Food safety knowledge, attitudes and practices of institutional food-handlers in Ghana

Background In large scale cooking, food is handled by many individuals, thereby increasing the chances of food contamination due to improper handling. Deliberate or accidental contamination of food during large scale production might endanger the health of consumers, and have very expensive repercussions on a country. The purpose of this study was to evaluate the food safety knowledge, attitudes, and practices among institutional food- handlers in Ghana. Methods The study was conducted using a descriptive, cross-sectional survey of 29 institutions by conducting face to face interview and administration of questionnaire to two hundred and thirty-five (235) institutional food-handlers. The questionnaire was peer-reviewed and pilot tested in three institutions in the Upper East Region of Ghana, before the final version was distributed to food-handlers. The questionnaire was structured into five distinctive parts to collect information on (i) demographic characteristics, (ii) employees’ work satisfaction, (iii) knowledge on food safety, (iv) attitudes towards food safety and (v) food hygiene practices. Results Majority of the food-handlers were between 41–50 years (39.1%). Female respondents were (76.6%). In our study, the food-handlers were knowledgeable about hygienic practices, cleaning and sanitation procedures. Almost all of the food-handlers were aware of the critical role of general sanitary practices in the work place, such as hand washing (98.7% correct answers), using gloves (77.9%), proper cleaning of the instruments/utensils (86.4%) and detergent use (72.8%). On disease transmission, the results indicates that 76.2% of the food- handlers did not know that Salmonella is a food borne pathogens and 70.6% did not know that hepatitis A is a food borne pathogen. However, 81.7% handlers agreed that typhoid fever is transmitted by food and 87.7% agreed that bloody diarrhea is transmitted by food. Logistic regression analysis testing four models showed statistically significant differences (p < 0.05), for models in which the explanatory variable was the level of education. Conclusions In generally, the institutional food-handlers have satisfactory knowledge in food safety but this does not translate into strict hygienic practices during processing and handling food products.


Background
When food is cooked on a large scale, it may be handled by many individuals and thus increasing the chances of contamination of the final food. Unintended contamination of food during large scale cooking, leading to food-borne disease outbreaks can pose danger to the health of consumers and economic consequence for nations [1][2][3].
Food-borne related illnesses have increased over the years, and negatively affected the health and economic well-being of many developing nations [4]. The World Health Organization (WHO) states that about 1.8 million persons died from diarrheal diseases in 2005, mainly due to the ingestion of contaminated food and drinking water. Food poisoning occurs as a result of consuming food contaminated with microorganisms or their toxins, the contamination arising from inadequate preservation methods, unhygienic handling practices, cross-contamination from food contact surfaces, or from persons harboring the microorganisms in their nares and on the skin [5,6]. Unhygienic practices during food preparation, handling and storage creates the conditions that allows the proliferation and transmission of disease causing organisms such as bacteria, viruses and other food-borne pathogens [7,8]. Additionally, many reported cases of food-borne viral diseases have been attributed to infected food-handlers involved in catering services [9].
In Ghana, both public and private institutions often have food service or catering units where meals are served to both staff and clients. Such institutions may include schools, research institutes, hospitals and prisons. To prevent outbreak of food-borne diseases in these institutions, high standards of hygienic and safety practices by foodhandlers are essential parts of an overall food safety program implemented by these institutions. Although institutional food-handlers may possess the required knowledge and skills needed in food safety practice, errors due to human handling are often cited in several food-borne disease outbreaks [10][11][12]. As Greig et al. [11] reports, about 97% of reported food poisoning cases are due to the improper handling of foods by persons involved in catering services.
The knowledge, attitudes and practices of food-handlers have been reported in studies from different countries around world [13][14][15][16][17][18]. This is because a combination the three factors: knowledge, attitude and practice of foodhandlers, play dominant role in food safety with regards to food service industry [19]. In Ghana, previous studies have evaluated the knowledge, attitudes and practices of foodhandlers in selected hotels in Accra [2], and food hygiene practices by street food vendors [20]. Recently, food safety knowledge, attitudes and self-reported practices of food handlers in institutional foodservice in Accra-Ghana has also been reported [21]. All these studies were however limiting in scope as they were restricted to only Accra, the capital city. At the moment, there is no published report on the knowledge, attitude and practice of food-handlers in institution selected from different geographical regions of Ghana. Such studies are however, important as they provide a nation-wide assessment of training needs, attitudinal changes and effectiveness of training and education to provide continuous consumer assurance of the safety of food. Such investigations will also provide better understanding of the interactions of prevailing food safety knowledge, attitudes and practices of food-handlers throughout the country, Ghana.
This study therefore sought to assess the knowledge, attitudes, and practices of institutional food-handlers in Ghana, with regard to food hygienic practices and over-all safety.

Study population
A total of 235 institutional food-handlers participated in the study. A descriptive, cross-sectional survey of 29 institutions was employed in this study. The institutions included ten (10) Senior High Schools, nine (9) District Hospitals, two (2) Prison Services, six (6) Universities/ Polytechnics and one (1) Health Research Center located in 5 administrative regions including Upper East, Northern, Ashanti, Volta, Brong-Ahafo and Eastern regions of Ghana (Fig 1).

Interviews
Face-to-face interviews were conducted using structured questionnaire to collect information on the knowledge, attitudes and practices of the food-handlers on food safety. The questionnaire was peer-reviewed and pilot tested in three institutions in the Upper East Region of Ghana, before a final version was administered to foodhandlers. Participants were interviewed by the researchers and trained research assistants using the structured questionnaire. Data was collected between December 2014 and June 2015.
The questionnaire was structured into five distinctive sections. Section one was to collect information on respondents' demographic characteristics such as gender, age, level of education and length of employment in the food service business. Section two was concerned with information on the employees' work satisfaction while Questions pertaining to demographic information of respondents and employees' work satisfaction were adapted from Soares et al. [22] and Jevšnik et al. [16]. Answers were graded on a scale of five, with 1 indicating "strongly disagree" and five indicating "strongly agree". Questions on food safety knowledge, attitudes and practices were adapted from previously published works [13,[22][23][24].
The section of questionnaire dealing with food safety knowledge comprised 25 close-ended questions with three possible answers; "true", "false", and "do not know". These questions specifically dealt with respondents' knowledge of personal hygiene, cross contamination, food-borne diseases, microorganisms, temperature control and hygienic practices. A scale ranging between 0 and 24 (representing the total number of questions on food safety knowledge) was used to evaluate the overall knowledge of respondents. Food-handlers that obtained total score ≤16 points were considered to have "insufficient" knowledge and those that had scores ≥17 points (≥68% accuracy) were considered to have "good" knowledge of food safety.
Questions pertaining to attitudes (section 4) were aimed at determining the understanding of foodhandlers about food safety. Here, attitudes was used to mean "a complex mental state involving beliefs, feelings, values and dispositions to act in certain ways" [19]. This section had 20 statements/questions that required three possible responses: "agree", "disagree", and "don't know or remember". For evaluation, food-handlers that answered to 13 or less statements/questions correctly were measured to have "insufficient or poor" understanding, whereas those that responded to 14 or more statements/ questions correctly were measured to have "good" understanding.
In section five, which dealt with food hygiene practices, the good hygienic practices of respondents (institutional food-handlers) were assessed and evaluated based on self-reporting of personal hygiene and other safe food handling practices. The section had 11 statements/questions with two possible responses: "yes", and "no". Each correct practice reported scored one (1) point. For evaluation, a score ≥ 70% by an individual respondent was considered as having "good" food hygienic practice.

Statistical analyses
The statistical package for social science (SPSS) for Windows (version 11.0, 2001, Chicago, IL) was used for analyses of data. Difference in means were considered statistically significant at p < 0.05. Mean scores of responses were converted into percentages for purposes of easy interpretation of results. One way analysis of variance (ANOVA) was used to compare the mean scores of knowledge, attitude, and practice among the different educational levels of respondents. The mean score of knowledge, attitude, and practice were compared by ttest. The responses were also reclassified into two categorical responses 'yes' and 'no' for correct and incorrect responses respectively.
In order to identify the variables that impacted on the observed results, four logistic regression analysis models were developed. The four models included knowledge of foodborne diseases, knowledge and attitudes regarding personal hygiene, knowledge and attitudes regarding temperature control, and knowledge and attitudes towards food hygienic practices. Predictive variables including age, length of employment and education level were incorporated into all models with general knowledge on food safety as the dependent variable.

Results and discussion
Demographic characteristics Table 1 presents the summarized demographic profile of respondents in this study. Out of the 235 food-handlers who participated in this study, 76.6% (n = 180) were female while 23.4% (n = 55) were males. Most studies have reported higher proportion of females [22,25,26] involvement in food handling. A greater number (39.1%) of the participants were in the age bracket of 41-50 years with average age of 41.5 ± 9.5 years. Similar studies showed that workers in older age brackets had better hygiene scores than their younger colleagues [27,28]. Approximately 14.5% of the participants in this study did not have any formal education. However, a previous study demonstrated that irrespective of educational level, employees performance in food safety knowledge was not satisfactory and thus a cause for public concern [29]. A greater number of participants (76.2%) had >5 years of experience working in the foodservice industry with an average length of 11 ± 7.8 years. Eighty three percent were full time workers in the institutions whiles the rest were part time workers. Only a few (8.1%) of the respondents self-reported that they have ever received training in food safety. Although several studies have shown that training may contribute to upgrading the food safety knowledge of food-handlers, this does not always translate into a positive change in food handling behavior and attitudes [12,30].

Employees' work satisfaction
Work satisfaction was surveyed to ascertain institutional food-handler's satisfaction with the conditions, work load, work relations and other people reaction toward them (Table 2). In general, 24.7% of the institutional food-handlers affirmed that if they had to choose a profession again, they would choose the same profession, 48.5% said they would not choose the same profession, whiles 26.8% were indifferent about the issue of choosing a profession again.
In answering the question; would you quit this work if you are offered something better at a different place, about 95.3% affirmed they will leave while 4.7% were not certain. About 62.1% said the workplace make available all the necessary conditions for guaranteeing food safety. On the issue of sharing problems, 64.3% agreed that they do share their personal problems with their head of departments.

Food safety knowledge of food-handlers
In our study, the food-handlers were knowledgeable about hygiene practices, cleaning and sanitation procedures ( Table 3). Majority of food-handlers in this study knew the importance of general sanitary practices such as regular hand washing at the work place (98.7% correct answers), wearing of gloves (77.9% correct answers), proper cleaning (86.4% correct answers) and detergent use (72.8%).
The awareness of such important hygienic procedures by majority of the institutional food-handlers in this study is very appropriate. This is because the hands of food-handlers can serve as vectors in the spread of foodborne diseases due to poor personal hygiene or crosscontamination [14,31]. Proper hand washing by foodhandlers has been reported to significantly decrease the threat of diarrheal disease in child care facilities [32] and can therefore be encouraged as it could similarly help minimize the risk of diarrhea and other foodborne diseases in similar institutions. Despite a self-reported hand washing practiced by food-handlers, many employees' in a study by Stepanović et al. [33] had coagulase-positive staphylococci isolated from their hands, and this could be a source of food contamination. Therefore, it is prudent to combine proper hand washing with the wearing of gloves and other hygienic practices in order to  minimize the risk of contamination during food handling [34]. Regarding foodborne disease transmission, 76.2% of the food-handlers (respondents) did not know or remember that Salmonella is a food-borne pathogens and 70.6% did not know/remember that hepatitis A is a foodborne pathogen. On the other, 81.7 and 87.7% of respondents agreed that typhoid fever and bloody diarrhea respectively can be transmitted by food. The majority (86.8%) of respondents disagreed that HIV/AIDS is transmitted by food, which is an indication that public education on HIV/AIDS by the Ghana AIDS commission could be yielding results. These results support recently published work where majority of the respondents did not know if Salmonella, hepatitis A and B viruses, and Staphylococcus caused foodborne diseases [13,22]. Over ninety percent (90%) of respondents agreed that taking leave from work in periods of infectious skin disease was necessary (Table 3). Additionally, 71.5% knew that microorganisms can be found on the skin and in the mouth and nose of healthy looking individuals. They also recognize that the health status of food-handlers should be assessed prior to employment.
On the other hand, food-handlers were less familiar with time and temperature abuse and its effect on food safety (Table 3). Anon [35] reported that improper handling of food, including the abuse of timetemperature, account for most food-borne disease outbreak. In this study, respondents had insufficient knowledge on time-temperature controls. This result is supported by others [14,29] whose report show that knowledge of critical temperatures were insufficient amongst food-handlers. Similar findings on the lack of adequate knowledge on temperature controls by food-handlers have also been reported from different countries [36][37][38]. During infectious disease of the skin, it is necessary to take leave from work. 93.6 (220) 0.0 (0) 6.4 (15) The health status of workers should be evaluated before employment. 99.6 (234) 0.4 (1) 0.0 (0) The ideal place to store raw meat in the refrigerator is on the bottom shelf. 40

Food safety attitudes of food-handlers
A reduction in the incidence of food-borne illnesses is strongly influenced by the attitudes of food-handlers towards the implementation of food safety plans. Thus, there is a strong linkage between positive behavior, attitudes and education of food-handlers in maintaining safe food handling practices [12]. Table 4 shows the attitudes of the food-handlers toward the prevention and control of food-borne diseases. About 60% of respondents indicated that using caps, masks, protective gloves and proper clothing can minimize the risk of food contamination, which is a positive attitude reported by majority of the respondents. Similarly, majority of respondents (93.6%) agreed that knives and cutting boards should be properly sanitized to prevent cross contamination of foods. Respondents also agreed that individuals with abrasions or cuts on their fingers or hands should not touch unwrapped foods (87.2%). The majority (88.1%) of food-handlers were aware that food should not be handled with long and painted fingernails. They were also mindful of the fact that dish towels could cross-contaminate foods (71.5%) and that well-cooked foods are free of contamination (86.4%). Thus, the general attitudes of the foodhandlers toward food safety was satisfactory, except on issues relating to refrozen of defrosted food. About 81.7% of food-handlers had unsatisfactory attitude towards defrosted and refrozen foods. Refreezing a completely thawed food can present a serious health risk, as this process leads faster growth of contaminating bacteria. Freezing food only slows bacterial growth and does not necessarily kill the pathogens [39]. Respondents (86.4%) did not find it necessary to check the temperatures of refrigerators and freezers periodically (86.4%). Table 5 shows the food safety practices by institutional food-handlers. In assessing the food safety practices of the institutional food-handlers, 88.1% reported that they do not use gloves during the distribution of unpackaged foods. Majority (61.7%) of the food-handlers do not use aprons or wear mask when necessary. Additionally, they eat and drink during working hours. On sanitizer use, 61.7% reported that they do not use sanitizer in washing utensils such as plates, mugs and spoons. All respondents reported that they do not use sanitizer when washing fruits or vegetables. About 83.8% of the institutional food-handlers do prepare meals in advance. Only 17% of respondents reported that they look out for the shelf-life of foods when taking delivery of them.

Food safety practices by food-handlers
Some previous studies suggest that the lack of knowledge in food safety can lead to poor hygienic practices by food-handlers [27,40]. However, Clayton et al. [41] reported that about 63% of food-handlers demonstrating Proper hand hygiene can prevent food-borne diseases.
93.6 (220) 0.0 (0) 6.4 (15) When cleaning products are closed, they can be stored with cans and jars of food that are also closed. The health status of workers should be evaluated before employment.
60.0 (141) 6.4 (15) 33.6 (79) The best way to thaw a chicken is in a bowl of cold water. Knives and cutting boards should be properly sanitized to prevent cross contamination.
87.2 (207) 0 (0) 12.8 (30) knowledge in food safety did not demonstrate a corresponding positive behavior towards food safety/hygienic practices. This shows that food-handlers might not necessarily be practicing strict food safety procedures during food handling, even when they provide answers to show that they are knowledgeable in a survey. Therefore, other factors such as employee motivation and continuous education and training on the job should be provided to inspire food-handlers, which will affect attitudes and subsequently food-safety practices [42].

Logistic regression analyses
Logistic regression analysis testing four models to identify the variables that impacted on the observed results are shown in Table 6. All models tested except model 2 showed statistically significant differences (p < 0.05). The significant differences were only observed for models in which the explanatory variable was the level of education.

Conclusions
In general, institutional food-handlers in Ghana had satisfactory knowledge in the areas of food safety, general and personal hygiene, cleaning and sanitation procedures. However, this did not translate into strict food hygiene practices. Therefore continuous food safety education and motivation for foodhandlers of various demographic backgrounds with special attention paid to those with lower levels of education would complement other interventions that pursue the enhancement of food safety systems in Ghana.