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LPS-Induced Immune System Stimulation Alters Urinary Volatiles and Behaviour in Growing Pigs

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Chemical Signals in Vertebrates 14

Abstract

Volatile compounds from body fluids and secretions may indicate the health status of individuals to other conspecifics. We sought to identify urinary volatiles that might act as biomarkers indicative of the health status of growing pigs. Immune system stimulation (ISS) was induced in pigs (N = 5) by intramuscular (IM) injection of bacterial lipopolysaccharide (LPS; 25 µg/kg BW). Urine samples were collected before (baseline) and after LPS treatment. The urinary headspace volatile compounds were identified using Solid-phase microextraction (SPME) coupled with GC-MS. Pig eye temperatures  was measured using an infrared imaging technique, and behaviours (i.e. standing, feeding, drinking, moving, lying, sitting and active) were video-recorded and quantified 24 h before and after ISS. Data were analysed using mixed model ANOVA examining periods before and after LPS administration with pigs serving as their own control. Pig eye/body temperature increased post-ISS (at 6 h, P = 0.03) and correlated negatively with active behaviours (r = −0.64, P = 0.048). Relative to pre-ISS, pigs spent less time standing (P = 0.018), moving (P = 0.061) and active (P < 0.0001) during the post-ISS period. SPME-GC-MS revealed 7.2- and 4.3-fold increases in 3-Methylphenol (P < 0.0001) and 4-Ethylphenol (P = 0.005), respectively, in post-ISS urine compared with urine collected during the pre-ISS period. In conclusion, ISS reduced pig activity, and elevated (P < 0.01) urinary levels of 3-Methylphenol and 4-Ethylphenol. Behavioural changes and volatile molecules may be used as a non-invasive method for detection of fever, illness and health in farm and possibly other animals. Furthermore, the effects of 3-Methylphenol and 4-Ethylphenol on the behaviour of other pigs remain to be determined.

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References

  • American Society of Animal Science (2010) 3rd edn. Champaign, IL, USA

    Google Scholar 

  • Amory JR, Pearce GP (2000) Alarm pheromones in urine modify the behavior of weaner pigs. Anim Welf 9:167–175

    Google Scholar 

  • Angle C, Waggoner LP, Ferrando A et al (2016) Canine detection of the volatilome: a review of implications for pathogen and disease detection. Front Vet Sci 3:47

    Article  Google Scholar 

  • Apfelbach R, Parsons MH, Soini HA et al (2015) Are single odorous components of a predator to elicit defensive behaviors in prey species? Front Neurosci 9:263

    Article  Google Scholar 

  • Arakawa H, Arakawa K, Deak T (2010) Acute illness induces the release of aversive odor cues from adult, but not prepubertal, male rats and suppresses social investigation by conspecifics. Behav Neurosci 123:964–978

    Article  Google Scholar 

  • Bouatra S, Aziat F, Mandal R et al (2013) The human urine metabolome. PLoS One 9:e73076

    Article  Google Scholar 

  • Brechbuhl J, Moine F, Klaey M et al (2013) Mouse alarm pheromone shares structural similarity with predator scents. Proc Natl Acad Sci USA 110:4762–4767

    Article  CAS  Google Scholar 

  • Brunius C, Vidanarachchi JK, Tomankova J et al (2016) Skatole metabolites in urine as a biological marker of pigs with enhanced hepatic metabolism. Animal 10:1734–1740

    Article  CAS  Google Scholar 

  • Būda V, Mozūraitis R, Kutra J et al (2012) p-Cresol: a sex pheromone component identified from the estrous urine of mares. J Chem Ecol 38:811–813

    Article  Google Scholar 

  • Buljubasic F, Buchbauer G (2015) The scent of human diseases: a review on specific volatile organic compounds as diagnostic biomarkers. Flavour Frag J 30:5–25

    Article  CAS  Google Scholar 

  • Gaykema RPA, Goehler LE (2009) Lipopolysaccharide challenge-induced suppression of Fos in hypothalamic orexin neurons: their potential role in sickness behavior. Brain Behav Immun 23:926–930

    Article  CAS  Google Scholar 

  • Gervasi SK, Opiekun M, Martin T, Beauchamp GK, Kimball BA (2018) Sharing an environment with sick conspecifics alters odor of health animals. Sci Rep 8:14255

    Article  Google Scholar 

  • Haick H, Broza YY, Pawel M et al (2014) Assessment, origin, and implementation of breath volatile cancer biomarkers. Chem Soc Rev 43:1423–1449

    Article  CAS  Google Scholar 

  • Human Metabolome Database. www.hmdb.ca/metabolites/HMDB11623. Accessed on 3rd Mar 2017

  • Johnson RW, von Borell E (1994) Lipopolysaccharide-induced sickness behavior in pigs is inhibited by pretreatment with indomethacin. J Anim Sci 72:309–314

    Article  CAS  Google Scholar 

  • Khalid T, Aggio R, White P et al (2015) Urinary volatile organic compounds for the detection of prostrate cancer. PLoS One 10:e0143283

    Article  Google Scholar 

  • Khamis MM, Adamko DJ, El-Aneed A (2017) Mass spectrometric based approaches in urine metabolomics and biomarker discovery. Mass Spectrom Rev 36:115–134

    Article  CAS  Google Scholar 

  • Kimball BA (2016) Volatile metabolome: problems and prospects. Bioanalysis 8:1987–1991

    CAS  PubMed  Google Scholar 

  • Kimball BA, Yamazaki K, Kohler D et al (2013) Avian influenza infection alters fecal odor in mallards. PLoS One 8:e75411

    Article  CAS  Google Scholar 

  • Kimball BA, Wilson DA, Daniel WW (2016a) Alterations of the volatile metabolome in mouse models of Alzheimer’s disease. Sci Rep 6:19495

    Article  CAS  Google Scholar 

  • Kimball BA, Cohen AS, Gordon AR et al (2016b) Brain injury alters volatile metabolome. Chem Senses 41:407–414

    Article  CAS  Google Scholar 

  • Kuehl RO (2000). Design of Experiments: Statistical principles of research design and analysis. 2nd edn, p 136

    Google Scholar 

  • Kwak J, Preti G (2011) Volatile disease biomarkers in breath: a critique. Curr Pharma Biotech 12:1067–1074

    Article  CAS  Google Scholar 

  • Lo YC, Koziel JA, Cai L et al (2008) Simultaneous chemical and sensory characterization of volatile organic compounds and semi-volatile organic compounds emitted from swine manure using solid phase microextraction and multidimensional gas chromatography-mass spectrometry-olfactometry. J Environ Qual 37:521–534

    Article  CAS  Google Scholar 

  • Lopes PC, Block P, Konig B (2016) Infection-induced behavioural changes reduce connectivity and the potential for disease spread in wild mice contact networks. Sci Rep 6:31790

    Article  CAS  Google Scholar 

  • Mozuraitis R, Buda V, Kutra J et al (2012) p- and m-Cresols emitted from estrous urine are reliable volatile chemical markers of ovulation in mares. Anim Reprod Sci 130:51–56

    Article  CAS  Google Scholar 

  • Nakhleh MK, Amal H, Jeries R et al (2017) Diagnosis and classification of 17 diseases from 1404 subjects via pattern analysis of exhaled molecules. ACS Nano 11:112–125

    Article  CAS  Google Scholar 

  • Ni JQ, Robarge WP, Xiao C et al (2012) Volatile organic compounds at swine facilities: a critical review. Chemosphere 89:769–788

    Article  CAS  Google Scholar 

  • Olsson MJ, Lundstrom JN, Kimball BA et al (2014) The scent of disease: human body odor contains an early chemosensory cues of sickness. Psychol Sci 25:817–823

    Article  Google Scholar 

  • Penn D, Schneider G, White K et al (1998) Influenza infection neutralizes the attractiveness of male odour to female mice (Mus musculus). Ethology 104:685–694

    Article  Google Scholar 

  • Petry A, McGilvray W, Rakhshandeh AR et al (2017) Technical note: assessment of an alternative technique for measuring body temperature in pigs. J Anim Sci 95:3270–3274

    CAS  PubMed  Google Scholar 

  • Pijls KE, Smolinska A, Jonkers DM et al (2016) A profile of volatile organic compounds in exhaled air as a potential non-invasive biomarker for liver cirrhosis. Sci Rep 6:19903

    Article  CAS  Google Scholar 

  • Poddar-Sarkar M, Brahmachary RL (2014) Pheromones of tiger and other big cats. In: Mucignat-Caretta C (ed) Neurobiology of chemical communication. CRC Press/Taylor & Francis, Boca Raton (FL); Chapter 15

    Google Scholar 

  • Rakhshandeh A, de Lange CF (2012) Evaluation of chronic immune system stimulation models in growing pigs. Animal 6:305–310

    Article  CAS  Google Scholar 

  • SAS Institute 2012. SAS statistics, Cary, NC. Version 9.4

    Google Scholar 

  • Sethi S, Nanda R, Chakraborty T (2013) Clinical applications of volatile organic compound analysis in detecting infectious diseases. Curr Microbiol Rev 26:462–475

    Article  CAS  Google Scholar 

  • Shirasu M, Touhara K (2011) The scent of disease: volatile organic compounds of the human body related to disease and disorder. J Biochem 150:257–266

    Article  CAS  Google Scholar 

  • Silva CL, Passos M, Camara JS (2011) Investigation of urinary volatile organic metabolites as potential cancer biomarkers by solid-phase microextraction in combination with gas chromatography-mass spectrometry. Br J Cancer 105:1894–1904

    Article  CAS  Google Scholar 

  • Tirindelli R, Dibattista M, Pifferi S et al (2009) From pheromones to behavior. Physiol Rev 89:921–956

    Article  CAS  Google Scholar 

  • Vieuille-Thomas C, Signoret JP (1992) Pheromonal transmission of an aversive experience in domestic pig. J Chem Ecol 18:1551–1557

    Article  CAS  Google Scholar 

  • Zhang JX, Sun L, Zhang JH et al (2008) Sex- and gonad-affecting scent compounds and 3 male pheromones in the rat. Chem Senses 33:611–621

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by funding from Animal Biotech LLC., to Texas Tech University. JJM declares a conflict of interest in that he is an equity partner in Animal Biotech LLC.

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Correspondence to John J. McGlone .

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Devaraj, S., Rakhshandeh, A., Aviles-Rosa, E., McGlone, J.J. (2019). LPS-Induced Immune System Stimulation Alters Urinary Volatiles and Behaviour in Growing Pigs. In: Buesching, C. (eds) Chemical Signals in Vertebrates 14. Springer, Cham. https://doi.org/10.1007/978-3-030-17616-7_5

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