Skip to main content

Advertisement

SpringerLink
Log in

Real-Time Detection of Volatiles Released During Meat Spoilage: a Case Study of Modified Atmosphere-Packaged Chicken Breast Fillets Inoculated with Br. thermosphacta

  • Published:
Food Analytical Methods Aims and scope Submit manuscript

Abstract

The microbial spoilage of meat is accompanied by the release of volatile organic compounds (VOCs), many of which are odorous. These compounds give spoiled meat its characteristic pungent, sour, sulphury odour that provides consumers with an indication that the meat is unpalatable. Characterising meat spoilage based on volatile markers is of interest to the food industry in view of developing food freshness indicators (FFIs) to maintain food quality and reduce food waste. Conventional analytical methods for detecting VOCs developing during food spoilage involve intermittent sampling that delivers only snapshots of the release processes and thereby only limited information on the kinetics of their production and release. Proton-transfer-reaction mass spectrometry (PTR-MS) is an on-line technique that enables the detection of VOCs in real-time, thereby offering the possibility to follow the release of VOCs with a high time resolution. An analytical method using PTR-MS was developed to enable the continuous detection of VOCs released from chicken breast fillets inoculated with Brochothrix thermosphacta and stored under modified atmosphere (30 % CO2, 70 % O2) at 4 °C for 1 week. The meat spoilage VOCs detected by PTR-MS displayed different temporal dynamics of production and release, depending on the extent of spoilage. This paper describes the development of an analytical set-up for real-time detection of volatile spoilage markers using PTR-MS. This case study using inoculated chicken breast fillets demonstrates the applicability of this method to characterise individual VOC release patterns, which is of potential utility in the development of FFIs for the consumer market.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ammor MS, Argyri A, Nychas G-JE (2009) Rapid monitoring of the spoilage of minced beef stored under conventionally and active packaging conditions using Fourier transform infrared spectroscopy in tandem with chemometrics. Meat Sci 81:507–514. doi:10.1016/j.meatsci.2008.10.015

    Article  CAS  Google Scholar 

  • Argyri AA, Jarvis RM, Wedge D, Xu Y, Panagou EZ, Goodacre R, Nychas G-JE (2013) A comparison of Raman and FT-IR spectroscopy for the prediction of meat spoilage. Food Control 29:461–470. doi:10.1016/j.foodcont.2012.05.040

    Article  CAS  Google Scholar 

  • Argyri AA, Mallouchos A, Panagou EZ, Nychas G-JE (2015) The dynamics of the HS/SPME–GC/MS as a tool to assess the spoilage of minced beef stored under different packaging and temperature conditions. Int J Food Microbiol 93:51–58. doi:10.1016/j.ijfoodmicro.2014.09.020

    Article  Google Scholar 

  • Balamatsia CC, Paleologos EK, Kontominas MG, Savvaidis IN (2006) Correlation between microbial flora, sensory changes and biogenic amines formation in fresh chicken meat stored aerobically or under modified atmosphere packaging at 4 °C: possible role of biogenic amines as spoilage indicators. Antonie Van Leeuwenhoek 89:9–17. doi:10.1007/s10482-005-9003-4

    Article  CAS  Google Scholar 

  • Balamatsia CC, Patsias A, Kontominas MG, Savvaidis IN (2007) Possible role of volatile amines as quality-indicating metabolites in modified atmosphere-packaged chicken fillets: correlation with microbiological and sensory attributes. Food Chem 104:1622–1628. doi:10.1016/j.foodchem.2007.03.013

    Article  CAS  Google Scholar 

  • Balasubramanian S, Panigrahi S, Logue CM, Marchello M, Doetkott C, Gu H, Sherwood JS, Nolan LK (2004) Spoilage identification of beef using an electronic nose system. Trans ASAE 47:1625–1633. doi:10.13031/2013.17593

    Article  Google Scholar 

  • Beauchamp J, Herbig J, Dunkl J, Singer W, Hansel A (2013) On the performance of proton-transfer-reaction mass spectrometry for breath-relevant gas matrices. Meas Sci Technol 24:125003. doi:10.1088/0957-0233/24/12/125003

    Article  Google Scholar 

  • Bhattacharjee P, Panigrahi S, Lin D, Logue CM, Sherwood JS, Doetkott C, Marchello M (2011) A comparative qualitative study of the profile of volatile organic compounds associated with Salmonella contamination of packaged aged and fresh beef by HS-SPME/GC-MS. J Food Sci Technol 48:1–13. doi:10.1007/s13197-010-0138-6

    Article  CAS  Google Scholar 

  • Blickstad E (1983) Growth and end product formation of two psychrotrophic Lactobacillus spp. and Brochothrix thermosphacta ATCC 11509 T at different pH values and temperatures. Appl Environ Microbiol 46:1345–1350

    CAS  Google Scholar 

  • Blickstad E, Molin G (1984) Growth and end-product formation in fermenter cultures of Brochothrix thermosphacta ATCC 11509T and two psychrotrophic Lactobacillus spp. in different gaseous atmospheres. J Appl Bacteriol 57:213–220. doi:10.1111/j.1365-2672.1984.tb01385.x

    Article  CAS  Google Scholar 

  • Bunge M, Araghipour N, Mikoviny T, Dunkl J, Schnitzhofer R, Hansel A, Schinner F, Wisthaler A, Margesin R, Märk TD (2008) On-line monitoring of microbial volatile metabolites by proton transfer reaction- mass spectrometry. Appl Environ Microbiol 74:2179–2186. doi:10.1128/AEM.02069-07

    Article  CAS  Google Scholar 

  • Casaburi A, de Filippis F, Villani F, Ercolino D (2014) Activities of strains of Brochothrix thermosphacta in vitro and in meat. Food Res Int 62:366–374. doi:10.1016/j.foodres.2014.03.019

    Article  CAS  Google Scholar 

  • Casaburi A, Piombino P, Nychas G-J, Villani F, Ercolini D (2015) Bacterial populations and the volatilome associated to meat spoilage. Food Microbiol 45A:83–102. doi:10.1016/j.fm.2014.02.002

    Article  Google Scholar 

  • Chen Q, Hui Z, Zhao J, Ouyang Q (2014) Evaluation of chicken freshness using a low-cost colorimetric sensor array with AdaBoosteOLDA classification algorithm. LWT Food Sci Technol 57:502–507. doi:10.1016/j.lwt.2014.02.031

    Article  Google Scholar 

  • Collins-Thompson DL, Sørhaug T, Witter LD, Ordal ZJ (1972) Taxonomic consideration of Microbacterium lacticum, Microbacterium flavum, and Microbacterium thermosphactum. Int J Syst Bacteriol 22:65–72. doi:10.1099/00207713-22-2-65

    Article  Google Scholar 

  • Dainty RH (1996) Chemical/biochemical detection of spoilage. Int J Food Microbiol 33:19–33. doi:10.1016/0168-1605(96)01137-3

    Article  CAS  Google Scholar 

  • Dainty RH, Hibbard CM (1980) Aerobic metabolism of Brochothrix thermosphacta growing on meat surfaces and in laboratory media. J Appl Bacteriol 48:387–396. doi:10.1111/j.1365-2672.1980.tb01027.x

    Article  CAS  Google Scholar 

  • Dainty RH, Hofman F (1983) The influence of glucose concentration and culture incubation time on end-product formation during aerobic growth of Brochothrix thermosphacta. J Appl Bacteriol 55:233–239. doi:10.1111/j.1365-2672.1983.tb01320.x

    Article  CAS  Google Scholar 

  • De Gouw J, Warneke C, Karl T, Eerdekens G, van der Veen C, Fall R (2003) Sensitivity and specificity of atmospheric trace gas detection by proton-transfer-reaction mass spectrometry. Int J Mass Spectrom 223-224:365–382. doi:10.1016/S1387-3806(02)00926-0

    Article  Google Scholar 

  • Doulgeraki AI, Ercolini D, Villani F, Nychas G-JE (2012) Spoilage microbiota associated to the storage of raw meat in different conditions. Int J Food Microbiol 157:130–141. doi:10.1016/j.ijfoodmicro.2012.05.020

    Article  Google Scholar 

  • Eilamo M, Kinnunen A, Latva-Kala K, Ahvenainen R (1998) Effects of packaging and storage conditions on volatile compounds in gas-packed poultry meat. Food Addit Contam 15:217–228. doi:10.1080/02652039809374633

    Article  CAS  Google Scholar 

  • Ercolini D, Russo F, Torrieri E, Masi P, Villani F (2006) Changes in the spoilage-related microbiota of beef during refrigerated storage under different packaging conditions. Appl Environ Microbiol 72:4663–4671. doi:10.1128/AEM.00468-06

    Article  CAS  Google Scholar 

  • Farber JM (1991) Microbiological aspects of modified-atmosphere packaging technology - a review. J Food Prot 54:58–70

    Article  Google Scholar 

  • Gallas L, Standarová E, Steinhauserová I, Steinhauser L, Vorlová L (2010) Formation of biogenic amines in chicken meat stored under modified atmosphere. Acta Vet Brno 79:107–116. doi:10.2754/avb201079S9S107

    Article  Google Scholar 

  • Grau FH (1983) End products of glucose fermentation by Brochothrix thermosphacta. Appl Environ Microbiol 45:84–90

    CAS  Google Scholar 

  • Herrero AM (2008) Raman spectroscopy a promising technique for quality assessment of meat and fish: a review. Food Chem 107:1642–1651. doi:10.1016/j.foodchem.2007.10.014

    Article  CAS  Google Scholar 

  • Herrero AM, Carmona P, López-López I, Jiménez-Colmenero F (2008) Raman spectroscopic evaluation of meat batter structural changes induced by thermal treatment and salt addition. J Agric Food Chem 56:7119–7124. doi:10.1021/jf800925s

    Article  CAS  Google Scholar 

  • Huang L, Zhao J, Chen Q, Zhang Y (2014) Nondestructive measurement of total volatile basic nitrogen (TVB-N) in pork meat by integrating near infrared spectroscopy, computer vision and electronic nose techniques. Food Chem 145:228–236. doi:10.1016/j.foodchem.2013.06.073

    Article  CAS  Google Scholar 

  • Jääskeläinen E, Hultmann J, Parshintsev J, Riekkola M-L, Björkroth J (2016) Development of spoilage bacterial community and volatile compounds in chilled beef under vacuum or high oxygen atmospheres. Int J Food Microbiol 223:25–32. doi:10.1016/j.ijfoodmicro.2016.01.022

    Article  Google Scholar 

  • Jiménez SM, Salsi MS, Tiburzi MC, Rafaghelli RC, Tessi MA, Coutaz VR (1997) Spoilage microflora in fresh chicken breast stored at 4 °C: influence of packaging methods. J Appl Microbiol 83:613–618. doi:10.1046/j.1365-2672.1997.00276.x

    Article  Google Scholar 

  • Keck L, Hoeschen C, Oeh U (2008) Effects of carbon dioxide in breath gas on proton transfer reaction-mass spectrometry (PTR-MS) measurements. Int J Mass Spectrom 270:156–165. doi:10.1016/j.ijms.2007.12.009

    Article  CAS  Google Scholar 

  • Lindinger W, Hansel A, Jordan A (1998a) On-line monitoring of volatile organic compounds at pptv levels by means of proton-transfer-reaction mass spectrometry (PTR-MS) medical applications, food control and environmental research. Int J Mass Spectrom Ion Process 173:191–241. doi:10.1016/S0168-1176(97)00281-4

    Article  CAS  Google Scholar 

  • Lindinger W, Hansel A, Jordan A (1998b) Proton-transfer-reaction mass spectrometry (PTR–MS): on-line monitoring of volatile organic compounds at pptv levels. Chem Soc Rev 27:347–354. doi:10.1039/A827347Z

    Article  CAS  Google Scholar 

  • Moon S-Y, Li-Chan ECY (2004) Development of solid-phase microextraction methodology for analysis of headspace volatile compounds in simulated beef flavour. Food Chem 88:141–149. doi:10.1016/j.foodchem.2004.04.002

    Article  CAS  Google Scholar 

  • Olivares A, Dryahina K, Španěl P, Flores M (2012) Rapid detection of lipid oxidation in beef muscle packed under modified atmosphere by measuring volatile organic compounds using SIFT-MS. Food Chem 135:1801–1808. doi:10.1016/j.foodchem.2012.06.075

    Article  CAS  Google Scholar 

  • Ordóñez JA, de Pablo B, de Castro BP, Asensio MA, Sanz B (1991) Selected chemical and microbiological changes in refrigerated pork stored in carbon dioxide and oxygen enriched atmospheres. J Agric Food Chem 39:668–672. doi:10.1021/jf00004a008

    Article  Google Scholar 

  • Pin C, Garcia de Fernando GD, Ordóñez JA (2002) Effect of modified atmosphere composition on the metabolism of glucose by Brochothrix thermosphacta. Appl Environ Microbiol 68:4441–4447. doi:10.1128/AEM.68.9.4441-4447.2002

    Article  CAS  Google Scholar 

  • Rajamäki T, Alakomi H-L, Ritvanen T, Skytta E, Smolander M, Ahvenainen R (2006) Application of an electronic nose for quality assessment of modified atmosphere packaged poultry meat. Food Control 17:5–13. doi:10.1016/j.foodcont.2004.08.002

    Article  Google Scholar 

  • Rokka M, Eerola S, Smolander M, Alakomi H-L, Ahvenainen R (2004) Monitoring of the quality of modified atmosphere packaged broiler chicken cuts stored in different temperature conditions. Food Control 15:601–607. doi:10.1016/j.foodcont.2003.10.002

    Article  CAS  Google Scholar 

  • Romano A, Fischer L, Herbig J, Campbell-Sills H, Coulon J, Lucas P, Cappelin L, Biasioli F (2014) Wine analysis by FastGC proton-transfer reaction-time-of-flight-mass spectrometry. Int J Mass Spectrom 369:81–86. doi:10.1016/j.ijms.2014.06.006

    Article  CAS  Google Scholar 

  • Sahar A, Dufour É (2014) Use of Fourier transform-infrared spectroscopy to predict spoilage bacteria on aerobically stored chicken breast fillets. LWT Food Sci Technol 56:315–320. doi:10.1016/j.lwt.2013.12.009

    Article  CAS  Google Scholar 

  • Silcock P, Alothman M, Zardin E, Heenan S, Siefarth C, Bremer PJ, Beauchamp J (2014) Microbially induced changes in the volatile constituents of fresh chilled pasteurised milk during storage. Food Packag Shelf Life 2:81–90. doi:10.1016/j.fpsl.2014.08.002

    Article  Google Scholar 

  • Steinbacher M, Dommen J, Ammann C, Spirig C, Neftel A, Prevot ASH (2004) Performance characteristics of a proton-transfer-reaction mass spectrometer (PTR-MS) derived from laboratory and field measurements. Int J Mass Spectrom 239:117–128. doi:10.1016/j.ijms.2004.07.015

    Article  CAS  Google Scholar 

  • Ye X, Jin J, Hui G, Yin F, Wang M, Huang J, Ying X, Deng S (2014) Determination of the freshness of beef strip loins (M. longissimus lumborum) using electronic nose. Food Anal Methods 7:1612–1618. doi:10.1007/s12161-014-9796-8

    Article  Google Scholar 

  • Zardin E, Tyapkova O, Büttner A, Beauchamp J (2014) Performance assessment of proton-transfer-reaction time-of-flight mass spectrometry (PTR-TOF-MS) for analysis of isobaric compounds in food-flavour applications. LWT Food Sci Technol 56:153–160. doi:10.1016/j.lwt.2013.10.041

    Article  CAS  Google Scholar 

  • Zhao J, Zhang R (2004) Proton transfer reaction rate constants between hydronium ion (H3O+) and volatile organic compounds. Atmos Environ 38:2177–2185. doi:10.1016/j.atmosenv.2004.01.019

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors are grateful for the financial support from the German Federal Ministry for Economic Affairs and Energy via the German Federation of Industrial Research Associations (AiF) and the Industry Association for Food Technology and Packaging (IVLV), project number AiF 17803N. We are grateful to Horst-Christian Langowski (Fraunhofer IVV and TUM) for his support and advice on performing these experiments, Linda Höll and Rudi Vogel (TUM) for consultation on the microbiology and for supplying the bacterial strain used in these studies and Hannes Petermeier and Bendix Koopmann (TUM) for programming an algorithm in R that was used here to process the PTR-MS data. We additionally thank Olivia Matheis (Fraunhofer IVV) for her assistance in conducting the fragmentation studies of the pure compounds.

Author information

Authors and Affiliations

  1. Chair of Food Packaging Technology, Technische Universität München, Weihenstephaner Steig 22, 85354, Freising, Germany

    Corinna Franke

  2. Department of Sensory Analytics, Fraunhofer Institute for Process Engineering and Packaging IVV, Giggenhauser Str. 35, 85354, Freising, Germany

    Jonathan Beauchamp

Authors
  1. Corinna Franke
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jonathan Beauchamp
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Corinna Franke.

Ethics declarations

Funding

This study was funded by the German Federation of Industrial Research Associations (AiF) and the Industry Association for Food Technology and Packaging (IVLV) project number AiF 17803N.

Conflict of Interest

CF has received a research grant from the AiF but declares no further conflict of interest. JB declares that he has no conflict of interest.

Ethical Approval

This study does not contain any studies with human participants or animals performed by any of the authors.

Informed Consent

Not applicable.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Franke, C., Beauchamp, J. Real-Time Detection of Volatiles Released During Meat Spoilage: a Case Study of Modified Atmosphere-Packaged Chicken Breast Fillets Inoculated with Br. thermosphacta . Food Anal. Methods 10, 310–319 (2017). https://doi.org/10.1007/s12161-016-0585-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12161-016-0585-4

Keywords

Search

Navigation