Food Safety Challenges Associated with Traditional Foods in German-Speaking Regions

Food Control 43 (2014) 217e230

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Food Control

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Review Food safety challenges associated with traditional foods in German-speaking regions

Friedrich-Karl Lücke a,*, Peter Zangerl b a Dept. Nutritional, Food and Consumer Sciences (OE), Hochschule (University of Applied Sciences), P.O. Box 2254, 36012 Fulda, Germany b Bundesanstalt für Alpenländische Milchwirtschaft (Federal Institute for Alpine Dairying, BAM), 6200 Jenbach/Rotholz 50a, Austria article info abstract

Article history: The “German-speaking region” in Central Europe is characterized by a large variety of regional food Received 4 January 2013 specialities and long tradition in craftsman’s skills and experience in safe small-scale food processing and Received in revised form preservation. There is also increasing interest in these traditional products in other countries. Hence, this 2 March 2014 paper discusses the properties of characteristic food products, and outlines the steps critical for their Accepted 11 March 2014 safety. Such foods include fermented milk products (in particular cheeses), meat and ﬁsh products, Available online 21 March 2014 fermented vegetables, and baked goods such as sourdough breads and spiced cookies. Data analysed show, among others, that (1) hard cheeses made from raw milk are regarded as safe, due to effective Keywords: Traditional food hurdles which eliminate foodborne pathogens during production and ripening, and semi-hard cheeses e e German-speaking regions made from raw milk which are generally ripened for more than 60 days exhibit only a low health Food safety risk if Good Manufacturing Practice (including mastitis control) and effective HACCP systems (e.g. control Dairy products of starter activity) are implemented; (2) Listeria monocytogenes is not a hazard speciﬁc to products from Meat products raw milk since it may grow on the surface of smear- and mold ripened cheeses after recontamination, Plant products and can be effectively controlled by monitoring systems including environmental samples; (3) semi-dry and dry sausages have a favourable record of safety whereas, in the manufacture of some undried, spreadable types, salmonellae (especially in pork sausages) and Shiga toxin-producing Escherichia coli (STEC; especially in sausages containing meat from ruminants) are frequently reduced only by one log cycle or less. Hence, the safety of these products critically depends on the quality of the raw material. This stresses the need of implementing Good Manufacturing Practice also in traditional processes. Ó 2014 Elsevier Ltd. All rights reserved.

Contents

1. Introduction: region, population, culture ...... 218 2. Traditional foods in German-speaking regions and associated risks ...... 218 3. Dairy products ...... 218 3.1. Pathogenic bacteria ...... 219 3.1.1. Fermented milks ...... 220 3.1.2. Butter...... 220 3.1.3. Cheese...... 221 3.2. Mycotoxins ...... 222 3.3. Biogenic amines ...... 223 3.4. Safety management in small-scale production units ...... 223 4. Meat and poultry products ...... 223 4.1. Minced meat and other fresh processed products (not or only lightly salted) ...... 224 4.2. Fermented sausages ...... 224 4.3. Raw salted/cured meats ...... 225 4.4. Kochwurst ...... 226 5. Lightly salted and/or smoked fish products, ready-to-eat ...... 226

* Corresponding author. Tel.: þ49 661 9640 376; fax: þ49 661 9640 399. E-mail addresses: [email protected] (F.-K. Lücke), [email protected] (P. Zangerl). http://dx.doi.org/10.1016/j.foodcont.2014.03.014 0956-7135/Ó 2014 Elsevier Ltd. All rights reserved. 218 F.-K. Lücke, P. Zangerl / Food Control 43 (2014) 217e230

6. Vegetable products ...... 227 7. Cereals and baked goods ...... 227 8. Concluding remarks ...... 227 References ...... 228

1. Introduction: region, population, culture Epidemiological data are also useful in selection of traditional foods to be treated in more detail. Many types of beer, wine, non- This paper focuses on traditional food in the German-speaking alcoholic beverages and sweets have also a long tradition in region of Central Europe, namely, Germany, Austria, parts of German-speaking countries, with consumption figures higher than Switzerland, Liechtenstein, Belgium and Luxemburg, and the in comparable regions, but they have a good record of safety and are northernmost part of Italy (“Südtirol”). There are about 90 million not discussed further in this paper. Table 1 lists some outbreaks of “native speakers” in this region. Pork and poultry production is foodborne diseases from traditional foods in German-speaking highest in the North West while milk and beef production is highest regions during the last few years. It indicates that products of an- in the marshlands, in some areas of the “Mittelgebirge” and, in imal origin are most relevant. However, only outbreaks are listed particular, in the regions adjacent to or within the Alps. Viticulture that have been “verified”, i.e., for which a clear link between the is possible in regions with a favourable (micro-)climate, in the disease and a food was established. This is very difficult for family- south-west, as well as in the eastern part of Austria. The geographic scale outbreaks with only mild symptoms, and for agents with a heterogeneity is reflected in history: over centuries, the region was long incubation time (time between ingestion of contaminated an “empire” on paper only, with plenty of small counties and local food and onset of disease symptoms). Hence, an additional criterion rulers, belonging to different religious denominations (protestant is the presence of pathogens in ready-to-eat food. Some data from and catholic) and sometimes fighting against each other. The fed- the official monitoring of food in Germany in 2009 are compiled in eral structure of Germany, Austria and Switzerland, and the large Table 2 (Hartung & Käsbohrer, 2011). Data from other European numbers of cultural and economic centres is a result of this history. countries are published by the European Food Safety Authority (see Hence, it is not surprising that culinary habits differ, too. For EFSA & ECDC, 2014; for most recent data). example, there is a gradient in rye bread consumption over the Based on all these considerations, this Chapter will focus on the region (high in the northeast, low in the southwest), reflecting following traditional ready-to-eat foods: conditions and traditions for cropping rye. It may also be mentioned that, depending on the region, there are different words e Dairy products, in particular cheese for the same commodity or food (see e.g. König, 2007). e Meat products, in particular, - minced meat to be eaten raw - fermented sausages 2. Traditional foods in German-speaking regions and - raw hams associated risks - cooked, in particular, canned sausages of the Kochwurst type e Lightly salted and/or smoked fish products, ready-to-eat fi fi The considerations above illustrate the dif culties in de ning e Vegetable products, in particular sauerkraut, fermented cu- which foods are typical traditional foods in German-speaking cumbers (“Salzgurken”) and canned vegetables countries. One issue that may be perceived as common to e Bakery products different regions is the tradition of one hot meal a day, mostly during lunch time, and another “cold” meal, mostly in the evening. This is related to traditional life in villages with short distances 3. Dairy products between work (on farms or craftsmen’s shop) and home where the housewife prepared the meals. The historic results have been in In the Central European countries, manufacture of dairy prod- high consumption figures for bread, sausage and cheese, in addition ucts has a long history. Traditional milk products include butter, to the renowned regional diversity of these and other traditional, fermented milks, and a huge variety of cheeses, partly made of raw ready-to-eat foods. In fact, when Germans returning from some or thermised milk (milk that has undergone a heat treatment lower time abroad are asked what they missed most of all, a frequent than pasteurisation). In the Alpine regions, a significant amount of answer is “German-style bread”. the produced milk is manufactured in small-scale facilities Another criterion for identifying “traditional foods” may be the throughout the entire year. Additionally, milk and raw milk prod- DOOR list set up by the European Union for agricultural products ucts are produced from June to September on Alpine pastures at (available at http://ec.europa.eu/agriculture/quality/). This list is 1000 to 2500 m sea level. In the Alpine regions of Germany, Austria based on Regulation (EC) No 1151/2012 and the preceding Regu- and Switzerland, silage was not fed to dairy cows because lactate lations (EC) No 509/2006 and No 510/2006 (EC, 2012; EC 2006a, fermenting clostridia present in silage would cause late blowing of 2006b) with the categories “protected designation of origin”, traditional hard and semi-hard cheese, and use of preservatives is “protected geographical indication” and “traditional speciality prohibited for the manufacture of these products. Except guaranteed”. It contains (as of January 2014) 74 and 14 registered Switzerland, these feeding restrictions are limited to certain areas products from Germany and Austria, respectively (Switzerland is today. In regions or areas where silage and other fermentable feeds not a member of the European Union). Meat products and cheeses, are banned mainly trade-marked dairy products are manufactured beer, mineral waters, sweet goods such as “Lebkuchen” and some in small-scale plants and often protected by designation of origin unprocessed products from plants and animals make up the ma- (PDO). In recent years, dairy products made from goat’s and ewe’s jority of the entries. General principles on the manufacture and milk are of increasing commercial relevance, especially for small- composition of food stuffs including traditional foods are laid down scale enterprises and farmhouse milk processing businesses. Mi- in national regulations or guidelines e.g. the German Code of crobial hazards in milk products may arise from pathogenic bac- Practice or the Codex Alimentarius Austriacus. teria, mycotoxins and biogenic amines. F.-K. Lücke, P. Zangerl / Food Control 43 (2014) 217e230 219

Table 1 Veriﬁed outbreaks of foodborne diseases in Germany that were linked to traditional products.

Location/Scale Agenta Food incriminated (Probable) main faults Reference

Hotel guests, Germany S. Brandenburg Various sausages from Poor hygiene of staff and equipment RKI, 2004b own production Several households, S. Typhimurium Raw minced meat Not identified RKI, 2010 southern part of state Niedersachsen, Germany Germany (nationwide) S. Bovismorbificans Fresh sausage Fermentation too short BfR, 2009b; Gilsdorf et al. 2005 (Zwiebelmettwurst) Not specified S. Bovismorbificans Raw cured poultry Not identified BfR, 2009a Germany (nationwide); S. Panama Minisalami sticks, Unknown RKI, 2008 28 notified cases not smoked (children) Not specified S. Panama Fermented sausage Inappropriate cleaning of casings BfR, 2009b Germany, regional S. Panama Raw minced meat, Primary contamination of pigs, BfR, 2013 fresh raw sausages slaughtering/butchering hygiene Customers of local meat S. Goldcoast Fermented sausageb Inappropriate fermentation Bremer, Leitmeyer, Jensen, Metzel, processor, Germany (only 4 days) Meczulat, Weise, et al., 2004 Various households, S. Typhimurium Pork products Not identified Schmid, Hächler, Stephan, Switzerland Baumgartner, & Boubaker, 2008 Single private household (?), C. botulinum Raw smoked ham Inappropriate salting/curing process BfR, 2009a Germany Single private household (?), C. botulinum Raw smoked ham Inappropriate salting/curing process BfR, 2009b Germany Single private household, C. botulinum type E Herring in vinegar Marinating at room temperature in BfR, 2010 Germany household Single private household, C. botulinum Canned green beans Insufficient heat treatment, storage BfR, 2009a Germany without refrigeration Single private household, C. botulinum Canned blood sausage Poor butchery hygiene, no control RKI, 2004a Germany of heat treatment Single private household, C. botulinum Raw salted lamb, Temperature during salting too high RKI, 2003 Germany processed on farm Single private household, C. botulinum Smoked trout Insufficient refrigeration RKI, 1998 Germany Austria, Germany Listeria monocytogenes Acid curd cheese (“quargel”) Recontamination during Fretz et al., 2010 (mostly elderly) smearing the surface Not specified Trichinella spiralis Raw ham, raw sausage Unlawful slaughtering/processing BfR, 2009a (no meat inspection) Not specified Sacrosporidium Raw minced meat Not identified BfR, 2009a

a S., Salmonella; C., Clostridium. b Not veriﬁed by isolation of the agent from the sausage.

3.1. Pathogenic bacteria survive milk pasteurisation but during the milk fermentation process, survivors are usually unable to germinate or multiply during Pathogenic and enterotoxin producing bacteria of most signiﬁ- production, due to rapid decrease in pH. Their role is therefore cance to dairy products are Listeria monocytogenes, Staphylococcus limited to pasteurised milk and unfermented pasteurised ﬂavoured aureus, Salmonella spp., Shiga toxin-producing Escherichia coli milk drinks where, in the case of temperature abuse, abundant (STEC), and Campylobacter spp. Campylobacter is very susceptible to growth may lead to gastrointestinal symptoms. The role of Myco- unfavourable environmental conditions (e.g. pH, salt concentra- bacterium avium subsp. paratuberculosis (MAP) in the pathogenesis tion) and will be inactivated during milk fermentation (Whyte, of Crohn’s disease is still under discussion. O’Brien, Fanning, O’Mahony, & Murphy, 2011). Thus, outbreaks of Faecal contamination of milk during milking is the main source of campylobacteriosis are limited to raw milk and improper pasteur- foodborne pathogens in raw milk. Many pathogens including ized or recontaminated pasteurized milk. Spores of Bacillus cereus L. monocytogenes, Salmonella spp., STEC, Campylobacter spp., MAP,

Table 2 Contamination of minced meat and ready-to-eat food by Salmonella, STEC and Listeria monocytogenes in Germany (data from state monitoring program 2009; see Hartung & Käsbohrer, 2011). n.r., not reported.

Food Salmonella STEC L. monocytogenes

n % Positive n % Positive n % Positive % >100/g % >104/g

Total serovars 1/2, 4a

Minced meat 2540 1.97 936 3.74 1276 21.94 1.49 1.55 0 Heat-treated meats 3075 0.07 61 0 2572 2.57 0.08 0.09 0 Otherwise stabilized meats 4331 0.79 299 1.34 2403 13.69 0.29 0.52 0 Hot-smoked fish 577 0 12 (All fish products) 0 853 3.05 0 0.81 0 Cold-smoked or “gravad” fish 247 0 0 590 17.63 0.68 1.51 0 Otherwise stabilized fish 754 0 0 715 3.78 0.14 0.15 0 Soft cheese from raw milk 107 0 59 0 123 1.63 1.63 0.54 0 Other cheese from raw milk 265 0 110 1.82 307 0.65 n.r. 0 0 Cheese from pasteurised milk 984 0 176 0 3937 0.74 n.r. 0.04 0 220 F.-K. Lücke, P. Zangerl / Food Control 43 (2014) 217e230

S. aureus and B. cereus are frequently found in faecal material and Table 4 may be widely disseminated in the farm environment. Spore for- Overview of fermented milk products produced in Germany, Switzerland and Austria grouped according to starter culture. mers (Bacillus spp., Clostridium spp.) may find their way into the milk as well by contaminationwith soil and bedding material. Improperly Mesophilic LAB Thermophilic LAB LAB and yeasts acidified silage is an important reservoir for Listeria. According to Sour milk Yoghurt Kefir Sanaa, Audurier, Poutrel, Menard, and Serieys (1996), the risk of Cultured buttermilka Yoghurt mildc Kefir mildd b contamination of raw milk increases with poor quality of silage and Natural (true) buttermilk Acidophilus milk fi insufficient housing and milking hygiene. Thus, the low incidence of Cultured cream (min. 10% fat) Bi dus milk Crème fraîche (min. 30% fat) Probiotics L. monocytogenes in three studies conducted in Switzerland and a Austria summarized in Table 3 (zero and 0.4% positive samples out of Made from pasteurised skim milk. b Released during the manufacture of ripened cream butter. a total of 4897 analysed samples, respectively) may be explained by c Yogurt of which Lactobacillus delbrueckii subsp. bulgaricus is replaced by any the feeding restrictions in the areas under study (ban of silage and Lactobacillus species according to Codex Standard for fermented milks CODEX STAN other fermentable feeds). Usually faecal contaminations result in 243-2003. d only low levels of pathogens in the milk, e.g. numbers of Kefir without lactose-fermenting yeasts according to Codex Alimentarius Aus- L. monocytogenes in positive milk samples generally do not exceed triacus for fermented milks. 10 cfu/ml (Ryser, 1999a). Mastitis caused by L. monocytogenes and Campylobacter spp. occurs only sporadically but if it does, high Leuconostoc spp.) were most common. Typical products are “Dick- 4 counts of approximately 10 cfu/ml are excreted into the milk (Sanaa milch” (from whole milk) and cultured cream (>10% fat; “Schmand” et al., 1996; Teufel, 2003). Acute salmonellosis in cattle may lead to usually with about 24% fat). Nowadays, yoghurts have the biggest shedding of Salmonella with the milk in a magnitude ranging from market share. However, most of the yoghurts are “mild” (Lactoba- 5 few hundred up to 10 bacteria/ml (Poppe, 2011). cillus delbrueckii ssp. bulgaricus (at least partially) replaced by other Although pathogenic bacteria are frequently found in faeces, thermophilic lactobacilli) and mixed with fruit preparations. Like- contamination of bulk tank milk with foodborne pathogens is rare wise, “mild” variants of “kefir” predominate in which lactose fer- fi (Table 3). The infrequent ndings of Salmonella spp., Campylobacter menting yeasts and consequently alcoholic fermentation are low or spp. and STEC in raw milk suggest good milking practice but also absent. show that the occasional occurrence of pathogens in raw milk Fermented milks are considered as safe because the raw milk is cannot be excluded. The high level of hygiene in milk production is heated at high temperatures of more than 85 C. If recontamination also supported by studies of an Irish-Belgian working group which occurs during manufacture, bacteria are rapidly inactivated due to found that bovine faeces are not an important source of contami- the low pH (3.9e4.6) and the bactericidal effect of organic acids nation of raw milk with coliforms and enterococci (Kagkli, (predominantly lactic acid) and, possibly, other inhibitory com- Vancanneyt, Vandamme, Hill, & Cogan, 2007). pounds produced by the lactic starter cultures. Except MAP, vegetative cells of pathogenic bacteria are completely destroyed by standard pasteurisation processes. How- 3.1.2. Butter ever, in spite of milk pasteurisation, outbreaks may occur due to The manufacturing process of butter in German-speaking re- recontamination when personal and plant hygiene is inadequate. gions is similar to that in other regions. Traditionally, ripened cream Consequently, pasteurisation cannot guarantee a save product. butter was manufactured by fermentation of cream with specific mesophilic starter bacteria before churning, resulting in pH values 3.1.1. Fermented milks of 5.1 or lower. To date, this process is still practised in small-scale In Germany, Austria and Switzerland a variety of dairy products establishments. However, on industrial scale, ripened cream butter are produced by fermentation of milk or cream without subsequent is commonly manufactured from sweet cream butter by adding removal of the whey (Table 4). The flavour and texture of these fer- culture concentrates and permeates during working at the correct mented milks are mainly determined by the species and strain of rate, to yield the characteristics of normal ripened cream butter lactic acid bacteria (LAB) used. Traditionally, buttermilk and semi- made by the traditional process. Butter can be regarded as safe solid products made with mesophilic LAB (Lactococcus lactis, because of the small size (10 mm) of the water droplets. Other

Table 3 Prevalence of pathogenic bacteria in herd milk samples of Germany (D), Switzerland (CH) and Austria (AT).

Species Country n Positive (%) Reference

L. monocytogenes CH 4386 16 (0.4) Bachmann and Spahr (1995) CH 310 0 Stephan and Bühler (2002) AT 201 0 Eliskases-Lechner and Ginzinger (1999) AT 30 1 (3.3) Much et al., 2011 D 635 10 (1.6) Hartung & Käsbohrer, 2011 Salmonella spp. CH 456 0 Bachmann & Spahr, 1995 CH 310 0 Stephan & Bühler, 2002 AT 201 0 Eliskases-Lechner & Ginzinger, 1999 D 719 0 Hartung & Käsbohrer, 2011 Campylobacter spp. CH 496 0 Bachmann & Spahr, 1995 CH 310 0 Stephan & Bühler, 2002 AT 55 0 Much et al., 2011 D 209 1 (0.5) Messelhäusser, Beck, Gallien, Schalch, & Busch, 2008 D 714 8 (1.1) Hartung & Käsbohrer, 2011 STEC CH 110 7 (6.4) Svoboda, Gautsch, & Lüthi, 1998 D 209 0 Messelhäusser et al., 2008 D 675 12 (1.8) Hartung & Käsbohrer, 2011 AT 27 0 Much et al., 2011 Viable MAP CH 232 0 Hummerjohann, Ulmann, & Schällibaum, 2008 F.-K. Lücke, P. Zangerl / Food Control 43 (2014) 217e230 221 factors include the high temperatures used for pasteurisation, and The cheeses are ripened by the action of yeasts present in the curd, e in the case of ripened cream butter e the low pH value. However, and of red-smear microflora in some varieties, sometimes in an outbreak in Finland in 1998/1999 (cited by Bell & Kyriakides, conjunction with moulds (Bockelmann & Heller, 2004). 2005) showed that inadequate sanitation procedures may lead to Intrinsic, extrinsic and processing factors differ considerably in contamination of the processing environment and equipment with the cheeses shown in Table 5. While fresh cheeses show a pH of less Listeria and may cause diseases by products normally considered as than 5, pH may rise during the manufacture of smear and/or mould safe. ripened cheeses to more than 7 at the cheese surface due to oxidation of lactic acid by yeasts and moulds and production of ammonia by the proteolytic activity of the red-smear bacteria. In 3.1.3. Cheese soft cheeses, a considerable increase of pH is also observed in the An overview of cheeses produced in Germany, Switzerland and core of the cheese. This is due to their small size and high water Austria is given in Table 5. Regardless of origin, these cheeses are activity which favours abundant microbial growth. Cheese milk is often now also produced in neighbouring countries, e.g. Emmental normally pasteurized, but raw milk is frequently used for the cheese is produced not only in Switzerland but also in Austria manufacture of hard and semi-hard cheeses with ripening times of (Austrian Emmentaler) and Germany (Allgäuer Emmentaler). several months. Such long-ripened cheeses reveal a more intensive Quarg (“Quark”) may be considered as a fresh cheese typical for flavour than the same cheeses made from pasteurised milk. In Central Europe. Many of the traditional ripened cheeses are “smear- small-scale establishments and farmhouse facilities, thermised ripened”. These cheeses are also called washed-rind cheeses because milk is often used for the production of semi-hard cheeses. the surface is washed with water (“smear water”) containing salt and Outbreaks associated with cheese are primarily attributed to ripening cultures (if necessary). This leads to the development of a L. monocytogenes, Salmonella spp., STEC and staphylococcal red-orange to brown smear during ripening. These cheeses are enterotoxin. The primary reasons for cheese-related outbreaks characterised by a complex surface microbiota consisting initially of include poor starter activity, poor hygiene in the plant, environ- yeasts and ultimately of salt-tolerant bacteria (particularly co- mental contamination, and/or faulty pasteurisation (Fox, Guinee, ryneforms). The microbiota originates primarily from the environ- Cogan, & McSweeney, 2000). Recently an outbreak of invasive ment e.g. smear water, brine, utensils, personnel, and there is poor listeriosis with 34 cases including 8 fatalities occurred in 2009e control of their composition. Traditionally young cheeses are 2010 in Germany, Austria and the Czech Republic (Fretz et al., 2010). smeared with the same smear water used previously to smear older The vehicle of transmission could be traced to Austrian Quargel, a cheeses, in order to encourage rapid development of the desired smear-ripened acid-curd cheese made from pasteurised milk. The microflora. To reduce the risk of L. monocytogenes being established outbreak showed that listeriae are still difficult to control in dairy on the cheese surface, the use of defined-strain smear starters as an plants. The ubiquitous organisms may find their way easily into the alternative to old smear increased significantly in the last years. To production and ripening rooms of dairy plants when preventive date, ripening cultures of the yeasts Debaryomyces hansenii and measures are inadequate or absent. During ripening of white- Geotrichum candidum and of the bacteria Brevibacterium linens/ mould and red-smear cheeses listeriae contaminating the cheese B. aurantiacum, Staphylococcus equorum, Staphylococcus xylosus, surface are able to multiply. Particularly in soft cheeses (high pH Microbacterium gubbeenense and Corynebacterium casei are 8 and aw) high densities (up to 10 cfu/g at cheese surface) are to be commercially available (Bockelmann, Willems, Neve, & Heller, 2005). expected. Although in blue cheeses the pH in the interior is also Ripened acid curd cheeses have a long tradition and are of regional increasing and favourable to growth, Listeria dies off during importance, especially in the “Mittelgebirge” region of Germany ripening, possibly due to the high level of salt (z10% salt-in- (“Harzer Käse”) and the alpine regions of Austria and Switzerland moisture) (Fox, Guinee, Cogan, & McSweeney, 2000) and the for- (e.g. “Graukäse”, “Ploderkäse”). They differ considerably in their mation of listeriostatic/listeriocidal free fatty acids and listeriocins appearance and weight but they have in common that they are pro- produced by Penicillium roqueforti (Ryser, 1999b). duced from a coagulum (“Trockenquark”) obtained by acidification of Surveys conducted in Germany, Austria and Switzerland skim milk without rennet addition and adjusted to >30% dry matter. generally found less than 2% of the cheese samples positive for L. monocytogenes (Bruhn, 2007; Hahn, Walte, Coenen, & Teufel, Table 5 1999; Hartung & Käsbohrer, 2011; Much, Salgado-Voss, Pichler, Overview of cheese varieties produced in Germany (D), Switzerland (CH) and Austria Rendi-Wagner, & Herzog, 2011). Similar low levels were observed (AT) (country of origin in parenthesis). by Fox et al. (2000) who analysed 1437 cheese samples originating Hard cheeses Soft cheeses from several European countries with a prevalence of 1.4%, 0.5% and Emmentaler (CH) Münster (D)a 1.4% for raw milk cheeses, pasteurised milk cheeses and unlabelled Gruyère (CH, F)a Romadur (D)a cheeses, respectively. However, in red smear cheeses the preva- a a Bergkäse (AT, CH, D) Limburger (D) lence is expected to be higher (Rudolf & Scherer, 2001). Further, the Sbrinz (CH) Vacherin Mont d0Or (CH)a Semi-hard cheeses White surface-mould cheeses authors found that more of the L. monocytogenes-positive cheeses (e.g. Camembert) were made from pasteurised milk (8%) compared to 4.8% of the raw Tête de Moine (CH)a Cambozola (D)b milk cheeses. Frequently contamination with L. monocytogenes was a Appenzeller (CH) Ripened acid curd cheeses found in the latter processing steps of cheese manufacture, i.e. after Raclette (CH, F)a Quargel (CZ, D, AT)a brining or during ripening (Wagner, Eliskases-Lechner, Rieck, Hein, Tilsiter (D, CH)a Harzer, Mainzer (D)a Butterkäse (D) Sauerkäse, Graukäse (AT) & Allerberger, 2006). This suggests that production hygiene in the Dutch-type cheeses Ploderkäse (Bloderkäse) (CH) processing plant determines primarily the risk of cheese contami- (e.g. Edam, Gouda) nation. The more frequent incidence of contaminated raw milk Blue-veined cheeses Fresh cheeses (unripened cheeses) cheeses in some studies (e. g. Loncarevic, Danielsson-Tham, & Cottage cheese Cream cheese Tham, 1995) may be explained by the fact that raw milk cheeses are Quarg (Quark) mostly produced in small-scale and farmhouse facilities that may not recognise and prevent L. monocytogenes contamination at the a smear-ripened cheese. b fi amalgamation of blue-veined (Gorgonzola) and white surface-mould cheese same ef ciency as large-scale plants producing pasteurised milk (Camembert). cheeses. 222 F.-K. Lücke, P. Zangerl / Food Control 43 (2014) 217e230

Salmonella spp. was not detected in surveys conducted in Ger- 4.5 many and Switzerland (Hahn et al., 1999; Hartung & Käsbohrer

2011; Lutz, Jost, & Overesch, 2010). STEC have been found in 4.0 about 1e2% of cheeses made from raw milk but rarely in cheeses including raw milk cheeses (Hahn et al., 1999; Hartung & Käsbohrer, 2011; Stephan et al., 2008). Although no viable MAP 3.5 S. aureus S. were detected in 143 raw milk cheese samples by Stephan,

Schumacher, Tasara, and Grant (2007), it cannot be excluded that 3.0

MAP are ingested during cheese consumption since the authors log increase detected MAP DNA by real-time PCR in 4.2% of the samples. 2.5 In cheeses made from pasteurised milk, S. aureus occurs only sporadically whereas raw milk cheeses are more frequently log increase S. aureus = log cfu/g cheese after brining - log cfu/ml vat milk contaminated. Surveys conducted in Germany and Austria showed 2.0 e 4 5.8 5.9 6 6.1 6.2 6.3 6.4 6.5 6.6 that 3% 46% of raw milk cheese samples exceeded 10 coagulase- pH of cheese 2 h after moulding positive staphylococci/g (Zangerl & Ginzinger, 2001). A high risk of staphylococcal food poising is to be expected when counts of > Fig. 1. Relationship between starter activity (pH of cheese 2 h after moulding) and 106 S. aureus/g are reached, as a consequence of contamination of increase in S. aureus counts during the first 30 h of cheese production. From Zangerl, P. 2007. Mikrobiologie der Produkte. In Kurzes Lehrbuch Milchkunde und Milchhygiene raw milk by mastitic milk and poor acidification during the first edited by V. Krömker, pp. 156e179. Stuttgart, Parey. ÓThieme, Stuttgart; reprinted with hours of cheese manufacture. Data of the French surveillance sys- permission. tem showed that from 1992 to 1997, S. aureus was by far the most frequent pathogen associated with outbreaks due to milk and milk products (85.5% of the 69 outbreaks). Of the 59 outbreaks of dairy Naturally contaminated milk with an indigenous flora of 100e200 associated staphylococcal intoxication, 53 (90%) were traced to coagulase-positive staphylococci/ml was used for the experiments. 6 cheese (with 28 raw milk cheeses and 25 cheeses made from un- Despite these relatively low counts in milk, high counts of >10 cfu/ specified milk involved) (De Buyser, Dufour, Maire, & Lafarge, g were observed in cheeses at insufficient starter activity, with the 2001). Staphylococcal food poisoning is caused by a number of risk of formation of staphylococcal enterotoxins. Thus measure- enterotoxins which are produced in contaminated food, predomi- ment of cheese pH 2 h after moulding estimates the rapidity of acid nantly by S. aureus strains. However, S. aureus is also considered the development and must be regarded as a Critical Control Point (CCP) most significant cause of mastitis not only in cows but also in sheep in the HACCP system of raw milk cheese production. and goats, and is therefore probably present in most raw milks. Hard cheeses originating from the Alpine regions of Germany, When the udder is infected, S. aureus is excreted into the milk in Austria and Switzerland are usually produced from raw milk. For variable numbers, a level of 104 cfu/ml being common (Tolle, 1980). the production of these cheeses, the curds-whey mixture is heated Hence, mastitis strains in the raw milk are the main reservoir of to temperatures as high as 50e57 C to promote syneresis, a pro- enterotoxigenic staphylococci in cheeses made from raw milk. The cess referred to as scalding or cooking. These cooking temperatures frequency of enterotoxigenic strains is highly variable. In an Aus- are more detrimental to pathogenic bacteria than to the thermo- trian study (Gonano, Hein, Zangerl, Rammelmayr, & Wagner, 2009), philic starter culture, so most pathogens are inactivated in the first only 9.9% of the strains derived from quarter milk samples of 24 h of production due to rapid acid production and the high mastitis cows (n ¼ 91) and 12.6% of the strains originating from raw cooking temperatures used (Bachmann & Spahr, 1995). In addition, bulk/vat milk and raw milk cheeses (n ¼ 247) made from cow’s milk the combination of low pH, low water activity and long ripening were able to produce the classical enterotoxins staphylococcal time of several months inactivate pathogenic bacteria. Hence, long enterotoxin A (SEA) to SED with SEC predominating. None of the ripened hard cheeses made from raw milk have a good safety re- strains produced SEE (when assayed by an ELISA-based method). cord. Even semi-hard cheeses made from raw milk represent only a Unlike Mycobacterium bovis, MAP, Brucella abortus and minor health risk if they are made properly and mastitis control Campylobacter spp., the most foodborne pathogens are able to programs are implemented. In general, if conditions for growth are multiply during the first steps of cheese manufacture (Fox et al., unfavourable to microorganisms, the decline in numbers during 2000). During cheesemaking, microorganisms in milk are physi- ripening is higher when higher ripening temperatures are applied cally concentrated approximately 10-fold in the curd due to (Bachmann & Spahr, 1995; Zangerl & Ginzinger, 2001). On smear- entrapment within the curd particles. Further, the organisms are ripened semi-hard cheeses, listeriae may multiply on the surface able to proliferate in the vat and particularly during pressing/ during ripening, so the rind of these cheeses should not be moulding, until the acids produced by the starters inhibit further consumed. On the other hand, foodborne pathogens contaminating growth. Growth rates are strongly dependent on the decrease of pH the surface of soft cheeses are able to proliferate during ripening, during the first hours of cheese manufacture i.e. the amount, ac- due to the rapid increase in pH and the high water activity, and tivity and type of starters used. Cheese making trials showed that growth is favoured at higher ripening temperatures. Thus, for the an increase in S. aureus-counts by 1.5e3 logs during the first 24 h of manufacture of soft cheeses made from raw milk, high milk quality, cheesemaking may be expected under normal conditions, but in use of fast acid-producing starters and a high level of plant and cheeses with suboptimal acidification increases up to 5 log cycles personal hygiene with effective Hazard Analysis Critical Control have been observed (Zangerl & Ginzinger, 2001). Other pathogens Point (HACCP) procedures are necessary to reduce health risks for capable to multiply during cheesemaking probably behave similar. consumers. Nevertheless, such cheeses should not be served to Low acidification is caused by insufficient starter development due vulnerable groups. to inhibition of LAB by antibiotic residues in milk or by bacterio- phage infection, but the acidification rate is also lowered when 3.2. Mycotoxins inadequate starter inocula are used or the starters lost activity due to prolonged storage. Fig. 1 shows that the increase in counts of Mycotoxin formation caused by unintentional fungal growth on S. aureus is directly correlated to starter activity, measured by pH of the surface of dairy products, in particular of cheese, may represent cheese 2 h after moulding (correlation coefficient r ¼ 0.84). a health risk. However, most studies reported the overall incidence F.-K. Lücke, P. Zangerl / Food Control 43 (2014) 217e230 223 of mycotoxins in unintentional mouldy cheeses to be low 4. Meat and poultry products (Sørhough, 2011). If mould growth occurred, toxin migration from the cheese surface into the interior was generally found to be not The main categories for meat products are (a) fresh processed more than 2 cm (Sørhough, 2011), so in hard and semi-hard cheeses meat products, (b) cured meat pieces (raw or cooked), (c) contaminated with a patch of mould, the cheese can be “salvaged” comminuted and subsequently cooked products, (d) raw- by removing the infested portion to a depth of 2e4 cm. Some fermented sausages, and (e) dried meats (Heinz & Hautzinger, traditional cheese varieties such as “Graukäse” may develop an 2007). A similar system is found in the German Code of Practice adventitious mould flora on the cheese surface. In this case a (“Leitsätze”; Anonymous, 2010). The category “cured meat mycotoxin monitoring is strongly recommended. pieces” include cooked (“Kochpökelwaren”) and raw salted/cured meats (“Rohpökelwaren”). The comminuted and cooked products 3.3. Biogenic amines include “Brühwurst” and “Kochwurst”. “Brühwurst” products (often referred to as “bologna-type” or “frankfurter-type” sau- Long ripened cheese have been incriminated in outbreaks of sages) are made from raw meat and fat and owe their charac- biogenic amine poisoning. Analyses of 410 ripened cheese samples teristics to the gel-forming ability of muscle proteins (Allais, between 1997 and 2003 revealed amounts ranging from <1 mg/kg 2010). Therefore, the process involves comminution of refriger- up to 1046 mg/kg histamine, 1023 mg/kg tyramine, 1024 mg/kg ated raw materials in a high-performance cutter. Accordingly, cadaverine, 467 mg/kg putrescine and 548 mg/kg phenylethyl- Brühwurst products have a shorter tradition in Germany, and amine, with a total biogenic amine content of up to 2640 mg/kg comparable products are manufactured in many other countries. (Federal Institute for Alpine Dairying, Jenbach, Austria, unpub- On the other hand, “Kochwurst” products (“pre-cooked” or “hot- lished results). In a recent study where 58 samples of European emulsions” according to Heinz & Hautzinger, 2007; Allais, 2010; cheeses from retail in Austria were analysed, 13.8% and 22.4% of respectively) are made from pre-cooked meat and fat tissues. the samples exceeded 100 mg histamine and 100 mg tyramine per Their manufacture has been the traditional way to utilize and kg, respectively (Mayer, Fiechter, & Fischer, 2010). However, most preserve lower-grade animal tissues and edible by-products in of the cheeses studied contain less than 10 mg amines/kg and Central Europe. Therefore, Kochwurst products are considered in increased amounts are exceptions (Maijala & Eerola, 2003). In old more detail in this paper. aged hard (12 months) and semi-hard cheeses (3e6 months), the The German Code of Practice defines “Bratwurst” (sausages to levels of biogenic amines may be considerably higher but not be fried) as another category of meat products since consumers in usually exceeding 500 mg amines/kg (Wechsler, Walther, Jakob, & different regions have different expectations. Bratwurst can be sold Winkler, 2009). The most important factor in preventing high to the final consumer as semi-processed (raw) sausages, as Brüh- levels of biogenic amines in raw milk cheese is minimising the wurst-type, Kochwurst-type or as fermented sausage. presence and activity of amino acid decarboxylating bacteria in In the years 2008e2012, meat and poultry products accounted milk and cheese. This can be achieved by good quality of raw milk for about 22% of the verified outbreaks of foodborne diseases in and maintaining high hygienic standards during the Germany (BfR, 2013). About 30e40% of these outbreaks could be manufacturing process. Obviously starter cultures lacking decar- linked to the consumption of raw minced meat, with Salmonella boxylase activity should be used. being the agent in most of these outbreaks. Fermented sausages (with very short ripening time) were incriminated in 6 outbreaks of 3.4. Safety management in small-scale production units salmonellosis. Two outbreaks of botulism could be traced to the consumption of raw salted/cured meats. In earlier years, outbreaks Traditional dairy products (butter, fermented milks and of botulism due to home-canned Kochwurst have also been cheeses) are sometimes made with raw milk in small-scale plants described (see Lücke & Roberts, 1993, for review; RKI, 2004a). and farmhouse processing units. In Alpine regions, manufacture of No meat-borne outbreaks of listeriosis or enteritis caused by raw milk cheeses on Alpine pastures is widely practised during the Shiga toxin-producing E. coli (STEC) or Campylobacter strains have summer months. Due to topographic conditions existing in been verified in the last years in Germany. However, this may be mountain areas and prevalent small-scale production units, milk is due to inherent difficulties to link these diseases to defined foods transported only over short distances every day. Generally milk is and thus providing “strong” or not even “weak evidence” for these processed within 15e18 h. Other factors also reduce microbiolog- links, according to the criteria set up by the European Food Safety ical risks: For example, in farmhouse establishments, milk pro- Authority (EFSA). Data from France (see De Valk et al., 2005) clearly duction and milk processing often fall under the same set of indicate that cooked and subsequently recontaminated ready-to- responsibilities. Hard cheeses made from raw milk have a good eat meats did cause listeriosis. For the control of L. monocytogenes safety record due to effective hurdles which eliminate foodborne in ready-to-eat meats, recontamination after cooking must be pathogens during production and ripening. Also semi-hard cheeses avoided, as well as extended storage, even though there is much made from raw milk e which are generally ripened for more than pressure from retailers to extend the “best-before date”. Measures 60 days e exhibit only a low health risk if Good Manufacturing to prevent these outbreaks are not specific to traditional food in Practice and effective HACCP systems are implemented. L. mono- Central Europe. cytogenes can be effectively controlled by monitoring systems Chemical hazards may be generated if excessive dry heat is used including environmental samples which have been implemented for cooking meat products. It is uncommon to cook cured and fer- for years. Application of “surface cultures” antagonistic against mented meats in this way, and Bratwurst is usually made without L. monocytogenes may further reduce the risk of growth of this or- added nitrite. There is no evidence that Central European con- ganisms on smear-ripened cheeses. In recent years buildings, ser- sumers are exposed to levels of nitrosamines higher than in other vices and equipment of Alpine pasture establishments improved countries. An additional exposure to polycyclic aromatic hydro- significantly. However, efforts are still necessary with regard to carbons may result from poor barbecuing practice, if fat from mastitis control and control of starter activity during production to Bratwurst burns after dropping onto the hot charcoal. Some heavily improve food safety. Further, HACCP training should be provided smoked traditional raw meats (“Schwarzgeräuchertes” in some and promoted among small-scale dairy plants, as well as Alpine parts of Bavaria) may also contain elevated levels of polycyclic ar- pasture and farmhouse establishments. omatic hydrocarbons. However, if no soot is deposited on the 224 F.-K. Lücke, P. Zangerl / Food Control 43 (2014) 217e230 surface, exceeding 5 mg benzo(a)pyrene/kg, the maximum level premium-type dry sausages. The water activity of fresh and/or permitted by Regulation (EC) No 1881/2006 (EC, 2006c), is unlikely. spreadable sausages is about 0.94e0.96. These sausages must be The Chapter on meat will focus on the safety of minced meat and stored at 7 C or below. Semi-dry sausages have water activity meat preparations eaten raw, fermented sausages, raw hams, and values of 0.90e0.94 and should be stored at 15 C or below while Kochwurst type sausages. dry sausages (stable at ambient temperature if mould growth is prevented) have water activity values of below 0.90. Under these 4.1. Minced meat and other fresh processed products (not or only circumstances, the shelf life of the products is normally limited by lightly salted) fat deterioration. Products ripened by surface growth of fungi are unusual in Germany but common in Switzerland. These are similar Minced meat may contain various agents of foodborne diseases, to Mediterranean-style products and are not discussed in detail albeit at low levels. In Germany, about 3% of minced (red) meat here. While nowadays, most sausages are fermented at 20e25 C samples investigated were found positive for Salmonella and/or and aged at about 15 C once the pH decreased to below 5.3, STEC (Hartung & Käsbohrer, 2011; see also Table 2). Protozoa such traditional sausages and some local specialities (e.g. “air-dried” as Sarcosporidium and Toxoplasma should also be included in the sausages common in Central Germany; see Lücke & Vogeley, 2012) list of hazards. There is neither a societally accepted nor feasible are ripened at 15 C or below. Small manufacturers often use an air- way to completely prevent the presence of STEC, Campylobacter and conditioned chamber for fermentation and smoking and an “ageing Salmonella in raw minced meats. Moreover, especially in Northern room” for drying. The walls of such rooms (“Wurstkammer”)have and Central Germany, it is common to eat minced red meat (“Mett”) been traditionally layered with loam capable of absorbing and from pork (e.g. “Thüringer Mett” containing spices, some salt and releasing moisture, thus allowing some control of relative sometimes onions) or beef (“Tatar”) without prior cooking. In the humidity. Netherlands, a nationwide outbreak of STEC infection has been Hazards of relevance to German-type fermented sausages are linked to the consumption of raw minced beef (“steak tartare”; listed in Table 6. Due to a well-functioning inspection system e Greenland et al., 2009). Moreover, there is strong evidence that even for animals slaughtered on farm, the presence of Trichinella consumption of raw minced meat by small children accounts for and other multicellular parasites in raw sausages is extremely un- most of the infections by Yersinia enterocolitica (Rosner, Stark, likely, and the few cases of parasitosis reported could be traced back Hohle, & Werber, 2012). Because of this situation, Germany used to unlawful slaughtering. Toxoplasma gondii may be present in raw to have very strict and detailed regulations about handling and pork but even in fresh raw sausages with very short ripening times, selling minced meat (Minced Meat Regulation or “Hack- the risk of survival of this organism is very small (Pott et al. 2012). fleischverordnung”). The subsequent regulations of the European To assess the risk of infections after consumption of raw sausages, Union (Regulation (EC) No 853/2004, Annex III Section V; EC, 2004) growth potential and inactivation rate of the bacterial agents must and on the national levels also contain specific rules for these types be considered, namely, of salmonellae, Shiga toxin-producing E. coli of products, albeit in less detail. To minimize the risk, it remains (STEC), and L. monocytogenes. Salmonellae may grow early in advisable that meat to be eaten raw should be minced only on the fermentation in the 20e25 C range before the pH is lowered to day of consumption, and not served to risk groups such as pregnant about 5.3. Addition of about 100 mg sodium nitrite per kg inhibits women, small children, elderly and immuno-compromised this growth (Kabisch, Scheuer, Rödel, & Gareis, 2008; Sirviö, Nurmi, persons. Puolanne, & Niinivaara, 1977). This effect of nitrite can be replaced by lowering the fermentation temperature. Hence, traditional 4.2. Fermented sausages sausages manufactured with nitrate, as well as sausages without curing agents (in particular, from organic production) are generally The annual consumption figure of fermented sausages in fermented at temperatures below 18 C. There is little if any growth German-speaking regions in 2008 was about 5.5 kg per capita (DFV, of STEC and L. monocytogenes during sausage fermentation. 2011), probably the highest consumption worldwide. Hams ac- Table 7 (see also Lücke, 2000a; Skandamis & Nychas, 2007; for count for 5.1 kg of which raw hams account for approx. 3 kg. The reviews) shows data on inactivation of salmonellae, E. coli and German Code of Practice (“Leitsätze”; Anonymous, 2010) distin- L. monocytogenes during ripening of German-type sausages. As a guishes 16 varieties of sliceable and 5 varieties of spreadable fer- “rule-of-thumb”, it may be stated that the common production mented sausages. Criteria for subdivision (see Lücke, 2000a; process of semi-dry sausages reduces the level of these bacteria by Ockerman & Basu, 2007)are about 2 log cycles during ripening while in undried, spreadable sausages (making up about 20% of the consumption of raw sausages e the raw material (pork, beef, mutton, poultry and mixtures of in Germany), one decimal reduction or less is achieved. The risk of these; amount and type of fatty tissue) pathogen survival is lower if the products are aged and/or stored for e the degree of comminution extended periods, and at high levels of acids and salt (Heir et al., e the diameter of the casing 2010; Rödel & Scheuer, 2006). Storing semi-dry or dry sausages at e the rate and extent of acid formation and decrease of pH (as refrigeration slows down the inactivation rate (Faith et al., 1998; influenced by the addition of sugar and lactic acid bacteria, and Lindqvist & Lindblad, 2009; Nissen & Holck, 1998). Outbreaks of by fermentation temperature) salmonellosis due to minisalami sticks (Cowden, O’Mahony, e the ripening time and the final water activity (as influenced by Bartlett, Rana, Smyth, Lynch, et al., 1989; Gareis, Kabisch, Pichner, temperature and humidity in the ripening chamber) & Hechelmann, 2010a, 2010b) indicates that salmonellae may sur- e the treatment of the surface (smoking, mould growth or none). vive on dry sausages for considerable periods. By appropriate combination of various “hurdles”, a reduction of In principle, muscle and fatty tissues are chilled, comminuted, bacterial infectious agents by 3e4 log cycles may be feasible with mixed with salt, curing agents, sugars, spices, and, in most cases, semi-dry or dry products but not with spreadable sausages (see e.g. starter cultures. The mix is then filled in casings (without air in- Kofoth, Rödel, & Gareis, 1998; Stiebing, Vogt, Baumgart, & Putzfeld, clusion), fermented and aged. The total ripening time 2000, Stiebing, Vogt, Baumgart, Putzfeld, & Bergt, 2000). Use of (fermentation þ ageing, i.e. from stuffing until shipment) can be appropriate bacteriocin-forming starter cultures may reduce the between 2 days for “fresh sausages” and several months for level of L. monocytogenes by 1e2 log cycles (see Lücke, 2000b; Lahti, F.-K. Lücke, P. Zangerl / Food Control 43 (2014) 217e230 225

Table 6 Hazards relevant to German-style fermented sausages.

Johansson, Honkanen-Buzalski, Hill, & Nurmi, 2001) but bacterio- unsmoked salami where abundant growth of fungal starter on the cins have little if any effects on Gram-negative bacteria. A 5 log surface raised the pH value before the product was sufficiently dry reduction of STEC (as originally stipulated by the US Food Safety (Hechelmann, Lücke, & Leistner, 1988). and Inspection Service; see Adams & Mitchell, 2002) is not gener- Biogenic amines may be formed during sausage ripening if ally achieved by using the present production processes, and proteolysis liberates free amino acids and bacteria with amino acid products subjected to a final heat treatment, as suggested in the decarboxylase activity multiply. Vidal-Carou, Veciana-Nogués, United States, will not be accepted by European consumers. On the Latorre-Moratala, and Bover-Cid (2007) compiled data on the other hand, outbreaks of STEC infections have been reported in levels of various biogenic amines in fermented sausages in retail. Norway and Sweden and traced to commercially prepared semi- Concentrations vary over a wide range, even within an individual dry sausages. The incriminated sausages were produced with category of product. In Finnish dry sausages (comparable to contaminated mutton (Sekse et al., 2009) and beef (Sartz et al. German-style products), tyramine concentrations ranged from 3 to 2008), respectively. In Germany, Teewurst prepared from beef 310 mg/kg, and for histamine, from 0 to 200 mg/kg (Eerola, Roig was suspected e but not verified according to the EFSA criteria e to Sagués, & Hirvi, 1998). The use of fresh meat is important to limit be the vehicle of an outbreak of STEC infection in Bavaria (Ammon, proteolysis by endogenous enzymes and the activity of acid sensi- Petersen, & Karch, 1999; Werber et al., 2007). It may be concluded tive decarboxylase-positive microorganisms such as certain Enter- that avoiding contamination of beef and mutton with animal faeces obacteriaceae and enterococci, where suitable starter cultures may is crucial for the safe production of spreadable and semi-dry fer- help to suppress decarboxylase-positive lactic acid bacteria mented sausages. (Paulsen & Bauer, 1997). S. aureus may grow during sausage fermentation if acid formation is slow and fermentation temperature too high. In German- 4.3. Raw salted/cured meats type sausages, the organism is well under control by using low fermentation temperatures (in traditional processes) and/or lactic In Germany, almost all raw salted/cured meats are prepared acid bacteria as starters. One outbreak of intoxication was linked to from pork muscles while in Switzerland, salted/cured beef such as

Table 7 Pathogen reduction in German-type semi-dry fermented sausage (fermented at 20e24 C with starter cultures; pH 5.2 or below after fermentation; ageing at 15e18 C; no mould growth on surface).

Product Approx. ripening Pathogen Approx. decimal Reference time (days) reduction during ripening (fermentation þ ageing)

Dry, thin (25 mm) 8 Salmonella, STEC 2 Gareis et al., 2010a, 2010b Semi-dry 21e23 Salmonella 3e3.5 Kabisch et al., 2008 E. coli including STEC 1.3e3 Heir et al., 2010; Lindqvist & Lindblad, 2009; Kabisch et al., 2008; Faith et al., 1998; Stiebing, Vogt, Baumgart, Putzfeld, & Bergt, 2000b; Kofoth et al., 1998; Lahti et al., 2001 L. monocytogenes 1e3 Lindqvist & Lindblad, 2009; Lahti et al., 2001; Kabisch et al., 2008; Farber, Daley, Holley, & Usborne, 1993 Spreadable 14 E. coli including STEC 0e1 Kofoth et al., 1998; Kabisch et al., 2008; Stiebing et al., 2000a (Teewurst type) L. monocytogenes 0.2e0.4 Albert, Rödel, Hechelmann, & Gareis, 2002; Kabisch et al., 2008 Salmonella 0.5e1 Kabisch et al., 2008 226 F.-K. Lücke, P. Zangerl / Food Control 43 (2014) 217e230

“Bündner Fleisch” also has a long tradition. Other criteria for dis- e Due to the lower acidity of liver, blood and rinds, the pH of the tinguishing raw salted/cured meats include sausages may be as high as 6.8 (for blood sausage) e Nitrite has no effect in blood sausage because of the high pH. e the type of muscle(s) used (normally muscles from the hind Moreover, it is oxidized to nitrate in the presence of haem quarters of pigs, but products like “Lachsschinken” are also (Fischer & Hilmes, 2007). In liver sausages, nitrite is inactivated made from back muscle e M. longissimus dorsi) by the non-haem iron liberated when the product is heated to e the type of salting: Traditional products are salted dry, in brine higher temperatures. This results in little if any inhibition of or by combinations thereof; injection of brine is uncommon clostridia by nitrite in liver sausages (Hauschild, Hilsheimer, e the extent of drying Jarvis, & Raymond, 1982; Lücke, 2008; Lücke & Roberts, 1993). e the ageing time: Muscle proteases tenderize the meat and improve the aroma and taste On the other hand, Sülzwurst is a safer product because it is e the treatment of the surface: Typical ham from Westphalia or usually prepared by adding vinegar to the mixtures of gelatine or the Black Forest (“Schwarzwälder Schinken”) is smoked where preparations from collagen tissues such as pork rinds. This inhibits some other varieties may be aged without smoke, similar to acid-sensitive microorganisms. French, Italian and Spanish hams. Classical “Speck” from South In perishable products, heat processing is a CCP for the control of Tirol (German-speaking region in Northern Italy) is ripened vegetative pathogens, and F70 values should be above 40. In com- while moulds grow on the surface and thereby affect appear- mercial practice, perishable sausages are cooked to about 75e80 C ance and taste. core temperature. Undercooking these products normally results in sensory deﬁciencies and is therefore, in most cases, noticed prior to Microbial hazards of relevance to hams include Clostridium shipment or consumption. Storage temperature is critical and botulinum and S. aureus. Because hams are salted at low temper- should be below 5 C. Recontamination of the products should be atures (5e8 C), there is no growth potential for pathogenic avoided in order to control L. monocytogenes. For shelf-stable bacteria that may be present on the surface. However, if the products, C. botulinum is the most important hazard. The combi- interior of the tissue is contaminated with spores of C. botulinum, nation of heat and intrinsic factors such as water activity should there is a risk of toxin formation if the hams are salted/cured at reduce the probability of development of spores of proteolytic too high temperature for too short time. For many years, toxic raw C. botulinum by at least 8 log cycles (as suggested as the target for hams were the predominant cause of botulism in Central Europe, the manufacture of shelf-stable canned cured meats by Hauschild & with psychrotrophic, non-proteolytic strains being the main Simonsen, 1985). Hence, the target F0 value should be 1.5 or above agents (see Lücke & Roberts, 1993; Lücke, 2000a). Almost all of for such products (see also Codex Alimentarius Commission, 1993), these outbreaks were due to home-slaughtering and home- and heat processing is a CCP. A F0 value of 0.4 or above is sufﬁcient if processing. Risk factors include use of meat of pH above 6.0 the water activity is reduced to 0.96 or below by adding more fat or (even though salt diffusion is very slow) and poor temperature salt or by drying the product (Lücke & Roberts, 1993). If this is done, control during salting. Critical Control Points are the pH of the raw the process of adding salt and fat and/or the drying conditions will material (<6.0, preferably below 5.8), and the salting/curing be critical for product safety, too. temperature and time (salting at 5 C or below should continue Especially in small-scale operations, canned liver sausages and until the water activity is below 0.96 in the centre of the ham). In blood sausages are only heated in open water baths for about 2 h. the last decade, only very sporadic cases of botulism from hams This treatment will eliminate spores of non-proteolytic have been recorded. This could be related to the fact that farm- C. botulinum whereas the probability of growth from spores of scale slaughtering and meat processing have been either given proteolytic strains is only reduced by 1e3 log cycles (see Lücke & up or “professionalized” by using modern equipment and tem- Roberts, 1993). Therefore, it is essential to use material with a low perature controls. spore load and to indicate the need for refrigeration (below 10 C) Some outbreaks of intoxications due to S. aureus enterotoxins clearly on the label, bearing in mind that the consumer is used to have been recorded (RKI, 1997). The main failure leading to these store canned food at ambient temperatures. Non-compliance with outbreaks was inappropriate washing and drying of the surface these rules caused some outbreaks of botulism (RKI, 2004a; Lücke between salting and smoking (Hechelmann et al., 1988). & Roberts, 1993).

4.4. Kochwurst 5. Lightly salted and/or smoked ﬁsh products, ready-to-eat

Many traditional sausages in Germany are of the Kochwurst Although the consumption of fish in German-speaking Central type. These sausages have in common that the meat cuts used are Europe is rather low, there are some traditional ready-to-eat fish pre-cooked. In small-scale processing, this makes it easier to products on the market. They are stabilized by a combination of debone them and to use lower-grade tissues such as head meat. salting, acid treatment, heat treatment, smoking and cold storage. However, heated muscle proteins can no longer bind water, and do The German Code of Practice (“Leitsätze”; Anonymous, 2008b) not form a stable “cold-emulsion”. Therefore, other water-binding describes the following perishable ready-to-eat fish products: and emulsifying components must be added such as liver (for liver sausage) or pork rinds (for “Sülzwurst” and, in conjunction e Cold-smoked fish with blood, for blood sausage). e Hot-smoked fish (core temperature >60 C), e.g. smoked trout Risk assessment must consider that liver sausages and blood from aquaculture sausages provide good growth conditions for microorganisms. This e Heavily salted (>20 g salt/100 ml tissue water) fish or products is due to various factors: thereof e Lightly salted fish or products thereof e Ingoing material such as head meat, liver, blood and pork rinds e Ripened (by endogenous proteases) fish products (“Anchosen”), may contain elevated levels of bacterial spores capable of e.g. Matjes surviving the heat treatment (Hechelmann & Kasprowiak, e Marinated fish products 1991) e Boiled or fried fish products. F.-K. Lücke, P. Zangerl / Food Control 43 (2014) 217e230 227

Of the sea fish, herring and related species such as Baltic herring place. Proteolytic strains of C. botulinum do not grow below 10 C, or sprats have been traditionally processed into fish products in and very slowly e if at all e at 15 C. Old farmhouses usually have Germany because these species were common in the North Sea and cellars in which the temperature rarely exceeds 15 C even without Baltic. “Matjes” is a lightly salted herring that is ripened by the refrigeration while modern houses do not. It is not realistic to as- action of endogenous proteases. “Rollmops” is herring marinated in sume that the latter households store canned food in their re- brine containing 10e14% salt and 5e8% vinegar (see e.g. Ballin, frigerators over extended periods. 2005). A typical product made from freshwater fish is smoked trout. Table 8 gives an overview about the hazards relevant to 7. Cereals and baked goods perishable ready-to-eat fish products common in Germany. Spores of non-proteolytic strains of C. botulinum may be present in fish, Cereals and baked goods contribute significantly to the expo- especially in farmed trout and fish caught in the Baltic Sea (see sure of the population to certain mycotoxins. Ochratoxin A is Hielm, Hyytiä, Andersin, & Korkeala, 1998; for details). Outbreaks of normally formed in all types of grain after storage under too moist botulism caused by home-processed, ready-to-eat fish in Germany conditions while Fusarium toxins are formed after infestation of have been reported; these were due to inappropriate marinating, the maturing grain in the field. Ergot alkaloids may be present drying and/or storage of the products in the home under insuffi- particularly for rye products because the open flowersofryeare cient refrigeration (RKI, 1998; BfR, 2010). Processed fish products much more prone to infection by the fungus Claviceps purpurea accounted for three outbreaks in Europe between 2000 and 2005 than flowering wheat. Concentrations are usually low and do not (De Valk et al., 2005). Two outbreaks of histamine intoxications represent a health hazard but occasionally, some samples of rye from fish were reported in Germany in 2008 (BfR, 2009b). flour were found to contain levels higher than those corresponding to the legal limit (EC, 2009) of 0.05% ergots in wheat grain to 6. Vegetable products be bought in public intervention (BfR, 2004). The toxins are stable during milling and processing, and are only slowly inactivated The process of sauerkraut manufacture includes shredding and during storage of flour or by baking. Hence, infected grains (er- ensiling cabbage without inclusion of air. The subsequent hetero- gots) must be sorted out as completely as possible, using specific lactic fermentationeffectively suppresses foodborne pathogens, machinery in mills. These processes are Critical Control Points in and no foodborne infections due to sauerkraut consumption have milling, but since they cannot eliminate the infected grains been reported. However, biogenic amines may be formed during completely, it is even more important to keep infection rate on the sauerkraut fermentation. At the beginning of fermentation, Enter- field at a minimum by appropriate agricultural practice (Münzing, obacteriaceae may form putrescine and cadaverine whereas his- 2006). tamine and tyramine are formed by lactic acid bacteria during For some traditional dry baked products (e.g. “Lebkuchen”, extended fermentation (Künsch, Schaerer, Pulver, & Temperli, “Spekulatius”), acrylamide is a hazard to be controlled. This com- 1990). This hazard may be controlled by ensuring rapid initiation pound is formed from reducing sugars and L-asparagine by of the fermentation and stopping it before a secondary flora de- Maillard-type reactions. To minimize the acrylamide content, the velops (Buckenhüskes, 2007). Use of selected starter cultures can raw material should contain as little of these precursor compounds also contribute to the suppression of microorganisms forming as possible, sodium bicarbonate rather than ammonium carbonate biogenic amines (Halász, Baráth, & Holzapfel, 1999; Künsch et al., should be used as leavening agent, and temperature and moisture 1990). during baking should be controlled to limit the extent of non- Preserved gherkins pickled in vinegar or by lactic fermentation enzymatic browning (Weibhaar, 2004). are also frequently served with cold meals in Germany. The German Analyses in Germany in 2010/2011 revealed median values for Code of Practice (“Leitsätze”; Anonymous, 2008a) specifies a min- acrylamide of 138 mg/kg in “Lebkuchen” (n ¼ 263) and of 100 mg/kg imum acid content of 0.5% (as acetic acid) for products pickled in for “Spekulatius” cookies (n ¼ 60; BVL, 2011). All “Spekulatius” vinegar and of 0.6% total acids, of which at least 0.2% lactic acid, for samples were below the EC indicative value of 500 mg/kg (European fermented products. Usually, these products are subsequently Commission, 2011) whereas 48 of the 263 “Lebkuchen”samples pasteurised. No food safety problems have been reported so far contained more than 1000 mg/kg, which is the current German with commercially prepared products of this kind. “signal value”. Due to endeavours of industry, there is a trend to- Home-canned low-acid vegetables have occasionally caused wards the reduction of acrylamide levels. botulism (BfR, 2009a). The thermal treatment in an open water bath usually results in the reduction of spore levels by only 2e4 log 8. Concluding remarks cycles. Since intrinsic factors permit growth from spores, these products are only safe if the spore load of the raw material is kept The wide choice of different regional specialities in German- low by thorough cleaning, and if the products are stored in a cold speaking regions is an important contribution to the quality of

Table 8 Hazards relevant to perishable ready-to-eat ﬁsh products.

Hazard to be controlled Products mainly affected Preventative measures

Clostridium botulinum Various semi-preserved fish Salting and/or marinating (vinegar) at (non-proteolytic strains) chill temperatures until final pH below 4.8, and/or final water activity below 0.97 Listeria monocytogenes Smoked and/or lightly salted Prevention of post-process contamination fish products Nematodes Uncooked products from Freezing of raw material; alternatively herring, mackerel, salmon salting and/or marinating (vinegar), e.g. 4 weeks at 15% salt-on-water, 5 weeks at 6% salt-on-water þ2.4% acetic acid Histamine Mackerel and other scombroid fish Use of fresh (unspoiled) fish for processing 228 F.-K. Lücke, P. Zangerl / Food Control 43 (2014) 217e230 life and should be maintained. Nevertheless, risks may be associ- Cowden, J. M., O’Mahony, M., Bartlett, C. L. R., et al. (1989). A national outbreak of ated with certain foods and eating habits, and it will remain a Salmonella typhimurium DT 124 caused by contaminated salami sticks. 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