Stress and Cancer in Dogs: Comparison Between a Population of Dogs Diagnosed with Cancer and a Control Population - A Pilot Study

Open access

Abstract

It is widely accepted that psychological stress and mental illness can compromise the function of the immune system. Clinical and epidemiological studies on humans recognized that specific psychosocial factors, such as stress, chronic depression and lack of social support are risk factors for the development and progression of cancer. Unfortunately, most of the animals studies on this subject are based on laboratory tests performed on mice. This retrospective cohort study aims to analyze the relation between stress and tumor in pet dogs, by evaluating and comparing the stress level in two groups of 69 dogs each, balanced for sex and age: the oncologic group consists of dogs diagnosed with cancer and the control group consists of healthy dogs. Our results show that, before the cancer diagnosis, more dogs in the oncologic group faced changes in their household and routine as opposed to the control group (p<0.05). More dogs of the oncologic group than the control group also showed signs of stress and anxiety, before the cancer diagnosis (p<0.05). As reported by their owners, these included attention seeking, hiding without a specific reason, following the owner around the house, hyper-vigilance, fear of fireworks and gunshots, biting, aggression towards other dogs, licking and chewing excessively parts of their body. Our results are aligned with the evidence from human research, indicating that dogs with cancer are significantly more likely to have shown signs of stress compared to the control dogs during their life.

1. Leonard, B.E., Song, C. (1996). Stress and the Immune System in the Etiology of Anxiety and Depression. Pharmacol. Biochem. Behav. 54 (1): 299-303. http://dx.doi.org/10.1016/0091-3057(95)02158-2

2. Graham, J., Ramirez, A., Love, S., Richards, M., Burgess, C. (2002). Stressful life experiences and risk of relapse of breast cancer: observational cohort study. Brit. Med. J. 324 (7351): 1420-1424. http://dx.doi.org/10.1136/bmj.324.7351.1420 PMid:12065263 PMCid:PMC115851

3. Lillberg, K., Verkasalo, P. K., Kaprio, J., Teppo, L., Helenius, H., Koskenvuo, M. (2003). Stressful life events and risk of breast cancer in 10,808 women: a cohort study. Am. J. Epidemiol. 157 (5): 415-423. http://dx.doi.org/10.1093/aje/kwg002 PMid:12615606

4. Kyrou, I., Tsigos, C. (2007). Stress mechanisms and metabolic complications. Horm. Metab. Res. 39 (6): 430-438. http://dx.doi.org/10.1055/s-2007-981462 PMid:17578760

5. Kruk, J., Aboul-Enein, H.Y. (2004). Psychological stress and the risk of breast cancer: a case-control study. Cancer Detect. Prev. 28 (6): 399-408. http://dx.doi.org/10.1016/j.cdp.2004.07.009 PMid:15582263

6. Armaiz-Pena, G.N., Lutgendorf, S.K., Cole, S.W., Sood, A.K. (2009). Neuroendocrine modulation of cancer progression. Brain Behav. Immun. 23 (1): 10–15. http://dx.doi.org/10.1016/j.bbi.2008.06.007 PMid:18638541 PMCid:PMC2630522

7. Lutgendorf, S.K., Sood A. K. (2011). Biobehavioral factors and cancer progression: physiological pathways and mechanisms. Psychosom. Med. 73(9): 724–730. http://dx.doi.org/10.1097/PSY.0b013e318235be76 PMid:22021459 PMCid:PMC3319047

8. Rabin, B.S (1999). Stress, immune function and health: the connection. New York, NY: Wiley-Liss Sons Inc.

9. Yang, E.V., Glaser, R. (2003). Stress-induced immunomodulation: implication for tumorigenesis. Brain Behav. Immun. 17, 37-40. http://dx.doi.org/10.1016/S0889-1591(02)00064-8

10. Reiche, E.M., Nunes, S.O., Morimoto, H.K. (2004). Stress, depression, the immune system, and cancer. Lancet Oncol. 5, 617–625. http://dx.doi.org/10.1016/S1470-2045(04)01597-9

11. Azpiroz, A., De Miguel, Z., Fano E. Vegas O. (2008). Relations between different coping strategies for social stress, tumor development and neuroendocrine and immune activity in male mice. Brain, Behav. Immun. 22, 690-698. http://dx.doi.org/10.1016/j.bbi.2007.10.007 PMid:18061400

12. Selye, H. (1936). A syndrome produced by diverse nocious agentes. Nature 138, 32. http://dx.doi.org/10.1038/138032a0

13. Neylan, T. C. (1998). Hans Selye and the field of stress research. Neuropsychiatry Classics 10 (2): 230-231. http://dx.doi.org/10.1176/jnp.10.2.230

14. Breazile, J.E. (1987). Physiologic basis and consequences of distress in animals. J. A. V. M. A. 191 (10): 1212-1215.

15. Casey, R. (2002). Fear and stress in companion animals. In: D. Horwitz, D. Mills, S. Heath, (Eds.), BSAVA Manual of Canine and Feline Behavioural Medicine (pp. 144–153). Gloucester, UK: British Small Animal Veterinary Association PMid:12124759

16. Le Roith, D., Shiloach, J., Roth, J. (1982). Is there an earlier phylogenetic precursor that is common to both the nervous and endocrine systems? Peptides 3, 211-215. http://dx.doi.org/10.1016/0196-9781(82)90080-8

17. Black, H.P. (1994). Immune system-central nervous system interaction: effect and immunomodulatory consequences of immune system mediators on the brain. Antimicrob. Agents Ch. 38 (1): 7-12. http://dx.doi.org/10.1128/AAC.38.1.7

18. Dantzer, R., Kelley, K.W. (1989). Stress and immunity: an integrated view of relationships between the brain and the immune system. Life Sci. 44 (26): 1995-2008. http://dx.doi.org/10.1016/0024-3205(89)90345-7

19. Dunn, G. P., Old, L. J., Schreiber, R. D. (2004). The immunobiology of cancer immunosurveilance and immunoediting. Immunity 21, 137-148. http://dx.doi.org/10.1016/j.immuni.2004.07.017 PMid:15308095

20. Lang, K., Entschladen, F., Weidt, C., Zaenker, K. (2006). Tumor immune escape mechanisms: impact of the neuroendocrine system. Cancer Immunol. Immun. 55 (7): 749-776. http://dx.doi.org/10.1007/s00262-006-0126-x PMid:16435128

21. Antoni, M.H., Lutgendorf, S.K., Cole, S.W., Dhabhar, F.S., Sephton, S.E., Green McDonalc, P., Stefanek, M., Sood Anil, K. (2006). The influence of bio-behavioural factors on tumours biology: pathways and mechanisms. Nat. Rev. Cancer 6 (3): 240-248. http://dx.doi.org/10.1038/nrc1820 PMid:16498446 PMCid:PMC3146042

22. Ben-Eliyahu, S. (2003). The promotion of tumor metastasis by surgery and stress: Immunological basis and implication for psychoneuroimmunology. Brain Behav. Immun. 17, 27-37. http://dx.doi.org/10.1016/S0889-1591(02)00063-6

23. Thaker, P.H., Sood, A.K. (2008). Neuroendocrine influences on cancer biology. Semin. Cancer Biol. 164-170. http://dx.doi.org/10.1016/j.semcancer.2007.12.005

24. Kiecolt-Glaser, J.K., Preacher, K.J., MacCallum, R.C., Atkinson, C., Malarkey, W.B., Glaser, R. (2003). Chronic stress and age-related increases in the proinflammatory cytokine IL-6. Proceedings of the National Academy of Sciences, 100, (pp. 9090-9095). US http://dx.doi.org/10.1073/pnas.1531903100 PMid:12840146 PMCid:PMC166443

25. Mills, D. S., Dube, M. B., Zulch, H. (2012). Stress and pheromonatherapy in small animal clinical behaviour. Oxford: Wiley-Blackwell. http://dx.doi.org/10.1002/9781118702642

26. Mills, D., Karagiannis, C., Zulch, H. (2014). Stress-Its effects on health and behavior: A guide for practitioners. Vet. Clin. N. Am. Small. 44(3): 525-541. http://dx.doi.org/10.1016/j.cvsm.2014.01.005 PMid:24766698

27. Overall, K.L. (1997). Clinical behavioral medicine for small animals (pp. 209-250). St. Louis: Mosby-Year Book Inc.

28. Berteselli, G., Servida, F., Dall’Ara, P., Verga, M., Piola, E., Puricelli, M., Palestrini, C., (2005). Evaluation of immunological, stress and behavioural parameters in dogs (Canis familiaris) with anxiety-related disorders. In: D. Mills, E. Levine, G. Landsberg, A.E. Horwitz, A.E. Duxbury (Eds.), Current Issues and Research in Veterinary Behavioral Medicine (pp. 18–22). USA: Purdue Press.

29. Debenedetti, A. (1998). Endocrinologia. In: G. Aguggini, V. Beghelli, L. F. Giulio (Eds), Fisiologia degli Animali Domestici (pp. 645-748). Torino: UTET.

30. Veissier, I., Boissy, A. (2007). Stress and welfare: two complementary concepts that are intrinsically related to the animal’s point of view. Physiol. Behav. 92 (3): 429-433. http://dx.doi.org/10.1016/j.physbeh.2006.11.008 PMid:17182067

31. Overall, K. L. (2000). Natural animal models of human psychiatric conditions: assessment of mechanism and validity. Prog. Neuro-Psychoph. 24(5): 727-776. http://dx.doi.org/10.1016/S0278-5846(00)00104-4

32. Takahashi, T., Ikeda, K., Ishikawa, M., Kitamura, N., Tsukasaki, T., Nakama, D., Kameda, T. (2005). Anxiety, reactivity, and social stress-induced cortisol elevation in humans. Neuroendocrinol. Lett. 26(4): 351-354. PMid:16136010

33. MacEwen, E. G. (1990). Spontaneous tumors in dogs and cats: models for the study of cancer biology and treatment. Cancer Metast. Rev. 9 (2): 125-136. http://dx.doi.org/10.1007/BF00046339 PMid:2253312

34. Vail, D.M., MacEwen, E.G. (2000). Spontaneously occurring tumors of companion animals as models for human cancer. Cancer Invest. 18 (8): 781-792. http://dx.doi.org/10.3109/07357900009012210 PMid:11107448

35. Borgatti, A, Buracco, P. (2009). Un legame che va oltre l’amicizia: cane, uomo ed oncologia comparata. Veterinaria. 23 (2): 9-25.

36. Lagadic, M. (2006). I diversi fattori predisponenti le neoplasie. In: AA. Vv., Oncologia pratica del cane e del gatto (pp 9-13). Collana di Summa - animali da compagnia. Milano: Le Point Vétérinaire Italie.

37. Glaser, R., Kiecolt-Glaser, J. (2005). Stress-induced immune dysfunction: implications for health. Nat. Rev. Immunol. 5, 243-251. http://dx.doi.org/10.1038/nri1571 PMid:15738954

38. Danzer, R., Mormede, P. (1981). Pituitary adrenal consequence of adjunctive behaviours in pigs. Horm. Behav. 15, 386-395. http://dx.doi.org/10.1016/0018-506X(81)90003-9

39. Ohl, F., Arndt, S. S., van der Staay, F. J. (2008). Pathological anxiety in animals. Vet. J. 175, 18-26. http://dx.doi.org/10.1016/j.tvjl.2006.12.013 PMid:17321766

40. Cannas, S., Frank, D., Minero, M., Aspesi, A., Benedetti, R., Palestrini, C. (2014). Video analysis of dogs suffering from anxiety when left home alone and treated with clomipramine. Journal of Veterinary Behavior: Clinical Applications and Research 9(2): 50-57. http://dx.doi.org/10.1016/j.jveb.2013.12.002

41. Godbout, M., Beauchamp, G., Palestrini, C., Frank, D. (2007). Puppy behavior at the veterinary clinic: a pilot study. J. Vet. Behav.: Clin. Appl. Res. 2, 126-135. http://dx.doi.org/10.1016/j.jveb.2007.06.002

42. Palestrini, C., Minero, M., Cannas, S., Rossi, E., Frank, D. (2010a). Video analysis of dogs with separation-related behaviors. Appl. Anim. Behav. Sci. 124, 61e67

43. Flannigan, G., Dodman, N. H. (2001). Risk factors and behaviors associated with separation anxiety in dog. J. A. V. M. A. 219 (4): 460-466. http://dx.doi.org/10.2460/javma.2001.219.460

44. McGreevy, P. D., Masters, A. M. (2008). Risk factors of separation-related distress and feed-related aggression in dogs: additional findings from a survey in Australian dog owners. Appl. Anim. Behav. Sci. 109, 320-328. http://dx.doi.org/10.1016/j.applanim.2007.04.001

45. Godbout, G.P., Glaser, R. (2006). Stress-induced immune dysregulation: implications for wound healing, infectious disease and cancer. J. Neuroimmune Pharmacol. 1 (4): 421-427. http://dx.doi.org/10.1007/s11481-006-9036-0 PMid:18040814

46. MacEwen, B. S. (2008). Central effects of stress hormones in health and disease: understanding the protective and damaging effects of stress and stress mediators. Eur. J. Pharmacol. 583 (2-3): 174–185. http://dx.doi.org/10.1016/j.ejphar.2007.11.071 PMid:18282566 PMCid:PMC2474765

47. Skandarkumar, S., Stodulski, G., Hau, J. (1995). Salivary IgA: a possible stress marker in dogs. Anim. Welfare 4 (4): 339-350.

48. Beerda, B., Schilder, M.B.H., van Hooff, J.A.R.A.M., de Vries, H.W., Mol, J.A. (2000). Behavioural and hormonal indicators of enduring environmental stress in dogs. Anim. Welfare 9, 49-62.

49. Yang, Y., Koh, D., Ng V., Lee, C.Y., Dong, F., Goh, S.H., Anantharaman, V., Chia, S.E. (2002). Self-perceived work related stress and the relation with salivary IgA and Lysozyme among emergency department nurses. Occup. Environ. Med. 59, 836-841. http://dx.doi.org/10.1136/oem.59.12.836 PMid:12468751 PMCid:PMC1763606

50. Ng, V., Koh, D., Mok, B.Y.Y., Chia, S.E., Lim, L.P. (2003). Salivary biomarkers associated with academic assessment stress among dental undergraduates. J. Dent. Edu. 67(10): 1091-1094. PMid:14587673

51. Frick, L.R., Rapanelli, M., Cremaschi, G. A., Genaro, A. M. (2009). Fluoxetine directly counteracts the adverse effects of chronic stress on T cell immunity by compensatory and specific mechanisms. Brain Behav. Immun. 23 (1): 36-40. http://dx.doi.org/10.1016/j.bbi.2008.06.010 PMid:18625298

Macedonian Veterinary Review

The Journal of the Faculty of Veterinary Medicine-Skopje at the Ss. Cyril and Methodius University in Skopje

Journal Information


CiteScore 2017: 0.32

SCImago Journal Rank (SJR) 2017: 0.195
Source Normalized Impact per Paper (SNIP) 2017: 0.387

Cited By

Metrics

All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 93 93 12
PDF Downloads 22 22 5