrossRefGoogle Scholar
- Finsterer J, Schöpper H, Breit S (2014) Steering and Communication: Nervous System and Sensory Organs. In: Jensen-Jarolim E (ed) Comparative medicine: anatomy and physiology. Springer Vienna, Vienna, pp 71–101. https://doi.org/10.1007/978-3-7091-1559-6_6CrossRefGoogle Scholar
- German AJ (2006) The growing problem of obesity in dogs and cats. J Nutr 136(7):1940S–1946S. https://doi.org/10.1093/jn/136.7.1940SCrossRefGoogle Scholar
- González-Gómez X, Cambeiro-Pérez N, Martínez-Carballo E, Simal-Gándara J (2018) Screening of organic pollutants in pet hair samples and the significance of environmental factors. Sci Total Environ 625:311–319. https://doi.org/10.1016/j.scitotenv.2017.12.270CrossRefGoogle Scholar
- Hansen JC, Danscher G (1995) Quantitative and qualitative distribution of mercury in organs from arctic sledgedogs: an atomic absorption spectrophotometric and histochemical study of tissue samples from natural long-termed high dietary organic mercury-exposed dogs from Thule, Greenland. Pharmacol Toxicol 77(3):189–195. https://doi.org/10.1111/j.1600-0773.1995.tb01011.xCrossRefGoogle Scholar
- Hayashi M, Okada I, Tate H, Miura Y, Ohhira S, Yamada Y (1981) Distribution of environmental pollutants in pet animals. VI. Heavy metals in hair of house-dogs. B Environ Contam Tox 26(1):60–64. https://doi.org/10.1007/bf01622055CrossRefGoogle Scholar
- Hayes HM, Tarone RE, Cantor KP, Jessen CR, McCurnin DM, Richardson RC (1991) Case-control study of canine malignant lymphoma: positive association with dog owner’s use of 2, 4-dichlorophenoxyacetic acid herbicides. JNCI J Natl Cancer Inst 83(17):1226–1231. https://doi.org/10.1093/jnci/83.17.1226CrossRefGoogle Scholar
- Head E, Moffat K, Das P, Sarsoza F, Poon WW, Landsberg G, Cotman CW, Murphy MP (2005) β-Amyloid deposition and tau phosphorylation in clinically characterized aged cats. Neurobiol Aging 26(5):749–763. https://doi.org/10.1016/j.neurobiolaging.2004.06.015CrossRefGoogle Scholar
- Keil DE, Berger-Ritchie J, McMillin GA (2011) Testing for toxic elements: a focus on arsenic, cadmium, lead, and mercury. Lab Med 42(12):735–742. https://doi.org/10.1309/lmykgu05bepe7iawCrossRefGoogle Scholar
- Klasing K, Goff J, Greger J, King J (2005) Mineral tolerance of animals, 2nd edn. (revised). National Academies Press, Washington, D.C.Google Scholar
- Kozak M, Kralova E, Sviatko P, Bilek J, Bugarsky A (2002) Study of the content of heavy metals related to environmental load in urban areas in Slovakia. Bratisl Lek Listy 103(7–8):231–237Google Scholar
- Kral T, Blahova J, Sedlackova L, Vecerek V, Svobodova Z (2015) Evaluation of mercury contamination in dogs using hair analysis. Neuro Endocrinol Lett 36(Suppl 1):68–72Google Scholar
- Lanocha N, Kalisinska E, Kosik-Bogacka D, Budis H (2012) Evaluation of dog bones in the indirect assessment of environmental contamination with trace elements. Biol Trace Elem Res 147(1):103–112. https://doi.org/10.1007/s12011-011-9315-3CrossRefGoogle Scholar
- Lieske CL, Moses SK, Castellini JM, Klejka J, Hueffer K, O’Hara TM (2011) Toxicokinetics of mercury in blood compartments and hair of fish-fed sled dogs. Acta Vet Scand 53(1):66. https://doi.org/10.1186/1751-0147-53-66CrossRefGoogle Scholar
- López-Alonso M, Miranda M, García-Partida P, Cantero F, Hernández J, Benedito JL (2007) Use of dogs as indicators of metal exposure in rural and urban habitats in NW Spain. Sci Total Environ 372(2–3):668–675CrossRefGoogle Scholar
- Martin MH, Coughtrey PJ (1982) Biological Monitoring of Heavy Metal Pollution: Land and Air. Springer, Dordrecht. ISBN 978-94-009-7354-1CrossRefGoogle Scholar
- Matsubara J, Machida K (1985) Significance of elemental analysis of hair as a means of detecting environmental pollution. Environ Res 38(2):225–238. https://doi.org/10.1016/0013-9351(85)90087-8CrossRefGoogle Scholar
- Merian E (1991) Metals and their compounds in the environment: occurrence, analysis and biological relevance, 2nd edn. VCH, CambridgeGoogle Scholar
- Mikulewicz M, Chojnacka K, Gedrange T, Górecki H (2013) Reference values of elements in human hair: a systematic review. Environ Toxicol Pharmacol 36(3):1077–1086. https://doi.org/10.1016/j.etap.2013.09.012CrossRefGoogle Scholar
- Minami A, Takeda A, Nishibaba D, Takefuta S, Oku N (2001) Cadmium toxicity in synaptic neurotransmission in the brain. Brain Res 894(2):336–339. https://doi.org/10.1016/S0006-8993(01)02022-4CrossRefGoogle Scholar
- Minganti V, Drava G (2018) Tree bark as a bioindicator of the presence of scandium, yttrium and lanthanum in urban environments. Chemosphere 193:847–851. https://doi.org/10.1016/j.chemosphere.2017.11.074CrossRefGoogle Scholar
- Needham LL, Sexton K (2000) Assessing children’s exposure to hazardous environmental chemicals: an overview of selected research challenges and complexities. J Expo Anal Env Epid 10(6 Pt 2):611–629CrossRefGoogle Scholar
- Neiger RD, Osweiler GD (1992) Arsenic concentrations in tissues and body fluids of dogs on chronic low-level dietary sodium arsenite. J Vet Diagn Investig 4(3):334–337. https://doi.org/10.1177/104063879200400318CrossRefGoogle Scholar
- Nikolovski G, Atanaskova E (2011) Use of canine hair samples as indicators of lead and cadmium pollution in the Republic of Macedonia. Bulg J Vet Med 14(1):57–61Google Scholar
- Nowak B, Chmielnicka J (2000) Relationship of lead and cadmium to essential elements in hair, teeth, and nails of environmentally exposed people. Ecotox Environ Safe 46(3):265–274. https://doi.org/10.1006/eesa.2000.1921CrossRefGoogle Scholar
- Nriagu JO (1988) A silent epidemic of environmental metal poisoning? Environ Pollut 50(1):139–161. https://doi.org/10.1016/0269-7491(88)90189-3CrossRefGoogle Scholar
- Nuttall KL (2006) Interpreting hair mercury levels in individual patients. Ann Clin Lab Sci 36(3):248–261Google Scholar
- Osweiler GD, Hovda L, Brutlag A, Lee JA (2011) Blackwell’s five-minute veterinary consult clinical companion: small animal toxicology. Wiley, New YorkGoogle Scholar
- Park SH, Lee MH, Kim SK (2005a) Studies on Cd, Pb, Hg and Cr values in dog hairs from Urban Korea. Asian-Australas J Anim Sci 18(8):1135–1140. https://doi.org/10.5713/ajas.2005.1135CrossRefGoogle Scholar
- Park SH, Lee MH, Kim SK (2005b) Studies on the concentrations of Cd, Pb, Hg and Cr in dog serum in Korea. Asian-Austral J Anim 18(11):1623–1627CrossRefGoogle Scholar
- Patrashkov SA, Petukhov VL, Korotkevich OS, Petukhov IV (2003) Content of heavy metals in the hair. J Phys IV France 107:1025–1027CrossRefGoogle Scholar
- Pollock C (2016) The canary in the coal mine. J Avian Med Surg 30(4):386–391, 386CrossRefGoogle Scholar
- Pozebon D, Scheffler GL, Dressler VL (2017) Elemental hair analysis: a review of procedures and applications. Anal Chim Acta 992:1–23. https://doi.org/10.1016/j.aca.2017.09.017CrossRefGoogle Scholar
- Rashed MN, Soltan ME (2005) Animal hair as biological indicator for heavy metal pollution in urban and rural areas. Environ Monit Assess 110(1):41–53. https://doi.org/10.1007/s10661-005-6288-8CrossRefGoogle Scholar
- Reif JS (2011) Animal sentinels for environmental and public health. Public Health Rep 126(1_suppl):50–57. https://doi.org/10.1177/00333549111260S108CrossRefGoogle Scholar
- Reif JS, Dunn K, Ogilvie GK, Harris CK (1992) Passive smoking and canine lung cancer risk. Am J Epidemiol 135(3):234–239. https://doi.org/10.1093/oxfordjournals.aje.a116276CrossRefGoogle Scholar
- Rodriguez Castro MC, Andreano V, Custo G, Vázquez C (2013) Potentialities of total reflection X-ray fluorescence spectrometry in environmental contamination: hair of owned dogs as sentinel of arsenic exposure. Microchem J 110:402–406. https://doi.org/10.1016/j.microc.2013.05.009CrossRefGoogle Scholar
- Rodushkin I, Axelsson MD (2000) Application of double focusing sector field ICP-MS for multielemental characterization of human hair and nails. Part II. A study of the inhabitants of northern Sweden. Sci Total Environ 262(1):21–36. https://doi.org/10.1016/S0048-9697(00)00531-3CrossRefGoogle Scholar
- Ruiz-Suárez N, Rial C, Boada LD, Henríquez-Hernández LA, Valeron PF, Camacho M, Zumbado M, Almeida González M, Lara P, Luzardo OP (2016) Are pet dogs good sentinels of human exposure to environmental polycyclic aromatic hydrocarbons, organochlorine pesticides and polychlorinated biphenyls? J Appl Anim Res 44(1):135–145. https://doi.org/10.1080/09712119.2015.1021808CrossRefGoogle Scholar
- Russo D, Ancillotto L (2015) Sensitivity of bats to urbanization: a review. Mamm Biol 80(3):205–212. https://doi.org/10.1016/j.mambio.2014.10.003CrossRefGoogle Scholar
- Rzymski P, Niedzielski P, Poniedziałek B, Rzymski P, Pacyńska J, Kozak L, Dąbrowski P (2015) Free-ranging domestic cats are characterized by increased metal content in reproductive tissues. Reprod Toxicol 58:54–60. https://doi.org/10.1016/j.reprotox.2015.08.004CrossRefGoogle Scholar
- Sakai T, Ito M, Aoki H, Aimi K, Nitaya R (1995) Hair mercury concentrations in cats anddogs in Central Japan. Br Vet J 151(2):215–219. https://doi.org/10.1016/S0007-1935(95)80013-1CrossRefGoogle Scholar
- Santorufo L, Van Gestel CAM, Rocco A, Maisto G (2012) Soil invertebrates as bioindicators of urban soil quality. Environ Pollut 161:57–63. https://doi.org/10.1016/j.envpol.2011.09.042CrossRefGoogle Scholar
- Schramm K-W (1997) Hair: a matrix for non-invasive biomonitoring of organic chemicals in mammals. B Environ Contam Tox 59(3):396–402. https://doi.org/10.1007/s001289900491CrossRefGoogle Scholar
- Schramm KW (2008) Hair-biomonitoring of organic pollutants. Chemosphere 72(8):1103–1111. https://doi.org/10.1016/j.chemosphere.2008.04.017CrossRefGoogle Scholar
- Skibniewski M, Kośla T, Skibniewska E (2013) Domestic cat (Felis catus) as a bioindicator of environmental lead contamination/Kot domowy (Felis catus) jako bioindykator zanieczyszczenia środowiska ołowiem. Ochrona Srodowiska i Zasobów Naturalnych 24(4):47. https://doi.org/10.2478/oszn-2013-0043CrossRefGoogle Scholar
- Sousa ACA, de Sá Teixeira IS, Marques B, Vilhena H, Vieira L, Soares AMVM, Nogueira AJA, Lillebø AI (2013) Mercury, pets’ and hair: baseline survey of a priority environmental pollutant using a noninvasive matrix in man’s best friend. Ecotoxicology 22(9):1435–1442. https://doi.org/10.1007/s10646-013-1130-5CrossRefGoogle Scholar
- Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. In: Luch A (ed) Molecular, clinical and environmental toxicology, Environmental toxicology, vol 3. Springer Basel, Basel, pp 133–164. https://doi.org/10.1007/978-3-7643-8340-4_6CrossRefGoogle Scholar
- Tomza-Marciniak A, Pilarczyk B, Bakowska M, Ligocki M, Gaik M (2012) Lead, cadmium and other metals in serum of pet dogs from an urban area of NW Poland. Biol Trace Elem Res 149(3):345–351. https://doi.org/10.1007/s12011-012-9433-6CrossRefGoogle Scholar
- Tsuchiya K (1992) Historical perspectives in occupational medicine. The discovery of the causal agent of minamata disease. Am J Ind Med 21(2):275–280. https://doi.org/10.1002/ajim.4700210215CrossRefGoogle Scholar
- UNEP (2013) Environmental risks and challenges of anthropogenic metals flows and cycles. A report of the Working Group on the Global Metal Flows to the International Resource PanelGoogle Scholar
- van Helden PD, van Helden LS, Hoal EG (2013) One world, one health. Humans, animals and the environment are inextricably linked – a fact that needs to be remembered and exploited in our modern approach to health. EMBO Rep 14(6):497–501. https://doi.org/10.1038/embor.2013.61CrossRefGoogle Scholar
- Vázquez C, Palacios O, Boeykens S, Parra LMM (2013) Domestic dog hair samples as biomarkers of arsenic contamination. X-Ray Spectrom 42(4):220–223. https://doi.org/10.1002/xrs.2487CrossRefGoogle Scholar
- Wallis LJ, Szabó D, Erdélyi-Belle B, Kubinyi E (2018) Demographic change across the lifespan of pet dogs and their impact on health status. Front Vet Sci 5:200. https://doi.org/10.3389/fvets.2018.00200CrossRefGoogle Scholar
- WHO (2013) Aging and life course. World Health Organization, GenevaGoogle Scholar
- WHO (2019) Risk reduction of cognitive decline and dementia: WHO guidelines. World Health Organization, GenevaGoogle Scholar
- Wolfe M, Norman D (1998) Effects of waterborne mercury on terrestrial wildlife at clear lake: evaluation and testing of a predictive model. Environ Toxicol Chem 17(2):214–227. https://doi.org/10.1002/etc.5620170213CrossRefGoogle Scholar
- Wołowiec P, Michalak I, Chojnacka K, Mikulewicz M (2013) Hair analysis in health assessment. Clin Chim Acta 419:139–171. https://doi.org/10.1016/j.cca.2013.02.001CrossRefGoogle Scholar
- Yoshinaga J, Morita M, Okamoto K (1997) New human hair certified reference material for methylmercury and trace elements. Fresenius J Anal Chem 357(3):279–283. https://doi.org/10.1007/s002160050153CrossRefGoogle Scholar
- Zaccaroni A, Corteggio A, Altamura G, Silvi M, Di Vaia R, Formigaro C, Borzacchiello G (2014) Elements levels in dogs from “triangle of death” and different areas of Campania region (Italy). Chemosphere 108:62–69. https://doi.org/10.1016/j.chemosphere.2014.03.041CrossRefGoogle Scholar