Kerry J., Butler P. Smart Packaging Technologies for Fast Moving Consumer Goods
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Freshness Indicators for Food Packaging 115
published. Cameron and Talasila (1995) explored the potential of detecting the unaccept-
ability of packaged, respiring products by measuring ethanol in the package headspace with
the aid of alcohol oxidase, peroxidase and a chromogenic substrate. Smyth et al. (1999)
reported that enzyme-based test strips for ethanol could be used to measure ethanol in the
gas phase and were suitable for detecting low-oxygen injury in modified atmosphere (MA)
packages containing lightly processed vegetables.
In addition to ethanol, organic acids like lactic acid and acetic acid are the major com-
pounds with a role in glucose fermentation by lactic acid bacteria. Acetate concentrations
have been reported to increase during storage of fresh fish (Kakouri et al., 1997). In our
unpublished studies with modified-atmosphere packaged poultry meat we have also found
that the concentration of acetic acid in the tissue fluid and homogenised meat increased
as a function of storage time and temperature. The amount of l-lactic acid has generally
been reported to decrease during storage of fish and meat (Kakouri et al., 1997; Drosinos
and Nychas, 1997; Nychas et al. 1998) whereas the concentration of d-lactate has been
reported to increase during storage of meat. Hence d-lactate seems to be a more promising
freshness indicator (Shu et al., 1993).
Glucose as an initial substrate for many spoilage bacteria in air, vacuum packages and
modified atmosphere packages is consumed from the meat surface as the microbial growth
takes place (Dainty, 1996). It has been proposed by Kress-Rogers et al. (1993) that the
measurement of the glucose gradient measured with a knife-type freshness probe could be
utilised to predict the remaining shelf-life of meat.
7.3 Volatile Nitrogen Compounds
Volatile amines such as trimethylamine (TMA), ammonia (NH
3
) and dimethylamine
(DMA) comprise total volatilebasic nitrogen compounds (TVB-N), the levels of which have
been recognised as useful indicators of seafood spoilage under EU Directive 95/149/EEC.
The European Commission has specified that TVB-N levels be used if sensory methods
raise doubts about the freshness of seafood species. Many studies have concentrated on
fish freshness determination by means of detecting trimethylamine, dimethylamine and/or
ammonia using either headspace-gas chromatography (Elias and Krzymien, 1990), semi-
conductor gas sensors (Ohashi et al., 1991) or ammonia ion-selective electrodes (Pivarnik
et al., 2001). Trimethylamine, formed by microbial action in the fish muscle, is gener-
ally considered as a major metabolite responsible for the spoilage odours of seafood. A
drawback of using trimethylamine as a quality indicator for seafood is the variation in the
concentration of its precursor trimethylamine N-oxide according to the species and season
(Dainty, 1996; Rodr´ıguez et al., 1999).
Numerous freshness indicator concepts targeted to volatile amines have been presented.
A concept of an indicator compound provided on a substrate and reacting to volatile amines
with a colour change hence indicating freshness of packaged food has been patented by
Miller et al. (1999). This concept has been marketed by COX Recorders (USA) with trade
name FreshTag
r
. Naturally occurring betalain or flavonoid based molecules have been used
as pH-sensitive dyes for detecting amines from packaged foodstuff (Williams and Myers,
2005; Williams et al., 2006). They describe a colour changing indicator, the sensitivity of
which can be adjusted by tuning the original pH of the indicator. By pH tuning, the indicator
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116 Smart Packaging Technologies for Fast Moving Consumer Goods
Figure 7.1 freshQ
TM
indicator. (Reproduced with permission from Food Quality Sensor In-
ternational, Inc.).
can also be used to observe production of acidic compounds during microbial spoilage. The
concept by Williams et al. is currently being marketed as freshQ
TM
(Figure 7.1).
Khalil et al. (2003) have presented a device for ammonia or volatile amines detection that
is based on the colour change of pH-dyes on PTFE-carrier solid phase indicator film. Morris
et al. (2004) have described a device detecting the presence of bacteria in a perishable food
product based on a pH indicator, the colour change of which is caused by the presence of
the spoilage metabolite (e.g. ammonia, CO
2
). The invention of Wallach (2002, 2003) is
also based on pH-sensitive dyes being used for detecting volatile amines, but also carbon
dioxide or volatile carboxylic acids from food packages.
Loughran and Diamond (2000) propose a simple method for the determination of volatile
nitrogen compounds (NH
3
, DMA, TMA) with the aid of chromogenic dye calix[4]arene
impregnated on a paper disk. Byrne et al. (2002) determined headspace-TVB-N from fish
samples using pH indicator dye (cresol red) films as sensors. It was suggested that in
the future, this approach could be used for making an on-package sensor in individual
packages, using inexpensive colour measurement equipment, e.g. an LED and photodiode
array detector, or using a reference set of colours to reflect the critical TVB-N concentration
and spoilage state of the specific fish species.
Oberget al. (2006) describe a simple optical sensor for amine vapours. The sensor is based
on silica microspheres dyed with the pH indicator bromocresol green. Bromocresol green
is also used by Pacquit et al. (2006, 2007), who describe an on-package sensor responding
through visible colour change and interrogated with LED-based reflectance colorimeter.
7.4 Biogenic Amines
Biogenic amines, tyramine, histamine, tryptamine, phenylethylamine, serotonin, pu-
trescine, cadaverine, spermine and spermidine, are found in fresh food only in small
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Freshness Indicators for Food Packaging 117
concentrations. They could hence serve as useful indicators of quality deterioration, even if
they do not themself contribute to the sensory quality of the product. In addition to the qual-
ity indicative nature, biogenic amines can have pharmacological, physiological and toxic
effects. Due to the health risks, a tolerance level of 100 mg/kg of fish has been established
for histamine by FDA (Kaniou, 2001).
Biogenic amines are produced in the growth of decarboxylase-positive microorganisms
under conditions favourable to enzyme activity (Roig, 2002). Many Enterobacteriaceae,
Pseudomonas spp. and certain lactobacilli, enterococci and staphylococci are active in the
formation of biogenic amines. These amine-positive microorganisms may constitute part
of the normally associated population of the food product or may appear in the product by
contamination before, during or after processing.
For instance the accumulation of tyramine at bacterial numbers above 10
6
/g has been
reported in many studies of different types of stored meat, and tyramine has been proposed
as a quality indicator for beef, pork and poultry (Edwards et al., 1987; Schmitt and Schmidt-
Lorenz, 1992; Ordonez et al., 1991; Smith et al., 1993; Yano et al., 1995b).
The effect of storage temperature in various constant and variable temperature schemes
on the formation of biogenic amines of modified atmosphere (MA)-packed broiler chicken
cuts, as well as the applicability of biogenic amines as quality indicating metabolites of
MA-packaged broiler chicken cuts, has been studied in collaboration between the former
National Veterinary and Food Research Institute of Finland EELA (presently Finnish Food
Safety Authority, Evira) and VTT (Rokka et al., 2004). In this study broiler chicken cuts,
which were stored in modified atmosphere packages in constant and variable tempera-
tures, were analysed for their content of biogenic amines. It was found out that the storage
temperature significantly affected the formation rate of tyramine (Figure 7.2). The levels
0.0
50.0
100.0
150.0
200.0
250.0
08642
AMBC (log cfu/g)
Tyramine (mg/kg)
10
Figure 7.2 Correlation between tyramine and aerobic mesophilic bacterial counts during
the storage of broiler chicken cuts. (Reproduced from Rokka et al., Food Control 15,8,pp.
601–607. Copyright (2004) with permission from Elsevier).
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118 Smart Packaging Technologies for Fast Moving Consumer Goods
of tyramine had increased after 5 days of storage if the storage temperature was above
6
◦
C, which is the highest statutory storage temperature in Finland. The levels of putrescine
increased after 7 days and the levels of cadaverine increased after 9 days, respectively.
The formation of tyramine seemed to be highly consistent with the increase in the aero-
bic mesophilic viable count. Putrescine and cadaverine were not formed below 6
◦
C. In
these conditions without putrescine and cadaverine formation the growth of Enterobac-
teriaceae, proteolytic bacteria, hydrogen sulphide producing bacteria and clostridia was
also clearly retarded. Thus the three amines tyramine, cadaverine and putrescine seemed
to be promising indicators for both storage time and temperature as well as for the micro-
biological quality of MA packed broiler chicken cuts. In the future the results could be
exploited in the development of new methods for the quality control of packaged poultry
products.
According to our knowledge, there are no specific freshness indicator concepts for bio-
genic amines, but several types of enzymatic biosensors have been developed for the detec-
tion of biogenic amines from, for instance, poultry (Okuma et al., 2000), fish (Niculescu et
al., 2000; Fr´ebort et al., 2000) and beef (Yano et al., 1995b). An enzymatic determination
of the total amount of biogenic amines with transglutaminase was suggested by Punakivi
et al. (2006).
7.5 Carbon Dioxide
Carbon dioxide (CO
2
) is produced during microbial growth. Due to its bacteriostatic ef-
fects it is also typically added as protecting gas to modified atmosphere packages, together
with inert nitrogen (typically 20–80 %). Due to microbial growth the CO
2
concentration
can further increase during storage (Fu et al., 1992). However, it is difficult to indicate
the microbial growth by CO
2
in these modified atmosphere packages that already contain
a high concentration of CO
2
, but it is possible to use the increase in CO
2
concentra-
tion as a means of determining microbial contamination in other types of products. For
instance Mattila et al. (1990) found a correlation between CO
2
concentration and the
growth of microbes in aseptically packed soup, either in air or in a mixture of oxygen and
nitrogen.
Several freshness indicator concepts based on pH dyes, using CO
2
as the main target
metabolite have been proposed. The use of the pH dye bromothymol blue as an indicator
for the formation of CO
2
by microbial growth has been suggested (e.g. Holte, 1993; Mattila
et al., 1990). A combination of bromothymol blue and methyl red solution packaged in
gas permeable film was recently suggested by Morris (2006). In addition to the detection
of spoilage, pH-dyes reacting to the presence of CO
2
have also been used to construct
intelligent packaging concepts indicating the ripeness of traditional fermented vegetable
foods in Korea (kimchi) (Hong and Park, 2000). In addition to the most frequently used
pH dye, bromothymol blue, many other reagents, e.g. xylenol blue, bromocresol purple,
bromocresol green, cresol red, phenol red, methyl red and alizarin, among others, have
been proposed for the same purpose (Horan, 2000). Besides CO
2
, also other metabolites
like SO
2
,NH
4
, volatile amines and organic acids have been proposed as suitable tar-
get molecules for these pH-sensitive indicators (Mattila and Auvinen, 1990a, b; Horan,
2000).
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Freshness Indicators for Food Packaging 119
7.5.1 ATP Degradation Products
K-Value is defined as the ratio of the sum of hypoxanthine and inosine and the total concen-
tration of ATP-related compounds (Henehan et al., 1997). This value indicating the extent
of ATP-degradation correlates with the sensory quality of fish and also other types of meat
and has been used as a freshness indicating parameter (Watanabe et al., 1989; Yano et al.,
1995a). For fresh meat the value is low since the concentration of ATP-degradation products
is low as compared with the concentration of all ATP-related compounds. The correlation
between ATP-degradation products and fish quality has been extensively studied, e.g. by
Hattula (1997). K-value can also be replaced by K
i
-value, which excludes ATP, ADP and
AMP determination (
¨
Ozogul and
¨
Ozogul, 2000).
Package integrated freshness-indicating concepts reacting to ATP degradation products
have not been presented to our knowledge. However ATP degradation products indicating
the quality deterioration of fish can be analysed by enzymatic test strips manufactured by
Transia. ATP degradation products have also been frequently measured with biosensors.
For instance, Yano et al. (1995a) and Mulchandani et al. (1990) developed an enzyme
based electrochemical sensor for the quality control of beef. Recently, a non-destructive
colorimetric test for the evaluation of remaining shelf-life of japanese raw fish dish, sashimi
was presented by Watanabe et al. (2005). The idea is that a test solution containing hypox-
anthine, thiazole blue redox dye and xanthine oxidase is kept with a fish product and reacts
analogously with it to the storage time and conditions.
7.5.2 Sulfuric Compounds
Sulfuric compounds have a remarkable effect on the sensory quality of meat products
due to their typical odour and low odour threshold. Hydrogen sulfide (H
2
S) is produced
from cysteine and triggered by glucose limitation (Borch et al., 1996). H
2
S forms a
green pigment, sulfmyoglobin, when it is bound to myoglobin (Paine and Paine, 1992;
Egan et al., 1989).
H
2
S and other sulfur compounds have been found to be produced during the spoilage of
poultry by Pseudomonas, Alteromonas sp. and psycrotrophic anaerobic clostridia (Freeman
et al., 1976; Lea et al., 1969; Russell et al., 1997, Vieshweg et al., 1989; Arnaut-Rollier
et al., 1999; Kalinowski and Tompkin, 1999). According to Dainty (1996), production of
H
2
S can be used as an indication of Enterobacteriacae and hence also of hygienic problems
in aerobically stored meat. H
2
S production by Alteromonas putrefaciens, Enterobacter
liquefaciens and pseudomonas was discovered in high ultimate pH beef from stressed
animals (Gill and Newton,1979; Nicol et al., 1970). It has also been found out that in vacuum
packed meat H
2
S indicates the growth of particular strains of lactic acid bacteria (Egan et
al., 1989). Additionally, volatile sulfur compounds have been suggested as the main cause of
putrid spoilage aromas in fish (Olafsdottir and Fleurence, 1997). In our studies we report that
modified-atmosphere packaged broiler chicken cuts shows a clear effect of the storage time
and temperature on the accumulation of hydrogen sulfide and dimethyl sulfide (Rajam¨aki
et al., 2006) and on the sulfurous odour of the product (Smolander et al., 2004a) (Figure 7.3).
In our work aiming at the development of freshness indicators for poultry products, we
have utilized a reaction between hydrogen sulfide and myoglobin in a freshness indicator
for the quality control of modified-atmosphere-packed poultry meat (Ahvenainen et al.,
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120 Smart Packaging Technologies for Fast Moving Consumer Goods
Sulphuric nature of odour: R
2
= 0.85
Storage time, d
Storage temp, °C
0
2
4
6
8
10
8
6
4
2
0101214
2
10
3
4
5
6
7
8
9
Figure 7.3 The effect of storage time and temperature on the sulfurous nature of the odour in
the package head-space of modified-atmosphere packaged broiler chicken cuts. (Reproduced
from Smolander et al., Food Control, 15, 3, pp. 217–229. Copyright (2004) with permission
from Elsevier).
1997; Smolander et al., 2002). Freshness indication is based on the colour change of
myoglobin by hydrogen sulfide (H
2
S) and the indicators were tested in the quality control
of MA-packaged fresh, unmarinated broiler cuts. It was found that the colour change of
the myoglobin-based indicators corresponded with the deterioration of the product quality,
hence it could be concluded that the myoglobin-based indicators seem to be promising for
the quality control of packaged poultry products.
The capability of sulfur compounds to indicate the quality of packaged poultry meat
has been exploited in the recently launched ‘Freshness Guard’ by UPM Raflatac, one of
the world’s leading suppliers of paper-based and filmic pressure sensitive labelstock. The
indicator specifically designed for use with fresh poultry is based on a reaction between
hydrogen sulfide and nano-scale layer of silver (Smolander et al., 2004b). Originally the
colour of the thin silver layer is opaque light brown, but as silver sulfide is formed the
colour of the layer is converted to transparent (Figure 7.4). The label can be used to evaluate
product quality throughout the distribution chain and can be considered particularly bene-
ficial at seasons like Christmas and Easter that require the maintenance of large stocks of
poultry.
Another concept relying on the utilisation of silver layer in RF readable, package inte-
grated sensors has also been presented by Smolander et al. (2003). The idea of this concept
is to measure the change in conductivity of a silver layer taking place due to the reaction
between silver and hydrogen sulfide.
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Freshness Indicators for Food Packaging 121
Figure 7.4 Freshness Guard. (Reproduced with permission from UPM-Kymmene).
7.6 Other Quality Indicators for Microbial Spoilage and Contamination
In addition to the indicators reacting to the volatiles produced by normal spoilage of food
products as described above, other systems for the detection of microbial contamination in
the food product have also been presented.
A food freshness indicator for consumers’ own use is offered by It’sFresh! Inc. The
indicator is suitable for many types of meat-containing food products like salads as well
as cooked and deli meats (seafood, poultry, beef and pork). The idea of the concept is that
the consumer places the indicator inside a storage bag or container, which is then placed
in the refrigerator for 8 hours. If the colour of the indicator is changed from pink to yellow
the quality of the product is likely to be deteriorated (Figure 7.5).
Van Veen (2004) described a method for non-invasive detection of contamination by a
microorganism in a closed, sterile container, which is based on detecting an extracellular
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122 Smart Packaging Technologies for Fast Moving Consumer Goods
Figure 7.5 It’sFresh containers with indicators. (Used with permission from Packaging Mate-
rials and Technologies Ltd).
enzyme or its activity in the microorganism. A substrate is provided in either the contents of
the container or alternatively in a coating of the inner side of a package, and the conversion of
this substrate by the enzyme is detected either visually or by means of an optical measuring
device.
Under development for both commercial and military applications, is Toxin Guard
TM
by Toxin Alert, Inc. (Ontario, Canada), which is a polyethylene-based packaging film
that can detect the presence of specific pathogenic bacteria (Salmonella, Campylobacter,
Escherichia coli O157 and Listeria) with the aid of immobilized antibodies. As the analyte
(toxin, microorganism) is in contact with the material it will be bound first to a specific,
labelled antibody and then to a capturing antibody printed as a certain pattern (Bodenhamer,
2000). The method could also be applied to the detection of pesticide residues or proteins
resulting from genetic modifications.
Specific indicator material for the detection of Escherichia coli O157 enterotoxin
has been developed at Lawrence Berkeley National Laboratory (Kahn, 1996; Quan and
Stevens, 1998). This sensor material, which can be incorporated in the packaging mate-
rial, is composed of cross-polymerised polydiacetylene molecules and has a deep blue
colour. The molecules specifically binding the toxin are trapped in this polydiacetylene
matrix and as the toxin is bound to the film, the colour of the film changes from blue
to red.
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Freshness Indicators for Food Packaging 123
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