Abstract
Controlling and maintaining the cleanliness of the working environment in restaurants is crucial. The aim of this study was to determine the level of contamination on food contact surfaces in restaurants. A total of 28 restaurants were surveyed, and 500 samples were taken from food contact surfaces that appeared clean and ready for use. The surfaces evaluated in this research included workers’ hands, tools and equipment, worktops, chopping boards, meat grinders, spoons and forks, plates, and kebab skewers. Each sample was collected using a swab on a designated 10 cm × 10 cm square area of the surface. The samples were then tested using a luminometer device to measure enzyme levels and identify bacterial contamination, helping to maintain health and control contamination. The unit of measurement for this device is RLU (Relative Light Unit). The results showed that the cleanliness of contact surfaces varied as follows: workers’ hands (46.43%), worktops (53.57%), kebab skewers (89.29%), plates (92.86%), meat grinders (76%), chopping boards (60.71%), tools and equipment (89.29%), and spoons and forks (96.43%). Regarding foodstuff contamination levels, the chopping board, worktop, and workers’ hands had the highest contamination with average RLU values of 1700.89, 1184.50, and 790.71, respectively. In contrast, plates had the lowest contamination, with an average RLU value of 46.68. Based on these findings, training restaurant staff in personal health, food safety, and regular hygiene practices, along with routine inspections based on guidelines from inspectors, will improve restaurant health standards and help reduce foodborne illnesses.
Supplementary Information
The online version contains supplementary material available at 10.1038/s41598-025-86017-8.
Keywords: ATP bioluminescence, Food contact surfaces, Health inspection, Microbial contamination, Relative light unit (RLU), Restaurant health rating
Subject terms: Microbiology, Diseases, Health care
Introduction
Microbial contamination of foods prepared by catering establishments is a key factor that must be assessed to ensure food safety1. Foods can become contaminated by total mesophilic aerobes (saprophytic microorganisms), as well as spoilage and pathogenic microorganisms of genera such as Staphylococcus, Listeria, Escherichia coli, and Salmonella. Such contamination depends on the quality of raw materials, control of environmental conditions (temperature, humidity, and pH), staff adherence to personal hygiene, thorough cleaning of equipment and tools, and the application of good manufacturing practices (GMPs) by the staff2–4. The cleanliness of the restaurant environment, where food is prepared and consumed, is crucial in preventing foodborne illnesses. Outbreaks of foodborne illness can create unfavorable conditions for restaurants. Food health and safety are particularly important for restaurant owners and managers, as poor sanitation perceptions may lead consumers to choose other, safer options, resulting in a loss of income and credibility5. Microbiological evaluation of restaurants is usually not included in health inspection procedures because traditional microbiological analyses in laboratories can take up to 48 h after sample collection. Additionally, the equipment required for microbiological analysis is costly. This is problematic since bacterial and viral contaminants cannot be detected through visual inspection alone. Indeed, results from using hygiene swabs and agar plates show that visual inspection is an unreliable criterion for cleanliness6,7.
Cross-contamination of food contact surfaces is a major concern for food establishments, as improper cleaning with reusable cloths can spread harmful bacteria and viruses, posing serious health risks for consumers8,9. Approximately 80% of foodborne illness cases are attributed to food establishments, with primary causes being improper time and temperature control of prepared foods, inadequate personal health among food handlers, and cross-contamination10. Regular inspection of the effectiveness of cleaning methods can help prevent the spread of diseases that may be transmitted through food9. Health officers typically conduct visual inspections of food services to assess sanitary conditions11. Although visual inspection of a restaurant kitchen is an important factor in reducing the risk of foodborne illness, microbiological evaluation of specific kitchen areas is also needed to provide additional information to combat outbreaks11. Visual assessment alone is insufficient for health surveillance, as it cannot reliably determine the potential risks posed by contaminated food contact surfaces12. The presence of foodborne pathogens on surfaces in food service facilities and the risk of their transfer from surfaces to food are critical reasons for implementing stringent cleaning methods13. Equipment and surfaces that come into contact with food provide a suitable environment for bacterial spread and biofilm formation due to high exposure to liquids, water, and moisture14,15.
In the past, health inspections of restaurants in Iran were conducted through traditional procedures, with inspectors using paper checklists for visual assessments. In recent years, however, environmental health inspectors have been equipped with portable measuring instruments, including core thermometers, surface thermometers, humidity meters, salt meters, oil testers, pH meters, microbial surface tests, aflatoxin tests, iodized salt tests, and chlorimeters. Sanitary inspections are now conducted at the inspection site using electronic checklists via mobile phones, laptops, or tablets.
In Yasuj restaurants, hand washing, and cleaning of utensils and equipment are still performed using traditional methods that do not fully comply with the health guidelines established by the Ministry of Health in Iran. One of the main issues is the inadequate implementation of these guidelines in non-compliant restaurants, which causes them to fall below acceptable health standards. The purpose of this study was to examine the effect of different washing methods on the microbial contamination of food contact surfaces in Yasuj restaurants using the ATP bioluminescence technique in 2019.
Methods
Ethical approval and informed consent
This study was conducted with restaurant workers, containers, tools, and equipment in Yasuj city, Iran. The restaurants were selected based on a list provided by the health center of the county, under the supervision of Yasuj University of Medical Sciences, and obtained from the comprehensive environmental health inspection system. Only chefs and workers who had direct contact with food were included as participants in this study. Ethical approval was granted by the Ethics Committee of Yasuj University of Medical Sciences with the code IR.YUMS.REC.1398.005. The study adhered to the Ministry of Health guidelines in Iran. Participation was voluntary, with informed consent obtained from all participants and their supervisors. The consent form assured participants that all information and responses would remain confidential. Inspectors from the health center completed questionnaires by interviewing the workers and their supervisors.
This study involved two steps to evaluate the health status of restaurants: the Health Inspection Checklist (HIC) and Contamination of Food Contact Surfaces (CFCS).
Health Inspection Checklist (HIC)
In alignment with the restaurant health guidelines of the Iran Ministry of Health, a total of 28 restaurants were inspected using a standardized health checklist (Checklist S1). This checklist comprises two primary categories of questions: (1) those identifying critical violations, and (2) those identifying non-critical violations. Critical violations require immediate correction on-site or may result in the temporary closure of the establishment, while non-critical violations necessitate corrective action within a specified timeframe. The checklist includes 74 questions organized into four sections: personal health, food safety, sanitation of tools and equipment, and building hygiene (Supplementary information section). Each item is rated under one of four statuses: Yes, No, Correction in Place (CIP), or Not Applicable, with each status marked accordingly16.
The health inspection of restaurants was conducted in two stages. The first stage utilized traditional or visual methods without measuring CFCS, while the second stage involved CFCS measurement using a specialized instrument. In both stages, the inspection checklist responses were marked as “yes” to indicate compliance with the health guidelines established by the Ministry of Health of Iran, and “no” to indicate non-compliance. All inspection data were subsequently logged into the Comprehensive Occupational and Environmental Health Inspection Management System (COEHIMS), which systematically assigns health ratings and recommends necessary actions for each establishment17.
Based on inspection outcomes, restaurants scoring 90–100% receive an “Excellent” or “A” rating (symbolized by three health apples), while scores of 80–89.999% earn a “Satisfactory” or “B” rating (two health apples). Scores of 70–79.999% lead to a “Needs Improvement” or “C” rating (one health apple), and scores below 70% result in an “Unacceptable” rating, leading to suspension. Restaurants failing to achieve or maintain a satisfactory health rating are subject to further review and additional inspection17–19.
Cleaning and washing dishes
In this study, dishwashing was performed manually, with most restaurants utilizing two-stage sinks, while larger establishments employed three-stage sinks (three basins). In restaurants using the two-stage method (two basins), stages 1 and 2 were carried out in the first basin, and stages 3 and 4 were performed in the second basin. During the manual washing process, a thermometer was used to monitor the temperature of both the washing and disinfecting solutions repeatedly. The temperature of the washing solution was maintained at no less than 43 °C, unless otherwise specified in the manufacturer’s instructions or the cleaning agent’s label8,20,21.
The manual washing procedure consists of five steps:
Pre-washing: The first step involves removing and cleaning any food debris from the containers and utensils. To remove food residues, under-pressurized washing with warm water at 49 °C was applied. This initial step helps reduce detergent consumption during the subsequent washing stage (second step) by minimizing the entry of large food particles and waste into the wash water and wastewater. Additionally, any remaining food is collected and discarded dry.
Washing: The second step was conducted in the first basin with warm water at a temperature of 43–49 °C, containing an effective detergent compound. Glass containers were separated from other items for washing, draining, and disinfection.
Rinsing: The third step, final rinsing, was performed by immersing the items in warm water in the second basin. After washing, the dishes and other kitchen utensils were placed in a wire basket embedded in the sink to avoid unnecessary handling and movement of the items. Hot water spray was also utilized for draining, provided that it was fully used and the sink drain remained open. It may be necessary to change the wash water multiple times during this stage to ensure thorough cleanliness of the dishes.
Disinfection: The fourth stage involved submerging the containers in hot water (77–82 °C or higher) for at least 30 s, though a 2-minute duration was generally recommended. In this study, disinfectants were not used to wash the dishes. Disinfectants were primarily used to disinfect sinks and reduce contamination levels before washing to prevent the introduction of pollutants.
Drying: The fifth and final step involved air-drying the dishes. Towels were not used for drying, as they are time-consuming, costly, and, most importantly, unsanitary8,20,21.
Staff hand hygiene
The World Health Organization (WHO) guidelines on hand hygiene in healthcare emphasize the importance of promoting hand hygiene as a key component of a comprehensive approach to reducing healthcare-associated infections. Personnel hand contamination was measured in three stages: pre-wash (baseline condition), conventional washing, and washing according to the guidelines and instructions. Specifically, the conventional washing procedure involves cleaning the staff without any training or adherence to specific guidelines, in contrast to the washing procedure based on the instructions from the Iran Ministry of Health and the World Health Organization22,23. In general, the order of washing is considered conventional when it precedes cleaning and guideline-based washing when it follows cleaning.
Sample collection
Food contamination was evaluated in restaurants serving between 260 and 850 meals daily in Yasuj, Iran. The evaluation focused on food contact surfaces. Samples were taken from various items, including workers’ hands, chopping boards, meat grinders, kebab skewers, spoons, forks, plates, and other equipment. A total of 28 restaurants were sampled, specifically targeting food contact surfaces (workers’ hands, kebab skewers, chopping boards, spoons, forks, plates, tools, equipment, meat grinders, and worktops). These eight selected sampling items represent the surfaces that had the final contact with food before it was served to customers. In total, 500 swab samples were collected by swabbing 100 cm² (10 cm × 10 cm) areas of the eight different types of food contact surfaces. Food contamination was assessed using the ATP bioluminescence assay method with the SystemSURE Plus device for ATP monitoring (manufactured by Hygiena Company in the UK). This device measures the amount of light produced by a chemical reaction and displays the result in relative light units (RLU)24,25. The removal of microbial contamination was calculated using the following equation:
![]() |
Wherein
RLUo= Amount of contamination before cleaning. RLUi= Amount of contamination after cleaning. R = Removal efficiency.
Results and discussion
Health Inspection of restaurants
Inspections of restaurants were conducted using checklists titled “Health Inspection Checklists for Restaurants” in two phases. The first phase involved traditional inspections through visual assessment. The second phase included inspections using measuring tools and equipment, such as measuring food contact surfaces, thermometers, hygrometers, and oil testers, to monitor and control the restaurants. Figure 1 presents the findings from restaurant inspections conducted in two phases, categorized into four areas: personal health, food hygiene, health tools and equipment, and building health, as outlined in the health inspection checklist. A “yes” response indicates adherence to health guidelines, while a “no” response represents noncompliance. In the initial phase, which utilized visual inspection methods, the compliance rates for the four categories were as follows: 58.93% for personal health, 55.00% for food hygiene, 48.31% for health tools and equipment, and 68.88% for building health. Conversely, the second phase, which employed measuring instruments, showed significantly higher compliance rates of 90.05% for personal health, 93.39% for food hygiene, 92.29% for health tools and equipment, and 85.54% for building health. The notable differences between the two phases can be attributed to the incorporation of measurement tools in the second phase. These tools facilitated the evaluation of environmental conditions such as temperature and humidity within the building health category, as well as the assessment of food contact surfaces and cooking temperatures in the food hygiene category. Additionally, handwashing practices were evaluated in the personal health category, and refrigerator temperatures were monitored in the health tools and equipment category.
Fig. 1.
Comparison of restaurant health compliance rates across two stages of inspection: Visual inspection (First step) vs. health guidelines with measuring equipment (Second step).
Table 1 summarizes the results based on the health inspection checklist. The data revealed that during the first step of the inspection, which involved a visual assessment, the surveyed restaurants received the following ratings: 7.14% rated as excellent (A), 35.71% as satisfactory (B), 46.43% as needing improvement (C), and 10.71% classified as unacceptable (suspected or unrated). In contrast, the second step of the inspection, which employed measuring instruments, showed a significant change in ratings: 64.29% of restaurants were rated excellent, 28.57% satisfactory, 7.14% needed improvement, and notably, none were deemed unacceptable. Furthermore, a similar study by Janet Fleetwood emphasized that when inspections are conducted effectively, mandatory hygiene ratings can function as a powerful public policy tool. This approach has the potential to enhance transparency, improve public health, and empower consumers to make informed choices26.
Table 1.
Health ranking of restaurants in two steps inspection (first step inspection: visual inspection, second step inspection: based on health guidelines and measuring equipment’s).
Restaurant rating | First step inspection (%) | Second step inspection (%) |
---|---|---|
Excellent (A) | 7.14 | 64.29 |
Satisfactory (B) | 35.71 | 28.57 |
Needs improvement (C) | 46.43 | 7.14 |
Unacceptable (Unrated) | 10.71 | 0.00 |
The difference between the first and second stages of health inspections in restaurants can be attributed to the visual inspection conducted in the first stage and the use of measuring devices in the second stage. This suggests that restaurant ratings cannot rely solely on visual assessments. A significant portion of this difference in ratings is due to the measurement of microbial contamination on food contact and non-food contact surfaces, temperature and humidity control in the kitchen environment, the microbial quality of drinking water, food assessments—including oil testing—and compliance with health guidelines.
Relative humidity and temperature control
The average temperature and relative humidity in the kitchen environment were 35.89 °C and 29.41%, respectively. In comparison, a study by Angui Li et al. on temperature and humidity in commercial kitchens found that the average cooking temperature across four kitchens ranged from 18.2 to 31.5 °C, while the relative humidity varied between 60.9% and 65.7%28. Additionally, Ghasemkhani and Naseri, who monitored indoor air quality in a kitchen in Tehran, reported that a relative humidity below 30% leads to dry air, which can negatively affect the eyes, skin, and mucous membranes. On the other hand, relative humidity above 60% promotes the growth of pathogens and allergens28. When comparing these findings with those from Angui Li et al. and Ghasemkhani et al., it was observed that the ambient temperature in the studied restaurants was favorable. However, the relative humidity was notably lower, likely due to inadequate ventilation. Specifically, 42.86% of the restaurants had humidity levels below 30%, which contributed to symptoms like eye irritation caused by dry air, poor ventilation, and fumes from frying. Furthermore, the average cooking temperatures for food and catering were found to be 74.3 °C and 55.80 °C, respectively.
ATP bioluminescence assay
Dishwashing practices in all the studied restaurants were based on poor habits and non-compliance with health guidelines. Environmental health inspectors did not address this issue in their inspection checklists. However, improper and unsanitary dishwashing is a significant route for the transmission of contamination to food. In this study, the dishwashing practices of restaurant staff were compared with the washing methods outlined in the health guidelines. ATP bioluminescence assay values were used to assess the contamination levels of food contact surfaces, including knives, cleavers, worktops, kebab skewers, chopping boards, meat grinders, spoons, forks, plates, and workers’ hands. Contamination was determined before cleaning using the ATP bioluminescence method, which identified high RLU values as indicative of contamination (Table 2). The average RLU values before cleaning for all tested surfaces indicated higher contamination levels, as reflected by the elevated RLU values (Table 2).
Table 2.
Food contact surfaces values of before cleaning and after cleaning by ATP bioluminescence assay (RLU) and environment conditions.
Surface type | No. | Before cleaning (RLU) | After cleaning (RLU) | Environment temperature (oC) |
Relative humidity (%) |
Cooking temperature (oC) |
Dishwashing temperature (oC) |
||||
---|---|---|---|---|---|---|---|---|---|---|---|
Min. | Ave. | Max. | Min. | Ave. | Max. | ||||||
Worktop | 28 | 20 | 1184.50 | 6081 | 0 | 49.54 | 667 | 35.89 ± 3.73 | 29.41 ± 5.95 | 74.30 ± 8.06 | 69.32 ± 15.55 |
Worker hand | 28 | 27 | 790.71 | 2116 | 0 | 41.18 | 421 | ||||
Kebab skewer | 28 | 1 | 145.64 | 1933 | 0 | 4.50 | 25 | ||||
Chopping board | 28 | 33 | 1700.89 | 7372 | 0 | 20.71 | 123 | ||||
Meat grinder | 25 | 5 | 508.72 | 4089 | 0 | 12.44 | 96 | ||||
Spoon and fork | 28 | 1 | 113.04 | 454 | 0 | 1.71 | 12 | ||||
Plate | 28 | 1 | 46.68 | 188 | 0 | 3.18 | 34 | ||||
Tools (Knives and cleaver) | 28 | 5 | 486.61 | 2035 | 0 | 3.96 | 14 |
To reduce microbial contamination on food surfaces, both two-stage and three-stage dishwashing methods were employed. These methods did not involve the use of disinfectants. Hot water, with a temperature of 69.32 ± 15.55 °C, was used for washing dishes. As shown in Table 2, the highest contamination levels before cleaning (conventional washing) were observed on the chopping board and worktop, with average RLU values of 1700.89 and 1184.50, respectively. After cleaning, the highest contamination levels were found on the worktop and chopping board, with average RLU values of 49.54 and 20.71, respectively. Although the overall contamination removal efficiency for the worktop and chopping board was 95.82% and 98.78%, respectively, the actual cleanliness levels were 53.57% and 60.79%, based on the device’s standard (RLU values below 10 indicate cleanliness) (Table 3). The results of Monavvar Afzal-Aghaee et al. showed that 43.6% of the evaluated dishes were clean, 38.5% were dirty, and 17.9% were not clean enough. According to the ATP bioluminescence device results for tables, 23.1% of the tested tables were clean, 15.4% were cautionary, and 61.5% were dirty29. A comparison of our findings with those of Monavvar Afzal-Aghaee et al. indicates that the cleanliness of the tables in our study was 2.32 times higher29.
Table 3.
Assessment of cleanliness levels in restaurants before and after cleaning.
Treatments | % of sample before cleaning(RLU/100cm2) * | % of sample after cleaning(RLU/100cm2) | % of contamination removal | ||||
---|---|---|---|---|---|---|---|
< 10 | 11–29 | > 30 | < 10 | 11–29 | > 30 | ||
Worktop | 0.00 | 3.57 | 96.43 | 53.57 | 25 | 21.43 | 95.82 |
Worker hand | 0.00 | 3.57 | 96.43 | 46.43 | 32.14 | 21.43 | 94.79 |
Kebab skewer | 14.29 | 17.86 | 67.86 | 89.29 | 10.71 | 0.00 | 96.91 |
Chopping board | 0.00 | 0.00 | 100 | 60.79 | 14.29 | 25.00 | 98.78 |
Meat grinder | 4.00 | 12.00 | 84.00 | 76.00 | 8.00 | 16.00 | 97.55 |
Spoon and fork | 21.43 | 10.71 | 67.86 | 96.43 | 3.57 | 0.00 | 98.48 |
Plate | 25.00 | 35.71 | 39.29 | 92.86 | 3.57 | 3.57 | 93.19 |
Tools (Knives and cleaver) | 3.57 | 7.14 | 89.29 | 89.29 | 10.71 | 0.00 | 99.19 |
*RLU < 10 = Clean, RLU between 11 and 29 = Caution and RLU > 30 = Dirty.
The method for detecting the contamination of food contact surfaces used in this study (ATP-bioluminescence assay) has shown using a Pearson correlation coefficient (Table S1). The correlation coefficient (R), after cleaning stage, reached a relatively high correlation for the worktop, worker’s hands, and meat grinder compared to before cleaning stage. Statistical analysis indicated a strong correlation in thorough washing (after cleaning) with R = 0.628 for the worktop, R = 0.709 for the worker’s hands, and R = 0.591 for the meat grinder, with a significant relationship at P < 0.05. The reason for this is that food residues and fats on the aforementioned surfaces were not completely removed by the regular method, and the reduction in contamination with this method ranged from 40 to 74%. However, after the three-stage washing process, due to the three stages of washing—removal of food residues and fats, washing with detergents in water at a temperature of 43 °C, and final washing at a temperature of 69 °C—the reduction in contamination on the aforementioned surfaces was observed to be between 91% and 98%. Additionally, the cleanliness level (RLU < 10) increased from 0 to 53.57% on the worktop, from 0 to 42.86% on the worker’s hands, and from 4 to 64% on the meat grinder. Nonetheless, the results in terms of cleanliness after the thorough washing phase were not satisfactory. The type of washing performed after the cleaning stage showed that the detection using the ATP-bioluminescence method resulted in a significantly lower number of RLU compared to the regular cleaning stage. This is due to the presence of bacteria or organic residues from the food containers and equipment resulting from regular washing, which were largely reduced through the three-stage washing method with hot water, a physical sanitization method, resulting in over 91% reduction in contamination across all measured parameters. Particularly since the ATP-bioluminescence assay can detect residual food substances, a surface that has been cleaned and sanitized may still contain some organic materials from food in contact with food contact surfaces. The ATP assay via bioluminescence detected a high level of RLU on the worktop and chopping board sections. This may be due to organic residues remaining from foods or chopped meat on these surfaces, with residues not eliminated by the hot water washing method. The results of this study showed high RLU levels even after the washing stage of the worktop and chopping board. This result can be attributed to the study by Verran et al. regarding the resistance of food residues to cleaning and their adhesion to the worktop and chopping board. Moreover, some bacteria may have resistance to sanitization, allowing them to survive and thus be detectable via the ATP-bioluminescence method in RLU30,31. Murphy et al., and Aycicek et al., found a good correlation between cleaning methods in detecting food contamination32,33.
After the cleaning stage, the average RLU values obtained from the ATP bioluminescence assay remained relatively high for the chopping board, worktop, and worker’s hand, whereas other food contact surfaces displayed comparatively low RLU values (Fig. 2). Additionally, both the chopping board and worker’s hand demonstrated relatively high contamination levels in the ATP bioluminescence assay, both before and after cleaning. The analysis also evaluated the effect of hot water temperature on dishwashing post-cleaning. No significant correlation was identified between the before- and after-cleaning stages and the hot water temperature for the worktop, as indicated by a p-value greater than 0.05. This suggests that temperature had a limited effect on cleanliness due to the uneven surface and material composition, resulting in suboptimal cleanliness levels for the worktop surfaces. Our findings revealed that smoother surfaces, like stainless steel, had lower contamination levels, even at non-elevated water temperatures for disinfection. Although Table 2 indicates a 95.82% reduction in contamination on the worktop surface, this reduction does not reflect complete cleanliness. The average RLU across all restaurants was 49.54, which is still considered contaminated according to washing and measuring device standards. Furthermore, the comparison of pre- and post-cleaning contamination on food contact surfaces, as assessed by the ATP bioluminescence assay (RLU), uncovered very low correlation coefficients (R values) ranging from − 0.126 to 0.220 before cleaning, which improved after the cleaning stage, ranging from − 0.390 to -0.618.
Fig. 2.
RLU values for food contact surfaces in the before cleaning and after cleaning.
Some of the RLU results that appear low before cleaning may be due to excessive contamination, such as residual food materials that could obstruct light transfer to the detector. For example, remnants of meat on skewers or chopping boards, or certain food residues that interfere with luciferase activity in ATP, can result in reduced RLU readings. Contact surfaces with RLU levels exceeding 30 are considered contaminated32. The Public Health Laboratory Service (PHLS) in the UK, which was replaced by the Health Protection Agency in 2003, recommended that surfaces ready for use should not exceed the recommended RLU levels34. According to these guidelines, the cleanliness results obtained after the thorough washing stage for chopping boards and workers’ hand were unsatisfactory, as they contained over RLU 30, with readings of 39.29% and 28.57%, respectively. The results obtained for contact surfaces like skewers, spoons, forks, work tools (knives and cleavers), and plates were entirely satisfactory, while those for meat grinders were relatively satisfactory.
Additionally, 25% and 14.29% of the food contact surfaces were classified as being in a cautionary status (11–29 RLU), which is considered acceptable in terms of cleanliness. The lack of success in reducing microbial contamination through hot water washing can be attributed to the fact that, in 32.14% of the restaurants, the water temperature of the boiler or water heater did not reach the desired level, despite allowing sufficient time for contamination reduction during washing. In some cases, the equipment was also found to be damaged. Another issue was that the worktop and chopping board surfaces were not smooth due to the materials used (7.14% galvanized and 10.71% fiberglass, as indicated in Table 3), which resulted in relatively lower cleanliness levels on these surfaces. The highest average RLU values before the cleaning stage were recorded on the chopping board, worktop, worker’s hands, and meat grinder surfaces, while the plate exhibited the lowest RLU values. After the cleaning stage, the average RLU values were significantly reduced for surfaces such as the spoon and fork, plate, kebab skewer, and knives and cleaver (Fig. 2).
Training on the hand washing method was conducted in accordance with the health guidelines established by the Ministry of Health of Iran. These guidelines allowed for a comparison of the washing techniques: the guideline-based method (the second stage of washing) and the conventional method (the first stage of washing), along with the pre-wash stage. A comparison across all restaurants revealed that conventional washing achieved an average reduction in contamination of 73.80% (207.18 RLU) compared to the pre-wash method, whereas the guideline-based washing method resulted in a contamination reduction of 94.79% (41.18 RLU) (Fig. 2). Furthermore, the washing method following the guidelines was 80.12% more effective in reducing contamination compared to the conventional method, demonstrating that the second stage of washing was 6.33% more effective at reducing hand contamination than the first stage.
It is essential to emphasize that a reduction in contamination on contact surfaces does not necessarily imply cleanliness since cleanliness is defined by specific standards. According to the device’s standard, 46.43% of the workers’ hands were classified as clean (under 10 RLU) (Table 4).
Table 4.
Percentage distribution of materials for various utensils surfaces and tools in this study.
Surface type | Material (%)* | |||||
---|---|---|---|---|---|---|
FG | SS | G | Pl | M | PW | |
Worktop | 10.71 | 78.57 | 7.14 | – | – | 3.57 |
Kebab skewer | – | 85.71 | 14.29 | – | – | – |
Chopping board | 53.57 | 46.43 | – | – | – | – |
Meat grinder | – | 100 | – | – | – | – |
Spoon and fork | 100 | – | – | – | – | |
Plate | – | – | – | 89.28 | 10.72 | – |
Tools (Knives and cleaver) | – | 100 | – | – | – | – |
*Fiberglass (FG), Stainless steel (SS), Galvanized (G), Porcelain (Pl), Melamine (M) and Pressed wood (PW).
Several factors may describe the lack of correlation observed before cleaning food contact surfaces, such as worktops and chopping boards. These factors include the types of cleaning methods used, the materials comprising the food contact surfaces (e.g., stainless steel, galvanized metal, plastic), the varying levels of ATP present in microorganisms—which depend on their type and physiological state—the sensitivity of the ATP detection system, and the smoothness or roughness of the surfaces being cleaned35. Additionally, the differences between the two cleaning methods could be influenced by the locations of the swab sites. Even though the swabs were taken from nearby surfaces, they might contain varying levels of microbial contamination based on the specific site of contamination.
Conclusion
This study’s results indicate that health inspections in restaurants should incorporate control and monitoring instruments to measure critical factors, with results made accessible and easily readable as soon as possible. Even minor microbial contamination can trigger the spread of foodborne illnesses, resulting in significant harm to consumers. The use of sanitary swabs highlights that visual inspections alone are inadequate for assessing cleanliness. Additionally, sampling food contact surfaces and utensils for laboratory analysis is time-consuming and incurs economic losses. Therefore, employing portable devices in restaurants can yield timely results and help reduce foodborne diseases. The environmental health department supports restaurants involved in food preparation, cooking, and delivery. The Restaurant Health Rankings exemplify a public health transparency policy, summarizing the latest health reviews at restaurant entrances using words, letters, numbers, or symbols. This article explores various aspects of restaurant health inspections, including personal health, building cleanliness, equipment health, and food hygiene. To mitigate foodborne illnesses, reduce health violations and public complaints, and enhance food hygiene, fostering competition among restaurants proves beneficial. In conclusion, when health inspectors conduct thorough evaluations, implementing a voting system for restaurant health ratings can serve as an effective public policy that promotes transparency, improves population health, and encourages consumer awareness. It is also recommended to compare the results of the ATP device with laboratory data to ensure accuracy.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Acknowledgements
This article is extracted from a research project approved by Yasuj University of Medical Sciences with ethics code (IR.YUMS.REC.1398.005) and grant number (960406). The authors of the article appreciate the support of Yasuj University of Medical Sciences.
Abbreviations
- RLU
Relative Light Unit
- COEHIMS
Comprehensive Occupational and Environmental Health Inspection Management System
- CFCS
Contamination of Food Contact Surfaces
- CIP
Correction In Place
- GMPs
Good Manufacturing Practices
- HIC
Health Inspection Checklist
Author contributions
Saeid Fallahizadeh: Conceptualization, Methodology, Investigation, Formal analysis, Writing-original draft. Majid Majlesi, Mohammad Reza Ghalehgolab, Mohammad Hassan Sadeghi, Mohammad Reza Zarei, Alireza Raygan Shirazi: Investigation, Methodology, Writing-review& editing. All authors reviewed the manuscript.
Data availability
The datasets used and/or analysed during the current study available from the corresponding author on reasonable request. To access the data, write to email: saeid.eh89@gmail.com.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Contributor Information
Saeid Fallahizadeh, Email: saeid.eh89@gmail.com.
Alireza R. Raygan Shirazi, Email: alirezaraygan47@yahoo.com.
References
- 1.Valero, A. et al. Risk factors influencing microbial contamination in food service centers. Signif. Prev. Control Food Relat. Dis.2016, 27–58 (2016).
- 2.Rodrigues, L. B. et al. ATP-bioluminescence and conventional microbiology for hygiene evaluation of cutting room surfaces in poultry slaughterhouse. Acta Sci. Vet.46, 6 (2018).
- 3.Petruzzelli, A. et al. Microbiological quality assessment of meals and work surfaces in a school-deferred catering system. Int. J. Hospital. Manage.68, 105–114 (2018). [Google Scholar]
- 4.Rode, T. M., Langsrud, S., Holck, A. & Møretrø, T. Different patterns of biofilm formation in Staphylococcus aureus under food-related stress conditions. Int. J. Food Microbiol.116, 372–383 (2007). [DOI] [PubMed] [Google Scholar]
- 5.Choi, J., Almanza, B., Nelson, D., Neal, J. & Sirsat, S. A strategic cleaning assessment program: menu cleanliness at restaurants. J. Environ. Health76, 18–25 (2014). [PubMed] [Google Scholar]
- 6.Griffith, C., Cooper, R., Gilmore, J., Davies, C. & Lewis, M. An evaluation of hospital cleaning regimes and standards. J. Hosp. Infect.45, 19–28 (2000). [DOI] [PubMed] [Google Scholar]
- 7.Moore, G. & Griffith, C. A comparison of traditional and recently developed methods for monitoring surface hygiene within the food industry: an industry trial. Int. J. Environ. Health Res.12, 317–329 (2002). [DOI] [PubMed] [Google Scholar]
- 8.Seyed Reza, G. et al. Tehran University of Medical sciences-Institute for Environmental Research 34–38 (Wiley, 2012).
- 9.Marriott, N. G., Schilling, M. W. & Gravani, R. B. Principles of food Sanitation (Springer, 2018).
- 10.Collins, J. E. Impact of changing consumer lifestyles on the emergence/reemergence of foodborne pathogens. Emerg. Infect. Dis.3, 471 (1997). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Kassa, H., Harrington, B., Bisesi, M. & Khuder, S. Comparisons of microbiological evaluations of selected kitchen areas with visual inspections for preventing potential risk of foodborne outbreaks in food service operations. J. Food. Prot.64, 509–513 (2001). [DOI] [PubMed] [Google Scholar]
- 12.Tebbutt, G., Bell, V. & Aislabie, J. Verification of cleaning efficiency and its possible role in programmed hygiene inspections of food businesses undertaken by local authority officers. J. Appl. Microbiol.102, 1010–1017 (2007). [DOI] [PubMed] [Google Scholar]
- 13.Azizkhan, Z. Comparison between ATP bioluminescence technique and traditional microbiological method to detect contamination within food facilities in Saudi Arabia (Jiddah). J. Public. Health Front.3, 11–18 (2014). [Google Scholar]
- 14.Frank, J. F. Microbial Attachment to Food and Food Contact Surfaces (Wiley, 2001). [DOI] [PubMed]
- 15.Møretrø, T. & Langsrud, S. Residential bacteria on surfaces in the food industry and their implications for food safety and quality. Compr. Rev. Food Sci. Food Saf.16, 1022–1041 (2017). [DOI] [PubMed] [Google Scholar]
- 16.Health, C. f. E. a. O. H.-M. o. The Health Checklist of the Restaurant (2013). https://markazsalamat.behdasht.gov.ir/uploads/Untitled101_190975.pdf.
- 17.System, C. O. a. E. H. I. M. Restaurant health inspection (2019).
- 18.Health, C. f. E. a. O. H.-M. o. Instructions and requirements for giving health apples to restaurants, traditional restaurants, cafeterias, chelokbabi and self service (2013).
- 19.services, A. d. o. H. (2007).
- 20.Salvato, J. A., Nemerow, N. L. & Agardy, F. J. Environmental Engineering (Wiley, 2003).
- 21.Sun, X. Efficacy of Manual Dishwashing and Sanitizer Wiping in Removing Food Soils From Chel Knives (Wiley, 2014).
- 22.Anargh, V., Singh, H., Kulkarni, A., Kotwal, A. & Mahen, A. Hand hygiene practices among health care workers (HCWs) in a tertiary care facility in Pune. Med. J. Armed Forces India69, 54–56 (2013). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Boyce, J. et al. WHO Guidelines on Hand Hygiene in Health Care (World Health Organ, 2009).
- 24.Sanna, T. et al. ATP bioluminescence assay for evaluating cleaning practices in operating theatres: applicability and limitations. BMC Infect. Dis.18, 583 (2018). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Easter, M. & Way, C. Novel developments in ATP bioluminescence. Int. Food Hygiene21, 5–7 (2010). [Google Scholar]
- 26.Fleetwood, J. Scores on doors: restaurant hygiene ratings and public health policy. J. Public Health Policy40, 410–422 (2019). [DOI] [PubMed] [Google Scholar]
- 27.Li, A., Zhao, Y., Jiang, D. & Hou, X. Measurement of temperature, relative humidity, concentration distribution and flow field in four typical Chinese commercial kitchens. Build. Environ.56, 139–150 (2012). [Google Scholar]
- 28.Ghasemkhani, M. & Naseri, F. Comparison of indoor air quality in restaurant kitchens in Tehran with ambient air quality. J. Environ. Health Sci. Eng.5, 59–64 (2008). [Google Scholar]
- 29.Afzal Aghaee, M., Rahnama Bargard, Z., Nezakati Olfati, M. R., Ahooey, R. A. & Gohari, S. An adenosine triphosphate bioluminescence method for evaluating the microbial contamination of the salad-preparing tables and salad-serving dishes in restaurants of Mashhad City, Iran. J. Environ. Health Sustain. Dev.5, 948–954 (2020). [Google Scholar]
- 30.Verran, J. & Jones, M. Problems of Biofilms in the Food and Beverage Industry (Springer, 2000).
- 31.Verran, J., Boyd, R. D., Hall, K. & West, R. The detection of microorganisms and organic material on stainless steel food contact surfaces. Biofouling18, 167–176 (2002). [Google Scholar]
- 32.Murphy, S., Kozlowski, S., Bandler, D. & Boor, K. Evaluation of adenosine triphosphate-bioluminescence hygiene monitoring for trouble-shooting fluid milk shelf-life problems. J. Dairy Sci.81, 817–820 (1998). [DOI] [PubMed] [Google Scholar]
- 33.Aycicek, H., Oguz, U. & Karci, K. Comparison of results of ATP bioluminescence and traditional hygiene swabbing methods for the determination of surface cleanliness at a hospital kitchen. .Int. J. Hyg. Environ. Health209, 203–206 (2006). [DOI] [PubMed] [Google Scholar]
- 34.Survey, N. M. 3rdTrimester (06NS3) Examination of the microbiological status of food preparation surfaces, Final report 06NS3 (2006).
- 35.Leon, M. B. & Albrecht, J. A. Comparison of adenosine triphosphate (ATP) bioluminescence and aerobic plate counts (APC) on plastic cutting boards. J. Foodserv.18, 145–152 (2007). [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data Availability Statement
The datasets used and/or analysed during the current study available from the corresponding author on reasonable request. To access the data, write to email: saeid.eh89@gmail.com.