Abstract
This study aimed to develop a checklist for good hygiene practices (GHP) for raw material of vegetable origin using the focus groups (FGs) approach (n = 4). The final checklist for commercialization of horticultural products totaled 28 questions divided into six blocks, namely: water supply; hygiene, health, and training; waste control; control of pests; packaging and traceability; and hygiene of facilities and equipment. The FG methodology was efficient to elaborate a participatory and objective checklist, based on minimum hygiene requirements, serving as a tool for diagnosis, planning, and training in GHP of fresh vegetables, besides contributing to raise awareness of the consumers' food safety. The FG methodology provided useful information to establish the final checklist for GHP, with easy application, according to the previous participants' perception and experience.
Introduction
M
Good hygiene practices (GHP) of fresh-cut fruit and vegetables are normally evaluated using a checklist, which taken in account established concepts about food safety of this product category (Cruz et al., 2006a, b; Nunes et al., 2010; Pereira et al., 2013). However, the development of a checklist is a complex process, given the lack of information and the social and economic reality of different establishments (Alpuche-Navarrete et al., 2011) and sometimes does not take into account the different participant's perception about the risks involved in the routine activities.
Focus group (FG) is a qualitative technique defined as a carefully planned interview aimed at obtaining individual opinions about a particular area of interest (Kueger and Casey, 2010), being a popular data collection technique that relies on group interaction to elicit personal and emotional responses toward a product or a concept (Jervis and Drake, 2014). FGs have been used in sensory studies (Jervis et al., 2014) as well as to evaluate consumer perceptions regarding food safety (Mata et al., 2010; Tiozzo et al., 2017). However, the use of FG for the development of a checklist covering GHP of fresh-cut fruits and vegetables has not been reported. In this sense, this study aimed to develop a GHP checklist of the handling of fresh-cut fruits and vegetables produced by family farms and commercialized in a supply center in the State of Rio de Janeiro (CEASA-RJ), using the FG approach.
Materials and Methods
Definition of FG
Four FGs (n = 4) were performed with a total of 28 participants. Participants in each group had similar professional profiles, as follows: postgraduate students in food science and technology (GF1, n = 10), supply center (CEASA) staff (GF2, n = 6), Embrapa (Brazilian Agricultural Research Company) researchers (GF3, n = 6), or health surveillance staff (GF4, n = 6), aged 25–60 years, with similar gender distribution, which allowed a homogeneous session, favoring the discussion. All of the groups are involved in the different stages, with the products in this study being the postgraduate students representing ordinary consumers. Table 1 shows the composition of the different FGs of this study. Four sessions of ∼2 h were conducted, according to the recommendations of Casey and Krueger (1994). At the beginning of each session, the moderator, the first author of this study, informed the purpose of the methodology, its role, and the purpose of the study (Table 2).
CEASA-RJ, supply center in the State of Rio de Janeiro.
General questions were used to provoke discussion among participants, followed by other issues, including marketing practices, basic requirements, and critical hygiene requirements. At the end of each session, participants were asked to judge the individual issues as fundamental or recommended tasks. The specific issues were taken from the subitems of the preliminary checklist for GHP (presented on next item) to facilitate individual assessment. The questions were grouped into six issues: water supply; hygiene, health, and training; waste control; control of pests; packaging and traceability; and cleaning of facilities and equipment, with a total of 28 subitems.
Checklist
The preliminary checklist was developed based on the legislation in force, supporting the creation of the questionnaire used in the FG sessions (Brasil Resolution no. 216 of the 15th of September, 2004). The issues of the preliminary checklist were carefully selected by food professionals, based on existing lists in the legislation. These issues were classified as fundamental or recommended. The fundamental issues were those considered critical to prevent contamination, as there was no subsequent procedure to eliminate the hazard at safe levels. On the other hand, the recommended issues were those complementary to the checklist for GHP, with continuous improvement of hygiene practices in marketing, according to principles of the Hazard Analysis and Critical Control Point system.
Data analysis
Data were analyzed considering the context of the question and specificity of the responses, and no statistical analysis was performed due to the qualitative nature of the study (Jervis and Drake, 2014). The impressions and opinions reported during the sessions were recorded and later analyzed to obtain the final checklist for GHP in a qualitative and participatory manner.
Results and Discussion
The FG discussions had been concentrated on several factors, including the cleanliness and degraded structure of the sector of horticultural products, excess and improper handling of waste, the presence of pests, lack of cleaning and identification of packaging, staff training, and management responsibility and difficulties.
The participants pointed out the main problems according to their perceptions. Table 3 summarized the issues addressed by each group about the main problems related to quality assurance and adequacy of hygienic–sanitary conditions in the family agriculture sector at CEASA-RJ.
General questions
The four discussion groups pointed out a lack of cleanliness and adequacy of the facilities. According to the participants, this deficiency leads to food exposure, allowing the access of pests. In addition, precarious hygiene conditions were associated with lack of training and education of producers. Some participants have discussed the importance of establishing parameters for conservation and problem resolution, including a high volume of residues, improper handling and exposure of food to inadequate temperatures, lack of identification of a product's origin, and lack of professionals for inspection.
The participants belonging to the groups GF1, GF2, and GF3 believed cleaning of packages may be an economically viable and environmentally friendly issue. However, GF2 reported a resistance on the part of the producer, who uses packaging without the minimum quality standards required by the legislation.
Almost all FG considered the training program as an important task, due to the lack of information about the adequate procedures. The discussions pointed out that training can start with a re-registration of the merchants in the sector, being a prerequisite for food suppliers of government programs and school meals. Thus, the training program can start after application of the diagnostic checklist, which will subsidize the content and the form of training of the individuals involved. Training plays a key role in programs aimed to improve the safety of fresh fruits and vegetables (FAO, 2007; Cusato et al., 2013). Inadequate food handling is one of the main causes of food-borne outbreaks in Brazil and other countries, such as New Zealand and the United States, and training of food handlers is one of the most effective strategies for prevention of foodborne diseases, which is mandatory in Brazil and other countries (Rossi et al., 2017).
Specific questions
Water supply
The conservation and protection of water reservoirs and facilities were considered equally important for all FGs. Participants reported that it is essential to keep pipelines and reservoirs protected from vectors and contaminants since the water quality is ensured by the public supply network. Failures in the sewage system and infiltration may occur, leading to contamination of the products.
Concerning the hygiene of water reservoirs, the participants of GF2 and GF4 agreed to be extremely important, as a dirty reservoir can contaminate water over time by consuming residual chlorine. They also reported the importance of the periodic analysis to attest water potability in the reservoirs, as defined by the legislation.
The participants of GF2, formed by CEASA-RJ technicians, stated that cleaning the reservoirs implies their emptying and consequently suspension of water supply to the whole unit, which operates without interruption. Thus, the cleaning procedures need to be planned, without affecting food marketing. In addition, a participant of GF2 reported that water is used to wash floors, surfaces, and equipment that come in contact with food, as well as to moisten vegetables and keep them fresher.
According to GF3, pipelines and reservoirs should be protected from intrusion of pests and contaminants. Once the water quality is guaranteed by the water supply company, the facilities should be protected; otherwise, the sanitation of the reservoirs is ineffective. The construction of a system for the use of rainwater was suggested as an effective alternative for sustainable water consumption.
The discussions showed that water monitoring is considered important not only because of the environment impact, but also due to its use for human consumption and food preparation in restaurants and snack bars that operate within the supply center. As reported by Faour-Klingbeil et al. (2016), water is recognized as one of the most important vectors of human enteric pathogens in vegetables.
According to the FGs, an order of priority should be established for water control. First, an assessment of the conservation status of pipes and reservoirs should be performed to check for cracks, seepage, and protection against contaminants or invasions. In the case of lack of water potability, a specific analysis should be carried out after the observation of the conservation status of the pipes and reservoirs. Finally, a viable planning for cleaning and sanitizing of reservoirs should be provided to avoid impact on daily business activities.
Hygiene, health, and training
Regarding the health status of the workers in the sector of horticultural products, CEASA-RJ technicians (GF2) reported some difficulties in controlling the health status of the team and ascertaining previous diseases due to the high turnover; “there is no doctor in the supply center, thus an ambulance is called when someone is not feeling well”, said a participant. According to their reports, from the point of view of the food manipulators, the human figure poses no potential risk to food, which is observed in food services and industries; “for them, the manipulator does not play an important role because of the obligation to sanitize raw food before consumption”. The other participants emphasized the importance of preventing the increase in microbial load in the marketing stage since there is no guarantee that sanitation will totally eliminate the biological hazards in the later stages.
This information provides evidence that food safety knowledge and attitudes among food handlers are generally poor. The consumption, especially raw, of vegetables and fruits that have not been accurately sanitized can become unsafe to health and lead to foodborne illness (Faour-Klingbeil et al., 2016). It becomes even more serious if we consider that consumers often do not know how to perform the most basic hygiene practices properly, such as washing fruits and vegetables (Moreb et al., 2017) or underestimate their chances of becoming sick from homemade food and do not follow many recommended safe food handling practices (Young et al., 2017). In this context, training program involving this topic should be carried out in all handlers and managers of the food establishments as a potential approach to improve risk perceptions and their food safety knowledge.
According to the group GF2, manipulators have inappropriate habits and attitudes as they manipulate money and smoke along with food handling. Thus, training should be mandatory at the time of registration as a prerequisite for marketing. In addition, the sector should have an appropriate place for the training sessions, emphasizing GHP based on the actual experience of the horticultural products sector. According to GF3, the issues that most affect the consumers' perception and confidence in the purchase intention should be investigated immediately. The other issues, which are not perceptible, such as training and periodic examinations, involve more time and cultural changes. In addition, for changes to occur, people's routine should consider GHP, and the instructions should be focused on the importance of adopting new procedures.
Supervision of the team involved in the marketing tasks was considered as a strategy to detect and prevent health problems, including informal work activities. Training should be ongoing for changing habits and pointing out attitudes that should be cultivated throughout the food marketing process. In addition, the use of uniform was not considered a requirement with a direct impact on food quality. However, the uniform enhances individual posture and personal hygiene conditions. The criteria for wearing the uniform should be clear, with the participation of those involved to achieve the desired effect.
Waste management
All participants understood that waste control at CEASA and its sectors are a priority, once it has a direct impact on the GHP and the environment, as it contributes to the unhealthy conditions and proliferation of pests. In this context, the main issues include placing the garbage away from the marketing area and separated by differentiated collectors; use of sanitized resistant collectors, in sufficient number and capacity; and waste collection frequency according to the volume generated, without extravasations and with correct destination.
Packaging, which is responsible for large amounts of waste, should be recycled in the case of more frequent waste collection. Thus, effective strategies for handling, conservation, classification, and standardization of packaging can reduce waste, bringing benefits to producers. For some participants, waste control is more critical because it is related to people's habits. The group GF2 reported that individuals transporting and receiving food have disposed waste and spoiled food near the exhibition and marketing areas, and the waste collection should be within 2–3 h to avoid unpleasant odors, insects, and refuse collectors.
According to the FGs, large volumes of solid waste are generated by the supply centers. Thus, controlling the reception, destination, and segregation of organic waste and packaging is required, through the adoption of strict criteria in the reception of the goods, with the supervision of qualified personnel. Waste collection and cleaning of facilities should be performed according to standardized protocols. The groups suggested the creation of sectors to facilitate cleaning operations and to acquire compactors and biodigesters for organic packaging and waste, respectively. Concomitantly, farmers, permission holders, transporters, and shippers should be aware of reducing the waste volume and correct destination. Therefore, structural changes throughout the supply center as far as waste control were considered essential and urgent.
Pest control
This issue was also considered of great importance for GHP, and the subitem “actions against the presence of pests” was scored as 100% fundamental for all groups. The participants of GF2 reported that the presence of dogs and cats is facilitated by the permission holders, along with the lack of cooperation by the competent authorities responsible for the removal of animals. They emphasized the lack of a physical barrier to avoid animals from gaining access, besides the need for an adequate space for food storage to avoid exposure to pests. They reported the existence of pigeons that shelter in the beams of the roof, without an effective control of the population of these animals.
One of the participants of GF3 stated that the occurrence of injuries allows the contamination of plant pulps, leading to losses and consequent increase in waste, attracting pests, thus forming a vicious circle. Therefore, integrated and continuous actions in conjunction with the solid waste management plan can be effective for controlling of pests.
Packaging and traceability
The CEASA-RJ technicians (GF2) reported a lack of control of packaging and traceability of marketed foods. The packaging has no regular identification and hygiene and should be replaced by nonreusable containers or returnable plastic boxes, with a bank of boxes for hygiene. According to one participant, it is necessary to deploy the bank of boxes and gradually require the use of returnable sanitized boxes. However, the lack of staff and interest of the management team are still obstacles to be overcome due to economic pressures and marketing using nonreturnable packaging. They reported that there is no incentive to dispose of wooden containers, which leads to considerable losses due to contamination. The change involves the awareness and knowledge about the economic advantages of the appropriate packaging, with possible gains due to better product conservation.
The EMBRAPA technicians (GF3) revealed that customers and consumers' demands usually motivate market changes. They cited as examples the supermarket chains that buy directly from their suppliers and require returnable sanitized plastic boxes for the purchase of horticultural products. Thus, a concept of minimum handling and standardized packaging for products' preservation may be a good strategy for reducing injuries and losses.
The packaging conditions in the marketing of fresh vegetables have been defined in legislation, which has established integrity and size in accordance with the hygienic–sanitary standards and minimum labeling information (MAPA, 2002). In addition, there is another standard used for defining the checklist, which establishes the minimum requirements and testing methods for receiving, sanitizing, and distributing plastic returnable boxes.
FGs have argued that packaging is very important for perishable products such as horticultural products, being attractive at the time of purchase, adding value to food and protecting against contamination. Appropriate packaging and rules for products' traceability should be required for all horticultural products throughout the internal market. Thus, proper packaging and storage of the raw material, as well as the availability of suitable suppliers, hygiene of the handlers and proper management of the waste are issues that deserve attention. In this context, local regulations are required to protect consumers, and ongoing supplier training can help address the lack of quality and safety of foods of plant origin (Baser et al., 2017).
Hygiene of plant and equipment
This section was considered of great relevance, especially for groups GR3 and GR4. Participants of group GF2 were asked about the hygiene of the facilities and equipment, and pointed out that the layout of the sector should be changed to facilitate cleaning of the facilities, as there is no efficient sloping pipe to drain the washing water. According to GF2, an immediate cleaning is not possible when fruits arrive deteriorated in the sector because the collection of the residues is carried out at the end of the commercialization. Sinks with liquid soap and disposable towels should be installed in the marketing area, since there is no lavatory in the sector, without sink and soap in some places.
In addition, according to the participants of GF3 and GF4, several factors are required to minimize contamination, including adequate cleaning and sanitation, easily cleaned surfaces, preventing the access of pests, and adequate structures for temperature and humidity control.
Final checklist for GHP
The checklist for GHP was finalized through the selection of the responses obtained in the FG sessions, based on individuals' experiences. It is worth noting that the list is in accordance with the recommendations of the Recommended International Code of Practices: General Principles of Food Hygiene (Codex Alimentarius, 2006). The final checklist for commercialization of horticultural products totaled 28 questions divided into six blocks (Table 4), namely: water supply; hygiene, health, and training; waste control; control of pests; packaging and traceability; and hygiene of facilities and equipment, respectively, each presenting 3, 6, 5, 3, 5, and 6 issues, respectively. Of the 28 issues under discussion, 21 (75%) were considered as fundamental and 7 (25%) as recommendable in the case of use of the checklist.
F, fundamental; R, recommended.
However, it is worth mentioning that several factors can interfere with the effectiveness of the application of the checklist for GHP, such as awareness and willingness of the management team, existence of training structure, consumer and market demands, organization and changes in the production chain, and routine control by health agencies. These factors can affect the validation of the checklist and the implementation of the corrective measures for the sector.
In addition, the economic issues that also affect the motivations of the productive sectors should be considered for the success and applicability of the checklist for GHP. Although some issues can be addressed through awareness, education, and motivation, others depend on broader structural changes and interventions in the earlier stages of the distribution chain.
Additional studies for validation of GHP using the checklist proposed in this study should be carried out in other supply centers throughout Brazil.
Conclusion
The FG methodology provided useful information to establish the final checklist for GHP, with effortless application, according to the participants' perception and experience, being able to develop a checklist for raw material of vegetable origin considering the participants'perception and knowledge, which presented similar to the current Brazilian legistation.
The authorities should prioritize measures in GHP for marketing of fresh-cut vegetables and fruits in supply centers, which take into account the sanitary legislation and the participant's opinion about the different product categories. The findings of the study reinforce the importance of GHP as one of the prerequisite programs needed to be implemented to support a food safety management system.
Footnotes
Acknowledgments
A.S.S. thanks the financial support of the National Council for Scientific and Technological Development (CNPq) (Grant #302763/2014-7) and Coordination for the Improvement of Higher Level Personnel (CAPES) Grant #33003017027P1. All authors would like to acknowledge the financial support of CAPES and CNPq.
Disclosure Statement
No competing financial interests exist.
