Food handlers and foodborne diseases: grounds for safety and public and occupational health actions

| One of the causes of foodborne diseases is contamination during food preparation; food handlers carrying pathogens might be involved in the origin of this condition. This problem is more serious in health care facilities, since consumers of contaminated food are already ill. Therefore, operational procedures should be formulated to prevent incidents. We performed a review of scientific studies, legislation and regulations on this subject. The results indicate that the main causes of food contamination involving food handlers to be considered in strategies to reduce, or even eliminate foodborne diseases include: flaws in hand hygiene, intestinal parasites, lack of knowledge of good manufacturing practices (GMP) and of the etiologic agents of foodborne diseases, and lack of GMP monitoring. We conclude that standardized operational procedures should be developed, including clear and objective flowcharts (suggested here) to be managed by the safety and occupational medicine staff, in addition to providing training to food handlers on GMP and correct use of personal protective equipment and work clothes. 37.5% of nasal samples 88 food handlers tested positive Staphylococcus aureus to foodborne The authors analyzed the socioeconomic and occupational profile and level of knowledge of 192 food handlers and the impact of a good manufacturing practice (GMP) training course in Araraquara, São Paulo, Brazil, through 2 questionnaires administered before (baseline) and after (final evaluation) the training course. The results showed that the training course had positive impact on the participants’ level of knowledge. The proportion of right answers increased for all the considered GMP topics in the final compared to the baseline evaluation. 24 samples of sugarcane juice for consumption were tested by means of conventional methods for heterotrophic bacteria, total and thermotolerant coliforms, Salmonella spp. and parasites. 25% of the samples were rated unsatisfactory, since the levels of thermotolerant coliforms were above the maximum permissible in the Brazilian legislation. Thermotolerant coliforms were detected on the hands of 37% of food handlers, and the heterotrophic bacteria count was 2.0x10 3 CFU/hand. As per the responses given on questionnaires, 62% of participants admitted to ignore/not to implement any food hygiene/sanitation practice. The authors assessed the hygiene and sanitary conditions of kitchens in public and philanthropic daycare centers through a food contamination risk score. The results showed that the risk of food contamination was high, being food handlers behaviors one of the main risk factors. The authors concluded that investing in training and continuous monitoring of food handlers is the best and easiest means to ensure the hygiene, sanitation and quality of food. The authors observe that food handlers play a crucial role in food production, and may be determinant for the occurrence of foodborne diseases as a function of the epidemiological hygiene and sanitary conditions. Special attention should be paid to the formulation and implementation of good manufacturing practice training The authors investigated food handlers’ perception of hygiene practices in the workplace and its correlation with the results of bacteriological analysis of hand samples. 61.36% of hand and 25% of tool samples tested positive for the investigated pathogens (coliforms at 45ºC, sulfite-reducing Clostridia , coagulase-positive Staphylococcus and aerobic mesophilic heterotrophic bacteria). These findings were significantly associated with low self-perceived personal, environmental and food handling hygiene. To investigate microorganisms indicative of poor hand hygiene among food handlers, the authors collected 3 samples in each of 5 businesses on alternate days. None of the 15 samples met the Pan American Health Organization standards (maximum permissible count: 10 2 CFU/hand). The authors concluded that lack of information on correct hand washing might favor pathogen transmission to food, with serious consequences for the health of consumers. The aim of this study was to analyze the knowledge and attitudes of food handlers in the of hospitals in 20 food handlers were subjected to interviews and subungual examination in August 2012. The results showed that some aspects relative to personal and food hygiene still needed to be reinforced, even among the participants with adequate technical training to perform their work correctly, hand washing in particular, since 35% of the subungual samples tested positive for intestinal parasites (ameba, Ascaris lumbricoides ) and Enterobacteriaceae ( Escherichia coli ). species from workers’ and nails] The prevalence of fungi varied among the various occupational groups: food handlers, 26.3% to 63.4%; health care workers, 6.7% to 93%, with predominance of Candida spp. The prevalence rates were lower for other groups, with predominance


INTRODUCTION
In the state of São Paulo, Brazil, the Health Surveillance Center, State Secretariat of Health, is responsible for the control of the quality of food 1 . Within this context, one particular focus of concern for this agency -which mission is to preserve and promote the health of the population -is the prevention of foodborne diseases, i.e. those which result from the intake of contaminated foodstuffs and/or water. There are more than 250 types of foodborne diseases, most of them caused by bacteria or their toxins, viruses and parasites 2 .
The World Health Organization rates foodborne diseases a serious global public health problem, which accounts for illness in 1 in 10 people and 33 million years of life lost. The Centers for Disease Control and Prevention reported that foodborne diseases affect 1 in 6 people in the United States (48 million people) resulting in 128,000 admissions to hospital and 3,000 deaths 3 .
According to the Brazilian Ministry of Health, several factors contribute to the occurrence of foodborne diseases, including: poor sanitation, poor quality drinking water, inadequate personal hygiene, and intake of contaminated foodstuffs 3 .
In Brazil, the Collegiate Board Resolution no. 216, from 15 September 2004 4 , defines as food handlers all the individuals who work in a food business and are in direct or indirect contact with food. For this reason, this population of workers should receive special attention from health surveillance agencies. Indeed, food handlers carrying pathogens may contaminate the products or foodstuffs they handle, and thus put the health of consumers at risk 5 .
In the case of health care facilities this problem should receive utmost attention, since eventually contaminated food may be served to individuals with an already impaired state of health. Therefore, besides the tests indicated in the Occupational Health Medical Control Program (OHMCP) in compliance with the Ministry of Labor Regulatory Standard 7 6 , additional tests should be performed to investigate cases of infectious or parasitic diseases among food handlers, be they symptomatic or not.

OBJECTIVE
To provide technical and legal grounds for standard operational procedures (SOP) and flowcharts to monitor the state of hygiene and health of food handlers at the food services department of a large university hospital in São Paulo, Brazil.

MATERIALS AND METHODS
We performed a review of the Brazilian and international literature to establish the state of the art in the subject of interest, and analyze and synthesize the available information.
The literature search was conducted in databases Scientific Electronic Library Online (SciELO), Latin American and Caribbean Center of Information on Life Sciences (Regional Library of Medicine-BIREME) and Virtual Health Library (VHL) among others. We also looked for rulings (Google database), resolutions and regulatory standards (legislation databases). The time frame was set to the period from 1995 to 2017, and the keywords used were food safety, food contamination and food handling, in Portuguese and English, found in Health Sciences Descriptors (DeCS).
We selected 18 studies published in Portuguese, English or Spanish, and four pieces of legislation.
The results are presented in Charts 1 and 2. The software Excel was used to plot graphics and flowcharts to systematize the data considered relevant.

RESULTS AND DISCUSION
According to the Health Surveillance Center Regulatory Standard 5 7 , from 9 April, 2013, food handling comprises all the procedures used to transform raw materials into foodstuffs along the following steps: processing, fractioning, packaging, storage, transport, distribution, and retail display.
Food handlers are all the individuals who work in a food business and handle ingredients and raw materials, equipment and tools used in preparation and packaging, or are involved in the fractioning, distribution and transport of foodstuffs 7 .
The topics most frequently addressed in the selected studies were: pathogens among food handlers, training, and relevance of hand hygiene (Graphic 1). We also analyzed the frequency of the words used in abstracts (Graphic 2).
Some of the analyzed studies investigated intestinal parasites to call the attention to the transmission of foodborne diseases by food handlers. The parasites most frequently reported were Entamoeba coli, Endolimax nana and other commensals. Also pathogenic parasites were described, mainly Entamoeba histolytica/Entamoeba dispar, Giardia lamblia, Ancylostomidae and Strongyloides stercoralis, which represent a more serious situation as concerns contamination [8][9][10] . The authors analyzed the socioeconomic and occupational profile and level of knowledge of 192 food handlers and the impact of a good manufacturing practice (GMP) training course in Araraquara, São Paulo, Brazil, through 2 questionnaires administered before (baseline) and after (final evaluation) the training course. The results showed that the training course had positive impact on the participants' level of knowledge. The proportion of right answers increased for all the considered GMP topics in the final compared to the baseline evaluation.
[Actions for food sanitary quality and safety management in a self-service restaurant] 24 samples of sugarcane juice for consumption were tested by means of conventional methods for heterotrophic bacteria, total and thermotolerant coliforms, Salmonella spp. and parasites. 25% of the samples were rated unsatisfactory, since the levels of thermotolerant coliforms were above the maximum permissible in the Brazilian legislation. Thermotolerant coliforms were detected on the hands of 37% of food handlers, and the heterotrophic bacteria count was 2.0x10 3 CFU/hand. As per the responses given on questionnaires, 62% of participants admitted to ignore/not to implement any food hygiene/sanitation practice.
[Hygiene and sanitary conditions of kitchens in public and philanthropic daycare centers] Oliveira et al. 16 Ciência e Saúde Coletiva, vol. 13, no. 3, p. 1051-1060, Jun 2008 The authors assessed the hygiene and sanitary conditions of kitchens in public and philanthropic daycare centers in São Paulo, Brazil, through a food contamination risk score. The results showed that the risk of food contamination was high, being food handlers behaviors one of the main risk factors. The authors concluded that investing in training and continuous monitoring of food handlers is the best and easiest means to ensure the hygiene, sanitation and quality of food.
[ The authors observe that food handlers play a crucial role in food production, and may be determinant for the occurrence of foodborne diseases as a function of the epidemiological hygiene and sanitary conditions. Special attention should be paid to the formulation and implementation of good manufacturing practice training to prevent foodborne diseases.
[Good practices among food handlers in ice cream kiosks] Souza et al. 18 Higiene A review of observational, descriptive or analytical studies published from 1986 through 2014 concluded that food handler training programs might contribute to ensure the safety of food, with long-term benefits for the food and nutrition industry. Systematic assessment of food handlers' competence enables strategies to develop training models to achieve the desired behavioral changes. The authors investigated food handlers' perception of hygiene practices in the workplace and its correlation with the results of bacteriological analysis of hand samples. 61.36% of hand and 25% of tool samples tested positive for the investigated pathogens (coliforms at 45ºC, sulfite-reducing Clostridia, coagulase-positive Staphylococcus and aerobic mesophilic heterotrophic bacteria). These findings were significantly associated with low self-perceived personal, environmental and food handling hygiene. The aim of this study was to analyze the knowledge and attitudes of food handlers in the food and nutrition department of 2 private hospitals in Fortaleza, Ceará, Brazil. 20 food handlers were subjected to interviews and subungual examination in August 2012. The results showed that some aspects relative to personal and food hygiene still needed to be reinforced, even among the participants with adequate technical training to perform their work correctly, hand washing in particular, since 35% of the subungual samples tested positive for intestinal parasites (ameba, Ascaris lumbricoides) and Enterobacteriaceae (Escherichia coli).
[Fungal species isolated from workers' hands and nails]

Ferreira and Martins 25
Revista Brasileira de Medicina do Trabalho, vol. 14, no. 1, p. 60-70, 2016 The prevalence of fungi varied among the various occupational groups: food handlers, 26.3% to 63.4%; health care workers, 6.7% to 93%, with predominance of Candida spp. The prevalence rates were lower for other groups, with predominance of dermatophytes. In the study by Capuano et al. 8 , most individuals infected with parasites were asymptomatic at the time of medical visits, while only 14.7% reported complaints. Workers carrying commensals were not allowed any contact with food for the duration of treatment.
Yeasts were found during investigation of onychomycosis, sometimes associated with nail infection by Several authors stressed the relevance of familiarity with good manufacturing practices (GMP) and within this context, of training courses as the main means for food handlers to acquire such knowledge. The Brazilian Health Regulatory Agency (ANVISA) Collegiate Board Resolution no. 216 categorizes as "good practices" all the procedures which should be implemented in food services to ensure the hygiene of food as per the sanitary legislation. While knowledge of GMP was found to be poor among food handlers, it improved after they received training [12][13][14] , from 71 (minimum sufficient) to 89% (sufficient) in the study by González-Munõz and Palomino-Camaro 13 . Also other authors emphasized the relevance of training [15][16][17][18] and periodic refresher 8 courses, with assessment of their efficiency 19 . Some of the factors found to enhance the success of training programs are management support, equipment and tool availability, and motivation 19 .
Inspection by authorized agencies or food service managers was also mentioned as crucial to promote GMP. One single study 20 analyzed foodstuffs, and found that their condition complied with the hygiene and sanitary requirements in vigor. Yet the authors observed that some procedures were irregular, and attributed this fact to the lack of technical managers at the analyzed institutions (schools) 20 .
Some authors developed an instrument for internal monitoring -Analysis of Hazards and Critical Points for Control (Análise de Perigos e Pontos Críticos de Controle -APPCC) to be administered by owners or managers of foods services 8 .
Devides et al. 12 found that 23 of 192 participants in their study had taken some training course on food handling, however 47% of them only to comply with health surveillance agency requirements.
Some studies subjected samples taken from the hands of food handlers to microbiological analysis, and all were found to be contaminated, mainly by anaerobic mesophilic bacteria, Clostridium, Staphylococcus aureus, coliforms and Escherichia coli 15,[21][22][23][24] ; Candida spp. predominated among fungi 25 . Pathogens were also found on personal protective equipment (PPE) which situation further contributes to contaminate food 22 .
The findings reported in the analyzed studies were mainly due to lack of knowledge about hand hygiene and foodborne diseases among workers 15,23 . In one single study the participants reported to wash their hands and tools, but with water alone 15 .
Pathogens were found on the hands of workers even when they had received adequate technical training. This finding points to the need to insist on stressing the relevance of personal and food hygiene 24 .
Chart 3 describes the main reasons for food contamination pointed out in the analyzed studies and possible solutions.
The unfavorable findings reported in the analyzed studies occur against the good practice legislation for the food industry and services in the state of São Paulo. According to such legislation, food handlers cannot be carriers of any evident or non-evident infectious or parasitic disease, and their state of health should be duly documented in medical and laboratory reports as per the regulations in force 6,7 .
Workers with lesions or diseases involving the skin, mucous membranes or nails, wounds or cuts on the hands or arms, or acute or chronic eye, lung, pharyngeal or gastrointestinal infection cannot be allowed to handle foodstuffs. Workers with any of these conditions should be referred for medical examination and treatment and not permitted to handle foodstuffs as long as these conditions persist 7 .
The State Secretariat of Health Administrative Ruling no. 2,619 26 , from 2011, items 15.34.1 and 15.34.2, establishes that in addition to the tests described in the OHMCP, food handlers and all those involved in the distribution and serving of meals should be subjected to stool culture and the ova and parasite (O&P) exam at the time of hiring and on 6-month medical examinations; those who exclusively handle packaged foods should be tested once a year.
ANVISA established additional regulations for food handlers, further reinforced in later administrative rulings. Such regulations stress the need for adequate personal hygiene, wearing clothes appropriate for the job, in good state, clean and changed at least once daily. They further call the attention to the relevance of hand hygiene since the time of arriving in the workplace, after handling foodstuffs, and after any interruption of tasks. These rulings also state that employers/technical managers must mandatorily place posters in visible places providing orientation on appropriate hand washing and antisepsis, and other hygiene habits 4 .
Additional hygiene rules for food handlers include: not smoking, not singing, not whistling, not sneezing, not coughing, not eating, not spitting, not handling money, and avoid talking unnecessarily while handling food. In regard to personal hygiene: wearing hairnets or caps, keeping the nails short and without enamel, avoiding wearing jewelry and makeup, and beards in the case of men 4 .
Many of these requirements should be included in local SOPs for food handlers' hygiene and health, including the need for training programs and records of the employees who effectively attend sessions to be presented when requested by inspectors 27 .
None of these documents attribute food contamination and possible transmission of foodborne diseases to food handlers alone, but address in general terms structural aspects and work processes in food services facilities.

CONCLUSION
The results of the present study evidence the relevance of formulating SOPs for food handlers' hygiene and health, including personal hygiene and hand washing. Instructions should be given on appropriate hand washing, step by step, and describing the necessary products.
Employers should ensure adequate conditions for appropriate hand washing (number and distribution of washbasins, soap, paper towels, etc.) and place posters illustrating the procedure and its relevance.
SOPs should clearly describe the procedures to be implemented whenever food handlers exhibit respiratory Chart 3. Causes of contamination and suggested solutions in studies retrieved from databases ScieELO, BIREME and VHL, 2018 (n=18).

Causes of food contamination Suggested solutions
Poor hand hygiene Washing hands with tap water and neutral liquid soap, followed by iodophor-based antisepsis 21 as per the legislation in force 7,23,24 Intestinal parasites Pathogen investigation 9,10 -stool culture and ova and parasite exam 25 Ignorance of good manufacturing practices (GMP) Non-monitoring of GMP Systematic monitoring 8,14,20 or gastrointestinal symptoms, lesions on the skin, or any other health condition that might threaten the safety of food. The medical staff should formulate standardized measures, for instance, whether asymptomatic workers infected with commensals should or not receive treatment. Training has paramount importance (including duration, content and frequency) and attendance should be mandatorily recorded as per the legislation in force. Also appropriate PPE and daily changes of clothes are highly significant aspects.
OHMCP should indicate what tests will be required from food handlers and their periodicity, since the legislation affords some flexibility to the physicians in charge and as function of the geographical location of organizations.
To conclude, we developed two flowcharts with measures to monitor the state of health of food handlers (Flowcharts 1 and 2, Chart 4).