1399

Journal of Food Protection, Vol. 63, No. 10, 2000, Pages 1399±1403 Copyright ᮊ, International Association for Food Protection

The Mycobiota of , a Traditional Tyrolean Smoked and Cured

URSULA PEINTNER, JOHANNES GEIGER, AND REINHOLD POÈ DER*

Institute of Microbiology, Leopold-Franzens-University Innsbruck, Technikerstrasse 25, 6020 Innsbruck, Austria

MS 99-383: Received 22 December 1999/Accepted 20 May 2000

ABSTRACT Downloaded from http://meridian.allenpress.com/jfp/article-pdf/63/10/1399/1685977/0362-028x-63_10_1399.pdf by guest on 27 September 2021

Speck is a ham specialty product traditionally produced in South Tyrol (Italy) and North Tyrol (Austria) by farmers, butcheries, and meat industries. To date, nothing has been learned about fungi associated with this smoked and cured meat. Therefore, it was the main objective of this study to assess the typical mycobiota of Speck in relation to the different production types and the geographic provenance. A total of 121 Speck samples from North Tyrol and South Tyrol was analyzed. From 63 isolated fungal species, only a few can be regarded as typical colonizers: Eurotium rubrum and Penicillium solitum were the dominating species in all types and parts of Speck (crust, meat, and fat). Eight other Penicillium spp. were relatively frequent. The species diversity increased from industrially produced Speck to products from butcheries and farmers, and it was higher in all types of South Tyrolean products. Among the typical mycobiota, Penicillium verrucosum, Penicillium canescens, and Penicillium commune are known as potentially mycotoxigenic.

Speck is a smoked and cured meat specialty product known about the fungi associated with this special smoked produced in alpine regions for centuries, especially in South and cured meat product. An investigation of the molds Tyrol (Italy) and North Tyrol (Austria), using the same ba- growing on Speck is also important, because this traditional sic method. is brined with curing salts and left in the Tyrolean product is produced not only by farmers but, due resulting solution for about 3 to 4 weeks at 8ЊC. to increasing demand, also by butcheries and meat indus- Then the meat is periodically cold smoked with wood tries. Thus, Speck has become widely available in European smoke at a temperature of about 20ЊC for 6 to 8 weeks. supermarkets and specialty stores in recent years. No Eu- The frequency and the respective duration of dur- ropean Union standards exist regarding the fungal species ing this period vary strongly. After this, the Speck is rip- composition and the colonization rates of Speck, nor do ened in well-ventilated ripening chambers at 10 to 15ЊC for such standards exist in Austria or Italy, which are the main an average of 3 to 6 months. Speck-producing countries. However, directives regarding The technology of smoking and curing is used not only the production and quality of Speck have been established: as a preservation method, which prevents microbiological in Austria (North Tyrol and East Tyrol), Speck has to be spoilage through a combined salting-smoking-drying pro- produced following the general Austrian directives for salt cess, but also for the organoleptic qualities it confers to the meat (3). In Italy, the trademark South Tyrolean Speck meat. The availability of unbound water (water activity or (SuÈdtiroler Speck or Speck dell' Alto Adige) is marked aw), which is reduced in cured meat products, allows the with a protected logo and may be distributed only if strict growth of a limited number of competitive microorganisms, production guidelines and quality prescriptions are followed particularly in molds. The colonization of Speck occurs by the manufacturers (4). In both countries, the quality con- spontaneously by the mycobiota of the production environ- trol is mainly based on sensory testing, physicochemical ment or by contamination with spices (9). Also, the com- parameters (moisture, chlorides, nitrates, nitrites, pH), and panies that produce Speck on an industrial scale do not use classic hygienic parameters concerning bacteria, yeasts, starter cultures but rely on the indigenous mycobiota to mites, and parasites. Because of the lack of information carry out a spontaneous fermentation, because fungal concerning molds on and in Speck, no quality standards growth is appreciated for its bene®cial effects on ¯avor. regarding these organisms exist. Molds growing on the surface of meat products have li- Therefore, the objective of the present study was to polytic activities and, therefore, play a role in determining identify and characterize the typical mycobiota of Speck. the ¯avor and aroma of the product (21). However, these molds are potentially mycotoxigenic. The composition and A species-speci®c identi®cation of the fungi growing on development of the mycobiota of meat products, in general, this meat specialty product is important, because some usually depend on the nature of the product, processing mold species are known to produce mycotoxins in meat time, and ripening conditions (1). Up to now, nothing is products and may, thereby, represent a health hazard (1).A further aim was to compare the impact of the three different * Author for correspondence. Tel: ϩ43-(0)512-507-6002; Fax: ϩ43- production types (products made by farmers, butcheries, (0)512-507-2938; E-mail: [email protected]. and meat industries) and the geographic provenance (South 1400 PEINTNER ET AL. J. Food Prot., Vol. 63, No. 10

TABLE 1. Water activity (aw), average colonization rate, and percentage of Speck samples with fungal growth in fat and/or meat for the six types of Speck produced by industries, butcheries, and farmers in North Tyrol (Austria) and South Tyrol (Italy) Fat and/or meat sam-

aw Colonization (%) ples with fungal Type of Speck n Fat Meat Fat Meat growth (%)

Industrial, Italy 15 0.86 Ϯ 0.04 Aa 0.89 Ϯ 0.02 A 33 Ϯ 32 AB 16 Ϯ 21 A 80 Industrial, Austria 15 0.86 Ϯ 0.03 A 0.89 Ϯ 0.02 A 20 Ϯ 24 A 24 Ϯ 28 AB 93 Butcheries, Italy 15 0.86 Ϯ 0.05 A 0.89 Ϯ 0.02 A 44 Ϯ 43 B 36 Ϯ 34 B 67 Butcheries, Austria 15 0.84 Ϯ 0.03 AB 0.89 Ϯ 0.03 AB 43 Ϯ 37 B 32 Ϯ 35 B 80 Farmers, Italy 31 0.83 Ϯ 0.08 BD 0.86 Ϯ 0.07 B 47 Ϯ 42 B 44 Ϯ 39 B 81

Farmers, Austria 30 0.78 Ϯ 0.11 CD 0.85 Ϯ 0.08 B 20 Ϯ 29 A 18 Ϯ 29 A 73 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/63/10/1399/1685977/0362-028x-63_10_1399.pdf by guest on 27 September 2021 a Means in the column with different letters are signi®cantly different (P Ͻ 0.05).

Tyrol and North Tyrol) on fungal species composition and media were used for species identi®cation: Czapek yeast extract the extent of fungal colonization. agar, Czapek yeast extract agar with 20% sucrose, 25% glycerol nitrate agar, creatine sucrose neutral agar, oat agar, and synthetic MATERIALS AND METHODS nutrient agar. For formulations of the media see Klich and Pitt (10), Pitt (17), and Pitt and Hocking (18). The isolates were usu- Sampling. A total of 121 samples (60 from North Tyrol, ally incubated at 25ЊC for 7 days. Some molds (e.g., Fusarium Austria, and 61 from South Tyrol, Italy) were analyzed: 30/31 spp., Mycelia sterilia) were incubated for longer periods under produced by farmers, 15/15 from butcheries, and 15/15 from meat periodical changes of daylight and black light (360 nm; 12/12 h). industries. The samples were purchased as whole pieces of Speck (minimal size, 4 by 4 cm) in supermarkets, in stores, or directly Identi®cation of molds. As far as possible, all isolates were from the farmers. It was not possible to get Speck samples from identi®ed to species level using relevant taxonomical keys (6±8, exactly the same stages of ripening. However, all products were 10, 16±20, 23, 25). The nomenclature follows Pitt and Hocking sold as unspoiled products suitable for consumption. The indus- (18). Yeasts were not considered in this study. trial products were vacuum wrapped, and the other Speck samples were traditionally wrapped in paper (mostly plasticized paper). All Water activity (aw). The aw was measured at room temper- samples were photographed. Furthermore, the diameters of the fat ature by a thermohydrometer, Hygroskop DT (Rotronic AG, Zu- and meat parts were measured. As far as possible, all criteria con- rich, Switzerland) with a humidity sensor DMS 100 H (accuracy: Ϯ sidered in this study were investigated separately for the meat part, 2%) calibrated with saturated salt solutions. fat part, and crust (surface) of the Speck. After sampling, the Statistical analysis. The results were analyzed statistically Ϫ Њ remaining part of the Speck was deep frozen at 20 C for future using Statistica (Statsoft Inc., version 5, 1997). Data were ana- physicochemical and toxicological investigations. lyzed with one-way analysis of variance. Separation of means was Ͻ Microbiological assays. Molds were isolated from the sur- tested by the Tukey honestly signi®cant difference test (P 0.05). face of the Speck samples by contact plating a piece of crust (3 RESULTS AND DISCUSSION by 2 cm) onto DG18 (Oxoid) agar plates (three replicates). For isolation of molds from within Speck, a thin surface layer of the The aw of Speck. The aw of the fat and meat parts original cutting face of the Speck sample was aseptically removed differed signi®cantly. In general, meat had an aw of 0.85 to using a sterile, specially constructed bent razor blade on a handle. 0.89, and fat had an aw of 0.78 to 0.86 (Table 1). Statisti- After this, the fat and meat parts of the Speck were sampled sep- cally signi®cant differences also were found for the higher arately using a special sterile scalpel with two parallel blades: a of the fat part of Speck produced industrially compared 3 w small cubes (30 to 40 mm ) were cut from approximately the with farmer products. Furthermore, a clear trend toward middle of each part. Three cubes were put on one DG18 plate lower a in meat and fat of farmer products compared with (®ve replicates) and incubated at 25ЊC and a relative humidity of w both butchery and industrial products could be observed. 70% for 1 week. In this way, 3,978 random samples were taken from 121 Speck samples. Although no data were available concerning the age or ripening stage of the purchased Speck samples, the trend Colonization rates, species diversity, and abundance. Cu- toward lower aw in farmers' Speck indicates a longer rip- bes with hyphal growth within 3 weeks were recorded as ``colo- ening period of the latter. Actually, farmer products remain nized.'' Based on these counts, the percentage of colonization was longer in ripening chambers, and, therefore, they are ex- calculated separately for each part of the Speck sample. Pure cul- posed longer to mold contaminants, which may grow onto tures were obtained from all CFU, which were morphologically the Speck. On the other hand, only a few xerotolerant or different (Nikon SMZ-U Zoom 1:10 stereo lens, 75-fold magni- ®cation). The abundance of a species was de®ned as percentage xerophilic fungi are able to grow at low aw. Xerophilic of Speck samples (crust, fat, meat) on or within which the species fungi are de®ned as being able to grow below 0.85 aw (18). occurred. Following this de®nition, only a few specialized mold spe- cies should be able to grow in the fat part of Speck. Media and growth conditions. As standard isolation, me- dium dichloran 18% glycerol agar (DG18) was used. Pure cultures The fungal colonization of Speck. The results clearly were obtained on malt extract agar. When necessary, additional demonstrate that the crust of Speck is always colonized by J. Food Prot., Vol. 63, No. 10 THE MYCOBIOTA OF SPECK 1401

TABLE 2. Total number of isolated mold species and average number of species per sample for the six types of Speck produced by industries, butcheries, and farmers from North Tyrol (Austria) and South Tyrol (Italy) Number of species Species per sample

Type of Speck Crust Fat Meat Total Crust Fat Meat

Industrial, Italy 13 11 11 17 1.60 Ϯ 0.83 Ba 1.47 Ϯ 1.25 AB 1.47 Ϯ 1.55 A Industrial, Austria 8 6 3 10 2.27 Ϯ 1.28 AB 1.07 Ϯ 0.73 AB 0.93 Ϯ 0.72 B Butcheries, Italy 20 19 11 28 3.53 Ϯ 1.51 A 2.13 Ϯ 2.36 A 1.67 Ϯ 1.40 A Butcheries, Austria 15 7 6 18 2.87 Ϯ 1.73 AB 1.13 Ϯ 0.83 B 0.73 Ϯ 0.70 B Farmers, Italy 23 23 12 30 2.40 Ϯ 1.01 AB 1.83 Ϯ 1.78 AB 1.30 Ϯ 1.24 A Farmers, Austria 35 16 12 38 3.43 Ϯ 1.61 A 0.97 Ϯ 1.10 AB 0.80 Ϯ 0.92 B a Ͻ

Means in the column with different letters are signi®cantly different (P 0.05). Downloaded from http://meridian.allenpress.com/jfp/article-pdf/63/10/1399/1685977/0362-028x-63_10_1399.pdf by guest on 27 September 2021 various molds (colonization rate, 100%). Moreover, the data the individual ripening stage of this meat product. An in- presented in Table 1 show that molds could also be isolated creasing diversity of molds during ripening has, for ex- from the inner parts (fat or meat) of Speck in 79% of the ample, been reported for Iberian cured ham (15). Unfortu- samples on average. In 64% of the samples (data not nately, farmers and butcheries usually do not collect data shown), molds could be isolated both from the fat and meat. on the age of their products available to the consumers. The occurrence of molds in the fat and meat was con®rmed Therefore, it was not possible for us to evaluate any cor- by direct microscopical observation of hyphae in random relation between colonization rates or species diversity and samples of tissues. ripening stage. Applying the direct plating technique, a general mean Concerning the task outlined above, only experimen- colonization rate of 30% in both meat and fat without sig- tally inoculated Speck can provide more information about ni®cant differences was calculated. The percentage of col- the events, dynamics, and requirements of fungal growth in onization greatly varied within all types of Speck (Table 1). this substrate. Furthermore, studies on the effect of selected In general, the highest species diversity was found on mold strains on the physicochemical and organoleptic prop- the crust of Speck, where on average 2.7 Ϯ 1.3 species per erties of this product should demonstrate whether Speck can sample occurred. Signi®cantly fewer species could be iso- be regarded as a mold-fermented meat product. lated from the inner parts: fat was colonized by 1.4 Ϯ 1.3 Mold species. In total, 63 fungal taxa could be isolated and meat by 1.3 Ϯ 1.1 species per sample. Concerning the from the 121 Speck samples: 41 of them were found in the geographic provenance, however, a trend toward a higher meat and/or the fat part. The numbers of species isolated species diversity within fat and meat of Italian products from each production type are listed in Table 2. A closer could be noted (Table 2). evaluation of these results allowed an adequate distinction Few specialized mold species grow from the crust into between coincidental contamination and typical mycobiota: the meat and/or fat (compare Table 3). Because of the high 53 (84%) of the 63 identi®ed species occurred rather rarely rate of contamination of the crust, it would be advisable to (frequency, Ͻ5% on the crust and Ͻ3% in the fat or meat remove a generous quantity before consuming the product. part). Therefore, the following results concentrate on the One may in general assume that the diversity of molds most frequently encountered species, which are listed in and the extent of colonization are strongly in¯uenced by Table 3.

TABLE 3. Frequencies (% of samples from which the individual species were isolated) for all types of Speck (pooled values) and for the different production typesa Farmers Butcheries Industries

All types Austria Italy Austria Italy Austria Italy

Mold species Crust Fat Meat Fat Meat Fat Meat Fat Meat Fat Meat Fat Meat Fat Meat

Eurotium rubrum Jos. KoÈnig et al. 54 36 26 20 13 48 42 20 7 60 47 33 13 33 27 P. solitum Westling 60 33 28 16 16 48 32 20 13 27 7 53 66 33 40 P. nalgiovense Laxa 19 13 11 17 13 3 0 47 33 7 27 7 0 7 0 P. verrucosum Dierckx 9 7 7 0 0 13 16 0 0 20 20 7 0 7 7 P. canescens Sopp 9 7 4 3 3 6 0 0 0 7 0 13 0 13 27 P. brevicompactum Dierckx 17 4 6 0 3 3 3 0 0 0 20 13 13 13 0 P. chrysogenum Thom 8 4 3 3 3 0 0 0 0 0 0 13 0 13 13 P. glabrum (Wehner) Westling 5 3 5 0 7 3 6 0 0 7 7 7 0 7 7 P. commune Thom 20 3 4 3 7 3 3 7 7 7 7 0 0 0 0 P. waksmanii Zalessky 6 3 0 0 0 3 0 0 0 7 0 7 0 7 0 a Only molds that occurred in 5% or more of the samples on the crust and/or in 3% or less in the fat or the meat part are listed. 1402 PEINTNER ET AL. J. Food Prot., Vol. 63, No. 10

On the crust, Penicillium solitum and Eurotium rubrum three species were isolated only once or twice from these were by far the most frequent species, occurring in more products and can, therefore, be considered coincidental con- than 50% of the samples. Penicillium commune, Penicilli- tamination. Additional differences concern the colonization um nalgiovense, and Penicillium brevicompactum were also rate and the aw of the fat and meat part: for the Austrian abundant. These fungi seem to be typical colonizers of the products a lower aw and a lower colonization rate were crust of Speck, giving it the usual moldy appearance. But recorded. Statistical analysis of the average number of spe- which species penetrate into this substrate? Knowing the cies per sample revealed no signi®cant differences due to typical crust colonizers, it was not surprising that E. rub- high standard deviations (Tables 1 and 2). rum, P. solitum, and P. nalgiovense were the most fre- Summarizing these results, the following characteris- quently found species also in the fat and meat part. As tics become evident: (i) the species diversity increases from opposed to the three previously mentioned species, P. brev- industrial Speck toward Speck from butcheries and Speck icompactum and P. commune, which were also frequent on produced by farmers, (ii) species diversity is higher in all the crust, could be found in only 3 to 6% of the internal types of South Tyrolean products, (iii) P. verrucosum was Downloaded from http://meridian.allenpress.com/jfp/article-pdf/63/10/1399/1685977/0362-028x-63_10_1399.pdf by guest on 27 September 2021 parts of the samples. This indicates that these two species nearly exclusively isolated from South Tyrolean samples, do not penetrate easily into the meat or fat. None of the (iv) P. commune was never isolated from industrially pro- other species occurred simultaneously on the crust and in duced Speck, and (v) the frequent occurrence of P. nal- the internal parts. giovense is typical for North Tyrolean products. Further- Also, for other types of cured meat, the dominant my- more, regardless of production type or geographical origin, cobiota was reported to consist mainly of Penicillium and E. rubrum and P. solitum constantly occurred in all sam- Eurotium species (1, 12, 18). However, the composition of ples. the surface mycobiota changes during ripening of naturally fermented substrates (1). Many factors are important in de- The typical molds of Speck, their mycotoxigenic po- termining which fungi are most likely to colonize a partic- tential, and health risks. E. rubrum has been reported from other meat products (1, 11, 15, 18). In NaCl-based ular foodstuff: the aw, the pH, the carbon/nitrogen ratio, the type of packaging, and the gaseous atmosphere (22). The media, the minimum aw for spore germination of this xe- Њ impact of these factors on the fungal colonization of Speck rophilic fungus is 0.86 to 0.88 at 20 to 34 C. E. rubrum is remains a subject of future research. highly competitive over a wide range of aw and temperature in a glucose-based medium but not in NaCl-based media The impact of geographic provenance and produc- (24). P. solitum has been reported in European tion types. The industrially produced and vacuum-wrapped (1). P. nalgiovense is a cheese starter culture but has also Speck samples were characterized by a comparatively low been used in the fermentation of (2). Therefore, the number of species: only 19 species were isolated from this colonization of Speck with this species is likely to occur type of product. P. solitum and E. rubrum were the domi- by contamination from sausages. P. verrucosum has been nating species (Table 3). The species diversity, in general, reported frequently in meat products (1, 12, 22). P. canes- was higher in Italian than Austrian products. In this context, cens is known as food contaminant (e.g., of cheese). P. it is striking that P. commune was never isolated from in- brevicompactum is an extremely xerophilic mold, since its Њ dustrially produced Speck. Concerning all other investigat- minimum aw for germination and growth is 0.78 at 25 C ed parameters, no signi®cant differences between the prod- (18). P. camemberti and P. commune have been isolated ucts of North Tyrol and South Tyrol could be found. from cheese and cured meat products (1, 15), the latter pos- From the Speck produced by butcheries, 35 molds sibly causing the so-called phenol defect in Italian were isolated, with a general trend toward higher species during ripening (22). P. commune has low oxygen require- diversity in South Tyrolean products. Thus, for example, ments and is, therefore, able to penetrate deep into the meat. the average number of species per sample (Table 2) in the It causes spoilage in cheese but has also been estimated as meat part of Austrian products was signi®cantly lower. E. an essential part of the micro¯ora of Kopanisti, a traditional rubrum and P. solitum were again very frequent in the Greek cheese (18). products of both geographic regions. However, the different The ability of molds to produce mycotoxins depends provenance of the butchery products was also characterized on strain, temperature, aw, nutrient availability, oxygen ten- by the following two differences: P. nalgiovense clearly sion, and pH (5, 14). Toxicological studies of the investi- dominated in North Tyrolean products, and P. verrucosum gated samples are required to prove whether relevant quan- was frequently found in South Tyrolean Speck but was not tities of mycotoxins are produced within Speck, whereas isolated from North Tyrolean samples (Table 3). No other the controversy about the bene®ts or possible health hazards notable differences could be detected. of molds in meat or cheese still exists. The Speck produced by farmers showed the highest Nunez et al. (15) found ®ve Penicillium spp. dominat- species diversity: 51 mold species were isolated. E. rubrum ing in Iberian cured ham during most of the ripening time, and P. solitum clearly dominated in both North Tyrolean among them P. commune and P. chrysogenum (Eurotium and South Tyrolean Speck (Table 3). Similar to the butch- species increased in the ®nal product). Using chloroform ery products, P. nalgiovense was regularly and mainly iso- extracts from 59 selected isolates, they proved that most lated from North Tyrolean samples, whereas P. verrucosum molds were toxigenic to brine shrimp larvae and Vero cells. was exclusively found in South Tyrolean products. Thirty- The authors identi®ed nontoxigenic strains of P. chryso- J. Food Prot., Vol. 63, No. 10 THE MYCOBIOTA OF SPECK 1403 genum that could be used as starter cultures in this kind of Institut fuÈr Mikrobiologie, Kommissionsverlag Paul Parey, Berlin, ham. Also, other authors (13) suggested the application of Hamburg. 9. Hadlok, R. 1969. Schimmelpilzkontaminationen von Fleischerzeug- fungal starter cultures as the most satisfactory way to avoid nissen durch naturbelassene GewuÈrze. Fleischwirtschaft 49:1601± growth and secondary metabolite production by undesirable 1609. molds in cheese. Recently, Selgas et al. (21) investigated 10. Klich, M. A., and J. I. Pitt. 1988. A laboratory guide to common ®ve strains of molds belonging to the genera Penicillium Aspergillus species and their teleomorphs. Commonwealth Scienti®c and Mucor: two strains showed high lipolytic activity, but and Industrial Research Organization, Division of Food Processing, North Ryde, Australia. Reprint 1994. not all molds had a positive effect on the ®nal quality of 11. Leistner, L., and J. C. Ayres. 1968. Molds and meats. Fleischwirt- the product. In view of the considerations discussed above, schaft 48:62±65. the use of starter cultures is suggested, at least for indus- 12. Leistner, L., and C. Eckardt. 1979. Vorkommen toxinogener Peni- trially produced Speck. However, a careful selection of suit- cillien bei Fleischerzeugnissen. Fleischwirtschaft 59:1892±1896. able molds beforehand is necessary. 13. Nielsen, M. S., J. C. Frisvard, and P. V. Nielsen. 1998. Protection by fungal starters against growth and secondary metabolite produc- Downloaded from http://meridian.allenpress.com/jfp/article-pdf/63/10/1399/1685977/0362-028x-63_10_1399.pdf by guest on 27 September 2021 ACKNOWLEDGMENTS tion of fungal spoilers in cheese. Int. J. Food Microbiol. 42:91±99. 14. Northolt, M. D., H. P. van Egmond, and W. E. Paulsch. 1979. Och- We thank Heidi Ladurner, Gernot Walder, and Martin Gallmetzer, ratoxin A production by some fungal species in relation to water Handl Tyrol Gmbh, Pians, Austria, and all unnamed generous farmers for activity and temperature. J. Food Prot. 42:485±490. providing Speck samples. Our thanks are also extended to Dieter Jenewein 15. Nunez, F., M. M. Rodriguez, M. E. Bermudez, J. J. Cordoba, and and Bernhard Renzler from the Austrian Federal Of®ce for the Exami- M. A. Asensio. 1996. 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