Skip to main content

Accelerated Sample Preparation for Fast Salmonella Detection in Poultry Products

Part of the Methods in Molecular Biology book series (MIMB,volume 1918)

Abstract

Salmonella is the most burdensome foodborne pathogen in the USA and a major causal agent of foodborne outbreaks. Detection of a pathogen such as Salmonella can be achieved within a few hours using commercially available rapid methods, but the sample preparation is time consuming and may require multiple days. We have developed and successfully tested an accelerated sample preparation method based on microfiltration, in some cases preceded by a short enrichment step, for the rapid detection of selected pathogens. The time-frame of the overall process, from sample preparation (i.e., food rinse or homogenate preparation, microbial enrichment, and filtration steps) to detection is 8 h or less. While microfiltration has been practiced for 70 years, the complex interactions between food substances and filter membrane surfaces have shown that food pretreatment methods need to be developed on a case by case basis for the recovery of bacteria from food homogenates and/or rinses. We have also demonstrated that addition of protease to treat homogenates of different poultry products prior to microfiltration avoids the rapid decrease in flux that otherwise occurs during microfiltration. This protease treatment minimizes filter clogging, so that the microbial concentration, recovery and detection of 1 to 10 CFU/g of Salmonella in poultry products is possible in less than 8 h.

Key words

  • Sample preparation
  • Salmonella detection
  • Poultry products
  • Microfiltration
  • Hollow fiber membranes
  • Protease

This is a preview of subscription content, access via your institution.

Buying options

Protocol
USD   49.95
Price excludes VAT (USA)
  • DOI: 10.1007/978-1-4939-9000-9_1
  • Chapter length: 18 pages
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
eBook
USD   149.00
Price excludes VAT (USA)
  • ISBN: 978-1-4939-9000-9
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
Hardcover Book
USD   199.99
Price excludes VAT (USA)
Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Springer Nature is developing a new tool to find and evaluate Protocols. Learn more

References

  1. Brem-Stecher B, Young C, Jaykus LA, Tortorello ML (2009) Sample preparation: the forgotten beginning. J Food Prot 72:1774–1789

    Google Scholar 

  2. Dwivedi HP, Jaykus LA (2011) Detection of pathogens in foods: the current state-of the- art and future directions. Crit Rev Microbiol 37(1):40–63

    CAS  PubMed  Google Scholar 

  3. Li X, Ximenes E, Amalaradjou MAR, Vibbert HB, Foster K, Jones J, Liu X, Bhunia AK, Ladisch MR (2013) Rapid sample processing for detection of food-borne pathogens via cross-flow microfiltration. Appl Environ Microbiol 79:7048–7054

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Cho I, Ku S (2017) Current technical approaches for the early detection of foodborne pathogens: challenges and opportunities. Int J Mol Sci 18(10):2078

    PubMed Central  Google Scholar 

  5. Ladisch M.R., Ximenes E.A (2017) Methods and systems useful for foodborne pathogen detection. Patent # US US9651551 B2. Official Gazette of the United States Patent and Trademark Office Patents, Volume:1438 Issue:3 (Published on May 16, 2017)

    Google Scholar 

  6. Vibbert HB, Ku S, Li X, Liu X, Kreke T, Deering A, Gehring A, Ximenes E, Ladisch M (2015) Accelerating sample preparation through enzyme-assisted microfiltration of Salmonella in chicken extract. Biotechnol Prog 31(6):1551–1562

    CAS  PubMed  Google Scholar 

  7. Ku S, Ximenes E, Kreke T, Foster K, Deering AJ, Ladisch MR (2016) Microfiltration of enzyme treated egg whites for accelerated detection of viable Salmonella. Biotechnol Prog 32(6):1464–1471

    CAS  PubMed  Google Scholar 

  8. Ku S, Kreke T, Ximenes E, Foster K, Liu X, Gilpin CJ, Ladisch MR (2017) Protein particulate retention and microorganism recovery for rapid detection of Salmonella. Biotechnol Prog 33(3):687–695

    CAS  PubMed  Google Scholar 

  9. Bell RL, Jarvis KG, Ottesen AR, Mcfarland MA, Brown EW (2016) Recent and emerging innovations in Salmonella detection: a food and environmental perspective. Microb Biotechnol 2016(9):279–292

    Google Scholar 

  10. Heyndrickx M, Vandekerchove D, Herman L, Rolliers I, Grijspeerdt K, De Zutter L (2002) Routes for Salmonella contamination of poultry meat: epidemiological study from hatchery to slaughterhouse. Epidemiol Infect 129:253–265

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson M-A, Roy S et al (2011) Foodborne illness acquired in the United States–major pathogens. Emerg InfectDis 17:7–15

    Google Scholar 

  12. Anderson TC, Nguyen T-A, Adams JK et al (2016) Multistate outbreak of human Salmonella typhimurium infections linked to live poultry from agricultural feed stores and mail-order hatcheries, United States 2013. One Health 2:144–149

    PubMed  PubMed Central  Google Scholar 

  13. Hale CR, Scallan E, Cronquist AB, Dunn J, Smith K, Robinson T et al (2012) Estimates of enteric illness attributable to contact with animals and their environments in the United States. Clin Infect Dis 54:S472–S479

    PubMed  Google Scholar 

  14. Harris JR, Neil K, Barton Behravesh C, Sotir M, Angulo F (2010) Recent multistate outbreaks of human Salmonella infections acquired from turtles: a continuing public health challenge. Clin Infect Dis 50:554–559

    PubMed  Google Scholar 

  15. Basler C, Forshey TM, Machesky K, Erdman CM, Gomez TM, Nguyen T-A et al (2014) Notes from the field: multistate outbreak of human Salmonella infections linked to live poultry from a mail-order hatchery in Ohio—March–September 2013. MMWR Morb Mortal Wkly Rep 63:222

    PubMed  PubMed Central  Google Scholar 

  16. National association of state public health veterinarians animal contact compendium committee (2013) Compendium of measures to prevent disease associated with animals in public settings. J Am Vet Med Assoc 243:1270–1288

    Google Scholar 

  17. Barton Behravesh C, Brinson D, Hopkins BA, Gomez TM (2014) Backyard poultry flocks and salmonellosis: a recurring, yet preventable public health challenge. Clin Infect Dis 58:1432–1438

    Google Scholar 

  18. Mettee Zareki SL, Bennett SD, Hall J, Yaeger J, Lujan K, Adams-Cameron M et al (2013) US outbreak of human Salmonella infections associated with aquatic frogs, 2008–2011. Pediatrics 131:724–731

    Google Scholar 

  19. United States Department of Agriculture (2012) Poultry urban chicken ownership in four U.S. cities, U.S. Department of Agriculture, Animal and Plant Health Inspection Services, Veterinary Services, Center for Epidemiology and Animal Health, Fort Collins, CO.

    Google Scholar 

  20. Yaron S, Römling U (2014) Biofilm formation by enteric pathogens and its role in plant colonization and persistence. Microb Biotechnol 7(6):495–516

    Google Scholar 

  21. Jacques M, Aragon V, Tremblay YD (2010) Biofilm formation in bacterial pathogens of veterinary importance. Anim Health Res Rev 11:97–121

    PubMed  Google Scholar 

  22. Vogeleer P, Tremblay YDN, Mafu AA, Jacques M, Harel J (2014) Life on the outside: role of biofilms in environmental persistence of Shiga-toxin producing Escherichia coli. Front Microbiol 5(317):1–12

    Google Scholar 

  23. Flemming H-C, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633

    CAS  PubMed  Google Scholar 

  24. Ximenes E, Hoagland L, Ku S, Li X, Ladisch M (2017) Human pathogens in plant biofilms: formation, physiology, and detection. Biotechnol Bioeng 114(7):1403–1418

    CAS  PubMed  Google Scholar 

  25. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322

    CAS  PubMed  Google Scholar 

  26. Sharpe AN, Peterkin PI, Dudas I (1979) Membrane filtration of food suspensions. Appl Environ Microbiol 37:21–35

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Foley G Crossflow microfiltration. SciTopics. 27 Nov 27 2008. http://www.scitopics.com/Crossflow_Microfiltration.html

  28. Baker RW (2004) Membrane technology and applications, 2nd edn. J. Wiley, New York, NY, pp 89–155

    Google Scholar 

  29. Hill VR, Polaczyk AL, Hahn D, Narayanan J, Cromeans TL, Roberts JM, Amburgey JE (2005) Development of a rapid method for simultaneous recovery of diverse microbes in drinking water by ultrafiltration with sodium polyphosphate and surfactants. Appl Environ Microbiol 71:6878–6884

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Liu P, Hill VR, Hahn D, Johnson TB, Pan Y, Jothikumar N, Moe CL (2012) Hollow-fiber ultrafiltration for simultaneous recovery of viruses, bacteria and parasites from reclaimed water. J Microbiol Methods 88:155–161

    PubMed  Google Scholar 

  31. Morales-Morales HA, Vidal G, Olszewski J, Rock CM, Dasgupta D, Oshima KH, Smith GB (2003) Optimization of a reusable hollow-fiber ultrafilter for simultaneous concentration of enteric bacteria, protozoa, and viruses from water. Appl Environ Microbiol 69:4098–4102

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Smith CM, Hill VR (2009) Dead-end hollow-fiber ultrafiltration for recovery of diverse microbes from water. Appl Environ Microbiol 75:5284–5289

    PubMed  PubMed Central  Google Scholar 

  33. Hunter DM, Leskinen SD, Magana S, Schlemmer SH, Lim PV (2011) Dead-end ultrafiltration concentration and IMS/ATP-bioluminescence detection of Escherichia coli O157:H7 in recreational water and produce wash. J Microbiol Methods 87:338–342

    PubMed  Google Scholar 

  34. Kelly ST, Zydney AL (1997) Protein fouling during microfiltration: comparative behavior of different model proteins. Biotechnol Bioeng 55:91–100

    CAS  PubMed  Google Scholar 

  35. Mukhopadhyay S, Tomasula PM, Van Hekken DL, Luchansky JB, Call JE, Porto-Fett AC (2009) Effectiveness of cross-flow microfiltration for removal of microorganisms associated with unpasteurized liquid egg white from process plant. J Food Sci 74:319–327

    Google Scholar 

  36. United States Department of Agriculture. Food Safety and Inspection Service. Microbiology Laboratory Guidebook. Available at: http://www.fsis.usda.gov/wps/portal/fsis/topics/science/laboratories-and-procedures/guidebooks-and-methods/microbiology-laboratory-guidebook/microbiology-laboratory-guidebook. Accessed Feb 26 2018

  37. U.S. Food and Drug Administration. BAM: Salmonella. Available at: https://www.fsis.usda.gov/wps/wcm/connect/700c05fe-06a2-492a-a6e1-3357f7701f52/MLG-4.pdf?MOD=AJPERES. Accessed Mar 19 2018

  38. International Organization for Standardization. ISO-6579 (2002) Microbiology-general guidance on methods for the detection of Salmonella, 4th edn. International Organization for Standardization, Geneva: Switzerland

    Google Scholar 

  39. Gole VC, Chousalkar KK, Roberts JR, Sexton M, May D, Tan J, Kiermeier A (2014) Effect of egg washing and correlation between eggshell characteristics and egg penetration by various Salmonella typhimurium strains. PLoS One 9:e90987

    PubMed  PubMed Central  Google Scholar 

  40. Brewster J (2009) Large-volume filtration for recovery and concentration of Escherichia coli O157:h7 from ground beef. J Rapid Meth Aut Mic 17:242–256

    Google Scholar 

  41. Mukhopadhyay S, Tomasula PM, Luchansky JB, Porto-Fett A, Call JE (2010) Removal of Salmonella Enteritidis from commercial unpasteurized liquid egg white using pilot scale cross flow tangential microfiltration. Int J Food Microbiol 142:309–317

    PubMed  Google Scholar 

  42. Blanpain-Avet P, Faille C, Bénézech T (2009) Cleaning kinetics and related mechanisms of Bacillus cereus spore removal during an alkaline cleaning of a tubular ceramic microfiltration membrane. Desalin Water Treat 5:235–251

    CAS  Google Scholar 

  43. Hein I, Flekna G, Krassnig M, Wagner M (2006) Real-time PCR for the detection of Salmonella spp. in food: an alternative approach to a conventional PCR system suggested by the FOOD-PCR project. J Microbiol Methods 66:538–547

    CAS  PubMed  Google Scholar 

  44. Puolanne E, Kivikari R (2000) Determination of the buffering capacity of postrigor meat. Meat Sci 56:7–13

    CAS  PubMed  Google Scholar 

  45. Dickson J, Manke T, Wesley I, Baetz A (1996) Biphasic culture of Arcobacter spp. Lett Appl Microbiol 22:195–198

    CAS  PubMed  Google Scholar 

  46. Malorny B, Hoorfar J, Bunge C, Helmuth R (2003) Multicenter validation of the analytical accuracy of Salmonella PCR: towards an international standard. Appl Environ Microbiol 69:290–296

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The material in this work was supported by the FDA Food Safety Challenge Prize and a cooperative agreement with the Agriculture Research Service of the US Department of Agriculture project (OSQR 935-42000-049-00D), the Center for Food Safety Engineering at Purdue University, USDA Hatch project 10677, and the Department of Agricultural and Biological Engineering at Purdue University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael R. Ladisch .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and Permissions

Copyright information

© 2019 Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Verify currency and authenticity via CrossMark

Cite this protocol

Ximenes, E., Ku, S., Hoagland, L., Ladisch, M.R. (2019). Accelerated Sample Preparation for Fast Salmonella Detection in Poultry Products. In: Bridier, A. (eds) Foodborne Bacterial Pathogens. Methods in Molecular Biology, vol 1918. Humana, New York, NY. https://doi.org/10.1007/978-1-4939-9000-9_1

Download citation

  • DOI: https://doi.org/10.1007/978-1-4939-9000-9_1

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-4939-8999-7

  • Online ISBN: 978-1-4939-9000-9

  • eBook Packages: Springer Protocols