Potential for Glove Risk Amplification via Direct Physical, Chemical, and Microbiological Contamination.

This review focuses on the potential direct physical, chemical, and microbiological contamination from disposable gloves when utilized in food environments, inclusive of the risks posed to food products as well as worker safety. Unrecognized problems endemic to glove manufacturing were magnified during the COVID-19 pandemic due to high demand, increased focus on PPE performance, availability, supply chain instability, and labor shortages. Multiple evidence-based reports of contamination, toxicity, illness, deaths, and related regulatory action linked to contaminated gloves in food and healthcare have highlighted problems indicative of systemic glove industry shortcomings. The glove manufacturing process was diagramed with sources and pathways of contamination identified, indicating weak points with documented occurrences detailed. Numerous unsafe ingredients can introduce chemical contaminants, potentially posing risks to food and to glove users. Microbial hazards present significant challenges to overall glove safety as contaminants appear to be introduced via polluted water sources or flawed glove manufacturing processes, resulting in increased risks within food and healthcare environments. Frank and opportunistic pathogens along with food spoilage organisms can be introduced to foods and wearers. When the sources and pathways of glove-borne contamination were explored, it was found that physical failures play a pivotal role in the release of sweat build-up, liquefaction of chemical residues, and incubation of microbial contaminants from hands and gloves. Thus, with glove physical integrity issues, including punctures in new, unused gloves that can develop into significant rips and tears, not only can direct physical food contamination occur but also chemical and microbiological contamination can find their way into food. Enhanced regulatory requirements for Acceptable Quality Limits of food-grade gloves, and the establishment of appropriate bioburden standards would enhance safety in food applications. Based on the information provided, together with a false sense of security associated with glove use, the unconditional belief in glove chemical and microbiological purity may be unfounded.

Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 9. Washing and drying of hands to reduce microbial contamination.

During various daily activities at home and work, hands quickly become contaminated. Some activities increase the risk of finger contamination by pathogens more than others, such as the use of toilet paper to clean up following a diarrheal episode, changing the diaper of a sick infant, blowing a nose, or touching raw food materials. Many foodborne outbreak investigation reports have identified the hands of food workers as the source of pathogens in the implicated food. The most convenient and efficient way of removing pathogens from hands is through hand washing. Important components of hand washing are potable water for rinsing and soaps to loosen microbes from the skin. Hand washing should occur after any activity that soils hands and certainly before preparing, serving, or eating food. Antimicrobial soaps are marginally more effective than plain soaps, but constant use results in a buildup of the antimicrobial compound on the skin. The time taken to wash hands and the degree of friction generated during lathering are more important than water temperature for removing soil and microorganisms. However, excessive washing and scrubbing can cause skin damage and infections. Drying hands with a towel removes pathogens first by friction during rubbing with the drying material and then by wicking away the moisture into that material. Paper rather than cloth towels should be encouraged, although single-use cloth towels are present in the washrooms of higher class hotels and restaurants. Warm air dryers remove moisture and any surface microorganisms loosened by washing from hands by evaporation while the hands are rubbed together vigorously; however, these dryers take too long for efficient use. The newer dryers with high-speed air blades can achieve dryness in 10 to 15 s without hand rubbing.

Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 8. Gloves as barriers to prevent contamination of food by workers.

The role played by food workers and other individuals in the contamination of food has been identified as an important contributing factor leading to foodborne outbreaks. To prevent direct bare hand contact with food and food surfaces, many jurisdictions have made glove use compulsory for food production and preparation. When properly used, gloves can substantially reduce opportunities for food contamination. However, gloves have limitations and may become a source of contamination if they are punctured or improperly used. Experiments conducted in clinical and dental settings have revealed pinhole leaks in gloves. Although such loss of glove integrity can lead to contamination of foods and surfaces, in the food industry improper use of gloves is more likely than leakage to lead to food contamination and outbreaks. Wearing jewelry (e.g., rings) and artificial nails is discouraged because these items can puncture gloves and allow accumulation of microbial populations under them. Occlusion of the skin during long-term glove use in food operations creates the warm, moist conditions necessary for microbial proliferation and can increase pathogen transfer onto foods through leaks or exposed skin or during glove removal. The most important issue is that glove use can create a false sense of security, resulting in more high-risk behaviors that can lead to cross-contamination when employees are not adequately trained.

Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 7. Barriers to reduce contamination of food by workers.

Contamination of food and individuals by food workers has been identified as an important contributing factor during foodborne illness investigations. Physical and chemical barriers to prevent microbial contamination of food are hurdles that block or reduce the transfer of pathogens to the food surface from the hands of a food worker, from other foods, or from the environment. In food service operations, direct contact of food by hands should be prevented by the use of barriers, especially when gloves are not worn. Although these barriers have been used for decades in food processing and food service operations, their effectiveness is sometimes questioned or their use may be ignored. Physical barriers include properly engineered building walls and doors to minimize the flow of outside particles and pests to food storage and food preparation areas; food shields to prevent aerosol contamination of displayed food by customers and workers; work clothing designated strictly for work (clothing worn outdoors can carry undesirable microorganisms, including pathogens from infected family members, into the work environment); and utensils such as spoons, tongs, and deli papers to prevent direct contact between hands and the food being prepared or served. Money and ready-to-eat foods should be handled as two separate operations, preferably by two workers. Chemical barriers include sanitizing solutions used to remove microorganisms (including pathogens) from objects or materials used during food production and preparation and to launder uniforms, work clothes, and soiled linens. However, laundering as normally practiced may not effectively eliminate viral pathogens.

Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 10. Alcohol-based antiseptics for hand disinfection and a comparison of their effectiveness with soaps.

Alcohol compounds are increasingly used as a substitute for hand washing in health care environments and some public places because these compounds are easy to use and do not require water or hand drying materials. However, the effectiveness of these compounds depends on how much soil (bioburden) is present on the hands. Workers in health care environments and other public places must wash their hands before using antiseptics and/or wearing gloves. However, alcohol-based antiseptics, also called rubs and sanitizers, can be very effective for rapidly destroying some pathogens by the action of the aqueous alcohol solution without the need for water or drying with towels. Alcohol-based compounds seem to be the most effective treatment against gram-negative bacteria on lightly soiled hands, but antimicrobial soaps are as good or better when hands are more heavily contaminated. Instant sanitizers have no residual effect, unlike some antimicrobial soaps that retain antimicrobial activity after the hygienic action has been completed, e.g., after hand washing. Many alcohol-based hand rubs have antimicrobial agents added to them, but each formulation must be evaluated against the target pathogens in the environment of concern before being considered for use. Wipes also are widely used for quick cleanups of hands, other body parts, and surfaces. These wipes often contain alcohol and/or antimicrobial compounds and are used for personal hygiene where water is limited. However, antiseptics and wipes are not panaceas for every situation and are less effective in the presence of more than a light soil load and against most enteric viruses.

Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 11. Use of antiseptics and sanitizers in community settings and issues of hand hygiene compliance in health care and food industries.

Hand washing with soap is a practice that has long been recognized as a major barrier to the spread of disease in food production, preparation, and service and in health care settings, including hospitals, child care centers, and elder care facilities. Many of these settings present multiple opportunities for spread of pathogens within at-risk populations, and extra vigilance must be applied. Unfortunately, hand hygiene is not always carried out effectively, and both enteric and respiratory diseases are easily spread in these environments. Where water is limited or frequent hand hygiene is required on a daily basis, such as for many patients in hospitals and astronauts in space travel, instant sanitizers or sanitary wipes are thought to be an effective way of preventing contamination and spread of organisms among coworkers and others. Most concerns regarding compliance are associated with the health care field, but the food industry also must be considered. Specific reasons for not washing hands at appropriate times are laziness, time pressure, inadequate facilities and supplies, lack of accountability, and lack of involvement by companies, managers, and workers in supporting proper hand washing. To facilitate improvements in hand hygiene, measurement of compliant and noncompliant actions is necessary before implementing any procedural changes. Training alone is not sufficient for long-lasting improvement. Multiactivity strategies also must include modification of the organization culture to encourage safe hygienic practices, motivation of employees willing to use peer pressure on noncompliant coworkers, a reward and/or penalty system, and an operational design that facilitates regular hand hygiene.

Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 6. Transmission and survival of pathogens in the food processing and preparation environment.

This article, the sixth in a series reviewing the role of food workers in foodborne outbreaks, describes the source and means of pathogen transfer. The transmission and survival of enteric pathogens in the food processing and preparation environment through human and raw food sources is reviewed, with the main objective of providing information critical to the reduction of illness due to foodborne outbreaks. Pathogens in the food preparation area can originate from infected food workers, raw foods, or other environmental sources. These pathogens can then spread within food preparation or processing facilities through sometimes complex pathways and may infect one or more workers or the consumer of foods processed or prepared by these infected workers. The most frequent means of worker contamination is the fecal-oral route, and study results have indicated that toilet paper may not stop transmission of pathogens to hands. However, contact with raw foods of animal origin, worker aerosols (from sneezes), vomitus, and exposed hand lesions also have been associated with outbreaks. Transfer of pathogens has been documented through contaminated fabrics and carpets, rings, currency, skin surfaces, dust, and aerosols and though person-to-person transmission. Results of experiments on pathogen survival have indicated that transmission depends on the species, the inoculum delivery route, the contact surface type, the duration and temperature of exposure, and the relative humidity. Generally, viruses and encysted parasites are more resistant than enteric bacteria to adverse environmental conditions, but all pathogens can survive long enough for transfer from a contaminated worker to food, food contact surfaces, or fellow workers.

Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 4. Infective doses and pathogen carriage.

In this article, the fourth in a series reviewing the role of food workers in foodborne outbreaks, background information on the presence of enteric pathogens in the community, the numbers of organisms required to initiate an infection, and the length of carriage are presented. Although workers have been implicated in outbreaks, they were not always aware of their infections, either because they were in the prodromic phase before symptoms began or because they were asymptomatic carriers. Pathogens of fecal, nose or throat, and skin origin are most likely to be transmitted by the hands, highlighting the need for effective hand hygiene and other barriers to pathogen contamination, such as no bare hand contact with ready-to-eat food. The pathogens most likely to be transmitted by food workers are norovirus, hepatitis A virus, Salmonella, Shigella, and Staphylococcus aureus. However, other pathogens have been implicated in worker-associated outbreaks or have the potential to be implicated. In this study, the likelihood of pathogen involvement in foodborne outbreaks where infected workers have been implicated was examined, based on infectious dose, carriage rate in the community, duration of illness, and length of pathogen excretion. Infectious dose estimates are based on volunteer studies (mostly early experiments) or data from outbreaks. Although there is considerable uncertainty associated with these data, some pathogens appear to be able to infect at doses as low as 1 to 100 units, including viruses, parasites, and some bacteria. Lengthy postsymptomatic shedding periods and excretion by asymptomatic individuals of many enteric pathogens is an important issue for the hygienic management of food workers.

Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 5. Sources of contamination and pathogen excretion from infected persons.

In this article, the fifth in a series reviewing the role of food workers in foodborne outbreaks, background information on the routes of infection for food workers is considered. Contamination most frequently occurs via the fecal-oral route, when pathogens are present in the feces of ill, convalescent, or otherwise colonized persons. It is difficult for managers of food operations to identify food workers who may be excreting pathogens, even when these workers report their illnesses, because workers can shed pathogens during the prodrome phase of illness or can be long-term excretors or asymptomatic carriers. Some convalescing individuals excreted Salmonella for 102 days. Exclusion policies based on stool testing have been evaluated but currently are not considered effective for reducing the risk of enteric disease. A worker may exhibit obvious signs of illness, such as vomiting, but even if the ill worker immediately leaves the work environment, residual vomitus can contaminate food, contact surfaces, and fellow workers unless the clean-up process is meticulous. Skin infections and nasopharyngeal or oropharyngeal staphylococcal or streptococcal secretions also have been linked frequently to worker-associated outbreaks. Dermatitis, rashes, and painful hand lesions may cause workers to reduce or avoid hand washing. Regardless of the origin of the contamination, pathogens are most likely to be transmitted through the hands touching a variety of surfaces, highlighting the need for effective hand hygiene and the use of barriers throughout the work shift.

Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 3. Factors contributing to outbreaks and description of outbreak categories.

In this article, the third in a series of several reviewing the role of food workers in 816 foodborne outbreaks, factors contributing to outbreaks and descriptions of different categories of worker involvement are discussed. All the outbreaks had worker involvement of some kind, and the majority of food workers were infected. The most frequently reported factor associated with the involvement of the infected worker was bare hand contact with the food followed by failure to properly wash hands, inadequate cleaning of processing or preparation equipment or utensils, cross-contamination of ready-to-eat foods by contaminated raw ingredients, and (for bacterial pathogens) temperature abuse. Many of the workers were asymptomatic shedders or had infected family members and/or used improper hygienic practices. Outbreaks were sorted into categories based on how many workers were implicated, the origin of the infective agent (outbreak setting or off site), the degree of certainty that the worker(s) were the cause or were victims, whether or not the workers denied illness, the ability of the agent to grow in the food, whether only the workers and not the patrons were ill, and whether patrons were more responsible for their illnesses than were the workers. The most frequent scenarios were (i) a single worker causing an outbreak by directly infecting patrons; (ii) an infected worker fecally contaminating foods that were then temperature abused, leading to an outbreak; and (iii) multiple workers linked to an outbreak but with no clear initiating source. Multi-ingredient foods with limited descriptions were most frequently implicated and usually were served in restaurants or hotels, at schools, and at catered events. Identified contaminated ready-to-eat foods included produce, baked goods, beverages, and meat and poultry items. In some situations, it was not clear whether some of the workers were the cause or the victims of the outbreak. However, in other situations there may have been an underestimation of the role of the worker. For instance, workers sometimes denied infection or illness for a variety of reasons, but subsequent investigation provided evidence of infection.

Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 2. Description of outbreaks by size, severity, and settings.

This article is the second in a series of several by members of the Committee on the Control of Foodborne Illness of the International Association of Food Protection, and it continues the analysis of 816 outbreaks where food workers were implicated in the spread of foodborne disease. In this article, we discuss case morbidity and mortality and the settings where the 816 outbreaks occurred. Some of the outbreaks were very large; 11 involved more than 1,000 persons, 4 with more than 3,000 ill. The larger outbreaks tended to be extended over several days with a continuing source of infections, such as at festivals, resorts, and community events, or the contaminated product had been shipped to a large number of customers, e.g., icing on cakes or exported raspberries. There were five outbreaks with more than 100 persons hospitalized, with rates ranging from 9.9 to 100%. However, overall, the hospitalization rate was low (1.4%), and deaths were rare (0.11% of the 80,682 cases). Many of the deaths were associated with high-risk persons (i.e., those who had underlying diseases, malnutrition, or both, as in a refugee camp, or young children), but a few occurred with apparently healthy adults. An analysis of the settings for the food worker-related events showed that most of the outbreaks came from food service facilities (376 outbreaks [46.1%]), followed by catered events (126 outbreaks [15.4%]), the home (83 outbreaks [10.2%]), schools and day care centers (49 [6.0%]), and health care institutions (43 outbreaks [5.3%]). However, many cases resulted from relatively few outbreaks (< 30 each) associated with community events (9,726), processing plants (8,580), mobile/temporary service (5,367), and camps/ armed forces (5,117). The single most frequently reported setting was restaurants, with 324 outbreaks and 16,938 cases. Improper hygienic practices in homes, on picnics, or at community events accounted for 89 of the 816 outbreaks. There were 18 outbreaks associated with commercial travel in air flights, trains, and cruise ships over several decades, although only the last seems to be a major concern today. Sixteen outbreaks occurred where food, primarily produce, was harvested and shipped from one country to another. Sometimes the presence of an infected worker preparing food was only one of several factors contributing to the outbreak.

Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 1. Description of the problem, methods, and agents involved.

Food workers in many settings have been responsible for foodborne disease outbreaks for decades, and there is no indication that this is diminishing. The Committee on Control of Foodborne Illnesses of the International Association for Food Protection was tasked with collecting and evaluating any data on worker-associated outbreaks. A total of 816 reports with 80,682 cases were collected from events that occurred from 1927 until the first quarter of 2006. Most of the outbreaks reviewed were from the United States, Canada, Europe, and Australia, with relatively few from other parts of the world, indicating the skewed set of data because of availability in the literature or personal contact. Outbreaks were caused by 14 agents: norovirus or probable norovirus (338), Salmonella enterica (151), hepatitis A virus (84), Staphylococcus aureus (53), Shigella spp. (33), Streptococcus Lancefield groups A and G (17), and parasites Cyclospora, Giardia, and Cryptosporidium (23). Streptococcal, staphylococcal, and typhoid outbreaks seem to be diminishing over time; hepatitis A virus remains static, whereas norovirus and maybe nontyphoidal Salmonella are increasing. Multiple foods and multi-ingredient foods were identified most frequently with outbreaks, perhaps because of more frequent hand contact during preparation and serving.