Food Control 22 (2011) 831e837

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Food Control
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A HACCP plan for mycotoxigenic hazards associated with dry-cured meat production processes
Dereje T. Asefa a, Cathrine F. Kure b, Ragnhild O. Gjerde c, Solveig Langsrud b, Mohamed K. Omer d, Truls Nesbakken e, Ida Skaar a, *
a

The National Veterinary Institute, Ullevlsveien 68, P. Box 750, 0106 Sentrum, Oslo, Norway Noma mat, Osloveien 1, N-1430, s, Norway Stranda Spekemat AS, degrdsveien 89, 6200 Stranda, Norway d Norwegian Meat and Poultry Research Centre, P. Box 396, 0513 kern, Oslo, Norway e Norwegian School of Veterinary Medicine, Ullevlsveien 72, P. Box 8146 Dep, 0033 Oslo, Norway
b c

a r t i c l e i n f o
Article history: Received 19 May 2010 Received in revised form 12 August 2010 Accepted 3 September 2010 Keywords: Dry-cured meat products HACCP Mycotoxigenic hazards

a b s t r a c t
This work provided a HACCP plan for mycotoxigenic hazards associated with dry-cured meat production facility. Mycotoxigenic hazards that could emerge at each stage of the production were described. Pathogenic yeasts, toxic secondary metabolites of toxigenic moulds were identied as the potential hazards. Smoking and the dry-ripening stages of production were the critical control points identied. Critical limits for the critical control points were set based on scientic premises and recommendations set by legislative authorities. The status of the critical limits at the identied critical control points need to be monitored, veried and recorded. 2010 Elsevier Ltd. All rights reserved.

1. Introduction Hazard Analysis Critical Control Point (HACCP) is a scientic approach to assess hazards associated with food production and establish control systems to ensure food safety (FAO, 1997). It is a preventative system, that takes the whole chain of food production into consideration before biological, chemical and/or physical hazards affect the safety of food products (FAO, 1997; Food Product Association (FPA), 2006). The system focuses on assessing hazards associated with a particular food production, identifying production stages where the hazards occur and design control mechanisms (Ropkins & Beck, 2000). HACCP system is intended to address hazards that their elimination or reduction to acceptable levels is essential to the production of safe food (FAO, 1997; Orriss & Whitehead, 2000; Ropkins & Beck, 2000). An effective HACCP system should be built on a solid foundation of prerequisite programs, such as good manufacturing practices (GMP) and standard operational procedures (SOP) (FAO, 1997; Food Product Association (FPA), 2006). These programs provide the basic conditions that are necessary for the production of safe, wholesome

* Corresponding author. Tel.: 47 23216244; fax: 47 23216202. E-mail address: ida.skaar@vetinst.no (I. Skaar). 0956-7135/$ e see front matter 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodcont.2010.09.014

food (Orriss & Whitehead, 2000). GMPs are practices and procedures performed by food processors in order to keep the safety of the food products. GMPs may refer to the hygienic conditions of the people, equipment, process and the environment in the production process (Food Product Association (FPA), 2006). SOPs are written descriptions of specic tasks to be carried in a particular food processing activity. They are used in conjunction with GMPs to support a HACCP system (Food Product Association (FPA), 2006). Even if the HACCP system has been successfully applied in the food industry, there are food safety hazards that were not given signicant attentions. This is especially true with regard to mycotoxigenic hazards associated with animal food products. The term mycotoxigenic hazards is used in this manuscript to describe pathogenic yeasts, toxic secondary metabolites of toxigenic moulds that contaminate food products and affect food safety. Most HACCP plans in food processing activities, such as the production of cheeses and dry-cured meat products, considered mainly bacterial agents (Arvanitoyannis & Mavropoulos, 2000; Barbuti & Parolari, 2002), even if such food products get often contaminated with mycotoxigenic hazards. In earlier studies the potential pathogenic yeasts and toxigenic moulds in the production processes of Norwegian dry-cured meat products were reported with a recommendation for effective intervention measures to minimize the occurrence of potential food safety hazards (Asefa, Gjerde et al.

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2009; Asefa et al., 2010; Asefa, Mretr et al. 2009). Hence, the ndings were used to develop a HACCP plan specically for the mycotoxigenic hazards associated with the Norwegian dry-cured meat production processes. 2. Methods

set by the critical limits to guarantee the safety of the products. Verication and records systems were proposed to determine the effectiveness and tractability of the HACCP plan. 3. Results 3.1. The HACCP team

The tasks outlined in Codex Alimentarius (FAO, 1997) were followed to develop a HACCP plan for mycotoxigenic hazards that includes the following seven principles of HACCP.        Conduct hazard analysis (HA) Identify critical control points (CCP) Establish critical limits (CL) Monitor each CCP Establish corrective action Establish verication procedures Establish record keeping

Multidisciplinary HACCP team led by the quality manager of the dry-cured meat production facility was established. The team members were experts in mycology, food microbiology; veterinary medicine, meat science and have extensive experience in food safety research activities, HACCP systems for a range of food production activities, risk assessment procedures and food safety management systems. The team obtained the ow diagram from the producer and described the products with their intended use. 3.2. Dry-cured meat production processes and the ow diagram The production processes of two smoked dry-cured hams and one unsmoked Norwegian speciality called Fenalr (dry-cured leg of lamb) were considered. The only difference between the hams and fenalr production processes are the use of thawed meat and the absence of smoking in the later case (Fig. 2). In the processes, fresh and thawed meat pieces were deboned in the trimming room

The steps outside of the dry-cured meat production facility were excluded as the existence of effective control systems is expected. Tree diagram was used to identify each potential mycotoxigenic hazard at each processing stage and determine whether the stage is a CCP or not (Fig. 1). For the CCP identied reliable control mechanism and corrective actions established to full the requirements

Fig. 1. Decision tree diagram for CCP (FAO, 1997).

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Fig. 2. Flow diagram of the dry-cured meat production (Asefa, Mretr et al. 2009).

mycological quality compared to the outdoor air. Difference in the mould spore concentration was also observed among the different production rooms. Higher concentration of moulds associated with dry-cured meat products was observed in the air of salting, brining and smocking room. These rooms serve as important reservoirs of mould spores that contaminate the dry-cured meat products. The producer washed semi-dried meat products in between the drying and ripening processes in order to remove visible mould colonies that grew on the meat surfaces. The HACCP team believed rather the process could make the products wetter, increase the water activity and ultimately facilitate the proliferation of toxigenic moulds and might lead to the potential production of toxic secondary metabolites on the products. Hence, the team recommended the deletion of this process as long as it does not affect the sensory qualities of the products. Sorting and mould cleaning activities at the sorting room were also important in increasing the likelihood of product contamination by increasing the mould spores in the air of the production facility. For this HACCP plan to work these important deviations in the GMP has to be corrected. They need some technical solutions. Zoning (clean and unclean areas), improved air circulation systems, improved air pressure gradient that can limit the migration of spores from unclean to clean areas of the production facility could be of a great help. Organizational solutions such as training, clearly dened work responsibility that can restrict free movement of staffs, strict personal and environmental hygienic practices are also recommended (Asefa et al., 2010). 3.4. Hazard analysis, critical control points (CCP), critical limits (CL) and corrective actions identied for each stage of production In general, the mycotoxigenic hazards identied in the production processes were pathogenic yeasts and toxic secondary metabolites of toxigenic moulds (Asefa, Gjerde et al. 2009; Asefa, Mretr et al. 2009). 3.4.1. Hygienic quality of raw meat at reception The mycological hazards associated with fresh and thawed meat are pathogenic yeasts. (Asefa, Mretr et al. 2009; Bisbe et al., 1987; Nunez et al., 2000). Yeasts like Candida zeylanoides were frequently isolated from the fresh and frozen meats delivered by different slaughter houses (Asefa, Mretr et al. 2009). Our previous works indicated that subsequent processing activities such as salting, brining, smoking and drying, retarded the growth of pathogenic yeasts and facilitated their replacement by non-pathogenic, but important yeasts like Debaryomyces hansenii (Asefa, Mretr et al. 2009; Martin, Cordoba, Aranda, Cordoba & Asensio, 2006; Martin, Cordoba, Benito, Aranda & Asensio, 2003; Nunez, Rodriguez, Cordoba, Bermudez & Asensio, 1996). Hence, this stage did not full the criteria to be a CCP. The traces of toxic fungal secondary metabolites in fresh or thawed meat originated from contaminated feeds are the potential important chemical hazards at this stage (Mahmoud, Abou El-Alla & Sayed, 2001). The risk can only be minimised by demanding for documentation that indicates the animals slaughtered had received good animal husbandry practice. If so the animals would receive safe and quality feed which in turn is important for the quality and safety of the meat. Current regulatory programs such as Food Act of Norway (The Ministry of Health and Care Services in Norway, 2004), are expected to reduce the occurrence and transfer of natural chemical contaminates in use for animal production to the consumers. 3.4.2. Trimming The production activity at this stage is deboning. Pathogenic yeasts like C. zeylanoides, are still the potential hazards that could

and transferred to the salting room. Before the addition of salt, the meat pieces are pressed and kept in elastic nets. The pressed meat are dipped in a brine solution before they go through smoking, drying, washing, dry-ripening, sorting and packing production processes respectively. The nal products are for direct consumption with no further processing. The products have the shelf life of eight months at refrigeration temperature and their composition is described in Table 1. 3.3. The status of the prerequisite programmes Even though the producer follows standard good manufacturing practices (GMP), some deviations were observed as indicated in (Asefa et al., 2010) and were shortly described below. The pressing process at the salting room, spore concentration in the air of salting, brining and smoking rooms and the activity in the sorting room were identied as important factors facilitating the contamination of products by fungi, specically moulds. Visual observation revealed that most of the dry-cured meat products contaminated with toxigenic moulds were those that have cracks on the surface due to improper pressing activity (Asefa et al., 2010). The cracks seem to create hiding spots for mould spores, suitable microclimate for mould growth and possibly for the subsequent production of toxic secondary metabolites. Hence, reducing crack formations through a good GMP can minimise the risk of mould growth and the potential production of toxic secondary metabolites on the products. The indoor air had poor
Table 1 Composition of the products. Parameter Water activity (aw) Salt NaNO3 (E250) Protein Fat Antioxidant Level 0.84e0.90 6e8% 0.02% 28 gm/100 gm 13e14 gm/100 gm Sodium ascorbate (E301)

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occur (Asefa, Mretr et al., 2009; Bisbe et al., 1987). However, they do not compromise the safety of the products as subsequent salting, brining, smoking and drying production process control and will be replaced by important non-pathogenic yeasts as discussed earlier (Asefa, Mretr et al., 2009; Martin et al., 2006; Martin et al., 2003; Nunez et al., 1996). Moulds were not isolated frequently at this stage and the potential production of toxic metabolites that could raise a food safety hazard is minimum. 3.4.3. Salting and brining Bone free meat is treated with excess salt (NaCl) after pressing and netting processes. The meat was treated with curing salts like sodium nitrate (NaNO3) at refrigeration temperature. Pathogenic yeasts are still the mycotoxigenic hazards identied but the potential hazards could be controlled by the subsequent brining, smoking and drying processes (Asefa, Mretr et al. 2009; Martin et al., 2006; Martin et al., 2003). Salt lowers the water activity of the products by diffusing into the center of the meat. It inhibits microbial growth on the products there by enhances durability and safety (Blesa et al., 2001). 3.4.4. Smoking The meat was exposed to cold smoking (20e30  C) in order to facilitate a faster surface drying process and inhibit microbial growth. This process was identied as the rst critical control point (CCP1) as it minimizes the potential food safety hazards that could arise from pathogenic yeasts. 3.4.4.1. Hazard characterization. The pathogenic yeasts, such as C. zeylanoides, that were frequently isolated in the earlier production processes were the hazards to be controlled and their growth was completely inhibited by smoking process (Asefa, Mretr et al., 2009). The process facilitates the proliferation of important yeasts like D. hansenii in the late production stages by minimizing the potential competition that could arise from the pathogenic yeasts. 3.4.4.2. Critical limits. Time and temperature specications described in the ow diagram (Fig. 2), i.e., 2e4 days of light smoking and a temperature of 20  C are working well and can be used as the critical limits. Temperature and time of smoking should be recorded properly. 3.4.4.3. Verication. Samples should be taken at xed intervals, if possible frequently, for mycological analysis in order to verify the effectiveness of this process to control pathogenic yeasts and perform corrective actions in case of deviation. However, further research that increases our understanding about the effect of smoking on fungal growth is needed. 3.4.5. Dry-ripening The drying process is a critical step in ensuring product safety as it affects the microbiological and chemical aspect of the product. The meat undergoes a carefully controlled and monitored surfacedrying process using air. The ripening process starts right after the drying process, but interrupted only by the washing process. At the ripening process the dehydrating process continues while lipolysis and proteolysis activities that are responsible for sensory qualities (Toldra, 2002) of the products are initiated. A good temperature and humidity control in the drying chamber is required throughout the process. The drying and ripening rooms at the production facility have a temperature range of 12e16  C and a relative humidity of 70%e80%. With the exclusion of the washing process, the team considered the drying and ripening processes as one whole process and named it dry-ripening stage of production.

The occurrence of toxigenic moulds usually prevails at the drying and ripening stages of production (Asefa et al., 2010; Nunez, Rodriguez, Bermudez, Cordoba & Asensio, 1996). Hence the dryripening process was identied as an important critical point at which potential mycotoxigenic food safety hazards can emerge (Table 2). 3.4.5.1. Hazard characterisation. Secondary toxic metabolites such as penicillin, Ochratoxin A, cyclopiazonic acid, verrucosidin and aatoxins which can be produced by toxigenic moulds associated with dry-cured meat products (Chiavaro et al., 2002; Iacumin et al. 2009; Mintzlaff, Ciegler & Leistner, 1972; Monaci, Palmisano, Matrella & Tantillo, 2005; Nunez et al., 2000; Papagianni, Ambrosiadis & Filiousis, 2007; Petzinger & Weidenbach, 2002) are the important food safety hazards identied. The toxic secondary metabolites that could be produced on food products vary with the types of toxigenic moulds growing on them. Isolates of P. nalgiovense dominated on the dry-cured meat products of the production facility studied and most of them have the ability to produce penicillin (Asefa et al., 2010). Hence, penicillin is considered as the important food safety hazard that could occur. Research nding in other countries proved that toxic secondary metabolites of toxigenic moulds could be produced and accumulated on dry-cured meat products (Iacumin et al., 2009; Laich, Fierro, Cardoza, & Martin, 1999; Monaci et al., 2005; Nunez, Westphal, Bermdez, & Asensio, 2007; Toscani et al., 2007). If penicillin is produced on the products, the level should not expose the consumers to a point that exceeds the maximum tolerable weakly intake (TWI) set by the legislative authorities, which in Norway is 4 ug/kg of the body weight (Grnningen, 2008) (Table 3). Similarly, if moulds capable of producing Ochratoxins A are contaminating the dry-cured meat products, the level should not expose the consumers to a point that exceeds the maximum tolerable weekly intake (TWI) of 100 ng/kg of body weight (Norwegian Institute of Public Health, 2008). 3.4.5.2. Critical limits. Moulds ability to produce toxic secondary metabolites is highly affected by the water activity of the substrate (Gqaleni, Smith, Lacey & Gettinby, 1997; Nunez et al., 2000). It is possible to reduce the production and accumulation of toxic secondary metabolites by controlling the level of water activity and adjusting the drying and ripening temperatures. A signicantly higher verrucosidin production by P. polonicum was reported at a water activity of 0.99 in comparison to the water activities of 0.97 and 0.95 (Nunez et al., 2000). The production of aatoxin by A. avus was reported to reduce by 50e60% as the water activity dropped from 0.99 to 0.95 (Gqaleni et al., 1997). A temperature range from 20e30  C was reported as optimum for the production of high amount of toxic secondary metabolites range, given a higher water activity is in place (Gqaleni et al., 1997; Nunez et al., 2000). Hence any attempt to reduce the potential production of mycotoxins should consider water activity. A drying process that lowers the water activity of the products faster to a level near to 0.9 minimises the risk of the production of toxic secondary metabolites tremendously. Mycotoxins production by toxigenic moulds was not observed at a water activity of 0.9 (Gqaleni et al., 1997). The team used these research ndings and set critical limit for water activity of the products at 0.92 at the end of the drying process and 0.9 at the end of the ripening process. The critical limit for the drying and ripening temperature proposed by the team was 20  C and the drying and ripening rooms should have a relative humidity lower than 75%. The producer has a lower drying and ripening temperature (Fig. 2), and it is important to follow up the level of the temperature and relative humidity are consistent through out the drying and ripening processes.

D.T. Asefa et al. / Food Control 22 (2011) 831e837 Table 2 Mycotoxigenic hazards in dry-cured meat production processes. Process Reception Activities Receiving fresh and frozen meat Quality control (documentation) Thawing Trimming Salting Defrosting the frozen meat Deboning fresh and defrosted meats Netting Pressing Salting Dipping meat in brine solution Light smoking Drying and ripening processes responsible for the development of sensory qualities Hazard Pathogenic yeasts (Candida zeylanoides) Toxic secondary metabolites Pathogenic yeasts Pathogenic yeasts Pathogenic yeasts Risk of occurrence High Low High High Medium Control measures eControlled by subsequent steps eDocumentation from the supplier eControlled by subsequent steps eControlled by subsequent steps eControlled by subsequent steps eControlled by subsequent steps eSmoking for three days temperature of 20  C eZero tolerance for crack formation on product surface eaw of the products below 0,9 eTemperature below 20  C eThe identied CCPs are expected to minimize the occurrence of the hazards eIdeal for verication process eThe identied CCPs are expected to minimize the occurrences of the hazards CCP

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CP (GMP) CP (GMP) CP (GMP) CP (GMP) CP (GMP)

Brining Smoking Drying and ripening

Pathogenic yeasts Pathogenic yeasts Growth of toxigenic moulds and production and accumulation of toxic secondary metabolites

Medium

CP (GMP) CCP1 CCP2

High

Sorting

Product assessment and selection

Packing

Packing, storing until shipment and documentation at shipment

Growth of toxigenic moulds and production and accumulation of toxic secondary metabolites Toxic secondary metabolites

Medium

CP (GMP)

Low

CP (GMP)

3.4.5.3. Verication. Frequent visual inspections can be performed by the staffs in the production facility and samples of dry-cured meat products with safety concerns can be taken for the analysis of the occurrence of toxigenic moulds. Such analysis can be used as tools of decision to perform the analysis of the occurrence of potential toxic secondary metabolites. Temperature, relative humidity, water activity, types of moulds on the products and results of toxic secondary metabolite analysis are some of the important records to be documented. The maximum tolerable weekly intake values set by the legislative authorities could serve as tools to verify the effectiveness of the critical limits to reduce or eliminate occurrence of toxic secondary metabolites.

3.4.6. Sorting and packaging Products with visible moulds were sorted out from those without before packing. This is an important control point and can be used for verication of the identied CCPs to produce quality and safety (Table 2 and 3). A quality control system that facilitates the analysis of toxic secondary metabolite on selected products representative for the batch should be in place. This has to be done for products with and without visible mould growth and if toxins are found, the concentration should not exceed the acceptable level set by the legislative authorities (Grnningen, 2008; Norwegian Institute of Public Health, 2008). Before the actual packing process of sliced products, 3e4 pieces of unsliced dry-cured meat products are allowed to be vacuum

Table 3 The HACCP plan for mycotoxigenic hazards in dry-cured meat production processes. CCPs Hazard Description and HACCP plan Critical Limits CCP1 Controlling pathogenic yeasts CCP2 Products contaminated with toxigenic moulds and production and accumulation of toxic secondary metabolites eLight smoking for three days at 20  C eaw < 0.9 eZero tolerance for crack formation on product surfaces eTemperature lower than 20  C Monitoring eTemperature control eNumbers of smoking days. eControl the aw eControl performance of pressing machine in salting room eControl the drying and ripening temperature Corrective actions eMaintenance of smoking ovens in case of defection eFacilitate a correct drying and ripening temperature eHold all suspected products and test eaw below 0.9 eZero tolerance for crack formation while pressing the meat Verication eTemperature check eQC audits of the ovens eCheck aw of the products eTemperature check in the drying chamber eQC audits eRandom sampling to control the type of moulds growing on the products periodically and if toxigenic test selected products for the occurrence of potential toxic secondary metabolites HACCP Records eMaintenance and performance records eaw records eBatch records eMaintenance and performance records eResults of laboratory analysis

Date

Signature .

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Fig. 3. Modied Flow diagram with critical control points (CCP) and control points in the production of dry-cured meat products.

packed in order to facilitate an even distribution of salt through out the products. The vacuum packaging reduces the ability of fungi to grow further and become reasons for food safety hazards. It should be done properly as a part of the GMP. 3.4.7. Validation of the HACCP plan and record keeping Initial validation of this HACCP plan is necessary to determine its effectiveness to keep the identied hazards at an acceptable level. In addition, a systematic revalidation should be performed by reviewing the HACCP plans, and recording properly the identied CCPs, critical limits, deviations registered, corrective actions performed, verications performed via random sampling and analysis followed by continuous maintenance. 4. Conclusion Summaries of hazards, CCP and the HACCP plan are indicated in Tables 2 and 3 with critical limits and corrective actions. However, the successful implementation of this HACCP plan depends on the correction of the deviations in the prerequisite programs. The basic conditions and activities that maintains good hygienic and production practices and reduce product contamination by fungi should be in place. The full commitment of the management and the employees is also required. The commitment of the management to convey a positive message at all levels of the operation in both words and actions are important. Training of personnel at the two CCPs (Fig. 3) about the importance of food safety hazards is important for the effective implementation of this HACCP plan. Any concerns or weaknesses in these should be addressed to ensure product safety. Acknowledgements We wish to thank all the operators at the dry-cured meat production facility, staffs of Section of Mycology and Section of Food and Feed Microbiology at the National Veterinary for their support while developing the plan. This work was nanced by the Norwegian research council and Stranda Spekemat AS. References
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