Skip to main content
Log in

Change in Urine Odor of Mice in the Dynamics of Formation of a Transplanted Hepatocarcinoma H33 Tumor

  • ANIMAL AND HUMAN PHYSIOLOGY
  • Published:
Biology Bulletin Aims and scope Submit manuscript

Abstract—

The effect of the stage of development of a malignant tumor on successful detection in the urine of animals with oncology by dogs was studied. It was demonstrated that the success of dogs in the search for sick organisms among healthy ones is quite consistent with the dynamics of the development of transplanted tumor tissue; that is, dogs are able to perceive both the entire spectrum of volatile metabolites accompanying the disease and changes in this spectrum associated directly with the development of the tumor. The existence of volatile organic compounds associated with the growth of a malignant tumor was established.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

REFERENCES

  1. Amal, H., Ding, L., Liu, B.B., Tisch, U., Xu, Z.Q., Shi, D.Y., Zhao, Y., Chen, J., Sun, R.X., Liu, H., Ye, S.L., Tang, Z.Y., and Haick, H., The scent fingerprint of hepatocarcinoma: in-vitro metastasis prediction with volatile organic compounds (VOCs), Int. J. Nanomed., 2012, vol. 7, pp. 4135–4146.

    CAS  Google Scholar 

  2. Amann, A., Breath analysis for clinical diagnosis and therapeutic monitoring, Siriraj Med. J., 2012, vol. 6, suppl. 2, pp. 18–19.

    Google Scholar 

  3. American Lung Association. Lung cancer fact sheet. American Lung Association, 2015. http://www. lung. org/lung-health-and-diseases/lung-disease-lookup/lung-cancer/resource-library/lung-cancer-fact-sheet.html. Accessed March 22, 2020.

  4. Arakawa, H., Arakawa, K., and Deak, T., Sickness-related odor communication signals as determinants of social behavior in rat: a role for inflammatory processes, Horm. Behav., 2010, vol. 57, no. 3, pp. 330–341.

    CAS  PubMed  Google Scholar 

  5. Arakawa, H., Cruz, S., and Deak, T., From models to mechanisms: odorant communication as a key determinant of social behavior in rodents during illness-associated states, Neurosci. Biobehav. Rev., 2011, vol. 35, no. 9, pp. 1916–1928.

    PubMed  Google Scholar 

  6. Beauchamp, G.K. and Yamazaki, K., Individual differences and the chemical senses, Chem. Senses, 2005, vol. 30, suppl. 1, pp. i6–i9.

    PubMed  Google Scholar 

  7. Beauchamp, G.K., Yamazaki, K., Wysocki, C.J., Slotnick, B.M., Thomas, L., and Boyse, E.A., Chemosensory recognition of mouse major histocompatibility types by another species, Proc. Natl. Acad. Sci. U. S. A., 1985, vol. 82, pp. 4186–4188.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Bekoff, M., Observations of scent-marking and discriminating self from others by a domestic dog (Canis familiaris): tales of displaced yellow snow, Behav. Process, 2001, vol. 55, no. 2, pp. 75–79.

    CAS  Google Scholar 

  9. Bijland, L.R., Bomers, M.K., and Smulders, Y.M., Smelling the diagnosis. A review on the use of scent in diagnosing, Neth. J. Med., 2013, vol. 71, pp. 300–307.

    CAS  PubMed  Google Scholar 

  10. Boots, A.W., van Berkel, J.J.B.N., Dallinga, J.W., Smolinska, A., Wouters, M.F.M., and van Schooten, F.J., The versatile use of exhaled volatile organic compounds in health and disease, J. Breath Res., 2012, vol. 6, p. 027108.

    PubMed  Google Scholar 

  11. Brennan, P.A. and Kendrick, K.M., Mammalian social odours: attraction and individual recognition, Philos. Trans. R. Soc. Lond., B: Biol. Sci., 2006, vol. 361, pp. 2061–2078.

    CAS  Google Scholar 

  12. Chambers, S.T., Scott-Thomas, A., and Epton, M., Developments in novel breath tests for bacterial and fungal pulmonary infection, Curr. Opin. Pulm. Med., 2012, vol. 18, pp. 228–232.

    PubMed  Google Scholar 

  13. Cicolella, A., Volatile organic compounds (VOC): definition, classification and properties, Rev. Mal. Respir., 2008, vol. 25, pp. 155–163.

    CAS  PubMed  Google Scholar 

  14. Cornu, J.N., Cancal-Tassin, G., Ondet, V., Girardet, C., and Cussenot, O., Olfactory detection of prostate cancer by dogs sniffing urine: a step forward to early diagnosis, Eur. Urol., 2011, vol. 59, pp. 197–201.

    PubMed  Google Scholar 

  15. Dummer, J., Storer, SwanneyM., McEwan, M., Scott-Thomsad, A., Bhandari, S., Chambers, S., Dweik, R., and Epton, M., Analysis of biogenic volatile organic compounds in health and disease, TrAC, Trends Anal. Chem. (Pers. Ed.), 2011, vol. 30, pp. 960–967.

  16. Ehman, K.D. and Scott, M.E., Female mice mate preferentially with non-parasitized males, Parasitology, 2002, vol. 125, no. 5, pp. 461–466.

    CAS  PubMed  Google Scholar 

  17. Ehmann, R., Boedeker, E., Friedrich, U., Sagert, J., Dippon, J., Friedel, G., and Walles, T., Canine scent detection in the diagnosis of lung cancer: revisiting a puzzling phenomenon, Eur. Resp. J., 2011, vol. 39, pp. 669–676.

    Google Scholar 

  18. El-Serag, H.B., Marrero, J.A., Rudolph, L., and Reddy, K.R., Diagnosis and treatment of hepatocellular carcinoma, Gastroenterology, 2008, vol. 134, pp. 1752–1763.

    PubMed  Google Scholar 

  19. Filipiak, W., Sponring, A., Mikoviny, T., Ager, C., Schubert, J., Miekisch, W., Amann, A., and Troppmair, J., Release of volatile organic compounds (VOCs) from the lung cancer cell line CALU-1 in vitro, Cancer Cell Int., 2008, vol. 8, no. 1, pp. 17–28.

    PubMed  PubMed Central  Google Scholar 

  20. Fouad, Y.A. and Aanei, C., Revisiting the hallmarks of cancer, Am. J. Cancer Res., 2017, vol. 7, no. 5, pp. 1016–1036.

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Garner, C.E., Smith, S., Costello, B., White, P., Spencer, R., Prober, C.S.J., and Ratcliffe, M., Volatile organic compounds from feces and their potential for diagnosis of gastrointestinal disease, FASEB J., 2007, vol. 21, no. 8, pp. 1675–1688.

    CAS  PubMed  Google Scholar 

  22. Garner, C.E., Smith, S., Bardhan, P.K., Ratcliffe, N.M., and Probert, C.S., A pilot study of faecal volatile organic compounds in faeces from cholera patients in Bangladesh to determine their utility in disease diagnosis, Trans. R. Soc. Trop. Med. Hyg., 2009, vol. 103, no. 11, pp. 1171–1173.

    CAS  PubMed  Google Scholar 

  23. Guernion, N., Ratcliffe, M., Spencer-Phillips, P.T., and Howe, R.A., Identifying bacteria in human urine: current practice and the potential for rapid, near-patient diagnosis by sensing volatile organic compounds, Clin. Chem. Lab. Med., 2001, vol. 39, pp. 893–906.

    CAS  PubMed  Google Scholar 

  24. Hakim, M., Broza, Y.Y., Barash, O., Peled, N., Phillips, M., Amann, A., and Haick, H., Volatile organic compounds of lung cancer and possible biochemical pathways, Chem. Rev., 2012, vol. 112, pp. 5949–5966.

    CAS  PubMed  Google Scholar 

  25. Hanahan, D. and Weinberg, R.A., Hallmarks of cancer: the next generation, Cell, 2011, vol. 144, no. 5, pp. 646–674.

    CAS  PubMed  Google Scholar 

  26. Harrington, F.H., Asa, C.S., Mech, L., and Boitani, L., Wolf communication, in Wolves: Behavior, Ecology, and Conservation, Chicago: Univ. Chicago Press, 2003, vol. 3, pp. 66–103.

    Google Scholar 

  27. Hartke, J., Johnson, M., and Ghabril, M., The diagnosis and treatment of hepatocellular carcinoma, Semin. Diagn. Pathol., 2017, vol. 34, pp. 153–159.

    PubMed  Google Scholar 

  28. Horvath, I., Lazar, Z., Gyulai, N., Kollai, M., and Losonczy, G., Exhaled biomarkers in lung cancer, Eur. Respir. J., 2009, vol. 34, pp. 261–275.

    CAS  PubMed  Google Scholar 

  29. Jett, J.R., Limitations of screening for lung cancer with low-dose spiral computed tomography, Clin. Cancer Res., 2005, vol. 11, no. 13, pp. 4988s–4992s.

    PubMed  Google Scholar 

  30. Johnston, R.E., Chemical communication in rodents: from pheromones to individual recognition, J. Mammal., 2003, vol. 84, pp. 1141–1162.

    Google Scholar 

  31. Kang, J., Zhu, L., Lu, J., and Zhang, X., Application of metabolomics in autoimmune diseases: insight into biomarkers and pathology, J. Neuroimmunol., 2015, vol. 279, pp. 25–32.

    CAS  PubMed  Google Scholar 

  32. Kavaliers, M., Choleris, E., and Pfaff, D.W., Recognition and avoidance of the odors of parasitized conspecifics and predators: differential genomic correlates, Neurosci. Biobehav. Rev., 2005a, vol. 29, pp. 1347–1359.

    PubMed  Google Scholar 

  33. Kavaliers, M., Choleris, E., Agmo, A., Muglia, L.J., Ogawa, S., and Pfaff, D.W., Involvement of the oxytocin gene in the recognition and avoidance of parasitized males by female mice, Anim. Behav., 2005b, vol. 70, pp. 693–702.

    Google Scholar 

  34. Keller, M., Douhard, Q., Baum, M.J., and Bakker, J., Destruction of the main olfactory epithelium reduces female sexual behavior and olfactory investigation in female mice, Chem. Senses, 2006a, vol. 31, pp. 315–323.

    PubMed  Google Scholar 

  35. Keller, M., Pierman, S., Douhard, Q., Baum, M.J., and Bakker, J., The vomeronasal organ is required for the expression of lordosis behaviour, but not sex discrimination in female mice, Eur. J. Neurosci., 2006b, vol. 23, pp. 521–530.

    PubMed  PubMed Central  Google Scholar 

  36. Kelliher, K.R., The combined role of the main olfactory and vomeronasal systems in social communication in mammals, Horm. Behav., 2007, vol. 52, pp. 561–570.

    PubMed  PubMed Central  Google Scholar 

  37. Kimball, B.A., Volatile metabolome: problems and prospects, Bioanalysis, 2016a, vol. 8, no. 19, pp. 1987–1991.

    CAS  PubMed  Google Scholar 

  38. Kimball, B.A., Yamazaki, K., Kohler, D., Bowen, R.A., Muth, J.P., Opiekun, M., and Beauchamp, G.K., Avian influenza infection alters fecal odor in mallards, PLoS One, 2013, vol. 8, no. 10. e75411.

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Kimball, B.A., Opiekun, M., Yamazaki, K., and Beauchamp, G.K., Immunization alters body odor, Physiol. Behav., 2014, vol. 128, pp. 80–85.

    CAS  PubMed  Google Scholar 

  40. Kimball, B.A., Wilson, D.A., and Wesson, D.W., Alterations of the volatile metabolome in mouse models of Alzheimer’s disease, Sci. Rep., 2016b, vol. 14, no. 6, p. 19495.

    Google Scholar 

  41. Kimball, B.A., Cohen, A.S., Gordon, A.R., Opiekun, M., Martin, T., Elkind, J., Lundstrom, J.N., and Beauchamp, G.K., Brain injury alters volatile metabolome, Chem. Senses, 2016c, vol. 41, no. 5, pp. 407–414.

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Kochevalina, M.Yu. and Trunov, V.G., Principles of organizing a database for behavioral experiments with macrosmatic animals, Usp. Sovrem. Nauki, 2016, vol. 3, no. 4, pp. 130–133.

    Google Scholar 

  43. Kochevalina, M.Yu., Rodionova, E.I., Morozova, O.V., Ambaryan, A.V., and Borodkov, A.S., The study of the odorological profile of the urine of mice with hepatocarcinoma, Tr. Conf. IT, 2014, pp. 570–574. http://itas2014.iitp.ru/pdf/1569927987.pdf.

    Google Scholar 

  44. Krutova, V.I., Sulimov, K.T., and Zinkevich, E.P., The time of appearance of an individual odor in the ontogenesis of gray rats (Rattus norvegicus) according to cynological analysis, Sensorn.Sist., 1997, vol. 11, no. 3, pp. 340–345.

    Google Scholar 

  45. Lazarevich, N.L., Cheremnova, O.A., Varga, E.V., Ovchinnikov, D.A., Kudrjavtseva, E.I., Morozova, O.V., Fleishman, D.I., Engelhardt, N.V., and Duncan, S.A., Progression of HCC in mice is associated with a downregulation in the expression of hepatocyte nuclear factors, Hepatology, 2004, vol. 39, pp. 1038–1047.

    CAS  PubMed  Google Scholar 

  46. Liddell, K., Smell as a diagnostic marker, Postgrad. Med. J., 1976, vol. 52, no. 605, pp. 136–138.

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Lubes, G. and Goodarzi, M., GC-MS based metabolomics used for the identification of cancer volatile organic compounds biomarkers, J. Pharm. Biomed. Anal., 2017, vol. 147, pp. 313–322.

    PubMed  Google Scholar 

  48. Ludwig, J.A. and Weinstein, J.N., Biomarkers in cancer staging, prognosis and treatment selection, Nat. Rev. Cancer, 2005, vol. 5, no. 11, pp. 845–856.

    CAS  PubMed  Google Scholar 

  49. Masuda, T. and Miyoshi, E., Cancer biomarkers for hepatocellular carcinomas: from traditional markers to recent topics, Clin. Chem. Lab. Med., 2011, vol. 49, no. 6, pp. 959–966.

    CAS  PubMed  Google Scholar 

  50. Matsumura, K., Opiekun, M., Oka, H., Vachani, A., Albelda, S.M., Yamazaki, K., and Beauchamp, G.K., Urinary volatile compounds as biomarkers for lung cancer: a proof of principle study using odor signatures in mouse models of lung cancer, PLoS One, 2010, vol. 5, no. 1. e8819.

    PubMed  PubMed Central  Google Scholar 

  51. Mazzone, P.J., Analysis of volatile organic compounds in the exhaled breath for the diagnosis of lung cancer, J. Thorac. Oncol., 2008, vol. 3, pp. 774–780.

    PubMed  Google Scholar 

  52. Miekisch, W., Schubert, J.K., Gabriele, F.E., and Noelge-Schomburg, G.F.E., Diagnostic potential of breath analysis—focus on volatile organic compounds, Clin. Chim. Acta, 2004, vol. 347, pp. 25–39.

    CAS  PubMed  Google Scholar 

  53. Minino, A.M. and Kochanek, K.D., Deaths: preliminary data for 2008, Natl. Vital Stat. Rep., 2010, vol. 59, pp. 1–72.

    PubMed  Google Scholar 

  54. Moser, E. and McCulloch, M., Canine scent detection of human cancers: a review of methods and accuracy, J. Vet. Behav. Clin. Appl. Res., 2010, vol. 5, pp. 145–152.

    Google Scholar 

  55. Novak, B.J., Blake, D.R., Meinardi, S., Rowland, F.S., Pontello, A., Cooper, D.M., and Galassetti, P.R., Exhaled methyl nitrate as a noninvasive marker of hyperglycemia in type 1 diabetes, Proc. Natl. Acad. Sci. U. S. A., 2007, vol. 104, pp. 15613–15618.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Novotny, M., Harvey, S., Jemiolo, B., and Alberts, J., Synthetic pheromones that promote inter-male aggression in mice. Proc. Natl. Acad. Sci. U. S. A., 1985, vol. 82, pp. 2059–2061.

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Osada, K., Yamazaki, K., Curran, M., Bard, J., Smith, B.P., and Beauchamp, G.K., The scent of age, Proc. R. Soc. Lond. B. Biol. Sci., 2003, vol. 270, no. 1518, pp. 929–933.

    CAS  Google Scholar 

  58. Osada, K., Tashiro, T., Mori, K., and Izumi, H., The identification of attractive volatiles in aged male mouse urine, Chem. Senses, 2008, vol. 33, no. 9, pp. 815–823.

    CAS  PubMed  Google Scholar 

  59. Parkin, D.M., Bray, F., Ferlay, J., and Pisani, P., Estimating the world cancer burden: globocan 2000, Int. J. Cancer, 2001, vol. 94, no. 2, pp. 153–156.

    CAS  PubMed  Google Scholar 

  60. Pavlou, A.K. and Turner, A.P., Sniffing out the truth: clinical diagnosis using the electronic nose, Clin. Chem. Lab. Med., 2000, vol. 38, pp. 99–112.

    CAS  PubMed  Google Scholar 

  61. Peng, G., Hakim, M., Broza, Y.Y., Billan, S., Abdah-Bortnyak, R., Kuten, A., Tisch, U., and Haick, H., Detection of lung, breast, colorectal, and prostate cancers from exhaled breath using a single array of nanosensors, Br. J. Cancer, 2010, vol. 103, pp. 542–551.

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Penn, D. and Potts, W.K., Chemical signals and parasite-mediated sexual selection, Trends Ecol. Evol., 1998, vol. 13, pp. 391–396.

    CAS  PubMed  Google Scholar 

  63. Phillips, M., Cataneo, R.N., Cheema, T., and Greenberg, J., Increased breath biomarkers of oxidative stress in diabetes mellitus, Clin. Chim. Acta, 2004, vol. 344, pp. 189–194.

    CAS  PubMed  Google Scholar 

  64. Phillips, M., Cataneo, R.N., Condos, R. Ring, EriksonG.A., and Greenberg, J., La Bombardi, V., Munawar, M.I., and Tietje, O., Volatile biomarkers of pulmonary tuberculosis in the breath, Tuberculosis, 2007, vol. 87, pp. 44–52.

    CAS  PubMed  Google Scholar 

  65. Probert, C.S., Ahmed, I., Khalid, T., Johnson, E., Smith, S., and Ratcliffe, N., Volatile organic compounds as diagnostic biomarkers in gastrointestinal and liver diseases, J. Gastrointestin. Liver Dis., 2009, vol. 18, no. 3, pp. 337–343.

    PubMed  Google Scholar 

  66. Qin, T., Liu, H., Song, Q., Song, G., Wang, H.Z., Pan, Y.Y., Xiong, F.X., Gu, K.S., Sun, G.P., and Chen, Z.D., The screening of volatile markers for hepatocellular carcinoma, Cancer Epidemiol. Biomark. Prev., 2010, vol. 19, no. 9, pp. 2247–2253.

    CAS  Google Scholar 

  67. Rodionova, E.I., Kochevalina M.Yu., Kotenkova E.V., Morozova O.V., Kogun’ G.A., Bataeva, E.L., and Ambaryan, A.V., Detection of volatile organic compounds associated with hepatocellular carcinoma by macrosmatic animals: approaches to the search for new tumor markers, Biol. Bull. (Moscow), 2015, vol. 42, no. 3, pp. 239–245.

    CAS  Google Scholar 

  68. Rozhok, A.I. and DeGregori, J., The evolution of lifespan and age-dependent cancer risk, Trends Cancer, 2016, vol. 2, no. 10, pp. 552–560.

    PubMed  PubMed Central  Google Scholar 

  69. Sato, T., Katsuoka, Y., Yoneda, K., Nonomura, M., Uchimoto, S., Kobayakawa, R., Kobayakawa, K., and Mizutani, Y., Sniffer mice discriminate urine odours of patients with bladder cancer: a proof-of-principle study for non-invasive diagnosis of cancer-induced odour, Sci. Rep., 2017, vol. 7, no. 1, p. 14628.

    PubMed  PubMed Central  Google Scholar 

  70. Schaal, B., Coureaud, G., Langlois, D., Ginies, C., Semon, E., and Perrier, G., Chemical and behavioural characterization of the rabbit mammary pheromone, Nature, 2003, vol. 424, pp. 68–72.

    CAS  PubMed  Google Scholar 

  71. Schaefer, M.L., Yamazaki, K., Osada, K., Restrepo, D., and Beauchamp, G.K., Olfactory fingerprints for major histocompatibility complex-determined body odors ii: relationship among odor maps, genetics, odor composition, and behavior, J. Neurosci., 2002, vol. 22, pp. 9513–9521.

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Schellinck, H.M., West, A.M., and Brown, R.E., Rats can discriminate between the urine odors of genetically identical mice maintained on different diets, Physiol. Behav., 1992, vol. 51, no. 5, pp. 1079–1082.

    CAS  PubMed  Google Scholar 

  73. Schmidt, K. and Podmore, I., Current challenges in volatile organic compounds analysis as potential biomarkers of cancer, J. Biomark., 2015, vol. 2015, art. ID 981458.

    PubMed  PubMed Central  Google Scholar 

  74. Schoon, G.A.A., Scent identification lineups by dogs (Canis familiaris): experimental design and forensic application, Appl. Anim. Behav. Sci., 1996, vol. 49, pp. 257–267.

    Google Scholar 

  75. Shirasu, M. and Touhara, K., The scent of disease: volatile organic compounds of the human body related to disease and disorders, J. Biochem., 2011, vol. 150, pp. 257–266.

    CAS  PubMed  Google Scholar 

  76. Strauch, M., Lüdke, A., Münch, D., Laudes, T., Galizia, C.G., Martinelli, E., Lavra, L., Paolesse, R., Ulivieri, A., Catini, A., and Capuano, R., More than apples and oranges—detecting cancer with a fruit fly’s antenna, Sci. Rep., 2014, vol. 4, p. 3576.

    PubMed  PubMed Central  Google Scholar 

  77. Syhre, M., Manning, L., Phuanukoonnon, S., Harino, P., and Chambers, S.T., The scent of mycobacterium tuberculosis—part II breath, Tuberculosis, 2009, vol. 89, no. 4, pp. 263–266.

    CAS  PubMed  Google Scholar 

  78. Trinchet, J.C., Alperovitch, A., Bedossa, P., Degos, F., Hainaut, P., and Beers, B.V., Epidemiology, prevention, screening and diagnosis of hepatocellular carcinoma, Bull. Cancer, 2009, vol. 96, pp. 35–43.

    PubMed  Google Scholar 

  79. Wells, M.C. and Bekoff, M., An observational study of scent-marking in coyotes, Canis latrans,Anim. Behav., 1981, vol. 29, no. 2, pp. 332–350.

    Google Scholar 

  80. Willis, C. and Poulin, R., Preference of female rats for the odours of non-parasitised males: the smell of good genes?, Folia Parasitol., 2000, vol. 47, no. 1, pp. 6–10.

    CAS  Google Scholar 

  81. Yamazaki, K., Beauchamp, G.K., Singer, A., Bard, J., and Boyse, E.A., Odor types: their origin and composition, Proc. Natl. Acad. Sci. U. S. A., 1999, vol. 96, pp. 1522–1525.

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Yamazaki, K., Boyse, E.A., Bard, J., Curran, M., Kim, D., Ross, S.R., and Beauchamp, G.K., Presence of mouse mammary tumor virus specifically alters the body odor of mice, Proc. Natl. Acad. Sci. U. S. A., 2002, vol. 99, no. 8, pp. 5612–5615.

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Zlotta, A.R. and Nam, R.K., To biopsy or not to biopsy— thou shall think twice, Eur. Urol., 2012, vol. 61, no. 6, pp. 1115–1117.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. I. Rodionova.

Ethics declarations

Conflict of interests. The authors declare that they have no conflict of interest.

Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Translated by A. Barkhash

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kochevalina, M.Y., Trunov, V.G., Morozova, O.V. et al. Change in Urine Odor of Mice in the Dynamics of Formation of a Transplanted Hepatocarcinoma H33 Tumor. Biol Bull Russ Acad Sci 47, 506–513 (2020). https://doi.org/10.1134/S1062359020050052

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062359020050052

Navigation