Estimation of Listeria monocytogenes transfer coefficients and efficacy of bacterial removal through cleaning and sanitation

https://doi.org/10.1016/j.ijfoodmicro.2012.05.019Get rights and content

Abstract

Listeria monocytogenes is readily found in the environment of retail deli establishments and can occasionally contaminate food handled in these establishments. Here we synthesize the available scientific evidence to derive probability distributions and mathematical models of bacterial transfers between environmental surfaces and foods, including those during slicing of food, and of bacterial removal during cleaning and sanitizing (models available at www.foodrisk.org).

Transfer coefficients varied considerably by surface type, and after log10 transformation were best described by normal distributions with means ranging from − 0.29 to − 4.96 and standard deviations that ranged from 0.07 to 1.39. ‘Transfer coefficients’ during slicing were best described by a truncated logistic distribution with location 0.07 and scale 0.03. In the absence of protein residues, mean log inactivation indicated a greater than 5 log10 reduction for sanitization with hypochlorite (mean: 6.5 log10; 95% confidence interval (CI): 5.0–8.1 log10) and quaternary ammonium compounds (mean: 5.5 log10; 95% CI: 3.6–7.3 log10), but in the presence of protein residues efficacy reduced dramatically for hypochlorite (mean: 3.8 log10; 95% CI: 2.1–5.4 log10) as well as quaternary ammonium compounds (mean: 4.4log10; 95% CI: 2.5–6.4 log10).

Overall, transfer coefficients are therefore low, even though cross-contamination can be extremely efficient under certain conditions. Dozens of food items may consequently be contaminated from a single contaminated slicer blade, albeit at low concentrations. Correctly performed sanitizing efficiently reduces L. monocytogenes contamination in the environment and therefore limits cross-contamination, even though sanitization is only performed a few times per day. However, under unfavorable conditions reductions in bacterial concentration may be far below 5 log10.

The probability distributions and mathematical models derived here can be used to evaluate L. monocytogenes cross-contamination dynamics in environments where foods are handled, and to assess the potential impact of different intervention strategies.

Highlights

Listeria monocytogenes transfer coefficients (TCs) and sanitization were analyzed. ► TCs were generally low, indicating that contamination can be spread to many food items. ► Sanitizing efficacy was strongly affected by external conditions. ► Strict adherence to cleaning and sanitizing SOPs is thus crucial to assure efficacy. ► Stochastic models of transfer and sanitization were derived for risk assessments.

Introduction

Listeria monocytogenes has been estimated to cause approximately 1600 human invasive listeriosis cases in the United States each year (Scallan et al., 2011). Of these, as many as 1455 cases annually are predicted to result in hospitalization and 255 cases are expected to result in death, making L. monocytogenes one of the leading causes of death due to foodborne illness in the United States (Scallan et al., 2011). Epidemiological studies of sporadic cases, food surveys, and outbreak investigations have provided compelling evidence for contaminated ready-to-eat (RTE) foods as principal sources of listeriosis (FAO/WHO, 2004, FDA/FSIS, 2003). A risk assessment of 23 selected categories of RTE foods, published in 2003, identified deli meats as the food category with the greatest associated public health risk (FDA/FSIS, 2003). Importantly, deli meat products sliced and packaged at retail are more frequently contaminated, and with higher bacterial concentrations, compared to those sliced and packaged by the manufacturer at the processing facility (Endrikat et al., 2010, Gombas et al., 2003). Risk assessments estimate that more than 70% of those listeriosis cases attributable to deli meats are associated with deli meats sliced at retail and formulated without growth inhibitors (Endrikat et al., 2010, Pradhan et al., 2010). Cross-contamination at retail, combined with bacterial growth during storage, therefore likely represents a fundament risk factor for listeriosis. Environmental surfaces in retail operations can be frequently contaminated with L. monocytogenes (Hoelzer et al., 2011, Sauders et al., 2009). For instance, in a survey of retail operations in the state of New York, environmental contamination with L. monocytogenes was detected in 60% of the establishments (Hoelzer et al., 2011). Notably, 3% (5/183) of slicers and 4% (13/314) of other utensils in these establishments were contaminated with L. monocytogenes, emphasizing the considerable cross-contamination potential.

The factors contributing to L. monocytogenes cross-contamination at retail, however, are currently not well understood. Mathematical models of environmental cross-contamination offer a valuable alternative to observational studies in retail facilities or intervention studies in mock delis as they allow for the expeditious and cost-effective evaluation of cross-contamination risks and enable exploration of the effects of different management practices. However, data to populate such models are not readily available. Laboratory studies have analyzed bacterial transfers between solid surfaces and food, with sometimes contradictory results (see Perez-Rodriguez et al., 2008 for a review). Several factors, including the biological state of the bacterium (Midelet and Carpentier, 2002), the nature and intensity of the contact (Chen et al., 2001), the surface structure of the contamination source (Midelet and Carpentier, 2002, Silva et al., 2008), and the food type (Vorst et al., 2006) seem to impact transfer dynamics. It has been shown that a contaminated slicer blade can spread L. monocytogenes to many uncontaminated food slices, but the transfer dynamics vary considerably with the physico-chemical composition of the sliced product (Keskinen et al., 2008a, Sheen, 2008, Sheen and Hwang, 2010, Vorst et al., 2006). Cleaning and sanitation may effectively reduce bacterial contamination in the environment and therefore lower contamination of food, but the efficacy of different sanitizers in reducing L. monocytogenes contamination is highly dependent on a number of extrinsic factors related for instance to pathogen type, ambient temperature, water hardness, surface structure, or the presence of protein residues (Marriott and Gravani, 2006, New York State Department of Agriculture and Markets, 2011).

Here we synthesize the relevant peer-reviewed scientific literature to derive probability distributions that model i) transfers between various surfaces and food; ii) transfer dynamics during slicing of foods; and iii) removal of bacteria through cleaning and sanitizing. In a second step we derive mathematical models that can be used to describe these processes. The derived probability distributions and models can be incorporated into comprehensive models of L. monocytogenes cross-contamination to evaluate the public health impact of environmental contamination with L. monocytogenes in places where RTE foods are handled.

Section snippets

Materials and methods

The relevant peer-reviewed scientific literature was identified through searches in the National Center for Biotechnology Information (NCBI) PubMed database, cross references in related published manuscripts, and auxiliary data sources such as the Google search engine. Literature searches for transfer coefficients (including those specific to slicers) and for cleaning and sanitizing were performed in June 2009 and December 2010, respectively. For transfer coefficient studies (including those

Results

A total of 37 peer-reviewed studies met our inclusion criteria, and 2308 data points were extracted from these studies.

Discussion

Several food-safety related studies of bacterial transfer coefficients and cleaning and sanitization efficacy have been published in recent years. Unfortunately, the study results summarized here appear highly variable and conclusions sometimes seem contradictory. It has largely remained unclear whether this high inter-study variability reflects experimental artifacts such as experimental design differences or disparate detection and enumeration methods, or whether it reflects true biological

Conclusion

In general, transfer coefficients appear to be low, indicating the potential for wide-spread cross-contamination at low concentrations. Sanitizing can efficiently remove contamination under optimal conditions, but the true efficacy of bacterial inactivation in practice remains unclear given the large number of factors that may significantly hamper efficacy. The current probabilistic models derived here allow for the expeditious and cost-effective evaluation of different cross-contamination

Acknowledgments

This work was supported in part by appointments to the Research Participation Program at the Center for Food Safety and Applied Nutrition administered by the Oak Ridge Institute for Science and Education through an interagency agreement between the US Department of Energy and the U.S. Food and Drug Administration. Support for this work was also provided by Virginia Tech in collaboration with the U.S. Department of Agriculture, Food Safety and Inspection Service (FSIS contract # AG-3A94-P-08-0166

References (74)

  • D.E. Gombas et al.

    Survey of Listeria monocytogenes in ready-to-eat foods

    Journal of Food Protection

    (2003)
  • K. Hoelzer et al.

    Prevalence, distribution, and diversity of Listeria monocytogenes in retail environments, focusing on small establishments and establishments with a history of failed inspections

    Journal of Food Protection

    (2011)
  • R. Ivanek et al.

    Mathematical model of Listeria monocytogenes cross-contamination in a fish processing plant

    Journal of Food Protection

    (2004)
  • S. Keeratipibul et al.

    Risk assessment of Listeria spp. contamination in the production line of ready-to-eat chicken meat products

    Journal of Food Protection

    (2008)
  • L.A. Keskinen et al.

    Impact of bacterial stress and biofilm-forming ability on transfer of surface-dried Listeria monocytogenes during slicing of delicatessen meats

    International Journal of Food Microbiology

    (2008)
  • L.A. Keskinen et al.

    Transfer of surface-dried Listeria monocytogenes from stainless steel knife blades to roast turkey breast

    Journal of Food Protection

    (2008)
  • J. Knowles et al.

    Efficacy of chitosan, carvacrol, and a hydrogen peroxide-based biocide against foodborne microorganisms in suspension and adhered to stainless steel

    Journal of Food Protection

    (2001)
  • H.D. Kusumaningrum et al.

    Survival of foodborne pathogens on stainless steel surfaces and cross-contamination to foods

    International Journal of Food Microbiology

    (2003)
  • H.D. Kusumaningrum et al.

    A quantitative analysis of cross-contamination of Salmonella and Campylobacter spp. via domestic kitchen surfaces

    Journal of Food Protection

    (2004)
  • C. Liu et al.

    Effects of electrolyzed oxidizing water on reducing Listeria monocytogenes contamination on seafood processing surfaces

    International Journal of Food Microbiology

    (2006)
  • J.A. Lopes

    Susceptibility of antibiotic-resistant and antibiotic-sensitive foodborne pathogens to acid anionic sanitizers

    Journal of Food Protection

    (1998)
  • T. Meylheuc et al.

    Adsorption of a biosurfactant on surfaces to enhance the disinfection of surfaces contaminated with Listeria monocytogenes

    International Journal of Food Microbiology

    (2006)
  • R. Montville et al.

    Glove barriers to bacterial cross-contamination between hands to food

    Journal of Food Protection

    (2001)
  • C.M. Moore et al.

    Transfer of Salmonella and Campylobacter from stainless steel to romaine lettuce

    Journal of Food Protection

    (2003)
  • M.J. Nauta

    “Campylobacter transfer from naturally contaminated chicken thighs to cutting boards is inversely related to initial load,” a comment on: Journal of Food Protection 72: 1836–1840 (2009)

    Journal of Food Protection

    (2010)
  • F. Perez-Rodriguez et al.

    Modelling transfer of Escherichia coli O157:H7 and Staphylococcus aureus during slicing of a cooked meat product

    Meat Science

    (2007)
  • F. Perez-Rodriguez et al.

    Understanding and modelling bacterial transfer to foods: a review

    Trends in Food Science & Technology

    (2008)
  • R. Pouillot et al.

    Evaluating variability and uncertainty separately in microbial quantitative risk assessment using two R packages

    International Journal of Food Microbiology

    (2010)
  • A.K. Pradhan et al.

    Quantitative risk assessment of listeriosis-associated deaths due to Listeria monocytogenes contamination of deli meats originating from manufacture and retail

    Journal of Food Protection

    (2010)
  • A. Rodriguez et al.

    Evaluation of the transfer of Listeria monocytogenes from stainless steel and high-density polyethylene to Bologna and American cheese

    Journal of Food Protection

    (2007)
  • A. Rodriguez et al.

    Effects of inoculation level, material hydration, and stainless steel surface roughness on the transfer of Listeria monocytogenes from inoculated bologna to stainless steel and high-density polyethylene

    Journal of Food Protection

    (2007)
  • A. Rodriguez et al.

    Effect of biofilm dryness on the transfer of Listeria monocytogenes biofilms grown on stainless steel to bologna and hard salami

    Journal of Food Protection

    (2007)
  • J.L. Sagripanti et al.

    Comparative sensitivity of 13 species of pathogenic bacteria to seven chemical germicides

    American Journal of Infection Control

    (1997)
  • B.D. Sauders et al.

    Prevalence and molecular diversity of Listeria monocytogenes in retail establishments

    Journal of Food Protection

    (2009)
  • D.W. Schaffner et al.

    Management of risk of microbial cross-contamination from uncooked frozen hamburgers by alcohol-based hand sanitizer

    Journal of Food Protection

    (2007)
  • S. Sheen et al.

    Mathematical modeling the cross-contamination of Escherichia coli O157:H7 on the surface of ready-to-eat meat product while slicing

    Food Microbiology

    (2010)
  • S. Silva et al.

    Adhesion to and viability of Listeria monocytogenes on food contact surfaces

    Journal of Food Protection

    (2008)
  • Cited by (0)

    View full text