Retail Deli Slicer Cleaning Frequency — Six Selected Sites, United States, 2012

Listeria monocytogenes (Listeria) causes the third highest number of foodborne illness deaths (an estimated 255) in the United States annually, after nontyphoidal Salmonella species and Toxoplasma gondii (1). Deli meats are a major source of listeriosis illnesses (2,3), and meats sliced and packaged at retail delis are the major source of listeriosis illnesses attributed to deli meat (4). Mechanical slicers pose cross-contamination risks in delis and are an important source of Listeria cross-contamination (5,6). Reducing Listeria contamination of sliced meats in delis will likely reduce Listeria illnesses and outbreaks (6). Good slicer cleaning practices can reduce this foodborne illness risk (7). CDC’s Environmental Health Specialists Network (EHS-Net) studied how often retail deli slicers were fully cleaned (disassembled, cleaned, and sanitized) at the Food and Drug Administration (FDA) Food Code–specified minimum frequency of every 4 hours and examined deli and staff characteristics related to slicer cleaning frequency (8). Interviews with staff members in 298 randomly-selected delis in six EHS-Net sites showed that approximately half of delis fully cleaned their slicers less often than FDA’s specified minimum frequency. Chain-owned delis and delis with more customers, more slicers, required manager food safety training, food safety–knowledgeable workers, written slicer-cleaning policies, and food safety–certified managers fully cleaned their slicers more frequently than did other types of delis, according to deli managers or workers. States and localities should require deli manager training and certification, as specified in the FDA Food Code. They should also consider encouraging or requiring delis to have written slicer-cleaning policies. Retail food industry leaders can also implement these prevention efforts to reduce risk in their establishments. Because independent and smaller delis had lower frequencies of slicer cleaning, prevention efforts should focus on these types of delis.

The FDA Food Code is a model food code offered for adoption by state and local governmental jurisdictions that regulate retail food safety (i.e., states and localities). It contains science-based guidance to improve food safety in retail food service establishments. Although not all states and localities have adopted the latest version of the Food Code (2013), FDA and CDC strongly encourage its adoption at all levels of government.* The FDA Food Code states that food contact surfaces, including slicers, should be cleaned and sanitized at least every 4 hours (4–602.11[C]) (8), and that food contact surfaces should be disassembled before cleaning and sanitizing (4–202.11[A][5]) (8). U.S. Department of Agriculture (USDA) guidance also recommends slicer disassembly before cleaning and sanitizing (6). Knowledge about retail delis’ cleaning practices is critical to developing effective interventions. EHS-Net, a collaborative program of CDC, FDA, USDA, and six EHS-Net–funded state and local health departments,^† assessed how often deli slicers were fully cleaned (disassembled, cleaned, and sanitized) at the FDA–specified minimum frequency of every 4 hours. EHS-Net also assessed deli and staff characteristics related to slicer cleaning frequency.

Within each EHS-Net site, data collectors chose a convenient geographic area, based on reasonable travel distance, in which to survey delis by telephone to determine study eligibility and request study participation. A software program was then used to select a random sample of delis within in each of the site geographic areas. Delis eligible for the study had at least one slicer, prepared or served ready-to-eat foods (with a delay between purchase and consumption), and had staff members who could be interviewed in English. Data collectors assessed approximately 50 delis in each site. Data were collected during January–September 2012.

Data collectors interviewed deli managers about their characteristics, their deli’s characteristics; and how often slicers were fully cleaned (“On average, how many times are food slicers fully cleaned [disassembled, cleaned, and sanitized] during a shift?”). Deli managers also completed a written, eight-item food safety knowledge survey. Data collectors interviewed food workers, away from the manager, about their characteristics and food safety knowledge, and how often each slicer was fully cleaned (“How often do you break down, clean, then sanitize this slicer?”). Simple and multiple logistic regression models were used to examine associations between deli, manager, and worker characteristics and slicer-cleaning frequencies. The cut-off for variable inclusion in the multiple regression models was p≤0.10.

Among 691 managers of eligible delis who were contacted, 298 (43%) agreed to be interviewed. In 294 (98.7%) participating delis, data collectors were also able to interview a worker. The majority of delis were chains (55.0%) and had 1–2 slicers (56.8%) (Table 1).

Half of managers (49.5%) said that slicers were fully cleaned at least every 4 hours (Table 1). The remaining managers said that slicers were fully cleaned less frequently. Workers reported that 63.0% (393 of 624) of slicers were fully cleaned at least every 4 hours. Deli-level aggregation of these worker-reported data indicated that in 45.8% of delis, all slicers were fully cleaned at least every 4 hours (Table 1). In the remaining delis, at least one slicer was fully cleaned less frequently. Managers and workers agreed on cleaning frequency in 79.0% of delis (215 of 279, r = 0.587, p<0.001).

Simple regression models showed that the characteristics of deli chain ownership, a higher average number of workers per shift, more shifts per day, more customers served on the busiest day, more slicers, more chubs (plastic tubes of meat) sold daily, deli-required manager food safety training, a written policy on slicer cleaning, manager certification (current or ever), and manager and worker food safety knowledge were significantly associated with both managers and workers indicating that their slicers were fully cleaned at least every 4 hours (Table 2). Worker rating of deli slicers as easy to clean was significantly associated with managers indicating that slicers were fully cleaned at least every 4 hours. Deli-required manager food safety certification and more worker experience in the deli were significantly associated with workers indicating that slicers were fully cleaned at least every 4 hours.

A multiple regression model showed that deli chain ownership, more customers served on the busiest day, and worker food safety knowledge were significantly associated with managers indicating that slicers were fully cleaned at least every 4 hours. A second multiple regression model showed that deli chain ownership, more customers served on the busiest day, more slicers, more chubs sold daily, deli-required manager food safety training, and more worker experience in the deli were significantly associated with workers indicating that slicers were fully cleaned at least every 4 hours. (Table 3).

Acknowledgments

Participating deli managers and workers; EHS-Net site staff members; Food and Drug Administration (FDA), U.S. Department of Agriculture; Brenda Le, Carol Selman, CDC; Denita Williams, FDA.

Corresponding author: Laura G. Brown, lrgreen@cdc.gov, 770-488-4332.

¹Division of Emergency and Environmental Health Services, National Center for Environmental Health, CDC,²Tennessee Department of Health, ³New York City Department of Health and Mental Hygiene, ⁴New York State Department of Health, ⁵Minnesota Department of Health; ⁶California Department of Public Health.

References

1. Scallan E, Hoekstra RM, Angulo FJ, et al. Foodborne illness acquired in the United States—major pathogens. Emerg Infect Dis 2011;17:7–15. CrossRefexternal icon PubMedexternal icon
2. Batz MB, Hoffmann S, Morris JG . Ranking the disease burden of 14 pathogens in food sources in the United States using attribution data from outbreak investigations and expert elicitation. J Food Prot 2012;75:1278–91. CrossRefexternal icon PubMedexternal icon
3. Cartwright EJ, Jackson KA, Johnson SD, Graves LM, Silk BJ, Mahon BE. Listeriosis outbreaks and associated food vehicles, United States, 1998–2008. Emerg Infect Dis 2013;19:1–9. CrossRefexternal icon PubMedexternal icon
4. US Department of Agriculture. FSIS comparative risk assessment for Listeria monocytogenes in ready-to-eat meats and poultry deli meats. Washington, DC: US Department of Agriculture; 2010. http://www.fsis.usda.gov/wps/wcm/connect/c2ac97d0-399e-4c4a-a2bc-d338c2e201b3/Comparative_RA_Lm_Report_May2010.pdf?MOD=AJPERESpdf iconexternal icon
5. US Department of Agriculture. Interagency risk assessment: Listeria monocytogenes in retail delicatessens. Washington, DC: US Department of Agriculture; 2013. http://www.fsis.usda.gov/wps/wcm/connect/c0c6dfbc-ad83-47c1-bcb8-8db6583f762b/Lm-Retail-Technical-Report.pdf?MOD=AJPERESpdf iconexternal icon
6. US Department of Agriculture. FSIS best practices guidance for controlling Listeria monocytogenes (Lm) in retail delicatessens. Washington, DC: US Department of Agriculture; 2015. http://www.fsis.usda.gov/wps/wcm/connect/29d51258-0651-469b-99b8-e986baee8a54/Controlling-LM-Delicatessens.pdf?MOD=AJPERESpdf iconexternal icon
7. Hoelzer K, Pouillot R, Gallagher D, Silverman MB, Kause J, Dennis S. Estimation of Listeria monocytogenes transfer coefficients and efficacy of bacterial removal through cleaning and sanitation. Int J Food Microbiol 2012;157:267–77. CrossRefexternal icon PubMedexternal icon
8. Food and Drug Administration. Food and Drug Administration Food Code. Chapter 4. equipment, utensils, and linens. Silver Springs, MD: US Department of Health and Human Services, Food and Drug Administration; 2013. http://www.fda.gov/downloads/Food/GuidanceRegulation/RetailFoodProtection/FoodCode/UCM374510.pdfpdf iconexternal icon
9. Bogard AK, Fuller CC, Radke V, Selman CA, Smith KE. Ground beef handling and cooking practices in restaurants in eight States. J Food Prot 2013;76:2132–40. CrossRefexternal icon PubMedexternal icon
10. Brown LG. EHS-Net restaurant food safety studies: what have we learned? J Environ Health 2013;75:44–5. PubMedexternal icon

TABLE 1. Reported slicer cleaning frequency, and deli, manager, and worker characteristics, obtained from manager interviews and surveys, and worker interviews*— six EHS-Net sites,^† 2012

Abbreviation: EHS-Net = Environmental Health Specialists Network.
* Numbers vary because of missing data.
^† California, Minnesota, New York, New York City, Rhode Island, and Tennessee.
^§ Disassembled, cleaned, and sanitized.
^¶ Certification defined as having taken and passed a food safety test and been issued a certificate.
** Somewhat easy, neither easy nor difficult to clean, somewhat difficult, or difficult.

TABLE 2. Simple logistic regression models of deli, manager, and worker characteristics associated with managers and workers reporting that slicers in their delis are fully cleaned* at the FDA–specified frequency (at least every 4 hours) — six EHS-Net Sites,^† 2012

Abbreviations: CI = confidence interval; EHS-Net = Environmental Health Specialists Network; FDA = Food and Drug Administration; OR = odds ratio.
* Disassembled, cleaned, and sanitized.
^† California, Minnesota, New York, New York City, Rhode Island, and Tennessee.
^§ The reference level is the second category listed. Thus, the odds ratio is for the first category listed compared to the second category listed.
^¶ Numbers vary because of missing data.
** P-values for the overall ORs: p = 0.001 and p<0.001 for the manager and worker models, respectively.
^†† Certification defined as having taken and passed a food safety test and been issued a certificate.
^§§ Somewhat easy, neither easy nor difficult to clean, somewhat difficult, or difficult.
^¶¶ P-values for the overall ORs: p = 0.803 and p = 0.856 for the manager and worker models, respectively.
*** P-values for the overall ORs: p = 0.441 and p = 0.445 for the manager and worker models, respectively.

TABLE 3. Multiple logistic regression models* of deli, manager, and worker characteristics associated with managers and workers indicating that in their deli, slicers are fully cleaned^† at the FDA–specified frequency (at least every four hours) — six EHS-Net sites,^§ 2012

Abbreviations: CI = confidence interval; EHS-Net = Environmental Health Specialists Network; FDA = Food and Drug Administration; OR = odds ratio.
* Manager overall model (χ² = 36.54, degrees of freedom (df) = 4, p<0.001) created using forward selection criteria of p≤0.10. Worker overall model (χ² = 54.96, df = 7, p<0.001) created using forward selection criteria of p≤0.10. When employing a forward selection procedure, all predictors of interest (i.e., deli, manager, and worker characteristics in this study) are systematically individually tested to see which is most significant within the model. Once identified, this predictor is added to the model and the remaining predictors are retested. This procedure is repeated until all remaining predictors fail to meet the entrance criteria. Each final model presented above simultaneously included all variables shown in the table. Individual inclusion steps are not presented.
^† Disassembled, cleaned, and sanitized.
^§ California, Minnesota, New York, New York City, Rhode Island, and Tennessee.
^¶ The reference level is the second category listed. Thus, the odds ratio is for the first category listed compared to the second category listed.
** P-value for the overall OR: p = 0.003.
^†† P-value for the overall OR: p = 0.006.