Detecting Bacterial Biofilms Using Fluorescence Hyperspectral Imaging and Various Discriminant Analyses

Biofilms formed on the surface of agro-food processing facilities can cause food poisoning by providing an environment in which bacteria can be cultured. Therefore, hygiene management through initial detection is important. This study aimed to assess the feasibility of detecting Escherichia coli (E. coli) and Salmonella typhimurium (S. typhimurium) on the surface of food processing facilities by using fluorescence hyperspectral imaging. E. coli and S. typhimurium were cultured on high-density polyethylene and stainless steel coupons, which are the main materials used in food processing facilities. We obtained fluorescence hyperspectral images for the range of 420–730 nm by emitting UV light from a 365 nm UV light source. The images were used to perform discriminant analyses (linear discriminant analysis, k-nearest neighbor analysis, and partial-least squares discriminant analysis) to identify and classify coupons on which bacteria could be cultured. The discriminant performances of specificity and sensitivity for E. coli (1–4 log CFU·cm−2) and S. typhimurium (1–6 log CFU·cm−2) were over 90% for most machine learning models used, and the highest performances were generally obtained from the k-nearest neighbor (k-NN) model. The application of the learning model to the hyperspectral image confirmed that the biofilm detection was well performed. This result indicates the possibility of rapidly inspecting biofilms using fluorescence hyperspectral images.

[1]  Jieping Ye,et al.  Least squares linear discriminant analysis , 2007, ICML '07.

[2]  I. Singleton,et al.  Sources and contamination routes of microbial pathogens to fresh produce during field cultivation: A review , 2018, Food Microbiology.

[3]  P. Muriana,et al.  Efficacy of Commercial Sanitizers Used in Food Processing Facilities for Inactivation of Listeria monocytogenes, E. Coli O157:H7, and Salmonella Biofilms , 2019, Foods.

[4]  V. Rai,et al.  Bacterial Quorum Sensing and Food Industry , 2011 .

[5]  Brian Everitt,et al.  Miscellaneous Clustering Methods , 2011 .

[6]  Deepak Bhatnagar,et al.  Integration of Fluorescence and Reflectance Visible Near-Infrared (VNIR) Hyperspectral Images for Detection of Aflatoxins in Corn Kernels , 2016 .

[7]  David A. Landgrebe,et al.  A survey of decision tree classifier methodology , 1991, IEEE Trans. Syst. Man Cybern..

[8]  B. Hemdan,et al.  Prevalence of E. coli , Salmonella , and Listeria spp. as potential pathogens: A comparative study for biofilm of sink drain environment , 2020 .

[9]  Yoshio Makino,et al.  Hyperspectral imaging and multispectral imaging as the novel techniques for detecting defects in raw and processed meat products: Current state-of-the-art research advances , 2018 .

[10]  P. Dhulster,et al.  Biofilm formation and persistence on abiotic surfaces in the context of food and medical environments , 2014, Archives of Microbiology.

[11]  C. Basler,et al.  Outbreaks of Human Salmonella Infections Associated with Live Poultry, United States, 1990–2014 , 2016, Emerging infectious diseases.

[12]  Rosa María García-Gimeno,et al.  Cross-contamination and recontamination by Salmonella in foods: A review , 2012 .

[13]  Y. R. Chen,et al.  HYPERSPECTRAL REFLECTANCE AND FLUORESCENCE IMAGING SYSTEM FOR FOOD QUALITY AND SAFETY , 2001 .

[14]  Bing Li,et al.  Formation and development of Staphylococcus biofilm: With focus on food safety , 2017 .

[15]  G. A. Faria,et al.  Antimicrobial susceptibility, biofilm formation and genetic profiles of Escherichia coli isolated from retail chicken meat. , 2020, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[16]  Koon Hoong Teh,et al.  Proteolysis produced within biofilms of bacterial isolates from raw milk tankers. , 2012, International journal of food microbiology.

[17]  J. Meng,et al.  Development of a model for evaluation of microbial cross-contamination in the kitchen. , 1998, Journal of food protection.

[18]  F. Lombó,et al.  Biofilms in the Food Industry: Health Aspects and Control Methods , 2018, Front. Microbiol..

[19]  H. Einarsson,et al.  Microbial Adhesion to Processing Lines for Fish Fillets and Cooked Shrimp: Influence of Stainless Steel Surface Finish and Presence of Gram-Negative Bacteria on the Attachment of Listeria monocytogenes** , 2005 .

[20]  B. Sheldon,et al.  Transfer of Salmonella and Campylobacter from stainless steel to romaine lettuce. , 2003, Journal of food protection.

[21]  D. Davies,et al.  Understanding biofilm resistance to antibacterial agents , 2003, Nature Reviews Drug Discovery.

[22]  Jun-Hu Cheng,et al.  Hyperspectral Imaging Sensing of Changes in Moisture Content and Color of Beef During Microwave Heating Process , 2018, Food Analytical Methods.

[23]  S. Oshita,et al.  Rapid detection of Escherichia coli contamination in packaged fresh spinach using hyperspectral imaging. , 2011, Talanta.

[24]  F. López-Gálvez,et al.  Cross-contamination of fresh-cut lettuce after a short-term exposure during pre-washing cannot be controlled after subsequent washing with chlorine dioxide or sodium hypochlorite. , 2010, Food microbiology.

[25]  M. Kim,et al.  Rapid assessment of corn seed viability using short wave infrared line-scan hyperspectral imaging and chemometrics , 2018 .

[26]  Rebecca M. Goulter,et al.  Attachment of different Salmonella serovars to materials commonly used in a poultry processing plant. , 2009, Food microbiology.

[27]  Sang-Do Ha,et al.  Biofilm formation in food industries: A food safety concern , 2013 .

[28]  S. Lanteri,et al.  The potential of spectral and hyperspectral-imaging techniques for bacterial detection in food: A case study on lactic acid bacteria. , 2016, Talanta.

[29]  J. L. Hodges,et al.  Discriminatory Analysis - Nonparametric Discrimination: Consistency Properties , 1989 .

[30]  A. Ganapathiraju,et al.  LINEAR DISCRIMINANT ANALYSIS - A BRIEF TUTORIAL , 1995 .

[31]  M. Schaepman,et al.  Retrieval of spruce leaf chlorophyll content from airborne image data using continuum removal and radiative transfer , 2013 .

[32]  Moon S. Kim,et al.  Microbial biofilm detection on food contact surfaces by macro-scale fluorescence imaging , 2010 .

[33]  Renfu Lu,et al.  Hyperspectral and multispectral imaging for evaluating food safety and quality , 2013 .

[34]  Anália Lourenço,et al.  Critical review on biofilm methods , 2017, Critical reviews in microbiology.

[35]  G. Pugliese,et al.  Severe Streptococcus pyogenes Infections, United Kingdom, 2003–2004 , 2008, Emerging infectious diseases.

[36]  Qigang Jiang,et al.  Hyperspectral Inversion of Petroleum Hydrocarbon Contents in Soil Based on Continuum Removal and Wavelet Packet Decomposition , 2020 .

[37]  G. Nychas,et al.  Attachment and biofilm formation by foodborne bacteria in meat processing environments: causes, implications, role of bacterial interactions and control by alternative novel methods. , 2014, Meat science.

[38]  Da-Wen Sun,et al.  Hyperspectral imaging technique for evaluating food quality and safety during various processes: A review of recent applications , 2017 .

[39]  Ning Wang,et al.  Detecting chilling injury in Red Delicious apple using hyperspectral imaging and neural networks , 2009 .

[40]  S. Ha,et al.  A review of microbial biofilms of produce: Future challenge to food safety , 2012, Food Science and Biotechnology.

[41]  M. Nauta,et al.  Cross‐contamination in the kitchen: effect of hygiene measures , 2008, Journal of applied microbiology.

[42]  C. Wallace,et al.  Determining common contributory factors in food safety incidents – A review of global outbreaks and recalls 2008–2018 , 2020, Trends in Food Science & Technology.

[43]  D. Salvi,et al.  Role of contaminated organic particles in cross-contamination of fresh produce during washing and sanitation , 2020 .

[44]  B. Turner,et al.  Estimating foliage nitrogen concentration from HYMAP data using continuum, removal analysis , 2004 .

[45]  G. T. Werner [Salmonella infections]. , 1977, Fortschritte der Medizin.

[46]  E. Ferreira,et al.  Near-infrared spectroscopy for the detection and quantification of bacterial contaminations in pharmaceutical products. , 2015, International journal of pharmaceutics.

[47]  Transfer of Salmonella enterica Serovar Typhimurium from Beef to Tomato through Kitchen Equipment and the Efficacy of Intermediate Decontamination Procedures. , 2016, Journal of food protection.

[48]  Xujun Ye,et al.  Monitoring of bacterial contamination on chicken meat surface using a novel narrowband spectral index derived from hyperspectral imagery data. , 2016, Meat science.

[49]  G. M. Sapers,et al.  Biofilm formation, cellulose production, and curli biosynthesis by Salmonella originating from produce, animal, and clinical sources. , 2005, Journal of food protection.

[50]  Xingyi Huang,et al.  Application of Hyperspectral Imaging as a Nondestructive Technique for Foodborne Pathogen Detection and Characterization. , 2019, Foodborne pathogens and disease.

[51]  Di Wu,et al.  Potential of time series-hyperspectral imaging (TS-HSI) for non-invasive determination of microbial spoilage of salmon flesh. , 2013, Talanta.

[52]  Paolo Dario,et al.  Smartphone-Based Food Diagnostic Technologies: A Review , 2017, Sensors.

[53]  Da-Wen Sun,et al.  Recent development in rapid detection techniques for microorganism activities in food matrices using bio-recognition: A review , 2020 .

[54]  Da-Wen Sun,et al.  Recent Progress of Hyperspectral Imaging on Quality and Safety Inspection of Fruits and Vegetables: A Review. , 2015, Comprehensive reviews in food science and food safety.

[55]  C. Ripolles-Avila,et al.  Biofilms in the Spotlight: Detection, Quantification, and Removal Methods. , 2018, Comprehensive reviews in food science and food safety.

[56]  K. Bohinc,et al.  Bacterial adhesion rate on food grade ceramics and Teflon as kitchen worktop surfaces. , 2020, International journal of food microbiology.

[57]  B. F. Rossi,et al.  Cross-Contamination and Biofilm Formation by Salmonella enterica Serovar Enteritidis on Various Cutting Boards. , 2017, Foodborne pathogens and disease.

[58]  Hyun-Chul Kim,et al.  Face recognition using LDA mixture model , 2002, Object recognition supported by user interaction for service robots.