Amino acids and biogenic amines during spontaneous malolactic fermentation in Tempranillo red wines

Amino acids and biogenic amines during spontaneous malolactic fermentation in Tempranillo red wines

ARTICLE IN PRESS Journal of Food Composition and Analysis 21 (2008) 731– 735 Contents lists available at ScienceDirect Journal of Food Composition a...

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ARTICLE IN PRESS Journal of Food Composition and Analysis 21 (2008) 731– 735

Contents lists available at ScienceDirect

Journal of Food Composition and Analysis journal homepage: www.elsevier.com/locate/jfca

Original Article

Amino acids and biogenic amines during spontaneous malolactic fermentation in Tempranillo red wines ˜ as a,, E. Garcı´a Romero a, S. Go´mez Alonso a, M. Ferna´ndez Gonza´lez a, P.M. Izquierdo Can M.L.L. Palop Herreros b a b

Instituto de la Vid y del Vino de Castilla-La Mancha (IVICAM), Crta. Toledo-Albacete s/n, 13700 Tomelloso, Ciudad Real, Spain ´gico de la Fabrica de Armas, Facultad de Ciencias del Medio Ambiente, Universidad de Castilla-La Mancha, Avda. Carlos III s/n, 45071 Toledo, Spain Campus Tecnolo

a r t i c l e in fo

abstract

Article history: Received 5 February 2007 Received in revised form 2 July 2007 Accepted 7 November 2007

This paper examines the changes undergone by the nitrogenated fraction of wine during malolactic fermentation (MLF) produced by the indigenous microbiota in 16 industrial-scale vinifications at technologically well-equipped wineries. Statistically significant increases (between 5% and 35%) were found in 15 of the 24 amino acids analyzed; decreases (between 4% and 29%) were found only in four. The biogenic amines histamine, tyramine and putrescine increased by between 106% and 174%, but histamine final concentrations in wine were not too high, under the limit of 10 mg/L established by Switzerland. There was a non-significant increase of 2.0–2.3 mg/L in ethyl carbamate. & 2007 Elsevier Inc. All rights reserved.

Keywords: Wine Amino acids Biogenic amines Ethyl carbamate Malolactic fermentation MLF Lactic acid bacteria LAB Tempranillo red wine Winemaking Castilla-La Mancha region Sanitary quality in wine Food composition

1. Introduction Lactic acid bacteria (LAB) are responsible for malolactic fermentation (MLF), a process that takes place in red wines and some white wines. This process entails biological deacidification through the conversion of malic acid to lactic acid, but many other changes also occur which influence the sensory characteristics of the wines. When MLF occurs spontaneously without any control over the strains at work, undesirable compounds may be produced which detract from the quality and acceptability of the wines, to the extent that they may even be unfit for consumption (Moreno-Arribas et al., 2003). Hence, the interest in examining the factors that affect the sanitary quality of wines, particularly those produced by the metabolism of amino acids, such as biogenic amines (Soufleros et al., 1998) and ethyl carbamate

 Corresponding author.

˜ as). E-mail address: [email protected] (P.M. Izquierdo Can 0889-1575/$ - see front matter & 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.jfca.2007.11.002

(Uthurry et al., 2003). Some countries as Germany, Belgium and France have recommended upper limits for histamine in wine (Millies and Zimlich, 1988) and Switzerland has established a limit of 10 mg/L as a tolerable value (Les Autorite´s Fe´de´rales de la Confe´de´ration Suisse, 2002) in view of the risk it poses for human health. For instance, histamine can cause headaches, allergies, diarrhea, palpitations and vomiting (Stockley, 2004), while tyramine is strongly vasoconstrictive (Silla-Santos, 1996). In the case of wine, these effects may be enhanced by (a) the presence of other amines such as putrescine and cadaverine (Landete et al., 2005), both associated with poor sanitary quality of grapes (Leitao et al., 2005) and responsible for major sensory defects in wines (Lehtonen, 1996); and (b) the alcohol, which prevents the organism’s detoxifying mechanisms from working properly. A number of authors (Lonvaud-Funel, 1999; Soufleros et al., 1998) have reported that LABs can produce biogenic amines, for example, Oenococcus oeni produces a wide range of these compounds, although putrescine or cadaverine production is less common (Guerrini et al., 2002).

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In the wine industry, there is concern that LABs may be involved in the formation of ethyl carbamate (urethane) (Tegmo-Larsson et al., 1989; Liu et al., 1994). Ethyl carbamate is formed from ethanol and a compound that contains a carbamyl group, such as citrulline, carbamyl phosphate, or urea (Ough et al., 1988). Wine LABs are potential producers of one of the precursors of ethyl carbamate—citrulline—if arginine (an amino acid found in significant quantities in grape juice and wine) is catabolized. This paper examines the changes occurring in the nitrogenated composition (assimilable nitrogen, ammonium, urea, amino acids and biogenic amines) and the production of ethyl carbamate during spontaneous MLF of Cencibel (also called Tempranillo) red wines produced industrially at wineries in the Castilla-La Mancha region.

2. Material and methods 2.1. Samples Analyses were performed on 32 samples of wine made with the Cencibel variety, from nine wineries in Castilla-La Mancha, Spain, equipped with the latest technology. Samples of two different vats were taken at seven wineries, and samples of only one were taken at the remaining two. Winemaking methods were the habitual ones used at each winery. Vats for sampling were chosen at random, the only condition being that MLF should occur spontaneously. Two samples were taken in each case, one at the end of alcoholic fermentation and the other upon completion of MLF, which was identified by determining L-malic and L-lactic acid contents. 2.2. Chemical analysis Readily assimilable nitrogen content was analyzed by the method of So¨rensen (Aerny, 1996). L-malic acid L-lactic acid, ammonium ion (NH+4) and urea were determined using enzymatic kits (Boheringer Mannhein, R-Biopharm AG, Darmstadt, Germany), and ethyl carbamate was determined following the official method (European Union 1990). 2.3. Amino acid and biogenic amine analysis Amino acid and biogenic amine contents were determined simultaneously using the method described by Go´mez-Alonso et al. (2007). A Varian ProStar HPLC (Varian Inc., Walnut Creek, CA, USA) was used, equipped with a ProStar 240 pump, a ProStar 410 autosampler and a ProStar 330 photodiode array detector. The compounds analyzed were identified on the basis of the aminoenone derivative retention times of the corresponding patterns (Sigma-Aldrich Chemie, Steinheim, Germany) and were quantified using the internal pattern method. 2.4. Statistical analysis The paired Student t-test was used to determine whether there were statistically significant differences. For comparison of wines, statistical analysis (media and standard deviation) and a twotailed Pearson correlation test were carried out using SPSS 12.0 software.

3. Results and discussion The results are presented in various tables, where the concentrations of the different compounds are grouped for

examination of the differences caused by MLF. Variations of each compound were calculated as a percent of the initial concentration in wine before MLF. Paired Student t-tests and two-tailed Pearson correlations were run on the variations (final value–initial value) in the concentration of each compound during MLF. Table 1 shows the results (mean, standard deviation, and maximum and minimum values) for readily assimilable nitrogen, ammonium, urea and ethyl carbamate, and for the 24 amino acids analyzed before and after MLF. Total amino acid concentration was also calculated as the sum of the concentrations of the individual compounds. During MLF, there was a slight but not statistically significant increase in readily assimilable nitrogen and total amino acid concentrations. Ammonium ion and urea exhibited greater increases (46.4% and 16.2%, respectively), which in the former case was statistically significant. Significant increases were observed in 15 of the amino acids analyzed, ranging from 4.60% (cysteine) to 35.2% (lysine). In contrast, only in four of them (glutamine, arginine, histidine and methionine) were there significant reductions, ranging from 4.36% to 29.1%. Pozo-Bayon et al. (2005) reported similar results and concluded that the presence of fermentation-lees from AF and the autolysis of yeasts (Buteau et al., 1984) in the process would explain this fact. Production of extracellular peptidases and proteases, which are secreted by some strains of O. oeni (Remize et al., 2005), could contribute to the increase. However, Soufleros et al. (1998) reported a decrease in total amino acid content during MLF in some wines. A search of the findings published in literature indicates that there is no consensus as regards the evolution of the different amino acids during MLF, with the exception of arginine, in which case all authors (Tonon and Lonvaud-Funel, 2000; Pozo-Bayon et al., 2005) report a considerable decrease. Along with glutamic acid, arginine is the most abundant assimilable amino acid in musts and wines (Arena et al., 1999). It is also very important in that it can be metabolized by lactic bacteria in a process leading to the formation of citrulline, a precursor of ethylcarbamate (urethane), ornithine and NH+4, as well as ATP (Mira ˜ a et al., 2001). As noted earlier, in this study we also de Ordun observed a decrease in arginine concentration, which correlated negatively with the variation of ornithine (r ¼ 0.60, a ¼ 0.01) and ammonium (r ¼ 0.55, a ¼ 0.03). However, the rise in ethyl carbamate concentration during MLF was not statistically significant, and the final average concentration (2.21 mg/L) was well below the permitted ceiling of 15 mg/L (Uthurry et al., 2003). Table 2 shows the means, standard deviation, minima and maxima and variation (percentage of initial value) for each of the nine biogenic amines determined, before and after MLF. The mean total biogenic amine content was 10.3 mg/L before MLF and 16.8 mg/L after, giving a statistically significant increase in the region of 63%. These results could have been produced by the release of amino acids as a consequence of yeast lysis during AF (Kruger et al., 1992) and the proliferation of LABs with carboxylase activity during MLF (Lonvaud-Funel, 2001). These values are very similar to the ones reported by other authors (Landete et al., 2005). The largest increases, with statistically significant differences, were found in tyramine (175%), histamine (114%) and putrescine (107%). There were non-significant increases in the concentrations of all the other biogenic amines except for spermidine, which decreased significantly by about 5%. This amine is a common component of grapes (Broquedis et al., 1989) and its concentration does not normally increase as a consequence of lactic bacteria growth (Landete et al., 2005).

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Table 1 Mean value, standard deviation, minimum and maximum values of the nitrogen, ammonium, urea, ethyl carbamate and amino acids in wines Wines after alcoholic fermentation (n ¼ 16)

Wines after malolactic fermentation (n ¼ 16)

Mean

S.D.

Minimum

Maximum

Mean

S.D.

Minimum

Maximum

Easily assimilable nitrogen Ammonium *** Urea Ethyl carbamate (mg/L)

103 7.30 4.68 2.03

11.9 5.88 3.59 1.10

80.0 1.50 0.35 0.85

123 21.5 15.0 4.23

113 10.7 5.44 2.21

18.3 6.49 3.66 1.23

84.8 3.67 1.66 0.93

161 27.7 12.1 4.70

8.92 46.4 16.2 8.65

Amino acids Aspartic acid*** Glutamic acid Asparagine Serine*** HO-Proline Glutamine*** Histidine* Glycine*** Threonine*** b-Alanine Arginine** a-Alanine*** GABA*** Proline*** Isoleucine*** Tryptophan* Ornithine Leucine*** Lysine*** Phenylalanine*** Tyrosine* Valine*** Methionine*** Cysteine*

10.8 51.1 19.7 8.62 4.27 25.0 21.1 20.3 11.2 2.92 59.0 48.8 42.5 1430 5.27 6.91 26.4 6.93 8.01 4.66 5.93 6.53 5.27 5.34

4.92 26.1 9.31 5.00 0.79 13.6 17.6 9.38 8.27 1.11 45.3 27.0 39.3 310 2.72 3.12 26.5 5.13 4.75 2.89 3.87 4.33 3.76 3.63

4.17 11.5 7.29 1.97 3.17 6.39 5.89 7.23 2.71 0.72 14.0 12.3 8.04 956 2.38 2.52 3.29 1.47 1.86 1.50 1.60 1.42 1.35 1.81

22.1 85.5 39.1 17.5 5.86 47.4 68.3 34.7 30.3 4.51 151 96.2 125 2000 11.2 11.9 96.8 16.8 17.0 10.4 12.4 14.4 12.2 12.1

12.3 50.8 20.0 9.71 4.30 17.7 18.3 22.0 13.1 2.98 50.7 52.9 46.0 1520 6.01 7.34 25.5 9.19 10.8 5.83 7.54 7.83 5.04 5.58

5.64 26.2 8.85 5.04 0.63 10.8 18.4 8.95 8.31 1.12 35.6 26.8 36.2 206 2.36 2.80 35.7 5.07 4.80 2.86 3.22 4.18 3.03 2.58

0.12 9.85 7.07 3.13 3.17 2.92 1.87 7.90 4.35 0.91 5.40 13.8 10.8 1130 3.21 3.47 1.04 3.43 2.90 2.21 2.36 2.33 1.49 1.95

22.1 86.8 38.6 17.2 5.41 37.1 64.9 36.5 31.0 5.04 125 95.7 116 1830 10.7 11.5 128 21.5 19.8 13.1 12.6 15.2 10.8 11.3

13.6 0.41 1.48 12.6 0.67 29.1 13.4 8.04 17.0 2.11 14.1 8.46 8.23 6.10 14.1 6.29 3.34 32.7 35.2 25.1 27.1 19.9 4.36 4.60

1840

517

1110

2780

1930

397

1300

2570

5.02

Total amino acids

Variation (%)

Results expressed in mg/L.Different asterisks (*, **, ***) denote statistically significant differences for a ¼ 0.05, 0.01 and 0.001, respectively.

Table 2 Mean value, standard deviation, minimum and maximum values of the biogenic amines

*

Putrescine (mg/L) Histamine*** (mg/L) Tyramine* (mg/L) Cadaverine (mg/L) Spermidine** (mg/L) Agmatine (mg/L) Tryptamine (mg/L) Phenylethylamine (mg/L) Isoamylamine (mg/L) Total biogenic amines*** (mg/L)

Wines after alcoholic fermentation (n ¼ 16)

Wines after malolactic fermentation (n ¼ 16)

Mean

S.D.

Minimum

Maximum

Mean

S.D.

Minimum

Maximum

4.12 1.39 0.36 0.61 2.84 0.49 51.7 28.2 9.64 10.3

0.90 1.16 0.26 0.17 0.92 0.30 17.8 15.9 3.71 2.48

2.45 0.08 0.00 0.34 1.86 0.00 26.3 3.07 4.65 6.61

5.79 3.86 0.73 0.94 4.64 1.29 76.2 57.2 17.2 13.9

8.52 2.97 1.00 0.66 2.71 0.55 57.5 33.6 11.6 16.8

5.46 3.94 0.70 0.16 0.79 0.41 17.1 14.2 4.59 8.23

3.75 0.51 0.26 0.33 1.85 0.00 22.5 7.97 3.67 9.64

23.5 15.7 2.63 0.90 4.24 1.15 82.0 59.2 22.4 38.5

Variation (%)

107 114 175 8.24 4.82 11.1 11.3 19.4 20.3 63.4

Different asterisks (*, **, ***) denote statistically significant differences for a ¼ 0.05, 0.01 and 0.001, respectively.

Putrescine was the most abundant amine, with mean concentrations of 4.12 mg/L before MFL and 8.52 mg/L after. These results are similar to the findings of Va´zquez-Lasa et al. (1998) in Cencibel red wines from other Spanish regions. Putrescine is also a common component of grapes (Broquedis et al., 1989) whose presence is associated with potassium-poor soils (Vaz de Arruda Silveira et al., 2001), although concentrations frequently increase in the process of winemaking (Mangani et al., 2005). Putrescine can be produced by both decarboxylation of ornithine or metabolism of arginine, through being the agmantine intermediary (Guerrini et al., 2002), and it confers an unpleasant smell (of rotten fruit, with rancid, unclean overtones) on wine when present in high concentrations. The Pearson correlation test revealed a negative correlation (r ¼ 0.67, a ¼ 0.005) between

ornithine and putrescine and a positive correlation between agmantine and putrescine (r ¼ 0.55, a ¼ 0.02), highlighting the activity of the metabolic routes mentioned earlier. Histamine was the second most abundant amine in the wines analyzed in this study, with a mean concentration of 2.97 mg/L after MLF. Note that this was a particularly low mean value, well below those reported by Gerbaux and Nonamy (2000) for wines from other regions. Only one of the samples registered a concentration of 15.7 mg/L; this is close to 20 mg/L, above which it has been reported that certain undesirable physiological effects may occur (Bauza et al., 1995) and higher than maximum concentration admitted by Switzerland (Les Autorite´s Fe´de´rales de la Confe´de´ration Suisse, 2002). However, when the distribution of histamine content was studied, it could be observed that 50% of

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wines were under 1.30 mg/L and 90% under 6.17 mg/L. Histamine is one of the amines whose concentration normally increases during MLF due to decarboxylation of histidine, the concentration of which is thereby reduced. The Pearson correlation test showed a negative correlation between the variations in these compounds before and after MLF (r ¼ 0.62, a ¼ 0.05), which would appear to confirm the decarboxylase activity. Tyramine presented the largest increase in content during MLF, although concentrations both before and after were smaller than those of the previous two. In this case, the increase in concentration of the biogenic amine was not matched by a decrease in the amino acid from which it was derived; on the contrary, tyrosine concentration rose by 27.1% during MLF. Tyrosine is released into the medium through yeast lysis, as observed in Table 1, producing a precursor substrate favoring enhanced tyramine production. Tryptamine, phenylethylamine and isoamylamine showed very low contents both, before and after MLF. Medium content for tryptamine, phenylethylamine and isoamylamine after MLF were 57.5, 33.6 and 11.6 mg/L, respectively. These values are similar (Soufleros et al., 1998) or lower than that found on consulted bibliography (Hajo´s et al., 2000; Landete et al., 2005; Marcobal et al., 2006). There were other Pearson correlations which were also interesting, although they presented lower r and significance values. Lysine in the medium increased during MLF due to yeast autolysis, and this correlated with an increase in its derived amine, cadaverine (r ¼ 0.52, a ¼ 0.04). Serine also increased after MLF, and again correlated with the increase of ammonium ion (r ¼ 0.53, a ¼ 0.03); that is because some strains of O. oeni catabolize this amino acid to form ammonium and pyruvate by means of the enzyme serine dehydratase (deaminase) (Granchi et al., 1998). The increase in total amino acid content was found to correlate positively with the variation in biogenic amine concentrations, in particular agmantine (r ¼ 0.60, a ¼ 0.01), isoamylamine (r ¼ 0.73, a ¼ 0.001), phenylethylamine (r ¼ 0.59, a ¼ 0.02), tryptamine (r ¼ 0.55, a ¼ 0.03) and putrescine (r ¼ 0.60, a ¼ 0.02). These findings corroborate the work of Soufleros et al. (1998), who concluded that the increase of amino acids in the medium affects the overall concentration of biogenic amines. Finally, we additionally found a strong correlation of the variations in the amino acid pairs leucine/phenylalanine (r ¼ 0.94, a ¼ 0.001), valine/phenylalanine (r ¼ 0.91, a ¼ 0.001) and leucinevaline (r ¼ 0.84, a ¼ 0.001).

4. Conclusions The reductions in wine amino acid concentrations during MLF that have been observed in laboratory experiments were not observed on an industrial scale. We have found that as MLF on fermentation-lees occurs practically simultaneously to the final phases of AF, the concentration of amino acids is raised by yeast autolysis or by production of proteases by some strains of O. oeni. Although the advantages for the production of quality wines are beyond question, MLF entails a number of risks which it has not been possible to obviate so far. In this research, we have shown that the biogenic amines histamine, tyramine and putrescine augment to a statistically significant extent when this process of biological deacidification occurs spontaneously. However, the results show that in industrial-scale vinification at wineries with adequate sanitary conditions, final concentrations are not such as to raise consumer health concerns (especially when these concentrations are compared with those found in other food products). Ethyl carbamate concentrations in the wines

analyzed were relatively low, and certainly well below the permitted limits. On the basis of these results, we suggest that following a selection process, some of these autochthonous strains could be used as MLF starters, with the advantage that they would be perfectly adapted to the medium from which they were isolated in the first place.

Acknowledgments ´n y Ciencia The authors wish to thank the Consejerı´a de Educacio de la JCCM for project PCC-05-003-2, the Ministerio de Educacio´n y Ciencia (INIA) for project RM2006-00011-C02-02, and the wineries which took part in this study. References ˆ ts et de vins. Revue Suisse de Viticulture Aerny, J., 1996. Compose´s azotes des mou d’Arboriculture et horticulture 28, 161–165. Arena, M.E., Saguir, F.M., Manca Nadra, M.C., 1999. Arginine, citrulline and ornithine metabolism by lactic acid bacteria from wine. International Journal of Food Microbiology 52, 155–161. Bauza, T., Blaise, A., Mestres, J.P., Teissedre, P.L., Cabanis, J.C., Kanny, G., MoneretVautrin, A., 1995. Les amines bioge`nes du vin. Me´tabolisme et toxicite´. Bulletin OIV 767–776, 42–67. Broquedis, M., Dumery, B., Boucard, J., 1989. Mise en e´vidence de polyamines (putrescine, cadaverine, nor-spermidine, spermidine, spermin) dans les feuilles et les grappes de Vitis Vinifera. Connaissance Vigne et Vin 23, 1–6. Buteau, C., Duitschaver, C.L., Ashton, G.C., 1984. A study of biogenesis of amines in a Villard noir wine. American Journal of Enology and Viticulture 35, 228–236. European Union, 1990. Commission regulation determining community methods for the analysis of wines. 2676/90, Brussels. Gerbaux, V., Nonamy, C., 2000. Les amines bio`genes dans les vins de Bourgogne. 1a partie: teneurs, origine et maıˆtrise dans les vins. Revue Franc- aise d’Oenologie,% 183. Go´mez-Alonso, S., Hermosı´n, I., Garcı´a-Romero, E., 2007. Simultaneous HPLC analysis of biogenic amines, amino acids and ammonium ion as aminoenones derivatives in wine and beer samples. Journal of Agricultural and Food Chemistry 55, 608–613. Granchi, L., Paperi, R., Rosellini, D., Vincenzini, M., 1998. Strain variation of arginine catabolism among malolactic Oenococcus oeni strains of wine origin. Italian Journal of Food Science 10, 351–357. Guerrini, S., Mangani, S., Granchi, L., Vicenzini, M., 2002. Biogenic amine production by Oenococcus oeni. Current Microbiology 44, 374–378. Hajo´s, G., Sass-Kiss, A.E., Bardocz, S., 2000. Changes in biogenic amine content of Tokaj grapes, wines and aszu-wines. Journal of Food Science 65, 1142–1144. Kruger, L.C., Pickerell, A.T.W., Azcell, B., 1992. The sensitivity of different brewing yeast strains to dioxide inhibition: fermentation and production of flavouractive volatile compounds. Journal of the Institute of Brewing 98, 133–138. Landete, J.M., Ferrer, S., Polo, L., Pardo, I., 2005. Biogenic amines in wines from three Spanish regions. Journal of Agricultural and Food Chemistry 53, 1119–1124. Lehtonen, P., 1996. Determination of amines and amino acids in wine. American Journal of Enology and Viticulture 47, 127–133. Leitao, M., Marques, A.P., San Romao, M.V., 2005. A survey of biogenic amines in commercial Portuguese wines. Food Control 16, 199–204. Les Autorite´s Fe´de´rales de la Confe´de´ration Suisse, 2002. Ordonnance sur les substrates e´trange`res et les composants dans les denre´es alimentaires (OSEC). Le De´partament federal de l0 interieur. Annexe (art 2, al. 6), p. 1068. Liu, S.-Q., Pritchard, G.G., Hardman, M.J., Pilone, G.J., 1994. Citrulline production and ethyl carbamate (urethane) precursor formation from arginine degradation by wine lactic acid bacteria Leuconostoc oenos and Lactobacillus buchneri. American Journal of Enology and Viticulture 45, 235–242. Lonvaud-Funel, A., 1999. Lactic acid bacteria in the quality improvement and depreciation of wine. Antonie van Leeuwenhoek 67, 317–331. Lonvaud-Funel, A., 2001. Biogenic amines in wine: role of lactic acid bacteria. FEMS Microbiology Letters 199, 9–13. Mangani, S., Guerrini, S., Granchi, L., Vincenzini, M., 2005. Putrescine accumulation in wine: role of Oenococcus oeni. Current Microbiology 51, 6–10. ˜ oz, R., Moreno-Arribas, M.V., Marcobal, A., Martı´nez-A´lvarez, P.J., Polo, M.C., Mun 2006. Formation of biogenic amines throughout the industrial manufacture of red wine. Journal of Food Protection 69 (2), 397–404. Millies, K.D., Zimlich, D., 1988. Histamingehalte von Weinen und Schaumweinen. Weinwirtschaft-Technik 1, 21–24. ˜ a, R., Patchett, M.L., Liu, S.-Q., Pilone, G.J., 2001. Growth and arginine Mira de Ordun metabolism of the wine lactic acid bacteria Lactobacillus buchneri and Oenococcus oeni at different pH values and arginine concentrations. Applied and Environmental Microbiology 67, 1657–1662. ˜ oz, R., 2003. Alteraciones del vino por el Moreno-Arribas, M.V., Marcobal, A., Mun metabolismo de las bacterias la´cticas. Tecnologı´a del vino 14, 100–105.

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