Pathogen enrichment device (PED) enables one-step growth, enrichment and separation of pathogen from food matrices for detection using bioanalytical platforms

Journal of Microbiological Methods

Volumn 117, Issue , 2015, Pages 64-73

  Hahm, Byoung Kwon ^a   Kim, Hyochin ^a   Singh, Atul K ^a   Bhunia, Arun K ^a,b  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

Author keywords

Bacterial separation; Detection; Food; Lateral flow immunoassay; Light scattering sensor; Pathogen enrichment device; QPCR; Sample preparation

Indexed keywords

ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL RAPID DETECTION USING OPTICAL SCATTERING TECHNOLOGY; BACTERIAL SEPARATION; BACTERIUM DETECTION; BIOSENSOR; BIOTECHNOLOGY; CELL COUNT; CELL SUSPENSION; COMPARATIVE STUDY; CONTROLLED STUDY; EGG; ENRICHMENT CULTURE; EQUIPMENT DESIGN; ESCHERICHIA COLI; FILTER; FOOD ANALYSIS; FOOD CONTAMINATION; GENERAL DEVICE; GROUND BEEF; GROWTH CHAMBER; HOTDOG; IMMUNOASSAY; ION EXCHANGE CARTRIDGE; LATERAL FLOW IMMUNOASSAY; LIGHT SCATTERING SENSOR; LIMIT OF DETECTION; LISTERIA MONOCYTOGENES; MEAT; NONHUMAN; PATHOGEN ENRICHMENT DEVICE; PH; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SALMONELLA ENTERICA SEROVAR ENTERITIDIS; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SEPARATION TECHNIQUE; SPINACH; VALIDATION PROCESS; BACTERIUM; DEVICES; FOOD CONTROL; ISOLATION AND PURIFICATION; LIGHT; MICROBIOLOGICAL EXAMINATION; POLYMERASE CHAIN REACTION; PROCEDURES; RADIATION SCATTERING;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; LISTERIA MONOCYTOGENES; SALMONELLA ENTERICA; SPINACIA OLERACEA;

BACTERIA; BACTERIOLOGICAL TECHNIQUES; FOOD MICROBIOLOGY; IMMUNOASSAY; LIGHT; POLYMERASE CHAIN REACTION; SCATTERING, RADIATION;

EID: 84938125347     PISSN: 01677012     EISSN: 18728359     Source Type: Journal    
DOI: 10.1016/j.mimet.2015.07.016     Document Type: Article

References (73)

1. Ahmed W.M., Bayraktar B., Bhunia A.K., Hirleman E.D., Robinson J.P., Rajwa B. Classification of bacterial contamination using image processing and distributed computing. IEEE J. Biomed. Health Inform. 2013, 17:232-239.
2. Annonymous 2008 Listeriosis Outbreak in Ontario Epidemiologic Summary 2009, (Accessed on July 26, 2011).
3. Bae E., Bhunia A.K. Nano optical sensors for food safety and security. Optochemical Nanosensors 2013, 497-512. CRC Press, Taylor and Francis Group, Boca Raton, FL. A. Cusano, F.J. Arregui, M. Giordano, A. Cutolo (Eds.).
4. Bae E., Aroonnual A., Bhunia A.K., Hirleman E.D. On the sensitivity of forward scattering patterns from bacterial colonies to media composition. J. Biophotonics 2011, 4:236-243.
5. Banada P.P., Guo S., Bayraktar B., Bae E., Rajwa B., Robinson J.P., Hirleman E.D., Bhunia A.K. Optical forward-scattering for detection of Listeria monocytogenes and other Listeria species. Biosens. Bioelectron. 2007, 22:1664-1671.
6. Banada P.P., Huff K., Bae E., Rajwa B., Aroonnual A., Bayraktar B., Adil A., Robinson J.P., Hirleman E.D., Bhunia A.K. Label-free detection of multiple bacterial pathogens using light-scattering sensor. Biosens. Bioelectron. 2009, 24:1685-1692.
7. Bhunia A.K. Biosensors and bio-based methods for the separation and detection of foodborne pathogens. Adv. Food Nutr. Res. 2008, 54:1-44.
8. Bhunia A.K. One day to one hour: how quickly can foodborne pathogens be detected?. Future Microbiol 2014, 9:935-946.
9. Biao S., Yuexia W. Evaluation of a multiplex selective enrichment broth SEL for simultaneous detection of injured Salmonella, Escherichia coli O157:H7 and Listeria monocytogenes. Braz. J. Microbiol. 2013, 44:737-742.
10. Bisha B., Brehm-Stecher B.F. Flow-through imaging cytometry for characterization of Salmonella subpopulations in alfalfa sprouts, a complex food system. Biotechnol. J. 2009, 4:880-887.
11. Brehm-Stecher B., Young C., Jaykus L.-A., Tortorello M.L. Sample preparation: the forgotten beginning. J. Food Prot. 2009, 72:1774-1789.
12. CDC Multistate outbreak of listeriosis associated with Jensen Farms cantaloupe-United States, August-September 2011. MMWR Morb. Mortal. Wkly Rep. 2011, 60:1357-1358.
13. CDC Reports of Selected Salmonella Outbreak Investigations 2014, CDC, (http://www.cdc.gov/salmonella/outbreaks.html).
14. CDC Reports of selected E. coli outbreak investigations 2015, Vol. http://www.cdc.gov/ecoli/outbreaks.html, CDC.
15. Chen W.T., Hendrickson R.L., Huang C.P., Sherman D., Geng T., Bhunia A.K., Ladisch M.R. Mechanistic study of membrane concentration and recovery of Listeria monocytogenes. Biotechnol. Bioeng. 2005, 89:263-273.
16. Cho I.-H., Bhandari P., Patel P., Irudayaraj J. Membrane filter-assisted surface enhanced Raman spectroscopy for the rapid detection of E. coli O157:H7 in ground beef. Biosens. Bioelectron. 2015, 64:171-176.
17. Cho I.-H., Bhunia A., Irudayaraj J. Rapid pathogen detection by lateral-flow immunochromatographic assay with gold nanoparticle-assisted enzyme signal amplification. Int. J. Food Microbiol. 2015, 206:60-66.
18. Cocolin L., Rajkovic A., Rantsiou K., Uyttendaele M. The challenge of merging food safety diagnostic needs with quantitative PCR platforms. Trends Food Sci. Technol. 2011, 22(Supplement 1):S30-S38.
19. Dailey R.C., Martin K.G., Smiley R.D. The effects of competition from non-pathogenic foodborne bacteria during the selective enrichment of Listeria monocytogenes using buffered Listeria enrichment broth. Food Microbiol. 2014, 44:173-179.
20. Dwivedi H.P., Jaykus L.-A. Detection of pathogens in foods: the current state-of-the-art and future directions. Crit. Rev. Microbiol. 2011, 37:40-63.
21. Erickson M.C. Microbial risks associated with cabbage, carrots, celery, onions, and deli salads made with these produce items. Compr. Rev. Food Sci. Food Saf. 2010, 9:602-619.
22. Erlich H.A., Gelfand D., Sninsky J.J. Recent advances in the polymerase chain reaction. Science 1991, 252:1643-1651.
23. FDA Bacteriological Analytical Manual Online 2001, AOAC International, Arlington, VA, ([http://www.fda.gov/Food/ScienceResearch/LaboratoryMethods/BacteriologicalAnalyticalManualBAM/default.htm]; Date accessed, January 16, 2014). 8th ed.
24. Fretz R., Pichler J., Sagel U., Much P., Ruppitsch W., Pietzka A.T., Stöger A., Huhulescu S., Heuberger S., Appl G., Werber D., Stark K., Prager R., Flieger A., Karpíšková R., Pfaff G., Allerberger F. Update: multinational listeriosis outbreak due to 'Quargel', a sour milk curd cheese, caused by two different L. monocytogenes serotype 1/2a strains, 2009-2010. Euro Surveill. 2010, 15:1-2.
25. Fukushima H., Kawase J., Etoh Y., Sugama K., Yashiro S., Iida N., Yamaguchi K. Simultaneous screening of 24 target genes of foodborne pathogens in 35 foodborne outbreaks using multiplex real-time SYBR green PCR analysis. Int. J. Microbiol. 2010, 2010:18.
26. Gehring A.G., Albin D.M., Bhunia A.K., Kim H., Reed S.A., Tu S.-I. Mixed culture enrichment of Escherichia coli O157:H7, Listeria monocytogenes, Salmonella enterica, and Yersinia enterocolitica. Food Control 2012, 26:269-273.
27. Geng T., Hahm B.K., Bhunia A.K. Selective enrichment media affect the antibody-based detection of stress-exposed Listeria monocytogenes due to differential expression of antibody-reactive antigens identified by protein sequencing. J. Food Prot. 2006, 69:1879-1886.
28. Geng T., Uknalis J., Tu S.I., Bhunia A.K. Fiber-optic biosensor employing Alexa-Fluor conjugated antibody for detection of Escherichia coli O157:H7 from ground beef in four hours. Sensors 2006, 6:796-807.
29. Hahm B.K., Bhunia A.K. Effect of environmental stresses on antibody-based detection of Escherichia coli O157:H7, Salmonella enterica serotype Enteritidis and Listeria monocytogenes. J. Appl. Microbiol. 2006, 100:1017-1027.
30. Hahm B.K., Kim H., Bhunia A.K. Enrichment and detection of Escherichia coli O157:H7, Salmonella Typhimurium and Listeria monocytogenes using a sample preparation device, PEDD (Pathogen Enrichment and Detection Device). American Society for Microbiology General Meeting 2007, ASM, Toronto, ON, Canada, (pp. Abstr. P-118).
31. He Y., Reed S., Bhunia A.K., Gehring A., Nguyen L.-H., Irwin P.L. Rapid identification and classification of Campylobacter spp. using laser optical scattering technology. Food Microbiol. 2015, 47:28-35.
32. Hein I., Klein D., Lehner A., Bubert A., Brandl E., Wagner M. Detection and quantification of the iap gene of Listeria monocytogenes and Listeria innocua by a new real-time quantitative PCR assay. Res. Microbiol. 2001, 152:37-46.
33. Hill V.R., Polaczyk A.L., Kahler A.M., Cromeans T.L., Hahn D., Amburgey J.E. Comparison of hollow-fiber ultrafiltration to the USEPA VIRADEL technique and USEPA method 1623. J. Environ. Qual. 2009, 38:822-825.
34. Hoorfar J., Ahrens P., Radstrom P. Automated 5' nuclease PCR assay for identification of Salmonella enterica. J. Clin. Microbiol. 2000, 38:3429-3435.
35. Hossain S.M.Z., Ozimok C., Sicard C., Aguirre S.D., Ali M.M., Yingfu L., Brennan J.D. Multiplexed paper test strip for quantitative bacterial detection. Anal. Bioanal. Chem. 2012, 403:1567-1576.
36. Huff K., Aroonnual A., Littlejohn A.E.F., Rajwa B., Bae E., Banada P.P., Patsekin V., Hirleman E.D., Robinson J.P., Richards G.P., Bhunia A.K. Light-scattering sensor for real-time identification of Vibrio parahaemolyticus, Vibrio vulnificus and Vibrio cholerae colonies on solid agar plate. Microb. Biotechnol. 2012, 5:607-620.
37. Josefsen M.H., Lubeck P.S., Hansen F., Hoorfar J. Towards an international standard for PCR-based detection of foodborne thermotolerant campylobacters: interaction of enrichment media and pre-PCR treatment on carcass rinse samples. J. Microbiol. Methods 2004, 58:39-48.
38. Killgore G.E., Holloway B., Tenover F.C. A 5' nuclease PCR (TaqMan) high-throughput assay for detection of the mecA gene in staphylococci. J. Clin. Microbiol. 2000, 38:2516-2519.
39. Kim H., Bhunia A.K. SEL, a selective enrichment broth for simultaneous growth of Salmonella enterica, Escherichia coli O157:H7, and Listeria monocytogenes. Appl. Environ. Microbiol. 2008, 74:4853-4866.
40. Koo O.K., Liu Y., Shuaib S., Bhattacharya S., Ladisch M.R., Bashir R., Bhunia A.K. Targeted capture of pathogenic bacteria using a mammalian cell receptor coupled with dielectrophoresis on a biochip. Anal. Chem. 2009, 81:3094-3101.
41. Kuehn B.M. Salmonella cases traced to egg producers. JAMA, J. Am. Med. Assoc. 2010, 304:1316.
42. Lathrop A.A., Banada P.P., Bhunia A.K. Differential expression of InlB and ActA in Listeria monocytogenes in selective and nonselective enrichment broths. J. Appl. Microbiol. 2008, 104:627-639.
43. Lee J.-L., Levin R.E. Detection of 5CFU/g of Escherichia coli O157:H7 on lettuce using activated charcoal and real-time PCR without enrichment. Food Microbiol. 2011, 28:562-567.
44. Li X., Ximenes E., Amalaradjou M.A.R., Vibbert H.B., Foster K., Jones J., Liu X., Bhunia A.K., Ladisch M.R. Rapid sample processing for detection of food-borne pathogens via cross-flow microfiltration. Appl. Environ. Microbiol. 2013, 79:7048-7054.
45. Li Y., Yan X., Feng X., Wang J., Du W., Wang Y., Chen P., Xiong L., Liu B.-F. Agarose-based microfluidic device for point-of-care concentration and detection of pathogen. Anal. Chem. 2014, 86:10653-10659.
46. Lindqvist R. Preparation of PCR samples from food by a rapid and simple centrifugation technique evaluated by detection of Escherichia coli O157:H7. Int. J. Food Microbiol. 1997, 37:73-82.
47. Lofstrom C., Knutsson R., Axelsson C.E., Radstrom P. Rapid and specific detection of Salmonella spp. in animal feed samples by PCR after culture enrichment. Appl. Environ. Microbiol. 2004, 70:69-75.
48. Magana S., Schlemmer S.M., Davidson G.R., Ryser E.T., Lim D.V. Laboratory and pilot-scale dead-end ultrafiltration concentration of sanitizer-free and chlorinated lettuce wash water for improved detection of Escherichia coli O157:H7. J. Food Prot. 2014, 77:1260-1268.
49. Maki D.G. Coming to grips with foodborne infection with peanut butter, peppers, and nationwide Salmonella Outbreaks. New Engl. J. Med. 2009, 360:949-953.
50. Mondani L., Roupioz Y., Delannoy S., Fach P., Livache T. Simultaneous enrichment and optical detection of low levels of stressed Escherichia coli O157:H7 in food matrices. J. Appl. Microbiol. 2014, 117:537-546.
51. Mothershed E.A., Cassiday P.K., Pierson K., Mayer L.W., Popovic T. Development of a real-time fluorescence PCR assay for rapid detection of the diphtheria toxin gene. J. Clin. Microbiol. 2002, 40:4713-4719.
52. Mukhopadhyay S., Tomasula P.M., Luchansky J.B., Porto-Fett A., Call J.E. Removal of Salmonella Enteritidis from commercial unpasteurized liquid egg white using pilot scale cross flow tangential microfiltration. Int. J. Food Microbiol. 2010, 142:309-317.
53. Murakami T. Filter-based pathogen enrichment technology for detection of multiple viable foodborne pathogens in 1day. J. Food Prot. 2012, 75:1603-1610.
54. Najafi R., Mukherjee S., Hudson J., Sharma A., Banerjee P. Development of a rapid capture-cum-detection method for Escherichia coli O157 from apple juice comprising nano-immunomagnetic separation in tandem with surface enhanced Raman scattering. Int. J. Food Microbiol. 2014, 189:89-97.
55. Olaimat A.N., Holley R.A. Factors influencing the microbial safety of fresh produce: a review. Food Microbiol. 2012, 32:1-19.
56. Payne M.J., Campbell S., Patchett R.A., Kroll R.G. The use of immobilized lectins in the separation of Staphylococcus aureus, Escherichia coli, Listeria and Salmonella spp. from pure cultures and foods. J. Appl. Microbiol. 1992, 73:41-52.
57. Sapsford K.E., Rasooly A., Taitt C.R., Ligler F.S. Detection of Campylobacter and Shigella species in food samples using an array biosensor. Anal. Chem. 2004, 76:433-440.
58. Scallan E., Hoekstra R.M., Angulo F.J., Tauxe R.V., Widdowson M.A., Roy S.L., Jones J.L., Griffin P.M. Foodborne illness acquired in the United States-major pathogens. Emerg. Infect. Dis. 2011, 17:7-15.
59. Scharff R. Economic burden from health losses due to foodborne illness in the United States. J. Food Prot. 2012, 75:123-131.
60. Scheutz F., Møller Nielsen E., Frimodt-Møller J., Boisen N., M.S, Tozzoli R., Nataro J., Caprioli A. Characteristics of the enteroaggregative Shiga toxin/verotoxinproducing Escherichia coli O104:H4 strain causing the outbreak of haemolytic uraemic syndrome in Germany, May to June 2011. Euro Surveill. 2011, 6:19889.
61. Sharma H., Mutharasan R. Review of biosensors for foodborne pathogens and toxins. Sensors Actuators B Chem. 2013, 183:535-549.
62. Singh A.K., Bettasso A.M., Bae E., Rajwa B., Dundar M.M., Forster M.D., Liu L., Barrett B., Lovchik J., Robinson J.P., Hirleman E.D., Bhunia A.K. Laser optical sensor, a label-free on-plate Salmonella enterica colony detection tool. mBio 2014, 5:e01019.
63. Singh A.K., Sun X., Bai X., Kim H., Abdalhaseib M.U., Bae E., Bhunia A.K. Label-free, non-invasive light scattering sensor for rapid screening of Bacillus colonies. J. Microbiol. Methods 2015, 109:56-66.
64. Stevens K.A., Jaykus L.A. Bacterial separation and concentration from complex sample matrices: a review. Crit. Rev. Microbiol. 2004, 30:7-24.
65. Tang Y., Kim H., Singh A.K., Aroonnual A., Bae E., Rajwa B., Fratamico P.M., Bhunia A.K. Light scattering sensor for direct identification of colonies of Escherichia coli serogroups O26, O45, O103, O111, O121, O145 and O157. PLoS One 2014, 9. e105272.
66. USDA-FSIS Microbiology Laboratory Guidebook (Date Accessed June 1, 2015). http://www.fsis.usda.gov/wps/portal/fsis/topics/science/laboratories-and-procedures/guidebooks-and-methods/microbiology-laboratory-guidebook/microbiology-laboratory-guidebook.
67. Valadez A., Lana C., Tu S.-I., Morgan M., Bhunia A. Evanescent wave fiber optic biosensor for Salmonella detection in food. Sensors 2009, 9:5810-5824.
68. Varshney M., Li Y. Interdigitated array microelectrode based impedance biosensor coupled with magnetic nanoparticle-antibody conjugates for detection of Escherichia coli O157:H7 in food samples. Biosens. Bioelectron. 2007, 22:2408-2414.
69. Velusamy V., Arshak K., Korostynska O., Oliwa K., Adley C. An overview of foodborne pathogen detection: in the perspective of biosensors. Biotechnol. Adv. 2010, 28:232-254.
70. Walsh K.A., Bennett S.D., Mahovic M., Gould L.H. Outbreaks associated with cantaloupe, watermelon, and honeydew in the United States, 1973-2011. Foodborne Pathog. Dis. 2014, 11:945-952.
71. Wilson I.G. Inhibition and facilitation of nucleic acid amplification. Appl. Environ. Microbiol. 1997, 63:3741-3751.
72. Wolffs P.F.G., Glencross K., Thibaudeau R., Griffiths M.W. Direct quantitation and detection of salmonellae in biological samples without enrichment, using two-step filtration and real-time PCR. Appl. Environ. Microbiol. 2006, 72:3896-3900.
73. Zhou P., Hussain S.K., Liles M.R., Arias C.R., Backert S., Kieninger J., Oyarzabal O.A. A simplified and cost-effective enrichment protocol for the isolation of Campylobacter spp. from retail broiler meat without microaerobic incubation. BMC Microbiol. 2011, 11:175.