Concentration of blood heavy metals in terrier dogs with some common behavior problems

Iranian Journal of Veterinary Science and Technology

دوره 17، شماره 2 - شماره پیاپی 39، شهریور 2025، صفحه 69-77   

نوع مقاله: Research Article

شناسه دیجیتال (DOI): 10.22067/ijvst.2025.90435.1434

نویسندگان

Raha Bayazi؛ Mohammad Heidarpour؛ Mohammad Azizzadeh؛ Javad khoshnegah^*

Department of Clinical Sciences, School of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran.

چکیده

Behavioral disorders in companion animals, especially dogs, are a great concern. Due to the relationship between oxidative stress and behavior problems and also heavy metals’ capability of creating oxidative stress, in the current study, the effects of lead, mercury, arsenic, and cadmium on 13 common canine behavior problems (fearfulness, excessive barking, destructiveness, house soiling, inappropriate sexual behavior, coprophagia, wandering, shyness, aggression toward the owner, aggression toward familiar people, aggression toward strangers, aggression toward other dogs, and excessive activity) were evaluated. According to owners’ answers to the questionnaire, 43 terrier dogs were chosen. Of these 7 dogs showed no behavior problem and 36 dogs displayed at least one behavior problem. The blood concentrations of lead, mercury, arsenic, and cadmium were measured using Inductively Coupled Plasma Optical Emission Spectroscopy (ICP-OES). No significant differences in heavy metal concentrations were observed between the case and control groups. However, the cadmium concentration was significantly elevated in dogs displayed aggressive behavior toward their owners (p < 0.048, n=5). while arsenic level was significantly lower in dogs displaying fearfulness (p = 0.048, n= 25). Results of the study reported here do not support the hypothesis that “blood concentration of heavy metals may influence the occurrence or prevention of common behavioral problems in dogs”. Our results suggest that there may be a direct relationship between higher levels of cadmium and aggression toward the owner and arsenic with reduced fearfulness in dogs. However, we have to consider that the behavioral effects of heavy metals are likely very complex. 

کلیدواژه‌ها

Behavior problem؛ Terrier dog؛ Cadmium؛ Lead؛ Mercury؛ Arsenic

سایر فایل های مرتبط با مقاله

8-1434-persian abs-F.pdf

ferdousi-8.xml

مراجع

1.  Amat M, de la Torre JLR, Fatjó J, Mariotti VM, Van Wijk S, Manteca X. Potential risk factors associated with feline behavior problems. Applied Animal Behaviour Science. 2009; 21: 134-39.Doi:10.1016/j.applanim.2009.09.012.
2.  Khoshnegah J, Azizzadeh M, Mahmoodi Gharaie A. Risk factors for the development of behavior problems in a population of Iranian domestic dogs: Results of a pilot survey. Applied Animal Behaviour Science. 2011; 131 (3-4): 123-130. Doi:10.1016/j.applanim.2011.02.003.
3. Wells DL, Hepper PG. Prevalence of behavior problems reported by owners of dogs purchased from an animal rescue shelter. Applied Animal Behaviour Science.  2000; 69(1): 55-65. Doi:10.1016/S0168-1591(00)00118-0.
4. Gazzano A, Mariti C, Alvares S, Cozzi A, Tognetti R, Sighieri C. The prevention of undesirable behaviors in dogs: effectiveness of veterinary behaviorists' advice given to puppy owners. Journal of Veterinary Behaviour. 2008; 3(3):125-133. Doi:10.1016/j.jveb.2008.04.004.
5. Maffeo NN, Springer CM, Albright JD. A retrospective study on the clinical use and owner perception of venlafaxine efficacy as part of a multimodal treatment for canine fear, anxiety, and aggression. Journal of Veterinary Behaviour. 2023; 64–65, 54-59.Doi:10.1016/j.jveb.2023.06.004.
6. Martínez L, Jiménez V, García-Sepúlveda C, Ceballos F, Delgado JM, Niño-Moreno P, Jiménez-Capdeville M. Impact of early developmental arsenic exposure on promotor CpG-island methylation of genes involved in neuronal plasticity. Neurochem. Int. 2011; 58(5): 574-581. Doi:10.1016/j.neuint.2011.01.020.
7. Mason LH, Harp JP, Han DY. Pb neurotoxicity: neuropsychological effects of lead toxicity. BioMed Research International. 2014. Doi:10.1155/2014/840547.
8. Esposito M, De Roma A, Maglio P, Sansone D, Picazio G, Bianco R, Martinis DC0 Rosato G, Baldi L, Gallo P. Heavy metals in organs of stray dogs and cats from the city of Naples and its surroundings (Southern Italy). Environmental Science and Pollution Research. 2019; 26, 3473-3478. Doi:10.1007/s11356-018-3838-5.
9. Hassanien MA, Shahawy AME. Environmental heavy metals and mental disorders of children in developing countries. In Environmental Heavy Metal Pollution and Effects on Child Mental Development: Risk Assessment and Prevention Strategies. Springer Netherlands. 2011; 1-25. Doi:10.1007/978-94-007-0253-0_1.
10. Jaishankar M, Tseten T, Anbalagan N, Mathew BB, Beeregowda KN. Toxicity, mechanism and health effects of some heavy metals. Interdisciplinary Toxicology. 2014; 7(2): 60-72. Doi: 10.2478/intox-2014-0009.
11. Kuivenhoven M, Mason K. Arsenic Toxicity. Stat Pearls. Stat Pearls Publishing, Treasure Island (FL). 2019  https://europepmc.org/article/NBK/nbk541125.
12. Yang J, Langford F, Kiddie J. Risk factors for aggressive behaviour in domestic dogs (Canis familiaris), as reported by owners in mainland China. Applied Animal Behaviour Science. 2021; 234, 105211. Doi:10.1016/j.applanim.2020.105211.
13. Wismer T. Chapter 53 - Lead In ME Peterson, PA Talcott, editors Small Animal Toxicology (Philadelphia, PA: W.B. Saunders) (2013), 609–615.
14. Terçariol SG, Almeida AA, Godinho AF. Cadmium and exposure to stress increase aggressive behavior. Environ. Toxicology and Applied Pharmacology. 2011; 32(1): 40-45. Doi:10.1016/j.etap.2011.03.005.
15. Godinho AF, de Souza RP, Anselmo F, Silva NCC. Cadmium and Caffeine in Co-exposure but Not Alone, in Low Doses, Modulate Aggression Behavior in Rats. Journal of caffeine research. 2017; 7(1): 31-36. Doi:10.1089/jcr.2016.0016.
16. Mfem CC, SA S, Oyama SE. Effects of Heavy Metal Toxicity on Anxiety Disorder. Journal of Biomedical Research & Environmental. 2021; 2(8): 660-668. Doi:10.37871/jbres1294.
17. Alanazi MM, Ansari MA, Nadeem A, Attia SM, Bakheet SA, Al-Mazroua HA, Ahmad SF. Cadmium Exposure Is Associated with Behavioral Deficits and Neuroimmune Dysfunction in BTBR T+ Itpr3tf/J Mice. International Journal of Molecular Sciences. 2023; 24(7): 6575. Doi:10.3390/ijms24076575. 
18. Dési, I., Nagymajtényi, L. and Schulz, H. (1998) Behavioural and Neurotoxicological Changes Caused by Cadmium Treatment of Rats during Development. Journal of Applied Toxicology, 18, 63-70. Doi:10.1002/(SICI)1099-1263(199801/02)18:1<63::AID-JAT475>3.0.CO;2-Z.
19. Tolins M, Ruchirawat M, Landrigan,P. The developmental neurotoxicity of arsenic: cognitive and behavioral consequences of early life exposure. Annals of Global Health. 2014; 80(4): 303-14. Doi:10.1016/j.aogh.2014.09.005.
20. Tyler CR,  Allan AM. The Effects of Arsenic Exposure on Neurological and Cognitive Dysfunction in Human and Rodent Studies: A Review . Current Environmental Health Reports. 2014; 21;1(2):132-147.  Doi: 10.1007/s40572-014-0012-1. 
21. Cronican AA, Fitz NF, Carter A, Saleem M, Shiva S, Barchowsky A, Lefterov I. Genome-wide alteration of histone H3K9 acetylation pattern in mouse offspring prenatally exposed to arsenic. PloS one. 2013; 8(2): e53478. Doi:10.1371/journal.pone.0053478.
22. Niño SA, Martel-Gallegos G, Castro-Zavala A, Ortega-Berlanga B, Delgado JM, Hernández-Mendoza H, ZarazúaS. Chronic arsenic exposure increases Aβ (1–42) production and receptor for advanced glycation end products expression in rat brain. Chemical Research in Toxicology. 2018; 31(1): 13-21. Doi:10.1021/acs.chemrestox.7b00215.
23. Oostra B, Nelson DL. Animal models of fragile X syndrome: mice and flies. Genetic instabilities and neurological diseases. 2006; 175-193. Doi:10.1016/B978-012369462-1/50012-0.
24. Bratel J, Haraldson T, Ottosson JO. Potential side effects of dental amalgam restorations: (II). No relation between mercury levels in the body and mental disorders. European Journal of Oral Sciences. 1997; 105(3): 244-250. Doi:10.1111/j.1600-0722.1997.tb00207.x.
25. Lozano M, Murcia M, Soler-Blasco R, González L, Iriarte G, Rebagliato M, Llop S. Exposure to mercury among 9-year-old children and neurobehavioural function. Environment International. 2021.146: 106173. Doi:10.1016/j.envint.2020.106173.
26- Fisher JF, World Health Organization. Elemental mercury and inorganic mercury compounds: human health aspects. WHO. 2003; 17-25. https://www.who.int/publications/i/item/elemental-mercury-and-inorganic-mercury-compounds-human-health-aspects. 
27. Bruna Fernandes Azevedo  1 , Lorena Barros Furieri, Franck Maciel Peçanha, Giulia Alessandra Wiggers, Paula Frizera Vassallo, Maylla Ronacher Simões, Jonaina Fiorim, Priscila Rossi de Batista, Mirian Fioresi, Luciana Rossoni, Ivanita Stefanon, María Jesus Alonso, Mercedes Salaices, Dalton Valentim Vassallo, Toxic effects of mercury on the cardiovascular and central nervous systems. J Biomed Biotechnol. 2012:2012:949048.  Doi: 10.1155/2012/949048. 
28. Vänskä M, Diab SY, Perko K, Quota SR, Albarqouni NM, Myöhänen A, Manduca P. Toxic environment of war: maternal prenatal heavy metal load predicts infant emotional development. Infant Behavior & Development. 2019; 55, 1-9. Doi:10.1016/j.infbeh.2019.01.002.
29. Nkomo P, Naicker N, Mathee A, Galpin J, Richter LM, Norris SA. The association between environmental lead exposure with aggressive behavior, and dimensionality of direct and indirect aggression during mid-adolescence: Birth to Twenty Plus cohort. Science of the Total Environment. 2018; 612: 472-479. Doi:10.1016/j.scitotenv.2017.08.138.
30. Al Osman M, Yang F, Massey IY. Exposure routes and health effects of heavy metals on children. Biometals. 2019; 32: 563-573. Doi:10.1007/s10534-019-00193-5.
31. Bouchard MF, Bellinger DC, Weuve J, Matthews-Bellinger J, Gilman SE, Wright RO, Weisskopf MG. Blood Lead Levels and Major Depressive Disorder, Panic Disorder, and Generalized Anxiety Disorder in US Young Adults. Arch. Gen. Psychiatry. Archives of General Psychiatry. 2009; 66(12): 1313–1319. Doi:10.1001/archgenpsychiatry.2009.164.
32. McClelland SC, Ribeiro RD, Mielke HW, Finkelstein ME, Gonzales CR, Jones JA, Karubian J. Sub-lethal exposure to lead is associated with heightened aggression in an urban songbird. Science of the total environment. 2018; 654: 593-603. Doi:10.1016/j.scitotenv.2018.11.145.
33. Lee MJ, Chou MC, Chou WJ, Huang CW, Kuo HC, Lee SY, Wang LJ, Heavy metals’ effect on susceptibility to attention-deficit/hyperactivity disorder: implication of lead, cadmium, and antimony. International Journal of Environmental Research and Public Health. 2018; 15(6), 1221. Doi:10.3390/ijerph15061221.
34 . Rosendahl S, Anturaniemi J, Vuori KA, Moore R, Hemida M, Hielm-Björkman A. Diet and dog characteristics affect major and trace elements in hair and blood of healthy dogs. Vet Res Commun. (2022) 46:261–75. Doi: 10.1007/s11259-021-09854-8.