DOI QR코드

DOI QR Code

Canine Lymphoma as a Possible Human Lymphoma Model: A Case-Series Study

  • Kiavash Hushmandi (Division of Epidemiology & Zoonoses, Department of Food Hygiene and Quality Control, Faculty of Veterinary Medicine, University of Tehran ) ;
  • Saied Bokaie (Division of Epidemiology & Zoonoses, Department of Food Hygiene and Quality Control, Faculty of Veterinary Medicine, University of Tehran ) ;
  • Darioush Shirani (Department of Small Animals Internal Medicine, Faculty of Veterinary Medicine, University of Tehran) ;
  • Ali Taghipour (Department of Veterinary Clinical Sciences, Karaj Branch, Islamic Azad University)
  • Received : 2023.04.22
  • Accepted : 2023.05.30
  • Published : 2023.06.30

Abstract

Canine lymphoma (cL) is the most common hematopoietic cancer in dogs. Various determinants have been evaluated to find the predisposing factors in both human and canine lymphoma. Due to common risk factors and similar pathways, cL is considered a potential model for non-Hodgkin lymphoma (NHL) in humans. In this case-series study, major hospitals in Tehran consented to take part in this study and between the years of 2020-2022, provided us with 52 cL cases which were approved by the attended pathologist. We designed a questionnaire and collected information about the dogs and their owners. Most of the owners were women, young (younger than 50 years old), had at least diplomas and interestingly were housewives or househusbands. Male dogs with middle to old age (more than 6 years) were mostly referred. The most common characteristics were neutered, normal BCS, purebred, urban but not industrial residence, previous tobacco smoke exposure but no history of previous fungicide or pesticide exposure. Also, most of them did not have any previous autoimmune or immunosuppressive diseases. Presented characteristics should be considered risk determinants but to approve their validity, they should be further evaluated in epidemiological studies.

Keywords

Acknowledgement

We would like to thank all individuals who helped us in the process of producing this paper.

References

  1. Blackwood L, German AJ, Stell AJ, O'Neill T. Multicentric lymphoma in a dog after cyclosporine therapy. J Small Anim Pract 2004; 45: 259-262.  https://doi.org/10.1111/j.1748-5827.2004.tb00233.x
  2. Boffetta P. I. Epidemiology of adult non-Hodgkin lymphoma. Ann Oncol 2011; 22: IV27-IV31.  https://doi.org/10.1093/annonc/mdr167
  3. Carlo GL, Cole P, Miller AB, Munro IC, Solomon KR, Squire RA. Review of a study reporting an association between 2,4-dichlorophenoxyacetic acid and canine malignant lymphoma: report of an expert panel. Regul Toxicol Pharmacol 1992; 16: 245-252.  https://doi.org/10.1016/0273-2300(92)90004-S
  4. Chiou SH, Chow KC, Yang CH, Chiang SF, Lin CH. Discovery of Epstein-Barr virus (EBV)-encoded RNA signal and EBV nuclear antigen leader protein DNA sequence in pet dogs. J Gen Virol 2005; 86(Pt 4): 899-905.  https://doi.org/10.1099/vir.0.80792-0
  5. Dobson JM, Samuel S, Milstein H, Rogers K, Wood JL. Canine neoplasia in the UK: estimates of incidence rates from a population of insured dogs. J Small Anim Pract 2002; 43: 240-246.  https://doi.org/10.1111/j.1748-5827.2002.tb00066.x
  6. Elvers I, Turner-Maier J, Swofford R, Koltookian M, Johnson J, Stewart C, et al. Exome sequencing of lymphomas from three dog breeds reveals somatic mutation patterns reflecting genetic background. Genome Res 2015; 25: 1634-1645.  https://doi.org/10.1101/gr.194449.115
  7. Engels EA. Infectious agents as causes of non-Hodgkin lymphoma. Cancer Epidemiol Biomarkers Prev 2007; 16: 401-404.  https://doi.org/10.1158/1055-9965.EPI-06-1056
  8. Ernst T, Kessler M, Lautscham E, Willimzig L, Neiger R. [Multicentric lymphoma in 411 dogs - an epidemiological study]. Tierarztl Prax Ausg K Kleintiere Heimtiere 2016; 44: 245-251. German.  https://doi.org/10.15654/TPK-150338
  9. Farmanfarma KK, Kiasara SH, Hassanipour S, Salehiniya H. Non-Hodgkin's lymphoma in the world: an epidemiological review. WCRJ 2020; 7: e1520. 
  10. Garabrant DH, Philbert MA. Review of 2,4-dichlorophenoxyacetic acid (2,4-D) epidemiology and toxicology. Crit Rev Toxicol 2002; 32: 233-257.  https://doi.org/10.1080/20024091064237
  11. Gavazza A, Presciuttini S, Barale R, Lubas G, Gugliucci B. Association between canine malignant lymphoma, living in industrial areas, and use of chemicals by dog owners. J Vet Intern Med 2001; 15: 190-195.  https://doi.org/10.1111/j.1939-1676.2001.tb02310.x
  12. Hart BL, Hart LA, Thigpen AP, Willits NH. Long-term health effects of neutering dogs: comparison of Labrador Retrievers with Golden Retrievers. PLoS One 2014; 9: e102241. 
  13. Hayes HM, Tarone RE, Cantor KP, Jessen CR, McCurnin DM, Richardson RC. Case-control study of canine malignant lymphoma: positive association with dog owner's use of 2,4-dichlorophenoxyacetic acid herbicides. J Natl Cancer Inst 1991; 83: 1226-1231.  https://doi.org/10.1093/jnci/83.17.1226
  14. Huang SH, Kozak PJ, Kim J, Habineza-Ndikuyeze G, Meade C, Gaurnier-Hausser A, et al. Evidence of an oncogenic gammaherpesvirus in domestic dogs. Virology 2012; 427: 107-117.  https://doi.org/10.1016/j.virol.2012.02.013
  15. Ito D, Frantz AM, Modiano JF. Canine lymphoma as a comparative model for human non-Hodgkin lymphoma: recent progress and applications. Vet Immunol Immunopathol 2014; 159: 192-201.  https://doi.org/10.1016/j.vetimm.2014.02.016
  16. Jemal A, Tiwari RC, Murray T, Ghafoor A, Samuels A, Ward E, et al. Cancer statistics, 2004. CA Cancer J Clin 2004; 54: 8-29.  https://doi.org/10.3322/canjclin.54.1.8
  17. Kaiser HE. Neoplasms--comparative pathology of growth in animals, plants, and man. Baltimore: Williams & Wilkins. 1981: 747-812. 
  18. Kaneene JB, Miller R. Re-analysis of 2,4-D use and the occurrence of canine malignant lymphoma. Vet Hum Toxicol 1999; 41: 164-170. 
  19. Keller ET. Immune-mediated disease as a risk factor for canine lymphoma. Cancer 1992; 70: 2334-2337.  https://doi.org/10.1002/1097-0142(19921101)70:9<2334::AID-CNCR2820700920>3.0.CO;2-7
  20. Mafra A, Laversanne M, Gospodarowicz M, Klinger P, De Paula Silva N, Pineros M, et al. Global patterns of non-Hodgkin lymphoma in 2020. Int J Cancer 2022; 151: 1474-1481.  https://doi.org/10.1002/ijc.34163
  21. Marconato L, Leo C, Girelli R, Salvi S, Abramo F, Bettini G, et al. Association between waste management and cancer in companion animals. J Vet Intern Med 2009; 23: 564-569.  https://doi.org/10.1111/j.1939-1676.2009.0278.x
  22. Mee MW, Faulkner S, Wood GA, Woods JP, Bienzle D, Coomber BL. RNA-Seq analysis of gene expression in 25 cases of canine lymphoma undergoing CHOP chemotherapy. BMC Res Notes 2022; 15: 111. 
  23. Moulton JE. Tumors in domestic animals. Berkeley: University of California Press. 1978. 
  24. Mudaliar MA, Haggart RD, Miele G, Sellar G, Tan KA, Goodlad JR, et al. Comparative gene expression profiling identifies common molecular signatures of NF-kB activation in canine and human diffuse large B cell lymphoma (DLBCL). PLoS One 2013; 8: e72591. 
  25. Pastor M, Chalvet-Monfray K, Marchal T, Keck G, Magnol JP, Fournel-Fleury C, et al. Genetic and environmental risk indicators in canine non-Hodgkin's lymphomas: breed associations and geographic distribution of 608 cases diagnosed throughout France over 1 year. J Vet Intern Med 2009; 23: 301-310.  https://doi.org/10.1111/j.1939-1676.2008.0255.x
  26. Pinello KC, Santos M, Leite-Martins L, Niza-Ribeiro J, de Matos AJ. Immunocytochemical study of canine lymphomas and its correlation with exposure to tobacco smoke. Vet World 2017; 10: 1307-1313.  https://doi.org/10.14202/vetworld.2017.1307-1313
  27. Reif JS, Lower KS, Ogilvie GK. Residential exposure to magnetic fields and risk of canine lymphoma. Am J Epidemiol 1995; 141: 352-359.  https://doi.org/10.1093/aje/141.4.352
  28. Reynolds PM, Reif JS, Ramsdell HS, Tessari JD. Canine exposure to herbicide-treated lawns and urinary excretion of 2,4-dichlorophenoxyacetic acid. Cancer Epidemiol Biomarkers Prev 1994; 3: 233-237. 
  29. Ruple A, Avery AC, Morley PS. Differences in the geographic distribution of lymphoma subtypes in Golden retrievers in the USA. Vet Comp Oncol 2017; 15: 1590-1597.  https://doi.org/10.1111/vco.12258
  30. Safran N, Perk K, Eyal O, Dahlberg JE. Isolation and preliminary characterisation of a novel retrovirus isolated from a leukaemic dog. Res Vet Sci 1992; 52: 250-255.  https://doi.org/10.1016/0034-5288(92)90018-W
  31. Seelig DM, Avery AC, Ehrhart EJ, Linden MA. The comparative diagnostic features of canine and human lymphoma. Vet Sci 2016; 3: 11. 
  32. Takashima-Uebelhoer BB, Barber LG, Zagarins SE, Procter-Gray E, Gollenberg AL, Moore AS, et al. Household chemical exposures and the risk of canine malignant lymphoma, a model for human non-Hodgkin's lymphoma. Environ Res 2012; 112: 171-176.  https://doi.org/10.1016/j.envres.2011.12.003
  33. Thomas R, Demeter Z, Kennedy KA, Borst L, Singh K, Valli VE, et al. Integrated immunohistochemical and DNA copy number profiling analysis provides insight into the molecular pathogenesis of canine follicular lymphoma. Vet Comp Oncol 2017; 15: 852-867.  https://doi.org/10.1111/vco.12227
  34. Thomas R, Smith KC, Ostrander EA, Galibert F, Breen M. Chromosome aberrations in canine multicentric lymphomas detected with comparative genomic hybridisation and a panel of single locus probes. Br J Cancer 2003; 89: 1530-1537.  https://doi.org/10.1038/sj.bjc.6601275
  35. Tomley FM, Armstrong SJ, Mahy BW, Owen LN. Reverse transcriptase activity and particles of retroviral density in cultured canine lymphosarcoma supernatants. Br J Cancer 1983; 47: 277-284.  https://doi.org/10.1038/bjc.1983.36
  36. Torres de la Riva G, Hart BL, Farver TB, Oberbauer AM, Messam LL, Willits N, et al. Neutering dogs: effects on joint disorders and cancers in golden retrievers. PLoS One 2013; 8: e55937. 
  37. Vail DM, Thamm DH, Liptak JM. Withrow and MacEwen's small animal clinical oncology- e-book. Philadelphia: Elsevier Health Sciences. 2019. 
  38. Villamil JA, Henry CJ, Hahn AW, Bryan JN, Tyler JW, Caldwell CW. Hormonal and sex impact on the epidemiology of canine lymphoma. J Cancer Epidemiol 2009; 2009: 591753. 
  39. Zallio F, Limberti G, Ladetto M. Infections and Follicular Lymphoma: is there a Link? Mediterr J Hematol Infect Dis 2017; 9: e2017035. 
  40. Zandvliet M. Canine lymphoma: a review. Vet Q 2016; 36: 76-104.  https://doi.org/10.1080/01652176.2016.1152633
  41. Zink MC, Farhoody P, Elser SE, Ruffini LD, Gibbons TA, Rieger RH. Evaluation of the risk and age of onset of cancer and behavioral disorders in gonadectomized Vizslas. J Am Vet Med Assoc 2014; 244: 309-319.  https://doi.org/10.2460/javma.244.3.309
  42. Zintzaras E, Voulgarelis M, Moutsopoulos HM. The risk of lymphoma development in autoimmune diseases: a meta-analysis. Arch Intern Med 2005; 165: 2337-2344. https://doi.org/10.1001/archinte.165.20.2337