According to recent data from the U.S. Centers for Disease Control and Prevention (CDC), more than 60 percent of all the reported foodborne disease outbreaks in the United States are attributed to retail foodservice establishments.[1] As reported previously, failures to handle and prepare food safely in these establishments are the primary contributing factors that lead to foodborne disease outbreaks. The majority of the food safety hazards that exist in these establishments and their related probability of occurrence are well-known. According to the U.S. Food and Drug Administration (FDA) and CDC, the top five risk factors that contribute to the most foodborne disease outbreaks in foodservice establishments are:
1. Improper hot/cold holding temperatures of potentially hazardous foods
2. Improper cooking temperatures of food
3. Contaminated utensils and equipment
4. Poor personal hygiene
5. Food from unsafe sources
Scientific studies have also validated these factors, and there is continual evidence that the lack of their control leads directly to foodborne disease outbreaks from retail foodservice establishments.[2] One scientific study showed that certain local health department inspection violations (each related to the top-five risk factors) were more likely to be associated with restaurants that had actually caused foodborne disease outbreaks in Minnesota.[3] When the authors compared these violations with contributing factors of foodborne illness as defined by CDC,[4] they found that about two-thirds of the top violations observed during inspections at restaurants associated with outbreaks fell into the ‘‘contamination’’ category—for example, contamination of hands, surfaces, and food.
Why No Bare-Hand Contact?
Contamination of foods via the hands ranks highly among the contributing factors identified during outbreak investigations. In a report on the factors contributing to foodborne disease outbreaks from 1998 to 2002,[5] bare-hand contact, inadequate cleaning of processing or preparation equipment or utensils, and handling of food by an infected person or an asymptomatic carrier were among the most important factors (associated with 26%, 25%, and 22% of disease outbreaks, respectively). Foodborne pathogens with low infective doses may be present on hands in high numbers and can be easily transferred to foods, food contact, and nonfood contact surfaces, necessitating barriers to transmission.[6–8]
According to FDA, when hands are contaminated or soiled, effective hand hygiene (HH) practices may not be sufficient to prevent the transmission of transient pathogens from the hands to ready-to-eat (RTE) foods.[9] The 2017 FDA Food Code discourages bare-hand contact with RTE food and recommends the use of suitable utensils, deli tissues, single-use gloves, or dispensing equipment when handling these food items.[10] The majority of individual state food codes have adopted and enforce this rule.[11] The obvious objective in utilizing gloves in foodservice is to minimize physical, chemical, and microbiological contamination of food. Gloves can unfortunately offer a false sense of security both on the part of food workers and food safety managers when employees are not trained and glove use is not supervised properly.[12]
Improper Glove Use Increases Risk of Foodborne Disease Outbreaks
Although gloves (single-use and reusable) can be an effective tool to prevent cross-contamination of RTE foods from hands, improver glove use can actually increase this risk. In studies by the CDC Environmental Health Service (EHS-Net) and others between 2006 and 2016, around 16 percent of foodborne outbreaks implicated contaminated gloves or glove cross-contamination as a contributory cause.[13–17] A trend analysis of both gloved- and bare-hand contact, implicated as contributing factors from the time that glove rules were set into effect across the U.S. (2000–2015), shows a steady rise in percentages for both modes of cross-contamination.[18] Bare-hand contact was shown to be 15–18 percent higher (Figure 1). Taking model simulation results into consideration, a predictive cause for glove cross-contamination is quite likely on its way toward 20 percent or higher, based on the degree of variability and uncertainty presented by the data involved.[10] Trend analysis for the period from 2000 to 2015 and probably beyond indicates that current glove-use patterns, limitations, and relaxation of no-bare-hand contact rules (the “glove mandate”) due to glove failures could result in increasing numbers of foodborne illness outbreaks caused by gloves or glove cross-contamination. Affecting this would be improved glove types and management approaches designed to reduce cross-contamination risks.
The highest-risk glove/hand cross-contamination activity occurs when the same gloves are used to handle contaminated raw protein, then the employee touches food contact and nonfood contact surfaces (Figure 2), resulting in cross-contamination of food.[19] When food handlers touch raw proteins like chicken or ground beef and then touch other surfaces in the same kitchen, they can spread foodborne disease pathogens to these surfaces, where they can be “picked up” by the hands (with and without gloves) of other food handlers. Likewise, when a food handler switches tasks between handling raw and RTE foods and changes their gloves without washing their hands and forearms properly, they will contaminate the new pair of gloves because they have to touch the gloves to put them on. This can be a significant means of cross-contamination of RTE foods.[20]
In a study of 18 independent delicatessen operations, widespread microbial contamination (Escherichia coli, Staphylococcus aureus) was found on turkey, cream cheese, lettuce, and food contact surfaces.[21] A subsequent review of health inspection observations revealed that there was 1) inadequate HH, 2) no gloves used, 3) improper single-glove use, and 4) inadequate glove changes in 39 percent, 33 percent, 28 percent, and 67 percent of these delis inspected.[13] Other glove-use behaviors have been identified that cause cross-contamination when gloves are worn for long periods of food prep and not changed when punctured or contaminated.[21–23] Additionally, pathogens can be found to adhere better to the surface of gloves worn by food employees when gloves fit poorly or are not changed regularly.[24–28]
The use of gloves does not reduce the need to ensure proper handwashing before and after glove use. Because hands, like other surfaces, can become coated with oils, grease, and fats, for example, they should be both cleaned and sanitized, just as a food contact surface is cleaned and sanitized. This is especially important during use of foodservice gloves. The effective use of gloves depends on selection of the right glove type and maintenance of the glove barrier integrity. Undetected glove microperforations are a frequent occurrence. Microorganisms penetrate gloves via the microperforations under conditions of normal use. Puncture occurrence is directly related to duration of wearing and puncture hazards of procedures. With the interior of gloves presenting a warm, moist environment for microbial growth,[29] it is easy to understand why glove leaks would double cross-contamination risk. Handwashing is an important first step before every glove use, but preventing glove leaks is critical to ensure the final barrier between hands and foods is maintained because even with a prior handwash, interior glove counts of bacteria can be more than a million organisms.[30]
A glove puncture has been described as a “liquid bridge” of microbial contamination that can flow to food contact surfaces and foods.[31,32] Studies have shown that thousands of Staphylococcus bacteria can pass through a single glove hole during a 20-minute period, even though the hands were scrubbed prior to gloving.[9] Likewise, excess moisture buildup can release microbial contamination present in the difficult-to-clean fingernail regions that can then be spread all over the hand within the glove.[12,33–35] Leaks don’t just go in one direction out of the glove; they can also lead to permeation of microbial species, food debris, and chemical residues into the glove interior, leading to an increase in microbial load and chemicals that can then be released onto food and food contact surfaces.[36,37] This emphasizes the need to wash hands when they become contaminated with these soils, sometimes both before and after glove use.[12,38,39] Facility sanitizer chemicals, alcohol-based hand sanitizers (some but not all), or extreme temperature exposure can weaken glove material integrity[36,39,40] and thus, under conditions of use, should be monitored as part of the food safety management systems (FSMSs) outlined below.
Importance of FSMSs
The best means to prevent cross-contamination of foods is to ensure that all food contact surfaces are deep-cleaned and sanitized before food preparation, raw animal food prep is separated from RTE food prep, food handlers wash and sanitize their hands before glove use and do not handle RTE foods with bare hands, and the establishment has a monitoring and corrective action management system based on process Hazard Analysis and Critical Control Points (HACCP) principles to achieve active managerial control of cross-contamination.[41–43]
A FSMS to manage single-use gloves (a glove-use management system) employed along with handwashing can be an effective means to decrease the transfer of foodborne pathogens from the hands to food contact and nonfood contact surfaces and to food.[43]
A glove-use management system can be developed to include:
• Choice of the correct glove that with a specific glove-change frequency and type of foods prepared will minimize the risks related to undetected punctures
• Different-colored gloves for when employees handle/prep raw animal proteins versus RTE foods to provide a visual cue to managers for proper glove use and reduction of cross-contamination of food contact and nonfood contact surfaces from gloves
• Suggested raw animal protein-handling glove colors: