Detection of volatile organic compounds associated with hepatocellular carcinoma by macrosmatic animals: Approaches to the search for new tumor markers

Abstract

Macrosmatic animals (dogs and mice) have been proved to be able to distinguish between the urine or feces of mice with transplanted hepatocellular carcinoma and those of healthy mice by odor. The chemical composition of animal excreta was found to change with tumor growth; however, it is not clear yet if this results from tumor growth itself, inflammation, or immune response. We suggested that the use of the ability of macrosmatic animals to compare odor mixtures combined with mouse cancer models is a promising trend in the search for new tumor markers.

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References

  1. Ackerl, K., Atzmüller, A., and Grammer, K., The scent of fear, Neuroendocrinol. Lett., 2001, vol. 23, pp. 79–84.

    Google Scholar 

  2. Amal, H., Ding, L., Liu, B.B., et al., 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 

  3. Anisimov, V.N., Ukraintseva, S.V., and Yashin, A.I., Cancer in rodents: does it tell us about jarcer in humans?, Nat. Rev. Cancer, 2005, vol. 5, pp. 807–819.

    Article  CAS  PubMed  Google Scholar 

  4. 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, pp. 1916–1928.

    Article  PubMed  Google Scholar 

  5. Boedeker, E., Friedel, G., and Walles, T., Sniffer dogs as part of a bimodal bionic research approach to develop a lung cancer screening, Interact. Cardiovasc. Thorac. Surg., 2012, vol. 14, pp. 511–515.

    Article  PubMed Central  PubMed  Google Scholar 

  6. Bransbury, A.J., Church, M.R.T., and Church, J.C.T., Olfactory detection of human bladder cancer by dogs: proof of principle study, BMJ, 2004, vol. 329, pp. 712–717.

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  8. Gordon, R.T., Schatz, C.B., Myers, L.J., et al., The use of canines in the detection of human cancers, J. Altern. Compl. Med., 2008, vol. 14, pp. 61–67.

    Article  Google Scholar 

  9. Hakim, G.M., Broza, Y.Y., Billan, S., et al., 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.

    Article  PubMed Central  PubMed  Google Scholar 

  10. Hanai, Y., Shimono, K., Matsumura, K., et al., Urinary volatile compounds as biomarkers for lung cancer, Biosci. Biotechnol. Biochem., 2012a, vol. 76, pp. 679–684.

    Article  CAS  PubMed  Google Scholar 

  11. Hanai, Y., Shimono, K., Oka, H., et al., Analysis of volatile organic compounds released from human lung cancer cells and from the urine of tumor-bearing mice, Cancer Cell Int., 2012b, vol. 12, pp. 7–19.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Havlicek, J.1. and Roberts, S.C., MHC-correlated mate choice in humans: a review, Psychoneuroendocrinology, 2009, vol. 34, no. 4, pp. 497–512.

    Article  CAS  PubMed  Google Scholar 

  13. Heth, G. and Todrank, J., Individual odour similarities across species parallel phylogenetic relationships in the S. ehrenbergi superspecies of mole-rats, Anim. Behav., 2000, vol. 60, pp. 789–795.

    Article  PubMed  Google Scholar 

  14. Horvath, G., Järverud, G., Järverud, S., and Horváth, I., Human ovarian carcinomas detected by specific odor, Integrative Cancer Therapies, 2008, vol. 7, pp. 76–80.

    Article  PubMed  Google Scholar 

  15. Horváth, I., Lázár, Z., Gyulai, N., et al., Exhaled biomarkers in lung cancer, Eur. Respir. J., 2009, vol. 34, pp. 261–275.

    Article  PubMed  Google Scholar 

  16. Horvath, G., Andersson, H., and Paulsson, G., Characteristic odour in the blood reveals ovarian carcinoma, BMC Cancer, 2010, vol. 10, p. 643.

    Article  PubMed Central  PubMed  Google Scholar 

  17. Hussain, S.A., Ferry, D.R., El-Gazzaz, G., et al., Hepatocellular carcinoma, Ann. Oncol., 2001, vol. 12, pp. 161–172.

    Article  CAS  PubMed  Google Scholar 

  18. Jemal, A., Bray, F., Center, M.M., et al., Global cancer statistics, CA Cancer J. Clin., 2011, vol. 61, pp. 69–90.

    Article  PubMed  Google Scholar 

  19. Koczulla, R., Hattesohl, A., Biller, H., et al., Comparison of four identical electronic noses and three measurement set-ups, Pneumologie, 2011, vol. 65, pp. 465–470.

    Article  CAS  PubMed  Google Scholar 

  20. Korenevskii, Yu., Examination of olfactory traces in investigative and judicial practice, Ros. Yustitsiya, 2000, no. 8, p. 29.

    Google Scholar 

  21. Krutova, V.I., Sulimov, K.T., and Zinkevich, E.P., The time of appearance of individual odor in the ontogeny of the gray rat (Rattus norvegicus) according to dog training analysis, Sensorn. Sistemy, 1997, vol. 11, no. 3, pp. 340–345.

    Google Scholar 

  22. Kuano, M., Mendez, E., and Furton, K.G., Development of headspace SPME method or analysis of volatile organic compounds present in human biological specimens, Anal. Bioanal. Chem., 2011, vol. 400, pp. 1817–1826.

    Article  Google Scholar 

  23. Kwak, J., Gallagher, M., Ozdener, M.H., et al., Volatile biomarkers from human melanoma cells, J. Chromatogr. B. Analyt. Technol. Biomed. Life Sci., 2013, vol. 931, pp. 90–96.

    Article  CAS  PubMed  Google Scholar 

  24. Lazarevich, N.L., Cheremnova, O.A., Varga, E.V., et al., Progression of HCC in mice is associated with a down-regulation in the expression of hepatocyte nuclear factors, Hepatology, 2004, vol. 39, pp. 1038–1047.

    Article  CAS  PubMed  Google Scholar 

  25. Matsumura, K., Opiekun, M., Oka, H., et al., 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, p. e8819.

    Article  PubMed Central  PubMed  Google Scholar 

  26. McCulloch, M., Jezierski, T., Broffman, M., et al., Diagnostic accuracy of canine scent detection in early- and latestage lung and breast cancers, Interact. Cancer. Ther., 2006, vol. 5, pp. 30–39.

    Article  Google Scholar 

  27. O’Neill, H.J., Gordon, S.M., O’Neill, M.H., et al., A computerized classification technique for screening for the presence of breath biomarkers in lung cancer, Clin. Chem., 1988, vol. 34, no. 8, pp. 1613–1618.

    PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  29. Persaud, K. and Dodd, G., Analysis of discrimination mechanisms in the mammalian olfactory system using a model nose, Nature, 1982, vol. 299, pp. 352–355.

    Article  CAS  PubMed  Google Scholar 

  30. Qin, T., Liu, H., Song, Q., et al., The screening of volatile markers for hepatocellular carcinoma, Cancer Epidemiol. Biomark. Prev., 2010, vol. 19, pp. 2247–2253.

    Article  CAS  Google Scholar 

  31. Rivière, S., Challet, L., Fluegge, D., et al., Formyl peptide receptor-like proteins are a novel family of vomeronasal chemosensors, Nature, 2009, vol. 459, pp. 574–577.

    Article  PubMed  Google Scholar 

  32. Rodionova, E.I., Minor, A.V., Sulimov, K.T., and Kogun, G.A., Dogs are able to recognize insect individuals by odour, Chem. Senses, 2009, vol. 34, no. 3, p. E64.

    Google Scholar 

  33. 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.

    Article  Google Scholar 

  34. Schoon, A. and Haak, R., K9 Suspect Discrimination: Training and Practicing Scent Identification Line-Ups, Calgary, Alberta, Canada: Detselig Enterprises, 2002.

    Google Scholar 

  35. Sokolov, V.E., Sulimov, K.T., and Krutova, V.I., Dog identification of individual odors in live activity traces of four species of vertebrates, Izv. Akad. Nauk SSSR, Ser. Biol., 1990, no. 4, pp. 56–64.

    Google Scholar 

  36. Sonoda, H., Kohnoe, S., Yamazato, T., et al., Colorectal cancer screening with odour material by canine scent detection, Gut, 2011, vol. 60, pp. 814–819.

    Article  PubMed Central  PubMed  Google Scholar 

  37. Tisch, U. and Haick, H., Nanomaterials for cross-reactive sensor arrays, MRS Bull., 2010, vol. 35, p. 797.

    Article  CAS  Google Scholar 

  38. Walczak, M., Jezierskie, T., Górecka-Bruzda, A., et al., Impact of individual training parameters and manner of taking breath odor samples on the reliability of canines as cancer screeners, J. Vet. Behav., 2012, vol. 7, pp. 283–294.

    Article  Google Scholar 

  39. Williams, M. and Johnston, J.M., Training and maintaining the performance of dogs (Canis familiaris) on an increasing number of odor discriminations in a controlled setting, Appl. Anim. Behav. Sci., 2002, vol. 78, pp. 55–65.

    Article  Google Scholar 

  40. Xue, R., Dong, L., Zhang, S., et al., Investigation of volatile biomarkers in liver cancer blood using solid-phase microextraction and gas chromatography/mass spectrometry, Rapid Commun. Mass Spectrom., 2008, vol. 22, pp. 1181–1186.

    Article  CAS  PubMed  Google Scholar 

  41. Yamazaki, K. and Beauchamp, G.K., Genetic basis for MHC-dependent mate choice, Adv. Genet., 2007, vol. 59, pp. 129–145.

    PubMed  Google Scholar 

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Correspondence to E. I. Rodionova.

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Original Russian Text © E.I. Rodionova, M.Yu. Kochevalina, E.V. Kotenkova, O.V. Morozova, G.A. Kogun’, E.L. Bataeva, A.V. Ambaryan, 2015, published in Izvestiya Akademii Nauk, Seriya Biologicheskaya, 2015, No. 3, pp. 293–301.

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Rodionova, E.I., Kochevalina, M.Y., Kotenkova, E.V. et al. Detection of volatile organic compounds associated with hepatocellular carcinoma by macrosmatic animals: Approaches to the search for new tumor markers. Biol Bull Russ Acad Sci 42, 239–245 (2015). https://doi.org/10.1134/S1062359015030103

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Keywords

  • Volatile Organic Compound
  • Biology Bulletin
  • Healthy Mouse
  • Formyl Peptide Receptor
  • Aviation Security