Rapid and Quantitative Detection of the Microbial Spoilage of Meat by Fourier Transform Infrared Spectroscopy and Machine Learning

ABSTRACT Fourier transform infrared (FT-IR) spectroscopy is a rapid, noninvasive technique with considerable potential for application in the food and related industries. We show here that this technique can be used directly on the surface of food to produce biochemically interpretable “fingerprints.” Spoilage in meat is the result of decomposition and the formation of metabolites caused by the growth and enzymatic activity of microorganisms. FT-IR was exploited to measure biochemical changes within the meat substrate, enhancing and accelerating the detection of microbial spoilage. Chicken breasts were purchased from a national retailer, comminuted for 10 s, and left to spoil at room temperature for 24 h. Every hour, FT-IR measurements were taken directly from the meat surface using attenuated total reflectance, and the total viable counts were obtained by classical plating methods. Quantitative interpretation of FT-IR spectra was possible using partial least-squares regression and allowed accurate estimates of bacterial loads to be calculated directly from the meat surface in 60 s. Genetic programming was used to derive rules showing that at levels of 107 bacteria·g−1 the main biochemical indicator of spoilage was the onset of proteolysis. Thus, using FT-IR we were able to acquire a metabolic snapshot and quantify, noninvasively, the microbial loads of food samples accurately and rapidly in 60 s, directly from the sample surface. We believe this approach will aid in the Hazard Analysis Critical Control Point process for the assessment of the microbiological safety of food at the production, processing, manufacturing, packaging, and storage levels.

[1]  G. G. Stokes "J." , 1890, The New Yale Book of Quotations.

[2]  James M. Jay,et al.  Modern food microbiology , 1970 .

[3]  David G. Stork,et al.  Pattern Classification , 1973 .

[4]  John Holland,et al.  Adaptation in Natural and Artificial Sys-tems: An Introductory Analysis with Applications to Biology , 1975 .

[5]  J. Jacquet [Food microbiology]. , 1980, Annales de la nutrition et de l'alimentation.

[6]  David E. Goldberg,et al.  Genetic Algorithms in Search Optimization and Machine Learning , 1988 .

[7]  R B Tompkin,et al.  The Use of HACCP in the Production of Meat and Poultry Products 1. , 1990, Journal of food protection.

[8]  Harald Labischinski,et al.  Microbiological characterizations by FT-IR spectroscopy , 1991, Nature.

[9]  Blackie. , 2018, The American journal of nursing.

[10]  Mitsuru Mitsumoto,et al.  Near‐Infrared Spectroscopy Determination of Physical and Chemical Characteristics in Beef Cuts , 1991 .

[11]  D. Lin-Vien The Handbook of Infrared and Raman Characteristic Frequencies of Organic Molecules , 1991 .

[12]  John H. Holland,et al.  Adaptation in Natural and Artificial Systems: An Introductory Analysis with Applications to Biology, Control, and Artificial Intelligence , 1992 .

[13]  John R. Koza,et al.  Genetic programming - on the programming of computers by means of natural selection , 1993, Complex adaptive systems.

[14]  M B Cole,et al.  A substrate-mediated assay of bacterial proton efflux/influx to predict the degree of spoilage of beef mince stored at chill temperatures. , 1994, The Journal of applied bacteriology.

[15]  Una-May O'Reilly,et al.  Genetic Programming II: Automatic Discovery of Reusable Programs. , 1994, Artificial Life.

[16]  M. Koohmaraie,et al.  Muscle proteinases and meat aging. , 1994, Meat science.

[17]  G. Nychas,et al.  Storage of poultry meat under modified atmospheres or vacuum packs: possible role of microbial metabolites as indicator of spoilage. , 1994, The Journal of applied bacteriology.

[18]  M. Madruga,et al.  The effect of pH on the formation of maillard‐derived aroma volatiles using a cooked meat system , 1995 .

[19]  Douglas B. Kell,et al.  GMP — good modelling practice: an essential component of good manufacturing practice , 1995 .

[20]  R H Dainty,et al.  Chemical/biochemical detection of spoilage. , 1996, International journal of food microbiology.

[21]  Douglas L. Archer The validation of rapid methods in food microbiology , 1996 .

[22]  Thomas G. Dietterich What is machine learning? , 2020, Archives of Disease in Childhood.

[23]  Wolfgang Banzhaf,et al.  Genetic Programming: An Introduction , 1997 .

[24]  Seth J. Wenger,et al.  Classification of Vegetable Oils by FT-IR , 1997 .

[25]  D B Kell,et al.  Genetic programming:  a novel method for the quantitative analysis of pyrolysis mass spectral data. , 1997, Analytical chemistry.

[26]  Jeffrey Horn,et al.  Handbook of evolutionary computation , 1997 .

[27]  D. Kell,et al.  Classification of pyrolysis mass spectra by fuzzy multivariate rule induction-comparison with regression, K-nearest neighbour, neural and decision-tree methods , 1997 .

[28]  J S Holder,et al.  Microbial status of chicken portions and portioning equipment. , 1997, British poultry science.

[29]  Johanna Smeyers-Verbeke,et al.  Handbook of Chemometrics and Qualimetrics: Part A , 1997 .

[30]  Douglas B. Kell,et al.  Genetic algorithms as a method for variable selection in multiple linear regression and partial least squares regression, with applications to pyrolysis mass spectrometry , 1997 .

[31]  George-John E. Nychas,et al.  Spoilage Processes and Proteolysis in Chicken as Detected by HPLC , 1997 .

[32]  Inteaz Alli,et al.  Identification of proteolytic products as indicators of quality in ground and whole meat , 1998 .

[33]  Hans-Curt Flemming,et al.  FTIR-spectroscopy in microbial and material analysis , 1998 .

[34]  G Monin,et al.  Recent methods for predicting quality of whole meat. , 1998, Meat science.

[35]  F Baganz,et al.  Systematic functional analysis of the yeast genome. , 1998, Trends in biotechnology.

[36]  D. Kell,et al.  The exploitation of chemometric methods in the analysis of spectroscopic data: application to olive oils , 1998 .

[37]  P L Lang,et al.  The in situ infrared microspectroscopy of bacterial colonies on agar plates. , 1998, Cellular and molecular biology.

[38]  Royston Goodacre,et al.  Rapid Differentiation of Closely RelatedCandida Species and Strains by Pyrolysis-Mass Spectrometry and Fourier Transform-Infrared Spectroscopy , 1998, Journal of Clinical Microbiology.

[39]  Nathalie Dupuy,et al.  Identification of Modified Starches Using Infrared Spectroscopy and Artificial Neural Network Processing , 1998 .

[40]  Siegfried Scherer,et al.  Rapid and Reliable Identification of Food-Borne Yeasts by Fourier-Transform Infrared Spectroscopy , 1998, Applied and Environmental Microbiology.

[41]  U. Stahl,et al.  Detection of pathogenic and spoilage micro-organisms in food with the polymerase chain reaction , 1998 .

[42]  D B Kell,et al.  Rapid identification of urinary tract infection bacteria using hyperspectral whole-organism fingerprinting and artificial neural networks. , 1998, Microbiology.

[43]  R. G. Board,et al.  The microbiology of meat and poultry , 1998 .

[44]  John R. Koza Genetic Programming III - Darwinian Invention and Problem Solving , 1999, Evolutionary Computation.

[45]  E. K. Kemsley,et al.  Mid-infrared spectroscopy and chemometrics for the authentication of meat products. , 1999, Journal of agricultural and food chemistry.

[46]  Douglas B. Kell,et al.  SNAPSHOTS OF SYSTEMS - METABOLIC CONTROL ANALYSIS AND BIOTECHNOLOGY , 1999 .

[47]  Peggy G. Braun,et al.  Investigations into the activity of enzymes produced by spoilage-causing bacteria: a possible basis for improved shelf-life estimation , 1999 .

[48]  David G. Stork,et al.  Pattern Classification (2nd ed.) , 1999 .

[49]  John R. Koza,et al.  Genetic Programming III: Darwinian Invention & Problem Solving , 1999 .

[50]  D B Kell,et al.  Detection of the dipicolinic acid biomarker in Bacillus spores using Curie-point pyrolysis mass spectrometry and Fourier transform infrared spectroscopy. , 2000, Analytical chemistry.

[51]  E. Puolanne,et al.  Determination of the buffering capacity of postrigor meat. , 2000, Meat science.

[52]  Athel Cornish-Bowden,et al.  Technological and Medical Implications of Metabolic Control Analysis , 2000 .

[53]  H M Davey,et al.  Rapid analysis of high-dimensional bioprocesses using multivariate spectroscopies and advanced chemometrics. , 2000, Advances in biochemical engineering/biotechnology.

[54]  F.J.G. Schreurs,et al.  Post-mortem changes in chicken muscle , 2000 .

[55]  Douglas B. Kell,et al.  Snapshots of Systems , 2000 .

[56]  J Mackenzie,et al.  Geographical distribution of variant Creutzfeldt-Jakob disease in Great Britain, 1994–2000 , 2001, The Lancet.

[57]  D B Kell,et al.  Genomic computing. Explanatory analysis of plant expression profiling data using machine learning. , 2001, Plant physiology.

[58]  U. Chatterjee,et al.  Effect of unconventional feeds on production cost, growth performance and expression of quantitative genes in growing pigs , 2022, Journal of the Indonesian Tropical Animal Agriculture.

[59]  A. Rayner,et al.  The impact of food scares on price adjustment in the UK beef market , 2001 .

[60]  D Champiat,et al.  Applications of biochemiluminescence to HACCP. , 2001, Luminescence : the journal of biological and chemical luminescence.

[61]  D. G. Newell,et al.  Changes in the Carriage of CampylobacterStrains by Poultry Carcasses during Processing in Abattoirs , 2001, Applied and Environmental Microbiology.

[62]  Søren Balling Engelsen,et al.  Monitoring Industrial Food Processes Using Spectroscopy & Chemometrics , 2001 .

[63]  Lipid Analysis in Oils and Fats , 2001 .

[64]  Shigeo Abe DrEng Pattern Classification , 2001, Springer London.

[65]  S. Kathariou,et al.  Survival of Clinical and Poultry-Derived Isolates of Campylobacter jejuni at a Low Temperature (4°C) , 2001, Applied and Environmental Microbiology.

[66]  Royston Goodacre,et al.  Rapid and quantitative detection of the microbial spoilage of muscle foods: current status and future trends. , 2001 .

[67]  J. Collins,et al.  Quantitative investigation of the effects of chemical decontamination procedures on the microbiological status of broiler carcasses during processing. , 2001, Journal of food protection.

[68]  K V Kumudavally,et al.  Chromatographic analysis of cadaverine to detect incipient spoilage in mutton. , 2001, Meat science.

[69]  Ron Usami,et al.  Enzyme reactor system for the determination of the quality of chicken , 2001 .

[70]  Andrew G. Glen,et al.  APPL , 2001 .

[71]  M. L. González-Miret,et al.  Validation of parameters in HACCP verification using univariate and multivariate statistics. Application to the final phases of poultry meat production , 2001 .

[72]  Edward Giovannucci,et al.  Dietary fat and cancer. , 2002, The American journal of medicine.

[73]  Rudolf Krska,et al.  Fourier transform mid-infrared spectroscopy with attenuated total reflection (FT-IR/ATR) as a tool for the detection of Fusarium fungi on maize , 2002 .

[74]  E. K. Kemsley,et al.  Detection of adulteration in cooked meat products by mid-infrared spectroscopy. , 2002, Journal of agricultural and food chemistry.

[75]  N. Kreiger,et al.  Diet patterns and the risk of renal cell carcinoma , 2002, Public Health Nutrition.

[76]  Fred W. Pohlman,et al.  Rapid Determination of Spinal Cord Content in Ground Beef by Attenuated Total Reflectance Fourier Transform Infrared Spectroscopy , 2003 .

[77]  D. Mayr,et al.  Rapid Detection of Meat Spoilage by Measuring Volatile Organic Compounds by Using Proton Transfer Reaction Mass Spectrometry , 2003, Applied and Environmental Microbiology.

[78]  Royston Goodacre,et al.  Explanatory analysis of spectroscopic data using machine learning of simple, interpretable rules , 2003 .

[79]  A. Eynard,et al.  Characterization of meat consumption and risk of colorectal cancer in Cordoba, Argentina. , 2003, Nutrition.

[80]  R. Goodacre,et al.  Metabolic Profiling: Its Role in Biomarker Discovery and Gene Function Analysis , 2003, Springer US.

[81]  D. Kell,et al.  Explanatory optimization of protein mass spectrometry via genetic search. , 2003, Analytical chemistry.

[82]  Douglas B. Kell,et al.  Functional Genomics Via Metabolic Footprinting: Monitoring Metabolite Secretion by Escherichia Coli Tryptophan Metabolism Mutants Using FT–IR and Direct Injection Electrospray Mass Spectrometry , 2003, Comparative and functional genomics.

[83]  Z. Jiang,et al.  Infrared Spectroscopy , 2022 .