Current Knowledge About The Presence of Amines in Wine PDF

This article was downloaded by:[Alerta - Chile 2005/2006 Consortium]
On: 7 May 2008

Access Details: [subscription number 778577077]
Publisher: Taylor & Francis
Informa Ltd Registered in England and Wales Registered Number: 1072954
Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK
Critical Reviews in Food Science and
Nutrition
Publication details, including instructions for authors and subscription information:
http://www.informaworld.com/smpp/title~content=t713606380
Current Knowledge about the Presence of Amines in
Wine
Carmen Ancn-Azpilicueta
a
; Ana Gonzlez-Marco
a
; Nerea Jimnez-Moreno
a
a
Department of Applied Chemistry, Universidad P blica de Navarra, Pamplona,
Spain
Online Publication Date: 01 March 2008
To cite this Article: Ancn-Azpilicueta, Carmen, Gonzlez-Marco, Ana and
Jimnez-Moreno, Nerea (2008) 'Current Knowledge about the Presence of Amines
in Wine', Critical Reviews in Food Science and Nutrition, 48:3, 257 275
To link to this article: DOI: 10.1080/10408390701289441
URL: http://dx.doi.org/10.1080/10408390701289441
PLEASE SCROLL DOWN FOR ARTICLE
Full terms and conditions of use: http://www.informaworld.com/terms-and-conditions-of-access.pdf
This article maybe used for research, teaching and private study purposes. Any substantial or systematic reproduction,
re-distribution, re-selling, loan or sub-licensing, systematic supply or distribution in any form to anyone is expressly
forbidden.
The publisher does not give any warranty express or implied or make any representation that the contents will be
complete or accurate or up to date. The accuracy of any instructions, formulae and drug doses should be
independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings,
demand or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or
arising out of the use of this material.
D
o
w
n
l
o
a
d
e
d

B
y
:

[
A
l
e
r
t
a

-

C
h
i
l
e

2
0
0
5
/
2
0
0
6

C
o
n
s
o
r
t
i
u
m
]

A
t
:

2
3
:
5
5

7

M
a
y

2
0
0
8

Critical Reviews in Food Science and Nutrition, 48:257275 (2008)
Copyright C Taylor and Francis Group, LLC
ISSN: 1040-8398
DOI: 10.1080/10408390701289441
Current Knowl edge about the
Presence of Ami nes i n Wi ne
CARMEN ANCN-AZPILICUETA
, ANA GONZ
ALEZ-MARCO,
and NEREA JIM
ENEZ-MORENO
Department of Applied Chemistry, Universidad P ublica de Navarra, Campus de Arrosada s/n, E-31006 Pamplona, Spain
This review discusses those factors that have an inuence on amine concentration in wine, as well as the vinication stages
when these amines are formed and their evolution during the storage of the product. It also outlines the importance of these
biogenic and volatile amines both in the sensorial aspect as well as the toxic action. Amines are nitrogenous bases of low
molecular weight, which are especially found in food and beverages from the fermentation process, as is the case of wine.
Amine concentration in wine can be very variable, ranging from trace levels up to 130 mg/L, so it is difcult to predict the
content of these compounds in the product. At present this variability is of some concern in many countries, especially for the
toxic effect that some amines can have on people who are susceptible to these substances. Consequently, it is necessary to
develop new studies to learn more about the factors, which have an inuence on their concentration in wine, and to establish
limits for these substances in the product so as to prevent any toxic effects on the consumer.
Keywords biogenic amines, volatile amines, toxic action, wines
INTRODUCTION
Amines are organic nitrogenous bases of low molecular
weight which are formed during the metabolic processes of liv-
ing organisms and which are found especially in foods from fer-
mentative processes. Depending on their volatility, these com-
pounds can be divided into non-volatile amines and volatile
amines. The former virtually coincide with biogenic amines,
except in the case of phenylethylamine, which is a biogenic
volatile amine. Biogenic amines mainly come from the decar-
boxylation of amino acids (ten Brink et al., 1990). Figure 1
shows the precursor amino acids of biogenic amines in wine.
Some biogenic amines found in wine such as histamine, tyra-
mine and phenylethylamine have toxic effects on the organ-
ism (Radler and F ath, 1991). These substances are metabo-
lized in the liver and the intestine by the action of two en-
zymatic complexes, monoamine oxidase (MAO) and diamine
oxidase (DAO). Ethanol and acetaldehyde, compounds found
in wine, are inhibitors of MAO and DAO. Consequently, they
increase the toxic effect of the biogenic amines (ten Brink
et al., 1990). The volatile amines have been much less stud-
ied than the non-volatile ones and, with the exception of
phenylethylamine, it seems that they come from the amina-
tion of non-nitrogenous compounds such as aldehydes and ke-
Author to whom correspondence should be addressed Carmen Ancn-

Azpilicueta, Telephone: (34) 948-168909; Fax: (34) 948-169606; e-mail:
ancin@unavarra.es
tones found in wine (Ough et al., 1981). These compounds
could have an unfavorable effect on wine aroma, although the
studies carried out on their threshold levels have been made
on beer.
The total content of amines in wine vary from trace
levels up to 130 mg/L (Soueros et al., 1998). Among these
nitrogenous substances putrescine is normally the most abun-
dant (Soueros et al., 1998; Lethonen, 1996). The non-
volatile amines found most frequently in wine are histamine,
tyramine, putrescine, cadaverine, spermine, spermidine, al-
though agmatine, tryptamine and serotonine, have also been
sporadically found (Lethonen, 1996; Lehtonen et al., 1992;
Busto et al., 1995). The volatile amines found in wine
are, among others, phenylethylamine, methylamine, dimethy-
lamine, ethylamine, diethylamine, isopropylamine, isobuty-
lamine, amylamine, pyrrolidine, ethanolamine, and hexy-
lamine (Ough et al., 1981; Busto et al., 1995; Ough and
Daudt, 1981).
Amines are formed in wine during different vinication
stages. Formation of amines has been observed during alcoholic
fermentation due to the metabolism of different yeast strains
(Buteau et al., 1984; Vidal-Carou and Marin e-Font, 1985; Torrea
and Ancn, 2002). An increase in the concentration of these
compounds has also been observed during malolactic fermen-
tation due to the proliferation of lactic acid bacteria (Aerny,
1985; Bauza et al., 1995; Gerbaux and Monamy, 2000). Be-
sides, a great variability in the concentration of amines exists
between different wines as there are many factors which have
257
D
o
w
n
l
o
a
d
e
d

B
y
:

[
A
l
e
r
t
a

-

C
h
i
l
e

2
0
0
5
/
2
0
0
6

C
o
n
s
o
r
t
i
u
m
]

A
t
:

2
3
:
5
5

7

M
a
y

2
0
0
8

258 C. ANCN-AZPILICUETA ET AL.
Figure 1 Precursor amino acids of biogenic amines.
an inuence, to a greater or lesser extent, in the formation of
these substances. Among these factors, the content of nitroge-
nous compounds in the grape stands out which depends, among
other factors, on the level of maturation and on the nitroge-
nous fertilization of the soil. Another important factor is the
method of winemaking employed, since red wines showa larger
concentration of amines compared to the ros e or white wines
(Radler and F ath, 1991; Zee et al., 1983). Table 1 shows the
amine concentration in wines from different types and differ-
ent geographical origin. The wine generally contains a greater
concentration of amines than some foods such as fresh veg-
etables and yogurt. However, the concentration of these sub-
stances in wine is lower than in other fermented foods such as
cheese (Table 2).
At present, the great variability in the concentration of these
substances in wine is a source of concern in many countries as
well as the toxic effect of the amines that could affect some
Table 1 Concentration of amines (mg/L) in different wines
Type of wine Histamine Cadaverine Putrescine Tyramine 2Phenylethylamine Spermine Ethylamine Reference
Red Spanish
wines
0.0025.00 (R) 0.0014.00 (R) 0.0055.00 (R) 0.0019.00 (R) 0.0016.26 (R) 0.007.92 (R) Marcobal et al.
(2006)
Young
Chardonnay
wine
0.67 (A) 0.51 (A) 3.04 (A) 2.09 (A) 0.85 (A) Gonz alez-Marco
and Ancn-
Azpilicueta
(2006)
Red quality
Turkish wines
nd1.97 (R) nd3.94 (R) nd5.92 (R) nd0.29 (R) nd3.87 (R) nd1.75 (R) Anli et al. (2004)
Chardonnay wine
from inoculated
fermentations
0.310.36 (R) < 0.12 0.370.39 (R) < 0.18 2.482.89
(R) 1.141.58 (R) 0.811.00 (R) Torrea and Ancn

(2002)
Rioja young red
wines
8.72 (A) 0.61 (A) 32.97 (A) 4.98 (A) Vazquez-Lasa et al.
(1998)
Rioja crianza red
wines
6.67 (A) 1.74 (A) 31.35 (A) 5.78 (A) Vazquez-Lasa et al.
(1998)
Tokaj wines 0.020.04 (M) 0.070.19 (M) 2.142.55 (M) 0.050.31 (M) 0.153.09 (M) Haj os et al. (2000)
Red, white, rose
French wines
8.9 (A) 0.2 (A) 7.7 (A) 3.1 (A) 1.7 (A) 0.1 (A) Bauza et al. (1995)
A: average; M: means; R: range.
Phenylethylamine + Spermidine.
people who are particularly sensitive to the action of these com-
pounds. In Europe, a lack in community legislation about the
permitted levels of amines in wine affects the import and export
of this product. The aim of this paper is to review the differ-
ent factors, which inuence the formation of amines in wine,
and to study the formation of amines during both alcoholic and
malolactic fermentations. In addition, the evolution of these sub-
stances during aging and conservation of wine is considered as
well as the enological aspects of amines, both from their toxic
features as well as their sensorial ones. With this information
it should be possible to have a better control of the vinication
process, avoiding the formation of these compounds in wine
and to establish future limits with regard to the content of these
substances in the product.
FACTORS THAT INFLUENCE THE CONCENTRATION
OF AMINES IN WINE
As was stated earlier, the total content of amines in wine
is very variable. This variability is due to the fact that numer-
ous factors could inuence the formation of biogenic amines.
Some of these factors could have an indirect inuence due
to a modication in the concentration of precursor amino
acids of the biogenic amines in the medium. Other factors
could modify the development of microorganisms with amino-
genic capacity. Outlined below, the factors, which inuence
the concentration of amines in wine, are described. It is worth
pointing out that all these factors are interrelated and conse-
quently it is difcult to know the individual action of each
one of them. Table 3 shows the variability in the content
of histamine, tyramine, putrescine, and phenylethylamine, de-
pending on the different factors that affect the vinication
process.
D
o
w
n
l
o
a
d
e
d

B
y
:

[
A
l
e
r
t
a

-

C
h
i
l
e

2
0
0
5
/
2
0
0
6

C
o
n
s
o
r
t
i
u
m
]

A
t
:

2
3
:
5
5

7

M
a
y

2
0
0
8

CURRENT KNOWLEDGE ABOUT THE PRESENCE OF AMINES IN WINE 259
Table 2 Range of biogenic amines of several foods
Type of wine Histamine Cadaverine Putrescine Tyramine 2Phenylethylamine Spermine Spermidine Reference
Red wine (mg/L) 024 08 028 028 012.73 01.75 02.19 Marcobal et al. 2005;
Leit ao et al. 2005
Brazilian beers (mg/L) 01.46 02.6 0.859.8 0.336.8 01.72 02.05 06 Gl oria and Izquierdo-Pulido
1999
Dry fermented sausages
(mg/kg)
0357.7 0658.1 0500.7 0742.6 081 0119 091.3 Suzzi and Gardini 2003
Fresh and canned tuna
(mg/kg)
040.5 012.05 04.84 010.65 07.3 2.2337 1.2011.7 Veciana-Nogu es et al. 1997
Fresh vegetables (mg/100 g
fresh weight)
01.6 tr 0.24.9 01.2 00.3 01.1 0.44.5 Moret et al. 2005
Yogurt (mg/kg wet weight) nd 00.27 nd nd nd 00.34 00.43 Novella-Rodriguez et al.
2000
Unripened cheeses (mg/kg
wet weight)
nd 01.49 01.43 00.51 nd 0.390.82 01.12 Novella-Rodriguez et al.
2000
Ripened cheeses (mg/kg
wet weight)
2.21163.56 4.23215.28 0611.68 0241.92 029.03 018.69 043.01 Novella-Rodriguez et al.
2000
nd: not detected; tr: trazes (< 0.05 mg/100 g).
Raw Materials: Grapes and Must
In general, low concentrations of amines are present in
both the grape and the must. However, different concentra-
tions of these compounds have been found in raw materials
because amines, especially polyamines, are indispensable com-
ponents of all living cells (Silla-Santos, 1996). These com-
pounds may also be a key protective factor for stressed cell
(Bouchereau et al., 1999). Moreover, some amines at a lowlevel
such as putrescine, spermidine, and histamine are normal con-
stituents of the raw materials (Broquedis et al., 1989; Vidal-
Carou et al., 1990; Haj os et al., 2000). Buteau and Duitchaever
(1984) found that putrescine was the most abundant amine
in must from the Villard Noir variety, while Sass-Kiss et al.
Table 3 Variation of amine concentration (mg/L) in wine depending on various vinication factors
Histamine Tyramine Putrescine 2Phenylethylamine Reference
Skin maceration
<10 days 1.83 0.58 0.51 0.47 3.32 1.07 2.70 0.43 Martn-
Alvarez et al. (2006)

>10 days 4.48 0.79 2.22 0.65 11.07 1.46 2.95 0.59
Vintage
2001 4.87 0.67 2.12 0.55 9.69 1.24 3.36 0.50 Martn-
Alvarez et al. (2006)

2002 1.44 0.69 0.62 0.57 4.70 1.29 2.29 0.52
Total SO
2
<50 mg/L 5.91 (n = 56) 3.62 (n = 54)
50100 mg/L 2.54 (n = 31) 2.30 (n = 30) Vidal-Carou et al. (1990)
>100 mg/L 1.20 (n = 11) 1.91 (n = 11)
Volatile acidity
a
<0.5 g/L 4.01 (n = 11) 2.70 (n = 11)
0.51.0 g/L 4.12 (n = 70) 3.07 (n = 68) Vidal-Carou et al. (1990)
>1.0 g/L 5.29 (n = 17) 2.94 (n = 16)
Turbidity
b
Filtered wine 11.2 0.4 8.8 0.5 15 1.5 0.54 0.03
c
Jim enez-Moreno and Ancn-Azpilicueta (2004)
Unltered wine 11.1 0.4 8.9 0.4 14 1 0.6 0.1
c
a
Volatile acidity is expressed as acetic acid.
b
Turbidity of wine after 243 days of aging.
c
This value correspond to Phenylethylamine + Spermidine.
(2000) found in several different grape varieties that spermi-
dine was the most abundant, followed by putrescine. Other au-
thors have also found these two amines as the majority ones in
grapes and musts before their transformation into wine (Haj os
et al., 2000; Fern andes and Ferreira, 2000; Gonz alez-Marco
et al., 2006).
It has also been seen that stress in the vineyard arising from
different causes can alter the content of amines in grape. Thus,
Haj os et al. (2000) reported that in the case of grapevine, bi-
otic stress such as the one produced by Botrytis cinerea can
also alter the composition of grape berries, increasing the amine
content. As regards water-stress, Bover-Cid et al. (2006) stud-
ied its effect on the concentration of putrescine and cadaverine,
and concluded that there does not seem to be any factor able
D
o
w
n
l
o
a
d
e
d

B
y
:

[
A
l
e
r
t
a

-

C
h
i
l
e

2
0
0
5
/
2
0
0
6

C
o
n
s
o
r
t
i
u
m
]

A
t
:

2
3
:
5
5

7

M
a
y

2
0
0
8

to modify these aliphatic polyamine contents, although more
studies should be made.
Likewise, volatile amines have been found both in grape and
in must. Accordingly, Ough et al. (1981) found that volatile
amines were present in the grapes and unlike biogenic amines,
most of the volatile amines were foundinCalifornia musts before
alcoholic fermentation. Gonz alez-Marco et al. (2006) just like
the above-mentioned authors, also found volatile amines (ethy-
lamine, diethylamine, dimethylamine, pyrrolidine, and isobuty-
lamine) in Chardonnay Spanish must.
Amino Acid Concentration
Biogenic amines and phenylethylamine, which is a volatile
amine, are formed through the action of decarboxylase enzymes
produced by microorganisms (ten Brink et al., 1990) from the
corresponding amino acid precursors (Fig. 1). So, as amino acids
are the precursors of amines, the content of free amino acids in
the must could be related to the quantity of amines in wine. The
amino acids present in grape constitute a major source of yeast
assimilable nitrogen and they are used by yeast as sources of ni-
trogen during alcoholic fermentation (Huang and Ough, 1989;
Juh` asz and T orley, 1985; Tusseau et al., 1989). Furthermore,
amino acids also act as nutrients for the bacteria during the sec-
ondary fermentations (Soueros et al., 2003). The concentration
of aminoacids inmust depends onmanyfactors suchas grape va-
riety (Feuillat, 1974; Cantagrel et al., 1982; Millery et al., 1986;
Etievant et al., 1988; Huang and Ough, 1991; Sauvage et al.,

1993; Presa-Owens et al., 1995; Spayd and Andersen-Baggie,
1996), geographical origin (Spayd and Andersen-Baggie, 1996;
Ooghie, 1981; Carnevillier et al., 1999), nitrogenous fertilization
(Bertrand et al., 1991; Spayd et al., 1994), degree of grape ma-
turity (Millery et al., 1986; Kliewer, 1970), vintage and climatic
conditions (Feuillat, 1974; Milleryet al., 1986; HuangandOugh,
1991; FlanzyandPoux, 1965). Inaddition, different winemaking
technologies like prefermentation clarication (Ayestar an et al.,
1995), crushing(Poux, 1968) anddurationof macerationprocess
(Usseglio-Tomasset and Bosia, 1990; Guitart et al., 1997) have
an effect on the amino acid fraction in must. The concentration
of amino acids in must could also be modied by the addition
of nutrients to the medium, to avoid fermentation problems. In
this way, some authors have studied the possible relationship
between the distinct factors, which affect the concentration of
nitrogen, and amino acid precursors in the must, and the produc-
tion of amines in the wine. Bertrand et al. (1991) found that the
nitrogenous fertilization of vineyards of the Merlot variety pro-
duced an increase in the nitrogenous compounds of the grape, as
well as in the concentration of histamine, putrescine, cadaver-
ine and phenylethylamine in wine. Consequently, it would seem
that those factors that increase the concentration of total amino
acids in must means a wine production with a greater content
of amines in wine. However, in real vinications no correlation
has been observed between the formation of biogenic amines in
wine and the consumption by yeasts of their precursor amino
acids, during alcoholic fermentation. In this respect, Ancn et al.
(2004) using Garnacha must have found no relationship between
the content of biogenic amines in wine and the utilization of
their precursor amino acids during fermentation. In a later work,
Gonz alez-Marco et al. (2006) did not nd an increase in the con-
centration of amines in wine during alcoholic fermentation, af-
ter adding amino acids to the must from autolysate yeast. In this
same study, no correlation was found between the consumption
of amino nitrogen nor of the amino acid precursors of amines
with the formation of biogenic amines in wine after alcoholic
fermentation.
As regards the relationship between the consumption of
amino acid precursors and the formation of amines during mal-
olactic fermentation, Soueros et al. (1998) found that during
malolactic fermentation carried out by indigenous lactic acid
bacteria, amino acid concentrations declined signicantly while
biogenic amines increased. In the same way, Martin-
Alvarez
et al. (2006) observed that during malolactic fermentation the
increase in wine of histamine, tyramine and putrescine was ac-
companied by a signicant decline in their amino acid precur-
sors. In a more general way, Herbert et al. (2005) studied the
relationship between the quantity of free amino acids in musts
of different varieties from the Alentejo region with the total
quantity of biogenic amines in red wine that had undergone both
alcoholic and malolactic fermentation. They found that the grape
variety with the highest quantity of amino acids also showed the
highest quantity of amines in the wine.
From these studies it can be concluded that higher amounts
of amino acids in must produce higher amounts of biogenic
amines after malolactic fermentation. However, in real condi-
tions, it is difcult to establish a correlation between the con-
centration of biogenic amines and the consumption of their pre-
cursor amino acids during alcoholic fermentation. This could
be due to the fact that during alcoholic fermentation, yeasts
mainly use amino acids directly in biosynthesis or as a nitro-
gen source and to a lesser extent for decarboxylation reaction
where biogenic amines are formed. It is also necessary to take
into account that the formation of amines is highly inuenced
by the aminogenic capacity both of yeasts as well as of bacteria
that carry out the malolactic and alcoholic fermentations. This
would suggest that, for a better knowledge of the nitrogenous
metabolism, including the formation of biogenic amine, it would
be important to carry out studies in synthetic media and with se-
lected strains in order to eliminate variables from the natural
medium.
Inuence of Winemaking
In general, it has been observed in most of the studies carried
out, that red wines contain more amines than either white or ros e
wines. Likewise, different authors (Lethonen, 1996; Torrea and
Ancn, 2002; Gloria et al., 1998) have observed that putrescine
is the most abundant amine in red, white, and ros e wines. Zee
et al. (1983) compared biogenic amine contents in Canadian,
D
o
w
n
l
o
a
d
e
d

B
y
:

[
A
l
e
r
t
a

-

C
h
i
l
e

2
0
0
5
/
2
0
0
6

C
o
n
s
o
r
t
i
u
m
]

A
t
:

2
3
:
5
5

7

M
a
y

2
0
0
8

American, and European wines, as well as wines from differ-
ent regions in France to detect variations due to geographical
factors and possibly vinication processes. These authors found
that red wines had signicantly more histamine and putrescine
than white wines, but the concentration of cadaverine and tyra-
mine were not signicantly different. Among the French wines
studied the wines from Bourgogne and Champagne regions had
relatively higher amounts of the histamine, putrescine, cadav-
erine, and tyramine. Jimen ez-Moreno et al. (2003) found in a
red wine of Merlot variety (2001 vintage) a higher concentra-
tion of biogenic amines than that found by Gonz alez-Marco
and Ancn-Azpilicueta (2006) in a white wine of a Chardon-
nay variety (2003 vintage). Both vinications had been made
with varieties from the same geographical zone and in the same
cellar.
As red wines have generally a higher concentration of bio-
genic amines, they have been examined in different studies.
Accordingly, Gloria et al. (1998) determined the amine con-
centration in 59 samples of Pinot Noir and Cabernet Sauvi-
gnon wines produced in Oregon, USA, from the 1991 and 1992
vintages. Pinot Noir wine contained signicantly more concen-
tration of putrescine, histamine, 2-phenylethylamine, serotonin,
and spermine than Cabernet Sauvignon wine; however, this last
wine contained more concentration of cadaverine and spermi-
dine. Landete et al. (2005) quantied histamine, tyramine, pu-
trescine, and phenylethylamine in wines from three grape va-
rieties (Bobal, Garnacha, and Tempranillo) produced in Utiel-
Requena (Spain). In this work the authors found an appreciable
inuence of the grape variety in the concentration of amines in
wine. Thus, histamine and tyramine concentrations were simi-
lar in the wine from Tempranillo and Bobal varieties and higher
than in Garnacha wine. Putrescine concentration found in Bobal
wine was slightly lower than those in Tempranillo and Gar-
nacha wines. Phenylethylamine concentration was very similar
in wines from these three grape varieties. As the soils in which
the grape varieties were cultured are similar in composition and
they were all subjected to similar winemaking practices, differ-
ences in histamine, tyramine, and phenylethylamine concentra-
tion could be due to the different content in total amino acids
of these grape varieties (data not shown in the study) or be due
to the different aminogenic ability of the strains isolated in the
samples (Oenococcus oeni, Pediococcus parvulus, Lactobacil-
lus hilgardii and Lactobacilus brevis).
Martn-Alvarez et al. (2006) studied the inuence of certain
technological practices on biogenic amines content in red wines.
This study showed that there existed a wide variability between
different wine vintages for all the amines studied as well as the
fact that the addition of pectolytic enzymes did not inuence
the biogenic amine concentration. It was also observed that a
longer time period of skin maceration increased the formation
of histamine, tyramine, and putrescine and that the wine ag-
ing on lees mainly increased the concentration of putrescine
and methylamine. It would seem that the fungi that attack the
grape in certain vintages could also inuence the amino con-
centration in wine. Thus, Kiss and Sass-Kiss (2005) found that
the concentration of biogenic amines in nonbotrytized wines is
much poorer than in botrytized wines.
Some techniques usedinwinemakingcanreduce the biogenic
amine content in wine, such as the use of bentonite (Vidal-Carou
and Marin e-Font, 1985). In this work, it was found that, in order
to reduce the wine histamine in half, a dose of 1 kg/L of ben-
tonita should be used. This dose is much higher than the normal
dose used during the vinication process and it could affect the
red wine color. Another technique proposed for elimination of
histamine in wine is a thermal treatment of the grape after press-
ing (I nigo and Bravo, 1980). Besides, Ough (1971) set out the
possibility of making refermentations with histaminolytics, but
for the moment there does not seem to have been any positive
results.
The inuence of different vinication processes on the con-
centration of wine volatile amines has not been investigated as
much as the inuence that they have on the concentration of
biogenic amines. Ough and Daudt (1981) found that most of
the volatile amines in Pinot Noir and White Riesling wines
decreased during alcoholic fermentation. Kiss and Sass-Kiss
(2005) found that some amines increased during the wine-
making process in botrytized wines and Herbert et al. (2005)
concluded that the vintage had a great effect on total volatile
amines.
Inuence of Vinication Conditions
Other important factors which inuence the concentration of
amines in wine are the conditions in which both alcoholic and
malolactic fermentation are carried out. Thus, different authors
have studied factors such as pH, temperature, concentration of
SO
2
, turbidity, and volatile acidity.
Given that the vinication conditions can be very different,
the relationship between these conditions and the concentration
of biogenic amines in wine is not very well-understood. How-
ever, there are some studies which can provide some interesting
conclusions in this respect. Zee et al. (1983) did not nd any
relationship between pH, alcohol content, and amine concen-
trations in Canadian, American, and European wines. However,
the pH of wine would seem to have an importance in the for-
mation of biogenic amines during malolactic fermentation. Ac-
cordingly, Aerny (1990) found that high pH values favored the
proliferation of bacteria strains, which can be responsible for the
formation of biogenic amines in wine. In this work it was also
found that the addition of SO
2
, even in small quantities, after al-
coholic fermentation slowed down the malolactic fermentation
and favored the development of Pediococcus, which are bacteria
with a high aminogenic capacity. Bauza et al. (1995) found that
lees and marcs can contain high levels of biogenic amines, so
that the use of lees to facilitate malolactic fermentation has to
be avoided since that could increase the concentration of those
compounds in wine. Gerbaux et al. (1997) found that in wine
without stabilization by lysozime, the bacterial population could
remain stable for several months at high levels, and so produce
an increase in biogenic amines concentration in wine.
D
o
w
n
l
o
a
d
e
d

B
y
:

[
A
l
e
r
t
a

-

C
h
i
l
e

2
0
0
5
/
2
0
0
6

C
o
n
s
o
r
t
i
u
m
]

A
t
:

2
3
:
5
5

7

M
a
y

2
0
0
8

Vidal-Carou et al. (1990) studied the relationship between the
concentration of histamine and tyramine in wine with the level of
SO
2
and volatile acidity. These authors found there existed a cor-
relation (99.9%) between total sulfur dioxide level and biogenic
amines in red wines, the highest amine contents were found
in wines with low total sulfur dioxide level. They also found
that there existed a correlation (99.9%) between histamine and
tyramine contents and volatile acidity in white and ros e wines.
However, Bauza et al. (1995) found that using SO
2
(2030 mg/L)
to stabilize wine before bottling is insufcient to prevent the for-
mation of biogenic amines. Besides, Vidal-Carou et al. (1991)
examined changes in the histamine and the tyramine concentra-
tion during wine spoilage at various temperatures. No increase
in the biogenic amine content was observed during the spoilage
of wines, but a decrease of histamine and tyramine content was
observed during the spoilage of some wines. These changes were
independent of the storage temperature of the wine.
Gardini et al. (2005) studied the inuence of different fac-
tors on the production of tyramine, spermine and spermidine
of a strain of Oenococcus oeni in a model wine. These authors
found that the arabinose concentration had an effect on tyra-
mine concentration. They also observed that an increase of the
SO
2
concentration resulted in a reduction of spermine and sper-
midine, but this relationship was more complex in the case of
the formation of tyramine. The SO
2
effect on tyramine accumu-
lation depended also on other variables like pH. On the other
hand, Jim enez-Moreno and Ancn-Azpilicueta (2004) studied
the inuence of wine turbidity on the accumulation of biogenic
amines during aging and found that turbidity did not affect the
content of biogenic amines in Merlot wine.
The inuence of other wine compounds such as malic acid,
citric acid, ethanol and sugar has also been studied. Rollan et al.
(1995) foundthat highethanol (12%v/v), L-lactic acid, andcitric
acid concentrations reduced the histidine decarboxylase activity
of cell suspension of a strain of Oenococcus oeni (Leuconostos
oenos 9204). Soueros et al. (1996) found that biogenic amines
in wine, except for phenylethylamine and putrescine, showed
negative correlations with the quantity of malic acid and cit-
ric acid. Lonvaud-Funel and Joyeux (1994) found that in the
poorest growth conditions (without glucose and malic acid) the
production of histamine was enhanced while Moreno-Arribas
et al. (2000) found that tyramine formation was enhanced in a
rich medium (with glucose), so that it would seem that the for-
mation of these amines does not have the same metabolic role
for microorganisms.
As regards the inuence of different factors of vinication
on the accumulation of volatile amines, few studies have been
made and among these the work of Ough and Daudt (1981)
stands out. They studied the effect of fermentation temperature
on the concentration of volatile amines in Pinot Noir and White
Riesling wines. These authors found that medium fermentation
temperature ranges result in the lowest amine content in wine.
Consequently, although the factors which affect the forma-
tion of amines are multiple, and in most cases dependent on
each other, it may be concluded that the greater concentration
of amines that are generally found in red wine more than ros e or
white wine, are due to the inuence of different factors. These
factors which favor the formation of biogenic amines during red
wine vinication are high fermentation temperatures, macera-
tion of the solid parts of the grape, excessively non-acid pHs,
high yeast biomass, development of malolactic fermentation,
and low levels of free SO
2
. The effect of these factors will be
different. On the one hand, they could favor the growth of mi-
croorganisms with high aminogenic activity and on the other
hand they could increase the total content of amino acids in must.
It should also be pointed out that, once the amines have been
formed, their elimination would be difcult without changing
the wine composition. Accordingly, the most recommendable
thing would be to control, as far as possible, the factors, which
have an inuence in the formation of these substances.
FORMATION OF AMINES DURING ALCOHOLIC
AND MALOLACTIC FERMENTATION
Amines are formed during different stages of vinication as
the content of amines in wine is much higher than in must, where
the concentration is very low (Radler and F ath, 1991). In this
way, the formation of amines has been observed during alcoholic
fermentation, due to the metabolism of different yeast strains.
On the other hand, malolactic fermentation is one of the stages
of vinication where the formation of these compounds could be
most important. Outlined below are the most important aspects
about the formation of biogenic amines during the development
of these two fermentative processes.
Formation of Amines during Alcoholic Fermentation of Wine
Transformation of must into wine is the result of a com-
plex succession of different yeast species. During the rst
stages of fermentation, apiculated species with low tolerance
to ethanol predominate (Kloeckera, Hanseniaspora, Candida,
Pichia, Torulaspora), and later these are gradually replaced
by Saccharomyces cerevisiae and related species, with higher
ethanol tolerance. While some authors have not given much im-
portance to alcoholic fermentation in the formation of biogenic
amines, the species of yeast that intervene in this fermentation
could be responsible for the presence of biogenic amines in wine.
Buteau et al. (1984) found increases in the concentration
of histamine, tyramine, putrescine, agmatine, and cadaverine
during alcoholic fermentation of Villard Noir musts. Likewise,
Bauza et al. (1995) also found increases in the content of his-
tamine, putrescine, and phenylethylamine during alcoholic fer-
mentation of wine from the Rh one Valley, while the concentra-
tion of tyramine did not increase until malolactic fermentation.
In contrast, Vidal-Carou et al. (1990) did not detect the forma-
tion of histamine during alcoholic fermentation, although they
did nd tyramine formation in very low concentrations. Torrea-
Go ni and Ancn-Azpilicueta (20022001) studied the inuence
D
o
w
n
l
o
a
d
e
d

B
y
:

[
A
l
e
r
t
a

-

C
h
i
l
e

2
0
0
5
/
2
0
0
6

C
o
n
s
o
r
t
i
u
m
]

A
t
:

2
3
:
5
5

7

M
a
y

2
0
0
8

Table 4 Concentration of biogenic amines (g/L) after alcoholic
fermentation in both ros e wine (Gr: Garnacha) and white wine (Ch:
Chardonnay) inoculated with different strains of Saccharomyces cerevisiae.
Reproduced with permission. (Torrea and Ancn 2001; 2002)
Control Na33 D47 K1M
Histamine
Gr 428 36 406 18 436 39 514 33
Ch 210 19 362 41 309 38 360 22
Tyramine
Gr 224 15 227 25 nd 101 12
Ch nd nd nd nd
Putrescine
Gr 11536 549 8751 302 11977 540 10224 908
Ch 3074 160 3745 138 3910 282 3888 105
Cadaverine
Gr nd nd nd nd
Ch nd nd nd nd
Phe + Spd
a
Gr 99 8 58 4 234 24 158 15
Ch 2070 110 2896 161 2485 150 2518 190
Spermine
Gr 27 3 24 4 92 3 164 8
Ch 766 52 1482 116 1137 76 1575 78
a
Phenylethylamine + Spermidine; nd: not detected.
of different strains of Saccharomyces cerevisiae on the concen-
tration of biogenic amines in Garnacha ros e wines and Chardon-
nay white wines. The musts were inoculated with three different
strains of Saccharomyces cerevisiae (Na33 with a neutral phe-
notype and two killer strains, D47 and KIM), and these samples
were comparedwitha control sample, whichhadbeenfermented
by indigenous yeasts. In these works it was observed that dur-
ing alcoholic fermentation amines were formed and depending
on the yeast strain involved in the fermentation, there was a
slight difference in the content of biogenic amines in the wines
(Table 4). In these studies, no relationship was found between
the content of biogenic amines in the wine and the utilization
of the precursor amino acids during alcoholic fermentation. The
formation of volatile amines during fermentation was scant in
all cases.
More recently, Caruso et al. (2002) tested 50 yeast strains
of different species (Saccharomyces cerevisiae, Kloeckera
apiculata, Candida stellata, Brettanomyces bruxellienses and
Metschnicowia pulcherrima) with the aim of determining their
capacity to produce biogenic amines. In general, all of the
species produced very low or non-detectable quantities of his-
tamine, while agmatine was produced by all the species under
study. Brettanomyces bruxellensis produced the greatest con-
centration of total biogenic amines, with an average value of
15 mg/L, followed by Saccharomyces cerevisiae with an av-
erage of 12.14 mg/L. Histamine, putrescine, cadaverine and
tryptamine were produced by all the strains in non-detectable
or low amounts, always less than 4 mg/L. On comparing the
levels of biogenic amines formed during fermentation different
behavior was found. Wines fermented with the most highly fer-
mentative yeasts (Saccharomyces cerevisiae strains) showed the
highest amount of agmatine. Candida stellata strains, showing
good fermentation power, behaved in a similar way and also
show an important capacity to produce cadaverine. The strains
of other species, which showed lowfermentative ability, Kloeck-
era apiculata, Brettanomyces bruxellensis and Metschnicowia
pulcherrima, showed certain variability in the production of ag-
matine and phenylethylamine.
In conclusion, amines are formed during alcoholic fermenta-
tion, even from the very beginning, since it has been observed
that the apiculate yeasts possess the capacity for the formation
of these substances. During alcoholic fermentation, the forma-
tion of amines will depend, among other factors which have
been previously outlined, on the strain of Saccharomyces cere-
visiae that predominates during fermentation. This would prob-
ably help to explain the fact that different authors have found
such a variability of amines formation in wine with a similar
vinication process. Moreover, it would be interesting to make
new studies in order to nd yeast strains that would be capa-
ble of consuming these compounds as a source of nitrogen in
late stages of alcoholic fermentation when nitrogenous sources
become scarce in the medium. In addition, it would be interest-
ing to select lactic acid bacteria strains that would be capable
of consuming biogenic amines as a source of nitrogen during
malolactic fermentation.
Formation of Amines during Malolactic Fermentation
of Wine
Malolactic fermentation is required after alcoholic fermen-
tation for nearly all red wines and some white wines. This fer-
mentation mainly consists of the deacidication by decarboxy-
lation of malic acid, but other substrates can also be metabolized
such as amino acids producing biogenic amines. In wine just a
few species of lactic acid bacteria develop, belonging to four
different genera, Lactobacillus, Leuconostoc, Oenococcus, and
Pediococcus. This is because during alcoholic fermentation not
only the total bacterial population decreases but also the lac-
tic acid bacteria diversity is reduced. In most cases, Oenococcus
oeni (Leuconostoc oenos) predominates both at the end and after
alcoholic fermentation, although some of the other species can
survive (Lonvaud-Funel et al., 1991). Leuconostoc oenos species
were classied within the Leuconostoc genus until 1995, when
thanks to studies by Dicks et al. (1995) a newOenococcus genus
was created, with the sole species Oenococcus oeni.
The physiological function of amino acid decarboxylative
pathways in bacteria is still not fully clear. It seems that for the
lactic acidbacteria the accumulationof amines is a mechanismof
protection against the acid media (Lonvaud-Funel, 2001; Schelp
et al., 2001; van de Guchte et al., 2002) and/or of obtaining
metabolic energy through coupling amino acid decarboxylation
with electrogenic amino acid/amine antiporters (Molenaar et al.,
1993; Konnings et al., 1997; Abe et al., 2002). Furthermore, the
production of polyamines such as putrescine could intervene in
other physiological functions in bacteria such as osmotic stress
(Schiller et al., 2000) and oxidative stress (Tkachenko et al.,
D
o
w
n
l
o
a
d
e
d

B
y
:

[
A
l
e
r
t
a

-

C
h
i
l
e

2
0
0
5
/
2
0
0
6

C
o
n
s
o
r
t
i
u
m
]

A
t
:

2
3
:
5
5

7

M
a
y

2
0
0
8

2001) responses, and also bacterial cell cross-talk (swarming)
(Sturgill and Rather, 2004).
In the formation of biogenic amines in wine an important role
is attributed to the lactic acid bacteria responsible for carrying
out the malolactic fermentation. In fact, many authors feel that
lactic acid bacteria are responsible for large accumulations of
these compounds in wine (Soueros et al., 1998; Bauza et al.,
1995; Gerbaux and Monamy, 2000). Table 5 shows the lactic
acid bacteria species capable of producing different biogenic
amines. Marcobal et al. (2006) found a general increase in the
concentration of amines in the rst part of malolactic fermen-
tation. These results along with those studies made in vitro by
Pessione et al. (2005) would seemto indicate that the biosynthe-
sis of the amino acid decarboxylase enzymes (which intervene
in the formation of amines) could take place when the bacterial
Table 5 Species of lactic acid bacteria able to produce biogenic amines.
Species of lactic
acid bacteria References
Histamine Oenococcus oeni Lonvaud-Funel and Joyeux
(1994)
Coton et al. (1998b)
Guerrini et al. (2002)
Landete et al. (2005a)
Lactobacillus hilgardii Faras et al. (1993)
Landete et al. (2005b)
Constantini et al. (2006)
Lactobacillus 30a Moreno-Arribas et al., 2003
Constantini et al., 2006
Pediococcus damnosus Aerny (1985)
Delni (1989)
Pediococcus parvulus Landete et al. (2005b)
Tyramine Lactobacillus brevis Moreno-Arribas et al.
(2000)
Lucas and Lonvaud-Funel
(2002)
Lucas et al. (2003)
Constantini et al. (2006)
Lactobacillus hilgardii Moreno-Arribas et al.
(2000)
Leuconostoc mesenteroides Moreno-Arribas et al.
(2003)
Phenylethylamine Lactobacillus brevis Moreno-Arribas et al.
(2000)
Lactobacillus hilgardii Moreno-Arribas et al.
(2000)
Putrescine Oenococcus oeni Coton et al. (1999)
Guerrini et al. (2002)
Marcobal et al. (2004)
Mangani et al. (2005)
Lactobacillus 30a Gale (1946)
Tabor and Tabor (1985)
Lactobacillus hilgardii Arena and Manca de Nadra
(2001)
Lactobacillus plantarum Arena and Manca de Nadra
(2001)
Lactobacillus buchneri Moreno-Arribas et al.
(2003)
population are at the exponential growth stage and at the end
of the growth stage. Other authors have not found any relation
between the presence of lactic acid bacteria in wine and the
formation of biogenic amines. Buteau et al. (1984) have shown
that biogenic amines, especially histamine, decrease during mal-
olactic fermentation. Ough et al. (1987) studied the capacity of
different lactic acid bacteria (Lactobacillus, Oenococcus and
Pediococcus) to produce histamine from histidine under differ-
ent fermentation conditions and they did not nd signicant
amounts of histamine from decarboxylation of histidine nor in
model solutions nor in fermented juice samples. This variability
in the results could be explained by the fact that the lactic acid
bacteria of wine have a different capacity for producing amines,
and this capacity is strain dependent rather than being related to
specic species (Coton et al., 1998; Bover-Cid and Holzapfel,
1999; Leit ao et al., 2000). As a consequence of the variability
for producing biogenic amines that the lactic acid bacteria show,
several studies have been carried out over the last few years
where strains from different lactic acid bacteria, producers of
biogenic amines, especially histamine, tyramine and putrescine,
have been isolated. These bacteria were characterized later at a
biochemical and molecular scale.
Fromdifferent studies (Aerny, 1985; Delni, 1989) for a long
time it was believed that the formation of histamine and other
biogenic amines in wine was due to spoilage bacteria, mainly
Pediococcus damnosus strains and not to Oenococcus oeni, the
best adapted to carry out malolactic fermentation at the low
pH of wine. However, Lonvaud-Funel and Joyeux (1994) iso-
lated a strain of Oenococcus oeni able to produce histamine via
histidine decarboxylase, from a wine from the Bordeaux area.
Coton et al. (1998) puried and characterized this enzyme and
the cloning and sequencing of the corresponding gene were also
carried out. These authors concluded that histidine decarboxy-
lase enzyme of Oenococcus oeni requires pyridoxal phosphate
as cofactor. Likewise, Coton et al. (1998) examined 118 wines
from several wine producing regions and they found that prac-
tically half of these wines contained lactic acid bacteria with
the hdc gene, responsible for the histidine decarboxylase activ-
ity. On isolating and identifying the strains responsible for this
enzyme activity, they found that all of them belonged to the
Oenococcus oeni species. Landete et al. (2005) screened 136
strains of lactic acid bacteria belonging to different species (Lac-
tobacillus, Leuconostoc, Oenococcus, and Pediococcus) for the
presence of the hdc gene and their ability to form histamine in a
synthetic medium. These authors found that the species, which
showed the greatest frequency in the production of histamine
was Oenococcus oeni, although the concentration of histamine
produced by this species was less than the one produced by
strains belonging to the Lactobacillus and Pediococcus species.
Other authors have also shown that histamine-producing strains
of Oenococcus oeni are very frequent in wine (Guerrini et al.,
2002). However, in different studies no potential to form bio-
genic amines was observed in different Oenococcus oeni strains
(Straub et al., 1995; Moreno-Arribas et al., 2003; Constantini
et al., 2006). With regard to species of other genera different
D
o
w
n
l
o
a
d
e
d

B
y
:

[
A
l
e
r
t
a

-

C
h
i
l
e

2
0
0
5
/
2
0
0
6

C
o
n
s
o
r
t
i
u
m
]

A
t
:

2
3
:
5
5

7

M
a
y

2
0
0
8

to Oenococcus, Faras et al. (1993) isolated a histamine pro-
ducer strain of Lactobacillus hilgardii from Argentinean wines
and they partially characterized the histidine decarboxylase en-
zyme. Likewise, Constantini et al. (2006) after examining 133
strains of lactic acid bacteria only found a strain of Lactobacil-
lus hilgardii with the hdc gene responsible for the histidine de-
carboxylase activity. Moreno-Arribas et al. (2003) also found
histidine decarboxylase activity in Lactobacillus 30a. Landete
et al. (2005) found that as well as Oenococcus oeni other lac-
tic acid bacteria such as Lactobacillus hilgardii, Lactobacil-
lus mali, Leuconostoc mesenteroides, and Pediodoccus parvu-
lus can contribute to histamine synthesis in wine, but it would
seem that the most responsible for the high content of histamine
in wine are Lactobacillus hilgardii and Pediodoccus parvulus
(Landete et al., 2005).
With respect to the production of tyramine in wine, Moreno-
Arribas et al. (2000) studied the formation of this amine by
different lactic acid bacteria isolated from different samples of
wine that had undergone malolactic fermentation. They con-
cluded that Lactobacillus could be the main lactic acid bacteria
responsible for the formation of tyramine in wine, since their
results showed that some strains of Lactobacillus hilgardii and
Lactobacillus brevis were strong tyramine producers. Further-
more, these authors found that Lactobacillus brevis IOEB 9809
and Lactobacillus hilgardii IOEB9649 were capable of produc-
ing tyramine and phenylethylamine simultaneously. Gale (1946)
had also found that some strains under specic culture condi-
tions might possess more than one amino acid decarboxylase
activity. In a later study, Moreno-Arribas and Lonvaud-Funel
(2001) puried and characterized the tyrosine decarboxylase
enzyme from Lactobacillus brevis IOEB 9809. These authors
found that this enzyme required the cofactor pyridoxal phos-
phate just as was found by Coton et al. (1998) in the case of the
histidine decarboxylase enzyme from a Oenococcus oeni strain.
Lucas and Lonvaud-Funel (2002) and Lucas et al. (2003) have
reported the complete sequences of gene encoding the tyrosine
decarboxylase of Lactobacillus brevis IOEB 9809 and adjacent
genes found in the same locus. The sequence of the Lactobacil-
lus brevis tyrosine decarboxylase locus contained four complete
genes, which encode a tyrosyl-tRNA synthetase, the tyrosine
decarboxylase, a probable tyrosine permease and a Na
+
/H
+
an-
tiporter. Moreno-Arribas et al. (2003) found that Leuconostoc
mesenteroides may also be responsible for tyramine production
in wines. On the other hand, although Choudhury et al. (1990)
reported a Oenococcus oeni strain capable of forming tyramine
in a laboratory medium, it would seem that this metabolic prop-
erty is not very extended within the Oenococcus oeni species
(Lehtonen et al., 1992; Guerrini et al., 2002; Constantini et al.,
2006).
Putrescine, the biosynthetic precursor of polyamines, is
formed by the decarboxylation of either ornithine or arginine
into agmatine, which is then converted into putrescine either di-
rectly or indirectly via N-carbamoylputrescine (Tabor and Tabor,
1985). The ornithine decarboxylase activity in lactic acid bacte-
ria has been described in Lactobacillus 30a (Gale, 1946; Tabor
and Tabor, 1985). Later, it was shown that the IOEB 8419 strain
of Oenococcus oeni, isolated from a wine, was capable of pro-
ducing putrescine (Coton et al., 1999), and Moreno-Arribas et al.
(2003) found two strains of Lactobacillus buchneri able to form
putrescine via ornithine decarboxylase. Recently, Marcobal et
al. (2004) isolated a putrescine producer strain of Oenococcus
oeni from the lees of a Spanish wine, and sequenced its odc
gene, responsible for the ornithine decarboxylase activity. The
high concentration of putrescine observed in some wines af-
ter malolactic fermentation cannot only come from the decar-
boxylation of the free ornithine in wine since the levels of this
amino acid in this product is usually low. The explanation for
these high concentrations of putrescine in wine could be be-
cause some lactic acid bacteria show a capacity for degrading
arginine, one of the majority amino acids both in must as well as
wine, to ornithine. Arginine can be catabolized via the arginine-
deiminase (ADI) pathway, consisting of three enzymes, arginine
deiminase (ADI), ornithine transcarbamoylase (OTC) and car-
bamate kinase (CK) (Liu et al., 1996). Consequently, to form
ornithine in wine the bacteria strains should possess all the en-
zymes of the ADI pathway and these should be active in wine
conditions.
Arena and Manca de Nadra (2001) studied the capacity of two
strains of Lactobacillus (Lactobacillus hilgardii, Lactobacillus
plantarum) to produce putrescine and agmatine from arginine
and ornithine in a synthetic medium. During the growth of Lac-
tobacillus hilgardii X1B, arginine concentration declined and,
at the same time, citrulline and ornithine (ADI pathway) and
agmatine and putrescine (by decarboxylation) were formed.
However, Lactobacillus plantarum N4 was only capable of
producing putrescine from arginine and ornithine. This lactic
acid bacteria converted arginine into citrulline during which
an NH
2
group was removed from arginine, and then citrulline
was converted to ornithine, which nally underwent decar-
boxylation to form putrescine. Guerrini et al. (2002) showed
that the two catabolic properties (arginine degradation and or-
nithine decarboxylation) are not necessarily co-existing in pu-
trescine producer Oenococcus oeni strains. More recently, Man-
gani et al. (2005) showed that Oenococcus oeni can produce
putrescine in wine through a metabiotic association, with an
interchange of ornithine, between strains capable of metab-
olizing arginine to ornithine, but unable to form putrescine,
and strains capable of producing this amine from ornithine,
but unable to degrade arginine. In this study, the production
of putrescine through this metabiotic association took place
once the malolactic fermentation nished, while the conver-
sion of ornithine to putrescine by a single ornithine decarboxy-
lating strain took place simultaneously to the degradation of
malic acid.
From these studies it may be concluded that the control of
malolactic fermentation is one of the most important measures
to take in order to avoid important accumulations of biogenic
amines in wine. To do so, it would be essential to do some
investigation about the capacity of different lactic acid bacteria
to produce these compounds. It would be necessary to isolate and
D
o
w
n
l
o
a
d
e
d

B
y
:

[
A
l
e
r
t
a

-

C
h
i
l
e

2
0
0
5
/
2
0
0
6

C
o
n
s
o
r
t
i
u
m
]

A
t
:

2
3
:
5
5

7

M
a
y

2
0
0
8

select strains with little or no biogenic amine formation ability,
but it would also be necessary to check their effectiveness and
implantation in the specic conditions of each type of wine.
Furthermore, it would be interesting to study the proteolytic
capacity of the strains to be used in these fermentations, as a high
proteolytic enzyme activity could also potentially increase the
risk for biogenic amines formation, by increasing the availability
of free amino acids.
EVOLUTION OF AMINES DURING WINE AGING
Evolution of amines during wine storage in both bottle and
barrel has been little studied, because amines are usually related
to food rich in proteins with microbial proteolytic activity. Wine,
although not rich in proteins, contains high levels of free amino
acids that can be decarboxylated by residual microbial popula-
tions to produce the corresponding amines. Wine amino acids
come from the must amino acids not used by the yeasts during
alcoholic fermentation and also from the release to the medium
of cytoplasmic content of the yeast, which is produced at the
end of alcoholic fermentation.
Evolution of Amines in Wine Aged in Oak Barrels
and in Cement and Stainless Steel Tanks
Oak has been used for many centuries to produce barrels
to age wine. During wine maturation in a barrel the product
evolves since the oak releases compounds and the barrels per-
mit a moderate wine oxygenation. Marcobal et al. (2006) did
not nd signicant changes (p < 0.05) in the content of his-
tamine, tyramine, putrescine, and cadaverine with regard to the
concentration of these amines in red wine after malolactic fer-
mentation to which 100 mg/L of SO
2
had been added at the
beginning of alcoholic fermentation and 40 mg/L have been
added after completion of malolactic fermentation. As a re-
sult, these authors concluded that a high dose of SO
2
avoids
the formation of amines during wine aging. In this work the
formation of biogenic amines in red wines elaborated in ve
Spanish winemaking cellars was studied throughout the whole
process of vinication. The wine was aged during six months in
oak barrel. Conversely, Gerbaux and Monamy (2000) found im-
portant increases in the concentrations of histamine, tyramine,
and putrescine during barrel aging of Chardonnay and Pinot
Noir wines, especially between the fourth and eighth month
of aging. In this work the wines studied came from different
wineries of the Burgundy region and the vinication techniques
used were those of each particular winery. Jim enez, Torrea,
and Ancn (2003) studied the evolution of amines during eight
months of Merlot wine aging in oak barrels (Fig. 2). In this
study, the concentrations of histamine and tyramine increased
at the beginning of aging and later decreased, probably due to
their degradation. Putrescine was formed throughout the aging
period, reaching its maximum concentration at the end of the
period under study. The concentration of cadaverine increased
during the rst month of aging and later it hardly changed. The
concentration of phenylethylamine+spermidine in the wine in-
creased about the fourth month of storage in an oak barrel and
the concentration of spermine hardly varied during the studied
period.
The synthesis of biogenic amines during wine aging in oak
barrels would be due to the presence of residual populations of
lactic acid bacteria in the wine which, in case of a scarcity of
nutrients, obtain energy through the decarboxylation of amino
acids (Konnings et al., 1997). Therefore, it would seem that the
strains of lactic acid bacteria with decarboxylase activity sur-
vive more time in wine than those that do not have this activity
(Lonvaud-Funel, 2001). Coton et al. (1998) found that the his-
tidine descarboxilase activity and the capacity to form colonies
of Leuconostoc oenos 9204 during wine aging decreased with
time. They also observed that after 2 months of aging bacteria
population had completely disappeared while there still existed
a notable enzyme activity that lasted even after 4 months. This
would suggest that the biogenic amines could be formed in the
absence of viable lactic acid bacteria in wine. Another factor,
which could favor the production of amines during wine barrel
aging, is the release of amino acids after fermentation due to the
autolysis of some yeasts (Slaughter et al., 1987; Kruger et al.,
1992) and the alteration of the plasmic membrane of the living
yeasts (Ayestar an et al., 1995; Monteiro and Bisson, 1991). In
many fermented foods the degradation of histamine and tyra-
mine has been observed due to the action of histamine and tyra-
mine oxidase enzymes present in some bacteria. These enzymes
act by degrading the histamine and tyramine respectively (Voigt
and Eitenmiller, 1978; Leuschner et al., 1998; Enes-Dapkevicius
et al., 2000). The results of Jim enez, Torrea, and Ancn (2003)
suggest that inwine this enzyme activityalsoexists andcatalyzes
the oxidation of histamine and tyramine so that the concentration
of these amines decreased after the rst months of wine aging in
barrel. In wine, the action of these enzymes would be hindered
by acid pH as the greatest activity of these enzymes takes place
at neutral or basic pH. It is not likely the oxygen requirement
of these enzymes would be a limiting factor for their activity, as
the barrels permit the micro-oxygenation of the wine.
Wine aging in barrels may be carried out either retaining wine
turbidity or after ltering the wine, thus avoiding racking and
saving on costs. Jim enez-Moreno and Ancn-Azpilicueta (2004)
studied the accumulation of biogenic amines both in red wine
from Merlot variety aged after diatomaceous earth ltration and
in the same wine aged without ltration. The wine remained for
243 days in American oak and French oak barrels. Diatoma-
ceous earth has a relatively large negative surface charge and
so nitrogenous compounds from must such as cationic amino
acids and proteins can be expected to be partially adsorbed on
the surface (Boulton et al., 1996). Consequently, ltration using
diatomaceous earth could inuence the evolution of biogenic
amines during wine aging. The results of this work showed
that the different degree of wine turbidity did not have any
D
o
w
n
l
o
a
d
e
d

B
y
:

[
A
l
e
r
t
a

-

C
h
i
l
e

2
0
0
5
/
2
0
0
6

C
o
n
s
o
r
t
i
u
m
]

A
t
:

2
3
:
5
5

7

M
a
y

2
0
0
8

Figure 2 Evolution of biogenic amines in wine aged in French (Allier and Nevers) and American oak barrels. Reproduced with permission (Jim enez-Moreno
et al., 2003).
inuence on the accumulation of biogenic amines during the
aging period.
With regard to the behavior of the volatile amines during wine
aging in barrel, Jimen ez, Torrea, and Ancn (2003) found that
dimethylamine and isobutylamine showed less concentration in
wine aged 8 months than in young wine. Pyrrolidine and ethy-
lamine increased in some samples at the end of aging, while
isopropylamine, diethylamine, amylamine, and hexylamine re-
mained practically constant during the whole aging process in
the barrel. The decrease in the concentration of volatile amines
could be due to the consumption of these amines by residual bac-
teria populations present in wine, to obtain carbonated skeletons
or amino groups (Boulton et al., 1996).
Aging of wine in cement deposits is less frequent although,
depending on the needs of the winery, sometimes the wines are
kept in simple cement deposits, nowadays always covered over
D
o
w
n
l
o
a
d
e
d

B
y
:

[
A
l
e
r
t
a

-

C
h
i
l
e

2
0
0
5
/
2
0
0
6

C
o
n
s
o
r
t
i
u
m
]

A
t
:

2
3
:
5
5

7

M
a
y

2
0
0
8

(alicated, glass-covered, covered in epoxy resin). Other times,
well-protected iron, PVCor stainless steel tanks are used. Bauza
et al. (1995) studied the evolution of biogenic amines during
the vinication process of different wines from the Rh one Val-
ley, including 3 months of wine aging in cement and steel de-
posits. These authors found important increases in histamine,
putrescine, and tyramine during wine aging while the concen-
tration of phenylethylamine hardly evolved.
From these studies it may be concluded that at the begin-
ning of wine aging the concentration of most of the biogenic
amines increases. Later, the concentration of some amines such
as histamine and tyramine decreases. In this respect, it would be
important to carry out further studies to get a better knowledge
about the evolution of biogenic amines as well as to determine
whether these amines could bind to the barrel wood or whether
their concentration diminished by oxidative degradation or from
reactions with other substances present in wine. On the other
hand, some authors have suggested using high concentrations
of SO
2
in order to control the formation of biogenic amines dur-
ing aging as this prevents the proliferation of microorganisms.
However, the efciency of this vinication practice is uncertain
as viable decarboxylase activity could remain in the medium.
Evolution of Amines in Wine Aged in a Bottle
Sooner or later wine is bottled and this becomes its nal and
denitive storage container. In this form the wine will stay for
different lengths of time depending on whether they are young
wines or vintage wines. These latter reach their full maturity
in the bottle and the former also improve their quality. Vidal-
Carou, Codony-Salcedo, and Marin e-Font (1991) studied the
evolution of four commercial wines, with different contents of
histamine and tyramine, during their storage in bottle at differ-
ent temperatures. These authors did not nd any increase in the
concentration of these amines at any of the temperatures studied
(4
Cto 6
C, 20
Cto 24
C, 30
Cto 35
C). However, they found

a decrease in the content of histamine in one of the bottles kept
at between 2024
C after 78 days of wine aging, when it began

to showclear signs of spoilage (volatile acidity higher than 1 g/L
acetic acid). Likewise, they found that the concentration of tyra-
mine decreased after 80 days of aging in one of the bottles kept at
between 46
C. More recently, Landete et al. (2005) studied the

inuence of aging in a bottle on the content of biogenic amines
in young wines from Utiel-Requena and they found an increase
in the concentration of histamine during the rst 6 months of
wine storage in a bottle. Later, the concentration of this amine
decreased. Tyramine, putrescine and phenylethylamine did not
show any important changes during 12 months of wine storage
in a bottle.
Gonz alez-Marco and Ancn-Azpilicueta (2006) studied the
evolution of amines from a Chardonnay wine aged in a bottle at
different temperatures (4
C, 20
C, and 35
C) over 105 days. In

this study the concentration of histamine increased during the
rst 45 days in all the samples, independently of the temperature.
At the end of the studied period, the wine kept at 20
C showed
a greater concentration of this amine than the wines stored at
more extreme temperatures. This difference is probably due to
the fact that decarboxylase activity was more favored at room
temperature than at extreme temperatures of 4
C and 35
C. In
addition, tyramine, putrescine, and cadaverine were formed at
the beginningof aginginall samples andlater their concentration
hardly varied, except in the case of tyramine, whose concentra-
tion decreased in all samples after 75 storage days in a bottle.
The evolution of spermine was completely different to the rest
of the amines, as this compound progressively disappeared from
the wine in all the samples, although it did so quicker in the wine
kept at 4
C and 35
C than in the wine at room temperature. So,

it would seem that the utilization of this amine by residual pop-
ulations of microorganisms is not important to obtain energy.
In this study, the evolution of volatile amines was also studied.
The concentrations of ethylamine, pyrrolidine, and hexylamine
increased slightly at the beginning of aging, while the concen-
tration of dimethylamine decreased during the rst 45 days and
later remained constant. The concentrations of isobutylamine
and isopropylamine did not show important variations during
the studied period and the content of diethylamine decreased
slightly in the wine kept at 35
C.
Consequently, it would seem that, just as was observed in a
wine aging in a barrel, the amines are also formed at the begin-
ning of wine storage in a bottle. On the other hand, the evolution
of these compounds in a bottle scarcely depends on the wine
conservation temperature.
ENOLOGICAL ASPECTS OF AMINES
Some polyamines have an important biological function as a
source of nitrogen for cells and as precursors in the synthesis of
hormones, alkaloids, nucleic acids, and proteins (Silla-Santos,
1996). Furthermore, some amines play an important role in the
regulation of body temperature, as well as in the volume and pH
of the stomach and in brain activity (Silla-Santos, 1996). How-
ever, besides their biological function, amines are important in
other aspects. Some biogenic amines, if they are consumed in
certain concentrations, can act on the neurotransmitters of the
central nervous system or on the vascular system, producing,
among other symptoms, important modications in blood pres-
sure (Bard ocz et al., 1995). Besides, some amines can be precur-
sors of nitrosamines and nally, the volatile amines can affect
wine aroma.
Toxic Action
Of the amines found in wine, not all of them present toxic
effects for consumers. The main biogenic amines implicated in
food poisoning are: histamine, tyramine, putrescine, cadaver-
ine, phenylethylamine and tryptamine. Table 6 shows the main
effects that these amines produce in human beings.
D
o
w
n
l
o
a
d
e
d

B
y
:

[
A
l
e
r
t
a

-

C
h
i
l
e

2
0
0
5
/
2
0
0
6

C
o
n
s
o
r
t
i
u
m
]

A
t
:

2
3
:
5
5

7

M
a
y

2
0
0
8

Table 6 Biogenic amines and their pharmacological effects (Shalaby, 1996)
Amine Precursor Pharmacological effects
Histamine Histidine Liberates adrenaline and noradrenaline
Excites the smooth muscles of uterus, the intestine and the respiratory tract
Stimulates both sensory and motor neurons
Controls gastric acid secretion
Tyramine Tyrosine Peripheral vasoconstriction
Increases the cardiac output
Causes lacrimation and salivation
Increases respiration
Increases blood sugar level
Release noradrenaline from the sympathetic nervous system
Causes migraine
Putrescine and cadaverine Ornithine and lysine Hypotension
Bradycardia
Lockjaw Paresis of the extremities
Potentiate the toxicity of other amines
Phenylethylamine Phenylalanine Releases noradrenaline from the sympathetic nervous system
Increases the blood pressure
Causes migraine
Tryptamine Tryptophane Increase the blood pressure
Histamine is found in a natural way in blood and the concen-
tration of this amine in the blood ow is normally at between
25 to 130 mg/L (Cardona-G alvez and Gonz alez-Domnguez,
2005). Histamine is the most studied biogenic amine and it is
usually taken as an indicator of freshness and quality in many
foods. The effects produced by histamine are the most well-
known as they are implicated in most cases of food poisoning
(Taylor, 1983). This amine is freed in certain tissues as a result
of allergic hyper-sensitivity or of inammations and has a potent
vasodilatory action which could cause important drops in blood
pressure (Rice et al., 1976). Other symptoms of intoxication
by histamine are vomiting, diarrhea, headaches, facial ushes,
itching, and throat inammation (Silla-Santos, 1996). Histamine
has traditionally been the amine most related to the so-called
wine intolerance that some sensitive people have to this product.
However, at present, a certain controversy exists as to whether
histamine in wine is the cause of all cases of toxic effects pro-
duced by the product. In this respect, Kanny et al. (2001) using
histamine-poor or histamine-rich wines demonstrated that there
is no correlation between the histamine content of wine and hu-
man wine tolerance. Consequently, these authors conclude that
the presence of other compounds in wine, such as acetaldehyde,
could explain the fact that there are some people who are in-
tolerant to this beverage as these compounds could provoke the
liberation of endogenous histamine as the cause of the intol-
erance. Histamine consumed in food and drinks is detoxied
in the intestine gut by two enzymes, diamine oxidase (DAO)
and histamine N-methyl transferase (HMT) (Shalaby, 1996).
This protection mechanism can become inhibited if the intake
of histamine and/or other biogenic amines is very high, or if
the enzymes are blocked by other compounds (Hayashi, 1954;
Bjedanes et al., 1978). Figure 3 shows the difference between
normal conditions where the MAO and DAO enzymes act so
that innocuous oxidation products reach the bloodstream and
conditions where there is an absence of enzyme activity where
there is an entry of amines with a toxic activity in the blood-
stream. Among the possible compounds which increase the his-
tamine toxicity are trimethylamine, oxide of trimethylamine,
acetaldehyde and other biogenic amines such as putrescine, ca-
daverine, spermine, spermidine (Cardona-G alvez and Gonz alez-
Domnguez, 2005). The action of these enzymes is also reduced
with the consumption of ethanol and by the secondary effects of
some drugs (Gafner, 2003). The presence of histamine in food
Figure 3 Representation of the biogenic amines absorption through the in-
testine gut (normal conditions and in absence of enzyme activity).
D
o
w
n
l
o
a
d
e
d

B
y
:

[
A
l
e
r
t
a

-

C
h
i
l
e

2
0
0
5
/
2
0
0
6

C
o
n
s
o
r
t
i
u
m
]

A
t
:

2
3
:
5
5

7

M
a
y

2
0
0
8

and drinks does not necessarily imply danger. Many foods con-
tain small doses of histamine, which can be easily metabolized
by the human organism. Histamine intolerance seems to be re-
lated to a reduced gastrointestinal DAO activity (Wantke et al.,
1993; Wantke et al., 1994; Jarisch and Wantke, 1996; Wantke
et al., 1996). Few rigorous studies exist about the different lev-
els of activity of the gastrointestinal DAO in both tolerant and
intolerant individuals, nor about the differences that could exist
between the sexes or between people of different ages or even
of people with different physical conditions. In addition, genetic
polymorphisms or differences for DAO activity have been iden-
tied between tolerant and intolerant individuals (Petersen et al.,
2003; Schewelberger et al., 2003). Accordingly, further studies
are needed to determine the mechanism of intolerance to wine.
Tyramine, tryptamine, and phenylethylamine form part of
the group of vaso-constrictor amines. Tyramine has a vaso-
constricting action due to the fact that it provokes a release of
noradrenaline (Forsythe and Redmond, 1974), which increases
arterial pressure. The importance of tyramine infoods exists both
in its toxic effect and that it also reacts with drugs that inhibit
the (MAOI) giving place to hypertensive crisis (Marin e-Font,
1978). The use of drugs that inhibit the MAO for the treatment
of mental depression interferes in the detoxication process of
these amines and can produce hypertensive crisis in patients that
accumulate tyramine in their blood (Blackwell, 1963; Lejonic
et al., 1979; Smith and Durack, 1978). Phenylethylamine, like
tyramine, provokes increases in blood pressure but in this case
it is due to the liberation of norefedrine (Radler and F ath, 1991).
Another symptom of poisoning by these amines could be the
appearance of string migraine attacks (Sandler et al., 1974).
Polyamines (putrescine, cadaverine, spermidine, and sper-
mine) are indispensable compounds for the living cells. These
compounds are necessary for the tissues in growth, given the di-
versity of functions attributed to them in the metabolism and the
cell growth (Bard ocz, 1989). Although cells are able to synthe-
size these compounds, diet would seem to be their main source.
Besides, spermine and spermidine were seen to be implicated in
the evolution of the intestine tissue. These compounds, although
they do not have any toxic activity, can inhibit the action of the
MAO and DAO enzymes which are responsible for the degrada-
tion of histamine, tyramine, and phenylethylamine and so, they
can reinforce the toxic activity of these amines. In experiments
with animals, it has been proved that toxicity of histamine is
increased by a factor of 10 when this amine is administered 40
minutes after the ingestion of putrescine (Parrot and Nicot, 1966)
and cadaverine (Hui and Taylor, 1985; Bjedanes et al., 1978).
On the other hand, those amines which contain secondary
amino groups (spermine, spermidine, dimethylamine, pyrroli-
dine. . . ) can react with the nitrous acid and its salts to form
nitrosamines (Scheme 1) which are compounds with carcino-
genic, mutagenic, and theratogenic activity (Scanlan et al., 1982;
Gl oria et al., 1997). Although wine hardly has any nitrites (Ough
and Crowell, 1980) these compounds could reach the intestine
gut due to the intake of other types of food and could react with
the secondary amines present in wine in a reaction catalyzed by
SCHEME 1 General reaction of the nitrosamines formation.
enzymes of the intestine ora (Allison and McFarlane, 1989).
Maduagwu and Uhaerghu (1986) found that the concentration
of nitrosamines in Nigerian brewed beers and palm wine was
negligible even though no amount of a chemical carcinogen in
human foodstuff could be regarded as a safe level.
The toxic limits of biogenic amines have still not been estab-
lished and depend on the type of amine, on the food simultane-
ously being taken which could interact with them, and on the
efciency of the detoxication mechanisms of different people
(Taylor, 1985), although some authors have established different
ranges. The different food and drinks and even the different vari-
eties of the same food can have different toxic limits. In general,
840 mg of histamine can cause slight poisoning, over 40 mg
moderate, while over 100 mg severe poisoning. However, it
would seemlogical to think that the human tolerance level to this
amine would depend on the sensitivity of each consumer to this
compound. At present, there are few studies that determine the
histamine concentrations that produce toxic effects on sensitive
people. The study made by Wankle et al. (1994) stands out. This
work was carried out with 28 patients who showed symptoms of
being intolerant to wine. These patients, after oral ingestion of
125 mL of red wine (equivalent to 50 g of histamine), showed
allergy problems at these levels, and which are easily tolerated
by healthy people. Tyramine doses of 1080 mg could cause
toxic swelling and over 100 mg may cause migraine (Askar and
Terptow, 1986). The dose of phenylethylamine able to produce
symptoms is much lower than that of histamine or tyramine.
Sandler et al. (1974) reported that 3 mg of phenylethylamine
causes migraine. Spanjer and van Roode (1971) suggested that
the sum total of tyramine, histamine, putrescine, and cadaverine
in cheese should not exceed 900 mg/kg. Most countries have not
established limits of concentration for these substances for wine
although there are some pioneer states whose laws recommend
limits for the content of histamine, which as was stated earlier,
is one of the most dangerous amines for human health. Thus,
Switzerland will not accept wines whose content of histamine is
higher than 10 mg/L, and the quantities recommended in other
countries is even lower than that Germany (2 mg/L), Belgium
(from5 to 6 mg/L), France (8 mg/L) (Bauza et al., 1995; Landete
et al., 2005).
In conclusion, limits in the amine content in wine are difcult
to establish. As was mentioned earlier, the appearance of symp-
toms after the ingestion of a determined quantity of biogenic
amines varies widely from individual to individual as it would
seemto be due to a reduced gastrointestinal DAOactivity. There-
fore, before beginning to legislate about recommended or per-
mitted levels, it will be necessary to nd out what concentrations
D
o
w
n
l
o
a
d
e
d

B
y
:

[
A
l
e
r
t
a

-

C
h
i
l
e

2
0
0
5
/
2
0
0
6

C
o
n
s
o
r
t
i
u
m
]

A
t
:

2
3
:
5
5

7

M
a
y

2
0
0
8

of biogenic amines can provoke toxic effects in both tolerant and
intolerant individuals, and the level of intolerance that can ex-
ist as well as the fundamental causes for these. Consequently,
it would be convenient to study a wide range of individuals,
which would include healthy people and those with different
intolerance levels, as well as including members of both sexes
and people from a wide range of ages.
Sensorial Effect
The non-proteic nitrogenous compounds such as amines and
peptides contribute to the avor and taste of food (Maga, 1978).
Volatile amines have intense and characteristic odors and this
type of compound could affect wine avor. Few studies have
been made on the inuence of the concentration of volatile
amines in wine and their sensorial effects. Lehtonen et al. (1992)
described how the volatile amines, at the pH of wine, are odor-
less, but once in contact with the mouth they become par-
tially liberated and their undesirable odor comes out. Palamand
et al. (1969) studied the effect of these amines on beer aroma
and they found that the threshold perception for ethylamine,
methylamine, and dimethylamine was at 2 mg/L, 40 g/L and
50 g/L, respectively. These authors along with Slaughter and
Uvgart (1971) found that important concentrations of amines
are associated with a decrease in aroma intensity and with the
appearance of a vaguely harsh or unpleasant taste in beer. They
are the only researchers who have attempted to assess the ef-
fect of amines on beer aroma while none have been made to
determine the role played by amines in wine avor. However,
it is important to bear in mind that it generally takes a greater
quantity of a compound to cause sensory effects in wine than in
beer because of the greater levels of the alcohol and the avor
components in the rst product (Ough and Daudt, 1981).
The majority volatile amines in both white and red wines
are ethylamine, dimethylamine, isopropylamine, and pyrroli-
dine. Although there are few studies on the content of these
amines in wine Ough and Daudt, (1981) Torrea and Ancn
(2002), Jim enez et al. (2003)
,
and Gonz alez-Marco and Ancn-
Azpilicueta (2006) found that dimethylamine was the only
volatile amine in wine which exceeded the limits established
by Palamand et al. (1969) affecting beer aroma.
CONCLUSIONS
A wide variability in amine content exists in wine, although
it can be generally stated that red wine shows a higher con-
centration of these substances than ros e or white wine. In gen-
eral, putrescine is the most abundant amine in most wines. Nu-
merous factors can inuence the formation of amines, among
them the maceration of must with the solid parts of the grape,
higher fermentation temperatures, not-very-acid pH values, a
high biomass of yeasts, and lactic acid bacteria. The biogenic
amines are mainly formed during malolactic fermentation, al-
though yeasts also synthesize them during alcoholic fermenta-
tion. Formation of these substances during alcoholic fermen-
tation depends, among other things, on the type of yeast that
predominates in the fermentation. Although it would seem that,
the higher the content of nitrogenous compounds in must, the
higher the content of biogenic amines, no direct correlation has
been found between the formation of biogenic amines by the
yeasts and the consumption of their precursor amino acids by
these microorganisms. Amines also evolve during wine aging in
such a way that histamine and tyramine are produced at the be-
ginning of the aging process, although they do not accumulate in
wine, due to their degradation. The concentration of cadaverine
increase slightly at the rst stage of aging and, like putrescine,
does not degrade at all. In order to better establish the permitted
levels of amines in wine, it would be necessary to know more
about their toxic effect as well as the inuence they have on
wine aroma. It is also necessary to do further studies to learn
more about the factors that determine the formation of these
substances in wine.
In summary, there are some practices that might permit wine-
makers to reduce amine accumulation. Among these, the most
important are healthy grape, less excessive nitrogenous fertiliza-
tion, yeast and, especially, lactic acid bacteria selected with low
aminogenic capacity, and also a maceration process as short as
possible. Given that, at present, the concentration of amines,
which produce toxic effects among the different population
groups, is not known or indeed, whether there are other wine
compounds which release endogenous histamine, it is very dif-
cult at the moment to recommend concrete limits for these sub-
stances. In any case, it might be proper to indicate the histamine
content on the bottle labels as this is the indicator amine for the
presence of other amines and an indicator of the hygienic-health
conditions in the elaboration of the product.
ACKNOWLEDGEMENT
This work was supported by the Ministerio de Ciencia y Tec-
nologa through the project AGL 200602414.
REFERENCES
Abe, K., Ohnishi, F., Yagi, K., Nakajima, T., Higuchi, T., Sano, M., Machida, M.,
Sarder, R. I., and Maloney, P. C. (2002). Plasmid-encoded as operon confers
a proton motive metabolic cycle catalyzed by an aspartate-alanine exchange
reaction. J. Bacteriol., 184:29062913.
Aerny, J. (1985). Orig` ene de lhistamine dans les vins. Connaissances actuales.
Bull. O.I.V., 656657:10161019.
Aerny, J. (1990). Pr esence dhistamine et dautres amines biog` enes dans les
vins. Off. Int. Vigne Vin, 656657:10171020.
Allison, C., and McFarlane, G. T. (1989). Inuence of pH, nutrient availability,
and growth rate on amine production by Bacteroides fragilis and Clostridium
perfringens. Appl. Environ. Microbiol., 55:28942898.
Ancn, C., Torrea, D., Fraile, P., and Garde, T. (2004). Amino acids and volatiles
compounds in the fermentation of inoculated musts: biogenic amines in the
wines. In: Shahidi, F., and Weerasinghe, D. K. Eds. Nutraceutical Beverages.
D
o
w
n
l
o
a
d
e
d

B
y
:

[
A
l
e
r
t
a

-

C
h
i
l
e

2
0
0
5
/
2
0
0
6

C
o
n
s
o
r
t
i
u
m
]

A
t
:

2
3
:
5
5

7

M
a
y

2
0
0
8

Chemical, Nutrition and Health effects. Washington: ACS Symposium series
871. 302313.
Anli, R. E., Vural, N., Yilmaz, S., and Vural, Y. H. (2004). The determination
of biogenic amines in Turkish red wines. J. Food Comp. Anal., 17:5362.
Arena, M. E., and Manca de Nadra, M. C. (2001). Biogenic amine production
by Lactobacillus. J. Appl. Microbiol., 90:158162.
Askar, A., and Terptow, H. (1986). Biogene amine in Lebensmitteln. Vorkorn-
men, Bedeutung und Bestimmung. Stuttgart, Germany: Eugen Ulmer GmbH
and Co.
Ayestar an, B. M., Ancn, M. C., Garca, A. M., Gonz alez, A., and Garrido, J. J.
(1995). Inuence of prefermentation clarication on nitrogenous contents of
musts and wines. J. Agric. Food Chem., 43:476482.
Bard ocz, S. (1989). Polyamines in tissue regeneration. In: Barhrach, U., and
Heimer, Y. M. Eds. Physiology of Polyamines. Vol I. CRC Press, Boca Rat on,
FL, USA, 96106.
Bard ocz, S., Grant, G., Brow, D. S., Ralph, A., and Pusztai, A. (1995).
Polyamines in food-implications for growth and health. J. Nutr. Biochem.,
4:6671.
Bauza, T., Blaise, A., Teissedre, P. L., Mestres, J. P., Daumas, F., and Cabanis,
J. C. (1995).

Evolution des teneurs en amines biog` enes des mo uts et des vins
au cours de la vinication. Sci. Aliments., 15:559570.
Bertrand, A., Ingargiola, M. C., and Delas, J. (1991). Effects of nitrogen fertil-
ization and grafting on the composition of must and wine from merlot grapes,
particularly on the presence of ethyl carbamate. Internat. Symp. Nitrogen in
Grapes and Wine, 215220.
Bjedanes, L. F., Schutz, D. E., and Morris, M. M. (1978). On the aetiology
of scromboid poisoning: cadaverine potentiation of histamine toxicity in the
guinea pig. Food Cosmet. Toxicol., 167:157159.
Blackwell, B. (1963). Hypertensive crises due to monoamine oxidase inhibitors.
Lancet, 2:849851.
Bouchereau, A., Aziz, A., Larher, F., and Martin-Tanguy, J. (1999). Polyamines
and environmental challenges: recent development. Plant Sci., 140:103125.
Boulton, R. B., Singleton, V. L., Bisson, L. F., and Kunkee, R. E. (1996). The
ning and clarication of wines. In: Boulton, R. B., Singleton, V. L., Bisson,
L. F., and Kunkee, R. E. Eds. Principles and Practices of Winemaking. New
York: Chapman & Hall, 279319.
Bover-Cid, S., and Holzapfel, W. H. (1999). Improved screening procedure for
biogenic amine production by lactic acid bacteria. Int. J. Food Microbiol.,
53:3341.
Bover-Cid, S., Izquierdo-Pulido, M., Marin e-Font, A., and Vidal-Carou, M. C.
(2006). Biogenic mono-, di- and polyamine contents in Spanish wines and
inuence of a limited irrigation. Food Chem., 96:4347.
Broquedis, M., Dumery, B., and Boucard, J. (1989). Miss en evidence de
polyamines (putrescine, cadaverine, nor-spermidine, spermidine et spermine)
dans les feuilles et les grappes de Vitis vinifera L. Conn. Vigne Vin, 23:1
6.
Busto, O., Guasch, J., and Borrull, F. (1995). Improvement of solid-phase extrac-
tion applied to the determination of biogenic amines in wines. J. Chromatogr.,
718:307317.
Buteau, C., and Duitschaever, C. L. (1984). High-performance liquid chromato-
graphic detectionandquantitationof amines inmust andwine. J. Chromatogr.,
284:201210.
Buteau, C., Duitschaever, C. L., and Ashton, G. C. (1984). High performance
liquidchromatographic detectionandquantitationof amines inmust andwine.
J. Chromatogr., 284:201210.
Cantagrel, R., Symonds, P., and Carles, J. (1982). Composition en acides amin es
du mo ut en fonction du c epage et de la technologie et son inuence sur la
qualit e du vin. Sci. Aliments, 2:109142.
Cardona-G alvez, M., and Gonz alez-Domnguez, A. (2005). Intoxicaci on his-
tamnica o escombroidosis en pescados. Alimentaria, 365:6873.
Carnevillier, V., Schlich, P., Guerreau, J., Charpentier, C., and Feuillat, M.
(1999). Characterization of the production regions of Chardonnay wines by
analysis of free amino acids. Vitis, 38:3742.
Caruso, M., Fiore, C., Contursi, M., Salzano, G., Paparella, A., and Romano,
P. (2002). Formation of biogenic amines as criteria for the selection of wine
yeasts. World J. Microbiol. Biotechnol., 18:159163.
Choudhury, N., Hansen, W., Engesser, D., Hammes, H. P., and Holzapfel, W.
H. (1990). Formation of histamine and tyramine by lactic acid bacteria in
decarboxylase assay medium. Lett. Appl. Microbiol., 11:278281.
Constantini, A., Cersosimo, M., del Prete, V., and Garca-Moruno, E. (2006).
Production of biogenic amines by lactic acid bacteria: screening by PCR,
thin-layer chromatography, and High-Performance Liquid Chromatography
of strains isolated from wine and must. J. Food Prot., 69:391396.
Coton, E., Rollan, G. C., and Lonvaud-Funel, A. (1998). Histidine decarboxy-
lase of Leuconostoc oenos 9204: purication, kinetic properties, cloning and
nucleotide sequence of the hdc gene. J. Appl. Microbiol., 84:143151.
Coton, E., Rollan, G., Bertrand, A., and Lonvaud-Funel, A. (1998). Histamine-
producing lactic acid bacteria in wines: early detection, frequency, and distri-
bution. Am. J. Enol. Vitic., 49:199204.
Coton, E., Torlois, S., Bertrand, A., and Lonvaud-Funel, A. (1999). Biogenic
amines and wine lactic acid bacteria. Bull. O.I.V., 72:2234.
Delni, C. (1989). Ability of wine malolactic bacteria to produce histamine. Sci.
Aliments, 9:413416.
Dicks, L. M., Dellaglio, F., and Collins, M. G. (1995). Proposal to reclassify
Leuconostoc oenos as Oenococcus oeni gen. nov., comb. nov. Int. J. Syst.
Bacteriol., 45:395397.
Enes-Dapkevicius, M. L. N., Nout, M. J. R., Rombouts, F. M., Houben, J. H.,
and Wymenga, W. (2000). Biogenic amine formation and degradation by
potential sh silage starter microorganisms. Int. J. Food Microbiol., 57:107
114.
Etievant, P., Schlich, P., Bouvier, J. C., Symonds, P., and Bertrand, A. (1988). Va-
rietal and geographic classication of French red wines in terms of elements,
amino acids and aromatic alcohols. J. Sci. Food Agricult., 45:2541.
Faras, M. E., Manca de Nadra, M. C., Rollan, G. C., and Strasser de Saad, A.
M. (1993). Histidine decarboxylase activity in lactic acid bacteria from wine.
J. Int. Sci. Vigne Vin, 27:191199.
Fern andes, J. O., and Ferreira, M. A. (2000). Combined ion-pair extraction and
gas chromatography-mass spectrometry for the simultaneous determination
of diamines, polyamines and aromatic amines in Port wine and grape juice.
J. Chromatogr. A, 886:183195.
Feuillat, M. (1974). Contribution ` a l etude des compos es azot es du mo ut de
raisin et du vin, Th` ese Univ. Dijon, France.
Flanzy, C., and Poux, C. (1965). Note sur la teneur en acides amin es du mo ut
de raisin et du vin en fonction des conditions de lann ee (maturation et fer-
mentation). Ann. Technol. Agric., 14:8791.
Forsythe, W. I., and Redmond, A. (1974). Two controlled trials of tyramine in
children with migraine. Develop. Med. Child Neurol., 16:794799.
Gafner, J. (2003). Biological stability of wine and biogenic amines. Proceedings
of the 32nd Annual New York Wine Industry Workshop, Geneva: New York
State Agricultural Experiment Station. Dept. of FoodScience andTechnology,
7480.
Gale, E. F. (1946). The bacterial amino acid decarboxylases. Adv. Enzym., 6:1
32.
Gardini, F., Zaccarelli, A., Belletti, N., Faustini, F., Cavazza, A., Martuscelli,
M., Mastracola, D., and Suzzi, G. (2005). Factors inuencing biogenic amine
production by a strain of Oenococcus oeni in a model system. Food Control,
16:609616.
Gerbaux, V., and Monamy, C. (2000). Biogenic amines in Burgundy wines.
Contents and origin in wines. Rev. Fr. Oenol., 183:2528.
Gerbaux, V., Villa, A., Monamy, C., and Bertrand, A. (1997). Use of lysoz-
ime to inhibit malolactic fermentation and to stabilize wine after malolactic
fermentation. Am. J. Enol. Vitic., 48:4954.
Gloria, M. B. A., Watson, B. T., Simon-Sarkardi, L., and Daeschel, M. A. (1998).
A survey of biogenic amines in Oregon Pinot noir and Cabernet sauvignon
wines. Am. J. Enol. Vitic., 49:279282.
Gl oria, M. B. A., and Izquierdo-Pulido, M. (1999). Levels and signicance of
biogenic amines in Brazilian beers. J. Food Comp. Anal., 12:129136.
Gl oria, M. B. A., Barbour, J. F., and Scanlan, R. A. (1997). N-
Nitrosodimehtylamine in Brazilian, U.S. domestic and U.S. imported beers.
J. Agric. Food Chem., 45:814816.
Gonz alez-Marco, A., and Ancn-Azpilicueta, C. (2006). Amine concentrations
in wine stored in bottles at different temperatures. Food Chem., 99:680685.
D
o
w
n
l
o
a
d
e
d

B
y
:

[
A
l
e
r
t
a

-

C
h
i
l
e

2
0
0
5
/
2
0
0
6

C
o
n
s
o
r
t
i
u
m
]

A
t
:

2
3
:
5
5

7

M
a
y

2
0
0
8

Gonz alez-Marco, A., Jim enez-Moreno, N., and Ancn-Azpilicueta, C. (2006).
Inuence of addition of yeast autolysate on the formation of amines in wine.
J. Sci. Food Agric., 86:22212227.
Guerrini, S., Mangani, S., Granchi, L., and Vincenzini, M. (2002). Biogenic
amine production by Oenococcus oeni. Curr. Microbiol., 44:374378.
Guitart, A., Hernandez-Orte, P., and Cacho, J. (1997). Effects of maceration on
the amino acid content of Chardonnay musts and wines. Vitis, 36:4347.
Haj os, G., Sass-Kiss, A., Szerdahelyi, E., and Bard ocz, S. (2000). Changes in
biogenic amine content of Tokaj grapes, wines and Asz u-wines. J. Food Sci.,
65:11421144.
Hayashi, M. (1954). Investigations on food poisoning caused by ordinary pu-
trefaction. IV. Synergism between histamine and several biogenic amines. J.
Pharm. Soc. Jpn., 74:11481151.
Herbert, P., Cabrita, M. J., Ratola, N., Laureano, O., and Alves, A. (2005).
Free amino acids and biogenic amines in wines and musts from the Alen-
tejo region. Evolution of amines during alcoholic fermentation and re-
lationship with variety, sub-region and vintage. J. Food Eng., 66:315
322.
Huang, Z., and Ough, C. S. (1989). Effect of vineyard locations, varieties and
rootstocks on the juice amino acid composition of several cultivars. Am. J.
Enol. Vitic., 40:135139.
Huang, Z., and Ough, C. S. (1991). Amino acid proles of commercial grape
juices and wines. Am. J. Enol. Vitic., 42:261267.
Hui, J. Y., and Taylor, S. L. (1985). Inhibition in vivo histamine metabolism
in rats by foodborne and pharmacologic inhibitors of diamine oxidases, N-
methyl transferase, and monoamine oxidase. Food Add. Contam., 8:531542.
I nigo, B., and Bravo, F. (1980). Histaminog enesis en vinos. I. Estudio de vinos
de diversas regiones espa nolas. Aliment., 117:5763.
Jarisch, R., and Wantke, F. (1996). Wine and headache. Int. Arch. Allergy Im-
munol., 110:712.
Jim enez-Moreno, N., and Ancn-Azpilicueta, C. (2004). Inuence of wine tur-
bidity on the accumulation of biogenic amines during aging. J. Sci. Food
Agric., 84:15711576.
Jim enez-Moreno, N., Torrea-Go ni, D., and Ancn-Azpilicueta, C. (2003).
Changes in amine concentrations during aging of red wine in oak barrels.
J. Agric. Food Chem., 51:57325737.
Juh` asz, O., and T orley, D. (1985). Effect of free amino acids of the grape on the
development of organoleptic properties of wine. Acta Aliment., 14:101112.
Kanny, G., Gerbaux, V., Olszewski, A., Fr emont, S., Empereur, F., Nabet, F.,
Cabanis, J. C., and Moneret-Vautrin, D. A. (2001). No correlation between
wine intolerance and histamine content of wine. J. Allergy Clin. Immunol.,
107:375378.
Kiss, J., and Sass-Kiss, A. (2005). Protection of originality of Tokaji Asz u:
amines and organic acids in botrytized wines by high-performance liquid
chromatography. J. Agric. Food Chem., 53:1004210050.
Kliewer, W. H. (1970). Free amino acids and other nitrogenous substances in
wine grapes varieties. J. Food Sci., 35:1721.
Konnings, W. N., Lolkema, J. S., Bolhuis, H., van Veen, H. W., Poolman, B.,
and Driessen, A. J. M. (1997). The role of transport processes in survival of
lactic acid bacteria. Antonie van Leeuwenhoek, 71:117128.
Kruger, L., Pickerell, A. T. W., and Axcell, B. (1992). The sensitivity of dif-
ferent brewing yeast strain to carbon dioxide inhibition: Fermentation and
production of avour-active volatile compounds. J. Inst. Brew., 98:133138.
Landete, J. M., Ferrer, S., and Pardo, I. (2005). Which lactic acid bacteria are
responsible for histamine production in wine? J. Appl. Microbiol., 99:580
586.
Landete, J. M., Ferrer, S., Polo, L., and Pardo, I. (2005). Biogenic amines in
wines from three Spanish regions. J. Agric. Food Chem., 53:11191124.
Lehtonen, P., Saarinen, M., Vesanto, M., and Riekkola, M. L. (1992). Determina-
tion of wine amines by HPLCusing automated precolumn derivatisation with
o-phtahaldehyde and uorescence detection. Z. Lebensm. Unters. Forsch.,
194:434437.
Leit ao, M. C., Marques, A. P., andSanRomao, M. V. (2005). Asurveyof biogenic
amines in commercial Portuguese wines. Food Control, 16:199204.
Leit ao, M. C.; Teixeira, H. C., Barreto Crespo, M. T., and San Rom ao, M. V.
(2000). Biogenic amines occurrence in wine. Amino acid decarboxylase and
proteolytic activities expression by Oenococcus oeni. J. Agric. Food Chem.,
48:27802784.
Lehtonen, P. (1996). Determination of amines and amino acids in wine. Areview.
Am. J. Enol. Vitic., 47:127133.
Lejonic, J. L., Gusmini, D., and Brochard, P. (1979). Isoniazid and reaction to
cheese. Ann. Int. Med., 91:793.
Leuschner, R. G., Heidel, M., and Hammes, W. P. (1998). Histamine and tyra-
mine degradation by food fermenting microorganisms. Int. J. Food Microbiol.,
39:110.
Liu, S. Q., Pritchard, G. G., Hardman, M. J., and Pilone, G. J. (1996). Arginine
catabolismin wine lactic acid bacteria: is it via the arginine deiminase pathway
or the arginase-urease pathway? J. Appl. Bacteriol., 81:486492.
Lonvaud-Funel, A. (2001). Biogenic amines in wines: role of lactic acid bacteria.
FEMS Microbiol. Lett., 199:913.
Lonvaud-Funel, A., and Joyeux, A. (1994). Histamine production by wine lactic
acid bacteria. Isolation of a histamine-producing strain of Leuconostoc oenos.
J. Appl. Bacteriol., 77:401407.
Lonvaud-Funel, A., Joyeux, A., and Ledoux, O. (1991). Specic enumeration of
lactic acid bacteria in fermenting grape must and wine by colony hybridization
with non-isotopic DNA probes. J. Appl. Bacteriol., 71:501508.
Lucas, P., and Lonvaud-Funel, A. (2002). Purication and partial gene sequence
of the tyrosine decarboxylase of Lactobacillus brevis IOEB 9809. FEMS
Microbiol. Lett., 211:8589.
Lucas, P., Landete, J., Coton, M., Coton, E., and Lonvaud-Funel, A. (2003). The
tyrosine decarboxylase operon of Lactobacillus brevis IOEB 9809: charac-
terization and conservation in tyramine-producing bacteria. FEMS Microbiol.
Lett., 229:6571.
Maduagwu, E. N., and Uhegbu, F. O. (1986). N-Nitrosamines and Nigerian
habitual drinks, and cancer. Carcinogenesis, 7:149151.
Maga, J. A. (1978). Amines in foods. Crit. Rev. Food Sci. Nutri., 12:373403.
Mangani, S., Guerrini, S., Granchi, L., and Vincenzini, M. (2005). Putrescine
accumulation in wine: role of Oenococcus oeni. Curr. Microbiol., 51:610.
Marcobal, A., de las Rivas, B., Moreno-Arribas, M. V., and Mu noz, R. (2004).
Identication of the ornithine decarboxylase gene in the putrescine-producer
Oenococcus oeni BIFI-83. FEMS Microbiol. Lett., 239:213220.
Marcobal, A., Martn-
Alvarez, P. J., Polo, M. C., Mu noz, R., and Moreno-

Arribas, M. V. (2006). Formation of biogenic amines throughout the industrial
manufacture of red wine. J. Food Prot., 69:397404.
Marcobal, A., Polo, M. C., Martin-Alvarez, P. J., and Moreno-Arribas, M. V.
(2005). Biogenic amine content of red Spanish wines: comparison of a direct
ELISA and an HPLC mehtod for the determination of histamine in wines.
Food Res. Int., 38:387394.
Marin e-Font, A. (1978). Alimentos y medicamentos: Interacciones (3a parte).
Circ. Farm., 258:4345.
Martn-
Alvarez, P. J., Marcobal, A., Polo. C., and Moreno-Arribas, M. V. (2006).

Inuence of technological practices on biogenic amine contents in red wines.
Eur. Food Res. Technol., 222:420424.
Millery, A., Duteurtre, B., Boudaille, J. P., and Maujean, A. (1986).
Diff erenciation des trois c epages champenois ` a partir de lanalyse des acides
amin es libres des mo uts des r ecoltes 1983 et 1984. Rev. Fr. Oenol., 103:32
50.
Molenaar, D., Bosscher, J. S., ten Brink, B., Driessen, A. J. M., and Konings, W.
N. (1993). Generation of a proton motive force by histidine decarboxylation
and electrogenic histidine/histamine antiport in Lactobacillus buchneri. J.
Bacteriol., 175:28642870.
Monteiro, F., and Bisson, L. F. (1991). Amino acid utilization and urea formation
during vinication fermentations. Am. J. Enol. Vitic., 42:199208.
Moreno-Arribas, M. V., Polo, M. C., Jorganes, F., and Mu noz, R. (2003). Screen-
ing of biogenic amine production by lactic acid bacteria isolated from grape
must and wine. Int. J. Food Microbiol., 84:117123.
Moreno-Arribas, V., and Lonvaud-Funel, A. (2001). Purication and character-
ization of tyrosine decarboxylase of Lactobacillus brevis IOEB 9809 isolated
from wine. FEMS Microbiol. Lett., 195:103107.
Moreno-Arribas, V., Torlois, S., Joyeux, A., Bertrand, A., and Lonvaud-Funel,
A. (2000). Isolation, properties and behaviour of tyramine-producing lactic
acid bacteria from wine. J. Appl. Microbiol., 88:584593.
D
o
w
n
l
o
a
d
e
d

B
y
:

[
A
l
e
r
t
a

-

C
h
i
l
e

2
0
0
5
/
2
0
0
6

C
o
n
s
o
r
t
i
u
m
]

A
t
:

2
3
:
5
5

7

M
a
y

2
0
0
8

Moret, S., Smela, D., Populin, T., and Conte, L. S. (2005). A survey of biogenic
amine content of fresh and preserved vegetables. Food Chem., 89:355361.
Novella-Rodriguez, S., Veciana-Nogu es, M. T., and Vidal-Carou, M. C.
(2000). Biogenic amines and polyamines in miles and cheeses by iron
high performance liquid chromatography. J. Agric. Food Chem., 48:5117
5123.
Ooghie, W., Kastelijn, H., De Waele, A. (1981). D etermination de lorigine
dun vin rouge ` a laide du spectre des acides amin es. Ann. Fals. Exp. Chim.,
789:381408.
Ough, C. S. (1971). Measurement of histamine in California wines. J. Agric.
Food Chem., 19:241244.
Ough, C. S., and Crowell, E. A. (1980). Nitrate determination in California musts
and wines. Am. J. Enol. Vitic., 31:344:346.
Ough, C. S., and Daudt, C. E. (1981). Quantitative determination of volatile
amines in grapes and wines. I. Effect of fermentation and storage temperature
on amine concentrations. Am. J. Enol. Vitic., 32:185188.
Ough, C. S., Crowell, E. A., Kunkee, R. E., Vilas, M. R., and Lagier, S. (1987).
A study of histamine production by various wine bacteria in model solutions
and in wine. J. Food Proc. Pres., 12:6370.
Ough, C. S., Daudt, C. E., and Crowell, E. A. (1981). Identication of new
volatile amines in grapes and wines. J. Agric. Food Chem., 29:938941.
Palamand, S. R., Hardwick, W. A., and Markl, K. S. (1969). Volatile amines in
beer andtheir inuence onbeer avour.Proceedings of the AmericanSociety of
Brewing Chemists. Baltimore, MD: American Society of Brewing Chemists.
Parrot, J., and Nicot, G. (1966). Pharmacology of histamine. In: Roche e Silva,
M., Ed. Handbuch der Experimentellen Pharmakologie. Vol XVIII, NewYork:
Springer-Verlag, 148.
Pessione, E., Mazzoli, R., Giuffrida, M. G., Lamberti, C., Garcia-Moruno, E.,
Barello, C., Conti, A., and Giunta, C. (2005). A proteomic approach to study-
ing biogenic amine producing lactic acid bacteria. Proteomics, 5:687698.
Petersen, J., Drasche, A., Raithel, M., and Schwelberger, H. G. (2003). Analysis
of genetic polymorphisms of enzymes involved in histamine metabolism.
Inamm. Res., 52:S6970.
Poux, C. (1968). Compos es azot es dans les vins de goutte vins de presse et vins
de lies. Ann. Technol. Agric., 17:315332.
Presa-Owens, C., Lamuela-Raventos, R., Buxaderas, S., and Torre-Boronat, C.
(1995). Characterization of Macabeo, Xarel.lo and Parrellada white wines
from the Penedes region. II. Am. J. Enol. Vitic., 46:529541.
Radler, F., and F ath, K. P. (1991). Histamine and others amines in wines. In:
Rantz, J. Ed. Proceedings of the international symposium on nitrogen in
grapes and wine. Davis, CA: American Society for Enology and Viticulture,
185195.
Rice, S. L., Eitenmiller, R. R., and Koehler, P. E. (1976). Biologically active
amines in food. A review. J. Milk Food Technol., 39:353358.
Rollan, G. C., Coton, E., and Lonvaud-Funel, A. (1995). Histidine decarboxylase
activity of Leuconostos oenos 9204. Food Microbiol., 12:455461.
Sandler, M., Youdin, M. B. H., and Hanington, E. (1974). A phenylethylamine
oxidizing defect in migraine. Nature, 250:335336.
Sass-Kiss, A., Szerdahelyi, E., and Haj os, G. (2000). Study of biologically active
amines in grapes and wines by HPLC. Chromatrogr. Suppl., 51: 316320.
Sauvage, F. X., Nicol, M. Z., Verries, C., Sarris, J., Pradal, M., and Robin, J. P.
(1993). Acides amin es libres et quelques activit es enzymatiques de mo uts de
raisins m urs. Analyses statistiques de leffect vari etal. Sci. Aliments, 13:443
462.
Scanlan, R. A., Barbour, J. F., Castegnaro, M., Clark, T., Fazio. T., Feit, M.,
Fiddler, W., Grifth, A., Herwig, W., and Koski, P. (1982). Nitrosamines in
malt and beer. J. Am. Soc. Brew. Chem., 9295.
Schelp, E., Worley, S., Monzingo, A. F., Ernst, S., and Robertus, J. D. (2001).
pH-induced structural changes regulate histidine decarboxylase activity in
Lactobacillus 30a. J. Mol. Biol., 306: 727732.
Schewelberger, H. G., Drasche, A., Petersen, J., and Raithel, M. (2003). Genetic
polymorphisms of histamine degrading enzymes: from small-scale screening
to high-throughput routine testing. Inamm. Res., 52:S7173.
Schiller, D., Kruse, D., Kneifel, H., Kr amer, R., and Burkovski, A. (2000).
Polyamine transport and role of potE in response to osmotic stress in Es-
cherichia coli. J. Bacteriol., 182:62476249.
Shalaby, A. R. (1996). Signicance of biogenic amines to food safety and human
health. Food Res. Int., 29:675690.
Silla-Santos, M. H. (1996). Biogenic amines: their importance in foods. Int. J.
Food Microbiol., 29:213231.
Slaughter, J. C., and Uvgard, A. R. (1971). Volatile amines of malt and beer. J.
Inst. Brew., 77:446450.
Slaughter, J. C., Flint, P. W. N., and Kular, K. S. (1987). The effect of CO
2
on
the absorption of amino acids from malt extract medium by Saccharomyces
cerevisiae. FEMS Microbiol. Lett. 40:239243.
Smith, C. K., and Durack, D. T. (1978). Isoniazid and reaction to cheese. Ann.
Int. Med., 88:520521.
Soueros, E. H., Bouloumpasi, E., Tsarchopoulos, C., and Biliaderis, C. G.
(2003). Primary amino acid proles of Greek white wines and their use in
classication according to variety, origin and vintage. Food Chem., 80:261
273.
Soueros, E., Barrios, M. L., and Bertrand, A. (1996). Correlations en-
tre les amines biog` enes et dautres constituants du vin adaptation dune
m ethode HPLC au dosage des acides amin es. Oenologie 95: 5e Sym-
posium International dOenologie/ coord par Aline Lonvaud-Funel. 665
669.
Soueros, E., Barrios, M. L., and Bertrand, A. (1998). Correlation between the
content of biogenic amines and other wine compounds. Am. J. Enol. Vitic.,
49:266278.
Spanjer, M. C., and Van Roode, B. A. S. W. (1991). Towards a regulatory limit
for biogenic amines in sh, cheese and sauerkraut. De Ware (n)-Chemicus,
21:139167.
Spayd, S. E., and Andersen-Baggie, J. (1996). Free amino acid composition of
grape juice from 12 Vitis vinifera cultivars in Washington. Am. J. Enol. Vitic.,
47:389402.
Spayd, S. E., Wample, R. L., Evans, R. G., Stevens, R. G., Seymour, B. J.,
and Nagel, C. W. (1994). Nitrogen fertilization of white Riesling grapes
in Washington. Must and wine composition. Am. J. Enol. Vitic., 45:34
42.
Straub, B. W., Kicherer, M., Schilcher, S. M., and Hammes, W. P. (1995). The
formation of biogenic amines by fermentation organisms. Z. Lebensm. Unters.
Forsch., 201:7982.
Sturgill, G., and Rather, P. N. (2004). Evidence that putrescine acts as an extra-
cellular signal required for swarming in Proteus mirabilis. Mol. Microbiol.,
51:437446.
Suzzi, G., and Gardini, F. (2003). Biogenic amines in dry fermented sausages:
a review. Int. J. Food Microbiol., 88:4154.
Tabor, C. W., and Tabor, H. (1985). Polyamines in microorganisms. Microbiol.
Rev., 49:8199.
Taylor, S. L. (1983). Histamine poisoning associated with sh, cheese and other
foods. FAO/WHO monograph CX/PH 83/11.
Taylor, S. L. (1985). Histamine poisoning associated with sh, cheese
and other food. Monograph VPH/FOS/85.1. World Health Organization,
Geneva.
ten Brink, B., Damink, C., Joosten, H. M. L. J., and Huis in t Veld, J. H. J.
(1990). Occurrence and formation of biologically active amines in foods. Int.
J. Food. Microbiol., 11:7384.
Tkachenko, A., Nesterova, L., and Pshenichnov, M. (2001). The role of the
natural polyamine putrescine indefense against oxidative stress inEscherichia
coli. Arch. Microbiol., 176:155157.
Torrea, D., and Ancn C. (2002). Content of biogenic amines in a Chardonnay
wine obtained through spontaneous and inoculated fermentations. J. Agric.
Food Chem., 50:48954899.
Torrea-Go ni, D., and Ancn-Azpilicueta, C. (2001). Inuence of yeast
strain on biogenic amines content in wines: relationship with the uti-
lization of amino acids during fermentation. Am. J. Enol. Vitic., 52:185
190.
Tusseau, D., Benoit, C., and Valade, M. (1989).

Etude de levolution des acides
amin es au cours de la maturation. Actual. Oenol., 2024.
Usseglio-Tomasset, L., and Bosia, P. D. (1990).

Evolution des acides
amin es et des oligopeptides du mo ut au vin. Bull. O.I.V., 63:21
46.
D
o
w
n
l
o
a
d
e
d

B
y
:

[
A
l
e
r
t
a

-

C
h
i
l
e

2
0
0
5
/
2
0
0
6

C
o
n
s
o
r
t
i
u
m
]

A
t
:

2
3
:
5
5

7

M
a
y

2
0
0
8

van de Guchte, M., Serror, P., Chervaux, C., Smokvina, T., Ehrlich, S. D.,
and Maguin, E. (2002). Stress responses in lactic acid bacteria. Antonie van
Leewenhoek., 82:187216.
Vazquez-Lasa, M. B., I niguez-Crespo. M., Gonz alez-Larraina, M., and
Gonz alez-Guerrero, A. (1998). Biogenic amines in Rioja wines. Am. J. Enol.
Vitic., 49:229.
Veciana-Nogu es, M. T., Marin e-Font, A., and Vidal-Carou, M. C. (1997). Bio-
genic amines in fresh and canned tuna. Effects of canning on biogenic amines
contents. J. Agric. Food Chem., 45:43244328.
Vidal-Carou, M. C., Ambatle-Espunyes, A., Ulla-Ulla, M. C., and Marin e-Font,
A. (1990). Histamine and tyramine in Spanish wines: their formation during
the winemaking process. Am. J. Enol. Vitic., 41:160167.
Vidal-Carou, M. C., and Marin e-Font, A. (1985). Histamina en vinos. Rev. Agro-
quim. Tecnol. Aliment., 25:5878.
Vidal-Carou, M. C., Codony-Salcedo, R., and Marin e-Font, A. (1990). His-
tamine and tyramine in Spanish wines relationships with total sulfur diox-
ide level, volatile acidity and malolactic fermentation intensity. Food Chem.,
35:217227.
Vidal-Carou, M. C., Codony-Salcedo, R., and Marin e-Font, A. (1991). Changes
in the concentration of histamine and tyramine during wine spoilage at various
temperatures. Am. J. Enol. Vitic., 42:145149.
Voigt, M. N., and Eitenmiller, R. R. (1978). Role of histidine and tyrosine
decarboxylases and mono- and diamine oxidases in amine build-up in cheese.
J. Food Prot., 41:182186.
Wantke, F., Gotz, M., and Jarisch R. (1993). Histamine-free diet: treatment of
choice for histamin-induced food intolerance and supporting treatment for
chronic headaches. Clin. Exp. Allergy, 12:982985.
Wantke, F., Hemmer, W., Haglmuller, T., Gotz, M., and Jarisch, R. (1996).
Histamine in wine. Bronchoconstriction after a double-blind placebo-
controlled red wine provocation test. Int. Arch. Allergy Immunol., 110:397
400.
Wantke, F., Manfred, G., and Jarisch, R. (1994). The red wine provocation
test: intolerance to histamine as a model for food intolerance. Allergy Proc.,
15:2732.
Zee, J. A., Simard, R. E., Heureux, L. L., and Tremblay, J. (1983). Biogenic
amines in wines. Am. J. Enol. Vitic., 34:69.

Current Knowledge About The Presence of Amines in Wine PDF

Uploaded by

Document Information

Original Description:

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Current Knowledge About The Presence of Amines in Wine PDF

Uploaded by

Copyright:

Available Formats

This article was downloaded by:[Alerta - Chile 2005/2006 Consortium]

On: 7 May 2008

Author to whom correspondence should be addressed Carmen Ancn-

(R) 1.141.58 (R) 0.811.00 (R) Torrea and Ancn

Alvarez et al. (2006)

Alvarez et al. (2006)

Etievant et al., 1988; Huang and Ough, 1991; Sauvage et al.,

C). However, they found

C after 78 days of wine aging, when it began

C. More recently, Landete et al. (2005) studied the

C) over 105 days. In

C than in the wine at room temperature. So,

Alvarez, P. J., Polo, M. C., Mu noz, R., and Moreno-

Alvarez, P. J., Marcobal, A., Polo. C., and Moreno-Arribas, M. V. (2006).

You might also like